What the loss of the hormone neuroparsin in the melanogaster subgroup of Drosophila can tell us about its function

Insect Biochemistry and Molecular Biology

Volumn 40, Issue 4, 2010, Pages 354-361

  Veenstra, Jan A ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Development; Metamorphosis; Reproduction

Indexed keywords

INSECT HORMONE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BIOLOGY; DROSOPHILA; GENE; GENETIC TRANSFORMATION; GENETICS; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; COMPUTATIONAL BIOLOGY; DROSOPHILA; GENES, INSECT; INSECT HORMONES; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; TRANSFORMATION, GENETIC;

DROSOPHILA ANANASSAE; DROSOPHILA AURARIA; DROSOPHILA MELANOGASTER; ENDOPTERYGOTA; EXOPTERYGOTA; MELANOGASTER SUBGROUP;

EID: 77950461285     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2010.03.001     Document Type: Article

References (44)

1. Adams M.D., Celniker S.E., Holt R.A., Evans C.A., Gocayne J.D., Amanatides P.G., Scherer S.E., Li P.W., Hoskins R.A., Galle R.F., George R.A., Lewis S.E., Richards S., Ashburner M., Henderson S.N., Sutton G.G., Wortman J.R., Yandell M.D., Zhang Q., Chen L.X., Brandon R.C., Rogers Y.H., Blazej R.G., Champe M., Pfeiffer B.D., Wan K.H., Doyle C., Baxter E.G., Helt G., Nelson C.R., Gabor G.L., Abril J.F., Agbayani A., An H.J., Andrews-Pfannkoch C., Baldwin D., Ballew R.M., Basu A., Baxendale J., Bayraktaroglu L., Beasley E.M., Beeson K.Y., Benos P.V., Berman B.P., Bhandari D., Bolshakov S., Borkova D., Botchan M.R., Bouck J., Brokstein P., Brottier P., Burtis K.C., Busam D.A., Butler H., Cadieu E., Center A., Chandra I., Cherry J.M., Cawley S., Dahlke C., Davenport L.B., Davies P., de Pablos B., Delcher A., Deng Z., Mays A.D., Dew I., Dietz S.M., Dodson K., Doup L.E., Downes M., Dugan-Rocha S., Dunkov B.C., Dunn P., Durbin K.J., Evangelista C.C., Ferraz C., Ferriera S., Fleischmann W., Fosler C., Gabrielian A.E., Garg N.S., Gelbart W.M., Glasser K., Glodek A., Gong F., Gorrell J.H., Gu Z., Guan P., Harris M., Harris N.L., Harvey D., Heiman T.J., Hernandez J.R., Houck J., Hostin D., Houston K.A., Howland T.J., Wei M.H., Ibegwam C., Jalali M., Kalush F., Karpen G.H., Ke Z., Kennison J.A., Ketchum K.A., Kimmel B.E., Kodira C.D., Kraft C., Kravitz S., Kulp D., Lai Z., Lasko P., Lei Y., Levitsky A.A., Li J., Li Z., Liang Y., Lin X., Liu X., Mattei B., McIntosh T.C., McLeod M.P., McPherson D., Merkulov G., Milshina N.V., Mobarry C., Morris J., Moshrefi A., Mount S.M., Moy M., Murphy B., Murphy L., Muzny D.M., Nelson D.L., Nelson D.R., Nelson K.A., Nixon K., Nusskern D.R., Pacleb J.M., Palazzolo M., Pittman G.S., Pan S., Pollard J., Puri V., Reese M.G., Reinert K., Remington K., Saunders R.D., Scheeler F., Shen H., Shue B.C., Sidén-Kiamos I., Simpson M., Skupski M.P., Smith T., Spier E., Spradling A.C., Stapleton M., Strong R., Sun E., Svirskas R., Tector C., Turner R., Venter E., Wang A.H., Wang X., Wang Z.Y., Wassarman D.A., Weinstock G.M., Weissenbach J., Williams S.M., Woodage T., Worley K.C., Wu D., Yang S., Yao Q.A., Ye J., Yeh R.F., Zaveri J.S., Zhan M., Zhang G., Zhao Q., Zheng L., Zheng X.H., Zhong F.N., Zhong W., Zhou X., Zhu S., Zhu X., Smith H.O., Gibbs R.A., Myers E.W., Rubin G.M., and Venter J.C. The genome sequence of Drosophila melanogaster. Science 287 (2000) 2185-2195
2. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
3. Badisco L., Claeys I., Van Loy T., Van Hiel M., Franssens V., Simonet G., and Vanden Broeck J. Neuroparsins, a family of conserved arthropod neuropeptides. Gen. Comp. Endocrinol. 153 (2007) 64-71
4. Bahn J.H., Lee G., and Park J.H. Comparative analysis of Pdf-mediated circadian behaviors between Drosophila melanogaster and D. virilis. Genetics 181 (2009) 965-975
5. Bendtsen J.D., Nielsen H., von Heijne G., and Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340 (2004) 783-795
6. Broughton S., Alic N., Slack C., Bass T., Ikeya T., Vinti G., Tommasi A.M., Driege Y., Hafen E., and Partridge L. Reduction of DILP2 in Drosophila triages a metabolic phenotype from lifespan revealing redundancy and compensation among DILPs. PLoS One 3 (2008) e3721 10.1371/journal.pone.0003721
7. Brown M.R., and Cao C. Distribution of ovary ecdysteroidogenic hormone I in the nervous system and gut of mosquitoes. J. Insect Sci. 1 (2001) 3
8. Brown M.R., Graf R., Swiderek K.M., Fendley D., Stracker T.H., Champagne D.E., and Lea A.O. Identification of a steroidogenic neurohormone in female mosquitoes. J. Biol. Chem. 273 (1998) 3967-3971
9. Brown M.R., Clark K.D., Gulia M., Zhao Z., Garczynski S.F., Crim J.W., Suderman R.J., and Strand M.R. An insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 5716-5721
10. Claeys I., Breugelmans B., Simonet G., Franssens V., Van Soest S., and Vanden Broeck J. Regulation of Schistocerca gregaria neuroparsin transcript levels by juvenile hormone and 20-hydroxyecdysone. Arch. Insect Biochem. Physiol. 62 (2006) 107-115
11. Clark A.G., Eisen M.B., Smith D.R., Bergman C.M., Oliver B., Markow T.A., Kaufman T.C., Kellis M., Gelbart W., Iyer V.N., Pollard D.A., Sackton T.B., Larracuente A.M., Singh N.D., Abad J.P., Abt D.N., Adryan B., Aguade M., Akashi H., Anderson W.W., Aquadro C.F., Ardell D.H., Arguello R., Artieri C.G., Barbash D.A., Barker D., Barsanti P., Batterham P., Batzoglou S., Begun D., Bhutkar A., Blanco E., Bosak S.A., Bradley R.K., Brand A.D., Brent M.R., Brooks A.N., Brown R.H., Butlin R.K., Caggese C., Calvi B.R., Bernardo de Carvalho A., Caspi A., Castrezana S., Celniker S.E., Chang J.L., Chapple C., Chatterji S., Chinwalla A., Civetta A., Clifton S.W., Comeron J.M., Costello J.C., Coyne J.A., Daub J., David R.G., Delcher A.L., Delehaunty K., Do C.B., Ebling H., Edwards K., Eickbush T., Evans J.D., Filipski A., Findeiss S., Freyhult E., Fulton L., Fulton R., Garcia A.C., Gardiner A., Garfield D.A., Garvin B.E., Gibson G., Gilbert D., Gnerre S., Godfrey J., Good R., Gotea V., Gravely B., Greenberg A.J., Griffiths-Jones S., Gross S., Guigo R., Gustafson E.A., Haerty W., Hahn M.W., Halligan D.L., Halpern A.L., Halter G.M., Han M.V., Heger A., Hillier L., Hinrichs A.S., Holmes I., Hoskins R.A., Hubisz M.J., Hultmark D., Huntley M.A., Jaffe D.B., Jagadeeshan S., Jeck W.R., Johnson J., Jones C.D., Jordan W.C., Karpen G.H., Kataoka E., Keightley P.D., Kheradpour P., Kirkness E.F., Koerich L.B., Kristiansen K., Kudrna D., Kulathinal R.J., Kumar S., Kwok R., Lander E., Langley C.H., Lapoint R., Lazzaro B.P., Lee S.J., Levesque L., Li R., Lin C.F., Lin M.F., Lindblad-Toh K., Llopart A., Long M., Low L., Lozovsky E., Lu J., Luo M., Machado C.A., Makalowski W., Marzo M., Matsuda M., Matzkin L., McAllister B., McBride C.S., McKernan B., McKernan K., Mendez-Lago M., Minx P., Mollenhauer M.U., Montooth K., Mount S.M., Mu X., Myers E., Negre B., Newfeld S., Nielsen R., Noor M.A., O'Grady P., Pachter L., Papaceit M., Parisi M.J., Parisi M., Parts L., Pedersen J.S., Pesole G., Phillippy A.M., Ponting C.P., Pop M., Porcelli D., Powell J.R., Prohaska S., Pruitt K., Puig M., Quesneville H., Ram K.R., Rand D., Rasmussen M.D., Reed L.K., Reenan R., Reily A., Remington K.A., Rieger T.T., Ritchie M.G., Robin C., Rogers Y.H., Rohde C., Rozas J., Rubenfield M.J., Ruiz A., Russo S., Salzberg S.L., Sanchez-Gracia A., Saran D.J., Sato H., Schaeffer S.W., Schatz M.C., Schlenke T., Schwartz R., Segarra C., Singh R.S., Sirot L., Sirota M., Sisneros N.B., Smith C.D., Smith T.F., Spieth J., Stage D.E., Stark A., Stephan W., Strausberg R.L., Strempel S., Sturgill D., Sutton G., Sutton G.G., Tao W., Teichmann S., Tobari Y.N., Tomimura Y., Tsolas J.M., Valente V.L., Venter E., Venter J.C., Vicario S., Vieira F.G., Vilella A.J., Villasante A., Walenz B., Wang J., Wasserman M., Watts T., Wilson D., Wilson R.K., Wing R.A., Wolfner M.F., Wong A., Wong G.K., Wu C.I., Wu G., Yamamoto D., Yang H.P., Yang S.P., Yorke J.A., Yoshida K., Zdobnov E., Zhang P., Zhang Y., Zimin A.V., Baldwin J., Abdouelleil A., Abdulkadir J., Abebe A., Abera B., Abreu J., Acer S.C., Aftuck L., Alexander A., An P., Anderson E., Anderson S., Arachi H., Azer M., Bachantsang P., Barry A., Bayul T., Berlin A., Bessette D., Bloom T., Blye J., Boguslavskiy L., Bonnet C., Boukhgalter B., Bourzgui I., Brown A., Cahill P., Channer S., Cheshatsang Y., Chuda L., Citroen M., Collymore A., Cooke P., Costello M., D'Aco K., Daza R., De Haan G., DeGray S., DeMaso C., Dhargay N., Dooley K., Dooley E., Doricent M., Dorje P., Dorjee K., Dupes A., Elong R., Falk J., Farina A., Faro S., Ferguson D., Fisher S., Foley C.D., Franke A., Friedrich D., Gadbois L., Gearin G., Gearin C.R., Giannoukos G., Goode T., Graham J., Grandbois E., Grewal S., Gyaltsen K., Hafez N., Hagos B., Hall J., Henson C., Hollinger A., Honan T., Huard M.D., Hughes L., Hurhula B., Husby M.E., Kamat A., Kanga B., Kashin S., Khazanovich D., Kisner P., Lance K., Lara M., Lee W., Lennon N., Letendre F., LeVine R., Lipovsky A., Liu X., Liu J., Liu S., Lokyitsang T., Lokyitsang Y., Lubonja R., Lui A., MacDonald P., Magnisalis V., Maru K., Matthews C., McCusker W., McDonough S., Mehta T., Meldrim J., Meneus L., Mihai O., Mihalev A., Mihova T., Mittelman R., Mlenga V., Montmayeur A., Mulrain L., Navidi A., Naylor J., Negash T., Nguyen T., Nguyen N., Nicol R., Norbu C., Norbu N., Novod N., O'Neill B., Osman S., Markiewicz E., Oyono O.L., Patti C., Phunkhang P., Pierre F., Priest M., Raghuraman S., Rege F., Reyes R., Rise C., Rogov P., Ross K., Ryan E., Settipalli S., Shea T., Sherpa N., Shi L., Shih D., Sparrow T., Spaulding J., Stalker J., Stange-Thomann N., Stavropoulos S., Stone C., Strader C., Tesfaye S., Thomson T., Thoulutsang Y., Thoulutsang D., Topham K., Topping I., Tsamla T., Vassiliev H., Vo A., Wangchuk T., Wangdi T., Weiand M., Wilkinson J., Wilson A., Yadav S., Young G., Yu Q., Zembek L., Zhong D., Zimmer A., Zwirko Z., Jaffe D.B., Alvarez P., Brockman W., Butler J., Chin C., Gnerre S., Grabherr M., Kleber M., Mauceli E.
12. Coast G.M., Orchard I., Philips J.E., and Schooley D.A. Insect diuretic and antidiuretic hormones. Adv. Insect Physiol. 29 (2002) 279-409
13. Eddy S.R. Profile hidden Markov models. Bioinformatics 14 (1998) 755-763
14. Finn R.D., Tate J., Mistry J., Coggill P.C., Sammut S.J., Hotz H.R., Ceric G., Forslund K., Eddy S.R., Sonnhammer E.L., and Bateman A. The Pfam protein families database. Nucleic Acids Res. 36 (2008) D281-D288
15. Fraser A. Neurosecretory cells in the brain of the larva of Lucilia caesar L. Nature 179 (1957) 257-258
16. Girardie J., Bourême D., Couillaud F., Tamarelle M., and Girardie A. Anti-juvenile hormone effect of neuroparsin A, a neuroprotein isolated from locust corpora cardiaca. Insect Biochem. 17 (1987) 977-983
17. Girardie J., Girardie A., Huet J.C., and Pernollet J.C. Amino acid sequence of locust neuroparsins. FEBS Lett. 245 (1989) 4-8
18. Gloor G.B., Preston C.R., Johnson-Schlitz D.M., Nassif N.A., Phillis R.W., Benz W.K., Robertson H.M., and Engels W.R. Type I repressors of P element mobility. Genetics 135 (1993) 81-95
19. Goltzené F., Holder F., Charlet M., Meister M., and Oka T. Immunocytochemical localization of Bombyx-PTTH-like molecules in neurosecretory cells of the brain of the migratory locust, Locusta migratoria. A comparison with neuroparsin and insulin-related peptide. Cell Tissue Res. 269 (1992) 133-140
20. Hauser F., Cazzamali G., Williamson M., Park Y., Li B., Tanaka Y., Predel R., Neupert S., Schachtner J., Verleyen P., and Grimmelikhuijzen C.J.P. A genome-wide inventory of neurohormone GPCRs in the red flour beetle Tribolium castaneum. Front. Neuroendocrinol. 29 (2008) 142-165
21. Horn C., and Wimmer E.A. A versatile vector set for animal transgenesis. Dev. Genes Evol. 210 (2000) 630-637
22. Hummon A.B., Richmond T.A., Verleyen P., Baggerman G., Huybrechts J., Ewing M.A., Vierstraete E., Rodriguez-Zas S.L., Schoofs L., Robinson G.E., and Sweedler J.V. From the genome to the proteome: uncovering peptides in the Apis brain. Science 314 (2006) 647-649
23. Ikeya T., Galic M., Belawat P., Nairz K., and Hafen E. Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr. Biol. 12 (2002) 1293-1300
24. Isabel G., Martin J.R., Chidami S., Veenstra J.A., and Rosay P. AKH-producing neuroendocrine cell ablation decreases trehalose and induces behavioral changes in Drosophila. Am. J. Physiol. Regul. Comp. Physiol. 268 (2005) R531-R538
25. Kim Y.J., Zitnan D., Galizia C.G., Cho K.H., and Adams M.E. A command chemical triggers an innate behavior by sequential activation of multiple peptidergic ensembles. Curr. Biol. 16 (2006) 1395-1407
26. Li B., Predel R., Neupert S., Hauser F., Tanaka Y., Cazzamali G., Williamson M., Arakane Y., Verleyen P., Schoofs L., Schachtner J., Grimmelikhuijzen C.J.P., and Park Y. Genomics, transcriptomics, and peptidomics of neuropeptides and protein hormones in the red flour beetle Tribolium castaneum. Genome Res. 18 (2008) 113-122
27. Mitsialis S.A., and Kafatos F.C. Regulatory elements controlling chorion gene expression are conserved between flies and moths. Nature 317 (1985) 453-456
28. Moreau R., Gourdoux L., and Girardie J. Neuroparsin - a new energetic neurohormone in the African locust. Arch. Insect Biochem. Physiol. 8 (1988) 135-145
29. Negre B., and Ruiz A. HOM-C evolution in Drosophila: is there a need for Hox gene clustering?. Trends Genet. 23 (2007) 55-59
30. Panov A.A. Comparison between pars intercerebralis neurosecretory cells of Glossina and those of other higher Diptera. J. Zool. 187 (1979) 455-463
31. Pevzner P., and Tesler G. Human and mouse genomic sequences reveal extensive breakpoint reuse in mammalian evolution. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 7672-7677
32. Raabe M. Insect Neurohormones (1982), Plenum Press, New York and London xvi+352 pp.
33. Ranz J.M., Maurin D., Chan Y.S., von Grotthuss M., Hillier L.W., Roote J., Ashburner M., and Bergman C.M. Principles of genome evolution in the Drosophila melanogaster species group. PLoS Biol. 5 (2007) e152 10.1371/journal.pbio.0050152
34. Roller L., Yamanaka N., Watanabe K., Daubnerová I., Zitnan D., Kataoka H., and Tanaka Y. The unique evolution of neuropeptide genes in the silkworm Bombyx mori. Insect Biochem. Mol. Biol. 38 (2008) 1147-1157
35. Shen H.-B., and Chou K.-C. Signal-3L: a 3-layer approach for predicting signal peptides. Biochem. Biophys. Res. Commun. 363 (2007) 297-303
36. Taghert P.H., and Veenstra J.A. Drosophila neuropeptide signaling. Adv. Genet. 49 (2003) 1-65
37. Tamarelle M., and Girardie J. Immunohistochemical investigation of locust neuroparsin-like substances in several insects, in some other invertebrates, and vertebrates. Histochemistry 91 (1989) 431-435
38. Tamura K., Subramanian S., and Kumar S. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol. Biol. Evol. 21 (2004) 36-44
39. Vanhems E., Delbos M., and Girardie J. Insulin and neuroparsin promote neurite outgrowth in cultured locust CNS. Eur. J. Neurosci. 2 (1990) 776-782
40. Veenstra J.A. Allatostatin C and its paralog allatostatin double C: the arthropod somatostatins. Insect Biochem. Mol. Biol. 39 (2009) 161-170
41. Veenstra J.A., Agricola H.-J., and Sellami A. Regulatory peptides in fruit fly midgut. Cell Tissue Res. 334 (2008) 499-516
42. Wegener C., and Gorbashov A. Molecular evolution of neuropeptides in the genus Drosophila. Genome Biol. 9 (2008) R131
43. Wernersson R. Virtual Ribosome - a comprehensive DNA translation tool with support for integration of sequence feature annotation. Nucleic Acids Res. 34 (2006) W385-W388
44. Xiong B., and Jacobs-Lorena M. Gut-specific transcriptional regulatory elements of the carboxypeptidase gene are conserved between black flies and Drosophila. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 9313-9317