Possible roles of robo1+ ensheathing cells in guiding dorsal-zone olfactory sensory neurons in mouse

Developmental Neurobiology

Volumn 73, Issue 11, 2013, Pages 828-840

  Aoki, Mari ^a   Takeuchi, Haruki ^a,b   Nakashima, Ai ^a,b   Nishizumi, Hirofumi ^a   Sakano, Hitoshi ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF FUKUI   (Japan)

Author keywords

Axonal projection; Glial cells; Olfactory neurons; Robo1

Indexed keywords

PROTEIN P75; RECEPTOR; ROBO1 RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; EMBRYO; GLIA CELL; MOUSE; NERVE FIBER; NERVE PROJECTION; NONHUMAN; OLFACTORY ENSHEATHING CELL; OLFACTORY NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL;

AXONAL PROJECTION; GLIAL CELLS; OLFACTORY NEURONS; ROBO1;

ANIMALS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEUROGENESIS; OLFACTORY BULB; OLFACTORY RECEPTOR NEURONS; RECEPTORS, IMMUNOLOGIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84885418497     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22103     Document Type: Article

References (45)

1. Astic L, Pellier-Monnin V, Godinot F. 1998. Spatio-temporal patterns of ensheathing cell differentiation in the rat olfactory system during development. Neuroscience 84:295-307.
2. Astic L, Saucier D, Holley A. 1987. Topographical relationships between olfactory receptor cells and glomerular foci in the rat olfactory bulb. Brain Res 424:144-152.
3. Au WW, Treloar HB, Greer CA. 2002. Sublaminar organization of the mouse olfactory bulb nerve layer. J Comp Neurol 446:68-80.
4. Brose K, Bland K, Wang K, Arnott D, Henzel W, Goodman C, Tessier-Lavigne M, et al. 1999. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell Mar 19:795-806.
5. 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 371:269-279.
6. 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 27:9094-9104.
7. Cho JH, Prince JE, Cutforth T, Cloutier JF. 2011. The pattern of glomerular map formation defines responsiveness to aversive odorants in mice. J Neurosci 31:7920-7926.
8. Chuah MI, West AK. 2002. Cellular and molecular biology of ensheathing cells. Microsc Res Tech 58:216-227.
9. Cloutier JF, Sahay A, Chang EC, Tessier-Lavigne M, Dulac C, Kolodkin AL, Ginty DD. 2004. Differential requirements for semaphorin 3F and Slit-1 in axonal targeting, fasciculation, and segregation of olfactory sensory neuron projections. J Neurosci 41:9087-9096.
10. Crandall JE, Dibble C, Butler D, Pays L, Ahmad N, Kostek C, Puschel AW, et al. 2000. Patterning of olfactory sensory connections is mediated by extracellular matrix proteins in the nerve layer of the olfactory bulb. J Neurobiol 45:195-206.
11. Farbman AI, Squinto LM. 1985. Early development of olfactory receptor cell axons. Brain Res 351:205-213.
12. Feinstein P, Bozza T, Rodriguez I, Vassalli A, Mombaerts P. 2004. Axon guidance of mouse olfactory sensory neurons by odorant receptors and the β2 adrenergic receptor. Cell 117:833-846.
13. Franceschini I, Barnett S. 1996. Low-affinity NGF-receptor and E-N-CAM expression define two types of olfactory nerve ensheathing cells that share a common lineage. 173:327-343.
14. Gall CM, Berschauer R, Isackson PJ. 1994. Seizures increase basic fibroblast growth factor mRNA in adult rat forebrain neurons and glia. Brain Res Mol Brain Res 21:190-205.
15. Gong Q, Bailey MS, Pixley SK, Ennis M, Liu W, Shipley MT. 1994. Localization and regulation of low affinity nerve growth factor receptor expression in the rat olfactory system during development and regeneration. J Comp Neurol 344:336-348.
16. Hirota S, Ito A, Morii E, Wanaka A, Tohyama M, Kitamura Y, Nomura S. 1992. Localization of mRNA for c-kit receptor and its ligand in the brain of adult rats: An analysis using in situ hybridization histochemistry. Brain Res Mol Brain Res 15:47-54.
17. Hivert B, Liu Z, Chuang CY, Doherty P, Sundaresan V. 2002. Robo1 and Robo2 are homophilic binding molecules that promote axonal growth. Mol Cell Neurosci 21:534-545.
18. Honore A, Le Corre S, Derambure C, Normand R, Duclos C, Boyer O, Marie JP, et al. 2012. Isolation, characterization, and genetic profiling of subpopulations of olfactory ensheathing cells from the olfactory bulb. Glia 60:404-413.
19. 2+-dependent cofilin activation and RhoA inhibition. J Cell Sci 124:186-197.
20. Kafitz KW, Greer CA. 1999. Olfactory ensheathing cells promote neurite extension from embryonic olfactory receptor cells in vitro. Glia 25:99-110.
21. Kaneko-Goto T, Yoshihara S, Miyazaki H, Yoshihara Y. 2008. BIG-2 mediates olfactory axon convergence to target glomeruli. Neuron 57:834-846.
22. Key B, Treloar HB, Wangerek L, Ford MD, Nurcombe V. 1996. Expression and localization of FGF-1 in the developing rat olfactory system. J Comp Neurol 366:197-206.
23. Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, et al. 2007. Innate versus learned odour processing in the mouse olfactory bulb. Nature 450:503-508.
24. Kott JN, Westrum LE, Raines EW, Sasahara M, Ross R. 1994. Olfactory ensheathing glia and platelet-derived growth factor B-chain reactivity in the transplanted rat olfactory bulb. Int J Dev Neurosci 12:315-323.
25. Liu KL, Chuah MI, Lee KK. 1995. Soluble factors from the olfactory bulb attract olfactory Schwann cells. J Neurosci 15:990-1000.
26. Long H, Sabatier C, Ma L, Plump A, Yuan W, Ornitz DM, Tamada A, et al. 2004. Conserved roles for Slit and Robo proteins in midline commissural axon guidance. Neuron 42:213-223.
27. Miller AM, Treloar HB, Greer CA. 2010. Composition of the migratory mass during development of the olfactory nerve. J Comp Neurol 518:4825-4841.
28. Miragall F, Kadmon G, Schachner M. 1989. Expression of L1 and N-CAM cell adhesion molecules during development of the mouse olfactory system. Dev Biol 135:272-286.
29. Miyamichi K, Serizawa S, Kimura HM, Sakano H. 2005. Continuous and overlapping expression domains of odorant receptor genes in the olfactory epithelium determine the dorsal/ventral positioning of glomeruli in the olfactory bulb. J Neurosci 25:3586-3592.
30. Miyasaka N, Sato Y, Yeo SY, Hutson LD, Chien CB, Okamoto H, Yoshihara Y. 2005. Robo2 is required for establishment of a precise glomerular map in the zebrafish olfactory system. Development 132:1283-1293.
31. Nguyen Ba-Charvet KT, Brose K, Marillat V, Kidd T, Goodman CS, Tessier-Lavigne M, Sotelo C, et al. 1999. Slit2-Mediated chemorepulsion and collapse of developing forebrain axons. Neuron 22:463-473.
32. 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 28:4244-4249.
33. Norlin EM, Alenius M, Gussing F, Hägglund M, Vedin V, Bohm S. 2001. Evidence for gradients of gene expression correlating with zonal topography of the olfactory sensory map. Mol Cell Neurosci 18:283-295.
34. Puche AC, Key B. 1995. Identification of cells expressing galectin-1, a galactose-binding receptor, in the rat olfactory system. J Comp Neurol 357:513-523.
35. Raisman G. 1985. Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 14:237-254.
36. Ramon-Cueto A, Perez J, Nieto-Sampedro M. 1993. In vitro enfolding of olfactory neurites by p75 NGF receptor positive ensheathing cells from adult rat olfactory bulb. Eur J Neurosci 5:1172-1180.
37. Sakano H. 2010. Neural map formation in the mouse olfactory system. Neuron 67:530-542.
38. Schwarting GA, Kostek C, Ahmad N, Dibble C, Pays L, Puschel AW. 2000. Semaphorin 3A is required for guidance of olfactory axons in mice. J Neurosci 20:7691-7697.
39. Serizawa S, Miyamichi K, Takeuchi H, Yamagishi Y, Suzuki M, Sakano H. 2006. A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting. Cell 127:1057-1069.
40. Takeuchi H, Inokuchi K, Aoki M, Suto F, Tsuboi A, Matsuda I, Suzuki M, et al. 2010. Sequential arrival and graded secretion of Sema3F by olfactory neuron axons specify map topography at the bulb. Cell 141:1056-1067.
41. Treloar H, Tomasiewicz H, Magnuson T, Key B. 1997. The central pathway of primary olfactory axons is abnormal in mice lacking the N-CAM-180 isoform. J Neurobiol 32:643-658.
42. Tsuboi A, Yoshihara S, Yamazaki N, Kasai H, Asai-Tsuboi H, Komatsu M, Serizawa S, et al. 1999. Olfactory neurons expressing closely linked and homologous odorant receptor genes tend to project their axons to neighboring glomeruli on the olfactory bulb. J Neurosci 19:8409-8418.
43. Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall LB, Axel R. 1994. Topographic organization of sensory projections to the olfactory bulb. Cell 79:981-991.
44. Walz A, Rodriguez I, Mombaerts P. 2002. Aberrant sensory innervation of the olfactory bulb in neuropilin-2 mutant mice. J Neurosci 22:4025-4035.
45. Yoshihara Y, Kawasaki M, Tamada A, Fujita H, Hayashi H, Kagamiyama H, Mori K. 1997. OCAM: A new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons. J Neurosci 17:5830-5842.