Mitochondria-associated membranes (MAMs) as hotspot Ca 2+ signaling units

Advances in Experimental Medicine and Biology

Volumn 740, Issue , 2012, Pages 411-437

  Bononi, Angela ^a   Missiroli, Sonia ^a   Poletti, Federica ^a   Suski, Jan M ^a   Agnoletto, Chiara ^a   Bonora, Massimo ^a   De Marchi, Elena ^a   Giorgi, Carlotta ^a   Marchi, Saverio ^a   Patergnani, Simone ^a   Rimessi, Alessandro ^a   Wieckowski, Mariusz R ^b   Pinton, Paolo ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

Akt; Apoptosis; Bap31; Bip; Ca 2+ signaling; Calcium ions; Endoplasmic Reticulum; Ero1 ; ERp44; GM1 ganglioside; grp75; IP3Rs; MCU; Microdomains; MICU1; Mitochondria; Mitochondria Associated Membranes; Mitofusin 1 and 2; p66Shc; PACS 2; Plasma Membrane Associated Membranes; PML; PP2a; Presenilin 1 and 2; Sig 1R; VDAC

Indexed keywords

CALCIUM ION; MITOCHONDRIAL PROTEIN;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL FATE; CELL SURVIVAL; ENDOPLASMIC RETICULUM; ENERGY YIELD; HUMAN; MITOCHONDRIAL MEMBRANE; MOLECULAR INTERACTION; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CALCIUM SIGNALING; ENDOPLASMIC RETICULUM; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES;

EID: 84859920313     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-2888-2_17     Document Type: Article

References (173)

1. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11-21
2. Brini M, Carafoli E (2009) Calcium pumps in health and disease. Physiol Rev 89:1341-1378
3. Blaustein MP, Lederer WJ (1999) Sodium/calcium exchange: its physiological implications. Physiol Rev 79:763-854
4. Bertolino M, Llinas RR (1992) The central role of voltage-activated and receptor-operated calcium channels in neuronal cells. Annu Rev Pharmacol Toxicol 32:399-421
5. McFadzean I, Gibson A (2002) The developing relationship between receptor-operated and store-operated calcium channels in smooth muscle. Br J Pharmacol 135:1-13
6. Meldolesi J, Pozzan T (1987) Pathways of Ca2+ influx at the plasma membrane: voltage-, receptor-, and second messenger-operated channels. Exp Cell Res 171:271-283
7. Foskett JK, White C, Cheung KH, Mak DO (2007) Inositol trisphosphate receptor Ca2+ release channels. Physiol Rev 87:593-658
8. Sutko JL, Airey JA (1996) Ryanodine receptor Ca2+ release channels: does diversity in form equal diversity in function? Physiol Rev 76:1027-1071
9. Patel S, Joseph SK, Thomas AP (1999) Molecular properties of inositol 1,4,5-trisphosphate receptors. Cell Calcium 25:247-264
10. Patterson RL, Boehning D, Snyder SH (2004) Inositol 1,4,5-trisphosphate receptors as signal integrators. Annu Rev Biochem 73:437-465
11. Berridge MJ (2006) Calcium microdomains: organization and function. Cell Calcium 40:405-412
12. John LM, Lechleiter JD, Camacho P (1998) Differential modulation of SERCA2 isoforms by calreticulin. J Cell Biol 142:963-973
13. Carafoli E (2003) Historical review: mitochondria and calcium: ups and downs of an unusual relationship. Trends Biochem Sci 28:175-181
14. Rizzuto R, Simpson AW, Brini M, Pozzan T (1992) Rapid changes of mitochondrial Ca2+ revealed by specifically targeted recombinant aequorin. Nature 358:325-327
15. Nicholls DG, Crompton M (1980) Mitochondrial calcium transport. FEBS Lett 111:261-268
16. Rizzuto R, Brini M, Murgia M, Pozzan T (1993) Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science 262:744-747
17. Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft RA, Pozzan T (1998) Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280:1763-1766
18. Csordas G, Thomas AP, Hajnoczky G (1999) Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria. EMBO J 18:96-108
19. Rizzuto R, Pozzan T (2006) Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol Rev 86:369-408
20. Giacomello M, Drago I, Bortolozzi M, Scorzeto M, Gianelle A, Pizzo P, Pozzan T (2010) Ca2+ hot spots on the mitochondrial surface are generated by Ca2+ mobilization from stores, but not by activation of store-operated Ca2+ channels. Mol Cell 38:280-290
21. Palmer AE, Giacomello M, Kortemme T, Hires SA, Lev-Ram V, Baker D, Tsien RY (2006) Ca2+ indicators based on computationally redesigned calmodulin-peptide pairs. Chem Biol 13:521-530
22. Csordas G, Varnai P, Golenar T, Roy S, Purkins G, Schneider TG, Balla T, Hajnoczky G (2010) Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol Cell 39:121-132
23. Inoue T, Heo WD, Grimley JS, Wandless TJ, Meyer T (2005) An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways. Nat Methods 2:415-418
24. Simamura E, Shimada H, Hatta T, Hirai K (2008) Mitochondrial voltage-dependent anion channels (VDACs) as novel pharmacological targets for anti-cancer agents. J Bioenerg Biomembr 40:213-217
25. De Pinto V, Reina S, Guarino F, Messina A (2008) Structure of the voltage dependent anion channel: state of the art. J Bioenerg Biomembr 40:139-147
26. Colombini M (2009) The published 3D structure of the VDAC channel: native or not? Trends Biochem Sci 34:382-389
27. Shoshan-Barmatz V, De Pinto V, Zweckstetter M, Raviv Z, Keinan N, Arbel N (2010) VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 31:227-285
28. Perocchi F, Gohil VM, Girgis HS, Bao XR, McCombs JE, Palmer AE, Mootha VK (2010) MICU1 encodes a mitochondrial EF hand protein required for Ca(2+) uptake. Nature 467:291-296
29. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong SE, Walford GA, Sugiana C, Boneh A, Chen WK, Hill DE, Vidal M, Evans JG, Thorburn DR, Carr SA, Mootha VK (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134: 112-123
30. De Stefani D, Raffaello A, Teardo E, Szabo I, Rizzuto R (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476:336-340
31. Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, Koteliansky V, Mootha VK (2011) Integrative genomics identifi es MCU as an essential component of the mitochondrial calcium uniporter. Nature 476:341-345
32. Bernardi P (1999) Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 79:1127-1155
33. Palty R, Silverman WF, Hershfi nkel M, Caporale T, Sensi SL, Parnis J, Nolte C, Fishman D, Shoshan-Barmatz V, Herrmann S, Khananshvili D, Sekler I (2010) NCLX is an essential component of mitochondrial Na+/Ca2+ exchange. Proc Natl Acad Sci USA 107:436-441
34. Baines CP (2009) The molecular composition of the mitochondrial permeability transition pore. J Mol Cell Cardiol 46:850-857
35. Rasola A, Bernardi P (2007) The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 12:815-833
36. Rasola A, Sciacovelli M, Pantic B, Bernardi P (2010) Signal transduction to the permeability transition pore. FEBS Lett 584:1989-1996
37. McCormack JG, Halestrap AP, Denton RM (1990) Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 70:391-425
38. Carafoli E (2010) The fateful encounter of mitochondria with calcium: how did it happen? Biochim Biophys Acta 1797:595-606
39. Maes K, Missiaen L, De Smet P, Vanlingen S, Callewaert G, Parys JB, De Smedt H (2000) Differential modulation of inositol 1,4,5-trisphosphate receptor type 1 and type 3 by ATP. Cell Calcium 27:257-267
40. Betzenhauser MJ, Wagner LE 2nd, Iwai M, Michikawa T, Mikoshiba K, Yule DI (2008) ATP modulation of Ca2+ release by type-2 and type-3 inositol (1, 4, 5)-triphosphate receptors. Differing ATP sensitivities and molecular determinants of action. J Biol Chem 283:21579-21587
41. Walsh C, Barrow S, Voronina S, Chvanov M, Petersen OH, Tepikin A (2009) Modulation of calcium signalling by mitochondria. Biochim Biophys Acta 1787:1374-1382
42. Arnaudeau S, Kelley WL, Walsh JV Jr (2001) Demaurex N: mitochondria recycle Ca(2+) to the endoplasmic reticulum and prevent the depletion of neighboring endoplasmic reticulum regions. J Biol Chem 276:29430-29439
43. Tinel H, Cancela JM, Mogami H, Gerasimenko JV, Gerasimenko OV, Tepikin AV, Petersen OH (1999) Active mitochondria surrounding the pancreatic acinar granule region prevent spreading of inositol trisphosphate-evoked local cytosolic Ca(2+) signals. EMBO J 18:4999-5008
44. Goetz JG, Genty H, St-Pierre P, Dang T, Joshi B, Sauve R, Vogl W, Nabi IR (2007) Reversible interactions between smooth domains of the endoplasmic reticulum and mitochondria are regulated by physiological cytosolic Ca2+ levels. J Cell Sci 120:3553-3564
45. Wang HJ, Guay G, Pogan L, Sauve R, Nabi IR (2000) Calcium regulates the association between mitochondria and a smooth subdomain of the endoplasmic reticulum. J Cell Biol 150:1489-1498
46. Yi M, Weaver D, Hajnoczky G (2004) Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol 167:661-672
47. Westermann B (2010) Mitochondrial fusion and fi ssion in cell life and death. Nat Rev Mol Cell Biol 11:872-884
48. Rintoul GL, Filiano AJ, Brocard JB, Kress GJ, Reynolds IJ (2003) Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J Neurosci 23:7881-7888
49. Germain M, Mathai JP, McBride HM, Shore GC (2005) Endoplasmic reticulum BIK initiates DRP1-regulated remodelling of mitochondrial cristae during apoptosis. EMBO J 24: 1546-1556
50. Alirol E, James D, Huber D, Marchetto A, Vergani L, Martinou JC, Scorrano L (2006) The mitochondrial fi ssion protein hFis1 requires the endoplasmic reticulum gateway to induce apoptosis. Mol Biol Cell 17:4593-4605
51. Szabadkai G, Simoni AM, Chami M, Wieckowski MR, Youle RJ, Rizzuto R (2004) Drp-1-dependent division of the mitochondrial network blocks intraorganellar Ca2+ waves and protects against Ca2 + -mediated apoptosis. Mol Cell 16:59-68
52. Lu B (2009) Mitochondrial dynamics and neurodegeneration. Curr Neurol Neurosci Rep 9:212-219
53. Giorgi C, Romagnoli A, Pinton P, Rizzuto R (2008) Ca2+ signaling, mitochondria and cell death. Curr Mol Med 8:119-130
54. Harr MW, Distelhorst CW (2010) Apoptosis and autophagy: decoding calcium signals that mediate life or death. Cold Spring Harb Perspect Biol 2:a005579
55. Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99-163
56. Tait SW, Green DR (2010) Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 11:621-632
57. Armstrong JS (2006) The role of the mitochondrial permeability transition in cell death. Mitochondrion 6:225-234
58. Rong Y, Distelhorst CW (2008) Bcl-2 protein family members: versatile regulators of calcium signaling in cell survival and apoptosis. Annu Rev Physiol 70:73-91
59. Trinei M, Berniakovich I, Beltrami E, Migliaccio E, Fassina A, Pelicci P, Giorgio M (2009) P66Shc signals to age. Aging (Albany NY) 1:503-510
60. Pinton P, Rimessi A, Marchi S, Orsini F, Migliaccio E, Giorgio M, Contursi C, Minucci S, Mantovani F, Wieckowski MR, Del Sal G, Pelicci PG, Rizzuto R (2007) Protein kinase C beta and prolyl isomerase 1 regulate mitochondrial effects of the life-span determinant p66Shc. Science 315:659-663
61. Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124:573-586
62. Shibata Y, Voeltz GK, Rapoport TA (2006) Rough sheets and smooth tubules. Cell 126:435-439
63. English AR, Zurek N, Voeltz GK (2009) Peripheral ER structure and function. Curr Opin Cell Biol 21:596-602
64. Shibata Y, Shemesh T, Prinz WA, Palazzo AF, Kozlov MM, Rapoport TA (2010) Mechanisms determining the morphology of the peripheral ER. Cell 143:774-788
65. Chevet E, Cameron PH, Pelletier MF, Thomas DY, Bergeron JJ (2001) The endoplasmic reticulum: integration of protein folding, quality control, signaling and degradation. Curr Opin Struct Biol 11:120-124
66. Palade G (1975) Intracellular aspects of the process of protein synthesis. Science 189:347-358
67. Bootman MD, Petersen OH, Verkhratsky A (2002) The endoplasmic reticulum is a focal point for co-ordination of cellular activity. Cell Calcium 32:231-234
68. Verkhratsky A, Petersen OH (2002) The endoplasmic reticulum as an integrating signalling organelle: from neuronal signalling to neuronal death. Eur J Pharmacol 447:141-154
69. Jobsis FF, O'Connor MJ (1966) Calcium release and reabsorption in the sartorius muscle of the toad. Biochem Biophys Res Commun 25:246-252
70. Ridgway EB, Ashley CC (1967) Calcium transients in single muscle fibers. Biochem Biophys Res Commun 29:229-234
71. Ashley CC, Ridgway EB (1970) On the relationships between membrane potential, calcium transient and tension in single barnacle muscle fi bres. J Physiol 209:105-130
72. MacKrill JJ (1999) Protein-protein interactions in intracellular Ca2 + -release channel function. Biochem J 337(Pt 3):345-361
73. Rizzuto R, Marchi S, Bonora M, Aguiari P, Bononi A, De Stefani D, Giorgi C, Leo S, Rimessi A, Siviero R, Zecchini E, Pinton P (2009) Ca(2+) transfer from the ER to mitochondria: when, how and why. Biochim Biophys Acta 1787:1342-1351
74. Iino M, Endo M (1992) Calcium-dependent immediate feedback control of inositol 1,4,5-triphosphate-induced Ca2+ release. Nature 360:76-78
75. Missiaen L, Taylor CW, Berridge MJ (1992) Luminal Ca2+ promoting spontaneous Ca2+ release from inositol trisphosphate-sensitive stores in rat hepatocytes. J Physiol 455: 623-640
76. Nunn DL, Taylor CW (1992) Luminal Ca2+ increases the sensitivity of Ca2+ stores to inositol 1,4,5-trisphosphate. Mol Pharmacol 41:115-119
77. Smith JB, Smith L, Higgins BL (1985) Temperature and nucleotide dependence of calcium release by myo-inositol 1,4,5-trisphosphate in cultured vascular smooth muscle cells. J Biol Chem 260:14413-14416
78. Bezprozvanny I, Ehrlich BE (1993) ATP modulates the function of inositol 1,4,5-trisphosphate-gated channels at two sites. Neuron 10:1175-1184
79. Iino M (1991) Effects of adenine nucleotides on inositol 1,4,5-trisphosphate-induced calcium release in vascular smooth muscle cells. J Gen Physiol 98:681-698
80. Vanderheyden V, Devogelaere B, Missiaen L, De Smedt H, Bultynck G, Parys JB (2009) Regulation of inositol 1,4,5-trisphosphate-induced Ca2+ release by reversible phosphorylation and dephosphorylation. Biochim Biophys Acta 1793:959-970
81. Khan MT, Wagner L 2nd, Yule DI, Bhanumathy C, Joseph SK (2006) Akt kinase phosphorylation of inositol 1,4,5-trisphosphate receptors. J Biol Chem 281:3731-3737
82. Bugrim AE (1999) Regulation of Ca2+ release by cAMP-dependent protein kinase. A mechanism for agonist-specific calcium signaling? Cell Calcium 25:219-226
83. Murthy KS, Zhou H (2003) Selective phosphorylation of the IP3R-I in vivo by cGMP-dependent protein kinase in smooth muscle. Am J Physiol Gastrointest Liver Physiol 284:G221-G230
84. Bagni C, Mannucci L, Dotti CG, Amaldi F (2000) Chemical stimulation of synaptosomes modulates alpha -Ca2+/calmodulin-dependent protein kinase II mRNA association to polysomes. J Neurosci 20:RC76
85. Vermassen E, Fissore RA, Nadif Kasri N, Vanderheyden V, Callewaert G, Missiaen L, Parys JB, De Smedt H (2004) Regulation of the phosphorylation of the inositol 1,4,5-trisphosphate receptor by protein kinase C. Biochem Biophys Res Commun 319:888-893
86. Jayaraman T, Ondrias K, Ondriasova E, Marks AR (1996) Regulation of the inositol 1,4,5-trisphosphate receptor by tyrosine phosphorylation. Science 272:1492-1494
87. Joseph SK, Hajnoczky G (2007) IP3 receptors in cell survival and apoptosis: Ca2+ release and beyond. Apoptosis 12:951-968
88. Pinton P, Giorgi C, Siviero R, Zecchini E, Rizzuto R (2008) Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene 27:6407-6418
89. Pinton P, Ferrari D, Magalhaes P, Schulze-Osthoff K, Di Virgilio F, Pozzan T, Rizzuto R (2000) Reduced loading of intracellular Ca(2+) stores and downregulation of capacitative Ca(2+) influx in Bcl-2-overexpressing cells. J Cell Biol 148:857-862
90. Foyouzi-Youssefi R, Arnaudeau S, Borner C, Kelley WL, Tschopp J, Lew DP, Demaurex N, Krause KH (2000) Bcl-2 decreases the free Ca2+ concentration within the endoplasmic reticulum. Proc Natl Acad Sci USA 97:5723-5728
91. Palmer AE, Jin C, Reed JC, Tsien RY (2004) Bcl-2-mediated alterations in endoplasmic reticulum Ca2+ analyzed with an improved genetically encoded fluorescent sensor. Proc Natl Acad Sci USA 101:17404-17409
92. White C, Li C, Yang J, Petrenko NB, Madesh M, Thompson CB, Foskett JK (2005) The endoplasmic reticulum gateway to apoptosis by Bcl-X(L) modulation of the InsP3R. Nat Cell Biol 7:1021-1028
93. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T, Korsmeyer SJ (2003) BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 300:135-139
94. Oakes SA, Scorrano L, Opferman JT, Bassik MC, Nishino M, Pozzan T, Korsmeyer SJ (2005) Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc Natl Acad Sci USA 102:105-110
95. Pinton P, Rizzuto R (2006) Bcl-2 and Ca2+ homeostasis in the endoplasmic reticulum. Cell Death Differ 13:1409-1418
96. Copeland DE, Dalton AJ (1959) An association between mitochondria and the endoplasmic reticulum in cells of the pseudobranch gland of a teleost. J Biophys Biochem Cytol 5: 393-396
97. Lewis JA, Tata JR (1973) A rapidly sedimenting fraction of rat liver endoplasmic reticulum. J Cell Sci 13:447-459
98. Morre DJ, Merritt WD, Lembi CA (1971) Connections between mitochondria and endoplasmic reticulum in rat liver and onion stem. Protoplasma 73:43-49
99. Mannella CA, Buttle K, Rath BK, Marko M (1998) Electron microscopic tomography of ratliver mitochondria and their interaction with the endoplasmic reticulum. Biofactors 8:225-228
100. Soltys BJ, Gupta RS (1992) Interrelationships of endoplasmic reticulum, mitochondria, intermediate filaments, and microtubules-a quadruple fluorescence labeling study. Biochem Cell Biol 70:1174-1186
101. Mannella CA, Marko M, Penczek P, Barnard D, Frank J (1994) The internal compartmentation of rat-liver mitochondria: tomographic study using the high-voltage transmission electron microscope. Microsc Res Tech 27:278-283
102. Achleitner G, Gaigg B, Krasser A, Kainersdorfer E, Kohlwein SD, Perktold A, Zellnig G, Daum G (1999) Association between the endoplasmic reticulum and mitochondria of yeast facilitates interorganelle transport of phospholipids through membrane contact. Eur J Biochem 264:545-553
103. Csordas G, Renken C, Varnai P, Walter L, Weaver D, Buttle KF, Balla T, Mannella CA, Hajnoczky G (2006) Structural and functional features and signifi cance of the physical linkage between ER and mitochondria. J Cell Biol 174:915-921
104. de Brito OM, Scorrano L (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456:605-610
105. Dennis EA, Kennedy EP (1972) Intracellular sites of lipid synthesis and the biogenesis of mitochondria. J Lipid Res 13:263-267
106. Vance JE (1990) Phospholipid synthesis in a membrane fraction associated with mitochondria. J Biol Chem 265:7248-7256
107. Vance JE, Stone SJ, Faust JR (1997) Abnormalities in mitochondria- associated membranes and phospholipid biosynthetic enzymes in the mnd/mnd mouse model of neuronal ceroid lipofuscinosis. Biochim Biophys Acta 1344:286-299
108. Wieckowski MR, Giorgi C, Lebiedzinska M, Duszynski J, Pinton P (2009) Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells. Nat Protoc 4:1582-1590
109. Pichler H, Gaigg B, Hrastnik C, Achleitner G, Kohlwein SD, Zellnig G, Perktold A, Daum G (2001) A subfraction of the yeast endoplasmic reticulum associates with the plasma membrane and has a high capacity to synthesize lipids. Eur J Biochem 268:2351-2361
110. Wu MM, Buchanan J, Luik RM, Lewis RS (2006) Ca2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J Cell Biol 174:803-813
111. Frieden M, Arnaudeau S, Castelbou C, Demaurex N (2005) Subplasmalemmal mitochondria modulate the activity of plasma membrane Ca2 + -ATPases. J Biol Chem 280:43198-43208
112. Koziel K, Lebiedzinska M, Szabadkai G, Onopiuk M, Brutkowski W, Wierzbicka K, Wilczynski G, Pinton P, Duszynski J, Zablocki K, Wieckowski MR (2009) Plasma membrane associated membranes (PAM) from Jurkat cells contain STIM1 protein is PAM involved in the capacitative calcium entry? Int J Biochem Cell Biol 41:2440-2449
113. Piccini M, Vitelli F, Bruttini M, Pober BR, Jonsson JJ, Villanova M, Zollo M, Borsani G, Ballabio A, Renieri A (1998) FACL4, a new gene encoding long-chain acyl-CoA synthetase 4, is deleted in a family with Alport syndrome, elliptocytosis, and mental retardation. Genomics 47:350-358
114. Stone SJ, Vance JE (2000) Phosphatidylserine synthase-1 and -2 are localized to mitochondria-associated membranes. J Biol Chem 275:34534-34540
115. Lebiedzinska M, Szabadkai G, Jones AW, Duszynski J, Wieckowski MR (2009) Interactions between the endoplasmic reticulum, mitochondria, plasma membrane and other subcellular organelles. Int J Biochem Cell Biol 41:1805-1816
116. Hayashi T, Rizzuto R, Hajnoczky G, Su TP (2009) MAM: more than just a housekeeper. Trends Cell Biol 19:81-88
117. Giorgi C, De Stefani D, Bononi A, Rizzuto R, Pinton P (2009) Structural and functional link between the mitochondrial network and the endoplasmic reticulum. Int J Biochem Cell Biol 41:1817-1827
118. Decuypere JP, Monaco G, Bultynck G, Missiaen L, De Smedt H, Parys JB (2011) The IP(3) receptor-mitochondria connection in apoptosis and autophagy. Biochim Biophys Acta 1813:1003-1013
119. Mendes CC, Gomes DA, Thompson M, Souto NC, Goes TS, Goes AM, Rodrigues MA, Gomez MV, Nathanson MH, Leite MF (2005) The type III inositol 1,4,5-trisphosphate receptor preferentially transmits apoptotic Ca2+ signals into mitochondria. J Biol Chem 280:40892-40900
120. Hajnoczky G, Robb-Gaspers LD, Seitz MB, Thomas AP (1995) Decoding of cytosolic calcium oscillations in the mitochondria. Cell 82:415-424
121. Rizzuto R, Duchen MR, Pozzan T (2004) Flirting in little space: the ER/mitochondria Ca2+ liaison. Sci STKE 2004:re1
122. Walter L, Hajnoczky G (2005) Mitochondria and endoplasmic reticulum: the lethal interorganelle cross-talk. J Bioenerg Biomembr 37:191-206
123. Green DR, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305:626-629
124. Bernardi P, Rasola A (2007) Calcium and cell death: the mitochondrial connection. Subcell Biochem 45:481-506
125. Garcia-Perez C, Hajnoczky G, Csordas G (2008) Physical coupling supports the local Ca2+ transfer between sarcoplasmic reticulum subdomains and the mitochondria in heart muscle. J Biol Chem 283:32771-32780
126. Pacher P, Sharma K, Csordas G, Zhu Y, Hajnoczky G (2008) Uncoupling of ER-mitochondrial calcium communication by transforming growth factor-beta. Am J Physiol Renal Physiol 295:F1303-F1312
127. Szabadkai G, Bianchi K, Varnai P, De Stefani D, Wieckowski MR, Cavagna D, Nagy AI, Balla T, Rizzuto R (2006) Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J Cell Biol 175:901-911
128. Rapizzi E, Pinton P, Szabadkai G, Wieckowski MR, Vandecasteele G, Baird G, Tuft RA, Fogarty KE, Rizzuto R (2002) Recombinant expression of the voltage-dependent anion channel enhances the transfer of Ca2+ microdomains to mitochondria. J Cell Biol 159:613-624
129. De Stefani D, Bononi A, Romagnoli A, Messina A, De Pinto V, Pinton P, Rizzuto R (2011) VDAC1 selectively transfers apoptotic Ca(2+) signals to mitochondria. Cell Death Differ 2011 Jul 1. doi: 10.1038/cdd.2011.92. [Epub ahead of print]
130. Roderick HL, Lechleiter JD, Camacho P (2000) Cytosolic phosphorylation of calnexin controls intracellular Ca(2+) oscillations via an interaction with SERCA2b. J Cell Biol 149: 1235-1248
131. Camacho P, Lechleiter JD (1995) Calreticulin inhibits repetitive intracellular Ca2+ waves. Cell 82:765-771
132. Michalak M, Groenendyk J, Szabo E, Gold LI, Opas M (2009) Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem J 417:651-666
133. Molinari M, Eriksson KK, Calanca V, Galli C, Cresswell P, Michalak M, Helenius A (2004) Contrasting functions of calreticulin and calnexin in glycoprotein folding and ER quality control. Mol Cell 13:125-135
134. Simmen T, Aslan JE, Blagoveshchenskaya AD, Thomas L, Wan L, Xiang Y, Feliciangeli SF, Hung CH, Crump CM, Thomas G (2005) PACS-2 controls endoplasmic reticulummitochondria communication and Bid-mediated apoptosis. EMBO J 24:717-729
135. Kottgen M, Benzing T, Simmen T, Tauber R, Buchholz B, Feliciangeli S, Huber TB, Schermer B, Kramer-Zucker A, Hopker K, Simmen KC, Tschucke CC, Sandford R, Kim E, Thomas G, Walz G (2005) Trafficking of TRPP2 by PACS proteins represents a novel mechanism of ion channel regulation. EMBO J 24:705-716
136. Myhill N, Lynes EM, Nanji JA, Blagoveshchenskaya AD, Fei H, Carmine Simmen K, Cooper TJ, Thomas G, Simmen T (2008) The subcellular distribution of calnexin is mediated by PACS-2. Mol Biol Cell 19:2777-2788
137. Breckenridge DG, Stojanovic M, Marcellus RC, Shore GC (2003) Caspase cleavage product of BAP31 induces mitochondrial fi ssion through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J Cell Biol 160:1115-1127
138. Bui M, Gilady SY, Fitzsimmons RE, Benson MD, Lynes EM, Gesson K, Alto NM, Strack S, Scott JD, Simmen T (2010) Rab32 modulates apoptosis onset and mitochondria-associated membrane (MAM) properties. J Biol Chem 285:31590-31602
139. Hayashi T, Su TP (2007) Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 131:596-610
140. Maurice T, Su TP (2009) The pharmacology of sigma-1 receptors. Pharmacol Ther 124:195-206
141. Aydar E, Palmer CP, Djamgoz MB (2004) Sigma receptors and cancer: possible involvement of ion channels. Cancer Res 64:5029-5035
142. Marrazzo A, Caraci F, Salinaro ET, Su TP, Copani A, Ronsisvalle G (2005) Neuroprotective effects of sigma-1 receptor agonists against beta-amyloid-induced toxicity. Neuroreport 16:1223-1226
143. Vagnerova K, Hurn PD, Bhardwaj A, Kirsch JR (2006) Sigma 1 receptor agonists act as neuroprotective drugs through inhibition of inducible nitric oxide synthase. Anesth Analg 103:430-434, table of contents
144. Spruce BA, Campbell LA, McTavish N, Cooper MA, Appleyard MV, O'Neill M, Howie J, Samson J, Watt S, Murray K, McLean D, Leslie NR, Safrany ST, Ferguson MJ, Peters JA, Prescott AR, Box G, Hayes A, Nutley B, Raynaud F, Downes CP, Lambert JJ, Thompson AM, Eccles S (2004) Small molecule antagonists of the sigma-1 receptor cause selective release of the death program in tumor and self-reliant cells and inhibit tumor growth in vitro and in vivo. Cancer Res 64:4875-4886
145. Higo T, Hattori M, Nakamura T, Natsume T, Michikawa T, Mikoshiba K (2005) Subtypespecific and ER lumenal environment-dependent regulation of inositol 1,4,5-trisphosphate receptor type 1 by ERp44. Cell 120:85-98
146. Li G, Mongillo M, Chin KT, Harding H, Ron D, Marks AR, Tabas I (2009) Role of ERO1-alpha-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis. J Cell Biol 186:783-792
147. Szalai G, Krishnamurthy R, Hajnoczky G (1999) Apoptosis driven by IP(3)-linked mitochondrial calcium signals. EMBO J 18:6349-6361
148. Gilady SY, Bui M, Lynes EM, Benson MD, Watts R, Vance JE, Simmen T (2010) Ero1alpha requires oxidizing and normoxic conditions to localize to the mitochondria-associated membrane (MAM). Cell Stress Chaperones 15:619-629
149. Cartoni R, Martinou JC (2009) Role of mitofusin 2 mutations in the physiopathology of Charcot-Marie-Tooth disease type 2A. Exp Neurol 218:268-273
150. Guo X, Chen KH, Guo Y, Liao H, Tang J, Xiao RP (2007) Mitofusin 2 triggers vascular smooth muscle cell apoptosis via mitochondrial death pathway. Circ Res 101:1113-1122
151. Vecchione A, Fassan M, Anesti V, Morrione A, Goldoni S, Baldassarre G, Byrne D, D'Arca D, Palazzo JP, Lloyd J, Scorrano L, Gomella LG, Iozzo RV, Baffa R (2009) MITOSTATIN, a putative tumor suppressor on chromosome 12q24.1, is downregulated in human bladder and breast cancer. Oncogene 28:257-269
152. Cerqua C, Anesti V, Pyakurel A, Liu D, Naon D, Wiche G, Baffa R, Dimmer KS, Scorrano L (2010) Trichoplein/mitostatin regulates endoplasmic reticulum-mitochondria juxtaposition. EMBO Rep 11:854-860
153. Iwasawa R, Mahul-Mellier AL, Datler C, Pazarentzos E, Grimm S (2011) Fis1 and Bap31 bridge the mitochondria-ER interface to establish a platform for apoptosis induction. EMBO J 30:556-568
154. Celsi F, Pizzo P, Brini M, Leo S, Fotino C, Pinton P, Rizzuto R (2009) Mitochondria, calcium and cell death: a deadly triad in neurodegeneration. Biochim Biophys Acta 1787:335-344
155. Contreras L, Drago I, Zampese E, Pozzan T (2010) Mitochondria: the calcium connection. Biochim Biophys Acta 1797:607-618
156. Area-Gomez E, de Groof AJ, Boldogh I, Bird TD, Gibson GE, Koehler CM, Yu WH, Duff KE, Yaffe MP, Pon LA, Schon EA (2009) Presenilins are enriched in endoplasmic reticulum membranes associated with mitochondria. Am J Pathol 175:1810-1816
157. Zampese E, Fasolato C, Kipanyula MJ, Bortolozzi M, Pozzan T, Pizzo P (2011) Presenilin 2 modulates endoplasmic reticulum (ER)-mitochondria interactions and Ca2+ cross-talk. Proc Natl Acad Sci USA 108:2777-2782
158. Smith IF, Green KN, LaFerla FM (2005) Calcium dysregulation in Alzheimer's disease: recent advances gained from genetically modified animals. Cell Calcium 38:427-437
159. Small DH (2009) Dysregulation of calcium homeostasis in Alzheimer's disease. Neurochem Res 34:1824-1829
160. Yu JT, Chang RC, Tan L (2009) Calcium dysregulation in Alzheimer's disease: from mechanisms to therapeutic opportunities. Prog Neurobiol 89:240-255
161. Sano R, Annunziata I, Patterson A, Moshiach S, Gomero E, Opferman J, Forte M, d'Azzo A (2009) GM1-ganglioside accumulation at the mitochondria-associated ER membranes links ER stress to Ca(2+)-dependent mitochondrial apoptosis. Mol Cell 36:500-511
162. d'Azzo A, Tessitore A, Sano R (2006) Gangliosides as apoptotic signals in ER stress response. Cell Death Differ 13:404-414
163. Wu G, Lu ZH, Obukhov AG, Nowycky MC, Ledeen RW (2007) Induction of calcium influx through TRPC5 channels by cross-linking of GM1 ganglioside associated with alpha5beta1 integrin initiates neurite outgrowth. J Neurosci 27:7447-7458
164. Szado T, Vanderheyden V, Parys JB, De Smedt H, Rietdorf K, Kotelevets L, Chastre E, Khan F, Landegren U, Soderberg O, Bootman MD, Roderick HL (2008) Phosphorylation of inositol 1,4,5-trisphosphate receptors by protein kinase B/Akt inhibits Ca2+ release and apoptosis. Proc Natl Acad Sci USA 105:2427-2432
165. Marchi S, Rimessi A, Giorgi C, Baldini C, Ferroni L, Rizzuto R, Pinton P (2008) Akt kinase reducing endoplasmic reticulum Ca2+ release protects cells from Ca2 + -dependent apoptotic stimuli. Biochem Biophys Res Commun 375:501-505
166. Giorgi C, Ito K, Lin HK, Santangelo C, Wieckowski MR, Lebiedzinska M, Bononi A, Bonora M, Duszynski J, Bernardi R, Rizzuto R, Tacchetti C, Pinton P, Pandolfi PP (2010) PML regulates apoptosis at endoplasmic reticulum by modulating calcium release. Science 330:1247-1251
167. Pinton P, Giorgi C, Pandolfi PP (2011) The role of PML in the control of apoptotic cell fate: a new key player at ER-mitochondria sites. Cell Death Differ 18:1450-1456
168. Lebiedzinska M, Duszynski J, Rizzuto R, Pinton P, Wieckowski MR (2009) Age-related changes in levels of p66Shc and serine 36-phosphorylated p66Shc in organs and mouse tissues. Arch Biochem Biophys 486:73-80
169. Bozidis P, Williamson CD, Colberg-Poley AM (2008) Mitochondrial and secretory human cytomegwalovirus UL37 proteins Traffic into mitochondrion- associated membranes of human cells. J Virol 82:2715-2726
170. Sheikh MY, Choi J, Qadri I, Friedman JE, Sanyal AJ (2008) Hepatitis C virus infection: molecular pathways to metabolic syndrome. Hepatology 47:2127-2133
171. Criollo A, Maiuri MC, Tasdemir E, Vitale I, Fiebig AA, Andrews D, Molgo J, Diaz J, Lavandero S, Harper F, Pierron G, di Stefano D, Rizzuto R, Szabadkai G, Kroemer G (2007) Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Differ 14:1029-1039
172. Cardenas C, Miller RA, Smith I, Bui T, Molgo J, Muller M, Vais H, Cheung KH, Yang J, Parker I, Thompson CB, Birnbaum MJ, Hallows KR, Foskett JK (2010) Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell 142:270-283
173. Levine B, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132:27-42