Parvalbumin-positive GABAergic interneurons are increased in the dorsal hippocampus of the dystrophic mdx mouse

Acta Neuropathologica

Volumn 118, Issue 6, 2009, Pages 803-812

  Del Tongo, Claudia ^a   Carretta, Donatella ^a   Fulgenzi, Gianluca ^b,c   Catini, Claudio ^a   Minciacchi, Diego ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Dentate gyrus; Duchenne muscular dystrophy; Dystrophin; Immunohistochemistry; Mutant mouse strain

Indexed keywords

PARVALBUMIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL STRUCTURE; CELLULAR DISTRIBUTION; DENTATE GYRUS; DUCHENNE MUSCULAR DYSTROPHY; GABAERGIC SYSTEM; HIPPOCAMPUS; INTERNEURON; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CELL COUNT; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; MICE; MICE, INBRED MDX; PARVALBUMINS;

EID: 71449105214     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-009-0567-3     Document Type: Article

References (65)

1. JL Anderson SI Head C Rae JW Morley 2002 Brain function in Duchenne muscular dystrophy Brain 125 4 13 10.1093/brain/awf012 1:STN:280: DC%2BD387gsFOhtg%3D%3D 11834588
2. KG Baimbridge MR Celio JH Rogers 1992 Calcium-binding proteins in the nervous system Trends Neurosci 15 303 308 10.1016/0166-2236(92)90081-I 1:CAS:528:DyaK38XlvVyksrY%3D 1384200
3. M Bartos I Vida M Frotscher A Meyer H Monyer JR Geiger P Jonas 2002 Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks Proc Natl Acad Sci USA 99 13222 13227 10.1073/pnas. 192233099 1:CAS:528:DC%2BD38XnvFGgsro%3D 12235359
4. A receptor alpha1 subunit, somatostatin and Connexin36 distinguishes axoaxonic, basket, and bistratified interneurons of the rat hippocampus Cereb Cortex 17 2094 2107 10.1093/cercor/bhl117 17122364 (Pubitemid 47283681)
5. E Braak B Strotkamp H Braak 1991 Parvalbumin-immunoreactive structures in the hippocampus of the human adult Cell Tissue Res 264 33 48 10.1007/BF00305720 1:STN:280:DyaK3M3nsFWrug%3D%3D 2054844
6. O Caillard H Moreno B Schwaller I Llano MR Celio A Marty 2000 Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity Proc Natl Acad Sci USA 97 13372 13377 10.1073/pnas.230362997 1:CAS:528: DC%2BD3cXosVOjs7k%3D 11069288
7. D Carretta M Santarelli D Vanni R Carrai A Sbriccoli F Pinto D Minciacchi 2001 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 10.1016/S0006-8993(01)02108-4 1:CAS:528:DC%2BD3MXitVOnsL4%3D 11259780 (Pubitemid 32231158)
8. D Carretta M Santarelli D Vanni S Ciabatti A Sbriccoli F Pinto D Minciacchi 2003 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 10.1002/cne.10506 1:CAS:528:DC%2BD3sXpsVKhtg%3D%3D 12508313 (Pubitemid 36043642)
9. D Carretta M Santarelli A Sbriccoli F Pinto C Catini D Minciacchi 2004 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 10.1016/j.brainres.2004.04.021 1:CAS:528:DC%2BD2cXltl2hsbo%3D 15234246 (Pubitemid 38834268)
10. MR Celio 1986 Parvalbumin in most g-aminobutyric acid-containing neurons of the rat cerebral cortex Science 231 995 997 10.1126/science.3945815 1:CAS:528:DyaL28XhsVGqtLg%3D 3945815
11. MR Celio 1990 Calbindin D-28K and parvalbumin in rat nervous system Neuroscience 35 375 475 10.1016/0306-4522(90)90091-H 1:CAS:528: DyaK3cXkt1Whtrw%3D 2199841 (Pubitemid 20176750)
12. J Chelly JC Kaplan P Maire S Gautron J Kahn 1988 Transcription of dystrophin gene in human muscle and non-muscle tissues Nature 333 858 860 10.1038/333858a0 1:CAS:528:DyaL1cXks1yjurY%3D 3290682 (Pubitemid 18163324)
13. S Cotton NJ Voudouris KM Greenwood 2001 Intelligence and Duchenne muscular dystrophy: full-scale, verbal, and performance intelligence quotients Dev Med Child Neurol 43 497 501 10.1017/S0012162201000913 1:STN:280: DC%2BD3Mvhtl2juw%3D%3D 11463183
14. SE Cyrulnik VJ Hinton 2008 Duchenne muscular dystrophy: a cerebellar disorder? Neurosci Biobehav Rev 32 486 496 10.1016/j.neubiorev.2007.09.001 1:CAS:528:DC%2BD1cXhsVOqsLY%3D 18022230 (Pubitemid 351173333)
15. V Dubowitz 1965 Intellectual impairment in muscular dystrophy Arch Dis Child 40 296 301 10.1136/adc.40.211.296
16. Dubowitz V (1978) Muscle disorders in childhood. WB Saunders Company Ltd, London
17. M Durbeej KP Campbell 2002 Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models Curr Opin Genet Dev 12 349 361 10.1016/S0959-437X(02)00309-X 1:CAS:528: DC%2BD38XktFShsrw%3D 12076680 (Pubitemid 34669835)
18. AE Emery 1993 Duchenne muscular dystrophy-Meryon's disease Neuromuscul Disord 3 263 266 10.1016/0960-8966(93)90018-F 1:STN:280:DyaK2c%2Fptlejtw%3D%3D 8268722 (Pubitemid 23345041)
19. TF Freund G Buzsaki 1996 Interneurons of the hippocampus Hippocampus 6 347 470 10.1002/(SICI)1098-1063(1996)6:4<347::AID-HIPO1>3.0.CO;2-I 1:STN:280:DyaK2s%2Fnt12htQ%3D%3D 8915675
20. N Fujise Y Liu N Hori T Kosaka 1998 Distribution of calretinin immunoreactivity in the mouse dentate gyrus: II. Mossy cells, with special reference to their dorsoventral difference in calretinin immunoreactivity Neuroscience 82 181 200 10.1016/S0306-4522(97)00261-3 1:CAS:528: DyaK2sXmvFCqsL4%3D 9483514
21. FB Gaarskjaer 1978 Organization of the mossy fiber system of the rat studied in extended hippocampi. I. Terminal area related to number of granule and pyramidal cells J Comp Neurol 178 49 72 10.1002/cne.901780104 1:STN:280:DyaE1c7jtVensA%3D%3D 632370
22. A receptors containing the alpha 1 subunit to neurochemically distinct subpopulations of rat hippocampal interneurons Eur J Neurosci 6 837 853 10.1111/j.1460-9568.1994. tb00994.x 1:STN:280:DyaK2czls1amsw%3D%3D 8075825
23. L Graciotti A Minelli D Minciacchi A Procopio G Fulgenzi 2008 GABAergic miniature spontaneous activity is increased in the CA1 hippocampal region of dystrophic mdx mice Neuromuscul Disord 18 220 226 10.1016/j.nmd.2007.11.009 18207404
24. AI Gulyás K Toth P Danos TF Freund 1991 Subpopulations of GABAergic neurons containing parvalbumin, calbindin D28k, and cholecystokinin in the rat hippocampus J Comp Neurol 312 371 378 10.1002/cne.903120305 1721075
25. T Haenggi JM Fritschy 2006 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 10.1007/s00018-005-5461-0 1:CAS:528: DC%2BD28XosVemtbk%3D 16710609 (Pubitemid 44252175)
26. AE Hendrickson JF Van Brederode KA Mulligan MR Celio 1991 Development of the calcium-binding protein parvalbumin and calbindin in monkey striate cortex J Comp Neurol 307 626 646 10.1002/cne.903070409 1:CAS:528:DyaK3MXks12isbo%3D 1651352
27. TK Hensch 2005 Critical period plasticity in local cortical circuits Nat Rev Neurosci 6 877 888 10.1038/nrn1787 1:CAS:528:DC%2BD2MXhtFKls7bM 16261181 (Pubitemid 41568729)
28. EP Hoffman RH Brown LM Kundel 1987 Dystrophin: the protein product of the Duchenne muscular dystrophy locus Cell 51 919 928 10.1016/0092-8674(87)90579-4 1:CAS:528:DyaL1cXntlWqug%3D%3D 3319190 (Pubitemid 18099471)
29. FW Hopf PR Turner RA Steinhardt 2007 Calcium misregulation and the pathogenesis of muscular dystrophy Subcell Biochem 45 429 464 10.1007/978-1-4020-6191-2-16 1:STN:280:DC%2BD1c%2FktVagtQ%3D%3D 18193647
30. S Jinno T Kosaka 2002 Patterns of expression of calcium binding proteins and neuronal nitric oxide synthase in different populations of hippocampal GABAergic neurons in mice J Comp Neurol 449 1 25 10.1002/cne.10251 1:CAS:528:DC%2BD38XltlOmtbg%3D 12115690 (Pubitemid 34625691)
31. S Jinno T Kosaka 2006 Cellular architecture of the mouse hippocampus: a quantitative aspect of chemically defined GABAergic neurons with stereology Neurosci Res 56 229 245 10.1016/j.neures.2006.07.007 1:CAS:528: DC%2BD28XhtFSlu7vN 16930755 (Pubitemid 44572535)
32. S Jinno T Klausberger LF Marton Y Dalezios JD Roberts P Fuentealba EA Bushong D Henze G Buzsáki P Somogyi 2007 Neuronal diversity in GABAergic long-range projections from the hippocampus J Neurosci 27 8790 8804 10.1523/JNEUROSCI.1847-07.2007 1:CAS:528:DC%2BD2sXhtVegt7nJ 17699661 (Pubitemid 47292765)
33. Y Kawaguchi H Katsumaru T Kosaka CW Heizmann K Hama 1987 Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin Brain Res 416 369 374 10.1016/0006-8993(87)90921-8 1:CAS:528:DyaL2sXltFejurc%3D 3304536 (Pubitemid 17103934)
34. TW Kim K Wu JL Xu IB Black 1992 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 10.1073/pnas.89.23. 11642 1:CAS:528:DyaK3sXlslCrsw%3D%3D 1454857
35. T Klausberger LF Marton J O'Neill JH Huck Y Dalezios P Fuentealba WY Suen E Papp T Kaneko M Watanabe J Csicsvari P Somogyi 2005 Complementary roles of cholecystokinin- and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations J Neurosci 25 9782 9793 10.1523/JNEUROSCI.3269-05.2005 1:CAS:528:DC%2BD2MXht1WqsrbL 16237182 (Pubitemid 41510918)
36. I Knuesel M Mastrocola RA Zuellig B Bornhauser MC Schaub JM Fritschy 1999 Short communication: altered synaptic clustering of GABAA receptors in mice lacking dystrophin (mdx mice) Eur J Neurosci 11 4457 4462 10.1046/j.1460-9568. 1999.00887.x 1:STN:280:DC%2BD3c%2Fmt1Gitg%3D%3D 10594673 (Pubitemid 30009278)
37. I Knuesel RA Zuellig MC Schaub JM Fritschy 2001 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 10.1046/j.0953-816x.2001.01476.x 1:STN:280:DC%2BD3MzlsFSjuw%3D%3D 11285009 (Pubitemid 32275749)
38. JS Lee Z Pfund C Juhász ME Behen O Muzik DC Chugani MA Nigro HT Chugani 2002 Altered regional brain glucose metabolism in Duchenne muscular dystrophy: a pet study Muscle Nerve 26 506 512 10.1002/mus.10238 12362416
39. C Leranth CE Ribak 1991 Calcium-binding proteins are concentrated in the CA2 field of the monkey hippocampus: a possible key to this region's resistance to epileptic damage Exp Brain Res 85 129 136 10.1007/BF00229993 1:STN:280:DyaK3MzlslSrtw%3D%3D 1884753
40. HG Lidov 1996 Dystrophin in the nervous system Brain Pathol 6 63 77 10.1111/j.1750-3639.1996.tb00783.x 1:CAS:528:DyaK28Xhs1Klurg%3D 8866748
41. HG Lidov TJ Byers LM Kunkel 1993 The distribution of dystrophin in the murine central nervous system: an immunocytochemical study Neuroscience 54 167 187 10.1016/0306-4522(93)90392-S 1:CAS:528:DyaK3sXksVGqtrs%3D 8515841 (Pubitemid 23147097)
42. Y Liu N Fujise T Kosaka 1996 Distribution of calretinin immunoreactivity in the mouse dentate gyrus. I. General description Exp Brain Res 108 389 403 10.1007/BF00227262 1:STN:280:DyaK283msFOqsg%3D%3D 8801119
43. Luna LG (1968) Manual of histologic staining methods of the armed forces institute of pathology, vol 3rd. McGraw-Hill, New York
44. MF Mehler KZ Haas JA Kessler PK Stanton 1992 Enhanced sensitivity of hippocampal pyramidal neurons from mdx mice to hypoxia-induced loss of synaptic transmission Proc Natl Acad Sci USA 89 2461 2465 10.1073/pnas.89.6.2461 1:CAS:528:DyaK38XitFags7Y%3D 1549609
45. A Mercer HL Trigg AM Thomson 2007 Characterization of neurons in the CA2 subfield of the adult rat hippocampus J Neurosci 27 7329 7338 10.1523/JNEUROSCI.1829-07.2007 1:CAS:528:DC%2BD2sXot1egtb8%3D 17611285 (Pubitemid 47037564)
46. Minciacchi D, Del Tongo C, Nosi D, Carretta D, Catini C, Granato A (2007) Organization of cortico-cortical associative projections in the motor and somatosensory regions of the mutant mdx mouse. Italian Society for Neuroscence Congress 2007, Verona, 27-30 September, SUN-41
47. R Miranda C Sébrié J Degrouard B Gillet D Jaillard S Laroche C Vaillend 2009 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 10.1093/cercor/bhn135 1:STN:280:DC%2BD1M7oslelug%3D%3D 18794205
48. E Moser MB Moser P Andersen 1993 Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions J Neurosci 13 3916 3925 1:STN:280:DyaK3sznsFehtg%3D%3D 8366351
49. MB Moser EI Moser 1998 Functional differentiation in the hippocampus Hippocampus 8 608 619 10.1002/(SICI)1098-1063(1998)8:6<608::AID-HIPO3>3.0. CO;2-7 1:STN:280:DyaK1M%2Fps1entw%3D%3D 9882018 (Pubitemid 29010188)
50. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic Press, San Diego
51. C Pittenger YY Huang RF Paletzki R Bourtchouladze H Scanlin S Vronskaya ER Kandel 2002 Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory Neuron 34 447 462 10.1016/S0896-6273(02)00684-0 1:CAS:528:DC%2BD38XjsFGgu7Y%3D 11988175 (Pubitemid 34465502)
52. C Rae JL Griffin DH Blair JH Bothwell WA Bubb A Maitland S Head 2002 Abnormalities in brain biochemistry associated with lack of dystrophin: studies of the mdx mouse Neuromuscul Disord 12 121 129 10.1016/S0960-8966(01)00253-X 11738353 (Pubitemid 33152729)
53. O Sakurai T Kosaka 2007 Nonprincipal neurons and CA2 pyramidal cells, but not mossy cells are immunoreactive for calcitonin gene-related peptide in the mouse hippocampus Brain Res 1186 129 143 10.1016/j.brainres.2007.10.032 1:CAS:528:DC%2BD2sXhsVSmu7%2FN 18005945
54. A Sbriccoli M Santarelli D Carretta F Pinto A Granato D Minciacchi 1995 Architectural changes of the cortico-spinal system in the mouse dystrophin defective mdx mouse Neurosci Lett 200 53 56 10.1016/0304-3940(95)12079-J 1:CAS:528:DyaK2MXpt1arsr4%3D 8584266
55. EM Schneider Gasser V Duveau GA Prenosil JM Fritschy 2007 Reorganization of GABAergic circuits maintains GABAA receptor-mediated transmission onto CA1 interneurons in alpha1-subunit-null mice Eur J Neurosci 25 3287 3304 10.1111/j.1460-9568.2007.05558.x 17552997 (Pubitemid 46872760)
56. DC Sterio 1984 The unbiased estimation of number and sizes of arbitrary particles using the disector J Microsc 134 127 136 1:STN:280: DyaL2c3kt1yjtw%3D%3D 6737468
57. S Torelli V Sogos MG Ennas F Muntoni A Clerk PN Strong F Gremo 1992 Dystrophin immunoreactivity in normal and Duchenne human fetal neurons in culture J Neurosci Res 32 116 125 10.1002/jnr.490320114 1:CAS:528: DyaK38XisFenur8%3D 1378503
58. M Uchino H Teramoto H Naoe K Yoshioka T Miike M Ando 1994 Localisation and characterisation of dystrophin in the central nervous system of controls and patients with Duchenne muscular dystrophy J Neurol Neurosurg Psychiatry 57 426 429 10.1136/jnnp.57.4.426 1:STN:280:DyaK2c3hs1yrtw%3D%3D 8163990 (Pubitemid 24118137)
59. C Vaillend JM Billard P Dutar T Claudepierre A Rendon A Ungerer 1998 Spatial discrimination learning and CA1 hippocampal synaptic plasticity in mdx and mdx3cv mice lacking dystrophin-brain isoforms Neuroscience 86 53 66 10.1016/S0306-4522(98)00023-2 1:CAS:528:DyaK1cXktFCnt70%3D 9692743 (Pubitemid 28270855)
60. C Vaillend JM Billard 2002 Facilitated CA1 hippocampal synaptic plasticity in dystrophin-deficient mice: role for GABAA receptors? Hippocampus 12 713 717 10.1002/hipo.10068 1:CAS:528:DC%2BD3sXotFCitg%3D%3D 12542223 (Pubitemid 36113671)
61. C Vaillend JM Billard S Laroche 2004 Impaired long-term spatial and recognition memory and enhanced CA1 hippocampal LTP in the dystrophin-deficient Dmd(mdx) mouse Neurobiol Dis 17 10 20 10.1016/j.nbd.2004.05.004 1:CAS:528:DC%2BD2cXntlaru78%3D 15350961 (Pubitemid 39209308)
62. EA van Vliet E Aronica EA Tolner FH Lopes da Silva JA Gorter 2004 Progression of temporal lobe epilepsy in the rat is associated with immunocytochemical changes in inhibitory interneurons in specific regions of the hippocampal formation Exp Neurol 187 367 379 10.1016/j.expneurol.2004.01.016 15144863 (Pubitemid 38610283)
63. T Wallis WA Bubb JA McQuillan VJ Balcar C Rae 2004 For want of a nail. Ramifications of a single gene deletion, dystrophin, in the brain of the mouse Front Biosci 9 74 84 10.2741/1209 1:CAS:528:DC%2BD2cXhtFCktb0%3D 14766346
64. MJ West L Slomianka HJ Gundersen 1991 Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator Anat Rec 231 482 497 10.1002/ar.1092310411 1:STN:280:DyaK387ntFWrtw%3D%3D 1793176
65. Y Yoshihara H Onodera K Iinuma Y itoyama 2003 Abnormal kainic acid receptor density and reduced seizure susceptibility in dystrophin-deficient mdx mice Neuroscience 117 391 395 10.1016/S0306-4522(02)00876-X 1:CAS:528: DC%2BD3sXhsVChs7Y%3D 12614679 (Pubitemid 36259753)