Helicobacter pylori-Induced Progranulin Promotes the Progression of the Gastric Epithelial Cell Cycle by Regulating CDK4 |
Ren, Zongjiao
(Department of Pathogenic Microbiology, Basic Medical College, Weifang Medical University)
Li, Jiayi (Department of Pathogenic Microbiology, Basic Medical College, Weifang Medical University) Du, Xianhong (Department of Pathogenic Microbiology, Basic Medical College, Weifang Medical University) Shi, Wenjing (Department of Gynecology, Weifang Medical University Affiliated Hospital) Guan, Fulai (Laboratory of Morphology, Weifang Medical University) Wang, Xiaochen (Department of Pathogenic Microbiology, Basic Medical College, Weifang Medical University) Wang, Linjing (Clinical Medical College, Weifang Medical University) Wang, Hongyan (Department of Pathogenic Microbiology, Basic Medical College, Weifang Medical University) |
1 | Tadesse S, Caldon EC, Tilley W, Wang S. 2019. Cyclin-eependent kinase 2 inhibitors in cancer therapy: An update. J. Med. Chem. 62: 4233-4251. DOI |
2 | Sherr CJ. 1996. Cancer cell cycles. Science 274: 1672-1677. DOI |
3 | Evan GI, Vousden KH. 2001. Proliferation, cell cycle and apoptosis in cancer. Nature 411: 342-348. DOI |
4 | Kar S. 2016. Unraveling cell-cycle dynamics in cancer. Cell Syst. 2: 8-10. DOI |
5 | Campbell GJ, Hands EL, Van de Pette M. 2020. The role of CDKs and CDKIs in murine development. Int. J. Mol. Sci. 21: 5343. |
6 | Canepa ET, Scassa ME, Ceruti JM, Marazita MC, Carcagno AL, Sirkin PF, et al. 2007. INK4 proteins, a family of mammalian CDK inhibitors with novel biological functions. IUBMB Life 59: 419-426. DOI |
7 | Ahmed A, Smoot D, Littleton G, Tackey R, Walters CS, Kashanchi F, et al. 2000. Helicobacter pylori inhibits gastric cell cycle progression. Microbes Infect. 2: 1159-1169. DOI |
8 | Li N, Xie C, Lu NH. 2016. p53, a potential predictor of Helicobacter pylori infection-associated gastric carcinogenesis? Oncotarget 7: 66276-66286. DOI |
9 | Shirin H, Sordillo EM, Oh SH, Yamamoto H, Delohery T, Weinstein IB, et al. 1999. Helicobacter pylori inhibits the G1 to S transition in AGS gastric epithelial cells. Cancer Res. 59: 2277-2281. |
10 | Scotti C, Sommi P, Pasquetto MV, Cappelletti D, Stivala S, Mignosi P, et al. 2010. Cell-cycle inhibition by Helicobacter pylori Lasparaginase. PLoS One 5: e13892. |
11 | Alquezar C, Esteras N, de la Encarnacion A, Alzualde A, Moreno F, Lopez de Munain A, et al. 2014. PGRN haploinsufficiency increased Wnt5a signaling in peripheral cells from frontotemporal lobar degeneration-progranulin mutation carriers. Neurobiol. Aging 35: 886-898. DOI |
12 | Kim KM, Lee SG, Kim JM, Kim DS, Song JY, Kang HL, et al. 2010. Helicobacter pylori gamma-glutamyltranspeptidase induces cell cycle arrest at the G1-S phase transition. J. Microbiol. 48: 372-377. DOI |
13 | Li H, Liang D, Hu N, Dai X, He J, Zhuang H, et al. 2019. Helicobacter pylori inhibited cell proliferation in human periodontal ligament fibroblasts through the Cdc25C/CDK1/cyclinB1 signaling cascade. J. Periodontal. Implant Sci. 49: 138-147. DOI |
14 | Dong T, Yang D, Li R, Zhang L, Zhao H, Shen Y, et al. 2016. PGRN promotes migration and invasion of epithelial ovarian cancer cells through an epithelial mesenchymal transition program and the activation of cancer associated fibroblasts. Exp. Mol. Pathol. 100: 17-25. DOI |
15 | Lu R, Serrero G. 2000. Inhibition of PC cell-derived growth factor (PCDGF, epithelin/granulin precursor) expression by antisense PCDGF cDNA transfection inhibits tumorigenicity of the human breast carcinoma cell line MDA-MB-468. Proc. Natl. Acad. Sci. USA 97: 3993-3998. DOI |
16 | Ho JC, Ip YC, Cheung ST, Lee YT, Chan KF, Wong SY, et al. 2008. Granulin-epithelin precursor as a therapeutic target for hepatocellular carcinoma. Hepatology 47: 1524-1532. DOI |
17 | Wu JY, Lee YC, Graham DY. 2019. The eradication of Helicobacter pylori to prevent gastric cancer: a critical appraisal. Expert Rev. Gastroenterol. Hepatol. 13: 17-24. DOI |
18 | Molaei F, Forghanifard MM, Fahim Y, Abbaszadegan MR. 2018. Molecular signaling in tumorigenesis of gastric cancer. Iran Biomed. J. 22: 217-230. DOI |
19 | Woodward TA, Klingler PD, Genko PV, Wolfe JT. 2000. Barrett's esophagus, apoptosis and cell cycle regulation: correlation of p53 with Bax, Bcl-2 and p21 protein expression. Anticancer Res. 20: 2427-2432. |
20 | Padda J, Khalid K, Cooper AC, Jean-Charles G. 2021. Association between Helicobacter pylori and gastric carcinoma. Cureus 13: e15165. |
21 | Chinzei N, Hayashi S, Ueha T, Fujishiro T, Kanzaki N, Hashimoto S, et al. 2015. P21 deficiency delays regeneration of skeletal muscular tissue. PLoS One 10: e0125765. |
22 | Wang W, Hayashi J, Kim WE, Serrero G. 2003. PC cell-derived growth factor (granulin precursor) expression and action in human multiple myeloma. Clin. Cancer Res. 9: 2221-2228. |
23 | Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. 2021. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 71: 209-249. DOI |
24 | Karimi P, Islami F, Anandasabapathy S, Freedman ND, Kamangar F. 2014. Gastric cancer: descriptive epidemiology, risk factors, screening, and prevention. Cancer Epidemiol. Biomarkers Prev. 23: 700-713. DOI |
25 | Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7-14 June 1994. IARC Monogr. Eval. Carcinog. Risks Hum. 61: 1-241. |
26 | Gonzalez CA, Megraud F, Buissonniere A, Lujan Barroso L, Agudo A, Duell EJ, et al. 2012. Helicobacter pylori infection assessed by ELISA and by immunoblot and noncardia gastric cancer risk in a prospective study: the Eurgast-EPIC project. Ann. Oncol. 23: 1320-1324. DOI |
27 | Cho J, Prashar A, Jones NL, Moss SF. 2021. Helicobacter pylori infection. Gastroenterol. Clin. North Am. 50: 261-282. DOI |
28 | Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408. DOI |
29 | Sherr CJ. 1995. D-type cyclins. Trends Biochem. Sci. 20: 187-190. DOI |
30 | Jackson RJ, Adnane J, Coppola D, Cantor A, Sebti SM, Pledger WJ. 2002. Loss of the cell cycle inhibitors p21(Cip1) and p27(Kip1) enhances tumorigenesis in knockout mouse models. Oncogene 21: 8486-8497. DOI |
31 | Jian J, Li G, Hettinghouse A, Liu C. 2018. Progranulin: A key player in autoimmune diseases. Cytokine 101: 48-55. DOI |
32 | Klupp F, Kahlert C, Franz C, Halama N, Schleussner N, Wirsik NM, et al. 2021. Granulin: an invasive and survival-determining marker in colorectal cancer patients. Int. J. Mol. Sci. 22: 6436. |
33 | Serrero G, Hawkins DM, Yue B, Ioffe O, Bejarano P, Phillips JT, et al. 2012. Progranulin (GP88) tumor tissue expression is associated with increased risk of recurrence in breast cancer patients diagnosed with estrogen receptor positive invasive ductal carcinoma. Breast Cancer Res. 14: R26. |
34 | Kastan MB, Bartek J. 2004. Cell-cycle checkpoints and cancer. Nature 432: 316-323. DOI |
35 | Wang F, Meng W, Wang B, Qiao L. 2014. Helicobacter pylori-induced gastric inflammation and gastric cancer. Cancer Lett. 345: 196-202. DOI |
36 | Enders GH. 2012. Mammalian interphase cdks: dispensable master regulators of the cell cycle. Genes Cancer 3: 614-618. DOI |
37 | Gao X, Leone GW, Wang H. 2020. Cyclin D-CDK4/6 functions in cancer. Adv. Cancer Res. 148: 147-169. DOI |
38 | Ford HL, Pardee AB. 1999. Cancer and the cell cycle. J. Cell Biochem. Suppl 32-33: 166-172. DOI |
39 | Yang D, Wang LL, Dong TT, Shen YH, Guo XS, Liu CY, et al. 2015. Progranulin promotes colorectal cancer proliferation and angiogenesis through TNFR2/Akt and ERK signaling pathways. Am. J. Cancer Res. 5: 3085-3097. |
40 | Yabe K, Yamamoto Y, Takemura M, Hara T, Tsurumi H, Serrero G, et al. 2021. Progranulin depletion inhibits proliferation via the transforming growth factor beta/SMAD family member 2 signaling axis in Kasumi-1 cells. Heliyon 7: e05849. |
41 | Fang W, Zhou T, Shi H, Yao M, Zhang D, Qian H, et al. 2021. Progranulin induces immune escape in breast cancer via up-regulating PD-L1 expression on tumor-associated macrophages (TAMs) and promoting CD8(+ ) T cell exclusion. J. Exp. Clin. Cancer Res. 40: 4. |
42 | Liu B, Li X, Sun F, Tong X, Bai Y, Jin K, et al. 2019. HP-CagA+ regulates the expression of CDK4/CyclinD1 via reg3 to change cell cycle and promote cell proliferation. Int. J. Mol. Sci. 21: 224. |
43 | Pack LR, Daigh LH, Meyer T. 2019. Putting the brakes on the cell cycle: mechanisms of cellular growth arrest. Curr. Opin. Cell Biol. 60: 106-113. DOI |
44 | Zhou Z, Ye G, Peng J, He B, Xu S, Fan W, et al. 2021. Expression of Wnt3, beta-catenin and MMP-7 in gastric cancer and precancerous lesions and their correlations with Helicobacter pylori infection. Zhong Nan Da Xue Xue Bao Yi Xue Ban 46: 575-582. |
45 | Kato MV, Sato H, Anzai H, Nagayoshi M, Ikawa Y. 1997. Up-regulation of cell cycle-associated genes by p53 in apoptosis of an erythroleukemic cell line. Leukemia 11 Suppl 3: 389-392. |
46 | Megraud F, Bessede E, Varon C. 2015. Helicobacter pylori infection and gastric carcinoma. Clin. Microbiol. Infect. 21: 984-990. DOI |
47 | Demorrow S. 2013. Progranulin: a novel regulator of gastrointestinal cancer progression. Transl. Gastrointest. Cancer 2: 145-151. |
48 | Wang H, Sun Y, Liu S, Yu H, Li W, Zeng J, et al. 2011. Upregulation of progranulin by Helicobacter pylori in human gastric epithelial cells via p38MAPK and MEK1/2 signaling pathway: role in epithelial cell proliferation and migration. FEMS Immunol. Med. Microbiol. 63: 82-92. DOI |
49 | Tang W, Lu Y, Tian QY, Zhang Y, Guo FJ, Liu GY, et al. 2011. The growth factor progranulin binds to TNF receptors and is therapeutic against inflammatory arthritis in mice. Science 332: 478-484. DOI |
50 | Arechavaleta-Velasco F, Perez-Juarez CE, Gerton GL, Diaz-Cueto L. 2017. Progranulin and its biological effects in cancer. Med. Oncol. 34: 194. |
51 | Guha R, Yue B, Dong J, Banerjee A, Serrero G. 2021. Anti-progranulin/GP88 antibody AG01 inhibits triple negative breast cancer cell proliferation and migration. Breast Cancer Res. Treat. 186: 637-653. DOI |
52 | Walsh CE, Hitchcock PF. 2017. Progranulin regulates neurogenesis in the developing vertebrate retina. Dev. Neurobiol. 77: 1114-1129. DOI |
53 | He Z, Ong CH, Halper J, Bateman A. 2003. Progranulin is a mediator of the wound response. Nat. Med. 9: 225-229. DOI |
54 | Xu B, Chen X, Ding Y, Chen C, Liu T, Zhang H. 2020. Abnormal angiogenesis of placenta in progranulindeficient mice. Mol. Med. Rep. 22: 3482-3492. |
55 | Lu J, Huang J, Shan M, Hu X, Guo W, Xie W, et al. 2021. Progranulin ameliorates lung inflammation in an LPS-induced acute lung injury mouse model by modulating macrophage polarization and the MAPK pathway. Ann. Clin. Lab. Sci. 51: 220-230. |
56 | Feng JQ, Guo FJ, Jiang BC, Zhang Y, Frenkel S, Wang DW, et al. 2010. Granulin epithelin precursor: a bone morphogenic protein 2- inducible growth factor that activates Erk1/2 signaling and JunB transcription factor in chondrogenesis. FASEB J. 24: 1879-1892. DOI |
57 | Abdulrahman A, Eckstein M, Jung R, Guzman J, Weigelt K, Serrero G, et al. 2019. Expression of GP88 (Progranulin) protein is an independent prognostic factor in prostate cancer patients. Cancers (Basel). 11: 2029. |
58 | Kimura A, Takemura M, Serrero G, Yoshikura N, Hayashi Y, Saito K, et al. 2018. Higher levels of progranulin in cerebrospinal fluid of patients with lymphoma and carcinoma with CNS metastasis. J. Neurooncol. 137: 455-462. DOI |
59 | Alquezar C, Esteras N, Bartolome F, Merino JJ, Alzualde A, Lopez de Munain A, et al. 2012. Alteration in cell cycle-related proteins in lymphoblasts from carriers of the c.709-1G>A PGRN mutation associated with FTLD-TDP dementia. Neurobiol. Aging 33: 429.e427-420. |
60 | Cover TL, Krishna US, Israel DA, Peek RM, Jr. 2003. Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin. Cancer Res. 63: 951-957. |
61 | Kollmann K, Briand C, Bellutti F, Schicher N, Blunder S, Zojer M, et al. 2019. The interplay of CDK4 and CDK6 in melanoma. Oncotarget 10: 1346-1359. DOI |
62 | Lu Y, Zheng L, Zhang W, Feng T, Liu J, Wang X, et al. 2014. Growth factor progranulin contributes to cervical cancer cell proliferation and transformation in vivo and in vitro. Gynecol. Oncol. 134: 364-371. DOI |
63 | Feng T, Zheng L, Liu F, Xu X, Mao S, Wang X, et al. 2016. Growth factor progranulin promotes tumorigenesis of cervical cancer via PI3K/Akt/mTOR signaling pathway. Oncotarget 7: 58381-58395. DOI |
64 | Fong LY, Nguyen VT, Farber JL, Huebner K, Magee PN. 2000. Early deregulation of the the p16ink4a-cyclin D1/cyclin-dependent kinase 4-retinoblastoma pathway in cell proliferation-driven esophageal tumorigenesis in zinc-deficient rats. Cancer Res. 60: 4589-4595. |
65 | Teo ZL, Versaci S, Dushyanthen S, Caramia F, Savas P, Mintoff CP, et al. 2017. Combined CDK4/6 and PI3Kalpha inhibition is synergistic and immunogenic in triple-negative breast cancer. Cancer Res. 77: 6340-6352. DOI |
66 | Buraschi S, Neill T, Xu SQ, Palladino C, Belfiore A, Iozzo RV, et al. 2020. Progranulin/EphA2 axis: A novel oncogenic mechanism in bladder cancer. Matrix Biol. 93: 10-24. DOI |
67 | Zhou C, Huang Y, Wu J, Wei Y, Chen X, Lin Z, et al. 2021. A narrative review of multiple mechanisms of progranulin in cancer: a potential target for anti-cancer therapy. Transl. Cancer Res. 10: 4207-4216. DOI |
68 | Zhao J, Li X, Liu J, Jiang W, Wen D, Xue H. 2018. Effect of progranulin on migration and invasion of human colon cancer cells. J. Coll. Physicians Surg. Pak. 28: 607-611. DOI |
69 | Wei J, Zhang L, Ding Y, Liu R, Guo Y, Hettinghouse A, et al. 2020. Progranulin promotes diabetic fracture healing in mice with type 1 diabetes. Ann. NY Acad. Sci. 1460: 43-56. DOI |
70 | Li H, Zhang Z, Feng D, Xu L, Li F, Liu J, et al. 2020. PGRN exerts inflammatory effects via SIRT1-NF-kappaB in adipose insulin resistance. J. Mol. Endocrinol. 64: 181-193. DOI |
71 | Hochegger H, Takeda S, Hunt T. 2008. Cyclin-dependent kinases and cell-cycle transitions: does one fit all? Nat. Rev. Mol. Cell Biol. 9: 910-916. DOI |
72 | Peek RM, Jr., Wirth HP, Moss SF, Yang M, Abdalla AM, Tham KT, et al. 2000. Helicobacter pylori alters gastric epithelial cell cycle events and gastrin secretion in Mongolian gerbils. Gastroenterology 118: 48-59. DOI |
73 | He Z, Ismail A, Kriazhev L, Sadvakassova G, Bateman A. 2002. Progranulin (PC-cell-derived growth factor/acrogranin) regulates invasion and cell survival. Cancer Res. 62: 5590-5596. |
74 | Ford AC, Yuan Y, Moayyedi P. 2020. Helicobacter pylori eradication therapy to prevent gastric cancer: systematic review and metaanalysis. Gut 69: 2113-2121. DOI |
75 | Song Z, Wu Y, Yang J, Yang D, Fang X. 2017. Progress in the treatment of advanced gastric cancer. Tumour Biol. 39: 1010428317714626. |
76 | Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, et al. 2017. Global prevalence of Helicobacter pylori infection: Systematic review and meta-analysis. Gastroenterology 153: 420-429. DOI |