Activation of PPARγ in myeloid cells promotes lung cancer progression and metastasis

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Li, Howard ^a,c   Sorenson, Amber L ^a   Poczobutt, Joanna ^a   Amin, Jay ^a   Joyal, Teresa ^a   Sullivan, Timothy ^b   Crossno, Joseph T ^a,b,c   Weiser Evans, Mary C M ^a   Nemenoff, Raphael A ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; ARGINASE 1; BETA ACTIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; 2,4 THIAZOLIDINEDIONE DERIVATIVE; ANTIDIABETIC AGENT; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; ROSIGLITAZONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BRAIN METASTASIS; CANCER GROWTH; CANCER TRANSPLANTATION; COCULTURE; CONTROLLED STUDY; DRUG CARCINOGENICITY; GENE DELETION; GENE TARGETING; IMMUNOFLUORESCENCE TEST; LIVER METASTASIS; LUNG ALVEOLUS MACROPHAGE; LUNG CANCER; LUNG CARCINOGENESIS; LUNG METASTASIS; MALE; METASTASIS; METASTASIS INHIBITION; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; WILD TYPE; ADENOCARCINOMA; ANIMAL; BONE MARROW; C57BL MOUSE; DISEASE COURSE; DRUG POTENTIATION; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HUMAN; LUNG TUMOR; MACROPHAGE; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ADENOCARCINOMA; ANIMALS; BONE MARROW; COCULTURE TECHNIQUES; DISEASE PROGRESSION; FLUORESCENT ANTIBODY TECHNIQUE; GREEN FLUORESCENT PROTEINS; HUMANS; HYPOGLYCEMIC AGENTS; LUNG NEOPLASMS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYELOID CELLS; PPAR GAMMA; THIAZOLIDINEDIONES;

EID: 82455167201     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028133     Document Type: Article

References (38)

1. Jemal A, Siegel R, Ward E, Murray T, Xu J, et al. (2006) Cancer statistics. CA Cancer J Clin 56: 106-30.
2. Kenny PA, Lee GY, Bissell MJ, (2007) Targeting the tumor microenvironment. Front Biosci 12: 3468-74.
3. Johnson L, Mercer K, Greenbaum D, Bronson RT, Crowley D, et al. (2001) Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 410: 1111-6.
4. Smith GJ, Le Mesurier SM, de Montfort ML, Lykke AW, (1984) Establishment of epithelial cell strains from normal adult mouse lung resembling a urethane-induced lung adenoma cell strain and a metastasizing mouse lung carcinoma cell line. Cell Biol Int Rep 8: 161-9.
5. Weiser-Evans MCM, Wang X-Q, Amin J, Van Putten V, Choudhary R, et al. (2009) Depletion of Cytosolic Phospholipase A2 in Bone Marrow-Derived Macrophages Protects against Lung Cancer Progression and Metastasis. Cancer Res 69: 1733-8.
6. Tontonoz P, Spiegelman BM, (2008) Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 77: 289-312.
7. Lehmann JM, Moore LB, Smith-Oliver TA, Wilkison WO, Willson TM, et al. (1995) An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J Biol Chem 270: 12953-6.
8. Sasaki H, Tanahashi M, Yukiue H, Moiriyama S, Kobayashi Y, et al. (2002) Decreased perioxisome proliferator-activated receptor gamma gene expression was correlated with poor prognosis in patients with lung cancer. Lung Cancer 36: 71-6.
9. Govindarajan R, Ratnasinghe L, Simmons DL, Siegel ER, Midathada MV, et al. (2007) Thiazolidinediones and the Risk of Lung, Prostate, and Colon Cancer in Patients With Diabetes. J Clin Oncol 25: 1476-81.
10. Bren-Mattison Y, Meyer AM, Van Putten V, Li H, Kuhn K, et al. (2008) Antitumorigenic Effects of Peroxisome Proliferator-Activated Receptor-{gamma} in Non-Small-Cell Lung Cancer Cells Are Mediated by Suppression of Cyclooxygenase-2 via Inhibition of Nuclear Factor-{kappa}B. Mol Pharmacol 73: 709-17.
11. Bren-Mattison Y, Van Putten V, Chan D, Winn R, Geraci MW, et al. (2005) Peroxisome proliferator-activated receptor-gamma (PPAR(gamma)) inhibits tumorigenesis by reversing the undifferentiated phenotype of metastatic non-small-cell lung cancer cells (NSCLC). Oncogene 24: 1412-22.
12. Nemenoff R, Meyer AM, Hudish TM, Mozer AB, Snee A, et al. (2008) Prostacyclin Prevents Murine Lung Cancer Independent of the Membrane Receptor by Activation of Peroxisomal Proliferator-Activated Receptor {gamma}. Cancer Prev Res 1: 349-56.
13. Franks LM, Carbonell AW, Hemmings VJ, Riddle PN, (1976) Metastasizing tumors from serum-supplemented and serum-free cell lines from a C57BL mouse lung tumor. Cancer Res 36: 1049-55.
14. Maeda N, Takahashi M, Funahashi T, Kihara S, Nishizawa H, et al. (2001) PPARgamma ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein. Diabetes 50: 2094-9.
15. Mantovani A, Marchesi F, Porta C, Sica A, Allavena P, (2007) Inflammation and cancer: breast cancer as a prototype. Breast 16 (Suppl 2): S27-33.
16. Riches DW, Henson PM, Remigio LK, Catterall JF, Strunk RC, (1988) Differential regulation of gene expression during macrophage activation with a polyribonucleotide. The role of endogenously derived IFN. J Immunol 141: 180-8.
17. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A, (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23: 549-55.
18. Han SW, Roman J, (2008) Activated PPARgamma Targets Surface and Intracellular Signals That Inhibit the Proliferation of Lung Carcinoma Cells. PPAR Res 2008: 254108.
19. Li M, Lee TW, Yim AP, Mok TS, Chen GG, (2006) Apoptosis induced by troglitazone is both peroxisome proliferator-activated receptor-gamma- and ERK-dependent in human non-small lung cancer cells. J Cell Physiol 209: 428-38.
20. Zou W, Liu X, Yue P, Khuri FR, Sun SY, (2007) PPARgamma ligands enhance TRAIL-induced apoptosis through DR5 upregulation and c-FLIP downregulation in human lung cancer cells. Cancer Biol Ther 6: 99-106.
21. Choudhary R, Li H, Winn RA, Sorenson AL, Weiser-Evans MC, et al. (2009) Peroxisome Proliferator-Activated Receptor-gamma Inhibits Transformed Growth of Non-Small Cell Lung Cancer Cells through Selective Suppression of Snail. Neoplasia 12: 224-34.
22. Li MY, Yuan H, Ma LT, Kong AW, Hsin MK, et al. (2010) Roles of peroxisome proliferator-activated receptor-alpha and-gamma in the development of non-small cell lung cancer. Am J Respir Cell Mol Biol 43: 674-83.
23. Lewis CE, Pollard JW, (2006) Distinct Role of Macrophages in Different Tumor Microenvironments. Cancer Res 66: 605-12.
24. Rodriguez PC, Quiceno DG, Zabaleta J, Ortiz B, Zea AH, et al. (2004) Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses. Cancer Res 64: 5839-49.
25. Liu Q, Zhang C, Sun A, Zheng Y, Wang L, et al. (2009) Tumor-educated CD11bhighIalow regulatory dendritic cells suppress T cell response through arginase I. J Immunol 182: 6207-16.
26. Norian LA, Rodriguez PC, O'Mara LA, Zabaleta J, Ochoa AC, et al. (2009) Tumor-infiltrating regulatory dendritic cells inhibit CD8+ T cell function via L-arginine metabolism. Cancer Res 69: 3086-94.
27. Bak SP, Alonso A, Turk MJ, Berwin B, (2008) Murine ovarian cancer vascular leukocytes require arginase-1 activity for T cell suppression. Mol Immunol 46: 258-68.
28. Oberlies J, Watzl C, Giese T, Luckner C, Kropf P, et al. (2009) Regulation of NK cell function by human granulocyte arginase. J Immunol 182: 5259-67.
29. Gupta RA, Dubois RN, (2002) Controversy: PPARgamma as a target for treatment of colorectal cancer. Am J Physiol Gastrointest Liver Physiol 283: G266-9.
30. Lefebvre AM, Chen I, Desreumaux P, Najib J, Fruchart JC, et al. (1998) Activation of the peroxisome proliferator-activated receptor gamma promotes the development of colon tumors in C57BL/6J-APCMin/+ mice. Nat Med 4: 1053-7.
31. Pino MV, Kelley MF, Jayyosi Z, (2004) Promotion of colon tumors in C57BL/6J-APC(min)/+ mice by thiazolidinedione PPARgamma agonists and a structurally unrelated PPARgamma agonist. Toxicol Pathol 32: 58-63.
32. Girnun GD, Smith WM, Drori S, Sarraf P, Mueller E, et al. (2002) APC-dependent suppression of colon carcinogenesis by PPARgamma. Proc Natl Acad Sci U S A 99: 13771-6.
33. Nemenoff RA, (2007) Peroxisome proliferator-activated receptor-gamma in lung cancer: defining specific versus "off-target" effectors. J Thorac Oncol 2: 989-92.
34. Bonfield TL, Thomassen MJ, Farver CF, Abraham S, Koloze MT, et al. (2008) Peroxisome Proliferator-Activated Receptor-{gamma} Regulates the Expression of Alveolar Macrophage Macrophage Colony-Stimulating Factor. J Immunol 181: 235-42.
35. Crossno JT Jr, Garat CV, Reusch JEB, Morris KG, Dempsey EC, et al. (2007) Rosiglitazone attenuates hypoxia-induced pulmonary arterial remodeling. Am J Physiol Lung Cell Mol Physiol 292: L885-97.
36. Budde K, Neumayer HH, Fritsche L, Sulowicz W, Stompor T, et al. (2003) The pharmacokinetics of pioglitazone in patients with impaired renal function. Br J Clin Pharmacol 55: 368-74.
37. Heasley LE, Thaler S, Nicks M, Price B, Skorecki K, et al. (1997) Induction of cytosolic phospholipase A2 by oncogenic Ras in human non-small cell lung cancer. J Biol Chem 272: 14501-4.
38. Wick M, Hurteau G, Dessev C, Chan D, Geraci MW, et al. (2002) Peroxisome Proliferator-Activated Receptor-gamma Is a Target of Nonsteroidal Anti-Inflammatory Drugs Mediating Cyclooxygenase-Independent Inhibition of Lung Cancer Cell Growth. Mol Pharmacol 62: 1207-14.