Seasonal variations in circadian rhythms coincide with a phase of sensitivity to short photoperiods in the European hamster

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 175, Issue 3, 2005, Pages 167-183

  Monecke, Stefanie ^a   Wollnik, Franziska ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

Author keywords

Activity; Body mass; Melatonin; Reproduction; Seasonal rhythms

Indexed keywords

6 HYDROXYMELATONIN O SULFATE; 6-SULFATOXYMELATONIN; CREATININE; DRUG DERIVATIVE; MELATONIN;

ANIMAL; ARTICLE; BODY WEIGHT; CIRCADIAN RHYTHM; FEMALE; GONAD; HAMSTER; MALE; MOTOR ACTIVITY; PHOTOPERIODICITY; PHYSIOLOGY; REGRESSION ANALYSIS; REPRODUCTION; SEASON; SEX DIFFERENCE; URINE;

ANIMALS; BODY WEIGHT; CIRCADIAN RHYTHM; CREATININE; CRICETINAE; FEMALE; GONADS; MALE; MELATONIN; MOTOR ACTIVITY; PHOTOPERIOD; REGRESSION ANALYSIS; REPRODUCTION; SEASONS; SEX FACTORS;

ANIMALIA; CRICETINAE; CRICETUS CRICETUS;

EID: 17644396383     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-005-0472-6     Document Type: Article

References (75)

1. Barassin S, Kalsbeek A, Saboureau M, Bothorel B, Vivien-Roels B, Malan A, Buijs RM, Pévet P (2000) Potentiation effect of vasopressin on melatonin secretion as determined by transpineal microdialysis in the rat. J Neuroendocrinol 12:61-68
2. Bartness TJ, Goldman BD (1989) Mammalian pineal melatonin: a clock for all seasons. Experientia 45:939-945
3. Bihari Z (2002) The wakening time of the Common hamster (Cricetus cricetus) from the hibernation based on sexual differences. In: Proceedings of 10th meeting of the international hamsterworkgroup, Tongeren. Natuurpunt Studie, pp 91-93
4. Brainard GC, Petterborg LJ, Richardson BA, Reiter RJ (1982) Pineal melatonin in Syrian hamsters: circadian and seasonal rhythms in animals maintained under laboratory and natural conditions. Neuroendocrinology 35:342-348
5. Brown GM, Bar-Or A, Grossi D, Kashur S, Johannson E, Yie SM (1991) Urinary 6-sulphatoxymelatonin, an index of pineal function in the rat. J Pineal Res 10:141-147
6. Buijs RM, Pévet P, Masson-Pévet M, Pool CW, de Vries GJ, Canguilhem B, Vivien-Roels B (1986) Seasonal variation in vasopressin innervation in the brain of the European hamster (Cricetus cricetus). Brain Res 371:193-196
7. Bünning E (1936) Die endonome Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Ber Deutschen Bot Gesellsch 54:590-607
8. Canguilhem B (1989) External and endogenous control of body weight rhythm in the European hamster, Cricetus cricetus. In: Malan A, Canguilhem B (eds) Living in the cold, colloque INSERM. John Libbey Eurotext, London, pp 25-32
9. Canguilhem B, Masson-Pévet M, Koehl C, Pévet P, Bentz I (1988a) Non-gonadal mediated effect of photoperiod on hibernation and body weight cycles of the European hamster. Comp Biochem Physiol 89A:575-578
10. Canguilhem B, Vaultier J-P, Pévet P, Coumaros G, Masson-Pévet M, Bentz I (1988b) Photoperiodic regulation of body mass, food intake, hibernation, and reproduction in intact and castrated male European hamsters, Cricetus cricetus. J Comp Physiol [A] 163:549-557
11. Canguilhem B, Masson-Pévet M, Pévet P, Bentz I (1992) Endogenous, photoperiodic and hormonal control of the body weight rhythm in the female European hamster, Cricetus cricetus. Comp Biochem Physiol 101A:465-470
12. Daan S, Aschoff J (1975) Circadian rhythms of locomotor activity in captive birds and mammals: their variations with season and latitude. Oecologia 18:269-316
13. Daan S, Albrecht U, Van der Horst GTJ, Illnerová H, Roenneberg T, Wehr TA, Schwartz WJ (2001) Assembling a clock for all seasons: are there M and E oscillators in the genes? J Biol Rhythms 16:105-116
14. Darrow JM, Duncan MJ, Bartke A, Bona-Gallo A, Goldman BD (1988) Influence of photoperiod and gonadal steroids on hibernation in the European hamster. J Comp Physiol [A] 163:339-348
15. Elliott JA, Tamarkin L (1994) Complex circadian regulation of pineal melatonin and wheel-running in Syrian hamsters. J Comp Physiol [A] 174:469-484
16. Garidou ML, Vivien-Roels B, Pévet P, Miguez J, Simonneaux V (2003) Mechanisms regulating the marked seasonal variation in melatonin synthesis in the European hamster pineal gland. Am J Physiol Regul Integr Comp Physiol 284:R1043-R1052
17. Gattermann R (1985) Zur Biorhythmik des Goldhamsters (Mesocricetus auratus Waterhouse 1839) IV. Annuale Rhythmen. Zool Jb Physiol 89:279-285
18. Goldman BD (2001) Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J Biol Rhythms 16:283-301
19. Gorman MR, Freeman DA, Zucker I (1997) Photoperiodism in hamsters: abrupt versus gradual changes in day length differentially entrain morning and evening circadian oscillators. J Biol Rhythms 12:122-135
20. Gorman MR, Goldman BD, Zucker I (2001) Mammalian photoperiodism. In: Takahashi JS, Turek FW, Moore RY (eds) Handbook of behavioral neurobiology: circadian clocks, vol 12. Kluwer Academic/Plenum, New York, pp 481-508
21. Gwinner E, Brandstätter R (2001) Complex bird clocks. Philos Trans R Soc Lond B Biol Sci 356:1801-1810
22. Hastings MH, Walker AP, Herbert J (1987) Effect of asymmetrical reductions of photoperiod on pineal melatonin, locomotor activity and gonadal condition of male Syrian hamsters. J Endocrinol 114:221-229
23. Hoffmann K, Illnerová H (1986) Photoperiodic effects in the Djungarian hamster. Rate of testicular regression and extension of pineal melatonin pattern depend on the way of change from long to short photoperiods. Neuroendocrinology 43:317-321
24. Illnerová H, Hoffmann K, Vaněček J (1984) Adjustment of pineal melatonin and N-acetyltransferase rhythms to change from long to short photoperiod in the Djungarian hamster Phodopus sungorus. Neuroendocrinology 38:226-231
25. Klante G, Brinschwitz T, Secci K, Wollnik F, Steinlechner S (1997) Creatinine is an appropriate reference for urinary sulphatoxymelatonin of laboratory animals and humans. J Pineal Res 23:191-197
26. Klante G, Secci K, Masson-Pévet M, Pévet P, Vivien-Roels B, Steinlechner S, Wollnik F (1999) Interstrain differences in activity pattern, pineal function, and SCN melatonin receptor density of rats. Am J Physiol 276:R1078-R1086
27. Krsmanovic L, Mikeš M, Habijan V, Mikeš B (1984) Reproductive activity of Cricelus cricetus L. in Vojvodina-Yugoslavia. Acta Zool Fennica 171:173-174
28. Lee TM, Zucker I (1995) Seasonal variations in circadian rhythms persist in gonadectomized golden-mantled ground squirrels. J Biol Rhythms 10:188-195
29. Lee TM, Carmichael MS, Zucker I (1986) Circannual variations in circadian rhythms of ground squirrels. Am J Physiol 250:R831-R836
30. Lerchl A, Schlatt S (1993) Influence of photoperiod on pineal melatonin synthesis, fur color, body weight, and reproductive function in the female Djungarian hamster, Phodopus sungorus. Neuroendocrinology 57:359-364
31. Masson-Pévet M, Pévet P, Vivien-Roels B (1987) Pinealectomy and constant release of melatonin or 5-methoxytryptamine induce testicular atrophy in the European hamster (Cricetus cricetus L.). J Pineal Res 4:79-88
32. Masson-Pévet M, Naimi F, Canguilhem B, Saboureau M, Bonn D, Pévet P (1994) Are the annual reproductive and body weight rhythms in the male European hamster (Cricetus cricetus) dependent upon a photoperiodically entrained circannual clock? J Pineal Res 17:151-163
33. McEachron DL, Schull J (1993) Hormones, rhythms, and the blues. In: Schulkin J (ed) Hormonally induced changes in mind and brain. Academic Press, New York, pp 287-355
34. Messager S, Ross AW, Barren P, Morgan PJ (1999) Decoding photoperiodic time through Per1 and ICER gene amplitude. Proc Natl Acad Sci USA 96:9938-9943
35. Messager S, Hazlerigg DG, Mercer JG, Morgan PJ (2000) Photoperiod differentially regulates the expression of Per1 and ICER in the pars tuberalis and the suprachiasmatic nucleus of the Siberian hamster. Eur J Neurosci 12:2865-2870
36. Michener GR (1992) Sexual differences in over-winter torpor patterns of Richardson's ground squirrels in natural hibernacula. Oecologia 89:397-406
37. Monecke S, Wollnik F (2004) European hamsters (Cricetus cricetus) show a transient phase of insensitivity to long photoperiods after gonadal regression. Biol Reprod 70:1438-1443. DOI 10.1095/biolreprod.103.023002
38. Mrosovsky N, Boshes M, Hallonquist JD, Lang K (1976) Circ-annual cycle of circadian cycles in a golden-mantled ground squirrel. Naturwissenschaften 63:298-299
39. Nechay G (2000) Status of hamsters Cricetus cricetus, Cricetus migratorius, Mesocricetus Newtoni and other hamster species in Europe. Series: nature and environment, vol 106. Council of Europe, Strasbourg Cedex, p 73
40. Nowak R, McMillen IC, Redman J, Short RV (1987) The correlation between serum and salivary melatonin concentrations and urinary 6-hydroxymelatonin sulphate excretion rates: two non-invasive techniques for monitoring human circadian rhythmicity. Clin Endocrinol (Oxf) 27:445-452
41. Nuesslein-Hildesheim B, O'Brien JA, Ebling JP, Maywood ES, Hastings MH (2000) The circadian cycle of mPER clock gene products in the suprachiasmatic nucleus of the Siberian hamster encodes both daily and seasonal time. Eur J Neurosci 12:2856-2864
42. Pévet P (2003) Melatonin: from seasonal to circadian signal. J Neuroendocrinol 15:422-426
43. Pévet P, Masson-Pévet M, Hermès MLHJ, Buijs RM, Canguilhem B (1989) Photoperiod, pineal gland, vasopressinergic innervation and timing of hibernation. In: Malan A, Canguilhem B (eds) Living in the cold colloque INSERM. John Libbey Eurotext, London, pp 43-51
44. Pévet P, Pitrosky B, Vuillez P, Jacob N, Teclemariam-Mesbah R, Kirsch R, Vivien-Roels B, Lakhdar-Ghazal N, Canguilhem B, Masson-Pévet M (1996) The suprachiasmatic nucleus: the biological clock of all seasons. Prog Brain Res 111:369-384
45. Pittendrigh CS, Daan S (1976) A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: a clock for all seasons. J Comp Physiol [A] 106:333-355
46. Pittendrigh CS, Minis DH (1964) The entrainment of circadian oscillations by light and their role as photoperiodic clocks. Am Nat 98:261-294
47. Pohl H (1985) The circadian system of the Turkish hamster, Mesocricetus brandti: responses to light. Comp Biochem Physiol A 81:613-618
48. Pohl H (1987) Circadian pacemaker does not arrest in deep hibernation. Evidence for desynchronization from the light cycle. Experientia 43:293-294
49. Puchalski W, Lynch GR (1986) Evidence for differences in the circadian organization of hamsters exposed to short day photoperiod. J Comp Physiol [A] 159:7-11
50. Puchalski W, Lynch GR (1991) Circadian characteristics of Djungarian hamsters: effects of photoperiodic pretreatment and artificial selection. Am J Physiol 261:R670-R676
51. Reiter RJ (1993) The melatonin rhythm: both a clock and a calendar. Experientia 49:654-664
52. Rollag MD, O'Callaghan PL, Niswender GD (1978) Serum melatonin concentrations during different stages of the annual reproductive cycle in ewes. Biol Reprod 18:279-285
53. Ružić A (1976) Some peculiarities in the hibernation of the hamster (Cricetus cricetus) and their importance for the control of that pest. Plant Protection (Beograd) 27:397-417
54. Saboureau M (1986) Hibernation in the hedgehog: influence of external and internal factors. In: Heller HC et al (ed) Living in the cold: physiological and biochemical adaptations. Elsevier, New York, pp 253-263
55. Saboureau M, Laurent G, Boissin J (1979) Daily and seasonal rhythms of locomotor activity and adrenal function in male hedgehogs (Erinaceus europaeus L.). J Interdiscipl Cycle Res 10:249-266
56. Saboureau M, Masson-Pévet M, Canguilhem B, Pévet P (1999) Circannual reproductive rhythm in the European hamster (Cricetus cricetus): demonstration of the existence of an annual phase of sensitivity to short photoperiod. J Pineal Res 26:9-16
57. Schwartz WJ, de la Iglesia HO, Zlomanczuk P, Illnerová H (2001) Encoding le quattro stagioni within the mammalian brain: photoperiodic orchestration through the suprachiasmatic nucleus. J Biol Rhythms 16:302-311
58. Spencer K (1986) Analytical reviews in clinical biochemistry: the estimate of creatinine. Ann Clin Biochem 23(Pt 1):1-25
59. Steinlechner S, Buchberger A, Heldmaier G (1987) Circadian rhythms of pineal N-acetyltransferase activity in the Djungarian hamster, Phodopus sungorus, in response to seasonal changes of natural photoperiod. J Comp Physiol [A] 160:593-597
60. Steinlechner S, Baumgartner I, Klante G, Reiter RJ (1995) Melatonin synthesis in the retina and pineal gland of Djungarian hamsters at different times of the year. Neurochem Int 27:245-251
61. Stieglitz A, Spiegelhalter F, Klante G, Heldmaier G (1995) Urinary 6-sulphatoxymelatonin excretion reflects pineal melatonin secretion in the Djungarian hamster (Phodopus sungorus). J Pineal Res 18:69-76
62. Sumová A, Trávníčková Z, Illnerová H (1995a) Memory on long but not on short days is stored in the rat suprachiasmatic nucleus. Neurosci Lett 200:191-194
63. Sumová A, Trávníčková Z, Peters R, Schwartz W, Illnerová H (1995b) The rat suprachiasmatic nucleus is a clock for all seasons. Proc Natl Acad Sci USA 92:7754-7758
64. Sumová A, Sládek M, Jáč M, Illnerová H (2002) The circadian rhythm of Perl gene product in the rat suprachiasmatic nucleus and its modulation by seasonal changes in daylength. Brain Res 947:260-270
65. Tournier BB, Menet JS, Dardente H, Poirel VJ, Malan A, Masson-Pévet M, Pévet P, Vuillez P (2003) Photoperiod differentially regulates clock genes' expression in the suprachiasmatic nucleus of Syrian hamster. Neuroscience 118:317-322
66. Turek FW, Gwinner E (1982) Role of hormones in the circadian organization of vertebrates. In: Aschoff J, Daan S, Groos GA (eds) Vertebrate circadian systems. Springer, Berlin Heidelberg New York, pp 173-182
67. Vieth E (1989) Fitting piecewise linear regression functions to biological responses. J Appl Physiol 67:390-396
68. Vivien-Roels B, Pévet P, Masson-Pévet M, Canguilhem B (1992) Seasonal variations in the daily rhythm of pineal gland and/or circulating melatonin and 5-methoxytryptophol concentrations in the European hamster, Cricetus cricetus. Gen Comp Endocrinol 86:239-247
69. Vivien-Roels B, Pitrosky B, Zitouni M, Malan A, Canguilhem B, Bonn D, Pévet P (1997) Environmental control of the seasonal variations in the daily pattern of melatonin synthesis in the European hamster, Cricetus cricetus. Gen Comp Endocrinol 106:85-94
70. Vohralík V (1974) Biology of the reproduction of the common hamster, Cricetus cricetus (L.). Věstník Č eskoslovenské Společnosti Zoologické 38:288-240
71. Vuillez P, Jacob N, Teclemariam-Mesbah R, Pévet P (1996) In Syrian and European hamsters, the duration of sensitive phase to light of the suprachiasmatic nuclei depends on the photoperiod. Neurosci Lett 208:37-40
72. Wollnik F, Schmidt B (1995) Seasonal and daily rhythms of body temperature in the European hamster (Cricetus cricetus) under semi-natural conditions. J Comp Physiol [B] 165:171-82
73. Wollnik F, Breit A, Reinke D (1991) Seasonal change in the temporal organization of wheel-running activity in the European hamster, Cricetus cricetus. Naturwissenschaften 78:419-422
74. Zucker I (1979) Hormones and hamster circadian organization. In: Suda M, Hayaishi O, Nakagawa H (eds) Biological rhythms and their central mechanisms. Elsevier/North-Holland Biomedical Press, Amsterdam, pp 369-381
75. Zucker I (2001) Circannual rhythms. In: Adler NT (ed) Handbook of behavioral neurobiology. Kluwer Academic/Plenum Publishers, New York, Boston, Dordrecht, London, Moscow, pp 509-528