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Investigation of the Interaction between Fat body and Ovary Development during Pupal Transformation in Silkworm, Bombyx mori

Year 2013, Volume: 72 Issue: 2, 1 - 13, 12.05.2014

Esen Poyraz Ebru Göncü Osman Parlak

Abstract

The insect fat body is the major biosynthetic and storage organ involved in lipid, carbohydrate, amino

acid and nitrogen metabolism and protein synthesis. It also actively participates in vitellogenesis and

ovary development, synthesizing the soluble precursor for yolk, i.e., vitellogenin in stage specific

manner. The continual substance exchange among fat body, hemolymph and ovary is controlled by

hormones, ecdysteroids and juvenile hormone, during metamorphosis of

Bombyx mori

(L.). The aim

of the present study was to clarify the interactions between major proteins of fat body and hemolymph

 

and their effect on ovarian development under hormonal factors during pupal-adult transformation.

 

Detected fat body, hemolymph and ovary proteins are grouped as follows by using sodium dodecyl

 

sulfate polyacrylamide gel electrophoresis (SDS-PAGE): storage proteins (72 kDa and 76 kDa), 30

 

kDa proteins, ApoLp-I (230-250 kDa), egg specific protein (72 kDa and 64 kDa) and vitellogenins

 

(178 kDa). Our results suggest that changes in the well-defined and characterized protein fractions

 

quality and quantity of the fat body had a direct effect under hormonal factors on the ovary and egg

 

development during metamorphosis.

 

 

Keywords

Bombyx mori hemolymph proteins fat body proteins yolk proteins SDS-PAGE.

References

  • Belle’s X. (1998) Endocrine effectors in insect vitellogenesis, In: Coast, G.M., Webster, S.G., Recent advances in arthropod endocrinology. Cambridge University Press, 68Belle’s X. (1995) Interactions between Corpora Allata, Fat Body and Ovary in insect Reproduction: Which Controls Which?. Netherlands Journal of Zoology, 45: 152-156.
  • 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 Chemistry, 72: 248-254.
  • Chatani F. and Ohnishi E. (1976) Effect of ecdysone on the ovarian development of Bombyx silkworm, Development, Growth & Differantiation, 18: 481-484.
  • Engelmann F. (1979) Insect vitellogenin: identification, biosynthesis, and the role in vitellogenesis. Advances in Insect Physiology, 14: 49-108.
  • Goncu E. and Parlak O. (2008) Some autophagic and apoptotic features of programmed cell death in the anterior silk glands of the silkworm, Bombyx mori. Autophagy, 4:1069-1072.
  • Hanaoka K. and Ohnishi E. (1974) Changes in Ecdysone titre during pupal-adult development in the silkworm, Bombyx mori. J. Insect Physiology, 20: 2375- 2384.
  • Hyrsl P. and Simek V. (2005) An analysis of hemolymph protein profiles during the final instar, prepupa and pupa of the silkworm Bombyx mori (Lepidoptera, Bombycidae). Biologia, Bratislava, 60: 207-213.
  • Izumi S., Tomino S. and H. Chino (1980) Purification and molecular properties of vitellin from the silkworm, Bombyx mori. Insect Biochemistry, 10: 199-208.
  • Izumi S. and Tomino S. (1983) Vitellogenin synthesis in the silkworm, Bombyx mori: separate mRNAs encode two subunits of vitellogenin. Insect Biochemistry, 13: 81-85.
  • Janarthanan S. , Krishnan M. and Ignacimuthu S. (1998) Changes in protein profiles during pupal development in the silkworm, Bombyx mori (L.). Indian Journal of Experimental Biology, 36, 1158- 1160.
  • Kawaguchi Y., Banno Y., Koga K. and H. Doira (1996) Changes of yolk and hemolymph proteins during ovarian development in the miniature egg mutant, emi, of Bombyx mori. J. Serie. Sci. Jpn., 65: 13-20.
  • Kawaguchi Y. and Doira H. (1973) Gene-controlled incorporation of hemolymph protein into the ovaries of Bombyx mori, J. Insect Physiology, 19: 2083- 2096.
  • Kawooya J.K. and Law J.H. (1988) Role of lipophorin in lipid transport to the insect egg. The Journal of Biological Chemistry, 263: 8748-8753.
  • Kendirgi F., Swevers L. and Iatrou K. (2002) An ovarian follicular epithelium protein of the silkworm (Bombyx mori) that associates with the vitelline membrane and contributes to the structural integrity of the follicle. FEBS Letters, 524: 59-68.
  • Kishimoto A., Nakato H., Izumi S. and Tomino S. (1999) Biosynthesis of major plasma proteins in the primaiy culture of fat body cells from the silkworm, Bombyx mori. Cell and Tissue Research, 297: 329-335.
  • Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227: 680-685.
  • Liu Y., Liu H., Liu S., Wang S., Jiang R.J. and S. Li (2009) Hormonal and nutritional regulation of insect fat body development and function, Archives of Insect Biochemistry and Physiology, 71: 16-30.
  • Mpakou V.E., Nezis I.P., Stravopodis D.J, Margaritis L.H. and Papassideri I.S. (2008) Different modes of programmed cell death during oogenesis of the silkmoth Bombyx mori. Autophagy, 4: 97-100.
  • Nagaraju J. and Goldsmith M.R. (2002) Silkworm genomics-progress and prospects. Curr. Sci. India, 83: 415-425.
  • Nijhout H.F. (1994) Insect Hormone, Princeton University Pres, 142-170.
  • 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: 288-294.
  • Ohnishi E. and Chatani F. (1977) Biosynthesis of ecdysone in the isolated abdomen of the silkworm, Bombyx mori. Development, Growth & Differentiation , 19: 67-70.
  • Ohnishi E. and Watanabe K. (1985) Biosynthesis and accumulation of ecdysteroids in the ovary of the silkworm, Bombyx mori. Current Trends in Comparative Endocrinology, 1: 327-328.
  • Oliveira V.T.P. and Cruz-Landim C. (2003) Morphology and function of insect fat body cells: A review. Biociéncias, 11: 19520
  • Oliveira V.T.P. and Cruz-Landim C. (2004) Protein content and electrophoretic profile of fat body and ovary extracts from workers of Melipona quadrifasciata anthidioides (Hymenoptera, Meliponini). Iheringia. Série Zoologia, Porto Alegre, 94: 417-419.
  • Ono S., Nagayama H. and Shimura K. (1975) The occurrence and synthesis of femaleand egg- specific proteins in the silkworm, Bombyx mori, Insect Biochemistry, , 5: 319-3
  • Parlak O., Sakurai S., Kaya M. and Ohtaki T. (1992) Content and possible role of ecdysteroids in the larval ovary of the silkworm, Bombyx mori. Invertebrate Reproduction & Development, 21: 1-6.
  • Pho D.B., Pennanech M. and Jallon J.M. (1996)
  • Purification of adult Drosophila melanogaster Lipophorin and its role in Hydrocarbon transport. Archives of Insect Biochemistry and Physiology, 31: 289-303. Raikhel A.S. and Dhadialla T.S. (1992) Accumulation of yolk proteins in insect oocytes.
  • Annual Review of Entomology, 37: 2172
  • Smith A.F., Owen L.M., Strobel L.M., Chen H., Kanost M.R., Hanneman E. and Wells M.A. (1994) Exchangeable apolipoproteins of insects share a common structural motif. The Journal of Lipid Research, 35: 1976-1984.
  • Sumithra P.H., Cathrin P., Britto C.P. and Krishnan M.K. (2010) Modes of cell death in the pupal perivisceral fat body tissue of the silkworm Bombyx mori L. Cell and tissue Research, 339: 349-358.
  • Sun Q., Zhao P., Lin Y., Hou Y., Xia Q. and Xiang Z. (2007) Analysis of the structure and expression of the 30K protein genes in silkworm, Bombyx mori. Insect Science, 14: 5-13.
  • Swevers L., Raikhel A.S., Sappington T.W., Shirk P. and Iatrou K. (2005) Vitellogenesis and Post- Vitellogenic Maturation of the Insect Ovarian Follicle. Comprehensive Molecular Insect Science, Elsevier, 1: 87-1
  • Telfer W. H. (1965) The mechanism and control ofyolk formation. A. Rev. Ent, 10: 161-1
  • Telfer W.H. (2009) Egg formation in Lepidoptera. Journal of Insect Science 9, article 50.
  • Tojo S., Kiguchi K. and Kimura S. (1981) Hormonal control of storage protein synthesis and uptake by the fat body in the silkworm, Bombyx mori. Journal of Insect Physiology, 27: 491-497.
  • Tsuchida K., Nagata M. and Suzuki A. (1987)
  • Hormonal control of ovarian development in the silkworm, Bombyx mori. Archives 13 of Insect Biochemistry and Physiology, 5: 167-1 Uranlı R., Goncu E. and Parlak O. (2011) Investigation Investigation of the influence of the juvenile hormone analogue fenoxycarb on major hemolymph proteins of the silkworm Bombyx mori during the last larval instar. Turkish Journal of Zoology, 35: 1-14.
  • Vale D. (1993) Vitellogenesis in Insects and other Groups- A Review, Mem. Inst. Oswaldo Cruz, Rio de Janeiro, 88: 1-26.
  • Wigglesworth V.B. (1942) The storage of protein, fat, glycogen and uric acid in the fat body and other tissues of mosquito larvae, J. Exp. Biol., Cambridge, 19: 56-77.
  • Yamauchi H. and Yoshitake N. (1984) Developmental stages of ovarian follicles of the silkworm, Bombyx mori L. Journal of Morphology, 179: 21-31.
  • Yang H., Zhou Z., Zhang H., Chen M., Li J., Ma Y. and Zhong B. (2010) Shotgun proteomic analysis of the fat body during metamorphosis of domesticated silkworm (Bombyx morí). Amino Acids, 38: 1333-1342.
  • Zara F.J. and Caetano F.H. (2004) Ultramorphology and Histochemistry of fat body cells from last instar larval of the Pachycondyla (=Neoponera) villosa (Fabricus) (Formicidae: Ponerinae). Brazilian Journal of Biology, 64: 725-735.
  • Zhu J., Indrasith L. and Yamashita O. (1986) Characterization of vitellin, egg- specific protein and 30-kDa protein from Bombyx eggs, and their fates during oogenesis and embryogenesis. Biochimica et Biophysica Acta, 882: 427-436.
  • Arrese E.L., Soulages J.L. (2010) Insect fat body: energy, metabolism, and regulation. Annual Review of Entomology, 55: 207– 2
  • Oliveira V. T. P., Berger, B., Cruz-Landim C., and Simões Z. L. P., (2012) Vitellogenin content in fat body and ovary homogenates of workers and queens of Melipona quadrifasciata anthidioides during vitellogenesis, Insect Science, 19: 213–219.

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Year 2013, Volume: 72 Issue: 2, 1 - 13, 12.05.2014

Esen Poyraz Ebru Göncü Osman Parlak

Abstract

Böcek yağ dokusu, lipit, karbohidrat, aminoasit ve nitrojen metabolizmalarına katılan ve protein sentezinde rol alan en büyük biyosentetik depo organıdır. Bunun yanı sıra, vitellogenin gibi yumurta depo proteinlerinin öncülerini sentezleyerek aktif olarak vitellogenezde ve ovaryum gelişiminde rol alır. Bombyx mori’de (L.)’te metamorfoz süresince, yağ doku, hemolenf ve ovaryum arasında meydana gelen sürekli madde değişimi ekdisteroidler ve juvenile hormonun kontrolü altında gerçekleşir. Elektroforetik olarak belirlenen temel hemolenf proteinleri şu şekilde gruplandırılmıştır: depo proteinleri (72 kDa ve 76 kDa), 30K polipeptidleri, ApoLp-I (230- 250 kDa), yumurta spesifik proteini (/2 kDa ve 64 kDa) ve vitellogenin (178 kDa). Çalışmamızın sonucunda metamorfoz süresince yağ doku proteinlerinin nitelik ve niceliğindeki değişimlerin ovaryum ve yumurta gelişimi üzerinde doğrudan etkiye sahip olduğu sonucuna ulaşılmıştır.

Keywords

Bombyx mori hemolenf proteinleri yağ doku proteinleri yumurta depo proteinleri

References

  • Belle’s X. (1998) Endocrine effectors in insect vitellogenesis, In: Coast, G.M., Webster, S.G., Recent advances in arthropod endocrinology. Cambridge University Press, 68Belle’s X. (1995) Interactions between Corpora Allata, Fat Body and Ovary in insect Reproduction: Which Controls Which?. Netherlands Journal of Zoology, 45: 152-156.
  • 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 Chemistry, 72: 248-254.
  • Chatani F. and Ohnishi E. (1976) Effect of ecdysone on the ovarian development of Bombyx silkworm, Development, Growth & Differantiation, 18: 481-484.
  • Engelmann F. (1979) Insect vitellogenin: identification, biosynthesis, and the role in vitellogenesis. Advances in Insect Physiology, 14: 49-108.
  • Goncu E. and Parlak O. (2008) Some autophagic and apoptotic features of programmed cell death in the anterior silk glands of the silkworm, Bombyx mori. Autophagy, 4:1069-1072.
  • Hanaoka K. and Ohnishi E. (1974) Changes in Ecdysone titre during pupal-adult development in the silkworm, Bombyx mori. J. Insect Physiology, 20: 2375- 2384.
  • Hyrsl P. and Simek V. (2005) An analysis of hemolymph protein profiles during the final instar, prepupa and pupa of the silkworm Bombyx mori (Lepidoptera, Bombycidae). Biologia, Bratislava, 60: 207-213.
  • Izumi S., Tomino S. and H. Chino (1980) Purification and molecular properties of vitellin from the silkworm, Bombyx mori. Insect Biochemistry, 10: 199-208.
  • Izumi S. and Tomino S. (1983) Vitellogenin synthesis in the silkworm, Bombyx mori: separate mRNAs encode two subunits of vitellogenin. Insect Biochemistry, 13: 81-85.
  • Janarthanan S. , Krishnan M. and Ignacimuthu S. (1998) Changes in protein profiles during pupal development in the silkworm, Bombyx mori (L.). Indian Journal of Experimental Biology, 36, 1158- 1160.
  • Kawaguchi Y., Banno Y., Koga K. and H. Doira (1996) Changes of yolk and hemolymph proteins during ovarian development in the miniature egg mutant, emi, of Bombyx mori. J. Serie. Sci. Jpn., 65: 13-20.
  • Kawaguchi Y. and Doira H. (1973) Gene-controlled incorporation of hemolymph protein into the ovaries of Bombyx mori, J. Insect Physiology, 19: 2083- 2096.
  • Kawooya J.K. and Law J.H. (1988) Role of lipophorin in lipid transport to the insect egg. The Journal of Biological Chemistry, 263: 8748-8753.
  • Kendirgi F., Swevers L. and Iatrou K. (2002) An ovarian follicular epithelium protein of the silkworm (Bombyx mori) that associates with the vitelline membrane and contributes to the structural integrity of the follicle. FEBS Letters, 524: 59-68.
  • Kishimoto A., Nakato H., Izumi S. and Tomino S. (1999) Biosynthesis of major plasma proteins in the primaiy culture of fat body cells from the silkworm, Bombyx mori. Cell and Tissue Research, 297: 329-335.
  • Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227: 680-685.
  • Liu Y., Liu H., Liu S., Wang S., Jiang R.J. and S. Li (2009) Hormonal and nutritional regulation of insect fat body development and function, Archives of Insect Biochemistry and Physiology, 71: 16-30.
  • Mpakou V.E., Nezis I.P., Stravopodis D.J, Margaritis L.H. and Papassideri I.S. (2008) Different modes of programmed cell death during oogenesis of the silkmoth Bombyx mori. Autophagy, 4: 97-100.
  • Nagaraju J. and Goldsmith M.R. (2002) Silkworm genomics-progress and prospects. Curr. Sci. India, 83: 415-425.
  • Nijhout H.F. (1994) Insect Hormone, Princeton University Pres, 142-170.
  • 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: 288-294.
  • Ohnishi E. and Chatani F. (1977) Biosynthesis of ecdysone in the isolated abdomen of the silkworm, Bombyx mori. Development, Growth & Differentiation , 19: 67-70.
  • Ohnishi E. and Watanabe K. (1985) Biosynthesis and accumulation of ecdysteroids in the ovary of the silkworm, Bombyx mori. Current Trends in Comparative Endocrinology, 1: 327-328.
  • Oliveira V.T.P. and Cruz-Landim C. (2003) Morphology and function of insect fat body cells: A review. Biociéncias, 11: 19520
  • Oliveira V.T.P. and Cruz-Landim C. (2004) Protein content and electrophoretic profile of fat body and ovary extracts from workers of Melipona quadrifasciata anthidioides (Hymenoptera, Meliponini). Iheringia. Série Zoologia, Porto Alegre, 94: 417-419.
  • Ono S., Nagayama H. and Shimura K. (1975) The occurrence and synthesis of femaleand egg- specific proteins in the silkworm, Bombyx mori, Insect Biochemistry, , 5: 319-3
  • Parlak O., Sakurai S., Kaya M. and Ohtaki T. (1992) Content and possible role of ecdysteroids in the larval ovary of the silkworm, Bombyx mori. Invertebrate Reproduction & Development, 21: 1-6.
  • Pho D.B., Pennanech M. and Jallon J.M. (1996)
  • Purification of adult Drosophila melanogaster Lipophorin and its role in Hydrocarbon transport. Archives of Insect Biochemistry and Physiology, 31: 289-303. Raikhel A.S. and Dhadialla T.S. (1992) Accumulation of yolk proteins in insect oocytes.
  • Annual Review of Entomology, 37: 2172
  • Smith A.F., Owen L.M., Strobel L.M., Chen H., Kanost M.R., Hanneman E. and Wells M.A. (1994) Exchangeable apolipoproteins of insects share a common structural motif. The Journal of Lipid Research, 35: 1976-1984.
  • Sumithra P.H., Cathrin P., Britto C.P. and Krishnan M.K. (2010) Modes of cell death in the pupal perivisceral fat body tissue of the silkworm Bombyx mori L. Cell and tissue Research, 339: 349-358.
  • Sun Q., Zhao P., Lin Y., Hou Y., Xia Q. and Xiang Z. (2007) Analysis of the structure and expression of the 30K protein genes in silkworm, Bombyx mori. Insect Science, 14: 5-13.
  • Swevers L., Raikhel A.S., Sappington T.W., Shirk P. and Iatrou K. (2005) Vitellogenesis and Post- Vitellogenic Maturation of the Insect Ovarian Follicle. Comprehensive Molecular Insect Science, Elsevier, 1: 87-1
  • Telfer W. H. (1965) The mechanism and control ofyolk formation. A. Rev. Ent, 10: 161-1
  • Telfer W.H. (2009) Egg formation in Lepidoptera. Journal of Insect Science 9, article 50.
  • Tojo S., Kiguchi K. and Kimura S. (1981) Hormonal control of storage protein synthesis and uptake by the fat body in the silkworm, Bombyx mori. Journal of Insect Physiology, 27: 491-497.
  • Tsuchida K., Nagata M. and Suzuki A. (1987)
  • Hormonal control of ovarian development in the silkworm, Bombyx mori. Archives 13 of Insect Biochemistry and Physiology, 5: 167-1 Uranlı R., Goncu E. and Parlak O. (2011) Investigation Investigation of the influence of the juvenile hormone analogue fenoxycarb on major hemolymph proteins of the silkworm Bombyx mori during the last larval instar. Turkish Journal of Zoology, 35: 1-14.
  • Vale D. (1993) Vitellogenesis in Insects and other Groups- A Review, Mem. Inst. Oswaldo Cruz, Rio de Janeiro, 88: 1-26.
  • Wigglesworth V.B. (1942) The storage of protein, fat, glycogen and uric acid in the fat body and other tissues of mosquito larvae, J. Exp. Biol., Cambridge, 19: 56-77.
  • Yamauchi H. and Yoshitake N. (1984) Developmental stages of ovarian follicles of the silkworm, Bombyx mori L. Journal of Morphology, 179: 21-31.
  • Yang H., Zhou Z., Zhang H., Chen M., Li J., Ma Y. and Zhong B. (2010) Shotgun proteomic analysis of the fat body during metamorphosis of domesticated silkworm (Bombyx morí). Amino Acids, 38: 1333-1342.
  • Zara F.J. and Caetano F.H. (2004) Ultramorphology and Histochemistry of fat body cells from last instar larval of the Pachycondyla (=Neoponera) villosa (Fabricus) (Formicidae: Ponerinae). Brazilian Journal of Biology, 64: 725-735.
  • Zhu J., Indrasith L. and Yamashita O. (1986) Characterization of vitellin, egg- specific protein and 30-kDa protein from Bombyx eggs, and their fates during oogenesis and embryogenesis. Biochimica et Biophysica Acta, 882: 427-436.
  • Arrese E.L., Soulages J.L. (2010) Insect fat body: energy, metabolism, and regulation. Annual Review of Entomology, 55: 207– 2
  • Oliveira V. T. P., Berger, B., Cruz-Landim C., and Simões Z. L. P., (2012) Vitellogenin content in fat body and ovary homogenates of workers and queens of Melipona quadrifasciata anthidioides during vitellogenesis, Insect Science, 19: 213–219.
There are 47 citations in total.

Details

Primary Language English
Journal Section Research Articles
Authors

Esen Poyraz

Ebru Göncü

Osman Parlak This is me

Publication Date May 12, 2014
Submission Date May 12, 2014
Published in Issue Year 2013 Volume: 72 Issue: 2

Cite

AMA Poyraz E, Göncü E, Parlak O. Investigation of the Interaction between Fat body and Ovary Development during Pupal Transformation in Silkworm, Bombyx mori. Eur J Biol. May 2014;72(2):1-13.
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