The worm's sense of smell: Development of functional diversity in the chemosensory system of Caenorhabditis elegans

Developmental Biology

Volumn 265, Issue 2, 2004, Pages 302-319

  Melkman, Tali ^a   Sengupta, Piali ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

C. elegans; Chemosensory system; Functional diversity

Indexed keywords

BIODIVERSITY; BRAIN DEVELOPMENT; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL REGENERATION; CHEMICAL ENVIRONMENT; DROSOPHILA; FLY; GENE EXPRESSION; MOLECULAR BIOLOGY; NEMATODE; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENSORY SYSTEM; WORM;

ANIMALIA; CAENORHABDITIS; CAENORHABDITIS ELEGANS;

EID: 0346654062     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2003.07.005     Document Type: Review

References (213)

1. Acampora D., Avantaggiato V., Tuorto F., Barone P., Reichert H., Finkelstein R., Simeone A. Murine Otx1 and Drosophila otd genes share conserved genetic functions required in invertebrate and vertebrate brain development. Development. 125:1998;1691-1702.
2. Acampora D., Avantaggiato V., Tuorto F., Briata P., Corte G., Simeone A. Visceral endoderm-restricted translation of Otx1 mediates recovery of Otx2 requirements for specification of anterior neural plate and normal gastrulation. Development. 125:1998;5091-5104.
3. Acampora D., Avantaggiato V., Tuorto F., Barone P., Perera M., Choo D., Wu D., Corte G., Simeone A. Differential transcriptional control as the major molecular event in generating Otx1-/- and Otx2-/- divergent phenotypes. Development. 126:1999;1417-1426.
4. Albert P.S., Riddle D.L. Developmental alterations in sensory neuroanatomy of the Caenorhabditis elegans dauer larva. J. Comp. Neurol. 219:1983;461-481.
5. Alenius M., Bohm S. Identification of a novel neural cell adhesion molecule-related gene with a potential role in selective axonal projection. J. Biol. Chem. 272:1997;26083-26086.
6. Altun-Gultekin Z., Andachi Y., Tsalik E.L., Pilgrim D., Kohara Y., Hobert O. A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23 controls cell fate specification of a defined interneuron class in C. elegans. Development. 128:2001;1951-1969.
7. Artavanis-Tsakonas S., Rand M.D., Lake R.J. Notch signaling: cell fate control and signal integration in development. Science. 284:1999;770-776.
8. Baier H., Rotter S., Korsching S. Connectional topography in the zebrafish olfactory system: random positions but regular spacing of sensory neurons projecting to an individual glomerulus. Proc. Natl. Acad. Sci. U. S. A. 91:1994;11646-11650.
9. Baran R., Aronoff R., Garriga G. The C. elegans homeodomain gene unc-42 regulates chemosensory and glutamate receptor expression. Development. 126:1999;2241-2251.
10. Bargmann C.I., Horvitz H.R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron. 7:1991;729-742.
11. Bargmann C.I., Horvitz H.R. Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science. 251:1991;1243-1246.
12. Bargmann C.I., Mori I. Chemotaxis and thermotaxis. Riddle D.S., Blumenthal T., Meyer B.J., Priess J.R. C. elegans II. 1997;717-737 Cold Spring Harbor Press, Cold Spring Harbor.
13. Bargmann C.I., Hartwieg E., Horvitz H.R. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell. 74:1993;515-527.
14. Barth A.L., Justice N.J., Ngai J. Asynchronous onset of odorant receptor expression in the developing zebrafish olfactory system. Neuron. 16:1995;23-34.
15. Baumeister R., Liu Y., Ruvkun G. Lineage-specific regulators couple cell lineage asymmetry to the transcription of the Caenorhabditis elegans POU gene unc-86 during neurogenesis. Genes Dev. 10:1996;1395-1410.
16. Bei Y., Hogan J., Berkowitz L.A., Soto M., Rocheleau C.E., Pang K.M., Collins J., Mello C.C. SRC-1 and Wnt signaling act together to specify endoderm and to control cleavage orientation in early C. elegans embryos. Dev. Cell. 3:2002;113-125.
17. Bowerman B. Determinants of blastomere identity in the early C. elegans embryo. BioEssays. 17:1995;405-414.
18. Brunet J.F., Ghysen A. Deconstructing cell determination: proneural genes and neuronal identity. BioEssays. 21:1999;313-318.
19. Buck L., Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 65:1991;175-187.
20. Calof A.L., Chikaraishi D.M. Analysis of neurogenesis in a mammalian neuroepithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron. 3:1989;115-127.
21. Cassata G., Kagoshima H., Andachi Y., Kohara Y., Durrenberger M.B., Hall D.H., Burglin T.R. The LIM homeobox gene ceh-14 confers thermosensory function to the AFD neurons in Caenorhabditis elegans. Neuron. 25:2000;587-597.
22. Cau E., Gradwohl G., Fode C., Guillemot F. Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors. Development. 124:1997;1611-1621.
23. Cau E., Gradwohl G., Casarosa S., Kageyama R., Guillemot F. Hes genes regulate sequential stages of neurogenesis in the olfactory epithelium. Development. 127:2000;2323-2332.
24. Cau E., Casarosa S., Guillemot F. Mash1 and Ngn1 control distinct steps of determination and differentiation in the olfactory sensory neuron lineage. Development. 129:2002;1871-1880.
25. Chalfie M., Au M. Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. Science. 243:1989;1027-1033.
26. Chang S., Johnston R.J. Jr., Hobert O. A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans. Genes Dev. 17:2003;2123-2137.
27. Cheah P.Y., Chia W., Yang X. Jumeaux, a novel Drosophila winged-helix family protein, is required for generating asymmetric sibling neuronal cell fates. Development. 127:2000;3325-3335.
28. Chess A., Simon I., Cedar H., Axel R. Allelic inactivation regulates olfactory receptor gene expression. Cell. 78:1994;823-834.
29. Chou J.H., Bargmann C.I., Sengupta P. The Caenorhabditis elegans odr-2 gene encodes a novel ly-6-related protein required for olfaction. Genetics. 157:2001;211-224.
30. Clyne P.J., Certel S.J., de Bruyne M., Zaslavsky L., Johnson W.A., Carlson J.R. The odor specificities of a subset of olfactory receptor neurons are governed by Acj6, a POU-domain transcription factor. Neuron. 22:1999;339-347.
31. Clyne P.J., Warr C.G., Freeman M.R., Lessing D., Kim J., Carlson J.R. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron. 22:1999;327-338.
32. Coburn C., Bargmann C.I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron. 17:1996;695-706.
33. Colbert H.A., Bargmann C.I. Environmental signals modulate olfactory acuity, discrimination, and memory in Caenorhabditis elegans. Learn. Mem. 4:1997;179-191.
34. Colbert H.A., Smith T.L., Bargmann C.I. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J. Neurosci. 17:1997;8259-8269.
35. Cole D.G., Diener D.R., Himelblau A.L., Beech P.L., Fuster J.C., Rosenbaum J.L. Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J. Cell Biol. 141:1998;993-1008.
36. Collet J., Spike C.A., Lundquist E.A., Shaw J.E., Herman R.K. Analysis of osm-6, a gene that affects sensory cilium structure and sensory neuron function in Caenorhabditis elegans. Genetics. 148:1998;187-200.
37. Colosimo M.E., Tran S., Sengupta P. The divergent orphan nuclear receptor ODR-7 regulates olfactory neuron gene expression via multiple mechanisms in C. elegans. Genetics. 2003;. (in press).
38. Dambly-Chaudiere C., Vervoort M. The bHLH genes in neural development. Int. J. Dev. Biol. 42:1998;269-273.
39. Dambly-Chaudiere C., Jamet E., Burri M., Bopp D., Basler K., Hafen E., Dumont N., Spielmann P., Ghysen A., Noll M. The paired box gene pox neuro: a determinant of poly-innervated sense organs in Drosophila. Cell. 69:1992;159-172.
40. de Bruyne M., Foster K., Carlson J.R. Odor coding in the Drosophila antenna. Neuron. 30:2001;537-552.
41. Desai C., Garriga G., McIntire S.L., Horvitz H.R. A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature. 336:1988;638-646.
42. Dobritsa A.A., van der Goes van Naters W., Warr C.G., Steinbrecht R.A., Carlson J.R. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron. 37:2003;827-841.
43. Dubois L., Vincent A. The COE-Collier/Olf1/EBF-transcription factors: structural conservation and diversity of developmental functions. Mech. Dev. 108:2001;3-12.
44. Dubruille R., Laurencon A., Vandaele C., Shishido E., Coulon-Bublex M., Swoboda P., Couble P., Kernan M., Durand B. Drosophila regulatory factor X is necessary for ciliated sensory neuron differentiation. Development. 129:2002;5487-5498.
45. Dugas J.C., Ngai J. Analysis and characterization of an odorant receptor gene cluster in the zebrafish genome. Genomics. 71:2001;53-65.
46. Dusenbery D.B., Sheridan R.E., Russell R.L. Chemotaxis-defective mutants of the nematode Caenorhabditis elegans. Genetics. 80:1975;297-309.
47. Evans T.C., Crittenden S.L., Kodoyianni V., Kimble J. Translational control of maternal glp-1 mRNA establishes an asymmetry in the C. elegans embryo. Cell. 77:1994;183-194.
48. Finney M., Ruvkun G. The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell. 63:1990;895-905.
49. Finney M., Ruvkun G., Horvitz H.R. The C. elegans cell lineage and differentiation gene unc-86 encodes a protein with a homeodomain and extended similarity to transcription factors. Cell. 55:1988;757-769.
50. Fisher A., Caudy M. The function of hairy-related bHLH repressor proteins in cell fate decisions. BioEssays. 20:1998;298-306.
51. Fox A.N., Pitts R.J., Robertson H.M., Carlson J.R., Zwiebel L.J. Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding. Proc. Natl. Acad. Sci. U. S. A. 98:2001;14693-14697.
52. Freund C.L., Gregory-Evans C.Y., Furukawa T., Papaioannou M., Looser J., Ploder L., Bellingham J., Ng D., Herbrick J.A., Duncan A., Scherer S.W., Tsui L.C., Loutradis-Anagnostou A., Jacobson S.G., Cepko C.L., Bhattacharya S.S., McInnes R.R. Cone-rod dystrophy due to mutations in a novel photoreceptor- specific homeobox gene (CRX) essential for maintenance of the photoreceptor. Cell. 91:1997;543-553.
53. Furukawa T., Morrow E.M., Cepko C.L. Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell. 91:1997;531-541.
54. Garcia-Bellido A., Ripoll P., Morata G. Developmental compartmentalisation of the wing disk of Drosophila. Nature (London), New Biol. 245:1973;251-253.
55. Gendreau S.B., Moskowitz I.P., Terns R.M., Rothman J.H. The potential to differentiate epidermis is unequally distributed in the AB lineage during early embryonic development in C. elegans. Dev. Biol. 166:1994;770-781.
56. Gesteland R.C., Lettvin J.Y., Pitts W.H. Chemical transmission in the nose of the frog. J. Physiol. 181:1965;525-559.
57. Getchell T.V. Unitary responses in frog olfactory epithelium to sterically related molecules at low concentrations. J. Gen. Physiol. 64:1974;241-261.
58. Getchell T.V., Shepherd G.M. Responses of olfactory receptor cells to step pulses of odour at different concentrations in the salamander. J. Phys. 282:1978;521-540.
59. Ghysen A., Dambly-Chaudiere C. Genesis of the Drosophila peripheral nervous system. Trends Genet. 5:1989;251-255.
60. Glusman G., Sosinsky A., Ben-Asher E., Avidan N., Sonkin D., Bahar A., Rosenthal A., Clifton S., Roe B., Ferraz C., Demaille J., Lancet D. Sequence, structure, and evolution of a complete human olfactory receptor gene cluster. Genomics. 63:2000;227-245.
61. Gomez-Skarmeta J.L., Diez del Corral R., de la Calle-Mustienes E., Ferre-Marco D., Modolell J. Araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell. 85:1996;95-105.
62. Goulding S.E., zur Lage P., Jarman A.P. amos, a proneural gene for Drosophila olfactory sense organs that is regulated by lozenge. Neuron. 25:2000;69-78.
63. Graziadei P.P.C., Monti Graziadei G.A. Continuous nerve cell renewal in the olfactory system. Jacobson M. Handbook of Sensory Physiology. vol. IX:1978;Springer-Verlag, New York.
64. Greenwald I. LIN-12/Notch signaling: lessons from worms and flies. Genes Dev. 12:1998;1751-1762.
65. Guenther C., Garriga G. Asymmetric distribution of the C. elegans HAM-1 protein in neuroblasts enables daughter cells to adopt distinct fates. Development. 122:1996;3509-3518.
66. Guillemot F., Lo L.C., Johnson J.E., Auerbach A., Anderson D.J., Joyner A.L. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell. 75:1993;463-476.
67. Guo M., Jan L.Y., Jan Y.N. Control of daughter cell fates during cell division: interaction between Numb and Notch. Neuron. 17:1996;27-41.
68. Gupta B.P., Rodrigues V. Atonal is a proneural gene for a subset of olfactory sense organs in Drosophila. Genes Cells. 2:1997;225-233.
69. Gupta B.P., Flores G.V., Banerjee U., Rodrigues V. Patterning an epidermal field: Drosophila lozenge, a member of the AML-1/Runt family of transcription factors, specifies olfactory sense organ type in a dose-dependent manner. Dev. Biol. 203:1998;400-411.
70. Hallam S., Singer E., Waring D., Jin Y. The C. elegans NeuroD homolog cnd-1 functions in multiple aspects of motor neuron fate specification. Development. 127:2000;4239-4252.
71. Hanson I.M. Mammalian homologues of the Drosophila eye specification genes. Semin. Cell Dev. Biol. 12:2001;475-484.
72. Hart A., Sims S., Kaplan J. Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature. 378:1995;82-85.
73. Hartenstein V., Posakony J.W. A dual function of the Notch gene in Drosophila sensillum development. Dev. Biol. 142:1990;13-30.
74. Hawkins N., Garriga G. Asymmetric cell division: from A to Z. Genes Dev. 12:1998;3625-3638.
75. Hedgecock E.M., Russell R.L. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 72:1975;4061-4065.
76. Hobert O., Johnston R.J. Jr., Chang S. Left-right asymmetry in the nervous system: the Caenorhabditis elegans model. Nat. Rev. Neurosci. 3:2002;629-640.
77. Horner M.A., Quintin S., Domeier M.E., Kimble J., Labouesse M., Mango S.E. pha-4, an HNF-3 homolog, specifies pharyngeal organ identity in Caenorhabditis elegans. Genes Dev. 12:1998;1947-1952.
78. Huang M.L., Hsu C.H., Chien C.T. The proneural gene amos promotes multiple dendritic neuron formation in the Drosophila peripheral nervous system. Neuron. 25:2000;57-67.
79. Hutter H., Schnabel R. glp-1 and inductions establishing embryonic axes in C. elegans. Development. 120:1994;2051-2064.
80. Hutter H., Schnabel R. Establishment of left-right asymmetry in the Caenorhabditis elegans embryo: a multistep process involving a series of inductive events. Development. 121:1995;3417-3424.
81. Hutter H., Schnabel R. Specification of anterior-posterior differences within the AB lineage in the C. elegans embryo: a polarising induction. Development. 121:1995;1559-1568.
82. Ishitani T., Ninomiya-Tsuji J., Nagai S., Nishita M., Meneghini M., Barker N., Waterman M., Bowerman B., Clevers H., Shibuya H., Matsumoto K. The TAK1-NLK-MAPK-related pathway antagonizes signalling between beta-catenin and transcription factor TCF. Nature. 399:1999;798-802.
83. Jan Y.N., Jan L.Y. Genetic control of cell fate specification in Drosophila peripheral nervous system. Annu. Rev. Genet. 28:1994;373-393.
84. Jan Y.N., Jan L.Y. Asymmetric cell division. Nature. 392:1998;775-778.
85. Jan Y.N., Jan L.Y. Asymmetric cell division in the Drosophila nervous system. Nat. Rev. Neurosci. 2:2001;772-779.
86. Jansen G., Thijssen K.L., Werner P., van der Horst M., Hazendonk E., Plasterk R.H. The complete family of genes encoding G proteins of Caenorhabditis elegans. Nat. Genet. 21:1999;414-419.
87. Jarman A.P., Grau Y., Jan L.Y., Jan Y.N. atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell. 73:1993;1307-1321.
88. Jarman A.P., Grell E.H., Ackerman L., Jan L.Y., Jan Y.N. atonal is the proneural gene for Drosophila photoreceptors. Nature. 369:1994;398-400.
89. Jhaveri D., Sen A., Reddy G.V., Rodrigues V. Sense organ identity in the Drosophila antenna is specified by the expression of the proneural gene atonal. Mech. Dev. 99:2000;101-111.
90. Kageyama R., Nakanishi S. Helix-loop-helix factors in growth and differentiation of the vertebrate nervous system. Curr. Opin. Genet. Dev. 7:1997;659-665.
91. Kalb J.M., Lau K.K., Goszczynski B., Fukushige T., Moons D., Okkema P.G., McGhee J.D. pha-4 is Ce-fkh-1, a fork head/HNF-3α, β, γ homolog that functions in organogenesis of the C. elegans pharynx. Development. 125:1998;2171-2180.
92. Kaletta T., Schnabel H., Schnabel R. Binary specification of the embryonic lineage in Caenorhabditis elegans. Nature. 390:1997;294-298.
93. Kaplan J., Horvitz H. A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 90:1993;2227-2231.
94. Keynes R., Lumsden A. Segmentation and the origin of regional diversity in the vertebrate central nervous system. Neuron. 4:1990;1-9.
95. Komatsu H., Mori I., Ohshima Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron. 17:1996;707-718.
96. Krause M., Park M., Zhang J.M., Yuan J., Harfe B., Xu S.Q., Greenwald I., Cole M., Paterson B., Fire A. A C. elegans E/Daughterless bHLH protein marks neuronal but not striated muscle development. Development. 124:1997;2179-2189.
97. Kudrycki K., Steinizsak C., Behn C., Grillo M. Olf-1 binding site-characterization of an olfactory neuron-specific promoter motif. Mol. Cell. Biol. 13:1993;3002-3014.
98. Labouesse M., Mango S.E. Patterning the C. elegans embryo: moving beyond the cell lineage. Trends Genet. 15:1999;307-313.
99. LaMantia A.S., Bhasin N., Rhodes K., Heemskerk J. Mesenchymal/epithelial induction mediates olfactory pathway formation. Neuron. 28:2000;411-425.
100. Lanjuin A., Sengupta P. Regulation of chemosensory receptor expression and sensory signaling by the KIN-29 Ser/Thr kinase. Neuron. 33:2002;369-381.
101. Lanjuin A., VanHoven M.K., Bargmann C.I., Thompson J.K., Sengupta P. Otx/otd homeobox genes specify distinct neuron identities in C. elegans. Dev. Cell. 5:2003;621-633.
102. Lawrence P.A., Struhl G. Morphogens, compartments, and pattern: lessons from Drosophila? Cell. 85:1996;951-961.
103. Lee J.E. Basic helix-loop-helix genes in neural development. Curr. Opin. Neurobiol. 7:1997;13-20.
104. L'Etoile N.D., Bargmann C.I. Olfaction and odor discrimination are mediated by the C. elegans guanylyl cyclase ODR-1. Neuron. 25:2000;575-586.
105. Leuzinger S., Hirth F., Gerlich D., Acampora D., Simeone A., Gehring W.J., Finkelstein R., Furukubo-Tokunaga K., Reichert H. Equivalence of the fly orthodenticle gene and the human OTX genes in embryonic brain development of Drosophila. Development. 125:1998;1703-1710.
106. Li C., Kim K., Nelson L.S. FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Brain Res. 848:1999;26-34.
107. Lin R., Thompson S., Priess J.R. pop-1 encodes an HMG box protein required for the specification of a mesoderm precursor in early C. elegans embryos. Cell. 83:1995;599-609.
108. Lin R., Hill R.J., Priess J.R. POP-1 and anterior-posterior fate decisions in C. elegans embryos. Cell. 92:1998;229-239.
109. Liu K.S., Sternberg P.W. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron. 14:1995;79-89.
110. Livesey F.J., Furukawa T., Steffen M.A., Church G.M., Cepko C.L. Microarray analysis of the transcriptional network controlled by the photoreceptor homeobox gene Crx. Curr. Biol. 10:2000;301-310.
111. Lo L., Tiveron M.C., Anderson D.J. MASH1 activates expression of the paired homeodomain transcription factor Phox2a, and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. Development. 125:1998;609-620.
112. Lu B., Jan L., Jan Y.-N. Control of cell divisions in the nervous system: symmetry and asymmetry. Annu. Rev. Neurosci. 23:2000;531-556.
113. Lumsden A. The cellular basis of segmentation in the developing hindbrain. Trends Neurosci. 13:1990;329-335.
114. Malnic B., Hirono J., Sato T., Buck L.B. Combinatorial receptor codes for odors. Cell. 96:1999;713-723.
115. Mango S.E., Lambie E.J., Kimble J. The pha-4 gene is required to generate the pharyngeal primordium of Caenorhabditis elegans. Development. 120:1994;3019-3031.
116. Mango S.E., Thorpe C.J., Martin P.R., Chamberlain S.H., Bowerman B. Two maternal genes, apx-1 and pie-1, are required to distinguish the fates of equivalent blastomeres in the early Caenorhabditis elegans embryo. Development. 120:1994;2305-2315.
117. Maricq A.V., Peckol E., Bargmann C.I. Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor. Nature. 378:1995;78-81.
118. Mello C., Draper B., Priess J. The maternal genes apx-1 and glp-1 and establishment of dorsal-ventral polarity in the early C. elegans embryo. Cell. 77:1994;95-106.
119. Meneghini M.D., Ishitani T., Carter J.C., Hisamoto N., Ninomiya-Tsuji J., Thorpe C.J., Hamill D.R., Matsumoto K., Bowerman B. MAP kinase and Wnt pathways converge to downregulate an HMG-domain repressor in Caenorhabditis elegans. Nature. 399:1999;793-797.
120. Modolell J. Patterning of the adult peripheral nervous system of Drosophila. Perspect. Dev. Neurobiol. 4:1997;285-296.
121. Mombaerts P., Wang F., Dulac C., Chao S.K.A.N., Mendelsohn M., Edmondson J., Axel R. Visualizing an olfactory sensory map. Cell. 87:1996;675-686.
122. Mori T., Sakai M., Matsuoka I., Kurihara K. Analysis of promoter activity of 5′-upstream regions of zebrafish olfactory receptor genes. Biol. Pharm. Bull. 23:2000;165-173.
123. Moskowitz I.P., Gendreau S.B., Rothman J.H. Combinatorial specification of blastomere identity by glp-1-dependent cellular interactions in the nematode Caenorhabditis elegans. Development. 120:1994;3325-3338.
124. Nagao T., Leuzinger S., Acampora D., Simeone A., Finkelstein R., Reichert H., Furukubo-Tokunaga K. Developmental rescue of Drosophila cephalic defects by the human Otx genes. Proc. Natl. Acad. Sci. U. S. A. 95:1998;3737-3742.
125. Nolan K.M., Sarafi-Reinach T.R., Horne J.G., Saffer A.M., Sengupta P. The DAF-7 TGF-beta signaling pathway regulates chemosensory receptor gene expression in C. elegans. Genes Dev. 16:2002;3061-3073.
126. Norlin E.M., Berghard A. Spatially restricted expression of regulators of G-protein signaling in primary olfactory neurons. Mol. Cell. Neurosci. 17:2001;872-882.
127. Norlin E.M., Alenius M., Gussing F., Hagglund M., Vedin V., Bohm S. Evidence for gradients of gene expression correlating with zonal topography of the olfactory sensory map. Mol. Cell. Neurosci. 18:2001;283-295.
128. O'Connell R.J., Mozell M.M. Quantitative stimulation of frog olfactory receptors. J. Neurophysiol. 32:1969;51-63.
129. Oliver G., Gruss P. Current views on eye development. Trends Neurosci. 20:1997;415-421.
130. Orozco J.T., Wedaman K.P., Signor D., Brown H., Rose L., Scholey J.M. Movement of motor and cargo along cilia. Nature. 398:1999;674.
131. Page B.D., Zhang W., Steward K., Blumenthal T., Priess J.R. ELT-1, a GATA-like transcription factor, is required for epidermal cell fates in Caenorhabditis elegans embryos. Genes Dev. 11:1997;1651-1661.
132. Peckol E.L., Troemel E.R., Bargmann C.I. Sensory experience and sensory activity regulate chemosensory receptor gene expression in C. elegans. Proc. Natl. Acad. Sci. U. S. A. 98:2001;11032-11038.
133. Perkins L.A., Hedgecock E.M., Thomson J.N., Culotti J.G. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev. Biol. 117:1986;456-487.
134. Petersen P.H., Zou K., Hwang J.K., Jan Y.N., Zhong W. Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature. 419:2002;929-934.
135. Pierce-Shimomura J.T., Faumont S., Gaston M.R., Pearson B.J., Lockery S.R. The homeobox gene lim-6 is required for distinct chemosensory representations in C. elegans. Nature. 410:2001;694-698.
136. Portman D.S., Emmons S.W. The basic helix-loop-helix transcription factors LIN-32 and HLH-2 function together in multiple steps of a C. elegans neuronal sublineage. Development. 127:2000;5415-5426.
137. Prasad B.C., Ye B., Zackhary R., Schrader K., Seydoux G., Reed R.R. unc-3, a gene required for axonal guidance in Caenorhabditis elegans, encodes a member of the O/E family of transcription factors. Development. 125:1998;1561-1568.
138. Priess J.R., Thomson J.N. Cellular interactions in early C. elegans embryos. Cell. 48:1987;241-250.
139. Ray K., Hartenstein V., Rodrigues V. Development of the taste bristles on the labellum of Drosophila melanogaster. Dev Biol. 155:1993;26-37.
140. Reddy G.V., Gupta B., Ray K., Rodrigues V. Development of the Drosophila olfactory sense organs utilizes cell-cell interactions as well as lineage. Development. 124:1997;703-712.
141. Ressler K.J., Sullivan S.L., Buck L.B. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell. 73:1993;597-609.
142. Ressler K.J., Sullivan S.L., Buck L.B. Information coding in the olfactory system: evidence for a sterotyped and highly organized epitope map in the olfactory bulb. Cell. 79:1994;1245-1255.
143. Riddle D.L., Albert P.S. Genetic and environmental regulation of dauer larva development. Riddle D.S., Blumenthal T., Meyer B.J., Priess J.R. C. elegans II. 1997;739-768 Cold Spring Harbor Press, Cold Spring Harbor.
144. Roayaie K., Crump J.G., Sagasti A., Bargmann C.I. The Gα protein ODR-3 mediates olfactory and nociceptive function and controls cilium morphogenesis in C. elegans olfactory neurons. Neuron. 20:1998;55-67.
145. Robertson H.M. Two large families of chemoreceptor genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae reveal extensive gene duplication, diversification, movement, and intron loss. Genome Res. 8:1998;449-463.
146. Robertson H.M. The large srh family of chemoreceptor genes in Caenorhabditis nematodes reveals processes of genome evolution involving large duplications and deletions and intron gains and losses. Genome Res. 10:2000;192-203.
147. Rocheleau C.E., Downs W.D., Lin R., Wittmann C., Bei Y., Cha Y.H., Ali M., Priess J.R., Mello C.C. Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos. Cell. 90:1997;707-716.
148. Rocheleau C.E., Yasuda J., Shin T.H., Lin R., Sawa H., Okano H., Priess J.R., Davis R.J., Mello C.C. WRM-1 activates the LIT-1 protein kinase to transduce anterior/posterior polarity signals in C. elegans. Cell. 97:1999;717-726.
149. Rodriguez I., Feinstein P., Mombaerts P. Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell. 97:1999;199-208.
150. Ruvkun G., Hobert O. The taxonomy of developmental control in Caenorhabditis elegans. Science. 282:1998;2033-2041.
151. Sagasti A., Hobert O., Troemel E.R., Ruvkun G., Bargmann C.I. Alternative olfactory neuron fates are specified by the LIM homeobox gene lim-4. Genes Dev. 13:1999;1794-1806.
152. Sagasti A., Hisamoto N., Hyodo J., Tanaka-Hino M., Matsumoto K., Bargmann C.I. The CaMKII UNC-43 activates the MAPKKK NSY-1 to execute a lateral signaling decision required for asymmetric olfactory neuron fates. Cell. 105:2001;221-232.
153. Saito T., Lo L., Anderson D.J., Mikoshiba K. Identification of novel paired homeodomain protein related to C. elegans unc-4 as a potential downstream target of MASH1. Dev. Biol. 180:1996;143-155.
154. Sarafi-Reinach, T.R., 2001. Generation of chemosensory neuron diversity in Caenorhabditis elegans. PhD thesis, Brandeis University, Waltham.
155. Sarafi-Reinach T.R., Sengupta P. The forkhead domain gene unc-130 generates chemosensory neuron diversity in C. elegans. Genes Dev. 14:2000;2472-2485.
156. Sarafi-Reinach T.R., Melkman T., Hobert O., Sengupta P. The lin-11 LIM homeobox gene specifies olfactory and chemosensory neuron fates in C. elegans. Development. 128:2001;3269-3281.
157. Satterlee J.S., Sasakura H., Kuhara A., Berkeley M., Mori I., Sengupta P. Specification of thermosensory neuron fate in C. elegans requires ttx-1, a homolog of otd/Otx. Neuron. 31:2001;943-956.
158. Schackwitz W.S., Inoue T., Thomas J.H. Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron. 17:1996;719-728.
159. Schnabel R. Cellular interactions involved in the determination of the early C. elegans embryo. Mech. Dev. 34:1991;85-99.
160. Schnabel R. Pattern formation: regional specification in the early C. elegans embryo. BioEssays. 18:1996;591-594.
161. Schnabel R., Hutter H., Moerman D., Schnabel H. Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification. Dev. Biol. 184:1997;234-265.
162. Sengupta P., Colbert H.A., Bargmann C.I. The C. elegans gene odr-7 encodes an olfactory-specific member of the nuclear receptor superfamily. Cell. 79:1994;971-980.
163. Sengupta P., Chou J.H., Bargmann C.I. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell. 84:1996;899-909.
164. 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. Mutually exclusive expression of odorant receptor transgenes. Nat. Neurosci. 3:2000;687-693.
165. Shen Q., Zhong W., Jan Y.N., Temple S. Asymmetric Numb distribution is critical for asymmetric cell division of mouse cerebral cortical stem cells and neuroblasts. Development. 129:2002;4843-4853.
166. Shin T.H., Yasuda J., Rocheleau C.E., Lin R., Soto M., Bei Y., Davis R.J., Mello C.C. MOM-4, a MAP kinase kinase kinase-related protein, activates WRM-1/LIT-1 kinase to transduce anterior/posterior polarity signals in C. elegans. Mol. Cell. 4:1999;275-280.
167. Signor D., Wedaman K.P., Orozco J.T., Dwyer N.D., Bargmann C.I., Rose L.S., Scholey J.M. Role of a class DHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans. J. Cell Biol. 147:1999;519-530.
168. Simpson P. A prepattern for sensory organs. Drosophila development. Curr. Biol. 6:1996;948-950.
169. Skeath J.B., Panganiban G., Selegue J., Carroll S.B. Gene regulation in two dimensions: the proneural achaete and scute genes are controlled by combinations of axis-patterning genes through a common intergenic control region. Genes Dev. 6:1992;2606-2619.
170. Sosinsky A., Glusman G., Lancet D. The genomic structure of human olfactory receptor genes. Genomics. 70:2000;49-61.
171. Spana E.P., Doe C.Q. Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron. 17:1996;21-26.
172. Stocker R.F. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275:1994;3-26.
173. Strotmann J., Wanner I., Krieger J., Raming K., Breer H. Expression of odorant receptors in spatially restricted subsets of chemosensory neurons. NeuroReport. 3:1992;1053-1056.
174. Strotmann J., Konzelmann S., Breer H. Laminar segregation of odorant receptor expression in the olfactory epithelium. Cell Tissue Res. 284:1996;347-354.
175. Sullivan S.L., Bohm S., Ressler K.J., Horowitz L.F., Buck L.B. Target-independent pattern specification in the olfactory epithelium. Neuron. 15:1995;779-789.
176. Sulston J.E., Horvitz H.R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56:1977;110-156.
177. Sulston J.E., Albertson D.G., Thomson J.N. The Caenorhabditis elegans male: postembryonic development of nongonadal structures. Dev. Biol. 78:1980;542-576.
178. Sulston J.E., Schierenberg E., White J.G., Thomson J.N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100:1983;64-119.
179. Swoboda P., Adler H.T., Thomas J.H. The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol. Cell. 5:2000;411-421.
180. Tabish M., Siddiqui Z.K., Nishikawa K., Siddiqui S.S. Exclusive expression of C. elegans osm-3 kinesin gene in chemosensory neurons open to the external environment. J. Mol. Biol. 247:1995;377-389.
181. 2+ signaling to determine neuronal asymmetric development in Caenorhabditis elegans. EMBO Rep. 3:2002;56-62.
182. Thorpe C.J., Schlesinger A., Carter J.C., Bowerman B. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell. 90:1997;695-705.
183. Tirindelli R., Mucignat-Caretta C., Ryba N.J. Molecular aspects of pheromonal communication via the vomeronasal organ of mammals. Trends Neurosci. 21:1998;482-486.
184. Tobin D., Madsen D., Kahn-Kirby A., Peckol E., Moulder G., Barstead R., Maricq A., Bargmann C.I. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron. 35:2002;307-318.
185. Troemel, E.R., 1999a. Chemosensory receptors in Caenorhabditis elegans.
186. Troemel E.R. Chemosensory signaling in C. elegans. BioEssays. 21:1999;1011-1020.
187. Troemel E.R., Chou J.H., Dwyer N.D., Colbert H.A., Bargmann C.I. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell. 83:1995;207-218.
188. Troemel E.R., Kimmel B.E., Bargmann C.I. Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans. Cell. 91:1997;161-169.
189. Troemel E.R., Sagasti A., Bargmann C.I. Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression in C. elegans. Cell. 99:1999;387-398.
190. Uchida O., Nakano H., Koga M., Ohshima Y. The C. elegans che-1 gene encodes a zinc finger transcription factor required for specification of the ASE chemosensory neurons. Development. 130:2003;1215-1224.
191. Vassalli A., Rothman A., Feinstein P., Zapotocky M., Mombaerts P. Minigenes impart odorant receptor-specific axon guidance in the olfactory bulb. Neuron. 35:2002;681-696.
192. Vassar R., Ngai J., Axel R. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell. 74:1993;309-318.
193. Vassar R., Chao S.K., Sitcheran R., Nunez J.M., Vosshall L.B., Axel R. Topographic organization of sensory projections in the olfactory bulb. Cell. 79:1994;981-991.
194. Vosshall L.B., Amrein H., Morozov P.S., Rzhetsky A., Axel R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell. 96:1999;725-736.
195. Vosshall L.B., Wong A.M., Axel R. An olfactory sensory map in the fly brain. Cell. 102:2000;147-159.
196. Wang S.S., Tsai R.Y.L., Reed R.R. The characterization of the Olf-1/EBF-like HLH transcription factor family: implications in olfactory gene regulation and neuronal development. J. Neurosci. 17:1997;4149-4158.
197. Wang F., Nemes A., Mendelsohn M., Axel R. Odorant receptors govern the formation of a precise topographic map. Cell. 93:1998;47-60.
198. Wang S.S., Betz A.G., Reed R.R. Cloning of a novel Olf-1/EBF-like gene, O/E-4, by degenerate oligo-based direct selection. Mol. Cell. Neurosci. 20:2002;404-414.
199. Ward S., Thomson N., White J.G., Brenner S. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J. Comp. Neurol. 160:1975;313-337.
200. Wawersik S., Maas R.L. Vertebrate eye development as modeled in Drosophila. Hum. Mol. Genet. 9:2000;917-925.
201. Wes P.D., Bargmann C.I. C. elegans odour discrimination requires asymmetric diversity in olfactory neurons. Nature. 410:2001;698-701.
202. White J.G., Southgate E., Thomson J.N., Brenner S. The structure of the ventral nerve cord of Caenorhabditis elegans. Philos. Trans. R. Soc. London, Ser. B. 275:1976;327-348.
203. White J.G., Southgate E., Thomson J.N., Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. London, Ser. B. 314:1986;1-340.
204. Whitesides J., Hall M., Anchan R., LaMantia A.S. Retinoid signaling distinguishes a subpopulation of olfactory receptor neurons in the developing and adult mouse. J. Comp. Neurol. 394:1998;445-461.
205. Wood W.B. Evidence from reversal of handedness in C. elegans embryos for early cell interactions determining cell fates. Nature. 349:1991;536-538.
206. Xu Y., Baldassare M., Fisher P., Rathbun G., Oltz E.M., Yancopoulos G.D., Jessell T.M., Alt F.W. LH-2: a LIM/homeodomain gene expressed in developing lymphocytes and neural cells. Proc. Natl. Acad. Sci. U. S. A. 90:1993;227-321.
207. Yoshihara Y., Kawasaki M., Tamada A., Fujita H., Hayashi H., Kagamiyama H., Mori K. OCAM: a new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons. J. Neurosci. 17:1997;5830-5842.
208. Yu S., Avery L., Baude E., Garbers D.A. Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc. Natl. Acad. Sci. U. S. A. 94:1997;3384-3387.
209. Zeng C., Younger-Shepherd S., Jan L.Y., Jan Y.N. Delta and Serrate are redundant Notch ligands required for asymmetric cell divisions within the Drosophila sensory organ lineage. Genes Dev. 12:1998;1086-1091.
210. Zhao C., Emmons S.W. A transcription factor controlling development of peripheral sense organs in C. elegans. Nature. 373:1995;74-78.
211. Zhong W., Feder J.N., Jiang M.M., Jan L.Y., Jan Y.N. Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron. 17:1996;43-53.
212. Zhong W., Jiang M.M., Weinmaster G., Jan L.Y., Jan Y.N. Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development. 124:1997;1887-1897.
213. Zhong W., Jiang M.M., Schonemann M.D., Meneses J.J., Pedersen R.A., Jan L.Y., Jan Y.N. Mouse numb is an essential gene involved in cortical neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 97:2000;6844-6849.