Mitochondrial dysfunction in primary human fibroblasts triggers an adaptive cell survival program that requires AMPK-α

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 3, 2015, Pages 529-540

  Distelmaier, Felix ^a,b,c   Valsecchi, Federica ^a,b,i   Liemburg Apers, Dania C ^a   Lebiedzinska, Magdalena ^d   Rodenburg, Richard J ^b   Heil, Sandra ^e,j   Keijer, Jaap ^e   Fransen, Jack ^a   Imamura, Hiromi ^f   Danhauser, Katharina ^c   Seibt, Annette ^c   Viollet, Benoit ^g   Gellerich, Frank N ^h   Smeitink, Jan A M ^b   Wieckowski, Mariusz R ^d   Willems, Peter H G M ^a   Koopman, Werner J H ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^d NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^e WAGENINGEN UNIVERSITY   (Netherlands)

^f KYOTO UNIVERSITY   (Japan)

^g INSTITUT COCHIN   (France)

^h OTTO VON GUERICKE UNIVERSITY   (Germany)

ⁱ Department of Stereotactic Neurosurgery Otto von Guericke Universität ^*  (United States)

^j ERASMUS MEDICAL CENTER   (Netherlands)

more..

Author keywords

Calcium homeostasis; Glycolysis; Metabolic regulation; Mitochondrial dynamics; Redox signaling; Respirometry

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATE; CALCIUM; CATALASE; GLUCOSE; GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 1; GLUTATHIONE PEROXIDASE 2; GLUTATHIONE PEROXIDASE 5; GLUTATHIONE REDUCTASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA; LACTIC ACID; MAMMALIAN TARGET OF RAPAMYCIN; MANGANESE SUPEROXIDE DISMUTASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PYRUVIC ACID; SIRTUIN 1; SUPEROXIDE; UNCLASSIFIED DRUG; CHLORIDE; MTOR PROTEIN, HUMAN; MTOR PROTEIN, MOUSE; MULTIENZYME COMPLEX; PEROXISOME-PROLIFERATOR-ACTIVATED RECEPTOR-GAMMA COACTIVATOR-1; SIRT1 PROTEIN, HUMAN; SIRT1 PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR;

ADAPTATION; ARTICLE; BIOGENESIS; CALCIUM CELL LEVEL; CELL DEATH; CELL METABOLISM; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSOL; DEPOLARIZATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXTRACELLULAR SPACE; FIBROBLAST; HOMEOSTASIS; HUMAN; HUMAN CELL; LIPID PEROXIDATION; MITOCHONDRIAL MEMBRANE POTENTIAL; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PHENOTYPE; SENESCENCE; ANIMAL; CYTOLOGY; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRION; MOUSE; SIGNAL TRANSDUCTION; TRANSFORMED CELL LINE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CALCIUM; CELL LINE, TRANSFORMED; CELL SURVIVAL; CHLORIDES; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ENDOPLASMIC RETICULUM; FIBROBLASTS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, KNOCKOUT; MITOCHONDRIA; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; SIRTUIN 1; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS;

EID: 84920607070     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.12.012     Document Type: Article

References (71)

1. Rizzuto R., De Stefani D., Raffaello A., Mammucari C. Mitochondria as sensors and regulators of calcium signalling. Nat. Rev. Mol. Cell Biol. 2012, 13:566-578.
2. Koopman W.J.H., Willems P.H.G.M., Smeitink J.A.M. Monogenic mitochondrial disorders. N. Engl. J. Med. 2012, 366:1132-1141.
3. Koopman W.J.H., Distelmaier F., Smeitink J.A.M., Willems P.H.G.M. OXPHOS mutations and neurodegeneration. EMBO J. 2013, 32:9-29.
4. Mitchel P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 1961, 191:144-148.
5. Kilbride S.M., Prehn J.H. Central roles of apoptotic proteins in mitochondrial function. Oncogene 2013, 32:2703-2711.
6. Benard G., Trian T., Bellance N., Berger P., Lavie J., Espil-Taris C., et al. Adaptative capacity of mitochondrial biogenesis and of mitochondrial dynamics in response to pathogenic respiratory chain dysfunction. Antioxid. Redox Signal. 2013, 19:350-365.
7. Germain M., Nguyen A.P., Khacho M., Patten D.A., Screaton R.A., Park D.S., et al. LKB1-regulated adaptive mechanisms are essential for neuronal survival following mitochondrial dysfunction. Hum. Mol. Genet. 2013, 22:952-962.
8. Hao W., Chang C.P., Tsao C.C., Xu J. Oligomycin-induced bioenergetic adaptation in cancer cells with heterogeneous bioenergetic organization. J. Biol. Chem. 2010, 285:12647-12654.
9. Koopman W.J.H., Nijtmans L.G., Dieteren C.E., Roestenberg P., Valsecchi F., Smeitink J.A.M., et al. Mammalian mitochondrial complex I: Biogenesis, Regulation and Reactive Oxygen Species generation. Antioxid. Redox Signal. 2010, 12:1431-1470.
10. Rambold A.S., Kostelecky B., Elia N., Lippincott-Schwartz J. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:10190-10195.
11. Hardie D.G., Ross F.A., Hawley S.A. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 2012, 13:251-262.
12. Brose R.D., Shin G., McGuinness M.C., Schneidereith T., Purvis S., Dong G.X., et al. Activation of the stress proteome as a mechanism for small molecule therapeutics. Hum. Mol. Genet. 2012, 21:4237-4252.
13. Stranahan A.M., Mattson M.P. Recruiting adaptive cellular stress responses for successful brain ageing. Nat. Rev. Neurosci. 2012, 13:209-216.
14. Distelmaier F., Koopman W.J.H., van den Heuvel L.W., Rodenburg R.J., Mayatepek E., Willems P.H.G.M., et al. Mitochondrial complex I deficiency: from organelle dysfunction to clinical disease. Brain 2009, 132:833-842.
15. Valsecchi F., Koopman W.J.H., Manjeri G.R., Rodenburg R.J., Smeitink J.A.M., 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.
16. Golubitzky A., Dan P., Weissman S., Link G., Wikstrom J.D., Saada A. Screening for active small molecules in mitochondrial complex I deficient patient's fibroblasts, reveals AICAR as the most beneficial compound. PLoS ONE 2011, 6:e26883.
17. Kruse S.E., Watt W.C., Marcinek D.J., Kapur R.P., Schenkman K.A., et al. Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy. Cell Metab. 2008, 7:312-320.
18. Roestenberg P., Manjeri G.R., Valsecchi F., Smeitink J.A.M., Willems P.H.G.M., Koopman W.J.H. Mini-review: Pharmacological targeting of complex I deficiency: the cellular level and beyond. Mitochondrion 2012, 12:57-65.
19. Valsecchi F., Monge C., Forkink M., de Groof A.J., Benard G., Rossignol R., et al. Metabolic consequences of NDUFS4 gene deletion in immortalized mouse embryonic fibroblasts. Biochim. Biophys. Acta 2012, 1817:1925-1936.
20. Blanchet L., Buydens M.C., Smeitink J.A., Willems P.H., Koopman W.J.H. Isolated mitochondrial complex I deficiency: explorative data analysis of patient cell parameters. Curr. Pharm. Des. 2011, 17:4023-4033.
21. Forkink M., Manjeri G.R., Liemburg-Apers D.C., Nibbeling E., Blanchard M., et al. Mitochondrial hyperpolarization during chronic complex I inhibition is sustained by low activity of complex II, III, IV and V. Biochim. Biophys. Acta 2014, 1837:1247-1256.
22. 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.
23. Koopman W.J.H., Verkaart S., Visch H.J., van der Westhuizen F.H., Murphy M.P., van den Heuvel L.W., et al. Inhibition of complex I of the electron transport chain causes O2-.-mediated mitochondrial outgrowth. Am. J. Physiol. Cell Physiol. 2005, 288:C1440-C1450.
24. Stöckl P., Hütter E., Zwerschke W., Jansen-Dürr P. Sustained inhibition of oxidative phosphorylation impairs cell proliferation and induces premature senescence in human fibroblasts. Exp. Gerontol. 2006, 41:674-682.
25. Laderoute K.R., Amin K., Calaoagan J.M., Knapp M., Le T., Orduna J., et al. 5'-AMP-Activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid tumor microenvironments. Mol. Cell. Biol. 2006, 26:5336-5347.
26. Distelmaier F., Valsecchi F., Forkink M., van Emst-de Vries S., Swarts H.G., Rodenburg R.J., et al. Trolox-sensitive reactive oxygen species regulate mitochondrial morphology, oxidative phosphorylation and cytosolic calcium handling in healthy cells. Antioxid. Redox Signal. 2012, 17:1657-1669.
27. Visch H.J., Rutter G.A., Koopman W.J., Koenderink J.B., Verkaart S., de Groot T., et al. Inhibition of mitochondrial Na+-Ca2+ exchange restores agonist-induced ATP production and Ca2+ handling in human complex I deficiency. J. Biol. Chem. 2004, 279:40328-40336.
28. Koopman W.J.H., Distelmaier F., Esseling J.J., Smeitink J.A., Willems P.H. Computer-assisted live cell analysis of mitochondrial membrane potential, morphology and calcium handling. Methods 2008, 46:304-311.
29. Verkaart S., Koopman W.J.H., Cheek J., van Emst-de Vries S.E., van den Heuvel L.W., Smeitink J.A., et al. Mitochondrial and cytosolic thiol redox state are not detectably altered in isolated human NADH:ubiquinone oxidoreductase deficiency. Biochim. Biophys. Acta 2007, 1772:1041-1051.
30. Koopman W.J.H., Distelmaier F., Hink M.A., Verkaart S., Wijers M., Fransen J., et al. Inherited complex I deficiency is associated with faster protein diffusion in the matrix of moving mitochondria. Am. J. Physiol. Cell Physiol. 2008, 294:C1124-C1132.
31. Verkaart S., Koopman W.J.H., van Emst-de Vries S.E., Nijtmans L.G., van den Heuvel L.W., Smeitink J.A., et al. Superoxide production is inversely related to complex I activity in inherited complex I deficiency. Biochim. Biophys. Acta 2007, 1772:373-381.
32. Chinopoulos C. Mitochondrial consumption of ATP: Not so fast. FEBS Lett. 2011, 585:1255-1259.
33. Wijburg F.A., Feller N., Ruitenbeek W., Trijbels J.M., Sengers R.C., Scholte H.R., et al. Detection of respiratory chain dysfunction by measuring lactate and pyruvate production in cultured fibroblasts. J. Inherit. Metab. Dis. 1990, 13:355-358.
34. Mailloux R.J., McBride S.L., Harper M.E. Unearthing the secrets of mitochondrial ROS and glutathione in bioenergetics. Trends Biochem. Sci. 2013, 38:592-602.
35. Koopman W.J.H., Verkaart S., Visch H.J., van Emst-de Vries S., Nijtmans L.G., et al. Human NADH:ubiquinone oxidoreductase deficiency: radical changes in mitochondrial morphology?. Am. J. Physiol. Cell Physiol. 2007, 293:C22-C29.
36. Willems P.H.G.M., Wanschers B.F., Esseling J., Szklarczyk R., Kudla U., et al. BOLA1 is an aerobic protein that prevents mitochondrial morphology changes induced by glutathione depletion. Antioxid. Redox Signal. 2013, 18:129-138.
37. Auré K., Fayet G., Leroy J.P., Lacène E., Romero N.B., Lombès A. Apoptosis in mitochondrial myopathies is linked to mitochondrial proliferation. Brain 2006, 129:1249-1259.
38. 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.
39. Koopman W.J.H., Hink M.A., Verkaart S., Visch H.J., Smeitink J.A.M., et al. Partial complex I inhibition decreases mitochondrial motility and increases matrix protein diffusion as revealed by fluorescence correlation spectroscopy. Biochim. Biophys. Acta 2007, 1767:940-947.
40. Tronstad K.J., Nooteboom M., Nilsson L.I., Nikolaisen J., Sokolewicz M., et al. Regulation and quantification of cellular mitochondrial morphology and content. Curr. Pharm. Des. 2014, 20:5634-5652.
41. Gertz M., Steegborn C. The Lifespan-regulator p66Shc in mitochondria: redox enzyme or redox sensor?. Antioxid. Redox Signal. 2010, 13:1417-1428.
42. Lebiedzinska M., Karkucinska-Wieckowska A., Wojtala A., Suski J.M., Szabadkai G., et al. Disrupted ATP synthase activity and mitochondrial hyperpolarisation-dependent oxidative stress is associated with p66Shc phosphorylation in fibroblasts of NARP patients. Int. J. Biochem. Cell Biol. 2013, 45:141-150.
43. Hardie D.G., Ross F.A., Hawley S.A. AMP-activated protein kinase: A target for drugs both ancient and modern. Chem. Biol. 2012, 19:1222-1236.
44. Visch H.J., Koopman W.J.H., Zeegers D., van Emst-de Vries S.E., van Kuppeveld F.J., et al. Ca2+-mobilizing agonists increase mitochondrial ATP production to accelerate cytosolic Ca2+ removal: aberrations in human complex I deficiency. Am. J. Physiol. Cell Physiol. 2006, 291:C308-C316.
45. Willems P.H.G.M., Valsecchi F., Distelmaier F., Verkaart S., Visch H.J., Smeitink J.A., et al. Mitochondrial Ca2+ homeostasis in human NADH:ubiquinone oxidoreductase deficiency. Cell Calcium 2008, 44:123-133.
46. Valsecchi F., Grefte S., Roestenberg P., Joosten-Wagenaars J., Smeitink J.A., Willems P.H., et al. Primary fibroblasts of NDUFS4-/- mice display increased ROS levels and aberrant mitochondrial morphology. Mitochondrion 2013, 13:436-443.
47. Robinson B.H. Lactic acidemia and mitochondrial disease. Mol. Genet. Metab. 2006, 89:3-13.
48. McKay N.D., Robinson B., Brodie R., Rooke-Allen N. Glucose transport and metabolism in cultured human skin fibroblasts. Biochim. Biophys. Acta 1983, 762:198-204.
49. Ganapathy V., Thangaraju M., Prasad P.D. Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol. Ther. 2008, 121:29-40.
50. O'Donnell-Tormey J., Nathan C.F., Lanks K., DeBoer C.J., de la Harpe Secretion of pyruvate: An antioxidant defense of mammalian cells. J. Exp. Med. 1987, 165:500-514.
51. Donnelly M., Scheffler I.E. Energy metabolism in respiration-deficient and wild type Chinese hamster fibroblasts in culture. J. Cell. Physiol. 1976, 89:39-51.
52. Reitzer L.J., Wice B.M., Kennell D.J. Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells. Biol. Chem. 1979, 254:2669-2676.
53. Seo B.B., Kitajima-Ihara T., Chan E.K., Scheffler I.E., Matsuno-Yagi A., et al. Molecular remedy of complex I defects: rotenone-insensitive internal NADH-quinone oxidoreductase of Saccharomyces cerevisiae mitochondria restores the NADH oxidase activity of complex I-deficient mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:9167-9171.
54. Weinberg F., Chandel N.S. Mitochondrial metabolism and cancer. Ann. N. Y. Acad. Sci. 2009, 1177:66-73.
55. Gohil V.M., Sheth S.A., Nilsson R., Wojtovich A.P., Lee J.H., et al. Nutrient-sensitized screening for drugs that shift energy metabolism from mitochondrial respiration to glycolysis. Nat. Biotechnol. 2010, 28:249-255.
56. Kaelin W.G., Thompson C.B. Cancer: clues from cell metabolism. Nature 2010, 465:562-564.
57. Robinson K.M., Janes M.S., Pehar M., Monette J.S., Ross M.F., et al. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:15038-15043.
58. Robinson K.M., Janes M.S., Beckman J.S. The selective detection of mitochondrial superoxide by live cell imaging. Nat. Protoc. 2008, 3:941-947.
59. Sarsour E.H., Agarwal M., Pandita T.K., Oberley L.W., Goswami P.C. Manganese superoxide dismutase protects the proliferative capacity of confluent normal human fibroblasts. J. Biol. Chem. 2005, 280:18033-18041.
60. Tondera D., Grandemange S., Jourdain A., Karbowski M., Mattenberger Y., et al. SLP-2 is required for stress-induced mitochondrial hyperfusion. EMBO J. 2009, 28:1589-1600.
61. Molina A.J., Wikstrom J.D., Stiles L., Las G., Mohamed H., et al. Mitochondrial networking protects beta-cells from nutrient-induced apoptosis. Diabetes 2009, 58:2303-2315.
62. Rimbaud S., Garnier A., Ventura-Clapier R. Mitochondrial biogenesis in cardiac pathophysiology. Pharmacol. Rep. 2009, 61:131-138.
63. Coller H.A., Sang L., Roberts J.M. A new description of cellular quiescence. PLoS Biol. 2006, 4:e83.
64. Lemons J.M., Feng X.J., Bennett B.D., Legesse-Miller A., Johnson E.L., et al. Quiescent fibroblasts exhibit high metabolic activity. PLoS Biol. 2010, 8:e1000514.
65. Benard G., Bellance N., Jose C., Melser S., Nouette-Gaulain K., et al. Multi-site control and regulation of mitochondrial energy production. Biochim. Biophys. Acta 2010, 1797:698-709.
66. Ruderman N.B., Xu X.J., Nelson L., Cacicedo J.M., Saha A.K., et al. AMPK and SIRT1: a long-standing partnership?. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E751-E760.
67. Witczak C.A., Sharoff C.G., Goodyear L.J. AMP-activated protein kinase in skeletal muscle: from structure and localization to its role as a master regulator of cellular metabolism. Cell. Mol. Life Sci. 2008, 65:3737-3755.
68. Hawley S.A., Ross F.A., Chevtzoff C., Green K.A., Evans A., et al. Use of cells expressing gamma subunit variants to identify diverse mechanisms of AMPK activation. Cell Metab. 2010, 11:554-565.
69. Han Y., Wang Q., Song P., Zhu Y., Zou M.H. Redox regulation of the AMP-activated protein kinase. PLoS ONE 2010, 5:e15420.
70. Zmijewski J.W., Banerjee S., Bae H., Friggeri A., Lazarowski E.R., Abraham E. Exposure to hydrogen peroxide induces oxidation and activation of AMP-activated protein kinase. J. Biol. Chem. 2010, 285:33154-33164.
71. Trenker M., Malli R., Fertschai I., Levak-Frank S., Graier W.F. Uncoupling proteins 2 and 3 are fundamental for mitochondrial Ca2+ uniport. Nat. Cell Biol. 2007, 9:445-452.