PTEN deficiency in mast cells causes a mastocytosis-like proliferative disease that heightens allergic responses and vascular permeability

Blood

Volumn 118, Issue 20, 2011, Pages 5466-5475

  Furumoto, Yasuko ^a   Charles, Nicolas ^a   Olivera, Ana ^a   Leung, Wai Hang ^b   Dillahunt, Sandra ^a   Sargent, Jennifer L ^a   Tinsley, Kevin ^a   Odom, Sandra ^a   Scott, Eric ^a   Wilson, Todd M ^b   Ghoreschi, Kamran ^a   Kneilling, Manfred ^c   Chen, Mei ^d   Lee, David M ^d   Bolland, Silvia ^b   Rivera, Juan ^a  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BCL XL; STAT5 PROTEIN; STEM CELL FACTOR;

ALLERGIC REACTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL DIFFERENTIATION; CELL HYPERPLASIA; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE DELETION; GENE MUTATION; HYPERSENSITIVITY; MAST CELL; MASTOCYTOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 81555208939     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-09-309955     Document Type: Article

References (49)

1. Wedemeyer J, Tsai M, Galli SJ. Role of mast cells and basophils in innate and acquired immunity. Curr Opin Immunol. 2000;12(6):624-631.
2. Williams CM, Galli SJ. The diverse potential effector and immunoregulatory roles of mast cells in allergic disease. J Allergy Clin Immunol. 2000;105(5):847-859. (Pubitemid 30324391)
3. Galli SJ, Kalesnikoff J, Grimbaldeston MA, Piliponsky AM, Williams CM, Tsai M. Mast cells as "tunable" effector and immunoregulatory cells: recent advances. Annu Rev Immunol. 2005;23:749-786. (Pubitemid 40563184)
4. Valent P, Akin C, Escribano L, et al. Standards and standardization in mastocytosis: consensus statements on diagnostics, treatment recommendations and response criteria. Eur J Clin Invest. 2007;37(6):435-453. (Pubitemid 46817344)
5. Akin C, Jaffe ES, Raffeld M, et al. An immunohistochemical study of the bone marrow lesions of systemic mastocytosis: expression of stem cell factor by lesional mast cells. Am J Clin Pathol. 2002;118(2):242-247. (Pubitemid 44698450)
6. Akin C, Metcalfe DD. Systemic mastocytosis. Annu Rev Med. 2004;55:419-432. (Pubitemid 38316735)
7. Munugalavadla V, Sims EC, Chan RJ, Lenz SD, Kapur R. Requirement for p85alpha regulatory subunit of class IA PI3K in myeloproliferative disease driven by an activation loop mutant of KIT. Exp Hematol. 2008;36(3):301-308.
8. Harir N, Boudot C, Friedbichler K, et al. Oncogenic Kit controls neoplastic mast cell growth through a Stat5/PI3-kinase signaling cascade. Blood. 2008;112(6):2463-2473.
9. Chian R, Young S, Danilkovitch-Miagkova A, et al. Phosphatidylinositol 3 kinase contributes to the transformation of hematopoietic cells by the D816V c-Kit mutant. Blood. 2001;98(5):1365-1373.
10. Lu-Kuo JM, Fruman DA, Joyal DM, Cantley LC, Katz HR. Impaired kit- but not FcepsilonRIinitiated mast cell activation in the absence of phosphoinositide 3-kinase p85alpha gene products. J Biol Chem. 2000;275(8):6022-6029. (Pubitemid 30115253)
11. Smith TJ, Ducharme LA, Weis JH. Preferential expression of IL-12 or IL-4 by murine bone marrow mast cells derived in mast cell growth factor or IL-3. Eur J Immunol. 1994;24(4):822-826. (Pubitemid 24093776)
12. Hültner L, Szöts H, Welle M, Van Snick J, Moeller J, Dörmer P. Mouse bone marrowderived IL-3-dependent mast cells and autonomous sublines produce IL-6. Immunology. 1989;67(3):408-413. (Pubitemid 19178862)
13. Gebhardt T, Sellge G, Lorentz A, Raab R, Manns MP, Bischoff SC. Cultured human intestinal mast cells express functional IL-3 receptors and respond to IL-3 by enhancing growth and IgE receptor-dependent mediator release. Eur J Immunol. 2002;32(8):2308-2316. (Pubitemid 34965894)
14. Fox BC, Crew TE, Welham MJ. Phosphoinositide 3-kinases can act independently of p27Kip1 to regulate optimal IL-3-dependent cell cycle progression and proliferation. Cell Signal. 2005;17(4):473-487. (Pubitemid 39643065)
15. Moon JJ, Rubio ED, Martino A, Krumm A, Nelson BH. A permissive role for phosphatidylinositol 3-kinase in the Stat5-mediated expression of cyclin D2 by the interleukin-2 receptor. J Biol Chem. 2004;279(7):5520-5527. (Pubitemid 38220577)
16. Furumoto Y, Brooks S, Olivera A, et al. Cutting edge: lentiviral shRNA silencing of PTEN in human mast cells reveals constitutive signals that promote cytokine secretion and cell survival. J Immunol. 2006;176(9):5167-5171.
17. Brockow K, Jofer C, Behrendt H, Ring J. Anaphylaxis in patients with mastocytosis: a study on history, clinical features and risk factors in 120 patients. Allergy. 2008;63(2):226-232.
18. Parravicini V, Gadina M, Kovarova M, et al. Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat Immunol. 2002;3(8):741-748.
19. Liu FT, Bohn JW, Ferry EL, et al. Monoclonal dinitrophenyl- specific murine IgE antibody: preparation, isolation, and characterization. J Immunol. 1980;124(6):2728-2737. (Pubitemid 10116046)
20. Blank U, Rivera J. Assays for regulated exocytosis of mast cell granules. Curr Protoc Cell Biol. 2006;Chapter 15:Unit 15 11.
21. Lee DM, Friend DS, Gurish MF, Benoist C, Mathis D, Brenner MB. Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science. 2002;297(5587):1689-1692. (Pubitemid 35000781)
22. Olivera A, Eisner C, Kitamura Y, et al. Sphingosine kinase 1 and sphingosine-1-phosphate receptor 2 are vital to recovery from anaphylactic shock in mice. J Clin Invest. 2010;120(5):1429-1440.
23. Di Cristofano A, Pesce B, Cordon-Cardo C, Pandolfi PP. Pten is essential for embryonic development and tumour suppression. Nat Genet. 1998;19(4):348-355. (Pubitemid 28357906)
24. Kalesnikoff J, Huber M, Lam V, et al. Monomeric IgE stimulates signaling pathways in mast cells that lead to cytokine production and cell survival. Immunity. 2001;14(6):801-811. (Pubitemid 32592426)
25. Asai K, Kitaura J, Kawakami Y, et al. Regulation of mast cell survival by IgE. Immunity. 2001;14(6):791-800. (Pubitemid 32592425)
26. Kawakami T, Galli SJ. Regulation of mast-cell and basophil function and survival by IgE. Nat Rev Immunol. 2002;2(10):773-786. (Pubitemid 37328717)
27. Yang TJ. Immunobiology of a spontaneously regressive tumor, the canine transmissible venereal sarcoma [review]. Anticancer Res. 1988;8(1):93-95.
28. Bos JL. A target for phosphoinositide 3-kinase: Akt/PKB. Trends Biochem Sci. 1995;20(11):441-442.
29. Jahn T, Leifheit E, Gooch S, Sindhu S,Weinberg K. Lipid rafts are required for Kit survival and proliferation signals. Blood. 2007;110(6):1739- 1747. (Pubitemid 47443883)
30. Shivakrupa R, Linnekin D. Lyn contributes to regulation of multiple Kit-dependent signaling pathways in murine bone marrow mast cells. Cell Signal. 2005;17(1):103-109. (Pubitemid 39286785)
31. Hundley TR, Gilfillan AM, Tkaczyk C, Andrade MV, Metcalfe DD, Beaven MA. Kit and FcepsilonRI mediate unique and convergent signals for release of inflammatory mediators from human mast cells. Blood. 2004;104(8):2410-2417. (Pubitemid 39331841)
32. Barnstein BO, Li G, Wang Z, et al. Stat5 expression is required for IgE-mediated mast cell function. J Immunol. 2006;177(5):3421-3426. (Pubitemid 44277863)
33. Shelburne CP, McCoy ME, Piekorz R, et al. Stat5 expression is critical for mast cell development and survival. Blood. 2003;102(4):1290-1297. (Pubitemid 36988035)
34. Ryan JJ, Huang H, McReynolds LJ, et al. Stem cell factor activates STAT-5 DNA binding in IL-3-derived bone marrow mast cells. Exp Hematol. 1997;25(4):357-362. (Pubitemid 27236662)
35. Zuluaga Toro T, Hsieh FH, Bodo J, Dong HY, Hsi ED. Detection of phospho-STAT5 in mast cells: a reliable phenotypic marker of systemic mast cell disease that reflects constitutive tyrosine kinase activation. Br J Haematol. 2007;139(1):31-40. (Pubitemid 47389913)
36. Baumgartner C, Cerny-Reiterer S, Sonneck K, et al. Expression of activated STAT5 in neoplastic mast cells in systemic mastocytosis: subcellular distribution and role of the transforming oncoprotein KIT D816V. Am J Pathol. 2009;175(6):2416-2429.
37. Aichberger KJ, Gleixner KV, Mirkina I, et al. Identification of proapoptotic Bim as a tumor suppressor in neoplastic mast cells: role of KIT D816V and effects of various targeted drugs. Blood. 2009;114(26):5342-5351.
38. Akin C. Recent advances in mast cell clonality and anaphylaxis. F1000 Med Rep. 2009;1:97.
39. Kneilling M, Hultner L, Pichler BJ, et al. Targeted mast cell silencing protects against joint destruction and angiogenesis in experimental arthritis in mice. Arthritis Rheum. 2007;56(6):1806-1816. (Pubitemid 47110380)
40. Mickys U, Barakauskiene A, De Wolf-Peeters C, Geboes K, De Hertogh G. Aggressive systemic mastocytosis complicated by protein-losing enteropathy. Dig Liver Dis. 2007;39(7):693-697. (Pubitemid 46888203)
41. Iwaki S, Spicka J, Tkaczyk C, et al. Kit- and Fc epsilonRI-induced differential phosphorylation of the transmembrane adaptor molecule NTAL/LAB/LAT2 allows flexibility in its scaffolding function in mast cells. Cell Signal. 2008;20(1):195-205. (Pubitemid 350138381)
42. Gilfillan AM, Tkaczyk C. Integrated signalling pathways for mast-cell activation. Nat Rev Immunol. 2006;6(3):218-230. (Pubitemid 43290991)
43. Huber M, Helgason CD, Scheid MP, Duronio V, Humphries RK, Krystal G. Targeted disruption of SHIP leads to Steel factor-induced degranulation of mast cells. EMBO J. 1998;17(24):7311-7319. (Pubitemid 29002700)
44. Shelburne CP, McCoy ME, Piekorz R, et al. Stat5: an essential regulator of mast cell biology. Mol Immunol. 2002;38(16):1187-1191. (Pubitemid 35264526)
45. Li G, Miskimen KL, Wang Z, et al. STAT5 requires the N-domain for suppression of miR15/16, induction of bcl-2, and survival signaling in myeloproliferative disease. Blood. 2010;115(7):1416-1424.
46. Nyga R, Pecquet C, Harir N, et al. Activated STAT5 proteins induce activation of the PI 3-kinase/Akt and Ras/MAPK pathways via the Gab2 scaffolding adapter. Biochem J. 2005;390(1):359-366. (Pubitemid 41192263)
47. Li J, Yen C, Liaw D, et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science. 1997;275(5308):1943-1947. (Pubitemid 27148818)
48. Lu TL, Chang JL, Liang CC, You LR, Chen CM. Tumor spectrum, tumor latency and tumor incidence of the Pten-deficient mice. PLoS One. 2007;2(11):e1237.
49. Fearfield LA, Francis N, Henry K, Costello C, Bunker CB. Bone marrow involvement in cutaneous mastocytosis. Br J Dermatol. 2001;144(3):561-566. (Pubitemid 32232012)