The mitochondrial unfolded protein response-synchronizing genomes

Current Opinion in Cell Biology

Volumn 33, Issue , 2015, Pages 74-81

  Jovaisaite, Virginija ^a   Auwerx, Johan ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; PROTEOME;

AGING; CELL COMMUNICATION; CELL ENERGY; FEEDBACK SYSTEM; GENOME; HUMAN; INTRACELLULAR SIGNALING; LIFESPAN; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL TARGETING SIGNAL; MITOCHONDRION; MITOPHAGY; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OXIDATIVE STRESS; PROTEIN HOMEOSTASIS; PROTEIN INDUCTION; QUALITY CONTROL; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; CELL NUCLEUS; CELL PROTECTION; GENETICS; MAMMAL; METABOLISM; MITOCHONDRIAL GENOME;

AGING; ANIMALS; CELL NUCLEUS; CYTOPROTECTION; GENOME; GENOME, MITOCHONDRIAL; HUMANS; MAMMALS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROTEOME; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84919775416     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2014.12.003     Document Type: Review

References (60)

1. Dillin A., Gottschling D.E., Nystrom T. The good and the bad of being connected: the integrons of aging. Curr Opin Cell Biol 2014, 26:107-112.
2. Houtkooper R.H., Williams R.W., Auwerx J. Metabolic networks of longevity. Cell 2010, 142:9-14.
3. Andreux P.A., Houtkooper R.H., Auwerx J. Pharmacological approaches to restore mitochondrial function. Nat Rev Drug Discov 2013, 12:465-483.
4. Nunnari J., Suomalainen A. Mitochondria: in sickness and in health. Cell 2012, 148:1145-1159.
5. Jensen M.B., Jasper H. Mitochondrial proteostasis in the control of aging and longevity. Cell Metab 2014, 20:214-225.
6. Haynes C.M., Ron D. The mitochondrial UPR - protecting organelle protein homeostasis. J Cell Sci 2010, 123:3849-3855.
7. Jovaisaite V., Mouchiroud L., Auwerx J. The mitochondrial unfolded protein response, a conserved stress response pathway with implications in health and disease. J Exp Biol 2014, 217:137-143.
8. Gray M.W., Burger G., Lang B.F. The origin and early evolution of mitochondria. Genome Biol 2001, 2. reviews1018.
9. 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., et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
10. Neupert W., Herrmann J.M. Translocation of proteins into mitochondria. Annu Rev Biochem 2007, 76:723-749.
11. Lane N. Mitonuclear match: optimizing fitness and fertility over generations drives ageing within generations. Bioessays 2011, 33:860-869.
12. Baker B.M., Haynes C.M. Mitochondrial protein quality control during biogenesis and aging. Trends Biochem Sci 2011, 36:254-261.
13. Tatsuta T., Langer T. Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J 2008, 27:306-314.
14. Rainbolt T.K., Atanassova N., Genereux J.C., Wiseman R.L. Stress-regulated translational attenuation adapts mitochondrial protein import through Tim17A degradation. Cell Metab 2013, 18:908-919.
15. Nargund A.M., Pellegrino M.W., Fiorese C.J., Baker B.M., Haynes C.M. Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation. Science 2012, 337:587-590.
16. Schleit J., Johnson S.C., Bennett C.F., Simko M., Trongtham N., Castanza A., Hsieh E.J., Moller R.M., Wasko B.M., Delaney J.R., et al. Molecular mechanisms underlying genotype-dependent responses to dietary restriction. Aging Cell 2013, 12:1050-1061.
17. Yoneda T., Benedetti C., Urano F., Clark S.G., Harding H.P., Ron D. Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. J Cell Sci 2004, 117:4055-4066.
18. Wu Y., Williams Evan G., Dubuis S., Mottis A., Jovaisaite V., Houten Sander M., Argmann Carmen A., Faridi P., Wolski W., Kutalik Z., et al. Multilayered genetic and omics dissection of mitochondrial activity in a mouse reference population. Cell 2014, 158:1415-1430.
19. Burbulla L.F., Fitzgerald J.C., Stegen K., Westermeier J., Thost A.K., Kato H., Mokranjac D., Sauerwald J., Martins L.M., Woitalla D., et al. Mitochondrial proteolytic stress induced by loss of mortalin function is rescued by Parkin and PINK1. Cell Death Dis 2014, 5:e1180.
20. Zhao Q., Wang J., Levichkin I.V., Stasinopoulos S., Ryan M.T., Hoogenraad N.J. A mitochondrial specific stress response in mammalian cells. EMBO J 2002, 21:4411-4419.
21. Papa L., Germain D. SirT3 regulates the mitochondrial unfolded protein response. Mol Cell Biol 2014, 34:699-710.
22. Pimenta de Castro I., Costa A.C., Lam D., Tufi R., Fedele V., Moisoi N., Dinsdale D., Deas E., Loh S.H., Martins L.M. Genetic analysis of mitochondrial protein misfolding in Drosophila melanogaster. Cell Death Differ 2012, 19:1308-1316.
23. Runkel E.D., Liu S., Baumeister R., Schulze E. Surveillance-activated defenses block the ROS-induced mitochondrial unfolded protein response. PLoS Genet 2013, 9:e1003346.
24. Liu Y., Samuel B.S., Breen P.C., Ruvkun G. Caenorhabditis elegans pathways that surveil and defend mitochondria. Nature 2014, 508:406-410.
25. Pellegrino M.W., Nargund A.M., Kirienko N.V., Gillis R., Fiorese C.J., Haynes C.M. Mitochondrial UPR-regulated innate immunity provides resistance to pathogen infection. Nature 2014, (in press).
26. Houtkooper R.H., Mouchiroud L., Ryu D., Moullan N., Katsyuba E., Knott G., Williams R.W., Auwerx J. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 2013, 497:451-457.
27. Durieux J., Wolff S., Dillin A. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 2011, 144:79-91.
28. Rath E., Berger E., Messlik A., Nunes T., Liu B., Kim S.C., Hoogenraad N., Sans M., Sartor R.B., Haller D. Induction of dsRNA-activated protein kinase links mitochondrial unfolded protein response to the pathogenesis of intestinal inflammation. Gut 2012, 61:1269-1278.
29. Mouchiroud L., Houtkooper R.H., Moullan N., Katsyuba E., Ryu D., Canto C., Mottis A., Jo Y.S., Viswanathan M., Schoonjans K., et al. The NAD(+)/sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling. Cell 2013, 154:430-441.
30. Pirinen E., Canto C., Jo Y.S., Morato L., Zhang H., Menzies K.J., Williams E.G., Mouchiroud L., Moullan N., Hagberg C., et al. Pharmacological inhibition of poly(ADP-ribose) polymerases improves fitness and mitochondrial function in skeletal muscle. Cell Metab 2014, 19:1034-1041.
31. Dillin A., Hsu A.L., Arantes-Oliveira N., Lehrer-Graiwer J., Hsin H., Fraser A.G., Kamath R.S., Ahringer J., Kenyon C. Rates of behavior and aging specified by mitochondrial function during development. Science 2002, 298:2398-2401.
32. Tsang W.Y., Lemire B.D. Mitochondrial genome content is regulated during nematode development. Biochem Biophys Res Commun 2002, 291:8-16.
33. Houtkooper R.H., Pirinen E., Auwerx J. Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol 2012, 13:225-238.
34. Khan N.A., Auranen M., Paetau I., Pirinen E., Euro L., Forsstrom S., Pasila L., Velagapudi V., Carroll C.J., Auwerx J., et al. Effective treatment of mitochondrial myopathy by nicotinamide riboside, a vitamin B3. EMBO Mol Med 2014, 6:721-731.
35. Cerutti R., Pirinen E., Lamperti C., Marchet S., Sauve A.A., Li W., Leoni V., Schon E.A., Dantzer F., Auwerx J., et al. NAD(+)-dependent activation of Sirt1 corrects the phenotype in a mouse model of mitochondrial disease. Cell Metab 2014, 19:1042-1049.
36. Ryu D., Jo Y.S., Lo Sasso G., Stein S., Zhang H., Perino A., Lee J.U., Zeviani M., Romand R., Hottiger M.O., et al. A SIRT7-dependent acetylation switch of GABPbeta1 controls mitochondrial function. Cell Metab 2014, 20:856-869.
37. Haynes C.M., Petrova K., Benedetti C., Yang Y., Ron D. ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev Cell 2007, 13:467-480.
38. Haynes C.M., Yang Y., Blais S.P., Neubert T.A., Ron D. The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans. Mol Cell 2010, 37:529-540.
39. Benedetti C., Haynes C.M., Yang Y., Harding H.P., Ron D. Ubiquitin-like protein 5 positively regulates chaperone gene expression in the mitochondrial unfolded protein response. Genetics 2006, 174:229-239.
40. Horibe T., Hoogenraad N.J. The chop gene contains an element for the positive regulation of the mitochondrial unfolded protein response. PLoS ONE 2007, 2:e835.
41. Owusu-Ansah E., Song W., Perrimon N. Muscle mitohormesis promotes longevity via systemic repression of insulin signaling. Cell 2013, 155:699-712.
42. -/- mice initiate mitochondrial stress responses. Biochem J 2014, 462:359-371.
43. Aldridge J.E., Horibe T., Hoogenraad N.J. Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR) and cognate promoter elements. PLoS ONE 2007, 2:e874.
44. Baker B.M., Nargund A.M., Sun T., Haynes C.M. Protective coupling of mitochondrial function and protein synthesis via the eIF2alpha kinase GCN-2. PLoS Genet 2012, 8:e1002760.
45. Martinus R.D., Garth G.P., Webster T.L., Cartwright P., Naylor D.J., Hoj P.B., Hoogenraad N.J. Selective induction of mitochondrial chaperones in response to loss of the mitochondrial genome. Eur J Biochem 1996, 240:98-103.
46. Jeyapaul J., Jaiswal A.K. Nrf2 and c-Jun regulation of antioxidant response element (ARE)-mediated expression and induction of gamma-glutamylcysteine synthetase heavy subunit gene. Biochem Pharmacol 2000, 59:1433-1439.
47. Rauthan M., Ranji P., Aguilera Pradenas N., Pitot C., Pilon M. The mitochondrial unfolded protein response activator ATFS-1 protects cells from inhibition of the mevalonate pathway. Proc Natl Acad Sci U S A 2013, 110:5981-5986.
48. Jin S.M., Youle R.J. The accumulation of misfolded proteins in the mitochondrial matrix is sensed by PINK1 to induce PARK2/Parkin-mediated mitophagy of polarized mitochondria. Autophagy 2013, 9:1750-1757.
49. Guo B., Huang X., Zhang P., Qi L., Liang Q., Zhang X., Huang J., Fang B., Hou W., Han J., et al. Genome-wide screen identifies signaling pathways that regulate autophagy during Caenorhabditis elegans development. EMBO Rep 2014, 15:705-713.
50. Sentelle R.D., Senkal C.E., Jiang W., Ponnusamy S., Gencer S., Selvam S.P., Ramshesh V.K., Peterson Y.K., Lemasters J.J., Szulc Z.M., et al. Ceramide targets autophagosomes to mitochondria and induces lethal mitophagy. Nat Chem Biol 2012, 8:831-838.
51. Kroemer G., Marino G., Levine B. Autophagy and the integrated stress response. Mol Cell 2010, 40:280-293.
52. Thomas R.E., Andrews L.A., Burman J.L., Lin W.Y., Pallanck L.J. PINK1-Parkin pathway activity is regulated by degradation of PINK1 in the mitochondrial matrix. PLoS Genet 2014, 10:e1004279.
53. Wong A., Boutis P., Hekimi S. Mutations in the clk-1 gene of Caenorhabditis elegans affect developmental and behavioral timing. Genetics 1995, 139:1247-1259.
54. Munkacsy E., Rea S.L. The paradox of mitochondrial dysfunction and extended longevity. Exp Gerontol 2014, 56:221-233.
55. Pulliam D.A., Bhattacharya A., Van Remmen H. Mitochondrial dysfunction in aging and longevity: a causal or protective role?. Antioxid Redox Signal 2013, 19:1373-1387.
56. Rea S.L., Ventura N., Johnson T.E. Relationship between mitochondrial electron transport chain dysfunction, development, and life extension in Caenorhabditis elegans. PLoS Biol 2007, 5:e259.
57. Ventura N., Rea S.L. Caenorhabditis elegans mitochondrial mutants as an investigative tool to study human neurodegenerative diseases associated with mitochondrial dysfunction. Biotechnol J 2007, 2:584-595.
58. Schieber M., Chandel N.S. TOR signaling couples oxygen sensing to lifespan in C. elegans. Cell Rep 2014, 9:9-15.
59. Yokoyama K., Fukumoto K., Murakami T., Harada S., Hosono R., Wadhwa R., Mitsui Y., Ohkuma S. Extended longevity of Caenorhabditis elegans by knocking in extra copies of hsp70F, a homolog of mot-2 (mortalin)/mthsp70/Grp75. FEBS Lett 2002, 516:53-57.
60. Bennett C.F., Vander Wende H., Simko M., Klum S., Barfield S., Choi H., Pineda V.V., Kaeberlein M. Activation of the mitochondrial unfolded protein response does not predict longevity in Caenorhabditis elegans. Nat Commun 2014, 5:3483.