Mammalian hibernation: Differential gene expression and novel application of epigenetic controls

International Journal of Developmental Biology

Volumn 53, Issue 2-3, 2009, Pages 433-442

  Morin Jr , Pier ^a   Storey, Kenneth B ^b  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b CARLETON UNIVERSITY   (Canada)

Author keywords

Epigenetics; Histone modification; Hypometabolism; microRNA

Indexed keywords

DNA; HISTONE DEACETYLASE; HISTONE H3; MESSENGER RNA; MICRORNA; RNA POLYMERASE II; SIRTUIN;

DNA METHYLATION; EPIGENETICS; GENE EXPRESSION REGULATION; HIBERNATION; MAMMAL; NONHUMAN; POLYSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REVIEW; RNA TRANSLATION; SUMOYLATION; TRANSCRIPTION INITIATION; ANIMAL; BASAL METABOLIC RATE; BIOLOGICAL MODEL; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY; PROMOTER REGION; SKELETAL MUSCLE;

MAMMALIA;

ANIMALS; BASAL METABOLISM; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; HIBERNATION; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; PROMOTER REGIONS, GENETIC; TRANSCRIPTION, GENETIC;

EID: 70349322563     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.082643pm     Document Type: Review

References (96)

1. ANDREWS, M.T., SQUIRE, T.L., BOWEN, C.M. and ROLLINS, M.B. (1998). Lowtemperature carbon utilization is regulated by novel gene activity in the heart of a hibernating mammal. Proc. Natl. Acad. Sci. USA 95: 8392-8397.
2. BARTEL, D.P. (2004). MicroRNAs: genomics, biogenesis, mechanism and function. Cell 116: 281-297.
3. BERGER, J. and MOLLER, D.E. (2002). The mechanisms of action of PPARs. Ann. Rev. Med. 53: 409-435.
4. BERRIEL DIAZ, M., LANGE, M., HELDMAIER, G. and KLINGENSPOR, M. (2004). Depression of transcription and translation during daily torpor in the Djungarian hamster (Phodopus sungorus). J. Comp. Physiol. B 174: 495-502.
5. BIGGIOGERA, M. and PELLICCIARI, C. (2000). Heterogeneous ectopic RNPderived structures (HERDS) are markers of transcriptional arrest. FASEB J. 14: 828-834.
6. BOCHAROVA, L.S., GORDON, R. and ARKHIPOV, V.I. (1992). Uridine uptake and RNA synthesis in the brain of torpid and awakened ground squirrels. Comp. Biochem. Physiol. B 101: 189-192.
7. BROOKS, S.P.J. and STOREY, K.B. (1992). Mechanisms of glycolytic control during hibernation in the ground squirrel Spermophilus lateralis. J. Comp. Physiol. B 162: 23-28.
8. BRUNET, A., SWEENEY, L.B., STURGILL, J.F., CHUA, K.F., GREER, P.L., LIN, Y., TRAN, H., ROSS, S.E., MOSTOSLAVSKY, R., COHEN, H.Y., HU, L.S., CHENG, H.L., JEDRYCHOWSKI, M.P., GYGI, S.P., SINCLAIR, D.A., ALT, F.W. and GREENBERG, M.E. (2004). Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303: 2011-2015.
9. BUCK, M.J. and BARNES B.M. (2000). Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator. Am. J. Physiol. 279: R255-R262.
10. CALIN, G.A., SEVIGNANI, C., DUMITRU, C.D., HYSLOP, T., NOCH, E., YENDAMURI, S., SHIMIZU, M., RATTAN, S., BULLRICH, F., NEGRINI, M. and CROCE, C.M. (2004). Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc. Natl. Acad. Sci. USA 101: 2999-3004.
11. CAREY, H.V., ANDREWS, M.T. and MARTIN, S.L. (2003). Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol. Rev. 83: 1153-1181.
12. CHAN, J.A., KRICHEVSKY, A.M. and KOSIK, K.S. (2005). MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 65: 6029-6033.
13. CHEN, J.F., MANDEL, E.M., THOMSON, J.M., WU, Q., CALLIS, T.E., HAMMOND, S.M., CONLON, F.L. and WANG, D.Z. (2006). The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38: 228-233.
14. CHEN, Y., MATSUHITA, M., NAIRN, A.C., DAMUNI, Z., Cai, D., FRERICHS, K.U. and HALLENBECK, J.M. (2001). Mechanisms for increased levels of phosphorylation of elongation factor-2 during hibernation in ground squirrels. Biochemistry 40: 11565-11570.
15. CHENG, A.M., BYROM, M.W., SHELTON, J. and FORD, L.P. (2005). Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucl. Acids Res. 33: 1290-1297.
16. CHEUNG, P., ALLIS, C.D. and SASSONE-CORSI, P. (2000). Signaling to chromatin through histone modifications. Cell 103: 263-271.
17. CLARK, S.J., HARRISON, J., PAUL, C.L. and FROMMER, M. (1994). High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 22: 2990-2997.
18. CRAWFORD, F.I., HODGKINSON, C.L., IVANOVA, E.A., LOGUNOVA, L.B., EVANS, G.J., STEINLECHNER, S. and LOUDON, A.S. (2007). The influence of torpor on cardiac expression of genes involved in the circadian clock and protein turnover in the Siberian hamster (Phodopus sungorus). Physiol. Genomics 31: 521-30.
19. DAVIE, J.R. (1998). Covalent modifications of histones: expression from chromatin templates. Curr. Opin. Genet. Dev. 8: 173-178.
20. DENU, J.M. (2003). Linking chromatin function with metabolic networks: Sir2 family of NAD(+)-dependent deacetylases. Trends Biochem. Sci. 28: 41-48.
21. DOBROVIC, A. and SIMPFENDORFER, D. (1997). Methylation of the BRCA1 gene in sporadic breast cancer. Cancer Res. 57: 3347-3350.
22. EDDY, S.F. and STOREY, K.B. (2002). Dynamic use of cDNA arrays: heterologous probing for gene discovery and exploration of organismal adaptation to environment stress. In: Cell and Molecular Responses to Stress (Storey, K.B. and Storey, J.M., eds.), Vol. 3: Sensing, Signaling and Cell Adaptation. Elsevier Press, Amsterdam, pp. 315-325.
23. EDDY, S.F. and STOREY, K.B. (2003). Differential expression of Akt, PPARgamma, and PGC-1 during hibernation in bats. Biochem. Cell Biol. 81: 269-274.
24. EDDY, S.F. and STOREY, K.B. (2007). p38(MAPK) regulation of transcription factor targets in muscle and heart of the hibernating bat, Myotis lucifugus. Cell Biochem. Funct. 25: 759-765.
25. EDDY, S.F., MORIN, P. Jr. and STOREY, K.B. (2004). Cloning and expression of PPAR-gamma and PGC-1alpha from the hibernating ground squirrel, Spermophilus tridecemlineatus. Mol. Cell. Biochem. 269: 175-182.
26. EDDY, S.F., MCNALLY, J.D. and STOREY, K.B. (2005). Up-regulation of a thioredoxin peroxidase-like protein, proliferation associated gene, in hibernating bats. Arch. Biochem. Biophys. 435: 101-111.
27. EDEN, S., HASHIMSHONY, T., KESHET, I., CEDAR, H. and THORNE, A.W. (1998). DNA methylation models histone acetylation. Nature 394: 842.
28. ESAU, C., DAVIS, S., MURRAY, S.F., YU, X.X., PANDEY, S.K., PEAR, M., WATTS, L., BOOTEN, S.L., GRAHAM, M., MCKAY, R., SUBRAMANIAM, A., PROPP, S., LOLLO, B.A., FREIER, S., BENNETT, C.F., BHANOT, S. and MONIA, B.P. (2006). miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab. 3: 87-98.
29. FRAGA, M.F. and ESTELLER, M. (2007). Epigenetics and aging: the targets and the marks. Trends Genet. 23: 413-418.
30. FRANK, C.L. and STOREY, K.B. (1995). Optimal depot fat composition for hibernation by golden-mantled ground squirrels (Spermophilus lateralis). J. Comp. Physiol. B 164: 536-542.
31. 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.
32. FRESCAS, D., VALENTI, L. and ACCILI, D. (2005). Nuclear trapping of the forkhead transcription factor FoxO1 via Sirt-dependent deacetylation promotes expression of glucogenetic genes. J. Biol. Chem. 280: 20589-20595.
33. FRYE, R.A. (2000). Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem. Biophys. Res. Commun. 273: 793-798.
34. FUJII, G., NAKAMURA, Y., TSUKAMOTO, D., ITO, M., SHIBA, T. and TAKAMATSU, N. (2006). CpG methylation at the USF-binding site is important for the liverspecific transcription of the chipmunk HP-27 gene. Biochem J. 395: 203-209.
35. GEISER, F. (2004). Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66: 239-274.
36. GIRDWOOD, D.W., TATHAM, M.H. and HAY, R.T. (2004). SUMO and transcriptional regulation. Semin. Cell. Dev. Biol. 15: 201-210.
37. HARDEN, S.V., TOKUMARU, Y., WESTRA, W.H., GOODMAN, S., AHRENDT, S.A., YANG, S.C. and SIDRANSKY, D. (2003). Gene promoter hypermethylation in tumors and lymph nodes of stage I lung cancer patients. Clin. Cancer Res. 9: 1370-1375.
38. HAY, R.T. (2005). SUMO: a history of modification. Mol. Cell. 18: 1-12.
39. HELLER, H.C. and RUBY, N.F. (2004). Sleep and circadian rhythms in mammalian torpor. Annu. Rev. Physiol. 66: 275-289.
40. HITTEL, D., and STOREY, K.B. (2002). The translation state of differentially expressed mRNAs in the hibernating thirteen-lined ground squirrel (Spermophilus tridecemlineatus). Arch. Biochem. Biophys. 401: 244-254.
41. HOPFL, G., OGUNSHOLA, O. and GASSMANN, M. (2003). Hypoxia and high altitude. The molecular response. Adv. Exp. Med. Biol. 543: 89-115.
42. HUPPI, K., VOLFOVSKY, N., MACKIEWICZ, M., RUNFOLA, T., JONES, T.L., MARTIN, S.E., STEPHENS, R. and CAPLEN, N.J. (2007). MicroRNAs and genomic instability. Sem. Cancer Biol. 17: 65-73.
43. HUTVAGNER,G. and ZAMORE, P.D. (2002). A miRNA in a multiple-turnover RNAi enzyme complex. Science 297: 2056-2060.
44. IORIO, M.V., FERRACIN, M., LIU, C.G., VERONESE, A., SPIZZO, R., SABBIONI, S., MAGRI, E., PEDRIALI, M., FABBRI, M., CAMPIGLIO, M., MENARD, S., PALAZZO, J.P., ROSENBERG, A., MUSIANI, P., VOLINIA, S., NENCI, I., CALIN, G.A., QUERZOLI, P., NEGRINI, M. and CROCE, C.M. (2005). MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 65: 7065-7070.
45. JENUWEIN, T. and ALLIS, C.D. (2001). Translating the histone code. Science 293: 1074-1080.
46. KIM, E., DU, L., BREGMAN, D.B. and WARREN S.L. (1997). Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of premRNA. J. Cell. Biol. 136: 19-28.
47. 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.
48. LAGOS-QUINTANA, M., RAUHUT, R., YALCIN, A., MEYER, J., LENDECKEL, W. and TUSCHL, T. (2002). Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12: 735-739.
49. LAGOUGE, M., ARGMANN, C., GERHART-HINES, Z., MEZIANE, H., LERIN, C., DAUSSIN, F., MESSADEQ, N., MILNE, J., LAMBERT, P., ELLIOTT, P., GENY, B., LAAKSO, M., PUIGSERVER, P. and AUWERX, J. (2006). Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127: 1109-1122.
50. LANDE-DINER, L. and CEDAR, H. (2005). Silence of the genes - mechanisms of long-term repression. Nat. Rev. Genet. 6: 648-654.
51. LEE, Y., JEON, K.,nLEE, J.T., KIM, S., and KIM, V.N. (2002). MiRNA maturation: stepwise processing and subcellular localization. EMBO J. 21: 4663-4670.
52. LEE, Y.J. and HALLENBECK, J.M. (2006). Insights into cytoprotection from ground squirrel hibernation, a natural model of tolerance to profound brain oligaemia. Biochem. Soc. Trans. 34: 1295-1298.
53. 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.
54. LIM, L.P., LAU, N.C., GARRETT-ENGELE, P., GRIMSON, A., SCHELTER, J.M., CASTLE, J., BARTEL, D.P., LINSLEY, P.S. and JOHNSON, J.M. (2005). Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769-773.
55. MACDONALD, J.A. and STOREY, K.B. (1999). Regulation of ground squirrel Na+ K+-ATPase activity by reversible phosphorylation during hibernation. Biochem. Biophys. Res. Commun. 254: 424-429.
56. MACK, G.S. (2006). Epigenetic cancer therapy makes headway. J. Natl. Cancer Inst. 98: 1443-1444.
57. 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.
58. MALYSHEVA, I.N., STOREY, K.B., LOPINA, O.D. and RUBTSOV, A.M. (2001). Ca-ATPase activity and protein composition of sarcoplasmic reticulum membranes isolated from skeletal muscles of typical hibernator, the ground squirrel Spermophilus undulatus. Biosci. Rep. 21: 831-838.
59. MAMADY, H. and STOREY, K.B. (2006). Up-regulation of the endoplasmic reticulum molecular chaperone GRP78 during hibernation in thirteen-lined ground squirrels. Mol. Cell. Biochem. 292: 89-98.
60. MAMADY, H. and STOREY, K.B. (2008). Coping with stress: expression of ATF4, ATF6 and downstream targets in organs of hibernating ground squirrels. Arch. Biochem. Biophys. 477: 77-85.
61. MIAO, F., WU, X., ZHANG, L., YUAN, Y.C., RIGGS, A.D. and NATARAJAN, R. (2007). Genome-wide analysis of histone lysine methylation variations caused by diabetic conditions in human monocytes. J. Biol. Chem. 282: 13854-13863.
62. MORIN, P. Jr. and STOREY, K.B. (2005). Cloning and expression of hypoxiainducible factor 1alpha from the hibernating ground squirrel, Spermophilus tridecemlineatus. Biochem. Biophys. Acta 1729: 32-40.
63. MORIN, P. Jr. and STOREY, K.B. (2006). Evidence for a reduced transcriptional state during hibernation in ground squirrels. Cryobiology 53: 310-318.
64. MORIN, P. Jr., NI, J., MCMULLEN, D.C. and STOREY, K.B. (2008a). Expression of Nrf2 and its downstream gene targets in hibernating thirteen-lined ground squirrels, Spermophilus tridecemlineatus. Mol. Cell. Biochem. 312: 121-129.
65. MORIN, P. Jr., DUBUC, A. and STOREY, K.B. (2008b). Differential expression of microRNA species in organs of hibernating ground squirrels: a role in translational suppression during torpor. Biochim. Biophys. Acta 1779: 628-633.
66. MOTTA, M.C., DIVECHA, N., LEMIEUX, M., KAMEL, C., CHEN, D., GU, W., BULTSMA, Y., MCBURNEY, M. and GUARENTE, L. (2004). Mammalian SIRT1 represses forkhead transcription factors. Cell 116: 551-563.
67. O'DRISCOLL, L. (2006). The emerging world of microRNA. Anticancer Res. 26(6B): 4271-7278.
68. OELTGEN, P.R., NILEKANI, S.P., NUCHOLS, P.A., SPURRIER, W.A. and SU, T.P. (1988). Further studies on opioids and hibernation: delta opioid receptor ligand selectively induced hibernation in summer-active ground squirrels. Life Sci. 43: 1565-1574.
69. OHTANI-FUJITA, N., DRYJA, T.P., RAPAPORT, J.M., FUJITA, T., MATSUMURA, S., OZASA, K., WATANABE, Y., HAYASHI, K., MAEDA, K., KINOSHITA, S., MATSUMURA, T., OHNISHI, Y., HOTTA, Y., TAKAHASHI, R., KATO, M.V., ISHIZAKI, K., SASAKI, M.S., HORSTHEMKE, B., MINODA, K. and SAKAI, T. (1997). Hypermethylation in the retinoblastoma gene is associated with unilateral, sporadic retinoblastoma. Cancer Genet. Cytogenet. 98: 43-49.
70. 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. Japan J. Physiol. 54: 295-305.
71. PICARD, F., KURTEV, M., CHUNG, N., TOPARK-NGARM, A., SENAWONG, T., MACHADO De OLIVEIRA, R., LEID, M., MCBURNEY, M.W. and GUARENTE, L. (2004). Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 429: 771-776.
72. PILLAI, R.S., BHATTACHARYYA, S.N. and FILIPOWICZ, W. (2007). Repression of protein synthesis by miRNAs: how many mechanisms. Trends Cell Biol. 17: 118-126.
73. PRENDERGAST, B.J., FREEMAN, D.A., ZUCKER, I. and NELSON, R.J. (2002). Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. Am. J. Physiol. 282: R1054-R1062.
74. RATCLIFFE, P.J., O'ROURKE, J.F., MAXWELL, P.H. and PUGH, C.W. (1998). Oxygen sensing, hypoxia-inducible factor-1 and the regulation of mammalian gene expression. J. Exp. Biol. 201: 1153-1162.
75. RODGERS, J.T., LERIN, C., HAAS, W., GYGI, S.P., SPIEGELMAN, B.M. and PUIGSERVER, P. (2005). Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434: 113-118.
76. SARRAF, S.A. and STANCHEVA, I. (2004). Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol. Cell 15: 595-605.
77. SEMENZA, G.L. (2000). HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 88: 1474-1480.
78. SHAVLAKADZE, T. and GROUNDS, M. (2006). Of bears, frogs, meat, mice and men: complexity of factors affecting skeletal muscle mass and fat. Bioessays 28: 994-1009.
79. SHI, T., WANG, F., STIEREN, E. and TONG, Q. (2005). SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J. Biol. Chem. 280: 13560-13567.
80. STERNSDORF, T., JENSEN, K. and WILL, H. (1997). Evidence for covalent modification of the nuclear dot-associated proteins PML and Sp100 by PIC1/ SUMO-1. J. Cell. Biol. 139: 1621-134.
81. STOREY, K.B. (2003). Mammalian hibernation: transcriptional and translational controls. Adv. Exp. Med. Biol. 543: 21-38.
82. STOREY, K.B. (2004). Cold, ischemic organ preservation: lessons from natural systems. J. Invest. Med. 52: 315-322.
83. STOREY, K.B. and STOREY, J.M. (1990). Facultative metabolic rate depression: molecular regulation and biochemical adaptation in anaerobiosis, hibernation, and estivation. Quart. Rev. Biol. 65, 145-174.
84. STOREY, K.B. and STOREY, J.M. (2004). Metabolic rate depression in animals: transcriptional and translational controls. Biol. Rev. Camb. Phil. Soc. 79: 207-233.
85. STOREY, K.B. and STOREY, J.M. (2007). Putting life on 'pause' - molecular regulation of hypometabolism. J. Exp. Biol. 210: 1700-1714.
86. TATE, P.H. and BIRD A.P. (1993). Effects of DNA methylation on DNA-binding proteins and gene expression. Curr. Opin. Genet. Develop. 3: 226-231.
87. THOMSON, J.M., PARKER, J., PEROU, C.M. and HAMMOND, S.M.(2004). A custom microarray platform for analysis of microRNA gene expression. Nat. Methods 1: 47-53.
88. VAN BREUKELEN, F. and MARTIN, S.L. (2002). Reversible depression of transcription during hibernation. J. Comp. Physiol. B 172: 355-361.
89. VAQUERO, A., SCHER, M., LEE, D., ERDJUMENT-BROMAGE, H., TEMPST, P. and REINBERG, D. (2004). Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin. Mol. Cell 16: 93-105.
90. VECCHIO, L., SOLDANI, C., BOTTONE, M.G., MALATESTA, M., MARTIN, T.E., ROTHBLUM, L.I., PELLICCIARI, C. and BIGGIOGERA, M. (2006). DADLE induces a reversible hibernation-like state in HeLa cells. Histochem. Cell Biol. 125: 193-201.
91. WANG, L.C.H. and LEE, T.F (1996). Torpor and hibernation in mammals: metabolic, physiological and biochemical adaptations. In Handbook of Physiology: Environmental Physiology (Fregley, M.J., and Blatteis, C.M., eds.). Oxford University Press, New York, pp. 507-532.
92. WAY, J.M., HARRINGTON, W.W., BROWN, K.K., GOTTSCHALK, W.K., SUNDSETH, S.S., MANSFIELD, T.A., RAMACHANDRAN, R.K., WILLSON, T.M. and KLIEWER, S.A. (2001). Comprehensive messenger ribonucleic acid profiling reveals that peroxisome proliferator-activated receptor gamma activation has coordinate effects on gene expression in multiple insulin-sensitive tissues. Endocrinology 142: 1269-1277.
93. YEUNG, F., HOBERG, J.E., RAMSEY, C.S., KELLER, M.D., JONES, D.R., FRYE, R.A. and MAYO, M.W. (2004). Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 23: 2369-2380.
94. YI, R., QIN, Y., MACARA, I.G. and CULLEN, B.R. (2003). Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17: 3011-3016.
95. ZENG, Y., YI, R. and CULLEN B.R. (2003). MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc. Natl. Acad. Sci. USA 100: 9779-9784.
96. ZHONG, S. SALOMONI, P. and PANDOLFI, P.P. (2000). The transcriptional role of PML and the nuclear body. Nat. Cell Biol. 2: E85-E90.