Insulin-like growth factor (IGF)-1 suppresses oligodendrocyte caspase-3 activation and increases glial proliferation after ischemia in near-term fetal sheep

Journal of Cerebral Blood Flow and Metabolism

Volumn 23, Issue 6, 2003, Pages 739-747

  Cao, Yun ^a,b   Gunn, Alistair Jan ^a   Bennet, Laura ^a   Wu, David ^a   George, Sherly ^a   Gluckman, Peter D ^a   Shao, Xiao Mei ^b   Guan, Jian ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b CHILDREN S HOSPITAL OF FUDAN UNIVERSITY   (China)

Author keywords

Caspase 3; Fetal sheep; Glial reaction; IGF 1; Proliferation; White matter injury

Indexed keywords

CASPASE 3; CYCLINE; MYELIN BASIC PROTEIN; SOMATOMEDIN C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CAROTID ARTERY OBSTRUCTION; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; DOSE RESPONSE; ENZYME ACTIVATION; GLIA CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROGLIA; MYELINATION; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; SHEEP; WHITE MATTER;

EID: 0038119611     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.WCB.0000067720.12805.6F     Document Type: Article

References (47)

1. Back SA, Han BH, Luo N, Chricton CA, Xanthoudakis S, Tam J, Arvin KL, Holtzman DM (2002) Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischaemia. J Neurosci 22:455-463
2. Barres BA, Hart IK, Coles HS, Burne JF, Voyvodic JT, Richardson WD, Raff MC (1992) Cell death in the oligodendrocyte lineage. J Neurobiol 23:1221-1230
3. Baxter RC (1993) Circulating binding proteins for the insulinlike growth factors. Trends Endocrinol Metab 4:91-96
4. Chernausek SD (1993) Insulin-like growth factor-I (IGF-I) production by astroglial cells: regulation and importance for epidermal growth factor- induced cell replication. J Neurosci Res 34:189-197
5. 6 integrin-laminin-dependent mechanism. Glia 36:281-294
6. Dougherty KD, Dreyfus CF, Black IB (2000) Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/macrophages after spinal cord injury. Neurobiol Dis 7:574-585
7. Edwards AD, Cox P, Hope PL, Azzopardi DV, Squier MV, Mehmet H (1997) Apoptosis in the brains of infants suffering intrauterine cerebral injury. Pediatr Res 42:684-689
8. Galli C, Meucci O, Scorziello A, Werge TM, Calissano P, Schettini G (1995) Apoptosis in cerebellar granule cells is blocked by high KCl, forskolin, and IGF-1 through distinct mechanisms of action: the involvement of intracellular calcium and RNA synthesis. J Neurosci 15:1172-1179
9. Giulian D, Vaca K, Corpuz M (1993) Brain glia release factors with opposing actions upon neuronal survival. J Neurosci 13:29-37
10. Goddard DR, Berry M, Butt AM (1999) In vivo actions of fibroblast growth factor-2 and insulin-like growth factor-I on oligodendrocyte development and myelination in the central nervous system. J Neurosci Res 57:74-85
11. Guan J, Williams CE, Skinner SJM, Mallard EC, Gluckman PD (1996) The effects of insulin-like growth factor (IGF)-1, IGF-2, and Des-IGF-1 on neuronal loss after hypoxic-ischemic brain injury in adult rats - evidence for a role for IGF binding proteins. Endocrinology 137:893-898
12. Guan J, Beilharz EJ, Skinner SJM, Williams CE, Gluckman PD (2000) Intracerebral transportation and cellular localisation of insulin-like growth factor-1 following central administration to rats with hypoxic-ischemic brain injury. Brain Res 853:163-173
13. Guan J, Gunn AJ, Sirimanne ES, Tuffin J, Gunning M, Clark RG, Gluckman PD (2000) The window of opportunity for neuronal rescue with insulin-like growth factor-1 after hypoxia-ischemia in rats is critically modulated by cerebral temperature during recovery. J Cereb Blood Flow Metab 20:513-519
14. Guan J, Bennet L, Wu D, George S, Waldvogel HJ, Faull RLM, Gluckman PD, Crosier PS, Gunn AJ (2001) Insulin-like growth factor-1 reduces white matter damage following ischemic brain injury in fetal sheep. J Cereb Blood Flow Metab 21:493-502
15. Guler HP, Zapf J, Schmid C, Froesch ER (1989) Insulin-like growth factors I and II in healthy man. Estimations of half-lives and production rates. Acta Endocrinol 121:753-758
16. Hack M (2000) Perinatal brain injury in preterm infants and later neurobehavioral function. JAMA 284:1973-1974
17. Hu BR, Liu CL, Ouyang Y, Blomgren K, Siesjo BK (2000) Involvement of caspase-3 in cell death after hypoxia-ischemia declines during brain maturation. J Cereb Blood Flow Metab 20:1294-1300
18. Ikeda T, Murata Y, Quilligan EJ, Choi BH, Parer JT, Doi S, Park SD (1998) Physiologic and histologic changes in near-term fetal lambs exposed to asphyxia by partial umbilical cord occlusion. Am J Obstet Gynecol 178:24-32
19. Johnston BM, Mallard EC, Williams CE, Gluckman PD (1996) Insulin-like growth factor-1 is a potent neuronal rescue agent after hypoxic-ischemic injury in fetal lambs. J Clin Invest 97:300-308
20. Ju WK, Kim KY, Hofmann HD, Kim IB, Lee MY, Oh SJ, Chun MH (2000) Selective neuronal survival and upregulation of PCNA in the rat inner retina following transient ischaemia. J Neuropathol Exp Neurol 59:241-250
21. Leist M, Jaattela M (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2:589-598
22. Liedtka W, Edelmann W, Bieri PL, Chiu FC, Cowan NJ, Kucherlapati R, Raine CS (1996) GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination. Neuron 17:607-615
23. Ludwin SK (1988) Remyelination in the central nervous system and the peripheral nervous system. Adv Neurol 47:215-254
24. Marin-Padilla M (1997) Developmental neuropathology and impact of perinatal brain damage. II: white matter lesions of the neocortex. J Neuropathol Exp Neurol 56:219-235
25. 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
26. McMorris FA, Mckinnon RD (1996) Regulation of oligodendrocyte development and CNS myelination by growth factors: prospects for therapy of demyelinating disease. Brain Pathol 6:313-329
27. Miyazaki H, Nagashima K, Okuma Y, Nomura Y (2001) Expression of glial cell line-derived neurotrophic factor induced by transient forebrain ischaemia in rats. Brain Res 922:165-172
28. Nagata K, Takai N, Nakajima K, Saitoh H, Kohsaka S (1993) Microglia conditioned medium promotes survival and development of cultured mesencephalic neurons from embryonic rat brain. J Neurosci Res 34:357-363
29. Nakajima K, Tsuzaki N, Shimojo M, Hamanoue M, Kohsaka S (1992) Microglia isolated from rat brain secrete a urokinase-type plasminogen activator. Brain Res 577:285-292
30. Nawashiro H, Brenner M, Fukni S, Shima K, Hallenbeck JM (2000) High susceptibility to cerebral ischemia in GFAP-null mice. J Cereb Blood Flow Metab 20:1040-1044
31. Ness JK, Wood TL (2002) Insulin-like growth factor I, but not neurotrophin-3, sustains Akt activation and provides long-term protection of immature oligodendrocytes from glutamate-mediated apoptosis. Mol Cell Neurosci 20:476-488
32. O'Donnell SL, Frederick TJ, Krady JK, Vannucci SJ, Wood TL (2002) IGF-I and microglia/macrophage proliferation in the ischemic mouse brain. Glia 39:85-97
33. Pantoni L, Garcia JH, Gutierrez JA (1996) Cerebral white matter is highly vulnerable to ischemia. Stroke 27:1641-1646
34. Parrizas M, Saltiel AR, LeRoith D (1997) Insulin-like growth factor 1 inhibits apoptosis using the phosphatidylinositol 3′-kinase and mitogen-activated protein kinase pathways. J Biol Chem 272:154-161
35. Peruzzi F, Prisco M, Dews M, Salomoni P, Grassilli E, Romano G, Calabretta B (1999) Multiple signal pathways of the insulin-like growth factor 1 receptor in protection from apoptosis. Mol Cell Biol 19:7203-7215
36. Petersson KH, Pinar H, Stopa EG, Faris RA, Sadowska GB, Hanumara RC, Stonestreet BS (2002) White matter injury after cerebral ischemia in ovine fetuses. Pediatr Res 51:768-776
37. Petito CK, Olarte JP, Roberts B, Nowak TS, Pulsinelli WA (1998) Selective glial vulnerability following transient global ischemia in rat brain. J Neuropathol Exp Neurol 57:231-238
38. Petty MA, Wettstein JG (1999) White matter ischaemia. Brain Res Brain Res Rev 31:58-64
39. Pulera MR, Adams LM, Liu H, Santos DG, Nishimura RN, Yang F, Cole GM, Wasterlain CG (1998) Apoptosis in a neonatal model of cerebral hypoxia-ischaemia. Stroke 29:2622-2630
40. Rabchevsky AG, Streit WJ (1998) Role of microglia in postinjury repair and regeneration of the CNS. Ment Retard Dev Disabil Res Rev 4:187-192
41. Skoff RP, Bessert DA, Barks JD, Song D, Cerghet M, Silverstein FS (2001) Hypoxic-ischemic injury results in acute disruption of myelin gene expression and death of oligodendroglial precursors in neonatal mice. Int J Dev Neurosci 19:197-208
42. Takadera T, Matsuda I, Ohyashiki T (1999) Apoptotic cell death and caspase-3 activation induced by N-methyl-D-aspartate receptor antagonists and their prevention by insulin-like growth factor 1. J Neurochem 73:548-556
43. Tamatani M, Ogawa S, Tohyama M (1998) Roles of Bcl-2 and caspases in hypoxia-induced neuronal cell death: a possible neuroprotective mechanism of peptide growth factors. Mol Brain Res 58:27-39
44. Tomasevic G, Kamme F, Wieloch Y (1998) Changes in proliferating cell nuclear antigen, a protein involved in DNA repair, in vulnerable hippocampal neurons following global cerebral ischaemia. Brain Res 60:168-176
45. Wang JM, Hayashi T, Zhang WR, Li F, Iwai M, Abe K (2001) Reduction of ischemic damage by application of insulin-like growth factor-1 in rat brain after transient ischemia. Acta Med Okayama 55:25-30
46. Yin QW, Johnson J, Prevette D, Oppenheim RW (1994) Cell death of spinal motoneurons in the chick embryo following deafferentation: rescue effects of tissue extracts, soluble proteins, and neurotrophic agents. J Neurosci 14:7629-7640
47. Yue X, Mehmet H, Penrice J, Cooper C, Cady E, Wyatt JS, Reynolds EO, Edwards AD, Squier MV (1997) Apoptosis and necrosis in the newborn piglet brain following transient cerebral hypoxia-ischaemia. Neuropathol Appl Neurobiol 23:16-25