Integrated Transcriptomic and Epigenomic Analysis of Primary Human Lung Epithelial Cell Differentiation

PLoS Genetics

Volumn 9, Issue 6, 2013, Pages

  Marconett, Crystal N ^a,b   Zhou, Beiyun ^a,b   Rieger, Megan E ^a,b   Selamat, Suhaida A ^a,b   Dubourd, Mickael ^a,b   Fang, Xiaohui ^c,d   Lynch, Sean K ^e   Stueve, Theresa Ryan ^a,b   Siegmund, Kimberly D ^a,b   Berman, Benjamin P ^a,b   Borok, Zea ^a,b   Laird Offringa, Ite A ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Department of Product Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 4ALPHA; RETINOID X RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL TYPE; CHROMATIN STRUCTURE; EPIGENETICS; EPITHELIUM CELL; GENE CONTROL; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS EPITHELIUM; LUNG INJURY; NONHUMAN; PHENOTYPE; RAT; TRANSCRIPTION INITIATION; TRANSCRIPTOMICS;

ADULT; ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; EPIGENOMICS; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; PRIMARY CELL CULTURE; RATS; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84879629126     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003513     Document Type: Article

References (70)

1. Sharma S, Kelly TK, Jones PA, (2010) Epigenetics in cancer. Carcinogenesis 31: 27-36.
2. Vasanthi D, Mishra RK, (2008) Epigenetic regulation of genes during development: a conserved theme from flies to mammals. J Genet Genomics 35: 413-429.
3. Bernstein BE, Meissner A, Lander ES, (2007) The mammalian epigenome. Cell 128: 669-681.
4. Hirschhorn JN, Brown SA, Clark CD, Winston F, (1992) Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev 6: 2288-2298.
5. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA, (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130: 77-88.
6. Jia L, Shen HC, Wantroba M, Khalid O, Wang Q, et al. (2006) Locus-wide chromatin remodeling and enhanced androgen receptor-mediated transcription in recurrent prostate tumor cells. Mol Cell Bio 26: 7331-7341.
7. Wan H, Dingle S, Xu Y, Besnard V, Kaestner KH, et al. (2005) Compensatory roles of Foxa1 and Foxa2 during lung morphogenesis. J Biol Chem 280: 13809-13816.
8. Mai A, Massa S, Rotili D, Cerbara I, Valente S, et al. (2005) Histone deacetylation in epigenetics: an attractive target for anticancer therapy. Med Res Rev 25: 261-309.
9. Saraiva NZ, Oliveira CS, Garcia JM, (2010) Histone acetylation and its role in embryonic stem cell differentiation. World J Stem Cells 2: 121-126.
10. Boeger H, Griesenbeck J, Strattan JS, Kornberg RD, (2003) Nucleosomes unfold completely at a transcriptionally active promoter. Mol Cell 11: 1587-1598.
11. Sparmann A, van Lohuizen M, (2006) Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer 6: 846-856.
12. Müller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, et al. (2002) Histone methyltransferase activity of a Drosophila polycomb group repressor complex. Cell 111: 197-208.
13. Schwartz YB, Pirrotta V, (2008) Polycomb complexes and epigenetic states. Curr Opin Cell Biol 20: 266-273.
14. Murry CE, Keller G, (2008) Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132: 661-680.
15. Fuchs S, Hollins AJ, Laue M, Schaefer UF, Roemer K, et al. (2003) Differentiation of human alveolar epithelial cells in primary culture: morphological characterization and synthesis of caveolin-1 and surfactant protein-C. Cell Tissue Res 311: 31-45.
16. Zhou B, Ann DK, Flodby P, Minoo P, Liebler JM, et al. (2008) Rat aquaporin-5 4.3-kb 5′-flanking region differentially regulates expression in salivary gland and lung in vivo. Am J Physiol Cell Physiol 295: C111-C120.
17. Fehrenbach H, (2001) Alveolar epithelial type II cell: defender of the alveolus revisited. Respir Res 2: 33-46.
18. Chapman HA, Li X, Alexander JP, Brumwell A, Lorizio W, et al. (2011) Integrin α6β4 identifies an adult distal epithelial population with regenerative potential in mice. J Clin Invest 121: 2855-2862.
19. Borok Z, Danto SI, Lubman RL, Cao Y, Williams MC, et al. (1998) Modulation of t1α expression with alveolar epithelial cell phenotype in vitro. Am J Physiol Lung Cell Mol Physiol 275: L155-164.
20. Fang X, Song Y, Zemans R, Hirsch J, Matthay MA, (2004) Fluid transport across cultured rat alveolar epithelial cells: a novel in vitro system. Am J Physiol Lung Cell Mol Physiol 287: L104-10.
21. Flodby P, Borok Z, Banfalvi A, Zhou B, Gao D, et al. (2010) Directed expression of Cre in alveolar epithelial type 1 cells. Am J Respir Cell Mol Biol 43: 173-178.
22. Nielsen S, King LS, Christensen BM, Agre P, (1997) Aquaporins in complex tissues. II. Subcellular distribution in respiratory and glandular tissues of rat. Am J Physiol Cell Physiol 273: C1549-C1561.
23. Campbell L, Hollins AJ, Al-Eid A, Newman GR, von Ruhland C, et al. (1999) Caveolin-1 expression and caveolae biogenesis during cell transdifferentiation in lung alveolar epithelial primary cultures. Biochem Biophys Res Commun 262: 744-751.
24. Newman DR, Zhang H, Bortoff K, Bonner JC, Sannes PL, (2010) Alveolar epithelial differentiation during repair involves FoxA1, Wnt7A, and TGF-β. Proc Am Thorac Soc 7: 155-156.
25. Ramirez MI, Millien G, Hinds A, Cao Y, Seldin DC, et al. (2003) T1alpha, a lung type I cell differentiation gene, is required for normal lung cell proliferation and alveolus formation at birth. Dev Biol 256: 61-72.
26. Millien G, Spira A, Hinds A, Wang J, Williams MC, et al. (2006) Alterations in gene expression in T1α null lung: a model of deficient alveolar sac development. BMC Dev Biol 6: 35.
27. Mason RJ, Williams MC, Widdicombe JH, Sanders MJ, Misfeldt DS, et al. (1982) Transepithelial transport by pulmonary alveolar type II cells in primary culture. Proc Natl Acad Sci U S A 79: 6033-6037.
28. Qiao R, Zhou B, Liebler JM, Li X, Crandall ED, et al. (2003) Identification of three genes of known function expressed by alveolar epithelial type I cells. Am J Respir Cell Mol Biol 29: 98-105.
29. Ballard PL, Lee JW, Fang X, Chapin C, Allen L, et al. (2010) Regulated gene expression in cultured type II cells of adult human lung. Am J Physiol Lung Cell Mol Physiol 299: L36-50.
30. Cheek JM, Evans MJ, Crandall ED, (1989) Type I cell-like morphology in tight alveolar epithelial monolayers. Exp Cell Res 184: 375-387.
31. Cheek JM, Kim KJ, Crandall ED, (1989) Tight monolayers of rat alveolar epithelial cells: bioelectric properties and active sodium transport. Am J Physiol 256: C688-93.
32. Wang J, Edeen K, Manzer R, Chang Y, Wang S, et al. (2007) Differentiated human alveolar epithelial cells and reversibility of their phenotype in vitro. Am J Respir Cell Mol Biol 36: 661-668.
33. Zhou B, Francis TA, Yang H, Tseng W, Zhong Q, et al. (2008) GATA-6 mediates transcriptional activation of aquaporin-5 through interactions with Sp1. Am J Physiol Cell Physiol 295: C1141-C1150.
34. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, et al. (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38: 576-589.
35. Flozak AS, Lam AP, Russell S, Jain M, Peled ON, et al. (2010) Beta-catenin/T cell factor signaling is activated during lung injury and promotes the survival and migration of alveolar epithelial cells. J Biol Chem 285: 3157-3167.
36. Newman GR, Campbell L, von Ruhland C, Jasani B, Gumbleton M, (1999) Caveolin and its cellular and subcellular immunolocalisation in lung alveolar epithelium: implications for alveolar epithelial type I cell function. Cell Tissue Res 295: 111-120.
37. Foster C, Aktar A, Kopf D, Zhang P, Guttentag S, (2004) Pepsinogen C: a type 2 cell-specific protease. Am J Physiol Lung Cell Mol Physiol 286: L382-L387.
38. Mucenski ML, Wert SE, Nation JM, Loudy DE, Huelsken J, et al. (2003) β-catenin is required for specification of proximal/distal cell fate during lung morphogenesis. J Biol Chem 278: 40231-40238.
39. Tebar M, Destree O, de Vree WJ, Ten Have-Opbroek AA, (2001) Expression of Tcf/Lef and sFrp and localization of beta-catenin in the developing mouse lung. Mech Dev 109: 437-440.
40. Lefebvre P, Benomar Y, Staels B, (2010) Retinoid X receptors: common heterodimerization partners with distinct functions. Trends Endocrinol Metabol 21: 676-683.
41. McGowan S, Jackson SK, Jenkins-Moore M, Dai HH, Chambon P, et al. (2000) Mice bearing deletions of retinoic acid receptors demonstrate reduced lung elastin and alveolar numbers. Am J Respir Cell Mol Biol 23: 162-167.
42. Simon DM, Mariani TJ, (2007) Role of PPARs and retinoid X receptors in the regulation of lung maturation and development. PPAR Res 2007: 91240.
43. Zhang H, Garber SJ, Cui Z, Foley JP, Mohan GS, et al. (2009) The angiogenic factor midkine is regulated by dexamethasome and retinoic acid during alveolarization and in alveolar epithelial cells. Respir Res 10: 77.
44. Kimura Y, Suzuki T, Kaneko C, Darnel AD, Moriya T, et al. (2002) Retinoid receptors in the developing human lung. Clin Sci 103: 613-621.
45. Hind M, Maden M, (2004) Retinoic acid induces alveolar regeneration in the adult mouse lung. Eur Respir J 23: 20-27.
46. Sugimoto K, Takayasu H, Nakazawa N, Montedonico S, Puri P, (2008) Prenatal treatment with retinoic acid accelerates type 1 alveolar cell proliferation of the hypoplastic lung in the nitrofen model of congenital diaphragmatic hernia. J Pediatr Surg 43: 367-372.
47. Montedocino S, Sugimoto K, Felle P, Bannigan J, Puri P, (2008) Prenatal treatment with retinoic acid promotes pulmonary alveologenesis in the nitrofen model of congenital diaphragmatic hernia. J Pediatr Surg 43: 500-507.
48. Baybutt RC, Smith BW, Donskaya EV, Hu L, Li T, et al. (2010) The proliferative effects of retinoic acid on primary cultures of adult rat type II pneumocytes depend upon cell density. In Vitro Cell Dev Biol Anim 46: 20-27.
49. Perez E, Bourguet W, Gronemeyer H, de Lera AR, (2012) Modulation of RXR function through ligand design. Biochim Biophys Acta 1821: 57-69.
50. Nahoum V, Pérez E, Germain P, Rodríquez-Barrios F, Manzo F, et al. (2007) Modulators of the structural dynamics of the retinoid X receptor to reveal receptor function. Proc Natl Acad Sci U S A 104: 17323-17328.
51. Fujino N, Kubo H, Ota C, Suzuki T, Suzuki S, et al. (2012) A novel method for isolating individual cellular components from the adult human distal lung. Am J Respir Cell Mol Biol 46: 442-430.
52. Sugahara K, Sadohara T, Sugita M, Iyama K, Takiguchi M, (1999) Differential expression of CCAAT enhancer binding protein family in rat alveolar epithelial cell proliferation and in acute lung injury. Cell Tissue Res 297: 261-270.
53. Balci O, Ozdemir S, Mahmoud AS, Acar A, Colakoglu MC, (2010) The effect of antenatal steroids on fetal lung maturation between the 34th and 36th week of pregnancy. Gynecol Obstet Invest 70: 95-99.
54. Oikonomou N, Harokopos V, Zalevsky J, Valavanis C, Kotanidou A, et al. (2006) Soluble TNF mediates the transition from pulmonary inflammation to fibrosis. PLoS One 1: e108.
55. Besnard V, Wert SE, Kaestner KH, Whitsett JA, (2005) Stage-specific regulation of respiratory epithelial cell differentiation by Foxa1. Am J Physiol Lung Cell Mol Physiol 289: L750-L759.
56. Kel AE, Gössling E, Reuter I, Cheremushkin E, Kel-Margoulis OV, et al. (2003) MATCH: A tool for searching transcription factor binding sites in DNA sequences. Nucleic Acids Res 31: 3576-3579.
57. Zhou B, Zhong Q, Minoo P, Li C, Ann DK, et al. (2008) Foxp2 inhibits Nkx2.1-mediated transcription of SP-C via interactions with the Nkx2.1 homeodomain. Am J Respir Cell Mol Biol 38: 750-758.
58. Du P, Kibbe WA, Lin SM, (2008) lumi: a pipeline for processing Illumina microarray. Bioinformatics 24: 1547-1548.
59. Smyth GK, (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3Article 3.
60. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57: 289-300.
61. Huang DW, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protoc 4: 44-57.
62. Huang DW, Sherman BT, Lempicki RA, (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13.
63. Mouse Genome Informatics (MGI) Web, The Jackson Laboratory, Bar Harbor, Maine. (URL: http://www.informatics.jax.org). [retrieved 2/2011].
64. Jia L, Kim J, Shen H, Clark PE, Tilley WD, et al. (2003) Androgen receptor activity at the prostate specific antigen locus: steroidal and non-steroidal mechanisms. Mol Cancer Res 1: 385-392.
65. Zang C, Schones DE, Zeng C, Cui K, Zhao K, et al. (2009) A clustering approach for identification of enriched domains from histone modification ChIP-seq data. Bioinformatics 25: 1952-1958.
66. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, et al. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39: 311-318.
67. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, et al. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
68. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560.
69. Pan G, Tian S, Nie J, Yang C, Ruotti V, et al. (2007) Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1: 299-312.
70. Zhao XD, Han X, Chew JL, Liu J, Chiu KP, et al. (2007) Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 1: 286-298.