Epigenetic switching by the metabolism-sensing factors in the generation of orexin neurons from mouse embryonic stem cells

Journal of Biological Chemistry

Volumn 288, Issue 24, 2013, Pages 17099-17110

  Hayakawa, Koji ^a   Hirosawa, Mitsuko ^a   Tabei, Yasuyuki ^a   Arai, Daisuke ^a   Tanaka, Satoshi ^a   Murakami, Noboru ^b   Yagi, Shintaro ^a   Shiota, Kunio ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CREB BINDING PROTEINS; DNA METHYLATION ANALYSIS; EPIGENETIC MECHANISMS; HISTONE ACETYLTRANSFERASES; HISTONE DEACETYLASE INHIBITOR; MOUSE EMBRYONIC STEM CELLS; PLURIPOTENT STEM CELLS; TRANSCRIPTION START SITE;

ACETYLATION; GENES; MAMMALS; METABOLISM; STEM CELLS; TISSUE; TRANSCRIPTION;

NEURONS;

HISTONE ACETYLTRANSFERASE PCAF; HISTONE H3; HISTONE H4; MENINGIOMA EXPRESSED ANTIGEN 5; O N ACETYL GLUCOSAMINE TRANSFERASE; OREXIN; REGULATOR PROTEIN; SIRTUIN 1; TRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; EMBRYONIC STEM CELL; EPIGENETICS; FEMALE; GENE; GENE EXPRESSION; GENE LOCUS; HCRT GENE; HISTONE ACETYLATION; MOUSE; NERVE CELL CULTURE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TRANSCRIPTION INITIATION SITE;

DNA METHYLATION; EMBRYONIC STEM CELL; EPIGENETICS; HISTONE ACETYLASE; HISTONE ACETYLATION; MGEA5; NEUROGENESIS; O-GLCNACYLATION; OGT; SIRT1;

ACETYLATION; ANIMALS; CELL DIFFERENTIATION; CYTIDINE; DEOXYCYTIDINE; DNA METHYLATION; DNA-CYTOSINE METHYLASES; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; FEMALE; GLYCOSYLATION; HEXOSAMINES; HISTONE DEACETYLASE INHIBITORS; HISTONES; HYDROXAMIC ACIDS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; NEURONS; NEUROPEPTIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE ANALYSIS, DNA; SIRTUIN 1; SPHEROIDS, CELLULAR; TRANSCRIPTION INITIATION SITE;

EID: 84879063538     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.455899     Document Type: Article

References (60)

1. Sakurai, T., Amemiya, A., Ishii, M., Matsuzaki, I., Chemelli, R. M., Tanaka, H., Williams, S. C., Richarson, J. A., Kozlowski, G. P., Wilson, S., Arch, J. R., Buckingham, R. E., Haynes, A. C., Carr, S. A., Annan, R. S., McNulty, D. E., Liu, W. S., Terrett, J. A., Elshourbagy, N. A., Bergsma, D. J., and Yanagisawa, M. (1998) Orexins and orexin receptors. A family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92, 1 page following 696
2. de Lecea, L., Kilduff, T. S., Peyron, C., Gao, X., Foye, P. E., Danielson, P. E., Fukuhara, C., Battenberg, E. L., Gautvik, V. T., Bartlett, F. S., 2nd, Frankel, W. N., van den Pol, A. N., Bloom, F. E., Gautvik, K. M., and Sutcliffe, J. G. (1998) The hypocretins. Hypothalamus-specific peptides with neuroexcitatory activity. Proc. Natl. Acad. Sci. U.S.A. 95, 322-327 (Pubitemid 28103952)
3. Tsujino, N., and Sakurai, T. (2009) Orexin/hypocretin. A neuropeptide at the interface of sleep, energy homeostasis, and reward system. Pharmacol. Rev. 61, 162-176
4. De la Herrán-Arita, A. K., Guerra-Crespo, M., and Drucker-Colín, R. (2011) Narcolepsy and orexins. An example of progress in sleep research. Front Neurol. 2, 26
5. Takahashi, K., and Yamanaka, S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (Pubitemid 44233629)
6. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872 (Pubitemid 350138099)
7. Westmoreland, J. J., Hancock, C. R., and Condie, B. G. (2001) Neuronal development of embryonic stem cells. A model of GABAergic neuron differentiation. Biochem. Biophys. Res. Commun. 284, 674-680 (Pubitemid 32924781)
8. Kawasaki, H., Suemori, H., Mizuseki, K., Watanabe, K., Urano, F., Ichinose, H., Haruta, M., Takahashi, M., Yoshikawa, K., Nishikawa, S., Nakatsuji, N., and Sasai, Y. (2002) Generation of dopaminergic neurons and pigmented epithelia from primate ES cells by stromal cell-derived inducing activity. Proc. Natl. Acad. Sci. U.S.A. 99, 1580-1585 (Pubitemid 34136535)
9. Wataya, T., Ando, S., Muguruma, K., Ikeda, H., Watanabe, K., Eiraku, M., Kawada, M., Takahashi, J., Hashimoto, N., and Sasai, Y. (2008) Minimization of exogenous signals in ES cell culture induces rostral hypothalamic differentiation. Proc. Natl. Acad. Sci. U.S.A. 105, 11796-11801
10. Love, D. C., and Hanover, J. A. (2005) The hexosamine signaling pathway. Deciphering the "O-GlcNAc code." Sci. STKE 2005, re13
11. Butkinaree, C., Park, K., and Hart, G. W. (2010) O-linked β-N-acetylglucosamine (O-GlcNAc). Extensive cross-talk with phosphorylation to regulate signaling and transcription in response to nutrients and stress. Biochim. Biophys. Acta 1800, 96-106
12. Rossetti, L., Hawkins, M., Chen, W., Gindi, J., and Barzilai, N. (1995) In vivo glucosamine infusion induces insulin resistance in normoglycemic but not in hyperglycemic conscious rats. J. Clin. Invest. 96, 132-140
13. Patti, M. E., Virkamäki, A., Landaker, E. J., Kahn, C. R., and Yki-Järvinen, H. (1999) Activation of the hexosamine pathway by glucosamine in vivo induces insulin resistance of early postreceptor insulin signaling events in skeletal muscle. Diabetes 48, 1562-1571
14. Balkan, B., and Dunning, B. E. (1994) Glucosamine inhibits glucokinase in vitro and produces a glucose-specific impairment of in vivo insulin secretion in rats. Diabetes 43, 1173-1179 (Pubitemid 24361180)
15. Houtkooper, R. H., Pirinen, E., and Auwerx, J. (2012) Sirtuins as regulators of metabolism and healthspan. Nat. Rev. Mol. Cell Biol. 13, 225-238
16. Imai, S., Armstrong, C. M., Kaeberlein, M., and Guarente, L. (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403, 795-800 (Pubitemid 30111843)
17. Gambetta, M. C., Oktaba, K., and Müller, J. (2009) Essential role of the glycosyltransferase sxc/Ogt in polycomb repression. Science 325, 93-96
18. Sakabe, K., Wang, Z., and Hart, G. W. (2010) β-N-Acetylglucosamine (O-GlcNAc) is part of the histone code. Proc. Natl. Acad. Sci. U.S.A. 107, 19915-19920
19. Fujiki, R., Hashiba, W., Sekine, H., Yokoyama, A., Chikanishi, T., Ito, S., Imai, Y., Kim, J., He, H. H., Igarashi, K., Kanno, J., Ohtake, F., Kitagawa, H., Roeder, R. G., Brown, M., and Kato, S. (2011) GlcNAcylation of histone H2B facilitates its monoubiquitination. Nature 480, 557-560
20. Fong, J. J., Nguyen, B. L., Bridger, R., Medrano, E. E., Wells, L., Pan, S., and Sifers, R. N. (2012) β-N-Acetylglucosamine (O-GlcNAc) is a novel regulator of mitosis-specific phosphorylations on histone H3. J. Biol. Chem. 287, 12195-12203
21. Hanover, J. A. (2010) Epigenetics gets sweeter. O-GlcNAc joins the "histone code". Chem. Biol. 17, 1272-1274
22. Toleman, C., Paterson, A. J., Whisenhunt, T. R., and Kudlow, J. E. (2004) Characterization of the histone acetyltransferase (HAT) domain of a bifunctional protein with activable O-GlcNAcase and HAT activities. J. Biol. Chem. 279, 53665-53673 (Pubitemid 40051874)
23. Shiota, K., Kogo, Y., Ohgane, J., Imamura, T., Urano, A., Nishino, K., Tanaka, S., and Hattori, N. (2002) Epigenetic marks by DNA methylation specific to stem, germ, and somatic cells in mice. Genes Cells 7, 961-969
24. Shiota, K. (2004) DNA methylation profiles of CpG islands for cellular differentiation and development in mammals. Cytogenet. Genome Res. 105, 325-334
25. Sato, S., Yagi, S., Arai, Y., Hirabayashi, K., Hattori, N., Iwatani, M., Okita, K., Ohgane, J., Tanaka, S., Wakayama, T., Yamanaka, S., and Shiota, K. (2010) Genome-wide DNA methylation profile of tissue-dependent and differentially methylated regions (T-DMRs) residing in mouse pluripotent stem cells. Genes Cells 15, 607-618
26. Li, E. (2002) Chromatin modification and epigenetic reprogramming in mammalian development. Nat. Rev. Genet. 3, 662-673
27. Lieb, J. D., Beck, S., Bulyk, M. L., Farnham, P., Hattori, N., Henikoff, S., Liu, X. S., Okumura, K., Shiota, K., Ushijima, T., and Greally, J. M. (2006) Applying whole-genome studies of epigenetic regulation to study human disease. Cytogenet Genome Res. 114, 1-15 (Pubitemid 43890713)
28. Ikegami, K., Ohgane, J., Tanaka, S., Yagi, S., and Shiota, K. (2009) Interplay between DNA methylation, histone modification and chromatin remodeling in stem cells and during development. Int. J. Dev. Biol. 53, 203-214
29. Cedar, H., and Bergman, Y. (2009) Linking DNA methylation and histone modification. patterns and paradigms. Nat. Rev. Genet. 10, 295-304
30. Yagi, S., Hirabayashi, K., Sato, S., Li, W., Takahashi, Y., Hirakawa, T., Wu, G., Hattori, N., Hattori, N., Ohgane, J., Tanaka, S., Liu, X. S., and Shiota, K. (2008) DNA methylation profile of tissue-dependent and differentially methylated regions (T-DMRs) in mouse promoter regions demonstrating tissue-specific gene expression. Genome Res. 18, 1969-1978
31. Takasugi, M., Yagi, S., Hirabayashi, K., and Shiota, K. (2010) DNA methylation status of nuclear-encoded mitochondrial genes underlies the tissue-dependent mitochondrial functions. BMC Genomics 11, 481
32. Hattori, N., Nishino, K., Ko, Y. G., Hattori, N., Ohgane, J., Tanaka, S., and Shiota, K. (2004) Epigenetic control of mouse Oct-4 gene expression in embryonic stem cells and trophoblast stem cells. J. Biol. Chem. 279, 17063-17069 (Pubitemid 38560461)
33. Ernst, J., Kheradpour, P., Mikkelsen, T. S., Shoresh, N., Ward, L. D., Epstein, C. B., Zhang, X., Wang, L., Issner, R., Coyne, M., Ku, M., Durham, T., Kellis, M., and Bernstein, B. E. (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43-49
34. Armstrong, L. (2012) Epigenetic control of embryonic stem cell differentiation. Stem. Cell Rev. 8, 67-77
35. McBurney, M. W., Yang, X., Jardine, K., Hixon, M., Boekelheide, K., Webb, J. R., Lansdorp, P. M., and Lemieux, M. (2003) The mammalian SIR2α protein has a role in embryogenesis and gametogenesis. Mol. Cell. Biol. 23, 38-54 (Pubitemid 36008499)
36. Mizuseki, K., Sakamoto, T., Watanabe, K., Muguruma, K., Ikeya, M., Nishiyama, A., Arakawa, A., Suemori, H., Nakatsuji, N., Kawasaki, H., Murakami, F., and Sasai, Y. (2003) Generation of neural crest-derived peripheral neurons and floor plate cells from mouse and primate embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 100, 5828-5833 (Pubitemid 36576893)
37. Chou, T. C., Lee, C. E., Lu, J., Elmquist, J. K., Hara, J., Willie, J. T., Beuckmann, C. T., Chemelli, R. M., Sakurai, T., Yanagisawa, M., Saper, C. B., and Scammell, T. E. (2001) Orexin (hypocretin) neurons contain dynorphin. J. Neurosci. 21, RC168
38. Dalal, J., Roh, J. H., Maloney, S. E., Akuffo, A., Shah, S., Yuan, H., Wamsley, B., Jones, W. B., Strong, C. de G., Gray, P. A., Holtzman, D. M., Heintz, N., and Dougherty, J. D. (2013) Translational profiling of hypocretin neurons identifies candidate molecules for sleep regulation. Genes Dev. 27, 565-578
39. Dunn-Meynell, A. A., Routh, V. H., Kang, L., Gaspers, L., and Levin, B. E. (2002) Glucokinase is the likely mediator of glucosensing in both glucose-excited and glucose-inhibited central neurons. Diabetes 51, 2056-2065 (Pubitemid 34729008)
40. Yamanaka, A., Beuckmann, C. T., Willie, J. T., Hara, J., Tsujino, N., Mieda, M., Tominaga, M., Yagami, K. i., Sugiyama, F., Goto, K., Yanagisawa, M., and Sakurai, T. (2003) Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron 38, 701-713 (Pubitemid 36694778)
41. + channels stimulated by glucose. A new energy-sensing pathway. Pflugers Arch. 454, 19-27
42. Moriguchi, T., Sakurai, T., Takahashi, S., Goto, K., and Yamamoto, M. (2002) The human prepro-orexin gene regulatory region that activates gene expression in the lateral region and represses it in the medial regions of the hypothalamus. J. Biol. Chem. 277, 16985-16992 (Pubitemid 34967727)
43. Tanaka, S., Kodama, T., Nonaka, T., Toyoda, H., Arai, M., Fukazawa, M., Honda, Y., Honda, M., and Mignot, E. (2010) Transcriptional regulation of the hypocretin/orexin gene by NR6A1. Biochem. Biophys. Res. Commun. 403, 178-183
44. De La Herrán-Arita, A. K., Zomosa-Signoret, V. C., Millán-Aldaco, D. A., Palomero-Rivero, M., Guerra-Crespo, M., Drucker-Colín, R., and Vidaltamayo, R. (2011) Aspects of the narcolepsy-cataplexy syndrome in O/E3-null mutant mice. Neuroscience 183, 134-143
45. Cetinba, N., Macauley, M. S., Stubbs, K. A., Drapala, R., and Vocadlo, D. J. (2006) Identification of Asp-174 and Asp-175 as the key catalytic residues of human O-GlcNAcase by functional analysis of site-directed mutants. Biochemistry 45, 3835-3844
46. Kontou, M., Weidemann, W., Bork, K., and Horstkorte, R. (2009) Beyond glycosylation. Sialic acid precursors act as signaling molecules and are involved in cellular control of differentiation of PC12 cells. Biol. Chem. 390, 575-579
47. Marshall, S., Bacote, V., and Traxinger, R. R. (1991) Complete inhibition of glucose-induced desensitization of the glucose transport system by inhibitors of mRNA synthesis. Evidence for rapid turnover of glutamine:fructose-6-phosphate amidotransferase. J. Biol. Chem. 266, 10155-10161 (Pubitemid 21906781)
48. Buse, M. G. (2006) Hexosamines, insulin resistance, and the complications of diabetes. Current status. Am. J. Physiol. Endocrinol. Metab. 290, E1-E8
49. Kreppel, L. K., and Hart, G. W. (1999) Regulation of a cytosolic and nuclear O-GlcNAc transferase. Role of the tetratricopeptide repeats. J. Biol. Chem. 274, 32015-32022
50. Wells, L., Kreppel, L. K., Comer, F. I., Wadzinski, B. E., and Hart, G. W. (2004) O-GlcNAc transferase is in a functional complex with protein phosphatase 1 catalytic subunits. J. Biol. Chem. 279, 38466-38470 (Pubitemid 39295998)
51. Gu, X., and Wang, D. I. (1998) Improvement of interferon-γ sialylation in Chinese hamster ovary cell culture by feeding of N-acetylmannosamine. Biotechnol. Bioeng. 58, 642-648 (Pubitemid 28210860)
52. Maru, I., Ohta, Y., Murata, K., and Tsukada, Y. (1996) Molecular cloning and identification of N-acyl-D-glucosamine 2-epimerase from porcine kidney as a renin-binding protein. J. Biol. Chem. 271, 16294-16299 (Pubitemid 26236251)
53. Luchansky, S. J., Yarema, K. J., Takahashi, S., and Bertozzi, C. R. (2003) GlcNAc 2-epimerase can serve a catabolic role in sialic acid metabolism. J. Biol. Chem. 278, 8035-8042 (Pubitemid 36800542)
54. Schauer, R. (2009) Sialic acids as regulators of molecular and cellular interactions. Curr. Opin Struct. Biol. 19, 507-514
55. Toleman, C. A., Paterson, A. J., and Kudlow, J. E. (2006) The histone acetyltransferase NCOAT contains a zinc finger-like motif involved in substrate recognition. J. Biol. Chem. 281, 3918-3925 (Pubitemid 43847815)
56. Yang, X., Zhang, F., and Kudlow, J. E. (2002) Recruitment of O-GlcNAc transferase to promoters by corepressor mSin3A. Coupling protein O-GlcNAcylation to transcriptional repression. Cell 110, 69-80 (Pubitemid 34874607)
57. Myers, S. A., Panning, B., and Burlingame, A. L. (2011) Polycomb repressive complex 2 is necessary for the normal site-specific O-GlcNAc distribution in mouse embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 108, 9490-9495
58. Blom, N., Sicheritz-Pontén, T., Gupta, R., Gammeltoft, S., and Brunak, S. (2004) Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4, 1633-1649 (Pubitemid 38738322)
59. Anekonda, T. S. (2006) Resveratrol. A boon for treating Alzheimer's disease? Brain Res. Rev. 52, 316-326
60. Panossian, L., Fenik, P., Zhu, Y., Zhan, G., McBurney, M. W., and Veasey, S. (2011) SIRT1 regulation of wakefulness and senescence-like phenotype in wake neurons. J. Neurosci. 31, 4025-4036