Motor axon guidance of the mammalian trochlear and phrenic nerves: Dependence on the netrin receptor Unc5c and modifier loci

Journal of Neuroscience

Volumn 26, Issue 21, 2006, Pages 5756-5766

  Burgess, Robert W ^a   Jucius, Thomas J ^a   Ackerman, Susan L ^a,b  

^a JACKSON LABORATORY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Genetic background; Modifier gene; Mouse; Ophthalmic; QTL; rcm; Trigeminal; Unc5h3

Indexed keywords

LIGAND; NEOGENIN; NERVE PROTEIN; NETRIN; NETRIN 1; PROTEIN UNC5C; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; NERVE GROWTH FACTOR RECEPTOR; NETRIN RECEPTORS; UNC5C PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHROMOSOME 17; CONTROLLED STUDY; DIAPHRAGM; EMBRYO; FEMALE; GENE LOCUS; GENE MUTATION; GENE REPRESSION; GENOME; HYBRID; IMMUNOHISTOCHEMISTRY; INBRED STRAIN; INNERVATION; LETHALITY; MALE; MAMMAL; MOTOR NERVE; MOUSE; MUTATION; NERVE FIBER; NERVE GROWTH; NERVE MALFORMATION; NERVE PROJECTION; NEWBORN; NONHUMAN; PHENOTYPE; PHRENIC NERVE; PRIORITY JOURNAL; RESPIRATORY DISTRESS; SIGNAL TRANSDUCTION; TROCHLEAR NERVE; ANIMAL; C57BL MOUSE; GENETICS; METABOLISM; MOTONEURON; QUANTITATIVE TRAIT LOCUS; ULTRASTRUCTURE;

ANIMALS; AXONS; MICE; MICE, INBRED C57BL; MOTOR NEURONS; PHENOTYPE; PHRENIC NERVE; QUANTITATIVE TRAIT LOCI; RECEPTORS, CELL SURFACE; RECEPTORS, NERVE GROWTH FACTOR; TROCHLEAR NERVE;

EID: 33744994347     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0736-06.2006     Document Type: Article

References (53)

1. Ackerman SL, Kozak LP, Przyborski SA, Rund LA, Boyer BB, Knowles BB (1997) The mouse rostral cerebellar malformation gene encodes an UNC-5-like protein. Nature 386:838-842.
2. Barallobre MJ, Pascual M, Del Rio JA, Soriano E (2005) The netrin family of guidance factors: emphasis on netrin-1 signalling. Brain Res Brain Res Rev 49:22-47.
3. Bloch-Gallego E, Ezan F, Tessier-Lavigne M, Sotelo C (1999) Floor plate and netrin-1 are involved in the migration and survival of inferior olivary neurons. J Neurosci 19:4407-4420.
4. Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889-890.
5. Burgess RW, Peterson KA, Johnson MJ, Roix JJ, Welsh IC, O'Brien TP (2004) Evidence for a conserved function in synapse formation reveals Phr1 as a candidate gene for respiratory failure in newborn mice. Mol Cell Biol 24:1096-1105.
6. Chan SS, Zheng H, Su MW, Wilk R, Killeen MT, Hedgecock EM, Culotti JG (1996) UNC-40, a C. elegans homolog of DCC (Deleted in colorectal cancer), is required in motile cells responding to UNC-6 netrin cues. Cell 87:187-195.
7. Chang C, Yu TW, Bargmann CI, Tessier-Lavigne M (2004) Inhibition of netrin-mediated axon attraction by a receptor protein tyrosine phosphatase. Science 305:103-106.
8. Chen H, Bagri A, Zupicich JA, Zou Y, Stoeckli E, Pleasure SJ, Lowenstein DH, Skarnes WC, Chédotal A, Tessier-Lavigne M (2000) Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections. Neuron 25:43-56.
9. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963-971.
10. Colamarino SA, Tessier-Lavigne M (1995) The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81:621-629.
11. Colavita A, Culotti JG (1998) Suppressors of ectopic UNC-5 growth cone steering identify eight genes involved in axon guidance in Caenorhabditis elegans. Dev Biol 194:72-85.
12. Coppola E, Pattyn A, Guthrie SC, Goridis C, Studer M (2005) Reciprocal gene replacements reveal unique functions for Phox2 genes during neural differentiation. EMBO J 24:4392-4403.
13. Fazeli A, Dickinson SL, Hermiston ML, Tighe RV, Steen RG, Small CG, Stoeckli ET, Keino-Masu K, Masu M, Rayburn H, Simons J, Bronson RT, Gordon JI, Tessier-Lavigne M, Weinberg RA (1997) Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386:796-804.
14. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
15. Finger JH, Bronson RT, Harris B, Johnson K, Przyborski SA, Ackerman SL (2002) The netrin 1 receptors Unc5h3 and Dcc are necessary at multiple choice points for the guidance of corticospinal tract axons. J Neurosci 22:10346-10356.
16. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, Merlie JP, Sanes JR (1996) Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85:525-535.
17. Giger RJ, Cloutier JF, Sahay A, Prinjha RK, Levengood DV, Moore SE, Pickering S, Simmons D, Rastan S, Walsh FS, Kolodkin AL, Ginty DD, Geppert M (2000) Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 25:29-41.
18. Goldowitz D, Hamre KM, Przyborski SA, Ackerman SL (2000) Granule cells and cerebellar boundaries: analysis of Unc5h3 mutant chimeras. J Neurosci 20:4129-4137.
19. Hedgecock EM, Culotti JG, Hall DH, Stern BD (1987) Genetics of cell and axon migrations in Caenorhabditis elegans. Development 100:365-382.
20. Hedgecock EM, Culotti JG, Hall DH (1990) 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 2:61-85.
21. Hong K, Hinck L, Nishiyama M, Poo MM, Tessier-Lavigne M, Stein E (1999) A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 97:927-941.
22. Irving C, Malhas A, Guthrie S, Mason I (2002) Establishing the trochlear motor axon trajectory: role of the isthmic organiser and Fgf8. Development 129:5389-5398.
23. Keino Masu K, Masu M, Hinck L, Leonardo ED, Chan SS, Culotti JG, Tessier-Lavigne M (1996) Deleted in colorectal cancer (DCC) encodes a netrin receptor. Cell 87:175-185.
24. Keleman K, Dickson BJ (2001) Short- and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron 32:605-617.
25. Kitsukawa T, Shimizu M, Sanbo M, Hirata T, Taniguchi M, Bekku Y, Yagi T, Fujisawa H (1997) Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19:995-1005.
26. Koch M, Murrell JR, Hunter DD, Olson PF, Jin W, Keene DR, Brunken WJ, Burgeson RE (2000) A novel member of the netrin family, beta-netrin, shares homology with the beta chain of laminin: identification, expression, and functional characterization. J Cell Biol 151:221-234.
27. Kolodziej PA, Timpe LC, Mitchell KJ, Fried SR, Goodman CS, Jan LY, Jan YN (1996) Frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 87:197-204.
28. Labrador JP, O'Keefe D, Yoshikawa S, McKinnon RD, Thomas JB, Bashaw GJ (2005) The homeobox transcription factor Even-skipped regulates Netrin-receptor expression to control dorsal motor-axon projections in Drosophila. Curr Biol 15:1413-1419.
29. Leighton PA, Mitchell KJ, Goodrich LV, Lu X, Pinson K, Scherz P, Skarnes WC, Tessier-Lavigne M (2001) Defining brain wiring patterns and mechanisms through gene trapping in mice. Nature 410:174-179.
30. Lin W, Sanchez HB, Deerinck T, Morris JK, Ellisman M, Lee KF (2000) Aberrant development of motor axons and neuromuscular synapses in erbB2-deficient mice. Proc Natl Acad Sci USA 97:1299-1304.
31. Lin W, Burgess RW, Dominguez B, Pfaff SL, Sanes JR, Lee KF (2001) Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410:1057-1064.
32. Mitchell KJ, Doyle JL, Serafini T, Kennedy TE, Tessier-Lavigne M, Goodman CS, Dickson BJ (1996) Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 17:203-215.
33. Mitchell KJ, Pinson KI, Kelly OG, Brennan J, Zupicich J, Scherz P, Leighton PA, Goodrich LV, Lu X, Avery BJ, Tate P, Dill K, Pangilinan E, Wakenight P, Tessier-Lavigne M, Skarnes WC (2001) Functional analysis of secreted and transmembrane proteins critical to mouse development. Nat Genet 28:241-249.
34. Morris JK, Lin W, Hauser C, Marchuk Y, Getman D, Lee KF (1999) Rescue of the cardiac defect in ErbB2 mutant mice reveals essential roles of ErbB2 in peripheral nervous system development. Neuron 23:273-283.
35. Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF (1997) Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 124:4065-4075.
36. Przyborski SA, Knowles BB, Ackerman SL (1998) Embryonic phenotype of Unc5h3 mutant mice suggests chemorepulsion during the formation of the rostral cerebellar boundary. Development 125:41-50.
37. Puschel AW (1999) Divergent properties of mouse netrins. Mech Dev 83:65-75.
38. Sahay A, Molliver ME, Ginty DD, Kolodkin AL (2003) Semaphorin 3F is critical for development of limbic system circuitry and is required in neurons for selective CNS axon guidance events. J Neurosci 23:6671-6680.
39. Sanes JR, Lichtman JW (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2:791-805.
40. Schneider VA, Granato M (2003) Motor axon migration: a long way to go. Dev Biol 263:1-11.
41. Seaman C, Cooper HM (2001) Netrin-3 protein is localized to the axons of motor, sensory, and sympathetic neurons. Mech Dev 101:245-248.
42. Sen S, Churchill GA (2001) A statistical framework for quantitative trait mapping. Genetics 159:371-387.
43. Serafini T, Colamarino SA, Leonardo ED, Wang H, Beddington R, Skarnes WC, Tessier-Lavigne M (1996) Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87:1001-1014.
44. Shirasaki R, Mirzayan C, Tessier-Lavigne M, Murakami F (1996) Guidance of circumferentially growing axons by netrin-dependent and -independent floor plate chemotropism in the vertebrate brain. Neuron 17:1079-1088.
45. Srinivasan K, Strickland P, Valdes A, Shin GC, Hinck L (2003) Netrin-1/neogenin interaction stabilizes multipotent progenitor cap cells during mammary gland morphogenesis. Dev Cell 4:371-382.
46. Valenzuela DM, Stitt TN, DiStefano PS, Rojas E, Mattsson K, Compton DL, Nunez L, Park JS, Stark JL, Gies DR, et al (1995) Receptor tyrosine kinase specific for the skeletal muscle lineage: expression in embryonic muscle, at the neuromuscular junction, and after injury. Neuron 15:573-584.
47. Varela-Echavarria A, Tucker A, Puschel AW, Guthrie S (1997) Motor axon subpopulations respond differentially to the chemorepellents netrin-1 and semaphorin D. Neuron 18:193-207.
48. Wadsworth WG, Hedgecock EM (1996) Hierarchical guidance cues in the developing nervous system of C. elegans. BioEssays 18:355-362.
49. Wadsworth WG, Bhatt H, Hedgecock EM (1996) Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 16:35-46.
50. Wang H, Copeland NG, Gilbert DJ, Jenkins NA, Tessier-Lavigne M (1999) Netrin-3, a mouse homolog of human NTN2L, is highly expressed in sensory ganglia and shows differential binding to netrin receptors. J Neurosci 19:4938-4947.
51. Watanabe Y, Toyoda R, Nakamura H (2004) Navigation of trochlear motor axons along the midbrain-hindbrain boundary by neuropilin 2. Development 131:681-692.
52. Yang X, Arber S, William C, Li L, Tanabe Y, Jessell TM, Birchmeier C, Burden SJ (2001) Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 30:399-410.
53. Yin Y, Sanes JR, Miner JH (2000) Identification and expression of mouse netrin-4. Mech Dev 96:115-119.