Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching

Cell

Volumn 96, Issue 6, 1999, Pages 771-784

  Kuan, Hong Wang ^a   Brose, Katja ^a   Arnott, David ^c   Kidd, Thomas ^b   Goodman, Corey S ^b   Henzel, William ^c   Tessier Lavigne, Marc ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; REGULATOR PROTEIN;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CATTLE; EMBRYO; MAMMAL; NERVE FIBER GROWTH; NERVE SPROUTING; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; SENSORY NERVE; SPINAL CORD;

EID: 0033582915     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/s0092-8674(00)80588-7     Document Type: Article

References (45)

1. Altman, J., and Bayer, S.A. (1984). The development of the rat spinal cord. Adv. Anat. Embryol. Cell Biol. 85, 1-164.
2. Arnott, D., Henzel, W.J., and Stults, J.T. (1998a). Rapid identification of comigrating gel-isolated proteins by ion trap-mass spectrometry. Electrophoresis 19, 968-980.
3. Arnott, D., O'Connell, K.L., King, K.L., and Stults, J.T. (1998b). An integrated approach to proteome analysis: Identification of proteins associated with cardiac hypertrophy. Anal. Biochem. 258, 1-18.
4. Brose, K., Bland, K.S., Wang, K.H., Arnott, D., Henzel, W., Goodman, C.S., Tessier-Lavigne, M., and Kidd, T. (1999). Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96, this issue, 795-806.
5. Campenot, R.B. (1982). Development of sympathetic neurons in compartmentalized cultures. II Local control of neurite growth by nerve growth factor. Dev. Biol. 93, 1-12.
6. Castellani, V., Yue, Y., Gao, P.P., Zhou, R., and Bolz, J. (1998). Dual action of a ligand for Eph receptor tyrosine kinases on specific populations of axons during the development of cortical circuits. J. Neurosci. 18, 4663-4672.
7. Cohen-Cory, S., and Fraser, S.E. (1995). Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378, 192-196.
8. Diamond, J., Holmes, M., and Coughlin, M. (1992). Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat. J. Neurosci. 12, 1454-1466.
9. Flanagan, J.G., and Vanderhaeghen, P. (1998). The ephrins and Eph receptors in neural development. Annu. Rev. Neurosci. 21, 309-345.
10. Gallo, G., and Letourneau, P.C. (1998). Localized sources of neurotrophins initiate axon collateral sprouting. J. Neurosci. 18, 5403-5414.
11. Harris, W.A., Holt, C.E., Smith, T.A., and Gallenson, N. (1985). Growth cones of developing retinal cells in vivo, on culture surfaces, and incollagen matrices. J. Neurosci. Res. 13, 101-122.
12. Heffner, C.D, Lumsden A.G., and O'Leary, D.D. (1990). Target control of collateral extension and directional axon growth in the mammalian brain. Science 247, 217-220.
13. Henzel, W.J., and Stults, J.T. (1995). Reversed phase isolation of peptides. In Current Protocols in Protein Science, Vol. 1, J.E. Coligan et al., eds. (New York: John Wiley & Sons), pp. 1161-11614.
14. Henzel, W.J., Rodriguez, H., and Watanabe, C. (1987). Computer analysis of automated Edman degradation and amino acid analysis data. J. Chromatogr. 404, 41-52.
15. Henzel, W.J., Billeci, T.M., Stults, J.T., Wong, S.C., Grimley, C., and Watanabe, C. (1993). Identifying proteins from two-dimensional gels by molecular mass searching of peptide fragments in protein sequence databases. Proc. Natl. Acad. Sci. USA 90, 5011-5015.
16. Holmes, G.P., Negus, K., Burridge, L., Raman, S., Algar, E., Yamada, T., and Little, M.H. (1998). Distinct but overlapping expression patterns of two vertebrate slit homologs implies functional roles in CNS development and organogenesis. Mech. Dev. 79, 57-72.
17. Hory-Lee, F., Russell, M., Lindsay, R.M., and Frank, E. (1993). Neurotrophin 3 supports the survival of developing muscle sensory neurons in culture. Proc. Natl. Acad. Sci. USA 90, 2613-2617.
18. Itoh, A., Miyabayashi, T., Ohno, M., and Sakano, S. (1998). Cloning and expressions of three mammalian homologues of Drosophila slit suggest possible roles for slit in the formation and maintenance of the nervous system. Mol. Brain Res. 62, 175-186.
19. Kennedy, T.E., and Tessier-Lavigne, M. (1995). Guidance and induction of branch formation in developing axons by target-derived diffusible factors. Curr. Opin. Neurobiol. 5, 83-90.
20. Kidd, T., Bland, K.S., and Goodman, C.S. (1999). Slit is the midline repellent for the Robo receptor in Drosophila. Cell 96, this issue, 785-794.
21. Krutzsch, H.C., and Inman, J.K. (1993). N-isopropyliodoacetamide in the reduction and alkylation of proteins: Use in microsequence analysis. Anal. Biochem. 209, 109-116.
22. Lentz, S.I., Knudson, C.M., Korsemeyer, S.J., and Snider, W.D. (1999). Neurotrophins support the development of diverse sensory axon morphologies. J. Neurosci. 79, 1038-1048.
23. Levi-Montalcini, R. (1964). The nerve growth factor. Ann. N Y Acad. Sci. 118, 149-168.
24. Li, H.-s., Chen, J.-H., Wu, W., Fagaly, T., Zhou, L., Yuan, W., Dupuis, S., Jiang, Z.-H., Nash, W., Gick, C., Et Al. (1999). Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 96, this issue, 807-818.
25. Lui, M., Tempst, P., and Erdjmuent-Bromage, H. (1996). Methodical analysis of protein-nitrocellulose interactions to design a refined digestion protocol. Anal. Biochem. 241, 156-166.
26. Maina, F., Hilton, M.C., Andres, R., Wyatt, S., Klein, R., and Davies, A.M. (1998). Multiple roles for hepatocyte growth factor in sympathetic neuron development. Neuron 20, 835-846.
27. Messersmith, E.K., Leonardo, E.D., Shatz, C., Tessier-Lavigne, M., Goodman, C.S., and Kolodkin, A.L. (1995). Semaphorin III can function as a selective chemorepellent to pattern sensory projections into the spinal cord. Neuron 14, 949-959.
28. Nakayama, M., Nakajima, D., Nagase, T., Nomura, N., Seki, N., and Ohara, O. (1998). Identification of high-molecular-weight proteins with multiple EGF-like motifs by motif-trap screening. Genomics 51, 27-34.
29. Oakley, R.A., Garner, A.S., Large, T.H., and Frank, E. (1995). Muscle sensory neurons require neurotrophin-3 from peripheral tissues during the period of normal cell death. Development 121, 1341-1350.
30. O'Leary, D.D. (1992). Development of connectional diversity and specificity in the mammalian brain by the pruning of collateral projections. Curr. Opin. Neurobiol. 2, 70-77.
31. O'Leary, D.D., Bicknese, A.R., De Carlos, J.A., Heffner, C.D., Koester, S.E., Kutka, L.J., and Terashima, T. (1990). Target selection by cortical axons: Alternative mechanisms to establish axonal connections in the developing brain. Cold Spring Harbor Symp. Quant. Biol. 55, 453-468.
32. Ozaki, S., and Snider, W.D. (1997). Initial trajectories of sensory axons toward laminar targets in the developing mouse spinal cord. J. Comp. Neurol. 380, 215-229.
33. Rothberg, J.M., Hartley, D.A., Walther, Z., and Artavanis-Tsakonas, S. (1988). Slit: An EGF-homologous locus of D. melanogaster involved in the development of the embryonic central nervous system. Cell 55, 1047-1059.
34. Rothberg, J.M., Jacobs, J.R., Goodman, C.S., and Artavanis-Tsakonas, S. (1990). Slit: An extracellular protein necessary for development of midline glia and commissural axon pathways contains both EGF and LRR domains. Genes Dev. 4, 2169-2187.
35. Sato, M., Lopez-Mascaraque, L., Heffner, C.D., and O'Leary, D.D. (1994). Action of a diffusible target-derived chemoattractant on cortical axon branch induction and directed growth. Neuron 13, 791-803.
36. Scott, S.A., and Davies, A.M. (1993). Age-related effects of nerve growth factor on the morphology of embryonic sensory neurons in vitro. J. Comp. Neurol. 337, 277-285.
37. Serafini, T., Kennedy, T.E., Galko, M.J., Mirzayan, C., Jessell, T.M., and Tessier-Lavigne, M. (1994). The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424.
38. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996). Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal. Chem. 68, 850-858.
39. Snider, W.D. (1994). Functions of the neurotrophins during nervous system development: What the knockouts are teaching us. Cell 77, 627-638.
40. Tessier-Lavigne, M., and Goodman, C.S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
41. White, F.A., Keller-Peck, C.R., Knudson, C.M., Korsmeyer, S.J., and Snider, W.D. (1998). Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J. Neurosci. 18, 1428-1439.
42. Winslow, J.W., Moran, P., Valverde, J., Shih, A., Yuan, J.Q., Wong, S.C., Tsai, S.P., Goddard, A., Henzel, W.J., Hefti, F., et al. (1995). Cloning of AL-1, a ligand for an Eph-related tyrosine kinase receptor involved in axon bundle formation. Neuron 14, 973-981.
43. Yang, X.M., Toma, J.G., Bamji, S.X., Belliveau, D.J., Kohn, J., Park, M., and Miller, F.D. (1998). Autocrine hepatocyte growth factor provides a local mechanism for promoting axonal growth. J. Neurosci. 18, 8369-8381.
44. Yu, W., Ahmad, F.J., and Baas, P.W. (1994). Microtubule fragmentation and partitioning in the axon during collateral branch formation. J. Neurosci. 14, 5872-5884.
45. Zhang, L., Schmidt, R.E., Yan, Q., and Snider, W.D. (1994). NGF and NT-3 have differing effects on the growth of dorsal root axons in developing mammalian spinal cord. J. Neurosci. 14, 5187-5201.