Evidence for multiple roles for grainyheadlike 2 in the establishment and maintenance of human mucociliary airway epithelium

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 23, 2013, Pages 9356-9361

  Gao, Xia ^a   Vockley, Christopher M ^a   Pauli, Florencia ^b   Newberry, Kimberly M ^b   Xue, Yan ^a   Randell, Scott H ^c   Reddy, Timothy E ^a,d   Hogan, Brigid L M ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRAINYHEADLIKE 2 PROTEIN; RNA; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; BRONCHIAL EPITHELIAL CELL; BRONCHUS MUCOSA; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTILITY; CELL STRUCTURE; CHROMATIN IMMUNOPRECIPITATION; CILIATED EPITHELIUM; CONTROLLED STUDY; EPITHELIUM BASAL CELL; EPITHELIUM CELL; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE TARGETING; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MICROARRAY; RESPIRATORY EPITHELIUM; RNA SEQUENCE; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

CELL ADHESION; CELL DIFFERENTIATION; CELL MOVEMENT; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GENETIC VECTORS; HUMANS; IMMUNOHISTOCHEMISTRY; LENTIVIRUS; MICROARRAY ANALYSIS; MORPHOGENESIS; REAL-TIME POLYMERASE CHAIN REACTION; RESPIRATORY MUCOSA; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION FACTORS;

EID: 84878734846     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1307589110     Document Type: Article

References (47)

1. Rock JR, Randell SH, Hogan BL (2010) Airway basal stem cells: A perspective on their roles in epithelial homeostasis and remodeling. Dis Model Mech 3(9-10):545-556.
2. Crystal RG, Randell SH, Engelhardt JF, Voynow J, Sunday ME (2008) Airway epithelial cells: Current concepts and challenges. Proc Am Thorac Soc 5(7):772-777.
3. Shen L, Weber CR, Raleigh DR, Yu D, Turner JR (2011) Tight junction pore and leak pathways: A dynamic duo. Annu Rev Physiol 73:283-309.
4. Koval M (2013) Claudin heterogeneity and control of lung tight junctions. Annu Rev Physiol 75:551-567.
5. Man Y, Hart VJ, Ring CJ, Sanjar S, West MR (2000) Loss of epithelial integrity resulting from E-cadherin dysfunction predisposes airway epithelial cells to adenoviral infection. Am J Respir Cell Mol Biol 23(5):610-617.
6. Shaykhiev R, et al. (2011) Cigarette smoking reprograms apical junctional complex molecular architecture in the human airway epithelium in vivo. Cell Mol Life Sci 68(5): 877-892.
7. Xiao C, et al. (2011) Defective epithelial barrier function in asthma. J Allergy Clin Immunol 128(3):549-556.
8. Que J, Luo X, Schwartz RJ, Hogan BL (2009) Multiple roles for Sox2 in the developing and adult mouse trachea. Development 136(11):1899-1907.
9. Werth M, et al. (2010) The transcription factor grainyhead-like 2 regulates the molecular composition of the epithelial apical junctional complex. Development 137(22): 3835-3845.
10. Hopkin AS, et al. (2012) GRHL3/GET1 and trithorax group members collaborate to activate the epidermal progenitor differentiation program. PLoS Genet 8(7):e1002829.
11. Wang S, Samakovlis C (2012) Grainy head and its target genes in epithelial morphogenesis and wound healing. Curr Top Dev Biol 98:35-63.
12. Wilanowski T, et al. (2008) Perturbed desmosomal cadherin expression in grainy head-like 1-null mice. EMBO J 27(6):886-897.
13. Senga K, Mostov KE, Mitaka T, Miyajima A, Tanimizu N (2012) Grainyhead-like 2 regulates epithelial morphogenesis by establishing functional tight junctions through the organization of a molecular network among claudin3, claudin4, and Rab25. Mol Biol Cell 23(15):2845-2855.
14. Ting SB, et al. (2005) A homolog of Drosophila grainy head is essential for epidermal integrity in mice. Science 308(5720):411-413.
15. Auden A, et al. (2006) Spatial and temporal expression of the Grainyhead-like transcription factor family during murine development. Gene Expr Patterns 6(8):964-970.
16. Varma S, et al. (2012) The transcription factors Grainyhead-like 2 and NK2-homeobox 1 form a regulatory loop that coordinates lung epithelial cell morphogenesis and differentiation. J Biol Chem 287(44):37282-37295.
17. Pyrgaki C, Liu A, Niswander L (2011) Grainyhead-like 2 regulates neural tube closure and adhesion molecule expression during neural fold fusion. Dev Biol 353(1):38-49.
18. Pezzulo AA, et al. (2011) The air-liquid interface and use of primary cell cultures are important to recapitulate the transcriptional profile of in vivo airway epithelia. Am J Physiol Lung Cell Mol Physiol 300(1):L25-L31.
19. Bhandari A, et al. (2013) The Grainyhead transcription factor Grhl3/Get1 suppresses miR-21 expression and tumorigenesis in skin: Modulation of the miR-21 target MSH2 by RNA-binding protein DND1. Oncogene 32(12):1497-1507.
20. McLean CY, et al. (2010) GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 28(5):495-501.
21. Bauer H, Zweimueller-Mayer J, Steinbacher P, Lametschwandtner A, Bauer HC (2010) The dual role of zonula occludens (ZO) proteins. J Biomed Biotechnol 2010:402593.
22. Cheng TL, et al. (2011) Functions of rhomboid family protease RHBDL2 and thrombomodulin in wound healing. J Invest Dermatol 131(12):2486-2494.
23. Tarbé NG, Rio MC, Weidle UH (2004) SMAGP, a new small trans-membrane glycoprotein altered in cancer. Oncogene 23(19):3395-3403.
24. Ding X, Jiang QB, Li R, Chen S, Zhang S (2012) NOK/STYK1 has a strong tendency towards forming aggregates and colocalises with epidermal growth factor receptor in endosomes. Biochem Biophys Res Commun 421(3):468-473.
25. Caddy J, et al. (2010) Epidermal wound repair is regulated by the planar cell polarity signaling pathway. Dev Cell 19(1):138-147.
26. Liu JY, et al. (2009) Vav proteins are necessary for correct differentiation of mouse cecal and colonic enterocytes. J Cell Sci 122(Pt 3):324-334.
27. Willems A, et al. (2010) Selective ablation of the androgen receptor in mouse Sertoli cells affects Sertoli cell maturation, barrier formation and cytoskeletal development. PLoS One 5(11):e14168.
28. Brancati F, et al. (2010) Mutations in PVRL4, encoding cell adhesion molecule nectin-4, cause ectodermal dysplasia-syndactyly syndrome. Am J Hum Genet 87(2):265-273.
29. Shapiro IM, et al. (2011) An EMT-driven alternative splicing program occurs in human breast cancer and modulates cellular phenotype. PLoS Genet 7(8):e1002218.
30. Faucheux C, et al. (2010) Vestigial like gene family expression in Xenopus: Common and divergent features with other vertebrates. Int J Dev Biol 54(8-9):1375-1382.
31. Cohen I, et al. (2012) ZNF750 is expressed in differentiated keratinocytes and regulates epidermal late differentiation genes. PLoS One 7(8):e42628.
32. Francis SM, et al. (2009) Expression profiling identifies genes involved in emphysema severity. Respir Res 10:81.
33. Singer S, et al. (2009) Coordinated expression of stathmin family members by far upstream sequence element-binding protein-1 increases motility in non-small cell lung cancer. Cancer Res 69(6):2234-2243.
34. Fulcher ML, Gabriel S, Burns KA, Yankaskas JR, Randell SH (2005) Well-differentiated human airway epithelial cell cultures. Methods Mol Med 107:183-206.
35. Dull T, et al. (1998) A third-generation lentivirus vector with a conditional packaging system. J Virol 72:8463-8471.
36. Rock JR, et al. (2011) Notch-dependent differentiation of adult airway basal stem cells. Cell Stem Cell 8(6):639-648.
37. Gertz J, et al. (2012) Transposase mediated construction of RNA-seq libraries. Genome Res 22(1):134-141.
38. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11(10):R106.
39. Beissbarth T, Speed TP (2004) GOstat: Find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics 20(9):1464-1465.
40. Johnson DS, Mortazavi A, Myers RM, Wold B (2007) Genome-wide mapping of in vivo protein-DNA interactions. Science 316(5830):1497-1502.
41. Reddy TE, et al. (2012) Effects of sequence variation on differential allelic transcription factor occupancy and gene expression. Genome Res 22(5):860-869.
42. Zhang Y, et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9(9): R137.
43. Li Q, Brown JB, Huang HH, Bickel PJ (2011) Measuring reproducibility of highthroughput experiments. Ann Appl Stat 5(3):1752-1779.
44. Landt SG, et al. (2012) ChIP-seq guidelines and practices of the ENCODE and mod- ENCODE consortia. Genome Res 22(9):1813-1831.
45. Ashburner M, et al.; The Gene Ontology Consortium (2000) Gene Ontology: Tool for the unification of biology. Nat Genet 25(1):25-29.
46. Falcon S, Gentleman R (2007) Using GOstats to test gene lists for GO term association. Bioinformatics 23(2):257-258.
47. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Delta Delta c(T)) Method. Methods 25(4):402-408.