Cerebellar cortex development in the weaver condition presents regional and age-dependent abnormalities without differences in Purkinje cells neurogenesis

• Autorzy: Marti J. , Santa-Cruz M.C. , Hervas J.P. , Bayer S.A. , Villegas S.
• Języki publikacji: EN

Abstrakty

EN

Ataxias are neurological disorders associated with the degeneration of Purkinje cells (PCs). Homozygous weaver mice (wv/wv) have been proposed as a model for hereditary cerebellar ataxia because they present motor abnormalities and PC loss. To ascertain the physiopathology of the weaver condition, the development of the cerebellar cortex lobes was examined at postnatal day (P): P8, P20 and P90. Three approaches were used: 1) quantitative determination of several cerebellar features; 2) qualitative evaluation of the developmental changes occurring in the cortical lobes; and 3) autoradiographic analyses of PC generation and placement. Our results revealed a reduction in the size of the wv/wv cerebellum as a whole, confirming previous results. However, as distinguished from these reports, we observed that quantified parameters contribute differently to the abnormal growth of the wv/wv cerebellar lobes. Qualitative analysis showed anomalies in wv/wv cerebellar cytoarchitecture, depending on the age and lobe analyzed. Such abnormalities included the presence of the external granular layer after P20 and, at P90, ectopic cells located in the molecular layer following several placement patterns. Finally, we obtained autoradiographic evidence that wild-type and wv/wv PCs presented similar neurogenetic timetables, as reported. However, the innovative character of this current work lies in the fact that the neurogenetic gradients of wv/wv PCs were not modified from P8 to P90. A tendency for the accumulation of late-formed PCs in the anterior and posterior lobes was found, whereas early-generated PCs were concentrated in the central and inferior lobes. These data suggested that wv/wv PCs may migrate properly to their final destinations. The extrapolation of our results to patients affected with cerebellar ataxias suggests that all cerebellar cortex lobes are affected with several age-dependent alterations in cytoarchitectonics. We also propose that PC loss may be regionally variable and not related to their neurogenetic timetables.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2016
• Tom: 76
• Numer: 1
• Opis fizyczny: p.53-65,fig.,ref.

Twórcy

autor

Marti J.

• Departament de Biologia Cellular, de Fisiologia i d’Immunologia, Unidad de Citologia i d’Histologia, Facultat de Biociències, Universitat Autonoma de Barcelona, Barcelona, Spain

autor

Santa-Cruz M.C.

• Departament de Biologia Cellular, de Fisiologia i d’Immunologia, Unidad de Citologia i d’Histologia, Facultat de Biociències, Universitat Autonoma de Barcelona, Barcelona, Spain

autor

Hervas J.P.

• Departament de Biologia Cellular, de Fisiologia i d’Immunologia, Unidad de Citologia i d’Histologia, Facultat de Biociències, Universitat Autonoma de Barcelona, Barcelona, Spain

autor

Bayer S.A.

• Laboratory of Developmental Neurobiology, Indianapolis, USA

autor

Villegas S.

• Departament de Bioquímica i Biologia Molecular, Facultat de Biociencies, Universitat Autonoma de Barcelona, Barcelona, Spain

Bibliografia

• Ahmed OM, Abd El-Tawab SM, Ahmed RG (2010) Effects of experimentally induced maternal hypothyroidism and hyperthyroidism on the development of rat offspring: I. The development of the thyroid hormones-neurotransmitters and adenosinergic system interactions. Int J Dev Neurosci 28: 437–454.
• Altman J (1973) Experimental reorganization of the cerebellar cortex III. Regeneration of the external germinal layer and granule cell ectopia. J Comp Neurol 149: 153–180.
• Altman J, Bayer SA (1997) Development of the Cerebellar System: In Relation to its Evolution, Structure and Functions. CRC Press, Inc. Boca Raton, USA. Armstrong C, Hawkes R (2001) Selective Purkinje cell ectopia in the cerebellum of the weaver mouse. J Comp Neurol 439: 151–161.
• Bayer SA, Altman J (1987) Directions in neurogenetic gradients and patterns of anatomical connections in the telencephalon. Prog Neurobiol 29: 57–106.
• Bayer SA, Wills KV, Wei J, Feng Y, Dlouhy SR, Hodes ME, Verina T, Ghetti B (1996) Phenotypic effects of the weaver gene are evident in the embryonic cerebellum but not in the ventral midbrain. Brain Res Dev Brain Res 96: 130–137.
• Blatt BJ, Eisenman LM (1985) A quantitative and quantitative light microscopic study of the inferior olivary complex of normal, reeler, and weaver mutant mice. J Comp Neurol 232: 117–128.
• Bottone MG, Veronica DB, Piccolini VM, Bottiroli G, De Pascali SA, Fanizzi FP, Bernocchi G (2012) Developmental expression of cellular prion protein and apoptotic molecules in the rat cerebellum: effects of platinum compounds. J Chem Neuroanat 46: 19–29.
• Cavalcanti-Kwiatkoski R, Raisman-Vozari R, Ginestet L, Del Bel E (2010) Altered expression of neuronal nitric oxide synthase in weaver mutant mice. Brain Res 1326: 40–50.
• Cedelin J (2014) From mice to men: lessons from mutant ataxic mice. Cerebellum Ataxias 1: 4 [doi:10.1186/2053-8871-1-4].
• Chedotal A (2010) Should I stay or should I go? Becoming a granule cell. Trends Neurosci 33: 163–172.
• Cheng SV, Nadeau JH, Tanzi RE, Watkins PC, Jagadesh J, Taylor BA, Haines JL, Sacchi N, Gusella JF (1988) Comparative mapping of DNA markers from familial Alzheimer disease and Down syndrome regions of human chromosome 21 to mouse chromosomes 16 and 17. Proc Natl Acad Sci USA 85: 6032–6036.
• Eisenman LM, Gallagher E, Hawkes R (1998) Regionalization defects in the weaver cerebellum. J Comp Neurol 394: 431–444.
• Goldowitz D, Hamre K (1998) The cells and molecules that make a cerebellum. Trends Neurosci 21: 375–382.
• Grüsser-Cornehls U, Bäule J (2001) Mutant mice as a model for cerebellar ataxia. Progress in Neurobiology 63: 489–540.
• Harkins AB, Fox AP (2002) Cell death in weaver mouse cerebellum. Cerebellum 3: 201–206.
• Harrison SM, Roffler-Tarlov S K (1998). Cell death during development of testis and cerebellum in the mutant mouse weaver. Dev Biol 195: 174–178.
• Hashimoto M, Mikoshiba K (2003) Mediolateral compartmentalization of the cerebellum is determined on the birth date of Purkinje cells. J Neurosci 23: 11342–11351.
• Hatten ME, Liem RKH, Mason CA (1986) Weaver mouse cerebellar granule neurons fail to migrate on wild-type astroglial processes in vitro. J Neurosci 6: 2676–2683.
• Herrup K, Trenkner E (1987) Regional differences in cytoarchitecture of the weaver cerebellum suggest a new model for weaver gene action. Neuroscience 23: 871–885.
• Lalonde R, Strazielle C (2007) Spontaneous and induced mouse mutations with cerebellar dysfunctions: behavior and neurochemistry. Brain Res 1140: 51–74
• Lange W (1982) Regional differences in the cytoarchitecture of the cerebellar cortex. In: The cerebellum: new vistas (Palay SL CV, Ed.). Springer-Verlag, Berlin, Germany. p. 93–107.
• Larsell O (1952) The morphogenesis and adult pattern of the lobules and fissures of the cerebellum of the white rat. J Comp Neurol 97: 281–356.
• Leto K, Rolando C, Rossi F (2012) The genesis of cerebellar GABAergic neurons: fate potential and specification mechanisms. Front Neuroanat 6: 6 [doi: 10.3389/fnana.2012.00006].
• Manto M, Marmolino D (2009) Animal models of human cerebellar ataxias: a cornerstone for the therapies of the twenty-first century. Cerebellum 8: 137–154.
• Maricich SM, Soha J, Trenkner E, Herrup K (1997) Failed cell migration and death of Purkinje cells and deep nuclear neurons in the weaver cerebellum. J Neurosci 17: 3675–3683.
• Martí J, Santa-Cruz MC, Bayer SA, Ghetti B, Hervas JP (2007) Purkinje cell age-distribution in fissures and in foliar crowns: a comparative study in the weaver cerebellum. Brain Struct Funct 212: 347–357.
• Martí J, Santa-Cruz MC, Molina V, Serra R, Bayer SA, Ghetti, B and Hervás JP (2009) Regional differences in the vulnerability of substantia nigra dopaminergic neurons in weaver mice. Acta Neurobiol Exp (Wars) 69: 198–206.
• Martí J, Santa-Cruz MC, Serra R, Valero O, Molina V, Hervás JP, Villegas S (2013) Principal component and cluster analysis of morphological variables reveals multiple discrete sub-phenotypes in weaver mouse mutants. Cerebellum 12: 406–417.
• Martí J, Wills KW, Ghetti B, Bayer SA (2001) Evidence that the loss of Purkinje cells and deep cerebellar nuclei neurons in homozygous weaver is not related to neurogenetic patterns. Int J Dev Neuroscience 19: 599–610.
• Martí J, Wills KV, Ghetti B, Bayer SA (2002) A combined immunohistochemical and autoradiographic method to detect midbrain dopaminergic neurons and determine their time of origin. Brain Res Brain Res Protoc 9: 197–205.
• Namba K, Sugihara I, Hashimoto M (2011) Close correlation between the birth date of Purkinje cells and the longitudinal compartmentalization of the mouse adult cerebellum. J Comp Neurol 519: 2594–2614.
• Oster-Granite ML, Herndon RM (1976) The pathogenesis of parvovirusinduced cerebellar hypoplasia in the Syrian hamster, Mesocricetus auratus. Fluorescent antibody, foliation, cytoarchitecture, Golgi and electron microscopic studies. J Comp Neurol 169: 481–521.
• Ozaki M, Hashikawa T, Ikeda K, Miyakawa Y, Ichikawa T, Ishihara Y, Kumanishi T, Yano R (2002) Degeneration of pontine mossy fibers during cerebellar development in weaver mutant mice. Eur J Neurosci 16: 565–574.
• Patil N, Cox DR, Bhat D, Faham M, Myers RM, Peterson AS (1995) A  potassium channel mutation in weaver mice implicates membrane excitability in granule cell differentiation. Nat Genet 11: 126–129.
• Rakic P, Sidman RL (1973a) Sequence of development abnormalities leading to granule cell deficit in cerebellar cortex of weaver mutant mice. J Comp Neurol 152: 103–132.
• Rakic P, Sidman RL (1973b) Organization of cerebellar cortex secondary to deficit of granule cells in weaver mutant mice. J Comp Neurol 152: 133–162.
• Reeber SL, Otis, TS, Sillitoe RV (2013) New roles for the cerebellum in heath and disease. Front Syst Neurosci 7: 83 [doi: 10.3389/fnsys.2013.00083].
• Reeves RH, Crowley MR, Lorenzon N, Pavan WJ, Smeyne RJ, Goldowitz D (1989) The mouse neurological mutant weaver maps within the region of chromosome 16 that is homologous to human chromosome 21. Genomics 5: 522–526.
• Rezai Z, Yoon CH (1972) Abnormal rate of granule cell migration in the cerebellum of weaver mutant mice. Dev Biol 29: 17–26.
• Schein JC, Hunter DD, Roffler-Tarlov S (1998) Girk2 expression in the ventral midbrain, cerebellum, and olfactory bulb and its relationship to the murine mutation weaver. Dev Biol 204: 432–450. 5_595_Marti_v4.indd 64 18/04/16 21:14
• Schilling K, Oberdick J, Rossi F, Baader SL (2008) Besides Purkinje cells and granule neurons: an appraisal of the cell biology of the interneurons of the cerebellar cortex. Histochem Cell Biol 130: 601–615.
• Sekigucchi M, Nowakowski RS, Nagato Y, Tanaka O, Guo H, Madoka M, Abe  H (1995) Morphologial abnormalities in the hippocampus of the weaver mutant mouse. Brain Res 696: 262–267.
• Smeyne RJ, Pickford LB, Rouse RV, Napieralski J, Goldowitz D (1991) Abormalities in premigratory granule cells in the weaver cerebellum defined by monoclonal OZ42. Anat Embryol (Berl) 183: 213–219.
• Triarhou LC, Norton J, Ghetti B (1988) Mesencephalic dopamine cell deficit involves areas A8, A9 and A10 in weaver mutant mice. Exp Brain Res 70: 256–265.
• Vaillant C, Monard D (2009) SHH pathway and cerebellar development. Cerebellum 8: 291–301.
• Verina T, Tang X, Fitzpatrick L, Norton J, Vogelweid CM, Ghetti B (1995). Degeneration of Sertoli and spermatogenic cells in homozygous and heterozygous weaver mice. J. Neurogenet 9: 251–265.
• Wahlsten D, Andison M (1991) Patterns of cerebellar foliation in recombinant inbred mice. Brain Res 557: 184–189.
• Wei J, Dlouhy S R, Bayer S, Piva R, Verina T, Wang Y, Feng Y, Dupree B, Hodes ME, Ghetti B (1997) In situ hybridization analysis of Girk2 expression in the developing central nervous system in normal and weaver Mice. J Neuropathol Exp Neurol 56: 762–771.
• Wei J, Hodes ME, Piva R, Feng Y, Wang B, Ghetti B (1998) Characterization of murine Girk2 transcript isoforms: structure and differential expression. Genomics 51: 379–390.
• Wei J, Hodes ME, Wang Y, Feng Y, Ghetti B, Dlouhy SR (1996) cDNA selection with DNA microdissected from mouse chromosome 16: isolation of novel clones and construction of a partial transcription map of the C3-C4 region. Genome Res 6: 678–687.
• Whorton MR, Mackkinnon R (2013). X-ray structure of the mammalian GIRK2-βγ G-protein complex. Nature 498: 190–197.
• Willinger M, Margolis DM (1985). Effect of the weaver (wv) mutation on cerebellar neuron differentiation. II. Quantification of neuron behavior in culture. Dev Biol 107: 173–179.
• Wullimann MF, Mueller T, Distel M, Babaryka A, Grothe B, Köster RW (2011) The long adventurous journey of rhombic lip cells in jawed vertebrates: a comparative developmental analysis. Front Neuroanat 21: 5–27.