Abstract
This study quantitatively compared proliferation and cell death in the remodeling of the midgut epithelium in Melipona quadrifasciata anthidioides during metamorphosis to elucidate the renewal mechanism of the midgut in bees during postembryonic development. An anti-phosphohistone H3 antibody was used to mark mitotic cells. An apoptotic cell marking kit was used (Apo-TRACE®) to identify cells undergoing the process of cell death. The ultrastructural aspects of cell death were also analyzed. The highest proliferative and apoptotic rates were observed in pink-eyed pupae. An increased number of cells and rebuilding of regenerative cell nests at the end of metamorphosis is a consequence of cell division in black-eyed pupae because cell division occurs at this stage in the absence of apoptosis. During metamorphosis, midgut epithelial cell death in M. quadrifasciata anthidioides occurs as a result of apoptosis and autophagy.
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References
Aloya, R., Shirvan, A., Grimberg, H., Reshefm, A., Levin, G., Kidron, D., Cohen, A., Ziv, I. (2006) Molecular imaging of cell death in vivo by a novel small molecule probe. Apoptosis 11, 2089–2101
Baldwin, K.M., Hakim, R.S. (1991) Growth and differentiation of the larval midgut epithelium during molt in the moth, Manduca sexta. Tissue Cell 23, 411–422
Champlin, D.T., Truman, J.W. (1998) Ecdysteroid control of cell proliferation during optic lobe formation in the moth Manduca sexta. Development 125, 269–277
Chapman, R.F. (1998) The Insects—Structure and Function. Cambridge, Cambridge
Corley, L.S., Lavine, M.D. (2006) A review of insect stem cell types. Semin. Cell. Dev. Biol. 17, 510–517
Cruz, L.C., Araújo, V.A., Dolder, H., Araújo, A.P.A., Serrão, J.E., Neves, C.A. (2011) Morphometry of the midgut of Melipona quadrifasciata anthidioides (Lepeletier) (Hymenoptera: Apidae) during metamorphosis. Neotrop. Entomol. 40, 677–681
Cruz-Landim, C. (2009) Abelhas: Morfologia e função de sistemas, 1st edn. UNESP, Rio Claro
Cruz-Landim, C., Cavalcante, V.M. (2003) Ultrastructural and cytochemical aspects of metamorphosis in the midgut of Apis mellifera L. (Hymenoptera: Apidae: Apinae). Zool. Sci. 20, 1099–1107
Cruz-Landim, C., Silva-de-Moraes, R.L.M. (2000) Morte celular programada em abelhas como uma forma de redirecionar a morfologia e a fisiologia adaptativa. Editora e Tipografia Costa, Rio Claro
Cruz-Landim, C., Mello, M.L.S. (1970) Post-embryonic changes in Melipona quadrifasciata anthidioides Lep. IV. Development of the digestive tract. Bol. Zool. Biol. Mar. 27, 229–263
Cruz-Landim, C., Silva-de-Moraes, R.L.M., Serrão, J.E. (1996) Ultrastructural aspects of epithelial renewal in the midgut of adult worker bees (Hymenoptera, Apidae). J. Comp. Biol. 1, 29–40
Denton, D., Shravage, B., Simin, R., Mills, K., Berry, D.L., Baehrecke, E.H., Kumar, S. (2009) Autophagy, not apoptosis, is essential for midgut cell death in Drosophila. Curr. Biol. 19, 1741–1746
Ferreira, R.A.C., Malaspina, O. (2009) Avaliação da toxicidade de doses sub-letais de fipronil e ácido bórico em adultos de Scaptotrigona postica (Latreille, 1807) (Hymenoptera, Apidae). O Biológico 71, 178–178
Franzetti, E., Huang, Z.J., Shi, Y.X., Xie, K., Deng, X.J., Li, J.P., Li, Q.R., Yang, W.Y., Zeng, W.N., Casartelli, M., Deng, H.M., Cappellozza, S., Grimaldi, A., Xia, Q., Tettamanti, G., Cao, Y., Feng, Q. (2012) Autophagy precedes apoptosis during the remodeling of silkworm larval midgut. Apoptosis 17, 305–324
Gama, V., Cruz-Landim, C. (1984) Morfologia do tubo digestivo de Camponotus (Myrmothix) rufipes (Fabricius, 1975) (Hymenoptera, Formicidae) durante a metamorfose. Naturalia 9, 43–55
Hakim, R.S., Baldwin, K., Smagghe, G. (2010) Regulation of midgut growth, development, and metamorphosis. Annu. Rev. Ent. 55, 593–608
Hendzel, M.J., Wei, Y., Mancini, M.A., Van-Hooser, A., Ranalli, T., Brinkley, B.R., Bazett-Jones, D.P., Allis, C.D. (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348–60
Illa-Bochaca, I., Montuenga, L.M. (2006) The regenerative nidi of the locust midgut as a model to study epithelial cell differentiation from stem cells. J. Exp. Biol. 209, 2215–2223
Jiang, C., Baehrecke, E.H., Thummel, C.S. (1997) Steroid regulated programmed cell death during Drosophila metamorphosis. Development 124, 4673–4683
Martins, G.F., Neves, C.A., Campos, L.O., Serrão, J.E. (2006) The regenerative cells during the metamorphosis in the midgut of bees. Micron 37, 161–168
Nardi, J.B., Bee, C.M., Miller, L.A. (2010) Stem cells of the beetle midgut epithelium. J. Insect Physiol. 56, 296–303
Neves, C.A., Serrão, J.E., Gitirana, L.B. (2003) Ultrastructural study of the metamorphosis in the midgut of Melipona quadrifasciata anthidioides (Apidae, Meliponini) worker. Sociobiology 41, 443–459
Pinto, L.Z., Hartfelder, K., Gentile-Bitondi, M.M., Simões, Z.L.P. (2002) Ecdysteroid titers in pupae of highly social bees relate to distinct modes of caste development. J. Insect Physiol. 48, 783–790
Rost, M.M. (2006) Ultrastructural changes in the midgut epithelium in Podura aquatica L. (Insecta, Collembola, Arthropleona) during regeneration. Arthrop. Struct. Devel. 35, 69–76
Rost-Roszkowska, M.M. (2008) Ultrastructural Changes in the midgut epithelium of Acheta domesticus (Orthoptera: Gryllidae) during degeneration and regeneration. Ann. Entomol. Soc. Am. 101, 151–158
Rost-Roszkowska, M.M., Machidab, R., Fukuib, M. (2010) The role of cell death in the midgut epithelium in Filientomon takanawanum (Protura). Tissue Cell 42, 24–31
Santos, C.G., Neves, C.A., Zanuncio, J.C., Serrão, J.E. (2009) Postembryonic development of rectal pads in bees (Hymenoptera, Apidae). Anat. Rec. 292, 1602–1611
Serrão, J.E., Cruz-Landim, C. (1996) Ultrastructure of digestive cells in stingless bees of various ages (Hymenoptera, Apidae, Meliponinae). Cytobios 88, 161–171
Snodgrass, R.E. (1956) Anatomy of the Honey Bee. Comstock, Ithaca. 333
Stefanini, M., De Martino, C., Zamboni, L. (1967) Fixation of ejaculated spermatozoa for electron microscopy. Nature 216, 173–174
Tettamanti, G., Crimaldi, A., Casartelli, M., Ambrosetti, E., Ponti, B., Congiu, T., Ferrrese, R., Rivas-Pena, M.L., Pennacchio, F., Eguileor, M. (2007) Programmed cell death and stem cell differentiation are responsible for midgut replacement in Heliothis virescens during prepupal instar. Cell Tiss. Res. 330(2), 345–359
Uwo, M.F., Ui-Tei, K., Park, P., Takeda, M. (2002) Replacement of midgut epithelium in the greater wax moth, Galleria mellonela, during larval-pupal moult. Cell Tiss. Res. 308, 319–331
Ward, K.N., Coleman, J.L., Clinnin, K., Fahrbach, S., Rueppell, O. (2008) Age, caste, and behavior determine the replicative activity of intestinal stem cells in honeybees (Apis mellifera L.). Exp. Gerontol. 43, 530–537
Acknowledgments
We are grateful to the Microscopy and Microanalysis Center of the Federal University of Viçosa, for technical assistance. This research was supported by Brazilian research agencies CAPES (PDSE–Proc. 4850-11-4), FAPEMIG, and CNPq.
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Manuscript editor: Klaus Hartfelder
Prolifération et mort cellulaire dans l’intestin moyen de l’abeille sans aiguillon Melipona quadrifasciata anthidioides (Apidae, Meliponini) durant la métamorphose
Intestin moyen / cellule régénératrice / mort cellulaire / apoptose / métamorphose / Hymenoptera
Zellteilung und Zelltod im Mitteldarm der Stachellosen Biene Melipona quadrifasciata anthidioides (Apidae, Meliponini) im Verlauf der Metamorphose
Mitteldarm / regenerative Zellen / Zelltod / Metamorphose / Hymenoptera
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Cruz, L.C., Araújo, V.A., do Carmo Queiroz Fialho, M. et al. Proliferation and cell death in the midgut of the stingless bee Melipona quadrifasciata anthidioides (Apidae, Meliponini) during metamorphosis. Apidologie 44, 458–466 (2013). https://doi.org/10.1007/s13592-013-0196-7
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DOI: https://doi.org/10.1007/s13592-013-0196-7