Proteomic analysis of insecticide triazophos-induced mating-responsive proteins of Nilaparvata lugens Stål (Hemiptera: Delphacidae)

Journal of Proteome Research

Volumn 10, Issue 10, 2011, Pages 4597-4612

  Ge, Lin Quan ^a   Cheng, Yao ^a   Wu, Jin Cai ^a   Jahn, Gary C ^b  

^a YANGZHOU UNIVERSITY   (China)

^b GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

2 DE; LC MS MS; mating; Nilaparvata lugens; proteomics; reproductive response; triazophos

Indexed keywords

ACTIN; ACTIN 5C; ARGININE KINASE; INSECT PROTEIN; MATING RESPONSIVE PROTEIN; NYD SP6 PROTEIN; OVARIAN SERINE PROTEASE; REPRODUCTIVE PROTEIN; SPERMATOGENESIS ASSOCIATED PROTEIN 5; TRIAZOPHOS; UNCLASSIFIED DRUG; VITELLOGENIN;

ACCESSORY SEX GLAND; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FERTILITY; HEMIPTERA; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MATING; NILAPARVATA LUGENS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY; REPRODUCTION; SPERMATOGENESIS; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION;

ANIMALS; CHROMATOGRAPHY, LIQUID; DNA PRIMERS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; GENE EXPRESSION PROFILING; HEMIPTERA; INSECTICIDES; MALE; MASS SPECTROMETRY; PROTEINS; PROTEOME; PROTEOMICS; REAL-TIME POLYMERASE CHAIN REACTION; THIOPHOSPHORIC ACID ESTERS; TRIAZOLES;

DELPHACIDAE; HEMIPTERA; NILAPARVATA LUGENS;

EID: 80053925036     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200414g     Document Type: Article

References (74)

1. Heinrichs, E. A. Impact of insecticides on the resistance and resurgence of rice planthoppers. In Planthoppers: Their Ecology and Management; Denno, R. F. and Perfect, T. J., Eds.; Chapman and Hall Press: New York, 1994; pp 571-614.
2. Gao, C. X.; Gu, X. H.; Bei, Y. W.; Wang, R. M. Approach of causes on brown planthopper resurgence Acta Ecol. Sin. 1988, 8, 155-163
3. Chelliah, S.; Heinrichs, E. A. Factors affecting insecticide-induced resurgence of the brown planthopper, Nilaparvata lugens on rice Environ. Entomol. 1980, 9, 773-777
4. Wang, L. P.; Shen, J.; Ge, L. Q.; Wu, J. C.; Yang, G. Q.; Jahn, G. C. Insecticide-induced increase in the protein content of male accessory glands and its effect on the fecundity of females in the brown planthopper Nilaparvata lugens Stål (Hemiptera: Delphacidae) Crop Prot. 2010, 29, 1280-1285
5. Ge, L. Q.; Wang, L. P.; Zhao, K. F.; Wu, J. C.; Huang, L. J. Mating pair combinations of insecticide-treated male and female Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) planthoppers influence protein content in the male accessory glands (MAGs) and vitellin content in both fat bodies and ovaries of adult females Pestic. Biochem. Physiol. 2010, 98, 279-288
6. Chen, P. S. The functional morphology and biochemistry of insect male accessory glands and their secretions Annu. Rev. Entomol. 1984, 2, 233-255
7. Kalb, J. M.; Dibenedetto, A. J.; Wolfner, M. F. Probing the function of Drosophila melanogaster accessory glands by directed cell ablation Proc. Natl. Acad. Sci. U. S. A. 1993, 90, 8093-8097 (Pubitemid 23260861)
8. Aigaki, T.; Fleischmann, I.; Chen, P. S.; Kubli, E. Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster Neuron 1991, 7, 557-563
9. Chen, P. S.; Stumm-Zollinger, E.; Aigaki, T.; Balmer, J.; Bienz, M.; Bohler, P. A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster Cell 1988, 54, 291-298
10. Gillott, C. Male accessory gland secretions: modulators of female reproductive physiology and behavior Annu. Rev. Entomol. 2003, 48, 163-184 (Pubitemid 37365390)
11. Lay, M.; Loher, W.; Hartmann, R. Pathways and destination of some male gland secretions in female Locusta migratoria migratorioides (R&F) after insemination Arch. Insect Biochem. Physiol. 2004, 55, 1-25 (Pubitemid 38592047)
12. Komatsu, S.; Rakwal, R.; Li, Z. Separation and characterization of proteins in rice (Oryza sativa) suspension cultured cells Plant Cell, Tissue Organ Cult. 1999, 55, 183-192
13. Antelman, H.; Scharf, C.; Hecker, M. Phosphate starvation inducible proteins in Bacilus subtilis: proteomics and transcriptional analysis J. Bacteriol. 2000, 182, 4478-4490 (Pubitemid 30599811)
14. Konishi, H.; Ishiguro, K.; Komatsu, S. A proteomics approach towards understanding blast fungus infection in rice grown under different levels of nitrogen fertilization Proteomics 2001, 1, 1162-1171 (Pubitemid 33696481)
15. Chen, G.; Gharib, T. G.; Huang, C. C.; Thomas, D. G.; Sheddan, K. A.; Taylor, J. M. G.; Kardia, S. L. R.; Misek, D. E.; Giordano, T. J. Proteomic analysis of lung adenocarcinoma: identification of a highly expressed set of proteins in tumors Clin. Cancer Res. 2002, 8, 2298-2305 (Pubitemid 34753604)
16. Natera, S. H.; Guerreiro, N.; Djordjevic, M. A. Proteome analysis of differentially displayed proteins as a tool for investigation of symbiosis Mol. Plant-Microbe Interact. 2000, 13, 995-1009 (Pubitemid 30648047)
17. Ishimura, R.; Ohsako, S.; Kawakami, T.; Sakaue, M.; Aoki, Y.; Tohyama, C. Altered protein profile and possible hypoxia in the placenta of 2,3,7,8-tetrachlorodibenzo- p -dioxin-exposed rats Toxicol. Appl. Pharmacol. 2002, 185, 197-206 (Pubitemid 36062793)
18. Adachi, J.; Kunmar-Kunmar, C.; Zhang, Y.; Olsen, J. V.; Mann, M. The human urinary proteome contains more than 1500 proteins, including a large proportion of membrane proteins Genome Biol. 2006, 7, R80
19. Zhou, Z. H.; Yang, H. J.; Chen, M.; Lou, C. F.; Zhang, Y. Z.; Chen, K. P.; Wang, Y.; Yu, M. L.; Yu, F.; Li, J. Y.; Zhong, B. X. Comparative proteomic analysis between the domesticated silkworm (Bombyx mori) reared on fresh mulberry leaves and on artificial diet J. Proteome Res. 2008, 7, 5103-5011
20. Hossein Mohaddam, S.; Du, X.; Li, J.; Cao, J. R.; Zhong, B. X.; Chen, Y. Y. Proteome analysis on differentially expressed proteins of the fat body of two silkworm breeds, Bombyx mori, exposed to heat shock exposure Biotechnol. Bioprocess Eng. 2008, 13, 624-631
21. de Souza, G. A.; Godoy, L. M.; Mann, M. Identification of 491 proteins in the tear fluid proteome reveals a large number of proteases and protease inhibitors Genome Biol. 2006, 7, R72
22. Li, J. Y.; Chen, X.; Fan, W.; Hosseini Moghaddam, S. H.; Chen, M.; Zhou, Z. H.; Yang, H. J.; Chen, J. E.; Zhong, B. X. Proteomic and bioinformatic analysis on endocrine organs of domesticated silkworm, Bombyx mori for a comprehensive understanding of their roles and relateions J. Proteome Res. 2009, 8, 2620-2632
23. Li, J. Y.; Chen, X.; Hosseini Moghaddam, S. H.; Chen, M.; Wei, H.; Zhong, B. X. Shortgun proteomics approach to characterizing the embryonic proteome of silkworm, Bombyx mori, at labrum appearance stage Insect Mol. Biol. 2009, 18, 649-660
24. Azzam, S.; Wang, F.; Wu, J. C.; Shen, J.; Wang, L. P.; Yang, G. Q.; Guo, H. R. Comparisons of stimulatory effects of a series of concentrations of four insecticides on reproduction in the rice brown planthopper Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) Int. J. Pest Manage. 2009, 55, 347-358
25. Dai, H. G.; Wu, X. Y.; Feng, C. J.; Yang, Y. H. The relationship between mating behaviour and titer of juvenile hormone in brown planthopper, Nilaparvata lugens (Stål) Acta Entomol. Sin. 1997, 40, 153-158
26. -ΔΔCT method Methods 2001, 25, 402-408 (Pubitemid 34164012)
27. Noda, H.; Kawai, S.; Koizumi, Y.; Matsui, K.; Zhang, Q.; Furukawa, S.; Shimomura, M.; Mita, K. Annotated ESTs from various tissues of the brown planthopper Nilaparvata lugens: A genomic resource for studying agricultural pests BMC Genomics 2008, 9, 117
28. Xue, J.; Bao, Y. Y.; Li, B. L.; Cheng, Y. B.; Peng, Z. Y.; Liu, H.; Xu, H. J.; Zhu, Z. R.; Lou, Y. G.; Cheng, J. A.; Zhang, C. X. Transcriptome analysis of the brown planthopper Nilaparvata lugens PLoS One 2010, 5 (12) e14233 10.137/journal.pone.001423
29. Sharma, R.; Komatsu, S.; Noda, H. Proteomic analysis of brown planthopper: application to the study of carbamate toxicity Insect Biochem. Mol. Biol. 2004, 34, 425-432 (Pubitemid 38527138)
30. Zhao, K. F.; Shi, Z. P.; Wu, J. C. Insecticide-induced enhancement of flight capacity of the brown planthopper Nilaparvata lugens Stål (Hemiptera: Delphacidae) Crop Prot. 2011, 30, 475-482
31. Shen, L.; Cheng, X. N. The effect of migration on reproduction of Nilaparvata lugens (Stål). J. Nanjing Agric. Univ. 1998, 21, 31-35.
32. Phelan, P. L.; Barker, J. C. Male size related to courtship success and intersexual selection on tobacco moth Ephesia cautella Experientia 1986, 42, 1291-1293
33. Bissoondath, C. J.; Wiklund, C. Effect of male mating history and body size on ejaculate size and quantity in two polyandrous butterflies, Pieris napi and Pieris rapae (Lepidoptera: Pieridae) Funct. Ecol. 1996, 10, 457-464
34. Ponlawat, A.; Harrington, L. C. Age and body size influence male sperm capacity of the dengue vector Aedes aegypti (Diptera: Culicidae) J. Med. Entomol. 2007, 44, 422-426 (Pubitemid 46842138)
35. Russel, L. D. Morphological and functional evidence for Sertoli-germ cell relationship. In The Sertoli Cell; Russel, L. D.; Griswold, M. D., Eds.; Cache River Press: Clearwater, FL, 1993; pp 65-390.
36. Kuubli, E. Sex-peptides: seminal peptides of the Drosophila male Cell. Mol. Life Sci. 2003, 60, 1689-1704
37. Wolfner, M. F. The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila Heredity 2002, 88, 85-93 (Pubitemid 34196700)
38. Swanson, W. J.; Vacquier, V. D. The rapid evolution of reproductive proteins Nat. Rev. Genet. 2002, 3, 137-144 (Pubitemid 34506597)
39. Chapman, T. Seminal fluid-mediated fitness traits in Drosophila Heredity 2001, 87, 511-521 (Pubitemid 34067638)
40. McGraw, L. A.; Gibson, G.; Clark, A. G.; Wolfner, M. F. Genes regulated by mating, sperm or seminal proteins in mated female Drosophila melanogaster Curr. Biol. 2004, 14, 1509-1514 (Pubitemid 39123751)
41. Xiao, J. H.; Xu, M.; Li, J. M.; Chan, H. C.; Lin, M.; Zhu, H.; Zhang, W.; Zhou, M.; Zhao, B.; Sha, J. H. NYD-SP6, a novel gene potentially involved in regulating testicular development/spermatogenesis Biochem. Biophys. Res. Commun. 2002, 291, 101-110 (Pubitemid 34681144)
42. Seth, R. K.; Kaur, J. J.; Reynolds, S. E. Sperm transfer during mating, movement of sperm in the female reproductive tract, and sperm precedence in the common cutworm Spodoptera litura Physiol. Entomol. 2002, 27, 1-14 (Pubitemid 34267845)
43. Fujisawa, M.; Yamanaka, K.; Tanaka, H.; Okada, H.; Arakawa, S.; Kamidono, S. Expression of endothelial nitric oxide synthase in the sertoli cells of men with infertility of various causes BJU Int. 2001, 87, 85-88
44. Zhang, H.; Zheng, R. L. Possible role of nitric oxide on fertile and asthenozoospermic infertile human sperm functions Free Radical Res. 1996, 25, 347-354 (Pubitemid 26354246)
45. Yamamoto, I.; Tomizawa, M.; Saito, T.; Miyamoto, T.; Walcott, E. C.; Sumikawa, K. Structural factors contributing to insecticidal selective actions of neonicotinoids Arch. Insect Biochem. Physiol. 1998, 37, 24-32 (Pubitemid 128436943)
46. Byrne, B. M.; Gruber, M.; Ab, G. The evolution of egg yolk proteins Prog. Biophys. Mol. Biol. 1989, 53, 33-69
47. Raikhel, A. S.; Dhadialla, T. S. Accumulation of yolk proteins in insect oocytes Annu. Rev. Entomol. 1992, 37, 217-251
48. Hagedorn, H. H.; Maddison, D. R.; Tu, Z. The evolution of vitellogenins, cyclorrhaphan yolk proteins and related molecules Adv. Insect Physiol. 1998, 27, 335-384
49. Snigirevskaya, E. S.; Raikhel, A. S. Receptor-mediated endocytosis of yolk proteins in insect oocytes. In Progress in Vitellogenesis; Raikhel, A. S.; Sappington, T. W., Eds.; Reproductive Biology of Vertebrates; Adiyodi, K. G.; Adiyodi, R. G., Eds.; Science Publishers, Inc.: Enfield, NH, Plymouth, U.K., 2005; Vol XII, Part B, pp 199-228.
50. Tufail, M.; Takeda, M. Insect vitellogenin/lipophorin receptors: molecular structures, role in oogenesis, and regulatiory mechanisms J. Insect Physiol. 2009, 55, 87-103
51. Tufail, M.; Naeemullah, M.; Elmogy, M.; Sharma, P. N.; Takeda, M.; Nakamura, C. Molecular cloning, transcriptional regulation, and differential expression profiling of vitellogenin in two wing-morphs of the brown planthopper, Nilaparvata lugens Stål (Hemiptera: Delphacidae) Insect Mol. Biol. 2010, 19, 787-798
52. Ge, L. Q.; Wu, J. C.; Zhao, K. F.; Chen, Y.; Yang, G. Q. Induction of Nlvg and suppression of Nljhe gene expression in Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) adult females and males exposed to two insecticides Pestic. Biochem. Physiol. 2010, 98, 269-278
53. Bao, Y. Y.; Li, L.; Liu, Z. B.; Xue, J.; Zhu, Z. R.; Cheng, J. A.; Zhang, C. X. Triazophos up-regulated expression in the female brown planthooper, Nilaparvata lugens J. Insect Physiol. 2010, 56, 1087-1094
54. Cloutier, C.; Duperron, J.; Tertuliano, M.; McNeil, J. N. Host instar, body size and fitness in the koinobiotic parastoid Aphidius negripes Entomol. Exp. Appl. 2000, 97, 29-40
55. García-Barros, E. Body size, egg size, and their interspecific relationships with ecological and life history traits in butterflies (Lepidoptera: Papilionoidea, Hesperioidea) Biol. J. Linn. Soc. 2000, 70, 251-284 (Pubitemid 30656626)
56. Iyengar, V.; Eisner, T. Parental body mass as a determinant of egg size and egg output in an arctiid moth (Utetheisa ornatrix) J. Insect Behav. 2002, 15, 309-318 (Pubitemid 34850448)
57. Schüpbach, T.; Clifford, R. J.; Manseau, L. J.; Price, J. V. Dorsoventral signaling processes in Drosophila oogenesis. In Cell-Cell Interactions in Early Development; Gerhart, J., Ed.; Wiley-Liss: New York, 1991; pp 163-174.
58. Stein, D.; Roth, S.; Vogelsang, E.; Nüsslein-Volhard, C. The polarity of the dorsoventral axis in the Drosophila embryo is defined by an extracellular signal Cell 1991, 65, 429-440
59. Hong, C. C.; Hashimoto, C. An unusual mosaic protein with a protease domain, encoded by the nudel gene, is involoved in defining embryonic dorsoventral polarity in Drosophila Cell 1995, 82, 785-794
60. Lemosy, E. K.; Kemler, D.; Hashimoto, C. Role of nudel protease activation in triggering dorsoventral polarization of the Drosophila embryo Development 1998, 125, 4045-4053 (Pubitemid 28515442)
61. Bensaude, O.; Pinto, M.; Dubois, M. F.; Vanrung, N.; Morange, M. Protein denaturation during heat shock and related stress. In Stress Proteins: Induction and Function; Schlesinger, M. J.; Santoro, M. G.; Garaci, E., Eds.; Springer-Verlag: Berlin, Germany, 1990; pp 89-99.
62. Ohtsuka, K.; Hata, M. Molecular chaperone function of mammalian Hsp 70 and Hsp 40, a review Int. J. Hyperthermia 2000, 16, 231-245 (Pubitemid 30391859)
63. Canback, B.; Andwesson, S. G. E.; Kurland, C. G. The global phylogeny of glycolytic enzymes Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 6097-6012
64. Small, G. J.; Hemingway, J. Molecular characterization of the amplified carboxylesterase gene associated with organophosphorus insecticide resistance in the brown planthopper, Nilaparvata lugens Insect Mol. Biol. 2000, 9, 647-653 (Pubitemid 32040054)
65. Wyatt, G. R. The biochemistry of sugars and polysaccharides in insects Adv. Insect Physiol. 1967, 4, 287-360
66. Kikawada, T.; Saito, A.; Kanamori, Y.; Nakahara, Y.; Lwata, K.; Tanaka, D.; Watanabe, M.; Okuda, T. Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 11585-11590 (Pubitemid 47175056)
67. Cuber, R.; Eleutherio, E. C. A.; Pereira, M. D.; Panek, A. D. The role of the trehalose transporter during germination Biochim. Biophys. Acta 1997, 1330, 165-171 (Pubitemid 27522773)
68. Yin, J. L.; Xu, H. W.; Wu, J. C.; Hu, J. H.; Yang, G. Q. Cultivar and insecticide applications affect the physiological development of the brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) Environ. Entomol. 2008, 37, 206-212
69. Hamilton, C. A.; Good, A. G.; Taylor, G. J. Induction of vacuolar ATPase and mitochondrial ATP synthase by aluminium in aluminium-resistant cultivar of wheat Plant Phyiol. 2001, 125, 2068-2077 (Pubitemid 32375788)
70. Silvia, V.; Brown, B.; Stanislawski, A.; Quinesha, L.; Williams, P. N. Cloning and characterization of the subunits comprising the catalytic core of Trypanosaoma brucei mitochondrial ATP synthase Mol. Biochem. Parasitol. 2011, 113, 289-301
71. Parker, G. A. Sexual selection and sexual conflict. In Sexual Selection and Reproductive Competition in Insects; Blum, M. S.; Blum, N. A., Eds.; Academic: New York, 1979; pp 123-166.
72. Rice, W. R. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution Nature 1996, 361, 232-234
73. Parker, G. A. Sperm competition and its evolutionary consequences in the insects Biol. Rev. 1970, 45, 525-567
74. Eberhard, W. G. Female Control: Sexual Selection by Cryptic Female Choice; Princeton University Press: Princeton, NJ, 1996.