The MAL Family of Proteins: Normal Function, Expression in Cancer, and Potential Use as Cancer Biomarkers
Abstract
:Simple Summary
Abstract
1. Introduction
2. The MAL Protein Family
2.1. Members and Structure
2.2. Biochemical Features
3. MAL-Family Protein Function
3.1. The MAL-MAL2-MALL Branch
3.2. The PLLP-CMTM8 Branch
3.3. The MYADM-MYADML2 Branch
4. The MAL Gene Family
4.1. Chromosome Location, Exon/Intron Organization, and CpG Island Content
4.2. Tissue Expression
4.3. Association with Non-Cancerous Diseases
5. The MAL Gene Family in Human Cancer
5.1. Expression of MAL-Family Genes in Cancer
5.2. MAL-Family Gene Methylation in Cancer
5.3. Amplification, Deletion and Mutation of MAL-Family Genes in Cancer
5.4. MAL-Family Gene Regulation by Non-Coding RNA
5.5. Role of MAL-Family Proteins in Cancer
5.6. The MAL-Protein Family as Tumor Suppressors
5.7. MAL-Family Proteins as Potential Therapeutic Targets in Cancer
5.8. MAL-Family Genes as Prognostic Cancer Biomarkers: Analysis of Large-Scale Cancer Datasets
5.9. MAL-Family Genes as Prognostic Cancer Biomarkers: Analysis of the Literature
5.10. MAL-Family Expression as Biomarkers to Predict Response to Cancer Chemotherapy
5.11. MAL-Family Proteins and Antitumor Drug Development
5.12. Tools for MAL-Family Proteins as Cancer Biomarkers
Protein | Antibody | Source | Address | Validation 1–5 | Applications 6 | References |
---|---|---|---|---|---|---|
MAL | Mouse 6D9 mAb | MA Alonso | Centro de Biología Molecular, Madrid, Spain | Endog, Exog, +/−, KD/KO, Compet | WB, IHC, IP, FACS | [18,24,25,53,67,69,78,91,92,93,94,129,156,157,176,186,187,188,189,190,191] |
Unknown | Unknown | Unknown | Unknown | WB, IHC | [152] | |
Goat polycl MAL (H-70) | Santa Cruz Biotech | scbt.com, discontinued product | Unknown | WB, IF | ||
Rabbit polycl | Santa Cruz Biotech | scbt.com, discontinued product | Unknown | IHC | [74] | |
Mouse mAb MT3 | W Kasinrek | Chiang Mai University, Thailand | Expression cloning; KO | IF, FACS | [26] | |
MAL2 | Mouse 9D1 mAb | MA Alonso | Centro de Biología Molecular, Madrid, Spain | Endog, Exog, +/− KD/KO | WB, IHC, IF, IP | [12,29,30,31,52,146,158,191] |
Rabbit polycl ab217919 | Abcam | abcam.com, accessed on 24 February 2023 | Unknown | IHC | [111] | |
Rabbit polycl ab75347 | Abcam | abcam.com, accessed on 24 February 2023 | Exog, KD | WB, IHC, IF | [102,108,131,148] | |
Rabbit polycl bs-7175R | Bioss Antibodies | biossusa.com, accessed on 24 february 2023 | Exog, KD | IWB, IF | [147,149] | |
Rabbit polycl | JA Byrne | The Children’s Hospital, Westmead, Australia | Exog | WB, IF, IHC | [95,105,192] | |
Rabbit polycl sc-87994 | Santa Cruz Biotech | scbt.com, discontinued product | Unknown | IHC | [99] | |
Unknown | Unknown | Unknown | Unknown | WB, IHC | [155] | |
MALL | Mouse 2G8 mAb | MA Alonso | Centro de Biología Molecular, Madrid, Spain | Exog, KD/KO | WB, IHC, IF, IP | [38] |
Rabbit polycl | Abgent | Abgent.com, accessed on 24 February 2023. Product not found in the catalog | Unknown | IHC | [113] | |
PLLP | Rabbit polycl | J Millán | Centro de Biología Molecular, Madrid, Spain | Exog, KD/KO | WB, IHC, IF, IP | [41,42] |
Rabbit polycl | HW Müller | Heinrich-Heine Univ. Düsseldorf, Germany | Exog | WB, IHC | [15,193,194] | |
Rabbit polycl | VS Sapirtstein | Medical College of Pennsylvania, Philadelphia, PA | Exog | WB, IHC | [4,195,196,197,198,199] | |
CMTM8 | Rabbit polycl | Y Wang | Peking Univ. Health Science Center, Beijing, China | Exog, KD, Compet | WB, IHC | [116,118,153,200] |
Unknown | Unknown | Unknown | Unknown | WB, IHC, IP | [119] | |
Rabbit polycl 15039-1-AP | Proteintech | ptglab.com, accessed on 24 February 2023 | Unknown | IHC | [117,185] | |
MYADM | Mouse 2B12 mAb | MA Alonso | Centro de Biología Molecular, Madrid, Spain | Exog, KD/KO | WB, IP | [14,48] |
MYADML2 | Bs-19119R7 | Bioss | Biosusa.com, accessed on 24 February 2023. Product not found in the catalog | Endog | WB, IHC | [150] |
6. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Pérez, P.; Puertollano, R.; Alonso, M.A. Structural and Biochemical Similarities Reveal a Family of Proteins Related to the MAL Proteolipid, a Component of Detergent-Insoluble Membrane Microdomains. Biochem. Biophys. Res. Commun. 1997, 232, 618–621. [Google Scholar] [CrossRef]
- Magyar, J.P.; Ebensperger, C.; Schaeren-Wiemers, N.; Suter, U. Myelin and Lymphocyte Protein (MAL/MVP17/VIP17) and Plasmolipin Are Members of an Extended Gene Family. Gene 1997, 189, 269–275. [Google Scholar] [CrossRef]
- Sanchez-Pulido, L.; Martin-Belmonte, F.; Valencia, A.; Alonso, M.A. MARVEL: A Conserved Domain Involved in Membrane Apposition Events. Trends Biochem. Sci. 2002, 27, 599–601. [Google Scholar] [CrossRef] [PubMed]
- Fischer, I.; Durrie, R.; Sapirstein, V.S. Plasmolipin: The Other Myelin Proteolipid. A Review of Studies on Its Structure, Expression, and Function. Neurochem. Res. 1994, 19, 959–966. [Google Scholar] [CrossRef]
- Rancaño, C.; Rubio, T.; Correas, I.; Alonso, M.A. Genomic Structure and Subcellular Localization of MAL, a Human T-Cell-Specific Proteolipid Protein. J. Biol. Chem. 1994, 269, 8159–8164. [Google Scholar] [CrossRef] [PubMed]
- De Marco, M.C.; Kremer, L.; Albar, J.P.; Martínez-Menárguez, J.A.; Ballesta, J.; García-López, M.A.; Marazuela, M.; Puertollano, R.; Alonso, M.A. BENE, a Novel Raft-Associated Protein of the MAL Proteolipid Family, Interacts with Caveolin-1 in Human Endothelial-like ECV304 Cells. J. Biol. Chem. 2001, 276, 23009–23017. [Google Scholar] [CrossRef] [PubMed]
- Folch, J.; Lees, M. Proteolipides, a New Type of Tissue Lipoproteins; Their Isolation from Brain. J. Biol. Chem. 1951, 191, 807–817. [Google Scholar] [CrossRef] [PubMed]
- Greer, J.M.; Lees, M.B. Myelin Proteolipid Protein—The First 50 Years. Int. J. Biochem. Cell Biol. 2002, 34, 211–215. [Google Scholar] [CrossRef]
- Sapirstein, V.S.; Rounds, T.C. Circular Dichroism and Fluorescence Studies on a Cation Channel Forming Plasma Membrane Proteolipid. Biochemistry 1983, 22, 3330–3335. [Google Scholar] [CrossRef]
- Cockle, S.A.; Epand, R.M.; Moscarello, M.A. Intrinsic Fluorescence of a Hydrophobic Myelin Protein and Some Complexes with Phospholipids. Biochemistry 1978, 17, 630–637. [Google Scholar] [CrossRef]
- Cockle, S.A.; Epand, R.M.; Boggs, J.M.; Moscarello, M.A. Circular Dichroism Studies on Lipid-Protein Complexes of a Hydrophobic Myelin Protein. Biochemistry 1978, 17, 624–629. [Google Scholar] [CrossRef]
- De Marco, M.C.; Martín-Belmonte, F.; Kremer, L.; Albar, J.P.; Correas, I.; Vaerman, J.P.; Marazuela, M.; Byrne, J.A.; Alonso, M.A. MAL2, a Novel Raft Protein of the MAL Family, Is an Essential Component of the Machinery for Transcytosis in Hepatoma HepG2 Cells. J. Cell Biol. 2002, 159, 37–44. [Google Scholar] [CrossRef]
- Millan, J.; Alonso, M.A. MAL, a Novel Integral Membrane Protein of Human T Lymphocytes, Associates with Glycosylphosphatidylinositol-Anchored Proteins and Src-like Tyrosine Kinases. Eur. J. Immunol. 1998, 28, 3675–3684. [Google Scholar] [CrossRef]
- Aranda, J.F.; Reglero-Real, N.; Kremer, L.; Marcos-Ramiro, B.; Ruiz-Sáenz, A.; Calvo, M.; Enrich, C.; Correas, I.; Millán, J.; Alonso, M.A. MYADM Regulates Rac1 Targeting to Ordered Membranes Required for Cell Spreading and Migration. Mol. Biol. Cell 2011, 22, 1252–1262. [Google Scholar] [CrossRef]
- Hasse, B.; Bosse, F.; Müller, H.W. Proteins of Peripheral Myelin Are Associated with Glycosphingolipid/Cholesterol-Enriched Membranes: Myelin Proteins Are Associated with GEMs. J. Neurosci. Res. 2002, 69, 227–232. [Google Scholar] [CrossRef]
- Lingwood, D.; Simons, K. Lipid Rafts as a Membrane-Organizing Principle. Science 2010, 327, 46–50. [Google Scholar] [CrossRef]
- Yaffe, Y.; Hugger, I.; Yassaf, I.N.; Shepshelovitch, J.; Sklan, E.H.; Elkabetz, Y.; Yeheskel, A.; Pasmanik-Chor, M.; Benzing, C.; Macmillan, A.; et al. The Myelin Proteolipid Plasmolipin Forms Oligomers and Induces Liquid-Ordered Membranes in the Golgi Complex. J. Cell Sci. 2015, 128, 2293–2302. [Google Scholar] [CrossRef]
- Antón, O.M.; Andrés-Delgado, L.; Reglero-Real, N.; Batista, A.; Alonso, M.A. MAL Protein Controls Protein Sorting at the Supramolecular Activation Cluster of Human T Lymphocytes. J. Immunol. 2011, 186, 6345–6356. [Google Scholar] [CrossRef]
- Magal, L.G.; Yaffe, Y.; Shepshelovich, J.; Aranda, J.F.; de Marco, M.D.C.; Gaus, K.; Alonso, M.A.; Hirschberg, K. Clustering and Lateral Concentration of Raft Lipids by the MAL Protein. Mol. Biol. Cell 2009, 20, 3751–3762. [Google Scholar] [CrossRef]
- Gaus, K.; Gratton, E.; Kable, E.P.W.; Jones, A.S.; Gelissen, I.; Kritharides, L.; Jessup, W. Visualizing Lipid Structure and Raft Domains in Living Cells with Two-Photon Microscopy. Proc. Nat. Acad. Sci. USA 2003, 100, 15554–15559. [Google Scholar] [CrossRef]
- Rubio-Ramos, A.; Labat-de-Hoz, L.; Correas, I.; Alonso, M.A. The MAL Protein, an Integral Component of Specialized Membranes, in Normal Cells and Cancer. Cells 2021, 10, 1065. [Google Scholar] [CrossRef] [PubMed]
- Alonso, M.A.; Weissman, S.M. CDNA Cloning and Sequence of MAL, a Hydrophobic Protein Associated with Human T-Cell Differentiation. Proc. Natl. Acad. Sci. USA 1987, 84, 1997–2001. [Google Scholar] [CrossRef] [PubMed]
- Ramnarayanan, S.P.; Cheng, C.A.; Bastaki, M.; Tuma, P.L. Exogenous MAL Reroutes Selected Hepatic Apical Proteins into the Direct Pathway in WIF-B Cells. Mol. Biol. Cell 2007, 18, 2707–2715. [Google Scholar] [CrossRef]
- Antón, O.; Batista, A.; Millan, J.; Andres-Delgado, L.; Puertollano, R.; Correas, I.; Alonso, M.A. An Essential Role for the MAL Protein in Targeting Lck to the Plasma Membrane of Human T Lymphocytes. J. Exp. Med. 2008, 205, 3201–3213. [Google Scholar] [CrossRef] [PubMed]
- Soares, H.; Henriques, R.; Sachse, M.; Ventimiglia, L.; Alonso, M.A.; Zimmer, C.; Thoulouze, M.-I.; Alcover, A. Regulated Vesicle Fusion Generates Signaling Nanoterritories That Control T Cell Activation at the Immunological Synapse. J. Exp. Med. 2013, 210, 2415–2433. [Google Scholar] [CrossRef]
- Leitner, J.; Mahasongkram, K.; Schatzlmaier, P.; Pfisterer, K.; Leksa, V.; Pata, S.; Kasinrerk, W.; Stockinger, H.; Steinberger, P. Differentiation and Activation of Human CD4 T Cells Is Associated with a Gradual Loss of Myelin and Lymphocyte Protein. Eur. J. Immunol. 2021, 51, 848–863. [Google Scholar] [CrossRef]
- Wilson, S.H.D.; Bailey, A.M.; Nourse, C.R.; Mattei, M.-G.; Byrne, J.A. Identification of MAL2, a Novel Member of the MAL Proteolipid Family, Though Interactions with TPD52-like Proteins in the Yeast Two-Hybrid System. Genomics 2001, 76, 81–88. [Google Scholar] [CrossRef]
- Byrne, J.A.; Frost, S.; Chen, Y.; Bright, R.K. Tumor Protein D52 (TPD52) and Cancer—Oncogene Understudy or Understudied Oncogene? Tumor Biol. 2014, 35, 7369–7382. [Google Scholar] [CrossRef]
- Marazuela, M.; Martín-Belmonte, F.; García-López, M.A.; Aranda, J.F.; de Marco, M.C.; Alonso, M.A. Expression and Distribution of MAL2, an Essential Element of the Machinery for Basolateral-to-Apical Transcytosis, in Human Thyroid Epithelial Cells. Endocrinology 2004, 145, 1011–1016. [Google Scholar] [CrossRef]
- De Marco, M.C.; Puertollano, R.; Martínez-Menárguez, J.A.; Alonso, M.A. Dynamics of MAL2 During Glycosylphosphatidylinositol-Anchored Protein Transcytotic Transport to the Apical Surface of Hepatoma HepG2 Cells. Traffic 2006, 7, 61–73. [Google Scholar] [CrossRef]
- Madrid, R.; Aranda, J.F.; Rodríguez-Fraticelli, A.E.; Ventimiglia, L.; Andres-Delgado, L.; Shehata, M.; Fanayan, S.; Shahheydari, H.; Gomez, S.; Jimenez, A.; et al. The Formin INF2 Regulates Basolateral-to-Apical Transcytosis and Lumen Formation in Association with Cdc42 and MAL2. Dev. Cell 2010, 18, 814–827. [Google Scholar] [CrossRef]
- In, J.G.; Tuma, P.L. MAL2 Selectively Regulates Polymeric IgA Receptor Delivery from the Golgi to the Plasma Membrane in WIF-B Cells. Traffic 2010, 11, 1056–1066. [Google Scholar] [CrossRef]
- Lautner-Rieske, A.; Thiebe, R.; Zachau, H.G. Searching for Non-Vκ Transcripts from the Human Immunoglobulin κ Locus. Gene 1995, 159, 199–202. [Google Scholar] [CrossRef]
- Saunier, S. A Novel Gene That Encodes a Protein with a Putative Src Homology 3 Domain Is a Candidate Gene for Familial Juvenile Nephronophthisis. Hum. Mol. Genet. 1997, 6, 2317–2323. [Google Scholar] [CrossRef]
- Hildebrandt, F.; Otto, E.; Rensing, C.; Nothwang, H.G.; Vollmer, M.; Adolphs, J.; Hanusch, H.; Brandis, M. A Novel Gene Encoding an SH3 Domain Protein Is Mutated in Nephronophthisis Type 1. Nat. Genet. 1997, 17, 149–153. [Google Scholar] [CrossRef]
- Lyon, A.S.; Peeples, W.B.; Rosen, M.K. A Framework for Understanding the Functions of Biomolecular Condensates across Scales. Nat. Rev. Mol. Cell Biol. 2021, 22, 215–235. [Google Scholar] [CrossRef]
- Lallemand-Breitenbach, V.; de Thé, H. PML Nuclear Bodies: From Architecture to Function. Curr. Opin. Cell Biol. 2018, 52, 154–161. [Google Scholar] [CrossRef]
- Rubio-Ramos, A.; Bernabé-Rubio, M.; Labat-de-Hoz, L.; Casares-Arias, J.; Kremer, L.; Correas, I.; Alonso, M.A. MALL, a Membrane-Tetra-Spanning Proteolipid Overexpressed in Cancer, Is Present in Membraneless Nuclear Biomolecular Condensates. Cell Mol. Life Sci. 2022, 79, 236. [Google Scholar] [CrossRef]
- Tosteson, M.T.; Sapirstein, V.S. Protein Interactions with Lipid Bilayers: The Channels of Kidney Plasma Membrane Proteolipids. J. Membr. Biol. 1981, 63, 77–84. [Google Scholar] [CrossRef]
- Shulgin, A.A.; Lebedev, T.D.; Prassolov, V.S.; Spirin, P.V. Plasmolipin and Its Role in Cell Processes. Mol. Biol. 2021, 55, 773–785. [Google Scholar] [CrossRef]
- Rodríguez-Fraticelli, A.E.; Bagwell, J.; Bosch-Fortea, M.; Boncompain, G.; Reglero-Real, N.; García-León, M.J.; Andrés, G.; Toribio, M.L.; Alonso, M.A.; Millán, J.; et al. Developmental Regulation of Apical Endocytosis Controls Epithelial Patterning in Vertebrate Tubular Organs. Nat. Cell Biol. 2015, 17, 241–250. [Google Scholar] [CrossRef] [PubMed]
- Cacho-Navas, C.; Reglero-Real, N.; Colás-Algora, N.; Barroso, S.; de Rivas, G.; Stamatakis, K.; Feito, J.; Andrés, G.; Fresno, M.; Kremer, L.; et al. Plasmolipin Regulates Basolateral-to-Apical Transcytosis of ICAM-1 and Leukocyte Adhesion in Polarized Hepatic Epithelial Cells. Cell Mol. Life Sci. 2022, 79, 61. [Google Scholar] [CrossRef] [PubMed]
- Han, W.; Ding, P.; Xu, M.; Wang, L.; Rui, M.; Shi, S.; Liu, Y.; Zheng, Y.; Chen, Y.; Yang, T.; et al. Identification of Eight Genes Encoding Chemokine-like Factor Superfamily Members 1–8 (CKLFSF1–8) by in Silico Cloning and Experimental Validation. Genomics 2003, 81, 609–617. [Google Scholar] [CrossRef] [PubMed]
- Jin, C.; Ding, P.; Wang, Y.; Ma, D. Regulation of EGF Receptor Signaling by the MARVEL Domain-Containing Protein CKLFSF8. FEBS Lett. 2005, 579, 6375–6382. [Google Scholar] [CrossRef]
- Pettersson, M.; Dannaeus, K.; Nilsson, K.; Jönsson, J.I. Isolation of MYADM, a Novel Hematopoietic-Associated Marker Gene Expressed in Multipotent Progenitor Cells and up-Regulated during Myeloid Differentiation. J. Leukoc. Biol. 2000, 67, 423–431. [Google Scholar] [CrossRef]
- Cui, W.; Yu, L.; He, H.; Chu, Y.; Gao, J.; Wan, B.; Tang, L.; Zhao, S. Cloning of Human Myeloid-Associated Differentiation Marker (MYADM) Gene Whose Expression Was up-Regulated in NB4 Cells Induced by All-Trans Retinoic Acid. Mol. Biol. Rep. 2001, 28, 123–138. [Google Scholar] [CrossRef]
- Wang, Q.; Li, N.; Wang, X.; Shen, J.; Hong, X.; Yu, H.; Zhang, Y.; Wan, T.; Zhang, L.; Wang, J.; et al. Membrane Protein HMYADM Preferentially Expressed in Myeloid Cells Is Up-Regulated during Differentiation of Stem Cells and Myeloid Leukemia Cells. Life Sci. 2007, 80, 420–429. [Google Scholar] [CrossRef]
- Aranda, J.F.; Reglero-Real, N.; Marcos-Ramiro, B.; Ruiz-Sáenz, A.; Fernández-Martín, L.; Bernabé-Rubio, M.; Kremer, L.; Ridley, A.J.; Correas, I.; Alonso, M.A.; et al. MYADM Controls Endothelial Barrier Function through ERM-Dependent Regulation of ICAM-1 Expression. Mol. Biol. Cell 2013, 24, 483–494. [Google Scholar] [CrossRef]
- Edwards, J.R.; Yarychkivska, O.; Boulard, M.; Bestor, T.H. DNA Methylation and DNA Methyltransferases. Epigenetics Chromatin 2017, 10, 23. [Google Scholar] [CrossRef]
- Deaton, A.M.; Bird, A. CpG Islands and the Regulation of Transcription. Genes. Dev. 2011, 25, 1010–1022. [Google Scholar] [CrossRef]
- Brenet, F.; Moh, M.; Funk, P.; Feierstein, E.; Viale, A.J.; Socci, N.D.; Scandura, J.M. DNA Methylation of the First Exon Is Tightly Linked to Transcriptional Silencing. PLoS ONE 2011, 6, e14524. [Google Scholar] [CrossRef]
- Marazuela, M.; Acevedo, A.; García-López, M.A.; Adrados, M.; de Marco, M.C.; Alonso, M.A. Expression of MAL2, an Integral Protein Component of the Machinery for Basolateral-to-Apical Transcytosis, in Human Epithelia. J. Histochem. Cytochem. 2004, 52, 243–252. [Google Scholar] [CrossRef]
- Marazuela, M.; Acevedo, A.; Adrados, M.; García-López, M.A.; Alonso, M.A. Expression of MAL, an Integral Protein Component of the Machinery for Raft-Mediated Pical Transport, in Human Epithelia. J. Histochem. Cytochem. 2003, 51, 665–674. [Google Scholar] [CrossRef]
- Elpidorou, M.; Poulter, J.A.; Szymanska, K.; Baron, W.; Junger, K.; Boldt, K.; Ueffing, M.; Green, L.; Livingston, J.H.; Sheridan, E.G.; et al. Missense Mutation of MAL Causes a Rare Leukodystrophy Similar to Pelizaeus-Merzbacher Disease. Eur. J. Hum. Genet. 2022, 30, 860–864. [Google Scholar] [CrossRef]
- Osório, M.J.; Goldman, S.A. Neurogenetics of Pelizaeus–Merzbacher Disease. In Handbook of Clinical Neurology; Elsevier: Amsterdam, The Netherlands, 2018; Volume 148, pp. 701–722. ISBN 978-0-444-64076-5. [Google Scholar]
- McCourt, A.C.; Parker, J.; Silajdžić, E.; Haider, S.; Sethi, H.; Tabrizi, S.J.; Warner, T.T.; Björkqvist, M. Analysis of White Adipose Tissue Gene Expression Reveals CREB1 Pathway Altered in Huntington’s Disease. J. Huntingt. Dis. 2015, 4, 371–382. [Google Scholar] [CrossRef]
- Hasan, M.I.; Hossain, M.A.; Bhuiyan, P.; Miah, M.S.; Rahman, M.H. A System Biology Approach to Determine Therapeutic Targets by Identifying Molecular Mechanisms and Key Pathways for Type 2 Diabetes That Are Linked to the Development of Tuberculosis and Rheumatoid Arthritis. Life Sci. 2022, 297, 120483. [Google Scholar] [CrossRef]
- Yagil, C.; Hubner, N.; Monti, J.; Schulz, H.; Sapojnikov, M.; Luft, F.C.; Ganten, D.; Yagil, Y. Identification of Hypertension-Related Genes Through an Integrated Genomic-Transcriptomic Approach. Circ. Res. 2005, 96, 617–625. [Google Scholar] [CrossRef]
- Huan, T.; Esko, T.; Peters, M.J.; Pilling, L.C.; Schramm, K.; Schurmann, C.; Chen, B.H.; Liu, C.; Joehanes, R.; Johnson, A.D.; et al. A Meta-Analysis of Gene Expression Signatures of Blood Pressure and Hypertension. PloS Genet. 2015, 11, e1005035. [Google Scholar] [CrossRef]
- Zeller, T.; Schurmann, C.; Schramm, K.; Müller, C.; Kwon, S.; Wild, P.S.; Teumer, A.; Herrington, D.; Schillert, A.; Iacoviello, L.; et al. Transcriptome-Wide Analysis Identifies Novel Associations with Blood Pressure. Hypertension 2017, 70, 743–750. [Google Scholar] [CrossRef]
- Bai, Y.; Wang, J.; Chen, Y.; Lv, T.; Wang, X.; Liu, C.; Xue, H.; He, K.; Sun, L. The MiR-182/Myadm Axis Regulates Hypoxia-Induced Pulmonary Hypertension by Balancing the BMP- and TGF-β-Signalling Pathways in an SMC/EC-Crosstalk-Associated Manner. Basic. Res. Cardiol. 2021, 116, 53. [Google Scholar] [CrossRef]
- Sun, L.; Lin, P.; Chen, Y.; Yu, H.; Ren, S.; Wang, J.; Zhao, L.; Du, G. MiR-182-3p/Myadm Contribute to Pulmonary Artery Hypertension Vascular Remodeling via a KLF4/P21-Dependent Mechanism. Theranostics 2020, 10, 5581–5599. [Google Scholar] [CrossRef] [PubMed]
- Sun, L.; Bai, Y.; Zhao, R.; Sun, T.; Cao, R.; Wang, F.; He, G.; Zhang, W.; Chen, Y.; Ye, P.; et al. Oncological MiR-182-3p, a Novel Smooth Muscle Cell Phenotype Modulator, Evidences from Model Rats and Patients. Arterioscler. Thromb. Vasc. Biol. 2016, 36, 1386–1397. [Google Scholar] [CrossRef] [PubMed]
- Dy, A.B.C.; Langlais, P.R.; Barker, N.K.; Addison, K.J.; Tanyaratsrisakul, S.; Boitano, S.; Christenson, S.A.; Kraft, M.; Meyers, D.; Bleecker, E.R.; et al. Myeloid-Associated Differentiation Marker Is a Novel SP-A-Associated Transmembrane Protein Whose Expression on Airway Epithelial Cells Correlates with Asthma Severity. Sci. Rep. 2021, 11, 23392. [Google Scholar] [CrossRef] [PubMed]
- Watson, A.; Madsen, J.; Clark, H.W. SP-A and SP-D: Dual Functioning Immune Molecules with Antiviral and Immunomodulatory Properties. Front. Immunol. 2021, 11, 622598. [Google Scholar] [CrossRef]
- Yıldız Bölükbaşı, E.; Shabbir, R.M.K.; Malik, S.; Tolun, A. Homozygous Deletion of MYADML2 in Cranial Asymmetry, Reduced Bone Maturation, Multiple Dislocations, Lumbar Lordosis, and Prominent Clavicles. J. Hum. Genet. 2021, 66, 171–179. [Google Scholar] [CrossRef]
- Horne, H.N.; Lee, P.S.; Murphy, S.K.; Alonso, M.A.; Olson, J.A.; Marks, J.R. Inactivation of the MAL Gene in Breast Cancer Is a Common Event that Predicts Benefit from Adjuvant Chemotherapy. Mol. Cancer Res. 2009, 7, 199–209. [Google Scholar] [CrossRef]
- Kazemi-Noureini, S.; Colonna-Romano, S.; Ziaee, A.-A.; Malboobi, M.-A.; Yazdanbod, M.; Setayeshgar, P.; Maresca, B. Differential Gene Expression between Squamous Cell Carcinoma of Esophageus and Its Normal Epithelium; Altered Pattern of Mal, Akr1c2, and Rab11a Expression. World J. Gastroenterol. 2004, 10, 1716–1721. [Google Scholar] [CrossRef]
- Mimori, K.; Nishida, K.; Nakamura, Y.; Ieta, K.; Yoshikawa, Y.; Sasaki, A.; Ishii, H.; Alonso, M.A.; Mori, M. Loss of MAL Expression in Precancerous Lesions of the Esophagus. Ann. Surg. Oncol. 2007, 14, 1670–1677. [Google Scholar] [CrossRef]
- Beder, L.B.; Gunduz, M.; Hotomi, M.; Fujihara, K.; Shimada, J.; Tamura, S.; Gunduz, E.; Fukushima, K.; Yaykasli, K.; Grenman, R.; et al. T-Lymphocyte Maturation-Associated Protein Gene as a Candidate Metastasis Suppressor for Head and Neck Squamous Cell Carcinomas. Cancer Sci. 2009, 100, 873–880. [Google Scholar] [CrossRef]
- Cao, W.; Zhang, Z.-Y.; Xu, Q.; Sun, Q.; Yan, M.; Zhang, J.; Zhang, P.; Han, Z.-G.; Chen, W.-T. Epigenetic Silencing of MAL, a Putative Tumor Suppressor Gene, Can Contribute to Human Epithelium Cell Carcinoma. Mol. Cancer 2010, 9, 296. [Google Scholar] [CrossRef]
- Lallemant, B.; Evrard, A.; Combescure, C.; Chapuis, H.; Chambon, G.; Raynal, C.; Reynaud, C.; Sabra, O.; Joubert, D.; Hollande, F.; et al. Clinical Relevance of Nine Transcriptional Molecular Markers for the Diagnosis of Head and Neck Squamous Cell Carcinoma in Tissue and Saliva Rinse. BMC Cancer 2009, 9, 370. [Google Scholar] [CrossRef]
- Maruya, S.; Kim, H.-W.; Weber, R.S.; Lee, J.J.; Kies, M.; Luna, M.A.; Batsakis, J.G.; El-Naggar, A.K. Gene Expression Screening of Salivary Gland Neoplasms: Molecular Markers of Potential Histogenetic and Clinical Significance. J. Mol. Diagn. 2004, 6, 180–190. [Google Scholar] [CrossRef]
- Pal, S.K.; Noguchi, S.; Yamamoto, G.; Yamada, A.; Isobe, T.; Hayashi, S.; Tanaka, J.-I.; Tanaka, Y.; Kamijo, R.; Yamane, G.-Y.; et al. Expression of Myelin and Lymphocyte Protein (MAL) in Oral Carcinogenesis. Med. Mol. Morphol. 2012, 45, 222–228. [Google Scholar] [CrossRef]
- Buffart, T.E.; Overmeer, R.M.; Steenbergen, R.D.M.; Tijssen, M.; van Grieken, N.C.T.; Snijders, P.J.F.; Grabsch, H.I.; van de Velde, C.J.H.; Carvalho, B.; Meijer, G.A. MAL Promoter Hypermethylation as a Novel Prognostic Marker in Gastric Cancer. Br. J. Cancer 2008, 99, 1802–1807. [Google Scholar] [CrossRef]
- Kurashige, J.; Sawada, G.; Takahashi, Y.; Eguchi, H.; Sudo, T.; Ikegami, T.; Yoshizumi, T.; Soejima, Y.; Ikeda, T.; Kawanaka, H.; et al. Suppression of MAL Gene Expression in Gastric Cancer Correlates with Metastasis and Mortality. Fukuoka Igaku Zasshi Hukuoka Acta Med. 2013, 104, 344–349. [Google Scholar]
- Kalmár, A.; Péterfia, B.; Hollósi, P.; Galamb, O.; Spisák, S.; Wichmann, B.; Bodor, A.; Tóth, K.; Patai, Á.V.; Valcz, G.; et al. DNA Hypermethylation and Decreased mRNA Expression of MAL, PRIMA1, PTGDR and SFRP1 in Colorectal Adenoma and Cancer. BMC Cancer 2015, 15, 736. [Google Scholar] [CrossRef]
- Lind, G.E.; Ahlquist, T.; Kolberg, M.; Berg, M.; Eknaes, M.; Alonso, M.A.; Kallioniemi, A.; Meling, G.I.; Skotheim, R.I.; Rognum, T.O.; et al. Hypermethylated MAL Gene—A Silent Marker of Early Colon Tumorigenesis. J. Transl. Med. 2008, 6, 13. [Google Scholar] [CrossRef]
- Lind, G.E.; Ahlquist, T.; Lothe, R.A. DNA Hypermethylation of MAL: A Promising Diagnostic Biomarker for Colorectal Tumors. Gastroenterology 2007, 132, 1631–1632. [Google Scholar] [CrossRef]
- Mori, Y.; Cai, K.; Cheng, Y.; Wang, S.; Paun, B.; Hamilton, J.P.; Jin, Z.; Sato, F.; Berki, A.T.; Kan, T.; et al. A Genome-Wide Search Identifies Epigenetic Silencing of Somatostatin, Tachykinin-1, and 5 Other Genes in Colon Cancer. Gastroenterology 2006, 131, 797–808. [Google Scholar] [CrossRef]
- Patai, A.V.; Valcz, G.; Hollösi, P.; Kalm√ár, A.; Péterfia, B.; Patai, Ä.; Wichmann, B.; Spisák, S.; Barták, B.K.; Leiszter, K.; et al. Comprehensive DNA Methylation Analysis Reveals a Common Ten-Gene Methylation Signature in Colorectal Adenomas and Carcinomas. PLoS ONE 2015, 10, e0133836. [Google Scholar] [CrossRef]
- Sambuudash, O.; Kim, H.-S.; Cho, M.Y. Lack of Aberrant Methylation in an Adjacent Area of Left-Sided Colorectal Cancer. Yonsei Med. J. 2017, 58, 749. [Google Scholar] [CrossRef] [PubMed]
- Suzuki, M.; Shiraishi, K.; Eguchi, A.; Ikeda, K.; Mori, T.; Yoshimoto, K.; Ohba, Y.; Yamada, T.; Ito, T.; Baba, Y.; et al. Aberrant Methylation of LINE-1, SLIT2, MAL and IGFBP7 in Non-Small Cell Lung Cancer. Oncol. Rep. 2013, 29, 1308–1314. [Google Scholar] [CrossRef] [PubMed]
- Teneng, I.; Tellez, C.S.; Picchi, M.A.; Klinge, D.M.; Yingling, C.M.; Snider, A.M.; Liu, Y.; Belinsky, S.A. Global Identification of Genes Targeted by DNMT3b for Epigenetic Silencing in Lung Cancer. Oncogene 2015, 34, 621–630. [Google Scholar] [CrossRef] [PubMed]
- Hatta, M.; Nagai, H.; Okino, K.; Onda, M.; Yoneyama, K.; Ohta, Y.; Nakayama, H.; Araki, T.; Emi, M. Down-Regulation of Members of Glycolipid-Enriched Membrane Raft Gene Family, MAL and BENE, in Cervical Squamous Cell Cancers. J. Obstet. Gynaecol. Res. 2004, 30, 53–58. [Google Scholar] [CrossRef]
- Wong, Y.-F.; Cheung, T.-H.; Tsao, G.S.W.; Lo, K.W.K.; Yim, S.-F.; Wang, V.W.; Heung, M.M.S.; Chan, S.C.S.; Chan, L.K.Y.; Ho, T.W.F.; et al. Genome-Wide Gene Expression Profiling of Cervical Cancer in Hong Kong Women by Oligonucleotide Microarray. Int. J. Cancer 2006, 118, 2461–2469. [Google Scholar] [CrossRef]
- Overmeer, R.M.; Henken, F.E.; Bierkens, M.; Wilting, S.M.; Timmerman, I.; Meijer, C.J.L.M.; Snijders, P.J.F.; Steenbergen, R.D.M. Repression of MAL Tumour Suppressor Activity by Promoter Methylation during Cervical Carcinogenesis. J. Pathol. 2009, 219, 327–336. [Google Scholar] [CrossRef]
- Blaveri, E.; Simko, J.P.; Korkola, J.E.; Brewer, J.L.; Baehner, F.; Mehta, K.; Devries, S.; Koppie, T.; Pejavar, S.; Carroll, P.; et al. Bladder Cancer Outcome and Subtype Classification by Gene Expression. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2005, 11, 4044–4055. [Google Scholar] [CrossRef]
- Bosschieter, J.; Nieuwenhuijzen, J.A.; Hentschel, A.; van Splunter, A.P.; Segerink, L.I.; Vis, A.N.; Wilting, S.M.; Lissenberg-Witte, B.I.; A van Moorselaar, R.J.; Steenbergen, R.D. A Two-Gene Methylation Signature for the Diagnosis of Bladder Cancer in Urine. Epigenomics 2019, 11, 337–347. [Google Scholar] [CrossRef]
- Hentschel, A.E.; Nieuwenhuijzen, J.A.; Bosschieter, J.; Splunter, A.P.V.; Lissenberg-Witte, B.I.; Voorn, J.P.V.D.; Segerink, L.I.; Moorselaar, R.J.A.V.; Steenbergen, R.D.M. Comparative Analysis of Urine Fractions for Optimal Bladder Cancer Detection Using DNA Methylation Markers. Cancers 2020, 12, 859. [Google Scholar] [CrossRef]
- Pileri, S.A.; Gaidano, G.; Zinzani, P.L.; Falini, B.; Gaulard, P.; Zucca, E.; Pieri, F.; Berra, E.; Sabattini, E.; Ascani, S.; et al. Primary Mediastinal B-Cell Lymphoma. Am. J. Pathol. 2003, 162, 243–253. [Google Scholar] [CrossRef]
- Copie-Bergman, C.; Plonquet, A.; Alonso, M.A.; Boulland, M.-L.; Marquet, J.; Divine, M.; Moller, P.; Leroy, K.; Gaulard, P. MAL Expression in Lymphoid Cells: Further Evidence for MAL as a Distinct Molecular Marker of Primary Mediastinal Large B-Cell Lymphomas. Mod. Pathol. 2002, 15, 1172–1180. [Google Scholar] [CrossRef]
- Copie-Bergman, C.; Gaulard, P.; Maouche-Chrétien, L.; Brière, J.; Haioun, C.; Alonso, M.A.; Roméo, P.H.; Leroy, K. The MAL Gene Is Expressed in Primary Mediastinal Large B-Cell Lymphoma. Blood 1999, 94, 3567–3575. [Google Scholar] [CrossRef]
- Dorfman, D.M.; Shahsafaei, A.; Alonso, M.A. Utility of CD200 Immunostaining in the Diagnosis of Primary Mediastinal Large B Cell Lymphoma: Comparison with MAL, CD23, and Other Markers. Mod. Pathol. 2012, 25, 1637–1643. [Google Scholar] [CrossRef]
- Shehata, M.; Bièche, I.; Boutros, R.; Weidenhofer, J.; Fanayan, S.; Spalding, L.; Zeps, N.; Byth, K.; Bright, R.K.; Lidereau, R.; et al. Nonredundant Functions for Tumor Protein D52-like Proteins Support Specific Targeting of TPD52. Clin. Cancer Res. 2008, 14, 5050–5060. [Google Scholar] [CrossRef]
- Bhandari, A.; Shen, Y.; Sindan, N.; Xia, E.; Gautam, B.; Lv, S.; Zhang, X. MAL2 Promotes Proliferation, Migration, and Invasion through Regulating Epithelial-Mesenchymal Transition in Breast Cancer Cell Lines. Biochem. Biophys. Res. Commun. 2018, 504, 434–439. [Google Scholar] [CrossRef]
- Zhong, Y.; Zhuang, Z.; Mo, P.; Shang, Q.; Lin, M.; Gong, J.; Huang, J.; Mo, H.; Huang, M. Overexpression of MAL2 Correlates with Immune Infiltration and Poor Prognosis in Breast Cancer. Evid.-Based Complement. Altern. Med. 2021, 2021, 5557873. [Google Scholar] [CrossRef]
- Chen, Y.; Zheng, B.; Robbins, D.H.; Lewin, D.N.; Mikhitarian, K.; Graham, A.; Rumpp, L.; Glenn, T.; Gillanders, W.E.; Cole, D.J.; et al. Accurate Discrimination of Pancreatic Ductal Adenocarcinoma and Chronic Pancreatitis Using Multimarker Expression Data and Samples Obtained by Minimally Invasive Fine Needle Aspiration. Int. J. Cancer 2007, 120, 1511–1517. [Google Scholar] [CrossRef]
- Eguchi, D.; Ohuchida, K.; Kozono, S.; Ikenaga, N.; Shindo, K.; Cui, L.; Fujiwara, K.; Akagawa, S.; Ohtsuka, T.; Takahata, S.; et al. MAL2 Expression Predicts Distant Metastasis and Short Survival in Pancreatic Cancer. Surgery 2013, 154, 573–582. [Google Scholar] [CrossRef]
- Iacobuzio-Donahue, C.A.; Maitra, A.; Olsen, M.; Lowe, A.W.; Van Heek, N.T.; Rosty, C.; Walter, K.; Sato, N.; Parker, A.; Ashfaq, R.; et al. Exploration of Global Gene Expression Patterns in Pancreatic Adenocarcinoma Using cDNA Microarrays. Am. J. Pathol. 2003, 162, 1151–1162. [Google Scholar] [CrossRef]
- Dasgupta, S.; Tripathi, P.K.; Qin, H.; Bhattacharya-Chatterjee, M.; Valentino, J.; Chatterjee, S.K. Identification of Molecular Targets for Immunotherapy of Patients with Head and Neck Squamous Cell Carcinoma. Oral. Oncol. 2006, 42, 306–316. [Google Scholar] [CrossRef]
- Li, J.; Li, Y.; Liu, H.; Liu, Y.; Cui, B. The Four-Transmembrane Protein MAL2 and Tumor Protein D52 (TPD52) Are Highly Expressed in Colorectal Cancer and Correlated with Poor Prognosis. PLoS ONE 2017, 12, e0178515. [Google Scholar] [CrossRef] [PubMed]
- Weis, V.G.; Petersen, C.P.; Mills, J.C.; Tuma, P.L.; Whitehead, R.H.; Goldenring, J.R. Establishment of Novel in Vitro Mouse Chief Cell and SPEM Cultures Identifies MAL2 as a Marker of Metaplasia in the Stomach. Am. J. Physiol. Gastrointest. Liver Physiol. 2014, 307, G777–G792. [Google Scholar] [CrossRef] [PubMed]
- Wang, A.; Guo, H.; Long, Z. Integrative Analysis of Differently Expressed Genes Reveals a 17-Gene Prognosis Signature for Endometrial Carcinoma. BioMed Res. Int. 2021, 2021, 4804694. [Google Scholar] [CrossRef] [PubMed]
- Byrne, J.A.; Maleki, S.; Hardy, J.R.; Gloss, B.S.; Murali, R.; Scurry, J.P.; Fanayan, S.; Emmanuel, C.; Hacker, N.F.; Sutherland, R.L.; et al. MAL2 and Tumor Protein D52 (TPD52) Are Frequently Overexpressed in Ovarian Carcinoma, but Differentially Associated with Histological Subtype and Patient Outcome. BMC Cancer 2010, 10, 497. [Google Scholar] [CrossRef]
- Hoang, C.D.; D’Cunha, J.; Kratzke, M.G.; Casmey, C.E.; Frizelle, S.P.; Maddaus, M.A.; Kratzke, R.A. Gene Expression Profiling Identifies Matriptase Overexpression in Malignant Mesothelioma. Chest 2004, 125, 1843–1852. [Google Scholar] [CrossRef]
- Khan, F.H.; Pandian, V.; Ramraj, S.; Natarajan, M.; Aravindan, S.; Herman, T.S.; Aravindan, N. Acquired Genetic Alterations in Tumor Cells Dictate the Development of High-Risk Neuroblastoma and Clinical Outcomes. BMC Cancer 2015, 15, 514. [Google Scholar] [CrossRef]
- López-Coral, A.; Del Vecchio, G.-J.; Chahine, J.J.; Kallakury, B.V.; Tuma, P.L. MAL2-Induced Actin-Based Protrusion Formation Is Anti-Oncogenic in Hepatocellular Carcinoma. Cancers 2020, 12, E422. [Google Scholar] [CrossRef]
- Yoo, H.-J.; Yun, B.-R.; Kwon, J.-H.; Ahn, H.-S.; Seol, M.-A.; Lee, M.-J.; Yu, G.-R.; Yu, H.-C.; Hong, B.; Choi, K.; et al. Genetic and Expression Alterations in Association with the Sarcomatous Change of Cholangiocarcinoma Cells. Exp. Mol. Med. 2009, 41, 102–115. [Google Scholar] [CrossRef]
- Gao, F.; Shi, L.; Russin, J.; Zeng, L.; Chang, X.; He, S.; Chen, T.C.; Giannotta, S.L.; Weisenberger, D.J.; Zada, G.; et al. DNA Methylation in the Malignant Transformation of Meningiomas. PLoS ONE 2013, 8, e54114. [Google Scholar] [CrossRef]
- Canisius, J.; Wagner, A.; Bunk, E.C.; Spille, D.C.; Stögbauer, L.; Grauer, O.; Hess, K.; Thomas, C.; Paulus, W.; Stummer, W.; et al. Expression of Decitabine-Targeted Oncogenes in Meningiomas in Vivo. Neurosurg. Rev. 2022, 45, 2767–2775. [Google Scholar] [CrossRef]
- Fan, J.; Yan, D.; Teng, M.; Tang, H.; Zhou, C.; Wang, X.; Li, D.; Qiu, G.; Peng, Z. Digital Transcript Profile Analysis with ARNA-LongSAGE Validates FERMT1 as a Potential Novel Prognostic Marker for Colon Cancer. Clin. Cancer Res. 2011, 17, 2908–2918. [Google Scholar] [CrossRef]
- Wang, X.; Fan, J.; Yu, F.; Cui, F.; Sun, X.; Zhong, L.; Yan, D.; Zhou, C.; Deng, G.; Wang, B.; et al. Decreased MALL Expression Negatively Impacts Colorectal Cancer Patient Survival. Oncotarget 2016, 7, 22911–22927. [Google Scholar] [CrossRef]
- Kettunen, E.; Anttila, S.; Seppänen, J.K.; Karjalainen, A.; Edgren, H.; Lindström, I.; Salovaara, R.; Nissén, A.-M.; Salo, J.; Mattson, K.; et al. Differentially Expressed Genes in Nonsmall Cell Lung Cancer: Expression Profiling of Cancer-Related Genes in Squamous Cell Lung Cancer. Cancer Genet. Cytogenet. 2004, 149, 98–106. [Google Scholar] [CrossRef]
- Sato, R.; Nakano, T.; Hosonaga, M.; Sampetrean, O.; Harigai, R.; Sasaki, T.; Koya, I.; Okano, H.; Kudoh, J.; Saya, H.; et al. RNA Sequencing Analysis Reveals Interactions between Breast Cancer or Melanoma Cells and the Tissue Microenvironment during Brain Metastasis. BioMed Res. Int. 2017, 2017, 8032910. [Google Scholar] [CrossRef]
- Gao, D.; Hu, H.; Wang, Y.; Yu, W.; Zhou, J.; Wang, X.; Wang, W.; Zhou, C.; Xu, K. CMTM8 Inhibits the Carcinogenesis and Progression of Bladder Cancer. Oncol. Rep. 2015, 34, 2853–2863. [Google Scholar] [CrossRef]
- Yan, M.; Zhu, X.; Qiao, H.; Zhang, H.; Xie, W.; Cai, J. Downregulated CMTM8 Correlates with Poor Prognosis in Gastric Cancer Patients. DNA Cell Biol. 2021, 40, 791–797. [Google Scholar] [CrossRef]
- Zhang, W.; Qi, H.; Mo, X.; Sun, Q.; Li, T.; Song, Q.; Xu, K.; Hu, H.; Ma, D.; Wang, Y. CMTM8 Is Frequently Downregulated in Multiple Solid Tumors. Appl. Immunohistochem. Mol. Morphol. 2017, 25, 122–128. [Google Scholar] [CrossRef]
- Shi, W.; Zhang, C.; Ning, Z.; Hua, Y.; Li, Y.; Chen, L.; Liu, L.; Chen, Z.; Meng, Z. CMTM8 as an LPA1-Associated Partner Mediates Lysophosphatidic Acid-Induced Pancreatic Cancer Metastasis. Ann. Transl. Med. 2021, 9, 42. [Google Scholar] [CrossRef]
- De Wit, N.J.W.; Rijntjes, J.; Diepstra, J.H.S.; van Kuppevelt, T.H.; Weidle, U.H.; Ruiter, D.J.; van Muijen, G.N.P. Analysis of Differential Gene Expression in Human Melanocytic Tumour Lesions by Custom Made Oligonucleotide Arrays. Br. J. Cancer 2005, 92, 2249–2261. [Google Scholar] [CrossRef]
- Tang, Z.; Kang, B.; Li, C.; Chen, T.; Zhang, Z. GEPIA2: An Enhanced Web Server for Large-Scale Expression Profiling and Interactive Analysis. Nucleic Acids Res. 2019, 47, W556–W560. [Google Scholar] [CrossRef]
- Ostrow, K.L.; Park, H.L.; Hoque, M.O.; Kim, M.S.; Liu, J.; Argani, P.; Westra, W.; Van Criekinge, W.; Sidransky, D. Pharmacologic Unmasking of Epigenetically Silenced Genes in Breast Cancer. Clin. Cancer Res. 2009, 15, 1184–1191. [Google Scholar] [CrossRef] [PubMed]
- Ahlquist, T.; Lind, G.E.; Costa, V.L.; Meling, G.I.; Vatn, M.; Hoff, G.S.; Rognum, T.O.; Skotheim, R.I.; Thiis-Evensen, E.; Lothe, R.A. Gene Methylation Profiles of Normal Mucosa, and Benign and Malignant Colorectal Tumors Identify Early Onset Markers. Mol. Cancer 2008, 7, 94. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Bi, H.; Ge, A.; Xia, T.; Fu, J.; Liu, Y.; Sun, H.; Li, D.; Zhao, Y. DNA Hypermethylation of MAL Gene May Act as an Independent Predictor of Favorable Prognosis in Patients with Colorectal Cancer. Transl. Cancer Res. 2019, 8, 1985–1996. [Google Scholar] [CrossRef] [PubMed]
- Jin, Z.; Wang, L.; Zhang, Y.; Cheng, Y.; Gao, Y.; Feng, X.; Dong, M.; Cao, Z.; Chen, S.; Yu, H.; et al. MAL Hypermethylation Is a Tissue-Specific Event That Correlates with MAL mRNA Expression in Esophageal Carcinoma. Sci. Rep. 2013, 3, 2838. [Google Scholar] [CrossRef]
- Su, C.; Huang, R.; Yu, Z.; Zheng, J.; Liu, F.; Liang, H.; Mo, Z. Myelin and Lymphocyte Protein Serves as a Prognostic Biomarker and Is Closely Associated with the Tumor Microenvironment in the Nephroblastoma. Cancer Med. 2022, 11, 1427–1438. [Google Scholar] [CrossRef]
- Ahmad, A.S.; Vasiljeviƒá, N.; Carter, P.; Berney, D.M.; Moller, H.; Foster, C.S.; Cuzick, J.; Lorincz, A.T. A Novel DNA Methylation Score Accurately Predicts Death from Prostate Cancer in Men with Low to Intermediate Clinical Risk Factors. Oncotarget 2015, 7, 71833–71840. [Google Scholar] [CrossRef]
- Vasiljević, N.; Ahmad, A.S.; Thorat, M.A.; Fisher, G.; Berney, D.M.; Møller, H.; Foster, C.S.; Cuzick, J.; Lorincz, A.T. DNA Methylation Gene-Based Models Indicating Independent Poor Outcome in Prostate Cancer. BMC Cancer 2014, 14, 655. [Google Scholar] [CrossRef]
- Mimori, K.; Shiraishi, T.; Mashino, K.; Sonoda, H.; Yamashita, K.; Yoshinaga, K.; Masuda, T.; Utsunomiya, T.; Alonso, M.A.; Inoue, H.; et al. MAL Gene Expression in Esophageal Cancer Suppresses Motility, Invasion and Tumorigenicity and Enhances Apoptosis through the Fas Pathway. Oncogene 2003, 22, 3463–3471. [Google Scholar] [CrossRef]
- Lee, P.S.; Teaberry, V.S.; Bland, A.E.; Huang, Z.; Whitaker, R.S.; Baba, T.; Fujii, S.; Secord, A.A.; Berchuck, A.; Murphy, S.K. Elevated MAL Expression Is Accompanied by Promoter Hypomethylation and Platinum Resistance in Epithelial Ovarian Cancer. Int. J. Cancer 2010, 126, 1378–1389. [Google Scholar] [CrossRef]
- Yuan, J.; Jiang, X.; Lan, H.; Zhang, X.; Ding, T.; Yang, F.; Zeng, D.; Yong, J.; Niu, B.; Xiao, S. Multi-Omics Analysis of the Therapeutic Value of MAL2 Based on Data Mining in Human Cancers. Front. Cell Dev. Biol. 2021, 9, 736649. [Google Scholar] [CrossRef]
- Cerami, E.; Gao, J.; Dogrusoz, U.; Gross, B.E.; Sumer, S.O.; Aksoy, B.A.; Jacobsen, A.; Byrne, C.J.; Heuer, M.L.; Larsson, E.; et al. The CBio Cancer Genomics Portal: An Open Platform for Exploring Multidimensional Cancer Genomics Data. Cancer Discov. 2012, 2, 401–404. [Google Scholar] [CrossRef]
- Gao, J.; Aksoy, B.A.; Dogrusoz, U.; Dresdner, G.; Gross, B.; Sumer, S.O.; Sun, Y.; Jacobsen, A.; Sinha, R.; Larsson, E.; et al. Integrative Analysis of Complex Cancer Genomics and Clinical Profiles Using the CBioPortal. Sci. Signal. 2013, 6, pl1. [Google Scholar] [CrossRef]
- Yu, W.; Kanaan, Y.; Bae, Y.K.; Baed, Y.-K.; Gabrielson, E. Chromosomal Changes in Aggressive Breast Cancers with Basal-like Features. Cancer Genet. Cytogenet. 2009, 193, 29–37. [Google Scholar] [CrossRef]
- Lakhotia, S.C.; Mallick, B.; Roy, J. Non-Coding RNAs: Ever-Expanding Diversity of Types and Functions. In RNA-Based Regulation in Human Health and Disease; Elsevier: Amsterdam, The Netherlands, 2020; pp. 5–57. ISBN 978-0-12-817193-6. [Google Scholar]
- Gebert, L.F.R.; MacRae, I.J. Regulation of MicroRNA Function in Animals. Nat. Rev. Mol. Cell Biol. 2019, 20, 21–37. [Google Scholar] [CrossRef]
- Guo, J.U.; Agarwal, V.; Guo, H.; Bartel, D.P. Expanded Identification and Characterization of Mammalian Circular RNAs. Genome Biol. 2014, 15, 409. [Google Scholar] [CrossRef]
- Smolarz, B.; Zadrożna-Nowak, A.; Romanowicz, H. The Role of LncRNA in the Development of Tumors, Including Breast Cancer. Int. J. Mol. Sci. 2021, 22, 8427. [Google Scholar] [CrossRef]
- Gao, X.; Chen, Z.; Li, A.; Zhang, X.; Cai, X. MiR-129 Regulates Growth and Invasion by Targeting MAL2 in Papillary Thyroid Carcinoma. Biomed. Pharmacother. Biomed. Pharmacother. 2018, 105, 1072–1078. [Google Scholar] [CrossRef]
- Chen, L.; Li, H.; Yao, D.; Zou, Q.; Yu, W.; Zhou, L. The Novel Circ_0084904/MiR-802/MAL2 Axis Promotes the Development of Cervical Cancer. Reprod. Biol. 2022, 22, 100600. [Google Scholar] [CrossRef]
- Tao, L.; Mu, X.; Chen, H.; Jin, D.; Zhang, R.; Zhao, Y.; Fan, J.; Cao, M.; Zhou, Z. FTO Modifies the M6A Level of MALAT and Promotes Bladder Cancer Progression. Clin. Transl. Med. 2021, 11, e310. [Google Scholar] [CrossRef]
- Zhang, C.; Xu, L.; Li, X.; Chen, Y.; Shi, T.; Wang, Q. LINC00460 Facilitates Cell Proliferation and Inhibits Ferroptosis in Breast Cancer Through the MiR-320a/MAL2 Axis. Technol. Cancer Res. Treat. 2023, 22, 153303382311643. [Google Scholar] [CrossRef]
- Liu, Y.-T.; Xu, Z.; Liu, W.; Ren, S.; Xiong, H.-W.; Jiang, T.; Chen, J.; Kang, Y.; Li, Q.-Y.; Wu, Z.-H.; et al. The Circ_0002538/MiR-138-5p/Plasmolipin Axis Regulates Schwann Cell Migration and Myelination in Diabetic Peripheral Neuropathy. Neural Regen. Res. 2023, 18, 1591. [Google Scholar] [CrossRef] [PubMed]
- Zeng, X.; Ma, X.; Guo, H.; Wei, L.; Zhang, Y.; Sun, C.; Han, N.; Sun, S.; Zhang, N. MicroRNA-582-5p Promotes Triple-Negative Breast Cancer Invasion and Metastasis by Antagonizing CMTM8. Bioengineered 2021, 12, 10126–10135. [Google Scholar] [CrossRef]
- Sanz-Moreno, V.; Gadea, G.; Ahn, J.; Paterson, H.; Marra, P.; Pinner, S.; Sahai, E.; Marshall, C.J. Rac Activation and Inactivation Control Plasticity of Tumor Cell Movement. Cell 2008, 135, 510–523. [Google Scholar] [CrossRef] [PubMed]
- Fang, Y.; Wang, L.; Wan, C.; Sun, Y.; Van der Jeught, K.; Zhou, Z.; Dong, T.; So, K.M.; Yu, T.; Li, Y.; et al. MAL2 Drives Immune Evasion in Breast Cancer by Suppressing Tumor Antigen Presentation. J. Clin. Investig. 2021, 131, 140837. [Google Scholar] [CrossRef] [PubMed]
- Jeong, J.; Shin, J.H.; Li, W.; Hong, J.Y.; Lim, J.; Hwang, J.Y.; Chung, J.-J.; Yan, Q.; Liu, Y.; Choi, J.; et al. MAL2 Mediates the Formation of Stable HER2 Signaling Complexes within Lipid Raft-Rich Membrane Protrusions in Breast Cancer Cells. Cell Rep. 2021, 37, 110160. [Google Scholar] [CrossRef]
- Zhang, B.; Xiao, J.; Cheng, X.; Liu, T. MAL2 Interacts with IQGAP1 to Promote Pancreatic Cancer Progression by Increasing ERK1/2 Phosphorylation. Biochem. Biophys. Res. Commun. 2021, 554, 63–70. [Google Scholar] [CrossRef]
- Lian, Z.; Yan, X.; Diao, Y.; Cui, D.; Liu, H. T Cell Differentiation Protein 2 Facilitates Cell Proliferation by Enhancing MTOR-Mediated Ribosome Biogenesis in Non-Small Cell Lung Cancer. Discov. Oncol. 2022, 13, 26. [Google Scholar] [CrossRef]
- Zhang, B.; Ren, Z.; Zheng, H.; Lin, M.; Chen, G.; Luo, O.J.; Zhu, G. CRISPR Activation Screening in a Mouse Model for Drivers of Hepatocellular Carcinoma Growth and Metastasis. iScience 2023, 26, 106099. [Google Scholar] [CrossRef]
- Kazanets, A.; Shorstova, T.; Hilmi, K.; Marques, M.; Witcher, M. Epigenetic Silencing of Tumor Suppressor Genes: Paradigms, Puzzles, and Potential. Biochim. Biophys. Acta BBA—Rev. Cancer 2016, 1865, 275–288. [Google Scholar] [CrossRef]
- Li, D.; Zhang, J.; Wu, L.; Yang, X.; Chen, Z.; Yuan, J. Myelin and Lymphocyte Protein (MAL): A Novel Biomarker for Uterine Corpus Endometrial Carcinoma. Cancer Manag. Res. 2021, 13, 7311–7323. [Google Scholar] [CrossRef]
- Zhang, W.; Mendoza, M.C.; Pei, X.; Ilter, D.; Mahoney, S.J.; Zhang, Y.; Ma, D.; Blenis, J.; Wang, Y. Down-Regulation of CMTM8 Induces Epithelial-to-Mesenchymal Transition-like Changes via c-MET/Extracellular Signal-Regulated Kinase (ERK) Signaling. J. Biol. Chem. 2012, 287, 11850–11858. [Google Scholar] [CrossRef] [PubMed]
- Wang, K.; Yang, Y.; Zheng, S.; Hu, W. Association Mining Identifies MAL2 as a Novel Tumor Suppressor in Colorectal Cancer. OncoTargets Ther. 2022, 15, 761–769. [Google Scholar] [CrossRef] [PubMed]
- Zheng, C.; Wang, J.; Zhang, J.; Hou, S.; Zheng, Y.; Wang, Q. Myelin and Lymphocyte Protein 2 Regulates Cell Proliferation and Metastasis through the Notch Pathway in Prostate Adenocarcinoma. Transl. Androl. Urol. 2021, 10, 2067–2077. [Google Scholar] [CrossRef] [PubMed]
- Berchuck, A.; Iversen, E.S.; Luo, J.; Clarke, J.P.; Horne, H.; Levine, D.A.; Boyd, J.; Alonso, M.A.; Secord, A.A.; Bernardini, M.Q.; et al. Microarray Analysis of Early Stage Serous Ovarian Cancers Shows Profiles Predictive of Favorable Outcome. Clin. Cancer Res. 2009, 15, 2448. [Google Scholar] [CrossRef]
- Hsi, E.D.; Sup, S.J.; Alemany, C.; Tso, E.; Skacel, M.; Elson, P.; Alonso, M.A.; Pohlman, B. MAL Is Expressed in a Subset of Hodgkin Lymphoma and Identifies a Population of Patients with Poor Prognosis. Am. J. Clin. Pathol. 2006, 125, 776–782. [Google Scholar] [CrossRef]
- Rohan, S.; Tu, J.J.; Kao, J.; Mukherjee, P.; Campagne, F.; Zhou, X.K.; Hyjek, E.; Alonso, M.A.; Chen, Y.-T. Gene Expression Profiling Separates Chromophobe Renal Cell Carcinoma from Oncocytoma and Identifies Vesicular Transport and Cell Junction Proteins as Differentially Expressed Genes. Clin. Cancer Res. 2006, 12, 6937–6945. [Google Scholar] [CrossRef]
- Bhosale, P.G.; Cristea, S.; Ambatipudi, S.; Desai, R.S.; Kumar, R.; Patil, A.; Kane, S.; Borges, A.M.; Schäffer, A.A.; Beerenwinkel, N.; et al. Chromosomal Llterations and Gene Expression Changes Associated with the Progression of Leukoplakia to Advanced Gingivobuccal Cancer. Transl. Oncol. 2017, 10, 396–409. [Google Scholar] [CrossRef]
- Hesselink, A.T.; Heideman, D.A.M.; Steenbergen, R.D.M.; Coupé, V.M.H.; Overmeer, R.M.; Rijkaart, D.; Berkhof, J.; Meijer, C.J.L.M.; Snijders, P.J.F. Combined Promoter Methylation Analysis of CADM1 and MAL: An Objective Triage Tool for High-Risk Human Papillomavirus DNA-Positive Women. Clin. Cancer Res. 2011, 17, 2459–2465. [Google Scholar] [CrossRef]
- Holubekova, V.; Mersakova, S.; Grendar, M.; Snahnicanova, Z.; Kudela, E.; Kalman, M.; Lasabova, Z.; Danko, J.; Zubor, P. The Role of CADM1 and MAL Promoter Methylation in Inflammation and Cervical Intraepithelial Neoplasia. Genet. Test. Mol. Biomark. 2020, 24, 256–263. [Google Scholar] [CrossRef]
- Meršaková, S.; Holubeková, V.; Grendár, M.; Višňovsky, J.; Ňachajová, M.; Kalman, M.; Kúdela, E.; Žúbor, P.; Bielik, T.; Lasabová, Z.; et al. Methylation of CADM1 and MAL Together with HPV Status in Cytological Cervical Specimens Serves an Important Role in the Progression of Cervical Intraepithelial Neoplasia. Oncol. Lett. 2018, 16, 7166–7174. [Google Scholar] [CrossRef]
- Uijterwaal, M.H.; van Zummeren, M.; Kocken, M.; Luttmer, R.; Berkhof, J.; Witte, B.I.; van Baal, W.M.; Graziosi, G.C.M.; Verheijen, R.H.M.; Helmerhorst, T.J.M.; et al. Performance of CADM1/MAL-Methylation Analysis for Monitoring of Women Treated for High-Grade CIN. Gynecol. Oncol. 2016, 143, 135–142. [Google Scholar] [CrossRef]
- Van Baars, R.; van der Marel, J.; Snijders, P.J.F.; Rodriquez-Manfredi, A.; ter Harmsel, B.; van den Munckhof, H.A.M.; Ordi, J.; del Pino, M.; van de Sandt, M.M.; Wentzensen, N.; et al. CADM1 and MAL Methylation Status in Cervical Scrapes Is Representative of the Most Severe Underlying Lesion in Women with Multiple Cervical Biopsies: CADM1 and MAL Methylation on Lesion Level. Int. J. Cancer 2016, 138, 463–471. [Google Scholar] [CrossRef]
- Hutajulu, S.H.; Indrasari, S.R.; Indrawati, L.P.L.; Harijadi, A.; Duin, S.; Haryana, S.M.; Steenbergen, R.D.M.; Greijer, A.E.; Middeldorp, J.M. Epigenetic Markers for Early Detection of Nasopharyngeal Carcinoma in a High Risk Population. Mol. Cancer 2011, 10, 48. [Google Scholar] [CrossRef]
- Hassan, Z.K.; Hafez, M.M.; Kamel, M.M.; Zekri, A.R.N. Human Papillomavirus Genotypes and Methylation of CADM1, PAX1, MAL and ADCYAP1 Genes in Epithelial Ovarian Cancer Patients. Asian Pac. J. Cancer Prev. 2017, 18, 169–176. [Google Scholar] [CrossRef]
- Iwasaki, T.; Matsushita, M.; Nonaka, D.; Nagata, K.; Kato, M.; Kuwamoto, S.; Murakami, I.; Hayashi, K. Lower Expression of CADM1 and Higher Expression of MAL in Merkel Cell Carcinomas Are Associated with Merkel Cell Polyomavirus Infection and Better Prognosis. Hum. Pathol. 2016, 48, 1–8. [Google Scholar] [CrossRef]
- Martins, I.; Ribeiro, I.P.; Jorge, J.; Gonçalves, A.C.; Sarmento-Ribeiro, A.B.; Melo, J.B.; Carreira, I.M. Liquid Biopsies: Applications for Cancer Diagnosis and Monitoring. Genes 2021, 12, 349. [Google Scholar] [CrossRef]
- Liu, Y.; Chew, M.H.; Tham, C.K.; Tang, C.L.; Ong, S.Y.K.; Zhao, Y. Methylation of Serum SST Gene Is an Independent Prognostic Marker in Colorectal Cancer. Am. J. Cancer Res. 2016, 6, 2098–2108. [Google Scholar]
- Agostini, M.; Enzo, M.V.; Bedin, C.; Belardinelli, V.; Goldin, E.; Del Bianco, P.; Maschietto, E.; D’Angelo, E.; Izzi, L.; Saccani, A.; et al. Circulating Cell-Free DNA: A Promising Marker of Regional Lymphonode Metastasis in Breast Cancer Patients. Cancer Biomark. Sect. Dis. Markers 2012, 11, 89–98. [Google Scholar] [CrossRef]
- Guerrero-Preston, R.; Hadar, T.; Ostrow, K.L.; Soudry, E.; Echenique, M.; Ili-Gangas, C.; Pérez, G.; Perez, J.; Brebi-Mieville, P.; Deschamps, J.; et al. Differential Promoter Methylation of Kinesin Family Member 1a in Plasma Is Associated with Breast Cancer and DNA Repair Capacity. Oncol. Rep. 2014, 32, 505–512. [Google Scholar] [CrossRef]
- Leffers, M.; Herbst, J.; Kropidlowski, J.; Prieske, K.; Bohnen, A.L.; Peine, S.; Jaeger, A.; Oliveira-Ferrer, L.; Goy, Y.; Schmalfeldt, B.; et al. Combined Liquid Biopsy Methylation Analysis of CADM1 and MAL in Cervical Cancer Patients. Cancers 2022, 14, 3954. [Google Scholar] [CrossRef]
- Lind, G.E.; Danielsen, S.A.; Ahlquist, T.; Merok, M.A.; Andresen, K.; Skotheim, R.I.; Hektoen, M.; Rognum, T.O.; Meling, G.I.; Hoff, G.; et al. Identification of an Epigenetic Biomarker Panel with High Sensitivity and Specificity for Colorectal Cancer and Adenomas. Mol. Cancer 2011, 10, 85. [Google Scholar] [CrossRef] [PubMed]
- Obermayr, E.; Sanchez-Cabo, F.; Tea, M.-K.M.; Singer, C.F.; Krainer, M.; Fischer, M.B.; Sehouli, J.; Reinthaller, A.; Horvat, R.; Heinze, G.; et al. Assessment of a Six Gene Panel for the Molecular Detection of Circulating Tumor Cells in the Blood of Female Cancer Patients. BMC Cancer 2010, 10, 666. [Google Scholar] [CrossRef] [PubMed]
- Obermayr, E.; Maritschnegg, E.; Agreiter, C.; Pecha, N.; Speiser, P.; Helmy-Bader, S.; Danzinger, S.; Krainer, M.; Singer, C.; Zeillinger, R. Efficient Leukocyte Depletion by a Novel Microfluidic Platform Enables the Molecular Detection and Characterization of Circulating Tumor Cells. Oncotarget 2018, 9, 812–823. [Google Scholar] [CrossRef] [PubMed]
- Tracey, L.; Villuendas, R.; Ortiz, P.; Dopazo, A.; Spiteri, I.; Lombardia, L.; Rodríguez-Peralto, J.L.; Fernández-Herrera, J.; Hernández, A.; Fraga, J.; et al. Identification of Genes Involved in Resistance to Interferon-Alpha in Cutaneous T-Cell Lymphoma. Am. J. Pathol. 2002, 161, 1825–1837. [Google Scholar] [CrossRef] [PubMed]
- Berchuck, A.; Iversen, E.S.; Lancaster, J.M.; Pittman, J.; Luo, J.; Lee, P.; Murphy, S.; Dressman, H.K.; Febbo, P.G.; West, M.; et al. Patterns of Gene ExpressionThat Characterize Long-Term Survival in Advanced Stage Serous Ovarian Cancers. Clin. Cancer Res. 2005, 11, 3686–3696. [Google Scholar] [CrossRef]
- Zanotti, L.; Romani, C.; Tassone, L.; Todeschini, P.; Tassi, R.A.; Bandiera, E.; Damia, G.; Ricci, F.; Ardighieri, L.; Calza, S.; et al. MAL Gene Overexpression as a Marker of High-Grade Serous Ovarian Carcinoma Stem-like Cells That Predicts Chemoresistance and Poor Prognosis. BMC Cancer 2017, 17, 366. [Google Scholar] [CrossRef]
- Arumugam, T.; Ramachandran, V.; Fournier, K.F.; Wang, H.; Marquis, L.; Abbruzzese, J.L.; Gallick, G.E.; Logsdon, C.D.; McConkey, D.J.; Choi, W. Epithelial to Mesenchymal Transition Contributes to Drug Resistance in Pancreatic Cancer. Cancer Res. 2009, 69, 5820–5828. [Google Scholar] [CrossRef]
- Lánczky, A.; Győrffy, B. Web-Based Survival Analysis Tool Tailored for Medical Research (KMplot): Development and Implementation. J. Med. Internet Res. 2021, 23, e27633. [Google Scholar] [CrossRef]
- Ding, W.; Li, Z.; Wang, C.; Dai, J.; Ruan, G.; Tu, C. Anthracycline versus Nonanthracycline Adjuvant Therapy for Early Breast Cancer: A Systematic Review and Meta-Analysis. Medicine 2018, 97, e12908. [Google Scholar] [CrossRef]
- Willson, M.L.; Burke, L.; Ferguson, T.; Ghersi, D.; Nowak, A.K.; Wilcken, N. Taxanes for Adjuvant Treatment of Early Breast Cancer. Cochrane Database Syst. Rev. 2019, 2019, CD004421. [Google Scholar] [CrossRef]
- Dawson, P.A.; Lan, T.; Rao, A. Bile Acid Transporters. J. Lipid Res. 2009, 50, 2340–2357. [Google Scholar] [CrossRef]
- Deng, F.; Han Bae, Y. Lipid Raft-Mediated and Upregulated Coordination Pathways Assist Transport of Glycocholic Acid-Modified Nanoparticle in a Human Breast Cancer Cell Line of SK-BR-3. Int. J. Pharm. 2022, 617, 121589. [Google Scholar] [CrossRef]
- Kang, N.; Xie, X.; Zhou, X.; Wang, Y.; Chen, S.; Qi, R.; Liu, T.; Jiang, H. Identification and Validation of EMT-Immune-Related Prognostic Biomarkers CDKN2A, CMTM8 and ILK in Colon Cancer. BMC Gastroenterol. 2022, 22, 190. [Google Scholar] [CrossRef]
- Martin-Belmonte, F.; Kremer, L.; Albar, J.P.; Marazuela, M.; Alonso, M.A. Expression of the MAL Gene in the Thyroid: The MAL Proteolipid, a Component of Glycolipid-Enriched Membranes, Is Apically Distributed in Thyroid Follicles. Endocrinology 1998, 139, 2077–2084. [Google Scholar] [CrossRef]
- Traverse-Glehen, A.; Pittaluga, S.; Gaulard, P.; Sorbara, L.; Alonso, M.A.; Raffeld, M.; Jaffe, E.S. Mediastinal Gray Zone Lymphoma: The Missing Link Between Classic Hodgkin??S Lymphoma and Mediastinal Large B-Cell Lymphoma. Am. J. Surg. Pathol. 2005, 29, 1411–1421. [Google Scholar] [CrossRef]
- Ventimiglia, L.N.; Fernández-Martín, L.; Martínez-Alonso, E.; Antón, O.M.; Guerra, M.; Martínez-Menárguez, J.A.; Andrés, G.; Alonso, M.A. Cutting Edge: Regulation of Exosome Secretion by the Integral MAL Protein in T Cells. J. Immunol. 2015, 195, 810. [Google Scholar] [CrossRef]
- Andres-Delgado, L.; Anton, O.M.; Madrid, R.; Byrne, J.A.; Alonso, M.A. Formin INF2 Regulates MAL-Mediated Transport of Lck to the Plasma Membrane of Human T Lymphocytes. Blood 2010, 116, 5919–5929. [Google Scholar] [CrossRef]
- Ortonne, N.; Copie-Bergman, C.; Remy, P.; Delfau-Larue, M.-H.; Alonso, M.A.; Mariette, X.; Dierlamm, J.; Leroy, K.; Gaulard, P. Mucosa-Associated Lymphoid Tissue Lymphoma of the Thymus: A Case Report with No Evidence of MALT1 Rearrangement. Virchows Arch. 2005, 446, 189–193. [Google Scholar] [CrossRef]
- Llorente, A.; de Marco, M.C.; Alonso, M.A. Caveolin-1 and MAL Are Located on Prostasomes Secreted by the Prostate Cancer PC-3 Cell Line. J. Cell Sci. 2004, 117, 5343–5351. [Google Scholar] [CrossRef]
- Fanayan, S.; Shehata, M.; Agterof, A.P.; McGuckin, M.A.; Alonso, M.A.; Byrne, J.A. Mucin 1 (MUC1) Is a Novel Partner for MAL2 in Breast Carcinoma Cells. BMC Cell Biol. 2009, 10, 7. [Google Scholar] [CrossRef]
- Bosse, F.; Hasse, B.; Pippirs, U.; Greiner-Petter, R.; Müller, H.-W. Proteolipid Plasmolipin: Localization in Polarized Cells, Regulated Expression and Lipid Raft Association in CNS and PNS Myelin: Polarized Plasmolipin Expression. J. Neurochem. 2004, 86, 508–518. [Google Scholar] [CrossRef] [PubMed]
- Hamacher, M.; Pippirs, U.; Köhler, A.; Müller, H.W.; Bosse, F. Plasmolipin: Genomic Structure, Chromosomal Localization, Protein Expression Pattern, and Putative Association with Bardet-Biedl Syndrome. Mamm. Genome 2001, 12, 933–937. [Google Scholar] [CrossRef] [PubMed]
- Fischer, I.; Sapirstein, V.S. Molecular Cloning of Plasmolipin. Characterization of a Novel Proteolipid Restricted to Brain and Kidney. J. Biol. Chem. 1994, 269, 24912–24919. [Google Scholar] [CrossRef] [PubMed]
- Sapirstein, V.S.; Nolan, C.E.; Fischer, I.; Cochary, E.; Blau, S.; Flynn, C.J. The Phylogenic Expression of Plasmolipin in the Vertebrate Nervous System. Neurochem. Res. 1991, 16, 123–128. [Google Scholar] [CrossRef] [PubMed]
- Cochary, E.F.; Bizzozero, O.A.; Sapirstein, V.S.; Nolan, C.E.; Fischer, I. Presence of the Plasma Membrane Proteolipid (Plasmolipin) in Myelin. J. Neurochem. 1990, 55, 602–610. [Google Scholar] [CrossRef]
- Sapirstein, V.S.; Nolan, C.E.; Stern, R.; Gray-Board, G.; Beard, M.E. Identification of Plasmolipin as a Major Constituent of White Matter Clathrin-Coated Vesicles. J. Neurochem. 1992, 58, 1372–1378. [Google Scholar] [CrossRef]
- Sapirstein, V.S.; Nolan, C.; Stern, R.; Ciocci, M.; Masur, S.K. Identification of the Plasma Membrane Proteolipid Protein as a Constituent of Brain Coated Vesicles and Synaptic Plasma Membrane. J. Neurochem. 1988, 51, 925–933. [Google Scholar] [CrossRef]
- Zhang, S.; Pei, X.; Hu, H.; Zhang, W.; Mo, X.; Song, Q.; Zhang, Y.; Xu, K.; Wang, Y.; Na, Y. Functional Characterization of the Tumor Suppressor CMTM8 and Its Association with Prognosis in Bladder Cancer. Tumour Biol. 2016, 37, 6217–6225. [Google Scholar] [CrossRef]
- Sterner, R.C.; Sterner, R.M. CAR-T Cell Therapy: Current Limitations and Potential Strategies. Blood Cancer J. 2021, 11, 69. [Google Scholar] [CrossRef]
- Feins, S.; Kong, W.; Williams, E.F.; Milone, M.C.; Fraietta, J.A. An Introduction to Chimeric Antigen Receptor (CAR) T-cell Immunotherapy for Human Cancer. Am. J. Hematol. 2019, 94, S3–S9. [Google Scholar] [CrossRef]
- Xie, N.; Shen, G.; Gao, W.; Huang, Z.; Huang, C.; Fu, L. Neoantigens: Promising Targets for Cancer Therapy. Signal. Transduct. Target. Ther. 2023, 8, 9. [Google Scholar] [CrossRef]
- Zhang, Z.; Lu, M.; Qin, Y.; Gao, W.; Tao, L.; Su, W.; Zhong, J. Neoantigen: A New Breakthrough in Tumor Immunotherapy. Front. Immunol. 2021, 12, 672356. [Google Scholar] [CrossRef]
- Lee, C.-H.; Yelensky, R.; Jooss, K.; Chan, T.A. Update on Tumor Neoantigens and Their Utility: Why It Is Good to Be Different. Trends Immunol. 2018, 39, 536–548. [Google Scholar] [CrossRef]
Gene | Cancer | Prognosis 1 | p Value | Technique | References |
---|---|---|---|---|---|
MAL | COAD-READ | Favorable | <0.05 | DNA methyl | [124] |
cHL | Unfavorable | 0.002 | IHC | [157] | |
OV | Unfavorable | 0.0004 | IHC | [156] | |
STAD | Favorable | 0.03 | DNA methyl | [75] | |
STAD | Favorable | <0.05 | RT-qPCR | [76] | |
UCEC | Unfavorable | <0.05 | IHC | [152] | |
MAL2 | COAD-READ | Unfavorable | <0.001 | IHC | [102] |
PAAD | Unfavorable | 0.03 | IHC | [99] | |
MALL | COAD | Favorable | 0.008 | IHC | [113] |
CMTM8 | STAD | Favorable | <0.05 | IHC | [117] |
MYADML2 | LIHC | Unfavorable | 0.013 | IHC | [150] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Labat-de-Hoz, L.; Rubio-Ramos, A.; Correas, I.; Alonso, M.A. The MAL Family of Proteins: Normal Function, Expression in Cancer, and Potential Use as Cancer Biomarkers. Cancers 2023, 15, 2801. https://doi.org/10.3390/cancers15102801
Labat-de-Hoz L, Rubio-Ramos A, Correas I, Alonso MA. The MAL Family of Proteins: Normal Function, Expression in Cancer, and Potential Use as Cancer Biomarkers. Cancers. 2023; 15(10):2801. https://doi.org/10.3390/cancers15102801
Chicago/Turabian StyleLabat-de-Hoz, Leticia, Armando Rubio-Ramos, Isabel Correas, and Miguel A. Alonso. 2023. "The MAL Family of Proteins: Normal Function, Expression in Cancer, and Potential Use as Cancer Biomarkers" Cancers 15, no. 10: 2801. https://doi.org/10.3390/cancers15102801
APA StyleLabat-de-Hoz, L., Rubio-Ramos, A., Correas, I., & Alonso, M. A. (2023). The MAL Family of Proteins: Normal Function, Expression in Cancer, and Potential Use as Cancer Biomarkers. Cancers, 15(10), 2801. https://doi.org/10.3390/cancers15102801