Unmasking a temperature-dependent effect of the P. anserina i-AAA protease on aging and development

Cell Cycle

Volumn 10, Issue 24, 2011, Pages 4280-4290

  Weil, Andrea ^a   Luce, Karin ^a   Dröse, Stefan ^a   Wittig, Ilka ^a   Brandt, Ulrich ^a   Osiewacz, Heinz D ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Aging; i AAA protease; Mitochondria; Podospora anserina; Protein quality control; Temperature

Indexed keywords

FUNGAL ENZYME; PODOSPORA ANSERINA I AAA PROTEASE; UNCLASSIFIED DRUG;

AGING; ARTICLE; CONTROLLED STUDY; FRUITING BODY; FUNGAL DEVELOPMENT; FUNGAL SPORE GERMINATION; FUNGAL STRAIN; GENE DELETION; INCUBATION TEMPERATURE; LIFESPAN; NONHUMAN; PHENOTYPE; PODOSPORA ANSERINA; WILD TYPE;

EID: 84055190025     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.24.18560     Document Type: Article

References (58)

1. Brand MD. The sites and topology of mitochondrial superoxide production. Exp Gerontol 2010; 45:466- 72; PMID:20064600; http://dx.doi.org/10.1016/j. exger.2010.01.003.
2. Luce K, Weil AC, Osiewacz HD. Mitochondrial protein quality control systems in aging and disease. In: Tavernarakis N, Ed. Protein metabolism and homeostasis in aging. New York: Springer US 2010:108-125.
3. Tatsuta T, Langer T. Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J 2008; 27:306-14; PMID:18216873; http:// dx.doi.org/10.1038/sj.emboj.7601972.
4. Osiewacz HD. Mitochondrial quality control in aging and lifespan control of the fungal aging model Podospora anserina. Biochem Soc Trans 2011; 39:1488- 92; PMID:21936839.
5. Juhola MK, Shah ZH, Grivell LA, Jacobs HT. The mitochondrial inner membrane AAA metalloprotease family in metazoans. FEBS Lett 2000; 481:91-5; PMID:10996302; http://dx.doi.org/10.1016/S0014- 5793(00)01989-X.
6. Leonhard K, Herrmann JM, Stuart RA, Mannhaupt G, Neupert W, Langer T. AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. EMBO J 1996; 15:4218-29; PMID:8861950.
7. Leonhard K, Stiegler A, Neupert W, Langer T. Chaperone-like activity of the AAA domain of the yeast Yme1 AAA protease. Nature 1999; 398:348-51; PMID:10192337; http://dx.doi.org/10.1038/18704.
8. Thorsness PE, Fox TD. Nuclear mutations in Saccharomyces cerevisiae that affect the escape of DNA from mitochondria to the nucleus. Genetics 1993; 134:21-8; PMID:8514129.
9. Campbell CL, Tanaka N, White KH, Thorsness PE. Mitochondrial morphological and functional defects in yeast caused by yme1 are suppressed by mutation of a 26S protease subunit homologue. Mol Biol Cell 1994; 5:899-905; PMID:7803857.
10. Pearce DA, Sherman F. Degradation of cytochrome oxidase subunits in mutants of yeast lacking cytochrome c and suppression of the degradation by mutation of yme1. J Biol Chem 1995; 270:20879- 82; PMID:7673107; http://dx.doi.org/10.1074/ jbc.270.36.20879.
11. Augustin S, Nolden M, Müller S, Hardt O, Arnold I, Langer T. Characterization of peptides released from mitochondria: evidence for constant proteolysis and peptide efflux. J Biol Chem 2005; 280:2691- 9; PMID:15556950; http://dx.doi.org/10.1074/jbc. M410609200.
12. Kambacheld M, Augustin S, Tatsuta T, Müller S, Langer T. Role of the novel metallopeptidase Mop112 and saccharolysin for the complete degradation of proteins residing in different subcompartments of mitochondria. J Biol Chem 2005; 280:20132-9; PMID:15772085; http://dx.doi.org/10.1074/jbc. M500398200.
13. Rainey RN, Glavin JD, Chen HW, French SW, Teitell MA, Koehler CM. A new function in translocation for the mitochondrial i-AAA protease Yme1: import of polynucleotide phosphorylase into the intermembrane space. Mol Cell Biol 2006; 26:8488- 97; PMID:16966379; http://dx.doi.org/10.1128/ MCB.01006-06.
14. Nebauer R, Schuiki I, Kulterer B, Trajanoski Z, Daum G. The phosphatidylethanolamine level of yeast mitochondria is affected by the mitochondrial components Oxa1p and Yme1p. FEBS J 2007; 274:6180-90; PMID:17976194; http://dx.doi.org/10.1111/j.1742- 4658.2007.06138.x.
15. Klanner C, Prokisch H, Langer T. MAP-1 and IAP- 1, two novel AAA proteases with catalytic sites on opposite membrane surfaces in mitochondrial inner membrane of Neurospora crassa. Mol Biol Cell 2001; 12:2858-69; PMID:11553723.
16. Graef M, Seewald G, Langer T. Substrate recognition by AAA+ ATPases: Distinct substrate binding modes in the ATP-dependent protease Yme1 of the mitochondrial intermembrane space. Mol Cell Biol 2007; 27:2476-85; PMID:17261594; http://dx.doi. org/10.1128/MCB.01721-06.
17. Shah ZH, Hakkaart GA, Arku B, de Jong L, van der Spek H, Grivell LA, et al. The human homologue of the yeast mitochondrial AAA metalloprotease Yme1p complements a yeast yme1 disruptant. FEBS Lett 2000; 478:267-70; PMID:10930580; http://dx.doi. org/10.1016/S0014-5793(00)01859-7.
18. Aldridge JE, Horibe T, Hoogenraad NJ. Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR) and cognate promoter elements. PLoS ONE 2007; 2:874; PMID:17849004; http:// dx.doi.org/10.1371/journal.pone. 0000874.
19. Edgar D, Trifunovic A. The mtDNA mutator mouse: Dissecting mitochondrial involvement in aging. Aging (Albany NY) 2009; 1:1028-32; PMID:20157586.
20. Hur JH, Cho J, Walker DW. Aging: Dial M for Mitochondria. Aging (Albany NY) 2010; 2:69-73; PMID:20228940.
21. Osiewacz HD. Mitochondrial functions and aging. Gene 2002; 286:65-71; PMID:11943461; http:// dx.doi.org/10.1016/S0378-1119(01)00804-6.
22. Wallace DC. A mitochondrial paradigm of metabolic and degenerative diseases, aging and cancer: a dawn for evolutionary medicine. Annu Rev Genet 2005; 39:359- 407; PMID:16285865; http://dx.doi.org/10.1146/ annurev.genet.39.110304.095751.
23. Osiewacz HD, Hermanns J, Marcou D, Triffi M, Esser K. Mitochondrial DNA rearrangements are correlated with a delayed amplification of the mobile intron (plDNA) in a long-lived mutant of Podospora anserina. Mutat Res 1989; 219:9-15; PMID:2911274.
24. Soerensen M, Gredilla R, Müller-Ohldach M, Werner A, Bohr VA, Osiewacz HD, et al. A potential impact of DNA repair on ageing and lifespan in the ageing model organism Podospora anserina: decrease in mitochondrial DNA repair activity during ageing. Mech Ageing Dev 2009; 130:487-96; PMID:19486911; http://dx.doi. org/10.1016/j.mad.2009.05.003.
25. Gredilla R, Grief J, Osiewacz HD. Mitochondrial free radical generation and lifespan control in the fungal aging model Podospora anserina. Exp Gerontol 2006; 41:439-47; PMID:16530367; http://dx.doi. org/10.1016/j.exger.2006.01.010.
26. Zintel S, Schwitalla D, Luce K, Hamann A, Osiewacz HD. Increasing mitochondrial superoxide dismutase abundance leads to impairments in protein quality control and ROS scavenging systems and to lifespan shortening. Exp Gerontol 2010; 45:525- 32; PMID:20080171; http://dx.doi.org/10.1016/j. exger.2010.01.006.
27. Zintel S, Bernhardt D, Rogowska-Wrzesinska A, Osiewacz HD. PaCATB, a secreted catalase protecting Podospora anserina against exogenous oxidative stress. Aging (Albany NY) 2011; 3:768-81; PMID:21865610.
28. Stumpferl SW, Stephan O, Osiewacz HD. Impact of a disruption of a pathway delivering copper to mitochondria on Podospora anserina metabolism and life span. Eukaryot Cell 2004; 3:200-11; PMID:14871950; http://dx.doi.org/10.1128/EC. 3.1.200-211.2004.
29. Scheckhuber CQ, Erjavec N, Tinazli A, Hamann A, Nyström T, Osiewacz HD. Reducing mitochondrial fission results in increased life span and fitness of two fungal ageing models. Nat Cell Biol 2007; 9:99- 105; PMID:17173038; http://dx.doi.org/10.1038/ ncb1524.
30. Brust D, Daum B, Breunig C, Hamann A, Kühlbrandt W, Osiewacz HD. Cyclophilin D links programmed cell death and organismal aging in Podospora anserina. Aging Cell 2010; 9:761-75; PMID:20626725; http:// dx.doi.org/10.1111/ j.1474-9726.2010.00609.x.
31. Hamann A, Brust D, Osiewacz HD. Deletion of putative apoptosis factors leads to lifespan extension in the fungal ageing model Podospora anserina. Mol Microbiol 2007; 65:948-58; PMID:17627766; http://dx.doi. org/10.1111/j.1365- 2958.2007.05839.x.
32. Osiewacz HD. Regulation of the mitochondrial transition pore: impact on mammalian aging. Aging (Albany NY) 2011; 3:10-1; PMID:21248375.
33. Luce K, Osiewacz HD. Increasing organismal healths pan by enhancing mitochondrial protein quality control. Nat Cell Biol 2009; 11:852-8; PMID:19543272; http://dx.doi.org/10.1038/ncb1893.
34. Osiewacz HD, Brust D, Hamann A, Kunstmann B, Luce K, Müller-Ohldach M, et al. Mitochondrial pathways governing stress resistance, life and death in the fungal aging model Podospora anserina. Ann NY Acad Sci 2010; 1197:54-66; PMID:20536834; http:// dx.doi.org/10.1111/j.1749-6632.2010.05190.x.
35. Hamann A, Krause K, Werner A, Osiewacz HD. A two-step protocol for efficient deletion of genes in the filamentous ascomycete Podospora anserina. Curr Genet 2005; 48:270-5; PMID:16160832; http:// dx.doi.org/10.1007/s00294-005- 0018-1.
36. Campbell CL, Thorsness PE. Escape of mitochondrial DNA to the nucleus in yme1 yeast is mediated by vacuolar-dependent turnover of abnormal mitochondrial compartments. J Cell Sci 1998; 111:2455-64; PMID:9683639.
37. Weber ER, Hanekamp T, Thorsness PE. Biochemical and functional analysis of the YME1 gene product, an ATP and zinc-dependent mitochondrial protease from S. cerevisiae. Mol Biol Cell 1996; 7:307-17; PMID:8688560.
38. Arnold I, Wagner-Ecker M, Ansorge W, Langer T. Evidence for a novel mitochondria-to-nucleus signalling pathway in respiring cells lacking i-AAA protease and the ABC-transporter Mdl1. Gene 2006; 367:74- 88; PMID:16403607; http://dx.doi.org/10.1016/j. gene.2005.09.044.
39. Leonhard K, Guiard B, Pellecchia G, Tzagoloff A, Neupert W, Langer T. Membrane protein degradation by AAA proteases in mitochondria: extraction of substrates from either membrane surface. Mol Cell 2000; 5:629-38; PMID:10882099; http://dx.doi. org/10.1016/S1097-2765(00)80242-7.
40. Kolodziejczak M, Gibala M, Urantowka A, Janska H. The significance of Arabidopsis AAA proteases for activity and assembly/stability of mitochondrial OXPHOS complexes. Physiol Plant 2007; 129:135-42; http://dx.doi.org/10.1111/j. 1399-3054.2006.00835.x.
41. Krause F, Scheckhuber CQ, Werner A, Rexroth S, Reifschneider NH, Dencher NA, et al. Supramolecular organization of cytochrome c oxidase- and alternative oxidase-dependent respiratory chains in the filamentous fungus Podospora anserina. J Biol Chem 2004; 279:26453-61; PMID:15044453; http://dx.doi. org/10.1074/jbc.M402756200.
42. Harman D. Free radical theory of aging: dietary implications. Am J Clin Nutr 1972; 25:839-43; PMID:5046729.
43. Kunstmann B, Osiewacz HD. Overexpression of an S-adenosylmethionine- dependent methyltransferase leads to an extended lifespan of Podospora anserina without impairments in vital functions. Aging Cell 2008; 7:651-62; PMID:18616635; http://dx.doi. org/10.1111/j.1474-9726.2008.00412.x.
44. Kunstmann B, Osiewacz HD. The S-adenosylmethionine dependent O-methyltransferase PaMTH1: a longevity assurance factor protecting Podospora anserina against oxidative stress. Aging (Albany NY) 2009; 1:328-34; PMID:20157520.
45. Palermo V, Falcone C, Mazzoni C. Apoptosis and aging in mitochondrial morphology mutants of S. cerevisiae. Folia Microbiol (Praha) 2007; 52:479- 83; PMID:18298044; http://dx.doi.org/10.1007/ BF02932107.
46. Gibala M, Kicia M, Sakamoto W, Gola EM, Kubrakiewicz J, Smakowska E, et al. The lack of mitochondrial AtFtsH4 protease alters Arabidopsis leaf morphology at the late stage of rosette development under short-day photoperiod. Plant J 2009; 59:685-99; PMID:19453455; http://dx.doi.org/10.1111/j.1365-313X. 2009.03907.x.
47. Thorsness PE, White KH, Fox TD. Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae. Mol Cell Biol 1993; 13:5418- 26; PMID:8355690.
48. Potting C, Wilmes C, Engmann T, Osman C, Langer T. Regulation of mitochondrial phospholipids by Ups1/PRELI-like proteins depends on proteolysis and Mdm35. EMBO J 2010; 29:2888-98; PMID:20657548; http://dx.doi.org/10.1038/ emboj.2010.169.
49. Chen Z, Seo JY, Kim YK, Lee SR, Kim KH, Cho KH, et al. Heat modulation of tropoelastin, fibrillin-1 and matrix metalloproteinase-12 in human skin in vivo. J Invest Dermatol 2005; 124:70-8; PMID:15654955; http://dx.doi.org/10. 1111/j.0022-202X.2004.23550.x.
50. Tulapurkar ME, Asiegbu BE, Singh IS, Hasday JD. Hyperthermia in the febrile range induces HSP72 expression proportional to exposure temperature but not to HSF-1 DNA-binding activity in human lung epithelial A549 cells. Cell Stress Chaperones 2009; 14:499-508; PMID:19221897; http://dx.doi. org/10.1007/s12192-009-0103-3.
51. Ellis S, Killender M, Anderson RL. Heat-induced alterations in the localization of HSP72 and HSP73 as measured by indirect immunohistochemistry and immunogold electron microscopy. J Histochem Cytochem 2000; 48:321-32; PMID:10681386; http:// dx.doi.org/10.1177/002215540004800302.
52. Rizet G. Sur l'impossibilité d'obtenir la multiplication végétative ininterrompue illimitée de l'ascomycète Podospora anserina. C R Acad Sci Paris 1953; 237:838- 40; PMID:13107134.
53. Müller-Ohldach M, Brust D, Hamann A, Osiewacz HD. Overexpression of PaParp encoding the poly(ADPribose) polymerase of Podospora anserina affects organismal aging. Mech Ageing Dev 2011; 132:33-42; PMID:21145908; http://dx.doi.org/10.1016/j. mad.2010.11.003.
54. Esser K. Podospora anserina. In: King RC, Ed. Handbook of Genetics. New York: Plenum Press 1974; 531-51.
55. Osiewacz HD. A versatile shuttle cosmid vector for the efficient construction of genomic libraries and for the cloning of fungal genes. Curr Genet 1994; 26:87-90; PMID:7954902; http://dx.doi.org/10.1007/ BF00326309.
56. Wittig I, Braun HP, Schägger H. Blue native PAGE. Nat Protoc 2006; 1:418-28; PMID:17406264; http:// dx.doi.org/10.1038/nprot.2006.62.
57. Borghouts C, Werner A, Elthon T, Osiewacz HD. Copper-modulated gene expression and senescence in the filamentous fungus Podospora anserina. Mol Cell Biol 2001; 21:390-9; PMID:11134328; http://dx.doi. org/10.1128/MCB.21.2.390- 399.2001.
58. Tocilescu MA, Fendel U, Zwicker K, Kerscher S, Brandt U. Exploring the ubiquinone binding cavity of respiratory complex I. J Biol Chem 2007; 282:29514- 20; PMID:17681940; http://dx.doi.org/10.1074/jbc. M704519200.