STAT1 activation causes translocation of Bax to the endoplasmic reticulum during the resolution of airway mucous cell hyperplasia by IFN-γ

Journal of Immunology

Volumn 178, Issue 12, 2007, Pages 8107-8116

  Stout, Barbara A ^a   Melendez, Karla ^a   Seagrave, JeanClare ^a   Holtzman, Michael J ^b   Wilson, Bridget ^c   Xiang, Jialing ^d   Tesfaigzi, Yohannes ^a  

^a LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^d ILLINOIS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; CYTOCHROME C; GAMMA INTERFERON; PROTEIN BAX; STAT1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL HYPERPLASIA; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; INFLAMMATION; MOUSE; MUCOUS CELL; MUCOUS CELL HYPERPLASIA; MUCUS SECRETION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; RESPIRATORY EPITHELIUM;

EID: 34250204442     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.12.8107     Document Type: Article

References (56)

1. Harris, J. F., M. J. Fischer, J. A. Hotchkiss, B. P. Monia, S. H. Randell, J. R. Harkema, and Y. Tesfaigzi. 2005. Bcl-2 sustains increased mucous and epithelial cell numbers in metaplastic airway epithelium. Am. J. Respir. Crit. Care Med. 171: 764-772.
2. Bartner, L. R., N. E. Robinson, M. Kiupel, and Y. Tesfaigzi. 2006. Persistent mucus accumulation: a consequence of delayed bronchial mucous cell apoptosis in RAO-affected horses? Am. J. Physiol. 291: L862-L870.
3. Blyth, D. I., M. S. Pedrick, T. J. Savage, H. Bright, J. E. Beesley, and S. Sanjar. 1998. Induction, duration, and resolution of airway goblet cell hyperplasia in a murine model of atopic asthma: effect of concurrent infection with respiratory syncytial virus and response to dexamethasone. Am. J. Respir. Cell Mol. Biol. 19: 38-54.
4. Shi, Z. Q., M. J. Fischer, G. T. De Sanctis, M. Schuyler, and Y. Tesfaigzi. 2002. IFNγ but not Fas mediates reduction of allergen-induced mucous cell metaplasia by inducing apoptosis. J. Immunol. 168: 4764-4771.
5. Tesfaigzi, J., J. A. Hotchkiss, and J. R. Harkema. 1998. Expression of Bcl-2 during mucous cell metaplasia and remodeling in F344/N rats. Am. J. Resp. Cell Mol. Biol. 18: 704-799.
6. Tesfaigzi, Y., M. I. Fischer, A. J. Martin, and J. Seagrave. 2000. Bcl-2 in LPS-and allergen-induced hyperplastic mucous cells in airway epithelia of Brown Norway rats. Am. J. Physiol. 279: L1210-L1217.
7. Adams, J. M., and S. Cory. 1998. The Bcl-2 protein family: arbiters of cell survival. Science 281: 1322-1326.
8. Thornberry, N. A., and Y. Luzebnik. 1998. Caspases: enemies within. Science 281: 1312-1316.
9. 2+: a control point for apoptosis. Science 300: 135-139.
10. 2+ dynamics by proapoptotic BCL-2 family members. Biochem. Pharmacol. 66: 1335-1340.
11. Tesfaigzi, Y., M. J. Fischer, F. H. Y. Green, G. T. De Sanctis, and J. A. Wilder. 2002. Bax is crucial for IFNγ-induced resolution of allergen-induced mucous cell metaplasia. J. Immunol. 169: 5919-5925.
12. Kumar, A., M. Commane, T. W. Flickinger, C. M. Horvath, and G. R. Stark. 1997. Defective TNF-α-induced apoptosis in STAT1-null cells due to low constitutive levels of caspases. Science 278: 1630-1632.
13. Chin, Y. E., M. Kitagawa, K. Kuida, R. A. Flavell, and X. Y. Fu. 1997. Activation of the STAT signaling pathway can cause expression of caspase 1 and apoptosis. Mol. Cell. Biol. 17: 5328-5337.
14. Lee, C. K., E. Smith, R. Gimeno, R. Gertner, and D. E. Levy. 2000. STAT1 affects lymphocyte survival and proliferation partially independent of its role downstream of IFN-γ. J. Immunol. 164: 1286-1292.
15. Lundberg, A. S., S. H. Randell, S. A. Stewart, B. Elenbaas, K. A. Hartwell, M. W. Brooks, M. D. Fleming, J. C. Olsen, S. W. Miller, R. A. Weinberg, and W. C. Hahn. 2002. Immortalization and transformation of primary human airway epithelial cells by gene transfer. Oncogene 21: 4577-4586.
16. You, Y., E. J. Richer, T. Huang, and S. L. Brody. 2002. Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am. J. Physiol. 283: L1315-L1321.
17. Tesfaigzi, J., M. B. Wood, N. F. Johnson, and K. J. Nikula. 1998. Apoptosis is a major pathway responsible for the resolution of endotoxin-induced type II cell hyperplasia in the rat. Int. J. Exp. Pathol. 79: 303-312.
18. Harkema, J. R., and J. A. Hotchkiss. 1992. In vivo effects of endotoxin on intraepithelial mucosubstances in rat pulmonary airways: quantitative histochemistry. Am. J. Pathol. 141: 307-317.
19. Stout, B. A., M. E. Bates, L. Y. Liu, N. N. Farrington, and P. J. Bertics. 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. Immunol. 173: 6409-6417.
20. Griffiths, G., G. Warren, P. Quinn, O. Mathieu-Costello, and H. Hoppeler. 1984. Density of newly synthesized plasma membrane proteins in intracellular membranes. I. Stereological studies. J. Cell Biol. 98: 2133-2141.
21. Pfeiffer, J. R., J. C. Seagrave, B. H. Davis, G. G. Deanin, and J. M. Oliver. 1985. Membrane and cytoskeletal changes associated with IgE-mediated serotonin release from rat basophilic leukemia cells. J. Cell Biol. 101: 2145-2155.
22. Schroder, K., P. J. Hertzog, T. Ravasi, and D. A. Hume. 2004. Interferon-γ: an overview of signals, mechanisms and functions. J. Leukocyte Biol. 75: 163-189.
23. 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: 1744-1746.
24. Liu, X., C. N. Kim, J. Yang, R. Jemmerson, and X. Wang. 1996. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157.
25. Wolter, K. G., Y. T. Hsu, C. L. Smith, A. Nechushtan, X. G. Xi, and R. J. Youle. 1997. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139: 1281-1292.
26. Green, D. R., and J. C. Reed. 1998. Mitochondria and apoptosis. Science 281: 1309-1312.
27. Breckenridge, D. G., M. Germain, J. P. Mathai, M. Nguyen, and G. C. Shore. 2003. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 22: 8608-8618.
28. Baffy, G., T. Miyashita, J. R. Williamson, and J. C. Reed. 1993. Apoptosis induced by withdrawal of interleukin-3 (IL-3) from an IL-3-dependent hematopoietic cell line is associated with repartitioning of intracellular calcium and is blocked by enforced Bcl-2 oncoprotein production. J. Biol. Chem. 268: 6511-6519.
29. 2+ fluxes. Proc. Natl. Acad. Sci. USA 91: 6569-6573.
30. He, H., M. Lam, T. S. McCormick, and C. W. Distelhorst. 1997. Maintenance of calcium homeostasis in the endoplasmic reticulum by Bcl-2. J. Cell Biol. 138: 1219-1228.
31. Xu, C. B. Bailly-Maitre, and J. C. Reed. 2005. Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 115: 2656-2664.
32. Boyce, M., and J. Yuan. 2006. Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ. 13: 363-373.
33. Kuwano, Y., T. Kawahara, H. Yamamoto, S. Teshima-Kondo, K. Tominaga, K. Masuda, K. Kishi, K. Morita, and K. Rokutan. 2006. Interferon-γ activates transcription of NADPH oxidase 1 gene and up-regulates production of superoxide anion by human large intestinal epithelial cells. Am. J. Physiol. 290: C433-C443.
34. Ito, M., R. Karmali, and M. Krim. 1985. Effect of interferon on chemiluminescence and hydroxyl radical production in murine macrophages stimulated by PMA. Immunology 56: 533-541.
35. Kim, H. S., and M. S. Lee. 2005. Essential role of STAT1 in caspase-independent cell death of activated macrophages through the p38 mitogen-activated protein kinase/STAT1/reaetive oxygen species pathway. Mol. Cell. Biol. 25: 6821-6833.
36. Wong, L. H., I. Hatzinisiriou, R. J. Devenish, and S. J. Ralph. 1998. IFN-γ priming up-regulates IFN-stimulated gene factor 3 (ISGF3) components, augmenting responsiveness of IFN-resistant melanoma cells to type I IFNs. J. Immunol. 160: 5475-5484.
37. Wong, L. H., H. Sim, M. Chatterjee-Kishore, I. Hatzinisiriou, R. J. Devenish, G. Stark, and S. J. Ralph. 2002. Isolation and characterization of a human STAT1 gene regulatory element: inducibility by interferon (IFN) types I and II and role of IFN regulatory factor-1. J. Biol. Chem. 277: 19408-19417.
38. Wen, Z., Z. Zhong, and J. E. Darnell, Jr. 1995. Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82: 241-250.
39. Zhang, X., J. Blenis, H. C. Li, C. Schindler, and S. Chen-Kiang. 1995. Requirement of serine phosphorylation for formation of STAT-promoter complexes. Science 267: 1990-1994.
40. Gross, A., J. Joekel, M. C. Wei, and S. J. Korsmeyer. 1998. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J. 17: 3878-3885.
41. Zou, H., W. J. Henzel, X. Liu, A. Lutschg, and X. Wang. 1997. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspasc-3. Cell 90: 405-413.
42. Li, P., D. Nijhawan, I. Budihardjo, S. M. Srinivasula, M. Ahmad, E. S. Alnemri, and X. Wang. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/ caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489.
43. Antonsson, B., S. Montessuit, S. Lauper, R. Eskes, and J. C. Martinou. 2000. Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem. J. 345(Pt. 2): 271-278.
44. Tjoelker, L. W., C. E. Seyfried, R. L. Eddy, Jr., M. G. Byers, T. B. Shows, J. Calderon, R. B. Schreiber, and P. W. Gray. 1994. Human, mouse, and rat calnexin cDNA cloning: identification of potential calcium binding motifs and gene localization to human chromosome 5. Biochemistry 33: 3229-3236.
45. Hoetelmans, R., H. J. van Slooten, R. Keijzer, S. Erkeland, C. J. van de Velde, and J. H. Dierendonck. 2000. Bcl-2 and Bax proteins are present in interphase nuclei of mammalian cells. Cell Death Differ. 7: 384-392.
46. Gajkowska, B., T. Motyl, H. Olszewska-Badarczuk, and M. M. Godlewski. 2001. Expression of BAX in cell nucleus after experimentally induced apoptosis revealed by immunogold and embedment-free electron microscopy. Cell Biol. Int. 25: 725-733.
47. Hetz, C., P. Bernasconi, J. Fisher, A. H. Lee, M. C. Bassik, B. Antonsson, G. S. Brandt, N. N. Iwakoshi, A. Schinzel, L. H. Glimcher, and S. J. Korsmeyer. 2006. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1α. Science 312: 572-576.
48. Zong, W. X., C. Li, G. Hatzivassiliou, T. Lindsten, Q. C. Yu, J. Yuan, and C. B. Thompson. 2003. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J. Cell Biol. 162: 59-69.
49. Keenan, K. P., J. W. Comhs, and E. M. McDowell. 1982. Regeneration of hamster tracheal epithelium after mechanical injury. I. Focal lesions: quantitative morphologic study of cell proliferation. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 41: 193-214.
50. Keenan, K. P., J. W. Combs, and E. M. McDowell. 1982. Regeneration of hamster tracheal epithelium after mechanical injury. II. Multifocal lesions: stathmokinetic and autoradiographic studies of cell proliferation. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 41: 215-229.
51. Keenan, K. P., J. W. Combs, and E. M. McDowell. 1982. Regeneration of hamster tracheal epithelium after mechanical injury. III. Large and small lesions: comparative stathmokinetic and single pulse and continuous thymidine labeling autoradiographic studies. Virchows Arch. B Cell Pathol Incl. Mol Pathol. 41: 231-252.
52. Jeffery, P. K., and L. Reid. 1975. New observations of rat airway epithelium: a quantitative and electron microscopic study. J. Anat. 120: 295-320.
53. Tesfaigzi, Y., J. F. Harris, J. A. Hotchkiss, and J. R. Harkema. 2004. DNA synthesis and Bcl-2 expression during the development of mucous cell metaplasia in airway epithelium of rats exposed to LPS. Am. J. Physiol. 286: L268-L274.
54. Hockenbery, D. M., Z. N. Oltvai, X. M. Yin, C. L. Milliman, and S. J. Korsmeyer. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75: 241-251.
55. Kaufman, R. J. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13: 1211-1233.
56. Li, J., B. Lee, and A. S. Lee. 2006. Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-reguluted modulator of apoptosis (PUMA) and NOXA by p53. J. Biol. Chem. 281: 7260-7270.