Abstract
The innate immune response is a critical hallmark of Helicobacter pylori infection. Epithelial and myeloid cells produce effectors, including the chemokine CXCL8, reactive oxygen species (ROS), and nitric oxide (NO), in response to bacterial components. Mechanistic and epidemiologic studies have emphasized that dysregulated and persistent release of these products leads to the development of chronic inflammation and to the molecular and cellular events related to carcinogenesis. Moreover, investigations in H. pylori-infected patients about polymorphisms of the genes encoding CXCL8 and inducible NO synthase, and epigenetic control of the ROS-producing enzyme spermine oxidase, have further proven that overproduction of these molecules impacts the severity of gastric diseases. Lastly, the critical effect of the crosstalk between the human host and the infecting bacterium in determining the severity of H. pylori-related diseases has been supported by phylogenetic analysis of the human population and their H. pylori isolates in geographic areas with varying clinical and pathologic outcomes of the infection.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Allen LA, Beecher BR, Lynch JT, Rohner OV, Wittine LM (2005) Helicobacter pylori disrupts NADPH oxidase targeting in human neutrophils to induce extracellular superoxide release. J Immunol 174(6):3658–3667. doi:10.4049/jimmunol.174.6.3658
Allison CC, Kufer TA, Kremmer E, Kaparakis M, Ferrero RL (2009) Helicobacter pylori induces MAPK phosphorylation and AP-1 activation via a NOD1-dependent mechanism. J Immunol 183(12):8099–8109. doi:10.4049/jimmunol.0900664
Ando T, Kusugami K, Ohsuga M, Shinoda M, Sakakibara M, Saito H, Fukatsu A, Ichiyama S, Ohta M (1996) Interleukin-8 activity correlates with histological severity in Helicobacter pylori-associated antral gastritis. Am J Gastroenterol 91(6):1150–1156
Ando T, Yoshida T, Enomoto S, Asada K, Tatematsu M, Ichinose M, Sugiyama T, Ushijima T (2009) DNA methylation of microRNA genes in gastric mucosae of gastric cancer patients: its possible involvement in the formation of epigenetic field defect. Int J Cancer 124(10):2367–2374. doi:10.1002/ijc.24219
Antos D, Enders G, Rieder G, Stolte M, Bayerdorffer E, Hatz RA (2001) Inducible nitric oxide synthase expression before and after eradication of Helicobacter pylori in different forms of gastritis. FEMS Immunol Med Microbiol 30(2):127–131. doi:10.1111/j.1574-695X.2001.tb01560.x
Asfaha S, Dubeykovskiy AN, Tomita H, Yang X, Stokes S, Shibata W, Friedman RA, Ariyama H, Dubeykovskaya ZA, Muthupalani S, Ericksen R, Frucht H, Fox JG, Wang TC (2013) Mice that express human interleukin-8 have increased mobilization of immature myeloid cells, which exacerbates inflammation and accelerates colon carcinogenesis. Gastroenterology 144(1):155–166. doi:10.1053/j.gastro.2012.09.057
Atherton JC, Peek RM Jr, Tham KT, Cover TL, Blaser MJ (1997) Clinical and pathological importance of heterogeneity in vacA, the vacuolating cytotoxin gene of Helicobacter pylori. Gastroenterology 112(1):92–99. doi:10.1016/S0016-5085(97)70223-3
Belogolova E, Bauer B, Pompaiah M, Asakura H, Brinkman V, Ertl C, Bartfeld S, Nechitaylo TY, Haas R, Machuy N, Salama N, Churin Y, Meyer TF (2013) Helicobacter pylori outer membrane protein HopQ identified as a novel T4SS-associated virulence factor. Cell Microbiol 15(11):1896–1912. doi:10.1111/cmi.12158
Betten A, Bylund J, Christophe T, Boulay F, Romero A, Hellstrand K, Dahlgren C (2001) A proinflammatory peptide from Helicobacter pylori activates monocytes to induce lymphocyte dysfunction and apoptosis. J Clin Invest 108(8):1221–1228. doi:10.1172/JCI13430
Bhattacharyya A, Pathak S, Datta S, Chattopadhyay S, Basu J, Kundu M (2002) Mitogen-activated protein kinases and nuclear factor-kappaB regulate Helicobacter pylori-mediated interleukin-8 release from macrophages. Biochem J 368(Pt 1):121–129. doi:10.1042/BJ20020555
Blanchard TG, Yu F, Hsieh CL, Redline RW (2003) Severe inflammation and reduced bacteria load in murine helicobacter infection caused by lack of phagocyte oxidase activity. J Infect Dis 187(10):1609–1615. doi:10.1086/374780
Brandt S, Kwok T, Hartig R, Konig W, Backert S (2005) NF-kappaB activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc Natl Acad Sci U S A 102(26):9300–9305. doi:10.1073/pnas.0409873102
Byun E, Lim JW, Kim JM, Kim H (2014) Alpha-lipoic acid inhibits Helicobacter pylori-induced oncogene expression and hyperproliferation by suppressing the activation of NADPH oxidase in gastric epithelial cells. Mediat Inflamm 2014:380830. doi:10.1155/2014/380830
Canedo P, Castanheira-Vale AJ, Lunet N, Pereira F, Figueiredo C, Gioia-Patricola L, Canzian F, Moreira H, Suriano G, Barros H, Carneiro F, Seruca R, Machado JC (2008) The interleukin-8-251*T/*A polymorphism is not associated with risk for gastric carcinoma development in a Portuguese population. Eur J Cancer Prev 17(1):28–32. doi:10.1097/CEJ.0b013e32809b4d0f
Chaturvedi R, Cheng Y, Asim M, Bussiere FI, Xu H, Gobert AP, Hacker A, Casero RA Jr, Wilson KT (2004) Induction of polyamine oxidase 1 by Helicobacter pylori causes macrophage apoptosis by hydrogen peroxide release and mitochondrial membrane depolarization. J Biol Chem 279(38):40161–40173. doi:10.1074/jbc.M401370200
Chaturvedi R, Asim M, Hoge S, Lewis ND, Singh K, Barry DP, de Sablet T, Piazuelo MB, Sarvaria AR, Cheng Y, Closs EI, Casero RA Jr, Gobert AP, Wilson KT (2010) Polyamines impair immunity to Helicobacter pylori by inhibiting L-Arginine uptake required for nitric oxide production. Gastroenterology 139(5):1686–1698. doi:10.1053/j.gastro.2010.06.060
Chaturvedi R, Asim M, Romero-Gallo J, Barry DP, Hoge S, de Sablet T, Delgado AG, Wroblewski LE, Piazuelo MB, Yan F, Israel DA, Casero Jr RA, Correa P, Gobert AP, Polk DB, Peek Jr RM, Wilson KT (2011) Spermine oxidase mediates the gastric cancer risk associated with Helicobacter pylori CagA. Gastroenterology 141(5):1696–1708, e1691–1692. doi:10.1053/j.gastro.2011.07.045
Chaturvedi R, Asim M, Piazuelo MB, Yan F, Barry DP, Sierra JC, Delgado AG, Hill S, Casero Jr RA, Bravo LE, Dominguez RL, Correa P, Polk DB, Washington MK, Rose KL, Schey KL, Morgan DR, Peek Jr RM, Wilson KT (2014) Activation of EGFR and ERBB2 by Helicobacter pylori results in survival of gastric epithelial cells with DNA damage. Gastroenterology 146(7):1739–1751, e1714. doi:10.1053/j.gastro.2014.02.005
Chaturvedi R, de Sablet T, Asim M, Piazuelo MB, Barry DP, Verriere TG, Sierra JC, Hardbower DM, Delgado AG, Schneider BG, Israel DA, Romero-Gallo J, Nagy TA, Morgan DR, Murray-Stewart T, Bravo LE, Peek RM Jr, Fox JG, Woster PM, Casero RA Jr, Correa P, Wilson KT (2015) Increased Helicobacter pylori-associated gastric cancer risk in the Andean region of Colombia is mediated by spermine oxidase. Oncogene 34(26):3429–3440. doi:10.1038/onc.2014.273
Chu SH, Kim H, Seo JY, Lim JW, Mukaida N, Kim KH (2003) Role of NF-kappaB and AP-1 on Helicobater pylori-induced IL-8 expression in AGS cells. Dig Dis Sci 48(2):257–265. doi:10.1023/A:1021963007225
Correa P (1988) A human model of gastric carcinogenesis. Cancer Res 48(13):3554–3560
Correa P, Cuello C, Duque E, Burbano LC, Garcia FT, Bolanos O, Brown C, Haenszel W (1976) Gastric cancer in Colombia. III. Natural history of precursor lesions. J Natl Cancer Inst 57(5):1027–1035. doi:10.1093/jnci/57.5.1027
Crabtree JE, Farmery SM, Lindley IJ, Figura N, Peichl P, Tompkins DS (1994) CagA/cytotoxic strains of Helicobacter pylori and interleukin-8 in gastric epithelial cell lines. J Clin Pathol 47(10):945–950. doi:10.1136/jcp.47.10.945
de Oliveira JG, Rossi AF, Nizato DM, Cadamuro AC, Jorge YC, Valsechi MC, Venancio LP, Rahal P, Pavarino EC, Goloni-Bertollo EM, Silva AE (2015) Influence of functional polymorphisms in TNF-alpha, IL-8, and IL-10 cytokine genes on mRNA expression levels and risk of gastric cancer. Tumour Biol 36(12):9159–9170. doi:10.1007/s13277-015-3593-x
de Sablet T, Piazuelo MB, Shaffer CL, Schneider BG, Asim M, Chaturvedi R, Bravo LE, Sicinschi LA, Delgado AG, Mera RM, Israel DA, Romero-Gallo J, Peek RM Jr, Cover TL, Correa P, Wilson KT (2011) Phylogeographic origin of Helicobacter pylori is a determinant of gastric cancer risk. Gut 60(9):1189–1195. doi:10.1136/gut.2010.234468
den Hartog G, Chattopadhyay R, Ablack A, Hall EH, Butcher LD, Bhattacharyya A, Eckmann L, Harris PR, Das S, Ernst PB, Crowe SE (2016) Regulation of Rac1 and reactive oxygen species production in response to infection of gastrointestinal epithelia. PLoS Pathog 12(1):e1005382. doi:10.1371/journal.ppat.1005382
Devi SM, Ahmed I, Khan AA, Rahman SA, Alvi A, Sechi LA, Ahmed N (2006) Genomes of Helicobacter pylori from native Peruvians suggest admixture of ancestral and modern lineages and reveal a western type cag-pathogenicity island. BMC Genom 7:191. doi:10.1186/1471-2164-7-191
Eck M, Schmausser B, Scheller K, Toksoy A, Kraus M, Menzel T, Muller-Hermelink HK, Gillitzer R (2000) CXC chemokines Gro(alpha)/IL-8 and IP-10/MIG in Helicobacter pylori gastritis. Clin Exp Immunol 122(2):192–199. doi:10.1046/j.1365-2249.2000.01374.x
Elfvin A, Bolin I, Lonroth H, Fandriks L (2006) Gastric expression of inducible nitric oxide synthase and myeloperoxidase in relation to nitrotyrosine in Helicobacter pylori-infected Mongolian gerbils. Scand J Gastroenterol 41(9):1013–1018. doi:10.1080/00365520600633537
Elfvin A, Edebo A, Bolin I, Fandriks L (2007) Quantitative measurement of nitric oxide and hydrogen peroxide in Helicobacter pylori-infected Mongolian gerbils in vivo. Scand J Gastroenterol 42(10):1175–1181. doi:10.1080/00365520701288306
Evans DJ Jr, Evans DG, Takemura T, Nakano H, Lampert HC, Graham DY, Granger DN, Kvietys PR (1995) Characterization of a Helicobacter pylori neutrophil-activating protein. Infect Immun 63(6):2213–2220
Felley CP, Pignatelli B, Van Melle GD, Crabtree JE, Stolte M, Diezi J, Corthesy-Theulaz I, Michetti P, Bancel B, Patricot LM, Ohshima H, Felley-Bosco E (2002) Oxidative stress in gastric mucosa of asymptomatic humans infected with Helicobacter pylori: effect of bacterial eradication. Helicobacter 7(6):342–348. doi:10.1046/j.1523-5378.2002.00107.x
Fischer W, Puls J, Buhrdorf R, Gebert B, Odenbreit S, Haas R (2001) Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol Microbiol 42(5):1337–1348. doi:10.1046/j.1365-2958.2001.02677.x
Fox JG, Rogers AB, Ihrig M, Taylor NS, Whary MT, Dockray G, Varro A, Wang TC (2003) Helicobacter pylori-associated gastric cancer in INS-GAS mice is gender specific. Cancer Res 63(5):942–950
Fu S, Ramanujam KS, Wong A, Fantry GT, Drachenberg CB, James SP, Meltzer SJ, Wilson KT (1999) Increased expression and cellular localization of inducible nitric oxide synthase and cyclooxygenase 2 in Helicobacter pylori gastritis. Gastroenterology 116(6):1319–1329. doi:10.1016/S0016-5085(99)70496-8
Gobert AP, Cheng Y, Wang JY, Boucher JL, Iyer RK, Cederbaum SD, Casero RA Jr, Newton JC, Wilson KT (2002) Helicobacter pylori induces macrophage apoptosis by activation of arginase II. J Immunol 168(9):4692–4700. doi:10.4049/jimmunol.168.9.4692
Gobert AP, Verriere T, de Sablet T, Peek RM Jr, Chaturvedi R, Wilson KT (2013) Haem oxygenase-1 inhibits phosphorylation of the Helicobacter pylori oncoprotein CagA in gastric epithelial cells. Cell Microbiol 15(1):145–156. doi:10.1111/cmi.12039
Gobert AP, Verriere T, Asim M, Barry DP, Piazuelo MB, de Sablet T, Delgado AG, Bravo LE, Correa P, Peek RM Jr, Chaturvedi R, Wilson KT (2014) Heme oxygenase-1 dysregulates macrophage polarization and the immune response to Helicobacter pylori. J Immunol 193(6):3013–3022. doi:10.4049/jimmunol.1401075
Goto T, Haruma K, Kitadai Y, Ito M, Yoshihara M, Sumii K, Hayakawa N, Kajiyama G (1999) Enhanced expression of inducible nitric oxide synthase and nitrotyrosine in gastric mucosa of gastric cancer patients. Clin Cancer Res 5(6):1411–1415
Hahm KB, Lee KJ, Choi SY, Kim JH, Cho SW, Yim H, Park SJ, Chung MH (1997) Possibility of chemoprevention by the eradication of Helicobacter pylori: oxidative DNA damage and apoptosis in H. pylori infection. Am J Gastroenterol 92(10):1853–1857
Hardbower DM, Asim M, Murray-Stewart T, Casero RA Jr, Verriere T, Lewis ND, Chaturvedi R, Piazuelo MB, Wilson KT (2016a) Arginase 2 deletion leads to enhanced M1 macrophage activation and upregulated polyamine metabolism in response to Helicobacter pylori infection. Amino Acids. doi:10.1007/s00726-016-2231-2
Hardbower DM, Singh K, Asim M, Verriere TG, Olivares-Villagómez D, Barry DP, Allaman MM, Washington MK, Peek Jr RM, Piazuelo MB, Wilson KT (2016b) EGFR regulates macrophage polarization and function in bacterial infection. J Clin Invest (in press). doi:10.1172/JCI83585
Harris PR, Mobley HL, Perez-Perez GI, Blaser MJ, Smith PD (1996) Helicobacter pylori urease is a potent stimulus of mononuclear phagocyte activation and inflammatory cytokine production. Gastroenterology 111(2):419–425. doi:10.1053/gast.1996.v111.pm8690207
Higashi H, Tsutsumi R, Muto S, Sugiyama T, Azuma T, Asaka M, Hatakeyama M (2002) SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 295(5555):683–686. doi:10.1126/science.1067147
Hirahashi M, Koga Y, Kumagai R, Aishima S, Taguchi K, Oda Y (2014) Induced nitric oxide synthetase and peroxiredoxin expression in intramucosal poorly differentiated gastric cancer of young patients. Pathol Int 64(4):155–163. doi:10.1111/pin.12152
Hisatsune J, Nakayama M, Isomoto H, Kurazono H, Mukaida N, Mukhopadhyay AK, Azuma T, Yamaoka Y, Sap J, Yamasaki E, Yahiro K, Moss J, Hirayama T (2008) Molecular characterization of Helicobacter pylori VacA induction of IL-8 in U937 cells reveals a prominent role for p38MAPK in activating transcription factor-2, cAMP response element binding protein, and NF-kappaB activation. J Immunol 180(7):5017–5027. doi:10.4049/jimmunol.180.7.5017
Jorge YC, Duarte MC, Silva AE (2010) Gastric cancer is associated with NOS2-954G/C polymorphism and environmental factors in a Brazilian population. BMC Gastroenterol 10:64. doi:10.1186/1471-230X-10-64
Kaise M, Miwa J, Suzuki N, Mishiro S, Ohta Y, Yamasaki T, Tajiri H (2007) Inducible nitric oxide synthase gene promoter polymorphism is associated with increased gastric mRNA expression of inducible nitric oxide synthase and increased risk of gastric carcinoma. Eur J Gastroenterol Hepatol 19(2):139–145. doi:10.1097/01.meg.0000252637.11291.1d
Kang JM, Kim N, Lee DH, Park JH, Lee MK, Kim JS, Jung HC, Song IS (2009) The effects of genetic polymorphisms of IL-6, IL-8, and IL-10 on Helicobacter pylori-induced gastroduodenal diseases in Korea. J Clin Gastroenterol 43(5):420–428. doi:10.1097/MCG.0b013e318178d1d3
Katsurahara M, Kobayashi Y, Iwasa M, Ma N, Inoue H, Fujita N, Tanaka K, Horiki N, Gabazza EC, Takei Y (2009) Reactive nitrogen species mediate DNA damage in Helicobacter pylori-infected gastric mucosa. Helicobacter 14(6):552–558. doi:10.1111/j.1523-5378.2009.00719.x
Keates S, Keates AC, Warny M, Peek RM Jr, Murray PG, Kelly CP (1999) Differential activation of mitogen-activated protein kinases in AGS gastric epithelial cells by cag+ and cag− Helicobacter pylori. J Immunol 163(10):5552–5559 ji_v163n10p5552
Keenan JI, Peterson RA 2nd, Hampton MB (2005) NADPH oxidase involvement in the pathology of Helicobacter pylori infection. Free Radic Biol Med 38(9):1188–1196. doi:10.1016/j.freeradbiomed.2004.12.025
Kim SY, Lee YC, Kim HK, Blaser MJ (2006) Helicobacter pylori CagA transfection of gastric epithelial cells induces interleukin-8. Cell Microbiol 8(1):97–106. doi:10.1111/j.1462-5822.2005.00603.x
Kitadai Y, Takahashi Y, Haruma K, Naka K, Sumii K, Yokozaki H, Yasui W, Mukaida N, Ohmoto Y, Kajiyama G, Fidler IJ, Tahara E (1999) Transfection of interleukin-8 increases angiogenesis and tumorigenesis of human gastric carcinoma cells in nude mice. Br J Cancer 81(4):647–653. doi:10.1038/sj.bjc.6690742
Kodaman N, Pazos A, Schneider BG, Piazuelo MB, Mera R, Sobota RS, Sicinschi LA, Shaffer CL, Romero-Gallo J, de Sablet T, Harder RH, Bravo LE, Peek RM Jr, Wilson KT, Cover TL, Williams SM, Correa P (2014) Human and Helicobacter pylori coevolution shapes the risk of gastric disease. Proc Natl Acad Sci U S A 111(4):1455–1460. doi:10.1073/pnas.1318093111
Konturek SJ, Starzynska T, Konturek PC, Karczewska E, Marlicz K, Lawniczak M, Jaroszewicz-Heigelman H, Bielanski W, Hartwich A, Ziemniak A, Hahn EG (2002) Helicobacter pylori and CagA status, serum gastrin, interleukin-8 and gastric acid secretion in gastric cancer. Scand J Gastroenterol 37(8):891–898. doi:10.1080/003655202760230838
Lamb A, Yang XD, Tsang YH, Li JD, Higashi H, Hatakeyama M, Peek RM, Blanke SR, Chen LF (2009) Helicobacter pylori CagA activates NF-kappaB by targeting TAK1 for TRAF6-mediated Lys 63 ubiquitination. EMBO Rep 10(11):1242–1249. doi:10.1038/embor.2009.210
Lancaster JR Jr, Hibbs JB Jr (1990) EPR demonstration of iron-nitrosyl complex formation by cytotoxic activated macrophages. Proc Natl Acad Sci U S A 87(3):1223–1227. doi:10.1073/pnas.87.3.1223
Lee KH, Bae SH, Lee JL, Hyun MS, Kim SH, Song SK, Kim HS (2004) Relationship between urokinase-type plasminogen receptor, interleukin-8 gene expression and clinicopathological features in gastric cancer. Oncology 66(3):210–217. doi:10.1159/000077997
Lee WP, Tai DI, Lan KH, Li AF, Hsu HC, Lin EJ, Lin YP, Sheu ML, Li CP, Chang FY, Chao Y, Yen SH, Lee SD (2005) The –251T allele of the interleukin-8 promoter is associated with increased risk of gastric carcinoma featuring diffuse-type histopathology in Chinese population. Clin Cancer Res 11(18):6431–6441. doi:10.1158/1078-0432.CCR-05-0942
Lee CW, Rickman B, Rogers AB, Ge Z, Wang TC, Fox JG (2008) Helicobacter pylori eradication prevents progression of gastric cancer in hypergastrinemic INS-GAS mice. Cancer Res 68(9):3540–3548. doi:10.1158/0008-5472.CAN-07-6786
Lewis ND, Asim M, Barry DP, de Sablet T, Singh K, Piazuelo MB, Gobert AP, Chaturvedi R, Wilson KT (2011) Immune evasion by Helicobacter pylori is mediated by induction of macrophage arginase II. J Immunol 186(6):3632–3641. doi:10.4049/jimmunol.1003431
Li CQ, Pignatelli B, Ohshima H (2001) Increased oxidative and nitrative stress in human stomach associated with cagA+ Helicobacter pylori infection and inflammation. Dig Dis Sci 46(4):836–844. doi:10.1023/A:1010764720524
Li X, Liu S, Luo J, Liu A, Tang S, Liu S, Yu M, Zhang Y (2015) Helicobacter pylori induces IL-1beta and IL-18 production in human monocytic cell line through activation of NLRP3 inflammasome via ROS signaling pathway. Pathog Dis 73(4). doi:10.1093/femspd/ftu024
Lu H, Wu JY, Kudo T, Ohno T, Graham DY, Yamaoka Y (2005a) Regulation of interleukin-6 promoter activation in gastric epithelial cells infected with Helicobacter pylori. Mol Biol Cell 16(10):4954–4966. doi:10.1091/mbc.E05-05-0426
Lu W, Pan K, Zhang L, Lin D, Miao X, You W (2005b) Genetic polymorphisms of interleukin (IL)-1B, IL-1RN, IL-8, IL-10 and tumor necrosis factor alpha and risk of gastric cancer in a Chinese population. Carcinogenesis 26(3):631–636. doi:10.1093/carcin/bgh349
Ma N, Adachi Y, Hiraku Y, Horiki N, Horiike S, Imoto I, Pinlaor S, Murata M, Semba R, Kawanishi S (2004) Accumulation of 8-nitroguanine in human gastric epithelium induced by Helicobacter pylori infection. Biochem Biophys Res Commun 319(2):506–510. doi:10.1016/j.bbrc.2004.04.193
Maeda S, Akanuma M, Mitsuno Y, Hirata Y, Ogura K, Yoshida H, Shiratori Y, Omata M (2001) Distinct mechanism of Helicobacter pylori-mediated NF-kappa B activation between gastric cancer cells and monocytic cells. J Biol Chem 276(48):44856–44864. doi:10.1074/jbc.M105381200
Mai UE, Perez-Perez GI, Wahl LM, Wahl SM, Blaser MJ, Smith PD (1991) Soluble surface proteins from Helicobacter pylori activate monocytes/macrophages by lipopolysaccharide-independent mechanism. J Clin Invest 87(3):894–900. doi:10.1172/JCI115095
Mannick EE, Bravo LE, Zarama G, Realpe JL, Zhang XJ, Ruiz B, Fontham ET, Mera R, Miller MJ, Correa P (1996) Inducible nitric oxide synthase, nitrotyrosine, and apoptosis in Helicobacter pylori gastritis: effect of antibiotics and antioxidants. Cancer Res 56(14):3238–3243
Matsubara S, Shibata H, Takahashi M, Ishikawa F, Yokokura T, Sugimura T, Wakabayashi K (2004) Cloning of Mongolian gerbil cDNAs encoding inflammatory proteins, and their expression in glandular stomach during H. pylori infection. Cancer Sci 95(10):798–802
Menheniott TR, Peterson AJ, O’Connor L, Lee KS, Kalantzis A, Kondova I, Bontrop RE, Bell KM, Giraud AS (2010) A novel gastrokine, Gkn3, marks gastric atrophy and shows evidence of adaptive gene loss in humans. Gastroenterology 138(5):1823–1835. doi:10.1053/j.gastro.2010.01.050
Miyazawa M, Suzuki H, Masaoka T, Kai A, Suematsu M, Nagata H, Miura S, Ishii H (2003) Suppressed apoptosis in the inflamed gastric mucosa of Helicobacter pylori-colonized iNOS-knockout mice. Free Radic Biol Med 34(12):1621–1630. doi:10.1016/S0891-5849(03)00218-1
Mueller D, Tegtmeyer N, Brandt S, Yamaoka Y, De Poire E, Sgouras D, Wessler S, Torres J, Smolka A, Backert S (2012) c-Src and c-Abl kinases control hierarchic phosphorylation and function of the CagA effector protein in Western and East Asian Helicobacter pylori strains. J Clin Invest 122(4):1553–1566. doi:10.1172/JCI61143
Murray-Stewart T, Sierra JC, Piazuelo MB, Mera RM, Chaturvedi R, Bravo LE, Correa P, Schneider BG, Wilson KT, Casero RA (2016) Epigenetic silencing of miR-124 prevents spermine oxidase regulation: implications for Helicobacter pylori-induced gastric cancer. Oncogene. doi:10.1038/onc.2016.91
Ngo HK, Lee HG, Piao JY, Zhong X, Lee HN, Han HJ, Kim W, Kim DH, Cha YN, Na HK, Surh YJ (2016) Helicobacter pylori induces Snail expression through ROS-mediated activation of Erk and inactivation of GSK-3beta in human gastric cancer cells. Mol Carcinog. doi:10.1002/mc.22464
Nielsen H, Andersen LP (1992) Activation of human phagocyte oxidative metabolism by Helicobacter pylori. Gastroenterology 103(6):1747–1753
Nielsen H, Birkholz S, Andersen LP, Moran AP (1994) Neutrophil activation by Helicobacter pylori lipopolysaccharides. J Infect Dis 170(1):135–139. doi:10.1093/infdis/170.1.135
Noto JM, Gaddy JA, Lee JY, Piazuelo MB, Friedman DB, Colvin DC, Romero-Gallo J, Suarez G, Loh J, Slaughter JC, Tan S, Morgan DR, Wilson KT, Bravo LE, Correa P, Cover TL, Amieva MR, Peek RM Jr (2013) Iron deficiency accelerates Helicobacter pylori-induced carcinogenesis in rodents and humans. J Clin Invest 123(1):479–492. doi:10.1172/JCI64373
Obonyo M, Guiney DG, Fierer J, Cole SP (2003) Interactions between inducible nitric oxide and other inflammatory mediators during Helicobacter pylori infection. Helicobacter 8(5):495–502. doi:10.1046/j.1523-5378.2003.00171.x
Ohyauchi M, Imatani A, Yonechi M, Asano N, Miura A, Iijima K, Koike T, Sekine H, Ohara S, Shimosegawa T (2005) The polymorphism interleukin 8 −251 A/T influences the susceptibility of Helicobacter pylori related gastric diseases in the Japanese population. Gut 54(3):330–335. doi:10.1136/gut.2003.033050
Olczak AA, Olson JW, Maier RJ (2002) Oxidative-stress resistance mutants of Helicobacter pylori. J Bacteriol 184(12):3186–3193. doi:10.1128/JB.184.12.3186-3193.2002
Papa A, Danese S, Sgambato A, Ardito R, Zannoni G, Rinelli A, Vecchio FM, Gentiloni-Silveri N, Cittadini A, Gasbarrini G, Gasbarrini A (2002) Role of Helicobacter pylori CagA+ infection in determining oxidative DNA damage in gastric mucosa. Scand J Gastroenterol 37(4):409–413. doi:10.1080/003655202317316033
Piao JY, Lee HG, Kim SJ, Kim DH, Han HJ, Ngo HK, Park SA, Woo JH, Lee JS, Na HK, Cha YN, Surh YJ (2016) Helicobacter pylori activates IL-6-STAT3 signaling in human gastric cancer cells: potential roles for reactive oxygen species. Helicobacter. doi:10.1111/hel.12298
Pignatelli B, Bancel B, Plummer M, Toyokuni S, Patricot LM, Ohshima H (2001) Helicobacter pylori eradication attenuates oxidative stress in human gastric mucosa. Am J Gastroenterol 96(6):1758–1766. doi:10.1111/j.1572-0241.2001.03869.x
Raju D, Hussey S, Ang M, Terebiznik MR, Sibony M, Galindo-Mata E, Gupta V, Blanke SR, Delgado A, Romero-Gallo J, Ramjeet MS, Mascarenhas H, Peek RM, Correa P, Streutker C, Hold G, Kunstmann E, Yoshimori T, Silverberg MS, Girardin SE, Philpott DJ, El Omar E, Jones NL (2012) Vacuolating cytotoxin and variants in Atg16L1 that disrupt autophagy promote Helicobacter pylori infection in humans. Gastroenterology 142(5):1160–1171. doi:10.1053/j.gastro.2012.01.043
Rizwan M, Alvi A, Ahmed N (2008) Novel protein antigen (JHP940) from the genomic plasticity region of Helicobacter pylori induces tumor necrosis factor alpha and interleukin-8 secretion by human macrophages. J Bacteriol 190(3):1146–1151. doi:10.1128/JB.01309-07
Sakaguchi AA, Miura S, Takeuchi T, Hokari R, Mizumori M, Yoshida H, Higuchi H, Mori M, Kimura H, Suzuki H, Ishii H (1999) Increased expression of inducible nitric oxide synthase and peroxynitrite in Helicobacter pylori gastric ulcer. Free Radic Biol Med 27(7–8):781–789. doi:10.1016/S0891-5849(99)00124-0
Salih BA, Guner A, Karademir A, Uslu M, Ovali MA, Yazici D, Bolek BK, Arikan S (2014) Evaluation of the effect of cagPAI genes of Helicobacter pylori on AGS epithelial cell morphology and IL-8 secretion. Antonie Van Leeuwenhoek 105(1):179–189. doi:10.1007/s10482-013-0064-5
Salles N, Szanto I, Herrmann F, Armenian B, Stumm M, Stauffer E, Michel JP, Krause KH (2005) Expression of mRNA for ROS-generating NADPH oxidases in the aging stomach. Exp Gerontol 40(4):353–357. doi:10.1016/j.exger.2005.01.007
Satin B, Del Giudice G, Della Bianca V, Dusi S, Laudanna C, Tonello F, Kelleher D, Rappuoli R, Montecucco C, Rossi F (2000) The neutrophil-activating protein (HP-NAP) of Helicobacter pylori is a protective antigen and a major virulence factor. J Exp Med 191(9):1467–1476. doi:10.1084/jem.191.9.1467
Sawa T, Mounawar M, Tatemichi M, Gilibert I, Katoh T, Ohshima H (2008) Increased risk of gastric cancer in Japanese subjects is associated with microsatellite polymorphisms in the heme oxygenase-1 and the inducible nitric oxide synthase gene promoters. Cancer Lett 269(1):78–84. doi:10.1016/j.canlet.2008.04.015
Schneider BG, Mera R, Piazuelo MB, Bravo JC, Zabaleta J, Delgado AG, Bravo LE, Wilson KT, El-Rifai W, Peek RM Jr, Correa P (2015) DNA methylation predicts progression of human gastric lesions. Cancer Epidemiol Biomarkers Prev 24(10):1607–1613. doi:10.1158/1055-9965.EPI-15-0388
Sharma SA, Tummuru MK, Miller GG, Blaser MJ (1995) Interleukin-8 response of gastric epithelial cell lines to Helicobacter pylori stimulation in vitro. Infect Immun 63(5):1681–1687
Sheh A, Chaturvedi R, Merrell DS, Correa P, Wilson KT, Fox JG (2013) Phylogeographic origin of Helicobacter pylori determines host-adaptive responses upon coculture with gastric epithelial cells. Infect Immun 81(7):2468–2477. doi:10.1128/IAI.01182-12
Shimoyama T, Fukuda S, Liu Q, Nakaji S, Fukuda Y, Sugawara K (2003) Helicobacter pylori water soluble surface proteins prime human neutrophils for enhanced production of reactive oxygen species and stimulate chemokine production. J Clin Pathol 56(5):348–351. doi:10.1136/jcp.56.5.348
Shirai K, Ohmiya N, Taguchi A, Mabuchi N, Yatsuya H, Itoh A, Hirooka Y, Niwa Y, Mori N, Goto H (2006) Interleukin-8 gene polymorphism associated with susceptibility to non-cardia gastric carcinoma with microsatellite instability. J Gastroenterol Hepatol 21(7):1129–1135. doi:10.1111/j.1440-1746.2006.04443.x
Son HJ, Rhee JC, Park DI, Kim YH, Rhee PL, Koh KC, Paik SW, Choi KW, Kim JJ (2001) Inducible nitric oxide synthase expression in gastroduodenal diseases infected with Helicobacter pylori. Helicobacter 6(1):37–43. doi:10.1046/j.1523-5378.2001.00004.x
Song JH, Kim SG, Jung SA, Lee MK, Jung HC, Song IS (2010) The interleukin-8-251 AA genotype is associated with angiogenesis in gastric carcinogenesis in Helicobacter pylori-infected Koreans. Cytokine 51(2):158–165. doi:10.1016/j.cyto.2010.05.001
Supajatura V, Ushio H, Wada A, Yahiro K, Okumura K, Ogawa H, Hirayama T, Ra C (2002) Cutting edge: VacA, a vacuolating cytotoxin of Helicobacter pylori, directly activates mast cells for migration and production of proinflammatory cytokines. J Immunol 168(6):2603–2607. doi:10.4049/jimmunol.168.6.2603
Suzuki M, Mimuro H, Kiga K, Fukumatsu M, Ishijima N, Morikawa H, Nagai S, Koyasu S, Gilman RH, Kersulyte D, Berg DE, Sasakawa C (2009) Helicobacter pylori CagA phosphorylation-independent function in epithelial proliferation and inflammation. Cell Host Microbe 5(1):23–34. doi:10.1016/j.chom.2008.11.010
Suzuki M, Kiga K, Kersulyte D, Cok J, Hooper CC, Mimuro H, Sanada T, Suzuki S, Oyama M, Kozuka-Hata H, Kamiya S, Zou QM, Gilman RH, Berg DE, Sasakawa C (2011) Attenuated CagA oncoprotein in Helicobacter pylori from Amerindians in Peruvian Amazon. J Biol Chem 286(34):29964–29972. doi:10.1074/jbc.M111.263715
Szoke D, Molnar B, Solymosi N, Klausz G, Gyulai Z, Toth B, Mandi Y, Tulassay Z (2008) T-251A polymorphism of IL-8 relating to the development of histological gastritis and G-308A polymorphism of TNF-alpha relating to the development of macroscopic erosion. Eur J Gastroenterol Hepatol 20(3):191–195. doi:10.1097/MEG.0b013e3282f1d29f
Taguchi A, Ohmiya N, Shirai K, Mabuchi N, Itoh A, Hirooka Y, Niwa Y, Goto H (2005) Interleukin-8 promoter polymorphism increases the risk of atrophic gastritis and gastric cancer in Japan. Cancer Epidemiol Biomarkers Prev 14(11 Pt 1):2487–2493. doi:10.1158/1055-9965.EPI-05-0326
Tahara T, Shibata T, Wang F, Nakamura M, Okubo M, Yoshioka D, Sakata M, Nakano H, Hirata I, Arisawa T (2009a) Association of polymorphism of the p22PHOX component of NADPH oxidase in gastroduodenal diseases in Japan. Scand J Gastroenterol 44(3):296–300. doi:10.1080/00365520701702348
Tahara T, Shibata T, Wang F, Nakamura M, Sakata M, Nakano H, Hirata I, Arisawa T (2009b) A genetic variant of the p22PHOX component of NADPH oxidase C242T is associated with reduced risk of functional dyspepsia in Helicobacter pylori-infected Japanese individuals. Eur J Gastroenterol Hepatol 21(12):1363–1368. doi:10.1097/MEG.0b013e32830e2871
Tatemichi M, Ogura T, Nagata H, Esumi H (1998) Enhanced expression of inducible nitric oxide synthase in chronic gastritis with intestinal metaplasia. J Clin Gastroenterol 27(3):240–245
Tatemichi M, Sawa T, Gilibert I, Tazawa H, Katoh T, Ohshima H (2005) Increased risk of intestinal type of gastric adenocarcinoma in Japanese women associated with long forms of CCTTT pentanucleotide repeat in the inducible nitric oxide synthase promoter. Cancer Lett 217(2):197–202. doi:10.1016/j.canlet.2004.09.002
Tominaga K, Kawahara T, Sano T, Toida K, Kuwano Y, Sasaki H, Kawai T, Teshima-Kondo S, Rokutan K (2007) Evidence for cancer-associated expression of NADPH oxidase 1 (Nox1)-based oxidase system in the human stomach. Free Radic Biol Med 43(12):1627–1638. doi:10.1016/j.freeradbiomed.2007.08.029
Tonello F, Dundon WG, Satin B, Molinari M, Tognon G, Grandi G, Del Giudice G, Rappuoli R, Montecucco C (1999) The Helicobacter pylori neutrophil-activating protein is an iron-binding protein with dodecameric structure. Mol Microbiol 34(2):238–246. doi:10.1046/j.1365-2958.1999.01584.x
Touati E, Michel V, Thiberge JM, Wuscher N, Huerre M, Labigne A (2003) Chronic Helicobacter pylori infections induce gastric mutations in mice. Gastroenterology 124(5):1408–1419. doi:10.1016/S0016-5085(03)00266-X
Tsuji S, Tsujii M, Sun WH, Gunawan ES, Murata H, Kawano S, Hori M (1997) Helicobacter pylori and gastric carcinogenesis. J Clin Gastroenterol 25(Suppl 1):S186–S197
Umeda M, Murata-Kamiya N, Saito Y, Ohba Y, Takahashi M, Hatakeyama M (2009) Helicobacter pylori CagA causes mitotic impairment and induces chromosomal instability. J Biol Chem 284(33):22166–22172. doi:10.1074/jbc.M109.035766
Varga MG, Shaffer CL, Sierra JC, Suarez G, Piazuelo MB, Whitaker ME, Romero-Gallo J, Krishna US, Delgado A, Gomez MA, Good JA, Almqvist F, Skaar EP, Correa P, Wilson KT, Hadjifrangiskou M, Peek RM (2016) Pathogenic Helicobacter pylori strains translocate DNA and activate TLR9 via the cancer-associated cag type IV secretion system. Oncogene. doi:10.1038/onc.2016.158
Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, Moran AP, Athman R, Memet S, Huerre MR, Coyle AJ, DiStefano PS, Sansonetti PJ, Labigne A, Bertin J, Philpott DJ, Ferrero RL (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 5(11):1166–1174. doi:10.1038/ni1131
Vinall LE, King M, Novelli M, Green CA, Daniels G, Hilkens J, Sarner M, Swallow DM (2002) Altered expression and allelic association of the hypervariable membrane mucin MUC1 in Helicobacter pylori gastritis. Gastroenterology 123(1):41–49. doi:10.1053/gast.2002.34157
Wang Y, Devereux W, Woster PM, Stewart TM, Hacker A, Casero RA Jr (2001) Cloning and characterization of a human polyamine oxidase that is inducible by polyamine analogue exposure. Cancer Res 61(14):5370–5373
Wang G, Hong Y, Olczak A, Maier SE, Maier RJ (2006) Dual roles of Helicobacter pylori NapA in inducing and combating oxidative stress. Infect Immun 74(12):6839–6846. doi:10.1128/IAI.00991-06
Wilson KT, Crabtree JE (2007) Immunology of Helicobacter pylori: insights into the failure of the immune response and perspectives on vaccine studies. Gastroenterology 133(1):288–308. doi:10.1053/j.gastro.2007.05.008
Xu H, Chaturvedi R, Cheng Y, Bussiere FI, Asim M, Yao MD, Potosky D, Meltzer SJ, Rhee JG, Kim SS, Moss SF, Hacker A, Wang Y, Casero RA Jr, Wilson KT (2004) Spermine oxidation induced by Helicobacter pylori results in apoptosis and DNA damage: implications for gastric carcinogenesis. Cancer Res 64(23):8521–8525. doi:10.1158/0008-5472.CAN-04-3511
Yamaoka Y, Kudo T, Lu H, Casola A, Brasier AR, Graham DY (2004) Role of interferon-stimulated responsive element-like element in interleukin-8 promoter in Helicobacter pylori infection. Gastroenterology 126(4):1030–1043. doi:10.1053/j.gastro.2003.12.048
Ye BD, Kim SG, Park JH, Kim JS, Jung HC, Song IS (2009) The interleukin-8-251 A allele is associated with increased risk of noncardia gastric adenocarcinoma in Helicobacter pylori-infected Koreans. J Clin Gastroenterol 43(3):233–239. doi:10.1097/MCG.0b013e3181646701
Yermilov V, Rubio J, Becchi M, Friesen MD, Pignatelli B, Ohshima H (1995) Formation of 8-nitroguanine by the reaction of guanine with peroxynitrite in vitro. Carcinogenesis 16(9):2045–2050. doi:10.1093/carcin/16.9.2045
Yuan A, Chen JJ, Yao PL, Yang PC (2005) The role of interleukin-8 in cancer cells and microenvironment interaction. Front Biosci 10:853–865. doi:10.2741/1579
Zhang L, Du C, Guo X, Yuan L, Niu W, Yu W, Er L, Wang S (2010) Interleukin-8-251A/T polymorphism and Helicobacter pylori infection influence risk for the development of gastric cardiac adenocarcinoma in a high-incidence area of China. Mol Biol Rep 37(8):3983–3989. doi:10.1007/s11033-010-0057-7
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Gobert, A.P., Wilson, K.T. (2017). Human and Helicobacter pylori Interactions Determine the Outcome of Gastric Diseases. In: Tegtmeyer, N., Backert, S. (eds) Molecular Pathogenesis and Signal Transduction by Helicobacter pylori. Current Topics in Microbiology and Immunology, vol 400. Springer, Cham. https://doi.org/10.1007/978-3-319-50520-6_2
Download citation
DOI: https://doi.org/10.1007/978-3-319-50520-6_2
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-50519-0
Online ISBN: 978-3-319-50520-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)