Adult-onset deficiency in growth hormone and insulin-like growth factor-I decreases survival of dentate granule neurons: Insights into the regulation of adult hippocampal neurogenesis

Journal of Neuroscience Research

Volumn 83, Issue 2, 2006, Pages 199-210

  Lichtenwalner, Robin J ^a,b   Forbes, M Elizabeth ^a   Sonntag, William E ^a   Riddle, David R ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Dentate gyrus; Growth hormone; Insulin like growth factor I; Neurogenesis; Proliferation

Indexed keywords

BROXURIDINE; CELL MARKER; GROWTH HORMONE; PROTEIN NEUN; PROTEIN TUC4; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CULTURE MEDIUM; DENTATE GYRUS; EVALUATION; FEMALE; GRANULE CELL; GROWTH HORMONE DEFICIENCY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INSULIN LIKE GROWTH FACTOR I DEFICIENCY; MALE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RAT STRAIN;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; BROMODEOXYURIDINE; CELL COUNT; CELL PROLIFERATION; CELL SURVIVAL; DENTATE GYRUS; DWARFISM; FEMALE; GROWTH HORMONE; IMMUNOHISTOCHEMISTRY; INSULIN-LIKE GROWTH FACTOR I; MALE; NERVE TISSUE PROTEINS; NEURONS; ORGANOGENESIS; PHOSPHOPYRUVATE HYDRATASE; RATS; RATS, MUTANT STRAINS;

EID: 31844450693     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.20719     Document Type: Article

References (78)

1. Åberg MAI, Åberg ND, Hedbacker H, Oscarsson J, Eriksson PS. 2000. Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 20:2896-2903.
2. Åberg MAI, Åberg ND, Palmer TD, Alborn AM, Carlsson-Skwirut C, Bang P, Rosengren LE, Olsson T, Gage FH, Eriksson PS. 2003. IGF-I has a direct proliferative effect in adult hippocampal progenitor cells. Mol Cell Neurosci 24:23-40.
3. Altman J, Das GD. 1965. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
4. Anderson MF, Åberg MAI, Nilsson M, Eriksson PS. 2002. Insulin-like growth factor-I and neurogenesis in the adult mammalian brain. Brain Res Dev Brain Res 134:115-122.
5. Anlar B, Sullivan KA, Feldman EL. 1999. Insulin-like growth factor-I and central nervous system development. Horm Metab Res 31:120-125.
6. Armstrong CS, Wuarin L, Ishii DN. 2000. Uptake of circulating insulin-like growth factor-I into the cerebrospinal fluid of normal and diabetic rats and normalization of IGF-II mRNA content in diabetic rat brain. J Neurosci Res 59:649-660.
7. Baker J, Liu JP, Robertson EJ, Efstratiadis A. 1993. Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75:73-82.
8. Barnes CA. 1979. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol 93:74-104.
9. Beck KD, Powell-Braxton L, Widmer HR, Valverde J, Hefti F. 1995. Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 14:717-730.
10. Bohannon NJ, Corp ES, Wilcox BJ, Figlewicz DP, Dorsa DM, Baskin DG. 1988. Localization of binding sites for insulin-like growth factor-I (IGF-I) in the rat brain by quantitative autoradiography. Brain Res 444:205-213.
11. Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, Bick-Sander A, von der Behrens W, Kempermann G. 2003. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci 24:603-613.
12. Breese CR, Ingram RL, Sonntag WE. 1991. Influence of age and long-term dietary restriction on plasma insulin-like growth factor-1 (IGF-1), IGF-1 gene expression, and IGF-1 binding proteins. J Gerontol 46: B180-B187.
13. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. 2003. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
14. Butler AA, LeRoith D. 2001. Control of growth by the somatropic axis: growth hormone and the insulin-like growth factors have related and independent roles. Ann Rev Physiol 63:141-164.
15. Cameron HA, McKay RD. 2001. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406-417.
16. Cameron HA, Woolley CS, McEwen BS, Gould E. 1993. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337-344.
17. Carro E, Trejo JL, Nunez A, Torres-Aleman I. 2003. Brain repair and neuroprotection by serum insulin-like growth factor I. Mol Neurobiol 27:153-162.
18. Carter CS, Ramsey MM, Ingram RL, Cashion AB, Cefalu WT, Wang ZQ, Sonntag WE. 2002. Models of growth hormone and IGF-1 deficiency: applications to studies of aging processes and life-span determination. J Gerontol A Biol Sci Med Sci 57:B177-B188.
19. Charlton HM, Clark RG, Robinson IC, Goff AE, Cox BS, Bugnon C, Bloch BA. 1988. Growth hormone-deficient dwarfism in the rat: a new mutation. J Endocrinol 119:51-58.
20. Cheng CM, Cohen M, Tseng V, Bondy CA. 2001. Endogenous IGF1 enhances cell survival in the postnatal dentate gyrus. J Neurosci Res 64:341-347.
21. Cheng TC, Beamer WG, Phillips JA, Bartke A, Mallonee RL, Dowling C. 1983. Etiology of growth hormone deficiency in little, Ames, and Snell dwarf mice. Endocrinology 113:1669-1678.
22. Churchill JD, Galvez R, Colcombe S, Swain RA, Kramer AF, Greenough WT. 2002. Exercise, experience and the aging brain. Neurobiol Aging 23:941-955.
23. Coculescu M. 1999. Blood-brain barrier for human growth hormone and insulin-like growth factor-I. J Pediatr Endocrinol Metab 12:113-124.
24. Daughaday WH, Parker KA, Borowsky S, Trivedi B, Kapadia M. 1982. Measurement of somatomedin-related peptides in fetal, neonatal, and maternal rat serum by insulin-like growth factor (IGF) I radioimmunoassay, IGF-II radioreceptor assay (RRA), and multiplication-stimulating activity RRA after acid-ethanol extraction. Endocrinology 110:575-581.
25. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA. 2003. Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563-572.
26. Edén S. 1979. Age- and sex-related differences in episodic growth hormone secretion in the rat. Endocrinology 105:555-560.
27. Gabriel SM, Roncancio JR, Ruiz NS. 1992. Growth hormone pulsatility and the endocrine milieu during sexual maturation in male and female rats. Neuroendocrinology 56:619-625.
28. Gould E, Tanapat P. 1997. Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience 80:427-436.
29. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS. 1992. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 12:3642-3650.
30. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
31. Guan J, Bennet L, Gluckman PD, Gunn AJ. 2003. Insulin-like growth factor-1 and post ischemic brain injury. Prog Neurobiol 70:443-462.
32. Guan X-M, Yu H, Palyha OC, McKee KK, Feighner SD, Sirinathsinghji DJS, Smith RG, Van der Ploeg LHT, Howard AD. 1997. Distribution of mRNA encoding the growth hormone secretagogue receptor in brain and peripheral tissues. Brain Res Mol Brain Res 48:23-29.
33. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Møller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sørensen FB, Versterby A, West MJ. 1988. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. Acta Pathol Microbiol Immunol Scand 96:857-881.
34. Kempermann G. 2002. Why new neurons? Possible functions for adult hippocampal neurogenesis. J Neurosci 22:635-638.
35. Kempermann G, Kuhn HG, Gage FH. 1997. More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
36. Kempermann G, Kuhn HG, Gage FH. 1998. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18:3206-3212.
37. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH. 2003. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391-399.
38. Kronenberg G, Reuter K, Steiner B, Brandt MD, Jessberger S, Yamaguchi M, Kempermann G. 2003. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J Comp Neurol 467:455-463.
39. Kuhn HG, Dickinson-Anson H, Gage FH. 1996. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
40. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH. 1997. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 17:5820-5829.
41. LeRoith D, Bondy C, Yakar S, Liu JL, Butler A. 2001. The somatomedin hypothesis: 2001. Endocr Rev 22:53-74.
42. Lesniak MA, Hill JM, Kiess W, Rojeski M, Pert CB, Roth J. 1988. Receptors for insulin-like growth factors I and II: autoradiographic localization in rat brain and comparison to receptors for insulin. Endocrinology 123:2089-2099.
43. Lichtenwalner RJ, Forbes ME, Bennett SA, Lynch CD, Sonntag WE, Riddle DR. 2001. Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience 107:603-613.
44. Liu J, Solway K, Messing RO, Sharp FR. 1998. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 18:7768-7778.
45. Liu JL, Yakar S, LeRoith D. 2000. Conditional knockout of mouse insulin-like growth factor-1 gene using the Cre/loxP system. Proc Soc Exp Biol Med 223:344-351.
46. Lobie PE, Garcia-Aragon J, Lincoln DT, Barnard R, Wilcox JN, Waters MJ. 1993. Localization and ontogeny of growth hormone receptor gene expression in the central nervous system. Brain Res Dev Brain Res 74:225-233.
47. Lupien SB, Bluhm EJ, Ishii DN. 2003. 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 74:512-523.
48. Madsen TM, Kristjansen PE, Bolwig TG, Wortwein G. 2003. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119:635-642.
49. Markowska AL, Mooney M, Sonntag WE. 1998. Insulin-like growth factor-1 ameliorates age-related behavioral deficits. Neuroscience 87:559-569.
50. Mizumatsu S, Monje ML, Morhardt DR, Rola R, Palmer TD, Fike JR. 2003. Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res 63:4021-4027.
51. Monje ML, Palmer T. 2003. Radiation injury and neurogenesis. Curr Opin Neurol 16:129-134.
52. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
53. Nyberg F, Burman P. 1996. Growth hormone and its receptors in the central nervous system-location and functional significance. Horm Res 45:18-22.
54. O'Kusky JR, Ye P, D'Ercole AJ. 2000. Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyms during postnatal development. J Neurosci 20:8435-8442.
55. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH. 1997. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727-3738.
56. Perez-Martin M, Azcoitia I, Trejo JL, Sierra A, Garcia-Segura LM. 2003. An antagonist of estrogen receptors blocks the induction of adult neurogenesis by insulin-like growth factor-I in the dentate gyrus of adult female rat. Eur J Neurosci 18:923-930.
57. Quinn CC, Gray GE, Hockfield S. 1999. A family of proteins implicated in axon guidance and outgrowth. J Neurobiol 41:158-164.
58. Ramsey MM, Weiner JL, Moore TP, Carter CS, Sonntag WE. 2004. Growth hormone treatment attenuates age-related changes in hippocampal short-term plasticity and spatial learning. Neuroscience 129:119-127.
59. Rao MS, Hattiangady B, Abdel-Rahman A, Stanley DP, Shetty AK. 2005. Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur J Neurosci 21:464-476.
60. Rotwein P, Burgess SK, Milbrandt JD, Krause JE. 1988. Differential expression of insulin-like growth factor genes in rat central nervous system. Proc Natl Acad Sci USA 85:265-269.
61. Rubin R, Baserga R. 1995. Insulin-like growth factor-I receptor: its role in cell proliferation, apoptosis, and tumorigenicity. Lab Invest 73:311-331.
62. Schoenle E, Zapf J, Humbel RE, Froesch ER. 1982. Insulin-like growth factor I stimulates growth in hypophysectomized rats. Nature 296:252-253.
63. Seki T, Arai Y. 1995. Age-related production of new granule cells in the adult dentate gyrus. Neuroreport 6:2479-2482.
64. Shetty AK, Hattiangady B, Shetty GA. 2005. Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: role of astrocytes. Glia 51:173-186.
65. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C, Cross JC, Weiss S. 2003. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299:117-120.
66. Shors TJ. 2004. Memory traces of trace memories: neurogenesis, synaptogenesis and awareness. Trends Neurosci 27:250-256.
67. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. 2001. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376.
68. Sonntag WE, Lenham JE, Ingram RL. 1992. Effects of aging and dietary restriction on tissue protein synthesis: relationship to plasma insulin-like growth factor-1. J Gerontol 47:B159-B163.
69. Sonntag WE, Lynch CD, Bennett SA, Khan AS, Thornton PL, Cooney PT, Ingram RL, McShane T, Brunso-Bechtold JK. 1999. Alterations in insulin-like growth factor-1 gene and protein expression and type 1 insulin-like growth factor receptors in the brains of ageing rats. Neuroscience 88:269-279.
70. Sonntag WE, Carter CS, Ikeno Y, Ekenstedt K, Carlson CS, Loeser RF, Chakrabarty S, Lee S, Bennett C, Ingram R, Moore T, Ramsey M. 2005. Adult-onset growth hormone and insulin-like growth factor I deficiency reduces neoplastic disease, modifies age-related pathology, and increases life span. Endocrinology 146:2920-2932.
71. Sun LY, Al-Regaiey K, Masternak MM, Wang J, Bartke A. 2005. Local expression of GH and IGF-1 in the hippocampus of GH-deficient long-lived mice. Neurobiol Aging 26:929-937.
72. Sytze Van Dam P, Aleman A. 2004. Insulin-like growth factor-I, cognition and brain aging. Eur J Pharmacol 490:87-95.
73. Tada E, Parent JM, Lowenstein DH, Fike JR. 2000. X-irradiation causes a prolonged reduction in cell proliferation in the dentate gyrus of adult rats. Neuroscience 99:33-41.
74. Tanapat P, Hastings NB, Reeves AJ, Gould E. 1999. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19:5792-5801.
75. Thornton PL, Ingram RL, Sonntag WE. 2000. Chronic [D-Ala2]-growth hormone-releasing hormone administration attenuates age-related deficits in spatial memory. J Gerontol A Biol Sci Med Sci 55:B106-B112.
76. Trejo JL, Carro E, Torres-Aleman I. 2001. Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 21:1628-1634.
77. van Praag H, Kempermann G, Gage FH. 1999. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270.
78. Zhai Q, Lai Z, Roos P, Nyberg F. 1994. Characterization of growth hormone binding sites in rat brain. Acta Paediatr Suppl 406:92-95.