56
Views
4
CrossRef citations to date
0
Altmetric
Review Article

Mitochondria and lysosomes play a key role in HepG2 cell apoptosis induced by microcystin-LR

&
Pages 63-72 | Received 02 Jul 2016, Accepted 25 Aug 2016, Published online: 11 Oct 2016

References

  • Alsharafi WA, Bi FF, Hu YQ, et al. (2014). Effect of khat on apoptosis and related gene smac/diablo expression in the cerebral cortex of rats following transient focal ischemia. Environ Toxicol Pharmacol 39:424–32
  • Amar SK, Goyal S, Dubey D, et al. (2015). Benzophenone 1 induced photogenotoxicity and apoptosis via release of cytochrome c and Smac/DIABLO at environmental UV radiation. Toxicol Lett 239:182–93
  • Atencio L, Moreno I, Prieto AI, et al. (2008). Acute effects of microcystins MC-LR and MC-RR on acid and alkaline phosphatase activities and pathological changes in intraperitoneally exposed tilapia fish (Oreochromis sp.). Toxicol Pathol 36:449–58
  • Boaru DA, Dragoş N, Schirmer K. (2006). Microcystin-LR induced cellular effects in mammalian and fish primary hepatocyte cultures and cell lines: a comparative study. Toxicology 218:134–48
  • Brunk UT, Svensson I. (1999). Oxidative stress, growth factor starvation and FAS activation may all cause apoptosis through lysosomal leak. Redox Rep 4:3–11
  • Carmichael WW, Azevedo SM, An JS, et al. (2001). Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environ Health Perspect 109:663–8
  • Chen L, Chen J, Zhang X, Xie P. (2016). A review of reproductive toxicity of microcystins. J Hazard Mater 301:381–99
  • Cirman T, Oresic K, Mazovec GD, et al. (2004). Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papain-like lysosomal cathepsins. J Biol Chem 279:3578–87
  • Costantini S, Bernardo GD, Cammarota M, et al. (2013). Gene expression signature of human HepG2 cell line. Gene 518:335–45
  • Dias E, Andrade M, Alverca E, et al. (2009). Comparative study of the cytotoxic effect of microcystin-LR and purified extracts from M. aeruginosa on a kidney cell line. Toxicon 53:457–95
  • Dias E, Louro H, Pinto M, et al. (2014). Genotoxicity of microcystin-LR in vitro and in vivo experimental models. BioMed Res Int 2014:949521. doi: 10.1155/2014/949521
  • Ding WX, Shen HM, Ong CN. (2000). Critical role of reactive oxygen species and mitochondrial permeability transition in microcystin-induced rapid apoptosis in rat hepatocytes. Hepatology 32:547–55
  • Ding WX, Shen HM, Ong CN. (2001). Critical role of reactive oxygen species formation in microcystin-induced cytoskeleton disruption in primary cultured hepatocytes. J Toxicol Env Heal a 64:507–19
  • Ding WX, Ong CN. (2003). Role of oxidative stress and mitochondrial changes in cyanobacteria-induced apoptosis and hepatotoxicity. FEMS Microbiol Lett 220:1–7
  • Feng G, Abdalla M, Li Y, Bai Y. (2011). NF-κB mediates the induction of FAS receptor and FAS ligand by microcystin-LR in HepG2 cells. Mol Cell Biochem 352:209–19
  • French LE, Hahne M, Viard I, et al. (1996). FAS and FAS ligand in embryos and adult mice: ligand expression in several immune-privileged tissues and coexpression in adult tissues characterized by apoptotic cell turnover. J Cell Biol 133:335–43
  • Fu W, Chen J, Wang X, Xu L. (2005). Altered expression of p53, Bcl-2 and Bax induced by microcystin-LR in vivo and in vitro. Toxicon 46:171–7
  • Funari E, Testai E. (2008). Human health risk assessment related to cyanotoxins exposure. Crit Rev Toxicol 38:97–125
  • Gan N, Mi L, Sun X, et al. (2010). Sulforaphane protects microcystin-LR-induced toxicity through activation of the Nrf2-mediated defensive response. Toxicol Appl Pharm 247:129–37
  • Harada K-I, Tsuji K, Watanabe MF, Kondo F. (1996). Stability of microcystins from cyanobacteria: III. Effect of pH and temperature. Phycologia 35:83–8
  • Harada K-I, Tsuji K. (1998). Persistence and decomposition of hepatotoxic microcystins produced by cyanobacteria in natural environment. Toxin Rev 17:385–403
  • Hu Y, Chen J, Fan H, et al. (2016). A review of neurotoxicity of microcystins. Environ Sci Pollut Res Int 23:7211–19
  • Ji Y, Lu G, Chen G, et al. (2011). Microcystin-LR induces apoptosis via NF-κB/iNOS pathway in INS-1 cells. Int J Mol Sci 12:4722–34
  • Kawasaki S, Moriguchi R, Sekiya K, et al. (1994). The cell envelope structure of the lipopolysaccharide-lacking gram-negative bacterium Sphingomonas paucimobilis. J Bacteriol 176:284–90
  • Kim R, Emi M, Tanabe K. (2006). Role of mitochondria as the gardens of cell death. Cancer Chemother Pharmacol 57:545–53
  • Kurtz T, Terman A, Gustafsson B, Brunk UT. (2008). Lysosomes and oxidative stress in aging and apoptosis. Biochim Biophys Acta 1780:1291–303
  • Kullak-Ublick GA, Beuers U, Paumgartner G. (1996). Molecular and functional characterization of bile acid transport in human hepatoblastoma HepG2 cells. Hepatology 23:1053–60
  • Li G, Cai F, Yan W, et al. (2012). A proteomic analysis of MCLR-induced neurotoxicity: implications for Alzheimer's disease. Toxicol Sci 127:485–95
  • Li H, Zhu H, Xu CJ, Yuan J. (1998). Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491–501
  • Li L, Xie P, Chen J. (2007). Biochemical and ultrastructural changes of the liver and kidney of the phytoplanktivorous silver carp feeding naturally on toxic Microcystis blooms in Taihu Lake, China. Toxicon 49:1042–53
  • Li X, Liu Y, Song L, Liu J. (2003). Responses of antioxidant systems in the hepatocytes of common carp (Cyprinus carpio L.) to the toxicity of microcystin-LR. Toxicon 42:85–9
  • Li X, Ma J, Qian F, Li Y. (2013). Transcription alterations of microRNAs, cytochrome P4501A1 and 3A65, and AhR and PXR in the liver of zebrafish exposed to crude microcystins. Toxicon 73:17–22
  • Li W, Yuan XM, Nordgren G, et al. (2000). Induction of cell death by the lysosomotropic detergent MSDH. FEBS Lett 470:35–9
  • Liu J, Wang H, Wang B, et al. (2016). Microcystin-LR promotes proliferation by activating Akt/S6K1 pathway and disordering apoptosis and cell cycle associated proteins phosphorylation in HL7702 cells. Toxicol Lett 240:214–25
  • Livak KJ, Schmittgen TD. (2001). Analysis of relative gene expression data using real-time quantitative PCR and 2 (-Delta Delta Ct) method. Methods 25:402–8
  • Lone Y, Bhide M, Koiri RK. (2016). Microcystin-LR induced immunotoxicity in mammals. J Toxicol 2016:1–5
  • Luo X, Budihardjo I, Zou H, et al. (1998). Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94:481–90
  • Ma J, Bu Y, Li X. (2015). Immunological and histopathological responses of the kidney of common carp (Cyprinus carpio L.) sublethally exposed to glyphosate. Environ Toxicol Pharmacol 39:1–8
  • Maher S, Toomey D, Condron C, Bouchier-Hayes D. (2002). Activation-induced cell death: the controversial role of Fas and Fas ligand in immune privilege and tumour counterattack. Immunol Cell Biol 80:131–7
  • Menezes C, Valério E, Dias E. (2013a). The kidney Vero-E6 cell line: a suitable model to study the toxicity of microcystins. In: Gowder S, ed. New insights into toxicity and drug testing. InTech. doi: 10.5772/54463
  • Menezes C, Valério E, Dias E, et al. (2013b). Involvement of endoplasmic reticulum and autophagy in microcystin-LR toxicity in Vero-E6 and HepG2 cell lines. Toxicol in Vitro 27:138–48
  • Meriluoto JA, Spoof LE. (2008) Cyanotoxins: sampling, sample processing and toxin uptake. In: Kenneth Hudnell H, ed. Cyanobacterial harmful algal blooms: state of the science and research needs. New York: Springer Press, 483–499
  • Mersch-Sundermann V, Knasmuller S, Wu XJ, et al. (2004). Use of a human-derived liver cell line for the detection of cytoprotective, antigenotoxic and cogenotoxic agents. Toxicology 198:329–40
  • Nils W, Frazier AE, Nikolaus P. (2004). The protein import machinery of mitochondria. J Biol Chem 279:14473–6
  • Nong Q, Komatsu M, Izumo K, et al. (2007). Involvement of reactive oxygen species in Microcystin-LR-induced cytogenotoxicity. Free Radic Res 41:1326–37
  • O'Neil JM, Davis TW, Burford MA, Gobler CJ. (2012). The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–34
  • Runnegar MT, Kong S, Berndt N. (1993). Protein phosphatase inhibition and in vivo hepatotoxicity of microcystins. Am J Physiol 265:224–30
  • Saftig P. (2005). Lysosomes Landes Bioscience/Eurekah.com. Georgetown, TX; New York: Springer Science + Business Media
  • Shiozaki EN, Shi Y. (2004). Caspases, IAPs and Smac/DIABLO: mechanisms from structural biology. Trends Biochem Sci 29:486–94
  • Tsutsui H, Matsui K, Kawada N, et al. (1997). IL-18 accounts for both TNF-alpha- and FAS ligand-mediated hepatotoxic pathways in endotoxin-induced liver injury in mice. J Immunol 159:3961–7
  • van Apeldoorn ME, van Egmond HP, Speijers GJ, Bakker GJ. (2007). Toxins of cyanobacteria. Mol Nutr Food Res 51:7–60
  • Wang C, Gu S, Yin X, et al. (2016). The toxic effects of microcystin-lr on mouse lungs and alveolar type II epithelial cells. Toxicon 115:81–8
  • WHO. (1998). Guidelines for drinking-water quality. Addendum to Volume 2. Health Criteria and Other Supporting Information. Geneva, Switzerland: Word Health Organization
  • Wood R. (2016). Acute animal and human poisonings from cyanotoxin exposure: a review of the literature. Environ Int 91:276–82
  • Xu H, Ren D. (2015). Lysosomal physiology. Annu Rev Physiol 77:57–80
  • Yang E, Zha J, Jockel J, et al. (1995). Bad, a heterodimeric partner for Bcl-xL and Bcl-2, displaces Bax and promotes cell death. Cell 80:285–91
  • Zha J, Harada H, Osipov K, et al. (1997). BH3 domain of BAD is required for heterodimerization with BCL-XL and pro-apoptotic activity. J Biol Chem 272:24101–4
  • Zhang X, Xie P, Zhang X, et al. (2013). Toxic effects of microcystin-LR on the HepG2 cell line under hypoxic and normoxic conditions. J Appl Toxicol 33:1180–6
  • Zhang F, Lee J, Liang S, Shum CK. (2015). Cyanobacteria blooms and nonalcoholic liver disease: evidence from a county level ecological study in the United States. Environ Health 14:1–11
  • Zhou M, Tu WW, Xu J. (2015). Mechanisms of microcystin-LR-induced cytoskeletal disruption in animal cells. Toxicon 101:92–100

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.