An immortalization-dependent switch in integrin function up-regulates MMP-9 to enhance tumor cell invasion

Cancer Research

Volumn 68, Issue 18, 2008, Pages 7371-7379

  Lamar, John M ^a   Pumiglia, Kevin M ^a   DiPersio, C Michael ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE B; INTEGRIN; PROTEIN P53; VERY LATE ACTIVATION ANTIGEN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INVASION; CELL ADHESION; CELL IMMORTALIZATION; CELL TRANSFORMATION; CONTROLLED STUDY; EPITHELIUM CELL; EXTRACELLULAR MATRIX; GENE CONTROL; GENE MUTATION; HUMAN; HUMAN CELL; KERATINOCYTE; MOUSE; NONHUMAN; ONCOGENE H RAS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SQUAMOUS CELL CARCINOMA; TUMOR CELL; TUMOR GROWTH; UPREGULATION;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TRANSFORMED; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; GENE EXPRESSION; HUMANS; INTEGRIN ALPHA3BETA1; KERATINOCYTES; MATRIX METALLOPROTEINASE 9; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 54749100830     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-1080     Document Type: Article

References (50)

1. Yuspa SH. The pathogenesis of squamous cell cancer: lessons learned from studies of skin carcinogenesis. J Dermatol Sci 1998;17:1-7.
2. Azzoli CG, Sagar M, Wu A, et al. Cooperation of p53 loss of function and v-Ha-ras in transformation of mouse keratinocyte cell lines. Mol Carcinog 1998;21:50-61.
3. Lehman TA, Modali R, Boukamp P, et al. p53 mutations in human immortalized epithelial cell lines. Carcinogenesis 1993;14:833-9.
4. Burns J, Barton C, Wynford-Thomas D, Lemoine N. In vitro transformation of epithelial cells by ras oncogenes. Epithelial Cell Biol 1993;2:26-43.
5. Ziegler A, Jonason AS, Leffell DJ, et al. Sunburn and p53 in the onset of skin cancer. Nature 1994;372:773-6.
6. Papathoma AS, Zoumpourlis V, Balmain A, Pintzas A. Role of matrix metalloproteinase-9 in progression of mouse skin carcinogenesis. Mol Carcinog 2001;31:74-82.
7. Campbell C, Quinn AG, Ro YS, Angus B, Rees JL. p53 mutations are common and early events that precede tumor invasion in squamous cell neoplasia of the skin. J Invest Dermatol 1993;100:746-8.
8. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 2002;110:673-87.
9. Brakebusch C, Bouvard D, Stanchi F, Sakai T, Fassler R. Integrins in invasive growth. J Clin Invest 2002;109:999-1006.
10. Guo W, Giancotti FG. Integrin signalling during tumour progression. Nat Rev Mol Cell Biol 2004;5:816-26.
11. Lipscomb EA, Mercurio AM. Mobilization and activation of a signaling competent α6β4 integrin underlies its contribution to carcinoma progression. Cancer Metastasis Rev 2005;24:413-23.
12. Raymond K, Kreft M, Song JY, Janssen H, Sonnenberg A. Dual Role of α6β4 integrin in epidermal tumor growth: tumor-suppressive versus tumor-promoting function. Mol Biol Cell 2007;18:4210-21.
13. McCawley LJ, Matrisian LM. Matrix metalloproteinases: they're not just for matrix anymore! Curr Opin Cell Biol 2001;13:534-40.
14. Bergers G, Brekken R, McMahon G, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000;2:737-44.
15. Coussens LM, Tinkle CL, Hanahan D, Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000;103:481-90.
16. Kupferman ME, Fini ME, Muller WJ, Weber R, Cheng Y, Muschel RJ. Matrix metalloproteinase 9 promoter activity is induced coincident with invasion during tumor progression. Am J Pathol 2000;157:1777-83.
17. Bernhard EJ, Muschel RJ, Hughes EN. Mr 92,000 gelatinase release correlates with the metastatic phenotype in transformed rat embryo cells. Cancer Res 1990;50:3872-7.
18. Davidson B, Goldberg I, Kopolovic J, et al. Expression of matrix metalloproteinase-9 in squamous cell carcinoma of the uterine cervix-clinicopathologic study using immunohistochemistry and mRNA in situ hybridization. Gynecol Oncol 1999;72:380-6.
19. Pyke C, Ralfkiaer E, Huhtala P, Hurskainen T, Dano K, Tryggvason K. Localization of messenger RNA for Mr 72,000 and 92,000 type IV collagenases in human skin cancers by in situ hybridization. Cancer Res 1992;52:1336-41.
20. Kreidberg JA. Functions of a3h1 integrin. Curr Opin Cell Biol 2000;12:548-53.
21. Nguyen BP, Ren XD, Schwartz MA, Carter WG. Ligation of integrin α3β1 by laminin 5 at the wound edge activates Rho-dependent adhesion of leading keratinocytes on collagen. J Biol Chem 2001;276:43860-70.
22. Marinkovich MP. Tumour microenvironment: laminin 332 in squamous-cell carcinoma. Nat Rev Cancer 2007;7:370-80.
23. Bartolazzi A, Cerboni C, Nicotra MR, Mottolese M, Bigotti A, Natali PG. Transformation and tumor progression are frequently associated with expression of the a3h1 heterodimer in solid tumors. Int J Cancer 1994;58:488-91.
24. Morini M, Mottolese M, Ferrari N, et al. The a3h1 integrin is associated with mammary carcinoma cell metastasis, invasion, and gelatinase B (MMP-9) activity. Int J Cancer 2000;87:336-42.
25. Wang H, Fu W, Im JH, et al. Tumor cell α3β1 integrin and vascular laminin-5 mediate pulmonary arrest and metastasis. J Cell Biol 2004;164:935-41.
26. Giannelli G, Falk-Marzillier J, Schiraldi O, Stetler-Stevenson WG, Quaranta V. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 1997;277:225-8.
27. DiPersio CM, Shao M, Di Costanzo L, Kreidberg JA, Hynes RO. Mouse keratinocytes immortalized with large T antigen acquire a3h1 integrin-dependent secretion of MMP-9/gelatinase B. J Cell Sci 2000;113:2909-21.
28. Kreidberg JA, Donovan MJ, Goldstein SL, et al. α 3 β 1 integrin has a crucial role in kidney and lung organogenesis. Development 1996;122:3537-47.
29. Donehower LA, Harvey M, Slagle BL, et al. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992;356:215-21.
30. Iyer V, Pumiglia K, DiPersio CM. α3β1 integrin regulates MMP-9 mRNA stability in immortalized keratinocytes: a novel mechanism of integrin-mediated MMP gene expression. J Cell Sci 2005;118:1185-95.
31. Lamar JM, Iyer V, DiPersio CM. Integrin α3β1 potentiates TGFβ-mediated induction of MMP-9 in immortalized keratinocytes. J Invest Dermatol 2008;128:575-86.
32. Mukhopadhyay S, Munshi HG, Kambhampati S, Sassano A, Platanias LC, Stack MS. Calcium-induced matrix metalloproteinase 9 gene expression is differentially regulated by ERK1/2 and p38 MAPK in oral keratinocytes and oral squamous cell carcinoma. J Biol Chem 2004;279:33139-46.
33. Meadows KN, Bryant P, Pumiglia K. Vascular endothelial growth factor induction of the angiogenic phenotype requires Ras activation. J Biol Chem 2001;276:49289-98.
34. Frank DE, Carter WG. Laminin 5 deposition regulates keratinocyte polarization and persistent migration. J Cell Sci 2004;117:1351-63.
35. Sehgal I, Thompson TC. Novel regulation of type IV collagenase (matrix metalloproteinase-9 and -2) activities by transforming growth factor-β1 in human prostate cancer cell lines. Mol Biol Cell 1999;10:407-16.
36. Jat PS, Noble MD, Ataliotis P, et al. Direct derivation of conditionally immortal cell lines from an H-2Kb-tsA58 transgenic mouse. Proc Natl Acad Sci U S A 1991;88:5096-100.
37. Levine AJ. Tumor suppressor genes. Bioessays 1990;12:60-6.
38. Safina A, Vandette E, Bakin AV. ALK5 promotes tumor angiogenesis by upregulating matrix metalloproteinase-9 in tumor cells. Oncogene 2006;26:2407-22.
39. Min BM, Baek JH, Shin KH, Gujuluva CN, Cherrick HM, Park NH. Inactivation of the p53 gene by either mutation or HPV infection is extremely frequent in human oral squamous cell carcinoma cell lines. Eur J Cancer B Oral Oncol 1994;30B:338-45.
40. Brash DE, Rudolph JA, Simon JA, et al. A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc Natl Acad Sci U S A 1991;88:10124-8.
41. Verdolini R, Amerio P, Goteri G, et al. Cutaneous carcinomas and preinvasive neoplastic lesions. Role of MMP-2 and MMP-9 metalloproteinases in neoplastic invasion and their relationship with proliferative activity and p53 expression. J Cutan Pathol 2001;28:120-6.
42. Franchi A, Santucci M, Masini E, Sardi I, Paglierani M, Gallo O. Expression of matrix metalloproteinase 1, matrix metalloproteinase 2, and matrix metalloproteinase 9 in carcinoma of the head and neck. Cancer 2002;95:1902-10.
43. Ozdemir E, Kakehi Y, Okuno H, Habuchi T, Okada Y, Yoshida O. Strong correlation of basement membrane degradation with p53 inactivation and/or MDM2 overexpression in superficial urothelial carcinomas. J Urol 1997;158:206-11.
44. Akool el S, Kleinert H, Hamada FM, et al. Nitric oxide increases the decay of matrix metalloproteinase 9 mRNA by inhibiting the expression of mRNA-stabilizing factor HuR. Mol Cell Biol 2003;23:4901-16.
45. Shetty P, Velusamy T, Bhandary YP, Shetty RS, Liu MC, Shetty S. Urokinase Expression by Tumor Suppressor Protein p53: A Novel Role in mRNA Turnover. Am J Respir Cell Mol Biol. Epub 2008.
46. Chang TC, Wentzel EA, Kent OA, et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 2007;26:745-52.
47. Liu J. Control of protein synthesis and mRNA degradation by microRNAs. Curr Opin Cell Biol 2008;20:214-21.
48. Segrelles C, Ruiz S, Santos M, Martinez-Palacio J, Lara MF, Paramio JM. Akt mediates an angiogenic switch in transformed keratinocytes. Carcinogenesis 2004;25:1137-47.
49. Mira E, Lacalle RA, Buesa JM, et al. Secreted MMP9 promotes angiogenesis more efficiently than constitutive active MMP9 bound to the tumor cell surface. J Cell Sci 2004;117:1847-57.
50. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002;295:2387-92.