Autocrine signaling in carcinoma: VEGF and the α6β4 integrin

Seminars in Cancer Biology

Volumn 14, Issue 2, 2004, Pages 115-122

  Mercurio, Arthur M ^a   Bachelder, Robin E ^a   Bates, Richard C ^a   Chung, Jun ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Integrin; Migration; Signaling; Survival; VEGF

Indexed keywords

ALPHA6BETA4 INTEGRIN; VASCULOTROPIN;

ANGIOGENESIS; AUTOCRINE EFFECT; CANCER CELL; CANCER GROWTH; CANCER INVASION; CANCER SURVIVAL; CARCINOMA; CELL MIGRATION; HUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION;

EID: 1242272855     PISSN: 1044579X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcancer.2003.09.016     Document Type: Review

References (72)

1. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell. 100:2000;57-70.
2. Sporn M.B., Todaro G.J. Autocrine secretion and malignant transformation of cells. N. Engl. J. Med. 303:1980;878-880.
3. Hagios C., Lochter A., Bissell M.J. Tissue architecture: the ultimate regulator of epithelial function? Philos. Trans. R Soc. Lond. B Biol. Sci. 353:1998;857-870.
4. Bates R.C., Buret A., van Helden D.F., Horton M.A., Burns G.F. Apoptosis induced by inhibition of intercellular contact. J. Cell Biol. 125:1994;403-415.
5. Birchmeier W, Hulsken J, Behrens J. E-cadherin as an invasion suppressor. Ciba Found Symp 1995;189:124-36 (discussion 136-41, 174-26).
6. Daneker G.W. Jr., Piazza A.J., Steele G.D. Jr., Mercurio A.M. Relationship between extracellular matrix interactions and degree of differentiation in human colon carcinoma cell lines. Cancer Res. 49:1989;681-686.
7. Fearon E.R. Cancer progression. Curr. Biol. 9:1999;R873-R875.
8. Brown J.M. The hypoxic cell: a target for selective cancer therapy - eighteenth Bruce F. Cain Memorial Award lecture. Cancer Res. 59:1999;5863-5870.
9. Brizel D.M., Scully S.P., Harrelson J.M., Layfield L.J., Bean J.M., Prosnitz L.R.et al. Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Res. 56:1996;941-943.
10. Hockel M., Schlenger K., Aral B., Mitze M., Schaffer U., Vaupel P. Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res. 56:1996;4509-4515.
11. Bergers G., Benjamin L.E. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer. 3:2003;401-410.
12. Graeber T.G., Osmanian C., Jacks T., Housman D.E., Koch C.J., Lowe S.W. et al. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours [see comments]. Nature. 379:1996;88-91.
13. Dvorak H.F., Nagy J.A., Feng D., Brown L.F., Dvorak A.M. Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr. Top. Microbiol. Immunol. 237:1999;97-132.
14. Senger D.R., Van De Water L. VEGF expression by epithelial and stromal cell compartments: resolving a controversy. Am. J. Pathol. 157:2000;1-3.
15. Ferrara N., Gerber H.P., LeCouter J. The biology of VEGF and its receptors. Nat. Med. 9:2003;669-676.
16. Soker S., Takashima S., Miao H.Q., Neufeld G., Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform- specific receptor for vascular endothelial growth factor. Cell. 92:1998;735-745.
17. Kawasaki T., Kitsukawa T., Bekku Y., Matsuda Y., Sanbo M., Yagi T.et al. A requirement for neuropilin-1 in embryonic vessel formation. Development. 126:1999;4895-4902.
18. Bachelder R.E., Crago A., Chung J., Wendt M.A., Shaw L.M., Robinson G.et al. Vascular endothelial growth factor is an autocrine survival factor for neuropilin-expressing breast carcinoma cells. Cancer Res. 61:2001;5736-5740.
19. Bachelder R.E., Wendt M.A., Mercurio A.M. Vascular endothelial growth factor promotes breast carcinoma invasion in an autocrine manner by regulating the chemokine receptor CXCR4. Cancer Res. 62:2002;7203-7206.
20. Masood R., Cai J., Zheng T., Smith D.L., Hinton D.R., Gill P.S. Vascular endothelial growth factor (VEGF) is an autocrine growth factor for VEGF receptor-positive human tumors. Blood. 98:2001;1904-1913.
21. Soker S., Kaefer M., Johnson M., Klagsbrun M., Atala A., Freeman M.R. Vascular endothelial growth factor-mediated autocrine stimulation of prostate tumor cells coincides with progression to a malignant phenotype. Am. J. Pathol. 159:2001;651-659.
22. Dias S., Hattori K., Heissig B., Zhu Z., Wu Y., Witte L.et al. Inhibition of both paracrine and autocrine VEGF/VEGFR-2 signaling pathways is essential to induce long-term remission of xenotransplanted human leukemias. Proc. Natl. Acad. Sci. U.S.A. 98:2001;10857-10862.
23. Masood R., Kundra A., Zhu S., Xia G., Scalia P., Smith D.L.et al. Malignant mesothelioma growth inhibition by agents that target the VEGF and VEGF-C autocrine loops. Int. J. Cancer. 104:2003;603-610.
24. Lacal P.M., Failla C.M., Pagani E., Odorisio T., Schietroma C., Falcinelli S.et al. Human melanoma cells secrete and respond to placenta growth factor and vascular endothelial growth factor. J. Invest. Dermatol. 115:2000;1000-1007.
25. Takahashi T., Fournier A., Nakamura F., Wang L.H., Murakami Y., Kalb R.G.et al. Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell. 99:1999;59-69.
26. Tamagnone L., Artigiani S., Chen H., He Z., Ming G.I., Song H.et al. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell. 99:1999;71-80.
27. Oft M., Peli J., Rudaz C., Schwarz H., Beug H., Reichmann E. TGF-beta1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes Dev. 10:1996;2462-2477.
28. Oft M., Heider K.H., Beug H. TGFbeta signaling is necessary for carcinoma cell invasiveness and metastasis. Curr. Biol. 8:1998;1243-1252.
29. Bhowmick N.A., Ghiassi M., Bakin A., Aakre M., Lundquist C.A., Engel M.E.et al. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol. Biol. Cell. 12:2001;27-36.
30. Hay E.D. An overview of epithelio-mesenchymal transformation. Acta. Anat. (Basel). 154:1995;8-20.
31. Thiery J.P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer. 2:2002;442-454.
32. Bates R.C., Mercurio A.M. Tumor necrosis factor-alpha stimulates the epithelial-to-mesenchymal transition of human colonic organoids. Mol. Biol. Cell. 14:2003;1790-1800.
33. Bates R.C., Goldsmith J.D., Bachelder R.E., Brown C., Shibuya M., Oettgen P.et al. Flt-1 (VEGFR-1)-dependent survival characterizes the epithelial-mesenchymal transition of colonic organoids. Curr Biol. 13:2003;1721-1727.
34. Andre T., Kotelevets L., Vaillant J.C., Coudray A.M., Weber L., Prevot S.et al. Vegf, Vegf-B, Vegf-C and their receptors KDR, FLT-1 and FLT-4 during the neoplastic progression of human colonic mucosa. Int. J. Cancer. 86:2000;174-181.
35. Warren R.S., Yuan H., Matli M.R., Gillett N.A., Ferrara N. Regulation by vascular endothelial growth factor of human colon cancer tumorigenesis in a mouse model of experimental liver metastasis. J. Clin. Invest. 95:1995;1789-1797.
36. Muller A., Homey B., Soto H., Ge N., Catron D., Buchanan M.E.et al. Involvement of chemokine receptors in breast cancer metastasis. Nature. 410:2001;50-56.
37. Luo Y., Raible D., Raper J.A. Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell. 75:1993;217-227.
38. He Z., Tessier-Lavigne M. Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell. 90:1997;739-751.
39. Kolodkin A.L., Levengood D.V., Rowe E.G., Tai Y.T., Giger R.J., Ginty D.D. Neuropilin is a semaphorin III receptor. Cell. 90:1997;753-762.
40. Eickholt B.J., Walsh F.S., Doherty P. An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling. J. Cell Biol. 157:2002;211-217.
41. Bachelder R.E., Lipscomb E.A., Lin X., Wendt M.A., Chadborn N.H., Eickholt B.J.et al. Competing autocrine pathways involving alternative neuropilin-1 ligands regulate chemotaxis of carcinoma cells. Cancer Res. 63:2003;5230-5233.
42. Mercurio A.M., Rabinovitz I. Towards a mechanistic understanding of tumor invasion-lessons from thealpha 6 beta 4integrin. Semin. Cancer Biol. 11:2001;129-141.
43. Mercurio A.M., Rabinovitz I., Shaw L.M. The alpha 6 beta 4 integrin and epithelial cell migration. Curr. Opin. Cell Biol. 13:2001;541-545.
44. Chao C., Lotz M.M., Clarke A.C., Mercurio A.M. A function for the integrin alpha6beta4 in the invasive properties of colorectal carcinoma cells. Cancer Res. 56:1996;4811-4819.
45. O'Connor K.L., Shaw L.M., Mercurio A.M. Release of cAMP gating by the alpha6beta4 integrin stimulates lamellae formation and the chemotactic migration of invasive carcinoma cells. J. Cell Biol. 143:1998;1749-1760.
46. Trusolino L., Bertotti A., Comoglio P.M. A signaling adapter function for alpha6beta4 integrin in the control of HGF-dependent invasive growth. Cell. 107:2001;643-654.
47. Borradori L., Sonnenberg A. Structure and function of hemidesmosomes: more than simple adhesion complexes. J. Invest. Dermatol. 112:1999;411-418.
48. Bachelder R.E., Ribick M.J., Marchetti A., Falcioni R., Soddu S., Davis K.R.et al. p53 inhibits alpha 6 beta 4 integrin survival signaling by promoting the caspase 3-dependent cleavage of AKT/PKB. J. Cell Biol. 147:1999;1063-1072.
49. Chung J., Bachelder R.E., Lipscomb E.A., Shaw L.M., Mercurio A.M. Integrin (alpha 6 beta 4) regulation of eIF-4E activity and VEGF translation: a survival mechanism for carcinoma cells. J. Cell Biol. 158:2002;165-174.
50. Mercurio A.M., Rabinovitz I. Towards a mechanistic understanding of tumor invasion-lessons from the alpha6beta 4 integrin. Semin. Cancer Biol. 11:2001;129-141.
51. von Marschall Z., Cramer T., Hocker M., Burde R., Plath T., Schirner M. et al. De novo expression of vascular endothelial growth factor in human pancreatic cancer: evidence for an autocrine mitogenic loop. Gastroenterology. 119:2000;1358-1372.
52. Gingras A.C., Raught B., Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev. 15:2001;807-826.
53. Dennis P.B., Fumagalli S., Thomas G. Target of rapamycin (TOR): balancing the opposing forces of protein synthesis and degradation. Curr. Opin. Genet. Dev. 9:1999;49-54.
54. Schmelzle T., Hall M.N. TOR, a central controller of cell growth. Cell. 103:2000;253-262.
55. De Benedetti A., Harris A.L. eIF4E expression in tumors: its possible role in progression of malignancies. Int. J. Biochem. Cell Biol. 31:1999;59-72.
56. McKendrick L., Pain V.M., Morley S.J. Translation initiation factor 4E. Int. J. Biochem. Cell Biol. 31:1999;31-35.
57. Berkel H.J., Turbat-Herrera E.A., Shi R., de Benedetti A. Expression of the translation initiation factor eIF4E in the polyp-cancer sequence in the colon. Cancer Epidemiol. Biomarkers Prev. 10:2001;663-666.
58. DeFatta R.J., Nathan C.A., De Benedetti A. Antisense RNA to eIF4E suppresses oncogenic properties of a head and neck squamous cell carcinoma cell line. Laryngoscope. 110:2000;928-933.
59. Huang S., Houghton P.J. Inhibitors of mammalian target of rapamycin as novel antitumor agents: from bench to clinic. Curr. Opin. Invest. Drugs. 3:2002;295-304.
60. Dennis P.B., Jaeschke A., Saitoh M., Fowler B., Kozma S.C., Thomas G. Mammalian TOR: a homeostatic ATP sensor. Science. 294:2001;1102-1105.
61. Shaw L.M., Rabinovitz I., Wang H.H., Toker A., Mercurio A.M. Activation of phosphoinositide 3-OH kinase by the alpha6beta4 integrin promotes carcinoma invasion. Cell. 91:1997;949-960.
62. Gambaletta D., Marchetti A., Benedetti L., Mercurio A.M., Sacchi A., Falcioni R. Cooperative signaling between alpha(6)beta(4) integrin and ErbB-2 receptor is required to promote phosphatidylinositol 3-kinase-dependent invasion. J. Biol. Chem. 275:2000;10604-10610.
63. Nguyen B.P., Gil S.G., Carter W.G. Deposition of laminin 5 by keratinocytes regulates integrin adhesion and signaling. J. Biol. Chem. 275:2000;31896-31907.
64. Hintermann E., Bilban M., Sharabi A., Quaranta V. Inhibitory Role of alpha6beta4-associated erbB-2 and Phosphoinositide 3- Kinase in Keratinocyte Haptotactic Migration Dependent on alpha3beta1 Integrin. J. Cell Biol. 153:2001;465-478.
65. Shaw L.M. Identification of IRS-1 and IRS-2 as signaling intermediates in the a6b4 integrin-dependent activation of phosphoinositide 3-OH kinase and promotion of invasion. Mol. Cell. Biol. 21:2001;5082-5093.
66. Kabbinavar F., Hurwitz H.I., Fehrenbacher L., Meropol N.J., Novotny W.F., Lieberman G.et al. Phase II, randomized trial comparing bevacizumab plus fluorouracil (FU)/leucovorin (LV) with FU/LV alone in patients with metastatic colorectal cancer. J. Clin. Oncol. 21:2003;60-65.
67. Colognato H., Baron W., Avellana-Adalid V., Relvas J.B., Baron-Van Evercooren A., Georges-Labouesse E.et al. CNS integrins switch growth factor signalling to promote target-dependent survival. Nat. Cell Biol. 4:2002;833-841.
68. Datta S.R., Brunet A., Greenberg M.E. Cellular survival: a play in three Akts. Genes Dev. 13:1999;2905-2927.
69. Semenza G.L. Involvement of hypoxia-inducible factor 1 in human cancer. Int. Med. 41:2002;79-83.
70. Oikawa M., Abe M., Kurosawa H., Hida W., Shirato K., Sato Y. Hypoxia induces transcription factor ETS-1 via the activity of hypoxia-inducible factor-1. Biochem. Biophys. Res. Commun. 289:2001;39-43.
71. Miao H.Q., Soker S., Feiner L., Alonso J.L., Raper J.A., Klagsbrun M. Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: functional competition of collapsin-1 and vascular endothelial growth factor-165. J. Cell Biol. 146:1999;233-242.
72. Serini G., Valdembri D., Zanivan S., Morterra G., Burkhardt C., Caccavari F.et al. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature. 424:2003;391-397.