A mutant Drosophila homolog of mammalian clock disrupts circadian rhythms and transcription of period and timeless

Cell

Volumn 93, Issue 5, 1998, Pages 791-804

  Allada, Ravi ^a,b   White, Neal E ^a   So, W Venus ^a   Hall, Jeffrey C ^a   Rosbash, Michael ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CIRCADIAN RHYTHM; DROSOPHILA; GENE EXPRESSION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; TIME;

DROSOPHILA; INSECTA; MAMMALIA;

EID: 17044451254     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81440-3     Document Type: Article

References (74)

1. Albrecht, U., Sun, Z.S., Eichele, G., and Lee, C.C. (1997). A differential response of two putative mammalian circadian regulators, mper1 and mper2, to light. Cell 91, 1055-1064.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
3. Antoch, M.P., Song, E.-J., Chang, A.-M., Vitaterna, M.H., Zhao, Y., Wilsbacher, L.D., Sangoram, A.M., King, D.P., Pinto, L.H., and Takahashi, J.S. (1997). Functional identification of the mouse circadian clock gene by transgenic BAC rescue. Cell 89, 655-667.
4. Aronson, B.D., Johnson, K.A., and Dunlap, J.C. (1994). Circadian clock locus frequency: protein encoded by a single open reading frame defines period length and temperature compensation. Proc. Natl. Acad. Sci. USA 91, 7683-7687.
5. Baca, M., Borgstahl, G.E., Boissinot, M., Burke, P.M., Williams, D.R., Slater, K.A., and Getzoff, E.D. (1994). Complete chemical structure of photoactive yellow protein: novel thioester-linked 4-hydroxycinnamyl chromophore and photocycle chemistry. Biochem. 33, 14369-14377.
6. Blackman, R.K. (1996). Streamlined protocol for polytene chromosome in situ hybridization. BioTechniques 21, 226-229.
7. Brandes, C., Plautz, J.D., Stanewsky, R., Jamison, C.F., Straume, M., Wood, K.V., Kay, S.A., and Hall, J.C. (1996). Novel features of Drosophila period transcription revealed by real-time luciferase reporting. Neuron 16, 687-692.
8. Crews, S.T. (1998). Control of cell lineage-specific development and transcription by bHLH-PAS proteins. Genes Dev. 12, 607-620.
9. Crosthwaite, S.K., Dunlap, J.C., and Loros, J.J. (1997). Neurospora wc-1 and wc-2: transcription, photoresponses, and the origins of circadian rhythmicity. Science 276, 763-769.
10. Dolwick, K.M., Swanson, H.I., and Bradfield, C.A. (1993). In vitro analysis of Ah receptor domains involved in ligand-activated DNA recognition. Proc. Natl. Acad. Sci. USA 90, 8566-8570.
11. Edery, I., Zwiebel, L.J., Dembinska, M.E., and Rosbash, M. (1994). Temporal phosphorylation of the Drosophila period protein. Proc. Natl. Acad. Sci. USA 91, 2260-2264.
12. Engels, W.R., Preston, C.R., Thompson, P., and Eggleston, W.B. (1986). In situ hybridization to Drosophila salivary chromosomes with biotinylated DNA probes and alkaline phosphatase. BRL Focus 8, 6-8.
13. Ewer, J., Frisch, B., Hamblen-Coyle, M.J., Rosbash, M., and Hall, J.C. (1992). Expression of the period clock gene within different cell types in the brain of Drosophila adults and mosaic analysis of these cells' influence on circadian behavioral rhythms. J. Neurosci. 12, 3321-3349.
14. Feldman, J.F., and Dunlap, J.C. (1989). Neurospora crassa: a unique system for studying circadian rhythms. Photochem. Photobiol. Rev. 7, 319-368.
15. Feldman, J.F., and Hoyle, M. (1973). Isoaltion of circadian clock mutants of Neurospora crassa. Genetics 755, 605-613.
16. FlyBase Consortium (1998). FlyBase: a Drosophila database. Nucleic Acids Res. 26, 85-88.
17. Grasso, G., Bordne, D., and White, K. (1996). Drosophila Info. Serv. 77, 94-96.
18. Hamblen-Coyle, M., Konopka, R.J., Zwiebel, L.J., Colot, H.V., Dowse, H.B., Rosbash, M., and Hall, J.C. (1989). A new mutation at the period locus with some novel effects on circadian rhythms. J. Neurogenet. 5, 229-256.
19. Hamblen-Coyle, M.J., Wheeler, D.A., Rutila, J.E., Rosbash, M., and Hall, J.C. (1992). Behavior of period-altered circadian rhythm mutants of Drosophila light:dark cycles. J. Insect Behav. 5, 417-446.
20. - mutants. J. Neurogenet. 3, 249-291.
21. Hao, H., Allen, D.L., and Hardin, P.E. (1997). A circadian enhancer mediates PER-dependent mRNA cycling in Drosophila melanogaster. Mol. Cell. Biol. 17, 3687-3693.
22. Hardin, P.E. (1994). Analysis of period mRNA cycling in Drosophila head and body tissues indicates that body oscillators behave differently from head oscillators. Mol. Cell. Biol. 14, 7211-7218.
23. Hardin, P.E., Hall, J.C., and Rosbash, M. (1990). Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343, 536-540.
24. Hardin, P.E., Hall, J.C., and Rosbash, M. (1992). Circadian oscillations in period gene mRNA levels are transcriptionally regulated. Proc. Natl. Acad. Sci. USA 89, 11711-11715.
25. Hartl, D.L., Nurminsky, D.I., Jones, R.W., and Lozovskaya, E.R. (1994). Genome structure and evolution in Drosophila: applications of the framework P1 map. Proc. Natl. Acad. Sci. USA 91, 6824-6829.
26. Hogenesch, J.B., Chan, W.K., Jackiw, V.H., Brown, B.C., Gu, Y.-Z., Pray-Grant, M., Perdew, G.H., and Bradfield, C.A. (1997). Characterization of a subset of the basic-helix-loop-helix-PAS superfamily that interacts with components of the dioxin signaling pathway. J. Biol. Chem. 272, 8581-8593.
27. Hogenesch, J.B., Gu, Y.-Z., Jain, S., and Bradfield, C.A. (1998). The basic-helix-loop-helix-PAS orphan MOP3 forms transcriptionally active complexes with circadian and hypoxia factors. Proc. Natl. Acad. Sci. USA 95, 5474-5479.
28. Huang, Z.J., Edery, I., and Rosbash, M. (1993). PAS is a dimerization domain common to Drosophila Period and several transcription factors. Nature 364, 259-262.
29. Kimmerly, W., Stultz, K., Lewis, S., Lewis, K., Lustre, V., Romero, R., Benke, J., Sun, D., Shirley, G., Martin, C., and Palazzolo, M. (1996). A P1-based physical map of the Drosophila euchromatic genome. Genome Res. 6, 414-430.
30. 19H deletion, distal of kit. Genetics 146, 1049-1060.
31. Kondo, T., Strayer, C.A., Kulkarni, R.D., Taylor, W., Ishiura, M., Golden, S.S., and Johnson, C.H. (1993). Circadian rhythms in prokaryotes: luciferase as a reporter of circadian gene expression in cyanobacteria. Proc. Natl. Acad. Sci. USA 90, 5672-5676.
32. Kondo, T., Tsinoremas, N.F., Golden, S.S., Johnson, C.H., Kutsuna, S., and Isjiura, M. (1994). Circadian Clock mutants of Cyanobacteria. Science 266, 1233-1236.
33. Konopka, R.J., and Benzer, S. (1971). Clock mutants of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 68, 2112-2116.
34. Konopka, R.J., Hamblen-Coyle, M.J., Jamison, C.F., and Hall, J.C. (1994). An ultrashort clock mutation at the period locus of Drosophila melanogaster that reveals some new features of the fly's circadian system. J. Biol. Rhythms 9, 189-216.
35. Kornhauser, J.M., Nelson, D.E., Mayo, K.E., and Takahashi, J.S. (1990). Photic and circadian regulation of c-fos gene expression in the hamster suprachiasmatic nucleus. Neuron 5, 127-134.
36. Kornhauser, J.M., Nelson, D.E., Mayo, K.E., and Takahashi, J.S. (1992). Regulation of jun-B messenger RNA and AP-1 activity by light and a circadian clock. Science 255, 1581-1584.
37. Lewis, E.B., and Bacher, F. (1968). Method of feeding ethyl methane sulfonate (EMS) to Drosophila males. Drosophila Info. Serv. 43, 193.
38. Lindebro, M.C., Poellinger, L., and Whitelaw, M.L. (1995). Protein-protein interaction via PAS domains: role of the PAS domain in positive and negative regulation of the bHLH/PAS dioxin receptor-Arnt transcription factor complex. EMBO J. 14, 3528-3539.
39. Linden, H., and Macino, G. (1997). White collar 2, a partner in blue-light signal transduction, controlling expresssion of light-regulated genes in Neurospora crassa. EMBO J. 16, 98-109.
40. Liu, X., Yu, Q., Huang, Z., Zwiebel, L.J., Hall, J.C., and Rosbash, M. (1991). The strength and periodicity of Drosophila melanogaster circadian rhythms are differentially affected by alterations in period gene expression. Neuron 6, 753-766.
41. Ma, P.C.M., Rould, M.A., Weintraub, H., and Pabo, C.O. (1994). Crystal structure of MyoD bHLH domain-DNA complex: perspectives on DNA recognition and implications for transcriptional activation. Cell 77, 451-459.
42. S flies: evidence for light-mediated delay of the negative feedback loop in Drosophila. EMBO J. 15, 6877-6886.
43. Mitas, M. (1997). Trinucleotide repeats associated with human disease. Nucleic Acids Res. 25, 2245-2254.
44. Mitchell, P.J., and Tjian, R. (1989). Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science 245, 371-378.
45. Morris, M.E., Viswanathan, N., Kuhlman, S., Davis, F.C., and Weitz, C.J. (1998). A screen for genes induced in the suprachiasmatic nucleus by light. Science 279, 1544-1547.
46. Murre, C., McCae, P.S., and Baltimore, D. (1989). Anew DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56, 777-783.
47. Nagase, T., Ishikawa, K., Nakajima, D., Ohira, M., Seki, N., Miyajima, N., Tanaka, A., Kotani, H., Nomura, N., and Ohara, O. (1997). Prediction of the coding sequences of unidentified human genes. VII. The complete sequences of 10 new cDNA clones from brain which can code for large proteins in vitro. DNA Res. 4, 141-150.
48. Palazzolo, M.J., Hamilton, B.A., Ding, D., Martin, C.H., Mead, D.A., Mierendorf, R.C., Raghavan, K.V., Meyerowitz, E.M., and Lipshitz, H.D. (1990). Phage lambda cDNA cloning vectors for subtractive hybridization, fusion protein expression and Cre-loxP automatic plasmid subcloning. Gene 88, 25-36.
49. Pollenz, R.S., Sullivan, H.R., Holmes, J., Necela, B., and Peterson, R.E. (1996). Isolation and expression of cDNAs from rainbow trout (Oncorhynchus mykiss) that encode two novel basic helix-loop-helix/PER-ARNT-SIM (bHLH/PAS) proteins with distinct functions in the presence of the aryl hydrocarbon receptor. Evidence for alternative mRNA splicing and dominant negative activity in the bHLH/ PAS family. J. Biol. Chem. 271, 30886-30896.
50. Robertson, L.M., and Takshashi, J.S. (1988). Circadian clock in cell culture: I. Oscillation of melatonin release from dissociated chick pineal cells in flow-through microcarrier culture. J. Neurosci. 8, 12-21.
51. Rouyer, F., Rachidi, M., Pikielny, C., and Rosbash, M. (1997). A new clock gene regulated by the circadian clock in the Drosophila head. EMBO J. 16, 3944-3954.
52. Rusak, B., Robertson, H.A., Wisden, W., and Hunt, S.P. (1990). Light pulses that shift rhythms induce gene expression in the suprachiasmatic nucleus. Science 248, 1237-1240.
53. Rutila, J.E., Suri, V., Le, M., So, W.V., Rosbash, M., and Hall, J.C. (1998). CYCLE is a second bHLH-PAS Clock protein essential for circadian rhythmicity and transcription of Drosophila period and timeless. Cell 93, this issue, 805-814.
54. SL mutant of the Drosophila rhythm gene timeless manifests allele-specific interactions with period gene mutants. Neuron 17, 921-929.
55. Sawyer, L.A., Hennessy, J.M., Peixoto, A.A., Rosato, E., Parkinson, H., Costa, R., and Kyriacou, C.P. (1997). Natural variation in a Drosophila clock gene and temperature compensation. Science 278, 2117-2120.
56. Sehgal, A., Rothenfluh-Hilfiker, A., Hunter-Ensor, M., Chen, Y., Myers, M., and Young, M.W. (1995). Circadian oscillations and autoregulation of timeless RNA. Science 270, 808-810.
57. Shearman, L.P., Zylka, M.J., Weaver, D.R., Kolakowski, L.F., Jr., and Reppert, S.M. (1997). Two period homologs: circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron 19, 1261-1269.
58. Shigeyoshi, Y., Taguchi, K., Yamamoto, S., Takekida, S., Yan, L., Tei, H., Moriya, T., Shibata, S., Loros, J.J., Dunlap, J.C., and Okamura, H. (1997). Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell 91, 1043-1053.
59. Smith, R.F., and Konopka, R.J. (1981). Circadian clock phenotypes of chromosome aberrations with a breakpoint at the per locus. Mol. Gen. Genet. 183, 243-251.
60. So, W.V., and Rosbash, M. (1997). Post-transcriptional regulation contributes to Drosophila clock gene mRNA cycling. EMBO J. 16, 7146-7155.
61. Stanewsky, R., Fry, T.A., Reim, I., Saumweber, H., and Hall, J.C. (1996). Bioassaying putative RNA-binding motifs in a protein encoded by a gene that influences courtship and visualy mediated behavior in Drosophila: in vitro mutagenesisof nonA. Genetics 143, 259-275.
62. Stanewsky, R., Jamison, C.F., Plautz, J.D., Kay, S.A., and Hall, J.C. (1997). Multiple circadian-regulated elements contribute to cycling period gene expression in Drosophila. EMBO J. 16, 5006-5018.
63. Su, L.K., Burrell, M., Hill, D.E., Gyuris, J., Brent, R., Wiltshire, R., Trent, J., Vogelstein, B., and Kinzler, K.W. (1995). APC binds to the novel protein EB1. Cancer Res. 55, 2972-2977.
64. Sun, Z.S., Albrecht, U., Zhuchenko, O., Bailey, J., Eichele, G., and Lee, C.C. (1997). RIGUI, a putative mammalian ortholog of the Drosophila period gene. Cell 90, 1003-1011.
65. Swanson, H.I., Chan, W.K., and Bradfield, C.A. (1995). DNA binding specificities and pairing rules of the Ah receptor, ARNT, and SIM proteins. J. Biol. Chem. 270, 26292-26302.
66. Tei, H., Okamura, H., Shigeyoshi, Y., Fukuhara, C., Ozawa, R., Hirose, M., and Sakaki, Y. (1997). Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature 389, 512-516.
67. Tut, T.G., Ghadessy, F.J., Trifiro, M.A., Pinsky, L., and Young, E.L. (1997). Long polyglutamine tracts in the androgen receptor are associated with reduced trans-activation, impaired sperm production, and male infertility. J. Clin. Endocrinol. Metab. 82, 3777-3782.
68. Vitaterna, M.H., King, D.P., Chang, A.-M., Kornhauser, J.M., Lowrey, P.L., McDonald, J.D., Dove, W.F., Pinto, L.H., Turek, F.W., and Takahashi, J.S. (1994). Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 264, 719-725.
69. Welsh, D.K., Logothetis, D.E., Meister, M., and Reppert, S.M. (1995). Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14, 697-706.
70. Wheeler, D.A., Hamblen-Coyle, M.J., Dushay, M.S., and Hall, J.C. (1993). Behavior in light-dark cycles of Drosophila mutants that are arrhythmic, blind, or both. J. Biol. Rhythms 8, 67-94.
71. Whitelaw, M.L., Gottlicher, M., Gustafsson, J.-A., and Poellinger, L. (1993). Definition of a novel ligand binding domain of a nuclear bHLH receptor: co-localization of ligand and hsp90 binding activities within the regulable inactivation domain of the dioxin receptor. EMBO J. 12(11), 4169-4179.
72. Whitelaw, M.L., Gustafsson, J.A., and Poellinger, L. (1994). Identification of transactivation and repression functions of the dioxin receptor and its basic helix-loop-helix/PAS partner factor Arnt: inducible versus constitutive modes of regulation. Mol. Cell. Biol. 14, 8343-8355.
73. Zerr, D.M., Hall, J.C., Rosbash, M., and Siwicki, K.K. (1990). Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J. Neurosci. 10, 2749-2762.
74. Zhou, Y.D., Barnard, M., Tian, H., Li, X., Ring, H.Z., Francke, U., Shelton, J., Richardson, J., Russell, D.W., and McKnight, S.L. (1997). Molecular characterization of two mammalian bHLH-PAS domain proteins selectively expressed in the central nervous system. Proc. Natl. Acad. Sci. USA 94, 713-718.