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Sequestration of storage protein 1 (SP1) in differentiated fat body tissues of the female groundnut pest Amsacta albistriga (Lepidoptera: Arctiidae)

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Abstract

The transformation from larval caterpillar to non-feeding pupa and adult moth involves a complete remodelling and restructuring of an insect and its organs. In the groundnut pest Amsacta albistriga Walker, the female sex-specific storage protein 1 (SP1) was monitored from last larval instars, during pupal development to the adult stage. Staining intensity of SP1 (which resolved at 82 kDa) in the peripheral fat body (PF) tissues subjected to 10% SDS-PAGE was maximum at mid-stage last larval instars and declined subsequently. However, in perivisceral fat body (PVF) tissues, the staining intensity of SP1 increased significantly from mid-stage final instar. The presence of SP1 during pupal ovary and adult ovariole development and its availability during egg development was confirmed by immunoblot analysis. Electron microscopy data revealed that the decline of biosynthesis of SP1 in PF tissues and its disintegration were associated with the appearance of irregular nucleus and autophagic vacuoles during transformation of larva to pupa. In vitro and in vivo studies using [S]-methionine-labelled storage proteins showed that, unlike PF tissues, PVF tissue sequestered a significant amount of labelled SP1. During this transformation, SP1 was mainly sequestered as storage protein granules until they served as sources of amino acids for the production of egg yolk proteins. Localization of clathrin-coated pits and crystalline storage proteins was confirmed by immunogold tracer techniques.

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References

  • Bean D. W. and Silhacek D. L. (1989) Changes in the titer of the female-prodominant storage protein (81 kDa) during larval and pupal development of the wax moth, Galleria mellonela. Archives of Insect Biochemistry and Physiology 10, 333–348.

    Article  CAS  Google Scholar 

  • Beintema J. J., Stam W. T., Hazes B. and Smidt M. P. (1994) Evolution of arthropod hemocyanins and insect storage proteins (hexamerins). Molecular Biology and Evolution 11, 493–503.

    CAS  PubMed  Google Scholar 

  • Bonner M. V. and Laskey R. A. (1974) A film detection method for tritium labeled proteins and nucleic acids in Polyacrylamide gels. European Journal of Biochemistry 46, 83–88.

    Article  CAS  PubMed  Google Scholar 

  • Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.

    Article  CAS  PubMed  Google Scholar 

  • Burmester T. and Scheller K. (1992) Identification of binding proteins involved in the stage-specific uptake of arylphorin by the fat body cells of Calliphora vicina. Insect Biochemistry and Molecular Biology 22, 211–220.

    Article  CAS  Google Scholar 

  • Burmester T. and Scheller K. (1997) Conservation of hexamerin endocytosis in Diptera. European Journal of Biochemistry 244, 713–720.

    Article  CAS  PubMed  Google Scholar 

  • Burmester T. and Scheller K. (1999) Ligands and receptors: Common theme in insect storage protein transport. Naturwissenschaften 86, 468–474.

    Article  CAS  PubMed  Google Scholar 

  • Capurro M., Moreira-Ferro C. K., Marinotti O., James A. A. and de Bianchi A. G. (2000) Expression pattern of the larval and adult hexamerin genes of Musca domestica. Insect Molecular Biology 9, 169–177.

    Article  CAS  PubMed  Google Scholar 

  • Chandrasekar R. (2006) Expression and sequestration of SP1 in differentiated fat body tissue of red hairy caterpillar, Amsacta albistriga. PhD Thesis, Bharathidasan University, 150 pp.

    Google Scholar 

  • Chandrasekar R., Suganthi L. M. and Krishnan M. (2007a) Intraovarian synthesis and tissue distribution of hexameric storage protein-1 in the ovary of red hairy caterpillar, Amsacta albistriga. Journal of Asia-Pacific Entomology 10, 1–10.

    Article  Google Scholar 

  • Chandrasekar R., Suganthi L., Monohar N. X. and Krishnan M. (2007b) Expression of silk gene in response to P-soyatose (hydrolysed soy bean protein) supplementation in the fifth instar male larvae of Bombyx mori. Journal of Cellular and Molecular Biology 6(2), 163–174.

    Google Scholar 

  • Cheon H. M., Kim H. J., Chung D. H., Kim M. O., Park J. S., Yun C. Y. and Seo S. J. (2001) Local expression and distribution of a storage protein in ovary of Hyphantria cunea. Archives of Insect Biochemistry and Physiology 48, 111–120.

    Article  CAS  PubMed  Google Scholar 

  • Collins J. V. and Downe A. E. R. (1970) Selective accumulation of hemolymph protein by the fat body of Galleria mellonella. Journal of Insect Physiology 16, 1697–1708.

    Article  CAS  Google Scholar 

  • Dean R. L., Collins J. V. and Locke M. (1985) Structure of fat body, pp. 156–210. In Comprehensive Insect Physiology Biochemistry and Pharmacology (Edited by G. A. Kerkut and L. I. Gilbert). Vol. 4. Pergamon Press, Oxford.

    Google Scholar 

  • De Loof A. and Lagasse A. (1970) Juvenile hormone and the ultra structural properties of the fat body of the adult Colorado potato beetle, Leptinotarsa decemlineata Say. Zeitschrift für Zellforschung Und Mikroskopische Anatomie 106, 439–450.

    Article  PubMed  Google Scholar 

  • Dortland J. F. and Esch Th. H. (1979) A fine structural survey of the development of the adult fat body of Leptinotarsa decemlineata. Cell Tissue Research 201, 423–430.

    Article  CAS  PubMed  Google Scholar 

  • Hansen I. A., Meyer S. R., Schafer I. and Scheller K. (2002) Interaction of the anterior fat body protein with the hexamerin receptor in the blowfly Calliphora vicina. European Journal of Biochemistry 269, 954–960.

    Article  CAS  PubMed  Google Scholar 

  • Haunerland N. H. (1996) Insect storage proteins: Gene families and receptors. Insect Biochemistry and Molecular Biology 26, 755–765.

    Article  CAS  PubMed  Google Scholar 

  • Haunerland N. H., Nair K. K. and Bowers W. S. (1990) Fat body heterogeneity during development of Heliothis zea. Insect Biochemistry 20, 829–837.

    Article  CAS  Google Scholar 

  • Haunerland N. H. and Shirk P. D. (1995) Regional and functional differentiation in the insect fat body. Annual Review of Entomology 40, 121–145.

    Article  CAS  Google Scholar 

  • Jensen P. V. and Borgesen L. W. (2000) Regional and functional differentiation in the fat body of pharaoh’s ant queens, Monomorium pharaonis L. Arthropod Structure & Development 29, 171–184.

    Article  CAS  Google Scholar 

  • Jinwal U. K., Zakharkin S. O., Litvinova O. V., Jain S. and Benes H. (2006) Sex-, stage- and tissue-specific regulation by a mosquito hexamerin promoter. Insect Molecular Biology 15, 301–311.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaliafas A. D., Marmaras V. J. and Christodoulous C. (1984) Immunocytochemical and electrophoretic studies on the localization of the major haemolymph protein (ceratitins) Ceratitis capitata during development. Wilhelm Roux’s Archives of Developmental Biology 194, 37–43.

    Article  CAS  PubMed  Google Scholar 

  • Kanost M. R., Kawooya J. K., Law J. H., Ryan R. O., Van Heusdan M. C. and Zeigler R. (1990) Insect haemolymph proteins. Advances in Insect Physiology 22, 299–396.

    Article  Google Scholar 

  • Keeley L. (1985) Physiology and biochemistry of the fat body, pp. 211–248. In Comprehensive Insect Physiology Biochemistry and Pharmacology (Edited by G. A. Kerkut and L. I. Gilbert). Vol. 3. Pergamon Press, Oxford.

    Google Scholar 

  • Kim H. R., Seo S. J. and Mayer R. T. (1989) Properties, synthesis, and accumulation of storage proteins in Pieris rapae L. Archives of Insect Biochemistry and Physiology 10, 215–228.

    Article  CAS  Google Scholar 

  • Kinnear L. E. and Thomson J. A. (1975) Nature, origin and fat of major heamolymph proteins in Calliphora. Insect Biochemistry 5, 531–552.

    Article  CAS  Google Scholar 

  • Kiran Kumar N., Ismail S. M. and Dutta-Gupta A. (1997) Uptake of storage proteins in the rice moth Corcyra cephalonica: Identification of storage protein binding proteins in the fat body cell membranes. Insect Biochemistry and Molecular Biology 27, 269–278.

    Google Scholar 

  • Konig M., Agrawal O. P., Schenkel H. and Scheller K. (1986) Incorporation of calliphorin into the cuticle of the developing blowfly, Calliphora vicina. Wilhelm Roux’s Archives of Developmental Biology 195, 296–301.

    Article  Google Scholar 

  • Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 227, 680–685.

    Article  CAS  PubMed  Google Scholar 

  • Levenbook L. (1985) Insect storage proteins, pp. 307–346. In Comprehensive Insect Physiology Biochemistry and Pharmacology (Edited by G. A. Kerkut and L. I. Gilbert). Vol. 10. Pergamon Press, Oxford.

    Google Scholar 

  • Locke M. and Collins J. V (1965) The structure and formation of the protein granules in the fat body of an insect. Journal of Cell Biology 26, 857–885.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Locke M. and Collins J. V (1968) Protein uptake into multivesicular bodies and storage granules in the fat body of an insect. Journal of Cell Biology 36, 453–483.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Massey H. C. Jr, Kejzlarova-Lepesant J., Willis R. L., Castleberry A. B. and Benes H. (1997) The Drosophila Lsp-1 β gene: A structural and phylogenetic analysis. European Journal of Biochemistry/FEBS 245, 199–207.

    Article  CAS  Google Scholar 

  • Miller S. G. and Silhacek D. L. (1982) The synthesis and uptake of haemolymph storage protein by the fat body of the greater wax moth, Galleria mellonella. Insect Biochemistry 12, 293–300.

    Article  CAS  Google Scholar 

  • Müller F., Adori C. and Sass M. (2004) Autophagic and apoptotic features during programmed cell death in the fat body of the tobacco hornworm (Manduca sexto). European Journal of Cell Biology 83, 67–78.

    Article  PubMed  Google Scholar 

  • Munn E. A. and Greville G. D. (1969) The soluble proteins of developing Calliphora erythocephala particularly calliphorin and similar proteins in other insects. Journal of Insect Physiology 15, 1935–1950.

    Article  CAS  Google Scholar 

  • Ogawa K. and Tojo S. (1981) Quantitative changes of storage proteins and vitellogenin during the pupal-adult development in the silkworm, Bombyx mori (Lepidoptera: Bombycidae). Applied Entomology and Zoology 16, 288–296.

    Article  CAS  Google Scholar 

  • Pan M. and Telfer W. (1992) Selectivity in storage hexamerin cleaning demonstrated with hemolymph transfusion between Hyalophora cecropia and Actias luna. Archives of Insect Biochemistry and Physiology 19, 203–221.

    Article  CAS  PubMed  Google Scholar 

  • Pan M. L. and Telfer W. (2001) Storage hexamer utilization in two lepidopterans: Differences correlated with the timing of egg formation. Journal of Insect Science 1, 1–9.

    Article  Google Scholar 

  • Peter M. G. and Scheller K. (1991) Arylphorins and the integument, pp. 115–124. In Physiology of the Insect Epidermis (Edited by K. Binnington and A. Retnakaran). CSIRO, Melbourne.

    Google Scholar 

  • Riddiford L. M. and Law J. H. (1983) Larval serum proteins of Lepidoptera, pp. 75–85. In The larval Serum Proteins of Insects: Functions, Biosynthesis and Genetics (Edited by K. Scheller). Thieme-Verlag, Stuttgart, Germany.

    Google Scholar 

  • Reynolds E. S. (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. Journal of Cell Biology 17, 208–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds S. E. (1990) Feeding in caterpillars - maximizing or optimizing food acquisition? Animal Nutrition and Transport Processes 5, 106–118.

    Google Scholar 

  • Roberts D. B., Wolf J. and Akam M. E. (1977) The developmental profiles of two major hemolymph proteins from Drosophila melanogaster. Journal of Insect Physiology 23, 871–878.

    Article  CAS  PubMed  Google Scholar 

  • Ryan R. O., Keim P. S., Wells M. A. and Law J. H. (1985) Purification properties of a predominantly female-specific protein from the hemolymph of the larvae of the tobacco hornworm, Manduca sexta. Journal of Biological Chemistry 260, 782–787.

    CAS  PubMed  Google Scholar 

  • Salerno A. P., Dansa-Petretski M., Silva-Neto M. A. C., Coelho H. S. L. and Masuda H. (2002) Rhodnius prolixus vitellin is composed of three different populations: Comparison with vitellogenin. Insect Biochemistry and Molecular Biology 32, 709–717.

    Article  CAS  PubMed  Google Scholar 

  • Scheller K., Zimmerman H. P. and Sekeris C. E. (1990) Calliphorin, a protein involved in cuticle formation of the blowfly, Calliphora vicina. Verlag der Zeitschrift Naturforschchung C 35, 387–389.

    Article  Google Scholar 

  • Seo S. J., Kang Y., Chen H. and Kim H. (1998) Distribution and accumulation of SP-1 in ovary of Hypyantria cunea Drury. Archives of Insect Biochemistry and Physiology 37, 115–128.

    Article  CAS  PubMed  Google Scholar 

  • Shirk P. D. and Malone C. C. (1989) Regional differentiation of fat bodies in larvae of the Indian meal moth Plodia interpunctella. Archives of Insect Biochemistry and Physiology 12, 187–199.

    Article  CAS  Google Scholar 

  • Silhacek D. L., Miller S. G. and Murphy C. L. (1994) Purification and characterization of flavin-binding storage protein from the haemolymph of Galleria mellonella. Archives of Insect Biochemistry and Physiology 25, 55–72.

    Article  CAS  PubMed  Google Scholar 

  • Sonoda S., Fukumoto K., Izumi Y., Ashfaq M., Yoshida H. and Tsumuki H. (2006) Methionine-rich storage protein gene in the rice stem borer, Chilo suppressalis, is expressed during diapause in response to cold acclimation. Insect Molecular Biology 15, 853–859.

    Article  PubMed  Google Scholar 

  • Telfer W. H., Keim T. S. and Law J. H. (1983) Arylphorin, a new protein from Hyalophora cecropia: Comparison with calliphorin and manducin. Insect Biochemistry 13, 601–613.

    Article  CAS  Google Scholar 

  • Telfer W. H. and Kunkel J. (1991) The function and evolution of insect storage hexamerins. Annual Review of Entomology 36, 205–228.

    Article  CAS  PubMed  Google Scholar 

  • Telfer W. H. and Pan M. L. (2003) Storage hexamer utilization in Manduca sexta. Journal of Insect Science 3, 1–6.

    Article  Google Scholar 

  • Tojo S., Betchaku T., Ziccardi V. J. and Wyatt G. R. (1978) Fat body protein granules and storage protein in the silkmoth Hyalophora cecropia. Journal of Cell Biology 78, 823–838.

    Article  CAS  PubMed  Google Scholar 

  • Tojo S., Kiguchi K. and Kimura S. (1981) Hormonal control of storage protein synthesis and uptake by the fat body in the silk worm, Bombyx mori. Journal of Insect Physiology 27, 491–497.

    Article  CAS  Google Scholar 

  • Tojo S., Nakata M. and Kobayashi M. (1980) Storage proteins in the silkworm, Bombyx mori. Insect Biochemistry 10, 289–303.

    Article  CAS  Google Scholar 

  • Towbin H., Staehelin T. and Gordon J. (1979) Electro-phoretic transfer of proteins from Polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proceedings of the National Academy of Sciences of the USA 76, 4350–4354.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueno K. and Natori S. (1987) Possible involvement of lumichrome in the binding of storage protein to its receptor in Sarcophaga peregrine. Journal of Biological Chemistry 262, 12780–12784.

    CAS  PubMed  Google Scholar 

  • Vanishree V., Nirmala X., Arul E. and Krishnan M. (2005) Differential sequestration of storage proteins by various fat body tissues during post larval development in silkworm, Bombyx mori L. Invertebrate Reproduction and Development 48, 81–88.

    Article  Google Scholar 

  • Vanishree V., Nirmala X. and Krishnan M. (1999) Differential synthesis of storage protein by various fat body tissues during development of female silkworm, Bombyx mori. SAAS Bulletin: Biochemistry and Biotechnology 12, 69–89.

    CAS  Google Scholar 

  • von Gaudecker B. (1963) Über den Formenwechsel einiger Zellorganelle bei der Bildung der Reservestoffe im Fettkörper von Drosophila-Larven. Zeitschrift für Naturforschung 61, 56–91.

    Article  Google Scholar 

  • Wang Z. and Haunerland N. H. (1991) Ultrastructural study of storage protein granules in fat body of the corn earworm Heliothis zea. Journal of Insect Physiology 37, 353–363.

    Article  CAS  Google Scholar 

  • Wang Z. and Haunerland N. H. (1992) Fate of differentiated fat body tissues during metamorphosis of Helicoverpa zea. Journal of Insect Physiology 38, 199–213.

    Article  Google Scholar 

  • Wang Z. and Haunerland N. H. (1993) Storage protein uptake in Helicoverpa zea. Purification of the very high density lipoprotein receptor from perivisceral fat body. Journal of Biological Chemistry 268, 16673–18878.

    CAS  PubMed  Google Scholar 

  • Wheeler D. E., Tuchinskaya I., Buck N. A. and Tabashnik B. E. (2000) Hexameric storage proteins during metamorphosis and egg production in the diamond-back moth, Plutella xylostella (Lepidoptera). Journal of Insect Physiology 46, 951–958.

    Article  CAS  PubMed  Google Scholar 

  • Willott E., Bew L. K., Nagle R. B. and Wells M. A. (1988) Sequential structural changes in the fat body of the tobacco hornworm, Manduca sexta, during the fifth larval stadium. Tissue and Cell 20, 635–643.

    Article  CAS  PubMed  Google Scholar 

  • Wyatt G. (1991) Gene regulation in insect reproduction. Invertebrate Reproduction and Development 20, 1–35.

    Article  CAS  Google Scholar 

  • Wyatt G. and Pan M. (1978) Insect plasma proteins. Annual Review of Biochemistry 47, 779–817.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Division of Applied Life Sciences, Gyeongsang National University, Jinju, South Korea

    Raman Chandrasekar & Seo Sook Jae

  2. Insect Molecular Biology Laboratory, Department of Environmental Biotechnology, School of Environmental Sciences, Bharathidasan University, Tiruchirappalli, 620 024, Tamil Nadu, India

    Raman Chandrasekar, Prusothaman Sumithra & Muthukalingan Krishnan

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  1. Raman Chandrasekar
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  2. Prusothaman Sumithra
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Correspondence to Muthukalingan Krishnan.

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Chandrasekar, R., Sumithra, P., Jae, S.S. et al. Sequestration of storage protein 1 (SP1) in differentiated fat body tissues of the female groundnut pest Amsacta albistriga (Lepidoptera: Arctiidae). Int J Trop Insect Sci 28, 78–87 (2008). https://doi.org/10.1017/S1742758408007728

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