Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading

doi:10.1083/jcb.106.4.1281

This Article

	Full Text (PDF, 2409K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Caroni, P.
	Articles by Schwab, M. E.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Caroni, P.
	Articles by Schwab, M. E.

Social Bookmarking

	What's this?

ARTICLES

Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading

P Caroni and ME Schwab
Brain Research Institute, University of Zurich, Switzerland.

Lack of neurite growth in optic nerve explants in vitro has been suggested to be due to nonpermissive substrate properties of higher vertebrate central nervous system (CNS) white matter. We have searched for surface components in CNS white matter, which would prevent neurite growth. CNS, but not peripheral nervous system (PNS) myelin fractions from rat and chick were highly nonpermissive substrates in vitro. We have used an in vitro spreading assay with 3T3 cells to quantify substrate qualities of membrane fractions and of isolated membrane proteins reconstituted in artificial lipid vesicles. CNS myelin nonpermissiveness was abolished by treatment with proteases and was not associated with myelin lipid. Nonpermissive proteins were found to be membrane bound and yielded highly nonpermissive substrates upon reconstitution into liposomes. Size fractionation of myelin protein by SDS-PAGE revealed two highly nonpermissive minor protein fractions of Mr 35 and 250-kD. Removal of 35- and of 250-kD protein fractions yielded a CNS myelin protein fraction with permissive substrate properties. Supplementation of permissive membrane protein fractions (PNS, liver) with low amounts of 35- or of 250-kD CNS myelin protein was sufficient to generate highly nonpermissive substrates. Inhibitory 35- and 250-kD proteins were found to be enriched in CNS white matter and were found in optic nerve cell cultures which contained highly nonpermissive, differentiated oligodendrocytes. The data presented demonstrate the existence of membrane proteins with potent nonpermissive substrate properties. Distribution and properties suggest that these proteins might play a crucial inhibitory role during development and regeneration in CNS white matter.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Lee, J. K., Chan, A. F., Luu, S. M., Zhu, Y., Ho, C., Tessier-Lavigne, M., Zheng, B. (2009). Reassessment of Corticospinal Tract Regeneration in Nogo-Deficient Mice. J. Neurosci. 29: 8649-8654 [Abstract] [Full Text]
Kim, H.-J., Jung, C.-G., Jensen, M. A., Dukala, D., Soliven, B. (2008). Targeting of Myelin Protein Zero in a Spontaneous Autoimmune Polyneuropathy. J. Immunol. 181: 8753-8760 [Abstract] [Full Text]
Pernet, V., Joly, S., Christ, F., Dimou, L., Schwab, M. E. (2008). Nogo-A and Myelin-Associated Glycoprotein Differently Regulate Oligodendrocyte Maturation and Myelin Formation. J. Neurosci. 28: 7435-7444 [Abstract] [Full Text]
Cameron, J. S., Alexopoulou, L., Sloane, J. A., DiBernardo, A. B., Ma, Y., Kosaras, B., Flavell, R., Strittmatter, S. M., Volpe, J., Sidman, R., Vartanian, T. (2007). Toll-Like Receptor 3 Is a Potent Negative Regulator of Axonal Growth in Mammals. J. Neurosci. 27: 13033-13041 [Abstract] [Full Text]
El Maarouf, A., Petridis, A. K., Rutishauser, U. (2006). Use of polysialic acid in repair of the central nervous system. Proc. Natl. Acad. Sci. USA 103: 16989-16994 [Abstract] [Full Text]
Liu, B. P, Cafferty, W. B.J, Budel, S. O, Strittmatter, S. M (2006). Extracellular regulators of axonal growth in the adult central nervous system. Phil Trans R Soc B 361: 1593-1610 [Abstract] [Full Text]
Maier, I. C, Schwab, M. E (2006). Sprouting, regeneration and circuit formation in the injured spinal cord: factors and activity. Phil Trans R Soc B 361: 1611-1634 [Abstract] [Full Text]
Dimou, L., Schnell, L., Montani, L., Duncan, C., Simonen, M., Schneider, R., Liebscher, T., Gullo, M., Schwab, M. E. (2006). Nogo-A-Deficient Mice Reveal Strain-Dependent Differences in Axonal Regeneration. J. Neurosci. 26: 5591-5603 [Abstract] [Full Text]
Papadopoulos, C. M., Tsai, S.-Y., Cheatwood, J. L., Bollnow, M. R., Kolb, B. E., Schwab, M. E., Kartje, G. L. (2006). Dendritic Plasticity in the Adult Rat Following Middle Cerebral Artery Occlusion and Nogo-A Neutralization. Cereb Cortex 16: 529-536 [Abstract] [Full Text]
Neumann, S., Skinner, K., Basbaum, A. I. (2005). Sustaining intrinsic growth capacity of adult neurons promotes spinal cord regeneration. Proc. Natl. Acad. Sci. USA 102: 16848-16852 [Abstract] [Full Text]
Williams, G., Williams, E.-J., Maison, P., Pangalos, M. N., Walsh, F. S., Doherty, P. (2005). Overcoming the Inhibitors of Myelin with a Novel Neurotrophin Strategy. J. Biol. Chem. 280: 5862-5869 [Abstract] [Full Text]
Goldshmit, Y., Galea, M. P., Wise, G., Bartlett, P. F., Turnley, A. M. (2004). Axonal Regeneration and Lack of Astrocytic Gliosis in EphA4-Deficient Mice. J. Neurosci. 24: 10064-10073 [Abstract] [Full Text]
Tom, V. J., Doller, C. M., Malouf, A. T., Silver, J. (2004). Astrocyte-Associated Fibronectin Is Critical for Axonal Regeneration in Adult White Matter. J. Neurosci. 24: 9282-9290 [Abstract] [Full Text]
Ohno, T., Maeda, H., Sakurai, M. (2004). Regionally Specific Distribution of Corticospinal Synapses Because of Activity-Dependent Synapse Elimination In Vitro. J. Neurosci. 24: 1377-1384 [Abstract] [Full Text]
Kikuchi, K., Kishino, A., Konishi, O., Kumagai, K., Hosotani, N., Saji, I., Nakayama, C., Kimura, T. (2003). In Vitro and in Vivo Characterization of a Novel Semaphorin 3A Inhibitor, SM-216289 or Xanthofulvin. J. Biol. Chem. 278: 42985-42991 [Abstract] [Full Text]
Moreau-Fauvarque, C., Kumanogoh, A., Camand, E., Jaillard, C., Barbin, G., Boquet, I., Love, C., Jones, E. Y., Kikutani, H., Lubetzki, C., Dusart, I., Chedotal, A. (2003). The Transmembrane Semaphorin Sema4D/CD100, an Inhibitor of Axonal Growth, Is Expressed on Oligodendrocytes and Upregulated after CNS Lesion. J. Neurosci. 23: 9229-9239 [Abstract] [Full Text]
Oertle, T., van der Haar, M. E., Bandtlow, C. E., Robeva, A., Burfeind, P., Buss, A., Huber, A. B., Simonen, M., Schnell, L., Brosamle, C., Kaupmann, K., Vallon, R., Schwab, M. E. (2003). Nogo-A Inhibits Neurite Outgrowth and Cell Spreading with Three Discrete Regions. J. Neurosci. 23: 5393-5406 [Abstract] [Full Text]
Wong, E. V., David, S., Jacob, M. H., Jay, D. G. (2003). Inactivation of Myelin-Associated Glycoprotein Enhances Optic Nerve Regeneration. J. Neurosci. 23: 3112-3117 [Abstract] [Full Text]
Hulsebosch, C. E. (2002). RECENT ADVANCES IN PATHOPHYSIOLOGY AND TREATMENT OF SPINAL CORD INJURY. Adv. Physiol. Educ. 26: 238-255 [Abstract] [Full Text]
Fiedler, M., Horn, C., Bandtlow, C., Schwab, M.E., Skerra, A. (2002). An engineered IN-1 Fab fragment with improved affinity for the Nogo-A axonal growth inhibitor permits immunochemical detection and shows enhanced neutralizing activity. Protein Eng Des Sel 15: 931-941 [Abstract] [Full Text]
Horner, P. J., Gage, F. H. (2002). Regeneration in the Adult and Aging Brain. Arch Neurol 59: 1717-1720 [Full Text]
Fournier, A. E., Gould, G. C., Liu, B. P., Strittmatter, S. M. (2002). Truncated Soluble Nogo Receptor Binds Nogo-66 and Blocks Inhibition of Axon Growth by Myelin. J. Neurosci. 22: 8876-8883 [Abstract] [Full Text]
Bareyre, F. M., Haudenschild, B., Schwab, M. E. (2002). Long-Lasting Sprouting and Gene Expression Changes Induced by the Monoclonal Antibody IN-1 in the Adult Spinal Cord. J. Neurosci. 22: 7097-7110 [Abstract] [Full Text]
Dergham, P., Ellezam, B., Essagian, C., Avedissian, H., Lubell, W. D., McKerracher, L. (2002). Rho Signaling Pathway Targeted to Promote Spinal Cord Repair. J. Neurosci. 22: 6570-6577 [Abstract] [Full Text]
Kwon, B. K., Borisoff, J. F., Tetzlaff, W. (2002). Molecular Targets for Therapeutic Intervention after Spinal Cord Injury. Mol. Interv. 2: 244-258 [Abstract] [Full Text]
David, S., Ousman, S. S. (2002). Book Review: Recruiting the Immune Response to Promote Axon Regeneration in the Injured Spinal Cord. Neuroscientist 8: 33-41 [Abstract]
Grandpre, T., Strittmatter, S. M. (2001). Nogo: A Molecular Determinant of Axonal Growth and Regeneration. Neuroscientist 7: 377-386 [Abstract]
Raineteau, O., Fouad, K., Noth, P., Thallmair, M., Schwab, M. E. (2001). Functional switch between motor tracts in the presence of the mAb IN-1 in the adult rat. Proc. Natl. Acad. Sci. USA 10.1073/pnas.111165498v1 [Abstract] [Full Text]
Merkler, D., Metz, G. A. S., Raineteau, O., Dietz, V., Schwab, M. E., Fouad, K. (2001). Locomotor Recovery in Spinal Cord-Injured Rats Treated with an Antibody Neutralizing the Myelin-Associated Neurite Growth Inhibitor Nogo-A. J. Neurosci. 21: 3665-3673 [Abstract] [Full Text]
Fournier, A. E., Nakamura, F., Kawamoto, S., Goshima, Y., Kalb, R. G., Strittmatter, S. M. (2000). Semaphorin3a Enhances Endocytosis at Sites of Receptor-F-Actin Colocalization during Growth Cone Collapse. JCB 149: 411-422 [Abstract] [Full Text]
Shifman, M.I., Selzer, M.E. (2000). Expression of the Netrin Receptor UNC-5 in Lamprey Brain: Modulation by Spinal Cord Transection. Neurorehabil Neural Repair 14: 49-58 [Abstract]
Benowitz, L. I., Goldberg, D. E., Madsen, J. R., Soni, D., Irwin, N. (1999). Inosine stimulates extensive axon collateral growth in the rat corticospinal tract after injury. Proc. Natl. Acad. Sci. USA 96: 13486-13490 [Abstract] [Full Text]
Niederost, B. P., Zimmermann, D. R., Schwab, M. E., Bandtlow, C. E. (1999). Bovine CNS Myelin Contains Neurite Growth-Inhibitory Activity Associated with Chondroitin Sulfate Proteoglycans. J. Neurosci. 19: 8979-8989 [Abstract] [Full Text]
Pettigrew, D. B., Crutcher, K. A. (1999). White Matter of the CNS Supports or Inhibits Neurite Outgrowth In Vitro Depending on Geometry. J. Neurosci. 19: 8358-8366 [Abstract] [Full Text]
Lehmann, M., Fournier, A., Selles-Navarro, I., Dergham, P., Sebok, A., Leclerc, N., Tigyi, G., McKerracher, L. (1999). Inactivation of Rho Signaling Pathway Promotes CNS Axon Regeneration. J. Neurosci. 19: 7537-7547 [Abstract] [Full Text]
Walsh, G. S., Krol, K. M., Crutcher, K. A., Kawaja, M. D. (1999). Enhanced Neurotrophin-Induced Axon Growth in Myelinated Portions of the CNS in Mice Lacking the p75 Neurotrophin Receptor. J. Neurosci. 19: 4155-4168 [Abstract] [Full Text]
Kuhn, T. B., Brown, M. D., Wilcox, C. L., Raper, J. A., Bamburg, J. R. (1999). Myelin and Collapsin-1 Induce Motor Neuron Growth Cone Collapse through Different Pathways: Inhibition of Collapse by Opposing Mutants of Rac1. J. Neurosci. 19: 1965-1975 [Abstract] [Full Text]
Belien, A. T.J., Paganetti, P. A., Schwab, M. E. (1999). Membrane-type 1 Matrix Metalloprotease (MT1-MMP) Enables Invasive Migration of Glioma Cells in Central Nervous System White Matter. JCB 144: 373-384 [Abstract] [Full Text]
Zagrebelsky, M., Buffo, A., Skerra, A., Schwab, M. E., Strata, P., Rossi, F. (1998). Retrograde Regulation of Growth-Associated Gene Expression in Adult Rat Purkinje Cells by Myelin-Associated Neurite Growth Inhibitory Proteins. J. Neurosci. 18: 7912-7929 [Abstract] [Full Text]
Spillmann, A. A., Bandtlow, C. E., Lottspeich, F., Keller, F., Schwab, M. E. (1998). Identification and Characterization of a Bovine Neurite Growth Inhibitor (bNI-220). J. Biol. Chem. 273: 19283-19293 [Abstract] [Full Text]
Shibata, A., Wright, M.V., David, S., McKerracher, L., Braun, P.E., Kater, S.B. (1998). Unique Responses of Differentiating Neuronal Growth Cones to Inhibitory Cues Presented by Oligodendrocytes. JCB 142: 191-202 [Abstract] [Full Text]
Z'Graggen, W. J., Metz, G. A.�S., Kartje, G. L., Thallmair, M., Schwab, M. E. (1998). Functional Recovery and Enhanced Corticofugal Plasticity after Unilateral Pyramidal Tract Lesion and Blockade of Myelin-Associated Neurite Growth Inhibitors in Adult Rats. J. Neurosci. 18: 4744-4757 [Abstract] [Full Text]
Ramon-Cueto, A., Plant, G. W., Avila, J., Bunge, M. B. (1998). Long-Distance Axonal Regeneration in the Transected Adult Rat Spinal Cord Is Promoted by Olfactory Ensheathing Glia Transplants. J. Neurosci. 18: 3803-3815 [Abstract] [Full Text]
MAcLAREN, R. E (1998). Regeneration and transplantation of the optic nerve: developing a clinical strategy. Br J Ophthalmol 82: 577-583 [Full Text]
Knipper, M, Bandtlow, C, Gestwa, L, Kopschall, I, Rohbock, K, Wiechers, B, Zenner, H., Zimmermann, U (1998). Thyroid hormone affects Schwann cell and oligodendrocyte gene expression at the glial transition zone of the VIIIth nerve prior to cochlea function. Development 125: 3709-3718 [Abstract]
Tang, S., Shen, Y. J., DeBellard, M. E., Mukhopadhyay, G., Salzer, J. L., Crocker, P. R., Filbin, M. T. (1997). Myelin-associated Glycoprotein Interacts with Neurons via a Sialic Acid Binding Site at ARG118 and a Distinct Neurite Inhibition Site. JCB 138: 1355-1366 [Abstract] [Full Text]
Holtmaat, A. J.�G.�D., Hermens, W. T.�J.�M.�C., Sonnemans, M. A.�F., Giger, R. J., Van Leeuwen, F. W., Kaplitt, M. G., Oestreicher, A. B., Gispen, W. H., Verhaagen, J. (1997). Adenoviral Vector-Mediated Expression of B-50/GAP-43 Induces Alterations in the Membrane Organization of Olfactory Axon Terminals In Vivo. J. Neurosci. 17: 6575-6586 [Abstract] [Full Text]
Waxman, S. G., Kocsis, J. D. (1997). Spinal Cord Repair: Progress Towards a Daunting Goal. Neuroscientist 3: 263-269 [Abstract]
Lang, D. M., Hille, M. G., Schwab, M. E., Stuermer, C. A.�O. (1996). Modulation of the Inhibitory Substrate Properties of Oligodendrocytes by Platelet-Derived Growth Factor. J. Neurosci. 16: 5741-5748 [Abstract] [Full Text]
Bahr, M., Wizenmann, A. (1996). Retinal Ganglion Cell Axons Recognize Specific Guidance Cues Present in the Deafferented Adult Rat Superior Colliculus. J. Neurosci. 16: 5106-5116 [Abstract] [Full Text]
Fredette, B., Miller, J, Ranscht, B (1996). Inhibition of motor axon growth by T-cadherin substrata. Development 122: 3163-3171 [Abstract]
Strittmatter, S. M. (1995). Neuronal Guidance Molecules: Inhibitory and Soluble Factors. Neuroscientist 1: 255-258 [Abstract]
Connor, H., Nornes, H., Neuman, T. (1995). Expression Screening Reveals an Orphan Receptor Chick Ovalbumin Upstream Promoter Transcription Factor I as a Regulator of Neurite/Substrate-Cell Contacts and Cell Aggregation. J. Biol. Chem. 270: 15066-15070 [Abstract] [Full Text]
Thomas, L. B., Steindler, D. A. (1995). Review : Glial Boundaries and Scars: Programs for Normal Development and Wound Healing in the Brain. Neuroscientist 1: 142-154 [Abstract]
Selzer, M. E. (1995). Mechanisms of Functional Recovery in Traumatic Brain Injury. Neurorehabil Neural Repair 9: 73-82
Emerling, D., Lander, A. (1994). Laminar specific attachment and neurite outgrowth of thalamic neurons on cultured slices of developing cerebral neocortex. Development 120: 2811-2822 [Abstract]
Selzer, M. E. (1994). Regenerative Potential of the Spinal Cord. Neurorehabil Neural Repair 8: 11-15
Igarashi, M, Strittmatter, S., Vartanian, T, Fishman, M. (1993). Mediation by G proteins of signals that cause collapse of growth cones. Science 259: 77-79 [Abstract]
Bandtlow, C., Schmidt, M., Hassinger, T., Schwab, M., Kater, S. (1993). Role of intracellular calcium in NI-35-evoked collapse of neuronal growth cones. Science 259: 80-83 [Abstract]
Dodd, J, Jessell, T. (1988). Axon guidance and the patterning of neuronal projections in vertebrates. Science 242: 692-699 [Abstract]
Harrelson, A., Goodman, C. (1988). Growth cone guidance in insects: fasciclin II is a member of the immunoglobulin superfamily. Science 242: 700-708 [Abstract]
Raineteau, O., Fouad, K., Noth, P., Thallmair, M., Schwab, M. E. (2001). Functional switch between motor tracts in the presence of the mAb IN-1 in the adult rat. Proc. Natl. Acad. Sci. USA 98: 6929-6934 [Abstract] [Full Text]