Hypoxia-induced ischemic tolerance in neonatal rat brain involves enhanced ERK1/2 signaling

Journal of Neurochemistry

Volumn 89, Issue 1, 2004, Pages 157-167

  Jones, Nicole M ^a,b   Bergeron, Marcelle ^a  

^a ELI LILLY AND COMPANY   (United States)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Extracellular signal regulated kinase; Hypoxia; Ischemia; MAP kinase; PI3K; Preconditioning

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN HYPOXIA; BRAIN ISCHEMIA; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HISTOPATHOLOGY; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; INHIBITION KINETICS; MICROVASCULATURE; NEUROPROTECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; WHITE MATTER;

ANIMALIA;

EID: 1842562380     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02324.x     Document Type: Article

References (61)

1. Adams J. P., Roberson E. D., English J. D., Selcher J. C. and Sweatt J. D. (2000) MAPK regulation of gene expression in the central nervous system. Acta Neurobiol. Exp. 60, 377-394.
2. Alessandrini A., Namura S., Moskowitz M. A. and Bonventre J. V. (1999) MEK1 protein kinase inhibition protects against damage resulting from focal cerebral ischemia. Proc. Natl Acad. Sci. USA 96, 12866-12869.
3. Back S. A., Han B. H., Luo N. L., Chricton C. A., Xanthoudakis S., Tam J., Arvin K. L. and Holtzman D. M. (2002) Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J. Neurosci. 22, 455-463.
4. Beitner-Johnson D., Rust R. T., Hsieh T. C. and Millhorn D. E. (2001) Hypoxia activates Akt and induces phosphorylation of GSK-3 in PC12 cells. Cell Signal. 13, 23-27.
5. Bergeron M., Evans S. M., Sharp F. R., Koch C. J., Lord E. M. and Ferriero D. M. (1999) Detection of hypoxic cells with the 2-nitroimidazole, EF5, correlates with early redox changes in rat brain after perinatal hypoxia-ischemia. Neuroscience 89, 1357-1366.
6. Bergeron M., Gidday J. M., Yu A. Y., Semenza G. L., Ferriero D. M. and Sharp F. R. (2000) Role of hypoxia-inducible factor-1 in hypoxia-induced ischemic tolerance in neonatal rat brain. Ann. Neurol. 48, 285-296.
7. Bernaudin M., Tang Y., Reilly M., Petit E. and Sharp F. R. (2002) Brain genomic response following hypoxia and re-oxygenation in the neonatal rat. Identification of genes that might contribute to hypoxia-induced ischemic tolerance. J. Biol. Chem. 277, 39728-39738.
8. Bhat R. V., Shanley J., Correll M. P., Fieles W. E., Keith R. A., Scott C. W. and Lee C.-M. (2000) Regulation and localization of tyrosine216 phosphorylation of glycogen synthase kinase-3β in cellular and animal models of neuronal degeneration. Proc. Natl Acad. Sci. USA 97, 11074-11079.
9. Bruer U., Weih M. K., Isaev N. K., Meisel A., Ruscher K., Bergk A., Trendelenburg G., Wiegand F., Victorov I. V. and Dirnagl U. (1997) Induction of tolerance in rat cortical neurons: hypoxic preconditioning. FEBS Lett. 414, 117-121.
10. Brunet A., Datta S. R. and Greenberg M. E. (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 11, 297-305.
11. Chow A. K., Thompson C. S., Hogan M. J., Banner D., Sabourin L. A. and Hakim A. M. (2002) Cortical spreading depression transiently activates MAP kinases. Mol. Brain Res. 99, 75-81.
12. Conrad P. W., Millhom D. E. and Beitner-Johnson D. (2000) Hypoxia differentially regulates the mitogen- and stress-activated protein kinases. Role of Ca2+/CaM in the activation of MAPK and p38γ. Adv. Exp. Med. Biol. 475, 293-302.
13. Cuda G., Paternò R., Ceravolo R., Candigliota M., Perrotti N., Perticone F., Faniello M. C., Schepsis F., Ruocco A., Mele E. et al. (2002) Protection of human endothelial cells from oxidative stress. Role of Ras-ERK1/2 signaling. Circulation 105, 968-974.
14. D'Onofrio M., Cuomo L., Battaglia G., Ngomba R. T., Storto M., Kingston A. E., Orzi F., De Blasi A., Di Iorio P., Nicoletti F. et al. (2001) Neuroprotection mediated by glial group-II metabotropic glutamate receptors requires the activation of the MAP kinase and the phosphatidylinositol-3-kinase pathways. J. Neurochem. 78, 435-445.
15. Emerson M. R., Samson F. E. and Pazdernik T. L. (2000) Effects of hypoxia preconditioning on expression of metallothionein-1,2 and heme oxygenase-1 before and after kainic acid induced seizures. Cell Mol. Biol. 46, 619-626.
16. 2+ and phospholipase C. Brain Res. 958, 43-51.
17. Gidday J. M., Fitzgibbons J. C., Shah A. R. and Park T. S. (1994) Neuroprotection from ischemic brain injury by hypoxic preconditioning in the neonatal rat. Neurosci. Lett. 168, 221-224.
18. Gidday J. M., Shah A. R., Maceren R. G., Wang Q., Pelligrino D. A., Holtzman D. M. and Park T. S. (1999) Nitric oxide mediates cerebral ischemic tolerance in a neonatal rat model of hypoxic preconditioning. J. Cereb. Blood Flow Metab. 19, 331-340.
19. ras/extracellular regulated kinase in neuronal ischemic preconditioning. Proc. Natl Acad. Sci. USA 97, 436-441.
20. Gu Z., Jiang Q. and Zhang G. (2001) Extracellular signal-regulated kinase and c-Jun N-terminal protein kinase in ischemic tolerance. Neuroreport 12, 3487-3491.
21. Han B. H. and Holtzman D. M. (2000) BDNF protects the neonatal brain from hypoxic-ischemic injury in vivo via the ERK pathway. J. Neurosci. 20, 5775-5781.
22. Harper S. J. and LoGrasso P. (2001) Signalling for survival and death in neurones: the role of stress-activated kinases, JNK and p38. Cell Signal. 13, 299-310.
23. Hetman M., Kanning K., Cavanaugh J. E. and Xia Z. (1999) Neuroprotection by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase. J. Biol. Chem. 274, 22569-22580.
24. Hu B. R., Liu C. L. and Park D. J. (2000) Alteration of MAP kinase pathways after transient forebrain ischemia. J. Cereb. Blood Flow Metab. 20, 1089-1095.
25. Hu B. R. and Wieloch T. (1994) Tyrosine phosphorylation and activation of mitogen-activated protein kinase in the rat brain following transient cerebral ischemia. J. Neurochem. 62, 1357-1367.
26. Hur E., Chang K. Y., Lee E., Lee S. K. and Park H. (2001) Mitogen-activated protein kinase inhibitor PD98059 blocks the trans-activation but not the stabilization or DNA binding ability of hypoxia-inducible factor-1α. Mol. Pharmacol. 59, 1216-1224.
27. Jin K., Mao X. O., Zhu Y. and Greenberg D. A. (2002) MEK and ERK protect hypoxic cortical neurons via phosphorylation of Bad. J. Neurochem. 80, 119-125.
28. Jones N. M. and Bergeron M. (2001) Hypoxic preconditioning induces changes in HIF-1 target genes in neonatal rat brain. J. Cereb. Blood Flow Metab. 21, 1105-1114.
29. Kitagawa H., Warita H., Sasaki C., Zhang W. R., Sakai K., Shiro Y., Mitsumoto Y., Mori T. and Abe K. (1999) Immunoreactive Akt, PI3-K and ERK protein kinase expression in ischemic rat brain. Neurosci. Lett. 274, 45-48.
30. Kobayashi S., Harris V. A. and Welsh F. A. (1995) Spreading depression induces tolerance of cortical neurons to ischemia in rat brain. J. Cereb. Blood Flow Metab. 15, 721-727.
31. Koyama Y., Tsujikawa K., Matsuda T. and Baba A. (2003) Endothelin-1 stimulates glial cell line-derived neurotrophic factor expression in cultured rat astrocytes. Biochem. Biophys. Res. Commun. 303, 1101-1105.
32. Kuroki Y., Fukushima K., Kanda Y., Mizuno K. and Watanabe Y. (2001) Neuroprotection by estrogen via extracellular signal-related kinase against quinolinic acid-induced cell death in the rat hippocampus. Eur. J. Neurosci. 13, 472-476.
33. Liu Y., Silverstein F. S., Skoff R. and Barks J. D. E. (2002) Hypoxicischemic oligodendroglial injury in neonatal rat brain. Pediatr Res. 51, 25-33.
34. Marcus J. S., Karackattu, S. L., Fleegal M. A. and Sumners C. (2003) Cytokine-stimulated inducible nitric oxide synthase expression in astroglia: role of Erk mitogen-activated protein kinase and NF-κB. Glia 41, 152-160.
35. Masada T., Hua Y., Xi G., Ennis S. R. and Keep R. F. (2001) Attenuation of ischemic brain edema and cerebrovascular injury after ischemic preconditioning in the rat. J. Cereb. Blood Flow Metab. 21, 22-33.
36. Minet E., Amould T., Michel G., Roland I., Mottet D., Raes M., Remacle J. and Michiels C. (2000) ERK activation upon hypoxia: involvement in HIF-1 activation. FEBS Lett. 468, 53-58.
37. Murray B., Alessandrini A., Cole A. J., Yee A. G. and Furshpan E. J. (1998) Inhibition of the p44/42 MAP kinase pathway protects hippocampal neurons in a cell-culture model of seizure activity. Proc. Natl Acad. Sci. USA 95, 11975-11980.
38. Nakajima W., Ishida A., Lange M. S., Gabrielson K. L., Wilson M. A., Martin L. J., Blue M. E. and Johnston M. V. (2000) Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. J. Neurosci. 20, 7994-8004.
39. Namura S., Iihara K., Takami S., Nagata I., Kikuchi H., Matsushita K., Moskowitz M. A., Bonventre J. V. and Alessandrini A. (2001) Intravenous administration of MEK inhibitor U0126 affords brain protection against forebrain ischemia and focal cerebral ischemia. Proc. Natl Acad. Sci. USA 98, 11569-11574.
40. Ota A., Ikeda T., Xia X. Y., Xia Y. X. and Ikenoue T. (2000) Hypoxic-ischemic tolerance induced by hyperthermic pretreatment in newborn rats. J. Soc. Gynecol. Invest. 7, 102-105.
41. Rice J. E., Vannucci R. C. and Brierly J. B. (1981) The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 9, 131-141.
42. Richard D. E., Berra E., Gothie E., Roux D. and Pouysségur J. (1999) p42/p44 Mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1α (HIF-1α) and enhance the transcriptional activity of HIF-1. J. Biol. Chem. 274, 32631-32637.
43. Sato M., Cordis G. A., Maulik N. and Das D. K. (2000) SAPKs regulation of ischemic preconditioning. Am. J. Physiol. 279, H901-H907.
44. Satoh T., Nakatsuka D., Watanabe Y., Nagata I., Kikuchi H. and Namura S. (2000) Neuroprotection by MAPK/ERK kinase inhibition with U0126 against oxidative stress in a mouse neuronal cell line and rat primary cultured cortical neurons. Neurosci. Lett. 288, 163-166.
45. Semenza G. L. (2000) HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 88, 1474-1480.
46. Shamloo M., Rytter A. and Wieloch T. (1999) Activation of the extracellular signal-regulated protein kinase cascade in the hippocampal CA1 region in a rat model of global cerebral ischemic preconditioning. Neuroscience 93, 81-88.
47. Simon R. P., Niiro M. and Gwinn R. (1993) Prior ischemic stress protects against experimental stroke. Neurosci. Lett. 163, 135-137.
48. Stanciu M., Wang Y., Kentor R., Burke N., Watkins S., Kress G., Reynolds I., Klann E., Angiolieri M. R., Johnson J. W et al. (2000) Persistent activation of ERK contributes to glutamate-induced oxidative toxicity in a neuronal cell line and primary cortical neuron cultures. J. Biol. Chem. 275, 12200-12206.
49. Strohm C., Barancik T., Brühl M. L., Kilian S. A. and Schaper W. (2000) Inhibition of the ER-kinase cascade by PD98059 and U0126 counteracts ischemic preconditioning in pig myocardium. J. Cardiovasc. Pharmacol. 36, 218-229.
50. Sweatt J. D. (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem. 76, 1-10.
51. Tong H., Chen W., Steenburgen C. and Murphy E. (2000) Ischemic preconditioning activates phosphatidylinositol-3-kinase upstream of protein kinase C. Circ. Res. 87, 309-315.
52. Uehara T., Kaneko M., Tanaka S., Okuma Y. and Nomura Y. (1999) Possible involvement of p38 MAP kinase in HSP70 expression induced by hypoxia in rat primary astrocytes. Brain Res. 823, 226-230.
53. Vannucci R. C., Towfighi J. and Vannucci S. J. (1998) Hypoxic preconditioning and hypoxic-ischemic brain damage in the immature rat: pathologic and metabolic correlates. J. Neurochem. 71, 1215-1220.
54. Vannucci R. C. and Yager J. Y. (1992) Glucose, lactic acid, and perinatal hypoxic-ischemic brain damage. Pediatr. Neurol. 8, 3-12.
55. Volmat V., Camps M., Arkinstall S., Pouysségur J. and Lenormand P. (2001) The nucleus, a site for signal termination by sequestration and inactivation of p42/p44 MAPK kinases. J. Cell. Sci. 114, 3433-3443.
56. Wang X., Wang H., Xu L., Rozanski D. J., Sugawara T., Chan P. H., Trzaskos J. M. and Feuerstein G. Z. (2003a) Significant neuroprotection against ischemic brain injury by inhibition of the MEK1 protein kinase in mice: exploration of potential mechanism associated with apoptosis. J. Pharmacol. Exp. Ther. 304, 172-178.
57. Wang X., Zhu C., Qiu L., Hagberg H., Sandberg M. and Blomgren K. (2003b) Activation of ERK1/2 after neonatal rat cerebral hypoxia-ischemia. J. Neurochem. 86, 351-362.
58. Wick A., Wick W., Waltenberger J., Weller M., Dichgans J. and Schulz J. B. (2002) Neuroprotection by hypoxic preconditioning requires sequential activation of vascular endothelial growth factor receptor and Akt. J. Neurosci. 22, 6401-6407.
59. Wiegand F., Liao W., Busch C. et al. (1999) Respiratory chain inhibition induces tolerance to focal cerebral ischemia. J. Cereb. Blood Flow Metab. 19, 1229-1237.
60. Xi G., Hua Y., Keep R. F., Duong H. K. and Hoff J. T. (2001) Activation of p44/42 mitogen activated protein kinases in thrombin-induced brain tolerance. Brain Res. 895, 153-159.
61. Yano S., Morioka M., Fukunaga K., Kawano T., Hara T., Kai Y., Hamada J., Miyamoto E. and Ushio Y. (2001) Activation of Akt/protein kinase B contributes to induction of ischemic tolerance in the CA1 subfield of gerbil hippocampus. J. Cereb. Blood Flow Metab. 21, 351-360.