Genetic reduction of muscarinic M 4 receptor modulates analgesic response and acoustic startle response in a mouse model of fragile X syndrome (FXS)

Behavioural Brain Research

Volumn 228, Issue 1, 2012, Pages 1-8

  Veeraragavan, Surabi ^a   Graham, Deanna ^a   Bui, Nghiem ^a   Yuva Paylor, Lisa A ^a   Wess, Jürgen ^b   Paylor, Richard ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Analgesic response; Behavior; Fragile X syndrome; M 4 receptors; Muscarinic; Sensorimotor gating

Indexed keywords

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; AUDIOGENIC SEIZURE; CONTROLLED STUDY; FMR1 GENE; FRAGILE X SYNDROME; GENE; HEMIZYGOSITY; HETEROZYGOTE; HOT PLATE TEST; KNOCKOUT MOUSE; LEARNING; MALE; MEMORY; MOTOR COORDINATION; MOUSE; MUSCARINIC M4 RECEPTOR GENE; NEUROMODULATION; NONHUMAN; OPEN FIELD BEHAVIOR; PASSIVE AVOIDANCE; PERSEVERATION; PREPULSE INHIBITION; PRIORITY JOURNAL; ROTAROD TEST; SENSORY GATING; STARTLE REFLEX; TESTIS WEIGHT;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; ORGAN SIZE; PAIN MEASUREMENT; RECEPTOR, MUSCARINIC M4; STARTLE REACTION; TESTIS;

EID: 83655164085     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.11.018     Document Type: Article

References (59)

1. Hagerman R.J., Fragile Hagerman P.J. X syndrome: diagnosis, treatment, and research 2002, The Johns Hopkins University Press, Baltimore. 3rd ed.
2. Bakker C.E., Verheij C., Willemsen R., van der Helm R., Oerlemans F., Vermey M., et al. Fmr1 knockout mice: a model to study fragile X mental retardation. Cell 1994, 78(1):23-33.
3. Chen L., Fragile Toth M. X mice develop sensory hyperreactivity to auditory stimuli. Neuroscience 2001, 103(4):1043-1050.
4. Dobkin C., Rabe A., Dumas R., El Idrissi A., Haubenstock H., Brown W.T. Fmr1 knockout mouse has a distinctive strain-specific learning impairment. Neuroscience 2000, 100(2):423-429.
5. D'Hooge R., Nagels G., Franck F., Bakker C.E., Reyniers E., Storm K., et al. Mildly impaired water maze performance in male Fmr1 knockout mice. Neuroscience 1997, 76(2):367-376.
6. Frankland P.W., Wang Y., Rosner B., Shimizu T., Balleine B.W., Dykens E.M., et al. Sensorimotor gating abnormalities in young males with fragile X syndrome and Fmr1-knockout mice. Mol Psychiatry 2004, 9(4):417-425.
7. Musumeci S.A., Bosco P., Calabrese G., Bakker C., De Sarro G.B., Elia M., et al. Audiogenic seizures susceptibility in transgenic mice with fragile X syndrome. Epilepsia 2000, 41(1):19-23.
8. Nielsen D.M., Derber W.J., McClellan D.A., Crnic L.S. Alterations in the auditory startle response in Fmr1 targeted mutant mouse models of fragile X syndrome. Brain Res 2002, 927(1):8-17.
9. Spencer C.M., Alekseyenko O., Serysheva E., Yuva-Paylor L.A., Paylor R. Altered anxiety-related and social behaviors in the Fmr1 knockout mouse model of fragile X syndrome. Genes Brain Behav 2005, 4(7):420-430.
10. Yan Q.J., Asafo-Adjei P.K., Arnold H.M., Brown R.E., Bauchwitz R.P. A phenotypic and molecular characterization of the fmr1-tm1Cgr fragile X mouse. Genes Brain Behav 2004, 3(6):337-359.
11. Spencer C.M., Graham D.F., Yuva-Paylor L.A., Nelson D.L., Paylor R. Social behavior in Fmr1 knockout mice carrying a human FMR1 transgene. Behav Neurosci 2008, 122(3):710-715.
12. D'Antuono M., Merlo D., Avoli M. Involvement of cholinergic and gabaergic systems in the fragile X knockout mice. Neuroscience 2003, 119(1):9-13.
13. Volk L.J., Pfeiffer B.E., Gibson J.R., Huber K.M. Multiple Gq-coupled receptors converge on a common protein synthesis-dependent long-term depression that is affected in fragile X syndrome mental retardation. J Neurosci 2007, 27(43):11624-11634.
14. Caulfield M.P., Birdsall N.J. International Union of Pharmacology XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 1998, 50(2):279-290.
15. Levey A.I., Kitt C.A., Simonds W.F., Price D.L., Brann M.R. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci 1991, 11(10):3218-3226.
16. Levey A.I. Immunological localization of M1-M5 muscarinic acetycholine receptors in peripheral tissues and brains. Life Sci 1993, 52:441-448.
17. Yasuda R.P., Ciesla W., Flores L.R., Wall S.J., Li M., Satkus S.A., et al. Development of antisera selective for M4 and M5 muscarinic cholinergic receptors: distribution of M4 and M5 receptors in rat brain. Mol Pharmacol 1993, 43:149-157.
18. Wolfe B.B., Yasuda R.P. Development of selective antisera for muscarinic cholinergic receptor subtypes. Ann N Y Acad Sci 1995, 10:186-193.
19. Gomeza J., Zhang L., Kostenis E., Felder C., Bymaster F., Brondkin J., et al. Enhancement of D1 dopamine receptor-mediated locomotor stimulation in M4 muscarinic acetylcholine receptor knockout mice. Proc Natl Acad Sci USA 1999, 96:10483-10488.
20. Santiago M.P., Potter L.T. Biotinylated m4-toxin demonstrates more M4 muscarinic receptor protein on direct than indirect striatal projection neurons. Brain Res 2001, 894:12-20.
21. Oki T., Takagi Y., Inagaki S., Taketo M.M., Manabe T., Matsui M., et al. Quantitative analysis of binding parameters of [3H]N-methylscopolamine in central nervous system of muscarinic acetylcholine receptor knockout mice. Brain Res Mol Brain Res 2005, 133:6-11.
22. Thomsen M., Wess J., Fulton B.S., Fink-Jensen A., Caine S.B. Modulation of prepulse inhibition through both M(1) and M (4) muscarinic receptors in mice. Psychopharmacology 2010, 208(3):401-416.
23. Tzavara E.T., Bymaster F.P., Felder C.C., Wade M., Gomeza J., Wess J., et al. Dysregulated hippocampal acetylcholine neurotransmission and impaired cognition in M2, M4 and M2/M4 muscarinic receptor knockout mice. Mol Psychiatry 2003, 8:673-679.
24. Duttaroy A., Gomeza J., Gan J.W., Siddiqui N., Basile A.S., Harman W.D., et al. Evaluation of muscarinic agonist-induced analgesia in muscarinic acetylcholine receptor knockout mice. Mol Pharmacol 2002, 62(5):1084-1093.
25. Peier A.M., McIlwain K.L., Kenneson A., Warren S.T., Paylor R., Nelson D.L. (Over)correction of FMR1 deficiency with YAC transgenics: behavioral and physical features. Hum Mol Genet 2000, 9(8):1145-1159.
26. Qin M., Kang J., Smith C.B. Increased rates of cerebral glucose metabolism in a mouse model of fragile X mental retardation. Proc Natl Acad Sci USA 2002, 99(24):15758-15763.
27. Price T.J., Rashid M.H., Millecamps M., Sanoja R., Entrena J.M., et al. Decreased nociceptive sensitization in mice lacking the fragile X mental retardation protein: role of mGluR1/5 and mTOR. J Neurosci 2007, 27(51):13958-13967.
28. Spencer C.M., Alekseyenko O., Hamilton S.M., Thomas A.M., Serysheva E., Yuva-Paylor L.A., et al. Modifying behavioral phenotypes in Fmr1 KO mice: genetic background differences reveal autistic-like responses. Autism Res 2011, 4(1):40-56.
29. Veeraragavan S., Bui N., Perkins J.R., Paylor L.A., Paylor R. The modulation of fragile X behaviors by the muscarinic M4 antagonist, tropicamide. Behav Neurosci 2011, 125(5):783-790.
30. Veeraragavan S., Bui N., Perkins J.R., Yuva-Paylor L.A., Carpenter R.L., Paylor R. Modulation of behavioral phenotypes by a muscarinic M1 antagonist in a mouse model of fragile X syndrome. Psychopharmacology 2011, 217(1):143-151.
31. McIlwain K.L., Merriweather M.Y., Yuva-Paylor L.A., Paylor R. The use of behavioral test batteries: effects of training history. Physiol Behav 2001, 73:705-717.
32. Paylor R., Spencer C.M., Yuva-Paylor L.A., Pieke-Dahl S. The use of behavioral test batteries, II: effect of test interval. Physiol Behav 2006, 87(1):95-102.
33. Paylor R., Yuva-Paylor L.A., Nelson D.L., Spencer C.M. Reversal of sensorimotorgating abnormalities in Fmr1 knockout mice carrying a human FMR1 transgene. Behav Neurosci 2008, 122:1371-1377.
34. Thomas A., Burant A., Bui N., Graham D., Yuva-Paylor L.A., Paylor R. Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology (Berl) 2009, 204:361-373.
35. Yan Q.J., Rammal M., Tranfaglia M., Bauchwitz R.P. Suppression of two major fragile X syndrome mouse model phenotypes by the mGluR5 antagonist MPEP. Neuropharmacology 2005, 49:1053-1066.
36. Wess J., Duttaroy A., Gomeza J., Zhang W., Yamada M., Felder C.C., et al. Muscarinic receptor subtypes mediating central and peripheral antinociception studied with muscarinic receptor knockout mice: a review. Life Sci 2003, 72:2047-2054.
37. Thomas A.M., Bui N., Graham D., Perkins J.R., Yuva-Paylor L.A., Paylor R. Genetic reduction of group 1 metabotropic glutamate receptors alters select behaviors in a mouse model of Fragile X syndrome. Behav Brain Res 2011, 223:310-321.
38. Slegtenhorst-Eegdeman K.E., de Rooij D.G., Verhoef-Post M., van de Kant H.J., Bakker C.E., Oostra B.A., et al. Macroorchidism in FMR1 knockout mice is caused by increased sertoli cell proliferation during testicular development. Endocrinology 1998, 139(1):156-162.
39. Lucas T.F., Avellar M.C., Porto C.S. Effects of carbachol on rat sertoli cell proliferation and muscarinic acetylcholine receptors regulation: an in vitro study. Life Sci 2004, 75(14):1761-1773.
40. Zhao M.G., Toyoda H., Ko S.W., Ding H.K., Wu L.J., Zhuo M. Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome. J Neurosci 2005, 25:7385-7392.
41. Symons F.J., Clark R.D., Hatton D.D., Skinner M., Bailey D.B Self-injurious behavior in young boys with fragile X syndrome. Am J Med Genet A 2003, 118A:115-121.
42. Symons F.J., Danov S.E. A prospective clinical analysis of pain behavior and self-injurious behavior. Pain 2005, 117(3):473-477.
43. Symons F.J., Byiers B.J., Raspa M., Bishop E., Bailey D.B. Self-injurious behavior and fragile X syndrome: findings from the national fragile X survey. Am J Intellect Dev Disabil 2011, 115(6):473-481.
44. Bernardini N., Levey A.I., Augusti-Tocco G. Rat dorsal root ganglia express m1-m4 muscarinic receptor proteins. J Peripher Nerv Syst 1999, 4(3-4):222-232.
45. Xiong Y., Zhao X., Sun Q., Li R., Li C., Ye J. Antinociceptive mechanism of the spirocyclopiperazinium compound LXM-10 in mice and rats. Pharmacol Biochem Behav 2010, 95(2):192-197.
46. Swerdlow N.R., Geyer M.A. Prepulse inhibition of acoustic startle in rats after lesions of the pedunculopontine tegmental nucleus. Behav Neurosci 1993, 107(1):104-117.
47. Jones C.K., Shannon H.E. Bilateral lesions of the laterodorsal tegmental nucleus disrupt prepulse inhibition of acoustic startle reflex in rats. Schizophr Res 1998, 29:199.
48. Ukai M., Okuda A., Mamiya T. Effects of anticholinergic drugs selective for muscarinic receptor subtypes on prepulse inhibition in mice. Eur J Pharmacol 2004, 492(2-3):183-187.
49. Levey A.I. Muscarinic acetylcholine receptor expression in memory circuits: implications for treatment of Alzheimer disease. Proc Natl Acad Sci USA 1996, 93(24):13541-13546.
50. Power A.E., Vazdarjanova A., McGaugh J.L. Muscarinic cholinergic influences in memory consolidation. Neurobiol Learn Mem 2003, 80(3):178-193.
51. Hasselmo M.E. The role of acetylcholine in learning and memory. Curr Opin Neurobiol 2006, 16(6):710-715.
52. Hasselmo M.E., Sarter M. Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 2011, 36:52-73.
53. Di Chiara G., Morelli M., Consolo S. Modulatory functions of neurotransmitters in the striatum: ACh/dopamine/NMDA interactions. Trends Neurosci 1994, 17(6):228-233.
54. Wang H., Wu L.J., Kim S.S., Lee F.J., Gong B., Toyoda H., et al. FMRP acts as a key messenger for dopamine modulation in the forebrain. Neuron 2008, 59(4):634-647.
55. Betz A.J., McLaughlin P.J., Burgos M., Weber S.M., Salamone J.D. The muscarinic receptor antagonist tropicamide suppresses tremulous jaw movements in a rodent model of parkinsonian tremor: possible role of M4 receptors. Psychopharmacology (Berl) 2007, 194(3):347-359.
56. Davenport C.W., Heindel J.J. Cholinergic inhibition of cAMP accumulation in Sertoli cells cultured from immature hamsters. J Androl 1987, 8(5):307-313.
57. Palmero S., Bardi G., Coniglio L., Falugi C. Presence and localization of molecules related to the cholinergic system in developing rat testis. Eur J Histochem 1999, 43(4):277-283.
58. Borges M.O., Abreu M.L., Porto C.S., Avellar M.C. Characterization of muscarinic acetylcholine receptor in rat Sertoli cells. Endocrinology 2001, 142(11):4701-4710.
59. 4 binding sites in rabbit lung, chicken heart and NG108-15 cells. Mol Pharmacol 1990, 38:805-815.