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[Cancer Research 58, 1208-1216, March 15, 1998]
© 1998 American Association for Cancer Research
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Non-Small Cell Lung Cancer Cyclooxygenase-2-dependent Regulation of Cytokine Balance in Lymphocytes and Macrophages: Up-Regulation of Interleukin 10 and Down-Regulation of Interleukin 12 Production1

Min Huang, Marina Stolina, Sherven Sharma, Jenny T. Mao, Li Zhu, Patrice W. Miller, Jerome Wollman, Harvey Herschman and Steven M. Dubinett2

Pulmonary Immunology Laboratory, Division of Pulmonary and Critical Care Medicine, Departments of Medicine [M. H., M. S., S. S., J. T. M., L. Z., P. W. M., S. M. D.], Biological Chemistry and Molecular and Medical Pharmacology [H. H.], and Pathology [J. W.], and Jonsson Comprehensive Cancer Center [H. H., S. M. D.], UCLA School of Medicine and the West Los Angeles Veterans Affairs Medical Center, Los Angeles, California 90073

Tumor-derived prostaglandin E2 (PGE2) modifies cytokine balance and inhibits host immunity. We hypothesized that a high level of PGE2 production by lung tumor cells is dependent on tumor cyclooxygenase (COX)-2 expression. We found that PGE2 production by A549 non-small cell lung cancer (NSCLC) cells was elevated up to 50-fold in response to interleukin (IL)-1ß. Reversal of IL-1ß-induced PGE2 production in A549 cells was achieved by specific pharmacological or antisense oligonucleotide inhibition of COX-2 activity or expression. In contrast, specific COX-1 inhibition was not effective. Consistent with these findings, IL-1ß induced COX-2 mRNA expression and protein production in A549 cells. Specific inhibition of COX-2 abrogated the capacity of IL-1ß-stimulated A549 cells to induce IL-10 in lymphocytes and macrophages. Furthermore, specific inhibition of A549 COX-2 reversed the tumor-derived PGE2-dependent inhibition of macrophage IL-12 production when whole blood was cultured in tumor supernatants. Our results indicate that lung tumor-derived PGE2 plays a pivotal role in promoting lymphocyte and macrophage IL-10 induction while simultaneously inhibiting macrophage IL-12 production. Immunohistochemistry of human NSCLC tissues obtained from lung cancer resection specimens revealed cytoplasmic staining for COX-2 within tumor cells. This is the first description of functional COX-2 expression by NSCLC cells and the definition of a pathway whereby tumor COX-2 expression and a high level of PGE2 production mediate profound alteration in cytokine balance in the lung cancer microenvironment.

1 This work is supported by NIH Grants CA71818 and GM24797, the American Lung Association, Merit Review Research Funds from the Department of Veterans Affairs, and the Helen Neufeld Research Career Development Award (Stop Cancer Award). M. H. was supported by the American Lung Association of California Young Investigator Award and NIH Institutional Training Grant in Tumor Immunology CA09120. S. S. was supported by a Parker B. Francis Fellowship from the Francis Families Foundation. M. S. and J. T. M. were supported by NIH Institutional Training Grant in Pulmonary Medicine HL07104. S. M. D. is a Career Investigator of the American Lung Association.

2 To whom requests for reprints should be addressed, at Division of Pulmonary and Critical Care Medicine, Department of Medicine, UCLA School of Medicine, West Los Angeles Veterans Affairs Medical Center, 111Q, 11301 Wilshire Boulevard, Los Angeles, CA 90073, Phone: (310) 794-6566; Fax: (310) 268-4712; E-mail: sdubinet@ucla.edu.

Received 11/ 6/97. Accepted 1/29/98.




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S. Hillinger, S.-C. Yang, L. Zhu, M. Huang, R. Duckett, K. Atianzar, R. K. Batra, R. M. Strieter, S. M. Dubinett, and S. Sharma
EBV-Induced Molecule 1 Ligand Chemokine (ELC/CCL19) Promotes IFN-{gamma}-Dependent Antitumor Responses in a Lung Cancer Model
J. Immunol., December 15, 2003; 171(12): 6457 - 6465.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
T. L. Symensma, D. Martinez-Guzman, Q. Jia, E. Bortz, T.-T. Wu, N. Rudra-Ganguly, S. Cole, H. Herschman, and R. Sun
COX-2 Induction during Murine Gammaherpesvirus 68 Infection Leads to Enhancement of Viral Gene Expression
J. Virol., December 1, 2003; 77(23): 12753 - 12763.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
J. T. Mao, M. D. Roth, K. J. Serio, F. Baratelli, L. Zhu, E. C. Holmes, R. M. Strieter, and S. M. Dubinett
Celecoxib Modulates the Capacity for Prostaglandin E2 and Interleukin-10 Production in Alveolar Macrophages from Active Smokers
Clin. Cancer Res., December 1, 2003; 9(16): 5835 - 5841.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
P. DeLong, T. Tanaka, R. Kruklitis, A. C. Henry, V. Kapoor, L. R. Kaiser, D. H. Sterman, and S. M. Albelda
Use of Cyclooxygenase-2 Inhibition to Enhance the Efficacy of Immunotherapy
Cancer Res., November 15, 2003; 63(22): 7845 - 7852.
[Abstract] [Full Text] [PDF]

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 Ann. Thorac. Surg.Home page
J. E. Castelao, R. D. Bart III, C. A. DiPerna, E. M. Sievers, and R. M. Bremner
Lung cancer and cyclooxygenase-2
Ann. Thorac. Surg., October 1, 2003; 76(4): 1327 - 1335.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
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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 Clin. Cancer Res.Home page
E. G. Cohen, T. Almahmeed, B. Du, D. Golijanin, J. O. Boyle, R. A. Soslow, K. Subbaramaiah, and A. J. Dannenberg
Microsomal Prostaglandin E Synthase-1 Is Overexpressed in Head and Neck Squamous Cell Carcinoma
Clin. Cancer Res., August 1, 2003; 9(9): 3425 - 3430.
[Abstract] [Full Text] [PDF]

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 JCOHome page
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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 JCOHome page
A. Ribas, L. H. Butterfield, J. A. Glaspy, and J. S. Economou
Current Developments in Cancer Vaccines and Cellular Immunotherapy
J. Clin. Oncol., June 15, 2003; 21(12): 2415 - 2432.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
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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 J. Immunol.Home page
L. X. Zhu, S. Sharma, B. Gardner, B. Escuadro, K. Atianzar, D. P. Tashkin, and S. M. Dubinett
IL-10 Mediates Sigma1 Receptor-Dependent Suppression of Antitumor Immunity
J. Immunol., April 1, 2003; 170(7): 3585 - 3591.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
S. Sharma, M. Stolina, S.-C. Yang, F. Baratelli, J. F. Lin, K. Atianzar, J. Luo, L. Zhu, Y. Lin, M. Huang, et al.
Tumor Cyclooxygenase 2-dependent Suppression of Dendritic Cell Function
Clin. Cancer Res., March 1, 2003; 9(3): 961 - 968.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
N. Heuze-Vourc'h, L. Zhu, K. Krysan, R. K. Batra, S. Sharma, and S. M. Dubinett
Abnormal Interleukin 10R{alpha} Expression Contributes to the Maintenance of Elevated Cyclooxygenase-2 in Non-Small Cell Lung Cancer Cells
Cancer Res., February 15, 2003; 63(4): 766 - 770.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
M. Yao, S. Kargman, E. C. Lam, C. R. Kelly, Y. Zheng, P. Luk, E. Kwong, J. F. Evans, and M. M. Wolfe
Inhibition of Cyclooxygenase-2 by Rofecoxib Attenuates the Growth and Metastatic Potential of Colorectal Carcinoma in Mice
Cancer Res., February 1, 2003; 63(3): 586 - 592.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
R. K. Batra, Y. Lin, S. Sharma, M. Dohadwala, J. Luo, M. Pold, and S. M. Dubinett
Non-Small Cell Lung Cancer-derived Soluble Mediators Enhance Apoptosis in Activated T Lymphocytes through an I{kappa}B Kinase-dependent Mechanism
Cancer Res., February 1, 2003; 63(3): 642 - 646.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Dohadwala, R. K. Batra, J. Luo, Y. Lin, K. Krysan, M. Pold, S. Sharma, and S. M. Dubinett
Autocrine/Paracrine Prostaglandin E2 Production by Non-small Cell Lung Cancer Cells Regulates Matrix Metalloproteinase-2 and CD44 in Cyclooxygenase-2-dependent Invasion
J. Biol. Chem., December 20, 2002; 277(52): 50828 - 50833.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
A. G. Banerjee, V. K. Gopalakrishnan, I. Bhattacharya, and J. K. Vishwanatha
Deregulated Cyclooxygenase-2 Expression in Oral Premalignant Tissues
Mol. Cancer Ther., December 1, 2002; 1(14): 1265 - 1271.
[Abstract] [Full Text] [PDF]

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 Ann OncolHome page
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]

Home page
 CarcinogenesisHome page
K.-i. Sunayama, H. Konno, T. Nakamura, H. Kashiwabara, T. Shoji, T. Tsuneyoshi, and S. Nakamura
The role of cyclooxygenase-2 (COX-2) in two different morphological stages of intestinal polyps in APC{Delta}474 knockout mice
Carcinogenesis, August 1, 2002; 23(8): 1351 - 1359.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
S. A. Wardlaw, N. Zhang, and S. A. Belinsky
Transcriptional Regulation of Basal Cyclooxygenase-2 Expression in Murine Lung Tumor-Derived Cell Lines by CCAAT/Enhancer-Binding Protein and Activating Transcription Factor/cAMP Response Element-Binding Protein
Mol. Pharmacol., August 1, 2002; 62(2): 326 - 333.
[Abstract] [Full Text] [PDF]

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 Br J AnaesthHome page
A. M. Mahdy, H. F. Galley, M. A. Abdel-Wahed, K. F. El-Korny, S. A. Sheta, and N. R. Webster
Differential modulation of interleukin-6 and interleukin-10 by diclofenac in patients undergoing major surgery
Br. J. Anaesth., June 1, 2002; 88(6): 797 - 802.
[Abstract] [Full Text] [PDF]

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 Integr Cancer TherHome page
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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 Am. J. Pathol.Home page
C. Denkert, M. Kobel, S. Pest, I. Koch, S. Berger, M. Schwabe, A. Siegert, A. Reles, B. Klosterhalfen, and S. Hauptmann
Expression of Cyclooxygenase 2 Is an Independent Prognostic Factor in Human Ovarian Carcinoma
Am. J. Pathol., March 1, 2002; 160(3): 893 - 903.
[Abstract] [Full Text] [PDF]

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 ChestHome page
M. Pold, M. Dohadwala, J. Luo, Y. Lin, and S. Dubinett
Microarray Identifies Cyclo-oxygenase-2-Dependent Modulation of Insulin-like Growth Factor Binding Protein-3 in Non-small Cell Lung Cancer Cells
Chest, March 1, 2002; 121(2009): 29S - 30S.
[Full Text] [PDF]

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 JCOHome page
G. Ferrandina, L. Lauriola, M. G. Distefano, G. F. Zannoni, M. Gessi, F. Legge, N. Maggiano, S. Mancuso, A. Capelli, G. Scambia, et al.
Increased Cyclooxygenase-2 Expression Is Associated With Chemotherapy Resistance and Poor Survival in Cervical Cancer Patients
J. Clin. Oncol., February 15, 2002; 20(4): 973 - 981.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
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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 Clin. Cancer Res.Home page
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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 Infect. Immun.Home page
W. Thomas, Z. K. Ascott, D. Harmey, L. W. Slice, E. Rozengurt, and A. J. Lax
Cytotoxic Necrotizing Factor from Escherichia coli Induces RhoA-Dependent Expression of the Cyclooxygenase-2 Gene
Infect. Immun., November 1, 2001; 69(11): 6839 - 6845.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. Sharma, M. Stolina, L. Zhu, Y. Lin, R. Batra, M. Huang, R. Strieter, and S. M. Dubinett
Secondary Lymphoid Organ Chemokine Reduces Pulmonary Tumor Burden in Spontaneous Murine Bronchoalveolar Cell Carcinoma
Cancer Res., September 1, 2001; 61(17): 6406 - 6412.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
J. M. Kurie and R. N. Dubois
Prostaglandin E Synthase: Another Enzyme in the Cyclooxygenase Pathway Driving Epithelial Cancer?
Clin. Cancer Res., September 1, 2001; 7(9): 2608 - 2610.
[Full Text] [PDF]

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 Clin. Cancer Res.Home page
K. Yoshimatsu, N. K. Altorki, D. Golijanin, F. Zhang, P.-J. Jakobsson, A. J. Dannenberg, and K. Subbaramaiah
Inducible Prostaglandin E Synthase Is Overexpressed in Non-Small Cell Lung Cancer
Clin. Cancer Res., September 1, 2001; 7(9): 2669 - 2674.
[Abstract] [Full Text] [PDF]

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 BloodHome page
P. Kalinski, P. L. Vieira, J. H. N. Schuitemaker, E. C. de Jong, and M. L. Kapsenberg
Prostaglandin E2 is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer
Blood, June 1, 2001; 97(11): 3466 - 3469.
[Abstract] [Full Text] [PDF]

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 J Biomol ScreenHome page
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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 Cancer Res.Home page
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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 Cancer Res.Home page
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]

Home page
 CarcinogenesisHome page
J.H. Jeng, Y.S. Ho, C.P. Chan, Y.J. Wang, L.J. Hahn, D. Lei, C.C. Hsu, and M.C. Chang
Areca nut extract up-regulates prostaglandin production, cyclooxygenase-2 mRNA and protein expression of human oral keratinocytes
Carcinogenesis, July 1, 2000; 21(7): 1365 - 1370.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
S. A. Wardlaw, T. H. March, and S. A. Belinsky
Cyclooxygenase-2 expression is abundant in alveolar type II cells in lung cancer-sensitive mouse strains and in premalignant lesions
Carcinogenesis, July 1, 2000; 21(7): 1371 - 1377.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
L. X. Zhu, S. Sharma, M. Stolina, B. Gardner, M. D. Roth, D. P. Tashkin, and S. M. Dubinett
{Delta}-9-Tetrahydrocannabinol Inhibits Antitumor Immunity by a CB2 Receptor-Mediated, Cytokine-Dependent Pathway
J. Immunol., July 1, 2000; 165(1): 373 - 380.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
S. Sharma, M. Stolina, J. Luo, R. M. Strieter, M. Burdick, L. X. Zhu, R. K. Batra, and S. M. Dubinett
Secondary Lymphoid Tissue Chemokine Mediates T Cell-Dependent Antitumor Responses In Vivo
J. Immunol., May 1, 2000; 164(9): 4558 - 4563.
[Abstract] [Full Text] [PDF]

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 ANN INTERN MEDHome page
S. M. Albelda, R. Wiewrodt, and J. B. Zuckerman
Gene Therapy for Lung Disease: Hype or Hope?
Ann Intern Med, April 18, 2000; 132(8): 649 - 660.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
A. K. Bauer, L. D. Dwyer-Nield, and A. M. Malkinson
High cyclooxygenase 1 (COX-1) and cyclooxygenase 2 (COX-2) contents in mouse lung tumors
Carcinogenesis, April 1, 2000; 21(4): 543 - 550.
[Abstract] [Full Text] [PDF]


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