Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-10T16:11:36.223Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  01 June 2008

Raman Chandrasekar ,
Prusothaman Sumithra ,
Seo Sook Jae  and
Muthukalingan Krishnan
Raman Chandrasekar
Affiliation:
Division of Applied Life Sciences, Gyeongsang National University, Jinju, South Korea Insect Molecular Biology Laboratory, Department of Environmental Biotechnology, School of Environmental Sciences, Bharathidasan University, Tiruchirappalli620 024, Tamil Nadu, India
Prusothaman Sumithra
Affiliation:
Insect Molecular Biology Laboratory, Department of Environmental Biotechnology, School of Environmental Sciences, Bharathidasan University, Tiruchirappalli620 024, Tamil Nadu, India
Seo Sook Jae
Affiliation:
Division of Applied Life Sciences, Gyeongsang National University, Jinju, South Korea
Muthukalingan Krishnan*
Affiliation:
Insect Molecular Biology Laboratory, Department of Environmental Biotechnology, School of Environmental Sciences, Bharathidasan University, Tiruchirappalli620 024, Tamil Nadu, India
*
*E-mail: profmkrish@yahoo.com
Get access

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 [35S]-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.

Keywords

Amsacta albistrigahexamerinstorage protein 1peripheral fat bodyperivisceral fat bodyreceptor-mediated endocytosisprotein granulesimmunogold labelling[35S]-methionineovary
Type
Research Paper
Information
International Journal of Tropical Insect Science , Volume 28 , Issue 2 , June 2008 , pp. 78 - 87
Copyright
Copyright © ICIPE 2008

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.)

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.CrossRefGoogle 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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Burmester, T. and Scheller, K. (1997) Conservation of hexamerin endocytosis in Diptera. European Journal of Biochemistry 244, 713–720.CrossRefGoogle ScholarPubMed
Burmester, T. and Scheller, K. (1999) Ligands and receptors: Common theme in insect storage protein transport. Naturwissenschaften 86, 468–474.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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 Kerkut, G. A. and Gilbert, L. I.). 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Haunerland, N. H. (1996) Insect storage proteins: Gene families and receptors. Insect Biochemistry and Molecular Biology 26, 755–765.CrossRefGoogle ScholarPubMed
Haunerland, N. H., Nair, K. K. and Bowers, W. S. (1990) Fat body heterogeneity during development of Heliothis zea. Insect Biochemistry 20, 829–837.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Keeley, L. (1985) Physiology and biochemistry of the fat body, pp. 211–248. In Comprehensive Insect Physiology Biochemistry and Pharmacology (Edited by Kerkut, G. A. and Gilbert, L. I.). 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.CrossRefGoogle Scholar
Kinnear, L. E. and Thomson, J. A. (1975) Nature, origin and fat of major heamolymph proteins in Calliphora. Insect Biochemistry 5, 531–552.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 227, 680–685.CrossRefGoogle ScholarPubMed
Levenbook, L. (1985) Insect storage proteins, pp. 307–346. In Comprehensive Insect Physiology Biochemistry and Pharmacology (Edited by Kerkut, G. A. and Gilbert, L. I.). 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Muller, F., Adori, C. and Sass, M. (2004) Autophagic and apoptotic features during programmed cell death in the fat body of the tobacco hornworm (Manduca sexta). European Journal of Cell Biology 83, 67–78.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Peter, M. G. and Scheller, K. (1991) Arylphorins and the integument, pp. 115–124. In Physiology of the Insect Epidermis (Edited by Binnington, K. and Retnakaran, A.). 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 Scheller, K.). 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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, 115–128.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Telfer, W. H. and Kunkel, J. (1991) The function and evolution of insect storage hexamerins. Annual Review of Entomology 36, 205–228.CrossRefGoogle Scholar
Telfer, W. H. and Pan, M. L. (2003) Storage hexamer utilization in Manduca sexta. Journal of Insect Science 3, 1–6.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Tojo, S., Nakata, M. and Kobayashi, M. (1980) Storage proteins in the silkworm, Bombyx mori. Insect Biochemistry 10, 289–303.CrossRefGoogle Scholar
Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle 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.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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Wheeler, D. E., Tuchinskaya, I., Buck, N. A. and Tabashnik, B. E. (2000) Hexameric storage proteins during metamorphosis and egg production in the diamondback moth, Plutella xylostella (Lepidoptera). Journal of Insect Physiology 46, 951–958.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Wyatt, G. (1991) Gene regulation in insect reproduction. Invertebrate Reproduction and Development 20, 1–35.CrossRefGoogle Scholar
Wyatt, G. and Pan, M. (1978) Insect plasma proteins. Annual Review of Biochemistry 47, 779–817.CrossRefGoogle ScholarPubMed