Impact of reactive oxygen species generation on Helicobacter pylori-related extragastric diseases: a hypothesis

Free Radical Research

Volumn 51, Issue 1, 2017, Pages 73-79

  Kountouras, Jannis ^a   Boziki, Marina ^a   Polyzos, Stergios A ^a   Katsinelos, Panagiotis ^a   Gavalas, Emmanouel ^a   Zeglinas, Christos ^a   Tzivras, Dimitri ^a   Romiopoulos, Iordanis ^a   Giorgakis, Nikolaos ^a   Anastasiadou, Kyriaki ^a   Vardaka, Elizabeth ^a   Kountouras, Constantinos ^a   Kazakos, Evangelos ^a   Xiromerisiou, Georgia ^b   Dardiotis, Efthimios ^c   Deretzi, Georgia ^b  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b PAPAGEORGIOU GENERAL HOSPITAL   (Greece)

^c UNIVERSITY OF THESSALY   (Greece)

Author keywords

Helicobacter pylori; inflammation; neurodegenerative diseases; neuroinflammation; Reactive oxygen species

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ALZHEIMER DISEASE; ARTICLE; BACTERIAL CLEARANCE; BARRETT ESOPHAGUS; COLORECTAL CANCER; DEGENERATIVE DISEASE; ESOPHAGEAL ADENOCARCINOMA; GLAUCOMA; HELICOBACTER PYLORI; HUMAN; MALIGNANT NEOPLASM; MULTIPLE SCLEROSIS; NONHUMAN; PATHOPHYSIOLOGY; STOMACH DISEASE; SYSTEMIC DISEASE; ANIMAL; HELICOBACTER INFECTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY;

ANIMALS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HOST-PATHOGEN INTERACTIONS; HUMANS; NEURODEGENERATIVE DISEASES; REACTIVE OXYGEN SPECIES;

EID: 85009809574     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.1080/10715762.2016.1271122     Document Type: Article

References (84)

1. Bhattacharyya A, Chattopadhyay R, Mitra S, Crowe SE., Oxidative stress:an essential factor in the pathogenesis of gastrointestinal mucosal diseases. Physiol Rev 2014;94:329–354.
2. Wei B, Huang Q, Huang S, Mai W, Zhong X., Trichosanthin-induced autophagy in gastric cancer cell MKN-45 is dependent on reactive oxygen species (ROS) and NF-kappaB/p53 pathway. J Pharmacol Sci 2016;131:77–83.
3. Taha AS, Dahill S, Morran C, Hudson N, Hawkey CJ, Lee FD, et al. Neutrophils, Helicobacter pylori, and nonsteroidal anti-inflammatory drug ulcers. Gastroenterology 1999;116:254–258.
4. Nair S, Norkus EP, Hertan H, Pitchumoni CS., Micronutrient antioxidants in gastric mucosa and serum in patients with gastritis and gastric ulcer:does Helicobacter pylori infection affect the mucosal levels? J Clin Gastroenterol 2000;30:381–385.
5. Augusto AC, Miguel F, Mendonca S, Pedrazzoli J, Jr, Gurgueira SA., Oxidative stress expression status associated to Helicobacter pylori virulence in gastric diseases. Clin Biochem 2007;40:615–622.
6. Bhattacharyya A, Chattopadhyay R, Hall EH, Mebrahtu ST, Ernst PB, Crowe SE., Mechanism of hypoxia-inducible factor 1 alpha-mediated Mcl1 regulation in Helicobacter pylori-infected human gastric epithelium. Am J Physiol Gastrointest Liver Physiol 2010;299:G1177–G1186.
7. Papa A, Danese S, Sgambato A, Ardito R, Zannoni G, Rinelli A, et al. Role of Helicobacter pylori CagA + infection in determining oxidative DNA damage in gastric mucosa. Scand J Gastroenterol 2002;37:409–413.
8. Handa O, Naito Y, Yoshikawa T., Redox biology and gastric carcinogenesis:the role of Helicobacter pylori. Redox Rep 2011;16:1–7.
9. Gobert AP, Wilson KT., Polyamine- and NADPH-dependent generation of ROS during Helicobacter pylori infection:a blessing in disguise. Free Radic Biol Med 2016. [Epub ahead of print].
10. Olatunji OJ, Chen H, Zhou Y., Anti-ulcerogenic properties of lycium chinense mill extracts against ethanol-induced acute gastric lesion in animal models and its active constituents. Molecules 2015;20:22553–22564.
11. De Luca C, Kharaeva Z, Korkina L., Is there a role for antioxidants in the prevention of infection-associated carcinogenesis and in the treatment of infection-driven tumors? CTMC 2015;15:120–135.
12. Zulueta A, Caretti A, Signorelli P, Ghidoni R., Resveratrol:a potential challenger against gastric cancer. World J Gastroenterol 2015;21:10636–10643.
13. Song JH, Han YM, Kim WH, Park JM, Jeong M, Go EJ, et al. Oxidative stress from reflux esophagitis to esophageal cancer:the alleviation with antioxidants. Free Radic Res 2016;50:1071–1079.
14. Almasaudi SB, El-Shitany NA, Abbas AT, Abdel-dayem UA, Ali SS, Al Jaouni SK, et al. Antioxidant, Anti-inflammatory, and antiulcer potential of manuka honey against gastric ulcer in rats. Oxid Med Cell Longev 2016;2016:3643824.
15. Franceschi F, Gasbarrini A, Polyzos SA, Kountouras J., Extragastric diseases and Helicobacter pylori. Helicobacter 2015;20(Suppl 1):40–46.
16. Kountouras J, Chatzopoulos D, Zavos C., Reactive oxygen metabolites and upper gastrointestinal diseases. Hepatogastroenterology 2001; 48:743–751.
17. Gonzalez-Segovia R, Quintanar JL, Salinas E, Ceballos-Salazar R, Aviles-Jimenez F, Torres-Lopez J., Effect of the flavonoid quercetin on inflammation and lipid peroxidation induced by Helicobacter pylori in gastric mucosa of guinea pig. J Gastroenterol 2008;43:441–447.
18. Kountouras J, Zavos C, Diamantidis MD, Deretzi G, Grigoriadis N, Tsapournas G, et al. A concept of Helicobacter pylori and stress-secreted mast cells' potential involvement in brain metastases. J Neuroimmunol 2009;209:121–122.
19. Kountouras J, Gavalas E, Deretzi G, Boziki M, Zavos C, Chatzopoulos D, et al. Helicobacter pylori with or without its neutrophil-activating protein may be the common denominator associated with multiple sclerosis and neuromyelitis optica. Mult Scler 2010;16:376–377. author reply 8-9.
20. Tsai CC, Kuo TY, Hong ZW, Yeh YC, Shih KS, Du SY, et al. Helicobacter pylori neutrophil-activating protein induces release of histamine and interleukin-6 through G protein-mediated MAPKs and PI3K/Akt pathways in HMC-1 cells. Virulence 2015;6:755–765.
21. Kottakis F, Kouzi-Koliakou K, Pendas S, Kountouras J, Choli-Papadopoulou T., Effects of mastic gum Pistacia lentiscus var. Chia on innate cellular immune effectors. Eur J Gastroenterol Hepatol 2009;21:143–149.
22. Li W, Minohara M, Piao H, Matsushita T, Masaki K, Matsuoka T, et al. Association of anti-Helicobacter pylori neutrophil-activating protein antibody response with anti-aquaporin-4 autoimmunity in Japanese patients with multiple sclerosis and neuromyelitis optica. Mult Scler 2009; 15:1411–1421.
23. Kountouras J, Zavos C, Deretzi G, Gavalas E, Chatzopoulos D, Katsinelos P, et al. Potential implications of Helicobacter pylori-related neutrophil-activating protein. World J Gastroenterol 2012; 18:489–490.
24. Di Dalmazi G, Hirshberg J, Lyle D, Freij JB, Caturegli P., Reactive oxygen species in organ-specific autoimmunity. Autoimmun Highlights 2016;7:11.
25. Kountouras J, Boziki M, Zavos C, Gavalas E, Giartza-Taxidou E, Venizelos I, et al. A potential impact of chronic Helicobacter pylori infection on Alzheimer's disease pathobiology and course. Neurobiol Aging 2012;33:e3–e4.
26. Garcia-Redondo AB, Aguado A, Briones AM, Salaices M., NADPH oxidases and vascular remodeling in cardiovascular diseases. Pharmacol Res 2016; 114:110–120.
27. Rochfort KD, Cummins PM., The blood-brain barrier endothelium:a target for pro-inflammatory cytokines. Biochm Soc Trans 2015;43:702–706.
28. Tsugawa H, Suzuki H, Saya H, Hatakeyama M, Hirayama T, Hirata K, et al. Reactive oxygen species-induced autophagic degradation of Helicobacter pylori CagA is specifically suppressed in cancer stem-like cells. Cell Host Microbe 2012;12:764–777.
29. Kountouras J, Kapetanakis N., CD44 and Helicobacter pylori-related colon oncogenesis. Saudi Med J 2015; 36:1249.
30. Skaper SD., Mast Cell–glia dialogue in chronic pain and neuropathic pain:blood-brain barrier implications. CNS Neurol Disord Drug Targets 2016;15:1072–1078.
31. Kountouras J, Tsolaki M, Boziki M, Gavalas E, Zavos C, Stergiopoulos C, et al. Association between Helicobacter pylori infection and mild cognitive impairment. Eur J Neurol 2007;14:976–982.
32. Kountouras J, Polyzos SA, Gavalas E, Boziki M, Katsinelos P, Zeglinas C, et al. A potential impact of Helicobacter pylori infection on minimal hepatic encephalopathy pathobiology. J Gastrointestin Liver Dis 2016;25:405–406.
33. Kountouras J, Tsolaki M, Gavalas E, Boziki M, Zavos C, Karatzoglou P, et al. Relationship between Helicobacter pylori infection and Alzheimer disease. Neurology 2006;66:938–940.
34. Smith AD, Refsum H., Homocysteine, B vitamins, and cognitive impairment. Annu Rev Nutr 2016;36:211–239.
35. Wang XL, Zeng J, Feng J, Tian YT, Liu YJ, Qiu M, et al. Helicobacter pylori filtrate impairs spatial learning and memory in rats and increases beta-amyloid by enhancing expression of presenilin-2. Front Aging Neurosci 2014;6:66.
36. Wang XL, Zeng J, Yang Y, Xiong Y, Zhang ZH, Qiu M, et al. Helicobacter pylori filtrate induces Alzheimer-like tau hyperphosphorylation by activating glycogen synthase kinase-3beta. J Alzheimers Dis 2015;43:153–165.
37. Gavalas E, Kountouras J, Boziki M, Zavos C, Polyzos SA, Vlachaki E, et al. Relationship between Helicobacter pylori infection and multiple sclerosis. Ann Gastroenterol 2015;28:353–356.
38. Schuessel K, Schafer S, Bayer TA, Czech C, Pradier L, Muller-Spahn F, et al. Impaired Cu/Zn-SOD activity contributes to increased oxidative damage in APP transgenic mice. Neurobiol Dis 2005;18:89–99.
39. Murakami K, Murata N, Noda Y, Tahara S, Kaneko T, Kinoshita N, et al. SOD1 (copper/zinc superoxide dismutase) deficiency drives amyloid beta protein oligomerization and memory loss in mouse model of Alzheimer disease. J Biol Chem 2011;286:44557–44568.
40. Strozyk D, Launer LJ, Adlard PA, Cherny RA, Tsatsanis A, Volitakis I, et al. Zinc and copper modulate Alzheimer Abeta levels in human cerebrospinal fluid. Neurobiol Aging 2009;30:1069–1077.
41. Pal A, Badyal RK, Vasishta RK, Attri SV, Thapa BR, Prasad R., Biochemical, histological, and memory impairment effects of chronic copper toxicity:a model for non-Wilsonian brain copper toxicosis in Wistar rat. Biol Trace Elem Res 2013;153:257–268.
42. 2. J Neurochem 2013;126:234–242.
43. Gandy JC, Melendez-Ferro M, Bijur GN, Van Leuven F, Roche JK, Lechat B, et al. Glycogen synthase kinase-3beta (GSK3beta) expression in a mouse model of Alzheimer's disease:a light and electron microscopy study. Synapse 2013;67:313–327.
44. Farr SA, Ripley JL, Sultana R, Zhang Z, Niehoff ML, Platt TL, et al. Antisense oligonucleotide against GSK-3beta in brain of SAMP8 mice improves learning and memory and decreases oxidative stress:involvement of transcription factor Nrf2 and implications for Alzheimer disease. Free Radic Biol Med 2014;67:387–395.
45. Hoppe JB, Frozza RL, Horn AP, Comiran RA, Bernardi A, Campos MM, et al. Amyloid-beta neurotoxicity in organotypic culture is attenuated by melatonin:involvement of GSK-3beta, tau and neuroinflammation. J Pineal Res 2010;48:230–238.
46. Teixeira J, Silva T, Andrade PB, Borges F., Alzheimer's disease and antioxidant therapy:how long how far? Curr Med Chem 2013;20:2939–2952.
47. Wood PL, Khan MA, Moskal JR., The concept of “aldehyde load” in neurodegenerative mechanisms:cytotoxicity of the polyamine degradation products hydrogen peroxide, acrolein, 3-aminopropanal, 3-acetamidopropanal and 4-aminobutanal in a retinal ganglion cell line. Brain Res 2007;1145:150–156.
48. Di Filippo M, de Iure A, Giampa C, Chiasserini D, Tozzi A, Orvietani PL, et al. Persistent activation of microglia and NADPH oxidase [corrected] drive hippocampal dysfunction in experimental multiple sclerosis. Sci Rep 2016;6:20926.
49. Wilson C, Nunez MT, Gonzalez-Billault C., Contribution of NADPH oxidase to the establishment of hippocampal neuronal polarity in culture. J Cell Sci 2015;128:2989–2995.
50. Fischer MT, Sharma R, Lim JL, Haider L, Frischer JM, Drexhage J, et al. NADPH oxidase expression in active multiple sclerosis lesions in relation to oxidative tissue damage and mitochondrial injury. Brain 2012;135(Pt 3):886–899.
51. Kountouras J., Helicobacter pylori:an intruder involved in conspiring glaucomatous neuropathy. Br J Ophthalmol 2009;93:1413–1415.
52. Zavos C, Kountouras J., Further data on the association between Helicobacter pylori infection and primary open-angle glaucoma. Clin Ophthalmol 2012;6:243–245.
53. Babizhayev MA., Generation of reactive oxygen species in the anterior eye segment. Synergistic codrugs of N-acetylcarnosine lubricant eye drops and mitochondria-targeted antioxidant act as a powerful therapeutic platform for the treatment of cataracts and primary open-angle glaucoma. BBA Clin 2016;6:49–68.
54. Nita M, Grzybowski A., The role of the reactive oxygen species and oxidative stress in the pathomechanism of the age-related ocular diseases and other pathologies of the anterior and posterior eye segments in adults. Oxid Med Cell Longev 2016;2016:3164734.
55. Kountouras J, Zavos C, Chatzopoulos D., Induction of apoptosis as a proposed pathophysiological link between glaucoma and Helicobacter pylori infection. Med Hypotheses 2004;62:378–381.
56. Siu AW, Shan SW, Li KK, Lam HY, Fung MY, To CH, et al. Glutathione attenuates nitric oxide-induced retinal lipid and protein changes. Ophthalmic Physiol Opt 2015;35:135–146.
57. Sarenac Vulovic TS, Pavlovic SM, Jakovljevic V, Janicijevic KB, Zdravkovic NS., Nitric oxide and tumour necrosis factor alpha in the process of pseudoexfoliation glaucoma. Int J Ophthalmol 2016;9:1138–1142.
58. Kountouras J, Mylopoulos N, Chatzopoulos D, Zavos C, Boura P, Konstas AG, et al. Eradication of Helicobacter pylori may be beneficial in the management of chronic open-angle glaucoma. Arch Intern Med 2002;162:1237–1244.
59. Kountouras J, Boziki M, Gavalas E, Zavos C, Grigoriadis N, Deretzi G, et al. Eradication of Helicobacter pylori may be beneficial in the management of Alzheimer's disease. J Neurol 2009;256:758–767.
60. Chang YP, Chiu GF, Kuo FC, Lai CL, Yang YH, Hu HM, et al. Eradication of Helicobacter pylori is associated with the progression of dementia:a population-based study. Gastroenterol Res Pract 2013;2013:175729.
61. Adriani A, Fagoonee S,D, Angelis C, Altruda F, Pellicano R., Helicobacter pylori infection and dementia:can actual data reinforce the hypothesis of a causal association? Panminerva Med 2014;56:195–199.
62. Deretzi G, Gavalas E, Boziki M, Tsiptsios D, Polyzos SA, Venizelos I, et al. Impact of Helicobacter pylori on multiple sclerosis-related clinically isolated syndrome. Acta Neurol Scand 2016;133:268–275.
63. Gaskin J, Gomes J, Darshan S, Krewski D., Burden of neurological conditions in Canada. Neurotoxicology 2016. [Epub ahead of print]. doi:10.1016/j.neuro.2016.05.001.
64. Fiest KM, Roberts JI, Maxwell CJ, Hogan DB, Smith EE, Frolkis A, et al. The prevalence and incidence of dementia due to Alzheimer's Disease:a systematic review and meta-analysis. Can J Neurol Sci 2016;43 (Suppl 1):S51–S82.
65. Howard J, Trevick S, Younger DS., Epidemiology of multiple sclerosis. Neurol Clin 2016;34:919–939.
66. Bourne RR, Taylor HR, Flaxman SR, Keeffe J, Leasher J, Naidoo K, et al. Number of people blind or visually impaired by glaucoma worldwide and in world regions 1990–2010:a meta-analysis. PLoS ONE 2016;11:e0162229.
67. Siersema PD, Yu S, Sahbaie P, Steyerberg EW, Simpson PW, Kuipers EJ, et al. Colorectal neoplasia in veterans is associated with Barrett's esophagus but not with proton-pump inhibitor or aspirin/NSAID use. Gastrointest Endosc 2006;63:581–586.
68. Andrici J, Tio M, Cox MR, Eslick GD., Meta-analysis:Barrett's oesophagus and the risk of colonic tumours. Aliment Pharmacol Ther 2013;37:401–410.
69. Sonnenberg A, Genta RM., Barrett's metaplasia and colonic neoplasms:a significant association in a 203,534-patient study. Dig Dis Sci 2013;58:2046–2051.
70. Gatalica Z, Chen M, Snyder C, Mittal S, Lynch HT., Barrett's esophagus in the patients with familial adenomatous polyposis. Fam Cancer 2014;13:213–217.
71. Kountouras J, Zavos C, Chatzopoulos D., Pathogenetic links between colorectal neoplasia and Barrett's esophagus. Gastrointest Endosc 2006;64:298.
72. Marley AR, Nan H., Epidemiology of colorectal cancer. Int J Mol Epidemiol Genet 2016;7:105–114.
73. Mozdiak E, Tsertsvadze A, McFarlane M, Widlak M, Tabuso M, Dunlop A, et al. The effect of the 2-week wait referral system on the detection of and mortality from colorectal cancer:protocol of a systematic review and meta-analysis. Syst Rev 2016;5:182.
74. Mansour NM, Groth SS, Anandasabapathy S., Esophageal adenocarcinoma:screening, surveillance, and management. Annu Rev Med 2016. [Epub ahead of print].
75. Eusebi LH, Zagari RM, Bazzoli F., Epidemiology of Helicobacter pylori infection. Helicobacter 2014;19(Suppl 1):1–5.
76. Kapetanakis N, Kountouras J, Zavos C, Michael S, Tsarouchas G, Gavalas E, et al. Re:Helicobacter pylori infection and colorectal cancer risk:evidence from a large population-based case-control study in Germany. Am J Epidemiol 2012; 176:566–567.
77. Kountouras J, Kapetanakis N, Zavos C, Romiopoulos I., Impact of Helicobacter pylori infection on normal colorectal mucosa, adenomatous polyps and adenocarcinoma sequence. Colorectal Dis 2014;16:390–391.
78. Sonnenberg A, Genta RM., Helicobacter pylori is a risk factor for colonic neoplasms. Am J Gastroenterol 2013;108:208–215.
79. Selgrad M, Bornschein J, Kandulski A, Hille C, Weigt J, Roessner A, et al. Helicobacter pylori but not gastrin is associated with the development of colonic neoplasms. Int J Cancer 2014;135:1127–1131.
80. Joo JH, Oh H, Kim M, An EJ, Kim RK, Lee SY, et al. NADPH oxidase 1 activity and ROS generation are regulated by Grb2/Cbl-mediated proteasomal degradation of NoxO1 in colon cancer cells. Cancer Res 2016;76:855–865.
81. Kountouras J, Polyzos SA, Zeglinas C, Katsinelos P, Giorgakis N, Vardaka E, et al. Helicobacter pylori infection and oesophageal adenocarcinoma. Cancer Epidemiol 2016;42:206–207.
82. Li D, Cao W., Bile acid receptor TGR5, NADPH Oxidase NOX5-S and CREB mediate bile acid-induced DNA damage in Barrett's esophageal adenocarcinoma cells. Sci Rep 2016;6:31538.
83. Theoharides TC, Rozniecki JJ, Sahagian G, Jocobson S, Kempuraj D, Conti P, et al. Impact of stress and mast cells on brain metastases. J Neuroimmunol 2008;205:1–7.
84. Ribatti D, Crivellato E., Mast cells, angiogenesis and cancer. Adv Exp Med Biol 2011;716:270–288.