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3. Legionella pneumophila subversion of host vesicular transport by SidC effector proteins.

Author

Horenkamp, Florian A, Mukherjee, Shaeri, Alix, Eric, Schauder, Curtis M, Hubber, Andree M, Roy, Craig R, and Reinisch, Karin M

Subjects
Vacuoles, Legionella pneumophila, rab1 GTP-Binding Proteins, Bacterial Proteins, Crystallography, X-Ray, Amino Acid Sequence, Biological Transport, Molecular Sequence Data, Ubiquitination, Rab1 modification, Tethering, Rare Diseases, Pneumonia, Pneumonia & Influenza, Infectious Diseases, Lung, Aetiology, 2.1 Biological and endogenous factors, Infection, Biochemistry and Cell Biology, Medical Microbiology, Developmental Biology
Abstract

Tethering proteins play a key role in vesicular transport, ensuring that cargo arrives at a specific destination. The bacterial effector protein SidC and its paralog SdcA have been described as tethering factors encoded by the intracellular pathogen Legionella pneumophila. Here, we demonstrate that SidC proteins are important for early events unique to maturation of vacuoles containing Legionella and discover monoubiquitination of Rab1 as a new SidC-dependent activity. The crystal structure of the SidC N-terminus revealed a novel fold that is important for function and could be involved in Legionella adaptations to evolutionarily divergent host cells it encounters in natural environments.

Published
2014

5. Subversion of Host Membrane Dynamics by the Legionella Dot/Icm Type IV Secretion System

Author

Hilbi, Hubert, Nagai, Hiroki, Kubori, Tomoko, Roy, Craig R., Compans, Richard W, Series Editor, Malissen, Bernard, Series Editor, Aktories, Klaus, Series Editor, Rappuoli, Rino, Series Editor, Galan, Jorge E., Series Editor, Ahmed, Rafi, Series Editor, Palme, Klaus, Series Editor, Casadevall, Arturo, Series Editor, Garcia-Sastre, Adolfo, Series Editor, Iwasaki, Akiko, Series Editor, Akira, Shizuo, Series Editor, Backert, Steffen, editor, and Grohmann, Elisabeth, editor

Published
2017
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6. Structure of the Legionella effector AnkX reveals the mechanism of phosphocholine transfer by the FIC domain.

Author

Campanacci, Valérie, Mukherjee, Shaeri, Roy, Craig R, and Cherfils, Jacqueline

Subjects
Legionella pneumophila, Phosphorylcholine, Bacterial Proteins, Crystallography, X-Ray, Catalytic Domain, Ankyrin Repeat, Protein Conformation, Protein Structure, Tertiary, Models, Molecular, Infectious Diseases, Infection, Biological Sciences, Information and Computing Sciences, Medical and Health Sciences, Developmental Biology
Abstract

The FIC motif and the eukaryotic-like ankyrin repeats are found in many bacterial type IV effectors, yet little is known about how these domains enable bacteria to modulate host cell functions. Bacterial FIC domains typically bind ATP and transfer adenosine monophosphate moiety onto target proteins. The ankyrin repeat-containing protein AnkX encoded by the intracellular pathogen Legionella pneumophila is unique in that its FIC domain binds to CDP-choline and transfers a phosphocholine residue onto proteins in the Rab1 GTPase family. By determining the structures of unbound AnkX and AnkX with bound CDP-choline, CMP/phosphocholine and CMP, we demonstrate that the orientation of substrate binding in relation to the catalytic FIC motif enables this protein to function as a phosphocholinating enzyme rather than a nucleotidyl transferase. Additionally, the structure reveals that the ankyrin repeats mediate scaffolding interactions that resemble those found in protein-protein interactions, but are unprecedented in intramolecular interactions. Together with phosphocholination experiments, our structures unify a general phosphoryl transferase mechanism common to all FIC enzymes that should be conserved from bacteria to human.

Published
2013

7. CPAF: A Chlamydial Protease in Search of an Authentic Substrate

Author

Chen, Allan L, Johnson, Kirsten A, Lee, Jennifer K, Sütterlin, Christine, Tan, Ming, and Roy, Craig R

Subjects
trachomatis-infected cells, junction molecule nectin-1, genital epithelial-cells, secreted protease, chlamydophila-pneumoniae, protective immunity, bh3-only proteins, host, degradation, inhibition
Published
2012

8. Modulation of Rab GTPase function by a protein phosphocholine transferase.

Author

Mukherjee, Shaeri, Liu, Xiaoyun, Arasaki, Kohei, McDonough, Justin, Galán, Jorge E, and Roy, Craig R

Subjects
COS Cells, Animals, Humans, Legionella pneumophila, Legionnaires' Disease, rab GTP-Binding Proteins, Diacylglycerol Cholinephosphotransferase, Guanine Nucleotide Exchange Factors, Bacterial Proteins, Protein Processing, Post-Translational, Mass Spectrometry, Host-Pathogen Interactions, HEK293 Cells, Chlorocebus aethiops, General Science & Technology
Abstract

The intracellular pathogen Legionella pneumophila modulates the activity of host GTPases to direct the transport and assembly of the membrane-bound compartment in which it resides. In vitro studies have indicated that the Legionella protein DrrA post-translationally modifies the GTPase Rab1 by a process called AMPylation. Here we used mass spectrometry to investigate post-translational modifications to Rab1 that occur during infection of host cells by Legionella. Consistent with in vitro studies, DrrA-mediated AMPylation of a conserved tyrosine residue in the switch II region of Rab1 was detected during infection. In addition, a modification to an adjacent serine residue in Rab1 was discovered, which was independent of DrrA. The Legionella effector protein AnkX was required for this modification. Biochemical studies determined that AnkX directly mediates the covalent attachment of a phosphocholine moiety to Rab1. This phosphocholine transferase activity used CDP-choline as a substrate and required a conserved histidine residue located in the FIC domain of the AnkX protein. During infection, AnkX modified both Rab1 and Rab35, which explains how this protein modulates membrane transport through both the endocytic and exocytic pathways of the host cell. Thus, phosphocholination of Rab GTPases represents a mechanism by which bacterial FIC-domain-containing proteins can alter host-cell functions.

Published
2011

23. Proteins DotY and DotZ modulate the dynamics and localization of the type IVB coupling complex of Legionella pneumophila

Author

Macé, Kevin, Meir, Amit, Lukoyanova, Natalya, Liu, Luying, Chetrit, David, Hospenthal, Manuela K., Roy, Craig R., and Waksman, Gabriel

Subjects
type 4 secretion system, coupling complex, recruitment platform, effector recruitment, Legionella pneumophila, bcs
Abstract

Legionella pneumophila is an opportunistic pathogen infecting alveolar macrophages and protozoa species. Legionella utilizes a Type IV Secretion System (T4SS) to translocate over 300 effector proteins into its host cell. In a recent study, we have isolated and solved the cryo-EM structure of the Type IV Coupling Complex (T4CC), a large cytoplasmic determinant associated with the inner membrane that recruits effector proteins for delivery to the T4SS for translocation. The T4CC is composed of a DotLMNYZ hetero-pentameric core from which the flexible IcmSW module flexibly protrudes. The DotY and DotZ proteins were newly reported members of this complex and their role remained elusive. In this study, we observed the effect of deleting DotY and DotZ on T4CC stability and localization. Furthermore, we found these two proteins are co-dependent, whereby the deletion of DotY resulted in DotZ absence from the coupling complex, and vice versa. Additional cryo-EM data analysis revealed the dynamic movement of the IcmSW module is modified by the DotY/Z proteins. We therefore determined the likely function of DotY and DotZ and revealed their importance on T4CC function., Molecular Microbiology, 117 (2), ISSN:0950-382x, ISSN:1365-2958

Published
2022

28. Contributors

Author

Aagaard, Kjersti, primary, Abrahamian, Fredrick M., additional, Allos, Ban Mishu, additional, Andes, David R., additional, Aoki, Fred Y., additional, Apicella, Michael A., additional, Ard, Kevin L., additional, Arias, Cesar A., additional, Aronoff, David M., additional, Augenbraun, Michael H., additional, Averhoff, Francisco, additional, Azar, Dimitri T., additional, Baddour, Larry M., additional, Baden, Lindsey R., additional, Baker, Carol J., additional, Ballard, Ronald C., additional, Barber, Gerard R., additional, Barnes, Scott D., additional, Barouch, Dan H., additional, Barrett, Alan D., additional, Barshak, Miriam Baron, additional, Basavaraju, Sridhar V., additional, Batteiger, Byron E., additional, Baum, Stephen G., additional, Bayer, Arnold S., additional, Beckham, J. David, additional, Beekmann, Susan E., additional, Bell, Beth P., additional, Bennett, John E., additional, Bente, Dennis A., additional, Berbari, Elie F., additional, Berman, Jonathan, additional, Bertino, Joseph S., additional, Bhimraj, Adarsh, additional, Birdsall, Holly H., additional, Bisno, Alan L., additional, Blackburn, Brian G., additional, Blanton, Lucas S., additional, Blaser, Martin J., additional, Bleck, Thomas P., additional, Blijlevens, Nicole M.A., additional, Bobak, David A., additional, Bonnez, William, additional, Boothroyd, John C., additional, Borio, Luciana L., additional, Bosque, Patrick J., additional, Bower, John, additional, Bradsher, Robert W., additional, Brook, Itzhak, additional, Brown, Kevin E., additional, Brown, Patricia D., additional, Brown-Elliott, Barbara A., additional, Bruhn, Roberta L., additional, Bryant, Amy E., additional, Burd, Eileen M., additional, Burns, Jane C., additional, Bush, Larry M., additional, Calderwood, Stephen B., additional, Cano, Luz Elena, additional, Carpenter, Charles C.J., additional, Caserta, Mary T., additional, Castagnola, Elio, additional, Chaisson, Richard E., additional, Chambers, Henry F., additional, Chapman, Stephen J., additional, Chappell, James D., additional, Chen, Lea Ann, additional, Chen, Sharon C-A, additional, Chow, Anthony W., additional, Clark, Rebecca A., additional, Cohen, Jeffrey I., additional, Cohen, Myron S., additional, Cohen-Poradosu, Ronit, additional, Cohn, Susan E., additional, Connors, Mark, additional, Corey, Lawrence, additional, Cottrell, Mackenzie L., additional, Cover, Timothy L., additional, Cox, Heather L., additional, Craig, William A., additional, Crossley, Kent B., additional, Crumpacker, Clyde S., additional, Curran, James W., additional, Currie, Bart J., additional, D'Agata, Erika, additional, Damon, Inger K., additional, Darouiche, Rabih O., additional, DeBiasi, Roberta L., additional, Deepe, George S., additional, del Rio, Carlos, additional, Delemos, Andrew S., additional, DeLeo, Frank R., additional, DeMuri, Gregory P., additional, Densen, Peter, additional, Dermody, Terence S., additional, Dewar, Robin, additional, Diaz, James H., additional, Dieffenbach, Carl W., additional, Dienstag, Jules L., additional, Doi, Yohei, additional, Dolin, Raphael, additional, Donnelly, J. Peter, additional, Donnenberg, Michael S., additional, Donowitz, Gerald R., additional, Dormitzer, Philip R., additional, Drake, James M., additional, Dumler, J. Stephen, additional, Dummer, J. Stephen, additional, DuPont, Herbert L., additional, Durack, David T., additional, Durand, Marlene L., additional, Edelstein, Paul H., additional, Edmond, Michael B., additional, Edwards, John E., additional, Edwards, Morven S., additional, Eliopoulos, George M., additional, Ellison, Richard T., additional, Endy, Timothy P., additional, Engleberg, N. Cary, additional, Erdem, Hakan, additional, Ernst, Joel D., additional, Ernst, Peter B., additional, Fairhurst, Rick M., additional, Fairley, Jessica K., additional, Falkow, Stanley, additional, Falsey, Ann R., additional, Fauci, Anthony S., additional, Fekete, Thomas, additional, Fey, Paul D., additional, Fine, Steven M., additional, Fitzgerald, Daniel W., additional, Flores, Anthony R., additional, Forster, Derek, additional, Fowler, Vance G., additional, Freedman, David O., additional, Friedlander, Arthur M., additional, Galgiani, John N., additional, Gallin, John I., additional, Gallo, Robert C., additional, Gandhi, Tejal N., additional, Garrett, Wendy S., additional, Gaydos, Charlotte A., additional, Geisbert, Thomas W., additional, Gelfand, Jeffrey A., additional, Gelone, Steven P., additional, Gerding, Dale N., additional, Gershon, Anne A., additional, Gilsdorf, Janet R., additional, Goldstein, Ellie J.C., additional, Gordin, Fred M., additional, Graman, Paul S., additional, Grayson, M. Lindsay, additional, Greene, Jeffrey Bruce, additional, Griffin, Patricia M., additional, Griffith, David E., additional, Guerrant, Richard L., additional, Gul, H. Cem, additional, Haake, David A., additional, Haas, David W., additional, Haines, Charles, additional, Hall, Caroline Breese, additional, Hallak, Joelle, additional, Halperin, Scott A., additional, Hammerschlag, Margaret R., additional, Haque, Rashidul, additional, Harris, Jason B., additional, Hawkins, Claudia, additional, Hay, Roderick J., additional, Hedberg, Craig W., additional, Henderson, David K., additional, Henderson, Donald A., additional, High, Kevin P., additional, Hill, Adrian V.S., additional, Hill, David R., additional, Hinman, Alan R., additional, Hirsch, Martin S., additional, Hodowanec, Aimee, additional, Hohl, Tobias M., additional, Holland, Steven M., additional, Holzman, Robert S., additional, Hook, Edward W., additional, Hooper, David C., additional, Hooton, Thomas M., additional, Horowitz, Harold W., additional, Horsburgh, C. Robert, additional, Horton, James M., additional, Hospenthal, Duane R., additional, Hsueh, Kevin, additional, Hughes, James M., additional, Hynes, Noreen A., additional, Iovine, Nicole M., additional, Iredell, Jonathan R., additional, Ison, Michael G., additional, Janda, J. Michael, additional, Janoff, Edward N., additional, Johannsen, Eric C., additional, Kashuba, Angela D.M., additional, Kasper, Dennis L., additional, Kaye, Donald, additional, Kaye, Keith S., additional, Kaye, Kenneth M., additional, Kazura, James W., additional, Keystone, Jay S., additional, Khabbaz, Rima, additional, Khan, David A., additional, Khudyakov, Yury, additional, Kim, Rose, additional, King, Charles H., additional, Kirchhoff, Louis V., additional, Klein, Jerome O., additional, Klompas, Michael, additional, Knoll, Bettina M., additional, Knowlton, Kirk U., additional, Koehler, Jane E., additional, Kohlhoff, Stephan A., additional, Könönen, Eija, additional, Kontoyiannis, Dimitrios P., additional, Koralnik, Igor J., additional, Korpe, Poonum S., additional, Koshy, Anita A., additional, Kovacs, Joseph A., additional, Kozarsky, Phyllis, additional, Krieger, John, additional, Kroger, Andrew T., additional, Kuehnert, Matthew J., additional, Kumar, Nalin M., additional, Kuruvilla, Merin Elizabeth, additional, LaRocque, Regina C., additional, Leggett, James E., additional, Legido-Quigley, Helena, additional, Levett, Paul N., additional, Levine, Donald P., additional, Levison, Matthew E., additional, Levitt, Alexandra, additional, Lewis, Russell E., additional, Liles, W. Conrad, additional, Lima, Aldo A.M., additional, Limaye, Ajit P., additional, Lipkin, W. Ian, additional, Litman, Nathan, additional, Lorber, Bennett, additional, Luna, Ruth Ann, additional, MacDougall, Conan, additional, Roy, Rob, additional, Mackowiak, Philip A., additional, Madoff, Lawrence C., additional, Magill, Alan J., additional, Maguire, James H., additional, Maldarelli, Frank, additional, Markoff, Lewis, additional, Marrazzo, Jeanne M., additional, Marrie, Thomas J., additional, Marth, Thomas, additional, Martin, David H., additional, Martin, Gregory J., additional, Marty, Francisco M., additional, Maslow, Melanie Jane, additional, Masur, Henry, additional, Mawle, Alison, additional, Mayer, Kenneth H., additional, McBride, John T., additional, McCarthy, James S., additional, McCormack, William M., additional, McGowan, Catherine C., additional, McIntosh, Kenneth, additional, Mead, Paul S., additional, Mikulska, Malgorzata, additional, Miller, Robert F., additional, Miller, Samuel I., additional, Mitchell, David H., additional, Modlin, John F., additional, Mody, Rajal K., additional, Moellering, Robert C., additional, Moffa, Matthew, additional, Moir, Susan, additional, Montoya, José G., additional, Moore, Thomas A., additional, Moreillon, Philippe, additional, Morris, J. Glenn, additional, Morse, Caryn Gee, additional, Moseley, Robin, additional, Munford, Robert S., additional, Murphy, Edward L., additional, Murphy, Timothy F., additional, Murray, Barbara E., additional, Murray, Clinton K., additional, Murray, Patrick R., additional, Musher, Daniel M., additional, Nagel, Jerod L., additional, Nannini, Esteban C., additional, Narezkina, Anna, additional, Nash, Theodore E., additional, Nauseef, William M., additional, Nayak, Jennifer L., additional, Neill, Marguerite A., additional, O'Donnell, Judith A., additional, Ohl, Christopher A., additional, Okhuysen, Pablo C., additional, Onderdonk, Andrew B., additional, Opal, Steven M., additional, Orenstein, Walter A., additional, Osmon, Douglas R., additional, Osterholm, Michael T., additional, Ostroff, Stephen M., additional, Oxman, Michael N., additional, Paessler, Slobodan, additional, Page, Andrea V., additional, Pai, Manjunath P., additional, Palmore, Tara N., additional, Palraj, Raj, additional, Pappas, Peter G., additional, Pasternack, Mark S., additional, Patterson, Thomas F., additional, Pavan-Langston, Deborah, additional, Pegues, David A., additional, Penn, Robert L., additional, Perfect, John R., additional, Perlman, Stanley, additional, Petersen, Brett W., additional, Peterson, Phillip K., additional, Petri, William A., additional, Petti, Cathy A., additional, Philips, Jennifer A., additional, Philley, Julie V., additional, Phillips, Michael, additional, Pickering, Larry K., additional, Piot, Peter, additional, Pogue, Jason M., additional, Pop-Vicas, Aurora, additional, Portal-Celhay, Cynthia, additional, Powers, John H., additional, Price, Richard N., additional, Que, Yok-Ai, additional, Radolf, Justin D., additional, Ram, Sanjay, additional, Raoult, Didier, additional, Ravdin, Jonathan I., additional, Ray, Stuart C., additional, Reboli, Annette C., additional, Reitz, Marvin S., additional, Relman, David A., additional, Renault, Cybèle A., additional, Restrepo, Angela, additional, Rex, John H., additional, Rhee, Elizabeth G., additional, Roberts, Norbert J., additional, Romero, José R., additional, Rothman, Alan L., additional, Roy, Craig R., additional, Ruoff, Kathryn L., additional, Rupp, Mark E., additional, Rupprecht, Charles E., additional, Russo, Thomas A., additional, Rutala, William A., additional, Ryan, Edward T., additional, Safdar, Amar, additional, Sajadi, Mohammad M., additional, Salazar, Juan C., additional, Sarria, Juan Carlos, additional, Savoia, Maria C., additional, Sax, Paul E., additional, Scheld, W. Michael, additional, Schiffer, Joshua T., additional, Schlossberg, David, additional, Schneider, Thomas, additional, Schuchat, Anne, additional, Schwebke, Jane R., additional, Sears, Cynthia L., additional, Segal, Leopoldo N., additional, Sendi, Parham, additional, Sepkowitz, Kent A., additional, Septimus, Edward J., additional, Seregin, Alexey, additional, Shulman, Stanford T., additional, Siberry, George K., additional, Siddiqi, Omar K., additional, Sifri, Costi D., additional, Simberkoff, Michael S., additional, Simonetti, Francesco R., additional, Singh, Kamaljit, additional, Singh, Nina, additional, Singh, Upinder, additional, Sinner, Scott W., additional, Sivapalasingam, Sumathi, additional, Slater, Leonard N., additional, Smulian, A. George, additional, Sobel, Jack D., additional, Sohail, M. Rizwan, additional, Soper, David E., additional, Sorrell, Tania C., additional, Steckelberg, James M., additional, Steere, Allen C., additional, Steigbigel, Neal H., additional, Steinberg, James P., additional, Stephens, David S., additional, Sterling, Timothy R., additional, Stevens, David A., additional, Stevens, Dennis L., additional, Strahilevitz, Jacob, additional, Stratton, Charles W., additional, Suffredini, Anthony F., additional, Suh, Kathryn N., additional, Sulkowski, Mark S., additional, Swartz, Morton N., additional, Talbot, Thomas R., additional, Tan, C. Sabrina, additional, Tan, Ming, additional, Thio, Chloe Lynne, additional, Thomas, David L., additional, Thomas, Lora D., additional, Thomas, Stephen J., additional, Thorner, Anna R., additional, María Tobón, Angela, additional, Tramont, Edmund C., additional, Treanor, John J., additional, Trubiano, Jason, additional, Tsibris, Athe M.N., additional, Tunkel, Allan R., additional, Turner, Ronald B., additional, Tyler, Kenneth L., additional, Uluer, Ahmet, additional, van de Beek, Diederik, additional, van der Velden, Walter J.F.M., additional, Vannier, Edouard G., additional, Van, Trevor C., additional, Versalovic, James, additional, Viscoli, Claudio, additional, Wald, Ellen R., additional, Waldor, Matthew K., additional, Walker, David H., additional, Wallace, Richard J., additional, Walsh, Edward E., additional, Walsh, Stephen R., additional, Walzer, Peter D., additional, Wanke, Christine A., additional, Warren, Cirle A., additional, Washburn, Ronald G., additional, Waters, Valerie, additional, Weber, David J., additional, Weiden, Michael D., additional, Weinberg, Geoffrey A., additional, Weisdorf, Daniel J., additional, Weiss, Louis M., additional, Welch, David F., additional, Wellems, Thomas E., additional, Wenzel, Richard P., additional, Wharton, Melinda, additional, White, A. Clinton, additional, Whitley, Richard J., additional, Wilson, Walter R., additional, Wortmann, Glenn W., additional, Wright, William F., additional, Young, Jo-Anne H., additional, Young, Vincent B., additional, Yun, Nadezhda, additional, Zimmerli, Werner, additional, Zinner, Stephen H., additional, and Zurlo, John J., additional

Published
2015
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42. Cellular hijacking: a common strategy for microbial infection

Author

Kahn, Richard A., Fu, Haian, and Roy, Craig R.

Subjects
Biochemistry -- Research, Eukaryotic cells -- Research, Biological sciences, Chemistry
Abstract

Eukaryotic cells are under constant attack from microbial intruders seeking a selective advantage for survival, propagation and dissemination. Microbial infections can often result in disease and might even be lethal to the host if they are not combated effectively. Studies of host-pathogen interactions have revealed that virulence often requires the usurpation of existing cell signaling pathways or membrane traffic machinery of the host. Such studies provide a rich source of cell biological data that will probably prove essential for future efforts designed to either thwart these attacks or learn from them.

Published
2002

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