Phosphatidylinositol 3-Kinase γ Inhibition Ameliorates Inflammation and Tumor Growth in a Model of Colitis-Associated Cancer

Gastroenterology

Volumn 138, Issue 4, 2010, Pages 1374-1383

  González García, Ana ^a   Sánchez Ruiz, Jesús ^a   Flores, Juana M ^b   Carrera, Ana C ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Colitis; Inflammation Associated Cancer; Inflammatory Bowel Disease; Phosphatidylinositol 3 Kinase

Indexed keywords

DEXTRAN SULFATE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CELL INFILTRATION; CELL POPULATION; COLITIS; COLITIS ASSOCIATED CANCER; COLON; COLORECTAL TUMOR; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; ENTERITIS; ENZYME INHIBITION; FLOW CYTOMETRY; IN VIVO STUDY; INCIDENCE; LEUKOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TUMOR GROWTH; TUMOR LOCALIZATION; TUMOR VOLUME; ULCERATIVE COLITIS;

EID: 77949873730     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2009.12.001     Document Type: Article

References (45)

1. Xavier R.J., and Podolsky D.K. Unravelling the pathogenesis of inflammatory bowel disease. Nature 448 (2007) 427-434
2. Lashner B.A., Silverstein M.D., and Hanauer S.B. Hazard rates for dysplasia and cancer in ulcerative colitis. Results from a surveillance program. Dig Dis Sci 34 (1989) 1536-1541
3. Coussens L.M., and Werb Z. Inflammation and cancer. Nature 420 (2002) 860-867
4. Hirsch E., Katanaev V.L., Garlanda C., et al. Central role for G protein-coupled phosphoinositide 3-kinase γ in inflammation. Science 287 (2000) 1049-1053
5. Okkenhaug K., Bilancio A., Farjot G., et al. Impaired B- and T-cell antigen receptor signaling in p110δ PI 3-kinase mutant mice. Science 297 (2002) 1031-1034
6. Sasaki T., Irie-Sasaki J., Jones R.G., et al. Function of PI3Kγ in thymocyte development, T-cell activation, and neutrophil migration. Science 287 (2000) 1040-1046
7. Vanhaesebroeck B., Leevers S.J., Ahmadi K., et al. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70 (2001) 535-602
8. Stephens L.R., Eguinoa A., Erdjument-Bromage H., et al. The G βγ sensitivity of a PI3K is dependent upon a tightly associated adaptor, p101. Cell 89 (1997) 105-114
9. Suire S., Coadwell J., Ferguson G.J., et al. p84, A new Gβγ-activated regulatory subunit of the type IB phosphoinositide 3-kinase p110γ. Curr Biol 15 (2005) 566-570
10. Alcazar I., Marques M., Kumar A., et al. Phosphoinositide 3-kinase γ participates in T-cell receptor-induced T-cell activation. J Exp Med 204 (2007) 2977-2987
11. Stoyanov B., Volinia S., Hanck T., et al. Cloning and characterization of a G protein-activated human phosphoinositide-3 kinase. Science 269 (1995) 690-693
12. Laffargue M., Calvez R., Finan P., et al. Phosphoinositide 3-kinase γ is an essential amplifier of mast cell function. Immunity 16 (2002) 441-451
13. Barber D.F., Bartolome A., Hernandez C., et al. Class IB-phosphatidylinositol 3-kinase (PI3K) deficiency ameliorates IA-PI3K-induced systemic lupus but not T-cell invasion. J Immunol 176 (2006) 589-593
14. Cooper H.S., Murthy S.N., Shah R.S., et al. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest 69 (1993) 238-249
15. Kitajima S., Takuma S., and Morimoto M. Changes in colonic mucosal permeability in mouse colitis induced with dextran sulfate sodium. Exp Anim 48 (1999) 137-143
16. Okayasu I., Hatakeyama S., Yamada M., et al. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98 (1990) 694-702
17. Okayasu I., Ohkusa T., Kajiura K., et al. Promotion of colorectal neoplasia in experimental murine ulcerative colitis. Gut 39 (1996) 87-92
18. Okayasu I., Yamada M., Mikami T., et al. Dysplasia and carcinoma development in a repeated dextran sulfate sodium-induced colitis model. J Gastroenterol Hepatol 17 (2002) 1078-1083
19. Cooper H.S., Murthy S., Kido K., et al. Dysplasia and cancer in the dextran sulfate sodium mouse colitis model. Relevance to colitis-associated neoplasia in the human: a study of histopathology, B-catenin and p53 expression, and the role of inflammation. Carcinogenesis 21 (2000) 757-768
20. Takahashi T., Nosho K., Yamamoto H., et al. Flat-type colorectal advanced adenomas (laterally spreading tumors) have different genetic and epigenetic alterations from protruded-type advanced adenomas. Mod Pathol 20 (2007) 139-147
21. de Visser K.E., and Coussens L.M. The interplay between innate and adaptive immunity regulates cancer development. Cancer Immunol Immunother 54 (2005) 1143-1152
22. Cassatella M.A. Neutrophil-derived proteins: selling cytokines by the pound. Adv Immunol 73 (1999) 369-509
23. Rugtveit J., Nilsen E.M., Bakka A., et al. Cytokine profiles differ in newly recruited and resident subsets of mucosal macrophages from inflammatory bowel disease. Gastroenterology 112 (1997) 1493-1505
24. Reinecker H.C., Steffen M., Witthoeft T., et al. Enhanced secretion of tumour necrosis factor-α, IL-6, and IL-1β by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn's disease. Clin Exp Immunol 94 (1993) 174-181
25. Murata Y., Ishiguro Y., Itoh J., et al. The role of proinflammatory and immunoregulatory cytokines in the pathogenesis of ulcerative colitis. J Gastroenterol 30 Suppl 8 (1995) 56-60
26. Davidson N.J., Leach M.W., Fort M.M., et al. T helper cell 1-type CD4+ T cells, but not B cells, mediate colitis in interleukin 10-deficient mice. J Exp Med 184 (1996) 241-251
27. Shintani N., Nakajima T., Okamoto T., et al. Involvement of CD4+ T cells in the development of dextran sulfate sodium-induced experimental colitis and suppressive effect of IgG on their action. Gen Pharmacol 31 (1998) 477-481
28. Chen Y., Chou K., Fuchs E., et al. Protection of the intestinal mucosa by intraepithelial γ δ T cells. Proc Natl Acad Sci U S A 99 (2002) 14338-14343
29. Kuhl A.A., Pawlowski N.N., Grollich K., et al. Aggravation of intestinal inflammation by depletion/deficiency of γδ T cells in different types of IBD animal models. J Leukoc Biol 81 (2007) 168-175
30. Abe K., Nguyen K.P., Fine S.D., et al. Conventional dendritic cells regulate the outcome of colonic inflammation independently of T cells. Proc Natl Acad Sci U S A 104 (2007) 17022-17027
31. Berndt B.E., Zhang M., Chen G.H., et al. The role of dendritic cells in the development of acute dextran sulfate sodium colitis. J Immunol 179 (2007) 6255-6262
32. Puri K.D., Doggett T.A., Huang C.Y., et al. The role of endothelial PI3Kγ activity in neutrophil trafficking. Blood 106 (2005) 150-157
33. Vecchione C., Patrucco E., Marino G., et al. Protection from angiotensin II-mediated vasculotoxic and hypertensive response in mice lacking PI3Kγ. J Exp Med 201 (2005) 1217-1228
34. Camps M., Ruckle T., Ji H., et al. Blockade of PI3Kγ suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat Med 11 (2005) 936-943
35. Li Z., Jiang H., Xie W., et al. Roles of PLC-β2 and -β3 and PI3Kγ in chemoattractant-mediated signal transduction. Science 287 (2000) 1046-1049
36. Lupia E., Goffi A., De Giuli P., et al. Ablation of phosphoinositide 3-kinase-γ reduces the severity of acute pancreatitis. Am J Pathol 165 (2004) 2003-2011
37. Bono M.R., Elgueta R., Sauma D., et al. The essential role of chemokines in the selective regulation of lymphocyte homing. Cytokine Growth Factor Rev 18 (2007) 33-43
38. Powrie F., Leach M.W., Mauze S., et al. Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int Immunol 5 (1993) 1461-1471
39. Simpson S.J., Mizoguchi E., Allen D., et al. Evidence that CD4+, but not CD8+, T cells are responsible for murine interleukin-2-deficient colitis. Eur J Immunol 25 (1995) 2618-2625
40. Martin A.L., Schwartz M.D., Jameson S.C., et al. Selective regulation of CD8 effector T-cell migration by the p110 γ isoform of phosphatidylinositol 3-kinase. J Immunol 180 (2008) 2081-2088
41. Waldner M.J., and Neurath M.F. Colitis-associated cancer: the role of T cells in tumor development. Semin Immunopathol 31 (2009) 249-256
42. Carding S.R., and Egan P.J. The importance of γ δ T cells in the resolution of pathogen-induced inflammatory immune responses. Immunol Rev 173 (2000) 98-108
43. Inagaki-Ohara K., Chinen T., Matsuzaki G., et al. Mucosal T cells bearing TCRγδ play a protective role in intestinal inflammation. J Immunol 173 (2004) 1390-1398
44. Del Prete A., Vermi W., Dander E., et al. Defective dendritic cell migration and activation of adaptive immunity in PI3Kγ-deficient mice. EMBO J 23 (2004) 3505-3515
45. Juillerat P., Pittet V., Felley C., et al. Drug safety in Crohn's disease therapy. Digestion 76 (2007) 161-168