The mitochondrial unfolded protein response protects against anoxia in caenorhabditis elegans

PLoS ONE

Volumn 11, Issue 7, 2016, Pages

  Peña, Salvador ^a   Sherman, Teresa ^a   Brookes, Paul S ^a   Nehrke, Keith ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ATFS 1; UNCLASSIFIED DRUG; ATFS-1 PROTEIN, C ELEGANS; CAENORHABDITIS ELEGANS PROTEIN; M-AAA PROTEASES; METALLOPROTEINASE;

ANIMAL EXPERIMENT; ANOXIA; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GAIN OF FUNCTION MUTATION; MITOCHONDRIAL UNFOLDED PROTEIN RESPONSE; MITOCHONDRION; NERVE FIBER DEGENERATION; NONHUMAN; REPERFUSION INJURY; RNA INTERFERENCE; UNFOLDED PROTEIN RESPONSE; ANIMAL; GENETICS; HYPOXIA; METABOLISM; NERVE CELL;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; HYPOXIA; METALLOENDOPEPTIDASES; NEURONS; REPERFUSION INJURY; RNA INTERFERENCE; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE;

EID: 84980047540     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0159989     Document Type: Article

References (54)

1. Zhao Q, Wang J, Levichkin IV, Stasinopoulos S, Ryan MT, Hoogenraad NJ. A mitochondrial specific stress response in mammalian cells. The EMBO journal. 2002; 21(17):4411-9. Epub 2002/08/29. PMID: 12198143; PubMed Central PMCID: PMC126185.
2. Benedetti C, Haynes CM, Yang Y, Harding HP, Ron D. Ubiquitin-like protein 5 positively regulates chaperone gene expression in the mitochondrial unfolded protein response. Genetics. 2006; 174(1):229-39.doi: 10.1534/genetics.106.061580 PMID: 16816413; PubMed Central PMCID: PMC1569816.
3. Haynes CM, Petrova K, Benedetti C, Yang Y, Ron D. ClpP mediates activation of a mitochondrial unfolded protein response in C. Elegans. Developmental cell. 2007; 13(4):467-80. Epub 2007/10/11.doi: 10.1016/j.devcel.2007.07.016 PMID: 17925224.
4. Haynes CM, Yang Y, Blais SP, Neubert TA, Ron D. The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. Elegans. Molecular cell. 2010; 37 (4):529-40. doi: 10.1016/j.molcel.2010.01.015 PMID: 20188671; PubMed Central PMCID: PMC2846537.
5. Yoneda T, Benedetti C, Urano F, Clark SG, Harding HP, Ron D. Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. Journal of cell science. 2004; 117(Pt 18):4055-66. doi: 10.1242/jcs.01275 PMID: 15280428.
6. Lin YF, Haynes CM. Metabolism and the UPR(mt). Molecular cell. 2016; 61(5):677-82. doi: 10.1016/j. molcel.2016.02.004 PMID: 26942672; PubMed Central PMCID: PMC4779188.
7. Houtkooper RH, Mouchiroud L, Ryu D, Moullan N, Katsyuba E, Knott G, et al. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature. 2013; 497(7450):451-7. Epub 2013/05/24.doi: 10.1038/nature12188 PMID: 23698443; PubMed Central PMCID: PMC3663447.
8. Runkel ED, Liu S, Baumeister R, Schulze E. Surveillance-activated defenses block the ROS-induced mitochondrial unfolded protein response. PLoS genetics. 2013; 9(3):e1003346. doi: 10.1371/journal. pgen.1003346 PMID: 23516373; PubMed Central PMCID: PMC3597513.
9. Rauthan M, Ranji P, Abukar R, Pilon M. A Mutation in Caenorhabditis elegans NDUF-7 Activates the Mitochondrial Stress Response and Prolongs Lifespan via ROS and CED-4. G3. 2015; 5(8):1639-48.doi: 10.1534/g3.115.018598 PMID: 26038366; PubMed Central PMCID: PMC4528320.
10. Pellegrino MW, Nargund AM, Kirienko NV, Gillis R, Fiorese CJ, Haynes CM. Mitochondrial UPR-regulated innate immunity provides resistance to pathogen infection. Nature. 2014; 516(7531):414-7. doi: 10.1038/nature13818 PMID: 25274306; PubMed Central PMCID: PMC4270954.
11. Dunbar TL, Yan Z, Balla KM, Smelkinson MG, Troemel ER. C. Elegans detects pathogen-induced translational inhibition to activate immune signaling. Cell host & microbe. 2012; 11(4):375-86. doi: 10. 1016/j.chom.2012.02.008 PMID: 22520465; PubMed Central PMCID: PMC3334869.
12. Liu Y, Samuel BS, Breen PC, Ruvkun G. Caenorhabditis elegans pathways that surveil and defend mitochondria. Nature. 2014; 508(7496):406-10. doi: 10.1038/nature13204 PMID: 24695221; PubMed Central PMCID: PMC4102179.
13. Govindan JA, Jayamani E, Zhang X, Breen P, Larkins-Ford J, Mylonakis E, et al. Lipid signalling couples translational surveillance to systemic detoxification in Caenorhabditis elegans. Nature cell biology. 2015; 17(10):1294-303. doi: 10.1038/ncb3229 PMID: 26322678; PubMed Central PMCID: PMC4589496.
14. Durieux J, Wolff S, Dillin A. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell. 2011; 144(1):79-91. doi: 10.1016/j.cell.2010.12.016 PMID: 21215371; PubMed Central PMCID: PMC3062502.
15. Nargund AM, Fiorese CJ, Pellegrino MW, Deng P, Haynes CM. Mitochondrial and nuclear accumulation of the transcription factor ATFS-1 promotes OXPHOS recovery during the UPR(mt). Molecular cell. 2015; 58(1):123-33. doi: 10.1016/j.molcel.2015.02.008 PMID: 25773600; PubMed Central PMCID: PMC4385436.
16. Nargund AM, Pellegrino MW, Fiorese CJ, Baker BM, Haynes CM. Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation. Science. 2012; 337(6094):587-90. doi: 10.1126/ science.1223560 PMID: 22700657; PubMed Central PMCID: PMC3518298.
17. Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiological reviews. 2008; 88(2):581-609. doi: 10.1152/physrev.00024.2007 PMID: 18391174; PubMed Central PMCID: PMC3199571.
18. Hardy DL, Clark JB, Darley-Usmar VM, Smith DR. Reoxygenation of the hypoxic myocardium causes a mitochondrial complex I defect. Biochemical Society transactions. 1990; 18(4):549. PMID: 1703502.
19. Asimakis GK, Conti VR. Myocardial ischemia: correlation of mitochondrial adenine nucleotide and respiratory function. Journal of molecular and cellular cardiology. 1984; 16(5):439-47. PMID: 6737484.
20. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. American journal of physiology Cell physiology. 2004; 287(4):C817-33. doi: 10. 1152/ajpcell.00139.2004 PMID: 15355853.
21. Borutaite V, Mildaziene V, Brown GC, Brand MD. Control and kinetic analysis of ischemia-damaged heart mitochondria: which parts of the oxidative phosphorylation system are affected by ischemia? Biochimica et biophysica acta. 1995; 1272(3):154-8. PMID: 8541346.
22. Garcia-Rivas Gde J, Carvajal K, Correa F, Zazueta C. Ru360, a specific mitochondrial calcium uptake inhibitor, improves cardiac post-ischaemic functional recovery in rats in vivo. British journal of pharmacology. 2006; 149(7):829-37. doi: 10.1038/sj.bjp.0706932 PMID: 17031386; PubMed Central PMCID: PMC2014682.
23. Paradies G, Ruggiero FM, Petrosillo G, Quagliariello E. Peroxidative damage to cardiac mitochondria: cytochrome oxidase and cardiolipin alterations. FEBS letters. 1998; 424(3):155-8. PMID: 9539141.
24. Horwitz LD, Fennessey PV, Shikes RH, Kong Y. Marked reduction in myocardial infarct size due to prolonged infusion of an antioxidant during reperfusion. Circulation. 1994; 89(4):1792-801. PMID: 8149545.
25. Piot C, Croisille P, Staat P, Thibault H, Rioufol G, Mewton N, et al. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. The New England journal of medicine. 2008; 359(5):473-81. doi: 10.1056/NEJMoa071142 PMID: 18669426.
26. Argaud L, Gateau-Roesch O, Muntean D, Chalabreysse L, Loufouat J, Robert D, et al. Specific inhibition of the mitochondrial permeability transition prevents lethal reperfusion injury. Journal of molecular and cellular cardiology. 2005; 38(2):367-74. PMID: 15698843.
27. Kaufman DM, Crowder CM. Mitochondrial Proteostatic Collapse Leads to Hypoxic Injury. Current biology: CB. 2015; 25(16):2171-6. doi: 10.1016/j.cub.2015.06.062 PMID: 26234215.
28. Van Voorhies WA, Ward S. Broad oxygen tolerance in the nematode Caenorhabditis elegans. The Journal of experimental biology. 2000; 203(Pt 16):2467-78. PMID: 10903161.
29. Belke DD, Gloss B, Hollander JM, Swanson EA, Duplain H, Dillmann WH. In vivo gene delivery of HSP70i by adenovirus and adeno-associated virus preserves contractile function in mouse heart following ischemia-reperfusion. American journal of physiology Heart and circulatory physiology. 2006; 291(6):H2905-10. doi: 10.1152/ajpheart.00323.2006 PMID: 16920815.
30. Lin KM, Lin B, Lian IY, Mestril R, Scheffler IE, Dillmann WH. Combined and individual mitochondrial HSP60 and HSP10 expression in cardiac myocytes protects mitochondrial function and prevents apoptotic cell deaths induced by simulated ischemia-reoxygenation. Circulation. 2001; 103(13):1787-92. Epub 2001/04/03. PMID: 11282911.
31. Anderson LL, Mao X, Scott BA, Crowder CM. Survival from hypoxia in C. Elegans by inactivation of aminoacyl-tRNA synthetases. Science. 2009; 323(5914):630-3. Epub 2009/01/31. doi: 10.1126/science. 1166175 PMID: 19179530.
32. Stiernagle T. Maintenance of C. Elegans. WormBook: the online review of C elegans biology. 2006:1-11. doi: 10.1895/wormbook.1.101.1 PMID: 18050451; PubMed Central PMCID: PMC4781397.
33. Frokjaer-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM, Olesen SP, et al. Single-copy insertion of transgenes in Caenorhabditis elegans. Nature genetics. 2008; 40(11):1375-83. doi: 10. 1038/ng.248 PMID: 18953339; PubMed Central PMCID: PMC2749959.
34. Hagen FK, Nehrke K. cDNA cloning and expression of a family of UDP-N-acetyl-D-galactosamine:polypeptide N-acetylgalactosaminyltransferase sequence homologs from Caenorhabditis elegans. The Journal of biological chemistry. 1998; 273(14):8268-77. PMID: 9525933.
35. Rieckher M, Kourtis N, Pasparaki A, Tavernarakis N. Transgenesis in Caenorhabditis elegans. Methods in molecular biology. 2009; 561:21-39. doi: 10.1007/978-1-60327-019-9-2 PMID: 19504062.
36. Frokjaer-Jensen C, Davis MW, Ailion M, Jorgensen EM. Improved Mos1-mediated transgenesis in C. Elegans. Nature methods. 2012; 9(2):117-8. doi: 10.1038/nmeth.1865 PMID: 22290181; PubMed Central PMCID: PMC3725292.
37. Wojtovich AP, DiStefano P, Sherman T, Brookes PS, Nehrke K. Mitochondrial ATP-sensitive potassium channel activity and hypoxic preconditioning are independent of an inwardly rectifying potassium channel subunit in Caenorhabditis elegans. FEBS letters. 2012; 586(4):428-34. doi: 10.1016/j.febslet. 2012.01.021 PMID: 22281198; PubMed Central PMCID: PMC3288502.
38. Scott BA, Avidan MS, Crowder CM. Regulation of hypoxic death in C. Elegans by the insulin/IGF receptor homolog DAF-2. Science. 2002; 296(5577):2388-91. Epub 2002/06/18. doi: 10.1126/science.1072302 PMID: 12065745.
39. Queliconi BB, Marazzi TB, Vaz SM, Brookes PS, Nehrke K, Augusto O, et al. Bicarbonate modulates oxidative and functional damage in ischemia-reperfusion. Free radical biology & medicine. 2013; 55:46-53. doi: 10.1016/j.freeradbiomed.2012.11.007 PMID: 23195687; PubMed Central PMCID: PMC3995138.
40. Padilla PA, Nystul TG, Zager RA, Johnson AC, Roth MB. Dephosphorylation of cell cycle-regulated proteins correlates with anoxia-induced suspended animation in Caenorhabditis elegans. Molecular biology of the cell. 2002; 13(5):1473-83. doi: 10.1091/mbc.01-12-0594 PMID: 12006646; PubMed Central PMCID: PMC111120.
41. Rodriguez M, Snoek LB, De Bono M, Kammenga JE. Worms under stress: C. Elegans stress response and its relevance to complex human disease and aging. Trends in genetics: TIG. 2013; 29(6):367-74.doi: 10.1016/j.tig.2013.01.010 PMID: 23428113.
42. 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. Proceedings of the National Academy of Sciences of the United States of America. 2013; 110(15):5981-6. doi: 10.1073/ pnas.1218778110 PMID: 23530189; PubMed Central PMCID: PMC3625262.
43. Pinan-Lucarre B, Gabel CV, Reina CP, Hulme SE, Shevkoplyas SS, Slone RD, et al. The core apoptotic executioner proteins CED-3 and CED-4 promote initiation of neuronal regeneration in Caenorhabditis elegans. PLoS biology. 2012; 10(5):e1001331. doi: 10.1371/journal.pbio.1001331 PMID: 22629231; PubMed Central PMCID: PMC3358320.
44. Davis MW, Morton JJ, Carroll D, Jorgensen EM. Gene activation using FLP recombinase in C. Elegans. PLoS genetics. 2008; 4(3):e1000028. doi: 10.1371/journal.pgen.1000028 PMID: 18369447; PubMed Central PMCID: PMC2265415.
45. Groenewoud MJ, Zwartkruis FJ. Rheb and mammalian target of rapamycin in mitochondrial homoeostasis. Open biology. 2013; 3(12):130185. doi: 10.1098/rsob.130185 PMID: 24352740; PubMed Central PMCID: PMC3877845.
46. Tsang WY, Lemire BD. Mitochondrial genome content is regulated during nematode development. Biochemical and biophysical research communications. 2002; 291(1):8-16. doi: 10.1006/bbrc.2002.6394 PMID: 11829454.
47. Ratnappan R, Amrit FR, Chen SW, Gill H, Holden K, Ward J, et al. Germline signals deploy NHR-49 to modulate fatty-acid beta-oxidation and desaturation in somatic tissues of C. Elegans. PLoS genetics. 2014; 10(12):e1004829. doi: 10.1371/journal.pgen.1004829 PMID: 25474470; PubMed Central PMCID: PMC4256272.
48. Wang MC, O'Rourke EJ, Ruvkun G. Fat metabolism links germline stem cells and longevity in C. Elegans. Science. 2008; 322(5903):957-60. doi: 10.1126/science.1162011 PMID: 18988854; PubMed Central PMCID: PMC2760269.
49. Mohrin M, Shin J, Liu Y, Brown K, Luo H, Xi Y, et al. Stem cell aging. A mitochondrial UPR-mediated metabolic checkpoint regulates hematopoietic stem cell aging. Science. 2015; 347(6228):1374-7. doi: 10.1126/science.aaa2361 PMID: 25792330; PubMed Central PMCID: PMC4447312.
50. Mendenhall AR, LeBlanc MG, Mohan DP, Padilla PA. Reduction in ovulation or male sex phenotype increases long-term anoxia survival in a daf-16-independent manner in Caenorhabditis elegans. Physiological genomics. 2009; 36(3):167-78. doi: 10.1152/physiolgenomics.90278.2008 PMID: 19050081; PubMed Central PMCID: PMC2646460.
51. Dillin A, Hsu AL, Arantes-Oliveira N, Lehrer-Graiwer J, Hsin H, Fraser AG, et al. Rates of behavior and aging specified by mitochondrial function during development. Science. 2002; 298(5602):2398-401.doi: 10.1126/science.1077780 PMID: 12471266.
52. Mabon ME, Mao X, Jiao Y, Scott BA, Crowder CM. Systematic identification of gene activities promoting hypoxic death. Genetics. 2009; 181(2):483-96. doi: 10.1534/genetics.108.097188 PMID: 19047414; PubMed Central PMCID: PMC2644942.
53. Bennett CF, Vander Wende H, Simko M, Klum S, Barfield S, Choi H, et al. Activation of the mitochondrial unfolded protein response does not predict longevity in Caenorhabditis elegans. Nature communications. 2014; 5:3483. doi: 10.1038/ncomms4483 PMID: 24662282; PubMed Central PMCID: PMC3984390.
54. Arnould T, Michel S, Renard P. Mitochondria Retrograde Signaling and the UPR mt: Where Are We in Mammals? International journal of molecular sciences. 2015; 16(8):18224-51. doi: 10.3390/ ijms160818224 PMID: 26258774; PubMed Central PMCID: PMC4581242.