Poison domains block transit of translocated substrates via the Legionella pneumophila Icm/Dot system

Infection and Immunity

Volumn 81, Issue 9, 2013, Pages 3239-3252

  Amyot, Whitney M ^a,b   DeJesus, Dennise ^a,b   Isberg, Ralph R ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; DIHYDROFOLATE REDUCTASE; HYBRID PROTEIN; UBIQUITIN;

ARTICLE; BACTERIAL TRANSLOCATION; CELL GROWTH; CYTOSOL; HOST CELL; LEGIONELLA PNEUMOPHILA; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; SECRETION (PROCESS);

EID: 84884250041     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00552-13     Document Type: Article

References (68)

1. Fields BS. 1996. The molecular ecology of legionellae. Trends Microbiol. 4:286-290.
2. Fields BS, Benson RF, Besser RE. 2002. Legionella and Legionnaires' disease: 25 years of investigation. Clin. Microbiol. Rev. 15:506-526.
3. Fields BS, Shotts EB, Jr, Feeley JC, Gorman GW, Martin WT. 1984. Proliferation of Legionella pneumophila as an intracellular parasite of the ciliated protozoan Tetrahymena pyriformis. Appl. Environ. Microbiol. 47:467-471.
4. Wadowsky RM, Butler LJ, Cook MK, Verma SM, Paul MA, Fields BS, Keleti G, Sykora JL, Yee RB. 1988. Growth-supporting activity for Legionella pneumophila in tap water cultures and implication of hartmannellid amoebae as growth factors. Appl. Environ. Microbiol. 54:2677-2682.
5. Fraser DW, Tsai TR, Orenstein W, Parkin WE, Beecham HJ, Sharrar RG, Harris J, Mallison GF, Martin SM, McDade JE, Shepard CC, Brachman PS. 1977. Legionnaires' disease: description of an epidemic of pneumonia. N. Engl. J. Med. 297:1189-1197.
6. Horwitz MA, Silverstein SC. 1980. Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J. Clin. Invest. 66:441-450.
7. Segal G, Shuman HA. 1999. Legionella pneumophila utilizes the same genes to multiply within Acanthamoeba castellanii and human macrophages. Infect. Immun. 67:2117-2124.
8. Berger KH, Isberg RR. 1993. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 7:7-19.
9. Segal G, Shuman HA. 1997. Characterization of a new region required for macrophage killing by Legionella pneumophila. Infect. Immun. 65:5057-5066.
10. Altman E, Segal G. 2008. The response regulator CpxR directly regulates expression of several Legionella pneumophila icm/dot components as well as new translocated substrates. J. Bacteriol. 190:1985-1996.
11. de Felipe KS, Glover RT, Charpentier X, Anderson OR, Reyes M, Pericone CD, Shuman HA. 2008. Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog. 4:e1000117. doi:10.1371/journal.ppat.1000117.
12. de Felipe KS, Pampou S, Jovanovic OS, Pericone CD, Ye SF, Kalachikov S, Shuman HA. 2005. Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer. J. Bacteriol. 187:7716-7726.
13. Huang L, Boyd D, Amyot WM, Hempstead AD, Luo ZQ, O'Connor TJ, Chen C, Machner M, Montminy T, Isberg RR. 2011. The E block motif is associated with Legionella pneumophila translocated substrates. Cell Microbiol. 13:227-245.
14. Luo ZQ, Isberg RR. 2004. Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc. Natl. Acad. Sci. U. S. A. 101:841-846.
15. Nagai H, Kagan JC, Zhu X, Kahn RA, Roy CR. 2002. A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295:679-682.
16. Zusman T, Degtyar E, Segal G. 2008. Identification of a hypervariable region containing new Legionella pneumophila Icm/Dot translocated substrates by using the conserved icmQ regulatory signature. Infect. Immun. 76:4581-4591.
17. Zhu W, Banga S, Tan Y, Zheng C, Stephenson R, Gately J, Luo ZQ. 2011. Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila. PLoS One 6:e17638. doi:10.1371/journal.pone.0017638.
18. Nagai H, Kubori T. 2011. Type IVB secretion systems of Legionella and other Gram-negative bacteria. Front. Microbiol. 2:136. doi:10.3389/fmicb.2011.00136.
19. Lifshitz Z, Burstein D, Peeri M, Zusman T, Schwartz K, Shuman HA, Pupko T, Segal G. 2013. Computational modeling and experimental validation of the Legionella and Coxiella virulence-related type-IVB secretion signal. Proc. Nat. Acad. Sci., U. S. A. 110:E707-E715.
20. Kagan JC, Stein MP, Pypaert M, Roy CR. 2004. Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle. J. Exp. Med. 199:1201-1211.
21. Derre I, Isberg RR. 2004. Legionella pneumophila replication vacuole formation involves rapid recruitment of proteins of the early secretory system. Infect. Immun. 72:3048-3053.
22. Molmeret M, Santic M, Asare R, Carabeo RA, Abu Kwaik Y. 2007. Rapid escape of the dot/icm mutants of Legionella pneumophila into the cytosol of mammalian and protozoan cells. Infect. Immun. 75:3290-3304.
23. Christie PJ. 2001. Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol. Microbiol. 40:294-305.
24. Christie PJ, Vogel JP. 2000. Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8:354-360.
25. Wallden K, Rivera-Calzada A, Waksman G. 2010. Type IV secretion systems: versatility and diversity in function. Cell Microbiol. 12:1203-1212.
26. Nagai H, Roy CR. 2003. Show me the substrates: modulation of host cell function by type IV secretion systems. Cell Microbiol. 5:373-383.
27. Beare PA, Gilk SD, Larson CL, Hill J, Stead CM, Omsland A, Cockrell DC, Howe D, Voth DE, Heinzen RA. 2011. Dot/Icm type IVB secretion system requirements for Coxiella burnetii growth in human macrophages. mBio 2(4):e00175-00111. doi:10.1128/mBio.00175-11.
28. Leclerque A, Kleespies RG. 2008. Type IV secretion system components as phylogenetic markers of entomopathogenic bacteria of the genus Rickettsiella. FEMS Microbiol. Lett. 279:167-173.
29. Fronzes R, Christie PJ, Waksman G. 2009. The structural biology of type IV secretion systems. Nat. Rev. Microbiol. 7:703-714.
30. Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J, Waksman G. 2009. Structure of the outer membrane complex of a type IV secretion system. Nature 462:1011-1015.
31. Vincent CD, Friedman JR, Jeong KC, Buford EC, Miller JL, Vogel JP. 2006. Identification of the core transmembrane complex of the Legionella Dot/Icm type IV secretion system. Mol. Microbiol. 62:1278-1291.
32. Vincent CD, Friedman JR, Jeong KC, Sutherland MC, Vogel JP. 2012. Identification of the DotL coupling protein subcomplex of the Legionella Dot/Icm type IV secretion system. Mol. Microbiol. 85:378-391.
33. Klingenberg O, Olsnes S. 1996. Ability of methotrexate to inhibit translocation to the cytosol of dihydrofolate reductase fused to diphtheria toxin. Biochem. J. 313:647-653.
34. Cambronne ED, Roy CR. 2007. The Legionella pneumophila IcmSW complex interacts with multiple Dot/Icm effectors to facilitate type IV translocation. PLoS Pathog. 3:e188. doi:10.1371/journal.ppat.0030188.
35. Burstein D, Zusman T, Degtyar E, Viner R, Segal G, Pupko T. 2009. Genome-scale identification of Legionella pneumophila effectors using a machine learning approach. PLoS Pathog. 5:e1000508. doi:10.1371/journal.ppat.1000508.
36. Bieker KL, Silhavy TJ. 1989. PrlA is important for the translocation of exported proteins across the cytoplasmic membrane of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 86:968-972.
37. Eilers M, Schatz G. 1986. Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature 322:228-232.
38. Endo T, Kawakami M, Goto A, America T, Weisbeek P, Nakai M. 1994. Chloroplast protein import. Chloroplast envelopes and thylakoids have different abilities to unfold proteins. Eur. J. Biochem. 225:403-409.
39. Salvador N, Aguado C, Horst M, Knecht E. 2000. Import of a cytosolic protein into lysosomes by chaperone-mediated autophagy depends on its folding state. J. Biol. Chem. 275:27447-27456.
40. McNew JA, Goodman JM. 1994. An oligomeric protein is imported into peroxisomes in vivo. J. Cell Biol. 127:1245-1257.
41. Walton PA, Hill PE, Subramani S. 1995. Import of stably folded proteins into peroxisomes. Mol. Biol. Cell 6:675-683.
42. Wickner W, Schekman R. 2005. Protein translocation across biological membranes. Science 310:1452-1456.
43. Lee VT, Schneewind O. 2002. Yop fusions to tightly folded protein domains and their effects on Yersinia enterocolitica type III secretion. J. Bacteriol. 184:3740-3745.
44. Sorg JA, Miller NC, Marketon MM, Schneewind O. 2005. Rejection of impassable substrates by Yersinia type III secretion machines. J. Bacteriol. 187:7090-7102.
45. Akeda Y, Galan JE. 2005. Chaperone release and unfolding of substrates in type III secretion. Nature 437:911-915.
46. Feldman MF, Muller S, Wuest E, Cornelis GR. 2002. SycE allows secretion of YopE-DHFR hybrids by the Yersinia enterocolitica type III Ysc system. Mol. Microbiol. 46:1183-1197.
47. Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV, Waksman G. 2009. Structure of a type IV secretion system core complex. Science 323:266-268.
48. Feeley JC, Gibson RJ, Gorman GW, Langford NC, Rasheed JK, Mackel DC, Baine WB. 1979. Charcoal-yeast extract agar: primary isolation medium for Legionella pneumophila. J. Clin. Microbiol. 10:437-441.
49. Berger KH, Isberg RR. 1994. Intracellular survival by Legionella. Methods Cell. Biol. 45:247-259.
50. Coers J, Kagan JC, Matthews M, Nagai H, Zuckman DM, Roy CR. 2000. Identification of Icm protein complexes that play distinct roles in the biogenesis of an organelle permissive for Legionella pneumophila intracellular growth. Mol. Microbiol. 38:719-736.
51. Bardill JP, Miller JL, Vogel JP. 2005. IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol. Microbiol. 56:90-103.
52. Swanson MS, Isberg RR. 1995. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63:3609-3620.
53. Haug G, Wilde C, Leemhuis J, Meyer DK, Aktories K, Barth H. 2003. Cellular uptake of Clostridium botulinum C2 toxin: membrane translocation of a fusion toxin requires unfolding of its dihydrofolate reductase domain. Biochemistry 42:15284-15291.
54. Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA, Roy CR. 2005. A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc. Natl. Acad. Sci. U. S. A. 102:826-831.
55. Derre I, Isberg RR. 2005. LidA, a translocated substrate of the Legionella pneumophila type IV secretion system, interferes with the early secretory pathway. Infect. Immun. 73:4370-4380.
56. Sory MP, Cornelis GR. 1994. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14:583-594.
57. Williams MN, Poe M, Greenfield NJ, Hirshfield JM, Hoogsteen K. 1973. Methotrexate binding to dihydrofolate reductase from a methotrexateresistant strain of Escherichia coli. J. Biol. Chem. 248:6375-6379.
58. Charpentier X, Gabay JE, Reyes M, Zhu JW, Weiss A, Shuman HA. 2009. Chemical genetics reveals bacterial and host cell functions critical for type IV effector translocation by Legionella pneumophila. PLoS Pathog. 5:e1000501. doi:10.1371/journal.ppat.1000501.
59. Johnsson N, Varshavsky A. 1994. Ubiquitin-assisted dissection of protein transport across membranes. EMBO J. 13:2686-2698.
60. Vijay-Kumar S, Bugg CE, Cook WJ. 1987. Structure of ubiquitin refined at 1.8 Å resolution. J. Mol. Biol. 194:531-544.
61. Catic A, Fiebiger E, Korbel GA, Blom D, Galardy PJ, Ploegh HL. 2007. Screen for ISG15-crossreactive deubiquitinases. PLoS One 2:e679. doi:10.1371/journal.pone.0000679.
62. Johnson ES, Bartel B, Seufert W, Varshavsky A. 1992. Ubiquitin as a degradation signal. EMBO J. 11:497-505.
63. Ninio S, Zuckman-Cholon DM, Cambronne ED, Roy CR. 2005. The Legionella IcmS-IcmW protein complex is important for Dot/Icmmediated protein translocation. Mol. Microbiol. 55:912-926.
64. Vincent CD, Vogel JP. 2006. The Legionella pneumophila IcmS-LvgA protein complex is important for Dot/Icm-dependent intracellular growth. Mol. Microbiol. 61:596-613.
65. Sorg JA, Blaylock B, Schneewind O. 2006. Secretion signal recognition by YscN, the Yersinia type III secretion ATPase. Proc. Natl. Acad. Sci. U. S. A. 103:16490-16495.
66. Stebbins CE, Galan JE. 2001. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414:77-81.
67. Sutherland MC, Nguyen TL, Tseng V, Vogel JP. 2012. The Legionella IcmSW complex directly interacts with DotL to mediate translocation of adaptor-dependent substrates. PLoS Pathog. 8:e1002910. doi:10.1371/journal.ppat.1002910.
68. Buscher BA, Conover GM, Miller JL, Vogel SA, Meyers SN, Isberg RR, Vogel JP. 2005. The DotL protein, a member of the TraG-coupling protein family, is essential for Viability of Legionella pneumophila strain Lp02. J. Bacteriol. 187:2927-2938.