RabGDI controls axonal midline crossing by regulating Robo1 surface expression

Neural Development

Volumn 7, Issue 1, 2012, Pages

  Philipp, Melanie ^a   Niederkofler, Vera ^b   Debrunner, Marc ^c   Alther, Tobias ^c   Kunz, Beat ^c   Stoeckli, Esther T ^c  

^a UNIVERSITY OF ULM   (Germany)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Axon guidance; Chicken embryo; In ovo RNAi; Membrane trafficking; Mental retardation gene; Slit; Spinal cord development

Indexed keywords

GDP DISSOCIATION INHIBITOR 1; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; IMMUNOGLOBULIN RECEPTOR; NERVE PROTEIN; ROUNDABOUT RECEPTOR;

ANIMAL; ARTICLE; CELL LINE; CELL MOTION; CERCOPITHECUS; CHICK EMBRYO; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEMISPHERIC DOMINANCE; HUMAN; METABOLISM; NERVE CELL; NERVE FIBER; PHYSIOLOGY; PRENATAL DEVELOPMENT; RNA INTERFERENCE; SPINAL CORD; TRAFFIC AND TRANSPORT;

ANIMALS; AXONS; CELL LINE, TRANSFORMED; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; CHICK EMBRYO; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; HUMANS; NERVE TISSUE PROTEINS; NEURONS; RECEPTORS, IMMUNOLOGIC; RNA INTERFERENCE; SPINAL CORD; TRANSFECTION; TRANSPORTATION;

EID: 84868535089     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-7-36     Document Type: Article

References (69)

1. Tessier-Lavigne M, Goodman CS. The molecular biology of axon guidance. Science 1996, 274:1123-1133. 10.1126/science.274.5290.1123, 8895455.
2. Dickson BJ. Molecular mechanisms of axon guidance. Science 2002, 298:1959-1964. 10.1126/science.1072165, 12471249.
3. Stoeckli ET, Landmesser LT. Axon guidance at choice points. Curr Opin Neurobiol 1998, 8:73-79. 10.1016/S0959-4388(98)80010-X, 9568394.
4. Kaprielian Z, Runko E, Imondi R. Axon guidance at the midline choice point. Dev Dyn 2001, 221:154-181. 10.1002/dvdy.1143, 11376484.
5. Chisholm A, Tessier-Lavigne M. Conservation and divergence of axon guidance mechanisms. Curr Opin Neurobiol 1999, 9:603-615. 10.1016/S0959-4388(99)00021-5, 10508749.
6. Araujo SJ, Tear G. Axon guidance mechanisms and molecules: lessons from invertebrates. Nat Rev Neurosci 2003, 4:910-922.
7. Augsburger A, Schuchardt A, Hoskins S, Dodd J, Butler S. BMPs as mediators of roof plate repulsion of commissural neurons. Neuron 1999, 24:127-141. 10.1016/S0896-6273(00)80827-2, 10677032.
8. Butler SJ, Dodd J. A role for BMP heterodimers in roof plate-mediated repulsion of commissural axons. Neuron 2003, 38:389-401. 10.1016/S0896-6273(03)00254-X, 12741987.
9. Islam SM, Shinmyo Y, Okafuji T, Su Y, Naser IB, Ahmed G, Zhang S, Chen S, Ohta K, Kiyonari H, et al. Draxin, a repulsive guidance protein for spinal cord and forebrain commissures. Science 2009, 323:388-393. 10.1126/science.1165187, 19150847.
10. Charron F, Tessier-Lavigne M. Novel brain wiring functions for classical morphogens: a role as graded positional cues in axon guidance. Development 2005, 132:2251-2262. 10.1242/dev.01830, 15857918.
11. Tear G. Axon guidance at the central nervous system midline. Cell Mol Life Sci 1999, 55:1365-1376. 10.1007/s000180050377, 10518986.
12. Seeger M, Tear G, Ferres-Marco D, Goodman CS. Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 1993, 10:409-426. 10.1016/0896-6273(93)90330-T, 8461134.
13. 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. 10.1016/S0896-6273(00)80070-7, 8785048.
14. 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 evolutionarily conserved guidance receptors. Cell 1998, 92:205-215. 10.1016/S0092-8674(00)80915-0, 9458045.
15. Kidd T, Bland KS, Goodman CS. Slit is the midline repellent for the robo receptor in Drosophila. Cell 1999, 96:785-794. 10.1016/S0092-8674(00)80589-9, 10102267.
16. 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. 10.1016/S0896-6273(00)80431-6, 9459439.
17. Myat A, Henry P, McCabe V, Flintoft L, Rotin D, Tear G. Drosophila Nedd4, a ubiquitin ligase, is recruited by Commissureless to control cell surface levels of the roundabout receptor. Neuron 2002, 35:447-459. 10.1016/S0896-6273(02)00795-X, 12165468.
18. Keleman K, Rajagopalan S, Cleppien D, Teis D, Paiha K, Huber LA, Technau GM, Dickson BJ. Comm sorts robo to control axon guidance at the Drosophila midline. Cell 2002, 110:415-427. 10.1016/S0092-8674(02)00901-7, 12202032.
19. Keleman K, Ribeiro C, Dickson BJ. Comm function in commissural axon guidance: cell-autonomous sorting of Robo in vivo. Nat Neurosci 2005, 8:156-163. 10.1038/nn1388, 15657595.
20. Stoeckli ET, Landmesser LT. Axonin-1, Nr-CAM, and Ng-CAM play different roles in the in vivo guidance of chick commissural neurons. Neuron 1995, 14:1165-1179. 10.1016/0896-6273(95)90264-3, 7541632.
21. Stoeckli ET, Sonderegger P, Pollerberg GE, Landmesser LT. Interference with axonin-1 and NrCAM interactions unmasks a floor-plate activity inhibitory for commissural axons. Neuron 1997, 18:209-221. 10.1016/S0896-6273(00)80262-7, 9052792.
22. Fitzli D, Stoeckli ET, Kunz S, Siribour K, Rader C, Kunz B, Kozlov SV, Buchstaller A, Lane RP, Suter DM, Dreyer WJ, Sonderegger P. A direct interaction of axonin-1 with NgCAM-related cell adhesion molecule (NrCAM) results in guidance, but not growth of commissural axons. J Cell Biol 2000, 149:951-968. 10.1083/jcb.149.4.951, 2174557, 10811834.
23. Zou Y, Stoeckli E, Chen H, Tessier-Lavigne M. Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 2000, 102:363-375. 10.1016/S0092-8674(00)00041-6, 10975526.
24. Battye R, Stevens A, Jacobs JR. Axon repulsion from the midline of the Drosophila CNS requires slit function. Development 1999, 126:2475-2481.
25. Brose K, Bland KS, Wang KH, Arnott D, Henzel W, Goodman CS, Tessier-Lavigne M, Kidd T. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 1999, 96:795-806. 10.1016/S0092-8674(00)80590-5, 10102268.
26. Li HS, Chen JH, Wu W, Fagaly T, Zhou L, Yuan W, Dupuis S, Jiang ZH, Nash W, Gick C, Ornitz DM, Wu JY, Rao Y. Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 1999, 96:807-818. 10.1016/S0092-8674(00)80591-7, 10102269.
27. Long H, Sabatier C, Ma L, Plump A, Yuan W, Ornitz DM, Tamada A, Murakami F, Goodman CS, Tessier-Lavigne M. Conserved roles for Slit and Robo proteins in midline commissural axon guidance. Neuron 2004, 42:213-223. 10.1016/S0896-6273(04)00179-5, 15091338.
28. Sabatier C, Plump AS, Le M, Brose K, Tamada A, Murakami F, Lee EY, Tessier-Lavigne M. The divergent Robo family protein rig-1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell 2004, 117:157-169. 10.1016/S0092-8674(04)00303-4, 15084255.
29. Hammond R, Vivancos V, Naeem A, Chilton J, Mambetisaeva E, Andrews W, Sundaresan V, Guthrie S. Slit-mediated repulsion is a key regulator of motor axon pathfinding in the hindbrain. Development 2005, 132:4483-4495. 10.1242/dev.02038, 16162649.
30. Holmes GP, Negus K, Burridge L, Raman S, Algar E, Yamada T, Little MH. Distinct but overlapping expression patterns of two vertebrate Slit homologs implies functional roles in CNS development and organogenesis. Mech Dev 1998, 79:57-72. 10.1016/S0925-4773(98)00174-9, 10349621.
31. Itoh A, Miyabayashi T, Ohno M, Sakano S. Cloning and expressions of three mammalian homologues of Drosophila slit suggest possible roles for Slit in the formation and maintenance of the nervous system. Brain Res Mol Brain Res 1998, 62:175-186.
32. Wong K, Park HT, Wu JY, Rao Y. Slit proteins: molecular guidance cues for cells ranging from neurons to leukocytes. Curr Opin Genet Dev 2002, 12:583-591. 10.1016/S0959-437X(02)00343-X, 12200164.
33. Yuan W, Zhou L, Chen JH, Wu JY, Rao Y, Ornitz DM. The mouse SLIT family: secreted ligands for ROBO expressed in patterns that suggest a role in morphogenesis and axon guidance. Dev Biol 1999, 212:290-306. 10.1006/dbio.1999.9371, 10433822.
34. Camurri L, Mambetisaeva E, Sundaresan V. Rig-1 a new member of Robo family genes exhibits distinct pattern of expression during mouse development. Gene Expr Patterns 2004, 4:99-103. 10.1016/S1567-133X(03)00142-X, 14678835.
35. Sundaresan V, Mambetisaeva E, Andrews W, Annan A, Knoll B, Tear G, Bannister L. Dynamic expression patterns of Robo (Robo1 and Robo2) in the developing murine central nervous system. J Comp Neurol 2004, 468:467-481. 10.1002/cne.10984, 14689480.
36. Huminiecki L, Gorn M, Suchting S, Poulsom R, Bicknell R. Magic roundabout is a new member of the roundabout receptor family that is endothelial specific and expressed at sites of active angiogenesis. Genomics 2002, 79:547-552. 10.1006/geno.2002.6745, 11944987.
37. Weitzman M, Bayley EB, Naik UP. Robo4: a guidance receptor that regulates angiogenesis. Cell Adh Migr 2008, 2:220-222. 10.4161/cam.2.4.7061, 2637482, 19270536.
38. Park KW, Morrison CM, Sorensen LK, Jones CA, Rao Y, Chien CB, Wu JY, Urness LD, Li DY. Robo4 is a vascular-specific receptor that inhibits endothelial migration. Dev Biol 2003, 261:251-267. 10.1016/S0012-1606(03)00258-6, 12941633.
39. Bedell VM, Yeo SY, Park KW, Chung J, Seth P, Shivalingappa V, Zhao J, Obara T, Sukhatme VP, Drummond IA, et al. roundabout4 is essential for angiogenesis in vivo. Proc Natl Acad Sci USA 2005, 102:6373-6378. 10.1073/pnas.0408318102, 1088354, 15849270.
40. Chien CB. Why does the growth cone cross the road?. Neuron 1998, 20:3-6. 10.1016/S0896-6273(00)80427-4, 9459435.
41. Guthrie S. Axon guidance: mice and men need Rig and Robo. Curr Biol 2004, 14:R632-R634. 10.1016/j.cub.2004.07.050, 15296783.
42. Garbe DS, Bashaw GJ. Axon guidance at the midline: from mutants to mechanisms. Crit Rev Biochem Mol Biol 2004, 39:319-341. 10.1080/10409230490906797, 15763708.
43. Dickson BJ, Gilestro GF. Regulation of commissural axon pathfinding by slit and its Robo receptors. Annu Rev Cell Dev Biol 2006, 22:651-675. 10.1146/annurev.cellbio.21.090704.151234, 17029581.
44. Georgiou M, Tear G. Commissureless is required both in commissural neurones and midline cells for axon guidance across the midline. Development 2002, 129:2947-2956.
45. Chen Z, Gore BB, Long H, Ma L, Tessier-Lavigne M. Alternative splicing of the Robo3 axon guidance receptor governs the midline switch from attraction to repulsion. Neuron 2008, 58:325-332. 10.1016/j.neuron.2008.02.016, 18466743.
46. Seabra MC, Mules EH, Hume AN. Rab GTPases, intracellular traffic and disease. Trends Mol Med 2002, 8:23-30. 10.1016/S1471-4914(01)02227-4, 11796263.
47. Pfeffer S, Aivazian D. Targeting Rab GTPases to distinct membrane compartments. Nat Rev Mol Cell Biol 2004, 5:886-896.
48. D'Adamo P, Menegon A, Lo Nigro C, Grasso M, Gulisano M, Tamanini F, Bienvenu T, Gedeon AK, Oostra B, Wu SK, Tandon A, Valtorta F, Balch WE, Chelly J, Toniolo D. Mutations in GDI1 are responsible for X-linked non-specific mental retardation. Nat Genet 1998, 19:134-139. 10.1038/487, 9620768.
49. D'Adamo P, Welzl H, Papadimitriou S, Raffaele Di Barletta M, Tiveron C, Tatangelo L, Pozzi L, Chapman PF, Knevett SG, Ramsay MF, Valtorta F, Leoni C, Menegon A, Wolfer DP, Lipp HP, Toniolo D. Deletion of the mental retardation gene Gdi1 impairs associative memory and alters social behavior in mice. Hum Mol Genet 2002, 11:2567-2580. 10.1093/hmg/11.21.2567, 12354782.
50. Pekarik V, Bourikas D, Miglino N, Joset P, Preiswerk S, Stoeckli ET. Screening for gene function in chicken embryo using RNAi and electroporation. Nat Biotechnol 2003, 21:93-96. 10.1038/nbt770, 12496763.
51. Bourikas D, Pekarik V, Baeriswyl T, Grunditz A, Sadhu R, Nardo M, Stoeckli ET. Sonic hedgehog guides commissural axons along the longitudinal axis of the spinal cord. Nat Neurosci 2005, 8:297-304. 10.1038/nn1396, 15746914.
52. Mauti O, Sadhu R, Gemayel J, Gesemann M, Stoeckli ET. Expression patterns of plexins and neuropilins are consistent with cooperative and separate functions during neural development. BMC Dev Biol 2006, 6:32. 10.1186/1471-213X-6-32, 1543641, 16846494.
53. Simpson JH, Bland KS, Fetter RD, Goodman CS. Short-range and long-range guidance by Slit and its Robo receptors: a combinatorial code of Robo receptors controls lateral position. Cell 2000, 103:1019-1032. 10.1016/S0092-8674(00)00206-3, 11163179.
54. Bagri A, Marin O, Plump AS, Mak J, Pleasure SJ, Rubenstein JL, Tessier-Lavigne M. Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 2002, 33:233-248. 10.1016/S0896-6273(02)00561-5, 11804571.
55. Plump AS, Erskine L, Sabatier C, Brose K, Epstein CJ, Goodman CS, Mason CA, Tessier-Lavigne M. Slit1 and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 2002, 33:219-232. 10.1016/S0896-6273(01)00586-4, 11804570.
56. Mambetisaeva ET, Andrews W, Camurri L, Annan A, Sundaresan V. Robo family of proteins exhibit differential expression in mouse spinal cord and Robo-Slit interaction is required for midline crossing in vertebrate spinal cord. Dev Dyn 2005, 533:41-51.
57. Reeber SL, Sakai N, Nakada Y, Dumas J, Dobrenis K, Johnson JE, Kaprielian Z. Manipulating Robo expression in vivo perturbs commissural axon pathfinding in the chick spinal cord. J Neurosci 2008, 28:8698-8708. 10.1523/JNEUROSCI.1479-08.2008, 2886497, 18753371.
58. Ward ES, Martinez C, Vaccaro C, Zhou J, Tang Q, Ober RJ. From sorting endosomes to exocytosis: association of Rab4 and Rab11 GTPases with the Fc receptor, FcRn, during recycling. Mol Biol Cell 2005, 16:2028-2038. 10.1091/mbc.E04-08-0735, 1073680, 15689494.
59. Marillat V, Sabatier C, Failli V, Matsunaga E, Sotelo C, Tessier-Lavigne M, Chedotal A. The slit receptor Rig-1/Robo3 controls midline crossing by hindbrain precerebellar neurons and axons. Neuron 2004, 43:69-79. 10.1016/j.neuron.2004.06.018, 15233918.
60. Nawabi H, Briancon-Marjollet A, Clark C, Sanyas I, Takamatsu H, Okuno T, Kumanogoh A, Bozon M, Takeshima K, Yoshida Y, et al. A midline switch of receptor processing regulates commissural axon guidance in vertebrates. Genes Dev 2010, 24:396-410. 10.1101/gad.542510, 2816738, 20159958.
61. Parra LM, Zou Y. Sonic hedgehog induces response of commissural axons to Semaphorin repulsion during midline crossing. Nat Neurosci 2010, 13:29-35. 10.1038/nn.2457, 19946319.
62. Domanitskaya E, Wacker A, Mauti O, Baeriswyl T, Esteve P, Bovolenta P, Stoeckli ET. Sonic hedgehog guides post-crossing commissural axons both directly and indirectly by regulating Wnt activity. J Neurosci 2010, 30:11167-11176. 10.1523/JNEUROSCI.1488-10.2010, 20720124.
63. Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. J Morphol 1951, 88:49-92.
64. Perrin FE, Stoeckli ET. Use of lipophilic dyes in studies of axonal pathfinding in vivo. Microsc Res Tech 2000, 48:25-31. 10.1002/(SICI)1097-0029(20000101)48:1<25::AID-JEMT4>3.0.CO;2-F, 10620782.
65. Vargesson N, Luria V, Messina I, Erskine L, Laufer E. Expression patterns of Slit and Robo family members during vertebrate limb development. Mech Dev 2001, 106:175-180. 10.1016/S0925-4773(01)00430-0, 11472852.
66. Perrin FE, Rathjen FG, Stoeckli ET. Distinct subpopulations of sensory afferents require F11 or axonin-1 for growth to their target layers within the spinal cord of the chick. Neuron 2001, 30:707-723. 10.1016/S0896-6273(01)00315-4, 11430805.
67. Niederkofler V, Salie R, Sigrist M, Arber S. Repulsive guidance molecule (RGM) gene function is required for neural tube closure but not retinal topography in the mouse visual system. J Neurosci 2004, 24:808-818. 10.1523/JNEUROSCI.4610-03.2004, 14749425.
68. De Bellard ME, Rao Y, Bronner-Fraser M. Dual function of Slit2 in repulsion and enhanced migration of trunk, but not vagal, neural crest cells. J Cell Biol 2003, 162:269-279. 10.1083/jcb.200301041, 2172792, 12876276.
69. Ng EL, Tang BL. Rab GTPases and their roles in brain neurons and glia. Brain Res Rev 2008, 58:236-246. 10.1016/j.brainresrev.2008.04.006, 18485483.