Positive selection on a bacterial oncoprotein associated with gastric cancer

Gut Pathogens

Steven E Massey¹  Maria Gloria Dominguez-Bello¹  Gisela Delgado-Rosado¹ 

[1] Biology Department, University of Puerto Rico - Rio Piedras, PO Box 23360, San Juan, Puerto Rico, USA 00931

关键词: cagA;    Helicobacter pylori;    positive selection;    oncogene;    gastric cancer;   

Others  :  828863
DOI  :  10.1186/1757-4749-3-18

 received in 2011-09-27, accepted in 2011-11-11,  发布年份 2011

【 授权许可】

   
2011 Delgado-Rosado et al; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Bik EM, et al.: Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci USA 2006, 103:732-737.
• [2]Mbulaiteye SM, Hisada M, El-Omar EM: Helicobacter pylori associated global gastric cancer burden. Front Biosci 2009, 14:1490-1504.
• [3]Linz B, et al.: An African origin for the intimate association between humans and Helicobacter pylori. Nature 2007, 445:915-918.
• [4]Gueneau P, Loiseaux-De Goer S: Helicobacter: molecular phylogeny and the origin of gastric colonization in the genus. Infect, Gen and Evol 2002, 1:215-223.
• [5]Weeks DL, Eskandari S, Scott DR, Sachs G: A H+-gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 2000, 287:482-485.
• [6]Censini S, Lange C, Xiang Z, Crabtree JE, Ghiara P, Borodovsky M, Rappuoli R, Covacci A: Cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci USA 1996, 93:14648-14653.
• [7]Tummuru MK, Cover TL, Blaser MJ: Cloning and expression of a high-molecular-mass major antigen of Helicobacter pylori: evidence of linkage to cytotoxin production. Infect Immun 1993, 61:1799-1809.
• [8]Gressman H, Linz B, Ghai R, Schlapbach R, Yamaoka Y, Kraft C, Suerbaum S, Meyer TF, Achtman M: Gain and loss of multiple genes during the evolution of Helicobacter pylori. PloS Gen 2005, 1:e43.
• [9]Blaser MJ, Perez-Perez GI, Kleanthous H, Cover TL, Peek RM, Chyou PH, Stemmermann GN, Nomura A: Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 1995, 55:2111-2115.
• [10]Nomura N, Lee J, Stemmermann GN, Nomura RY, Perez-Perez GI, Blaser MJ: Helicobacter pylori CagA seropositivity and gastric carcinoma risk in a Japanese American population. J Infect Dis 2002, 186:1138-1144.
• [11]Personnet J, Friedman GD, Orentreich N, Vogelman H: Risk for gastric cancer in people with CagA positive or CagA negative Helicobacter pylori infection. Gut 1997, 40:297-301.
• [12]Parkin DM, Bray F, Ferlay J, Pisani P: Global cancer statistics, 2002. CA Cancer J Clin 2005, 55:74-108.
• [13]Atherton JC, Blaser MJ: Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. J Clin Invest 2009, 119:2475-2487.
• [14]Backert S, Selbach M: Role of type IV secretion in Helicobacter pylori pathogenesis. Cell Microbiol 2008, 10:1573-1581.
• [15]Selbach M, Moese S, Hauck CR, Meyer TF, Backert S: Src is the kinase of the Helicobacter pylori CagA protein in vitro and in vivo. J Biol Chem 2002, 277:6775-6778.
• [16]Stein M, Bagnoli F, Halenbeck R, Rappuoli R, Fantl WJ, Covacci A: c-Src/Lyn kinases activate Helicobacter pylori CagA through tyrosine phosphorylation of the EPIYA motifs. Mol Microbiol 2002, 43:971-980.
• [17]Poppe M, Feller SM, Römer G, Wessler S: Phosphorylation of Helicobacter pylori CagA by c-Abl leads to cell motility. Oncogene 2007, 26:3462-3472.
• [18]Higashi H, Tsutsumi R, Muto S, Sugiyama T, Azuma T, Asaka M, Hatakeyama M: SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 2002, 295:683-686.
• [19]Saadat I, Higashi H, Obuse C, Umeda M, Murata-Kamiya N, Saito Y, Lu H, Ohnishi N, Azuma T, Suzuki A, Ohno S, Hatakeyama M: Helicobacter pylori CagA targets PAR1/MARK kinase to disrupt epithelial cell polarity. Nature 2007, 447:330-333.
• [20]Mimuro H, Suzuki J, Tanaka J, Asahi M, Haas R, Sasakawa H: Grb2 is a key mediator of Helicobacter pylori CagA protein activities. Mol Cell 2002, 10:745-755.
• [21]Churin Y, Al-Ghoul L, Kepp O, Meyer TF, Birchmeier W, Naumann M: Helicobacter pylori CagA protein targets the c-Met receptor and enhances the motogenic response. J Cell Biol 2003, 161:249-255.
• [22]Tsutsumi R, Higashi H, Higuchi M, Okada M, Hatakeyama M: Attenuation of Helicobacter pylori CagA °-- SHP-2 signaling by interaction between CagA and C-terminal Src kinase. J Biol Chem 2003, 278:3664-3670.
• [23]Suzuki M, Mimuro H, Suzuki T, Park M, Yamamoto T, Sasakawa C: Interaction of CagA with Crk plays an important role in Helicobacter pylori induced loss of gastric epithelial cell adhesion. J Exp Med 2005, 202:1235-1247.
• [24]Hatakeyama M: Helicobacter pylori CagA--a potential bacterial oncoprotein that functionally mimics the mammalian Gab family of adaptor proteins. Microbes and Infections 2003, 5:143-150.
• [25]Botham CM, Wandler AM, Guillemin K: A transgenic Drosophila model demonstrates that the Helicobacter pylori CagA protein functions as a eukaryotic Gab adaptor. PLOS Pathogens 2008, 4:e1000064.
• [26]Segal ED, Cha J, Lo J, Falkow S, Tompkins LS: Altered states: Involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc Natl Acad Sci USA 1999, 96:14559-14564.
• [27]Brandt S, Kwok T, Hartig R, Konig W, Backert S: NF-kappaB activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc Natl Acad Sci USA 2005, 102:9300-9305.
• [28]Higashi H, Tsutsumi R, Fujita A, Yamazaki S, Asaka M, Azuma T, Hatakeyama M: Biological activity of the Helicobacter pylori virulence factor CagA is determined by variation in the tyrosine phosphorylation sites. Proc Natl Acad Sci USA 2002, 99:14428-14433.
• [29]Falush D, et al.: Traces of human migrations in Helicobacter pylori populations. Science 2003, 299:1582-1585.
• [30]Katoh K, Kuma K, Toh H, Miyata T: MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nuc Acid Res 2005, 33:511-518.
• [31]Suyama M, Torrents D, Bork P: PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nuc Acids Res 2006, 34:W609-W612.
• [32]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
• [33]Posada D: jModelTest: Phylogenetic Model Averaging. Mol Biol Evol 2008, 25:1253-1256.
• [34]Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24:1586-1591.
• [35]Yang Z: Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 1998, 15:568-573.
• [36]Nielsen R, Yang Z: Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 1998, 148:929-936.
• [37]Yang Z, Nielsen R: Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 2002, 19:908-917.
• [38]Anisimova M, Yang Z: Multiple hypothesis testing to detect lineages under positive selection that affects only a few sites. Mol Biol Evol 2007, 24:1219-1228.
• [39]Yang Z, Wong WSW, Nielsen R: Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 2005, 22:1107-1118.
• [40]Olberman P, Josenhans C, Moodley Y, Uhr M, Stamer C, Vauterin M, Suerbaum S, Achtman M, Linz B: A global overview of the genetic and functional diversity in the Helicobacter pylori cag pathogenicity island. PloS Genet 2010, 19:e1001069.
• [41]Dominguez-Bello MG, Blaser MJ: The human microbiota as a marker for migrations of individuals and populations. Ann Rev Anthropol 2011, 40:451-474.
• [42]Devi SM, Ahmed I, Francalacci P, Hussain MA, Akhter Y, Alvi A, Sechi LA, Megraud F, Ahmed N: Ancestral European roots of Helicobacter pylori in India. BMC Genomics 2007, 8:184. BioMed Central Full Text
• [43]Breurec S, et al.: Evolutionary history of Helicobacter pylori sequences reflect past human migrations in southeast asia. PLoS One 2011, 6:e22058.
• [44]Torres-Morquecho A, Giono-Cerezo S, Camorlinga-Ponce M, Vargas-Mendoza CF, Torres J: Evolution of bacterial genes: evidence of positive Darwinian selection and fixation of base substitutions in virulence genes of Helicobacter pylori. Inf, Genetics and Evol 2010, 10:764-776.
• [45]Smith NH, Maynard Smith J, Spratt BG: Sequence Evolution of the porB Gene of Neisseria gonorrhoeae and Neisseria meningitidis: Evidence of Positive Darwinian Selection. Mol Biol Evol 1995, 12:363-370.
• [46]Petersen L, Bollback JP, Dimmic M, Hubisz M, Nielsen R: Genes under positive selection in Escherichia coli. Genome Res 2007, 17:1336-1343.
• [47]Ogura M, Perez JC, Mittl PRE, Dailide G, Tan S, Ito Y, Secka O, Dailidiene D, Putty K, Berg DE, Kalia A: Helicobacter pylori evolution: lineage-specific adaptations in homologs of eukaryotic Sel1-like genes. PloS Comp Biol 2007, 3:e151.
• [48]Bonatto SL, Salzano FM: A single and early migration for the peopling of the Americas supported by mitochondrial DNA sequence data. Proc Natl Acad Sci USA 1997, 94:1866-1871.
• [49]Oota H, Kitano T, Jin F, Yuasa I, Wang L, Ueda S, Saitou N, Stoneking M: Extreme mtDNA homogeneity in continental asian populations. Am J Phys Anthropol 2002, 118:146-153.
• [50]Liu H, Prugnolle F, Manica A, Balloux F: A geographically explicit genetic model of worldwide human-settlement history. Am J Hum Genet 2006, 79:230-237.
• [51]dos Reis M, Savva R, Wernisch L: Solving the riddle of codon usage preferences: a test for translational selection. Nuc Acids Res 2004, 32:5036-5044.
• [52]Parmley JL, Hurst L: How common are intragene windows with Ka > Ks owing to purifying selection on synonymous mutations? J Mol Evol 2007, 64:646-655.
• [53]El-Omar EM, Carrington M, Chow WH, McColl KE, Bream JH, Young HA, Herrera J, Lissowska J, Yuan CC, Rothman N, Lanyon G, Martin M, Fraumeni JF Jr, Rabkin CS: Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 2000, 404:398-402.
• [54]Dominguez-Bello MG, Perez ME, Bortolini MC, Salzano FM, Pericchi LR, Zambrano-Guzman O, Linz B: Amerindian Helicobacter pylori strains go extinct, as European strains expand their host range. PloS One 2008, 3:e3307.
• [55]Aspholm-Hurtig M, Dailide G, Lahmann M, Kalia A, Ilver D, et al.: Functional adaptation of BabA, the H pylori ABO blood group antigen binding adhesin. Science 2004, 305:519-522.
• [56]Crabtree JE, Covacci A, Farmery SM, Xiang Z, Tompkins DS, Perry S, Lindley IJD, Rappuoli R: Helicobacter pylori induced interleukin-8 expression in gastric epithelial cells is associated with CagA positive phenotype. J Clin Pathol 1995, 48:41-45.
• [57]Peek RMJ, Miller GG, Tham KT, Perez-Perez GI, Zhao X, Atherton JC, Blaser MJ: Heightened inflammatory response and cytokine expression in vivo to cagA+Helicobacter pylori strains. Lab Invest 1995, 71:760-770.
• [58]Yamaoka Y, Kita M, Kodama T, Sawai N, Kashima K, Imanishi J: Induction of various cytokines and development of severe mucosal inflammation by cagA gene positive Helicobacter pylori strains. Gut 1997, 41:442-451.
• [59]Baldary CT, Lanzavecchia A, Telford JL: Immune subversion by Helicobacter pylori. Trends Immun 2005, 26:199-207.
• [60]Prinz C, Schwendy S, Voland P: Hpylori and gastric cancer: shifting the global burden. World J Gastroenterol 2006, 12:5458-5464.
• [61]Bravo LE, van Doom LJ, Realpe JL, Correa P: Virulence-associated genotypes of Helicobacter pylori: do they explain the African enigma? Am J Gastroenterol 2002, 97:2899-2842.
• [62]Breurec S, et al.: Expansion of European vacA and cagA alleles to East Asian Helicobacter pylori strains in Cambodia. Infect Genet Evol 2011, in press.
• [63]Juhas M, van der Meer JR, Gaillard M, Harding RM, Hood DW, Crook DW: Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 2009, 33:376-393.
• [64]Burrows JM, Bromham L, Woolfit M, Piganeau G, Tellam J, Connolly G, Webb N, Poulsen L, Cooper L, Burrows SR, Moss DJ, Haryana SM, Ng M, Nicholls JM, Khanna R: Selection pressure-driven evolution of the Epstein-Barr virus encoded oncogene LMP1 in virus isolates from Southeast Asia. J Virol 2004, 78:7131-7137.
• [65]DeFilippis VR, Ayala FJ, Villarreal LP: Evidence of diversifying selection in human papillomavirus type 16 E6 but not E7 oncogenes. J Mol Evol 2002, 55:491-499.
• [66]Chen Z, Terai M, Fu L, Herrero R, DeSalle R, Burk RD: Diversifying selection in human papillomavirus type 16 lineages based on complete genome analyses. J Virol 2005, 79:7014-7023.
• [67]Anderson RM, May RM: Coevolution of hosts and parasites. Parasitology 1982, 85:411-426.
• [68]Lenski RE, May RM: The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. J Theor Biol 1994, 169:253-265.
• [69]Fine PEM: Vectors and vertical transmission: an epidemiologic perspective. Ann NY Acad Sci 1975, 266:173-194.
• [70]Hamilton WD: The genetical evolution of social behaviour I and II --. Journal of Theoretical Biology 1964, 7:1-16. 17-52
• [71]Blaser MJ: Disappearing microbiota Helicobacter pylori protection against esophageal adenocarcinoma. Cancer Prev Res (Phila Pa) 2008, 1:308-311.
• [72]Islami F, Kamangar F: Helicobacter pylori and esophageal cancer risk: a meta-analysis. Cancer Prev Res (Phila Pa) 2008, 1:329-338.
• [73]Christie J, Shepherd N, Codling B, Valori R: Gastric cancer below the age of 55: implications for screening patients with uncomplicated dyspepsia. Gut 1997, 41:513-517.
• [74]Chen Y, Blaser MJ: Inverse associations of Helicobacter pylori with asthma and allergy. Arch Intern Med 2007, 167:821-827.
• [75]Chen Y, Blaser MJ: Helicobacter pylori colonization is inversely associated with childhood asthma. J Infect Dis 2008, 198:553-560.
• [76]Codolo G, et al.: The neutrophil-activating protein of Helicobacter pylori down-modulates Th2 inflammation in ovalbumin-induced allergic asthma. Cell Microbiol 2008, 10:2355-2363.
• [77]Kamada T, Hata J, Kusonoki H, Ito M, Tanaka S, Kawamura Y, Chayama K, Haruma K: Eradication of Helicobacter pylori increases the incidence of hyperlipidaemia and obesity in peptic ulcer patients. Dig Liver Dis 2005, 37:39-43.
• [78]Rothenbascher D, Blaser MJ, Bode G, Brenner H: Inverse relationship between gastric colonization of Helicobacter pylori and diarrheal illnesses in children: results of a population-based cross-sectional study. J Infect Dis 2000, 182:1446-1449.
• [79]Baron JH, Sonnenberg A: Period- and cohort-age contours of deaths from gastric and duodenal ulcer in New York 1804-1998. Am J Gastroenterol 2001, 96:2887-2891.
• [80]Herrera PM, Mendez M, Velapatio B, Santivaez L, Balqui J, Finger SA, Sherman J, Zimic M, Cabrera L, Watanabe J, Rodriguez C, Gilman RH, Berg DE: DNA-level diversity and relatedness of Helicobacter pylori strains in shantytown families in Peru and transmission in a developing country setting. J Clin Microbiol 2008, 46:3912-3918.
• [81]Schwarz S, Morelli G, Kusecek B, Manica A, Balloux F, Owen RJ, Graham DY, van der Merwe S, Achtman M, Suerbaum S: Horizontal versus familial transmission of Helicobacter pylori. PloS Pathogens 2008, 4:e1000180.
• [82]Librado P, Rozas J: DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
• [83]Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986, 3:418-426.