Mast cell 5-lipoxygenase activity promotes intestinal polyposis in APC Δ468 mice

Cancer Research

Volumn 71, Issue 5, 2011, Pages 1627-1636

  Cheon, Eric C ^a,b   Khazaie, Khashayarsha ^c   Khan, Mohammad W ^c   Strouch, Matthew J ^b   Krantz, Seth B ^b   Phillips, Joseph ^b   Blatner, Nichole R ^c   Hix, Laura M ^d   Zhang, Ming ^d   Dennis, Kristen L ^c   Salabat, Mohammed R ^b   Heiferman, Michael ^b   Grippo, Paul J ^b   Munshi, Hidayatullah G ^c,e   Gounaris, Elias ^c   Bentrem, David J ^b,e  

^a UNIVERSITY OF ILLINOIS   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c NORTHWESTERN MEMORIAL HOSPITAL   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; ARACHIDONATE 5 LIPOXYGENASE; ARGINASE 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CARCINOGENESIS; CELL PROLIFERATION; COLON POLYPOSIS; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVITY; GASTROINTESTINAL POLYPOSIS; GENE DELETION; HEMATOPOIETIC CELL; IN VITRO STUDY; INTESTINE EPITHELIUM; MAST CELL; MESENTERY LYMPH NODE; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; SUPPRESSOR CELL; TISSUE SPECIFICITY; TUMOR LOCALIZATION;

ANIMALS; ARACHIDONATE 5-LIPOXYGENASE; CELL SEPARATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENES, APC; INTESTINAL POLYPOSIS; MAST CELLS; MICE; MICE, MUTANT STRAINS;

EID: 79952236009     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-1923     Document Type: Article

References (47)

1. Morris HR, Taylor GW, Piper PJ, Tippins JR. Structure of slow-reacting substance of anaphylaxis from guinea-pig lung. Nature 1980;285:104-6. (Pubitemid 10032836)
2. Murphy RC, Hammarstrom S, Samuelsson B. Leukotriene C: a slow-reacting substance from murine mastocytoma cells. Proc Natl Acad Sci U S A 1979;76:4275-9. (Pubitemid 9256544)
3. Borgeat P, Hamberg M, Samuelsson B. Transformation of arachidonic acid and homo-gamma-linolenic acid by rabbit polymorphonuclear leukocytes. Monohydroxy acids from novel lipoxygenases. J Biol Chem 1976;251:7816-20. (Pubitemid 8015793)
4. Gunning WT, Kramer PM, Steele VE, Pereira MA. Chemoprevention by lipoxygenase and leukotriene pathway inhibitors of vinyl carbamate-induced lung tumors in mice. Cancer Res 2002;62:4199-201. (Pubitemid 34827271)
5. Hennig R, Ding XZ, Tong WG, Schneider MB, Standop J, Friess H, et al. 5-Lipoxygenase and leukotriene B(4) receptor are expressed in human pancreatic cancers but not in pancreatic ducts in normal tissue. Am J Pathol 2002;161:421-8.
6. Hennig R, Grippo P, Ding XZ, Rao SM, Buchler MW, Friess H, et al. 5-Lipoxygenase, a marker for early pancreatic intraepithelial neoplastic lesions. Cancer Res 2005;65:6011-6. (Pubitemid 40994383)
7. Tong WG, Ding XZ, Witt RC, Adrian TE. Lipoxygenase inhibitors attenuate growth of human pancreatic cancer xenografts and induce apoptosis through the mitochondrial pathway. Mol Cancer Ther 2002;1:929-35.
8. Ding XZ, Iversen P, Cluck MW, Knezetic JA, Adrian TE. Lipoxygenase inhibitors abolish proliferation of human pancreatic cancer cells. Biochem Biophys Res Commun 1999;261:218-23. (Pubitemid 29371644)
9. Ding XZ, Kuszynski CA, El-Metwally TH, Adrian TE. Lipoxygenase inhibition induced apoptosis, morphological changes, and carbonic anhydrase expression in human pancreatic cancer cells. Biochem Biophys Res Commun 1999;266:392-9. (Pubitemid 30028679)
10. Melstrom LG, Bentrem DJ, Salabat MR, et al. Overexpression of 5-lipoxygenase in colon polyps and cancer and the effect of 5LOX inhibitors in vitro and in a murine model. Clin Cancer Res 2008;14:6525-30.
11. Ohd JF, Nielsen CK, Campbell J, Landberg G, Lofberg H, Sjolander A. Expression of the leukotriene D4 receptor CysLT1, COX-2, and other cell survival factors in colorectal adenocarcinomas. Gastroenterology 2003;124:57-70.
12. Ohd JF, Wikstrom K, Sjolander A. Leukotrienes induce cell-survival signaling in intestinal epithelial cells. Gastroenterology 2000;119:1007-18.
13. Gounaris E, Erdman SE, Restaino C, Gurish MF, Friend DS, Gounari FS, et al. Mast cells are an essential hematopoietic component for polyp development. Proc Natl Acad Sci U S A 2007;104:19977-82.
14. Blatner NR, Bonertz A, Beckhove P, Cheon EC, Krantz SB, Strouch M, et al. In colorectal cancer mast cells contribute to systemic regulatory T-cell dysfunction. Proc Natl Acad Sci U S A 107:6430-5.
15. Galli SJ, Nakae S, Tsai M. Mast cells in the development of adaptive immune responses. Nat Immunol 2005;6:135-42. (Pubitemid 40268194)
16. Weller CL, Collington SJ, Brown JK, Miller HR, Al-Kashi A, Clark P, et al. Leukotriene B4, an activation product of mast cells, is a chemoattractant for their progenitors. J Exp Med 2005;201:1961-71. (Pubitemid 41002932)
17. Ford-Hutchinson AW, Bray MA, Doig MV, Shipley ME, Smith MJ. Leukotriene B, a potent chemokinetic and aggregating substance released from polymorphonuclear leukocytes. Nature 1980;286:264-5. (Pubitemid 10009985)
18. Ng CF, Sun FF, Taylor BM, Wolin MS, Wong PY. Functional properties of guinea pig eosinophil leukotriene B4 receptor. J Immunol 1991;147:3096-103.
19. Fischer TA, Palmetshofer A, Gambaryan S, Butt E, Jassoy C, Walter U, et al. Activation of cGMP-dependent protein kinase Ibeta inhibits interleukin 2 release and proliferation of T cell receptor-stimulated human peripheral T cells. J Biol Chem 2001;276:5967-74.
20. Kusmartsev S, Nefedova Y, Yoder D, Gabrilovich DI. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J Immunol 2004;172:989-99. (Pubitemid 38113758)
21. Rodriguez PC, Quiceno DG, Zabaleta J, Ortiz B, Zea AH, Piazuelo MB, et al. Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses. Cancer Res 2004;64:5839-49. (Pubitemid 39095585)
22. Pan PY, Wang GX, Yin B, Ozao J, Ku T, Divino CM, et al. Reversion of immune tolerance in advanced malignancy: modulation of myeloid-derived suppressor cell development by blockade of stem-cell factor function. Blood 2008;111:219-28.
23. Ko HJ, Kim YJ, Kim YS, Chang WS, Ko SY, Chang SY, et al. A combination of chemoimmunotherapies can efficiently break self-tolerance and induce antitumor immunity in a tolerogenic murine tumor model. Cancer Res 2007;67:7477-86.
24. Zhang Y, Liu Q, Zhang M, Yu Y, Liu X, Cao X. Fas signal promotes lung cancer growth by recruiting myeloid-derived suppressor cells via cancer cell-derived PGE2. J Immunol 2009;182:3801-8.
25. Huang B, Lei Z, Zhao J, et al. CCL2/CCR2 pathway mediates recruitment of myeloid suppressor cells to cancers. Cancer Lett 2007;252:86-92. (Pubitemid 46734559)
26. Sinha P, Okoro C, Foell D, Freeze HH, Ostrand-Rosenberg S, Srikrishna G. Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells. J Immunol 2008;181:4666-75.
27. Gurish MF, Tao H, Abonia JP, Arya A, Friend DS, Parker CM, et al. Intestinal mast cell progenitors require CD49dbeta7 (alpha4beta7 integrin) for tissue-specific homing. J Exp Med 2001;194:1243-52. (Pubitemid 33055043)
28. D'Abaco GM, Whitehead RH, Burgess AW. Synergy between Apc min and an activated ras mutation is sufficient to induce colon carcinomas. Mol Cell Biol 1996;16:884-91.
29. Goodarzi K, Goodarzi M, Tager AM, Luster AD, von Andrian UH. Leukotriene B4 and BLT1 control cytotoxic effector T cell recruitment to inflamed tissues. Nat Immunol 2003;4:965-73. (Pubitemid 37265917)
30. Gounari F, Chang R, Cowan J, Guo Z, Dose M, Gounaris E, et al. Loss of adenomatous polyposis coli gene function disrupts thymic development. Nat Immunol 2005;6:800-9. (Pubitemid 43090466)
31. Hestdal K, Ruscetti FW, Ihle JN, Jacobsen SE, Dubois CM, Kopp WC, et al. Characterization and regulation of RB6-8C5 antigen expression on murine bone marrow cells. J Immunol 1991;147:22-8.
32. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008;181:5791-802.
33. Yang Z, Zhang B, Li D, et al. Mast cells mobilize myeloid-derived suppressor cells and Treg cells in tumor microenvironment via IL-17 pathway in murine hepatocarcinoma model. PLoS One 5:e8922.
34. Gounaris E, Blatner NR, Dennis K, Magnusson F, Gurish MF, Strom TB, et al. T-regulatory cells shift from a protective anti-inflammatory to a cancer-promoting proinflammatory phenotype in polyposis. Cancer Res 2009;69:5490-7.
35. Paruchuri S, Mezhybovska M, Juhas M, Sjolander A. Endogenous production of leukotriene D4 mediates autocrine survival and proliferation via CysLT1 receptor signalling in intestinal epithelial cells. Oncogene 2006;25:6660-5. (Pubitemid 44646193)
36. Poeckel D, Zemski Berry KA, Murphy RC, Funk CD. Dual 12/15- and 5-lipoxygenase deficiency in macrophages alters arachidonic acid metabolism and attenuates peritonitis and atherosclerosis in ApoE knock-out mice. J Biol Chem 2009;284:21077-89.
37. Sun D, Funk CD. Disruption of 12/15-lipoxygenase expression in peritoneal macrophages. Enhanced utilization of the 5-lipoxygenase pathway and diminished oxidation of low density lipoprotein. J Biol Chem 1996;271:24055-62. (Pubitemid 26327385)
38. Tager AM, Dufour JH, Goodarzi K, Bercury SD, von Andrian UH, Luster AD. BLTR mediates leukotriene B(4)-induced chemotaxis and adhesion and plays a dominant role in eosinophil accumulation in a murine model of peritonitis. J Exp Med 2000;192:439-46.
39. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-74.
40. Peranzoni E, Zilio S, Marigo I, Dolcetti L, Zanovello P, Mandruzzato S, et al. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr Opin Immunol 22:238-44.
41. Sinha P, Clements VK, Fulton AM, Ostrand-Rosenberg S. Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res 2007;67:4507-13. (Pubitemid 46815102)
42. Rodriguez PC, Ochoa AC. Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives. Immunol Rev 2008;222:180-91. (Pubitemid 351430370)
43. Rodriguez PC, Quiceno DG, Ochoa AC. L-arginine availability regulates T-lymphocyte cell-cycle progression. Blood 2007;109:1568-73. (Pubitemid 46239590)
44. Toller IM, Hitzler I, Sayi A, Mueller A. Prostaglandin E2 prevents Helicobacter-induced gastric preneoplasia and facilitates persistent infection in a mouse model. Gastroenterology 138:1455-67, 67e1-4.
45. Cheroutre H. IELs: enforcing law and order in the court of the intestinal epithelium. Immunol Rev 2005;206:114-31. (Pubitemid 41105166)
46. Guy-Grand D, Vassalli P. Gut intraepithelial T lymphocytes. Curr Opin Immunol 1993;5:247-52. (Pubitemid 23125300)
47. Jones TG, Finkelman FD, Austen KF, Gurish MF. T regulatory cells control antigen-induced recruitment of mast cell progenitors to the lungs of C57BL/6 mice. J Immunol 185:1804-11.