Abnormal cerebellar histogenesis in PEX2 Zellweger mice reflects multiple neuronal defects induced by peroxisome deficiency

Journal of Comparative Neurology

Volumn 461, Issue 3, 2003, Pages 394-413

  Faust, Phyllis L ^a  

^a Columbia University ^*  (United States)

Author keywords

Apoptosis; Biogenesis disorder; Climbing fibers; Granule cell migration; Lipids; Malnutrition; Purkinje cell

Indexed keywords

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CEREBELLUM; CLIMBING FIBER; CONTROLLED STUDY; DENDRITIC CELL; GOLGI COMPLEX; GROWTH RETARDATION; HISTOGENESIS; IMMUNOHISTOCHEMISTRY; MALNUTRITION; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NEWBORN; NONHUMAN; PEROXISOME; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PURKINJE CELL; SURVIVAL RATE; ZELLWEGER SYNDROME;

AGING; ANIMALS; ANIMALS, NEWBORN; AXONS; CELL DEATH; CELL DIFFERENTIATION; CELL DIVISION; CELL MOVEMENT; CEREBELLUM; CHOLESTEROL 7-ALPHA-HYDROXYLASE; DENDRITES; GROWTH DISORDERS; IMMUNOHISTOCHEMISTRY; MALABSORPTION SYNDROMES; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; NERVE FIBERS; NEURONS; OLIVARY NUCLEUS; PEROXISOMES; PURKINJE CELLS; TIME FACTORS; ZELLWEGER SYNDROME;

EID: 0038779399     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10699     Document Type: Article

References (77)

1. Adams NC, Tomoda T, Cooper M, Dietz, Hatten ME. 2002. Mice that lack astrotactin have slowed neuronal migration. Development 129:965-972.
2. Altman J. 1972. Postnatal development of the cerebellar cortex in the rat. J Comp Neurol 145:353-398.
3. Altman J, Bayer S. 1985. Embryonic development of the rat cerebellum: deliniation of the cerebellar primordium and early cell movements. J Comp Neurol 231:1-26.
4. Altman J, Bayer SA. 1997. Development of the cerebellar system. New York: CRC Press.
5. Angaut P, Alvarado-Mallart RM, Sotelo C. 1982. Ultrastructural evidence for compensatory sprouting of climbing and mossy afferents to the cerebellar hemisphere after ipsilateral pedunculotomy in the newborn rat. J Comp Neurol 205:101-111.
6. Arnold G, Holtzman E. 1978. Microperoxisomes in the central nervous system of the postnatal rat. Brain Res. 155:1-17.
7. Aruga J, Minowa O, Yaginuma H, Kuno J, Nagai T, Nodo T, Mikoshiba K. 1998. Mouse Zic1 is involved in cerebellar development. J Neurosci 18:284-293.
8. Baes M, Gressens P, Baumgart E, Carmeliet P, Casteels M, Fransen M, Evrard P, Fahimi D, Declercq PE, Collen D, van Veldhoven PP, Mannaerts GP. 1997. A mouse model for Zellweger syndrome. Nat Genet 17:49-57.
9. Baptista CA, Hatten ME, Blazeski R, Mason CA. 1994. Cell-cell interactions influence survival and differentiation of purified Purkinje cells in vitro. Neuron 12:1-20.
10. Baürle J, Grüsser-Cornehls U. 1994. Axonal torpedoes in cerebellar Purkinje cells of two normal mouse strains during aging. Acta Neuropathol 88:237-245.
11. Borghesani PR, Peyrin JM, Klein R, Rubin J, Carter AR, Schwartz PM, Luster A, Corfas G, Segal RA. 2002. BDNF stimulates migration of cerebellar granule neurons. Development 129:1435-1442.
12. Bradke F, Dotti CG. 1997. Neuronal polarity: vectorial cytoplasmic flow precedes axon formation. Neuron 19:1175-1186.
13. Brochu G, Maler L, Hawkes R. 1990. Zebrin II: a polypeptide antigen expressed selectively by Purkinje cells reveals compartments in rat and fish cerebellum. J Comp Neurol 291:538-552.
14. Caddy KWT, Sidman RL. 1981. Purkinje cells and granule cells in the cerebellum of the stumbler mutant mouse. Dev Brain Res 1:221-226.
15. Carlberg M, Dricu A, Blegen H, Wang M, Hjertman M, Zickert P, Hoog A, Larsson O. 1996. Mevalonic acid is limiting for N-linked glycosylation and translocation of the insulin-like growth factor-1 receptor to the cell surface. Evidence for a new link between 3-hydroxy-3-methylglutaryl-coenzyme a reductase and cell growth. J Biol Chem 271:17453-17462.
16. Chen S, Hillman DE. 1980. Giant spines and enlarged synapses induced in Purkinje cells by malnutrition. Brain Res 187:487-493.
17. Edmondson JC, Hatten ME. 1987. Glial-guided granule neuron migration in vitro: a high-resolution time-lapse video microscopic study. J Neurosci 7:1928-1934.
18. Evrard P, Caviness VS, Prats-Vinas J, Lyon G. 1978. The mechanism of arrest ofneuronal migration in the Zellweger malformation: an hypothesis bases on cytoarchitectonic analysis. Acta Neuropathol (Berl) 41:109-117.
19. Faust PL, Hatten ME. 1997. Targeted deletion of the PEX2 peroxisome assembly gene in mice provides a model for Zellweger syndrome, a human neuronal migration disorder. J Cell Biol 139:1293-1305.
20. Faust PL, Su-H-M, Moser A, Moser HW. 2001. The peroxisome deficient PEX2 Zellweger mouse: pathologic and biochemical correlates of lipid dysfunction. J Mol Neurosci 16:289-297.
21. Fujiki Y. 2000. Peroxisome biogenesis and peroxisome biogenesis disorders. FEBS Lett 476:42-46.
22. Fujita S. 1967. Quantitative analysis of cell proliferation and differentiation in the cortex of the postnatal mouse cerebellum. J Cell Biol 32:277-287.
23. Furley AJ, Morton S, Manalo D, Karagogeos D, Dodd J, Jessel T. 1990. The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell 61:157-170.
24. Goldstein JL, Brown MS. 1990. Regulation of the mevalonate pathway. Nature 343:425-430.
25. Gould SJ, Valle D. 2000. Peroxisome biogenesis disorders: genetics and cell biology. Trends Genet 16:340-345.
26. Gould SJ, Raymond GV, Valle D. 2001. The peroxisome biogenesis disorders. In: Scriver CR, Beaudet AL, Sly WS, Valle D, editors. The metabolic and molecular bases of inherited disease. New York: McGraw Hill. p 3181-3217.
27. Gressens P, Baes M, Lerous P, Lombert A, Van Veldhoven P, Janssen A, Vamecq J, Marret S, Evrard P. 2000. Neuronal migration disorder in Zellweger syndrome is secondary to glutamate receptor dysfunction. Ann Neurol 48:336-343.
28. Guastavino J-M, Sotelo C, Damez-Kinselle I. 1990. Hot-foot murine mutation: behavioral effects and neuroanatomical alterations. Brain Res 523:199-210.
29. Guenet JL, Sotelo C, Mariani J. 1983. Hyperspiny Purkinje cell, a new neurological mutation in the mouse. J Hered 74:105-108.
30. Hawkes R, Herrup K. 1996. Aldolase C/zebrin II and the regionalization of the cerebellum. J Mol Neurobiol 6:147-158.
31. Heckroth JA, Goldowitz D, Eisenman LM. 1990. Olivocerebellar fiber maturation in normal and lurcher mutant mice: defective development in Lurcher. J Comp Neurol 291:415-430.
32. Hatten M, Heintz N. 1995. Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 18:385-408.
33. Hatten ME, Mason CA. 1990. Mechanisms of glial-guided neuronal migration in vitro and in vivo. Experientia 46:907-916.
34. Heintz N, Norman DJ, Gao W-Q, Hatten ME. 1993. Neurogenetic approaches to mammalian brain development. In: Genome analysis. 6:19-44. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
35. Hendelman WJ, Aggerwal AS. 1980. The Purkinje neuron. I. A Golgi study of its development in mouse and in culture. J Comp Neurol 193:1063-1079.
36. Hengartner MO. 2000. The biochemistry of apoptosis. Nature 407:770-776.
37. Herrup K, Kuemerle B. 1997. The compartmentalization of the cerebellum. Annu Rev Neurosci 20:61-90.
38. Hillman DE, Chen S. 1981. Vulnerability of cerebellar development in malnutrition-I. Quantitation of layer volume and neuron numbers. Neuroscience 6:1249-1262.
39. Ingham PW. 2001. Hedgehog signaling: A tale of two lipids. Science 294:1879-1881.
40. Inouye M, Oda S-I. 1980. Strain-specific variations in the folial pattern of mouse cerebellum. J Comp Neurol 190:357-362.
41. Ishibashi S, Schwarz M, Frykman PK, Herz J, Russell DW. 1996. Disruption of cholesterol 7α-hydroxylase gene in mice. I. Postnatal lethality reversed by bile acid and vitamin supplementation. J Biol Chem 271:18017-18023.
42. Ito M. 1984. Purkinje cells: abnormal morphology. In: The cerebellum and neural control. New York: Raven Press. p 40-50.
43. 1 receptor mRNA in the mouse cerebellum. In: de Zeeuw CI, Strata P, Voogd J, editors. The cerebellum: from stucture to control, progress in brain research. BV: Elsevier Science. 114:55-66.
44. Komuro H, Rakic, P. 1993. Modulation of neuronal migration by NMDA receptors. Science 260:95-97.
45. 2+ fluctuations. J Neurobiol 37:110-130.
46. Kumar SG, Feng L, Vidan S, Ross ME, Hatten ME, Heintz, N. 1993. Changing patterns of gene expression define four stages of cerebellar granule neuron differentiation. Development 117:97-104.
47. Lewis PD, Balazs R, Patel AJ, Johnson AL. 1975. The effect of undernutrition in early life on cell generation in the rat brain. Brain Res 83:235-247.
48. Mares V, Lodin Z. 1970. The cellular kinetics of the developing mouse cerebellum II. The function of the external granular layer in the process of foliation. Brain Res 23:343-352.
49. McConnell P, Berry M. 1978. The effects of undernutrition on Purkinje cell dendritic growth in the rat. J Comp Neurol 177:159-172.
50. McConnell P, Berry M. 1981. The effects of refeeding after varying periods of neonatal undernutrition on the morphology of Purkinje cells in the cerebellum of the rat. J Comp Neurol 200:463-479.
51. McKenna O, Arnold G, Holtzman E. 1976. Microperoxisome distribution in the central nervous system of the rat. Brain Res 117:181-194.
52. Miller MW, Nowakowski RS. 1988. Use of bromodeoxyuridineimmunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res 457:44-52.
53. Millhouse OE. 1981. The Golgi method. In: Heimer L, Robards MJ, editors. Neuroanatomical tract-tracing methods. New York: Plenum Press. p 311-344.
54. Opitz JM, ZuRhein GM, Vitale L, Shahidi NT, Howe JJ, Chou SM, Shanklin DR, Sybers HD, Dood AR, Gerritsen T. 1969. The Zellweger syndrome (cerebro-hepato-renal syndrome). Birth Defects 5:144-158.
55. Ozol K, Hayden JM, Oberdick J, Hawkes R. 1999. Transverse zones in the vermis of the mouse cerebellum. J Comp Neurol 412:95-111.
56. Purpura DP. 1975. Dendritic differentiation in human cerebral cortex: Normal and aberrant developmental patterns. In: Kreutzberg GW, editor: Advances in neurology, vol. 12. New York: Raven Press. p 91-116.
57. Pysh JJ, Perkins RE, Singer Beck L. 1979. The effect of postnatal undernutrition on the development of the mouse Purkinje cell dendritic trees. Brain Res 163:165-170.
58. Rakic P. 1971. Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electron microscopic study in Macacus rhesus. J Comp Neurol 141:283-312.
59. Ramon y Cajal S. 1911. Histologie du systeme nerveux de l'homme et des vertebres. Maloine, Paris. (Reprinted by Consejo Superior de Investigaciones Cientificas, Madrid, 1955.)
60. Ramon y Cajal S. 1960. Studies on vertebrate neurogenesis. [Translator, L. Guth]. Springfield, IL: Charles C. Thomas.
61. Ross ME, Walsh CA. 2001. Human brain malformations and their lessons for neuronal migration. Annu Rev Neurosci 24:1041-1070.
62. Rossi F, Jankovski A, Sotelo C. 1995. Target neuron controls the integrity of afferent axon phenotype: a study on the Purkinje cell-climbing fiber system in cerebellar mutant mice. J Neurosci 15:2040-2056
63. Salem N Jr, Litman B, Kim HY, Gawrisch K. 2001. Mechanisms of action of docosahexaenoic acid in the nervous system. Lipids 36:945-959.
64. Sindelar PJ, Guan Z, Dallner G, Ernster L. 1999. The protective role of plasmalogens in iron-induced lipid peroxidation. Free Radic Biol Med 26:318-324.
65. Sotelo C. 1990a. Axonal abnormalities in cerebellar Purkinje cells of the 'hyperspiny Purkinje cell' mutant mouse. J Neurocytol 19:737-755.
66. Sotelo C. 1990b. Cerebellar synaptogenesis: what we can learn from mutant mice. J Exp Biol 153:225-249.
67. Sotelo C, Arsenio-Nunes ML. 1976. Development of Purkinje cells in absence of climbing fibers. Brain Res 111:389-395.
68. Tano D, Napieralski JA, Eisenman LM, Messer A, Plummer J, Hawkes R. 1992. Novel developmental boundary in the cerebellum revealed by Zebrin expression in the Lurcher (Lc/+) mutant mouse. J Comp Neurol 323:128-136.
69. Urbanek P, Wang Z, Fetka, I, Wagner E, Busslinger M. 1994. Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell 79:901-912.
70. Vitiello F, Gombos G. 1987. Cerebellar development and nutrition. In: Rassin DK, Haber B, Drujan B, editors. Current topics in nutrition and disease. New York: Alan R. Liss. p 99-130.
71. Volpe JJ, Adams RD. 1972. Cerebro-hepato-renal syndrome of Zellweger: an inherited disorder of neuronal migration. Acta Neuropathol (Berl) 20:175-198.
72. Wahlsten D, Andison M. 1991. Patterns of cerebellar foliation in recombinant mice. Brain Res 557:184-189.
73. Wanders RJA, Tager JM. 1998. Lipid metabolism in peroxisomes in relation to human disease. Mol Aspects Med 19:69.
74. Wechsler-Reya RJ, Scott MP. 1999. Control of neuronal precursor proliferation in the cerebellum by sonic hedgehog, Neuron 22:103-114.
75. Whiteside G, Cougnon N, Hunt SP, Munglani R. 1998. An improved method for detection of apoptosis in tissue sections and cell culture, using the TUNEL technique combined with Hoechst stain. Brain Res Brain Res Protoc 2:160-164.
76. Yamano M, Tohyama M. 1994. Distribution of corticotropin-releasing factor and calcitonin gene-related peptide in the developing mouse cerebellum. Neurosci Res 19:387-396.
77. Yavin E, Brand A, Green P. 2002. Docosahexaenoic acid abundance in the brain: a biodevice to combat oxidative stress. Nutr Neurosci 5:149-157.