NR4A1 Antagonists Inhibit β1-Integrin-Dependent Breast Cancer Cell Migration

REFERENCES

• Shattil SJ, Kim C, Ginsberg MH. 2010. The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol 11:288–300. http://dx.doi.org/10.1038/nrm2871.
   PubMed Web of Science ®Google Scholar
• Arnaout MA, Goodman SL, Xiong JP. 2007. Structure and mechanics of integrin-based cell adhesion. Curr Opin Cell Biol 19:495–507. http://dx.doi.org/10.1016/j.ceb.2007.08.002.
   PubMed Web of Science ®Google Scholar
• Hynes RO. 2002. Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687. http://dx.doi.org/10.1016/S0092-8674(02)00971-6.
   PubMed Web of Science ®Google Scholar
• Goodman SL, Picard M. 2012. Integrins as therapeutic targets. Trends Pharmacol Sci 33:405–412. http://dx.doi.org/10.1016/j.tips.2012.04.002.
   PubMed Web of Science ®Google Scholar
• Desgrosellier JS, Cheresh DA. 2010. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 10:9–22. http://dx.doi.org/10.1038/nrc2748.
   PubMed Web of Science ®Google Scholar
• Brakebusch C, Fassler R. 2005. β1-Integrin function in vivo: adhesion, migration and more. Cancer Metastasis Rev 24:403–411. http://dx.doi.org/10.1007/s10555-005-5132-5.
   PubMed Web of Science ®Google Scholar
• Barkan D, Chambers AF. 2011. β1-Integrin: a potential therapeutic target in the battle against cancer recurrence. Clin Cancer Res 17:7219–7223. http://dx.doi.org/10.1158/1078-0432.CCR-11-0642.
   PubMed Web of Science ®Google Scholar
• Howe GA, Addison CL. 2012. β1 Integrin: an emerging player in the modulation of tumorigenesis and response to therapy. Cell Adh Migr 6:71–77. http://dx.doi.org/10.4161/cam.20077.
   PubMed Web of Science ®Google Scholar
• Lahlou H, Muller WJ. 2011. Beta1-integrins signaling and mammary tumor progression in transgenic mouse models: implications for human breast cancer. Breast Cancer Res 13:229. http://dx.doi.org/10.1186/bcr2905.
   PubMedGoogle Scholar
• Wang D, Muller S, Amin AR, Huang D, Su L, Hu Z, Rahman MA, Nannapaneni S, Koenig L, Chen Z, Tighiouart M, Shin DM, Chen ZG. 2012. The pivotal role of integrin beta1 in metastasis of head and neck squamous cell carcinoma. Clin Cancer Res 18:4589–4599. http://dx.doi.org/10.1158/1078-0432.CCR-11-3127.
   PubMedGoogle Scholar
• Oshita F, Kameda Y, Hamanaka N, Saito H, Yamada K, Noda K, Mitsuda A. 2004. High expression of integrin beta1 and p53 is a greater poor prognostic factor than clinical stage in small-cell lung cancer. Am J Clin Oncol 27:215–219. http://dx.doi.org/10.1097/01.COC.0000054894.64867.80.
   PubMedGoogle Scholar
• Yao ES, Zhang H, Chen YY, Lee B, Chew K, Moore D, Park C. 2007. Increased beta1 integrin is associated with decreased survival in invasive breast cancer. Cancer Res 67:659–664. http://dx.doi.org/10.1158/0008-5472.CAN-06-2768.
   PubMed Web of Science ®Google Scholar
• dos Santos PB, Zanetti JS, Ribeiro-Silva A, Beltrao EI. 2012. Beta 1 integrin predicts survival in breast cancer: a clinicopathological and immunohistochemical study. Diagn Pathol 7:104. http://dx.doi.org/10.1186/1746-1596-7-104.
   PubMed Web of Science ®Google Scholar
• Wei G, Du Y, Yang C, Zhang X. 2008. The expression and significance of integrin beta1 and focal adhesion kinase and its clinical value in laryngeal carcinoma. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 22:1112–1114. ( In Chinese.)
   PubMedGoogle Scholar
• Nikkola J, Vihinen P, Vlaykova T, Hahka-Kemppinen M, Heino J, Pyrhonen S. 2004. Integrin chains beta1 and alphav as prognostic factors in human metastatic melanoma. Melanoma Res 14:29–37.
   PubMed Web of Science ®Google Scholar
• Pontes-Junior J, Reis ST, de Oliveira LC, Sant'anna AC, Dall'oglio MF, Antunes AA, Ribeiro-Filho LA, Carvalho PA, Cury J, Srougi M, Leite KR. 2010. Association between integrin expression and prognosis in localized prostate cancer. Prostate 70:1189–1195. http://dx.doi.org/10.1002/pros.21153.
   PubMed Web of Science ®Google Scholar
• Bottger TC, Maschek H, Lobo M, Gottwohl RG, Brenner W, Junginger T. 1999. Prognostic value of immunohistochemical expression of beta-1 integrin in pancreatic carcinoma. Oncology 56:308–313. http://dx.doi.org/10.1159/000011984.
   PubMedGoogle Scholar
• Luo M, Guan JL. 2010. Focal adhesion kinase: a prominent determinant in breast cancer initiation, progression and metastasis. Cancer Lett 289:127–139. http://dx.doi.org/10.1016/j.canlet.2009.07.005.
   PubMedGoogle Scholar
• Theocharis SE, Klijanienko JT, Padoy E, Athanassiou S, Sastre-Garau XX. 2009. Focal adhesion kinase (FAK) immunocytochemical expression in breast ductal invasive carcinoma (DIC): correlation with clinicopathological parameters and tumor proliferative capacity. Med Sci Monit 15:BR221–BR226.
   PubMed Web of Science ®Google Scholar
• Yom CK, Noh DY, Kim WH, Kim HS. 2011. Clinical significance of high focal adhesion kinase gene copy number and overexpression in invasive breast cancer. Breast Cancer Res Treat 128:647–655. http://dx.doi.org/10.1007/s10549-010-1150-2.
   PubMedGoogle Scholar
• Lahlou H, Sanguin-Gendreau V, Zuo D, Cardiff RD, McLean GW, Frame MC, Muller WJ. 2007. Mammary epithelial-specific disruption of the focal adhesion kinase blocks mammary tumor progression. Proc Natl Acad Sci U S A 104:20302–20307. http://dx.doi.org/10.1073/pnas.0710091104.
   PubMed Web of Science ®Google Scholar
• White DE, Kurpios NA, Zuo D, Hassell JA, Blaess S, Mueller U, Muller WJ. 2004. Targeted disruption of beta1-integrin in a transgenic mouse model of human breast cancer reveals an essential role in mammary tumor induction. Cancer Cell 6:159–170. http://dx.doi.org/10.1016/j.ccr.2004.06.025.
   PubMed Web of Science ®Google Scholar
• Huck L, Pontier SM, Zuo DM, Muller WJ. 2010. β1-Integrin is dispensable for the induction of ErbB2 mammary tumors but plays a critical role in the metastatic phase of tumor progression. Proc Natl Acad Sci U S A 107:15559–15564. http://dx.doi.org/10.1073/pnas.1003034107.
   PubMed Web of Science ®Google Scholar
• Safe S, Jin UH, Hedrick E, Reeder A, Lee SO. 2014. Role of orphan nuclear receptors in cancer and potential as drug targets. Mol Endocrinol 28:157–172. http://dx.doi.org/10.1210/me.2013-1291.
   PubMed Web of Science ®Google Scholar
• Lee SO, Abdelrahim M, Yoon K, Chintharlapalli S, Papineni S, Kim K, Wang H, Safe S. 2010. Inactivation of the orphan nuclear receptor TR3/Nur77 inhibits pancreatic cancer cell and tumor growth. Cancer Res 70:6824–6836. http://dx.doi.org/10.1158/0008-5472.CAN-10-1992.
   PubMed Web of Science ®Google Scholar
• Lee SO, Andey T, Jin UH, Kim K, Singh M, Safe S. 2012. The nuclear receptor TR3 regulates mTORC1 signaling in lung cancer cells expressing wild-type p53. Oncogene 31:3265–3276. http://dx.doi.org/10.1038/onc.2011.504.
   PubMed Web of Science ®Google Scholar
• Lee SO, Jin UH, Kang JH, Kim SB, Guthrie AS, Sreevalsan S, Lee JS, Safe S. 2014. The orphan nuclear receptor NR4A1 (Nur77) regulates oxidative and endoplasmic reticulum stress in pancreatic cancer cells. Mol Cancer Res 12:527–538. http://dx.doi.org/10.1158/1541-7786.MCR-13-0567.
   PubMed Web of Science ®Google Scholar
• Lee SO, Li X, Hedrick E, Jin UH, Tjalkens RB, Backos DS, Li L, Zhang Y, Wu Q, Safe S. 2014. Diindolylmethane analogs bind NR4A1 and are NR4A1 antagonists in colon cancer cells. Mol Endocrinol 28:1729–1739. http://dx.doi.org/10.1210/me.2014-1102.
   PubMed Web of Science ®Google Scholar
• Hedrick E, Lee SO, Kim G, Abdelrahim M, Jin UH, Safe S, Abudayyeh A. 2015. Nuclear receptor 4A1 (NR4A1) as a drug target for renal cell adenocarcinoma. PLoS One 10:e0128308. http://dx.doi.org/10.1371/journal.pone.0128308.
   PubMedGoogle Scholar
• Hedrick E, Lee SO, Doddapaneni R, Singh M, Safe S. 2015. Nuclear receptor 4A1 as a drug target for breast cancer chemotherapy. Endocr Relat Cancer 22:831–840. http://dx.doi.org/10.1530/ERC-15-0063.
   PubMedGoogle Scholar
• Zhou F, Drabsch Y, Dekker TJ, de Vinuesa AG, Li Y, Hawinkels LJ, Sheppard KA, Goumans MJ, Luwor RB, de Vries CJ, Mesker WE, Tollenaar RA, Devilee P, Lu CX, Zhu H, Zhang L, Dijke PT. 2014. Nuclear receptor NR4A1 promotes breast cancer invasion and metastasis by activating TGF-beta signalling. Nat Commun 5:3388. http://dx.doi.org/10.1038/ncomms4388.
   PubMed Web of Science ®Google Scholar
• Wilson TE, Padgett KA, Johnston M, Milbrandt J. 1993. A genetic method for defining DNA-binding domains: application to the nuclear receptor NGFI-B. Proc Natl Acad Sci U S A 90:9186–9190. http://dx.doi.org/10.1073/pnas.90.19.9186.
   PubMedGoogle Scholar
• Philips A, Lesage S, Gingras R, Maira MH, Gauthier Y, Hugo P, Drouin J. 1997. Novel dimeric Nur77 signaling mechanism in endocrine and lymphoid cells. Mol Cell Biol 17:5946–5951. http://dx.doi.org/10.1128/MCB.17.10.5946.
   PubMed Web of Science ®Google Scholar
• Parvani JG, Galliher-Beckley AJ, Schiemann BJ, Schiemann WP. 2013. Targeted inactivation of β1 integrin induces β3 integrin switching, which drives breast cancer metastasis by TGF-β. Mol Biol Cell 24:3449–3459. http://dx.doi.org/10.1091/mbc.E12-10-0776.
   PubMedGoogle Scholar
• Truong HH, Xiong J, Ghotra VP, Nirmala E, Haazen L, Le Devedec SE, Balcioglu HE, He S, Snaar-Jagalska BE, Vreugdenhil E, Meerman JH, van de Water B, Danen EH. 2014. β1 Integrin inhibition elicits a prometastatic switch through the TGFβ-miR-200-ZEB network in E-cadherin-positive triple-negative breast cancer. Sci Signal 7:ra15. http://dx.doi.org/10.1126/scisignal.2004751.
   PubMedGoogle Scholar
• Madamanchi A, Zijlstra A, Zutter MM. 2014. Flipping the switch: integrin switching provides metastatic competence. Sci Signal 7:pe9. http://dx.doi.org/10.1126/scisignal.2005236.
   PubMedGoogle Scholar
• Villa-Garcia M, Li L, Riely G, Bray PF. 1994. Isolation and characterization of a TATA-less promoter for the human β3 integrin gene. Blood 83:668–676.
   PubMedGoogle Scholar
• Kurakula K, Koenis DS, van Tiel CM, de Vries CJ. 2014. NR4A nuclear receptors are orphans but not lonesome. Biochim Biophys Acta 1843:2543–2555. http://dx.doi.org/10.1016/j.bbamcr.2014.06.010.
   PubMed Web of Science ®Google Scholar
• Pearen MA, Muscat GE. 2010. Nuclear hormone receptor 4A signaling: implications for metabolic disease. Mol Endocrinol 24:1891–1903. http://dx.doi.org/10.1210/me.2010-0015.
   PubMed Web of Science ®Google Scholar
• Safe S, Jin UH, Morpurgo B, Abudayyeh A, Singh M, Tjalkens RB. 23 April 2015. Nuclear receptor 4A (NR4A) family - orphans no more. J Steroid Biochem Mol Biol http://dx.doi.org/10.1016/j.jsbmb.2015.04.016.
   Google Scholar
• Liu JJ, Zeng HN, Zhang LR, Zhan YY, Chen Y, Wang Y, Wang J, Xiang SH, Liu WJ, Wang WJ, Chen HZ, Shen YM, Su WJ, Huang PQ, Zhang HK, Wu Q. 2010. A unique pharmacophore for activation of the nuclear orphan receptor Nur77 in vivo and in vitro. Cancer Res 70:3628–3637. http://dx.doi.org/10.1158/0008-5472.CAN-09-3160.
   PubMed Web of Science ®Google Scholar
• Kolluri SK, Zhu X, Zhou X, Lin B, Chen Y, Sun K, Tian X, Town J, Cao X, Lin F, Zhai D, Kitada S, Luciano F, O'Donnell E, Cao Y, He F, Lin J, Reed JC, Satterthwait AC, Zhang XK. 2008. A short Nur77-derived peptide converts Bcl-2 from a protector to a killer. Cancer Cell 14:285–298. http://dx.doi.org/10.1016/j.ccr.2008.09.002.
   PubMed Web of Science ®Google Scholar
• Zhan YY, Chen Y, Zhang Q, Zhuang JJ, Tian M, Chen HZ, Zhang LR, Zhang HK, He JP, Wang WJ, Wu R, Wang Y, Shi C, Yang K, Li AZ, Xin YZ, Li TY, Yang JY, Zheng ZH, Yu CD, Lin SC, Chang C, Huang PQ, Lin T, Wu Q. 2012. The orphan nuclear receptor Nur77 regulates LKB1 localization and activates AMPK. Nat Chem Biol 8:897–904. http://dx.doi.org/10.1038/nchembio.1069.
   PubMed Web of Science ®Google Scholar
• Wu H, Lin Y, Li W, Sun Z, Gao W, Zhang H, Xie L, Jiang F, Qin B, Yan T, Chen L, Zhao Y, Cao X, Wu Y, Lin B, Zhou H, Wong AS, Zhang XK, Zeng JZ. 2011. Regulation of Nur77 expression by beta-catenin and its mitogenic effect in colon cancer cells. FASEB J 25:192–205. http://dx.doi.org/10.1096/fj.10-166462.
   PubMedGoogle Scholar
• Lin B, Kolluri SK, Lin F, Liu W, Han YH, Cao X, Dawson MI, Reed JC, Zhang XK. 2004. Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/TR3. Cell 116:527–540. http://dx.doi.org/10.1016/S0092-8674(04)00162-X.
   PubMed Web of Science ®Google Scholar
• Zhang XK. 2007. Targeting Nur77 translocation. Expert Opin Ther Targets 11:69–79. http://dx.doi.org/10.1517/14728222.11.1.69.
   PubMed Web of Science ®Google Scholar
• Ferlini C, Cicchillitti L, Raspaglio G, Bartollino S, Cimitan S, Bertucci C, Mozzetti S, Gallo D, Persico M, Fattorusso C, Campiani G, Scambia G. 2009. Paclitaxel directly binds to Bcl-2 and functionally mimics activity of Nur77. Cancer Res 69:6906–6914. http://dx.doi.org/10.1158/0008-5472.CAN-09-0540.
   PubMed Web of Science ®Google Scholar
• Pipaon C, Tsai SY, Tsai MJ. 1999. COUP-TF upregulates NGFI-A gene expression through an Sp1 binding site. Mol Cell Biol 19:2734–2745. http://dx.doi.org/10.1128/MCB.19.4.2734.
   PubMedGoogle Scholar
• Shimada J, Suzuki Y, Kim SJ, Wang PC, Matsumura M, Kojima S. 2001. Transactivation via RAR/RXR-Sp1 interaction: characterization of binding between Sp1 and GC box motif. Mol Endocrinol 15:1677–1692. http://dx.doi.org/10.1210/mend.15.10.0707.
   PubMedGoogle Scholar
• Sugawara A, Uruno A, Kudo M, Ikeda Y, Sato K, Taniyama Y, Ito S, Takeuchi K. 2002. Transcription suppression of thromboxane receptor gene by peroxisome proliferator-activated receptor-gamma via an interaction with Sp1 in vascular smooth muscle cells. J Biol Chem 277:9676–9683. http://dx.doi.org/10.1074/jbc.M104560200.
   PubMed Web of Science ®Google Scholar