Dynamic post-transcriptional regulation by Mrn1 links cell wall homeostasis to mitochondrial structure and function


Autoři: Kendra Reynaud aff001;  Molly Brothers aff002;  Michael Ly aff002;  Nicholas T. Ingolia aff001
Působiště autorů: California Institute for Quantitative Biosciences, University of California, Berkeley, Berkeley, California, United States of America aff001;  Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California, United States of America aff002
Vyšlo v časopise: Dynamic post-transcriptional regulation by Mrn1 links cell wall homeostasis to mitochondrial structure and function. PLoS Genet 17(4): e1009521. doi:10.1371/journal.pgen.1009521
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009521

Souhrn

The RNA-binding protein Mrn1 in Saccharomyces cerevisiae targets over 300 messenger RNAs, including many involved in cell wall biogenesis. The impact of Mrn1 on these target transcripts is not known, however, nor is the cellular role for this regulation. We have shown that Mrn1 represses target mRNAs through the action of its disordered, asparagine-rich amino-terminus. Its endogenous targets include the paralogous SUN domain proteins Nca3 and Uth1, which affect mitochondrial and cell wall structure and function. While loss of MRN1 has no effect on fermentative growth, we found that mrn1Δ yeast adapt more quickly to respiratory conditions. These cells also have enlarged mitochondria in fermentative conditions, mediated in part by dysregulation of NCA3, and this may explain their faster switch to respiration. Our analyses indicated that Mrn1 acts as a hub for integrating cell wall integrity and mitochondrial biosynthesis in a carbon-source responsive manner.

Klíčová slova:

Mitochondria – Biosynthesis – Cell walls – Gene expression – Glucose – Membrane proteins – Messenger RNA – Yeast


Zdroje

1. Gerstberger S, Hafner M, Tuschl T. A census of human RNA-binding proteins. Nat Rev Genet. 2014;15: 829–845. doi: 10.1038/nrg3813 25365966

2. Keene JD. RNA regulons: coordination of post-transcriptional events. Nat Rev Genet. 2007;8: 533–543. doi: 10.1038/nrg2111 17572691

3. Miller D, Brandt N, Gresham D. Systematic identification of factors mediating accelerated mRNA degradation in response to changes in environmental nitrogen. PLoS Genet. 2018;14: e1007406. doi: 10.1371/journal.pgen.1007406 29782489

4. Harvey R, Dezi V, Pizzinga M, Willis AE. Post-transcriptional control of gene expression following stress: the role of RNA-binding proteins. Biochem Soc Trans. 2017;45: 1007–1014. doi: 10.1042/BST20160364 28710288

5. Hogan DJ, Riordan DP, Gerber AP, Herschlag D, Brown PO. Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol. 2008;6: e255. doi: 10.1371/journal.pbio.0060255 18959479

6. Düring L, Thorsen M, Petersen DSN, Køster B, Jensen TH, Holmberg S. MRN1 implicates chromatin remodeling complexes and architectural factors in mRNA maturation. PLoS One. 2012;7: e44373. doi: 10.1371/journal.pone.0044373 23028530

7. Calabretta S, Richard S. Emerging Roles of Disordered Sequences in RNA-Binding Proteins. Trends Biochem Sci. 2015;40: 662–672. doi: 10.1016/j.tibs.2015.08.012 26481498

8. Zagrovic B, Bartonek L, Polyansky AA. RNA-protein interactions in an unstructured context. FEBS Lett. 2018;592: 2901–2916. doi: 10.1002/1873-3468.13116 29851074

9. Mitchell SF, Jain S, She M, Parker R. Global analysis of yeast mRNPs. Nat Struct Mol Biol. 2013;20: 127–133. doi: 10.1038/nsmb.2468 23222640

10. Chang Y, Huh W-K. Ksp1-dependent phosphorylation of eIF4G modulates post-transcriptional regulation of specific mRNAs under glucose deprivation conditions. Nucleic Acids Res. 2018;46: 3047–3060. doi: 10.1093/nar/gky097 29438499

11. Swisher KD, Parker R. Localization to, and effects of Pbp1, Pbp4, Lsm12, Dhh1, and Pab1 on stress granules in Saccharomyces cerevisiae. PLoS One. 2010;5: e10006. doi: 10.1371/journal.pone.0010006 20368989

12. Bresson S, Shchepachev V, Spanos C, Turowski TW, Rappsilber J, Tollervey D. Stress-Induced Translation Inhibition through Rapid Displacement of Scanning Initiation Factors. Mol Cell. 2020. doi: 10.1016/j.molcel.2020.09.021 33053322

13. Pélissier P, Camougrand N, Velours G, Guérin M. NCA3, a nuclear gene involved in the mitochondrial expression of subunits 6 and 8 of the Fo-F1 ATP synthase of S. cerevisiae. Curr Genet. 1995;27: 409–416. doi: 10.1007/BF00311209 7586026

14. Roncero C, Vázquez de Aldana CR. Glucanases and Chitinases. Curr Top Microbiol Immunol. 2020;425: 131–166. doi: 10.1007/82_2019_185 31807894

15. Coller JM, Gray NK, Wickens MP. mRNA stabilization by poly(A) binding protein is independent of poly(A) and requires translation. Genes Dev. 1998;12: 3226–3235. doi: 10.1101/gad.12.20.3226 9784497

16. Ritch JJ, Davidson SM, Sheehan JJ, Austriaco N. The Saccharomyces SUN gene, UTH1, is involved in cell wall biogenesis. FEMS Yeast Res. 2010;10: 168–176. doi: 10.1111/j.1567-1364.2009.00601.x 20070376

17. Balcerak A, Trebinska-Stryjewska A, Konopinski R, Wakula M, Grzybowska EA. RNA-protein interactions: disorder, moonlighting and junk contribute to eukaryotic complexity. Open Biol. 2019;9: 190096. doi: 10.1098/rsob.190096 31213136

18. Muller R, Meacham ZA, Ferguson L, Ingolia NT. CiBER-seq dissects genetic networks by quantitative CRISPRi profiling of expression phenotypes. bioRxiv. 2020. p. 2020.03.29.015057. doi: 10.1126/science.abb9662 33303588

19. Gilbert LA, Horlbeck MA, Adamson B, Villalta JE, Chen Y, Whitehead EH, et al. Genome-Scale CRISPR-Mediated Control of Gene Repression and Activation. Cell. 2014;159: 647–661. doi: 10.1016/j.cell.2014.09.029 25307932

20. Smith JD, Suresh S, Schlecht U, Wu M, Wagih O, Peltz G, et al. Quantitative CRISPR interference screens in yeast identify chemical-genetic interactions and new rules for guide RNA design. Genome Biol. 2016;17: 45. doi: 10.1186/s13059-016-0900-9 26956608

21. Muller R, Meacham ZA, Ferguson L, Ingolia NT. CiBER-seq dissects genetic networks by quantitative CRISPRi profiling of expression phenotypes. Science. 2020;370. doi: 10.1126/science.abb9662 33303588

22. Aranda-Díaz A, Mace K, Zuleta I, Harrigan P, El-Samad H. Robust Synthetic Circuits for Two-Dimensional Control of Gene Expression in Yeast. ACS Synth Biol. 2017;6: 545–554. doi: 10.1021/acssynbio.6b00251 27930885

23. Lobel JH, Gross JD. Pat1 increases the range of decay factors and RNA bound by the Lsm1-7 complex. RNA. 2020. doi: 10.1261/rna.075812.120 32513655

24. Bonnerot C, Boeck R, Lapeyre B. The two proteins Pat1p (Mrt1p) and Spb8p interact in vivo, are required for mRNA decay, and are functionally linked to Pab1p. Mol Cell Biol. 2000;20: 5939–5946. doi: 10.1128/mcb.20.16.5939-5946.2000 10913177

25. Wu D, Muhlrad D, Bowler MW, Jiang S, Liu Z, Parker R, et al. Lsm2 and Lsm3 bridge the interaction of the Lsm1-7 complex with Pat1 for decapping activation. Cell Res. 2014;24: 233–246. doi: 10.1038/cr.2013.152 24247251

26. Larimer FW, Stevens A. Disruption of the gene XRN1, coding for a 5’—-3’ exoribonuclease, restricts yeast cell growth. Gene. 1990;95: 85–90. doi: 10.1016/0378-1119(90)90417-p 1979303

27. Rendl LM, Bieman MA, Vari HK, Smibert CA. The eIF4E-binding protein Eap1p functions in Vts1p-mediated transcript decay. PLoS One. 2012;7: e47121. doi: 10.1371/journal.pone.0047121 23071728

28. Xing Z, Ma WK, Tran EJ. The DDX5/Dbp2 subfamily of DEAD-box RNA helicases. Wiley Interdiscip Rev RNA. 2019;10: e1519. doi: 10.1002/wrna.1519 30506978

29. Santiveri CM, Mirassou Y, Rico-Lastres P, Martínez-Lumbreras S, Pérez-Cañadillas JM. Pub1p C-terminal RRM domain interacts with Tif4631p through a conserved region neighbouring the Pab1p binding site. PLoS One. 2011;6: e24481. doi: 10.1371/journal.pone.0024481 21931728

30. Duttagupta R, Tian B, Wilusz CJ, Khounh DT, Soteropoulos P, Ouyang M, et al. Global analysis of Pub1p targets reveals a coordinate control of gene expression through modulation of binding and stability. Mol Cell Biol. 2005;25: 5499–5513. doi: 10.1128/MCB.25.13.5499-5513.2005 15964806

31. Levin DE. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 2005;69: 262–291. doi: 10.1128/MMBR.69.2.262-291.2005 15944456

32. Bresson S, Shchepachev V, Spanos C, Turowski T, Rappsilber J, Tollervey D. Stress-induced translation inhibition through rapid displacement of scanning initiation factors. Available: https://www.biorxiv.org/content/10.1101/2020.05.14.096354v2.full.pdf 33053322

33. Kawai S, Hashimoto W, Murata K. Transformation of Saccharomyces cerevisiae and other fungi: methods and possible underlying mechanism. Bioeng Bugs. 2010;1: 395–403. doi: 10.4161/bbug.1.6.13257 21468206

34. Wallace EWJ, Kear-Scott JL, Pilipenko EV, Schwartz MH, Laskowski PR, Rojek AE, et al. Reversible, Specific, Active Aggregates of Endogenous Proteins Assemble upon Heat Stress. Cell. 2015;162: 1286–1298. doi: 10.1016/j.cell.2015.08.041 26359986

35. Di Bartolomeo F, Malina C, Campbell K, Mormino M, Fuchs J, Vorontsov E, et al. Absolute yeast mitochondrial proteome quantification reveals trade-off between biosynthesis and energy generation during diauxic shift. Proc Natl Acad Sci U S A. 2020;117: 7524–7535. doi: 10.1073/pnas.1918216117 32184324

36. Kroschwald S, Munder MC, Maharana S, Franzmann TM, Richter D, Ruer M, et al. Different Material States of Pub1 Condensates Define Distinct Modes of Stress Adaptation and Recovery. Cell Rep. 2018;23: 3327–3339. doi: 10.1016/j.celrep.2018.05.041 29898402

37. Stovicek V, Borja GM, Forster J, Borodina I. EasyClone 2.0: expanded toolkit of integrative vectors for stable gene expression in industrial Saccharomyces cerevisiae strains. J Ind Microbiol Biotechnol. 2015;42: 1519–1531. doi: 10.1007/s10295-015-1684-8 26376869

38. Vongsamphanh R, Fortier PK, Ramotar D. Pir1p mediates translocation of the yeast Apn1p endonuclease into the mitochondria to maintain genomic stability. Mol Cell Biol. 2001;21: 1647–1655. doi: 10.1128/MCB.21.5.1647-1655.2001 11238901

39. Green R, Lesage G, Sdicu A-M, Ménard P, Bussey H. A synthetic analysis of the Saccharomyces cerevisiae stress sensor Mid2p, and identification of a Mid2p-interacting protein, Zeo1p, that modulates the PKC1-MPK1 cell integrity pathway. Microbiology. 2003;149: 2487–2499. doi: 10.1099/mic.0.26471-0 12949174

40. Teixeira D, Parker R. Analysis of P-body assembly in Saccharomyces cerevisiae. Mol Biol Cell. 2007;18: 2274–2287. doi: 10.1091/mbc.e07-03-0199 17429074

41. Bouveret E, Rigaut G, Shevchenko A, Wilm M, Séraphin B. A Sm-like protein complex that participates in mRNA degradation. EMBO J. 2000;19: 1661–1671. doi: 10.1093/emboj/19.7.1661 10747033

42. Kuznetsov E, Kučerová H, Váchová L, Palková Z. SUN family proteins Sun4p, Uth1p and Sim1p are secreted from Saccharomyces cerevisiae and produced dependently on oxygen level. PLoS One. 2013;8: e73882. doi: 10.1371/journal.pone.0073882 24040106

43. Fehrenbacher KL, Boldogh IR, Pon LA. A role for Jsn1p in recruiting the Arp2/3 complex to mitochondria in budding yeast. Mol Biol Cell. 2005;16: 5094–5102. doi: 10.1091/mbc.e05-06-0590 16107558

44. Haramati O, Brodov A, Yelin I, Atir-Lande A, Samra N, Arava Y. Identification and characterization of roles for Puf1 and Puf2 proteins in the yeast response to high calcium. Sci Rep. 2017;7: 3037. doi: 10.1038/s41598-017-02873-z 28596535

45. Malina C, Larsson C, Nielsen J. Yeast mitochondria: an overview of mitochondrial biology and the potential of mitochondrial systems biology. FEMS Yeast Res. 2018;18. doi: 10.1093/femsyr/foy040 29788060

46. Cadenas E, Davies KJA. Mitochondrial free radical generation, oxidative stress, and aging11This article is dedicated to the memory of our dear friend, colleague, and mentor Lars Ernster (1920–1998), in gratitude for all he gave to us. Free Radical Biology and Medicine. 2000;29: 222–230. doi: 10.1016/s0891-5849(00)00317-8 11035250

47. Lapointe CP, Stefely JA, Jochem A, Hutchins PD, Wilson GM, Kwiecien NW, et al. Multi-omics Reveal Specific Targets of the RNA-Binding Protein Puf3p and Its Orchestration of Mitochondrial Biogenesis. Cell Syst. 2018;6: 125–135.e6. doi: 10.1016/j.cels.2017.11.012 29248374

48. Almagro Armenteros JJ, Salvatore M, Emanuelsson O, Winther O, von Heijne G, Elofsson A, et al. Detecting sequence signals in targeting peptides using deep learning. Life Sci Alliance. 2019;2. doi: 10.26508/lsa.201900429 31570514

49. Donzeau M, Káldi K, Adam A, Paschen S, Wanner G, Guiard B, et al. Tim23 links the inner and outer mitochondrial membranes. Cell. 2000;101: 401–412. doi: 10.1016/s0092-8674(00)80850-8 10830167

50. Voisine C, Schilke B, Ohlson M, Beinert H, Marszalek J, Craig EA. Role of the mitochondrial Hsp70s, Ssc1 and Ssq1, in the maturation of Yfh1. Mol Cell Biol. 2000;20: 3677–3684. doi: 10.1128/mcb.20.10.3677-3684.2000 10779357

51. Lewrenz I, Rietzschel N, Guiard B, Lill R, van der Laan M, Voos W. The functional interaction of mitochondrial Hsp70s with the escort protein Zim17 is critical for Fe/S biogenesis and substrate interaction at the inner membrane preprotein translocase. J Biol Chem. 2013;288: 30931–30943. doi: 10.1074/jbc.M113.465997 24030826

52. Wei J, Sherman F. Sue1p is required for degradation of labile forms of altered cytochromes C in yeast mitochondria. J Biol Chem. 2004;279: 30449–30458. doi: 10.1074/jbc.M403742200 15123691

53. Wenz L-S, Ellenrieder L, Qiu J, Bohnert M, Zufall N, van der Laan M, et al. Sam37 is crucial for formation of the mitochondrial TOM-SAM supercomplex, thereby promoting β-barrel biogenesis. J Cell Biol. 2015;210: 1047–1054. doi: 10.1083/jcb.201504119 26416958

54. Zheng J, Li L, Jiang H. Molecular pathways of mitochondrial outer membrane protein degradation. Biochem Soc Trans. 2019;47: 1437–1447. doi: 10.1042/BST20190275 31652437

55. Horn D, Barrientos A. Mitochondrial copper metabolism and delivery to cytochrome c oxidase. IUBMB Life. 2008;60: 421–429. doi: 10.1002/iub.50 18459161

56. Kumar A, Agarwal S, Heyman JA, Matson S, Heidtman M, Piccirillo S, et al. Subcellular localization of the yeast proteome. Genes Dev. 2002;16: 707–719. doi: 10.1101/gad.970902 11914276

57. Nilsen TW. The fundamentals of RNA purification. Cold Spring Harb Protoc. 2013;2013: 618–624. doi: 10.1101/pdb.top075838 23818674

58. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15: 550. doi: 10.1186/s13059-014-0550-8 25516281


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