MALDI mass spectrometry imaging of 1-Methyl-4-phenylpyridinium (MPP +) in Mouse Brain

Neurotoxicity Research

Volumn 25, Issue 1, 2014, Pages 135-145

  Kadar, Hanane ^a   Le Douaron, Gael ^a,b   Amar, Majid ^b   Ferrié, Laurent ^a   Figadère, Bruno ^a   Touboul, David ^a   Brunelle, Alain ^a   Raisman Vozari, Rita ^b  

^a CNRS   (France)

^b INSERM   (France)

Author keywords

Intranasal administration; MALDI; Mass spectrometry imaging; MPTP; Parkinson's disease

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; 1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN CORTEX; BRAIN REGION; CEREBELLUM; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC SYSTEM; HIPPOCAMPUS; IMAGE ANALYSIS; LOCUS CERULEUS; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY IMAGING; MOUSE; NEUROIMAGING; NONHUMAN; NORADRENERGIC SYSTEM; NUCLEUS ACCUMBENS; OLFACTORY BULB; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SEROTONINERGIC SYSTEM; SUBSTANTIA NIGRA PARS COMPACTA; SUBSTANTIA NIGRA PARS RETICULATA; VENTRAL MESENCEPHALON; VENTRAL TEGMENTUM; ANIMAL; BRAIN LEVEL; C57BL MOUSE; INTOXICATION; INTRANASAL DRUG ADMINISTRATION; MASS SPECTROMETRY; METABOLISM;

1-METHYL-4-PHENYLPYRIDINIUM; ADMINISTRATION, INTRANASAL; ANIMALS; BRAIN CHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MPTP POISONING; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84891874104     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-013-9449-5     Document Type: Article

References (77)

1. Baker H, Spencer RF (1986) Trans-neuronal transport of peroxidase-conjugated wheat-germ agglutinin (wga-hrp) from the olfactory epithelium to the brain of the adult-rat. Exp Brain Res 63:461-473. doi: 10.1007/bf00237470 (Pubitemid 16036221)
2. Bakry R, Rainer M, Huck CW, Bonn GK (2011) Protein profiling for cancer biomarker discovery using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and infrared imaging: a review. Anal Chim Acta 690:26-34. doi: 10.1016/j.aca.2011.01.044
3. Becker JSa, Zoriy M, Matusch A, Wu B, Salber D, Palm C, Becker JSu (2010) Bioimaging of metals by laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS). Mass Spectrom Rev 29:156-175. doi: 10.1002/mas.20239
4. Behrouz B, Drolet RE, Sayed ZA, Lookingland KJ, Goudreau JL (2007) Unique responses to mitochondrial complex I inhibition in tuberoinfundibular dopamine neurons may impart resistance to toxic insult. Neuroscience 147:592-598. doi: 10.1016/j.neuroscience.2007.05.007 (Pubitemid 46990663)
5. Benabdellah F, Yu H, Brunelle A, Laprévote O, De La Porte S (2009) MALDI reveals membrane lipid profile reversion in MDX mice. Neurobiol Dis 36:252-258. doi: 10.1016/j.nbd.2009.07.013
6. Boeckler F, Leng A, Mura A, Bettinetti L, Feldon J, Gmeiner P, Ferger B (2003) Attenuation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) neurotoxicity by the novel selective dopamine d-3-receptor partial agonist FAUC 329 predominantly in the nucleus accumbens of mice. Biochem Pharmacol 66:1025-1032. doi: 10.1016/s0006-2952(03)00451-9 (Pubitemid 37083598)
7. Brignole-Baudouin F, Desbenoit N, Hamm G, Liang H, Both J-P, Brunelle A, Fournier I, Guérineau V, Legouffe R, Stauber J, Touboul D, Wisztorski M, Salzet M, Laprévote O, Baudouin C (2012) A new safety concern for glaucoma treatment demonstrated by mass spectrometry imaging of benzalkonium chloride distribution in the eye, an experimental study in rabbits. PLoS ONE 7:e50180. doi: 10.1371/journal.pone.0050180
8. Broadwell RD, Balin BJ (1985) Endocytic and exocytic pathways of the neuronal secretory process and transsynaptic transfer of wheat-germ agglutinin-horseradish peroxidase in vivo. J Comp Neurol 242:632-650. doi: 10.1002/cne.902420410 (Pubitemid 16176081)
9. Broadwell RD, Balin BJ, Salcman M (1988) Transcytotic pathway for blood-borne protein through the blood-brain barrier. Proc Natl Acad Sci USA 85:632-636 (Pubitemid 18059323)
10. Buck KJ, Amara SG (1994) Chimeric dopamine norepinephrine transporters delineate structural domains influencing selectivity for catecholamines and 1-methyl-4-phenylpyridinium. Proc Natl Acad Sci USA 91:12584-12588. doi: 10.1073/pnas.91.26.12584
11. Burrell MM, Earnshaw CJ, Clench MR (2007) Imaging matrix assisted laser desorption ionization mass spectrometry: a technique to map plant metabolites within tissues at high spatial resolution. J Exp Bot 58:757-763. doi: 10.1093/jxb/erl139 (Pubitemid 46363172)
12. Caprioli RM, Farmer TB, Gile J (1997) Molecular imaging of biological samples: localization of peptides and proteins using MALDI-TOF MS. Anal Chem 69:4751-4760. doi: 10.1021/ac970888i
13. Castellino S, Groseclose MR, Wagner D (2011) MALDI imaging mass spectrometry: bridging biology and chemistry in drug development. Bioanalysis 3:2427-2441. doi: 10.4155/bio.11.232
14. Cazares LH, Troyer DA, Wang B, Drake RR, Semmes OJ (2011) MALDI tissue imaging: from biomarker discovery to clinical applications. Anal Bioanal Chem 401:17-27. doi: 10.1007/s00216-011-5003-6
15. Cerruti CD, Touboul D, Guerineau V, Petit VW, Laprévote O, Brunelle A (2011) MALDI imaging mass spectrometry of lipids by adding lithium salts to the matrix solution. Anal Bioanal Chem 401:75-87. doi: 10.1007/s00216-011-4814-9
16. Chapman DC, Frey WH, Craft S, Danielyan L, Hallschmid M, Schiöth HB, Benedict C (2012) Intranasal treatment of central nervous system dysfunction in Humans. Pharm Res 30:2475-2484. doi: 10.1007/s11095-012-0915-1
17. Chen J, Zhang C, Liu QF, Shao XY, Feng CC, Shen YH, Zhang QZ, Jiang XG (2012) Solanum tuberosum lectin-conjugated PLGA nanoparticles for nose-to-brain delivery: in vivo and in vitro evaluations. J Drug Target 20:174-184. doi: 10.3109/1061186x.2011.622396
18. Chiba K, Trevor A, Castagnoli N (1984) Metabolism of the neurotoxic tertiary amine, MPTP, by brain monoamine-oxidase. Biochem Biophys Res Commun 120:574-578. doi: 10.1016/0006-291x(84)91293-2 (Pubitemid 14101750)
19. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39:889-909. doi: 10.1016/s0896-6273(03)00568-3 (Pubitemid 37130207)
20. Di Monte DA (2003) The environment and Parkinson's disease: is the nigrostriatal system preferentially targeted by neurotoxins? Lancet Neurol 2:531-538. doi: 10.1016/S1474-4422(03)00501-5 (Pubitemid 36994992)
21. Donnan GA, Kaczmarczyk SJ, Solopotias T, Rowe P, Kalnins RM, Vajda FJ, Mendelsohn FA (1986) The neurochemical and clinical effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in small animals. Clin Exp Neurol 22:155-164
22. Doty RL (2008) The olfactory vector hypothesis of neurodegenerative disease: is it viable? Ann Neurol 63:7-15. doi: 10.1002/ana.21327 (Pubitemid 351240546)
23. Feany MB, Bender WW (2000) A Drosophila model of Parkinson's disease. Nature 404:394-398. doi: 10.1038/35006074 (Pubitemid 30164341)
24. Fernandez JA, Ochoa B, Fresnedo O, Giralt MT, Rodriguez-Puertas R (2011) Matrix-assisted laser desorption ionization imaging mass spectrometry in lipidomics. Anal Bioanal Chem 401:29-51. doi: 10.1007/s00216-011-4696-x
25. Filipov NM, Norwood AB, Sistrunk SC (2009) Strain-specific sensitivity to MPTP of C57BL/6 and BALB/c mice is age dependent. Neuroreport 20:713-717. doi: 10.1097/WNR.0b013e32832aa95b
26. Fonville JM, Carter C, Cloarec O, Nicholson JK, Lindon JC, Bunch J, Holmes E (2012) Robust data processing and normalization strategy for MALDI mass spectrometric imaging. Anal Chem 84:1310-1319. doi: 10.1021/ac201767g
27. Fornai F, Bassi L, Torracca MT, Allessandri MG, Scalori V, Corsini GU (1996) Region- and neurotransmitter-dependent species and strain differences in DSP-4-induced monoamine depletion in rodents. Neurodegeneration 5:241-249. doi: 10.1006/neur.1996.0032 (Pubitemid 26360052)
28. Fuller RW, Steranka LR (1985) Central and peripheral catecholamine depletion by 1-methyl-4-phenyl-tetrahydropyridine (MPTP) in rodents. Life Sci 36:243-247. doi: 10.1016/0024-3205(85)90066-9 (Pubitemid 15193985)
29. Gemoll T, Roblick UJ, Habermann JK (2011) MALDI mass spectrometry imaging in oncology (review). Mol Med Rep 4:1045-1051. doi: 10.3892/mmr.2011.566
30. Girod M, Shi YZ, Cheng JX, Cooks RG (2011) Mapping lipid alterations in traumatically injured rat spinal cord by desorption electrospray ionization imaging mass spectrometry. Anal Chem 83:207-215. doi: 10.1021/ac102264z
31. Guerquin-Kern JL, Wu TD, Quintana C, Croisy A (2005) Progress in analytical imaging of the cell by dynamic secondary ion mass spectrometry (SIMS microscopy). Biochim Biophys Acta 1724:228-238. doi: 10.1016/j.bbagen.2005.05. 013 (Pubitemid 41080032)
32. Hallman H, Olson L, Jonsson G (1984) Neurotoxicity of the meperidine analog N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine on brain catecholamine neurons in the mouse. Eur J Pharmacol 97:133-136. doi: 10.1016/0014-2999(84) 90521-1 (Pubitemid 14184574)
33. Hamm G, Bonnel D, Legouffe R, Pamelard F, Delbos JM, Bouzom F, Stauber J (2012) Quantitative mass spectrometry imaging of propranolol and olanzapine using tissue extinction calculation as normalization factor. J Proteomics 75:4952-4961. doi: 10.1016/j.jprot.2012.07.035
34. + within the monoaminergic systems of the primate brain following MPTP administration - an in vivo autoradiographic study. Neuroscience 40:133-158. doi: 10.1016/0306-4522(91)90180-v
35. Illum L (2000) Transport of drugs from the nasal cavity to the central nervous system. Eur J Pharm Sci 11:1-18. doi: 10.1016/s0928-0987(00)00087-7 (Pubitemid 30410839)
36. Jackson-Lewis V, Jakowec M, Burke RE, Przedborski S (1995) Time-course and morphology of dopaminergic neuronal death caused by the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neurodegeneration 4:257-269. doi: 10.1016/1055-8330(95)90015-2
37. Javitch JA, Snyder SH (1984) Uptake of MPP(+) by dopamine neurons explains selectivity of parkinsonism-inducing neurotoxin, MPTP. Eur J Pharmacol 106:455-456. doi: 10.1016/0014-2999(84)90740-4 (Pubitemid 15210642)
38. Javoy-Agid F, Agid Y (1980) Is the mesocortical dopaminergic system involved in Parkinson disease? Neurology 30:1326-1330. doi: 10.1212/WNL.30.12. 1326 (Pubitemid 11209189)
39. Jimenez-Jimenez FJ, Tabernero C, Mena MA, Deyebenes JG, Deyebenes MJG, Casarejos MJ, Pardo B, Garciaagundez JA, Benitez J, Martinez A, Garciaasenjo AL (1991) Acute effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in a model of rat designated a poor metabolizer of debrisoquine. J Neurochem 57:81-87. doi: 10.1111/j.1471-4159.1991.tb02102.x
40. Kitamura Y, Kakimura J, Taniguchi T (1998) Protective effect of talipexole on MPTP-treated planarian, a unique Parkinsonian worm model. Jpn J Pharmacol 78:23-29. doi: 10.1254/jjp.78.23 (Pubitemid 28464209)
41. Kolata G (1983) Monkey model of Parkinson's disease. Science 220:705. doi: 10.1126/science.6403987 (Pubitemid 13081943)
42. Lehner A, Johnson M, Simkins T, Janis K, Lookingland K, Goudreau J, Rumbeiha W (2011) Liquid chromatographic-electrospray mass spectrometric determination of 1-methyl-4-phenylpyridine (MPP+) in discrete regions of murine brain. Toxicol Mech Methods 21:171-182. doi: 10.3109/15376516.2010.538753
43. Lochhead JJ, Thorne RG (2012) Intranasal delivery of biologics to the central nervous system. Adv Drug Deliv Rev 64:614-628. doi: 10.1016/j.addr.2011. 11.002
44. Mainini V, Angel PM, Magni F, Caprioli RM (2011) Detergent enhancement of on-tissue protein analysis by matrix-assisted laser desorption/ionization imaging mass spectrometry. Rapid Commun Mass Spectrom 25:199-204. doi: 10.1002/rcm.4850
45. McDonnell LA, Heeren RMA (2007) Imaging mass spectrometry. Mass Spectrom Rev 26:606-643. doi: 10.1002/mas.20124 (Pubitemid 47169781)
46. Merkus P, Guchelaar HJ, Bosch A, Merkus F (2003) Direct access of drugs to the human brain after intranasal drug administration? Neurology 60:1669-1671. doi: 10.1212/01.WNL.0000067993.60735.77 (Pubitemid 36618097)
47. Nayyar T, Bubser M, Ferguson MC, Neely MD, Goodwin JS, Montine TJ, Deutch AY, Ansah TA (2009) Cortical serotonin and norepinephrine denervation in parkinsonism: preferential loss of the beaded serotonin innervation. Eur J Neurosci 30:207-216. doi: 10.1111/j.1460-9568.2009.06806.x
48. Norris JL, Cornett DS, Mobley JA, Andersson M, Seeley EH, Chaurand P, Caprioli RM (2007) Processing MALDI mass spectra to improve mass spectral direct tissue analysis. Int J Mass Spectrom 260:212-221. doi: 10.1016/j.ijms.2006.10. 005
49. Pain S, Gochard A, Bodard S, Gulhan Z, Prunier-Aesch C, Chalon S (2012) Toxicity of MPTP on neurotransmission in three mouse models of Parkinson's disease. Exp Toxicol Pathol 65:689-694. doi: 10.1016/j.etp.2012.09.001
50. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic Press, San Diego
51. Pifl C, Schingnitz G, Hornykiewicz O (1991) Effect of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine on the regional distribution of brain monoamines in the rhesus-monkey. Neuroscience 44:591-605. doi: 10.1016/0306-4522(91)90080-8
52. Pifl C, Hornykiewicz O, Giros B, Caron MG (1996) Catecholamine transporters and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine neurotoxicity: studies comparing the cloned human noradrenaline and human dopamine transporter. J Pharmacol Exp Ther 277:1437-1443
53. Pirman DA, Reich RF, Kiss A, Heeren RMA, Yost RA (2013) Quantitative MALDI tandem mass spectrometric imaging of cocaine from brain tissue with a deuterated internal standard. Anal Chem 85:1081-1089. doi: 10.1021/ac302960j
54. Prediger RDS, Aguiar AS, Rojas-Mayorquin AE, Figueiredo CP, Matheus FC, Ginestet L, Chevarin C, Del Bel E, Mongeau R, Hamon M, Lanfumey L, Raisman-Vozari R (2010) Single intranasal administration of 1-methyl-4-phenyl-1, 2,3,6-tetrahydropyridine in C57BL/6 mice models early preclinical phase of Parkinson's disease. Neurotox Res 17:114-129. doi: 10.1007/s12640-009-9087-0
55. Prediger RDS, Aguiar AS Jr, Matheus FC, Walz R, Antoury L, Raisman-Vozari R, Doty RL (2012) Intranasal administration of neurotoxicants in animals: support for the olfactory vector hypothesis of Parkinson's disease. Neurotox Res 21:90-116. doi: 10.1007/s12640-011-9281-8
56. Prideaux B, Stoeckli M (2012) Mass spectrometry imaging for drug distribution studies. J Proteomics 75:4999-5013. doi: 10.1016/j.jprot.2012.07. 028
57. Prideaux B, Dartois V, Staab D, Weiner DM, Goh A, Via LE, Barry CE, Stoeckli M (2011) High-sensitivity MALDI-MRM-MS imaging of moxifloxacin distribution in tuberculosis-infected rabbit lungs and granulomatous lesions. Anal Chem 83:2112-2118. doi: 10.1021/ac1029049
58. Przedborski S, Chen QP, Vila M, Giasson BI, Djaldatti R, Vukosavic S, Souza JM, Jackson-Lewis V, Lee VMY, Ischiropoulos H (2001) Oxidative post-translational modifications of alpha-synuclein in the 1-methyl-4-phenyl-1, 2,3,6-tetrahydropyridine (MPTP) mouse model of Parkinson's disease. J Neurochem 76:637-640. doi: 10.1046/j.1471-4159.2001.00174.x (Pubitemid 32097040)
59. Rojo AI, Montero C, Salazar M, Close RM, Fernandez-Ruiz J, Sanchez-Gonzalez MA, de Sagarra MR, Jackson-Lewis V, Cavada C, Cuadrado A (2006) Persistent penetration of MPTP through the nasal route induces Parkinson's disease in mice. Eur J Neurosci 24:1874-1884. doi: 10.1111/j.1460-9568.206. 05060.x (Pubitemid 44583472)
60. Rozas G, Liste I, Guerra MJ, Labandeira-Garcia JL (1998) Sprouting of the serotonergic afferents into striatum after selective lesion of the dopaminergic system by MPTP in adult mice. Neurosci Lett 245:151-154. doi: 10.1016/s0304-3940(98)00198-0 (Pubitemid 28287345)
61. Salach JI, Singer TP, Castagnoli N, Trevor A (1984) Oxidation of the neurotoxic amine 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) by monoamine oxidase-a and oxidase-b and suicide inactivation of the enzymes by MPTP. Biochem Biophys Res Commun 125:831-835. doi: 10.1016/0006-291x(84)90614-4 (Pubitemid 15155769)
62. Scatton B, Javoy-Agid F, Rouquier L, Dubois B, Agid Y (1983) Reduction of cortical dopamine, noradrenaline, serotonin and their metabolites in Parkinson's disease. Brain Res 275:321-328. doi: 10.1016/0006-8993(83)90993-9 (Pubitemid 13004530)
63. Scranton RA, Fletcher L, Sprague S, Jimenez DF, Digicaylioglu M (2011) The rostral migratory stream plays a key role in intranasal delivery of drugs into the CNS. PLoS ONE 6:018711. doi: 10.1371/journal.pone.0018711
64. Setou M (ed) (2010) Imaging mass spectrometry. Springer, Dordrecht. doi: 10.1007/978-4-431-09425-8
65. Stoeckli M, Staab D, Schweitzer A (2007) Compound and metabolite distribution measured by MALDI mass spectrometric imaging in whole-body tissue sections. Int J Mass Spectrom 260:195-202. doi: 10.1016/j.ijms.2006.10.007
66. Sugiura Y, Setou M (2009) Selective imaging of positively charged polar and nonpolar lipids by optimizing matrix solution composition. Rapid Commun Mass Spectrom 23:3269-3278. doi: 10.1002/rcm.4242
67. Taylor JW, Kaiser ET (1986) The structural characterization of beta-endorphin and related peptide-hormones and neurotransmitters. Pharmacol Rev 38:291-319 (Pubitemid 17229058)
68. Thorne RG, Emory CR, Ala TA, Frey WH (1995) Quantitative-analysis of the olfactory pathway for drug-delivery to the brain. Brain Res 692:278-282. doi: 10.1016/0006-8993(95)00637-6
69. Thorne RG, Pronk GJ, Padmanabhan V, Frey WH (2004) Delivery of insulin-like growth factor-I to the rat brain and spinal cord along olfactory and trigeminal pathways following intranasal administration. Neuroscience 127:481-496. doi: 10.1016/j.neuroscience.2004.05.029 (Pubitemid 38950662)
70. Touboul D, Piednoël H, Voisin V, De La Porte S, Brunelle A, Halgand F, Laprévote O (2004) Changes in phospholipid composition within the dystrophic muscle by matrix-assisted laser desorption/ionization mass spectrometry and mass spectrometry imaging. Eur J Mass Spectrom 10:657-664. doi: 10.1255/ejms.671 (Pubitemid 39611657)
71. Touboul D, Brunelle A, Halgand F, De La Porte S, Laprévote O (2005) Lipid imaging by gold cluster time-of-flight secondary ion mass spectrometry: application to Duchenne muscular dystrophy. J Lipid Res 46:1388-1395. doi: 10.1194/jlr.M500058-JLR200 (Pubitemid 43109802)
72. Touboul D, Roy S, Germain DP, Chaminade P, Brunelle A, Laprévote O (2007) MALDI-TOF and cluster-TOF-SIMS imaging of Fabry disease biomarkers. Int J Mass Spectrom 260:158-165. doi: 10.1016/j.ijms.2006.09.027
73. Touboul D, Laprévote O, Brunelle A (2011) Micrometric molecular histology of lipids by mass spectrometry imaging. Curr Opin Chem Biol 15:725-732. doi: 10.1016/j.cbpa.2011.04.017
74. Uhl G, Hedreen JC, Price DLMD (1985) Parkinson's disease: loss of ineurons from the ventral tegmental area contralateral to therapeutic surgical lesions. Neurology 35:1215-1218 (Pubitemid 15003464)
75. + levels do not necessarily correlate with striatal dopamine levels after MPTP treatment in mice. Neurodegeneration 5:129-136. doi: 10.1006/neur.1996.0019 (Pubitemid 26248602)
76. Vila M, Jackson-Lewis V, Guegan C, Wu DC, Teismann P, Choi DK, Tieu K, Przedborski S (2001) The role of glial cells in Parkinson's disease. Curr Opin Neurol 14:483-489. doi: 10.1097/00019052-200108000-00009 (Pubitemid 32703541)
77. Vuckovic MG, Wood RI, Holschneider DP, Abernathy A, Togasaki DM, Smith A, Petzinger GM, Jakowec MW (2008) Memory, mood, dopamine, and serotonin in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse model of basal ganglia injury. Neurobiol Dis 32:319-327. doi: 10.1016/j.nbd.2008.07.015