Photobiomodulation preserves behaviour and midbrain dopaminergic cells from MPTP toxicity: evidence from two mouse strains

BMC Neuroscience

Alim-Louis Benabid²  John Mitrofanis³  Jonathan Stone¹  Daniel M Johnstone¹  David Ratel²  Nabil El Massri³  Napoleon Torres²  Cécile Moro² 

[1] Department of Physiology, University of Sydney, Sydney, Australia;CEA, LETI, CLINATEC, Grenoble, 38054, France;Department of Anatomy & Histology, University of Sydney, Sydney, Australia

关键词: Neuroprotection;    C57BL/6;    Balb/c;    Substantia nigra;    Tyrosine hydroxylase;   

Others  :  1140347
DOI  :  10.1186/1471-2202-14-40

 received in 2012-10-26, accepted in 2013-03-21,  发布年份 2013

【 摘 要 】

Background

We have shown previously that near-infrared light (NIr) treatment or photobiomodulation neuroprotects dopaminergic cells in substantia nigra pars compacta (SNc) from degeneration induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in Balb/c albino mice, a well-known model for Parkinson’s disease. The present study explores whether NIr treatment offers neuroprotection to these cells in C57BL/6 pigmented mice. In addition, we examine whether NIr influences behavioural activity in both strains after MPTP treatment. We tested for various locomotive parameters in an open-field test, namely velocity, high mobility and immobility.

Results

Balb/c (albino) and C57BL/6 (pigmented) mice received injections of MPTP (total of 50 mg/kg) or saline and NIr treatments (or not) over 48 hours. After each injection and/or NIr treatment, the locomotor activity of the mice was tested. After six days survival, brains were processed for TH (tyrosine hydroxylase) immunochemistry and the number of TH⁺ cells in the substantia nigra pars compacta (SNc) was estimated using stereology. Results showed higher numbers of TH⁺ cells in the MPTP-NIr groups of both strains, compared to the MPTP groups, with the protection greater in the Balb/c mice (30% vs 20%). The behavioural tests revealed strain differences also. For Balb/c mice, the MPTP-NIr group showed greater preservation of locomotor activity than the MPTP group. Behavioural preservation was less evident in the C57BL/6 strain however, with little effect of NIr being recorded in the MPTP-treated cases of this strain. Finally, there were differences between the two strains in terms of NIr penetration across the skin and fur. Our measurements indicated that NIr penetration was considerably less in the pigmented C57BL/6, compared to the albino Balb/c mice.

Conclusions

In summary, our results revealed the neuroprotective benefits of NIr treatment after parkinsonian insult at both cellular and behavioural levels and suggest that Balb/c strain, due to greater penetration of NIr through skin and fur, provides a clearer model of protection than the C57BL/6 strain.

【 授权许可】

   
2013 Moro et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Blandini F, Nappi G, Tassorelli C, Martignoni E: Functional changes of the basal ganglia circuitry in Parkinson’s disease. Prog Neurobiol 2000, 2:63-88.
• [2]Bergman H, Deuschl G: Pathophysiology of Parkinson’s disease: from clinical neurology to basic neuroscience and back. Mov Disord 2002, 17:S28-S40.
• [3]Rinne JO: Nigral degeneration in Parkinson’s disease. Mov Disord 8 Suppl 1993, 1:S31-S35.
• [4]McRitchie DA, Cartwright HR, Halliday GM: Specific A10 dopaminergic nuclei in the midbrain degenerate in Parkinson’s disease. Exp Neurol 1997, 144:202-213.
• [5]Langston JW: The etiology of Parkinson’s disease with emphasis on the MPTP story. Neurology 1996, 47:S153-S160.
• [6]Kruger R, Kuhn W, Muller T, Woitalla D, Graeber M, Kosel S, Przuntek H, Epplen JT, Schols L, Riess O: Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson’s disease. Nat Genet 1998, 18:106-118.
• [7]LeWitt PA: Neuroprotection for Parkinson’s disease. J Neural Transm Suppl 2006, 71:113-122.
• [8]Ma J, Shaw VE, Mitrofanis J: Does melatonin help save dopaminergic cells in MPTP-treated mice? Parkinsonism Relat Disord 2009, 15:307-314.
• [9]Liang HL, Whelan HT, Eells JT, Wong-Riley MT: Near-infrared light via light-emitting diode treatment is therapeutic against rotenone- and 1-methyl-4-phenylpyridinium ion-induced neurotoxicity. Neurosci 2008, 153:963-974.
• [10]Ying R, Liang HL, Whelan HT, Eells JT, Wong-Riley MT: Pretreatment with near-infrared light via light-emitting diode provides added benefit against rotenone - and MPP+- induced neurotoxicity. Brain Res 2008, 1243:167-173.
• [11]Shaw VE, Spana S, Ashkan K, Benabid AL, Stone J, Baker GE, Mitrofanis J: Neuroprotection of midbrain dopaminergic cells in MPTP-treated mice after near-infrared light treatment. J Comp Neurol 2010, 1518:25-40.
• [12]Peoples CL, Spana S, Ashkan K, Benabid AL, Stone J, Baker GE, Mitrofanis J: Photobiomodulation enhances nigral dopaminergic cell survival in a chronic MPTP mouse model of Parkinson’s disease. Parkinsonism Relat Disord 2012, 18:469-476.
• [13]Whelan HT, DeSmet KD, Buchmann E, Henry M, Wong-Riley M, Eells JT, Verhoeve J: Harnessing the cell’s own ability to repair and prevent neurodegenerative disease. SPIE Newsroom 2008, 1-3.
• [14]Desmet KD, Paz DA, Corry JJ, Eells JT, Wong-Riley MT, Henry MM, Buchmann EV, Connelly MP, Dovi JV, Liang HL, Henshel DS, Yeager RL, Millsap DS, Lim J, Gould LJ, Das R, Jett M, Hodgson BD, Margolis D, Whelan HT: Clinical and experimental applications of NIR-LED photobiomodulation. Photomed Laser Surg 2006, 24:121-128.
• [15]Hamblin MR, Demidova TN: Mechanisms of low level light therapy. In Mechanisms for low-light therapy. Edited by Hamblin MR, Waynart RW, Anders J. San Jose, CA, USA: Proc SPIE; 2006:6140.
• [16]Shaw VE, Peoples CL, Spana S, Ashkan K, Benabid AL, Stone J, Baker GE, Mitrofanis J: Patterns of cell activity in the subthalamic region associated with the neuroprotective action of near-infrared light treatment in MPTP-treated mice. Parkinson’s disease 2012., (ID 296875)
• [17]Sedelis M, Hofele K, Auburger GW, Morgan S, Huston JP, Schwarting RKW: MPTP Susceptibility in the Mouse: Behavioural, Neurochemical, and Histological Analysis of Gender and Strain Differences. Behav Gen 2000, 30:171-182.
• [18]Ito T, Suzuki K, Uchida K, Nakayama H: Different susceptibility to 1-methyl-4-phenylpyridium (MPP+)-induced nigro-striatal dopaminergic cell loss between C57BL/6 and BALB/c mice is not related to the difference of monoamine oxidase-B (MAO-B). Exp Toxic Path 2011. EPub
• [19]Riachi NJ, Behmand RA, Harik SI: Correlation of MPTP neurotoxicity in vivo with oxidation of MPTP by the brain and blood–brain barrier in vitro in five rat strains. Brain Res 1991, 555:19-24.
• [20]Schober A: Classic toxin-induced animal models of Parkinson’s disease: 6OHDA and MPTP. Cell Tissue Res 2004, 318:215-24.
• [21]Bové J, Perier C: Neurotoxin-based models of Parkinson’s disease. Neurosci 2012, 211:51-76.
• [22]Piallat B, Benazzouz A, Benabid AL: Subthalamic nucleus lesion in rats prevents dopaminergic nigral neuron degeneration after striatal 6-OHDA injection: behavioural and immunohistochemical studies. Eur J Neurosci 1996, 8:1408-1414.
• [23]Wallace BA, Ashkan K, Heise CE, Foote KD, Torres N, Mitrofanis J, Benabid AL: Survival of midbrain dopaminergic cells after lesion or deep brain stimulation of the subthalamic nucleus in MPTP-treated monkeys. Brain 2007, 130:2129-2145.
• [24]Luquin N, Mitrofanis J: Does the cerebral cortex exacerbate dopamineric cell death in the substantia nigra of 6OHDA-lesioned rats? Parkinson Related Disord 2008, 14:213-223.
• [25]Björklund A, Rosenblad C, Winkler C, Kirik D: Studies on neuroprotective and regenerative effects of GDNF in a partial lesion model of Parkinson’s disease. Neurobiol Dis 1997, 4:186-200.
• [26]Huot P, Lévesque M, Parent A: The fate of striatal dopaminergic neurons in Parkinson’s disease and Huntington’s chorea. Brain 2007, 130:222-32.
• [27]Paxinos G, Franklin BJ: The mouse brain in stereotaxic coordinates. 2nd edition. San Diego, CA, USA: Academic Press California USA; 2001.
• [28]Bezard E, Dovero S, Bioulac B, Gross C: Effects of different schedules of MPTP administration on dopaminergic neurodegeneration in mice. Exp Neurol 1997, 148:288-292.
• [29]Goldberg NR, Haack AK, Lim NS, Janson OK, Meshul CK: Dopaminergic and behavioural correlates of progressive lesioning of the nigrostriatal pathway with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neurosci 2011, 180:256-271.
• [30]Meredith P, Powell BJ, Riesz J, Nighswander-Rempel S, Pederson MR, Moore E: Towards structure–property-function relationships for eumelanin. Soft Matter 2006, 2:37.