Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau

Science

Volumn 288, Issue 5465, 2000, Pages 483-491

  Lowrey, Phillip L ^a   Shimomura, Kazuhiro ^a   Antoch, Marina P ^a   Yamazaki, Shin ^b   Zemenides, Peter D ^a   Ralph, Martin R ^c   Menaker, Michael ^b   Takahashi, Joseph S ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE I; TAU PROTEIN;

ALLELE; ARTICLE; AUTOPHOSPHORYLATION; CIRCADIAN RHYTHM; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GENETIC CONSERVATION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SEQUENCE HOMOLOGY;

ALLELES; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CASEIN KINASES; CELL CYCLE PROTEINS; CHROMOSOME MAPPING; CIRCADIAN RHYTHM; CLONING, MOLECULAR; CRICETINAE; FEMALE; HETEROZYGOTE; HUMANS; MALE; MESOCRICETUS; MICE; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHENOTYPE; PHOSPHORYLATION; POINT MUTATION; POLYMERASE CHAIN REACTION; POLYMORPHISM, GENETIC; PROTEIN KINASES; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; SUPRACHIASMATIC NUCLEUS;

ANIMALIA; CRICETINAE; MAMMALIA; MESOCRICETUS AURATUS; RODENTIA;

EID: 0034697099     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.288.5465.483     Document Type: Article

References (103)

1. J. Aschoff, Handbook of Behavioral Neurobiology: Biological Rhythms (Plenum, New York, 1981).
2. C. S. Pittendrigh, Annu. Rev. Physiol. 55, 16 (1993).
3. T. Kondo, M. Ishiura, Bioessays 22, 10 (2000).
4. C. H. Johnson, S. S. Golden, Annu. Rev. Microbiol. 53, 389 (1999).
5. S. L. Anderson and S. A. Kay, Adv. Genet. 35, 1 (1997).
6. M. W. Young, Annu. Rev. Biochem. 67, 135 (1998).
7. J. C. Dunlap, Cell 96, 271 (1999).
8. L. D. Wilsbacher, J. S. Takahashi, Curr. Opin. Genet. Dev. 8, 595 (1998).
9. D. P. King and J. S. Takahashi, Annu. Rev. Neurosci. 23, 713 (2000).
10. M. H. Vitaterna et al. Science 264, 719 (1994).
11. D. King et al., Cell 89, 641 (1997).
12. M. P. Antoch et al., Cell 89, 655 (1997).
13. Z. S. Sun et al., Cell 90, 1003 (1997).
14. H. Tei et al., Nature 389, 512 (1997),
15. L P. Shearman, M. J. Zylka, D. R. Weaver, L F. Kolakowski Jr., S. M. Reppert, Neuron 19, 1261 (1997).
16. U. Albrecht, Z. S. Sun, G. Eichele, C. C. Lee, Cell 91, 1055 (1997).
17. T. Takumi et al., Genes Cells 3, 167 (1998).
18. M. J. Zylka, L. P. Shearman, D. R. Weaver, S. M. Reppert, Neuron 20, 1103 (1998).
19. T. Takumi et al., EMBO J. 17, 4753 (1998).
20. A. Sangoram et al., Neuron 21, 1101 (1998).
21. M. J. Zylka et al., Neuron 21, 1115 (1998).
22. N. Koike et al., FEBS Lett. 441, 427 (1998).
23. T. Takumi et al., Genes Cells 4, 67 (1999).
24. S. A. Tischkau et al., J. Neurosci. 19, RC15 (1999).
25. M. Ikeda and M. Nomura, Biochem. Biophys. Res. Comm. 233, 258 (1997).
26. N. Gekakis et al., Science 280, 1564 (1998).
27. H. Hao, D. L. Allen, P. E. Hardin, Mol. Cell. Biol. 17, 3687 (1997).
28. T. K. Darlington et al., Science 280, 1599 (1998).
29. C. Lee, K. Bae, I. Edery, Mol. Cell. Biol. 19, 5316 (1999).
30. K. Bae, C. Lee, P. E. Hardin, I. Edery, J. Neurosci. 20, 1746 (2000).
31. P. E. Hardin, J. C. Halt, M. Rosbash, Nature 343, 536 (1990).
32. R. Allada, N. E. White, W. V. So, J. C. Hall, M. Rosbash, Cell 93, 791 (1998).
33. J. E. Rutila et al., Cell 93, 805 (1998).
34. A. Sehgal et al., Science 270, 808 (1995).
35. M. P. Myers, K. Wager-Smith, A. Rothenfluh-Hilfiker, M. W. Young, Science 271, 1736 (1996).
36. L. Saez and M. W. Young, Neuron 17, 911 (1996).
37. W. V. So and M. Rosbash, EMBO J. 16, 7146 (1997).
38. I. Edery, L. J. Zwiebel, M. E. Dembinska, M. Rosbash, Proc. Natl. Acad. Sci. U.S.A. 91, 2260 (1994).
39. J. L. Price et al., Cell 94, 83 (1998).
40. B. Kloss et al., Cell 94, 97 (1998).
41. D. C. Klein, R. Y. Moore, S. M. Reppert, Eds., Suprachiasmatic Nucleus: The Mind's Clock (Oxford Univ. Press, New York, 1991).
42. Y. Shigeyoshi et al., Cell 91, 1043 (1997).
43. M. H. Hastings, M. D. Field, E. S. Maywood, D. R. Weaver, S. M. Reppert, J. Neurosci. 19, RC11 (1999).
44. C. T. van der Horst et al., Nature 398, 627-30 (1999).
45. M. H. Vitaterna et al., Proc. Natl. Acad. Sci. U.S.A. 96, 12114 (1999).
46. E. A. Griffin Jr., D. Staknis, C. J. Weitz, Science 286, 768 (1999).
47. K. Kume et al., Cell 98, 193 (1999).
48. H. Okamura et al., Science 286, 2531 (1999).
49. M. D. Field et al., Neuron 25, 437 (2000).
50. M. R. Ralph and M. Menaker, Science 241, 1225 (1988).
51. M. R. Ralph, R. G. Foster, F. C. Davis, M. Menaker, Science 247, 975 (1990).
52. R. Silver, J. LeSauter, P. A. Tresco, M. N. Lehman, Nature 382, 810 (1996).
53. G. Tosini, M. Menaker, Science 272, 419 (1996).
54. E. S. Lander, Nature Genet. 4, 5 (1993).
55. H. Okuizumi et al., Mamm. Genome 8, 121 (1997).
56. N. A. Lisitsyn et al., Nature Genet. 6, 57 (1994).
57. N. A. Lisitsyn, Trends Genet. 11, 303 (1995).
58. S. Adler, Nature 162, 256 (1948).
59. M. Murphy, in The Hamster: Reproduction and Behavior. H. I. Siegel, Ed. (Plenum, New York, 1985). pp. 3-20.
60. 2 generation consisting of 237 progeny.
61. See supplementary material at Science Online at www.sciencemag.org/feature/data/1050211.shl.
62. N. Lisitsyn and M. Wigler, Science 259, 946 (1993).
63. _, Methods Enzymol. 254, 291 (1995).
64. J. Ott, Analysis of Human Genetic Linkage (Johns Hopkins Univ. Press, Baltimore, MD, revised edition, 1991).
65. Large-insert λ clones of approximately 12 kb and 20 kb containing the RDA-650 and RDA-750 products, respectively, were obtained by screening a commercially-available Syrian hamster genomic library (λ DASH II genomic library, Stratagene #945900). Standard library screening protocols were used (97). CsCl-purified clones were prepared and partially sequenced from both ends by primer walking from T7 and T3 bacteriophage promoter sites.
66. 10 was identified in the RDA-750 λ genomic clone by sequencing. PCR primers flanking the microsatellite were designed to test for polymorphism: F 5′-GTGCAGTTGAGGAAGATATCTG-3′, R 5′-CAGTACTAGCAGTTGAATCAAGG-3′. Analysis of products on 7% denaturing polyacrylamide gels using methods modified from (98) revealed a product of approximately 230 bp in tau homozygous animals and of about 225 bp in homozygous wild-type animals.
67. L. B. Rowe et al., Mamm. Genome 5, 253 (1994).
68. The locus amplified in mouse by the hamster SSR2 primers has been assigned the mouse locus symbol, D 15Nwu1, in the Mouse Genome Database (MGD).
69. 2,50 pmol of each primer, 200 μM dNTPs, 100 ng genomic DNA (M70 and tau parental samples), 1 M betaine (Sigma #8-2629), and 2.5 units AmpliTaq DNA polymerase (Perkin Elmer). A "hot start" reaction profile of 30 cycles of 95°C for 1 min, 53°C for 1 min, and 72°C for 2.5 min was used followed by a final extension at 72°C for 10 min. Products were resolved on 1% agarose gels. Those reactions resulting in products in the expected size range were analyzed further by agarose gel electrophoresis, temperature modulated heteroduplex HPLC (WAVE DNA Fragment Analysis System, Transgenomic) or denaturing polyacrylamide gel electrophoresis as described herein.
70. A single nucleotide polymorphism was identified in the Mb gene (myoglobin) by sequencing an intronic PCR product. New primers were designed to amplify a product of approximately 350 bp containing the polymorphism F 5′-CAGAGGGTGCCCTTGACTTCCACC-3′, R 5′-TGGAGGTAGGTGGCCGCCGCTAAA-3′. Products were analyzed by temperature-modulated heteroduplex HPLC according to manufacturer's protocols (Transgenomic).
71. A polymorphism in the Cacng2 gene (calcium channel, voltage-dependent, gamma subunit 2, stargazer) was identified using the following primers: F′ 5′-CCCTGGCGCGCTGTGGAAGCCATC-3′ and R 5′-ATTCCACTACTAATATAATGGATATATGT-3′. An altele of about 310 bp was amplified in tau homozygous animals and an allele of about 320 bp was amplified in homozygous wild-type animals. These products were resolved on 7% denaturing PAGE gels using protocols modified from (98).
72. V. A. Letts et al., Nature Genet. 19, 340 (1998).
73. A polymorphism in the gene Cyp 11b2 (aldosterone synthase) was identified using the following primers: F 5′-GCATGCATCCACCAGTGTACATTC-3′ and R 5′ -GACCACTTACAACATGTACAAACCACAGCC-3′. Agarose gel analysis revealed an allele of approximately 1 kb in tau homozygous animals and an allele of 1.7 kb in homozygous wild-type animals.
74. A polymorphism in the Ela1 gene (elastase) was identified using the following primers: F 5′-GGAAAGTCCTGGGTACTGTGTC-3′ and R 5′-GTTCGCTTCCCTGGTCCTGTAT-3′. Agarose gel analysis revealed an allele of approximately 730 bp in the tau homozygous animals and an allele of about 760 bp in the homozygous wild-type animals.
75. The mouse SSLP marker D15Mit146 was used to amplify a hamster polymorphism of approximately 200 bp in tau homozygous animals and approximately 205 bp in wild-type homozygotes. Products were separated on 7% denaturing PAGE gels using protocols modified from (98).
76. Linkage analysis was performed with the program Map Manager QTb286SK (99).
77. K. J. Fish, A. Cegielska, M. E. Getman, G. M. Landes, D. M. Virshup, J. Biol. Chem. 270, 14875 (1995).
78. PCR primers were designed around the CKlε point mutation in tau homozygous animals such that a product of approximately 160 bp was amplified: F 5′-CATAACTTTCTCATGGGCTTGG-3′ and R 5′-GGGTGTTGATGGAGGCATAG-3′. PCR products were digested for 2 hours at 60°C directly in PCR reaction buffer without purification, using the restriction enzyme Bst API (New England Biolabs). The point mutation in tau animals results in the creation of a Bst API restriction site. Agarose gel analysis revealed an undigested product of approximately 160 bp in wild-type homozygous animals and a digested product of about 137 bp in tau homozygous animals.
79. 2 intercross: D15Mit28 (4/88), D75Mit146 (3/90), and D15Mit35 (14/78). The number of recombinations from CKlε: out of the total number of meioses tested is given in parentheses following the marker name (76). All reactions were separated on 7% PAGE gels using protocols modified from (98).
80. Homozygous tau and wild-type full-length cDNA products were cloned into the pET-30 LIC T7 expression vector according to the manufacturer's protocols (Novagen). Expression of recombinant hamster tau and wild-type CKlε was achieved by growing 250 ml cultures of BL21(DE3)pLysS E. coli hosts containing expression constructs for 16 to 18 hours at 23°C in LB medium supplemented with 34 μg/ml chloramphenicol and 30 μg/ml kanamycin. During incubation, cultures were shaken at 150 rpm. Expression of recombinant protein in the soluble phase was higher in the absence of IPTG; the addition of IPTG decreased the yield of soluble recombinant protein. Expressed protein from the soluble phase was purified by means of a 15-amino acid amino-terminal S-Tag fusion using S-protein agarose according to the manufacturer's protocols (Novagen). S-protein agarose bound with expressed protein was resuspended in 30 mM HEPES, pH 7.5 and stored at 4°C for up to one week. Protein concentrations were determined by taking several 5 μl aliquots of bound S-protein agarose, boiling each for 3 min to release protein, cooling on ice, spinning briefly in a microcentrifuge and then removing supernatants for analysis using a colorimetric protein assay according to the manufacturer's instructions (DC Protein Assay, Bio-Rad).
81. 32P incorporation was detected in dried gels with a Storm Phosphorimager (Molecular Dynamics) and by exposure of X-OMAT AR (Kodak) film at -8O°C.
82. K. F. Gietzen and D. M. Virshup, J. Biol. Chem. 274, 32063 (1999).
83. A. Cegielska, K. F. Gietzen, A. Rivers, D. M. Virshup, J. Biol. Chem. 273, 1357 (1998).
84. 32P]ATP, 3000 Ci/mmol. Reactions were incubated at 37°C for 5 min. To stop reactions, 2X sample buffer was added, followed by boiling for 2 min. Products were separated on 12% SDS-PAGE gels, and dried gels were exposed to phosphor screens and to X-OMAT AR film at -80°C
85. S. D. Gross and R. A. Anderson, Cell. Signal. 10, 699 (1998).
86. P. R. Graves and P. J. Roach, J. Biol. Chem. 270, 21689 (1995).
87. 35S signal. Covered gels were exposed to phosphor screens for 36 hours.
88. R. M. Xu, G. Carmel, R. M. Sweet, J. Kuret, X. Cheng, EMBO J. 14, 1015 (1995).
89. K. L Longenecker, P. J. Roach, T. D. Hurley, J. Mol. Biol. 257, 618 (1996).
90. _, Acta Crystallogr. D 54, 473 (1998).
91. H. Flotow et al., J. Biol. Chem. 265, 14264 (1990).
92. H. Flotow, P. J. Roach, J. Biol. Chem. 266, 3724 (1991).
93. F. Meggio, J. W. Perich, E. C. Reynolds, L. A. Pinna, FEBS Lett. 283, 303 (1991).
94. Z. Songyang et al., Mol Cell. Biol. 16, 6486 (1996).
95. D. O. Morgan and H. L. De Bondt, Curr. Opin. Cell Biol. 6, 239 (1994).
96. S. S. Taylor, E. Radzio-Andzelm, Structure 2, 345 (1994).
97. F. M. Ausube et al., Eds., Current Protocols in Molecular Biology (Wiley, New York, 1993).
98. W. Dietrich et al., Genetics 131, 423 (1992).
99. K. F. Manly and J. M. Olson, Mamm. Genome 10, 327 (1999).
100. Single-letter abbreviations for the amino acid residues are as follows: A, Ala; C, Cys; D, Asp; E, Glu; F, Phe; G, Gly; H, His; I, Ile; K. Lys; L, Leu; M. Met; N, Asn; P, Pro; Q, Gln; R, Arg; S, Ser; T, Thr; V, Val; W, Trp; and Y, Tyr.
101. S. K. Hanks and T. Hunter, FASEB J. 9, 576 (1995).
102. The Mesocricetus auratus DNA sequences reported here have been assigned the following GenBank accession numbers: casein kinase lε (AF242536) and Period 1 (AF249882).
103. Supported by NIMH Grant R37MH39592 (J.S.T.), an Unrestricted Grant in Neuroscience from Bristol-My-ers Squibb (J.S.T.) NIH Grant R01MH56647 (M.M.) and the NSF Center for Biological Timing. We thank T. Jardetzky for creating the three-dimensional images of Cki1 used here; S. M. Reppert for the expression clones of mouse Per1 and Per2; A. Un for assistance with genotyping; M. Goto, E. Freuchte, D. Kolker, L. Raddiffe, and V. Alones for technical assistance; and M. H. Vitaterna, S.-H. Yoo, K. J. Seidenman, L. D. Wilsbacher, and A. M. Sangoram for helpful discussions and advice. J. S. T. is an Investigator of the Howard Hughes Medical Institute.