Signal transduction underlying growth cone guidance by diffusible factors

Current Opinion in Neurobiology

Volumn 9, Issue 3, 1999, Pages 355-363

  Song, Hong Jun ^a   Poo, Mu Ming ^b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM; CHEMOTACTIC FACTOR; CYCLIC NUCLEOTIDE; GROWTH FACTOR; GUANOSINE TRIPHOSPHATASE; NERVE GROWTH FACTOR; NETRIN; NEUROPILIN; NEUROTROPHIC FACTOR; PROTEIN TYROSINE KINASE; SEMAPHORIN;

GROWTH CONE; NERVE FIBER GROWTH; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 0033152924     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(99)80052-X     Document Type: Article

References (88)

1. Tessier-Lavigne M, Goodman CS: The molecular biology of axon guidance. Science 1996, 274:1123-1133.
2. Mueller BK: Growth cone guidance: First steps towards a deeper understanding. Annu Rev Neurosci 1999, 22:351-388. A recent detailed review of the current understanding of axon guidance.
3. Gundersen RW, Barrett JN: Neuronal chemotaxis: Chick dorsal-root axons turn toward high concentrations of nerve growth factor. Science 1979, 206:1079-1080.
4. Letourneau PC: Chemotactic response of nerve fiber elongation to nerve growth factor. Dev Biol 1978, 66:183-196.
5. Ming GI, Lohof AM, Zheng JQ: Acute morphogenic and chemotropic effects of neurotrophins on cultured embryonic Xenopus spinal neurons. J Neurosci 1997, 17:7860-7871.
6. Cook G, Tannahill D, Keynes R: Axon guidance to and from choice points. Curr Opin Neurobiol 1998, 8:64-72.
7. Stoeckli ET, Landmesser LT: Axon guidance at choice points. Curr Opin Neurobiol 1998, 8:73-79.
8. Holt CE, Harris WA: Target selection: Invasion, mapping and cell choice. Curr Opin Neurobiol 1998, 8:98-105.
9. Culotti JG, Merz DC: DCC and netrins. Curr Opin Cell Biol 1998, 10:609-613.
10. Fujisawa H, Kitsukawa T: Receptors for collapsin/semaphorins. Curr Opin Neurobiol 1998, 8:587-592.
11. Hedgecock EM, Culotti JG, Hall DH: The unc-5, unc-6, and unc- 40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 1990, 4:61-85.
12. Hamelin M, Zhou Y, Su MW, Scott IM, Culotti JG: Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature 1993, 364:327-330.
13. 2+ and the netrin receptor DCC. Thus, netrin-1 can attract and repel the same population of axons through similar signal transduction mechanisms.
14. Keino-Masu K, Masu M, Hinck L, Leonardo ED, Chan SS, Culotti JG, Tessier-Lavigne M: Deleted in colorectal cancer (DCC) encodes a netrin receptor. Cell 1996, 87:175-185.
15. Chan SS, Zheng H, Su MW, Wilk R, Killeen MT, Hedgecock EM, Culotti JG: UNC-40, a C. elegans homolog of DCC (deleted in colorectal cancer), is required in motile cells responding to UNC-6 netrin cues. Cell 1996, 87:187-195.
16. Kolodziej PA, Timpe LC, Mitchell KJ, Fried SR, Goodman CS, Jan LY, Jan YN: Frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 1996, 87:197-204.
17. Hu G, Zhang S, Vidal M, Baer JL, Xu T, Fearon ER: Mammalian homologs of seven in absentia regulate DCC via the ubiquitin-proteasome pathway. Genes Dev 1997, 11:2701-2714.
18. Leonardo ED, Hinck L, Masu M, Keino-Masu K, Ackerman SL, Tessier- Lavigne M: Vertebrate homologs of C. elegans UNC-5 are candidate netrin receptors. Nature 1997, 386:833-838.
19. Bennett V: Ankyrins. Adaptors between diverse plasma membrane proteins and the cytoplasm. J Biol Chem 1992, 267:8703-8706.
20. Colavita A, Culotti JG: Suppressors of ectopic UNC-5 growth cone steering identify eight genes involved in axon guidance in Caenorhabditis elegans. Dev Biol 1998, 194:72-85.
21. Wills Z, Marr L, Zinn K, Goodman CS, Van Vactor D: Profilin and the Abl tyrosine kinase are required for motor axon outgrowth in the Drosophila embryo. Neuron 1999, 22:291-299.
22. Wills Z, Bateman J, Korey CA, Comer A, Van Vactor D: The tyrosine kinase Abl and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron 1999, 22:301-312.
23. Lanier LM, Gates MA, Witke W, Sheila Menzies A, Wehman AM, Macklis JD, Kwiatkowski D, Soriano P, Gertler FB: Mena is required for neurulation and commissure formation. Neuron 1999, 22:313-325.
24. Yu HH, Kolodkin AL: Semaphorin signaling: A little less per-plexin. Neuron 1999, 22:11-14.
25. Isbister CM, Tsai A, Wong ST, Kolodkin AL, O'Connor TP: Discrete roles for secreted and transmembrane semaphorins in neuronal growth cone guidance in vivo. Development 1999, 126:2007-2019.
26. Adams RH, Lohrum M, Klostermann A, Betz H, Puschel AW: The chemorepulsive activity of secreted semaphorins is regulated by furin-dependent proteolytic processing. EMBO J 1997, 16:6077-6086.
27. Song H, Ming G, He Z, Lehmann M, Tessier-Lavigne M, Poo M-m: Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 1998, 281:1515-1518. Microscopic gradients of Sema III and MAG trigger repulsive turning responses by growth cones of cultured Xenopus spinal neurons; the repulsion can be converted to attraction by pharmacological activation of cGMP and cAMP signaling pathways, respectively. Together with other findings [13•,53••,84•], these point to the notion that there are shared signal transduction mechanisms for a large group of guidance cues, and that cyclic nucleotides are key modulators in setting the neuronal response to different guidance cues.
28. Bagnard D, Lohrum M, Uziel D, Puschel AW, Bolz J: Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections. Development 1998, 125:5043-5053. Early studies showed that Sema D and Sema E function as chemorepellents for sympathetic neurons. This paper reports that for cortical axons, Sema D functions as a chemorepellent, whereas Sema E acts as a chemoattractant. Thus, semaphorins are bifunctional guidance cues, acting in opposite manners for different axons.
29. He Z, Tessier-Lavigne M: Neuropilin is a receptor for the axonal chemorepellent semaphorin III. Cell 1997, 90:739-751. See annotation [30••].
30. Kolodkin AL, Levengood DV, Rowe EG, Tai YT, Giger RJ, Ginty DD: Neuropilin is a semaphorin III receptor. Cell 1997, 90:753-762. Together with [29••], this paper reports the expression cloning and binding properties of neuropilin-1 as a repulsive receptor for Sema III. Neuropilin was previously cloned by Fujisawa's group (see [10]), with no definitive physiological function.
31. Chen H, Chedotal A, He Z, Goodman CS, Tessier-Lavigne M: Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 1997, 19:547-559. This paper reports the cloning of NPN-2, a homolog of NPN-1 (see also [30••]). Unlike the NPN-1 receptor, which binds with high affinity to the three structurally related semaphorins (Sema III, E, and IV), the NPN-2 receptor shows high-affinity binding only to Sema E and Sema IV, not Sema III.
32. Kitsukawa T, Shimizu M, Sanbo M, Hirata T, Taniguchi M, Bekku Y, Yagi T, Fujisawa H: Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 1997, 19:995-1005.
33. Giger RJ, Urquhart ER, Gillespie SK, Levengood DV, Ginty DD, Kolodkin AL: Neuropilin-2 is a receptor for semaphorin IV: Insight into the structural basis of receptor function and specificity. Neuron 1998, 21:1079-1092. The authors identified NPN-2 as a receptor for Sema IV and found that NPN-1 could homomultimerize and heteromultimerize with NPN-2. Together with [34,35•], they dissected the specificity of Sema and NPN interactions.
34. Takahashi T, Nakamura F, Jin Z, Kalb RG, Strittmatter SM: Semaphorins A and E act as antagonists of neuropilin-1 and agonists of neuropilin-2 receptors. Nat Neurosci 1998, 1:487-493.
35. Chen H, He Z, Bagri A, Tessier-Lavigne M: Semaphorin-neuropilin interactions underlying sympathetic axon responses to class III semaphorins. Neuron 1998, 21:1283-1290. Using functional blocking antibodies to NPN-1, the authors dissected the specificity of different class III semaphorins for the two receptors NPN-1 and NPN-2 in sympathetic axons. They proposed that Sema III or Sema IV signaling is mediated by NPN-1 or NPN-2 homo-oligomers, respectively, whereas Sema E signaling is mediated by both NPN-1 and NPN-2, as homo- or hetero-oligomers.
36. Nakamura F, Tanaka M, Takahashi T, Kalb RG, Strittmatter SM: Neuropilin-1 extracellular domains mediate semaphorin D/III-induced growth cone collapse. Neuron 1998, 21:1093-1100. Using virus-mediated overexpression of NPN-1 mutants in chick retinal ganglion cells, the authors demonstrate that Sema-D-induced growth cone collapse requires two segments of the ectodomain of NPN-1, the CUB domain and MAM domain. In contrast, the transmembrane segment and cytoplasmic tail of NPN-1 are not required for biologic activity, suggesting a co-receptor is required for Sema-D-induced responses.
37. Goshima Y, Nakamura F, Strittmatter P, Strittmatter SM: Collapsin- Induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 1995, 376:509-514.
38. Jin Z, Strittmatter SM: Rac1 mediates collapsin-1-induced growth cone collapse. J Neurosci 1997, 17:6256-6263.
39. Kuhn TB, Brown MD, Wilcox CL, Raper JA, Bamburg JR: Myelin and collapsin-1 induce motor neuron growth cone collapse through different pathways: Inhibition of collapse by opposing mutants of rac1. J Neurosci 1999, 19:1965-1975.
40. Comeau MR, Johnson R, DuBose RF, Petersen M, Gearing P, Vandenbos T, Park L, Farrah T, Buller RM, Cohen JI et al.: A poxvirus- Encoded semaphorin induces cytokine production from monocytes and binds to a novel cellular semaphorin receptor, VESPR. Immunity 1998, 8:473-482.
41. Winberg ML, Noordermeer JN, Tamagnone L, Comoglio PM, Spriggs MK, Tessier-Lavigne M, Goodman CS: Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 1998, 95:903-916. Genetic studies of Drosophila indicate that plexin A is a neuronal receptor for class I semaphorins (Sema 1a and Sema 1b) to control motor and CNS axon guidance. Together with the finding in the immune system that VESPR, a member of the plexin family, is a receptor for a viral-encoded semaphorin [40], this suggests that members of the plexin family may constitute the receptors for different semaphorins.
42. Kidd T, Brose K, Mitchell KJ, Fetter RD, Tessier-Lavigne M, Goodman CS, Tear G: Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionary conserved guidance receptors. Cell 1998, 92:205-215. This paper reports cloning of the robo gene in Drosophila and shows that Robo is expressed on ipsilateral projecting axons from the onset of growth, whereas on commissural axons, it is upregulated only after the axons have crossed the midline. Thus, Robo mediates a repulsive signal to prevent axons from crossing the midline. The ligand for Robo has now been identified as the diffusible extracellular protein Slit [46••-48••].
43. Tear G, Harris R, Sutaria S, Kilomanski K, Goodman CS, Seeger MA: Commissureless controls growth cone guidance across the CNS midline in Drosophila and encodes a novel membrane protein. Neuron 1996, 16:501-514.
44. Kidd T, Russell C, Goodman CS, Tear G: Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron 1998, 20:25-33.
45. Zallen JA, Yi BA, Bargmann CI: The conserved immunoglobulin superfamily member SAX-3/robo directs multiple aspects of axon guidance in C. elegans. Cell 1998, 92:217-227. This paper reports that sax-3 in C. elegans is a homolog of the Drosophila robo gene. Mutations in sax-3 lead to repeated midline crossing by ventral cord axons that normally do not cross the midline after they join the ventral cord, a phenotype similar to that of robo mutants [42••]. In addition, sax-3 is also required for guidance of some axons to the ventral cord.
46. Kidd T, Bland KS, Goodman CS: Slit is the midline repellent for the robo receptor in drosophila. Cell 1999, 96:785-794. Together with two other papers [47••,48••], Slit is identified as a Robo ligand. In this paper, the authors demonstrate genetic interactions between slit and robo, suggesting that these two molecules act in the same pathway. Slit appears to function as a short-range repellent controlling axon crossing of the midline and as a long-range chemorepellent controlling mesoderm migration away from the midline.
47. Brose K, Bland KS, Wang KH, Arnott D, Henzel W, Goodman CS, Tessier-Lavigne M, Kidd T: Evolutionary conservation of the repulsive axon guidance function of slit proteins and of their interactions with robo receptors. Cell 1999, 96:795-806. This paper provides biochemical evidence that the Drosophila Slit protein and at least one of the mammalian Slit proteins, Slit2, bind Robo proteins with high affinity (see also [48••]). Furthermore, recombinant Slit2 can repel embryonic spinal motor axons in cell culture.
48. Li H, Chen J, WU W, Fagaly T, Zhou L, Yuan W, Dupuis S, Jiang ZH, Nash W, Gick C et al.: Vertebrate slit, a ligand for the transmembrane protein roundabout, is repellent for olfactory bulb axons. Cell 1999, 96:807-818. This paper reports the isolation of vertebrate homologs of the Drosophila slit gene and shows that Slit protein binds to Robo (see also [47••]). These authors also show that Slit, expressed in the septum, acts a chemorepellent for olfactory bulb axons that express Robo.
49. Rothberg JM, Hartley DA, Walther Z, Artavanis-Tsakonas S: Slit: An EGF-homologous locus of D. melanogaster involved in the development of the embryonic central nervous system. Cell 1988, 55:1047-1059.
50. Ba-Charvet KTN, Brose K, Marillat V, Kidd T, Goodman CS, Tessier- Lavigne M, Sotelo C, Chédotal A: Slit2-mediated chemorepulsion and collapse of developing forebrain axons. Neuron 1999, 22:463-473.
51. Wang KH, Brose K, Arnott D, Kidd T, Goodman CS, Henzel W, Tessier-Lavigne M: Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 1999, 96:771-784.
52. Menesini-Chen MG, Chen JS, Levi-Montalcini R: Sympathetic nerve fibers ingrowth in the central nervous system of neonatal rodent upon intracerebral NGF injections. Arch Ital Biol 1978, 116:53-84.
53. Song HJ, Ming GL, Poo M-m: cAMP-induced switching in turning direction of nerve growth cones. Nature 1997, 388:275-279. A gradient of BDNF normally triggers an attractive turning response of the growth cones of cultured Xenopus spinal neurons, but the same gradient induces repulsive turning of these growth cones in the presence of a competitive analogue of cAMP or of a specific inhibitor of PKA. Thus, the response of a growth cone to a particular guidance cue may depend critically on other coincident signals received by the neuron.
54. ElShamy WM, Linnarsson S, Lee KF, Jaenisch R, Ernfors P: Prenatal and postnatal requirements of NT-3 for sympathetic neuroblast survival and innervation of specific targets. Development 1996, 122:491-500.
55. Wang Q, Zheng JQ: cAMP-mediated regulation of neurotrophin-induced collapse of nerve growth cones. J Neurosci 1998, 18:4973-4984.
56. Segal RA, Greenberg ME: Intracellular signaling pathways activated by neurotrophic factors. Annu Rev Neurosci 1996, 19:463-489.
57. Ebens A, Brose K, Leonardo ED, Hanson MG Jr, Bladt F, Birchmeier C, Barres BA, Tessier-Lavigne M: Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 1996, 17:1157-1172.
58. McFarlane S, McNeiLL L, Holt CE: FGF signaling and target recognition in the developing xenopus visual system. Neuron 1995, 15:1017-1028.
59. McFarlane S, Cornel E, Amaya E, Holt CE: Inhibition of FGF receptor activity in retinal ganglion cell axons causes errors in target recognition. Neuron 1996, 17:245-254.
60. ColavitA A, Krishna S, Zheng H, Padgett RW, Culotti JG: Pioneer axon guidance by UNC-129, a C. elegans TGF-β. Science 1998, 281:706-709. This paper reports that UNC-129, a member of the transforming growth factor-β superfamily of secreted factors, is required to guide pioneer motor axons along the dorsal-ventral axis of C. elegans. Ectopic expression of UNC-129 from ventral body wall disrupts the growth cone and cell migration that normally take place along the dorsal-ventral axis.
61. Tang S, Woodhall RW, Shen YJ, deBellard ME, Saffell JL, Doherty P, Walsh FS, Filbin MT: Soluble myelin-associated glycoprotein (MAG) found in vivo inhibits axonal regeneration. Mol Cell Neurosci 1997, 9:333-346.
62. Walsh FS, Doherty P: Neural cell adhesion molecules of the immunoglobulin superfamily: Role in axon growth and guidance. Annu Rev Cell Dev Biol 1997, 13:425-456.
63. Goodman CS: Mechanisms and molecules that control growth cone guidance. Annu Rev Neurosci 1996, 19:341-377.
64. 2+ transients. Nature 1995, 375:784-787.
65. 2+ transients.
66. Bandtlow CE, Schmidt MF, Hassinger TD, Schwab ME, Kater SB: Role of intracellular calcium in NI-35-evoked collapse of neuronal growth cones. Science 1993, 259:80-83.
67. Zheng JQ, Felder M, Connor JA, Poo M-m: Turning of nerve growth cones induced by neurotransmitters. Nature 1994, 368:140-144.
68. Berridge MJ: Neuronal calcium signaling. Neuron 1998, 21:13-26.
69. 3 receptor in the growth cone induced by chromophore-assisted laser inactivation results in growth arrest and neurite retraction.
70. 2+-calmodulin signaling in drosophila growth cones leads to stalls in axon extension and errors in axon guidance. Neuron 1995, 14:43-56.
71. Strittmatter SM, Fankhauser C, Huang PL, Mashimo H, Fishman MC: Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell 1995, 80:445-452.
72. Xia Z, Storm DR: Calmodulin-regulated adenylyl cyclases and Neuromodulation. Curr Opin Neurobiol 1997, 7:391-396.
73. Abdel-Majid RM, Leong WL, Schalkwyk LC, Smallman DS, Wong ST, Storm DR, Fine A, Dobson MJ, Guernsey DL, Neumann PE: Loss of adenylyl cyclase I activity disrupts patterning of mouse somatosensory cortex. Nat Genet 1998, 19:289-291. The somatosensory cortex of mice displays a patterned, nonuniform distribution of neurons in layer IV. Mice homozygous for the barrelless (brl) mutant, which occurs spontaneously, fail to develop the normal patterned distribution of neurons. The authors identified adenylyl cyclase type I as the gene disrupted in brl mutant mice, providing evidence for the involvement of cAMP signaling pathways in pattern formation during brain development.
74. Kim YT, Wu CF: Reduced growth cone motility in cultured neurons from Drosophila memory mutants with a defective cAMP cascade. J Neurosci 1996, 16:5593-5602.
75. Lohof AM, Quillan M, Dan Y, Poo M-m: Asymmetric modulation of cytosolic cAMP activity induces growth cone turning. J Neurosci 1992, 12:1253-1261.
76. O'Connor KL, Shaw LM, Mercurio AM: Release of cAMP gating by the alpha6beta4 integrin stimulates lamellae formation and the chemotactic migration of invasive carcinoma cells. J Cell Biol 1998, 143:1749-1760.
77. Haug LS, Jensen V, Hvalby O, Walaas SI, Ostvold AC: Phosphorylation of the inositol 1,4,5-trisphosphate receptor by cyclic nucleotide-dependent kinases in vitro and in rat cerebellar slices in situ. J Biol Chem 1999, 274:7467-7473.
78. Gradin HM, Larsson N, Marklund U, Gullberg M: Regulation of microtubule dynamics by extracellular signals: cAMP-dependent protein kinase switches off the activity of oncoprotein 18 in intact cells. J Cell Biol 1998, 140:131-141.
79. Lang P, Gesbert F, Delespine-Carmagnat M, Stancou R, Pouchelet M, Bertoglio J: Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J 1996, 15:510-519.
80. Laudanna C, Campbell JJ, Butcher EC: Elevation of intracellular cAMP inhibits RhoA activation and integrin-dependent leukocyte adhesion induced by chemoattractants. J Biol Chem 1997, 272:24141-241444.
81. Foster DC, Wedel BJ, Robinson SW, Garbers DL: Mechanisms of regulation and functions of guanylyl cyclases. Rev Physiol Biochem Pharmacol 1999, 135:1-39.
82. Wu HH, Williams CV, McLoon SC: Involvement of nitric oxide in the elimination of a transient retinotectal projection in development. Science 1994, 265:1593-1596.
83. Gibbs SM, Truman JW: Nitric oxide and cyclic GMP regulate retinal patterning in the optic lobe of Drosophila. Neuron 1998, 20:83-93.
84. Ming GL, Song HJ, Berninger B, Inagaki N, Tessier-Lavigne M, Poo M-m: Phospholipase c-γ and phosphoinositide 3-kinase mediate cytoplasmic signaling in nerve growth cone guidance. Neuron 1999, 22: in press. This paper provides additional evidence that two independent pathways are shared by the two groups of guidance cues [13•,27••,53••]: there is complete cross-desensitization of turning responses for each pair of guidance cues within the same group but not with the other group (see Figure 1 in this review). Furthermore, the actions of group I cues may require co-activation of PLC-γ and PI-3 kinase pathways.
85. Tigyi G, Fischer DJ, Sebok A, Marshall F, Dyer DL, Miledi R: Lysophosphatidic acid-induced neurite retraction in PC12 cells: Neurite-protective effects of cyclic AMP signaling. J Neurochem 1996, 66:549-558.
86. Cai D, Shen Y, De Bellard M, Tang S, Filbin MT: Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron 1999, 22:89-101.
87. HAll A: Rho GTPpases and the actin cytoskeleton. Science 1998, 279:509-514.
88. Garrity PA, Rao Y, Salecker I, McGlade J, Pawson T, Zipursky SL: Drosophila photoreceptor axon guidance and targeting requires the dreadlocks SH2/SH3 adapter protein. Cell 1996, 85:639-650.