Modulation of host autophagy during bacterial infection: Sabotaging host munitions for pathogen nutrition

Frontiers in Immunology

Volumn 7, Issue MAR, 2016, Pages

  Escoll, Pedro ^a,b   Rolando, Monica ^a,b   Buchrieser, Carmen ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

Author keywords

Autophagosome; Autophagy modulators; Bacterial nutrition; Intracellular bacteria; Xenophagy

Indexed keywords

AUTOPHAGY PROTEIN 5; AZITHROMYCIN; BACTERIUM LIPOPOLYSACCHARIDE; BECLIN 1; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CHLOROQUINE; CYCLIC AMP; DOXYCYCLINE; HYDROXYCHLOROQUINE; ISONIAZID; METFORMIN; PHOSPHATIDYLETHANOLAMINE; PYRAZINAMIDE; RAPAMYCIN; RILMENIDINE; TOLL LIKE RECEPTOR 4;

ANAPLASMA PHAGOCYTOPHILUM; AUTOLYSOSOME; AUTOPHAGY; BACTERIAL INFECTION; CELL VACUOLE; DRUG APPROVAL; GOLGI COMPLEX; LISTERIA MONOCYTOGENES; LYSOSOME; MICROBIAL GROWTH; MICROBIOLOGICAL PARAMETERS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NOTE; NUTRITION; PHAGOCYTOSIS; Q FEVER; SABOTAGING HOST MUNITION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; STREPTOCOCCUS GROUP A; XENOPHAGY;

EID: 84964661163     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00081     Document Type: Note

References (45)

1. Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol (2013) 13:722-37. doi: 10.1038/nri3532
2. Huang J, Brumell JH. Bacteria-autophagy interplay: a battle for survival. Nat Rev Microbiol (2014) 12:101-14. doi:10.1038/nrmicro3160
3. Rubinsztein DC, Codogno P, Levine B. Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov (2012) 11:709-30. doi:10.1038/nrd3802
4. Birmingham CL, Smith AC, Bakowski MA, Yoshimori T, Brumell JH. Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J Biol Chem (2006) 281:11374-83. doi:10.1074/jbc.M509157200
5. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell (2004) 119:753-66. doi:10.1016/j.cell.2004.11.038
6. Zhao Z, Fux B, Goodwin M, Dunay IR, Strong D, Miller BC, et al. Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe (2008) 4:458-69. doi:10.1016/j.chom.2008.10.003
7. Py BF, Lipinski MM, Yuan J. Autophagy limits Listeria monocytogenes intracellular growth in the early phase of primary infection. Autophagy (2007) 3:117-25. doi:10.4161/auto.3618
8. Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, Kamimoto T, et al. Autophagy defends cells against invading Group A Streptococcus. Science (2004) 306:1037-40. doi:10.1126/science.1103966
9. Xu Y, Jagannath C, Liu X-D, Sharafkhaneh A, Kolodziejska KE, Eissa NT. Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity (2007) 27:135-44. doi:10.1016/j.immuni.2007.05.022
10. Travassos LH, Carneiro LAM, Ramjeet M, Hussey S, Kim YG, Magalhães JG, et al. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat Immunol (2010) 11:55-62. doi:10.1038/ni.1823
11. Sanjuan MA, Dillon CP, Tait SWG, Moshiach S, Dorsey F, Connell S, et al. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature (2007) 450:1253-7. doi:10.1038/nature06421
12. Kageyama S, Omori H, Saitoh T, Sone T, Guan J-L, Akira S, et al. The LC3 recruitment mechanism is separate from Atg9L1-dependent membrane formation in the autophagic response against Salmonella. Mol Biol Cell (2011) 22:2290-300. doi:10.1091/mbc.E10-11-0893
13. Itakura E, Kishi-Itakura C, Mizushima N. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell (2012) 151:1256-69. doi:10.1016/j.cell.2012.11.001
14. Shin DM, Jeon BY, Lee HM, Jin HS, Yuk JM, Song CH, et al. Mycobacterium tuberculosis eis regulates autophagy, inflammation, and cell death through redox-dependent signaling. PLoS Pathog (2010) 6:e1001230. doi:10.1371/journal.ppat.1001230
15. Tattoli I, Sorbara MT, Vuckovic D, Ling A, Soares F, Carneiro LAM, et al. Amino acid starvation induced by invasive bacterial pathogens triggers an innate host defense program. Cell Host Microbe (2012) 11:563-75. doi:10.1016/j.chom.2012.04.012
16. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C. Escape of intracellular Shigella from autophagy. Science (2005) 307:727-31. doi:10.1126/science.1106036
17. Mostowy S, Cossart P. Bacterial autophagy: restriction or promotion of bacterial replication? Trends Cell Biol (2012) 22:283-91. doi:10.1016/j.tcb.2012.03.006
18. Steele S, Brunton J, Kawula T. The role of autophagy in intracellular pathogen nutrient acquisition. Front Cell Infect Microbiol (2015) 5:51. doi:10.3389/fcimb.2015.00051
19. Niu H, Xiong Q, Yamamoto A, Hayashi-Nishino M, Rikihisa Y. Autophagosomes induced by a bacterial Beclin 1 binding protein facilitate obligatory intracellular infection. Proc Natl Acad Sci U S A (2012) 109:20800-7. doi:10.1073/pnas.1218674109
20. Niu H, Yamaguchi M, Rikihisa Y. Subversion of cellular autophagy by Anaplasma phagocytophilum. Cell Microbiol (2008) 10:593-605. doi:10.1111/j.1462-5822.2007.01068.x
21. Moreau K, Lacas-Gervais S, Fujita N, Sebbane F, Yoshimori T, Simonet M, et al. Autophagosomes can support Yersinia pseudotuberculosis replication in macrophages. Cell Microbiol (2010) 12:1108-23. doi:10.1111/j.1462-5822.2010.01456.x
22. Pujol C, Klein KA, Romanov GA, Palmer LE, Cirota C, Zhao Z, et al. Yersinia pestis can reside in autophagosomes and avoid xenophagy in murine macrophages by preventing vacuole acidification. Infect Immun (2009) 77:2251-61. doi:10.1128/IAI.00068-09
23. Gutierrez MG, Vázquez CL, Munafó DB, Zoppino FCM, Berón W, Rabinovitch M, et al. Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles. Cell Microbiol (2005) 7:981-93. doi:10.1111/j.1462-5822.2005.00527.x
24. Vázquez CL, Colombo MI. Coxiella burnetii modulates Beclin 1 and Bcl-2, preventing host cell apoptosis to generate a persistent bacterial infection. Cell Death Differ (2010) 17:421-38. doi:10.1038/cdd.2009.129
25. Berón W, Gutierrez MG, Rabinovitch M, Colombo MI. Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics. Infect Immun (2002) 70:5816-21. doi:10.1128/IAI.70.10.5816-5821.2002
26. Steele S, Brunton J, Ziehr B, Taft-Benz S, Moorman N, Kawula T. Francisella tularensis harvests nutrients derived via ATG5-independent autophagy to support intracellular growth. PLoS Pathog (2013) 9:e1003562. doi:10.1371/journal.ppat.1003562
27. Starr T, Child R, Wehrly TD, Hansen B, Hwang S, López-Otin C, et al. Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle. Cell Host Microbe (2012) 11:33-45. doi:10.1016/j.chom.2011.12.002
28. Mestre MB, Fader CM, Sola C, Colombo MI. Alpha-hemolysin is required for the activation of the autophagic pathway in Staphylococcus aureus-infected cells. Autophagy (2010) 6:110-25. doi:10.4161/auto.6.1.10698
29. Mestre MB, Colombo MI. cAMP and EPAC are key players in the regulation of the signal transduction pathway involved in the a-hemolysin autophagic response. PLoS Pathog (2012) 8:e1002664. doi:10.1371/journal.ppat.1002664
30. Amer AO, Swanson MS. Autophagy is an immediate macrophage response to Legionella pneumophila. Cell Microbiol (2005) 7:765-78. doi:10.1111/j.1462-5822.2005.00509.x
31. Kagan JC, Roy CR. Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol (2002) 4:945-54. doi:10.1038/ncb883
32. Khweek AA, Caution K, Akhter A, Abdulrahman BA, Tazi M, Hassan H, et al. A bacterial protein promotes the recognition of the Legionella pneumophila vacuole by autophagy. Eur J Immunol (2013) 43:1333-44. doi:10.1002/eji.201242835
33. Amer AO, Byrne BG, Swanson MS. Macrophages rapidly transfer pathogens from lipid raft vacuoles to autophagosomes. Autophagy (2005) 1:53-8. doi:10.4161/auto.1.1.1589
34. Choy A, Dancourt J, Mugo B, O'Connor TJ, Isberg RR, Melia TJ, et al. The Legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation. Science (2012) 338:1072-6. doi:10.1126/science.1227026
35. Rolando M, Escoll P, Nora T, Botti J, Boitez V, Bedia C, et al. Legionella pneumophila S1P-lyase targets host sphingolipid metabolism and restrains autophagy. Proc Natl Acad Sci U S A (2016) 113(7):1901-6. doi:10.1073/pnas.1522067113
36. Joshi AD, Swanson MS. Secrets of a successful pathogen: Legionella resistance to progression along the autophagic pathway. Front Microbiol (2011) 2:138. doi:10.3389/fmicb.2011.00138
37. Vakifahmetoglu-Norberg H, Xia H-G, Yuan J. Pharmacologic agents targeting autophagy. J Clin Invest (2015) 125:5-13. doi:10.1172/JCI73937
38. Siddiqi SH, Hawkins JE, Laszlo A. Interlaboratory drug susceptibility testing of Mycobacterium tuberculosis by a radiometric procedure and two conventional methods. J Clin Microbiol (1985) 22:919-23.
39. Stottmeier KD, Beam RE, Kubica GP. Determination of drug susceptibility of mycobacteria to pyrazinamide in 7H10 agar. Am Rev Respir Dis (1967) 96:1072-5.
40. Kim JJ, Lee HM, Shin DM, Kim W, Yuk JM, Jin HS, et al. Host cell autophagy activated by antibiotics is required for their effective antimycobacterial drug action. Cell Host Microbe (2012) 11:457-68. doi:10.1016/j.chom.2012.03.008
41. Zullo AJ, Lee S. Old antibiotics target TB with a new trick. Cell Host Microbe (2012) 11:419-20. doi:10.1016/j.chom.2012.05.002
42. Renna M, Schaffner C, Brown K, Shang S, Tamayo MH, Hegyi K, et al. Azithromycin blocks autophagy and may predispose cystic fibrosis patients to mycobacterial infection. J Clin Invest (2011) 121:3554-63. doi:10.1172/JCI46095
43. Conway KL, Kuballa P, Song J-H, Patel KK, Castoreno AB, Yilmaz OH, et al. Atg16l1 is required for autophagy in intestinal epithelial cells and protection of mice from Salmonella infection. Gastroenterology (2013) 145:1347-57. doi:10.1053/j.gastro.2013.08.035
44. Kuo S-Y, Castoreno AB, Aldrich LN, Lassen KG, Goel G, Dancík V, et al. Small-molecule enhancers of autophagy modulate cellular disease phenotypes suggested by human genetics. Proc Natl Acad Sci U S A (2015) 112:E4281-7. doi:10.1073/pnas.1512289112
45. Raoult D, Houpikian P, Tissot Dupont H, Riss JM, Arditi-Djiane J, Brouqui P. Treatment of Q fever endocarditis: comparison of 2 regimens containing doxycycline and ofloxacin or hydroxychloroquine. Arch Intern Med (1999) 159:167-73. doi:10.1001/archinte.159.2.167