Budowa IV systemu sekrecji Legionella pneumophilai jego znaczenie w patogenezie

Bożena Kowalczyk; Agata Małek; Marta Palusińska-Szysz

doi:10.2478/ahem-2021-0023

.blurhash-client-img { display: none !important; }

Budowa IV systemu sekrecji Legionella pneumophilai jego znaczenie w patogenezie

Postępy Higieny i Medycyny Doświadczalnej

Volume 75 (2021): Issue 1 (January 2021)

By: Bożena Kowalczyk, Agata Małek and Marta Palusińska-Szysz

Open Access

|Oct 2021

Abstract

Legionella pneumophila bacteria in the natural environment parasitize the cells of selected species of protozoa and, when present in artificial water distribution systems, they become an important etiological factor of pneumonia in humans. The main determinant of the pathogenicity of these bacteria is the capability to live and multiply in pulmonary macrophages, i.e. cells specialized in phagocytosis, killing, and digesting microorganisms. A prerequisite for the development of infection is the breakdown of the killing mechanisms of macrophages and the formation of the replication vacuole LCV (Legionella-containing vacuole). The biogenesis of the LCV vacuole is possible due to the efficient functioning of the IV secretion system Dot/Icm, which is a multi-protein complex located in the inner and outer membranes of the cell envelope. The Dot/Icm system consists of 27 components, including a core-transmembrane complex, which is the structural backbone of the entire system, and a complex of coupling proteins. Genes encoding the Dot/Icm system components are organized into two regions of the bacterial chromosome. The Dot/Icm secretion system enables L. pneumophila to introduce more than 300 effector proteins into the cytosol of the host cell, whose coordinated action maintains the integrity of the replication vacuole membrane and allows the manipulation of various cell processes. An important element of the intracellular multiplication strategy of L. pneumophila is the modulation of vesicular transport, interaction with the endoplasmic reticulum, and disruption of protein biosynthesis, autophagy, and apoptosis of the host cell. Understanding the complex mechanisms of regulation and function of the Dot/Icm effector proteins is critical in the prevention and treatment of Legionnaires' disease.

References

Cazalet C., Rusniok C., Brüggemann H., Zidane N., Magnier A., Ma L., Tichit M., Jarraud S., Bouchier C., Vandenesch F., Kunst F., Etienne J., Glaser P., Buchrieser C.: Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat. Genet., 2004; 36:1165-1173
Open DOI Search in Google Scholar Back to article
Rolando M., Sanulli S., Rusniok C., Gomez-Valero L., Bertholet C., Sahr T., Margueron R., Buchrieser C.: Legionella pneumophila effector RomA uniquely modifies host chromatin to repress gene expression and promote intracellular bacterial replication. Cell Host Microbe, 2013; 13: 395-405
Open DOI Search in Google Scholar Back to article
Nisar M.A., Ross K.E., Brown M.H., Bentham R., Whiley H.: Legionella pneumophila and protozoan hosts: Implications for the control of hospital and potable water systems. Pathogens, 2020; 9: 286
Open DOI Search in Google Scholar Back to article
Palazzolo C., Maffongelli G., D’Abramo A., Lepore L., Mariano A., Vulcano A., Bartoli T.A., Bevilacqua N., Giancola M.L., Di Rosa E., Nicastri E.: Legionella pneumonia: Increased risk after CO-VID-19 lockdown? Italy, May to June 2020. Euro. Surveill., 2020; 25: 2001372
Open DOI Search in Google Scholar Back to article
Finnerty W.R., Makula R.A., Feeley J.C.: Cellular lipids of the Legionnaires’ disease bacterium. Ann. Intern. Med., 1979; 90: 631634
Open DOI Search in Google Scholar Back to article
Vincent C.D., Friedman J.R., Jeong K.C., Buford E.C., Miller J.L., Vogel J.P.: Identification of the core transmembrane complex of the Legionella Dot/Icm type IV secretion system. Mol. Microbiol., 2006; 62: 1278-1291
Open DOI Search in Google Scholar Back to article
Palusińska-Szysz M., Russa R.: Chemical structure and biological significance of lipopolysaccharide from Legionella. Recent Pat. Antiinfect. Drug Discov., 2009; 4: 96-107
Open DOI Search in Google Scholar Back to article
Shevchuk O., Jäger J., Steinert M.: Virulence properties of the Legionella pneumophila cell envelope. Front. Microbiol., 2011; 2: 74
Open DOI Search in Google Scholar Back to article
Locht C., Coutte L., Mielcarek N.: The ins and outs of pertussis toxin. FEBS J., 2011; 278: 4668-4682
Open DOI Search in Google Scholar Back to article
Schmölders J., Manske C., Otto A., Hoffmann C., Steiner B., Welin A., Becher D., Hilbi H.: Comparative proteomics of purified pathogen vacuoles correlates intracellular replication of Legionella pneumophila with the small GTPase Ras-related protein 1 (Rap1). Mol. Cell. Proteomics, 2017; 16: 622-641
Open DOI Search in Google Scholar Back to article
Isberg R.R., O’Connor T.J., Heidtman M.: The Legionella pneumophila replication vacuole: Making a cosy niche inside host cells. Nat. Rev. Microbiol., 2009; 7: 13-24
Open DOI Search in Google Scholar Back to article
de la Cruz F., Frost L.S., Meyer R.J., Zechner E.L.: Conjugative DNA metabolism in gram-negative bacteria. FEMS Microbiol. Rev., 2010; 34: 18-40
Open DOI Search in Google Scholar Back to article
Newton H.J., Ang D.K., van Driel I.R., Hartland E.L.: Molecular pathogenesis of infections caused by Legionella pneumophila. Clin. Microbiol. Rev., 2010; 23: 274-298
Open DOI Search in Google Scholar Back to article
Palusińska-Szysz M., Cendrowska-Pinkosz M.: Występowanie i chorobotwórczość bakterii z rodziny Legionellaceae. Postępy Hig. Med. Dośw., 2008; 62: 337-353
Search in Google Scholar Back to article
Paumet F., Wesolowski J., Garcia-Diaz A., Delevoye C., Aulner N., Shuman H.A., Subtil A., Rothman J.E.: Intracellular bacteria encode inhibitory SNARE-like proteins. PLoS One, 2009; 4: e7375
Open DOI Search in Google Scholar Back to article
Chandran Darbari V., Waksman G.: Structural biology of bacterial type IV secretion systems. Annu. Rev. Biochem., 2015; 84: 603629
Open DOI Search in Google Scholar Back to article
Inaba J.I., Xu K., Kovalev N., Ramanathan H., Roy C.R., Lindenbach B.D., Nagy P.D.: Screening Legionella effectors for antiviral effects reveals Rab1 GTPase as a proviral factor coopted for tombusvirus replication. Proc. Natl. Acad. Sci. USA, 2019; 116: 21739-21747
Open DOI Search in Google Scholar Back to article
Segal G., Purcell M., Shuman H.A.: Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc. Natl. Acad. Sci. USA, 1998; 95: 1669-1674
Open DOI Search in Google Scholar Back to article
Zuckman D.M., Hung J.B., Roy C.R.: Pore-forming activity is not sufficient for Legionella pneumophila phagosome trafficking and intracellular growth. Mol. Microbiol., 1999; 32: 990-1001
Open DOI Search in Google Scholar Back to article
Sutherland M.C., Nguyen T.L., Tseng V., Vogel J.P.: The Legionella IcmSW complex directly interacts with DotL to mediate translocation of adaptor-dependent substrates. PLoS Path., 2012; 8: e1002910
Open DOI Search in Google Scholar Back to article
Nakano N., Kubori T., Kinoshita M., Imada K., Nagai H.: Crystal structure of Legionella DotD: Insights into the relationship between type IVB and type II/III secretion systems. PLoS Pathog., 2010; 6: e1001129
Open DOI Search in Google Scholar Back to article
Kirby J.E., Vogel J.P., Andrews H.L., Isberg R.R.: Evidence for pore-forming ability by Legionella pneumophila. Mol. Microbiol., 1998; 27: 323-336
Open DOI Search in Google Scholar Back to article
Durie C.L., Sheedlo M.J., Chung J.M., Byrne B.G., Su M., Knight T., Swanson M., Lacy D.B., Ohi M.D.: Structural analysis of the Legionella pneumophila Dot/Icm type IV secretion system core complex. eLife, 2020; 9: e59530
Open DOI Search in Google Scholar Back to article
Luo Z.Q., Isberg R.R.: Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc. Natl. Acad. Sci. USA, 2004; 101: 841-846
Open DOI Search in Google Scholar Back to article
Dorer M.S., Kirton D., Bader J.S., Isberg R.R.: RNA interference analysis of Legionella in Drosophila cells: Exploitation of early secretory apparatus dynamics. PLoS Pathog., 2006; 2: e34
Open DOI Search in Google Scholar Back to article
Kubori T., Koike M., Bui X.T., Higaki S., Aizawa S.I., Nagai H.: Native structure of a type IV secretion system core complex essential for Legionella pathogenesis. Proc. Natl. Acad. Sci. USA, 2014; 111: 11804-11809
Open DOI Search in Google Scholar Back to article
Meir A., Macé K., Lukoyanova N., Chetrit D., Hospenthal M.K., Redzej A., Roy C., Waksman G.: Mechanism of effector capture and delivery by the type IV secretion system from Legionella pneumophila. Nat. Commun., 2020; 11: 2864
Open DOI Search in Google Scholar Back to article
Vincent C.D., Friedman J.R., Jeong K.C., Sutherland M.C., Vogel J.P.: Identification of the DotL coupling protein subcomplex of the Legionella Dot/Icm type IV secretion system. Mol. Microbiol., 2012; 85: 378-391
Open DOI Search in Google Scholar Back to article
Kwak M.J., Kim J.D., Kim H., Kim C., Bowman J.W., Kim S., Joo K., Lee J., Jin K.S., Kim Y.G., Lee N.K., Jung J.U., Oh B.H.: Architecture of the type IV coupling protein complex of Legionella pneumophila. Nat. Microbiol., 2017; 2: 17114
Open DOI Search in Google Scholar Back to article
Massey T.H., Mercogliano C.P., Yates J., Sherratt D.J., Löwe J.: Double-stranded DNA translocation: Structure and mechanism of hexameric FtsK. Mol. Cell, 2006; 23: 457-469
Open DOI Search in Google Scholar Back to article
Morozova I., Qu X., Shi S., Asamani G., Greenberg J.E., Shuman H.A., Russo J.J.: Comparative sequence analysis of the icm/dot genes in Legionella. Plasmid, 2004; 51: 127-147
Open DOI Search in Google Scholar Back to article
Szpirer C.Y., Faelen M., Couturier M.: Interaction between the RP4 coupling protein TraG and the pBHR1 mobilization protein Mob. Mol. Microbiol., 2000; 37: 1283-1292
Open DOI Search in Google Scholar Back to article
Tato I., Zunzunegui S., de la Cruz F., Cabezon E.: TrwB, the coupling protein involved in DNA transport during bacterial conjugation, is a DNA-dependent ATPase. Proc. Natl. Acad. Sci. USA, 2005; 102: 8156-8161
Open DOI Search in Google Scholar Back to article
Sexton J.A., Miller J.L., Yoneda A., Kehl-Fie T.E., Vogel J.P.: Legionella pneumophila DotU and IcmF are required for stability of the Dot/Icm complex. Infect. Immun., 2004; 72: 5983-5992
Open DOI Search in Google Scholar Back to article
Kim H., Kubori T., Yamazaki K., Kwak M.J., Park S.Y., Nagai H., Vogel J.P., Oh B.H.: Structural basis for effector protein recognition by the Dot/Icm Type IVB coupling protein complex. Nat. Commun., 2020; 11: 2623
Open DOI Search in Google Scholar Back to article
Parsot C., Hamiaux C., Page A.L.: The various and varying roles of specific chaperones in type III secretion systems. Curr. Opin. Microbiol., 2003; 6: 7-14
Open DOI Search in Google Scholar Back to article
Ninio S., Zuckman-Cholon D.M., Cambronne E.D., Roy C.R.: The Legionella IcmS-IcmW protein complex is important for Dot/Icmmediated protein translocation. Mol. Microbiol., 2005; 55: 912-926
Open DOI Search in Google Scholar Back to article
Nagai H., Cambronne E.D., Kagan J.C., Amor J.C., Kahn R.A., Roy C.R.: A C-terminal translocation signal required for Dot/Icmdependent delivery of the Legionella RalF protein to host cells. Proc. Natl. Acad. Sci. USA, 2005; 102: 826-831
Open DOI Search in Google Scholar Back to article
Huang L., Boyd D., Amyot W.M., Hempstead A.D., Luo Z.Q., O’Connor T.J., Chen C., Machner M., Montminy T., Isberg R.R.: The E Block motif is associated with Legionella pneumophila translocated substrates. Cell. Microbiol., 2011; 13: 227-245
Open DOI Search in Google Scholar Back to article
Matthews M., Roy C.R.: Identification and subcellular localization of the Legionella pneumophila IcmX protein: A factor essential for establishment of a replicative organelle in eukaryotic host cells. Infect. Immun., 2000; 68: 3971-3982
Open DOI Search in Google Scholar Back to article
Schuelein R., Spencer H., Dagley L.F., Li P.F., Luo L., Stow J.L., Abraham G., Naderer T., Gomez-Valero L., Buchrieser C., Sugimoto C., Yamagishi J., Webb A.I., Pasricha S., Hartland E.L.: Targeting of RNA polymerase II by a nuclear Legionella pneumophila Dot/Icm effector SnpL. Cell. Microbiol., 2018; 20: e12852
Open DOI Search in Google Scholar Back to article
Farelli J.D., Gumbart J.C., Akey I.V., Hempstead A., Amyot W., Head J.F., McKnight C.J., Isberg R.R., Akey C.W.: IcmQ in the type 4b secretion system contains an NAD⁺ binding domain. Structure, 2013; 21: 1361-1373
Open DOI Search in Google Scholar Back to article
Jørgensen R., Wang Y., Visschedyk D., Merrill A.R.: The nature and character of the transition state for the ADP-ribosyltransferase reaction. EMBO Rep., 2008; 9: 802-809
Open DOI Search in Google Scholar Back to article
Quaile A.T., Stogios P.J., Egorova O., Evdokimova E., Valleau D., Nocek B., Kompella P.S., Peisajovich S., Yakunin A.F., Ensminger A.W., Savchenko A.: The Legionella pneumophila effector Ceg4 is a phosphotyrosine phosphatase that attenuates activation of eukaryotic MAPK pathways. J. Biol. Chem., 2018; 293: 3307-3320
Open DOI Search in Google Scholar Back to article
Sexton J.A., Yeo H.J., Vogel J.P.: Genetic analysis of the Legionella pneumophila DotB ATPase reveals a role in type IV secretion system protein export. Mol. Microbiol., 2005: 57, 70-84
Open DOI Search in Google Scholar Back to article
Sherwood R.K., Roy C.R.: Autophagy evasion and endoplasmic reticulum subversion: The yin and yang of Legionella intracellular infection. Annu. Rev. Microbiol., 2016; 70: 413-433
Open DOI Search in Google Scholar Back to article
Laguna R.K., Creasey E.A., Li Z., Valtz N., Isberg R.R.: A Legionella pneumophila translocated substrate that is required for growth within macrophages and protection from host cell death. Proc. Natl. Acad. Sci. USA, 2006; 103: 18745-18750
Open DOI Search in Google Scholar Back to article
Quan F.S., Kong H.H., Lee H.A., Chu K.B., Moona E.K.: Identification of differentially expressed Legionella genes during its intracellular growth in Acanthamoeba. Heliyon., 2020; 6: e05238
Open DOI Search in Google Scholar Back to article
Park D., Chetrit D., Hu B., Roy C.R., Liu J.: Analysis of Dot/Icm type IVB secretion system subassemblies by cryoelectron tomography reveals conformational changes induced by DotB binding. mBio, 2020; 11: e03328-19
Open DOI Search in Google Scholar Back to article
Nagai H., Kubori T.: Type IVB Secretion systems of Legionella and other Gram-negative bacteria. Front. Microbiol., 2011; 2: 136
Open DOI Search in Google Scholar Back to article
Kuroda T., Kubori T., Bui X.T., Hyakutake A., Uchida Y, Imad K., Nagai H.: Molecular and structural analysis of Legionella DotI gives insights into an inner membrane complex essential for type IV secretion. Sci. Rep., 2015; 5: 10912
Open DOI Search in Google Scholar Back to article
Kubori T., Nagai H.: The Type IVB secretion system: An enigmatic chimera. Curr. Opin. Microbiol., 2016; 29: 22-29
Open DOI Search in Google Scholar Back to article
Roy C.R., Isberg R.R.: Topology of Legionella pneumophila DotA: An inner membrane protein required for replication in macrophages. Infect. Immun., 1997; 65: 571-578
Open DOI Search in Google Scholar Back to article
Higgins C.F.: The ABC of channel regulation. Cell, 1995; 82: 693696
Open DOI Search in Google Scholar Back to article
Hsu F.S., Zhu W., Brennan L., Tao L., Luo Z.Q., Mao Y.: Structural basis for substrate recognition by a unique Legionella phos-phoinositide phosphatase. Proc. Natl. Acad. Sci. USA, 2012; 1090: 13567-13572
Open DOI Search in Google Scholar Back to article
Vance J.E., Vance D.E.: Phospholipid biosynthesis in mammalian cells. Biochem. Cell Biol., 2004; 82: 113-128
Open DOI Search in Google Scholar Back to article
Gal-Mor O., Zusman T., Segal G.: Analysis of DNA regulatory elements required for expression of the Legionella pneumophila icm and dot virulence genes. J. Bacteriol., 2002; 184: 3823-3833
Open DOI Search in Google Scholar Back to article
Ramsey M.E., Woodhams K.L., Dillard J.P.: The gonococcal genetic island and type IV secretion in the pathogenic Neisseria. Front. Microbiol., 2011; 2: 61
Open DOI Search in Google Scholar Back to article
Heidtman M., Chen E.J., Moy M.Y., Isberg R.R.: Large-scale identification of Legionella pneumophila Dot/Icm substrates that modulate host cell vesicle trafficking pathways. Cell. Microbiol., 2009; 11: 230-248
Open DOI Search in Google Scholar Back to article
Hirsch C., Gauss R., Horn S.C., Neuber O., Sommer T.: The ubiquitylation machinery of the endoplasmic reticulum. Nature, 2009; 458: 453-460
Open DOI Search in Google Scholar Back to article
Price C.T., Al-Khodor S., Al-Quadan T., Santic M., Habyarimana F., Kalia A., Kwaik Y.A.: Molecular mimicry by an F-box effector of Legionella pneumophila hijacks a conserved polyubiquitination machinery within macrophages and protozoa. PLoS Pathog., 2009; 5: e1000704
Open DOI Search in Google Scholar Back to article
Sampei G., Furuya N., Tachibana K., Saitou Y., Suzuki T., Mizobuchi K., Komano T.: Complete genome sequence of the incompatibility group I1 plasmid R64. Plasmid, 2010; 64: 92-103
Open DOI Search in Google Scholar Back to article
Rolando M., Escoll P., Nora T., Botti J., Boitez V., Bedia C., Daniels C., Abraham G., Stogios P.J., Skarina T. i wsp.: Legionella pneumophila S1P-lyase targets host sphingolipid metabolism and restrains autophagy. Proc. Natl. Acad. Sci. USA, 2016; 113: 19011906
Open DOI Search in Google Scholar Back to article
Nachmias N., Zusman T., Segal G.: Study of Legionella effector domains revealed novel and prevalent phosphatidylinositol 3-phosphate binding domains. Infect. Immun., 2019; 87: e00153-19
Open DOI Search in Google Scholar Back to article
Grohmann E., Christie P.J., Waksman G., Backert S.: Type IV secretion in gram-negative and gram-positive bacteria. Mol. Microbiol., 2018; 107: 455-471
Open DOI Search in Google Scholar Back to article
Hoffmann C., Finsel I., Otto A., Pfaffinger G., Rothmeier E., Hecker M., Becher D., Hilbi H.: Functional analysis of novel Rab GT-Pases identified in the proteome of purified Legionella-containing vacuoles from macrophages. Cell. Microbiol., 2014; 16: 1034-1052
Open DOI Search in Google Scholar Back to article
Lightfield K.L., Persson J., Brubaker S.W., Witte C.E., von Moltke J., Dunipace E.A., Henry T., Sun Y.H., Cado D., Dietrich W.F., Monack D.M., Tsolis R.M., Vance R E.: Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat. Immunol., 2008; 9: 1171-1178
Open DOI Search in Google Scholar Back to article
Rothmeier E., Pfaffinger G., Hoffmann C., Harrison C.F., Grabmayr H., Repnik U., Hannemann M., Wölke S., Bausch A., Griffiths G. i wsp.: Activation of Ran GTPase by a Legionella effector promotes microtubule polymerization, pathogen vacuole motility and infection. PLoS Pathog., 2013; 9: e1003598
Open DOI Search in Google Scholar Back to article
Shen X., Banga S., Liu Y., Xu L., Gao P., Shamovsky I., Nudler E., Luo Z.Q.: Targeting eEF1A by a Legionella pneumophila effector leads to inhibition of protein synthesis and induction of host stress response. Cell. Microbiol., 2009; 11: 911-926
Open DOI Search in Google Scholar Back to article
Derré I., Isberg R.R.: Legionella pneumophila replication vacuole formation involves rapid recruitment of proteins of the early secretory system. Infect. Immun., 2004; 72: 3048-3053
Open DOI Search in Google Scholar Back to article
Ingmundson A., Delprato A., Lambright D.G., Roy C.R.: Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature, 2007; 450: 365-369
Open DOI Search in Google Scholar Back to article
Machner M.P., Isberg R.R.: A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science, 2007; 318: 974977
Open DOI Search in Google Scholar Back to article
Shin S., Case C.L., Archer K.A., Nogueira C.V., Kobayashi K.S., Flavell R.A., Roy C.R., Zamboni D.S.: Type IV secretion-dependent activation of host MAP kinases induces an increased proinflammatory cytokine response to Legionella pneumophila. PLoS Pathog., 2008; 4: e1000220
Open DOI Search in Google Scholar Back to article
Pan X., Lührmann A., Satoh A., Laskowski-Arce M.A., Roy C.R.: Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science, 2008; 320: 1651-1654
Open DOI Search in Google Scholar Back to article
Purcell M., Shuman H.A.: The Legionella pneumophila icmGCD-JBF genes are required for killing of human macrophages. Infect. Immun., 1998; 66: 2245-2255
Open DOI Search in Google Scholar Back to article
Qiu J., Sheedlo M.J., Yu K., Tan Y., Nakayasu E.S., Das C., Liu X., Luo Z.Q.: Ubiquitination independent of E1 and E2 enzymes by bacterial effectors. Nature, 2016; 533: 120-124
Open DOI Search in Google Scholar Back to article
Steiner B., Swart A.L., Welin A., Weber S., Personnic N., Kaech A., Freyre C., Ziegler U., Klemm R.W., Hilbi H.: ER remodeling by the large GTPase atlastin promotes vacuolar growth of Legionella pneumophila. EMBO Rep., 2017; 18: 1817-1836
Open DOI Search in Google Scholar Back to article
Escoll P., Song O.R., Viana F., Steiner B., Lagache T., Olivo-Marin J.C., Impens F., Brodin P., Hilbi H., Buchrieser C.: Legionella pneumophila modulates mitochondrial dynamics to trigger metabolic repurposing of infected macrophages. Cell. Host Microbe, 2017; 22: 302-316.e7
Open DOI Search in Google Scholar Back to article
Machner M.P., Isberg R.R.: Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev. Cell., 2006; 11: 47-56
Open DOI Search in Google Scholar Back to article
Amor J.C., Swails J., Zhu X., Roy C.R., Nagai H., Ingmundson A., Cheng X., Kahn R.A.: The structure of RalF, an ADP-ribosylation factor guanine nucleotide exchange factor from Legionella pneumophila, reveals the presence of a cap over the active site. J. Biol. Chem., 2005; 280: 1392-1400
Open DOI Search in Google Scholar Back to article
Meir A., Chetrit D., Liu L., Roy C.R., Waksman G.: Legionella DotM structure reveals a role in effector recruiting to the Type 4B secretion system. Nat. Commun., 2018; 9: 507
Open DOI Search in Google Scholar Back to article
Nagai H., Kagan J.C., Zhu X., Kahn R.A., Roy C.R.: A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science, 2002; 295: 679-682
Open DOI Search in Google Scholar Back to article
Brombacher E., Urwyler S., Ragaz C., Weber S.S., Kami K., Overduin M., Hilbi H.: Rab1 guanine nucleotide exchange factor SidM is a major phosphatidylinositol 4-phosphate-binding effector protein of Legionella pneumophila. J. Biol. Chem., 2009; 284: 4846-4856
Open DOI Search in Google Scholar Back to article
Chen J., Reyes M., Clarke M., Shuman H.A.: Host cell-dependent secretion and translocation of the LepA and LepB effectors of Legionella pneumophila. Cell. Microbiol., 2007; 9: 1660-1671
Open DOI Search in Google Scholar Back to article
Conover G.M., Derré I., Vogel J.P., Isberg R.R.: The Legionella pneumophila LidA protein: A translocated substrate of the Dot/Icm system associated with maintenance of bacterial integrity. Mol. Microbiol., 2003; 48: 305-321
Open DOI Search in Google Scholar Back to article
Choy A., Dancourt J., Mugo B., O’Connor T.J., Isberg R.R., Melia T.J., Roy C.R.: The Legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation. Science, 2012; 338: 1072-1076
Open DOI Search in Google Scholar Back to article
Creasey E.A., Isberg R.R.: The protein SdhA maintains the integrity of the Legionella-containing vacuole. Proc. Natl. Acad. Sci. USA, 2012: 109: 3481-3486
Open DOI Search in Google Scholar Back to article
Banga S., Gao P., Shen X., Fiscus V., Zong W.X., Chen L., Luo Z.Q.: Legionella pneumophila inhibits macrophage apoptosis by targeting pro-death members of the Bcl2 protein family. Proc. Natl. Acad. Sci. USA, 2007; 104: 5121-5126
Open DOI Search in Google Scholar Back to article
Gan N., Nakayasu E.S., Hollenbeck P.J., Luo Z.Q.: Legionella pneumophila inhibits immune signalling via MavC-mediated transglutaminase-induced ubiquitination of UBE2N. Nat. Microbiol., 2019; 4: 134-143
Open DOI Search in Google Scholar Back to article
Losick V.P., Haenssler E., Moy M.Y., Isberg R.R.: LnaB: A Legionella pneumophila activator of NF-κB. Cell. Microbiol., 2010: 12: 1083-1097
Open DOI Search in Google Scholar Back to article
Ge J., Xu H., Li T., Zhou Y., Zhang Z., Li S., Liu L., Shao F.: A Legionella type IV effector activates the NF-κB pathway by phosphorylating the IκB family of inhibitors. Proc. Natl. Acad. Sci. USA, 2009; 106: 13725-13730
Open DOI Search in Google Scholar Back to article
Ivanov S.S., Roy C.R.: Modulation of ubiquitin dynamics and suppression of DALIS formation by the Legionella pneumophila Dot/ Icm system. Cell. Microbiol., 2009; 11: 261-278
Open DOI Search in Google Scholar Back to article
Fontana M.F., Banga S., Barry K.C., Shen X., Tan Y., Luo Z.Q., Vance R.E.: Secreted bacterial effectors that inhibit host protein synthesis are critical for induction of the innate immune response to virulent Legionella pneumophila. PLoS Pathog., 2011; 7: e1001289
Open DOI Search in Google Scholar Back to article
Joseph A.M., Pohl A., Ball T.J., Abram T.G., Johnson D.K., Geisbrecht B.V., Shames S.R.: The Legionella pneumophila metaef-fector Lpg2505 (MesI) regulates SidI-mediated translation inhibition and novel glycosyl hydrolase activity. Infect. Immun., 2020; 88: e00853-19
Open DOI Search in Google Scholar Back to article
Belyi Y., Niggeweg R., Opitz B., Vogelsgesang M., Hippenstiel S., Wilm M., Aktories K.: Legionella pneumophila glucosyl transfer-ase inhibits host elongation factor 1A. Proc. Natl. Acad. Sci. USA, 2006; 103: 16953-16958
Open DOI Search in Google Scholar Back to article
Silverman P.M., Clarke M.B.: New insights into F-pilus structure, dynamics, and function. Integr. Biol., 2010; 2: 25-31
Open DOI Search in Google Scholar Back to article

Articles in this issue

DOI: https://doi.org/10.2478/ahem-2021-0023 | Journal eISSN: 1732-2693

Journal RSS Feed

Language: English, Polish

Page range: 548 - 562

Submitted on: Sep 19, 2020

Accepted on: Feb 24, 2021

Published on: Oct 21, 2021

Published by: Hirszfeld Institute of Immunology and Experimental Therapy

In partnership with: Paradigm Publishing Services

Publication frequency: 1 issue per year

Keywords:

Legionella pneumophila,

intracellular pathogens,

Dot/Icm secretion system,

replication vacuole,

Legionnaires’ disease

Related subjects:

Life sciences,

Molecular biology,

Microbiology and virology,

Medicine,

Basic medical science,

Immunology

© 2021 Bożena Kowalczyk, Agata Małek, Marta Palusińska-Szysz, published by Hirszfeld Institute of Immunology and Experimental Therapy
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.

Volume 75 (2021): Issue 1 (January 2021)