Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T12:20:26.686Z Has data issue: false hasContentIssue false
  • English
  • Français

Insulin-like peptides regulate vitellogenesis and oviposition in the green lacewing, Chrysopa septempunctata

Published online by Cambridge University Press:  30 August 2016

T.T. Zhang ,
G.C. Zhang ,
F.F. Zeng ,
C.Y. Liu  and
J.J. Mao
T.T. Zhang
Affiliation:
School of Forestry, Northeast Forestry University, Harbin, Heilongjiang 150040, China
G.C. Zhang
Affiliation:
School of Forestry, Northeast Forestry University, Harbin, Heilongjiang 150040, China
F.F. Zeng
Affiliation:
Key Laboratory for Biology of Plant Diseases and Insect Pests, Ministry of Agriculture, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
C.Y. Liu
Affiliation:
Food Crops Institute, Hubei Academy of Agricultural Sciences, Wuhan 430064, China
J.J. Mao*
Affiliation:
Key Laboratory for Biology of Plant Diseases and Insect Pests, Ministry of Agriculture, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
*
*Author for correspondence Phone: +86 10 62815504 Fax: +86 10 82109714 E-mail: maojianjun0615@126.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Insulin-like peptides (ILPs) act through a conserved insulin signaling pathway and play crucial roles in insect metabolism, growth, reproduction, and aging. Application of bovine insulin is able to increase vitellogenin (Vg) mRNA and protein levels in female insects. Here, we first show that injection of bovine insulin into previtellogenic Chrysopa septempunctata female adults promoted ovarian growth, increased Vg protein abundance, elevated reproductive performance, and enhanced protease activity. These data suggested that ILPs play crucial roles in reproductive regulation of the green lacewing, C. septempunctata.

Keywords

Bovine insulinILPsreproductionChrysopa septempunctata
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 2 , April 2017 , pp. 148 - 154
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

T.T. Zhang and G.C. Zhang contributed equally to this work.

References

Bellés, X. (2005) Vitellogenesis directed by juvenile hormone. pp. 157–197 in Raikhel, A.S. (Eds) Reproductive Biology of Invertebrates, Progress in Vitellogenesis. USA/Plymouth, UK, Science Publishers, Enfield.Google Scholar
Bellés, X. & Maestro, J.L. (2005) Endocrine peptides and insect reproduction. Invertebrate Reproduction and Development 47, 23–37.Google Scholar
Brogiolo, W., Stocker, H., Ikeya, T., Rintelen, F., Fernandez, R. & Hafen, E. (2001) An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Current Biology 11, 213–221.Google Scholar
Brown, M.R., Clark, K.D., Gulia, M., Zhao, Z., Garczynski, S.F., Crim, J.W., Suderman, R.J. & Strand, M.R. (2008) An insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti . PNAS 105, 5716–5721.Google Scholar
Claeys, I., Simonet, G., Poels, J., Van Loy, T., Vercammen, L., De Loof, A. & Vanden Broeck, J. (2002) Insulin related peptides and their conserved signal transduction pathway. Peptides 23, 807–816.CrossRefGoogle ScholarPubMed
Garelli, A., Gontijo, A.M., Miguela, V., Caparros, E. & Dominguez, M. (2012) Imaginal discs secrete insulin-like peptide 8 to mediate plasticity of growth and maturation. Science 336, 579–592.Google Scholar
Garofalo, R.S. (2002) Genetic analysis of insulin signaling in Drosophila . Trends in Endocrinology & Metabolism 13, 156–162.CrossRefGoogle ScholarPubMed
Geminard, C., Rulifson, E.J. & Leopold, P. (2009) Remote control of insulin secretion by fat cells in Drosophila . Cell Metabolism 10, 199–207.Google Scholar
Goberdhan, D.C. & Wilson, C. (2003) The functions of insulin signaling: size isn't everything, even in Drosophila . Differentiation 71, 375–397.Google Scholar
Goodman, W.G. & Cusson, M. (2012) The juvenile hormones. pp. 310–365 in Gilbert, L.I. (Eds) Insect Endocrinology. Amsterdam, Elsevier.Google Scholar
Hartfelder, K. & Emlen, D.J. (2012) Endocrine control of insect polyphenism. pp. 464–522 in Gilbert, L.I. (Eds) Insect Endocrinology. Amsterdam, Elsevier.Google Scholar
Ikeya, T., Galic, M., Belawat, P., Nairz, K. & Hafen, E. (2002) Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila . Current Biology 12, 1293–1300.Google Scholar
Jindra, M., Palli, S.R. & Riddiford, L.M. (2013) The juvenile hormone signaling pathway in insect development. Annual Review of Entomology 58, 181–204.Google Scholar
Krieger, M.J.B., Jahan, N., Riehle, M.A., Cao, C. & Brown, M.R. (2004) Molecular characterization of insulin-like peptide genes and their expression in the African malaria mosquito, Anopheles gambiae . Insect Molecular Biology 13, 305–315.Google Scholar
Leplé, J.C., Bonadé-Bottino, M., Augustin, S., Pilate, G., Tân, D.L.V., Delplanque, A., Cornu, D. & Jouanin, L. (1995) Toxicity to Chrysomela tremulae (Coleoptera: chrysomelidae) of transgenic poplars expressing acysteine proteinase inhibitor. Molecular Breeding 1, 319–328.Google Scholar
Liu, F., Liu, C. & Zeng, F. (2013) Effects of an artificial diet on development, reproduction and digestive physiology of Chrysopa septempunctata . BioControl 58, 789–795.Google Scholar
Livak, K.J. & Schmittgen, S.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.Google Scholar
Masumura, M., Satake, S., Saegusa, H. & Mizoguchi, A. (2000) Glucose stimulates the release of bombyxin, an insulin-related peptide of the silkworm Bombyx mori . General and Comparative Endocrinology 118, 393–399.Google Scholar
Mochizuki, A. (1998) Characteristics of digestive proteases in the gut of some insect orders. Applied Entomology and Zoology 33, 401–408.CrossRefGoogle Scholar
Mohan, V. (2002) Which insulin to use? Human or animal? Current Science India 83, 1544–1547.Google Scholar
Mulligan, E.A., Ferry, N., Jouanin, L., Romeis, J. & Gatehouse, A.M.R. (2010) Characterisation of adult green lacewing (Chrysoperla carnea) digestive physiology: impact of a cysteine protease inhibitor and a synthetic pyrethroid. Pest Management Science 66, 325–336.Google Scholar
Nagasawa, H., Kataoka, H., Isogai, A., Tamura, S., Suzuki, H., Ishi-zaki, A., Mizoguchi, A., Fujishita, Y. & Suzuki, A. (1984) Isolation and some characterization of the prothoracicotropic hormone from Bombyx mori . General and Comparative Endocrinology 53, 143–152.Google Scholar
Nagata, K., Hatanaka, H., Kohda, D., Kataoka, H., Nagasawa, H., Isogai, A., Ishizaki, H., Suzuki, A. & Inagaki, F. (1995) Three-dimensional solution structure of bombyxin-II an insulin-like peptide of the silkmoth Bombyx mori: structural comparison with insulin and relaxin. Journal of Molecular Biology 253, 749–758.Google Scholar
Nijhout, H.F. (1994) Insect Hormones. Princeton University Press, Princeton, New Jersey.Google Scholar
Parthasarathy, R. & Palli, S.R. (2011) Molecular analysis of nutritional and hormonal regulation of female reproduction in the red flour beetle, Tribolium castaneum . Insect Biochemistry and Molecular Biology 41, 294–305.Google Scholar
Raikhel, A.S., Brown, M.R. & Belles, X. (2005) Hormonal control of reproductive processes. Pp. 433–491 in Gilbert, L.I., Iatrou, K. & Gill, S.S. (Eds) Comprehensive Molecular Insect Science. Boston, Elsevier.Google Scholar
Riddiford, L.M. (1994) Cellular and molecular actions of juvenile hormone I. general considerations and premetamorphic actions. Advances in Insect Physiology 24, 213–274.Google Scholar
Riehle, M.A., Fan, Y., Cao, C. & Brown, M.R. (2006) Molecular characterization of insulin-like peptides in the yellow fever mosquito, Aedes aegypti: expression, cellular localization, and phylogeny. Peptides 27, 2547–2560.Google Scholar
Satake, S., Masumura, M., Ishizaki, H., Nagata, K., Kataoka, H., Suzuki, A. & Mizoguchi, A. (1997) Bombyxin, an insulin-related peptide of insects, reduces the major storage carbohydrates in the silkworm Bombyx mori . Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology 118, 349–57.CrossRefGoogle ScholarPubMed
Satake, S., Nagata, K., Kataoka, H. & Mizoguchi, A. (1999) Bombyxin secretion in the adult silkmoth Bombyx mori: sex-specificity and its correlation with metabolism. Journal of Insect Physiology 45, 939–45.Google Scholar
Sheng, Z., Xu, J. & Bai, H. (2011) Juvenile hormone regulates vitellogenin gene expression through insulin-like peptide signaling pathway in the red flour beetle, Tribolium castaneum . Journal of Biological Chemistry 286, 41924–41936.Google Scholar
Sim, C. & Denlinger, D.L. (2008) Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens . PNAS 105, 6777–6781.Google Scholar
Süren-Castillo, S., Abrisqueta, M. & Maestro, J.L. (2012) FoxO inhibits juvenile hormone biosynthesis and vitellogenin production in the German cockroach. Insect Biochemistry and Molecular Biology 42, 491–498.Google Scholar
Tatar, M., Bartke, A. & Antebi, A. (2003) The endocrine regulation of aging by insulin-like signals. Science 299, 1346–1351.Google Scholar
Tatar, M., Kopelman, A., Epstein, D., Tu, M.P., Yin, C.M. & Garofalo, R.S. (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292, 107–110.Google Scholar
Tauber, M.J., Tauber, C.A., Daane, K.M. & Hagen, K.S. (2000) Commercialization of predators: recent lessons from green lacewings (Neuroptera: Chrysopidae: Chrosoperla). Amercan Entomologist 46, 26–38.Google Scholar
Tufail, M. & Takeda, M. (2008) Molecular characteristics of insect vitellogenins. Journal of Insect Physiology 54, 1447–1458.Google Scholar
Wang, S.F., Zhu, J., Martin, D. & Raikhel, A.S. (2004) Regulation of vitellogenin gene expression by ecdysteroids. pp. 69–94 in Raikhel, A.S. & Sappington, T.W. (Eds) Reproductive Biology of Invertebrates, Progress in Vitellogenesis. USA/Plymouth, UK, Science Publishers, Enfield.Google Scholar
Wu, Q. & Brown, M.R. (2006) Signaling and function of insulin-like peptides in insects. Annual Review of Entomology 51, 1–24.Google Scholar
Wyatt, G.R. & Davey, K.G. (1996) Cellular and molecular actions of juvenile hormone. II. Roles of juvenile hormone in adult insects. Advances in Insect Physiology 26, 1–155.Google Scholar
Xu, H.J., Xue, J., Lu, B., Zhang, X.C., Zhuo, J.C., He, S.F., Ma, X.F., Jiang, Y.Q., Fan, H.W., Xu, J.Y., Ye, Y.X., Pan, P.L., Li, Q., Bao, Y.Y., Nijhout, H.F. & Zhang, C.X. (2015) Two insulin receptors determine alternative wing morphs in planthoppers. Nature 519, 464–467.Google Scholar