CRF-like diuretic hormone negatively affects both feeding and reproduction in the desert locust, Schistocerca gregaria

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  van Wielendaele, Pieter ^a   Dillen, Senne ^a   Marchal, Elisabeth ^a   Badisco, Liesbeth ^a   Vanden Broeck, Jozef ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CORTICOTROPIN RELEASING FACTOR; ECDYSTEROID; ISOPROTEIN; OMP ISOFORM; UNCLASSIFIED DRUG; DIURETIC AGENT; INSECT PROTEIN; MESSENGER RNA;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EXCRETION; FEMALE; FEMALE GENITAL SYSTEM; FOOD INTAKE; GENE SILENCING; GENETIC TRANSCRIPTION; HEMOLYMPH; HORMONAL REGULATION; HORMONE BLOOD LEVEL; LOCUST; MALE; NEGATIVE FEEDBACK; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; OVARY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE REAL TIME POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SATIETY; SCHISTOCERA GREGARIA; STEROIDOGENESIS; ANIMAL; CHEMISTRY; DESERT CLIMATE; DRUG EFFECT; FEEDING BEHAVIOR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GRASSHOPPER; INJECTION; METABOLISM; MOLECULAR GENETICS; OOCYTE; PHYSIOLOGY; REPRODUCTION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CONSERVED SEQUENCE; CORTICOTROPIN-RELEASING HORMONE; DESERT CLIMATE; DIURETICS; DNA, COMPLEMENTARY; FEEDING BEHAVIOR; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GRASSHOPPERS; INJECTIONS; INSECT PROTEINS; MALE; MOLECULAR SEQUENCE DATA; OOCYTES; REPRODUCTION; RNA INTERFERENCE; RNA, MESSENGER;

EID: 84857381364     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031425     Document Type: Article

References (78)

1. Gäde G, (2004) Regulation of intermediary metabolism and water balance of insects by neuropeptides. Annu Rev Entomol 49: 93-113.
2. Kataoka H, Troetschler RG, Li JP, Kramer SJ, Carney RL, et al. (1989) Isolation and identification of a diuretic hormone from the tobacco hornworm, Manduca sexta. Proc Natl Acad Sci U S A 86 (8): 2976-2980.
3. Furuya K, Schegg KM, Schooley DA, (1998) Isolation and identification of a second diuretic hormone from Tenebrio molitor. Peptides 19 (4): 619-626.
4. Baldwin DC, Schegg KM, Furuya K, Lehmberg E, Schooley DA, (2001) Isolation and identification of a diuretic hormone from Zootermopsis nevadensis. Peptides 22 (2): 147-152.
5. Te Brugge V, Paluzzi JP, Schooley DA, Orchard I, (2011) Identification of the elusive peptidergic diuretic hormone in the blood-feeding bug Rhodnius prolixus: a CRF-related peptide. J Exp Biol 214 (3): 371-381.
6. Kay I, Wheeler CH, Coast GM, Totty NF, Cusinato O, et al. (1991) Characterization of a diuretic peptide from Locusta migratoria. Biol Chem Hoppe Seyler 372 (10): 929-934.
7. Lehmberg E, Ota RB, Furuya K, King DS, Applebaum SW, et al. (1991) Identification of a diuretic hormone of Locusta migratoria. Biochem Biophys Res Commun 179 (2): 1036-1041.
8. Goldsworthy GJ, Owusu M, Ross KTA, Simmonds MSJ, Coast GM, et al.Roubos EW, Wendelaar Bonga SE, Vaudry H, De Loof A, (1999) Locusta CRF-related diuretic peptide is a factor mediating satiety in locusts. Recent developments in comparative endocrinology and neurobiology Maastricht Shaker Publishing BV pp. 231-234.
9. Goldsworthy GJ, Chung JS, Simmonds MSJ, Tatari M, Varouni S, et al. (2003) The synthesis of an analogue of the locust CRF-like diuretic peptide, and the biological activities of this and some C-terminal fragments. Peptides 24 (10): 1607-1613.
10. Audsley N, Goldsworthy GJ, Coast GM, (1997) Circulating levels of Locusta diuretic hormone: the effects of feeding. Peptides 18 (1): 59-65.
11. Audsley N, Goldsworthy GJ, Coast GM, (1997) Quantification of Locusta diuretic hormone in the central nervous system and corpora cardiaca: influence of age and feeding status, and mechanism of release. Regul Pept 69 (1): 25-32.
12. Gäde G, Goldsworthy GJ, (2003) Insect peptide hormones: a selective review of their physiology and potential application for pest control. Pest Manag Sci 59 (10): 1063-1075.
13. Digan ME, Roberts DN, Enderlin FE, Woodworth AR, Kramer SJ, (1992) Characterization of the precursor for Manduca sexta diuretic hormone Mas-DH. Proc Natl Acad Sci U S A 89 (22): 11074-11078.
14. Cabrero P, Radford JC, Broderick KE, Costes L, Veenstra JA, et al. (2002) The Dh gene of Drosophila melanogaster encodes a diuretic peptide that acts through cyclic AMP. J Exp Biol 205 (24): 3799-3807.
15. Roller L, Yamanaka N, Watanabe K, Daubnerová I, Zitnan D, et al. (2008) The unique evolution of neuropeptide genes in the silkworm Bombyx mori. Insect Biochem Mol Biol 38 (12): 1147-1157.
16. Hummon AB, Richmond TA, Verleyen P, Baggerman G, Huybrechts J, et al. (2006) From the genome to the proteome: uncovering peptides in the Apis brain. Science 314 (5799): 647-649.
17. Li B, Predel R, Neupert S, Hauser F, Tanaka Y, et al. (2008) Genomics, transcriptomics, and peptidomics of neuropeptides and protein hormones in the red flour beetle Tribolium castaneum. Genome Res 18: 113-122.
18. Tamarelle M, Coast GM, Veenstra JA, (2000) Ovary Maturing Parsin and Diuretic Hormone are produced by the same neuroendocrine cells in the migratory locust, Locusta migratoria. Peptides 21 (5): 737-739.
19. Girardie J, Richard O, Huet JC, Nespoulous C, Vandorsselaer A, et al. (1991) Physical characterization and sequence identification of the ovary maturating parsin - a new neurohormone purified from the nervous corpora cardiaca of the african locust (Locusta migratoria migratorioides). Eur J Biochem 202 (3): 1121-1126.
20. Girardie J, Geoffre S, Delbecque JP, Girardie A, (1998) Arguments for two distinct gonadotropic activities triggered by different domains of the ovary maturating parsin of Locusta migratoria. J Insect Physiol 44 (11): 1063-1071.
21. Girardie J, Girardie A, (1996) Lom OMP, a putative ecdysiotropic factor for the ovary in Locusta migratoria. J Insect Physiol 42 (3): 215-221.
22. Girardie J, Huet JC, Atay-Kadiri Z, Ettaouil S, Delbecque JP, et al. (1998) Isolation, sequence determination, physical and physiological characterization of the neuroparsins and ovary maturing parsins of Schistocerca gregaria. Insect Biochem Mol Biol 28 (9): 641-650.
23. Richard O, Tamarelle M, Girardie J, Geoffre S, (1994) Restricted occurrence of Locusta migratoria ovary maturing parsin in the brain-corpora cardiaca complex of various insect species. Histochemistry 102 (3): 233-239.
24. Badisco L, Huybrechts J, Simonet G, Verlinden H, Marchal E, et al. (2011) Transcriptome Analysis of the Desert Locust Central Nervous System: Production and Annotation of a Schistocerca gregaria EST Database. PLoS One 6 (3): e17274.
25. Uvarov B, Uvarov B, (1966) Phase polymorphism. Grasshoppers and locusts: a handbook of general acridology Cambridge Anti-Locust Research Centre (Cambridge University Press) pp. 332-386.
26. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3 (7): research0034-research0034.11.
27. Van Hiel MB, Van Wielendaele P, Temmerman L, Van Soest S, Vuerinckx K, et al. (2009) Identification and validation of housekeeping genes in brains of the desert locust Schistocerca gregaria under different developmental conditions. BMC Mol Biol 10: 56.
28. Tawfik AI, Vedrová A, Sehnal F, (1999) Ecdysteroids During Ovarian Development and Embryogenesis in Solitary and Gregarious Schistocerca gregaria. Arch Insect Biochem Physiol 41 (3): 134-143.
29. Porcheron P, Morinière M, Grassi J, Pradelles P, (1989) Development of an enzyme immunoassay for ecdysteroids using acetylcholinesterase as label. Insect Biochem 19: 117-122.
30. Pascual N, Bellés X, Delbecque JP, Hua YJ, Koolman J, (1995) Quantification of ecdysteroids by immunoassay: comparison of enzyme immunoassay and radioimmunoassay. Z Naturforsch C 50 (11-12): 862-867.
31. Tawfik AI, Vedrová A, Li W, Sehnal F, Obeng-Ofori D, (1997) Haemolymph ecdysteroids and the prothoracic glands in the solitary and gregarious adults of Schistocerca gregaria. J Insect Physiol 43 (5): 485-493.
32. Bendtsen JD, Nielsen H, von Heijne G, Brunak S, (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340 (4): 783-795.
33. Furutani Y, Morimoto Y, Shibahara S, Noda M, Takahashi H, et al. (1983) Cloning and sequence analysis of cDNA for ovine corticotropin-releasing factor precursor. Nature 301 (5900): 537-540.
34. Lu W, Dow L, Gumusgoz S, Brierley MJ, Warne JM, et al. (2004) Coexpression of corticotropin-releasing hormone and urotensin i precursor genes in the caudal neurosecretory system of the euryhaline flounder (Platichthys flesus): a possible shared role in peripheral regulation. Endocrinology 145 (12): 5786-5797.
35. Patel M, Chung JS, Kay I, Mallet AI, Gibbon CR, et al. (1994) Localization of Locusta-DP in locust CNS and hemolymph satisfies initial hormonal criteria. Peptides 15 (4): 591-602.
36. Richard O, Girardie J, (1992) Immunochemical analysis of the distribution of the new ovary maturating neurohormone during development of the African locust, Locusta migratoria. Cell Tissue Res 270 (3): 587-596.
37. Zitnan D, Sehnal F, Bryant PJ, (1993) Neurons producing specific neuropeptides in the central nervous system of normal and pupariation-delayed Drosophila. Dev Biol 156 (1): 117-135.
38. Chen Y, Veenstra JA, Hagedorn H, Davis NT, (1994) Leucokinin and diuretic hormone immunoreactivity of neurons in the tobacco hornworm, Manduca sexta and co-localization of this immunoreactivity in lateral neurosecretory cells of abdominal ganglia. Cell Tissue Res 278 (3): 493-507.
39. Te Brugge VA, Miksys SM, Coast GM, Schooley DA, Orchard I, (1999) The distribution of a CRF-like diuretic peptide in the blood-feeding bug Rhodnius prolixus. J Exp Biol 202 (15): 2017-2027.
40. Montuenga LM, Zudaire E, Prado MA, Audsley N, Burrell MA, et al. (1996) Presence of Locusta diuretic hormone in endocrine cells of the ampullae of locust Malpighian tubules. Cell Tissue Res 285 (2): 331-339.
41. Badisco L, Marchal E, Van Wielendaele P, Verlinden H, Vleugels R, et al. (2011) RNA interference of insulin-related peptide and neuroparsins affects vitellogenesis in the desert locust Schistocerca gregaria. Peptides 32 (3): 573-580.
42. Marchal E, Zhang J, Badisco L, Verlinden H, Hult EF, et al. (2011) Final steps in juvenile hormone biosynthesis in the desert locust, Schistocerca gregaria. Insect Biochem Mol Biol 41 (4): 219-227.
43. van Hoef V, Breugelmans B, Spit J, Simonet G, Zels S, et al. (2011) Functional analysis of a pancreatic secretory trypsin inhibitor-like protein in insects: Silencing effects resemble the human pancreatic autodigestion phenotype. Insect Biochem Mol Biol 41 (9): 688-695.
44. Wei Z, Baggerman G, Nachman RJ, Goldsworthy G, Verhaert P, et al. (2000) Sulfakinins reduce food intake in the desert locust, Schistocerca gregaria. J Insect Physiol 46 (9): 1259-1265.
45. Downer KE, Haselton AT, Nachman RJ, Stoffolano JG, (2007) Insect satiety: sulfakinin localization and the effect of drosulfakinin on protein and carbohydrate ingestion in the blow fly, Phormia regina (Diptera: Calliphoridae). J Insect Physiol 53 (1): 106-112.
46. Keeley LL, Chung JS, Hayes TK, (1992) Diuretic and antifeedant actions by Manduca sexta diuretic hormone in lepidopteran larvae. Cell Mol Life Sci 48 (11-12): 1145-1148.
47. Ma M, Emery SB, Wong W-KR, De Loof A, (2000) Effects of Manduca Diuresin on Neonates of the Tobacco Hornworm, Manduca sexta. Gen Comp Endocrinol 118 (1): 1-7.
48. Chapman RF, (2003) Contact chemoreception in feeding by phytophagous insects. Annu Rev Entomol 48: 455-484.
49. Takken W, Knols BG, (1999) Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 44: 131-157.
50. Wada-Katsumata A, Silverman J, Schal C, (2011) Differential Inputs from Chemosensory Appendages Mediate Feeding Responses to Glucose in Wild-Type and Glucose-Averse German Cockroaches Blattella germanica. Chem Senses 36 (7): 589-600.
51. Glinwood R, Ahmed E, Qvarfordt E, Ninkovic V, (2011) Olfactory learning of plant genotypes by a polyphagous insect predator. Oecologia 166 (3): 637-647.
52. Opstad R, Rogers SM, Behmer ST, Simpson SJ, (2004) Behavioural correlates of phenotypic plasticity in mouthpart chemoreceptor numbers in locusts. J Insect Physiol 50 (8): 725-736.
53. Turner SL, Li N, Guda T, Githure J, Cardé RT, et al. (2001) Ultra-prolonged activation of CO2-sensing neurons disorients mosquitoes. Nature 474 (7349): 87-91.
54. Ignell R, Root CM, Birse RT, Wang JW, Nässel DR, et al. (2009) Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. Proc Natl Acad Sci U S A 106 (31): 13070-13075.
55. Winther AM, Acebes A, Ferrús A, (2006) Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila. Mol Cell Neurosci 31 (3): 399-406.
56. Root CM, Ko KI, Jafari A, Wang JW, (2011) Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145 (1): 133-144.
57. López-Arias B, Dorado B, Herrero P, (2011) Blockade of the release of the neuropeptide leucokinin to determine its possible functions in fly behavior: chemoreception assays. Peptides 32 (3): 545-552.
58. Al-Anzi B, Armand E, Nagamei P, Olszewski M, Sapin V, et al. (2010) The leucokinin pathway and its neurons regulate meal size in Drosophila. Curr Biol 20 (11): 969-978.
59. Coast GM, Chung JS, Goldsworthy GJ, Patel M, Hayes TK, et al.Davey KG, Peters RE, Tobe SS, (1994) Corticotropin releasing factor related diuretic peptides in locusts. Perspectives in Comparative Endocrinology Ottawa National Research Council of Canada pp. 67-73.
60. Johnson EC, Bohn LM, Taghert PH, (2004) Drosophila CG8422 encodes a functional diuretic hormone receptor. J Exp Biol 207 (5): 743-748.
61. Hector CE, Bretz CA, Zhao Y, Johnson EC, (2009) Functional differences between two CRF-related diuretic hormone receptors in Drosophila. J Exp Biol 212 (19): 3142-3147.
62. Arase K, Shargill NS, Bray GA, (1989) Effects of corticotropin releasing factor on genetically obese (fatty) rats. Physiol Behav 45 (3): 565-570.
63. Stengel A, Goebel M, Million M, Stenzel-Poore MP, Kobelt P, et al. (2009) Corticotropin-releasing factor-overexpressing mice exhibit reduced neuronal activation in the arcuate nucleus and food intake in response to fasting. Endocrinology 150 (1): 153-160.
64. Matsuda K, Kang KS, Sakashita A, Yahashi S, Vaudry H, (2011) Behavioral effect of neuropeptides related to feeding regulation in fish. Ann N Y Acad Sci 1220: 117-126.
65. Ronan PJ, Summers CH, (2011) Molecular signaling and translational significance of the corticotropin releasing factor system. Prog Mol Biol Transl Sci 98: 235-292.
66. Van Huis A, Woldewahid G, Toleubayev K, Van Der Werf W, (2008) Relationships between food quality and fitness in the desert locust, Schistocerca gregaria, and its distribution over habitats on the Red Sea coastal plain of Sudan. Entomologia Experimentalis et Applicata 127 (2): 144-156.
67. Maeno K, Tanaka S, (2011) Phase-specific responses to different qualities of food in the desert locust, Schistocerca gregaria: Developmental, morphological and reproductive characteristics. J Insect Physiol 57 (4): 514-520.
68. Hatle JD, Waskey T, Juliano SA, (1979) Plasticity of grasshopper vitellogenin production in response to diet is primarily a result of changes in fat body mass. J Insect Physiol 25 (9): 701-708.
69. Cooper RA, Schal C, (1992) Differential Development and Reproduction of the German Cockroach (Dictyoptera: Blatlellidae) on Three Laboratory Diets. J Econ Entomol 85 (3): 838-844.
70. Shobana K, Murugan K, Naresh Kumar A, (2010) Influence of host plants on feeding, growth and reproduction of Papilio polytes (The common mormon). J Insect Physiol 56 (9): 1065-1070.
71. Bonte M, De Clercq P, (2008) Developmental and reproductive fitness of Orius laevigatus (Hemiptera: Anthocoridae) reared on factitious and artificial diets. J Econ Entomol 101 (4): 1127-1133.
72. Li XF, Knox AM, O'Byrne KT, (2010) Corticotrophin-releasing factor and stress-induced inhibition of the gonadotrophin-releasing hormone pulse generator in the female. Brain Res 1364: 153-163.
73. Ferin M, (1993) Neuropeptides, the stress response, and the hypothalamo-pituitary-gonadal axis in the female rhesus monkey. Ann N Y Acad Sci 697: 106-116.
74. Kozlova T, Thummel CS, (2003) Essential Roles for Ecdysone Signaling During Drosophila Mid-Embryonic Development. Science 301 (5641): 1911-1914.
75. Yamada R, Yamahama Y, Sonobe H, (2005) Release of ecdysteroid-phosphates from egg yolk granules and their dephosphorylation during early embryonic development in silkworm, Bombyx mori. Zoolog Sci 22 (2): 187-198.
76. Bownes M, Shirras A, Blair M, Collins J, Coulson A, (1988) Evidence that insect embryogenesis is regulated by ecdysteroids released from yolk proteins. Proc Natl Acad Sci U S A 85 (5): 1554-1557.
77. Isaac RE, Rees HH, (1984) Isolation and identification of ecdysteroid phosphates and acetylecdysteroid phosphates from developing eggs of the locust, Schistocerca gregaria. Biochem J 221 (2): 459-464.
78. Hatle JD, Juliano SA, Borst DW, (2003) Hemolymph ecdysteroids do not affect vitellogenesis in the lubber grasshopper. Arch Insect Biochem Physiol 52 (1): 45-57.