Advertisement

Neuroscience Bulletin

, Volume 33, Issue 1, pp 62–72 | Cite as

A New Perspective for Parkinson’s Disease: Circadian Rhythm

  • Siyue Li
  • Yali Wang
  • Fen Wang
  • Li-Fang Hu
  • Chun-Feng LiuEmail author
Review

Abstract

Circadian rhythm is manifested by the behavioral and physiological changes from day to night, which is controlled by the pacemaker and its regulator. The former is located at the suprachiasmatic nuclei (SCN) in the anterior hypothalamus, while the latter is composed of clock genes present in all tissues. Circadian desynchronization influences normal patterns of day-night rhythms such as sleep and alertness cycles, rest and activity cycles. Parkinson’s disease (PD) exhibits diurnal fluctuations. Circadian dysfunction has been observed in PD patients and animal models, which may result in negative consequences to the homeostasis and even exacerbate the disease progression. Therefore, circadian therapies, including light stimulation, physical activity, dietary and social schedules, may be helpful for PD patients. However, the cellular and molecular mechanisms that underlie the circadian dysfunction in PD remain elusive. Further research on circadian patterns is needed. This article summarizes the existing research on the circadian rhythms in PD, focusing on the clinical symptom variations, molecular changes, as well as the available treatment options.

Keywords

Parkinson’s disease Circadian rhythm Sleep Dopamine 

Notes

Acknowledgements

This review was supported by the National Natural Science Foundation of China (81471299), Jiangsu Provincial Special Program of Medical Science (BL2014042), Suzhou Clinical Key Disease Diagnosis and Treatment Technology Foundation (LCZX201304), the Plans for Graduate Research and Innovation in Colleges and Universities of Jiangsu Province, China (KYZZ15_0334) and Suzhou Medical Key Discipline Project, the Priority Academic Program Development of Jiangsu Higher Education Institutions, China (PAPD) and Suzhou Clinical Research Center of Neurological Disease (Szzx201503).

References

  1. 1.
    Pringsheim T, Jette N, Frolkis A, Steeves TD. The prevalence of Parkinson’s disease: a systematic review and meta-analysis. Mov Disord 2014, 29: 1583–1590.PubMedCrossRefGoogle Scholar
  2. 2.
    Boeve BF. REM sleep behavior disorder: Updated review of the core features, the REM sleep behavior disorder-neurodegenerative disease association, evolving concepts, controversies, and future directions. Ann N Y Acad Sci 2010, 1184: 15–54.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 2003, 24: 197–211.PubMedCrossRefGoogle Scholar
  4. 4.
    McClung CA, Sidiropoulou K, Vitaterna M, Takahashi JS, White FJ, Cooper DC, et al. Regulation of dopaminergic transmission and cocaine reward by the Clock gene. Proc Natl Acad Sci U S A 2005, 102: 9377–9381.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Kawarai T, Kawakami H, Yamamura Y, Nakamura S. Structure and organization of the gene encoding human dopamine transporter. Gene 1997, 195: 11–18.PubMedCrossRefGoogle Scholar
  6. 6.
    Mukherjee S, Coque L, Cao JL, Kumar J, Chakravarty S, Asaithamby A, et al. Knockdown of Clock in the ventral tegmental area through RNA interference results in a mixed state of mania and depression-like behavior. Biol Psychiatry 2010, 68: 503–511.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Imbesi M, Yildiz S, Dirim Arslan A, Sharma R, Manev H, Uz T. Dopamine receptor-mediated regulation of neuronal “clock” gene expression. Neuroscience 2009, 158: 537–544.PubMedCrossRefGoogle Scholar
  8. 8.
    Yujnovsky I, Hirayama J, Doi M, Borrelli E, Sassone-Corsi P. Signaling mediated by the dopamine D2 receptor potentiates circadian regulation by CLOCK:BMAL1. Proc Natl Acad Sci U S A 2006, 103: 6386–6391.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Hood S, Cassidy P, Cossette MP, Weigl Y, Verwey M, Robinson B, et al. Endogenous dopamine regulates the rhythm of expression of the clock protein PER2 in the rat dorsal striatum via daily activation of D2 dopamine receptors. J Neurosci 2010, 30: 14046–14058.PubMedCrossRefGoogle Scholar
  10. 10.
    Kovacikova Z, Sladek M, Bendova Z, Illnerova H, Sumova A. Expression of clock and clock-driven genes in the rat suprachiasmatic nucleus during late fetal and early postnatal development. J Biol Rhythms 2006, 21: 140–148.PubMedCrossRefGoogle Scholar
  11. 11.
    Seron-Ferre M, Mendez N, Abarzua-Catalan L, Vilches N, Valenzuela FJ, Reynolds HE, et al. Circadian rhythms in the fetus. Mol Cell Endocrinol 2012, 349: 68–75.PubMedCrossRefGoogle Scholar
  12. 12.
    Torres-Farfan C, Rocco V, Monso C, Valenzuela FJ, Campino C, Germain A, et al. Maternal melatonin effects on clock gene expression in a nonhuman primate fetus. Endocrinology 2006, 147: 4618–4626.PubMedCrossRefGoogle Scholar
  13. 13.
    Gonzalez S, Moreno-Delgado D, Moreno E, Perez-Capote K, Franco R, Mallol J, et al. Circadian-related heteromerization of adrenergic and dopamine D(4) receptors modulates melatonin synthesis and release in the pineal gland. PLoS Biol 2012, 10: e1001347.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Mistlberger RE. Circadian regulation of sleep in mammals: role of the suprachiasmatic nucleus. Brain Res Brain Res Rev 2005, 49: 429–454.PubMedCrossRefGoogle Scholar
  15. 15.
    Barone P, Antonini A, Colosimo C, Marconi R, Morgante L, Avarello TP, et al. The PRIAMO study: A multicenter assessment of nonmotor symptoms and their impact on quality of life in Parkinson’s disease. Mov Disord 2009, 24: 1641–1649.PubMedCrossRefGoogle Scholar
  16. 16.
    Lee MA, Prentice WM, Hildreth AJ, Walker RW. Measuring symptom load in Idiopathic Parkinson’s disease. Parkinsonism Relat Disord 2007, 13: 284–289.PubMedCrossRefGoogle Scholar
  17. 17.
    Martinez-Martin P, Schapira AH, Stocchi F, Sethi K, Odin P, MacPhee G, et al. Prevalence of nonmotor symptoms in Parkinson’s disease in an international setting; study using nonmotor symptoms questionnaire in 545 patients. Mov Disord 2007, 22: 1623–1629.PubMedCrossRefGoogle Scholar
  18. 18.
    van Hilten B, Hoff JI, Middelkoop HA, van der Velde EA, Kerkhof GA, Wauquier A, et al. Sleep disruption in Parkinson’s disease. Assessment by continuous activity monitoring. Arch Neurol 1994, 51: 922–928.PubMedCrossRefGoogle Scholar
  19. 19.
    Kurtis MM, Rodriguez-Blazquez C, Martinez-Martin P, Group E. Relationship between sleep disorders and other non-motor symptoms in Parkinson’s disease. Parkinsonism Relat Disord 2013, 19: 1152–1155.CrossRefGoogle Scholar
  20. 20.
    Happe S, Schrodl B, Faltl M, Muller C, Auff E, Zeitlhofer J. Sleep disorders and depression in patients with Parkinson’s disease. Acta Neurol Scand 2001, 104: 275–280.PubMedCrossRefGoogle Scholar
  21. 21.
    Chahine LM, Daley J, Horn S, Duda JE, Colcher A, Hurtig H, et al. Association between dopaminergic medications and nocturnal sleep in early-stage Parkinson’s disease. Parkinsonism Relat Disord 2013, 19: 859–863.PubMedCrossRefGoogle Scholar
  22. 22.
    Suzuki K, Miyamoto M, Miyamoto T, Iwanami M, Hirata K. Sleep disturbances associated with Parkinson’s disease. Parkinsons Dis 2011, 2011: 219056.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Tan EK, Lum SY, Fook-Chong SM, Teoh ML, Yih Y, Tan L, et al. Evaluation of somnolence in Parkinson’s disease: comparison with age- and sex-matched controls. Neurology 2002, 58: 465–468.PubMedCrossRefGoogle Scholar
  24. 24.
    Tholfsen LK, Larsen JP, Schulz J, Tysnes OB, Gjerstad MD. Development of excessive daytime sleepiness in early Parkinson disease. Neurology 2015, 85: 162–168.PubMedCrossRefGoogle Scholar
  25. 25.
    Yi PL, Tsai CH, Lu MK, Liu HJ, Chen YC, Chang FC. Interleukin-1beta mediates sleep alteration in rats with rotenone-induced parkinsonism. Sleep 2007, 30: 413–425.PubMedGoogle Scholar
  26. 26.
    Lu CY, Yi PL, Tsai CH, Cheng CH, Chang HH, Hsiao YT, et al. TNF-NF-kappaB signaling mediates excessive somnolence in hemiparkinsonian rats. Behav Brain Res 2010, 208: 484–496.PubMedCrossRefGoogle Scholar
  27. 27.
    Videnovic A, Golombek D. Circadian and sleep disorders in Parkinson’s disease. Exp Neurol 2013, 243: 45–56.PubMedCrossRefGoogle Scholar
  28. 28.
    Claassen DO, Josephs KA, Ahlskog JE, Silber MH, Tippmann-Peikert M, Boeve BF. REM sleep behavior disorder preceding other aspects of synucleinopathies by up to half a century. Neurology 2010, 75: 494–499.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Postuma RB, Gagnon JF, Vendette M, Fantini ML, Massicotte-Marquez J, Montplaisir J. Quantifying the risk of neurodegenerative disease in idiopathic REM sleep behavior disorder. Neurology 2009, 72: 1296–1300.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Sorensen GL, Mehlsen J, Jennum P. Reduced sympathetic activity in idiopathic rapid-eye-movement sleep behavior disorder and Parkinson’s disease. Auton Neurosci 2013, 179: 138–141.PubMedCrossRefGoogle Scholar
  31. 31.
    Vendette M, Gagnon JF, Decary A, Massicotte-Marquez J, Postuma RB, Doyon J, et al. REM sleep behavior disorder predicts cognitive impairment in Parkinson disease without dementia. Neurology 2007, 69: 1843–1849.PubMedCrossRefGoogle Scholar
  32. 32.
    Postuma RB, Bertrand JA, Montplaisir J, Desjardins C, Vendette M, Rios Romenets S, et al. Rapid eye movement sleep behavior disorder and risk of dementia in Parkinson’s disease: a prospective study. Mov Disord 2012, 27: 720–726.PubMedCrossRefGoogle Scholar
  33. 33.
    Luppi PH, Clement O, Valencia Garcia S, Brischoux F, Fort P. New aspects in the pathophysiology of rapid eye movement sleep behavior disorder: the potential role of glutamate, gamma-aminobutyric acid, and glycine. Sleep Med 2013, 14: 714–718.PubMedCrossRefGoogle Scholar
  34. 34.
    Vilas D, Iranzo A, Tolosa E, Aldecoa I, Berenguer J, Vilaseca I, et al. Assessment of alpha-synuclein in submandibular glands of patients with idiopathic rapid-eye-movement sleep behaviour disorder: a case-control study. Lancet Neurol 2016, 15: 708–718.PubMedCrossRefGoogle Scholar
  35. 35.
    Barraud Q, Lambrecq V, Forni C, McGuire S, Hill M, Bioulac B, et al. Sleep disorders in Parkinson’s disease: the contribution of the MPTP non-human primate model. Exp Neurol 2009, 219: 574–582.PubMedCrossRefGoogle Scholar
  36. 36.
    Verhave PS, Jongsma MJ, Van den Berg RM, Vis JC, Vanwersch RA, Smit AB, et al. REM sleep behavior disorder in the marmoset MPTP model of early Parkinson disease. Sleep 2011, 34: 1119–1125.PubMedPubMedCentralGoogle Scholar
  37. 37.
    van Hilten JJ, Hoogland G, van der Velde EA, Middelkoop HA, Kerkhof GA, Roos RA. Diurnal effects of motor activity and fatigue in Parkinson’s disease. J Neurol Neurosurg Psychiatry 1993, 56: 874–877.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    van Hilten JJ, Middelkoop HA, Kerkhof GA, Roos RA. A new approach in the assessment of motor activity in Parkinson’s disease. J Neurol Neurosurg Psychiatry 1991, 54: 976–979.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Niwa F, Kuriyama N, Nakagawa M, Imanishi J. Circadian rhythm of rest activity and autonomic nervous system activity at different stages in Parkinson’s disease. Auton Neurosci 2011, 165: 195–200.PubMedCrossRefGoogle Scholar
  40. 40.
    Pan W, Kwak S, Li F, Wu C, Chen Y, Yamamoto Y, et al. Actigraphy monitoring of symptoms in patients with Parkinson’s disease. Physiol Behav 2013, 119: 156–160.PubMedCrossRefGoogle Scholar
  41. 41.
    Bonuccelli U, Del Dotto P, Lucetti C, Petrozzi L, Bernardini S, Gambaccini G, et al. Diurnal motor variations to repeated doses of levodopa in Parkinson’s disease. Clin Neuropharmacol 2000, 23: 28–33.PubMedCrossRefGoogle Scholar
  42. 42.
    Nutt JG, Carter JH, Lea ES, Woodward WR. Motor fluctuations during continuous levodopa infusions in patients with Parkinson’s disease. Mov Disord 1997, 12: 285–292.PubMedCrossRefGoogle Scholar
  43. 43.
    Piccini P, Del Dotto P, Pardini C, D’Antonio P, Rossi G, Bonuccelli U. Diurnal worsening in Parkinson patients treated with levodopa. Riv Neurol 1991, 61: 219–224.PubMedGoogle Scholar
  44. 44.
    Baier PC, Branisa P, Koch R, Schindehutte J, Paulus W, Trenkwalder C. Circadian distribution of motor-activity in unilaterally 6-hydroxy-dopamine lesioned rats. Exp Brain Res 2006, 169: 283–288.PubMedCrossRefGoogle Scholar
  45. 45.
    Kudo T, Loh DH, Truong D, Wu Y, Colwell CS. Circadian dysfunction in a mouse model of Parkinson’s disease. Exp Neurol 2011, 232: 66–75.PubMedCrossRefGoogle Scholar
  46. 46.
    Monville C, Torres EM, Pekarik V, Lane EL, Dunnett SB. Genetic, temporal and diurnal influences on L-dopa-induced dyskinesia in the 6-OHDA model. Brain Res Bull 2009, 78: 248–253.PubMedCrossRefGoogle Scholar
  47. 47.
    Tong J, Qin LQ, Wang DJ. Mechanism of pineal and suprachiasmatic regulation on circadian rhythm of body temperature in rats. Space Med Med Eng (Beijing) 2000, 13: 101–103.Google Scholar
  48. 48.
    Zhong G, Bolitho S, Grunstein R, Naismith SL, Lewis SJ. The relationship between thermoregulation and REM sleep behaviour disorder in Parkinson’s disease. PLoS One 2013, 8: e72661.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Cagnacci A, Bonuccelli U, Melis GB, Soldani R, Piccini P, Napolitano A, et al. Effect of naloxone on body temperature in postmenopausal women with Parkinson’s disease. Life Sci 1990, 46: 1241–1247.PubMedCrossRefGoogle Scholar
  50. 50.
    Suzuki K, Miyamoto T, Miyamoto M, Kaji Y, Takekawa H, Hirata K. Circadian variation of core body temperature in Parkinson disease patients with depression: a potential biological marker for depression in Parkinson disease. Neuropsychobiology 2007, 56: 172–179.PubMedCrossRefGoogle Scholar
  51. 51.
    Lax P, Esquiva G, Esteve-Rudd J, Otalora BB, Madrid JA, Cuenca N. Circadian dysfunction in a rotenone-induced parkinsonian rodent model. Chronobiol Int 2012, 29: 147–156.PubMedCrossRefGoogle Scholar
  52. 52.
    Rango M, Arighi A, Bonifati C, Bresolin N. Increased brain temperature in Parkinson’s disease. Neuroreport 2012, 23: 129–133.PubMedCrossRefGoogle Scholar
  53. 53.
    Sumida K, Sato N, Ota M, Sakai K, Nippashi Y, Sone D, et al. Intraventricular cerebrospinal fluid temperature analysis using MR diffusion-weighted imaging thermometry in Parkinson’s disease patients, multiple system atrophy patients, and healthy subjects. Brain Behav 2015, 5: e00340.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Ejaz AA, Sekhon IS, Munjal S. Characteristic findings on 24-h ambulatory blood pressure monitoring in a series of patients with Parkinson’s disease. Eur J Intern Med 2006, 17: 417–420.PubMedCrossRefGoogle Scholar
  55. 55.
    Schmidt C, Berg D, Herting, Prieur S, Junghanns S, Schweitzer K, et al. Loss of nocturnal blood pressure fall in various extrapyramidal syndromes. Mov Disord 2009, 24: 2136–2142.PubMedCrossRefGoogle Scholar
  56. 56.
    Berganzo K, Diez-Arrola B, Tijero B, Somme J, Lezcano E, Llorens V, et al. Nocturnal hypertension and dysautonomia in patients with Parkinson’s disease: are they related? J Neurol 2013, 260: 1752–1756.PubMedCrossRefGoogle Scholar
  57. 57.
    Kallio M, Haapaniemi T, Turkka J, Suominen K, Tolonen U, Sotaniemi K, et al. Heart rate variability in patients with untreated Parkinson’s disease. Eur J Neurol 2000, 7: 667–672.PubMedCrossRefGoogle Scholar
  58. 58.
    Devos D, Kroumova M, Bordet R, Vodougnon H, Guieu JD, Libersa C, et al. Heart rate variability and Parkinson’s disease severity. J Neural Transm (Vienna) 2003, 110: 997–1011.CrossRefGoogle Scholar
  59. 59.
    Harnod D, Wen SH, Chen SY, Harnod T. The association of heart rate variability with parkinsonian motor symptom duration. Yonsei Med J 2014, 55: 1297–1302.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Salsone M, Vescio B, Fratto A, Sturniolo M, Arabia G, Gambardella A, et al. Cardiac sympathetic index identifies patients with Parkinson’s disease and REM behavior disorder. Parkinsonism Relat Disord 2016, 26: 62–66.PubMedCrossRefGoogle Scholar
  61. 61.
    Boulamery A, Simon N, Vidal J, Bruguerolle B. Effects of L-dopa on circadian rhythms of 6-OHDA striatal lesioned rats: a radiotelemetric study. Chronobiol Int 2010, 27: 251–264.PubMedCrossRefGoogle Scholar
  62. 62.
    McDonald C, Newton JL, Burn DJ. Orthostatic hypotension and cognitive impairment in Parkinson’s disease: Causation or association? Mov Disord 2016, 31: 937–946.PubMedCrossRefGoogle Scholar
  63. 63.
    McMahon DG, Iuvone PM, Tosini G. Circadian organization of the mammalian retina: from gene regulation to physiology and diseases. Prog Retin Eye Res 2014, 39: 58–76.PubMedCrossRefGoogle Scholar
  64. 64.
    Witkovsky P. Dopamine and retinal function. Doc Ophthalmol 2004, 108: 17–40.PubMedCrossRefGoogle Scholar
  65. 65.
    Struck LK, Rodnitzky RL, Dobson JK. Circadian fluctuations of contrast sensitivity in Parkinson’s disease. Neurology 1990, 40: 467–470.PubMedCrossRefGoogle Scholar
  66. 66.
    Van Hook MJ, Wong KY, Berson DM. Dopaminergic modulation of ganglion-cell photoreceptors in rat. Eur J Neurosci 2012, 35: 507–518.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Ruan GX, Allen GC, Yamazaki S, McMahon DG. An autonomous circadian clock in the inner mouse retina regulated by dopamine and GABA. PLoS Biol 2008, 6: e249.PubMedCrossRefGoogle Scholar
  68. 68.
    Garfinkel D, Laudon M, Zisapel N. Improvement of sleep quality by controlled-release melatonin in benzodiazepine-treated elderly insomniacs. Arch Gerontol Geriatr 1997, 24: 223–231.PubMedCrossRefGoogle Scholar
  69. 69.
    Fertl E, Auff E, Doppelbauer A, Waldhauser F. Circadian secretion pattern of melatonin in Parkinson’s disease. J Neural Transm Park Dis Dement Sect 1991, 3: 41–47.PubMedCrossRefGoogle Scholar
  70. 70.
    Fertl E, Auff E, Doppelbauer A, Waldhauser F. Circadian secretion pattern of melatonin in de novo parkinsonian patients: evidence for phase-shifting properties of L-dopa. J Neural Transm Park Dis Dement Sect 1993, 5: 227–234.PubMedCrossRefGoogle Scholar
  71. 71.
    Bordet R, Devos D, Brique S, Touitou Y, Guieu JD, Libersa C, et al. Study of circadian melatonin secretion pattern at different stages of Parkinson’s disease. Clin Neuropharmacol 2003, 26: 65–72.PubMedCrossRefGoogle Scholar
  72. 72.
    Bolitho SJ, Naismith SL, Rajaratnam SM, Grunstein RR, Hodges JR, Terpening Z, et al. Disturbances in melatonin secretion and circadian sleep-wake regulation in Parkinson disease. Sleep Med 2014, 15: 342–347.PubMedCrossRefGoogle Scholar
  73. 73.
    Videnovic A, Noble C, Reid KJ, Peng J, Turek FW, Marconi A, et al. Circadian melatonin rhythm and excessive daytime sleepiness in Parkinson disease. JAMA Neurol 2014, 71: 463–469.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Breen DP, Vuono R, Nawarathna U, Fisher K, Shneerson JM, Reddy AB, et al. Sleep and circadian rhythm regulation in early Parkinson disease. JAMA Neurol 2014, 71: 589–595.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Breen DP, Nombela C, Vuono R, Jones PS, Fisher K, Burn DJ, et al. Hypothalamic volume loss is associated with reduced melatonin output in Parkinson’s disease. Mov Disord 2016.Google Scholar
  76. 76.
    Bogaerts V, Theuns J, van Broeckhoven C. Genetic findings in Parkinson’s disease and translation into treatment: a leading role for mitochondria? Genes Brain Behav 2008, 7: 129–151.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Hartmann A, Veldhuis JD, Deuschle M, Standhardt H, Heuser I. Twenty-four hour cortisol release profiles in patients with Alzheimer’s and Parkinson’s disease compared to normal controls: ultradian secretory pulsatility and diurnal variation. Neurobiol Aging 1997, 18: 285–289.PubMedCrossRefGoogle Scholar
  78. 78.
    Tornhage CJ, Skogar O, Borg A, Larsson B, Robertsson L, Andersson L, et al. Short- and long-term effects of tactile massage on salivary cortisol concentrations in Parkinson’s disease: a randomised controlled pilot study. BMC Complement Altern Med 2013, 13: 357.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Mizobuchi M, Hineno T, Kakimoto Y, Hiratani K. Increase of plasma adrenocorticotrophin and cortisol in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated dogs. Brain Res 1993, 612: 319–321.PubMedCrossRefGoogle Scholar
  80. 80.
    Aziz NA, Pijl H, Frolich M, Roelfsema F, Roos RA. Diurnal secretion profiles of growth hormone, thyrotrophin and prolactin in Parkinson’s disease. J Neuroendocrinol 2011, 23: 519–524.PubMedCrossRefGoogle Scholar
  81. 81.
    Langston JW, Forno LS. The hypothalamus in Parkinson disease. Ann Neurol 1978, 3: 129–133.PubMedCrossRefGoogle Scholar
  82. 82.
    Javoy-Agid F, Ruberg M, Pique L, Bertagna X, Taquet H, Studler JM, et al. Biochemistry of the hypothalamus in Parkinson’s disease. Neurology 1984, 34: 672–675.PubMedCrossRefGoogle Scholar
  83. 83.
    Shannak K, Rajput A, Rozdilsky B, Kish S, Gilbert J, Hornykiewicz O. Noradrenaline, dopamine and serotonin levels and metabolism in the human hypothalamus: observations in Parkinson’s disease and normal subjects. Brain Res 1994, 639: 33–41.PubMedCrossRefGoogle Scholar
  84. 84.
    Moore RY, Whone AL, Brooks DJ. Extrastriatal monoamine neuron function in Parkinson’s disease: an 18F-dopa PET study. Neurobiol Dis 2008, 29: 381–390.PubMedCrossRefGoogle Scholar
  85. 85.
    Politis M, Piccini P, Pavese N, Koh SB, Brooks DJ. Evidence of dopamine dysfunction in the hypothalamus of patients with Parkinson’s disease: an in vivo 11C-raclopride PET study. Exp Neurol 2008, 214: 112–116.PubMedCrossRefGoogle Scholar
  86. 86.
    Videnovic A, Lazar AS, Barker RA, Overeem S. ‘The clocks that time us’–circadian rhythms in neurodegenerative disorders. Nat Rev Neurol 2014, 10: 683–693.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Yamamoto T, Nakahata Y, Soma H, Akashi M, Mamine T, Takumi T. Transcriptional oscillation of canonical clock genes in mouse peripheral tissues. BMC Mol Biol 2004, 5: 18.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Guo H, Brewer JM, Champhekar A, Harris RB, Bittman EL. Differential control of peripheral circadian rhythms by suprachiasmatic-dependent neural signals. Proc Natl Acad Sci U S A 2005, 102: 3111–3116.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Cai Y, Liu S, Sothern RB, Xu S, Chan P. Expression of clock genes Per1 and Bmal1 in total leukocytes in health and Parkinson’s disease. Eur J Neurol 2010, 17: 550–554.PubMedCrossRefGoogle Scholar
  90. 90.
    Ding H, Liu S, Yuan Y, Lin Q, Chan P, Cai Y. Decreased expression of Bmal2 in patients with Parkinson’s disease. Neurosci Lett 2011, 499: 186–188.PubMedCrossRefGoogle Scholar
  91. 91.
    Gu Z, Wang B, Zhang YB, Ding H, Zhang Y, Yu J, et al. Association of ARNTL and PER1 genes with Parkinson’s disease: a case-control study of Han Chinese. Sci Rep 2015, 5: 15891.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Mattam U, Jagota A. Daily rhythms of serotonin metabolism and the expression of clock genes in suprachiasmatic nucleus of rotenone-induced Parkinson’s disease male Wistar rat model and effect of melatonin administration. Biogerontology 2015, 16: 109–123.PubMedCrossRefGoogle Scholar
  93. 93.
    Liu C, Chung M. Genetics and epigenetics of circadian rhythms and their potential roles in neuropsychiatric disorders. Neurosci Bull 2015, 31: 141–159.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Liu HC, Hu CJ, Tang YC, Chang JG. A pilot study for circadian gene disturbance in dementia patients. Neurosci Lett 2008, 435: 229–233.PubMedCrossRefGoogle Scholar
  95. 95.
    West RL, Lee JM, Maroun LE. Hypomethylation of the amyloid precursor protein gene in the brain of an Alzheimer’s disease patient. J Mol Neurosci 1995, 6: 141–146.PubMedCrossRefGoogle Scholar
  96. 96.
    Lin Q, Ding H, Zheng Z, Gu Z, Ma J, Chen L, et al. Promoter methylation analysis of seven clock genes in Parkinson’s disease. Neurosci Lett 2012, 507: 147–150.PubMedCrossRefGoogle Scholar
  97. 97.
    Curtis AM, Fagundes CT, Yang G, Palsson-McDermott EM, Wochal P, McGettrick AF, et al. Circadian control of innate immunity in macrophages by miR-155 targeting Bmal1. Proc Natl Acad Sci U S A 2015, 112: 7231–7236.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Dudley CA, Erbel-Sieler C, Estill SJ, Reick M, Franken P, Pitts S, et al. Altered patterns of sleep and behavioral adaptability in NPAS2-deficient mice. Science 2003, 301: 379–383.PubMedCrossRefGoogle Scholar
  99. 99.
    Franken P, Dudley CA, Estill SJ, Barakat M, Thomason R, O’Hara BF, et al. NPAS2 as a transcriptional regulator of non-rapid eye movement sleep: genotype and sex interactions. Proc Natl Acad Sci U S A 2006, 103: 7118–7123.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB, et al. Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 2000, 103: 1009–1017.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Laposky A, Easton A, Dugovic C, Walisser J, Bradfield C, Turek F. Deletion of the mammalian circadian clock gene BMAL1/Mop3 alters baseline sleep architecture and the response to sleep deprivation. Sleep 2005, 28: 395–409.PubMedGoogle Scholar
  102. 102.
    Zheng B, Albrecht U, Kaasik K, Sage M, Lu W, Vaishnav S, et al. Nonredundant roles of the mPer1 and mPer2 genes in the mammalian circadian clock. Cell 2001, 105: 683–694.PubMedCrossRefGoogle Scholar
  103. 103.
    Xie Z, Su W, Liu S, Zhao G, Esser K, Schroder EA, et al. Smooth-muscle BMAL1 participates in blood pressure circadian rhythm regulation. J Clin Invest 2015, 125: 324–336.PubMedCrossRefGoogle Scholar
  104. 104.
    Ait-Hmyed Hakkari O, Acar N, Savier E, Spinnhirny P, Bennis M, Felder-Schmittbuhl MP, et al. Rev-Erbalpha modulates retinal visual processing and behavioral responses to light. FASEB J 2016, 30: 3690-3701.PubMedCrossRefGoogle Scholar
  105. 105.
    Kandalepas PC, Mitchell JW, Gillette MU. Melatonin signal transduction pathways require E-box-mediated transcription of Per1 and Per2 to reset the SCN clock at dusk. PLoS One 2016, 11: e0157824.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Terman M. Evolving applications of light therapy. Sleep Med Rev 2007, 11: 497–507.PubMedCrossRefGoogle Scholar
  107. 107.
    Witkovsky P, Veisenberger E, Haycock JW, Akopian A, Garcia-Espana A, Meller E. Activity-dependent phosphorylation of tyrosine hydroxylase in dopaminergic neurons of the rat retina. J Neurosci 2004, 24: 4242–4249.PubMedCrossRefGoogle Scholar
  108. 108.
    Paus S, Schmitz-Hubsch T, Wullner U, Vogel A, Klockgether T, Abele M. Bright light therapy in Parkinson’s disease: a pilot study. Mov Disord 2007, 22: 1495–1498.PubMedCrossRefGoogle Scholar
  109. 109.
    Willis GL, Turner EJ. Primary and secondary features of Parkinson’s disease improve with strategic exposure to bright light: a case series study. Chronobiol Int 2007, 24: 521–537.PubMedCrossRefGoogle Scholar
  110. 110.
    Willis GL, Moore C, Armstrong SM. A historical justification for and retrospective analysis of the systematic application of light therapy in Parkinson’s disease. Rev Neurosci 2012, 23: 199–226.PubMedGoogle Scholar
  111. 111.
    Yamanaka Y, Hashimoto S, Masubuchi S, Natsubori A, Nishide SY, Honma S, et al. Differential regulation of circadian melatonin rhythm and sleep-wake cycle by bright lights and nonphotic time cues in humans. Am J Physiol Regul Integr Comp Physiol 2014, 307: R546–557.PubMedCrossRefGoogle Scholar
  112. 112.
    Yamanaka Y, Hashimoto S, Takasu NN, Tanahashi Y, Nishide SY, Honma S, et al. Morning and evening physical exercise differentially regulate the autonomic nervous system during nocturnal sleep in humans. Am J Physiol Regul Integr Comp Physiol 2015, 309: R1112–1121.PubMedCrossRefGoogle Scholar
  113. 113.
    Yasumoto Y, Nakao R, Oishi K. Free access to a running-wheel advances the phase of behavioral and physiological circadian rhythms and peripheral molecular clocks in mice. PLoS One 2015, 10: e0116476.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Klamroth S, Steib S, Devan S, Pfeifer K. Effects of Exercise Therapy on Postural Instability in Parkinson Disease: A Meta-analysis. J Neurol Phys Ther 2016, 40: 3–14.PubMedCrossRefGoogle Scholar
  115. 115.
    Rios Romenets S, Anang J, Fereshtehnejad SM, Pelletier A, Postuma R. Tango for treatment of motor and non-motor manifestations in Parkinson’s disease: a randomized control study. Complement Ther Med 2015, 23: 175–184.PubMedCrossRefGoogle Scholar
  116. 116.
    Li F, Harmer P. Economic evaluation of a Tai Ji Quan intervention to reduce falls in people with Parkinson disease, Oregon, 2008–2011. Prev Chronic Dis 2015, 12: E120.PubMedPubMedCentralGoogle Scholar
  117. 117.
    Fonken LK, Frank MG, Kitt MM, Barrientos RM, Watkins LR, Maier SF. Microglia inflammatory responses are controlled by an intrinsic circadian clock. Brain Behav Immun 2015, 45: 171–179.PubMedCrossRefGoogle Scholar
  118. 118.
    He Y, Cornelissen-Guillaume GG, He J, Kastin AJ, Harrison LM, Pan W. Circadian rhythm of autophagy proteins in hippocampus is blunted by sleep fragmentation. Chronobiol Int 2016, 33: 553–560.PubMedCrossRefGoogle Scholar
  119. 119.
    Neufeld-Cohen A, Robles MS, Aviram R, Manella G, Adamovich Y, Ladeuix B, et al. Circadian control of oscillations in mitochondrial rate-limiting enzymes and nutrient utilization by PERIOD proteins. Proc Natl Acad Sci U S A 2016, 113: E1673–1682.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Shanghai Institutes for Biological Sciences, CAS and Springer Science+Business Media Singapore 2016

Authors and Affiliations

  • Siyue Li
    • 1
    • 2
  • Yali Wang
    • 1
    • 2
  • Fen Wang
    • 2
  • Li-Fang Hu
    • 2
  • Chun-Feng Liu
    • 1
    • 2
    Email author
  1. 1.Department of Neurology and Suzhou Clinical Research Center of Neurological DiseaseThe Second Affiliated Hospital of Soochow UniversitySuzhouChina
  2. 2.Institutes of NeuroscienceSoochow UniversitySuzhouChina

Personalised recommendations