PMT1 deficiency enhances basal UPR activity and extends replicative lifespan of Saccharomyces cerevisiae

Age

Volumn 37, Issue 3, 2015, Pages

  Cui, Hong Jing ^a   Liu, Xin Guang ^b,c   McCormick, Mark ^d   Wasko, Brian M ^e   Zhao, Wei ^b,c   He, Xin ^b,c   Yuan, Yuan ^b,c   Fang, Bing Xiong ^b,c   Sun, Xue Rong ^b,c   Kennedy, Brian K ^b,d   Suh, Yousin ^b,f   Zhou, Zhong Jun ^b,g   Kaeberlein, Matt ^b,e   Feng, Wen Li ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

^b GUANGDONG MEDICAL UNIVERSITY   (China)

^c Key Laboratory for Medical Molecular Diagnostics of Guangdong Province   (China)

^d BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^g UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Lifespan; Protein O mannosyltransferase; Saccharomyces cerevisiae; Unfolded protein response

Indexed keywords

ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FUNGAL GENE; GENE DELETION; GENE DISRUPTION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HAC1 GENE; HOMOLOGOUS RECOMBINATION; IRE1 GENE; LIFE EXTENSION; NONHUMAN; PMT1 GENE; PROTEIN FOLDING; RNA SPLICING; SACCHAROMYCES CEREVISIAE; UNFOLDED PROTEIN RESPONSE; UPREGULATION; AGING; GENETICS; LONGEVITY; METABOLISM; POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; HAC1 PROTEIN, S CEREVISIAE; IRE1 PROTEIN, S CEREVISIAE; MANNOSYLTRANSFERASE; MEMBRANE PROTEIN; PROTEIN O-MANNOSYLTRANSFERASE; PROTEIN SERINE THREONINE KINASE; REPRESSOR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

AGING; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; BLOTTING, WESTERN; ENDOPLASMIC RETICULUM STRESS; LONGEVITY; MANNOSYLTRANSFERASES; MEMBRANE GLYCOPROTEINS; POLYMERASE CHAIN REACTION; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UNFOLDED PROTEIN RESPONSE;

EID: 84928910731     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-015-9788-7     Document Type: Article

References (49)

1. Arroyo J, Hutzler J, Bermejo C et al (2011) Functional and genomic analyses of blocked protein O-mannosylation in baker's yeast. Mol Microbiol 79(6):1529–1546. doi:10.1111/j.1365-2958.2011.07537.x
2. Baudin A, Ozier-Kalogeropoulos O, Denouel A et al (1993) A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res 21(14):3329–3330
3. Boisson-Dernier A, Lituiev DS, Nestorova A et al (2013) ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLoS Biol 11(11):e1001719. doi:10.1371/journal.pbio.1001719
4. Burtner CR, Murakami CJ, Olsen B et al (2011) A genomic analysis of chronological longevity factors in budding yeast. Cell Cycle 10(9):1385–1396
5. Chen D, Thomas EL, Kapahi P (2009) HIF-1 modulates dietary restriction-mediated lifespan extension via IRE-1 in Caenorhabditis elegans. PLoS Genet 5(5):e1000486. doi:10.1371/journal.pgen.1000486
6. Cox JS, Walter P (1996) A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87(3):391–404
7. Delaney JR, Ahmed U, Chou A et al (2013) Stress profiling of longevity mutants identifies Afg3 as a mitochondrial determinant of cytoplasmic mRNA translation and aging. Aging Cell 12(1):156–166. doi:10.1111/acel.12032
8. Gentzsch M, Tanner W (1996) The PMT gene family: protein O-glycosylation in Saccharomyces cerevisiae is vital. EMBO J 15(21):5752–5759
9. Girrbach V, Strahl S (2003) Members of the evolutionarily conserved PMT family of protein O-mannosyltransferases form distinct protein complexes among themselves. J Biol Chem 278(14):12554–12562. doi:10.1074/jbc.M212582200 M212582200
10. Gonzalez M, Brito N, Frias M et al (2013) Botrytis cinerea protein O-mannosyltransferases play critical roles in morphogenesis, growth, and virulence. PLoS One 8(6):e65924. doi:10.1371/journal.pone.0065924
11. Goto M (2007) Protein O-glycosylation in fungi: diverse structures and multiple functions. Biosci Biotechnol Biochem 71(6):1415–1427
12. Hamann T, Denness L (2011) Cell wall integrity maintenance in plants: lessons to be learned from yeast? Plant Signal Behav 6(11):1706–1709. doi:10.4161/psb.6.11.17782 17782
13. Harty C, Strahl S, Romisch K (2001) O-mannosylation protects mutant alpha-factor precursor from endoplasmic reticulum-associated degradation. Mol Biol Cell 12(4):1093–1101
14. Henis-Korenblit S, Zhang P, Hansen M et al (2010) Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity. Proc Natl Acad Sci U S A 107(21):9730–9735. doi:10.1073/pnas.1002575107
15. Henry KA, Blank HM, Hoose SA et al (2010) The unfolded protein response is not necessary for the G1/S transition, but it is required for chromosome maintenance in Saccharomyces cerevisiae. PLoS One 5(9):e12732. doi:10.1371/journal.pone.0012732
16. Immervoll T, Gentzsch M, Tanner W (1995) PMT3 and PMT4, two new members of the protein-O-mannosyltransferase gene family of Saccharomyces cerevisiae. Yeast 11(14):1345–1351. doi:10.1002/yea.320111403
17. Jonikas MC, Collins SR, Denic V et al (2009) Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 323(5922):1693–1697. doi:10.1126/science.1167983 323/5922/1693
18. Kaeberlein M (2010) Lessons on longevity from budding yeast. Nature 464(7288):513–519. doi:10.1038/nature08981 nature08981
19. Kaeberlein M, Guarente L (2002) Saccharomyces cerevisiae MPT5 and SSD1 function in parallel pathways to promote cell wall integrity. Genetics 160(1):83–95
20. Kaeberlein M, Kennedy BK (2005) Large-scale identification in yeast of conserved ageing genes. Mech Ageing Dev (1) 17–21. doi:10.1016/j.mad.2004.09.013
21. Kaeberlein M, McVey M, Guarente L (1999) The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev 13(19):2570–2580
22. Kaeberlein M, Andalis AA, Liszt GB et al (2004) Saccharomyces cerevisiae SSD1-V confers longevity by a Sir2p-independent mechanism. Genetics 166(4):1661–1672
23. Kaeberlein M, Powers RW 3rd, Steffen KK et al (2005) Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310(5751):1193–1196. doi:10.1126/science.1115535
24. Kennedy BK, Gotta M, Sinclair DA et al (1997) Redistribution of silencing proteins from telomeres to the nucleolus is associated with extension of life span in S. cerevisiae. Cell 89(3):381–391
25. Kimata Y, Ishiwata-Kimata Y, Yamada S et al (2006) Yeast unfolded protein response pathway regulates expression of genes for anti-oxidative stress and for cell surface proteins. Genes Cells 11(1):59–69. doi:10.1111/j.1365-2443.2005.00921.x
26. Labunskyy VM, Gerashchenko MV, Delaney JR et al (2014) Lifespan extension conferred by endoplasmic reticulum secretory pathway deficiency requires induction of the unfolded protein response. PLoS Genet 10(1):e1004019. doi:10.1371/journal.pgen.1004019
27. Lengeler KB, Tielker D, Ernst JF (2008) Protein-O-mannosyltransferases in virulence and development. Cell Mol Life Sci 65(4):528–544. doi:10.1007/s00018-007-7409-z
28. Loibl M, Strahl S (2013) Protein O-mannosylation: what we have learned from baker's yeast. Biochim Biophys Acta 1833(11):2438–2446. doi:10.1016/j.bbamcr.2013.02.008
29. Longo VD, Shadel GS, Kaeberlein M et al (2012) Replicative and chronological aging in Saccharomyces cerevisiae. Cell Metab 16(1):18–31. doi:10.1016/j.cmet.2012.06.002
30. Lussier M, Gentzsch M, Sdicu AM et al (1995) Protein O-glycosylation in yeast. The PMT2 gene specifies a second protein O-mannosyltransferase that functions in addition to the PMT1-encoded activity. J Biol Chem 270(6):2770–2775
31. McCormick MA, Mason AG, Guyenet SJ et al (2014) The SAGA histone deubiquitinase module controls yeast replicative lifespan via Sir2 interaction. Cell Rep 8(2):477–486. doi:10.1016/j.celrep.2014.06.037
32. Mori T, Ogasawara C, Inada T et al (2010) Dual functions of yeast tRNA ligase in the unfolded protein response: unconventional cytoplasmic splicing of HAC1 pre-mRNA is not sufficient to release translational attenuation. Mol Biol Cell 21(21):3722–3734. doi:10.1091/mbc.E10-08-0693
33. Mortimer RK, Johnston JR (1959) Life span of individual yeast cells. Nature 183(4677):1751–1752
34. Nishida N, Jing D, Kuroda K et al (2014) Activation of signaling pathways related to cell wall integrity and multidrug resistance by organic solvent in Saccharomyces cerevisiae. Curr Genet 60(3):149–162. doi:10.1007/s00294-013-0419-5
35. Ray A, Hector RE, Roy N et al (2003) Sir3p phosphorylation by the Slt2p pathway effects redistribution of silencing function and shortened lifespan. Nat Genet 33(4):522–526. doi:10.1038/ng1132
36. Salminen A, Kaarniranta K (2010) ER stress and hormetic regulation of the aging process. Ageing Res Rev 9(3):211–217. doi:10.1016/j.arr.2010.04.003
37. Sikorski RS, Hieter P (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122(1):19–27
38. Stearns T, Ma H, Botstein D (1990) Manipulating yeast genome using plasmid vectors. Methods Enzymol 185:280–297
39. Steffen KK, MacKay VL, Kerr EO et al (2008) Yeast life span extension by depletion of 60s ribosomal subunits is mediated by Gcn4. Cell 133(2):292–302. doi:10.1016/j.cell.2008.02.037
40. Steffen KK, Kennedy BK, Kaeberlein M (2009) Measuring replicative life span in the budding yeast. J Vis Exp (28). doi:10.3791/1209 1209
41. Steffen KK, McCormick MA, Pham KM et al (2012) Ribosome deficiency protects against ER stress in Saccharomyces cerevisiae. Genetics 191(1):107–118. doi:10.1534/genetics.111.136549
42. Taylor RC, Dillin A (2013) XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity. Cell 153(7):1435–1447. doi:10.1016/j.cell.2013.05.042
43. Travers KJ, Patil CK, Wodicka L et al (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101(3):249–258
44. Viswanathan M, Kim SK, Berdichevsky A et al (2005) A role for SIR-2.1 regulation of ER stress response genes in determining C. elegans life span. Dev Cell 9(5):605–615
45. Wang SL, Cheng MY (2012) The defects in cell wall integrity and G2-M transition of the htl1 mutant are interconnected. Yeast 29(1):45–57. doi:10.1002/yea.1916
46. Welihinda AA, Kaufman RJ (1996) The unfolded protein response pathway in Saccharomyces cerevisiae. Oligomerization and trans-phosphorylation of Ire1p (Ern1p) are required for kinase activation. J Biol Chem 271(30):18181–18187
47. Xu C, Wang S, Thibault G et al (2013) Futile protein folding cycles in the ER are terminated by the unfolded protein O-mannosylation pathway. Science 340(6135):978–981. doi:10.1126/science.1234055
48. Zhao W, Fang BX, Niu YJ et al (2014) Nar1 deficiency results in shortened lifespan and sensitivity to paraquat that is rescued by increased expression of mitochondrial superoxide dismutase. Mech Ageing Dev 138:53–58. doi:10.1016/j.mad.2014.01.007
49. Zhou J, Zhou BO, Lenzmeier BA et al (2009) Histone deacetylase Rpd3 antagonizes Sir2-dependent silent chromatin propagation. Nucleic Acids Res 37(11):3699–3713. doi:10.1093/nar/gkp233