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Ovaries and testes of Lithobius forficatus (Myriapoda, Chilopoda) react differently to the presence of cadmium in the environment

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  • Sieńczuk, W. Toksykologia (PZWL Warszawa, 1999) (in Polish).

    Google Scholar 

  • Kabata-Pendias, A. & Pendias, H. Biochemia pierwiastków śladowych (PZWL Warszawa, 1999) (in Polish).

    Google Scholar 

  • Sharma, H., Rawal, N. & Mathew, B. B. The characteristics, toxicity and effects of cadmium. Int. J. Nanosci. Nanotechnol. 3, 1–9 (2015).

    Google Scholar 

  • Duarte, A. et al. (eds) Soil pollution: From Monitoring to Remediation 1st edn. (Academic Press, 2017).

    Google Scholar 

  • Zhang, H. & Reynolds, M. Cadmium exposure in living organisms: A short review. Sci. Total Environ. 678, 761–767 (2019).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Lane, T. W. et al. A cadmium enzyme from a marine diatom. Nature 435, 42 (2005).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Jӓrup, L. Hazards of heavy metal contamination. Br. Med. Bull. 68, 167–182 (2003).

    Article 

    Google Scholar 

  • Massányi, P., Massányi, M., Madeddu, R., Stawarz, R. & Lukáč, N. Effects of cadmium, lead, and mercury on the structure and function of reproductive organs. Toxics 8, 94 (2020).

    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Roy, S. Cadmium accumulation in crops and the increasing risk of dietary cadmium exposure: An overview. In Cadmium Tolerance in Plants: Agronomic, Molecular, Signaling, and Omic Approaches (eds Hasanuzzaman, M. et al.) 247–254 (Academic Press, 2019).

    Chapter 

    Google Scholar 

  • Templeton, D. M. & Liu, Y. Multiple roles of cadmium in cell death and survival. Chem. Biol. Interact. 188, 267–275 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Stojsavljević, A. et al. Evaluation of trace metals in thyroid tissues: Comparative analysis with benign and malignant thyroid diseases. Ecotoxicol. Environ. Saf. 183, 109479 (2019).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Lewis, J. G. E. The Biology of Centipedes 1st edn. (Cambridge University Press, 1981).

    Book 

    Google Scholar 

  • Hopkin, S. P. Ecophysiology of Metals in Terrestrial Invertebrates 1st edn. (Elsevier Applied Science, 1989).

    Google Scholar 

  • Hopkin, S. P. & Read, H. J. The Biology of Millipedes (Oxford University Press, 1992).

    Google Scholar 

  • Lipovšek, S., Letofsy-Papst, I., Hofer, F. & Pabst, M. A. Seasonal- and age-dependent changes of the structure and chemical composition of the spherites in the midgut gland of the harvestmen Gyas annulatus (Opiliones). Micron 33, 647–654 (2002).

    PubMed 
    Article 

    Google Scholar 

  • Chajec, Ł, Rost-Roszkowska, M. M., Vilimova, J. & Sosinka, A. Ultrastructure and regeneration of midgut epithelial cells in Lithobius forficatus (Chilopoda, Lithobiidae). Invertebr. Biol. 131, 119–132 (2012).

    Article 

    Google Scholar 

  • Hopkin, S. P., Watson, K., Martin, M. H. & Mould, M. L. The assimilation of heavy metals by Lithobius variegatus and Glomeris marginata (Chilopoda; Diplopoda). Bijdr. Dierkd. 55, 88–94 (1985).

    Google Scholar 

  • Adiyodi, K. G. & Adiyodi, R. G. (eds) Reproductive Biology of Invertebrates. Volume I. Oogenesis, Oviposition, and Oosorption (Wiley, 1983).

    Google Scholar 

  • Adiyodi, K. G. & Adiyodi, R. G. (eds) Reproductive Biology of Invertebrates. Volume II. Spermatogenesis and Sperm Function (Wiley, 1983).

    Google Scholar 

  • Sareen, M. L. & Adiyodi, K. G. Arthropoda – Myriapoda. In Reproductive Biology of Invertebrates. Volume I. Oogenesis, Oviposition, and Oosorption (eds Adiyodi, K. G. & Adiyodi, R. G.) 497–520 (Wiley, 1983).

    Google Scholar 

  • Minelli, A. Chilopoda – Reproduction. In Treatise on Zoology – Anatomy, Taxonomy, Biology. The Myriapoda. Vol. 1. Chilopoda (ed. Minelli, A.) 279–294 (Brill, 2011).

    Chapter 

    Google Scholar 

  • Parolini, M. Toxicity of the non-steroidal anti-inflammatory drugs (NSAIDs) acetylsalicylic acid, paracetamol, diclofenac, ibuprofen and naproxen towards freshwater invertebrates: A review. Sci. Total Environ. 740, 140043 (2020).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Nath, V. Oogenesis of Lithobius forficatus. Biol. Rev. 1, 148–157 (1924).

    Article 

    Google Scholar 

  • Nath, V. Spermathogenesis of Lithobius forficatus. Biol. Rev. 1, 270–277 (1925).

    Article 

    Google Scholar 

  • Descamps, M. Etude ultrastructurale des spermatogonies et de la croissance spermatocytaire chez Lithobius forficatus L. (Myriapode Chilopode). Z. Zellforsch. 121, 14–26 (1971).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Descamps, M. Le cycle spermatogenétique chez Lithobius forficatus L. (Myriapode, Chilopode). I. Evolution et etude quantitative des populations cellulaires du tes ticle au cours du développement post-embryonnaire. Arch. Zool. Exp. Gen. 112, 199–209 (1971).

    Google Scholar 

  • Herbaut, C. Etude cytochimique et ultrastructurale de l’ovogenése chez Lithobius forficatus L. (Myriapode Chilopode). Evolution des constituants cellulaires. Wilhelm Roux’ Arch. 170, 115–134 (1972).

    CAS 
    Article 

    Google Scholar 

  • Descamps, M., Fabre, M. C., Grelle, C. & Gerard, S. Cadmium and lead kinetics during experimental contamination of the centipede Lithobius forficatus L. Arch. Environ. Contam. Toxicol. 31, 350–353 (1996).

    CAS 
    Article 

    Google Scholar 

  • Vandenbulcke, F., Grelle, C., Fabre, M.-C. & Descamps, M. Implication of the midgut of the centipede Lithobius forficatus in the heavy metal detoxification process. Ecotoxicol. Environ. Saf. 41, 258–268 (1998).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Rost-Roszkowska, M. et al. Influence of soil contaminated with cadmium on cell death in the digestive epithelium of soil centipede Lithobius forficatus (Myriapoda, Chilopoda). Eur. Zool. J. 87, 242–262 (2020).

    CAS 
    Article 

    Google Scholar 

  • Rost-Roszkowska, M. et al. Effects of short- and long-term exposure to cadmium on salivary glands and fat body of soil centipede Lithobius forficatus (Myriapoda, Chilopoda): Histology and ultrastructure. Micron 137, 102915 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Rost-Roszkowska, M. et al. Effects of cadmium on mitochondrial structure and function in different organs: Studies on the soil centipede Lithobius forficatus (Myriapoda, Chilopoda). Eur. Zool. J. 88, 632–664 (2021).

    CAS 
    Article 

    Google Scholar 

  • Włodarczyk, A., Student, S. & Rost-Roszkowska, M. Autophagy and apoptosis in starved and refed Neocaridina davidi (Crustacea, Malacostraca) midgut. Can. J. Zool. 97, 294–303 (2019).

    Article 

    Google Scholar 

  • Bradford, M. M. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Wieser, W. Conquering terra firma: The copper problem from the isopod’s point of view. Helgolander Wiss. Meeresunters. 15, 282–293 (1967).

    ADS 
    Article 

    Google Scholar 

  • Gräff, S., Berkus, M., Alberti, G. & Köhler, H. R. Metal accumulation strategies in saprophagous and phytophagous soil invertebrates: A quantitative comparison. Biometals 10, 45–53 (1997).

    Article 

    Google Scholar 

  • Siekierska, E. & Urbańska-Jasik, D. The effect of cadmium and selenium ions on the ovary structure in leech Herpobdella octooculata (L.). Folia Morphol. 57, 61 (1998).

    Google Scholar 

  • Siekierska, E. & Urbańska-Jasik, D. Cadmium effect on the ovarian structure in earthworm Dendrobaena veneta (Rosa). Environ. Pollut. 120, 289–297 (2002).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Osman, W., El-Samad, L. M., Mokhamer, E.L.-H., El-Touhamy, A. & Shonouda, M. Ecological, morphological, and histological studies on Blaps polycresta (Coleoptera: Tenebrionidae) as biomonitors of cadmium soil pollution. Environ. Sci. Pollut. Res. Int. 22, 14104–14115 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Siekierska, E. & Brzozowa, M. Cadmium effect on the seminal vesicles structure and spermatogenesis in the earthworm Dendrobaena veneta (Rosa). In 8th International Symposium on Earthworm Ecology. Book of abstracts, 231 (2006).

  • Siekierska, E. & Brzozowa, M. Changes in primary and secondary spermatocytes in seminal vesicles in the earthworm Dendrobaena veneta (Rosa) after 10 days of cadmium exposure. Acta Biol. Cracov. Bot. 50, 68 (2008).

    Google Scholar 

  • Brzozowa, M. Wpływ kadmu na przebieg spermiogenezy u dżdżownicy Dendrobaena veneta (Rosa). PhD Thesis, University of Silesia in Katowice Poland (2009).

  • Papathanassiou, E. Cadmium accumulation and ultrastructural alterations in oogenesis of the prawn Palaemon serratus (Pennant). Bull. Environ. Contam. Toxicol. 36, 192–198 (1986).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Au, D. W. T., Chiang, M. W. L. & Wu, R. Effect of cadmium and phenol on mortality and ultrastructure of sea urchin and mussel spermatozoa. Arcg. Environ. Contam. Toxicol. 38, 455–463 (2000).

    CAS 
    Article 

    Google Scholar 

  • Au, D. W. T., Lee, C. Y., Chan, K. L. & Wu, R. Reproductive impairment of sea urchins upon chronic exposure to cadmium. Part I: Effects on gamete quality. Environ. Pollut. 111, 1–9 (2001).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Au, D. W. T., Reunov, A. A. & Wu, R. Reproductive impairment of sea urchins upon chronic exposure to cadmium. Part II: Effects on sperm development. Environ. Pollut. 111, 11–20 (2001).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Eckelbarger, K. J. Diversity of metazoan ovaries and vitellogenic mechanisms – implications for life history theory. Proc. Biol. Soc. Wash. 107, 193–218 (1994).

    Google Scholar 

  • Suzuki, K. T., Yamamura, M. & Mori, T. Cadmium-binding proteins induced in earthworm. Arch. Environ. Contam. Toxicol. 9, 415–424 (1980).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Maroni, G., Wise, J., Young, J. E. & Otto, E. Metallothionein gene duplications and metal tolerance in natural populations of Drosophila melanogaster. Genetics 117, 739–744 (1987).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Luo, M., Finet, C., Cong, H., Wei, H. & Chung, H. The evolution of insect metallothioneins. Proc. R. Soc. B 287, 20202189 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Turbeck, B. O. A study of the concentrically laminated concretions, ‘spherites’, in the regenerative cells of the midgut of Lepidopterous larvae. Tissue Cell. 6, 627–640 (1974).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Cruz-Landim, C. Localization of calcium and acid phosphatase in the Malpighian tubules of nurse workers of Melipona quadrifasciata anthidioides Lep. (Hymenoptera, Apidae, Meliponini). Biosci. J. 16, 87–99 (2000).

    Google Scholar 

  • Lipovšek, S., Letofsky-Papst, I., Hofer, F., Pabst, M. A. & Devetak, D. Application of analytical electron microscopic methods to investigate the function of spherites in the midgut of the larval antlion Euroleon nostras (Neuroptera: Myrmeleontidae). Microsc. Res. Tech. 75, 397–407 (2012).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Pinheiro, D. O., Conte, H. & Gregório, E. A. Spherites in the midgut epithelial cells of the sugarcane borer parasitized by Cotesia flavipes. Biocell 32, 61–67 (2008).

    Article 

    Google Scholar 

  • Rost-Roszkowska, M. M., Kszuk-Jendrysik, M., Marchewka, A. & Poprawa, I. Fine structure of the midgut epithelium in the millipede Telodeinopus aoutii (Myriapoda, Diplopoda) with special emphasis on epithelial regeneration. Protoplasma 255, 43–55 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Lipovšek, S. et al. Ultrastructure of spherites in the midgut diverticula and Malpighian tubules of the harvestman Amilenus aurantiacus during the winter diapause. Histochem. Cell Biol. 157, 107–118 (2022).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Kramarz, P. Dynamics of accumulation and decontamination of cadmium and zinc in carnivorous invertebrates. 2. The centipede Lithobius mutabilis Koch. Bull. Environ. Contam. Toxicol. 63, 538–545 (1999).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Rost-Roszkowska, M. M. et al. Structure of the midgut epithelium in four diplopod species: Histology, histochemistry and ultrastructure. Arthropod Syst. Phylogeny 79, 295–308 (2021).

    Article 

    Google Scholar 

  • Köhler, H.-R. Localization of metals in cells of saprophagous soil arthropods (Isopoda, Diplopoda, Collembola). Microsc. Res. Tech. 56, 393–401 (2002).

    ADS 
    PubMed 
    Article 

    Google Scholar 

  • Cervera, A., Maymó, A. C., Martínez-Pardo, R. & Garcerá, M. D. Vitellogenesis inhibition in Oncopeltus fasciatus females (Heteroptera: Lygaeidae) exposed to cadmium. J. Insect Physiol. 51, 895–911 (2005).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Cervera, A., Maymó, A. C., Martínez-Pardo, R. & Garcerá, M. D. Vitellogenin polypeptide levels in one susceptible and one cadmium-resistant strain of Oncopeltus fasciatus (Heteroptera: Lygaeidae), and its role in cadmium resistance. J. Insect Physiol. 52, 158–168 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Sehgal, A., Osgood, C. & Zimmering, S. Aneuploid in Drosophila. III: Aneuploidogens inhibit in vitro assembly of taxol-purified Drosophila microtubules. Environ. Mol. Mutagen. 16, 217–224 (1990).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Li, W., Zhao, Y. & Cou, I. N. Alterations in cytoskeletal protein sulfhydryls and cellular glutathione in cultured cells exposed to cadmium and nickel ions. Toxicology 77, 65–79 (1993).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • dos Santos, D. C., Gregorio, E. A. & Moreli Silva de Moraes, R. L. Programmed cell death during early oogenesis in the Diatraea saccharalis germarium. Acta Microsc. 16, 311–312 (2007).

    Google Scholar 

  • Hoeppner, D. J., Hengartner, M. O. & Schnabel, R. Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans. Nature 412, 202–206 (2001).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Hikim, A. P. S. et al. Key apoptotic pathways for heat-induced programmed germ cell death in the testis. Endocrinology 144, 3167–3175 (2003).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Russell, L. D., Chiarini-Garcia, H., Korsmeyer, S. J. & Knudson, C. M. Bax-dependent spermatogonia apoptosis is required for testicular development and spermatogenesis. Biol. Reprod. 66, 950–958 (2002).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Shaha, C., Tripathi, R. & Mishra, D. P. Male germ cell apoptosis: Regulation and biology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 1501–1515 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Devine, P. J., Payne, C. M., McCuskey, M. K. & Hoyer, P. B. Ultrastructural evaluation of oocytes during atresia in rat ovarian follicles. Biol. Reprod. 63, 1245–1252 (2000).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Hussein, M. R. Apoptosis in the ovary: Molecular mechanisms. Hum. Reprod. Update 11, 162–177 (2005).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Miller, M. A., Technau, U., Smith, K. M. & Steele, R. E. Oocyte development in Hydra involves selection from competent precursor cells. Dev. Biol. 224, 326–338 (2000).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Matova, N. & Cooley, L. Comparative aspects of animal oogenesis. Dev. Biol. 231, 291–320 (2001).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Technau, U., Miller, M. A., Bridge, D. & Steele, R. E. Arrested apoptosis of nurse cells during Hydra oogenesis and embryogenesis. Dev. Biol. 260, 191–206 (2003).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Mpakou, V. E., Nezis, I. P., Stravopodis, D. J., Margaritis, L. H. & Papassideri, I. S. Programmed cell death of the ovarian nurse cells during oogenesis of the silkmoth Bombyx mori. Dev. Growth Differ. 48, 419–428 (2006).

    PubMed 
    Article 

    Google Scholar 

  • Mpakou, V. E. et al. Different modes of programmed cel death during oogenesis of the silkmoth Bombyx mori. Autophagy 4, 97–100 (2008).

    PubMed 
    Article 

    Google Scholar 

  • Mpakou, V. E. et al. Programmed cell death of the ovarian nurse cells during oogenesis of the ladybird beetle Adalia bipunctata (Coleoptera: Coccinellidae). Dev. Growth Differ. 53, 804–815 (2011).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Poprawa, I., Hyra, M., Kszuk-Jendrysik, M. & Rost-Roszkowska, M. M. Ultrastructural changes and programmed cell death of trophocytes in the gonad of Isohypsibius granulifer granulifer Thulin, 1928 (Tardigrada, Eutardigrada, Isohypsibiidae). Micron 70, 26–33 (2015).

    PubMed 
    Article 

    Google Scholar 

  • Janelt, K., Jezierska, M. & Poprawa, I. The female reproductive system and oogenesis in Thulinius ruffoi (Tardigrada, Eutardigrada, Isohypsibiidae). Arthropod. Struct. Dev. 50, 53–63 (2019).

    PubMed 
    Article 

    Google Scholar 

  • Mooyottu, S., Anees, C. & Cherian, S. Ovarian stem cells and neo-oogenesis: A breakthrough in reproductive biology research. Vet. World 4, 89–91 (2011).

    Google Scholar 

  • Tiwari, M. et al. Apoptosis in mammalian oocytes: A review. Apoptosis 20, 1019–1025 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Xiu, Y.-R. & Yang, W.-X. Roles of three Es-Caspases during spermatogenesis and cadmium-induced apoptosis in Eriocheir sinensis. Aging 10, 1146–1165 (2018).

    Article 

    Google Scholar 

  • Redza-Dutordoir, M. & Averill-Bates, D. A. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim. Biophys. Acta 1863, 2977–2992 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Sonakowska, L. et al. Cell death in the epithelia of the intestine and hepatopancreas in Neocaridina heteropoda (Crustacea, Malacostraca). PLoS ONE 11, e0147582 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Włodarczyk, A. et al. The effect of starvation and re-feeding on mitochondrial potential in the midgut of Neocaridina davidi (Crustacea, Malacostraca). PLoS ONE 12, e0173563 (2017).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Zorova, L. D. et al. Mitochondrial membrane potential. Anal. Biochem. 552, 50–59 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Ossola, J. O. & Tomaro, M. L. Heme oxygenase induction by cadmium chloride: Evidence for oxidative stress involvement. Toxicology 104, 141–147 (1995).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Levine, B. & Klionsky, D. J. Development by self-digestion: Molecular mechanisms and biological functions of autophagy. Dev. Cell. 6, 463–477 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Kourtis, N. & Tavernarakis, N. Autophagy and cell death in model organisms. Cell Death Differ. 16, 21–30 (2009).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Kliosnky, D. et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12, 1–222 (2016).

    Article 

    Google Scholar 

  • Kliosnky, D. et al. Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition). Autophagy 17, 1–382 (2021).

    Article 

    Google Scholar 

  • Velentzas, A. D., Nezis, I. P., Stravopodis, D. J., Papassideri, I. S. & Margaritis, L. H. Apoptosis and autophagy function cooperatively for the efficacious execution of programmed nurse cell death during Drosophila virilis oogenesis. Autophagy 3, 130–132 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Lipovšek, S. et al. Changes in the midgut cells in the European cave spider, Meta menardi, during starvation in spring and autumn. Histochem. Cell Biol. 149, 245–260 (2018).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Rost-Roszkowska, M. M. et al. Autophagy and apoptosis in the midgut epithelium of millipedes. Microsc. Microanal. 25, 1004–1016 (2019).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Nezis, I. P. et al. Autophagy as a trigger for cell death: Autophagic degradation of inhibitor of apoptosis dBruce controls DNA fragmentation during late oogenesis in Drosophila. Autophagy 6, 1214–1215 (2010).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Rost-Roszkowska, M. M., Janelt, K. & Poprawa, I. The role of autophagy in the midgut epithelium of Parachela (Tardigrada). Zoomorphology 137, 501–509 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Leist, M., Single, B., Castoldi, A. F., Kühnle, S. & Nicotera, P. Intracellular adenosine triphosphate (ATP) concentration: A switch in the decision between apoptosis and necrosis. J. Exp. Med. 185, 1481–1486 (1997).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Nikoletopoulou, V., Markaki, M., Palikaras, K. & Tavernarakis, N. Crosstalk between apoptosis, necrosis and autophagy. Biochim. Biophys. Acta. 1833, 3448–3459 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar 


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