High Tiam1 expression predicts positive lymphatic metastasis and worse survival in patients with malignant solid tumors: a systematic review and meta-analysis

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68(1):7–30. doi:10.3322/caac.2144229313949
   PubMed Web of Science ®Google Scholar
• Kalia M. Biomarkers for personalized oncology: recent advances and future challenges. Metabolism. 2015;64(3 Suppl 1):S16–S21. doi:10.1016/j.metabol.2014.10.02725468140
   PubMed Web of Science ®Google Scholar
• Kulasingam V, Prassas I, Diamandis EP. Towards personalized tumor markers. NPJ Precis Oncol. 2017;1(1):17. doi:10.1038/s41698-017-0021-229872704
   PubMedGoogle Scholar
• Habets GG, Scholtes EH, Zuydgeest D, et al. Identification of an invasion-inducing gene, Tiam-1, that encodes a protein with homology to GDP-GTP exchangers for Rho-like proteins. Cell. 1994;77(4):537–549.7999144
   PubMed Web of Science ®Google Scholar
• Mertens AE, Roovers RC, Collard JG. Regulation of Tiam1-Rac signalling. FEBS Lett. 2003;546(1):11–16.12829230
   PubMed Web of Science ®Google Scholar
• Ding M, Li Y, Yang Y, et al. Elevated expression of Tiam1 is associated with poor prognosis and promotes tumor progression in pancreatic cancer. Onco Targets Ther. 2018;11:4367–4375. doi:10.2147/OTT.S17142530100742
   PubMed Web of Science ®Google Scholar
• Boissier P, Huynh-Do U. The guanine nucleotide exchange factor Tiam1: a Janus-faced molecule in cellular signaling. Cell Signal. 2014;26(3):483–491.24308970
   PubMed Web of Science ®Google Scholar
• Ding Y, Chen B, Huang J, et al. Overexpression of Tiam1 is associated with malignant phenotypes of nasopharyngeal carcinoma. Oncol Rep. 2014;32(2):607–618.24912585
   PubMed Web of Science ®Google Scholar
• Ding Y, Chen B, Wang S, et al. Overexpression of Tiam1 in hepatocellular carcinomas predicts poor prognosis of HCC patients. Int J Cancer. 2009;124(3):653–658.18972435
   PubMed Web of Science ®Google Scholar
• Du X, Wang S, Lu J, et al. Clinical value of Tiam1-Rac1 signaling in primary gallbladder carcinoma. Med Oncol. 2012;29(3):1873–1878. doi:10.1007/s12032-011-0046-221853342
   PubMed Web of Science ®Google Scholar
• Engers R, Mueller M, Walter A, Collard JG, Willers R, Gabbert HE. Prognostic relevance of Tiam1 protein expression in prostate carcinomas. Br J Cancer. 2006;95(8):1081–1086. doi:10.1038/sj.bjc.660338517003780
   PubMed Web of Science ®Google Scholar
• Hsueh C, Lin JD, Yang CF, et al. Prognostic significance of Tiam1 expression in papillary thyroid carcinoma. Virchows Arch. 2011;459(6):587–593. doi:10.1007/s00428-011-1164-022075848
   PubMed Web of Science ®Google Scholar
• Li H, Cui X, Chen D, et al. Clinical implication of Tiam1 overexpression in the prognosis of patients with serous ovarian carcinoma. Oncol Lett. 2016;12(5):3492–3498. doi:10.3892/ol.2016.509127900026
   PubMed Web of Science ®Google Scholar
• Li Z, Liu Q, Piao J, et al. Clinicopathological implications of Tiam1 overexpression in invasive ductal carcinoma of the breast. BMC Cancer. 2016;16(1):681. doi:10.1186/s12885-016-2724-027562113
   PubMedGoogle Scholar
• Liu H, Shi G, Liu X, Wu H, Fan Q, Wang X. Overexpression of Tiam1 predicts poor prognosis in patients with esophageal squamous cell carcinoma. Oncol Rep. 2011;25(3):841–848. doi:10.3892/or.2010.112221186404
   PubMed Web of Science ®Google Scholar
• Liu N, Tang LL, Sun Y, et al. MiR-29c suppresses invasion and metastasis by targeting TIAM1 in nasopharyngeal carcinoma. Cancer Lett. 2013;329(2):181–188. doi:10.1016/j.canlet.2012.10.03223142282
   PubMed Web of Science ®Google Scholar
• Liu S, Li Y, Qi W, et al. Expression of Tiam1 predicts lymph node metastasis and poor survival of lung adenocarcinoma patients. Diagn Pathol. 2014;9:69. doi:10.1186/1746-1596-9-6924661909
   PubMed Web of Science ®Google Scholar
• Walch A, Seidl S, Hermannstadter C, et al. Combined analysis of Rac1, IQGAP1, Tiam1 and E-cadherin expression in gastric cancer. Mod Pathol. 2008;21(5):544–552. doi:10.1038/modpathol.2008.318246045
   PubMed Web of Science ®Google Scholar
• Yang H, Cai YC, Cao Y, et al. The prognostic value of Tiam1 protein expression in head and neck squamous cell carcinoma: a retrospective study. Chin J Cancer. 2015;34(12):614–621. doi:10.1186/s40880-015-0053-326369827
   PubMedGoogle Scholar
• Yang Y, Wu Q, Li N, et al. Upregulation of Tiam1 contributes to cervical cancer disease progression and indicates poor survival outcome. Hum Pathol. 2018;75:179–188. doi:10.1016/j.humpath.2018.02.00629452216
   PubMed Web of Science ®Google Scholar
• Wang S, Li S, Yang X, et al. Elevated expression of T-lymphoma invasion and metastasis inducing factor 1 in squamous-cell carcinoma of the head and neck and its clinical significance. Eur J Cancer. 2014;50(2):379–387. doi:10.1016/j.ejca.2013.10.00324189000
   PubMed Web of Science ®Google Scholar
• Qi Y, Huang B, Yu L, Wang Q, Lan G, Zhang Q. Prognostic value of Tiam1 and Rac1 overexpression in nasopharyngeal carcinoma. ORL J Otorhinolaryngol Relat Spec. 2009;71(3):163–171. doi:10.1159/00022344019506399
   PubMedGoogle Scholar
• Zhao L, Liu Y, Sun X, He M, Ding Y. Overexpression of T lymphoma invasion and metastasis 1 predict renal cell carcinoma metastasis and overall patient survival. J Cancer Res Clin Oncol. 2011;137(3):393–398. doi:10.1007/s00432-010-0895-720429013
   PubMed Web of Science ®Google Scholar
• Hofbauer SW, Krenn PW, Ganghammer S, et al. Tiam1/Rac1 signals contribute to the proliferation and chemoresistance, but not motility, of chronic lymphocytic leukemia cells. Blood. 2014;123(14):2181–2188. doi:10.1182/blood-2013-08-52356324501217
   PubMed Web of Science ®Google Scholar
• Chen G, Lu L, Liu C, Shan L, Yuan D. MicroRNA-377 suppresses cell proliferation and invasion by inhibiting TIAM1 expression in hepatocellular carcinoma. PLoS One. 2015;10(3):e0117714. doi:10.1371/journal.pone.011771425739101
   PubMed Web of Science ®Google Scholar
• Liu Y, Wang X, Jiang X, et al. Tumor-suppressive microRNA-10a inhibits cell proliferation and metastasis by targeting Tiam1 in esophageal squamous cell carcinoma. J Cell Biochem. 2018. doi:10.1002/jcb.28059
   Web of Science ®Google Scholar
• Zhou H, Kann MG, Mallory EK, et al. Recruitment of Tiam1 to semaphorin 4D activates rac and enhances proliferation, invasion, and metastasis in oral squamous cell carcinoma. Neoplasia. 2017;19(2):65–74.28038319
   PubMed Web of Science ®Google Scholar
• Liao TT, Yang MH. Revisiting epithelial-mesenchymal transition in cancer metastasis: the connection between epithelial plasticity and stemness. Mol Oncol. 2017;11(7):792–804. doi:10.1002/1878-0261.1209628649800
   PubMed Web of Science ®Google Scholar
• Shi C, Chen Y, Chen Y, Yang Y, Bing W, Qi J. CD4(+) CD25(+) regulatory T cells promote hepatocellular carcinoma invasion via TGF-beta1-induced epithelial-mesenchymal transition. Onco Targets Ther. 2019;12:279–289. doi:10.2147/OTT.S17241730643426
   PubMed Web of Science ®Google Scholar
• Sun R, Lu X, Gong L, Jin F. TCTP promotes epithelial-mesenchymal transition in lung adenocarcinoma. Onco Targets Ther. 2019;12:1641–1653. doi:10.2147/OTT.S18455530881019
   PubMedGoogle Scholar
• Wang J, Li H, Xia C, et al. Downregulation of CENPK suppresses hepatocellular carcinoma malignant progression through regulating YAP1. Onco Targets Ther. 2019;12:869–882. doi:10.2147/OTT.S19006130774374
   PubMed Web of Science ®Google Scholar
• Zhu G, Zhang Y, Wang Q, et al. The prognostic value of Tiam1 correlates with its roles in epithelial-mesenchymal transition progression and angiogenesis in lung adenocarcinoma. Cancer Manag Res. 2019;11:1741–1752. doi:10.2147/CMAR.S19509330863182
   PubMed Web of Science ®Google Scholar
• Izumi D, Toden S, Ureta E, Ishimoto T, Baba H, Goel A. TIAM1 promotes chemoresistance and tumor invasiveness in colorectal cancer. Cell Death Dis. 2019;10(4):267. doi:10.1038/s41419-019-1300-330890693
   PubMedGoogle Scholar
• Choe C, Shin YS, Kim C, et al. Crosstalk with cancer-associated fibroblasts induces resistance of non-small cell lung cancer cells to epidermal growth factor receptor tyrosine kinase inhibition. Onco Targets Ther. 2015;8:3665–3678. doi:10.2147/OTT.S8965926676152
   PubMed Web of Science ®Google Scholar
• Hu G, Zhong K, Chen W, Wang S, Huang L. Podoplanin-positive cancer-associated fibroblasts predict poor prognosis in lung cancer patients. Onco Targets Ther. 2018;11:5607–5619. doi:10.2147/OTT.S17556630254454
   PubMed Web of Science ®Google Scholar
• Knobloch K, Yoon U, Vogt PM. Preferred reporting items for systematic reviews and meta-analyses (PRISMA) statement and publication bias. J Craniomaxillofac Surg. 2011;39(2):91–92. doi:10.1016/j.jcms.2010.11.00121145753
   PubMed Web of Science ®Google Scholar
• Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–605. doi:10.1007/s10654-010-9491-z20652370
   PubMed Web of Science ®Google Scholar
• Dai K, Quan J, Yan F, et al. lncRNAs as potential molecular biomarkers in the clinicopathology and prognosis of cholangiocarcinoma: a systematic review and meta-analysis. Onco Targets Ther. 2019;12:1905–1915. doi:10.2147/OTT.S18813430881042
   PubMed Web of Science ®Google Scholar
• Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–1101.7786990
   PubMed Web of Science ®Google Scholar
• Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–634. doi:10.1136/bmj.315.7109.6299310563
   PubMed Web of Science ®Google Scholar
• Gao XL, Zhang M, Tang YL, Liang XH. Cancer cell dormancy: mechanisms and implications of cancer recurrence and metastasis. Onco Targets Ther. 2017;10:5219–5228. doi:10.2147/OTT.S14085429138574
   PubMed Web of Science ®Google Scholar
• Wei C, Wang Y, Li X. The role of Hippo signal pathway in breast cancer metastasis. Onco Targets Ther. 2018;11:2185–2193. doi:10.2147/OTT.S15705829713187
   PubMed Web of Science ®Google Scholar
• Xue JY, Huang C, Wang W, Li HB, Sun M, Xie M. HOXA11-AS: a novel regulator in human cancer proliferation and metastasis. Onco Targets Ther. 2018;11:4387–4393. doi:10.2147/OTT.S16696130100744
   PubMed Web of Science ®Google Scholar
• Jin J, Cai L, Liu ZM, Zhou XS. miRNA-218 inhibits osteosarcoma cell migration and invasion by down-regulating of TIAM1, MMP2 and MMP9. Asian Pac J Cancer Prev. 2013;14(6):3681–3684.23886165
   PubMedGoogle Scholar
• Subramanian N, Navaneethakrishnan S, Biswas J, Kanwar RK, Kanwar JR, Krishnakumar S. RNAi mediated Tiam1 gene knockdown inhibits invasion of retinoblastoma. PLoS One. 2013;8(8):e70422. doi:10.1371/journal.pone.007042223950931
   PubMed Web of Science ®Google Scholar
• Li Z, Yu X, Wang Y, et al. By downregulating TIAM1 expression, microRNA-329 suppresses gastric cancer invasion and growth. Oncotarget. 2015;6(19):17559–17569. doi:10.18632/oncotarget.275525654811
   PubMedGoogle Scholar
• Poudel KR, Roh-Johnson M, Su A, et al. Competition between TIAM1 and membranes balances endophilin A3 activity in cancer metastasis. Dev Cell. 2018;45(6):738–752 e736. doi:10.1016/j.devcel.2018.05.02129920278
   PubMed Web of Science ®Google Scholar
• Zhu G, Fan Z, Ding M, et al. An EGFR/PI3K/AKT axis promotes accumulation of the Rac1-GEF Tiam1 that is critical in EGFR-driven tumorigenesis. Oncogene. 2015;34(49):5971–5982. doi:10.1038/onc.2015.4525746002
   PubMed Web of Science ®Google Scholar
• Wang B, Li W, Liu H, et al. miR-29b suppresses tumor growth and metastasis in colorectal cancer via downregulating Tiam1 expression and inhibiting epithelial-mesenchymal transition. Cell Death Dis. 2014;5:e1335. doi:10.1038/cddis.2014.30425032858
   PubMed Web of Science ®Google Scholar
• Minard ME, Ellis LM, Gallick GE. Tiam1 regulates cell adhesion, migration and apoptosis in colon tumor cells. Clin Exp Metastasis. 2006;23(5–6):301–313. doi:10.1007/s10585-006-9040-z17086355
   PubMed Web of Science ®Google Scholar
• Minard ME, Herynk MH, Collard JG, Gallick GE. The guanine nucleotide exchange factor Tiam1 increases colon carcinoma growth at metastatic sites in an orthotopic nude mouse model. Oncogene. 2005;24(15):2568–2573. doi:10.1038/sj.onc.120850315735692
   PubMed Web of Science ®Google Scholar
• Liu Y, Ding Y, Huang J, et al. MiR-141 suppresses the migration and invasion of HCC cells by targeting Tiam1. PLoS One. 2014;9(2):e88393. doi:10.1371/journal.pone.008839324551096
   PubMed Web of Science ®Google Scholar
• Minard ME, Kim LS, Price JE, Gallick GE. The role of the guanine nucleotide exchange factor Tiam1 in cellular migration, invasion, adhesion and tumor progression. Breast Cancer Res Treat. 2004;84(1):21–32. doi:10.1023/B:BREA.0000018421.31632.e614999151
   PubMed Web of Science ®Google Scholar
• Cheng W, Liu Y, Zuo Z, et al. Biological effects of RNAi targeted inhibiting Tiam1 gene expression on cholangiocarcinoma cells. Int J Clin Exp Pathol. 2015;8(12):15511–15526.26884821
   PubMed Web of Science ®Google Scholar
• Li J, Liang S, Jin H, Xu C, Ma D, Lu X. Tiam1, negatively regulated by miR-22, miR-183 and miR-31, is involved in migration, invasion and viability of ovarian cancer cells. Oncol Rep. 2012;27(6):1835–1842. doi:10.3892/or.2012.174422469921
   PubMed Web of Science ®Google Scholar
• Wang S, Li S, Tang Q, et al. Overexpression of Tiam1 promotes the progression of laryngeal squamous cell carcinoma. Oncol Rep. 2015;33(4):1807–1814. doi:10.3892/or.2015.378525672412
   PubMed Web of Science ®Google Scholar
• Liu L, Wu B, Cai H, et al. Tiam1 promotes thyroid carcinoma metastasis by modulating EMT via Wnt/beta-catenin signaling. Exp Cell Res. 2018;362(2):532–540. doi:10.1016/j.yexcr.2017.12.01929277502
   PubMed Web of Science ®Google Scholar
• Guo X, Wang M, Jiang J, et al. Balanced Tiam1-rac1 and RhoA drives proliferation and invasion of pancreatic cancer cells. Mol Cancer Res. 2013;11(3):230–239. doi:10.1158/1541-7786.MCR-12-063223322732
   PubMed Web of Science ®Google Scholar
• Cruz-Monserrate Z, O’Connor KL. Integrin alpha 6 beta 4 promotes migration, invasion through Tiam1 upregulation, and subsequent Rac activation. Neoplasia. 2008;10(5):408–417.18472958
   PubMed Web of Science ®Google Scholar
• Malliri A, Rygiel TP, van der Kammen RA, et al. The rac activator Tiam1 is a Wnt-responsive gene that modifies intestinal tumor development. J Biol Chem. 2006;281(1):543–548. doi:10.1074/jbc.M50758220016249175
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100(1):57–70.10647931
   PubMed Web of Science ®Google Scholar
• Bai ZG, Zhang ZT. A systematic review and meta-analysis on the effect of angiogenesis blockade for the treatment of gastric cancer. Onco Targets Ther. 2018;11:7077–7087. doi:10.2147/OTT.S16948430410364
   PubMed Web of Science ®Google Scholar
• Peng T, Li Z, Li D, Wang S. MACC1 promotes angiogenesis in cholangiocarcinoma by upregulating VEGFA. Onco Targets Ther. 2019;12:1893–1903. doi:10.2147/OTT.S19731930881041
   PubMed Web of Science ®Google Scholar
• Guerra L, Odorisio T, Zambruno G, Castiglia D. Stromal microenvironment in type VII collagen-deficient skin: the ground for squamous cell carcinoma development. Matrix Biol. 2017;63:1–10. doi:10.1016/j.matbio.2017.01.00228126522
   PubMed Web of Science ®Google Scholar
• Vail ME, Murone C, Tan A, et al. Targeting EphA3 inhibits cancer growth by disrupting the tumor stromal microenvironment. Cancer Res. 2014;74(16):4470–4481. doi:10.1158/0008-5472.CAN-14-021825125683
   PubMed Web of Science ®Google Scholar
• Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med. 2013;19(11):1423–1437.24202395
   PubMed Web of Science ®Google Scholar
• Achyut BR, Arbab AS. Myeloid cell signatures in tumor microenvironment predicts therapeutic response in cancer. Onco Targets Ther. 2016;9:1047–1055.27042097
   PubMed Web of Science ®Google Scholar
• Wang L, Yang X, Li D, et al. The elevated glutaminolysis of bladder cancer and T cells in a simulated tumor microenvironment contributes to the up-regulation of PD-L1 expression by interferon-gamma. Onco Targets Ther. 2018;11:7229–7243.30425515
   PubMed Web of Science ®Google Scholar
• Xu K, Rajagopal S, Klebba I, et al. The role of fibroblast Tiam1 in tumor cell invasion and metastasis. Oncogene. 2010;29(50):6533–6542.20802514
   PubMed Web of Science ®Google Scholar
• Xu K, Tian X, Oh SY, et al. The fibroblast Tiam1-osteopontin pathway modulates breast cancer invasion and metastasis. Breast Cancer Res. 2016;18(1):14.26821678
   PubMedGoogle Scholar