Avoidance of autophagy mediated by PlcA or ActA is required for listeria monocytogenes growth in macrophages

Infection and Immunity

Volumn 83, Issue 5, 2015, Pages 2175-2184

  Mitchell, Gabriel ^a   Ge, Liang ^a   Huang, Qiongying ^a,b   Chen, Chen ^a   Kianian, Sara ^a   Roberts, Mary F ^b   Schekman, Randy ^a   Portnoy, Daniel A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BOSTON COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTA PROTEIN; BACTERIAL PROTEIN; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHOLIPASE C; UNCLASSIFIED DRUG; ACTA PROTEIN, LISTERIA MONOCYTOGENES; MEMBRANE PROTEIN; VIRULENCE FACTOR;

ACTIN POLYMERIZATION; ALLELE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL GRANULE; CELL GROWTH; CONTROLLED STUDY; HUMAN; HUMAN CELL; LISTERIA MONOCYTOGENES; MACROPHAGE; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CELL CULTURE; GENE DELETION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY;

ANIMALS; AUTOPHAGY; BACTERIAL PROTEINS; CELLS, CULTURED; GENE DELETION; IMMUNE EVASION; LISTERIA MONOCYTOGENES; MACROPHAGES; MEMBRANE PROTEINS; MICE, INBRED C57BL; TYPE C PHOSPHOLIPASES; VIRULENCE FACTORS;

EID: 84928183057     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00110-15     Document Type: Article

References (64)

1. Cossart P. 2011. Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proc Natl Acad Sci U S A 108:19484-19491. http://dx.doi.org/10.1073/pnas.1112371108.
2. Hamon M, Bierne H, Cossart P. 2006. Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 4:423-434. http://dx.doi.org/10.1038/nrmicro1413.
3. Vazquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Dominguez-Bernal G, Goebel W, Gonzalez-Zorn B, Wehland J, Kreft J. 2001. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14:584-640. http://dx.doi.org/10.1128/CMR.14.3.584-640.2001.
4. Schnupf P, Portnoy DA. 2007. Listeriolysin O: a phagosome-specific lysin. Microbes Infect 9:1176-1187. http://dx.doi.org/10.1016/j.micinf.2007.05.005.
5. Goldfine H, Bannam T, Johnston NC, Zuckert WR. 1998. Bacterial phospholipases and intracellular growth: the two distinct phospholipases C of Listeria monocytogenes. Symp Ser Soc Appl Microbiol 27:7S-14S.
6. Smith GA, Marquis H, Jones S, Johnston NC, Portnoy DA, Goldfine H. 1995. The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread. Infect Immun 63:4231-4237.
7. Camilli A, Tilney LG, Portnoy DA. 1993. Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol Microbiol 8:143-157. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01211.x.
8. Lambrechts A, Gevaert K, Cossart P, Vandekerckhove J, Van Troys M. 2008. Listeria comet tails: the actin-based motility machinery at work. Trends Cell Biol 18:220-227. http://dx.doi.org/10.1016/j.tcb.2008.03.001.
9. de las Heras A, Cain RJ, Bielecka MK, Vazquez-Boland JA. 2011. Regulation of Listeria virulence: PrfA master and commander. Curr Opin Microbiol 14:118-127. http://dx.doi.org/10.1016/j.mib.2011.01.005.
10. Freitag NE, Port GC, Miner MD. 2009. Listeria monocytogenes-from saprophyte to intracellular pathogen. Nat Rev Microbiol 7:623-628. http://dx.doi.org/10.1038/nrmicro2171.
11. Codogno P, Mehrpour M, Proikas-Cezanne T. 2012. Canonical and non-canonical autophagy: variations on a common theme of self-eating? Nat Rev Mol Cell Biol 13:7-12. http://dx.doi.org/10.1038/nrm3249.
12. Deretic V, Saitoh T, Akira S. 2013. Autophagy in infection, inflammation and immunity. Nat Rev Immunol 13:722-737. http://dx.doi.org/10.1038/nri3532.
13. Funderburk SF, Wang QJ, Yue Z. 2010. The Beclin 1-VPS34 complex-at the crossroads of autophagy and beyond. Trends Cell Biol 20:355-362. http://dx.doi.org/10.1016/j.tcb.2010.03.002.
14. Lam GY, Cemma M, Muise AM, Higgins DE, Brumell JH. 2013. Host and bacterial factors that regulate LC3 recruitment to Listeria monocytogenes during the early stages of macrophage infection. Autophagy 9:985-995. http://dx.doi.org/10.4161/auto.24406.
15. Sanjuan MA, Dillon CP, Tait SW, Moshiach S, Dorsey F, Connell S, Komatsu M, Tanaka K, Cleveland JL, Withoff S, Green DR. 2007. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450:1253-1257. http://dx.doi.org/10.1038/nature06421.
16. Huang J, Brumell JH. 2014. Bacteria-autophagy interplay: a battle for survival. Nat Rev Microbiol 12:101-114. http://dx.doi.org/10.1038/nrmicro3160.
17. Choy A, Roy CR. 2013. Autophagy and bacterial infection: an evolving arms race. Trends Microbiol 21:451-456. http://dx.doi.org/10.1016/j.tim.2013.06.009.
18. Deretic V, Levine B. 2009. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5:527-549. http://dx.doi.org/10.1016/j.chom.2009.05.016.
19. Meyer-Morse N, Robbins JR, Rae CS, Mochegova SN, Swanson MS, Zhao Z, Virgin HW, Portnoy D. 2010. Listeriolysin O is necessary and sufficient to induce autophagy during Listeria monocytogenes infection. PLoS One 5:e8610. http://dx.doi.org/10.1371/journal.pone.0008610.
20. Lam GY, Czuczman MA, Higgins DE, Brumell JH. 2012. Interactions of Listeria monocytogenes with the autophagy system of host cells. Adv Immunol 113:7-18. http://dx.doi.org/10.1016/B978-0-12-394590-7.00008-7.
21. Dortet L, Mostowy S, Samba-Louaka A, Gouin E, Nahori MA, Wiemer EA, Dussurget O, Cossart P. 2011. Recruitment of the major vault protein by InlK: a Listeria monocytogenes strategy to avoid autophagy. PLoS Pathog 7:e1002168. http://dx.doi.org/10.1371/journal.ppat.1002168.
22. Yoshikawa Y, Ogawa M, Hain T, Yoshida M, Fukumatsu M, Kim M, Mimuro H, Nakagawa I, Yanagawa T, Ishii T, Kakizuka A, Sztul E, Chakraborty T, Sasakawa C. 2009. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat Cell Biol 11:1233-1240. http://dx.doi.org/10.1038/ncb1967.
23. Birmingham CL, Canadien V, Gouin E, Troy EB, Yoshimori T, Cossart P, Higgins DE, Brumell JH. 2007. Listeria monocytogenes evades killing by autophagy during colonization of host cells. Autophagy 3:442-451. http://dx.doi.org/10.4161/auto.4450.
24. Rich KA, Burkett C, Webster P. 2003. Cytoplasmic bacteria can be targets for autophagy. Cell Microbiol 5:455-468. http://dx.doi.org/10.1046/j.1462-5822.2003.00292.x.
25. Py BF, Lipinski MM, Yuan J. 2007. Autophagy limits Listeria monocytogenes intracellular growth in the early phase of primary infection. Autophagy 3:117-125. http://dx.doi.org/10.4161/auto.3618.
26. Tattoli I, Sorbara MT, Yang C, Tooze SA, Philpott DJ, Girardin SE. 2013. Listeria phospholipases subvert host autophagic defenses by stalling pre-autophagosomal structures. EMBOJ 32:3066-3078. http://dx.doi.org/10.1038/emboj.2013.234.
27. Sauer JD, Sotelo-Troha K, von Moltke J, Monroe KM, Rae CS, Brubaker SW, Hyodo M, Hayakawa Y, Woodward JJ, Portnoy DA, Vance RE. 2011. The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect Immun 79:688-694. http://dx.doi.org/10.1128/IAI.00999-10.
28. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N. 2004. The role of autophagy during the early neonatal starvation period. Nature 432:1032-1036. http://dx.doi.org/10.1038/nature03029.
29. Zhao Z, Fux B, Goodwin M, Dunay IR, Strong D, Miller BC, Cadwell K, Delgado MA, Ponpuak M, Green KG, Schmidt RE, Mizushima N, Deretic V, Sibley LD, Virgin HW. 2008. Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe 4:458-469. http://dx.doi.org/10.1016/j.chom.2008.10.003.
30. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, Al-Zeer MA, Albert ML, Albin RL, Alegre-Abarrategui J, Aleo MF, Alirezaei M, Almasan A, Almonte-Becerril M, Amano A, Amaravadi R, Amarnath S, Amer AO, Andrieu-Abadie N, Anantharam V, Ann DK, Anoopkumar-Dukie S, Aoki H, Apostolova N, Arancia G, Aris JP, Asanuma K, Asare NY, Ashida H, Askanas V, Askew DS, Auberger P, Baba M, Backues SK, Baehrecke EH, Bahr BA, Bai XY, Bailly Y, Baiocchi R, Baldini G, et al. 2012. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8:445-544. http://dx.doi.org/10.4161/auto.19496.
31. Skoble J, Portnoy DA, Welch MD. 2000. Three regions within ActA promote Arp2/3 complex-mediated actin nucleation and Listeria monocytogenes motility. J Cell Biol 150:527-538. http://dx.doi.org/10.1083/jcb.150.3.527.
32. Jones S, Portnoy DA. 1994. Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysinOin place of listeriolysin O. Infect Immun 62:5608-5613.
33. Lauer P, Chow MY, Loessner MJ, Portnoy DA, Calendar R. 2002. Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J Bacteriol 184:4177-4186. http://dx.doi.org/10.1128/JB.184.15.4177-4186.2002.
34. Slepkov ER, Pavinski Bitar A, Marquis H. 2010. Differentiation of propeptide residues regulating the compartmentalization, maturation and activity of the broad-range phospholipaseCof Listeria monocytogenes. Biochem J 432:557-563. http://dx.doi.org/10.1042/BJ20100557.
35. Shen A, Higgins DE. 2005. The 5' untranslated region-mediated enhancement of intracellular listeriolysin O production is required for Listeria monocytogenes pathogenicity. Mol Microbiol 57:1460-1473. http://dx.doi.org/10.1111/j.1365-2958.2005.04780.x.
36. Portnoy DA, Jacks PS, Hinrichs DJ. 1988. Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167:1459-1471. http://dx.doi.org/10.1084/jem.167.4.1459.
37. Chong S, Mersha FB, Comb DG, Scott ME, Landry D, Vence LM, Perler FB, Benner J, Kucera RB, Hirvonen CA, Pelletier JJ, Paulus H, Xu MQ. 1997. Single-column purification of free recombinant proteins using a self-cleavable affinity tag derived from a protein splicing element. Gene 192:271-281. http://dx.doi.org/10.1016/S0378-1119(97)00105-4.
38. Chen W, Goldfine H, Ananthanarayanan B, Cho W, Roberts MF. 2009. Listeria monocytogenes phosphatidylinositol-specific phospholipase C: kinetic activation and homing in on different interfaces. Biochemistry 48:3578-3592. http://dx.doi.org/10.1021/bi802312d.
39. Hergenrother PJ, Martin SF. 1997. Determination of the kinetic parameters for phospholipase C (Bacillus cereus) on different phospholipid substrates using a chromogenic assay based on the quantitation of inorganic phosphate. Anal Biochem 251:45-49. http://dx.doi.org/10.1006/abio.1997.2251.
40. Ge L, Melville D, Zhang M, Schekman R. 2013. The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. eLife 2:e00947. http://dx.doi.org/10.7554/eLife.00947.
41. Goldfine H, Johnston NC, Knob C. 1993. Nonspecific phospholipase C of Listeria monocytogenes: activity on phospholipids in Triton X-100-mixed micelles and in biological membranes. J Bacteriol 175:4298-4306.
42. Ge L, Wang J, Qi W, Miao HH, Cao J, Qu YX, Li BL, Song BL. 2008. The cholesterol absorption inhibitor ezetimibe acts by blocking the sterolinduced internalization of NPC1L1. Cell Metab 7:508-519. http://dx.doi.org/10.1016/j.cmet.2008.04.001.
43. Ge L, Qi W, Wang LJ, Miao HH, Qu YX, Li BL, Song BL. 2011. Flotillins play an essential role in Niemann-Pick C1-like 1-mediated cholesterol uptake. Proc Natl Acad Sci U S A 108:551-556. http://dx.doi.org/10.1073/pnas.1014434108.
44. Research Council National. 1996. Guide for the care and use of laboratory animals. National Academies Press, Washington, DC.
45. Ge L, Schekman R. 2014. The ER-Golgi intermediate compartment feeds the phagophore membrane. Autophagy 10:170-172. http://dx.doi.org/10.4161/auto.26787.
46. Ge L, Zhang M, Schekman R. 2014. Phosphatidylinositol 3-kinase and COPII generate LC3 lipidation vesicles from the ER-Golgi intermediate compartment. eLife 3:e04135. http://dx.doi.org/10.7554/eLife.04135.
47. Geoffroy C, Raveneau J, Beretti JL, Lecroisey A, Vazquez-Boland JA, Alouf JE, Berche P. 1991. Purification and characterization of an extracellular 29-kilodalton phospholipase C from Listeria monocytogenes. Infect Immun 59:2382-2388.
48. Sibelius U, Chakraborty T, Krogel B, Wolf J, Rose F, Schmidt R, Wehland J, Seeger W, Grimminger F. 1996. The listerial exotoxins listeriolysin and phosphatidylinositol-specific phospholipase C synergize to elicit endothelial cell phosphoinositide metabolism. J Immunol 157:4055-4060.
49. Sibelius U, Schulz EC, Rose F, Hattar K, Jacobs T, Weiss S, Chakraborty T, Seeger W, Grimminger F. 1999. Role of Listeria monocytogenes exotoxins listeriolysin and phosphatidylinositol-specific phospholipase C in activation of human neutrophils. Infect Immun 67:1125-1130.
50. Huang J, Birmingham CL, Shahnazari S, Shiu J, Zheng YT, Smith AC, Campellone KG, Heo WD, Gruenheid S, Meyer T, Welch MD, Ktistakis NT, Kim PK, Klionsky DJ, Brumell JH. 2011. Antibacterial autophagy occurs at PI(3)P-enriched domains of the endoplasmic reticulum and requires Rab1 GTPase. Autophagy 7:17-26. http://dx.doi.org/10.4161/auto.7.1.13840.
51. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT. 2008. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182:685-701. http://dx.doi.org/10.1083/jcb.200803137.
52. Burman C, Ktistakis NT. 2010. Regulation of autophagy by phosphatidylinositol 3-phosphate. FEBS Lett 584:1302-1312. http://dx.doi.org/10.1016/j.febslet.2010.01.011.
53. Di Paolo G, De Camilli P. 2006. Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651-657. http://dx.doi.org/10.1038/nature05185.
54. Hilbi H. 2006. Modulation of phosphoinositide metabolism by pathogenic bacteria. Cell Microbiol 8:1697-1706. http://dx.doi.org/10.1111/j.1462-5822.2006.00793.x.
55. Pizarro-Cerda J, Kuhbacher A, Cossart P. 19 September 2014. Phosphoinositides and host-pathogen interactions. Biochim Biophys Acta http://dx.doi.org/10.1016/j.bbalip.2014.09.011.
56. Steffen P, Schafer DA, David V, Gouin E, Cooper JA, Cossart P. 2000. Listeria monocytogenes ActA protein interacts with phosphatidylinositol 4,5-bisphosphate in vitro. Cell Motil Cytoskeleton 45:58-66. http://dx.doi.org/10.1002/(SICI)1097-0169(200001)45:1<58::AID-CM6>3.0.CO;2-Y.
57. Cicchetti G, Maurer P, Wagener P, Kocks C. 1999. Actin and phosphoinositide binding by the ActA protein of the bacterial pathogen Listeria monocytogenes. J Biol Chem 274:33616-33626. http://dx.doi.org/10.1074/jbc.274.47.33616.
58. Choy A, Dancourt J, Mugo B, O'Connor TJ, Isberg RR, Melia TJ, Roy CR. 2012. The Legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation. Science 338:1072-1076. http://dx.doi.org/10.1126/science.1227026.
59. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C. 2005. Escape of intracellular Shigella from autophagy. Science 307:727-731. http://dx.doi.org/10.1126/science.1106036.
60. Baxt LA, Goldberg MB. 2014. Host and bacterial proteins that repress recruitment of LC3 to Shigella early during infection. PLoS One 9:e94653. http://dx.doi.org/10.1371/journal.pone.0094653.
61. Poussin MA, Goldfine H. 2010. Evidence for the involvement of ActA in maturation of the Listeria monocytogenes phagosome. Cell Res 20:109-112. http://dx.doi.org/10.1038/cr.2009.142.
62. Bécavin C, Bouchier C, Lechat P, Archambaud C, Creno S, Gouin E, Wu Z, Kühbacher A, Brisse S, Pucciarelli MG, Garcia-del Portillo F, Hain T, Portnoy DA, Chakraborty T, Lecuit M, Pizarro-Cerdá J, Moszer I, Bierne H, Cossart P. 2014. Comparison of widely used Listeria monocytogenes strains EGD, 10403S, and EGD-e highlights genomic variations underlying variations in pathogenicity. mBio 5:e00969-14. http://dx.doi.org/10.1128/mBio.00969-14.
63. Cheng LW, Portnoy DA. 2003. Drosophila S2 cells: an alternative infection model for Listeria monocytogenes. Cell Microbiol 5:875-885. http://dx.doi.org/10.1046/j.1462-5822.2003.00327.x.
64. Angelakopoulos H, Loock K, Sisul DM, Jensen ER, Miller JF, Hohmann EL. 2002. Safety and shedding of an attenuated strain of Listeria monocytogenes with a deletion of actA/plcB in adult volunteers: a dose escalation study of oral inoculation. Infect Immun 70:3592-3601. http://dx.doi.org/10.1128/IAI.70.7.3592-3601.2002.