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PMID: 19308686 Published · ppublish English Journal Article

Role of cancer microenvironment in metastasis: focus on colon cancer.

Cancer microenvironment : official journal of the International Cancer Microenvironment Society ·Vol. 1 ·No. 1 ·2008-12-00 ·Pages 69-83

Gout S, Huot J

Abstract

One person on three will receive a diagnostic of cancer during his life. About one third of them will die of the disease. In most cases, death will result from the formation of distal secondary sites called metastases. Several events that lead to cancer are under genetic control. In particular, cancer initiation is tightly associated with specific mutations that affect proto-oncogenes and tumour suppressor genes. These mutations lead to unrestrained growth of the primary neoplasm and a propensity to detach and to progress through the subsequent steps of metastatic dissemination. This process depends tightly on the surrounding microenvironment. In fact, several studies support the point that tumour development relies on a continuous cross-talk between cancer cells and their cellular and extracellular microenvironments. This signaling cross-talk is mediated by transmembrane receptors expressed on cancer cells and stromal cells. The aim of this manuscript is to review how the cancer microenvironment influences the journey of a metastatic cell taking liver invasion by colorectal cancer cells as a model.

Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Gout Stéphanie
Le Centre de recherche en cancérologie de l'Université Laval, L'Hôtel-Dieu de Québec, 9 rue McMahon, Quebec, Canada.
Huot Jacques
References (150)
150 references, click to expand
  1. Integrins can directly mediate metastatic tumor cell adhesion within the liver sinusoids.
    J Gastrointest Surg. 2004 Dec;8(8):1049-59; discussion 1060 PMID: 15585393
  2. B16 melanoma cell arrest in the mouse liver induces nitric oxide release and sinusoidal cytotoxicity: a natural hepatic defense against metastasis.
    Cancer Res. 2000 Oct 15;60(20):5862-9 PMID: 11059784
  3. The epithelial-mesenchymal transition (EMT) and colorectal cancer progression.
    Cancer Biol Ther. 2005 Apr;4(4):365-70 PMID: 15846061
  4. Src SH3/2 domain-mediated peripheral accumulation of Src and phospho-myosin is linked to deregulation of E-cadherin and the epithelial-mesenchymal transition.
    Mol Biol Cell. 2004 Jun;15(6):2794-803 PMID: 15075377
  5. Extracellular matrix modulates expression of growth factors and growth-factor receptors in liver-colonizing colon-cancer cell lines.
    Int J Cancer. 1998 Jul 17;77(2):295-301 PMID: 9650567
  6. Angiopoietin-1 promotes lymphatic sprouting and hyperplasia.
    Blood. 2005 Jun 15;105(12):4642-8 PMID: 15746084
  7. Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts.
    Cancer Res. 2007 Nov 1;67(21):10123-8 PMID: 17974953
  8. The A9 antigen associated with aggressive human squamous carcinoma is structurally and functionally similar to the newly defined integrin alpha 6 beta 4.
    Cancer Res. 1991 May 1;51(9):2395-402 PMID: 1750876
  9. Basal cell-specific and hyperproliferation-related keratins in human breast cancer.
    Am J Pathol. 1991 Mar;138(3):751-63 PMID: 1705754
  10. Co-culturing human prostate carcinoma cells with hepatocytes leads to increased expression of E-cadherin.
    Br J Cancer. 2007 Apr 23;96(8):1246-52 PMID: 17406365
  11. Pancreatic carcinomas deposit laminin-5, preferably adhere to laminin-5, and migrate on the newly deposited basement membrane.
    Am J Pathol. 1997 Nov;151(5):1289-302 PMID: 9358755
  12. Hypoxia inducible factor-1 independent pathways in tumor angiogenesis.
    Clin Cancer Res. 2007 Oct 1;13(19):5670-4 PMID: 17908955
  13. Soluble CD44 secretion contributes to the acquisition of aggressive tumor phenotype in human colon cancer cells.
    Exp Mol Pathol. 2007 Dec;83(3):341-6 PMID: 17945213
  14. Apoptosis: an early event in metastatic inefficiency.
    Cancer Res. 2001 Jan 1;61(1):333-8 PMID: 11196183
  15. Preexisting lymphatic endothelium but not endothelial progenitor cells are essential for tumor lymphangiogenesis and lymphatic metastasis.
    Cancer Res. 2004 Jun 1;64(11):3737-40 PMID: 15172976
  16. Targeted tumor therapy with the TGF-beta 2 antisense compound AP 12009.
    Cytokine Growth Factor Rev. 2006 Feb-Apr;17(1-2):129-39 PMID: 16377233
  17. Clinical, cellular, and molecular aspects of cancer invasion.
    Physiol Rev. 2003 Apr;83(2):337-76 PMID: 12663862
  18. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy.
    J Exp Med. 2001 Mar 19;193(6):727-40 PMID: 11257139
  19. Using a xenograft model of human breast cancer metastasis to find genes associated with clinically aggressive disease.
    Cancer Res. 2005 Jul 1;65(13):5578-87 PMID: 15994930
  20. Cancer: an inflammatory link.
    Nature. 2004 Sep 23;431(7007):405-6 PMID: 15385993
  21. Metastasis: quantitative analysis of distribution and fate of tumor emboli labeled with 125 I-5-iodo-2'-deoxyuridine.
    J Natl Cancer Inst. 1970 Oct;45(4):773-82 PMID: 5513503
  22. The gamma 2 chain of kalinin/laminin 5 is preferentially expressed in invading malignant cells in human cancers.
    Am J Pathol. 1994 Oct;145(4):782-91 PMID: 7943170
  23. Colon cancer metastatic to the lung and the thyroid gland.
    Arch Surg. 2006 Jan;141(1):93-6 PMID: 16415418
  24. Laminin-5 is a marker of invading cancer cells in some human carcinomas and is coexpressed with the receptor for urokinase plasminogen activator in budding cancer cells in colon adenocarcinomas.
    Cancer Res. 1995 Sep 15;55(18):4132-9 PMID: 7664291
  25. Lymphangiogenesis in colorectal cancer--prognostic and therapeutic aspects.
    Int J Cancer. 2007 Oct 1;121(7):1401-9 PMID: 17640040
  26. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome.
    Science. 2006 Sep 29;313(5795):1960-4 PMID: 17008531
  27. Adhesion Molecules: The Path to a New Understanding of Acute Inflammation.
    News Physiol Sci. 2000 Jun;15:107-113 PMID: 11390891
  28. Cell adhesion and signalling by cadherins and Ig-CAMs in cancer.
    Nat Rev Cancer. 2004 Feb;4(2):118-32 PMID: 14964308
  29. Intravasation-related metastatic factors in colorectal cancer.
    Tumour Biol. 2004 Jan-Apr;25(1-2):48-55 PMID: 15192312
  30. Pre-EMTing metastasis? Recapitulation of morphogenetic processes in cancer.
    Clin Exp Metastasis. 2007;24(8):587-97 PMID: 17978854
  31. Induction of E-selectin expression on vascular endothelium by digestive system cancer cells.
    J Gastroenterol. 1996 Apr;31(2):299-301 PMID: 8680556
  32. Epithelial-mesenchymal transition and colorectal cancer: gaining insights into tumor progression using LIM 1863 cells.
    Cells Tissues Organs. 2007;185(1-3):29-39 PMID: 17587805
  33. Imatinib mesylate inhibits proliferation and modulates cytokine expression of human cancer-associated stromal fibroblasts from colorectal metastases.
    Cancer Lett. 2007 Jun 8;250(2):329-38 PMID: 17141949
  34. Chemokines and the molecular basis of cancer metastasis.
    N Engl J Med. 2001 Sep 13;345(11):833-5 PMID: 11556308
  35. Lethal deformation of cancer cells in the microcirculation: a potential rate regulator of hematogenous metastasis.
    Int J Cancer. 1992 Jan 2;50(1):103-7 PMID: 1728600
  36. Tiam1 regulates cell adhesion, migration and apoptosis in colon tumor cells.
    Clin Exp Metastasis. 2006;23(5-6):301-13 PMID: 17086355
  37. Tumour vascularization: sprouting angiogenesis and beyond.
    Cancer Metastasis Rev. 2007 Dec;26(3-4):489-502 PMID: 17717633
  38. NKG2D recognition and perforin effector function mediate effective cytokine immunotherapy of cancer.
    J Exp Med. 2004 Nov 15;200(10):1325-35 PMID: 15545356
  39. Metastasis: a question of life or death.
    Nat Rev Cancer. 2006 Jun;6(6):449-58 PMID: 16723991
  40. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism.
    Mol Biol Cell. 2001 Jan;12(1):27-36 PMID: 11160820
  41. The role of gelatinases in colorectal cancer progression and metastasis.
    Biochim Biophys Acta. 2004 Dec 17;1705(2):69-89 PMID: 15588763
  42. Hypoxia: a key regulator of angiogenesis in cancer.
    Cancer Metastasis Rev. 2007 Jun;26(2):281-90 PMID: 17603752
  43. The host inflammatory response promotes liver metastasis by increasing tumor cell arrest and extravasation.
    Am J Pathol. 2007 May;170(5):1781-92 PMID: 17456781
  44. A critical step in metastasis: in vivo analysis of intravasation at the primary tumor.
    Cancer Res. 2000 May 1;60(9):2504-11 PMID: 10811132
  45. Sulfated glycosphingolipid as mediator of phagocytosis: SM4s enhances apoptotic cell clearance and modulates macrophage activity.
    J Immunol. 2007 Nov 15;179(10):6770-82 PMID: 17982067
  46. [Extraction and identification of circulating immune complexes from the serum of cancer patient by affinity chromatography followed by high pressure steric exclusion chromatography. Demonstration of their effect on the mitogenesis of normal lymphocytes].
    Ann Med Interne (Paris). 1982;133(5):362-6 PMID: 7149514
  47. Expression of hemidesmosomal and extracellular matrix proteins by normal and malignant human prostate tissue.
    Am J Pathol. 1995 Jun;146(6):1498-507 PMID: 7778688
  48. Mechanisms of metastasis: epithelial-to-mesenchymal transition and contribution of tumor microenvironment.
    J Cell Biochem. 2007 Jul 1;101(4):816-29 PMID: 17243120
  49. Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors.
    Cancer Res. 1995 Jul 1;55(13):2752-5 PMID: 7796399
  50. Colorectal cancer.
    BMJ. 2007 Oct 6;335(7622):715-8 PMID: 17916855
  51. Fibroblasts in cancer.
    Nat Rev Cancer. 2006 May;6(5):392-401 PMID: 16572188
  52. Hepatocyte growth factor inhibits anoikis in head and neck squamous cell carcinoma cells by activation of ERK and Akt signaling independent of NFkappa B.
    J Biol Chem. 2002 Jul 12;277(28):25203-8 PMID: 11994287
  53. Coagulation facilitates tumor cell spreading in the pulmonary vasculature during early metastatic colony formation.
    Cancer Res. 2004 Dec 1;64(23):8613-9 PMID: 15574768
  54. Molecular determinants in the biology of liver metastasis.
    Surg Oncol Clin N Am. 1996 Apr;5(2):215-29 PMID: 9019348
  55. Role of lymphangiogenesis in cancer.
    J Clin Oncol. 2007 Sep 20;25(27):4298-307 PMID: 17878481
  56. Plasminogen activators and inhibitor type 1 in neoplastic colonic tissue from patients with familial adenomatous polyposis.
    Br J Cancer. 1995 Feb;71(2):393-6 PMID: 7841059
  57. Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis.
    J Cell Biol. 2000 Feb 21;148(4):779-90 PMID: 10684258
  58. Development of lymphatic vessels: tumour lymphangiogenesis and lymphatic invasion.
    Curr Med Chem. 2005;12(26):3043-53 PMID: 16375699
  59. Chemokines and leukocyte traffic.
    Nature. 1998 Apr 9;392(6676):565-8 PMID: 9560152
  60. T-cell death and cancer immune tolerance.
    Cell Death Differ. 2008 Jan;15(1):70-9 PMID: 18007660
  61. New approaches in angiogenic targeting for colorectal cancer.
    World J Gastroenterol. 2007 Nov 28;13(44):5857-66 PMID: 17990351
  62. Potential role of doppler perfusion index in selection of patients with colorectal cancer for adjuvant chemotherapy.
    Lancet. 2000 Jan 1;355(9197):34-7 PMID: 10615889
  63. Regulation of transendothelial migration of colon cancer cells by E-selectin-mediated activation of p38 and ERK MAP kinases.
    Oncogene. 2006 Oct 26;25(50):6563-73 PMID: 16715142
  64. Complex networks orchestrate epithelial-mesenchymal transitions.
    Nat Rev Mol Cell Biol. 2006 Feb;7(2):131-42 PMID: 16493418
  65. Galectin-1: a link between tumor hypoxia and tumor immune privilege.
    J Clin Oncol. 2005 Dec 10;23(35):8932-41 PMID: 16219933
  66. Tumor necrosis factor-alpha stimulates the epithelial-to-mesenchymal transition of human colonic organoids.
    Mol Biol Cell. 2003 May;14(5):1790-800 PMID: 12802055
  67. Transcriptional induction of the urokinase receptor gene by a constitutively active Src. Requirement of an upstream motif (-152/-135) bound with Sp1.
    J Biol Chem. 1999 Jun 25;274(26):18428-37 PMID: 10373450
  68. Dendritic cell vaccination.
    Expert Rev Vaccines. 2007 Aug;6(4):617-33 PMID: 17669014
  69. Expression of surface protein receptors in lung cancer.
    Anticancer Res. 2002 Nov-Dec;22(6C):4039-43 PMID: 12553029
  70. Microvessel morphology and vascular endothelial growth factor expression in human colonic carcinoma with or without metastasis.
    Lab Invest. 2002 May;82(5):555-62 PMID: 12003996
  71. Escape from immune- and nonimmune-mediated tumor surveillance.
    Semin Cancer Biol. 2006 Feb;16(1):16-31 PMID: 16140546
  72. Inhibition of tumor angiogenesis as a strategy to circumvent acquired resistance to anti-cancer therapeutic agents.
    Bioessays. 1991 Jan;13(1):31-6 PMID: 1722975
  73. The genetics of colorectal cancer.
    Ann Intern Med. 2002 Oct 1;137(7):603-12 PMID: 12353948
  74. In vivo natural killer cell activities revealed by natural killer cell-deficient mice.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2731-6 PMID: 10694580
  75. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis.
    Cell. 2006 Jan 27;124(2):263-6 PMID: 16439202
  76. Involvement of tumor necrosis factor-related apoptosis-inducing ligand in NK cell-mediated and IFN-gamma-dependent suppression of subcutaneous tumor growth.
    Cell Immunol. 2001 Dec 15;214(2):194-200 PMID: 12088418
  77. Phosphorylation of p68 RNA helicase plays a role in platelet-derived growth factor-induced cell proliferation by up-regulating cyclin D1 and c-Myc expression.
    J Biol Chem. 2007 Jun 8;282(23):16811-9 PMID: 17412694
  78. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium.
    Cancer Res. 1999 Oct 1;59(19):5002-11 PMID: 10519415
  79. The Fas counterattack: Fas-mediated T cell killing by colon cancer cells expressing Fas ligand.
    J Exp Med. 1996 Sep 1;184(3):1075-82 PMID: 9064324
  80. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies.
    J Pathol. 2002 Mar;196(3):254-65 PMID: 11857487
  81. The role of E-selectin for neutrophil activation and tumor metastasis in vivo.
    Leukemia. 1997 Apr;11 Suppl 3:209-12 PMID: 9209343
  82. A urokinase-type plasminogen activator deficiency diminishes the frequency of intestinal adenomas in ApcMin/+ mice.
    J Pathol. 2007 Nov;213(3):266-74 PMID: 17893885
  83. Epithelial--mesenchymal and mesenchymal--epithelial transitions in carcinoma progression.
    J Cell Physiol. 2007 Nov;213(2):374-83 PMID: 17680632
  84. Critical steps in hematogenous metastasis: an overview.
    Surg Oncol Clin N Am. 2001 Apr;10(2):243-55, vii PMID: 11382585
  85. Role of nitric oxide and superoxide anion in elimination of low metastatic human colorectal carcinomas by unstimulated hepatic sinusoidal endothelial cells.
    Cancer Res. 1998 Apr 1;58(7):1524-31 PMID: 9537259
  86. Clinical translation of angiogenesis inhibitors.
    Nat Rev Cancer. 2002 Oct;2(10):727-39 PMID: 12360276
  87. The chemokine receptor CXCR4 is required for outgrowth of colon carcinoma micrometastases.
    Cancer Res. 2003 Jul 1;63(13):3833-9 PMID: 12839981
  88. Constitutive and stimulated expression of ICAM-1 protein on pulmonary endothelial cells in vivo.
    Microvasc Res. 1997 Sep;54(2):135-44 PMID: 9327384
  89. VEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cells.
    Blood. 2003 Jan 1;101(1):168-72 PMID: 12393704
  90. Carbohydrate-mediated cell adhesion in cancer metastasis and angiogenesis.
    Cancer Sci. 2004 May;95(5):377-84 PMID: 15132763
  91. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression.
    Nat Cell Biol. 2000 Feb;2(2):76-83 PMID: 10655586
  92. Lymphatic endothelium: a new frontier of metastasis research.
    Nat Cell Biol. 2002 Jan;4(1):E2-5 PMID: 11780131
  93. Effector memory T cells, early metastasis, and survival in colorectal cancer.
    N Engl J Med. 2005 Dec 22;353(25):2654-66 PMID: 16371631
  94. Epithelial-mesenchymal transitions in tumour progression.
    Nat Rev Cancer. 2002 Jun;2(6):442-54 PMID: 12189386
  95. Integrin beta 1 signaling is necessary for transforming growth factor-beta activation of p38MAPK and epithelial plasticity.
    J Biol Chem. 2001 Dec 14;276(50):46707-13 PMID: 11590169
  96. Analysis of the tumor-associated antigen TSP-180. Identity with alpha 6-beta 4 in the integrin superfamily.
    J Biol Chem. 1989 Sep 15;264(26):15515-21 PMID: 2475502
  97. Cancer metastasis: tumor cell and host organ properties important in metastasis to specific secondary sites.
    Biochim Biophys Acta. 1988 Nov 15;948(2):175-224 PMID: 3052592
  98. Color Doppler vascularity index can predict distant metastasis and survival in colon cancer patients.
    Cancer Res. 2000 Jun 1;60(11):2892-7 PMID: 10850434
  99. Endothelial cell migration during angiogenesis.
    Circ Res. 2007 Mar 30;100(6):782-94 PMID: 17395884
  100. The CXCR5 chemokine receptor is expressed by carcinoma cells and promotes growth of colon carcinoma in the liver.
    Cancer Res. 2006 Oct 1;66(19):9576-82 PMID: 17018614
  101. Expression of tumor antigen correlated with metastatic potential of Lewis lung carcinoma and B16 melanoma clones in mice.
    Cancer Res. 1986 Nov;46(11):5772-8 PMID: 3756921
  102. Biomechanical destruction of cancer cells in the heart: a rate regulator for hematogenous metastasis.
    Invasion Metastasis. 1988;8(4):228-37 PMID: 3170116
  103. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases.
    Am J Pathol. 1998 Sep;153(3):865-73 PMID: 9736035
  104. Elevated c-Src protein expression is an early event in colonic neoplasia.
    Lab Invest. 1998 Mar;78(3):365-71 PMID: 9520949
  105. Alphavbeta5-integrins mediate early steps of metastasis formation.
    Eur J Cancer. 2005 May;41(7):1065-72 PMID: 15862757
  106. Smoldering and polarized inflammation in the initiation and promotion of malignant disease.
    Cancer Cell. 2005 Mar;7(3):211-7 PMID: 15766659
  107. BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury.
    Nat Med. 2003 Jul;9(7):964-8 PMID: 12808448
  108. The epithelial-mesenchymal transition of colon carcinoma involves expression of IL-8 and CXCR-1-mediated chemotaxis.
    Exp Cell Res. 2004 Oct 1;299(2):315-24 PMID: 15350531
  109. Alpha 6 beta 4 integrin and newly deposited laminin-1 and laminin-5 form the adhesion mechanism of gastric carcinoma. Continuous expression of laminins but not that of collagen VII is preserved in invasive parts of the carcinomas: implications for acquisition of the invading phenotype.
    Am J Pathol. 1996 Sep;149(3):781-93 PMID: 8780383
  110. Soluble fibrin augments platelet/tumor cell adherence in vitro and in vivo, and enhances experimental metastasis.
    Clin Exp Metastasis. 1999;17(8):723-30 PMID: 10919717
  111. Preparing the "soil": the premetastatic niche.
    Cancer Res. 2006 Dec 1;66(23):11089-93 PMID: 17145848
  112. Characterization of the host proinflammatory response to tumor cells during the initial stages of liver metastasis.
    Am J Pathol. 2005 Sep;167(3):749-59 PMID: 16127154
  113. Tumor microenvironment: the role of the tumor stroma in cancer.
    J Cell Biochem. 2007 Jul 1;101(4):805-15 PMID: 17226777
  114. Functional imaging of colorectal cancer angiogenesis.
    Lancet Oncol. 2007 Mar;8(3):245-55 PMID: 17329195
  115. Intratumoral cytokines/chemokines/growth factors and tumor infiltrating dendritic cells: friends or enemies?
    Cancer Metastasis Rev. 2006 Sep;25(3):333-56 PMID: 17029028
  116. Death receptor-3, a new E-Selectin counter-receptor that confers migration and survival advantages to colon carcinoma cells by triggering p38 and ERK MAPK activation.
    Cancer Res. 2006 Sep 15;66(18):9117-24 PMID: 16982754
  117. Tumor-stroma interactions in pancreatic ductal adenocarcinoma.
    Mol Cancer Ther. 2007 Apr;6(4):1186-97 PMID: 17406031
  118. The hallmarks of cancer.
    Cell. 2000 Jan 7;100(1):57-70 PMID: 10647931
  119. Vascular endothelial growth factor secretion by tumor-infiltrating macrophages essentially supports tumor angiogenesis, and IgG immune complexes potentiate the process.
    Cancer Res. 2002 Dec 1;62(23):7042-9 PMID: 12460925
  120. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition.
    J Cell Biol. 2006 Jul 17;174(2):175-83 PMID: 16831886
  121. Progress in human tumour immunology and immunotherapy.
    Nature. 2001 May 17;411(6835):380-4 PMID: 11357146
  122. The integrin alpha6beta4 functions in carcinoma cell migration on laminin-1 by mediating the formation and stabilization of actin-containing motility structures.
    J Cell Biol. 1997 Dec 29;139(7):1873-84 PMID: 9412479
  123. Anoikis and metastatic potential of cloudman S91 melanoma cells.
    Cancer Res. 2001 Feb 15;61(4):1707-16 PMID: 11245487
  124. Role of cancer-associated stromal fibroblasts in metastatic colon cancer to the liver and their expression profiles.
    Oncogene. 2004 Sep 23;23(44):7366-77 PMID: 15326482
  125. Cancerous colonic polyps. "Hands on" or "hands off?".
    Am Surg. 1990 Mar;56(3):148-52 PMID: 2180352
  126. Selectins and selectin ligands in extravasation of cancer cells and organ selectivity of metastasis.
    Clin Exp Metastasis. 2008;25(4):335-44 PMID: 17891461
  127. The crucial role of macrophages in lymphangiogenesis.
    J Clin Invest. 2005 Sep;115(9):2316-9 PMID: 16138185
  128. Tumor angiogenesis: cause or consequence of cancer?
    Cancer Res. 2007 Aug 1;67(15):7059-61 PMID: 17671171
  129. Type VII collagen antibody LH 7.2 identifies basement membrane characteristics of thin malignant melanomas.
    J Pathol. 1989 Mar;157(3):243-7 PMID: 2647941
  130. Tumour-educated macrophages promote tumour progression and metastasis.
    Nat Rev Cancer. 2004 Jan;4(1):71-8 PMID: 14708027
  131. Induction of interleukin-8 preserves the angiogenic response in HIF-1alpha-deficient colon cancer cells.
    Nat Med. 2005 Sep;11(9):992-7 PMID: 16127434
  132. Lymphangiogenesis in development and human disease.
    Nature. 2005 Dec 15;438(7070):946-53 PMID: 16355212
  133. Specific deletion of focal adhesion kinase suppresses tumor formation and blocks malignant progression.
    Genes Dev. 2004 Dec 15;18(24):2998-3003 PMID: 15601818
  134. Involvement of chemokine receptors in breast cancer metastasis.
    Nature. 2001 Mar 1;410(6824):50-6 PMID: 11242036
  135. Stromal fibroblasts in colorectal liver metastases originate from resident fibroblasts and generate an inflammatory microenvironment.
    Am J Pathol. 2007 Nov;171(5):1608-18 PMID: 17916596
  136. Targeting the expression of platelet-derived growth factor receptor by reactive stroma inhibits growth and metastasis of human colon carcinoma.
    Am J Pathol. 2006 Dec;169(6):2054-65 PMID: 17148668
  137. Src induces urokinase receptor gene expression and invasion/intravasation via activator protein-1/p-c-Jun in colorectal cancer.
    Mol Cancer Res. 2007 May;5(5):485-96 PMID: 17510314
  138. A nude mouse model of massive liver and lymph node metastasis of human colon cancer.
    Anticancer Res. 2000 Mar-Apr;20(2A):715-22 PMID: 10810345
  139. Molecular mechanisms for organ-specific colon carcinoma metastasis.
    Eur J Cancer. 1995 Jul-Aug;31A(7-8):1091-5 PMID: 7576998
  140. Ras and TGF[beta] cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways.
    J Cell Biol. 2002 Jan 21;156(2):299-313 PMID: 11790801
  141. Biomechanical destruction of cancer cells in skeletal muscle: a rate-regulator for hematogenous metastasis.
    Clin Exp Metastasis. 1989 Sep-Oct;7(5):483-91 PMID: 2752602
  142. Current views concerning the influences of murine hepatic endothelial adhesive and cytotoxic properties on interactions between metastatic tumor cells and the liver.
    Comp Hepatol. 2005 Dec 09;4:8 PMID: 16336680
  143. Reciprocal regulation of RhoA and RhoC characterizes the EMT and identifies RhoC as a prognostic marker of colon carcinoma.
    Oncogene. 2006 Nov 2;25(52):6959-67 PMID: 16715134
  144. Essential roles of tumor necrosis factor receptor p55 in liver metastasis of intrasplenic administration of colon 26 cells.
    Cancer Res. 2002 Nov 15;62(22):6682-7 PMID: 12438267
  145. Targeting transforming growth factor-beta signaling.
    Curr Opin Oncol. 2007 Nov;19(6):579-85 PMID: 17906455
  146. TGF-beta and epithelial-to-mesenchymal transitions.
    Oncogene. 2005 Aug 29;24(37):5764-74 PMID: 16123809
  147. Kinase substrate protein microarray analysis of human colon cancer and hepatic metastasis.
    Clin Chim Acta. 2005 Jul 24;357(2):180-3 PMID: 15921671
  148. Expression of P-selectin on endothelial cells is upregulated by LPS and TNF-alpha in vivo.
    Cell Adhes Commun. 1994 Apr;2(1):7-14 PMID: 7526954
  149. Combination of an SRC kinase inhibitor with a novel pharmacological antagonist of the urokinase receptor diminishes in vitro colon cancer invasiveness.
    Clin Cancer Res. 2004 Feb 15;10(4):1545-55 PMID: 14977859
  150. The tumor cell-host organ interface in the early onset of metastatic organ colonisation.
    Clin Exp Metastasis. 2008;25(2):171-81 PMID: 18058027
Article Info
Journal
Cancer microenvironment : official journal of the International Cancer Microenvironment Society
Abbr.
Cancer Microenviron
ISSN
1875-2292
DOI
10.1007/s12307-008-0007-2
Published
2008-12-00
Epub
2008-00-14
Pages
69-83
Language
English
Region
Netherlands
NLM ID
101322634
PMCID
PMC2654352
External Links
PubMed source DOI: 10.1007/s12307-008-0007-2 PMC Full Text
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