PEGylation enhances the therapeutic potential for insulin-like growth factor I in central nervous system disorders

Growth Hormone and IGF Research

Volumn 21, Issue 5, 2011, Pages 292-303

  Saenger, S ^a   Goeldner, C ^a   Frey, J R ^a   Ozmen, L ^a   Ostrowitzki, S ^a   Spooren, W ^a   Ballard, T M ^a   Prinssen, E ^a   Borroni, E ^a   Metzger, F ^a  

^a F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

Brain homeostasis; IGF 1; Neurodevelopmental disorders; PEGylated IGF; Synaptic plasticity

Indexed keywords

INSULIN; MACROGOL; RECOMBINANT SOMATOMEDIN C; SOMATOMEDIN C;

ACUTE DRUG ADMINISTRATION; AMYLOIDOSIS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM DISEASE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG CEREBROSPINAL FLUID LEVEL; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG EFFICACY; DRUG HALF LIFE; DRUG MECHANISM; DRUG PENETRATION; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; STEADY STATE;

ANIMALS; BRAIN; BRAIN CHEMISTRY; CENTRAL NERVOUS SYSTEM DISEASES; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; POLYETHYLENE GLYCOLS; RATS; RATS, WISTAR; TIME FACTORS;

EID: 80052565466     PISSN: 10966374     EISSN: 15322238     Source Type: Journal    
DOI: 10.1016/j.ghir.2011.07.006     Document Type: Article

References (86)

1. F. Metzger, W. Sajid, C. Staudenmaier, et al., Separation of fast from slow anabolism by site-specific PEGylation of insulin-like growth factor I. J. Biol. Chem. 286 (2011) 19501-19510.
2. Yakar S., Liu J.L., Stannard B., Butler A., Accili D., Sauer B., LeRoith D. Normal growth and development in the absence of hepatic insulin-like growth factor I. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7324-7329.
3. Werther G.A., Abate M., Hogg A., et al. Localization of insulin-like growth factor-I mRNA in rat brain by in situ hybridization-relationship to IGF-I receptors. Mol. Endocrinol. 1990, 4:773-778.
4. Bondy C.A. Transient IGF-I gene expression during the maturation of functionally related central projection neurons. J. Neurosci. 1991, 11:3442-3455.
5. Lee W., Clemens J., Bondy C. Insulin-like growth factors in the response to cerebral ischemia. Mol. Cell. Neurosci. 1992, 3:36-43.
6. Bondy C.A., Cheng C.M. Signaling by insulin-like growth factor 1 in brain. Eur. J. Pharmacol. 2004, 490:25-31.
7. Knusel B., Michel P.P., Schwaber J.S., Hefti F. Selective and nonselective stimulation of central cholinergic and dopaminergic development in vitro by nerve growth factor, basic fibroblast growth factor, epidermal growth factor, insulin and the insulin-like growth factors I and II. J. Neurosci. 1990, 10:558-570.
8. Svrzic D., Schubert D. Insulin-like growth factor 1 supports embryonic nerve cell survival. Biochem. Biophys. Res. Commun. 1990, 172:54-60.
9. Hughes R.A., Sendtner M., Thoenen H. Members of several gene families influence survival of rat motoneurons in vitro and in vivo. J. Neurosci. Res. 1993, 36:663-671.
10. Neff N.T., Prevette D., Houenou L.J., et al. Insulin-like growth factors: putative muscle-derived trophic agents that promote motoneuron survival. J. Neurobiol. 1993, 24:1578-1588.
11. Åberg N.D., Brywe K.G., Isgaard J. Aspects of growth hormone and insulin-like growth factor-I related to neuroprotection, regeneration, and functional plasticity in the adult brain. Sci. World J. 2006, 6:53-80.
12. D'Ercole A.J., Ye P. Expanding the mind: insulin-like growth factor I and brain development. Endocrinology 2008, 149:5958-5962.
13. Aleman A., Torres-Alemán I. Circulating insulin-like growth factor I and cognitive function: neuromodulation throughout the lifespan. Prog. Neurobiol. 2009, 89:256-265.
14. Jones J.I., Clemmons D.R. Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 1995, 16:3-34.
15. Seto D., Zheng W.H., McNicoll A., Collier B., Quirion R., Kar S. Insulin-like growth factor-I inhibits endogenous acetylcholine release from the rat hippocampal formation: possible involvement of GABA in mediating the effects. Neuroscience 2002, 115:603-612.
16. Arsenijevic Y., Weiss S. Insulin-like growth factor-I is a differentiation factor for postmitotic CNS stem cell-derived neuronal precursors: distinct actions from those of brain-derived neurotrophic factor. J. Neurosci. 1998, 18:2118-2128.
17. Åberg M.A., Åberg N.D., Hedbäcker H., Oscarsson J., Eriksson P.S. Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J. Neurosci. 2000, 20:2896-2903.
18. O'Kusky J.R., Ye P., D'Ercole A.J. Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development. J. Neurosci. 2000, 20:8435-8442.
19. Arsenijevic Y., Weiss S., Schneider B., Aebischer P. Insulin-like growth factor-I is necessary for neural stem cell proliferation and demonstrates distinct actions of epidermal growth factor and fibroblast growth factor-2. J. Neurosci. 2001, 21:7194-7202.
20. Cheng C.M., Cohen M., Tseng V., Bondy C.A. Endogenous IGF1 enhances cell survival in the postnatal dentate gyrus. J. Neurosci. Res. 2001, 64:341-347.
21. Niblock M.M., Brunso-Bechtold J.K., Riddle D.R. Insulin-like growth factor I stimulates dendritic growth in primary somatosensory cortex. J. Neurosci. 2000, 20:4165-4176.
22. Cheng C.M., Mervis R.F., Niu S.L., et al. Insulin-like growth factor 1 is essential for normal dendritic growth. J. Neurosci. Res. 2003, 73:1-9.
23. O'Kusky J.R., Ye P., D'Ercole A.J. Increased expression of insulin-like growth factor I augments the progressive phase of synaptogenesis without preventing synapse elimination in the hypoglossal nucleus. J. Comp. Neurol. 2003, 464:382-391.
24. Gillespie C.M., Merkel A.L., Martin A.A. Effects of insulin-like growth factor-I and LR3IGF-I on regional blood flow in normal rats. J. Endocrinol. 1997, 155:351-358.
25. Zeger M., Popken G., Zhang J., et al. Insulin-like growth factor type 1 receptor signaling in the cells of oligodendrocyte lineage is required for normal in vivo oligodendrocyte development and myelination. Glia 2007, 55:400-411.
26. Taguchi A., White M.F. Insulin-like signaling, nutrient homeostasis, and life span. Annu. Rev. Physiol. 2008, 70:191-212.
27. Frölich L., Blum-Degen D., Bernstein H.G., Engelsberger S., Humrich J., Laufer S., et al. Brain insulin and insulin receptors in aging and sporadic Alzheimer's disease. J. Neural Transm. 1998, 105:423-438.
28. Hoyer S., Muller D., Plaschke K. Desensitization of brain insulin receptor. Effect on glucose/energy and related metabolism. J. Neural Transm. Suppl. 1994, 44:259-268.
29. Schubert M., Gautam D., Surjo D., et al. Role for neuronal insulin resistance in neurodegenerative diseases. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3100-3105.
30. Steen E., Terry B.M., Rivera E.J., et al. Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease-is this type 3 diabetes?. J. Alzheimers Dis. 2005, 7:63-80.
31. Tong M., Dong M., de la Monte S.M. Brain insulin-like growth factor and neurotrophin resistance in Parkinson's disease and dementia with Lewy bodies: potential role of manganese neurotoxicity. J. Alzheimers Dis. 2009, 16:585-599.
32. Gasparini L., Netzer W.J., Greengard P., Xu H. Does insulin dysfunction play a role in Alzheimer's disease?. Trends Pharmacol. Sci. 2002, 23:288-293.
33. Hoyer S. Glucose metabolism and insulin receptor signal transduction in Alzheimer disease. Eur. J. Pharmacol. 2004, 490:115-125.
34. Craft S. Insulin resistance and Alzheimer's disease pathogenesis: potential mechanisms and implications for treatment. Curr. Alzheimer Res. 2007, 4:147-152.
35. de la Monte S.M. Insulin resistance and Alzheimer's disease. BMB Rep. 2009, 42:475-481.
36. Cusi K., DeFronzo R. Recombinant human insulin like growth factor I treatment for one week improves metabolic control in type 2 diabetes by ameliorating hepatic and muscle insulin resistance. J. Clin. Endocrinol. Metab. 2000, 85:3077-3084.
37. Torres-Aleman I. Targeting insulin-like growth factor-1 to treat Alzheimer's disease. Expert Opin. Ther. Targets 2007, 11:1535-1542.
38. Vaccarello M.A., Diamond F.B., Guevara-Aguirre J., et al. Hormonal and metabolic effects and pharmacokinetics of recombinant insulin-like growth factor-I in growth hormone receptor deficiency/Laron syndrome. J. Clin. Endocrinol. Metab. 1993, 77:273-280.
39. Cheetham T.D., Connors M., Clayton K., Watts A., Dunger D.B. The relationship between overnight GH levels and insulin concentrations in adolescents with insulin-dependent diabetes mellitus (IDDM) and the impact of recombinant human insulin-like growth factor I (IGF-I). Clin. Endocrinol. 1997, 46:415-424.
40. Ozmen L., Albientz A., Czech C., Jacobsen H. Expression of transgenic APP mRNA is the key determinant for beta-amyloid deposition in PS2APP transgenic mice. Neurodegener. Dis. 2009, 6:29-36.
41. El Mouedden M., Haseldonckx M., Mackie C., Meert T., Mercken M. Method for the determination of the levels of beta-amyloid peptide in the CSF sampled from freely moving rats. J. Pharmacol. Toxicol. Meth. 2005, 52:229-233.
42. Czirr E., Cottrell B.A., Leuchtenberger S., et al. Independent generation of Abeta42 and Abeta38 peptide species by gamma-secretase. J. Biol. Chem. 2008, 283:17049-17054.
43. Ozmen L., Woolley M., Albientz A., et al. BACE/APPV717F Double-transgenic mice develop cerebral amyloidosis and inflammation. Neurodegener. Dis. 2005, 2:284-298.
44. Olsson A., Csajbok L., Ost M., et al. Marked increase of beta-amyloid(1-42) and amyloid precursor protein in ventricular cerebrospinal fluid after severe traumatic brain injury. J. Neurol. 2004, 251:870-876.
45. Carro E., Trejo J.L., Gomez-Isla T., LeRoith D., Torres-Aleman I. Serum insulin-like growth factor I regulates brain amyloid-beta levels. Nat. Med. 2002, 8:1390-1397.
46. Carro E., Trejo J.L., Gerber A., et al. Therapeutic actions of insulin-like growth factor I on APP/PS2 mice with severe brain amyloidosis. Neurobiol. Aging 2006, 27:1250-1257.
47. Poirier R., Veltman I., Pflimlin M.C., Knoflach F., Metzger F. Enhanced dentate gyrus synaptic plasticity but reduced neurogenesis in a mouse model of amyloidosis. Neurobiol. Dis. 2010, 40:386-393.
48. Dulawa S.C., Hen R. Recent advances in animal models of chronic antidepressant effects: the novelty-induced hypophagia test. Neurosci. Biobehav. Rev. 2005, 29:771-783.
49. Duman C.H., Schlesinger L., Terwilliger R., Russell D.S., Newton S.S., Duman R.S. Peripheral insulin-like growth factor-I produces antidepressant-like behavior and contributes to the effect of exercise. Behav. Brain Res. 2009, 198:366-371.
50. Krishnan V., Nestler E.J. The molecular neurobiology of depression. Nature 2008, 455:894-902.
51. Lopez-Lopez C., LeRoith D., Torres-Aleman I. Insulin-like growth factor I is required for vessel remodeling in the adult brain. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9833-9838.
52. Ho L., Qin W., Pompl P.N., et al. Diet-induced insulin resistance promotes amyloidosis in a transgenic mouse model of Alzheimer's disease. FASEB J. 2004, 18:902-904.
53. Freude S., Schilbach K., Schubert M. The role of IGF-1 receptor and insulin receptor signaling for the pathogenesis of Alzheimer's disease: from model organisms to human disease. Curr. Alzheimer Res. 2009, 6:213-223.
54. Luchsinger J.A. Insulin resistance, type 2 diabetes, and AD: cerebrovascular disease or neurodegeneration?. Neurology 2010, 75:758-759.
55. Matsuzaki T., Sasaki K., Tanizaki Y., Hata J., Fujimi K., Matsui Y., et al. Insulin resistance is associated with the pathology of Alzheimer disease: the Hisayama study. Neurology 2010, 75:764-770.
56. Moloney A.M., Griffin R.J., Timmons S., O'Connor R., Ravid R., O'Neill C. Defects in IGF-1 receptor, insulin receptor and IRS-1/2 in Alzheimer's disease indicate possible resistance to IGF-1 and insulin signalling. Neurobiol. Aging 2010, 31:224-243.
57. Pessin J.E., Saltiel A.R. Signaling pathways in insulin action: molecular targets of insulin resistance. J. Clin. Investig. 2000, 106:165-169.
58. Shulman G.I. Cellular mechanisms of insulin resistance. J. Clin. Investig. 2000, 106:171-176.
59. Pulford B.E., Ishii D.N. Uptake of circulating insulin-like growth factors (IGFs) into cerebrospinal fluid appears to be independent of the IGF receptors as well as IGF-binding proteins. Endocrinology 2001, 142:213-220.
60. Yu Y., Kastin A.J., Pan W. Reciprocal interactions of insulin and insulin-like growth factor I in receptor-mediated transport across the blood-brain barrier. Endocrinology 2006, 147:2611-2615.
61. Chauhan N.B., Siegel G.J. Reversal of amyloid beta toxicity in Alzheimer's disease model Tg2576 by intraventricular antiamyloid beta antibody. J. Neurosci. Res. 2003, 69:10-23.
62. Chauhan N.B., Lichtor T., Siegel G.J. Aging potentiates Abeta-induced depletion of SNAP-25 in mouse hippocampus. Brain Res. 2003, 982:219-227.
63. Trejo J.L., Piriz J., Llorens-Martin M.V., Torres-Aleman I. The effects of exercise on spatial learning and anxiety-like behavior are mediated by an IGF-I-dependent mechanism related to hippocampal neurogenesis. Mol. Cell. Neurosci. 2008, 37:402-411.
64. Kobayashi D.T., Chen K.S. Behavioral phenotypes of amyloid-based genetically modified mouse models of Alzheimer's disease. Genes Brain Behav. 2005, 4:173-196.
65. Eriksen J.L., Janus C.G. Plaques, tangles, and memory loss in mouse models of neurodegeneration. Behav. Genet. 2007, 37:79-100.
66. Kokjohn T.A., Roher A.E. Amyloid precursor protein transgenic mouse models and Alzheimer's disease: understanding the paradigms, limitations, and contributions. Alzheimers Dement. 2009, 5:340-347.
67. Epis R., Gardoni F., Marcello E., Genazzani A., Canonico P.L., Di Luca M. Searching for new animal models of Alzheimer's disease. Eur. J. Pharmacol. 2010, 626:57-63.
68. Castro-Alamancos M.A., Torres-Aleman I. Learning of the conditioned eye-blink response is impaired by an antisense insulin-like growth factor I oligonucleotide. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:10203-10207.
69. Markowska A.L., Mooney M., Sonntag W.E. Insulin-like growth factor-1 ameliorates age-related behavioral deficits. Neuroscience 1998, 87:559-569.
70. Lupien S.B., Bluhm E.J., Ishii D.N. Systemic insulin-like growth factor-I administration prevents cognitive impairment in diabetic rats, and brain IGF regulates learning/memory in normal adult rats. J. Neurosci. Res. 2003, 74:512-523.
71. Rollero A., Murialdo G., Fonzi S., et al. Relationship between cognitive function, growth hormone and insulin-like growth factor I plasma levels in aged subjects. Neuropsychobiology 1998, 38:73-79.
72. Aleman A., Verhaar H.J., De Haan E.H., et al. Insulin-like growth factor-I and cognitive function in healthy older men. J. Clin. Endocrinol. Metab. 1999, 84:471-475.
73. Kalmijn S., Janssen J.A., Pols H.A., Lamberts S.W., Breteler M.M. A prospective study on circulating insulin-like growth factor I (IGFI), IGF-binding proteins, and cognitive function in the elderly. J. Clin. Endocrinol. Metab. 2000, 85:4551-4555.
74. Dik M.G., Pluijm S.M., Jonker C., Deeg D.J., Lomecky M.Z., Lips P. Insulin-like growth factor I (IGF-I) and cognitive decline in older persons. Neurobiol. Aging 2003, 24:573-581.
75. Arwert L.I., Deijen J.B., Drent M.L. The relation between insulin-like growth factor I levels and cognition in healthy elderly: a metaanalysis. Growth Horm. IGF Res. 2005, 15:416-422.
76. Okereke O., Kang J.H., Ma J., Hankinson S.E., Pollak M.N., Grodstein F. Plasma IGF-I levels and cognitive performance in older women. Neurobiol. Aging 2007, 28:135-142.
77. Trejo J.L., Piriz J., Llorens-Martin M.V., et al. Central actions of liver-derived insulin-like growth factor I underlying its pro-cognitive effects. Mol. Psychiatry 2007, 12:1118-1128.
78. Geschwind D.H., Levitt P. Autism spectrum disorders: developmental disconnection syndromes. Curr. Opin. Neurobiol. 2007, 17:103-111.
79. Betancur C., Sakurai T., Buxbaum J.D. The emerging role of synaptic cell-adhesion pathways in the pathogenesis of autism spectrum disorders. Trends Neurosci. 2009, 32:402-412.
80. Toro R., Konyukh M., Delorme R., et al. Key role for gene dosage and synaptic homeostasis in autism spectrum disorders. Trends Genet. 2010, 26:363-372.
81. Greer J.M., Wynshaw-Boris A. Pten and the brain: sizing up social interaction. Neuron 2006, 50:343-345.
82. Kwon C.H., Luikart B.W., Powell C.M., et al. Pten regulates neuronal arborization and social interaction in mice. Neuron 2006, 50:377-388.
83. Bourgeron T. A synaptic trek to autism. Curr. Opin. Neurobiol. 2009, 19:231-234.
84. Tropea D., Giacometti E., Wilson N.R., et al. Partial reversal of Rett Syndrome-like symptoms in MeCP2 mutant mice. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2029-2034.
85. Schaevitz L.R., Moriuchi J.M., Nag N., Mellot T.J., Berger-Sweeney J. Cognitive and social functions and growth factors in a mouse model of Rett syndrome. Physiol. Behav. 2010, 100:255-263.
86. Marchetto M.C.N., Carromeu C., Acab A., et al. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 2010, 143:527-539.