Airway progenitor clone formation is enhanced by Y-27632-dependent changes in the transcriptome

American Journal of Respiratory Cell and Molecular Biology

Volumn 55, Issue 3, 2016, Pages 323-336

  Reynolds, Susan D ^a   Rios, Cydney ^b   Wesolowska Andersen, Agata ^b   Zhuang, Yongbin ^b   Pinter, Mary ^b   Happoldt, Carrie ^b   Hill, Cynthia L ^a   Lallier, Scott W ^a   Cosgrove, Gregory P ^b,c   Solomon, George M ^d   Nichols, David P ^b,c   Seibold, Max A ^b,c  

^a NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b DEPARTMENT OF MEDICINE   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d University of Alabama at Birmingham   (United States)

Author keywords

Airway stem progenitor; Clone forming cell frequency; Conditionally reprogrammed cells; Y 27632

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ADAM PROTEIN; ADAMTS1 PROTEIN; CHEMOKINE RECEPTOR CXCR; CHEMOKINE RECEPTOR CXCR1; CXCL16 CHEMOKINE; CXCL3 CHEMOKINE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; FORKHEAD BOX J1; FORKHEAD TRANSCRIPTION FACTOR; GELATINASE A; GELATINASE B; GRANULOCYTE CHEMOTACTIC PROTEIN 2; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 15; INTERLEUKIN 32; INTERLEUKIN 33; INTERLEUKIN 6 RECEPTOR; INTERLEUKIN 7 RECEPTOR; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 28; MUCIN 5AC; MUCIN 5B; NERVE CELL ADHESION MOLECULE; PROTEINASE; THROMBOSPONDIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; AMIDE; CULTURE MEDIUM; PYRIDINE DERIVATIVE;

3T3 CELL LINE; AIRWAY EPITHELIAL CELL; ARTICLE; BASAL CELL; CELL DIFFERENTIATION; CELL GROWTH; CELL INTERACTION; CELL JUNCTION; CELL REPROGRAMMING TECHNIQUE; CILIARY MOTILITY; CLONOGENESIS; COMPARATIVE STUDY; CONTROLLED STUDY; CULTURE MEDIUM; CYTOSKELETON; DESMOSOME; DOWN REGULATION; EXTRACELLULAR MATRIX; FIBROBLAST; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; NOSE; PROGENITOR CELL LINE; TRANSCRIPTOMICS; UPREGULATION; ANIMAL; BRONCHUS; CELL CLONE; CELL COMMUNICATION; CELL CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECTS; EPITHELIUM CELL; FOCAL ADHESION; GENE EXPRESSION REGULATION; GENETICS; LUNG; METABOLISM; MOUSE; NIH 3T3 CELL LINE; NUCLEAR REPROGRAMMING; PHARMACOLOGY; STEM CELL;

AMIDES; ANIMALS; BRONCHI; CELL COMMUNICATION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL-MATRIX JUNCTIONS; CELLULAR REPROGRAMMING; CLONE CELLS; CULTURE MEDIA; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; LUNG; MICE; NIH 3T3 CELLS; NOSE; PYRIDINES; STEM CELLS; TRANSCRIPTOME;

EID: 84988946309     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2015-0274MA     Document Type: Article

References (57)

1. Hogg JC, McDonough JE, Gosselink JV, Hayashi S. What drives the peripheral lung-remodeling process in chronic obstructive pulmonary disease? Proc Am Thorac Soc 2009;6:668-672.
2. Fields WR, Desiderio JG, Putnam KP, Bombick DW, Doolittle DJ. Quantification of changes in c-myc mRNA levels in normal human bronchial epithelial (NHBE) and lung adenocarcinoma (A549) cells following chemical treatment. Toxicol Sci 2001;63: 107-114.
3. Karp PH, Moninger TO, Weber SP, Nesselhauf TS, Launspach JL, Zabner J, Welsh MJ. An in vitro model of differentiated human airway epithelia: methods for establishing primary cultures. Methods Mol Biol 2002;188:115-137.
4. Fulcher ML, Gabriel S, Burns KA, Yankaskas JR, Randell SH. Welldifferentiated human airway epithelial cell cultures. Methods Mol Med 2005;107:183-206.
5. Wu R. Culture of normal human airway epithelial cells and measurement of mucin synthesis and secretion. Methods Mol Med 2000;44:31-39.
6. Chapman S, Liu X, Meyers C, Schlegel R, McBride AA. Human keratinocytes are efficiently immortalized by a Rho kinase inhibitor. J Clin Invest 2010;120:2619-2626.
7. Liu X, Ory V, Chapman S, Yuan H, Albanese C, Kallakury B, Timofeeva OA, Nealon C, Dakic A, Simic V, et al. ROCK inhibitor and feeder cells induce the conditional reprogramming of epithelial cells. Am J Pathol 2012;180:599-607.
8. Suprynowicz FA, Upadhyay G, Krawczyk E, Kramer SC, Hebert JD, Liu X, Yuan H, Cheluvaraju C, Clapp PW, Boucher RC Jr, et al. Conditionally reprogrammed cells represent a stem-like state of adult epithelial cells. Proc Natl Acad Sci USA 2012;109: 20035-20040.
9. Bove PF, Dang H, Cheluvaraju C, Jones LC, Liu X, O?Neal WK, Randell SH, Schlegel R, Boucher RC. Breaking the in vitro alveolar type II cell proliferation barrier while retaining ion transport properties. Am J Respir Cell Mol Biol 2014;50:767-776.
10. Horani A, Nath A, Wasserman MG, Huang T, Brody SL. Rho-associated protein kinase inhibition enhances airway epithelial basal-cell proliferation and lentivirus transduction. Am J Respir Cell Mol Biol 2013;49:341-347.
11. Fahy JV. Type 2 inflammation in asthma-present in most, absent in many. Nat Rev Immunol 2015;15:57-65.
12. Wesolowska-Andersen A, Seibold MA. Airway molecular endotypes of asthma: dissecting the heterogeneity. Curr Opin Allergy Clin Immunol 2015;15:163-168.
13. Gauthier M, Ray A, Wenzel SE. Evolving concepts of asthma. Am J Respir Crit Care Med 2015;192:660-668.
14. Harkema JR. Comparative pathology of the nasal mucosa in laboratory animals exposed to inhaled irritants. Environ Health Perspect 1990; 85:231-238.
15. Harkema JR, Carey SA, Wagner JG. The nose revisited: a brief review of the comparative structure, function, and toxicologic pathology of the nasal epithelium. Toxicol Pathol 2006;34:252-269.
16. Poole A, Urbanek C, Eng C, Schageman J, Jacobson S, O?Connor BP, Galanter JM, Gignoux CR, Roth LA, Kumar R, et al. Dissecting childhood asthma with nasal transcriptomics distinguishes subphenotypes of disease. J Allergy Clin Immunol 2014;133: 670-678.e612.
17. McDougall CM, Blaylock MG, Douglas JG, Brooker RJ, Helms PJ, Walsh GM. Nasal epithelial cells as surrogates for bronchial epithelial cells in airway inflammation studies. Am J Respir Cell Mol Biol 2008; 39:560-568.
18. Yaghi A, Zaman A, Cox G, Dolovich MB. Ciliary beating is depressed in nasal cilia from chronic obstructive pulmonary disease subjects. Respir Med 2012;106:1139-1147.
19. Clarke LA, Sousa L, Barreto C, Amaral MD. Changes in transcriptome of native nasal epithelium expressing F508del-CFTR and intersecting data from comparable studies. Respir Res 2013;14:38.
20. Sridhar S, Schembri F, Zeskind J, Shah V, Gustafson AM, Steiling K, Liu G, Dumas YM, Zhang X, Brody JS, et al. Smoking-induced gene expression changes in the bronchial airway are reflected in nasal and buccal epithelium. BMC Genomics 2008;9:259.
21. Lee J, Park S, Roh S. Y-27632, a ROCK inhibitor, delays senescence of putative murine salivary gland stem cells in culture. Arch Oral Biol 2015;60:875-882.
22. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-676.
23. Taswell C. Limiting dilution assays for the determination of immunocompetent cell frequencies. I. Data analysis. J Immunol 1981;126:1614-1619.
24. Ghosh M, Ahmad S, Jian A, Li B, Smith RW, Helm KM, Seibold MA, Groshong SD, White CW, Reynolds SD. Human tracheobronchial basal cells: normal versus remodeling/repairing phenotypes in vivo and in vitro. Am J Respir Cell Mol Biol 2013;49:1127-1134.
25. Ghosh M, Helm KM, Smith RW, Giordanengo MS, Li B, Shen H, Reynolds SD. A single cell functions as a tissue-specific stem cell and the in vitro niche-forming cell. Am J Respir Cell Mol Biol 2011;45: 459-469.
26. Ghosh M, Smith RW, Runkle CM, Hicks DA, Helm KM, Reynolds SD. Regulation of trachebronchial tissue-specific stem cell pool size. Stem Cells 2013;31:2767-2778.
27. Ahmad S, Ahmad A, Rancourt RC, Neeves KB, Loader JE, Hendry-Hofer T, Di Paola J, Reynolds SD, White CW. Tissue factor signals airway epithelial basal cell survival via coagulation and proteaseactivated receptor isoforms 1 and 2. Am J Respir Cell Mol Biol 2013; 48:94-104.
28. Krishan A. Rapid flow cytofluorometric analysis of mammalian cell cycle by propidium iodide staining. J Cell Biol 1975;66:188-193.
29. Seibold MA, Smith RW, Urbanek C, Groshong SD, Cosgrove GP, Brown KK, Schwarz MI, Schwartz DA, Reynolds SD. The idiopathic pulmonary fibrosis honeycomb cyst contains a mucocilary pseudostratified epithelium. PLoS One 2013;8:e58658.
30. Luo W, Friedman MS, Shedden K, Hankenson KD, Woolf PJ. GAGE: generally applicable gene set enrichment for pathway analysis. BMC Bioinformatics 2009;10:161.
31. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014;15: 550.
32. Hackett NR, Shaykhiev R, Walters MS, Wang R, Zwick RK, Ferris B, Witover B, Salit J, Crystal RG. The human airway epithelial basal cell transcriptome. PLoS One 2011;6:e18378.
33. Cole BB, Smith RW, Jenkins KM, Graham BB, Reynolds PR, Reynolds SD. Tracheal basal cells: a facultative progenitor cell pool. Am J Pathol 2010;177:362-376.
34. Eriksson JE, Dechat T, Grin B, Helfand B, Mendez M, Pallari HM, Goldman RD. Introducing intermediate filaments: from discovery to disease. J Clin Invest 2009;119:1763-1771.
35. Yin T, Green KJ. Regulation of desmosome assembly and adhesion. Semin Cell Dev Biol 2004;15:665-677.
36. Kojima T, Go M, Takano K, Kurose M, Ohkuni T, Koizumi J, Kamekura R, Ogasawara N, Masaki T, Fuchimoto J, et al. Regulation of tight junctions in upper airway epithelium. Biomed Res Int2013;2013: 947072.
37. Zemke AC, Snyder JC, Brockway BL, Drake JA, Reynolds SD, Kaminski N, Stripp BR. Molecular staging of epithlieial maturation using secretory cell-specific genes as markers. Am J Respir Cell Mol Biol 2009;40:340-348.
38. Georas SN, Rezaee F. Epithelial barrier function: at the front line of asthma immunology and allergic airway inflammation. J Allergy Clin Immunol 2014;134:509-520.
39. Ribeiro AS, Paredes J. P-cadherin linking breast cancer stem cells and invasion: a promising marker to identify an ?intermediate/metastable? EMT state. Front Oncol 2015;4:371.
40. Harris TJ, Tepass U. Adherens junctions: from molecules to morphogenesis. Nat Rev Mol Cell Biol 2010;11:502-514.
41. Radice GL. N-cadherin-mediated adhesion and signaling from development to disease: lessons from mice. Prog Mol Biol Transl Sci 2013;116:263-289.
42. Byers DE, Alexander-Brett J, Patel AC, Agapov E, Dang-Vu G, Jin X, Wu K, You Y, Alevy Y, Girard JP, et al. Long-term IL-33-producing epithelial progenitor cells in chronic obstructive lung disease. J Clin Invest 2013;123:3967-3982.
43. Tadokoro T, Wang Y, Barak LS, Bai Y, Randell SH, Hogan BL. IL-6/STAT3 promotes regeneration of airway ciliated cells from basal stem cells. Proc Natl Acad Sci USA 2014;111: E3641-E3649.
44. Palechor-Ceron N, Suprynowicz FA, Upadhyay G, Dakic A, Minas T, Simic V, Johnson M, Albanese C, Schlegel R, Liu X. Radiation induces diffusible feeder cell factor(s) that cooperate with ROCK inhibitor to conditionally reprogram and immortalize epithelial cells. Am J Pathol 2013;183:1862-1870.
45. Chu HW, Rios C, Huang C, Wesolowska-Andersen A, Burchard EG, O?Connor BP, Fingerlin TE, Nichols D, Reynolds SD, Seibold MA. CRISPR-Cas9-mediated gene knockout in primary human airway epithelial cells reveals a proinflammatory role for MUC18. Gene Ther 2015;22:822-829.
46. Zhang L, Valdez JM, Zhang B, Wei L, Chang J, Xin L. ROCK inhibitor Y-27632 suppresses dissociation-induced apoptosis of murine prostate stem/progenitor cells and increases their cloning efficiency. PLoS One 2011;6:e18271.
47. Terunuma A, Limgala RP, Park CJ, Choudhary I, Vogel JC. Efficient procurement of epithelial stem cells from human tissue specimens using a Rho-associated protein kinase inhibitor Y-27632. Tissue Eng Part A 2010;16:1363-1368.
48. Ishizaki T, Uehata M, Tamechika I, Keel J, Nonomura K, Maekawa M, Narumiya S. Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Mol Pharmacol 2000;57: 976-983.
49. Narumiya S, Ishizaki T, Uehata M. Use and properties of ROCKspecific inhibitor Y-27632. Methods Enzymol 2000;325: 273-284.
50. Rath N, Olson MF. Rho-associated kinases in tumorigenesis: reconsidering ROCK inhibition for cancer therapy. EMBO Rep 2012;13: 900-908.
51. Hegab AE, Ha VL, Gilbert JL, Zhang KX, Malkoski SP, Chon AT, Darmawan DO, Bisht B, Ooi AT, Pellegrini M, et al. Novel stem/progenitor cell population from murine tracheal submucosal gland ducts with multipotent regenerative potential. Stem Cells 2011; 29:1283-1293.
52. Schlake T, Schorpp M, Maul-Pavicic A, Malashenko AM, Boehm T. Forkhead/winged-helix transcription factor Whn regulates hair keratin gene expression: molecular analysis of the nude skin phenotype. Dev Dyn 2000;217:368-376.
53. Evans MJ, Cox RA, Shami SG, Wilson B, Plopper CG. The role of basal cells in attachment of columnar cells to the basal lamina of the trachea. Am J Respir Cell Mol Biol 1989;1:463-469.
54. Evans MJ, Van Winkle LS, Fanucchi MV, Plopper CG. Cellular and molecular characteristics of basal cells in airway epithelium. Exp Lung Res 2001;27:401-415.
55. Vermeer PD, Einwalter LA, Moninger TO, Rokhlina T, Kern JA, Zabner J, Welsh MJ. Segregation of receptor and ligand regulates activation of epithelial growth factor receptor. Nature 2003;422: 322-326.
56. Gilmore AP. Anoikis. Cell Death Differ 2005;12:1473-1477.
57. Kumar PA, Hu Y, Yamamoto Y, Hoe NB, Wei TS, Mu D, Sun Y, Joo LS, Dagher R, Zielonka EM, et al. Distal airway stem cells yield alveoli in vitro and during lung regeneration following H1N1 influenza infection. Cell 2011;147: 525-538.