Increased expression of insulin-like growth factor I augments the progressive phase of synaptogenesis without preventing synapse elimination in the hypoglossal nucleus

Journal of Comparative Neurology

Volumn 464, Issue 3, 2003, Pages 382-391

  O'Kusky, John Robert ^a   Ye, Ping ^b   Joseph D'Ercole, A ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Neurogenesis; Postnatal development; Stereology; Transgenic mice

Indexed keywords

SOMATOMEDIN C;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE OVEREXPRESSION; HYPOGLOSSAL NERVE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEREOLOGY; SYNAPTOGENESIS; TRANSGENIC MOUSE;

AGING; ANIMALS; ANIMALS, NEWBORN; HYPOGLOSSAL NERVE; INSULIN-LIKE GROWTH FACTOR I; MEDIAN EMINENCE; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; SYNAPSES;

EID: 0043233070     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10794     Document Type: Article

References (65)

1. Aizeman Y, De Vellis J. 1987. Brain neurons develop in a serum and glia free environment: effects of transferrin, insulin, insulin-like growth factor-I and thyroid hormones on survival, growth and differentiation. Brain Res 406:32-42.
2. Arsenijevic Y, Weiss S, Schneider B, Aebischer P. 2001. 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 21:7194-7202.
3. Asher RA, Morgenstern DA, Fidler PS, Adcock KH, Oohira A, Braistead JE, Levine JM, Margolis RU, Rogers JH, Fawcett JW. 2000. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 20:2427-2438.
4. Asher RA, Morgenstern DA, Shearer MC, Adcock KH, Pesheva P, Fawcett JW. 2002. Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells. J Neurosci 22:2225-2236.
5. Bach MA, Shen-Orr Z, Lower WL, Roberts CT, LeRoith D. 1991. Insulin-like growth factor I mRNA levels are developmentally regulated in specific regions of the rat brain. Mol Brain Res 10:43-48.
6. Baker J, Liu J, Robertson EJ, Efstratiadis A. 1993. Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75:73-82.
7. Bandtlow CE, Schwab ME. 2000. NI-35/250/Nogo-A: a neurite growth inhibitor restricting structural plasticity and regeneration of nerve fibers in the adult vertebrate CNS. Glia 29:175-181.
8. Barres BA, Hart IK, Coles HS, Burne JF, Voyvodic JT, Richardson WD, Raff MC. 1992. Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70:31-46.
9. Bartlett WP, Li XS, Williams M, Benkovic S. 1991. Localization of insulin-like growth factor-I mRNA in murine central nervous system during postnatal development. Dev Biol 147:239-250.
10. Beck KD, Powell-Braxton L, Widmer HR, Valverde J, Hefti F. 1995. IGF-I gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 14:717-730.
11. Behringer RR, Lewin TM, Quaife CJ, Palmiter RD, Brinster RL, D'Ercole AJ. 1990. Expression of insulin-like growth factor I stimulates normal somatic growth in growth hormone-deficient transgenic mice. Endocrinology 127:1033-1040.
12. Bondy C. 1991. Transient IGF-I gene expression during maturation of functionally related central projection neurons. J Neurosci 11:3442-3455.
13. Brooker GJ, Kalloniatis M, Russo VC, Murphy M, Werther GA, Bartlett PF. 2000. Endogenous IGF-1 regulates the neuronal differentiation of adult stem cells. J Neurosci Res 59:332-341.
14. Camarero G, Avendano C, Fernandez-Moreno C, Villar A, Contreras J, de Pablo F, Pichel JG, Varela-Nieto I. 2001. Delayed inner ear maturation and neuronal loss in postnatal Igf-1-deficient mice. J Neurosci 21: 7630-7641.
15. Caroni P, Grandes P. 1990. Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated insulin-like growth factors. J Cell Biol 110:1307-1317.
16. Carson MJ, Behringer RR, Brinster RL, McMorris FA. 1993. Insulin-like growth factor I increases brain growth and central nervous system myelination in transgenic mice. Neuron 10:729-740.
17. Chen MS, Huber AB, van der Haar ME, Frank M, Schnell L, Spillmann AA, Christ F, Schwab ME. 2000. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403:434-439.
18. Chrysis D, Calikoglu AS, Ye P, D'Ercole AJ. 2001. Insulin-like growth factor-I overexpression attenuates cerebellar apoptosis by altering the expression of Bcl family proteins in a developmentally specific manner. J Neurosci 21:1481-1489.
19. Dai Z, Takahashi SI, van Wyk JJ, D'Ercole AJ. 1992. Creation of an autocrine model of insulin-like growth factor-I action in transfected FRTL-5 cells. Endocrinology 130:3175-3183.
20. Dentremont KD, Ye P, D'Ercole AJ, O'Kusky JR. 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.
21. D'Ercole AJ, Ye P, Calikoglu AS, Gutierrez-Ospina G. 1996. The role of the insulin-like growth factors in the central nervous system. Mol Neurobiol 13:227-255.
22. D'Ercole AJ, Ye P, O'Kusky JR. 2002. Mutant mouse models of insulin-like growth factor actions in the central nervous system. Neuropeptides 36:1-12.
23. D'Mello SR, Galli C, Ciotti T, Calissano P. 1993. Induction of apoptosis in cerebellar granule cells by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc Natl Acad Sci USA 90: 10989-10993.
24. Drago J, Murphy M, Carroll SM, Harvey RP, Bartlett PF. 1991. Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor I. Proc Natl Acad Sci USA 88:2199-2203.
25. Fernyhough P, Mill JF, Roberts JL, Ishii DN. 1989. Stabilization of tubulin mRNAs by insulin and insulin-like growth factor I during neurite formation. Mol Brain Res 6:109-120.
26. Folli F, Ghidella S, Bonfanti L, Kahn CR, Merighi A. 1996. The early intracellular signalling pathway for the insulin/insulin-like growth factor receptor family in the mammalian central nervous system. Mol Neurobiol 13:155-183.
27. Franklin KBJ, Paxinos G. 1997. The mouse brain in stereotaxic coordinates. San Diego: Academic Press.
28. Friedland DR, Eden AR, Laitman JT. 1995. Naturally occurring motoneuron cell death in rat upper respiratory tract motor nuclei: a histological, fast DiI and immunocytochemical study in the hypoglossal nucleus. J Neurobiol 27:520-534.
29. Friedlander DR, Milev P, Karthikeyan L, Margolis RK, Margolis RU, Grumet M. 1994. The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J Cell Biol 125:669-680.
30. Garwood J, Schnadelbach O, Clement A, Schutte K, Bach A, Faissner A. 1999. DSD-1-proteoglycan is the mouse homolog of phosphican and displays opposing effects on neurite outgrowth dependent on neuronal lineage. J Neurosci 19:3888-3899.
31. Glazner GW, Ishii DN. 1995. Insulin-like growth factor gene expression in rat muscle during reinnervation. Muscle Nerve 18:1433-1442.
32. Gundersen HJG, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, West MJ. 1988a. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96:379-394.
33. Gundersen HJG, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, West MJ. 1988b. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857-881.
34. Gutierrez-Ospina G, Calikoglu AS, Ye P, D'Ercole AJ. 1996. In vivo effects of insulin-like growth factor-I on the development of sensory pathways: analysis of the primary somatic sensory cortex (S1) of transgenic mice. Endocrinology 137:5484-5492.
35. Huber AB, Weinmann O, Brosamle C, Oertle T, Schwab ME. 2002. Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J Neurosci 22:3553-3567.
36. Ishii DN. 1993. Neurobiology of insulin and insulin-like growth factors. In: Loughlin SE, Fallon JH, editors. Neurotrophic factors. San Diego: Academic Press. p 415-442.
37. Katz LC, Shatz, CJ. 1996. Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
38. Kim B, Feldman EL. 1998. Differential regulation of focal adhesion kinase and mitogen activated protein kinase tyrosine phosphorylation during insulin-like growth factor-I-mediated cytoskeletal reorganization. J Neurochem 71:1333-1336.
39. Leventhal PS, Shelden EA, Kim B, Feldman EL. 1997. Tyrosine phosphorylation of paxillin and focal adhesion kinase during insulin-like growth factor-I-stimulated lamellipodial advance. J Biol Chem 272:5214-5218.
40. Liu J, Baker J, Perkins AS, Robertson EJ, Efstratiadis A. 1993. Mice carrying null mutations of the genes encoding insulin-like growth factor-I (IGF-1) and type-I IGF receptor. Cell 75:59-72.
41. Lohof AM, Delhaye-Bouchaud N, Mariani J. 1996. Synapse elimination in the central nervous system: functional significance and cellular mechanisms. Rev Neurosci 7:85-101.
42. Mason JL, Ye P, Suzuki K, D'Ercole AJ, Matsushima GK. 2000. Insulin-like growth factor-1 inhibits mature oligodendrocyte apoptosis during primary demyelination. J Neurosci 20:5703-5708.
43. Mathews LS, Hammer RE, Behringer RR, D'Ercole AJ, Bell GI, Brinster RL, Palmiter RD. 1988. Growth enhancement of transgenic mice expressing human insulin-like growth factor I. Endocrinology 123:2827-2833.
44. Mayhew TM. 1996. How to count synapses unbiasedly and efficiently at the ultrastructural level: proposal for a standard sampling and counting protocol. J Neurocytol 25:793-804.
45. McMorris FA, Dubois-Dalcq M. 1988. Insulin-like growth factor I promotes cell proliferation and oligodendroglial commitment in rat glial progenitor cells developing in vitro. J Neurosci Res 21:199-209.
46. Mozell RL, McMorris FA. 1991. Insulin-like growth factor I stimulates oligodendrocyte development and myelination in rat brain aggregate cultures. J Neurosci Res 30:382-390.
47. Ni W, Rajkumar K, Nagy JI, Murphy LJ. 1997. Impaired brain development and reduced astrocyte response to injury in transgenic mice expressing IGF binding protein-1. Brain Res 769:97-107.
48. Niblock MM, Brunso-Bechtold JK, Riddle DR. 2000. Insulin-like growth factor I stimulates dendritic growth in primary somatosensory cortex. J Neurosci 20:4165-4176.
49. O'Kusky JR. 1998. Postnatal changes in the numerical density and total number of asymmetric and symmetric synapses in the hypoglossal nucleus of the rat. Dev Brain Res 108:179-191.
50. O'Kusky JR, Ye P, D'Ercole AJ. 2000. Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development. J Neurosci 20:8435-8442.
51. Pesheva P, Gennarini G, Goridis C, Schachner M. 1993. The F3/11 cell adhesion molecule mediates the repulsion of neurons by the extracellular matrix glycoprotein J1-160/180. Neuron 10:69-82.
52. Pons S, Torres-Aleman I. 1992. Basic fibroblast growth factor modulates insulin-like growth factor-I, its receptor, and its binding proteins in hypothalamic cell cultures. Endocrinology 131:2271-2278.
53. Purves D, Lichtman JW. 1980. Elimination of synapses in the developing nervous system. Science 210:153-157.
54. Schwab ME, Caroni P. 1988. Oligodendrocytes and CNS myelin are non-permissive substrates for neurite outgrowth and fibroblast spreading in vitro. J Neurosci 8:2381-2393.
55. Sumantran VN, Feldman EL. 1993. Insulin-like growth factor I regulates c-myc and GAP-43 messenger ribonucleic acid expression in SH-SY5Y human neuroblastoma cells. Endocrinology 132:2017-2023.
56. Taber Pierce E. 1973. Time of origin of neurons in the brain stem of the mouse. Prog Brain Res 40:53-65.
57. Torres-Aleman I, Naftolin F, Robbins RJ. 1990. Trophic effects of insulin-like growth factor-I on fetal rat hypothalamic cells in culture. Neuroscience 35:601-608.
58. Wang C, Li Y, Wible B, Angelides KJ, Ishii DN. 1992. Effects of insulin and insulin-like growth factors on neurofilament mRNA and tubulin mRNA content in human neuroblastoma SH-SY5Y cells. Mol Brain Res 13: 289-300.
59. Weibel ER. 1979. Stereological methods. Volume 1. Practical methods for biological morphometry. Orlando: Academic Press.
60. Werther GA, Cheesman H, Russo V. 1993. Olfactory bulb organ culture is supported by combined insulin-like growth factor-I and basic fibroblast growth factor. Brain Res 617:339-342.
61. Ye P, D'Ercole AJ. 1999. Insulin-like growth factor I protects oligodendrocytes from tumor necrosis factor-α-induced injury. Endocrinology 140: 3063-3072.
62. Ye P, Carson J, D'Ercole AJ. 1995. In vivo actions of insulin-like growth factor-I (IGF-I) on brain myelination: studies of IGF-I and IGF binding protein-1 (IGFBP-1) transgenic mice. J Neurosci 15:7344-7356.
63. Ye P, Xing Y, Dai Z, D'Ercole AJ. 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.
64. Ye P, Lee KH, D'Ercole AJ. 2000. Insulin-like growth factor-I (IGF-I) protects myelination from undernutritional insult: studies of transgenic mice overexpressing IGF-I in brain. J Neurosci Res 62:700-708.
65. Zackenfels K, Oppenheim RW, Rohrer H. 1995. Evidence for an important role of IGF-I and IGF-II for the early development of chick sympathetic neurons. Neuron 14:731-741.