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Activation of ERK1/2 after neonatal rat cerebral hypoxia–ischaemia

  1. Xiaoyang Wang1,3,
  2. Changlian Zhu1,3,
  3. Lin Qiu1,3,
  4. Henrik Hagberg1,4,
  5. Mats Sandberg5,
  6. Klas Blomgren1,2

Article first published online: 4 FEB 2004

DOI: 10.1046/j.1471-4159.2003.01838.x

Issue

Journal of Neurochemistry

Journal of Neurochemistry

Volume 86, Issue 2, pages 351–362, July 2003

Additional Information

How to Cite

Wang, X., Zhu, C., Qiu, L., Hagberg, H., Sandberg, M. and Blomgren, K. (2003), Activation of ERK1/2 after neonatal rat cerebral hypoxia–ischaemia. Journal of Neurochemistry, 86: 351–362. doi: 10.1046/j.1471-4159.2003.01838.x

Author Information

  1. 1

    Perinatal Center, Departments of Physiology and

  2. 2

    Pediatrics, Göteborg University, Göteborg, Sweden

  3. 3

    Department of Pediatrics, The Third Affiliated Hospital of Zhengzhou University, Zhengzhou, People's Republic of China

  4. 4

    Perinatal Center, Department of Obstetrics and Gynecology, Sahlgrenska University Hospital/Östra, Göteborg, Sweden

  5. 5

    Department of Medical Biophysics, Göteborg University, Göteborg, Sweden

*Address correspondence and reprint requests to Klas Blomgren, Perinatal Center, Department of Physiology, Göteborg University, Medicinaregatan 13, SE 413 90 Göteborg, Sweden. E-mail: klas.blomgren@fysiologi.gu.se

Publication History

  1. Issue published online: 4 FEB 2004
  2. Article first published online: 4 FEB 2004
  3. Received November 25, 2002; revised manuscript received March 23, 2003; accepted April 3, 2003.

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References

  • Abe K. and Saito H. (2000) Amyloid beta neurotoxicity not mediated by the mitogen-activated protein kinase cascade in cultured rat hippocampal and cortical neurons. Neurosci. Lett. 292, 1–4.
  • Adachi M., Fukuda M. and Nishida E. (1999) Two co-existing mechanisms for nuclear import of MAP kinase: passive diffusion of a monomer and active transport of a dimer. EMBO J. 18, 5347–5358.
  • 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.
  • Bading H. and Greenberg M. E. (1991) Stimulation of protein tyrosine phosphorylation by NMDA receptor activation. Science 253, 912–914.
  • Blomgren K., Kawashima S., Saido T. C., Karlsson J. O., Elmered A. and Hagberg H. (1995) Fodrin degradation and subcellular distribution of calpains after neonatal rat cerebral hypoxia–ischemia. Brain Res. 684, 143–149.
  • Blomgren K., Zhu C., Wang X., Karlsson J. O., Leverin A. L., Bahr B. A., Mallard C. and Hagberg H. (2001) Synergistic activation of caspase-3 by M-calpain after neonatal hypoxia–ischemia: a mechanism of ‘pathological apoptosis’? J. Biol. Chem. 276, 10191–10198.
  • Boulton T. G., Nye S. H., Robbins D. J., Ip N. Y., Radziejewska E., Morgenbesser S. D., DePinho R. A., Panayotatos N., Cobb M. H. and Yancopoulos G. D. (1991) ERKs: a family of protein–serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65, 663–675.
  • DeFranco D. B. (2002) Navigating steroid hormone receptors through the nuclear compartment. Mol. Endocrinol. 16, 1449–1455.
  • Didenko V. V. and Hornsby P. J. (1996) Presence of double-strand breaks with single-base 3′ overhangs in cells undergoing apoptosis but not necrosis. J. Cell Biol. 135, 1369–1376.
  • Garrido Y. C., Sanabria E. R., Funke M. G., Cavalheiro E. A. and Naffah-Mazzacoratti M. G. (1998) Mitogen-activated protein kinase is increased in the limbic structures of the rat brain during the early stages of status epilepticus. Brain Res. Bull. 47, 223–229.
  • Gerdes J., Lemke H., Baisch H., Wacker H. H., Schwab U. and Stein H. (1984) Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol. 133, 1710–1715.
  • Gilland E. and Hagberg H. (1997) Is MK-801 neuroprotection mediated by systemic hypothermia in the immature rat? Neuroreport 8, 1603–1605.
  • Gilland E., Bona E. and Hagberg H. (1998) Temporal changes of regional glucose use, blood flow, and microtubule-associated protein 2 immunostaining after hypoxia–ischemia in the immature rat brain. J. Cereb. Blood Flow Metab. 18, 222–228.
  • Glading A., Uberall F., Keyse S. M., Lauffenburger D. A. and Wells A. (2001) Membrane proximal ERK signaling is required for M-calpain activation downstream of epidermal growth factor receptor signaling. J. Biol. Chem 276, 23341–23348.
  • Grewal S. S., York R. D. and Stork P. J. (1999) Extracellular-signal-regulated kinase signalling in neurons. Curr. Opin. Neurobiol. 9, 544–553.
  • Gu Z., Jiang Q. and Zhang G. (2001) Extracellular signal-regulated kinase 1/2 activation in hippocampus after cerebral ischemia may not interfere with post-ischemic cell death. Brain Res. 901, 79–84.
  • Hagberg H., Gilland E., Diemer N. H. and Andine P. (1994) Hypoxia–ischemia in the neonatal rat brain: histopathology after post- treatment with NMDA and non-NMDA receptor antagonists. Biol. Neonate 66, 205–213.
  • Halliday A. L. and Cepko C. L. (1992) Generation and migration of cells in the developing striatum. Neuron 9, 15–26.
  • Han B. H. and Holtzman D. M. (2000) BDNF protects the neonatal brain from hypoxia–ischemic injury in vivo via the ERK pathway. J. Neurosci. 20, 5775–5781.
  • 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.
  • Hu B. 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.
  • 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.
  • Irving E. A. and Bamford M. (2002) Role of mitogen- and stress-activated kinases in ischemic injury. J. Cereb. Blood Flow Metab. 22, 631–647.
  • Irving E. A., Barone F. C., Reith A. D., Hadingham S. J. and Parsons A. A. (2000) Differential activation of MAPK/ERK and p38/SAPK in neurons and glia following focal cerebral ischaemia in the rat. Brain Res. Mol. Brain Res. 77, 65–75.
  • Kee N., Sivalingam S., Boonstra R. and Wojtowicz J. M. (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J. Neurosci. Methods 115, 97–105.
  • Khokhlatchev A. V., Canagarajah B., Wilsbacher J., Robinson M., Atkinson M., Goldsmith E. and Cobb M. H. (1998) Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation. Cell 93, 605–615.
  • 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.
  • Kulich S. M. and Chu C. T. (2001) Sustained extracellular signal-regulated kinase activation by 6-hydroxydopamine: implications for Parkinson's disease. J. Neurochem. 77, 1058–1066.
    Direct Link:
  • Kuroki Y., Fukushima K., Kanda Y., Mizuno K. and Watanabe Y. (2001) Neuroprotection by estrogen via extracellular signal-regulated kinase against quinolinic acid-induced cell death in the rat hippocampus. Eur J. Neurosci. 13, 472–476.
    Direct Link:
  • Lenormand P., Sardet C., Pages G., L'Allemain G., Brunet A. and Pouyssegur J. (1993) Growth factors induce nuclear translocation of MAP kinases (p42 MAPK and p44 MAPK) but not of their activator MAP kinase kinase (p45 MAPKK) in fibroblasts. J. Cell Biol. 122, 1079–1088.
  • Lesuisse C. and Martin L. J. (2002) Immature and mature cortical neurons engage different apoptotic mechanisms involving caspase-3 and the mitogen-activated protein kinase pathway. J. Cereb. Blood Flow Metab. 22, 935–950.
  • Levison S. W. and Goldman J. E. (1993) Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of post-natal rat forebrain. Neuron 10, 201–212.
  • Lois C. and Alvarez-Buylla A. (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl Acad. Sci. USA 90, 2074–2077.
  • McRae A., Gilland E., Bona E. and Hagberg H. (1995) Microglia activation after neonatal hypoxic-ischemia. Brain Res. Dev Brain Res. 84, 245–252.
  • Marshall C. J. (1995) Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179–185.
  • 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.
  • 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.
  • Oppenheim R. W. (1991) Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453–501.
  • Ortiz J., Harris H. W., Guitart X., Terwilliger R. Z., Haycock J. W. and Nestler E. J. (1995) Extracellular signal-regulated protein kinases (ERKs) and ERK kinase (MEK) in brain: regional distribution and regulation by chronic morphine. J. Neurosci. 15, 1285–1297.
  • Reffas S. and Schlegel W. (2000) Compartment-specific regulation of extracellular signal-regulated kinase (ERK) and c-Jun N-terminal kinase (JNK) mitogen-activated protein kinases (MAPKs) by ERK-dependent and non-ERK-dependent inductions of MAPK phosphatase (MKP)-3 and MKP-1 in differentiating P19 cells. Biochem. J. 352 Part 3, 701–708.
  • Reiser V., Ammerer G. and Ruis H. (1999) Nucleocytoplasmic traffic of MAP kinases. Gene Expr 7, 247–254.
  • Rice J. E., Vannucci R. C. and Brierley J. B. (1981) The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 9, 131–141.
    Direct Link:
  • Roberts-Lewis J., Savage M., Marcy V., Pinsker L. and Siman R. (1994) Immunolocalization of calpain I-mediated spectrin degradation to vulnerable neurons in the ischemic gerbil brain. J. Neurosci. 14, 3934–3944.
  • Saido T., Yokota M., Nagao S., Yamaura I., Tani E., Tsuchiya T., Suzuki K. and Kawashima S. (1993) Spatial resolution of fodrin proteolysis in post-ischemic brain. J. Biol. Chem 268, 25239–25243.
  • 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.
  • Segal R. A. and Greenberg M. E. (1996) Intracellular signaling pathways activated by neurotrophic factors. Annu. Rev. Neurosci. 19, 463–489.
  • Seubert P., Lee K. and Lynch G. (1989) Ischemia triggers NMDA receptor-linked cytoskeletal proteolysis in hippocampus. Brain Res. 492, 366–370.
  • Siman R. and Noszek J. (1988) Excitatory amino acids activate calpain I and induce structural protein breakdown in vivo. Neuron 1, 279–287.
  • Singer C. A., Figueroa-Masot X. A., Batchelor R. H. and Dorsa D. M. (1999) The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J. Neurosci. 19, 2455–2463.
  • Stanciu M. and DeFranco D. B. (2002) Prolonged nuclear retention of activated extracellular signal-regulated protein kinase promotes cell death generated by oxidative toxicity or proteasome inhibition in a neuronal cell line. J. Biol. Chem 277, 4010–4017.
  • Stanciu M., Wang Y., Kentor R., Burke N., Watkins S., Kress G., Reynolds I., Klann E., Angiolieri M. R., Johnson J. W. and DeFranco D. B. (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.
  • Tanapat P., Hastings N. B., Reeves A. J. and Gould E. (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19, 5792–5801.
  • Whitaker J. R. and Granum P. E. (1980) An absolute method for protein determination based on difference in absorbance at 235 and 280 nm. Anal Biochem. 109, 156–159.
  • Xia Z., Dickens M., Raingeaud J., Davis R. J. and Greenberg M. E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326–1331.
  • Zhu C., Wang X., Hagberg H. and Blomgren K. (2000) Correlation between caspase-3 activation and three different markers of DNA damage in neonatal cerebral hypoxia–ischemia. J. Neurochem. 75, 819–829.
    Direct Link:
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