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Advances in Brief |
Departments of Surgery [O. N. T., A. J. D., L. T., J. M. D., T. J. F.], Medicine [A. J. D., E. K. Y.], and Pathology [R. A. S.], New York Presbyterian Hospital and Weill Medical College of Cornell University, and Strang Cancer Prevention Center [A. J. D., F. Z., T. J. F.], New York, New York 10021; and Searle Discovery Research, Monsanto Company, St. Louis, Missouri 63017 [J. L. M., B. M. W., A. T. K.]
| ABSTRACT |
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| Introduction |
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25,000 new cases of pancreatic cancer are diagnosed annually (1)
. Pancreatic cancer now ranks fourth and fifth as a cause of cancer death in men and women, respectively, in the United States (1)
. Unfortunately, >90% of pancreatic cancer patients present with metastatic disease or advanced local disease, precluding a curative surgical resection. Chemotherapy has not resulted in a significant survival benefit, and the 5-year survival rate is <1.3% in the United States (1)
, with a median survival of 4.1 months. On the basis of these observations, it is clear that new molecular targets are needed for the prevention and treatment of pancreatic cancer. Results from recent studies have established the presence of two distinct COX3 enzymes, a constitutive enzyme (COX-1) and an inducible form (COX-2). COXs catalyze the formation of prostaglandins from arachidonic acid. COX-1 is thought to be a housekeeping gene with essentially constant levels of expression, whereas COX-2 is an early response gene that, like c-jun and c-fos, is induced rapidly by growth factors, tumor promoters, oncogenes, and carcinogens (2) .
Multiple lines of evidence suggest that COX-2 is important in carcinogenesis. For example, COX-2 is up-regulated in transformed cells (3)
and in various forms of cancer (4, 5, 6, 7)
, whereas levels of COX-1 are relatively constant. Moreover, a null mutation for COX-2 caused a marked reduction in the number and size of intestinal polyps in APC
716 mice, a murine model of familial adenomatous polyposis (8)
. COX-2 knockout mice also developed
75% fewer chemically induced skin papillomas than control mice (9)
. In addition to the genetic evidence implicating COX-2 in carcinogenesis, newly developed selective inhibitors of COX-2 protect against gastrointestinal tumor formation (8
, 10)
. Here, we investigated whether COX-2 was up-regulated in pancreatic cancer. Our data show that levels of COX-2 are increased in adenocarcinoma of the pancreas and raise the possibility that selective inhibitors of COX-2 may be useful in the prevention or treatment of this disease.
| Materials and Methods |
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Patient Samples.
Biopsy specimens were obtained at the time of surgery from 10 patients with adenocarcinoma of the exocrine pancreas. Tissue samples were taken from a nonnecrotic area of the tumor and from adjacent nontumorous tissue; samples were immediately frozen in liquid nitrogen and subsequently stored at -80°C. Informed consent was obtained from each patient. The study was approved by the Committee on Human Rights in Research at Weill Medical College of Cornell University.
Tissue Culture.
Three human pancreatic adenocarcinoma cell lines (Su 86.86, BxPC-3, and Panc-1) were obtained from American Type Culture Collection (Manassas, VA). The Su 86.86 and BxPC-3 cell lines were maintained in RPMI 1640; the Panc-1 cell line was maintained in DMEM supplemented with 10% FCS, 100 units/ml penicillin, and 100 µg/ml streptomycin. Cells were plated for experimental use in complete medium and allowed to attach and grow for 48 h in a 5% CO2/water-saturated incubator at 37°C. The medium was then replaced with serum-free medium. Twenty-four h later, cells were treated with vehicle or PMA under serum-free conditions.
Western Blotting.
Frozen tissue was thawed in ice-cold homogenization buffer containing 150 mM NaCl, 100 mM Tris-buffered saline (pH 8), 1% Tween 20, 50 mM diethyldithiocarbamate, 1 mM EDTA, 1 mM phenylmethylsulfonyl fluoride, 10 µg/ml leupeptin, 10 µg/ml aprotinin, 10 µg/ml trypsin-chymotrypsin inhibitor, and 10 µg/ml pepstatin. Tissues were homogenized using a glass-on-glass tissue homogenizer. Homogenates were centrifuged at 11,750 x g for 10 min at 4°C to remove the particulate material.
Cellular lysates were prepared by treating cells with the same lysis buffer that was used for the tissue samples. Lysates were sonicated for 20 s on ice and centrifuged at 11,750 x g for 10 min to sediment the particulate material. The protein concentration of the supernatant was measured using the Lowry protein assay kit. Immunoblot analysis for COX-2 was performed as in previous studies (11) .
Construction of a COX-2 Competitor Template Containing a nt Deletion.
A competitive RT-PCR deletion construct (mimic) for COX-2 was synthesized using a mutant sense primer (nt 932955 attached to nt 11111130; 5'-GGTCTGGTGCCTGGTCTGATGATGGAGTGGCTATCACTTCAAAC-3') and an antisense primer (nt 16341655; 5'-GTCCTTTCAAGGAGAATGGTGC-3'), producing a 569-bp PCR product. The mutant sense primer contains the primer-binding sequence of endogenous target (from nt 932 to 955) attached to the end of an intervening DNA sequence (a 156-bp deletion from nt 956 to nt 1110). Thus, the mimic DNA has primer binding sequences that are identical to the target cDNA. The 569-bp mimic was further amplified using the sense primer (5'-GGTCTGGTGCCTGGTCTGATGATG-3') and the antisense primer (5'-GTCCTTTCAAGGAGAATGGTGC-3') in a reaction mixture containing 10 mM Tris-HCl (pH 8.3), 50 mM KCl, 2 mM MgCl2, 0.2 mM dNTP, 2.5 units of AmpiTaq DNA polymerase, and 400 nM primers for 35 cycles consisting of denaturation at 94°C for 20 s, annealing at 60°C for 20 s, and extension at 72°C for 30 s in a Perkin Elmer 2400 thermal cycler. The PCR products were electrophoresed on 1% agarose gels and gel-purified using GenElute Agarose Spin Columns according to the manufacturers protocol.
RNA Isolation and Reverse Transcription.
Total RNA was isolated from pancreatic tissue (
50 mg) and cell monolayers using an RNeasy Mini Kits from Qiagen. One µg of total RNA was reverse-transcribed using the GeneAmp RNA PCR kit according to the manufacturers protocol.
Quantitative PCR for COX-2 in Human Pancreatic Tissue.
Each PCR was carried out in 25 µl of a reaction mix, containing 10 mM Tris-HCl (pH 8.3), 50 mM KCl, 2 mM MgCl2, 0.2 mM dNTP, 2.5 units of Amplitaq DNA polymerase, and 400 nM primers (sense primer, 5'-GGTCTGGTGCCTGGTCTGATGATG-3'; antisense primer, 5'-GTCCTTTCAAGGAGAATGGTGC-3'). Five-µl aliquots of the reverse-transcribed cDNA samples and various known amounts of COX-2 mimic (between 0.0001 and 0.05 pg), adjusted to the abundance of the target cDNA, were added to the reaction mix and coamplified for 35 cycles: denaturation at 94°C for 20 s, annealing at 65°C for 20 s, extension at 72°C for 90 s, and final extension at 72°C for 10 min. Ten µl of PCR products, 724-bp fragments from endogenous target cDNA, and 569-bp fragments from mimic COX-2 were then separated by electrophoresis on 1% agarose gels and visualized by ethidium bromide staining.
Semiquantitative PCR for COX-2 and ß2-microglobulin in Pancreatic Cell Lines.
The semiquantitative analysis for COX-2 was performed using the same COX-2 primers as listed above in a 25-µl reaction mixture containing 5-µl aliquots of reverse transcribed cDNA samples, 10 mM Tris-HCl (pH 8.3), 50 mM KCl, 2 mM MgCl2, 0.2 mM dNTP, 2.5 units of AmpliTaq DNA polymerase, and 400 nM primers for 35 cycles consisting of denaturation at 94°C for 20 s, annealing at 65°C for 20 s, extension at 72°C for 30 s, and final extension at 72°C for 10 min. A constitutively expressed gene, ß2-microglobulin, was used as an internal control, generating a 266-bp PCR product. The primers for ß2-microglobulin (from nt 75 to nt 340) were 5'-AGCAGAGAATGGAAAGTCAAA-3' (sense) and 5'-ATGCTGCTTACATGTCTCGAT-3' (antisense). The PCR conditions for ß2-microglobulin were identical to that for COX-2, except for annealing at 55°C for 20 s.
Immunohistochemistry.
Tissues from 10 patients with adenocarcinoma of the pancreas were fixed in formalin, embedded in paraffin, cut into 4-µm sections and mounted onto polylysine-coated slides. Sections were dewaxed in xylene, rehydrated in descending alcohols, and blocked for endogenous peroxidase (3% H2O2 in MeOH) and avidin/biotin (Vector Blocking Kit). The sections were permeabilized in TNB-BB [0.1 M Tris (pH 7.5), 0.15 M NaCl, 0.5% blocking agent, 0.3% Triton X-100, and 0.2% saponin) and incubated in primary antibody overnight at 4°C. The polyclonal antiserum to COX-2 (PG-27; Oxford Biomedical Research Inc.) was used at a 1:500 dilution in TNB-BB. Control sections were incubated with antisera in the presence of a 100-fold excess of human recombinant COX-2 protein or with isotype-matched IgG normal rabbit serum. Immunoreactive complexes were detected using tyramide signal and amplification (TSA-indirect) and visualized with the peroxidase substrate, AEC. Slides were then counter stained in aqueous hematoxylin, mounted in crystal mount, and coverslipped in 50:50 xylene/Permount.
Statistical Analysis.
Results were analyzed by the Wilcoxon signed rank test. A difference between groups of P < 0.05 was considered significant.
| Results |
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| Discussion |
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COX-2 can potentially predispose to carcinogenesis via multiple mechanisms. In extrahepatic tissues in which cytochrome P450 content is low, COX may be important for metabolism of carcinogens. For example, several classes of chemical carcinogens, e.g., dihydrodiol derivatives of polycyclic aromatic hydrocarbons, aromatic amines, and heterocyclic amines, are activated to mutagenic derivatives by COX (12) . The metabolism of carcinogens by COX-2 may be important, therefore, for understanding the link between cigarette smoking (1) or consumption of grilled or fried meat (1) and pancreatic cancer. Additionally, enhanced synthesis of prostaglandins, a consequence of up-regulation of COX-2, favors the growth of malignant cells by increasing cell proliferation (13) , promoting angiogenesis (14) , and inhibiting immune surveillance (15) . In intestinal epithelial cells, overexpression of COX-2 inhibits apoptosis (16) and increases the invasiveness of malignant cells (17) . Additional studies are needed to determine which of these mechanisms are important in adenocarcinoma of the pancreas.
It also is interesting to consider the possible link between the known genetic alterations in pancreatic cancer and COX-2. Mutations in the Ki-ras oncogene (18) are common in pancreatic cancer. Levels of COX-2 are increased in Ras-transformed epithelial cells (3 , 19) . It is reasonable to postulate, therefore, that activation of the Ras pathway contributes to the up-regulation of COX-2 in pancreatic cancer. Mutations of the Apc gene also occur in pancreatic cancer (20) . The potential significance of the link between COX-2 and Apc was highlighted by the finding that COX-2 deficiency protects against tumor formation in mice carrying a defective Apc gene (8) .
Recently, selective inhibitors of COX-2 have been developed. These compounds possess anticancer properties (8 , 10) and appear to be safer than traditional nonsteroidal anti-inflammatory drugs. On the basis of results of this study, it will be important to establish whether inhibiting COX-2 will be useful alone or in combination with chemotherapy or radiotherapy as a novel treatment for pancreatic cancer.
| FOOTNOTES |
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1 This work was supported by the Alice Bohmfalk Charitable Trust to T. J. F. ![]()
2 To whom requests for reprints should be addressed, at New York Presbyterian Hospital-Cornell University, Room F-2024, 525 East 68th Street, New York, NY 10021. Phone: (212) 746-5130; Fax: (212) 746-8771; E-mail: tjfahey{at}mail.med.cornell.edu ![]()
3 The abbreviations used are: COX, cyclooxygenase; PMA, phorbol 12-myristate 13-acetate; RT-PCR, reverse transcription-PCR; nt, nucleotide(s). ![]()
Received 11/19/98. Accepted 1/14/99.
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716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell, 87: 803-809, 1996.[Medline]
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M. ROMANO and J. CLARIA Cyclooxygenase-2 and 5-lipoxygenase converging functions on cell proliferation and tumor angiogenesis: implications for cancer therapy FASEB J, November 1, 2003; 17(14): 1986 - 1995. [Abstract] [Full Text] [PDF] |
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M. S. De Lorenzo, K. Yamaguchi, K. Subbaramaiah, and A. J. Dannenberg Bryostatin-1 Stimulates the Transcription of Cyclooxygenase-2: Evidence for an Activator Protein-1-Dependent Mechanism Clin. Cancer Res., October 15, 2003; 9(13): 5036 - 5043. [Abstract] [Full Text] [PDF] |
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H. Choy and L. Milas Enhancing Radiotherapy With Cyclooxygenase-2 Enzyme Inhibitors: A Rational Advance? J Natl Cancer Inst, October 1, 2003; 95(19): 1440 - 1452. [Abstract] [Full Text] [PDF] |
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K.-T. Kuo, K.-C. Chow, Y.-C. Wu, C.-S. Lin, H.-W. Wang, W.-Y. Li, and L.-S. Wang Clinicopathologic significance of cyclooxygenase-2 overexpression in esophageal squamous cell carcinoma Ann. Thorac. Surg., September 1, 2003; 76(3): 909 - 914. [Abstract] [Full Text] [PDF] |
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N.K. Altorki, R.S. Keresztes, J.L. Port, D.M. Libby, R.J. Korst, D.B. Flieder, C.A. Ferrara, D.F. Yankelevitz, K. Subbaramaiah, M.W. Pasmantier, et al. Celecoxib, a Selective Cyclo-Oxygenase-2 Inhibitor, Enhances the Response to Preoperative Paclitaxel and Carboplatin in Early-Stage Non-Small-Cell Lung Cancer J. Clin. Oncol., July 15, 2003; 21(14): 2645 - 2650. [Abstract] [Full Text] [PDF] |
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L. Ermert, C. Dierkes, and M. Ermert Immunohistochemical Expression of Cyclooxygenase Isoenzymes and Downstream Enzymes in Human Lung Tumors Clin. Cancer Res., May 1, 2003; 9(5): 1604 - 1610. [Abstract] [Full Text] [PDF] |
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Y. Miyata, S. Koga, S. Kanda, M. Nishikido, T. Hayashi, and H. Kanetake Expression of Cyclooxygenase-2 in Renal Cell Carcinoma: Correlation with Tumor Cell Proliferation, Apoptosis, Angiogenesis, Expression of Matrix Metalloproteinase-2, and Survival Clin. Cancer Res., May 1, 2003; 9(5): 1741 - 1749. [Abstract] [Full Text] [PDF] |
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T. Inaba, H. Sano, Y. Kawahito, T. Hla, K. Akita, M. Toda, I. Yamashina, M. Inoue, and H. Nakada Induction of cyclooxygenase-2 in monocyte/macrophage by mucins secreted from colon cancer cells PNAS, March 4, 2003; 100(5): 2736 - 2741. [Abstract] [Full Text] [PDF] |
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D. Bagga, L. Wang, R. Farias-Eisner, J. A. Glaspy, and S. T. Reddy Differential effects of prostaglandin derived from omega -6 and omega -3 polyunsaturated fatty acids on COX-2 expression and IL-6 secretion PNAS, February 18, 2003; 100(4): 1751 - 1756. [Abstract] [Full Text] [PDF] |
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J. Chu, F. L. Lloyd, O. C. Trifan, B. Knapp, and M. T. Rizzo Potential Involvement of the Cyclooxygenase-2 Pathway in the Regulation of Tumor-associated Angiogenesis and Growth in Pancreatic Cancer Mol. Cancer Ther., January 1, 2003; 2(1): 1 - 7. [Abstract] [Full Text] [PDF] |
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R. J. Levitt and M. Pollak Insulin-like Growth Factor-I Antagonizes the Antiproliferative Effects of Cyclooxygenase-2 Inhibitors on BxPC-3 Pancreatic Cancer Cells Cancer Res., December 15, 2002; 62(24): 7372 - 7376. [Abstract] [Full Text] [PDF] |
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B. S. Zweifel, T. W. Davis, R. L. Ornberg, and J. L. Masferrer Direct Evidence for a Role of Cyclooxygenase 2-derived Prostaglandin E2 in Human Head and Neck Xenograft Tumors Cancer Res., November 15, 2002; 62(22): 6706 - 6711. [Abstract] [Full Text] [PDF] |
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G. Ferrandina, L. Lauriola, G. F. Zannoni, A. Fagotti, F. Fanfani, F. Legge, N. Maggiano, M. Gessi, S. Mancuso, F. O. Ranelletti, et al. Increased cyclooxygenase-2 (COX-2) expression is associated with chemotherapy resistance and outcome in ovarian cancer patients Ann. Onc., August 1, 2002; 13(8): 1205 - 1211. [Abstract] [Full Text] [PDF] |
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P. S. Carlton, R. Gopalakrishnan, A. Gupta, B. W. Liston, S. Habib, M. A. Morse, and G. D. Stoner Piroxicam Is an Ineffective Inhibitor of N-Nitrosomethylbenzylamine-induced Tumorigenesis in the Rat Esophagus Cancer Res., August 1, 2002; 62(15): 4376 - 4382. [Abstract] [Full Text] [PDF] |
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R. Hennig, X.-Z. Ding, W.-G. Tong, M. B. Schneider, J. Standop, H. Friess, M. W. Buchler, P. M. Pour, and T. E. Adrian 5-Lipoxygenase and Leukotriene B4 Receptor Are Expressed in Human Pancreatic Cancers But Not in Pancreatic Ducts in Normal Tissue Am. J. Pathol., August 1, 2002; 161(2): 421 - 428. [Abstract] [Full Text] [PDF] |
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M. Tamura, S. Sebastian, S. Yang, B. Gurates, K. Ferrer, H. Sasano, K. Okamura, and S. E. Bulun Up-regulation of Cyclooxygenase-2 Expression and Prostaglandin Synthesis in Endometrial Stromal Cells by Malignant Endometrial Epithelial Cells. A PARACRINE EFFECT MEDIATED BY PROSTAGLANDIN E2 AND NUCLEAR FACTOR-kappa B J. Biol. Chem., July 12, 2002; 277(29): 26208 - 26216. [Abstract] [Full Text] [PDF] |
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I. F. Orengo, J. Gerguis, R. Phillips, A. Guevara, A. T. Lewis, and H. S. Black Celecoxib, a Cyclooxygenase 2 Inhibitor as a Potential Chemopreventive to UV-Induced Skin Cancer: A Study in the Hairless Mouse Model Arch Dermatol, June 1, 2002; 138(6): 751 - 755. [Abstract] [Full Text] [PDF] |
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C Costa, R Soares, J S Reis-Filho, D Leitao, I Amendoeira, and F C Schmitt Cyclo-oxygenase 2 expression is associated with angiogenesis and lymph node metastasis in human breast cancer J. Clin. Pathol., June 1, 2002; 55(6): 429 - 434. [Abstract] [Full Text] [PDF] |
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G. Davies, L.-A. Martin, N. Sacks, and M. Dowsett Cyclooxygenase-2 (COX-2), aromatase and breast cancer: a possible role for COX-2 inhibitors in breast cancer chemoprevention Ann. Onc., May 1, 2002; 13(5): 669 - 678. [Abstract] [Full Text] [PDF] |
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K. Subbaramaiah, P. A. Cole, and A. J. Dannenberg Retinoids and Carnosol Suppress Cyclooxygenase-2 Transcription by CREB-binding Protein/p300-dependent and -independent Mechanisms Cancer Res., May 1, 2002; 62(9): 2522 - 2530. [Abstract] [Full Text] [PDF] |
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J. M. Wallace Nutritional and Botanical Modulation of the Inflammatory Cascade--Eicosanoids, Cyclooxygenases, and Lipoxygenases-- As an Adjunct in Cancer Therapy Integr Cancer Ther, March 1, 2002; 1(1): 7 - 37. [Abstract] [PDF] |
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J. D. Wayne, E. K. Abdalla, R. A. Wolff, C. H. Crane, P. W.T. Pisters, and D. B. Evans Localized Adenocarcinoma of the Pancreas: The Rationale for Preoperative Chemoradiation Oncologist, February 1, 2002; 7(1): 34 - 45. [Abstract] [Full Text] [PDF] |
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J. Portnow, S. Suleman, S. A. Grossman, S. Eller, and K. Carson A cyclooxygenase-2 (COX-2) inhibitor compared with dexamethasone in a survival study of rats with intracerebral 9L gliosarcomas Neuro-oncol, January 1, 2002; 4(1): 22 - 25. [Abstract] [PDF] |
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M. C. Specht, O. N. Tucker, M. Hocever, D. Gonzalez, L. Teng, and T. J. Fahey III Cyclooxygenase-2 Expression in Thyroid Nodules J. Clin. Endocrinol. Metab., January 1, 2002; 87(1): 358 - 363. [Abstract] [Full Text] [PDF] |
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K. J. Sales, A. A. Katz, B. Howard, R. P. Soeters, R. P. Millar, and H. N. Jabbour Cyclooxygenase-1 Is Up-Regulated in Cervical Carcinomas: Autocrine/Paracrine Regulation of Cyclooxygenase-2, Prostaglandin E Receptors, and Angiogenic Factors by Cyclooxygenase-1 Cancer Res., January 1, 2002; 62(2): 424 - 432. [Abstract] [Full Text] [PDF] |
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K. Yoshimatsu, D. Golijanin, P. B. Paty, R. A. Soslow, P.-J. Jakobsson, R. A. DeLellis, K. Subbaramaiah, and A. J. Dannenberg Inducible Microsomal Prostaglandin E Synthase Is Overexpressed in Colorectal Adenomas and Cancer Clin. Cancer Res., December 1, 2001; 7(12): 3971 - 3976. [Abstract] [Full Text] [PDF] |
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K. Salmenkivi, C. Haglund, A. Ristimaki, J. Arola, and P. Heikkila Increased Expression of Cyclooxygenase-2 in Malignant Pheochromocytomas J. Clin. Endocrinol. Metab., November 1, 2001; 86(11): 5615 - 5619. [Abstract] [Full Text] [PDF] |
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J. Fujita, J. R. Mestre, J. B. Zeldis, K. Subbaramaiah, and A. J. Dannenberg Thalidomide and Its Analogues Inhibit Lipopolysaccharide-mediated Induction of Cyclooxygenase-2 Clin. Cancer Res., November 1, 2001; 7(11): 3349 - 3355. [Abstract] [Full Text] [PDF] |
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A. H. Klimp, H. Hollema, C. Kempinga, A. G. J. van der Zee, E. G. E. de Vries, and T. Daemen Expression of Cyclooxygenase-2 and Inducible Nitric Oxide Synthase in Human Ovarian Tumors and Tumor-associated Macrophages Cancer Res., October 1, 2001; 61(19): 7305 - 7309. [Abstract] [Full Text] [PDF] |
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H. Pyo, H. Choy, G. P. Amorino, J.-s. Kim, Q. Cao, S. K. Hercules, and R. N. DuBois A Selective Cyclooxygenase-2 Inhibitor, NS-398, Enhances the Effect of Radiation in Vitro and in Vivo Preferentially on the Cells That Express Cyclooxygenase-2 Clin. Cancer Res., October 1, 2001; 7(10): 2998 - 3005. [Abstract] [Full Text] [PDF] |
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M. T. Yip-Schneider, C. J. Sweeney, S.-H. Jung, P. L. Crowell, and M. S. Marshall Cell Cycle Effects of Nonsteroidal Anti-Inflammatory Drugs and Enhanced Growth Inhibition in Combination with Gemcitabine in Pancreatic Carcinoma Cells J. Pharmacol. Exp. Ther., September 1, 2001; 298(3): 976 - 985. [Abstract] [Full Text] |
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E. M. P. de Almeida, C. Piche, J. Sirois, and M. Dore Expression of Cyclo-oxygenase-2 in Naturally Occurring Squamous Cell Carcinomas in Dogs J. Histochem. Cytochem., July 1, 2001; 49(7): 867 - 876. [Abstract] [Full Text] [PDF] |
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S. Kern, R. Hruban, M. A. Hollingsworth, R. Brand, T. E. Adrian, E. Jaffee, and M. A. Tempero A White Paper: The Product of a Pancreas Cancer Think Tank Cancer Res., June 1, 2001; 61(12): 4923 - 4932. [Full Text] [PDF] |
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K. J. Sales, A. A. Katz, M. Davis, S. Hinz, R. P. Soeters, M. D. Hofmeyr, R. P. Millar, and H. N. Jabbour Cyclooxygenase-2 Expression and Prostaglandin E2 Synthesis Are Up-Regulated in Carcinomas of the Cervix: A Possible Autocrine/Paracrine Regulation of Neoplastic Cell Function via EP2/EP4 Receptors J. Clin. Endocrinol. Metab., May 1, 2001; 86(5): 2243 - 2249. [Abstract] [Full Text] |
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K. Subbaramaiah, P. Bulic, Y. Lin, A. J. Dannenberg, and D. S. Pasco Development and Use of a Gene Promoter-Based Screen to Identify Novel Inhibitors of Cyclooxygenase-2 Transcription J Biomol Screen, April 1, 2001; 6(2): 101 - 110. [Abstract] [PDF] |
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Z. Li, Y. Shimada, A. Kawabe, F. Sato, M. Maeda, I. Komoto, T. Hong, Y. Ding, J. Kaganoi, and M. Imamura Suppression of N-nitrosomethylbenzylamine (NMBA)-induced esophageal tumorigenesis in F344 rats by JTE-522, a selective COX-2 inhibitor Carcinogenesis, April 1, 2001; 22(4): 547 - 551. [Abstract] [Full Text] [PDF] |
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T. Shirahama and C. Sakakura Overexpression of Cyclooxygenase-2 in Squamous Cell Carcinoma of the Urinary Bladder Clin. Cancer Res., March 1, 2001; 7(3): 558 - 561. [Abstract] [Full Text] |
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H. Shiotani, A. Denda, K. Yamamoto, W. Kitayama, T. Endoh, Y. Sasaki, M. Tsutsumi, M. Sugimura, and Y. Konishi Increased Expression of Cyclooxygenase-2 Protein in 4-Nitroquinoline-1-oxide-induced Rat Tongue Carcinomas and Chemopreventive Efficacy of a Specific Inhibitor, Nimesulide Cancer Res., February 1, 2001; 61(4): 1451 - 1456. [Abstract] [Full Text] |
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S. Kulkarni, J. S. Rader, F. Zhang, H. Liapis, A. T. Koki, J. L. Masferrer, K. Subbaramaiah, and A. J. Dannenberg Cyclooxygenase-2 Is Overexpressed in Human Cervical Cancer Clin. Cancer Res., February 1, 2001; 7(2): 429 - 434. [Abstract] [Full Text] |
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S Chariyalertsak, V Sirikulchayanonta, D Mayer, A Kopp-Schneider, G Furstenberger, F Marks, and K Muller-Decker Aberrant cyclooxygenase isozyme expression in human intrahepatic cholangiocarcinoma Gut, January 1, 2001; 48(1): 80 - 86. [Abstract] [Full Text] [PDF] |
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C. Denkert, M. Köbel, S. Berger, A. Siegert, A. Leclere, U. Trefzer, and S. Hauptmann Expression of Cyclooxygenase 2 in Human Malignant Melanoma Cancer Res., January 1, 2001; 61(1): 303 - 308. [Abstract] [Full Text] |
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R. F. Souza, K. Shewmake, D. G. Beer, B. Cryer, and S. J. Spechler Selective Inhibition of Cyclooxygenase-2 Suppresses Growth and Induces Apoptosis in Human Esophageal Adenocarcinoma Cells Cancer Res., October 1, 2000; 60(20): 5767 - 5772. [Abstract] [Full Text] |
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S. H. HONG, F. G. ONDREY, I. M. AVIS, Z. CHEN, E. LOUKINOVA, P. F. CAVANAUGH JR, C. VAN WAES, and J. L. MULSHINE Cyclooxygenase regulates human oropharyngeal carcinomas via the proinflammatory cytokine IL-6: a general role for inflammation? FASEB J, August 1, 2000; 14(11): 1499 - 1507. [Abstract] [Full Text] |
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R. H. Hruban, M. Goggins, J. Parsons, and S. E. Kern Progression Model for Pancreatic Cancer Clin. Cancer Res., August 1, 2000; 6(8): 2969 - 2972. [Full Text] |
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M. Komhoff, Y. Guan, H. W. Shappell, L. Davis, G. Jack, Y. Shyr, M. O. Koch, S. B. Shappell, and M. D. Breyer Enhanced Expression of Cyclooxygenase-2 in High Grade Human Transitional Cell Bladder Carcinomas Am. J. Pathol., July 1, 2000; 157(1): 29 - 35. [Abstract] [Full Text] [PDF] |
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T. Shirahama Cyclooxygenase-2 Expression Is Up-Regulated in Transitional Cell Carcinoma and Its Preneoplastic Lesions in the Human Urinary Bladder Clin. Cancer Res., June 1, 2000; 6(6): 2424 - 2430. [Abstract] [Full Text] |
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C. Petersen, S. Petersen, L. Milas, F. F. Lang, and P. J. Tofilon Enhancement of Intrinsic Tumor Cell Radiosensitivity Induced by a Selective Cyclooxygenase-2 Inhibitor Clin. Cancer Res., June 1, 2000; 6(6): 2513 - 2520. [Abstract] [Full Text] |
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R. H. Hruban, R. E. Wilentz, and S. E. Kern Genetic Progression in the Pancreatic Ducts Am. J. Pathol., June 1, 2000; 156(6): 1821 - 1825. [Abstract] [Full Text] [PDF] |
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K. Subbaramaiah, P. Michaluart, M. B. Sporn, and A. J. Dannenberg Ursolic Acid Inhibits Cyclooxygenase-2 Transcription in Human Mammary Epithelial Cells Cancer Res., May 1, 2000; 60(9): 2399 - 2404. [Abstract] [Full Text] |
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A. Shamma, H. Yamamoto, Y. Doki, J. Okami, M. Kondo, Y. Fujiwara, M. Yano, M. Inoue, N. Matsuura, H. Shiozaki, et al. Up-Regulation of Cyclooxygenase-2 in Squamous Carcinogenesis of the Esophagus Clin. Cancer Res., April 1, 2000; 6(4): 1229 - 1238. [Abstract] [Full Text] |
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M. B. Sporn and N. Suh Chemoprevention of cancer Carcinogenesis, March 1, 2000; 21(3): 525 - 530. [Abstract] [Full Text] [PDF] |
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J. L. Masferrer, K. M. Leahy, A. T. Koki, B. S. Zweifel, S. L. Settle, B. M. Woerner, D. A. Edwards, A. G. Flickinger, R. J. Moore, and K. Seibert Antiangiogenic and Antitumor Activities of Cyclooxygenase-2 Inhibitors Cancer Res., March 1, 2000; 60(5): 1306 - 1311. [Abstract] [Full Text] |
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, , , , , J. , P. , and Preferential Enhancement of Tumor Radioresponse by a Cyclooxygenase-2 Cancer Res., March 1, 2000; 60(5): 1326 - 1331. [Abstract] [Full Text] [PDF] |
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M. T. Yip-Schneider, D. S. Barnard, S. D. Billings, L. Cheng, D. K. Heilman, A. Lin, S. J. Marshall, P. L. Crowell, M. S. Marshall, and C. J. Sweeney Cyclooxygenase-2 expression in human pancreatic adenocarcinomas Carcinogenesis, February 1, 2000; 21(2): 139 - 146. [Abstract] [Full Text] [PDF] |
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M. Stolina, S. Sharma, Y. Lin, M. Dohadwala, B. Gardner, J. Luo, L. Zhu, M. Kronenberg, P. W. Miller, J. Portanova, et al. Specific Inhibition of Cyclooxygenase 2 Restores Antitumor Reactivity by Altering the Balance of IL-10 and IL-12 Synthesis J. Immunol., January 1, 2000; 164(1): 361 - 370. [Abstract] [Full Text] [PDF] |
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