Genetic microheterogeneity and phenotypic variation of Helicobacter pylori arginase in clinical isolates

BMC Microbiology

Volumn 7, Issue , 2007, Pages

  Hovey, Justin G ^a   Watson, Emily L ^b   Langford, Melanie L ^c   Hildebrandt, Ellen ^d   Bathala, Sangeetha ^a   Bolland, Jeffrey R ^e   Spadafora, Domenico ^a   Mendz, George L ^f   McGee, David J ^d  

^a UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

^b CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^d LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^e University of Alabama at Birmingham   (United States)

^f UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE; BACTERIAL DNA; BACTERIAL ENZYME; BACTERIAL PROTEIN; ROCF PROTEIN, HELICOBACTER PYLORI; SERINE; UNCLASSIFIED DRUG; UREASE;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CORRELATION ANALYSIS; DNA SEQUENCE; ENZYME ACTIVITY; GENETIC HETEROGENEITY; HELICOBACTER PYLORI; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC VARIATION; PROMOTER REGION; PROTEIN EXPRESSION; WESTERN BLOTTING; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; HELICOBACTER INFECTION; HUMAN; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHENOTYPE; PHYLOGENY; POLYACRYLAMIDE GEL ELECTROPHORESIS; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS;

HELICOBACTER PYLORI;

ARGINASE; BACTERIAL PROTEINS; BASE SEQUENCE; BLOTTING, WESTERN; CLONING, MOLECULAR; DNA, BACTERIAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC HETEROGENEITY; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHENOTYPE; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SERINE; UREASE; VARIATION (GENETICS);

EID: 34247534614     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-7-26     Document Type: Article

References (66)

1. Gastric Campylobacter-like organisms, gastritis, and peptic ulcer disease. MJ Blaser, Gastroenterology 1987 93 2 371 383 3297911
2. Helicobacter pylori and the pathogenesis of gastroduodenal inflammation. MJ Blaser, Journal of Infectious Diseases 1990 161 4 626 633 2181029
3. Pyloric Campylobacter infection and gastroduodenal disease. BJ Marshall DB McGechie PA Rogers RJ Glancy, Medical Journal of Australia 1985 142 8 439 444 3982346
4. Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii.[see comment]. A Nomura GN Stemmermann PH Chyou I Kato GI Perez-Perez MJ Blaser, New England Journal of Medicine 1991 325 16 1132 1136 1891021
5. Helicobacter pylori infection and the risk of gastric carcinoma. J Parsonnet GD Friedman DP Vandersteen Y Chang JH Vogelman N Orentreich RK Sibley, N Engl J Med 1991 325 16 1127 1131 1891020
6. PCR-based RFLP analysis of DNA sequence diversity in the gastric pathogen Helicobacter pylori. N Akopyanz NO Bukanov TU Westblom DE Berg, Nucleic Acids Research 1992 20 23 6221 6225 1361982 10.1093/nar/20.23.6221
7. DNA diversity among clinical isolates of Helicobacter pylori detected by PCR-based RAPD fingerprinting. N Akopyanz NO Bukanov TU Westblom S Kresovich DE Berg, Nucleic Acids Research 1992 20 19 5137 5142 1408828 10.1093/nar/20.19.5137
8. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. RA Alm LS Ling DT Moir BL King ED Brown PC Doig DR Smith B Noonan BC Guild BL deJonge G Carmel PJ Tummino A Caruso M Uria-Nickelsen DM Mills C Ives R Gibson D Merberg SD Mills Q Jiang DE Taylor GF Vovis TJ Trust, Nature 1999 397 6715 176 180 10.1038/16495 9923682
9. Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. Association of specific vacA types with cytotoxin production and peptic ulceration. JC Atherton P Cao RM Peek Jr. MK Tummuru MJ Blaser TL Cover, J Biol Chem 1995 270 30 17771 17777 10.1074/jbc.270.30.17771 7629077
10. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. S Censini C Lange Z Xiang JE Crabtree P Ghiara M Borodovsky R Rappuoli A Covacci, Proc Natl Acad Sci U S A 1996 93 25 14648 14653 8962108 10.1073/pnas.93.25.14648
11. Use of polymerase chain reaction-amplified Helicobacter pylori urease structural genes for differentiation of isolates. PA Foxall LT Hu HL Mobley, Journal of Clinical Microbiology 1992 30 3 739 741 1313051
12. Genotypical variation of Campylobacter pylori from gastric mucosa. JH Oudbier W Langenberg EA Rauws C Bruin-Mosch, Journal of Clinical Microbiology 1990 28 3 559 565 2324277
13. A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. N Salama K Guillemin TK McDaniel G Sherlock L Tompkins S Falkow, Proc Natl Acad Sci U S A 2000 97 26 14668 14673 11121067 10.1073/pnas.97.26. 14668
14. Typing of Campylobacter pylori by bacterial DNA restriction endonuclease analysis and determination of plasmid profile. AE Simor B Shames B Drumm P Sherman DE Low JL Penner, Journal of Clinical Microbiology 1990 28 1 83 86 2153701
15. Two different families of hopQ alleles in Helicobacter pylori. P Cao TL Cover, J Clin Microbiol 2002 40 12 4504 4511 12454143 10.1128/JCM.40.12.4504- 4511.2002
16. Heterogeneity of cag genotypes in Helicobacter pylori isolates from human biopsy specimens. ML Tomasini S Zanussi M Sozzi R Tedeschi G Basaglia P De Paoli, J Clin Microbiol 2003 41 3 976 980 12624018 10.1128/JCM.41.3.976-980.2003
17. Genotypic profile of the outer membrane proteins BabA and BabB in clinical isolates of Helicobacter pylori. JC Colbeck LM Hansen JM Fong JV Solnick, Infect Immun 2006 74 7 4375 4378 16790815 10.1128/IAI.00485-06
18. Multiple chromosomal loci for the babA gene in Helicobacter pylori. EE Hennig JM Allen TL Cover, Infect Immun 2006 74 5 3046 3051 16622249 10.1128/IAI.74.5.3046-3051.2006
19. Genetic organization and heterogeneity of the iceA locus of Helicobacter pylori. C Figueiredo WG Quint R Sanna E Sablon JP Donahue Q Xu GG Miller RM Peek Jr. MJ Blaser LJ van Doorn, Gene 2000 246 1-2 59 68 10.1016/S0378-1119(00) 00054-8 10767527
20. Population genetic analysis of Helicobacter pylori by multilocus enzyme electrophoresis: extensive allelic diversity and recombinational population structure. MF Go V Kapur DY Graham JM Musser, Journal of Bacteriology 1996 178 13 3934 3938 8682800
21. Genetic diversity of Helicobacter pylori.[erratum appears in Lancet 1997 Jan 4;349(9044):64]. RP Logan DE Berg, Lancet 1996 348 9040 1462 1463 10.1016/S0140-6736(05)65885-0 8942769
22. Pathological significance and molecular characterization of the vacuolating toxin gene of Helicobacter pylori. SH Phadnis D Ilver L Janzon S Normark TU Westblom, Infection & Immunity 1994 62 5 1557 1565
23. Panmictic structure of Helicobacter pylori demonstrated by the comparative study of six genetic markers. L Salaun C Audibert G Le Lay C Burucoa JL Fauchere B Picard, FEMS Microbiol Lett 1998 161 2 231 239 9570115
24. Single-step PCR amplification and enzyme restriction analysis of the entire Helicobacter pylori cytotoxin vacA gene for genetic variability studies. G Perales J Sanchez A Mohar R Lara-Lemus A Hernandez R Herrera-Goepfert I Barrios-Jacobo G Ayala, FEMS Microbiology Letters 1999 178 1 55 62 10.1111/j.1574-6968.1999.tb13759.x 10483723
25. The vacuolating cytotoxin of Helicobacter pylori. TL Cover, Mol Microbiol 1996 20 2 241 246 10.1111/j.1365-2958.1996.tb02612.x 8733223
26. Evidence of gastritis with several Helicobacter pylori strains. A Beji P Vincent I Darchis MO Husson A Cortot H Leclerc, Lancet 1989 2 8676 1402 1403 10.1016/S0140-6736(89)92020-5 2574351
27. Quasispecies development of Helicobacter pylori observed in paired isolates obtained years apart from the same host. EJ Kuipers DA Israel JG Kusters MM Gerrits J Weel A van Der Ende RW van Der Hulst HP Wirth J Hook-Nikanne SA Thompson MJ Blaser, J Infect Dis 2000 181 1 273 282 10.1086/315173 10608776
28. Helicobacter pylori genetic diversity within the gastric niche of a single human host. DA Israel N Salama U Krishna UM Rieger JC Atherton S Falkow RM Peek Jr., Proc Natl Acad Sci U S A 2001 98 25 14625 14630 11724955 10.1073/pnas.251551698
29. Mechanisms of Helicobacter pylori infection: bacterial factors. DJ McGee HL Mobley, Curr Top Microbiol Immunol 1999 241 155 180 10087661
30. Urea protects Helicobacter (Campylobacter) pylori from the bactericidal effect of acid. BJ Marshall LJ Barrett C Prakash RW McCallum RL Guerrant, Gastroenterology 1990 99 3 697 702 2379775
31. The role of Helicobacter pylori urease in the pathogenesis of gastritis and peptic ulceration. HL Mobley, Alimentary Pharmacology & Therapeutics 1996 10 Suppl 1 57 64 8730260
32. Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets. KA Eaton CL Brooks DR Morgan S Krakowka, Infect Immun 1991 59 7 2470 2475 2050411
33. Effect of gastric pH on urease-dependent colonization of gnotobiotic piglets by Helicobacter pylori. KA Eaton S Krakowka, Infect Immun 1994 62 9 3604 3607 8063376
34. Identification of the urease operon in Helicobacter pylori and its control by mRNA decay in response to pH. JK Akada M Shirai H Takeuchi M Tsuda T Nakazawa, Mol Microbiol 2000 36 5 1071 1084 10.1046/j.1365-2958.2000.01918.x 10844692
35. Helicobacter pylori rocF is required for arginase activity and acid protection in vitro but is not essential for colonization of mice or for urease activity. DJ McGee FJ Radcliff GL Mendz RL Ferrero HL Mobley, J Bacteriol 1999 181 23 7314 7322 10572136
36. The urea cycle of Helicobacter pylori. GL Mendz SL Hazell, Microbiology 1996 142 ( Pt 10) 2959 2967 8885413
37. In situ characterization of Helicobacter pylori arginase. GL Mendz EM Holmes RL Ferrero, Biochim Biophys Acta 1998 1388 2 465 477 9858781
38. Aminoacid utilization by Helicobacter pylori. GL Mendz SL Hazell, Int J Biochem Cell Biol 1995 27 10 1085 1093 10.1016/1357-2725(95)00069-2 7496998
39. Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: a strategy for bacterial survival. AP Gobert DJ McGee M Akhtar GL Mendz JC Newton Y Cheng HL Mobley KT Wilson, Proc Natl Acad Sci U S A 2001 98 24 13844 13849 11717441 10.1073/pnas.241443798
40. Helicobacter pylori arginase inhibits T cell proliferation and reduces the expression of the TCR z-chain (CD3z). J Zabaleta DJ McGee AH Zea CP Hernandez PC Rodriguez RA Sierra P Correa AC Ochoa, J Immunol 2004 173 1 586 593 15210820
41. Purification and characterization of urease from Helicobacter pylori. BE Dunn GP Campbell GI Perez-Perez MJ Blaser, Journal of Biological Chemistry 1990 265 16 9464 9469 2188975
42. The urease enzymes of Campylobacter pylori and a related bacterium. RL Ferrero SL Hazell A Lee, Journal of Medical Microbiology 1988 27 1 33 40 3172169
43. Purification and characterization of Helicobacter pylori arginase, RocF: unique features among the arginase superfamily. DJ McGee J Zabaleta RJ Viator TL Testerman AC Ochoa GL Mendz, Eur J Biochem 2004 271 10 1952 1962 10.1111/j.1432-1033.2004.04105.x 15128304
44. In Vitro and In Vivo Complementation of the Helicobacter pylori Arginase Mutant Using an Intergenic Chromosomal Site. ML Langford J Zabaleta AC Ochoa TL Testerman DJ McGee, Helicobacter 2006 11 5 477 493 10.1111/j.1523-5378.2006. 00441.x 16961811
45. The complete genome sequence of a chronic atrophic gastritis Helicobacter pylori strain: evolution during disease progression. JD Oh H Kling-Backhed M Giannakis J Xu RS Fulton LA Fulton HS Cordum C Wang G Elliott J Edwards ER Mardis LG Engstrand JI Gordon, Proc Natl Acad Sci U S A 2006 103 26 9999 10004 16788065 10.1073/pnas.0603784103
46. Who ate whom? Adaptive Helicobacter genomic changes that accompanied a host jump from early humans to large felines. M Eppinger C Baar B Linz G Raddatz C Lanz H Keller G Morelli H Gressmann M Achtman SC Schuster, PLoS Genet 2006 2 7 e120 16789826 10.1371/journal.pgen.0020120
47. Characteristics of Helicobacter pylori growth in a defined medium and determination of its amino acid requirements. DJ Reynolds CW Penn, Microbiology 1994 140 ( Pt 10) 2649 2656 8000535
48. Nutritional requirements and antibiotic resistance patterns of Helicobacter species in chemically defined media. TL Testerman PB Conn HL Mobley DJ McGee, J Clin Microbiol 2006 44 5 1650 1658 16672389 10.1128/JCM.44.5.1650- 1658.2006
49. Helicobacter pylori growth and urease detection in the chemically defined medium Ham's F-12 nutrient mixture. TL Testerman DJ McGee HL Mobley, J Clin Microbiol 2001 39 11 3842 3850 11682496 10.1128/JCM.39.11.3842-3850.2001
50. Free recombination within Helicobacter pylori. S Suerbaum JM Smith K Bapumia G Morelli NH Smith E Kunstmann I Dyrek M Achtman, Proc Natl Acad Sci U S A 1998 95 21 12619 12624 9770535 10.1073/pnas.95.21.12619
51. The complete genome sequence of the gastric pathogen Helicobacter pylori. JF Tomb O White AR Kerlavage RA Clayton GG Sutton RD Fleischmann KA Ketchum HP Klenk S Gill BA Dougherty K Nelson J Quackenbush L Zhou EF Kirkness S Peterson B Loftus D Richardson R Dodson HG Khalak A Glodek K McKenney LM Fitzegerald N Lee MD Adams EK Hickey DE Berg JD Gocayne TR Utterback JD Peterson JM Kelley MD Cotton JM Weidman C Fujii C Bowman L Watthey E Wallin WS Hayes M Borodovsky PD Karp HO Smith CM Fraser JC Venter, Nature 1997 388 6642 539 547 10.1038/41483 9252185
52. Heterogeneity among Helicobacter pylori strains in expression of the outer membrane protein BabA. EE Hennig R Mernaugh J Edl P Cao TL Cover, Infect Immun 2004 72 6 3429 3435 15155649 10.1128/IAI.72.6.3429-3435.2004
53. Influence of EPIYA-repeat polymorphism on the phosphorylation-dependent biological activity of Helicobacter pylori CagA. M Naito T Yamazaki R Tsutsumi H Higashi K Onoe S Yamazaki T Azuma M Hatakeyama, Gastroenterology 2006 130 4 1181 1190 10.1053/j.gastro.2005.12.038 16618412
54. Distinct variants of Helicobacter pylori cagA are associated with vacA subtypes. LJ van Doorn C Figueiredo R Sanna MJ Blaser WG Quint, J Clin Microbiol 1999 37 7 2306 2311 10364602
55. Characterization of the ArsRS regulon of Helicobacter pylori, involved in acid adaptation. M Pflock N Finsterer B Joseph H Mollenkopf TF Meyer D Beier, Journal of Bacteriology 2006 188 10 3449 3462 16672598 10.1128/JB.188.10.3449- 3462.2006
56. Acid-adaptive genes of Helicobacter pylori. Y Wen EA Marcus U Matrubutham MA Gleeson DR Scott G Sachs, Infect Immun 2003 71 10 5921 5939 14500513 10.1128/IAI.71.10.5921-5939.2003
57. The Helicobacter pylori flbA flagellar biosynthesis and regulatory gene is required for motility and virulence and modulates urease of H. pylori and Proteus mirabilis. DJ McGee C Coker TL Testerman JM Harro SV Gibson HL Mobley, J Med Microbiol 2002 51 11 958 970 12448680
58. Isolation of Helicobacter pylori genes that modulate urease activity. DJ McGee CA May RM Garner JM Himpsl HL Mobley, J Bacteriol 1999 181 8 2477 2484 10198012
59. Molecular Cloning: A Laboratory Manual. J Sambrook E. F. Fritsch, and T. Maniatis., Cold Spring Harbor, N. Y., Laboratory. CSH, 2nd 1989
60. National Center for Biotechnology Information. http://www.ncbi.nlm.nih. gov
61. ExPASy Proteomics Server. http://us.expasy.org
62. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. JD Thompson Higgins, D.G. and Gibson, T.J., Nucleic Acids Research 1994 22 4673 4680 7984417 10.1093/nar/22.22.4673
63. European Bioinformatics Institute: ClustalW. http://www.ebi.ac.uk/ clustalw/
64. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. JD Thompson Gibson,T.J., Plewniak,F., Jeanmougin,F. and Higgins,D.G., Nucleic Acids Research 1997 24 4876 4882 10.1093/nar/25.24.4876
65. Rod Page's Home Page. http://taxonomy.zoology.gla.ac.uk/rod/rod.html
66. TREEVIEW: An application to display phylogenetic trees on personal computers. RDM Page, Computer Applications in the Biosciences 1996 12 357 358 8902363