Publication Cover
Chronobiology International
The Journal of Biological and Medical Rhythm Research
Volume 39, 2022 - Issue 12
1,334
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Dim light melatonin onset following simulated eastward travel is earlier in young males genotyped as PER35/5 than PER34/4

ORCID Icon, & ORCID Icon
Pages 1611-1623 | Received 26 Apr 2022, Accepted 18 Oct 2022, Published online: 02 Nov 2022

References

  • An H, Zhu Z, Zhou C, Geng P, Xu H, Wang H, Chen R, Qu X, Qian H, Gao Y, et al. 2014. Chronotype and a PERIOD3 variable number tandem repeat polymorphism in Han Chinese pilots. Int J Clin Exp Med. 7:3770–76.
  • Archer SN, Carpen JD, Gibson M, Lim GH, Johnston JD, Skene DJ, Von Schantz M. 2010. Polymorphism in the PER3 promoter associates with diurnal preference and delayed sleep phase disorder. Sleep. 33:695–701. doi:10.1093/sleep/33.5.695
  • Archer SN, Robilliard DL, Skene DJ, Smits M, Williams A, Arendt J, Von Schantz M. 2003. A length polymorphism in the circadian clock gene Per3 is linked to delayed sleep phase syndrome and extreme diurnal preference. Sleep. 26:413–15. doi:10.1093/sleep/26.4.413
  • Archer SN, Schmidt C, Vandewalle G, Dijk DJ. 2018. Phenotyping of PER3 variants reveals widespread effects on circadian preference, sleep regulation, and health. Sleep Med Rev. 40:109–26. doi:10.1016/j.smrv.2017.10.008
  • Archer SN, Viola AU, Kyriakopoulou V, Von Schantz M, Dijk DJ. 2008. Inter-individual differences in habitual sleep timing and entrained phase of endogenous circadian rhythms of BMAL1, PER2 and PER3 mRNA in human leukocytes. Sleep. 31:608–17. doi:10.1093/sleep/31.5.608
  • Arendt J. 2009. Managing jet lag: Some of the problems and possible new solutions. Sleep Med Rev. 13:249–56. doi:10.1016/j.smrv.2008.07.011
  • Arendt J. 2019. Melatonin: Countering Chaotic Time Cues. Front Endocrinol (Lausanne). 10:391. doi:10.3389/fendo.2019.00391
  • Bedini G, Bersano A, Sebastiano DR, Sattin D, Ciaraffa F, Tosetti V, Brenna G, Franceschetti S, Ciusani E, Leonardi M, et al. 2016. Is period3 genotype associated with sleep and recovery in patients with disorders of consciousness? Neurorehabil Neural Repair. 30:461–69. doi:10.1177/1545968315604398
  • Bin YS, Ledger S, Nour M, Postnova S, Stamatakis E, Cistulli PA, de Chazal P, Allman-Farinelli M, Caillaud C, Bauman A, et al. 2020. How do travelers manage jetlag and travel fatigue? A survey of passengers on long-haul flights. Chronobiol Int. 37:1621–28. doi:10.1080/07420528.2020.1787427
  • Bin YS, Postnova S, Cistulli PA. 2019. What works for jetlag? A systematic review of non-pharmacological interventions. Sleep Med Rev. 43:47–59. doi:10.1016/j.smrv.2018.09.005
  • Birch J. 1997. Efficiency of the Ishihara test for identifying red-green colour deficiency. Ophthalmic Physiol Opt. 17:403–08. doi:10.1016/S0275-5408(97)00022-7
  • Blume C, Garbazza C, Spitschan M. 2019. Effects of light on human circadian rhythms, sleep and mood. Somnologie. 23:147–56. doi:10.1007/s11818-019-00215-x
  • Burgess HJ, Fogg LF, Yamazaki S. 2008. Individual differences in the amount and timing of salivary melatonin secretion. PLoS One. 3:e3055. doi:10.1371/journal.pone.0003055
  • Burgess HJ, Savic N, Sletten T, Roach G, Gilbert SS, Dawson D. 2003. The relationship between the dim light melatonin onset and sleep on a regular schedule in young healthy adults. Behavioral Sleep Medicine. 1:102–14. doi:10.1207/S15402010BSM0102_3
  • Buysse DJ, Reynolds CF, Monk TH, Berman SR, Kupfer DJ. 1989. The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research. Psychiatry Res. 28:193–213. doi:10.1016/0165-1781(89)90047-4
  • Cajochen C, Khalsa SBS, Wyatt JK, Czeisler CA, Dijk DJ. 1999. EEG and ocular correlates of circadian melatonin phase and human performance decrements during sleep loss. Am J Physiol - Regul Integr Comp Physiol. 277:R640–9. doi:10.1152/ajpregu.1999.277.3.r640
  • Cedernaes J, Schiöth HB, Benedict C. 2015. Determinants of shortened, disrupted, and mistimed sleep and associated metabolic health consequences in healthy humans. Diabetes. 64:1073–80. doi:10.2337/db14-1475
  • Chellappa SL, Viola AU, Schmidt C, Bachmann V, Gabel V, Maire M, Reichert CF, Valomon A, Götz T, Landolt HP, et al. 2012. Human melatonin and alerting response to blue-enriched light depend on a polymorphism in the clock gene PER3. J Clin Endocrinol Metab. 97:E433–7. doi:10.1210/jc.2011-2391
  • Chellappa SL, Viola AU, Schmidt C, Bachmann V, Gabel V, Maire M, Reichert CF, Valomon A, Landolt HP, Cajochen C. 2014. Light modulation of human sleep depends on a polymorphism in the clock gene Period3. Behav Brain Res. 271:23–29. doi:10.1016/j.bbr.2014.05.050
  • Cingi C, Emre IE, Muluk NB. 2018. Jetlag related sleep problems and their management: A review. Travel Med Infect Dis. 24:59–64. doi:10.1016/j.tmaid.2018.05.008
  • Dagmura H, Yiǧit S, Nursal AF, Duman E, Gumusay O. 2021. Possible association of per2/per3 variable number tandem repeat polymorphism variants with susceptibility and clinical characteristics in Pancreatic Cancer. Genet Test Mol Biomarkers. 25:124–30. doi:10.1089/gtmb.2020.0179
  • Dijk DJ, Archer SN. 2010. PERIOD3, circadian phenotypes, and sleep homeostasis. Sleep Med Rev. 14:151–60. doi:10.1016/j.smrv.2009.07.002
  • Dijk DJ, Czeisler CA. 1994. Paradoxical timing of the circadian rhythm of sleep propensity serves to consolidate sleep and wakefulness in humans. Neurosci Lett. 166:63–68. doi:10.1016/0304-3940(94)90841-9
  • Drake CL, Belcher R, Howard R, Roth T, Levin AM, Gumenyuk V. 2015. Length polymorphism in the Period 3 gene is associated with sleepiness and maladaptive circadian phase in night-shift workers. J Sleep Res. 24:254–61. doi:10.1111/jsr.12264
  • Eastman CI, Gazda CJ, Burgess HJ, Crowley SJ, Fogg LF. 2005. Advancing circadian rhythms before eastward flight: A strategy to prevent or reduce jet lag. Sleep. 28:33–44. doi:10.1093/sleep/28.1.33
  • Eastman CI, Tomaka VA, Crowley SJ. (2016). Circadian rhythms of European and African-Americans after a large delay of sleep as in jet lag and night work. Sci Rep. 6:20–22. doi:10.1038/srep36716. Internet.
  • Ebisawa T, Uchiyama M, Kajimura N, Mishima K, Kamei Y, Katoh M, Watanabe T, Sekimoto M, Shibui K, Kim K, et al. 2001. Association of structural polymorphisms in the human period3 gene with delayed sleep phase syndrome. EMBO Rep. 2:342–46. doi:10.1093/embo-reports/kve070
  • Flynn-Evans EE, Shekleton JA, Miller B, Epstein LJ, Kirsch D, Brogna LA, Burke LM, Bremer E, Murray JM, Gehrman P, et al. 2017. Circadian phase and phase angle disorders in primary insomnia. Sleep. 40. doi:10.1093/sleep/zsx163
  • Goel N, Banks S, Mignot E, Dinges DF, Bartell PA. 2009. PER3 polymorphism predicts cumulative sleep homeostatic but not neurobehavioral changes to chronic partial sleep deprivation. PLoS One. 4:e5874. doi:10.1371/journal.pone.0005874
  • Gooley JJ, Chamberlain K, Smith KA, Khalsa SBS, Rajaratnam SMW, Van Reen E, Zeitzer JM, Czeisler CA, Lockley SW. 2011. Exposure to room light before bedtime suppresses melatonin onset and shortens melatonin duration in humans. J Clin Endocrinol Metab. 93:E463–E472. doi:10.1210/jc.2010-2098
  • Groeger JA, Viola AU, Lo JCY, Von Schantz M, Archer SN, Dijk DJ. 2008. Early morning executive functioning during sleep deprivation is compromised by a PERIOD3 polymorphism. Sleep. 31:1159–67. doi:10.5665/sleep/31.8.1159
  • Hida A, Kitamura S, Katayose Y, Kato M, Ono H, Kadotani H, Uchiyama M, Ebisawa T, Inoue Y, Kamei Y, et al. 2014. Screening of clock gene polymorphisms demonstrates association of a PER3 polymorphism with morningness-eveningness preference and circadian rhythm sleep disorder. Sci Rep. 4:1–6. doi:10.1038/srep06309
  • Hoddes E, Dement W, Zarcone V. 1972. The development and use of the Stanford sleepiness scale (SSS). Psychophysiology. 369–70. https://doi.org/10.1007/978-1-4419-9893-4_91
  • Horne JA, Ostberg O. 1976. A self assessment questionnaire to determine Morningness Eveningness in human circadian rhythms. Int J Chronobiol. 4:97–110.
  • Janse Van Rensburg DC, Fowler P, Racinais S. 2020a. Practical tips to manage travel fatigue and jet lag in athletes. Br J Sports Med. 55:821–22. doi:10.1136/bjsports-2020-103163
  • Janse Van Rensburg DC, Jansen Van Rensburg A, Fowler P, Fullagar H, Stevens D, Halson S, Bender A, Vincent G, Claassen-Smithers A, Dunican I, et al. 2020b. How to manage travel fatigue and jet lag in athletes? A systematic review of interventions. Br J Sports Med. 0:1–11. doi:10.1136/bjsports-2019-101635.
  • Keijzer H, Smits MG, Peeters T, Looman CW, Endenburg SC, Gunnewiek JM. 2011. Evaluation of salivary melatonin measurements for Dim Light Melatonin Onset calculations in patients with possible sleep-wake rhythm disorders. Clin Chim Acta. 412:1616–20. doi:10.1016/j.cca.2011.05.014
  • Kennaway DJ. 2020. Kennaway DJ measuring melatonin by immunoassay. J Pineal Res. 69:e12657. doi:10.1111/jpi.12657
  • Knutson KL, Spiegel K, Penev P, Van Cauter E. 2007. The metabolic consequences of sleep deprivation. Sleep Med Rev. 11:163–78. doi:10.1016/j.smrv.2007.01.002
  • Kölling S, Treff G, Winkert K, Ferrauti A, Meyer T, Pfeiffer M, Kellmann M. 2017. The effect of westward travel across five time zones on sleep and subjective jet-lag ratings in athletes before and during the 2015ʹs World Rowing Junior Championships. J Sports Sci. 35:2240–48. doi:10.1080/02640414.2016.1265141
  • Kozaki T, Lee S, Nishimura T, Katsuura T, Yasukouchi A. 2011. Effects of saliva collection using cotton swabs on melatonin enzyme immunoassay. Journal of Circadian Rhythms. 9:1. doi:10.1186/1740-3391-9-1
  • Kunorozva L, Stephenson KJ, Rae DE, Roden LC. 2012. Chronotype and PERIOD3 variable number tandem repeat polymorphism in individual sports athletes. Chronobiol Int. 29:1004–10. doi:10.3109/07420528.2012.719966
  • Lavie P. 1986. Ultrashort sleep-waking schedule. III. “Gates” and “Forbidden zones” for sleep. Electroencephalogr Clin Neurophysiol. 63:414–25. doi:10.1016/0013-4694(86)90123-9
  • Lavric A, Pompe MT. 2014. Do blue-light filtering intraocular lenses affect visual function? Optom Vis Sci. 91:1348–54. doi:10.1097/OPX.0000000000000390
  • Lázár AS, Slak A, JCY L, Santhi N, Von Schantz M, Archer SN, Groeger JA, Dijk DJ. 2012. Sleep, diurnal preference, health, and psychological well-being: A prospective single-allelic-variation study. Chronobiol Int. 29:131–46. doi:10.3109/07420528.2011.641193
  • Lee A, Galvez JC. 2012. Jet lag in athletes. Sports Health. 4:211–16. doi:10.1177/1941738112442340
  • Lo JC, Groeger JA, Santhi N, Arbon EL, Lazar AS, Hasan S, von Schantz M, Archer SN, Dijk DJ, Yamazaki S. 2012. Effects of partial and acute total sleep deprivation on performance across cognitive domains. Individuals and Circadian Phase PLoS One. 7:e45987. doi:10.1371/journal.pone.0045987
  • Lok R, Kchj S, Beersma DGM, de Kort Yaw, de Kort YAW. 2018. Light, alertness, and alerting effects of white light: A literature overview. J Biol Rhythms. 33:589–601. doi:10.1177/0748730418796443
  • Maire M, Reichert CF, Gabel V, Viola AU, Krebs J, Strobel W, Landolt HP, Bachmann V, Cajochen C, Schmidt C. 2014a. Time-on-task decrement in vigilance is modulated by inter-individual vulnerability to homeostatic sleep pressure manipulation. Front Behav Neurosci. 8:1–10. doi:10.3389/fnbeh.2014.00059
  • Maire M, Reichert CF, Gabel V, Viola AU, Strobel W, Krebs J, Landolt HP, Bachmann V, Cajochen C, Schmidt C. 2014b. Sleep ability mediates individual differences in the vulnerability to sleep loss: Evidence from a PER3 polymorphism. Cortex. 52:47–59. doi:10.1016/j.cortex.2013.11.008
  • Micic G, Lovato N, Gradisar M, Burgess HJ, Ferguson SA, Kennaway DJ, Lack L. 2015. Nocturnal melatonin profiles in patients with delayed sleep-wake phase disorder and control sleepers. J Biol Rhythms. 30:437–48. doi:10.1177/0748730415591753
  • Moline ML, Pollak CP, Monk TH, Lester LS, Wagner DR, Zendell SM, Graeber RC, Salter CA, Hirsch E. 1992. Age-related differences in recovery from simulated jet lag. Sleep. 15:28–40. doi:10.1093/sleep/15.1.28
  • Mongrain V, Carrier J, Dumont M. 2006. Circadian and homeostatic sleep regulation in morningness-eveningness. J Sleep Res. 15:162–66. doi:10.1111/j.1365-2869.2006.00532.x
  • Monk TH, Buysse DJ, Kennedy KS, Potts JM, DeGrazia JM, Miewald JM. 2003. Measuring sleep habits without using a diary: The sleep timing questionnaire. Sleep. 26:208–12. doi:10.1093/sleep/26.2.208
  • Nadkarni NA, Weale ME, Von Schantz M, Thomas MG. 2005. Evolution of a length polymorphism in the human PER3 gene, a component of the circadian system. J Biol Rhythms. 20:490–99. doi:10.1177/0748730405281332
  • Ozsoy F, Yigit S, Nursal AF, Kulu M, Nevin K. 2021. The impact of PER3 VNTR polymorphism on the development of schizophrenia in a Turkish population. Cytol Genet. 55:188–93. doi:10.1242/dev.157966
  • Pereira DS, Tufik S, Louzada FM, Benedito-Silva AA, Lopez AR, Lemos NA, Korczak AL, D’Almeida V, Pedrazzoli M. 2005. Association of the length polymorphism in the human Per3 gene with the delayed sleep-phase syndrome: Does latitude have an influence upon it? Sleep. 28:29–32. doi:10.1093/sleep/28.1.29
  • Phillips AJK, Vidafar P, Burns AC, McGlashan EM, Anderson C, Rajaratnam SMW, Lockley SW, Cain SW. 2019. High sensitivity and interindividual variability in the response of the human circadian system to evening light. Proc Natl Acad Sci U S A. 116:12019–24. doi:10.1073/pnas.1901824116
  • Qian J, Fajl S. 2016. Circadian system and glucose metabolism: Implications for physiology and disease. Trends Endocrinol Metab. 27:282–93. doi:10.1016/j.tem.2016.03.005
  • Rajaratnam SMW, Middleton B, Stone BM, Arendt J, Dijk DJ. 2004. Melatonin advances the circadian timing of EEG sleep and directly facilitates sleep without altering its duration in extended sleep opportunities in humans. J Physiol. 561:339–51. doi:10.1113/jphysiol.2004.073742
  • Revell VL, Kim H, Tseng CY, Crowley SJ, Eastman CI. 2005. Circadian phase determined from melatonin profiles is reproducible after 1 wk in subjects who sleep later on weekends. J Pineal Res. 39:195–200. doi:10.1111/j.1600-079X.2005.00236.x
  • Roach GD, Sargent C. 2019. Interventions to minimize jet lag after westward and eastward flight. Front Physiol. 10:1–11. doi:10.3389/fphys.2019.00927
  • Ruderman NB, Saha AK. 2006. Metabolic syndrome: Adenosine monophosphate-activated protein kinase and malonyl coenzyme A. Obesity (Silver Spring). Suppl 14:25S–33S. doi:10.1038/oby.2006.279
  • Rüger M, St Hilaire MA, Brainard GC, Khalsa SBS, Kronauer RE, Czeisler CA, Lockley SW. 2013. Human phase response curve to a single 6.5 h pulse of short-wavelength light. J Physiol. 591:353–63. doi:10.1113/jphysiol.2012.239046
  • Sletten TL, Segal AY, Flynn-Evans EE, Lockley SW, Rajaratnam SMW. (2015). Inter-individual differences in neurobehavioural impairment following sleep restriction are associated with circadian rhythm phase. PLoS One [Internet]. 10:1–16. doi:10.1371/journal.pone.0128273
  • Sletten TL, Vincenzi S, Redman JR, Lockley SW, Rajaratnam SM. 2010. Timing of sleep and its relationship with the endogenous melatonin rhythm. Front Neurol. 1:137. doi:10.3389/fneur.2010.00137
  • Smith MR, Eastman CI. 2009. Phase delaying the human circadian clock with blue-enriched polychromatic light. Chronobiol Int. 26:709–25. doi:10.1080/07420520902927742
  • Smith MR, Revell VL, Eastman CI. 2009. Phase advancing the human circadian clock with blue-enriched polychromatic light. Sleep Med. 10:287–94. doi:10.1016/j.sleep.2008.05.005
  • Spiegel K, Knutson K, Leproult R, Tasali E, Van Cauter E. 2005. Sleep loss: A novel risk factor for insulin resistance and Type 2 diabetes. J Appl Physiol. 99:2008–19. doi:10.1152/japplphysiol.00660.2005
  • Taillard J, Philip P, Coste O, Sagaspe P, Bioulac B. 2003. The circadian and homeostatic modulation of sleep pressure during wakefulness differs between morning and evening chronotypes. J Sleep Res. 12:275–82. doi:10.1046/j.0962-1105.2003.00369.x
  • Tasali E, Leproult R, Ehrmann DA, Van Cauter E. 2008. Slow-wave sleep and the risk of type 2 diabetes in humans. Proc Natl Acad Sci U S A. 105:1044–49. doi:10.1073/pnas.0706446105
  • Vandewalle G, Archer SN, Wuillaume C, Balteau E, Degueldre C, Luxen A, Dijk DJ, Maquet P. 2011. Effects of light on cognitive brain responses depend on circadian phase and sleep homeostasis. J Biol Rhythms. 26:249–59. doi:10.1177/0748730411401736
  • Van Dongen HPA, Bender AM, Dinges DF. 2012. Systematic individual differences in sleep homeostatic and circadian rhythm contributions to neurobehavioral impairment during sleep deprivation. Accid Anal Prev. 45:11–16. doi:10.1016/j.aap.2011.09.018
  • Viola AU, Archer SN, James LMM, Groeger JA, Lo JCY, Skene DJ, von Schantz M, Dijk DJ. 2007. PER3 polymorphism predicts sleep structure and waking performance. Curr Biol. 17:613–18. doi:10.1016/j.cub.2007.01.073
  • Viola AU, Chellappa SL, Archer SN, Pugin F, Götz T, Dijk DJ, Cajochen C. 2012. Interindividual differences in circadian rhythmicity and sleep homeostasis in older people: Effect of a PER3 polymorphism. Neurobiol Aging. 33:1010.e17–27. doi:10.1016/j.neurobiolaging.2011.10.024
  • Voinescu BI, Coogan AN. 2012. A variable-number tandem repeat polymorphism in PER3 is not associated with chronotype in a population with self-reported sleep problems. Sleep Biol Rhythms. 10:23–26. doi:10.1111/j.1479-8425.2011.00514.x
  • Waterhouse J, Reilly T, Atkinson G, Edwards B. 2007. Jet lag: Trends and coping strategies. Lancet. 369:1117–29. doi:10.1016/S0140-6736(07)60529-7
  • Watson LA, Phillips AJK, Hosken IT, McGlashan EM, Anderson C, Lack LC, Lockley SW, Rajaratnam SMW, Cain SW. 2018. Increased sensitivity of the circadian system to light in delayed sleep–wake phase disorder. J Physiol. 596:6249–61. doi:10.1113/JP275917
  • Wehr TA, Aeschbach D, Duncan J. 2001. Evidence for a biological Dawn and dusk in the human circadian timing system. J Physiol. 535:937–51. doi:10.1111/j.1469-7793.2001.t01-1-00937.x
  • Weingarten JA, Collop NA. 2013. Air travel: Effects of sleep deprivation and jet lag. Chest. 144:1394–401. doi:10.1378/chest.12-2963
  • Wen B, He M, Song J, Zong B, Lu Y, Shu X. 2000. Study on DeNOx performance of Ce-Mg-Al mixed oxides. Chinese J Catal. 21:34.
  • Winget CM, Deroshia CW, Markley CL, Holley DC. 1984. A review of human physiological and performance changes associated with desynchronosis of biological rhythms. Aviat Sp Environ Med. 55:1086–96.
  • Wirth M, Burch J, Violanti J, Burchfiel C, Fekedulegn D, Andrew M, Zhang H, Miller DB, Youngstedt SD, Hébert JR, et al. 2013. Association of the period3 clock gene length polymorphism with salivary cortisol secretion among police officers. Neuro Endocrinol Lett. 34:27–37.
  • World Medical Association 2013. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 310:2191–2194. doi:10.1001/jama.2013.281053.
  • Wright KP, Drake AL, Frey DJ, Fleshner M, Desouza CA, Gronfier C, Czeisler CA. 2015. Influence of sleep deprivation and circadian misalignment on cortisol, inflammatory markers, and cytokine balance. Brain Behav Immun. 47:24–34. doi:10.1016/j.bbi.2015.01.004
  • Wright HR, Lack LC, Kennaway DJ. 2004. Differential effects of light wavelength in phase advancing the melatonin rhythm. J Pineal Res. 36:140–44. doi:10.1046/j.1600-079X.2003.00108.x
  • Zacharko M, Konefał M, Ł R, Chmura P, Błażejczyk K, Chmura J, Andrzejewski M. 2020. Direction of travel of time zones crossed and results achieved by soccer players. The road from the 2018 FIFA world cup to UEFA EURO 2020. Res Sport Med. 30:145–55. doi:10.1080/15438627.2020.1853545