COUP-TFI modifies CXCL12 and CXCR4 expression by activating EGF signaling and stimulates breast cancer cell migration

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Boudot, Antoine ^a,d   Kerdivel, Gwenneg ^a   Lecomte, Sylvain ^a   Flouriot, Gilles ^a   Desille, Mireille ^b,c   Godey, Florence ^b   Leveque, Jean ^b   Tas, Patrick ^b   Le Dréan, Yves ^a   Pakdel, Farzad ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b RENNES UNIVERSITY HOSPITAL   (France)

^c Univ Rennes   (France)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Breast cancer; Cell migration; COUP TF; CXCL12 signaling; Estrogen receptor

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR 1; EPIDERMAL GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; CXCL12 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; NR2F1 PROTEIN, HUMAN; STROMAL CELL DERIVED FACTOR 1;

AMINO ACID SEQUENCE; ARTICLE; BIOASSAY; BREAST CANCER CELL LINE; CANCER GRADING; CELL GROWTH; CELL MIGRATION; CELL MOTILITY; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; METASTASIS POTENTIAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN TARGETING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; BIOSYNTHESIS; BREAST TUMOR; CELL MOTION; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MCF 7 CELL LINE; METABOLISM; PATHOLOGY; PROMOTER REGION;

BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; CHEMOKINE CXCL12; COUP TRANSCRIPTION FACTOR I; EPIDERMAL GROWTH FACTOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MCF-7 CELLS; PROMOTER REGIONS, GENETIC; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION;

EID: 84902661563     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-407     Document Type: Article

References (46)

1. Barone I, Brusco L, Fuqua SAW. Estrogen receptor mutations and changes in downstream gene expression and signaling. Clin Cancer Res Off J Am Assoc Cancer Res 2010, 16:2702-2708.
2. Rochefort H, Platet N, Hayashido Y, Derocq D, Lucas A, Cunat S, Garcia M. Estrogen receptor mediated inhibition of cancer cell invasion and motility: an overview. J Steroid Biochem Mol Biol 1998, 65:163-168. 10.1016/S0960-0760(98)00010-7, 9699869.
3. Platet N, Cunat S, Chalbos D, Rochefort H, Garcia M. Unliganded and liganded estrogen receptors protect against cancer invasion via different mechanisms. Mol Endocrinol Baltim Md 2000, 14:999-1009.
4. Kerdivel G, Flouriot G, Pakdel F. Modulation of estrogen receptor alpha activity and expression during breast cancer progression. Vitam Horm 2013, 93:135-160.
5. Platet N, Cathiard AM, Gleizes M, Garcia M. Estrogens and their receptors in breast cancer progression: a dual role in cancer proliferation and invasion. Crit Rev Oncol Hematol 2004, 51:55-67. 10.1016/j.critrevonc.2004.02.001, 15207254.
6. Kim JJ, Kurita T, Bulun SE. Progesterone action in endometrial cancer, endometriosis, uterine fibroids, and breast cancer. Endocr Rev 2013, 34:130-162. 10.1210/er.2012-1043, 3565104, 23303565.
7. Pegram MD, Konecny G, Slamon DJ. The molecular and cellular biology of HER2/neu gene amplification/overexpression and the clinical development of herceptin (trastuzumab) therapy for breast cancer. Cancer Treat Res 2000, 103:57-75. 10.1007/978-1-4757-3147-7_4, 10948442.
8. Métivier R, Gay FA, Hübner MR, Flouriot G, Salbert G, Gannon F, Kah O, Pakdel F. Formation of an hER$\alpha$-COUP-TFI complex enhances hER$\alpha$ AF-1 through Ser118 phosphorylation by MAPK. EMBO J 2002, 21:3443-3453. 10.1093/emboj/cdf344, 126093, 12093745.
9. Le Dily F, Métivier R, Guéguen M-M, Le Péron C, Flouriot G, Tas P, Pakdel F. COUP-TFI modulates estrogen signaling and influences proliferation, survival and migration of breast cancer cells. Breast Cancer Res Treat 2007, 110:69-83.
10. Park J-I, Tsai SY, Tsai M-J. Molecular mechanism of chicken ovalbumin upstream promoter-transcription factor (COUP-TF) actions. Keio J Med 2003, 52:174-181. 10.2302/kjm.52.174, 14529150.
11. Boudot A, Le Dily F, Pakdel F. Involvement of COUP-TFs in Cancer Progression. Cancers 2011, 3:700-715. 10.3390/cancers3010700, 3756385, 24212637.
12. Nagasaki S, Suzuki T, Miki Y, Akahira J, Shibata H, Ishida T, Ohuchi N, Sasano H. Chicken ovalbumin upstream promoter transcription factor II in human breast carcinoma: Possible regulator of lymphangiogenesis via vascular endothelial growth factor-C expression. Cancer Sci 2009, 100:639-645. 10.1111/j.1349-7006.2008.01078.x, 19154418.
13. Qin J, Wu S-P, Creighton CJ, Dai F, Xie X, Cheng C-M, Frolov A, Ayala G, Lin X, Feng X-H, Ittmann MM, Tsai S-J, Tsai M-J, Tsai SY. COUP-TFII inhibits TGF-β-induced growth barrier to promote prostate tumorigenesis. Nature 2013, 493:236-240. 4022346, 23201680.
14. Hawkins SM, Loomans HA, Wan YW, Ghosh-Choudhury T, Coffey D, Xiao W, Liu Z, Sangi-Haghpeykar H, Anderson ML. Expression of COUP-TFII in epithelial ovarian cancers. J Clin Endocrinol Metab 2013, 98:E1152-E1162. 10.1210/jc.2013-1081, 23690307.
15. Sun X, Cheng G, Hao M, Zheng J, Zhou X, Zhang J, Taichman RS, Pienta KJ, Wang J. CXCL12 / CXCR4 / CXCR7 chemokine axis and cancer progression. Cancer Metastasis Rev 2010, 29:709-722. 10.1007/s10555-010-9256-x, 3175097, 20839032.
16. Luker KE, Luker GD. Functions of CXCL12 and CXCR4 in breast cancer. Cancer Lett 2006, 238:30-41. 10.1016/j.canlet.2005.06.021, 16046252.
17. Müller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verástegui E, Zlotnik A. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410:50-56. 10.1038/35065016, 11242036.
18. Kang H, Watkins G, Parr C, Douglas-Jones A, Mansel RE, Jiang WG. Stromal cell derived factor-1: its influence on invasiveness and migration of breast cancer cells in vitro, and its association with prognosis and survival in human breast cancer. Breast Cancer Res 2005, 7:R402-R410. 10.1186/bcr1022, 1175055, 15987445.
19. Burger JA, Kipps TJ. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 2006, 107:1761-1767. 10.1182/blood-2005-08-3182, 16269611.
20. Wendt MK, Cooper AN, Dwinell MB. Epigenetic silencing of CXCL12 increases the metastatic potential of mammary carcinoma cells. Oncogene 2008, 27:1461-1471. 10.1038/sj.onc.1210751, 17724466.
21. Zhou W, Jiang Z, Liu N, Xu F, Wen P, Liu Y, Zhong W, Song X, Chang X, Zhang X, Wei G, Yu J. Down-regulation of CXCL12 mRNA expression by promoter hypermethylation and its association with metastatic progression in human breast carcinomas. J Cancer Res Clin Oncol 2009, 135:91-102. 10.1007/s00432-008-0435-x, 18670789.
22. Wendt MK, Johanesen PA, Kang-Decker N, Binion DG, Shah V, Dwinell MB. Silencing of epithelial CXCL12 expression by DNA hypermethylation promotes colonic carcinoma metastasis. Oncogene 2006, 25:4986-4997. 10.1038/sj.onc.1209505, 16568088.
23. Boudot A, Kerdivel G, Habauzit D, Eeckhoute J, Le Dily F, Flouriot G, Samson M, Pakdel F. Differential estrogen-regulation of CXCL12 chemokine receptors, CXCR4 and CXCR7, contributes to the growth effect of estrogens in breast cancer cells. PLoS One 2011, 6:e20898. 10.1371/journal.pone.0020898, 3112227, 21695171.
24. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3:RESEARCH0034. 126239, 12184808.
25. Eeckhoute J, Lupien M, Meyer CA, Verzi MP, Shivdasani RA, Liu XS, Brown M. Cell-type selective chromatin remodeling defines the active subset of FOXA1-bound enhancers. Genome Res 2008, 19:372-380.
26. Kishimoto H, Wang Z, Bhat-Nakshatri P, Chang D, Clarke R, Nakshatri H. The p160 family coactivators regulate breast cancer cell proliferation and invasion through autocrine/paracrine activity of SDF-1 (alpha)/CXCL12. Carcinogenesis 2005, 26:1706. 10.1093/carcin/bgi137, 15917309.
27. Moré E, Fellner T, Doppelmayr H, Hauser-Kronberger C, Dandachi N, Obrist P, Sandhofer F, Paulweber B. Activation of the MAP kinase pathway induces chicken ovalbumin upstream promoter-transcription factor II (COUP-TFII) expression in human breast cancer cell lines. J Endocrinol 2003, 176:83-94. 10.1677/joe.0.1760083, 12525252.
28. Nagy PL, Cleary ML, Brown PO, Lieb JD. Genomewide demarcation of RNA polymerase II transcription units revealed by physical fractionation of chromatin. Proc Natl Acad Sci U S A 2003, 100:6364-6369. 10.1073/pnas.1131966100, 164452, 12750471.
29. Petit FG, Métivier R, Valotaire Y, Pakdel F. Synergism between a half-site and an imperfect estrogen-responsive element, and cooperation with COUP-TFI are required for estrogen receptor (ER) to achieve a maximal estrogen-stimulation of rainbow trout ER gene. Eur J Biochem FEBS 1999, 259:385-395.
30. Rahimi M, George J, Tang C. EGFR variant-mediated invasion by enhanced CXCR4 expression through transcriptional and post-translational mechanisms. Int J Cancer Int Cancer 2010, 126:1850-1860.
31. Burbach JP, Lopes da Silva S, Cox JJ, Adan RA, Cooney AJ, Tsai MJ, Tsai SY. Repression of estrogen-dependent stimulation of the oxytocin gene by chicken ovalbumin upstream promoter transcription factor I. J Biol Chem 1994, 269:15046-15053.
32. Liu Y, Yang N, Teng CT. COUP-TF acts as a competitive repressor for estrogen receptor-mediated activation of the mouse lactoferrin gene. Mol Cell Biol 1993, 13:1836-1846. 359496, 8441416.
33. Lu X, Kang Y. Epidermal growth factor signalling and bone metastasis. Br J Cancer 2010, 102:457-461. 10.1038/sj.bjc.6605490, 2822931, 20010942.
34. Foley J, Nickerson NK, Nam S, Allen KT, Gilmore JL, Nephew KP, Riese DJ. EGFR signaling in breast cancer: bad to the bone. Semin Cell Dev Biol 2010, 21:951-960. 10.1016/j.semcdb.2010.08.009, 2991402, 20813200.
35. Nakayama T, Mutsuga N, Tosato G. FGF2 posttranscriptionally down-regulates expression of SDF1 in bone marrow stromal cells through FGFR1 IIIc. Blood 2007, 109:1363-1372. 10.1182/blood-2006-06-028217, 1794071, 17077327.
36. Nakayama T, Mutsuga N, Tosato G. Effect of fibroblast growth factor 2 on stromal cell-derived factor 1 production by bone marrow stromal cells and hematopoiesis. J Natl Cancer Inst 2007, 99:223-235. 10.1093/jnci/djk031, 17284717.
37. Wright N, de Lera TL, García-Moruja C, Lillo R, García-Sánchez F, Caruz A, Teixidó J. Transforming growth factor-beta1 down-regulates expression of chemokine stromal cell-derived factor-1: functional consequences in cell migration and adhesion. Blood 2003, 102:1978-1984. 10.1182/blood-2002-10-3190, 12775566.
38. Grandis JR, Sok JC. Signaling through the epidermal growth factor receptor during the development of malignancy. Pharmacol Ther 2004, 102:37-46. 10.1016/j.pharmthera.2004.01.002, 15056497.
39. Uchida D, Onoue T, Kuribayashi N, Tomizuka Y, Tamatani T, Nagai H, Miyamoto Y. Blockade of CXCR4 in oral squamous cell carcinoma inhibits lymph node metastases. Eur J Cancer Oxf Engl 1990 2011, 47:452-459.
40. Chen G, Wang Z, Liu X, Liu F. High-level CXCR4 expression correlates with brain-specific metastasis of non-small cell lung cancer. World J Surg 2011, 35:56-61. 10.1007/s00268-010-0784-x, 21046385.
41. Furusato B, Mohamed A, Uhlén M, Rhim JS. CXCR4 and cancer. Pathol Int 2010, 60:497-505. 10.1111/j.1440-1827.2010.02548.x, 20594270.
42. Zabel BA, Wang Y, Lewén S, Berahovich RD, Penfold MET, Zhang P, Powers J, Summers BC, Miao Z, Zhao B, Jalili A, Janowska-Wieczorek A, Jaen JC, Schall TJ. Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. J Immunol Baltim Md 1950 2009, 183:3204-3211.
43. Christopher MJ, Liu F, Hilton MJ, Long F, Link DC. Suppression of CXCL12 production by bone marrow osteoblasts is a common and critical pathway for cytokine-induced mobilization. Blood 2009, 114:1331-1339. 10.1182/blood-2008-10-184754, 2727413, 19141863.
44. Calonge MJ, Seoane J, Massagué J. Opposite Smad and chicken ovalbumin upstream promoter transcription factor inputs in the regulation of the collagen VII gene promoter by transforming growth factor-beta. J Biol Chem 2004, 279:23759-23765. 10.1074/jbc.M402178200, 15047696.
45. Connor H, Nornes H, Neuman T. Expression screening reveals an orphan receptor chick ovalbumin upstream promoter transcription factor I as a regulator of neurite/substrate-cell contacts and cell aggregation. J Biol Chem 1995, 270:15066-15070. 10.1074/jbc.270.25.15066, 7797489.
46. Pradet-Balade B, Boulmé F, Beug H, Müllner EW, Garcia-Sanz JA. Translation control: bridging the gap between genomics and proteomics?. Trends Biochem Sci 2001, 26:225-229. 10.1016/S0968-0004(00)01776-X, 11295554.