Close homologue of adhesion molecule L1 promotes survival of purkinje and granule cells and granule cell migration during murine cerebellar development

Journal of Comparative Neurology

Volumn 513, Issue 5, 2009, Pages 496-510

  Jakovcevski, Igor ^a,d   Siering, Janina ^a   Hargus, Gunnar ^a   Karl, Nicole ^a   Hoelters, Laura ^a   Djogo, Nevena ^a,b   Yin, Shengming ^a,c   Zecevic, Nada ^d   Schachner, Melitta ^a,c,e   Irintchev, Andrey ^a,f  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF BELGRADE   (Serbia)

^c DALIAN MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^e RUTGERS UNIVERSITY   (United States)

^f FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Cell migration; Cerebellar development; CHL1; Granule cells; Purkinje cells; Synaptic terminals

Indexed keywords

4 AMINOBUTYRIC ACID; CELL ADHESION MOLECULE; CLOSE HOMOLOGUE OF ADHESION MOLECULE L1; UNCLASSIFIED DRUG; CHL1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; CELL COUNT; CELL DENSITY; CELL LOSS; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CELL SIZE; CELL SURVIVAL; CEREBELLUM DEVELOPMENT; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; GOLGI COMPLEX; GRANULE CELL; IMMUNOHISTOCHEMISTRY; INTERNEURON; MICROGLIA; MOUSE; NERVE CELL; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PURKINJE CELL; STELLATE CELL; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CELL CULTURE; CELL DEATH; CELL DIFFERENTIATION; CELL MOTION; CEREBELLUM; CYTOLOGY; DENDRITE; FEMALE; GENETICS; GLIA; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; MALE; METABOLISM; METHODOLOGY; MOUSE MUTANT; NEWBORN; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PREGNANCY;

ANIMALS; ANIMALS, NEWBORN; CELL ADHESION MOLECULES; CELL COUNT; CELL DEATH; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; CEREBELLUM; DENDRITES; EMBRYO, MAMMALIAN; FEMALE; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROGLIA; NEURONS; POLYMERASE CHAIN REACTION; PREGNANCY; PURKINJE CELLS;

EID: 64549128165     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21981     Document Type: Article

References (51)

1. Angeloni D, Lindor NM, Pack S, Latif F, Wei MH, Lerman MI. 1999. CALL gene is haploinsufficient in a 3p-syndrome patient. Am J Med Genet 86:482-485.
2. Ango F, di Cristo G, Higashiyama H, Bennett V, Wu P, Huang ZJ. 2004. Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at Purkinje axon initial segment. Cell 119:257-272.
3. Ango F, Wu C, Van der Want JJ, Wu P, Schachner M, Huang ZJ. 2008. Bergmann glia and the recognition molecule CHL1 organize GABAergic axons and direct innervation of Purkinje cell dendrites. PLoS Biol 6:e103.
4. Boyden ES, Katoh A, Raymond JL. 2004. Cerebellum-dependent learning: the role of multiple plasticity mechanisms. Annu Rev Neurosci 27:581-609.
5. Buhusi M, Midkiff BR, Gates AM, Richter M, Schachner M, Maness PF. 2003. Close homolog of L1 is an enhancer of integrin-mediated cell migration. J Biol Chem 278:25024-25031.
6. Chaisuksunt V, Campbell G, Zhang Y, Schachner M, Lieberman AR, Anderson PN. 2000a. The cell recognition molecule CHL1 is strongly upregulated by injured and regenerating thalamic neurons. J Comp Neurol 425:382-392.
7. Chaisuksunt V, Zhang Y, Anderson PN, Campbell G, Vaudano E, Schachner M, Lieberman AR. 2000b. Axonal regeneration from CNS neurons in the cerebellum and brainstem of adult rats: correlation with the patterns of expression and distribution of messenger RNAs for L1, CHL1, c-jun and growth-associated protein-43. Neuroscience 100:87-108.
8. Chen QY, Chen Q, Feng GY, Lindpaintner K, Chen Y, Sun X, Chen Z, Gao Z, Tang J, He L. 2005. Case-control association study of the close homologue of L1 (CHL1) gene and schizophrenia in the Chinese population. Schizophr Res 73:269-274.
9. Chen S, Mantei N, Dong L, Schachner M. 1999. Prevention of neuronal cell death by neural adhesion molecules L1 and CHL1. J Neurobiol 38: 428-439.
10. Dahme M, Bartsch U, Martini R, Anliker B, Schachner M, Mantei N. 1997. Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat Genet 17:346-349.
11. Demyanenko GP, Schachner M, Anton E, Schmid R, Feng G, Sanes J, Maness PF. 2004. Close homolog of l1 modulates area-specific neuronal positioning and dendrite orientation in the cerebral cortex. Neuron 44:423-437.
12. Dijkhuizen T, van Essen T, van der Vlies P, Verheij JB, Sikkema-Raddatz B, van der Veen AY, Gerssen-Schoorl KB, Buys CH, Kok K. 2006. FISH and array-CGH analysis of a complex chromosome 3 aberration suggests that loss of CNTN4 and CRBN contributes to mental retardation in 3pter deletions. Am J Med Genet A 140:2482-2487.
13. Dusart I, Guenet JL, Sotelo C. 2006. Purkinje cell death: differences between developmental cell death and neurodegenerative death in mutant mice. Cerebellum 5:163-173.
14. Falk J, Bonnon C, Girault JA, Faivre-Sarrailh C. 2002. F3/contactin, a neuronal cell adhesion molecule implicated in axogenesis and myelination. Biol Cell 94:327-334.
15. Frints SG, Marynen P, Hartmann D, Fryns JP, Steyaert J, Schachner M, Rolf B, Craessaerts K, Snellinx A, Hollanders K, D'Hooge R, De Deyn PP, Froyen G. 2003. CALL interrupted in a patient with non-specific mental retardation: gene dosage-dependent alteration of murine brain development and behavior. Hum Mol Genet 12:1463-1474.
16. Higgins JJ, Rosen DR, Loveless JM, Clyman JC, Grau MJ. 2000. A gene for nonsyndromic mental retardation maps to chromosome 3p25-pter. Neurology 55:335-340.
17. Hillenbrand R, Molthagen M, Montag D, Schachner M. 1999. The close homologue of the neural adhesion molecule L1 (CHL1): patterns of expression and promotion of neurite outgrowth by heterophilic interactions. Eur J Neurosci 11:813-826.
18. Holm J, Hillenbrand R, Steuber V, Bartsch U, Moos M, Luebbert H, Montag D, Schachner M. 1996. Structural features of a close homologue of L1 (CHL1) in the mouse: a new member of the L1 family of neural recognition molecules. Eur J Neurosci 8:1613-1629.
19. Huang ZJ, Di Cristo G, Ango F. 2007. Development of GABA innervation in the cerebral and cerebellar cortices. Nat Rev Neurosci 8:673-686.
20. Irintchev A, Koch M, Needham LK, Maness P, Schachner M. 2004. Impairment of sensorimotor gating in mice deficient in the cell adhesion molecule L1 or its close homologue, CHL1. Brain Res 1029:131-134.
21. Irintchev A, Rollenhagen A, Troncoso E, Kiss JZ, Schachner M. 2005. Structural and functional aberrations in the cerebral cortex of tenascin-C deficient mice. Cereb Cortex 15:950-962.
22. Ito M. 2006. Cerebellar circuitry as a neuronal machine. Prog Neurobiol 78:272-303.
23. Jakovcevski I, Wu J, Karl N, Leshchyns'ka I, Sytnyk V, Chen J, Irintchev A, Schachner M. 2007. Glial scar expression of CHL1, the close homolog of the adhesion molecule L1, limits recovery after spinal cord injury. J Neurosci 27:7222-7233.
24. Jiao Y, Sun Z, Lee T, Fusco FR, Kimble TD, Meade CA, Cuthbertson S, Reiner A. 1999. A simple and sensitive antigen retrieval method for free-floating and slide-mounted tissue sections. J Neurosci Methods 93:149-162.
25. Kalus I, Schnegelsberg B, Seidah NG, Kleene R, Schachner M. 2003. The proprotein convertase PC5A and a metalloprotease are involved in the proteolytic processing of the neural adhesion molecule L1. J Biol Chem 278:10381-10388.
26. Kamiguchi H, Hlavin ML, Lemmon V. 1998a. Role of L1 in neural development: what the knockouts tell us. Mol Cell Neurosci 12:48-55.
27. Kamiguchi H, Hlavin ML, Yamasaki M, Lemmon V. 1998b. Adhesion molecules and inherited diseases of the human nervous system. Annu Rev Neurosci 21:97-125.
28. Lalonde R, Strazielle C. 2007. Spontaneous and induced mouse mutations with cerebellar dysfnuctions: behavior and neurochemistry. Brain Res 1140:51-74.
29. Leshchyns'ka I, Sytnyk V, Richter M, Andreyeva A, Puchkov D, Schachner M. 2006. The adhesion molecule CHL1 regulates uncoating of clathrincoated synaptic vesicles. Neuron 52:1011-1025.
30. Leto K, Carletti B, Williams IM, Magrassi L, Rossi F. 2006. Different types of cerebellar GABAergic interneurons originate from a common pool of multipotent progenitor cells. J Neurosci 26:11682-11694.
31. Lewis PM, Gritli-Linde A, Smeyne R, Kottman A, McMahon AP. 2004. Sonic hedgehog signaling is required for expansion of granule neuron precursors and patterning of the mouse cerebellum. Dev Biol 270:393-410.
32. Loers G, Chen S, Grumet M, Schachner M. 2005. Signal transduction pathways implicated in neural recognition molecule L1 triggered neuroprotection and neuritogenesis. J Neurochem 92:1463-1476.
33. Madalosso SH, Perez-Villegas EM, Armengol JA. 2005. Naturally occuring neuronal death during the postnatal development of Purkinje cells and their precerebellar afferent projections. Brain Res Rev 49:267-279.
34. Montag-Sallaz M, Schachner M, Montag D. 2002. Misguided axonal projections, neural cell adhesion molecule 180 mRNA upregulation, and altered behavior in mice deficient for the close homolog of L1. Mol Cell Biol 22:7967-7981.
35. Morellini F, Lepsveridze E, Kahler B, Dityatev A, Schachner M. 2007. Reduced reactivity to novelty, impaired social behavior, and enhanced basal synaptic excitatory activity in perforant path projections to the dentate gyrus in young adult mice deficient in the neural cell adhesion molecule CHL1. Mol Cell Neurosci 34:121-136.
36. Nikonenko AG, Sun M, Lepsveridze E, Apostolova I, Petrova I, Irintchev A, Dityatev A, Schachner M. 2006. Enhanced perisomatic inhibition and impaired long-term potentiation in the CA1 region of juvenile CHL1-deficient mice. Eur J Neurosci 23:1839-1852.
37. Rakic P, Sidman RL. 1973. Weaver mutant mouse cerebellum: defective neuronal migration secondary to abnormality of Bergmann glia. Proc Natl Acad Sci U S A 70:240-244.
38. Rolf B, Lang D, Hillenbrand R, Richter M, Schachner M, Bartsch U. 2003. Altered expression of CHL1 by glial cells in response to optic nerve injury and intravitreal application of fibroblast growth factor-2. J Neurosci Res 71:835-843.
39. Sakurai T, Lustig M, Babiarz J, Furley AJ, Tait S, Brophy PJ, Brown SA, Brown LY, Mason CA, Grumet M. 2001. Overlapping functions of the cell adhesion molecules Nr-CAM and L1 in cerebellar granule cell development. J Cell Biol 154:1259-1273.
40. Sakurai K, Migita O, Toru M, Arinami T. 2002. An association between a missense polymorphism in the close homologue of L1 (CHL1, CALL) gene and schizophrenia. Mol Psychiatry 7:412-415.
41. Simat M, Ambrosetti L, Lardi-Studler B, Fritschy JM. 2007. GABAergic synaptogenesis marks the onset of differentiation of basket and stellate cells in mouse cerebellum. Eur J Neurosci 26:2239-2256.
42. Singec I, Knoth R, Ditter M, Frotscher M, Volk B. 2003. Neurogranin expression by cerebellar neurons in rodents and non-human primates. J Comp Neurol 459:278-289.
43. Sotelo C. 2004. Cellular and genetic regulation of the development of the cerebellar system. Prog Neurobiol 72:295-339.
44. Stitt TN, Hatten ME. 1990. Antibodies that recognize astrotactin block granule neuron binding to astroglia. Neuron 5:639-649.
45. Vogel MW, Sunter K, Herrup K. 1989. Numerical matching between granule and Purkinje cells in lurcher chimeric mice: a hypothesis for the tropic rescue of granule cells from target-related cell death. J Neurosci 9:3454-3462.
46. Watanabe D, Inokawa H, Hashimoto K, Suzuki N, Kano M, Shigemoto R, Hirano T, Toyama K, Kaneko S, Yokoi M, Moriyoshi K, Suzuki M, Kobayashi K, Nagatsu T, Kreitman RJ, Pastan I, Nakanishi S. 1998. Ablation of cerebellar Golgi cells disrupts synaptic integration involving GABA inhibition and NMDA receptor activation in motor coordination. Cell 95:17-27.
47. Weiss GM, Pysh JJ. 1978. Evidence for loss of Purkinje cell dendrites during late development: a morphometric Golgi analysis in the mouse. Brain Res 154:219-230.
48. Weller S, Gaertner J. 2001. Genetic and clinical aspects of X-linked hydrocephalus (L1 disease): mutations in the L1CAM gene. Hum Mutat 18:1-12.
49. Wright AG, Demyanenko GP, Powell A, Schachner M, Enriquez-Barreto L, Tran TS, Polleux F, Maness PF. 2007. Close homolog of L1 and neuropilin 1 mediate guidance of thalamocortical axons at the ventral telencephalon. J Neurosci 27:13667-13679.
50. Yang Q, Hamberger A, Hyden H, Wang S, Stigbrand T, Haglid KG. 1995. S-100 beta has a neuronal localisation in the rat hindbrain revealed by an antigen retrieval method. Brain Res 696:49-61.
51. Zhang Y, Roslan R, Lang D, Schachner M, Lieberman AR, Anderson PN. 2000. Expression of CHL1 and L1 by neurons and glia following sciatic nerve and dorsal root injury. Mol Cell Neurosci 16:71-86.