IGF-II regulates metastatic properties of choriocarcinoma cells through the activation of the insulin receptor

Molecular Human Reproduction

Volumn 13, Issue 8, 2007, Pages 567-576

  Diaz, L E ^a   Chuan, Y C ^b   Lewitt, M ^b   Fernandez Perez, L ^c   Carrasco Rodriguez S ^a   Sanchez Gomez, M ^a   Flores Morales, A ^b  

^a UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

Author keywords

Choriocarcinoma; Hydatidiform; IGF II; Insulin receptor; Metastasis; Mole

Indexed keywords

COLLAGEN TYPE 4; INSULIN RECEPTOR; SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR; SOMATOMEDIN C;

ADULT; ARTICLE; CANCER INVASION; CANCER TISSUE; CARCINOMA CELL; CELL ADHESION; CELL INVASION; CHEMOTAXIS; CHORIOCARCINOMA; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GESTATIONAL AGE; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDATIDIFORM MOLE; IMMUNORADIOMETRIC ASSAY; METASTASIS; PLACENTA DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SPONTANEOUS ABORTION; TROPHOBLAST; TROPHOBLASTIC DISEASE;

ADULT; ANTIGENS, CD; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CHORIOCARCINOMA; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; INSULIN-LIKE GROWTH FACTOR II; NAPHTHALENES; PHOSPHONIC ACIDS; PREGNANCY; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, IGF TYPE 1; RECEPTOR, INSULIN; UTERINE NEOPLASMS;

EID: 34547838385     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gam039     Document Type: Article

References (39)

1. Altieri A, Franceschi S, Ferlay J, Smith J, La Vecchia C. Epidemiology and aetiology of gestational trophoblastic diseases. Lancet Oncol 2003;4:670-678.
2. Baker J, Liu JP, Robertson EJ, Efstratiadis A. Role of insulin-like growth factors in embryonic and postnatal growth. Cell 1993;75 73-82.
3. Benecke H, Flier JS, Moller DE. Alternatively spliced variants of the insulin receptor protein. Expression in normal and diabetic human tissues. J Clin Invest 1992;89:2066-2070.
4. Chuan YC, Pang ST, Cedazo-Minguez A, Norstedt G, Pousette A, Flores-Morales A. Androgen induction of prostate cancer cell invasion is mediated by ezrin. J Biol Chem 2006;281:29938-29948.
5. Conforti G, Zanetti A, Colella S, Abbadini M, Marchisio PC, Pytela R, Giancotti F, Tarone G, Languino LR, Dejana E. Interaction of fibronectin with cultured human endothelial cells: Characterization of the specific receptor. Blood 1989;73:1576-1585.
6. Constancia M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, Stewart F, Kelsey G, Fowden A, Sibley C et al. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 2002;417:945-948.
7. Crossey PA, Pillai CC, Miell JP. Altered placental development and intrauterine growth restriction in IGF binding protein-1 transgenic mice. J Clin Invest 2002;110:411-418.
8. Denley A, Bonython ER, Booker GW, Cosgrove LJ, Forbes BE, Ward CW, Wallace JC. Structural determinants for high-affinity binding of insulin-like growth factor II to insulin receptor (IR)-A, the exon 11 minus isoform of the IR. Mol Endocrinol 2004;18:2502-2512.
9. Denley A, Cosgrove U, Booker GW, Wallace JC, Forbes BE. Molecular interactions of the IGF system. Cytokine Growth Factor Rev 2005; 16:421-439.
10. Denley A, Brierley GV, Carroll JM, Lindenberg A, Booker GW, Cosgrove LJ, Wallace JC, Forbes BE, Roberts CT, Jr. Differential activation of insulin receptor isoforms by insulin-like growth factors is determined by the C domain. Endocrinology 2006;147:1029-1036.
11. Frasca F, Pandini G, Scalia P, Sciacca L, Mineo R, Costantino A, Goldfine ID, Belfiore A, Vigneri R. Insulin receptor isoform A, a newly recognized, high-affinity insulin-like growth factor II receptor in fetal and cancer cells. Mol Cell Biol 1999;19:3278-3288.
12. Gleeson LM, Chakraborty C, McKinnon T, Lala PK. Insulin-like growth factor-binding protein 1 stimulates human trophoblast migration by signaling through alpha 5 beta 1 integrin via mitogen-activated protein Kinase pathway. J Clin Endocrinol Metab 2001;86:2484-2493.
13. Han VK, Carter AM. Spatial and temporal patterns of expression of messenger RNA for insulin-like growth factors and their binding proteins in the placenta of man and laboratory animals. Placenta 2000;21 289-305.
14. He L, Cui H, Walsh C, Mattsson R, Lin W, Anneren G, Pfeifer-Ohlsson S, Ohlsson R. Hypervariable allelic expression patterns of the imprinted IGF2 gene in tumor cells. Oncogene 1998;16:113-119.
15. Jones JI, Gockerman A, Busby WH, Jr, Wright G, Clemmons DR. Insulin-like growth factor binding protein 1 stimulates cell migration and binds to the alpha 5 beta 1 integrin by means of its Arg-Gly-Asp sequence. Proc Natl Acad Sci U S A 1993;90:10553-10557.
16. Kim SJ, Park SE, Lee C, Lee SY, Kim IH, An HJ, Oh YK. Altered imprinting, promoter usage, and expression of insulin-like growth factor-II gene in gestational trophoblastic diseases. Gynecol Oncol 2003;88:411-418.
17. Korner C, Nurnberg B, Uhde M, Braulke T. Mannose 6-phosphate/ insulin-like growth factor II receptor fails to interact with G-proteins analysis of mutant cytoplasmic receptor domains. J Biol Chem 1995;270:287-295.
18. Kricker JA, Towne CL, Firth SM, Herington AC, Upton Z. Structural and functional evidence for the interaction of insulin-like growth factors (IGFs) and IGF binding proteins with vitronectin. Endocrinology 2003;144:2807-2815.
19. Li J, Sahagian GG. Demonstration of tumor suppression by mannose 6-phosphate/insulin-like growth factor 2 receptor. Oncogene 2004;23: 9359-9368
20. Louvi A, Accili D, Efstratiadis A. Growth-promoting interaction of IGF-II with the insulin receptor during mouse embryonic development. Dev Biol 1997;189:33-48.
21. Ludwig T, Eggenschwiler J, Fisher P, D'Ercole AJ, Davenport ML, Efstratiadis A. Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev Biol 1996;177:517-535.
22. Lustig-Yariv O, Schulze E, Komitowski D, Erdmann V, Schneider T, de Groot N, Hochberg A. The expression of the imprinted genes H19 and IGF-2 in choriocarcinoma cell lines. Is H19 a tumor suppressor gene? Oncogene 1997;15:169-177.
23. McKinnon T, Chakraborty C, Gleeson LM, Chidiac P, Lala PK. Stimulation of human extravillous trophoblast migration by IGF-II is mediated by IGF type 2 receptor involving inhibitory G protein(s) and phosphorylation of MAPK. J Clin Endocrinol Metab 2001;86:3665-3674.
24. Moller DE, Yokota A, Caro JF, Flier JS. Tissue-specific expression of two alternatively spliced insulin receptor mRNAs in man. Mol Endocrinol 1989;3:1263-1269.
25. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63.
26. O'Gorman DB, Costello M, Weiss J, Firth SM, Scott CD. Decreased insulin-like growth factor-II/mannose 6-phosphate receptor expression enhances tumorigenicity in JEG-3 cells. Cancer Res 1999;59 5692-5694.
27. O'Gorman DB, Weiss J, Hettiaratchi A, Firth SM, Scott CD. Insulin-like growth factor-II/mannose 6-phosphate receptor overexpression reduces growth of choriocarcinoma cells in vitro and in vivo. Endocrinology 2002;143:4287-4294.
28. Pandini G, Frasca F, Mineo R, Sciacca L, Vigneri R, Belfiore A. Insulin/ insulin-like growth factor I hybrid receptors have different biological characteristics depending on the insulin receptor isoform involved. J Biol Chem 2002;277:39684-39695.
29. Pandini G, Medico E, Conte E, Sciacca L, Vigneri R, Belfiore A. Differential gene expression induced by insulin and insulin-like growth factor-II through the insulin receptor isoform A. J Biol Chem 2003;278: 42178-42189.
30. Pandini G, Conte E, Medico E, Sciacca L, Vigneri R, Belfiore A. IGF-II binding to insulin receptor isoform A induces a partially different gene expression profile from insulin binding. Ann N Y Acad Sci 2004; 1028: 450-456.
31. Ritvos O, Rutanen EM, Pekonen F, Jalkanen J, Suikkari AM, Ranta T. Characterization of functional type I insulin-like growth factor receptors from human choriocarcinoma cells. Endocrinology 1988; 122:395-401.
32. Saperstein R, Vicario PP, Strout HV, Brady E, Slater EE, Greenlee WJ, Ondeyka DL, Patchett AA, Hangauer DG. Design of a selective insulin receptor tyrosine kinase inhibitor and its effect on glucose uptake and metabolism in intact cells. Biochemistry 1989;28:5694-5701.
33. Sciacca L, Mineo R, Pandini G, Murabito A, Vigneri R, Belfiore A. In IGF-I receptor-deficient leiomyosarcoma cells autocrine IGF-II induces cell invasion and protection from apoptosis via the insulin receptor isoform A. Oncogene 2002;21:8240-8250.
34. Sciacca L, Prisco M, Wu A, Belfiore A, Vigneri R, Baserga R. Signaling differences from the A and B isoforms of the insulin receptor (IR) in 32D cells in the presence or absence of IR substrate-1. Endocrinology 2003;144:2650-2658.
35. Seckl MJ, Fisher RA, Salemo G, Rees H, Paradinas FJ, Foskett M, Newlands ES. Choriocarcinoma and partial hydatidiform moles. Lancet 2000; 356:36-39.
36. Soper JT. Gestational trophoblastic disease. Obstet Gynecol 2006;108: 176-187.
37. Uhles S, Moede T, Leibiger B, Berggren PO, Leibiger IB. Isoform-specific insulin receptor signaling involves different plasma membrane domains. J Cell Biol 2003;163:1327-1337.
38. Zhang L, Shiverick KT. Benzo(a)pyrene, but not 2,3,7,8-tetrachlorodibenzo-p-dioxin, alters cell proliferation and c-myc and growth factor expression in human placental choriocarcinoma JEG-3 cells. Biochem Biophys Res Commun 1997;231:117-120.
39. Zhang M AS, Yeh S. RRR-alpha-tocopheryl succinate inhibits human prostate cancer cell invasiveness. Oncogene 2004;23 3080-3088.