A genetic variant of p53 restricts the mucous secretory phenotype by regulating SPDEF and Bcl-2 expression

Nature Communications

Volumn 5, Issue , 2014, Pages

  Chand, Hitendra S ^a   Montano, Gilbert ^a   Huang, Xuesong ^a   Randell, Scott H ^b   Mebratu, Yohannes ^a   Petersen, Hans ^a   Tesfaigzi, Yohannes ^a  

^a LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; MESSENGER RNA; PROLINE; PROTEIN BCL 2; PROTEIN P53; PROTEIN SPDEF; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; MUCIN; SPDEF PROTEIN, HUMAN; SPDEF PROTEIN, MOUSE; TRANSCRIPTION FACTOR ETS;

AMINO ACID; CARCINOGEN; GENE EXPRESSION; GENETIC VARIATION; MUCUS; PHENOTYPE; RNA; RODENT; SECRETION;

5' UNTRANSLATED REGION; ADULT; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; GENETIC VARIABILITY; HALF LIFE TIME; HUMAN; HUMAN CELL; MALE; MOUSE; MUCOUS CELL; NONHUMAN; ONCOGENE; PHENOTYPE; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; AGED; ANIMAL; GENETICS; GOBLET CELL; LUNG; METABOLISM; MIDDLE AGED; SECRETION (PROCESS); SMOKING; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE;

MUS;

ADULT; AGED; ANIMALS; CELL LINE, TUMOR; FEMALE; GENES, P53; GOBLET CELLS; HUMANS; LUNG; MALE; MICE; MIDDLE AGED; MUCINS; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-ETS; RNA, MESSENGER; SMOKING;

EID: 84923375508     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6567     Document Type: Article

References (68)

1. McCall, T. D., Pedone, C. A. & Fults, D. W. Apoptosis suppression by somatic cell transfer of Bcl-2 promotes Sonic hedgehog-dependent medulloblastoma formation in mice. Cancer Res. 67, 5179-5185 (2007).
2. Stathopoulos, G. T. et al. Epithelial NF-{kappa}B activation promotes urethane-induced lung carcinogenesis. Proc. Natl Acad. Sci. USA 104, 18514-18519 (2007).
3. Vaux, D. L., Cory, S. & Adams, J. M. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335, 440-442 (1988).
4. Cory, S., Vaux, D. L., Strasser, A., Harris, A. W. & Adams, J. M. Insights from Bcl-2 and Myc: malignancy involves abrogation of apoptosis as well as sustained proliferation. Cancer Res. 59, 1685s-1692s (1999).
5. Cleary, M., Smith, S. & Sklar, J. Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2/immunoglobulin transcript resulting from the t(14;18) translocation. Cell 47, 19-28 (1986).
6. Pezzella, F. et al. bcl-2 protein in non-small-cell lung carcinoma. New Engl. J. Med. 329, 690-694 (1993).
7. Bredow, S., Juri, D. E., Cardon, K. & Tesfaigzi, Y. Identification of a novel Bcl-2 promoter region that counteracts in a p53-dependent manner the inhibitory P2 region. Gene 404, 110-116 (2007).
8. Wu, Y., Mehew, J. W., Heckman, C. A., Arcinas, M. & Boxer, L. M. Negative regulation of bcl-2 expression by p53 in hematopoietic cells. Oncogene 20, 240-251 (2001).
9. Miyashita, T., Harigai, M., Hanada, M. & Reed, J. C. Identification of a p53-dependent negative response element in the bcl-2 gene. Cancer Res. 54, 3131-3135 (1994).
10. Vousden, K. H. & Lane, D. P. p53 in health and disease. Nat. Rev. Mol. Cell Biol. 8, 275-283 (2007).
11. Young, R. L. & Korsmeyer, S. J. A negative regulatory element in the bcl-2 50-untranslated region inhibits expression from an upstream promoter. Mol. Cell Biol. 13, 3686-3697 (1993).
12. Tsujimoto, Y. & Croce, C. M. Analysis of the structure, transcripts, and protein products of bcl-2, the gene involved in human follicular lymphoma. Proc. Natl Acad. Sci. USA 83, 5214-5218 (1986).
13. Tesfaigzi, Y., Fischer, M. J., Martin, A. J. & Seagrave, J. Bcl-2 in LPS- and allergen-induced hyperplastic mucous cells in airway epithelia of Brown Norway rats. Am. J. Physiol. Lung. Cell Mol. Physiol. 279, L1210-L1217 (2000).
14. Tesfaigzi, Y., Harris, J. F., Hotchkiss, J. A. & Harkema, J. R. DNA synthesis and Bcl-2 expression during the development of mucous cell metaplasia in airway epithelium of rats exposed to LPS. Am. J. Physiol. Lung. Cell Mol. Physiol. 286, L268-L274 (2004).
15. Harris, J. F. et al. Bcl-2 sustains increased mucous and epithelial cell numbers in metaplastic airway epithelium. Am. J. Respir. Crit. Care Med. 171, 764-772 (2005).
16. Chand, H. S., Woldegiorgis, Z., Schwalm, K., McDonald, J. & Tesfaigzi, Y. Acute inflammation induces insulin-like growth factor-1 to mediate Bcl-2 and Muc5ac expression in airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 47, 784-791 (2012).
17. Vignola, A. M. et al. Proliferation and activation of bronchial epithelial cells in corticosteroid-dependent asthma. J. Allergy. Clin. Immunol. 108, 738-746 (2001).
18. National Heart Lung and Blood Institute & Health, N.I.o. Global Initiative for Chronic Obstructive Lung Disease (GOLD) guidelines, global strategy for the diagnosis, management and prevention of chronic obstructive lung disease. NHLBI/WHO Workshop Report (NIH 2701, 2001).
19. Kim, V. & Criner, G. J. Chronic Bronchitis and COPD. Am. J. Respir. Crit. Care Med. (2012).
20. Spira, A. et al. Effects of cigarette smoke on the human airway epithelial cell transcriptome. Proc. Natl Acad. Sci. USA 101, 10143-10148 (2004).
21. Seemungal, T. A., Donaldson, G. C., Bhowmik, A., Jeffries, D. J. & Wedzicha, J. A. Time course and recovery of exacerbations in patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 161, 1608-1613 (2000).
22. Prescott, E., Lange, P. & Vestbo, J. Chronic mucus hypersecretion in COPD and death from pulmonary infection. Eur. Respir. J. 8, 1333-1338 (1995).
23. Spencer, S. & Jones, P. W. Time course of recovery of health status following an infective exacerbation of chronic bronchitis. Thorax 58, 589-593 (2003).
24. Montes de Oca, M. et al. Chronic bronchitis phenotype in subjects with and without COPD: the PLATINO study. Eur. Respir. J. 40, 28-36 (2012).
25. Hancox, R. J. et al. Accelerated decline in lung function in cigarette smokers is associated with TP53/MDM2 polymorphisms. Hum. Genet. 126, 559-565 (2009).
26. Lange, P., Nyboe, J., Appleyard, M., Jensen, G. & Schnohr, P. Ventilatory function and chronic mucus hypersecretion as predictors of death from lung cancer. Am. Rev. Respir. Dis. 141, 613-617 (1990).
27. Brenner, D. R. et al. Previous lung diseases and lung cancer risk: a pooled analysis from the International Lung Cancer Consortium. Am. J. Epidemiol. 176, 573-585 (2012).
28. Hogg, J. C. et al. Survival after lung volume reduction in chronic obstructive pulmonary disease: insights from small airway pathology. Am. J. Respir. Crit. Care Med. 176, 454-459 (2007).
29. Chand, H. S. et al. Intracellular insulin-like growth factor-1 induces Bcl-2 expression in airway epithelial cells. J. Immunol. 188, 4581-4589 (2012).
30. Boers, J. E., ten Velde, G. P. & Thunnissen, F. B. P53 in squamous metaplasia: a marker for risk of respiratory tract carcinoma. Am. J. Respir. Crit. Care Med. 153, 411-416 (1996).
31. Smith, M. D., Ensor, E. A., Coffin, R. S., Boxer, L. M. & Latchman, D. S. Bcl-2 transcription from the proximal P2 promoter is activated in neuronal cells by the Brn-3a POU family transcription factor. J. Biol. Chem. 273, 16715-16722 (1998).
32. Venot, C. et al. The requirement for the p53 proline-rich functional domain for mediation of apoptosis is correlated with specific PIG3 gene transactivation and with transcriptional repression. EMBO J. 17, 4668-4679 (1998).
33. Thomas, M. et al. Two polymorphic variants of wild-type p53 differ biochemically and biologically. Mol. Cell Biol. 19, 1092-1100 (1999).
34. Imboden, M. et al. Decreased PM10 exposure attenuates age-related lung function decline: genetic variants in p53, p21, and CCND1 modify this effect. Environ. Health. Perspect. 117, 1420-1427 (2009).
35. Committee. A statement by the Committee on Diagnostic Standards for Nontuberculous Respiratory Diseases. Am. Rev. Respir. Dis. 85, 762 (1962).
36. Park, K. S. et al. SPDEF regulates goblet cell hyperplasia in the airway epithelium. J. Clin. Invest. 117, 978-988 (2007).
37. Chen, G. et al. SPDEF is required for mouse pulmonary goblet cell differentiation and regulates a network of genes associated with mucus production. J. Clin. Invest. 119, 2914-2924 (2009).
38. Wang, B., Xiao, Z. & Ren, E. C. Redefining the p53 response element. Proc. Natl Acad. Sci. USA 106, 14373-14378 (2009).
39. Youle, R. J. & Strasser, A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9, 47-59 (2008).
40. Toledo, F. et al. A mouse p53 mutant lacking the proline-rich domain rescues Mdm4 deficiency and provides insight into the Mdm2-Mdm4-p53 regulatory network. Cancer Cell 9, 273-285 (2006).
41. Toledo, F. et al. Mouse mutants reveal that putative protein interaction sites in the p53 proline-rich domain are dispensable for tumor suppression. Mol. Cell Biol. 27, 1425-1432 (2007).
42. Contreras, A. U. et al. Deacetylation of p53 induces autophagy by suppressing Bmf expression. J. Cell Biol. 201, 427-437 (2013).
43. Wei, C. L. et al. A global map of p53 transcription-factor binding sites in the human genome. Cell 124, 207-219 (2006).
44. Michalak, E., Villunger, A., Erlacher, M. & Strasser, A. Death squads enlisted by the tumour suppressor p53. Biochem. Biophys. Res. Commun. 331, 786-798 (2005).
45. Seto, M. et al. Alternative promoters and exons, somatic mutation and deregulation of the Bcl-2-Ig fusion gene in lymphoma. EMBO J. 7, 123-131 (1988).
46. Schiavone, N. et al. A conserved AU-rich element in the 30 untranslated region of bcl-2 mRNA is endowed with a destabilizing function that is involved in bcl-2 down-regulation during apoptosis. FASEB J. 14, 174-184 (2000).
47. Donnini, M. et al. Identification of TINO: a new evolutionarily conserved BCL-2 AU-rich element RNA-binding protein. J. Biol. Chem. 279, 20154-20166 (2004).
48. Sengupta, T. K., Bandyopadhyay, S., Fernandes, D. J. & Spicer, E. K. Identification of nucleolin as an AU-rich element binding protein involved in bcl-2 mRNA stabilization. J. Biol. Chem. 279, 10855-10863 (2004).
49. Miller, S. J., Suthiphongchai, T., Zambetti, G. P. & Ewen, M. E. p53 binds selectively to the 50 untranslated region of cdk4, an RNA element necessary and sufficient for transforming growth factor beta- and p53-mediated translational inhibition of cdk4. Mol. Cell Biol. 20, 8420-8431 (2000).
50. Olsson, A., Manzl, C., Strasser, A. & Villunger, A. How important are posttranslational modifications in p53 for selectivity in target-gene transcription and tumour suppression? Cell Death. Differ. 14, 1561-1575 (2007).
51. Frank, A. K. et al. The codon 72 polymorphism of p53 regulates interaction with NF-{kappa}B and transactivation of genes involved in immunity and inflammation. Mol. Cell Biol. 31, 1201-1213 (2011).
52. Walker, K. K. & Levine, A. J. Identification of a novel p53 functional domain that is necessary for efficient growth suppression. Proc. Natl Acad. Sci. USA 93, 15335-15340 (1996).
53. Schneider-Stock, R. et al. Retention of the arginine allele in codon 72 of the p53 gene correlates with poor apoptosis in head and neck cancer. Am. J. Pathol. 164, 1233-1241 (2004).
54. Gray, T. et al. Regulation of MUC5AC mucin secretion and airway surface liquid metabolism by IL-1beta in human bronchial epithelia. Am. J. Physiol. Lung. Cell Mol. Physiol. 286, L320-L330 (2004).
55. Fischer, B. M. & Voynow, J. A. Neutrophil elastase induces MUC5AC gene expression in airway epithelium via a pathway involving reactive oxygen species. Am. J. Respir. Cell Mol. Biol. 26, 447-452 (2002).
56. Dumont, P., Leu, J. I., Della Pietra, 3rd A. C., George, D. L. & Murphy, M. The codon 72 polymorphic variants of p53 have markedly different apoptotic potential. Nat. Genet. 33, 357-365 (2003).
57. Pietsch, E. C., Humbey, O. & Murphy, M. E. Polymorphisms in the p53 pathway. Oncogene 25, 1602-1611 (2006).
58. Tuveson, D. & Hanahan, D. Translational medicine: Cancer lessons from mice to humans. Nature 471, 316-317 (2011).
59. Chen, Z. et al. A murine lung cancer co-clinical trial identifies genetic modifiers of therapeutic response. Nature 483, 613-617 (2012).
60. Hunninghake, G. M. et al. MMP12, lung function, and COPD in high-risk populations. New Engl. J. Med. 361, 2599-2608 (2009).
61. Sood, A. et al. Wood Smoke-Associated Chronic Obstructive Pulmonary Disease (COPD)-Underappreciated in the United States? Am. J. Respir. Crit. Care Med. 179, A4742 (2009).
62. Akinbami, L. J. & Liu, X. Chronic obstructive pulmonary disease among adults aged 18 and over in the United States, 1998-2009. NCHS Data Brief 63, 1-8 (2011).
63. Silverman, E. K. et al. Gender-related differences in severe, early-onset chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 162, 2152-2158 (2000).
64. You, Y., Richer, E. J., Huang, T. & Brody, S. L. Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am. J. Physiol. Lung. Cell Mol. Physiol. 283, L1315-L1321 (2002).
65. Lundberg, A. S. et al. Immortalization and transformation of primary human airway epithelial cells by gene transfer. Oncogene 21, 4577-4586 (2002).
66. Stout, B. et al. STAT1 activation causes translocation of Bax to the endoplasmic reticulum during the resolution of airway mucous cell hyperplasia by IFNg. J. Immunol. 178, 8107-8116 (2007).
67. Tesfaigzi, J., Smith-Harrison, W. & Carlson, D. M. A simple method for reusing western blots on PVDF membranes. BioTechniques 17, 268-269 (1994).
68. Niranjanakumari, S., Lasda, E., Brazas, R. & Garcia-Blanco, M. A. Reversible cross-linking combined with immunoprecipitation to study RNA-protein interactions in vivo. Methods 26, 182-190 (2002).