Regulation of eotaxin gene expression by TNF-α and IL-4 through mRNA stabilization: Involvement of the RNA-binding protein HuR

Journal of Immunology

Volumn 171, Issue 8, 2003, Pages 4369-4378

  Atasoy, Ulus ^b   Curry, Stephanie L ^a   López De Silanes, Isabel ^c   Shyu, Ann Bin ^d   Casolaro, Vincenzo ^f   Gorospe, Myriam ^c   Stellato, Cristiana ^a,e  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c NATIONAL INSTITUTE ON AGING   (United States)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^e JOHNS HOPKINS ASTHMA AND ALLERGY CENTER   (United States)

^f NONE

Author keywords

[No Author keywords available]

Indexed keywords

DACTINOMYCIN; EOTAXIN; HUR PROTEIN; INTERLEUKIN 4; MESSENGER RNA; RNA BINDING PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; BRONCHUS MUCOSA; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPITHELIUM CELL; GENE EXPRESSION REGULATION; HALF LIFE TIME; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOPATHOLOGY; IMMUNOPRECIPITATION; INFLAMMATORY DISEASE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA BINDING; RNA STABILITY; TRANSCRIPTION REGULATION;

EID: 0141889091     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.8.4369     Document Type: Article

References (74)

1. Baggiolini, M. 2001. Chemokines in pathology and medicine. J. Intern. Med. 250:91.
2. Mackay, C. R. 2001. Chemokines: immunology's high impact factors. Nat. Immunol. 2:95.
3. Proudfoot, A. E. 2002. Chemokine receptors: multifaceted therapeutic targets. Nat. Rev. Immunol. 2:106.
4. Foster, P. S., A. W. Mould. M. Yang, J. Mackenzie, J. Mattes, S. P. Hogan, S. Mahalingam, A. N. McKenzie, M. E. Rothenberg, I. G. Young, et al. 2001. Elemental signals regulating eosinophil accumulation in the lung. Immunol. Rev. 179:173.
5. Lamkhioued, B., P. M. Renzi, S. Abi-Younes, E. A. Garcia-Zepada, Z. Allakhverdi, O. Ghaffar, M. D. Rothenberg, A. D. Luster, and Q. Hamid. 1997. Increased expression of eotaxin in bronchoalveolar lavage and airways of asthmatics contributes to the chemotaxis of eosinophils to the site of inflammation. J. Immunol. 159:4593.
6. Ying, S., Q. Meng, K. Zeibecoglou, D. S. Robinson, A. Macfarlane, M. Humbert. and A. B. Kay. 1999. Eosinophil chemotactic chemokines (eotaxin, eotaxin-2, RANTES, monocyte chemoattractant protein-3 (MCP-3), and MCP-4), and C-C chemokine receptor 3 expression in bronchial biopsies from atopic and nonatopic (intrinsic) asthmatics. J. Immunol. 163:6321.
7. Lilly, C. M., H. Nakamura, O. I. Belostotsky, K. J. Haley, E. A. Garcia-Zepeda, A. D. Luster, and E. Israel. 2001. Eotaxin expression after segmental allergen challenge in subjects with atopic asthma. Am. J. Respir. Crit. Care Med. 163:1669.
8. Greiff, L., M. Andersson, E. Andersson, M. Linden, S. Myint, C. Svensson, and C. G. Persson. 1999. Experimental common cold increases mucosal output of eotaxin in atopic individuals. Allergy 54:1204.
9. Jafri, H. S. 2002. Role of chemokines in respiratory syncytial virus disease. Pediatr. Infect. Dis J. 21:454.
10. Gonzalo, J. A., C. M. Lloyd, D. Wen, J. P. Albar, T. N. Wells, A. Proudfoot, A. C. Martinez, M. Dorf, T. Bjerke, A. J. Coyle, and J. C. Gutierrez-Ramos. 1998. The coordinated action of CC chemokines in the lung orchestrates allergic inflammation and airway hyperresponsiveness. J. Exp. Med. 188:157.
11. Nakamura, H., S. T. Weiss, E. Israel, A. D. Luster, J. M. Drazen, and C. M. Lilly. 1999. Eotaxin and impaired lung function in asthma. Am. J. Respir. Crit. Care Med. 160:1952.
12. Mould, A. W., A. J. Ramsay, K. I. Matthaei, I. G. Young, M. E. Rothenberg, and P. S. Foster. 2000. The effect of IL-5 and eotaxin expression in the lung on eosinophil trafficking and degranulation and the induction of bronchial hyperreactivity. J. Immunol. 164:2142.
13. Mishra, A., S. P. Hogan, E. B. Brandt, N. Wagner, M. W. Crossman, P. S. Foster, and M. E. Rothenberg. 2002. Enterocyte expression of the eotaxin and interleukin-5 transgenes induces compartmentalized dysregulation of eosinophil trafficking. J. Biol. Chem. 277:4406.
14. Yawalkar, N., M. Uguccioni, J. Scharer, J. Braunwalder, S. Karlen, B. Dewald, L. R. Braathen, and M. Baggiolini. 1999. Enhanced expression of eotaxin and CCR3 in atopic dermatitis. J. Invest. Dermatol. 113:43.
15. Minshall, E. M., L. Cameron, F. Lavigne, D. Y. Leung, D. Hamilos, E. A. Garcia-Zepada, M. Rothenberg, A. D. Luster, and Q. Hamid. 1997. Eotaxin mRNA and protein expression in chronic sinusitis and allergen-induced nasal responses in seasonal allergic rhinitis. Am. J. Respir. Cell Mol. Biol. 17:683.
16. Hogan, S. P., A. Mishra, E. B. Brandt, M. P. Royalty, S. M. Pope, N. Zimmermann, P. S. Foster, and M. E. Rothenberg. 2001. A pathological function for eotaxin and eosinophils in eosinophilic gastrointestinal inflammation. Nat. Immunol. 2:353.
17. + endothelial cells. J. Immunol. 166:7571.
18. Stellato, C., B. Tancowny, M. E. Brummet, S. L. Curry, C. E. Austin, and L. A. Beck. 2003. Functional analysis of the chemokine receptor CCR3 on airway epithelial cells. J. Allergy Clin. Immunol. 111:S148 (Abstr.).
19. Haley, K. J., C. M. Lilly, J. H. Yang, Y. Feng, S. P. Kennedy, T. G. Turi, J. F. Thompson, G. H. Sukhova, P. Libby, and R. T. Lee. 2000. Overexpression of eotaxin and the CCR3 receptor in human atherosclerosis: using genomic technology to identify a potential novel pathway of vascular inflammation. Circulation 102:2185.
20. Teruya-Feldstein, J., E. S. Jaffe, P. R. Burd, D. W. Kingma, J. E. Setsuda, and G. Tosato. 1999. Differenfial chemokine expression in tissues involved by Hodgkin's disease: direct correlation of eotaxin expression and tissue eosinophilia. Blood 93:2463.
21. Nickel, R., L. A. Beck, C. Stellato, and R. P. Schleimer. 1999. Chemokines and allergic disease. J. Allergy Clin. Immunol. 104:723.
22. Rosenwasser, L. J., N. Zimmermann, G. K. Hershey, P. S. Foster, and M. E. Rothenberg. 2003. Chemokines in asthma: cooperative interaction between chemokines and IL-13. J. Allergy Clin. Immunol. 111:227.
23. Stellato, C., S. Matsukura, A. Fal, J. White, L. A. Beck, D. Proud, and R. P. Schleimer. 1999. Differential regulation of epithelial-derived C-C chemokine expression by IL-4 and the glucocorticoid budesonide. J. Immunol. 163:5624.
24. Matsukura, S., C. Stellato, J. R. Plitt, C. Bickel, K. Miura, S. N. Georas, V. Casolaro, and R. P. Schleimer. 1999. Activation of eotaxin gene transcription by NF-κB and STAT6 in human airway epithelial cells. J. Immunol. 163:6876.
25. Banwell, M. E., N. S. Tolley, T. J. Williams, and T. J. Mitchell. 2002. Regulation of human eotaxin-3/CCL26 expression: modulation by cytokines and glucocorticoids. Cytokine 17:317.
26. Hoeck, J., and M. Woisetschlager. 2001. Activation of eotaxin-3/CCL126 gene expression in human dermal fibroblasts is mediated by STAT6. J. Immunol. 167:3216.
27. Shinkai, A., H. Yoshisue, M. Koike, E. Shoji, S. Nakagawa, A. Saito, T. Takeda, S. Imabeppu, Y. Kato, N. Hanai, et al. 1999. A novel human CC chemokine, eotaxin-3, which is expressed in IL-4-stimulated vascular endothelial cells, exhibits potent activity toward eosinophils. J. Immunol. 163:1602.
28. Terada, N., T. Nomura, W. J. Kim, Y. Otsuka, R. Takahashi, H. Kishi, T. Yamashita, N. Sugawara, S. Fukuda, T. Ikeda-Ito, and A. Konno. 2001. Expression of C-C chemokine TARC in human nasal mucosa and its regulation by cytokines. Clin. Exp. Allergy 31:1923.
29. Bonecchi, R., S. Sozzani, J. T. Stine, W. Luini, G. D'Amico, P. Allavena, D. Chantry, and A. Mantovani. 1998. Divergent effects of interleukin-4 and interferon-γ on macrophage-derived chemokine production: an amplification circuit of polarized T helper 2 responses. Blood 92:2668.
30. Fujisawa, T., Y. Kato, J. Atsuta, A. Terada, K. Iguchi, H. Kamiya, H. Yamada, T. Nakajima, M. Miyamasu, and K. Hirai. 2000. Chemokine production by the BEAS-2B human bronchial epithelial cells: differential regulation of eotaxin, IL-8, and RANTES by TH2- and TH1-derived cytokines. J. Allergy Clin. Immunol. 105:126.
31. Thomas, P. S. 2001. Tumour necrosis factor-α the role of this multifunctional cytokine in asthma. Immunol. Cell Biol. 79:132.
32. Luster, A. D. 2002. The role of chemokines in linking innate and adaptive immunity. Curr. Opin. Immunol. 14:129.
33. Heller, N. M., S. Curry, R. Nickel, B. Plunkett, S. Huang, A.-B. Shyu, R. P. Schleimer, and C. Stellato. 2002. Post-transcriptional regulation of eotaxin by glucocorticoids (GC) and by interleukin (IL)-4. J. Allergy Clin. Immunol. 109:S159.
34. Croft, D., P. McIntyre, A. Wibulswas, and I. Kramer. 1999. Sustained elevated levels of VCAM-1 in cultured fibroblast-like synoviocytes can be achieved by TNF-α in combination with either IL-4 or IL-13 through increased mRNA stability. Am. J. Pathol. 154:1149.
35. Kracht, M., and J. Saklatvala. 2002. Transcriptional and post-transcriptional control of gene expression in inflammation. Cytokine 20:91.
36. Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465.
37. Ross. J. 1995. mRNA stability in mammalian cells. Microbiol. Rev. 59:423.
38. Wilusz, C. J., M. Wormington, and S. W. Peltz. 2001. The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell Biol. 2:237.
39. Guhaniyogi, J., and G. Brewer. 2001. Regulation of mRNA stability in mammalian cells. Gene 265:11.
40. Shaw, G., and R. Kamen. 1986. A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46:659.
41. Caput, D., B. Beutler, K. Hartog, R. Thayer, S. Brown-Shimer, and A. Cerami. 1986. Identification of a common nucleotide sequence in the 3′-untranslated region of mRNA molecules specifying inflammatory mediators. Proc. Natl. Acad. Sci. USA 83:1670.
42. Chen, C. Y., N. Xu, and A. B. Shyu. 1995. mRNA decay mediated by two distinct AU-rich elements from c-fos and granulocyte-macrophage colony-stimulating factor transcripts: different deadenylation kinetics and uncoupling from translation. Mol. Cell. Biol. 15:5777.
43. Fan, X. C., and J. A. Steitz. 1998. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17:3448.
44. Wang, W., H. Furneaux, H. Cheng, M. C. Caldwell, D. Hutter, Y. Liu, N. Holbrook, and M. Gorospe. 2000. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20:760.
45. Hollams, E. M., K. M. Giles. A. M. Thomson, and P. J. Leedman. 2002. mRNA stability and the control of gene expression: implications for human disease. Neurochem. Res. 27:957.
46. Atasoy, U., J. Watson. D. Patel, and J. D. Keene. 1998. ELAV protein HuA (HuR) can redistribute between nucleus and cytoplasm and is upregulated during serum stimulation and T cell activation. J. Cell Sci. 111(Pt. 21):3145.
47. Kontoyiannis, D., M. Pasparakis, T. T. Pizarro, F. Cominelli, and G. Kollias. 1999. Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity 10:387.
48. Esnault, S., and J. S. Malter. 2001. Granulocyte macrophage-colony-stimulating factor mRNA is stabilized in airway eosinophils and peripheral blood eosinophils activated by TNF-α plus fibronectin. J. Immunol. 166:4658.
49. Butler, N. S., M. M. Monick, T. O. Yarovinsky, L. S. Powers, and G. W. Hunninghake. 2002. Altered IL-4 mRNA stability correlates with Th1 and Th2 bias and susceptibility to hypersensitivity pneumonitis in two inbred strains of mice. J. Immunol. 169:3700.
50. Brennan, C. M., I. E. Gallouzi, and J. A. Steitz. 2000. Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J. Cell Biol. 151:1.
51. Peng, S. S., C. Y. Chen, N. Xu, and A. B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17:3461.
52. Jain, R. G., L. G. Andrews, K. M. McGowan, P. H. Pekala, and J. D. Keene. 1997. Ectopic expression of He1-N1, an RNA-binding protein, increases glucose transporter (GLUT1) expression in 3T3-L1 adipocytes. Mol. Cell. Biol. 17:954.
53. Antic, D., and J. D. Keene. 1998. Messenger ribonucleoprotein complexes containing human ELAV proteins: interactions with cytoskeleton and translational apparatus. J. Cell Sci. 111(Pt 2):183.
54. Taha, R. A., E. M. Minshall, D. Miotto, A. Shimbara, A. Luster, J. C. Hogg, and Q. A. Hamid. 1999. Eotaxin and monocyte chemotactic protein-4 mRNA expression in small airways of asthmatic and nonasthmatic individuals. J. Allergy Clin. Immunol. 103:476.
55. Ying, S., D. S. Robinson, Q. Meng, J. Rottman, R. Kennedy, D. J. Ringler, C. R. Mackay, B. L. Daugherty, M. S. Springer, S. R. Durham, et al. 1997. Enhanced expression of eotaxin and CCR3 mRNA and protein in atopic asthma: association with airway hyperresponsiveness and predominant co-localization of eotaxin mRNA to bronchial epithelial and endothelial cells. Eur. J. Immunol. 27:3507.
56. Churchill, L., B. Friedman, R. P. Schleimer, and D. Proud. 1992. Production of granulocyte-macrophage colony-stimulating factor by cultured human tracheal epithelial cells. Immunology 75:189.
57. Reddel, R. R., S. E. Salghetti, J. C. Willey, Y. Ohnuki, Y. Ke, B. I. Gerwin, J. F. Lechner, and C. C. Harris. 1993. Development of tumorigenicity in simian virus 40-immortalized human bronchial epithelial cell lines. Cancer Res. 53:985.
58. Shyu, A. B., J. G. Belasco, and M. E. Greenberg. 1991. Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Dev. 5:221.
59. Tenenbaum, S. A., C. C. Carson, P. J. Lager, and J. D. Keene. 2000. Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc. Natl. Acad. Sci. USA 97:14085.
60. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156.
61. Ponath, P. D., S. Qin, D. J. Ringler, I. Clark-Lewis, J. Wang, N. Kassam. H. Smith, X. Shi, J. A. Gonzalo, W. Newman, et al. 1996. Cloning of the human eosinophil chemoattractant, eotaxin: expression, receptor binding, and functional properties suggest a mechanism for the selective recruitment of eosinophils. J. Clin. Invest. 97:604.
62. Tenenbaum, S. A., P. J. Lager, C. C. Carson, and J. D. Keene. 2002. Ribonomics: identifying mRNA subsets in mRNP complexes using antibodies to RNA-binding proteins and genomic arrays. Methods 26:191.
63. Gallouzi, I. E., C. M. Brennan, M. G. Stenberg, M. S. Swanson, A. Eversole, N. Maizels, and J. A. Steitz. 2000. HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc. Natl. Acad. Sci. USA 97:3073.
64. Nakamura, H., A. D. Luster, H. Tateno, S. Jedrzkiewicz, G. Tamura, K. J. Haley, E. A. Garcia-Zepeda, K. Yamaguchi, and C. M. Lilly. 2001. IL-4 differentially regulates eotaxin and MCP-4 in lung epithelium and circulating mononuclear cells. Am. J. Physiol. 281:L1288.
65. Loflin, P. T., C. Y. Chen, N. Xu, and A. B. Shyu. 1999. Transcriptional pulsing approaches for analysis of mRNA turnover in mammalian cells. Methods 17:11.
66. Wang, W., J. Fan, X. Yang, S. Furer-Galban, I. Lopez de Silanes, C. von Kobbe, J. Guo, S. N. Georas, F. Foufelle, D. G. Hardie, et al. 2002. AMP-activated kinase regulates cytoplasmic HuR. Mol. Cell. Biol. 22:3425.
67. Wang, W., X. Yang, V. J. Cristofalo, N. J. Holbrook, and M. Gorospe. 2001. Loss of HuR is linked to reduced expression of proliferative genes during replicative senescence. Mol. Cell. Biol. 21:5889.
68. Stellato, C., and L. A. Beck. 2000. Expression of eosinophil-specific chemokines by human epithelial cells. Chem. Immunol. 76:156.
69. Brown, C. Y., C. A. Lagnado, and G. J. Goodall. 1996. A cytokine mRNA-destabilizing element that is structurally and functionally distinct from A + U-rich elements. Proc. Natl. Acad. Sci. USA 93:13721.
70. Chen, C. Y., R. Gherzi, J. S. Andersen, G. Gaietta, K. Jurchott, H. D. Royer, M. Mann, and M. Karin. 2000. Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Genes Dev. 14:1236.
71. Linder, P., and M. F. Tuite. 1999. The versatility of RNA structure and function. Jacques Monod Conference: new insights into the mechanism of mRNA translation: the significance of RNA structure, Aussois, France, 22-26 March 1999. Trends Genet. 15:302.
72. Levy, N. S., S. Chung, H. Furneaux, and A. P. Levy. 1998. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 273:6417.
73. Millard, S. S., A. Vidal, M. Markus, and A. Koff. 2000. A U-rich element in the 5′ untranslated region is necessary for the translation of p27 mRNA. Mol. Cell. Biol. 20:5947.
74. Keene, J. D. 2003. Organizing mRNA export. Nat. Genet. 33:111.