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Molecular Cloning and Characterization of Homologs of Achaete–Scute and Hairy–Enhancer of Split in the Olfactory Organ of the Spiny Lobster Panulirus argus

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Abstract

The olfactory organ of the Caribbean spiny lobster Panulirus argus maintains lifelong proliferation and turnover of olfactory receptor neurons (ORNs). Towards examining the molecular basis of this adult neurogenesis, we search for expression of homologs of proneural, neurogenic, and pre-pattern genes in this olfactory organ. We report here a homolog of the proneural Achaete–Scute family, called splash (spiny lobster achaete–scute homolog), and a homolog of the pre-pattern and neurogenic hairy–enhancer of split family, called splhairy (spiny lobster hairy). Semi-quantitative reverse transcriptase–polymerase chain reaction (RT-PCR) indicates a molt stage dependence of the levels of expression of splash and splhairy mRNA in the olfactory organ, with higher expression in premolt than in postmolt or intermolt animals, which is positively correlated with rates of neurogenesis. splash and splhairy mRNA are expressed not only in the olfactory organ but also in other tissues, albeit at lower levels, irrespective of molt stage. We conclude that the expression of achaete–scute and hairy–enhancer of split in the proliferation zone of the olfactory organ of spiny lobsters and their enhanced expression in premolt animals suggest that they play a role in the proliferation of ORNs and that their expression in regions of the olfactory organ populated by mature ORNs and in other tissues suggests that they have additional functions.

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References

  • Ache, B. W. (2002). Crustaceans as animal models for olfactory research. In K. Wiese (Ed.), Frontiers in Crustacean neurobiology (pp. 189–199). Heidelberg: Springer.

    Google Scholar 

  • Akazawa, C., Sasai, Y., Nakanishi, S., & Kageyama, R. (1992). Molecular characterization of a rat negative regulator with a basic helix-loop-helix structure predominantly expressed in the developing nervous system. The Journal of Biological Chemistry, 267, 21879–21885.

    PubMed  CAS  Google Scholar 

  • Allen, T., & Lobe, C. G. (1999). A comparison of Notch, Hes and Grg expression during murine embryonic and post-natal development. Cellular Molecular Biology (Noisy-le-grand), 45, 687–708.

    CAS  Google Scholar 

  • Alonso, M. C., & Cabrera, C. V. (1988). The achaete–scute gene complex of Drosophila melanogaster comprises four homologous genes. The EMBO Journal, 7, 2585–2591.

    PubMed  CAS  Google Scholar 

  • Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., et al. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402. doi:10.1093/nar/25.17.3389.

    Article  PubMed  CAS  Google Scholar 

  • Beites, C. L., Kawauchi, S., Crocker, C. E., & Calof, A. L. (2005). Identification and molecular regulation of neural stem cells in the olfactory epithelium. Experimental Cell Research, 306, 309–316. doi:10.1016/j.yexcr.2005.03.027.

    Article  PubMed  CAS  Google Scholar 

  • Brunjes, P. C. (1992). Lessons from lesions—The effects of olfactory bulbectomy. Chemical Senses, 17, 729–763. doi:10.1093/chemse/17.6.729.

    Article  Google Scholar 

  • Cabrera, C. V., Martinez-Arias, A., & Bale, M. (1987). The expression of three members of the achaete–scute gene complex correlates with neuroblast segregation in Drosophila. Cell, 50, 425–433. doi:10.1016/0092-8674(87)90496-X.

    Article  PubMed  CAS  Google Scholar 

  • Calof, A. L., Bonnin, A., Crocker, C., Kawauchi, S., Murray, R. C., Shou, J., et al. (2002). Progenitor cells of the olfactory receptor neuron lineage. Microscopy Research and Technique, 58, 176–188. doi:10.1002/jemt.10147.

    Article  PubMed  CAS  Google Scholar 

  • Campuzano, S., & Modolell, J. (1992). Patterning of the Drosophila nervous system: The achaete–scute gene complex. Trends in Genetics, 8, 202–208.

    PubMed  CAS  Google Scholar 

  • Caprio, J., & Derby, C. D. (2008). Aquatic animal models in the study of chemoreception. In A. I. Basbaum, A. Maneko, G. M. Shepherd, & G. Westheimer (Eds.), The senses: A comprehensive reference, vol. 4 (pp. 97–134). San Diego: Academic.

    Google Scholar 

  • Carter, L. A., & Roskams, A. J. (2002). Neurotrophins and their receptors in the primary olfactory neuraxis. Microscopy Research and Technique, 58, 189–196. doi:10.1002/jemt.10148.

    Article  PubMed  CAS  Google Scholar 

  • Cate, H. S., & Derby, C. D. (2001). Morphology and distribution of setae on the antennules of the Caribbean spiny lobster Panulirus argus reveal new types of bimodal chemo-mechanosensilla. Cell and Tissue Research, 304, 439–454. doi:10.1007/s004410100377.

    Article  PubMed  CAS  Google Scholar 

  • Cate, H. S., & Derby, C. D. (2002). Ultrastructure and physiology of the hooded sensillum, a bimodal chemo-mechanosensillum of lobsters. The Journal of Comparative Neurology, 442, 293–307. doi:10.1002/cne.10106.

    Article  PubMed  Google Scholar 

  • Cau, E., Gradwohl, G., Kageyama, R., & Guillemot, F. (2000). Hes genes regulate sequential stages of neurogenesis in the olfactory epithelium. Development, 127, 2323–2332.

    PubMed  CAS  Google Scholar 

  • Chase, R., & Rieling, J. (1986). Autoradiographic evidence for receptor cell renewal in the olfactory epithelium of a snail Achatina fulica. Brain Research, 384, 232–239. doi:10.1016/0006-8993(86)91159-5.

    Article  PubMed  CAS  Google Scholar 

  • Chipman, A. D., & Akam, M. (2008). The segmentation cascade in the centipede Strigamia maritima: Involvement of the Notch pathway and pair-rule gene homologues. Developmental Biology, 319, 160–169. doi:10.1016/j.ydbio.2008.02.038.

    Article  PubMed  CAS  Google Scholar 

  • Chitnis, A., & Kintner, C. (1996). Sensitivity of proneural genes to lateral inhibition affects the pattern of primary neurons in Xenopus embryos. Development, 122, 2295–2301.

    PubMed  CAS  Google Scholar 

  • Dawson, S. R., Turner, D. L., Weintraub, H., & Parkhurst, S. M. (1995). Specificity for the hairy/enhancer of split basic helix-loop-helix (bHLH) proteins maps outside the bHLH domain and suggests two separable modes of transcriptional repression. Molecular and Cellular Biology, 15, 6923–6931.

    PubMed  CAS  Google Scholar 

  • Delidakis, C., & Artavanis-Tsakonas, S. (1992). The Enhancer of split [E(spl)] locus of Drosophila encodes seven independent helix-loop-helix proteins. Proceedings of the National Academy of Sciences of the United States of America, 89, 8731–8735. doi:10.1073/pnas.89.18.8731.

    Article  PubMed  CAS  Google Scholar 

  • Derby, C. D., Steullet, P., Cate, H. S., & Harrison, P. J. H. (2002). A compound nose: Functional organization and development of aesthetasc sensilla. In K. Wiese (Ed.), The Crustacean nervous system (pp. 346–358). Heidelberg: Springer.

    Google Scholar 

  • Derby, C. D., Cate, H. S., Steullet, P., & Harrison, P. J. H. (2003). Comparison of turnover in the olfactory organ of early juvenile stage and adult Caribbean spiny lobsters. Arthropod Structure & Development, 31, 297–311. doi:10.1016/S1467-8039(02)00050-6.

    Article  Google Scholar 

  • Doonan, R., Hatzold, J., Raut, S., Conradt, B., & Alfonso, A. (2008). HLH-3 is a C. elegans Achaete/Scute protein required for differentiation of the hermaphrodite-specific motor neurons. Mechanisms of Development, 125, 883–893. doi:10.1016/j.mod.2008.06.002.

    Article  PubMed  CAS  Google Scholar 

  • Dove, H., & Stollewerk, A. (2003). Comparative analysis of neurogenesis in the myriapod Glomeris marginata (Diplopoda) suggests more similarities to chelicerates than to insects. Development, 130, 2161–2171. doi:10.1242/dev.00442.

    Article  PubMed  CAS  Google Scholar 

  • Feder, J. N., Jan, L. Y., & Jan, Y. N. (1993). A rat gene with sequence homology to the Drosophila gene hairy is rapidly induced by growth factors known to influence neuronal differentiation. Molecular and Cellular Biology, 13, 105–113.

    PubMed  CAS  Google Scholar 

  • Feder, J. N., Li, L., Jan, L. Y., & Jan, Y. N. (1994). Genomic cloning and chromosomal localization of HRY, the human homolog to the Drosophila segmentation gene, hairy. Genomics, 20, 56–61. doi:10.1006/geno.1994.1126.

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein, J. (1993). PHYLIP (phylogeny inference package) v3.5c. Cladistics, 5, 164–166.

    Google Scholar 

  • Frank, C. A., Baum, P. D., & Garriga, G. (2003). HLH-14 is a C. elegans Achaete–Scute protein that promotes neurogenesis through asymmetric cell division. Development, 130, 6507–6518. doi:10.1242/dev.00894.

    Article  PubMed  CAS  Google Scholar 

  • Galant, R., Skeath, J. B., Paddocks, S., Lewis, D. L., & Carroll, S. B. (1998). Expression pattern of a butterfly achaete–scute homolog reveals the homology of butterfly wing scales and insect sensory bristles. Current Biology, 8, 807–813. doi:10.1016/S0960-9822(98)70322-7.

    Article  PubMed  CAS  Google Scholar 

  • Greenwood, S., & Struhl, G. (1999). Progression of the morphogenetic furrow in the Drosophila eye: the roles of Hedgehog, Decapentaplegic and the Raf pathway. Development, 126, 5795–5808.

    PubMed  CAS  Google Scholar 

  • Grens, A., Mason, E., Marsh, J. L., & Bode, H. R. (1995). Evolutionary conservation of a cell fate specification gene: the Hydra achaete–scute homolog has proneural activity in Drosophila. Development, 121, 4027–4035.

    PubMed  CAS  Google Scholar 

  • Grünert, U., & Ache, B. W. (1988). Ultrastructure of the aesthetasc (olfactory) sensilla of the spiny lobster, Panulirus argus. Cell and Tissue Research, 251, 95–103. doi:10.1007/BF00215452.

    Article  Google Scholar 

  • Gupta, B. P., & Rodrigues, V. (1997). Atonal is a proneural gene for a subset of olfactory sense organs in Drosophila. Genes to Cells, 2, 225–233. doi:10.1046/j.1365-2443.1997.d01-312.x.

    Article  PubMed  CAS  Google Scholar 

  • Guse, G.-W. (1979). Feinstruktur der Aesthetasken von Neomysis integer (Leach) (Crustacea, Mysidacea). Zoologischer Anzeiger, 203, 170–176.

    Google Scholar 

  • Harrison, P. J. H., Cate, H. S., Swanson, E. S., & Derby, C. D. (2001a). Postembryonic proliferation in the spiny lobster antennular epithelium: Rate of genesis of olfactory receptor neurons is dependent on molt stage. Journal of Neurobiology, 47, 51–66. doi:10.1002/neu.1015.

    Article  PubMed  CAS  Google Scholar 

  • Harrison, P. J. H., Cate, H. S., Steullet, P., & Derby, C. D. (2001b). Structural plasticity in the olfactory system of adult spiny lobsters: Postembryonic development permits life-long growth, turnover, and regeneration. Marine & Freshwater Research, 52, 1357–1365. doi:10.1071/MF01103.

    Article  Google Scholar 

  • Harrison, P. J. H., Cate, H. S., Steullet, P., & Derby, C. D. (2003). Amputation-induced activity of progenitor cells leads to rapid regeneration of olfactory tissue in lobsters. Journal of Neurobiology, 55, 97–114. doi:10.1002/neu.10206.

    Article  PubMed  Google Scholar 

  • Harrison, P. J. H., Cate, H. S., & Derby, C. D. (2004). Localized ablation of olfactory receptor neurons induces both localized regeneration and widespread replacement of neurons in spiny lobsters. The Journal of Comparative Neurology, 471, 72–84. doi:10.1002/cne.20020.

    Article  PubMed  Google Scholar 

  • Hayakawa, E., Fujisawa, C., & Fujisawa, T. (2004). Involvement of Hydra achaete–scute gene CnASH in the differentiation pathway of sensory neurons in the tentacles. Development Genes and Evolution, 214, 486–492.

    PubMed  CAS  Google Scholar 

  • Heimann, P. (1984). Fine structure and molting of aesthetasc sense organs on the antennules of the isopod Asellus aquaticus (Crustacea). Cell and Tissue Research, 235, 117–128. doi:10.1007/BF00213731.

    Article  PubMed  CAS  Google Scholar 

  • Henrique, D., Tyler, D., Kintner, C., Heath, J. K., Lewis, J. H., Ish-Horowicz, D., et al. (1997). Cash4, a novel achaete–scute homolog induced by Hensen’s node during generation of the posterior nervous system. Genes & Development, 11, 603–615. doi:10.1101/gad.11.5.603.

    Article  CAS  Google Scholar 

  • Ishibashi, M., Moriyoshi, K., Sasai, Y., Shiota, K., Nakanishi, S., & Kageyama, R. (1994). Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. The EMBO Journal, 13, 1799–1805.

    PubMed  CAS  Google Scholar 

  • Ishibashi, M., Sasai, Y., Nakanishi, S., & Kageyama, R. (1993). Molecular characterization of HES-2, a mammalian helix-loop-helix factor structurally related to Drosophila hairy and Enhancer of split. European Journal of Biochemistry, 215, 645–652. doi:10.1111/j.1432-1033.1993.tb18075.x.

    Article  PubMed  CAS  Google Scholar 

  • Jan, Y. N., & Jan, L. Y. (1994). Genetic control of cell fate specification in Drosophila peripheral nervous system. Annual Review of Genetics, 28, 373–393. doi:10.1146/annurev.ge.28.120194.002105.

    Article  PubMed  CAS  Google Scholar 

  • Jarman, A. P., Brand, M., Jan, L. Y., & Jan, Y. N. (1993). The regulation and function of the helix-loop-helix gene, asense, in Drosophila neural precursors. Development, 119, 19–29.

    PubMed  CAS  Google Scholar 

  • Jasoni, C. L., Walker, M. B., Morris, M. D., & Reh, T. A. (1994). A chicken achaete–scute homolog (CASH-1) is expressed in a temporally and spatially discrete manner in the developing nervous system. Development, 120, 769–783.

    PubMed  CAS  Google Scholar 

  • Johnson, J. E., Birren, S. J., & Anderson, D. J. (1990). Two rat homologues of Drosophila achaete–scute specifically expressed in neuronal precursors. Nature, 346, 858–861. doi:10.1038/346858a0.

    Article  PubMed  CAS  Google Scholar 

  • Joshi, M. K., Buchanan, T., Shroff, S., & Orenic, T. V. (2006). Delta and Hairy establish a periodic prepattern that positions sensory bristles in Drosophila legs. Developmental Biology, 295, 64–76. doi:10.1016/j.ydbio.2006.01.005.

    Article  CAS  Google Scholar 

  • Kawauchi, S., Beites, C. L., Crocker, C. E., Wu, H. H., Bonnin, A., Murray, R., et al. (2004). Molecular signals regulating proliferation of stem and progenitor cells in mouse olfactory epithelium. Developmental Neuroscience, 26, 166–180. doi:10.1159/000082135.

    Article  PubMed  CAS  Google Scholar 

  • Klämbt, C., Knust, E., Tietze, K., & Campos-Ortega, J. A. (1989). Closely related transcripts encoded by the neurogenic gene complex enhancer of split of Drosophila melanogaster. The EMBO Journal, 8, 203–210.

    PubMed  Google Scholar 

  • Knust, E., Schrons, H., Grawe, F., & Campos-Ortega, J. A. (1992). Seven genes of the Enhancer of split complex of Drosophila melanogaster encode helix-loop-helix proteins. Genetics, 132, 505–518.

    PubMed  CAS  Google Scholar 

  • Kohler, K., Thayer, W., Le, T., Sembhi, A., Vasanthavada, K., Moore, A. M., et al. (2005). Characterization of a novel class II bHLH transcription factor from the black widow spider, Latrodectus hesperus, with silk-gland restricted patterns of expression. DNA and Cell Biology, 24, 371–380. doi:10.1089/dna.2005.24.371.

    Article  PubMed  CAS  Google Scholar 

  • Lai, E. C., & Orgogozo, V. (2004). A hidden program in Drosophila peripheral neurogenesis revealed: Fundamental principles underlying sensory organ diversity. Developmental Biology, 269, 1–17. doi:10.1016/j.ydbio.2004.01.032.

    Article  PubMed  CAS  Google Scholar 

  • Lesaffre, B., Joliot, A., Prochiantz, A., & Volovitch, M. (2007). Direct non-cell autonomous Pax6 activity regulates eye development in the zebrafish. Neural Development, 2, 2. doi:10.1186/1749-8104-2-2.

    Article  PubMed  CAS  Google Scholar 

  • Lim, J., Jafar-Nejad, H., Hsu, Y.-C., & Choi, K.-W. (2008). Novel function of the class I bHLH protein Daughterless in the negative regulation of proneural gene expression in the Drosophila eye. EMBO Reports, 9, 1128–1133. doi:10.1038/embor.2008.166].

    Article  PubMed  CAS  Google Scholar 

  • Lo, L. C., Johnson, J. E., Wuenschell, C. W., Saito, T., & Anderson, D. J. (1991). Mammalian achaete–scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes & Development, 5, 1524–1537. doi:10.1101/gad.5.9.1524.

    Article  CAS  Google Scholar 

  • Lyle, W. G., & MacDonald, C. D. (1983). Molt stage determination in the Hawaiian spiny lobster, Panulirus marginatus. Journal of Crustacean Biology, 3, 208–216. doi:10.2307/1548257.

    Article  Google Scholar 

  • Manglapus, G. L., Youngentob, S. L., & Schwob, J. E. (2004). Expression patterns of basic helix-loop-helix transcription factors define subsets of olfactory progenitor cells. The Journal of Comparative Neurology, 479, 216–233. doi:10.1002/cne.20316.

    Article  PubMed  CAS  Google Scholar 

  • Martín-Bermudo, M. D., Martínez, C., Rodríguez, A., & Jiménez, F. (1991). Distribution and function of the lethal of scute gene product during early neurogenesis in Drosophila. Development, 113, 445–454.

    PubMed  Google Scholar 

  • Martínez-Marcos, A., Ubeda-Bañón, I., Deng, L., & Halpern, M. (2000a). Neurogenesis in the vomeronasal epithelium of adult rats: Evidence for different mechanisms for growth and neuronal turnover. Journal of Neurobiology, 44, 423–435. doi:10.1002/1097-4695(20000915)44:4<423::AID-NEU5>3.0.CO;2-H.

    Article  PubMed  Google Scholar 

  • Martínez-Marcos, A., Ubeda-Bañón, I., & Halpern, M. (2000b). Cell turnover in the vomeronasal epithelium: Evidence for differential migration and maturation of subclasses of vomeronasal neurons in the adult opossum. Journal of Neurobiology, 43, 50–63. doi:10.1002/(SICI)1097-4695(200004)43:1<50::AID-NEU5>3.0.CO;2-N.

    Article  PubMed  Google Scholar 

  • Maung, S. M. T. W., & Jarman, A. P. (2007). Functional distinctness of closely related transcription factors: A comparison of the Atonal and Amos proneural factors. Mechanisms of Development, 124, 647–656. doi:10.1016/j.mod.2007.07.006.

    Article  PubMed  CAS  Google Scholar 

  • McClintock, T. S., & Xu, F. (2002). Molecular physiology of G-proteins in olfactory transduction and CNS neurotransmission. In K. Wiese (Ed.), The Crustacean nervous system (pp. 359–366). Heidelberg: Springer.

    Google Scholar 

  • McClintock, T. S., Ache, B. W., & Derby, C. D. (2006). Lobster olfactory genomics. Integrative and Comparative Biology, 46, 940–947. doi:10.1093/icb/icj050.

    Article  CAS  Google Scholar 

  • Mueller, T., & Wullimann, M. F. (2003). Anatomy of neurogenesis in the early zebrafish brain. Brain Research. Developmental Brain Research, 140, 137–155. doi:10.1016/S0165-3806(02)00583-7.

    Article  PubMed  CAS  Google Scholar 

  • Murray, R. C., Navi, D., Fesenko, J., Lander, A. D., & Calof, A. L. (2003). Widespread defects in the primary olfactory pathway caused by loss of Mash1 function. The Journal of Neuroscience, 23, 1769–1780.

    PubMed  CAS  Google Scholar 

  • Nakamura, Y., Sakakibara, S., Miyata, T., Ogawa, M., Shimazaki, T., Weiss, S., et al. (2000). The bHLH gene hes1 as a repressor of the neuronal commitment of CNS stem cells. The Journal of Neuroscience, 20, 283–293.

    PubMed  CAS  Google Scholar 

  • Ohsako, S., Hyer, J., Panganiban, G., Oliver, I., & Causy, M. (1994). hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. Genes & Development, 8, 2743–2755. doi:10.1101/gad.8.22.2743.

    Article  CAS  Google Scholar 

  • Ohtsuka, T., Sakamoto, M., Guillemot, F., & Kageyama, R. (2001). Roles of the basic helix-loop-helix genes Hes1 and Hes5 in expansion of neural stem cells of the developing brain. The Journal of Biological Chemistry, 276, 30467–30474. doi:10.1074/jbc.M102420200.

    Article  PubMed  CAS  Google Scholar 

  • Pistillo, D., Skaer, N., & Simpson, P. (2002). scute expression in Calliphora vicina reveals an ancestral pattern of longitudinal stripes on the thorax of higher Diptera. Development, 129, 563–572.

    PubMed  CAS  Google Scholar 

  • Prochiantz, A., & Joliot, A. (2003). Can transcription factors function as cell–cell signalling molecules? Nature Reviews. Molecular Cell Biology, 4, 814–819.

    PubMed  CAS  Google Scholar 

  • Ray, K., & Rodrigues, V. (1995). Cellular events during development of the olfactory sense organs in Drosophila melanogaster. Developmental Biology, 167, 426–438. doi:10.1006/dbio.1995.1039.

    Article  PubMed  CAS  Google Scholar 

  • Rebay, I., Silver, S. J., & Tootle, T. L. (2005). New vision for Eyes absent: Transcription factors as enzymes. Trends in Genetics, 21, 163–171. doi:10.1016/j.tig.2005.01.005.

    Article  PubMed  CAS  Google Scholar 

  • Reddy, G. V., Gupta, B., Ray, K., & Rodrigues, V. (1997). Development of the Drosophila olfactory sense organs utilizes cell–cell interactions as well as lineage. Development, 124, 703–712.

    PubMed  CAS  Google Scholar 

  • Rebeiz, M., Stone, T., & Posakony, J. W. (2005). An ancient transcriptional regulatory linkage. Developmental Biology, 281, 299–308. doi:10.1016/j.ydbio.2005.03.004.

    Article  PubMed  CAS  Google Scholar 

  • Sasai, Y., Kageyama, R., Sasai, Y., Kageyama, R., Tagawa, Y., Shigemoto, R., et al. (1992). Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes & Development, 6, 2620–2634. doi:10.1101/gad.6.12b.2620.

    Article  CAS  Google Scholar 

  • Schachtner, J., Schmidt, M., & Homberg, U. (2005). Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Structure & Development, 34, 257–299. doi:10.1016/j.asd.2005.04.003.

    Article  Google Scholar 

  • Schmidt, M., & Derby, C. D. (2005). Non-olfactory chemoreceptors in asymmetric setae activate antennular grooming behavior in the Caribbean spiny lobster, Panulirus argus. The Journal of Experimental Biology, 208, 233–248. doi:10.1242/jeb.01357.

    Article  PubMed  CAS  Google Scholar 

  • Seipel, K., Yanze, N., & Schmid, V. (2004). Developmental and evolutionary aspects of the basic helix-loop-helix transcription factors Atonal-like 1 and Achaete–scute homolog 2 in the jellyfish. Developmental Biology, 269, 331–345. doi:10.1016/j.ydbio.2004.01.035.

    Article  PubMed  CAS  Google Scholar 

  • Shetty, R. S., Bose, S. C., Nickell, M. D., McIntyre, J. C., Hardin, D. H., Harris, A. M., et al. (2005). Transcriptional changes during neuronal death and replacement in the olfactory epithelium. Molecular and Cellular Neurosciences, 30, 583–600. doi:10.1016/j.mcn.2005.06.003.

    PubMed  CAS  Google Scholar 

  • Simionato, E., Kerner, P., Dray, N., Le Gouar, M., Ledent, V., Arendt, D., et al. (2008). atonal- and achaete–scute-related genes in the annelid Platynereis dumerilii: Insights into the evolution of neural basic-Helix-Loop-Helix genes. BMC Evolutionary Biology, 8, 170. doi:10.1186/1471-2148-8-170.

    Article  PubMed  CAS  Google Scholar 

  • Skaer, N., Pistillo, D., & Simpson, P. (2002a). Transcriptional heterochrony of scute and changes in bristle pattern between two closely related species of blowfly. Developmental Biology, 252, 31–45. doi:10.1006/dbio.2002.0841.

    Article  PubMed  CAS  Google Scholar 

  • Skaer, N., Pistillo, D., Gibert, J. M., Lio, P., Wülbeck, C., & Simpson, P. (2002b). Gene duplication at the achaete–scute complex and morphological complexity of the peripheral nervous system in Diptera. Trends in Genetics, 18, 399–405. doi:10.1016/S0168-9525(02)02747-6.

    Article  PubMed  CAS  Google Scholar 

  • Skeath, J. B., & Carroll, S. B. (1992). Regulation of proneural gene expression and cell fate during neuroblast segregation in the Drosophila embryo. Development, 114, 939–946.

    PubMed  CAS  Google Scholar 

  • Smith, R. F., Wiese, B. A., Wojzynski, M. K., Davison, D. B., & Worley, K. C. (1996). BCM Search Launcher—An integrated interface to molecular biology data base search and analysis services available on the World Wide Web. Genome Research, 6, 454–462. doi:10.1101/gr.6.5.454.

    Article  PubMed  CAS  Google Scholar 

  • Stepanyan, R., Day, K., Urban, J., Hardin, D. H., Shetty, R. S., et al. (2006). Gene expression and specificity in the mature zone of the lobster olfactory organ. Physiological Genomics, 25, 224–233. doi:10.1152/physiolgenomics.00276.2005.

    Article  PubMed  CAS  Google Scholar 

  • Steullet, P., Cate, H. S., Michel, W. C., & Derby, C. D. (2000a). Functional units of a compound nose: aesthetasc sensilla house similar populations of olfactory receptor neurons on the crustacean antennule. The Journal of Comparative Neurology, 418, 270–280. doi:10.1002/(SICI)1096-9861(20000313)418:3<270::AID-CNE3>3.0.CO;2-G.

    Article  PubMed  CAS  Google Scholar 

  • Steullet, P., Cate, H. S., & Derby, C. D. (2000b). A spatiotemporal wave of turnover and functional maturation of olfactory receptor neurons in the spiny lobster Panulirus argus. The Journal of Neuroscience, 20, 3282–3294.

    PubMed  CAS  Google Scholar 

  • Stifani, S., Blaumueller, C. M., Redhead, N. J., Hill, R. E., & Artavanis-Tsakonas, S. (1992). Human homologs of a Drosophila Enhancer of split gene product define a novel family of nuclear proteins. Nature Genetics, 2, 343. doi:10.1038/ng1092-119.

    Article  PubMed  CAS  Google Scholar 

  • Stollewerk, A., Weller, M., & Tautz, D. (2001). Neurogenesis in the spider Cupiennius salei. Development, 128, 2673–2688.

    PubMed  CAS  Google Scholar 

  • Stoss, T. D., Nickell, M. D., Hardin, D., Derby, C. D., & McClintock, T. S. (2004). Inducible transcript expressed by reactive epithelial cells at sites of olfactory sensory neuron proliferation. Journal of Neurobiology, 58, 355–368. doi:10.1002/neu.10294.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680. doi:10.1093/nar/22.22.4673.

    Article  PubMed  CAS  Google Scholar 

  • Tong, X.-L., Dai, F.-Y., Su, M.-K., Ma, Y., Tan, D., Zhang, Z., et al. (2008). Identification and expression of the achaete–scute complex in the silkworm, Bombyx mori. Insect Molecular Biology, 17, 395–404. doi:10.1111/j.1365-2583.2008.00811.x.

    Article  PubMed  CAS  Google Scholar 

  • Van Doren, M., Bailey, A. M., Esnayra, J., Ede, K., & Posakony, J. W. (1994). Negative regulation of proneural gene activity: hairy is a direct transcriptional repressor of achaete. Genes & Development, 8, 2729–2742. doi:10.1101/gad.8.22.2729.

    Article  Google Scholar 

  • Verma-Kurvari, S., & Johnson, J. E. (1997). Identification of an achaete–scute homolog, Fash1, from Fugu rubripes. Gene, 200, 145–148. doi:10.1016/S0378-1119(97)00394-6.

    Article  PubMed  CAS  Google Scholar 

  • Vervoot, M., Merritt, D. J., Ghysen, A., & Dambly-Chaudiere, C. (1997). Genetic basis of the formation and identity of type I and type II neurons in Drosophila embryos. Development, 124, 2819–2828.

    Google Scholar 

  • Wheeler, S. R., & Skeath, J. B. (2005). The identification and expression of achaete–scute genes in the branchiopod crustacean Triops longicaudatus. Gene Expression Patterns, 5, 695–700. doi:10.1016/j.modgep.2005.02.005.

    Article  PubMed  CAS  Google Scholar 

  • Wheeler, S. R., Carrico, M. L., Wilson, B. A., Brown, S. J., & Skeath, J. B. (2003). The expression and function of the achaete–scute genes in Tribolium castaneum reveals conservation and variation in neural pattern formation and cell fate specification. Development, 130, 4373–4381. doi:10.1242/dev.00646.

    Article  PubMed  CAS  Google Scholar 

  • Wülbeck, C., & Simpson, P. (2000). Expression of achaete–scute homologues in discrete proneural clusters on the developing notum of the medfly Ceratitis capitata, suggests a common origin for the stereotyped bristle patterns of higher Diptera. Development, 127, 1411–1420.

    PubMed  Google Scholar 

  • Wülbeck, C., & Simpson, P. (2002). The expression of pannier and achaete–scute homologues in a mosquito suggests an ancient role of pannier as a selector gene in the regulation of the dorsal body pattern. Development, 129, 3861–3871.

    PubMed  Google Scholar 

  • Zhou, Q., Zhang, T., Xu, W., Yu, L., Yi, Y., & Zhang, Z. (2008). Analysis of four achaete–scute homologs in Bombyx mori reveals new viewpoints of the evolution and functions of this gene family. BMC Genetics, 9, 24. doi:10.1186/1471-2156-9-24.

    Article  PubMed  CAS  Google Scholar 

  • zur Lage, P. I., Prentice, D. R. A., Holohan, E. E., & Jarman, A. P. (2003). The Drosophila proneural gene amos promotes olfactory sensillum formation and suppresses bristle formation. Development, 130, 4683–4693. doi:10.1242/dev.00680.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

We thank the staff of the Keys Marine Laboratory (www.keysmarinelab.org) for supplying spiny lobsters and Dr. Timothy McClintock for many helpful discussions, advice, and assistance. This work was supported by NIH grant DC-00312 and the Georgia Research Alliance.

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  1. Neuroscience Institute and Department of Biology, Georgia State University, P.O. Box 5030, Atlanta, GA, 30302-5030, USA

    Hsin Chien, Tizeta Tadesse, Huijie Liu, Manfred Schmidt, W. William Walthall, Phang C. Tai & Charles D. Derby

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  1. Hsin Chien
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  2. Tizeta Tadesse
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  3. Huijie Liu
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  4. Manfred Schmidt
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  6. Phang C. Tai
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  7. Charles D. Derby
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Correspondence to Charles D. Derby.

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Chien, H., Tadesse, T., Liu, H. et al. Molecular Cloning and Characterization of Homologs of Achaete–Scute and Hairy–Enhancer of Split in the Olfactory Organ of the Spiny Lobster Panulirus argus . J Mol Neurosci 39, 294–307 (2009). https://doi.org/10.1007/s12031-009-9195-6

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