HGF and ligation of αvβ5 integrin induce a novel, cancer cell-specific gene expression required for cell scattering

Experimental Cell Research

Volumn 292, Issue 2, 2004, Pages 274-287

  Crouch, Sonya ^b   Spidel, Celee S ^b   Lindsey, J Suzanne ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b NONE

Author keywords

Antisense; c Met; Cell specific; Cross talk; Endometrial epithelial cells (EEC); Hepatocyte growth factor; Integrin; Scatter factor; Tumor stroma interaction

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; BLOCKING ANTIBODY; COMPLEMENTARY DNA; INTEGRIN; SCATTER FACTOR; ALPHAVBETA5 INTEGRIN; ANTIBODY; MESSENGER RNA; MIG 7 PROTEIN, HUMAN; MIG-7 PROTEIN, HUMAN; SCATTER FACTOR RECEPTOR; TUMOR MARKER; TUMOR PROTEIN; VITRONECTIN RECEPTOR;

ARTICLE; CANCER CELL; CARCINOMA CELL; CELL ISOLATION; CELL MIGRATION; CELL PROLIFERATION; COLON CARCINOMA; CONTROLLED STUDY; ENDOMETRIUM; ENDOMETRIUM CARCINOMA; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYBRIDIZATION; MESSENGER RNA SYNTHESIS; NUCLEOTIDE SEQUENCE; OVARY CELL; PRIORITY JOURNAL; SQUAMOUS CELL; AGED; AMINO ACID SEQUENCE; CANCER INVASION; CARCINOMA; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; METASTASIS; MIDDLE AGED; MOLECULAR GENETICS; STROMA CELL; TUMOR CELL LINE;

AGED; AGED, 80 AND OVER; AMINO ACID SEQUENCE; ANTIBODIES; BASE SEQUENCE; CARCINOMA; CELL LINE, TUMOR; DNA, COMPLEMENTARY; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATOCYTE GROWTH FACTOR; HUMANS; INTEGRINS; MIDDLE AGED; MOLECULAR SEQUENCE DATA; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM PROTEINS; OLIGORIBONUCLEOTIDES, ANTISENSE; PROTO-ONCOGENE PROTEINS C-MET; RECEPTORS, VITRONECTIN; RNA, MESSENGER; STROMAL CELLS; TRANSCRIPTION, GENETIC; TUMOR MARKERS, BIOLOGICAL;

EID: 0346362273     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2003.09.016     Document Type: Article

References (74)

1. Jian W., Hiscox S., Matsumoto K., Nakamura T. Hepatocyte growth factor/scatter factor, its molecular, cellular and clinical implications in cancer. Crit. Rev. Oncol./Hematol. 29:1999;209-248.
2. Vande Woude G.F., Jeffers M., Cortner J., Alvord G., Tsarfaty I., Resau J. Met-HGF/SF: tumorigenesis, invasion and metastasis. Ciba Found. Symp. 212:1997;119-130.
3. Bae-Jump V., Segreti E.M., Vandermolen D., Kauma S. Hepatocyte growth factor (HGF) induces invasion of endometrial carcinoma cell lines in vitro. Gynecol. Oncol. 73:1999;265-272.
4. Birchmeier W., Brinkmann V., Niemann C., Meiners S., DiCesare S., Naundorf H., Sachs M. Role of HGF/SF and c-Met in morphogenesis and metastasis of epithelial cells. Ciba Found. Symp. 212:1997;230-246.
5. 4 integrin in the control of HGF-dependent invasive growth. Cell. 107:2001;643-654.
6. Chan A.M., Rubin J.S., Bottaro D.P., Hirschfield D.W., Chedid M., Aaronson S.A. Identification of a competitive HGF antagonist encoded by an alternative transcript. Science. 251:1991;802-804.
7. Lokker N.A., Godowski P.J. Generation and characterization of a competitive antagonist of human hepatocyte growth factor, HGF/NK1. J. Biol. Chem. 268:1993;17145-17150.
8. Cao B., Su Y., Oskarsson M., Zhao P., Kort E.J., Fisher R.J., Wang L.M., Vande Woude G.F. Neutralizing monoclonal antibodies to hepatocyte growth factor/scatter factor (HGF/SF display antitumor activity in animal models. Proc. Natl. Acad. Sci. 98:2001;7443-7448.
9. Ferrara N. Vascular endothelial growth factor and the regulation of angiogenesis. Recent Prog. Horm. Res. 55:2000;15-36.
10. Imanishi J., Kamiyama K., Iguchi I., Kita M., Sotozono C., Kinoshita S. Growth factors: importance in wound healing and maintenance of transparency of the cornea. Prog. Retin. Eye Res. 19:2000;113-129.
11. van der Voort R., Keehnen R.M.J., Smit L., Groenink M., Pals S.T. Paracrine regulation of germinal center B cell adhesion through the c-Met-hepatocyte growth factor/scatter factor pathway. J. Exp. Med. 185:1997;2121-2131.
12. Watanabe L., Hirose M., Wang X.E., Kobayashi O., Nagahara A., Murai T., Iwazaki R., Miwa H., Miyazaki A., Sato N. Epithelial-mesenchymal interaction in gastric mucosal restoration. J. Gastroenterol. 35:2000;65-68.
13. Fuller K., Owens J., Chambers T.J. The effect of hepatocyte growth factor on the behaviour of osteoclasts. Biochem. Biophys. Res. Commun. 212:1995;334-340.
14. Grano M., Galimi F., Zambonin G., Colucci S., Cottone E., Zallone A.Z., Comoglio P.M. Hepatocyte growth factor is a coupling factor for osteoclasts and osteoblasts in vitro. Proc. Natl. Acad. Sci. 93:1996;7644-7648.
15. Jiang W.G., Hiscox S. Hepatocyte growth factor/scatter factor, a cytokine playing multiple and converse roles. Histol. Histopathol. 12:1997;537-555.
16. Fehlner-Gardiner C.C., Cao H., Jackson-Boeters L., Nakamura T., Elliott B.E., Uniyal S., Chan B.M. Characterization of a functional relationship between hepatocyte growth factor and mouse bone marrow-derived mast cells. Differentiation. 65:1999;27-42.
17. Byers S., Park M., Sommers C., Seslar S. Breast carcinoma: a collective disorder. Breast Cancer Res. Treat. 31:1994;203-215.
18. Beviglia L., Kramer R.H. HGF induces FAK activation and integrin-mediated adhesion in MTLn3 breast carcinoma cells. Int. J. Cancer. 83:1999;640-649.
19. Trusolino L., Cavassa S., Angelini P., Ando M., Bertotti A., Comoglio P.M., Boccaccio C. HGF/scatter factor selectively promotes cell invasion by increasing integrin avidity. FASEB J. 14:2000;1629-1640.
20. Rosen E.M., Meromsky L., Goldberg I.D., Bhargava M.M., Setter E. Studies on the mechanism of scatter factor. Effects of agents that modulate intracellular signal transduction, macromolecule synthesis and cytoskeleton assembly. J. Cell Sci. 96:1990;639-649.
21. Dunsmore S.E., Rubin J.S., Kovacs S.O., Chedid M., Parks W.C., Welgus H.G. Mechanisms of hepatocyte growth factor stimulation of keratinocyte metalloproteinase production. J. Biol. Chem. 271:1996;24576-24582.
22. Tuck A.B., Elliott B.E., Hota C., Tremblay E., Chambers A.F. Osteopontin-induced, integrin-dependent migration of human mammary epithelial cells involves activation of the hepatocyte growth factor receptor. J. Cell. Biochem. 78:2000;465-475.
23. Liang C.C., Chen H.C. Sustained activation of extracellular signal-regulated kinase stimulated by hepatocyte growth factor leads to integrin alpha 2 expression that is involved in cell scattering. J. Biol. Chem. 276:2001;21146-21152.
24. Miura H., Nishimura K., Tsujimura A., Matsumiya K., Matsumoto K., Nakamura T., Okuyama A. Effects of hepatocyte growth factor on E-cadherin-mediated cell-cell adhesion in DU145 prostate cancer cells. Urology. 58:2001;1064-1069.
25. Davies G., Jiang W.G., Mason M.D. Matrilysin mediates extracellular cleavage of E-cadherin from prostate cancer cells: a key mechanism in hepatocyte growth factor/scatter factor-induced cell-cell dissociation and in vitro invasion. Clin. Cancer Res. 7:2001;3289-3297.
26. Lindsey J.S., Wilkinson M.F. Pem: a testosterone- and LH-regulated homeobox gene expressed in mouse Sertoli cells and epididymis. Dev. Biol. 179:1996;471-484.
27. Witzenbichler B., Kureishi Y., Luo Z., Le Roux A., Branellec D., Walsh K. Regulation of smooth muscle cell migration and integrin expression by the Gax transcription factor. J. Clin. Invest. 104:1999;1469-1480.
28. Brooks P.C., Klemke R.L., Schon S., Lewis J.M., Schwartz M.A., Cheresh D.A. Insulin-like growth factor receptor cooperates with integrin alpha v beta 5 to promote tumor cell dissemination in vivo. J. Clin. Invest. 99:1997;1390-1398.
29. Fujisaki T., Tanaka Y., Fujii K., Mine S., Saito K., Yamada S., Yamashita U., Irimura T., Eto S. CD44 stimulation induces integrin-mediated adhesion of colon cancer cell lines to endothelial cells by up-regulation of integrins, c-Met and activation of integrins. Cancer Res. 59:1999;4427-4434.
30. Trusolino L., Serini G., Cecchini G., Besati C., Ambesi-Impiombato F.S., Marchisio P.C., De Filippi R. Growth Factor-dependent activation of ?v?3 integrin in normal epithelial cells: implications for tumor invasion. J. Cell Biol. 142:1998;1145-1156.
31. Moghul A., Lin L., Beedle A., Kanbour-Shakir A., DeFrances M.C., Liu Y., Zarnegar R. Modulation of c-MET proto-oncogene (HGF receptor) mRNA abundance by cytokines and hormones: evidence for rapid decay of the 8 kb c-MET transcript. Oncogene. 9:1994;2045-2052.
32. Emoto K., Yamada Y., Sawada H., Fujimoto H., Ueno M., Takayama T., Kamada K., Naito A., Hirao S., Nakajima Y. Annexin II overexpression correlates with stromal tenascin-C overexpression: a prognostic marker in colorectal carcinoma. Cancer. 92:2001;1419-1426.
33. Euer N., Schwirzke M., Evtimova V., Burtscher H., Jarsch M., Tarin D., Weidle U.H. Identification of genes associated with metastasis of mammary carcinoma in metastatic versus non-metastatic cell lines. Anticancer Res. 22:2002;733-740.
34. Matsuyama Y., Takao S., Aikou T. Comparison of matrix metalloproteinase expression between primary tumors with or without liver metastasis in pancreatic and colorectal carcinomas. J. Surg. Oncol. 80:2002;105-110.
35. Classen-Linke I., Kusche M., Knauthe R., Beier H.M. Establishment of a human endometrial cell culture system and characterization of its polarized hormone responsive epithelial cells. Cell Tissue Res. 287:1997;171-185.
36. Sugawara J., Fukaya T., Murakami T., Yoshida H., Yajima A. Hepatocyte growth factor stimulated proliferation, migration, and lumen formation of human endometrial epithelial cells in vitro. Biol. Reprod. 57:1997;936-942.
37. Chomczyncki P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocynate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
38. Shaefer B. Revolution in rapid amplification of cDNA ends: new strategies for polymerase chain reaction cloning of full-length cDNA ends. Anal. Biochem. 227:1995;255-273.
39. Diatchenko L., Lau Y.-F.C., Campbell A.P., Chenchik A., Moqadam F., Huang B., Lukyanov S., Lukyanov K., Gurskaya N., Sverdlov E.D., Siebert P.D. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc. Natl. Acad. Sci. 93:1996;6025-6030.
40. Dokras A., Gardner L.M.G., Seftor E.A., Hendrix M.J.C. Regulation of human cytotrophoblast morphogenesis hepatocyte growth factor/scatter factor. Biol. Reprod. 65:2001;1278-1288.
41. Uehara Y., Minowa O., Mori C., Shiota K., Kuno J., Noda T., Klagsbrun M. Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature. 373:1995;702-705.
42. To C.T., Tsao M.S. The roles of hepatocyte growth factor/scatter factor and met receptor in human cancers. Oncol. Rep. 5:1998;1013-1024.
43. Wagatsuma S., Konno R., Sato S., Yajima A. Tumor angiogenesis, hepatocyte growth factor, and c-Met expression in endometrial carcinoma. Cancer. 82:1998;520-530.
44. Di Renzo M.F., Olivero M., Katsaros D., Crepaldi T., Gaglia P., Zola P., Sismondi P., Comoglio P.M. Overexpression of the Met/HGF receptor in ovarian cancer. Int. J. Cancer. 58:1994;658-662.
45. Morello S., Olivero M., Aimetti M., Bernardi M., Berrone S., Di Renzo M.F., Giordano S. Met receptor is overexpressed but not mutated in oral squamous cell carcinomas. J. Cell. Physiol. 189:2001;285-290.
46. Fazekas K., Csuka O., Koves I., Raso E., Timar J. Experimental and clinicopathologic studies on the function of the HGF receptor in human colon cancer metastasis. Clin. Exp. Metastasis. 18:2000;639-649.
47. Clark D.E., Smith S.K., Sharkey A.M., Sowter H.M., Charnock-Jones D.S. Hepatocyte growth factor/scatter factor and its receptor c-met: localisation and expression in the human placenta throughout pregnancy. J. Endocrinol. 151:1996;459-467.
48. Lail-Trecker M., Fulati R., Peluso J.J. A role for hepatocyte growth factor/scatter factor in regulating normal and neoplastic cells of reproductive tissues. J. Soc. Gynecol. Investig. 5:1998;114-121.
49. Lindsey J.S., Brenner R.M. Novel hepatocyte growth factor/scatter factor isoform transcripts in the macaque endometrium and placenta. Mol. Hum. Reprod. 8:2002;81-87.
50. Matsumoto K., Nakamura T. Hepatocyte growth factor (HGF) as a tissue organizer for organogenesis and regeneration. Biochem. Biophys. Res. Commun. 239:1997;639-644.
51. Moriyama T., Kataoka H., Hamasuna R., Yokogami K., Uehara H., Kawano H., Goya T., Tsubouchi H., Koono M., Wakisaka S. Up-regulation of vascular endothelial growth factor induced by hepatocyte growth factor/scatter factor stimulation in human glioma cells. Biochem. Biophys. Res. Commun. 249:1998;73-77.
52. Parrott J.A., Skinner M.K. Developmental and hormonal regulation of hepatocyte growth factor expression and action in the bovine ovarian follicle. Biol. Reprod. 59:1998;553-560.
53. Weimar I.S., Miranda N., Muller E.J., Hekman A., Kerst J.M., deGast F.C., Gerritsen W.R. Hepatocyte growth factor/scatter factor (HGF/SF) is produced by human bone marrow stromal cells and promotes proliferation, adhesion and survival of human hematopoietic progenitor cells (CD34+). Exp. Hematol. 26:1998;885-894.
54. Zachow R.J., Weitsman S.R., Magoffin D.A. Hepatocyte growth factor regulates ovarian theca-interstitial cell differentiation and androgen production. Endocrinology. 138:1997;691-697.
55. FAK) and promotes migration and invasion by oral squamous cell carcinoma cells. J. Biol. Chem. 269:1994;31807-31820.
56. Hegerfeldt Y., Tusch M., Bröcker E.-B., Friedl P. Collective cell movement in primary melanoma explants: plasticity of cell-cell interaction, ?1 integrin function, and migration strategies. Cancer Res. 62:2002;2125-2130.
57. Jones J., Watt F.M., Speight P.M. Changes in the expression of alpha v integrins in oral squamous cell carcinomas. J. Oral Pathol. Med. 26:1997;63-68.
58. Klemke R.L., Yebra M., Bayna E.M., Cheresh D.A. Receptor tyrosine kinase signaling required for integrin alpha v beta 5-directed cell motility but not adhesion on vitronectin. J. Cell Biol. 127:1994;859-866.
59. Breuss J.M., DeLisser H.M., Klimanskaya I.V., Folkesson H.G., Pittet J.F., Nishimura S.L., Aldape K., Landers D.V., Carpenter W., Gillett N., Sheppard D., Matthay M.A., Albelda S.M., Kramer R.H., Pytela R. Expression of the ?6 integrin subunit in development, neoplasia and tissue repair suggests a role in epithelial remodeling. J. Cell Sci. 108:1995;2241-2251.
60. Munger J.S., Huang X., Kawakatsu H., Griffiths M.J., Dalton S.L., Wu J., Pittet J.F., Kaminski N., Garat C., Matthay M.A., Rifkin D.B., Sheppard D. The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell. 96:1999;319-328.
61. Gao J.X., Wilkins J., Issekutz A.C. Migration of human polymorphonuclear leukocytes through a synovial fibroblast barrier is mediated by both beta 2 (CD11/CD18) integrins and the beta 1 (CD29) integrins VLA-5 and VLA-6. Cell. Immunol. 163:1995;178-186.
62. Wayner E.A., Orland R.A., Cheresh D.A. Integrins alpha v beta 3 and alpha v beta 5 contribute to cell attachment to vitronectin but differentially distribute on the cell surface. J. Cell Biol. 113:1991;919-929.
63. Huang X., Wu J., Spong S., Sheppard D. The integrin ?v?5 is critical for keratinocyte migration of both its known ligand, fibronectin, and on vitronectin. J. Cell Sci. 111:1998;2189-2195.
64. Tonn J.C., Wunderlich S., Kerkau S., Klein C.E., Roosen K. Invasive behaviour of human gliomas is mediated by interindividually different integrin patterns. Anticancer Res. 18:1998;2599-2605.
65. Bokel C., Brown N.H. Integrins in development: moving on, responding to, and sticking to the extracellular matrix. Dev. Cell. 3:2002;311-321.
66. van der F.A., Sonnenberg A. Function and interactions of integrins. Cell Tissue Res. 305:2001;285-298.
67. Giancotti F.G., Ruoslahti E. Integrin signaling. Science. 285:1999;1028-1032.
68. Lessey B.A., Ilesanmi A.O., Lessey M.A., Riben M., Harris J.E., Chwalisz K. Luminal and glandular endometrial epithelium express integrins differentially throughout the menstrual cycle: implications for implantation, contraception, and infertility. Am. J. Reprod. Immunol. 35:1996;195-204.
69. Fournier T.M., Lamorte L., Maroun C.R., Lupher M., Band H., Langdon W., Park M. Cbl-transforming variants trigger a cascade of molecular alterations that lead to epithelial mesenchymal conversion. Mol. Biol. Cell. 11:2000;3397-3410.
70. Boyer B., Vallés A.M., Edme N. Induction and regulation of epithelial-mesenchymal transitions. Biochem. Pharmacol. 60:2000;1091-1099.
71. Cho S.Y., Klemke R.L. Extracellular-regulated kinase activation and CAS/Crk coupling regulate cell migration and suppress apoptosis during invasion of the extracellular matrix. J. Cell Biol. 149:2000;223-236.
72. Lamorte L., Royal I., Naujokas M., Park M. Crk adapter proteins promote an epithelial-mesenchymal-like transition and are required for HGF-mediated cell spreading and breakdown of epithelial adherens junctions. Mol. Biol. Cell. 13:2002;1449-1461.
73. Kitamura S., Kondo S., Shinomura Y., Kanayama S., Miyazaki Y., Kiyohara T., Hiraoka S., Matsuzawa Y. Met/HGF receptor modulates bcl-w expression and inhibits apoptosis in human colorectal cancers. Br. J. Cancer. 83:2000;668-673.
74. Tamagnone L., Comoglio P.M. Control of invasive growth by hepatocyte growth factor and related scatter factors. Cytokine Growth Factor Rev. 8:1997;129-142.