CryomiRs: Towards the identification of a cold-associated family of microRNAs

Comparative Biochemistry and Physiology - Part D: Genomics and Proteomics

Volumn 8, Issue 4, 2013, Pages 358-364

  Lyons, Pierre J ^a   Lang Ouellette, Daneck ^a   Morin, Pier Jr ^a  

^a UNIVERSITÉ DE MONCTON   (Canada)

Author keywords

Cold hardiness; Hibernation; Hypometabolism; microRNAs

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; COLD MODULATED MICRORNA; DICER; EXPORTIN 5; MICRORNA; MICRORNA 1; MICRORNA 107; MICRORNA 122; MICRORNA 124; MICRORNA 182; MICRORNA 200; MICRORNA 21; MICRORNA 24; MICRORNA 29A; MICRORNA 29B; MICRORNA 375; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RIBONUCLEASE III; SIRTUIN 6; UNCLASSIFIED DRUG;

ADENYLATION; AMINO ACID METABOLISM; ARTICLE; BIOGENESIS; CELL CYCLE REGULATION; COLD ACCLIMATIZATION; COLD TOLERANCE; CORE TEMPERATURE; DOWN REGULATION; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; FATTY ACID METABOLISM; FATTY ACID SYNTHESIS; GENE EXPRESSION REGULATION; GENE REPRESSION; GLUCONEOGENESIS; GLUCOSE METABOLISM; GLYCOLYSIS; HIBERNATION; HUMAN; INSULIN RELEASE; LONG TERM SURVIVAL; LOW TEMPERATURE; METABOLIC INHIBITION; MOLECULAR WEIGHT; NONHUMAN; OVERWINTERING; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RESTING METABOLIC RATE; RNA CLEAVAGE; RNA DEGRADATION; RNA TRANSLATION; SIGNAL TRANSDUCTION; SUMOYLATION; TRANSLATION INITIATION; UPREGULATION;

HEXAPODA; MAMMALIA;

ACC; ACETYL-COA CARBOXYLASE; CARNITINE PALMITOYLTRANSFERASE 1A; COLD HARDINESS; CPT1A; DGCR8; DIGEORGE SYNDROME CRITICAL REGION GENE 8; EBP-Α; ENHANCER-BINDING PROTEIN-Α; FABP4; FASN; FATTY ACID BINDING PROTEIN 4; FATTY ACID SYNTHASE; HEAT SHOCK PROTEINS; HIBERNATION; HIF-1Α; HSP; HYPOMETABOLISM; HYPOXIA INDUCIBLE TRANSCRIPTION FACTOR-1Α; LIVER X RECEPTOR Α; LXRΑ; MCT1; MICRORNAS; MIRISC; MIRNA-INDUCED SILENCING COMPLEX; MONOCARBOXYLATE TRANSPORTER 1; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA; PPARΓ; REVERSIBLE PROTEIN PHOSPHORYLATION; RPP; SARCO/ENDOPLASMIC RETICULUM CA(2+)-ATPASE; SERCA; SIRT6; SIRTUIN 6;

ACCLIMATIZATION; ANIMALS; COLD TEMPERATURE; FATTY ACIDS; FREEZING; GENE EXPRESSION REGULATION; HIBERNATION; INSECTS; MICRORNAS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84887055610     PISSN: 1744117X     EISSN: 18780407     Source Type: Journal    
DOI: 10.1016/j.cbd.2013.10.001     Document Type: Review

References (87)

1. K. Abnous, C.A. Dieni, and K.B. Storey Regulation of Akt during hibernation in Richardson's ground squirrels Biochim. Biophys. Acta 1780 2008 185 193 (Pubitemid 351162895)
2. A. Ansart, and P. Vernon Cold hardiness in molluscs Acta Oecol. 24 2003 95 102 (Pubitemid 36599538)
3. J.S. Bale Insects and low temperatures: from molecular biology to distributions and abundance Philos. Trans. R. Soc. Lond. B 357 2002 849 862 (Pubitemid 34829651)
4. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
5. E. Basyuk, F. Suavet, A. Doglio, R. Bordonne, and E. Bertrand Human let-7 stem-loop precursors harbor features of RNase III cleavage products Nucleic Acids Res. 31 2003 6593 6597 (Pubitemid 37508765)
6. K.K. Biggar, A. Dubuc, and K. Storey MicroRNA regulation below zero: differential expression of miRNA-21 and miRNA-16 during freezing in wood frogs Cryobiology 59 2009 317 321
7. K.K. Biggar, S.F. Kornfeld, Y. Maistrovski, and K.B. Storey MicroRNA regulation in extreme environments: differential expression of microRNAs in the intertidal snail Littorina littorea during extended periods of freezing and anoxia Genomics Proteomics Bioinformatics 10 2012 302 309
8. K.M. Brauch, N.D. Dhruv, E.A. Hanse, and M.T. Andrews Digital transcriptome analysis indicates adaptive mechanisms in the heart of a hibernating mammal Physiol. Genomics 23 2005 227 234 (Pubitemid 44437981)
9. R.W. Carthew, and E.J. Sontheimer Origins and mechanisms of miRNAs and siRNAs Cell 136 2009 642 655
10. T.P. Chendrimada, K.J. Finn, X. Ji, D. Baillat, R.I. Gregory, S.A. Liebhaber, A.E. Pasquinelli, and R. Shiekhattar microRNA silencing through RISC recruitment of eIF6 Nature 447 2007 823 828 (Pubitemid 46920131)
11. L.A. Courteau, K.B. Storey, and P. Morin Jr. Differential expression of microRNA species in a freeze tolerant insect, Eurosta solidaginis Cryobiology 65 2012 210 214
12. A. Davalos, L. Goedeke, P. Smibert, C.M. Ramirez, N.P. Warrier, U. Andreo, D. Cirera-Salinas, K. Rayner, U. Suresh, J.C. Pastor-Pareja, E. Esplugues, E.A. Fisher, L.O. Penalva, K.J. Moore, Y. Suarez, E.C. Lai, and C. Fernandez-Hernando miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling Proc. Natl. Acad. Sci. U. S. A. 108 2011 9232 9237
13. D.L. Denlinger Regulation of diapause Annu. Rev. Entomol. 47 2002 93 122 (Pubitemid 34108577)
14. J.G. Duman, V. Bennett, T. Sformo, R. Hochstrasser, and B.M. Barnes Antifreeze proteins in Alaskan insects and spiders J. Insect Physiol. 50 2004 259 266 (Pubitemid 38484720)
15. S.F. Eddy, and K.B. Storey Differential expression of Akt, PPAR, and PGC-1 during hibernation in bats Biochem. Cell Biol. 81 2003 269 274 (Pubitemid 37475769)
16. J.L. Esguerra, C. Bolmeson, C.M. Cilio, and L. Eliasson Differential glucose-regulation of microRNAs in pancreatic islets of non-obese type 2 diabetes model Goto-Kakizaki rat PLoS One 6 2011 e18613
17. W. Filipowicz, S.N. Bhattacharyya, and N. Sonenberg Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9 2008 102 114
18. K.U. Frerichs, C.B. Smith, M. Brenner, D.J. DeGracia, G.S. Krause, L. Marrone, T.E. Dever, and J.M. Hallenbeck Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation Proc. Natl. Acad. Sci. U. S. A. 95 1998 14511 14516 (Pubitemid 28549398)
19. R.C. Friedman, K.K. Farh, C.B. Burge, and D.P. Bartel Most mammalian mRNAs are conserved targets of microRNAs Genome Res. 19 2009 92 105
20. F. Geiser Metabolic rate and body temperature reduction during hibernation and daily torpor Annu. Rev. Physiol. 66 2004 239 274 (Pubitemid 40614445)
21. F. Geiser Hibernation Curr. Biol. 23 2013 188 193
22. I. Gerin, L.A. Clerbaux, O. Haumont, N. Lanthier, A.K. Das, C.F. Burant, I.A. Leclercq, O.A. MacDougald, and G.T. Bommer Expression of miR-33 from an SREBP2 intron inhibits cholesterol export and fatty acid oxidation J. Biol. Chem. 285 2010 33652 33661
23. A.J. Giraldez, Y. Mishima, J. Rihel, R.J. Grocock, S. Van Dongen, K. Inoue, A.J. Enright, and A.F. Schier Zebrafish MiRâ 430 promotes deadenylation and clearance of maternal mRNAs Science 312 2006 75 79
24. R.I. Gregory, K.P. Yan, G. Amuthan, T. Chendrimada, B. Doratotaj, N. Cooch, and R. Shiekhattar The microprocessor complex mediates the genesis of microRNAs Nature 432 2004 235 240 (Pubitemid 39545855)
25. A. Grimson, K.K. Farh, W.K. Johnston, P. Garrett-Engele, L.P. Lim, and D.P. Bartel MicroRNA targeting specificity in mammals: determinants beyond seed pairing Mol. Cell 27 2007 91 105 (Pubitemid 46991392)
26. M. Guppy, and P. Withers Metabolic depression in animals: physiological perspectives and biochemical generalizations Biol. Rev. Camb. Philos. Soc. 74 1999 1 40 (Pubitemid 29215911)
27. Y. Hayakawa Activation mechanism of insect fat body phosphorylase by cold phosphorylase kinase, phosphatase and ATP level Insect Biochem. 15 1985 123 128
28. D.T. Humphreys, B.J. Westman, D.I. Martin, and T. Preiss MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function Proc. Natl. Acad. Sci. U. S. A. 102 2005 16961 16966 (Pubitemid 41692666)
29. D. Iliopoulos, K. Drosatos, Y. Hiyama, I.J. Goldberg, and V.I. Zannis MicroRNA-370 controls the expression of microRNA-122 and Cpt1alpha and affects lipid metabolism J. Lipid Res. 51 2010 1513 1523
30. T. Kawamata, and Y. Tomari Making RISC Trends Biochem. Sci. 35 2010 368 376
31. T. Kayukawa, B. Chen, S. Hoshizaki, and Y. Ishikawa Upregulation of a desaturase is associated with the enhancement of cold hardiness in the onion maggot, Delia antiqua Insect Biochem. Mol. Biol. 37 2007 1160 1167 (Pubitemid 47488876)
32. B.J. Kemp, E. Allman, L. Immerman, M. Mohnen, M.A. Peters, K. Nehrke, and A.L. Abbott miR-786 regulation of a fatty-acid elongase contributes to rhythmic calcium-wave initiation in C. elegans Curr. Biol. 22 2012 2213 2220
33. S.F. Kornfeld, K.K. Biggar, and K.B. Storey Differential expression of mature microRNAs involved in muscle maintenance of hibernating little brown bats, Myotis lucifugus: a model of muscle atrophy resistance Genomics Proteomics Bioinformatics 10 2012 295 301
34. A. Krivoruchko, and K.B. Storey Epigenetics in anoxia tolerance: a role for histone deacetylases Mol. Cell. Biochem. 342 2010 151 161
35. J. Krol, I. Loedige, and W. Filipowicz The widespread regulation of microRNA biogenesis, function and decay Nat. Rev. Genet. 11 2010 597 610
36. R.C. Lee, R.L. Feinbaum, and V. Ambros The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14 Cell 75 1993 843 854 (Pubitemid 24014542)
37. Y.J. Lee, S. Miyake, H. Wakita, D.C. McMullen, Y. Azuma, S. Auh, and J.M. Hallenbeck Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells J. Cereb. Blood Flow Metab. 27 2007 950 962 (Pubitemid 46659023)
38. E.K. Lee, M.J. Lee, K. Abdelmohsen, W. Kim, M.M. Kim, S. Srikantan, J.L. Martindale, E.R. Hutchison, H.H. Kim, B.S. Marasa, R. Selimyan, J.M. Egan, S.R. Smith, S.K. Fried, and M. Gorospe miR-130 suppresses adipogenesis by inhibiting peroxisome proliferator-activated receptor gamma expression. Mol Cell Biol. 31 2011 626 638
39. Y.J. Lee, K.R. Johnson, and J.M. Hallenbeck Global protein conjugation by ubiquitin-like-modifiers during ischemic stress is regulated by microRNAs and confers robust tolerance to ischemia PLoS One 7 2012 e47787
40. H.X. Li, Z. Zhang, X. Zhou, Z.Y. Wang, G.L. Wang, and Z.Y. Han Effets of MicroRNA-143 in the differentiation and proliferation of bovine intramuscular preadipocytes Mol. Biol. Rep. 38 2011 4273 4280
41. W.Q. Li, C. Chen, M.D. Xu, J. Guo, Y.M. Li, Q.M. Xia, H.M. Lui, J. He, H.Y. Yu, and L. Zhul The rno-miR-34 family, is upregulated and targets ACSL1 in dimethylnitrosamine-induced hepatic fibrosis in rats FEBS J. 278 2011 1522 1532
42. Y. Liu, W. Hu, H. Wang, M. Lu, C. Shao, C. Menzel, Z. Yan, Y. Li, S. Zhao, P. Khaitovich, M. Liu, W. Chen, B.M. Barnes, and J. Yan Genomic analysis of miRNAs in an extreme mammalian hibernator, the Arctic ground squirrel Physiol. Genomics 42A 2010 39 51
43. X.H. Long, J.H. Mao, A.F. Peng, Y. Zhou, S.H. Huang, and Z.L. Liu Tumor suppressive microRNA-424 inhibits osteosarcoma cell migration and invasion via targeting fatty acid synthase Exp. Ther. Med. 5 2013 1048 1052
44. E. Lund, S. Güttinger, A. Calado, J.E. Dahlberg, and U. Kutay Nuclear export of miRNA precursors Science 303 2004 95 98
45. C.P. Lyman, J.S. Willis, A. Malan, and L.C.H. Wang Hibernation and torpor in mammals and birds 1982 NY Academic Press Inc. New York, NY
46. P.J. Lyons, J.J. Poitras, L.A. Courteau, K.B. Storey, and P. Morin Jr. Identification of differentially regulated micrornas in cold-hardy insects Cryo Letters 34 2013 83 89
47. Y. Maistrovski, K.K. Biggar, and K.B. Storey 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 2012 849 859
48. J.H. Mao, R.P. Zhou, A.F. Peng, Z.L. Liu, S.H. Huang, X.H. Long, and Y. Shu microRNA-195 suppresses osteosarcoma cell invasion and migration in vitro by targeting FASN Oncol. Lett. 4 2012 1125 1129
49. D.C. McMullen, and K.B. Storey Suppression of Na + K + - ATPase activity by reversible phosphorylation over the winter in freeze-tolerant insect J. Insect Physiol. 54 2008 1023 1027
50. D.C. McMullen, C.J. Ramnanan, and K.B. Storey In cold-hardy insects, seasonal, temperature, and reversible phosphorylation controls regulate sarco/endoplasmic reticulum Ca2 + - ATPase (SERCA) Physiol. Biochem. Zool. 83 2010 677 686
51. M.R. Michaud, and D.L. Denlinger Oleic acid is elevated in cell membranes during rapid cold-hardening and pupal diapause in the flesh fly, Sarcophaga crassipalpis J. Insect Physiol. 52 2006 1073 1082 (Pubitemid 44634515)
52. P. Morin Jr., and K.B. Storey Mammalian hibernation: differential gene expression and novel application of epigenetic controls Int. J. Dev. Biol. 53 2009 433 442
53. P. Morin Jr., A. Dubuc, and K.B. Storey Differential expression of microRNA species in organs of hibernating ground squirrels: a role in translational suppression during torpor Biochim. Biophys. Acta 1779 2008 628 633
54. L.G. Nenev, J.G. Duman, M.G. Low, L.C. Sehl, and F.J. Castellino Purification and characterization of an insect hemolymph lipoprotein ice nucleator: evidence for the importance of phosphatidylinositol and apolipoprotein in the ice nucleator activity Cryobiology 27 1989 416 422
55. S. Nottrott, M.J. Simard, and J.D. Richter Human let-7a miRNA blocks protein production on actively translating polyribosomes Nat. Struct. Mol. Biol. 13 2006 1108 1114 (Pubitemid 44885922)
56. P.G. Osborne, B. Gao, and M. Hashimoto Determination in vivo of newly synthesized gene expression in hamsters during phases of the hibernation cycle Jpn. J. Physiol. 54 2004 295 305 (Pubitemid 39539302)
57. Z. Ou, T. Wada, R. Gramignoli, S. Li, S.C. Strom, M. Huang, and W. Xie MicroRNA hsa-miR-613 targets the human LXRα gene and mediates a feedback loop of LXRα autoregulation Mol. Endocrinol. 25 2011 584 596
58. J.H. Park, J. Ahn, S. Kim, D.Y. Kwon, and T.Y. Ha Murine hepatic miRNAs expression and regulation of gene expression in diet-induced obese mice Mol. Cells 31 2011 33 38
59. Y. Peng, H. Xiang, C. Chen, R. Zheng, J. Chai, J. Peng, and S. Jiang MiR-224 impairs adipocyte early differentiation and regulates fatty acid metabolism Int. J. Biochem. Cell Biol. 45 2013 1585 1593
60. C.P. Petersen, M.E. Bordeleau, J. Pelletier, and P.A. Sharp Short RNAs repress translation after initiation in mammalian cells Mol. Cell 21 2006 533 542 (Pubitemid 43228008)
61. R.S. Pillai, S.N. Bhattacharyya, C.G. Artus, T. Zoller, N. Cougot, E. Basyuk, E. Bertrand, and W. Filipowicz Inhibition of translational initiation by letâ 7 microRNA in human cells Science 309 2005 1573 1576 (Pubitemid 41266485)
62. M.N. Poy, L. Eliasson, J. Krutzfeldt, S. Kuwajima, X. Ma, P.E. Macdonald, S. Pfeffer, T. Tuschl, N. Rajewsky, P. Rorsman, and M. Stoffel A pancreatic islet-specific microRNA regulates insulin secretion Nature 432 2004 226 230 (Pubitemid 39545853)
63. T.J. Pullen, G. da Silva Xavier, G. Kelsey, and G.A. Rutter miR-29a and miR-29b contribute to pancreatic β-cell-specific silencing of monocarbolylates transporter 1 (MCT1) Mol. Cell. Biol. 31 2011 3182 3194
64. J.A. Raymond, and A.L. DeVries Adsorption inhibition as a mechanism of freezing resistance in polar fishes Proc. Natl. Acad. Sci. U. S. A. 74 1977 2589 2593 (Pubitemid 8137032)
65. J.A. Reynolds, J. Clark, S.J. Diakoff, and D.L. Denlinger Transcriptional evidence for small RNA regulation of pupal diapause in the flesh fly, Sarcophaga bullata Insect Biochem. Mol. Biol. 43 2013 982 989
66. J.P. Rinehart, R.M. Robich, and D.L. Denlinger Isolation of diapause-regulated genes from the flesh fly, Sarcophaga crassipalpis by suppressive subtractive hybridization J. Insect Physiol. 56 2010 603 609
67. J.P. Rinehart, G.D. Yocum, and R.M. Robich Sugar feeding improves survival of nondiapausing cold-stored Culex pipiens J. Med. Entomol. 49 2012 1347 1354
68. R.M. Robich, J.P. Rinehart, L.J. Kitchen, and D.L. Denlinger Diapause-specific gene expression in the northern house mosquito, Culex pipiens L., identified by suppressive subtractive hybridization J. Insect Physiol. 53 2007 235 245 (Pubitemid 46349109)
69. C. Shao, Y. Liu, H. Ruan, Y. Li, H. Wang, F. Kohl, A.V. Goropashnaya, V.B. Fedorov, R. Zeng, B.M. Barnes, and J. Yan Shotgun proteomics analysis of hibernating arctic ground squirrels Mol. Cell. Proteomics 9 2010 313 326
70. D. Shin, J.Y. Shin, M.T. McManus, L.J. Ptácek, and Y.H. Fu Dicer ablation in oligodendrocytes provokes neuronal impairment in mice Ann. Neurol. 66 2009 843 857
71. E.M. Small, J.R. O'Rourke, V. Moresi, L.B. Sutherland, J. McAnally, R.D. Gerard, J.A. Richardson, and E.N. Olson Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486 Proc. Natl. Acad. Sci. U. S. A. 107 2010 4218 4223
72. L. Sømme, and W. Block Cold hardiness of Collembola at Signy Island, maritime Antarctic Oikos 38 1982 168 176
73. K.B. Storey, and J.M. Storey Freeze tolerance and intolerance as strategies of winter survival in terrestrially-hibernating amphibians Comp. Biochem. Physiol. A Physiol. 83 1986 613 617
74. K.B. Storey, and J.M. Storey Metabolic rate depression in animals: transcriptional and translational controls Biol. Rev. Camb. Philos. Soc. 79 2004 207 233 (Pubitemid 38282052)
75. K.B. Storey, and J.M. Storey Putting life on 'pause' - molecular regulation of hypometabolism J. Exp. Biol. 210 2007 1700 1714 (Pubitemid 46953573)
76. K.B. Storey, and J.M. Storey Molecular biology of freeze tolerance Comp. Physiol. 3 2013 1283 1308
77. M. Trajkovski, J. Hausser, J. Soutschek, B. Bhat, A. Akin, M. Zavolan, M.H. Heim, and M. Stoffel MicroRNAs 103 and 107 regulate insulin sensitivity Nature 474 2011 649 653
78. K.M. Turczyńska, A. Bhattachariya, J. Säll, O. Göransson, K. Swärd, P. Hellstrand, and S. Albinsson Strech-sensitive down-regulation of the miR-144/451 cluster in vascular smooth muscle and its role in AMP-activated protein kinase signaling PLoS One 8 2013 e65135
79. F. van Breukelen, and H.V. Carey Ubiquitin conjugate dynamics in the gut and liver of hibernating ground squirrels J. Comp. Physiol. B. 172 2002 269 273 (Pubitemid 36059321)
80. L.C.H. Wang, and M.W. Wolowyk Torpor in mammals and birds Can. J. Zool. 66 1988 133 137
81. M.R. Worland, and P. Convey The significance of the moult cycle to cold tolerance in the Antarctic collembolan Cryptopygus antarcticus J. Insect Physiol. 54 2008 1281 1285
82. L. Wu, J. Fan, and J.G. Belasco microRNAs direct rapid deadenylation of mRNA Proc. Natl. Acad. Sci. U. S. A. 103 2006 4034 4039
83. J. Yan, B.M. Barnes, F. Kohl, and T.G. Marr Modulation of gene expression in hibernating arctic ground squirrels Physiol. Genomics 32 2008 170 181 (Pubitemid 351186324)
84. C.H. Yu, C.F. Xu, and Y.M. Li Association of microRNA-223 expression with hepatic ischemia/reperfusion injury in mice Dig. Dis. Sci. 54 2009 2362 2366
85. Y. Zeng, and B.R. Cullen Efficient processing of primary microRNA hairpins by Drosha requires flanking nonstructured RNA sequences J. Biol. Chem. 280 2005 27595 27603 (Pubitemid 41076871)
86. Y. Zhang, S.D. Chou, A. Murshid, T.L. Prince, S. Schreiner, M.A. Stevenson, and S.K. Calderwood The role of heat shock factors in stress-induced transcription Methods Mol. Biol. 787 2011 21 32
87. D. Zhong, G. Huang, Y. Zhang, Y. Zeng, Z. Xu, Y. Zhao, X. He, and F. He MicroRNA-1 and microRNA-206 suppress LXRα-induced lipogenesis in hepatocytes Cell. Signal. 25 2013 1429 1437 of Canada