Photoreceptor phagocytosis is mediated by phosphoinositide signaling

FASEB Journal

Volumn 27, Issue 11, 2013, Pages 4585-4595

  Mustafi, Debarshi ^a   Kevany, Brian M ^a   Genoud, Christel ^c   Bai, Xiaodong ^b   Palczewski, Krzysztof ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

LincRNA; Retina; RNA Seq; RPE

Indexed keywords

HISTONE; PHOSPHATIDYLINOSITIDE; TRANSCRIPTION FACTOR CLOCK; TRANSCRIPTOME; UNTRANSLATED RNA;

ANIMAL EXPERIMENT; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENE EXPRESSION; MOLECULAR IMAGING; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPIC VARIATION; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROMOTER REGION; RNA SEQUENCE; SIGNAL TRANSDUCTION;

LINCRNA; RETINA; RNA-SEQ; RPE;

ANIMALS; CIRCADIAN RHYTHM; GENE REGULATORY NETWORKS; HISTONES; MICE; MICE, INBRED C57BL; OPEN READING FRAMES; PHAGOCYTOSIS; PHOSPHATIDYLINOSITOLS; PHOTORECEPTOR CELLS, VERTEBRATE; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; RNA, UNTRANSLATED; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84887087876     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-237537     Document Type: Article

References (88)

1. Asher, G., and Schibler, U. (2011) Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab. 13, 125-137
2. Hogenesch, J. B., and Ueda, H. R. (2011) Understanding systems-level properties: timely stories from the study of clocks. Nat. Rev. Genet. 12, 407-416
3. Panda, S., and Antoch., M. P., Miller, B. H., Su, A. I., and Schook., A. B., Straume, M., Schultz, P. G., and Kay., S. A., Takahashi, J. S., and Hogenesch, J. B. (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109, 307-320 (Pubitemid 34606874)
4. Abruzzi, K. C., Rodriguez, J., Menet, J. S., Desrochers, J., Zadina, A., Luo, W., Tkachev, S., and Rosbash, M. (2011) Drosophila CLOCK target gene characterization: implications for circadian tissue-specific gene expression. Genes Dev. 25, 2374-2386
5. Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R., Ueda, M., Block, G. D., Sakaki, Y., Menaker, M., and Tei, H. (2000) Resetting central and peripheral circadian oscillators in transgenic rats. Science 288, 682-685 (Pubitemid 30241573)
6. Tosini, G., and Menaker, M. (1996) Circadian rhythms in cultured mammalian retina. Science 272, 419-421 (Pubitemid 26138180)
7. Lee, H. S., and Nelms., J. L., Nguyen, M., Silver, R., and Lehman, M. N. (2003) The eye is necessary for a circadian rhythm in the suprachiasmatic nucleus. Nat. Neurosci. 6, 111-112 (Pubitemid 36182776)
8. Huang, W., and Ramsey., K. M., Marcheva, B., and Bass, J. (2011) Circadian rhythms, sleep, and metabolism. J. Clin. Invest. 121, 2133-2141
9. Terman, J. S., and Reme., C. E., and Terman, M. (1993) Rod outer segment disk shedding in rats with lesions of the suprachiasmatic nucleus. Brain Res. 605, 256-264 (Pubitemid 23083086)
10. Lavail, M. M. (1976) Rod outer segment disk shedding in rat retina - relationship to cyclic lighting. Science 194, 1071-1073
11. Kevany, B. M., and Palczewski, K. (2010) Phagocytosis of retinal rod and cone photoreceptors. Physiology 25, 8-15
12. Gal, A., Li, Y., Thompson, D. A., Weir, J., Orth, U., Jacobson, S. G., Apfelstedt-Sylla, E., and Vollrath, D. (2000) Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat. Genet. 26, 270-271
13. D'Cruz, P. M., Yasumura, D., Weir, J., and Matthes., M. T., Abderrahim, H., LaVail, M. M., and Vollrath, D. (2000) Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum. Mol. Genet. 9, 645-651 (Pubitemid 30154023)
14. Flannagan, R. S., Cosio, G., and Grinstein, S. (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat. Rev. Microbiol. 7, 355-366
15. Heth, C. A., and Marescalchi, P. A. (1994) Inositol triphosphate generation in cultured rat retinal-pigment epithelium. Invest. Ophth. Vis. Sci. 35, 409-416 (Pubitemid 24078094)
16. Heth, C. A., and Marescalchi., P. A., and Ye, L. Y. (1995) Ip3 generation increases rod outer segment phagocytosis by cultured royal-college of surgeons retinal-pigment epithelium. Invest. Ophth. Vis. Sci. 36, 984-989
17. Hall, M. O., and Burgess., B. L., Abrams, T. A., and Martinez, M. O. (1996) Carbachol does not correct the defect in the phagocytosis of outer segments by royal college of surgeons rat retinal pigment epithelial cells. Invest. Ophth. Vis. Sci. 37, 1473-1477 (Pubitemid 26177324)
18. Dunlap, J. C. (1999) Molecular bases for circadian clocks. Cell 96, 271-290 (Pubitemid 29059356)
19. Kouzarides, T. (2007) Chromatin modifications and their function. Cell 128, 693-705 (Pubitemid 46273577)
20. Masri, S., and Sassone-Corsi, P. (2010) Plasticity and specificity of the circadian epigenome. Nat. Neurosci. 13, 1324-1329
21. Etchegaray, J. P., Lee, C., Wade, P. A., and Reppert, S. M. (2003) Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 421, 177-182 (Pubitemid 36090986)
22. Katada, S., and Sassone-Corsi, P. (2010) The histone methyltransferase MLL1 permits the oscillation of circadian gene expression. Nat. Struct. Mol. Biol. 17, 1414-1421
23. Valekunja, U. K., and Edgar., R. S., Oklejewicz, M., van der Horst, G. T., O'Neill, J. S., Tamanini, F., Turner, D. J., and Reddy, A. B. (2013) Histone methyltransferase MLL3 contributes to genomescale circadian transcription. Proc. Natl. Acad. Sci. U. S. A. 110, 1554-1559
24. Coon, S. L., and Munson., P. J., Cherukuri, P. F., Sugden, D., Rath, M. F., Moller, M., and Clokie., S. J., Fu, C., Olanich, M. E., Rangel, Z., Werner, T., Program, N. C. S., Mullikin, J. C., and Klein, D. C. (2012) Circadian changes in long noncoding RNAs in the pineal gland. Proc. Natl. Acad. Sci. U. S. A. 109, 13319-13324
25. Lehner, B. (2013) Genotype to phenotype: lessons from model organisms for human genetics. Nat. Rev. Genet. 14, 168-178
26. Wang, Z., Gerstein, M., and Snyder, M. (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10, 57-63
27. Mustafi, D., and Kevany., B. M., Genoud, C., Okano, K., Cideciyan, A. V., Sumaroka, A., and Roman., A. J., Jacobson, S. G., Engel, A., Adams, M. D., and Palczewski, K. (2011) Defective photoreceptor phagocytosis in a mouse model of enhanced S-cone syndrome causes progressive retinal degeneration. FASEB J. 25, 3157-3176
28. Mustafi, D., Maeda, T., Kohno, H., Nadeau, J. H., and Palczewski, K. (2012) Inflammatory priming predisposes mice to age-related retinal degeneration. J. Clin. Invest. 122, 2989-3001
29. Grant, C. E., and Bailey., T. L., and Noble, W. S. (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics 27, 1017-1018
30. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., and Cardona, A. (2012) Fiji: an open-source platform for biological-image analysis. Nat. Meth. 9, 676-682
31. Fiala, J. C. (2005) Reconstruct: a free editor for serial section microscopy. J. Microsc. 218, 52-61 (Pubitemid 40524168)
32. Maeda, A., Maeda, T., Imanishi, Y., Kuksa, V., Alekseev, A., Bronson, J. D., and Zhang., H. B., Zhu, L., Sun, W. Y., Saperstein, D. A., Rieke, F., Baehr, W., and Palczewski, K. (2005) Role of photoreceptor-specific retinol dehydrogenase in the retinoid cycle in vivo. J. Biol. Chem. 280, 18822-18832 (Pubitemid 41379584)
33. Denk, W., and Horstmann, H. (2004) Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol. 2, e329
34. Mortazavi, A., and Williams., B. A., McCue, K., Schaeffer, L., and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Meth. 5, 621-628 (Pubitemid 351911867)
35. Feng, D., and Lazar, M. A. (2012) Clocks, metabolism, and the epigenome. Mol. Cell 47, 158-167
36. Schibler, U., and Sassone-Corsi, P. (2002) A web of circadian pacemakers. Cell 111, 919-922 (Pubitemid 36044683)
37. Reppert, S. M., and Weaver, D. R. (2002) Coordination of circadian timing in mammals. Nature 418, 935-941 (Pubitemid 34976023)
38. Takeda, Y., and Kang., H. S., Angers, M., and Jetten, A. M. (2011) Retinoic acid-related orphan receptor gamma directly regulates neuronal PAS domain protein 2 transcription in vivo. Nucleic Acids Res. 39, 4769-4782
39. Sato, T. K., Panda, S., Miraglia, L. J., and Reyes., T. M., Rudic, R. D., McNamara, P., Naik, K. A., and Fitzgerald., G. A., Kay, S. A., and Hogenesch, J. B. (2004) A functional genomics strategy reveals rora as a component of the mammalian circadian clock. Neuron 43, 527-537 (Pubitemid 39094679)
40. Preitner, N., Damiola, F., Molina, L. L., Zakany, J., Duboule, D., Albrecht, U., and Schibler, U. (2002) The orphan nuclear receptor REV-ERB alpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110, 251-260 (Pubitemid 34876552)
41. Doi, M., Hirayama, J., and Sassone-Corsi, P. (2006) Circadian regulator CLOCK is a histone acetyltransferase. Cell 125, 497-508
42. Liu, X., Zhang, Z., and Ribelayga, C. P. (2012) Heterogeneous expression of the core circadian clock proteins among neuronal cell types in mouse retina. Plos One 7, e50602
43. Tosini, G., and Davidson., A. J., Fukuhara, C., Kasamatsu, M., and Castamon-Cervantes, O. (2007) Localization of a circadian clock in mammalian photoreceptors. FASEB J. 21, 3866-3871 (Pubitemid 350232343)
44. Chowers, I., and Kim., Y. H., Farkas, R. H., Gunatilaka, T. L., and Hackam., A. S., Campochiaro, P. A., Finnemann, S. C., and Zack, D. J. (2004) Changes in retinal pigment epithelial gene expression induced by rod outer segment uptake. Invest. Ophth. Vis. Sci. 45, 2098-2106 (Pubitemid 38902576)
45. Moisseiev, J., and Jerdan., J. A., Dyer, K., Maglione, A., and Glaser, B. M. (1990) Retinal-pigment epithelium-cells can influence endothelial-cell plasminogen activators. Invest. Ophth. Vis. Sci. 31, 1070-1078 (Pubitemid 20197629)
46. Maemura, K., de la Monte, S. M., Chin, M. T., Layne, M. D., Hsieh, C. M., Yet, S. F., Perrella, M. A., and Lee, M. E. (2000) CLIF, a novel cycle-like factor, regulates the circadian oscillation of plasminogen activator inhibitor-1 gene expression. J. Biol. Chem. 275, 36847-36851 (Pubitemid 32002096)
47. Schoenhard, J. A., and Smith., L. H., Painter, C. A., Eren, M., Johnson, C. H., and Vaughan, D. E. (2003) Regulation of the PAI-1 promoter by circadian clock components: differential activation by BMAL1 and BMAL2. J. Mol. Cell. Cardiol. 35, 473-481 (Pubitemid 36539453)
48. Wang, J., Yin, L., and Lazar, M. A. (2006) The orphan nuclear receptor Rev-erb alpha regulates circadian expression of plasminogen activator inhibitor type 1. J. Biol. Chem. 281, 33842-33848 (Pubitemid 46036596)
49. Cho, H., Zhao, X., Hatori, M., Yu, R. T., and Barish., G. D., Lam, M. T., Chong, L. W., DiTacchio, L., and Atkins., A. R., Glass, C. K., Liddle, C., Auwerx, J., Downes, M., Panda, S., and Evans, R. M. (2012) Regulation of circadian behaviour and metabolism by REV-ERB-alpha and REV-ERB-beta. Nature 485, 123-127
50. Botelho, R. J., and Harrison., R. E., Stone, J. C., Hancock, J. F., and Philips., M. R., Jongstra-Bilen, J., Mason, D., Plumb, J., Gold, M. R., and Grinstein, S. (2009) Localized diacylglycerol-dependent stimulation of Ras and Rap1 during phagocytosis. J. Biol. Chem. 284, 28522-28532
51. Almena, M., and Merida, I. (2011) Shaping up the membrane: diacylglycerol coordinates spatial orientation of signaling. Trends Biochem. Sci. 36, 593-603
52. Botelho, R. J., Teruel, M., Dierckman, R., Anderson, R., Wells, A., York, J. D., Meyer, T., and Grinstein, S. (2000) Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151, 1353-1367 (Pubitemid 32047586)
53. Ding, L., Traer, E., McIntyre, T. M., and Zimmerman., G. A., and Prescott, S. M. (1998) The cloning and characterization of a novel human diacylglycerol kinase, DGK iota. J. Biol. Chem. 273, 32746-32752 (Pubitemid 28557660)
54. Kolko, M., and Wang., J. M., Zhan, C., Poulsen, K. A., and Prause., J. U., Nissen, M. H., Heegaard, S., and Bazan, N. G. (2007) Identification of intracellular phospholipases A(2) in the human eye: Involvement in phagocytosis of photoreceptor outer segments. Invest. Ophth. Vis. Sci. 48, 1401-1409 (Pubitemid 351261440)
55. Strunnikova, N. V., Maminishkis, A., Barb, J. J., Wang, F., Zhi, C., Sergeev, Y., Chen, W., and Edwards., A. O., Stambolian, D., Abecasis, G., Swaroop, A., Munson, P. J., and Miller, S. S. (2010) Transcriptome analysis and molecular signature of human retinal pigment epithelium. Hum. Mol. Genet. 19, 2468-2486
56. Shelby, S. J., Colwill, K., Dhe-Paganon, S., Pawson, T., and Thompson, D. A. (2013) MERTK interactions with SH2-domain proteins in the retinal pigment epithelium. PLoS One 8, e53964
57. Green, C. B., and Takahashi., J. S., and Bass, J. (2008) The meter of metabolism. Cell 134, 728-742
58. Hughes, M. E., and Grant., G. R., Paquin, C., Qian, J., and Nitabach, M. N. (2012) Deep sequencing the circadian and diurnal transcriptome of Drosophila brain. Genome Res. 22, 1266-1281
59. Tovin, A., Alon, S., Ben-Moshe, Z., Mracek, P., Vatine, G., Foulkes, N. S., Jacob-Hirsch, J., Rechavi, G., Toyama, R., Coon, S. L., Klein, D. C., Eisenberg, E., and Gothilf, Y. (2012) Systematic identification of rhythmic genes reveals camk1gb as a new element in the circadian clockwork. PLoS Genetics 8, e1003116
60. Ruggiero, L., and Connor., M. P., Chen, J., Langen, R., and Finnemann, S. C. (2012) Diurnal, localized exposure of phosphati-dylserine by rod outer segment in wild-type but not Itgb5(-/-) or Mfge8(-/-) mouse retina. Proc. Natl. Acad. Sci. U. S. A. 109, 8145-8148
61. Finnemann, S. C., and Bonilha., V. L., Marmorstein, A. D., and RodriguezBoulan, E. (1997) Phagocytosis of rod outer segments by retinal pigment epithelial cells requires alpha v beta 5 integrin for binding but not for internalization. Proc. Natl. Acad. Sci. U. S. A. 94, 12932-12937 (Pubitemid 27518454)
62. Ryeom, S. W., and Sparrow., J. R., and Silverstein, R. L. (1996) CD36 participates in the phagocytosis of rod outer segments by retinal pigment epithelium. J. Cell Sci. 109, 387-395 (Pubitemid 26057121)
63. Crandall, D. L., and Busler., D. E., McHendry-Rinde, B., Groeling, T. M., and Kral, J. G. (2000) Autocrine regulation of human preadipocyte migration by plasminogen activator inhibitor-1. J. Clin. Endocrinol. Metab. 85, 2609-2614 (Pubitemid 32269222)
64. Nandrot, E. E., and Kim., Y. H., Brodie, S. E., Huang, X. Z., Sheppard, D., and Finnemann, S. C. (2004) Loss of synchronized retinal phagocytosis and age-related blindness in mice lacking alpha v beta 5 integrin. J. Exp. Med. 200, 1539-1545 (Pubitemid 40094178)
65. Jeon, H., and Kim., J. H., Kim, J. H., Lee, W. H., and Lee., M. S., and Suk, K. (2012) Plasminogen activator inhibitor type 1 regulates microglial motility and phagocytic activity. J. Neuroinflammation 9, 149
66. Park, Y. J., Liu, G., Lorne, E. F., Zhao, X., Wang, J., Tsuruta, Y., Zmijewski, J., and Abraham, E. (2008) PAI-1 inhibits neutrophil efferocytosis. Proc. Natl. Acad. Sci. U. S. A. 105, 11784-11789
67. Burstyn-Cohen, T., Lew, E. D., and Traves., P. G., Burrola, P. G., Hash, J. C., and Lemke, G. (2012) Genetic dissection of TAM receptor-ligand interaction in retinal pigment epithelial cell phagocytosis. Neuron 76, 1123-1132
68. Finnemann, S. C. (2003) Focal adhesion kinase signaling promotes phagocytosis of integrin-bound photoreceptors. EMBO J. 22, 4143-4154 (Pubitemid 37021743)
69. Todt, J. C., Hu, B., and Curtis, J. L. (2004) The receptor tyrosine kinase MerTK activates phospholipase C gamma 2 during recognition of apoptotic thymocytes by murine macrophages. J. Leukoc. Biol. 75, 705-713 (Pubitemid 38405663)
70. Posor, Y., Eichhorn-Gruenig, M., Puchkov, D., Schoneberg, J., Ullrich, A., Lampe, A., Muller, R., Zarbakhsh, S., Gulluni, F., Hirsch, E., Krauss, M., Schultz, C., Schmoranzer, J., Noe, F., and Haucke, V. (2013) Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate. Nature 499, 233-237
71. Steinckwich, N., Schenten, V., Melchior, C., Brechard, S., and Tschirhart, E. J. (2011) An essential role of STIM1, Orai1, and S100A8-A9 proteins for Ca(2+) signaling and Fc gamma R-mediated phagosomal oxidative activity. J. Immunol. 186, 2182-2191
72. Berridge, M. J., and Bootman., M. D., and Roderick, H. L. (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517-529 (Pubitemid 36773404)
73. Swanson, J. A. (2008) Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 9, 639-649
74. Carrasco, S., and Merida, I. (2004) Diacylglycerol-dependent binding recruits PKC theta and RasGRP1 C1 domains to specific subcellular localizations in living T lymphocytes. Mol. Biol. Cell 15, 2932-2942 (Pubitemid 38691880)
75. Lorenzo, P. S., Beheshti, M., Pettit, G. R., Stone, J. C, and Blumberg, P. M. (2000) The guanine nucleotide exchange factor RasGRP is a high-affinity target for diacylglycerol and phorbol esters. Mol. Pharmacol. 57, 840-846 (Pubitemid 30253365)
76. Regier, D. S., Higbee, J., Lund, K M., Sakane, F., Prescott, S. M., and Topham, M. K. (2005) Diacylglycerol kinase iota regulates Ras guanyl-releasing protein 3 and inhibits Rap1 signaling. Proc. Natl. Acad. Sci. U. S. A. 102, 7595-7600 (Pubitemid 40741016)
77. Huynh, K K, Eskelinen, E. L., Scott, C. C, Malevanets, A., Saftig, P., and Grinstein, S. (2007) LAMP proteins are required for fusion of lysosomes with phagosomes. EMBOJ. 26, 313-324 (Pubitemid 46160933)
78. Araki, N., and Johnson., M. T., and Swanson, J. A. (1996) A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J. CellBiol. 135, 1249-1260 (Pubitemid 27014597)
79. Glaser, M., Wanaski, S., Buser, C. A., Boguslavsky, V., Rashidzada, W., Morris, A., Rebecchi, M., and Scarlata., S. F., Runnels, L. W., Prestwich, G. D., Chen, J., Aderem, A., Ahn, J., and McLaughlin, S. (1996) Myristoylated alanine-rich C kinase substrate (MARCKS) produces reversible inhibition of phospholipase C by sequestering phosphatidylinositol 4,5-bisphosphate in lateral domains. J. Biol. Chem. 271, 26187-26193 (Pubitemid 26347465)
80. Allen, L. A. H., and Aderem, A. (1995) A role for Marcks, the alpha-isozyme of protein-kinase-C and myosin-I in zymosan phagocytosis by macrophages. J. Exp. Med. 182, 829-840
81. Van den Bout, I., Truong, H. H., Huveneers, S., Kuikman, I., Danen, E. H. J., and Sonnenberg, A. (2007) The regulation of MacMARCKS expression by integrin beta 3. Exp. Cell Res. 313, 1260-1269 (Pubitemid 46427817)
82. Rey, G., Cesbron, F., Rougemont, J., Reinke, H., Brunner, M., and Naef, F. (2011) Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver. PLoS Biol. 9, e1000595
83. Vollmers, C., and Schmitz., R. J., Nathanson, J., Yeo, G., Ecker, J. R., and Panda, S. (2012) Circadian oscillations of protein-coding and regulatory RNAs in a highly dynamic mammalian liver epigenome. Cell Metab. 16, 833-845
84. Mustafi, D., and Kevany., B. M., Bai, X., Maeda, T., Sears, J. E., and Khalil., A. M., and Palczewski, K (2013) Evolutionarily conserved long intergenic non-coding RNAs in the eye. Hum. Mol. Genet. 22, 2992-3002
85. Koike, N., and Yoo., S. H., Huang, H. C, Kumar, V., Lee, C., Kim, T. K, and Takahashi, J. S. (2012) Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338, 349-354
86. Alenghat, T., Meyers, K, and Mullican., S. E., Leitner, K, Adeniji-Adele, A., Avila, J., Bucan, M., Ahima, R. S., Kaestner, K H., and Lazar, M. A. (2008) Nuclear receptor corepressor and histone deacetylase 3 govern circadian metabolic physiology. Nature 456, 997-1000
87. Gregory, G. D., and Vakoc., C. R., Rozovskaia, T., Zheng, X., Patel, S., Nakamura, T., Canaani, E., and Blobel, G. A. (2007) Mammalian ASH1L is a histone methyltransferase that occupies the transcribed region of active genes. Mol. Cell. Biol. 27, 8466-8479
88. Zhang, E. E., and Liu., A. C., Hirota, T., Miraglia, L. J., Welch, G., and Pongsawakul., P. Y., Liu, X., Atwood, A., Huss, J. W., 3rd, Janes, J., Su, A. I., Hogenesch, J. B., and Kay, S. A. (2009) A genomewide RNAi screen for modifiers of the circadian clock in human cells. Cell 139, 199-210