Skip to main content
Log in

Differential expression and emerging functions of non-coding RNAs in cold adaptation

  • Review
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Several species undergo substantial physiological and biochemical changes to confront the harsh conditions associated with winter. Small mammalian hibernators and cold-hardy insects are examples of natural models of cold adaptation that have been amply explored. While the molecular picture associated with cold adaptation has started to become clearer in recent years, notably through the use of high-throughput experimental approaches, the underlying cold-associated functions attributed to several non-coding RNAs, including microRNAs (miRNAs) and long non-coding RNAs (lncRNAs), remain to be better characterized. Nevertheless, key pioneering work has provided clues on the likely relevance of these molecules in cold adaptation. With an emphasis on mammalian hibernation and insect cold hardiness, this work first reviews various molecular changes documented so far in these processes. The cascades leading to miRNA and lncRNA production as well as the mechanisms of action of these non-coding RNAs are subsequently described. Finally, we present examples of differentially expressed non-coding RNAs in models of cold adaptation and elaborate on the potential significance of this modulation with respect to low-temperature adaptation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alvarado S, Mak T, Liu S, Storey KB, Szyf M (2015) Dynamic changes in global and gene-specific DNA methylation during hibernation in adult thirteen-lined ground squirrels, Ictidomys tridecemlineatus. J Exp Biol 218:1787–1795

    Article  PubMed  Google Scholar 

  • Andrews MT (2004) Genes controlling the metabolic switch in hibernating mammals. Biochem Soc Trans 32:1021–1024

    Article  CAS  PubMed  Google Scholar 

  • Aravin AA, Sachidanandam R, Bourc’his D, Schaefer C, Pezic D, Toth KF, Bestor T, Hannon GJ (2008) A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31:785–799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashwal-Fluss R, Meyer M, Pamudurti NR, Ivanov A, Bartok O, Hanan M, Evantal N, Memczak S, Rajewsky N, Kadener S (2014) circRNA biogenesis competes with pre-mRNA splicing. Mol Cell 56:55–66

    Article  CAS  PubMed  Google Scholar 

  • Bale JS (2002) Insects and low temperatures: from molecular biology to distributions and abundance. Philos Trans R Soc B 357:849–861

    Article  CAS  Google Scholar 

  • Bale JS, Hayward SA (2010) Insect overwintering in a changing climate. J Exp Biol 213:980–994

    Article  CAS  PubMed  Google Scholar 

  • Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basu K, Wasserman SS, Jeronimo PS, Graham LA, Davies PL (2016) Intermediate activity of midge antifreeze protein is due to a tyrosine-rich ice-binding site and atypical ice plane affinity. FEBS J 283:1504–1515

    Article  CAS  PubMed  Google Scholar 

  • Bell RA, Storey KB (2010) Regulation of liver glutamate dehydrogenase by reversible phosphorylation in a hibernating mammal. Comp Biochem Physiol B: Biochem Mol Biol 157:310–316

    Article  Google Scholar 

  • Bianchessi V, Badi I, Bertolotti M, Nigro P, D’Alessandra Y, Capogrossi MC, Zanobini M, Pompilio G, Raucci A, Lauri A (2015) The mitochondrial lncRNA ASncmtRNA-2 is induced in aging and replicative senescence in Endothelial Cells. J Mol Cell Cardiol 81:62–70

    Article  CAS  PubMed  Google Scholar 

  • Biggar Y, Storey KB (2014a) Global DNA modifications suppress transcription in brown adipose tissue during hibernation. Cryobiology 69:333–338

    Article  CAS  PubMed  Google Scholar 

  • Biggar KK, Storey KB (2014b) Identification and expression of microRNA in the brain of hibernating bats, Myotis lucifugus. Gene 544:67–74

    Article  CAS  PubMed  Google Scholar 

  • Biggar KK, Storey KB (2015a) Insight into post-transcriptional gene regulation:stress-responsive microRNAs and their role in the environmental stress survival of tolerant animals. J Exp Biol 218:1281–1289

    Article  PubMed  Google Scholar 

  • Biggar KK, Storey KB (2015b) Low-temperature microRNA expression in the painted turtle, Chrysemys picta during freezing stress. FEBS Lett 589:3665–3670

    Article  CAS  PubMed  Google Scholar 

  • Biggar KK, Kornfeld SF, Maistrovski Y, Storey KB (2012) MicroRNA regulation in extreme environments: differential expression of microRNAs in the intertidal snail Littorina littorea during extended periods of freezing and anoxia. Genom Proteom Bioinform 10:302–309

    Article  CAS  Google Scholar 

  • Braun JE, Huntzinger E, Fauser M, Izaurralde E (2011) GW182 proteins directly recruit cytoplasmic deadenylase complexes to miRNA targets. Mol Cell 44:120–133

    Article  CAS  PubMed  Google Scholar 

  • Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25:1915–1927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai X, Cullen BR (2007) The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 13:313–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai H, Xue Y, Wang P, Wang Z, Li Z, Hu Y, Li Z, Shang X, Liu Y (2015) The long noncoding RNA TUG1 regulates blood-tumor barrier permeability by targeting miR-144. Oncotarget 6:19759–19779

    Article  PubMed  PubMed Central  Google Scholar 

  • Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181

    Article  CAS  PubMed  Google Scholar 

  • Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147:358–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chekulaeva M, Mathys H, Zipprich JT, Attig J, Colic M, Parker R, Filipowicz W (2011) miRNA repression involves GW182-mediated recruitment of CCR4–NOT through conserved W-containing motifs. Nat Struct Mol Biol 18:1218–1226

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Boland A, Kuzuoğlu-Öztürk D, Bawankar P, Loh B, Chang CT, Weichenrieder O, Izaurralde E (2014) A DDX6-CNOT1 complex and W-binding pockets in CNOT9 reveal direct links between miRNA target recognition and silencing. Mol Cell 54:737–750

    Article  CAS  PubMed  Google Scholar 

  • Chendrimada TP, Gregory RI, Kumaraswamy E, Norman J, Cooch N, Nishikura K, Shiekhattar R (2005) TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436:740–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark MS, Worland MR (2008) How insects survive the cold: molecular mechanisms-a review. J Comp Physiol B 178:917–933

    Article  CAS  PubMed  Google Scholar 

  • Courteau LA, Storey KB, Morin P Jr (2012) Differential expression of microRNA species in a freeze tolerant insect, Eurosta solidaginis. Cryobiology 65:210–214

    Article  CAS  PubMed  Google Scholar 

  • Danks HV (2005) Key themes in the study of seasonal adaptations in insects I. Patterns of cold hardiness. Appl Entomol Zool 40:199–211

    Article  Google Scholar 

  • Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Physiology: hibernation in a tropical primate. Nature 429:825–826

    Article  CAS  PubMed  Google Scholar 

  • Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigo R (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22:1775–1789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dimitrova N, Zamudio JR, Jong RM, Soukup D, Resnick R, Sarma K, Ward AJ, Raj A, Lee JT, Sharp PA, Jacks T (2014) LincRNA-p21 Activates p21 In cis to Promote Polycomb Target Gene Expression and to Enforce the G1/S Checkpoint. Mol Cell 54:777–790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding XC, Großhans H (2009) Repression of C. elegans microRNA targets at the initiation level of translation requires GW182 proteins. EMBO J 28:213–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duman JG, Morris JP, Castellino FJ (1984) Purification and composition of an ice nucleating protein from queens of the hornet, Vespula maculata. J Comp Physiol B 154:79–83

    Article  CAS  Google Scholar 

  • Duman JG, Bennett T, Sformo T, Hochstrasser R, Barnes BM (2004) Antifreeze proteins in Alaskan insects and spiders. J Insect Physiol 50:259–266

    Article  CAS  PubMed  Google Scholar 

  • Frerichs KU, Smith CB, Brenner M, DeGracia DJ, Krause GS, Marrone L, Dever TE, Hallenbeck JM (1998) Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc Natl Acad Sci USA 95:14511–14516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frigault JJ, Lang-Ouellette D, Morin P Jr (2016) Up-regulation of long non-coding RNA TUG1 in hibernating thirteen-lined ground squirrels. Genom Proteom Bioinform 14:113–118

    Article  Google Scholar 

  • Fu A, Jacobs DI, Zhu Y (2014) Epigenome-wide analysis of piRNAs in gene-specific DNA methylation. RNA Biol 11:1301–1312

    Article  PubMed  Google Scholar 

  • Fukao A, Mishima Y, Takizawa N, Oka S, Imataka H, Pelletier J, Sonenberg N, Thoma C, Fujiwara T (2014) MicroRNAs trigger dissociation of eIF4AI and eIF4AII from target mRNAs in humans. Mol Cell 56:79–89

    Article  CAS  PubMed  Google Scholar 

  • Gardini A, Shiekhattar R (2015) The many faces of long noncoding RNAs. FEBS J 282:1647–1657

    Article  CAS  PubMed  Google Scholar 

  • Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274

    Article  CAS  PubMed  Google Scholar 

  • Grabek KR, Diniz Behn C, Barsh GS, Hesselberth JR, Martin SL (2015) Enhanced stability and polyadenylation of select mRNAs support rapid thermogenesis in the brown fat of a hibernator. Elife 27:4

    Google Scholar 

  • Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R (2004) The Microprocessor complex médiates the genesis of microRNAs. Nature 432:235–240

    Article  CAS  PubMed  Google Scholar 

  • Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, Cabili MN, Jaenisch R, Mikkelsen TS, Jacks T, Hacohen N, Bernstein BE, Kellis M, Regev A, Rinn JL, Lander ES (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458:223–227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hadj-Moussa H, Moggridge JA, Luu BE, Quintero-Galvis JF, Gaitán-Espitia JD, Nespolo RF, Storey KB (2016) The hibernating South American marsupial, Dromiciops gliroides, displays torpor-sensitive microRNA expression patterns. Sci Rep 6:24627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hampton M, Melvin RG, Kendall AH, Kirkpatrick BR, Peterson N, Andrews MT (2011) Deep sequencing the transcriptome reveals seasonal adaptive mechanisms in a hibernating mammal. PLoS ONE 6:e27021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hampton M, Melvin RG, Andrews MT (2013) Transcriptomic analysis of brown adipose tissue across the physiological extremes of natural hibernation. PLoS ONE 8:e85157

    Article  PubMed  PubMed Central  Google Scholar 

  • Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495:384–388

    Article  CAS  PubMed  Google Scholar 

  • Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and daily torpor in mammals. Respir Physiol Neurobiol 141:317–329

    Article  PubMed  Google Scholar 

  • Hendrickson DG, Hogan DJ, McCullough HL, Myers JW, Herschlag D, Ferrell JE, Brown PO (2009) Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA. PLoS Biol 7:e1000238

    Article  PubMed  PubMed Central  Google Scholar 

  • Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, Marzluff WF, Sharpless NE (2013) Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19:141–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  CAS  PubMed  Google Scholar 

  • Kornfeld SF, Biggar KK, Storey KB (2012) Differential expression of mature microRNAs involved in muscle maintenance of hibernating little brown bats, Myotis lucifugus: a model of muscle atrophy resistance. Genom Proteom Bioinform 10:295–301

    Article  CAS  Google Scholar 

  • Krol J, Loedige I, Filipowicz W (2010) The widespread regulation of microRNA biogenesis, function and decay. Nature Rev Genet 11:597–610

    CAS  PubMed  Google Scholar 

  • Lang-Ouellette D, Morin P Jr (2014) Differential expression of miRNAs with metabolic implications in hibernating thirteen-lined ground squirrels, Ictidomys tridecemlineatus. Mol Cell Biochem 394:291–298

    Article  CAS  PubMed  Google Scholar 

  • Lee RE, Denlinger DL (1991) Insects at low temperature. Chapman and Hall, London

    Book  Google Scholar 

  • Lee YJ, Johnson KR, Hallenbeck JM (2012) Global protein conjugation by ubiquitin-like-modifiers during ischemic stress is regulated by microRNAs and confers robust tolerance to ischemia. PLoS ONE 7:e47787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li P, Ruan X, Yang L, Kiesewetter K, Zhao Y, Luo H, Chen Y, Gucek M, Zhu J, Cao H (2015) A liver-enriched long non-coding RNA, lncLSTR, regulates systemic lipid metabolism in mice. Cell Metab 21:455–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li M, Sun X, Cai H, Sun Y, Plath M, Li C, Lan X, Lei C, Lin F, Bai Y, Chen H (2016) Long non-coding RNA ADNCR suppresses adipogenic differentiation by targeting miR-204. Biochim Biophys Acta 1859:871–882

    Article  CAS  PubMed  Google Scholar 

  • Lin SP, Ye S, Long Y, Fan Y, Mao HF, Chen MT, Ma QJ (2016) Circular RNA expression alterations are involved in OGD/R-induced neuron injury. Biochem Biophys Res Commun 471:52–56

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Hu W, Wang H, Lu M, Shao C, Menzel C, Yan Z, Li Y, Zhao S, Khaitovich P, Liu M, Chen W, Barnes BM, Yan J (2010) Genomic analysis of miRNAs in an extreme mammalian hibernator, the Arctic ground squirrel. Physiol Genom 42A:39–51

    Article  CAS  Google Scholar 

  • Lucas K, Raikhel AS (2013) Insect microRNAs: biogenesis, expression profiling and biological functions. Insect Biochem Mol Biol 43:24–38

    Article  CAS  PubMed  Google Scholar 

  • Lyons PJ, Lang-Ouellette D, Morin P Jr (2013) CryomiRs: towards the identification of a cold-associated family of microRNAs. Comp Biochem Physiol Part D Genom Proteom 8:358–364

    CAS  Google Scholar 

  • Lyons PJ, Crapoulet N, Storey KB, Morin P Jr (2015a) Identification and profiling of miRNAs in the freeze-avoiding gall moth Epiblema scudderiana via next-generation sequencing. Mol Cell Biochem 410:155–163

    Article  CAS  PubMed  Google Scholar 

  • Lyons PJ, Storey KB, Morin P Jr (2015b) Expression of miRNAs in response to freezing and anoxia stresses in the freeze tolerant fly Eurosta solidaginis. Cryobiology 71:97–102

    Article  CAS  PubMed  Google Scholar 

  • MacDonald JA, Storey KB (1999) Regulation of ground squirrel Na + K + -ATPase activity by reversible phosphorylation during hibernation. Biochem Biophys Res Commun 254:424–429

    Article  CAS  PubMed  Google Scholar 

  • Maistrovski Y, Biggar KK, Storey KB (2012) HIF-1α regulation in mammalian hibernators: role of non-coding RNA in HIF-1α control during torpor in ground squirrels and bats. J Comp Physiol B 182:849–859

    Article  CAS  PubMed  Google Scholar 

  • Mathonnet G, Fabian MR, Svitkin YV, Parsyan A, Huck L, Murata T, Biffo S, Merrick WC, Darzynkiewicz E, Pillai RS, Filipowicz W, Duchaine TF, Sonenberg N (2007) MicroRNA inhibition of translation initiation in vitro by targeting the cap-binding complex eIF4F. Science 17:1764–1767

    Article  Google Scholar 

  • McHugh CA, Chen CK, Chow A, Surka CF, Tran C, McDonel P, Pandya-Jones A, Blanco M, Burghard C, Moradian A, Sweredoski MJ, Shishkin AA, Su J, Lander ES, Hess S, Plath K, Guttman M (2015) The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 521:232–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10:155–159

    Article  CAS  PubMed  Google Scholar 

  • Milsom WK, Jackson DC (2011) Hibernation and gas exchange. Compr Physiol 1:397–420

    PubMed  Google Scholar 

  • Morin P Jr, Storey KB (2005) Cloning and expression of hypoxia-inducible factor 1alpha from the hibernating ground squirrel, Spermophilus tridecemlineatus. Biochim Biophys Acta 1729:32–40

    Article  CAS  PubMed  Google Scholar 

  • Morin P Jr, McMullen DC, Storey KB (2005) HIF-1alpha involvement in low temperature and anoxia survival by a freeze tolerant insect. Mol Cell Biochem 280:99–106

    Article  CAS  PubMed  Google Scholar 

  • Morin P Jr, Dubuc A, Storey KB (2008) Differential expression of microRNA species in organs of hibernating ground squirrels: a role in translational suppression during torpor. Biochim Biophys Acta 1779:628–633

    Article  CAS  PubMed  Google Scholar 

  • Mueller AC, Cichewicz MA, Dey BK, Layer R, Reon BJ, Gagan JR, Dutta A (2015) MUNC, a long noncoding RNA that facilitates the function of MyoD in skeletal myogenesis. Mol Cell Biol 35:498–513

    Article  PubMed  Google Scholar 

  • Osborne PG, Gao B, Hashimoto M (2004) Determination in vivo of newly synthesized gene expression in hamsters during phases of the hibernation cycle. Jpn J Physiol 54:295–305

    Article  CAS  PubMed  Google Scholar 

  • Quinn JJ, Chang HY (2016) Unique features of long non-coding RNA biogenesis and function. Nat Rev Genet 17:47–62

    Article  CAS  PubMed  Google Scholar 

  • Raymond JA, DeVries AL (1977) Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc Natl Acad Sci USA 74:2589–2593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rinehart JP, Li A, Yocum GD, Robich RM, Hayward SA, Denlinger DL (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proc Natl Acad Sci USA 104:11130–11137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129:1311–1323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rouya C, Siddiqui N, Morita M, Duchaine TF, Fabian MR, Sonenberg N (2014) Human DDX6 effects miRNA-mediated gene silencing via direct binding to CNOT1. RNA 20:1398–1409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sleutels F, Zwart R, Barlow DP (2002) The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415:810–813

    Article  CAS  PubMed  Google Scholar 

  • Smolle E, Haybaeck J (2014) Non-coding RNAs and lipid metabolism. Int J Mol Sci 15:13494–13513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Storey KB, Storey JM (2004) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev Camb Philos Soc 79:207–233

    Article  PubMed  Google Scholar 

  • Storey KB, Storey JM (2010) Metabolic rate depression: the biochemistry of mammalian hibernation. Adv Clin Chem 52:77–108

    Article  CAS  PubMed  Google Scholar 

  • Su S, Liu J, He K, Zhang M, Feng C, Peng F, Li B, Xia X (2016) Overexpression of the long noncoding RNA TUG1 protects against cold-induced injury of mouse livers by inhibiting apoptosis and inflammation. FEBS J 283:1261–1274

    Article  CAS  PubMed  Google Scholar 

  • Tessier SN, Storey KB (2010) Expression of myocyte enhancer factor-2 and downstream genes in ground squirrel skeletal muscle during hibernation. Mol Cell Biochem 344:151–162

    Article  CAS  PubMed  Google Scholar 

  • Tessier SN, Storey KB (2012) Myocyte enhancer factor-2 and cardiac muscle gene expression during hibernation in thirteen-lined ground squirrels. Gene 501:8–16

    Article  CAS  PubMed  Google Scholar 

  • Wang LCH, Wolowyk MW (1988) Torpor in mammals and birds. Can J Zool 66:133–137

    Article  CAS  Google Scholar 

  • Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie BR, Protacio A, Flynn RA, Gupta RA, Wysocka J, Lei M, Dekker J, Helms JA, Chang HY (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472:120–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen X, Wang S, Duman JG, Arifin JF, Juwita V, Goddard WA 3rd, Rios A, Liu F, Kim SK, Abrol R, DeVries AL, Henling LM (2016) Antifreeze proteins govern the precipitation of trehalose in a freezing-avoiding insect at low temperature. Proc Natl Acad Sci USA 113:6683–6688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu CW, Biggar KK, Storey KB (2014) Expression profiling and structural characterization of microRNAs in adipose tissues of hibernating ground squirrels. Genomics Proteomics Bioinformatics 12:284–291

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu D, Fu H, Zhou H, Su J, Zhang F, Shen J (2015) Effects of Novel ncRNA Molecules, p15-piRNAs, on the Methylation of DNA and Histone H3 of the CDKN2B Promoter Region in U937 Cells. J Cell Biochem 116:2744–2754

    Article  CAS  PubMed  Google Scholar 

  • Wu CW, Biggar KK, Luu BE, Szereszewski KE, Storey KB (2016) Analysis of microRNA expression during the torpor-arousal cycle of a mammalian hibernator, the 13-lined ground squirrel. Physiol Genom 48:388–396

    Article  Google Scholar 

  • Xu Y, Shao C, Fedorov VB, Goropashnaya AV, Barnes BM, Yan J (2013) Molecular signatures of mammalian hibernation: comparisons with alternative phenotypes. BMC Genom 14:567

    Article  Google Scholar 

  • Yuan L, Geiser F, Lin B, Sun H, Chen J, Zhang S (2015) Down but Not Out: the role of MicroRNAs in hibernating bats. PLoS ONE 10:e0135064

    Article  PubMed  PubMed Central  Google Scholar 

  • Zachariassen KE, Hammel HT (1976) Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262:285–287

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Storey JM, Storey KB (2011) Chaperone proteins and winter survival by a freeze tolerant insect. J Insect Physiol 57:1115–1122

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada (RGPIN/402222-2012) awarded to P. J. M.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pier Jr Morin.

Ethics declarations

Conflict of interest

The authors declare no conflict of interests.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Frigault, J.J., Morin, M.D. & Morin, P.J. Differential expression and emerging functions of non-coding RNAs in cold adaptation. J Comp Physiol B 187, 19–28 (2017). https://doi.org/10.1007/s00360-016-1049-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-016-1049-2

Keywords

Navigation