TTF-1 response element is critical for temporal and spatial regulation and necessary for hormonal regulation of human surfactant protein-A2 promoter activity

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 295, Issue 2, 2008, Pages

  Liu, Dongyuan ^a   Yi, Ming ^a   Smith, Margaret ^a   Mendelson, Carole R ^a  

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

Author keywords

Adenosine 3 ,5 cyclic monophosphate; Fetal lung; Glucocorticoid; Tissue specific; Type II cell

Indexed keywords

CYCLIC AMP; DEXAMETHASONE; DNA; ESTROGEN RELATED RECEPTOR ALPHA; HUMAN GROWTH HORMONE; INTERLEUKIN 1; SURFACTANT PROTEIN A; THYROID TRANSCRIPTION FACTOR 1; UPSTREAM STIMULATORY FACTOR 1; UPSTREAM STIMULATORY FACTOR 2; GLUCOCORTICOID; NUCLEAR PROTEIN; SFTPA2 PROTEIN, HUMAN; THYROID NUCLEAR FACTOR 1; TRANSCRIPTION FACTOR;

ANIMAL TISSUE; ARTICLE; CLARA CELL; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; GENE; GENE EXPRESSION; HORMONAL REGULATION; HSP A2 GENE; HUMAN; LUNG ALVEOLUS CELL TYPE 2; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; TISSUE SPECIFICITY; TRANSGENIC MOUSE; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; DRUG EFFECT; FETUS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHYSIOLOGY; RESPIRATORY TRACT MUCOSA; TRANSGENE;

ANIMALS; CELLS, CULTURED; CYCLIC AMP; DEXAMETHASONE; FETUS; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; HUMANS; INTERLEUKIN-1; MICE; MICE, TRANSGENIC; MUTATION; NUCLEAR PROTEINS; PULMONARY SURFACTANT-ASSOCIATED PROTEIN A; RESPIRATORY MUCOSA; RESPONSE ELEMENTS; TRANSCRIPTION FACTORS; TRANSGENES;

EID: 52149118463     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00069.2008     Document Type: Article

References (64)

1. Acarregui MJ, Snyder JM, Mendelson CR. Oxygen modulates the differentiation of human fetal lung in vitro and its responsiveness to cAMP. Am J Physiol Lung Cell Mol Physiol 264: L465-L474, 1993.
2. Acarregui MJ, Snyder JM, Mitchell MD, Mendelson CR. Prostaglandins regulate surfactant protein A (SP-A) gene expression in human fetal lung in vitro. Endocrinology 127: 1105-1113, 1990.
3. Alcorn JL, Gao E, Chen Q, Smith ME, Gerard RD, Mendelson CR. Genomic elements involved in transcriptional regulation of the rabbit surfactant protein-A gene. Mol Endocrinol 7: 1072-1085, 1993.
4. Alcorn JL, Hammer RE, Graves KR, Smith ME, Maika SD, Michael LF, Gao E, Wang Y, Mendelson CR. Analysis of genomic regions involved in regulation of the rabbit surfactant protein A gene in transgenic mice. Am J Physiol Lung Cell Mol Physiol 277: L349-L361, 1999.
5. Alcorn JL, Islam KN, Young PP, Mendelson CR. Glucocorticoid inhibition of SP-A gene expression in lung type II cells is mediated via the TTF-1-binding element. Am J Physiol Lung Cell Mol Physiol 286: L767-L776, 2004.
6. Auten RL, Watkins RH, Shapiro DL, Horowitz S. Surfactant apoprotein A (SP-A) is synthesized in airway cells. Am J Respir Cell Mol Biol 3: 491-496, 1990.
7. Baldwin ASJ. The NF-κB and IκB proteins: new discoveries and insights. Annu Rev Immunol 14: 649-683, 1996.
8. Boggaram V, Mendelson CR. Transcriptional regulation of the gene encoding the major surfactant protein (SP-A) in rabbit fetal lung. J Biol Chem 263: 19060-19065, 1988.
9. Boggaram V, Qing K, Mendelson CR. The major apoprotein of rabbit pulmonary surfactant. Elucidation of primary sequence and cyclic AMP and developmental regulation. J Biol Chem 263: 2939-2947, 1988.
10. Bruno MD, Bohinski RJ, Huelsman KM, Whitsett JA, Korfhagen TR. Lung cell-specific expression of the murine surfactant protein A (SP-A) gene is mediated by interactions between the SP-A promoter and thyroid transcription factor-1. J Biol Chem 270: 6531-6536, 1995.
11. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
12. Condon JC, Hardy DB, Kovaric K, Mendelson CR. Upregulation of the progesterone receptor (PR)-C isoform in laboring myometrium by activation of NF-κB may contribute to the onset of labor through inhibition of PR function. Mol Endocrinol 20: 764-775, 2006.
13. Condon JC, Jeyasuria P, Faust JM, Mendelson CR. Surfactant protein secreted by the maturing mouse fetal lung acts as a hormone that signals the initiation of parturition. Proc Natl Acad Sci USA 101: 4978-4983, 2004.
14. Davé V, Childs T, Whitsett JA. Nuclear factor of activated T cells regulates transcription of the surfactant protein D gene (Sftpd) via direct interaction with thyroid transcription factor-1 in lung epithelial cells. J Biol Chem 279: 34578-34588, 2004.
15. Di Palma T, Nitsch R, Mascia A, Nitsch L, Di Lauro R, Zannini M. The paired domain-containing factor Pax8 and the homeodomain-containing factor TTF-1 directly interact and synergistically activate transcription. J Biol Chem 278: 3395-3402, 2003.
16. Gao E, Alcorn JL, Mendelson CR. Identification of enhancers in the 5′-flanking region of the rabbit surfactant protein A (SP-A) gene and characterization of their binding proteins. J Biol Chem 268: 19697-19709, 1993.
17. Gao E, Wang Y, Alcorn JL, Mendelson CR. The basic helix-loop-helixzipper transcription factor USF1 regulates expression of the surfactant protein-A gene. J Biol Chem 272: 23398-23406, 1997.
18. Gao E, Wang Y, Alcorn JL, Mendelson CR. Transcription factor USF2 is developmentally regulated in fetal lung and acts together with USF1 to induce SP-A gene expression. Am J Physiol Lung Cell Mol Physiol 284: L1027-L1036, 2003.
19. Gao E, Wang Y, McCormick SM, Li J, Seidner SR, Mendelson CR. Characterization of two baboon surfactant protein A genes. Am J Physiol Lung Cell Mol Physiol 271: L617-L630, 1996.
20. Guazzi S, Lonigro R, Pintonello L, Boncinelli E, Di Lauro R, Mavilio F. The thyroid transcription factor-1 gene is a candidate target for regulation by Hox proteins. EMBO J 13: 3339-3347, 1994.
21. Hardy DB, Janowski BA, Corey DR, Mendelson CR. Progesterone receptor (PR) plays a major anti-inflammatory role in human myometrial cells by antagonism of NF-κB activation of cyclooxygenase 2 (COX-2) expression. Mol Endocrinol 20: 2724-2733, 2006.
22. Hardy DB, Mendelson CR. Progesterone receptor (PR) antagonism of the inflammatory signals leading to labor. Fetal Maternal Med Rev 17: 281-289, 2006.
23. Herias MV, Hogenkamp A, van Asten AJ, Tersteeg MH, van Eijk M, Haagsman HP. Expression sites of the collectin SP-D suggest its importance in first line host defence: power of combining in situ hybridisation, RT-PCR and immunohistochemistry. Mol Immunol 44: 3324-3332, 2007.
24. Islam KN, Mendelson CR. Potential role of nuclear factor κB and reactive oxygen species in cAMP and cytokine regulation of surfactant protein-A gene expression in lung type II cells. Mol Endocrinol 16: 1428-1440, 2002.
25. Islam KN, Mendelson CR. Permissive effects of oxygen on cyclic AMP and interleukin-1 stimulation of surfactant protein A gene expression are mediated by epigenetic mechanisms. Mol Cell Biol 26: 2901-2912, 2006.
26. Islam KN, Mendelson CR. Glucocorticoid/glucocorticoid receptor inhibition of surfactant protein-A (SP-A) gene expression in lung type II cells is mediated by repressive changes in histone modification at the SP-A promoter. Mol Endocrinol 22: 585-596, 2008.
27. Jenuwein T, Allis CD. Translating the histone code. Science 293: 1074-1080, 2001.
28. Katyal SL, Singh G, Locker J. Characterization of a second human pulmonary surfactant-associated protein SP-A gene. Am J Respir Cell Mol Biol 6: 446-452, 1992.
29. Kelly SE, Bachurski CJ, Burhans MS, Glasser SW. Transcription of the lung-specific surfactant protein C gene is mediated by thyroid transcription factor 1. J Biol Chem 271: 6881-6888, 1996.
30. Kimura S, Hara Y, Pineau T, Fernandez-Salguero P, Fox CH, Ward JM, Gonzalez FJ. The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev 10: 60-69, 1996.
31. Korfhagen TR, Bruno MD, Glasser SW, Ciraolo PJ, Whitsett JA, Lattier DL, Wikenheiser KA, Clark JC. Murine pulmonary surfactant SP-A gene: cloning, sequence, and transcriptional activity. Am J Physiol Lung Cell Mol Physiol 263: L546-L554, 1992.
32. Kumar AR, Snyder JM. Differential regulation of SP-A1 and SP-A2 genes by cAMP, glucocorticoids, and insulin. Am J Physiol Lung Cell Mol Physiol 274: L177-L185, 1998.
33. Kumar AS, Gonzales LW, Ballard PL. Transforming growth factor-β(1) regulation of surfactant protein B gene expression is mediated by protein kinase dependent intracellular translocation of thyroid transcription factor-1 and hepatocyte nuclear factor 3. Biochim Biophys Acta 1492: 45-55, 2000.
34. Kumar AS, Venkatesh VC, Planer BC, Feinstein SI, Ballard PL. Phorbol ester down-regulation of lung surfactant protein B gene expression by cytoplasmic trapping of thyroid transcription factor-1 and hepatocyte nuclear factor 3. J Biol Chem 272: 20764-20773, 1997.
35. Lazzaro D, Price M, De Felice M, Di Lauro R. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113: 1093-1104, 1991.
36. Li J, Gao E, Mendelson CR. Cyclic AMP-responsive expression of the surfactant protein-A gene is mediated by increased DNA binding and transcriptional activity of thyroid transcription factor-1. J Biol Chem 273: 4592-4600, 1998.
37. Li J, Gao E, Seidner SR, Mendelson CR. Differential regulation of baboon SP-A1 and SP-A2 genes: structural and functional analysis of 5′-flanking DNA. Am J Physiol Lung Cell Mol Physiol 275: L1078-L1088, 1998.
38. Lin S, Perl AK, Shannon JM. Erm/thyroid transcription factor 1 interactions modulate surfactant protein C transcription. J Biol Chem 281: 16716-16726, 2006.
39. Liu D, Hinshelwood MM, Giguere V, Mendelson CR. Estrogen related receptor-α enhances surfactant protein-A gene expression in fetal lung type II cells. Endocrinology 147: 5187-5195, 2006.
40. McCormick SM, Boggaram V, Mendelson CR. Characterization of mRNA transcripts and organization of human SP-A1 and SP-A2 genes. Am J Physiol Lung Cell Mol Physiol 266: L354-L366, 1994.
41. McCormick SM, Mendelson CR. Human SP-A1 and SP-A2 genes are differentially regulated during development and by cAMP and glucocorticoids. Am J Physiol Lung Cell Mol Physiol 266: L367-L374, 1994.
42. Mendelson CR. Role of transcription factors in fetal lung development and surfactant protein gene expression. Annu Rev Physiol 62: 875-915, 2000.
43. Mendelson CR, Chen C, Boggaram V, Zacharias C, Snyder JM. Regulation of the synthesis of the major surfactant apoprotein in fetal rabbit lung tissue. J Biol Chem 261: 9938-9943, 1986.
44. Mendelson CR, Gao E, Li J, Young PP, Michael LF, Alcorn JL. Regulation of expression of surfactant protein-A. Biochim Biophys Acta 1408: 132-149, 1998.
45. Michael LF, Alcorn JL, Gao E, Mendelson CR. Characterization of the cyclic adenosine 3′,5′-monophosphate response element of the rabbit surfactant protein-A gene: evidence for transactivators distinct from CREB/ATF family members. Mol Endocrinol 10: 159-170, 1996.
46. Na SY, Lee SK, Han SJ, Choi HS, Im SY, Lee JW. Steroid receptor coactivator-1 interacts with the p50 subunit and coactivates nuclear factor κB mediated transactivations. J Biol Chem 273: 10831-10834, 1998.
47. Naumann M, Scheidereit C. Activation of NF-κB in vivo is regulated by multiple phosphorylations. EMBO J 13: 4597-4607, 1994.
48. Nichols KV, Floros J, Dynia DW, Veletza SV, Wilson CM, Gross I. Regulation of surfactant protein A mRNA by hormones and butyrate in cultured fetal rat lung. Am J Physiol Lung Cell Mol Physiol 259: L488-L495, 1990.
49. Odom MJ, Snyder JM, Boggaram V, Mendelson CR. Glucocorticoid regulation of the major surfactant associated protein (SP-A) and its messenger ribonucleic acid and of morphological development of human fetal lung in vitro. Endocrinology 123: 1712-1720, 1988.
50. Odom MJ, Snyder JM, Mendelson CR. Adenosine 3′,5′- monophosphate analogs and beta-adrenergic agonists induce the synthesis of the major surfactant apoprotein in human fetal lung in vitro. Endocrinology 121: 1155-1163, 1987.
51. O'Reilly MA, Gazdar AF, Morris RE, Whitsett JA. Differential effects of glucocorticoid on expression of surfactant proteins in a human lung adenocarcinoma cell line. Biochim Biophys Acta 970: 194-204, 1988.
52. Phelps DS, Floros J. Localization of surfactant protein synthesis in human lung by in situ hybridization. Am Rev Respir Dis 137: 939-942, 1988.
53. Ray MK, Chen CY, Schwartz RJ, DeMayo FJ. Transcriptional regulation of a mouse Clara cell-specific protein (mCC10) gene by the NKx transcription factor family members thyroid transciption factor 1 and cardiac muscle-specific homeobox protein (CSX). Mol Cell Biol 16: 2056-2064, 1996.
54. Seidner SR, Smith ME, Mendelson CR. Developmental and hormonal regulation of SP-A gene expression in baboon fetal lung. Am J Physiol Lung Cell Mol Physiol 271: L609-L616, 1996.
55. Selden RF, Howie KB, Rowe ME, Goodman HM, Moore DD. Human growth hormone as a reporter gene in regulation studies employing transient gene expression. Mol Cell Biol 6: 3173-3179, 1986.
56. Snyder JM, Johnston JM, Mendelson CR. Differentiation of type II cells of human fetal lung in vitro. Cell Tissue Res 220: 17-25, 1981.
57. Wohlford-Lenane CL, Snyder JM. Localization of surfactant-associated proteins SP-A and SP-B mRNA in rabbit fetal lung tissue by in situ hybridization. Am J Respir Cell Mol Biol 7: 335-343, 1992.
58. Wong CJ, Akiyama J, Allen L, Hawgood S. Localization and developmental expression of surfactant proteins D and A in the respiratory tract of the mouse. Pediatr Res 39: 930-937, 1996.
59. Wright JR. Immunomodulatory functions of surfactant. Physiol Rev 77: 931-962, 1997.
60. Yi M, Tong GX, Murry B, Mendelson CR. Role of CBP/p300 and SRC-1 in transcriptional regulation of the pulmonary surfactant protein-A (SP-A) gene by thyroid transcription factor-1 (TTF-1). J Biol Chem 277: 2997-3005, 2001.
61. Young PP, Mendelson CR. A CRE-like element plays an essential role in cAMP regulation of human SP-A2 gene in alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 271: L287-L299, 1996.
62. Young PP, Mendelson CR. A GT box element is essential for basal and cyclic adenosine 3′,5′-monophosphate regulation of the human surfactant protein A2 gene in alveolar type II cells: evidence for the binding of lung nuclear factors distinct from Sp1. Mol Endocrinol 11: 1082-1093, 1997.
63. Zhong H, SuYang H, Erdjument-Bromage H, Tempst P, Ghosh S. The transcriptional activity of NF-κB is regulated by the IκB-associated PKAc subunit through a cyclic AMP-independent mechanism. Cell 89: 413-424, 1997.
64. Zhong H, Voll RE, Ghosh S. Phosphorylation of NF-κB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol Cell 1: 661-671, 1998.