Determinants of eosinophil survival and apoptotic cell death

Apoptosis

Volumn 20, Issue 2, 2015, Pages 224-234

  Shen, Zhong Jian ^a   Malter, James S ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Asthma; Cytokines; Eosinophils; Prolyl isomerase Pin1; Signal transduction

Indexed keywords

CYTOKINE; DEATH RECEPTOR; FAS ASSOCIATED DEATH DOMAIN PROTEIN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 5 RECEPTOR; LIGAND; PEPTIDYLPROLYL ISOMERASE PIN1; PROTEIN BAX; APOPTOSIS REGULATORY PROTEIN; NIMA-INTERACTING PEPTIDYLPROLYL ISOMERASE; PEPTIDYLPROLYL ISOMERASE;

APOPTOSIS; ARTICLE; CELL SURVIVAL; ENZYME ACTIVATION; EOSINOPHIL; EOSINOPHIL SURVIVAL; GRANULOCYTE FUNCTION; HUMAN; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; PHYSIOLOGY;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL SURVIVAL; CYTOKINES; EOSINOPHILS; HUMANS; PEPTIDYLPROLYL ISOMERASE; SIGNAL TRANSDUCTION;

EID: 84925515946     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-014-1072-2     Document Type: Article

References (103)

1. Holgate ST (2012) Innate and adaptive immune responses in asthma. Nat Med 18(5):673-683
2. Fulkerson PC, Rothenberg ME (2013) Targeting eosinophils in allergy, inflammation and beyond. Nat Rev Drug Discov 12(2):117-129
3. Rothenberg ME, Hogan SP (2006) The eosinophil. Annu Rev Immunol 24:147-174
4. Bochner BS, Gleich GJ (2010) What targeting eosinophils has taught us about their role in diseases. 126(1):16-25
5. Walsh GM (2000) Eosinophil apoptosis: mechanisms and clinical relevance in asthmatic and allergic inflammation. Br J Haematol 111(1):61-67
6. Caramori G, Adcock I (2005) Anti-inflammatory mechanisms of glucocorticoids targeting granulocytes. Curr Drug Targets Inflamm Allergy 4(4):455-463
7. Colice GL (2011) Emerging therapeutic options for asthma. Am J Manag Care 17(Suppl 3):S82-S89
8. Iversen PO, Robinson D, Ying S, Meng Q, Kay AB, Clark-Lewis I, Lopez AF (1997) The GM-CSF analogue E21R induces apoptosis of normal and activated eosinophils. Am J Respir Crit Care Med 156(5):1628-1632
9. Wong CK, Zhang J, Ip WK, Lam CW (2002) Intracellular signal transduction in eosinophils and its clinical significance. Immunopharmacol Immunotoxicol 24(2):165-186
10. Simon HU, Yousefi S, Dibbert B, Hebestreit H, Weber M, Branch DR, Blaser K, Levi-Schaffer F, Anderson GP (1998) Role for tyrosine phosphorylation and Lyn tyrosine kinase in fas receptor-mediated apoptosis in eosinophils. Blood 92(2):547-557
11. Simon HU, Yousefi S, Dibbert B, Levi-Schaffer F, Blaser K (1997) Anti-apoptotic signals of granulocyte-macrophage colony-stimulating factor are transduced via Jak2 tyrosine kinase in eosinophils. Eur J Immunol 27(12):3536-3539
12. Wedi B, Straede J, Wieland B, Kapp A (1999) Eosinophil apoptosis is mediated by stimulators of cellular oxidative metabolisms and inhibited by antioxidants: involvement of a thiol-sensitive redox regulation in eosinophil cell death. Blood 94(7):2365-2373
13. Luttmann W, Knoechel B, Foerster M, Matthys H, Virchow JC Jr, Kroegel C (1996) Activation of human eosinophils by IL-13. Induction of CD69 surface antigen, its relationship to messenger RNA expression, and promotion of cellular viability. J Immunol 157(4):1678-1683
14. Horie S, Okubo Y, Hossain M, Sato E, Nomura H, Koyama S, Suzuki J, Isobe M, Sekiguchi M (1997) Interleukin-13 but not interleukin-4 prolongs eosinophil survival and induces eosinophilchemotaxis. Intern Med 36(3):179-185
15. Shakoory B, Fitzgerald SM, Lee SA, Chi DS, Krishnaswamy G (2004) The role of human mast cell-derived cytokines in eosinophil biology. J Interferon Cytokine Res 24(5):271-281
16. Knobloch J, Peters H, Jungck D, Müller K, Strauch J, Koch A (2009) TNFalpha-induced GM-CSF release from human airway smooth muscle cells depends on activation of an ET-1 autoregulatory positive feedback mechanism. Thorax 64(12):1044-1052
17. Vignola AM, Chanez P, Chiappara G, Siena L, Merendino A, Reina C, Gagliardo R, Profita M, Bousquet J, Bonsignore G (1999) Evaluation of apoptosis of eosinophils, macrophages, and T lymphocytes in mucosal biopsy specimens of patients with asthma and chronic bronchitis. J Allergy Clin Immunol 103(4):563-573
18. Takatsu K, Nakajima H (2008) IL-5 and eosinophilia. Curr Opin Immunol 20(3):288-294
19. Zhu Z, Lee CG, Zheng T, Chupp G, Wang J, Homer RJ, Noble PW, Hamid Q, Elias JA, Airway inflammation and remodeling in asthma (2001) Lessons from interleukin 11 and interleukin 13transgenic mice. Am J Respir Crit Care Med 164(10 Pt 2):S67-S70
20. Ingram JL, Kraft M (2012) IL-13 in asthma and allergic disease: asthma phenotypes and targeted therapies. J Allergy Clin Immunol 130(4):829-842
21. Flood-Page P, Menzies-Gow A, Phipps S, Ying S, Wangoo A, Ludwig MS, Barnes N, Robinson D, Kay AB (2003) Anti-IL-5 treatment reduces deposition of ECM proteins in the bronchial subepithelial basement membrane of mild atopic asthmatics. J Clin Invest. 112(7):1029-1036
22. Conus S, Bruno A, Simon HU (2005) Leptin is an eosinophil survival factor. J Allergy Clin Immunol. 116(6):1228-1234
23. Temkin V, Levi-Schaffer F (2001) Mechanism of tumour necrosis factor alpha mediated eosinophil survival. Cytokine 15(1):20-26
24. Suzukawa M, Koketsu R, Iikura M, Nakae S, Matsumoto K, Nagase H, Saito H, Matsushima K, Ohta K, Yamamoto K, Yamaguchi M (2008) Interleukin-33 enhances adhesion, CD11b expression and survival in human eosinophils. Lab Invest 88(11):1245-1253
25. Ochiai K, Tanabe E, Ishihara C, Kagami M, Sugiyama T, Sueishi M, Koya N, Tomioka H (1999) Role of JAK2 signal transductional pathway in activation and survival of human peripheral eosinophils by interferon-gamma (IFN-gamma). Clin Exp Immunol 118(3):340-343
26. Esnault S, Malter JS (2003) Hyaluronic acid or TNF-alpha plus fibronectin triggers granulocyte macrophage-colony-stimulating factor mRNA stabilization in eosinophils yet engages differential intracellular pathways and mRNA binding proteins. J Immunol 171(12):6780-6787
27. Cherry WB, Yoon J, Bartemes KR, Iijima K, Kita H (2008) A novel IL-1 family cytokine, IL-33, potently activates human eosinophils. J Allergy Clin Immunol 121(6):1484-1490
28. Chow JY, Wong CK, Cheung PF, Lam CW (2010) Intracellular signaling mechanisms regulating the activation of human eosinophils by the novel Th2 cytokine IL-33: implications for allergic inflammation. Cell Mol Immunol 7(1):26-34
29. Fujisawa T, Fukuda S, Atsuta J, Ichimi R, Kamiya H, Sakurai M (1994) Interferon-gamma induces interleukin-3 release from peripheral blood eosinophils. Int Arch Allergy Immunol 104 Suppl 1(1):41-43
30. Létuvé S, Druilhe A, Grandsaigne M, Aubier M, Pretolani M (2001) Involvement of caspases and of mitochondria in Fas ligation-induced eosinophil apoptosis: modulation by interleukin-5 and interferon-gamma. J Leukoc Biol 70(5):767-775
31. Druilhe A, Arock M, Le Goff L, Pretolani M (1998) Human eosinophils express bcl-2 family proteins: modulation of Mcl-1 expression by IFN-gamma. Am J Respir Cell Mol Biol 18(3):315-322
32. Barin JG, Baldeviano GC, Talor MV, Wu L, Ong S, Fairweather D, Bedja D, Stickel NR, Fontes JA, Cardamone AB, Zheng D, Gabrielson KL, Rose NR, Ciháková D (2013) Fatal eosinophilic myocarditis develops in the absence of IFN-γ and IL-17A. J Immunol 191(8):4038-4047
33. Alam R, Forsythe P, Stafford S, Fukuda Y (1994) Transforming growth factor beta abrogates the effects of hematopoietins on eosinophils and induces their apoptosis. J Exp Med 179(3):1041-1045
34. Goplen N, Gorska MM, Stafford SJ, Rozario S, Guo L, Liang Q, Alam R (2008) A phosphosite screen identifies autocrine TGF-beta-driven activation of protein kinase R as a survival-limiting factor for eosinophils. J Immunol 180(6):4256-4264
35. Halwani R, Al-Muhsen S, Al-Jahdali H, Hamid Q (2011) Role of transforming growth factor-β in airway remodeling in asthma. Am J Respir Cell Mol Biol 44(2):127-133
36. Kanzaki M, Shibagaki N, Hatsushika K, Mitsui H, Inozume T, Okamoto A, Dobashi Y, Ogawa H, Shimada S, Nakao A (2007) Human eosinophils have an intact Smad signaling pathway leading to a major transforming growth factor-beta target gene expression. Int Arch Allergy Immunol 142(4):309-317
37. Pazdrak K, Justement L, Alam R (1995) Mechanism of inhibition of eosinophil activation by transforming growth factor-beta. Inhibition of Lyn, MAP, Jak2 kinases and STAT1 nuclear factor. J Immunol 155(9):4454-4458
38. Xie Q, Shen ZJ, Oh J, Chu H, Malter JS (2011) Transforming Growth Factor-β1 Antagonizes Interleukin-5 Pro-Survival Signaling by Activating Calpain-1 in Primary Human Eosinophils. J Clin Cell Immunol. Suppl 1. pii: 003
39. Altznauer F, Conus S, Cavalli A, Folkers G, Simon HU (2004) Calpain-1 regulates Bax and subsequent Smac-dependent caspase-3 activation in neutrophil apoptosis. J Biol Chem 279(7):5947-5957
40. Squier MK, Sehnert AJ, Sellins KS, Malkinson AM, Takano E, Cohen JJ (1999) Calpain and calpastatin regulate neutrophil apoptosis. J Cell Physiol 178(3):311-319
41. Hebestreit H, Yousefi S, Balatti I, Weber M, Crameri R, Simon D, Hartung K, Schapowal A, Blaser K, Simon HU (1996) Expression and function of the Fas receptor on human blood and tissue eosinophils. Eur J Immunol 26(8):1775-1780
42. Tsuyuki S, Bertrand C, Erard F, Trifilieff A, Tsuyuki J, Wesp M, Andersen GP, Coyle AJ (1995) Activation of the Fas receptor on lung eosinophils leads to apoptosis and the resolution of eosinophilic inflammation of the airways. J Clin Invest 96:2924-2931
43. Druilhe A, Wallaert B, Tsicopoulos A, Lapa e Silva JR, Tillie-Leblond I, Tonnel AB, Pretolani M (1998) Apoptosis, proliferation, and expression of Bcl-2, Fas, and Fas ligand in bronchial biopsies from asthmatics. Am J Respir Cell Mol Biol 19(5):747-757
44. Bochner BS (2009) Siglec-8 on human eosinophils and mast cells, and Siglec-F on murine eosinophils, are functionally related inhibitory receptors. Clin Exp Allergy 39(3):317-324
45. Kiwamoto T, Katoh T, Tiemeyer M, Bochner BS (2013) The role of lung epithelial ligands for Siglec-8 and Siglec-F in eosinophilic inflammation. Curr Opin Allergy Clin Immunol 13(1):106-111
46. Zangrilli J, Robertson N, Shetty A, Wu J, Hastie A, Fish JE, Litwack G, Peters SP (2000) Effect of IL-5, glucocorticoid, and Fas ligation on Bcl-2 homologue expression and caspase activation in circulating human eosinophils. Clin Exp Immunol 120(1):12-21
47. Ochiai K, Kagami M, Matsumura R, Tomioka H (1997) IL-5 but not interferon-gamma (IFN-gamma) inhibits eosinophil apoptosis by up-regulation of bcl-2 expression. Clin Exp Immunol 107(1):198-204
48. Simon HU (2001) Regulation of eosinophil and neutrophil apoptosis-similarities and differences. Immunol Rev 179:156-162
49. Dewson G, Walsh GM, Wardlaw AJ (1999) Expression of Bcl-2 and its homologues in human eosinophils. Modulation by interleukin-5. Am J Respir Cell Mol Biol 20(4):720-728
50. Temple R, Allen E, Fordham J, Phipps S, Schneider HC, Lindauer K, Hayes I, Lockey J, Pollock K, Jupp R (2001) Microarray analysis of eosinophils reveals a number of candidate survival and apoptosis genes. Am J Respir Cell Mol Biol 25(4):425-433
51. Esnault S, Malter JS (2001) Granulocyte macrophage-colony-stimulating factor mRNA is stabilized in airway eosinophils and peripheral blood eosinophils activated by TNF-alpha plus fibronectin. J Immunol 166(7):4658-4663
52. Shen ZJ, Esnault S, Malter JS (2005) The peptidyl-prolyl isomerase Pin1 regulates the stability of granulocyte-macrophage colony-stimulating factor mRNA in activated eosinophils. Nat Immunol 6(12):1280-1287
53. Shen ZJ, Esnault S, Schinzel A, Borner C, Malter JS (2009) The peptidyl-prolyl isomerase Pin1 facilitates cytokine-induced survival of eosinophils by suppressing Bax activation. Nat Immunol 10(3):257-265
54. Pinho V, Souza DG, Barsante MM, Hamer FP, De Freitas MS, Rossi AG, Teixeira MM (2005) Phosphoinositide-3 kinases critically regulate the recruitment and survival of eosinophils in vivo: importance for the resolution of allergic inflammation. J Leukoc Biol 77(5):800-810
55. Duan W, Aguinaldo Datiles AM, Leung BP, Vlahos CJ, Wong WS (2005) An anti-inflammatory role for a phosphoinositide 3-kinase inhibitor LY294002 in a mouse asthma model. Int Immunopharmacol 5(3):495-502
56. Andina N, Didichenko S, Schmidt-Mende J, Dahinden CA, Simon HU (2009) Proviral integration site for Moloney murine leukemia virus 1, but not phosphatidylinositol-3 kinase, is essential in the antiapoptotic signaling cascade initiated by IL-5 in eosinophils. J Allergy Clin Immunol 123(3):603-611
57. Nagase H, Okugawa S, Ota Y, Yamaguchi M, Tomizawa H, Matsushima K, Ohta K, Yamamoto K, Hirai K (2003) Expression and function of Toll-like receptors in eosinophils: activation by Toll-like receptor 7 ligand. J Immunol 171(8):3977-3982
58. Kvarnhammar AM, Cardell LO (2012) Pattern-recognition receptors in human eosinophils. Immunology 136(1):11-20
59. Hiraguchi Y, Tanida H, Hosoki K, Nagao M, Tokuda R, Fujisawa T (2011) Inhibition of eosinophil activation mediated by a Toll-like receptor 7 ligand with a combination of procaterol and budesonide. Int Arch Allergy Immunol 155(Suppl 1):85-89
60. Wong CK, Cheung PF, Ip WK, Lam CW (2007) Intracellular signaling mechanisms regulating toll-like receptor-mediated activation of eosinophils. Am J Respir Cell Mol Biol 37(1):85-96
61. Zarember KA, Godowski PJ (2002) Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J Immunol 168(2):554-561
62. Sabroe I, Jones EC, Usher LR, Whyte MK, Dower SK (2002) Toll-like receptor (TLR)2 and TLR4 in human peripheral blood granulocytes: a critical role for monocytes in leukocyte lipopolysaccharide responses. J Immunol 168(9):4701-4710
63. Phipps S, Lam CE, Mahalingam S, Newhouse M, Ramirez R, Rosenberg HF, Foster PS, Matthaei KI (2007) Eosinophils contribute to innate antiviral immunity and promote clearance of respiratory syncytial virus. Blood 110(5):1578-1586
64. Månsson A, Cardell LO (2009) Role of atopic status in Toll-like receptor (TLR)7- and TLR9-mediated activation of human eosinophils. J Leukoc Biol 85(4):719-727
65. Månsson A, Fransson M, Adner M, Benson M, Uddman R, Björnsson S, Cardell LO (2010) TLR3 in human eosinophils: functional effects and decreased expression during allergic rhinitis. Int Arch Allergy Immunol 151(2):118-128
66. Plötz SG, Lentschat A, Behrendt H, Plötz W, Hamann L, Ring J, Rietschel ET, Flad HD, Ulmer AJ (2001) The interaction of human peripheral blood eosinophils with bacterial lipopolysaccharide is CD14 dependent. Blood 97(1):235-241
67. Ilmarinen P, Hasala H, Sareila O, Moilanen E, Kankaanranta H (2009) Bacterial DNA delays human eosinophil apoptosis. Pulm Pharmacol Ther 22(3):167-176
68. Mattsson E, Persson T, Andersson P, Rollof J, Egesten A (2003) Peptidoglycan induces mobilization of the surface marker for activation marker CD66b in human neutrophils but not in eosinophils. Clin Diagn Lab Immunol 10(3):485-488
69. Cheung PF, Wong CK, Ip WK, Lam CW (2008) FAK-mediated activation of ERK for eosinophil migration: a novel mechanism for infection-induced allergic inflammation. Int Immunol 20(3):353-363
70. Esnault S, Shen ZJ, Malter JS (2008) Pinning down signaling in the immune system: the role of the peptidyl-prolyl isomerase Pin1 in immune cell function. Crit Rev Immunol 28(1):45-60
71. Pastorino L, Sun A, Lu PJ, Zhou XZ, Balastik M, Finn G, Wulf G, Lim J, Li SH, Li X, Xia W, Nicholson LK, Lu KP (2006) The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-beta production. Nature 440:528-534
72. Yao JL, Kops O, Lu PJ, Lu KP (2001) Functional conservation of hosphorylation-specific prolyl isomerases in plants. J Biol Chem 276(17):13517-13523
73. Landrieu I, De Veylder L, Fruchart JS, Odaert B, Casteels P, Portetelle D, Van Montagu M, Inzé D, Lippens G (2000) The Arabidopsis thaliana PIN1At gene encodes a single-domain phosphorylation-dependent peptidyl prolyl cis/trans isomerase. J Biol Chem 275(14):10577-10581
74. Liou YC, Zhou XZ, Lu KP (2011) Prolyl isomerase Pin1 as a molecular switch to determine the fate of phosphoproteins. Trends Biochem Sci 36(10):501-514
75. Lee TH, Pastorino L, Lu KP (2011) Peptidyl-prolyl cis-trans isomerase Pin1 in ageing, cancer and Alzheimer disease. Expert Rev Mol Med 13:e21
76. Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP (1999) The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature 399(6738):784-788
77. Butterfield DA, Abdul HM, Opii W, Newman SF, Joshi G, Ansari MA, Sultana R (2006) Pin1 in Alzheimer's disease. J Neurochem 98(6):1697-1706
78. Theuerkorn M, Fischer G, Schiene-Fischer C (2011) Prolyl cis/trans isomerase signalling pathways in cancer. Curr Opin Pharmacol 11(4):281-287
79. Oh J, Malter JS (2013) Pin1-FADD interactions regulate Fas-mediated apoptosis in activated eosinophils. J Immunol 190(10):4937-4945
80. Pathan N, Aime-Sempe C, Kitada S, Haldar S, Reed JC (2001) Microtubule-targeting drugs induce Bcl-2 phosphorylation and association with Pin1. Neoplasia 3(1):70-79
81. Basu A, Das M, Qanungo S, Fan XJ, DuBois G, Haldar S (2002) Proteasomal degradation of human peptidyl prolyl isomerase pin1-pointing phospho Bcl2 toward dephosphorylation. Neoplasia 4(3):218-227
82. Pathan N, Aime-Sempe C, Kitada S, Basu A, Haldar S, Reed JC (2001) Microtubule-targeting drugs induce bcl-2 phosphorylation and association with Pin1. Neoplasia 3(6):550-559
83. Geijsen N, Koenderman L, Coffer PJ (2001) Specificity in cytokine signal transduction: lessons learned from the IL-3/IL-5/GM-CSF receptor family. Cytokine Growth Factor Rev 12(1):19-25
84. Stout BA, Bates ME, Liu LY, Farrington NN, Bertics PJ (2004) IL-5 and granulocyte-macrophage colony-stimulating factor activate STAT3 and STAT5 and promote Pim-1 and cyclin D3 protein expression in human eosinophils. J mmunol 173(10):6409-6417
85. Dewson G, Cohen GM, Wardlaw AJ (2001) Interleukin-5 inhibits translocation of Bax to the mitochondria, cytochrome c release, and activation of caspases in human eosinophils. Blood 98(7):2239-2247
86. Gardai SJ, Hildeman DA, Frankel SK, Whitlock BB, Frasch SC, Borregaard N, Marrack P, Bratton DL, Henson PM (2004) Phosphorylation of Bax Ser184 by Akt regulates its activity and apoptosis in neutrophils. J Biol Chem 279(20):21085-21095
87. Kim BJ, Ryu SW, Song BJ (2006) JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J Biol Chem 281(30):21256-21265
88. Zhang XD, Borrow JM, Zhang XY, Nguyen T, Hersey P (2003) Activation of ERK1/2 protects melanoma cells from TRAIL-induced apoptosis by inhibiting Smac/DIABLO release from mitochondria. Oncogene 22(19):2869-2881
89. Li Y, Yokota T, Gama V, Yoshida T, Gomez JA, Ishikawa K, Sasaguri H, Cohen HY, Sinclair DA, Mizusawa H, Matsuyama S (2007) Bax-inhibiting peptide protects cells from polyglutamine toxicity caused by Ku70 acetylation. Cell Death Differ 14(12):2058-2067
90. Guo B, Zhai D, Cabezas E, Welsh K, Nouraini S, Satterthwait AC, Reed JC (2003) Humanin peptide suppresses apoptosis by interfering with Bax activation. Nature 423(6938):456-461
91. Zhang H, Kim JK, Edwards CA, Xu Z, Taichman R, Wang CY (2005) Clusterin inhibits apoptosis by interacting with activated Bax. Nat Cell Biol 7(9):909-915
92. Jang MS, Lee SJ, Kim CJ, Lee CW, Kim E (2011) Phosphorylation by polo-like kinase 1 induces the tumor-suppressing activity of FADD. Oncogene 30(4):471-481
93. Alappat EC, Feig C, Boyerinas B, Volkland J, Samuels M, Murmann AE, Thorburn A, Kidd VJ, Slaughter CA, Osborn SL, Winoto A, Tang WJ, Peter ME (2005) Phosphorylation of FADD at serine 194 by CKIalpha regulates its nonapoptotic activities. Mol Cell 19(3):321-332
94. Levi-Schaffer F, Temkin V, Malamud V, Feld S, Zilberman Y (1998) Mast cells enhance eosinophil survival in vitro: role of TNF-alpha and granulocyte-macrophage colony-stimulating factor. J Immunol 160(11):5554-5562
95. Hallsworth MP, Soh CP, Twort CH, Lee TH, Hirst SJ (1998) Cultured human airway smooth muscle cells stimulated by interleukin-1beta enhance eosinophil survival. Am J Respir Cell Mol Biol 19(6):910-919
96. Esnault S, Malter JS (2002) GM-CSF regulation in eosinophils. Arch Immunol Ther Exp (Warsz) 50(2):121-130
97. Esnault S, Shen ZJ, Whitesel E, Malter JS (2006) The peptidyl-prolyl isomerase Pin1 regulates granulocyte-macrophage colony-stimulating factor mRNA stability in T lymphocytes. J Immunol 177(10):6999-7006
98. Lang RA, Metcalf D, Cuthbertson RA, Lyons I, Stanley E, Kelso A, Kannourakis G, Williamson DJ, Klintworth GK, Gonda TJ et al (1987) Transgenic mice expressing a hemopoietic growth factor gene (GM-CSF) develop accumulations of macrophages, blindness, and a fatal syndrome of tissue damage. Cell 51(4):675-686
99. Biondo M, Nasa Z, Marshall A, Toh BH, Alderuccio F (2001) Local transgenic expression of granulocyte macrophage-colony stimulating factor initiates autoimmunity. J Immunol 166(3):2090-2099
100. Johnson GR, Gonda TJ, Metcalf D, Hariharan IK, Cory S (1989) A lethal myeloproliferative syndrome in mice transplanted with bone marrow cells infected with a retrovirus expressing granulocyte-macrophage colony stimulating factor. EMBO J 8(2):441-448
101. Xing Z, Ohkawara Y, Jordana M, Graham F, Gauldie J (1996) Transfer of granulocyte-macrophage colony-stimulating factor gene to rat lung induces eosinophilia, monocytosis, and fibrotic reactions. J Clin Invest 97(4):1102-1110
102. Nechama M, Uchida T, Mor Yosef-Levi I, Silver J, Naveh-Many T (2009) The peptidyl-prolyl isomerase Pin1 determines parathyroid hormone mRNA levels and stability in rat models of secondary hyperparathyroidism. J Clin Invest 119(10):3102-3114
103. Esnault S, Rosenthal LA, Shen ZJ, Sedgwick JB, Szakaly RJ, Sorkness RL, Malter JS (2007) A critical role for Pin1 in allergic pulmonary eosinophilia in rats. J Allergy Clin Immunol 120(5):1082-1088