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ISSN: 1895-5770
Gastroenterology Review/Przegląd Gastroenterologiczny
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vol. 13
Review paper

Morphology of Helicobacter pylori as a result of peptidoglycan and cytoskeleton rearrangements

Paweł Krzyżek, Grażyna Gościniak

Gastroenterology Rev 2018; 13 (3): 182–195
Online publish date: 2018/09/17
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Helicobacter pylori is a Gram-negative, microaerophilic bacterium colonising the gastric mucosa. Normally, this bacterium has a spiral shape, which is crucial for proper colonisation of the stomach and cork-screwing penetration of dense mucin covering this organ. However, H. pylori may also form curved/straight rods, filamentous forms and coccoid forms. This morphological variability affects nutrient transport and respiration processes, as well as motility, the ability to form aggregates/biofilms, and resistance to adverse environmental factors. For this reason, a more accurate understanding of the molecular determinants that control the morphology of H. pylori seems to be crucial in increasing the effectiveness of antibacterial therapies directed against this microorganism. This article focuses on the molecular factors responsible for peptidoglycan and cytoskeleton rearrangements affecting H. pylori morphology and survivability. In addition, the existence of proteins associated with modifications of H. pylori morphology as potential targets in therapies reducing the virulence of this bacterium has been suggested.

coccoid form, filamentous form, murein, shape

Robinson K, Letley DP, Kaneko K. The human stomach in health and disease: infection strategies by Helicobacter pylori. Curr Top Microbiol Immunol 2017; 400: 1-26.
Malfertheiner P, Link A, Selgrad M. Helicobacter pylori: perspectives and time trends. Nat Rev Gastroenterol Hepatol 2014; 11: 628-38.
Venerito M, Vasapolli R, Malfertheiner P. Helicobacter pylori and gastric cancer: timing and impact of preventive measures. Adv Exp Med Biol 2016; 908: 409-18.
Dunne C, Dolan B, Clyne M. Factors that mediate colonization of the human stomach by Helicobacter pylori. World J Gastroenterol 2014; 20: 5610-24.
Hazell SL, Lee A, Brady L, et al. Campylobacter pyloridis and gastritis: association with intercellular spaces and adaptation to an environment of mucus as important factors in colonization of the gastric epithelium. J Infect Dis 1986; 153: 658-63.
Keshavarz T, Walker MM, Karim QN, et al. The relationship between Helicobacter pylori motility, morphology and phase of growth: implications for gastric colonization and pathology. Microbiology 1999; 145: 2803-11.
Sycuro LK, Pincus Z, Gutierrez KD, et al. Peptidoglycan crosslinking relaxation promotes Helicobacter pylori’s helical shape and stomach colonization. Cell 2010; 141: 822-33.
Sycuro LK, Wyckoff TJ, Biboy J, et al. Multiple peptidoglycan modification networks modulate Helicobacter pylori’s cell shape, motility, and colonization potential. PLoS Pathog 2012; 8: e1002603.
An DR, Kim HS, Kim J, et al. Structure of Csd3 from Helicobacter pylori, a cell shape-determining metallopeptidase. Acta Crystallogr Sect D Biol Crystallogr 2015; 71: 675-86.
Martínez LE, Hardcastle JM, Wang J, et al. Helicobacter pylori strains vary cell shape and flagellum number to maintain robust motility in viscous environments. Mol Microbiol 2016; 99: 88-110.
French S, Côté JP, Stokes JM, et al. Bacteria getting into shape: genetic determinants of E. coli morphology. MBio 2017; 8: e01977-16.
van Teeseling MCF, de Pedro MA, Cava F. Determinants of bacterial morphology: from fundamentals to possibilities for antimicrobial targeting. Front Microbiol 2017; 8: 1264.
Yang DC, Blair KM, Salama NR. Staying in shape: the impact of cell shape on bacterial survival in diverse environments. Microbiol Mol Biol Rev 2016; 80: 187-203.
Krzyżek P, Gościniak G. A proposed role for diffusible signal factors in the biofilm formation and morphological transformation of Helicobacter pylori. Turk J Gastroenterol 2018; 29: 7-13.
Chaput C, Ecobichon C, Cayet N, et al. Role of AmiA in the morphological transition of Helicobacter pylori and in immune escape. PLoS Pathog 2006; 2: e97.
Chaput C, Ecobichon C, Pouradier N, et al. Role of the N-acetylmuramoyl-l-alanyl amidase, AmiA, of Helicobacter pylori in peptidoglycan metabolism, daughter cell separation, and virulence. Microb Drug Resist 2016; 22: 477-86.
Zhao X, Zhong J, Wei C, et al. Current perspectives on viable but non-culturable state in foodborne pathogens. Front Microbiol 2017; 8: 580.
Li L, Mendis N, Trigui H, et al. The importance of the viable but non-culturable state in human bacterial pathogens. Front Microbiol 2014; 5: 258.
Enroth H, Engstrand L. Egg passage of rodshaped and coccoid forms of Helicobacter pylori: preliminary studies. Helicobacter 1996; 1: 183-6.
Shao C, Sun Y, Wang N, et al. Changes of proteome components of Helicobacter pylori biofilms induced by serum starvation. Mol Med Rep 2013; 8: 1761-6.
Nilsson HO, Blom J, Abu-Al-Soud W, et al. Effect of cold starvation, acid stress, and nutrients on metabolic activity of Helicobacter pylori. Appl Environ Microbiol 2002; 68: 11-9.
Cellini L, Allocati N, Di Campli E, et al. Helicobacter pylori: a fickle germ. Microbiol Immunol 1994; 38: 25-30.
Tominaga K, Hamasaki N, Watanabe T, et al. Effect of culture conditions on morphological changes of Helicobacter pylori. J Gastroenterol 1999; 34 Suppl: 28-31.
Jiang X, Doyle MP. Effect of environmental and substrate factors on survival and growth of Helicobacter pylori. J Food Prot 1998; 61: 929-33.
Catrenich CE, Makin KM. Characterization of the morphologic conversion of Helicobacter pylori from bacillary to coccoid forms. Scand J Gastroenterol 1991; 26: 58-64.
She FF, Lin JY, Liu JY, et al. Virulence of water-induced coccoid Helicobacter pylori and its experimental infection in mice. World J Gastroenterol 2003; 9: 516-20.
West AP, Millar MR, Tompkins DS. Survival of Helicobacter pylori in water and saline. J Clin Pathol 1990; 43: 609.
Bury-Mone S, Kaakoush NO, Asencio C, et al. Is Helicobacter pylori a true microaerophile? Helicobacter 2006; 11: 296-303.
Park SA, Ko A, Lee NG. Stimulation of growth of the human gastric pathogen Helicobacter pylori by atmospheric level of oxygen under high carbon dioxide tension. BMC Microbiol 2011; 11: 96.
Faghri J, Poursina F, Moghim S, et al. Morphological and bactericidal effects of different antibiotics on Helicobacter pylori. Jundishapur J Microbiol 2014; 7: e8704.
She FF, Su DH, Lin JY, et al. Virulence and potential pathogenicity of coccoid Helicobacter pylori induced by antibiotics. World J Gastroenterol 2001; 7: 254-8.
Saniee P, Shahreza S, Siavoshi F. Negative effect of proton-pump inhibitors (PPIs) on Helicobacter pylori growth, morphology, and urease test and recovery after PPI removal – an in vitro study. Helicobacter 2016; 21: 143-52.
Kim TS, Hur JW, Yu MA, et al. Antagonism of Helicobacter pylori by bacteriocins of lactic acid bacteria. J Food Prot 2003; 66: 3-12.
Le Moal VL, Fayol-Messaoudi D, Servin AL. Compound(s) secreted by Lactobacillus casei strain Shirota YIT9029 irreversibly and reversibly impair the swimming motility of Helicobacter pylori and Salmonella enterica serovar Typhimurium, respectively. Microbiology 2013; 159: 1956-71.
Khosravi Y, Dieye Y, Loke MF, et al. Streptococcus mitis induces conversion of Helicobacter pylori to coccoid cells during co-culture in vitro. PLoS One 2014; 9: e112214.
Janas B, Czkwianianc E, Bak-Romaniszyn L, et al. Electron microscopic study of association between coccoid forms of Helicobacter pylori and gastric epithelial cells. Am J Gastroenterol 1995; 90: 1829-33.
Chan WY, Hui PK, Leung KM, et al. Coccoid forms of Helicobacter pylori in the human stomach. Am J Clin Pathol 1994; 102: 503-7.
Balakrishna JP, Filatov A. Coccoid forms of Helicobacter pylori causing active gastritis. Am J Clin Pathol 2013; 140: A101.
Wang X, Sturegard E, Rupar R, et al. Infection of BALB/c A mice by spiral and coccoid forms of Helicobacter pylori. J Med Microbiol 1997; 46: 657-63.
Cellini L, Allocati N, Angelucci D, et al. Coccoid Helicobacter pylori not culturable in vitro reverts in mice. Microbiol Immunol 1994; 38: 843-50.
Loke MF, Ng CG, Vilashni Y, et al. Understanding the dimorphic lifestyles of human gastric pathogen Helicobacter pylori using the SWATH-based proteomics approach. Sci Rep 2016; 6: 26784.
Krzyżek P, Gościniak G. Oral Helicobacter pylori: interactions with host and microbial flora of the oral cavity. Dent Med Probl 2018; 55: 75-82.
Hirsch C, Tegtmeyer N, Rohde M, et al. Live Helicobacter pylori in the root canal of endodontic-infected deciduous teeth. J Gastroenterol 2012; 47: 936-40.
Waidner B, Specht M, Dempwolff F, et al. A novel system of cytoskeletal elements in the human pathogen Helicobacter pylori. PLoS Pathog 2009; 5: e1000669.
Fernandes RM, Silva H, Oliveira R, et al. Morphological transition of Helicobacter pylori adapted to water. Future Microbiol 2017; 12: 1167-79.
Aziz RK, Khalifa MM, Sharaf RR. Contaminated water as a source of Helicobacter pylori infection: a review. J Adv Res 2015; 6: 539-47.
Ranjbar R, Khamesipour F, Jonaidi-Jafari N, et al. Helicobacter pylori in bottled mineral water: genotyping and antimicrobial resistance properties. BMC Microbiol 2016; 16: 40.
Gancz H, Jones KR, Merrell DS. Sodium chloride affects Helicobacter pylori growth and gene expression. J Bacteriol 2008; 190: 4100-5.
Takeuchi H, Nakazawa T, Okamoto T, et al. Cell elongation and cell death of Helicobacter pylori is modulated by the disruption of cdrA (cell division-related gene A). Microbiol Immunol 2006; 50: 487-97.
Singh M, Prasad K, Yachha S. Elongated Helicobacter pylori in gastric mucosa of children associated with gastric disease. J Pediatr Infect Dis 2015; 3: 35-9.
Ingerson-Mahar M, Gitai Z. A growing family: the expanding universe of the bacterial cytoskeleton. FEMS Microbiol Rev 2012; 36: 256-66.
Cho H. The role of cytoskeletal elements in shaping bacterial cells. J Microbiol Biotechnol 2015; 25: 307-16.
Cabeen MT, Jacobs-Wagner C. Bacterial cell shape. Nat Rev Microbiol 2005; 3: 601-10.
Celler K, Koning RI, Koster AJ, et al. Multidimensional view of the bacterial cytoskeleton. J Bacteriol 2013; 195: 1627-36.
El Ghachi M, Matteï PJ, Ecobichon C, et al. Characterization of the elongasome core PBP2:MreC complex of Helicobacter pylori. Mol Microbiol 2011; 82: 68-86.
Zepeda G, Reyna C, Fu Y, et al. Novel protein interactions with an actin homolog (MreB) of Helicobacter pylori determined by bacterial two-hybrid system. Microbiol Res 2017; 201: 39-45.
Nishida Y, Takeuchi H, Morimoto N, et al. Intrinsic characteristics of Min proteins on the cell division of Helicobacter pylori. FEMS Microbiol Lett 2016; 363: fnw025.
Yu XC, Margolin W. Deletion of the min operon results in increased thermosensitivity of an ftsZ84 mutant and abnormal FtsZ ring assembly, placement, and disassembly. J Bacteriol 2000; 182: 6203-13.
Chiou PY, Luo CH, Chang KC, et al. Maintenance of the cell morphology by MinC in Helicobacter pylori. PLoS One 2013; 8: e71208.
Specht M, Schatzle S, Graumann PL, et al. Helicobacter pylori possesses four coiled-coil-rich proteins that form extended filamentous structures and control cell shape and motility. J Bacteriol 2011; 193: 4523-30.
Schätzle S, Specht M, Waidner B. Coiled coil rich proteins (Ccrp) influence molecular pathogenicity of Helicobacter pylori. PLoS One 2015; 10: e0121463.
Vollmer W. Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev 2008; 32: 287-306.
Typas A, Banzhaf M, Gross CA, et al. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 2011; 10: 123-36.
Cava F, de Pedro MA. Peptidoglycan plasticity in bacteria: Emerging variability of the murein sacculus and their associated biological functions. Curr Opin Microbiol 2014; 18: 46-53.
Scheffers DJ, Pinho MG. Bacterial cell wall synthesis: new insights from localization studies. Microbiol Mol Biol Rev 2005; 69: 585-607.
Kim HS, Kim J, Im HN, et al. Structural basis for the recognition of muramyltripeptide by Helicobacter pylori Csd4, a D,L-carboxypeptidase controlling the helical cell shape. Acta Crystallogr Sect D Biol Crystallogr 2014; 70: 2800-12.
An DR, Im HN, Jang JY, et al. Structural basis of the heterodimer formation between cell shape-determining proteins Csd1 and Csd2 from Helicobacter pylori. PLoS One 2016; 11: e0164243.
Sycuro LK, Rule CS, Petersen TW, et al. Flow cytometry-based enrichment for cell shape mutants identifies multiple genes that influence Helicobacter pylori morphology. Mol Microbiol 2013; 90: 869-83.
Bonis M, Ecobichon C, Guadagnini S, et al. A M23B family metallopeptidase of Helicobacter pylori required for cell shape, pole formation and virulence. Mol Microbiol 2010; 78: 809-19.
Kim HS, Im HN, An DR, et al. The cell shape-determining Csd6 protein from Helicobacter pylori constitutes a new family of L,D-carboxypeptidase. 2015; 290: 25103-17.
Hung WC, Jane WN, Wong HC. Association of a D-alanyl-D-alanine carboxypeptidase gene with the formation of aberrantly shaped cells during the induction of viable but nonculturable Vibrio parahaemolyticus. Appl Environ Microbiol 2013; 79: 7305-12.
Costa K, Bacher G, Allmaier G, et al. The morphological transition of Helicobacter pylori cells from spiral to coccoid is preceded by a substantial modification of the cell wall. J Bacteriol 1999; 181: 3710-5.
Esson D, Mather AE, Scanlan E, et al. Genomic variations leading to alterations in cell morphology of Campylobacter spp. Sci Rep 2016; 6: 38303.
Frirdich E, Vermeulen J, Biboy J, et al. Peptidoglycan LD-carboxypeptidase Pgp2 influences Campylobacter jejuni helical cell shape and pathogenic properties and provides the substrate for the DL-carboxypeptidase Pgp1. J Biol Chem 2014; 289: 8007-18.
Frirdich E, Biboy J, Adams C, et al. Peptidoglycan-modifying enzyme Pgp1 Is required for helical cell shape and pathogenicity traits in Campylobacter jejuni. PLoS Pathog 2012; 8: e1002602.
Hay NA, Tipper DJ, Gygi D, et al. A novel membrane protein influencing cell shape and multicellular swarming of Proteus mirabilis. J Bacteriol 1999; 181: 2008-16.
Constantino MA, Jabbarzadeh M, Fu HC, et al. Helical and rod-shaped bacteria swim in helical trajectories with little additional propulsion from helical shape. Sci Adv 2016; 2: e1601661.
Celli JP, Turner BS, Afdhal NH, et al. Helicobacter pylori moves through mucus by reducing mucin viscoelasticity. Proc Natl Acad Sci 2009; 106: 14321-6.
Austin CM, Maier RJ. Aconitase-mediated posttranscriptional regulation of Helicobacter pylori peptidoglycan deacetylase. J Bacteriol 2013; 195: 5316-22.
Wang G, Maier SE, Lo LF, et al. Peptidoglycan deacetylation in Helicobacter pylori contributes to bacterial survival by mitigating host immune responses. Infect Immun 2010; 78: 4660-6.
Wang G, Lo LF, Forsberg LS, et al. Helicobacter pylori peptidoglycan modifications confer lysozyme resistance and contribute to survival in the host. MBio 2012; 3: e00409-12.
Bush K. Antimicrobial agents targeting bacterial cell walls and cell membranes. Rev Sci Tech 2012; 31: 43-56.
Jovetic S, Zhu Y, Marcone GL, et al. Beta-Lactam and glycopeptide antibiotics: first and last line of defense? Trends Biotechnol 2010; 28: 596-604.
Mégraud F. Resistance of Helicobacter pylori to antibiotics. Aliment Pharmacol Ther 1997; 11: 43-53.
Nishizawa T, Suzuki H. Mechanisms of Helicobacter pylori antibiotic resistance and molecular testing. Front Mol Biosci 2014; 1: 19.
Tseng YS, Wu DC, Chang CY, et al. Amoxicillin resistance with beta-lactamase production in Helicobacter pylori. Eur J Clin Invest 2009; 39: 807-12.
Matteo MJ, Granados G, Olmos M, et al. Helicobacter pylori amoxicillin heteroresistance due to point mutations in PBP-1A in isogenic isolates. J Antimicrob Chemother 2008; 61: 474-7.
Gerrits MM, Godoy APO, Kuipers EJ, et al. Multiple mutations in or adjacent to the conserved penicillin-binding protein motifs of the penicillin-binding protein 1A confer amoxicillin resistance to Helicobacter pylori. Helicobacter 2006; 11: 181-7.
Liu Y, Frirdich E, Taylor JA, et al. A bacterial cell shape-determining inhibitor. ACS Chem Biol 2016; 11: 981-91.
Sychantha D, Jones CS, Little DJ, et al. In vitro characterization of the antivirulence target of Gram-positive pathogens, peptidoglycan O-acetyltransferase A (OatA). PLoS Pathog 2017; 13: e1006667.
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