Structural and functional similarities of calcium homeostasis modulator 1 (CALHM1) ion channel with connexins, pannexins, and innexins

Journal of Biological Chemistry

Volumn 288, Issue 9, 2013, Pages 6140-6153

  Siebert, Adam P ^a   Ma, Zhongming ^a   Grevet, Jeremy D ^a   Demuro, Angelo ^a   Parker, Ian ^a   Foskett, J Kevin ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM HOMEOSTASIS; CHARGED MOLECULE; EXTRACELLULAR; FUNCTIONAL PROPERTIES; FUNCTIONAL SIMILARITY; HEXAMERS; ION CHANNEL; MEMBRANE ION CHANNELS; PORE DIAMETERS; PROTEIN FAMILY; STRUCTURAL SIMILARITY; TRANS-MEMBRANE DOMAINS;

ACTIVATION ANALYSIS; AMINO ACIDS; CELL MEMBRANES; PHYSIOLOGY; PROTEINS;

CALCIUM;

CALCIUM HOMEOSTASIS MODULATOR 1; CYSTEINE; GAP JUNCTION PROTEIN; INNEXIN; MEMBRANE PROTEIN; PANNEXIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; CYTOPLASM; FEMALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; STRUCTURAL HOMOLOGY; XENOPUS LAEVIS;

ANIMALS; CALCIUM CHANNELS; CELL LINE, TUMOR; CONNEXINS; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84874773135     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.409789     Document Type: Article

References (90)

1. Dreses-Werringloer, U., Lambert, J. C., Vingtdeux, V., Zhao, H., Vais, H., Siebert, A., Jain, A., Koppel, J., Rovelet-Lecrux, A., Hannequin, D., Pasquier, F., Galimberti, D., Scarpini, E., Mann, D., Lendon, C., Campion, D., Amouyel, P., Davies, P., Foskett, J. K., Campagne, F., and Marambaud, P. (2008) A polymorphism in CALHM1 influences Ca2+ homeostasis, Aβ levels, and Alzheimer's disease risk. Cell 133, 1149-1161
2. Lambert, J. C., and Amouyel, P. (2007) Genetic heterogeneity of Alzheimer's disease. Complexity and advances. Psychoneuroendocrinology 32, S62-S70
3. Ma, Z., Siebert, A. P., Cheung, K. H., Lee, R. J., Johnson, B., Cohen, A. S., Vingtdeux, V., Marambaud, P., and Foskett, J. K. (2012) Calcium homeostasis modulator 1 (CALHM1) is the pore-forming subunit of an ion channel that mediates extracellular Ca2+ regulation of neuronal excitability. Proc. Natl. Acad. Sci. U.S.A. 109, E1963-E1971
4. Gallego-Sandín, S., Alonso, M. T., and García-Sancho, J. (2011) Calcium homoeostasis modulator 1 (CALHM1) reduces the calcium content of the endoplasmic reticulum (ER) and triggers ER stress. Biochem. J. 437, 469-475
5. Moreno-Ortega, A. J., Ruíz-Nuño, A., García, A. G., and Cano-Abad, M. F. (2010) Mitochondria sense with different kinetics the calcium entering into HeLa cells through calcium channels CALHM1 and mutated P86LCALHM1. Biochem. Biophys. Res. Commun. 391, 722-726
6. Bahima, L., Aleu, J., Elias, M., Martín-Satué, M., Muhaisen, A., Blasi, J., Marsal, J., and Solsona, C. (2006) Endogenous hemichannels play a role in the release of ATP from Xenopus oocytes. J. Cell Physiol. 206, 95-102
7. Ebihara, L. (1996) Xenopus connexin38 forms hemi-gap-junctional channels in the nonjunctional plasma membrane of Xenopus oocytes. Biophys. J. 71, 742-748
8. Weber, W. (1999) Ion currents of Xenopus laevis oocytes. State of the art. Biochim. Biophys. Acta 1421, 213-233
9. Hille, B. (2001) Ion Channels of Excitable Membranes, 3rd Ed., Sinauer, Sunderland, MA
10. Hamer, W. J., and Wu, Y.-C. (1972) Osmotic coefficients and mean activity coefficients of univalent electrolytes in water at 25 °C. J. Phys. Chem. Ref. Data 1, 1047-1099
11. Adams, D. J., Dwyer, T. M., and Hille, B. (1980) The permeability of endplate channels to monovalent and divalent metal cations. J. Gen. Physiol. 75, 493-510
12. Dwyer, T. M., Adams, D. J., and Hille, B. (1980) The permeability of the endplate channel to organic cations in frog muscle. J. Gen. Physiol. 75, 469-492
13. Farris, H. E., LeBlanc, C. L., Goswami, J., and Ricci, A. J. (2004) Probing the pore of the auditory hair cell mechanotransducer channel in turtle. J. Physiol. 558, 769-792
14. Sun, Y. M., Favre, I., Schild, L., and Moczydlowski, E. (1997) On the structural basis for size-selective permeation of organic cations through the voltage-gated sodium channel. Effect of alanine mutations at the DEKA locus on selectivity, inhibition by Ca2+ and H+, and molecular sieving. J. Gen. Physiol. 110, 693-715
15. Penna, A., Demuro, A., Yeromin, A. V., Zhang, S. L., Safrina, O., Parker, I., and Cahalan, M. D. (2008) The CRAC channel consists of a tetramer formed by Stim-induced dimerization of Orai dimers. Nature 456, 116-120
16. Demuro, A., and Parker, I. (2005) Optical single-channel recording. Imaging Ca2+ flux through individual ion channels with high temporal and spatial resolution. J. Biomed. Opt. 10, 11002
17. Kerssemakers, J. W., Munteanu, E. L., Laan, L., Noetzel, T. L., Janson, M. E., and Dogterom, M. (2006) Assembly dynamics of microtubules at molecular resolution. Nature 442, 709-712
18. Demuro, A., Penna, A., Safrina, O., Yeromin, A. V., Amcheslavsky, A., Cahalan, M. D., and Parker, I. (2011) Subunit stoichiometry of human Orai1 and Orai3 channels in closed and open states. Proc. Natl. Acad. Sci. U.S.A. 108, 17832-17837
19. Ding, H., Wong, P. T., Lee, E. L., Gafni, A., and Steel, D. G. (2009) Determination of the oligomer size of amyloidogenic protein β-amyloid(1-40) by single-molecule spectroscopy. Biophys. J. 97, 912-921
20. Ji, W., Xu, P., Li, Z., Lu, J., Liu, L., Zhan, Y., Chen, Y., Hille, B., Xu, T., and Chen, L. (2008) Functional stoichiometry of the unitary calcium-releaseactivated calcium channel. Proc. Natl. Acad. Sci. U.S.A. 105, 13668-13673
21. Ulbrich, M. H., and Isacoff, E. Y. (2007) Subunit counting in membranebound proteins. Nat. Methods 4, 319-321
22. Nakajo, K., Ulbrich, M. H., Kubo, Y., and Isacoff, E. Y. (2010) Stoichiometry of the KCNQ1-KCNE1 ion channel complex. Proc. Natl. Acad. Sci. U.S.A. 107, 18862-18867
23. Yu, Y., Ulbrich, M. H., Li, M. H., Buraei, Z., Chen, X. Z., Ong, A. C., Tong, L., Isacoff, E. Y., and Yang, J. (2009) Structural and molecular basis of the assembly of the TRPP2/PKD1 complex. Proc. Natl. Acad. Sci. U.S.A. 106, 11558-11563
24. Sitaram, A., Piccirillo, R., Palmisano, I., Harper, D. C., Dell'Angelica, E. C., Schiaffino, M. V., and Marks, M. S. (2009) Localization to mature melanosomes by virtue of cytoplasmic dileucine motifs is required for human OCA2 function. Mol. Biol. Cell 20, 1464-1477
25. Hille, B. (1971) The permeability of the sodium channel to organic cations in myelinated nerve. J. Gen. Physiol. 58, 599-619
26. McCleskey, E. W., and Almers, W. (1985) The Ca channel in skeletal muscle is a large pore. Proc. Natl. Acad. Sci. U.S.A. 82, 7149-7153
27. Meuser, D., Splitt, H., Wagner, R., and Schrempf, H. (1999) Exploring the open pore of the potassium channel from Streptomyces lividans. FEBS Lett. 462, 447-452
28. Nishida, M., and MacKinnon, R. (2002) Structural basis of inward rectification. Cytoplasmic pore of theGprotein-gated inward rectifier GIRK1 at 1.8 Å resolution. Cell 111, 957-965
29. Maeda, S., Nakagawa, S., Suga, M., Yamashita, E., Oshima, A., Fujiyoshi, Y., and Tsukihara, T. (2009) Structure of the connexin 26 gap junction channel at 3.5 Å resolution. Nature 458, 597-602
30. Weber, P. A., Chang, H. C., Spaeth, K. E., Nitsche, J. M., and Nicholson, B. J. (2004) The permeability of gap junction channels to probes of different size is dependent on connexin composition and permeant-pore affinities. Biophys. J. 87, 958-973
31. Elfgang, C., Eckert, R., Lichtenberg-Fraté, H., Butterweck, A., Traub, O., Klein, R. A., Hülser, D. F., and Willecke, K. (1995) Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J. Cell Biol. 129, 805-817
32. Silverman, W., Locovei, S., and Dahl, G. (2008) Probenecid, a gout remedy, inhibits pannexin 1 channels. Am. J. Physiol. Cell Physiol. 295, C761-C767
33. Cruikshank, S. J., Hopperstad, M., Younger, M., Connors, B. W., Spray, D. C., and Srinivas, M. (2004) Potent block of Cx36 and Cx50 gap junction channels by mefloquine. Proc. Natl. Acad. Sci. U.S.A. 101, 12364-12369
34. Martinez-Wittinghan, F. J., Srinivas, M., Sellitto, C., White, T. W., and Mathias, R. T. (2006) Mefloquine effects on the lens suggest cooperative gating of gap junction channels. J. Membr. Biol. 211, 163-171
35. Srinivas, M., Hopperstad, M. G., and Spray, D. C. (2001) Quinine blocks specific gap junction channel subtypes. Proc. Natl. Acad. Sci. U.S.A. 98, 10942-10947
36. Maeda, S., and Tsukihara, T. (2011) Structure of the gap junction channel and its implications for its biological functions. Cell Mol. Life Sci. 68, 1115-1129
37. Schägger, H., Cramer, W. A., and von Jagow, G. (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by twodimensional native electrophoresis. Anal. Biochem. 217, 220-230
38. Schägger, H., and von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199, 223-231
39. Tombola, F., Ulbrich, M. H., and Isacoff, E. Y. (2008) The voltage-gated proton channel Hv1 has two pores, each controlled by one voltage sensor. Neuron 58, 546-556
40. Claros, M. G., and von Heijne, G. (1994) TopPred II. An improved software for membrane protein structure predictions. Comput. Appl. Biosci. 10, 685-686
41. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E. L. (2001) Predicting transmembrane protein topology with a hidden Markov model. Application to complete genomes. J. Mol. Biol. 305, 567-580
42. Rost, B., Fariselli, P., and Casadio, R. (1996) Topology prediction for helical transmembrane proteins at 86% accuracy. Protein Sci. 5, 1704-1718
43. Sonnhammer, E. L., von Heijne, G., and Krogh, A. (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 6, 175-182
44. Tusnády, G. E., and Simon, I. (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849-850
45. von Heijne, G. (1992) Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J. Mol. Biol. 225, 487-494
46. Common, J. E., Becker, D., Di, W. L., Leigh, I. M., O'Toole, E. A., and Kelsell, D. P. (2002) Functional studies of human skin disease- and deafness- associated connexin 30 mutations. Biochem. Biophys. Res. Commun. 298, 651-656
47. Beblo, D. A., and Veenstra, R. D. (1997) Monovalent cation permeation through the connexin40 gap junction channel. Cs, Rb, K, Na, Li, TEA, TMA, TBA, and effects of anions Br, Cl, F, acetate, aspartate, glutamate, and NO3. J. Gen. Physiol. 109, 509-522
48. Wang, H. Z., and Veenstra, R. D. (1997) Monovalent ion selectivity sequences of the rat connexin43 gap junction channel. J. Gen. Physiol. 109, 491-507
49. Dani, J. A. (1989) Open channel structure and ion binding sites of the nicotinic acetylcholine receptor channel. J. Neurosci. 9, 884-892
50. Zarei, M. M., and Dani, J. A. (1995) Structural basis for explaining openchannel blockade of the NMDA receptor. J. Neurosci. 15, 1446-1454
51. Yamashita, M., Navarro-Borelly, L., McNally, B. A., and Prakriya, M. (2007) Orai1 mutations alter ion permeation and Ca2+-dependent fast inactivation of CRAC channels. Evidence for coupling of permeation and gating. J. Gen. Physiol. 130, 525-540
52. Schindl, R., Bergsmann, J., Frischauf, I., Derler, I., Fahrner, M., Muik, M., Fritsch, R., Groschner, K., and Romanin, C. (2008) 2-Aminoethoxydiphenyl borate alters selectivity of Orai3 channels by increasing their pore size. J. Biol. Chem. 283, 20261-20267
53. Bezanilla, F., and Armstrong, C. M. (1972) Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axons. J. Gen. Physiol. 60, 588-608
54. Balasubramanian, S., Lynch, J. W., and Barry, P. H. (1995) The permeation of organic cations through cAMP-gated channels in mammalian olfactory receptor neurons. J. Membr. Biol. 146, 177-191
55. Oh, S., Ri, Y., Bennett, M. V., Trexler, E. B., Verselis, V. K., and Bargiello, T. A. (1997) Changes in permeability caused by connexin 32 mutations underlie X-linked Charcot-Marie-Tooth disease. Neuron 19, 927-938
56. Ambrosi, C., Gassmann, O., Pranskevich, J. N., Boassa, D., Smock, A., Wang, J., Dahl, G., Steinem, C., and Sosinsky, G. E. (2010) Pannexin1 and Pannexin2 channels show quaternary similarities to connexons and different oligomerization numbers from each other. J. Biol. Chem. 285, 24420-24431
57. Harris, A. L. (2007) Connexin channel permeability to cytoplasmic molecules. Prog. Biophys. Mol. Biol. 94, 120-143
58. Das, S. K., Darshi, M., Cheley, S., Wallace, M. I., and Bayley, H. (2007) Membrane protein stoichiometry determined from the step-wise photobleaching of dye-labelled subunits. Chembiochem 8, 994-999
59. Panchin, Y., Kelmanson, I., Matz, M., Lukyanov, K., Usman, N., and Lukyanov, S. (2000) A ubiquitous family of putative gap junction molecules. Curr. Biol. 10, R473-R474
60. Fushiki, D., Hamada, Y., Yoshimura, R., and Endo, Y. (2010) Phylogenetic and bioinformatic analysis of gap junction-related proteins, innexins, pannexins and connexins. Biomed. Res. 31, 133-142
61. Phelan, P., Bacon, J. P., Davies, J. A., Stebbings, L. A., Todman, M. G., Avery, L., Baines, R. A., Barnes, T. M., Ford, C., Hekimi, S., Lee, R., Shaw, J. E., Starich, T. A., Curtin, K. D., Sun, Y. A., and Wyman, R. J. (1998) Innexins. A family of invertebrate gap-junction proteins. Trends Genet. 14, 348-349
62. Barnes, T. M. (1994) OPUS. A growing family of gap junction proteins? Trends Genet. 10, 303-305
63. Starich, T. A., Lee, R. Y., Panzarella, C., Avery, L., and Shaw, J. E. (1996) eat-5 and unc-7 represent a multigene family in Caenorhabditis elegans involved in cell-cell coupling. J. Cell Biol. 134, 537-548
64. Landesman, Y., White, T. W., Starich, T. A., Shaw, J. E., Goodenough, D. A., and Paul, D. L. (1999) J. Cell Sci. 112, 2391-2396
65. Bruzzone, R., White, T. W., and Paul, D. L. (1996) Connections with connexins. The molecular basis of direct intercellular signaling. Eur. J. Biochem. 238, 1-27
66. White, T. W., Deans, M. R., O'Brien, J., Al-Ubaidi, M. R., Goodenough, D. A., Ripps, H., and Bruzzone, R. (1999) Functional characteristics of skate connexin35, a member of the γ subfamily of connexins expressed in the vertebrate retina. Eur. J. Neurosci. 11, 1883-1890
67. Baranova, A., Ivanov, D., Petrash, N., Pestova, A., Skoblov, M., Kelmanson, I., Shagin, D., Nazarenko, S., Geraymovych, E., Litvin, O., Tiunova, A., Born, T. L., Usman, N., Staroverov, D., Lukyanov, S., and Panchin, Y. (2004) The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 83, 706-716
68. Yen, M. R., and Saier, M. H., Jr. (2007) Gap junctional proteins of animals. The innexin/pannexin superfamily. Prog. Biophys. Mol. Biol. 94, 5-14
69. Sosinsky, G. E., Boassa, D., Dermietzel, R., Duffy, H. S., Laird, D. W., MacVicar, B., Naus, C. C., Penuela, S., Scemes, E., Spray, D. C., Thompson, R. J., Zhao, H. B., and Dahl, G. (2011) Pannexin channels are not gap junction hemichannels. Channels 5, 193-197
70. Boassa, D., Ambrosi, C., Qiu, F., Dahl, G., Gaietta, G., and Sosinsky, G. (2007) Pannexin1 channels contain a glycosylation site that targets the hexamer to the plasma membrane. J. Biol. Chem. 282, 31733-31743
71. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) ClustalW and ClustalX version 2.0. Bioinformatics 23, 2947-2948
72. Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J., and Lopez, R. (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res. 38, W695-W699
73. Pei, J., and Grishin, N. V. (2007) PROMALS. Towards accurate multiple sequence alignments of distantly related proteins. Bioinformatics 23, 802-808
74. Barbe, M. T., Monyer, H., and Bruzzone, R. (2006) Cell-cell communication beyond connexins. The pannexin channels. Physiology 21, 103-114
75. Hua, V. B., Chang, A. B., Tchieu, J. H., Kumar, N. M., Nielsen, P. A., and Saier, M. H., Jr. (2003) Sequence and phylogenetic analyses of 4 TMS junctional proteins of animals. Connexins, innexins, claudins and occludins. J. Membr. Biol. 194, 59-76
76. Penuela, S., Bhalla, R., Gong, X. Q., Cowan, K. N., Celetti, S. J., Cowan, B. J., Bai, D., Shao, Q., and Laird, D. W. (2007) Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins. J. Cell Sci. 120, 3772-3783
77. Boassa, D., Qiu, F., Dahl, G., and Sosinsky, G. (2008) Trafficking dynamics of glycosylated pannexin 1 proteins. Cell Commun. Adhes. 15, 119-132
78. Dahl, G., Nonner, W., and Werner, R. (1994) Attempts to define functional domains of gap junction proteins with synthetic peptides. Biophys. J. 67, 1816-1822
79. Srinivas, M., Calderon, D. P., Kronengold, J., and Verselis, V. K. (2006) Regulation of connexin hemichannels by monovalent cations. J. Gen. Physiol. 127, 67-75
80. Verselis, V. K., and Srinivas, M. (2008) Divalent cations regulate connexin hemichannels by modulating intrinsic voltage-dependent gating. J. Gen. Physiol. 132, 315-327
81. Ebihara, L. (2003) New roles for connexons. News Physiol. Sci. 18, 100-103
82. Bao, L., Locovei, S., and Dahl, G. (2004) Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett. 572, 65-68
83. Bruzzone, R., Barbe, M. T., Jakob, N. J., and Monyer, H. (2005) Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J. Neurochem. 92, 1033-1043
84. Bruzzone, R., Hormuzdi, S. G., Barbe, M. T., Herb, A., and Monyer, H. (2003) Pannexins, a family of gap junction proteins expressed in brain. Proc. Natl. Acad. Sci. U.S.A. 100, 13644-13649
85. Locovei, S., Wang, J., and Dahl, G. (2006) Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett. 580, 239-244
86. Eskandari, S., Zampighi, G. A., Leung, D. W., Wright, E. M., and Loo, D. D. (2002) Inhibition of gap junction hemichannels by chloride channel blockers. J. Membr. Biol. 185, 93-102
87. Qiu, F., and Dahl, G. (2009) A permeant regulating its permeation pore. Inhibition of pannexin 1 channels by ATP. Am. J. Physiol. Cell Physiol. 296, C250-C255
88. Shestopalov, V. I., and Panchin, Y. (2008) Pannexins and gap junction protein diversity. Cell Mol. Life Sci. 65, 376-394
89. Veenstra, R. D., Wang, H. Z., Beyer, E. C., Ramanan, S. V., and Brink, P. R. (1994) Connexin37 forms high conductance gap junction channels with subconductance state activity and selective dye and ionic permeabilities. Biophys. J. 66, 1915-1928
90. Nightingale, E. R., Jr. (1959) Phenomenological theory of ion solvation. Effective radii of hydrated ions. J. Phys. Chem. 63, 1381-1387