Yeast DJ-1 Superfamily Members Are Required for Diauxic-shift Reprogramming and Cell Survival in Stationary Phase

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2014 Apr 8

PMID 24706893

Citations 26

Authors

Leonor Miller-Fleming

Pedro Antas

Teresa Faria Pais

Joshua L Smalley

Flaviano Giorgini

Tiago Fleming Outeiro

Affiliations

Soon will be listed here.

Abstract

The yeast Hsp31 minifamily proteins (Hsp31, Hsp32, Hsp33, Hsp34) belong to the highly conserved DJ-1 superfamily. The human DJ-1 protein is associated with cancer and neurodegenerative disorders, such as Parkinson disease. However, the precise function of human and yeast DJ-1 proteins is unclear. Here we show that the yeast DJ-1 homologs have a role in diauxic-shift (DS), characterized by metabolic reprogramming because of glucose limitation. We find that the Hsp31 genes are strongly induced in DS and in stationary phase (SP), and that deletion of these genes reduces chronological lifespan, impairs transcriptional reprogramming at DS, and impairs the acquisition of several typical characteristics of SP, including autophagy induction. In addition, under carbon starvation, the HSP31 family gene-deletion strains display impaired autophagy, disrupted target of rapamycin complex 1 (TORC1) localization to P-bodies, and caused abnormal TORC1-mediated Atg13 phosphorylation. Repression of TORC1 by rapamycin in the gene-deletion strains completely reversed their sensitivity to heat shock. Taken together, our data indicate that Hsp31 minifamily is required for DS reprogramming and cell survival in SP, and plays a role upstream of TORC1. The enhanced understanding of the cellular function of these genes sheds light into the biological role of other members of the superfamily, including DJ-1, which is an attractive target for therapeutic intervention in cancer and in Parkinson disease.

Citing Articles

Elucidation and engineering mitochondrial respiratory-related genes for improving bioethanol production at high temperature in .

Qi X, Wang Z, Lin Y, Guo Y, Dai Z, Wang Q Eng Microbiol. 2024; 4(2):100108.

PMID: 39629328 PMC: 11610969. DOI: 10.1016/j.engmic.2023.100108.

Screening and In Silico Analyses of the Yeast Σ1278b Bank Mutants Using Citral as a Natural Antimicrobial.

El Harati R, Fancello F, Multineddu C, Zara G, Zara S Foods. 2024; 13(10).

PMID: 38790757 PMC: 11119076. DOI: 10.3390/foods13101457.

Contrasting views on the role of AMPK in autophagy.

Kim D Bioessays. 2024; 46(3):e2300211.

PMID: 38214366 PMC: 10922896. DOI: 10.1002/bies.202300211.

Divergence in the Saccharomyces Species' Heat Shock Response Is Indicative of Their Thermal Tolerance.

Fay J, Alonso-Del-Real J, Miller J, Querol A Genome Biol Evol. 2023; 15(11).

PMID: 37972247 PMC: 10683043. DOI: 10.1093/gbe/evad207.

Interplay of energy metabolism and autophagy.

Feng Y, Chen Y, Wu X, Chen J, Zhou Q, Liu B Autophagy. 2023; 20(1):4-14.

PMID: 37594406 PMC: 10761056. DOI: 10.1080/15548627.2023.2247300.

References

Takahara T, Maeda T . Transient sequestration of TORC1 into stress granules during heat stress. Mol Cell. 2012; 47(2):242-52. DOI: 10.1016/j.molcel.2012.05.019. View

Buchan J, Parker R . Eukaryotic stress granules: the ins and outs of translation. Mol Cell. 2010; 36(6):932-41. PMC: 2813218. DOI: 10.1016/j.molcel.2009.11.020. View

Hod Y, Pentyala S, Whyard T, El-Maghrabi M . Identification and characterization of a novel protein that regulates RNA-protein interaction. J Cell Biochem. 1999; 72(3):435-44. View

Ren H, Fu K, Mu C, Li B, Wang D, Wang G . DJ-1, a cancer and Parkinson's disease associated protein, regulates autophagy through JNK pathway in cancer cells. Cancer Lett. 2010; 297(1):101-8. DOI: 10.1016/j.canlet.2010.05.001. View

Wei Y, Ringe D, Wilson M, Ondrechen M . Identification of functional subclasses in the DJ-1 superfamily proteins. PLoS Comput Biol. 2007; 3(1):e10. PMC: 1782040. DOI: 10.1371/journal.pcbi.0030010. View

Cookson M . Parkinsonism due to mutations in PINK1, parkin, and DJ-1 and oxidative stress and mitochondrial pathways. Cold Spring Harb Perspect Med. 2012; 2(9):a009415. PMC: 3426824. DOI: 10.1101/cshperspect.a009415. View

Irrcher I, Aleyasin H, Seifert E, Hewitt S, Chhabra S, Phillips M . Loss of the Parkinson's disease-linked gene DJ-1 perturbs mitochondrial dynamics. Hum Mol Genet. 2010; 19(19):3734-46. DOI: 10.1093/hmg/ddq288. View

Dechant R, Peter M . Nutrient signals driving cell growth. Curr Opin Cell Biol. 2008; 20(6):678-87. DOI: 10.1016/j.ceb.2008.09.009. View

Lee J, Kim C, Kim J, Park C . DJR-1.2 of Caenorhabditis elegans is induced by DAF-16 in the dauer state. Gene. 2013; 524(2):373-6. DOI: 10.1016/j.gene.2013.04.032. View

10.

Wei M, Fabrizio P, Hu J, Ge H, Cheng C, Li L . Life span extension by calorie restriction depends on Rim15 and transcription factors downstream of Ras/PKA, Tor, and Sch9. PLoS Genet. 2008; 4(1):e13. PMC: 2213705. DOI: 10.1371/journal.pgen.0040013. View

11.

Rustici G, Kolesnikov N, Brandizi M, Burdett T, Dylag M, Emam I . ArrayExpress update--trends in database growth and links to data analysis tools. Nucleic Acids Res. 2012; 41(Database issue):D987-90. PMC: 3531147. DOI: 10.1093/nar/gks1174. View

12.

Santos P, Simoes T, Sa-Correia I . Insights into yeast adaptive response to the agricultural fungicide mancozeb: a toxicoproteomics approach. Proteomics. 2009; 9(3):657-70. DOI: 10.1002/pmic.200800452. View

13.

DeRisi J, Iyer V, Brown P . Exploring the metabolic and genetic control of gene expression on a genomic scale. Science. 1997; 278(5338):680-6. DOI: 10.1126/science.278.5338.680. View

14.

Pedruzzi I, Burckert N, Egger P, de Virgilio C . Saccharomyces cerevisiae Ras/cAMP pathway controls post-diauxic shift element-dependent transcription through the zinc finger protein Gis1. EMBO J. 2000; 19(11):2569-79. PMC: 212766. DOI: 10.1093/emboj/19.11.2569. View

15.

Laplante M, Sabatini D . mTOR signaling in growth control and disease. Cell. 2012; 149(2):274-93. PMC: 3331679. DOI: 10.1016/j.cell.2012.03.017. View

16.

Wilson M, St Amour C, Collins J, Ringe D, Petsko G . The 1.8-A resolution crystal structure of YDR533Cp from Saccharomyces cerevisiae: a member of the DJ-1/ThiJ/PfpI superfamily. Proc Natl Acad Sci U S A. 2004; 101(6):1531-6. PMC: 341769. DOI: 10.1073/pnas.0308089100. View

17.

Wilson M . The role of cysteine oxidation in DJ-1 function and dysfunction. Antioxid Redox Signal. 2010; 15(1):111-22. PMC: 3110098. DOI: 10.1089/ars.2010.3481. View

18.

Xie Z, Nair U, Klionsky D . Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell. 2008; 19(8):3290-8. PMC: 2488302. DOI: 10.1091/mbc.e07-12-1292. View

19.

Galdieri L, Mehrotra S, Yu S, Vancura A . Transcriptional regulation in yeast during diauxic shift and stationary phase. OMICS. 2010; 14(6):629-38. PMC: 3133784. DOI: 10.1089/omi.2010.0069. View

20.

Krebiehl G, Ruckerbauer S, Burbulla L, Kieper N, Maurer B, Waak J . Reduced basal autophagy and impaired mitochondrial dynamics due to loss of Parkinson's disease-associated protein DJ-1. PLoS One. 2010; 5(2):e9367. PMC: 2826413. DOI: 10.1371/journal.pone.0009367. View