Mg2+ homeostasis: The balancing act of TRPM6

Current Opinion in Nephrology and Hypertension

Volumn 23, Issue 4, 2014, Pages 361-369

  Van Der Wijst, Jenny ^a   Bindels, René J M ^a   Hoenderop, Joost G J ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Distal convoluted tubule; Hypomagnesemia; Magnesium channel; TRPM

Indexed keywords

MAGNESIUM ION; TRANSIENT RECEPTOR POTENTIAL CHANNEL M6; MAGNESIUM; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPM6 PROTEIN, HUMAN;

GENE; GENE MUTATION; HEART DISEASE; HOMEOSTASIS; HYPOCALCEMIA; HYPOMAGNESEMIA; KIDNEY DISTAL TUBULE; KIDNEY TUBULE ABSORPTION; MAGNESIUM BLOOD LEVEL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSTEOPOROSIS; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRPM6 GENE; VASCULAR DISEASE; BLOOD; EPITHELIUM; GENETICS; HUMAN; HYPERCALCIURIA; KIDNEY CALCIFICATION; KIDNEY TUBULE DISORDER; METABOLISM; PHYSIOLOGY;

EPITHELIUM; HOMEOSTASIS; HUMANS; HYPERCALCIURIA; KIDNEY TUBULES, DISTAL; MAGNESIUM; NEPHROCALCINOSIS; RENAL TUBULAR TRANSPORT, INBORN ERRORS; SIGNAL TRANSDUCTION; TRPM CATION CHANNELS;

EID: 84902146665     PISSN: 10624821     EISSN: 14736543     Source Type: Journal    
DOI: 10.1097/01.mnh.0000447023.59346.ab     Document Type: Review

References (92)

1. Topf JM, Murray PT. Hypomagnesemia and hypermagnesemia. Rev Endocr Metab Disord 2003; 4:195-206.
2. Agus ZS. Hypomagnesemia. J Am Soc Nephrol 1999; 10:1616-1622.
3. Andoh TF, Burdmann EA, Fransechini N, et al. Comparison of acute rapamycin nephrotoxicity with cyclosporine and FK506. Kidney Int 1996; 50:1110-1117.
4. Cundy T, Dissanayake A. Severe hypomagnesaemia in long-Term users of proton-pump inhibitors. Clin Endocrinol (Oxf) 2008; 69:338-341.
5. Schrag D, Chung KY, Flombaum C, Saltz L. Cetuximab therapy and symptomatic hypomagnesemia. J Natl Cancer Inst 2005; 97:1221-1224.
6. Schilsky RL, Anderson T. Hypomagnesemia and renal magnesium wasting in patients receiving cisplatin. Ann Intern Med 1979; 90:929-931.
7. Alamoudi OS. Hypomagnesaemia in chronic, stable asthmatics: prevalence, correlation with severity and hospitalization. Eur Respir J 2000; 16:427-431.
8. Chakraborti S, Chakraborti T, Mandal M, et al. Protective role of magnesium in cardiovascular diseases: a review. Mol Cell Biochem 2002; 238:163-179.
9. Nieves JW. Osteoporosis: the role of micronutrients. Am J Clin Nutr 2005; 81:1232S-1239S.
10. Sales CH, Pedrosa Lde F. Magnesium and diabetes mellitus: their relation. Clin Nutr 2006; 25:554-562.
11. Beyer FR, Dickinson HO, Nicolson DJ, et al. Combined calcium, magnesium and potassium supplementation for the management of primary hypertension in adults. Cochrane Database Sits Rev 2006; 3:CD004805.
12. Simon DB, Nelson-Williams C, Bia MJ, et al. Gitelmans variant of Bartters syndrome, inherited hypokalaemic alkalosis, is caused by mutations in the thiazide-sensitive Na-Cl cotransporter. Nat Genet 1996; 12:24-30.
13. Weber S, Schneider L, Peters M, et al. Novel paracellin-1 mutations in 25 families with familial hypomagnesemia with hypercalciuria and nephrocalcinosis. J Am Soc Nephrol 2001; 12:1872-1881.
14. Konrad M, Schaller A, Seelow D, et al. Mutations in the tight-junction gene claudin 19 (CLDN19) are associated with renal magnesium wasting, renal failure, and severe ocular involvement. Am J Hum Genet 2006; 79:949-957.
15. Meij IC, Koenderink JB, De Jong JC, et al. Dominant isolated renal magnesium loss is caused by misrouting of the Na+,K+-ATPase gamma-subunit. Ann N Y Acad Sci 2003; 986:437-443.
16. Groenestege WMT, Thebault S, van der Wijst J, et al. Impaired basolateral sorting of pro-EGF causes isolated recessive renal hypomagnesemia. J Clin Invest 2007; 117:2260-2267.
17. Stuiver M, Lainez S, Will C, et al. CNNM2, encoding a basolateral protein required for renal Mg2+ handling, is mutated in dominant hypomagnesemia. Am J Hum Genet 2011; 88:333-343.
18. Glaudemans B, van der Wijst J, Scola RH, et al. A missense mutation in the Kv1.1 voltage-gated potassium channel-encoding gene KCNA1 is linked to human autosomal dominant hypomagnesemia. J Clin Invest 2009; 119:936-942.
19. Scholl UI, Choi M, Liu T, et al. Seizures, sensorineural deafness, ataxia, mental retardation, and electrolyte imbalance (SeSAME syndrome) caused by mutations in KCNJ10. Proc Natl Acad Sci U S A 2009; 106:5842-5847.
20. Adalat S, Woolf AS, Johnstone KA, et al. HNF1B mutations associate with hypomagnesemia and renal magnesium wasting. J Am Soc Nephrol 2009; 20:1123-1131.
21. Ferre S, de Baaij JHF, Ferreira P, et al. Mutations in PCBD1 cause hypomagnesemia and renal magnesium wasting. J Am Soc Nephrol 2013; 25:574-586.
22. Schlingmann KP, Weber S, Peters M, et al. Hypomagnesemia with secondary hypocalcemia is caused by mutations in TRPM6, a new member of the TRPM gene family. Nat Genet 2002; 31:166-170.
23. Walder RY, Landau D, Meyer P, et al. Mutation of TRPM6 causes familial hypomagnesemia with secondary hypocalcemia. Nat Genet 2002; 31:171-174.
24. Chubanov V, Waldegger S, Mederos y Schnitzler M, et al. Disruption of TRPM6/TRPM7 complex formation by a mutation in the TRPM6 gene causes hypomagnesemia with secondary hypocalcemia. Proc Natl Acad Sci U S A 2004; 101:2894-2899.
25. Li M, Jiang J, Yue L. Functional characterization of homo- And heteromeric channel kinases TRPM6 and TRPM7. J Gen Physiol 2006; 127:525-537.
26. Schlingmann KP, Sassen MC, Weber S, et al. Novel TRPM6 mutations in 21 families with primary hypomagnesemia and secondary hypocalcemia. J Am Soc Nephrol 2005; 16:3061-3069.
27. Jalkanen R, Pronicka E, Tyynismaa H, et al. Genetic background of HSH in three Polish families and a patient with an X;9 translocation. Eur J Hum Genet 2006; 14:55-62.
28. Zhao Z, Pei Y, Huang X, et al. Novel TRPM6 mutations in familial hypomagnesemia with secondary hypocalcemia. Am J Nephrol 2013; 37:541-548.
29. Guran T, Akcay T, Bereket A, et al. Clinical and molecular characterization of Turkish patients with familial hypomagnesaemia: novel mutations in TRPM6 and CLDN16 genes. Nephrol Dial Transplant 2012; 27:667-673.
30. Voets T, Nilius B, Hoefs S, et al. TRPM6 forms the Mg2+ influx channel involved in intestinal and renal Mg2+absorption. J Biol Chem 2004; 279:19-25.
31. Lainez S, Schlingmann KP, van der Wijst J, et al. New TRPM6 missense mutations linked to hypomagnesemia with secondary hypocalcemia. Eur J Hum Genet 2014; 22:497-504.
32. Habeb AM, Al-Harbi H, Schlingmann KP. Resolving basal ganglia calcification in hereditary hypomagnesemia with secondary hypocalcemia due to a novel TRPM6 gene mutation. Saudi J Kidney Dis Transpl 2012; 23:1038-1042.
33. Chubanov V, Schlingmann KP, Wäring J, et al. Hypomagnesemia with secondary hypocalcemia due to a missense mutation in the putative poreforming region of TRPM6. J Biol Chem 2007; 282:7656-7667.
34. Dai LJ, Ritchie G, Kerstan D, et al. Magnesium transport in the renal distal convoluted tubule. Physiol Rev 2001; 81:51-84.
35. Walder RY, Yang B, Stokes JB, et al. Mice defective in Trpm6 show embryonic mortality and neural tube defects. Hum Mol Genet 2009; 18:4367-4375.
36. Woudenberg-Vrenken TE, Sukinta A, van der Kemp AW, et al. Transient receptor potential melastatin 6 knockout mice are lethal whereas heterozygous deletion results in mild hypomagnesemia. Nephron Physiol 2011; 117:11-19.
37. Schaefer M. Homo- And heteromeric assembly of TRP channel subunits. Pflugers Arch 2005; 451:35-42.
38. Ramsey IS, Delling M, Clapham DE. An introduction to TRP channels. Annu Rev Physiol 2006; 68:619-647.
39. Runnels LW, Yue L, Clapham DE. TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 2001; 291:1043-1047.
40. Montell C. Mg2+ homeostasis: the Mg2+nificent TRPM chanzymes. Curr Biol 2003; 13:R799-R801.
41. Li M, Du J, Jiang J, et al. Molecular determinants of Mg2+ and Ca2+ permeability and pH sensitivity in TRPM6 and TRPM7. J Biol Chem 2007; 282:25817-25830.
42. Xie J, Sun B, Du J, et al. Phosphatidylinositol 4,5-bisphosphate (PIP(2)) controls magnesium gatekeeper TRPM6 activity. Sci Rep 2011; 1:146.
43. Qin X, Yue Z, Sun B, et al. Sphingosine and FTY720 are potent inhibitors of the transient receptor potential melastatin 7 (TRPM7) channels. Br J Pharmacol 2013; 168:1294-1312.
44. Zhang Z, Yu H, Huang J, et al. The TRPM6 kinase domain determines the Mg ATP-sensitivity of TRPM7/M6 heteromeric ion channels. J Biol Chem 2014; 289:5217-5227. doi:10.1074/jbc.M113.512285. [Epub ahead of print]
45. Matsushita M, Kozak JA, Shimizu Y, et al. Channel function is dissociated from the intrinsic kinase activity and autophosphorylation of TRPM7/ChaK1. J Biol Chem 2005; 280:20793-20803.
46. Cao G, Thebault S, van der Wijst J, et al. RACK1 inhibits TRPM6 activity via phosphorylation of the fused alpha-kinase domain. Curr Biol 2008; 18:168-176.
47. Cao G, van der Wijst J, van der Kemp A, et al. Regulation of the epithelial Mg2+ channel TRPM6 by estrogen and the associated repressor protein of estrogen receptor activity (REA). J Biol Chem 2009; 284:14788-14795.
48. Nadler MJ, Hermosura MC, Inabe K, et al. LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 2001; 411:590-595.
49. Demeuse P, Penner R, Fleig A. TRPM7 channel is regulated by magnesium nucleotides via its kinase domain. J Gen Physiol 2006; 127:421-434.
50. Thebault S, Cao G, Venselaar H, et al. Role of the alpha-kinase domain in transient receptor potential melastatin 6 channel and regulation by intracellular ATP. J Biol Chem 2008; 283:19999-20007.
51. Gwanyanya A, Sipido KR, Vereecke J, Mubagwa K. ATP and PIP2 dependence of the magnesium-inhibited, TRPM7-like cation channel in cardiac myocytes. Am J Physiol Cell Physiol 2006; 291:C627-C635.
52. Kozak JA, Cahalan MD. MIC channels are inhibited by internal divalent cations but not ATP. Biophys J 2003; 84:922-927.
53. Yu H, Zhang Z, Lis A, et al. TRPM7 is regulated by halides through its kinase domain. Cell Mol Life Sci 2013; 70:2757-2771.
54. Groenestege WMT, Hoenderop JG, van den Heuvel L, et al. The epithelial Mg2+ channel transient receptor potential melastatin 6 is regulated by dietary Mg2+ content and estrogens. J Am Soc Nephrol 2006; 17:1035-1043.
55. van Angelen AA, San-Cristobal P, Pulskens WP, et al. The impact of dietary magnesium restriction on magnesiotropic and calciotropic genes. Nephrol Dial Transplant 2013; 28:2983-2993.
56. Thebault S, Alexander RT, Tiel Groenestege WM, et al. EGF increases TRPM6 activity and surface expression. J Am Soc Nephrol 2009; 20:78-85.
57. Ikari A, Sanada A, Okude C, et al. Up-regulation of TRPM6 transcriptional activity by AP-1 in renal epithelial cells. J Cell Physiol 2010; 222:481-487.
58. Tejpar S, Piessevaux H, Claes K, et al. Magnesium wasting associated with epidermal-growth-factor receptor-Targeting antibodies in colorectal cancer: a prospective study. Lancet Oncol 2007; 8:387-394.
59. Fakih MG, Wilding G, Lombardo J. Cetuximab-induced hypomagnesemia in patients with colorectal cancer. Clin Colorectal Cancer 2006; 6:152-156.
60. Barbagallo M, Dominguez LJ, Resnick LM. Magnesium metabolism in hypertension and type 2 diabetes mellitus. Am J Ther 2007; 14:375-385.
61. Barbagallo M, Dominguez L J, Galioto A, et al. Role of magnesium in insulin action, diabetes and cardio-metabolic syndrome X. Mol Aspects Med 2003; 24:39-52.
62. Song Y, Manson JE, Buring JE, Liu S. Dietary magnesium intake in relation to plasma insulin levels and risk of type 2 diabetes in women. Diabetes Care 2004; 27:59-65.
63. Hruby A, McKeown NM, Song Y, Djoussé L. Dietary magnesium and genetic interactions in diabetes and related risk factors: a brief overview of current knowledge. Nutrients 2013; 5:4990-5011.
64. Lee C-T, Lien Y-HH, Lai L-W, et al. Increased renal calcium and magnesium transporter abundance in streptozotocin-induced diabetes mellitus. Kidney Int 2006; 69:1786-1791.
65. Song Y, Hsu Y-H, Niu T, et al. Common genetic variants of the ion channel transient receptor potential membrane melastatin 6 and 7 (TRPM6 and TRPM7), magnesium intake, and risk of type 2 diabetes in women. BMC Med Genet 2009; 10:4.
66. Nair AV, Hocher B, Verkaart S, et al. Loss of insulin-induced activation of TRPM6 magnesium channels results in impaired glucose tolerance during pregnancy. Proc Natl Acad Sci U S A 2012; 109:11324-11329.
67. de Baaij JHF, Blanchard MG, Lavrijsen M, et al. P2X4 receptor regulation of transient receptor potential melastatin type 6 (TRPM6) Mg(2+) channels. Pflugers Arch 2014. doi:10.1007/s00424-014-1440-3. [Epub ahead of print]
68. Duarte CG. Effects of ethacrynic acid and furosemide on urinary calcium, phosphate and magnesium. Metab Clin Exp 1968; 17:867-876.
69. Cohen N, Almoznino-Sarafian D, Zaidenstein R, et al. Serum magnesium aberrations in furosemide (frusemide) treated patients with congestive heart failure: pathophysiological correlates and prognostic evaluation. Heart 2003; 89:411-416.
70. Davies DL, Fraser R. Do diuretics cause magnesium deficiency? Br J Clin Pharmacol 1993; 36:1-10.
71. van Angelen AA, van der Kemp AW, Hoenderop JG, Bindels RJ. Increased expression of renal TRPM6 compensates for Mg2+ wasting during furosemide treatment. Clin Kidney J 2012; 5:535-544.
72. Hess MW, Hoenderop JGJ, Bindels RJM, Drenth JPH. Systematic review: hypomagnesaemia induced by proton pump inhibition. Aliment Pharmacol Ther 2012; 36:405-413.
73. Lameris ALL, Hess MW, van Kruijsbergen I, et al. Omeprazole enhances the colonic expression of the Mg(2+) transporter TRPM6. Pflugers Arch 2013; 465:1613-1620.
74. Barton CH, Vaziri ND, Martin DC, et al. Hypomagnesemia and renal magnesium wasting in renal transplant recipients receiving cyclosporine. Am J Med 1987; 83:693-699.
75. McDiarmid SV, Colonna JO, Shaked A, et al. A comparison of renal function in cyclosporine- And FK-506-Treated patients after primary orthotopic liver transplantation. Transplantation 1993; 56:847-853.
76. Nijenhuis T, Hoenderop JGJ, Bindels RJM. Downregulation of Ca(2+) and Mg(2+) transport proteins in the kidney explains tacrolimus (FK506)-induced hypercalciuria and hypomagnesemia. J Am Soc Nephrol 2004; 15:549-557.
77. Ledeganck KJ, Boulet GA, Horvath CA, et al. Expression of renal distal tubule transporters TRPM6 and NCC in a rat model of cyclosporine nephrotoxicity and effect of EGF treatment. Am J Physiol Renal Physiol 2011; 301:F486-F493.
78. Ledeganck KJ, De Winter BY, Van den Driessche A, et al. Magnesium loss in cyclosporine-Treated patients is related to renal epidermal growth factor downregulation. Nephrol Dial Transplant 2014; 29:1097-1102. doi:10.1093/ndt/ gft498. [Epub ahead of print]
79. Gouadon E, Lecerf F, German-Fattal M. Differential effects of cyclosporin A and tacrolimus on magnesium influx in Caco2 cells. J Pharm Pharm Sci 2012; 15:389-398.
80. van Angelen AA, Glaudemans B, van der Kemp AWCM, et al. Cisplatininduced injury of the renal distal convoluted tubule is associated with hypomagnesaemia in mice. Nephrol Dial Transplant 2013; 28:879-889.
81. Günther T, Höllriegl V. Na(+)- And anion-dependent Mg2+ influx in isolated hepatocytes. Biochim Biophys Acta 1993; 1149:49-54.
82. Romani A. Regulation of magnesium homeostasis and transport in mammalian cells. Arch Biochem Biophys 2007; 458:90-102.
83. Hurd TW, Otto EA, Mishima E, et al. Mutation of the Mg2+ transporter SLC41A1 results in a nephronophthisis-like phenotype. J Am Soc Nephrol 2013; 24:967-977.
84. Kolisek M, Nestler A, Vormann J, Schweigel-Röntgen M. Human gene SLC41A1 encodes for the Na+/Mg2+ exchanger. Am J Physiol Cell Physiol 2012; 302:C318-C326.
85. Piskacek M, Zotova L, Zsurka G, Schweyen RJ. Conditional knockdown of hMRS2 results in loss of mitochondrial Mg(2+) uptake and cell death. J Cell Mol Med 2009; 13:693-700.
86. Shindo Y, Fujii T, Komatsu H, et al. Newly developed Mg2+-selective fluorescent probe enables visualization of Mg2+ dynamics in mitochondria. PLoS ONE 2011; 6:e23684.
87. Arjona FJ, de Baaij JHF, Schlingmann KP, et al. CNNM2 mutations cause impaired brain development and seizures in patients with hypomagnesemia. PLoS Genet 2014; 10:e1004267.
88. Cittadini A, Scarpa A. Intracellular Mg2+ homeostasis of Ehrlich ascites tumor cells. Arch Biochem Biophys 1983; 227:202-209.
89. Ogoma Y, Kobayashi H, Fujii T, et al. Binding study of metal ions to S100 protein: 43Ca, 25Mg, 67Zn and 39K n.m.r. Int J Biol Macromol 1992; 14:279-286.
90. Ohki S, Ikura M, Zhang M. Identification of Mg2+-binding sites and the role of Mg2+ on target recognition by calmodulin. Biochemistry 1997; 36:4309-4316.
91. Schwaller B. Cytosolic Ca2+ buffers. Cold Spring Harb Perspect Biol 2010; 2:a004051-A14051.
92. de Baaij JHF, Groot Koerkamp MJ, Lavrijsen M, et al. Elucidation of the distal convoluted tubule transcriptome identifies new candidate genes involved in renal Mg(2+) handling. Am J Physiol Renal Physiol 2013; 305:F1563-F1573.