Regulation of hypometabolism: Insights into epigenetic controls

Journal of Experimental Biology

Volumn 218, Issue 1, 2015, Pages 150-159

  Storey, Kenneth B ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

Anoxia tolerance; Hibernation; Histone control; Metabolic rate depression; MiRNA; Posttranslational modification; RNA binding proteins

Indexed keywords

ANIMALIA; MAMMALIA; TESTUDINES;

MESSENGER RNA; MICRORNA;

ANIMAL; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; PROTEIN PROCESSING;

ANIMALS; EPIGENESIS, GENETIC; HUMANS; METABOLISM; MICRORNAS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 84926059600     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.106369     Document Type: Review

References (102)

1. Abboud, J. and Storey, K. B. (2013). Novel control of lactate dehydrogenase from the freeze tolerant wood frog: role of posttranslational modifications. Peer J 1, e12.
2. Bar, N. and Dikstein, R. (2010). miR-22 forms a regulatory loop in PTEN/AKT pathway and modulates signaling kinetics. PLoS ONE 5, e10859.
3. Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
4. Baugh, L. R., Demodena, J. and Sternberg, P. W. (2009). RNA Pol II accumulates at promoters of growth genes during developmental arrest. Science 324, 92-94.
5. Biggar, K. K. and Storey, K. B. (2009). Perspectives in cell cycle regulation: lessons from an anoxic vertebrate. Curr. Genomics 10, 573-584.
6. Biggar, K. K. and Storey, K. B. (2011). The emerging roles of microRNAs in the molecular responses of metabolic rate depression. J. Mol. Cell Biol. 3, 167-175.
7. Biggar, K. K. and Storey, K. B. (2012). Evidence for cell cycle suppression and microRNA regulation of cyclin D1 during anoxia exposure in turtles. Cell Cycle 11, 1705-1713.
8. Biggar, Y. and Storey, K. B. (2014). Global DNA modifications suppress transcription in brown adipose tissue during hibernation. Cryobiology 69, 333-338.
9. Biggar, K. K., Dubuc, A. and Storey, K. (2009). MicroRNA regulation below zero: differential expression of miRNA-21 and miRNA-16 during freezing in wood frogs. Cryobiology 59, 317-321.
10. Biggar, K. K., Kornfeld, S. F., Maistrovski, Y. and Storey, K. B. (2012). 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, 302-309.
11. Bocharova, L. S., Ya Gordon R. and Arkhipov, V. I. (1992). Uridine uptake and RNA synthesis in the brain of torpid and awakened ground squirrels. Comp. Biochem. Physiol. 101B, 189-192.
12. Bogdanović, O. and Veenstra, G. J. (2009). DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Chromosoma 118, 549-565.
13. Bommer, G. T., Gerin, I., Feng, Y., Kaczorowski, A. J., Kuick, R., Love, R. E., Zhai, Y., Giordano, T. J., Qin, Z. S., Moore, B. B. et al. (2007). p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr. Biol. 17, 1298-1307.
14. Burggren, W. W. (2014). Epigenetics as a source of variation in comparative animal physiology-or-Lamarck is lookin' pretty good these days. J. Exp. Biol. 217, 682-689.
15. Cannon, B. and Nedergaard, J. (2004). Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359.
16. Chen, M. and Storey, K. B. (2014). Large-scale identification and comparative analysis of miRNA expression profile in the respiratory tree of the sea cucumber Apostichopus japonicus during aestivation. Mar. Genomics 13, 39-44.
17. Chen, M., Zhang, X., Liu, J. and Storey, K. B. (2013). High-throughput sequencing reveals differential expression of miRNAs in intestine from sea cucumber during aestivation. PLoS ONE 8, e76120.
18. Cherkasova, V., Ayyadevara, S., Egilmez, N. and Shmookler Reis, R. (2000). Diverse Caenorhabditis elegans genes that are upregulated in dauer larvae also show elevated transcript levels in long-lived, aged, or starved adults. J. Mol. Biol. 300, 433-448.
19. Dawson, N. J., Bell, R. A. V. and Storey, K. B. (2013). Purification and properties of white muscle lactate dehydrogenase from the anoxia-tolerant turtle, the red-eared slider, Trachemys scripta elegans. Enzyme Res. 2013, 784973.
20. Ebert, M. S. and Sharp, P. A. (2012). Roles for microRNAs in conferring robustness to biological processes. Cell 149, 515-524.
21. Frerichs, K. U., Smith, C. B., Brenner, M., DeGracia, D. J., Krause, G. S., Marrone, L., Dever, T. E. and Hallenbeck, J. M. (1998). Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc. Natl. Acad. Sci. USA 95, 14511-14516.
22. Guan, K.-L. and Xiong, Y. (2011). Regulation of intermediary metabolism by protein acetylation. Trends Biochem. Sci. 36, 108-116.
23. Hanover, J. A., Krause, M. W. and Love, D. C. (2012). Bittersweet memories: linking metabolism to epigenetics through O-GlcNAcylation. Nat. Rev. Mol. Cell Biol. 13, 312-321.
24. Hartley, I., Elkhoury, F. F., Heon Shin, J., Xie, B., Gu, X., Gao, Y., Zhou, D. and Haddad, G. G. (2013). Long-lasting changes in DNA methylation following shortterm hypoxic exposure in primary hippocampal neuronal cultures. PLoS ONE 8, e77859.
25. He, L., He, X., Lim, L. P., de Stanchina, E., Xuan, Z., Liang, Y., Xue, W., Zender, L., Magnus, J., Ridzon, D. et al. (2007). A microRNA component of the p53 tumour suppressor network. Nature 447, 1130-1134.
26. Herbert, C. V. and Jackson, D. C. (1985). Temperature effects on the responses to prolonged submergence in the turtle Chrysemys picta bellii. II. Metabolic rate, blood acid-base and ionic changes, and cardiovascular function in aerated and anoxic water. Physiol. Zool. 58, 670-681.
27. Hindle, A. G., Grabek, K. R., Epperson, L. E., Karimpour-Fard, A. and Martin, S. L. (2014). Metabolic changes associated with the long winter fast dominate the liver proteome in 13-lined ground squirrels. Physiol. Genomics 46, 348-361.
28. Hittel, D. and Storey, K. B. (2002). The translation state of differentially expressed mRNAs in the hibernating 13-lined ground squirrel (Spermophilus tridecemlineatus). Arch. Biochem. Biophys. 401, 244-254.
29. Ho, D. H. and Burggren, W. W. (2012). Parental hypoxic exposure confers offspring hypoxia resistance in zebrafish (Danio rerio). J. Exp. Biol. 215, 4208-4216.
30. Hochachka, P. W., Buck, L. T., Doll, C. J. and Land, S. C. (1996). Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc. Natl. Acad. Sci. USA 93, 9493-9498.
31. Hudson, N. J., Lonhienne, T. G., Franklin, C. E., Harper, G. S. and Lehnert, S. A. (2008). Epigenetic silencers are enriched in dormant desert frog muscle. J. Comp. Physiol. B 178, 729-734.
32. Icardi, L., Mori, R., Gesellchen, V., Eyckerman, S., De Cauwer, L., Verhelst, J., Vercauteren, K., Saelens, X., Meuleman, P., Leroux-Roels, G. et al. (2012). The Sin3a repressor complex is a master regulator of STAT transcriptional activity. Proc. Natl. Acad. Sci. USA 109, 12058-12063.
33. Jackson, D. C. and Ultsch, G. R. (2010). Physiology of hibernation under the ice by turtles and frogs. J. Exp. Zool. A 313, 311-327.
34. Jenuwein, T. and Allis, C. D. (2001). Translating the histone code. Science 293, 1074-1080.
35. Jud, M. C., Czerwinski, M. J., Wood, M. P., Young, R. A., Gallo, C. M., Bickel, J. S., Petty, E. L., Mason, J. M., Little, B. A., Padilla, P. A. et al. (2008). Large P bodylike RNPs form in C. elegans oocytes in response to arrested ovulation, heat shock, osmotic stress, and anoxia and are regulated by the major sperm protein pathway. Dev. Biol. 318, 38-51.
36. Kayes, S. M., Cramp, R. L. and Franklin, C. E. (2009). Metabolic depression during aestivation in Cyclorana alboguttata. Comp. Biochem. Physiol. 154A, 557-563.
37. Kedersha, N. and Anderson, P. (2007). Mammalian stress granules and processing bodies. Methods Enzymol. 431, 61-81.
38. Knight, J. E., Narus, E. N., Martin, S. L., Jacobson, A., Barnes, B. M. and Boyer, B. B. (2000). mRNA stability and polysome loss in hibernating Arctic ground squirrels (Spermophilus parryii). Mol. Cell. Biol. 20, 6374-6379.
39. Kornfeld, S. F., Biggar, K. K. and Storey, K. B. (2012). 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, 295-301.
40. Krivoruchko, A. and Storey, K. B. (2010a). Forever young: mechanisms of anoxia tolerance in turtles and possible links to longevity. Oxid. Med. Cell. Longev. 3, 186-198.
41. Krivoruchko, A. and Storey, K. B. (2010b). Epigenetics in anoxia tolerance: a role for histone deacetylases. Mol. Cell. Biochem. 342, 151-161.
42. Kulkarni, M., Ozgur, S. and Stoecklin, G. (2010). On track with P-bodies. Biochem. Soc. Trans. 38, 242-251.
43. Larade, K. and Storey, K. B. (2002). A profile of the metabolic responses to anoxia in marine invertebrates. In Sensing, Signaling and Cell Adaptation (ed. K. B. Storey and J. M. Storey), pp. 27-46. Amsterdam: Elsevier Science.
44. Lee, Y. J., Miyake, S., Wakita, H., McMullen, D. C., Azuma, Y., Auh, S. and Hallenbeck, J. M. (2007). 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, 950-962.
45. Lee, Y. J., Castri, P., Bembry, J., Maric, D., Auh, S. and Hallenbeck, J. M. (2009). SUMOylation participates in induction of ischemic tolerance. J. Neurochem. 109, 257-267.
46. Lewis, B. A. (2013). O-GlcNAcylation at promoters, nutrient sensors, and transcriptional regulation. Biochim. Biophys. Acta 1829, 1202-1206.
47. Li, Q., Burgess, R. and Zhang, Z. (2012). All roads lead to chromatin: Multiple pathways for histone deposition. Biochim. Biophys. Acta 1819, 238-246.
48. Liu, Y., Hu, W., Wang, H., Lu, M., Shao, C., Menzel, C., Yan, Z., Li, Y., Zhao, S., Khaitovich, P. et al. (2010). Genomic analysis of miRNAs in an extreme mammalian hibernator, the Arctic ground squirrel. Physiol. Genomics 42A, 39-51.
49. Maistrovski, Y., Biggar, K. K. and Storey, K. B. (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.
50. Malatesta, M., Zancanaro, C., Martin, T. E., Chan, E. K. L., Amalric, F., Lührmann, R., Vogel, P. and Fakan, S. (1994). Cytochemical and immunocytochemical characterization of nuclear bodies during hibernation. Eur. J. Cell Biol. 65, 82-93.
51. Malatesta, M., Cardinali, A., Battistelli, S., Zancanaro, C., Martin, T. E., Fakan, S. and Gazzanelli, G. (1999). Nuclear bodies are usual constituents in tissues of hibernating dormice. Anat. Rec. 254, 389-395.
52. Malatesta, M., Luchetti, F., Marcheggiani, F., Fakan, S. and Gazzanelli, G. (2001). Disassembly of nuclear bodies during arousal from hibernation: an in vitro study. Chromosoma 110, 471-477.
53. Malatesta, M., Zancanaro, C., Baldelli, B. and Gazzanelli, G. (2002). Quantitative ultrastructural changes of hepatocyte constituents in euthermic, hibernating and arousing dormice (Muscardinus avellanarius). Tissue Cell 34, 397-405.
54. Malatesta, M., Biggiogera, M., Baldelli, B., Barabino, S. M., Martin, T. E. and Zancanaro, C. (2008). Hibernation as a far-reaching program for the modulation of RNA transcription. Microsc. Res. Tech. 71, 564-572.
55. Malatesta, M., Zancanaro, C. and Biggiogera, M. (2011). Immunoelectron microscopic characterization of nucleolus-associated domains during hibernation. Microsc. Res. Tech. 74, 47-53.
56. Meléndez, A., Tallóczy, Z., Seaman, M., Eskelinen, E. L., Hall, D. H. and Levine, B. (2003). Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301, 1387-1391.
57. Molina-Serrano, D., Schiza, V. and Kirmizis, A. (2013). Cross-talk among epigenetic modifications: lessons from histone arginine methylation. Biochem. Soc. Trans. 41, 751-759.
58. Moore, M. J. (2005). From birth to death: the complex lives of eukaryotic mRNAs. Science 309, 1514-1518.
59. Morin, P., Jr and Storey, K. B. (2006). Evidence for a reduced transcriptional state during hibernation in ground squirrels. Cryobiology 53, 310-318.
60. Morin, P., Jr, Dubuc, A. and Storey, K. B. (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.
61. Osborne, P. G., Gao, B. and 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.
62. Padilla, P. A. and Ladage, M. L. (2012). Suspended animation, diapause and quiescence: arresting the cell cycle in C. elegans. Cell Cycle 11, 1672-1679.
63. Padilla, P. A., Nystul, T. G., Zager, R. A., Johnson, A. C. M. and Roth, M. B. (2002). Dephosphorylation of cell cycle-regulated proteins correlates with anoxiainduced suspended animation in Caenorhabditis elegans. Mol. Biol. Cell 13, 1473-1483.
64. Pile, L. A., Spellman, P. T., Katzenberger, R. J. and Wassarman, D. A. (2003). The SIN3 deacetylase complex represses genes encoding mitochondrial proteins: implications for the regulation of energy metabolism. J. Biol. Chem. 278, 37840-37848.
65. Qureshi, I. A. and Mehler, M. F. (2012). Emerging roles of non-coding RNAs in brain evolution, development, plasticity and disease. Nat. Rev. Neurosci. 13, 528-541.
66. Rolfe, D. F. and Brown, G. C. (1997). Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77, 731-758.
67. Sadoul, K., Boyault, C., Pabion, M. and Khochbin, S. (2008). Regulation of protein turnover by acetyltransferases and deacetylases. Biochimie 90, 306-312.
68. Seibel, B. A., Häfker, N. S., Trübenbach, K., Zhang, J., Tessier, S. N., Pörtner, H. O., Rosa, R. and Storey, K. B. (2014). Metabolic suppression during protracted exposure to hypoxia in the jumbo squid, Dosidicus gigas, living in an oxygen minimum zone. J. Exp. Biol. 217, 2555-2568.
69. Storey, K. B. (2007). Anoxia tolerance in turtles: metabolic regulation and gene expression. Comp. Biochem. Physiol. 147A, 263-276.
70. Storey, K. B. and Storey, J. M. (1990). Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. Q. Rev. Biol. 65, 145-174.
71. Storey, K. B. and Storey, J. M. (2004). Metabolic rate depression in animals: transcriptional and translational controls. Biol. Rev. Camb. Philos. Soc. 79, 207-233.
72. Storey, K. B. and Storey, J. M. (2007). Tribute to P. L. Lutz: putting life on 'pause'-molecular regulation of hypometabolism. J. Exp. Biol. 210, 1700-1714.
73. Storey, K. B. and Storey, J. M. (2010). Metabolic rate depression: the biochemistry of mammalian hibernation. Adv. Clin. Chem. 52, 77-108.
74. Storey, K. B. and Storey, J. M. (2012a). Aestivation: signaling and hypometabolism. J. Exp. Biol. 215, 1425-1433.
75. Storey, K. B. and Storey, J. M. (2012b). Insect cold hardiness: recent advances in metabolic, gene and protein adaptation. Can. J. Zool. 90, 456-475.
76. Storey, K. B. and Storey, J. M. (2013). Molecular biology of freeze tolerance in animals. Comp. Biochem. Physiol. 3A, 1283-1308.
77. Storey, K. B. and Wu, C.-W. (2013). Stress response and adaptation: a new molecular toolkit for the 21st century. Comp. Biochem. Physiol. 165, 417-428.
78. Suswam, E. A., Li, Y. Y., Mahtani, H. and King, P. H. (2005). Novel DNA-binding properties of the RNA-binding protein TIAR. Nucleic Acids Res. 33, 4507-4518.
79. Suzuki, H., Maruyama, R., Yamamoto, E. and Kai, M. (2013). Epigenetic alteration and microRNA dysregulation in cancer. Front. Genet. 4, 258.
80. Tempé, D., Piechaczyk, M. and Bossis, G. (2008). SUMO under stress. Biochem. Soc. Trans. 36, 874-878.
81. Tessier, S. N., Audas, T. E. and Wu, C.-W., Lee, S. and Storey, K. B. (2014). The involvement of mRNA processing factors TIA-1, TIAR, and PABP-1 during mammalian hibernation. Cell Stress Chaperones 19, 813-825.
82. Tsuchida, A., Ohno, S., Wu, W., Borjigin, N., Fujita, K., Aoki, T., Ueda, S., Takanashi, M. and Kuroda, M. (2011). miR-92 is a key oncogenic component of the miR-17-92 cluster in colon cancer. Cancer Sci. 102, 2264-2271.
83. van Breukelen, F. and Martin, S. L. (2002). Reversible depression of transcription during hibernation. J. Comp. Physiol. B 172, 355-361.
84. van Breukelen, F., Maier, R. and Hand, S. C. (2000). Depression of nuclear transcription and extension of mRNA half-life under anoxia in Artemia franciscana embryos. J. Exp. Biol. 203, 1123-1130.
85. Ventura, M., Mateo, F., Serratosa, J., Salaet, I., Carujo, S., Bachs, O. and Pujol, M. J. (2010). Nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase is regulated by acetylation. Int. J. Biochem. Cell Biol. 42, 1672-1680.
86. Waddington, C. H. (1942). The epigenotype. Endeavor 1, 18-20.
87. Wade, P. A. (2001). Methyl CpG-binding proteins and transcriptional repression. BioEssays 23, 1131-1137.
88. Webster, B. R., Scott, I., Traba, J., Han, K. and Sack, M. N. (2014). Regulation of autophagy and mitophagy by nutrient availability and acetylation. Biochim. Biophys. Acta 1841, 525-534.
89. Whitten, B. K., Schrader, L. E., Huston, R. L. and Honold, G. R. (1970). Hepatic polyribosomes and protein synthesis: seasonal changes in a hibernator. Int. J. Biochem. 1, 406-408.
90. Wolffe, A. P. and Matzke, M. A. (1999). Epigenetics: regulation through repression. Science 286, 481-486.
91. Wu, C.-W., Biggar, K. K. and Storey, K. B. (2013). Dehydration mediated microRNA response in the African clawed frog Xenopus laevis. Gene 529, 269-275.
92. Xiong, Y. and Guan, K.-L. (2012). Mechanistic insights into the regulation of metabolic enzymes by acetylation. J. Cell Biol. 198, 155-164.
93. Xiong, Z. J. and Storey, K. B. (2012). Regulation of liver lactate dehydrogenase by reversible phosphorylation in response to anoxia in a freshwater turtle. Comp. Biochem. Physiol. 163B, 221-228.
94. Xu, Y., Li, L., Xiang, X., Wang, H., Cai, W., Xie, J., Han, Y., Bao, S. and Xie, Q. (2013). Three common functional polymorphisms in microRNA encoding genes in the susceptibility to hepatocellular carcinoma: a systematic review and metaanalysis. Gene 527, 584-593.
95. Yang, X. J. (2005). Multisite protein modification and intramolecular signaling. Oncogene 24, 1653-1662.
96. Yang, H. S., Zhou, Y., Zhang, T., Yuan, X. T., Li, X., Liu, Y. and Zhang, F. (2006). Metabolic characteristics of sea cucumber Apostichopus japonicus (Selenka) during aestivation. J. Exp. Mar. Biol. Ecol. 330, 505-510.
97. Zhang, J. and Storey, K. B. (2013). Akt signaling and freezing survival in the wood frog, Rana sylvatica. Biochim. Biophys. Acta 1830, 4828-4837.
98. Zhang, J., Tessier, S. N. and Storey, K. B. (2011). PI3K-Akt regulation as a molecular mechanism of the stress response during aerobic dormancy. In Hypometabolism: Strategies of Survival in Vertebrates and Invertebrates (ed. A. Nowakowska and M. Caputa), pp. 147-182. Kerala: Research Signpost.
99. Zhang, T., Wang, S., Lin, Y., Xu, W., Ye, D., Xiong, Y., Zhao, S. and Guan, K.-L. (2012). Acetylation negatively regulates glycogen phosphorylase by recruiting protein phosphatase 1. Cell Metab. 15, 75-87.
100. Zhang, J., Biggar, K. K. and Storey, K. B. (2013). Regulation of p53 by reversible post-transcriptional and post-translational mechanisms in liver and skeletal muscle of an anoxia tolerant turtle, Trachemys scripta elegans. Gene 513, 147-155.
101. Zhao, S., Xu, W., Jiang, W., Yu, W., Lin, Y., Zhang, T., Yao, J., Zhou, L., Zeng, Y., Li, H. et al. (2010). Regulation of cellular metabolism by protein lysine acetylation. Science 327, 1000-1004.
102. Zhou, Z. S., Rasmann, S., Li, M., Guo, J. Y., Chen, H. S. and Wan, F. H. (2013). Cold temperatures increase cold hardiness in the next generation Ophraella communa beetles. PLoS ONE 8, e74760.