Developmental regulation of neural map formation in the mouse olfactory system

Developmental Neurobiology

Volumn 75, Issue 6, 2015, Pages 594-607

  Nishizumi, Hirofumi ^a   Sakano, Hitoshi ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF FUKUI   (Japan)

Author keywords

Axonal projection; Cyclic AMP; Neural map; Odorant receptors; Olfactory sensory neurons; Receptor baseline activity

Indexed keywords

CYCLIC AMP; TRANSCRIPTION FACTOR; G PROTEIN COUPLED RECEPTOR; OLFACTORY RECEPTOR;

ALLELE; ARTICLE; CHROMATIN STRUCTURE; CONFORMATIONAL TRANSITION; DNA RECOMBINATION; EMBRYO DEVELOPMENT; GENE CLUSTER; GENE CONVERSION; GENE EXPRESSION; GENE LOCUS; GENE PRODUCT; GENE TRANSLOCATION; GLOMERULAR STRUCTURE; NEGATIVE FEEDBACK; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; OLFACTORY EPITHELIUM; OLFACTORY NERVE; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CONFORMATION; REGULATOR GENE; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; AXON; BRAIN MAPPING; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE; MUTATION; OLFACTORY RECEPTOR; OLFACTORY RECEPTOR NEURON; PHYSIOLOGY;

ANIMALS; AXONS; BRAIN MAPPING; MICE; MUTATION; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, ODORANT; SIGNAL TRANSDUCTION;

EID: 84929516017     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.22268     Document Type: Article

References (73)

1. 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.
2. Bailey MS, Puche AC, Shipley MT. 1999. Development of the olfactory bulb: Evidence for glia-neuron interactions in glomerular formation. J Comp Neurol 415:423-448.
3. Ballesteros JA, Jensen AD, Liapakis G, Rasmussen SG, Shi L, Gether U, Javitch JA. 2001. Activation of the β 2-adrenergic receptor involves disruption of an ionic lock between the cytoplasmic ends of transmembrane segments 3 and 6. J Biol Chem 276:29171-29177.
4. Barnea G, O'Donnell S, Mancia F, Sun X, Nemes A, Mendelsohn M, Axel R. 2004. Odorant receptors on axon termini in the brain. Science 304:1468.
5. olf are anosmic. Neuron 20:69-81.
6. Brunet LJ, Gold GH, Ngai J. 1996. General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17:681-693.
7. Buck L, Axel R. 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175-187.
8. Chess A, Simon I, Cedar H, Axel R. 1994. Allelic inactivation regulates olfactory receptor gene expression. Cell 78:823-834.
9. 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.
10. Clowney EJ, LeGros MA, Mosley CP, Clowney FG, Markenskoff-Papadimitriou EC, Myllys M, Barnea G, et al. 2012. Nuclear aggregation of olfactory receptor genes governs their monogenic expression. Cell 151:724-737.
11. Dalton RP, Lyons DB, Lomvardas S. 2013. Co-opting the unfolded protein response to elicit olfactory receptor feedback. Cell 155:321-332.
12. Duggan CD, DeMaria S, Baudhuin A, Stafford D, Ngai J. 2008. Foxg1 is required for development of the vertebrate olfactory system. J Neurosci 28:5229-5239.
13. Eggan K, Baldwin K, Tackett M, Osborne J, Gogos J, Chess A, Axel R, et al. 2004. Mice cloned from olfactory sensory neurons. Nature 428:44-49.
14. 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.
15. Feinstein P, Mombaerts P. 2004. A contextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell 117:817-831.
16. Fuss SH, Omura M, Mombaerts P. 2007. Local and cis effects of the H element on expression of odorant receptor genes in mouse. Cell 130:373-384.
17. Hirota J, Mombaerts P. 2004. The LIM-homeodomain protein Lhx2 is required for complete development of mouse olfactory sensory neurons. Proc Natl Acad Sci USA 101:8751-8755.
18. Ishii T, Serizawa S, Kohda A, Nakatani H, Shiroishi T, Okumura K, Iwakura Y, et al. 2001. Monoallelic expression of the odourant receptor gene and axonal projection of olfactory sensory neurons. Genes Cells 6:71-78.
19. Imai T, Suzuki M, Sakano H. 2006. Odorant receptor-derived cAMP signals direct axonal targeting. Science 314:657-661.
20. Imai, T, Yamazaki, T, Kobayakawa, R, Kobayakawa, K, Abe, T, Suzuki, M., Sakano, H. 2009. Pre-target axon sorting establishes the neural map topography. Science 325:585-590.
21. Khan M, Vaes E, Mombaerts P. 2011. Regulation of the probability of mouse odorant receptor gene choice. Cell 147:907-921.
22. Kobilka BK, Deupi X. 2007. Conformational complexity of G-protein coupled receptors. Trends Pharmacol Sci 28:397-406.
23. Lemke G, Reber M. 2005. Retinotectal mapping: new insights from molecular genetics. Annu Rev Cell Dev Biol 21:551-580.
24. Lewcock JW, Reed RR. 2004. A feedback mechanism regulates monoallelic odorant receptor expression. Proc Natl Acad Sci USA 101:1069-1074.
25. Li J, Ishii T, Feinstein P, Mombaerts P. 2004. Odorant receptor gene choice is reset by nuclear transfer from mouse olfactory sensory neurons. Nature 428:393-399.
26. Lin DM, Wang F, Lowe G, Gold GH, Axel R, Ngai J, Brunet L. 2000. Formation of precise connections in the olfactory bulb occurs in the absence of odorant-evoked neuronal activity. Neuron 26:69-80.
27. Lomvardas S, Barnea G, Pisapia DJ, Mendelsohn M, Kirkland J, Axel R. 2006. Interchromosomal interactions and olfactory receptor choice. Cell, 126:403-413.
28. Luo L, Flanagan JG. 2007. Development of continuous and discrete neural maps. Neuron 56:284-300.
29. Lyons DB, Allen WE, Goh T, Tsai L, Barnea G, Lomvardas S. 2013. An epigenetic trap stabilizes singular olfactory receptor expression. Cell 154:325-336.
30. Magklara A, Yen A, Colquitt BM, Clowney EJ, Allen W, Markenscoff-Papadimitriou E, Evans ZA, et al. 2011. An epigenetic signature for monoallelic olfactory receptor expression. Cell 145:555-570.
31. Malnic B, Hirono J, Sato T, Buck LB. 1999. Combinatorial receptor codes for odors. Cell 96:713-723.
32. Markenscoff-Papadimitriou E, Allen WE, Colquitt BM, Goh T, Murphy KK, Monahan K, Mosley CP, et al. 2014. Enhancer interaction networks as a means for singular olfactory receptor expression. Cell 159:543-557.
33. McLaughlin T, O'Leary DD. 2005. Molecular gradients and development of retinotopic maps. Annu Rev Neurosci 28:327-355.
34. Michaloski JS, Galante PA, Malnic B. 2006. Identification of potential regulatory motifs in odorant receptor genes by analysis of promoter sequences. Genome Res 16:1091-1098.
35. 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.
36. Mombaerts P. 2006. Axonal wiring in the mouse olfactory system. Annu Rev Cell Dev Biol 22:713-737.
37. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, et al. 1996. Visualizing an olfactory sensory map. Cell 87:675-686.
38. Mori K, Sakano H. 2011. How is the olfactory map formed and interpreted in the mammalian brain? Annu Rev Neurosci 34:467-499.
39. Nakashima A, Takeuchi H, Imai T, Saito H, Kiyonari H, Abe T, Chen M, et al. 2013. Agonist-independent GPCR activity regulates axon targeting of olfactory sensory neurons. Cell 154:1314-1325.
40. 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.
41. Nishizumi H, Kumasaka K, Inoue N, Nakashima A, Sakano H. 2007. Deletion of the core-H region in mice abolishes the expression of three proximal odorant receptor genes in cis. Proc Natl Acad Sci USA 104:20067-20072.
42. 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.
43. O'Dowd BF, Hnatowich M, Regan JW, Leader WM, Caron MG, Lefkowitz RJ. 1988. Site-directed mutagenesis of the cytoplasmic domains of the human β 2-adrenergic receptor. Localization of regions involved in G protein-receptor coupling. J Biol Chem 263:15985-15992.
44. Petersen CC. 2007. The functional organization of the barrel cortex. Neuron 56:339-355.
45. Rasmussen SG, Choi HJ, Fung JJ, Pardon E, Casarosa P, Chae PS, Devree BT, et al. 2011a. Structure of a nanobody-stabilized active state of the β(2) adrenoceptor. Nature 469:175-180.
46. Rasmussen SG, DeVree BT, Zou Y, Kruse AC, Chung KY, Kobilka TS, Thian FS, et al. 2011b. Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477:549-555.
47. Reisert J. 2010. Origin of basal activity in mammalian olfactory receptor neurons. J Gen Physiol 136:529-540.
48. Ressler KJ, Sullivan SL, Buck LB. 1993. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73:597-609.
49. Ressler KJ, Sullivan SL, Buck LB. 1994. Information coding in the olfactory system: Evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79:1245-1255.
50. Rodriguez I. 2013. Singular expression of olfactory receptor genes. Cell 155:274-277.
51. Rothman A, Feinstein P, Hirota J, Mombaerts P. 2005. The promoter of the mouse odorant receptor gene M71. Mol Cell Neurosci 28:535-546.
52. Saito H, Chi Q, Zhuang H, Matsunami H, Mainland JD. 2009. Odor coding by a Mammalian receptor repertoire. Sci Signal 2:ra9.
53. Sakano H. 2010. Neural map formation in the mouse olfactory system. Neuron 67:530-542.
54. Satoda M, Takagi S, Ohta K, Hirata T, Fujisawa H. 1995. Differential expression of two cell surface proteins, neuropilin and plexin, in Xenopus olfactory axon subclasses. J Neurosci 15:942-955.
55. Savarese TM, Fraser CM. 1992. In vitro mutagenesis and the search for structure-function relationships among G protein-coupled receptors. Biochem J 283:1-19.
56. Serizawa S, Ishii T, Nakatani H, Tsuboi A, Nagawa F, Asano M, Sudo K, Sakagami J, Sakano H, Ijiri T, Matsuda Y, Suzuki M, Yamamori T, Iwakura Y, Sakano H. 2000. Mutually exclusive expression of odorant receptor transgenes. Nat Neurosci 3:687-693.
57. Serizawa S, Miyamichi K, Nakatani H, Suzuki M, Saito M, Yoshihara Y, Sakano H. 2003. Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 302:2088-2094.
58. Serizawa S, Miyamichi K, Sakano H. 2004. One neuron - one receptor rule in the mouse olfactory system. Trends Genet 20:648-653.
59. 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.
60. Shykind BM, Rohani SC, O'Donnell S, Nemes A, Mendelsohn M, Sun Y, Axel R, Barnea G. 2004. Gene switching and the stability of odorant receptor gene choice. Cell 1174:801-815.
61. Spilianakis CG, Lalioti MD, Town T, Lee GR, Flavell RA. 2005. Interchromosomal associations between alternatively expressed loci. Nature 435:637-645.
62. Stephan AB, Shum EY, Hirsh S, Cygnar KD, Reisert J, Zhao H. 2009. ANO2 is the cilial calcium-activated chloride channel that may mediate olfactory amplification. Proc Natl Acad Sci USA 106:11776-11781.
63. Strotmann J, Levai O, Fleischer J, Schwarzenbacher K, Breer H. 2004. Olfactory receptor proteins in axonal processes of chemosensory neurons. J Neurosci 24:7754-7761.
64. 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.
65. Tsuboi A, Miyazaki T, Imai T, Sakano H. 2006. Olfactory sensory neurons expressing class I odorant receptors converge their axons on an antero-dorsal domain of the olfactory bulb in the mouse. Eur J Neurosci 23:1436-1444.
66. Vassalli A1, Rothman A, Feinstein P, Zapotocky M, Mombaerts P. 2002. Minigenes impart odorant receptor-specific axon guidance in the olfactory bulb. Neuron 15:681-696.
67. Vassar R, Ngai J, Axel R. 1993. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74:309-318.
68. 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.
69. Wang F, Nemes A, Mendelsohn M, Axel R. 1998. Odorant receptors govern the formation of a precise topographic map. Cell 93:47-60.
70. Wong ST1, Trinh K, Hacker B, Chan GC, Lowe G, Gaggar A, Xia Z, et al. 2000. Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27:487-497.
71. Yu CR, Power J, Barnea G, O'Donnell S, Brown HE, Osborne J, Axel R, Gogos JA. 2004. Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553-566.
72. Zhao H, Reed RR. 2001. X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 104:651-660.
73. Zheng C, Feinstein P, Bozza T, Rodriguez I, Mombaerts P. 2000. Peripheral olfactory projections are differentially affected in mice deficient in a cyclic nucleotide-gated channel subunit. Neuron 26:81-91.