Abnormal nociception and opiate sensitivity of STOP null mice exhibiting elevated levels of the endogenous alkaloid morphine

Molecular Pain

Volumn 6, Issue , 2010, Pages

  Charlet, Alexandre ^a   Muller, Arnaud H ^b   Laux, Alexis ^a,b   Kemmel, Véronique ^c   Schweitzer, Annie ^d   Deloulme, Jean Christophe ^d   Stuber, Denise ^a   Delalande, François ^e   Bianchi, Enrica ^f   Van Dorsselaer, Alain ^e   Aunis, Dominique ^b   Andrieux, Annie ^d   Poisbeau, Pierrick ^a   Goumon, Yannick ^a,b  

^a CNRS   (France)

^b INSERM   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^e INSTITUT DE RECHERCHES SUBATOMIQUES   (France)

^f UNIVERSITY OF SIENA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALMODULIN BINDING PROTEIN; MORPHINE; MU OPIATE RECEPTOR; NALOXONE; OPIATE; STABLE TUBULE ONLY POLYPEPTIDE; UNCLASSIFIED DRUG; MICROTUBULE ASSOCIATED PROTEIN; MTAP6 PROTEIN, MOUSE; NARCOTIC ANALGESIC AGENT; NARCOTIC ANTAGONIST; NERVE PROTEIN;

ANALGESIC ACTIVITY; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; BINDING AFFINITY; BRAIN CORTEX; BRAIN LEVEL; BRAIN REGION; CEREBELLUM; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG MEGADOSE; DRUG RECEPTOR BINDING; DRUG SENSITIVITY; HIPPOCAMPUS; LOW DRUG DOSE; MOUSE; NOCICEPTION; NONHUMAN; NULL ALLELE; PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SINGLE DRUG DOSE; SPINAL CORD; WILD TYPE; ANIMAL; METABOLISM; MOUSE MUTANT; PAIN; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANALGESICS, OPIOID; ANIMALS; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MORPHINE; NALOXONE; NARCOTIC ANTAGONISTS; NERVE TISSUE PROTEINS; OPIATE ALKALOIDS; PAIN; RECEPTORS, OPIOID, MU;

EID: 78650256753     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-6-96     Document Type: Article

References (61)

1. Denarier E, Aguezzoul M, Jolly C, Vourc'h C, Roure A, Andrieux A, Bosc C, Job D. Genomic structure and chromosomal mapping of the mouse STOP gene (Mtap6). Biochem Biophys Res Commun 1998, 243:791-796. 10.1006/bbrc.1998.8179, 9501006.
2. Denarier E, Fourest-Lieuvin A, Bosc C, Pirollet F, Chapel A, Margolis RL, Job D. Nonneuronal isoforms of STOP protein are responsible for microtubule cold stability in mammalian fibroblasts. Proc Natl Acad Sci USA 1998, 95:6055-6060. 10.1073/pnas.95.11.6055, 27584, 9600916.
3. Bosc C, Andrieux A, Job D. STOP proteins. Biochemistry 2003, 42:12125-12132. 10.1021/bi0352163, 14567673.
4. Aguezzoul M, Andrieux A, Denarier E. Overlap of promoter and coding sequences in the mouse STOP gene (Mtap6). Genomics 2003, 81:623-627. 10.1016/S0888-7543(03)00053-3, 12782132.
5. Baas PW, Heidemann SR. Microtubule reassembly from nucleating fragments during the regrowth of amputated neurites. J Cell Biol 1986, 103:917-927. 10.1083/jcb.103.3.917, 2114289, 3745275.
6. Guillaud L, Bosc C, Fourest-Lieuvin A, Denarier E, Pirollet F, Lafanechere L, Job D. STOP proteins are responsible for the high degree of microtubule stabilization observed in neuronal cells. J Cell Biol 1998, 142:167-179. 10.1083/jcb.142.1.167, 2133033, 9660871.
7. Schaar BT, McConnell SK. Cytoskeletal coordination during neuronal migration. Proc Natl Acad Sci USA 2005, 102:13652-13657. 10.1073/pnas.0506008102, 1199551, 16174753.
8. Tsai LH, Gleeson JG. Nucleokinesis in neuronal migration. Neuron 2005, 46:383-388. 10.1016/j.neuron.2005.04.013, 15882636.
9. Baratier J, Peris L, Brocard J, Gory-Faure S, Dufour F, Bosc C, Fourest-Lieuvin A, Blanchoin L, Salin P, Job D, Andrieux A. Phosphorylation of microtubule-associated protein STOP by calmodulin kinase II. J Biol Chem 2006, 281:19561-19569. 10.1074/jbc.M509602200, 16651267.
10. Gory-Faure S, Windscheid V, Bosc C, Peris L, Proietto D, Franck R, Denarier E, Job D, Andrieux A. STOP-like protein 21 is a novel member of the STOP family, revealing a Golgi localization of STOP proteins. J Biol Chem 2006, 281:28387-28396. 10.1074/jbc.M603380200, 16837464.
11. Andrieux A, Salin PA, Vernet M, Kujala P, Baratier J, Gory-Faure S, Bosc C, Pointu H, Proietto D, Schweitzer A, Denarier E, Klumperman J, Job D. The suppression of brain cold-stable microtubules in mice induces synaptic defects associated with neuroleptic-sensitive behavioral disorders. Genes Dev 2002, 16:2350-2364. 10.1101/gad.223302, 187434, 12231625.
12. Brun P, Begou M, Andrieux A, Mouly-Badina L, Clerget M, Schweitzer A, Scarna H, Renaud B, Job D, Suaud-Chagny MF. Dopaminergic transmission in STOP null mice. J Neurochem 2005, 94:63-73. 10.1111/j.1471-4159.2005.03166.x, 15953350.
13. Begou M, Volle J, Bertrand JB, Brun P, Job D, Schweitzer A, Saoud M, D'Amato T, Andrieux A, Suaud-Chagny MF. The stop null mice model for schizophrenia displays cognitive and social deficits partly alleviated by neuroleptics. Neuroscience 2008, 157:29-39. 10.1016/j.neuroscience.2008.07.080, 18804150.
14. Fradley RL, O'Meara GF, Newman RJ, Andrieux A, Job D, Reynolds DS. STOP knockout and NMDA NR1 hypomorphic mice exhibit deficits in sensorimotor gating. Behav Brain Res 2005, 163:257-264. 10.1016/j.bbr.2005.05.012, 16046005.
15. Zervas M, Opitz T, Edelmann W, Wainer B, Kucherlapati R, Stanton PK. Impaired hippocampal long-term potentiation in microtubule-associated protein 1B-deficient mice. J Neurosci Res 2005, 82:83-92. 10.1002/jnr.20624, 16118800.
16. Eastwood SL, Lyon L, George L, Andrieux A, Job D, Harrison PJ. Altered expression of synaptic protein mRNAs in STOP (MAP6) mutant mice. J Psychopharmacol 2007, 21:635-644. 10.1177/0269881106068825, 17050659.
17. Charlton JJ, Allen PB, Psifogeorgou K, Chakravarty S, Gomes I, Neve RL, Devi LA, Greengard P, Nestler EJ, Zachariou V. Multiple actions of spinophilin regulate mu opioid receptor function. Neuron 2008, 58:238-247. 10.1016/j.neuron.2008.02.006, 18439408.
18. Stefano GB, Goumon Y, Casares F, Cadet P, Fricchione GL, Rialas C, Peter D, Sonetti D, Guarna M, Welters ID, Bianchi E. Endogenous morphine. Trends Neurosci 2000, 23:436-442. 10.1016/S0166-2236(00)01611-8, 10941194.
19. Herbert RB, Venter H, Pos S. Do mammals make their own morphine?. Nat Prod Rep 2000, 17:317-322. 10.1039/a809409h, 11014334.
20. Goumon Y, Laux A, Muller A, Aunis D. Central and Peripheral Endogenous Morphine. An R Acad Nac Farm 2009, 75:389-418.
21. Glattard E, Welters ID, Lavaux T, Muller A, Laux A, Zhang D, Schmidt AR, Delalande F, Lavantie BJ, Dirrig-Grosch S, Colin DA, Van Dorsselaer A, Aunis D, Metz-Boutigue MH, Schneider F, Goumon Y. Endogenous Morphine Levels are Increased in Sepsis: a Partial Implication of Neutrophils. PLoS One 2010, 1:e8791.
22. Goumon Y, Muller A, Glattard E, Marban C, Gasnier C, Strub JM, Chasserot-Golaz S, Rohr O, Stefano GB, Welters ID, Van Dorsselaer A, Schoentgen F, Aunis D, Metz-Boutigue MH. Identification of Morphine-6-glucuronide in Chromaffin Cell Secretory Granules. J Biol Chem 2006, 281:8082-8089. 10.1074/jbc.M502298200, 16434406.
23. Muller A, Glattard E, Taleb O, Kemmel V, Laux A, Miehe M, Delalande F, G R, Van Dorsselaer A, Metz-Boutigue MH, Aunis D, Goumon Y. Endogenous Morphine in SH-SY5Y Cells and the Mouse Cerebellum. PLoS One 2008, 3. 2265639, 18327293., http://www.plosone.org/doi/pone.0001641
24. Hazum E, Sabatka JJ, Chang KJ, Brent DA, Findlay JW, Cuatrecasas P. Morphine in cow and human milk: could dietary morphine constitute a ligand for specific morphine (mu) receptors?. Science 1981, 213:1010-1012. 10.1126/science.6267691, 6267691.
25. Goldstein A, Barrett RW, James IF, Lowney LI, Weitz CJ, Knipmeyer LL, Rapoport H. Morphine and other opiates from beef brain and adrenal. Proc Natl Acad Sci USA 1985, 82:5203-5207. 10.1073/pnas.82.15.5203, 390528, 3860854.
26. Goumon Y, Bouret S, Casares F, Zhu W, Beauvillain JC, Stefano GB. Lipopolysaccharide increases endogenous morphine levels in rat brain. Neurosci Lett 2000, 293:135-138. 10.1016/S0304-3940(00)01507-X, 11027852.
27. Gintzler AR, Gershon MD, Spector S. A nonpeptide morphine-like compound: immunocytochemical localization in the mouse brain. Science 1978, 199:447-448. 10.1126/science.339350, 339350.
28. Guarna M, Bianchi E, Bartolini A, Ghelardini C, Galeotti N, Bracci L, Neri C, Sonetti D, Stefano G. Endogenous morphine modulates acute thermonociception in mice. J Neurochem 2002, 80:271-277. 10.1046/j.0022-3042.2001.00708.x, 11902117.
29. Bianchi E, Guarna M, Tagliamonte A. Immunocytochemical localization of endogenous codeine and morphine. Adv Neuroimmunol 1994, 4:83-92. 10.1016/S0960-5428(05)80003-8, 7952831.
30. Zhu W, Ma Y, Bell A, Esch T, Guarna M, Bilfinger TV, Bianchi E, Stefano GB. Presence of morphine in rat amygdala: evidence for the mu3 opiate receptor subtype via nitric oxide release in limbic structures. Med Sci Monit 2004, 10:BR433-439.
31. Bianchi E, Alessandrini C, Guarna M, Tagliamonte A. Endogenous codeine and morphine are stored in specific brain neurons. Brain Res 1993, 627:210-215. 10.1016/0006-8993(93)90323-F, 8298964.
32. Boettcher C, Fellermeier M, Boettcher C, Drager B, Zenk MH. How human neuroblastoma cells make morphine. Proc Natl Acad Sci USA 2005, 102:8495-8500. 10.1073/pnas.0503244102, 1150847, 15937106.
33. Kream RM, Stefano GB. De novo biosynthesis of morphine in animal cells: An evidence-based model. Med Sci Monit 2006, 12:RA207-219.
34. Neri C, Ghelardini C, Sotak B, Palmiter RD, Guarna M, Stefano G, Bianchi E. Dopamine is necessary to endogenous morphine formation in mammalian brain in vivo. J Neurochem 2008, 106:2337-2344. 10.1111/j.1471-4159.2008.05572.x, 18643791.
35. Poeaknapo C, Schmidt J, Brandsch M, Drager B, Zenk MH. Endogenous formation of morphine in human cells. Proc Natl Acad Sci USA 2004, 101:14091-14096. 10.1073/pnas.0405430101, 521124, 15383669.
36. Lotsch J, Geisslinger G. Morphine-6-glucuronide: an analgesic of the future?. Clin Pharmacokinet 2001, 40:485-499. 10.2165/00003088-200140070-00001, 11510626.
37. Cadet P, Mantione KJ, Stefano GB. Molecular identification and functional expression of mu 3, a novel alternatively spliced variant of the human mu opiate receptor gene. J Immunol 2003, 170:5118-5123.
38. Cadet P, Mantione KJ, Zhu W, Kream RM, Sheehan M, Stefano GB. A functionally coupled mu3-like opiate receptor/nitric oxide regulatory pathway in human multi-lineage progenitor cells. J Immunol 2007, 179:5839-5844.
39. Aloisi AM, Aurilio C, Bachiocco V, Biasi G, Fiorenzani P, Pace MC, Paci V, Pari G, Passavanti G, Ravaioli L, Sindaco G, Vellucci R, Ceccarelli I. Endocrine consequences of opioid therapy. Psychoneuroendocrinology 2009, 34(Suppl 1):S162-168. 10.1016/j.psyneuen.2009.05.013, 19540049.
40. Loeser JD, Treede RD. The Kyoto protocol of IASP Basic Pain Terminology. Pain 2008, 137:473-477. 10.1016/j.pain.2008.04.025, 18583048.
41. Doyle GA, Sheng XR, Lin SS, Press DM, Grice DE, Buono RJ, Ferraro TN, Berrettini WH. Identification of five mouse mu-opioid receptor (MOR) gene (Oprm1) splice variants containing a newly identified alternatively spliced exon. Gene 2007, 395:98-107. 10.1016/j.gene.2007.02.004, 2573390, 17398041.
42. Skyers PS, Einheber S, Pierce JP, Milner TA. Increased mu-opioid receptor labeling is found on inner molecular layer terminals of the dentate gyrus following seizures. Exp Neurol 2003, 179:200-209. 10.1016/S0014-4886(02)00018-3, 12618127.
43. Sargeant TJ, Day DJ, Mrkusich EM, Foo DF, Miller JH. Mu opioid receptors are expressed on radial glia but not migrating neuroblasts in the late embryonic mouse brain. Brain Res 2007, 1175:28-38. 10.1016/j.brainres.2007.07.091, 17888889.
44. Zhang Y, Pan YX, Kolesnikov Y, Pasternak GW. Immunohistochemical labeling of the mu opioid receptor carboxy terminal splice variant mMOR-1B4 in the mouse central nervous system. Brain Res 2006, 1099:33-43. 10.1016/j.brainres.2006.04.133, 16793025.
45. Pawar M, Kumar P, Sunkaraneni S, Sirohi S, Walker EA, Yoburn BC. Opioid agonist efficacy predicts the magnitude of tolerance and the regulation of mu-opioid receptors and dynamin-2. Eur J Pharmacol 2007, 563:92-101. 10.1016/j.ejphar.2007.01.059, 1995431, 17349996.
46. Brady LS, Herkenham M, Long JB, Rothman RB. Chronic morphine increases mu-opiate receptor binding in rat brain: a quantitative autoradiographic study. Brain Res 1989, 477:382-386. 10.1016/0006-8993(89)91432-7, 2539233.
47. Bergasa NV, Rothman RB, Mukerjee E, Vergalla J, Jones EA. Up-regulation of central mu-opioid receptors in a model of hepatic encephalopathy: a potential mechanism for increased sensitivity to morphine in liver failure. Life Sci 2002, 70:1701-1708. 10.1016/S0024-3205(02)01487-X, 11991257.
48. Guarna M, Ghelardini C, Galeotti N, Bartolini A, Noli L, Neri C, Stefano GB, Bianchi E. Effects of endogenous morphine deprivation on memory retention of passive avoidance learning in mice. Int J Neuropsychopharmacol 2004, 7:311-319. 10.1017/S1461145704004341, 15320957.
49. van Dorp EL, Kest B, Kowalczyk WJ, Morariu AM, Waxman AR, Arout CA, Dahan A, Sarton EY. Morphine-6beta-glucuronide Rapidly Increases Pain Sensitivity Independently of Opioid Receptor Activity in Mice and Humans. Anesthesiology 2009, 110:1356-1363. 10.1097/ALN.0b013e3181a105de, 19461298.
50. Liang D, Shi X, Qiao Y, Angst MS, Yeomans DC, Clark JD. Chronic morphine administration enhances nociceptive sensitivity and local cytokine production after incision. Mol Pain 2008, 4:7. 10.1186/1744-8069-4-7, 2279109, 18294378.
51. Li X, Angst MS, Clark JD. Opioid-induced hyperalgesia and incisional pain. Anesth Analg 2001, 93:204-209. 10.1097/00000539-200107000-00040, 11429366.
52. Crain SM, Shen KF. Opioids can evoke direct receptor-mediated excitatory effects on sensory neurons. Trends Pharmacol Sci 1990, 11:77-81. 10.1016/0165-6147(90)90322-Y, 2156364.
53. Crain SM, Shen KF. Ultra-low concentrations of naloxone selectively antagonize excitatory effects of morphine on sensory neurons, thereby increasing its antinociceptive potency and attenuating tolerance/dependence during chronic cotreatment. Proc Natl Acad Sci USA 1995, 92:10540-10544. 10.1073/pnas.92.23.10540, 40647, 7479836.
54. Powell KJ, Abul-Husn NS, Jhamandas A, Olmstead MC, Beninger RJ, Jhamandas K. Paradoxical effects of the opioid antagonist naltrexone on morphine analgesia, tolerance, and reward in rats. J Pharmacol Exp Ther 2002, 300:588-596. 10.1124/jpet.300.2.588, 11805221.
55. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53:55-63. 10.1016/0165-0270(94)90144-9, 7990513.
56. Yalcin I, Charlet A, Freund-Mercier MJ, Barrot M, Poisbeau P. Differentiating thermal allodynia and hyperalgesia using dynamic hot and cold plate in rodents. J Pain 2009, 10:767-773. 10.1016/j.jpain.2009.01.325, 19409860.
57. Hedou G, Chasserot-Golaz S, Kemmel V, Gobaille S, Roussel G, Artault JC, Andriamampandry C, Aunis D, Maitre M. Immunohistochemical studies of the localization of neurons containing the enzyme that synthesizes dopamine, GABA, or gamma-hydroxybutyrate in the rat substantia nigra and striatum. J Comp Neurol 2000, 426:549-560. 10.1002/1096-9861(20001030)426:4<549::AID-CNE4>3.0.CO;2-Y, 11027398.
58. Goumon Y, Angelone T, Schoentgen F, Chasserot-Golaz S, Almas B, Fukami MM, Langley K, Welters ID, Tota B, Aunis D, Metz-Boutigue MH. The hippocampal cholinergic neurostimulating peptide, the N-terminal fragment of the secreted phosphatidylethanolamine-binding protein, possesses a new biological activity on cardiac physiology. J Biol Chem 2004, 279:13054-13064. 10.1074/jbc.M308533200, 14724289.
59. Coles R, Kushnir MM, Nelson GJ, McMillin GA, Urry FM. Simultaneous determination of codeine, morphine, hydrocodone, hydromorphone, oxycodone, and 6-acetylmorphine in urine, serum, plasma, whole blood, and meconium by LC-MS-MS. J Anal Toxicol 2007, 31:1-14.
60. Huang DK, Liu C, Huang MK, Chien CS. Simultaneous determination of morphine, codeine, 6-acetylmorphine, cocaine and benzoylecgonine in hair by liquid chromatography/electrospray ionization tandem mass spectrometry. Rapid Commun Mass Spectrom 2009, 23:957-962. 10.1002/rcm.3955, 19241414.
61. Rook EJ, Hillebrand MJ, Rosing H, van Ree JM, Beijnen JH. The quantitative analysis of heroin, methadone and their metabolites and the simultaneous detection of cocaine, acetylcodeine and their metabolites in human plasma by high-performance liquid chromatography coupled with tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 2005, 824:213-221. 10.1016/j.jchromb.2005.05.048, 16103023.