Reduced subventricular zone proliferation and white matter damage in juvenile ferrets with kaolin-induced hydrocephalus

(STAIR) STAIR Group, 1999, Recommendations for standards regarding preclinical neuroprotective and restorative drug development, Stroke, 30, 2752, 10.1161/01.STR.30.12.2752 Aliev, 2006, Ultrastructural analysis of a murine model of congenital hydrocephalus produced by overexpression of transforming growth factor-beta1 in the central nervous system, Submicrosc. Cytol. Pathol., 38, 85 Barnette, 2009, Characterization of brain development in the ferret via MRI, Pediatr. Res., 66, 80, 10.1203/PDR.0b013e3181a291d9 Boillat, 1997, Ultrastructural changes in the deep cortical pyramidal cells of infant rats with inherited hydrocephalus and the effect of shunt treatment, Exp. Neurol., 147, 377, 10.1006/exnr.1997.6617 Borrell, 2012, Emerging roles of neural stem cells in cerebral cortex development and evolution, Dev. Neurobiol., 72, 955, 10.1002/dneu.22013 Bradley, 1986, Flowing cerebrospinal fluid in normal and hydrocephalic states: appearance on MR images, Radiology, 159, 611, 10.1148/radiology.159.3.3704142 Braun, 1988, lmmunocytochemical localization by electron microscopy of 2′,3′-cyclic nucleotide 3′-phosphodiesterase in developing oligodendrocytes of normal and mutant brain, J. Neurosci., 8, 3057, 10.1523/JNEUROSCI.08-08-03057.1988 Brewer, 2001, Attention processes in children with shunted hydrocephalus versus attention deficit-hyperactivity disorder, Neuropsychology, 15, 185, 10.1037/0894-4105.15.2.185 Brody, 1987, Sequence of central nervous system myelination in human infancy. I. An autopsy study of myelination, J. Neuropathol. Exp. Neurol., 46, 283, 10.1097/00005072-198705000-00005 Burmeister, 2005, Attention problems and executive functions in children with spina bifida and hydrocephalus, Child Neuropsychol., 11, 265, 10.1080/092970490911324 Castejon, 1994, Transmission electron microscope study of human hydrocephalic cerebral cortex, J. Submicrosc. Cytol. Pathol., 26, 29 Chen, 2008, The basic helix–loop–helix transcription factor Olig2 is critical for reactive astrocyte proliferation after cortical injury, J. Neurosci., 28, 10983, 10.1523/JNEUROSCI.3545-08.2008 Christensson, 2005, Time course of postnatal motor development in ferrets: ontogenetic and comparative perspectives, Behav. Brain Res., 158, 231, 10.1016/j.bbr.2004.09.003 Clancy, 2001, Translating developmental time across mammalian species, Neuroscience, 105, 7, 10.1016/S0306-4522(01)00171-3 da Silva Lopes, 2009, Characterization of juvenile and young adult mice following induction of hydrocephalus with kaolin, Exp. Neurol., 219, 187, 10.1016/j.expneurol.2009.05.015 Darlington, 1999, Neural development in metatherian and eutherian mammals: variation and constraint, J. Comp. Neurol., 411, 359, 10.1002/(SICI)1096-9861(19990830)411:3<359::AID-CNE1>3.0.CO;2-J Del Bigio, 1993, Neuropathological changes caused by hydrocephalus, Acta Neuropathol., 85, 573, 10.1007/BF00334666 Del Bigio, 2000, Calcium-mediated proteolytic damage in white matter of hydrocephalic rats?, J. Neuropathol. Exp. Neurol., 59, 946, 10.1093/jnen/59.11.946 Del Bigio, 2001, Future directions for therapy of childhood hydrocephalus: a view from the laboratory, Pediatr. Neurosurg., 34, 172, 10.1159/000056016 Del Bigio, 2001, Pathophysiologic consequences of hydrocephalus, Neurosurg. Clin. N. Am., 12, 639, 10.1016/S1042-3680(18)30022-6 Del Bigio, 2004, Cellular damage and prevention in childhood hydrocephalus, Brain Pathol., 14, 317, 10.1111/j.1750-3639.2004.tb00071.x Del Bigio, 2010, Neuropathology and structural changes in hydrocephalus, Dev. Disabil. Res. Rev., 16, 16, 10.1002/ddrr.94 Del Bigio, 1988, Changes in periventricular vasculature of rabbit brain following induction of hydrocephalus and after shunting, J. Neurosurg., 69, 115, 10.3171/jns.1988.69.1.0115 Del Bigio, 1998, Cell death, axonal damage, and cell birth in the immature rat brain following induction of hydrocephalus, Exp. NeuroI., 154, 157, 10.1006/exnr.1998.6922 Del Bigio, 1994, Acute and chronic cerebral white matter damage in neonatal hydrocephalus, Can. J. Neurol. Sci., 21, 299, 10.1017/S0317167100040865 Del Bigio, 1997, Magnetic resonance imaging and behavioral analysis of immature rats with kaolin-induced hydrocephalus: pre- and postshunting observations, Exp. Neurol., 148, 256, 10.1006/exnr.1997.6644 Del Bigio, 1997, Myelination delay in the cerebral white matter of immature rats with kaolin-induced hydrocephalus is reversible, J. Neuropathol. Exp. Neurol., 56, 1053, 10.1097/00005072-199709000-00010 Del Bigio, 2003, Chronic hydrocephalus in rats and humans: white matter loss and behavior changes, Ann. Neurol., 53, 337, 10.1002/ana.10453 Dimou, 2008, Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex, J. Neurosci., 28, 10434, 10.1523/JNEUROSCI.2831-08.2008 Dixon, 1932, Experimentelle hypertonie durch Eröhung des intrakaniellen Druckes, Arch. Exp. Pathol. Pharmakol., 166, 265, 10.1007/BF01860670 Eskandari, 2004, Effects of hydrocephalus and ventriculoperitoneal shunt therapy on afferent and efferent connections in the feline sensorimotor cortex, J. Neurosurg., 101, 196 Eskandari, 2011, Reactive astrocytosis in feline neonatal hydrocephalus: acute, chronic, and shunt-induced changes, Childs Nerv. Syst., 27, 2067, 10.1007/s00381-011-1552-4 Fietz, 2010, OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling, Nat. Neurosci., 13, 690, 10.1038/nn.2553 Fisher, 2009, Update of the stroke therapy academic industry roundtable preclinical recommendations, Stroke, 40, 2244, 10.1161/STROKEAHA.108.541128 Haddad, 1980, Use of the ferret in experimental neuroteratology: cerebral, cerebellar, and retinal dysplasias induced Ьу methylazoxymethanol acetate (chapter 3), vol. 4, 45 Hayes, 2003, Two epochs in the development of gamma-aminobutyric acidergic neurons in the ferret thalamus, J. Comp. Neurol., 463, 45, 10.1002/cne.10749 Hochwald, 1985, Animal models of hydrocephalus: recent developments, Proc. Soc. Exp. Biol. Med., 178, 1, 10.3181/00379727-178-41977 Jack, 1987, MR findings in normal-pressure hydrocephalus: significance and comparison with other forms of dementia, J. Comput. Assist. Tomogr., 11, 923, 10.1097/00004728-198711000-00001 Jackson, 1985, Use of ferrets in studies of the visual system, Lab. Anim. Sci., 35, 211 Jackson, 1989, Visual cortex development in the ferret. I. Genesis and migration of visual cortical neurons, J. Neurosci., 9, 1242, 10.1523/JNEUROSCI.09-04-01242.1989 Jacobson, 1963, Sequence of myelinization in the brain of the albino rat. A. Cerebral cortex, thalamus and related structures, J. Comp. Neurol., 121, 5, 10.1002/cne.901210103 Janzen, 1990, Glycerylphosphocholine phosphocholine phosphodiesterase activity is reduced in multiple sclerosis plaques, Exp. Neurol., 109, 243, 10.1016/0014-4886(90)90079-8 Jiménez, 2009, Disruption of the neurogenic niche in the subventricular zone of postnatal hydrocephalic hyh mice, J. Neuropathol. Exp. Neurol., 68, 1006, 10.1097/NEN.0b013e3181b44a5a Kanfer, 1990, An unusual phosphodiesterase activity towards p-nitrophenylphosphorylcholine present in rat brain membranes, Neurochem. Res., 15, 987, 10.1007/BF00965744 Khan, 2006, Experimental models of hydrocephalus (chapter 26), 457 Khan, 2003, Magnesium sulfate therapy is of mild benefit to young rats with kaolin-induced hydrocephalus, Pediatr. Res., 53, 970, 10.1203/01.PDR.0000061561.42921.5B Khan, 2006, Brain damage in neonatal rats following kaolin induction of hydrocephalus, Exp. Neurol., 200, 311, 10.1016/j.expneurol.2006.02.113 Khan, 2007, Calcium antagonism in neonatal rats with kaolin-induced hydrocephalus, J. Child Neurol., 22, 1161, 10.1177/0883073807306259 Koul, 1980, UDP-galactose-ceramide galactosyltransferase in rat brain myelin subfractions during development, Biochem. J., 186, 959, 10.1042/bj1860959 Kriebel, 2000, Pathology of the hippocampus in experimental feline infantile hydrocephalus, Neurol. Res., 22, 29, 10.1080/01616412.2000.11741035 Kriebel, 1993, The microstructure of cortical neuropil before and after decompression in experimental infantile hydrocephalus, Exp. Neurol., 119, 89, 10.1006/exnr.1993.1009 Lockard, 1985, The forebrain of the ferret, Lab. Anim. Sci., 35, 216 Margolis, 1969, Hydrocephalus in hamsters, ferrets, rats, and mice following inoculations with reovirus type I. II. Pathologic studies, Lab. Invest., 21, 189 Marshall, 2005, Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells, J. Neurosci., 25, 7289, 10.1523/JNEUROSCI.1924-05.2005 Martínez-Cerdeño, 2012, Comparative analysis of the subventricular zone in rat, ferret and macaque: evidence for an outer subventricular zone in rodents, PLoS One, 7, 1, 10.1371/journal.pone.0030178 Mashayekhi, 2002, Deficient cortical development in the hydrocephalic Texas (H-Tx) rat: a role for CSF, Brain, 125, 1859, 10.1093/brain/awf182 McAllister, 2012, Pathophysiology of congenital and neonatal hydrocephalus, Semin. Fetal Neonatal. Med., 17, 285, 10.1016/j.siny.2012.06.004 McAllister, 1998, Neonatal hydrocephalus. Mechanisms and consequences, Neurosurg. Clin. N. Am., 9, 73, 10.1016/S1042-3680(18)30281-X McAllister, 1991, Progression of experimental infantile hydrocephalus and effects of ventriculoperitoneal shunts: an analysis correlating magnetic resonance imaging with gross morphology, Neurosurgery, 29, 329, 10.1227/00006123-199109000-00001 McSherry, 1986, Cell production gradients in the developing ferret isocortex, J. Anat., 144, 1 Miller, 2007, Reduction of astrogliosis and microgliosis by cerebrospinal fluid shunting in experimental hydrocephalus, Cerebrospinal Fluid Res., 4, 5, 10.1186/1743-8454-4-5 Miyan, 1998, Cell death in the brain of the HTx rat, Eur. J. Pediatr. Surg., 8, 43, 10.1055/s-2008-1071253 Neal, 2007, Insights into the gyrification of developing ferret brain by magnetic resonance imaging, J. Anat., 210, 66, 10.1111/j.1469-7580.2006.00674.x Noctor, 1997, Histogenesis of ferret somatosensory cortex, J. Comp. Neurol., 387, 179, 10.1002/(SICI)1096-9861(19971020)387:2<179::AID-CNE2>3.0.CO;2-Y Owen-Lynch, 2003, Defective cell cycle control underlies abnormal cortical development in the hydrocephalic Texas rat, Brain, 126, 623, 10.1093/brain/awg058 Rabe, 1985, Behavior and neurobehavioral teratology using the ferret, Lab. Anim. Sci., 35, 256 Reillo, 2012, Germinal zones in the developing cerebral cortex of ferret: ontogeny, cell cycle kinetics, and diversity of progenitors, Cereb. Cortex, 22, 2039, 10.1093/cercor/bhr284 Reillo, 2011, A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex, Cereb. Cortex, 21, 1674, 10.1093/cercor/bhq238 Remahl, 1982, Changing relation between onset of myelination and axon diameter range in developing feline white matter, J. Neurol. Sci., 54, 33, 10.1016/0022-510X(82)90216-7 Roussel, 1987, Immunocytochemical localization of UDP-galactose: ceramide galactosyltransferase in myelin and oligodendroglial cells of rat brain, J. Neurocytol, 16, 85, 10.1007/BF02456700 Sarnat, 2011, Mitochondrial “hypermetabolic” neurons in paediatric epileptic foci, Can. J. Neurol. Sci., 38, 909, 10.1017/S0317167100012518 Schmechel, 1979, A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes, Anat. Embryol., 156, 115, 10.1007/BF00300010 Sok, 1994, Brain myelin-bound Zn(2+)-glycerophosphocholine cholinephosphodiesterase is a glycosylphosphatidylinositol-anchored enzyme of two different molecular forms, Neurochem. Res., 19, 97, 10.1007/BF00966735 Sokoloff, 1997, Thermogenic, respiratory, and ultrasonic responses of week-old rats across the transition from moderate to extreme cold exposure, Dev. Psychobiol., 30, 181, 10.1002/(SICI)1098-2302(199704)30:3<181::AID-DEV1>3.0.CO;2-L Takebayashi, 2002, The basic helix–loop–helix factor Olig2 is essential for the development of motoneuron and oligodendrocyte lineages, Curr. Biol., 12, 1157, 10.1016/S0960-9822(02)00926-0 Tamaki, 1990, Cerebral energy metabolism in experimental canine hydrocephalus, Childs Nerv. Syst., 6, 172, 10.1007/BF00308496 Tao, 2012, Histopathologic correlation with diffusion tensor imaging after chronic hypoxia in the immature ferret, Pediatr. Res., 71, 192, 10.1038/pr.2011.32 Tatsumi, 2008, Genetic fate mapping of Olig2 progenitors in the injured adult cerebral cortex reveals preferential differentiation into astrocytes, J. Neurosci. Res., 86, 3494, 10.1002/jnr.21862 Voigt, 1989, Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes, J. Comp. Neurol., 289, 74, 10.1002/cne.902890106 Weller, 1972, Infantile hydrocephalus: clinical, histological, and ultrastructural study of brain damage, J. Neurosurg., 36, 255, 10.3171/jns.1972.36.3.0255 Weller, 1969, Histological and ultrastructural changes with experimental hydrocephalus in adult rabbits, Brain, 92, 819, 10.1093/brain/92.4.819 Weller, 1971, Experimental hydrocephalus in young dogs: histological and ultrastructural study of the brain tissue damage, J. Neuropathol. Exp. Neurol., 30, 613, 10.1097/00005072-197110000-00006 Weller, 1978, The effects of hydrocephalus upon the developing brain. Histological and quantitative studies of the ependyma and subependyma in hydrocephalic rats, J. Neurol. Sci., 36, 383, 10.1016/0022-510X(78)90046-1 Williamson, 1992, Gliosis and ganglion cell death in the developing cat retina during hydrocephalus and after decompression, Dev. Brain Res., 70, 47, 10.1016/0165-3806(92)90102-3 Wright, 1990, Cytological and cytoarchitectural changes in the feline cerebral cortex during experimental infantile hydrocephalus, Pediatr. Neurosurg., 16, 139, 10.1159/000120516