Suppression of tumor cell invasion by cyclooxygenase inhibitors is mediated by thrombospondin-1 via the early growth response gene Egr-1

Molecular Cancer Therapeutics

Volumn 4, Issue 10, 2005, Pages 1551-1558

  Moon, Yuseok ^a   Bottone Jr , Frank G ^a   McEntee, Michael F ^b   Eling, Thomas E ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 (4 CHLOROPHENYL) 1 (4 METHOXYPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOLE; 5 (4 FLUOROPHENYL) 1 [(4 METHYLSULFONYL)PHENYL] 3 TRIFLUOROMETHYLPYRAZOLE; ACETYLSALICYLIC ACID; EARLY GROWTH RESPONSE FACTOR 1; IBUPROFEN; INDOMETACIN; MATRIGEL; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; NONSTEROID ANTIINFLAMMATORY AGENT; PROSTAGLANDIN SYNTHASE INHIBITOR; PROTEIN ANTIBODY; SMALL INTERFERING RNA; SULINDAC SULFIDE; THROMBOSPONDIN 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CONTROLLED STUDY; DRUG MECHANISM; GENE CONTROL; GENE OVEREXPRESSION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG ADENOCARCINOMA; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL; UPREGULATION;

ADENOCARCINOMA; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; CYCLOOXYGENASE INHIBITORS; EARLY GROWTH RESPONSE PROTEIN 1; GENES, TUMOR SUPPRESSOR; HUMANS; INDOMETHACIN; LUNG NEOPLASMS; MICE; NEOPLASM INVASIVENESS; RNA, MESSENGER; RNA, SMALL INTERFERING; SULINDAC; THROMBOSPONDIN 1;

EID: 27644525709     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-05-0213     Document Type: Article

References (52)

1. Thun MJ, Henley SJ, Patrono C. Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues. J Natl Cancer Inst 2002;94:252-66.
2. Gwyn K, Sinicrope FA. Chemoprevention of colorectal cancer. Am J Gastroenterol 2002;97:13-21.
3. Reddy BS, Rao CV, Seibert K. Evaluation of cyclooxygenase-2 inhibitor for potential chemopreventive properties in colon carcinogenesis. Cancer Res 1996;56:4566-9.
4. Rao CV, Rivenson A, Simi B, et al. Chemoprevention of colon carcinogenesis by sulindac, a nonsteroidal anti-inflammatory agent. Cancer Res 1995;55:1464-72.
5. Peluffo GD, Stillitani I, Rodriguez VA, Diament MJ, Klein SM. Reduction of tumor progression and paraneoplastic syndrome development in murine lung adenocarcinoma by nonsteroidal antiinflammatory drugs. Int J Cancer 2004;110:825-30.
6. Wei D, Wang L, He Y, Xiong HQ, Abbruzzese JL, Xie K. Celecoxib inhibits vascular endothelial growth factor expression in and reduces angiogenesis and metastasis of human pancreatic cancer via suppression of Sp1 transcription factor activity. Cancer Res 2004;64:2030-8.
7. Yao M, Lam EC, Kelly CR, Zhou W, Wolfe MM. Cyclooxygenase-2 selective inhibition with NS-398 suppresses proliferation and invasiveness and delays liver metastasis in colorectal cancer. Br J Cancer 2004;90: 712-9.
8. Connolly EM, Harmey JH, O'Grady T, et al. Cyclo-oxygenase inhibition reduces tumour growth and metastasis in an orthotopic model of breast cancer. Br J Cancer 2002;87:231-7.
9. Masferrer J. Approach to angiogenesis inhibition based on cyclooxygenase-2. Cancer J 2001;7 Suppl 3:S144-50.
10. Yoshida S, Amano H, Hayashi I, et al. COX-2/VEGF-dependent facilitation of tumor-associated angiogenesis and tumor growth in vivo. Lab Invest 2003;83:1385-94.
11. Tegeder I, Pfeilschifter J, Geisslinger G. Cyclooxygenase-independent actions of cyclooxygenase inhibitors. FASEB J 2001;15:2057-72.
12. Zhang X, Morham SG, Langenbach R, Young DA. Malignant transformation and antineoplastic actions of nonsteroidal antiinflammatory drugs (NSAIDs) on cyclooxygenase-null embryo fibroblasts. J Exp Med 1999;190:451-9.
13. Baek SJ, Kim JS, Moore SM, Lee SH, Martinez J, Eling TE. Cyclooxygenase inhibitors induce the expression of the tumor suppressor gene EGR-1, which results in the up-regulation of NAG-1, an antitumorigenic protein. Mol Pharmacol 2005;67:356-64.
14. Baek SJ, Kim JS, Nixon JB, DiAugustine RP, Eling TE. Expression of NAG-1, a transforming growth factor-β superfamily member, by troglitazone requires the early growth response gene EGR-1. J Biol Chem 2004; 279:6883-92.
15. Baek SJ, Wilson LC, Hsi LC, Eling TE. Troglitazone, a peroxisome proliferator-activated receptor γ (PPAR γ) ligand, selectively induces the early growth response-1 gene independently of PPAR γ. A novel mechanism for its anti-tumorigenic activity. J Biol Chem 2003;278: 5845-53.
16. Bottone FG, Jr., Moon Y, Alston-Mills B, Eling TE. Transcriptional regulation of activating transcription factor 3 (ATF3) involves early growth response-1 (Egr-1) gene. J Pharmacol Exp Ther. Epub 2005 Aug 3.
17. Bottone FG, Jr., Moon Y, Kim JS, Alston-Mills B, Ishibashi M, Eling TE. The anti-invasive activity of cyclooxygenase inhibitors is regulated by the transcription factor ATF3 (activating transcription factor 3). Mol Cancer Ther 2005;4:693-703.
18. Quinones A, Dobberstein KU, Rainov NG. The egr-1 gene is induced by DNA-damaging agents and non-genotoxic drugs in both normal and neoplastic human cells. Life Sci 2003;72:2975-92.
19. Thiel G, Cibelli G. Regulation of life and death by the zinc finger transcription factor Egr-1. J Cell Physiol 2002;193:287-92.
20. Huang RP, Liu C, Fan Y, Mercola D, Adamson ED. Egr-1 negatively regulates human tumor cell growth via the DNA-binding domain. Cancer Res 1995;55:5054-62.
21. Liu C, Adamson E, Mercola D. Transcription factor EGR-1 suppresses the growth and transformation of human HT-1080 fibrosarcoma cells by induction of transforming growth factor β 1. Proc Natl Acad Sci U S A 1996;93:11831-6.
22. Liu C, Rangnekar VM, Adamson E, Mercola D. Suppression of growth and transformation and induction of apoptosis by EGR-1. Cancer Gene Ther 1998;5:3-28.
23. Liu C, Yao J, Mercola D, Adamson E. The transcription factor EGR-1 directly transactivates the fibronectin gene and enhances attachment of human glioblastoma cell line U251. J Biol Chem 2000;275: 20315-23.
24. Muthukkumar S, Han SS, Rangnekar VM, Bondada S. Role of Egr-1 gene expression in B cell receptor-induced apoptosis in an immature B cell lymphoma. J Biol Chem 1997;272:27987-93.
25. Muthukkumar S, Nair P, Sells SF, Maddiwar NG, Jacob RJ, Rangnekar VM. Role of EGR-1 in thapsigargin-inducible apoptosis in the melanoma cell line A375-C6. Mol Cell Biol 1995;15:6262-72.
26. Nair P, Muthukkumar S, Sells SF, Han SS, Sukhatme VP, Rangnekar VM. Early growth response-1-dependent apoptosis is mediated by p53. J Biol Chem 1997;272:20131-8.
27. Shin SY, Ko J, Chang JS, et al. Negative regulatory role of overexpression of PLC γ 1 in the expression of early growth response 1 gene in rat 3Y1 fibroblasts. FASEB J 2002;16:1504-14.
28. Shingu T, Bornstein P. Overlapping Egr-1 and Sp1 sites function in the regulation of transcription of the mouse thrombospondin 1 gene. J Biol Chem 1994;269:32551-7.
29. Castle VP, Dixit VM, Polverini PJ. Thrombospondin-1 suppresses tumorigenesis and angiogenesis in serum- and anchorage-independent NIH 3T3 cells. Lab Invest 1997;77:51-61.
30. Gutierrez LS, Suckow M, Lawler J, Ploplis VA, Castellino FJ. Thrombospondin 1: a regulator of adenoma growth and carcinoma progression in the APC(Min/+) mouse model. Carcinogenesis 2003;24: 199-207.
31. Weinstat-Saslow DL, Zabrenetzky VS, VanHoutte K, Frazier WA, Roberts DD, Steeg PS. Transfection of thrombospondin 1 complementary DNA into a human breast carcinoma cell line reduces primary tumor growth, metastatic potential, and angiogenesis. Cancer Res 1994;54: 6504-11.
32. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 2000;6:41-8.
33. Lawler J, Miao WM, Duquette M, Bouck N, Bronson RT, Hynes RO. Thrombospondin-1 gene expression affects survival and tumor spectrum of p53-deficient mice. Am J Pathol 2001;159:1949-56.
34. de Fraipont F, Nicholson AC, Feige JJ, Van Meir EG. Thrombospondins and tumor angiogenesis. Trends Mol Med 2001;7: 401-7.
35. Lawler J. Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J Cell Mol Med 2002;6:1-12.
36. Yao L, Zhao YL, Itoh S, Wada S, Yue L, Furuta I. Thrombospondin-1 expression in oral squamous cell carcinomas: correlations with tumor vascularity, clinicopathological features and survival. Oral Oncol 2000;36: 539-44.
37. Chiu CH, McEntee MF, Whelan J. Sulindac causes rapid regression of preexisting tumors in Min/+ mice independent of prostaglandin biosynthesis. Cancer Res 1997;57:4267-73.
38. Bottone FG, Jr., Martinez JM, Collins JB, Afshari CA, Eling TE. Gene modulation by the cyclooxygenase inhibitor, sulindac sulfide, in human colorectal carcinoma cells: possible link to apoptosis. J Biol Chem 2003; 278:25790-801.
39. McEntee MF, Chiu CH, Whelan J. Relationship of β-catenin and Bcl-2 expression to sulindac-induced regression of intestinal tumors in Min mice. Carcinogenesis 1999;20:635-40.
40. Huang WC, Chan ST, Yang TL, Tzeng CC, Chen CC. Inhibition of ICAM-1 gene expression, monocyte adhesion and cancer cell invasion by targeting IKK complex: molecular and functional study of novel α-methylene-γ-butyrolactone derivatives. Carcinogenesis 2004; 25:1925-34.
41. Niki T, Kohno T, Iba S, et al. Frequent co-localization of Cox-2 and laminin-5 γ2 chain at the invasive front of early-stage lung adenocarcinomas. Am J Pathol 2002;160:1129-41.
42. American Society of Health-System Pharmacists. AHFS drug information. Bethesda (MD): Published by authority of the Board of Directors of the American Society of Hospital Pharmacists; 2003:x.
43. Liu C, Yao J, de Belle I, Huang RP, Adamson E, Mercola D. The transcription factor EGR-1 suppresses transformation of human fibrosarcoma HT1080 cells by coordinated induction of transforming growth factor-β1, fibronectin, and plasminogen activator inhibitor-1. J Biol Chem 1999;274:4400-11.
44. Albo D, Arnoletti JP, Castiglioni A, et al. Thrombospondin (TSP) and transforming growth factor β 1 (TGF-β) promote human A549 lung carcinoma cell plasminogen activator inhibitor type 1 (PAI-1) production and stimulate tumor cell attachment in vitro. Biochem Biophys Res Commun 1994;203:857-65.
45. Tarnawski AS, Jones MK. Inhibition of angiogenesis by NSAIDs: molecular mechanisms and clinical implications. J Mol Med 2003;81: 627-36.
46. Winde G, Gumbinger HG, Osswald H, Kemper F, Bunte H. The NSAID sulindac reverses rectal adenomas in colectomized patients with familial adenomatous polyposis: clinical results of a dose-finding study on rectal sulindac administration. Int J Colorectal Dis 1993;8:13-7.
47. Yamaguchi M, Sugio K, Ondo K, Yano T, Sugimachi K. Reduced expression of thrombospondin-1 correlates with a poor prognosis in patients with non-small cell lung cancer. Lung Cancer 2002;36:143-50.
48. Watnick RS, Cheng YN, Rangarajan A, Ince TA, Weinberg RA. Ras modulates Myc activity to repress thrombospondin-1 expression and increase tumor angiogenesis. Cancer Cell 2003;3:219-31.
49. Yang QW, Liu S, Tian Y, et al. Methylation-associated silencing of the thrombospondin-1 gene in human neuroblastoma. Cancer Res 2003;63: 6299-310.
50. Friedl P, Vischer P, Freyberg MA. The role of thrombospondin-1 in apoptosis: Cell Mol Life Sci 2002;59:1347-57.
51. Rodriguez-Manzaneque JC, Lane TF, Ortega MA, Hynes RO, Lawler J, Iruela-Arispe ML. Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proc Natl Acad Sci U S A 2001;98:12485-90.
52. Liu G, Shuman MA, Cohen RL. Co-expression of urokinase, urokinase receptor and PAI-1 is necessary for optimum invasiveness of cultured lung cancer cells. Int J Cancer 1995;60:501-6.