Krüppel-like factor 4 mediates cellular migration and invasion by altering RhoA activity

References

• Boguski MS, McCormick F. 1993. Proteins regulating ras and its relatives. Nature. 366:643–654.
   PubMed Web of Science ®Google Scholar
• Chen X, Johns DC, Geiman DE, Marban E, Dang DT, Hamlin G, Sun R, Yang VW. 2001. Krüppel-like Factor 4 (Gut-enriched Krüppel-like Factor) inhibits cell proliferation by blocking G1/S progression of the cell cycle. J Biol Chem. 276:30423–30428.
   PubMed Web of Science ®Google Scholar
• Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, et al. 2008. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell. 133:1106–1117.
   PubMed Web of Science ®Google Scholar
• Chen X, Corbin JM, Tipton GJ, Yang LV, Asch AS, Ruiz-Echevarria MJ. 2014. The TMEFF2 tumor suppressor modulates integrin expression, RhoA activation and migration of prostate cancer cells. Biochim Biophys Acta Res. 1843:1216–1224.
   PubMed Web of Science ®Google Scholar
• Dang DT, Mahatan CS, Dang LH, Agboola IA, Yang VW. 2001. Expression of the gut-enriched Krüppel-like factor (Krüppel-like factor 4) gene in the human colon cancer cell line RKO is dependent on CDX2. Oncogene. 20:4884–4890.
   PubMed Web of Science ®Google Scholar
• Dang DT, Chen X, Feng J, Torbenson M, Dang LH, Yang VW. 2003. Overexpression of Krüppel-like factor 4 in the human colon cancer cell line RKO leads to reduced tumorigenicity. Oncogene. 22:3424–3430.
   PubMed Web of Science ®Google Scholar
• El-Karim EA, Hagos EG, Ghaleb AM, Yu B, Yang VW. 2013. Krüppel-like factor 4 regulates genetic stability in mouse embryonic fibroblasts. Mol Cancer. 12:89.
   PubMed Web of Science ®Google Scholar
• Garrett-Sinha LA, Eberspaecher H, Seldin MF, de Crombrugghe B. 1996. A gene for a novel zinc-finger protein expressed in differentiated epithelial cells and transiently in certain mesenchymal cells. J Biol Chem. 271:31384–31390.
   PubMed Web of Science ®Google Scholar
• Goulimari P, Kitzing TM, Knieling H, Brandt DT, Offermanns S, Grosse R. 2005. Galpha12/13 is essential for directed cell migration and localized Rho-Dia1 function. J Biol Chem. 280:42242–42251.
   PubMed Web of Science ®Google Scholar
• Hagos EG, Ghaleb AM, Dalton WB, Bialkowska AB, Yang VW. 2009. Mouse embryonic fibroblasts null for the Krüppel-like factor 4 gene are genetically unstable. Oncogene. 28:1197–1205.
   PubMed Web of Science ®Google Scholar
• Hagos EG, Ghaleb AM, Kumar A, Neish AS, Yang VW. 2011. Expression profiling and pathway analysis of Krüppel-like factor 4 in mouse embryonic fibroblasts. Am J Cancer Res. 1:85–97.
   PubMed Web of Science ®Google Scholar
• Huang CC, Liu Z, Li X, Bailey SK, Nail CD, Foster KW, Frost AR, Ruppert JM, Lobo-Ruppert SM. 2005. KLF4 and PCNA identify stages of tumor initiation in a conditional model of cutaneous squamous epithelial neoplasia. Cancer Bio Ther. 4:1401–1408.
   PubMed Web of Science ®Google Scholar
• Katz JP, Perreault N, Goldstein BG, Lee CS, Labosky PA, Yang VW, Kaestner KH. 2002. The zinc-finger transcription factor Klf4 is required for terminal differentiation of goblet cells in the colon. Development. 129:2619–2628.
   PubMed Web of Science ®Google Scholar
• Lehtimaki J, Hakala M, Lappalainen P. 2017. Actin filament structures in migrating cells. Handb Exp Pharmacol. 235:123–152.
   PubMedGoogle Scholar
• Lei R, Tang J, Zhuang X, Deng R, Li G, Yu J, Liang Y, Xiao J, Wang HY, Yang Q, Hu G. 2014. Suppression of MIM by microRNA 182 activates RhoA and promotes breast cancer metastasis. Oncogene. 33:1287–1296.
   PubMed Web of Science ®Google Scholar
• Li J, Zheng H, Yu F, Yu T, Liu C, Huang S, Wang TC, Ai W. 2012. Deficiency of the Kruppel-like factor KLF4 correlates with increased cell proliferation and enhanced skin tumorigenesis. Carcinogenesis. 33:1239–1246.
   PubMed Web of Science ®Google Scholar
• Liu C, La Rosa S, Hagos EG. 2014. Oxidative DNA damage causes premature senescence in mouse embryonic fibroblasts deficient for Krüppel-like factor 4. Mol Carcinog. 54:889–899.
   PubMed Web of Science ®Google Scholar
• Liu C, Deroo EP, Stecyk C, Wolsey M, Szuchnicki M, Hagos EG. 2015. Impaired autophagy in mouse embryonic fibroblasts null for Krüppel-like Factor 4 promotes DNA damage and increases apoptosis upon serum starvation. Mol Cancer 14:101.
   PubMed Web of Science ®Google Scholar
• Liu L, Wang Y, Yu Q. 2014. The PI3K/Akt signaling pathway exerts effects on the implantation of mouse embryos by regulating the expression of RhoA. Int J Mol Med. 33:1089–1096.
   PubMed Web of Science ®Google Scholar
• Lv H, Zhang Z, Wang Y, Li C, Gong W, Wang X. 2016. MicroRNA-92a promotes colorectal cancer cell growth and migration by inhibiting KLF4. Oncol Res. 23:283–290.
   PubMed Web of Science ®Google Scholar
• O’Connor K, Chen M. 2013. Dynamic functions of RhoA in tumor cell migration and invasion. Small GTPases. 4:141–147.
   PubMedGoogle Scholar
• Ohnishi S, Ohnami S, Laub F, Aoki K, Suzuki K, Kanai Y, Haga K, Asaka M, Ramirez F, Yoshida T. 2003. Downregulation and growth inhibitory effect of epithelial-type Krüppel-like transcription factor KLF4, but not KLF5, in bladder cancer. Biochem Biophys Res Commun. 308:251–256.
   PubMed Web of Science ®Google Scholar
• Orellana R, Kato S, Erices R, Bravo ML, Gonzalez P, Oliva B, Valdivia A, Ibañez A, Brañes J, Barriga MI, et al. 2015. Platelets enhance tissue factor protein and metastasis initiating cell markers, and act as chemoattractants increasing the migration of ovarian cancer cells. BMC Cancer. 15:290.
   PubMed Web of Science ®Google Scholar
• Pandya AY, Talley LI, Frost AR, Fitzgerald TJ, Trivedi V, Chakravarthy M, Chhieng DC, Grizzle WE, Engler JA, Krontiras H, et al. 2004. Nuclear localization of KLF4 is associated with an aggressive phenotype in early-stage breast cancer. Clin Cancer Res. 10:2709–2719.
   PubMed Web of Science ®Google Scholar
• Pollard TD, Borisy GG. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell. 112:453–465.
   PubMed Web of Science ®Google Scholar
• Raftopoulou M, Hall A. 2004. Cell migration: Rho GTPases lead the way. Dev Bio. 265:23–32.
   PubMed Web of Science ®Google Scholar
• Ren X, Kiosses WB, Schwarz MA. 1999. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18:578–585.
   PubMed Web of Science ®Google Scholar
• Ridley AJ, Hall A. 1992. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 70:389–399.
   PubMed Web of Science ®Google Scholar
• Ridley AJ. 2013. RhoA, RhoB and RhoC have different roles in cancer cell migration. J Microsc. 251:242–249.
   PubMed Web of Science ®Google Scholar
• Rowland BD, Peeper DS. 2006. KLF4, p21 and context-dependant opposing forces in cancer. Nat Rev Cancer. 6:11–23.
   PubMed Web of Science ®Google Scholar
• Shields JM, Christy RJ, Yang VW. 1996. Identification and characterization of a gene encoding a gut-enriched Krüppel-like factor expressed during growth arrest. J Biol Chem. 271:20009–20017.
   PubMed Web of Science ®Google Scholar
• Takahashi R, Nagayama S, Furu M, Kajita Y, Jin Y, Kato T, Imoto S, Sakai Y, Junya T. 2014. AFAP1L1, a novel associating partner with vinculin, modulates cellular morphology and motility, and promotes the progression of colorectal cancers. Cancer Med. 3:759–774.
   PubMed Web of Science ®Google Scholar
• Thievessen I, Fakhri N, Steinwachs J, Kraus V, McIsaac RS, Gao L, Chen BC, Baird MA, Davidson MW, Betzig E, et al. 2015. Vinculin is required for cell polarization, migration, and extracellular matrix remodeling in 3D collagen. FASEB J. 29:4555–4567.
   PubMed Web of Science ®Google Scholar
• Todaro GJ, Green H. 1963. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J Cell Biol. 17:299–313.
   PubMed Web of Science ®Google Scholar
• Van Aelst L, D’Souza-Schorey C. 1997. Rho GTPases and signaling networks. Genes Dev. 11:2295–2322.
   PubMed Web of Science ®Google Scholar
• Wei D, Gong W, Kanal M, Schlunk C, Wang L, Yao JC, Wu TT, Huang S, Xie K. 2005. Drastic down-regulation of Krüppel-like factor 4 expression is critical in human gastric cancer development and progression. Cancer Res. 65:2746–2754.
   PubMed Web of Science ®Google Scholar
• Wheeler A, Ridley A. 2004. Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility. Exp Cell Res. 301:43–49.
   PubMed Web of Science ®Google Scholar
• Yamazaki D, Kurisu S, Takenawa T. 2005. Regulation of cancer cell motility through actin reorganization. Cancer Sci. 96:379–386.
   PubMed Web of Science ®Google Scholar
• Yori J, Seachrist D, Johnson E, Lozada K, Abdul-Karim F, Chodosh L, Schiemann W, Keri R. 2011. Krüppel-like factor 4 inhibits tumorigenic progression and metastasis in a mouse model of breast cancer. Neoplasia. 3:601–610.
   Web of Science ®Google Scholar
• Zammarchi F, Morelli M, Menicagli M, Di Cristofano C, Zavaglia K, Paolucci A, Campani D, Aretini P, Boggi U, Mosca F, Cavazzana A, et al. 2010. KLF4 is a novel candidate tumor suppressor gene in pancreatic ductal carcinoma. Am J Pathol. 178:361–372.
   PubMed Web of Science ®Google Scholar
• Zhao W, Hisamuddin IM, Nandan MO, Babbin BA, Lamb NE, Yang VW. 2004. Identification of Krüppel-like factor 4 as a potential tumor suppressor gene in colorectal cancer. Oncogene. 23:395–402.
   PubMed Web of Science ®Google Scholar
• Zhou J, Xiang Y, Yoshimura T, Chen K, Gong W, Huang J, Zhou Y, Yao X, Bian J, Wang JM. 2014. The role of chemoattractant receptors in shaping the tumor microenvironment. BioMed Res Int. 2014:751392.
   PubMed Web of Science ®Google Scholar