Lack of long-term changes in circadian, locomotor, and cognitive functions in acute and chronic MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) mouse models of parkinson's disease

Chronobiology International

Volumn 30, Issue 6, 2013, Pages 741-755

  Fifel, Karim ^a,b   Dkhissi Benyahya, Ouria ^a,b   Cooper, Howard M ^a,b  

^a STEM CELL AND BRAIN RESEARCH INSTITUTE   (France)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

Chronobiology; Circadian entrainment; Cognitive deficits; Masking; Mouse model; Nonmotor symptoms; Radial water maze; Sleep

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; DOPAMINE RECEPTOR STIMULATING AGENT; TYROSINE 3 MONOOXYGENASE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; C57BL MOUSE; CIRCADIAN RHYTHM; COGNITION; COGNITIVE DEFECT; DISEASE MODEL; DRUG EFFECT; LEARNING; LOCOMOTION; MALE; MAZE TEST; MEMORY; METABOLISM; MOTOR ACTIVITY; MOUSE; PARKINSON DISEASE;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ANIMALS; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; COGNITION; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DOPAMINE AGENTS; LEARNING; LOCOMOTION; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; PARKINSON DISEASE; TYROSINE 3-MONOOXYGENASE;

ANIMALIA;

EID: 84879374202     PISSN: 07420528     EISSN: 15256073     Source Type: Journal    
DOI: 10.3109/07420528.2012.762011     Document Type: Article

References (76)

1. Alamed J, Wilcock DM, Diamond DM, et al. (2006). Two-day radialarm water maze learning and memory task; robust resolution of amyloid-related memory deficits in transgenic mice. Nat Protocols, 1, 1671-9. (Pubitemid 46773288)
2. Alvarez-Fischer D, Guerreiro S, Hunot S, et al. (2008). Modelling Parkinson-like neurodegeneration via osmotic minipump delivery of MPTP and probenecid. J Neurochem, 107, 701-11.
3. Baier PC, Branisa P, Koch R, et al. (2006). Circadian distribution of motor-activity in unilaterally 6-hydroxy-dopamine lesioned rats. Exp Brain Res, 169, 283-8. (Pubitemid 43221156)
4. Barraud Q, Lambrecq V, Forni C, et al. (2009). Sleep disorders in Parkinson's disease: The contribution of the MPTP non-human primate model. Exp Neurol, 2, 574-82.
5. Beal MF. (2001). Experimental models of Parkinson's disease. Nature, 2, 325-32. (Pubitemid 33680574)
6. Beal MF. (2010). Parkinson's disease: A model dilemma. Nature, 466, S8-10.
7. Ben V, Bruguerolle B. (2000). Effects of bilateral striatal 6-OHDA lesions on circadian rhythms in the rat: A radiotelemetric study. Life Sci, 67, 1549-58. (Pubitemid 30663012)
8. Bezard E, Dovero S, Bioulac B, Gross CE. (1997). Kinetics of nigral degeneration in a chronic model of MPTP-treated mice. Neurosci Lett, 234, 47-50. (Pubitemid 27435966)
9. Bezard E, Dovero S, Imbert C, et al. (2000a). Spontaneous longterm compensatory dopaminergic sprouting in MPTP-treated mice. Synapse, 38, 363-8.
10. Bezard E, Jaber M, Gonon F, et al. (2000b). Adaptive changes in the nigrostriatal pathway in response to increased 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine-induced neurodegeneration in the mouse. Eur J Neurosci, 12, 2892-900.
11. Borbély AA, Achermann P. (1999). Sleep homeostasis and models of sleep regulation. J Biol Rhythms, 14, 557-68. (Pubitemid 30086864)
12. Bosboom JL, Stoffers D, Wolters ECH. (2004). Cognitive dysfunction and dementia in Parkinson's disease. J Neural Transm, 111, 1303-15. (Pubitemid 39468392)
13. Bubser M, Schmidt WJ. (1990). 6-Hydroxydopamine lesion of the rat prefrontal cortex increases locomotor activity, impairs acquisition of delayed alternation tasks, but does not affect uninterrupted tasks in the radial maze. Behav Brain Res, 37, 157-68. (Pubitemid 20085404)
14. Chaudhuri KR, Schapira AH. (2009). Non-motor symptoms of Parkinson's disease: Dopaminergic pathophysiology and treatment. Lancet Neurol, 8, 464-74.
15. Chaudhuri KR, Healy DG, Schapira AH. (2006). Non-motor symptoms of Parkinson's disease: Diagnosis and management. Lancet Neurol, 5, 235-45. (Pubitemid 43238347)
16. Chesselet MF, Richter F. (2011). Modelling of Parkinson's disease in mice. Lancet Neurol, 10, 1108-18.
17. Cleren C, Yang L, Lorenzo B, et al. (2008). Therapeutic effects of coenzyme Q10 (CoQ10) and reduced CoQ10 in the MPTP model of Parkinsonism. J Neurochem, 104, 1613-21. (Pubitemid 351316765)
18. Collier TJ, Kanaan NM, Kordower JH. (2011). Ageing as a primary risk factor for Parkinson's disease: Evidence from studies of non-human primates. Nat Rev Neurosci, 12, 359-66.
19. Da Cunha C, Angelucci ME, Canteras NS, et al. (2002). The lesion of the rat substantia nigra pars compacta dopaminergic neurons as a model for Parkinson's disease memory disabilities. Cell Mol Neurobiol, 22, 227-37. (Pubitemid 35364882)
20. Dawson TM, Ko HS, Dawson VL. (2010). Genetic animal models of Parkinson's disease. Neuron, 66, 646-61.
21. De Cock VC, Vidailhet M, Arnulf I. (2008). Sleep disturbances in patients with parkinsonism. Nat Clin Pract Neurol, 4, 254-66. (Pubitemid 351639546)
22. Deguil J, Chavant F, Lafay-Chebassier C, et al. (2010). Neuroprotective effect of PACAP on translational control alteration and cognitive decline in MPTP parkinsonian mice. Neurotox Res, 17, 142-55.
23. Dijk DJ, Lockley SW. (2002). Integration of human sleepwake regulation and circadian rhythmicity. J Appl Physiol, 92, 852-62. (Pubitemid 34671057)
24. Dkhissi-Benyahya O, Sicard B, Cooper HM. (2000). Effects of irradiance and stimulus duration on early gene expression (Fos) in the suprachiasmatic nucleus: Temporal summation and reciprocity. J Neurosci, 20, 7790-7.
25. Dluzen DE, Kreutzberg JD. (1993). 1-Methyl-4-phenyl-1,2,3,6- tetrahydropyridine (MPTP) disrupts social memory/recognition processes in the male mouse. Brain Res, 609, 98-102. (Pubitemid 23136806)
26. Doi M, Yujnovsky I, Hirayama J, et al. (2006). Impaired light masking in dopamine D2 receptor-null mice. Nat Neurosci, 9, 732-4.
27. Fleming SM, Salcedo J, Hutson CB, et al. (2008). Impaired reversal learning in transgenic mice overexpressing human wildtype alpha-synuclein. Soc. Neurosci. Abstract 341.1, N3.
28. Fornai F, Schlüter OM, Lenzi P, et al. (2005). Parkinson-like syndrome induced by continuous MPTP infusion: Convergent roles of the ubiquitin-proteasome system and alpha-synuclein. Proc Natl Acad Sci U S A, 102, 3413-8. (Pubitemid 40328059)
29. Fox SH, Brotchie JM. (2010). The MPTP-lesioned non-human primate models of Parkinson's disease: Past, present, and future. Prog Brain Res, 184, 133-57.
30. Fujita K, Seike T, Yutsudo N, et al. (2009). Hydrogen in drinking water reduces dopaminergic neuronal loss in the 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine mouse model of Parkinson's disease. PLoS ONE, 4, e7247.
31. Gibrat C, Saint-Pierre M, Bousquet M, et al. (2009). Differences between subacute and chronic MPTP mice models: Investigation of dopaminergic neuronal degeneration and alpha-synuclein inclusions. J Neurochem, 109, 1469-82.
32. Gravotta L, Gavrila AM, Hood S, Amir S. (2011). Global depletion of dopamine using intracerebroventricular 6-hydroxydopamine injection disrupts normal circadian wheel-running patterns and PERIOD2 expression in the rat forebrain. J Mol Neurosci, 45, 162-71.
33. Hood S, Cassidy P, Cossette MP, et al. (2010). 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, 30, 14046-58.
34. Imbesi M, Yildiz S, Dirim Arslan A, et al. (2009). Dopamine receptor mediated regulation of neuronal ''clock'' gene expression. Neuroscience, 158, 537-44.
35. Ishida Y, Yokoyama C, Inatomi T, et al. (2002). Circadian rhythm of aromatic L-amino acid decarboxylase in the rat suprachiasmatic nucleus: Gene expression and decarboxylating activity in clock oscillating cells. Genes Cells, 7, 447-59. (Pubitemid 34537770)
36. Jackson-Lewis V, Przedborski S. (2007). Protocol for the MPTP mouse model of Parkinson's disease. Nat Protocols, 2, 141-51. (Pubitemid 47044700)
37. Jackson-Lewis V, Przedborski S. (2008). The MPTP mouse model of Parkinson's disease: The true, the false and the unknown. In Nass R, Przedborski S. (eds.). Parkinson's disease: Molecular and therapeutic insights from model systems. Amsterdam: Elsevier, pp. 147-58.
38. Johnson CH, Elliott JA, Foster R. (2003). Entrainment of circadian programs. Chronobiol Int, 20, 741-74. (Pubitemid 37187518)
39. Kudo T, Loh DH, Truong D, et al. (2011). Circadian dysfunction in a mouse model of Parkinson's disease. Exp Neurol, 232, 66-75.
40. Laloux C, Derambure P, Kreisler A, et al. (2008). MPTP-treated mice: Long-lasting loss of nigral TH-ir neurons but not paradoxical sleep alterations. Exp Brain Res, 186, 635-42.
41. Lax P, Esquiva G, Esteve-Rudd J, et al. (2012). Circadian dysfunction in a rotenone-induced parkinsonian rodent model. Chronobiol Int, 29, 147-56.
42. Lima MM, Andersen ML, Reksidler AB, et al. (2007). The role of the substantia nigra pars compacta in regulating sleep patterns in rats. PLoS ONE, 6, e513.
43. Maetzler W, Liepelt I, Berg D. (2009). Progression of Parkinson's disease in the clinical phase: Potential markers. Lancet Neurol, 8, 1158-71.
44. Magen I, Chesselet MF. (2010). Genetic mouse models of Parkinson's disease: The state of the art. Prog Brain Res, 184, 53-87.
45. Mrosovsky N. (1999). Masking: History, definitions, and measurement. Chronobiol Int, 4, 415-29. (Pubitemid 29362565)
46. Pfeffer M, Plenzig S, Gispert S, et al. (2012). Disturbed sleep/wake rhythms and neuronal cell loss in lateral hypothalamus and retina of mice with a spontaneous deletion in the ubiquitin carboxyl-terminal hydrolase L1 gene. Neurobiol Aging, 33, 393-403.
47. Pham TT, Giesert F, Röthig A, et al. (2010). DJ-1-deficient mice show less TH-positive neurons in the ventral tegmental area and exhibit non-motoric behavioural impairments. Genes Brain Behav, 9, 305-17.
48. Pifl C, Hornykiewicz O. (2006). Dopamine turnover is upregulated in the caudate/putamen of asymptomatic MPTP-treated rhesus monkeys. Neurochem Int, 49, 519-24. (Pubitemid 44189648)
49. Plowman EK, Kleim JA. (2011). Behavioral and neurophysiological correlates of striatal dopamine depletion: A rodent model of Parkinson's disease. J Commun Disord, 44, 549-56.
50. Portaluppi F, Smolensky MH, Touitou Y. (2010). Ethics and methods for biological rhythm research on animals and human beings. Chronobiol Int, 27, 1911-29.
51. Potashkin JA, Blume SR, Runkle NK. (2011). Limitations of animal models of Parkinson's disease. Parkinsons Dis. 2011:658083.
52. Pothakos K, Kurz MJ, Lau YS. (2009). Restorative effect of endurance exercise on behavioral deficits in the chronic mouse model of Parkinson's disease with severe neurodegeneration. BMC Neurosci, 10, 6.
53. Przedborski S, Vila M (2003). The 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine mouse model: A tool to explore the pathogenesis of Parkinson's disease. Ann N Y Acad Sci, 991, 189-98. (Pubitemid 36793814)
54. Redlin U. (2001). Neural basis and biological function of masking by light in mammals: Suppression of melatonin and locomotor activity. Chronobiol Int, 5, 737-58. (Pubitemid 33139497)
55. Reppert SM, Weaver DR. (2002). Coordination of circadian timing in mammals. Nature, 418, 935-41. (Pubitemid 34976023)
56. Rieux C, Carney R, Lupi D, et al. (2002). Analysis of immunohistochemical label of Fos protein in the suprachiasmatic nucleus: Comparison of different methods of quantification. J Biol Rhythms, 17, 121-36. (Pubitemid 37187352)
57. Rye D. (2010). Seeing beyond one's nose: Sleep disruption and excessive sleepiness accompany motor disability in the MPTP treated primate. Exp Neurol, 2, 179-80.
58. Schapira AH, Jenner P. (2011). Etiology and pathogenesis of Parkinson's disease. Mov Disord, 26, 1049-55.
59. Schneider JS, Pope-Coleman A. (1995). Cognitive deficits precede motor deficits in a slowly progressing model of parkinsonism in the monkey. Neurodegeneration, 4, 245-55.
60. Sedelis M, Schwarting RK, Huston JP. (2001). Behavioral phenotyping of the MPTP mouse model of Parkinson's disease. Behav Brain Res, 125, 109-25. (Pubitemid 33000449)
61. Simon H, Taghzouti K, Le Moal M. (1986). Deficits in spatialmemory tasks following lesions of septal dopaminergic terminals in the rat. Behav Brain Res, 19, 7-16. (Pubitemid 16168020)
62. Sokolove PG, Bushell WN. (1978). The chi square periodogram: Its utility for analysis of circadian rhythms. J Theor Biol, 72, 131-60. (Pubitemid 8350595)
63. Stam CJ, de Bruin JP, van Haelst AM, et al. (1989). Influence of the mesocortical dopaminergic system on activity, food hoarding, social-agonistic behavior, and spatial delayed alternation in male rats. Behav Neurosci, 103, 24-35. (Pubitemid 19058641)
64. Tanila H, Björklund M, Riekkinen Jr. P. (1998). Cognitive changes in mice following moderate MPTP exposure. Brain Res Bull, 45, 577-82. (Pubitemid 28262597)
65. Taylor TN, Greene JG, Miller GW. (2010). Behavioral phenotyping of mouse models of Parkinson's disease. Behav Brain Res, 211, 1-10.
66. Thomas B, von Coelln R, Mandir AS, et al. (2007). MPTP and DSP-4 susceptibility of substantia nigra and locus coeruleus catecholaminergic neurons in mice is independent of parkin activity. Neurobiol Dis, 26, 312-22. (Pubitemid 46561335)
67. Valentinuzzi VS, Scarbrough K, Takahashi JS, Turek FW. (1997). Effects of aging on the circadian rhythm of wheel-running activity in C57BL/6 mice. Am J Physiol, 273, R1957-64.
68. Vezoli J, Fifel K, Leviel V, et al. (2011). Early presymptomatic and long-term changes of rest activity cycles and cognitive behavior in a MPTP-monkey model of Parkinson's disease. PLoS ONE, 6, e23952.
69. Videnovic A, Golombek D. (2013). Circadian and sleep disorders in Parkinson's disease. Exp Neurol, 243, 45-56.
70. Viyoch J, Matsunaga N, Yoshida M, et al. (2005). Effect of haloperidol on mPer1 gene expression in mouse suprachiasmatic nuclei. J Biol Chem, 280, 6309-15. (Pubitemid 40341177)
71. Vorhees CV, Williams MT. (2006). Morris water maze: Procedures for assessing spatial and related forms of learning and memory. Nat Protocols, 1, 848-58.
72. Weaver DR, Rivkees SA, Reppert SM. (1992). D1-dopamine receptors activate c-fos expression in the fetal suprachiasmatic nuclei. Proc Natl Acad Sci U. S. A, 89, 9201-4.
73. Yang J, He L, Wang J, Adams Jr. JD (2004). Early administration of nicotinamide prevents learning and memory impairment in mice induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Pharmacol Biochem Behav, 78, 179-83. (Pubitemid 38670527)
74. Yang L, Calingasan NY, Thomas B, et al. (2009a). Neuroprotective effects of the triterpenoid, CDDO methyl amide, a potent inducer of Nrf2-mediated transcription. PLoS ONE, 4, e5757.
75. Yang L, Calingasan NY, Wille EJ, et al. (2009b). Combination therapy with coenzyme Q10 and creatine produces additive neuroprotective effects in models of Parkinson's and Huntington's diseases. J Neurochem, 109, 1427-39.
76. Zhu XR, Maskri L, Herold C, et al. (2007). Non-motor behavioural impairments in parkin-deficient mice. Eur J Neurosci, 26, 1902-11. (Pubitemid 47493196)