Hostname: page-component-77c89778f8-rkxrd Total loading time: 0 Render date: 2024-07-20T21:56:09.687Z Has data issue: false hasContentIssue false
  • English
  • Français

The natural history of the myelin-derived nerve growth inhibitor Nogo-A

Published online by Cambridge University Press:  08 September 2009

Rüdiger Schweigreiter
Rüdiger Schweigreiter*
Affiliation:
Innsbruck Medical University, Biocenter, Division of Neurobiochemistry, 6020 Innsbruck, Austria
*
Correspondence should be addressed to: Rüdiger Schweigreiter, Innsbruck Medical University, Biocenter, Division of Neurobiochemistry, Fritz-Pregl-Strasse3, A-6020 Innsbruck, Austria phone: +43-(0)512-9003-70284 fax: +43-(0)512-9003-73280 email: ruediger.schweigreiter@i-med.ac.at
Get access Rights & Permissions [Opens in a new window]

Abstract

Nogo-A is possibly the best characterized myelin-derived inhibitor of nerve growth in the adult central nervous system (CNS). It is a member of the ancient reticulon family of mainly endoplasmic reticulum resident proteins with representatives found throughout the eukaryotic domain. Orthologs of the nogo gene were identified in tetrapods and teleost fish but none have been detected in invertebrates. Evolution of the nogo gene has been non-homogeneous. The exon–intron arrangement is conserved from amphibians (Xenopus) to mammals, but partly deviates from that found in several teleost fish species, indicating that the recruitment of nogo exons proceeded along at least two independent lines during early vertebrate evolution. This might have far-reaching consequences. Tetrapod nogo orthologs encode two neurite growth inhibitory domains whereas in fish nogo only one of the inhibitory domains is present. These distinct paths in nogo evolution have potentially contributed to the regeneration permissive CNS in fish as opposed to the non-regenerating CNS in higher vertebrates.

Keywords

Myelinnogoevolutionvertebratesteleost fish
Type
Research Article
Information
Neuron Glia Biology , Volume 4 , Issue 2 , May 2008 , pp. 83 - 89
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Amores, A., Force, A., Yan, Y.L., Joly, L., Amemiya, C., Fritz, A. et al. (1998) Zebrafish hox clusters and vertebrate genome evolution. Science 282, 1711–1714.CrossRefGoogle ScholarPubMed
Anderson, D.J. and Hetzer, M.W. (2008) Reshaping of the endoplasmic reticulum limits the rate for nuclear envelope formation. Journal of Cell Biology 182, 911–924.CrossRefGoogle ScholarPubMed
Atwal, J.K., Pinkston-Gosse, J., Syken, J., Stawicki, S., Wu, Y., Shatz, C. et al. (2008) PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 322, 967–970.CrossRefGoogle ScholarPubMed
Bareyre, F.M., Haudenschild, B. and Schwab, M.E. (2002) Long-lasting sprouting and gene expression changes induced by the monoclonal antibody IN-1 in the adult spinal cord. Journal of Neuroscience 22, 7097–7110.CrossRefGoogle ScholarPubMed
Bregman, B.S., Kunkel-Bagden, E., Schnell, L., Dai, H.N., Gao, D. and Schwab, M.E. (1995) Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378, 498–501.CrossRefGoogle ScholarPubMed
Brosamle, C. and Halpern, M.E. (2009) Nogo–Nogo receptor signalling in PNS axon outgrowth and pathfinding. Molecular and Cellular Neurosciences 40, 401–409.CrossRefGoogle ScholarPubMed
Buffo, A., Zagrebelsky, M., Huber, A.B., Skerra, A., Schwab, M.E., Strata, P. et al. (2000) Application of neutralizing antibodies against NI-35/250 myelin-associated neurite growth inhibitory proteins to the adult rat cerebellum induces sprouting of uninjured purkinje cell axons. Journal of Neuroscience 20, 2275–2286.CrossRefGoogle Scholar
Burridge, K. and Wennerberg, K. (2004) Rho and Rac take center stage. Cell 116, 167–179.CrossRefGoogle ScholarPubMed
Cafferty, W.B., Kim, J.E., Lee, J.K. and Strittmatter, S.M. (2007) Response to correspondence: Kim et al., “axon regeneration in young adult mice lacking Nogo-A/B.” Neuron 38, 187–199. Neuron 54, 195–199.CrossRefGoogle Scholar
Caroni, P. and Schwab, M.E. (1988) Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1, 85–96.CrossRefGoogle ScholarPubMed
Chen, M.S., Huber, A.B., van der Haar, M.E., Frank, M., Schnell, L., Spillmann, A.A. et al. (2000) Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403, 434–439.CrossRefGoogle Scholar
David, S. and Aguayo, A.J. (1981) Axonal elongation into peripheral nervous system “bridges” after central nervous system injury in adult rats. Science 214, 931–933.CrossRefGoogle ScholarPubMed
Diekmann, H., Klinger, M., Oertle, T., Heinz, D., Pogoda, H.M., Schwab, M.E. et al. (2005) Analysis of the reticulon gene family demonstrates the absence of the neurite growth inhibitor Nogo-A in fish. Molecular Biology and Evolution 22, 1635–1648.CrossRefGoogle ScholarPubMed
Dodd, D.A., Niederoest, B., Bloechlinger, S., Dupuis, L., Loeffler, J.P. and Schwab, M.E. (2005) Nogo-A, -B, and -C are found on the cell surface and interact together in many different cell types. Journal of Biological Chemistry 280, 12494–12502.CrossRefGoogle Scholar
Fournier, A.E., GrandPrè, T. and Strittmatter, S.M. (2001) Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409, 341–346.CrossRefGoogle ScholarPubMed
Freund, P., Schmidlin, E., Wannier, T., Bloch, J., Mir, A., Schwab, M.E. et al. (2006) Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nature Medicine 12, 790–792.CrossRefGoogle ScholarPubMed
Goldberg, J.L. and Barres, B.A. (2000) Nogo in nerve regeneration. Nature 403, 369–370.CrossRefGoogle ScholarPubMed
GrandPrè, T., Nakamura, F., Vartanian, T. and Strittmatter, S.M. (2000) Identification of the Nogo inhibitor of axon regeneration as a reticulon protein. Nature 403, 439–444.CrossRefGoogle ScholarPubMed
Hickmann, C.P., Roberts, L.S., Larson, A., l'Anson, H. and Eisenhour, D.J. (eds) (2005) Integrated Principles of Zoology. Blacklick, Ohio: McGraw-Hill.Google Scholar
Hu, F. and Strittmatter, S.M. (2008) The N-terminal domain of Nogo-A inhibits cell adhesion and axonal outgrowth by an integrin-specific mechanism. Journal of Neuroscience 28, 1262–1269.CrossRefGoogle ScholarPubMed
Huber, A.B., Weinmann, O., Brosamle, C., Oertle, T. and Schwab, M.E. (2002) Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. Journal of Neuroscience 22, 3553–3567.CrossRefGoogle ScholarPubMed
Hunt, D., Coffin, R.S., Prinjha, R.K., Campbell, G. and Anderson, P.N. (2003) Nogo-A expression in the intact and injured nervous system. Molecular and Cellular Neurosciences 24, 1083–1102.CrossRefGoogle ScholarPubMed
Iwahashi, J., Hamada, N. and Watanabe, H. (2007) Two hydrophobic segments of the RTN1 family determine the ER localization and retention. Biochemical and Biophysical Research Communications 355, 508–512.CrossRefGoogle ScholarPubMed
Kim, J.E., Li, S., GrandPre, T., Qiu, D. and Strittmatter, S.M. (2003) Axon regeneration in young adult mice lacking Nogo-A/B. Neuron 38, 187–199.CrossRefGoogle ScholarPubMed
Kiseleva, E., Morozova, K.N., Voeltz, G.K., Allen, T.D. and Goldberg, M.W. (2007) Reticulon 4a/NogoA locates to regions of high membrane curvature and may have a role in nuclear envelope growth. Journal of Structural Biology 160, 224–235.CrossRefGoogle ScholarPubMed
Klinger, M., Diekmann, H., Heinz, D., Hirsch, C., Hannbeck von Hanwehr, S., Petrausch, B. et al. (2004) Identification of two NOGO/RTN4 genes and analysis of Nogo-A expression in Xenopus laevis. Molecular and Cellular Neurosciences 25, 205–216.CrossRefGoogle ScholarPubMed
Kuraku, S., Meyer, A. and Kuratani, S. (2009) Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after? Molecular Biology and Evolution 26, 47–59.CrossRefGoogle ScholarPubMed
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.CrossRefGoogle ScholarPubMed
Liu, H., Ng, C.E. and Tang, B.L. (2002) Nogo-A expression in mouse central nervous system neurons. Neuroscience Letters 328, 257–260.CrossRefGoogle ScholarPubMed
McGee, A.W., Yang, Y., Fischer, Q.S., Daw, N.W. and Strittmatter, S.M. (2005) Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science 309, 2222–2226.CrossRefGoogle ScholarPubMed
McKerracher, L. and Higuchi, H. (2006) Targeting Rho to stimulate repair after spinal cord injury. Journal of Neurotrauma 23, 309–317.CrossRefGoogle ScholarPubMed
Merkler, D., Metz, G.A., Raineteau, O., Dietz, V., Schwab, M.E. and Fouad, K. (2001) Locomotor recovery in spinal cord-injured rats treated with an antibody neutralizing the myelin-associated neurite growth inhibitor Nogo-A. Journal of Neuroscience 21, 3665–3673.CrossRefGoogle ScholarPubMed
Oertle, T., Huber, C., van der Putten, H. and Schwab, M.E. (2003a) Genomic structure and functional characterisation of the promoters of human and mouse nogo/rtn4. Journal of Molecular Biology 325, 299–323.CrossRefGoogle ScholarPubMed
Oertle, T., Klinger, M., Stuermer, C.A. and Schwab, M.E. (2003b) A reticular rhapsody: phylogenic evolution and nomenclature of the RTN/Nogo gene family. FASEB Journal 17, 1238–1247.CrossRefGoogle ScholarPubMed
Oertle, T., Merkler, D. and Schwab, M.E. (2003c) Do cancer cells die because of Nogo-B? Oncogene 22, 1390–1399.CrossRefGoogle ScholarPubMed
Oertle, T. and Schwab, M.E. (2003d) Nogo and its paRTNers. Trends in Cell Biology 13, 187–194.CrossRefGoogle ScholarPubMed
Oertle, T., van der Haar, M.E., Bandtlow, C.E., Robeva, A., Burfeind, P., Buss, A. et al. (2003e) Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. Journal of Neuroscience 23, 5393–5406.CrossRefGoogle ScholarPubMed
Prinjha, R., Moore, S.E., Vinson, M., Blake, S., Morrow, R., Christie, G. et al. (2000) Inhibitor of neurite outgrowth in humans. Nature 403, 383–384.CrossRefGoogle ScholarPubMed
Qi, B., Qi, Y., Watari, A., Yoshioka, N., Inoue, H., Minemoto, Y. et al. (2003) Pro-apoptotic ASY/Nogo-B protein associates with ASYIP. Journal of Cell Physiology 196, 312–318.CrossRefGoogle ScholarPubMed
Richardson, P.M., McGuinness, U.M. and Aguayo, A.J. (1980) Axons from CNS neurons regenerate into PNS grafts. Nature 284, 264–265.CrossRefGoogle ScholarPubMed
Roebroek, A.J., van de Velde, H.J., Van Bokhoven, A., Broers, J.L., Ramaekers, F.C. and Van de Ven, W.J. (1993) Cloning and expression of alternative transcripts of a novel neuroendocrine-specific gene and identification of its 135-kDa translational product. Journal of Biological Chemistry 268, 13439–13447.CrossRefGoogle ScholarPubMed
Schnell, L. and Schwab, M.E. (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343, 269–272.CrossRefGoogle ScholarPubMed
Schwab, M.E. and Caroni, P. (1988) Oligodendrocytes and CNS myelin are nonpermissive substrates for neurite growth and fibroblast spreading in vitro. Journal of Neuroscience 8, 2381–2393.CrossRefGoogle ScholarPubMed
Schwab, M.E. and Thoenen, H. (1985) Dissociated neurons regenerate into sciatic but not optic nerve explants in culture irrespective of neurotrophic factors. Journal of Neuroscience 5, 2415–2423.CrossRefGoogle Scholar
Schweigreiter, R. and Bandtlow, C.E. (2006) Nogo in the injured spinal cord. Journal of Neurotrauma 23, 384–396.CrossRefGoogle ScholarPubMed
Schweigreiter, R., Roots, B.I., Bandtlow, C.E. and Gould, R.M. (2006) Understanding myelination through studying its evolution. International Review of Neurobiology 73, 219–273.CrossRefGoogle ScholarPubMed
Shibata, Y., Voss, C., Rist, J.M., Hu, J., Rapoport, T.A., Prinz, W.A. et al. (2008) The reticulon and DP1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. Journal of Biological Chemistry 283, 18892–18904.CrossRefGoogle ScholarPubMed
Simonen, M., Pedersen, V., Weinmann, O., Schnell, L., Buss, A., Ledermann, B. et al. (2003) Systemic deletion of the myelin-associated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 38, 201–211.CrossRefGoogle ScholarPubMed
Spillmann, A.A., Bandtlow, C.E., Lottspeich, F., Keller, F. and Schwab, M.E. (1998) Identification and characterization of a bovine neurite growth inhibitor (bNI-220). Journal of Biological Chemistry 273, 19283–19293.CrossRefGoogle ScholarPubMed
Steward, O., Zheng, B., Banos, K. and Yee, K.M. (2007) Response to: Kim et al., “axon regeneration in young adult mice lacking Nogo-A/B.” Neuron 38, 187–199. Neuron 54, 191–195.CrossRefGoogle Scholar
Syken, J., Grandpre, T., Kanold, P.O. and Shatz, C.J. (2006) PirB restricts ocular-dominance plasticity in visual cortex. Science 313, 1795–1800.CrossRefGoogle ScholarPubMed
Teng, F.Y. and Tang, B.L. (2008) Cell autonomous function of Nogo and reticulons: The emerging story at the endoplasmic reticulum. Journal of Cellular Physiology 216, 303–308.CrossRefGoogle Scholar
van de Velde, H.J., Roebroek, A.J., Senden, N.H., Ramaekers, F.C. and Van de Ven, W.J. (1994) NSP-encoded reticulons, neuroendocrine proteins of a novel gene family associated with membranes of the endoplasmic reticulum. Journal of Cell Science 107, 2403–2416.CrossRefGoogle ScholarPubMed
Voeltz, G.K., Prinz, W.A., Shibata, Y., Rist, J.M. and Rapoport, T.A. (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124, 573–586.CrossRefGoogle ScholarPubMed
Zheng, B., Ho, C., Li, S., Keirstead, H., Steward, O. and Tessier-Lavigne, M. (2003) Lack of enhanced spinal regeneration in Nogo-deficient mice. Neuron 38, 213–224.CrossRefGoogle ScholarPubMed