Polyphosphate and associated enzymes as global regulators of stress response and virulence in Campylobacter jejuni

Kumar, Anand; Gangaiah, Dharanesh; Torrelles, Jordi B.; Rajashekara, Gireesh

doi:10.3748/wjg.v22.i33.7402

Title: Polyphosphate and associated enzymes as global regulators of stress response and virulence in Campylobacter jejuni

Journal Article · Wed Sep 07 00:00:00 EDT 2016 · World Journal of Gastroenterology

DOI:https://doi.org/10.3748/wjg.v22.i33.7402· OSTI ID:1628601

Kumar, Anand ^[1]; Gangaiah, Dharanesh ^[2]; Torrelles, Jordi B. ^[3]; Rajashekara, Gireesh ^[3]

The Ohio State Univ., Columbus, OH (United States); Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Indiana Univ. School of Medicine, Indianapolis, IN (United States)
The Ohio State Univ., Columbus, OH (United States)

Campylobacter jejuni (C. jejuni), a Gram-negative microaerophilic bacterium, is a predominant cause of bacterial foodborne gastroenteritis in humans worldwide. Despite its importance as a major foodborne pathogen, our understanding of the molecular mechanisms underlying C. jejuni stress survival and pathogenesis is limited. Inorganic polyphosphate (poly P) has been shown to play significant roles in bacterial resistance to stress and virulence in many pathogenic bacteria. C. jejuni contains the complete repertoire of enzymes required for poly P metabolism. Recent work in our laboratory and others have demonstrated that poly P controls a plethora of C. jejuni properties that impact its ability to survive in the environment as well as to colonize/infect mammalian hosts. This review article summarizes the current literature on the role of poly P in C. jejuni stress survival and virulence and discusses on how poly P-related enzymes can be exploited for therapeutic/prevention purposes. Additionally, the review article identifies potential areas for future investigation that would enhance our understanding of the role of poly P in C. jejuni and other bacteria, which ultimately would facilitate design of effective therapeutic/preventive strategies to reduce not only the burden of C. jejuni-caused foodborne infections but also of other bacterial infections in humans.

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Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC); Agriculture and Food Research Initiative (AFRI)

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 1628601

Journal Information:: World Journal of Gastroenterology, Vol. 22, Issue 33; ISSN 1007-9327

Publisher:: Baishideng Publishing Group Inc.Copyright Statement

Country of Publication:: United States

Language:: English

References (83)

A role for Campylobacter jejuni-induced enteritis in inflammatory bowel disease? Kalischuk, Lisa D.; Buret, Andre G. American Journal of Physiology-Gastrointestinal and Liver Physiology, Vol. 298, Issue 1 https://doi.org/10.1152/ajpgi.00193.2009	journal	January 2010
A Polyphosphate-Lon Protease Complex in the Adaptation of Escherichia coli to Amino Acid Starvation Kuroda, Akio Bioscience, Biotechnology, and Biochemistry, Vol. 70, Issue 2 https://doi.org/10.1271/bbb.70.325	journal	January 2006
Alginate, inorganic polyphosphate, GTP and ppGpp synthesis co-regulated in Pseudomonas aeruginosa: implications for stationary phase survival and synthesis of RNA/DNA precursors Kim, Hong-Yeoul; Schlictman, D.; Shankar, Sandeep Molecular Microbiology, Vol. 27, Issue 4 https://doi.org/10.1046/j.1365-2958.1998.00702.x	journal	February 1998
Campylobacter showae sp. nov., Isolated from the Human Oral Cavity Etoh, Y.; Dewhirst, F. E.; Paster, B. J. International Journal of Systematic Bacteriology, Vol. 43, Issue 4 https://doi.org/10.1099/00207713-43-4-631	journal	October 1993
The long and short of it – polyphosphate, PPK and bacterial survival Brown, Michael R. W.; Kornberg, Arthur Trends in Biochemical Sciences, Vol. 33, Issue 6 https://doi.org/10.1016/j.tibs.2008.04.005	journal	June 2008
Inorganic polyphosphate kinase is required to stimulate protein degradation and for adaptation to amino acid starvation in Escherichia coli Kuroda, A.; Tanaka, S.; Ikeda, T. Proceedings of the National Academy of Sciences, Vol. 96, Issue 25 https://doi.org/10.1073/pnas.96.25.14264	journal	December 1999
Evaluation of periodontal pathogens in amniotic fluid and the role of periodontal disease in pre-term birth and low birth weight Ercan, Esra; Eratalay, Kenan; Deren, Ozgur Acta Odontologica Scandinavica, Vol. 71, Issue 3-4 https://doi.org/10.3109/00016357.2012.697576	journal	July 2012
Polyphosphate kinase 2: a modulator of nucleoside diphosphate kinase activity in mycobacteria Sureka, Kamakshi; Sanyal, Sourav; Basu, Joyoti Molecular Microbiology, Vol. 74, Issue 5 https://doi.org/10.1111/j.1365-2958.2009.06925.x	journal	December 2009
Postinfectious Irritable Bowel Syndrome Ericsson, C. D.; Hatz, C.; DuPont, A. W. Clinical Infectious Diseases, Vol. 46, Issue 4 https://doi.org/10.1086/526774	journal	February 2008
Campylobacter Reactive Arthritis: A Systematic Review Pope, Janet E.; Krizova, Adriana; Garg, Amit X. Seminars in Arthritis and Rheumatism, Vol. 37, Issue 1 https://doi.org/10.1016/j.semarthrit.2006.12.006	journal	August 2007
Three cases of cardiac complications associated with Campylobacter jejuni infection and review of the literature Hannu, T.; Mattila, L.; Rautelin, H. European Journal of Clinical Microbiology & Infectious Diseases, Vol. 24, Issue 9 https://doi.org/10.1007/s10096-005-0001-2	journal	September 2005
The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences Parkhill, J.; Wren, B. W.; Mungall, K. Nature, Vol. 403, Issue 6770 https://doi.org/10.1038/35001088	journal	February 2000
The Structure of the Exopolyphosphatase (PPX) from Escherichia coli O157:H7 Suggests a Binding Mode for Long Polyphosphate Chains Rangarajan, Erumbi S.; Nadeau, Guy; Li, Yunge Journal of Molecular Biology, Vol. 359, Issue 5 https://doi.org/10.1016/j.jmb.2006.04.031	journal	June 2006
Oral Campylobacter Species Involved in Extraoral Abscess: a Report of Three Cases Han, X. Y.; Tarrand, J. J.; Rice, D. C. Journal of Clinical Microbiology, Vol. 43, Issue 5 https://doi.org/10.1128/jcm.43.5.2513-2515.2005	journal	May 2005
Polyphosphate kinases modulate Campylobacter jejuni outer membrane constituents and alter its capacity to invade and survive in intestinal epithelial cells in vitro Pina-Mimbela, Ruby; Madrid, Jesús Arcos; Kumar, Anand Emerging Microbes & Infections, Vol. 4, Issue 1 https://doi.org/10.1038/emi.2015.77	journal	January 2015
Abortion and Perinatal Sepsis Associated with Campylobacter Infection Simor, A. E.; Karmali, M. A.; Jadavji, T. Clinical Infectious Diseases, Vol. 8, Issue 3 https://doi.org/10.1093/clinids/8.3.397	journal	May 1986
Campylobacter Species in Health, Gingivitis, and Periodontitis Macuch, P. J.; Tanner, A. C. R. Journal of Dental Research, Vol. 79, Issue 2 https://doi.org/10.1177/00220345000790021301	journal	February 2000
Prevalence of Campylobacter Species in Adult Crohn's Disease and the Preferential Colonization Sites of Campylobacter Species in the Human Intestine Mahendran, Vikneswari; Riordan, Stephen M.; Grimm, Michael C. PLoS ONE, Vol. 6, Issue 9 https://doi.org/10.1371/journal.pone.0025417	journal	September 2011
Inorganic Polyphosphate: Essential for Growth and Survival Rao, Narayana N.; Gómez-García, María R.; Kornberg, Arthur Annual Review of Biochemistry, Vol. 78, Issue 1 https://doi.org/10.1146/annurev.biochem.77.083007.093039	journal	June 2009
Polyphosphate Degradation in Stationary Phase Triggers Biofilm Formation via LuxS Quorum Sensing System in Escherichia coli Grillo-Puertas, Mariana; Villegas, Josefina M.; Rintoul, María R. PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0050368	journal	November 2012
Recrudescent Campylobacter jejuni Infection in an Immunocompetent Adult following Experimental Infection with a Well-Characterized Organism Baqar, Shahida; Tribble, David R.; Carmolli, Marya Clinical and Vaccine Immunology, Vol. 17, Issue 1 https://doi.org/10.1128/cvi.00252-09	journal	November 2009
Campylobacter concisus – A New Player in Intestinal Disease Kaakoush, Nadeem Omar; Mitchell, Hazel Marjory Frontiers in Cellular and Infection Microbiology, Vol. 2 https://doi.org/10.3389/fcimb.2012.00004	journal	January 2012
Putative structure and functions of a poly-beta-hydroxybutyrate/calcium polyphosphate channel in bacterial plasma membranes. Reusch, R. N.; Sadoff, H. L. Proceedings of the National Academy of Sciences, Vol. 85, Issue 12 https://doi.org/10.1073/pnas.85.12.4176	journal	June 1988
Evaluation of safety and protection efficacy on cpxR and lon deleted mutant of Salmonella Gallinarum as a live vaccine candidate for fowl typhoid Matsuda, Kiku; Chaudhari, Atul A.; Lee, John Hwa Vaccine, Vol. 29, Issue 4 https://doi.org/10.1016/j.vaccine.2010.11.039	journal	January 2011
Campylobacter species isolated from extra-oro-intestinal abscesses: a report of four cases and literature review Vries, J. J. C.; Arents, N. L. A.; Manson, W. L. European Journal of Clinical Microbiology & Infectious Diseases, Vol. 27, Issue 11 https://doi.org/10.1007/s10096-008-0550-2	journal	May 2008
A tangle of poly-phosphate in Campylobacter Jeon, Byeonghwa Virulence, Vol. 5, Issue 4 https://doi.org/10.4161/viru.28690	journal	April 2014
Campylobacter jejuni Strain CG8421: A Refined Model for the Study of Campylobacteriosis and Evaluation of Campylobacter Vaccines in Human Subjects Tribble, David R.; Baqar, Shahida; Carmolli, Marya P. Clinical Infectious Diseases, Vol. 49, Issue 10 https://doi.org/10.1086/644622	journal	November 2009
Inorganic Polyphosphates in the Acquisition of Competence in Escherichia coli Castuma, Celina E.; Huang, Ruiping; Kornberg, Arthur Journal of Biological Chemistry, Vol. 270, Issue 22 https://doi.org/10.1074/jbc.270.22.12980	journal	June 1995
Intestinal Microbes in Inflammatory Bowel Diseases Sartor, R. Balfour; Mazmanian, Sarkis K. The American Journal of Gastroenterology Supplements, Vol. 1, Issue 1 https://doi.org/10.1038/ajgsup.2012.4	journal	July 2012
The physiology of Campylobacter species and its relevance to their role as foodborne pathogens Park, Simon F. International Journal of Food Microbiology, Vol. 74, Issue 3 https://doi.org/10.1016/s0168-1605(01)00678-x	journal	April 2002
Cardiovascular and Bacteremic Manifestations of Campylobacter fetus Infection: Case Report and Review Morrison, V. A.; Lloyd, B. K.; Chia, J. K. S. Clinical Infectious Diseases, Vol. 12, Issue 3 https://doi.org/10.1093/clinids/12.3.387	journal	May 1990
Polyphosphate kinase (PPK2), a potent, polyphosphate-driven generator of GTP Ishige, K.; Zhang, H.; Kornberg, A. Proceedings of the National Academy of Sciences, Vol. 99, Issue 26 https://doi.org/10.1073/pnas.262655299	journal	December 2002
Inorganic polyphosphate and the induction of rpoS expression Shiba, T.; Tsutsumi, K.; Yano, H. Proceedings of the National Academy of Sciences, Vol. 94, Issue 21 https://doi.org/10.1073/pnas.94.21.11210	journal	October 1997
Campylobacter jejuni: molecular biology and pathogenesis Young, Kathryn T.; Davis, Lindsay M.; DiRita, Victor J. Nature Reviews Microbiology, Vol. 5, Issue 9 https://doi.org/10.1038/nrmicro1718	journal	September 2007
Campylobacter jejuni 81-176 forms distinct microcolonies on in vitro-infected human small intestinal tissue prior to biofilm formation Haddock, Graham; Mullin, Margaret; MacCallum, Amanda Microbiology, Vol. 156, Issue 10 https://doi.org/10.1099/mic.0.039867-0	journal	October 2010
Antimicrobial Resistance and Genotypic Diversity of Campylobacter Isolated from Pigs, Dairy, and Beef Cattle in Tanzania Kashoma, Isaac P.; Kassem, Issmat I.; Kumar, Anand Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01240	journal	November 2015
Ultrastructure and complex polar architecture of the human pathogen Campylobacter jejuni Müller, Axel; Beeby, Morgan; McDowall, Alasdair W. MicrobiologyOpen, Vol. 3, Issue 5 https://doi.org/10.1002/mbo3.200	journal	July 2014
Endopolyphosphatases for Long Chain Inorganic Polyphosphate in Yeast and Mammals Kumble, Krishnanand D.; Kornberg, Arthur Journal of Biological Chemistry, Vol. 271, Issue 43 https://doi.org/10.1074/jbc.271.43.27146	journal	October 1996
Physiology, pathogenicity and immunogenicity of live, attenuated Salmonella enterica serovar Enteritidis mutants in chicks Si, Wei; Wang, Xiumei; Liu, Huifang Microbial Pathogenesis, Vol. 83-84 https://doi.org/10.1016/j.micpath.2015.03.018	journal	June 2015
Physiological Characterization of Viable-but-Nonculturable Campylobacter jejuniCells Tholozan, J. L.; Cappelier, J. M.; Tissier, J. P. Applied and Environmental Microbiology, Vol. 65, Issue 3 https://doi.org/10.1128/aem.65.3.1110-1116.1999	journal	March 1999
Nosocomial Outbreak of Campylobacter Jejuni Meningitis in Newborn Infants Goossens, Herman; Kremp, Louis; Boury, Richard The Lancet, Vol. 328, Issue 8499 https://doi.org/10.1016/s0140-6736(86)91956-2	journal	July 1986
Biofilm Formation by Campylobacter jejuni Is Increased under Aerobic Conditions Reuter, Mark; Mallett, Arthur; Pearson, Bruce M. Applied and Environmental Microbiology, Vol. 76, Issue 7 https://doi.org/10.1128/aem.01878-09	journal	February 2010
Formation of volutin granules in Corynebacterium glutamicum Pallerla, Srinivas Reddy; Knebel, Sandra; Polen, Tino FEMS Microbiology Letters, Vol. 243, Issue 1 https://doi.org/10.1016/j.femsle.2004.11.047	journal	February 2005
The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes: C. jejuni stringent response Gaynor, Erin C.; Wells, Derek H.; MacKichan, Joanna K. Molecular Microbiology, Vol. 56, Issue 1 https://doi.org/10.1111/j.1365-2958.2005.04525.x	journal	February 2005
Co-occurrence of anaerobic bacteria in colorectal carcinomas Warren, René L.; Freeman, Douglas J.; Pleasance, Stephen Microbiome, Vol. 1, Issue 1 https://doi.org/10.1186/2049-2618-1-16	journal	January 2013
Mutational analysis of nucleoside diphosphate kinase from Pseudomonas aeruginosa: characterization of critical amino acid residues involved in exopolysaccharide alginate synthesis. Sundin, G. W.; Shankar, S.; Chakrabarty, A. M. Journal of bacteriology, Vol. 178, Issue 24 https://doi.org/10.1128/jb.178.24.7120-7128.1996	journal	January 1996
Polyphosphate Kinase 2: A Novel Determinant of Stress Responses and Pathogenesis in Campylobacter jejuni Gangaiah, Dharanesh; Liu, Zhe; Arcos, Jesús PLoS ONE, Vol. 5, Issue 8 https://doi.org/10.1371/journal.pone.0012142	journal	August 2010
Bacterial stress responses as determinants of antimicrobial resistance Poole, K. Journal of Antimicrobial Chemotherapy, Vol. 67, Issue 9 https://doi.org/10.1093/jac/dks196	journal	May 2012
Transcriptome analysis of Campylobacter jejuni polyphosphate kinase ( ppk1 and ppk2 ) mutants Chandrashekhar, Kshipra; Kassem, Issmat I.; Nislow, Corey Virulence, Vol. 6, Issue 8 https://doi.org/10.1080/21505594.2015.1104449	journal	November 2015
Contribution of TAT System Translocated PhoX to Campylobacter jejuni Phosphate Metabolism and Resilience to Environmental Stresses Drozd, Mary; Gangaiah, Dharanesh; Liu, Zhe PLoS ONE, Vol. 6, Issue 10 https://doi.org/10.1371/journal.pone.0026336	journal	October 2011
Novel Anti-Campylobacter Compounds Identified Using High Throughput Screening of a Pre-selected Enriched Small Molecules Library Kumar, Anand; Drozd, Mary; Pina-Mimbela, Ruby Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00405	journal	April 2016
Campylobacter biofilm phenotype exhibits reduced colonization potential in young chickens and altered in vitro virulence Hanning, I.; Donoghue, D. J.; Jarquin, R. Poultry Science, Vol. 88, Issue 5 https://doi.org/10.3382/ps.2008-00307	journal	May 2009
Polyphosphate kinase regulates error-prone replication by DNA polymerase IV in Escherichia coli: Ppk regulates polymerase IV activity Stumpf, Jeffrey D.; Foster, Patricia L. Molecular Microbiology, Vol. 57, Issue 3 https://doi.org/10.1111/j.1365-2958.2005.04724.x	journal	June 2005
Functional analysis of a Campylobacter jejuni alkaline phosphatase secreted via the Tat export machinery van Mourik, Andries; Bleumink-Pluym, Nancy M. C.; van Dijk, Linda Microbiology, Vol. 154, Issue 2 https://doi.org/10.1099/mic.0.2007/012120-0	journal	February 2008
Nucleoside diphosphate kinase: role in bacterial growth, virulence, cell signalling and polysaccharide synthesis Chakrabarty, A. M. Molecular Microbiology, Vol. 28, Issue 5 https://doi.org/10.1046/j.1365-2958.1998.00846.x	journal	June 1998
Importance of Polyphosphate Kinase 1 for Campylobacter jejuni Viable-but-Nonculturable Cell Formation, Natural Transformation, and Antimicrobial Resistance Gangaiah, Dharanesh; Kassem, Issmat I.; Liu, Zhe Applied and Environmental Microbiology, Vol. 75, Issue 24 https://doi.org/10.1128/aem.01603-09	journal	October 2009
Functional characterization of exopolyphosphatase/guanosine pentaphosphate phosphohydrolase (PPX/GPPA) of Campylobacter jejuni Malde, Anandkumar; Gangaiah, Dharanesh; Chandrashekhar, Kshipra Virulence, Vol. 5, Issue 4 https://doi.org/10.4161/viru.28311	journal	February 2014
Campylobacter jejuni cholecystitis: a rare but significant clinical entity Vaughan-Shaw, P. G.; Rees, J. R.; White, D. Case Reports, Vol. 2010, Issue apr08 1 https://doi.org/10.1136/bcr.10.2009.2365	journal	April 2010
Campylobacter jejuni meningitis in an immunocompetent adult male [健常成人に発症したＣａｍｐｙｌｏｂａｃｔｅｒ　ｊｅｊｕｎｉ　髄膜炎の１例] Kogawa, Shuro; Furukawa, Kaoru Rinsho Shinkeigaku, Vol. 50, Issue 4 https://doi.org/10.5692/clinicalneurol.50.262	journal	January 2010
Antecedent infections in Fisher syndrome: A common pathogenesis of molecular mimicry Koga, M.; Gilbert, M.; Li, J. Neurology, Vol. 64, Issue 9 https://doi.org/10.1212/01.wnl.0000160399.08456.7c	journal	May 2005
Microbial Colonization of the Upper Gastrointestinal Tract in Patients with Barrett's Esophagus Macfarlane, S.; Furrie, E.; Macfarlane, G. T. Clinical Infectious Diseases, Vol. 45, Issue 1 https://doi.org/10.1086/518578	journal	July 2007
DNA Sequence and Mutational Analyses of the pVir Plasmid of Campylobacter jejuni 81-176 Bacon, David J.; Alm, Richard A.; Hu, Lan Infection and Immunity, Vol. 70, Issue 11 https://doi.org/10.1128/IAI.70.11.6242-6250.2002	journal	November 2002
Guanosine Tetra- and Pentaphosphate Promote Accumulation of Inorganic Polyphosphate in Escherichia coli Kuroda, Akio; Murphy, Helen; Cashel, Michael Journal of Biological Chemistry, Vol. 272, Issue 34 https://doi.org/10.1074/jbc.272.34.21240	journal	August 1997
NCgl2620 Encodes a Class II Polyphosphate Kinase in Corynebacterium glutamicum Lindner, Steffen N.; Vidaurre, Dolores; Willbold, Sabine Applied and Environmental Microbiology, Vol. 73, Issue 15 https://doi.org/10.1128/aem.00600-07	journal	June 2007
Structural Characterization of the Stringent Response Related Exopolyphosphatase/Guanosine Pentaphosphate Phosphohydrolase Protein Family ^† ^, ^‡ Kristensen, Ole; Laurberg, Martin; Liljas, Anders Biochemistry, Vol. 43, Issue 28 https://doi.org/10.1021/bi049083c	journal	July 2004
Molecular detection identified a type six secretion system in Campylobacter jejuni from various sources but not from human cases Siddiqui, F.; Champion, O.; Akram, M. Journal of Applied Microbiology, Vol. 118, Issue 5 https://doi.org/10.1111/jam.12748	journal	March 2015
Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence Guerry, Patricia; Ewing, Cheryl P.; Schirm, Michael Molecular Microbiology, Vol. 60, Issue 2 https://doi.org/10.1111/j.1365-2958.2006.05100.x	journal	April 2006
Campylobacter Species and Guillain-Barré Syndrome Nachamkin, Irving; Allos, Ban Mishu; Ho, Tony Clinical Microbiology Reviews, Vol. 11, Issue 3 https://doi.org/10.1128/cmr.11.3.555	journal	July 1998
Prevalence and Antimicrobial Resistance of Campylobacter Isolated from Dressed Beef Carcasses and Raw Milk in Tanzania Kashoma, Isaac P.; Kassem, Issmat I.; John, Julius Microbial Drug Resistance, Vol. 22, Issue 1 https://doi.org/10.1089/mdr.2015.0079	journal	January 2016
Reiter's syndrome in association with enteritis due to Campylobacter fetus ssp. jejuni. Ponka, A.; Martio, J.; Kosunen, T. U. Annals of the Rheumatic Diseases, Vol. 40, Issue 4 https://doi.org/10.1136/ard.40.4.414	journal	August 1981
Meningitis and Endocarditis Caused by Campylobacter fetus after Raw-Liver Ingestion Suy, F.; Le Du, D.; Roux, A. -L. Journal of Clinical Microbiology, Vol. 51, Issue 9 https://doi.org/10.1128/jcm.00631-13	journal	July 2013
Polyphosphate kinase from Escherichia coli. Purification and demonstration of a phosphoenzyme intermediate. Ahn, K.; Kornberg, A. Journal of Biological Chemistry, Vol. 265, Issue 20 https://doi.org/10.1016/s0021-9258(19)38459-5	journal	July 1990
Deficiency of the Novel Exopolyphosphatase Rv1026/PPX2 Leads to Metabolic Downshift and Altered Cell Wall Permeability in Mycobacterium tuberculosis Chuang, Yu-Min; Bandyopadhyay, Nirmalya; Rifat, Dalin mBio, Vol. 6, Issue 2 https://doi.org/10.1128/mbio.02428-14	journal	March 2015
Microbiota disbiosis is associated with colorectal cancer Gao, Zhiguang; Guo, Bomin; Gao, Renyuan Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00020	journal	February 2015
Campylobacter bacteremia: A rare and under-reported event? Louwen, Rogier; van Baarlen, P.; van Vliet, A. H. M. European Journal of Microbiology and Immunology, Vol. 2, Issue 1 https://doi.org/10.1556/eujmi.2.2012.1.11	journal	March 2012
Maladie immunoproliférative de l’intestin grêle associée à Campylobacter jejuni Lecuit, Marc; Suarez, Felipe; Lortholary, Olivier médecine/sciences, Vol. 20, Issue 6-7 https://doi.org/10.1051/medsci/2004206-7638	journal	June 2004
Polyphosphate-mediated modulation of Campylobacter jejuni biofilm growth and stability Drozd, Mary; Chandrashekhar, Kshipra; Rajashekara, Gireesh Virulence, Vol. 5, Issue 6 https://doi.org/10.4161/viru.34348	journal	August 2014
Of energy and survival incognito: a relationship between viable but non-culturable cells formation and inorganic polyphosphate and formate metabolism in Campylobacter jejuni Kassem, Issmat I.; Chandrashekhar, Kshipra; Rajashekara, Gireesh Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00183	journal	January 2013
Campylobacter jejuni 81-176 Associates with Microtubules and Dynein during Invasion of Human Intestinal Cells Hu, Lan; Kopecko, Dennis J. Infection and Immunity, Vol. 67, Issue 8 https://doi.org/10.1128/IAI.67.8.4171-4182.1999	journal	August 1999
The microbiology of biological phosphorus removal in activated sludge systems Seviour, Robert J.; Mino, Takashi; Onuki, Motoharu FEMS Microbiology Reviews, Vol. 27, Issue 1 https://doi.org/10.1016/s0168-6445(03)00021-4	journal	April 2003
Phenotypic and Genotypic Diversity of Thermophilic Campylobacter spp. in Commercial Turkey Flocks: A Longitudinal Study Kashoma, Isaac P.; Kumar, Anand; Sanad, Yasser M. Foodborne Pathogens and Disease, Vol. 11, Issue 11 https://doi.org/10.1089/fpd.2014.1794	journal	November 2014
The polyphosphate kinase gene of Escherichia coli. Isolation and sequence of the ppk gene and membrane location of the protein. Akiyama, M.; Crooke, E.; Kornberg, A. Journal of Biological Chemistry, Vol. 267, Issue 31 https://doi.org/10.1016/S0021-9258(18)41708-5	journal	November 1992
Genetically altered levels of inorganic polyphosphate in Escherichia coli. Crooke, E.; Akiyama, M.; Rao, N. N. Journal of Biological Chemistry, Vol. 269, Issue 9 https://doi.org/10.1016/S0021-9258(17)37370-2	journal	March 1994

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Title: Polyphosphate and associated enzymes as global regulators of stress response and virulence in Campylobacter jejuni

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