Are the transient receptor potential melastatin (TRPM) channels important in magnesium homeostasis following traumatic brain injury?

Magnesium Research

Volumn 22, Issue 4, 2009, Pages 225-234

  Cook, Naomi L ^a   Van Den Heuvel, Corinna ^a   Vink, Robert ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Calcium; Free magnesium; Ischemia; Magnesium transporters; Neurotrauma

Indexed keywords

CALCIUM; MAGNESIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL M;

ARTICLE; BRAIN INJURY; CELL DEATH; HOMEOSTASIS; HUMAN; MORTALITY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SURVIVOR;

BRAIN INJURIES; CALCIUM; CELL DEATH; HOMEOSTASIS; HUMANS; MAGNESIUM; RECEPTORS, N-METHYL-D-ASPARTATE; SURVIVORS; TRPM CATION CHANNELS;

EID: 73649098261     PISSN: 09531424     EISSN: 19524021     Source Type: Journal    
DOI: 10.1684/mrh.2009.0189     Document Type: Article

References (104)

1. Fleminger S, Ponsford J. Long term outcome after traumatic brain injury. Br Med J 2005; 331: 1419-20.
2. León-Carrión J, del Rosario Domínguez-Morales M, Barosso y Martin JM, Murillo-Cabezas F. Epidemiology of traumatic brain injury and subarachnoid hemorrhage. Pituitary 2005; 8: 197-202.
3. Khan F, Baguley IJ, Cameron ID. Rehabilitation after traumatic brain injury. Med J Aust 2003; 178: 290-5.
4. Hirtz D, Thurman DJ, Gwinn-Hardy K, Mohamed M, Chaudhuri AR, Zalutsky R. How common are the 'common' neurologic disorders? Neurology 2007; 68: 326-37.
5. Morales DM, Marklund N, Lebold D, Thompson HJ, Pitkanen A, Maxwell WL, et al. Experimental models of traumatic brain injury: do we really need to build a better mousetrap? Neuroscience 2005; 136: 971-89.
6. Gentile NT, McIntosh TK. Antagonists of excitatory amino acids and endogenous opioid peptides in the treatment of experimental central nervous system injury. Ann Emerg Med 1993; 22: 1028-34.
7. Roth P, Farls K. Pathophysiology of traumatic brain injury. Crit Care Nurs Q 2000; 23: 14-25.
8. Barone FC, Kilgore KS. Role of inflammation and cellular stress in brain injury and central nervous system diseases. Clin Neurosci Res 2006; 6: 329-56.
9. Cormio M, Robertson CS, Narayan RK. Secondary insults to the injured brain. J Clin Neurosci 1997; 4: 132-48.
10. Kahraman S, Ozgurtas T, Kayalt H, Atabey C, Kutluay T, Timurkaynak E. Monitoring of serum ionized magnesium in neurosurgical intensive care unit: preliminary results. Clin Chim Acta 2003; 334: 211-5.
11. Heath DL, Vink R. Traumatic brain axonal injury produces sustained decline in intracellular free magnesium concentration. Brain Res 1996; 738: 150-3.
12. 2++ is associated with irreversible tissue injury after brain trauma. J Biol Chem 1988; 263: 757-61.
13. Saatman KE, Bareyre FM, Grady MS, McIntosh TK. Acute cytoskeletal alterations and cell death induced by experimental brain injury are attenuated by magnesium treatment and exacerbated by magnesium deficiency. J Neuropathol Exp Neurol 2001; 60: 183-94.
14. Mazur A, Maier JAM, Rock E, Gueux E, Nowacki W, Rayssiguier Y. Magnesium and the inflammatory response: potential physiopathological implications. Arch Biochem Biophys 2006; 458: 48-56.
15. Altura BM, Gebrewold A, Zhang A, Altura BT. Low extracellular magnesium ions induce lipid peroxidation and activation of nuclear factor-kappa B in canine cerebral vascular smooth muscle: possible relation to traumatic brain injury and strokes. Neurosci Lett 2003; 341: 189-92.
16. Oyanagi K, Kawakami E, Kikuchi-Horie K, et al. Magnesium deficiency over generations in rats with special references to the pathogenesis of the parkinsonismdementia complex and amyotrophic lateral sclerosis of Guam. Neuropathol 2006; 26: 115-28.
17. Ebel H, Günther T. Magnesium metabolism: a review. J Clin Chem Clin Biochem 1980; 18: 257-70.
18. 2++-activated enzymes. Magnes Res 2008; 21: 185-7.
19. Van Den Heuvel C, Vink R. The role of magnesium in traumatic brain injury. Clin Calcium 2004; 14: 1187-92.
20. Terasaki M, Rubin H. Evidence that intracellular magnesium is present in cells at a regulatory concentration for protein synthesis. Proc Natl Acad Sci USA 1985; 82: 7324-6.
21. Fawcett WJ, Haxby EJ, Male DA. Magnesium: physiology and pharmacology. Br J Anaesth 1999; 83: 302-20.
22. Iseri LT, French JH. Magnesium: nature's physiologic calcium blocker. Am Heart J 1984; 108: 188-93.
23. Bara M, Guiet-Bara A. Potassium, magnesium and membranes. Magnesium 1984; 3: 212-25.
24. Saris N-E, Mervaala E, Karppanen H, Khawaja JA, Lewenstam A. Magnesium - an update on physiological, clinical and analytical aspects. Clin Chim Acta 2000; 294: 1-26.
25. Vink R, Cernak I. Regulation of intracellular free magnesium in central nervous system injury. Front Biosci 2000; 5: d656-d665.
26. Royo NC, Shimizu S, Schouten JW, Stover JF, McIntosh TK. Pharmacology of traumatic brain injury. Curr Opin Pharmacol 2003; 3: 27-32.
27. Sacco RL, Chong JY, Prabhakaran S, Elkind MSV. Experimental treatments for acute ischaemic stroke. Lancet 2007; 369: 331-41.
28. Blache D, Devaux S, Joubert O, Loreau N, Schneider M, Durand P, et al. Long-term magnesium-deficient diet shows relationships between blood pressure, inflammation and oxidant stress defense in aging rats. Free Radic Biol Med 2006; 41: 277-84.
29. Gorelick PB, Ruland S. IMAGES and FAST-MAG: magnesium for acute ischaemic stroke. Lancet Neurol 2004; 3: 330-1.
30. Von Lubitz DKJE. Adenosine and cerebral ischemia: therapeutic future or death of a brave concept? Eur J Pharmacol 1999; 365: 9-25.
31. Lee JS, Han YM, Yoo DS, et al. A molecular basis for the efficacy of magnesium treatment following traumatic brain injury. J Neurotrauma 2004; 21: 549-61.
32. Ravishankar S, Ashraf QM, Fritz K, Mishra OP, Delivoria-Papadopoulos M. Expression of Bax and Bcl-2 proteins during hypoxia in cerebral cortical neuronal nuclei of newborn piglets: effect of administration of magnesium sulfate. Brain Res 2001; 901: 23-9.
33. Bareyre FM, Saatman KE, Helfaer MA, Sinson G, Weisser JD, Brown AL, et al. Alterations in ionized and total blood magnesium after experimental traumatic brainiInjury: relationship to neurobehavioral outcome and neuroprotective efficacy of magnesium chloride. J Neurochem 1999; 73: 271-80.
34. Turner RJ, DaSilva KW, O'Connor C, Van Den Heuvel C, Vink R. Magnesium gluconate offers no more protection than magnesium sulphate following diffuse traumatic brain injury in rats. J Am Coll Nutr 2004; 23: 541S-544S.
35. Hoane MR, Barth TM. The window of opportunity for administration of magnesium therapy following focal brain injury is 24 h but is task dependent in the rat. Physiol Behav 2002; 76: 271-80.
36. Temkin NR, Anderson GD, Winn HR, et al. Magnesium sulfate for neuroprotection after traumatic brain injury: a randomised controlled trial. Lancet Neurol 2007; 6: 29-38.
37. Dhandapani SS, Gupta A, Vivekanandhan S, Sharma BS, Mahapatra AK. Randomized controlled trial of magnesium sulphate in severe closed traumatic brain injury. Ind J Neurotrauma 2008; 5: 27-33.
38. McKee JA, Brewer RP, Macy GE, Borel CO, Reynolds JD, Warner DS. Magnesium neuroprotection is limited in humans with acute brain injury. Neurocrit Care 2005; 2: 342-51.
39. Venkatachalam K, Montell C. TRP Channels. Annu Rev Biochem 2007; 76: 387-417.
40. Nilius B, Voets T. TRP channels: a TR(I)P through a world of multifunctional cation channels. Pflugers Arch 2005; 451: 1-10.
41. Clapham DE, Runnels LW, Strübing C. The TRP ion channel family. Nat Rev Neurosci 2001; 2: 387-95.
42. Pedersen SF, Owsianik G, Nilius B. TRP channels: an overview. Cell Calcium 2005; 38: 233-52.
43. Ramsey IS, Delling M, Clapham DE. An introduction to TRP channels. Annu Rev Physiol 2006; 68: 619-47.
44. Kraft R, Harteneck C. The mammalian melastatinrelated transient receptor potential cation channels: an overview. Pflugers Arch 2005; 451: 204-11.
45. Harteneck C. Function and pharmacology of TRPM cation channels. Naunyn Sch Arch Pharmacol 2005; 371: 307-14.
46. Fleig A, Penner R. The TRPM ion channel subfamily: molecular, biophysical and functional features. Trends Pharmacol Sci 2004; 25: 633-9.
47. Monteilh-Zoller MK, Hermosura MC, Nadler MJS, Scharenberg AM, Penner R, Fleig A. TRPM7 provides an ion channel mechanism for cellular entry of trace metal ions. J Gen Physiol 2003; 121: 49-60.
48. 2++-homeostasis regulation. Magnes Res 2007; 20: 6-18.
49. Nadler MJS, Hermosura MC, Inabe K, Perraud A-L, Zhu Q, Stokes AJ, et al. LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 2001; 411: 590-5.
50. Krapivinsky G, Mochida S, Krapivinsky L, Cibulsky SM, Clapham DE. The TRPM7 ion channel functions in cholinergic synaptic vesicles and affects transmitter release. Neuron 2006; 52: 485-96.
51. 2++-nucleotide-regulated MagNuM (TRPM7) currents. Cell Calcium 2006; 41: 249-60.
52. Elizondo MR, Arduini BL, Paulsen J, et al. Defective skeletogenesis with kidney stone formation in dwarf zebrafish mutant for trpm7. Curr Biol 2005; 15: 667-71.
53. He Y, Yao G, Savoia C, Touyz RM. Transient receptor potential melastatin 7 ion channels regulate magnesium homeostasis in vascular smooth muscle cells: role of angiotensin II. Circ Res 2005; 96: 207-15.
54. Hanano T, Hara Y, Shi J, Morita H, Umebayashi C, Mori E, et al. Involvement of TRPM7 in cell growth as a spontaneously activated Ca2+ entry pathway in human retinoblastoma cells. J Pharmacol Sci 2004; 95: 403-19.
55. 2++ homeostasis. Science 2008; 322: 756-60.
56. 2++ homeostasis by TRPM7. Cell 2003; 114: 191-200.
57. Demeuse P, Penner R, Fleig A. TRPM7 channel is regulated by magnesium nucleotides via its kinase domain. J Gen Physiol 2006; 127: 421-34.
58. Jiang X, Newell EW, Schlichter LC. Regulation of a TRPM7-like current in rat brain microglia. J Biol Chem 2003; 278: 42687-876.
59. Matsushita M, Kozak JA, Shimizu Y, McLachlin DT, Yamaguchi H, Wei F-W, et al. Channel function is dissociated from the intrinsic kinase activity and autophosphorylation of TRPM7/ChaK1. J Biol Chem 2005; 280: 20793-803.
60. Kozak JA, Cahalan ND. MIC channels are inhibited by internal divalent cations but not ATP. Biophys J 2003; 84: 922-7.
61. Takezawa R, Schmitz C, Demeuse P, Scharenberg AM, Penner R, Fleig A. Receptor-mediated regulation of the TRPM7 channel through its endogenous protein kinase domain. Proc Natl Acad Sci USA 2004; 101: 6009-14.
62. Runnels LW, Yue L, Clapham DE. The TRPM7 channel is inactivated by PIP2 hydrolysis. Nat Cell Biol 2002; 4: 329-36.
63. Nilius B, Owsianik G, Voets T, Peters JA. Transient receptor potential cation channels in disease. Physiol Rev 2007; 87: 165-217.
64. Huang Y, Cheung L, Rowe DB, Halliday GM. Genetic contributions to Parkinson's disease. Brain Res Rev 2004; 46: 44-70.
65. Hermosura MC, Cui AM, Go RCV, et al. Altered functional properties of a TRPM2 variant in Guamanian ALS and PD. Proc Natl Acad Sci USA 2008; 105: 18029-34.
66. Hermosura MC, Nayakanti H, Dorovkov MV, Calderon FR, Ryazanov AG, Haymer DS, et al. TRPM7 variant shows altered sensitivity to magnesium that may contribute to the pathogenesis of two Guamanian neurodegenerative disorders. Proc Natl Acad Sci USA 2005; 102: 11510-5.
67. Topala CN, Groenestege WT, Thébault S, et al. Molecular determinants of permeation through the cation channel TRPM6. Cell Calcium 2006; 41: 513-23.
68. Li M, Jiang J, Yue L. Functional characterization of homo- and heteromeric channel kinases TRPM6 and TRPM7. J Gen Physiol 2006; 127: 525-37.
69. Schlingmann KP, Weber S, Peters M, Nejsum LN, Vitzhum H, Klingel K, et al. Hypomagnesemia with secondary hypocalcemia is caused by mutations in TRPM6, a new member of the TRPM family. Nat Genet 2002; 31: 166-70.
70. Fonfria E, Murdock PR, Cusdin FS, Benham CD, Kelsell RE, McNulty S. Tissue distribution profiles of the human TRPM cation channel family. J Recept Signal Transduct Res 2006; 26: 159-78.
71. Walder RY, Landau D, Meyer P, et al. Mutation of TRPM6 causes familial hypomagnesemia with secondary hypocalcemia. Nat Genet 2002; 31: 171-4.
72. Chubanov V, Schlingmann KP, Wäring J, Heinzinger J, Kaske S, Waldegger S, et al. Hypomagnesemia with secondary hypocalcemia due to a missense mutation in the putative pore-forming region of TRPM6. J Biol Chem 2007; 282: 7656-67.
73. Schlingmann KP, Waldegger S, Konrad M, Chubanov V, Gudermann T. TRPM6 and TRPM7 - Gatekeepers of human magnesium metabolism. Biochim Biophys Acta 2007; 1772: 813-21.
74. Ryazanova LV, Pavur KS, Petrov AN, Dorovkov MV, Ryazanov AG. Novel type of signaling molecules: protein kinases covalently linked with ion channels. Mol Biol 2001; 35: 271-83.
75. Ryazanova LV, Dorovkov MV, Ansari A, Ryazanov AG. Characterisation of the protein kinase activity of TRPM7/ChaK1, a protein kinase fused to the transient receptor potential ion channel. J Biol Chem 2004; 279: 3708-16.
76. Schmitz C, Dorovkov MV, Zhao X, Davenport BJ, Ryazanov AG, Perraud A-L. The channel kinases TRPM6 and TRPM7 are functionally nonredundant. J Biol Chem 2005; 280: 37763-71.
77. Aarts M, Iihara K, Wei W-L, Xiong Z. -G., Arundine M, Cerwinski W, MacDonald JF, Tymianski M. A key role for TRPM7 channels in anoxic neuronal death. Cell 2003; 115: 863-77.
78. Aarts MM, Tymiansaki M. TRPMs and neuronal cell death. Pflugers Arch 2005; 451: 243-9.
79. MacDonald JF, Xiong Z. -G., Jackson MF. Paradox of Ca2+ signaling, cell death and stroke. Trends Neurosci 2006; 29: 75-81.
80. Sun HS, Jackson MF, Martin LJ, et al. Suppression of hippocampal TRPM7 protein prevents delayed neuronal death in brain ischemia. Nat Neurosci 2009; 12: 1300-7.
81. Heiner I, Eisfeld J, Warnstedt M, Radukina N, Jüngling E, Lückhoff A. Endogenous ADP-ribose enables calciumregulated cation currents through TRPM2 channels in neutrophil granulocytes. Biochem J 2006; 398: 225-32.
82. Lange I, Penner R, Fleig A, Beck A. Synergistic regulation of endogenous TRPM2 channels by adenine dinucleotides in primary human neutrophils. Cell Calcium 2008; 44: 604-15.
83. Nagamine K, Kudoh J, Minoshima S, Kawasaki K, Asakawa S, Ito F, et al. Molecular cloning of a novel putative Ca2+ channel protein (TRPC7) highly expressed in brain. Genomics 1998; 54: 124-31.
84. Hara Y, Wakamori M, Ishii M, et al. LTRPC2 Ca2+-permeable channel activated by changes in redox status confers susceptibility to cell death. Mol Cell 2002; 9: 163-73.
85. Fonfria E, Marshall ICB, Boyfield I, Skaper SD, Hughes JP, Owen DE, et al. Amyloid beta-peptide(1-42) and hydrogen peroxide-induced toxicity are mediated by TRPM2 in rat primary striatal cultures. J Neurochem 2005; 95: 715-23.
86. Wehage E, Eisfeld J, Heiner I, Jüngling E, Zitt C, Lückhoff A. Activation of the cation channel long transient receptor potential channel 2 (LTRPC2) by hydrogen peroxide. J Biol Chem 2002; 277: 23150-6.
87. Perraud A-L, Fleig A, Dunn CA, et al. ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature 2001; 411: 595-9.
88. Kühn FJP, Heiner I, Lückhoff A. TRPM2: a calcium influx pathway regulated by oxidative stress and the novel second messenger ADP-ribose. Pflugers Arch 2005; 451: 212-9.
89. Yamamoto S, Shimizu N, Kiyonaka S, Takahashi N, Wajima T, Hara Y, et al. TRPM2-mediated Ca2+ influx induces chemokine production in monocytes that aggravates inflammatory neutrophil infiltration. Nat Med 2008; 14: 738-47.
90. Aarts MM, Tymianski M. TRPM7 and ischemic CNS injury. Neuroscientist 2005; 11: 116-23.
91. McNulty S, Fonfria E. The role of TRPM channels in cell death. Pflugers Arch 2005; 451: 235-42.
92. Simard JM, Kent TA, Chen M, Tarasov KV, Gerzanich V. Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol 2007; 6: 258-68.
93. Hermosura MC, Monteilh-Zoller MK, Scharenberg AM, Penner R, Fleig A. Dissociation of the store-operated calcium current ICRAC and the Mg-nucleotideregulatetd metal ion current MagNuM. J Physiol 2002; 539: 445-58.
94. Heo JH, Han SW, Lee SK. Free radicals as triggers of brain edema formation after stroke. Free Radic Biol Med 2005; 39: 51-70.
95. Marmarou A, Fatouros PP, Barzo P, et al. Contribution of edema and cerebral blood volume to traumatic brain swelling in head-injured patients. J Neurosurg 2000; 93: 183-93.
96. Starkus J, Beck A, Fleig A, Penner R. Regulation of TRPM2 by extra- and intracellular calcium. J Gen Physiol 2007; 130: 427-40.
97. Hellmich HL, Eidson KA, Capra BA, Garcia JM, Boone DR, Hawkins BE, et al. Injured Fluoro-Jade-positive hippocampal neurons contain high levels of zinc after traumatic brain injury. Brain Res 2007; 1127: 119-26.
98. Suh SW, Chen JW, Motamedi M, et al. Evidence that synaptically-released zinc contributes to neuronal injury after traumatic brain injury. Brain Res 2000; 852: 268-73.
99. Vink R, Van Den Heuvel C. Recent advances in the development of multifactorial therapies for the treatment of traumatic brain injury. Exp Opin Investig Drugs 2004; 13: 1263-74.
100. Oancea E, Wolfe JT, Clapham DE. Functional TRPM7 channels accumulate at the plasma membrane in response to fluid flow. Circ Res 2005; 98: 245-53.
101. Numata T, Shimizu T, Okada Y. TRPM7 is a stretchand swelling-activated cation channel involved in volume regulation in human epithelial cells. Am J Physiol Cell Physiol 2007; 292: C460-C4C7.
102. Jiang J, Li M, Yue L. Potentiation of TRPM7 inward currents by protons. J Gen Physiol 2005; 126: 137-50.
103. Kozak JA, Matsushita M, Nairn AC, Cahalan ND. Charge screening by internal pH and polyvalent cations as a mechanism for activation, inhibition, and rundown of TRPM7/MIC channels. J Gen Physiol 2005; 126: 499-514.
104. Dorovkov MV, Ryazanov AG. Phosphorylation of annexin I by TRPM7 channel-kinase. J Biol Chem 2004; 279: 50643-6.