Relationship between Tumor Budding and Partial Epithelial–Mesenchymal Transition in Head and Neck Cancer
Abstract
Simple Summary
Abstract
1. Introduction
2. EMT Status and Stemness on TB in HNSCC
3. Evidence of p-EMT
4. Plasticity and EMT
5. Immunity Relating to TB Formation
6. Representative Drivers for TB Development and p-EMT Induction
6.1. Hypoxia
6.2. CAFs
6.3. Tumor-Associated Macrophages (TAMs)
6.4. Laminin-5γ2 (LN-5γ2) and Integrin β1
6.5. Fusobacterium nucleatum (F. nucleatum)
6.6. Human Papilloma Virus (HPV) Status
6.7. Methylthioadenosine Phosphorylase (MTAP)
7. Conclusions and Future Perspective
Author Contributions
Funding
Conflicts of Interest
References
- Ueno, H.; Murphy, J.; Jass, J.R.; Mochizuki, H.; Talbot, I.C. Tumourbudding’as an index to estimate the potential of aggressiveness in rectal cancer. Histopathology 2002, 40, 127–132. [Google Scholar] [CrossRef] [PubMed]
- Almangush, A.; Pirinen, M.; Heikkinen, I.; Mäkitie, A.A.; Salo, T.; Leivo, I. Tumour budding in oral squamous cell carcinoma: A meta-analysis. Br. J. Cancer 2018, 118, 577–586. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.; Liu, H.; Xie, N.; Liu, X.; Huang, H.; Wang, C.; Hou, J. Impact of tumor budding in head and neck squamous cell carcinoma: A meta-analysis. Head Neck 2019, 41, 542–550. [Google Scholar] [CrossRef] [PubMed]
- Okuyama, K.; Fukushima, H.; Naruse, T.; Yanamoto, S.; Tsuchihashi, H.; Umeda, M. CD44 Variant 6 Expression and Tumor Budding in the Medullary Invasion Front of Mandibular Gingival Squamous Cell Carcinoma Are Predictive Factors for Cervical Lymph Node Metastasis. Pathol. Oncol. Res. 2019, 25, 603–609. [Google Scholar] [CrossRef] [PubMed]
- Attramadal, C.G.; Kumar, S.; Boysen, M.E.; Dhakal, H.P.; Nesland, J.M.; Bryne, M. Tumor Budding, EMT and Cancer Stem Cells in T1-2/N0 Oral Squamous Cell Carcinomas. Anticancer Res. 2015, 35, 6111–6120. [Google Scholar]
- Dolens, E.D.S.; Dourado, M.R.; Almangush, A.; Salo, T.A.; Gurgel Rocha, C.A.; da Silva, S.D.; Brennan, P.A.; Coletta, R.D. The Impact of Histopathological Features on the Prognosis of Oral Squamous Cell Carcinoma: A Comprehensive Review and Meta-Analysis. Front. Oncol. 2021, 11, 784924. [Google Scholar] [CrossRef]
- Karjol, U.; Jonnada, P.; Annavarjula, V.; Cherukuru, S.; Chandranath, A.; Anwar, A. Prognostic Role of Tumor Budding in Carcinoma Tongue: A Systemic Review and Meta-Analysis. Cureus 2020, 12, e9316. [Google Scholar] [CrossRef]
- Lugli, A.; Karamitopoulou, E.; Zlobec, I. Tumour budding: A promising parameter in colorectal cancer. Br. J. Cancer 2012, 106, 1713–1717. [Google Scholar] [CrossRef]
- Rogers, A.C.; Winter, D.C.; Heeney, A.; Gibbons, D.; Lugli, A.; Puppa, G.; Sheahan, K. Systematic review and meta-analysis of the impact of tumour budding in colorectal cancer. Br. J. Cancer 2016, 115, 831–840. [Google Scholar] [CrossRef]
- Beaton, C.; Twine, C.P.; Williams, G.L.; Radcliffe, A.G. Systematic review and meta-analysis of histopathological factors influencing the risk of lymph node metastasis in early colorectal cancer. Color. Dis. 2013, 15, 788–797. [Google Scholar] [CrossRef]
- Niwa, Y.; Yamada, S.; Koike, M.; Kanda, M.; Fujii, T.; Nakayama, G.; Sugimoto, H.; Nomoto, S.; Fujiwara, M.; Kodera, Y. Epithelial to Mesenchymal Transition Correlates with Tumor Budding and Predicts Prognosis in Esophageal Squamous Cell Carcinoma. J. Surg. Oncol. 2014, 110, 764–769. [Google Scholar] [CrossRef]
- Brown, M.; Sillah, K.; Griffiths, E.A.; Swindell, R.; West, C.M.; Page, R.D.; Welch, I.M.; Pritchard, S.A. Tumour budding and a low host inflammatory response are associated with a poor prognosis in oesophageal and gastro-oesophageal junction cancers. Histopathology 2010, 56, 893–899. [Google Scholar] [CrossRef]
- Koelzer, V.H.; Langer, R.; Zlobec, I.; Lugli, A. Tumor budding in upper gastrointestinal carcinomas. Front. Oncol. 2014, 4, 216. [Google Scholar] [CrossRef]
- Xiang, Z.; He, Q.; Huang, L.; Xiong, B.; Xiang, Q. Breast Cancer Classification Based on Tumor Budding and Stem Cell-Related Signatures Facilitate Prognosis Evaluation. Front. Oncol. 2022, 11, 818869. [Google Scholar] [CrossRef]
- Masuda, R.; Kijima, H.; Imamura, N.; Aruga, N.; Nakamura, Y.; Masuda, D.; Takeichi, H.; Kato, N.; Nakagawa, T.; Tanaka, M.; et al. Tumor budding is a significant indicator of a poor prognosis in lung squamous cell carcinoma patients. Mol. Med. Rep. 2012, 6, 937–943. [Google Scholar] [CrossRef]
- Kadota, K.; Yeh, Y.C.; Villena-Vargas, J.; Cherkassky, L.; Drill, E.N.; Sima, C.S.; Jones, D.R.; Travis, W.D.; Adusumilli, P.S. Tumor Budding Correlates with the Protumor Immune Microenvironment and Is an Independent Prognostic Factor for Recurrence of Stage I Lung Adenocarcinoma. Chest 2015, 148, 711–721. [Google Scholar] [CrossRef]
- Budau, K.L.; Sigel, C.S.; Bergmann, L.; Lüchtenborg, A.M.; Wellner, U.; Schilling, O.; Werner, M.; Tang, L.; Bronsert, P. Prognostic Impact of Tumor Budding in Intrahepatic Cholangiocellular Carcinoma. J. Cancer 2022, 13, 2457–2471. [Google Scholar] [CrossRef]
- Argon, A.; Öz, Ö.; Kebat, T.A. Evaluation and prognostic significance of tumor budding in pancreatic ductal adenocarcinomas. Indian J. Pathol. Microbiol. 2023, 66, 38–43. [Google Scholar] [CrossRef]
- Szalai, L.; Jakab, Á.; Kocsmár, I.; Szirtes, I.; Kenessey, I.; Szijártó, A.; Schaff, Z.; Kiss, A.; Lotz, G.; Kocsmár, É. Prognostic Ability of Tumor Budding Outperforms Poorly Differentiated Clusters in Gastric Cancer. Cancers 2022, 14, 4731. [Google Scholar] [CrossRef]
- Le, T.M.; Nguyen, H.D.T.; Lee, E.; Lee, D.; Choi, Y.S.; Cho, J.; Park, N.J.; Han, H.S.; Chong, G.O. Transcriptomic Immune Profiles Can Represent the Tumor Immune Microenvironment Related to the Tumor Budding Histology in Uterine Cervical Cancer. Genes 2022, 13, 1405. [Google Scholar] [CrossRef]
- Choi, Y.; Park, N.J.; Le, T.M.; Lee, E.; Lee, D.; Nguyen, H.D.T.; Cho, J.; Park, J.Y.; Han, H.S.; Chong, G.O. Immune Pathway and Gene Database (IMPAGT) Revealed the Immune Dysregulation Dynamics and Overactivation of the PI3K/Akt Pathway in Tumor Buddings of Cervical Cancer. Curr. Issues Mol. Biol. 2022, 44, 5139–5152. [Google Scholar] [CrossRef] [PubMed]
- Ocal, I.; Guzelis, I. Tumor budding is a valuable prognostic parameter in endometrial carcinomas. Indian J. Pathol. Microbiol. 2022, 65, 851–855. [Google Scholar] [PubMed]
- Yang, Y.; Xu, H.; Zhu, H.; Yuan, D.; Zhang, H.; Liu, Z.; Zhao, F.; Liang, G. EPDR1 levels and tumor budding predict and affect the prognosis of bladder carcinoma. Front. Oncol. 2022, 12, 986006. [Google Scholar] [CrossRef] [PubMed]
- Lino-Silva, L.S.; Zepeda-Najar, C.; Caro-Sánchez, C.H.; Herrera-Gómez, Á.; Salcedo-Hernández, R.A. Prognostic significance of tumor budding in melanoma. Melanoma Res. 2022, 32, 318–323. [Google Scholar] [CrossRef] [PubMed]
- Ling, Z.; Cheng, B.; Tao, X. Epithelial-to-mesenchymal transition in oral squamous cell carcinoma: Challenges and opportunities. Int. J. Cancer 2020, 148, 1548–1561. [Google Scholar] [CrossRef]
- Grigore, A.D.; Jolly, M.K.; Jia, D.; Farach-Carson, M.C.; Levine, H. Tumor budding: The name is EMT. Partial EMT. J. Clin. Med. 2016, 5, 51. [Google Scholar] [CrossRef]
- Wang, C.; Huang, H.; Huang, Z.; Wang, A.; Chen, X.; Huang, L.; Zhou, X.; Liu, X. Tumor budding correlates with poor prognosis and epithelial- mesenchymal transition in tongue squamous cell carcinoma. J. Oral Pathol. Med. 2011, 40, 545–551. [Google Scholar] [CrossRef]
- Zlobec, I.; Lugli, A. Epithelial mesenchymal transition and tumor budding in aggressive colorectal cancer: Tumor budding as oncotarget. Oncotarget 2010, 1, 651–661. [Google Scholar] [CrossRef]
- Galván, J.A.; Zlobec, I.; Wartenberg, M.; Lugli, A.; Gloor, B.; Perren, A.; Karamitopoulou, E. Expression of E-cadherin repressors SNAIL, ZEB1 and ZEB2 by tumour and stromal cells influences tumour-budding phenotype and suggests heterogeneity of stromal cells in pancreatic cancer. Br. J. Cancer 2015, 112, 1944–1950. [Google Scholar] [CrossRef]
- Bradley, C.A.; Dunne, P.D.; Bingham, V.; McQuaid, S.; Khawaja, H.; Craig, S.; James, J.; Moore, W.L.; McArt, D.G.; Lawler, M.; et al. Transcriptional upregulation of c-MET is associated with invasion and tumor budding in colorectal cancer. Oncotarget 2016, 7, 78932–78945. [Google Scholar] [CrossRef]
- Miyake, M.; Hori, S.; Morizawa, Y.; Tatsumi, Y.; Toritsuka, M.; Ohnishi, S.; Shimada, K.; Furuya, H.; Khadka, V.S.; Deng, Y.; et al. Collagen type IV alpha 1 (COL4A1) and collagen type XIII alpha 1 (COL13A1) produced in cancer cells promote tumor budding at the invasion front in human urothelial carcinoma of the bladder. Oncotarget 2017, 8, 36099–36114. [Google Scholar] [CrossRef]
- Arroyo-Solera, I.; Pavón, M.Á.; Leon, X.; Lopez, M.; Gallardo, A.; Céspedes, M.V.; Casanova, I.; Pallares, V.; López-Pousa, A.; Mangues, M.A.; et al. Effect of serpinE1 overexpression on the primary tumor and lymph node, and lung metastases in head and neck squamous cell carcinoma. Head Neck 2019, 41, 429–439. [Google Scholar] [CrossRef]
- Xie, N.; Wang, C.; Zhuang, Z.; Hou, J.; Liu, X.; Wu, Y.; Liu, H.; Huang, H. Decreased miR-320a promotes invasion and metastasis of tumor budding cells in tongue squamous cell carcinoma. Oncotarget 2016, 7, 65744–65757. [Google Scholar] [CrossRef]
- Parikh, A.S.; Puram, S.V.; Faquin, W.C.; Richmon, J.D.; Emerick, K.S.; Deschler, D.G.; Varvares, M.A.; Tirosh, I.; Bernstein, B.E.; Lin, D.T. Immunohistochemical quantification of partial-EMT in oral cavity squamous cell carcinoma primary tumors is associated with nodal metastasis. Oral Oncol. 2019, 99, 104458. [Google Scholar] [CrossRef]
- Xie, N.; Wang, C.; Liu, X.; Li, R.; Hou, J.; Chen, X.; Huang, H. Tumor budding correlates with occult cervical lymph node metastasis and poor prognosis in clinical early-stage tongue squamous cell carcinoma. J. Oral Pathol. Med. 2015, 44, 266–272. [Google Scholar] [CrossRef]
- Pastushenko, I.; Brisebarre, A.; Sifrim, A.; Fioramonti, M.; Revenco, T.; Boumahdi, S.; Van Keymeulen, A.; Brown, D.; Moers, V.; Lemaire, S.; et al. Identification of the tumour transition states occurring during EMT. Nature 2018, 556, 463–468. [Google Scholar] [CrossRef]
- Pastushenko, I.; Blanpain, C. EMT transition states during tumor progression and metastasis. Trends Cell Biol. 2019, 29, 212–226. [Google Scholar] [CrossRef]
- Sarioglu, S.; Acara, C.; Akman, F.C.; Dag, N.; Ecevit, C.; Ikiz, A.O.; Cetinayak, O.H.; Ada, E. Tumor budding as a prognostic marker in laryngeal carcinoma. Pathol. Res. Pract. 2010, 206, 88–92. [Google Scholar] [CrossRef]
- Gonzalez-Guerrero, M.; Martínez-Camblor, P.; Vivanco, B.; Fernández-Vega, I.; Munguía-Calzada, P.; Gonzalez-Gutierrez, M.P.; Rodrigo, J.P.; Galache, C.; Santos-Juanes, J. The adverse prognostic effect of tumor budding on the evolution of cutaneous head and neck squamous cell carcinoma. J. Am. Acad. Dermatol. 2017, 76, 1139–1145. [Google Scholar] [CrossRef]
- De Smedt, L.; Palmans, S.; Andel, D.; Govaere, O.; Boeckx, B.; Smeets, D.; Galle, E.; Wouters, J.; Barras, D.; Suffiotti, M.; et al. Expression profiling of budding cells in colorectal cancer reveals an EMT-like phenotype and molecular subtype switching. Br. J. Cancer 2017, 116, 58–65. [Google Scholar] [CrossRef]
- Mannelli, G.; Gallo, O. Cancer stem cells hypothesis and stem cells in head and neck cancers. Cancer Treat. Rev. 2012, 38, 515–539. [Google Scholar] [CrossRef] [PubMed]
- Duester, G. Retinoic acid synthesis and signaling during early organogenesis. Cell 2008, 134, 921–931. [Google Scholar] [CrossRef] [PubMed]
- Luo, W.R.; Gao, F.; Li, S.Y.; Yao, K.T. Tumour budding and the expression of cancer stem cell marker aldehyde dehydrogenase 1 in nasopharyngeal carcinoma. Histopathology 2012, 61, 1072–1081. [Google Scholar] [CrossRef] [PubMed]
- Marangon Junior, H.; Melo, V.V.M.; Caixeta, Â.B.; Souto, G.R.; Souza, P.E.A.; de Aguiar, M.C.F.; Horta, M.C.R. Immunolocalization of cancer stem cells marker ALDH1 and its association with tumor budding in oral squamous cell carcinoma. Head Neck Pathol 2019, 13, 535–542. [Google Scholar] [CrossRef]
- Boxberg, M.; Götz, C.; Haidari, S.; Dorfner, C.; Jesinghaus, M.; Drecoll, E.; Boskov, M.; Wolff, K.D.; Weichert, W.; Haller, B.; et al. Immunohistochemical expression of CD44 in oral squamous cell carcinoma in relation to histomorphological parameters and clinicopathological factors. Histopathology 2018, 73, 559–572. [Google Scholar] [CrossRef]
- Mäkitie, A.A.; Almangush, A.; Rodrigo, J.P.; Ferlito, A.; Leivo, I. Hallmarks of cancer: Tumor budding as a sign of invasion and metastasis in head and neck cancer. Head Neck 2019, 41, 3712–3718. [Google Scholar] [CrossRef]
- Jensen, D.H.; Dabelsteen, E.; Specht, L.; Fiehn, A.M.K.; Therkildsen, M.H.; Jønson, L.; Vikesaa, J.; Nielsen, F.C.; Von Buchwald, C. Molecular profiling of tumour budding implicates TGF beta-mediated epithelial-mesenchymal transition as a therapeutic target in oral squamous cell carcinoma. J. Pathol. 2015, 236, 505–516. [Google Scholar] [CrossRef]
- Bronsert, P.; Enderle-Ammour, K.; Bader, M.; Timme, S.; Kuehs, M.; Csanadi, A.; Kayser, G.; Kohler, I.; Bausch, D.; Hoeppner, J.; et al. Cancer cell invasion and EMT marker expression: A three-dimensional study of the human cancer-host interface. J. Pathol. 2014, 234, 410–422. [Google Scholar] [CrossRef]
- Sharaf, K.; Lechner, A.; Haider, S.P.; Wiebringhaus, R.; Walz, C.; Kranz, G.; Canis, M.; Haubner, F.; Gires, O.; Baumeister, P. Discrimination of Cancer Stem Cell Markers ALDH1A1, BCL11B, BMI-1, and CD44 in Different Tissues of HNSCC Patients. Curr. Oncol. 2021, 28, 2763–2774. [Google Scholar] [CrossRef]
- Jakob, M.; Sharaf, K.; Schirmer, M.; Leu, M.; Küffer, S.; Bertlich, M.; Ihler, F.; Haubner, F.; Canis, M.; Kitz, J. Role of cancer stem cell markers ALDH1, BCL11B, BMI-1, and CD44 in the prognosis of advanced HNSCC. Strahlenther. Onkol. 2021, 197, 231–245. [Google Scholar] [CrossRef]
- Wang, W.; Xie, N.; Yi, C.; Zhang, M.; Xiong, G.; Xu, X.; Hou, J.; Wang, C. Prognostic and clinicopathological significance of cytocapsular tubes in oral squamous cell carcinoma. J. Oral Pathol. Med. 2022, 51, 520–528. [Google Scholar] [CrossRef]
- Puram, S.V.; Parikh, A.S.; Tirosh, I. Single cell RNA- seq highlights a role for a partial EMT in head and neck cancer. Mol. Cell. Oncol. 2018, 5, e1448244. [Google Scholar] [CrossRef]
- Puram, S.V.; Tirosh, I.; Parikh, A.S.; Patel, A.P.; Yizhak, K.; Gillespie, S.; Rodman, C.; Luo, C.L.; Mroz, E.A.; Emerick, K.S.; et al. Single-Cell Transcriptomic Analysis of Primary and Metastatic Tumor Ecosystems in Head and Neck Cancer. Cell 2017, 171, 1611–1624. [Google Scholar] [CrossRef]
- Bolós, V.; Peinado, H.; Pérez-Moreno, M.A.; Fraga, M.F.; Esteller, M.; Cano, A. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: A comparison with Snail and E47 repressors. J. Cell Sci. 2003, 116 Pt 3, 499–511. [Google Scholar] [CrossRef]
- Yang, J.; Antin, P.; Berx, G.; Blanpain, C.; Brabletz, T.; Bronner, M.; Campbell, K.; Cano, A.; Casanova, J.; Christofori, G.; et al. Guidelines and definitions for research on epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 2020, 21, 341–352, Erratum in Nat. Rev. Mol. Cell Biol. 2021, 22, 834. [Google Scholar] [CrossRef]
- Okuyama, K.; Suzuki, K.; Yanamoto, S.; Naruse, T.; Tsuchihashi, H.; Yamashita, S.; Umeda, M. Anaplastic transition within the cancer microenvironment in early-stage oral tongue squamous cell carcinoma is associated with local recurrence. Int. J. Oncol. 2018, 53, 1713–1720. [Google Scholar] [CrossRef]
- Kohler, I.; Bronsert, P.; Timme, S.; Werner, M.; Brabletz, T.; Hopt, U.T.; Schilling, O.; Bausch, D.; Keck, T.; Wellner, U.F. Detailed analysis of epithelial-mesenchymal transition and tumor budding identifies predictors of long-term survival in pancreatic ductal adenocarcinoma. J. Gastroenterol. Hepatol. 2015, 30 (Suppl. 1), 78–84. [Google Scholar] [CrossRef]
- Saini, S.; Tulla, K.; Maker, A.V.; Burman, K.D.; Prabhakar, B.S. Therapeutic advances in anaplastic thyroid cancer: A current perspective. Mol. Cancer 2018, 17, 154. [Google Scholar] [CrossRef]
- O’Neill, J.P.; Shaha, A.R. Anaplastic thyroid cancer. Oral Oncol. 2013, 49, 702–726. [Google Scholar] [CrossRef]
- Perrier, N.D.; Brierley, J.D.; Tuttle, R.M. Differentiated and anaplastic thyroid carcinoma: Major changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J. Clin. 2018, 68, 55–63. [Google Scholar] [CrossRef]
- Meyer, S.N.; Galván, J.A.; Zahnd, S.; Sokol, L.; Dawson, H.; Lugli, A.; Zlobec, I. Co-expression of cytokeratin and vimentin in colorectal cancer highlights a subset of tumor buds and an atypical cancer-associated stroma. Hum. Pathol. 2019, 87, 18–27. [Google Scholar] [CrossRef] [PubMed]
- Wartenberg, M.; Zlobec, I.; Perren, A.; Koelzer, V.H.; Gloor, B.; Lugli, A.; Eva, K. Accumulation of FOXP3+T-cells in the tumor microenvironment is associated with an epithelial-mesenchymal-transition-type tumor budding phenotype and is an independent prognostic factor in surgically resected pancreatic ductal adenocarcinoma. Oncotarget 2015, 6, 4190–4201. [Google Scholar] [CrossRef] [PubMed]
- Wartenberg, M.; Cibin, S.; Zlobec, I.; Vassella, E.; Eppenberger-Castori, S.; Terracciano, L.; Eichmann, M.D.; Worni, M.; Gloor, B.; Perren, A.; et al. Integrated Genomic and Immunophenotypic Classification of Pancreatic Cancer Reveals Three Distinct Subtypes with Prognostic/Predictive Significance. Clin. Cancer Res. 2018, 24, 4444–4454. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.J.; Liu, H.; Liao, C.T.; Huang, P.J.; Huang, Y.; Hsu, A.; Tang, P.; Chang, Y.S.; Chen, H.C.; Yen, T.C. Ultra-deep targeted sequencing of advanced oral squamous cell carcinoma identifies a mutation-based prognostic gene signature. Oncotarget 2015, 6, 18066–18080. [Google Scholar] [CrossRef]
- Moreira, A.; Poulet, A.; Masliah-Planchon, J.; Lecerf, C.; Vacher, S.; Chérif, L.L.; Dupain, C.; Marret, G.; Girard, E.; Syx, L.; et al. Prognostic value of tumor mutational burden in patients with oral cavity squamous cell carcinoma treated with upfront surgery. ESMO Open 2021, 6, 100178. [Google Scholar] [CrossRef]
- Sadozai, H.; Acharjee, A.; Gruber, T.; Gloor, B.; Karamitopoulou, E. Pancreatic Cancers with High Grade Tumor Budding Exhibit Hallmarks of Diminished Anti-Tumor Immunity. Cancers 2021, 13, 1090. [Google Scholar] [CrossRef]
- Wong, C.C.; Kai, A.K.; Ng, I.O. The impact of hypoxia in hepatocellular carcinoma metastasis. Front. Med. 2014, 8, 33–41. [Google Scholar] [CrossRef]
- Nakashima, C.; Kirita, T.; Yamamoto, K.; Mori, S.; Luo, Y.; Sasaki, T.; Fujii, K.; Ohmori, H.; Kawahara, I.; Mori, T.; et al. Malic Enzyme 1 Is Associated with Tumor Budding in Oral Squamous Cell Carcinomas. Int. J. Mol. Sci. 2020, 21, 7149. [Google Scholar] [CrossRef]
- Nakashima, C.; Yamamoto, K.; Kishi, S.; Sasaki, T.; Ohmori, H.; Fujiwara-Tani, R.; Mori, S.; Kawahara, I.; Nishiguchi, Y.; Mori, T.; et al. Clostridium perfringens enterotoxin induces claudin-4 to activate YAP in oral squamous cell carcinomas. Oncotarget 2020, 11, 309–321. [Google Scholar] [CrossRef]
- Greenhough, A.; Bagley, C.; Heesom, K.J.; Gurevich, D.B.; Gay, D.; Bond, M.; Collard, T.J.; Paraskeva, C.; Martin, P.; Sansom, O.J.; et al. Cancer cell adaptation to hypoxia involves a HIF-GPRC5A-YAP axis. EMBO Mol. Med. 2018, 10, e8699. [Google Scholar] [CrossRef]
- Zhang, X.; Li, Y.; Ma, Y.; Yang, L.; Wang, T.; Meng, X.; Zong, Z.; Sun, X.; Hua, X.; Li, H. Yes-associated protein (YAP) binds to HIF-1α and sustains HIF-1α protein stability to promote hepatocellular carcinoma cell glycolysis under hypoxic stress. J. Exp. Clin. Cancer Res. 2018, 37, 216. [Google Scholar] [CrossRef]
- Guzińska-Ustymowicz, K. MMP-9 and cathepsin B expression in tumor budding as an indicator of a more aggressive phenotype of colorectal cancer (CRC). Anticancer Res. 2006, 26, 1589–1594. [Google Scholar]
- Masaki, T.; Matsuoka, H.; Sugiyama, M.; Abe, N.; Goto, A.; Sakamoto, A.; Atomi, Y. Matrilysin (MMP-7) as a significant determinant of malignant potential of early invasive colorectal carcinomas. Br. J. Cancer 2001, 84, 1317–1321. [Google Scholar] [CrossRef]
- Nascimento, G.J.F.D.; Silva, L.P.D.; Matos, F.R.; Silva, T.A.D.; Medeiros, S.R.B.; Souza, L.B.; Freitas, R.A. Polymorphisms of matrix metalloproteinase-7 and -9 are associated with oral tongue squamous cell carcinoma. Braz. Oral Res. 2020, 35, e019. [Google Scholar] [CrossRef]
- King, H.W.; Michael, M.Z.; Gleadle, J.M. Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer 2012, 12, 421. [Google Scholar] [CrossRef]
- Montecalvo, A.; Larregina, A.T.; Shufesky, W.J.; Beer Stolz, D.; Sullivan, M.L.; Karlsson, J.M.; Baty, C.J.; Gibson, G.A.; Erdos, G.; Wang, Z.; et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 2012, 119, 756–766. [Google Scholar] [CrossRef]
- Li, J.; Zhang, Y.; Liu, Y.; Dai, X.; Li, W.; Cai, X.; Yin, Y.; Wang, Q.; Xue, Y.; Wang, C.; et al. Microvesicle-mediated transfer of microRNA-150 from monocytes to endothelial cells promotes angiogenesis. J. Biol. Chem. 2013, 288, 23586–23596. [Google Scholar] [CrossRef]
- Quante, M.; Tu, S.P.; Tomita, H.; Gonda, T.; Wang, S.S.; Takashi, S.; Baik, G.H.; Shibata, W.; DiPrete, B.; Betz, K.S.; et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 2011, 19, 257–272. [Google Scholar] [CrossRef]
- Wang, H.X.; Gires, O. Tumor-derived extracellular vesicles in breast cancer: From bench to bedside. Cancer Lett. 2019, 460, 54–64. [Google Scholar] [CrossRef]
- Zhou, J.; Schwenk-Zieger, S.; Kranz, G.; Walz, C.; Klauschen, F.; Dhawan, S.; Canis, M.; Gires, O.; Haubner, F.; Baumeister, P.; et al. Isolation and characterization of head and neck cancer-derived peritumoral and cancer-associated fibroblasts. Front. Oncol. 2022, 12, 984138. [Google Scholar] [CrossRef]
- Wang, J.; Min, A.; Gao, S.; Tang, Z. Genetic regulation and potentially therapeutic application of cancer-associated fibroblasts in oral cancer. J. Oral Pathol. Med. 2014, 43, 323–334. [Google Scholar] [CrossRef] [PubMed]
- Xu, H.; Zhao, J.; Li, J.; Zhu, Z.; Cui, Z.; Liu, R.; Lu, R.; Yao, Z.; Xu, Q. Cancer associated fibroblast-derived CCL5 promotes hepatocellular carcinoma metastasis through activating HIF1α/ZEB1 axis. Cell Death Dis. 2022, 13, 478. [Google Scholar] [CrossRef] [PubMed]
- Chang, L.Y.; Lin, Y.C.; Mahalingam, J.; Huang, C.T.; Chen, T.W.; Kang, C.W.; Peng, H.M.; Chu, Y.Y.; Chiang, J.M.; Dutta, A.; et al. Tumor-derived chemokine CCL5 enhances TGF-β-mediated killing of CD8(+) T cells in colon cancer by T-regulatory cells. Cancer Res. 2012, 72, 1092–1102. [Google Scholar] [CrossRef] [PubMed]
- Aldinucci, D.; Borghese, C.; Casagrande, N. The CCL5/CCR5 Axis in Cancer Progression. Cancers 2020, 12, 1765. [Google Scholar] [CrossRef] [PubMed]
- Aldinucci, D.; Colombatti, A. The inflammatory chemokine CCL5 and cancer progression. Mediat. Inflamm. 2014, 2014, 292376. [Google Scholar] [CrossRef]
- Mielcarska, S.; Kula, A.; Dawidowicz, M.; Kiczmer, P.; Chrabańska, M.; Rynkiewicz, M.; Wziątek-Kuczmik, D.; Świętochowska, E.; Waniczek, D. Assessment of the RANTES Level Correlation and Selected Inflammatory and Pro-Angiogenic Molecules Evaluation of Their Influence on CRC Clinical Features: A Preliminary Observational Study. Medicina 2022, 58, 203. [Google Scholar] [CrossRef]
- Okuyama, K.; Yanamoto, S. TMEM16A as a potential treatment target for head and neck cancer. J. Exp. Clin. Cancer Res. 2022, 41, 196. [Google Scholar] [CrossRef]
- Liu, J.; Wang, C.; Ma, X.; Tian, Y.; Wang, C.; Fu, Y.; Luo, Y. High expression of CCR5 in melanoma enhances epithelial-mesenchymal transition and metastasis via TGFβ1. J. Pathol. 2019, 247, 481–493. [Google Scholar] [CrossRef]
- Gao, L.F.; Zhong, Y.; Long, T.; Wang, X.; Zhu, J.X.; Wang, X.Y.; Hu, Z.Y.; Li, Z.G. Tumor bud-derived CCL5 recruits fibroblasts and promotes colorectal cancer progression via CCR5-SLC25A24 signaling. J. Exp. Clin. Cancer Res. 2022, 41, 81. [Google Scholar] [CrossRef]
- Chuang, J.Y.; Yang, W.H.; Chen, H.T. CCL5/CCR5 axis promotes the motility of human oral cancer cells. J. Cell Physiol. 2009, 220, 418–426. [Google Scholar] [CrossRef]
- Lang, S.; Lauffer, L.; Clausen, C.; Löhr, I.; Schmitt, B.; Hölzel, D.; Wollenberg, B.; Gires, O.; Kastenbauer, E.; Zeidler, R. Impaired monocyte function in cancer patients: Restoration with a cyclooxygenase-2 inhibitor. FASEB J. 2003, 17, 286–288. [Google Scholar] [CrossRef]
- Li, C.; Chen, S.; Liu, C.; Mo, C.; Gong, W.; Hu, J.; He, M.; Xie, L.; Hou, X.; Tang, J.; et al. CCR5 as a prognostic biomarker correlated with immune infiltrates in head and neck squamous cell carcinoma by bioinformatic study. Hereditas 2022, 159, 37. [Google Scholar] [CrossRef]
- González-Arriagada, W.A.; Lozano-Burgos, C.; Zúñiga-Moreta, R.; González-Díaz, P.; Coletta, R.D. Clinicopathological significance of chemokine receptor (CCR1, CCR3, CCR4, CCR5, CCR7 and CXCR4) expression in head and neck squamous cell carcinomas. J. Oral Pathol. Med. 2018, 47, 755–763. [Google Scholar] [CrossRef]
- Trumpi, K.; Frenkel, N.; Peters, T.; Korthagen, N.M.; Jongen, J.M.; Raats, D.; van Grevenstein, H.; Backes, Y.; Moons, L.M.; Lacle, M.M.; et al. Macrophages induce “budding” in aggressive human colon cancer subtypes by protease-mediated disruption of tight junctions. Oncotarget 2018, 9, 19490–19507. [Google Scholar] [CrossRef]
- Wang, M.; Su, Z.; Amoah Barnie, P. Crosstalk among colon cancer-derived exosomes, fibroblast-derived exosomes, and macrophage phenotypes in colon cancer metastasis. Int. Immunopharmacol. 2020, 81, 106298. [Google Scholar] [CrossRef]
- Xiao, M.; Zhang, J.; Chen, W.; Chen, W. M1-like tumor-associated macrophages activated by exosome-transferred THBS1 promote malignant migration in oral squamous cell carcinoma. J. Exp. Clin. Cancer Res. 2018, 37, 143. [Google Scholar] [CrossRef]
- You, Y.; Tian, Z.; Du, Z.; Wu, K.; Xu, G.; Dai, M.; Wang, Y.; Xiao, M. M1-like tumor-associated macrophages cascade a mesenchymal/stem-like phenotype of oral squamous cell carcinoma via the IL6/Stat3/THBS1 feedback loop. J. Exp. Clin. Cancer Res. 2022, 41, 10. [Google Scholar] [CrossRef]
- Peixoto da-Silva, J.; Lourenço, S.; Nico, M.; Silva, F.H.; Martins, M.T.; Costa-Neves, A. Expression of laminin-5 and integrins in actinic cheilitis and superficially invasive squamous cell carcinomas of the lip. Pathol. Res. Pract. 2012, 208, 598–603. [Google Scholar] [CrossRef]
- Marangon Junior, H.; Rocha, V.N.; Leite, C.F.; de Aguiar, M.C.F.; Souza, P.E.A.; Horta, M.C.R. Laminin-5 gamma 2 chain expression is associated with intensity of tumor budding and density of stromal myofibroblasts in oral squamous cell carcinoma. J. Oral Pathol. Med. 2014, 43, 199–204. [Google Scholar] [CrossRef]
- Zhou, B.; Zong, S.; Zhong, W.; Tian, Y.; Wang, L.; Zhang, Q.; Zhang, R.; Li, L.; Wang, W.; Zhao, J.; et al. Interaction between laminin-5γ2 and integrin β1 promotes the tumor budding of colorectal cancer via the activation of Yes-associated proteins. Oncogene 2020, 39, 1527–1542. [Google Scholar] [CrossRef]
- Fiore, V.F.; Krajnc, M.; Quiroz, F.G.; Levorse, J.; Pasolli, H.A.; Shvartsman, S.Y.; Fuchs, E. Mechanics of a multilayer epithelium instruct tumour architecture and function. Nature 2020, 585, 433–439. [Google Scholar] [CrossRef] [PubMed]
- Wang, M.; Nagle, R.B.; Knudsen, B.S.; Rogers, G.C.; Cress, A.E. A basal cell defect promotes budding of prostatic intraepithelial neoplasia. J. Cell Sci. 2017, 130, 104–110. [Google Scholar] [CrossRef] [PubMed]
- Gholizadeh, P.; Eslami, H.; Kafil, H.S. Carcinogenesis mechanisms of Fusobacterium nucleatum. Biomed. Pharmacother. 2017, 89, 918–925. [Google Scholar] [CrossRef] [PubMed]
- Al-Hebshi, N.N.; Nasher, A.T.; Maryoud, M.Y.; Homeida, H.E.; Chen, T.; Idris, A.M.; Johnson, N.W. Inflammatory bacteriome featuring Fusobacterium nucleatum and Pseudomonas aeruginosa identified in association with oral squamous cell carcinoma. Sci. Rep. 2017, 7, 1834. [Google Scholar] [CrossRef] [PubMed]
- Shao, W.; Fujiwara, N.; Mouri, Y.; Kisoda, S.; Yoshida, K.; Yoshida, K.; Yumoto, H.; Ozaki, K.; Ishimaru, N.; Kudo, Y. Conversion from epithelial to partial-EMT phenotype by Fusobacterium nucleatum infection promotes invasion of oral cancer cells. Sci. Rep. 2021, 11, 14943. [Google Scholar] [CrossRef]
- Kostic, A.D.; Gevers, D.; Pedamallu, C.S.; Michaud, M.; Duke, F.; Earl, A.M.; Ojesina, A.I.; Jung, J.; Bass, A.J.; Tabernero, J.; et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 2012, 22, 292–298. [Google Scholar] [CrossRef]
- Okuyama, K.; Yanamoto, S. Oral bacterial contributions to gingival carcinogenesis and progression. Cancer Prev. Res. 2023, in press. [Google Scholar] [CrossRef]
- Harrandah, A.M.; Chukkapalli, S.S.; Bhattacharyya, I.; Progulske-Fox, A.; Chan, E.K.L. Fusobacteria modulate oral carcinogenesis and promote cancer progression. J. Oral Microbiol. 2020, 13, 1849493. [Google Scholar] [CrossRef]
- Niño, J.L.G.; Wu, H.; LaCourse, K.D.; Kempchinsky, A.G.; Baryiames, A.; Barber, B.; Futran, N.; Houlton, J.; Sather, C.; Sicinska, E.; et al. Effect of the intratumoral microbiota on spatial and cellular heterogeneity in cancer. Nature 2022, 611, 810–817. [Google Scholar] [CrossRef]
- Salama, A.M.; Momeni-Boroujeni, A.; Vanderbilt, C.; Ladanyi, M.; Soslow, R. Molecular landscape of vulvovaginal squamous cell carcinoma: New insights into molecular mechanisms of HPV-associated and HPV-independent squamous cell carcinoma. Mod. Pathol. 2022, 35, 274–282. [Google Scholar] [CrossRef]
- Cho, Y.A.; Kim, E.K.; Cho, B.C.; Koh, Y.W.; Yoon, S.O. Twist and Snail/Slug Expression in Oropharyngeal Squamous Cell Carcinoma in Correlation with Lymph Node Metastasis. Anticancer Res. 2019, 39, 6307–6316. [Google Scholar] [CrossRef]
- Prall, F.; Ostwald, C.; Weirich, V.; Nizze, H. p16(INK4a) promoter methylation and 9p21 allelic loss in colorectal carcinomas: Relation with immunohistochemical p16(INK4a) expression and with tumor budding. Hum. Pathol. 2006, 37, 578–585. [Google Scholar] [CrossRef]
- Bertino, J.R.; Waud, W.R.; Parker, W.B.; Lubin, M. Targeting tumors that lack methylthioadenosine phosphorylase (MTAP) activity: Current strategies. Cancer Biol. Ther. 2011, 11, 627–632. [Google Scholar] [CrossRef]
- Bataille, F.; Rogler, G.; Modes, K.; Poser, I.; Schuierer, M.; Dietmaier, W.; Ruemmele, P.; Mühlbauer, M.; Wallner, S.; Hellerbrand, C.; et al. Strong expression of methylthioadenosine phosphorylase (MTAP) in human colon carcinoma cells is regulated by TCF1/[beta]-catenin. Lab. Investig. 2005, 85, 124–136. [Google Scholar] [CrossRef]
- Zhong, Y.; Lu, K.; Zhu, S.; Li, W.; Sun, S. Characterization of methylthioadenosin phosphorylase (MTAP) expression in colorectal cancer. Artif. Cells Nanomed. Biotechnol. 2018, 46, 2082–2087. [Google Scholar] [CrossRef]
- Amano, Y.; Matsubara, D.; Kihara, A.; Nishino, H.; Mori, Y.; Niki, T. Expression and localisation of methylthioadenosine phosphorylase (MTAP) in oral squamous cell carcinoma and their significance in epithelial-to-mesenchymal transition. Pathology 2022, 54, 294–301. [Google Scholar] [CrossRef]
- Yang, Z.; Zhang, C.; Qi, W.; Cui, C.; Cui, Y.; Xuan, Y. Tenascin-C as a prognostic determinant of colorectal cancer through induction of epithelial-to-mesenchymal transition and proliferation. Exp. Mol. Pathol. 2018, 105, 216–222. [Google Scholar] [CrossRef]
- Gao, Y.; Nan, X.; Shi, X.; Mu, X.; Liu, B.; Zhu, H.; Yao, B.; Liu, X.; Yang, T.; Hu, Y.; et al. SREBP1 promotes the invasion of colorectal cancer accompanied upregulation of MMP7 expression and NF-κB pathway activation. BMC Cancer 2019, 19, 685. [Google Scholar] [CrossRef]
- Roseweir, A.K.; Clark, J.; McSorley, S.T.; van Wyk, H.C.; Quinn, J.A.; Horgan, P.G.; McMillan, D.C.; Park, J.H.; Edwards, J. The association between markers of tumour cell metabolism, the tumour microenvironment and outcomes in patients with colorectal cancer. Int. J. Cancer 2019, 144, 2320–2329. [Google Scholar] [CrossRef]
- Olianas, A.; Serrao, S.; Piras, V.; Manconi, B.; Contini, C.; Iavarone, F.; Pichiri, G.; Coni, P.; Zorcolo, L.; Orrù, G.; et al. Thymosin β4 and β10 are highly expressed at the deep infiltrative margins of colorectal cancer—A mass spectrometry analysis. Eur. Rev. Med. Pharmacol. Sci. 2021, 25, 7285–7296. [Google Scholar]
- Farah, C.S. Molecular landscape of head and neck cancer and implications for therapy. Ann. Transl. Med. 2021, 9, 915. [Google Scholar] [CrossRef] [PubMed]
- Bronte, G.; Silvestris, N.; Castiglia, M.; Galvano, A.; Passiglia, F.; Sortino, G.; Cicero, G.; Rolfo, C.; Peeters, M.; Bazan, V.; et al. New findings on primary and acquired resistance to anti-EGFR therapy in metastatic colorectal cancer: Do all roads lead to RAS? Oncotarget 2015, 6, 24780–24796. [Google Scholar] [CrossRef] [PubMed]
- Komiya, Y.; Shimomura, Y.; Higurashi, T.; Sugi, Y.; Arimoto, J.; Umezawa, S.; Uchiyama, S.; Matsumoto, M.; Nakajima, A. Patients with colorectal cancer have identical strains of Fusobacterium nucleatum in their colorectal cancer and oral cavity. Gut 2019, 68, 1335–1337. [Google Scholar] [CrossRef] [PubMed]
- Kitamoto, S.; Nagao-Kitamoto, H.; Jiao, Y.; Gillilland, M.G., 3rd; Hayashi, A.; Imai, J.; Sugihara, K.; Miyoshi, M.; Brazil, J.C.; Kuffa, P.; et al. The Intermucosal Connection between the Mouth and Gut in Commensal Pathobiont-Driven Colitis. Cell 2020, 182, 447–462.e14. [Google Scholar] [CrossRef]
TB Driver | Mechanism | Cancer Type | Year | Reference |
---|---|---|---|---|
COL4A1/COL13A1 | Activation of intracellular AKT pathway leads to an E/N-cadherin switch | Urothelial carcinoma of bladder | 2017 | [31] |
SerpinE1 (known as plasminogen activator inhibitor type 1) | Regulation of the plasminogen activator system | HNSCC | 2019 | [32] |
c-MET | Upregulation of MET transcription | CRC | 2016 | [30] |
Tenascin-C | Tenascin-C induces cancer cell EMT-like change | CRC | 2018 | [117] |
SREBP1 | Upregulation of MMP7expression and NF-κB pathway activation | CRC | 2019 | [118] |
Increased tumor stroma Percentage and LDH-5 | Decrease CD3+ lymphocyte stromal density | CRC | 2019 | [119] |
Thymosin β4/β10 | Modulation of cytoskeleton organization | CRC | 2021 | [120] |
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
Okuyama, K.; Suzuki, K.; Yanamoto, S. Relationship between Tumor Budding and Partial Epithelial–Mesenchymal Transition in Head and Neck Cancer. Cancers 2023, 15, 1111. https://doi.org/10.3390/cancers15041111
Okuyama K, Suzuki K, Yanamoto S. Relationship between Tumor Budding and Partial Epithelial–Mesenchymal Transition in Head and Neck Cancer. Cancers. 2023; 15(4):1111. https://doi.org/10.3390/cancers15041111
Chicago/Turabian StyleOkuyama, Kohei, Keiji Suzuki, and Souichi Yanamoto. 2023. "Relationship between Tumor Budding and Partial Epithelial–Mesenchymal Transition in Head and Neck Cancer" Cancers 15, no. 4: 1111. https://doi.org/10.3390/cancers15041111
APA StyleOkuyama, K., Suzuki, K., & Yanamoto, S. (2023). Relationship between Tumor Budding and Partial Epithelial–Mesenchymal Transition in Head and Neck Cancer. Cancers, 15(4), 1111. https://doi.org/10.3390/cancers15041111