Abrogation of Eya1/Six1 disrupts the saccular phase of lung morphogenesis and causes remodeling

Developmental Biology

Volumn 382, Issue 1, 2013, Pages 110-123

  Lu, Karol ^a   Reddy, Raghava ^a   Berika, Mohamed ^c   Warburton, David ^a,b   El Hashash, Ahmed H K ^a,b  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

Eya1; Lung development; Saccular phase; SHH; Six1

Indexed keywords

ACTIN; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ALVEOLARIZATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DISEASE SEVERITY; EMBRYO; EYA1 GENE; FEMALE; FIBROBLAST; GENE DELETION; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS; LUNG ARTERY; LUNG DEVELOPMENT; LUNG MALFORMATION; MALE; MESENCHYMAL DEVELOPMENT; MESENCHYME; MESENCHYME CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SHH GENE; SIGNAL TRANSDUCTION; SIX1 GENE; SMOOTH MUSCLE; TRANSGENIC MOUSE;

MUS;

EID: 84884411039     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.07.019     Document Type: Article

References (66)

1. Abdelhak S., Kalatzis V., Heilig R., Compain S., Samson D., Vincent C., Weil D., Cruaud C., Sahly I., Leibovici M., et al. A human homologue of the Drosophila eyes absent gene underlies branchio-oto-renal (BOR) syndrome and identifies a novel gene family. Nat. Genet. 1997, 15:157-164.
2. Ahlfeld S.K., Conway S.J. Aberrant signaling pathways of the lung mesenchyme and their contributions to the pathogenesis of bronchopulmonary dysplasia. Birth Defects Res. A Clin. Mol. Teratol. 2012, 94(1):3-15.
3. Baraldi E., Filippone M. Chronic lung disease after premature birth. New Engl. J. Med. 2007, 357:1946-1955.
4. Bassères D.S., Levantini E., Ji H., Monti S., Elf S., Dayaram T., Fenyus M., Kocher O., Golub T., Wong K., Halmos B., Tenen D.G. Respiratory failure due to differentiation arrest and expansion of alveolar cells following lung-specific loss of the transcription factor C/EBPalpha in mice. Mol. Cell. Biol. 2006, 3:1109-1123.
5. Bellusci S., Furuta Y., Rush M.G., Henderson R., Winnier G., Hogan B.L. Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 1997, 124(1):53-63.
6. 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(23):4867-4878.
7. Bolaños A.L., Milla C.M., Lira J.C., Ramírez R., Checa M., Barrera L., García-Alvarez J., Carbajal V., Becerril C., Gaxiola M., Pardo A., Selman M. Role of Sonic hedgehog in idiopathic pulmonary fibrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 2012, 303(11):L978-L990.
8. Bostrom H., Willetts K., Pekny M., Leveen P., Lindahl P., Hedstrand H., Pekna M., Hellstrom M., Gebre-Medhin S., Schalling M., Nilsson M., Kurland S., Tornell J., Heath J.K., Betsholtz C. PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 1996, 85:863-873.
9. Buller C., Xu X., Marquis V., Schwanke R., Xu P.X. Molecular effects of Eya1 domain mutations causing organ defects in BOR syndrome. Hum. Mol. Genet. 2001, 10(24):2775-2781.
10. Burri, P.H. 1985. Lung development and growth. In: Handbook of Physiology. The Respiratory System. Circulation and Nonrespiratory Functions. Bethesda, MD: American Physiological Society, section 3, vol. I, chapter 1, pp. 1-46.
11. Burri P.H. Structural aspects of prenatal and postnatal development and growth of the lung. Lung Growth and Development 1997, 1-35. Marcel Dekker, New York. J.A. McDonald (Ed.).
12. Chuang P.T., McMahon A.P. Branching morphogenesis of the lung: new molecular insights into an old problem. Trends Cell Biol. 2003, 13(2):86-91.
13. Coalson J.J. Pathology of chronic lung disease of early infancy. Chronic Lung Disease in Early Infancy 2000, 85-124. Dekker, New York. R.D. Bland, J.J. Coalson (Eds.).
14. Coalson J.J. Pathology of new bronchopulmonary dysplasia. Semin. Neonatol 2003, 8:73-81.
15. Coletta R.D., Christensen K., Reichenberger K., Lamb J., Micomonaco D., Wolf D., Müller-Tidow C., Golub T., Kawakami K., Ford H.L. The Six1 homeoprotein stimulates tumorigenesis by reactivation of cyclin A1. Proc. Nat. Acad. Sci. U.S.A. 2004, 101(17):6478-6483.
16. De Langhe S.P., Carraro G., Tefft D., Li C., Xu X., Chai Y., Minoo P., Hajihosseini M.K., Drouin J., Kaartinen V., Bellusci S. Formation and differentiation of multiple mesenchymal lineages during lung development is regulated by beta-catenin signaling. PLoS One 2008, 3(1):e1516.
17. deMello D.E., Sawyer D., Galvin N., Reid L.M. Early fetal development of lung vasculature. Am. J. Respir. Cell Mol. Biol. 1997, 16:568-581.
18. Dishop M.K. Paediatric interstitial lung disease: classification and definitions. Paediatr. Respir. Rev. 2011, 12(4):230-237.
19. El-Hashash A.H., Al Alam D., Turcatel G., Bellusci S., Warburton D. Eyes absent 1 (Eya1) is a critical coordinator of epithelial, mesenchymal and vascular morphogenesis in the mammalian lung. Dev. Biol. 2011, 350(1):112-126.
20. El-Hashash A.H., Al Alam D., Turcatel G., Rogers O., Li X., Bellusci S., Warburton D. Six1 transcription factor is critical for coordination of epithelial, mesenchymal and vascular morphogenesis in the mammalian lung. Dev. Biol. 2011, 353(2):242-258.
21. El-Hashash A.H., Esbrit P., Kimber S.J. PTHrP promotes murine secondary trophoblast giant cell differentiation through induction of endocycle, upregulation of giant-cell-promoting transcription factors and suppression of other trophoblast cell types. Differentiation 2005, 73:154-174.
22. El-Hashash A.H., Turcatel G., Al Alam D., Buckley S., Tokumitsu H., Bellusci S., Warburton D. Eya1 controls cell polarity, spindle orientation, cell fate and Notch signaling in distal embryonic lung epithelium. Development 2011, 138(7):1395-1407.
23. El-Hashash A.H., Turcatel G., Varma S., Berika M., Al Alam D., Warburton D. Eya1 protein phosphatase regulates tight junction formation in lung distal epithelium. J. Cell Sci. 2012, 125(17):4036-4048.
24. Ford H.L., Kabingu E.N., Bump E., Mutter G., Pardee A.B. Abrogation of the G2 cell cycle checkpoint associated with overexpression of HSIX1: a possible mechanism of breast carcinogenesis. Proc. Nat. Acad. Sci. U.S.A. 1998, 95(21):12608-12613.
25. Fougerousse F., Durand M., Lopez S., Suel L., Demignon J., Thornton C., Ozaki H., Kawakami K., Barbet P., Beckmann J., Maire P. Six and Eya expression during human somitogenesis and MyoD gene family activation. J. Muscle Res. Cell Motil. 2002, 23:255-264.
26. Gauldie J., Sime P., Xing Z., Marr B., Tremblay G. Transforming growth factor beta gene transfer to the lung induces myofibroblast presence and pulmonary fibrosis. Curr. Top. Pathol. 1999, 93:35-45.
27. Handrigan G.R., Richman J.M. Autocrine and paracrine Shh signaling are necessary for tooth morphogenesis, but not tooth replacement in snakes and lizards (Squamata). Dev. Biol. 2010, 337:171-186.
28. Jobe A.J. The new BPD: an arrest of lung development. Pediatr. Res. 1999, 46:641-643.
29. Kapanchi Y., Gabbiani G. Contractile cells in pulmonary alveolar tissue. The Lung: Scientific Foundations 1997, 697-707. Lippincott-Raven Publishers, Philadelphia. R.G. Crystal, J.B. West, E.R. Weibel, P.J. Barnes (Eds.).
30. McGlinn E., Tabin C.J. Mechanistic insight into how Shh patterns the vertebrate limb. Curr. Opin. Genet. Dev. 2006, 16:426-432.
31. Mushaben E.M., Hershey G.K., Pauciulo M.W., Nichols W.C., Le Cras T.D. Chronic allergic inflammation causes vascular remodeling and pulmonary hypertension in Bmpr2 hypomorph and wild-type mice. PLoS One 2012, 7(3):e32468.
32. Kumar J.P. The sine oculis homeobox (SIX) family of transcription factors as regulators of development and disease. Cell. Mol. Life Sci. 2009, 66:565-583.
33. Laclef C., Hamard G., Demignon J., Souil E., Houbron C., Maire P. Altered myogenesis in Six1-deficient mice. Development 2003, 130(10):2239-2252.
34. Laclef C., Souil E., Demignon J., Maire P. Thymus, kidney and craniofacial abnormalities in Six1-deficient mice. Mech. Dev. 2003, 120:669-679.
35. Li X., Oghi K., Zhang J., Krones A., Bush K., Glass C., Nigam S., Aggarwal A., Maas R., Rose D., Rosenfeld M.G. Eya protein phosphatase activity regulates Six1-Dach-Eya transcriptional effects in mammalian organogenesis. Nature 2003, 426(6964):238-239.
36. Lin X., Sime P.J., Xu H., Williams M.A., LaRussa L., Georas S.N., Guo J. Yin yang 1 is a novel regulator of pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 2011, 183(12):1689-1697.
37. Mariani T.J., Reed J.J., Shapiro S.D. Expression profiling of the developing mouse lung: insights into the establishment of the extracellular matrix. Am. J. Respir. Cell Mol. Biol. 2002, 26:541-548.
38. McGowan S.E., Torday J.S. The pulmonary lipofibroblast (lipid interstitial cell) and its contributions to alveolar development. Annu. Rev. Physiol. 1997, 59:43-62.
39. Neptune E.R., Frischmeyer P.A., Arking D.E., Myers L., Bunton T.E., Gayraud B., Ramirez F., Sakai L.Y., Dietz H.C. Dysregulation of TGF-beta activation contributes to pathogenesis in Marfan syndrome. Nat. Genet. 2003, 33:407-411.
40. Nie X., Sun J., Gordon R.E., Cai C.L., Xu P.X. SIX1 acts synergistically with TBX18 in mediating ureteral smooth muscle formation. Development 2010, 137(5):755-765. (Epub 2010 Jan 28). 10.1242/dev.045757.
41. Partanen J., Puri M.C., Schwartz L., Fischer K.D., Bernstein A., Rossant J. Cell autonomous functions of the receptor tyrosine kinase TIE in a late phase of angiogenic capillary growth and endothelial cell survival during murine development. Development 1996, 122:3013-3021.
42. Pepicelli C.V., Lewis P.M., McMahon A.P. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr. Biol. 1998, 8:1083-1086.
43. Perl A.K., Wert S.E., Nagy A., Lobe C.G., Whitsett J.A. Early restriction of peripheral and proximal cell lineages during formation of the lung. Proc. Nat. Acad. Sci. U.S.A. 2002, 99:10482-10487.
44. Plumb D.J., Dubaybo B.A., Thet L.A. Changes in lung tissue fibronectin content and synthesis during postnatal lung growth. Pediatr. Pulmonol. 1987, 3:413-419.
45. Rubin L.P., Kovacs C.S., De Paepe M.E., Tsai S.W., Torday J.S., Kronenberg H.M. Arrested pulmonary alveolar cytodifferentiation and defective surfactant synthesis in mice missing the gene for parathyroid hormone-related protein. Dev. Dyn. 2004, 230(2):278-289.
46. Ruf R.G., Xu P.X., Silvius D., Otto E.A., Beekmann F., Muerb U.T., Kumar S., Neuhaus T.J., Kemper M.J., Raymond R.M., et al. SIX1 mutations cause branchio-oto renal syndrome by disruption of EYA1-SIX1-DNA complexes. Proc. Nat. Acad. Sci. U.S.A. 2004, 101(21):8090-8095.
47. Schlosser G., Awtry T., Brugmann S., Jensen E., Neilson K., Ruan G., Stammler A., Voelker D., Yan B., Zhang C., et al. Eya1 and Six1 promote neurogenesis in the cranial placodes in a SoxB1-dependent fashion. Dev. Biol. 2008, 320(1):199-214.
48. Shannon J.M., Hyatt B.A. Epithelial mesenchymal interactions in the developing lung. Annu. Rev. Physiol. 2004, 66:625-645.
49. Sime P.J., Xing Z., Graham F., Csaky K., 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.
50. Shu W., Lu M., Zhang Y., Tucker P., Zhou D., Morrisey E.E. Foxp2 and Foxp1 cooperatively regulate lung and esophagus development. Development 2007, 134:1991-2000.
51. Tefft D., Lee M., Smith S., Crowe D.L., Bellusci S., Warburton D. mSprouty2 inhibits FGF10-activated MAP kinase by differentially binding to upstream target proteins. Am. J. Physiol. Cell Physiol. 2002, 283:L700-L706.
52. Thibeault D.W., Mabry S.M., Ekekezie I.I., Truog W.E. Lung elastic tissue maturation and perturbations during the evolution of chronic lung disease. Pediatrics 2000, 106:1452-1459.
53. Thibeault D.W., Mabry S.M., Ekekezie I.I., Zhang X., Truog W.E. Collagen scaffolding during development and its deformation with chronic lung disease. Pediatrics 2003, 111:766-776.
54. Thurlbeck W.M. Measurement of pulmonary emphysema. Am. Rev. Respir. Dis. 1967, 95:752-764.
55. Vicencio A.F., Lee C., Cho S., Eickelberg O., Chuu Y., Haddad G., Elias J.A. Conditional overexpression of bioactive transforming growth factor-_1 in neonatal mouse lung: a new model for bronchopulmonary dysplasia?. Am. J. Respir. Cell Mol. Biol. 2004, 31:650-656.
56. Warburton D., El-Hashash A.H., Carraro G., Tiozzo C., Sala F., Rogers O., De Langhe S., Kemp P.J., Riccardi D., Torday J., Bellusci S., Shi W., Lubkin S.R., Jesudason E. Lung organogenesis. Curr. Top. Dev. Biol. 2010, 90:73-158.
57. Weaver M., Batts L., Hogan B.L. Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev. Biol. 2003, 258:169-184.
58. Xiong W., Dabbouseh N., Rebay I. Interactions with the Abelson tyrosine kinase reveal compartmentalization of eyes absent function between nucleus and cytoplasm. Dev. Cell 2009, 16:271-279.
59. Xu P.X., Adams J., Peters H., Brown M., Heaney S., Maas R. Eya1-deficient mice lack ears and kidneys and show abnormal apoptosis of organ primordia. Nat. Genet. 1999, 23:113-117.
60. Xu P.X., Cheng J., Epstein J., Maas R.L. Mouse Eya genes are expressed during limb tendon development and encode a transcriptional activation function. Proc. Nat. Acad. Sci. U.S.A. 1997, 94:11974-11979.
61. Xu P.X., Woo I., Her H., Beier D., Maas R.L. Mouse Eya homologues of the Drosophilia eyes absent gene require Pax6 for expression in lens and nasal placode. Development 1997, 124(1):219-231.
62. Xu P.X., Zheng W., Laclef C., Maire P., Maas R.L., Peters H., Xu X. Eya1 is required for the morphogenesis of mammalian thymus, parathyroid and thyroid. Development 2002, 129:3033-3044.
63. Yang L., Wang Y., Mao H., Fleig S., Omenetti A., Brown K.D., Sicklick J.K., Li Y.X., Diehl A.M. Sonic hedgehog is an autocrine viability factor for myofibroblastic hepatic stellate cells. J. Hepatol. 2008, 48:98-106.
64. Yao H.H., Whoriskey W., Capel B. Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev. 2002, 16:1433-1440.
65. Zheng W., Huang L., Wei Z., Silvius D., Tang B., Xu P.X. The role of Six1 in mammalian auditory system development. Development 2003, 130(17):3989-4000.
66. Zou D., Silvius D., Fritzsch B., Xu P.X. Eya1 and Six1 are essential for early steps of sensory neurogenesis in mammalian cranial placodes. Development 2004, 131(22):5561-5572.