Lipidomic-Based Advances in Diagnosis and Modulation of Immune Response to Cancer
Abstract
1. Introduction
2. Lipid Metabolism Impacts Immune Activation against Tumor Progression
2.1. Lipid Interplay with Immune Regulation
2.2. Short-Chain Fatty Acids from Gut Microbiota as Effectors of the Immune System
3. Lipids as Biomarkers of Immune Response to Cancer
4. Active Modulation of Lipid Metabolism to Improve CAR T Cell Therapy
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Watson, J.D.; Crick, F.H.C. Molecular Structure of Nucleic Acids: A Structure for Deoxyribose Nucleic Acid. Nature 1953, 171, 737–738. [Google Scholar] [CrossRef] [PubMed]
- Check Hayden, E. Technology: The $1,000 genome. Nature 2014, 507, 294–295. [Google Scholar] [CrossRef] [PubMed]
- Rattray, N.J.W.; Deziel, N.C.; Wallach, J.D.; Khan, S.A.; Vasiliou, V.; Ioannidis, J.P.A.; Johnson, C.H. Beyond genomics: Understanding exposotypes through metabolomics. Hum. Genom. 2018, 12, 4. [Google Scholar] [CrossRef] [PubMed]
- Romero, R.; Espinoza, J.; Gotsch, F.; Kusanovic, J.; Friel, L.; Erez, O.; Mazaki-Tovi, S.; Than, N.; Hassan, S.; Tromp, G. The use of high-dimensional biology (genomics, transcriptomics, proteomics, and metabolomics) to understand the preterm parturition syndrome. BJOG Int. J. Obstet. Gynaecol. 2006, 113, 118–135. [Google Scholar] [CrossRef]
- Lam, S.M.; Tian, H.; Shui, G. Lipidomics, en route to accurate quantitation. Biochim. Biophys. Acta (BBA) Mol. Cell Biol. Lipids 2017, 1862, 752–761. [Google Scholar] [CrossRef]
- Mancini, R.; Noto, A.; Pisanu, M.E.; De Vitis, C.; Maugeri-Saccà, M.; Ciliberto, G. Metabolic features of cancer stem cells: The emerging role of lipid metabolism. Oncogene 2018, 37, 2367–2378. [Google Scholar] [CrossRef]
- Mohamed, A.; Collins, J.; Jiang, H.; Molendijk, J.; Stoll, T.; Torta, F.; Wenk, M.R.; Bird, R.J.; Marlton, P.; Mollee, P.; et al. Concurrent lipidomics and proteomics on malignant plasma cells from multiple myeloma patients: Probing the lipid metabolome. PLoS ONE 2020, 15, e0227455. [Google Scholar] [CrossRef]
- Domblides, C.; Lartigue, L.; Faustin, B. Control of the Antitumor Immune Response by Cancer Metabolism. Cells 2019, 8, 104. [Google Scholar] [CrossRef]
- Hanahan, D.; Weinberg, R.A. Hallmarks of Cancer: The Next Generation. Cell 2011, 144, 646–674. [Google Scholar] [CrossRef]
- Krawczyk, C.M.; Holowka, T.; Sun, J.; Blagih, J.; Amiel, E.; DeBerardinis, R.J.; Cross, J.R.; Jung, E.; Thompson, C.B.; Jones, R.G.; et al. Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 2010, 115, 4742–4749. [Google Scholar] [CrossRef]
- Lauterbach, M.A.; Hanke, J.E.; Serefidou, M.; Mangan, M.S.J.; Kolbe, C.C.; Hess, T.; Rothe, M.; Kaiser, R.; Hoss, F.; Gehlen, J.; et al. Toll-like Receptor Signaling Rewires Macrophage Metabolism and Promotes Histone Acetylation via ATP-Citrate Lyase. Immunity 2019, 51, 997–1011. [Google Scholar] [CrossRef] [PubMed]
- Márquez, S.; Fernández, J.J.; Mancebo, C.; Herrero-Sánchez, C.; Alonso, S.; Sandoval, T.A.; Rodríguez Prados, M.; Cubillos-Ruiz, J.R.; Montero, O.; Fernández, N.; et al. Tricarboxylic Acid Cycle Activity and Remodeling of Glycerophosphocholine Lipids Support Cytokine Induction in Response to Fungal Patterns. Cell Rep. 2019, 27, 525–536. [Google Scholar] [CrossRef]
- Pardoll, D.M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 2012, 12, 252–264. [Google Scholar] [CrossRef] [PubMed]
- Brahmer, J.R.; Tykodi, S.S.; Chow, L.Q.M.; Hwu, W.J.; Topalian, S.L.; Hwu, P.; Drake, C.G.; Camacho, L.H.; Kauh, J.; Odunsi, K.; et al. Safety and Activity of Anti–PD-L1 Antibody in Patients with Advanced Cancer. New Engl. J. Med. 2012, 366, 2455–2465. [Google Scholar] [CrossRef]
- Donini, C.; D’Ambrosio, L.; Grignani, G.; Aglietta, M.; Sangiolo, D. Next generation immune-checkpoints for cancer therapy. J. Thorac. Dis. 2018, 10, S1581–S1601. [Google Scholar] [CrossRef]
- Patsoukis, N.; Bardhan, K.; Chatterjee, P.; Sari, D.; Liu, B.; Bell, L.N.; Karoly, E.D.; Freeman, G.J.; Petkova, V.; Seth, P.; et al. PD-1 alters T-cell metabolic reprogramming by inhibiting glycolysis and promoting lipolysis and fatty acid oxidation. Nat. Commun. 2015, 6, 6692. [Google Scholar] [CrossRef] [PubMed]
- Ogando, J.; Sáez, M.E.; Santos, J.; Nuevo-Tapioles, C.; Gut, M.; Esteve-Codina, A.; Heath, S.; González-Pérez, A.; Cuezva, J.M.; Lacalle, R.A.; et al. PD-1 signaling affects cristae morphology and leads to mitochondrial dysfunction in human CD8+ T lymphocytes. J. Immunother. Cancer 2019, 7, 151. [Google Scholar] [CrossRef] [PubMed]
- Varga, T.; Czimmerer, Z.; Nagy, L. PPARs are a unique set of fatty acid regulated transcription factors controlling both lipid metabolism and inflammation. Biochim. Biophys. Acta (BBA) Mol. Basis Dis. 2011, 1812, 1007–1022. [Google Scholar] [CrossRef]
- Cipolletta, D.; Feuerer, M.; Li, A.; Kamei, N.; Lee, J.; Shoelson, S.E.; Benoist, C.; Mathis, D. PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature 2012, 486, 549–553. [Google Scholar] [CrossRef]
- Zhao, Y.; Lee, C.K.; Lin, C.H.; Gassen, R.B.; Xu, X.; Huang, Z.; Xiao, C.; Bonorino, C.; Lu, L.F.; Bui, J.D.; et al. PD-L1:CD80 Cis-Heterodimer Triggers the Co-stimulatory Receptor CD28 While Repressing the Inhibitory PD-1 and CTLA-4 Pathways. Immunity 2019, 51, 1059–1073. [Google Scholar] [CrossRef]
- Chowdhury, P.S.; Chamoto, K.; Kumar, A.; Honjo, T. PPAR-Induced Fatty Acid Oxidation in T Cells Increases the Number of Tumor-Reactive CD8+ T Cells and Facilitates Anti-PD-1 Therapy. Cancer Immunol. Res. 2018, 6, 1375–1387. [Google Scholar] [CrossRef] [PubMed]
- Saibil, S.D.; St. Paul, M.; Laister, R.C.; Garcia-Batres, C.R.; Israni-Winger, K.; Elford, A.R.; Grimshaw, N.; Robert-Tissot, C.; Roy, D.G.; Jones, R.G.; et al. Activation of Peroxisome Proliferator-Activated Receptors α and δ Synergizes with Inflammatory Signals to Enhance Adoptive Cell Therapy. Cancer Res. 2019, 79, 445–451. [Google Scholar] [CrossRef] [PubMed]
- Gutiérrez, S.; Svahn, S.L.; Johansson, M.E. Effects of Omega-3 Fatty Acids on Immune Cells. Int. J. Mol. Sci. 2019, 20, 5028. [Google Scholar] [CrossRef] [PubMed]
- Mukaro, V.R.; Costabile, M.; Murphy, K.J.; Hii, C.S.; Howe, P.R.; Ferrante, A. Leukocyte numbers and function in subjects eating n-3 enriched foods: Selective depression of natural killer cell levels. Arthritis Res. Ther. 2008, 10, R57. [Google Scholar] [CrossRef]
- Miles, E.A.; Banerjee, T.; Wells, S.J.; Calder, P.C. Limited effect of eicosapentaenoic acid on T-lymphocyte and natural killer cell numbers and functions in healthy young males. Nutrition 2006, 22, 512–519. [Google Scholar] [CrossRef]
- Ichimura, A.; Hirasawa, A.; Poulain-Godefroy, O.; Bonnefond, A.; Hara, T.; Yengo, L.; Kimura, I.; Leloire, A.; Liu, N.; Iida, K.; et al. Dysfunction of lipid sensor GPR120 leads to obesity in both mouse and human. Nature 2012, 483, 350–354. [Google Scholar] [CrossRef]
- Liu, Z.; Hopkins, M.M.; Zhang, Z.; Quisenberry, C.B.; Fix, L.C.; Galvan, B.M.; Meier, K.E. Omega-3 fatty acids and other FFA4 agonists inhibit growth factor signaling in human prostate cancer cells. J. Pharmacol. Exp. Ther. 2015, 352, 380–394. [Google Scholar] [CrossRef]
- Thirunavukkarasan, M.; Wang, C.; Rao, A.; Hind, T.; Teo, Y.R.; Siddiquee, A.A.M.; Goghari, M.A.I.; Kumar, A.P.; Herr, D.R. Short-chain fatty acid receptors inhibit invasive phenotypes in breast cancer cells. PLoS ONE 2017, 12, e0186334. [Google Scholar] [CrossRef]
- Berod, L.; Friedrich, C.; Nandan, A.; Freitag, J.; Hagemann, S.; Harmrolfs, K.; Sandouk, A.; Hesse, C.; Castro, C.N.; Bähre, H.; et al. De novo fatty acid synthesis controls the fate between regulatory T and T helper 17 cells. Nat. Med. 2014, 20, 1327–1333. [Google Scholar] [CrossRef]
- Ecker, C.; Guo, L.; Voicu, S.; Gil-de-Gómez, L.; Medvec, A.; Cortina, L.; Pajda, J.; Andolina, M.; Torres-Castillo, M.; Donato, J.L.; et al. Differential Reliance on Lipid Metabolism as a Salvage Pathway Underlies Functional Differences of T Cell Subsets in Poor Nutrient Environments. Cell Rep. 2018, 23, 741–755. [Google Scholar] [CrossRef]
- Essig, K.; Hu, D.; Guimaraes, J.C.; Alterauge, D.; Edelmann, S.; Raj, T.; Kranich, J.; Behrens, G.; Heiseke, A.; Floess, S.; et al. Roquin Suppresses the PI3K-mTOR Signaling Pathway to Inhibit T Helper Cell Differentiation and Conversion of Treg to Tfr Cells. Immunity 2017, 47, 1067–1082. [Google Scholar] [CrossRef] [PubMed]
- Angelin, A.; Gil-de-Gómez, L.; Dahiya, S.; Jiao, J.; Guo, L.; Levine, M.H.; Wang, Z.; Quinn, W.J.; Kopinski, P.K.; Wang, L.; et al. Foxp3 Reprograms T Cell Metabolism to Function in Low-Glucose, High-Lactate Environments. Cell Metab. 2017, 25, 1282–1293. [Google Scholar] [CrossRef] [PubMed]
- Miska, J.; Lee-Chang, C.; Rashidi, A.; Muroski, M.E.; Chang, A.L.; Lopez-Rosas, A.; Zhang, P.; Panek, W.K.; Cordero, A.; Han, Y.; et al. HIF-1α Is a Metabolic Switch between Glycolytic-Driven Migration and Oxidative Phosphorylation-Driven Immunosuppression of Tregs in Glioblastoma. Cell Rep. 2019, 27, 226–237. [Google Scholar] [CrossRef] [PubMed]
- Mizuno, R.; Kawada, K.; Sakai, Y. Prostaglandin E2/EP Signaling in the Tumor Microenvironment of Colorectal Cancer. Int. J. Mol. Sci. 2019, 20, 6254. [Google Scholar] [CrossRef]
- Gil-de-Gómez, L.; Astudillo, A.M.; Lebrero, P.; Balboa, M.A.; Balsinde, J. Essential Role for Ethanolamine Plasmalogen Hydrolysis in Bacterial Lipopolysaccharide Priming of Macrophages for Enhanced Arachidonic Acid Release. Front. Immunol. 2017, 8, 1251. [Google Scholar] [CrossRef]
- Li, J.; Feng, G.; Liu, J.; Rong, R.; Luo, F.; Guo, L.; Zhu, T.; Wang, G.; Chu, Y. Renal cell carcinoma may evade the immune system by converting CD4+Foxp3- T cells into CD4+CD25+Foxp3+ regulatory T cells: Role of tumor COX-2-derived PGE2. Mol. Med. Rep. 2010, 3, 959–963. [Google Scholar] [CrossRef]
- Kalinski, P. Regulation of Immune Responses by Prostaglandin E2. J. Immunol. 2012, 188, 21–28. [Google Scholar] [CrossRef]
- Trinath, J.; Hegde, P.; Sharma, M.; Maddur, M.S.; Rabin, M.; Vallat, J.M.; Magy, L.; Balaji, K.N.; Kaveri, S.V.; Bayry, J. Intravenous immunoglobulin expands regulatory T cells via induction of cyclooxygenase-2–dependent prostaglandin E2 in human dendritic cells. Blood 2013, 122, 1419–1427. [Google Scholar] [CrossRef]
- Loew, A.; Köhnke, T.; Rehbeil, E.; Pietzner, A.; Weylandt, K.H. A Role for Lipid Mediators in Acute Myeloid Leukemia. Int. J. Mol. Sci. 2019, 20, 2425. [Google Scholar] [CrossRef]
- Prima, V.; Kaliberova, L.N.; Kaliberov, S.; Curiel, D.T.; Kusmartsev, S. COX2/mPGES1/PGE 2 pathway regulates PD-L1 expression in tumor-associated macrophages and myeloid-derived suppressor cells. Proc. Natl. Acad. Sci. USA 2017, 114, 1117–1122. [Google Scholar] [CrossRef]
- Miao, J.; Lu, X.; Hu, Y.; Piao, C.; Wu, X.; Liu, X.; Huang, C.; Wang, Y.; Li, D.; Liu, J. Prostaglandin E2 and PD-1 mediated inhibition of antitumor CTL responses in the human tumor microenvironment. Oncotarget 2017, 8, 89802–89810. [Google Scholar] [CrossRef] [PubMed]
- Mock, A.; Zschäbitz, S.; Kirsten, R.; Scheffler, M.; Wolf, B.; Herold-Mende, C.; Kramer, R.; Busch, E.; Jenzer, M.; Jäger, D.; et al. Serum very long-chain fatty acid-containing lipids predict response to immune checkpoint inhibitors in urological cancers. Cancer Immunol. Immunother. 2019, 68, 2005–2014. [Google Scholar] [CrossRef] [PubMed]
- Wu, A.; Wu, Q.; Deng, Y.; Liu, Y.; Lu, J.; Liu, L.; Li, X.; Liao, C.; Zhao, B.; Song, H. Loss of VGLL4 Suppresses Tumor PD-L1 Expression and Immune Evasion. EMBO J. 2019, 38. [Google Scholar] [CrossRef] [PubMed]
- Huang, S.C.C.; Everts, B.; Ivanova, Y.; O’Sullivan, D.; Nascimento, M.; Smith, A.M.; Beatty, W.; Love-Gregory, L.; Lam, W.Y.; O’Neill, C.M.; et al. Cell-intrinsic lysosomal lipolysis is essential for alternative activation of macrophages. Nat. Immunol. 2014, 15, 846–855. [Google Scholar] [CrossRef] [PubMed]
- Oishi, Y.; Spann, N.J.; Link, V.M.; Muse, E.D.; Strid, T.; Edillor, C.; Kolar, M.J.; Matsuzaka, T.; Hayakawa, S.; Tao, J.; et al. SREBP1 Contributes to Resolution of Pro-inflammatory TLR4 Signaling by Reprogramming Fatty Acid Metabolism. Cell Metab. 2017, 25, 412–427. [Google Scholar] [CrossRef] [PubMed]
- Griffiths, B.; Lewis, C.A.; Bensaad, K.; Ros, S.; Zhang, Q.; Ferber, E.C.; Konisti, S.; Peck, B.; Miess, H.; East, P.; et al. Sterol regulatory element binding protein-dependent regulation of lipid synthesis supports cell survival and tumor growth. Cancer Metab. 2013, 1, 3. [Google Scholar] [CrossRef] [PubMed]
- Liu, C.; Chikina, M.; Deshpande, R.; Menk, A.V.; Wang, T.; Tabib, T.; Brunazzi, E.A.; Vignali, K.M.; Sun, M.; Stolz, D.B.; et al. Treg Cells Promote the SREBP1-Dependent Metabolic Fitness of Tumor-Promoting Macrophages via Repression of CD8+ T Cell-Derived Interferon-γ. Immunity 2019, 51, 381–397. [Google Scholar] [CrossRef] [PubMed]
- Wu, S.; Näär, A.M. SREBP1-dependent de novo fatty acid synthesis gene expression is elevated in malignant melanoma and represents a cellular survival trait. Sci. Rep. 2019, 9, 10369. [Google Scholar] [CrossRef] [PubMed]
- Li, L.; Hua, L.; Fan, H.; He, Y.; Xu, W.; Zhang, L.; Yang, J.; Deng, F.; Zeng, F. Interplay of PKD3 with SREBP1 Promotes Cell Growth via Upregulating Lipogenesis in Prostate Cancer Cells. J. Cancer 2019, 10, 6395–6404. [Google Scholar] [CrossRef]
- Wang, B.; Tontonoz, P. Liver X receptors in lipid signalling and membrane homeostasis. Nat. Rev. Endocrinol. 2018, 14, 452–463. [Google Scholar] [CrossRef]
- Shimano, H.; Sato, R. SREBP-regulated lipid metabolism: Convergent physiology–divergent pathophysiology. Nat. Rev. Endocrinol. 2017, 13, 710–730. [Google Scholar] [CrossRef] [PubMed]
- Costales, P.; Castellano, J.; Revuelta-López, E.; Cal, R.; Aledo, R.; Llampayas, O.; Nasarre, L.; Juarez, C.; Badimon, L.; Llorente-Cortés, V. Lipopolysaccharide downregulates CD91/low-density lipoprotein receptor-related protein 1 expression through SREBP-1 overexpression in human macrophages. Atherosclerosis 2013, 227, 79–88. [Google Scholar] [CrossRef] [PubMed]
- Im, S.S.; Yousef, L.; Blaschitz, C.; Liu, J.Z.; Edwards, R.A.; Young, S.G.; Raffatellu, M.; Osborne, T.F. Linking Lipid Metabolism to the Innate Immune Response in Macrophages through Sterol Regulatory Element Binding Protein-1a. Cell Metab. 2011, 13, 540–549. [Google Scholar] [CrossRef]
- Joseph, S.B.; Castrillo, A.; Laffitte, B.A.; Mangelsdorf, D.J.; Tontonoz, P. Reciprocal regulation of inflammation and lipid metabolism by liver X receptors. Nat. Med. 2003, 9, 213–219. [Google Scholar] [CrossRef] [PubMed]
- Chausse, B.; Kakimoto, P.A.; Caldeira-Da-Silva, C.C.; Chaves-Filho, A.B.; Yoshinaga, M.Y.; Da Silva, R.P.; Miyamoto, S.; Kowaltowski, A.J. Distinct metabolic patterns during microglial remodeling by oleate and palmitate. Biosci. Rep. 2019, 39. [Google Scholar] [CrossRef] [PubMed]
- Oh, Y.T.; Lee, J.Y.; Lee, J.; Kim, H.; Yoon, K.S.; Choe, W.; Kang, I. Oleic acid reduces lipopolysaccharide-induced expression of iNOS and COX-2 in BV2 murine microglial cells: Possible involvement of reactive oxygen species, p38 MAPK, and IKK/NF-κB signaling pathways. Neurosci. Lett. 2009, 464, 93–97. [Google Scholar] [CrossRef] [PubMed]
- Krycer, J.R.; Brown, A.J. Cross-talk between the androgen receptor and the liver X receptor: Implications for cholesterol homeostasis. J. Biol. Chem. 2011, 286, 20637–20647. [Google Scholar] [CrossRef]
- Balgoma, D.; Zelleroth, S.; Grönbladh, A.; Hallberg, M.; Pettersson, C.; Hedeland, M. Anabolic androgenic steroids exert a selective remodeling of the plasma lipidome that mirrors the decrease of the de novo lipogenesis in the liver. Metabolomics 2020, 16, 12. [Google Scholar] [CrossRef]
- Zhu, P.; Baek, S.H.; Bourk, E.M.; Ohgi, K.A.; Garcia-Bassets, I.; Sanjo, H.; Akira, S.; Kotol, P.F.; Glass, C.K.; Rosenfeld, M.G.; et al. Macrophage/Cancer Cell Interactions Mediate Hormone Resistance by a Nuclear Receptor Derepression Pathway. Cell 2006, 124, 615–629. [Google Scholar] [CrossRef]
- Perucha, E.; Melchiotti, R.; Bibby, J.A.; Wu, W.; Frederiksen, K.S.; Roberts, C.A.; Hall, Z.; LeFriec, G.; Robertson, K.A.; Lavender, P.; et al. The cholesterol biosynthesis pathway regulates IL-10 expression in human Th1 cells. Nat. Commun. 2019, 10, 498. [Google Scholar] [CrossRef]
- Rodrigues, N.V.; Correia, D.V.; Mensurado, S.; Nóbrega-Pereira, S.; DeBarros, A.; Kyle-Cezar, F.; Tutt, A.; Hayday, A.C.; Norell, H.; Silva-Santos, B.; et al. Low-Density Lipoprotein Uptake Inhibits the Activation and Antitumor Functions of Human Vγ9Vδ2 T Cells. Cancer Immunol. Res. 2018, 6, 448–457. [Google Scholar] [CrossRef] [PubMed]
- Chaudhary, J.; Bower, J.; Corbin, I.R. Lipoprotein Drug Delivery Vehicles for Cancer: Rationale and Reason. Int. J. Mol. Sci. 2019, 20, 6327. [Google Scholar] [CrossRef] [PubMed]
- Yao, H.; Lan, J.; Li, C.; Shi, H.; Brosseau, J.P.; Wang, H.; Lu, H.; Fang, C.; Zhang, Y.; Liang, L.; et al. Inhibiting PD-L1 palmitoylation enhances T-cell immune responses against tumours. Nat. Biomed. Eng. 2019, 3, 306–317. [Google Scholar] [CrossRef] [PubMed]
- Sharma, C.; Wang, H.X.; Li, Q.; Knoblich, K.; Reisenbichler, E.S.; Richardson, A.L.; Hemler, M.E. Protein Acyltransferase DHHC3 Regulates Breast Tumor Growth, Oxidative Stress, and Senescence. Cancer Res. 2017, 77, 6880–6890. [Google Scholar] [CrossRef] [PubMed]
- Louis, P.; Flint, H.J. Formation of propionate and butyrate by the human colonic microbiota. Environ. Microbiol. 2017, 19, 29–41. [Google Scholar] [CrossRef]
- Kim, C.H. Immune regulation by microbiome metabolites. Immunology 2018, 154, 220–229. [Google Scholar] [CrossRef]
- Botticelli, A.; Vernocchi, P.; Marini, F.; Quagliariello, A.; Cerbelli, B.; Reddel, S.; Del Chierico, F.; Di Pietro, F.; Giusti, R.; Tomassini, A.; et al. Gut metabolomics profiling of non-small cell lung cancer (NSCLC) patients under immunotherapy treatment. J. Transl. Med. 2020, 18, 49. [Google Scholar] [CrossRef]
- Belcheva, A.; Irrazabal, T.; Robertson, S.J.; Streutker, C.; Maughan, H.; Rubino, S.; Moriyama, E.H.; Copeland, J.K.; Surendra, A.; Kumar, S.; et al. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell 2014, 158, 288–299. [Google Scholar] [CrossRef]
- Ruemmele, F.M. Butyrate induced Caco-2 cell apoptosis is mediated via the mitochondrial pathway. Gut 2003, 52, 94–100. [Google Scholar] [CrossRef]
- Singh, N.; Gurav, A.; Sivaprakasam, S.; Brady, E.; Padia, R.; Shi, H.; Thangaraju, M.; Prasad, P.D.; Manicassamy, S.; Munn, D.H.; et al. Activation of Gpr109a, Receptor for Niacin and the Commensal Metabolite Butyrate, Suppresses Colonic Inflammation and Carcinogenesis. Immunity 2014, 40, 128–139. [Google Scholar] [CrossRef]
- Park, J.; Kim, M.; Kang, S.G.; Jannasch, A.H.; Cooper, B.; Patterson, J.; Kim, C.H. Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR–S6K pathway. Mucosal Immunol. 2015, 8, 80–93. [Google Scholar] [CrossRef] [PubMed]
- Bilotta, A.J.; Cong, Y. Gut microbiota metabolite regulation of host defenses at mucosal surfaces: Implication in precision medicine. Precis. Clin. Med. 2019, 2, 110–119. [Google Scholar] [CrossRef]
- Bachem, A.; Makhlouf, C.; Binger, K.J.; De Souza, D.P.; Tull, D.; Hochheiser, K.; Whitney, P.G.; Fernandez-Ruiz, D.; Dähling, S.; Kastenmüller, W.; et al. Microbiota-Derived Short-Chain Fatty Acids Promote the Memory Potential of Antigen-Activated CD8+ T Cells. Immunity 2019, 51, 285–297. [Google Scholar] [CrossRef] [PubMed]
- O’Sullivan, D.; Van Der Windt, G.J.W.; Huang, S.C.C.; Curtis, J.D.; Chang, C.H.; Buck, M.D.; Qiu, J.; Smith, A.M.; Lam, W.Y.; DiPlato, L.M.; et al. Memory CD8+ T Cells Use Cell-Intrinsic Lipolysis to Support the Metabolic Programming Necessary for Development. Immunity 2014, 41, 75–88. [Google Scholar] [CrossRef] [PubMed]
- Van Der Windt, G.J.W.; Everts, B.; Chang, C.H.; Curtis, J.D.; Freitas, T.C.; Amiel, E.; Pearce, E.J.; Pearce, E.L. Mitochondrial Respiratory Capacity Is a Critical Regulator of CD8+ T Cell Memory Development. Immunity 2012, 36, 68–78. [Google Scholar] [CrossRef] [PubMed]
- Nastasi, C.; Candela, M.; Bonefeld, C.M.; Geisler, C.; Hansen, M.; Krejsgaard, T.; Biagi, E.; Andersen, M.H.; Brigidi, P.; Ødum, N.; et al. The effect of short-chain fatty acids on human monocyte-derived dendritic cells. Sci. Rep. 2015, 5, 16148. [Google Scholar] [CrossRef]
- Nastasi, C.; Fredholm, S.; Willerslev-Olsen, A.; Hansen, M.; Bonefeld, C.M.; Geisler, C.; Andersen, M.H.; Ødum, N.; Woetmann, A. Butyrate and propionate inhibit antigen-specific CD8+ T cell activation by suppressing IL-12 production by antigen-presenting cells. Sci. Rep. 2017, 7, 14516. [Google Scholar] [CrossRef]
- Coutzac, C.; Jouniaux, J.-M.; Paci, A.; Schmidt, J.; Mallardo, D.; Seck, A.; Asvatourian, V.; Cassard, L.; Saulnier, P.; Lacroix, L.; et al. Systemic short chain fatty acids limit antitumor effect of CTLA-4 blockade in hosts with cancer. Nat. Commun. 2020, 11, 2168. [Google Scholar] [CrossRef]
- Zhang, W.Q.; Zhao, S.K.; Luo, J.W.; Dong, X.P.; Hao, Y.T.; Li, H.; Shan, L.; Zhou, Y.; Shi, H.B.; Zhang, Z.Y.; et al. Alterations of fecal bacterial communities in patients with lung cancer. Am. J. Transl. Res. 2018, 10, 3171–3185. [Google Scholar]
- Sivan, A.; Corrales, L.; Hubert, N.; Williams, J.B.; Aquino-Michaels, K.; Earley, Z.M.; Benyamin, F.W.; Man Lei, Y.; Jabri, B.; Alegre, M.L.; et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 2015, 350, 1084–1089. [Google Scholar] [CrossRef]
- Chalmin, F.; Bruchard, M.; Vegran, F.; Ghiringhelli, F. Regulation of T cell antitumor immune response by tumor induced metabolic stress. Cell Stress 2019, 3, 9–18. [Google Scholar] [CrossRef] [PubMed]
- Michalek, R.D.; Gerriets, V.A.; Jacobs, S.R.; Macintyre, A.N.; MacIver, N.J.; Mason, E.F.; Sullivan, S.A.; Nichols, A.G.; Rathmell, J.C. Cutting Edge: Distinct Glycolytic and Lipid Oxidative Metabolic Programs Are Essential for Effector and Regulatory CD4 + T Cell Subsets. J. Immunol. 2011, 186, 3299–3303. [Google Scholar] [CrossRef] [PubMed]
- Santaren, I.D.; Bazinet, R.P.; Liu, Z.; Johnston, L.W.; Sievenpiper, J.L.; Giacca, A.; Retnakaran, R.; Harris, S.B.; Zinman, B.; Hanley, A.J. The Distribution of Fatty Acid Biomarkers of Dairy Intake across Serum Lipid Fractions: The Prospective Metabolism and Islet Cell Evaluation (PROMISE) Cohort. Lipids 2019, 54, 617–627. [Google Scholar] [CrossRef] [PubMed]
- Olazarán, J.; Gil-de-Gómez, L.; Rodríguez-Martín, A.; Valentí-Soler, M.; Frades-Payo, B.; Marín-Muñoz, J.; Antúnez, C.; Frank-García, A.; Acedo-Jiménez, C.; Morlán-Gracia, L.; et al. A Blood-Based, 7-Metabolite Signature for the Early Diagnosis of Alzheimer’s Disease. J. Alzheimer’s Dis. 2015, 45, 1157–1173. [Google Scholar] [CrossRef] [PubMed]
- Stuani, L.; Riols, F.; Millard, P.; Sabatier, M.; Batut, A.; Saland, E.; Viars, F.; Tonini, L.; Zaghdoudi, S.; Linares, L.; et al. Stable Isotope Labeling Highlights Enhanced Fatty Acid and Lipid Metabolism in Human Acute Myeloid Leukemia. Int. J. Mol. Sci. 2018, 19, 3325. [Google Scholar] [CrossRef] [PubMed]
- Pabst, T.; Kortz, L.; Fiedler, G.M.; Ceglarek, U.; Idle, J.R.; Beyoğlu, D. The plasma lipidome in acute myeloid leukemia at diagnosis in relation to clinical disease features. BBA Clin. 2017, 7, 105–114. [Google Scholar] [CrossRef]
- Stefanko, A.; Thiede, C.; Ehninger, G.; Simons, K.; Grzybek, M. Lipidomic approach for stratification of acute myeloid leukemia patients. PLoS ONE 2017, 12, e0168781. [Google Scholar] [CrossRef]
- Lavoie, J.M.; Black, P.C.; Eigl, B.J. Predictive Biomarkers for Checkpoint Blockade in Urothelial Cancer: A Systematic Review. J. Urol. 2019, 202, 49–56. [Google Scholar] [CrossRef]
- Wang, B.; Tontonoz, P. Phospholipid Remodeling in Physiology and Disease. Annu. Rev. Physiol. 2019, 81, 165–188. [Google Scholar] [CrossRef]
- Yang, L.; Bai, Y.; Han, X.; Shi, Y.; Liu, H. Plasma Lipidomic Analysis to Identify Novel Biomarkers for Hepatocellular Carcinoma. J. Anal. Test. 2017, 1, 223–232. [Google Scholar] [CrossRef]
- Lee, J.W.; Mok, H.J.; Lee, D.Y.; Park, S.C.; Kim, G.S.; Lee, S.E.; Lee, Y.S.; Kim, K.P.; Kim, H.D. UPLC-QqQ/MS-Based Lipidomics Approach To Characterize Lipid Alterations in Inflammatory Macrophages. J. Proteome Res. 2017, 16, 1460–1469. [Google Scholar] [CrossRef]
- Balgoma, D.; Pettersson, C.; Hedeland, M. Common Fatty Markers in Diseases with Dysregulated Lipogenesis. Trends Endocrinol. Metab. 2019, 30, 283–285. [Google Scholar] [CrossRef] [PubMed]
- Balgoma, D.; Guitton, Y.; Evans, J.J.; Le Bizec, B.; Dervilly-Pinel, G.; Meynier, A. Modeling the fragmentation patterns of triacylglycerides in mass spectrometry allows the quantification of the regioisomers with a minimal number of standards. Anal. Chim. Acta 2019, 1057, 60–69. [Google Scholar] [CrossRef] [PubMed]
- O’Keefe, S.J.D.; Ou, J.; Aufreiter, S.; O’Connor, D.; Sharma, S.; Sepulveda, J.; Fukuwatari, T.; Shibata, K.; Mawhinney, T. Products of the colonic microbiota mediate the effects of diet on colon cancer risk. J. Nutr. 2009, 139, 2044–2048. [Google Scholar] [CrossRef] [PubMed]
- Chen, H.M.; Yu, Y.N.; Wang, J.L.; Lin, Y.W.; Kong, X.; Yang, C.Q.; Yang, L.; Liu, Z.J.; Yuan, Y.Z.; Liu, F.; et al. Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma. Am. J. Clin. Nutr. 2013, 97, 1044–1052. [Google Scholar] [CrossRef] [PubMed]
- Uribe-Herranz, M.; Rafail, S.; Beghi, S.; Gil-de-Gómez, L.; Verginadis, I.; Bittinger, K.; Pustylnikov, S.; Pierini, S.; Perales-Linares, R.; Blair, I.A.; et al. Gut microbiota modulate dendritic cell antigen presentation and radiotherapy-induced antitumor immune response. J. Clin. Investig. 2020, 130, 466–479. [Google Scholar] [CrossRef]
- Matson, V.; Fessler, J.; Bao, R.; Chongsuwat, T.; Zha, Y.; Alegre, M.L.; Luke, J.J.; Gajewski, T.F. The commensal microbiome is associated with anti–PD-1 efficacy in metastatic melanoma patients. Science 2018, 359, 104–108. [Google Scholar] [CrossRef]
- Milone, M.C.; Fish, J.D.; Carpenito, C.; Carroll, R.G.; Binder, G.K.; Teachey, D.; Samanta, M.; Lakhal, M.; Gloss, B.; Danet-Desnoyers, G.; et al. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol. Ther. 2009, 17, 1453–1464. [Google Scholar] [CrossRef]
- George, P.; Dasyam, N.; Giunti, G.; Mester, B.; Bauer, E.; Andrews, B.; Perera, T.; Ostapowicz, T.; Frampton, C.; Li, P.; et al. Third-generation anti-CD19 chimeric antigen receptor T-cells incorporating a TLR2 domain for relapsed or refractory B-cell lymphoma: A phase I clinical trial protocol (ENABLE). BMJ Open 2020, 10, e034629. [Google Scholar] [CrossRef]
- June, C.H.; O’Connor, R.S.; Kawalekar, O.U.; Ghassemi, S.; Milone, M.C. CAR T cell immunotherapy for human cancer. Science 2018, 359, 1361–1365. [Google Scholar] [CrossRef]
- Wang, D.; Starr, R.; Chang, W.C.; Aguilar, B.; Alizadeh, D.; Wright, S.L.; Yang, X.; Brito, A.; Sarkissian, A.; Ostberg, J.R.; et al. Chlorotoxin-directed CAR T cells for specific and effective targeting of glioblastoma. Sci. Transl. Med. 2020, 12. [Google Scholar] [CrossRef] [PubMed]
- Schulz, G.; Cheresh, D.A.; Varki, N.M.; Yu, A.; Staffileno, L.K.; Reisfeld, R.A. Detection of ganglioside GD2 in tumor tissues and sera of neuroblastoma patients. Cancer Res. 1984, 44, 5914–5920. [Google Scholar] [PubMed]
- Dobrenkov, K.; Ostrovnaya, I.; Gu, J.; Cheung, I.Y.; Cheung, N.K.V. Oncotargets GD2 and GD3 are highly expressed in sarcomas of children, adolescents, and young adults. Pediatric Blood Cancer 2016, 63, 1780–1785. [Google Scholar] [CrossRef] [PubMed]
- Richman, S.A.; Nunez-Cruz, S.; Moghimi, B.; Li, L.Z.; Gershenson, Z.T.; Mourelatos, Z.; Barrett, D.M.; Grupp, S.A.; Milone, M.C. High-Affinity GD2-Specific CAR T Cells Induce Fatal Encephalitis in a Preclinical Neuroblastoma Model. Cancer Immunol. Res. 2018, 6, 36–46. [Google Scholar] [CrossRef]
- Tasian, S.K.; Loh, M.L.; Hunger, S.P. Philadelphia chromosome–like acute lymphoblastic leukemia. Blood 2017, 130, 2064–2072. [Google Scholar] [CrossRef]
- Finney, O.C.; Brakke, H.; Rawlings-Rhea, S.; Hicks, R.; Doolittle, D.; Lopez, M.; Futrell, B.; Orentas, R.J.; Li, D.; Gardner, R.; et al. CD19 CAR T cell product and disease attributes predict leukemia remission durability. J. Clin. Investig. 2019, 129, 2123–2132. [Google Scholar] [CrossRef]
- Konjar, Š.; Veldhoen, M. Dynamic Metabolic State of Tissue Resident CD8 T Cells. Front. Immunol. 2019, 10, 1683. [Google Scholar] [CrossRef]
- Kondo, T.; Ando, M.; Nagai, N.; Tomisato, W.; Srirat, T.; Liu, B.; Mise-Omata, S.; Ikeda, M.; Chikuma, S.; Nishimasu, H.; et al. The NOTCH–FOXM1 Axis Plays a Key Role in Mitochondrial Biogenesis in the Induction of Human Stem Cell Memory–like CAR-T Cells. Cancer Res. 2020, 80, 471–483. [Google Scholar] [CrossRef]
- Martinez, M.; Moon, E.K. CAR T Cells for Solid Tumors: New Strategies for Finding, Infiltrating, and Surviving in the Tumor Microenvironment. Front. Immunol. 2019, 10, 128. [Google Scholar] [CrossRef]
- Fucà, G.; Reppel, L.; Landoni, E.; Savoldo, B.; Dotti, G. Enhancing Chimeric Antigen Receptor T-Cell Efficacy in Solid Tumors. Clin. Cancer Res. 2020, 26, 2444–2451. [Google Scholar] [CrossRef]
- Vartak, S.; Robbins, M.E.C.; Spector, A.A. Polyunsaturated fatty acids increase the sensitivity of 36B10 rat astrocytoma cells to radiation-induced cell kill. Lipids 1997, 32, 283–292. [Google Scholar] [CrossRef] [PubMed]
- Das, U.N. Gamma-linolenic acid therapy of human glioma-a review of in vitro, in vivo, and clinical studies. Med. Sci. Monit. 2007, 13, RA119–RA131. [Google Scholar] [PubMed]
- Belavgeni, A.; Bornstein, S.R.; Von Mässenhausen, A.; Tonnus, W.; Stumpf, J.; Meyer, C.; Othmar, E.; Latk, M.; Kanczkowski, W.; Kroiss, M.; et al. Exquisite sensitivity of adrenocortical carcinomas to induction of ferroptosis. Proc. Natl. Acad. Sci. USA 2019, 116, 22269–22274. [Google Scholar] [CrossRef] [PubMed]
- Das, U.N. Can Bioactive Lipids Augment Anti-cancer Action of Immunotherapy and Prevent Cytokine Storm? Arch. Med. Res. 2019, 50, 342–349. [Google Scholar] [CrossRef]
- Van Bruggen, J.A.C.; Martens, A.W.J.; Fraietta, J.A.; Hofland, T.; Tonino, S.H.; Eldering, E.; Levin, M.D.; Siska, P.J.; Endstra, S.; Rathmell, J.C.; et al. Chronic lymphocytic leukemia cells impair mitochondrial fitness in CD8+ T cells and impede CAR T-cell efficacy. Blood 2019, 134, 44–58. [Google Scholar] [CrossRef]
© 2020 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 (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Gil-de-Gómez, L.; Balgoma, D.; Montero, O. Lipidomic-Based Advances in Diagnosis and Modulation of Immune Response to Cancer. Metabolites 2020, 10, 332. https://doi.org/10.3390/metabo10080332
Gil-de-Gómez L, Balgoma D, Montero O. Lipidomic-Based Advances in Diagnosis and Modulation of Immune Response to Cancer. Metabolites. 2020; 10(8):332. https://doi.org/10.3390/metabo10080332
Chicago/Turabian StyleGil-de-Gómez, Luis, David Balgoma, and Olimpio Montero. 2020. "Lipidomic-Based Advances in Diagnosis and Modulation of Immune Response to Cancer" Metabolites 10, no. 8: 332. https://doi.org/10.3390/metabo10080332
APA StyleGil-de-Gómez, L., Balgoma, D., & Montero, O. (2020). Lipidomic-Based Advances in Diagnosis and Modulation of Immune Response to Cancer. Metabolites, 10(8), 332. https://doi.org/10.3390/metabo10080332