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Cancer and Metastasis: Importance of Cell Adhesion Molecules and Cell Junctions

Year 2020, Volume: 10 Issue: 1, 38 - 48, 13.03.2020
https://doi.org/10.26650/experimed.2020.0003

Abstract

Metastasis is a complex process which is driven by several biochemical and molecular factors. Metastasis is a condition which severely limits cancer therapies and is responsible for 90% of cancer deaths. Therefore, it is of crucial importance to gain a greater understanding of the underlying mechanisms of metastasis in terms of developing treatment methods for metastasis prevention. Included in metastasis are multiple steps such as local invasion (epithelial-mesenchymal transition), intravasation, survival in the circulatory system, extravasation (transendothelial migration/ diapedesis), formation of micrometastasis and metastatic colony. Tumor cells escape from circulating immune cells and apoptosis using platelets as a ‘‘shield’’ and a ‘‘link’’ for binding to endothelium via altering expression patterns of adhesion molecules. Extravasation in tumor cells is one of the key steps of metastasis and despite small differences in molecules, the whole process is basically the same in leukocytes; rolling, adhesion, and transmigration. Cell adhesion molecules such as integrins, and cell junctions such as Jam proteins, are key players in the extravasation step. Therefore, cell adhesion molecules and cell junctions can be used as potential targets for cancer therapy. In this review, the general processes of metastasis and the roles of cell adhesion molecules/cell junctions on metastasis were summarized.

References

  • 1. Reymond N, d'Águal BB, Ridley AJ. Crossing the endothelial barrier during metastasis. Nature Reviews Cancer 2013; 13(12): 858-70. [CrossRef]
  • 2. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011; 147: 275-92. [CrossRef]
  • 3. Pacmayr E, Treese C, Stein U. Underlying Mechanisms for Distant Metastasis - Molecular Biology. Visc Med. 2017; 33: 11-20. [CrossRef]
  • 4. Knights AJ., Funnell APW, Crossley M, Pearson CMR. Holding Tight: Cell Junctions and Cancer Spread. Trends Cancer Res. 2012; 8: 61-9.
  • 5. Sökeland G, Schumacher U. The functional role of integrins during intra- and extravasation within the metastatic cascade. Molecular Cancer 2019; 18:12. [CrossRef]
  • 6. Gheldof A, Berx G. Cadherins and epithelial-to-mesenchymal transition. Prog Mol Biol Transl Sci. 2013; 116: 317-36. [CrossRef]
  • 7. Farahani E, Patra HK, Jangamreddy JR, Rashedi I, Kawalec M, Rao Pariti RK, et al. Cell adhesion molecules and their relation to (cancer) cell stemness. Carcinogenesis 2014; 35(4): 747-59. [CrossRef]
  • 8. Anderberg C, Cunha SI, Zhai Z, Cortez E, Pardali E, Johnson JR, et al. Deficiency for endoglin in tumor vasculature weakens the endothelial barrier to metastatic dissemination. J. Exp. Med. 2013; 210: 563-79. [CrossRef]
  • 9. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-74. [CrossRef]
  • 10. Erler JT, Bennewith KL, Nicolau M, Dornhöfer N, Kong C, Le QT, et al. Lysyl oxidase is essential for hypoxia -induced metastasis. Nature 2006; 440: 1222-6. [CrossRef]
  • 11. Kozłowski J, KozłowskaA, Kocki J. Breast cancer metastasis - insight into selected molecular mechanisms of the phenomenon. Postepy Hig Med Dosw 2015; 69: 447-51. [CrossRef]
  • 12. Paoli P, Giannoni E, Chiarugi P. Anoikis molecular pathways and its role in cancer progression. Biochim Biophys Acta 2013; 1833(12): 3481-98. [CrossRef]
  • 13. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009; 9: 239-52. [CrossRef]
  • 14. Yan M, Jurasz P. The role of platelets in the tumor microenvironment: from solid tumors to leukemia. Biochim Biophys Acta 2016; 1863: 392-400. [CrossRef]
  • 15. Weil RJ, Palmieri DC, Bronder JL, Stark AM, Steeg PS. Breast cancer metastasis to the central nervous system. Am. J. Pathol. 2005; 167: 913-20. [CrossRef]
  • 16. Sarvaiya PJ, Guo D, Ulasov I, Gabikian P, Lesniak MS. Chemokines in tumor progression and metastasis. Oncotarget 2013; 4: 217185. [CrossRef]
  • 17. DeNardo DG, Barreto JB, Andreu P, Vasquez L, Tawfik D, Kolhatkar N, et al. CD4+ cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009; 16: 91-102. [CrossRef]
  • 18. Gocheva V, Wang HW, Gadea BB, Shree T, Hunter KE, Garfall AL, et al. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev. 2010; 24: 241-55. [CrossRef]
  • 19. Strell C, Entschladen F. Extravasation of leukocytes in comparison to tumor cells. Cell Communication and Signaling 2008; 6: 10. [CrossRef]
  • 20. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005; 438: 820-7. [CrossRef]
  • 21. Psaila B, Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer 2009; 9: 285-93. [CrossRef]
  • 22. Makrilia N, Kollias A, Manolopoulos L, Sygios K. Cell adhesion molecules: role and clinical significance in cancer. Cancer Invest. 2009; 27: 1023-37. [CrossRef]
  • 23. Harjunpää H, Llort Asens M, Guenther C, Fagerholm SC. Cell Adhesion Molecules and Their Roles and Regulation in the Immune and Tumor Microenvironment. Front. Immunol. 2019; 10:1078. [CrossRef]
  • 24. Bendas G, Borsig L. Cancer cell adhesion and metastasis: selectins, integrins and, the inhibitory potential of heparins. Int J Cell Biol. 2012; 2012: 676731. [CrossRef]
  • 25. Ludwig RJ, Boehme B, Podda M, Henscheler R, Jager E, Tandi C, et al. Endothelial P selectin as a target of heparin action in experimental melanoma lung metastasis. Cancer Research 2004; 64(8): 2743-50. [CrossRef]
  • 26. Laubli H, Borsig L. Selectins as mediators of lung metastasis. Cancer Microenvironment 2010; 3(1): 97-105. [CrossRef]
  • 27. Van Roy F, Berx G.The cell-cell adhesion molecule E-cadherin. Cell. Mol. Life Sci. 2008; 65: 3756-88. [CrossRef]
  • 28. Cao ZQ, Wang Z, Leng P. Aberrant N-cadherin expression in cancer. Biomedicine & Pharmacotherapy 2019; 118: 109320. [CrossRef]
  • 29. Vestweber D. VE-cadherin: The major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arteriosclerosis, Thrombosis, and Vascular Biology 2008; 28(2): 223-32. [CrossRef]
  • 30. Qureshi HS, Linden MD, Divine G. E-cadherin status in breast cancer correlates with histologic type but does not correlate with established prognostic parameters. Am J Clin Pathol 2006; 125: 377-85. [CrossRef]
  • 31. Elmoneim HM, Zaghoul NM. Expression of E-cadherin, N-cadherin and snail and therir correlation with clinopathological variant: an immunohistochemical study of 132 invasive ductal breast carsinomas in Egypt. Clinics (Sao Paulo) 2011; 66(10): 1765-71.
  • 32. Paredes J, Correia AL, Ribeiro AS, Milanezi F, Cameselle-Teijeiro J, Schmitt FC. Breast carcinomas that co-express E- and P- cadherin are associated with p120-cathenin cytoplasmatic localisation and poor patient survival. Journal Clin Pathol. 2008; 61: 856-62. [CrossRef]
  • 33. Shin K, Fogg VC, Margolis B. Tight junctions and cell polarity. Annu Rev Cell Dev Biol. 2006; 22: 207-235. [CrossRef]
  • 34. Barczyk M, Carracedo S, Gullberg D. Integrins. Cell Tissue Res. 2010; 339: 269-80. [CrossRef]
  • 35. Lahlou H, Muller WJ. β1-integrins signaling and mammary tumor progression in transgenic mouse models: implications for human breast cancer. Breast Cancer Research 2011; 13: 229. [CrossRef]
  • 36. Hamidi H, Pietila M, Ivaska J. The complexity of integrins in cancer and new scopes for therapeutic targeting. British Journal of Cancer 2016; 115: 1017-23. [CrossRef]
  • 37. Khapare N, Kundu ST, Sehgal L, Sawant M., Priya R, Gosavi P, et al. Plakhophilin3 leads to an increase in PRL3 levels promoting K8 dephosphorylation, which is required for transformation and metastasis. PLoS One 2012; 7:e38561. [CrossRef]
  • 38. Aaltomaa S, Karja V, Lipponen P, Isotalo T, Kankkunnen JP, Talja M, et al. Reduced α- and, β-catenin expression predicts shortened survival in local prostate cancer. Anticancer Research 2005; 25: 4707-4712.
  • 39. Salvador E, Burek M, Förster CY. Tight Junctions and the Tumor Microenvironment. Curr Pathobiol Rep. 2016; 4: 135-45. [CrossRef]
  • 40. Martin TA, Mansel RE, Jiang WG. Loss of occludin leads to the progression of human breast cancer. Int. J. Mol. Med. 2010; 26 (5): 723-34. [CrossRef]
  • 41. Osanai M, Murata M, Nishikiori N, Chiba H, Kojima T, Sawada N. Epigenetic silencing of occludin promotes tumorigenic and metastatic properties of cancer cells via modulations of unique sets of apoptosis-associated genes. Cancer Research 2006; 66(18): 912533. [CrossRef]
  • 42. Lanigan F, McKiernan E, Brennan DJ, Hegarty S, Millikan RC, McBryan J, et al. Increased claudin-4 expression is associated with poor prognosis and high tumor grade in breast cancer. Int. J. Cancer 2009; 124(9): 2088-97. [CrossRef]
  • 43. Morohashi S, Kusumi T, Sato F, Odagiri H, Chiba H, Yoshihara S, et al. Decreased expression of claudin-1 corraletes with recurrence status in breast cancer. Int. J. Mol. Med. 2007; 20(2): 139-43. [CrossRef]
  • 44. McSherry EA, McGee SF, Jirstrom K, Doyle EM., Brennan DJ., Landberg G, et al. JAM-A expression positively correlates with poor prognosis in breast cancer patients. Int J Cancer 2009; 125(6): 1343-51. [CrossRef]
  • 45. Naik UP, Eckfeld K. Junctional adhesion molecule 1 (JAM-1). J Biol Regul Homeost Agents 2003; 17(4): 341- 7.
  • 46. Tian Y, Tian Y, Zhang W, Wei F, Yang J, Luo X, et al. Junctional adhesion molecule-A, an epithelial-mesenchymal transition inducer, correlates with metastasis and poor prognosis in human nasopharyngeal cancer. Carcinogenesis 2015; 36: 41-8. [CrossRef]
  • 47. Ikeo K, Oshima T, Shan J, Matsui H, Tomita T, Fukui H. et al. Junctional adhesion molecule-A promotes proliferation and inhibits apoptosis of gastric cancer. Hepato-Gastroenterol. 2015; 62(138): 540-5.
  • 48. Zhao H, Yu H, Martin TA, Zhang Y, Chen G, Jiang WG. Effect of junctional adhesion molecule-2 expression on cell growth, invasion and migration in human colorectal cancer. Internatial Journal of Oncology 2016; 48: 929-6. [CrossRef]
  • 49. Garrido-Urbani S, Vonlaufen A, Stalin J, De Grandis M, Ropraz P, Jemelin S,et al. Junctional adhesion molecule C (JAM-C) dimerization aids cancer cell migration and metastasis. Biochim Biophys Acta Mol Cell Res. 2018; 1865(4): 638-49. [CrossRef]
  • 50. Lee HM, Hwang KA, Choi KC. Diverse pathways of epithelial mesenchymal transition related with cancer progression and metastasis and potential effects on endocrine distrupting chemicals on epithelial mesenchymal transition process. Molecular and Cellular Endocrinology 2017; 457: 103-13. [CrossRef]

Kanser ve Metastaz: Hücre Adezyon Molekülleri ve Hücreler Arası Bağlantıların Önemi

Year 2020, Volume: 10 Issue: 1, 38 - 48, 13.03.2020
https://doi.org/10.26650/experimed.2020.0003

Abstract

Kanser hücrelerinde metastaz pek çok biyokimyasal ve moleküler faktör tarafından yönlendirilen kompleks bir süreçtir. Metastaz kanser tedavilerinde yüksek oranda sınırlayıcı bir faktör olup kanserden ölümlerin %90’ından sorumludur. Bu nedenle kanser metastazında altta yatan mekanizmaların aydınlatılması kanser metastazının önlenmesi için tedavi yöntemleri geliştirmek açısından önemlidir. Metastaz, lokal invazyon (epitelyal-mezenkimal geçiş), intravazasyon, dolaşımda sağkalım, ekstravazasyon (transendotelyal migrasyon/diapedez), mikrometastaz oluşumu ve metastatik koloni oluşumu gibi basamakları içermektedir. Tümör hücreleri integrin selektin gibi adezyon moleküllerinde yaptıkları ekspresyon değişimleri aracılığıyla plateletleri ‘‘kalkan’’ ve endotele bağlanmak için ‘‘aracı’’ olarak kullanarak dolaşımdaki immün sistem hücrelerinden ve apoptoztan kaçarlar. Tümör hücrelerinde ekstravazasyon metastazın anahtar basamaklardan biridir ve moleküllerde ufak farklılıklar olsa da tüm süreç temel olarak lökositlerde olduğu gibidir; yuvarlanma, adezyon ve transmigrasyon (diapedez). İntegrinler gibi hücre adezyon molekülleri ve Jam proteinleri gibi hücreler arası bağlantılar ekstravazasyon aşamasında kilit rollere sahiptir. Bu sebeple hücre adezyon molekülleri ve hücreler arası bağlantılar kanser tedavisinde potansiyel hedefler olarak kullanılabilir. Bu derlemede kanser metastazında yer alan genel süreçler ile hücre adezyon molekülleri ve hücreler arası bağlantıların metastazdaki rolleri özetlenmiştir.

References

  • 1. Reymond N, d'Águal BB, Ridley AJ. Crossing the endothelial barrier during metastasis. Nature Reviews Cancer 2013; 13(12): 858-70. [CrossRef]
  • 2. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011; 147: 275-92. [CrossRef]
  • 3. Pacmayr E, Treese C, Stein U. Underlying Mechanisms for Distant Metastasis - Molecular Biology. Visc Med. 2017; 33: 11-20. [CrossRef]
  • 4. Knights AJ., Funnell APW, Crossley M, Pearson CMR. Holding Tight: Cell Junctions and Cancer Spread. Trends Cancer Res. 2012; 8: 61-9.
  • 5. Sökeland G, Schumacher U. The functional role of integrins during intra- and extravasation within the metastatic cascade. Molecular Cancer 2019; 18:12. [CrossRef]
  • 6. Gheldof A, Berx G. Cadherins and epithelial-to-mesenchymal transition. Prog Mol Biol Transl Sci. 2013; 116: 317-36. [CrossRef]
  • 7. Farahani E, Patra HK, Jangamreddy JR, Rashedi I, Kawalec M, Rao Pariti RK, et al. Cell adhesion molecules and their relation to (cancer) cell stemness. Carcinogenesis 2014; 35(4): 747-59. [CrossRef]
  • 8. Anderberg C, Cunha SI, Zhai Z, Cortez E, Pardali E, Johnson JR, et al. Deficiency for endoglin in tumor vasculature weakens the endothelial barrier to metastatic dissemination. J. Exp. Med. 2013; 210: 563-79. [CrossRef]
  • 9. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-74. [CrossRef]
  • 10. Erler JT, Bennewith KL, Nicolau M, Dornhöfer N, Kong C, Le QT, et al. Lysyl oxidase is essential for hypoxia -induced metastasis. Nature 2006; 440: 1222-6. [CrossRef]
  • 11. Kozłowski J, KozłowskaA, Kocki J. Breast cancer metastasis - insight into selected molecular mechanisms of the phenomenon. Postepy Hig Med Dosw 2015; 69: 447-51. [CrossRef]
  • 12. Paoli P, Giannoni E, Chiarugi P. Anoikis molecular pathways and its role in cancer progression. Biochim Biophys Acta 2013; 1833(12): 3481-98. [CrossRef]
  • 13. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009; 9: 239-52. [CrossRef]
  • 14. Yan M, Jurasz P. The role of platelets in the tumor microenvironment: from solid tumors to leukemia. Biochim Biophys Acta 2016; 1863: 392-400. [CrossRef]
  • 15. Weil RJ, Palmieri DC, Bronder JL, Stark AM, Steeg PS. Breast cancer metastasis to the central nervous system. Am. J. Pathol. 2005; 167: 913-20. [CrossRef]
  • 16. Sarvaiya PJ, Guo D, Ulasov I, Gabikian P, Lesniak MS. Chemokines in tumor progression and metastasis. Oncotarget 2013; 4: 217185. [CrossRef]
  • 17. DeNardo DG, Barreto JB, Andreu P, Vasquez L, Tawfik D, Kolhatkar N, et al. CD4+ cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009; 16: 91-102. [CrossRef]
  • 18. Gocheva V, Wang HW, Gadea BB, Shree T, Hunter KE, Garfall AL, et al. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev. 2010; 24: 241-55. [CrossRef]
  • 19. Strell C, Entschladen F. Extravasation of leukocytes in comparison to tumor cells. Cell Communication and Signaling 2008; 6: 10. [CrossRef]
  • 20. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005; 438: 820-7. [CrossRef]
  • 21. Psaila B, Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer 2009; 9: 285-93. [CrossRef]
  • 22. Makrilia N, Kollias A, Manolopoulos L, Sygios K. Cell adhesion molecules: role and clinical significance in cancer. Cancer Invest. 2009; 27: 1023-37. [CrossRef]
  • 23. Harjunpää H, Llort Asens M, Guenther C, Fagerholm SC. Cell Adhesion Molecules and Their Roles and Regulation in the Immune and Tumor Microenvironment. Front. Immunol. 2019; 10:1078. [CrossRef]
  • 24. Bendas G, Borsig L. Cancer cell adhesion and metastasis: selectins, integrins and, the inhibitory potential of heparins. Int J Cell Biol. 2012; 2012: 676731. [CrossRef]
  • 25. Ludwig RJ, Boehme B, Podda M, Henscheler R, Jager E, Tandi C, et al. Endothelial P selectin as a target of heparin action in experimental melanoma lung metastasis. Cancer Research 2004; 64(8): 2743-50. [CrossRef]
  • 26. Laubli H, Borsig L. Selectins as mediators of lung metastasis. Cancer Microenvironment 2010; 3(1): 97-105. [CrossRef]
  • 27. Van Roy F, Berx G.The cell-cell adhesion molecule E-cadherin. Cell. Mol. Life Sci. 2008; 65: 3756-88. [CrossRef]
  • 28. Cao ZQ, Wang Z, Leng P. Aberrant N-cadherin expression in cancer. Biomedicine & Pharmacotherapy 2019; 118: 109320. [CrossRef]
  • 29. Vestweber D. VE-cadherin: The major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arteriosclerosis, Thrombosis, and Vascular Biology 2008; 28(2): 223-32. [CrossRef]
  • 30. Qureshi HS, Linden MD, Divine G. E-cadherin status in breast cancer correlates with histologic type but does not correlate with established prognostic parameters. Am J Clin Pathol 2006; 125: 377-85. [CrossRef]
  • 31. Elmoneim HM, Zaghoul NM. Expression of E-cadherin, N-cadherin and snail and therir correlation with clinopathological variant: an immunohistochemical study of 132 invasive ductal breast carsinomas in Egypt. Clinics (Sao Paulo) 2011; 66(10): 1765-71.
  • 32. Paredes J, Correia AL, Ribeiro AS, Milanezi F, Cameselle-Teijeiro J, Schmitt FC. Breast carcinomas that co-express E- and P- cadherin are associated with p120-cathenin cytoplasmatic localisation and poor patient survival. Journal Clin Pathol. 2008; 61: 856-62. [CrossRef]
  • 33. Shin K, Fogg VC, Margolis B. Tight junctions and cell polarity. Annu Rev Cell Dev Biol. 2006; 22: 207-235. [CrossRef]
  • 34. Barczyk M, Carracedo S, Gullberg D. Integrins. Cell Tissue Res. 2010; 339: 269-80. [CrossRef]
  • 35. Lahlou H, Muller WJ. β1-integrins signaling and mammary tumor progression in transgenic mouse models: implications for human breast cancer. Breast Cancer Research 2011; 13: 229. [CrossRef]
  • 36. Hamidi H, Pietila M, Ivaska J. The complexity of integrins in cancer and new scopes for therapeutic targeting. British Journal of Cancer 2016; 115: 1017-23. [CrossRef]
  • 37. Khapare N, Kundu ST, Sehgal L, Sawant M., Priya R, Gosavi P, et al. Plakhophilin3 leads to an increase in PRL3 levels promoting K8 dephosphorylation, which is required for transformation and metastasis. PLoS One 2012; 7:e38561. [CrossRef]
  • 38. Aaltomaa S, Karja V, Lipponen P, Isotalo T, Kankkunnen JP, Talja M, et al. Reduced α- and, β-catenin expression predicts shortened survival in local prostate cancer. Anticancer Research 2005; 25: 4707-4712.
  • 39. Salvador E, Burek M, Förster CY. Tight Junctions and the Tumor Microenvironment. Curr Pathobiol Rep. 2016; 4: 135-45. [CrossRef]
  • 40. Martin TA, Mansel RE, Jiang WG. Loss of occludin leads to the progression of human breast cancer. Int. J. Mol. Med. 2010; 26 (5): 723-34. [CrossRef]
  • 41. Osanai M, Murata M, Nishikiori N, Chiba H, Kojima T, Sawada N. Epigenetic silencing of occludin promotes tumorigenic and metastatic properties of cancer cells via modulations of unique sets of apoptosis-associated genes. Cancer Research 2006; 66(18): 912533. [CrossRef]
  • 42. Lanigan F, McKiernan E, Brennan DJ, Hegarty S, Millikan RC, McBryan J, et al. Increased claudin-4 expression is associated with poor prognosis and high tumor grade in breast cancer. Int. J. Cancer 2009; 124(9): 2088-97. [CrossRef]
  • 43. Morohashi S, Kusumi T, Sato F, Odagiri H, Chiba H, Yoshihara S, et al. Decreased expression of claudin-1 corraletes with recurrence status in breast cancer. Int. J. Mol. Med. 2007; 20(2): 139-43. [CrossRef]
  • 44. McSherry EA, McGee SF, Jirstrom K, Doyle EM., Brennan DJ., Landberg G, et al. JAM-A expression positively correlates with poor prognosis in breast cancer patients. Int J Cancer 2009; 125(6): 1343-51. [CrossRef]
  • 45. Naik UP, Eckfeld K. Junctional adhesion molecule 1 (JAM-1). J Biol Regul Homeost Agents 2003; 17(4): 341- 7.
  • 46. Tian Y, Tian Y, Zhang W, Wei F, Yang J, Luo X, et al. Junctional adhesion molecule-A, an epithelial-mesenchymal transition inducer, correlates with metastasis and poor prognosis in human nasopharyngeal cancer. Carcinogenesis 2015; 36: 41-8. [CrossRef]
  • 47. Ikeo K, Oshima T, Shan J, Matsui H, Tomita T, Fukui H. et al. Junctional adhesion molecule-A promotes proliferation and inhibits apoptosis of gastric cancer. Hepato-Gastroenterol. 2015; 62(138): 540-5.
  • 48. Zhao H, Yu H, Martin TA, Zhang Y, Chen G, Jiang WG. Effect of junctional adhesion molecule-2 expression on cell growth, invasion and migration in human colorectal cancer. Internatial Journal of Oncology 2016; 48: 929-6. [CrossRef]
  • 49. Garrido-Urbani S, Vonlaufen A, Stalin J, De Grandis M, Ropraz P, Jemelin S,et al. Junctional adhesion molecule C (JAM-C) dimerization aids cancer cell migration and metastasis. Biochim Biophys Acta Mol Cell Res. 2018; 1865(4): 638-49. [CrossRef]
  • 50. Lee HM, Hwang KA, Choi KC. Diverse pathways of epithelial mesenchymal transition related with cancer progression and metastasis and potential effects on endocrine distrupting chemicals on epithelial mesenchymal transition process. Molecular and Cellular Endocrinology 2017; 457: 103-13. [CrossRef]
There are 50 citations in total.

Details

Primary Language Turkish
Subjects Clinical Sciences
Journal Section Review
Authors

Gülçin Özkara This is me 0000-0002-4383-6890

Oğuz Öztürk This is me 0000-0002-2439-9269

Hülya Yılmaz Aydoğan This is me 0000-0002-8837-6664

Publication Date March 13, 2020
Submission Date February 25, 2020
Published in Issue Year 2020 Volume: 10 Issue: 1

Cite

Vancouver Özkara G, Öztürk O, Yılmaz Aydoğan H. Kanser ve Metastaz: Hücre Adezyon Molekülleri ve Hücreler Arası Bağlantıların Önemi. Experimed. 2020;10(1):38-4.