Comparison of brain transcriptome of the greater horseshoe bats (Rhinolophus ferrumequinum) in active and torpid episodes

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Lei, Ming ^a   Dong, Dong ^a   Mu, Shuo ^a   Pan, Yi Hsuan ^a   Zhang, Shuyi ^a  

^a EAST CHINA NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

AESTIVATION; ANIMAL TISSUE; ARTICLE; BAT; BRAIN; CELLULAR STRESS RESPONSE; COMPARATIVE STUDY; CONTROLLED STUDY; GENE IDENTIFICATION; GENE ONTOLOGY; GENE OVEREXPRESSION; GENE REPRESSION; GENE SEQUENCE; HIBERNATION; MALE; NEUROPROTECTION; NEXT GENERATION SEQUENCING; NONHUMAN; OXIDATIVE STRESS; RHINOLOPHUS FERRUMEQUINUM; SEASONAL VARIATION; SUMMER; WINTER DORMANCY; ADAPTATION; ANIMAL; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; PROCEDURES; SEASON; SEQUENCE ANALYSIS;

RHINOLOPHUS FERRUMEQUINUM;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BRAIN; CHIROPTERA; GENE EXPRESSION PROFILING; GENE ONTOLOGY; HIBERNATION; SEASONS; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84907452556     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107746     Document Type: Article

References (66)

1. Geiser F (2013) Hibernation. Curr Biol 23: R188-193.
2. Carey HV, Andrews MT, Martin S.L. (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83: 1153-1181.
3. Storey KB, Storey J.M. (2004) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev Camb Philos Soc 79: 207-233.
4. Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66: 239-274.
5. Frerichs KU, Kennedy C, Sokoloff L., Hallenbeck J.M. (1994) Local cerebral blood flow during hibernation, a model of natural tolerance to "cerebral ischemia". J Cereb Blood Flow Metab 14: 193-205.
6. Frerichs KU, Hallenbeck J.M. (1998) Hibernation in ground squirrels induces state and species-specific tolerance to hypoxia and aglycemia: an in vitro study in hippocampal slices. J Cereb Blood Flow Metab 18: 168-175.
7. Drew KL, Buck CL, Barnes B.M., Christian SL, Rasley BT, et al. (2007) Central nervous system regulation of mammalian hibernation: implications for metabolic suppression and ischemia tolerance. J Neurochem 102: 1713-1726.
8. Pakhotin PI, Pakhotina ID, Belousov A.B. (1993) The study of brain slices from hibernating mammals in vitro and some approaches to the analysis of hibernation problems in vivo. Prog Neurobiol 40: 123-161.
9. Milsom WK, Zimmer MB, Harris M.B. (1999) Regulation of cardiac rhythm in hibernating mammals. Comp Biochem Physiol A Mol Integr Physiol 124: 383-391.
10. Yan J, Burman A, Nichols C., Alila L, Showe LC, et al (2006) Detection of differential gene expression in brown adipose tissue of hibernating arctic ground squirrels with mouse microarrays. Physiol Genomics 25: 346-353.
11. Fedorov VB, Goropashnaya AV, Toien O, Stewart N.C., Chang C., et al. (2011) Modulation of gene expression in heart and liver of hibernating black bears (Ursus americanus). BMC Genomics 12: 171.
12. Fedorov VB, Goropashnaya AV, Toien O, Stewart N.C., Gracey AY, et al. (2009) Elevated expression of protein biosynthesis genes in liver and muscle of hibernating black bears (Ursus americanus). Physiol Genomics 37: 108-118.
13. Dave KR, Christian SL, Perez-Pinzon MA, Drew K.L. (2012) Neuroprotection: lessons from hibernators. Comp Biochem Physiol B Biochem Mol Biol 162: 1-9.
14. Nathaniel TI (2008) Brain-regulated metabolic suppression during hibernation: a neuroprotective mechanism for perinatal hypoxia-ischemia. Int J Stroke 3: 98-104.
15. Drew KL, Rice ME, Kuhn T.B., Smith M.A. (2001) Neuroprotective adaptations in hibernation: therapeutic implications for ischemia-reperfusion, traumatic brain injury and neurodegenerative diseases. Free Radic Biol Med 31: 563-573.
16. Zhou F, Zhu X, Castellani R.J., Stimmelmayr R., Perry G, et al. (2001) Hibernation, a model of neuroprotection. Am J Pathol 158: 2145-2151.
17. Srere HK, Wang LC, Martin S.L. (1992) Central role for differential gene expression in mammalian hibernation. Proc Natl Acad Sci U S A 89: 7119-7123.
18. O'Hara B.F., Watson FL, Srere H.K., Kumar H., Wiler SW, et al. (1999) Gene expression in the brain across the hibernation cycle. J Neurosci 19: 3781-3790.
19. Williams DR, Epperson LE, Li W, Hughes M.A., Taylor R., et al. (2005) Seasonally hibernating phenotype assessed through transcript screening. Physiol Genomics 24: 13-22.
20. Schwartz C, Hampton M, Andrews M.T. (2013) Seasonal and regional differences in gene expression in the brain of a hibernating mammal. PLoS One 8: e58427.
21. Hampton M, Melvin RG, Kendall A.H., Kirkpatrick BR, Peterson N, et al. (2011) Deep sequencing the transcriptome reveals seasonal adaptive mechanisms in a hibernating mammal. PLoS One 6: e27021.
22. Teeling EC, Springer MS, Madsen O, Bates P., O'Brien SJ, et al. (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307: 580-584.
23. Wilkinson GS, South J.M. (2002) Life history, ecology and longevity in bats. Aging Cell 1: 124-131.
24. Jones G, Teeling E.C. (2006) The evolution of echolocation in bats. Trends Ecol Evol 21: 149-156.
25. Ransome R (1990) The natural history of hibernating bats: Helm London, United Kingdom.
26. Geiser F, Stawski C. (2011) Hibernation and torpor in tropical and subtropical bats in relation to energetics, extinctions, and the evolution of endothermy. Integr Comp Biol 51: 337-348.
27. Chen J, Yuan L, Sun M., Zhang L, Zhang S. (2008) Screening of hibernation-related genes in the brain of Rhinolophus ferrumequinum during hibernation. Comp Biochem Physiol B Biochem Mol Biol 149: 388-393.
28. Wang Z, Gerstein M, Snyder M. (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63.
29. Cox MP, Peterson DA, Biggs P.J. (2010) SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11: 485.
30. Grabherr MG, Haas BJ, Yassour M, Levin J.Z., Thompson DA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29: 644-652.
31. Li W, Godzik A. (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
32. Conesa A, Gotz S. (2008) Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008: 619832.
33. Li B, Dewey C.N. (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 323.
34. Robinson MD, McCarthy DJ, Smyth G.K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
35. Huang da W., Sherman BT, Lempicki R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
36. Goldfarb SB, Kashlan OB, Watkins J.N., Suaud L., Yan W, et al. (2006) Differential effects of Hsc70 and Hsp70 on the intracellular trafficking and functional expression of epithelial sodium channels. Proc Natl Acad Sci U S A 103: 5817-5822.
37. Mariman EC, Schepens JT, Wieringa B. (1989) Complete nucleotide sequence of the human creatine kinase B gene. Nucleic Acids Res 17: 6385.
38. Feder ME, Hofmann G.E. (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61: 243-282.
39. Kultz D (2005) Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 67: 225-257.
40. Love S (1999) Oxidative stress in brain ischemia. Brain Pathol 9: 119-131.
41. Teng J, Takei Y, Harada A., Nakata T, Chen J, et al (2001) Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization. J Cell Biol 155: 65-76.
42. Pan YH, Zhang Y, Cui J., Liu Y, McAllan BM, et al (2013) Adaptation of phenylalanine and tyrosine catabolic pathway to hibernation in bats. PloS one 8: e62039.
43. Srivastava RK, Krishna A. (2010) Melatonin modulates glucose homeostasis during winter dormancy in a vespertilionid bat, Scotophilus heathi. Comp Biochem Physiol A Mol Integr Physiol 155: 392-400.
44. Epperson LE, Rose JC, Russell R.L., Nikrad MP, Carey HV, et al. (2010) Seasonal protein changes support rapid energy production in hibernator brainstem. Journal of comparative physiology B, Biochemical, systemic, and environmental physiology 180: 599-617.
45. Frerichs KU, Smith CB, Brenner M, DeGracia D.J., Krause GS, et al. (1998) Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc Natl Acad Sci U S A 95: 14511-14516.
46. Brown IR (2007) Heat shock proteins and protection of the nervous system. Ann N Y Acad Sci 1113: 147-158.
47. Massa SM, Longo FM, Zuo J, Wang S., Chen J, et al. (1995) Cloning of rat grp75, an hsp70-family member, and its expression in normal and ischemic brain. J Neurosci Res 40: 807-819.
48. Xu L, Voloboueva LA, Ouyang Y, Emery J.F., Giffard R.G. (2009) Overexpres-sion of mitochondrial Hsp70/Hsp75 in rat brain protects mitochondria, reduces oxidative stress, and protects from focal ischemia. J Cereb Blood Flow Metab 29: 365-374.
49. Giffard RG, Xu L, Zhao H., Carrico W, Ouyang Y, et al (2004) Chaperones, protein aggregation, and brain protection from hypoxic/ischemic injury. J Exp Biol 207: 3213-3220.
50. Storey KB (1997) Metabolic regulation in mammalian hibernation: enzyme and protein adaptations. Comp Biochem Physiol A Physiol 118: 1115-1124.
51. Eddy SF, McNally JD, Storey K.B. (2005) Up-regulation of a thioredoxin peroxidase-like protein, proliferation-associated gene, in hibernating bats. Arch Biochem Biophys 435: 103-111.
52. Lee K, Park JY, Yoo W, Gwag T., Lee JW, et al. (2008) Overcoming muscle atrophy in a hibernating mammal despite prolonged disuse in dormancy: proteomic and molecular assessment. J Cell Biochem 104: 642-656.
53. Carey HV, Frank CL, Seifert J.P. (2000) Hibernation induces oxidative stress and activation of NK-kappaB in ground squirrel intestine. J Comp Physiol B 170: 551-559.
54. Osborne PG, Hashimoto M. (2006) Brain antioxidant levels in hamsters during hibernation, arousal and cenothermia. Behav Brain Res 168: 208-214.
55. Zhang Y, Pan Y-H, Yin Q, Yang T., Dong D, et al. (2014) Critical roles of mitochondria in brain activities of torpid Myotis ricketti bats revealed by a proteomic approach. Journal of proteomics 105: 266-284.
56. Treiber C, Pipkorn R, Weise C., Holland G, Multhaup G. (2007) Copper is required for prion protein-associated superoxide dismutase-I activity in Pichia pastoris. Febs Journal 274: 1304-1311.
57. Wong BS, Liu T, Li R., Pan T, Petersen RB, et al (2001) Increased levels of oxidative stress markers detected in the brains of mice devoid of prion protein. J Neurochem 76: 565-572.
58. Weissmann C (2004) The state of the prion. Nat Rev Microbiol 2: 861-871.
59. Zomosa-Signoret V., Arnaud JD, Fontes P, Alvarez-Martinez MT, Liautard J.P. (2008) Physiological role of the cellular prion protein. Vet Res 39: 9.
60. Oliver PL, Finelli MJ, Edwards B, Bitoun E., Butts DL, et al. (2011) Oxr1 Is Essential for Protection against Oxidative Stress-Induced Neurodegeneration. PLoS Genet 7.
61. von der Ohe CG, Darian-Smith C, Garner C.C., Heller H.C. (2006) Ubiquitous and temperature-dependent neural plasticity in hibernators. J Neurosci 26: 10590-10598.
62. Andrews MT (2007) Advances in molecular biology of hibernation in mammals. Bioessays 29: 431-440.
63. Millesi E, Prossinger H, Dittami J.P., Fieder M. (2001) Hibernation effects on memory in European ground squirrels (Spermophilus citellus). J Biol Rhythms 16: 264-271.
64. Ruczynski I, Siemers B.M. (2011) Hibernation does not affect memory retention in bats. Biology letters 7: 153-155.
65. Harada A, Teng JL, Takei Y, Oguchi K., Hirokawa N. (2002) MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. Journal of Cell Biology 158: 541-549.
66. Arendt T, Stieler J, Strijkstra A.M., Hut RA, Rudiger J, et al. (2003) Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J Neurosci 23: 6972-6981.