The molecular identity of the mitochondrial Ca2+ sequestration system: Minireview

FEBS Journal

Volumn 277, Issue 18, 2010, Pages 3652-3663

  Starkov, Anatoly A ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

brain mitochondria; Ca2+ accumulation; Ca2+ and Pi precipitate; calciphorin; calcium uniporter; calvectin; dense granules; gC1qR; liver mitochondria; permeability transition pore

Indexed keywords

CALCIPHORIN; CALCIUM; CALCIUM BINDING PROTEIN; CALVECTIN; PROTEIN KINASE C; UNCLASSIFIED DRUG;

APOPTOSIS; BRAIN MITOCHONDRION; CALCIUM BINDING; CALCIUM DEPLETION; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CARBOXY TERMINAL SEQUENCE; ELECTRON MICROSCOPY; IN VITRO STUDY; KIDNEY CORTEX; LIVER MITOCHONDRION; MITOCHONDRIAL PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY;

ANIMALS; CALCIUM; CALCIUM PHOSPHATES; CALCIUM SIGNALING; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; ORGAN SPECIFICITY;

EID: 77956322223     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07756.x     Document Type: Short Survey

References (85)

1. 2+ exchange. Proc Natl Acad Sci USA 107, 436 441.
2. + antiporter. Science 326, 144 147.
3. 2+ sequestration and precipitation revisited. FEBS J 277, 3637 3651.
4. Pivovarova NB Andrews SB (2010) Calcium-dependent mitochondrial function and dysfunction in neurons. FEBS J 277, 3622 3636.
5. Kirichok Y, Krapivinsky G Clapham DE (2004) The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427, 360 364.
6. 2+ uniporter by external adenine nucleotides: the uniporter behaves like a gated channel which is regulated by nucleotides and divalent cations. Biochemistry 36, 7071 7080.
7. Sparagna GC, Gunter KK, Sheu SS Gunter TE (1995) Mitochondrial calcium uptake from physiological-type pulses of calcium. A description of the rapid uptake mode. J Biol Chem 270, 27510 27515.
8. Igbavboa U Pfeiffer DR (1991) Regulation of reverse uniport activity in mitochondria by extramitochondrial divalent cations. Dependence on a soluble intermembrane space component. J Biol Chem 266, 4283 4287.
9. 2+ influx cooperativity. FEBS Lett 389, 293 296.
10. Sottocasa GL, Sandri G, Panfili E De Bernard B (1971) A glycoprotein located in the intermembrane space of rat liver mitochondria. FEBS Lett 17, 100 105.
11. 2+-binding factor extracted from rat liver mitochondria. Biochem Biophys Res Commun 42, 312 318.
12. 2+-binding factor from rat liver mitochondria. Biochem Biophys Res Commun 47, 814 819.
13. Blondin GA (1974) Isolation of a divalent cation ionophore from beef heart mitochondria. Biochem Biophys Res Commun 56, 97 105.
14. 2+ binding glycoprotein from ox liver mitochondria. Biochem Biophys Res Commun 47, 808 813.
15. 2+ carrier from calf heart inner mitochondrial membrane. Proc Natl Acad Sci USA 75, 2125 2129.
16. 2+ carrier from calf heart inner mitochondrial membrane. J Biol Chem 255, 6897 6903.
17. Shamoo AE Jeng AY (1978) Possible calcium carrier from the inner membrane of calf heart mitochondria. Ann NY Acad Sci 307, 235 237.
18. 2+ movements. Eur J Biochem 105, 205 210.
19. Makhmudova EM, Gagel'gans AI, Mirkhodzhaev UZ Tashmukhamedov BA (1975) Effect of the mitochondrial ionophore for divalent cations on bilayer phospholipid membranes. Biofizika 20, 225 227. In Russian.
20. Mironova GD, Baumann M, Kolomytkin O, Krasichkova Z, Berdimuratov A, Sirota T, Virtanen I Saris NE (1994) Purification of the channel component of the mitochondrial calcium uniporter and its reconstitution into planar lipid bilayers. J Bioenerg Biomembr 26, 231 238.
21. 2+-transporting glycoprotein and peptide from beef heart mitochondria. J Bioenerg Biomembr 14, 213 225.
22. 2+-binding glycoprotein with lipid bilayer membranes. FEBS Lett 45, 99 103.
23. Zazueta C, Masso F, Paez A, Bravo C, Vega A, Montano L, Vazquez M, Ramirez J Chavez E (1994) Identification of a 20-kDa protein with calcium uptake transport activity. Reconstitution in a membrane model. J Bioenerg Biomembr 26, 555 562.
24. Lars Ernster (1984) "Bioenergetics" New comprehensive biochemistry v9. Amsterdam, New York : Elsevier, New York, NY, USA, pp 274 277.
25. Saris NE Carafoli E (2005) A historical review of cellular calcium handling, with emphasis on mitochondria. Biochemistry (Mosc) 70, 187 194.
26. Panfili E, Sandri G, Liut G, Stancher B Sottocasa GL (1983) In Calcium-Binding Proteins (de Bernard B, Sottocasa GL, Sandri G, Carafoli E, Taylor AN, Vanaman TC Williams RJP eds pp 347 354. Elsevier Science Publishers, Amsterdam.
27. Sandri G, Panfili E Sottocasa GL (1974) Intramitochondrial location of the calcium binding glycoprotein. Acta Vitaminol Enzymol 28, 317 322.
28. 2+ binding glycoprotein to inner mitochondrial membrane. Bull Mol Biol Med 3, 179 188.
29. 2+ transport in glycoprotein-depleted rat liver mitochondria. Biochim Biophys Acta 558, 214 220.
30. Sandri G, Panfili E Sottocasa GL (1976) The calcium-binding glycoprotein and mitochondrial calcium movements. Biochem Biophys Res Commun 68, 1272 1279.
31. 2+-binding glycoprotein. Nature 264, 185 186.
32. Sottocasa G, Panfili E Sandri G (1977) The problem of mitochondrial calcium transport. Bull Mol Biol Med 2, 1 28.
33. 2+ carrier isolated from calf heart inner mitochondrial membrane. J Biol Chem 255, 6904 6912.
34. Shamoo AE Brenza JM (1980) Calciphorin structure and function. Ann NY Acad Sci 358, 73 82.
35. 2+ ionophore properties from rat liver mitochondria. Arch Biochem Biophys 221, 404 416.
36. 2+-cardiolipin interaction in a model system. Selectivity and apparent high affinity. Biochim Biophys Acta 732, 41 47.
37. Ambudkar IS, Kima PE Shamoo AE (1984) Characterization of calciphorin, the low molecular weight calcium ionophore, from rat liver mitochondria. Biochim Biophys Acta 771, 165 170.
38. Saris NE, Sirota TV, Virtanen I, Niva K, Penttila T, Dolgachova LP Mironova GD (1993) Inhibition of the mitochondrial calcium uniporter by antibodies against a 40-kDa glycoprotein. J Bioenerg Biomembr 25, 307 312.
39. Urry DW (1972) A molecular theory of ion-conductng channels: a field-dependent transition between conducting and nonconducting conformations. Proc Natl Acad Sci USA 69, 1610 1614.
40. Mironova GD Utesheva ZhA (1989) Molecular mechanism of calcium ion transport in mitochondria. I. Glycoprotein-peptide complex as a component of the electron transport system. Ukr Biokhim Zh 61, 48 54. In Russian.
41. 2+ uniporter using the labeled inhibitor 103Ru360. J Bioenerg Biomembr 30, 489 498.
42. Zazueta C, Correa F, Garcia N Garcia Gde J (2004) Different subunit location of the inhibition and transport sites in the mitochondrial calcium uniporter. J Bioenerg Biomembr 36, 439 445.
43. Correa F Zazueta C (2005) Mitochondrial glycosidic residues contribute to the interaction between ruthenium amine complexes and the calcium uniporter. Mol Cell Biochem 272, 55 62.
44. Greenawalt JW, Rossi CS Lehninger AL (1964) Effect of active accumulation of calcium and phosphate ions on the structure of rat liver mitochondria. J Cell Biol 23, 21 38.
45. Chalmers S Nicholls DG (2003) The relationship between free and total calcium concentrations in the matrix of liver and brain mitochondria. J Biol Chem 278, 19062 19070.
46. Price PA Lim JE (2003) The inhibition of calcium phosphate precipitation by fetuin is accompanied by the formation of a fetuin-mineral complex. J Biol Chem 278, 22144 22152.
47. 2+-binding protein with EF-hand and coiled-coil domains. J Neurochem 96, 292 304.
48. 30kDa (calretinin) are substantially localised in the particulate fraction of rat brain. FEBS Lett 374, 333 337.
49. Winsky L Kuznicki J (1995) Distribution of calretinin, calbindin D28k, and parvalbumin in subcellular fractions of rat cerebellum: effects of calcium. J Neurochem 65, 381 388.
50. Pasteels JL, Pochet R, Surardt L, Hubeau C, Chirnoaga M, Parmentier M Lawson DE (1986) Ultrastructural localization of brain 'vitamin D-dependent' calcium binding proteins. Brain Res 384, 294 303.
51. Yoshii K, Sugimoto K, Tai Y, Konishi R Tokuda M (2000) Purification, identification and phosphorylation of annexin I from rat liver mitochondria. Acta Med Okayama 54, 57 65.
52. Rainteau D, Mansuelle P, Rochat H Weinman S (1995) Characterization and ultrastructural localization of annexin VI from mitochondria. FEBS Lett 360, 80 84.
53. Genge BR, Wu LN Wuthier RE (2007) In vitro modeling of matrix vesicle nucleation: synergistic stimulation of mineral formation by annexin A5 and phosphatidylserine. J Biol Chem 282, 26035 26045.
54. n. Proc Natl Acad Sci USA 95, 5981 5986.
55. Weinbach EC Von Brand T (1967) Formation, isolation and composition of dense granules from mitochondria. Biochim Biophys Acta 148, 256 266.
56. Crompton M (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem J 341, 233 249.
57. Forte M Bernardi P (2005) Genetic dissection of the permeability transition pore. J Bioenerg Biomembr 37, 121 128.
58. Halestrap AP Brenner C (2003) The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr Med Chem 10, 1507 1525.
59. Nicholls DG (2005) Mitochondria and calcium signaling. Cell Calcium 38, 311 317.
60. Leung AW Halestrap AP (2008) Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore. Biochim Biophys Acta 1777, 946 952.
61. Bernardi P, Krauskopf A, Basso E, Petronilli V, Blachly-Dyson E, Di Lisa F Forte MA (2006) The mitochondrial permeability transition from in vitro artifact to disease target. Febs J 273, 2077 2099.
62. Bernardi P (1999) Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 79, 1127 1155.
63. Woodfield K, Ruck A, Brdiczka D Halestrap AP (1998) Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition. Biochem J 336, 287 290.
64. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW et al. (2005) Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434, 658 662.
65. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, Inohara H, Kubo T Tsujimoto Y (2005) Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434, 652 658.
66. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J, Hetz C, Danial NN, Moskowitz MA Korsmeyer SJ (2005) Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci USA 102, 12005 12010.
67. Basso E, Fante L, Fowlkes J, Petronilli V, Forte MA Bernardi P (2005) Properties of the permeability transition pore in mitochondria devoid of cyclophilin D. J Biol Chem 280, 18558 18561.
68. Kokoszka JE, Waymire KG, Levy SE, Sligh JE, Cai J, Jones DP, MacGregor GR Wallace DC (2004) The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427, 461 465.
69. Baines CP, Kaiser RA, Sheiko T, Craigen WJ Molkentin JD (2007) Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol 9, 550 555.
70. He L Lemasters JJ (2002) Regulated and unregulated mitochondrial permeability transition pores: a new paradigm of pore structure and function? FEBS Lett 512, 1 7.
71. Robles-Flores M, Rendon-Huerta E, Gonzalez-Aguilar H, Mendoza-Hernandez G, Islas S, Mendoza V, Ponce- Castaneda MV, Gonzalez-Mariscal L Lopez-Casillas F (2002) p32 (gC1qBP) is a general protein kinase C (PKC)-binding protein; interaction and cellular localization of p32-PKC complexes in ray hepatocytes. J Biol Chem 277, 5247 5255.
72. Muta T, Kang D, Kitajima S, Fujiwara T Hamasaki N (1997) p32 protein, a splicing factor 2-associated protein, is localized in mitochondrial matrix and is functionally important in maintaining oxidative phosphorylation. J Biol Chem 272, 24363 24370.
73. Soltys BJ, Kang D Gupta RS (2000) Localization of P32 protein (gC1q-R) in mitochondria and at specific extramitochondrial locations in normal tissues. Histochem Cell Biol 114, 245 255.
74. Ghebrehiwet B Peerschke EI (1998) Structure and function of gC1q-R: a multiligand binding cellular protein. Immunobiology 199, 225 238.
75. Ghebrehiwet B Peerschke EI (2004) cC1q-R (calreticulin) and gC1q-R/p33: ubiquitously expressed multi-ligand binding cellular proteins involved in inflammation and infection. Mol Immunol 41, 173 183.
76. Tye AJ, Ghebrehiwet B, Guo N, Sastry KN, Chow BK, Peerschke EI Lim BL (2001) The human gC1qR/p32 gene, C1qBP. Genomic organization and promoter analysis. J Biol Chem 276, 17069 17075.
77. Jiang J, Zhang Y, Krainer AR Xu RM (1999) Crystal structure of human p32, a doughnut-shaped acidic mitochondrial matrix protein. Proc Natl Acad Sci USA 96, 3572 3577.
78. Nicolli A, Basso E, Petronilli V, Wenger RM Bernardi P (1996) Interactions of cyclophilin with the mitochondrial inner membrane and regulation of the permeability transition pore, and cyclosporin A-sensitive channel. J Biol Chem 271, 2185 2192.
79. Jha BK, Salunke DM Datta K (2002) Disulfide bond formation through Cys186 facilitates functionally relevant dimerization of trimeric hyaluronan-binding protein 1 (HABP1)/p32/gC1qR. Eur J Biochem 269, 298 306.
80. Sunayama J, Ando Y, Itoh N, Tomiyama A, Sakurada K, Sugiyama A, Kang D, Tashiro F, Gotoh Y, Kuchino Y et al. (2004) Physical and functional interaction between BH3-only protein Hrk and mitochondrial pore-forming protein p32. Cell Death Differ 11, 771 781.
81. Reef S, Shifman O, Oren M Kimchi A (2007) The autophagic inducer smARF interacts with and is stabilized by the mitochondrial p32 protein. Oncogene 26, 6677 6683.
82. Majumdar M, Meenakshi J, Goswami SK Datta K (2002) Hyaluronan binding protein 1 (HABP1)/C1QBP/p32 is an endogenous substrate for MAP kinase and is translocated to the nucleus upon mitogenic stimulation. Biochem Biophys Res Commun 291, 829 837.
83. Storz P, Hausser A, Link G, Dedio J, Ghebrehiwet B, Pfizenmaier K Johannes FJ (2000) Protein kinase Cμ is regulated by the multifunctional chaperon protein p32. J Biol Chem 275, 24601 24607.
84. η): emerging role in cardiac protection from ischaemic damage. Biochem Soc Trans 35, 1052 1054.
85. Chowdhury AR, Ghosh I Datta K (2008) Excessive reactive oxygen species induces apoptosis in fibroblasts: role of mitochondrially accumulated hyaluronic acid binding protein 1 (HABP1/p32/gC1qR). Exp Cell Res 314, 651 667.