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Helicobacter Pylori Infection in a Mouse Model: Development, Optimization and Inhibitory Effects of Antioxidants Wang Helicobacter pylori infection in a mouse model: Development, optimization and inhibitory effects of antioxidants Wang, Xin 2001 Link to publication Citation for published version (APA): Wang, X. (2001). Helicobacter pylori infection in a mouse model: Development, optimization and inhibitory effects of antioxidants. Xin Wang, Dept. of Med. Microbiol., Dermatol. & Infect., Lund University, Sölvegatan 23, S-223 62 Lund, Sweden,. 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LUND UNIVERSITY PO Box 117 221 00 Lund +46 46-222 00 00 Helicobacter pylori infection in a mouse model Development, optimization and inhibitory effects of antioxidants Xin Wang 2001 Helicobacter pylori infection in a mouse model Development, optimization and inhibitory effects of antioxidants Akademisk avhanding som med vederborligt tillsttind av Medicinska fakulteten vid Lunds Universitet for avlaggande av doktorsexamen i medicinsk vetenskap kommer att offentligen forsvaras i Rune Grubb Salen, BMC, Solvegatan 19, Lund, Fredag den 12 Oktober 200 1, kl. 13.15 Xin Wang LUND UNIVERSITY Fakultetsopponent: Associate professor Elisabeth Norin, Microbiology and Tumor Biology Center (MTC), Karolinska Institutet, Stockholm 0 rga n iza r io ii Documeiir nanie LUND UNIVERSITY DOCTORAL DISSERTATION Dare of issue Department of Medical Microbiology, October 12,200 1 Dermatology and Infection S porisori tig org:i 11 iza t ion Solvegatan 23,223 62 Lund Au r ho r (\) Xin Wang Tide 'irid wbrirlc Helzcobacter pylori infection in a mouse model: Development, optimization and inhibitory effects of antioxidants A b 7 r r.ii I Heficobacterpyfori is a human pathogen strongly associated with chronic type B gastritis, peptic ulcer disease, gastric cancer and MALT lymphoma. Our aims were to establish a mouse model of H. pylori mfection, to study pathogenesis of gastritis and gastric cancer and to investigate new treatment strategies in this model. Both spiral and coccoid forms of H. pyfori strains 17874,25 and 553/93 caused chronic gastritis in BALB/cA mice during 30 weeks of infection. lnfection with strain 553/93 displayed the most severe gastritis. Specific antibodies were detected using ELISA and immunoblot in mice infected with H. pylori following 4 weeks for 17874 spirals, and 16 weeks for 17874 coccoids, and both sprials and coccoids of two other strains. Dietary factors influenced the abilities to recover H. pyfori from the infected mice through culture. One diet, without fish meal and heated at 140-15OvC, gave the optimal H. pyiori colonization and highest inflammation score in mufine stomach among 4 commercial rodent diets tested. The changes were most dramatic (100% to 10-20% infection rate) when the infection was carried out in animals already fed on a specific diet. A H. pylori strain 119/95 (CagA and VacA positive) was found to predominate (90.5%) in the murine stomach from inocula containing nine H. pyfori strains by WD-PCR among 577 colonies recovered fiom mice. C57BLf6 and BALB/cA mice showed higher inflammation scores than CBAlCa or NMRl mice at 4 andlor 10 weeks post-inoculation. Subsequently C57BL/6 mice (n=5) inoculated with a H. pylori mouse passaged strain 119195 developed a gastric squamous cell papilloma after 13 months. Three out of five animals developed high-grade B-cell lymphoma derived from a MALT Iymphoma at the squamous-corpus border with destations also in the liver, spleen and kidney. An astaxanthin-rich algal meal from the microalga ~umatococ~~pl~ial~sand vitamin C &bit €2 pylori growth at 0.3 125 to 2.5 mg/ml (astaxanthin content, 6.25 to 50 pg/ml) and 0.5 to 2 m@ml in vitro respectively. Furthermore, these antioxidants decreased the gastric colonization and &=tion signifkantly in infected BALB/cA mice. The effect on inhibition of H. pylori infection by the astaxanthin-rich algal meal was found to occur simultaneously with a modulation H. pyfori-induced T-lymphocyte response, switching from a Thl- to a Thlm-response. These studies illustrate that E. pyfori can induce chronic gastritis and gastric lymphoma in an optimized mouse model. Dietary factors influence H pylori infection and antioxidants may become a new treatment strategy against H. pylori infection in humans. Key wordc Yelicobacterpylori, mice, gastritis, lymphoma, ~tioxidant,diet, eytokines and Thl and Th2 Cl.i\\ilic'trioii \y\teni rtidlor iiidcv rcrmcc (ifdriyf S U p p Icni c n I;i ry I, i hI iogra ph ic'i I infor ni a r 10 n : Language English ISSN .Idkcv tl(k I ISBN 1 91-628-4864-X Xin Wang, Dept. ofhied. MicrobioL, Dermatol. & Infect., Ui\rribucion hy (n.inic arid addresi) d University, &3lvegaian23, S-223 62 Lund,Swsden I. the undcr\igiied. being the copyright owricr okcdhstracr of ifis .rt)t~\.c-rnriirioneddisscrrarron, hereby grdiit tti all rcferrncc sources pcrmtssrori CO publish arid dis,criiitiarc rhc .ili\rr.icr of the abovc-nicnrioticd dtsscrrrrion Helicobacter pylori infection in a mouse model Development, optimization and inhibitory effects of antioxidants Xin Wang Department of Medical Microbiology, Dermatology and Infection University of Lund Sweden 2001 3 Copyright © 2001 Xin Wang ISBN 91-628-4864-X 4 To Daiqing, Yinuo and my parents 5 6 Contents • List of papers 9 • Abbreviations 10 • Introduction 11 • History of Helicobacter pylori 11 • Microbiology 11 • Epidemiology and transmission 13 • Pathogenic mechanisms 14 • Virulence factors 14 • Immune response 14 • Free-radical injury 16 • Free radicals and lipid peroxidation 16 • H. pylori and free radical damage 17 • Antioxidants and their function 18 • Helicobacter pylori infection and gastric diseases 22 • Non-ulcer dyspepsia 22 • Gastritis 23 • Peptic ulcer disease 23 • Gastric cancer 23 • Gastric lymphoma 25 • Treatment, antibiotic resistance and vaccination 27 • Animal models 29 • Mouse 29 • Mongolian gerbil 32 • Guinea pig 32 • Ferret 33 • Cat and dog 33 • Primates 33 • Others 34 • Gnotobiotic piglet 34 7 • Rat 34 • Transgenic mice 35 • Aims of the present investigations 36 • Materials and Methods 37 • Results and discussion 45 • Conclusion and future prospects 54 • Sammanfattning på svenska 57 • Acknowledgment 58 • References 60 • Appendix (Paper I-VI) 8 List of Papers This thesis is based on the following papers, which will be referred to in the text by their Roman numerals I-VI. Reprints were made with permissions from the publishers. I. Wang X., E. Sturegård, R. Rupar, H. O. Nilsson, P. A. Aleljung, B. Carlen, R. Wíllén, and T. Wadström. Infection of BALB/cA mice by spiral and coccoid forms of Helicobacter pylori. J Med Microbiol. 1997;46:657-663. II. Wang X., H. Sjunnesson, E. Sturegård, T. Wadström, R. Willén, and P. Aleljung. Dietary factors influence the recovery rates of Helicobacter pylori in a BALB/cA mouse model. Zent bl Bakteriol. 1998;288:195-205. III. Wang X., R. Willén, T. Wadström, and P. Aleljung. RAPD-PCR, histopathological and serological analysis of four mouse strains infected with multiple strains of Helicobacter pylori. Microbial Ecology in Health and Disease. 1998;10:148-154. IV. Wang X., R. Willén, C. Andersson and T. Wadström. Development of high- grade lymphoma in Helicobacter pylori-infected C57BL/6 mice. APMIS 2000;108:503-508. V. Wang X., R. Willén and T. Wadström. Astaxanthin-rich algal meal and vitamin C inhibit Helicobacter pylori infection in BALB/cA mice. Antimicrob Agents Chemother. 2000;44:2452-2457. VI. Bennedsen M., X. Wang, R. Willén, T. Wadström and L. P. Andersen. Treatment of H. pylori infected mice with antioxidant astaxanthin reduces gastric inflammation, bacterial load and modulates cytokine release by splenocytes. Immunol Lett 1999;70:185-189. 9 Abbreviation cagA Cytotoxin-associated gene A CagA Cytotoxin associated protein CAT Catalase ELISA Enzyme linked immunosorbent assay GSH Glutathione H. pylori Helicobacter pylori Helicobacter spp. Helicobacter species HHLO Helicobacter heilmannii-like bacteria IFN Interferon IL Interleukin NF-κB Nuclear factor-kappa B NO Nitric oxide NUD Non-ulcer dyspepsia MALT Mucosa-associated lymphoid tissue MNU N-methyl-N-nitrosourea MNNG N-methyl-N'-nitro-N-nitrosoguanidine p.i. Post-inoculation RAPD-PCR Random Amplified Polymorphic DNA-polymerase chain reaction ROS Reactive oxygen species SOD Superoxide dismutase SPF Specific pathogen free Th T-cell helper TNF Tumor necrosis factor vacA Vacuolating cytotoxin gene A VacA Vaculating cytotoxin A VBNC Viable but non-culturable 10 Introduction The history of Helicobacter pylori The presence of spiral-shaped bacteria have been reported in studies including human patients since 1889, but the organism Helicobacter pylori was discovered almost one hundred years later [Kidd et al. 1998]. The organism associated with active chronic gastritis was isolated in 1983 and named Campylobacter pyloridis in 1984 [Warren et al. 1983; Marshall et al. 1984]. It fulfilled Koch’s postulates in one healthy volunteer [Marshall et al. 1985]. The name was first changed to Campylobacter pylori, then to Helicobacter pylori in 1989 when taxonomic studies showed that this organism did not belong to the genus Campylobacter [Goodwin et al. 1989]. Helicobacter pylori (H. pylori) infections are ubiquitous and causes chronic gastritis, peptic ulcer and gastric carcinoma [Hansson et al.
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