Table of Contents Author Guidelines Submit a Manuscript
Gastroenterology Research and Practice
Volume 2014 (2014), Article ID 580159, 7 pages
http://dx.doi.org/10.1155/2014/580159
Review Article

Colorectal Cancer and Basement Membranes: Clinicopathological Correlations

1st Department of Pathology, School of Medicine, National and Kapodistrian University of Athens, 11527 Athens, Greece

Received 29 October 2014; Accepted 16 December 2014; Published 28 December 2014

Academic Editor: Michel Kahaleh

Copyright © 2014 Charalampos C. Mylonas and Andreas C. Lazaris. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. R. Fearon and B. Vogelstein, “A genetic model for colorectal tumorigenesis,” Cell, vol. 61, no. 5, pp. 759–767, 1990. View at Publisher · View at Google Scholar
  2. S. D. Markowitz and M. M. Bertagnolli, “Molecular basis of colorectal cancer,” New England Journal of Medicine, vol. 361, no. 25, pp. 2449–2460, 2009. View at Publisher · View at Google Scholar
  3. J. Ferlay, H. R. Shin, F. Bray et al., GLOBOCAN 2008 v2.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10, International Agency for Research on Cancer, Lyon, France, 2010, http://globocan.iarc.fr/.
  4. R. R. Langley and I. J. Fidler, “The seed and soil hypothesis revisited—the role of tumor-stroma interactions in metastasis to different organs,” International Journal of Cancer, vol. 128, no. 11, pp. 2527–2535, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Robert, “Biology of cancer metastasis,” Bulletin du Cancer, vol. 100, no. 4, pp. 333–342, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. F. T. Bosman, World Health Organization, International Agency for Research on Cancer. Who Classification of Tumors of the Digestive System, International Agency for Research on Cancer, Lyon, France, 2010.
  7. A. I. Haq, J. Schneeweiss, V. Kalsi, and M. Arya, “The Dukes staging system: a cornerstone in the clinical management of colorectal cancer,” The Lancet Oncology, vol. 10, no. 11, p. 1128, 2009. View at Publisher · View at Google Scholar
  8. C. E. Dukes, “The classification of cancer of the rectum,” The Journal of Pathology and Bacteriology, vol. 35, no. 3, pp. 323–332, 1932. View at Publisher · View at Google Scholar
  9. I. Gockel, G. Sgourakis, O. Lyros et al., “Risk of lymph node metastasis in submucosal esophageal cancer: a review of surgically resected patients,” Expert Review of Gastroenterology and Hepatology, vol. 5, no. 3, pp. 371–384, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. D. Cunningham, W. Atkin, H.-J. Lenz et al., “Colorectal cancer,” The Lancet, vol. 375, no. 9719, pp. 1030–1047, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Shinto, K. Baker, H. Tsuda et al., “Tumor buds show reduced expression of laminin-5 gamma 2 chain in DNA mismatch repair deficient colorectal cancer,” Diseases of the Colon and Rectum, vol. 49, no. 8, pp. 1193–1202, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. J. García-Solano, P. Conesa-Zamora, J. Trujillo-Santos, D. Torres-Moreno, M. J. Mäkinen, and M. Pérez-Guillermo, “Immunohistochemical expression profile of β-catenin, E-cadherin, P-cadherin, laminin-5γ2 chain, and SMAD4 in colorectal serrated adenocarcinoma,” Human Pathology, vol. 43, no. 7, pp. 1094–1102, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. T. D. Tisty and L. M. Coussens, “Tumor stroma and regulation of cancer development,” Annual Review of Pathology Mechanisms of Disease, vol. 1, pp. 119–150, 2006. View at Publisher · View at Google Scholar
  14. N. H. Le, P. Franken, and R. Fodde, “Tumour-stroma interactions in colorectal cancer: converging on β-catenin activation and cancer stemness,” British Journal of Cancer, vol. 98, no. 12, pp. 1886–1893, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Zhang and J. Liu, “Tumor stroma as targets for cancer therapy,” Pharmacology & Therapeutics, vol. 137, no. 2, pp. 200–215, 2013. View at Google Scholar
  16. R. Timpl and J. C. Brown, “Supramolecular assembly of basement membranes,” BioEssays, vol. 18, no. 2, pp. 123–132, 1996. View at Publisher · View at Google Scholar · View at Scopus
  17. P. D. Yurchenco, “Basement membranes: cell scaffoldings and signaling platforms,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 2, Article ID a004911, 2011. View at Publisher · View at Google Scholar
  18. P. D. Yurchenco and J. J. O'Rear, “Basal lamina assembly,” Current Opinion in Cell Biology, vol. 6, no. 5, pp. 674–681, 1994. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Lohi, “Laminin-5 in the progression of carcinomas,” International Journal of Cancer, vol. 94, no. 6, pp. 763–767, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. H. K. Kleinman and G. R. Martin, “Matrigel: basement membrane matrix with biological activity,” Seminars in Cancer Biology, vol. 15, no. 5, pp. 378–386, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. N. Miosge, “The ultrastructural composition of basement membranes in vivo,” Histology and Histopathology, vol. 16, no. 4, pp. 1239–1248, 2001. View at Google Scholar · View at Scopus
  22. F. L. Chan and S. Inoue, “Lamina lucida of basement membrane: an artefact,” Microscopy Research and Technique, vol. 28, no. 1, pp. 48–59, 1994. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Aumailley, L. Bruckner-Tuderman, W. G. Carter et al., “A simplified laminin nomenclature,” Matrix Biology, vol. 24, no. 5, pp. 326–332, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. R. E. Hewitt, D. G. Powe, K. Morrell et al., “Laminin and collagen IV subunit distribution in normal and neoplastic tissues of colorectum and breast,” British Journal of Cancer, vol. 75, no. 2, pp. 221–229, 1997. View at Google Scholar
  25. S. Ricard-Blum, “The collagen family,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 1, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. J. D. Hood and D. A. Cheresh, “Role of integrins in cell invasion and migration,” Nature Reviews Cancer, vol. 2, no. 2, pp. 91–100, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. K. K. Ganguly, S. Pal, S. Moulik, and A. Chatterjee, “Integrins and metastasis,” Cell Adhesion & Migration, vol. 7, no. 3, pp. 251–261, 2014. View at Publisher · View at Google Scholar
  28. M. J. Bissell and D. Radisky, “Putting tumours in context,” Nature Reviews Cancer, vol. 1, no. 1, pp. 46–54, 2001. View at Publisher · View at Google Scholar
  29. E. Roeb and S. Matern, “Matrix metalloproteinases and colorectal cancer,” Medizinische Klinik, vol. 98, no. 12, pp. 763–770, 2003. View at Google Scholar
  30. S. Zucker and J. Vacirca, “Role of matrix metalloproteinases (MMPs) in colorectal cancer,” Cancer and Metastasis Reviews, vol. 23, no. 1-2, pp. 101–117, 2004. View at Publisher · View at Google Scholar
  31. E. Stadler and M. Dziadek, “Extracellular matrix penetration by epithelial cells is influenced by quantitative changes in basement membrane components and growth factors,” Experimental Cell Research, vol. 229, no. 2, pp. 360–369, 1996. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Simon-Assmann, G. Orend, E. Mammadova-Bach, C. Spenlé, and O. Lefebvre, “Role of laminins in physiological and pathological angiogenesis,” The International Journal of Developmental Biology, vol. 55, no. 4-5, pp. 455–465, 2011. View at Publisher · View at Google Scholar
  33. R. V. Iozzo, J. J. Zoeller, and A. Nyström, “Basement membrane proteoglycans: modulators Par Excellence of cancer growth and angiogenesis,” Molecules and Cells, vol. 27, no. 5, pp. 503–513, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Kalluri, “Basement membranes: structure, assembly and role in tumour angiogenesis,” Nature Reviews Cancer, vol. 3, no. 6, pp. 422–433, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. M. C. Ryan, R. Tizard, D. R. VanDevanter, and W. G. Carter, “Cloning of the LamA3 gene encoding the α3 chain of the adhesive ligand epiligrin expression in wound repair,” Journal of Biological Chemistry, vol. 269, no. 36, pp. 22779–22787, 1994. View at Google Scholar · View at Scopus
  36. D. R. Gerecke, D. W. Wagman, M. F. Champliaud, and R. E. Burgeson, “The complete primary structure for a novel laminin chain, the laminin B1k chain,” The Journal of Biological Chemistry, vol. 269, no. 15, pp. 11073–11080, 1994. View at Google Scholar
  37. P. Kallunki, K. Sainio, R. Eddy et al., “A truncated laminin chain homologous to the B2 chain: structure, spatial expression, and chromosomal assignment,” Journal of Cell Biology, vol. 119, no. 3, pp. 679–693, 1992. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Aumailley, “The laminin family,” Cell Adhesion & Migration, vol. 7, no. 1, pp. 48–55, 2013. View at Google Scholar
  39. P. Simon-Assmann and M. Kedinger, “Heterotypic cellular cooperation in gut morphogenesis and differentiation,” Seminars in Cell Biology, vol. 4, no. 3, pp. 221–230, 1993. View at Publisher · View at Google Scholar
  40. H. Mizushima, N. Koshikawa, K. Moriyama et al., “Wide distribution of laminin-5 γ2 chain in basement membranes of various human tissues,” Hormone Research, vol. 50, supplement 2, pp. 7–14, 1998. View at Publisher · View at Google Scholar · View at Scopus
  41. I. Sordat, F. T. Bosman, G. Dorta et al., “Differential expression of laminin-5 subunits and integrin receptors in human colorectal neoplasia,” The Journal of Pathology, vol. 185, no. 1, pp. 44–52, 1998. View at Publisher · View at Google Scholar
  42. P. Rousselle, G. P. Lunstrum, D. R. Keene, and R. E. Burgeson, “Kalinin: an epithelium-specific basement membrane adhesion molecule that is a component of anchoring filaments,” The Journal of Cell Biology, vol. 114, no. 3, pp. 567–576, 1991. View at Publisher · View at Google Scholar · View at Scopus
  43. D. Aberdam, T. Virolle, and P. Simon-Assmann, “Transcriptional regulation of laminin gene expression,” Microscopy Research and Technique, vol. 51, no. 3, pp. 228–237, 2000. View at Google Scholar
  44. I. Sordat, P. Rousselle, P. Chaubert et al., “Tumor cell budding and laminin5 expression in colorectal carcinoma can be modulated by the tissue microenvironment,” International Journal of Cancer, vol. 88, no. 5, pp. 708–717, 2000. View at Google Scholar
  45. F. Hlubek, A. Jung, N. Kotzor, T. Kirchner, and T. Brabletz, “Expression of the invasion factor laminin γ2 in colorectal carcinomas is regulated by -catenin,” Cancer Research, vol. 61, no. 22, pp. 8089–8093, 2001. View at Google Scholar · View at Scopus
  46. N. A. Wong and M. Pignatelli, “β-catenin—a linchpin in colorectal carcinogenesis?” American Journal of Pathology, vol. 160, no. 2, pp. 389–401, 2002. View at Publisher · View at Google Scholar
  47. C. M. Guess, B. J. LaFleur, B. L. Weidow, and V. A. Quaranta, “A decreased ratio of laminin-332 β3 to γ2 subunit mRNA is associated with poor prognosis in colon cancer,” Cancer Epidemiology Biomarkers & Prevention, vol. 18, no. 5, pp. 1584–1590, 2009. View at Publisher · View at Google Scholar
  48. M. G. Nievers, R. Q. J. Schaapveld, and A. Sonnenberg, “Biology and function of hemidesmosomes,” Matrix Biology, vol. 18, no. 1, pp. 5–17, 1999. View at Publisher · View at Google Scholar · View at Scopus
  49. G. Giannelli, J. Falk-Marzillier, O. Schiraldi, W. G. Stetler-Stevenson, and V. Quaranta, “Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5,” Science, vol. 277, no. 5323, pp. 225–228, 1997. View at Publisher · View at Google Scholar · View at Scopus
  50. N. Koshikawa, G. Giannelli, V. Cirulli, K. Miyazaki, and V. J. Quaranta, “Role of the cell surface MT1-MMP in epithelial over laminin-5,” The Journal of Cell Biology, vol. 148, no. 3, pp. 615–624, 2000. View at Google Scholar
  51. P. Rousselle and K. Beck, “Laminin 332 processing impacts cellular behavior,” Cell Adhesion & Migration, vol. 7, no. 1, pp. 122–134, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Schenk, E. Hintermann, M. Bilban et al., “Binding to EGF receptor of a laminin-5 EGF-like fragment liberated during MMP-dependent mammary gland involution,” Journal of Cell Biology, vol. 161, no. 1, pp. 197–209, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. J. P. Thiery, “Epithelial-mesenchymal transitions in development and pathologies,” Current Opinion in Cell Biology, vol. 15, no. 6, pp. 740–746, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Brabletz, A. Jung, S. Spaderna, F. Hlubek, and T. Kirchner, “Migrating cancer stem cells—an integrated concept of malignant tumour progression,” Nature Reviews Cancer, vol. 5, no. 9, pp. 744–749, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Brabletz, F. Hlubek, S. Spaderna et al., “Invasion and metastasis in colorectal cancer: epithelial-mesenchymal transition, mesenchymal-epithelial transition, stem cells and β-catenin,” Cells Tissues Organs, vol. 179, no. 1-2, pp. 56–65, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Brabletz, A. Jung, S. Reu et al., “Variable β-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 18, pp. 10356–10361, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. A. C. Lazaris, A. N. Tzoumani, I. Thimara et al., “Immunohistochemical assessment of basement membrane components in colorectal cancer: prognostic implications,” Journal of Experimental & Clinical Cancer Research, vol. 22, no. 4, pp. 599–606, 2003. View at Google Scholar · View at Scopus
  58. S. Spaderna, O. Schmalhofer, F. Hlubek et al., “A transient, EMT-linked loss of basement membranes indicates metastasis and poor survival in colorectal cancer,” Gastroenterology, vol. 131, no. 3, pp. 830–840, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Shi, B. Yu, H. Gao, J. Mu, and C. Ji, “Matrix metalloproteinase 2 overexpression and prognosis in colorectal cancer: a meta-analysis,” Molecular Biology Reports, vol. 40, no. 1, pp. 617–623, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Y. Li, P. Yuan, S. S. Lin et al., “Matrix metalloproteinase 9 expression and prognosis in colorectal cancer: a meta-analysis,” Tumor Biology, vol. 34, no. 2, pp. 735–741, 2013. View at Google Scholar
  61. A. H. Mekkawy, M. H. Pourgholami, and D. L. Morris, “Involvement of urokinase-type plasminogen activator system in cancer: an overview,” Medicinal Research Reviews, vol. 34, no. 5, pp. 918–956, 2014. View at Publisher · View at Google Scholar
  62. V. V. Delektorskaya and N. E. Kushlinskii, “Clinical significance of the content of biomolecular markers in invasive front of colon carcinomas,” Bulletin of Experimental Biology and Medicine, vol. 150, no. 3, pp. 368–371, 2011. View at Publisher · View at Google Scholar
  63. S. Aoki, Y. Nakanishi, S. Akimoto et al., “Prognostic significance of laminin-5 γ2 chain expression in colorectal carcinoma: immunohistochemical analysis of 103 cases,” Diseases of the Colon and Rectum, vol. 45, no. 11, pp. 1520–1527, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. C. Lenander, J. K. Habermann, Ä. Öst et al., “Laminin-5 γ2 chain expression correlates with unfavorable prognosis in colon carcinomas,” Analytical Cellular Pathology, vol. 22, no. 4, pp. 201–209, 2001. View at Google Scholar · View at Scopus
  65. E. Shinto, H. Tsuda, H. Ueno et al., “Prognostic implication of laminin-5 gamma 2 chain expression in the invasive front of colorectal cancers, disclosed by area-specific four-point tissue microarrays,” Laboratory Investigation, vol. 85, no. 2, pp. 257–266, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. C. Lenander, U. J. Roblick, J. K. Habermann, A. Ost, and K. Tryggvason, “Laminin 5 gamma 2 chain expression: a marker of early invasiveness in colorectal adenomas,” Molecular Pathology, vol. 56, no. 6, pp. 342–346, 2003. View at Google Scholar
  67. J. K. Habermann, M. B. Upender, U. J. Roblick et al., “Pronounced chromosomal instability and multiple gene amplifications characterize ulcerative colitis-associated colorectal carcinomas,” Cancer Genetics and Cytogenetics, vol. 147, no. 1, pp. 9–17, 2003. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Ogawa, K. Ikeuchi, M. Watanabe et al., “Expression of matrix metalloproteinase 7, laminin and type IV collagen-associated liver metastasis in human colorectal cancer: immunohistochemical approach,” Hepato-Gastroenterology, vol. 52, no. 63, pp. 875–880, 2005. View at Google Scholar · View at Scopus
  69. M. V. Gulubova and T. I. Vlaykova, “Significance of tenascin-C, fibronectin, laminin, collagen IV, α5β1 and α9β1 integrins and fibrotic capsule formation around liver metastases originating from cancers of the digestive tract,” Neoplasma, vol. 53, no. 5, pp. 372–383, 2006. View at Google Scholar · View at Scopus
  70. D. G. Jayne, R. M. Heath, O. Dewhurst, N. Scott, and P. J. Guillou, “Extracellular matrix proteins and chemoradiotherapy: α5β1 integrin as a predictive marker in rectal cancer,” European Journal of Surgical Oncology, vol. 28, no. 1, pp. 30–36, 2002. View at Publisher · View at Google Scholar · View at Scopus
  71. Y. Kikkawa, K. Hozumi, F. Katagiri, M. Nomizu, H. K. Kleinman, and J. E. Koblinski, “Laminin-111-derived peptides and cancer,” Cell Adhesion and Migration, vol. 7, no. 1, pp. 150–159, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. N. Pouliot and N. Kusuma, “Laminin-511: a multi-functional adhesion protein regulating cell migration, tumor invasion and metastasis,” Cell Adhesion and Migration, vol. 7, no. 1, pp. 142–149, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. A. De Arcangelis, O. Lefebvre, A. Méchine-Neuville et al., “Overexpression of laminin alpha1 chain in colonic cancer cells induces an increase in tumor growth,” International Journal of Cancer, vol. 94, no. 1, pp. 44–53, 2001. View at Publisher · View at Google Scholar
  74. N. Pouliot, E. C. Nice, and A. W. Burgess, “Laminin-10 mediates basal and EGF-stimulated motility of human colon carcinoma cells via α3β1 and α6β4 integrins,” Experimental Cell Research, vol. 266, no. 1, pp. 1–10, 2001. View at Publisher · View at Google Scholar · View at Scopus