Intranasal administration of IGF-1 attenuates hypoxic-ischemic brain injury in neonatal rats

Experimental Neurology

Volumn 217, Issue 2, 2009, Pages 361-370

  Lin, Shuying ^a   Fan, Lir Wan ^a   Rhodes, Philip G ^a   Cai, Zhengwei ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

Akt; Cerebral hypoxia ischemia; Insulin like growth factor 1; Intranasal administration; Newborn; Proliferation

Indexed keywords

OXYGEN; PROTEIN KINASE B; RECOMBINANT SOMATOMEDIN C; SOMATOMEDIN C;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN HYPOXIA; BRAIN INJURY; BRAIN ISCHEMIA; CAROTID ARTERY LIGATION; CELL PROLIFERATION; COGNITION; COMPARATIVE STUDY; CONTROL GROUP; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; NERVE CELL; NEUROPATHOLOGY; NEUROPROTECTION; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; SHAM PROCEDURE; SIGNAL TRANSDUCTION;

ADMINISTRATION, INTRANASAL; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BRAIN INFARCTION; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; HYPOXIA-ISCHEMIA, BRAIN; INSULIN-LIKE GROWTH FACTOR I; NERVE REGENERATION; NEUROGENESIS; NEUROPROTECTIVE AGENTS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; TREATMENT OUTCOME;

EID: 67349099863     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.03.021     Document Type: Article

References (46)

1. Agmo A., and Belzung C. The role of subtypes of the opioid receptor in the anxiolytic action of chlordiazepoxide. Neuropharmacology 37 (1998) 223-232
2. Altman J., and Sudarshan K. Postnatal development of locomotion in the laboratory rat. Anim. Behav. 23 (1975) 896-920
3. Balin B.J., Broadwell R.D., Salcman M., and el-Kalliny M. Avenues for entry of peripherally administered protein to the central nervous system in mouse, rat, and squirrel monkey. J. Comp. Neurol. 251 (1986) 260-280
4. Brywe K.G., Mallard C., Gustavsson M., Hedtjärn M., Leverin A.L., Wang X., Blomgren K., Isgaard J., and Hagberg H. IGF-I neuroprotection in the immature brain after hypoxia-ischemia, involvement of Akt and GSK3beta?. Eur. J. Neurosci. 21 (2005) 1489-1502
5. Cao Y., Gunn A.J., Bennet L., Wu D., George S., Gluckman P.D., Shao X.M., and Guan J. Insulin-like growth factor (IGF)-1 suppresses oligodendrocyte caspase-3 activation and increases glial proliferation after ischemia in near-term fetal sheep. J. Cereb. Blood Flow Metab. 23 (2003) 739-747
6. Cheng B., and Mattson M.P. IGF-I and IGF-II protect cultured hippocampal and septal neurons against calcium-mediated hypoglycemic damage. J. Neurosci. 12 (1992) 1558-1566
7. Clawson T.F., Vannucci S.J., Wang G.M., Seaman L.B., Yang X.L., and Lee W.H. Hypoxia-ischemia-induced apoptotic cell death correlates with IGF-I mRNA decrease in neonatal rat brain. Biol. Signals Recept. 8 (1999) 281-293
8. Crowder R.J., and Freeman R.S. Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factor-dependent sympathetic neurons. J. Neurosci. 18 (1998) 2933-2943
9. Cui Q.L., and Almazan G. IGF-I-induced oligodendrocyte progenitor proliferation requires PI3K/Akt, MEK/ERK, and Src-like tyrosine kinases. J. Neurochem. 100 (2007) 1480-1493
10. D'Ercole A.J., and Ye P. Expanding the mind: insulin-like growth factor I and brain development. Endocrinology 149 (2008) 5958-5962
11. D'Ercole A.J., Ye P., Calikoglu A.S., and Gutierrez-Ospina G. The role of the insulin-like growth factors in the central nervous system. Mol. Neurobiol. 13 (1996) 227-255
12. Dempsey R.J., Sailor K.A., Bowen K.K., Türeyen K., and Vemuganti R. Stroke-induced progenitor cell proliferation in adult spontaneously hypertensive rat brain: effect of exogenous IGF-1 and GDNF. J. Neurochem. 87 (2003) 586-597
13. Fan L.W., Lin S., Pang Y., Lei M., Zhang F., Rhodes P.G., and Cai Z. Hypoxia-ischemia induced neurological dysfunction and brain injury in the neonatal rat. Behav. Brain Res. 165 (2005) 80-90
14. Feldman E.L., Sullivan K.A., Kim B., and Russell J.W. Insulin-like growth factors regulate neuronal differentiation and survival. Neurobiol. Dis. 4 (1997) 201-214
15. Felling R.J., Snyder M.J., Romanko M.J., Rothstein R.P., Ziegler A.N., Yang Z., Givogri M.I., Bongarzone E.R., and Levison S.W. Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia/ischemia. J. Neurosci. 26 (2006) 4359-4369
16. Fukunaga K., and Kawano T. Akt is a molecular target for signal transduction therapy in brain ischemic insult. J. Pharmacol. Sci. 92 (2003) 317-327
17. Guan J. Insulin-like growth factor-1 and its derivatives: potential pharmaceutical application for ischemic brain injury. Recent. Patents. CNS Drug Discov. 3 (2008) 112-127
18. Guan J., Skinner S.J., Beilharz E.J., Hua K.M., Hodgkinson S., Gluckman P.D., and Williams C.E. The movement of IGF-I into the brain parenchyma after hypoxic-ischaemic injury. Neuroreport 7 (1996) 632-636
19. Guan J., Williams C.E., Skinner S.J., Mallard E.C., and Gluckman P.D. 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 (1996) 893-898
20. Guan J., Gunn A.J., Sirimanne E.S., Tuffin J., Gunning M.I., Clark R., and Gluckman P.D. 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 (2000) 513-519
21. Guan J., Bennet L., George S., Wu D., Waldvogel H.J., Gluckman P.D., Faull R.L., Crosier P.S., and Gunn A.J. Insulin-like growth factor-1 reduces postischemic white matter injury in fetal sheep. J. Cereb. Blood Flow Metab. 21 (2001) 493-502
22. Hermans R.H., Hunter D.E., McGivern R.F., Cain C.D., and Longo L.D. Behavioral sequelae in young rats of acute intermittent antenatal hypoxia. Neurotoxicol. Teratol. 14 (1992) 119-129
23. Johnston B.M., Mallard E.C., Williams C.E., and Gluckman P.D. Insulin-like growth factor-1 is a potent neuronal rescue agent after hypoxic-ischemic injury in fetal lambs. J. Clin. Invest. 97 (1996) 300-308
24. Kalluri H.S., Vemuganti R., and Dempsey R.J. Mechanism of insulin-like growth factor I-mediated proliferation of adult neural progenitor cells: role of Akt. Eur. J. Neurosci. 25 (2007) 1041-1048
25. LeRoith D., Werner H., Faria T.N., Kato H., Adamo M., and Roberts Jr. C.T. Insulin-like growth factor receptors. Implications for nervous system function. Ann. N. Y. Acad. Sci. 692 (1993) 22-32
26. Lin S., Fan L.W., Pang Y., Rhodes P.G., Mitchell H.J., and Cai Z. IGF-1 protects oligodendrocyte progenitor cells and improves neurological functions following cerebral hypoxia-ischemia in the neonatal rat. Brain Res. 1063 (2005) 15-26
27. Liu X., Fawcett J.R., Thorne R.G., DeFor T.A., and Frey II W.H. Intranasal administration of insulin-like growth factor-I bypasses the blood-brain barrier and protects against focal cerebral ischemic damage. J. Neurol. Sci. 187 (2001) 91-97
28. Liu X.F., Fawcett J.R., Thorne R.G., and Frey II W.H. Non-invasive intranasal insulin-like growth factor-I reduces infarct volume and improves neurologic function in rats following middle cerebral artery occlusion. Neurosci. Lett. 308 (2001) 91-94
29. Miles D.K., and Kernie S.G. Hypoxic-ischemic brain injury activates early hippocampal stem/progenitor cells to replace vulnerable neuroblasts. Hippocampus 18 (2008) 793-806
30. Otaegi G., Yusta-Boyo M.J., Vergaño-Vera E., Méndez-Gómez H.R., Carrera A.C., Abad J.L., González M., de la Rosa E.J., Vicario-Abejón C., and de Pablo F. Modulation of the PI 3-kinase-Akt signalling pathway by IGF-I and PTEN regulates the differentiation of neural stem/precursor cells. J. Cell. Sci. 119 (2006) 2739-2748
31. Ouyang Y.B., Tan Y., Comb M., Liu C.L., Martone M.E., Siesjö B.K., and Hu B.R. Survival- and death-promoting events after transient cerebral ischemia: phosphorylation of Akt, release of cytochrome C and Activation of caspase-like proteases. J. Cereb. Blood Flow Metab. 19 (1999) 1126-1135
32. Peltier J., O'Neill A., and Schaffer D.V. PI3K/Akt and CREB regulate adult neural hippocampal progenitor proliferation and differentiation. Dev. Neurobiol. 67 (2007) 1348-1361
33. Peng Y., Jiang B.H., Yang P.H., Cao Z., Shi X., Lin M.C., He M.L., and Kung H.F. Phosphatidylinositol 3-kinase signaling is involved in neurogenesis during Xenopus embryonic development. J. Biol. Chem. 279 (2004) 28509-28514
34. Popken G.J., Hodge R.D., Ye P., Zhang J., Ng W., O'Kusky J.R., and D'Ercole A.J. 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 (2004) 2056-2068
35. Rice J.E., Vannucci R.C., and Brierley J.B. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 9 (1981) 131-141
36. Russell J.W., Windebank A.J., Schenone A., and Feldman E.L. Insulin-like growth factor-I prevents apoptosis in neurons after nerve growth factor withdrawal. J. Neurobiol. 36 (1998) 455-467
37. Schäbitz W.R., Hoffmann T.T., Heiland S., Kollmar R., Bardutzky J., Sommer C., and Schwab S. Delayed neuroprotective effect of insulin-like growth factor-I after experimental transient focal cerebral ischemia monitored with MRI. Stroke 32 (2001) 1226-1233
38. Sung S.M., Jung D.S., Kwon C.H., Park J.Y., Kang S.K., and Kim Y.K. Hypoxia/reoxygenation stimulates proliferation through PKC-dependent activation of ERK and Akt in mouse neural progenitor cells. Neurochem. Res. 32 (2007) 1932-1939
39. Thorne R.G., Emory C.R., Ala T.A., and Frey II W.H. Quantitative analysis of the olfactory pathway for drug delivery to the brain. Brain Res. 692 (1995) 278-282
40. Thorne R.G., Pronk G.J., Padmanabhan V., and Frey II W.H. Delivery of insulin-like growth factor-I to the rat brain and spinal cord along olfactory and trigeminal pathways following intranasal administration. Neuroscience 127 (2004) 481-496
41. Tomimatsu T., Fukuda H., Endo M., Watanabe N., Mu J., Kohzuki M., Fujii E., Kanzaki T., and Murata Y. Effects of hypothermia on neonatal hypoxic-ischemic brain injury in the rat: phosphorylation of Akt, activation of caspase-3-like protease. Neurosci. Lett. 312 (2001) 21-24
42. Vig P.J., Subramony S.H., D'Souza D.R., Wei J., and Lopez M.E. Intranasal administration of IGF-I improves behavior and Purkinje cell pathology in SCA1 mice. Brain Res. Bull. 69 (2006) 573-579
43. Yan Y.P., Sailor K.A., Vemuganti R., and Dempsey R.J. Insulin-like growth factor-1 is an endogenous mediator of focal ischemia-induced neural progenitor proliferation. Eur. J. Neurosci. 24 (2006) 45-54
44. Yang Z., and Levison S.W. Perinatal hypoxic/ischemic brain injury induces persistent production of striatal neurons from subventricular zone progenitors. Dev. Neurosci. 29 (2007) 331-340
45. Yoshimoto T., Uchino H., He Q.P., Li P.A., and Siesjö B.K. Cyclosporin A, but not FK506, prevents the downregulation of phosphorylated Akt after transient focal ischemia in the rat. Brain Res. 899 (2001) 148-158
46. Wood T.L., Loladze V., Altieri S., Gangoli N., Levison S.W., Brywe K.G., Mallard C., and Hagberg H. Delayed IGF-1 administration rescues oligodendrocyte progenitors from glutamate-induced cell death and hypoxic-ischemic brain damage. Dev. Neurosci. 29 (2007) 302-310