Structural and functional link between the mitochondrial network and the endoplasmic reticulum

International Journal of Biochemistry and Cell Biology

Volumn 41, Issue 10, 2009, Pages 1817-1827

  Giorgi, Carlotta ^a,b   De Stefani, Diego ^a   Bononi, Angela ^a   Rizzuto, Rosario ^c   Pinton, Paolo ^a  

^a Interdisciplinary Center for the Study of Inflammation   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c UNIVERSITY OF PADOVA   (Italy)

Author keywords

Apoptosis; Calcium; ER stress; ER: endoplasmic reticulum; MAM: mitochondria associated membranes; Mitochondria

Indexed keywords

CALCIUM; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR;

APOPTOSIS; BIOENERGY; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL CONTACT; CELL FATE; CELL STRESS; CELL SURVIVAL; CELL TYPE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HOMEOSTASIS; HUMAN; MACROMOLECULE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NONHUMAN; REVIEW;

ANIMALS; APOPTOSIS; CALCIUM SIGNALING; ENDOPLASMIC RETICULUM; HUMANS; MITOCHONDRIA; MODELS, BIOLOGICAL;

EID: 69049098806     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2009.04.010     Document Type: Review

References (107)

1. Alirol E., James D., Huber D., Marchetto A., Vergani L., Martinou J.C., et al. The mitochondrial fission protein hFis1 requires the endoplasmic reticulum gateway to induce apoptosis. Mol Biol Cell 17 (2006) 4593-4605
2. Anesti V., and Scorrano L. The relationship between mitochondrial shape and function and the cytoskeleton. Biochim Biophys Acta 1757 (2006) 692-699
3. Assefa Z., Bultynck G., Szlufcik K., Nadif K.N., Vermassen E., Goris J., et al. Caspase-3-induced truncation of type 1 inositol trisphosphate receptor accelerates apoptotic cell death and induces inositol trisphosphate-independent calcium release during apoptosis. J Biol Chem 279 (2004) 43227-43236
4. Bayrhuber M., Meins T., Habeck M., Becker S., Giller K., Villinger S., Vonrhein C., Griesinger C., Zweckstetter M., and Zeth K. Structure of the human voltage-dependent anion channel. Proc Natl Acad Sci USA 105 (2008) 15370-15375
5. Berridge M.J. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32 (2002) 235-249
6. Blackshaw S., Sawa A., Sharp A.H., Ross C.A., Snyder S.H., and Khan A.A. Type 3 inositol 1,4,5-trisphosphate receptor modulates cell death. FASEB J 14 (2000) 1375-1379
7. Boehning D., Patterson R.L., Sedaghat L., Glebova N.O., Kurosaki T., and Snyder S.H. Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat Cell Biol 5 (2003) 1051-1061
8. 2+ waves in rat cortical astrocytes. J Cell Biol 145 (1999) 795-808
9. Bootman M.D., Petersen O.H., and Verkhratsky A. The endoplasmic reticulum is a focal point for co-ordination of cellular activity. Cell Calcium 32 (2002) 231-234
10. Borgese N., Francolini M., and Snapp E. Endoplasmic reticulum architecture: structures in flux. Curr Opin Cell Biol 18 (2006) 358-364
11. Brough D., Schell M.J., and Irvine R.F. Agonist-induced regulation of mitochondrial and endoplasmic reticulum motility. Biochem J 392 (2005) 291-297
12. Chan D.C. Mitochondria: dynamic organelles in disease, aging, and development. Cell 125 (2006) 1241-1252
13. Chan D.C. Mitochondrial fusion and fission in mammals. Annu Rev Cell Dev Biol 22 (2006) 79-99
14. Chen H., Detmer S.A., Ewald A.J., Griffin E.E., Fraser S.E., and Chan D.C. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160 (2003) 189-200
15. Chevet E., Cameron P.H., Pelletier M.F., Thomas D.Y., and Bergeron J.J. The endoplasmic reticulum: integration of protein folding, quality control, signaling and degradation. Curr Opin Struct Biol 11 (2001) 120-124
16. Cipolat S., Rudka T., Hartmann D., Costa V., Serneels L., Craessaerts K., et al. Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 126 (2006) 163-175
17. Clapham D.E. Calcium signaling. Cell 131 (2007) 1047-1058
18. Csordas G., Renken C., Varnai P., Walter L., Weaver D., Buttle K.F., et al. Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174 (2006) 915-921
19. De Pinto V., Reina S., Guarino F., and Messina A. Structure of the voltage dependent anion channel: state of the art. J Bioenerg Biomembr 40 (2008) 139-147
20. Deniaud A., Sharaf el dein O., Maillier E., Poncet D., Kroemer G., Lemaire C., et al. Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis. Oncogene 27 (2008) 285-299
21. 2+ release in gastric myocytes from Bufo marinus. J Physiol 522 Pt 3 (2000) 375-390
22. Ferri K.F., and Kroemer G. Organelle-specific initiation of cell death pathways. Nat Cell Biol 3 (2001) E255-E263
23. Filippin L., Magalhaes P.J., Di Benedetto G., Colella M., and Pozzan T. Stable interactions between mitochondria and endoplasmic reticulum allow rapid accumulation of calcium in a subpopulation of mitochondria. J Biol Chem 278 (2003) 39224-39234
24. 2+ concentration within the endoplasmic reticulum. Proc Natl Acad Sci USA 97 (2000) 5723-5728
25. Frezza C., Cipolat S., Martins de Brito O., Micaroni M., Beznoussenko G.V., Rudka T., et al. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126 (2006) 177-189
26. Germain M., Mathai J.P., McBride H.M., and Shore G.C. Endoplasmic reticulum BIK initiates DRP1-regulated remodelling of mitochondrial cristae during apoptosis. EMBO J 24 (2005) 1546-1556
27. 2+ signaling, mitochondria and cell death. Curr Mol Med 8 (2008) 119-130
28. Gunter T.E., and Pfeiffer D.R. Mechanisms by which mitochondria transport calcium. Am J Physiol 258 (1990) C755-C786
29. Hajnoczky G., Csordas G., Krishnamurthy R., and Szalai G. Mitochondrial calcium signaling driven by the IP3 receptor. J Bioenerg Biomembr 32 (2000) 15-25
30. Hamilton S.L. Ryanodine receptors. Cell Calcium 38 (2005) 253-260
31. Hayashi T., and Su T.P. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 131 (2007) 596-610
32. Hiller S., Garces R.G., Malia T.J., Orekhov V.Y., Colombini M., and Wagner G. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321 (2008) 1206-1210
33. Hirota J., Furuichi T., and Mikoshiba K. Inositol 1,4,5-trisphosphate receptor type 1 is a substrate for caspase-3 and is cleaved during apoptosis in a caspase-3-dependent manner. J Biol Chem 274 (1999) 34433-34437
34. Hoyer-Hansen M., Bastholm L., Szyniarowski P., Campanella M., Szabadkai G., Farkas T., et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol Cell 25 (2007) 193-205
35. Hoyer-Hansen M., and Jaattela M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 14 (2007) 1576-1582
36. Israelson A., Zaid H., Abu-Hamad S., Nahon E., and Shoshan-Barmatz V. Mapping the ruthenium red-binding site of the voltage-dependent anion channel-1. Cell Calcium 43 (2008) 196-204
37. Jayaraman T., and Marks A.R. T cells deficient in inositol 1,4,5-trisphosphate receptor are resistant to apoptosis. Mol Cell Biol 17 (1997) 3005-3012
38. John L.M., Lechleiter J.D., and Camacho P. Differential modulation of SERCA2 isoforms by calreticulin. J Cell Biol 142 (1998) 963-973
39. 2+ release and beyond. Apoptosis 12 (2007) 951-968
40. Karbowski M., Lee Y.J., Gaume B., Jeong S.Y., Frank S., Nechushtan A., et al. Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J Cell Biol 159 (2002) 931-938
41. Kaufman R.J. Orchestrating the unfolded protein response in health and disease. J Clin Invest 110 (2002) 1389-1398
42. Khan A.A., Soloski M.J., Sharp A.H., Schilling G., Sabatini D.M., Li S.H., et al. Lymphocyte apoptosis: mediation by increased type 3 inositol 1,4,5-trisphosphate receptor. Science 273 (1996) 503-507
43. Khan M.T., Wagner L., Yule D.I., Bhanumathy C., and Joseph S.K. Akt kinase phosphorylation of inositol 1,4,5-trisphosphate receptors. J Biol Chem 281 (2006) 3731-3737
44. Kincaid M.M., and Cooper A.A. ERADicate ER stress or die trying. Antioxid Redox Signal 9 (2007) 2373-2387
45. Kirichok Y., Krapivinsky G., and Clapham D.E. The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427 (2004) 360-364
46. Kottgen M., Benzing T., Simmen T., Tauber R., Buchholz B., Feliciangeli S., et al. Trafficking of TRPP2 by PACS proteins represents a novel mechanism of ion channel regulation. EMBO J 24 (2005) 705-716
47. Kroemer G., and Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol 9 (2008) 1004-1010
48. Kusano H., Shimizu S., Koya R.C., Fujita H., Kamada S., Kuzumaki N., et al. Human gelsolin prevents apoptosis by inhibiting apoptotic mitochondrial changes via closing VDAC. Oncogene 19 (2000) 4807-4814
49. Lawen A., Ly J.D., Lane D.J., Zarschler K., Messina A., and De Pinto V. Voltage-dependent anion-selective channel 1 (VDAC1)-a mitochondrial protein, rediscovered as a novel enzyme in the plasma membrane. Int J Biochem Cell Biol 37 (2005) 277-282
50. Lebiedzinska M., Szabadkai G., Jones A.W.E., Duszynski J., and Wieckowski M.R. Interactions between the endoplasmic reticulum, mitochondria, plasma membrane and other Subcellular organelles. Int J Biochem Cell Biol 41 (2009) 1805-1816
51. Lee A.C., Xu X., and Colombini M. The role of pyridine dinucleotides in regulating the permeability of the mitochondrial outer membrane. J Biol Chem 271 (1996) 26724-26731
52. Li C., Wang X., Vais H., Thompson C.B., Foskett J.K., and White C. Apoptosis regulation by Bcl-x(L) modulation of mammalian inositol 1,4,5-trisphosphate receptor channel isoform gating. Proc Natl Acad Sci USA 104 (2007) 12565-12570
53. 2+-release channel function. Biochem J 337 Pt 3 (1999) 345-361
54. Malhotra J.D., Miao H., Zhang K., Wolfson A., Pennathur S., Pipe S.W., et al. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc Natl Acad Sci USA 105 (2008) 18525-18530
55. Mannella C.A., Buttle K., Rath B.K., and Marko M. Electron microscopic tomography of rat-liver mitochondria and their interaction with the endoplasmic reticulum. Biofactors 8 (1998) 225-228
56. 2+-dependent apoptotic stimuli. Biochem Biophys Res Commun 375 (2008) 501-505
57. 2+ signals into mitochondria. J Biol Chem 280 (2005) 40892-40900
58. Mikoshiba K. Inositol 1,4,5-trisphosphate IP(3) receptors and their role in neuronal cell function. J Neurochem 97 (2006) 1627-1633
59. 2+ concentration in living single rat cardiac myocytes. Am J Physiol 261 (1991) H1123-H1134
60. Nicholls D.G., and Crompton M. Mitochondrial calcium transport. FEBS Lett 111 (1980) 261-268
61. Oakes S.A., Scorrano L., Opferman J.T., Bassik M.C., Nishino M., Pozzan T., et al. Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc Natl Acad Sci USA 102 (2005) 105-110
62. Palade G. Intracellular aspects of the process of protein synthesis. Science 189 (1975) 347-358
63. 2+ analyzed with an improved genetically encoded fluorescent sensor. Proc Natl Acad Sci USA 101 (2004) 17404-17409
64. Parone P.A., James D.I., Da Cruz S., Mattenberger Y., Donze O., Barja F., et al. Inhibiting the mitochondrial fission machinery does not prevent Bax/Bak-dependent apoptosis. Mol Cell Biol 26 (2006) 7397-7408
65. Pastorino J.G., and Hoek J.B. Regulation of hexokinase binding to VDAC. J Bioenerg Biomembr 40 (2008) 171-182
66. Patel S., Joseph S.K., and Thomas A.P. Molecular properties of inositol 1,4,5-trisphosphate receptors. Cell Calcium 25 (1999) 247-264
67. Patterson R.L., Boehning D., and Snyder S.H. Inositol 1,4,5-trisphosphate receptors as signal integrators. Annu Rev Biochem 73 (2004) 437-465
68. Peng S., Blachly-Dyson E., Forte M., and Colombini M. Large scale rearrangement of protein domains is associated with voltage gating of the VDAC channel. Biophys J 62 (1992) 123-131 discussion 131-125
69. Piccini M., Vitelli F., Bruttini M., Pober B.R., Jonsson J.J., Villanova M., et al. 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 (1998) 350-358
70. Pinton P., Ferrari D., Magalhaes P., Schulze-Osthoff K., Di Virgilio F., Pozzan T., et al. Reduced loading of intracellular Ca(2+) stores and downregulation of capacitative Ca(2+) influx in Bcl-2-overexpressing cells. J Cell Biol 148 (2000) 857-862
71. 2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2 action. EMBO J 20 (2001) 2690-2701
72. 2+ transfer in the control of apoptosis. Oncogene 27 (2008) 6407-6418
73. Pizzo P., and Pozzan T. Mitochondria-endoplasmic reticulum choreography: structure and signaling dynamics. Trends Cell Biol 17 (2007) 511-517
74. 2+ responses. Science 280 (1998) 1763-1766
75. 2+: molecular determinants and functional consequences. Physiol Rev 86 (2006) 369-408
76. 2+ revealed by specifically targeted recombinant aequorin. Nature 358 (1992) 325-327
77. Rostovtseva T., and Colombini M. ATP flux is controlled by a voltage-gated channel from the mitochondrial outer membrane. J Biol Chem 271 (1996) 28006-28008
78. Rostovtseva T.K., Sheldon K.L., Hassanzadeh E., Monge C., Saks V., Bezrukov S.M., et al. Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration. Proc Natl Acad Sci USA 105 (2008) 18746-18751
79. Santel A. Get the balance right: mitofusins roles in health and disease. Biochim Biophys Acta 1763 (2006) 490-499
80. Saris N.E., and Carafoli E. A historical review of cellular calcium handling, with emphasis on mitochondria. Biochemistry (Mosc) 70 (2005) 187-194
81. Schroder M. Endoplasmic reticulum stress responses. Cell Mol Life Sci 65 (2008) 862-894
82. Schwarzer C., Barnikol-Watanabe S., Thinnes F.P., and Hilschmann N. Voltage-dependent anion-selective channel (VDAC) interacts with the dynein light chain Tctex1 and the heat-shock protein PBP74. Int J Biochem Cell Biol 34 (2002) 1059-1070
83. 2+: a control point for apoptosis. Science 300 (2003) 135-139
84. Shoshan-Barmatz V., and Gincel D. The voltage-dependent anion channel: characterization, modulation, and role in mitochondrial function in cell life and death. Cell Biochem Biophys 39 (2003) 279-292
85. Shoshan-Barmatz V., Zalk R., Gincel D., and Vardi N. Subcellular localization of VDAC in mitochondria and ER in the cerebellum. Biochim Biophys Acta 1657 (2004) 105-114
86. Smirnova E., Griparic L., Shurland D.L., and van der Bliek A.M. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol Biol Cell 12 (2001) 2245-2256
87. Song J., Midson C., Blachly-Dyson E., Forte M., and Colombini M. The sensor regions of VDAC are translocated from within the membrane to the surface during the gating processes. Biophys J 74 (1998) 2926-2944
88. Stone S.J., and Vance J.E. Phosphatidylserine synthase-1 and -2 are localized to mitochondria-associated membranes. J Biol Chem 275 (2000) 34534-34540
89. Suen D.F., Norris K.L., and Youle R.J. Mitochondrial dynamics and apoptosis. Genes Dev 22 (2008) 1577-1590
90. Sugawara H., Kurosaki M., Takata M., and Kurosaki T. Genetic evidence for involvement of type 1, type 2 and type 3 inositol 1,4,5-trisphosphate receptors in signal transduction through the B-cell antigen receptor. EMBO J 16 (1997) 3078-3088
91. 2+ channels. J Cell Biol 175 (2006) 901-911
92. 2+-mediated apoptosis. Mol Cell 16 (2004) 59-68
93. 2+ release and apoptosis. Proc Natl Acad Sci USA 105 (2008) 2427-2432
94. Szegezdi E., Fitzgerald U., and Samali A. Caspase-12 and ER-stress-mediated apoptosis: the story so far. Ann N Y Acad Sci 1010 (2003) 186-194
95. Tan W., and Colombini M. VDAC closure increases calcium ion flux. Biochim Biophys Acta 1768 (2007) 2510-2515
96. Tanaka A., and Youle R.J. A chemical inhibitor of DRP1 uncouples mitochondrial fission and apoptosis. Mol Cell 29 (2008) 409-410
97. Ujwal R., Cascio D., Colletier J.P., Faham S., Zhang J., Toro L., Ping P., and Abramson J. The crystal structure of mouse VDAC1 at 2,3 A resolution reveals mechanistic insights into metabolite gating. Proc Natl Acad Sci USA 105 (2008) 17742-17747
98. Vance J.E. Phospholipid synthesis in a membrane fraction associated with mitochondria. J Biol Chem 265 (1990) 7248-7256
99. Vander Heiden M.G., Chandel N.S., Schumacker P.T., and Thompson C.B. Bcl-xL prevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange. Mol Cell 3 (1999) 159-167
100. Vander Heiden M.G., Li X.X., Gottleib E., Hill R.B., Thompson C.B., and Colombini M. Bcl-xL promotes the open configuration of the voltage-dependent anion channel and metabolite passage through the outer mitochondrial membrane. J Biol Chem 276 (2001) 19414-19419
101. Verkhratsky A., and Petersen O.H. The endoplasmic reticulum as an integrating signalling organelle: from neuronal signalling to neuronal death. Eur J Pharmacol 447 (2002) 141-154
102. Waterman-Storer C.M., and Salmon E.D. Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr Biol 8 (1998) 798-806
103. White C., Li C., Yang J., Petrenko N.B., Madesh M., Thompson C.B., et al. The endoplasmic reticulum gateway to apoptosis by Bcl-X(L) modulation of the InsP3R. Nat Cell Biol 7 (2005) 1021-1028
104. Yi M., Weaver D., and Hajnoczky G. Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol 167 (2004) 661-672
105. Yuan H., Gerencser A.A., Liot G., Lipton S.A., Ellisman M., Perkins G.A., et al. Mitochondrial fission is an upstream and required event for bax foci formation in response to nitric oxide in cortical neurons. Cell Death Differ 14 (2007) 462-471
106. Zaid H., Abu-Hamad S., Israelson A., Nathan I., and Shoshan-Barmatz V. The voltage-dependent anion channel-1 modulates apoptotic cell death. Cell Death Differ 12 (2005) 751-760
107. Zhang K., and Kaufman R.J. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66 (2006) S102-S109