Legionella pneumophila modulates host energy metabolism by ADP-ribosylation of ADP/ATP translocases

Fu, Jiaqi; Zhou, Mowei; Gritsenko, Marina A.; Nakayasu, Ernesto S.; Song, Lei; Luo, Zhao-Qing

doi:10.7554/eLife.73611

Title: Legionella pneumophila modulates host energy metabolism by ADP-ribosylation of ADP/ATP translocases

Journal Article · 26 January 2022 · eLife

DOI: https://doi.org/10.7554/eLife.73611 · OSTI ID:1854915

Fu, Jiaqi ^[1];

^[2];

^[2]; Song, Lei ^[3]; Luo, Zhao-Qing ^[1]

Purdue Univ., West Lafayette, IN (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Jilin Univ., Changchun (China). The First Hospital, Center of Pathogen Biology and Infectious Diseases, Key Lab. of Organ Regeneration and Transplantation, State Key Lab. of Zoonotic Diseases

The intracellular pathogen Legionella pneumophila delivers more than 330 effectors into host cells by its Dot/Icm type IV secretion system. Those effectors are essential for the biogenesis of the Legionella-containing vacuole (LCV) that permits its intracellular survival and replication. It has long been documented that the LCV is associated with mitochondria and a number of Dot/Icm effectors have been shown to target to this organelle. Yet, the biochemical function and host cell target of most of these effectors remain unknown. Here, we found that the Dot/Icm substrate Ceg3 (Lpg0080) is a mono-ADP-ribosyltransferase that localizes to the mitochondria in host cells where it attacks ADP/ATP translocases (ANTs) by ADP-ribosylation and blunts their ADP/ATP exchange activity. The modification occurs on the second arginine residue in the -RRRMMM- element, which is conserved among all known ADP/ATP carriers from different organisms. Our results reveal modulation of host energy metabolism as a novel virulence mechanism for L. pneumophila.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE; National Institutes of Health (NIH)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1854915

Report Number(s):: PNNL-SA-165115

Journal Information:: eLife, Journal Name: eLife Vol. 11; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

References (74)

Production and Titration of Lentiviral Vectors Salmon, Patrick; Trono, Didier Current Protocols in Human Genetics, Vol. 54, Issue 1 https://doi.org/10.1002/0471142905.hg1210s54	journal	July 2007
Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure Gietz, R. Daniel; Schiestl, Robert H.; Willems, Andrew R. Yeast, Vol. 11, Issue 4, p. 355-360 https://doi.org/10.1002/yea.320110408	journal	April 1995
Site-directed Mutagenesis of the Yeast Mitochondrial ADP/ATP Translocator Nelson, David R.; Lawson, Janet E.; Klingenberg, Martin Journal of Molecular Biology, Vol. 230, Issue 4 https://doi.org/10.1006/jmbi.1993.1233	journal	April 1993
Refined localization of the pyruvate dehydrogenase E1α gene (PDHA1) by linkage analysis Børglum, A. D.; Flint, Tracey; Hansen, Lise Lotte Human Genetics, Vol. 99, Issue 1 https://doi.org/10.1007/s004390050315	journal	December 1996
ADP-ribosylation of arginine Laing, Sabrina; Unger, Mandy; Koch-Nolte, Friedrich Amino Acids, Vol. 41, Issue 2 https://doi.org/10.1007/s00726-010-0676-2	journal	July 2010
Unspecific permeation and specific exchange of adenine nucleotides in liver mitochondria Pfaff, E.; Klingenberg, M.; Heldt, H. W. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 104, Issue 1 https://doi.org/10.1016/0304-4165(65)90258-8	journal	June 1965
Diphtheria Toxin-dependent Adenosine Diphosphate Ribosylation of Aminoacyl Transferase II and Inhibition of Protein Synthesis Honjo, T.; Nishizuka, Y.; Hayaishi, O. Journal of Biological Chemistry, Vol. 243, Issue 12 https://doi.org/10.1016/S0021-9258(18)93347-8	journal	June 1968
Mitochondrial membrane potential Zorova, Ljubava D.; Popkov, Vasily A.; Plotnikov, Egor Y. Analytical Biochemistry, Vol. 552 https://doi.org/10.1016/j.ab.2017.07.009	journal	July 2018
The peripheral stalk of the mitochondrial ATP synthase Walker, John E.; Dickson, Veronica Kane Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 5-6 https://doi.org/10.1016/j.bbabio.2006.01.001	journal	May 2006
The ADP and ATP transport in mitochondria and its carrier Klingenberg, Martin Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1778, Issue 10 https://doi.org/10.1016/j.bbamem.2008.04.011	journal	October 2008
Mitochondria: A target for bacteria Lobet, Elodie; Letesson, Jean-Jacques; Arnould, Thierry Biochemical Pharmacology, Vol. 94, Issue 3 https://doi.org/10.1016/j.bcp.2015.02.007	journal	April 2015
Phosphoribosylation of Ubiquitin Promotes Serine Ubiquitination and Impairs Conventional Ubiquitination Bhogaraju, Sagar; Kalayil, Sissy; Liu, Yaobin Cell, Vol. 167, Issue 6 https://doi.org/10.1016/j.cell.2016.11.019	journal	December 2016
The Molecular Mechanism of Transport by the Mitochondrial ADP/ATP Carrier Ruprecht, Jonathan J.; King, Martin S.; Zögg, Thomas Cell, Vol. 176, Issue 3 https://doi.org/10.1016/j.cell.2018.11.025	journal	January 2019
A Bacterial Effector Reveals the V-ATPase-ATG16L1 Axis that Initiates Xenophagy Xu, Yue; Zhou, Ping; Cheng, Sen Cell, Vol. 178, Issue 3 https://doi.org/10.1016/j.cell.2019.06.007	journal	July 2019
What Pathogens Have Taught Us About Posttranslational Modifications Salomon, Dor; Orth, Kim Cell Host & Microbe, Vol. 14, Issue 3 https://doi.org/10.1016/j.chom.2013.07.008	journal	September 2013
Vibrio cholerae T3SS Effector VopE Modulates Mitochondrial Dynamics and Innate Immune Signaling by Targeting Miro GTPases Suzuki, Masato; Danilchanka, Olga; Mekalanos, John J. Cell Host & Microbe, Vol. 16, Issue 5 https://doi.org/10.1016/j.chom.2014.09.015	journal	November 2014
A Single Legionella Effector Catalyzes a Multistep Ubiquitination Pathway to Rearrange Tubular Endoplasmic Reticulum for Replication Kotewicz, Kristin M.; Ramabhadran, Vinay; Sjoblom, Nicole Cell Host & Microbe, Vol. 21, Issue 2 https://doi.org/10.1016/j.chom.2016.12.007	journal	February 2017
Pseudomonas aeruginosa Effector ExoS Inhibits ROS Production in Human Neutrophils Vareechon, Chairut; Zmina, Stephanie Elizabeth; Karmakar, Mausita Cell Host & Microbe, Vol. 21, Issue 5 https://doi.org/10.1016/j.chom.2017.04.001	journal	May 2017
Legionella pneumophila Modulates Mitochondrial Dynamics to Trigger Metabolic Repurposing of Infected Macrophages Escoll, Pedro; Song, Ok-Ryul; Viana, Flávia Cell Host & Microbe, Vol. 22, Issue 3 https://doi.org/10.1016/j.chom.2017.07.020	journal	September 2017
The Legionella Effector Kinase LegK7 Hijacks the Host Hippo Pathway to Promote Infection Lee, Pei-Chung; Machner, Matthias P. Cell Host & Microbe, Vol. 24, Issue 3 https://doi.org/10.1016/j.chom.2018.08.004	journal	September 2018
Mitochondria: More Than Just a Powerhouse McBride, Heidi M.; Neuspiel, Margaret; Wasiak, Sylwia Current Biology, Vol. 16, Issue 14 https://doi.org/10.1016/j.cub.2006.06.054	journal	July 2006
A Legionella effector ADP-ribosyltransferase inactivates glutamate dehydrogenase Black, Miles H.; Osinski, Adam; Park, Gina J. Journal of Biological Chemistry, Vol. 296 https://doi.org/10.1016/j.jbc.2021.100301	journal	January 2021
Regulation of Phosphoribosyl-Linked Serine Ubiquitination by Deubiquitinases DupA and DupB Shin, Donghyuk; Mukherjee, Rukmini; Liu, Yaobin Molecular Cell, Vol. 77, Issue 1 https://doi.org/10.1016/j.molcel.2019.10.019	journal	January 2020
Threonine ADP-Ribosylation of Ubiquitin by a Bacterial Effector Family Blocks Host Ubiquitination Yan, Fujie; Huang, Chunfeng; Wang, Xiaofei Molecular Cell, Vol. 78, Issue 4 https://doi.org/10.1016/j.molcel.2020.03.016	journal	May 2020
Toward a unified nomenclature for mammalian ADP-ribosyltransferases Hottiger, Michael O.; Hassa, Paul O.; Lüscher, Bernhard Trends in Biochemical Sciences, Vol. 35, Issue 4 https://doi.org/10.1016/j.tibs.2009.12.003	journal	April 2010
The Crystal Structure of AF1521 a Protein from Archaeoglobus fulgidus with Homology to the Non-histone Domain of MacroH2A Allen, Mark D.; Buckle, Ashley M.; Cordell, Suzanne C. Journal of Molecular Biology, Vol. 330, Issue 3 https://doi.org/10.1016/s0022-2836(03)00473-x	journal	July 2003
Optimization of LTQ-Orbitrap Mass Spectrometer Parameters for the Identification of ADP-Ribosylation Sites Rosenthal, Florian; Nanni, Paolo; Barkow-Oesterreicher, Simon Journal of Proteome Research, Vol. 14, Issue 9 https://doi.org/10.1021/acs.jproteome.5b00432	journal	August 2015
Probing the Role of Positive Residues in the ADP/ATP Carrier from Yeast. The Effect of Six Arginine Mutations on Oxidative Phosphorylation and AAC Expression Müller, Veronika; Basset, Gabriele; Nelson, David R. Biochemistry, Vol. 35, Issue 50 https://doi.org/10.1021/bi960667r	journal	January 1996
Gas-Phase Fragmentation of ADP-Ribosylated Peptides: Arginine-Specific Side-Chain Losses and Their Implication in Database Searches Gehrig, Peter M.; Nowak, Kathrin; Panse, Christian Journal of the American Society for Mass Spectrometry, Vol. 32, Issue 1 https://doi.org/10.1021/jasms.0c00040	journal	November 2020
Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside Pebay-Peyroula, Eva; Dahout-Gonzalez, Cécile; Kahn, Richard Nature, Vol. 426, Issue 6962 https://doi.org/10.1038/nature02056	journal	November 2003
Modulation of Rab GTPase function by a protein phosphocholine transferase Mukherjee, Shaeri; Liu, Xiaoyun; Arasaki, Kohei Nature, Vol. 477, Issue 7362 https://doi.org/10.1038/nature10335	journal	August 2011
Ubiquitination independent of E1 and E2 enzymes by bacterial effectors Qiu, Jiazhang; Sheedlo, Michael J.; Yu, Kaiwen Nature, Vol. 533, Issue 7601 https://doi.org/10.1038/nature17657	journal	April 2016
The pharmacological regulation of cellular mitophagy Georgakopoulos, Nikolaos D.; Wells, Geoff; Campanella, Michelangelo Nature Chemical Biology, Vol. 13, Issue 2 https://doi.org/10.1038/nchembio.2287	journal	January 2017
Insights into the biogenesis, function, and regulation of ADP-ribosylation Cohen, Michael S.; Chang, Paul Nature Chemical Biology, Vol. 14, Issue 3 https://doi.org/10.1038/nchembio.2568	journal	February 2018
Genomic analysis of 38 Legionella species identifies large and diverse effector repertoires Burstein, David; Amaro, Francisco; Zusman, Tal Nature Genetics, Vol. 48, Issue 2 https://doi.org/10.1038/ng.3481	journal	January 2016
In-gel digestion for mass spectrometric characterization of proteins and proteomes Shevchenko, Andrej; Tomas, Henrik; Havli, Jan Nature Protocols, Vol. 1, Issue 6 https://doi.org/10.1038/nprot.2006.468	journal	December 2006
Mechanisms of mitophagy Youle, Richard J.; Narendra, Derek P. Nature Reviews Molecular Cell Biology, Vol. 12, Issue 1 https://doi.org/10.1038/nrm3028	journal	December 2010
Legionella and Coxiella effectors: strength in diversity and activity Qiu, Jiazhang; Luo, Zhao-Qing Nature Reviews Microbiology, Vol. 15, Issue 10 https://doi.org/10.1038/nrmicro.2017.67	journal	July 2017
The Legionella pneumophila replication vacuole: making a cosy niche inside host cells Isberg, Ralph R.; O'Connor, Tamara J.; Heidtman, Matthew Nature Reviews Microbiology, Vol. 7, Issue 1 https://doi.org/10.1038/nrmicro1967	journal	November 2008
Long noncoding RNA LINC00336 inhibits ferroptosis in lung cancer by functioning as a competing endogenous RNA Wang, Min; Mao, Chao; Ouyang, Lianlian Cell Death & Differentiation, Vol. 26, Issue 11 https://doi.org/10.1038/s41418-019-0304-y	journal	February 2019
Legionella pneumophila inhibits immune signalling via MavC-mediated transglutaminase-induced ubiquitination of UBE2N Gan, Ninghai; Nakayasu, Ernesto S.; Hollenbeck, Peter J. Nature Microbiology, Vol. 4, Issue 1 https://doi.org/10.1038/s41564-018-0282-8	journal	November 2018
The ADP/ATP translocase drives mitophagy independent of nucleotide exchange Hoshino, Atsushi; Wang, Wei-jia; Wada, Shogo Nature, Vol. 575, Issue 7782 https://doi.org/10.1038/s41586-019-1667-4	journal	October 2019
Mechanisms of cytochrome c release from mitochondria Garrido, C.; Galluzzi, L.; Brunet, M. Cell Death & Differentiation, Vol. 13, Issue 9 https://doi.org/10.1038/sj.cdd.4401950	journal	May 2006
The Legionella pneumophila IcmR protein exhibits chaperone activity for IcmQ by preventing its participation in high-molecular-weight complexes Dumenil, Guillaume; Isberg, Ralph R. Molecular Microbiology, Vol. 40, Issue 5 https://doi.org/10.1046/j.1365-2958.2001.02454.x	journal	June 2001
The Legionella pneumophila LidA protein: a translocated substrate of the Dot/Icm system associated with maintenance of bacterial integrity: The Legionella pneumophilia LidA translocated substrate Conover, Gloria M.; Derré, Isabelle; Vogel, Joseph P. Molecular Microbiology, Vol. 48, Issue 2 https://doi.org/10.1046/j.1365-2958.2003.03400.x	journal	April 2003
Abcb10 physically interacts with mitoferrin-1 (Slc25a37) to enhance its stability and function in the erythroid mitochondria Chen, Wen; Paradkar, Prasad N.; Li, Liangtao Proceedings of the National Academy of Sciences, Vol. 106, Issue 38 https://doi.org/10.1073/pnas.0904519106	journal	September 2009
Legionella pneumophila regulates the small GTPase Rab1 activity by reversible phosphorylcholination Tan, Y.; Arnold, R. J.; Luo, Z. -Q. Proceedings of the National Academy of Sciences, Vol. 108, Issue 52 https://doi.org/10.1073/pnas.1114023109	journal	December 2011
Structures of yeast mitochondrial ADP/ATP carriers support a domain-based alternating-access transport mechanism Ruprecht, Jonathan J.; Hellawell, Alex M.; Harding, Marilyn Proceedings of the National Academy of Sciences, Vol. 111, Issue 4 https://doi.org/10.1073/pnas.1320692111	journal	January 2014
Legionella pneumophila S1P-lyase targets host sphingolipid metabolism and restrains autophagy Rolando, Monica; Escoll, Pedro; Nora, Tamara Proceedings of the National Academy of Sciences, Vol. 113, Issue 7 https://doi.org/10.1073/pnas.1522067113	journal	February 2016
Mechanism of cholera toxin action: Covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system Cassel, Dan; Pfeuffer, Thomas Proceedings of the National Academy of Sciences, Vol. 75, Issue 6 https://doi.org/10.1073/pnas.75.6.2669	journal	June 1978
Signal-dependent DNA binding and functional domains of the quorum-sensing activator TraR as identified by repressor activity Luo, Z. -Q.; Farrand, S. K. Proceedings of the National Academy of Sciences, Vol. 96, Issue 16 https://doi.org/10.1073/pnas.96.16.9009	journal	August 1999
Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes Horwitz, M. A. Journal of Experimental Medicine, Vol. 158, Issue 4 https://doi.org/10.1084/jem.158.4.1319	journal	October 1983
The HHpred interactive server for protein homology detection and structure prediction Soding, J.; Biegert, A.; Lupas, A. N. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki408	journal	July 2005
Induction of caspase 3 activation by multipleLegionella pneumophila Dot/Icm substrates Zhu, Wenhan; Hammad, Loubna A.; Hsu, FoSheng Cellular Microbiology https://doi.org/10.1111/cmi.12157	journal	July 2013
ADP-ribosylation: new facets of an ancient modification Palazzo, Luca; Mikoč, Andreja; Ahel, Ivan The FEBS Journal, Vol. 284, Issue 18 https://doi.org/10.1111/febs.14078	journal	April 2017
Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila Berger, Karen H.; Isberg, Ralph R. Molecular Microbiology, Vol. 7, Issue 1 https://doi.org/10.1111/j.1365-2958.1993.tb01092.x	journal	January 1993
Altered intracellular targeting properties associated with mutations in the Legionella pneumophila dotA gene Berger, Karen H.; Merriam, Jennifer J.; Isberg, Ralph R. Molecular Microbiology, Vol. 14, Issue 4 https://doi.org/10.1111/j.1365-2958.1994.tb01317.x	journal	November 1994
The response regulator PmrA is a major regulator of the icm/dot type IV secretion system in Legionella pneumophila and Coxiella burnetii Zusman, Tal; Aloni, Gali; Halperin, Einat Molecular Microbiology, Vol. 63, Issue 5 https://doi.org/10.1111/j.1365-2958.2007.05604.x	journal	March 2007
A Legionella effector acquired from protozoa is involved in sphingolipids metabolism and is targeted to the host cell mitochondria Degtyar, Elena; Zusman, Tal; Ehrlich, Marcelo Cellular Microbiology, Vol. 11, Issue 8 https://doi.org/10.1111/j.1462-5822.2009.01328.x	journal	August 2009
Ehrlichia type IV secretion effector ECH0825 is translocated to mitochondria and curbs ROS and apoptosis by upregulating host MnSOD Liu, Hongyan; Bao, Weichao; Lin, Mingqun Cellular Microbiology, Vol. 14, Issue 7 https://doi.org/10.1111/j.1462-5822.2012.01775.x	journal	March 2012
Integral membrane proteins in the mitochondrial outer membrane of Saccharomyces cerevisiae Burri, Lena; Vascotto, Katherine; Gentle, Ian E. FEBS Journal, Vol. 273, Issue 7 https://doi.org/10.1111/j.1742-4658.2006.05171.x	journal	April 2006
Solution Structure of the Integral Human Membrane Protein VDAC-1 in Detergent Micelles Hiller, S.; Garces, R. G.; Malia, T. J. Science, Vol. 321, Issue 5893 https://doi.org/10.1126/science.1161302	journal	August 2008
The Legionella Effector Protein DrrA AMPylates the Membrane Traffic Regulator Rab1b Muller, M. P.; Peters, H.; Blumer, J. Science, Vol. 329, Issue 5994 https://doi.org/10.1126/science.1192276	journal	July 2010
Molecular Pathogenesis of Infections Caused by Legionella pneumophila Newton, H. J.; Ang, D. K. Y.; van Driel, I. R. Clinical Microbiology Reviews, Vol. 23, Issue 2 https://doi.org/10.1128/CMR.00052-09	journal	April 2010
Legionella pneumophila Replication Vacuole Formation Involves Rapid Recruitment of Proteins of the Early Secretory System Derré, Isabelle; Isberg, Ralph R. Infection and Immunity, Vol. 72, Issue 5 https://doi.org/10.1128/IAI.72.5.3048-3053.2004	journal	May 2004
Divergent Pathogenic Properties of Circulating Coxsackievirus A6 Associated with Emerging Hand, Foot, and Mouth Disease Wang, Shao-Hua; Wang, Ao; Liu, Pan-Pan Journal of Virology, Vol. 92, Issue 11 https://doi.org/10.1128/JVI.00303-18	journal	June 2018
Modulation of Host Cell Function by Legionella pneumophila Type IV Effectors Hubber, Andree; Roy, Craig R. Annual Review of Cell and Developmental Biology, Vol. 26, Issue 1 https://doi.org/10.1146/annurev-cellbio-100109-104034	journal	November 2010
How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane Tilney, Lewis G.; Harb, Omar S.; Connelly, Patricia S. Journal of Cell Science, Vol. 114, Issue 24 https://doi.org/10.1242/jcs.114.24.4637	journal	December 2001
Comprehensive Identification of Protein Substrates of the Dot/Icm Type IV Transporter of Legionella pneumophila Zhu, Wenhan; Banga, Simran; Tan, Yunhao PLoS ONE, Vol. 6, Issue 3 https://doi.org/10.1371/journal.pone.0017638	journal	March 2011
Inhibition of Host Vacuolar H+-ATPase Activity by a Legionella pneumophila Effector Xu, Li; Shen, Xihui; Bryan, Andrew PLoS Pathogens, Vol. 6, Issue 3 https://doi.org/10.1371/journal.ppat.1000822	journal	March 2010
Legionella pneumophila Secretes a Mitochondrial Carrier Protein during Infection Dolezal, Pavel; Aili, Margareta; Tong, Janette PLoS Pathogens, Vol. 8, Issue 1 https://doi.org/10.1371/journal.ppat.1002459	journal	January 2012
Modulation of phagosome phosphoinositide dynamics by a Legionella phosphoinositide 3‐kinase Li, Gen; Liu, Hongtao; Luo, Zhao‐Qing EMBO reports, Vol. 22, Issue 3 https://doi.org/10.15252/embr.202051163	journal	January 2021
Diverse mechanisms of metaeffector activity in an intracellular bacterial pathogen, Legionella pneumophila Urbanus, Malene L.; Quaile, Andrew T.; Stogios, Peter J. Molecular Systems Biology, Vol. 12, Issue 12 https://doi.org/10.15252/msb.20167381	journal	December 2016
Cellular microbiology and molecular ecology ofLegionella–amoeba interaction Richards, Ashley M.; Von Dwingelo, Juanita E.; Price, Christopher T. Virulence, Vol. 4, Issue 4 https://doi.org/10.4161/viru.24290	journal	May 2013

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59 BASIC BIOLOGICAL SCIENCES
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mART

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