Collapsin-1/semaphorin-III/D is regulated developmentally in Purkinje cells and collapses pontocerebellar mossy fiber neuronal growth cones

Journal of Neuroscience

Volumn 19, Issue 11, 1999, Pages 4437-4448

  Rabacchi, Sylvia A ^a,c   Solowska, Joanna M ^a   Kruk, Barbara ^a   Luo, Yuling ^b,d   Raper, Jonathan A ^b   Baird, Douglas H ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Columbia University ^*  (United States)

^d EXELIXIS INC   (United States)

Author keywords

Basilar pontine nuclei; Cerebellum; Climbing fiber; Collapsin; Mossy fiber; Purkinje cell; Semaphorin

Indexed keywords

SEMAPHORIN 3A;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL SPECIFICITY; CHICK EMBRYO; CLIMBING FIBER; CONTROLLED STUDY; EMBRYO; GROWTH CONE; IN SITU HYBRIDIZATION; IN VITRO STUDY; INFERIOR OLIVE; MICROSCOPY; MOSSY FIBER; MOUSE; NEWBORN; NONHUMAN; PONS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; SENSORY NERVE; TARGET CELL;

EID: 0033152334     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-11-04437.1999     Document Type: Article

References (69)

1. Adams RH, Betz H, Püschel AW (1996) A novel class of murine semaphorins with homology to thrombospondin is differentially expressed during early embryogenesis. Mech Dev 57:33-45.
2. Altman J (1972) Postnatal development of the cerebellar cortex in the rat. III. Maturation of the components of the granule layer. J Comp Neurol 145:465-514.
3. Altman J, Bayer SA (1987) Development of the precerebellar nuclei in the rat. IV. The anterior precerebellar extramural migratory stream and the nucleus reticularis tegmenti pontis and the basal pontine gray. J Comp Neurol 257:529-552.
4. Altman J, Bayer SA (1996) Development of the cerebellar system: in relation to its evolution, structure and functions. New York: CRC.
5. Azizi SA, Mihailoff GA, Burne RA, Woodward DJ (1981) The pontocerebellar system in the rat: an HRP study. I. Posterior vermis. J Comp Neurol 197:543-558.
6. Baird DH, Baptista CA, Wang L-C, Mason CA (1992a) Specificity of a target neuron-derived stop signal for afferent axonal growth. J Neurobiol 23:579-591.
7. Baird DH, Hatten ME, Mason CA (1992b) Cerebellar target neurons provide a stop signal for afferent neurite extension. J Neurosci 12:619-634.
8. Baird DH, Hatten ME, Heintz N, Mason CA (1994) Micro-methods for analyzing axon-target interactions in vitro. NeuroProtocols: Comp Methods Neurosci 4:106-115.
9. Baird DH, Trenkner E, Mason CA (1996) Arrest of afferent axon extension by target neurons in vitro is regulated by the NMDA receptor. J Neurosci 16:2642-2648.
10. Baird DH, Rabacchi SA, Solowska JM, Kruk B (1997) Regulation of pontocerebellar mossy fiber extension by BDNF and collapsin-1/semaphorin-III/D. Exp Neurol 151:151.
11. Baker GE, Reese BE (1993) Using confocal laser scanning microscopy to investigate the organization and development of neuronal projections labeled with Dil. Methods Cell Biol 38:325-344.
12. Baynard MD, Rabacchi SA, Carney C, Hoffman JR, Kruk B, Baird DH (1997) BDNF regulates cerebellar mossy fiber extension and fasciculation. Soc Neurosci Abstr 23:136.9.
13. Behar O, Golden JA, Mashimo H, Schoen FJ, Fishman MC (1996) Semaphorin III is needed for normal patterning of growth of nerves, bones, and heart. Nature 383:525-528.
14. Blanks RHI, Precht W, Torigoe Y (1983) Afferent projections to the cerebellar flocculus in the pigmented rat demonstrated by retrograde transport of horseradish peroxidase. Exp Brain Res 52:293-306.
15. Braissant O, Wahli W (1998) A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1:10-16.
16. Brodal P, Bjaalie JG (1992) Organization of the pontine nuclei. Neurosci Res 13:83-118.
17. Brodal P, Mihailoff G, Border B, Ottersen OP, Storm-Mathisen J (1988) GABA-containing neurons in the pontine nuclei of rat, cat and monkey. An immunocytochemical study. Neuroscience 25:27-45.
18. Burne RA, Eriksson MA, Saint-Cyr JA, Woodward DJ (1978) The organization of the pontine projection to lateral cerebellar areas in the rat: dual zones in the pons. Brain Res 139:340-347.
19. Catalano SM, Messersmith EK, Goodman CS, Shatz CJ, Chédotal A (1998) Many major CNS axon projections develop normally in the absence of semaphorin III. Mol Cell Neurosci 11:173-182.
20. Chédotal A, Pourquié O, Ezan F, San Clemente H, Sotelo C (1996) BEN as a presumptive target recognition molecule during the development of the olivocerebellar system. J Neurosci 16:3296-3310.
21. Chen H, Chédotal A, He Z, Goodman CS (1997) Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins E and sema IV but not sema III. Neuron 19:547-559.
22. Eisenman LM (1980) Pontocerebellar projections to the paraflocculus in the rat. Brain Res 188:550-554.
23. Eisenman LM (1981) Pontocerebellar projections to the pyramis and copula pyramidis in the rat: evidence for a mediolateral topography. J Comp Neurol 199:77-86.
24. Eisenman LM, Noback CR (1980) The ponto-cerebellar projection in the rat: differential projections to sublobules of the uvula. Exp Brain Res 38:11-17.
25. Giger RJ, Wolfer DP, de Wit GMJ, Verhaagen J (1996) Anatomy of rat semaphorin III/collapsin-1 mRNA expression and relationship to developing nerve tracts during embryogenesis. J Comp Neurol 3:378-392.
26. Goldman-Wohl D, Chan E, Baird D, Heintz N (1994) KV3.3b: a novel Shaw-type potassium channel expressed in terminally differentiated cerebellar Purkinje cells and deep cerebellar nuclei. J Neurosci 14:511-522.
27. Hámori J, Somogyi J (1983) Differentiation of cerebellar mossy fiber synapses in the rat: a quantitative electron microscope study. J Comp Neurol 220:365-377.
28. He Z, Tessier-Lavigne M (1997) Neuropilin is receptor for the axonal chemorepellent semaphorin III. Cell 90:739-751.
29. Inagaki S, Furuyama T, Iwahashi Y (1995) Identification of a member of mouse semaphorin family. FEBS Lett 370:269-272.
30. Kawakami A, Kitsukawa T, Takagi S, Fujisawa H (1996) Developmentally regulated expression of a cell surface protein, neuropilin, in the mouse nervous system. J Neurobiol 29:1-17.
31. Kitsukawa T, Shimizu M, Sanbo M, Hirata T, Taniguchi M, Bekku Y, Yagi T, Fujisawa H (1997) Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19:995-1005.
32. Kolodkin AL (1996) Semaphorins-mediators of repulsive growth cone guidance. Trends Cell Biol 6:15-22.
33. Kolodkin AL, Ginty DD (1997) Steering clear of semaphorins: neuropilins sound the retreat. Neuron 19:1159-1162.
34. Kolodkin AL, Matthes DJ, O'Connor TP, Patel NH, Bentley D, Goodman CS (1992) Fasciclin IV: sequence, expression and function during growth cone guidance in the grasshopper embryo. Neuron 9:831-845.
35. Kolodkin AL, Matthes DJ, Goodman CS (1993) The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75:1389-1399.
36. Kolodkin AL, Levengood DV, Rowe EG, Tai Y-T, Giger RJ, Ginty DD (1997) Neuropilin is a semaphorin III receptor. Cell 90:753-762.
37. Larramendi LMH (1969) Analysis of synaptogenesis in the cerebellum of the mouse. In: Proceedings of the first international symposium of the Institute for Biomedical Research. Neurobiology of cerebellar evolution and development (Llinás R, ed), pp 803-843. Chicago: American Medical Association.
38. Luo Y, Raible D, Raper JA (1993) Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75:217-227.
39. Luo Y, Shepherd I, Li J, Renzi MJ, Chang S, Raper JA (1995) A family of molecules related to collapsin in the embryonic chick nervous. Neuron 14:1131-1140.
40. Mason CA, Gregory E (1984) Postnatal maturation of cerebellar mossy and climbing fibers: transient expression of dual features on single axons. J Neurosci 4:1715-1735.
41. Mason CA, Morrison ME, Ward MS, Zhang Q, Baird DH (1997) Axon-target interactions in the developing cerebellum. Perspect Dev Neurobiol 5:69-82.
42. Matthes DJ, Sink HS, Kolodkin AL, Goodman CS (1995) Semaphorin II can function as a selective inhibitor of specific synaptic arborizations. Cell 81:631-639.
43. Messersmith EK, Leonardo ED, Shatz CJ, Tessier-Lavigne M, Goodman CS, Kolodkin AL (1995) Semaphorin III can function as a selective chemorepellent to pattern sensory projections in the spinal cord. Neuron 14:949-959.
44. Mihailoff GA (1993) Cerebellar nuclear projections from the basilar pontine nuclei and nucleus reticularis tegmenti pontis as demonstrated with PHA-L tracing in the rat. J Comp Neurol 330:130-146.
45. Mihailoff GA (1994) Identification of pontocerebellar axon collateral synaptic boutons in the rat cerebellar nuclei. Brain Res 648:313-318.
46. Mihailoff GA, Burne RA, Azizi SA, Norell G, Woodward DJ (1981) The pontocerebellar system in the rat: an HRP study. II. Hemispheral components. J Comp Neurol 197:559-577.
47. Nakamura F, Tanaka M, Takahashi T, Kalb RG, Strittmatter SM (1998) Neuropilin-1 extracellular domains mediate semaphorin-D/III-induced growth cone collapse. Neuron 21:1093-1100.
48. Nikundiwe AM, Bjaalie JG, Brodal P (1994) Lamellar organization of pontocerebellar neuronal populations. A multi-tracer and 3-D computer reconstruction study in the cat. Eur J Neurosci 6:173-186.
49. Palay SL, Chan-Palay V (1974) Cerebellar cortex: cytology and organization. New York: Springer.
50. Püschel AW, Adams RH, Betz H (1995) Murine semaphorin D/collapsin is a member of a diverse gene family and creates domains inhibitory for axonal extension. Neuron 14:941-948.
51. Raper JA, Kapfhammer JP (1990) The enrichment of a neuronal growth cone collapsing activity from embryonic chick brain. Neuron 4:21-29.
52. Ruigrok TJH, Cella F (1995) Precerebellar nuclei and red nucleus. In: The rat nervous system, 2nd Ed (Paxinos G, ed), pp 277-307. New York: Academic.
53. Shepherd I, Luo Y, Raper JA, Chang S (1996) The distribution of collapsin-1 mRNA in the developing chick nervous system. Dev Biol 173:185-199.
54. Shepherd IT, Luo Y, Lefcort F, Reichardt LF, Raper JA (1997) A sensory axon repellent secreted from ventral spinal cord explants is neutralized by antibodies raised against collapsin-1. Development 124:1377-1385.
55. Shinoda Y, Sugiuchi Y, Futami T, Izawa R (1992) Axon collaterals of mossy fibers from the pontine nucleus in the cerebellar dentate nucleus. J Neurophysiol 67:547-560.
56. Song H-j, Ming G-I, He Z, Lehmann M, McKerracher L, Tessier-Lavigne M, Poo M-m (1998) Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281:1515-1518.
57. Sotelo C, Wassef M (1991) Cerebellar development: afferent organization and Purkinje cell heterogeneity. Philos Trans R Soc Lond [Biol] 331:307-313.
58. Takahashi T, Nakamura F, Jin Z, Kalb RG, Strittmatter SM (1998) Semaphorins A and E act as antagonists of neuropilin-1 receptors and agonists of neuropilin-2 receptors. Nat Neurosci 1:487-493.
59. Taniguchi M, Yuasa S, Fujisawa H, Naruse I, Saga S, Mishina M, Yagi T (1997) Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron 19:519-530.
60. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123-1133.
61. Varela-Echavarria A, Tucker A, Püschel AW, Guthrie S (1997) Motor axon subpopulations respond differentially to the chemorepellents netrin-1 and semaphorin-D. Neuron 18:193-207.
62. Voogd J, Glickstein M (1998) The anatomy of the cerebellum. Trends Neurosci 21:370-375.
63. Wassef M, Chédotal A, Cholley B, Thomasset M, Heizmann CW, Sotelo C (1992) Development of the olivocerebellar projection in the rat. I. Transient biochemical compartmentation of the inferior olive. J Comp Neurol 323:519-536.
64. Wong JTW, Yu WTC, O'Connor TP (1997) Transmembrane grasshopper semaphorin I promotes axon outgrowth in vivo. Development 124: 3597-3609.
65. Wright DE, White FA, Gerfen RW, Silos-Santiago I, Snider WD (1995) The guidance molecule semaphorin III is expressed in regions of spinal cord and periphery avoided by growing sensory axons. J Comp Neurol 361:321-333.
66. Xu X, Ng S, Wu Z-L, Nguyen D, Homburger S, Seidel-Dugan C, Ebens A, Luo Y (1998) Human semaphorin K1 is glycosylphosphatidylinositol-linked and defines a new subfamily of viral-related semaphorins. J Biol Chem 273:22428-22434.
67. Yee KT, Simon HH, O'Leary DDM (1995) Chemorepulsive activity from the cerebellum inhibits neurite outgrowth from the basilar pons. Soc Neurosci Abstr 21:292.
68. Yu HH, Araj HH, Ralls SA, Kolodkin AL (1998) The transmembrane semaphorin sema I is required in Drosophila for embryonic motor and CNS axon guidance. Neuron 2:207-220.
69. Zhou L, White FA, Lentz SI, Wright DE, Fisher DA, Snider WD (1997) Cloning and expression of a novel murine semaphorin with structural similarity to insect semaphorin I. Mol Cell Neurosci 9:26-41.