Growth effects of insulin and insulin analogues

Archives of Physiology and Biochemistry

Volumn 115, Issue 2, 2009, Pages 72-85

  Sandow, Juergen ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Insulin; Insulin analogues; Mitogenicity; Risk assessment; Tumour progression

Indexed keywords

ANIMALIA; RODENTIA;

ANTIDIABETIC AGENT; DRUG DERIVATIVE; INSULIN; INSULIN, ASP(B10); INSULIN, ASP(B10)-; SOMATOMEDIN C RECEPTOR;

ANIMAL; CELL PROLIFERATION; DRUG EFFECT; HUMAN; METABOLISM; MITOSIS; REVIEW;

ANIMALS; CELL PROLIFERATION; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; MITOSIS; RECEPTOR, IGF TYPE 1;

EID: 68149134500     PISSN: 13813455     EISSN: 17444160     Source Type: Journal    
DOI: 10.1080/13813450902835690     Document Type: Review

References (111)

1. Andersen L, Jorgensen PN, Jensen LB, Walsh D. (2000). A new insulin immunoassay specific for the rapid-acting insulin analogue, insulin aspart, suitable for bioavailability, bioequivalence, and pharmacokinetic studies. Clin Biochem 33(8):627-633
2. August GP, Nissley SP, Kasuga M, Lee L, Greenstein L, Rechler MM. (1983). Purification of an insulin-like growth factor I1 receptor from rat chondrosarcoma cells. J Biol Chem 258:9033.
3. Baehr M, Kolter T, Seipke G, Eckel J. (1997). Growth-promoting and metabolic activity of the human insulin analog (Gly(a21), Arg(b31), Arg(b32)) insulin (Hoe-901) in muscle-cells. Eur J Pharmacol 320:259-265.
4. Bennett LM, Davis BJ. (2002). Identification of mammary carcinogens in rodent bioassays. Environ Mol Mutagen 39(2-3):150-157
5. Berster JM, Göke, B. (2008). Type 2 diabetes mellitus as risk factor for colorectal cancer. Arch Physiol Biochem 114(1):84-98.
6. Berti L, Kellerer M, Bossenmaier B, Seffer E, Seipke G, Haring H. (1998). The long-acting human insulin analog HOE901: Characteristics of insulin signalling in comparison to Asp(B10) and regular insulin. Horm Metab Res 30:123-129
7. Bode G. (2006). International guidelines for the development of pharmaceutical compounds (Chapter III.B). In: Vogel HG, editor. Drug discovery and the evaluation: Safety and pharmacokinetic assays. Berlin/New York: Springer Verlag, pp. 759-777
8. Chantelau E, Kimmerle R, Meyer-Schwickerath R. (2008). Insulin, insulin analogues and diabetic retinopathy. Arch Physiol Biochem 114(1):54-62.
9. Ciaraldi TP, Carter L, Seipke G, Mudaliar S, Henry RR. (2001). Effects of the long-acting insulin analog insulin glargine on cultured human skeletal muscle cells: Comparisons to insulin and IGF-I. J Clin Endocrinol Metab 86:5838-5847
10. Ciaraldi TP, Phillips SA, Carter L, Aroda V, Mudaliar S, Henry RR. (2005). Effects of the rapid-acting insulin analog glulisine on cultured human skeletal muscle cells: Comparisons with insulin and insulin-like growth factor I. J Clin Endocrinol Metab 90(10):5551-5558
11. Clarke R, Dickson RB, Brünner N. (1990). The process of malignant progression in human breast cancer. Ann Oncol 1(6):401-407
12. Clarke R, Skaar T, Baumann K, Leonessa F, James M, Lippman J, Thompson EW, Freter C, Brunner N. (1994). Hormonal carcinogenesis in breast cancer: cellular and molecular studies of malignant progression. Breast Cancer Res Treat 31(2-3):237-248
13. Cohen ND, Hilf R. (1974). Influence of insulin on growth and metabolism of 7,12-dimethylbenz(a)anthracene-induced mammary tumors. Cancer Res 34:3245-3252
14. Coughlin SS, Calle EE, Teras LR, Petrelli J, Thun MJ. (2004). Diabetes mellitus as a predictor of cancer mortality in a large cohort of US adults. Am J Epidemiol 159:1160-1167
15. Davis MD, Beck RW, Home PD, Sandow J, Ferris FL. (2007). Early retinopathy progression in four randomized trials comparing insulin glargine and NPH insulin. Exp Clin Endocrinol Diabetes 115:240-243 (Erratum in: Exp Clin Endocrinol Diabetes 2007; 115:473).
16. De Meyts P, Christoffersen CT, Urso B, Wallach B, Gronskov K, Yakushiji F, Shymko RM. (1995a). Role of the time factor in signaling specificity: Application to mitogenic and metabolic signaling by the insulin and insulin-like growth factor-I receptor tyrosine kinases. Metabolism 44(10, Suppl 4):2-11.
17. Dideriksen LH, Jorgensen LN, Drejer K. (1992). Carcinogenic effect on female rats after 12 months administration of the insulin analogue B10 Asp. Diabetes 41:143A.
18. Eckardt K, May C, Koenen M, Eckel J. (2007). IGF-1 receptor signalling determines the mitogenic potency of insulin analogues in human smooth muscle cells and fibroblasts. Diabetologia 50:2534-2540.
19. EMEA (2000). (European Medicines Agency). EPAR for authorised medicinal product for human use - Lantus (insulin glargine INN) - 061500en6 scientific discussion
20. EMEA (2001). (Scientific Guideline). Points to consider document on the non-clinical assessment of the carcinogenic potential of insulin analogues. CPMP/SWP/2877 EMEA Safety Working Party, document 037201en
21. EMEA (2003). (Scientific Guideline). Note for Guidance on Carcinogenic Potential CPMP/SWP/2877 EMEA Safety Working Party, document 287700en
22. EMEA (2004a). (European Medicines Agency). EPAR for authorised medicinal product for human use - Actrapid (insulin human INN) 204302en6 scientific discussion
23. EMEA (2004b). (European Medicines Agency). EPAR for authorised medicinal product for human use - NovoRapid (insulin aspart INN) 272799en6 scientific discussion
24. EMEA (2004c). (European Medicines Agency). EPAR for authorised medicinal product for human use - Levemir. (insulin detemir INN) 093604en6 scientific discussion
25. EMEA (2005a). (European Medicines Agency). EPAR for authorised medicinal product for human use - Apidra. (insulin glulisine INN) 121804en6 scientific discussion
26. EMEA (2005b). (European Medicines Agency). EPAR for authorised medicinal product for human use - Humalog. (insulin lispro INN) 060195en6 scientific discussion
27. EMEA (2005c). (European Medicines Agency). EPAR for authorised medicinal product for human use - Insuman. (insulin human INN) 089696en6 scientific discussion
28. EMEA (2007). (European Medicines Agency). EPAR for authorised medicinal product for human use - Increlex (mecasermin INN), Human Recombinant IGF-I, H-704-en6 scientific discussion
29. Erbel S, Reers C, Eckstein VW, Kleeff J, Büchler MW, Nawroth PP, Ritzel RA. (2008). Proliferation of Colo-357 pancreatic carcinoma cells and survival of patients with pancreatic carcinoma is not altered by insulin glargine. Diabetes Care 31:1105-1111
30. Frasca F, Pandini G, Vigneri R, Goldfine ID. (2003). Insulin and hybrid insulin/IGF receptors are major regulators of breast cancer cells. Breast Dis 17:73-89.
31. Frasca F, Pandini G, Sciacca L, Pezzino V, Squatrito S, Belfiore A. Vigneri R. (2008). The role of insulin receptors and IGF-I receptors in cancer and other diseases. Arch Physiol Biochem 114(1):23-37.
32. Friberg S, Mattson S. (1997). On the growth rates of human malignant tumors: Implications for medical decision making. J Surg Oncol, 65:284-297
33. Frittitta L, Vigneri R, Stampfer MR, Goldfine ID. (1995). Insulin receptor overexpression in 184B5 human mammary epithelial cells induces a ligand-dependent transformed phenotype. J Cell Biochem 57:666-669.
34. Fürstenberger G, Senn HJ. (2002). Insulin-like growth factors and cancer. Lancet Oncol 3:298-302.
35. Giovannucci E. (1995). Insulin and colon cancer. Cancer Causes Cont 6:164-179
36. Grasso P, Golberg L. (1966). Subcutaneous sarcoma as an index of carcinogenic potency. Food Cosmet Toxicol 4(3):297-320.
37. Hadsell DL, Bonnette SG. (2000). IGF and insulin action in the mammary gland: Lessons from transgenic and knockout models. J Mam Gland Biol Neoplasia 5(1):19-30.
38. Hansen BF, Danielsen GM, Drejer K, Sorensen AR, Wiberg FC, Klein HH, Lundemose AG. (1996). Sustained signalling from the insulin receptor after stimulation with insulin analogues exhibiting increased mitogenic potency. Biochem J 315:271-279
39. Hansen BF. (2008). Insulin analogues with increased mitogenic potency-are they safe? Horm Metab Res 40:431-433
40. Heise T, Bott S, Rave K, Dressler A, Rosskamp R, Heinemann L. (2002). No evidence for accumulation of insulin glargine (LANTUS): A multiple injection study in patients with Type 1 diabetes. Diabet Med 19:490-495
41. Hennige AM, Strack V, Metzinger E, Seipke G, Haering HU, Kellerer M. (2005a). Effects of new insulin analogues HMR1964 (insulin glulisine) and HMR1423 on insulin receptors. Diabetologia 48:1891-1897
42. Hennige AM, Lehmann R, Weigert C, Moeschel K, Schaeuble M, Metzinger E, Lammers R, Haering HU. (2005b). Insulin glulisine. Insulin receptor signaling characteristics in vivo. Diabetes 54:361-366
43. Hennige AM, Kellerer M, Strack V, Metzinger E, Seipke G, Haring HU. (1999). New human insulin analogs: Characteristics of insulin signalling in comparison to ASP (B10) and regular insulin. Diabetologia 42:A178 (Abstract 665).
44. Heuson JC, Coune A, Heimann R. (1967). Cell proliferation induced by insulin in organ culture of rat mammary carcinoma. Exp Cell Res 45:351-360
45. Heuson JC, Legros N, Heimann R. (1972). Influence of insulin administraton on growth of the 7,12-dimethylbenz(a) anthracene-induced mammary carcinoma in intact, oophorectomized and hypophysectomized rats. Cancer Res 32:233-238
46. Hill DJ, Milner RD. (1985). Insulin as a growth factor. Pediatr Res 19(9):879-886
47. IARC (2008). International Agency for Research on Carcinogenic Risks to Humans: Complete List of Agents evaluated and their classification. [http: monographs.iarc.fr/ENG/ Classification/index.php].
48. Ibrahim YH, Yee D. (2004). Insulin-like growth factor-I and cancer risk. Growth Horm & IGF Res 14(4):261-269
49. Ish-Shalom D, Tzivion G, Christoffersen CT, Ursø B, De Meyts P, Naor D. (1995). Mitogenic potential of insulin on lymphoma cells lacking IGF-I receptors. Ann NY Acad Sci 766:409-415
50. Kellerer M, Haering HU. (2001). Insulin analogues: Impact of cell model characteristics on results and conclusions regarding mitogenic properties. Exp Clin Endocrinol Diab 109:63-64.
51. Khandwala HM, McCutcheon IE, Flyvbjerg A, Friend KE. (2000). The effects of insulin-like growth factors on tumorigenesis and neoplastic growth. Endocr Rev 21(3):215-244
52. Koontz JW, Iwahashi M. (1981). Insulin as a potent, specific growth factor in a rat hepatoma cell line. Science 211:947.
53. Kurtzhals P, Schaeffer L, Sorensen A, Kristensen C, Jonassen I, Schmid C, Trueb T. (2000). Correlations of receptor binding and metabolic and mitogenic potencies of insulin analogs designed for clinical use. Diabetes 49:999-(1005).
54. Laron Z. (1981). Insulin as a growth-promoting hormone. In: Collu R, Ducharme JR, Guyda H, editors. Pediatric endocrinology. New York: Raven Press, pp 149-165
55. Laron Z. (2001). Insulin-like growth factor 1 (IGF-1): A growth hormone. J Clin Pathol Med: Mol Pathol 54:311-316
56. Laron Z. (2008). Insulin-a growth hormone. Arch Physiol Biochem 114(1):11-16.
57. Larsson SC, Orsini N, Wolk A. (2005). Diabetes mellitus and risk of colorectal cancer: A meta-analysis. J Natl Cancer Inst 97:1679-1687 (Pubitemid 41672234)
58. Leroith D, Roberts CT. (2003). The insulin-like growth factor system and cancer. Cancer Letters 195:127-137
59. Leroith D. (2007). Insulin glargine and receptor-mediated signalling: Clinical implications in treating type 2 diabetes. Diabetes Metab Res Rev 23(8):593-599
60. Li G, Barrett EJ, Wang H, Chai W, Liu Z. (2005). Insulin at physiological concentrations selectively activates insulin but not insulin-like growth factor I (IGF-I) or insulin/ IGF-I hybrid receptors in endothelial cells. Endocrinol 146(11):4690-4696
61. Liefvendahl E, Arnqvist HJ. (2008). Mitogenic effect of the insulin analogue glargine in malignant cells in comparison with insulin and IGF-1. Horm Metab Res 40(6):369-374
62. Lijinsky W. (1996). Modulating effects of hormones on carcinogenesis. Prog Clin Biol Res 394:57-76.
63. Lippman ME, Osborne CK, Knazek R, Young N. (1977). In vitro model systems for the study of hormone-dependent human breast cancer. New Engl J Med 296:154-159
64. Lu S, Lee WM, Archer MC. (1998) Insulin does not promote rat mammary carcinogenesis. Carcinogenesis. 19(4): 699-702.
65. Messerschmitt PJ, Rettew AN, Brookover RE, Garcia RM, Getty PJ, Greenfield EM. (2008). Specific tyrosine kinase inhibitors regulate human osteosarcoma cells in vitro. Clin Orthop Relat Res 466(9):2168-2175 (Epub 2008).
66. MacEwen EG, Pastor J, Kutzke J, Tsan R, Kurzman ID, Thamm DH, Wilson M, Radinsky R. (2004). IGF-1 receptor contributes to the malignant phenotype in human and canine osteosarcoma. J Cell Biochem 92(1):77-91.
67. Marquardt H, Pfau W. (2004). Epigenetische nicht-genotoxische Cancerogenese. In: Marquardt H, Schaefer S, editors. Lehrbuch der Toxikologie. Stuttgart, Germany: Wissenschaftl. Verlagsgesellsch., pp 171-174.
68. Massague J, Blinderman LA, Czech MP. (1982). The high affinity insulin receptor mediates growth stimulation in rat hepatoma cells. J Biol Chem 257:1(3958).
69. Mayer D, Shukla A, Enzmann H. (2008). Proliferative effects of insulin analogues on mammary epithelial cells. Arch Physiol Biochem 114(1):38-44.
70. Meister P. (1996). Malignant fibrous histiocytoma: Histomorphological pattern or tumor type. Pathol Res Pract 192(8):877-881
71. Milazzo G, Sciacca L, Papa V, Goldfine ID, Vigneri R. (1997). 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 Carcin 18:19-25.
72. Milazzo G, Giorgino F, Damante G, Sung C, Stampfer MR, Vigneri R, Goldfine ID, Belfiore A. (1992). Insulin receptor expression and function in human breast cancer cell lines. Cancer Res 52:3924-3930.
73. Mueller G, Herling AW, Sandow J. (2007). Antidiabetic activity (Chapter K). In: Vogel HG, editor. Drug discovery and evaluation: Pharmacological assays. Vol.2. Berlin/New York: Springer Verlag, pp. 1323-1589.
74. Osborne CK, Clemmons DR, Arteaga CL. (1990). Regulation of breast cancer growth by insulin-like growth factors. J Steroid Biochem Mol Biol 37(6):805-809
75. Osborne CK, Hobbs K, Trent JM. (1987). Biological differences among MCF-7 human breast cancer cell lines from different laboratories. Breast Cancer Res Treat 9(2):111-121
76. Osborne CK, Monaco ME, Lippman ME, Kahn CR. (1978). Correlation among insulin binding, degradation, and biological activity in human breast cancer cells in long-term tissue culture. Cancer Res 38(1):94-102.
77. Osborne CK, Bolain G, Monaco ME, Lippman ME. (1976). Hormone responsive human breast cancer in long termtissue culture. IV. The effect of insulin. Proc Nat Acad Sci US 73:4536-4540
78. Pandini G, Frasca F, Mineo R, Sciacca L, Vigneri R, Belfiore A. (2003). Insulin/insulin-like growth factor I hybrid receptors have different biological characteristics depending on the insulin receptor isoforms. Biochem J 290(Pt 2):419-426
79. Pisani P. (2008). Hyper-insulinaemia and cancer, meta- analyses of epidemiological studies. Arch Physiol Biochem 114(1):63-70.
80. Quattrin T, Thrailkill K, Baker L, Kuntze J, Compton P, Martha P; rhIGF-1 Study Group. (2001). Improvement of HbA1c without increased hypoglycemia in adolescents and young adults with type-1 diabetes mellitus treated with recombinant human insulin-like growth factor-1 and insulin. rhIGF-1 in IDDM Study Group. J Pediatr Endocrinol Metab 14:267-277
81. Renehan AG, Shalet SM. (2005). Diabetes, insulin therapy, and colorectal cancer. Br Med J 330:551-552
82. Renehan AG, Zwahlen M, Minder C, O'Dwyer ST, Shalet SM, Egger M. (2004). Insulin-like growth factor (IGF)-I, IGF binding protein-3, and cancer risk: Systematic review and meta-regression analysis. Lancet 363:1346-1353
83. Renehan AG, Roberts DL, Dive C. (2008). Obesity and cancer: Pathophysiological and biological mechanisms. Arch Physiol Biochem 114(1):71-83.
84. Rose DP, Haffner SM, and Baillargeon J. (2007). Adiposity, the metabolic syndrome, and breast cancer in African- American and white American women. Endocrine Reviews 28(7):763-777
85. Rosenstock J, Fonseca V, Mcgill J, Riddle M, Hallé Jp, Hramiak I, Johnston P, Davis M. (2008). Similar progression of diabetic retinopathy with glargine or NPH insulin in Type 2 diabetes (T2D). American Diabetes Association 68th Symposium 6-10 June 2008, San Francisco, CA, USA, Suppl. 2008:301-OR.
86. Russo IH, Russo J. (1996). Mammary gland neoplasia in long-term rodent studies. Environ Health Perspect 104(9):938-967
87. Russo IH, Russo J. (1998). Role of hormones in mammary cancer initiation and progression. J Mammary Gland Biol Neoplasia 3(1):49-61.
88. Sandow J. (2007). Insulin analogues: Assessment of insulin mitogenicity and IGF-I activity (Chapter K.9). In: Vogel HG, editor. Drug discovery and evaluation: Pharmacological assays. Vol.2. Berlin/New York: Springer Verlag, pp. 1592-1607.
89. Salter J, Best CH. (1953). Insulin as a growth hormone. Br Med J 2:353-356
90. Samani M, et al. (2007). The role of the IGF system in cancer growth and metastasis: Overview and recent insights. Endocrine Rev 28(1): 20-47.
91. Schmid C, Keller C, Gosteli PM, Zapf J. (1999). Mitogenic and antiapoptotic effects of insulin-like growth factor binding protein-6 in the human osteoblastic osteosarcoma cell line Saos-2/B-10. Biochem Biophys Res Commun 263(3): 786-789
92. Seipke G, Sandow J, Geisen K, Stammberger I. 2000. Preclinical profile of the new long-acting insulin glargine (HOE 901). Endocrine Society 82nd Annual Meeting 2000, 21-24 June 2000, Toronto Canada, Suppl. 2000:283-ABS.
93. Shukla A, Grisouard J, Ehemann V, Hermani A, Enzmann H, Mayer D. (2009). Analysis of signaling pathways related to cell proliferation stimulated by insulin analogs in human mammary epithelial cell lines. Endocr Relat Cancer (19 January 2009; Epub ahead of print).
94. Slaaby R, Schaffer L, Lautrup-Larsen I, Andersen AS, Shaw AC, Mathiasen IS, Brandt J. (2006). Hybrid receptors formed by insulin receptor (IR) and insulin-like growth factor I receptor (IGF-IR) have low insulin and high IGF-1 affinity irrespective of the IR splice variant. J Biol Chem 281(36): 25869-25874
95. Slieker LJ, Brooke GS, DiMarchi RD, Flora DB, Green LK, Hoffmann JA, Long HB, Fan L, Shields JE, Sundell KL et al. (1997). 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. 40(Suppl 2):S54-61.
96. Soule HD, Vazquez J, Long A, Albert S, Brennan MA. (1973). Human cell line from a pleural effusion derived from a breast carcinoma. J Natl Cancer Inst 57:1409-1417.
97. Staiger K, Hennige AM, Staiger H, Haering HU, Kellerer M. (2007). Comparison of the mitogenic potency of regular human insulin and its analogue glargine in normal and transformed human breast epithelial cells. Hormone Met 39:65-67
98. Stammberger I, Bube A, Durchfeld-Meyer B, Donaubauer H, Troschau G. (2002). Evaluation of the carcinogenic potential of insulin glargine (LANTUS) in rats and mice. Int J Toxicol 21:171-179 (Pubitemid 34803492)
99. Stammberger I, Seipke G, Bartels T. (2006). Insulin glulisine- a comprehensive preclinical evaluation. Int J Toxicol 25(1):25-33.
100. Straus DS. (1981). Effects of insulin on cellular growth and proliferation. Life Sci 29:2131.
101. Straus DS. (1984). Growth-stimulatory actions of insulin in vitro and in vivo. Endocrine Rev 5(2):356-369
102. Suntzeff V, Babcock R, Loeb L. (1940). The development of sarcoma in mice following long continued injections of a buffered solution of hydrochloric acid. Am J Cancer 39:36-60.
103. Surmacz E. (2000). Function of the IGF-I receptor in breast cancer. J Mammary Gland Biol Neoplasia 5(1):95-105.
104. Tran TT, Medline A, Bruce WR. (1996). Insulin promotion of colon tumours in rats. Cancer Epidemiol Biomarkers Prev 5:1013-1015
105. Weinstein D, Simon M, Yehezkel E, Laron Z, Werner H. (2009). Insulin analogues display IGF-I-like mitogenic and antiapoptotic activities in cultured cancer cells. Diabetes Metab Res Rev 25(1):41-49
106. Weiss SW, Enzinger FM. (1978). Malignant fibrous histiocytoma. Cancer 41:2250-2266.
107. Weiss SW, Rao VK. (1992). Well-differentiated liposarcoma (atypical lipoma) of deep soft tissue of the extremities, retroperitoneum, and miscellaneous sites. A follow-up study of 92 cases with analysis of the incidence of "dedifferentiation". Am J Surg Pathol 16:1051-1058
108. Whitehead JP, Clark SF, Urso B, James DE. (2000). Signalling through the insulin receptor. Curr Opin Cell Biol 12(2):222-228
109. Williams GM, Latropoulos MJ. (2001). Principles of testing for carcinogenic activity. In: Hayes W, editor. Principles and methods of toxicology. 4th edition. Taylor & Francis, pp. 959-1000.
110. Wu Y, Yakar S, Zhao L, Hennighausen L, LeRoith D. (2002). Circulating insulin-like growth factor-I levels regulate colon cancer growth and metastasis. Cancer Res 62(4):1030-1035
111. Zib I, Raskin P. (2006). Novel insulin analogues and its mitogenic potential. Diabetes Obes Metab 8(6):611-620