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Autophagy precedes apoptosis during the remodeling of silkworm larval midgut

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An Erratum to this article was published on 06 January 2012

Abstract

Although several features of apoptosis and autophagy have been reported in the larval organs of Lepidoptera during metamorphosis, solid experimental evidence for autophagy is still lacking. Moreover, the role of the two processes and the nature of their relationship are still cryptic. In this study, we perform a cellular, biochemical and molecular analysis of the degeneration process that occurs in the larval midgut of Bombyx mori during larval–adult transformation, with the aim to analyze autophagy and apoptosis in cells that die under physiological conditions. We demonstrate that larval midgut degradation is due to the concerted action of the two mechanisms, which occur at different times and have different functions. Autophagy is activated from the wandering stage and reaches a high level of activity during the spinning and prepupal stages, as demonstrated by specific autophagic markers. Our data show that the process of autophagy can recycle molecules from the degenerating cells and supply nutrients to the animal during the non-feeding period. Apoptosis intervenes later. In fact, although genes encoding caspases are transcribed at the end of the larval period, the activity of these proteases is not appreciable until the second day of spinning and apoptotic features are observable from prepupal phase. The abundance of apoptotic features during the pupal phase, when the majority of the cells die, indicates that apoptosis is actually responsible for cell death and for the disappearance of larval midgut cells.

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Acknowledgments

We thank Professor Congzhao Zhou (University of Science and Technology of China) for providing pET-28b-BmATG8 expression vector. This work was supported by a grant from the Italian Ministry of University and Research (PRIN 2008, protocol 2008SMMCJY) and by FAR 2009–2010 (University of Insubria) to GT, and by grants from the “973” National Basic Research Program of China (No. 2012CB114602), the “863” National High Technology and Research Program of China (No. SQ2010AA1000688007) and Guangdong Province Natural Science Foundation (No. 06105204) to YC and QF.

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Biotechnology and Life Sciences, University of Insubria, Via J. H. Dunant, 3, 21100, Varese, Italy

    Eleonora Franzetti, Annalisa Grimaldi & Gianluca Tettamanti

  2. Laboratory of Insect Molecular Biology and Biotechnology, Guangdong Provincial Key Laboratory of Agro-animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural University, TianHe, Wushan Street, Guangzhou, 510642, China

    Zhi-Jun Huang, Yan-Xia Shi, Kun Xie, Xiao-Juan Deng, Jian-Ping Li, Qing-Rong Li, Wan-Ying Yang, Wen-Nian Zeng & Yang Cao

  3. The Sericulture & Agri-Food Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, 510610, China

    Qing-Rong Li

  4. Department of Biology, Università degli Studi di Milano, 20133, Milano, Italy

    Morena Casartelli

  5. Guangdong Provincial Key Lab of Biotechnology for Plant Development, School of Life Sciences, South China Normal University, Guangzhou, 510631, China

    Hui-Min Deng & Qili Feng

  6. CRA - Honey Bee and Silkworm Research Unit, Padua Seat, 35143, Padova, Italy

    Silvia Cappellozza

  7. Institute of Sericulture and Systems Biology, Southwest University, Chongqing, 400716, China

    Qingyou Xia

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  1. Eleonora Franzetti
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  14. Qingyou Xia
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  15. Gianluca Tettamanti
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Corresponding authors

Correspondence to Gianluca Tettamanti, Yang Cao or Qili Feng.

Additional information

E. Franzetti and Z.-J. Huang contributed equally to this work.

An erratum to this article can be found at http://dx.doi.org/10.1007/s10495-011-0693-y.

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Franzetti, E., Huang, ZJ., Shi, YX. et al. Autophagy precedes apoptosis during the remodeling of silkworm larval midgut. Apoptosis 17, 305–324 (2012). https://doi.org/10.1007/s10495-011-0675-0

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