Suppression of hippocampal TRPM7 protein prevents delayed neuronal death in brain ischemia

Nature Neuroscience

Volumn 12, Issue 10, 2009, Pages 1300-1307

  Sun, Hong Shuo ^a   Jackson, Michael F ^b,c   Martin, Loren J ^b   Jansen, Karen ^d   Teves, Lucy ^a   Cui, Hong ^a   Kiyonaka, Shigeki ^e   Mori, Yasuo ^e   Jones, Michael ^a   Forder, Joan P ^a   Golde, Todd E ^d   Orser, Beverley A ^b,f   MacDonald, John F ^b,c   Tymianski, Michael ^a,b  

^a TORONTO WESTERN HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c ROBARTS RESEARCH INSTITUTE   (Canada)

^d MAYO GRADUATE SCHOOL   (United States)

^e KYOTO UNIVERSITY   (Japan)

^f SUNNYBROOK RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

SHORT HAIRPIN RNA; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL MELASTATIN 7 CHANNEL; UNCLASSIFIED DRUG; VIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CELL SURVIVAL; CONTROLLED STUDY; DELAYED NEUROTOXICITY; DENDRITE; EMBRYO DEVELOPMENT; HIPPOCAMPUS; HOMEOSTASIS; HUMAN; HUMAN CELL; LONG TERM POTENTIATION; MALE; NERVE CELL EXCITABILITY; NERVE CELL NECROSIS; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN ISCHEMIA; CELL DEATH; CELLS, CULTURED; DISEASE MODELS, ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIALS; FEAR; GENE EXPRESSION REGULATION; GENE TRANSFER TECHNIQUES; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HUMANS; MALE; MAZE LEARNING; MEMORY; MICE; MICROINJECTIONS; NEURONS; RATS; RATS, WISTAR; RNA, SMALL INTERFERING; TRANSFECTION; TRPM CATION CHANNELS;

EID: 70349558138     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2395     Document Type: Article

References (49)

1. Hausenloy, D.J. & Scorrano, L. Targeting cell death. Clin. Pharmacol. Ther. 82, 370-373 (2007).
2. Volpe, B.T. & Petito, C.K. Dementia with bilateral medial temporal lobe ischemia. Neurology 35, 1793-1797 (1985).
3. Petito, C.K., Feldmann, E., Pulsinelli, W.A. & Plum, F. Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology 37, 1281-1286 (1987).
4. Bennett, M.V. et al. The GluR2 hypothesis: Ca2+-permeable AMPA receptors in delayed neurodegeneration. Cold Spring Harb. Symp. Quant. Biol. 61, 373-384 (1996).
5. Volpe, B.T., Pulsinelli, W.A., Tribuna, J. & Davis, H.P. Behavioral performance of rats following transient forebrain ischemia. Stroke 15, 558-562 (1984).
6. Block, F. Global ischemia and behavioral defcits. Prog. Neurobiol. 58, 279-295 (1999).
7. Lipton, P. Ischemic cell death in brain neurons. Physiol. Rev. 79, 1431-1568 (1999).
8. Besancon, E., Guo, S., Lok, J., Tymianski, M. & Lo, E.H. Beyond NMDA and AMPA glutamate receptors: emerging mechanisms for ionic imbalance and cell death in stroke. Trends Pharmacol. Sci. 29, 268-275 (2008).
9. Aarts, M. et al. A key role for TRPM7 channels in anoxic neuronal death. Cell 115, 863-877 (2003).
10. Montell, C., Birnbaumer, L. & Flockerzi, V. The TRP channels, a remarkably functional family. Cell 108, 595-598 (2002).
11. Monteilh-Zoller, M.K. et al. TRPM7 provides an ion channel mechanism for cellular entry of trace metal ions. J. Gen. Physiol. 121, 49-60 (2003).
12. Nadler, M.J. et al. LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 411, 590-595 (2001).
13. Schmitz, C. et al. Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7. Cell 114, 191-200 (2003).
14. Jin, J. et al. Deletion of Trpm7 disrupts embryonic development and thymopoiesis without altering Mg2+ homeostasis. Science 322, 756-760 (2008).
15. Siesjo, B.K., Katsura, K. & Tibor, K. Acidosis related brain damage. in Advances in Neurology: Cellular and Molecular Mechanisms of Ischemic Brain Damage (eds. Siesjo, B.K. & Wieloch, T.) (Raven Press, New York, 1994).
16. Silver, I.A. & Erecinska, M. Intracellular and exctracellular changes of [Ca2+] in hypoxia and ischemia in rat brain in vivo. J. Gen. Physiol. 95, 837-866 (1990).
17. Lin, M.C. et al. Microdialysis analyzer and fame atomic absorption spectrometry in the determination of blood glucose, lactate and magnesium in gerbils subjected to cerebral ischemia/reperfusion. J. Am. Coll. Nutr. 23, 556S-560S (2004).
18. Runnels, L.W., Yue, L. & Clapham, D.E. TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 291, 1043-1047 (2001).
19. Kozak, J.A., Kerschbaum, H.H. & Cahalan, M.D. Distinct properties of CRAC and MIC channels in RBL cells. J. Gen. Physiol. 120, 221-235 (2002).
20. Wei, W.L. et al. TRPM7 channels in hippocampal neurons detect levels of extracellular divalent cations. Proc. Natl. Acad. Sci. USA 104, 16323-16328 (2007).
21. Kaneko, S. et al. A critical role of TRPM2 in neuronal cell death by hydrogen peroxide. J. Pharmacol. Sci. 101, 66-76 (2006).
22. Bridge, A.J., Pebernard, S., Ducraux, A., Nicoulaz, A.L. & Iggo, R. Induction of an interferon response by RNAi vectors in mammalian cells. Nat. Genet. 34, 263-264 (2003).
23. Sledz, C.A., Holko, M., de Veer, M.J., Silverman, R.H. & Williams, B.R. Activation of the interferon system by short-interfering RNAs. Nat. Cell Biol. 5, 834-839 (2003).
24. Schmitz, C. et al. The channel kinases TRPM6 and TRPM7 are functionally nonredundant. J. Biol. Chem. 280, 37763-37771 (2005).
25. Xiong, Z.G., Chu, X.P. & MacDonald, J.F. Effect of lamotrigine on the Ca2+-sensing cation current in cultured hippocampal neurons. J. Neurophysiol. 86, 2520-2526 (2001).
26. Xiong, Z., Lu, W. & MacDonald, J.F. Extracellular calcium sensed by a novel cation channel in hippocampal neurons. Proc. Natl. Acad. Sci. USA 94, 7012-7017 (1997).
27. Pulsinelli, W.A. & Brierly, J.B. A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke 10, 267-272 (1979).
28. Pulsinelli, W.A., Brierly, J.B. & Plum, F. Temporal profle of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol. 11, 491-498 (1982).
29. Saito, A. et al. Oxidative stress and neuronal death/survival signaling in cerebral ischemia. Mol. Neurobiol. 31, 105-116 (2005).
30. Corish, P. & Tyler-Smith, C. Attenuation of green fuorescent protein half-life in mammalian cells. Protein Eng. 12, 1035-1040 (1999).
31. Kumar, R. et al. Brain ischemia and reperfusion activates the eukaryotic initiation factor 2α kinase, PERK. J. Neurochem. 77, 1418-1421 (2001).
32. Stoll, G., Jander, S. & Schroeter, M. Infammation and glial responses in ischemic brain lesions. Prog. Neurobiol. 56, 149-171 (1998).
33. Gavrieli, Y., Sherman, Y. & Ben-Sasson, S.A. Indentifcation of programmed cell death in situ via specifc labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501 (1992).
34. Ji, J. & Maren, S. Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 17, 749-758 (2007).
35. Whitlock, J.R., Heynen, A.J., Shuler, M.G. & Bear, M.F. Learning induces long-term potentiation in the hippocampus. Science 313, 1093-1097 (2006).
36. Lisman, J., Schulman, H. & Cline, H. The molecular basis of CaMKII function in synaptic and behavioral memory. Nat. Rev. Neurosci. 3, 175-190 (2002).
37. Fanselow, M.S. Conditioned and unconditional components of post-shock freezing. Pavlov. J. Biol. Sci. 15, 177-182 (1980).
38. Morris, R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47-60 (1984).
39. Morris, G.F. et al. Failure of the competitive N-methyl-D-aspartate antagonist Selfotel (CGS 19755) in the treatment of severe head injury: results of two phase III clinical trials. The selfotel investigators. J. Neurosurg. 91, 737-743 (1999).
40. Davis, S.M., Albers, G.W., Diener, H.C., Lees, K.R. & Norris, J. Termination of acute stroke studies involving selfotel treatment. ASSIST steering committed. Lancet 349, 32 (1997).
41. Xiong, Z.G. et al. Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 118, 687-698 (2004).
42. Thompson, R.J., Zhou, N. & MacVicar, B.A. Ischemia opens neuronal gap junction hemichannels. Science 312, 924-927 (2006).
43. Lawlor, P.A. et al. Novel rat Alzheimer's disease models based on AAV-mediated gene transfer to selectively increase hippocampal Aβ levels. Mol. Neurodegener. 2, 11 (2007).
44. Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates (Academic Press, San Diego, 1998).
45. Mastakov, M.Y., Baer, K., Xu, R., Fitzsimons, H. & During, M.J. Combined injection of rAAV with mannitol enhances gene expression in the rat brain. Mol. Ther. 3, 225-232 (2001).
46. Sun, H.S., Feng, Z.P., Miki, T., Seino, S. & French, R.J. Enhanced neuronal damage after ischemic insults in mice lacking Kir6.2-containing ATP-sensitive K+ channels. J. Neurophysiol. 95, 2590-2601 (2006).
47. Mullen, R.J., Buck, C.R. & Smith, A.M. NeuN, a neuronal specifc nuclear protein in vertebrates. Development 116, 201-211 (1992).
48. Wang, L.Y. & MacDonald, J.F. Modulation by magnesium of the affnity of NMDA receptors for glycine in murine hippocampal neurones. J. Physiol. (Lond.) 486, 83-95 (1995).
49. Cheng, V.Y. et al. α5GABAA receptors mediate the amnestic, but not sedative-hypnotic, effects of the general anesthetic etomidate. J. Neurosci. 26, 3713-3720 (2006)