TGF-β signaling in stromal cells acts upstream of FGF-10 to regulate epithelial stem cell growth in the adult lung

Stem Cell Research

Volumn 11, Issue 3, 2013, Pages 1222-1233

  McQualter, Jonathan L ^a   McCarty, Rosa C ^a   Van der Velden, Joanne ^a   O'Donoghue, Robert J J ^a,b   Asselin Labat, Marie Liesse ^a,b   Bozinovski, Steven ^a   Bertoncello, Ivan ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; EPITHELIAL CELL ADHESION MOLECULE; FIBROBLAST GROWTH FACTOR 10; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIZATION; EX VIVO STUDY; FEMALE; GENE ACTIVATION; GENE EXPRESSION; INTRACELLULAR SIGNALING; LUNG ALVEOLUS CELL; MESENCHYMAL STROMA CELL; MICROENVIRONMENT; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; STEM CELL; STEM CELL CULTURE; UPREGULATION;

CFU-EPI; CFU-F; COLONY-FORMING UNIT-EPITHELIAL; COLONY-FORMING UNIT-FIBROBLAST; EPISPC; EPITHELIAL STEM/PROGENITOR CELL; MESENCHYMAL STROMAL CELL; MSC;

ACTIVATED-LEUKOCYTE CELL ADHESION MOLECULE; ANIMALS; BENZAMIDES; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELLS, CULTURED; DIOXOLES; EPITHELIAL CELLS; FEMALE; FIBROBLAST GROWTH FACTOR 10; LUNG; MICE; MICE, INBRED C57BL; MYOFIBROBLASTS; SIGNAL TRANSDUCTION; STEM CELLS; STROMAL CELLS; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 84883816017     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2013.08.007     Document Type: Article

References (51)

1. Nyeng P., Norgaard G.A., Kobberup S., Jensen J. FGF10 maintains distal lung bud epithelium and excessive signaling leads to progenitor state arrest, distalization, and goblet cell metaplasia. BMC Dev. Biol. 2008, 8:2.
2. Shannon J.M., Nielsen L.D., Gebb S.A., Randell S.H. Mesenchyme specifies epithelial differentiation in reciprocal recombinants of embryonic lung and trachea. Dev. Dyn. 1998, 212:482-494.
3. El Agha E., Al Alam D., Carraro G., MacKenzie B., Goth K., De Langhe S.P., Voswinckel R., Hajihosseini M.K., Rehan V.K., Bellusci S. Characterization of a novel fibroblast growth factor 10 (Fgf10) knock-in mouse line to target mesenchymal progenitors during embryonic development. PLoS One 2012, 7:e38452.
4. Warburton D., Berberich M.A., Driscoll B. Stem/progenitor cells in lung morphogenesis, repair, and regeneration. Curr. Top. Dev. Biol. 2004, 64:1-16.
5. Holgate S.T., Davies D.E., Lackie P.M., Wilson S.J., Puddicombe S.M., Lordan J.L. Epithelial-mesenchymal interactions in the pathogenesis of asthma. J. Allergy Clin. Immunol. 2000, 105:193-204.
6. Volckaert T., Dill E., Campbell A., Tiozzo C., Majka S., Bellusci S., De Langhe S.P. Parabronchial smooth muscle constitutes an airway epithelial stem cell niche in the mouse lung after injury. J. Clin. Invest. 2011, 121:4409-4419.
7. McQualter J.L., Yuen K., Williams B., Bertoncello I. Evidence of an epithelial stem/progenitor cell hierarchy in the adult mouse lung. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:1414-1419.
8. Teisanu R.M., Chen H., Matsumoto K., McQualter J.L., Potts E., Foster W.M., Bertoncello I., Stripp B.R. Functional analysis of two distinct bronchiolar progenitors during lung injury and repair. Am. J. Respir. Cell Mol. Biol. 2011, 44:794-803.
9. McQualter J.L., Brouard N., Williams B., Baird B.N., Sims-Lucas S., Yuen K., Nilsson S.K., Simmons P.J., Bertoncello I. Endogenous fibroblastic progenitor cells in the adult mouse lung are highly enriched in the sca-1 positive cell fraction. Stem Cells 2009, 27:623-633.
10. Summer R., Fitzsimmons K., Dwyer D., Murphy J., Fine A. Isolation of an adult mouse lung mesenchymal progenitor cell population. Am. J. Respir. Cell Mol. Biol. 2007, 37:152-159.
11. Martin J., Helm K., Ruegg P., Varella-Garcia M., Burnham E., Majka S. Adult lung side population cells have mesenchymal stem cell potential. Cytotherapy 2008, 10:140-151.
12. Giangreco A., Shen H., Reynolds S.D., Stripp B.R. Molecular phenotype of airway side population cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2004, 286:L624-L630.
13. Hennrick K.T., Keeton A.G., Nanua S., Kijek T.G., Goldsmith A.M., Sajjan U.S., Bentley J.K., Lama V.N., Moore B.B., Schumacher R.E., Thannickal V.J., Hershenson M.B. Lung cells from neonates show a mesenchymal stem cell phenotype. Am. J. Respir. Crit. Care 2007, 175:1158-1164.
14. McCarty R.C., Gronthos S., Zannettino A.C., Foster B.K., Xian C.J. Characterisation and developmental potential of ovine bone marrow derived mesenchymal stem cells. J. Cell. Physiol. 2009, 219:324-333.
15. Ritchie M.E., Silver J., Oshlack A., Holmes M., Diyagama D., Holloway A., Smyth G.K. A comparison of background correction methods for two-colour microarrays. Bioinformatics 2007, 23:2700-2707.
16. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
17. Huang da W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37:1-13.
18. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., Deans R., Keating A., Prockop D., Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
19. Varisco B.M., Ambalavanan N., Whitsett J.A., Hagood J.S. Thy-1 signals through PPARgamma to promote lipofibroblast differentiation in the developing lung. Am. J. Respir. Cell Mol. Biol. 2012, 46:765-772.
20. Hinz B., Phan S.H., Thannickal V.J., Galli A., Bochaton-Piallat M.L., Gabbiani G. The myofibroblast: one function, multiple origins. Am. J. Pathol. 2007, 170:1807-1816.
21. Hinz B., Phan S.H., Thannickal V.J., Prunotto M., Desmouliere A., Varga J., De Wever O., Mareel M., Gabbiani G. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am. J. Pathol. 2012, 180:1340-1355.
22. Inman G.J., Nicolas F.J., Callahan J.F., Harling J.D., Gaster L.M., Reith A.D., Laping N.J., Hill C.S. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 2002, 62:65-74.
23. Battula V.L., Treml S., Bareiss P.M., Gieseke F., Roelofs H., de Zwart P., Muller I., Schewe B., Skutella T., Fibbe W.E., Kanz L., Buhring H.J. Isolation of functionally distinct mesenchymal stem cell subsets using antibodies against CD56, CD271, and mesenchymal stem cell antigen-1. Haematologica Hematol. J. 2009, 94:173-184.
24. Buhring H.J., Treml S., Cerabona F., de Zwart P., Kanz L., Sobiesiak M. Phenotypic characterization of distinct human bone marrow-derived MSC subsets. Ann. N. Y. Acad. Sci. 2009, 1176:124-134.
25. Duffield J.S., Lupher M., Thannickal V.J., Wynn T.A. Host responses in tissue repair and fibrosis. Annu. Rev. Pathol. 2013, 8:241-276.
26. Scotton C.J., Chambers R.C. Molecular targets in pulmonary fibrosis: the myofibroblast in focus. Chest 2007, 132:1311-1321.
27. Willis B.C., Borok Z. TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 293:L525-L534.
28. Lama V.N., Smith L., Badri L., Flint A., Andrei A.C., Murray S., Wang Z., Liao H., Toews G.B., Krebsbach P.H., Peters-Golden M., Pinsky D.J., Martinez F.J., Thannickal V.J. Evidence for tissue-resident mesenchymal stem cells in human adult lung from studies of transplanted allografts. J. Clin. Invest. 2007, 117:989-996.
29. Mailleux A.A., Kelly R., Veltmaat J.M., De Langhe S.P., Zaffran S., Thiery J.P., Bellusci S. Fgf10 expression identifies parabronchial smooth muscle cell progenitors and is required for their entry into the smooth muscle cell lineage. Development 2005, 132:2157-2166.
30. Rock J.R., Barkauskas C.E., Cronce M.J., Xue Y., Harris J.R., Liang J., Noble P.W., Hogan B.L. Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:E1475-E1483.
31. Shan L., Subramaniam M., Emanuel R.L., Degan S., Johnston P., Tefft D., Warburton D., Sunday M.E. Centrifugal migration of mesenchymal cells in embryonic lung. Dev. Dyn. 2008, 237:750-757.
32. Walker N., Badri L., Wettlaufer S., Flint A., Sajjan U., Krebsbach P.H., Keshamouni V.G., Peters-Golden M., Lama V.N. Resident tissue-specific mesenchymal progenitor cells contribute to fibrogenesis in human lung allografts. Am. J. Pathol. 2011, 178:2461-2469.
33. Desmouliere A., Geinoz A., Gabbiani F., Gabbiani G. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J. Cell Biol. 1993, 122:103-111.
34. Sime P.J., Xing Z., Graham F.L., Csaky K.G., Gauldie J. Adenovector-mediated gene transfer of active transforming growth factor-beta1 induces prolonged severe fibrosis in rat lung. J. Clin. Invest. 1997, 100:768-776.
35. Thannickal V.J., Lee D.Y., White E.S., Cui Z., Larios J.M., Chacon R., Horowitz J.C., Day R.M., Thomas P.E. Myofibroblast differentiation by transforming growth factor-beta1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J. Biol. Chem. 2003, 278:12384-12389.
36. Gu L., Zhu Y.J., Yang X., Guo Z.J., Xu W.B., Tian X.L. Effect of TGF-beta/Smad signaling pathway on lung myofibroblast differentiation. Acta Pharmacol. Sin. 2007, 28:382-391.
37. Horowitz J.C., Rogers D.S., Sharma V., Vittal R., White E.S., Cui Z., Thannickal V.J. Combinatorial activation of FAK and AKT by transforming growth factor-beta1 confers an anoikis-resistant phenotype to myofibroblasts. Cell. Signal. 2007, 19:761-771.
38. Gauldie J., Kolb M., Ask K., Martin G., Bonniaud P., Warburton D. Smad3 signaling involved in pulmonary fibrosis and emphysema. Proc. Am. Thorac. Soc. 2006, 3:696-702.
39. Sekine K., Ohuchi H., Fujiwara M., Yamasaki M., Yoshizawa T., Sato T., Yagishita N., Matsui D., Koga Y., Itoh N., Kato S. Fgf10 is essential for limb and lung formation. Nat. Genet. 1999, 21:138-141.
40. Min H.S., Danilenko D.M., Scully S.A., Bolon B., Ring B.D., Tarpley J.E., DeRose M., Simonet W.S. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev. 1998, 12:3156-3161.
41. Park W.Y., Miranda B., Lebeche D., Hashimoto G., Cardoso W.V. FGF-10 is a chemotactic factor for distal epithelial buds during lung development. Dev. Biol. 1998, 201:125-134.
42. Bellusci S., Grindley J., Emoto H., Itoh N., Hogan B.L. Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 1997, 124:4867-4878.
43. Weng T., Chen Z., Jin N., Gao L., Liu L. Gene expression profiling identifies regulatory pathways involved in the late stage of rat fetal lung development. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 291:L1027-L1037.
44. Weng T., Gao L., Bhaskaran M., Guo Y., Gou D., Narayanaperumal J., Chintagari N.R., Zhang K., Liu L. Pleiotrophin regulates lung epithelial cell proliferation and differentiation during fetal lung development via beta-catenin and Dlk1. J. Biol. Chem. 2009, 284:28021-28032.
45. Reynolds P.R., Mucenski M.L., Le Cras T.D., Nichols W.C., Whitsett J.A. Midkine is regulated by hypoxia and causes pulmonary vascular remodeling. J. Biol. Chem. 2004, 279:37124-37132.
46. Reynolds P.R., Mucenski M.L., Whitsett J.A. Thyroid transcription factor (TTF) -1 regulates the expression of midkine (MK) during lung morphogenesis. Dev. Dyn. 2003, 227:227-237.
47. Visscher D.W., Myers J.L. Histologic spectrum of idiopathic interstitial pneumonias. Proc. Am. Thorac. Soc. 2006, 3:322-329.
48. Misumi S., Lynch D.A. Idiopathic pulmonary fibrosis/usual interstitial pneumonia: imaging diagnosis, spectrum of abnormalities, and temporal progression. Proc. Am. Thorac. Soc. 2006, 3:307-314.
49. Qunn L., Takemura T., Ikushima S., Ando T., Yanagawa T., Akiyama O., Oritsu M., Tanaka N., Kuroki T. Hyperplastic epithelial foci in honeycomb lesions in idiopathic pulmonary fibrosis. Virchows Arch. 2002, 441:271-278.
50. Kuhn C., Boldt J., King T.E., Crouch E., Vartio T., McDonald J.A. An immunohistochemical study of architectural remodeling and connective tissue synthesis in pulmonary fibrosis. Am. Rev. Respir. Dis. 1989, 140:1693-1703.
51. Kuhn C., McDonald J.A. The roles of the myofibroblast in idiopathic pulmonary fibrosis. Ultrastructural and immunohistochemical features of sites of active extracellular matrix synthesis. Am. J. Pathol. 1991, 138:1257-1265.