Spermine oxidase mediates Helicobacter pylori-induced gastric inflammation, DNA damage, and carcinogenic signaling.
Adenocarcinoma
/ etiology
Animals
Cell Transformation, Neoplastic
DNA Damage
Gastritis
/ enzymology
Helicobacter Infections
/ enzymology
Helicobacter pylori
/ pathogenicity
Mice
Mice, Inbred C57BL
Mice, Knockout
Organoids
Oxidoreductases Acting on CH-NH Group Donors
/ deficiency
Proteome
RNA, Messenger
/ biosynthesis
Signal Transduction
Spermidine
/ biosynthesis
Spermine
/ metabolism
Stomach Neoplasms
/ etiology
beta Catenin
/ physiology
Polyamine Oxidase
Journal
Oncogene
ISSN: 1476-5594
Titre abrégé: Oncogene
Pays: England
ID NLM: 8711562
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
26
11
2019
accepted:
16
04
2020
revised:
14
04
2020
pubmed:
1
5
2020
medline:
1
12
2020
entrez:
1
5
2020
Statut:
ppublish
Résumé
Helicobacter pylori infection is the main risk factor for the development of gastric cancer, the third leading cause of cancer death worldwide. H. pylori colonizes the human gastric mucosa and persists for decades. The inflammatory response is ineffective in clearing the infection, leading to disease progression that may result in gastric adenocarcinoma. We have shown that polyamines are regulators of the host response to H. pylori, and that spermine oxidase (SMOX), which metabolizes the polyamine spermine into spermidine plus H
Identifiants
pubmed: 32350444
doi: 10.1038/s41388-020-1304-6
pii: 10.1038/s41388-020-1304-6
pmc: PMC7260102
mid: NIHMS1585637
doi:
Substances chimiques
CTNNB1 protein, mouse
0
Proteome
0
RNA, Messenger
0
beta Catenin
0
Spermine
2FZ7Y3VOQX
Oxidoreductases Acting on CH-NH Group Donors
EC 1.5.-
Spermidine
U87FK77H25
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4465-4474Subventions
Organisme : NCI NIH HHS
ID : P01 CA028842
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK123704
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA190612
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI142042
Pays : United States
Organisme : NCCIH NIH HHS
ID : R01 AT006896
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA116087
Pays : United States
Organisme : BLRD VA
ID : I01 BX001453
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA100603
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK058404
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM131408
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA076292
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK034854
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA068485
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA204345
Pays : United States
Organisme : CSRD VA
ID : I01 CX002171
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA235863
Pays : United States
Organisme : NIDDK NIH HHS
ID : R03 DK107960
Pays : United States
Références
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.
Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, et al. Helicobacter pylori infection and the development of gastric cancer. N. Engl J Med. 2001;345:784–9.
doi: 10.1056/NEJMoa001999
Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology. 2017;153:420–9.
doi: 10.1053/j.gastro.2017.04.022
Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, et al. Helicobacter pylori infection and the risk of gastric carcinoma. N. Engl J Med. 1991;325:1127–31.
doi: 10.1056/NEJM199110173251603
Correa P. A human model of gastric carcinogenesis. Cancer Res. 1988;48:3554–60.
pubmed: 3288329
Mera RM, Bravo LE, Camargo MC, Bravo JC, Delgado AG, Romero-Gallo J, et al. Dynamics of Helicobacter pylori infection as a determinant of progression of gastric precancerous lesions: 16-year follow-up of an eradication trial. Gut. 2018;67:1239–46.
doi: 10.1136/gutjnl-2016-311685
Pegg AE. Functions of polyamines in mammals. J Biol Chem. 2016;291:14904–12.
doi: 10.1074/jbc.R116.731661
Chaturvedi R, Asim M, Hoge S, Lewis ND, Singh K, Barry DP, et al. Polyamines impair immunity to Helicobacter pylori by inhibiting L-Arginine uptake required for nitric oxide production. Gastroenterology. 2010;139:1686–98. 1698 e1681–1686.
doi: 10.1053/j.gastro.2010.06.060
Patchett SE, Alstead EM, Butruk L, Przytulski K, Farthing MJ. Ornithine decarboxylase as a marker for premalignancy in the stomach. Gut. 1995;37:13–6.
doi: 10.1136/gut.37.1.13
Hardbower DM, Asim M, Luis PB, Singh K, Barry DP, Yang C, et al. Ornithine decarboxylase regulates M1 macrophage activation and mucosal inflammation via histone modifications. Proc Natl Acad Sci USA. 2017;114:E751–60.
doi: 10.1073/pnas.1614958114
Chaturvedi R, de Sablet T, Asim M, Piazuelo MB, Barry DP, Verriere TG, et al. Increased Helicobacter pylori-associated gastric cancer risk in the Andean region of Colombia is mediated by spermine oxidase. Oncogene. 2015;34:3429–40.
doi: 10.1038/onc.2014.273
Sierra JC, Suarez G, Piazuelo MB, Luis PB, Baker DR, Romero-Gallo J, et al. alpha-Difluoromethylornithine reduces gastric carcinogenesis by causing mutations in Helicobacter pylori cagY. Proc Natl Acad Sci USA. 2019;116:5077–85.
doi: 10.1073/pnas.1814497116
Wang Y, Devereux W, Woster PM, Stewart TM, Hacker A, Casero RA Jr. Cloning and characterization of a human polyamine oxidase that is inducible by polyamine analogue exposure. Cancer Res. 2001;61:5370–3.
pubmed: 11454677
Vujcic S, Diegelman P, Bacchi CJ, Kramer DL, Porter CW. Identification and characterization of a novel flavin-containing spermine oxidase of mammalian cell origin. Biochem J. 2002;367:665–75.
doi: 10.1042/bj20020720
Xu H, Chaturvedi R, Cheng Y, Bussiere FI, Asim M, Yao MD, et al. Spermine oxidation induced by Helicobacter pylori results in apoptosis and DNA damage: implications for gastric carcinogenesis. Cancer Res. 2004;64:8521–5.
doi: 10.1158/0008-5472.CAN-04-3511
Hardbower DM, de Sablet T, Chaturvedi R, Wilson KT. Chronic inflammation and oxidative stress: the smoking gun for Helicobacter pylori-induced gastric cancer? Gut Microbes. 2013;4:475–81.
doi: 10.4161/gmic.25583
Chaturvedi R, Asim M, Piazuelo MB, Yan F, Barry DP, Sierra JC, et al. Activation of EGFR and ERBB2 by Helicobacter pylori results in survival of gastric epithelial cells with DNA damage. Gastroenterology. 2014;146:1739–51. e1714.
doi: 10.1053/j.gastro.2014.02.005
Chaturvedi R, Asim M, Romero-Gallo J, Barry DP, Hoge S, de Sablet T, et al. Spermine oxidase mediates the gastric cancer risk associated with Helicobacter pylori CagA. Gastroenterology. 2011;141:1696–708. e1691–1692.
doi: 10.1053/j.gastro.2011.07.045
Radulescu S, Ridgway RA, Cordero J, Athineos D, Salgueiro P, Poulsom R, et al. Acute WNT signalling activation perturbs differentiation within the adult stomach and rapidly leads to tumour formation. Oncogene. 2013;32:2048–57.
doi: 10.1038/onc.2012.224
Clements WM, Wang J, Sarnaik A, Kim OJ, MacDonald J, Fenoglio-Preiser C, et al. beta-Catenin mutation is a frequent cause of Wnt pathway activation in gastric cancer. Cancer Res. 2002;62:3503–6.
pubmed: 12067995
Ebert MP, Fei G, Kahmann S, Muller O, Yu J, Sung JJ, et al. Increased beta-catenin mRNA levels and mutational alterations of the APC and beta-catenin gene are present in intestinal-type gastric cancer. Carcinogenesis. 2002;23:87–91.
doi: 10.1093/carcin/23.1.87
Hardbower DM, Singh K, Asim M, Verriere TG, Olivares-Villagomez D, Barry DP, et al. EGFR regulates macrophage activation and function in bacterial infection. J Clin Invest. 2016;126:3296–312.
doi: 10.1172/JCI83585
Lewis ND, Asim M, Barry DP, de Sablet T, Singh K, Piazuelo MB, et al. Immune evasion by Helicobacter pylori is mediated by induction of macrophage arginase II. J Immunol. 2011;186:3632–41.
doi: 10.4049/jimmunol.1003431
Sierra JC, Asim M, Verriere TG, Piazuelo MB, Suarez G, Romero-Gallo J, et al. Epidermal growth factor receptor inhibition downregulates Helicobacter pylori-induced epithelial inflammatory responses, DNA damage and gastric carcinogenesis. Gut. 2018;67:1247–60.
doi: 10.1136/gutjnl-2016-312888
Toller IM, Neelsen KJ, Steger M, Hartung ML, Hottiger MO, Stucki M, et al. Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proc Natl Acad Sci USA. 2011;108:14944–9.
doi: 10.1073/pnas.1100959108
Franco AT, Israel DA, Washington MK, Krishna U, Fox JG, Rogers AB, et al. Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc Natl Acad Sci USA. 2005;102:10646–51.
doi: 10.1073/pnas.0504927102
Cancer Genome Atlas Research N. Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014;513:202–9.
doi: 10.1038/nature13480
Xue J, Chen Y, Wu Y, Wang Z, Zhou A, Zhang S, et al. Tumour suppressor TRIM33 targets nuclear beta-catenin degradation. Nat Commun. 2015;6:6156.
doi: 10.1038/ncomms7156
Sebrell TA, Sidar B, Bruns R, Wilkinson RA, Wiedenheft B, Taylor PJ, et al. Live imaging analysis of human gastric epithelial spheroids reveals spontaneous rupture, rotation and fusion events. Cell Tissue Res. 2018;371:293–307.
doi: 10.1007/s00441-017-2726-5
Holshouser S, Dunworth M, Murray-Stewart T, Peterson YK, Burger P, Kirkpatrick J, et al. Dual inhibitors of LSD1 and spermine oxidase. Medchemcomm. 2019;10:778–90.
doi: 10.1039/C8MD00610E
Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol. 2002;22:1172–83.
doi: 10.1128/MCB.22.4.1172-1183.2002
Malfertheiner P, Megraud F, O’Morain CA, Atherton J, Axon AT, Bazzoli F, et al. Management of Helicobacter pylori infection-the Maastricht IV/ Florence consensus report. Gut. 2012;61:646–64.
doi: 10.1136/gutjnl-2012-302084
Morgan DR, Torres J, Sexton R, Herrero R, Salazar-Martinez E, Greenberg ER, et al. Risk of recurrent Helicobacter pylori infection 1 year after initial eradication therapy in 7 Latin American communities. JAMA. 2013;309:578–86.
doi: 10.1001/jama.2013.311
Gobert AP, Al-Greene NT, Singh K, Coburn LA, Sierra JC, Verriere TG, et al. Distinct immunomodulatory effects of spermine oxidase in colitis induced by epithelial injury or infection. Front Immunol. 2018;9:1242.
doi: 10.3389/fimmu.2018.01242
Goodwin AC, Destefano Shields CE, Wu S, Huso DL, Wu X, Murray-Stewart TR, et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci USA. 2011;108:15354–9.
doi: 10.1073/pnas.1010203108
Jaiswal M, LaRusso NF, Gores GJ. Nitric oxide in gastrointestinal epithelial cell carcinogenesis: linking inflammation to oncogenesis. Am J Physiol Gastrointest Liver Physiol. 2001;281:G626–34.
doi: 10.1152/ajpgi.2001.281.3.G626
Chaturvedi R, Cheng Y, Asim M, Bussiere FI, Xu H, Gobert AP, et al. Induction of polyamine oxidase 1 by Helicobacter pylori causes macrophage apoptosis by hydrogen peroxide release and mitochondrial membrane depolarization. J Biol Chem. 2004;279:40161–73.
doi: 10.1074/jbc.M401370200
Yong X, Tang B, Xiao YF, Xie R, Qin Y, Luo G, et al. Helicobacter pylori upregulates Nanog and Oct4 via Wnt/beta-catenin signaling pathway to promote cancer stem cell-like properties in human gastric cancer. Cancer Lett. 2016;374:292–303.
doi: 10.1016/j.canlet.2016.02.032
Murata-Kamiya N, Kurashima Y, Teishikata Y, Yamahashi Y, Saito Y, Higashi H, et al. Helicobacter pylori CagA interacts with E-cadherin and deregulates the beta-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene. 2007;26:4617–26.
doi: 10.1038/sj.onc.1210251
Guo X, Rao JN, Liu L, Rizvi M, Turner DJ, Wang JY. Polyamines regulate beta-catenin tyrosine phosphorylation via Ca(2+) during intestinal epithelial cell migration. Am J Physiol Cell Physiol. 2002;283:C722–34.
doi: 10.1152/ajpcell.00054.2002