Novel mitochondria-targeted heat-soluble proteins identified in the anhydrobiotic tardigrade improve osmotic tolerance of human cells

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Tanaka, Sae ^a   Tanaka, Junko ^b   Miwa, Yoshihiro ^b   Horikawa, Daiki D ^c   Katayama, Toshiaki ^d   Arakawa, Kazuharu ^c   Toyoda, Atsushi ^e   Kubo, Takeo ^a   Kunieda, Takekazu ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c KEIO UNIVERSITY   (Japan)

^d Database Center for Life Science   (Japan)

^e NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASMIC ABUNDANT HEAT SOLUBLE PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MITOCHONDRIAL ABUNDANT HEAT SOLUBLE PROTEIN; PROTEIN; SECRETORY ABUNDANT HEAT SOLUBLE PROTEIN; UNCLASSIFIED DRUG; MITOCHONDRIAL PROTEIN;

ANHYDROBIOSIS; ANIMAL EXPERIMENT; ARTICLE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MITOCHONDRION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; RAMAZZOTTIUS VARIEORNATUS; SEQUENCE ANALYSIS; TARDIGRADA; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENETICS; HEAT; METABOLISM; MOLECULAR GENETICS; OSMOREGULATION; OSMOTIC PRESSURE; PHYSIOLOGY; PROTEIN MOTIF; PROTEIN TRANSPORT; SOLUBILITY;

RAMAZZOTTIUS; TARDIGRADA;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; HOT TEMPERATURE; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; OSMOREGULATION; OSMOTIC PRESSURE; PROTEIN TRANSPORT; SOLUBILITY; TARDIGRADA;

EID: 84923115967     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118272     Document Type: Article

References (45)

1. Møbjerg N, Halberg KA, Jørgensen A, Persson D, Bjørn M, Ramløv H, et al. (2011) Survival in extreme environments - on the current knowledge of adaptations in tardigrades. Acta physiologica (Oxford, England) 202: 1748-1716.
2. Jönsson KI, Rabbow E, Schill RO, Harms-Ringdahl M, Rettberg P. (2008) Tardigrades survive exposure to space in low Earth orbit. Curr. Biol. 18: R729-R731. doi: 10.1016/j.cub.2008.06.048 PMID: 18786368
3. Persson D, Halberg K A, Jørgensen A, Ricci C, Møbjerg N, Kristensen RM. (2011) Extreme stress tolerance in tardigrades: surviving space conditions in low earth orbit. J. Zoolog. Syst. Evol. Res. 49: 90-97.
4. Clegg JS. (1965) The origin of trehalose and its significance during emergence ofencysted dormant embryos of Artemia salina. Comp. Biochem. Physiol. 14: 135-143. PMID: 14288194
5. Madin KAC, Crowe JH. (1975) Anhydrobiosis in nematodes: carbohydrate and lipid metabolism during dehydration. J. Exp. Zool. 193: 335-342,
6. Watanabe M, Kikawada T, Okuda T. (2003) Increase of internal ion concentration triggers trehalose synthesis associated with cryptobiosis in larvae of Polypedilum vanderplanki. J. Exp. Biol. 206: 2281-2286. PMID: 12771176
7. Tunnacliffe A, Lapinski J, McGee B. (2005) A putative LEA protein, but no trehalose, is present in anhydrobiotic bdelloid rotifers. Hydrobiologia 546: 315-321.
8. Hengherr S, Heyer AG, Kohler H-R, Schill RO. (2008) Trehalose and anhydrobiosis in tardigrades-evidence for divergence in responses to dehydration. FEBS J. 275: 281-288. PMID: 18070104
9. Hand SC, Menze MA, Toner M, Boswell L, Moore D. (2011) LEA proteins during water stress: not just for plants anymore. Annu. Rev. Physiol. 73: 115-134. doi: 10.1146/annurev-physiol-012110-142203 PMID: 21034219
10. Browne JA, Dolan KM, Tyson T, Goyal K, Tunnacliffe A, Burnell AM. (2004) Dehydration-specific induction of hydrophilic protein genes in the anhydrobiotic nematode Aphelenchus avenae. Eukaryot. Cell. 3: 966-975. PMID: 15302829
11. Kikawada T, Nakahara Y, Kanamori Y, Iwata K, Watanabe M, McGee B, et al. (2006) Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochem. Biophys. Res. Commun. 348: 56-61. PMID: 16875677
12. Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA. (2008) The enigmatic LEA proteins and other hydrophilins. Plant Physiol. 148: 6-24. doi: 10.1104/pp.108.120725 PMID: 18772351
13. Tunnacliffe A, Wise MJ. (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften. 94: 791-812. PMID: 17479232
14. Goyal K, Walton LJ, Tunnacliffe A. (2005) LEA proteins prevent protein aggregation due to water stress. Biochem. J. 388: 151-157. PMID: 15631617
15. Pouchkina-Stantcheva NN, McGee BM, Boschetti C, Tolleter D, Chakrabortee S, Popova AV, et al. (2007) Functional divergence of former alleles in an ancient asexual invertebrate. Science 318: 268-271. PMID: 17932297
16. Chakrabortee S, Boschetti C, Walton LJ, Sarkar S, Rubinsztein DC, Tunnacliffe A. (2007) Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function. Proc. Natl. Acad. Sci. U. S. A. 104: 18073-18078. doi: 10.1073/pnas.0706964104 PMID: 17984052
17. Li S, Chakraborty N, Borcar A, Menze MA, Toner M, Hand SC. (2012) Late embryogenesis abundant proteins protect human hepatoma cells during acute desiccation. Proc. Natl. Acad. Sci. U.S.A. 18: 20859-20864.
18. Marunde MR, Samarajeewa DA, Anderson J, Li S, Hand SC, Menze MA. (2013) Improved tolerance to salt and water stress in Drosophila melanogaster cells conferred by late embryogenesis abundant protein. J. Insect Physiol. 59: 377-386. doi: 10.1016/j.jinsphys.2013.01.004 PMID: 23376561
19. Tripathi R, Boschetti C, McGee B, Tunnacliffe A. (2012) Trafficking of bdelloid rotifer late embryogenesis abundant proteins. J. Exp. Biol. 215: 2786-2794. doi: 10.1242/jeb.071647 PMID: 22837450
20. Förster F, Liang C, Shkumatov A, Beisser D, Engelmann JC, Schnölzer M, et al. (2009) Tardigrade workbench: comparing stress-related proteins, sequence-similar and functional protein clusters as well as RNA elements in tardigrades. BMC Genomics 10: 469. doi: 10.1186/1471-2164-10-469 PMID: 19821996
21. Mali B, Grohme MA, Förster F, Dandekar T, Schnölzer M, Reuter D, et al. (2010) Transcriptome survey of the anhydrobiotic tardigrade Milnesium tardigradum in comparison with Hypsibius dujardini and Richtersius coronifer. BMC Genomics 11: 168. doi: 10.1186/1471-2164-11-168 PMID: 20226016
22. Förster F, Beisser D, Grohme MA, Liang C, Mali B, Siegl AM, et al. (2012) Transcriptome analysis in tardigrade species reveals specific molecular pathways for stress adaptations. Bioinform. Biol. Insights 6: 69-96. doi: 10.4137/BBI.S9150 PMID: 22563243
23. Yamaguchi A, Tanaka S, Yamaguchi S, Kuwahara H, Takamura C, Imajoh-Ohmi S, et al. (2012) Two Novel Heat-Soluble Protein Families Abundantly Expressed in an Anhydrobiotic Tardigrade. PLoS ONE 7: e44209. doi: 10.1371/journal.pone.0044209 PMID: 22937162
24. Horikawa DD, Kunieda T, Abe W, Watanabe M, Nakahara Y, Yukuhiro F, et al. (2008) Establishment of a rearing system of the extremotolerant tardigrade Ramazzottius varieornatus: a new model animal for astrobiology. Astrobiology 8: 549-556. doi: 10.1089/ast.2007.0139 PMID: 18554084
25. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, et al. (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35: W585-W587. PMID: 17517783
26. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300: 1005-1016. PMID: 10891285
27. Nielsen H, Engelbrecht J, Brunak S, von Heijne G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10: 1-6. PMID: 9239223
28. Claros MG, Vincens P. (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241: 779-786. PMID: 8944766
29. Pollastri G, McLysaght A. (2005) Porter: a new, accurate server for protein secondary structure prediction. Bioinformatics 21: 1719-1720. PMID: 15585524
30. Kyte J, Doolittle RF. (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157: 105-132. PMID: 7108955
31. Zdobnov EM, Apweiler R. (2001) InterProScan - an integration platform for the signature-recognition methods in InterPro. Bioinformatics 9: 847-848.
32. Bailey TL, Elkan C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc.Int. Conf. Intell. Syst. Mol. Biol. 2: 28-36. PMID: 7584402
33. Tanaka J, Miwa Y, Miyoshi K, Ueno A, Inoue H. (1999) Construction of Epstein-Barr virus-based expression vector containing mini-oriP. Biochem. Biophys. Res. Commun. 264: 938-943. PMID: 10544034
34. Dure L III. (1993) A repeating 11-mer amino acid motif and plant desiccation. Plant J. 3: 363-369. PMID: 8220448
35. Hatanaka R, Hagiwara-Komoda Y, Furuki T, Kanamori Y, Fujita M, Cornette R, et al. (2013) An abundant LEA protein in the anhydrobiotic midge, PvLEA4, acts as a molecular shield by limiting growth of aggregating protein particles. Insect Biochem. Mol. Biol. 43: 1055-1067. doi: 10.1016/j.ibmb.2013.08.004 PMID: 23978448
36. Iturriaga G. (2008) The LEA proteins and trehalose loving couple: a step forward in anhydrobiotic engineering. Biochem. J. 410, e1-2. doi: 10.1042/BJ20071633 PMID: 18254727
37. Sharon MA, Kozarova A, Clegg JS, Vacratsis PO, Warner AH. (2009) Characterization of a group 1 late embryogenesis abundant protein in encysted embryos of the brine shrimp Artemia franciscana. Biochem. Cell Biol. 87, 415-430. doi: 10.1139/o09-001 PMID: 19370059
38. Furuki T, Shimizu T, Chakrabortee S, Yamakawa K, Hatanaka R, Takahashi T, et al. (2012) Effects of Group 3 LEA protein model peptides on desiccation-induced protein aggregation. Biochim. Biophys. Acta. 1824: 891-897. doi: 10.1016/j.bbapap.2012.04.013 PMID: 22579671
39. Furuki T, Sakurai M. (2014) Group 3 LEA protein model peptides protect liposomes during desiccation. Biochim. Biophys. Acta. 1838: 2757-2766. doi: 10.1016/j.bbamem.2014.07.009 PMID: 25037007
40. Kroemer G, Galluzzi L, Brenner C. (2007) Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87: 99-163. PMID: 17237344
41. Pereira Ede J, Panek AD, Eleutherio EC. (2003) Protection against oxidation during dehydration of yeast. Cell Stress Chaperones. 8: 120-124. PMID: 14627197
42. Contreras-Porcia L, Thomas D, Flores V, Correa JA. (2011) Tolerance to oxidative stress induced by desiccation in Porphyra columbina (Bangiales, Rhodophyta). J. Exp. Bot. 62:1815-1829. doi: 10.1093/jxb/erq364 PMID: 21196477
43. Cruz de Carvalho R, Catalá M, Marques da Silva J, Branquinho C, Barreno E. (2012) The impact of dehydration rate on the production and cellular location of reactive oxygen species in an aquatic moss. Ann. Bot. 110: 1007-1016. doi: 10.1093/aob/mcs180 PMID: 22875812
44. Kroemer G, Reed JC. (2000) Mitochondrial control of cell death. Nat. Med. 6: 513-519. PMID: 10802706
45. Danial NN, Korsmeyer SJ. (2004) Cell death: critical control points. Cell. 116: 205-219. PMID: 14744432