Metabolic and chaperone gene loss marks the origin of animals: Evidence for Hsp104 and Hsp78 chaperones sharing mitochondrial enzymes as clients

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Erives, Albert J ^a   Fassler, Jan S ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 104; HEAT SHOCK PROTEIN 78; MITOCHONDRIAL ENZYME; PROTEIN CLPB; UNCLASSIFIED DRUG; ACONITATE HYDRATASE; ENDOPEPTIDASE CLP; HEAT SHOCK PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CHOANOFLAGELLATE; CYTOSOL; EVOLUTION; FUNGUS; GASTRULATION; GENE; GENE CONTROL; GENE FUNCTION; GENE LOSS; LYS4 GENE; MASS SPECTROMETRY; MITOCHONDRION; NONHUMAN; PROMOTER REGION; PROTEIN INTERACTION; PROTEIN PURIFICATION; ANIMAL; BAYES THEOREM; CLASSIFICATION; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION; PHYLOGENY; SACCHAROMYCES CEREVISIAE; STATISTICAL MODEL;

ANIMALIA; CHOANOFLAGELLIDA; EUKARYOTA; FUNGI;

ACONITATE HYDRATASE; ANIMALS; BAYES THEOREM; CHOANOFLAGELLATA; ENDOPEPTIDASE CLP; HEAT-SHOCK PROTEINS; LIKELIHOOD FUNCTIONS; MITOCHONDRIA; MUTATION; PHYLOGENY; PROMOTER REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84923370377     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117192     Document Type: Article

References (86)

1. Degnan BM, Vervoort M, Larroux C, Richards GS (2009) Early evolution of metazoan transcription factors. Current opinion in genetics & development 19: 591-599.
2. Gazave E, Lapebie P, Richards GS, Brunet F, Ereskovsky AV, et al. (2009) Origin and evolution of the Notch signalling pathway: an overview from eukaryotic genomes. BMC Evol Biol 9: 249. doi: 10.1186/1471-2148-9-249 PMID: 19825158
3. Richards GS, Degnan BM (2009) The dawn of developmental signaling in the Metazoa. Cold Spring Harbor symposia on quantitative biology 74: 81-90. doi: 10.1101/sqb.2009.74.028 PMID: 19903747
4. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, et al. (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466: 720-726. doi: 10.1038/nature09201 PMID: 20686567
5. Sebe-Pedros A, de Mendoza A, Lang BF, Degnan BM, Ruiz-Trillo I (2011) Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol Biol Evol 28: 1241-1254. doi: 10.1093/molbev/msq309 PMID: 21087945
6. Larroux C, Fahey B, Liubicich D, Hinman VF, Gauthier M, et al. (2006) Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Evol Dev 8: 150-173. PMID: 16509894
7. Nakanishi N, Sogabe S, Degnan BM (2014) Evolutionary origin of gastrulation: insights from sponge development. BMC Biol 12: 26. doi: 10.1186/1741-7007-12-26 PMID: 24678663
8. Ryan JF, Pang K, Schnitzler CE, Nguyen AD, Moreland RT, et al. (2013) The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342: 1242592. doi: 10.1126/science.1242592 PMID: 24337300
9. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, et al. (2008) The Trichoplax genome and the nature of placozoans. Nature 454: 955-960. doi: 10.1038/nature07191 PMID: 18719581
10. Simakov O, Marletaz F, Cho SJ, Edsinger-Gonzales E, Havlak P, et al. (2013) Insights into bilaterian evolution from three spiralian genomes. Nature 493: 526-531. doi: 10.1038/nature11696 PMID: 23254933
11. King N, Westbrook MJ, Young SL, Kuo A, Abedin M, et al. (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451: 783-788. doi: 10.1038/nature06617 PMID: 18273011
12. Dayel MJ, Alegado RA, Fairclough SR, Levin TC, Nichols SA, et al. (2011) Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Dev Biol 357: 73-82. doi: 10.1016/j.ydbio.2011.06.003 PMID: 21699890
13. Suga H, Chen Z, de Mendoza A, Sebe-Pedros A, Brown MW, et al. (2013) The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat Commun 4: 2325. doi: 10.1038/ncomms3325 PMID: 23942320
14. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, et al. (2009) EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19: 327-335. doi: 10.1101/gr.073585.107 PMID: 19029536
15. Guberman JM, Ai J, Arnaiz O, Baran J, Blake A, et al. (2011) BioMart Central Portal: an open database network for the biological community. Database (Oxford) 2011: bar041. doi: 10.1093/database/bar041 PMID: 21930507
16. Mostafavi S, Ray D, Warde-Farley D, Grouios C, Morris Q (2008) GeneMANIA: a real-time multiple association network integration algorithm for predicting gene function. Genome biology 9 Suppl 1: S4. doi: 10.1186/gb-2008-9-s1-s4 PMID: 18613948
17. Warde-Farley D, Donaldson SL, Comes O, Zuberi K, Badrawi R, et al. (2010) The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res 38: W214-220. doi: 10.1093/nar/gkq537 PMID: 20576703
18. Yu RC, Resnekov O, Abola AP, Andrews SS, Benjamin KR, et al. (2008) The Alpha Project: a model system for systems biology research. IET Syst Biol 2: 222-233. doi: 10.1049/iet-syb:20080127 PMID: 19045818
19. Zarin T, Moses AM (2014) Insights into molecular evolution from yeast genomics. Yeast.
20. Fairclough SR, Chen Z, Kramer E, Zeng Q, Young S, et al. (2013) Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol 14: R15. doi: 10.1186/gb-2013-14-2-r15 PMID: 23419129
21. Haider S, Ballester B, Smedley D, Zhang J, Rice P, et al. (2009) BioMart Central Portal - unified access to biological data. Nucleic Acids Res 37: W23-27. doi: 10.1093/nar/gkp265 PMID: 19420058
22. Wendler P, Shorter J, Plisson C, Cashikar AG, Lindquist S, et al. (2007) Atypical AAA+ subunit packing creates an expanded cavity for disaggregation by the protein-remodeling factor Hsp104. Cell 131: 1366-1377. PMID: 18160044
23. Wendler P, Shorter J, Snead D, Plisson C, Clare DK, et al. (2009) Motor mechanism for protein threading through Hsp104. Molecular Cell 34: 81-92. doi: 10.1016/j.molcel.2009.02.026 PMID: 19362537
24. Leonhardt SA, Fearson K, Danese PN, Mason TL (1993) HSP78 encodes a yeast mitochondrial heat shock protein in the Clp family of ATP-dependent proteases. Mol Cell Biol 13: 6304-6313. PMID: 8413229
25. Moczko M, Schonfisch B, Voos W, Pfanner N, Rassow J (1995) The mitochondrial ClpB homolog Hsp78 cooperates with matrix Hsp70 in maintenance of mitochondrial function. J Mol Biol 254: 538-543. PMID: 7500331
26. Schmitt M, Neupert W, Langer T (1996) The molecular chaperone Hsp78 confers compartment-specific thermotolerance to mitochondria. J Cell Biol 134: 1375-1386. PMID: 8830768
27. Tkach JM, Glover JR (2008) Nucleocytoplasmic trafficking of the molecular chaperone Hsp104 in unstressed and heat-shocked cells. Traffic 9: 39-56. PMID: 17973656
28. Desantis ME, Leung EH, Sweeny EA, Jackrel ME, Cushman-Nick M, et al. (2012) Operational plasticity enables hsp104 to disaggregate diverse amyloid and nonamyloid clients. Cell 151: 778-793. doi: 10.1016/j.cell.2012.09.038 PMID: 23141537
29. Shorter J (2008) Hsp104: a weapon to combat diverse neurodegenerative disorders. Neuro-Signals 16: 63-74. PMID: 18097161
30. Neuwald AF, Aravind L, Spouge JL, Koonin EV (1999) AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9: 27-43. PMID: 9927482
31. Hibbs MA, Hess DC, Myers CL, Huttenhower C, Li K, et al. (2007) Exploring the functional landscape of gene expression: directed search of large microarray compendia. Bioinformatics 23: 2692-2699. PMID: 17724061
32. Amin J, Mestril R, Schiller P, Dreano M, Voellmy R (1987) Organization of the Drosophila melanogaster hsp70 heat shock regulation unit. Mol Cell Biol 7: 1055-1062. PMID: 3104769
33. Xiao H, Lis JT (1988) Germline transformation used to define key features of heat-shock response elements. Science 239: 1139-1142. PMID: 3125608
34. Perisic O, Xiao H, Lis JT (1989) Stable binding of Drosophila heat shock factor to head-to-head and tail-to- tail repeats of a conserved 5 bp recognition unit. Cell 59: 797-806. PMID: 2590940
35. Bonner JJ, Ballou C, Fackenthal DL (1994) Interactions between DNA-bound trimers of the yeast heat shock factor. Mol Cell Biol 14: 501-508. PMID: 8264619
36. Hashikawa N, Yamamoto N, Sakurai H (2007) Different mechanisms are involved in the transcriptional activation by yeast heat shock transcription factor through two different types of heat shock elements. J Biol Chem 282: 10333-10340. PMID: 17289668
37. Kobayashi N, McEntee K (1993) Identification of cis and trans components of a novel heat shock stress regulatory pathway in Saccharomyces cerevisiae. Mol Cell Biol 13: 248-256. PMID: 8417330
38. Martinez-Pastor MT, Marchler G, Schuller C, Marchler-Bauer A, Ruis H, et al. (1996) The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15: 2227-2235. PMID: 8641288
39. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431: 99-104. PMID: 15343339
40. Kominek J, Marszalek J, Neuveglise C, Craig EA, Williams BL (2013) The complex evolutionary dynamics of Hsp70s: a genomic and functional perspective. Genome Biol Evol 5: 2460-2477. doi: 10.1093/gbe/evt192 PMID: 24277689
41. Haslbeck M, Miess A, Stromer T, Walter S, Buchner J (2005) Disassembling protein aggregates in the yeast cytosol. The cooperation of Hsp26 with Ssa1 and Hsp104. J Biol Chem 280: 23861-23868. PMID: 15843375
42. Eliyahu E, Lesnik C, Arava Y (2012) The protein chaperone Ssa1 affects mRNA localization to the mitochondria. FEBS Lett 586: 64-69. doi: 10.1016/j.febslet.2011.11.025 PMID: 22138184
43. Meimaridou E, Gooljar SB, Chapple JP (2009) From hatching to dispatching: the multiple cellular roles of the Hsp70 molecular chaperone machinery. Journal of molecular endocrinology 42: 1-9. doi: 10.1677/JME-08-0116 PMID: 18852216
44. Malinovska L, Kroschwald S, Munder MC, Richter D, Alberti S (2012) Molecular chaperones and stress-inducible protein-sorting factors coordinate the spatiotemporal distribution of protein aggregates. Mol Biol Cell 23: 3041-3056. doi: 10.1091/mbc.E12-03-0194 PMID: 22718905
45. Kryndushkin DS, Smirnov VN, Ter-Avanesyan MD, Kushnirov VV (2002) Increased expression of Hsp40 chaperones, transcriptional factors, and ribosomal protein Rpp0 can cure yeast prions. J Biol Chem 277: 23702-23708. PMID: 11923285
46. Lian HY, Zhang H, Zhang ZR, Loovers HM, Jones GW, et al. (2007) Hsp40 interacts directly with the native state of the yeast prion protein Ure2 and inhibits formation of amyloid-like fibrils. J Biol Chem 282: 11931-11940. PMID: 17324933
47. Kryndushkin DS, Shewmaker F, Wickner RB (2008) Curing of the [URE3] prion by Btn2p, a Batten disease-related protein. EMBO J 27: 2725-2735. doi: 10.1038/emboj.2008.198 PMID: 18833194
48. Kanneganti V, Kama R, Gerst JE (2011) Btn3 is a negative regulator of Btn2-mediated endosomal protein trafficking and prion curing in yeast. Mol Biol Cell 22: 1648-1663. doi: 10.1091/mbc.E10-11-0878 PMID: 21441304
49. Lee TI, Rinaldi NJ, Robert F, Odom DT, Bar-Joseph Z, et al. (2002) Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298: 799-804. PMID: 12399584
50. Sanchez Y, Lindquist SL (1990) HSP104 required for induced thermotolerance. Science 248: 1112-1115. PMID: 2188365
51. Sanchez Y, Taulien J, Borkovich KA, Lindquist S (1992) Hsp104 is required for tolerance to many forms of stress. EMBO J 11: 2357-2364. PMID: 1600951
52. Glover JR, Lindquist S (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94: 73-82. PMID: 9674429
53. Krzewska J, Langer T, Liberek K (2001) Mitochondrial Hsp78, a member of the Clp/Hsp100 family in Saccharomyces cerevisiae, cooperates with Hsp70 in protein refolding. FEBS Lett 489: 92-96. PMID: 11231020
54. Rottgers K, Zufall N, Guiard B, Voos W (2002) The ClpB homolog Hsp78 is required for the efficient degradation of proteins in the mitochondrial matrix. J Biol Chem 277: 45829-45837. PMID: 12237310
55. Lewandowska A, Gierszewska M, Marszalek J, Liberek K (2006) Hsp78 chaperone functions in restoration of mitochondrial network following heat stress. Biochim Biophys Acta 1763: 141-151. PMID: 16545993
56. Kosuge T, Hoshino T (1999) The alpha-aminoadipate pathway for lysine biosynthesis is widely distributed among Thermus strains. J Biosci Bioeng 88: 672-675. PMID: 16232683
57. Fondi M, Brilli M, Emiliani G, Paffetti D, Fani R (2007) The primordial metabolism: an ancestral interconnection between leucine, arginine, and lysine biosynthesis. BMC Evol Biol 7 Suppl 2: S3. PMID: 17767731
58. Fazius F, Shelest E, Gebhardt P, Brock M (2012) The fungal alpha-aminoadipate pathway for lysine biosynthesis requires two enzymes of the aconitase family for the isomerization of homocitrate to homoisocitrate. Mol Microbiol 86: 1508-1530. doi: 10.1111/mmi.12076 PMID: 23106124
59. Quezada H, Marin-Hernandez A, Aguilar D, Lopez G, Gallardo-Perez JC, et al. (2011) The Lys20 homocitrate synthase isoform exerts most of the flux control over the lysine synthesis pathway in Saccharomyces cerevisiae. Mol Microbiol 82: 578-590. doi: 10.1111/j.1365-2958.2011.07832.x PMID: 21895798
60. Lill R, Dutkiewicz R, Elsasser HP, Hausmann A, Netz DJ, et al. (2006) Mechanisms of iron-sulfur protein maturation in mitochondria, cytosol and nucleus of eukaryotes. Biochim Biophys Acta 1763: 652-667. PMID: 16843540
61. Gautschi M, Lilie H, Funfschilling U, Mun A, Ross S, et al. (2001) RAC, a stable ribosome-associated complex in yeast formed by the DnaK-DnaJ homologs Ssz1p and zuotin. Proc Natl Acad Sci U S A 98: 3762-3767. PMID: 11274393
62. Gautschi M, Mun A, Ross S, Rospert S (2002) A functional chaperone triad on the yeast ribosome. Proc Natl Acad Sci U S A 99: 4209-4214. PMID: 11929994
63. Rakwalska M, Rospert S (2004) The ribosome-bound chaperones RAC and Ssb1/2p are required for accurate translation in Saccharomyces cerevisiae. Mol Cell Biol 24: 9186-9197. PMID: 15456889
64. Willmund F, del Alamo M, Pechmann S, Chen T, Albanese V, et al. (2013) The cotranslational function of ribosome-associated Hsp70 in eukaryotic protein homeostasis. Cell 152: 196-209. doi: 10.1016/j.cell.2012.12.001 PMID: 23332755
65. Yamamoto Y, Poole LB, Hantgan RR, Kamio Y (2002) An iron-binding protein, Dpr, from Streptococcus mutans prevents iron-dependent hydroxyl radical formation in vitro. J Bacteriol 184: 2931-2939. PMID: 12003933
66. Thomas C, Mackey MM, Diaz AA, Cox DP (2009) Hydroxyl radical is produced via the Fenton reaction in submitochondrial particles under oxidative stress: implications for diseases associated with iron accumulation. Redox report: communications in free radical research 14: 102-108. doi: 10.1179/135100009X392566 PMID: 19490751
67. Lee S, Carlson T, Christian N, Lea K, Kedzie J, et al. (2000) The yeast heat shock transcription factor changes conformation in response to superoxide and temperature. Mol Biol Cell 11: 1753-1764. PMID: 10793149
68. Imlay JA (2006) Iron-sulphur clusters and the problem with oxygen. Mol Microbiol 59: 1073-1082. PMID: 16430685
69. Py B, Moreau PL, Barras F (2011) Fe-S clusters, fragile sentinels of the cell. Curr Opin Microbiol 14: 218-223. doi: 10.1016/j.mib.2011.01.004 PMID: 21288764
70. Verghese J, Abrams J, Wang Y, Morano KA (2012) Biology of the heat shock response and protein chaperones: budding yeast (Saccharomyces cerevisiae) as a model system. Microbiology and molecular biology reviews: MMBR 76: 115-158. doi: 10.1128/MMBR.05018-11 PMID: 22688810
71. Lum R, Niggemann M, Glover JR (2008) Peptide and protein binding in the axial channel of Hsp104. Insights into the mechanism of protein unfolding. J Biol Chem 283: 30139-30150. doi: 10.1074/jbc.M804849200 PMID: 18755692
72. Thorsness PE, Fox TD (1990) Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Nature 346: 376-379. PMID: 2165219
73. Gong Y, Kakihara Y, Krogan N, Greenblatt J, Emili A, et al. (2009) An atlas of chaperone-protein interactions in Saccharomyces cerevisiae: implications to protein folding pathways in the cell. Molecular Systems Biology 5: 275. doi: 10.1038/msb.2009.26 PMID: 19536198
74. Degnan BM, Leys SP, Larroux C (2005) Sponge development and antiquity of animal pattern formation. Integr Comp Biol 45: 335-341. doi: 10.1093/icb/45.2.335 PMID: 21676778
75. Leys SP, Yahel G, Reidenbach MA, Tunnicliffe V, Shavit U, et al. (2011) The sponge pump: the role of current induced flow in the design of the sponge body plan. PLoS One 6: e27787. doi: 10.1371/journal.pone.0027787 PMID: 22180779
76. Nielsen C (2008) Six major steps in animal evolution: are we derived sponge larvae? Evol Dev 10: 241-257. doi: 10.1111/j.1525-142X.2008.00231.x PMID: 18315817
77. Mah JL, Christensen-Dalsgaard KK, Leys SP (2014) Choanoflagellate and choanocyte collar-flagellar systems and the assumption of homology. Evol Dev 16: 25-37. doi: 10.1111/ede.12060 PMID: 24393465
78. Birney E, Andrews D, Bevan P, Caccamo M, Cameron G, et al. (2004) Ensembl 2004. Nucleic Acids Res 32: D468-470. PMID: 14681459
79. Birney E, Andrews TD, Bevan P, Caccamo M, Chen Y, et al. (2004) An overview of Ensembl. Genome Res 14: 925-928. PMID: 15078858
80. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755. PMID: 11524383
81. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. PMID: 12912839
82. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61: 539-542. doi: 10.1093/sysbio/sys029 PMID: 22357727
83. Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18: 691-699. PMID: 11319253
84. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8: 275-282. PMID: 1633570
85. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739. doi: 10.1093/molbev/msr121 PMID: 21546353
86. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729. doi: 10.1093/molbev/mst197 PMID: 24132122