Cognitive dysfunction in Duchenne muscular dystrophy: A possible role for neuromodulatory immune molecules

Journal of Neurophysiology

Volumn 116, Issue 3, 2016, Pages 1304-1315

  Rae, Mark G ^a   O’Malley, Dervla ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Duchenne muscular dystrophy; Dystrophin; Hippocampus; Learning; Memory

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; AMPA RECEPTOR; DYSTROPHIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; KAINIC ACID RECEPTOR; MATRIX METALLOPROTEINASE; NICOTINIC RECEPTOR; NITRIC OXIDE; TUMOR NECROSIS FACTOR;

BRAIN DYSFUNCTION; BRAIN FUNCTION; CENTRAL NERVOUS SYSTEM; COGNITIVE DEFECT; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DUCHENNE MUSCULAR DYSTROPHY; HIPPOCAMPUS; HUMAN; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; STRESS; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; COGNITIVE DYSFUNCTION; COMPLICATION; IMMUNOLOGY; MALE; PSYCHOLOGY;

ANIMALS; COGNITIVE DYSFUNCTION; HIPPOCAMPUS; HUMANS; MALE; MUSCULAR DYSTROPHY, DUCHENNE;

EID: 84987770990     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00248.2016     Document Type: Review

References (199)

1. Allan SM, Rothwell NJ. Cytokines and acute neurodegeneration. Nat Rev Neurosci 2: 734–744, 2001.
2. Allan SM, Tyrrell PJ, Rothwell NJ. Interleukin-1 and neuronal injury. Nat Rev Immunol 5: 629–640, 2005.
3. al-Qudah AA, Kobayashi J, Chuang S, Dennis M, Ray P. Etiology of intellectual impairment in Duchenne muscular dystrophy. Pediatr Neurol 6: 57–59, 1990.
4. Amiry-Moghaddam M, Frydenlund DS, Ottersen OP. Anchoring of aqua-porin-4 in brain: molecular mechanisms and implications for the physiology and pathophysiology of water transport. Neuroscience 129: 999–1010, 2004.
5. Anderson JE, Ovalle WK, Bressler BH. Electron microscopic and autora-diographic characterization of hindlimb muscle regeneration in the mdx mouse. Anat Rec 219: 243–257, 1987.
6. Anderson JL, Head SI, Rae C, Morley JW. Brain function in Duchenne muscular dystrophy. Brain 125: 4–13, 2002.
7. Arechavala-Gomeza V, Kinali M, Feng L, Guglieri M, Edge G, Main M, Hunt D, Lehovsky J, Straub V, Bushby K, Sewry CA, Morgan JE, Muntoni F. Revertant fibres and dystrophin traces in Duchenne muscular dystrophy: implication for clinical trials. Neuromuscul Disord 20: 295–301, 2010.
8. Baier PC, May U, Scheller J, Rose-John S, Schiffelholz T. Impaired hippocampus-dependent and -independent learning in IL-6 deficient mice. Behav Brain Res 200: 192–196, 2009.
9. Baker KD, Edwards TM, Rickard NS. The role of intracellular calcium stores in synaptic plasticity and memory consolidation. Neurosci Biobehav Rev 37: 1211–1239, 2013.
10. Balschun D, Wetzel W, Del Rey A, Pitossi F, Schneider H, Zuschratter W, Besedovsky HO. Interleukin-6: a cytokine to forget. FASEB J 18: 1788–1790, 2004.
11. Banihani R, Smile S, Yoon G, Dupuis A, Mosleh M, Snider A, McAdam L. Cognitive and neurobehavioral profile in boys with Duchenne muscular dystrophy. J Child Neurol 30: 1472–1482, 2015.
12. Barbujani G, Russo A, Danieli GA, Spiegler AW, Borkowska J, Petruse-wicz IH. Segregation analysis of 1885 DMD families: significant departure from the expected proportion of sporadic cases. Hum Genet 84: 522–526, 1990.
13. Beattie EC, Stellwagen D, Morishita W, Bresnahan JC, Ha BK, Von Zastrow M, Beattie MS, Malenka RC. Control of synaptic strength by glial TNFα. Science 295: 2282–2285, 2002.
14. Bies RD, Phelps SF, Cortez MD, Roberts R, Caskey CT, Chamberlain JS. Human and murine dystrophin mRNA transcripts are differentially expressed during skeletal muscle, heart, and brain development. Nucleic Acids Res 20: 1725–1731, 1992.
15. Blake DJ, Kroger S. The neurobiology of Duchenne muscular dystrophy: learning lessons from muscle? Trends Neurosci 23: 92–99, 2000.
16. Blake DJ, Weir A, Newey SE, Davies KE. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82: 291–329, 2002.
17. Bogdanik L, Framery B, Frolich A, Franco B, Mornet D, Bockaert J, Sigrist SJ, Grau Y, Parmentier ML. Muscle dystroglycan organizes the postsynapse and regulates presynaptic neurotransmitter release at the Drosophila neuromuscular junction. PLoS One 3: e2084, 2008.
18. Braida D, Sacerdote P, Panerai AE, Bianchi M, Aloisi AM, Iosue S, Sala M. Cognitive function in young and adult IL (interleukin)-6 deficient mice. Behav Brain Res 153: 423–429, 2004.
19. Brenman JE, Chao DS, Xia H, Aldape K, Bredt DS. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 82: 743–752, 1995.
20. Bresolin N, Castelli E, Comi GP, Felisari G, Bardoni A, Perani D, Grassi F, Turconi A, Mazzucchelli F, Gallotti D, Moggio M, Prelle A, Ausenda C, Fazio G, Scarlato G. Cognitive impairment in Duchenne muscular dystrophy. Neuromuscul Disord 4: 359–369, 1994.
21. Brown ES, Wolfshohl J, Shad MU, Vazquez M, Osuji IJ. Attenuation of the effects of corticosteroids on declarative memory with lamotrigine. Neuro-psychopharmacology 33: 2376–2383, 2008.
22. A receptors and gephyrin. J Neurosci 22: 4805–4813, 2002.
23. Bulfield G, Siller WG, Wight PA, Moore KJ. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81: 1189–1192, 1984.
24. Calsavara AC, Soriani FM, Vieira LQ, Costa PA, Rachid MA, Teixeira AL. TNFR1 absence protects against memory deficit induced by sepsis possibly through over-expression of hippocampal BDNF. Metab Brain Dis 30: 669–678, 2015.
25. Carretta D, Santarelli M, Sbriccoli A, Pinto F, Catini C, Minciacchi D. Spatial analysis reveals alterations of parvalbumin- and calbindin-positive local circuit neurons in the cerebral cortex of mutant mdx mice. Brain Res 1016: 1–11, 2004.
26. Carretta D, Santarelli M, Vanni D, Carrai R, Sbriccoli A, Pinto F, Minciacchi D. The organisation of spinal projecting brainstem neurons in an animal model of muscular dystrophy. A retrograde tracing study on mdx mutant mice. Brain Res 895: 213–222, 2001.
27. Carretta D, Santarelli M, Vanni D, Ciabatti S, Sbriccoli A, Pinto F, Minciacchi D. Cortical and brainstem neurons containing calcium-binding proteins in a murine model of Duchenne’s muscular dystrophy: selective changes in the sensorimotor cortex. J Comp Neurol 456: 48–59, 2003.
28. Chahbouni M, Escames G, Venegas C, Sevilla B, Garcia JA, Lopez LC, Munoz-Hoyos A, Molina-Carballo A, Acuna-Castroviejo D. Melatonin treatment normalizes plasma pro-inflammatory cytokines and nitrosative/ oxidative stress in patients suffering from Duchenne muscular dystrophy. J Pineal Res 48: 282–289, 2010.
29. Chamberlain JS, Pearlman JA, Muzny DM, Gibbs RA, Ranier JE, Caskey CT, Reeves AA. Expression of the murine Duchenne muscular dystrophy gene in muscle and brain. Science 239: 1416–1418, 1988.
30. Chang WJ, Iannaccone ST, Lau KS, Masters BS, McCabe TJ, McMillan K, Padre RC, Spencer MJ, Tidball JG, Stull JT. Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc Natl Acad Sci USA 93: 9142–9147, 1996.
31. Chaussenot R, Edeline JM, Le Bec B, El Massioui N, Laroche S, Vaillend C. Cognitive dysfunction in the dystrophin-deficient mouse model of Duchenne muscular dystrophy: a reappraisal from sensory to executive processes. Neurobiol Learn Mem 124: 111–122, 2015.
32. Chelly J, Hamard G, Koulakoff A, Kaplan JC, Kahn A, Berwald-Netter Y. Dystrophin gene transcribed from different promoters in neuronal and glial cells. Nature 344: 64–65, 1990.
33. Coccurello R, Castellano C, Paggi P, Mele A, Oliverio A. Genetically dystrophic mdx/mdx mice exhibit decreased response to nicotine in passive avoidance. Neuroreport 13: 1219–1222, 2002.
34. Cohen EJ, Quarta E, Fulgenzi G, Minciacchi D. Acetylcholine, GABA and neuronal networks: a working hypothesis for compensations in the dystrophic brain. Brain Res Bull 110: 1–13, 2015.
35. Comim CM, Moraz T, Abreu I, Fraga DB, Ghedim FV, Mildner N, Tuon L, Vainzof M, Zugno AI, Quevedo J. Reduction of acethylcolinesterase activity in the brain of mdx mice. Neuromuscul Disord 21: 359–362, 2011.
36. Compton AG, Cooper ST, Hill PM, Yang N, Froehner SC, North KN. The syntrophin-dystrobrevin subcomplex in human neuromuscular disorders. J Neuropathol Exp Neurol 64: 350–361, 2005.
37. Corriveau RA, Huh GS, Shatz CJ. Regulation of class I MHC gene expression in the developing and mature CNS by neural activity. Neuron 21: 505–520, 1998.
38. Coulton GR, Morgan JE, Partridge TA, Sloper JC. The mdx mouse skeletal muscle myopathy: I. A histological, morphometric and biochemical investigation. Neuropathol Appl Neurobiol 14: 53–70, 1988.
39. Craig AM, Kang Y. Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 17: 43–52, 2007.
40. Cyrulnik SE, Hinton VJ. Duchenne muscular dystrophy: a cerebellar disorder? Neurosci Biobehav Rev 32: 486–496, 2008.
41. Dallerac G, Perronnet C, Chagneau C, Leblanc-Veyrac P, Samson-Desvignes N, Peltekian E, Danos O, Garcia L, Laroche S, Billard JM, Vaillend C. Rescue of a dystrophin-like protein by exon skipping normalizes synaptic plasticity in the hippocampus of the mdx mouse. Neurobiol Dis 43: 635–641, 2011.
42. Dangain J, Vrbova G. Muscle development in mdx mutant mice. Muscle Nerve 7: 700–704, 1984.
43. de Brouwer AP, Nabuurs SB, Verhaart IE, Oudakker AR, Hordijk R, Yntema HG, Hordijk-Hos JM, Voesenek K, de Vries BB, van Essen T, Chen W, Hu H, Chelly J, den Dunnen JT, Kalscheuer VM, Aartsma-Rus AM, Hamel BC, van Bokhoven H, Kleefstra T. A 3-base pair deletion, c.9711_9713del, in DMD results in intellectual disability without muscular dystrophy. Eur J Hum Genet 22: 480–485, 2014.
44. De Paepe B, De Bleecker JL. Cytokines and chemokines as regulators of skeletal muscle inflammation: presenting the case of Duchenne muscular dystrophy. Mediators Inflamm 2013: 540370, 2013.
45. De Pasquale L, D’Amico A, Verardo M, Petrini S, Bertini E, De Benedetti F. Increased muscle expression of interleukin-17 in Duchenne muscular dystrophy. Neurology 78: 1309–1314, 2012.
46. Del Tongo C, Carretta D, Fulgenzi G, Catini C, Minciacchi D. Parvalbu-min-positive GABAergic interneurons are increased in the dorsal hippocampus of the dystrophic mdx mouse. Acta Neuropathol (Berl) 118: 803–812, 2009.
47. Deng B, Glanzman D, Tidball JG. Nitric oxide generated by muscle corrects defects in hippocampal neurogenesis and neural differentiation caused by muscular dystrophy. J Physiol 587: 1769–1778, 2009.
48. Dubowitz V, Crome L. The central nervous system in Duchenne muscular dystrophy. Brain 92: 805–808, 1969.
49. Dummer W, Niethammer AG, Baccala R, Lawson BR, Wagner N, Reis-feld RA, Theofilopoulos AN. T cell homeostatic proliferation elicits effective antitumor autoimmunity. J Clin Invest 110: 185–192, 2002.
50. Evans NP, Misyak SA, Robertson JL, Bassaganya-Riera J, Grange RW. Immune-mediated mechanisms potentially regulate the disease time-course of Duchenne muscular dystrophy and provide targets for therapeutic intervention. PM R 1: 755–768, 2009.
51. Felisari G, Martinelli Boneschi F, Bardoni A, Sironi M, Comi GP, Robotti M, Turconi AC, Lai M, Corrao G, Bresolin N. Loss of Dp140 dystrophin isoform and intellectual impairment in Duchenne dystrophy. Neurology 55: 559–564, 2000.
52. Fitzpatrick C, Barry C, Garvey C. Psychiatric disorder among boys with Duchenne muscular dystrophy. Dev Med Child Neurol 28: 589–595, 1986.
53. Fradkin LG, Baines RA, van der Plas MC, Noordermeer JN. The dystrophin Dp186 isoform regulates neurotransmitter release at a central synapse in Drosophila. J Neurosci 28: 5105–5114, 2008.
54. Fritschy JM, Panzanelli P, Tyagarajan SK. Molecular and functional heterogeneity of GABAergic synapses. Cell Mol Life Sci 69: 2485–2499, 2012.
55. Fuenzalida M, Espinoza C, Perez MA, Tapia-Rojas C, Cuitino L, Brandan E, Inestrosa NC. Wnt signaling pathway improves central inhibitory synaptic transmission in a mouse model of Duchenne muscular dystrophy. Neurobiol Dis 86: 109–120, 2016.
56. Futai K, Kim MJ, Hashikawa T, Scheiffele P, Sheng M, Hayashi Y. Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin. Nat Neurosci 10: 186–195, 2007.
57. Gaffen SL. Structure and signalling in the IL-17 receptor family. Nat Rev Immunol 9: 556–567, 2009.
58. Gardoni F, Boraso M, Zianni E, Corsini E, Galli CL, Cattabeni F, Marinovich M, Di Luca M, Viviani B. Distribution of interleukin-1 receptor complex at the synaptic membrane driven by interleukin-1β and NMDA stimulation. J Neuroinflammation 8: 14, 2011.
59. Ghedini PC, Avellar MC, De Lima TC, Lima-Landman MT, Lapa AJ, Souccar C. Quantitative changes of nicotinic receptors in the hippocampus of dystrophin-deficient mice. Brain Res 1483: 96–104, 2012.
60. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH. Mechanisms underlying inflammation in neurodegeneration. Cell 140: 918–934, 2010.
61. Gloss D, Moxley RT, Ashwal S, Oskoui M. Practice guideline update summary: corticosteroid treatment of Duchenne muscular dystrophy. Report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology 86: 465–472, 2016.
62. Goddard CA, Butts DA, Shatz CJ. Regulation of CNS synapses by neuronal MHC class I. Proc Natl Acad Sci USA 104: 6828–6833, 2007.
63. 3cv). J Cereb Blood Flow Metab 20: 145–152, 2000.
64. Goodnough CL, Gao Y, Li X, Qutaish MQ, Goodnough LH, Molter J, Wilson D, Flask CA, Yu X. Lack of dystrophin results in abnormal cerebral diffusion and perfusion in vivo. Neuroimage 102: 809–816, 2014.
65. Gorecki DC, Barnard EA. Specific expression of G-dystrophin (Dp71) in the brain. Neuroreport 6: 893–896, 1995.
66. Goshen I, Kreisel T, Ounallah-Saad H, Renbaum P, Zalzstein Y, Ben-Hur T, Levy-Lahad E, Yirmiya R. A dual role for interleukin-1 in hippocam-pal-dependent memory processes. Psychoneuroendocrinology 32: 1106–1115, 2007.
67. Graciotti L, Minelli A, Minciacchi D, Procopio A, Fulgenzi G. GABAergic miniature spontaneous activity is increased in the CA1 hippocampal region of dystrophic mdx mice. Neuromuscul Disord 18: 220–226, 2008.
68. Graf ER, Zhang X, Jin SX, Linhoff MW, Craig AM. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119: 1013–1026, 2004.
69. Griffin WS. Inflammation and neurodegenerative diseases. Am J Clin Nutr 83: 470S–474S, 2006.
70. Grounds MD, Radley HG, Gebski BL, Bogoyevitch MA, Shavlakadze T. Implications of cross-talk between tumour necrosis factor and insulin-like growth factor-1 signalling in skeletal muscle. Clin Exp Pharmacol Physiol 35: 846–851, 2008.
71. Gulyas AI, Miles R, Sik A, Toth K, Tamamaki N, Freund TF. Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366: 683–687, 1993.
72. Haenggi T, Fritschy JM. Role of dystrophin and utrophin for assembly and function of the dystrophin glycoprotein complex in non-muscle tissue. Cell Mol Life Sci 63: 1614–1631, 2006.
73. Haenggi T, Soontornmalai A, Schaub MC, Fritschy JM. The role of utrophin and Dp71 for assembly of different dystrophin-associated protein complexes (DPCs) in the choroid plexus and microvasculature of the brain. Neuroscience 129: 403–413, 2004.
74. Haslett JN, Sanoudou D, Kho AT, Bennett RR, Greenberg SA, Kohane IS, Beggs AH, Kunkel LM. Gene expression comparison of biopsies from Duchenne muscular dystrophy (DMD) and normal skeletal muscle. Proc Natl Acad Sci USA 99: 15000–15005, 2002.
75. Hendriksen RG, Hoogland G, Schipper S, Hendriksen JG, Vles JS, Aalbers MW. A possible role of dystrophin in neuronal excitability: a review of the current literature. Neurosci Biobehav Rev 51: 255–262, 2015.
76. Hinton VJ, De Vivo DC, Nereo NE, Goldstein E, Stern Y. Poor verbal working memory across intellectual level in boys with Duchenne dystrophy. Neurology 54: 2127–2132, 2000.
77. Hinton VJ, De Vivo DC, Nereo NE, Goldstein E, Stern Y. Selective deficits in verbal working memory associated with a known genetic etiology: the neuropsychological profile of Duchenne muscular dystrophy. J Int Neuro-psychol Soc 7: 45–54, 2001.
78. Hinton VJ, Fee RJ, De Vivo DC, Goldstein E. Poor facial affect recognition among boys with Duchenne muscular dystrophy. J Autism Dev Disord 37: 1925–1933, 2007.
79. Hinton VJ, Nereo NE, Fee RJ, Cyrulnik SE. Social behavior problems in boys with Duchenne muscular dystrophy. J Dev Behav Pediatr 27: 470–476, 2006.
80. Hopf FW, Steinhardt RA. Regulation of intracellular free calcium in normal and dystrophic mouse cerebellar neurons. Brain Res 578: 49–54, 1992.
81. Hu J, Van den Steen PE, Sang QX, Opdenakker G. Matrix metalloproteinase inhibitors as therapy for inflammatory and vascular diseases. Nat Rev Drug Discov 6: 480–498, 2007.
82. Huang P, Zhao XS, Fields M, Ransohoff RM, Zhou L. Imatinib attenuates skeletal muscle dystrophy in mdx mice. FASEB J 23: 2539–2548, 2009.
83. Huh GS, Boulanger LM, Du H, Riquelme PA, Brotz TM, Shatz CJ. Functional requirement for class I MHC in CNS development and plasticity. Science 290: 2155–2159, 2000.
84. Huynh T, Uaesoontrachoon K, Quinn JL, Tatem KS, Heier CR, Van Der Meulen JH, Yu Q, Harris M, Nolan CJ, Haegeman G, Grounds MD, Nagaraju K. Selective modulation through the glucocorticoid receptor ameliorates muscle pathology in mdx mice. J Pathol 231: 223–235, 2013.
85. Inestrosa NC, Arenas E. Emerging roles of Wnts in the adult nervous system. Nat Rev Neurosci 11: 77–86, 2010.
86. Itoh K, Jinnai K, Tada K, Hara K, Itoh H, Takahashi K. Multifocal glial nodules in a case of Duchenne muscular dystrophy with severe mental retardation. Neuropathology 19: 322–327, 1999.
87. Jagadha V, Becker LE. Brain morphology in Duchenne muscular dystrophy: a Golgi study. Pediatr Neurol 4: 87–92, 1988.
88. Jankowsky JL, Derrick BE, Patterson PH. Cytokine responses to LTP induction in the rat hippocampus: a comparison of in vitro and in vivo techniques. Learn Mem 7: 400–412, 2000.
89. Jueptner M, Weiller C. Review: does measurement of regional cerebral blood flow reflect synaptic activity? Implications for PET and fMRI. Neuroimage 2: 148–156, 1995.
90. Kang Y, Zhang X, Dobie F, Wu H, Craig AM. Induction of GABAergic postsynaptic differentiation by alpha-neurexins. J Biol Chem 283: 2323–2334, 2008.
91. Kato T, Nishina M, Matsushita K, Hori E, Akaboshi S, Takashima S. Increased cerebral choline-compounds in Duchenne muscular dystrophy. Neuroreport 8: 1435–1437, 1997.
92. Kherif S, Lafuma C, Dehaupas M, Lachkar S, Fournier JG, Verdiere-Sahuque M, Fardeau M, Alameddine HS. Expression of matrix metallo-proteinases 2 and 9 in regenerating skeletal muscle: a study in experimentally injured and mdx muscles. Dev Biol 205: 158–170, 1999.
93. Kim TW, Wu K, Xu JL, Black IB. Detection of dystrophin in the postsynaptic density of rat brain and deficiency in a mouse model of Duchenne muscular dystrophy. Proc Natl Acad Sci USA 89: 11642–11644, 1992.
94. Knuesel I, Bornhauser BC, Zuellig RA, Heller F, Schaub MC, Fritschy JM. Differential expression of utrophin and dystrophin in CNS neurons: an in situ hybridization and immunohistochemical study. J Comp Neurol 422: 594–611, 2000.
95. A receptors in mice lacking dystrophin (mdx mice). Eur J Neurosci 11: 4457–4462, 1999.
96. Knuesel I, Zuellig RA, Schaub MC, Fritschy JM. Alterations in dystrophin and utrophin expression parallel the reorganization of GABAergic synapses in a mouse model of temporal lobe epilepsy. Eur J Neurosci 13: 1113–1124, 2001.
97. Koenig M, Hoffman EP, Bertelson CJ, Monaco AP, Feener C, Kunkel LM. Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50: 509–517, 1987.
98. Krasowska E, Zablocki K, Gorecki DC, Swinny JD. Aberrant location of inhibitory synaptic marker proteins in the hippocampus of dystrophin- deficient mice: implications for cognitive impairment in Duchenne muscular dystrophy. PLoS One 9: e108364, 2014.
99. Kreis R, Wingeier K, Vermathen P, Giger E, Joncourt F, Zwygart K, Kaufmann F, Boesch C, Steinlin M. Brain metabolite composition in relation to cognitive function and dystrophin mutations in boys with Duchenne muscular dystrophy. NMR Biomed 24: 253–262, 2011.
100. A receptor number and enhanced gaboxadol induced change in holding currents in Purkinje cells of the dystrophin-deficient mdx mouse. Neurobiol Dis 43: 558–564, 2011.
101. A receptor expression and inhibitory post-synaptic currents in cerebellar Purkinje cells in dystrophin-deficient mdx mice. Clin Exp Pharmacol Physiol 35: 207–210, 2008.
102. Kurek J, Bower J, Romanella M, Austin L. Leukaemia inhibitory factor treatment stimulates muscle regeneration in the mdx mouse. Neurosci Lett 212: 167–170, 1996.
103. Kuru S, Inukai A, Kato T, Liang Y, Kimura S, Sobue G. Expression of tumor necrosis factor-alpha in regenerating muscle fibers in inflammatory and non-inflammatory myopathies. Acta Neuropathol (Berl) 105: 217–224, 2003.
104. Lee JS, Pfund Z, Juhasz C, Behen ME, Muzik O, Chugani DC, Nigro MA, Chugani HT. Altered regional brain glucose metabolism in Duchenne muscular dystrophy: a pet study. Muscle Nerve 26: 506–512, 2002.
105. Levi S, Grady RM, Henry MD, Campbell KP, Sanes JR, Craig AM. Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation. J Neurosci 22: 4274–4285, 2002.
106. Li AJ, Katafuchi T, Oda S, Hori T, Oomura Y. Interleukin-6 inhibits long-term potentiation in rat hippocampal slices. Brain Res 748: 30–38, 1997.
107. Li H, Mittal A, Makonchuk DY, Bhatnagar S, Kumar A. Matrix metalloproteinase-9 inhibition ameliorates pathogenesis and improves skeletal muscle regeneration in muscular dystrophy. Hum Mol Genet 18: 2584–2598, 2009.
108. Lidov HG. Dystrophin in the nervous system. Brain Pathol 6: 63–77, 1996.
109. Lidov HG, Byers TJ, Kunkel LM. The distribution of dystrophin in the murine central nervous system: an immunocytochemical study. Neuroscience 54: 167–187, 1993.
110. Lidov HG, Byers TJ, Watkins SC, Kunkel LM. Localization of dystrophin to postsynaptic regions of central nervous system cortical neurons. Nature 348: 725–728, 1990.
111. Lv SY, Zou QH, Cui JL, Zhao N, Hu J, Long XY, Sun YC, He J, Zhu CZ, He Y, Zang YF. Decreased gray matter concentration and local synchronization of spontaneous activity in the motor cortex in Duchenne muscular dystrophy. AJNR Am J Neuroradiol 32: 2196–2200, 2011.
112. Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron 44: 5–21, 2004.
113. Manning J, Kulbida R, Rai P, Jensen L, Bouma J, Singh SP, O’Malley D, Yilmazer-Hanke D. Amitriptyline is efficacious in ameliorating muscle inflammation and depressive symptoms in the mdx mouse model of Duchenne muscular dystrophy. Exp Physiol 99: 1370–1386, 2014.
114. Manning J, O’Malley D. What has the mdx mouse model of Duchenne muscular dystrophy contributed to our understanding of this disease? J Muscle Res Cell Motil 36: 155–167, 2015.
115. Marin I, Kipnis J. Learning and memory … and the immune system. Learn Mem 20: 601–606, 2013.
116. Matsumura K, Ervasti JM, Ohlendieck K, Kahl SD, Campbell KP. Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature 360: 588–591, 1992.
117. McBain CJ, Dingledine R. Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J Physiol 462: 373–392, 1993.
118. Mehler MF, Haas KZ, Kessler JA, Stanton PK. Enhanced sensitivity of hippocampal pyramidal neurons from mdx mice to hypoxia-induced loss of synaptic transmission. Proc Natl Acad Sci USA 89: 2461–2465, 1992.
119. Messina S, Vita GL, Aguennouz M, Sframeli M, Romeo S, Rodolico C, Vita G. Activation of NF-κB pathway in Duchenne muscular dystrophy: relation to age. Acta Myol 30: 16–23, 2011.
120. Minciacchi D, Del Tongo C, Carretta D, Nosi D, Granato A. Alterations of the cortico-cortical network in sensori-motor areas of dystrophin deficient mice. Neuroscience 166: 1129–1139, 2010.
121. Miranda R, Nudel U, Laroche S, Vaillend C. Altered presynaptic ultrastruc-ture in excitatory hippocampal synapses of mice lacking dystrophins Dp427 or Dp71. Neurobiol Dis 43: 134–141, 2011.
122. Miranda R, Sebrie C, Degrouard J, Gillet B, Jaillard D, Laroche S, Vaillend C. Reorganization of inhibitory synapses and increased PSD length of perforated excitatory synapses in hippocampal area CA1 of dystrophin-deficient mdx mice. Cereb Cortex 19: 876–888, 2009.
123. Montgomery SL, Bowers WJ. Tumor necrosis factor-alpha and the roles it plays in homeostatic and degenerative processes within the central nervous system. J Neuroimmune Pharmacol 7: 42–59, 2012.
124. Moore AH, Wu M, Shaftel SS, Graham KA, O’Banion MK. Sustained expression of interleukin-1β in mouse hippocampus impairs spatial memory. Neuroscience 164: 1484–1495, 2009.
125. A receptor activation attenuates excitotoxicity but exacerbates oxygen-glucose deprivation-in-duced neuronal injury in vitro. J Cereb Blood Flow Metab 16: 1211–1218, 1996.
126. Muntoni F, Mateddu A, Serra G. Passive avoidance behaviour deficit in the mdx mouse. Neuromuscul Disord 1: 121–123, 1991.
127. Nagappa M, Nalini A, Narayanappa G. Major histocompatibility complex and inflammatory cell subtype expression in inflammatory myopathies and muscular dystrophies. Neurol India 61: 614–621, 2013.
128. Nagy V, Bozdagi O, Matynia A, Balcerzyk M, Okulski P, Dzwonek J, Costa RM, Silva AJ, Kaczmarek L, Huntley GW. Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J Neurosci 26: 1923–1934, 2006.
129. Nardes F, Araujo AP, Ribeiro MG. Mental retardation in Duchenne muscular dystrophy. J Pediatr (Rio J) 88: 6–16, 2012.
130. Nguyen KT, Deak T, Owens SM, Kohno T, Fleshner M, Watkins LR, Maier SF. Exposure to acute stress induces brain interleukin-1β protein in the rat. J Neurosci 18: 2239–2246, 1998.
131. Nico B, Paola Nicchia G, Frigeri A, Corsi P, Mangieri D, Ribatti D, Svelto M, Roncali L. Altered blood-brain barrier development in dystrophic MDX mice. Neuroscience 125: 921–935, 2004.
132. Oliva CA, Vargas JY, Inestrosa NC. Wnts in adult brain: from synaptic plasticity to cognitive deficiencies. Front Cell Neurosci 7: 224, 2013.
133. Olsen O, Moore KA, Nicoll RA, Bredt DS. Synaptic transmission regulated by a presynaptic MALS/liprin-α protein complex. Curr Opin Cell Biol 18: 223–227, 2006.
134. Pangalila RF, van den Bos GA, Bartels B, Bergen M, Stam HJ, Roebroeck ME. Prevalence of fatigue, pain, and affective disorders in adults with Duchenne muscular dystrophy and their associations with quality of life. Arch Phys Med Rehabil 96: 1242–1247, 2015.
135. Parames SF, Coletta-Yudice ED, Nogueira FM, Nering de Sousa MB, Hayashi MA, Lima-Landman MT, Lapa AJ, Souccar C. Altered acetylcholine release in the hippocampus of dystrophin-deficient mice. Neuroscience 269: 173–183, 2014.
136. Pelosi L, Berardinelli MG, Forcina L, Spelta E, Rizzuto E, Nicoletti C, Camilli C, Testa E, Catizone A, De Benedetti F, Musaro A. Increased levels of interleukin-6 exacerbate the dystrophic phenotype in mdx mice. Hum Mol Genet 24: 6041–6053, 2015.
137. Perronnet C, Chagneau C, Le Blanc P, Samson-Desvignes N, Mornet D, Laroche S, De La Porte S, Vaillend C. Upregulation of brain utrophin does not rescue behavioral alterations in dystrophin-deficient mice. Hum Mol Genet 21: 2263–2276, 2012.
138. Perronnet C, Vaillend C. Dystrophins, utrophins, and associated scaffolding complexes: role in mammalian brain and implications for therapeutic strategies. J Biomed Biotechnol 2010: 849426, 2010.
139. Pilgram GS, Potikanond S, Baines RA, Fradkin LG, Noordermeer JN. The roles of the dystrophin-associated glycoprotein complex at the synapse. Mol Neurobiol 41: 1–21, 2010.
140. Porreca E, Guglielmi MD, Uncini A, Di Gregorio P, Angelini A, Di Febbo C, Pierdomenico SD, Baccante G, Cuccurullo F. Haemostatic abnormalities, cardiac involvement and serum tumor necrosis factor levels in X-linked dystrophic patients. Thromb Haemost 81: 543–546, 1999.
141. Porter JD, Khanna S, Kaminski HJ, Rao JS, Merriam AP, Richmonds CR, Leahy P, Li J, Guo W, Andrade FH. A chronic inflammatory response dominates the skeletal muscle molecular signature in dystrophin-deficient mdx mice. Hum Mol Genet 11: 263–272, 2002.
142. A receptors. J Neurosci 33: 15879–15893, 2013.
143. Rada P, Mark GP, Vitek MP, Mangano RM, Blume AJ, Beer B, Hoebel BG. Interleukin-1 beta decreases acetylcholine measured by microdialysis in the hippocampus of freely moving rats. Brain Res 550: 287–290, 1991.
144. Rae C, Griffin JL, Blair DH, Bothwell JH, Bubb WA, Maitland A, Head S. Abnormalities in brain biochemistry associated with lack of dystrophin: studies of the mdx mouse. Neuromuscul Disord 12: 121–129, 2002.
145. 1H magnetic resonance and neuropsychological study. J Neurol Sci 160: 148–157, 1998.
146. Rodius F, Claudepierre T, Rosas-Vargas H, Cisneros B, Montanez C, Dreyfus H, Mornet D, Rendon A. Dystrophins in developing retina: Dp260 expression correlates with synaptic maturation. Neuroreport 8: 2383–2387, 1997.
147. Rosman NP. The cerebral defect and myopathy in Duchenne muscular dystrophy. A comparative clinicopathological study. Neurology 20: 329–335, 1970.
148. Rosman NP, Kakulas BA. Mental deficiency associated with muscular dystrophy. A neuropathological study. Brain 89: 769–788, 1966.
149. Ross FM, Allan SM, Rothwell NJ, Verkhratsky A. A dual role for interleukin-1 in LTP in mouse hippocampal slices. J Neuroimmunol 144: 61–67, 2003.
150. Rufo A, Del Fattore A, Capulli M, Carvello F, De Pasquale L, Ferrari S, Pierroz D, Morandi L, De Simone M, Rucci N, Bertini E, Bianchi ML, De Benedetti F, Teti A. Mechanisms inducing low bone density in Duchenne muscular dystrophy in mice and humans. J Bone Miner Res 26: 1891–1903, 2011.
151. Sairanen TR, Lindsberg PJ, Brenner M, Carpen O, Siren A. Differential cellular expression of tumor necrosis factor-α and type I tumor necrosis factor receptor after transient global forebrain ischemia. J Neurol Sci 186: 87–99, 2001.
152. Sakamoto T, Arima T, Ishizaki M, Kawano R, Koide T, Uchida Y, Yamashita S, Kimura E, Hirano T, Maeda Y, Uchino M. Regions downstream from the WW domain of dystrophin are important for binding to postsynaptic densities in the brain. Neuromuscul Disord 18: 382–388, 2008.
153. A dysregulation and impaired spatial learning. Am J Physiol Regul Integr Comp Physiol 290: R1345–R1356, 2006.
154. Sapolsky RM. Stress, glucocorticoids, and damage to the nervous system: the current state of confusion. Stress 1: 1–19, 1996.
155. Sbriccoli A, Santarelli M, Carretta D, Pinto F, Granato A, Minciacchi D. Architectural changes of the cortico-spinal system in the dystrophin defective mdx mouse. Neurosci Lett 200: 53–56, 1995.
156. Schneider H, Pitossi F, Balschun D, Wagner A, del Rey A, Besedovsky HO. A neuromodulatory role of interleukin-1beta in the hippocampus. Proc Natl Acad Sci USA 95: 7778–7783, 1998.
157. Schobitz B, de Kloet ER, Sutanto W, Holsboer F. Cellular localization of interleukin 6 mRNA and interleukin 6 receptor mRNA in rat brain. Eur J Neurosci 5: 1426–1435, 1993.
158. Sekiguchi M, Zushida K, Yoshida M, Maekawa M, Kamichi S, Yoshida M, Sahara Y, Yuasa S, Takeda S, Wada K. A deficit of brain dystrophin impairs specific amygdala GABAergic transmission and enhances defensive behaviour in mice. Brain 132: 124–135, 2009.
159. Septien L, Gras P, Borsotti JP, Giroud M, Nivelon JL, Dumas R. [Mental development in Duchenne muscular dystrophy. Correlation of data of the brain scanner]. Pediatrie 46: 817–819, 1991.
160. Sesay AK, Errington ML, Levita L, Bliss TV. Spatial learning and hippocampal long-term potentiation are not impaired in mdx mice. Neurosci Lett 211: 207–210, 1996.
161. Snow WM, Anderson JE, Jakobson LS. Neuropsychological and neurobehavioral functioning in Duchenne muscular dystrophy: a review. Neurosci Biobehav Rev 37: 743–752, 2013.
162. Sparkman NL, Buchanan JB, Heyen JR, Chen J, Beverly JL, Johnson RW. Interleukin-6 facilitates lipopolysaccharide-induced disruption in working memory and expression of other proinflammatory cytokines in hippocampal neuronal cell layers. J Neurosci 26: 10709–10716, 2006.
163. Stawarski M, Stefaniuk M, Wlodarczyk J. Matrix metalloproteinase-9 involvement in the structural plasticity of dendritic spines. Front Neuroanat 8: 68, 2014.
164. Stellwagen D, Malenka RC. Synaptic scaling mediated by glial TNF-α. Nature 440: 1054–1059, 2006.
165. Sudhof TC. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455: 903–911, 2008.
166. Sugita S, Saito F, Tang J, Satz J, Campbell K, Sudhof TC. A stoichiometric complex of neurexins and dystroglycan in brain. J Cell Biol 154: 435–445, 2001.
167. Sun J, Zhang S, Zhang X, Zhang X, Dong H, Qian Y. IL-17A is implicated in lipopolysaccharide-induced neuroinflammation and cognitive impairment in aged rats via microglial activation. J Neuroinflammation 12: 165, 2015.
168. Tadayoni R, Rendon A, Soria-Jasso LE, Cisneros B. Dystrophin Dp71: the smallest but multifunctional product of the Duchenne muscular dystrophy gene. Mol Neurobiol 45: 43–60, 2012.
169. Taepavarapruk P, Song C. Reductions of acetylcholine release and nerve growth factor expression are correlated with memory impairment induced by interleukin-1beta administrations: effects of omega-3 fatty acid EPA treatment. J Neurochem 112: 1054–1064, 2010.
170. Tanaka H, Shan W, Phillips GR, Arndt K, Bozdagi O, Shapiro L, Huntley GW, Benson DL, Colman DR. Molecular modification of N-cadherin in response to synaptic activity. Neuron 25: 93–107, 2000.
171. Terrando N, Rei Fidalgo A, Vizcaychipi M, Cibelli M, Ma D, Monaco C, Feldmann M, Maze M. The impact of IL-1 modulation on the development of lipopolysaccharide-induced cognitive dysfunction. Crit Care 14: R88, 2010.
172. Timpani CA, Hayes A, Rybalka E. Revisiting the dystrophin-ATP connection: how half a century of research still implicates mitochondrial dysfunction in Duchenne muscular Dystrophy aetiology. Med Hypotheses 85: 1021–1033, 2015.
173. Torres LF, Duchen LW. The mutant mdx: inherited myopathy in the mouse. Morphological studies of nerves, muscles and end-plates. Brain 110: 269–299, 1987.
174. Tracey I, Dunn JF, Radda GK. Brain metabolism is abnormal in the mdx model of Duchenne muscular dystrophy. Brain 119: 1039–1044, 1996.
175. Tracey I, Scott RB, Thompson CH, Dunn JF, Barnes PR, Styles P, Kemp GJ, Rae CD, Pike M, Radda GK. Brain abnormalities in Duchenne muscular dystrophy: phosphorus-31 magnetic resonance spectroscopy and neuropsychological study. Lancet 345: 1260–1264, 1995.
176. Tuckett E, Gosetti T, Hayes A, Rybalka E, Verghese E. Increased calcium in neurons in the cerebral cortex and cerebellum is not associated with cell loss in the mdx mouse model of Duchenne muscular dystrophy. Neuroreport 26: 785–790, 2015.
177. A receptors? Hippocampus 12: 713–717, 2002.
178. 3cv mice lacking dystrophin gene products. Neuroscience 86: 53–66, 1998.
179. mdx mouse. Neurobiol Dis 17: 10–20, 2004.
180. A-receptor clustering in the hippocampus of the mdx mouse. Mol Ther 18: 1683–1688, 2010.
181. Vaillend C, Rendon A, Misslin R, Ungerer A. Influence of dystrophin-gene mutation on mdx mouse behavior. I. Retention deficits at long delays in spontaneous alternation and bar-pressing tasks. Behav Genet 25: 569–579, 1995.
182. Vaillend C, Ungerer A. Behavioral characterization of mdx3cv mice deficient in C-terminal dystrophins. Neuromuscul Disord 9: 296–304, 1999.
183. Vaillend C, Ungerer A, Billard JM. Facilitated NMDA receptor-mediated synaptic plasticity in the hippocampal CA1 area of dystrophin-deficient mice. Synapse 33: 59–70, 1999.
184. van der Plas MC, Pilgram GS, Plomp JJ, de Jong A, Fradkin LG, Noordermeer JN. Dystrophin is required for appropriate retrograde control of neurotransmitter release at the Drosophila neuromuscular junction. J Neurosci 26: 333–344, 2006.
185. Vezzani A, Maroso M, Balosso S, Sanchez MA, Bartfai T. IL-1 receptor/ Toll-like receptor signaling in infection, inflammation, stress and neurodegeneration couples hyperexcitability and seizures. Brain Behav Immun 25: 1281–1289, 2011.
186. Vezzani A, Viviani B. Neuromodulatory properties of inflammatory cytokines and their impact on neuronal excitability. Neuropharmacology 96: 70–82, 2015.
187. Wairkar YP, Fradkin LG, Noordermeer JN, DiAntonio A. Synaptic defects in a Drosophila model of congenital muscular dystrophy. J Neurosci 28: 3781–3789, 2008.
188. Waite A, Brown SC, Blake DJ. The dystrophin-glycoprotein complex in brain development and disease. Trends Neurosci 35: 487–496, 2012.
189. Waite A, Tinsley CL, Locke M, Blake DJ. The neurobiology of the dystrophin-associated glycoprotein complex. Ann Med 41: 344–359, 2009.
190. Wallis T, Bubb WA, McQuillan JA, Balcar VJ, Rae C. For want of a nail. Ramifications of a single gene deletion, dystrophin, in the brain of the mouse. Front Biosci 9: 74–84, 2004.
191. A receptors. Cell Rep 2: 488–496, 2012.
192. Wei H, Chadman KK, McCloskey DP, Sheikh AM, Malik M, Brown WT, Li X. Brain IL-6 elevation causes neuronal circuitry imbalances and mediates autism-like behaviors. Biochim Biophys Acta 1822: 831–842, 2012.
193. Wojtowicz T, Mozrzymas JW. Late phase of long-term potentiation in the mossy fiber-CA3 hippocampal pathway is critically dependent on metallo-proteinases activity. Hippocampus 20: 917–921, 2010.
194. 1H MRS. Neuromuscul Disord 25: 764–772, 2015.
195. Yamamoto K, Yamada D, Kabuta T, Takahashi A, Wada K, Sekiguchi M. Reduction of abnormal behavioral response to brief restraint by information from other mice in dystrophin-deficient mdx mice. Neuromuscul Disord 20: 505–511, 2010.
196. Yiu EM, Kornberg AJ. Duchenne muscular dystrophy. Neurol India 56: 236–247, 2008.
197. Yoshihara Y, Onodera H, Iinuma K, itoyama Y. Abnormal kainic acid receptor density and reduced seizure susceptibility in dystrophin-deficient mdx mice. Neuroscience 117: 391–395, 2003.
198. Yoshioka M, Okuno T, Honda Y, Nakano Y. Central nervous system involvement in progressive muscular dystrophy. Arch Dis Child 55: 589–594, 1980.
199. A receptors. Neuron 66: 403–416, 2010.