Calcium and ATP handling in human NADH:Ubiquinone oxidoreductase deficiency

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1792, Issue 12, 2009, Pages 1130-1137

  Valsecchi, Federica ^a,b   Esseling, John J ^a   Koopman, Werner J H ^a   Willems, Peter H G M ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Complex I; Fibroblasts; Life cell microscopy; Mitochondria; ROS

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; CALRETICULIN; CELL NUCLEUS DNA; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

CALCIUM SIGNALING; CALCIUM TRANSPORT; COMPLEX I DEFICIENCY; CYTOSOL; ENDOPLASMIC RETICULUM; GENE MUTATION; HUMAN; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; REVIEW; SKIN FIBROBLAST;

ADENOSINE TRIPHOSPHATE; CALCIUM; ELECTRON TRANSPORT COMPLEX I; HUMANS; MITOCHONDRIAL DISEASES;

EID: 71949124041     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2009.01.001     Document Type: Review

References (89)

1. Alonso M.T., Villalobos C., Chamero P., Alvarez J., and García-Sancho J. Calcium microdomains in mitochondria and nucleus. Cell Calcium 40 (2006) 513-525
2. Barghuti F., Elian K., Gomori J.M., Shaag A., Edvardson S., Saada A., and Elpeleg O. The unique neuroradiology of complex I deficiency due to NDUFA12L defect. Mol. Genet. Metab. 94 (2008) 78-82
3. Baumann O., and Walz B. Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int. Rev. Cyt. 205 (2001) 149-214
4. Benard G., and Rossignol R. Ultrastructure of the mitochondrion and its bearing on function and bioenergetics. Antioxid. Redox Signal. 10 (2008) 1313-1342
5. Berger I., Hershkovitz E., Shaag A., Edvardson S., Saada A., and Elpeleg O. Mitochondrial complex I deficiency caused by a deleterious NDUFA11 mutation. Ann. Neurol. 63 (2008) 405-408
6. Berridge M.J. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32 (2002) 235-349
7. Bigelow D.J., and Squier T.C. Redox modulation of cellular signaling and metabolism through reversible oxidation of methionine sensors in calcium regulatory proteins. Biochim. Biophys. Acta 1703 (2005) 121-134
8. Brandt U. Energy converting NADH:quinone oxidoreductase (complex I). Annu. Rev. Biochem. 75 (2006) 69-92
9. Brini M., Pinton P., King M.P., Davidson M., Schon E.A., and Rizzuto R. A calcium signaling defect in the pathogenesis of a mitochondrial DNA inherited oxidative phosphorylation deficiency. Nat. Med. 5 (1999) 951-954
10. Burdakov D., Petersen O.H., and Verkhratsky A. Intraluminal calcium as a primary regulator of endoplasmic reticulum function. Cell Calcium 38 (2005) 303-310
11. 2+ signal. J. Biol. Chem. 276 (2001) 26411-26420
12. Condreay J.P., and Kost T.A. Baculovirus expression vectors for insect and mammalian cells. Curr. Drug Targets 8 (2007) 1126-1131
13. Csordás G., Renken C., Várnai P., Walter L., Weaver D., Buttle K.F., Balla T., Mannella C.A., and Hajnóczky G. Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 174 (2006) 915-921
14. Dieteren C.E.J., Willems P.H.G.M., Vogel R.O., Swarts H.G., Fransen J., Roepman R., Crienen G., Smeitink J.A.M., Nijtmans L.G.J., and Koopman W.J.H. Subunits of mitochondrial complex I exist as part of matrix- and membrane-associated subcomplexes in living cells. J. Biol. Chem. 283 (2008) 34753-34761
15. Distelmaier F., Koopman W.J.H., Testa E.R., de Jong A.S., Swarts H.G., Mayatepek E., Smeitink J.A.M., and Willems P.H.G.M. Life cell quantification of mitochondrial membrane potential at the single organelle level. Cytometry, Part A 73 (2008) 129-138
16. Droge W. Free radicals in the physiological control of cell function. Physiol. Rev. 82 (2002) 47-95
17. Dunning C.J., McKenzie M., Sugiana C., Lazarou M., Silke J., Connelly A., Fletcher J.M., Kirby D.M., Thorburn D.R., and Ryan M.T. Human CIA30 is involved in the early assembly of mitochondrial complex I and mutations in its gene cause disease. EMBO J. 26 (2007) 3227-3237
18. 2+ oscillations: a simple model. Cell Calcium 34 (2003) 485-497
19. Fernandez-Moreira D., Ugalde C., Smeets R., Rodenburg R.J., Lopez-Laso E., Ruiz-Falco M.L., Briones P., Martin M.A., Smeitink J.A.M., and Arenas J. X-linked NDUFA1 gene mutations associated with mitochondrial encephalomyopathy. Ann. Neurol. 61 (2007) 73-83
20. Filippin L., Magalhães 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
21. 2+ release channels. Physiol. Rev. 87 (2007) 593-658
22. Franzini-Armstrong C. ER-mitochondria communication. How privileged?. Physiology 22 (2007) 261-268
23. 2+-ATPases. J. Biol. Chem. 280 (2005) 43198-43208
24. 2+-binding chaperone of the endoplasmic reticulum. Int. J. Biochem. Cell Biol. 37 (2005) 260-266
25. 2+ oscillations and for their frequency encoding through protein phosphorylation. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 1461-1465
26. Gorlach A., Klappa P., and Kietzmann T. The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid. Redox Signal. 8 (2006) 1391-1418
27. Groenendyk J., and Michalak M. Endoplasmic reticulum quality control and apoptosis. Acta Biochim. Pol. 52 (2005) 381-395
28. 2+ signaling and cell survival. Cell 131 (2007) 596-610
29. 2+ oscillations. Cell Calcium 40 (2006) 53-61
30. Hoefs S.J., Dieteren C.E., Distelmaier F., Janssen R.J., Epplen A., Swarts H.G., Forkink M., Rodenburg R.J., Nijtmans L.G.J., Willems P.H.G.M., Smeitink J.A.M., and van den Heuvel L.P. NDUFA2 complex I mutation leads to Leigh disease. Am. J. Hum. Genet. 82 (2008) 1306-1315
31. Hool L.C., and Corry B. Redox control of calcium channels: from mechanisms to therapeutic opportunities. Antioxid. Redox Signal. 9 (2007) 409-435
32. Janssen R.J., Nijtmans L.G.J., van de Heuvel L.W.P.J., and Smeitink J.A.M. Mitochondrial complex I: structure, function and pathology. J. Inherit. Metab. Dis. 29 (2006) 499-515
33. Jouaville L.S., Pinton P., Bastianutto C., Rutter G.A., and Rizzuto R. Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 13807-13812
34. Klingenberg M. The ADP and ATP transport in mitochondria and its carrier. Biochim. Biophys. Acta 1778 (2008) 1978-2021
35. 2+ leak across the endoplasmic reticular membrane. J. Biol. Chem. 278 (2003) 13672-13679
36. 2+ buffering. Cell Calcium 38 (2005) 152-154
37. Koopman W.J.H., Visch H.J., Verkaart S., van den Heuvel L.W., Smeitink J.A.M., and Willems P.H.G.M. Mitochondrial network complexity and pathological decrease in complex I activity are tightly correlated in isolated human complex I deficiency. Am. J. Physiol., Cell Physiol. 289 (2005) C881-C890
38. Koopman W.J.H., Verkaart S., van Emst-de Vries S.E., Grefte S., Smeitink J.A.M., and Willems P.H.G.M. Simultaneous quantification of oxidative stress and cell spreading using 5-(and-6)-chloromethyl-2′,7′-dichlorofluorescein. Cytometry, Part A 69 (2006) 1184-1192
39. Koopman W.J.H., Verkaart S., Visch H.J., van Emst-de Vries S.E., Nijtmans L.G.J., Smeitink J.A.M., and Willems P.H.G.M. Human NADH: oxidoreductase deficiency: radical changes in mitochondrial morphology?. Am. J. Physiol., Cell Physiol. 293 (2007) C22-C29
40. Koopman W.J.H., Distelmaier F., Hink M.A., verkaart S., Wijers M., Fransen J., Smeitink J.A.M., and Willems P.H.G.M. Inherited complex I deficiency is associated with faster protein diffusion in the matrix of moving mitochondria. Am. J. Physiol., Cell Physiol. 294 (2008) C1124-C1132
41. Koopman W.J.H., Verkaart S., van Emst-de Vries S.E., Grefte S., Smeitink J.A.M., Nijtmans L.G.J., and Willems P.H.G.M. Mitigation of NADH: ubiquinone oxidoreductase deficiency by chronic Trolox treatment. Biochim. Biophys. Acta 1777 (2008) 853-859
42. Koopman W.J.H., Distelmaier F., Esseling J.J., Smeitink J.A.M., and Willems P.H.G.M. Computer-assisted live cell analysis of mitochondrial membrane potential, morphology and calcium handling. Methods 46 (2008) 304-311
43. Korzeniewski B. Regulation of oxidative phosphorylation through parallel activation. Biophys. Chem. 129 (2007) 93-110
44. Lazarou M., Thorburn D.R., Ryan M.T., and McKenzie M. Assembly of mitochondrial complex I and defects in disease. Biochim. Biophys. Acta. 1793 (2009) 78-88
45. Maack C., O B., and Rourke. Excitation-contraction coupling and mitochondrial energetics. Basic Res. Cardiol. 102 (2007) 369-392
46. Martins de Brito O., and Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456 (2008) 605-610
47. Matson M.P. Calcium and neurodegeneration. Aging Cell 6 (2007) 337-350
48. 2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium 32 (2002) 269-278
49. 2+ channel: from discovery to new signaling concepts. J. Neurochem. 102 (2007) 1426-1446
50. Morgan-Hughes J.A., Darveniza P., Landon D.N., Land J.M., and Clark J.B. A mitochondrial myopathy with a deficiency of respiratory chain NADH-CoQ reductase activity. J. Neurol. Sci. 43 (1979) 27-46
51. Ogilvie I., Kennaway N.G., and Shoubridge E.A. A molecular chaperone for mitochondrial complex I assembly is mutated in a progressive encephalopathy. J. Clin. Invest. 115 (2005) 2784-2792
52. Pacher P., Sharma K., Csordás G., Zhu Y., and Hajnóczky G. Uncoupling of ER-Mitochondrial calcium Communication by transforming growth factor-β. Am. J. Physiol. Renal. Physiol. 295 (2008) F1303-F1312
53. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., Hill D.E., Vidal M., Evans J.G., Thorburn D.R., Carr S.A., and Mootha V.K. A mitochondrial protein compendium elucidates complex I disease biology. Cell 134 (2008) 112-123
54. Pizzo P., and Pozzan T. Mitochondria-endoplasmic reticulum choreography: structure and signaling dynamics. Trends Cell Biol. 17 (2007) 511-517
55. 2+ microdomains to mitochondria. J. Cell Biol. 159 (2002) 613-624
56. 2+ release: an intimate connection. Trends Biochem. Sci. 25 (2000) 215-221
57. 2+ responses. Science 280 (1998) 1763-1766
58. 2+ from the endoplasmic reticulum to mitochondria: is spatial intimacy enough?. Biochem. Soc. Trans. 34 (2006) 351-355
59. Saada A., Edvardson S., Rapoport M., Shaag A., Amry K., Miller C., Lorberboum-Galski H., and Elpeleg O. C6ORF66 is an assembly factor of mitochondrial complex I. Am. J. Hum. Genet. 82 (2008) 32-38
60. 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. PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis. EMBO J. 24 (2005) 717-729
61. Smeitink J.A.M., van de Heuvel L.W.P.J., Koopman W.J.H., Nijtmans L.G.J., Ugalde C., and Willems P.H.G.M. Cell biological consequences of mitochondrial NADH: ubiquinone oxidoreductase deficiency. Curr. Neurovasc. Res. 1 (2004) 29-40
62. Smeitink J.A.M., van den Heuvel L.W.P.J., and DiMauro S. The genetics and pathology of oxidative phosphorylation. Nat. Rev., Genet. 2 (2001) 342-352
63. Spat A., Szanda G., Csordas G., and Hajnoczky G. High- and low-calcium-dependent mechanisms of mitochondrial calcium signalling. Cell Calcium 44 (2008) 51-63
64. Sugiana C., Pagliarini D.J., McKenzie M., Kirby D.M., Salemi R., Abu-Amero K.K., Dahl H.H., Hutchison W.M., Vascotto K.A., Smith S.M., Newbold R.F., Christodoulou J., Calvo S., Mootha V.K., Ryan M.T., and Thorburn D.R. Mutation of C20orf7 disrupts complex I assembly and causes lethal neonatal mitochondrial disease. Am. J. Hum. Genet. 83 (2008) 468-478
65. Squier T.C., and Bigelow D.J. Protein oxidation and age-dependent alterations in calcium homeostasis. Front. Biosci. 1 (2000) D504-D526
66. Szabo E., Qiu Y., Baksh S., Michalak M., and Opas M. Calreticulin inhibits commitment to adipocyte differentiation. J. Cell Biol. 182 (2008) 103-116
67. 2+ channels. J. Cell Biol. 175 (2006) 901-911
68. 1-ATPase. Am. J. Physiol., Cell Physiol. 278 (2000) C423-C435
69. 2+ oscillations. Europhys. Lett. 55 (2001) 746-752
70. Trachootham D., Lu W., Ogasawara M.A., Nilsa R.D., and Huang P. Redox regulation of cell survival. Antioxid. Redox Signal. 10 (2008) 1343-1374
71. 2+ uniport. Nat. Cell Biol. 9 (2007) 445-452
72. Trombetta E.S., and Parodi A.J. Quality control and protein folding in the secretory pathway. Annu. Rev. Cell Dev. Biol. 19 (2003) 649-766
73. Twig G., Graf S.A., Wikstrom J.D., Mohamed H., Haigh S.E., Elorza A., Deutsch M., Zurgil N., Reynolds N., and Shirih O.S. Tagging and tracking individual networks within a complex mitochondrial web with photoactivatable GFP. Am. J. Physiol., Cell Physiol. 291 (2006) C176-C184
74. Ugalde C., Janssen R.J., van den Heuvel L.P., Smeitink J.A.M., and Nijtmans L.G.J. Differences in assembly or stability of complex I and other mitochondrial OXPHOS complexes in inherited complex I deficiency. Hum. Mol. Genet. 13 (2004) 659-667
75. Valero R.A., Senovilla L., Nunez L., and Villalobos C. The role of mitochondrial potential in control of calcium signals involved in cell proliferation. Cell Calcium 44 (2008) 259-269
76. 2+ oscillations in HeLa cells and fibroblasts by mitochondrial Ca(2+) uniporter stimulation. J. Physiol. 580 (2007) 39-49
77. Verkaart S., Koopman W.J.H., van Emst-de Vries S.E., Nijtmans L.G.J., van den Heuvel L.W., Smeitink J.A.M., and Willems P.H.G.M. Superoxide production is inversely related to complex I activity in inherited complex I deficiency. Biochim. Biophys. Acta 1772 (2007) 373-381
78. Verkaart S., Koopman W.J.H., Cheek J., van Emst-de Vries S.E., van den Heuvel L.W.P.J., Smeitink J.A.M., and Willems P.H.G.M. Mitochondrial and cytosolic thiol redox state are not detectably altered in isolated human NADH:ubiquinone oxidoreductase deficiency. Biochim. Biophys. Acta 1772 (2007) 1041-1051
79. 2+ handling in human complex I deficiency. J. Biol. Chem. 279 (2004) 40328-40336
80. Visch H.J., Koopman W.J.H., Leusink A., van Emst-de Vries S.E., van den Heuvel L.W.P.J., Willems P.H.G.M., and Smeitink J.A.M. Decreased agonist-stimulated mitochondrial ATP production caused by a pathological reduction in endoplasmic reticulum calcium content in human complex I deficiency. Biochim. Biophys. Acta 1762 (2006) 115-123
81. 2+ removal: aberrations in human complex I deficiency. Am. J. Physiol., Cell Physiol. 291 (2006) C308-316
82. Vogel R.O., Janssen R.J., van den Brand M.A., Dieteren C.E., Verkaart S., Koopman W.J.H., Willems P.H.G.M., Pluk W., van den Heuvel L.P., Smeitink J.A.M., and Nijtmans L.G.J. Cytosolic signaling protein Ecsit also localizes to mitochondria where it interacts with chaperone NDUFAF1 and functions in complex I assembly. Genes Dev. 21 (2007) 615-624
83. Vogel R.O., Smeitink J.A.M., and Nijtmans L.G.J. Human mitochondrial complex I assembly: a dynamic and versatile process. Biochim. Biophys. Acta 1767 (2007) 1215-1227
84. 2+ homeostasis in respiratory chain-deficient cells but efficient compensation of energetic disadvantage by enhanced anaerobic glycolysis due to low ATP steady state levels. Exp. Cell Res. 313 (2007) 3076-3089
85. Wang H.J., Guay G., Pogan L., Sauvé R., and Nabi I.R. Calcium regulates the association between mitochondria and a smooth subdomain of the endoplasmic reticulum. J. Cell. Biol. 150 (2000) 1489-1498
86. Waring P. Redox active calcium ion channels and cell death. Arch. Biochem. Biophys. 434 (2005) 33-42
87. 2tavi+ signal transmission between the ER and mitochondria. Biochem. Biophys. Res. Commun. 348 (2006) 393-399
88. 2+ homeostasis in human NADH:ubiquinone oxidoreductase. Cell Calcium 44 (2008) 123-133
89. Tavi P., Hansson A., Zhang S.J., Larsson N.G., and Westerblad H. Abnormal Ca(2+) release and catecholamine-induced arrhythmias in mitochondrial cardiomyopathy. Hum. Mol. Genet. 14 (2005) 1069-1076