RNA-seq analyses of cellular responses to elevated body temperature in the high Antarctic cryopelagic nototheniid fish Pagothenia borchgrevinki

Marine Genomics

Volumn 18, Issue PB, 2014, Pages 163-171

  Bilyk, Kevin T ^a   Cheng, C H Christina ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

4 C warming; Antarctic notothenioid; Cold specialization; HSP down regulation; RNA seq; Slowing cell cycle

Indexed keywords

NOTOTHENIIDAE; PAGOTHENIA BORCHGREVINKI;

PRIMER DNA;

ADAPTATION; ANIMAL; ANTARCTICA; BODY TEMPERATURE; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETICS; LIVER; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PERCIFORMES; PHYSIOLOGY; SEQUENCE ANALYSIS;

ADAPTATION, BIOLOGICAL; ANIMALS; ANTARCTIC REGIONS; BASE SEQUENCE; BODY TEMPERATURE; DNA PRIMERS; GENE EXPRESSION REGULATION; GENE ONTOLOGY; LIVER; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; PERCIFORMES; SEQUENCE ANALYSIS, RNA;

EID: 84916202482     PISSN: 18747787     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.margen.2014.06.006     Document Type: Article

References (53)

1. Andriashev A.P. Cryopelagic fishes of the Arctic and Antarctic and their significance in polar ecosystems. Antarctic Ecology 1970, Academic Press, London. M.W. Holdgate (Ed.).
2. Benjamini Y., Hochberg Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. Ser. B 1995, 57:289-300.
3. Bilyk K.T., Cheng C.-H.C. Model of gene expression in extreme cold - reference transcriptome for the high-Antarctic cryopelagic notothenioid fish Pagothenia borchgrevinki. BMC Genomics 2013, 14(634).
4. Bilyk K.T., DeVries A.L. Heat tolerance and its plasticity in Antarctic fishes. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2011, 158:382-390.
5. Bond U., Schlesinger M.J. Ubiquitin is a heat-shock protein in chicken-embryo fibroblasts. Mol. Cell. Biol. 1985, 5:949-956.
6. Buckley B.A., Somero G.N. cDNA microarray analysis reveals the capacity of the cold-adapted Antarctic fish Trematomus bernacchii to alter gene expression in response to heat stress. Polar Biol. 2009, 32:403-415.
7. Buckley B.A., Gracey A.Y., Somero G.N. The cellular response to heat stress in the goby Gillichthys mirabilis: a cDNA microarray and protein-level analysis. J. Exp. Biol. 2006, 209:2660-2677.
8. Castedo M., Perfettini J.L., Roumier T., Kroemer G. Cyclin-dependent kinase-1: linking apoptosis to cell cycle and mitotic catastrophe. Cell Death Differ. 2002, 9:1287-1293.
9. Chen Z.Z., Cheng C.H.C., Zhang J.F., Cao L.X., Chen L., Zhou L.H., Jin Y.D., Ye H., Deng C., Dai Z.H., Xu Q.H., Hu P., Sun S.H., Shen Y., Chen L.B. Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:12944-12949.
10. Clark M.S., Fraser K.P.P., Burns G., Peck L.S. The HSP70 heat shock response in the Antarctic fish Harpagifer antarcticus. Polar Biol. 2008, 31:171-180.
11. Coppe A., Agostini C., Marino I.A.M., Zane L., Bargelloni L., Bortoluzzi S., Patarnello T. Genome evolution in the cold: Antarctic icefish muscle transcriptome reveals selective duplications increasing mitochondrial function. Genome Biol. Evol. 2013, 5:45-60.
12. DeVries A.L., Cheng C.-H.C. Antifreeze proteins and organismal freezing avoidance in polar fishes. The Physiology of Polar Fishes 2005, 155-201. Academic Press, San Diego. A.P. Farrell, J.F. Steffensen (Eds.).
13. Eastman J.T. Antarctic Fish Biology: Evolution in a Unique Environment 1993, Academic Press, Inc.
14. Ellgaard L., Molinari M., Helenius A. Setting the standards: quality control in the secretory pathway. Science 1999, 286:1882-1888.
15. Fornace A.J., Alamo I., Hollander M.C., Lamoreaux E. Ubiquitin messenger-RNA is a major stress-induced transcript in mammalian-cells. Nucleic Acids Res. 1989, 17:1215-1230.
16. Franklin C.E., Davison W., Seebacher F. Antarctic fish can compensate for rising temperatures: thermal acclimation of cardiac performance in Pagothenia borchgrevinki. J. Exp. Biol. 2007, 210:3068-3074.
17. Fu X., Fu N., Guo S., Yan Z., Xu Y., Hu H., Menzel C., Chen W., Li Y., Zeng R., Khaitovich P. Estimating accuracy of RNA-Seq and microarrays with proteomics. BMC Genomics 2009, 10.
18. Glickman M.H., Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 2002, 82:373-428.
19. +-ATPase activities. J. Exp. Biol. 1995, 198:2279-2291.
20. Graw J. The crystallins: genes, proteins and diseases. Biol. Chem. 1997, 378:1331-1348.
21. Hartl F.U., Bracher A., Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 2011, 475:324-332.
22. Haschemeyer A.E.V. l-Leucine transport in liver of Antarctic fish in vivo at 0-degrees-c. Am. J. Physiol. 1982, 242:R280-R284.
23. Haschemeyer A.E.V., Mathews R.W. Temperature dependency of protein-synthesis in isolated hepatocytes of Antarctic fish. Physiol. Zool. 1983, 56:78-87.
24. Hofmann G.E., Buckley B.A., Airaksinen S., Keen J.E., Somero G.N. Heat-shock protein expression is absent in the Antarctic fish Trematomus bernacchii (family Nototheniidae). J. Exp. Biol. 2000, 203:2331-2339.
25. Horwitz J. Alpha-crystallin. Exp. Eye Res. 2003, 76:145-153.
26. Huth T.J., Place S.P. De novo assembly and characterization of tissue specific transcriptomes in the emerald notothen, Trematomus bernacchii. BMC Genomics 2013, 14:805.
27. Ihara Y., Cohen-Doyle M.F., Saito Y., Williams D.B. Calnexin discriminates between protein conformational states and functions as a molecular chaperone in vitro. Mol. Cell 1999, 4:331-341.
28. Kiss A.J., Mirarefi A.Y., Ramakrishnan S., Zukoski C.F., DeVries A.L., Cheng C.H.C. Cold-stable eye lens crystallins of the Antarctic nototheniid toothfish Dissostichus mawsoni Norman. J. Exp. Biol. 2004, 207:4633-4649.
29. Kuhl N.M., Rensing L. Heat shock effects on cell cycle progression. Cell. Mol. Life Sci. 2000, 57:450-463.
30. Kültz D. Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 2005, 225-257.
31. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10.
32. Lindquist S. The heat-shock response. Annu. Rev. Biochem. 1986, 55:1151-1191.
33. Liu S.K., Wang X.L., Sun F.Y., Zhang J.R., Feng J.B., Liu H., Rajendran K.V., Sun L.Y., Zhang Y., Jiang Y.L., Peatman E., Kaltenboeck L., Kucuktas H., Liu Z.J. RNA-Seq reveals expression signatures of genes involved in oxygen transport, protein synthesis, folding, and degradation in response to heat stress in catfish. Physiol. Genomics 2013, 45:462-476.
34. Logan C.A., Somero G.N. Effects of thermal acclimation on transcriptional responses to acute heat stress in the eurythermal fish Gillichthys mirabilis (Cooper). Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300:R1373-R1383.
35. Long Y., Song G.L., Yan J.J., He X.Z., Li Q., Cui Z.B. Transcriptomic characterization of cold acclimation in larval zebrafish. BMC Genomics 2013, 14.
36. Michalak M., Corbett E.F., Mesaeli N., Nakamura K., Opas M. Calreticulin: one protein, one gene, many functions. Biochem. J. 1999, 344:281-292.
37. Ovsenek N., Heikkila J.J. Heat shock-induced accumulation of ubiquitin messenger-RNA in Xenopus laevis embryos is developmentally regulated. Dev. Biol. 1988, 129:582-585.
38. Parsell D.A., Lindquist S. The function of heat-shock proteins in stress tolerance - degradation and reactivation of damaged proteins. Annu. Rev. Genet. 1993, 27:437-496.
39. Place S.P., Zippay M.L., Hofmann G.E. Constitutive roles for inducible genes: evidence for the alteration in expression of the inducible HSP70 gene in Antarctic notothenioid fishes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 287:R429-R436.
40. Podrabsky J.E., Somero G.N. Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. J. Exp. Biol. 2004, 207:2237-2254.
41. Podrabsky J.E., Somero G.N. Inducible heat tolerance in Antarctic notothenioid fishes. Polar Biol. 2006, 30:39-43.
42. Rao P.N., Engelber J. HeLa cells - effects of temperature on life cycle. Science 1965, 148:1092-1094.
43. Robinson M.D., McCarthy D.J., Smyth G.K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140.
44. Shin S.C., Kim S.J., Lee J.K., Ahn D.H., Kim M.G., Lee H., Lee J., Kim B.K., Park H. Transcriptomics and comparative analysis of three antarctic notothenioid fishes. PLoS ONE 2012, 7.
45. Smolich B.D., Tarkington S.K., Saha M.S., Grainger R.M. Xenopus gamma-crystallin gene-expression - evidence that the gamma-crystallin gene family is transcribed in lens and nonlens tissues. Mol. Cell. Biol. 1994, 14:1355-1363.
46. Somero G.N., DeVries A.L. Temperature tolerance of some Antarctic fishes. Science 1967, 156:257-258.
47. Tachibana K.-e.K., Gonzalez M.A., Coleman N. Cell-cycle-dependent regulation of DNA replication and its relevance to cancer pathology. J. Pathol. 2005, 205:123-129.
48. Thorne M.A.S., Burns G., Fraser K.P.P., Hillyard G., Clark M.S. Transcription profiling of acute temperature stress in the Antarctic plunderfish Harpagifer antarcticus. Mar. Genomics 2010, 3:35-44.
49. Tye B.K. MCM proteins in DNA replication. Ann. Rev. Biochem. 1999, 68:649-686.
50. Vergauwen L., Benoot D., Blust R., Knapen D. Long-term warm or cold acclimation elicits a specific transcriptional response and affects energy metabolism in zebrafish. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2010, 157:149-157.
51. Wang Z., Gerstein M., Snyder M. RNA-seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 2009, 10:57-63.
52. Young J.C., Agashe V.R., Siegers K., Hartl F.U. Pathways of chaperone-mediated protein folding in the cytosol. Nat. Rev. Mol. Cell Biol. 2004, 5:781-791.
53. Young M.D., Wakefield M.J., Smyth G.K., Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010, 11.