Synchronization in G0/G1 enhances the mitogenic response of cells overexpressing the human insulin receptor A isoform to insulin

Cell Biology and Toxicology

Volumn 26, Issue 4, 2010, Pages 293-307

  Bonnesen, Christine ^a   Nelander, Gitte Mai ^a   Hansen, Bo Falck ^a   Jensen, Pia ^a   Krabbe, Jonas S ^a,b   Jensen, Marianne B ^a   Hegelund, Anne Charlotte ^a   Svendsen, Jette E ^a   Oleksiewicz, Martin B ^a,c  

^a NOVO NORDISK A S   (Denmark)

^b Nuevolution A/S   (Denmark)

^c INTERCELL AG   (Austria)

Author keywords

Flow cytometry; Insulin analog; Insulin receptor; Mitogenic effect; Molecular toxicology 3H thymidine

Indexed keywords

ACTIVE; INSULIN; INSULIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; SOMATOMEDIN B RECEPTOR; UNCLASSIFIED DRUG; INSR PROTEIN, HUMAN; ISOPROTEIN; LEUKOCYTE ANTIGEN; MITOGENIC AGENT;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE M PHASE; CELL CYCLE PARAMETERS; CELL CYCLE S PHASE; CELL FUNCTION; CELL PROLIFERATION; CELL SYNCHRONIZATION; CONTROLLED STUDY; DOSE RESPONSE; ELECTROPHORESIS; FLOW CYTOMETRY; HIR CELL LINE; IMMUNOFLUORESCENCE TEST; MITOGENESIS; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR SENSITIVITY; ANIMAL; CELL MEMBRANE; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECT; HUMAN; METABOLISM; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

RATTUS;

ANIMALS; ANTIGENS, CD; CELL MEMBRANE; CELL PROLIFERATION; CULTURE MEDIA, SERUM-FREE; G0 PHASE; G1 PHASE; HUMANS; INSULIN; MITOGENS; MUSCLE CELLS; MUSCLE, SKELETAL; PROTEIN ISOFORMS; RATS; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION;

EID: 77956267447     PISSN: 07422091     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10565-009-9142-x     Document Type: Article

References (59)

1. Ahmad T, Farnie G, Bundred NJ, Anderson NG. The mitogenic action of insulin-like growth factor I in normal human mammary epithelial cells requires the epidermal growth factor receptor tyrosine kinase. J Biol Chem. 2004;279:1713-9.
2. Alexander-Bridges M, Buggs C, Giere L, Denaro M, Kahn B, White M, et al. Models of insulin action on metabolic and growth response genes. Mol Cell Biochem. 1992;109:99-105.
3. Allegra JC, Lippman ME. Growth of a human breast cancer cell line in serum-free hormone-supplemented medium. Cancer Res. 1978;38:3823-9.
4. Bahr M, Kolter T, Seipke G, Eckel J. Growth promoting and metabolic activity of the human insulin analogue [GlyA21, ArgB31, ArgB32]insulin (HOE 901) in muscle cells. Eur J Pharmacol. 1997;320:259-65.
5. Berhanu P, Anderson C, Hickman M, Ciaraldi TP. Insulin signal transduction by a mutant human insulin receptor lacking the NPEY sequence. Evidence for an alternate mitogenic signaling pathway that is independent of Shc phosphorylation. J Biol Chem. 1997;272:22884-90.
6. Berti L, Kellerer M, Bossenmaier B, Seffer E, Seipke G, Haring HU. The long acting human insulin analog HOE 901: characteristics of insulin signalling in comparison to Asp (B10) and regular insulin. Horm Metab Res. 1998;30:123-9.
7. Bornfeldt KE, Gidlof RA, Wasteson A, Lake M, Skottner A, Arnqvist HJ. Binding and biological effects of insulin, insulin analogues and insulin-like growth factors in rat aortic smooth muscle cells. Comparison of maximal growth promoting activities. Diabetologia. 1991;34:307-13.
8. Chou CK, Dull TJ, Russell DS, Gherzi R, Lebwohl D, Ullrich A, et al. Human insulin receptors mutated at the ATP-binding site lack protein tyrosine kinase activity and fail to mediate postreceptor effects of insulin. J Biol Chem. 1987;262:1842-7.
9. Christov K, Grubbs CJ, Shilkaitis A, Juliana MM, Lubet RA. Short-term modulation of cell proliferation and apoptosis and preventive/therapeutic efficacy of various agents in a mammary cancer model. Clin Cancer Res. 2007;13:5488-96.
10. De Meyts P. The structural basis of insulin and insulin-like growth factor-I receptor binding and negative cooperativity, and its relevance to mitogenic versus metabolic signalling. Diabetologia. 1994;37(Suppl 2): S135-48.
11. De Meyts P, Christoffersen CT, Urso B, Ish-Shalom D, Sacerdoti-Sierra N, Drejer K, et al. Insulin's potency as a mitogen is determined by the half-life of the insulin-receptor complex. Exp Clin Endocrinol. 1993;101(Suppl. 2):22-3.
12. Derenzini M, Montanaro L, Chilla A, Tosti E, Vici M, Barbieri S, et al. Key role of the achievement of an appropriate ribosomal RNA complement for G1-S phase transition in H4-II-E-C3 rat hepatoma cells. J Cell Physiol. 2005;202:483-91.
13. Dupont J, Le Roith D. Insulin and insulin-like growth factor I receptors: similarities and differences in signal transduction. Horm Res. 2001;55(Suppl 2):22-6.
14. Eckardt K, May C, Koenen M, Eckel J. IGF-1 receptor signalling determines the mitogenic potency of insulin analogues in human smooth muscle cells and fibroblasts. Diabetologia. 2007;50:2534-43.
15. Eckel J. Insulin analogs revisited. Curr Med Chem Immunol Endocr Metab Agents. 2005;5:475-84.
16. Erbel S, Reers C, Eckstein VW, Kleeff J, Buchler MW, Nawroth PP, et al. Proliferation of Colo-357 pancreatic carcinoma cells and survival of patients with pancreatic carcinoma is not altered by insulin glargine. Diabetes Care. 2008;31:1105-11.
17. Garg SK. New insulin analogues. Diabetes Technol Ther. 2005;7:813-7.
18. Giorgino F, Belfiore A, Milazzo G, Costantino A, Maddux B, Whittaker J, et al. Overexpression of insulin receptors in fibroblast and ovary cells induces a ligand-mediated transformed phenotype. Mol Endocrinol. 1991;5:452-9.
19. Goberdhan DC, Wilson C. The functions of insulin signaling: size isn't everything, even in Drosophila. Differentiation. 2003;71:375-97.
20. Hamel FG, Siford GL, Fawcett J, Chance RE, Frank BH, Duckworth WC. Differences in the cellular processing of AspB10 human insulin compared with human insulin and LysB28ProB29 human insulin. Metabolism. 1999;48:611-7.
21. Hansen BF, Danielsen GM, Drejer K, Sorensen AR, Wiberg FC, Klein HH, et al. Sustained signalling from the insulin receptor after stimulation with insulin analogues exhibiting increased mitogenic potency. Biochem J. 1996;315(Pt 1):271-9.
22. Hofmann C, Goldfine ID, Whittaker J. The metabolic and mitogenic effects of both insulin and insulin-like growth factor are enhanced by transfection of insulin receptors into NIH3T3 fibroblasts. J Biol Chem. 1989;264:8606-11.
23. Kaburagi Y, Yamashita R, Ito Y, Okochi H, Yamamoto-Honda R, Yasuda K, et al. Insulin-induced cell cycle progression is impaired in Chinese hamster ovary cells overexpressing insulin receptor substrate-3. Endocrinology. 2004;145:5862-74.
24. Kellerer M, Haring HU. Insulin analogues: impact of cell model characteristics on results and conclusions regarding mitogenic properties. Exp Clin Endocrinol Diabetes. 2001;109:63-4.
25. Kimura T, Van KA, Golstein J, Fusco A, Dumont JE, Roger PP. Regulation of thyroid cell proliferation by TSH and other factors: a critical evaluation of in vitro models. Endocr Rev. 2001;22:631-56.
26. Koontz JW, Iwahashi M. Insulin as a potent, specific growth factor in a rat hepatoma cell line. Science. 1981;211:947-9.
27. Kreuzer J, Nurnberg B, Krieger-Brauer HI. Ligand-dependent autophosphorylation of the insulin receptor is positively regulated by Gi-proteins. Biochem J. 2004;380:831-6.
28. Kurtzhals P. Engineering predictability and protraction in a basal insulin analogue: the pharmacology of insulin detemir. Int J Obes Relat Metab Disord. 2004;28(Suppl 2): S23-8.
29. Kurtzhals P, Schaffer L, Sorensen A, Kristensen C, Jonassen I, Schmid C, et al. Correlations of receptor binding and metabolic and mitogenic potencies of insulin analogs designed for clinical use. Diabetes. 2000;49:999-1005.
30. Lammers R, Gray A, Schlessinger J, Ullrich A. Differential signalling potential of insulin-and IGF-1-receptor cytoplasmic domains. EMBO J. 1989;8:1369-75.
31. Le RD. Insulin glargine and receptor-mediated signalling: clinical implications in treating type 2 diabetes. Diabetes Metab Res Rev. 2007;23:593-9.
32. Liefvendahl E, Arnqvist HJ. Mitogenic effect of the insulin analogue glargine in malignant cells in comparison with insulin and IGF-I. Horm Metab Res. 2008;40:369-74.
33. Mastick CC, Kato H, Roberts CT Jr, LeRoith D, Saltiel AR. Insulin and insulin-like growth factor-I receptors similarly stimulate deoxyribonucleic acid synthesis despite differences in cellular protein tyrosine phosphorylation. Endocrinology. 1994;135:214-22.
34. Milazzo G, Giorgino F, Damante G, Sung C, Stampfer MR, Vigneri R, et al. Insulin receptor expression and function in human breast cancer cell lines. Cancer Res. 1992;52:3924-30.
35. Milazzo G, Sciacca L, Papa V, Goldfine ID, Vigneri R. ASPB10 insulin induction of increased mitogenic responses and phenotypic changes in human breast epithelial cells: evidence for enhanced interactions with the insulin-like growth factor-I receptor. Mol Carcinog. 1997;18:19-25.
36. Mur C, Valverde AM, Kahn CR, Benito M. Increased insulin sensitivity in IGF-1 receptor-deficient brown adipocytes. Diabetes. 2008;51(3):743-54.
37. Nakae J, Kido Y, Accili D. Distinct and overlapping functions of insulin and IGF-I receptors. Endocr Rev. 2001;22:818-35.
38. Ohsugi M, Cras-Meneur C, Zhou Y, Bernal-Mizrachi E, Johnson JD, Luciani DS, et al. Reduced expression of the insulin receptor in mouse insulinoma (MIN6) cells reveals multiple roles of insulin signaling in gene expression, proliferation, insulin content, and secretion. J Biol Chem. 2005;280:4992-5003.
39. Okada T, Liew CW, Hu J, Hinault C, Michael MD, Krtzfeldt J, et al. Insulin receptors in beta-cells are critical for islet compensatory growth response to insulin resistance. Proc Natl Acad Sci U S A. 2007;104:8977-82.
40. Ornskov D, Nexo E, Sorensen BS. Insulin-induced proliferation of bladder cancer cells is mediated through activation of the epidermal growth factor system. FEBS J. 2006;273:5479-89.
41. Osborne CK, Bolan G, Monaco ME, Lippman ME. Hormone responsive human breast cancer in long-term tissue culture: effect of insulin. Proc Natl Acad Sci U S A. 1976;73:4536-40.
42. Randazzo PA, Morey VA, Polishook AK, Jarett L. Characterization of the growth of murine fibroblasts that express human insulin receptors. I. The effect of insulin in the absence of other growth factors. Exp Cell Res. 1990;190:25-30.
43. Reid TW, Reid WA. The labile nature of the insulin signal (s) for the stimulation of DNA synthesis in mouse lens epithelial and 3T3 cells. J Biol Chem. 1987;262:229-33.
44. Riedel H, Dull TJ, Honegger AM, Schlessinger J, Ullrich A. Cytoplasmic domains determine signal specificity, cellular routing characteristics and influence ligand binding of epidermal growth factor and insulin receptors. EMBO J. 1989;8:2943-54.
45. Roche S, Downward J, Raynal P, Courtneidge SA. A function for phosphatidylinositol 3-kinase beta (p85alpha-p110beta) in fibroblasts during mitogenesis: requirement for insulin-and lysophosphatidic acid-mediated signal transduction. Mol Cell Biol. 1998;18:7119-29.
46. Schwartz GP, Burke GT, Katsoyannis PG. A superactive insulin: [B10-aspartic acid]insulin (human). Proc Natl Acad Sci U S A. 1987;84:6408-11.
47. 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;144:2650-8.
48. Shymko RM, De MP, Thomas R. Logical analysis of timingdependent receptor signalling specificity: application to the insulin receptor metabolic and mitogenic signalling pathways. Biochem J. 1997;326(Pt 2):463-9.
49. Shymko RM, Dumont E, De MP, Dumont JE. Timing-dependence of insulin-receptor mitogenic versus metabolic signalling: a plausible model based on coincidence of hormone and effector binding. Biochem J. 1999;339(Pt 3):675-83.
50. Slieker LJ, Brooke GS, DiMarchi RD, Flora DB, Green LK, Hoffmann JA, et al. Modifications in the B10 and B26-30 regions of the B chain of human insulin alter affinity for the human IGF-I receptor more than for the insulin receptor. Diabetologia. 1997;40(Suppl 2): S54-61.
51. Soos MA, Siddle K, Baron MD, Heward JM, Luzio JP, Bellatin J, et al. Monoclonal antibodies reacting with multiple epitopes on the human insulin receptor. Biochem J. 1986;235:199-208. (Pubitemid 16041992)
52. Staiger K, Hennige AM, Staiger H, Haring HU, Kellerer M. Comparison of the mitogenic potency of regular human insulin and its analogue glargine in normal and transformed human breast epithelial cells. Horm Metab Res. 2007;39:65-7.
53. Straus DS. Growth-stimulatory actions of insulin in vitro and in vivo. Endocr Rev. 1984;5:356-69.
54. The European Agency for the Evaluation of Medicinal Products. Points to consider document on the non-clinical assessment of the carcinogenic potential of insulin analogues. (CPMP/SWP/372/01). 2001.
55. Urso B, Cope DL, Kalloo-Hosein HE, Hayward AC, Whitehead JP, O'Rahilly S, et al. Differences in signaling properties of the cytoplasmic domains of the insulin receptor and insulinlike growth factor receptor in 3T3-L1 adipocytes. J Biol Chem. 1999;274:30864-73.
56. Urso B, Ilondo MM, Holst PA, Christoffersen CT, Ouwens M, Giorgetti S, et al. IRS-4 mediated mitogenic signalling by insulin and growth hormone in LB cells, a murine T-cell lymphoma devoid of IGF-I receptors. Cell Signal. 2003;15:385-94.
57. Vajo Z, Fawcett J, Duckworth WC. Recombinant DNA technology in the treatment of diabetes: insulin analogs. Endocr Rev. 2001;22:706-17.
58. Vincent MT, Carroll RJ, Hammer RE, Chan SJ, Guz Y, Steiner DF, et al. A transgene coding for a human insulin analog has a mitogenic effect on murine embryonic beta cells. Proc Natl Acad Sci U S A. 1995;92:6239-43.
59. Zib I, Raskin P. Novel insulin analogues and its mitogenic potential. Diabetes Obes Metab. 2006;8:611-20.