IL-4 induces the proteolytic processing of mast cell STAT6

Journal of Immunology

Volumn 169, Issue 7, 2002, Pages 3811-3818

  Sherman, Melanie A ^a   Powell, Doris R ^a   Brown, Melissa A ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS DNA; INTERLEUKIN 4; STAT6 PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ACTIVATION; CELL DEATH; CELL DIFFERENTIATION; CHROMATIN; CONTROLLED STUDY; DNA BINDING; DOWN REGULATION; GENE TARGETING; IMMUNOPRECIPITATION; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 0036785569     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.169.7.3811     Document Type: Article

References (74)

1. Takeda, K., T. Kishimoto, and S. Akira. 1997. STAT6: its role in interleukin 4-mediated biological functions. J. Mol. Med. 75:317.
2. Wurster, A. L., T. Tanaka, and M. J. Grusby. 2000. The biology of Stat4 and Stat6. Oncogene 19:2577.
3. Takeda, K., T. Tanaka, W. Shi, M. Matsumoto, M. Minami, S. Kashiwamura, K. Nakanishi, N. Yoshida, T. Kishimoto, and S. Akira. 1996. Essential role of Stat6 in IL-4 signalling. Nature 380:627.
4. Kaplan, M. H., U. Schindler, S. T. Smiley, and M. J. Grusby. 1996. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4:313.
5. Shimoda, K., J. van Deursen, M. Y. Sangster, S. R. Sarawar, R. T. Carson, R. A. Tripp, C. Chu, F. W. Quelle, T. Nosaka, D. A. Vignali, et al. 1996. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 380:630.
6. Ostrand-Rosenberg, S., M. J. Grusby, and V. K. Clements. 2000. Cutting edge: STAT6-deficient mice have enhanced tumor immunity to primary and metastatic mammary carcinoma. J. Immunol. 165:6015.
7. Kacha, A. K., F. Fallarino, M. A. Markiewicz, and T. F. Gajewski. 2000. Cutting edge: spontaneous rejection of poorly immunogenic P1.HTR tumors by Stat6-deficient mice. J. Immunol. 165:6024.
8. Yokozeki, H., M. Ghoreishi, S. Takagawa, K. Takayama, T. Satoh, I. Katayama, K. Takeda, S. Akira, and K. Nishioka. 2000. Signal transducer and activator of transcription 6 is essential in the induction of contact hypersensitivity. J. Exp. Med. 191:995.
9. Chen, X. P., J. A. Losman, and P. Rothman. 2000. SOCS proteins, regulators of intracellular signaling. Immunity 13:287.
10. Losman, J. A., X. P. Chen, D. Hilton, and P. Rothman. 1999. Cutting edge: SOCS-1 is a potent inhibitor of IL-4 signal transduction. J. Immunol. 162:3770.
11. Caldenhoven, E., T. B. van Dijk, R. Solari, J. Armstrong, J. A. Raaijmakers, J. W. Lammers, L. Koenderman, and R. P. de Groot. 1996. STAT3β, a splice variant of transcription factor STAT3, is a dominant negative regulator of transcription. J. Biol. Chem. 271:13221.
12. Schindler, C., X. Y. Fu, T. Improta, R. Aebersold, and J. E. Darnell, Jr. 1992. Proteins of transcription factor ISGF-3: one gene encodes the 91- and 84-kDa ISGF-3 proteins that are activated by interferon a. Proc. Natl. Acad. Sci. USA 89:7836.
13. Shuai, K., G. R. Stark, I. M. Kerr, and J. E. Darnell, Jr. 1993. A single phosphotyrosine residue of Stat91 required for gene activation by interferon-γ. Science 261:1744.
14. Wang, D., D. Stravopodis, S. Teglund, J. Kitazawa, and J. N. Ihle. 1996. Naturally occurring dominant negative variants of Stat5. Mol. Cell. Biol. 16:6141.
15. Azam, M., C. Lee, I. Strehlow, and C. Schindler. 1997. Functionally distinct isoforms of STAT5 are generated by protein processing. Immunity 6:691.
16. Azam, M., H. Erdjument-Bromage, B. L. Kreider, M. Xia, F. Quelle, R. Basu, C. Saris, P. Tempst, J. N. Ihle, and C. Schindler. 1995. Interleukin-3 signals through multiple isoforms of Stat5. EMBO J. 14:1402.
17. Mui, A. L., H. Wakao, A. M. O'Farrell, N. Harada, and A. Miyajima. 1995. Interleukin-3, granulocyte-macrophage colony stimulating factor and interleukin-5 transduce signals through two STAT5 homologs. EMBO J. 14: 1166.
18. Johnston, J. A., C. M. Bacon, D. S. Finbloom, R. C. Rees, D. Kaplan, K. Shibuya, J. R. Ortaldo, S. Gupta, Y. Q. Chen. J. D. Giri, et al. 1995. Tyrosine phosphorylation and activation of STAT5, STAT3, and Janus kinases by interleukins 2 and 15. Proc. Natl. Acad. Sci. USA 92:8705.
19. Piazza, F., J. Valens, E. Lagasse, and C. Schindler. 2000. Myeloid differentiation of FdCP1 cells is dependent on Stat5 processing. Blood 96:1358.
20. Lee, C., F. Piazza, S. Brutsaert, J. Valens, I. Strehlow, M. Jarosinski, C. Saris, and C. Schindler. 1999. Characterization of the Stat5 protease. J. Biol. Chem. 274: 26767.
21. Sherman, M. A., V. H. Secor, and M. A. Brown. 1999. IL-4 preferentially activates a novel STAT6 isoform in mast cells. J. Immunol. 162:2703.
22. Mirmonsef, P., C. P. Shelburne, C. Fitzhugh Yeatman II, H. J. Chong, and J. J. Ryan. 1999. Inhibition of kit expression by IL-4 and IL-10 in murine mast cells: role of STAT6 and phosphatidylinositol 3′-kinase. J. Immunol. 163:2530.
23. Ryan, J. J., S. DeSimone, G. Klisch, C. Shelburne, L. J. McReynolds, K. Han, R. Kovacs, P. Mirmonsef, and T. F. Huff. 1998. IL-4 inhibits mouse mast cell FcεRI expression through a STAT6-dependent mechanism. J. Immunol. 161: 6915.
24. Nilsson, G., U. Miettinen, T. Ishizaka, L. K. Ashman, A. M. Irani, and L. B. Schwartz. 1994. Interleukin-4 inhibits the expression of kit and tryptase during stem cell factor-dependent development of human mast cells from fetal liver cells. Blood 84:1519.
25. Pierce, J. H., P. P. Di Fiore, S. A. Aaronson, M. Potter, J. Pumphrey, A. Scott, and J. N. Ihle. 1985. Neoplastic transformation of mast cells by Abelson-MuLV: abrogation of IL-3 dependence by a nonautocrine mechanism. Cell 41:685.
26. Yung, Y. P., R. Eger, G. Tertian, and M. A. Moore. 1981. Long-term in vitro culture of murine mast cells. II. Purification of a mast cell growth factor and its dissociation from TCGF. J. Immunol. 127:794.
27. Alt, F. W., N. Rosenberg, R. J. Casanova, E. Thomas, and D. Baltimore. 1982. Immunoglobulin heavy-chain expression and class switching in a murine leukaemia cell line. Nature 296:325.
28. lo thymocytes in vivo. Science 250: 1720.
29. Lu, B., M. Reichel, D. A. Fisher, J. F. Smith, and P. Rothman. 1997. Identification of a STAT6 domain required for IL-4-induced activation of transcription. J. Immunol. 159:1255.
30. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248.
31. Fiering, S., J. P. Northrop, G. P. Nolan, P. S. Mattila, G. R. Crabtree, and L. A. Herzenberg. 1990. Single cell assay of a transcription factor reveals a threshold in transcription activated by signals emanating from the T-cell antigen receptor. Genes Dev. 4:1823.
32. Ndubuisi, M. I., G. G. Guo, V. A. Fried, J. D. Etlinger, and P. B. Sehgal. 1999. Cellular physiology of STAT3: where's the cytoplasmic monomer? J. Biol. Chem. 274:25499.
33. Schindler, C., H. Kashleva, A. Pernis, R. Pine, and P. Rothman. 1994. STF-IL-4: a novel IL-4-induced signal transducing factor. EMBO J. 13:1350.
34. Hou, J., U. Schindler, W. J. Henzel, T. C. Ho, M. Brasseur, and S. L. McKnight. 1994. An interleukin-4-induced transcription factor: IL-4 Stat. Science 265:1701.
35. Kotanides, H., and N. C. Reich. 1993. Requirement of tyrosine phosphorylation for rapid activation of a DNA binding factor by IL-4. Science 262:1265.
36. Meyer, J., M. Jucker, W. Ostertag, and C. Stocking. 1998. Carboxyl-truncated STAT5β is generated by a nucleus-associated serine protease in early hematopoietic progenitors. Blood 91:1901.
37. Sherman, M. A. 2001. The role of STAT6 in mast cell IL-4 production. Immunol. Rev. 179:48.
38. Xia, Z., R. R. Salzler, D. P. Kunz, M. R. Baer, L. Kazim, H. Baumann, and M. Wetzler. 2001. A novel serine-dependent proteolytic activity is responsible for truncated signal transducer and activator of transcription proteins in acute myeloid leukemia blasts. Cancer Res. 61:1747.
39. Sherman, M. A., V. H. Secor, S. K. Lee, R. D. Lopez, and M. A. Brown. 1999. STAT6-independent production of IL-4 by mast cells. Eur. J. Immunol. 29:1235.
40. Tara, D., D. L. Weiss, and M. A. Brown. 1995. Characterization of the constitutive and inducible components of a T cell IL-4 activation responsive element. J. Immunol. 154:4592.
41. Weiss, D. L., J. Hural, D. Tara, L. A. Timmerman, G. Henkel, and M. A. Brown. 1996. Nuclear factor of activated T cells is associated with a mast cell interleukin 4 transcription complex. Mol. Cell. Biol. 16:228.
42. Sherman, M. A., D. R. Powell, D. L. Weiss, and M. A. Brown. 1999. NF-ATc isoforms are differentially expressed and regulated in murine T and mast cells. J. Immunol. 162:2820.
43. Sherman, M. A., T. Y. Nachman, and M. A. Brown. 1999. Cutting edge: IL-4 production by mast cells does not require c-maf. J. Immunol. 163:1733.
44. Hural, J. A., M. Kwan, G. Henkel, M. B. Hock, and M. A. Brown. 2000. An intron transcriptional enhancer element regulates IL-4 gene locus accessibility in mast cells. J. Immunol. 165:3239.
45. Yeatman, C. F., II, S. M. Jacobs-Helber, P, Mirmonsef, S. R. Gillespie, L. A. Bouton, H. A. Collins, S. T. Sawyer, C. P. Shelburne, and J. J. Ryan. 2000. Combined stimulation with the T helper cell type 2 cytokines interleukin (IL)-4 and IL-10 induces mouse mast cell apoptosis. J. Exp. Med. 192:1093.
46. L expression. J. Biol. Chem. 276:26107.
47. Zornig, M., A. Hueber, W. Baum, and G. Evan. 2001. Apoptosis regulators and their role in tumorigenesis. Biochim. Biophys. Acta 1551:F1.
48. Freeman, J. G., J. J. Ryan, C. P. Shelburne, D. P. Bailey, L. A. Bouton, N. Narasimhachari, J. Domen, N. Simeon, F. Couderc, and J. K. Stewart. 2001. Catecholamines in murine bone marrow derived mast cells. J. Neuroimmunol. 119:231.
49. Suzuki, K., H. Nakajima, N. Watanabe, S. Kagami, A. Suto, Y. Saito, T. Saito, and I. Iwamoto. 2000. Role of common cytokine receptor γ chain (γc)- and Jak3-dependent signaling in the proliferation and survival of murine mast cells. Blood 96:2172.
50. Masuda, A., T. Matsuguchi, K. Yamaki, T. Hayakawa, M. Kubo, W. J. LaRochelle, and Y. Yoshikai, 2000. Interleukin-15 induces rapid tyrosine phosphorylation of STAT6 and the expression of interleukin-4 in mouse mast cells. J. Biol. Chem. 275: 29331.
51. Brown, M. A., J. H. Pierce, C. J. Watson, J. Falco, J. N. Ihle, and W. E. Paul. 1987. B cell stimulatory factor-1/interleukin-4 mRNA is expressed by normal and transformed mast cells. Cell 50:809.
52. Garren, H., P. J. Ruiz, T. A. Watkins, P. Fontoura, L. T. Nguyen, E. R. Estline, D. L. Hirschberg, and L. Steinman. 2001. Combination of gene delivery and DNA vaccination to protect from and reverse Th1 autoimmune disease via deviation to the Th2 pathway. Immunity 15:15.
53. Wang, H. W., N. Tedla, A. R. Lloyd, D. Wakefield, and P. H. McNeil. 1998. Mast cell activation and migration to lymph nodes during induction of an immune response in mice. J. Clin. Invest. 102:1617.
54. Mikita, T., D. Campbell, P. Wu, K. Williamson, and U. Schindler. 1996. Requirements for interleukin-4-induced gene expression and functional characterization of Stat6. Mol. Cell. Biol. 15:5811.
55. White, E. D., R. P. Andrews, and G. K. Hershey. 2001. Sulfhydryl-2 domain-containing protein tyrosine phosphatase-1 is not a negative regulator of interleukin-4 signaling in murine mast cells. J. Leukocyte Biol. 69:825.
56. Schleimer, R. P., S. A. Sterbinsky, J. Kaiser, C. A. Bickel, D. A. Klunk, K. Tomioka, W. Newman, F. W. Luscinskas, M. A. Gimbrone Jr., B. W. McIntyre, et al. 1992. IL-4 induces adherence of human eosinophils and basophils but not neutrophils to endothelium: association with expression of VCAM-1. J. Immunol. 148:1086.
57. Nelms, K., A. D. Keegan, J. Zamorano, J. J. Ryan, and W. E. Paul. 1999. The IL-4 receptor: signaling mechanisms and biologic functions. Annu. Rev. Immunol. 17:701.
58. Agarwal, S., and A. Rao. 1998. Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity 9:765.
59. Avni, O., D. Lee, F. Macian, S. Szabo, L. Glimcher, and A. Rao. 2002. Th cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes, Nat. Immunol. 3:643.
60. Morris, S. C., W. C. Gause, and F. D. Finkelman. 2000. IL-4 suppression of in vivo T cell activation and antibody production, J. Immunol. 164:1734.
61. Oskeritzian, C. A., Z. Wang. J. P. Kochan, M. Grimes, Z. Du, H. W. Chang, S. Grant, and L. B. Schwartz. 1999. Recombinant human (rh)IL-4-mediated apoptosis and recombinant human IL-6-mediated protection of recombinant human stem cell factor-dependent human mast cells derived from cord blood mononuclear cell progenitors. J. Immunol. 163:5105.
62. Bischoff, S. C., G. Sellge, A. Lorentz, W. Sebald, R. Raab, and M. P. Manns. 1999. IL-4 enhances proliferation and mediator release in mature human mast cells. Proc. Natl. Acad. Sci. USA 96:8080.
63. Vella, A., T. K. Teague, J. Ihle, J. Kappler, and P. Marrack. 1997. Interleukin 4 (IL-4) or IL-7 prevents the death of resting T cells: Stat6 is probably not required for the effect of IL-4. J. Exp. Med. 186:325.
64. Zamorano, J., A. L. Mora, M. Boothby, and A. D. Keegan. 2001. NF-κB activation plays an important role in the IL-4-induced protection from apoptosis. Int. Immunol. 13:1479.
65. Foote, L. C., R. G. Howard, A. Marshak-Rothstein, and T. L. Rothstein. 1996. IL-4 induces Fas resistance in B cells. J. Immunol. 157:2749.
66. Brunetti, M., N. Martelli, A. Colasante, M. Piantelli, P. Musiani, and F. B. Aiello. 1995. Spontaneous and glucocorticoid-induced apoptosis in human mature T lymphocytes. Blood 86:4199.
67. Illera, V. A., C. E. Perandones, L. L. Stunz, D. A. Mower Jr., and R. F. Ashman. 1993. Apoptosis in splenic B lymphocytes. Regulation by protein kinase C and IL-4. J. Immunol. 151:2965.
68. Parry, S. L., J. Hasbold, M. Holman, and G. G. Klaus. 1994. Hypercross-linking surface IgM or IgD receptors on mature B cells induces apoptosis that is reversed by costimulation with IL-4 and anti-CD40. J. Immunol. 152:2821.
69. Zamorano, J., H. Y. Wang, L. M. Wang, J. H. Pierce, and A. D. Keegan. 1996. IL-4 protects cells from apoptosis via the insulin receptor substrate pathway and a second independent signaling pathway. J. Immunol. 157:4926.
70. Wurster, A. L., D. J. Withers, T. Uchida, M. F. White, and M. J. Grusby. 2002. Stat6 and IRS-2 cooperate in interleukin 4 (IL-4)-induced proliferation and differentiation but are dispensable for IL-4-dependent rescue from apoptosis. Mol. Cell. Biol. 22:117.
71. Bischoff, S. C., G. Sellge, M. P. Manns, and A. Lorentz. 2001. Interleukin-4 induces a switch of human intestinal must cells from proinflammatory cells to Th2-type cells. Int. Arch. Allergy Immunol. 124:151.
72. Bovolenta. C., L. Testolin, L. Benussi, P. M. Lievens, and E. Liboi. 1998. Positive selection of apoptosis-resistant cells correlates with activation of dominant-negative STAT5. J. Biol. Chem. 273:20779.
73. Xia, Z., S. N. Sait, M. R. Baer, M. Barcos, K. A. Donohue, D. Lawrence, L. A. Ford, A. M. Block, H. Baumann, and M. Wetzler. 2001. Truncated STAT proteins are prevalent at relapse of acute myeloid leukemia. Leuk. Res. 25:473.
74. Suzuki, K., H. Nakajima, S. Kagami, A. Suto, K. Ikeda, K. Hirose, T. Hiwasa, K. Takeda, Y. Saito, S. Akira, and I. Iwamoto. 2002. Proteolytic processing of Stat6 signaling in must cells as a negative regulatory mechanism. J. Exp. Med. 196:27.