Insulin-like growth factor 1: At the crossroads of brain development and aging

Frontiers in Cellular Neuroscience

Volumn 11, Issue , 2017, Pages

  Wrigley, Sarah ^a   Arafa, Donia ^a   Tropea, Daniela ^b,c  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b ST JAMES S HOSPITAL   (Ireland)

^c TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Aging; Growth factors; Insulin like growth factor 1; Neurodevelopment

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; GROWTH FACTOR RECEPTOR; GROWTH HORMONE; INSULIN; INSULIN LIKE GROWTH FACTOR 1 RECEPTOR HOMOLOG DAF 2; INSULIN RECEPTOR SUBSTRATE 1; INSULIN RECEPTOR SUBSTRATE 2; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MESSENGER RNA; METHYL CPG BINDING PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN BINDING PROTEIN 5; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TRANSCRIPTION FACTOR DAF 16; UNCLASSIFIED DRUG;

AGING; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN MATURATION; BRAIN SIZE; CELL DEATH; CELL SURVIVAL; COGNITIVE DEFECT; DEGENERATIVE DISEASE; DEVELOPMENTAL DISORDER; DISEASE ASSOCIATION; GENE EXPRESSION; HUMAN; LIFESPAN; MYELINATION; NERVE CELL DIFFERENTIATION; NERVE CELL LESION; NERVE CELL PLASTICITY; NEURAL STEM CELL; NEURITE OUTGROWTH; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PATHOGENESIS; SIGNAL TRANSDUCTION;

EID: 85012040938     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2017.00014     Document Type: Article

References (121)

1. Aberg, M., Aberg, N., Hedbäcker, H., Oscarsson, J., and Eriksson, P. (2000). Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J. Neurosci. 20, 2896–2903.
2. Åberg, M. A. I., Åberg, N. D., Palmer, T. D., Allborn, A.-M., Carlsson-Skwirut, C., Bang, P., et al. (2003). IGF-1 has a direct proliferative effect in adult hippocampal progenitor cells. Mol. Cell. Neurosci. 24, 23–40. doi: 10.1016/s1044-7431(03)00082-4
3. Aleman, A., de Vries, W., Koppeschaar, H., Osman-Dualeh, A., Verhaar, H., Samson, M., et al. (2001). Relationship between circulating levels of sex hormones and insulin-like growth factor-1 and fluid intelligence in older men. Exp. Aging Res. 27, 283–291. doi: 10.1080/036107301300208718
4. Aleman, A., Verhaar, H., De Haan, E., De Vries, W., Samson, M., Drent, M., et al. (1999). Insulin-like growth factor-1 and cognitive function in healthy older men. J. Clin. Endocrinol. Metab. 84, 471–475. doi: 10.1210/jc.84.2.471
5. Anderson, M., Åberg, M., Nilson, M., and Erikkson, P. (2002). Insulin-like growth factor-1 and neurogenesis in the adult mammalian brain. Brain Res. 134, 115–122. doi: 10.1016/s0165-3806(02)00277-8
6. Apfeld, J., and Kenyon, C. (1999). Regulation of lifespan by sensory perception in Caenorhabditis elegans. Nature 402, 804–809. doi: 10.1038/45544
7. Bach, M., Shen-Orr, Z., Lowe, W., Roberts, C., and Leroith, D. (1991). Insulin-like growth factor 1 mRNA levels are developmentally regulated in specific regions of the rat brain. Mol. Brain Res. 10, 43–48. doi: 10.1016/0169-328x(91)90054-2
8. Barres, B., Hart, I., Coles, H., Burne, J., Voyvodic, J., Richardson, W., et al. (1992). Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70, 31–46. doi: 10.1016/0092-8674(92)90531-g
9. Bartlett, W. P., Li, X.-S., Williams, M., and Benkovic, S. (1991). Localisation of insulin-like growth factor-1 mRNA in murine central nervous system during post-natal development. Dev. Biol. 147, 239–250. doi: 10.1016/s0012-1606(05)80021-1
10. Beck, K. D., Powel-Braxton, L., Widmer, H., Valverde, J., and Hefti, F. (1995). IGF1 disruption results in reduced brain size, CNS hypomelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 14, 717–730. doi: 10.1016/0896-6273(95)90216-3
11. Bondy, C., Bach, M., and Lee, W.-H. (1992a). Mapping of brain insulin and insulin-like growth factor receptor gene expression by in situ hybridization. Neuroprotocols 1, 240–259. doi: 10.1016/1058-6741(92)90034-u
12. Bondy, C., Werner, H., Roberts, C. T., and LeRoith, D. (1992b). Cellular pattern of type-I insulin-like growth factor receptor gene expression during maturation of the rat brain: comparison with insulin-like growth factors I and II. Neuroscience 46, 909–923. doi: 10.1016/0306-4522(92)90193-6
13. Bondy, C. A., and Cheng, C. M. (2004). Signalling by insulin-like growth factor 1 in brain. Eur. J. Pharmacol. 490, 25–31. doi: 10.1016/j.ejphar.2004.02.042
14. Bozdagi, O., Tavassoli, T., and Buxbaum, J. (2013). Insulin-like growth factor-1 rescues synaptic and motor deficits in a mouse model of autism and developmental delay. Mol. Autism 4:9. doi: 10.1186/2040-2392-4-9
15. Brooker, G. J. F., Kalloniatis, M., Russo, V. C., Murphy, M., Werther, G. A., and Bartlett, P. F. (2000). Endogenous IGF-1 regulates the neuronal differentiation of adult stem cells. J. Neurosci. Res. 59, 332–341. doi: 10.1002/(sici)1097-4547(20000201)59:3<332::aid-jnr6>3.0.co;2-2
16. Brown-Borg, H., and Bartke, A. (2012). GH and IGF1: roles in energy metabolism of long-living GH mutant mice.J. Gerontol. A Biol. Sci. Med. Sci. 67A, 652–660. doi: 10.1093/gerona/gls086
17. Byrne, A. B., Walradt, T., Gardner, K. E., Hubbert, A., Reinke, V., and Hammarlund, M. (2014). Insulin/IGF1 signaling inhibits age-dependent axon regeneration. Neuron 81, 561–573. doi: 10.1016/j.neuron.2013.11.019
18. Cancedda, L., Putignano, E., Sale, A., Viegi, A., Berardi, N., and Maffei, L. (2004). Acceleration of visual system development by environmental enrichment. J. Neurosci. 24, 4840–4848. doi: 10.1523/JNEUROSCI.0845-04.2004
19. Carlson, S. W., Madathil, S. K., Sama, D. M., Gao, X., Chen, J., and Saatman, K. E. (2014). Conditional overexpression of insulin-like growth factor-1 enhances hippocampal neurogenesis and restores immature neuron dendritic processes after traumatic brain injury. J. Neuropathol. Exp. Neurol. 73, 734–746. doi: 10.1097/NEN.0000000000000092
20. Carro, E., Trejo, J., Busiguina, S., and Torres-Aleman, I. (2001). Circulating insulin-like growth factor I mediates the protective effects of physical exercise against brain insults of different aetiology and anatomy. J. Neurosci. 21, 5678–5684.
21. Carro, E., Trejo, J. L., Gomez-Isla, T., LeRoith, D., and Torres-Aleman, I. (2002). Serum insulin-like growth factor I regulates brain amyloid-ß levels. Nat. Med. 8, 1390–1397. doi: 10.1038/nm793
22. Carro, E., Trejo, J. L., Spuch, C., Bohl, D., Heard, J. M., and Torres-Aleman, I. (2006). Blockade of the insulin-like growth factor I receptor in the choroid plexus originates Alzheimer’s-like neuropathology in rodents: new cues into the human disease? Neurobiol. Aging 27, 1618–1631. doi: 10.1016/j.neurobiolaging.2005.09.039
23. Carson, M. J., Behringer, R. R., Brinster, R. L., and McMorris, F. (1993). Insulin-like growth factor-1 increases brain growth and central nervous system myelination in tTransgenic mice. Neuron 10, 729–740. doi: 10.1016/0896-6273(93)90173-o
24. Castro, J., Garcia, R. I., Kwok, S., Banerjee, A., Petravicz, J., Woodson, J., et al. (2014). Functional recovery with recombinant human IGF1 treatment in a mouse model of Rett syndrome. Proc. Natl. Acad. Sci. U S A 111, 9941–9946. doi: 10.1073/pnas.1311685111
25. Chen, M. J., and Russo-Neustadt, A. A. (2007). Running exercise- and antidepressant-induced increases in growth and survival-associated signaling molecules are IGF-dependent. Growth Factors 25, 118–131. doi: 10.1080/08977190701602329
26. Cheng, C., Cohen, M., Tseng, V., and Bondy, C. (2001). Endogeneous IGF1 enhances cell survival in the post-natal dentate gyrus. J. Neurosci. Res. 64, 341–347. doi: 10.1002/jnr.1084
27. Cheng, C. M., Mervis, R. F., Niu, S. L., Salem, N., Witters, L. A., Tseng, V., et al. (2003). Insulin-like growth factor 1 is essential for normal dendritic growth. J. Neurosci. Res. 73, 1–9. doi: 10.1002/jnr.10634
28. Cheng, C. M., Reinhardt, R. R., Lee, W.-H., Joncas, G., Patel, S. C., and Bondy, C. A. (2000). Insulin-like growth factor 1 regulates developing brain glucose metabolism. Proc. Natl. Acad. Sci. U S A 97, 10236–10241. doi: 10.1073/pnas.170008497
29. Chrysis, D., Calikoglu, A., Ye, P., and D’Ercole, A. (2001). Insulin-like growth factor 1 overexpression attenuates cerebellar apoptosis by altering expression of Bcl family proteins in a developmentally specific manner. J. Neurosci. 21, 1481–1489.
30. Chung, Y. H., Shin, C. M., Joo, K. M., Kim, M., and Cha, C. I. (2002). Region-specific alterations in insulin-like growth factor receptor type 1 in the cerebral cortex and hippocampus of aged rats. Brain Res. 946, 307–313. doi: 10.1016/s0006-8993(02)03041-x
31. Ciucci, F., Putignano, E., Baroncelli, L., Landi, S., Berardi, N., and Maffei, L. (2007). Insulin-like growth factor-1 (IGF-1) mediates the effects of enriched environment (EE) on visual cortical development. PLoS One 2:e475. doi: 10.1371/journal.pone.0000475
32. Clancy, D. J., Gems, D., Harshman, L. G., Oldham, S., Stocker, H., Hafen, E., et al. (2001). Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292, 104–106. doi: 10.1126/science.1057991
33. Clayton, D., Mesches, M., Alvarez, E., Bickford, P., and Browning, M. (2002). A hippocampal NR2B deficit can mimic age-related changes in long-term potentiation and spatial learning in the Fsicher 344 rat. J. Neurosci. 22, 3628–3637.
34. Cohen, E., Paulsson, J. F., Blinder, P., Burstyn-Cohen, T., Du, D., Estepa, G., et al. (2009). Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell 139, 1157–1169. doi: 10.1016/j.cell.2009.11.014
35. D’Costa, A. P., Lenham, J. E., Ingram, R. L., and Sonntag, W. E. (1993). Moderate calorie restriction increases type 1 IGF receptors and protein synthesis in aging rats. Mech. Aging Dev. 71, 59–71. doi: 10.1016/0047-6374(93)90035-p
36. Dentremont, K. D., Ye, P., D’Ercole, A. J., and O’Kusky, J. R. (1999). Increased insulin-like growth factor-I (IGF-I) expression during early postnatal development differentially increases neuron number and growth in medullary nuclei of the mouse. Dev. Brain Res. 114, 135–141. doi: 10.1016/s0165-3806(99)00024-3
37. DiCicco-Bloom, E., and Black, I. B. (1988). Insulin growth factors regulate the mititic cycle in cultured rat sympathetic neuroblasts. Proc. Natl. Acad. Sci. U S A 85, 4066–4070. doi: 10.1073/pnas.85.11.4066
38. Ding, Q., Vaynman, S., Akhavan, M., Ying, Z., and Gomez-Pinilla, F. (2006). Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neuroscience 140, 823–833. doi: 10.1016/j.neuroscience.2006.02.084
39. Drago, J., Murohy, M., Carrol, S. M., Harvey, R. P., and Bartlett, P. F. (1990). Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor-1. Proc. Natl. Acad. Sci. U S A 88, 2199–2203. doi: 10.1073/pnas.88.6.2199
40. Dyer, A. H., Vahdatpour, C., Sanfeliu, A., and Tropea, D. (2016). The role of insulin-like growth factor 1 (IGF1-1) in brain development, maturation and plasticity. Neuroscience 325, 89–99. doi: 10.1016/j.neuroscience.2016.03.056
41. Fernandez, A. M., de la Vega, A. G., and Torres-Aleman, I. (1998). Insulin-like growth factor I restores motor coordination in a rat model of of cerebellar ataxia. Proc. Natl. Acad. Sci. U S A 95, 1253–1258. doi: 10.1073/pnas.95.3.1253
42. Fernandez, A. M., and Torres-Alemán, I. (2012). The many faces of insulin-like peptide signalling in the brain. Nat. Rev. Neurosci. 13, 225–239. doi: 10.1038/nrn3209
43. Flachsbart, F., Caliebe, A., Kleindorp, R., Blanché, H., von Eller-Eberstein, H., Nikolaus, S., et al. (2009). Association of FOXO3A variation with human longevity confirmed in German centenarians. Proc. Natl. Acad. Sci. U S A 106, 2700–2705. doi: 10.1073/pnas.0809594106
44. Forbes, B. E. (2016). Two years in IGF1 research. Growth Horm. IGF Res. 30–31, 70–74. doi: 10.1016/j.ghir.2016.09.006
45. Friedlander, A., Butterfield, G., Moynihan, S., Grillo, J., Pollack, M., Holloway, L., et al. (2001). One year of insulin-like growth factor 1 treatment does not affect bone density, body composition, or psychological measures in postmenopausal women. J. Clin. Endocrinol. Metab. 85, 1496–1503. doi: 10.1210/jc.86.4.1496
46. Gami, M. S., and Wolkow, C. A. (2006). Studies of Caenorhabditis elegans DAF-2/insulin signaling reveal targets for pharmacological manipulation of lifespan. Aging Cell 5, 31–37. doi: 10.1111/j.1474-9726.2006.00188.x
47. García-Segura, L. M., Pérez, J., Pons, S., Rejas, M., and Torres-Alemán, I. (1991). Localization of insulin-like growth factor I (IGF-I)-like immunoreactivity in the developing and adult rat brain. Brain Res. 560, 167–174. doi: 10.1016/0006-8993(91)91228-s
48. Gontier, G., George, C., Chaker, Z., Holzenberger, M., and Aïd, S. (2015). Blocking IGF signaling in adult neurons alleviates Alzheimer’s disease pathology through amyloid-ß clearance. J. Neurosci. 35, 11500–11513. doi: 10.1523/JNEUROSCI.0343-15.2015
49. Guan, J., Bennett, T. L., George, S., Waldvogel, H. J., Faull, R. L., Gluckman, P., et al. (2000). Selective neuroprotective effects with insulin-like growth factor 1 in phenotypic striatal neurons following ischemic brain injury in fetal sheep. Neuroscience 95, 831–839. doi: 10.1016/s0306-4522(99)00456-x
50. Guan, J., Miller, O. T., Waugh, K. M., McCarthy, D. C., and Gluckman, P. D. (2001). Insulin-like growth factor-1 improves somatosensory function and reduces the extent of cortical infarction and ongoing neuronal loss after hypoxia-ischaemia in rats. Neuroscience 105, 299–306. doi: 10.1016/s0306-4522(01)00145-2
51. Guarente, L., and Kenyon, C. (2000). Genetic pathways that regulate aging in model organisms. Nature 408, 255–262. doi: 10.1038/35041700
52. Guzzetta, A., Baldini, S., Bancale, A., Baroncelli, L., Ciucci, F., Ghirri, P., et al. (2009). Massage accelerates brain development and the maturation of visual function. J. Neurosci. 29, 6042–6051. doi: 10.1523/JNEUROSCI.5548-08.2009
53. van der Heide, L., Ramakers, G., and Smidt, M. (2006). Insulin signalling in the central nervous system: learning to survive. Prog. Neurobiol. 79, 205–221. doi: 10.1016/j.pneurobio.2006.06.003
54. Hodge, R. D., D’Ercole, A. J., and O’Kusky, J. R. (2004). Insulin-like growth factor-I accelerates the cell cycle by decreasing G1 phase length and increases cell cycle reentry in the embryonic cerebral cortex. J. Neurosci. 24, 10201–10210. doi: 10.1523/JNEUROSCI.3246-04.2004
55. Hodge, R. D., D’Ercole, A. J., and O’Kusky, J. R. (2007). Insulin-like growth factor-I (IGF-I) inhibits neuronal apoptosis in the developing cerebral cortex in vivo. Int. J. Dev. Neurosci. 25, 233–241. doi: 10.1016/j.ijdevneu.2007.03.004
56. Holzenberger, M., Dupont, J., Ducos, B., Leneuve, P., Géloën, A., Even, P. C., et al. (2003). IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421, 182–187. doi: 10.1038/nature01298
57. Hu, F., and Liu, F. (2014). Targeting tissue-specific metabolic signalling pathways in aging: the promise and limitations. Protein Cell 5, 21–35. doi: 10.1007/s13238-013-0002-3
58. Humbert, S., Bryson, E. A., Cordelières, F. P., Connors, N. C., Datta, S. R., Finkbeiner, S., et al. (2002). The IGF-1/Akt pathway is neuroprotective in Huntington’s disease and involves Huntingtin phosphorylation by Akt. Dev. Cell 2, 831–837. doi: 10.1016/s1534-5807(02)00188-0
59. Hurtado-Chong, A., Yusta-Boyo, M. J., Vergaño-Vera, E., Bulfone, A., de Pablo, F., and Vicario-Abejón, C. (2009). IGF-I promotes neuronal migration and positioning in the olfactory bulb and the exit of neuroblasts from the subventricular zone. Eur. J. Neurosci. 30, 742–755. doi: 10.1111/j.1460-9568.2009.06870.x
60. Johanson, A. J., and Blizzard, R. M. (1981). Low somatomedin-C levels in older men rise in response to growth hormone administration. John Hopkins Med. J. 149, 115–117.
61. Junnila, R. K., List, E. O., Berryman, D. E., Murrey, J. W., and Kopchick, J. J. (2013). The GH/IGF-1 axis in ageing and longevity. Nat. Rev. Endocrinol. 9, 366–376. doi: 10.1038/nrendo.2013.67
62. Kenyon, C. J. (2010). The genetics of ageing. Nature 464, 504–512. doi: 10.1038/nature08980
63. Kenyon, C., Chang, J., Gensch, E., Rudner, A., and Tabtiang, R. (1993). A C. elegans mutant that lives twice as long as wild type. Nature 366, 461–464. doi: 10.1038/366461a0
64. Killick, R., Scales, G., Leroy, K., Causevic, M., Hooper, C., Irvine, E. E., et al. (2009). Deletion of Irs2 reduces amyloid deposition and rescues behavioural deficits in APP transgenic mice. Biochem. Biophys. Res. Commun. 386, 257–262. doi: 10.1016/j.bbrc.2009.06.032
65. Landi, S., Ciucci, F., Maffei, L., Berardi, N., and Cenni, M. (2009). Setting the pace for retinal development: environmental enrichment acts thorugh insulin-like growth factor-1 and brain-derived neurotrophic factor. J. Neurosci. 29, 10809–10819. doi: 10.1523/JNEUROSCI.1857-09.2009
66. Laron, Z., Doron, M., and Amikan, B. (1969). Plasma growth hormone in men and women over 70 years of age. Med. Sports Phys. 4, 126–131. doi: 10.1159/000387283
67. Lichtenwalder, R. J., Forbes, M. E., Lynch, C. D., Sonntag, W. E., and Riddle, D. R. (2001). Intracerebroventricular infusion of insulin-like growth factor-1 ameliorates age-related decline in hippocampal neurogenesis. Neuroscience 107, 603–613. doi: 10.1016/s0306-4522(01)00378-5
68. Lin, K., Dorman, J. B., Rodan, A., and Kenyon, C. (1997). daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278, 1319–1322. doi: 10.1126/science.278.5341.1319
69. Liquitaya-Montiel, A., Aguilar-Arredondo, A., Arias, C., and Zepeda, A. (2012). Insulin growth factor-I promotes functional recovery after a focal lesion in the dentate gyrus. CNS Neurol. Disord. Drug Targets 11, 818–828. doi: 10.2174/1871527311201070818
70. Liu, J.-P., Baker, J., Perkins, J. A., Robertson, E. J., and Efstratiadis, A. (1993). Mice carrying null mutations of the genes encoding insulin-like growth factor, I (lgf-1) and type 1 IGF receptor (lgf1r). Cell 75, 59–72. doi: 10.1016/s0092-8674(05)80084-4
71. Liu, W., Ye, P., O’Kusky, J., and D’Ercole, A. (2009). Type 1 insulin-like growth factor receptor signalling is essential for the development of the hippocampal formation and dentate gyrus. J. Neurosci. Res. 87, 2821–2832. doi: 10.1002/jnr.22129
72. Lynch, C., Lyons, D., Khan, A., Bennett, S., and Sonntag, W. E. (2001). Insulin-like growth factor-1 increases glucose utilisation in brains of aged animals. Endocrinology 142, 506–509. doi: 10.1210/en.142.1.506
73. Maggio, M., De Vita, F., Lauretani, F., Buttò, V., Bondi, G., Cattabiani, C., et al. (2013). IGF1, the cross road of the nutritional, inflammatory and hormonal pathways to frailty. Nutrients 5, 4184–4205. doi: 10.3390/nu5104184
74. De Maghalaes Filho, C. D., Kappeler, L., Dupont, J., Solinc, J., Villapol, S., Denis, C., et al. (2016). Deleting IGF-1 receptor from forebrain neurons confers neuroprotection during stroke and upregulates endocrine somatotropin. J. Cereb. Blood Flow Metab. doi: 10.1177/0271678x15626718 [Epub ahead of print].
75. Markowska, A. L., Mooney, M., and Sonntag, W. E. (1998). Insulin-like growth factor-1 ameliorates age-related behavioral deficits. Neuroscience 87, 559–569. doi: 10.1016/s0306-4522(98)00143-2
76. Maya-Vetencourt, J. F., Baroncelli, L., Viegi, A., Tiraboschi, E., Castren, E., Cattaneo, A., et al. (2012). IGF-1 restores visual cortex plasticity in adult life by reducing local GABA levels. Neural Plast. 2012:250421. doi: 10.1155/2012/250421
77. McMorris, F., and Dubois-Dalcq, M. (1988). Insulin-like growth factor 1 promotes cell proliferation and oligodendroglial commitment in rat progenitor cells in vitro. J. Neurosci. Res. 21, 199–209. doi: 10.1002/jnr.490210212
78. Moloney, A. M., Griffin, R. J., Timmons, S., O’Connor, R., Ravid, R., and O’Neill, C. (2010). 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 31, 224–243. doi: 10.1016/j.neurobiolaging.2008.04.002
79. Morris, J. Z., Tissenbaum, H. A., and Ruvkun, G. (1996). A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382, 536–539. doi: 10.1038/382536a0
80. Mosconi, L., Pupi, A., and De Leon, M. (2013). Brain glucose hypometabolism and oxidatice stress in preclinical Alzheimer’s disease. Ann. N Y Acad. Sci. 1147, 180–195. doi: 10.1196/annals.1427.007
81. Mozell, R., and McMorris, F. (1991). Insulin like growth factor 1 stimulates oligodendrocyte development and myelination in rat brain aggregate cultures. J. Neurosci. Res. 30, 382–390. doi: 10.1002/jnr.490300214
82. Mysoet, J., Canu, M., Cieniewski-Bernard, C., Bastide, B., and Dupont, E. (2014). Hypoactivity affects IGF-1 level and PI3K/AKT signaling pathway in cerebral structures implied in motor control. PLoS One 9:e107631. doi: 10.1371/journal.pone.0107631
83. Mysoet, J., Dupont, E., Bastide, B., and Canu, M. (2015). Role of IGF-1 in cortical plasticity and functional deficit induced by sensorimotor restriction. Behav. Brain Res. 290, 117–123. doi: 10.1016/j.bbr.2015.04.055
84. Nieto-Estévez, V., Defterali, Ç., and Vicario-Abejón, C. (2016a). IGF-I: a key growth factor that regulates neurogenesis and synaptogenesis from embryonic to adult stages of the brain. Front. Neurosci., 10:52. doi: 10.3389/fnins.2016.00052
85. Nieto-Estévez, V., Oueslati-Morales, C. O., Lingling, L., Pickel, J., Morales, A. V., and Vicario-Abejón, C. (2016b). Brain insulin-like growth factor-1 directs the transition from stem cells to mature neurons during postnatal/adult hippocampal neurogenesis. Stem Cells 34, 2194–2209. doi: 10.1002/stem.2397
86. O’Kusky, J. R., Ye, P., and D’Ercole, A. J. (2000). Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development. J. Neurosci. 20, 8435–8442.
87. Pañeda, C., Arroba, A. I., Frago, L. M., Holm, A. M., Rømer, J., Argente, J., et al. (2003). Growth hormone releasing peptide-6 inhibits cerebellar cell death in aged rats. Neuroreport 14, 1633–1635. doi: 10.1097/00001756-200308260-00018
88. Paolisso, G., Ammendola, S., Del Buono, A., Gambardella, A., Riondino, M., Tagliamonte, M., et al. (1997). Serum levels of insulin-like growth factor-1 (IGF1) and IGF-binding protein-3 in healthy centenarians: relationship with plasma leptin and lipid concentrations, insulin action, and cognitive function. J. Clin. Endocrinol. Metab. 82, 2204–2209. doi: 10.1210/jc.82.7.2204
89. Papadakis, M. A., Grady, D., Black, D., Tierney, M. J., Gooding, G. A., Schambelan, M., et al. (1996). Growth hormone replacement in healthy older men improves body composition but not functional ability. Ann. Int. Med. 124, 708–716. doi: 10.7326/0003-4819-124-8-199604150-00002
90. Papadakis, M. A., Grady, D., Tierney, M. J., Black, D., Wells, L., and Grunfeld, C. (1995). Insulin-like growth factor-1 and functional status in healthy older men. J. Am. Geriatr. Soc. 43, 1350–1355. doi: 10.1111/j.1532-5415.1995.tb06613.x
91. Popken, G. J., Hodge, R. D., Ye, P., Zhang, J., Ng, W., O’Kusky, J. R., et al. (2004). In vivo effects of insulin-like growth factor-I (IGF-I) on prenatal and early postnatal development of the central nervous system. Eur. J. Neurosci. 19, 2056–2068. doi: 10.1111/j.0953-816x.2004.03320.x
92. Rollero, A., Murialdo, G., Fonzi, S., Garrone, S., Gianelli, M. V., Gazzerro, E., et al. (1998). Relationship between cognitive function, growth hormone and insulin-like growth factor 1 plasma levels in aged subjects. Neuropsychobiology 38, 73–79. doi: 10.1159/000026520
93. Sadagurski, M., Cheng, Z., Rozzo, A., Palazzolo, I., Kelley, G. R., Dong, X., et al. (2011). IRS2 increases mitochondrial dysfunction and oxidative stress in a mouse model of Huntington disease. J. Clin. Invest. 121, 4070–4081. doi: 10.1172/JCI46305
94. Sadagurski, M., and White, M. F. (2013). Integrating metabolism and longevity through insulin and IGF-1 signalling. Endocrinol. Metab. Clin. North Am. 42, 127–148. doi: 10.1016/j.ecl.2012.11.008
95. Sharples, A. P., Hughes, D. C., Deane, C. S., Saini, A., Selman, C., and Stewart, C. E. (2015). Longevity and skeletal muscle mass: the role of the sirtuins, dietary restriction and protein intake. Aging Cell 14, 511–523. doi: 10.1111/acel.12342
96. Shcheglovitov, A., Shcheglovitova, O., Yazawa, M., Portmann, T., Shu, R., Sebastiano, V., et al. (2013). SHANK3 and IGF1 restore synaptic deficits in neurons from 22q13 deletion syndrome patients. Nature 503, 267–271. doi: 10.1038/nature12618
97. Sherrard, R. M., and Bower, A. J. (2003). IGF-1 induces neonatal climbing-fibre plasticity in the mature rat cerebellum. Neuroreport 14, 1713–1716. doi: 10.1097/01.wnr.0000087732.58565.f2
98. Sonntag, W. E., Bennett, S. A., Khan, A. S., Thornton, P. L., Xu, X., Ingram, R. L., et al. (2000a). Age and insulin-like growth factor-1modulate N-methyl-D-aspartate receptor subtype expression in rats. Brain Res. Bull. 51, 331–338. doi: 10.1016/s0361-9230(99)00259-2
99. Sonntag, W. E., Lynch, C., Thornton, P., Khan, A., Bennett, S., and Ingam, R. (2000b). The effects of growth hormone and IGF1 deficiency on cerebrovascular and brain ageing. J. Anat. 197, 575–585. doi: 10.1046/j.1469-7580.2000.19740575.x
100. Sonntag, W. E., Lynch, C. D., Bennett, S. A., Khan, A. S., Thornton, P. L., Cooney, P. T., et al. (1999). Alterations in insulin-like growth factor-1 gene and protein expression and type-1 insulin-like growth factor receptors in the brains of aging rats. Neuroscience 88, 269–279. doi: 10.1016/s0306-4522(98)00192-4
101. Steen, E., Terry, B. M., Rivera, E. J., Cannon, J. L., Neely, T. R., Tavares, R., et al. (2005). Impaired insulin resistance and insulin-like growth factor expression and sginalling mechanisms in Alzheimer’s disease—is this type 3 diabetes? J. Alzheimers Dis. 7, 63–80.
102. Suh, Y., Atzmon, G., Cho, M. O., Hwang, D., Liu, B., Leahy, D. J., et al. (2008). Functionally significant insulin-like growth factor I receptor mutations in centenarians. Proc. Natl. Acad. Sci. U S A 105, 3438–3442. doi: 10.1073/pnas.0705467105
103. Sun, L. Y., Evans, M. S., Hsieh, J., Oanici, J., and Bartke, A. (2005). Increased neurogenesis in dentate gyrus of long-lived Ames dwarf mice. Endocrinology 146, 1138–1144. doi: 10.1210/en.2004-1115
104. Supeno, N., Pati, S., Hadi, R., Ghani, A., Mustafa, Z., Abdullah, J., et al. (2013). IGF-1 acts as a controlling switch for long-term proliferation and maintenance of EGF/FGF-responsive striatal neural stem cells. Int. J. Med. Sci. 10, 522–531. doi: 10.7150/ijms.5325
105. Talbot, K., Wang, H. Y., Kazi, H., Han, L. Y., Bakshi, K. P., Stucky, A., et al. (2012). Demonstrated brain insulin resistance in Alzheimer’s disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J. Clin. Invest. 122, 1316–1338. doi: 10.1172/JCI59903
106. Tatar, M., Kopelman, A., Epstein, D., Tu, M.-P., Yin, C. M., and Garofalo, R. S. (2001). A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292, 107–110. doi: 10.1126/science.1057987
107. Trejo, J., Carro, E., and Torres-Aleman, I. (2001). Circulating insulin-like growth factor-1 mediates exercise-induced increases in the of new neurons in the adult hippocampus. J. Neurosci. 21, 1628–1634.
108. Tropea, D., Giacometti, E., Wilson, N. R., Beard, C., McCurry, C., Fu, D. D., et al. (2009). Patrial reversal of Rett syndrome-like symptoms in MECP2 mutant mice. Proc. Natl. Acad. Sci. U S A 106, 2029–2034. doi: 10.1073/pnas.0812394106
109. Tropea, D., Krerman, G., Lyckman, A., Mukherjee, S., Yu, H., Horng, S., et al. (2006). Gene expression changes and molecular pathways mediating activity-dependent plasticity in the visual cortex. Nat. Neurosci. 9, 660–668. doi: 10.1038/nn1689
110. Vahdatpour, C., Dyer, A. H., and Tropea, D. (2016). Insulin-like growth factor 1 and related compounds in the treatment of childhood-onset neurodevelopmental disorders. Front. Neurosci. 10:450. doi: 10.3389/fnins.2016.00450
111. White, M. (2014). IRS2 integrates insulin/IGF1 signalling with metabolism, neurodegeneration and longevity. Diabetes Obes. Metab. 16, 4–15. doi: 10.1111/dom.12347
112. Willcox, B. J., Donlon, T. A., He, Q., Chen, R., Grove, J. S., Yano, K., et al. (2008). FOXO3A genotype is strongly associated with human longevity. Proc. Natl. Acad. Sci. U S A 105, 13987–13992. doi: 10.1073/pnas.0801030105
113. Wine, R. N., McPherson, C. A., and Harry, G. J. (2009). IGF-1 and pAKT signaling promote hippocampal CA1 neuronal survival following injury to dentate granule cells. Neurotox. Res. 16, 280–292. doi: 10.1007/s12640-009-9060-y
114. Wolkow, C. A., Kimura, K. D., Lee, M.-S., and Ruvkun, G. (2000). Regulation of C. elegans life-span by insulin like signaling in the nervous system. Science 290, 147–150. doi: 10.1126/science.290.5489.147
115. Ye, P., Carson, J., and D’Ercole, A. (1995). In vivo actions of insulin-like growth factor-1 (IGF-1) on brain myelination: studies of IGF-1 and IGF-binding protein (IGFBP-1) transgenic mice. J. Neuro. 15, 7344–7356.
116. Ye, P., and D’Ercole, A. J. (1999). Insulin-like growth factor I protects oligodendrocytes from tumor necrosis factor-a-induced injury. Endocrinology 140, 3063–3072. doi: 10.1210/en.140.7.3063
117. Ye, P., Lee, K., and D’Ercole, A. (2000). Insulin-like growth factor-1 (IGF-1) protects myelination from under-nutritional insult: studies of transgenic mice overexpressing IGF1 in the brain. J. Neurosci. Res. 62, 700–708. doi: 10.1002/1097-4547(20001201)62:5<700::aid-jnr9>3.0.co;2-1
118. Ye, P., Li, L., Richards, R. G., DiAugustine, R. P., and D’Ercole, A. J. (2002). Myelination is altered in insulin-like growth factor null mice. J. Neurosci. 22, 6041–6051.
119. Ye, P., Xing, Y., Dai, Z., and D’Ercole, A. J. (1996). In vivo actions of insulin-like growth factor-I (IGF-I) on cerebellum development in transgenic mice: evidence that IGF-I increases proliferation of granule cell progenitors. Dev. Brain Res. 95, 44–54. doi: 10.1016/0165-3806(96)00492-0
120. Yin, F., Jiang, T., and Cadenas, E. (2013). Metabolic traid in brain aging: mitochondria, insulin/IGF1 signalling and JNK signalling. Biochem. Soc. Trans. 41, 101–105. doi: 10.1042/BST20120260
121. Yuan, H., Chen, R., Wu, L., Chen, Q., Hu, A., Zhang, T., et al. (2015). The regulatory mechanisms of neurogenesis by IGF1 in adult mice. Mol. Neurobiol. 51, 512–522. doi: 10.1007/s12035-014-8717-6