Retinal axon guidance: Novel mechanisms for steering

Current Opinion in Neurobiology

Volumn 14, Issue 1, 2004, Pages 61-66

  Van Horck, Francis P G ^a   Weinl, Christine ^a   Holt, Christine E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

CAMP; CGMP; Cyclic adenosine monophosphate; Cyclic guanosine monophosphate; DCC; Deleted in colorectal cancer; LPA; Lysophosphatidic acid; MAPK; Mitogen activated protein kinase; ONH; Optic nerve head; Retinal ganglion cell; RGC; SDF 1

Indexed keywords

CELL SURFACE PROTEIN; CYCLIC AMP; CYCLIC GMP; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; NERVE CELL ADHESION MOLECULE; NETRIN; PHOSPHATIDYLINOSITOL 3 KINASE;

CELL COMPARTMENTALIZATION; CYTOSKELETON; DROSOPHILA; FILOPODIUM; INTRACELLULAR MEMBRANE; MOLECULAR INTERACTION; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; RETINA CONE; RETINA NERVE CELL; REVIEW; SIGNAL TRANSDUCTION; TRANSLATION INITIATION; VISUAL SYSTEM;

EID: 1342285543     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2004.01.002     Document Type: Review

References (45)

1. Dickson B.J. Molecular mechanisms of axon guidance. Science. 298:2002;1959-1964.
2. Tessier-Lavigne M., Goodman C.S. The molecular biology of axon guidance. Science. 274:1996;1123-1133.
3. Oster S.F., Sretavan D.W. Connecting the eye to the brain: the molecular basis of ganglion cell axon guidance. Br J Ophthalmol. 87:2003;639-645.
4. Herrera E., Brown L., Aruga J., Rachel R.A., Dolen G., Mikoshiba K., Brown S., Mason C.A. Zic2 patterns binocular vision by specifying the uncrossed retinal projection. Cell. 114:2003;545-557.
5. Williams S.E., Mann F., Erskine L., Sakurai T., Wei S., Rossi D.J., Gale N.W., Holt C.E., Mason C.A., Henkemeyer M. Ephrin-B2 and EphB1 mediate retinal axon divergence at the optic chiasm. Neuron. 39:2003;919-935.
6. Nakagawa S., Brennan C., Johnson K.G., Shewan D., Harris W.A., Holt C.E. Ephrin-B regulates the ipsilateral routing of retinal axons at the optic chiasm. Neuron. 25:2000;599-610.
7. Rasband K., Hardy M., Chien C.B. Generating X: formation of the optic chiasm. Neuron. 39:2003;885-888.
8. Hutson L.D., Chien C.B. Pathfinding and error correction by retinal axons: the role of astray/robo2. Neuron. 33:2002;205-217.
9. Irie A., Yates E.A., Turnbull J.E., Holt C.E. Specific heparan sulfate structures involved in retinal axon targeting. Development. 129:2002;61-70.
10. Hutson L.D., Chien C.B. Wiring the zebrafish: axon guidance and synaptogenesis. Curr Opin Neurobiol. 12:2002;87-92.
11. Plump A.S., Erskine L., Sabatier C., Brose K., Epstein C.J., Goodman C.S., Mason C.A., Tessier-Lavigne M. Slit1 and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron. 33:2002;219-232.
12. Hindges R., McLaughlin T., Genoud N., Henkemeyer M., O'Leary D.D. EphB forward signaling controls directional branch extension and arborization required for dorsal-ventral retinotopic mapping. Neuron. 35:2002;475-487.
13. Mann F., Ray S., Harris W., Holt C. Topographic mapping in dorsoventral axis of the Xenopus retinotectal system depends on signaling through ephrin-B ligands. Neuron. 35:2002;461-473.
14. Song H.J., Poo M.M. Signal transduction underlying growth cone guidance by diffusible factors. Curr Opin Neurobiol. 9:1999;355-363.
15. Nishiyama M., Hoshino A., Tsai L., Henley J.R., Goshima Y., Tessier-Lavigne M., Poo M.M., Hong K. Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning. Nature. 424:2003;990-995.
16. Hopker V.H., Shewan D., Tessier-Lavigne M., Poo M., Holt C. Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature. 401:1999;69-73.
17. Chalasani S.H., Sabelko K.A., Sunshine M.J., Littman D.R., Raper J.A. A chemokine, SDF-1, reduces the effectiveness of multiple axonal repellents and is required for normal axon pathfinding. J Neurosci. 23:2003;1360-1371 This study shows that SDF-1 modulates the repellent activity of slit-2 on retinal axons, Sema3A on dorsal root ganglion cells and Sema3C on sympathetic neurons in chicks. This is a modulatory effect, because SDF-1 has no detectable attractant or repellent activity on retinal ganglion cell growth cones itself. This is in contrast to cultured rat cerebellar axons, which turn away from a gradient of SDF-1.
18. Zhu Y., Yu T., Zhang X.C., Nagasawa T., Wu J.Y., Rao Y. Role of the chemokine SDF-1 as the meningeal attractant for embryonic cerebellar neurons. Nat Neurosci. 5:2002;719-720.
19. Bagri A., Gurney T., He X., Zou Y.R., Littman D.R., Tessier-Lavigne M., Pleasure S.J. The chemokine SDF1 regulates migration of dentate granule cells. Development. 129:2002;4249-4260.
20. Xiang Y., Li Y., Zhang Z., Cui K., Wang S., Yuan X.B., Wu C.P., Poo M.M., Duan S. Nerve growth cone guidance mediated by G protein-coupled receptors. Nat Neurosci. 5:2002;843-848.
21. Song J., Wu L., Chen Z., Kohanski R.A., Pick L. Axons guided by insulin receptor in Drosophila visual system. Science. 300:2003;502-505.
22. Dickson B.J. Development. Wiring the brain with insulin. Science. 300:2003;440-441.
23. Brittis P.A., Lu Q., Flanagan J.G. Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell. 110:2002;223-235 The authors show that the EphA2 receptor expression is upregulated in the distal segments of a subset of commissural axons at the midline. This expression can be mimicked by the introduction of EphA2 3′UTR (untranslated region) RNA, attached to a reporter, into embryonic spinal cord, resulting in upregulated protein expression in distal segments of commissural axons that had reached or crossed the midline floor plate. Mutation of the cytoplasmic polyadenylation element binding sequence, present in the 3′UTR, abolishes this specific upregulation, demonstrating that an RNA-based mechanism is required for specific expression in the distal axon segments at the midline.
24. Zheng J.Q., Kelly T.K., Chang B., Ryazantsev S., Rajasekaran A.K., Martin K.C., Twiss J.L. A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J Neurosci. 21:2001;9291-9303.
25. 3H -leucine incorporation) and degradation of proteins in isolated growth cones on a surprisingly rapid timescale (5-10 min).
26. Campenot R.B., Eng H. Protein synthesis in axons and its possible functions. J Neurocytol. 29:2000;793-798.
27. Campbell D.S., Holt C.E. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron. 37:2003;939-952 This study demonstrates that p42/44 and p38 MAPK pathways are key regulators of protein synthesis and proteasomal degradation, induced by netrin-1, Sema3A and LPA. It also shows that inhibition of the apoptotic enzyme, caspase-3, blocks netrin- and LPA-induced chemorepulsion and that it mediates the protein degradation that is required for netrin and LPA growth cone guidance in vitro.
28. Lee S.K., Hollenbeck P.J. Organization and translation of mRNA in sympathetic axons. J Cell Sci. 116:2003;4467-4478.
29. Shirasaki R., Mirzayan C., Tessier-Lavigne M., Murakami F. Guidance of circumferentially growing axons by netrin-dependent and -independent floor plate chemotropism in the vertebrate brain. Neuron. 17:1996;1079-1088.
30. Ming G.L., Wong S.T., Henley J., Yuan X.B., Song H.J., Spitzer N.C., Poo M.M. Adaptation in the chemotactic guidance of nerve growth cones. Nature. 417:2002;411-418.
31. Steward O., Schuman E.M. Compartmentalized synthesis and degradation of proteins in neurons. Neuron. 40:2003;347-359.
32. Mann F., Miranda E., Weinl C., Harmer E., Holt C. B-type Eph receptors and Ephrins induce growth cone collapse through distinct intracellular pathways. J Neurobiol. 57:2003;323-336 This study analyses the two different forward and reverse signaling pathways that are triggered by ephrinB and EphB receptors in Xenopus, in vitro. Dorsal growth cones expressing ephrinB show a fast but transient collapse response when stimulated with unclustered EphB2-Fc, which is mediated by low cGMP levels and requires proteasomal function. Ventral growth cones, expressing EphB receptors, exhibit a slow collapse response, which is dependent on high levels of cGMP, independent of proteasomal function. Endocytosis seems to be functionally important because blocking of endocytosis also inhibits the collapse response. Endocytosis in this system could only be visualized in the reverse signaling.
33. Clemens M.J., Bushell M., Morley S.J. Degradation of eukaryotic polypeptide chain initiation factor (eIF) 4G in response to induction of apoptosis in human lymphoma cell lines. Oncogene. 17:1998;2921-2931.
34. Marissen W.E., Lloyd R.E. Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells. Mol Cell Biol. 18:1998;7565-7574.
35. Hattori M., Osterfield M., Flanagan J.G. Regulated cleavage of a contact-mediated axon repellent. Science. 289:2000;1360-1365.
36. Stein E., Tessier-Lavigne M. Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science. 291:2001;1928-1938.
37. Webber C.A., Hocking J.C., Yong V.W., Stange C.L., McFarlane S. Metalloproteases and guidance of retinal axons in the developing visual system. J Neurosci. 22:2002;8091-8100 Metalloproteases have been described to terminate receptor ligand signaling in vitro. This study illustrates the relevance for metalloproteases acting in axon guidance in the visual pathway in vivo. Using the exposed brain preparation in Xenopus embryos, the authors show that retinal ganglion cell axons make pathfinding errors in the diencephalon and fail to enter the tectum after the application of metalloprotease inhibitors.
38. Galko M.J., Tessier-Lavigne M. Function of an axonal chemoattractant modulated by metalloprotease activity. Science. 289:2000;1365-1367.
39. McFarlane S. Metalloproteases: carving out a role in axon guidance. Neuron. 37:2003;559-562.
40. Zimmer M., Palmer A., Kohler J., Klein R. EphB-ephrinB bi-directional endocytosis terminates adhesion allowing contact mediated repulsion. Nat Cell Biol. 5:2003;869-878 After stimulation with either the soluble Fc-constructs or cells expressing ephrinB1 or EphB2, endocytosis occurs, as shown in cell lines and forebrain neurons. Full-length ephrin and EphB are endocytosed in a bidirectional manner in both forward and reverse signaling. This event is sufficient for cell detachment and necessary for collapse; truncation of the C-terminal results in an abnormal adhesion between normally retracting cells.
41. Marston D.J., Dickinson S., Nobes C.D. Rac-dependent trans-endocytosis of ephrinBs regulates Eph-ephrin contact repulsion. Nat Cell Biol. 5:2003;879-888.
42. Fournier A.E., Nakamura F., Kawamoto S., Goshima Y., Kalb R.G., Strittmatter S.M. Semaphorin3A enhances endocytosis at sites of receptor-F-actin colocalization during growth cone collapse. J Cell Biol. 149:2000;411-422.
43. Jurney W.M., Gallo G., Letourneau P.C., McLoon S.C. Rac1-mediated endocytosis during ephrin-A2- and semaphorin 3A-induced growth cone collapse. J Neurosci. 22:2002;6019-6028 This study shows that two repulsive axon guidance cues, ephrin-A2 and semaphorin 3A, induce rapid endocytosis in retinal growth cones via the small GTPase, Rac1. Inhibition of Rac1 function prevents growth cone collapse in vitro and, significantly, causes abnormal retinotectal targeting in vivo.
44. Campbell D.S., Regan A.G., Lopez J.S., Tannahill D., Harris W.A., Holt C.E. Semaphorin 3A elicits stage-dependent collapse, turning, and branching in Xenopus retinal growth cones. J Neurosci. 21:2001;8538-8547.
45. Shewan D., Dwivedy A., Anderson R., Holt C.E. Age-related changes underlie switch in netrin-1 responsiveness as growth cones advance along visual pathway. Nat Neurosci. 5:2002;955-962 Using a whole visual pathway preparation, combined with turning assays, this study shows that Xenopus retinal growth cones change their responsiveness to netrin gradually as they advance through the pathway. Axons without pathway experience but aged in culture show similar responses. Looking at the mechanisms in detail, the authors found that DCC and the A2b receptor mediate this netrin responsiveness, either independently or as co-receptors.