Glucocorticoid genes and the developmental origins of asthma susceptibility and treatment response

American Journal of Respiratory Cell and Molecular Biology

Volumn 52, Issue 5, 2015, Pages 543-553

  Sharma, Sunita ^a   Kho, Alvin T ^a   Chhabra, Divya ^a   Qiu, Weiliang ^a   Gaedigk, Roger ^b   Vyhlidal, Carrie A ^b   Leeder, J Steven ^b   Barraza Villarreal, Albino ^c   London, Stephanie J ^d   Gilliland, Frank ^e   Raby, Benjamin A ^a   Weiss, Scott T ^a   Tantisira, Kelan G ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b CHILDREN S MERCY HOSPITAL   (United States)

^c INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Asthma; Asthma treatment; Glucocorticoid genes; Lung development

Indexed keywords

DEXAMETHASONE; GLUCOCORTICOID; CCAAT ENHANCER BINDING PROTEIN DELTA; CEBPD PROTEIN, HUMAN; CORTICOSTEROID; DDIT4 PROTEIN, HUMAN; FK 506 BINDING PROTEIN; GENETIC MARKER; TACROLIMUS BINDING PROTEIN 5; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CLINICAL ARTICLE; CONTROLLED STUDY; CORTICOSTEROID THERAPY; FETUS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; HUMAN; HUMAN TISSUE; LUNG DEVELOPMENT; LYMPHOBLASTOID CELL LINE; MOUSE; NONHUMAN; PRINCIPAL COMPONENT ANALYSIS; TREATMENT RESPONSE; ANIMAL; C57BL MOUSE; CASE CONTROL STUDY; DRUG EFFECTS; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETIC MARKER; GENETIC PREDISPOSITION; GENETICS; LUNG; METABOLISM; NEWBORN; PHENOTYPE; PROCEDURES; TREATMENT OUTCOME;

MURINAE;

ADRENAL CORTEX HORMONES; ANIMALS; ANIMALS, NEWBORN; ASTHMA; CASE-CONTROL STUDIES; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; DATABASES, GENETIC; DEXAMETHASONE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC MARKERS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; LUNG; MICE; MICE, INBRED C57BL; PHENOTYPE; PRINCIPAL COMPONENT ANALYSIS; TACROLIMUS BINDING PROTEINS; TRANSCRIPTION FACTORS; TREATMENT OUTCOME;

EID: 84929453325     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2014-0109OC     Document Type: Article

References (47)

1. Bolt RJ, Van Weissenbruch MM, Lafeber HN, Delemarre-Van De Waal HA. Glucocorticoids and lung development in the fetus and preterm infant. Pediatr Pulmonol 2001;32:76-91.
2. Fowden AL, Forhead AJ. Hormones as epigenetic signals in developmental programming. Exp Physiol 2009;94:607-625.
3. Wang JY, Yeh TF, Lin YC, Miyamura K, Holmskov U, Reid KB. Measurement of pulmonary status and surfactant protein levels during dexamethasone treatment of neonatal respiratory distress syndrome. Thorax 1996;51:907-913.
4. Jaskoll T, Choy HA, Melnick M. The glucocorticoid-glucocorticoid receptor signal transduction pathway, transforming growth factorbeta, and embryonic mouse lung development in vivo. Pediatr Res 1996;39:749-759.
5. Grigsby PL, Novy MJ, Sadowsky DW, Morgan TK, Long M, Acosta E, Duffy LB, Waites KB. Maternal azithromycin therapy for Ureaplasma intraamniotic infection delays preterm delivery and reduces fetal lung injury in a primate model. Am J Obstet Gynecol 2012;207:475, e471-475, e414.
6. Crowley P, Chalmers I, Keirse MJ. The effects of corticosteroid administration before preterm delivery: an overview of the evidence from controlled trials. Br J Obstet Gynaecol 1990;97:11-25.
7. Seliem WA, Falk MC, Shadbolt B, Kent AL. Antenatal and postnatal risk factors for neonatal hypertension and infant follow-up. Pediatr Nephrol 2007;22:2081-2087.
8. Pole JD, Mustard CA, To T, Beyene J, Allen AC. Antenatal steroid therapy for fetal lung maturation and the subsequent risk of childhood asthma: a longitudinal analysis. J Pregnancy 2010;2010:789748.
9. Ververeli K, Chipps B. Oral corticosteroid-sparing effects of inhaled corticosteroids in the treatment of persistent and acute asthma. Ann Allergy Asthma Immunol 2004;92:512-522.
10. Pauwels RA, Pedersen S, Busse WW, Tan WC, Chen YZ, Ohlsson SV, Ullman A, Lamm CJ, O'Byrne PM; START Investigators Group. Early intervention with budesonide in mild persistent asthma: a randomised, double-blind trial. Lancet 2003;361:1071-1076.
11. Tantisira KG, Lasky-Su J, Harada M, Murphy A, Litonjua AA, Himes BE, Lange C, Lazarus R, Sylvia J, Klanderman B, et al. Genomewide association between GLCCI1 and response to glucocorticoid therapy in asthma. N Engl J Med 2011;365:1173-1183.
12. Heine VM, Rowitch DH. Hedgehog signaling has a protective effect in glucocorticoid-induced mouse neonatal brain injury through an 11betaHSD2-dependent mechanism. J Clin Invest 2009;119:267-277.
13. Kho AT, Zhao Q, Cai Z, Butte AJ, Kim JY, Pomeroy SL, Rowitch DH, Kohane IS. Conserved mechanisms across development and tumorigenesis revealed by a mouse development perspective of human cancers. Genes Dev 2004;18:629-640.
14. Reddy TE, Pauli F, Sprouse RO, Neff NF, Newberry KM, Garabedian MJ, Myers RM. Genomic determination of the glucocorticoid response reveals unexpected mechanisms of gene regulation. Genome Res 2009;19:2163-2171.
15. Moffatt MF, Kabesch M, Liang L, Dixon AL, Strachan D, Heath S, Depner M, Von Berg A, Bufe A, Rietschel E, et al. Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma. Nature 2007;448:470-473.
16. Qiu W, Koppelman GH, Carey VJ, Ziniti J, London S, Barnes KC, Gilliland FD, Lemanske R, Guilbert TW, Liu A, et al. Expression quantitative trait locus (eqtl) mapping in diverse populations and cell types identifies numerous asthma-associated regulatory variants. American Thoracic Society International Conference. Philadelphia, PA; May 18-22, 2012. p. A2521.
17. Roscioli E, Hamon R, Ruffin RE, Lester S, Zalewski P. Cellular inhibitor of apoptosis-2 is a critical regulator of apoptosis in airway epithelial cells treated with asthma-related inflammatory cytokines. Physiol Rep 2013;1:e00123.
18. Burioka N, Fukuoka Y, Takata M, Endo M, Miyata M, Chikumi H, Tomita K, Kodani M, Touge H, Takeda K, et al. Circadian rhythms in the CNS and peripheral clock disorders: function of clock genes: influence of medication for bronchial asthma on circadian gene. J Pharmacol Sci 2007;103:144-149.
19. Bateman ED, Bousquet J, Busse WW, Clark TJ, Gul N, Gibbs M, Pedersen S; GOAL Steering Committee and Investigators. Stability of asthma control with regular treatment: an analysis of the Gaining Optimal Asthma controL (GOAL) study. Allergy 2008;63:932-938.
20. Cole TJ, Blendy JA, Monaghan AP, Krieglstein K, Schmid W, Aguzzi A, Fantuzzi G, Hummler E, Unsicker K, Schütz G. Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev 1995;9:1608-1621.
21. Kotas RV, Fletcher BD, Torday J, Avery ME. Evidence for independent regulators of organ maturation in fetal rabbits. Pediatrics 1971;47:57-64.
22. Haas DM, Sischy AC, McCullough W, Simsiman AJ. Maternal ethnicity influences on neonatal respiratory outcomes after antenatal corticosteroid use for anticipated preterm delivery. J Matern Fetal Neonatal Med 2011;24:516-520.
23. San Feliciano L, Remesal A, Isidoro-García M, Ludeña D. Dexamethasone and betamethasone for prenatal lung maturation: differences in vascular endothelial growth factor expression and alveolarization in rats. Neonatology 2011;100:105-110.
24. Beers MF, Shuman H, Liley HG, Floros J, Gonzales LW, Yue N, Ballard PL. Surfactant protein B in human fetal lung: developmental and glucocorticoid regulation. Pediatr Res 1995;38:668-675.
25. Jobe AH, Polk D, Ikegami M, Newnham J, Sly P, Kohen R, Kelly R. Lung responses to ultrasound-guided fetal treatments with corticosteroids in preterm lambs. J Appl Physiol (1985) 1993;75:2099-2105.
26. McEvoy C, Bowling S, Williamson K, Stewart M, Durand M. Functional residual capacity and passive compliance measurements after antenatal steroid therapy in preterm infants. Pediatr Pulmonol 2001;31:425-430.
27. McEvoy C, Schilling D, Peters D, Tillotson C, Spitale P, Wallen L, Segel S, Bowling S, Gravett M, Durand M. Respiratory compliance in preterm infants after a single rescue course of antenatal steroids: a randomized controlled trial. Am J Obstet Gynecol 2010;202:544, e541-e549.
28. Pole JD, Mustard CA, To T, Beyene J, Allen AC. Antenatal steroid therapy for fetal lung maturation: is there an association with childhood asthma? J Asthma 2009;46:47-52.
29. Kallapur SG, Kramer BW, Moss TJ, Newnham JP, Jobe AH, Ikegami M, Bachurski CJ. Maternal glucocorticoids increase endotoxin-induced lung inflammation in preterm lambs. Am J Physiol Lung Cell Mol Physiol 2003;284:L633-L642.
30. Kuypers E, Collins JJ, Kramer BW, Ofman G, Nitsos I, Pillow JJ, Polglase GR, Kemp MW, Newnham JP, Gavilanes AW, et al. Intraamniotic LPS and antenatal betamethasone: inflammation and maturation in preterm lamb lungs. Am J Physiol Lung Cell Mol Physiol 2012;302:L380-L389.
31. Cao Z, Umek RM, McKnight SL. Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev 1991;5:1538-1552.
32. Gonzales LW, Guttentag SH, Wade KC, Postle AD, Ballard PL. Differentiation of human pulmonary type II cells in vitro by glucocorticoid plus cAMP. Am J Physiol Lung Cell Mol Physiol 2002;283:L940-L951.
33. Breed DR, Margraf LR, Alcorn JL, Mendelson CR. Transcription factor C/EBPdelta in fetal lung: developmental regulation and effects of cyclic adenosine 39, 59-monophosphate and glucocorticoids. Endocrinology 1997;138:5527-5534.
34. Mendelson CR, Johnston JM, MacDonald PC, Snyder JM. Multihormonal regulation of surfactant synthesis by human fetal lung in vitro. J Clin Endocrinol Metab 1981;53:307-317.
35. 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 1988;123:1712-1720.
36. Ballard PL, Lee JW, Fang X, Chapin C, Allen L, Segal MR, Fischer H, Illek B, Gonzales LW, Kolla V, et al. Regulated gene expression in cultured type II cells of adult human lung. Am J Physiol Lung Cell Mol Physiol 2010;299:L36-L50.
37. Wade KC, Guttentag SH, Gonzales LW, Maschhoff KL, Gonzales J, Kolla V, Singhal S, Ballard PL. Gene induction during differentiation of human pulmonary type II cells in vitro. Am J Respir Cell Mol Biol 2006;34:727-737.
38. Hakonarson H, Maskeri N, Carter C, Hodinka RL, Campbell D, Grunstein MM. Mechanism of rhinovirus-induced changes in airway smooth muscle responsiveness. J Clin Invest 1998;102:1732-1741.
39. Oliver BG, Johnston SL, Baraket M, Burgess JK, King NJ, Roth M, Lim S, Black JL. Increased proinflammatory responses from asthmatic human airway smooth muscle cells in response to rhinovirus infection. Respir Res 2006;7:71.
40. Brugarolas J, Lei K, Hurley RL, Manning BD, Reiling JH, Hafen E, Witters LA, Ellisen LW, Kaelin WG Jr. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev 2004;18:2893-2904.
41. Otulakowski G, Duan W, Sarangapani A, Gandhi S, O'Brodovich H. Glucocorticoid-mediated repression of REDD1 mRNA expression in rat fetal distal lung epithelial cells. Pediatr Res 2009;65:514-519.
42. Yoshida T, Mett I, Bhunia AK, Bowman J, Perez M, Zhang L, Gandjeva A, Zhen L, Chukwueke U, Mao T, et al. Rtp801, a suppressor of mTOR signaling, is an essential mediator of cigarette smoke-induced pulmonary injury and emphysema. Nat Med 2010;16:767-773.
43. Davies TH, Ning YM, Sánchez ER. A new first step in activation of steroid receptors: hormone-induced switching of FKBP51 and FKBP52 immunophilins. J Biol Chem 2002;277:4597-4600.
44. Chivers JE, Gong W, King EM, Seybold J, Mak JC, Donnelly LE, Holden NS, Newton R. Analysis of the dissociated steroid RU24858 does not exclude a role for inducible genes in the anti-inflammatory actions of glucocorticoids. Mol Pharmacol 2006;70:2084-2095.
45. Kaur M, Chivers JE, Giembycz MA, Newton R. Long-acting beta2-adrenoceptor agonists synergistically enhance glucocorticoiddependent transcription in human airway epithelial and smooth muscle cells. Mol Pharmacol 2008;73:203-214.
46. Kelly MM, King EM, Rider CF, Gwozd C, Holden NS, Eddleston J, Zuraw B, Leigh R, O'Byrne PM, Newton R. Corticosteroid-induced gene expression in allergen-challenged asthmatic subjects taking inhaled budesonide. Br J Pharmacol 2012;165:1737-1747.
47. Hawkins GA, Lazarus R, Smith RS, Tantisira KG, Meyers DA, Peters SP, Weiss ST, Bleecker ER. The glucocorticoid receptor heterocomplex gene STIP1 is associated with improved lung function in asthmatic subjects treated with inhaled corticosteroids. J Allergy Clin Immunol 2009;123:1376-1383, e1377.