DCC mediated axon guidance of spinal interneurons is essential for normal locomotor central pattern generator function

Developmental Biology

Volumn 366, Issue 2, 2012, Pages 279-289

  Rabe Bernhardt, Nadine ^a   Memic, Fatima ^a   Gezelius, Henrik ^a   Thiebes, Anja Lena ^a   Vallstedt, Anna ^a   Kullander, Klas ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Axon guidance; Commissural interneuron; Development; Neuronal network; V3 subtype

Indexed keywords

DELETED IN COLORECTAL CANCER PROTEIN; NETRIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL LOSS; CELL SUBPOPULATION; CONTROLLED STUDY; LOCOMOTION; MOTOR COORDINATION; MOUSE; MUSCULOSKELETAL FUNCTION; MUTANT; NERVE CELL MEMBRANE POTENTIAL; NERVE CONDUCTION; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; SPINAL CORD; SPINAL CORD NERVE CELL; VISUAL AREA V3;

MUS;

EID: 84861226043     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.03.017     Document Type: Article

References (69)

1. Ackerman S., Kozak L., Przyborski S., Rund L., Boyer B., Knowles B. The mouse rostral cerebellar malformation gene encodes an UNC-5-like protein. Nature 1997, 386:838-842.
2. Barrett C., Guthrie S. Expression patterns of the netrin receptor UNC5H1 among developing motor neurons in the embryonic rat hindbrain. Mech. Dev. 2001, 106:163-166.
3. Bennett K.L., Bradshaw J., Youngman T., Rodgers J., Greenfield B., Aruffo A., Linsley P.S. Deleted in colorectal carcinoma (DCC) binds heparin via its fifth fibronectin type III domain. J. Biol. Chem. 1997, 272:26940-26946.
4. Bermingham N.A., Hassan B.A., Wang V.Y., Fernandez M., Banfi S., Bellen H.J., Fritzsch B., Zoghbi H.Y. Proprioceptor pathway development is dependent on Math1. Neuron 2001, 30:411-422.
5. Briscoe J., Sussel L., Serup P., Hartigan-O'Connor D., Jessell T.M., Rubenstein J.L., Ericson J. Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 1999, 398:622-627.
6. Brownstone R.M., Wilson J.M. Strategies for delineating spinal locomotor rhythm-generating networks and the possible role of Hb9 interneurones in rhythmogenesis. Brain Res. Rev. 2008, 57:64-76.
7. Burgess R.W., Jucius T.J., Ackerman S.L. Motor axon guidance of the mammalian trochlear and phrenic nerves: dependence on the netrin receptor Unc5c and modifier loci. J. Neurosci. 2006, 26:5756-5766.
8. 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.
9. Cheng L., Arata A., Mizuguchi R., Qian Y., Karunaratne A., Gray P.A., Arata S., Shirasawa S., Bouchard M., Luo P., Chen C.-L., Busslinger M., Goulding M., Onimaru H., Ma Q. Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat. Neurosci. 2004, 7:510-517.
10. Cohen A.H., Harris-Warrick R.M. Strychnine eliminates alternating motor output during fictive locomotion in the lamprey. Brain Res. 1984, 293:164-167.
11. Cooper H., Armes P., Britto J., Gad J., Wilks A. Cloning of the mouse homologue of the deleted in colorectal cancer gene (mDCC) and its expression in the developing mouse embryo. Oncogene 1995, 11:2243-2254.
12. Corset V., Nguyen-Ba-Charvet K.T., Forcet C., Moyse E., Chédotal A., Mehlen P. Netrin-1-mediated axon outgrowth and cAMP production requires interaction with adenosine A2b receptor. Nature 2000, 407:747-750.
13. Cowley K.C., Schmidt B.J. Effects of inhibitory amino acid antagonists on reciprocal inhibitory interactions during rhythmic motor activity in the in vitro neonatal rat spinal cord. J Neurophysiol 1995, 74:1109-1117.
14. Crone S.A., Quinlan K.A., Zagoraiou L., Droho S., Restrepo C.E., Lundfald L., Endo T., Setlak J., Jessell T.M., Kiehn O., Sharma K. Genetic ablation of V2a ipsilateral interneurons disrupts left-right locomotor coordination in mammalian spinal cord. Neuron 2008, 60:70-83.
15. Dillon A.K., Fujita S.C., Matise M.P., Jarjour A.A., Kennedy T.E., Kollmus H., Arnold H.-H., Weiner J.A., Sanes J.R., Kaprielian Z. Molecular control of spinal accessory motor neuron/axon development in the mouse spinal cord. J. Neurosci. 2005, 25:10119-10130.
16. Eide A.L., Glover J.C. Development of the longitudinal projection patterns of lumbar primary sensory afferents in the chicken embryo. J. Comp. Neurol. 1995, 353:247-259.
17. Fazeli A., Dickinson S.L., Hermiston M.L., Tighe R.V., Steen R.G., Small C.G., Stoeckli E.T., Keino-Masu K., Masu M., Rayburn H., Simons J., Bronson R.T., Gordon J.I., Tessier-Lavigne M., Weinberg R.A. Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 1997, 386:796-804.
18. Fearon E.R., Cho K.R., Nigro J.M., Kern S.E., Simons J.W., Ruppert J.M., Hamilton S.R., Preisinger A.C., Thomas G., Kinzler K.W. Identification of a chromosome 18q gene that is altered in colorectal cancers. Science 1990, 247:49-56.
19. Finger J.H., Bronson R.T., Harris B., Johnson K., Przyborski S.A., Ackerman S.L. The netrin 1 receptors Unc5h3 and Dcc are necessary at multiple choice points for the guidance of corticospinal tract axons. J. Neurosci. 2002, 22:10346-10356.
20. Goulding M., Lanuza G., Sapir T., Narayan S. The formation of sensorimotor circuits. Curr. Opin. Neurobiol. 2002, 12:508-515.
21. Goulding M., Pfaff S.L. Development of circuits that generate simple rhythmic behaviors in vertebrates. Curr. Opin. Neurobiol. 2005, 15:14-20.
22. Grillner S. The motor infrastructure: from ion channels to neuronal networks. Nat. Rev. Neurosci. 2003, 4:573-586.
23. Grillner S. Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 2006, 52:751-766.
24. Grillner S., Wallén P. Does the central pattern generation for locomotion in lamprey depend on glycine inhibition?. Acta Physiol. Scand. 1980, 110:103-105.
25. Gross M.K., Moran-Rivard L., Velasquez T., Nakatsu M.N., Jagla K., Goulding M. Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development 2000, 127:413-424.
26. Hedgecock E.M., Culotti J.G., Hall D.H. 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.
27. Hedgecock E.M., Culotti J.G., Hall D.H., Stern B.D. Genetics of cell and axon migrations in Caenorhabditis elegans. Development 1987, 100:365-382.
28. Hong K., Hinck L., Nishiyama M., Poo M.M., Tessier-Lavigne M., Stein E. A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 1999, 97:927-941.
29. Honigberg L., Kenyon C. Establishment of left/right asymmetry in neuroblast migration by UNC-40/DCC, UNC-73/Trio and DPY-19 proteins in C. elegans. Development 2000, 127:4655-4668.
30. Jankowska E., Noga B.R. Contralaterally projecting lamina VIII interneurones in middle lumbar segments in the cat. Brain Res. 1990, 535:327-330.
31. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 2000, 1:20-29.
32. Keino-Masu K., Masu M., Hinck L., Leonardo E., Chan S., Culotti J., Tessier-Lavigne M. Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 1996, 87:175-185.
33. Kennedy T.E., Serafini T., de la Torre J.R., Tessier-Lavigne M. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 1994, 78:425-435.
34. Kiehn O. Locomotor circuits in the mammalian spinal cord. Annu. Rev. Neurosci. 2006, 29:279-306.
35. Kiehn O., Butt S.J. Physiological, anatomical and genetic identification of CPG neurons in the developing mammalian spinal cord. Prog. Neurobiol. 2003, 70:347-361.
36. Kiehn O., Kullander K. Central pattern generators deciphered by molecular genetics. Neuron 2004, 41:317-321.
37. Kim S., Ren X., Fox E., Wadsworth W. SDQR migrations in Caenorhabditis elegans are controlled by multiple guidance cues and changing responses to netrin UNC-6. Development 1999, 126:3881-3890.
38. Kolodziej P., Timpe L., Mitchell K., Fried S., Goodman C., Jan L., Jan Y. frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 1996, 87:197-204.
39. Kullander K. Genetics moving to neuronal networks. Trends Neurosci. 2005, 28:239-247.
40. Kullander K., Butt S.J.B., Lebret J.M., Lundfald L., Restrepo C.E., Rydström A., Klein R., Kiehn O. Role of EphA4 and EphrinB3 in local neuronal circuits that control walking. Science 2003, 299:1889-1892.
41. Lanuza G.M., Gosgnach S., Pierani A., Jessell T.M., Goulding M. Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 2004, 42:375-386.
42. Leonardo E., Hinck L., Masu M., Keino-Masu K., Ackerman S., Tessier-Lavigne M. Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 1997, 386:833-838.
43. Li X., Meriane M., Triki I., Shekarabi M., Kennedy T., Larose L., Lamarche-Vane N. The adaptor protein Nck-1 couples the netrin-1 receptor DCC (deleted in colorectal cancer) to the activation of the small GTPase Rac1 through an atypical mechanism. J. Biol. Chem. 2002, 277:37788-37797.
44. Ly A., Nikolaev A., Suresh G., Zheng Y., Tessier-Lavigne M., Stein E. DSCAM is a netrin receptor that collaborates with DCC in mediating turning responses to netrin-1. Cell 2008, 133:1241-1254.
45. Matsumoto Y., Irie F., Inatani M., Tessier-Lavigne M., Yamaguchi Y. Netrin-1/DCC signaling in commissural axon guidance requires cell-autonomous expression of heparan sulfate. J. Neurosci. 2007, 27:4342-4350.
46. McCrea D.A., Rybak I.A. Organization of mammalian locomotor rhythm and pattern generation. Brain Res. Rev. 2008, 57:134-146.
47. Meriane M., Tcherkezian J., Webber C.A., Danek E.I., Triki I., McFarlane S., Bloch-Gallego E., Lamarche-Vane N. Phosphorylation of DCC by Fyn mediates Netrin-1 signaling in growth cone guidance. J. Cell Biol. 2004, 167:687-698.
48. Moran-Rivard L., Kagawa T., Saueressig H., Gross M.K., Burrill J., Goulding M. Evx1 is a postmitotic determinant of v0 interneuron identity in the spinal cord. Neuron 2001, 29:385-399.
49. Müller T., Brohmann H., Pierani A., Heppenstall P.A., Lewin G.R., Jessell T.M., Birchmeier C. The homeodomain factor lbx1 distinguishes two major programs of neuronal differentiation in the dorsal spinal cord. Neuron 2002, 34:551-562.
50. Nissen U.V., Mochida H., Glover J.C. Development of projection-specific interneurons and projection neurons in the embryonic mouse and rat spinal cord. J. Comp. Neurol. 2005, 483:30-47.
51. Pearson K.G. Common principles of motor control in vertebrates and invertebrates. Annu. Rev. Neurosci. 1993, 16:265-297.
52. Pierani A., Moran-Rivard L., Sunshine M.J., Littman D.R., Goulding M., Jessell T.M. Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 2001, 29:367-384.
53. Quinlan K.A., Kiehn O. Segmental, synaptic actions of commissural interneurons in the mouse spinal cord. J. Neurosci. 2007, 27:6521-6530.
54. Rabe N., Gezelius H., Vallstedt A., Memic F., Kullander K. Netrin-1-dependent spinal interneuron subtypes are required for the formation of left-right alternating locomotor circuitry. J. Neurosci. 2009, 29:15642-15649.
55. Ruiz de Almodovar C., Fabre P.J., Knevels E., Coulon C., Segura I., Haddick P.C.G., Aerts L., Delattin N., Strasser G., Oh W.-J., Lange C., Vinckier S., Haigh J., Fouquet C., Gu C., Alitalo K., Castellani V., Tessier-Lavigne M., Chedotal A., Charron F., Carmeliet P. VEGF mediates commissural axon chemoattraction through its receptor Flk1. Neuron 2011, 70:966-978.
56. Saueressig H., Burrill J., Goulding M. Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 1999, 126:4201-4212.
57. Serafini T., Colamarino S.A., Leonardo E.D., Wang H., Beddington R., Skarnes W.C., Tessier-Lavigne M. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 1996, 87:1001-1014.
58. Serafini T., Kennedy T.E., Galko M.J., Mirzayan C., Jessell T.M., Tessier-Lavigne M. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 1994, 78:409-424.
59. Soffe S.R., Clarke J.D., Roberts A. Activity of commissural interneurons in spinal cord of Xenopus embryos. J. Neurophysiol. 1984, 51:1257-1267.
60. Srour M., Rivière J.-B., Pham J.M.T., Dubé M.-P., Girard S., Morin S., Dion P.A., Asselin G., Rochefort D., Hince P., Diab S., Sharafaddinzadeh N., Chouinard S., Théoret H., Charron F., Rouleau G.A. Mutations in DCC cause congenital mirror movements. Science 2010, 328:592.
61. Stein E., Tessier-Lavigne M. Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 2001, 291:1928-1938.
62. Stein E., Zou Y., Poo M., Tessier-Lavigne M. Binding of DCC by netrin-1 to mediate axon guidance independent of adenosine A2B receptor activation. Science 2001, 291:1976-1982.
63. Stokke M.F., Nissen U.V., Glover J.C., Kiehn O. Projection patterns of commissural interneurons in the lumbar spinal cord of the neonatal rat. J. Comp. Neurol. 2002, 446:349-359.
64. Wallén-Mackenzie A., Gezelius H., Thoby-Brisson M., Nygård A., Enjin A., Fujiyama F., Fortin G., Kullander K. Vesicular glutamate transporter 2 is required for central respiratory rhythm generation but not for locomotor central pattern generation. J. Neurosci. 2006, 26:12294-12307.
65. Wegmeyer H., Egea J., Rabe N., Gezelius H., Filosa A., Enjin A., Varoqueaux F., Deininger K., Schnütgen F., Brose N., Klein R., Kullander K., Betz A. EphA4-dependent axon guidance is mediated by the RacGAP alpha2-chimaerin. Neuron 2007, 55:756-767.
66. Wilson S.I., Shafer B., Lee K.J., Dodd J. A molecular program for contralateral trajectory: Rig-1 control by LIM homeodomain transcription factors. Neuron 2008, 59:413-424.
67. Xie Y., Ding Y., Hong Y., Feng Z., Navarre S., Xi C., Zhu X., Wang C., Ackerman S., Kozlowski D., Mei L., Xiong W. Phosphatidylinositol transfer protein-alpha in netrin-1-induced PLC signalling and neurite outgrowth. Nat. Cell Biol. 2005, 7:1124-1132.
68. Yu T.W., Hao J.C., Lim W., Tessier-Lavigne M., Bargmann C.I. Shared receptors in axon guidance: SAX-3/Robo signals via UNC-34/Enabled and a Netrin-independent UNC-40/DCC function. Nat. Neurosci. 2002, 5:1147-1154.
69. Zhang Y., Narayan S., Geiman E., Lanuza G.M., Velasquez T., Shanks B., Akay T., Dyck J., Pearson K., Gosgnach S., Fan C.-M., Goulding M. V3 spinal neurons establish a robust and balanced locomotor rhythm during walking. Neuron 2008, 60:84-96.