How temperature changes reset a circadian oscillator

Science

Volumn 281, Issue 5378, 1998, Pages 825-829

  Liu, Yi ^a   Merrow, Martha ^a,b   Loros, Jennifer J ^a   Dunlap, Jay C ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CIRCADIAN RHYTHM; ENVIRONMENTAL FACTOR; FEEDBACK SYSTEM; GENETIC TRANSCRIPTION; LIGHT; NEUROSPORA; NONHUMAN; OSCILLATION; PHOTOPERIODICITY; PRIORITY JOURNAL; THERMOREGULATION; TIME;

BIOLOGICAL CLOCKS; BLOTTING, NORTHERN; CIRCADIAN RHYTHM; DARKNESS; FUNGAL PROTEINS; IMMUNOBLOTTING; KINETICS; LIGHT; NEUROSPORA; RNA, FUNGAL; RNA, MESSENGER; TEMPERATURE;

NEUROSPORA;

EID: 0032493875     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.281.5378.825     Document Type: Article

References (62)

1. J. C. Dunlap, Science 280, 1548 (1998) ; Annu. Rev. Genet. 17, 579 (1996).
2. J. C. Dunlap, Science 280, 1548 (1998) ; Annu. Rev. Genet. 17, 579 (1996).
3. T. Kondo et al., Science 266, 1233 (1994); A. J. Millar, I. A. Carré, C. A. Strayer, N.-H. Chua, S. A. Kay, ibid. 267, 1161 (1995) ; L. A. Sawyer et al., ibid. 278, 2117 (1997) ; J. Loros, Semin. Neurosci. 7, 3 (1995); A. Sehgal, ibid., p. 27 ; P. Hardin and K. Siwicki, ibid., p. 15; D. Bell-Pedersen, N. Garceau, J. J. Loros, J. Genet. 75, 387 (1996) ; J. C. Hall, Trends Neurosci. 18, 230 (1995) ; M. W. Young et al., Cold Spring Harbor Symp. Quant. Biol. 61, 279 (1996) ; M. Rosbash et al., ibid., p. 265 ; P. Y. King et al., Cell 89, 641 (1997).
4. T. Kondo et al., Science 266, 1233 (1994); A. J. Millar, I. A. Carré, C. A. Strayer, N.-H. Chua, S. A. Kay, ibid. 267, 1161 (1995) ; L. A. Sawyer et al., ibid. 278, 2117 (1997) ; J. Loros, Semin. Neurosci. 7, 3 (1995); A. Sehgal, ibid., p. 27 ; P. Hardin and K. Siwicki, ibid., p. 15; D. Bell-Pedersen, N. Garceau, J. J. Loros, J. Genet. 75, 387 (1996) ; J. C. Hall, Trends Neurosci. 18, 230 (1995) ; M. W. Young et al., Cold Spring Harbor Symp. Quant. Biol. 61, 279 (1996) ; M. Rosbash et al., ibid., p. 265 ; P. Y. King et al., Cell 89, 641 (1997).
5. T. Kondo et al., Science 266, 1233 (1994); A. J. Millar, I. A. Carré, C. A. Strayer, N.-H. Chua, S. A. Kay, ibid. 267, 1161 (1995) ; L. A. Sawyer et al., ibid. 278, 2117 (1997) ; J. Loros, Semin. Neurosci. 7, 3 (1995); A. Sehgal, ibid., p. 27 ; P. Hardin and K. Siwicki, ibid., p. 15; D. Bell-Pedersen, N. Garceau, J. J. Loros, J. Genet. 75, 387 (1996) ; J. C. Hall, Trends Neurosci. 18, 230 (1995) ; M. W. Young et al., Cold Spring Harbor Symp. Quant. Biol. 61, 279 (1996) ; M. Rosbash et al., ibid., p. 265 ; P. Y. King et al., Cell 89, 641 (1997).
6. T. Kondo et al., Science 266, 1233 (1994); A. J. Millar, I. A. Carré, C. A. Strayer, N.-H. Chua, S. A. Kay, ibid. 267, 1161 (1995) ; L. A. Sawyer et al., ibid. 278, 2117 (1997) ; J. Loros, Semin. Neurosci. 7, 3 (1995); A. Sehgal, ibid., p. 27 ; P. Hardin and K. Siwicki, ibid., p. 15; D. Bell-Pedersen, N. Garceau, J. J. Loros, J. Genet. 75, 387 (1996) ; J. C. Hall, Trends Neurosci. 18, 230 (1995) ; M. W. Young et al., Cold Spring Harbor Symp. Quant. Biol. 61, 279 (1996) ; M. Rosbash et al., ibid., p. 265 ; P. Y. King et al., Cell 89, 641 (1997).
7. T. Kondo et al., Science 266, 1233 (1994); A. J. Millar, I. A. Carré, C. A. Strayer, N.-H. Chua, S. A. Kay, ibid. 267, 1161 (1995) ; L. A. Sawyer et al., ibid. 278, 2117 (1997) ; J. Loros, Semin. Neurosci. 7, 3 (1995); A. Sehgal, ibid., p. 27 ; P. Hardin and K. Siwicki, ibid., p. 15; D. Bell-Pedersen, N. Garceau, J. J. Loros, J. Genet. 75, 387 (1996) ; J. C. Hall, Trends Neurosci. 18, 230 (1995) ; M. W. Young et al., Cold Spring Harbor Symp. Quant. Biol. 61, 279 (1996) ; M. Rosbash et al., ibid., p. 265 ; P. Y. King et al., Cell 89, 641 (1997).
8. T. Kondo et al., Science 266, 1233 (1994); A. J. Millar, I. A. Carré, C. A. Strayer, N.-H. Chua, S. A. Kay, ibid. 267, 1161 (1995) ; L. A. Sawyer et al., ibid. 278, 2117 (1997) ; J. Loros, Semin. Neurosci. 7, 3 (1995); A. Sehgal, ibid., p. 27 ; P. Hardin and K. Siwicki, ibid., p. 15; D. Bell-Pedersen, N. Garceau, J. J. Loros, J. Genet. 75, 387 (1996) ; J. C. Hall, Trends Neurosci. 18, 230 (1995) ; M. W. Young et al., Cold Spring Harbor Symp. Quant. Biol. 61, 279 (1996) ; M. Rosbash et al., ibid., p. 265 ; P. Y. King et al., Cell 89, 641 (1997).
9. T. Kondo et al., Science 266, 1233 (1994); A. J. Millar, I. A. Carré, C. A. Strayer, N.-H. Chua, S. A. Kay, ibid. 267, 1161 (1995) ; L. A. Sawyer et al., ibid. 278, 2117 (1997) ; J. Loros, Semin. Neurosci. 7, 3 (1995); A. Sehgal, ibid., p. 27 ; P. Hardin and K. Siwicki, ibid., p. 15; D. Bell-Pedersen, N. Garceau, J. J. Loros, J. Genet. 75, 387 (1996) ; J. C. Hall, Trends Neurosci. 18, 230 (1995) ; M. W. Young et al., Cold Spring Harbor Symp. Quant. Biol. 61, 279 (1996) ; M. Rosbash et al., ibid., p. 265 ; P. Y. King et al., Cell 89, 641 (1997).
10. T. Kondo et al., Science 266, 1233 (1994); A. J. Millar, I. A. Carré, C. A. Strayer, N.-H. Chua, S. A. Kay, ibid. 267, 1161 (1995) ; L. A. Sawyer et al., ibid. 278, 2117 (1997) ; J. Loros, Semin. Neurosci. 7, 3 (1995); A. Sehgal, ibid., p. 27 ; P. Hardin and K. Siwicki, ibid., p. 15; D. Bell-Pedersen, N. Garceau, J. J. Loros, J. Genet. 75, 387 (1996) ; J. C. Hall, Trends Neurosci. 18, 230 (1995) ; M. W. Young et al., Cold Spring Harbor Symp. Quant. Biol. 61, 279 (1996) ; M. Rosbash et al., ibid., p. 265 ; P. Y. King et al., Cell 89, 641 (1997).
11. T. Kondo et al., Science 266, 1233 (1994); A. J. Millar, I. A. Carré, C. A. Strayer, N.-H. Chua, S. A. Kay, ibid. 267, 1161 (1995) ; L. A. Sawyer et al., ibid. 278, 2117 (1997) ; J. Loros, Semin. Neurosci. 7, 3 (1995); A. Sehgal, ibid., p. 27 ; P. Hardin and K. Siwicki, ibid., p. 15; D. Bell-Pedersen, N. Garceau, J. J. Loros, J. Genet. 75, 387 (1996) ; J. C. Hall, Trends Neurosci. 18, 230 (1995) ; M. W. Young et al., Cold Spring Harbor Symp. Quant. Biol. 61, 279 (1996) ; M. Rosbash et al., ibid., p. 265 ; P. Y. King et al., Cell 89, 641 (1997).
12. T. Kondo et al., Science 266, 1233 (1994); A. J. Millar, I. A. Carré, C. A. Strayer, N.-H. Chua, S. A. Kay, ibid. 267, 1161 (1995) ; L. A. Sawyer et al., ibid. 278, 2117 (1997) ; J. Loros, Semin. Neurosci. 7, 3 (1995); A. Sehgal, ibid., p. 27 ; P. Hardin and K. Siwicki, ibid., p. 15; D. Bell-Pedersen, N. Garceau, J. J. Loros, J. Genet. 75, 387 (1996) ; J. C. Hall, Trends Neurosci. 18, 230 (1995) ; M. W. Young et al., Cold Spring Harbor Symp. Quant. Biol. 61, 279 (1996) ; M. Rosbash et al., ibid., p. 265 ; P. Y. King et al., Cell 89, 641 (1997).
13. T. Kondo et al., Science 266, 1233 (1994); A. J. Millar, I. A. Carré, C. A. Strayer, N.-H. Chua, S. A. Kay, ibid. 267, 1161 (1995) ; L. A. Sawyer et al., ibid. 278, 2117 (1997) ; J. Loros, Semin. Neurosci. 7, 3 (1995); A. Sehgal, ibid., p. 27 ; P. Hardin and K. Siwicki, ibid., p. 15; D. Bell-Pedersen, N. Garceau, J. J. Loros, J. Genet. 75, 387 (1996) ; J. C. Hall, Trends Neurosci. 18, 230 (1995) ; M. W. Young et al., Cold Spring Harbor Symp. Quant. Biol. 61, 279 (1996) ; M. Rosbash et al., ibid., p. 265 ; P. Y. King et al., Cell 89, 641 (1997).
14. S. C. Crosthwaite, J. J. Loros, J. C. Dunlap, Cell 81, 1003 (1995).
15. M. Hunter-Ensor, A. Ousley, A. Sehgal, ibid. 84, 677 (1996) ; H. Zeng, Z. Qian, M. Myers, M. Rosbash, Nature 380, 129 (1996) ; C. Lee, V. Parikh, T. Itsukaichi, K. Bae, I. Edery, Science 271, 1740 (1996).
16. M. Hunter-Ensor, A. Ousley, A. Sehgal, ibid. 84, 677 (1996) ; H. Zeng, Z. Qian, M. Myers, M. Rosbash, Nature 380, 129 (1996) ; C. Lee, V. Parikh, T. Itsukaichi, K. Bae, I. Edery, Science 271, 1740 (1996).
17. M. Hunter-Ensor, A. Ousley, A. Sehgal, ibid. 84, 677 (1996) ; H. Zeng, Z. Qian, M. Myers, M. Rosbash, Nature 380, 129 (1996) ; C. Lee, V. Parikh, T. Itsukaichi, K. Bae, I. Edery, Science 271, 1740 (1996).
18. M. P. Myers, K. Wager-Smith, A. Rothenfluh-Hilfiker, M. W. Young, Science 271, 1736 (1996).
19. Y. Shigeyoshi et al., Cell 91, 1043 (1997) ; U. Albrecht, Z. S. Sun, G. Eichele, C. C. Lee, ibid., p. 1055 ; L. P. Shearman, M. J. Zylka, D. R. Weaver, L. F. Kolakowski Jr., S. M. Reppert, Neuron 19, 1261 (1997).
20. Y. Shigeyoshi et al., Cell 91, 1043 (1997) ; U. Albrecht, Z. S. Sun, G. Eichele, C. C. Lee, ibid., p. 1055 ; L. P. Shearman, M. J. Zylka, D. R. Weaver, L. F. Kolakowski Jr., S. M. Reppert, Neuron 19, 1261 (1997).
21. Y. Shigeyoshi et al., Cell 91, 1043 (1997) ; U. Albrecht, Z. S. Sun, G. Eichele, C. C. Lee, ibid., p. 1055 ; L. P. Shearman, M. J. Zylka, D. R. Weaver, L. F. Kolakowski Jr., S. M. Reppert, Neuron 19, 1261 (1997).
22. C. S. Pittendrigh and V. G. Bruce, in Photoperiodism and Related Phenomena in Plants and Animals, R. B. Withrow, Ed. (American Association for the Advancement of Science, Washington, DC, 1959), pp. 475-505; C. S. Pittendrigh, Cold Spring Harbor Symp. Quant. Biol. 25, 159 (1960).
23. C. S. Pittendrigh and V. G. Bruce, in Photoperiodism and Related Phenomena in Plants and Animals, R. B. Withrow, Ed. (American Association for the Advancement of Science, Washington, DC, 1959), pp. 475-505; C. S. Pittendrigh, Cold Spring Harbor Symp. Quant. Biol. 25, 159 (1960).
24. V. G. Bruce, Cold Spring Harbor Symp. Quant. Biol. 25, 29 (1960) ; B. Sweeney and J. W. Hastings, ibid., p. 87 ; W. F. Zimmerman, C. S. Pittendrigh, T. Pavlidis, J. Insect Physiol. 14, 669 (1968) ; E. Bünning, The Physiological Clock (Springer-Verlag, New York, ed. 3, revised, 1973).
25. V. G. Bruce, Cold Spring Harbor Symp. Quant. Biol. 25, 29 (1960) ; B. Sweeney and J. W. Hastings, ibid., p. 87 ; W. F. Zimmerman, C. S. Pittendrigh, T. Pavlidis, J. Insect Physiol. 14, 669 (1968) ; E. Bünning, The Physiological Clock (Springer-Verlag, New York, ed. 3, revised, 1973).
26. V. G. Bruce, Cold Spring Harbor Symp. Quant. Biol. 25, 29 (1960) ; B. Sweeney and J. W. Hastings, ibid., p. 87 ; W. F. Zimmerman, C. S. Pittendrigh, T. Pavlidis, J. Insect Physiol. 14, 669 (1968) ; E. Bünning, The Physiological Clock (Springer-Verlag, New York, ed. 3, revised, 1973).
27. V. G. Bruce, Cold Spring Harbor Symp. Quant. Biol. 25, 29 (1960) ; B. Sweeney and J. W. Hastings, ibid., p. 87 ; W. F. Zimmerman, C. S. Pittendrigh, T. Pavlidis, J. Insect Physiol. 14, 669 (1968) ; E. Bünning, The Physiological Clock (Springer-Verlag, New York, ed. 3, revised, 1973).
28. V. D. Gooch, R. A. Wehseler, C. G. Gross, J. Biol. Rhythms 9, 83 (1994).
29. S. Dharmananda, thesis, University of California, Santa Cruz (1980) ; H. Nakashima, J. Interdiscip. Cycle Res. 18, 1 (1987).
30. S. Dharmananda, thesis, University of California, Santa Cruz (1980) ; H. Nakashima, J. Interdiscip. Cycle Res. 18, 1 (1987).
31. I. Edery, J. E. Rutila, M. Rosbash, Science 263, 237 (1994).
32. R. K. Barrett and J. S. Takahashi, J. Neurosci. 15, 5681 (1995) ; M. Zatz, G. Lange, M. Rollag, Am. J. Physiol. 266, R50 (1994) ; C. Heintzen et al., Plant J. 5, 799 (1994).
33. R. K. Barrett and J. S. Takahashi, J. Neurosci. 15, 5681 (1995) ; M. Zatz, G. Lange, M. Rollag, Am. J. Physiol. 266, R50 (1994) ; C. Heintzen et al., Plant J. 5, 799 (1994).
34. R. K. Barrett and J. S. Takahashi, J. Neurosci. 15, 5681 (1995) ; M. Zatz, G. Lange, M. Rollag, Am. J. Physiol. 266, R50 (1994) ; C. Heintzen et al., Plant J. 5, 799 (1994).
35. C. H. Johnson, An Atlas of Phase Response Curves for Circadian and Circatidal Rhythms (Department of Biology, Vanderbilt University, Nashville, TN, 1990).
36. H. Underwood and M. Calaban, J. Biol. Rhythms 2, 179 (1987) ; K. Hoffman, Z. Vgl. Physiol. 62, 93 (1969).
37. H. Underwood and M. Calaban, J. Biol. Rhythms 2, 179 (1987) ; K. Hoffman, Z. Vgl. Physiol. 62, 93 (1969).
38. D. A. Wheeler, M. J. Hamblen-Coyle, M. S. Dushay, J. C. Hall, J. Biol. Rhythms 8, 67 (1993).
39. C. Francis and M. L. Sargent, Plant Physiol. 64, 1000 (1979).
40. N. Y. Garceau, Y. Liu, J. J. Loros, J. C. Dunlap, Cell 87, 469 (1997).
41. Y. Liu, N. Y. Garceau, J. J. Loros, J. C. Dunlap, Ibid., p. 477.
42. Y. Liu, M. Merrow, J. Loros, J. C. Dunlap, data are not shown.
43. A. T. Winfree, The Geometry of Biological Time, vol. 8 of Biomathematics (Springer-Verlag, New York, 1980) ; M. Menaker et al., Eds., Biochronometry (National Academy of Sciences, Washington, DC, 1971), pp. 81-106 ; E. L. Petersen, J. Theor. Biol. 84, 281 (1980) ; V. D. Gooch, in Temporal Order, L. Rensing and N. I. Jaeger, Eds. (Springer-Verlag, New York, 1985), p. 232 ; P. L. Lakin-Thomas, S. Brody, G. G. Coté, J. Biol. Rhythms 6, 281 (1991).
44. A. T. Winfree, The Geometry of Biological Time, vol. 8 of Biomathematics (Springer-Verlag, New York, 1980) ; M. Menaker et al., Eds., Biochronometry (National Academy of Sciences, Washington, DC, 1971), pp. 81-106 ; E. L. Petersen, J. Theor. Biol. 84, 281 (1980) ; V. D. Gooch, in Temporal Order, L. Rensing and N. I. Jaeger, Eds. (Springer-Verlag, New York, 1985), p. 232 ; P. L. Lakin-Thomas, S. Brody, G. G. Coté, J. Biol. Rhythms 6, 281 (1991).
45. A. T. Winfree, The Geometry of Biological Time, vol. 8 of Biomathematics (Springer-Verlag, New York, 1980) ; M. Menaker et al., Eds., Biochronometry (National Academy of Sciences, Washington, DC, 1971), pp. 81-106 ; E. L. Petersen, J. Theor. Biol. 84, 281 (1980) ; V. D. Gooch, in Temporal Order, L. Rensing and N. I. Jaeger, Eds. (Springer-Verlag, New York, 1985), p. 232 ; P. L. Lakin-Thomas, S. Brody, G. G. Coté, J. Biol. Rhythms 6, 281 (1991).
46. A. T. Winfree, The Geometry of Biological Time, vol. 8 of Biomathematics (Springer-Verlag, New York, 1980) ; M. Menaker et al., Eds., Biochronometry (National Academy of Sciences, Washington, DC, 1971), pp. 81-106 ; E. L. Petersen, J. Theor. Biol. 84, 281 (1980) ; V. D. Gooch, in Temporal Order, L. Rensing and N. I. Jaeger, Eds. (Springer-Verlag, New York, 1985), p. 232 ; P. L. Lakin-Thomas, S. Brody, G. G. Coté, J. Biol. Rhythms 6, 281 (1991).
47. A. T. Winfree, The Geometry of Biological Time, vol. 8 of Biomathematics (Springer-Verlag, New York, 1980) ; M. Menaker et al., Eds., Biochronometry (National Academy of Sciences, Washington, DC, 1971), pp. 81-106 ; E. L. Petersen, J. Theor. Biol. 84, 281 (1980) ; V. D. Gooch, in Temporal Order, L. Rensing and N. I. Jaeger, Eds. (Springer-Verlag, New York, 1985), p. 232 ; P. L. Lakin-Thomas, S. Brody, G. G. Coté, J. Biol. Rhythms 6, 281 (1991).
48. D. Sidote, J. Majercak, V. Parikh, I. Edery, Mol. Cell. Biol. 18, 2004 (1998).
49. E. Bünning, Jahrb. Wiss. Bot. 81, 411 (1935) ; D. Njus, L. McMurry, J. W. Hastings, J. Comp. Physiol. B 117, 335 (1977).
50. E. Bünning, Jahrb. Wiss. Bot. 81, 411 (1935) ; D. Njus, L. McMurry, J. W. Hastings, J. Comp. Physiol. B 117, 335 (1977).
51. S. K. Crosthwaite, J. C. Dunlap, J. J. Loros, Science 276, 763 (1997).
52. B. D. Aronson, K. A. Johnson, J. J. Loros, J. C. Dunlap, ibid. 263, 1578 (1994).
53. S. A. Finlayson, I. Lee, P. W. Morgan, Plant Physiol. 116, 17 (1998).
54. L. Rensing, Chronobiol. Int. 6, 297 (1989).
55. The further delay of phases with decreasing temperature is not due to a long time being needed for warming of the culture; warming of the race tubes from 4° to 30°C occurs in less than 20 min. To confirm this, in another set of experiments, we first transferred the cultures to 30°C LL for 20 min before the light was turned off, and the same amount of phase delay was observed (19).
56. C. A. Czeisler, thesis, Stanford University (1978); J. Aschoff and R. Wever, in Handbook of Behavioral Neurobiology, J. Aschoff, Ed. (Plenum, New York, 1981), vol. 4, pp. 311-336.
57. C. A. Czeisler, thesis, Stanford University (1978); J. Aschoff and R. Wever, in Handbook of Behavioral Neurobiology, J. Aschoff, Ed. (Plenum, New York, 1981), vol. 4, pp. 311-336.
58. H. Tei et al., Nature 389, 512 (1997) ; Z. S. Sun et al., Cell 90, 1003 (1997).
59. H. Tei et al., Nature 389, 512 (1997) ; Z. S. Sun et al., Cell 90, 1003 (1997).
60. Cultures of bdA were inoculated into 14 sets of six race tubes each prepared as previously described (18, 24). The cultures were grown in constant light for ∼24 hours and then were transferred into constant darkness either at 21°C (seven sets) or 28°C (seven sets). After 48 hours and at five 4-hour intervals thereafter, groups of race tubes were reciprocally shifted from 21° to 28°C or vice versa; for two control sets, there was no temperature step given after they were transferred into darkness. As a result of the difference in temperature, there were slight differences in the period length between the two sets: the average period length was 22.3 hours at 21°C and 20.5 hours at 28°C.
61. The bdA (wild-type clock) strain was used in all the experiments described in this study. Conditions used for liquid culture experiments were as described (3, 24). For the experiment shown in Fig. 1A, after the cultures were grown in LL at 25°C for a few hours, they were transferred from L to D and from 25°C to either 21° or 28°C at hour 0. Thirteen hours later and, subsequently, at 5-to 6-hour intervals, samples were collected and used as a source for RNA and protein (3, 17, 23, 24). Equal amounts of total RNA (40 μg) or protein (100 μg) were loaded onto agarose or acrylamide gels for electrophoresis as previously described (3, 18, 23), and the gels were blotted and probed as appropriate either with a frq RNA-specific probe (3) or with an antibody to FRQ (17). Equal loading among lanes was confirmed by probing the RNA blot with a ribosomal DNA probe (3) and by staining the protein blot with amido black (18). After developing the blots, densitometry was performed (17, 18).
62. We thank C. H. Johnson for seminal discussions and members of our laboratories for help and advice. This work was supported by grants from NIH (GM34985 and MH01186 to J.C.D and MH44651 to J.C.D and J.J.L.), the Air Force Office of Scientific Research (F49620-94-1-0260 to J.J.L.), NSF (MCB-9307299 to J.J.L.), and the Norris Cotton Cancer Center core grant at Dartmouth Medical School.