NFAT3 transcription factor inhibits breast cancer cell motility by targeting the Lipocalin 2 gene

Oncogene

Volumn 29, Issue 15, 2010, Pages 2292-2301

  Fougere M ^a   Gaudineau, B ^a   Barbier, J ^a   Guaddachi, F ^a   Feugeas, J P ^a   Auboeuf, D ^a   Jauliac, S ^a  

^a SAINT LOUIS HOSPITAL   (France)

Author keywords

Breast; Estrogen receptor a; LCN2; Motility; NFAT3

Indexed keywords

ESTROGEN RECEPTOR ALPHA; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; TRANSCRIPTION FACTOR NFAT3;

ARTICLE; BREAST CARCINOMA; CANCER INVASION; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; GENE; GENE TARGETING; HUMAN; HUMAN CELL; LIPOCALIN 2 GENE; METASTASIS POTENTIAL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ACTINS; ACUTE-PHASE PROTEINS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; ESTROGEN RECEPTOR ALPHA; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIPOCALINS; NEOPLASM INVASIVENESS; NFATC TRANSCRIPTION FACTORS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS;

EID: 77951028117     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.499     Document Type: Article

References (47)

1. Ayers M, Symmans WF, Stec J, Damokosh AI, Clark E, Hess K et al. (2004). Gene expression profiles predict complete pathologic response to neoadjuvant paclitaxel and fluorouracil, doxorubicin, and cyclophosphamide chemotherapy in breast cancer. J Clin Oncol 22: 2284-2293. (Pubitemid 41115384)
2. Baksh S, Widlund HR, Frazer-Abel AA, Du J, Fosmire S, Fisher DE et al. (2002). NFATc2-mediated repression of cyclin-dependent kinase 4 expression. Mol Cell 10: 1071-1081.
3. Bauer M, Eickhoff JC, Gould MN, Mundhenke C, Maass N, Friedl A. (2008). Neutrophil gelatinase-associated lipocalin (NGAL) is a predictor of poor prognosis in human primary breast cancer. Breast Cancer Res Treat 108: 389-397.
4. Benedito AB, Lehtinen M, Massol R, Lopes UG, Kirchhausen T, Rao A et al. (2005). The transcription factor NFAT3 mediates neuronal survival. J Biol Chem 280: 2818-2825.
5. Bertheau P, Turpin E, Rickman DS, Espie M, de Reynies A, Feugeas JP et al. (2007). Exquisite sensitivity of TP53 mutant and basal breast cancers to a dose-dense epirubicin-cyclophosphamide regimen. PLoS Med 4: e90.
6. Buchholz M, Schatz A, Wagner M, Michl P, Linhart T, Adler G et al. (2006). Overexpression of c-myc in pancreatic cancer caused by ectopic activation of NFATc1 and the Ca2+/calcineurin signaling pathway. EMBO J 25: 3714-3724.
7. Chuvpilo S, Jankevics E, Tyrsin D, Akimzhanov A, Moroz D, Jha MK et al. (2002). Autoregulation of NFATc1/A expression facilitates effector T cells to escape from rapid apoptosis. Immunity 16: 881-895.
8. Devireddy LR, Teodoro JG, Richard FA, Green MR. (2001). Induction of apoptosis by a secreted lipocalin that is transcription-ally regulated by IL-3 deprivation. Science 293: 829-834.
9. Dutertre M, Smith CL. (2003). Ligand-independent interactions of p160/Steroid Receptor Coactivators And CREB-binding protein (CBP) w. Mol Endocrinol 17: 1296-1314.
10. Ellison G, Klinowska T, Westwood RF, Docter E, French T, Fox JC. (2002). Further evidence to support the melanocytic origin of MDA-MB-435. Mol Pathol 55: 294-299.
11. Flower DR. (1996). The lipocalin protein family: structure and function. Biochem J 318(Part 1): 1-14.
12. Fowler AM, Solodin N, Preisler-Mashek MT, Zhang P, Lee AV, Alarid ET. (2004). Increases in estrogen receptor-\{alpha\} con-centrati. FASEB J 18: 81-93.
13. Friedl A, Stoesz SP, Buckley P, Gould MN. (1999). Neutrophil gelatinase-associated lipocalin in normal and neoplastic human tissues cell type-specific pattern of expression. Histochem J 31: 433-441.
14. Friedl P, Wolf K. (2003). Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3: 362-374.
15. Furutani M, Arii S, Mizumoto M, Kato M, Imamura M. (1998). Identification of a neutrophil gelatinase-associated lipocalin mRNA in human pancreatic cancers using a modified signal sequence trap method. Cancer Lett 122: 209-214.
16. Gruvberger S, Ringner M, Chen Y, Panavally S, Saal LH, Borg A et al. (2001). Estrogen receptor status in breast cancer is associated with remarkably distinct gene expression patterns. Cancer Res 61: 5979-5984.
17. Gwira JA, Wei F, Ishibe S, Ueland JM, Barasch J, Cantley LG. (2005). Expression of neutrophil gelatinase-associated lipocalin regulates epithelial morphogenesis in vitro. J Biol Chem 280: 7875-7882.
18. Hill-Eubanks DC, Gomez MF, Stevenson AS, Nelson MT. (2003). NFAT regulation in smooth muscle. Trends Cardiovasc Med 13: 56-62.
19. Ho IC, Kim JH, Rooney JW, Spiegelman BM, Glimcher LH. (1998). A potential role for the nuclear factor of activated T cells family of transcriptional regulatory proteins in adipogenesis. Proc Natl Acad Sci USA 95: 15537-15541.
20. Holzmann K, Kohlhammer H, Schwaenen C, Wessendorf S, Kestler HA, Schwoerer A et al. (2004). Genomic DNA-chip hybridization reveals a higher incidence of genomic amplifications in pancreatic cancer than conventional comparative genomic hybridization and leads to the identification of novel candidate genes. Cancer Res 64: 4428-4433.
21. Irie HY, Pearline RV, Grueneberg D, Hsia M, Ravichandran P, Kothari N et al. (2005). Distinct roles of Akt1 and Akt2 in regulating cell migration and epithelial-mesenchymal transition. J Cell Biol 171: 1023-1034.
22. Jauliac S, Lopez-Rodriguez C, Shaw LM, Brown LF, Rao A, Toker A. (2002). The role of NFAT transcription factors in integrin-mediated carcinoma invasion. Nat Cell Biol 4: 540-544.
23. Krueger JS, Keshamouni VG, Atanaskova N, Reddy KB. (2001). Temporal and quantitative regulation of mitogen-activated protein kinase (MAPK) modulates cell motility and invasion. Oncogene 20: 4209-4218.
24. Leng X, Ding T, Lin H, Wang Y, Hu L, Hu J et al. (2009). Inhibition of lipocalin 2 impairs breast tumorigenesis and metastasis. Cancer Res 69: 8579-8584.
25. Leng X, Lin H, Ding T, Wang Y, Wu Y, Klumpp S et al. (2008). Lipocalin 2 is required for BCR-ABL-induced tumorigenesis. Oncogene 27: 6110-6119.
26. Li CI, Malone KE, Weiss NS, Daling JR. (2001). Tamoxifen therapy for primary breast cancer and risk of contralateral breast cancer. J Natl Cancer Inst 93: 1008-1013.
27. Lim R, Ahmed N, Borregaard N, Riley C, Wafai R, Thompson EW et al. (2007). Neutrophil gelatinase-associated lipocalin (NGAL) an early-screening biomarker for ovarian cancer: NGAL is associated with epidermal growth factor-induced epithelio-mesenchymal transition. Int J Cancer 120: 2426-2434.
28. Lopez-Rodriguez C, Aramburu J, Rakeman AS, Rao A. (1999). NFAT5, a constitutively nuclear NFAT protein that does not cooperate with Fos and Jun. Proc Natl Acad Sci USA 96: 7214-7219.
29. Mancini M, Toker A. (2009). NFAT proteins: emerging roles in cancer progression. Nat Rev Cancer 9: 810-820.
30. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J et al. (1998). A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93: 215-228. (Pubitemid 28180855)
31. Neal JW, Clipstone NA. (2003). A constitutively active NFATc1 mutant induces a transformed phenotype in 3T3-L1 fibroblasts. J Biol Chem 278: 17246-17254.
32. Nielsen BS, Borregaard N, Bundgaard JR, Timshel S, Sehested M, Kjeldsen L. (1996). Induction of NGAL synthesis in epithelial cells of human colorectal neoplasia and inflammatory bowel diseases. Gut 38: 414-420.
33. Platet N, Cunat S, Chalbos D, Rochefort H, Garcia M. (2000). Unliganded and liganded estrogen receptors protect against cancer invasion via different mechanisms. Mol Endocrinol 14: 999-1009.
34. Playford RJ, Belo A, Poulsom R, Fitzgerald AJ, Harris K, Pawluczyk I et al. (2006). Effects of mouse and human lipocalin homologues 24p3/lcn2 and neutrophil gelatinase-associated lipocalin on gastrointestinal mucosal integrity and repair. Gastroenterology 131: 809-817.
35. Price JE, Polyzos A, Zhang RD, Daniels LM. (1990). Tumorigenicity and metastasis of human breast carcinoma cell lines in nude mice. Cancer Res 50: 717-721.
36. Provatopoulou X, Gounaris A, Kalogera E, Zagouri F, Flessas I, Goussetis E et al. (2009). Circulating levels of matrix metallopro-teinase-9 (MMP-9), neutrophil gelatinase-associated lipocalin (NGAL) and their compex MMP-9/NGAL in breast cancer disease. BMC Cancer 9: 390.
37. Qin X, Wang XH, Yang ZH, Ding LH, Xu XJ, Cheng L et al. (2008). Repression of NFAT3 transcriptional activity by estrogen receptors. Cell Mol Life Sci 65: 2752-2762.
38. Ranger AM, Gerstenfeld LC, Wang J, Kon T, Bae H, Gravallese EM et al. (2000). The nuclear factor of activated T cells (NFAT) transcription factor NFATp (NFATc2) is a repressor of chondro-genesis. J Exp Med 191: 9-22.
39. Shaw JP, Utz PJ, Durand DB, Toole JJ, Emmel EA, Crabtree GR. (1988). Identification of a putative regulator of early T cell activation genes. Science 241: 202-205.
40. Shi H, Gu Y, Yang J, Xu L, Mi W, Yu W. (2008). Lipocalin 2 promotes lung metastasis of murine breast cancer cells. J Exp Clin Cancer Res 27: 83.
41. Stoesz SP, Friedl A, Haag JD, Lindstrom MJ, Clark GM, Gould MN. (1998). Heterogeneous expression of the lipocalin NGAL in primary breast cancers. Int J Cancer 79: 565-572.
42. Thompson EW, Reich R, Shima TB, Albini A, Graf J, Martin GR et al. (1988). Differential regulation of growth and invasiveness of MCF-7 breast cancer cells by antiestrogens. Cancer Res 48: 6764-6768.
43. Xanthoudakis S, Viola JP, Shaw KT, Luo C, Wallace JD, Bozza PT et al. (1996). An enhanced immune response in mice lacking the transcription factor NFAT1. Science 272: 892-895.
44. Yang J, Bielenberg DR, Rodig SJ, Doiron R, Clifton MC, Kung AL et al. (2009). Lipocalin 2 promotes breast cancer progression. Proc Natl Acad Sci USA 106: 3913-3918.
45. Zhang H, Xie X, Zhu X, Zhu J, Hao C, Lu Q et al. (2005). Stimulatory cross-talk between NFAT3 and estrogen receptor in breast cancer cells. J Biol Chem 280: 43188-43197.
46. Zhang J, Wu Y, Zhang Y, LeRoith D, Bernlohr DA, Chen X. (2008). The role of lipocalin 2 in the regulation of inflammation in adipocytes and macrophages. Mol Endocrinol 22: 1416-1426.
47. Zhong L, Peng X, Hidalgo GE, Doherty DE, Stromberg AJ, Hirschowitz EA. (2004). Identification of circulating antibodies to tumor-associated proteins for combined use as markers of non-small cell lung cancer. Proteomics 4: 1216-1225. (Pubitemid 38445978)