The E3 ubiquitin ligase Mycbp2 genetically interacts with Robo2 to modulate axon guidance in the mouse olfactory system

Brain Structure and Function

Volumn 219, Issue 3, 2014, Pages 861-874

  James, G ^a   Key, B ^a   Beverdam, A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Axon guidance; Mycbp2; Olfactory; Robo

Indexed keywords

MYCBP2 PROTEIN; PROTEIN; ROBO2 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CARRIER PROTEIN; IMMUNOGLOBULIN RECEPTOR; MYCBP2 PROTEIN, MOUSE; ROBO2 PROTEIN, MOUSE; UBIQUITIN PROTEIN LIGASE;

ADULT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS CALLOSUM; EMBRYO; GENE INTERACTION; HETEROZYGOSITY; HISTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOUSE; NERVE CELL NECROSIS; NERVE FIBER; NISSL STAINING; NONHUMAN; NOSE CAVITY; OLFACTORY BULB; OLFACTORY SYSTEM; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; SENSORY NERVE CELL; STOP CODON; ANIMAL; CYTOLOGY; GENE REGULATORY NETWORK; GENETICS; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

CAENORHABDITIS ELEGANS; DANIO RERIO; MAMMALIA; MUS;

ANIMALS; AXONS; CARRIER PROTEINS; GENE REGULATORY NETWORKS; MICE; NEUROGENESIS; NEURONS; OLFACTORY BULB; OLFACTORY PATHWAYS; RECEPTORS, IMMUNOLOGIC; UBIQUITIN-PROTEIN LIGASES;

EID: 84902358481     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-013-0540-8     Document Type: Article

References (38)

1. Akins MR, Greer CA (2006) Axon behavior in the olfactory nerve reflects the involvement of catenin-cadherin mediated adhesion. J Comp Neurol 499(6):979-989 (Pubitemid 44892823)
2. Au WW, Treloar HB, Greer CA (2002) Sublaminar organization of the mouse olfactory bulb nerve layer. J Comp Neurol 446(1):68-80 (Pubitemid 34252851)
3. Berghard A, Hagglund AC, Bohm S, Carlsson L (2012) Lhx2-dependent specification of olfactory sensory neurons is required for successful integration of olfactory, vomeronasal, and GnRH neurons. Faseb J 26(8):3464-3472
4. Bloom AJ, Miller BR, Sanes JR, DiAntonio A (2007) The requirement for Phr1 in CNS axon tract formation reveals the corticostriatal boundary as a choice point for cortical axons. Genes Dev 21(20):2593-2606 (Pubitemid 47607670)
5. Borrell V, Cardenas A, Ciceri G, Galceran J, Flames N, Pla R, Nobrega-Pereira S, Garcia-Frigola C, Peregrin S, Zhao Z et al (2012) Slit/Robo signaling modulates the proliferation of central nervous system progenitors. Neuron 76(2):338-352
6. 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(3):1096-1105 (Pubitemid 38112173)
7. Cho JH, Lepine M, Andrews W, Parnavelas J, Cloutier JF (2007) Requirement for slit-1 and robo-2 in zonal segregation of olfactory sensory neuron axons in the main olfactory bulb. J Neurosci 27(34):9094-9104 (Pubitemid 47312056)
8. Cho JH, Prince JEA, Cutforth T, Cloutier JF (2011) The pattern of glomerular map formation defines responsiveness to aversive odorants in mice. J Neurosci 31(21):7920-7926
9. Cho JH, Kam JW, Cloutier JF (2012) Slits and Robo-2 regulate the coalescence of subsets of olfactory sensory neuron axons within the ventral region of the olfactory bulb. Dev Biol 371(2):269-279
10. Culican SM, Bloom AJ, Weiner JA, DiAntonio A (2009) Phr1 regulates retinogeniculate targeting independent of activity and ephrin-A signalling. Mol Cell Neurosci 41(3):304-312
11. Danciger E, Mettling C, Vidal M, Morris R, Margolis F (1989) Olfactory marker protein gene-its structure and olfactory neuron-specific expression in transgenic mice. Proc Natl Acad Sci USA 86(21):8565-8569 (Pubitemid 19286096)
12. Ekberg JAK, Amaya D, Chehrehasa F, Lineburg K, Claxton C, Windus LCE, Key B, Mackay-Sim A, St John JA (2011) OMPZsGreen fluorescent protein transgenic mice for visualisation of olfactory sensory neurons in vivo and in vitro. J Neurosci Methods 196(1):88-98
13. Engle EC (2010) Human genetic disorders of axon guidance, Cold Spring Harbor Perspectives in Biology 2(3)
14. Gussing F, Bohm S (2004) NQO1 activity in the main and the accessory olfactory systems correlates with the zonal topography of projection maps. Eur J Neurosci 19(9):2511-2518 (Pubitemid 38621848)
15. Hagarman JA, O'Brien TP (2009) An essential gene mutagenesis screen across the highly conserved piebald deletion region of mouse chromosome 14. Genesis 47(6):392-403
16. Hicke L (2001) Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2(3):195-201
17. Hirata T, Nakazawa M, Yoshihara S, Miyachi H, Kitamura K, Yoshihara Y, Hibi M (2006) Zinc-finger gene Fez in the olfactory sensory neurons regulates development of the olfactory bulb non-cell-autonomously. Development 133(8):1433-1443 (Pubitemid 43732957)
18. Holland S, Coste O, Zhang DD, Pierre SC, Geisslinger G, Scholich K (2011) The ubiquitin ligase MYCBP2 regulates transient receptor potential vanilloid receptor 1 (TRPV1) internalization through inhibition of p38 MAPK signaling. J Biol Chem 286(5):3671-3680
19. Kawabe H, Brose N (2011) The role of ubiquitination in nerve cell development. Nat Rev Neurosci 12(5):251-268
20. Key B, Akeson RA (1993) Distinct subsets of sensory olfactory neurons in mouse: possible role in the formation of the mosaic olfactory projection. J Comp Neurol 335(3):355-368 (Pubitemid 23260375)
21. Key B, St John J (2002) Axon navigation in the mammalian primary olfactory pathway: where to next? Chem Senses 27(3):245-260 (Pubitemid 34428955)
22. Lehman NL (2009) The ubiquitin proteasome system in neuropathology. Acta Neuropathol 118(3):329-347
23. Li HC, Kulkarni G, Wadsworth WG (2008a) RPM-1, a Caenorhabditis elegans protein that functions in presynaptic differentiation, negatively regulates axon outgrowth by controlling SAX-3/robo and UNC-5/UNC5 activity. J Neurosci 28(14):3595-3603
24. Li W, Bengtson MH, Ulbrich A, Matsuda A, Reddy VA, Orth A, Chanda SK, Batalov S, Joazeiro CAP (2008b) Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelle's dynamics and signaling. Plos One 3(1):e1487
25. Lipscomb BW, Treloar HB, Klenoff J, Greer CA (2003) Cell surface carbohydrates and glomerular targeting of olfactory sensory neuron axons in the mouse. J Comp Neurol 467(1):22-31 (Pubitemid 37339755)
26. Lopez-Bendito G, Flames N, Ma L, Fouquet C, Di Meglio T, Chedotal A, Tessier-Lavigne M, Marin O (2007) Robo1 and Robo2 cooperate to control the guidance of major axonal tracts in the mammalian forebrain. J Neurosci 27(13):3395-3407 (Pubitemid 46515124)
27. Lu WN, van Eerde AM, Fan XP, Quintero-Rivera F, Kulkarni S, Ferguson H, Kim HG, Fan YL, Xi QC, Li QG et al (2007) Disruption of ROBO2 is associated with urinary tract anomalies and confers risk of vesicoureteral reflux. Am J Hum Genet 80(4):616-632 (Pubitemid 46564400)
28. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87(4):675-686 (Pubitemid 26386941)
29. Myat A, Henry P, McCabe V, Flintoft L, Rotin D, Tear G (2002) Drosophila Nedd4, a ubiquitin ligase, is recruited by commissureless to control cell surface levels of the roundabout receptor. Neuron 35(3):447-459 (Pubitemid 34879945)
30. Nguyen-Ba-Charvet KT, Di Meglio T, Fouquet C, Chedotal A (2008) Robos and slits control the pathfinding and targeting of mouse olfactory sensory axons. J Neurosci 28(16):4244-4249
31. Po MD, Hwang C, Zhen M (2010) PHRs: bridging axon guidance, outgrowth and synapse development. Curr Opin Neurobiol 20(1):100-107
32. Simmons DG, Rawn S, Davies A, Hughes M, Cross JC (2008) Spatial and temporal expression of the 23 murine prolactin/placental lactogen-related genes is not associated with their position in the locus. Bmc Genomics 9:352
33. Sun W, Kim H, Moon Y (2010) Control of neuronal migration through rostral migration stream in mice. Anat Cell Biol 43(4):269-279
34. Takeuchi H, Inokuchi K, Aoki M, Suto F, Tsuboi A, Matsuda I, Suzuki M, Aiba A, Serizawa S, Yoshihara Y et al (2010) Sequential arrival and graded secretion of Sema3F by Olfactory neuron axons specify map topography at the bulb. Cell 141(6):1056-1067
35. Thrower JS, Hoffman L, Rechsteiner M, Pickart CM (2000) Recognition of the polyubiquitin proteolytic signal. EMBO J 19(1):94-102 (Pubitemid 30009229)
36. Treloar HB, Gabeau D, Yoshihara Y, Mori K, Greer CA (2003) Inverse expression of olfactory cell adhesion molecule in a subset of olfactory axons and a subset of mitral/tufted cells in the developing rat main olfactory bulb. J Comp Neurol 458(4):389-403 (Pubitemid 36337055)
37. Windus LCE, Claxton C, Allen CL, Key B, St John JA (2007) Motile membrane protrusions regulate cell-cell adhesion and migration of olfactory ensheathing glia. Glia 55(16):1708-1719 (Pubitemid 47612857)
38. Yuasa-Kawada J, Kinoshita-Kawada M, Wu G, Rao Y, Wu JY (2009) Midline crossing and slit responsiveness of commissural axons require USP33. Nat Neurosci 12(9):1087-1089