RNA-Seq transcriptome profiling identifies CRISPLD2 as a glucocorticoid responsive gene that modulates cytokine function in airway smooth muscle cells

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Himes, Blanca E ^a,b,c   Jiang, Xiaofeng ^d   Wagner, Peter ^d   Hu, Ruoxi ^d   Wang, Qiyu ^d   Klanderman, Barbara ^b   Whitaker, Reid M ^a   Duan, Qingling ^a   Lasky Su, Jessica ^a   Nikolos, Christina ^e   Jester, William ^e   Johnson, Martin ^e   Panettieri Jr , Reynold A ^e   Tantisira, Kelan G ^a   Weiss, Scott T ^a,b   Lu, Quan ^d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b LABORATORY FOR MOLECULAR MEDICINE   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEXAMETHASONE; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; PER1 PROTEIN; SMALL INTERFERING RNA; ANTIINFLAMMATORY AGENT; CELL ADHESION MOLECULE; CRISPLD2 PROTEIN, HUMAN; INTERFERON REGULATORY FACTOR;

AIRWAY SMOOTH MUSCLE CELL; ARTICLE; C7 GENE; CCDC69 GENE; CONTROLLED STUDY; CRISPLD2 GENE; CYTOKINE RESPONSE; DUSP1 GENE; GENE; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; KLF15 GENE; MALE; NUCLEOTIDE SEQUENCE; PER1 GENE; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; SMOOTH MUSCLE FIBER; TSC22D3 GENE; WESTERN BLOTTING; ASTHMA; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; INHALATIONAL DRUG ADMINISTRATION; LUNG; METABOLISM; PATHOLOGY; PROCEDURES; SEQUENCE ANALYSIS; SMOOTH MUSCLE;

ADMINISTRATION, INHALATION; ANTI-INFLAMMATORY AGENTS; ASTHMA; CELL ADHESION MOLECULES; CELL LINE; DEXAMETHASONE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; INTERFERON REGULATORY FACTORS; LUNG; MUSCLE, SMOOTH; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, RNA;

EID: 84903193221     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099625     Document Type: Article

References (68)

1. Akinbami L, Moorman J, Bailey C, Zahran H, King M, et al. (2012) Trends in asthma prevalence, health care use, and mortality in the United States, 2001-2010. Hyattsville, MD: National Center for Health Statistics.
2. Global Initiative for Asthma (GINA). (2012) Global Strategy for Asthma Management and Prevention. Available from: http://www.ginasthma.org/.
3. Rhen T, Cidlowski JA (2005) Antiinflammatory action of glucocorticoids - new mechanisms for old drugs. N Engl J Med 353: 1711-1723.
4. Fanta CH (2009) Asthma. N Engl J Med 360: 1002-1014.
5. Pratt WB, Morishima Y, Murphy M, Harrell M (2006) Chaperoning of glucocorticoid receptors. Handb Exp Pharmacol: 111-138.
6. McMaster A, Ray DW (2007) Modelling the glucocorticoid receptor and producing therapeutic agents with anti-inflammatory effects but reduced side-effects. Exp Physiol 92: 299-309. (Pubitemid 46376317)
7. Slats AM, Sont JK, van Klink RH, Bel EH, Sterk PJ (2006) Improvement in bronchodilation following deep inspiration after a course of high-dose oral prednisone in asthma. Chest 130: 58-65. (Pubitemid 44116841)
8. Trifilieff A, El-Hashim A, Bertrand C (2000) Time course of inflammatory and remodeling events in a murine model of asthma: effect of steroid treatment. Am J Physiol Lung Cell Mol Physiol 279: L1120-1128. (Pubitemid 32009498)
9. Lakser OJ, Dowell ML, Hoyte FL, Chen B, Lavoie TL, et al. (2008) Steroids augment relengthening of contracted airway smooth muscle: potential additional mechanism of benefit in asthma. Eur Respir J 32: 1224-1230.
10. Lamas AM, Leon OG, Schleimer RP (1991) Glucocorticoids inhibit eosinophil responses to granulocyte-macrophage colony-stimulating factor. J Immunol 147: 254-259.
11. Wallen N, Kita H, Weiler D, Gleich GJ (1991) Glucocorticoids inhibit cytokine-mediated eosinophil survival. J Immunol 147: 3490-3495.
12. Reddy TE, Pauli F, Sprouse RO, Neff NF, Newberry KM, et al. (2009) Genomic determination of the glucocorticoid response reveals unexpected mechanisms of gene regulation. Genome Res 19: 2163-2171.
13. Shore SA, Moore PE (2003) Regulation of beta-adrenergic responses in airway smooth muscle. Respir Physiol Neurobiol 137: 179-195. (Pubitemid 37158008)
14. Panettieri RA, Jr., Kotlikoff MI, Gerthoffer WT, Hershenson MB, Woodruff PG, et al. (2008) Airway smooth muscle in bronchial tone, inflammation, and remodeling: basic knowledge to clinical relevance. Am J Respir Crit Care Med 177: 248-252. (Pubitemid 351198366)
15. Nelson HS (1995) Beta-adrenergic bronchodilators. N Engl J Med 333: 499-506.
16. Hargreave FE, Ryan G, Thomson NC, O'Byrne PM, Latimer K, et al. (1981) Bronchial responsiveness to histamine or methacholine in asthma: measurement and clinical significance. J Allergy Clin Immunol 68: 347-355. (Pubitemid 12235137)
17. Masuno K, Haldar SM, Jeyaraj D, Mailloux CM, Huang X, et al. (2011) Expression profiling identifies Klf15 as a glucocorticoid target that regulates airway hyperresponsiveness. Am J Respir Cell Mol Biol 45: 642-649.
18. Misior AM, Deshpande DA, Loza MJ, Pascual RM, Hipp JD, et al. (2009) Glucocorticoid- and protein kinase A-dependent transcriptome regulation in airway smooth muscle. Am J Respir Cell Mol Biol 41: 24-39.
19. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63.
20. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
21. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, et al. (2012) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31: 46-53.
22. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18: 1509-1517.
23. Hochberg Y, Benjamini Y (1990) More powerful procedures for multiple significance testing. Stat Med 9: 811-818. (Pubitemid 20343989)
24. Shipp LE, Lee JV, Yu CY, Pufall M, Zhang P, et al. (2010) Transcriptional regulation of human dual specificity protein phosphatase 1 (DUSP1) gene by glucocorticoids. PLoS One 5: e13754.
25. Kelly MM, King EM, Rider CF, Gwozd C, Holden NS, et al. (2012) Corticosteroid-induced gene expression in allergen-challenged asthmatic subjects taking inhaled budesonide. Br J Pharmacol 165: 1737-1747.
26. Burioka N, Fukuoka Y, Takata M, Endo M, Miyata M, et al. (2007) 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 103: 144-149. (Pubitemid 46294644)
27. Eddleston J, Herschbach J, Wagelie-Steffen AL, Christiansen SC, Zuraw BL (2007) The anti-inflammatory effect of glucocorticoids is mediated by glucocorticoid-induced leucine zipper in epithelial cells. J Allergy Clin Immunol 119: 115-122. (Pubitemid 46037795)
28. Huang da W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
29. Kaur M, Chivers JE, Giembycz MA, Newton R (2008) Long-acting beta2-adrenoceptor agonists synergistically enhance glucocorticoid-dependent transcription in human airway epithelial and smooth muscle cells. Molecular pharmacology 73: 203-214. (Pubitemid 350294211)
30. Himes BE, Jiang X, Hu R, Wu AC, Lasky-Su JA, et al. (2012) Genome-Wide Association Analysis in Asthma Subjects Identifies SPATS2L as a Novel Bronchodilator Response Gene. PLoS Genet 8: e1002824.
31. Wang ZQ, Xing WM, Fan HH, Wang KS, Zhang HK, et al. (2009) The novel lipopolysaccharide-binding protein CRISPLD2 is a critical serum protein to regulate endotoxin function. J Immunol 183: 6646-6656.
32. Rincon M, Irvin CG (2012) Role of IL-6 in asthma and other inflammatory pulmonary diseases. Int J Biol Sci 8: 1281-1290.
33. Harada A, Sekido N, Akahoshi T, Wada T, Mukaida N, et al. (1994) Essential involvement of interleukin-8 (IL-8) in acute inflammation. J Leukoc Biol 56: 559-564. (Pubitemid 24348812)
34. Schacke H, Docke WD, Asadullah K (2002) Mechanisms involved in the side effects of glucocorticoids. Pharmacol Ther 96: 23-43. (Pubitemid 35346616)
35. Thierry-Mieg D, Thierry-Mieg J (2006) AceView: a comprehensive cDNA-supported gene and transcripts annotation. Genome Biol 7 Suppl 1: S12 11-14.
36. Lu NZ, Cidlowski JA (2006) Glucocorticoid receptor isoforms generate transcription specificity. Trends in cell biology 16: 301-307. (Pubitemid 43884980)
37. Doni A, Mantovani G, Porta C, Tuckermann J, Reichardt HM, et al. (2008) Cell-specific regulation of PTX3 by glucocorticoid hormones in hematopoietic and nonhematopoietic cells. The Journal of biological chemistry 283: 29983-29992.
38. Moodley T, Wilson SM, Joshi T, Rider CF, Sharma P, et al. (2013) Phosphodiesterase 4 inhibitors augment the ability of formoterol to enhance glucocorticoid-dependent gene transcription in human airway epithelial cells: a novel mechanism for the clinical efficacy of roflumilast in severe chronic obstructive pulmonary disease. Molecular pharmacology 83: 894-906.
39. Wang J, Zhuang J, Iyer S, Lin X, Whitfield TW, et al. (2012) Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome research 22: 1798-1812.
40. Lekstrom-Himes J, Xanthopoulos KG (1998) Biological role of the CCAAT/enhancer-binding protein family of transcription factors. The Journal of biological chemistry 273: 28545-28548. (Pubitemid 28507532)
41. Berg T, Cassel TN, Schwarze PE, Nord M (2002) Glucocorticoids regulate the CCSP and CYP2B1 promoters via C/EBPbeta and delta in lung cells. Biochemical and biophysical research communications 293: 907-912. (Pubitemid 34700185)
42. Yang H, Mammen J, Wei W, Menconi M, Evenson A, et al. (2005) Expression and activity of C/EBPbeta and delta are upregulated by dexamethasone in skeletal muscle. Journal of cellular physiology 204: 219-226. (Pubitemid 40776825)
43. Berg T, Didon L, Barton J, Andersson O, Nord M (2005) Glucocorticoids increase C/EBPbeta activity in the lung epithelium via phosphorylation. Biochemical and biophysical research communications 334: 638-645. (Pubitemid 40982414)
44. Akira S, Isshiki H, Sugita T, Tanabe O, Kinoshita S, et al. (1990) A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. The EMBO journal 9: 1897-1906.
45. Oyewumi L, Kaplan F, Gagnon S, Sweezey NB (2003) Antisense oligodeoxynucleotides decrease LGL1 mRNA and protein levels and inhibit branching morphogenesis in fetal rat lung. Am J Respir Cell Mol Biol 28: 232-240. (Pubitemid 36169653)
46. Chiquet BT, Lidral AC, Stal S, Mulliken JB, Moreno LM, et al. (2007) CRISPLD2: a novel NSCLP candidate gene. Hum Mol Genet 16: 2241-2248. (Pubitemid 47354906)
47. Wang T, Wang ZQ, Wang L, Yan L, Wan J, et al. (2013) CRISPLD2 is expressed at low levels during septic shock and is associated with procalcitonin. PloS one 8: e65743.
48. Patel GP, Balk RA (2012) Systemic steroids in severe sepsis and septic shock. American journal of respiratory and critical care medicine 185: 133-139.
49. Doreswamy V, Peden DB (2011) Modulation of asthma by endotoxin. Clin Exp Allergy 41: 9-19.
50. Roos AB, Barton JL, Miller-Larsson A, Dahlberg B, Berg T, et al. (2012) Lung epithelial-C/EBPbeta contributes to LPS-induced inflammation and its suppression by formoterol. Biochemical and biophysical research communications 423: 134-139.
51. Yick CY, Zwinderman AH, Kunst PW, Grunberg K, Mauad T, et al. (2013) Glucocorticoid-induced Changes in Gene Expression of Airway Smooth Muscle in Patients with Asthma. Am J Respir Crit Care Med 187: 1076-1084.
52. Panettieri RA, Murray RK, DePalo LR, Yadvish PA, Kotlikoff MI (1989) A human airway smooth muscle cell line that retains physiological responsiveness. Am J Physiol 256: C329-335.
53. Cooper PR, Mesaros AC, Zhang J, Christmas P, Stark CM, et al. (2010) 20-HETE mediates ozone-induced, neutrophil-independent airway hyper-responsiveness in mice. PLoS One 5: e10235.
54. Andrews S FastQC A Quality Control tool for High Throughput Sequence Data.
55. Pearson WR, Wood T, Zhang Z, Miller W (1997) Comparison of DNA sequences with protein sequences. Genomics 46: 24-36. (Pubitemid 27527688)
56. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, et al. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36.
57. Barnett DW, Garrison EK, Quinlan AR, Stromberg MP, Marth GT (2011) BamTools: a C++ API and toolkit for analyzing and managing BAM files. Bioinformatics 27: 1691-1692.
58. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628. (Pubitemid 351911867)
59. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, et al. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562-578.
60. Childhood Asthma Management Program Research Group. (1999) The Childhood Asthma Management Program (CAMP): design, rationale, and methods. Control Clin Trials 20: 91-120.
61. Peters SP, Anthonisen N, Castro M, Holbrook JT, Irvin CG, et al. (2007) Randomized comparison of strategies for reducing treatment in mild persistent asthma. N Engl J Med 356: 2027-2039. (Pubitemid 46789893)
62. Guilbert TW, Morgan WJ, Krawiec M, Lemanske RF, Jr., Sorkness C, et al. (2004) The Prevention of Early Asthma in Kids study: design, rationale and methods for the Childhood Asthma Research and Education network. Control Clin Trials 25: 286-310. (Pubitemid 38626165)
63. Denlinger LC, Sorkness CA, Chinchilli VM, Lemanske RF, Jr. (2007) Guideline-defining asthma clinical trials of the National Heart, Lung, and Blood Institute's Asthma Clinical Research Network and Childhood Asthma Research and Education Network. J Allergy Clin Immunol 119: 3-11; quiz 12-13.
64. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559-575. (Pubitemid 47330214)
65. Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. Bioinformatics and Computational Biology Solutions using R and Bioconductor. New York: Springer. pp. 397-420.
66. Gautier L, Cope L, Bolstad BM, Irizarry RA (2004) affy - analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315. (Pubitemid 38262761)
67. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature methods 9: 671-675.
68. Pruim RJ, Welch RP, Sanna S, Teslovich TM, Chines PS, et al. (2010) LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics 26: 2336-2337.