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Autophagy and Apoptosis in the Midgut Epithelium of Millipedes

Part of: Micrographia Collection

Published online by Cambridge University Press:  20 May 2019

M.M. Rost-Roszkowska ,
J. Vilimová ,
K. Tajovský ,
A. Chachulska-Żymełka ,
A. Sosinka ,
M. Kszuk-Jendrysik ,
A. Ostróżka  and
F. Kaszuba
M.M. Rost-Roszkowska*
Affiliation:
Department of Animal Histology and Embryology, University of Silesia in Katowice, Bankowa 9, 40-007 Katowice, Poland
J. Vilimová
Affiliation:
Department of Zoology, Charles University, Faculty of Science, Viničná 7, 128 44 Prague 2, Czech Republic
K. Tajovský
Affiliation:
Institute of Soil Biology, Biology Centre CAS, Na Sádkách 7, 370 05 České Budějovice, Czech Republic
A. Chachulska-Żymełka
Affiliation:
Department of Animal Histology and Embryology, University of Silesia in Katowice, Bankowa 9, 40-007 Katowice, Poland
A. Sosinka
Affiliation:
Department of Animal Histology and Embryology, University of Silesia in Katowice, Bankowa 9, 40-007 Katowice, Poland
M. Kszuk-Jendrysik
Affiliation:
Department of Animal Histology and Embryology, University of Silesia in Katowice, Bankowa 9, 40-007 Katowice, Poland
A. Ostróżka
Affiliation:
Department of Animal Histology and Embryology, University of Silesia in Katowice, Bankowa 9, 40-007 Katowice, Poland
F. Kaszuba
Affiliation:
Department of Animal Histology and Embryology, University of Silesia in Katowice, Bankowa 9, 40-007 Katowice, Poland
*
*Author for correspondence: M.M. Rost-Roszkowska, E-mail: magdalena.rost-roszkowska@us.edu.pl
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Abstract

The process of autophagy has been detected in the midgut epithelium of four millipede species: Julus scandinavius, Polyxenus lagurus, Archispirostreptus gigas, and Telodeinopus aoutii. It has been examined using transmission electron microscopy (TEM), which enabled differentiation of cells in the midgut epithelium, and some histochemical methods (light microscope and fluorescence microscope). While autophagy appeared in the cytoplasm of digestive, secretory, and regenerative cells in J. scandinavius and A. gigas, in the two other species, T. aoutii and P. lagurus, it was only detected in the digestive cells. Both types of macroautophagy, the selective and nonselective processes, are described using TEM. Phagophore formation appeared as the first step of autophagy. After its blind ends fusion, the autophagosomes were formed. The autophagosomes fused with lysosomes and were transformed into autolysosomes. As the final step of autophagy, the residual bodies were detected. Autophagic structures can be removed from the midgut epithelium via, e.g., atypical exocytosis. Additionally, in P. lagurus and J. scandinavius, it was observed as the neutralization of pathogens such as Rickettsia-like microorganisms. Autophagy and apoptosis ca be analyzed using TEM, while specific histochemical methods may confirm it.

Keywords

cell deathdigestive systemDiplopodahistochemistrymidgutultrastructure
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 25 , Issue 4 , August 2019 , pp. 1004 - 1016
Copyright
Copyright© Microscopy Society of America 2019 

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References

Allegranza, A, Tredici, G, Marmirolli, P, di Donato, S, Franceschetti, S & Mariani, C (1989). Sialidosis type I: Pathological study in an adult. Clin Neuropathol 8, 266–271.Google Scholar
Baton, LA & Ranford-Cartwright, LC (2007). Morphological evidence for proliferative regeneration of the Anopheles stephensi midgut epithelium following Plasmodium falciparum ookinete invasion. J Invertebr Pathol 96, 244–254.Google Scholar
Bernales, S, McDonald, KL & Walter, P (2006). Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 4(12), e423.Google Scholar
Bernales, S, Schuck, S & Walter, P (2007). Selective autophagy of the endoplasmic reticulum. Autophagy 3, 285–287.Google Scholar
Boya, P, Gonzales-Polo, RA, Casares, N, Perfettini, JL, Dessen, P, Larochette, N, Métivier, D, Meley, D, Souquere, S, Yoshimori, T, Pierron, G, Codogno, P & Kroemer, G (2005). Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25, 1025–1040.Google Scholar
Camargo-Mathias, MI, Fantazzini, ER & Fontanetti, CS (2004). Ultrastructural features of the midgut of Rhinocricus padbergi (Diplopoda: Spirobolida). Braz J Morphol Sci 21, 65–71.Google Scholar
Cebollero, E, Reggiori, F & Kraft, C (2012). Reticulophagy and ribophagy: Regulated degradation of protein production factories. Int J Cell Biol. 2012: 182834 (it is published abstract)Google Scholar
Chajec, Ł, Rost-Roszkowska, MM, Vilimova, J & Sosinka, A (2012). Ultrastructure and regeneration of midgut epithelial cells in Lithobius forficatus (Chilopoda, Lithobiidae). Inv Biol 131, 119–132.Google Scholar
Chajec, Ł, Sonakowska, L & Rost-Roszkowska, MM (2014). The fine structure of the midgut epithelium in a centipede, Scolopendra cingulata (Chilopoda, Scolopendridae) with the special emphasis on epithelial regeneration. Arthropod Struct Dev 43, 27–42.Google Scholar
Cruz, LC, Araújo, VA, Dolder, H, Araújo, APA, Serrão, JE & Neves, CA (2011). Morphometry of the midgut of Melipona quadrifasciata anthidioides (Lepeletier) (Hymenoptera: Apidae) during metamorphosis. Neotrop Entomol 40(6), 677–681.Google Scholar
De Godoy, JAP & Fontanetti, CS (2010). Diplopods as bioindicators of soils: Analysis of midgut of individuals maintained in substract containing sewage sludge. Water Air Soil Pollut 210, 389–398.Google Scholar
Demine, S, Michel, S, Vannuvel, K, Wanet, A, Renard, P & Arnould, T (2012). Macroautophagy and cell responses related to mitochondrial dysfunction, lipid metabolism and unconventional secretion of proteins. Cells 1(2), 168–203.Google Scholar
Eitzinger, B, Micic, A, Körner, M, Traugott, M & Scheu, S (2013). Unveiling soil food web links: New PCR assays for detection of prey DNA in the gut of soil arthropod predators. Soil Biol Biochem 57, 943–945.Google Scholar
Fantazzini, ER, Fontanetti, CS & Camargo-Mathias, MI (2002). Midgut of the millipede, Rhinocricus padbergi (Verhoeff, 1938) (Diplopoda: Spirobolida): Histology and histochemistry. Arthropoda Sel 11, 135–142.Google Scholar
Fernandes, KM, Neves, CA, Serrão, JE & Martins, GF (2014). Aedes aegypti midgut remodeling during metamorphosis. Parasitol Int 63(3), 506–512.Google Scholar
Fontanetti, CS & Camargo-Mathias, MI (1997). Histoanatomy of the digestive tract in Plusioporus setiger diplopod (Brolemann, 1901) (Spirostreptida, Spirostreptidae). Braz J Morphol Sci 14, 205–211.Google Scholar
Fontanetti, CS & de Godoy, JAP (2007). Ultrastructural alterations observed in the midgut of the diplopod Rhinocricus padbergi exposed to sewage mud. Acta Microsc 16, 191–192.Google Scholar
Fontanetti, CS, Tiritan, B & Camargo-Mathias, MI (2006). Mineralized bodies in the fat body of Rhinocricus padbergi (Diplopoda). Braz J Morphol Sci 23, 487–493.Google Scholar
Fontanetti, CS, Moreira-de-Sousa, C, Pinheiro, TG, Souza, RB & Francisco, A (2015). Diplopoda-digestive system. In The Myriapoda. Treatise on Zoology—Anatomy, Taxonomy, Biology, Minelli, A (Ed.), pp. 109–127. the Netherlands, Brill, Leiden, Boston: Printforce.Google Scholar
Franzetti, E, Huang, ZJ, Shi, Y, et al. (2012). Autophagy precedes apoptosis during the remodeling of silkworm larval midgut. Apoptosis 17, 305–324.Google Scholar
Giusti, F, Dallai, L, Beani, L, et al. (2007). The midgut ultrastructure of the endoparasite Xenos vesparum (Rossi) (Insecta, Strepsiptera) during post-embryonic development and stable carbon isotopic analyses of the nutrient uptake. Arthropod Struct Dev 36, 183–197.Google Scholar
Gozuacik, D & Kimchi, A (2007). Autophagy and cell death. Curr Top Dev Biol 78, 217–245.Google Scholar
Hakim, RS, Baldwin, KM & Loeb, M (2001). The role of stem cells in midgut growth and regeneration. In Vitro Cell Dev Biol Animal 37(6), 338–342.Google Scholar
Hakim, RS, Caccia, S & Loeb, M (2009). Primary culture of insect midgut cells. In Vitro Cell Dev Biol Animal 45(3–4), 106–110.Google Scholar
Hariri, M, Millane, G, Guimond, MP, Guay, G, Dennis, JW & Nabi, IR (2000). Biogenesis of multilamellar bodies via autophagy. Mol Biol Cell 11(1), 255–268.Google Scholar
He, C & Klionsky, D (2009). Regulation Mechanisms and Signaling Pathways of Autophagy. Annu Rev Genet 43, 67–93.Google Scholar
Hopkin, SP & Read, HJ (1992). The Biology of Millipedes, pp. 1–233. New York: Oxford University Press.Google Scholar
Karasov, WH, Martinez del Rio, C & Caviedes-Vidal, E (2011). Ecological physiology of diet and digestive systems. Annu Rev Physiol 73, 69–93.Google Scholar
Karpeta-Kaczmarek, J, Augustyniak, M & Rost-Roszkowska, M (2016). Ultrastructure of the gut epithelium in Acheta domesticus after long- term exposure to nanodiamonds supplied with food. Arthropod Struct Dev 45, 253–264.Google Scholar
Khoa, DB & Takeda, M (2012). Expression of autophagy 8 (Atg8) and its role in the midgut and other organs of the greater wax moth, Galleria mellonella, during metamorphic remodeling and under starvation. Insect Mol Biol 21, 473–487.Google Scholar
Larsson, N-G & Masucci, MG (2016). Scientific Background: Discoveries of Mechanisms for Autophagy. Nobel Media AB, 2014. The Nobel assembly at Karolinska Institutet. http://www.nobelprizemedicine.org/wpcontent/uploads/2016/10/Scientific-Background-2016.pdfGoogle Scholar
Lee, CY, Clough, EA, Yellon, P, Teslovich, TM, Stephan, DA & Baehrecke, EH (2003). Genome wide analyses of steroid—and radiation triggered programmed cell death in Drosophila. Curr Biol 13(4), 350–357.Google Scholar
Levine, B & Klionsky, DJ (2004). Development by self-digestion: Molecular mechanisms and biological functions of autophagy. Dev Cell 6, 463–477.Google Scholar
Lewis, PR & Knight, DP (1992). Cytochemical Staining Methods for Electron Microscopy. USA: Elsevier, University of Michigan.Google Scholar
Lipovšek, S & Novak, T (2015). Autophagy in the fat body cells of the cave cricket Troglophilus neglectus Krauss, 1878 (Rhaphidophoridae, Saltatoria) during overwintering. Protoplasma 253, 457–466.Google Scholar
Lipovšek, S, Novak, T, Janžekovič, F & Leitinger, G (2015). Changes in the midgut diverticula in the harvestmen Amilenus aurantiacus (Phalangiidae, Opiliones) during winter diapause. Arthropod Struct Dev 44, 131–141.Google Scholar
Lipovšek, S, Leitinger, G, Novak, T, Janžekovič, F, Gorgoń, S, Kamińska, K & Rost-Roszkowska, M (2018). Changes in the midgut cells in the European cave spider, Meta menardi, during starvation in spring and autumn. Histochem Cell Biol 149(3), 245–260.Google Scholar
Liu, K & Czaja, MJ (2013). Regulation of lipid stores and metabolism by lipophagy. Cell Death Differ 20, 3–11.Google Scholar
Maghsoudi, N, Zakeri, Z & Lockshin, RA (2012). Programmed cell death and apoptosis–where it came from and where it is going: From Elie Metchnikoff to the control of caspases. Exp Oncol 34, 146–152.Google Scholar
Malagoli, D, Abdalla, FC, Cao, Y, et al. (2010). Autophagy and its physiological relevance in arthropods current knowledge and perspectives. Autophagy 6, 575–588.Google Scholar
Mijaljica, D, Prescott, M & Devenish, RJ (2012). The intriguing life of autophagosomes. Int J Mol Sci 13, 3618–3635.Google Scholar
Mitra, A & Flynn, KJ (2007). Importance of interactions between food quality, quantity, and gut transit time on consumer feeding, growth, and trophic dynamics. Am Nat 169, 632–646.Google Scholar
Moreira-de-Sousa, C, Iamonte, M & Fontanetti, CS (2017). Midgut of the diplopod Urostreptus atrobrunneus: Structure, function, and redefinition of hepatic cells. Braz J Biol 77(1), 132–139.Google Scholar
Mpakou, VE, Velentzas, AD, Velentzas, PD, et al. (2011). Programmed cell death of the ovarian nurse cells during oogenesis of the ladybird beetle Adalia bipunctata (Coleoptera: Coccinellidae). Dev Growth Differ 53, 804–815.Google Scholar
Narendra, D, Tanaka, A, Suen, DF & Youle, RJ (2008). Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183, 795–803.Google Scholar
Nogarol, LR & Fontanetti, CS (2011). Ultrastructural alterations in the midgut of diplopods after subchronic exposure to substrate containing sewage mud. Water Air Soil Pollut 218, 539–547.Google Scholar
Orrenius, S (2004). Mitochondrial regulation of apoptotic cell death. Toxicol Lett 149, 19–23.Google Scholar
Park, MS, Park, P & Takeda, M (2013). Roles of fat body trophocytes, mycetocytes and urocytes in the American cockroach, Periplaneta americana under starvation conditions: An ultrastructural study. Arthropod Struct Dev 42, 287–295.Google Scholar
Rost-Roszkowska, M, Machida, R & Fukui, M (2010). The role of cell death in the midgut epithelium in Filientomon takanawanum (Protura). Tissue Cell 42, 24–31.Google Scholar
Rost-Roszkowska, MM, Vilimova, J, Sosinka, A, Skudlik, J & Franzetti, E (2012). The role of autophagy in the midgut epithelium of Eubranchipus grubii (Crustacea, Branchiopoda, Anostraca). Arthropod Struct Dev 41, 271–279.Google Scholar
Rost-Roszkowska, MM, Chajec, Ł, Vilimova, J, Tajovský, K & Kszuk-Jendrysik, M (2015). Does autophagy in the midgut epithelium of centipedes depend on the day/night cycle? Micron 68, 130–139.Google Scholar
Rost-Roszkowska, MM, Chajec, Ł, Vilimova, J & Tajovsky, K (2016). Apoptosis and necrosis during the circadian cycle in the centipede midgut. Protoplasma 253(4), 1051–1061.Google Scholar
Rost-Roszkowska, MM, Vilimová, J, Tajovský, K, et al. (2018 a). The ultrastructure of the hepatic cells in millipedes (Myriapoda, Diplopoda). Zool Anz 274, 95–102.Google Scholar
Rost-Roszkowska, M, Kszuk-Jendrysik, M, Marchewka, A & Poprawa, I (2018 b). Fine structure of the midgut epithelium in the millipede Telodeinopus aoutii (Myriapoda, Diplopoda) with special emphasis on epithelial regeneration. Protoplasma 255, 43–55.Google Scholar
Rost-Roszkowska, M, Janelt, K & Poprawa, I (2018 c). The role of autophagy in the midgut epithelium of Parachela (Tardigrada). Zoomorphology 137, 501–509.Google Scholar
Santos, DE, Zanuncio, JC, Gonçalves de Oliveira, AA & Serrao, JE (2016). Endocrine cells in the midgut of bees (Hymenoptera: Apoidea) with different levels of sociability. J Apicult Res 54(4), 394–398.Google Scholar
Schmitz, G & Müller, G (1991). Structure and function of lamellar bodies, lipid-protein complexes involved in storage and secretion of cellular lipids. J Lipid Res 32, 1539–1570.Google Scholar
Semenza, GL (2008). Mitochondrial autophagy: Life and breath of the cell. Autophagy 4(4), 534–536.Google Scholar
Sigling, S (2010). Professional Breeders Series: Millipedes, 205 pp. Edition Chimaira, Germany: Frankfurt am Main.Google Scholar
Sokolova, YY, Lange, CE & Fuxa, JR (2006). Development, ultrastructure, natural occurrence, and molecular characterization of Liebermannia patagonica n. g., n. sp., a microsporidian parasite of the grasshopper Tristira magellanica (Orthoptera: Tristiridae). J Inv Pathol 91, 168–182.Google Scholar
Sonakowska, L, Włodarczyk, A, Wilczek, G, Wilczek, P, Student, S & Rost-Roszkowska, MM (2016). Cell death in the epithelia of the intestine and hepatopancreas in Neocaridina heteropoda (Crustacea, Malacostraca). PLoS ONE, 11, e0147582.Google Scholar
Sosinka, A, Rost-Roszkowska, MM, Vilimova, J, Tajovský, K, Kszuk-Jendrysik, M, Chajec, Ł, Sonakowska, L, Kamińska, K, Hyra, M & Poprawa, I (2014). The ultrastructure of the midgut epithelium in millipedes (Myriapoda, Diplopoda). Arthropod Struct Dev 43, 477–492.Google Scholar
Souza, TS & Fontanetti, CS (2011). Morphological biomarkers in the Rhinocricus padbergi midgut exposed to contaminated soil. Ecotoxicol Environ Safety 74, 10–18.Google Scholar
Šustr, V, Tajovský, K, Semanová, S, Chronakova, A & Simek, M (2013). The giant African millipede, Archispirostreptus gigas (Diplopoda: Spirostreptida), a model species for ecophysiological studies. Acta Soc Zool Bochem 77, 145–158.Google Scholar
Teixeira, AD, Fialho, MCQ, Zanuncio, JC, Ramalho, FS & Serrão, JE (2013). Degeneration and cell regeneration in the midgut of Podisus nigrispinus (Heteroptera: Pentatomidae) during post-embryonic development. Arthropod Struct Dev 42, 237–246.Google Scholar
Tettamanti, G, Cao, Y, Feng, Q, Grimaldi, A & de Eguileor, M (2011). Autophagy in Lepidoptera: More than old wine in new bottle. ISJ 8, 5–14.Google Scholar
Tsujimoto, Y & Shimizu, S (2005). Another way to die: Autophagic programmed cell death. Cell Death Differ 12, 1528–1534.Google Scholar
Vaidyanathan, R & Scott, TW (2006). Apoptosis in mosquito midgut epithelia associated with West Nile virus infection. Apoptosis 11, 1643–1651.Google Scholar
Wilczek, G, Rost-Roszkowska, M, Wilczek, P, Babczyńska, A, Szulińska, E, Sonakowska, L & Marek-Swędzioł, M (2014). Apoptotic and necrotic changes in the midgut glands of the wolf spiders Xerolycosa nemoralis (Lycosidae) in response to starvation and dimethoate exposure. Ecotoxic Environ Safe 101, 157–167.Google Scholar
Włodarczyk, A, Sonakowska, L, Kamińska, K, Marchewka, A, Wilczek, G, Wilczek, P, Studnet, S & Rost-Roszkowska, M (2017). The effect of starvation and re-feeding on mitochondrial potential in the midgut of Neocaridina davidi (Crustacea, Malacostraca). PLoS ONE 12(3), e0173563.Google Scholar