The effect on motor cortical neuronal development of focal lesions to the sub-cortical white matter in the neonatal rat: A model for periventricular leukomalacia

International Journal of Developmental Neuroscience

Volumn 21, Issue 4, 2003, Pages 171-182

  Gibson, Claire L ^a,c   Clowry, Gavin J ^a,b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b ROYAL VICTORIA INFIRMARY   (United Kingdom)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

3 Nitropropionic acid; Brain development; Cerebral palsy; Hypoxia; Periventricular leukomalacia (PVL)

Indexed keywords

3 NITROPROPIONIC ACID; CALBINDIN; CALCIUM BINDING PROTEIN; GLUTAMIC ACID DERIVATIVE; IBOTENIC ACID; PARVALBUMIN; PROTEIN BAX; PROTEIN C JUN; SODIUM CHLORIDE; TOXIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN INJURY; BRAIN MITOCHONDRION; CALCIUM BINDING; CONTROLLED STUDY; DEVELOPMENT; FOREBRAIN; GRAY MATTER; IMMUNOHISTOCHEMISTRY; LEUKOMALACIA; MOTOR CORTEX; NERVE CELL DIFFERENTIATION; NERVE FIBER; NEURITE; NEUROFILAMENT; NISSL STAINING; NONHUMAN; PERIKARYON; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT STRAIN; WHITE MATTER;

EID: 0038022915     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0736-5748(03)00041-8     Document Type: Article

References (57)

1. Aisaka A., Aimi Y., Yasuhara O., Tooyama I., Kimura H., Shimada M. Two modes of corticospinal reinnervation occur close to spinal targets following unilateral lesion to the motor cortex in neonatal hamsters. Neuroscience. 90:1999;53-67.
2. Alcantara S., Soriano E., Ferrer I. Thalamic and basal forebrain afferents modulate the development of parvalbumin and calbindin D28k immunoreactivity in the barrel cortex of the rat. Eur. J. Neurosci. 8:1996;1522-1534.
3. Back S.A., Gan X., Li Y., Rosenberg P.A., Volpe J.J. Maturation dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J. Neurosci. 18:1998;6241-6253.
4. Back S.A., Volpe J.J. Cellular and molecular pathogenesis of periventricular white matter. Ment. Retard. Dev. Disabil. Res. Rev. 3:1997;96-107.
5. Brody B.A., Kinney H.C., Kloman A.S. Sequence of central nervous system myelination in human infancy. I. An autopsy study of myelination. J. Neuropathol. Exp. Neurol. 46:1987;283-301.
6. Cauli B., Audinat E., Lamobolez B., Angulo M.C., Ropert N., Tsuzuki K., Hestrin S., Rossier J. Molecular and physiological diversity of cortical non-pyramidal cells. J. Neurosci. 17:1997;3894-3906.
7. Celio M.R. Calbindin D28K and parvalbumin in the rat nervous system. Neuroscience. 35:1990;375-475.
8. Clowry G.J., Flecknell P.A. The successful use of fentanyl/fluanisone ('ypnorm') as an anaesthetic for intracranial surgery in neonatal rats. Lab. Anim. 34:2000;260-264.
9. Coles C.J., Edmondson D.E., Singer T.P. Inactivation of succinate dehydrogenase by 3-nitropropionate. J. Biol. Chem. 254:1979;5161-5167.
10. Dambska M., Laure-Kamionowska M., Schmidt-Sidor B. Early and late pathological changes in perinatal white matter damage. J. Child Neurol. 4:1989;29-38.
11. De Reuck J., Chatta A.S., Richardson E.P. Pathogenesis and evolution of periventricular leukomalacia in infancy. Arch. Neurol. 27:1972;229-236.
12. Donoghue J.P., Wise S.P. The motor cortex of the rat. J. Comp. Neurol. 212:1982;76-88.
13. Eyre J.A., Miller S., Clowry G.J., Conway E.A., Watts C. Functional corticospinal projections are established prenatally in the human foetus permitting involvement in the development of spinal motor centres. Brain. 123:2000;51-64.
14. Eyre J.A., Taylor J.P., Villagra F., Smith M.R., Miller S. Evidence of activity dependent withdrawal of corticospinal projections during human development. Neurology. 57:2001;1543-1554.
15. Follett P.L., Rosenberg P.A., Volpe J.J., Jensen F.E. NBQX attenuated excitotoxic injury in developing white matter. J. Neurosci. 20:2000;9235-9241.
16. Gallo V., Patneau D.K., Mayer M.L., Vaccarino F.M. Excitatory amino acid receptors in glial progenitor cells: molecular and functional properties. Glia. 11:1994;94-101.
17. Gibson C.L., Arnott G.A., Clowry G.J. Plasticity in the rat spinal cord seen in response to lesions to the motor cortex during development but not to lesions in maturity. Exp. Neurol. 166:2000;422-434.
18. Gibson C.L., Arnott G.A., Clowry G.J. Towards developing a rat model of periventricular leucomalacia. Br. Neurosci. Assoc. Abstr. 16:2001;43.
19. Gillardon F., Lenz C., Waschke K.F., Krajewski S., Reed J.C., Zimmermann M., Kuschinsky W. Altered expression of Bcl-2, Bcl-X, Bax and c-Fos colocalizes with DNA fragmentation and ischemic cell damage following middle cerebral artery occlusion in rats. Mol. Brain Res. 40:1996;254-260.
20. Grant P., Pant H.C. Neurofilament protein synthesis and phosphorylation. J. Neurocytol. 29:2000;843-872.
21. Gressens P., Besse L., Robberecht P., Gozes I., Fridkin M., Evrard P. Neuroprotection of the developing brain by systemic administration of vasoactive intestinal peptide derivatives. J. Pharmacol. Exp. Ther. 288:1999;1207-1213.
22. Hagberg H., Bona E., Gilland E., Puka-Sundvall M. Hypoxia-ischaemia model in the 7-day-old rat: possibilities and shortcomings. Acta Paediatr. Suppl. 422:1997;85-88.
23. Haldar S., Jena N., Croce C.M. Inactivation of Bcl-2 by phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 92:1995;4507-4511.
24. Herdegen T., Skene P., Bahr M. The c-Jun transcription factor - bipotential mediator of neuronal death, survival and regeneration. Trends Neurosci. 20:1997;227-231.
25. Hiscock J.J., Mackenzie L. Laminar distribution of Fos/calcium-binding protein and Fos/neurofilament protein-labeled neurons in rat motor and sensory cortex after picrotoxin-induced seizures. Exp. Neurol. 149:1998;373-383.
26. Hughes P.E., Alexi T., Walton M., Williams C.E., Dragunow M., Clark R.G., Gluckman P.D. Activity and injury dependent expression of inducible transcription factors, growth factors and apoptosis related genes within the central nervous system. Prog. Neurobiol. 57:1999;421-450.
27. Husain J., Juurlink B.H. Oligodendroglial precursor cell susceptibility to hypoxia is related to poor ability to cope with reactive oxygen species. Brain Res. 698:1995;86-94.
28. Iai M., Takashima S. Thalamocortical development of parvalbumin neurons in normal and periventricular leukomalacia brains. Neuropediatrics. 30:1999;14-18.
29. Iida K., Takashima S., Ueda K. Immunohistochemical study of myelination and oligodendrocytes in infants with periventricular leukomalacia. Pediatr. Neurol. 13:1995;296-304.
30. Johnston M.V. Selective vulnerability in the neonatal brain. Ann. Neurol. 44:1998;155-156.
31. Kawaguchi Y., Katsamuru H., Kosaka T., Heizmann C.W. Fast spiking cells in the rat hippocampus (CA1 region) contain the calcium binding protein parvalbumin. Brain Res. 416:1987;369-374.
32. King C.E., Canty A.J., Vickers J.C. Alterations in neurofilaments associated with reactive brain changes and axonal sprouting following acute physical injury to the rat neocortex. Neuropathol. Appl. Neurobiol. 27:2001;115-126.
33. Kuban K.C.K. White-matter disease of prematurity, periventricular leukomalacia, and ischemic lesions. Dev. Med. Child Neurol. 40:1998;571-573.
34. Leterrier J.F., Hartwig J., Kas J., Vegnrs R., Janmey P. Mechanical effects of neurofilament crossbridges: modulation by phosphorylation, lipids and interactions with F-actin. J. Biol. Chem. 271:1996;15687-15694.
35. Lu J., Moochhala S., Kaur C., Ling E.A. Changes in apoptosis-related protein (p53, Bax, Bcl-2 and Fos) expression with DNA fragmentation in the central nervous system of rats after closed head injury. Neurosci. Lett. 290:2000;89-92.
36. Marin-Padilla M. Developmental neuropathology and impact of perinatal brain damage. II. White matter lesions of the neocortex. J. Neuropathol. Exp. Neurol. 56:1997;219-235.
37. McCracken E., Dewar D., Hunter A.J. White matter damage following systemic injection of the mitochondrial inhibitor 3-nitropropionic acid in rat. Brain Res. 892:2001;329-335.
38. Miller P.J., Zaborsky L. 3-Nitropropionic acid neurotoxicity: visualization by silver staining and implications for use as an animal model of Huntington's disease. Exp. Neurol. 146:1997;212-229.
39. Miller S.P., Shevell M.I., Patenaude Y., O'Gorman A.M. Neuromotor spectrum of periventricular leukomalacia in children born at term. Pediatr. Neurol. 23:2000;155-159.
40. Mooney S.M., Miller M.W. Expression of bcl-2, bax and caspase-3 in the brain of the developing rat. Dev. Brain Res. 123:2000;103-117.
41. Nixon R.A., Shea T.B. Dynamics of neuronal intermediate filaments: a developmental perspective. Cell. Motil. Cytoskeleton. 22:1992;81-91.
42. Oudega M., Varon S., Haag T. Distribution of corticospinal motor neurons in the postnatal rat: quantitative evidence for massive collateral elimination and modest cell death. J. Comp. Neurol. 347:1994;115-126.
43. Paneth N., Rudeli R., Monte W., Rodriguez E. White matter necrosis in the very low birth weight infants: neuropathologic and ultrasonographic findings in infants surviving 6 days or longer. J. Pediatr. 116:1990;975-984.
44. Park S.K., Choi S.I., Jin J.K., Choi E.K., Kim J.I., Carp R.I., Kim Y.S. Differential expression of Bax and BCl-2 in the brains of hamsters infected with 263K scrapie agent. NeuroReport. 11:2000;1677-1682.
45. Perlman J.M. White matter injury in the preterm infant: an important determination of abnormal developmental outcome. Early Hum. Dev. 53:1998;99-120.
46. Raineteau O., Scwab M.E. Plasticity of motor systems after incomplete spinal cord injury. Nat. Rev. Neurosci. 2:2001;263-273.
47. Ravishankar S., Ashraf Q.M., Fritz K., Mishra O.P., Delivoria-Papadopoulos M. Expression of Bax and Bcl-2 proteins during hypoxia in cerebral cortical neuronal nuclei of newborn piglets: effects of administration of magnesium sulfate. Brain Res. 901:2001;23-29.
48. Reinoso B.S., Castro A.J. A study of corticospinal remodelling using retrograde fluorescent tracers in rats. Exp. Brain Res. 74:1989;387-394.
49. Sommer C., Gass P., Kiessling M. Selective cJun expression in CA1 neurons of the gerbil hippocampus during and after acquisition of an ischemia-tolerant state. Brain Pathol. 5:1995;135-144.
50. Staudt M., Niemann G., Grodd W., Krageloh-Mann I. The pyramidal tract in congenital hemiparesis: relationship between morphology and function in periventricular lesions. Neuropediatrics. 31:2000;257-264.
51. Sternberger L.A., Sternberger N.H. Monoclonal antibodies distinguish phosphorylated and non-phosphorylated forms of neurofilaments in situ. Proc. Natl. Acad. Sci. U.S.A. 80:1983;6126-6130.
52. Takashima S., Tanaka K. Development of cerebrovascular architecture and its relationship to periventricular leukomalacia. Arch. Neurol. 35:1978;11-16.
53. Terashima T. Anatomy, development and lesion-induced plasticity of rodent corticospinal tract. Neurosci. Res. 22:1995;139-161.
54. Thorburne S.K., Juurlink B.H. Low glutathione and high iron govern the susceptibility of oligodendroglial precursors to oxidative stress. J. Neurochem. 67:1996;1014-1022.
55. Trapp B.D., Peterson J., Ransohoff R.M., Rudick R., Mork S., Bo L. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 338:1998;278-285.
56. Vis J.C., de Boer-van Huizen R.T., Verbeek M.M., de Waal R.M.W., ten Donkelaar H.J., Kremer B. 3-Nitropropionic acid induces cell death and mitochondrial dysfunction in rat corticostriatal slices. Neurosci. Lett. 329:2002;86-90.
57. White E. Life, death and the pursuit of apoptosis. Genes Dev. 10:1996;1-15.