Mammalian complex I: A regulable and vulnerable pacemaker in mitochondrial respiratory function

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1777, Issue 7-8, 2008, Pages 719-728

  Papa, Sergio ^a,b   De Rasmo, Domenico ^a   Scacco, Salvatore ^a   Signorile, Anna ^a   Technikova Dobrova, Zuzana ^c   Palmisano, Giuseppe ^a   Sardanelli, Anna Maria ^a   Papa, Francesco ^a   Panelli, Damiano ^a   Scaringi, Raffaella ^a   Santeramo, Arcangela ^a  

^a UNIVERSITY OF BARI   (Italy)

^b CNR   (Italy)

^c INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

cAMP cascade; Complex I; Mitochondrial import; Mitochondrial phosphoproteome; PKA; Proton pump

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; OXYGEN RADICAL; PROTEIN SUBUNIT; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SERINE;

CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CELL LEVEL; CELL LINE; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE; HUMAN; MASS SPECTROMETRY; MITOCHONDRIAL RESPIRATION; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE) FE S PROTEIN 4 GENE; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; CYCLIC AMP; ELECTRON TRANSPORT COMPLEX I; HOMEOSTASIS; KINETICS; MAMMALS; MITOCHONDRIA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXYGEN CONSUMPTION; SEQUENCE HOMOLOGY, AMINO ACID;

MAMMALIA;

EID: 46349093680     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2008.04.005     Document Type: Review

References (64)

1. Hirst J., Carrol J., Fearnley I.M., Shannnon R.J., and Walker J.E. The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim. Biophys. Acta 1604 (2003) 135-150
2. Yagi T., and Matsuno-Yagi A. The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. Biochemistry 42 (2003) 2266-2274
3. Brandt U. Energy converting NADH:quinone oxidoreductase (complex I). Ann. Rev. Biochem. 75 (2006) 69-92
4. Papa S., Petruzzella V., and Scacco S. Electron transport, structure, redox-coupled protonmotive activity and pathological disorders of respiratory chain complexes. In: Lajtha A., Dienel G., and Gibson G. (Eds). Handbook of Neurochemistry and Molecular Neurobiology (2007), Springer Verlag, Berlin Heidelberg 93-118
5. Carroll J., Fearnley I.M., Skehel1 J.M., Shannon R.J., Hirst J., and Walker J.E. Bovine complex I is a complex of 45 different subunits. J. Biol. Chem 281 (2006) 32724-32727
6. Scacco S., Petruzzella V., Budde S., Vergari R., Tamborra R., Panelli D., van den Heuvel L.P., Smeitink J.A., and Papa S. Pathological mutations of the human NDUFS4 gene of the 18-kDa (AQDQ) subunit of complex I affect the expression of the protein and the assembly and function of the complex. J. Biol. Chem. 278 (2003) 44161-44167
7. Antonicka H., Ogilvie I., Taivassalo T., Anitori R.P., Haller R.G., Vissing J., Kennaway N.G., and Shoubridge E.A. Identification and characterization of a common set of complex I assembly intermediates in mitochondria from patients with complex I deficiency. J. Biol. Chem. 278 (2003) 43081-43088
8. Scheffler I.E., Yadava N., and Potluri P. Molecular genetics of complex I-deficient Chinese hamster cell lines. Biochim. Biophys. Acta 1659 (2004) 160-171
9. Fearnley I.M., Carroll J., Shannon R.J., Runswick M.J., Walker J.E., and Hirst J. GRIM-19, a cell death regulatory gene product, is a subunit of bovine mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Biol. Chem. 276 (2001) 38345-38348
10. Carrol J., Fearnley I.M., Shannon R.J., Hirst J., and Walker J.E. Analysis of the subunit composition of complex I from bovine heart mitochondria. Mol. Cell. Proteomics 2 (2003) 117-126
11. Sazanov L.A., and Hinchliffe P. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311 (2006) 1430-1436
12. Salerno J.C., and Ohnishi T. Studies on the stabilized ubisemiquinone species in the succinate-cytochrome c reductase segment of the intact mitochondrial membrane system. Biochem J. 192 (1980) 769-781
13. Wikström M., Krab K., and Saraste M. Proton-translocating cytochrome complexes. Annu. Rev. Biochem. 50 (1981) 623-655
14. Wikström M. Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone. FEBS Lett. 169 (1984) 300-304
15. Papa S., Capitanio N., and Villani G. Proton pumps of respiratory chain enzymes. In: Papa S., Guerrieri F., and Tager J.M. (Eds). Frontieres of Cellular Bioenergetics; Molecular Biology, Biochemistry and Phisiopathology (1999), Kluwer Academy-Plenum Press, New York 49-87
16. Capitanio N., Capitanio G., De Nitto E., Villani G., Minuto M., and Papa S. Variable H+/e- stoichiometry of mitochondrial respiratory chain, 36th Congress Italian Biochemical Society, Ferrara, Italy 1991, IBST Vol. 2. p98; 15th International Congress of Biochemistry, Jerusalem, Israel, August, Abstr. Vol. p.195 (1991)
17. T. Cocco, C. Pacelli, P. Sgobbo, G. Villani, Control of OXPHOS efficiency by complex I in brain mitochondria, Neurobiol Aging (2007) in press.
18. Papa S., Lorusso M., and Di Paola M. Cooperativity and flexibility of the protonmotive activity of mitochondrial respiratory chain. Biochim. Biophys. Acta 1757 (2006) 428-436
19. Ohnishi T. Iron-sulfur clusters/semiquinones in complex I. Biochim. Biophys. Acta 1363 (1998) 186-206
20. Ohnishi T., and Salerno J.C. Conformation-driven and semiquinone-gated proton-pump mechanism in the NADH-ubiquinone oxidoreductase (complex I). FEBS Lett. 579 (2005) 4555-4561
21. Mamedova A.A., Holt P.J., Carroll J., and Sazanov L.A. Substrate-induced conformational change in bacterial complex I. J. Biol. Chem. 279 (2004) 23830-23836
22. Hellwig P., Scheide D., Bungert S., Mäntele W., and Friedrich T. FT-IR spectroscopic characterization of NADH:ubiquinone oxidoreductase (complex I) from Escherichia coli: oxidation of FeS cluster N2 is coupled with the protonation of an aspartate or glutamate side chain. Biochemistry 39 (2000) 10884-10891
23. Flemming D., Schlitt A., Spehr V., Bischof T., and Friedrich T. Iron-sulfur cluster N2 of the Escherichia coli NADH:ubiquinone oxidoreductase (complex I) is located on subunit NuoB. J. Biol. Chem. 278 (2003) 47602-47609
24. Papa S., Lorusso M., and Capitanio N. Mechanistic and phenomenological features of proton pumps in the respiratory chain of mitochondria. J. Bioenerg. Biomembr. 26 (1994) 609-618
25. Scacco S., Vergari R., Scarpulla R.C., Technikova-Dobrova Z., Sardanelli A.M., Lambo R., Lorusso V., and Papa S. cAMP-dependent phosphorylation of the nuclear encoded 18-kDa (IP) subunit of respiratory complex I and activation of the complex in serum-starved mouse fibroblast cultures. J. Biol. Chem. 275 (2000) 17578-17582
26. Papa S., Scacco S., Sardanelli A.M., Vergari R., Papa F., Budde S., van den Heuvel L., and Smeitink J. Mutation in the NDUFS4 gene of complex I abolishes cAMP-dependent activation of the complex in a child with fatal neurological syndrome. FEBS Lett. 489 (2001) 259-262
27. Technikova-Dobrova Z., Sardanelli A.M., Speranza F., Scacco S., Signorile A., Lorusso V., and Papa S. Cyclic adenosine monophosphate-dependent phosphorylation of mammalian mitochondrial proteins: enzyme and substrate characterization and functional role. Biochemistry 40 (2001) 13941-13947
28. Piccoli C., Scacco S., Bellomo F., Signorile A., Iuso A., Boffoli D., Scrima R., Capitanio N., and Papa S. cAMP controls oxygen metabolism in mammalian cells. FEBS Lett. 580 (2006) 4539-4543
29. Han D., Williams E., and Cadenas E. Mitochondrial respiratory chain-dependent generation of superoxide anion and its release into the intermembrane space. Biochem J. 353 (2001) 411-416
30. Lambert A.J., and Brand M.D. Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Biol. Chem. 279 (2004) 39414-39420
31. Petruzzella V., Vergari R., Puzziferri I., Boffoli D., Lamantea E., Zeviani M., and Papa S. A nonsense mutation in the NDUFS4 gene encoding the 18 kDa (AQDQ) subunit of complex I abolishes assembly and activity of the complex in a patient with Leigh-like syndrome. Hum. Mol. Genet. 10 (2001) 529-535
32. Benit P., Steffann J., Lebon S., Chretien D., Kadhom N., de Lonlay P., Goldenberg A., Dumez Y., Dommergues M., Rustin P., Munnich A., and Rotig A. Genotyping microsatellite DNA markers at putative disease loci in inbred/multiplex families with respiratory chain complex I deficiency allows rapid identification of a novel nonsense mutation (IVS1nt-1) in the NDUFS4 gene in Leigh syndrome. Hum. Genet. 112 (2003) 563-566
33. Lazarou M., McKenzie M., Ohtake A., Thorburn D.R., and Ryan M.T. analysis of the assembly profiles for mitochondrial and nuclear-DNA-encoded subunits into complex I. Mol. Cell Biol. 27 (2007) 4228-4237
34. Papa S. Does cAMP play a part in the regulation of the mitochondrial electron transport chain in mammalian cells?. IUBMB Life 58 (2006) 173-175
35. Chen R., Fearnley I.M., Peak-Chew S.Y., and Walker J.E. The phosphorylation of subunits of complex I from bovine heart mitochondria. J. Biol. Chem. 279 (2004) 26036-26045
36. De Rasmo D., Panelli D., Sardanelli A.M., and Papa S. cAMP-dependent protein kinase regulates the mitochondrial import of the nuclear encoded NDUFS4 subunit of complex I. Cell. Signal. 20 (2008) 989-997
37. Technikova-Dobrova Z., Sardanelli A.M., Stanca M.R., and Papa S. cAMP-dependent protein phosphorylation in mitochondria of bovine heart. FEBS Lett. 22 (1994) 187-191
38. Sardanelli A.M., Technikova-Dobrova Z., Scacco S.C., Speranza F., and Papa S. Characterization of proteins phosphorylated by the cAMP-dependent protein kinase of bovine heart mitochondria. FEBS Lett. 377 (1995) 470-474
39. Papa S., Sardanelli A.M., Cocco T., Speranza F., Scacco S., and Technikova-Dobrova Z. The nuclear-encoded 18 kDa (IP) AQDQ subunit of bovine heart complex I is phosphorylated by the mitochondrial cAMP-dependent protein kinase. FEBS Lett. 379 (1996) 299-301
40. Carroll J., Shannon R.J., Fearnley I.M., Walker J.E., and Hirst J. Definition of the nuclear encoded protein composition of bovine heart mitochondrial complex I. Identification of two new subunits. J. Biol. Chem. 277 (2002) 50311-50317
41. Palmisano G., Sardanelli A.M., Signorile A., and Papa S. The phosphorylation of bovine heart complex I subunits. Proteomics 7 (2007) 1575-1583
42. Schilling B., Aggeler R., Schulenberg B., Murray J., Row R.H., Capaldi R.A., and Gibson B.W. Mass spectrometric identification of a novel phosphorylation site in subunit NDUFA10 of bovine mitochondrial complex I. FEBS Lett. 579 (2005) 2485-2490
43. Pocsfalvi G., Cuccurullo M., Schlosser G., Scacco S., Papa S., and Malorni A. Phosphorylation of B14.5a subunit from bovine heart complex I identified by titanium dioxide selective enrichment and shotgun proteomics. Mol. Cell Proteomics 6 (2007) 231-237
44. Hirst J., Carroll J., Fearnley I.M., Shannon R.J., and Walker J.E. The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim. Biophys. Acta 1604 (2003) 135-150
45. Huang G., Lu H., Hao A., Ng D.C., Ponniah S., Guo K., Lufei C., Zeng Q., and Cao X. GRIM-19, a cell death regulatory protein, is essential for assembly and function of mitochondrial complex I. Mol. Cell Biol. 24 (2004) 8447-8456
46. Angell J.E., Lindner D.J., Shapiro P.S., Hofmann E.R., and Kalvakolanu D.V. Identification of GRIM-19, a novel cell death-regulatory gene induced by the interferon-beta and retinoic acid combination, using a genetic approach. J Biol Chem. 275 (2000) 33416-33426
47. Schulenberg B., Goodman T.N., Aggeler R., Capaldi R.A., and Patton W.F. Characterization of dynamic and steady-state protein phosphorylation using a fluorescent phosphoprotein gel stain and mass spectrometry. Electrophoresis 25 (2004) 2526-2532
48. Murray J., Marusich M.F., Capaldi R.A., and Aggeler R. Focused proteomics: monoclonal antibody-based isolation of the oxidative phosphorylation machinery and detection of phosphoproteins using a fluorescent phosphoprotein gel stain. Electrophoresis 25 (2004) 2520-2525
49. Anandatheerthavarada H., Biswas G., Mullick J., Sepuris N., Pain D., and Avadhani G. Dual targeting of cytochrome P4502B1 to endoplasmic reticulum and mitochondria involves a novel signal activation by cyclic AMP-dependent phosphorylation at ser128. Embo. J. 18 (1999) 5494-5504
50. Robin M., Anandatheerthavarada H., Biswas G., Sepuris N., Gordon D., Pain D., and Avadhani G. Bimodal targeting of microsomal CYP2E1 to mitochondria through activation of an N-terminal chimeric signal by cAMP-mediated phosphorylation. J. Biol. Chem. 277 (2002) 40583-40593
51. Robin M., Prabu S., Raza H., Anandatheerthavarada H., and Avadhani G. Phosphorylation enhances mitochondrial targeting of GSTA4-4 through increased affinity for binding to cytoplasmic Hsp70. J. Biol. Chem 278 (2003) 18960-18970
52. Wiedemann N., Frazier A.E., and Pfanner N. The protein import machinery of mitochondria. J. Biol. Chem. 279 (2004) 14473-14476
53. Bohnert M., Pfanner N., and van der Laan M. A dynamic machinery for import of mitochondrial precursor proteins. FEBS Lett. 581 (2007) 2802-2810
54. Krayl M., Lim J.H., Martin F., Guiard B., and Voos W. A cooperative action of the ATP-dependent import motor complex and the inner membrane potential drives mitochondrial preprotein import. Mol. Cell. Biol. 27 (2007) 411-425
55. Ungermann C., Neupert W., and Cyr D.M. The role of Hsp70 in conferring unidirectionality on protein translocation into mitochondria. Science 266 (1994) 1250-1253
56. Taylor E.R., Hurrel F., Shannon R.J., Lin T.K., Hirst J., and Murphy M.P. Reversible glutathionylation of complex I increases mitochondrial superoxide formation. J. Biol. Chem. 278 (2003) 19603-19610
57. Beer S.M., R Taylor E., Brown S.E., Dahm C.C., Costa N.J., Runswick M.J., and Murphy M.P. Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol proteins: implications for mitochondrial redox regulation and antioxidant defense. J. Biol. Chem. 279 (2004) 47939-47951
58. Iuso A., Scacco S., Piccoli C., Bellomo F., Petruzzella V., Trentadue R., Minuto M., Ripoli M., Capitanio N., Zeviani M., and Papa S. Dysfunctions of cellular oxidative metabolism in patients with mutations in the NDUFS1 and NDUFS4 genes of complex I. J. Biol. Chem. 281 (2006) 10374-10380
59. Papa S., Sardanelli A.M., Cocco T., Speranza F., Scacco S., and Technikova-Dobrova Z. The nuclear-encoded 18 kDa (IP) AQDQ subunit of bovine heart complex I is phosphorylated by the mitochondrial cAMP-dependent protein kinase. FEBS Lett. 379 (1996) 299-301
60. Yadava N., Potluri P., and Scheffler I.E. Investigations of the potential effects of phosphorylation of the MWFE and ESSS subunits on complex I activity and assembly. Int. J. Biochem. Cell Biol. 40 (2008) 447-460
61. Livigni A., Scorziello A., Agnese S., Adornetto A., Carlucci A., Garbi C., Castaldo I., Annunziato L., Avvedimento E.V., and Feliciello A. Mitochondrial AKAP121 links cAMP and src signaling to oxidative metabolism. Mol. Biol. Cell. 17 (2006) 263-271
62. Plun-Favreau H., Klupsch K., Moisoi N., Gandhi S., Kjaer S., Frith D., Harvey K., Deas E., Harvey R.J., McDonald N., Wood N.W., Martins L.M., and Downward J. The mitochondrial protease HtrA2 is regulated by Parkinson's disease-associated kinase PINK1. Nat. Cell Biol. 9 (2007) 1243-1252
63. Ma X., Kalakonda S., Srinivasula S.M., Reddy S.P., Platanias L.C., and Kalvakolanu D.V. GRIM-19 associates with the serine protease HtrA2 for promoting cell death. Oncogene. 26 (2007) 4842-4849
64. Lin M.T., and Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443 (2006) 787-795