Full Text:   <421>

Summary:  <138>

Suppl. Mater.: 

CLC number: R573.9

On-line Access: 2018-09-30

Received: 2017-09-08

Revision Accepted: 2018-02-07

Crosschecked: 2018-09-11

Cited: 0

Clicked: 1714

Citations:  Bibtex RefMan EndNote GB/T7714

 ORCID:

Yan-yan Shi

https://orcid.org/0000-0003-0247-371X

Shi-gang Ding

https://orcid.org/0000-0002-0831-0965

-   Go to

Article info.
Open peer comments

Journal of Zhejiang University SCIENCE B 2018 Vol.19 No.10 P.750-763

10.1631/jzus.B1700456


Cellular stress and redox activity proteins are involved in gastric carcinogenesis associated with Helicobacter pylori infection expressing high levels of thioredoxin-1


Author(s):  Yan-yan Shi, Jing Zhang, Ting Zhang, Man Zhou, Ye Wang, He-jun Zhang, Shi-gang Ding

Affiliation(s):  Research Center of Clinical Epidemiology, Peking University Third Hospital, Beijing 100191, China; more

Corresponding email(s):   dingshigang222@163.com

Key Words:  Thioredoxin-1 (Trx1), Helicobacter pylori, Gastric carcinogenesis, Proteomics, Isobaric tags for relative and absolute quantitation (iTRAQ)


Yan-yan Shi, Jing Zhang, Ting Zhang, Man Zhou, Ye Wang, He-jun Zhang, Shi-gang Ding. Cellular stress and redox activity proteins are involved in gastric carcinogenesis associated with Helicobacter pylori infection expressing high levels of thioredoxin-1[J]. Journal of Zhejiang University Science B, 2018, 19(10): 750-763.

@article{title="Cellular stress and redox activity proteins are involved in gastric carcinogenesis associated with Helicobacter pylori infection expressing high levels of thioredoxin-1",
author="Yan-yan Shi, Jing Zhang, Ting Zhang, Man Zhou, Ye Wang, He-jun Zhang, Shi-gang Ding",
journal="Journal of Zhejiang University Science B",
volume="19",
number="10",
pages="750-763",
year="2018",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1700456"
}

%0 Journal Article
%T Cellular stress and redox activity proteins are involved in gastric carcinogenesis associated with Helicobacter pylori infection expressing high levels of thioredoxin-1
%A Yan-yan Shi
%A Jing Zhang
%A Ting Zhang
%A Man Zhou
%A Ye Wang
%A He-jun Zhang
%A Shi-gang Ding
%J Journal of Zhejiang University SCIENCE B
%V 19
%N 10
%P 750-763
%@ 1673-1581
%D 2018
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1700456

TY - JOUR
T1 - Cellular stress and redox activity proteins are involved in gastric carcinogenesis associated with Helicobacter pylori infection expressing high levels of thioredoxin-1
A1 - Yan-yan Shi
A1 - Jing Zhang
A1 - Ting Zhang
A1 - Man Zhou
A1 - Ye Wang
A1 - He-jun Zhang
A1 - Shi-gang Ding
J0 - Journal of Zhejiang University Science B
VL - 19
IS - 10
SP - 750
EP - 763
%@ 1673-1581
Y1 - 2018
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1700456


Abstract: 
Helicobacter pylori infection is related to the development of gastric diseases. Our previous studies showed that high thioredoxin-1 (Trx1) expression in H. pylori can promote gastric carcinogenesis. To explore the underlying molecular mechanisms, we performed an isobaric tags for relative and absolute quantitation (iTRAQ)-based quantitative proteomic analysis of stomach tissues from Mongolian gerbil infected with H. pylori expressing high and low Trx1. Differences in the profiles of the expressed proteins were analyzed by bioinformatics and verified using Western blot analysis. We found three candidate proteins, 14-3-3α/β, glutathione-S-transferase (GST), and heat shock protein 70 (HSP70), in high Trx1 tissues compared with low Trx1 tissues and concluded that cellular stress and redox activity-related proteins were involved in the pathogenesis of gastric cancer associated with H. pylori Trx1.

细胞应激和氧化还原活性蛋白参与硫氧还蛋白-1高表达幽门螺杆菌感染所致胃黏膜的癌变

目的:探索高表达硫氧还蛋白-1(Trx1)的幽门螺杆菌在致胃黏膜癌变过程中的作用机制.
创新点:首次分析临床分离菌株感染蒙古沙土鼠的胃黏膜疾病动物模型,首次对不同菌株感染所致的胃黏膜癌变相关分子机制进行探索.
方法:用同位素标记相对和绝对定量(iTRAQ)蛋白质组学及生物信息学分析方法进行分析,并用免疫印迹法(Western blot)对重要分子进行验证.
结论:高表达Trx1的幽门螺杆菌在致胃黏膜癌变过程中,三个重要的细胞应激和氧化还原活性蛋白包括14-3-3α/β、谷胱甘肽转移酶(GST)和热休克蛋白(HSP70)参与致病.

关键词:硫氧还蛋白-1(Trx1);幽门螺杆菌;胃黏膜癌变;蛋白质组学;同位素标记相对和绝对定量(iTRAQ)

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article

Reference

[1]Abadi ATB, Kusters JG, 2016. Management of Helicobacter pylori infections. BMC Gastroenterol, 16:94.

[2]Baek HY, Lim JW, Kim H, et al., 2004. Oxidative-stress-related proteome changes in Helicobacter pylori-infected human gastric mucosa. Biochem J, 379(Pt 2):291-299.

[3]Baker LMS, Raudonikiene A, Hoffman PS, et al., 2001. Essential thioredoxin-dependent peroxiredoxin system from Helicobacter pylori: genetic and kinetic characterization. J Bacteriol, 183(6):1961-1973.

[4]Bellini S, Barutta F, Mastrocola R, et al., 2017. Heat shock proteins in vascular diabetic complications: review and future perspective. Int J Mol Sci, 18(12):2709.

[5]Blaser MJ, Chyou PH, Nomura A, 1995. Age at establishment of Helicobacter pylori infection and gastric carcinoma, gastric ulcer, and duodenal ulcer risk. Cancer Res, 55(3):562-565.

[6]Carrasco V, Canfrán S, Rodriguez-Franco F, et al., 2011. Canine gastric carcinoma: immunohistochemical expression of cell cycle proteins (p53, p21, and p16) and heat shock proteins (Hsp27 and Hsp70). Vet Pathol, 48(1):322-329.

[7]Cesa LC, Shao H, Srinivasan SR, et al., 2017. X-linked inhibitor of apoptosis protein (XIAP) is a client of heat shock protein 70 (Hsp70) and a biomarker of its inhibition. J Biol Chem, 293(7):2370-2380.

[8]Comtois SL, Gidley MD, Kelly DJ, 2003. Role of the thioredoxin system and the thiol-peroxidases Tpx and Bcp in mediating resistance to oxidative and nitrosative stress in Helicobacter pylori. Microbiology, 149(Pt 1):121-129.

[9]Cybulsky AV, Guillemette J, Papillon J, 2016. Ste20-like kinase, SLK, activates the heat shock factor 1-Hsp70 pathway. Biochim Biophys Acta, 1863(9):2147-2155.

[10]Deng W, Yan M, Yu T, et al., 2015. Quantitative proteomic analysis of the metastasis-inhibitory mechanism of miR-193a-3p in non-small cell lung cancer. Cell Physiol Biochem, 35(5):1677-1688.

[11]Fock KM, Talley N, Moayyedi P, et al., 2008. Asia-pacific consensus guidelines on gastric cancer prevention. J Gastroenterol Hepatol, 23(3):351-365.

[12]García-González MA, Quintero E, Bujanda L, et al., 2012. Relevance of GSTM1, GSTT1, and GSTP1 gene polymorphisms to gastric cancer susceptibility and phenotype. Mutagenesis, 27(6):771-777.

[13]González CA, Figueiredo C, Lic CB, et al., 2011. Helicobacter pylori cagA and vacA genotypes as predictors of progression of gastric preneoplastic lesions: a long-term follow-up in a high-risk area in Spain. Am J Gastroenterol, 106(5):867-874.

[14]Hayes JD, Flanagan JU, Jowsey IR, 2005. Glutathione transferases. Annu Rev Pharmacol Toxicol, 45:51-88.

[15]Honda S, Fujioka T, Tokieda M, et al., 1998. Development of Helicobacter pylori-induced gastric carcinoma in Mongolian gerbils. Cancer Res, 58(19):4255-4259.

[16]Hsu CH, Hsu CW, Hsueh C, et al., 2016. Identification and characterization of potential biomarkers by quantitative tissue proteomics of primary lung adenocarcinoma. Mol Cell Proteomics, 15(7):2396-2410.

[17]Kanehisa M, Goto S, Sato Y, et al., 2012. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res, 40(D1):D109-D114.

[18]Kim HS, Kwack SJ, Lee BM, 2005. Alteration of cytochrome p-450 and glutathione S-transferase activity in normal and malignant human stomach. J Toxicol Environ Health, Part A, 68(19):1611-1620.

[19]Kuhns LG, Wang G, Maier RJ, 2015. Comparative roles of the two Helicobacter pylori thioredoxins in preventing macromolecule damage. Infect Immun, 83(7):2935-2943.

[20]Lim JW, Kim H, Kim JM, et al., 2004. Cellular stress-related protein expression in Helicobacter pylori-infected gastric epithelial AGS cells. Int J Biochem Cell Biol, 36(8):1624-1634.

[21]Liu LN, Ding SG, Shi YY, et al., 2016. Helicobacter pylori with high thioredoxin-1 expression promotes stomach carcinogenesis in Mongolian gerbils. Clin Res Hepatol Gastroenterol, 40(4):480-486.

[22]Long BS, Muhamad R, Yan GK, et al., 2016. Quantitative proteomics analysis reveals glutamine deprivation activates fatty acid β-oxidation pathway in HepG2 cells. Amino Acids, 48(5):1297-1307.

[23]Marshall BJ, Warren JR, 1984. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet, 323(8390):1311-1315.

[24]McGee DJ, Kumar S, Viator RJ, et al., 2006. Helicobacter pylori thioredoxin is an arginase chaperone and guardian against oxidative and nitrosative stresses. J Biol Chem, 281(6):3290-3296.

[25]Montecucco C, Rappuoli R, 2001. Living dangerously: how Helicobacter pylori survives in the human stomach. Nat Rev Mol Cell Biol, 2(6):457-466.

[26]Niforou K, Cheimonidou C, Trougakos IP, 2014. Molecular chaperones and proteostasis regulation during redox imbalance. Redox Biol, 2:323-332.

[27]Parsonnet J, Friedman GD, Vandersteen DP, et al., 1991. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med, 325(16):1127-1131.

[28]Shi YY, Liu LN, Zhang T, et al., 2013. The involvement of Helicobacter pylori thioredoxin-1 in gastric carcinogenesis. J Med Microbiol, 62(Pt 8):1226-1234.

[29]Shi YY, Chen M, Zhang YX, et al., 2014. Expression of three essential antioxidants of Helicobacter pylori in clinical isolates. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 15(5):500-506.

[30]Suerbaum S, Michetti P, 2002. Helicobacter pylori infection. N Engl J Med, 347(15):1175-1186.

[31]Suriani R, Venturini I, Taraglio S, et al., 2005. Type III intestinal metaplasia, Helicobacter pylori infection and gastric carcinoma risk index in an Italian series of 1750 patients. Hepatogastroenterology, 52(61):285-288.

[32]Targosz A, Brzozowski T, Pierzchalski P, et al., 2012. Helicobacter pylori promotes apoptosis, activates cyclooxygenase (COX)-2 and inhibits heat shock protein HSP70 in gastric cancer epithelial cells. Inflamm Res, 61(9):955-966.

[33]Townsend DM, Tew KD, 2003. The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene, 22(47):7369-7375.

[34]Tsukamoto T, Toyoda T, Mizoshita T, et al., 2013. Helicobacter pylori infection and gastric carcinogenesis in rodent models. Semin Immunopathol, 35(2):177-190.

[35]Uhart M, Bustos DM, 2014. Protein intrinsic disorder and network connectivity. The case of 14-3-3 proteins. Front Genet, 5:10.

[36]Wang G, Alamuri P, Maier RJ, 2006. The diverse antioxidant systems of Helicobacter pylori. Mol Microbiol, 61(4):847-860.

[37]Wang G, Romero-Gallo J, Benoit SL, et al., 2016. Hydrogen metabolism in Helicobacter pylori plays a role in gastric carcinogenesis through facilitating CagA translocation. mBio, 7(4):e01022-16.

[38]Watanabe T, Tada M, Nagai H, et al., 1998. Helicobacter pylori infection induces gastric cancer in Mongolian gerbils. Gastroenterology, 115(3):642-648.

[39]WHO, 1994. Schistosomes, Liver Flukes and Helicobacter Pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, IARC Scientific Publication No. 61, IARC, Lyon, France.

[40]Windle HJ, Fox Á, Nı́Eidhin D, et al., 2000. The thioredoxin system of Helicobacter pylori. J Biol Chem, 275(7):5081-5089.

[41]Wroblewski LE, Peek RM Jr, Wilson KT, 2010. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev, 23(4):713-739.

[42]Wu JM, Liu TE, Rios Z, et al., 2017. Heat shock proteins and cancer. Trends Pharmacol Sci, 38(3):226-256.

[43]Yang L, 2006. Incidence and mortality of gastric cancer in china. World J Gastroenterol, 12(1):17-20.

[44]Yeo M, Park HK, Kim DK, et al., 2004. Restoration of heat shock protein70 suppresses gastric mucosal inducible nitric oxide synthase expression induced by Helicobacter pylori. Proteomics, 4(11):3335-3342.

[45]Zhang J, Ding SG, Zhong LJ, et al., 2006. Difference analysis on proteome of Helicobacter pylori in patients with peptic ulcer, gastritis, and gastric cancer. Nat Med J China, 86(38):2690-2694 (in Chinese).

[46]Zhang YL, Liu HY, Zhou K, 2001. Lack of correlation of vacA genotype, cagA gene of Helicobacter pylori and their expression products with various gastroduodenal diseases. Chin Med J (Engl), 114(7):703-706.

[47]Zheng Q, Chen XY, Shi Y, et al., 2004. Development of gastric adenocarcinoma in Mongolian gerbils after long-term infection with Helicobacter pylori. J Gastroenterol Hepatol, 19(10):1192-1198.

[48]Zhou XY, Hu DX, Chen RQ, et al., 2017. 14-3-3 Isoforms differentially regulate NFκB signaling in the brain after ischemia-reperfusion. Neurochem Res, 42(8):2354-2362.

[49]List of electronic supplementary materials

[50]Table S1 Different expressed proteins for paired gastritis tissues infected by H. pylori expressing high or low Trx1

[51]Table S2 Different expressed proteins for paired dysplasia tissues infected by H. pylori expressing high or low Trx1

[52]Table S3 Different expressed proteins for paired gastric cancer tissues infected by H. pylori expressing high or low Trx1

[53]Table S4 Commonly and uniquely expressed 242 proteins in gastritis, dysplasia, and gastric cancer tissues infected by H. pylori expressing high or low Trx1

Open peer comments: Debate/Discuss/Question/Opinion

<1>

Please provide your name, email address and a comment





Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952783; E-mail: cjzhang@zju.edu.cn
Copyright © 2000 - Journal of Zhejiang University-SCIENCE