Ligand-binding affinity at the insulin receptor isoform-A and subsequent IR-A tyrosine phosphorylation kinetics are important determinants of mitogenic biological outcomes

Frontiers in Endocrinology

Volumn 6, Issue JUL, 2015, Pages

  Rajapaksha, Harinda ^a   Forbes, Briony E ^a,b  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b FLINDERS UNIVERSITY   (Australia)

Author keywords

Igf ii; Insulin analogs; Insulin receptor; Intracellular signaling; Metabolic; Mitogenic; Receptor internalization

Indexed keywords

INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR ISOFORM A; INSULIN RECEPTOR KINASE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PROTEIN S597; SOMATOMEDIN B; SOMATOMEDIN C; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL PROLIFERATION; COMPETITIVE BINDING ASSAY; CONTROLLED STUDY; DNA SYNTHESIS; EC50; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ANALYSIS; GENE OVEREXPRESSION; IMMUNOBLOTTING; INTERNALIZATION; LIGAND BINDING; MITOGENESIS; MYOBLAST; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 84938935332     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2015.00107     Document Type: Article

References (43)

1. Brown J, Jones EY, Forbes BE. Interactions of IGF-II with the IGF2R/cation-independent mannose-6-phosphate receptor mechanism and biological outcomes. Vitam Horm (2009) 80:699-719. doi:10.1016/S0083-6729(08)00625-0.
2. Denley A, Cosgrove LJ, Booker GW, Wallace JC, Forbes BE. Molecular interactions of the IGF system. Cytokine Growth Factor Rev (2005) 16:421-39. doi:10.1016/j.cytogfr.2005.04.004.
3. Ward CW, Menting JG, Lawrence MC. The insulin receptor changes conformation in unforeseen ways on ligand binding: sharpening the picture of insulin receptor activation. Bioessays (2013) 35:945-54. doi:10.1002/bies.201300065.
4. Belfiore A, Malaguarnera R. Insulin receptor and cancer. Endocr Relat Cancer (2011) 18:R125-47. doi:10.1530/ERC-11-0074.
5. Seino S, Bell GI. Alternative splicing of human insulin receptor messenger RNA. Biochem Biophys Res Commun (1989) 159:312-6. doi:10.1016/0006-291X(89)92439-X.
6. Denley A, Bonython ER, Booker GW, Cosgrove LJ, Forbes BE, Ward CW, et al. 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) 18:2502-12. doi:10.1210/me.2004-0183.
7. Gauguin L, Klaproth B, Sajid W, Andersen AS, Mcneil KA, Forbes BE, et al. Structural basis for the lower affinity of the insulin-like growth factors for the insulin receptor. J Biol Chem (2008) 283:2604-13. doi:10.1074/jbc.M709220200.
8. Belfiore A, Frasca F, Pandini G, Sciacca L, Vigneri R. Insulin receptor isoforms and insulin receptor/insulin-like growth factor receptor hybrids in physiology and disease. Endocr Rev (2009) 30:586-623. doi:10.1210/er.2008-0047.
9. 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. doi:10.1006/dbio.1997.8666.
10. Vella V, Pandini G, Sciacca L, Mineo R, Vigneri R, Pezzino V, et al. A novel autocrine loop involving IGF-II and the insulin receptor isoform-A stimulates growth of thyroid cancer. J Clin Endocrinol Metab (2002) 87:245-54. doi:10.1210/jcem.87.1.8142.
11. Frasca F, Pandini G, Sciacca L, Pezzino V, Squatrito S, Belfiore A, et al. The role of insulin receptors and IGF-I receptors in cancer and other diseases. Arch Physiol Biochem (2008) 114:23-37. doi:10.1080/13813450801969715.
12. Jiang L, Zhu W, Streicher K, Morehouse C, Brohawn P, Ge X, et al. Increased IR-A/IR-B ratio in non-small cell lung cancers associates with lower epithelial-mesenchymal transition signature and longer survival in squamous cell lung carcinoma. BMC Cancer (2014) 14:131. doi:10.1186/1471-2407-14-131.
13. 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) 278:42178-89. doi:10.1074/jbc.M304980200.
14. Sacco A, Morcavallo A, Pandini G, Vigneri R, Belfiore A. Differential signaling activation by insulin and insulin-like growth factors I and II upon binding to insulin receptor isoform A. Endocrinology (2009) 150:3594-602. doi:10.1210/en.2009-0377.
15. Morcavallo A, Gaspari M, Pandini G, Palummo A, Cuda G, Larsen MR, et al. Research resource: new and diverse substrates for the insulin receptor isoform A revealed by quantitative proteomics after stimulation with IGF-II or insulin. Mol Endocrinol (2011) 25:1456-68. doi:10.1210/me.2010-0484.
16. Jensen M, Hansen B, De Meyts P, Schaffer L, Urso B. Activation of the insulin receptor by insulin and a synthetic peptide leads to divergent metabolic and mitogenic signaling and responses. J Biol Chem (2007) 282:35179-86. doi:10.1074/jbc.M704599200.
17. Alvino CL, Ong SC, Mcneil KA, Delaine C, Booker GW, Wallace JC, et al. Understanding the mechanism of insulin and insulin-like growth factor (IGF) receptor activation by IGF-II. PLoS One (2011) 6:e27488. doi:10.1371/journal.pone.0027488.
18. Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E, Murray B, et al. PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res (2012) 40:D261-70. doi:10.1093/nar/gkr1122.
19. Taniguchi CM, Emanuelli B, Kahn CR. Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol (2006) 7:85-96. doi:10.1038/nrm1837.
20. Jensen M, De Meyts P. Molecular mechanisms of differential intracellular signaling from the insulin receptor. Vitam Horm (2009) 80:51-75. doi:10.1016/S0083-6729(08)00603-1.
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. De Meyts P, Shymko RM. Timing-dependent modulation of insulin mitogenic versus metabolic signalling. Novartis Found Symp (2000) 227:46-57. doi:10.1002/0470870796.ch4.
23. 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. doi:10.2337/diabetes.49.6.999.
24. Rakatzi I, Ramrath S, Ledwig D, Dransfeld O, Bartels T, Seipke G, et al. A novel insulin analog with unique properties: LysB3, GluB29 insulin induces prominent activation of insulin receptor substrate 2, but marginal phosphorylation of insulin receptor substrate 1. Diabetes (2003) 52:2227-38. doi:10.2337/diabetes.52.9.2227.
25. Foti M, Moukil MA, Dudognon P, Carpentier JL. Insulin and IGF-1 receptor trafficking and signalling. Novartis Found Symp (2004) 262:125-41. doi:10.1002/0470869976.ch8.
26. Hamer I, Foti M, Emkey R, Cordier-Bussat M, Philippe J, De Meyts P, et al. An arginine to cysteine(252) mutation in insulin receptors from a patient with severe insulin resistance inhibits receptor internalisation but preserves signalling events. Diabetologia (2002) 45:657-67. doi:10.1007/s00125-002-0798-5.
27. Ceresa BP, Kao AW, Santeler SR, Pessin JE. Inhibition of clathrin-mediated endocytosis selectively attenuates specific insulin receptor signal transduction pathways. Mol Cell Biol (1998) 18:3862-70.
28. Alvino CL, Mcneil KA, Ong SC, Delaine C, Booker GW, Wallace JC, et al. A novel approach to identify two distinct receptor binding surfaces of insulin-like growth factor II. J Biol Chem (2009) 284:7656-64. doi:10.1074/jbc.M808061200.
29. Jensen M, Palsgaard J, Borup R, De Meyts P, Schaffer L. Activation of the insulin receptor (IR) by insulin and a synthetic peptide has different effects on gene expression in IR-transfected L6 myoblasts. Biochem J (2008) 412:435-45. doi:10.1042/BJ20080279.
30. Pillutla RC, Hsiao KC, Beasley JR, Brandt J, Ostergaard S, Hansen PH, et al. Peptides identify the critical hotspots involved in the biological activation of the insulin receptor. J Biol Chem (2002) 277:22590-4. doi:10.1074/jbc.M202119200.
31. Schaffer L, Brissette RE, Spetzler JC, Pillutla RC, Ostergaard S, Lennick M, et al. Assembly of high-affinity insulin receptor agonists and antagonists from peptide building blocks. Proc Natl Acad Sci U S A (2003) 100:4435-9. doi:10.1073/pnas.0830026100.
32. Menting JG, Ward CW, Margetts MB, Lawrence MC. A thermodynamic study of ligand binding to the first three domains of the human insulin receptor: relationship between the receptor alpha-chain C-terminal peptide and the site 1 insulin mimetic peptides. Biochemistry (2009) 48:5492-500. doi:10.1021/bi900261q.
33. Gauguin L. (2008). Ph.D. thesis, The University of Copenhagen.
34. Soos MA, O'Brien RM, Brindle NP, Stigter JM, Okamoto AK, Whittaker J, et al. Monoclonal antibodies to the insulin receptor mimic metabolic effects of insulin but do not stimulate receptor autophosphorylation in transfected NIH 3T3 fibroblasts. Proc Natl Acad Sci U S A (1989) 86:5217-21. doi:10.1073/pnas.86.14.5217.
35. Ganderton RH, Stanley KK, Field CE, Coghlan MP, Soos MA, Siddle K. A monoclonal anti-peptide antibody reacting with the insulin receptor beta-subunit. Characterization of the antibody and its epitope and use in immunoaffinity purification of intact receptors. Biochem J (1992) 288(Pt 1):195-205.
36. Daunt DA, Hurt C, Hein L, Kallio J, Feng F, Kobilka BK. Subtype-specific intracellular trafficking of alpha2-adrenergic receptors. Mol Pharmacol (1997) 51:711-20.
37. Frasca F, Pandini G, Scalia P, Sciacca L, Mineo R, Costantino A, et al. Insulin receptor isoform A, a newly recognized, high-affinity insulin-like growth factor II receptor in fetal and cancer cells. Mol Cell Biol (1999) 19:3278-88.
38. Morcavallo A, Genua M, Palummo A, Kletvikova E, Jiracek J, Brzozowski AM, et al. Insulin and insulin-like growth factor II differentially regulate endocytic sorting and stability of the insulin receptor isoform A. J Biol Chem (2012) 287(14):11422-36. doi:10.1074/jbc.M111.252478.
39. Tinti M, Nardozza AP, Ferrari E, Sacco F, Corallino S, Castagnoli L, et al. The 4G10, pY20 and p-TYR-100 antibody specificity: profiling by peptide microarrays. N Biotechnol (2012) 29:571-7. doi:10.1016/j.nbt.2011.12.001.
40. Hansen BF, Glendorf T, Hegelund AC, Lundby A, Lutzen A, Slaaby R, et al. Molecular characterisation of long-acting insulin analogues in comparison with human insulin, IGF-1 and insulin X10. PLoS One (2012) 7:e34274. doi:10.1371/journal.pone.0034274.
41. Knudsen L, Hansen BF, Jensen P, Pedersen TA, Vestergaard K, Schaffer L, et al. Agonism and antagonism at the insulin receptor. PLoS One (2012) 7:e51972. doi:10.1371/journal.pone.0051972.
42. Whittaker L, Hao C, Fu W, Whittaker J. High-affinity insulin binding: insulin interacts with two receptor ligand binding sites. Biochemistry (2008) 47:12900-9. doi:10.1021/bi801693h.
43. Svendsen AM, Winge SB, Zimmermann M, Lindvig AB, Warzecha CB, Sajid W, et al. Down-regulation of cyclin G2 by insulin, IGF-I (insulin-like growth factor 1) and X10 (AspB10 insulin): role in mitogenesis. Biochem J (2014) 457:69-77. doi:10.1042/BJ20130490.