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Programmed Cell Death in the Digestive Canal of Bombyx mori (Lepidoptera: Bombycidae) during Prepupal Period

Year 2014, Volume: 73 Issue: 2, 1 - 29, 23.03.2016

Gözde Selek Ebru Göncü Osman Parlak

Abstract

In silkworms, like other holometabolus insects, larval digestive canal degenerates via programmed
cell death (PCD) during larval-pupal metamorphosis. PCD plays a key role in developmental biology.
It generally occurs with two major mechanisms; apoptosis and autophagic cell death. In this study,
we aimed to determine the metamorphic events in the digestive canal of Bombyx mori during the
prepupal period. The general morphological changes were studied by using histological techniques; the
degenerative cells were determined using H&E (Hematoxylen&Eosin) and PAS (Periodic Acid Schiff)
staining. We have used TUNEL (terminal transferase-mediated dUTP nick end-labeling) assay for
determination of apoptotic cell nuclei. Also, the acid phosphatase activity was calculated to determine
the autophagic cell death. In conclusion; our observations indicated a co-occurrence of apoptosis and
autophagy observed during the cell death of the digestive canal.

Keywords

Bombyx mori apoptosis digestive system autophagy TUNEL

References

  • Beaulaton J. and Lockshin R. A. (1982) The relation of programmed cell death to development and reproduction: comparative studies and an attempt at classification. Int. Rev. Cytol., 79,215-235.
  • Bergmeyer H.U. (1974) Methods of Enzymatic Analysis. 2nd edn, Volume 1, Academic Press, Inc., New York, Volume I, 495-496.
  • Billingsly P.F. and Lehane M.J. (1996) Structure and Ultrastructure of the insect midgut. Biology of the Insect Midgut. Chapman and Holl, London, 3-25.
  • Cavalcante V. M., Cruz-Landim C. Da (2004) Electrophoretic protein pattern and acid phosphatase activity in the midgut extracts of Apis mellifera L. during metamorphosis. Neotropical Entomology, 33(2): 169-172.
  • Clarke P.G. (1990) Developmental cell death: morphological diversity and multiple mechanism, Anatomy and Embryology (Berlin), 181, 195-213.
  • Kerr J.F.R., Wyllie A.H. and Currie A.R. (1972)
  • Eisenberg-Lerner A., Bialik S., Simon H.U. and Kimchi A. (2009) Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ., 16:966– 975.
  • Franzetti E., Huang Z., Shi Y., Xie K., Deng X., Li J., Yang W., Zeng W., Casartelli M., Deng H., Cappellozza S., Grimaldi A., Xia Q., Feng Q., Cao Y. and Tettamanti G. (2012) Autophagy precedes apoptosis during the remodeling of silkworm larval midgut. Apoptosis, 17 (3): 305-324
  • Gaikwad S. M., Aland S. R., Mamlayya A. B. and Bhawane G. P. (2011) Anatomy and histology of the alimentary canal of adult Papilio polytes polytes L. (Lepidoptera: Papilionidae). The Bioscan, 6(3):399-402.
  • Gavrieli Y., Sherman Y. and Ben-Sasson S.A. (1992) Identification of Programmed Cell Death In Situ via Nuclear DNA Fragmentation. International Journal Cell Biology, 119(3): 493-501.
  • 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, 4:8, 1069-1072.
  • Goncu E. and Parlak O. (2011) The influence of juvenile hormone analogue, fenoxycarb on the midgut remodeling in Bombyx mori (L., 1758) (Lepidoptera: Bombycidae) during larval-pupal metamorphosis. Türkiye Entomoloji Dergisi, 35 (2): 179-194.
  • Guillon-Munos A., van Bemmelen M.X.P. and Clarke P.G.H. (2006) Autophagy can be a killer even in apoptosis-competent cells. Autophagy, 2:140–142.
  • Jellinger K.A. and Stadelmann C. (2001) Problems of cell death in neurodegeneration and Alzheimer’s disease. J. Alzheimers Dis., 3:31–40.
  • Judy J.K. and Gilbert I.L. (1969) Morphology of the Alimentary Canal During the Metamorphosis of Hyalophora cecropia (Lepidoptera: Saturniidae). Annals of the Entomological Society of America, Vol.62, 1438-1445. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissues kinetics. British Journal of Cancer, 26:239-257.
  • Levy S.M., Falleiros A.M.F., Moscardi F. and Toledo L.A. (2004 a) Morphological Study of the Hindgut in Larvae of Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae). Neotropical Entomology, 33 (4): 427-431
  • Levy S.M., Falleiros AM.F., Gregorio E.A., Arrebola N.R.and Toledo, L.A. (2004 b) The larval midgut of Anticarsia gemmatalis (Hübner) (Lepidoptera: Noctuidea): Light and electron microscopy studies of the epithelial cells. Brazilian Journal of Biology, 64 (3b): 633-638.
  • Lockshin R. A. and Zakeri Z. (2004) Apoptosis, autophagy and more. The International Journal of Biochemistry & Cell Biology, 36: 2405–2419.
  • Loeb M.J., Clark E.A., Blackburn M., Hakim R.S., Elsen K. and Smagghe G. (2003) Stem Cells From Midguts of Lepidopteran Larvae: Clues to the Regulation of Stem Cell Fate. Archives of Insect Biochemistry and Physiology, 53, 186-198.
  • Malagoli D, Abdalla FC, Cao Y., Feng Q.L., Fujisaki K. and Gregorc A. (2010) Autophagy and its physiological relevance in arthropods: current knowledge and perspectives. Autophagy, 6:575–588.
  • Mathur L.M.L. (1973) Histology of the alimentary canal of the mature larva of Prodenia litura Fabr. (Lepidoptera). Tettamanti G., Grimaldi A., Casartelli M., Journal of Natural History, 7:653-664.
  • Nardi J. B., Miller L. A., Bee C. M., Lee Jr R. E. and Denlinger D. L. (2009) The larval alimentary canal of the Antarctic insect, Belgica antarctica. Arthropod Structure & Development, 38: 377-389.
  • Nijhout H.F.(1891) Physiological control of molting in insects. Amer. Zool., 21, 631- 640.
  • Parlak O. (2001) Silkworm Biology. Ege Üniversity Printery, 171, İzmir.
  • Parthasarathy R. and Palli S.R. (2007) Developmental and hormonal regulation of midgut remodeling in a lepidopteran insect, Heliothis virescens. Mechanisms of Development, 124:23–34.
  • Schweichel J.U. and Merker H.J. (1973) The morphology of various type of cell death in prenatal tissues. Teratology, 7:253-66.
  • Shen H.M. and Codogno P. (2011) Autophagic cell death: Loch Ness monster or endangered species. Autophagy, 7:457– 465.
  • Sridharan S., Jain K. and Basu A. (2011) Regulation of Autophagy by kinases. Cancers, 3,2630-2654. Ambrosetti E., Ponti B. and Congiu T. (2007) Programmed cell death and stem cell differentiation are responsible for midgut replacement in Heliothis virescens during prepupal instar. Cell Tissue Research, 330: 345–359.
  • Tettamanti G., Cao Y., Feng Q., Grimaldi A. and Eguileor M. (2011) Autophagy in Lepidoptera: more than old wine in new bottle. Invertebrate Survival Journal, 8:5– 14.

Bombyx mori (Lepidoptera: Bombycidae)

Year 2014, Volume: 73 Issue: 2, 1 - 29, 23.03.2016

Gözde Selek Ebru Göncü Osman Parlak

Abstract

Tam metamorfoz geçiren ipek böceklerinde, larval-pupal gelişim sırasında sindirim kanalı programlanmış hücre ölümü yoluyla dejenere olmaktadır. Gelişim biyolojisinde programlanmış hücre ölümü anahtar rol oynamaktadır. Programlanmış hücre ölümü genel olarak, Apoptotik ve otofajik hücre ölümü olarak isimlendirilen iki ana mekanizma ile gerçekleşmektedir. Bu çalışmadaki amacımız, larvalpupal metamorfoz sırasında, Bombyx mori sindirim sisteminde meydana gelen metamorfik olayların gösterilmesidir. Histolojik teknikler kullanılarak morfolojik değişimler gösterilmiştir; H&E ve PAS boyama yöntemleri kullanılarak dejeneratif hücreler belirlenmiştir. Apoptotik hücre nukleuslarını belirlemek için TUNEL yöntemi uygulanmıştır. Otofajik hücre ölümünü göstermek amacıyla ise Asit Fosfataz aktivite hesaplamaları gerçekleştirilmiştir. Sonuç olarak; bulgularımız, sindirim kanalında meydana gelen ölümde apoptoz ve otofajinin birlikte rol oynadığını göstermiştir

Keywords

Bombyx mori apoptoz sindirim sistemi otofaji TUNEL

References

  • Beaulaton J. and Lockshin R. A. (1982) The relation of programmed cell death to development and reproduction: comparative studies and an attempt at classification. Int. Rev. Cytol., 79,215-235.
  • Bergmeyer H.U. (1974) Methods of Enzymatic Analysis. 2nd edn, Volume 1, Academic Press, Inc., New York, Volume I, 495-496.
  • Billingsly P.F. and Lehane M.J. (1996) Structure and Ultrastructure of the insect midgut. Biology of the Insect Midgut. Chapman and Holl, London, 3-25.
  • Cavalcante V. M., Cruz-Landim C. Da (2004) Electrophoretic protein pattern and acid phosphatase activity in the midgut extracts of Apis mellifera L. during metamorphosis. Neotropical Entomology, 33(2): 169-172.
  • Clarke P.G. (1990) Developmental cell death: morphological diversity and multiple mechanism, Anatomy and Embryology (Berlin), 181, 195-213.
  • Kerr J.F.R., Wyllie A.H. and Currie A.R. (1972)
  • Eisenberg-Lerner A., Bialik S., Simon H.U. and Kimchi A. (2009) Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ., 16:966– 975.
  • Franzetti E., Huang Z., Shi Y., Xie K., Deng X., Li J., Yang W., Zeng W., Casartelli M., Deng H., Cappellozza S., Grimaldi A., Xia Q., Feng Q., Cao Y. and Tettamanti G. (2012) Autophagy precedes apoptosis during the remodeling of silkworm larval midgut. Apoptosis, 17 (3): 305-324
  • Gaikwad S. M., Aland S. R., Mamlayya A. B. and Bhawane G. P. (2011) Anatomy and histology of the alimentary canal of adult Papilio polytes polytes L. (Lepidoptera: Papilionidae). The Bioscan, 6(3):399-402.
  • Gavrieli Y., Sherman Y. and Ben-Sasson S.A. (1992) Identification of Programmed Cell Death In Situ via Nuclear DNA Fragmentation. International Journal Cell Biology, 119(3): 493-501.
  • 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, 4:8, 1069-1072.
  • Goncu E. and Parlak O. (2011) The influence of juvenile hormone analogue, fenoxycarb on the midgut remodeling in Bombyx mori (L., 1758) (Lepidoptera: Bombycidae) during larval-pupal metamorphosis. Türkiye Entomoloji Dergisi, 35 (2): 179-194.
  • Guillon-Munos A., van Bemmelen M.X.P. and Clarke P.G.H. (2006) Autophagy can be a killer even in apoptosis-competent cells. Autophagy, 2:140–142.
  • Jellinger K.A. and Stadelmann C. (2001) Problems of cell death in neurodegeneration and Alzheimer’s disease. J. Alzheimers Dis., 3:31–40.
  • Judy J.K. and Gilbert I.L. (1969) Morphology of the Alimentary Canal During the Metamorphosis of Hyalophora cecropia (Lepidoptera: Saturniidae). Annals of the Entomological Society of America, Vol.62, 1438-1445. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissues kinetics. British Journal of Cancer, 26:239-257.
  • Levy S.M., Falleiros A.M.F., Moscardi F. and Toledo L.A. (2004 a) Morphological Study of the Hindgut in Larvae of Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae). Neotropical Entomology, 33 (4): 427-431
  • Levy S.M., Falleiros AM.F., Gregorio E.A., Arrebola N.R.and Toledo, L.A. (2004 b) The larval midgut of Anticarsia gemmatalis (Hübner) (Lepidoptera: Noctuidea): Light and electron microscopy studies of the epithelial cells. Brazilian Journal of Biology, 64 (3b): 633-638.
  • Lockshin R. A. and Zakeri Z. (2004) Apoptosis, autophagy and more. The International Journal of Biochemistry & Cell Biology, 36: 2405–2419.
  • Loeb M.J., Clark E.A., Blackburn M., Hakim R.S., Elsen K. and Smagghe G. (2003) Stem Cells From Midguts of Lepidopteran Larvae: Clues to the Regulation of Stem Cell Fate. Archives of Insect Biochemistry and Physiology, 53, 186-198.
  • Malagoli D, Abdalla FC, Cao Y., Feng Q.L., Fujisaki K. and Gregorc A. (2010) Autophagy and its physiological relevance in arthropods: current knowledge and perspectives. Autophagy, 6:575–588.
  • Mathur L.M.L. (1973) Histology of the alimentary canal of the mature larva of Prodenia litura Fabr. (Lepidoptera). Tettamanti G., Grimaldi A., Casartelli M., Journal of Natural History, 7:653-664.
  • Nardi J. B., Miller L. A., Bee C. M., Lee Jr R. E. and Denlinger D. L. (2009) The larval alimentary canal of the Antarctic insect, Belgica antarctica. Arthropod Structure & Development, 38: 377-389.
  • Nijhout H.F.(1891) Physiological control of molting in insects. Amer. Zool., 21, 631- 640.
  • Parlak O. (2001) Silkworm Biology. Ege Üniversity Printery, 171, İzmir.
  • Parthasarathy R. and Palli S.R. (2007) Developmental and hormonal regulation of midgut remodeling in a lepidopteran insect, Heliothis virescens. Mechanisms of Development, 124:23–34.
  • Schweichel J.U. and Merker H.J. (1973) The morphology of various type of cell death in prenatal tissues. Teratology, 7:253-66.
  • Shen H.M. and Codogno P. (2011) Autophagic cell death: Loch Ness monster or endangered species. Autophagy, 7:457– 465.
  • Sridharan S., Jain K. and Basu A. (2011) Regulation of Autophagy by kinases. Cancers, 3,2630-2654. Ambrosetti E., Ponti B. and Congiu T. (2007) Programmed cell death and stem cell differentiation are responsible for midgut replacement in Heliothis virescens during prepupal instar. Cell Tissue Research, 330: 345–359.
  • Tettamanti G., Cao Y., Feng Q., Grimaldi A. and Eguileor M. (2011) Autophagy in Lepidoptera: more than old wine in new bottle. Invertebrate Survival Journal, 8:5– 14.
There are 29 citations in total.

Details

Primary Language English
Journal Section Research Articles
Authors

Gözde Selek

Ebru Göncü

Osman Parlak This is me

Publication Date March 23, 2016
Submission Date May 14, 2015
Published in Issue Year 2014 Volume: 73 Issue: 2

Cite

AMA Selek G, Göncü E, Parlak O. Programmed Cell Death in the Digestive Canal of Bombyx mori (Lepidoptera: Bombycidae) during Prepupal Period. Eur J Biol. March 2016;73(2):1-29.
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