Mitochondrial organization and Ca 2+ uptake

Biochemical Society Transactions

Volumn 40, Issue 1, 2012, Pages 158-167

  Olson, Marnie L ^a   Chalmers, Susan ^a   McCarron, John G ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

Calcium uptake; Local calcium signalling; Mitochondrion; Store organization; Tether

Indexed keywords

CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE; CELL ORGANELLE; CELL TYPE; CYTOPLASM; CYTOSOL; MITOCHONDRION; PRIORITY JOURNAL; REVIEW; SMOOTH MUSCLE FIBER; ANIMAL; ENDOPLASMIC RETICULUM; HUMAN; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; PHYSIOLOGY;

CALCIUM; CATION TRANSPORT PROTEIN;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CATION TRANSPORT PROTEINS; ENDOPLASMIC RETICULUM; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA;

EID: 84856264104     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20110705     Document Type: Review

References (95)

1. Deluca, H.F. and Engstrom, G.W. (1961) Calcium uptake by rat kidney mitochondria. Proc. Natl. Acad. Sci. U.S.A. 47, 1744-1750
2. 2+ ion uptake by rat kidney mitochondria and its dependence on respiration and phosphorylation. J. Biol. Chem. 237, 2670-2677
3. Gunter, T.E. and Pfeiffer, D.R. (1990) Mechanisms by which mitochondria transport calcium. Am. J. Physiol. 258, C755-C786 (Pubitemid 20179411)
4. Nicholls, D.G. and Chalmers, S. (2004) The integration of mitochondrial calcium transport and storage. J. Bioenerg. Biomembr. 36, 277-281 (Pubitemid 39619826)
5. Chalmers, S., Olson, M.L., MacMillan, D., Rainbow, R.D. and McCarron, J.G. (2007) Ion channels in smooth muscle: regulation by the sarcoplasmic reticulum and mitochondria. Cell Calcium 42, 447-466 (Pubitemid 47264012)
6. Kirichok, Y., Krapivinsky, G. and Clapham, D.E. (2004) The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427, 360-364 (Pubitemid 38133664)
7. Saris, N.E. and Carafoli, E. (2005) A historical review of cellular calcium handling, with emphasis on mitochondria. Biochemistry (Moscow) 70, 187-194
8. Baughman, J.M., Perocchi, F., Girgis, H.S., Plovanich, M., Belcher-Timme, C.A., Sancak, Y., Bao, X.R., Strittmatter, L., Goldberger, O., Bogorad, R.L. et al. (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476, 341-345
9. De Stefani, D., Raffaello, A., Teardo, E., Szabo, I. and Rizzuto, R. (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476, 336-340
10. 2+ uptake. Nature 467, 291-296
11. +homeostasis with a potential role in the Wolf-Hirschhorn syndrome. J. Biol. Chem. 279, 30307-30315
12. + exchange. J. Biol. Chem. 285, 14399-14414
13. + antiporter. Science 326, 144-147
14. Trenker, M., Malli, R., Fertschai, I., Levak-Frank, S. and Graier, W.F. (2007) Uncoupling proteins 2 and 3 are fundamental for mitochondrial Ca2+uniport. Nat. Cell Biol. 9, 445-452 (Pubitemid 46511078)
15. Brookes, P.S., Parker, N., Buckingham, J.A., Vidal-Puig, A., Halestrap, A.P., Gunter, T.E., Nicholls, D.G., Bernardi, P., Lemasters, J.J. and Brand, M.D. (2008) UCPs: unlikely calcium porters. Nat. Cell Biol. 10, 1235-1237
16. Beutner, G., Sharma, V.K., Giovannucci, D.R., Yule, D.I. and Sheu, S.S. (2001) Identification of a ryanodine receptor in rat heart mitochondria. J. Biol. Chem. 276, 21482-21488
17. Ryu, S.Y., Beutner, G., Kinnally, K.W., Dirksen, R.T. and Sheu, S.S. (2011) Single channel characterization of the mitochondrial ryanodine receptor in heart mitoplasts. J. Biol. Chem. 286, 21324-21329
18. Salnikov, V., Lukyanenko, Y.O., Lederer, W.J. and Lukyanenko, V. (2009) Distribution of ryanodine receptors in rat ventricular myocytes. J. Muscle Res. Cell Motil. 30, 161-170
19. Crompton, M., Capano, M. and Carafoli, E. (1976) Respiration-dependent efflux of magnesium ions from heart mitochondria. Biochem. J. 154, 735-742
20. 2+ transport mechanism in mitochondria. Biochemistry 15, 3834-3842
21. + antiport. J. Biol. Chem. 254, 6236-6239
22. 2+ exchange. Proc. Natl. Acad. Sci. U.S.A. 107, 436-441
23. Zoratti, M., Szabo, I. and De Marchi, U. (2005) Mitochondrial permeability transitions: how many doors to the house? Biochim. Biophys. Acta 1706, 40-52 (Pubitemid 40037759)
24. 2+ uptake by cardiac mitochondria. J. Gen. Physiol. 62, 756-772
25. Csordas, G., Thomas, A.P. and Hajnoczky, G. (1999) Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria. EMBO J. 18, 96-108 (Pubitemid 29005027)
26. 3-sensitive channels that are sensed by neighboring mitochondria. Science 262, 744-747
27. Szalai, G., Csordas, G., Hantash, B.M., Thomas, A.P. and Hajnoczky, G. (2000) Calcium signal transmission between ryanodine receptors and mitochondria. J. Biol. Chem. 275, 15305-15313 (Pubitemid 30337257)
28. 2+ channels. Mol. Cell 38, 280-290
29. 2+ transfer between sarcoplasmic reticulum subdomains and the mitochondria in heart muscle. J. Biol. Chem. 283, 32771-32780
30. Nixon, G.F., Mignery, G.A. and Somlyo, A.V. (1994) Immunogold localization of inositol 1,4,5-trisphosphate receptors and characterization of ultrastructural features of the sarcoplasmic reticulum in phasic and tonic smooth muscle. J. Muscle Res. Cell Motil. 15, 682-700
31. 2+ from sarcoplasmic reticulum to mitochondria in rat ventricular myocytes. J. Bioenerg. Biomembr. 32, 97-104
32. Dai, J., Kuo, K.H., Leo, J.M., van Breemen, C. and Lee, C.H. (2005) Rearrangement of the close contact between the mitochondria and the sarcoplasmic reticulum in airway smooth muscle. Cell Calcium 37, 333-340 (Pubitemid 40331451)
33. Tong, W.C., Sweeney, M., Jones, C.J., Zhang, H., O'Neill, S.C., Prior, I. and Taggart, M.J. (2009) Three-dimensional electron microscopic reconstruction of intracellular organellar arrangements in vascular smooth muscle: further evidence of nanospaces and contacts. J. Cell Mol. Med. 13, 995-998
34. Csordas, G., Renken, C., Varnai, P., Walter, L., Weaver, D., Buttle, K.F., Balla, T., Mannella, C.A. and Hajnoczky, G. (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 174, 915-921 (Pubitemid 44455180)
35. 2+ transients in smooth muscle. FASEB J. 17, 28-37
36. Boncompagni, S., Rossi, A.E., Micaroni, M., Beznoussenko, G.V., Polishchuk, R.S., Dirksen, R.T. and Protasi, F. (2009) Mitochondria are linked to calcium stores in striated muscle by developmentally regulated tethering structures. Mol. Biol. Cell 20, 1058-1067
37. Simmen, T., Aslan, J.E., Blagoveshchenskaya, A.D., Thomas, L., Wan, L., Xiang, Y., Feliciangeli, S.F., Hung, C.H., Crump, C.M. and Thomas, G. (2005) PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis. EMBO J. 24, 717-729 (Pubitemid 40396102)
38. de Brito, O.M. and Scorrano, L. (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605-610
39. Kornmann, B., Currie, E., Collins, S.R., Schuldiner, M., Nunnari, J., Weissman, J.S. and Walter, P. (2009) An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325, 477-481
40. 2+ signaling and cell survival. Cell 131, 596-610
41. Szabadkai, G., Bianchi, K., Varnai, P., De Stefani, D., Wieckowski, M.R., Cavagna, D., Nagy, A.I., Balla, T. and Rizzuto, R. (2006) Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J. Cell Biol. 175, 901-911 (Pubitemid 44969196)
42. Denton, R.M., Randle, P.J. and Martin, B.R. (1972) Stimulation by calcium ions of pyruvate dehydrogenase phosphate phosphatase. Biochem. J. 128, 161-163
43. + -linked isocitrate dehydrogenase from the mitochondria of rat heart and other tissues. Biochem. J. 176, 899-906
44. McCormack, J.G. and Denton, R.M. (1979) The effects of calcium ions and adenine nucleotides on the activity of pig heart 2-oxoglutarate dehydrogenase complex. Biochem. J. 180, 533-544 (Pubitemid 9208285)
45. 2+ ] in cardiac cells. EMBO J. 20, 4998-5007
46. 2+ indicator targeted to mitochondria. J. Mol. Cell. Cardiol. 46, 891-901
47. 2+ release in gastric myocytes from Bufo marinus. J. Physiol. 522, 375-390
48. 2+ ] in rat pulmonary artery smooth muscle cells. J. Physiol. 516, 139-147
49. Nassar, A. and Simpson, A.W. (2000) Elevation of mitochondrial calcium by ryanodine-sensitive calcium-induced calcium release. J. Biol. Chem. 275, 23661-23665 (Pubitemid 30627455)
50. 2+ dynamics in individual mitochondria in situ. Am. J. Physiol. 276, C1193-C1204
51. 2+ . J. Biol. Chem. 274, 14157-14162
52. 2+ network. J. Cell Biol. 136, 833-844
53. 2+ -entry and limit its diffusion into vascular smooth muscle cells. Cell Calcium 40, 359-371
54. 2+ signals. J. Biol. Chem. 276, 26411-26420
55. Hajnoczky, G., Robb-Gaspers, L.D., Seitz, M.B. and Thomas, A.P. (1995) Decoding of cytosolic calcium oscillations in the mitochondria. Cell 82, 415-424
56. 2+ homeostasis in intact cells. J. Cell Biol. 126, 1183-1194
57. 2+ to the endoplasmic reticulum and prevent the depletion of neighboring endoplasmic reticulum regions. J. Biol. Chem. 276, 29430-29439
58. Filippin, L., Magalhaes, P.J., Di Benedetto, G., Colella, M. and Pozzan, T. (2003) Stable interactions between mitochondria and endoplasmic reticulum allow rapid accumulation of calcium in a subpopulation of mitochondria. J. Biol. Chem. 278, 39224-39234 (Pubitemid 37221826)
59. Nagai, T., Sawano, A., Park, E.S. and Miyawaki, A. (2001) Circularly permuted green fluorescent proteins engineered to sense Ca2+ . Proc. Natl. Acad. Sci. U.S.A. 98, 3197-3202 (Pubitemid 32220822)
60. Park, M.K., Ashby, M.C., Erdemli, G., Petersen, O.H. and Tepikin, A.V. (2001) Perinuclear, perigranular and sub-plasmalemmal mitochondria have distinct functions in the regulation of cellular calcium transport. EMBO J. 20, 1863-1874 (Pubitemid 32397389)
61. Lawrie, A.M., Rizzuto, R., Pozzan, T. and Simpson, A.W. (1996) A role for calcium influx in the regulation of mitochondrial calcium in endothelial cells. J. Biol. Chem. 271, 10753-10759 (Pubitemid 26145812)
62. 2+ transport. FEBS Lett. 46, 109-114
63. Reed, K.C. and Bygrave, F.L. (1974) The inhibition of mitochondrial calcium transport by lanthanides and ruthenium red. Biochem. J. 140, 143-155
64. 2+ waves in rat cortical astrocytes. J. Cell Biol. 145, 795-808
65. i range in arterial smooth muscle. Am. J. Physiol. Heart Circ. Physiol. 283, H2431-H2439
66. Gurney, A.M., Drummond, R.M. and Fay, F.S. (2000) Calcium signalling in sarcoplasmic reticulum, cytoplasm and mitochondria during activation of rabbit aorta myocytes. Cell Calcium 27, 339-351
67. 2+ oscillations. EMBO Rep. 7, 390-396
68. 2+ waves in cultured oligodendrocytes. J. Biol. Chem. 271, 33493-33501
69. 2+ release is inhibited by mitochondrial depolarization. Biochem. J. 347, 593-600
70. 2+ oscillations in smooth muscle. J. Cell Sci. 121, 75-85
71. 2+ store in guinea-pig colonic smooth muscle. J. Physiol. 516, 149-161
72. 2+ release from inositol 1,4,5-trisphosphate receptor clusters in smooth muscle cells. J. Biol. Chem. 285, 2040-2050
73. Chalmers, S. and McCarron, J.G. (2009) Inhibition of mitochondrial calcium uptake rather than efflux impedes calcium release by inositol-1,4,5-trisphosphate-sensitive receptors. Cell Calcium 46, 107-113
74. Jouaville, L.S., Ichas, F., Holmuhamedov, E.L., Camacho, P. and Lechleiter, J.D. (1995) Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocytes. Nature 377, 438-441
75. 2+ uniporter stimulation. J. Physiol. 580, 39-49
76. i in rat tail artery. Circ. Res. 90, 792-799
77. 2+ store and mitochondria in rat aortic smooth muscle cells. Biochem. J. 357, 363-371
78. 2+ oscillations in vascular myocytes. Arterioscler. Thromb. Vasc. Biol. 23, 1567-1575
79. 2+ influx and subplasmalemmal mitochondria. Cell Calcium 46, 49-55
80. 2+ store refilling. J. Biol. Chem. 278, 44769-44779
81. 2+ uptake. EMBO J. 21, 6744-6754
82. Hoth, M., Button, D.C. and Lewis, R.S. (2000) Mitochondrial control of calcium-channel gating: a mechanism for sustained signaling and transcriptional activation in T lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 97, 10607-10612
83. 2+ release units and couplons in skeletal and cardiac muscles. Biophys. J. 77, 1528-1539
84. Swillens, S., Dupont, G., Combettes, L. and Champeil, P. (1999) From calcium blips to calcium puffs: theoretical analysis of the requirements for interchannel communication. Proc. Natl. Acad. Sci. U.S.A. 96, 13750-13755
85. 3 receptors underlying calcium puffs in Xenopus oocytes. Biophys. J. 91, 4033-4044
86. Parker, I. and Yao, Y. (1991) Regenerative release of calcium from functionally discrete subcellular stores by inositol trisphosphate. Proc. Biol. Sci. 246, 269-274
87. Bootman, M.D., Berridge, M.J. and Lipp, P. (1997) Cooking with calcium: the recipes for composing global signals from elementary events. Cell 91, 367-373 (Pubitemid 27467967)
88. 3-gated channels in rat ureteric myocytes. Biochem. J. 349, 323-332
89. Cheng, H., Lederer, W.J. and Cannell, M.B. (1993) Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 262, 740-744 (Pubitemid 23350693)
90. 2+ puffs and mitochondria in Xenopus oocytes. Am. J. Physiol. Cell Physiol. 282, C1374-C1386
91. 2+ marks: miniature calcium signals in single mitochondria driven by ryanodine receptors. Proc. Natl. Acad. Sci. U.S.A. 99, 2380-2385
92. Ichas, F., Jouaville, L.S. and Mazat, J.P. (1997) Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 89, 1145-1153 (Pubitemid 127678747)
93. 2+ and sustained opening of the permeability transition pore. J. Cell Sci. 115, 1175-1188
94. O'Reilly, C.M., Fogarty, K.E., Drummond, R.M., Tuft, R.A. and Walsh, Jr, J.V. (2004) Spontaneous mitochondrial depolarizations are independent of SR Ca2+ release. Am. J. Physiol. Cell Physiol. 286, C1139-C1151 (Pubitemid 38506929)
95. Avlonitis, N., Chalmers, S., McDougall, C., Stanton-Humphreys, M.N., Brown, C.T., McCarron, J.G. and Conway, S.J. (2009) Caged AG10: new tools for spatially predefined mitochondrial uncoupling. Mol. Biosyst. 5, 450-457