Transfer of in vivo primed transgenic T cells supports allergic lung inflammation and FIZZ1 and Ym1 production in an IL-4Rα and STAT6 dependent manner

BMC Immunology

Volumn 12, Issue , 2011, Pages

  Dasgupta, Preeta ^a   Chapoval, Svetlana P ^a   Smith, Elizabeth P ^a   Keegan, Achsah D ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN 20; COLLAGEN; HERMES ANTIGEN; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR; PROTEIN; PROTEIN FIZZ1; PROTEIN YM1; STAT6 PROTEIN; UNCLASSIFIED DRUG; BETA N ACETYLHEXOSAMINIDASE; CELL SURFACE RECEPTOR; CHI3L3 PROTEIN, MOUSE; IL4RA PROTEIN, MOUSE; LECTIN; RETNLA PROTEIN, MOUSE; SIGNAL PEPTIDE;

ALTERNATIVELY ACTIVATED MACROPHAGE GENE; ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; ASTHMA; CD4+ T LYMPHOCYTE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; CYTOKINE RELEASE; EFFECTOR CELL; EOSINOPHILIA; GENE; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PNEUMONIA; PROTEIN EXPRESSION; SMOOTH MUSCLE; T LYMPHOCYTE ACTIVATION; ADOPTIVE TRANSFER; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; COMPLEMENT ALTERNATIVE PATHWAY; DISEASE MODEL; GENETICS; IMMUNOLOGY; LOEFFLER PNEUMONIA; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; PATHOLOGY; SIGNAL TRANSDUCTION; TH2 CELL; TRANSGENIC MOUSE; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD44; ASTHMA; BETA-N-ACETYLHEXOSAMINIDASES; CELLS, CULTURED; COMPLEMENT PATHWAY, ALTERNATIVE; DISEASE MODELS, ANIMAL; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LECTINS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, TRANSGENIC; PNEUMONIA; PULMONARY EOSINOPHILIA; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; STAT6 TRANSCRIPTION FACTOR; TH2 CELLS;

EID: 80054680301     PISSN: None     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/1471-2172-12-60     Document Type: Article

References (69)

1. Kuperman D, Schofield B, Wills-Karp M, Grusby MJ. Signal transducer and activator of transcription factor 6 (Stat6)-deficient mice are protected from antigen-induced airway hyperresponsiveness and mucus production. J Exp Med 1998, 187:939-48. 10.1084/jem.187.6.939, 2212182, 9500796.
2. Corry DB, Grunig G, Hadeiba H, Kurup VP, Warnock ML, Sheppard D, Rennick DM, Locksley RM. Requirements for allergen-induced airway hyperreactivity in T and B cell-deficient mice. Mol Med 1998, 4:344-55. 10.1007/s008940050092, 2230383, 9642684.
3. Cohn L, Homer RJ, Marinov A, Rankin J, Bottomly K. Induction of airway mucus production By T helper 2 (Th2) cells: a critical role for interleukin 4 in cell recruitment but not mucus production. J Exp Med 1997, 186:1737-47. 10.1084/jem.186.10.1737, 2199146, 9362533.
4. Grunig G, Warnock M, Wakil AE, Venkayya R, Brombacher F, Rennick DM, Sheppard D, Mohrs M, Donaldson DD, Locksley RM, Corry DB. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 1998, 282:2261-3.
5. Wills-Karp M, Luyimbazi J, Xu X, Schofield B, Neben TY, Karp CL, Donaldson DD. Interleukin-13: central mediator of allergic asthma. Science 1998, 282:2258-61.
6. Mathew A, MacLean JA, DeHaan E, Tager AM, Green FH, Luster AD. Signal transducer and activator of transcription 6 controls chemokine production and T helper cell type 2 cell trafficking in allergic pulmonary inflammation. J Exp Med 2001, 193:1087-96. 10.1084/jem.193.9.1087, 2193434, 11342593.
7. Kelly-Welch AE, Melo ME, Smith E, Ford AQ, Haudenschild C, Noben-Trauth N, Keegan AD. Complex role of the IL-4 receptor alpha in a murine model of airway inflammation: expression of the IL-4 receptor alpha on nonlymphoid cells of bone marrow origin contributes to severity of inflammation. J Immunol 2004, 172:4545-55.
8. Brusselle GG, Kips JC, Tavernier JH, van der Heyden JG, Cuvelier CA, Pauwels RA, Bluethmann H. Attenuation of allergic airway inflammation in IL-4 deficient mice. Clin Exp Allergy 1994, 24:73-80. 10.1111/j.1365-2222.1994.tb00920.x, 8156448.
9. Foster PS, Hogan SP, Ramsay AJ, Matthaei KI, Young IG. Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damage in a mouse asthma model. J Exp Med 1996, 183:195-201. 10.1084/jem.183.1.195, 2192412, 8551223.
10. Robinson DS, Hamid Q, Ying S, Tsicopoulos A, Barkans J, Bentley AM, Corrigan C, Durham SR, Kay AB. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N Engl J Med 1992, 326:298-304. 10.1056/NEJM199201303260504, 1530827.
11. Li L, Xia Y, Nguyen A, Feng L, Lo D. Th2-induced eotaxin expression and eosinophilia coexist with Th1 responses at the effector stage of lung inflammation. J Immunol 1998, 161:3128-35.
12. Nelms K, Keegan AD, Zamorano J, Ryan JJ, Paul WE. The IL-4 receptor: signaling mechanisms and biologic functions. Annu Rev Immunol 1999, 17:701-38. 10.1146/annurev.immunol.17.1.701, 10358772.
13. Kaplan MH, Schindler U, Smiley ST, Grusby MJ. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 1996, 4:313-9. 10.1016/S1074-7613(00)80439-2, 8624821.
14. Takeda K, Tanaka T, Shi W, Matsumoto M, Minami M, Kashiwamura S, Nakanishi K, Yoshida N, Kishimoto T, Akira S. Essential role of Stat6 in IL-4 signalling. Nature 1996, 380:627-30. 10.1038/380627a0, 8602263.
15. Kabesch M, Schedel M, Carr D, Woitsch B, Fritzsch C, Weiland SK, von Mutius E. IL-4/IL-13 pathway genetics strongly influence serum IgE levels and childhood asthma. J Allergy Clin Immunol 2006, 117:269-74. 10.1016/j.jaci.2005.10.024, 16461126.
16. Tachdjian R, Mathias C, Al Khatib S, Bryce PJ, Kim HS, Blaeser F, O'Connor BD, Rzymkiewicz D, Chen A, Holtzman MJ, Hershey GK, Garn H, Harb H, Renz H, Oettgen HC, Chatila TA. Pathogenicity of a disease-associated human IL-4 receptor allele in experimental asthma. J Exp Med 2009, 206:2191-204. 10.1084/jem.20091480, 2757875, 19770271.
17. Cohn L, Homer RJ, MacLeod H, Mohrs M, Brombacher F, Bottomly K. Th2-induced airway mucus production is dependent on IL-4Ralpha, but not on eosinophils. J Immunol 1999, 162:6178-83.
18. Chapoval SP, Dasgupta P, Smith EP, DeTolla LJ, Lipsky MM, Kelly-Welch AE, Keegan AD. STAT6 expression in multiple cell types mediates the cooperative development of allergic airway disease. J Immunol 2011, 186:2571-83. 10.4049/jimmunol.1002567, 21242523.
19. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003, 3:23-35. 10.1038/nri978, 12511873.
20. Nair MG, Guild KJ, Artis D. Novel effector molecules in type 2 inflammation: lessons drawn from helminth infection and allergy. J Immunol 2006, 177:1393-9. 1780267, 16849442.
21. Holcomb IN, Kabakoff RC, Chan B, Baker TW, Gurney A, Henzel W, Nelson C, Lowman HB, Wright BD, Skelton NJ, Frantz GD, Tumas DB, Peale FV, Shelton DL, Hébert CC. FIZZ1, a novel cysteine-rich secreted protein associated with pulmonary inflammation, defines a new gene family. EMBO J 2000, 19:4046-55. 10.1093/emboj/19.15.4046, 306596, 10921885.
22. Pesce JT, Ramalingam TR, Wilson MS, Mentink-Kane MM, Thompson RW, Cheever AW, Urban JF, Wynn TA. Retnla (relmalpha/fizz1) suppresses helminth-induced Th2-type immunity. PLoS Pathog 2009, 5:e1000393. 10.1371/journal.ppat.1000393, 2663845, 19381262.
23. Stutz AM, Pickart LA, Trifilieff A, Baumruker T, Prieschl-Strassmayr E, Woisetschlager M. The Th2 cell cytokines IL-4 and IL-13 regulate found in inflammatory zone 1/resistin-like molecule alpha gene expression by a STAT6 and CCAAT/enhancer-binding protein-dependent mechanism. J Immunol 2003, 170:1789-96.
24. Welch JS, Escoubet-Lozach L, Sykes DB, Liddiard K, Greaves DR, Glass CK. TH2 cytokines and allergic challenge induce Ym1 expression in macrophages by a STAT6-dependent mechanism. J Biol Chem 2002, 277:42821-9. 10.1074/jbc.M205873200, 12215441.
25. Liu T, Jin H, Ullenbruch M, Hu B, Hashimoto N, Moore B, McKenzie A, Lukacs NW, Phan SH. Regulation of found in inflammatory zone 1 expression in bleomycin-induced lung fibrosis: role of IL-4/IL-13 and mediation via STAT-6. J Immunol 2004, 173:3425-31.
26. Yamaji-Kegan K, Su Q, Angelini DJ, Myers AC, Cheadle C, Johns RA. Hypoxia-Induced Mitogenic Factor (HIMF/FIZZ1/RELM{alpha}) Increases Lung Inflammation and Activates Pulmonary Microvascular Endothelial Cells via an IL-4-Dependent Mechanism. J Immunol
27. Heller NM, Qi X, Junttila IS, Shirey KA, Vogel SN, Paul WE, Keegan AD. Type I IL-4Rs selectively activate IRS-2 to induce target gene expression in macrophages. Sci Signal 2008, 1:ra17. 10.1126/scisignal.1164795, 2739727, 19109239.
28. Zhu J, Paul WE. CD4 T cells: fates, functions, and faults. Blood 2008, 112:1557-69. 10.1182/blood-2008-05-078154, 2518872, 18725574.
29. Paul WE. What determines Th2 differentiation, in vitro and in vivo?. Immunol Cell Biol 2010, 88:236-9. 10.1038/icb.2010.2, 20157328.
30. Merica R, Khoruts A, Pape KA, Reinhardt RL, Jenkins MK. Antigen-experienced CD4 T cells display a reduced capacity for clonal expansion in vivo that is imposed by factors present in the immune host. J Immunol 2000, 164:4551-7.
31. Hataye J, Moon JJ, Khoruts A, Reilly C, Jenkins MK. Naive and memory CD4+ T cell survival controlled by clonal abundance. Science 2006, 312:114-6. 10.1126/science.1124228, 16513943.
32. Laouar Y, Crispe IN. Functional flexibility in T cells: independent regulation of CD4+ T cell proliferation and effector function in vivo. Immunity 2000, 13:291-301. 10.1016/S1074-7613(00)00029-7, 11021527.
33. Holst J, Wang H, Eder KD, Workman CJ, Boyd KL, Baquet Z, Singh H, Forbes K, Chruscinski A, Smeyne R, Smeyne R, van Oers NS, Utz PJ, Vignali DA. Scalable signaling mediated by T cell antigen receptor-CD3 ITAMs ensures effective negative selection and prevents autoimmunity. Nat Immunol 2008, 9:658-66. 10.1038/ni.1611, 18469818.
34. Munitz A, Brandt EB, Mingler M, Finkelman FD, Rothenberg ME. Distinct roles for IL-13 and IL-4 via IL-13 receptor alpha1 and the type II IL-4 receptor in asthma pathogenesis. Proc Natl Acad Sci USA 2008, 105:7240-5. 10.1073/pnas.0802465105, 2386078, 18480254.
35. Bunting KD, Yu WM, Bradley HL, Haviernikova E, Kelly-Welch AE, Keegan AD, Qu CK. Increased numbers of committed myeloid progenitors but not primitive hematopoietic stem/progenitors in mice lacking STAT6 expression. J Leukoc Biol 2004, 76:484-90. 10.1189/jlb.0903440, 15123777.
36. Rothenberg ME. Eotaxin. An essential mediator of eosinophil trafficking into mucosal tissues. Am J Respir Cell Mol Biol 1999, 21:291-5.
37. Zimmermann N, Hogan SP, Mishra A, Brandt EB, Bodette TR, Pope SM, Finkelman FD, Rothenberg ME. Murine eotaxin-2: a constitutive eosinophil chemokine induced by allergen challenge and IL-4 overexpression. J Immunol 2000, 165:5839-46.
38. Zimmermann N, Hershey GK, Foster PS, Rothenberg ME. Chemokines in asthma: cooperative interaction between chemokines and IL-13. J Allergy Clin Immunol 2003, 111:227-42. quiz 243, 10.1067/mai.2003.139, 12589338.
39. Lowenthal JW, Castle BE, Christiansen J, Schreurs J, Rennick D, Arai N, Hoy P, Takebe Y, Howard M. Expression of high affinity receptors for murine interleukin 4 (BSF-1) on hemopoietic and nonhemopoietic cells. J Immunol 1988, 140:456-64.
40. Gavett SH, O'Hearn DJ, Karp CL, Patel EA, Schofield BH, Finkelman FD, Wills-Karp M. Interleukin-4 receptor blockade prevents airway responses induced by antigen challenge in mice. Am J Physiol 1997, 272:L253-61.
41. Humbles AA, Lloyd CM, McMillan SJ, Friend DS, Xanthou G, McKenna EE, Ghiran S, Gerard NP, Yu C, Orkin SH, Gerard C. A critical role for eosinophils in allergic airways remodeling. Science 2004, 305:1776-9. 10.1126/science.1100283, 15375268.
42. Cho JY, Miller M, Baek KJ, Han JW, Nayar J, Lee SY, McElwain K, McElwain S, Friedman S, Broide DH. Inhibition of airway remodeling in IL-5-deficient mice. J Clin Invest 2004, 113:551-60. 338264, 14966564.
43. Liu T, Dhanasekaran SM, Jin H, Hu B, Tomlins SA, Chinnaiyan AM, Phan SH. FIZZ1 stimulation of myofibroblast differentiation. Am J Pathol 2004, 164:1315-26. 10.1016/S0002-9440(10)63218-X, 1615359, 15039219.
44. Chang NC, Hung SI, Hwa KY, Kato I, Chen JE, Liu CH, Chang AC. A macrophage protein, Ym1, transiently expressed during inflammation is a novel mammalian lectin. J Biol Chem 2001, 276:17497-506. 10.1074/jbc.M010417200, 11297523.
45. Henderson WR, Tang LO, Chu SJ, Tsao SM, Chiang GK, Jones F, Jonas M, Pae C, Wang H, Chi EY. A role for cysteinyl leukotrienes in airway remodeling in a mouse asthma model. Am J Respir Crit Care Med 2002, 165:108-16.
46. Rangan GK, Tesch GH. Quantification of renal pathology by image analysis. Nephrology (Carlton) 2007, 12:553-8.
47. Kieper WC, Troy A, Burghardt JT, Ramsey C, Lee JY, Jiang HQ, Dummer W, Shen H, Cebra JJ, Surh CD. Recent immune status determines the source of antigens that drive homeostatic T cell expansion. J Immunol 2005, 174:3158-63.
48. Min B, Yamane H, Hu-Li J, Paul WE. Spontaneous and homeostatic proliferation of CD4 T cells are regulated by different mechanisms. J Immunol 2005, 174:6039-44.
49. Bird JJ, Brown DR, Mullen AC, Moskowitz NH, Mahowald MA, Sider JR, Gajewski TF, Wang CR, Reiner SL. Helper T cell differentiation is controlled by the cell cycle. Immunity 1998, 9:229-37. 10.1016/S1074-7613(00)80605-6, 9729043.
50. Pearson CI, van Ewijk W, McDevitt HO. Induction of apoptosis and T helper 2 (Th2) responses correlates with peptide affinity for the major histocompatibility complex in self-reactive T cell receptor transgenic mice. J Exp Med 1997, 185:583-99. 10.1084/jem.185.4.583, 2196136, 9034138.
51. Chen W, Sayegh MH, Khoury SJ. Mechanisms of acquired thymic tolerance in vivo: intrathymic injection of antigen induces apoptosis of thymocytes and peripheral T cell anergy. J Immunol 1998, 160:1504-8.
52. Eisenbarth SC, Colegio OR, O'Connor W, Sutterwala FS, Flavell RA. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 2008, 453:1122-6. 10.1038/nature06939, 18496530.
53. Paul WE, Zhu J. How are T(H)2-type immune responses initiated and amplified?. Nat Rev Immunol 2010, 10:225-35. 10.1038/nri2735, 20336151.
54. Brewer JM, Conacher M, Hunter CA, Mohrs M, Brombacher F, Alexander J. Aluminium hydroxide adjuvant initiates strong antigen-specific Th2 responses in the absence of IL-4- or IL-13-mediated signaling. J Immunol 1999, 163:6448-54.
55. Hogan SP, Rosenberg HF, Moqbel R, Phipps S, Foster PS, Lacy P, Kay AB, Rothenberg ME. Eosinophils: biological properties and role in health and disease. Clin Exp Allergy 2008, 38:709-50. 10.1111/j.1365-2222.2008.02958.x, 18384431.
56. Randolph DA, Stephens R, Carruthers CJ, Chaplin DD. Cooperation between Th1 and Th2 cells in a murine model of eosinophilic airway inflammation. J Clin Invest 1999, 104:1021-9. 10.1172/JCI7631, 408580, 10525040.
57. Lowenthal JW, MacDonald HR, Iacopetta BJ. Intracellular pathway of interleukin 2 following receptor-mediated endocytosis. Eur J Immunol 1986, 16:1461-3. 10.1002/eji.1830161125, 3096748.
58. Weissman AM, Harford JB, Svetlik PB, Leonard WL, Depper JM, Waldmann TA, Greene WC, Klausner RD. Only high-affinity receptors for interleukin 2 mediate internalization of ligand. Proc Natl Acad Sci USA 1986, 83:1463-6. 10.1073/pnas.83.5.1463, 323096, 3081898.
59. Lloyd CM, Hessel EM. Functions of T cells in asthma: more than just T(H)2 cells. Nat Rev Immunol 10:838-48.
60. Yamaji-Kegan K, Su Q, Angelini DJ, Myers AC, Cheadle C, Johns RA. Hypoxia-induced mitogenic factor (HIMF/FIZZ1/RELMalpha) increases lung inflammation and activates pulmonary microvascular endothelial cells via an IL-4-dependent mechanism. J Immunol 185:5539-48.
61. Nair MG, Gallagher IJ, Taylor MD, Loke P, Coulson PS, Wilson RA, Maizels RM, Allen JE. Chitinase and Fizz family members are a generalized feature of nematode infection with selective upregulation of Ym1 and Fizz1 by antigen-presenting cells. Infect Immun 2005, 73:385-94. 10.1128/IAI.73.1.385-394.2005, 538942, 15618176.
62. Sandler NG, Mentink-Kane MM, Cheever AW, Wynn TA. Global gene expression profiles during acute pathogen-induced pulmonary inflammation reveal divergent roles for Th1 and Th2 responses in tissue repair. J Immunol 2003, 171:3655-67.
63. Owhashi M, Maruyama H, Nawa Y. Kinetic study of eosinophil chemotactic factor production with reference to eosinophilia and granuloma formation in mice infected with Schistosoma japonicum. Int J Parasitol 1996, 26:705-11. 10.1016/0020-7519(96)00054-9, 8894761.
64. Falcone FH, Loke P, Zang X, MacDonald AS, Maizels RM, Allen JE. A Brugia malayi homolog of macrophage migration inhibitory factor reveals an important link between macrophages and eosinophil recruitment during nematode infection. J Immunol 2001, 167:5348-54.
65. Kay AB, Phipps S, Robinson DS. A role for eosinophils in airway remodelling in asthma. Trends Immunol 2004, 25:477-82. 10.1016/j.it.2004.07.006, 15324740.
66. Flood-Page P, Menzies-Gow A, Phipps S, Ying S, Wangoo A, Ludwig MS, Barnes N, Robinson D, Kay AB. Anti-IL-5 treatment reduces deposition of ECM proteins in the bronchial subepithelial basement membrane of mild atopic asthmatics. J Clin Invest 2003, 112:1029-36. 198522, 14523040.
67. Lee CG, Hartl D, Lee GR, Koller B, Matsuura H, Da Silva CA, Sohn MH, Cohn L, Homer RJ, Kozhich AA, Humbles A, Kearley J, Coyle A, Chupp G, Reed J, Flavell RA, Elias JA. Role of breast regression protein 39 (BRP-39)/chitinase 3-like-1 in Th2 and IL-13-induced tissue responses and apoptosis. J Exp Med 2009, 206:1149-66. 10.1084/jem.20081271, 2715037, 19414556.
68. Wang J, Homer RJ, Hong L, Cohn L, Lee CG, Jung S, Elias JA. IL-11 selectively inhibits aeroallergen-induced pulmonary eosinophilia and Th2 cytokine production. J Immunol 2000, 165:2222-31.
69. Kelly-Welch AE, Wang HY, Wang LM, Pierce JH, Jay G, Finkelman F, Keegan AD. Transgenic expression of insulin receptor substrate 2 in murine B cells alters the cell density-dependence of IgE production in vitro and enhances IgE production in vivo. J Immunol 2004, 172:2803-10.