Endogenous morphine-like compound immunoreactivity increases in parkinsonism

Brain

Volumn 134, Issue 8, 2011, Pages 2321-2338

  Charron, Giselle ^a,b   Doudnikoff, Evelyne ^a,b   Laux, Alexis ^c   Berthet, Amandine ^a,b   Porras, Gregory ^a,b   Canron, Marie Hélne ^a,b   Barroso Chinea, Pedro ^a,b   Li, Qin ^d   Qin, Chuan ^d   Nosten Bertrand, Marika ^e   Giros, Bruno ^e   Delalande, Franois ^f   Van Dorsselaer, Alain ^f   Vital, Anne ^a,b   Goumon, Yannick ^c   Bezard, Erwan ^a,b,d  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INSTITUT DES MALADIES NEURODÉGÉNÉRATIVES   (France)

^c Institut des Neurosciences Cellulaires et Intégratives UPR3212   (France)

^d INSTITUTE OF LABORATORY ANIMAL SCIENCE   (China)

^e SORBONNE UNIVERSITÉ   (France)

^f UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

astrocyte; dopamine; endogenous morphine; human; immunohistochemistry; medium spiny neuron; monkey; mouse; rat

Indexed keywords

CODEINE; LEVODOPA; MORPHINE; MORPHINE 3 GLUCURONIDE; MORPHINE 6 GLUCURONIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DEPRESSION; FATIGUE; GLIA CELL; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; MACACA; MALE; MOUSE; NONHUMAN; PAIN; PARKINSON DISEASE; PARKINSONISM; PHENOTYPE; PRIORITY JOURNAL; RAT; UPREGULATION;

EID: 80051991729     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr166     Document Type: Article

References (78)

1. Ahmed MR, Berthet A, Bychkov E, Porras G, Li Q, Bioulac BH, et al. Lentiviral overexpression of GRK6 alleviates L-dopa-induced dyskinesia in experimental Parkinson's disease. Sci Transl Med 2010; 2: 28ra28.
2. Albin RL, Young AB, Penney JB. The functional anatomy of basal ganglia disorders. Trends Neurosci 1989; 12: 366-75. (Pubitemid 19238787)
3. Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 1986; 9: 357-81. (Pubitemid 16055790)
4. Arun P, Ravikumar A, Leelamma S, Kurup PA. Endogenous alkaloids in the brain of rats loaded with tyrosine/tryptophan & in the serum of patients of neurodegenerative & psychiatric disorders. Indian J Med Res 1998; 107: 231-8. (Pubitemid 28297807)
5. Benoit-Marand M, Jaber M, Gonon F. Release and elimination of dopa-mine in vivo in mice lacking the dopamine transporter: functional consequences. Eur J Neurosci 2000; 12: 2985-92.
6. Berthet A, Porras G, Doudnikoff E, Stark H, Cador M, Bezard E, et al. Pharmacological analysis demonstrates dramatic alteration of D1 dopamine receptor neuronal distribution in the rat analog of L-DOPA-induced dyskinesia. J Neurosci 2009; 29: 4829-35.
7. Berton O, Guigoni C, Li Q, Bioulac BH, Aubert I, Gross CE, et al. Striatal overexpression of DeltaJunD resets L-DOPA-induced dyskinesia in a primate model of Parkinson disease. Biol Psychiatry 2009; 66: 554-61.
8. Bezard E, Ferry S, Mach U, Stark H, Leriche L, Boraud T, et al. Attenuation of levodopa-induced dyskinesia by normalizing dopamine D3 receptor function. Nature Med 2003a; 9: 762-67. (Pubitemid 36749227)
9. Bezard E, Gross CE. Compensatory mechanisms in experimental and human parkinsonism : towards a dynamic approach. Prog Neurobiol 1998; 55: 93-116. (Pubitemid 28218824)
10. Bezard E, Gross CE, Brotchie JM. Presymptomatic compensation in Parkinson's disease is not dopamine-mediated. Trends Neurosci 2003b; 26: 215-21. (Pubitemid 36412004)
11. Bianchi E, Alessandrini C, Guarna M, Tagliamonte A. Endogenous codeine and morphine are stored in specific brain neurons. Brain Res 1993; 627: 210-15. (Pubitemid 23313257)
12. Boettcher C, Fellermeier M, Drager B, Zenk MH. How human neuro-blastoma cells make morphine. Proc Natl Acad Sci USA 2005; 102: 8495-500. (Pubitemid 40862764)
13. Bourasset F, Cisternino S, Temsamani J, Scherrmann JM. Evidence for an active transport of morphine-6-beta-d-glucuronide but not P-glycoprotein- mediated at the blood-brain barrier. J Neurochem 2003; 86: 1564-7. (Pubitemid 37174273)
14. Brefel-Courbon C, Payoux P, Thalamas C, Ory F, Quelven I, Chollet F, et al. Effect of levodopa on pain threshold in Parkinson's disease: a clinical and positron emission tomography study. Mov Disord 2005; 20: 1557-63.
15. Brix-Christensen V, Goumon Y, Tonnesen E, Chew M, Bilfinger T, Stefano GB. Endogenous morphine is produced in response to cardio-pulmonary bypass in neonatal pigs. Acta Anaesthesiol Scand 2000; 44: 1204-8.
16. Brix-Christensen V, Tonnesen E, Sanchez RG, Bilfinger TV, Stefano GB. Endogenous morphine levels increase following cardiac surgery as part of the antiinflammatory response? Int J Cardiol 1997; 62: 191-7. (Pubitemid 28060149)
17. Cashaw JL. Determination of tetrahydropapaveroline in the urine of parkinsonian-patients receiving L-Dopa carbidopa (sinemet) therapy by high-performance liquid-chromatography. J Chromatogr Biomed Appl 1993a; 613: 267-73. (Pubitemid 23103582)
18. Cashaw JL. Tetrahydropapaveroline in brain-regions of rats after acute ethanol administration. Alcohol 1993b; 10: 133-8. (Pubitemid 23096842)
19. Chaudhuri KR, Odin P. The challenge of non-motor symptoms in Parkinson's disease. Prog Brain Res 2010; 184: 325-41.
20. Chaudhuri KR, Schapira AH. Non-motor symptoms of Parkinson's disease: dopaminergic pathophysiology and treatment. Lancet Neurol 2009; 8: 464-74.
21. Dumartin B, Caillé I, Gonon F, Bloch B. Internalization of D1 dopamine receptor in striatal neurons in vivo as evidence of activation by dopa-mine agonists. J Neurosci 1998; 18: 1650-1.
22. Dumartin B, Jaber M, Gonon F, Caron M, Giros B, Bloch B. Dopamine tone regulates D1 receptor trafficking and delivery in striatal neurons in dopamine trasnporter deficient mice. Proc Natl Acad Sci USA 2000; 97: 1879-84. (Pubitemid 30118537)
23. Ferreira SH, Duarte ID, Lorenzetti BB. The molecular mechanism of action of peripheral morphine analgesia: stimulation of the cGMP system via nitric oxide release. Eur J Pharmacol 1991; 201: 121-2.
24. Ford B. Pain in Parkinson's disease. Mov Disord 2010; 25 (Suppl 1): S98-S103.
25. Gintzler AR, Gershon MD, Spector S. A nonpeptide morphine-like compound: immunocytochemical localization in the mouse brain. Science 1978; 199: 447-8. (Pubitemid 8304180)
26. Giros B, Jaber M, Jones SR, Wightman RM, Caron MG. Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 1996; 379: 606-12. (Pubitemid 26052818)
27. Glattard E, Welters ID, Lavaux T, Muller AH, Laux A, Zhang D, et al. Endogenous morphine levels are increased in sepsis: a partial implication of neutrophils. PLoS One 2010; 5: e8791.
28. Gold SJ, Hoang CV, Potts BW, Porras G, Pioli E, Kim KW, et al. RGS9-2 negatively modulates L-3,4-dihydroxyphenylalanine-induced dyskin-esia in experimental Parkinson's disease. J Neurosci 2007; 27: 14338-48.
29. Goumon Y, Laux A, Muller A, Aunis D. Central and peripheral endogenous morphine. An R Acad Nac Farm 2009; 75: 389-418.
30. Goumon Y, Muller A, Glattard E, Marban C, Gasnier C, Strub JM, et al. Identification of morphine-6-glucuronide in chromaffin cell secretory granules. J Biol Chem 2006; 281: 8082-9. (Pubitemid 43847426)
31. Grobe N, Lamshoft M, Orth RG, Drager B, Kutchan TM, Zenk MH, et al. Urinary excretion of morphine and biosynthetic precursors in mice. Proc Natl Acad Sci USA 2010; 107: 8147-52.
32. Grobe N, Ren X, Kutchan TM, Zenk MH. An (R)-specific N-methyltransferase involved in human morphine biosynthesis. Arch Biochem Biophys 2011; 506: 42-7.
33. Guigoni C, Doudnikoff E, Li Q, Bloch B, Bezard E. Altered D1 dopamine receptor trafficking in parkinsonian and dyskinetic non-human primates. Neurobiol Dis 2007; 26: 452-63. (Pubitemid 46561343)
34. Guigoni C, Dovero S, Aubert I, Qin L, Bioulac BH, Bloch B, et al. Levodopa-induced dyskinesia in MPTP-treated macaque is not dependent of the extent and pattern of the nigrostrial lesion. Eur J Neurosci 2005; 22: 283-7. (Pubitemid 41059995)
35. Heurtaux T, Benani A, Moulin D, Muller N, Netter P, Minn A. Induction of UGT1A6 isoform by inflammatory conditions in rat astrocytes. Neuropharmacology 2006; 50: 317-28. (Pubitemid 43184360)
36. Hirrlinger J, Konig J, Dringen R. Expression of mRNAs of multidrug resistance proteins (Mrps) in cultured rat astrocytes, oligodendrocytes, microglial cells and neurones. J Neurochem 2002; 82: 716-19. (Pubitemid 34831509)
37. Hirrlinger J, Moeller H, Kirchhoff F, Dringen R. Expression of multidrug resistance proteins (Mrps) in astrocytes of the mouse brain: a single cell RT-PCR study. Neurochem Res 2005; 30: 1237-44. (Pubitemid 41772270)
38. Hnasko TS, Sotak BN, Palmiter RD. Morphine reward in dopamine-deficient mice. Nature 2005; 438: 854-7. (Pubitemid 41753067)
39. Hornykiewicz O. Dopamine and brain function. Pharmacol Rev 1966; 18: 925-64.
40. Iversen L. Neurotransmitter transporters and their impact on the development of psychopharmacology. Br J Pharmacol 2006; 147 (Suppl 1): S82-88. (Pubitemid 43077265)
41. Jaeger CB. Cytoarchitectonics of substantia nigra grafts: a light and electron microscopic study of immunocytochemically identified dopamin-ergic neurons and fibrous astrocytes. J Comp Neurol 1985; 231: 121-35. (Pubitemid 15199490)
42. Johansson PA, Andersson M, Andersson KE, Cenci MA. Alterations in cortical and basal ganglia levels of opioid receptor binding in a rat model of l-DOPA-induced dyskinesia. Neurobiol Dis 2001; 8: 220-39. (Pubitemid 32382477)
43. Jones SR, Gainetdinov RR, Jaber M, Giros B, Wightman RM, Caron MG. Profound neuronal plasticity in response to inactivation of the dopa-mine transporter. Proc Natl Acad Sci USA 1998; 95: 4029-34. (Pubitemid 28173248)
44. Kacem K, Lacombe P, Seylaz J, Bonvento G. Structural organization of the perivascular astrocyte endfeet and their relationship with the endothelial glucose transporter: a confocal microscopy study. Glia 1998; 23: 1-10. (Pubitemid 28174041)
45. Katsarou Z, Bostantjopoulou S, Hatzizisi O, Giza E, Soler-Cardona A, Kyriazis G. Immune factors or depression? Fatigue correlates in Parkinson's disease. Rev Neurol 2007; 45: 725-8.
46. Konradi C, Westin JE, Carta M, Eaton ME, Kuter K, Dekundy A, et al. Transcriptome analysis in a rat model of L-DOPA-induced dyskinesia. Neurobiol Dis 2004; 17: 219-36. (Pubitemid 39345778)
47. Kummer A, Teixeira AL. Depressive disorders in Parkinson's disease may be due to a shared immune-mediated neurodegenerative process. Med Hypotheses 2008; 70: 201-2. (Pubitemid 350161187)
48. Laux A, Muller AH, Miehe M, Dirrig-Grosch S, Deloulme JC, Delalande F, et al. Mapping of endogenous morphine-like compounds in the adult mouse brain: evidence of their localization in astrocytes and GABAergic cells. J Comp Neurol 2011; 519: 2390-416.
49. Majeed NH, Przewlocka B, Machelska H, Przewlocki R. Inhibition of nitric oxide synthase attenuates the development of morphine tolerance and dependence in mice. Neuropharmacology 1994; 33: 189-92. (Pubitemid 24104280)
50. Mallet N, Ballion B, Le Moine C, Gonon F. Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinso-nian rats. J Neurosci 2006; 26: 3875-84.
51. Mallet N, Le Moine C, Charpier S, Gonon F. Feedforward inhibition of projection neurons by fast-spiking GABA interneurons in the rat stri-atum in vivo. J Neurosci 2005; 25: 3857-69. (Pubitemid 40570419)
52. Matsubara K, Fukushima S, Akane A, Kobayashi S, Shiono H. Increased urinary morphine, codeine and tetrahydropapaveroline in parkinsonian patient undergoing L-3,4-dihydroxyphenylalanine therapy: a possible biosynthetic pathway of morphine from L-3,4-dihydroxyphenylalanine in humans. J Pharmacol Exp Ther 1992; 260: 974-8.
53. Molina PE, Hashiguchi Y, Meijerink WJ, Naukam RJ, Boxer R, Abumrad NN. Modulation of endogenous opiate production: effect of fasting. Biochem Biophys Res Commun 1995; 207: 312-7.
54. Muller A, Glattard E, Taleb O, Kemmel V, Laux A, Miehe M, et al. Endogenous morphine in SH-SY5Y cells and the mouse cerebellum. PLoS One 2008; 3: e1641.
55. Muzzi C, Bertocci E, Terzuoli L, Porcelli B, Ciari I, Pagani R, et al. Simultaneous determination of serum concentrations of levodopa, dopamine, 3-O-methyldopa and alpha-methyldopa by HPLC. Biomed Pharmacother 2008; 62: 253-8. (Pubitemid 351626443)
56. Nadjar A, Brotchie JM, Guigoni C, Li Q, Zhou SB, Wang GJ, et al. Phenotype of striatofugal medium spiny neurons in parkinsonian and dyskinetic nonhuman primates: a call for a reappraisal of the functional organization of the basal ganglia. J Neurosci 2006; 26: 8653-61. (Pubitemid 44319400)
57. Neri C, Ghelardini C, Sotak B, Palmiter RD, Guarna M, Stefano G, et al. Dopamine is necessary to endogenous morphine formation in mammalian brain in vivo. J Neurochem 2008; 106: 2337-44.
58. Pan YX. Diversity and complexity of the mu opioid receptor gene: alternative pre-mRNA splicing and promoters. DNA Cell Biol 2005; 24: 736-50.
59. Parent A, Cote PY, Lavoie B. Chemical anatomy of primate basal ganglia. Prog Neurobiol 1995; 46: 131-97.
60. Pasternak GW. When it comes to opiates, just say NO. J Clin Invest 2007; 117: 3185-7. (Pubitemid 350096976)
61. Poeaknapo C, Schmidt J, Brandsch M, Drager B, Zenk MH. Endogenous formation of morphine in human cells. Proc Natl Acad Sci USA 2004; 101: 14091-6. (Pubitemid 39305035)
62. Prensa L, Parent A. The Nigrostriatal Pathway in the Rat: A single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J Neurosci 2001; 21: 7247-60. (Pubitemid 32846972)
63. Przewlocki R, Machelska H, Przewlocka B. Inhibition of nitric oxide syn-thase enhances morphine antinociception in the rat spinal cord. Life Sci 1993; 53: PL1-PL5.
64. Raponi E, Agenes F, Delphin C, Assard N, Baudier J, Legraverend C, et al. S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 2007; 55: 165-77. (Pubitemid 46036463)
65. Sango K, Maruyama W, Matsubara K, Dostert P, Minami C, Kawai M, et al. Enantio-selective occurrence of (S)-tetrahydropapaveroline in human brain. Neurosci Lett 2000; 283: 224-6. (Pubitemid 30168973)
66. Schestatsky P, Kumru H, Valls-Sole J, Valldeoriola F, Marti MJ, Tolosa E, et al. Neurophysiologic study of central pain in patients with Parkinson disease. Neurology 2007; 69: 2162-9. (Pubitemid 350294696)
67. Schuster S, Doudnikoff E, Rylander D, Berthet A, Aubert I, Ittrich C, et al. Antagonizing L-type Ca2 + channel reduces development of abnormal involuntary movement in the rat model of L-3,4-dihydrox-yphenylalanine-induced dyskinesia. Biol Psychiatry 2009; 65: 518-26.
68. Schuster S, Nadjar A, Guo JT, Li Q, Ittrich C, Hengerer B, et al. The 3-hydroxy-3-methylglutaryl-CoA reductase inhibitor lovastatin reduces severity of L-DOPA-induced abnormal involuntary movements in experimental Parkinson's disease. J Neurosci 2008; 28: 4311-6.
69. Somogyi AA, Barratt DT, Coller JK. Pharmacogenetics of opioids. Clin Pharmacol Ther 2007; 81: 429-44. (Pubitemid 46364493)
70. Soto-Otero R, Sanmartin-Suarez C, Sanchez-Iglesias S, Hermida-Ameijeiras A, Sanchez-Sellero I, Mendez-Alvarez E. The ability of 1,2,3,4- Tetrahydropapaveroline to cause oxidative stress: potential implications in relation to Parkinson's disease. J Neurochem 2004; 90: 94-94.
71. Soto-Otero R, Sanmartin-Suarez C, Sanchez-Iglesias S, Hermida-Ameijeiras A, Sanchez-Sellero I, Mendez-Alvarez E. Study on the ability of 1,2,3,4-tetrahydropapaveroline to cause oxidative stress: Mechanisms and potential implications in relation to Parkinson's disease. J Biochem Mol Toxicol 2006; 20: 209-20. (Pubitemid 44569557)
72. Stefano GB, Cadet P, Kream RM, Zhu W. The presence of endogenous morphine signaling in animals. Neurochem Res 2008; 33: 1933-9.
73. Stefano GB, Goumon Y, Casares F, Cadet P, Fricchione GL, Rialas C, et al. Endogenous morphine. Trends Neurosci 2000; 23: 436-42.
74. Stefano GB, Scharrer B, Smith EM, Hughes TK Jr, Magazine HI, Bilfinger TV, et al. Opioid and opiate immunoregulatory processes. Crit Rev Immunol 1996; 16: 109-44. (Pubitemid 26303717)
75. Suleman FG, Abid A, Gradinaru D, Daval JL, Magdalou J, Minn A. Identification of the uridine diphosphate glucuronosyltransferase iso-form UGT1A6 in rat brain and in primary cultures of neurons and astrocytes. Arch Biochem Biophys 1998; 358: 63-7. (Pubitemid 28471374)
76. Thomas DM, Francescutti-Verbeem DM, Kuhn DM. The newly synthesized pool of dopamine determines the severity of methamphetamine-induced neurotoxicity. J Neurochem 2008; 105: 605-16. (Pubitemid 351562714)
77. Vital A, Fernagut PO, Canron MH, Joux J, Bezard E, Martin-Negrier ML, et al. The nigrostriatal pathway in Creutzfeldt-Jakob disease. J Neuropathol Exp Neurol 2009; 68: 809-15.
78. Weitz CJ, Faull KF, Goldstein A. Synthesis of the skeleton of the morphine molecule by mammalian liver. Nature 1987; 330: 674-77.