Primary fibroblasts of NDUFS4-/- mice display increased ROS levels and aberrant mitochondrial morphology

Mitochondrion

Volumn 13, Issue 5, 2013, Pages 436-443

  Valsecchi, Federica ^a,b   Grefte, Sander ^a   Roestenberg, Peggy ^a,b   Joosten Wagenaars, Jori ^a   Smeitink, Jan A M ^b   Willems, Peter H G M ^a   Koopman, Werner J H ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Bradykinin; Fura 2; Metabolic disorders; Rhodamine 123; Skeletal muscle

Indexed keywords

HYDROETHIDINE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; MITOCHONDRION; MOUSE; MUSCLE CELL; NDUFS4 GENE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; SKIN FIBROBLAST;

MUS;

4′,6-DIAMIDINO-2-PHENYLINDOLE; AR; BRADYKININ; CI; DAPI; ELECTRON TRANSPORT CHAIN; ETC; F; FURA-2; HEATSHOCK PROTEIN 47; HET; HSP47; HYDROETHIDIUM; KNOCKOUT; KO; MEF; METABOLIC DISORDERS; MIM; MITOCHONDRIAL ASPECT RATIO; MITOCHONDRIAL COMPLEX I OR NADH: UBIQUINONE OXIDOREDUCTASE; MITOCHONDRIAL FORMFACTOR; MITOCHONDRIAL INNER MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL OUTER MEMBRANE; MOM; MOUSE EMBRYONIC FIBROBLAST; MYOBLAST DETERMINATION PROTEIN 1; MYOD; NC; NUMBER OF MITOCHONDRIA PER CELL; OMIM; ONLINE MENDELIAN INHERITANCE IN MAN; OXIDATIVE PHOSPHORYLATION; OXPHOS; PHOSPHATIDYL SERINE; PI; PMF; PROPIDIUM IODIDE; PROTON-MOTIVE FORCE; PS; R123; REACTIVE OXYGEN SPECIES; RHODAMINE 123; ROS; SKELETAL MUSCLE; TCF4; TRANSCRIPTION FACTOR 4; WILDTYPE; WT; ΔΨ;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; ELECTRON TRANSPORT COMPLEX I; FIBROBLASTS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; REACTIVE OXYGEN SPECIES;

EID: 84882854431     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2012.12.001     Document Type: Article

References (57)

1. Auré K., Mamchaoui K., Frachon P., Butler-Browne G.S., Lombès A., Mouly V. Impact on oxidative phosphorylation of immortalization with the telomerase gene. Neuromuscul. Disord. 2007, 17:368-375.
2. Benard G., Rossignol R. Ultrastructure of the mitochondrion and its bearing on function and bioenergetics. Antioxid. Redox Signal. 2008, 10:1313-1342.
3. Bénit P., Steffann J., Lebon S., Chretien D., Kadhom N., de Lonlay P., Goldenberg A., Dumez Y., Dommergues M., Rustin P., Munnich A., Rötig 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. 2003, 112:563-566.
4. Bonifacino J.S. Current Protocols in Cell Biology 1998, John Wiley, New York.
5. Budde S.M., van den Heuvel L.P., Janssen A.J., Smeets R.J., Buskens C.A., DeMeirleir L., Van Coster R., Baethmann M., Voit T., Trijbels J.M., Smeitink J.A.M. Combined enzymatic complex I and III deficiency associated with mutations in the nuclear encoded NDUFS4 gene. Biochem. Biophys. Res. Commun. 2000, 275:63-68.
6. Budde S.M., van den Heuvel L.P., Smeitink J.A. The human complex I NDUFS4 subunit: from gene structure to function and pathology. Mitochondrion 2002, 2:109-115.
7. Budde S.M., van den Heuvel L.P., Smeets R.J., Skladal D., Mayr J.A., Boelen C., Petruzzella V., Papa S., Smeitink J.A. Clinical heterogeneity in patients with mutations in the NDUFS4 gene of mitochondrial complex I. J. Inherit. Metab. Dis. 2003, 26:813-815.
8. Calvaruso M.A., Willems P.H.G.M., van den Brand M., Valsecchi F., Kruse S., Palmiter R., Smeitink J.A.M., Nijtmans L.G. Mitochondrial complex III stabilizes complex I in the absence of NDUFS4 to provide partial activity. Hum. Mol. Genet. 2012, 21:115-120.
9. Choi W.S., Kruse S.E., Palmiter R.D., Xia Z. Mitochondrial complex I inhibition is not required for dopaminergic neuron death induced by rotenone, MPP+, or paraquat. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15136-15141.
10. Choi W.S., Palmiter R.D., Xia Z. Loss of mitochondrial complex I activity potentiates dopamine neuron death induced by microtubule dysfunction in a Parkinson's disease model. J. Cell Biol. 2011, 192:873-882.
11. Dairkee S.H., Nicolau M., Sayeed A., Champion S., Yi Y., Moore D.H., Yong B., Meng Z., Jeffrey S.S. Oxidative stress pathways highlighted in tumor cell immortalization: association with breast cancer outcome. Oncogene 2007, 26:6269-6279.
12. Dieteren C.E., Willems P.H., Vogel R.O., Swarts H.G., Fransen J., Roepman R., Crienen G., Smeitink J.A., Nijtmans L.G., Koopman W.J.H. Subunits of mitochondrial complex I exist as part of matrix- and membrane-associated subcomplexes in living cells. J. Biol. Chem. 2008, 283:34753-34761.
13. Dieteren C.E., Willems P.H., Swarts H.G., Fransen J., Smeitink J.A., Koopman W.J.H., Nijtmans L.G. Defective mitochondrial translation differently affects the live cell dynamics of complex I subunits. Biochim. Biophys. Acta 2011, 1807:1624-1633.
14. Distelmaier F., Koopman W.J.H., van den Heuvel L.P., Rodenburg R.J., Mayatepek E., Willems P.H., Smeitink J.A. Mitochondrial complex I deficiency: from organelle dysfunction to clinical disease. Brain 2009, 132:833-842.
15. Distelmaier F., Valsecchi F., Forkink M., van Emst-de Vries S., Swarts H.G., Rodenburg R.J., Verwiel E.T., Smeitink J.A.M., Willems P.H.G.M., Koopman W.J.H. Trolox-sensitive reactive oxygen species regulate mitochondrial morphology, oxidative phosphorylation and cytosolic calcium handling in healthy cells. Antioxid. Redox Signal. 2012, 17:1657-1669.
16. Efremov R.G., Sazanov L.A. The coupling mechanism of respiratory complex I - A structural and evolutionary perspective. Biochim. Biophys. Acta. 2012, 1817:1785-1795.
17. Forkink M., Smeitink J.A., Brock R., Willems P.H., Koopman W.J. Detection and manipulation of mitochondrial reactive oxygen species in mammalian cells. Biochim. Biophys. Acta 2010, 1797:1034-1044.
18. Fukui H., Moraes C.T. The mitochondrial impairment, oxidative stress and neurodegeneration connection: reality or just an attractive hypothesis?. Trends Neurosci. 2008, 31:251-256.
19. Grefte S., Kuijpers-Jagtman A.M., Torensma R., Von den Hoff J.W. Skeletal muscle fibrosis: the effect of stromal-derived factor-1α-loaded collagen scaffolds. Regen. Med. 2010, 5:737-747.
20. Iuso A., Scacco S., Piccoli C., Bellomo F., Petruzzella V., Trentadue R., Minuto M., Ripoli M., Capitanio N., Zeviani M., Papa S. Dysfunctions of cellular oxidative metabolism in patients with mutations in the NDUFS1 and NDUFS4 genes of complex I. J. Biol. Chem. 2006, 281:10374-10380.
21. Koene S., Willems P.H., Roestenberg P., Koopman W.J., Smeitink J.A. Mouse models for nuclear DNA-encoded mitochondrial complex I deficiency. J. Inherit. Metab. Dis. 2010, 34:293-307.
22. Kondoh H., Lleonart M.E., Bernard D., Gil J. Protection from oxidative stress by enhanced glycolysis: a possible mechanism of cellular immortalization. Histol. Histopathol. 2007, 22:85-90.
23. -.-mediated mitochondrial outgrowth. Am. J. Physiol. Cell Physiol. 2005, 288:C1440-C1450.
24. Koopman W.J.H., Visch H.J., Verkaart S., van den Heuvel L.W., Smeitink J.A., Willems P.H. Mitochondrial network complexity and pathological decrease in complex I activity are tightly correlated in isolated human complex I deficiency. Am. J. Physiol. Cell Physiol. 2005, 289:C881-C890.
25. Koopman W.J.H., Visch H.J., Smeitink J.A., Willems P.H. Simultaneous quantitative measurement and automated analysis of mitochondrial morphology, mass, potential, and motility in living human skin fibroblasts. Cytometry A 2006, 69:1-12.
26. Koopman W.J.H., Verkaart S., Visch H.J., van Emst-de Vries S., Nijtmans L.G., Smeitink J.A., Willems P.H. Human NADH:ubiquinone oxidoreductase deficiency: radical changes in mitochondrial morphology?. Am. J. Physiol. Cell Physiol. 2007, 293:C22-C29.
27. Koopman W.J.H., Nijtmans L.G., Dieteren C.E., Roestenberg P., Valsecchi F., Smeitink J.A., Willems P.H. Mammalian mitochondrial complex I: biogenesis, regulation, and reactive oxygen species generation. Antioxid. Redox Signal. 2010, 12:1431-1470.
28. Koopman W.J.H., Willems P.H.G.M., Smeitink J.A.M. Monogenic mitochondrial disorders. N. Engl. J. Med. 2012, 366:1132-1141.
29. Koopman W.J.H., Distelmaier F., Smeitink J.A.M., Willems P.H.G.M. OXPHOS mutations and neurodegeneration. EMBO J. 2012, 32:9-29.
30. Kruse S.E., Watt W.C., Marcinek D.J., Kapur R.P., Schenkman K.A., Palmiter R.D. Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy. Cell Metab. 2008, 7:312-320.
31. Lawson-Smith M.J., McGeachie J.K. The identification of myogenic cells in skeletal muscle, with emphasis on the use of tritiated thymidine autoradiography and desmin antibodies. J. Anat. 1998, 192:161-171.
32. Lazarou M., McKenzie M., Ohtake A., Thorburn D.R., Ryan M.T. Analysis of the assembly profiles for mitochondrial- and nuclear-DNA-encoded subunits into complex I. Mol. Cell. Biol. 2007, 27:4228-4237.
33. Mathew S.J., Hansen J.M., Merrell A.J., Murphy M.M., Lawson L.A., Hutcheson D.A., Hansen M.S., Angus-Hill M., Kardon G. Connective tissue fibroblasts and Tcf4 regulate myogenesis. Development 2011, 138:371-384.
34. Mimaki M., Wang X., McKenzie M., Thorburn D.R., Ryan M.T. Understanding mitochondrial complex I assembly in health and disease. Biochim. Biophys. Acta 2012, 1817:851-862.
35. Moreno-Lastres D., Fontanesi F., García-Consuegra I., Martín M.A., Arenas J., Barrientos A., Ugalde C. Mitochondrial complex I plays an essential role in human respirasome assembly. Cell Metab. 2012, 15:324-335.
36. Murphy M.P., Holmgren A., Larsson N.G., Halliwell B., Chang C.J., Kalyanaraman B., Rhee S.G., Thornalley P.J., Partridge L., Gems D., Nyström T., Belousov V., Schumacker P.T., Winterbourn C.C. Unraveling the biological roles of reactive oxygen species. Cell Metab. 2011, 13:361-366.
37. Nouws J., Nijtmans L.G., Smeitink J.A.M., Vogel R.O. Assembly factors as a new class of disease genes for mitochondrial complex I deficiency: cause, pathology and treatment options. Brain 2012, 135:12-22.
38. Pagniez-Mammeri H., Loublier S., Legrand A., Bénit P., Rustin P., Slama A. Mitochondrial complex I deficiency of nuclear origin I. Structural genes. Mol. Genet. Metab. 2012, 105:163-172.
39. Pagniez-Mammeri H., Rak M., Legrand A., Bénit P., Rustin P., Slama A. Mitochondrial complex I deficiency of nuclear origin II. Non-structural genes. Mol. Genet. Metab. 2012, 105:173-179.
40. Palomero J., Pye D., Kabayo T., Spiller D.G., Jackson M.J. In situ detection and measurement of intracellular reactive oxygen species in single isolated mature skeletal muscle fibers by real time fluorescence microscopy. Antioxid. Redox Signal. 2008, 10:1463-1474.
41. Papa S., Rasmo D.D., Technikova-Dobrova Z., Panelli D., Signorile A., Scacco S., Petruzzella V., Papa F., Palmisano G., Gnoni A., Micelli L., Sardanelli A.M. Respiratory chain complex I, a main regulatory target of the cAMP/PKA pathway is defective in different human diseases. FEBS Lett. 2012, 586:568-577.
42. Petruzzella V., Vergari R., Puzziferri I., Boffoli D., Lamantea E., Zeviani M., 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. 2001, 10:529-535.
43. Quintana A., Kruse S.E., Kapur R.P., Sanz E., Palmiter R.D. Complex I deficiency due to loss of Ndufs4 in the brain results in progressive encephalopathy resembling Leigh syndrome. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:10996-11001.
44. Roestenberg P., Manjeri G.R., Valsecchi F., Smeitink J.A., Willems P.H., Koopman W.J.H. Pharmacological targeting of mitochondrial complex I deficiency: the cellular level and beyond. Mitochondrion 2012, 12:57-65.
45. Rossignol R., Gilkerson R., Aggeler R., Yamagata K., Remington S.J., Capaldi R.A. Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res. 2004, 64:985-993.
46. Scharstuhl A., Mutsaers H.A., Pennings S.W., Szarek W.A., Russel F.G., Wagener F.A. Curcumin-induced fibroblast apoptosis and in vitro wound contraction are regulated by antioxidants and heme oxygenase: implications for scar formation. J. Cell. Mol. Med. 2009, 13:712-725.
47. Smeitink J.A.M., Sengers R., Trijbels F., van den Heuvel L. Human NADH:ubiquinone oxidoreductase. J. Bioenerg. Biomembr. 2001, 33:259-266.
48. Smeitink J.A.M., van den Heuvel L., DiMauro S. The genetics and pathology of oxidative phosphorylation. Nat. Rev. Genet. 2001, 2:342-352.
49. Taddei M.L., Giannoni E., Raugei G., Scacco S., Sardanelli A.M., Papa S., Chiarugi P. Mitochondrial Oxidative Stress due to Complex I Dysfunction Promotes Fibroblast Activation and Melanoma Cell Invasiveness. J. Signal Transduct. 2012, 2012:684592.
50. Tao W.A., Wollscheid B., O'Brien R., Eng J.K., Li X.J., Bodenmiller B., Watts J.D., Hood L., Aebersold R. Quantitative phosphoproteome analysis using a dendrimer conjugation chemistry and tandem mass spectrometry. Nat. Methods 2005, 2:591-598.
51. Ugalde C., Janssen R.J., van den Heuvel L.P., Smeitink J.A., Nijtmans L.G. Differences in assembly or stability of complex I and other mitochondrial OXPHOS complexes in inherited complex I deficiency. Hum. Mol. Genet. 2004, 13:659-667.
52. Valsecchi F., Koopman W.J., Manjeri G.R., Rodenburg R.J., Smeitink J.A., Willems P.H. Complex I disorders: causes, mechanisms, and development of treatment strategies at the cellular level. Dev. Disabil. Res. Rev. 2010, 16:175-182.
53. Valsecchi F., Monge C., Forkink M., de Groof A.J., Benard G., Rossignol R., Swarts H.G., van Emst-de Vries S.E., Rodenburg R.J., Calvaruso M.A., Nijtmans L.G., Heeman B., Roestenberg P., Wieringa B., Smeitink J.A., Koopman W.J.H., Willems P.H.G.M. Metabolic consequences of NDUFS4 gene deletion in immortalized mouse embryonic fibroblasts. Biochim. Biophys. Acta 2012, 1817:1925-1936.
54. Verkaart S., Koopman W.J.H., van Emst-de Vries S.E., Nijtmans L.G., van den Heuvel L.W., Smeitink J.A., Willems P.H. Superoxide production is inversely related to complex I activity in inherited complex I deficiency. Biochim. Biophys. Acta 2007, 1772:373-381.
55. Verkaart S., Koopman W.J.H., Cheek J., van Emst-de Vries S.E., van den Heuvel L.W.P., Smeitink J.A.M., Willems P.H.G.M. Mitochondrial and cytosolic redox state are not detectably altered in isolated human NADH:ubiquinone oxidoreductase deficiency. Biochim. Biophys. Acta 2007, 1772:1041-1051.
56. Vogel R.O., Dieteren C.E., van den Heuvel L.P., Willems P.H., Smeitink J.A., Koopman W.J.H., Nijtmans L.G. J. Biol. Chem. 2007, 282:7582-7590.
57. Westermann B. Bioenergetic role of mitochondrial fusion and fission. Biochim. Biophys. Acta 2012, 1817:1833-1838.