Interactions between Helicobacter pylori infection and host metabolic homeostasis: A comprehensive review.
Helicobacter pylori
insulin resistance
metabolism
metabolites
microbiota
nonalcoholic fatty liver disease
Journal
Helicobacter
ISSN: 1523-5378
Titre abrégé: Helicobacter
Pays: England
ID NLM: 9605411
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
revised:
06
10
2023
received:
17
09
2023
accepted:
10
10
2023
medline:
27
11
2023
pubmed:
24
10
2023
entrez:
23
10
2023
Statut:
ppublish
Résumé
The microbiota actively and extensively participates in the regulation of human metabolism, playing a crucial role in the development of metabolic diseases. Helicobacter pylori (H. pylori), when colonizing gastric epithelial cells, not only induces local tissue inflammation or malignant transformation but also leads to systemic and partial changes in host metabolism. These shifts can be mediated through direct contact, toxic components, or indirect immune responses. Consequently, they influence various molecular metabolic events that impact nutritional status and iron absorption in the host. Unraveling the intricate and diverse molecular interaction links between H. pylori and human metabolism modulation is essential for understanding pathogenesis mechanisms and developing targeted treatments for related diseases. However, significant challenges persist in comprehensively understanding the complex association networks among H. pylori itself, the infected host's status, the host microbiome, and the immune response. Previous metabolomics research has indicated that H. pylori infection and eradication may selectively shape the metabolite and microbial profiles of gastric lesions. Yet, it remains largely unknown how these diverse metabolic pathways, including isovaleric acid, cholesterol, fatty acids, and phospholipids, specifically modulate gastric carcinogenesis or affect the host's serum metabolism, consequently leading to the development of metabolic-associated diseases. The direct contribution of H. pylori to metabolisms still lacks conclusive evidence. In this review, we summarize recent advances in clinical evidence highlighting associations between chronic H. pylori infection and metabolic diseases, as well as its potential molecular regulatory patterns.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13030Subventions
Organisme : China Postdoctoral Science Foundation
Organisme : National Natural Science Foundation of China
Organisme : Natural Science Foundation of Guangdong Province
Informations de copyright
© 2023 John Wiley & Sons Ltd.
Références
Usui Y, Taniyama Y, Endo M, et al. Helicobacter pylori, homologous-recombination genes, and gastric cancer. N Engl J Med. 2023;388(13):1181-1190.
Ma L, Guo W, Zeng Z, Yang F, Tang S, Ling Y. Colorectal cancer risk in east Asian patients with Helicobacter pylori infection: a systematic review and meta-analysis. Medicine (Baltimore). 2023;102(10):e33177.
Ford AC, Yuan Y, Forman D, Hunt R, Moayyedi P. Helicobacter pylori eradication for the prevention of gastric neoplasia. Cochrane Database Syst Rev. 2020;7(7):CD005583.
Mohammadi M, Attar A, Mohammadbeigi M, Peymani A, Bolori S, Fardsanei F. The possible role of Helicobacter pylori in liver diseases. Arch Microbiol. 2023;205(8):281.
Kaewpitoon SJ, Loyd RA, Rujirakul R, et al. Helicobacter species are possible risk factors of cholangiocarcinoma. Asian Pac J Cancer Prev. 2016;17(1):37-44.
Durazzo M, Adriani A, Fagoonee S, Saracco GM, Pellicano R. Helicobacter pylori and respiratory diseases: 2021 update. Microorganisms. 2021;9(10):2033.
Tong L, Wang BB, Li FH, Lv SP, Pan FF, Dong XJ. An updated meta-analysis of the relationship between Helicobacter pylori infection and the risk of coronary heart disease. Front Cardiovasc Med. 2022;9:794445.
Simon OA, Görbe A, Hegyi P, et al. Helicobacter pylori infection is associated with carotid intima and media thickening: a systematic review and meta-analysis. J Am Heart Assoc. 2022;11(3):e022919.
Kountouras J, Papaefthymiou A, Polyzos SA, et al. Impact of Helicobacter pylori-related metabolic syndrome parameters on arterial hypertension. Microorganisms. 2021;9(11):2351.
De Francesco V, Manta R, Marmo R, et al. Efficacy of Helicobater pylori eradication in patients with diffuse large B-cell lymphoma of the stomach: a systematic review. Eur J Haematol. 2022;109(6):643-647.
Wang B, Yu M, Zhang R, Chen S, Xi Y, Duan G. A meta-analysis of the association between Helicobacter pylori infection and risk of atherosclerotic cardiovascular disease. Helicobacter. 2020;25(6):e12761.
Wernly S, Semmler G, Völkerer A, et al. Helicobacter pylori and cardiovascular risk: only a dead Helicobacter is a good Helicobacter? Helicobacter. 2022;27(6):e12928.
Chung J, Min KW, Son BK, Kim DH, Kim HL. Association between histological severity of Helicobacter pylori infection and cardiovascular risk scores in the Korean population. Atherosclerosis. 2021;333:124-130.
Dore MP, Saba PS, Tomassini G, Niolu C, Monaco M, Pes GM. Increased risk to develop hypertension and carotid plaques in patients with long-lasting Helicobacter pylori gastritis. J Clin Med. 2022;11(9):2282.
Schöttker B, Adamu MA, Weck MN, Müller H, Brenner H. Helicobacter pylori infection, chronic atrophic gastritis and major cardiovascular events: a population-based cohort study. Atherosclerosis. 2012;220(2):569-574.
Feng Y, Zhou W, Luo L, Xu W. Helicobacter pylori infection is not related to increased carotid intima-media thickness in general population. Sci Rep. 2018;8(1):14180.
Xu G, Ma S, Dong L, Mendez-Sanchez N, Li H, Qi X. Relationship of Helicobacter pylori infection with nonalcoholic fatty liver disease: a meta-analysis. Can J Gastroenterol Hepatol. 2023;5521239. doi:10.1155/2023/5521239
Chen Y, You N, Shen C, Wu J, Zhang J. Helicobacter pylori infection increases the risk of nonalcoholic fatty liver disease in diabetic population. Front Nutr. 2023;10:1076579.
Liu Y, Xu H, Zhao Z, Dong Y, Wang X, Niu J. No evidence for a causal link between Helicobacter pylori infection and nonalcoholic fatty liver disease: a bidirectional mendelian randomization study. Front Microbiol. 2022;13:1018322.
Doulberis M, Srivastava S, Polyzos SA, et al. Active Helicobacter pylori infection is independently associated with nonalcoholic steatohepatitis in morbidly obese patients. J Clin Med. 2020;9(4):933.
Yu YY, Tong YL, Wu LY, Yu XY. Helicobacter pylori infection eradication for nonalcoholic fatty liver disease: a randomized controlled trial. Sci Rep. 2022;12(1):19530.
Huang J, Zhang K, Wang F, Tang X. The associations between Helicobacter pylori immunoglobulin G seropositivity and body mass index in adults. BMC Infect Dis. 2023;23(1):485.
Wu MS, Lee WJ, Wang HH, Huang SP, Lin JT. A case-control study of association of Helicobacter pylori infection with morbid obesity in Taiwan. Arch Intern Med. 2005;165(13):1552.
Pundak OY, Topf Olivestone C, Hofi L, Kori M. Lack of association between Helicobacter pylori infection and childhood overweight/obesity. Helicobacter. 2020;25(5):e12728.
Azami M, Baradaran HR, Dehghanbanadaki H, et al. Association of Helicobacter pylori infection with the risk of metabolic syndrome and insulin resistance: an updated systematic review and meta-analysis. Diabetol Metab Syndr. 2021;13(1):145.
Liu Y, Shuai P, Chen W, Liu Y, Li D. Association between Helicobacter pylori infection and metabolic syndrome and its components. Front Endocrinol. 2023;14:1188487.
Chen J, Xing Y, Zhao L, Ma H. The association between Helicobacter pylori infection and glycated hemoglobin a in diabetes: a meta-analysis. J Diabetes Res. 2019;2019:3705264.
Chen C, Wang J, Pan D, et al. Applications of multi-omics analysis in human diseases. MedComm. 2020;4(4):e315.
Zang H, Wang J, Wang H, et al. Metabolic alterations in patients with Helicobacter pylori-related gastritis: the H. pylori-gut microbiota-metabolism axis in progression of the chronic inflammation in the gastric mucosa. Helicobacter. 2023;28(4):e12984.
Tayyeb JZ, Popeijus HE, Mensink RP, Konings MCJM, Mokhtar FBA, Plat J. Short-chain fatty acids (except hexanoic acid) lower NF-kB transactivation, which rescues inflammation-induced decreased apolipoprotein A-I transcription in HepG2 cells. Int J Mol Sci. 2020;21(14):5088.
Yang H, Rothenberger E, Zhao T, et al. Regulation of inflammation in cancer by dietary eicosanoids. Pharmacol Ther. 2023;248:108455.
Saresella M, Marventano I, Barone M, et al. Alterations in circulating fatty acid are associated with gut microbiota dysbiosis and inflammation in multiple sclerosis. Front Immunol. 2020;11:1390.
Haghikia A, Jörg S, Duscha A, et al. Dietary fatty acids directly impact central nervous system autoimmunity via the small intestine. Immunity. 2015;43(4):817-829.
Arpaia N, Campbell C, Fan X, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451-455.
Wang J, Shan J, Zhang Y, et al. Targeted metabolomics analysis for serum Helicobacter pylori-positive based on liquid chromatography-tandem mass spectrometry. Biomed Chromatogr. 2023;37(6):e5622.
Jie L, Ma Z, Gao Y, et al. The mechanism of palmatine-mediated intestinal flora and host metabolism intervention in OA-OP comorbidity rats. Front Med (Lausanne). 2023;10:1153360.
Peng L, Guo Y, Gerhard M, et al. Metabolite alterations and interactions with microbiota in Helicobacter pylori-associated gastric lesions. Microbiol Spectr. 2023;11(4):e0534722.
Cai X, Li X, Jin Y, et al. Vitamins and Helicobacter pylori: an updated comprehensive meta-analysis and systematic review. Front Nutr. 2022;8:781333.
El Shahawy MS, Hemida MH, El Metwaly I, Shady ZM. The effect of vitamin D deficiency on eradication rates of Helicobacter pylori infection. JGH Open. 2018;2(6):270-275.
Han C, Ni Z, Yuan T, et al. Influence of serum vitamin D level on Helicobacter pylori eradication: a multi-center, observational, prospective and cohort study. J Dig Dis. 2019;20(8):421-426.
Zhang Y, Wang C, Zhang L, Yu J, Yuan W, Li L. Vitamin D3 eradicates Helicobacter pylori by inducing VDR-CAMP signaling. Front Microbiol. 2022;13:1033201.
Zhao S, Wan D, Zhong Y, Xu X. 1α, 25-Dihydroxyvitamin D3 protects gastric mucosa epithelial cells against Helicobacter pylori-infected apoptosis through a vitamin D receptor-dependent c-Raf/MEK/ERK pathway. Pharm Biol. 2022;60(1):801-809.
Nabavi-Rad A, Jamshidizadeh S, Azizi M, et al. The synergistic effect of Levilactobacillus brevis IBRC-M10790 and vitamin D3 on Helicobacter pylori-induced inflammation. Front Cell Infect Microbiol. 2023;13:1171469.
Gajewski AŁ, Gawrysiak M, Krupa A, et al. Accumulation of deleterious effects in gastric epithelial cells and vascular endothelial cells in vitro in the milieu of Helicobacter pylori components, 7-ketocholesterol and acetylsalicylic acid. Int J Mol Sci. 2022;23(11):6355.
Morey P, Pfannkuch L, Pang E, et al. Helicobacter pylori depletes cholesterol in gastric glands to prevent interferon gamma signaling and escape the inflammatory response. Gastroenterology. 2018;154(5):1391-1404.e9.
Nagata M, Toyonaga K, Ishikawa E, et al. Helicobacter pylori metabolites exacerbate gastritis through C-type lectin receptors. J Exp Med. 2021;218(1):e20200815.
Mohammadzadeh R, Menbari S, Pishdadian A, Farsiani H. Helicobacter pylori virulence factors: subversion of host immune system and development of various clinical outcomes. Expert Rev Mol Med. 2023;25:e23.
Aziz F, Chakraborty A, Liu K, et al. Gastric tumorigenesis induced by combining Helicobacter pylori infection and chronic alcohol through IL-10 inhibition. Carcinogenesis. 2022;43(2):126-139.
Mi C, Zhao Y, Ren L, Zhang D. Inhibition of MDFI attenuates proliferation and glycolysis of Helicobacter pylori-infected gastric cancer cells by inhibiting Wnt/β-catenin pathway. Cell Biol Int. 2022;46(12):2198-2206.
You N, Chen Y, Yan X, Gu B, Wang J, Zhang J. Persistent Helicobacter pylori infection leads to elevated fasting plasma glucose level: a retrospective cohort study based on a nondiabetes Chinese population. J Gastroenterol Hepatol. 2023.doi:10.1111/jgh.16275
Cheng KP, Yang YJ, Hung HC, et al. Helicobacter pylori eradication improves glycemic control in type 2 diabetes patients with asymptomatic active Helicobacter pylori infection. J Diabetes Investig. 2019;10(4):1092-1101.
Abdel-Razik A, Mousa N, Shabana W, et al. Helicobacter pylori and non-alcoholic fatty liver disease: a new enigma? Helicobacter. 2018;23(6):e12537.
Castaño-Rodríguez N, Mitchell HM, Kaakoush NO. NAFLD, Helicobacter species and the intestinal microbiome. Best Pract Res Clin Gastroenterol. 2017;31(6):657-668.
Peng C, Xu X, He Z, et al. Helicobacter pylori infection worsens impaired glucose regulation in high-fat diet mice in association with an altered gut microbiome and metabolome. Appl Microbiol Biotechnol. 2021;105(5):2081-2095.
Goo MJ, Ki MR, Lee HR, et al. Helicobacter pylori promotes hepatic fibrosis in the animal model. Lab Invest. 2009;89(11):1291-1303.
Ye Y, Yu B, Wang H, Yi F. Glutamine metabolic reprogramming in hepatocellular carcinoma. Front Mol Biosci. 2023;10:1242059.
Cassier-Chauvat C, Marceau F, Farci S, Ouchane S, Chauvat F. The glutathione system: a journey from cyanobacteria to higher eukaryotes. Antioxidants. 2023;12(6):1199.
Abnousian A, Vasquez J, Sasaninia K, Kelley M, Venketaraman V. Glutathione modulates efficacious changes in the immune response against tuberculosis. Biomedicine. 2023;11(5):1340.
Baskerville MJ, Kovalyova Y, Mejías-Luque R, Gerhard M, Hatzios SK. Isotope tracing reveals bacterial catabolism of host-derived glutathione during Helicobacter pylori infection. PLoS Pathog. 2023;19(7):e1011526.
Oertli M, Noben M, Engler DB, et al. Helicobacter pylori γ-glutamyl transpeptidase and vacuolating cytotoxin promote gastric persistence and immune tolerance. Proc Natl Acad Sci U S A. 2013;110(8):3047-3052.
Schmees C, Prinz C, Treptau T, et al. Inhibition of T-cell proliferation by Helicobacter pylori γ-glutamyl transpeptidase. Gastroenterology. 2007;132(5):1820-1833.
Nigatie M, Melak T, Asmelash D, Worede A. Dyslipidemia and its associated factors among helicobacter pylori-infected patients attending at University of Gondar Comprehensive Specialized Hospital, Gondar, north-West Ethiopia: a comparative Cross-sectional study. J Multidiscip Healthc. 2022;15:1481-1491.
Watanabe J, Hamasaki M, Kotani K. The effect of Helicobacter pylori eradication on lipid levels: a meta-analysis. J Clin Med. 2021;10(5):904.
Kim JW, Baeg MK, Bang CS, Park JK, Oh JH. Effect of Helicobacter pylori eradication on body weight: a multicenter propensity score-matched analysis in Korea. J Neurogastroenterol Motil. 2023;29(3):352-359.
Park J, Kim N, Kim WS, et al. Long-term effects of the eradication of Helicobacter pylori on metabolic parameters, depending on sex, in South Korea. Gut Liver. 2023;17(1):58-68.
Liou JM, Chen CC, Chang CM, et al. Long-term changes of gut microbiota, antibiotic resistance, and metabolic parameters after Helicobacter pylori eradication: a multicentre, open-label, randomised trial. Lancet Infect Dis. 2019;19(10):1109-1120.
Martín-Núñez GM, Cornejo-Pareja I, Roca-Rodríguez MDM, et al. H. pylori eradication treatment causes alterations in the gut microbiota and blood lipid levels. Front Med. 2020;7:417.
Ninomiya R, Kubo S, Baba T, et al. Inhibition of low-density lipoprotein uptake by Helicobacter pylori virulence factor CagA. Biochem Biophys Res Commun. 2021;556:192-198.
Ali-Berrada S, Guitton J, Tan-Chen S, Gyulkhandanyan A, Hajduch E, Le Stunff H. Circulating sphingolipids and glucose homeostasis: an update. Int J Mol Sci. 2023;24(16):12720.
Gaggini M, Fenizia S, Vassalle C. Sphingolipid levels and signaling via resveratrol and antioxidant actions in cardiometabolic risk and disease. Antioxidants. 2023;12(5):1102.
Pachathundikandi SK, Tegtmeyer N, Backert S. Masking of typical TLR4 and TLR5 ligands modulates inflammation and resolution by Helicobacter pylori. Trends Microbiol. 2023;31(9):903-915.
Miyata N, Hayashi Y, Hayashi S, et al. Lipopolysaccharides from non-Helicobacter pylori gastric bacteria potently stimulate Interleukin-8 production in gastric epithelial cells. Clin Transl Gastroenterol. 2019;10(3):e00024.
Kuuskmäe C, Philips M-A, Kilk K, et al. Kynurenine pathway dynamics in patients with schizophrenia spectrum disorders across the disease trajectory. Psychiatry Res. 2023;328:115423.
Schlichtner S, Yasinska IM, Klenova E, et al. L-kynurenine participates in cancer immune evasion by downregulating hypoxic signaling in T lymphocytes. Onco Targets Ther. 2023;12(1):2244330.
Comas-Ghierra R, Alshaheeb AA, McReynolds MR, Shepherd JN, Salinas G. A minimal kynurenine pathway was preserved for rhodoquinone but not for de novo NAD((+)) biosynthesis in parasitic worms: the essential role of NAD((+)) rescue pathways. Antioxid Redox Signal. 2023;8. doi:10.1089/ars.2023.0293. Online ahead of print.
Engin AB, Karahalil B, Karakaya AE, Engin A. Helicobacter pylori and serum kynurenine-tryptophan ratio in patients with colorectal cancer. World J Gastroenterol. 2015;21(12):3636-3643.
Liang X, Du W, Huang L, et al. Helicobacter pylori promotes gastric intestinal metaplasia through activation of IRF3-mediated kynurenine pathway. Cell Commun Signal. 2023;21(1):141.
Ganz T. Anemia of inflammation. N Engl J Med. 2019;381(12):1148-1157.
Muckenthaler MU, Rivella S, Hentze MW, Galy B. A red carpet for iron metabolism. Cell. 2017;168(3):344-361.
Britton L, Bridle K, Reiling J, et al. Hepatic iron concentration correlates with insulin sensitivity in nonalcoholic fatty liver disease. Hepatol Commun. 2018;2(6):644-653.
Simcox JA, McClain DA. Iron and diabetes risk. Cell Metab. 2013;17(3):329-341.
Britton LJ, Subramaniam VN, Crawford DH. Iron and non-alcoholic fatty liver disease. World J Gastroenterol. 2016;22(36):8112-8122.
Iijima K, Koike T, Abe Y, et al. Alteration of correlation between serum pepsinogen concentrations and gastric acid secretion after H. pylori eradication. J Gastroenterol. 2009;44(8):819-825.
Hudak L, Jaraisy A, Haj S, Muhsen K. An updated systematic review and meta-analysis on the association between Helicobacter pylori infection and iron deficiency anemia. Helicobacter. 2017;22(1):e12330.
Lee JY, Kim SE, Park SJ, et al. Helicobacter pylori infection and iron deficiency in non-elderly adults participating in a health check-up program. Korean J Intern Med. 2022;37(2):304-312.
McCaddon A, Miller JW. Homocysteine-a retrospective and prospective appraisal. Front Nutr. 2023;10:1179807.
Kountouras J, Doulberis M, Polyzos SA, et al. Impact of Helicobacter pylori-related metabolic syndrome with hyperhomocysteinemia on extragastric pathologies. J Gastroenterol Hepatol. 2022;37(2):407-408.
Chen Y, Xu C, Xu H, et al. Persistent Helicobacter pylori infection for more than 3 years leads to elevated serum homocysteine concentration: a retrospective cohort study based on a healthy Chinese population. J Gastroenterol Hepatol. 2021;36(11):3077-3083.
Afsar MNA, Jhinu ZN, Bhuiyan MAI, Islam Z, Siddiqua TJ. Helicobacter pylori infection and micronutrient deficiency in pregnant women: a systematic review and meta-analysis. BMJ Open Gastroenterol. 2020;7(1):e000490.