publication . Article . 2017

Bcl-xL Affects Group A Streptococcus-Induced Autophagy Directly, by Inhibiting Fusion between Autophagosomes and Lysosomes, and Indirectly, by Inhibiting Bacterial Internalization via Interaction with Beclin 1-UVRAG

Nakajima, Shintaro; Aikawa, Chihiro; Nozawa, Takashi; Minowa-Nozawa, Atsuko; Toh, Hirotaka; Nakagawa, Ichiro;
Open Access English
  • Published: 13 Jan 2017 Journal: PLoS ONE, volume 12, issue 1 (issn: 1932-6203, eissn: 1932-6203, Copyright policy)
  • Publisher: Public Library of Science
Abstract
Anti-apoptotic Bcl-2 and Bcl-xL are proposed to regulate starvation-induced autophagy by directly interacting with Beclin 1. Beclin 1 is also thought to be involved in multiple vesicle trafficking pathways such as endocytosis by binding to Atg14L and UVRAG. However, how the interaction of Bcl-2 family proteins and Beclin 1 regulates anti-bacterial autophagy (xenophagy) is still unclear. In this study, we analyzed these interactions using Group A Streptococcus (GAS; Streptococcus pyogenes) infection as a model. GAS is internalized into epithelial cells through endocytosis, while the intracellular fate of GAS is degradation by autophagy. Here, we found that Bcl-xL...
Subjects
free text keywords: Cultured tumor cells, Precipitation Techniques, Research Article, Cell lines, Staining, Nuclear staining, Cell Processes, DAPI staining, Genetics, Immunoprecipitation, Light Microscopy, Autophagic Cell Death, Biology and life sciences, Non-coding RNA, Cell Death, RNA, Research and Analysis Methods, Medicine, Immunostaining, Nucleic acids, HeLa cells, Specimen Preparation and Treatment, Small interfering RNAs, Q, R, Cell Biology, Confocal Microscopy, Gene regulation, Science, Biological cultures, Biochemistry, Cell Staining, Cell cultures, Microscopy, Gene expression
52 references, page 1 of 4

1 Cunningham MW. Pathogenesis of group A streptococcal infections. Clinical microbiology reviews. 2000;13:470–511. 10885988 [OpenAIRE] [PubMed]

2 Aikawa C, Nozawa T, Maruyama F, Tsumoto K, Hamada S, Nakagawa I. Reactive oxygen species induced by Streptococcus pyogenes invasion trigger apoptotic cell death in infected epithelial cells. Cellular Microbiology. 2010;12:814–30. doi: 10.1111/j.1462-5822.2010.01435.x 20070306 [PubMed]

3 Nakagawa I, Nakata M, Kawabata S, Hamada S. Cytochrome c-mediated caspase-9 activation triggers apoptosis in Streptococcus pyogenes-infected epithelial cells. Cellular Microbiology. 2001;3:395–405. 11422082 [PubMed]

4 O'Seaghdha M, Wessels MR. Streptolysin O and its Co-Toxin NAD-glycohydrolase Protect Group A Streptococcus from Xenophagic Killing. PLoS Pathogens. 2013;9. [OpenAIRE]

5 Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, Kamimoto T, et al Autophagy defends cells against invading group A Streptococcus. Science (New York, NY). 2004;306(5698):1037–40. Epub 2004/11/06.

6 Cole JN, Barnett TC, Nizet V, Walker MJ. Molecular insight into invasive group A streptococcal disease. Nature reviews Microbiology. 2011;9(10):724–36. Epub 2011/09/17. doi: 10.1038/nrmicro2648 21921933 [PubMed]

7 Barnett TC, Liebl D, Seymour LM, Gillen CM, Lim JY, Larock CN, et al The globally di sseminated M1T1 clone of group a streptococcus evades autophagy for intracellular replication. Cell Host and Microbe. 2013;14:675–82. doi: 10.1016/j.chom.2013.11.003 24331465 [OpenAIRE] [PubMed]

8 Gross A, McDonnell JM, Korsmeyer SJ. BCL-2 family members and the mitochondria in apoptosis. Genes and Development. 1999;13:1899–911. 10444588 [PubMed]

9 Vento MT, Zazzu V, Loffreda A, Cross JR, Downward J, Stoppelli MP, et al Praf2 is a novel Bcl-xL/Bcl-2 interacting protein with the ability to modulate survival of cancer cells. PLoS ONE. 2010;5.

10 Maiuri MC, Le Toumelin G, Criollo A, Rain J-C, Gautier F, Juin P, et al Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. The EMBO journal. 2007;26:2527–39. doi: 10.1038/sj.emboj.7601689 17446862 [OpenAIRE] [PubMed]

11 Pattingre S, Tassa A, Qu X, Garuti R, Xiao HL, Mizushima N, et al Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005;122:927–39. doi: 10.1016/j.cell.2005.07.002 16179260 [OpenAIRE] [PubMed]

12 Birmingham CL, Brumell JH. Autophagy recognizes intracellular Salmonella enterica serovar typhimurium in damaged vacuoles. Autophagy. 2006;2:156–8. 16874057 [PubMed]

13 Birmingham CL, Canadien V, Gouin E, Troy EB, Yoshimori T, Cossart P, et al Listeria monocytogenes evades killing by autophagy during colonization of host cells. Autophagy. 2007;3:442–51. 17568179 [PubMed]

14 Yoshikawa Y, Ogawa M, Hain T, Chakraborty T, Sasakawa C. Listeria monocytogenes ActA is a key player in evading autophagic recognition. Autophagy. 2009;5:1220–1. 19855178 [PubMed]

15 Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C. Escape of intracellular Shigella from autophagy. Science (New York, NY). 2005;307(5710):727–31. Epub 2004/12/04.

52 references, page 1 of 4
Abstract
Anti-apoptotic Bcl-2 and Bcl-xL are proposed to regulate starvation-induced autophagy by directly interacting with Beclin 1. Beclin 1 is also thought to be involved in multiple vesicle trafficking pathways such as endocytosis by binding to Atg14L and UVRAG. However, how the interaction of Bcl-2 family proteins and Beclin 1 regulates anti-bacterial autophagy (xenophagy) is still unclear. In this study, we analyzed these interactions using Group A Streptococcus (GAS; Streptococcus pyogenes) infection as a model. GAS is internalized into epithelial cells through endocytosis, while the intracellular fate of GAS is degradation by autophagy. Here, we found that Bcl-xL...
Subjects
free text keywords: Cultured tumor cells, Precipitation Techniques, Research Article, Cell lines, Staining, Nuclear staining, Cell Processes, DAPI staining, Genetics, Immunoprecipitation, Light Microscopy, Autophagic Cell Death, Biology and life sciences, Non-coding RNA, Cell Death, RNA, Research and Analysis Methods, Medicine, Immunostaining, Nucleic acids, HeLa cells, Specimen Preparation and Treatment, Small interfering RNAs, Q, R, Cell Biology, Confocal Microscopy, Gene regulation, Science, Biological cultures, Biochemistry, Cell Staining, Cell cultures, Microscopy, Gene expression
52 references, page 1 of 4

1 Cunningham MW. Pathogenesis of group A streptococcal infections. Clinical microbiology reviews. 2000;13:470–511. 10885988 [OpenAIRE] [PubMed]

2 Aikawa C, Nozawa T, Maruyama F, Tsumoto K, Hamada S, Nakagawa I. Reactive oxygen species induced by Streptococcus pyogenes invasion trigger apoptotic cell death in infected epithelial cells. Cellular Microbiology. 2010;12:814–30. doi: 10.1111/j.1462-5822.2010.01435.x 20070306 [PubMed]

3 Nakagawa I, Nakata M, Kawabata S, Hamada S. Cytochrome c-mediated caspase-9 activation triggers apoptosis in Streptococcus pyogenes-infected epithelial cells. Cellular Microbiology. 2001;3:395–405. 11422082 [PubMed]

4 O'Seaghdha M, Wessels MR. Streptolysin O and its Co-Toxin NAD-glycohydrolase Protect Group A Streptococcus from Xenophagic Killing. PLoS Pathogens. 2013;9. [OpenAIRE]

5 Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, Kamimoto T, et al Autophagy defends cells against invading group A Streptococcus. Science (New York, NY). 2004;306(5698):1037–40. Epub 2004/11/06.

6 Cole JN, Barnett TC, Nizet V, Walker MJ. Molecular insight into invasive group A streptococcal disease. Nature reviews Microbiology. 2011;9(10):724–36. Epub 2011/09/17. doi: 10.1038/nrmicro2648 21921933 [PubMed]

7 Barnett TC, Liebl D, Seymour LM, Gillen CM, Lim JY, Larock CN, et al The globally di sseminated M1T1 clone of group a streptococcus evades autophagy for intracellular replication. Cell Host and Microbe. 2013;14:675–82. doi: 10.1016/j.chom.2013.11.003 24331465 [OpenAIRE] [PubMed]

8 Gross A, McDonnell JM, Korsmeyer SJ. BCL-2 family members and the mitochondria in apoptosis. Genes and Development. 1999;13:1899–911. 10444588 [PubMed]

9 Vento MT, Zazzu V, Loffreda A, Cross JR, Downward J, Stoppelli MP, et al Praf2 is a novel Bcl-xL/Bcl-2 interacting protein with the ability to modulate survival of cancer cells. PLoS ONE. 2010;5.

10 Maiuri MC, Le Toumelin G, Criollo A, Rain J-C, Gautier F, Juin P, et al Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. The EMBO journal. 2007;26:2527–39. doi: 10.1038/sj.emboj.7601689 17446862 [OpenAIRE] [PubMed]

11 Pattingre S, Tassa A, Qu X, Garuti R, Xiao HL, Mizushima N, et al Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005;122:927–39. doi: 10.1016/j.cell.2005.07.002 16179260 [OpenAIRE] [PubMed]

12 Birmingham CL, Brumell JH. Autophagy recognizes intracellular Salmonella enterica serovar typhimurium in damaged vacuoles. Autophagy. 2006;2:156–8. 16874057 [PubMed]

13 Birmingham CL, Canadien V, Gouin E, Troy EB, Yoshimori T, Cossart P, et al Listeria monocytogenes evades killing by autophagy during colonization of host cells. Autophagy. 2007;3:442–51. 17568179 [PubMed]

14 Yoshikawa Y, Ogawa M, Hain T, Chakraborty T, Sasakawa C. Listeria monocytogenes ActA is a key player in evading autophagic recognition. Autophagy. 2009;5:1220–1. 19855178 [PubMed]

15 Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C. Escape of intracellular Shigella from autophagy. Science (New York, NY). 2005;307(5710):727–31. Epub 2004/12/04.

52 references, page 1 of 4
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publication . Article . 2017

Bcl-xL Affects Group A Streptococcus-Induced Autophagy Directly, by Inhibiting Fusion between Autophagosomes and Lysosomes, and Indirectly, by Inhibiting Bacterial Internalization via Interaction with Beclin 1-UVRAG

Nakajima, Shintaro; Aikawa, Chihiro; Nozawa, Takashi; Minowa-Nozawa, Atsuko; Toh, Hirotaka; Nakagawa, Ichiro;