The insulin-like growth factor receptor I promotes motility and invasion of bladder cancer cells through Akt- and mitogen-activated protein kinase-dependent activation of paxillin

American Journal of Pathology

Volumn 176, Issue 6, 2010, Pages 2997-3006

  Metalli, David ^a,c   Lovat, Francesca ^a   Tripodi, Farida ^a,c   Genua, Marco ^a   Xu, Shi Qiong ^a   Spinelli, Michela ^a   Alberghina, Lilia ^c   Vanoni, Marco ^c   Baffa, Raffaele ^a,d   Gomella, Leonard G ^a   Iozzo, Renato V ^b   Morrione, Andrea ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

^d MEDIMMUNE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PAXILLIN; PROTEIN KINASE B; SOMATOMEDIN C RECEPTOR; FOCAL ADHESION KINASE; MITOGEN ACTIVATED PROTEIN KINASE; SMALL INTERFERING RNA;

ARTICLE; BLADDER CARCINOGENESIS; BLADDER CARCINOMA; CANCER CELL CULTURE; CANCER INVASION; CANCER TISSUE; CARCINOMA CELL; CELL MOTILITY; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR PROMOTION; WOUND HEALING; ANTAGONISTS AND INHIBITORS; BLADDER TUMOR; CELL MOTION; CELL TRANSFORMATION; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; TUMOR INVASION;

CELL LINE, TUMOR; CELL MOVEMENT; CELL TRANSFORMATION, NEOPLASTIC; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM INVASIVENESS; PAXILLIN; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, IGF TYPE 1; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; URINARY BLADDER NEOPLASMS;

EID: 77953190164     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090904     Document Type: Article

References (41)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ: Cancer statistics, 2009. CA Cancer J Clin 2009, 59:225-249
2. Knowles MA: Molecular pathogenesis of bladder cancer. Int J Clin Oncol 2008, 13:287-297
3. Mitra AP, Cote RJ: Molecular pathogenesis and diagnostics of bladder cancer. Annu Rev Pathol 2009, 4:251-285
4. Scher CD, Stone ME, Stiles CD: Platelet-derived growth factor prevents G0 growth arrest. Nature 1979, 281:390-392
5. Baserga R: The insulin-like growth factor I receptor: a key to tumor growth? Cancer Res 1995, 55:249-252
6. Baker J, Liu JP, Robertson EJ, Efstratiadis A: Role of insulin-like growth factors in embryonic and postnatal growth. Cell 1993, 75:73-82
7. Eggenschwiler J, Ludwig T, Fisher P, Leighton PA, Tilghman SM, Efstratiadis A: Mouse mutant embryos overexpressing IGF-II exhibit phenotypic features of the Beckwith-Wiedemann and Simpson-Golabi-Behmel syndromes. Genes Dev 1997, 11:3128-3142 (Pubitemid 27528054)
8. Surmacz E: Growth factor receptors as therapeutic targets: strategies to inhibit the insulin-like growth factor I receptor. Oncogene 2003, 22:6589-6597 (Pubitemid 37372339)
9. Baserga R, Morrione A: Differentiation and malignant transformation: two roads diverged in a wood. J Cell Biochem 1999, Suppl 32-33: 68-75 (Pubitemid 30041812)
10. Pollak MN, Schernhammer ES, Hankinson SE: Insulin-like growth factors and neoplasia. Nat Rev Cancer 2004, 4:505-518
11. Le Roith D, Karas M, Yakar S, Qu BH, Wu Y, Blakesley VA: The role of the insulin-like growth factors in cancer. Isr Med Assoc J 1999, 1:25-30
12. Cheng MC, Lin CH, Lin HJ, Yu YP, Wu SH: Hydrolysis, lactonization, and identification of alpha(2->8)/alpha(2->9) alternatively linked tri-, tetra-, and polysialic acids. Glycobiology 2004, 14:147-155
13. Baserga R: The contradictions of the insulin-like growth factor 1 receptor. Oncogene 2000, 19:5574-5581
14. Baserga R, Hongo A, Rubini M, Prisco M, Valentinis B: The IGF-I receptor in cell growth, transformation and apoptosis. Biochim Biophys Acta 1997, 1332:F105-F126
15. Le Roith D: Regulation of proliferation and apoptosis by the insulinlike growth factor I receptor. Growth Horm IGF Res 2000, 10(Suppl A):S12-S13
16. Chitnis MM, Yuen JS, Protheroe AS, Pollak M, Macaulay VM: The type 1 insulin-like growth factor receptor pathway. Clin Cancer Res 2008, 14:6364-6370
17. Rowinsky EK, Youssoufian H, Tonra JR, Solomon P, Burtrum D, Ludwig DL: IMC-A12, a human IgG1 monoclonal antibody to the insulin-like growth factor I receptor. Clin Cancer Res 2007, 13:5549S-5555S
18. Rochester MA, Patel N, Turney BW, Davies DR, Roberts IS, Crew J, Protheroe A, Macaulay VM: The type 1 insulin-like growth factor receptor is over-expressed in bladder cancer. BJU Int 2007, 100:1396-1401
19. Lovat F, Bitto A, Xu SQ, Fassan M, Goldoni S, Metalli D, Wubah V, McCue P, Serrero G, Gomella LG, Baffa R, Iozzo RV, Morrione A: Proepithelin is an autocrine growth factor for bladder cancer. Carcinogenesis 2009, 30:861-868
20. Monami G, Gonzalez EM, Hellman M, Gomella LG, Baffa R, Iozzo RV, Morrione A: Proepithelin promotes migration and invasion of 5637 bladder cancer cells through the activation of ERK1/2 and the formation of a paxillin/FAK/ERK complex. Cancer Res 2006, 66:7103-7110
21. Monami G, Emiliozzi V, Bitto A, Lovat F, Xu SQ, Goldoni S, Fassan M, Serrero G, Gomella LG, Baffa R, Iozzo RV, Morrione A: Proepithelin regulates prostate cancer cell biology by promoting cell growth, migration, and anchorage-independent growth. Am J Pathol 2009, 174:1037-1047
22. Belletti B, Nicoloso MS, Schiappacassi M, Berton S, Lovat F, Wolf K, Canzonieri V, D'Andrea S, Zucchetto A, Friedl P, Colombatti A, Baldassarre G: Stathmin activity influences sarcoma cell shape, motility, and metastatic potential. Mol Biol Cell 2008, 19:2003-2013
23. Guo W, Giancotti FG: Integrin signalling during tumour progression. Nat Rev Mol Cell Biol 2004, 5:816-826
24. Morrione A, Romano G, Navarro M, Reiss K, Valentinis B, Dews M, Eves E, Rosner MR, Baserga R: Insulin-like growth factor I receptor signaling in differentiation of neuronal H19-7 cells. Cancer Res 2000, 60:2263-2272 (Pubitemid 30225193)
25. Peruzzi F, Prisco M, Dews M, Salomoni P, Grassilli E, Romano G, Calabretta B, Baserga R: Multiple signaling pathways of the insulin-like growth factor 1 receptor in protection from apoptosis. Mol Cell Biol 1999, 19:7203-7215 (Pubitemid 29441900)
26. Peruzzi F, Prisco M, Morrione A, Valentinis B, Baserga R: Anti-apoptotic signaling of the insulin-like growth factor-I receptor through mitochondrial translocation of c-Raf and Nedd4. J Biol Chem 2001, 276:25990-25996 (Pubitemid 33730659)
27. Monami G, Emiliozzi V, Morrione A: Grb10/Nedd4-mediated multiubiquitination of the insulin-like growth factor receptor regulates receptor internalization. J Cell Physiol 2008, 216:426-437
28. Ishibe S, Joly D, Liu ZX, Cantley LG: Paxillin serves as an ERK-regulated scaffold for coordinating FAK and Rac activation in epithelial morphogenesis. Mol Cell 2004, 16:257-267
29. Ishibe S, Joly D, Zhu X, Cantley LG: Phosphorylation-dependent paxillin-ERK association mediates hepatocyte growth factor-stimulated epithelial morphogenesis. Mol Cell 2003, 12:1275-1285
30. Petit V, Boyer B, Lentz D, Turner CE, Thiery JP, Valles AM: Phosphorylation of tyrosine residues 31 and 118 on paxillin regulates cell migration through an association with CRK in NBT-II cells. J Cell Biol 2000, 148:957-970
31. Cai X, Li M, Vrana J, Schaller MD: Glycogen synthase kinase 3- and extracellular signal-regulated kinase-dependent phosphorylation of paxillin regulates cytoskeletal rearrangement. Mol Cell Biol 2006, 26:2857-2868
32. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, Parsons JT, Horwitz AF: FAK-Src signalling through paxillin, ERK, and MLCK regulates adhesion disassembly. Nat Cell Biol 2004, 6:154-161
33. Guvakova MA, Surmacz E: Overexpressed IGF-I receptors reduce estrogen growth requirements, enhance survival, and promote E-cadherin-mediated cell-cell adhesion in human breast cancer cells. Exp Cell Res 1997, 231:149-162
34. Mauro L, Sisci D, Bartucci M, Salerno M, Kim J, Tam T, Guvakova MA, Ando S, Surmacz E: SHC-alpha5beta1 integrin interactions regulate breast cancer cell adhesion and motility. Exp Cell Res 1999, 252:439-448
35. Doerr ME, Jones JI: The roles of integrins and extracellular matrix proteins in the insulin-like growth factor I-stimulated chemotaxis of human breast cancer cells. J Biol Chem 1996, 271:2443-2447 (Pubitemid 126549906)
36. Bartucci M, Morelli C, Mauro L, Ando S, Surmacz E: Differential insulin-like growth factor I receptor signaling and function in estrogen receptor (ER)-positive MCF-7 and ER-negative MDA-MB-231 breast cancer cells. Cancer Res 2001, 61:6747-6754 (Pubitemid 32896497)
37. Kim HJ, Litzenburger BC, Cui X, Delgado DA, Grabiner BC, Lin X, Lewis MT, Gottardis MM, Wong TW, Attar RM, Carboni JM, Lee AV: Constitutively active type I insulin-like growth factor receptor causes transformation and xenograft growth of immortalized mammary epithelial cells and is accompanied by an epithelial-to-mesenchymal transition mediated by NF-kappaB and snail. Mol Cell Biol 2007, 27:3165-3175
38. Manning DL, Daly RJ, Lord PG, Kelly KF, Green CD: Effects of oestrogen on the expression of a 4.4 kb mRNA in the ZR-75-1 human breast cancer cell line. Mol Cell Endocrinol 1988, 59:205-212
39. Zhao J, Guan JL: Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev 2009, 28:35-49
40. Pylayeva Y, Gillen KM, Gerald W, Beggs HE, Reichardt LF, Giancotti FG: Ras- and PI3K-dependent breast tumorigenesis in mice and humans requires focal adhesion kinase signaling. J Clin Invest 2009, 119:252-266
41. Bao W, Stromblad S: Integrin alphav-mediated inactivation of p53 controls a MEK1-dependent melanoma cell survival pathway in three-dimensional collagen. J Cell Biol 2004, 167:745-756