Krüppel like factor 6 splice variant 1 (KLF6-SV1) overexpression recruits macrophages to participate in lung cancer metastasis by up-regulating TWIST1

References

• Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, Patnaik A, Aggarwal C, Gubens M, Horn L, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 2015;372:2018–2028. doi:10.1056/NEJMoa1501824.
   PubMed Web of Science ®Google Scholar
• Wang T, Nelson RA, Bogardus A, Grannis FW Jr. Five-year lung cancer survival: which advanced stage nonsmall cell lung cancer patients attain long-term survival?. Cancer. 2010;116:1518–1525. doi:10.1002/cncr.24871.
   PubMed Web of Science ®Google Scholar
• Meguid RA, Hooker CM, Harris J, Xu L, Westra WH, Sherwood JT, Sussman M, Cattaneo SM, Shin J, Cox S, et al. Long-term survival outcomes by smoking status in surgical and nonsurgical patients with non-small cell lung cancer: comparing never smokers and current smokers. Chest. 2010;138:500–509. doi:10.1378/chest.08-2991.
   PubMed Web of Science ®Google Scholar
• Carnio S, Novello S, Mele T, Levra MG, Scagliotti GV. Extending survival of stage IV non-small cell lung cancer. Semin Oncol. 2014;41:69–92. doi:10.1053/j.seminoncol.2013.12.013.
   PubMed Web of Science ®Google Scholar
• Voltolini L, Bongiolatti S, Luzzi L, Bargagli E, Fossi A, Ghiribelli C, Rottoli P, Gotti G. Impact of interstitial lung disease on short-term and long-term survival of patients undergoing surgery for non-small-cell lung cancer: analysis of risk factors. Eur J Cardiothorac Surg. 2013;43:e17–23. doi:10.1093/ejcts/ezs560.
   PubMed Web of Science ®Google Scholar
• Cheung LW, Yung S, Chan TM, Leung PC, Wong AS. Targeting gonadotropin-releasing hormone receptor inhibits the early step of ovarian cancer metastasis by modulating tumor-mesothelial adhesion. Mol Ther. 2013;21:78–90. doi:10.1038/mt.2012.187.
   PubMed Web of Science ®Google Scholar
• Yin M, Li X, Tan S, Zhou HJ, Ji W, Bellone S, Xu X, Zhang H, Santin AD, Lou G, et al. Tumor-associated macrophages drive spheroid formation during early transcoelomic metastasis of ovarian cancer. J Clin Invest. 2016;126:4157–4173. doi:10.1172/JCI87252.
   PubMed Web of Science ®Google Scholar
• Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010;141:52–67. doi:10.1016/j.cell.2010.03.015.
   PubMed Web of Science ®Google Scholar
• Mittal K, Ebos J, Rini B. Angiogenesis and the tumor microenvironment: vascular endothelial growth factor and beyond. Semin Oncol. 2014;41:235–251. doi:10.1053/j.seminoncol.2014.02.007.
   PubMed Web of Science ®Google Scholar
• Yu H, Kortylewski M, Pardoll D. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat Rev Immunol. 2007;7:41–51. doi:10.1038/nri1995.
   PubMed Web of Science ®Google Scholar
• Yuan Z, Mehta HJ, Mohammed K, Nasreen N, Roman R, Brantly M, Sadikot RT, Mattei F. TREM-1 is induced in tumor associated macrophages by cyclo-oxygenase pathway in human non-small cell lung cancer. PLoS ONE. 2014;9:e94241. doi:10.1371/journal.pone.0094241.
   PubMed Web of Science ®Google Scholar
• Chanmee T, Ontong P, Konno K, Itano N. Tumor-associated macrophages as major players in the tumor microenvironment. Cancers. 2014;6:1670–1690. doi:10.3390/cancers6031670.
   PubMed Web of Science ®Google Scholar
• Hao NB, Lu MH, Fan YH, Cao YL, Zhang ZR, Yang SM. Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol. 2012;2012:948098. doi:10.1155/2012/948098.
   PubMedGoogle Scholar
• Martinez FO, Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 2014;6:13. doi:10.12703/P.
   PubMedGoogle Scholar
• Joshi S, Singh AR, Zulcic M, Bao L, Messer K, Ideker T, Dutkowski J, Durden DL, Chrzanowska-Wodnicka M. Rac2 controls tumor growth, metastasis and M1-M2 macrophage differentiation in vivo. PLoS ONE. 2014;9:e95893. doi:10.1371/journal.pone.0095893.
   PubMed Web of Science ®Google Scholar
• Festuccia WT, Pouliot P, Bakan I, Sabatini DM, Laplante M. Myeloid-specific Rictor deletion induces M1 macrophage polarization and potentiates in vivo pro-inflammatory response to lipopolysaccharide. PLoS ONE. 2014;9:e95432. doi:10.1371/journal.pone.0095432.
   PubMed Web of Science ®Google Scholar
• Ye Y, Xu Y, Lai Y, He W, Li Y, Wang R, Luo X, Chen R, Chen T. Long non-coding RNA cox-2 prevents immune evasion and metastasis of hepatocellular carcinoma by altering M1/M2 macrophage polarization. J Cell Biochem. 2018;119:2951–2963. doi:10.1002/jcb.26509.
   PubMed Web of Science ®Google Scholar
• Jia XH, Feng GW, Wang ZL, Du Y, Shen C, Hui H, Peng D, Li Z-J, Kong D-L, Tian J. Activation of mesenchymal stem cells by macrophages promotes tumor progression through immune suppressive effects. Oncotarget. 2016;7:20934–20944. doi:10.18632/oncotarget.8064.
   PubMedGoogle Scholar
• Velpula KK, Dasari VR, Tsung AJ, Dinh DH, Rao JS. Cord blood stem cells revert glioma stem cell EMT by down regulating transcriptional activation of Sox2 and Twist1. Oncotarget. 2011;2:1028–1042. doi:10.18632/oncotarget.367.
   PubMedGoogle Scholar
• Zhao N, Sun H, Sun B, Zhu D, Zhao X, Wang Y, Gu Q, Dong X, Liu F, Zhang Y, et al. miR-27a-3p suppresses tumor metastasis and VM by down-regulating VE-cadherin expression and inhibiting EMT: an essential role for Twist-1 in HCC. Sci Rep. 2016;6:23091. doi:10.1038/srep23091.
   PubMed Web of Science ®Google Scholar
• D’Angelo RC, Liu XW, Najy AJ, Jung YS, Won J, Chai KX, Fridman R, Kim H-RC. TIMP-1 via TWIST1 induces EMT phenotypes in human breast epithelial cells. Mol Cancer Res. 2014;12:1324–1333. doi:10.1158/1541-7786.MCR-14-0105.
   PubMed Web of Science ®Google Scholar
• Ito G, Uchiyama M, Kondo M, Mori S, Usami N, Maeda O, Kawabe T, Hasegawa Y, Shimokata K, Sekido Y. Kruppel-like factor 6 is frequently down-regulated and induces apoptosis in non-small cell lung cancer cells. Cancer Res. 2004;64:3838–3843. doi:10.1158/0008-5472.CAN-04-0185.
   PubMed Web of Science ®Google Scholar
• Ozdemir F, Koksal M, Ozmen V, Aydin I, Buyru N. Mutations and Kruppel-like factor 6 (KLF6) expression levels in breast cancer. Tumour Biol. 2014;35:5219–5225. doi:10.1007/s13277-014-1678-6.
   PubMedGoogle Scholar
• Liang WC, Wang Y, Xiao LJ, Wang YB, Fu WM, Wang WM, Jiang H-Q, Qi W, Wan DC-C, Zhang J-F, et al. Identification of miRNAs that specifically target tumor suppressive KLF6-FL rather than oncogenic KLF6-SV1 isoform. RNA Biol. 2014;11:845–854. doi:10.4161/rna.29356.
   PubMed Web of Science ®Google Scholar
• Hatami R, Sieuwerts AM, Izadmehr S, Yao Z, Qiao RF, Papa L, Look MP, Smid M, Ohlssen J, Levine AC, et al. KLF6-SV1 drives breast cancer metastasis and is associated with poor survival. Sci Transl Med. 2013;5:169ra12. doi:10.1126/scitranslmed.3004688.
   PubMed Web of Science ®Google Scholar
• Black AR, Black JD, Azizkhan-Clifford J. Sp1 and kruppel-like factor family of transcription factors in cell growth regulation and cancer. J Cell Physiol. 2001;188:143–160. doi:10.1002/jcp.1111.
   PubMed Web of Science ®Google Scholar
• Pei J, Grishin NV. A new family of predicted Kruppel-like factor genes and pseudogenes in placental mammals. PLoS ONE. 2013;8:e81109. doi:10.1371/journal.pone.0081109.
   PubMed Web of Science ®Google Scholar
• Jeng YM, Hsu HC. KLF6, a putative tumor suppressor gene, is mutated in astrocytic gliomas. Int J Cancer Manag. 2003;105:625–629. doi:10.1002/ijc.11123.
   PubMed Web of Science ®Google Scholar
• Boyault S, Herault A, Balabaud C, Zucman-Rossi J. Absence of KLF6 gene mutation in 71 hepatocellular carcinomas. Hepatology. 2005;41:681–2;author reply 2–3. doi:10.1002/hep.20588.
   PubMed Web of Science ®Google Scholar
• Hatami R, Sieuwerts AM, Izadmehr S, Yao Z, Qiao RF, Papa L, Look MP, Smid M, Ohlssen J, Levine AC, et al. An oncogenic splice variant drives EMT and metastasis in breast cancer. Cancer Discov. 2013;3:16. doi:10.1158/2159-8290.CD-RW2013-027.
   Google Scholar
• Narla G, Difeo A, Reeves HL, Schaid DJ, Hirshfeld J, Hod E, Katz A, Isaacs WB, Hebbring S, Komiya A, et al. A germline DNA polymorphism enhances alternative splicing of the KLF6 tumor suppressor gene and is associated with increased prostate cancer risk. Cancer Res. 2005;65:1213–1222. doi:10.1158/0008-5472.CAN-04-4249.
   PubMed Web of Science ®Google Scholar
• DiFeo A, Feld L, Rodriguez E, Wang C, Beer DG, Martignetti JA, Narla G. A functional role for KLF6-SV1 in lung adenocarcinoma prognosis and chemotherapy response. Cancer Res. 2008;68:965–970. doi:10.1158/0008-5472.CAN-07-2604.
   PubMed Web of Science ®Google Scholar
• Rokavec M, Öner MG, Li H, Jackstadt R, Jiang L, Lodygin D, Kaller M, Horst D, Ziegler PK, Schwitalla S, et al. Corrigendum. IL-6R/STAT3/miR-34a feedback loop promotes EMT-mediated colorectal cancer invasion and metastasis. J Clin Invest. 2015;125:1362. doi:10.1172/JCI80323.
   PubMed Web of Science ®Google Scholar
• Liu YN, Yin JJ, Abou-Kheir W, Hynes PG, Casey OM, Fang L, Yi M, Stephens RM, Seng V, Sheppard-Tillman H, et al. MiR-1 and miR-200 inhibit EMT via Slug-dependent and tumorigenesis via Slug-independent mechanisms. Oncogene. 2013;32:296–306. doi:10.1038/onc.2012.58.
   PubMed Web of Science ®Google Scholar
• Kaufhold S, Bonavida B. Central role of Snail1 in the regulation of EMT and resistance in cancer: a target for therapeutic intervention. J Exp Clin Cancer Res. 2014;33:62. doi:10.1186/s13046-014-0062-0.
   PubMed Web of Science ®Google Scholar
• Tao Y, Han T, Zhang T, Ma C, Sun C. LncRNA CHRF-induced miR-489 loss promotes metastasis of colorectal cancer via TWIST1/EMT signaling pathway. Oncotarget. 2017;8:36410–36422. doi:10.18632/oncotarget.16850.
   PubMedGoogle Scholar
• Shamir ER, Pappalardo E, Jorgens DM, Coutinho K, Tsai WT, Aziz K, Auer M, Tran PT, Bader JS, Ewald AJ. Twist1-induced dissemination preserves epithelial identity and requires E-cadherin. J Cell Biol. 2014;204:839–856. doi:10.1083/jcb.201306088.
   PubMed Web of Science ®Google Scholar
• Low-Marchelli JM, Ardi VC, Vizcarra EA, van Rooijen N, Quigley JP, Yang J. Twist1 induces CCL2 and recruits macrophages to promote angiogenesis. Cancer Res. 2013;73:662–671. doi:10.1158/0008-5472.CAN-12-0653.
   PubMed Web of Science ®Google Scholar
• Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, Kaiser EA, Snyder LA, Pollard JW. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011;475:222–225. doi:10.1038/nature10138.
   PubMed Web of Science ®Google Scholar
• Yaddanapudi K, Putty K, Rendon BE, Lamont GJ, Faughn JD, Satoskar A, Lasnik A, Eaton JW, Mitchell RA. Control of tumor-associated macrophage alternative activation by macrophage migration inhibitory factor. J Immunol. 1950;2013(190):2984–2993.
   Google Scholar
• Dwyer AR, Greenland EL, Pixley FJ. Promotion of Tumor Invasion by Tumor-Associated Macrophages: the Role of CSF-1-Activated Phosphatidylinositol 3 Kinase and Src Family Kinase Motility Signaling. Cancers. 2017;9(6).
   Web of Science ®Google Scholar
• Tseng WC, Chuang CW, Yang MH, Pan CC, Tarng DC. Kruppel-like factor 4 is a novel prognostic predictor for urothelial carcinoma of bladder and it regulates TWIST1-mediated epithelial-mesenchymal transition. Urol Oncol. 2016;34:485.e15-.e24. doi:10.1016/j.urolonc.2016.07.002.
   PubMed Web of Science ®Google Scholar
• Yang Y, Qin J, Lan L, Li N, Wang C, He P, Liu F, Ni H, Wang Y. M-CSF cooperating with NFkappaB induces macrophage transformation from M1 to M2 by upregulating c-Jun. Cancer Biol Ther. 2014;15:99–107. doi:10.4161/cbt.26718.
   PubMed Web of Science ®Google Scholar
• Craig DG, Lee P, Pryde EA, Hayes PC, Simpson KJ. Serum neopterin and soluble CD163 as markers of macrophage activation in paracetamol (acetaminophen)-induced human acute liver injury. Aliment Pharmacol Ther. 2013;38:1395–1404. doi:10.1111/apt.12530.
   PubMed Web of Science ®Google Scholar
• Weber M, Iliopoulos C, Moebius P, Buttner-Herold M, Amann K, Ries J, Preidl R, Neukam FW, Wehrhan F. Prognostic significance of macrophage polarization in early stage oral squamous cell carcinomas. Oral Oncol. 2016;52:75–84. doi:10.1016/j.oraloncology.2015.11.001.
   PubMed Web of Science ®Google Scholar
• Zhang J, Cao J, Ma S, Dong R, Meng W, Ying M, Weng Q, Chen Z, Ma J, Fang Q, et al. Tumor hypoxia enhances Non-Small Cell Lung Cancer metastasis by selectively promoting macrophage M2 polarization through the activation of ERK signaling. Oncotarget. 2014;5:9664–9677. doi:10.18632/oncotarget.1856.
   PubMedGoogle Scholar
• Zhang Y, Wei Y, Jiang B, Chen L, Bai H, Zhu X, Li X, Zhang H, Yang Q, Ma J, et al. Scavenger Receptor A1 Prevents Metastasis of Non-Small Cell Lung Cancer via Suppression of Macrophage Serum Amyloid A1. Cancer Res. 2017;77:1586–1598. doi:10.1158/0008-5472.CAN-16-1569.
   PubMed Web of Science ®Google Scholar
• Cho MS, Rupaimoole R, Choi HJ, Noh K, Chen J, Hu Q, Sood AK, Afshar-Kharghan V. Complement Component 3 Is Regulated by TWIST1 and Mediates Epithelial-Mesenchymal Transition. J Immunol. 2016;196:1412–1418. doi:10.4049/jimmunol.1501886.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Du W, Chen Z, Xiang C. Upregulation of PD-L1 by SPP1 mediates macrophage polarization and facilitates immune escape in lung adenocarcinoma. Exp Cell Res. 2017;359:449–457. doi:10.1016/j.yexcr.2017.08.028.
   PubMed Web of Science ®Google Scholar
• Jetten N, Verbruggen S, Gijbels MJ, Post MJ, De Winther MP, Donners MM. Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo. Angiogenesis. 2014;17:109–118. doi:10.1007/s10456-013-9381-6.
   PubMed Web of Science ®Google Scholar
• Oghumu S, Varikuti S, Terrazas C, Kotov D, Nasser MW, Powell CA, Ganju RK, Satoskar AR. CXCR3 deficiency enhances tumor progression by promoting macrophage M2 polarization in a murine breast cancer model. Immunology. 2014;143:109–119. doi:10.1111/imm.12293.
   PubMed Web of Science ®Google Scholar
• Ke X, Wu M, Lou J, Zhang S, Huang P, Sun R, Huang L, Xie E, Wang F, Gu B. Activation of Toll-like receptors signaling in non-small cell lung cancer cell line induced by tumor-associated macrophages. Chin J Cancer Res. 2015;27:181–189. doi:10.3978/j.issn.1000-9604.2015.03.07.
   PubMed Web of Science ®Google Scholar