Eicosanoid profiling in an orthotopic model of lung cancer progression by mass spectrometry demonstrates selective production of leukotrienes by inflammatory cells of the microenvironment

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Poczobutt, Joanna M ^a   Gijon, Miguel ^a   Amin, Jay ^a   Hanson, Dwight ^a   Li, Howard ^a,c   Walker, Deandra ^a   Weiser Evans, Mary ^a   Lu, Xian ^b   Murphy, Robert C ^a   Nemenoff, Raphael A ^a  

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

^b Food Science and Human Nutrition   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ICOSANOID; LEUKOTRIENE; LEUKOTRIENE B4; LEUKOTRIENE C4; LEUKOTRIENE D4; LEUKOTRIENE E4; LIPOXYGENASE; PHOSPHOLIPASE A2; PROSTAGLANDIN D2; PROSTAGLANDIN E2; PROSTAGLANDIN F2 ALPHA; PROSTAGLANDIN SYNTHASE; PHOSPHOLIPASE A2 GROUP IV;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CONTROLLED STUDY; INFLAMMATORY CELL; LIQUID CHROMATOGRAPHY; LUNG CANCER; MOUSE; NEUTROPHIL; NONHUMAN; PROSTAGLANDIN SYNTHESIS; PROTEIN EXPRESSION; TANDEM MASS SPECTROMETRY; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; ANIMAL; DISEASE COURSE; DISEASE MODEL; FEMALE; GENE DELETION; GENETICS; HUMAN; INFLAMMATION; KNOCKOUT MOUSE; LUNG TUMOR; MALE; METABOLISM; METABOLOMICS; PATHOLOGY; PROCEDURES; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EICOSANOIDS; FEMALE; GENE DELETION; GROUP IV PHOSPHOLIPASES A2; HUMANS; INFLAMMATION; LEUKOTRIENES; LUNG NEOPLASMS; MALE; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; MICE; MICE, KNOCKOUT; TUMOR MICROENVIRONMENT;

EID: 84893164443     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079633     Document Type: Article

References (37)

1. Nakanishi M, Rosenberg DW (2006) Roles of cPLA2alpha and arachidonic acid in cancer. Biochim Biophys Acta 1761: 1335-1343. (Pubitemid 44738711)
2. Schneider C, Pozzi A (2011) Cyclooxygenases and lipoxygenases in cancer. Cancer Metastasis Rev 30: 277-294.
3. Buczynski MW, Dumlao DS, Dennis EA (2009) Thematic Review Series: Proteomics. An integrated omics analysis of eicosanoid biology. J Lipid Res 50: 1015-1038.
4. Narumiya S, Sugimoto Y, Ushikubi F (1999) Prostanoid receptors: structures, properties, and functions. Physiol Rev 79: 1193-1226. (Pubitemid 29473315)
5. Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2008) Cancer statistics, 2008. CA Cancer J Clin 58: 71-96. (Pubitemid 351521864)
6. Hida T, Yatabe Y, Achiwa H, Muramatsu H, Kozaki K, et al. (1998) Increased expression of cyclooxygenase 2 occurs frequently in human lung cancers, specifically in adenocarcinomas. Cancer Res 58: 3761-3764. (Pubitemid 28405625)
7. Wolff H, Saukkonen K, Anttila S, Karjalainen A, Vainio H, et al. (1998) Expression of cyclooxygenase-2 in human lung carcinoma. Cancer Res 58: 4997-5001. (Pubitemid 28521147)
8. 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: 14501-14504. (Pubitemid 27251707)
9. Moody TW, Leyton J, Zakowicz H, Hida T, Kang Y, et al. (2001) Indomethacin reduces lung adenoma number in A/J mice. Anticancer Res 21: 1749-1755. (Pubitemid 32728908)
10. Meyer AM, Dwyer-Nield LD, Hurteau GJ, Keith RL, O'Leary E, et al. (2004) Decreased lung tumorigenesis in mice genetically deficient in cytosolic phospholipase A2. Carcinogenesis 25: 1517-1524. (Pubitemid 39162717)
11. Keith RL, Miller YE, Hoshikawa Y, Moore MD, Gesell TL, et al. (2002) Manipulation of Pulmonary Prostacyclin Synthase Expression Prevents Murine Lung Cancer. Cancer Res 62: 734-740. (Pubitemid 34126948)
12. Pidgeon GP, Lysaght J, Krishnamoorthy S, Reynolds JV, O'Byrne K, et al. (2007) Lipoxygenase metabolism: roles in tumor progression and survival. Cancer Metastasis Rev 26: 503-524. (Pubitemid 350115127)
13. Gonzalez AL, Roberts RL, Massion PP, Olson SJ, Shyr Y, et al. (2004) 15-Lipoxygenase-2 expression in benign and neoplastic lung: an immunohistochemical study and correlation with tumor grade and proliferation. Hum Pathol 35: 840-849. (Pubitemid 38903077)
14. Panigrahy D, Edin ML, Lee CR, Huang S, Bielenberg DR, et al. (2011) Epoxyeicosanoids stimulate multiorgan metastasis and tumor dormancy escape in mice. J Clin Invest 122: 178-191.
15. Soriano AF, Helfrich B, Chan DC, Heasley LE, Bunn PA, Jr., et al. (1999) Synergistic effects of new chemopreventive agents and conventional cytotoxic agents against human lung cancer cell lines. Cancer Res 59: 6178-6184. (Pubitemid 30035640)
16. Dohadwala M, Batra RK, Luo J, Lin Y, Krysan K, et al. (2002) 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 277: 50828-50833. (Pubitemid 36042248)
17. Dohadwala M, Yang SC, Luo J, Sharma S, Batra RK, et al. (2006) Cyclooxygenase-2-Dependent Regulation of E-Cadherin: Prostaglandin E2 Induces Transcriptional Repressors ZEB1 and Snail in Non-Small Cell Lung Cancer. Cancer Res 66: 5338-5345. (Pubitemid 43844959)
18. Katoh H, Hosono K, Ito Y, Suzuki T, Ogawa Y, et al. (2010) COX-2 and prostaglandin EP3/EP4 signaling regulate the tumor stromal proangiogenic microenvironment via CXCL12-CXCR4 chemokine systems. Am J Pathol 176: 1469-1483.
19. Sharma S, Yang SC, Zhu L, Reckamp K, Gardner B, et al. (2005) Tumor cyclooxygenase-2/prostaglandin E2-dependent promotion of FOXP3 expression and CD4+ CD25+ T regulatory cell activities in lung cancer. Cancer Res 65: 5211-5220. (Pubitemid 40827331)
20. Li H, Sorenson AL, Poczobutt J, Amin J, Joyal T, et al. (2011) Activation of PPARgamma in myeloid cells promotes lung cancer progression and metastasis. PLoS One 6: e28133.
21. Weiser-Evans MC, Wang XQ, 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: 1733-1738.
22. Norris PC, Reichart D, Dumlao DS, Glass CK, Dennis EA (2011) Specificity of eicosanoid production depends on the TLR-4-stimulated macrophage pheno-type. J Leukoc Biol 90: 563-574.
23. Bonventre JV, Huang Z, Taheri MR, O'Leary E, Li E, et al. (1997) Reduced fertility and postischaemic brain injury in mice deficient in cytosolic phospholipase A2. Nature 390: 622-625. (Pubitemid 28016198)
24. Gijon MA, Zarini S, Murphy RC (2007) Biosynthesis of eicosanoids and transcellular metabolism of leukotrienes in murine bone marrow cells. J Lipid Res 48: 716-725. (Pubitemid 46397475)
25. Hall LM, Murphy RC (1998) Electrospray mass spectrometric analysis of 5-hydroperoxy and 5-hydroxyeicosatetraenoic acids generated by lipid peroxidation of red blood cell ghost phospholipids. J Am Soc Mass Spectrom 9: 527-532.
26. Duan M, Li WC, Vlahos R, Maxwell MJ, Anderson GP, et al. (2012) Distinct macrophage subpopulations characterize acute infection and chronic inflammatory lung disease. J Immunol 189: 946-955.
27. Janssen WJ, Barthel L, Muldrow A, Oberley-Deegan RE, Kearns MT, et al. (2011) Fas determines differential fates of resident and recruited macrophages during resolution of acute lung injury. Am J Respir Crit Care Med 184: 547-560.
28. Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, et al. (2012) Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 13: 1118-1128.
29. Nomura DK, Hudak CS, Ward AM, Burston JJ, Issa RS, et al. (2008) Monoacylglycerol lipase regulates 2-arachidonoylglycerol action and arachidonic acid levels. Bioorg Med Chem Lett 18: 5875-5878.
30. Horn L, Backlund M, Johnson DH (2009) Targeting the eicosanoid pathway in non-small-cell lung cancer. Expert Opin Ther Targets 13: 675-688.
31. Singh RK, Gupta S, Dastidar S, Ray A (2010) Cysteinyl leukotrienes and their receptors: molecular and functional characteristics. Pharmacology 85: 336-349.
32. Kenny PA, Lee GY, Bissell MJ (2007) Targeting the tumor microenvironment. Front Biosci 12: 3468-3474.
33. Condeelis J, Pollard JW (2006) Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124: 263-266. (Pubitemid 43121975)
34. Joyce JA, Pollard JW (2009) Microenvironmental regulation of metastasis. Nat Rev Cancer 9: 239-252.
35. Nomura DK, Morrison BE, Blankman JL, Long JZ, Kinsey SG, et al. (2011) Endocannabinoid hydrolysis generates brain prostaglandins that promote neuroinflammation. Science 334: 809-813.
36. Gronich JH, Konieczkowski M, Gelb MH, Nemenoff RA, J.R S (1994) Interleukin-1a causes rapid activation of cytosolic phospholipase A2 by phosphorylation in rat mesangial cells. J Clin Invest 93: 1224-1233.
37. Nemenoff RA, Winitz S, Qian N-X, Van Putten V, Johnson GL, et al. (1993) Phosphorylation and activation of a high molecular weight form of phospholipase A2 by p42 MAP kinase and protein kinase C. J Biol Chem 268: 1960-1964. (Pubitemid 23033600)