Colorectal Cancer Metastases Settle in the Hepatic Microenvironment Through α5β1 Integrin

Journal of Cellular Biochemistry

Volumn 116, Issue 10, 2015, Pages 2385-2396

  Pelillo, Chiara ^a   Bergamo, Alberta ^a   Mollica, Hilaria ^a   Bestagno, Marco ^b   Sava, Gianni ^a,c  

^a Callerio Foundation   (Italy)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^c UNIVERSITY OF TRIESTE   (Italy)

Author keywords

COLON CANCER; FOCAL ADHESION KINASE; INTEGRINS; MICROENVIRONMENT

Indexed keywords

CELL ADHESION MOLECULE; FOCAL ADHESION KINASE; VERY LATE ACTIVATION ANTIGEN 5; FIBRONECTIN; FOCAL ADHESION KINASE 1; INTEGRIN ALPHAVBETA1; PTK2 PROTEIN, HUMAN; VITRONECTIN RECEPTOR;

ADHERENT CELL; ARTICLE; CANCER GROWTH; COLORECTAL CANCER; CONTROLLED STUDY; CULTURE MEDIUM; EXTRACELLULAR MATRIX; HCT116 CELL LINE; HUMAN; HUMAN CELL; LIVER CELL; LIVER METASTASIS; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; TARGET ORGAN; TUMOR INVASION; TUMOR MICROENVIRONMENT; BIOSYNTHESIS; CELL PROLIFERATION; COLORECTAL TUMOR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL PROLIFERATION; COLORECTAL NEOPLASMS; EXTRACELLULAR MATRIX; FIBRONECTINS; FOCAL ADHESION KINASE 1; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HUMANS; NEOPLASM METASTASIS; PHOSPHORYLATION; RECEPTORS, VITRONECTIN; TUMOR MICROENVIRONMENT;

EID: 84939215847     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25189     Document Type: Article

References (55)

1. Asthagiri AR, Nelson CM, Horwitz AF, Lauffenburger DA,. 1999. Quantitative relationship among integrin-ligand binding, adhesion, and signaling via focal adhesion kinase and extracellular signal-regulated kinase 2. J Biol Chem 274: 27119-27127.
2. Balkwill F, Mantovani A,. 2001. Inflammation and cancer: Back to Virchow?. Lancet 357: 539-545.
3. Barbera-Guillem E, Rocha M, Alvarez A, Vidal-Vanaclocha F,. 1991. Differences in the lectin-binding patterns of the periportal and perivenous endothelial domains in the liver sinusoids. Hepatology 14: 131-139.
4. Bradford MM, 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72: 248-254.
5. Cutroneo KR, White SL, Chiu JF, Ehrlich HP,. 2006. Tissue fibrosis and carcinogenesis: Divergent or successive pathways dictate multiple molecular therapeutic targets for oligo decoy therapies. J Cell Biochem 97: 1161-1174.
6. DeMali KA, Wennerberg K, Burridge K,. 2003. Integrin signaling to the actin cytoskeleton. Curr Opin Cell Biol 15: 572-582.
7. Desgrosellier JS, Cheresh DA,. 2010. Integrins in cancer: Biological implications and therapeutic opportunities. Nat Rev 10: 9-22.
8. Friedl P, Alexander S,. 2011. Cancer Invasion and the Microenvironment: Plasticity and Reciprocity. Cell Rev 147: 992-1009.
9. Friedl P, Wolf K,. 2003. Tumour-cell invasion and migration: Diversity and escape mechanisms. Nat Rev Cancer 3: 362-374.
10. Friedrichs J, Helenius J, Müller DJ,. 2010. Stimulated single-cell force spectroscopy to quantify cell adhesion receptor crosstalk. Proteomics 10: 1455-1462.
11. Hanahan D, Coussens LM,. 2012. Accessories to the crime: Functions of cells recruited to the tumor microenvironment. Cancer Cell 21: 309-322.
12. Hood JD, Cheresh DA,. 2002. Role of integrins in cell invasion and migration. Nat Rev Cancer 2: 91-100.
13. Huhtala P, Humphries MJ, McCarthy JB, Tremble PM, Werb Z, Damsky CH,. 1995. Cooperative signaling by α5β1 and α4β1 integrins regulates metalloproteinase gene expression in fibroblasts adhering to fibronectin. J Cell Biol 129: 867-879.
14. Hynes RO, 1992. Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 69: 11-25.
15. Janouskova H, Ray AM, Noulet F, Lelong-Rebel I, Choulier L, Schaffner F, Lehmen M, Martin S, Teisinger J, Dontenwill M,. 2013. Activation of p53 pathway by Nutlin-3a inhibits the expression of the therapeutic target α5 integrin in colon cancer cells. Cancer Letters 336: 307-318.
16. Jia Y, Zeng ZZ, Markwart SM, Rockwood KF, Ignatoski KM, Ethier SP, Livant DL,. 2004. Integrin fibronectin receptors in matrix metalloproteinase 1-dependent invasion by breast cancer and mammary epithelial cells. Cancer Res 64: 8674-8681.
17. Joyce JA, Pollard JW,. 2009. Microenvironmental regulation of metastasis. Nat Rev Cancer 9: 239-252.
18. Kaplan RN, Rafii S, Lyden D,. 2006. Preparing the "soil": The premetastatic niche. Cancer Res 66: 11089-11093.
19. Kershenobich Stalnikowitz D, Weissbrod AB,. 2003. Liver fibrosis and inflammation. A review. Ann Hepatol 2: 159-163.
20. Kueng W, Silber E, Eppenberger U,. 1989. Quantification of cells cultured on 96-well plates. Anal Biochem 182: 16-19.
21. Kuphal S, Bauer R, Bosserhoff AK,. 2005. Integrin signaling in malignant melanoma. Cancer Met Rev 24: 195-222.
22. Leitinger B, 2011. Transmembrane collagen receptors. Annu Rev Cell Dev Biol 27: 265-290.
23. Liu TJ, LaFortune T, Honda T, Ohmori O, Hatakeyama S, Meyer T, Jackson D, de Groot J, Yung WK,. 2007. Inhibition of both focal adhesion kinase and insulin-like growth factor-I receptor kinase suppresses glioma proliferation in vitro and in vivo. Mol Cancer Ther 6: 1357-1367.
24. Livak KJ, Schmittgen TD,. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
25. Michael KE, Dumbauld DW, Burns KL, Hanks SK, Garcia AJ,. 2009. Focal adhesion kinase modulates cell adhesion strengthening via integrin activation. Mol Biol Cell 20: 2508-2519.
26. Millard M, Odde S, Neamati N,. 2011. Integrin targeted therapeutics. Theranostics 1: 154-188.
27. Mitra SK, Schlaepfer DD,. 2006. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 18: 516-523.
28. Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM,. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66.
29. Reyes CD, Petrie TA, Garcia AJ,. 2008. Mixed extracellular matrix ligands synergistically modulate integrin adhesion and signalling. J Cell Physiol 217: 450-458.
30. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR,. 2003. Cell migration: Integrating signals from front to back. Science 302: 1704-1709.
31. Roberts WG, Ung E, Whalen P, Cooper B, Hulford C, Autry C, Richter D, Emerson E, Liu J, Kath J, Coleman K, Yao L, Martinez-Alsina L, Lorenzen M, Berliner M, Luzzio M, Patel N, Schmitt E, LaGreca S, Jani J, Wessel M, Marr E, Griffor M, Vajdos F,. 2008. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res 68: 1935-1944.
32. Robertson JH, Iga AM, Sales KM, Winslet MC, Seifalian AM,. 2008. Integrins: A method of early intervention in the treatment of colorectal liver metastases. Curr Pharm Des 14: 296-305.
33. Robertson JH, Yang SY, Winslet MC, Seifalian AM,. 2009. Functional blocking of specific integrins inhibit colonic cancer migration. Clin Exp Metastasis 26: 769-780.
34. Roman J, Ritzenthaler JD, Roser-Page S, Sun X, Han S,. 2010. α5β1-integrin expression is essential for tumor progression in experimental lung cancer. Am J Respir Cell Mol Biol 43: 684-691.
35. Ruoslahti E, Reed JC,. 1994. Anchorage dependence, integrins, and apoptosis. Cell 77: 477-478.
36. Schaffner F, Ray AM, Dontenwill M,. 2013. Integrin α5β1, the fibronectin receptor, as a pertinent therapeutic target in solid tumors. Cancers 5: 27-47.
37. Schedin P, Keely PJ,. 2011. Mammary gland ECM remodeling, stiffness, and mechanosignaling in normal development and tumor progression. Cold Spring Harb Perspect Biol 3: a003228.
38. Scoazec JY, Feldman G,. 1991. Immunophenotyping study of endothelial cells of the human hepatic sinusoid: Results and functional implications. Hepatology 14: 789-797.
39. Shi Q, Boettiger D,. 2003. A novel mode for integrin-mediated signaling: Tethering is required for phosphorylation of FAK Y397. Mol Cell Biol 14: 4306-4315.
40. Shi Q, Hjelmeland AB, Keir ST, Song L, Wickman S, Jackson D, Ohmori O, Bigner DD, Friedman HS, Rich JN,. 2007. A novel low molecular weight inhibitor of focal adhesion kinase, TAE226, inhibits glioma growth. Mol Carcinog 46: 488-496.
41. Shibue T, Weinberg RA,. 2009. Integrin beta1-focal adhesion kinase signaling directs the proliferation of metastatic cancer cells disseminated in the lungs. Proc Natl Acad Sci USA 106: 10290-10295.
42. Sieg DJ, Hauck CR, Ilic D, Klingbeil CK, Schaefer E, Damsky CH, Schlaepfer DD,. 2000. FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol 2: 249-256.
43. Sieg DJ, Hauck CR, Schlapfer DD,. 1999. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J Cell Sci 112: 2677-2691.
44. Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, Warren JT, Bokesh H, Kenney S, Boyd MR,. 1990. New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst 82: 1107-1112.
45. Slack-Davis JK, Hershey ED, Theodorescu D, Frierson HF, Parsons JT,. 2009. Differential requirement for focal adhesion kinase signalling in cancer progression in the transgenic adenocarcinoma of the mouse prostate model. Mol Cancer Ther 8: 2470-2477.
46. Slack-Davis JK, Martin KH, Tilghman RW, Iwanicki M, Ung EJ, Autry C, Luzzio MJ, Cooper B, Kath JC, Roberts WG, Parsons JT,. 2007. Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem 282: 14845-14852.
47. Szabo G, Mandrekar P, Dolganiuc A,. 1997. Innate immune response and hepatic inflammation. Semin Liver Dis 27: 339-350.
48. van der Bij GJ, Oosterling SJ, Bögels M, Bhoelan F, Fluitsma DM, Beelen RHJ, Meijer S, van Egmond M,. 2008. Blocking α2 integrins on rat CC531s colon carcinoma cells prevents operation-induced augmentation of liver metastases outgrowth. Hepatology 47: 532-543.
49. Vidal-Vanaclocha F, 2011. The liver prometastatic reaction of cancer patients: Implications for microenvironment-dependent colon cancer gene regulation. Cancer Microenviron 4: 163-180.
50. Walsh C, Tanjoni I, Uryu S, Tomar A, Nam JO, Luo H, Phillips A, Patel N, Kwok C, McMahon G, Stupack DG, Schlaepfer D,. 2010. Oral delivery of PND-1186 FAK inhibitor decreases tumor growth and spontaneous breast to lung metastasis in pre-clinical models. Cancer Biol and Ther 9: 778-790.
51. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Danesky C, Bissell MJ,. 1997. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 137: 231-245.
52. Weiss L, 1992. Comments on hematogenous metastatic patterns in humans as revealed by autopsy. Clin Exp Met 10: 191-199.
53. White DE, Muller WJ,. 2007. Multifaceted roles of integrins in breast cancer metastasis. J Mammary Gland Biol Neoplasia 12: 135-142. www.nlm.nih.gov/medlineplus/cancers.html.
54. Yang C, Zeisberg M, Lively JC, Nyberg P, Afdhal N, Kalluri R,. 2003. Integrin α1β1 and α2β1 are key regulators of hepatocarcinoma cell invasion across the fibrotic matrix microenvironment. Cancer Res 63: 8312-8317.
55. Zeng ZZ, Jia Y, Markwart SM, Rockwood KF, Livant DL,. 2006. Role of focal adhesion kinase and phosphatidylinositol-3'-kinase in integrin fibronectin receptor-mediated, matrix metalloproteinase-1-dependent invasion by metastatic prostate cancer cells. Cancer Res 66: 8091-8099.