Functional characterization of homo- and heteromeric channel kinases TRPM6 and TRPM7

Journal of General Physiology

Volumn 127, Issue 5, 2006, Pages 525-537

  Li, Mingjiang ^a,b   Jiang, Jianmin ^a,c   Yue, Lixia ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b RENMIN HOSPITAL OF WUHAN UNIVERSITY   (China)

^c SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRPM6 CHANNEL; TRPM7 CHANNEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONDUCTANCE; EMBRYO; HETEROLOGOUS EXPRESSION; HUMAN; HUMAN CELL; MUTANT; NONHUMAN; PH; STATISTICAL SIGNIFICANCE;

ANIMALS; BORON COMPOUNDS; CALCIUM; CELL LINE; CELL MEMBRANE PERMEABILITY; ELECTROPHYSIOLOGY; HOMEOSTASIS; HUMANS; HYDROGEN-ION CONCENTRATION; MACROMOLECULAR SUBSTANCES; MAGNESIUM; MEMBRANE POTENTIALS; MICE; MUTATION; PROTEIN KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRPM CATION CHANNELS;

EID: 33646140352     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200609502     Document Type: Article

References (62)

1. Aarts, M., K. Iihara, W.L. Wei, Z.G. Xiong, M. Arundine, W. Cerwinski, J.F. MacDonald, and M. Tymianski. 2003. A key role for TRPM7 channels in anoxic neuronal death. Cell. 115:863-877.
2. +-activated currents in hippocampal neurons. J. Biol. Chem. 279:18296-18305.
3. 2+-binding sites. Eur. J. Biochem. 269:3678-3687.
4. 2+ release. FASEB J. 16:1145-1150.
5. Braun, F.J., O. Aziz, and J.W. Putney Jr. 2003. 2- aminoethoxydiphenyl borane activates a novel calcium-permeable cation channel. Mol. Pharmacol. 63:1304-1311.
6. Chubanov, V., S. Waldegger, M. Mederos y Schnitzler, H. Vitzthum, M.C. Sassen, H.W. Seyberth, M. Konrad, and T. Gudermann. 2004. Disruption of TRPM6/TRPM7 complex formation by a mutation in the TRPM6 gene causes hypomagnesemia with secondary hypocalcemia. Proc. Natl. Acad. Sci. USA. 101:2894-2899.
7. Chubanov, V., Y.S.M. Mederos, J. Waring, A. Plank, and T. Gudermann. 2005. Emerging roles of TRPM6/TRPM7 channel kinase signal transduction complexes. Naunyn Schmiedebergs Arch. Pharmacol. 371:334-341.
8. Chung, M.K., H. Lee, A. Mizuno, M. Suzuki, and M.J. Caterina. 2004. 2-aminoethoxydiphenyl borate activates and sensitizes the heat-gated ion channel TRPV3. J. Neurosci. 24:5177-5182.
9. Chung, M.K., A.D. Guler, and M.J. Caterina. 2005. Biphasic currents evoked by chemical or thermal activation of the heat-gated ion channel, TRPV3. J. Biol. Chem. 280:15928-15941.
10. Clapham, D.E. 2003. TRP channels as cellular sensors. Nature. 426:517-524.
11. Durkin, J.T., R.E. Koeppe II, and O.S. Andersen. 1990. Energetics of gramicidin hybrid channel formation as a test for structural equivalence. Side-chain substitutions in the native sequence. J. Mol. Biol. 211:221-234.
12. Durkin, J.T., L.L. Providence, R.E. Koeppe II, and O.S. Andersen. 1993. Energetics of heterodimer formation among gramicidin analogues with an NH2-terminal addition or deletion. Consequences of missing a residue at the join in the channel. J. Mol. Biol. 231:1102-1121.
13. Elizondo, M.R., B.L. Arduini, J. Paulsen, E.L. MacDonald, J.L. Sabel, P.D. Henion, R.A. Cornell, and D.M. Parichy. 2005. Defective skeletogenesis with kidney stone formation in dwarf zebrafish mutant for trpm7. Curr. Biol. 15:667-671.
14. Fleig, A., and R. Penner. 2004. Emerging roles of TRPM channels. Novartis Found. Symp. 258:248-258.
15. 2+ entry pathway in human retinoblastoma cells. J. Pharmacol. Sci. 95:403-419.
16. Harteneck, C., T.D. Plant, and G. Schultz. 2000. From worm to man: three subfamilies of TRP channels. Trends Neurosci. 23:159-166.
17. Hermosura, M.C., H. Nayakanti, M.V. Dorovkov, F.R. Calderon, A.G. Ryazanov, D.S. Haymer, and R.M. Garruto. 2005. A TRPM7 variant shows altered sensitivity to magnesium that may contribute to the pathogenesis of two Guamanian neurodegenerative disorders. Proc. Natl. Acad. Sci. USA. 102:11510-11515.
18. Hille, B. 2003. Ion Channels of Excitable Membranes. Third edition. Sinauer Associates, Inc. Sunderland, MA. 471-502.
19. 2+ channels TRPV5 and TRPV6. EMBO J. 22:776-785.
20. Hu, H.Z., Q. Gu, C. Wang, C.K. Colton, J. Tang, M. Kinoshita-Kawada, L.Y. Lee, J.D. Wood, and M.X. Zhu. 2004. 2-aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3. J. Biol. Chem. 279:35741-35748.
21. Jiang, J., M. Li, and L. Yue. 2005. Potentiation of TRPM7 inward currents by protons. J. Gen. Physiol. 126:137-150.
22. Jordt, S.E., M. Tominaga, and D. Julius. 2000. Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc. Natl. Acad. Sci. USA. 97:8134-8139.
23. Kerschbaum, H.H., J.A. Kozak, and M.D. Cahalan. 2003. Polyvalent cations as permeant probes of MIC and TRPM7 pores. Biophys. J. 84:2293-2305.
24. Kozak, J.A., M. Matsushita, A.C. Nairn, and M.D. Cahalan. 2005. Charge screening by internal pH and polyvalent cations as a mechanism for activation, inhibition, and rundown of TRPM7/MIC channels. J. Gen. Physiol. 126:499-514.
25. Lemonnier, L., N. Prevarskaya, J. Mazurier, Y. Shuba, and R. Skryma. 2004. 2-APB inhibits volume-regulated anion channels independently from intracellular calcium signaling modulation. FEBS Lett. 556:121-126.
26. 2+-sensitive cation channels. J. Biol. Chem. 275:27799-27805.
27. Liu, D.T., G.R. Tibbs, and S.A. Siegelbaum. 1996. Subunit stoichiometry of cyclic nucleotide-gated channels and effects of subunit order on channel function. Neuron. 16:983-990.
28. Liu, D.T., G.R. Tibbs, P. Paoletti, and S.A. Siegelbaum. 1998. Constraining ligand-binding site stoichiometry suggests that a cyclic nucleotide-gated channel is composed of two functional dimers. Neuron. 21:235-248.
29. 2+ release. J. Biochem. (Tokyo). 122:498-505.
30. Matsushita, M., J.A. Kozak, Y. Shimizu, D.T. McLachlin, H. Yamaguchi, F.Y. Wei, K. Tomizawa, H. Matsui, B.T. Chait, M.D. Cahalan, and A.C. Nairn. 2005. Channel function is dissociated from the intrinsic kinase activity and autophosphorylation of TRPM7/CHAK1. J. Biol. Chem. 80:20793-20803.
31. Monteilh-Zoller, M.K., M.C. Hermosura, M.J. Nadler, A.M. Scharenberg, R. Penner, and A. Fleig. 2003. TRPM7 provides an ion channel mechanism for cellular entry of trace metal ions. J. Gen. Physiol. 121:49-60.
32. Montell, C. 2005. The TRP superfamily of cation channels. Sci. STKE. 2005:re3.
33. Nadler, M.J., M.C. Hermosura, K. Inabe, A.L. Perraud, Q. Zhu, A.J. Stokes, T. Kurosaki, J.P. Kinet, R. Penner, A.M. Scharenberg, and A. Fleig. 2001. LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature. 411:590-595.
34. Nilius, B., T. Voets, and J. Peters. 2005. TRP channels in disease. Sci. STKE. 2005:re8.
35. Owsianik, G., K. Talavera, T. Voets, and B. Nilius. 2005. Permeation and selectivity of TRP channels. Annu. Rev. Physiol. [Epub ahead of print]
36. 2+ channels by 2- aminoethyldiphenyl borate (2-APB) occurs independently of IP(3) receptors. J. Physiol. 536:3-19.
37. Reeh, P.W., and K.H. Steen. 1996. Tissue acidosis in nociception and pain. Prog. Brain Res. 113:143-151.
38. Runnels, L.W., L. Yue, and D.E. Clapham. 2001. TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science. 291:1043-1047.
39. Runnels, L.W., L. Yue, and D.E. Clapham. 2002. The TRPM7 channel is inactivated by PIP(2) hydrolysis. Nat. Cell Biol. 4:329-336.
40. Ryazanova, L.V., M.V. Dorovkov, A. Ansari, and A.G. Ryazanov. 2004. Characterization of the protein kinase activity of TRPM7/ChaK1, a protein kinase fused to TRP ion channel. J. Biol. Chem. 279:3708-3716.
41. Schlingmann, K.P., and T. Gudermann. 2005. A critical role of TRPM channel-kinase for human magnesium transport. J. Physiol. 566:301-308.
42. Schlingmann, K.P., S. Weber, M. Peters, L. Niemann Nejsum, H. Vitzthum, K. Klingel, M. Kratz, E. Haddad, E. Ristoff, D. Dinour, et al. 2002. Hypomagnesemia with secondary hypocalcemia is caused by mutations in TRPM6, a new member of the TRPM gene family. Nat. Genet. 31:166-170.
43. Schlingmann, K.P., M.C. Sassen, S. Weber, U. Pechmann, K. Kusch, L. Pelken, D. Lotan, M. Syrrou, J.J. Prebble, D.E.C. Cole, et al. 2005. Novel TRPM6 mutations in 21 families with primary hypomagnesemia and secondary hypocalcemia. J. Am. Soc. Nephrol. 16:3061-3069.
44. Schmitz, C., A.L. Perraud, C.O. Johnson, K. Inabe, M.K. Smith, R. Penner, T. Kurosaki, A. Fleig, and A.M. Scharenberg. 2003. Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7. Cell. 114:191-200.
45. Schmitz, C., A.L. Perraud, A. Fleig, and A.M. Scharenberg. 2004. Dual-function ion channel/protein kinases: novel components of vertebrate magnesium regulatory mechanisms. Pediatr. Res. 55:734-737.
46. Schmitz, C., M.V. Dorovkov, X. Zhao, B.J. Davenport, A.G. Ryazanov, and A.L. Perraud. 2005. The channel kinases TRPM6 and TRPM7 are functionally non-redundant. J. Biol. Chem. 280:37763-37771.
47. Strubing, C., G. Krapivinsky, L. Krapivinsky, and D.E. Clapham. 2001. TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron. 29:645-655.
48. Strubing, C., G. Krapivinsky, L. Krapivinsky, and D.E. Clapham. 2003. Formation of novel TRPC channels by complex subunit interactions in embryonic brain. J. Biol. Chem. 278:39014-39019.
49. Takezawa, R., C. Schmitz, P. Demeuse, A.M. Scharenberg, R. Penner, and A. Fleig. 2004. Receptor-mediated regulation of the TRPM7 channel through its endogenous protein kinase domain. Proc. Natl. Acad. Sci. USA. 101:6009-6014.
50. Voets, T., J. Prenen, A. Fleig, R. Vennekens, H. Watanabe, J.G. Hoenderop, R.J. Bindels, G. Droogmans, R. Penner, and B. Nilius. 2001. CaT1 and the calcium release-activated calcium channel manifest distinct pore properties. J. Biol. Chem. 276:47767-47770.
51. 2+ absorption. J. Biol. Chem. 279:19-25.
52. Walder, R.Y., D. Landau, P. Meyer, H. Shalev, M. Tsolia, Z. Borochowitz, M.B. Boettger, G.E. Beck, R.K. Englehardt, R. Carmi, and V.C. Sheffield. 2002. Mutation of TRPM6 causes familial hypomagnesemia with secondary hypocalcemia. Nat. Genet. 31:171-174.
53. Wang, R., J. Su, X. Wang, H. Piao, X. Zhang, C.Y. Adams, N. Cui, and C. Jiang. 2005. Subunit stoichiometry of the Kir1.1 channel in proton-dependent gating. J. Biol. Chem. 280:13433-13441.
54. Wicher, D., H.-J. Agricola, R. Schonherr, S.H. Heinemann, and C. Derst. 2005. TRPγ channels are inhibited by cAMP and contribute to pacemaking in neurosecretory insect neurons. J. Biol. Chem. 281:3227-3236.
55. 2+ stores in single pancreatic acinar cells of mouse. Mol. Pharmacol. 58:1368-1374.
56. Xu, S.Z., F. Zeng, G. Boulay, C. Grimm, C. Harteneck, and D.J. Beech. 2005. Block of TRPC5 channels by 2-aminoethoxydiphenyl borate: a differential, extracellular and voltage-dependent effect. Br. J. Pharmacol. 145:405-414.
57. Yermolaieva, O., A.S. Leonard, M.K. Schnizler, F.M. Abboud, and M.J. Welsh. 2004. Extracellular acidosis increases neuronal cell calcium by activating acid-sensing ion channel 1a. Proc. Natl. Acad. Sci. USA. 101:6752-6757.
58. Yue, L., J.L. Feng, Z. Wang, and S. Nattel. 2000. Effects of ambasilide, quinidine, flecainide and verapamil on ultra-rapid delayed rectifier potassium currents in canine atrial myocytes. Cardiovasc. Res. 46:151-161.
59. Yue, L., P. Melnyk, R. Gaspo, Z. Wang, and S. Nattel. 1999. Molecular mechanisms underlying ionic remodeling in a dog model of atrial fibrillation. Circ. Res. 84:776-784.
60. Yue, L., J.B. Peng, M.A. Hediger, and D.E. Clapham. 2001. CaT1 manifests the pore properties of the calcium-release-activated calcium channel. Nature. 410:705-709.
61. Yue, L., B. Navarro, D. Ren, A. Ramos, and D. Clapham. 2002. The cation selectivity filter of the bacterial sodium channel, NaChBac. J. Gen. Physiol. 120:845-853.
62. Zheng, J., and F.J. Sigworth. 1998. Intermediate conductances during deactivation of heteromultimeric Shaker potassium channels. J. Gen. Physiol. 112:457-474.