Trio controls the mature organization of neuronal clusters in the hindbrain

Journal of Neuroscience

Volumn 27, Issue 39, 2007, Pages 10323-10332

  Backer, Stéphanie ^a,b   Hidalgo Sánchez, Matías ^a,b   Offner, Nicolas ^a,b   Portales Casamar, Elodie ^c   Debant, Anne ^c   Fort, Philippe ^c   Gauthier Rouvière, Cécile ^c   Bloch Gallego, Evelyne ^a,b  

^a INSTITUT COCHIN   (France)

^b INSERM   (France)

^c Centre National de la Recherche Scientifique   (France)

Author keywords

Cadherin 11; In situ hybridization; Mice; Motoneurons; Olivary neurons; Rho GTPases

Indexed keywords

CADHERIN; CADHERIN 11; FRAGILE X MENTAL RETARDATION PROTEIN; PROTEIN CDC42; PROTEIN RHOG; PROTEIN S 100; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CLUSTER ANALYSIS; CONTROLLED STUDY; IN VIVO STUDY; INFERIOR OLIVE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHOMBENCEPHALON;

ANIMALS; CADHERINS; FACIAL NERVE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MICE; MOTOR NEURONS; NEUROPEPTIDES; OLIVARY NUCLEUS; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; RAC GTP-BINDING PROTEINS; RHOMBENCEPHALON;

EID: 34848902986     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1102-07.2007     Document Type: Article

References (49)

1. Azizi SA, Woodward DJ (1987) Inferior olivary nuclear complex of the rat: morphology and comments on the principles of organization within the olivocerebellar system. J Comp Neurol 263:467-484.
2. Backer S, Sakurai T, Grumet M, Sotelo C, Bloch-Gallego E (2002) Nr-CAM and TAG-1 are expressed in distinct populations of developing precerebellar and cerebellar neurons. Neuroscience 113:743-748.
3. Barrett C, Guthrie S (2001) Expression patterns of the netrin receptor UNC5H1 among developing motor neurons in the embryonic rat hindbrain. Mech Dev 106:163-166.
4. Bateman J, Van Vactor D (2001) The Trio family of guanine-nucleotide- exchange factors: regulators of axon guidance. J Cell Sci 114:1973-1980.
5. Bellanger JM, Lazaro JB, Diriong S, Fernandez A, Lamb N, Debant A (1998) The two guanine nucleotide exchange factor domains of Trio link the Rac1 and the RhoA pathways in vivo. Oncogene 16:147-152.
6. 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.
7. Bourrat F, Sotelo C (1990) Early development of the rat precerebellar system: migratory routes, selective aggregation and neuritic differentiation of the inferior olive and lateral reticular nucleus neurons. An overview. Arch Ital Biol 128:151-170.
8. Bourrat F, Sotelo C (1991) Relationships between neuronal birthdates and cytoarchitecture in the rat inferior olivary complex. J Comp Neurol 313:509-521.
9. Braga V (2002) Cell-cell adhesion and signalling. Curr Opin Cell Biol 14:546-556.
10. Causeret F, Hidalgo-Sanchez M, Fort P, Backer S, Popoff MR, Gauthier-Rouviere C, Bloch-Gallego E (2004) Distinct roles of Rac1/Cdc42 and Rho/Rock for axon outgrowth and nucleokinesis of precerebellar neurons toward netrin 1. Development 131:2841-2852.
11. Charrasse S, Causeret M, Comunale F, Bonet-Kerrache A, Gauthier-Rouviere C (2003) Rho GTPases and cadherin-based cell adhesion in skeletal muscle development. J Muscle Res Cell Motil 24:309-313.
12. Charrasse S, Comunale F, Fortier M, Portales-Casamar E, Debant A, Gauthier-Rouviere C (2007) M-Cadherin activates Rac1 GTPase through the Rho-GEF Trio during myoblast fusion. Mol Biol Cell 18:1734-1743.
13. Chedotal A, Pourquie O, Ezan F, San Clemente H, Sotelo C (1996) BEN as a presumptive target recognition molecule during the development of the olivocerebellar system. J Neurosci 16:3296-3310.
14. Debant A, Serra-Pages C, Seipel K, O'Brien S, Tang M, Park SH, Streuli M (1996) The multidomain protein Trio binds the LAR transmembrane tyrosine phosphatase, contains a protein kinase domain, and has separate rac-specific and rho-specific guanine nucleotide exchange factor domains. Proc Natl Acad Sci USA 93:5466-5471.
15. Erasmus JC, Braga VM (2006) Rho GTPase activation by cell-cell adhesion. Methods Enzymol 406:402-415.
16. Etienne-Manneville S, Hall A (2002) Rho GTPases in cell biology. Nature 420:629-635.
17. Forsthoefel DJ, Liebl EC, Kolodziej PA, Seeger MA (2005) The Abelson tyrosine kinase, the Trio GEF and Enabled interact with the Netrin receptor Frazzled in Drosophila. Development 132:1983-1994.
18. Garel S, Garcia-Dominguez M, Charnay P (2000) Control of the migratory pathway of facial branchiomotor neurones. Development 127:5297-5307.
19. Gauthier-Rouviere C, Vignal E, Meriane M, Roux P, Montcourier P, Fort P (1998) RhoG GTPase controls a pathway that independently activates Rac1 and Cdc42Hs. Mol Biol Cell 9:1379-1394.
20. Gilland E, Baker R (1993) Conservation of neuroepithelial and mesodermal segments in the embryonic vertebrate head. Acta Anat (Basel) 148:110-123.
21. Jossin Y (2004) Neuronal migration and the role of reelin during early development of the cerebral cortex. Mol Neurobiol 30:225-251.
22. Kaibuchi K, Kuroda S, Fukata M, Nakagawa M (1999) Regulation of cadherin-mediated cell-cell adhesion by the Rho family GTPases. Curr Opin Cell Biol 11:591-596.
23. Kimura Y, Matsunami H, Takeichi M (1996) Expression of cadherin-11 delineates boundaries, neuromeres, and nuclei in the developing mouse brain. Dev Dyn 206:455-462.
24. Ko J, Humbert S, Bronson RT, Takahashi S, Kulkarni AB, Li E, Tsai LH (2001) p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment. J Neurosci 21:6758-6771.
25. Lanier LM, Gertler FB (2000) From Abl to actin: Abl tyrosine kinase and associated proteins in growth cone motility. Curr Opin Neurobiol 10:80-87.
26. Lumsden A, Keynes R (1989) Segmental patterns of neuronal development in the chick hindbrain. Nature 337:424-428.
27. Manabe T, Togashi H, Uchida N, Suzuki SC, Hayakawa Y, Yamamoto M, Yoda H, Miyakawa T, Takeichi M, Chisaka O (2000) Loss of cadherin-11 adhesion receptor enhances plastic changes in hippocampal synapses and modifies behavioral responses. Mol Cell Neurosci 15:534-546.
28. Marillat V, Sabatier C, Failli V, Matsunaga E, Sotelo C, Tessier-Lavigne M, Chedotal A (2004) The slit receptor Rig-1/Robo3 controls midline crossing by hindbrain precerebellar neurons and axons. Neuron 43:69-79.
29. Marthiens V, Gavard J, Padilla F, Monnet C, Castellani V, Lambert M, Mege RM (2005) A novel function for cadherin-11 in the regulation of motor axon elongation and fasciculation. Mol Cell Neurosci 28:715-726.
30. McPherson CE, Eipper BA, Mains RE (2005) Multiple novel isoforms of Trio are expressed in the developing rat brain. Gene 347:125-135.
31. O'Brien SP, Seipel K, Medley QG, Bronson R, Segal R, Streuli M (2000) Skeletal muscle deformity and neuronal disorder in Trio exchange factor-deficient mouse embryos. Proc Natl Acad Sci USA 97:12074-12078.
32. Ohshima T, Ogawa M, Takeuchi K, Takahashi S, Kulkarni AB, Mikoshiba K (2002) Cyclin-dependent kinase 5/p35 contributes synergistically with Reelin/Dab1 to the positioning of facial branchiomotor and inferior olive neurons in the developing mouse hindbrain. J Neurosci 22:4036-4044.
33. Padilla F, Broders F, Nicolet M, Mege RM (1998) Cadherins M, 11, and 6 expression patterns suggest complementary roles in mouse neuromuscular axis development. Mol Cell Neurosci 11:217-233.
34. Pfaff SL, Mendelsohn M, Stewart CL, Edlund T, Jessell TM (1996) Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84:309-320.
35. Price SR, De Marco Garcia NV, Ranscht B, Jessell TM (2002) Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109:205-216.
36. Rossel M, Loulier K, Feuillet C, Alonso S, Carroll P (2005) Reelin signaling is necessary for a specific step in the migration of hindbrain efferent neurons. Development 132:1175-1185.
37. Saburi S, McNeill H (2005) Organising cells into tissues: new roles for cell adhesion molecules in planar cell polarity. Curr Opin Cell Biol 17:482-488.
38. Schiffmann SN, Bernier B, Goffinet AM (1997) Reelin mRNA expression during mouse brain development. Eur J Neurosci 9:1055-1071.
39. Steven R, Zhang L, Culotti J, Pawson T (2005) The UNC-73/Trio RhoGEF-2 domain is required in separate isoforms for the regulation of pharynx pumping and normal neurotransmission in C. elegans. Genes Dev 19:2016-2029.
40. Studer M, Lumsden A, Ariza-McNaughton L, Bradley A, Krumlauf R (1996) Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384:630-634.
41. Suzuki SC, Inoue T, Kimura Y, Tanaka T, Takeichi M (1997) Neuronal circuits are subdivided by differential expression of type-II classic cadherins in postnatal mouse brains. Mol Cell Neurosci 9:433-447.
42. Taniguchi H, Kawauchi D, Nishida K, Murakami F (2006) Classic cadherins regulate tangential migration of precerebellar neurons in the caudal hindbrain. Development 133:1923-1931.
43. Terashima T, Kishimoto Y, Ochiishi T (1993) Musculotopic organization of the facial nucleus of the reeler mutant mouse. Brain Res 617:1-9.
44. Vigorito E, Bell S, Hebeis BJ, Reynolds H, McAdam S, Emson PC, McKenzie A, Turner M (2004) Immunological function in mice lacking the Racrelated GTPase RhoG. Mol Cell Biol 24:719-729.
45. Wassef M, Chedotal A, Cholley B, Thomasset M, Heizmann CW, Sotelo C (1992) Development of the olivocerebellar projection in the rat. I. Transient biochemical compartmentation of the inferior olive. J Comp Neurol 323:519-536.
46. Wheelock MJ, Johnson KR (2003) Cadherins as modulators of cellular phenotype. Annu Rev Cell Dev Biol 19:207-235.
47. Wild JM, Zeigler HP (1980) Central representation and somatotopic organization of the jaw muscles within the facial and trigeminal nuclei of the pigeon (Columba livia). J Comp Neurol 192:175-201.
48. Xin X, Ferraro F, Back N, Eipper BA, Mains RE (2004) Cdk5 and Trio modulate endocrine cell exocytosis. J Cell Sci 117:4739-4748.
49. Yap AS, Kovacs EM (2003) Direct cadherin-activated cell signaling: a view from the plasma membrane. J Cell Biol 160:11-16.