Function and regulation of the channel-kinase TRPM7 in health and disease

European Journal of Cell Biology

Volumn 93, Issue 10-12, 2014, Pages 455-465

  Visser, Daan ^a   Middelbeek, Jeroen ^b   Van Leeuwen, Frank N ^b   Jalink, Kees ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Diseases; Embryonic development; TRPM7

Indexed keywords

CALCIUM; ION CHANNEL; MAGNESIUM; PHOSPHOLIPASE C; TRANSIENT RECEPTOR POTENTIAL CHANNEL M7; PROTEIN SERINE THREONINE KINASE; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPM7 PROTEIN, HUMAN;

BRAIN ISCHEMIA; CARDIOVASCULAR DISEASE; CELL ADHESION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CYTOSKELETON; DEGENERATIVE DISEASE; EMBRYO DEVELOPMENT; HUMAN; NONHUMAN; ORGANOGENESIS; PATHOPHYSIOLOGY; PROTEIN DOMAIN; PROTEIN FAMILY; REGULATORY MECHANISM; SHORT SURVEY; SIGNAL TRANSDUCTION; ANIMAL; CHANNEL GATING; ISCHEMIA; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

ANIMALIA;

ANIMALS; CARDIOVASCULAR DISEASES; CELL PROLIFERATION; CELL SURVIVAL; CYTOSKELETON; EMBRYONIC DEVELOPMENT; HUMANS; ION CHANNEL GATING; ISCHEMIA; MAGNESIUM; NEOPLASMS; NEURODEGENERATIVE DISEASES; PROTEIN-SERINE-THREONINE KINASES; TRPM CATION CHANNELS;

EID: 84920580399     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2014.07.001     Document Type: Short Survey

References (132)

1. Aarts M., Iihara K., Wei W.L., Xiong Z.G., Arundine M., Cerwinski W., MacDonald J.F., Tymianski M. A key role for TRPM7 channels in anoxic neuronal death. Cell 2003, 115(7):863-877.
2. Abed E., Moreau R. Importance of melastatin-like transient receptor potential 7 and cations (magnesium, calcium) in human osteoblast-like cell proliferation. Cell Prolif. 2007, 40(6):849-865.
3. Abed E., Moreau R. Importance of melastatin-like transient receptor potential 7 and magnesium in the stimulation of osteoblast proliferation and migration by platelet-derived growth factor. Am. J. Physiol. Cell Physiol. 2009, 297(2):C360-C368.
4. Bae C.Y., Sun H.S. TRPM7 in cerebral ischemia and potential target for drug development in stroke. Acta Pharmacol. Sin. 2011, 32(6):725-733.
5. Baldoli E., Maier J.A. Silencing TRPM7 mimics the effects of magnesium deficiency in human microvascular endothelial cells. Angiogenesis 2012, 15(1):47-57.
6. Bessac B.F., Fleig A. TRPM7 channel is sensitive to osmotic gradients in human kidney cells. J. Physiol. 2007, 582(Pt 3):1073-1086.
7. Brandao K., Deason-Towne F., Zhao X., Perraud A.L., Schmitz C. TRPM6 kinase activity regulates TRPM7 trafficking and inhibits cellular growth under hypomagnesic conditions. Cell Mol. Life Sci. 2014, 10.1007/s00018-014-1647-7.
8. Callera G.E., He Y., Yogi A., Montezano A.C., Paravicini T., Yao G., Touyz R.M. Regulation of the novel Mg2+ transporter transient receptor potential melastatin 7 (TRPM7) cation channel by bradykinin in vascular smooth muscle cells. J. Hypertens. 2009, 27(1):155-166.
9. Chen H.C., Su L.T., Gonzalez-Pagan O., Overton J.D., Runnels L.W. A key role for Mg(2+) in TRPM7s control of ROS levels during cell stress. Biochem. J. 2012, 445(3):441-448.
10. Chen H.C., Xie J., Zhang Z., Su L.T., Yue L., Runnels L.W. Blockade of TRPM7 channel activity and cell death by inhibitors of 5-lipoxygenase. PLoS ONE 2010, 5(6). e11161.
11. Chen J.P., Luan Y., You C.X., Chen X.H., Luo R.C., Li R. TRPM7 regulates the migration of human nasopharyngeal carcinoma cell by mediating Ca(2+) influx. Cell Calcium 2010, 47(5):425-432.
12. 2+ and pH sensitivity of human TRPM7 channels. Am. J. Physiol. Cell Physiol. 2012, 302(7):C1004-C1011.
13. Chubanov V., Mederos Y.S., Meissner M., Schafer S., Abstiens K., Hofmann T., Gudermann T. Natural and synthetic modulators of SK (K(ca) 2) potassium channels inhibit magnesium-dependent activity of the kinase-coupled cation channel TRPM7. Br. J. Pharmacol. 2012, 166(4):1357-1376.
14. Chubanov V., Waldegger S., Schnitzler M., Vitzthum H., Sassen M.C., Seyberth H.W., Konrad M., Gudermann T. 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(9):2894-2899.
15. Clapham D.E. TRP channels as cellular sensors. Nature 2003, 426(6966):517-524.
16. Clapham D.E., Julius D., Montell C., Schultz G. International Union of Pharmacology. XLIX. Nomenclature and structure-function relationships of transient receptor potential channels. Pharmacol. Rev. 2005, 57(4):427-450.
17. Clark K., Langeslag M., van Leeuwen B., Ran L., Ryazanov A.G., Figdor C.G., Moolenaar W.H., Jalink K., van Leeuwen F.N. TRPM7, a novel regulator of actomyosin contractility and cell adhesion. EMBO J. 2006, 25(2):290-301.
18. Clark K., Middelbeek J., Dorovkov M.V., Figdor C.G., Ryazanov A.G., Lasonder E., van Leeuwen F.N. The alpha-kinases TRPM6 and TRPM7, but not eEF-2 kinase, phosphorylate the assembly domain of myosin IIA, IIB and IIC. FEBS Lett. 2008, 582(20):2993-2997.
19. Clark K., Middelbeek J., Lasonder E., Dulyaninova N.G., Morrice N.A., Ryazanov A.G., Bresnick A.R., Figdor C.G., van Leeuwen F.N. TRPM7 regulates myosin IIA filament stability and protein localization by heavy chain phosphorylation. J. Mol. Biol. 2008, 378(4):790-803.
20. Clark K., Middelbeek J., Morrice N.A., Figdor C.G., Lasonder E., van Leeuwen F.N. Massive autophosphorylation of the Ser/Thr-rich domain controls protein kinase activity of TRPM6 and TRPM7. PLoS ONE 2008, 3(3). e1876.
21. Coombes E., Jiang J., Chu X.P., Inoue K., Seeds J., Branigan D., Simon R.P., Xiong Z.G. Pathophysiologically relevant levels of hydrogen peroxide induce glutamate-independent neurodegeneration that involves activation of transient receptor potential melastatin 7 channels. Antioxid. Redox Signal. 2011, 14(10):1815-1827.
22. Cosens D.J., Manning A. Abnormal electroretinogram from a Drosophila mutant. Nature 1969, 224(5216):285-287.
23. Crawley S.W., Cote G.P. Identification of dimer interactions required for the catalytic activity of the TRPM7 alpha-kinase domain. Biochem. J. 2009, 420(1):115-122.
24. Dai Q., Shrubsole M.J., Ness R.M., Schlundt D., Cai Q., Smalley W.E., Li M., Shyr Y., Zheng W. The relation of magnesium and calcium intakes and a genetic polymorphism in the magnesium transporter to colorectal neoplasia risk. Am. J. Clin. Nutr. 2007, 86(3):743-751.
25. Damann N., Voets T., Nilius B. TRPs in our senses. Curr. Biol. 2008, 18(18):R880-R889.
26. Davis F.M., Azimi I., Faville R.A., Peters A.A., Jalink K., Putney J.W., Goodhill G.J., Thompson E.W., Roberts-Thomson S.J., Monteith G.R. Induction of epithelial-mesenchymal transition (EMT) in breast cancer cells is calcium signal dependent. Oncogene 2013, 33:2307-2316.
27. 2+ uptake in cells lacking the channel-kinase TRPM7. FEBS Lett. 2011, 585(14):2275-2278.
28. Deason-Towne F., Perraud A.L., Schmitz C. Identification of Ser/Thr phosphorylation sites in the C2-domain of phospholipase C gamma2 (PLCgamma2) using TRPM7-kinase. Cell Signal. 2012, 24(11):2070-2075.
29. Demeuse P., Penner R., Fleig A. TRPM7 channel is regulated by magnesium nucleotides via its kinase domain. J. Gen. Physiol. 2006, 127(4):421-434.
30. Desai B.N., Krapivinsky G., Navarro B., Krapivinsky L., Carter B.C., Febvay S., Delling M., Penumaka A., Ramsey I.S., Manasian Y., Clapham D.E. Cleavage of TRPM7 releases the kinase domain from the ion channel and regulates its participation in Fas-induced apoptosis. Dev. Cell 2012, 22(6):1149-1162.
31. Dhennin-Duthille I., Gautier M., Faouzi M., Guilbert A., Brevet M., Vaudry D., Ahidouch A., Sevestre H., Ouadid-Ahidouch H. High expression of transient receptor potential channels in human breast cancer epithelial cells and tissues: correlation with pathological parameters. Cell Physiol. Biochem. 2011, 28(5):813-822.
32. Dorovkov M.V., Beznosov S.N., Shah S., Kotlianskaia L., Kostiukova A.S. Effect of mutations imitating the phosphorylation by TRPM7 kinase on the function of the N-terminal domain of tropomodulin. Biofizika 2008, 53(6):943-949.
33. Dorovkov M.V., Kostyukova A.S., Ryazanov A.G. Phosphorylation of annexin A1 by TRPM7 kinase: a switch regulating the induction of an alpha-helix. Biochemistry 2011, 50(12):2187-2193.
34. Dorovkov M.V., Ryazanov A.G. Phosphorylation of annexin I by TRPM7 channel-kinase. J. Biol. Chem. 2004, 279(49):50643-50646.
35. 2+ signals confer fibrogenesis in human atrial fibrillation. Circ. Res. 2010, 106(5):992-1003.
36. Elizondo M.R., Arduini B.L., Paulsen J., MacDonald E.L., Sabel J.L., Henion P.D., Cornell R.A., Parichy D.M. Defective skeletogenesis with kidney stone formation in dwarf zebrafish mutant for trpm7. Curr. Biol. 2005, 15(7):667-671.
37. Fonfria E., Murdock P.R., Cusdin F.S., Benham C.D., Kelsell R.E., McNulty S. Tissue distribution profiles of the human TRPM cation channel family. J. Recept. Signal Transduct. Res. 2006, 26(3):159-178.
38. Gao H., Chen X., Du X., Guan B., Liu Y., Zhang H. EGF enhances the migration of cancer cells by up-regulation of TRPM7. Cell Calcium 2011, 50(6):559-568.
39. 2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 2005, 6(6):449-461.
40. Guilbert A., Gautier M., Dhennin-Duthille I., Haren N., Sevestre H., Ouadid-Ahidouch H. Evidence that TRPM7 is required for breast cancer cell proliferation. Am. J. Physiol. Cell Physiol. 2009, 297(3):C493-C502.
41. Guilbert A., Gautier M., Dhennin-Duthille I., Rybarczyk P., Sahni J., Sevestre H., Scharenberg A.M., Ouadid-Ahidouch H. Transient receptor potential melastatin 7 is involved in oestrogen receptor-negative metastatic breast cancer cells migration through its kinase domain. Eur. J. Cancer 2013, 49(17):3694-3707.
42. Gwanyanya A., Sipido K.R., 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(4):C627-C635.
43. Hanano T., Hara Y., Shi J., Morita H., Umebayashi C., Mori E., Sumimoto H., Ito Y., Mori Y., Inoue R. Involvement of TRPM7 in cell growth as a spontaneously activated Ca2+ entry pathway in human retinoblastoma cells. J. Pharmacol. Sci. 2004, 95(4):403-419.
44. Hara K., Kokubo Y., Ishiura H., Fukuda Y., Miyashita A., Kuwano R., Sasaki R., Goto J., Nishizawa M., Kuzuhara S., Tsuji S. TRPM7 is not associated with amyotrophic lateral sclerosis-parkinsonism dementia complex in the Kii peninsula of Japan. Am. J. Med. Genet. B: Neuropsychiatr. Genet. 2010, 153B(1):310-313.
45. Hayes M.J., Rescher U., Gerke V., Moss S.E. Annexin-actin interactions. Traffic 2004, 5(8):571-576.
46. He Y., Yao G., Savoia C., Touyz R.M. Transient receptor potential melastatin 7 ion channels regulate magnesium homeostasis in vascular smooth muscle cells: role of angiotensin II. Circ. Res. 2005, 96(2):207-215.
47. Hermosura M.C., Nayakanti H., Dorovkov M.V., Calderon F.R., Ryazanov A.G., Haymer D.S., Garruto R.M. A TRPM7 variant shows altered sensitivity to magnesium that may contribute to the pathogenesis of two Guamanian neurodegenerative disorders. Proc. Natl. Acad. Sci. U.S.A. 2005, 102(32):11510-11515.
48. Hofmann T., Schafer S., Linseisen M., Sytik L., Gudermann T., Chubanov V. Activation of TRPM7 channels by small molecules under physiological conditions. Pflugers Arch. 2014, 166(4):1357-1376.
49. Inoue K., Branigan D., Xiong Z.G. Zinc-induced neurotoxicity mediated by transient receptor potential melastatin 7 channels. J. Biol. Chem. 2010, 285(10):7430-7439.
50. Inoue K., Xiong Z.G. Silencing TRPM7 promotes growth/proliferation and nitric oxide production of vascular endothelial cells via the ERK pathway. Cardiovasc. Res. 2009, 83(3):547-557.
51. Jeong S.Y., Shin S.Y., Kim H.S., Bae C.D., Uhm D.Y., Park M.K., Chung S. Regulation of magnesium-inhibited cation current by actin cytoskeleton rearrangement. Biochem. Biophys. Res. Commun. 2006, 339(3):810-815.
52. Jiang H., Tian S.L., Zeng Y., Li L.L., Shi J. TrkA pathway(s) is involved in regulation of TRPM7 expression in hippocampal neurons subjected to ischemic-reperfusion and oxygen-glucose deprivation. Brain Res. Bull. 2008, 76(1-2):124-130.
53. Jiang J., Li M., Yue L. Potentiation of TRPM7 inward currents by protons. J. Gen. Physiol. 2005, 126(2):137-150.
54. Jiang J., Li M.H., Inoue K., Chu X.P., Seeds J., Xiong Z.G. Transient receptor potential melastatin 7-like current in human head and neck carcinoma cells: role in cell proliferation. Cancer Res. 2007, 67(22):10929-10938.
55. 2+ homeostasis. Science 2008, 322(5902):756-760.
56. Jin J., Wu L.J., Jun J., Cheng X., Xu H., Andrews N.C., Clapham D.E. The channel kinase, TRPM7, is required for early embryonic development. Proc. Natl. Acad. Sci. U.S.A. 2012, 109(5):E225-E233.
57. Kaneko Y., Szallasi A. Transient receptor potential (TRP) channels: a clinical perspective. Br. J. Pharmacol. 2014, 171(10):2474-2507.
58. Kim B.J., Lim H.H., Yang D.K., Jun J.Y., Chang I.Y., Park C.S., So I., Stanfield P.R., Kim K.W. Melastatin-type transient receptor potential channel 7 is required for intestinal pacemaking activity. Gastroenterology 2005, 129(5):1504-1517.
59. Kim B.J., Park E.J., Lee J.H., Jeon J.H., Kim S.J., So I. Suppression of transient receptor potential melastatin 7 channel induces cell death in gastric cancer. Cancer Sci. 2008, 99(12):2502-2509.
60. Kim B.J., Nah S.Y., Jeon J.H., So I., Kim S.J. Transient receptor potential melastatin 7 channels are involved in ginsenoside Rg3-induced apoptosis in gastric cancer cells. Basic Clin. Pharmacol. Toxicol. 2011, 109(4):233-239.
61. Kim B.J., Nam J.H., Kwon Y.K., So I., Kim S.J. The role of waixenicin a as transient receptor potential melastatin 7 blocker. Basic Clin. Pharmacol. Toxicol. 2013, 112(2):83-89.
62. Kozak J.A., Cahalan M.D. MIC channels are inhibited by internal divalent cations but not ATP. Biophys. J. 2003, 84(2 Pt 1):922-927.
63. Kozak J.A., Matsushita M., Nairn A.C., Cahalan M.D. 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(5):499-514.
64. Krapivinsky G., Krapivinsky L., Manasian Y., Clapham D.E. The TRPM7 chanzyme is cleaved to release a chromatin-modifying kinase. Cell 2014, 157(5):1061-1072.
65. Krapivinsky G., Mochida S., Krapivinsky L., Cibulsky S.M., Clapham D.E. The TRPM7 ion channel functions in cholinergic synaptic vesicles and affects transmitter release. Neuron 2006, 52(3):485-496.
66. Kuipers A.J., Middelbeek J., van Leeuwen F.N. Mechanoregulation of cytoskeletal dynamics by TRP channels. Eur. J. Cell Biol. 2012, 91(11-12):834-846.
67. Kuras Z., Yun Y.H., Chimote A.A., Neumeier L., Conforti L. KCa3.1 and TRPM7 channels at the uropod regulate migration of activated human T cells. PLOS ONE 2012, 7(8). e43859.
68. Landman N., Jeong S.Y., Shin S.Y., Voronov S.V., Serban G., Kang M.S., Park M.K., Di P.G., Chung S., Kim T.W. Presenilin mutations linked to familial Alzheimer's disease cause an imbalance in phosphatidylinositol 4,5-bisphosphate metabolism. Proc. Natl. Acad. Sci. U.S.A. 2006, 103(51):19524-19529.
69. Langeslag M., Clark K., Moolenaar W.H., van Leeuwen F.N., Jalink K. Activation of TRPM7 channels by phospholipase C-coupled receptor agonists. J. Biol. Chem. 2007, 282(1):232-239.
70. Li M., Du J., Jiang J., Ratzan W., Su L.T., Runnels L.W., Yue L. Molecular determinants of Mg2+ and Ca2+ permeability and pH sensitivity in TRPM6 and TRPM7. J. Biol. Chem. 2007, 282(35):25817-25830.
71. Liu W., Su L.T., Khadka D.K., Mezzacappa C., Komiya Y., Sato A., Habas R., Runnels L.W. TRPM7 regulates gastrulation during vertebrate embryogenesis. Dev. Biol. 2011, 350(2):348-357.
72. Low S.E., Amburgey K., Horstick E., Linsley J., Sprague S.M., Cui W.W., Zhou W., Hirata H., Saint-Amant L., Hume R.I., Kuwada J.Y. TRPM7 is required within zebrafish sensory neurons for the activation of touch-evoked escape behaviors. J. Neurosci. 2011, 31(32):11633-11644.
73. Macianskiene R., Gwanyanya A., Vereecke J., Mubagwa K. Inhibition of the magnesium-sensitive TRPM7-like channel in cardiac myocytes by nonhydrolysable GTP analogs: involvement of phosphoinositide metabolism. Cell Physiol. Biochem. 2008, 22(1-4):109-118.
74. Matsushita M., Kozak J.A., Shimizu Y., McLachlin D.T., Yamaguchi H., Wei F.Y., Tomizawa K., Matsui H., Chait B.T., Cahalan M.D., Nairn A.C. Channel function is dissociated from the intrinsic kinase activity and autophosphorylation of TRPM7/ChaK1. J. Biol. Chem. 2005, 280(21):20793-20803.
75. Middelbeek J., Clark K., Venselaar H., Huynen M.A., van Leeuwen F.N. The alpha-kinase family: an exceptional branch on the protein kinase tree. Cell Mol. Life Sci. 2010, 67(6):875-890.
76. Middelbeek J., Kuipers A.J., Henneman L., Visser D., Eidhof I., van Horssen R., Wieringa B., Canisius S.V., Zwart W., Wessels L.F., Sweep F.C., Bult P., Span P.N., van Leeuwen F.N., Jalink K. TRPM7 is required for breast tumor cell metastasis. Cancer Res. 2012, 72(16):4250-4261.
77. Montell C., Birnbaumer L., Flockerzi V., Bindels R.J., Bruford E.A., Caterina M.J., Clapham D.E., Harteneck C., Heller S., Julius D., Kojima I., Mori Y., Penner R., Prawitt D., Scharenberg A.M., Schultz G., Shimizu N., Zhu M.X. A unified nomenclature for the superfamily of TRP cation channels. Mol. Cell 2002, 9(2):229-231.
78. Montell C., Rubin G.M. Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 1989, 2(4):1313-1323.
79. Nadler M.J., Hermosura M.C., Inabe K., Perraud A.L., Zhu Q., Stokes A.J., Kurosaki T., Kinet J.P., Penner R., Scharenberg A.M., Fleig A. LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 2001, 411(6837):590-595.
80. Nilius B., Owsianik G. Transient receptor potential channelopathies. Pflugers Arch. 2010, 460(2):437-450.
81. Nilius B., Owsianik G. The transient receptor potential family of ion channels. Genome Biol. 2011, 12(3). 218.
82. Numata T., Shimizu T., Okada Y. Direct mechano-stress sensitivity of TRPM7 channel. Cell Physiol. Biochem. 2007, 19(1-4):1-8.
83. Numata T., Shimizu T., Okada Y. TRPM7 is a stretch- and swelling-activated cation channel involved in volume regulation in human epithelial cells. Am. J. Physiol. Cell Physiol. 2007, 292(1):C460-C467.
84. Nunez-Villena F., Becerra A., Echeverria C., Briceno N., Porras O., Armisen R., Varela D., Montorfano I., Sarmiento D., Simon F. Increased expression of the transient receptor potential melastatin 7 channel is critically involved in lipopolysaccharide-induced reactive oxygen species-mediated neuronal death. Antioxid. Redox Signal. 2011, 15(9):2425-2438.
85. Oancea E., Wolfe J.T., Clapham D.E. Functional TRPM7 channels accumulate at the plasma membrane in response to fluid flow. Circ. Res. 2006, 98(2):245-253.
86. Oh H.G., Chun Y.S., Kim Y., Youn S.H., Shin S., Park M.K., Kim T.W., Chung S. Modulation of transient receptor potential melastatin related 7 channel by presenilins. Dev. Neurobiol. 2012, 72(6):865-877.
87. Paravicini T.M., Yogi A., Mazur A., Touyz R.M. Dysregulation of vascular TRPM7 and annexin-1 is associated with endothelial dysfunction in inherited hypomagnesemia. Hypertension 2009, 53(2):423-429.
88. Parnas M., Peters M., Dadon D., Lev S., Vertkin I., Slutsky I., Minke B. Carvacrol is a novel inhibitor of Drosophila TRPL and mammalian TRPM7 channels. Cell Calcium 2009, 45(3):300-309.
89. Penner R., Fleig A. The Mg2+ and Mg(2+)-nucleotide-regulated channel-kinase TRPM7. Handb. Exp. Pharmacol. 2007, (179):313-328.
90. Prevarskaya N., Skryma R., Shuba Y. Calcium in tumour metastasis: new roles for known actors. Nat. Rev. Cancer 2011, 11(8):609-618.
91. Qin X., Yue Z., Sun B., Yang W., Xie J., Ni E., Feng Y., Mahmood R., Zhang Y., Yue L. Sphingosine and FTY720 are potent inhibitors of the transient receptor potential melastatin 7 (TRPM7) channels. Br. J. Pharmacol. 2013, 168(6):1294-1312.
92. Rohacs T., Nilius B. Regulation of transient receptor potential (TRP) channels by phosphoinositides. Pflugers Arch. 2007, 455(1):157-168.
93. Romani A.M. Cellular magnesium homeostasis. Arch. Biochem. Biophys. 2011, 512(1):1-23.
94. Romero J.R., Ridker P.M., Zee R.Y. Gene variation of the transient receptor potential cation channel, subfamily M, member 7 (TRPM7), and risk of incident ischemic stroke: prospective, nested, case-control study. Stroke 2009, 40(9):2965-2968.
95. Runnels L.W., Yue L., Clapham D.E. TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 2001, 291(5506):1043-1047.
96. Runnels L.W., Yue L., Clapham D.E. The TRPM7 channel is inactivated by PIP(2) hydrolysis. Nat. Cell Biol. 2002, 4(5):329-336.
97. Ryazanov A.G. Elongation factor-2 kinase and its newly discovered relatives. FEBS Lett. 2002, 514(1):26-29.
98. Ryazanova L.V., Dorovkov M.V., Ansari A., Ryazanov A.G. Characterization of the protein kinase activity of TRPM7/ChaK1, a protein kinase fused to the transient receptor potential ion channel. J. Biol. Chem. 2004, 279(5):3708-3716.
99. Ryazanova L.V., Pavur K.S., Petrov A.N., Dorovkov M.V., Ryazanov A.G. Novel type of signaling molecules: protein kinases covalently linked with ion channels. Mol. Biol. 2001, 35(2):271-283.
100. Ryazanova L.V., Rondon L.J., Zierler S., Hu Z., Galli J., Yamaguchi T.P., Mazur A., Fleig A., Ryazanov A.G. TRPM7 is essential for Mg(2+) homeostasis in mammals. Nat. Commun. 2010, 1. 109.
101. Rybarczyk P., Gautier M., Hague F., Dhennin-Duthille I., Chatelain D., Kerr-Conte J., Pattou F., Regimbeau J.M., Sevestre H., Ouadid-Ahidouch H. Transient receptor potential melastatin-related 7 channel is overexpressed in human pancreatic ductal adenocarcinomas and regulates human pancreatic cancer cell migration. Int. J. Cancer 2012, 131(6):E851-E861.
102. Sah R., Mesirca P., Mason X., Gibson W., Bates-Withers C., Van den Boogert M., Chaudhuri D., Pu W.T., Mangoni M.E., Clapham D.E. Timing of myocardial trpm7 deletion during cardiogenesis variably disrupts adult ventricular function, conduction, and repolarization. Circulation 2013, 128(2):101-114.
103. Sah R., Mesirca P., Van den Boogert M., Rosen J., Mably J., Mangoni M.E., Clapham D.E. Ion channel-kinase TRPM7 is required for maintaining cardiac automaticity. Proc. Natl. Acad. Sci. U.S.A. 2013, 110(32):E3037-E3046.
104. Sahni J., Tamura R., Sweet I.R., Scharenberg A.M. TRPM7 regulates quiescent/proliferative metabolic transitions in lymphocytes. Cell Cycle 2010, 9(17):3565-3574.
105. Schlingmann K.P., Weber S., Peters M., Niemann N.L., Vitzthum H., Klingel K., Kratz M., Haddad E., Ristoff E., Dinour D., Syrrou M., Nielsen S., Sassen M., Waldegger S., Seyberth H.W., Konrad M. Hypomagnesemia with secondary hypocalcemia is caused by mutations in TRPM6, a new member of the TRPM gene family. Nat. Genet. 2002, 31(2):166-170.
106. Schmitz C., Perraud A.L., Johnson C.O., Inabe K., Smith M.K., Penner R., Kurosaki T., Fleig A., Scharenberg A.M. Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7. Cell 2003, 114(2):191-200.
107. Sontia B., Montezano A.C., Paravicini T., Tabet F., Touyz R.M. Downregulation of renal TRPM7 and increased inflammation and fibrosis in aldosterone-infused mice: effects of magnesium. Hypertension 2008, 51(4):915-921.
108. Su L.T., Agapito M.A., Li M., Simonson W.T., Huttenlocher A., Habas R., Yue L., Runnels L.W. TRPM7 regulates cell adhesion by controlling the calcium-dependent protease calpain. J. Biol. Chem. 2006, 281(16):11260-11270.
109. Su L.T., Chen H.C., Gonzalez-Pagan O., Overton J.D., Xie J., Yue L., Runnels L.W. TRPM7 activates m-calpain by stress-dependent stimulation of p38 MAPK and c-Jun N-terminal kinase. J. Mol. Biol. 2010, 396(4):858-869.
110. Su L.T., Liu W., Chen H.C., Gonzalez-Pagan O., Habas R., Runnels L.W. TRPM7 regulates polarized cell movements. Biochem. J. 2011, 434(3):513-521.
111. Sun H.S., Jackson M.F., Martin L.J., Jansen K., Teves L., Cui H., Kiyonaka S., Mori Y., Jones M., Forder J.P., Golde T.E., Orser B.A., MacDonald J.F., Tymianski M. Suppression of hippocampal TRPM7 protein prevents delayed neuronal death in brain ischemia. Nat. Neurosci. 2009, 12(10):1300-1307.
112. 2+ ratio promotes proliferation of prostate cancer cells by activating TRPM7 channels. J. Biol. Chem. 2013, 288(1):255-263.
113. 2+-nucleotide-regulated MagNuM (TRPM7) currents. Cell Calcium 2007, 41(3):249-260.
114. Touyz R.M. Transient receptor potential melastatin 6 and 7 channels, magnesium transport, and vascular biology: implications in hypertension. Am. J. Physiol. Heart Circ. Physiol. 2008, 294(3):H1103-H1118.
115. Touyz R.M., He Y., Montezano A.C., Yao G., Chubanov V., Gudermann T., Callera G.E. Differential regulation of transient receptor potential melastatin 6 and 7 cation channels by ANG II in vascular smooth muscle cells from spontaneously hypertensive rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290(1):R73-R78.
116. van der Wijst J., Blanchard M.G., Woodroof H.I., Macartney T.J., Gourlay R., Hoenderop J.G., Bindels R.J., Alessi D.R. Kinase and channel activity of TRPM6 are co-ordinated by a dimerization motif and pocket interaction. Biochem. J. 2014, 460(2):165-175.
117. Van Rossum D.B., Patterson R.L., Sharma S., Barrow R.K., Kornberg M., Gill D.L., Snyder S.H. Phospholipase Cgamma1 controls surface expresion of TRPC3 through an intermolecular PH domain. Nature 2005, 434(7029):99-104.
118. Venkatachalam K., Montell C. TRP channels. Annu. Rev. Biochem. 2007, 76:387-417.
119. 2+ sparks and invadosome formation in neuroblastoma cells. Cell Calcium 2013, 54(6):404-415.
120. Walder R.Y., Landau D., Meyer P., Shalev H., Tsolia M., Borochowitz Z., Boettger M.B., Beck G.E., Englehardt R.K., Carmi R., Sheffield V.C. Mutation of TRPM6 causes familial hypomagnesemia with secondary hypocalcemia. Nat. Genet. 2002, 31(2):171-174.
121. Wei C., Wang X., Chen M., Ouyang K., Song L.S., Cheng H. Calcium flickers steer cell migration. Nature 2009, 457(7231):901-905.
122. Xie J., Sun B., Du J., Yang W., Chen H.C., Overton J.D., Runnels L.W., Yue L. Phosphatidylinositol 4,5-bisphosphate (PIP(2)) controls magnesium gatekeeper TRPM6 activity. Sci. Rep. 2011, 1. 146.
123. Yamaguchi H., Matsushita M., Nairn A.C., Kuriyan J. Crystal structure of the atypical protein kinase domain of a TRP channel with phosphotransferase activity. Mol. Cell 2001, 7(5):1047-1057.
124. Yamashiro S., Gokhin D.S., Kimura S., Nowak R.B., Fowler V.M. Tropomodulins: pointed-end capping proteins that regulate actin filament architecture in diverse cell types. Cytoskeleton (Hoboken) 2012, 69(6):337-370.
125. Yee N.S., Zhou W., Lee M., Yee R.K. Targeted silencing of TRPM7 ion channel induces replicative senescence and produces enhanced cytotoxicity with gemcitabine in pancreatic adenocarcinoma. Cancer Lett. 2012, 318(1):99-105.
126. 2+-sensitive Socs3a signaling in development and cancer. Dis. Model Mech. 2011, 4(2):240-254.
127. Yogi A., Callera G.E., Antunes T.T., Tostes R.C., Touyz R.M. Transient receptor potential melastatin 7 (TRPM7) cation channels, magnesium and the vascular system in hypertension. Circ. J. 2011, 75(2):237-245.
128. Yogi A., Callera G.E., Tostes R., Touyz R.M. Bradykinin regulates calpain and proinflammatory signaling through TRPM7-sensitive pathways in vascular smooth muscle cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296(2):R201-R207.
129. Zhang J., Zhao F., Zhao Y., Wang J., Pei L., Sun N., Shi J. Hypoxia induces an increase in intracellular magnesium via transient receptor potential melastatin 7 (TRPM7) channels in rat hippocampal neurons in vitro. J. Biol. Chem. 2011, 286(23):20194-20207.
130. Zhang Y., Zhou L., Zhang X., Bai J., Shi M., Zhao G. Ginsenoside-Rd attenuates TRPM7 and ASIC1a but promotes ASIC2a expression in rats after focal cerebral ischemia. Neurol. Sci. 2012, 33(5):1125-1131.
131. Zhang Z., Yu H., Huang J., Faouzi M., Schmitz C., Penner R., Fleig A. The TRPM6 kinase domain determines the Mg.ATP sensitivity of TRPM7/M6 heteromeric ion channels. J. Biol. Chem. 2014, 289(8):5217-5227.
132. Zierler S., Yao G., Zhang Z., Kuo W.C., Porzgen P., Penner R., Horgen F.D., Fleig A. Waixenicin A inhibits cell proliferation through magnesium-dependent block of transient receptor potential melastatin 7 (TRPM7) channels. J. Biol. Chem. 2011, 286(45):39328-39335.