Fetal and postnatal lung defects reveal a novel and required role for Fgf8 in lung development

Developmental Biology

Volumn 347, Issue 1, 2010, Pages 92-108

  Yu, Shibin ^a   Poe, Bryan ^a   Schwarz, Margaret ^b   Elliot, Sarah A ^a   Albertine, Kurt H ^a   Fenton, Stephen ^a   Garg, Vidu ^b   Moon, Anne M ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Alveologenesis; Differentiation; FGF; Lung development; Mouse model; Proliferation; Pulmonary vascular development; Type I alveolar cell; Type II alveolar cell

Indexed keywords

FIBROBLAST GROWTH FACTOR 8;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRANCHING MORPHOGENESIS; CELL DIFFERENTIATION; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DEVELOPMENTAL STAGE; EMBRYO; FETUS; FETUS DEVELOPMENT; FETUS DISEASE; GENE FUNCTION; LUNG ALVEOLUS EPITHELIUM; LUNG DEVELOPMENT; LUNG DISEASE; LUNG DYSPLASIA; MESENCHYME; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POSTNATAL DEVELOPMENT; PREMATURITY; PRIORITY JOURNAL; RESPIRATORY FAILURE; TISSUE DIFFERENTIATION;

VERTEBRATA;

EID: 77957320930     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.08.013     Document Type: Article

References (98)

1. Abler L.L., Mansour S.L., Sun X. Conditional gene inactivation reveals roles for Fgf10 and Fgfr2 in establishing a normal pattern of epithelial branching in the mouse lung. Dev. Dyn. 2009, 238:1999-2013.
2. Abu-Issa R., Smyth G., Smoak I., Yamamura K., Meyers E.N. Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 2002, 129:4613-4625.
3. Alcorn D.G., Adamson T.M., Maloney J.E., Robinson P.M. A morphologic and morphometric analysis of fetal lung development in the sheep. Anat. Rec. 1981, 201:655-667.
4. Aprelikova O., Wood M., Tackett S., Chandramouli G.V., Barrett J.C. Role of ETS transcription factors in the hypoxia-inducible factor-2 target gene selection. Cancer Res. 2006, 66:5641-5647.
5. Arman E., Haffner-Krausz R., Gorivodsky M., Lonai P. Fgfr2 is required for limb outgrowth and lung-branching morphogenesis. Proc. Natl Acad. Sci. USA 1999, 96:11895-11899.
6. Batchelor D.C., Hutchins A.M., Klempt M., Skinner S.J. Developmental changes in the expression patterns of IGFs, type 1 IGF receptor and IGF-binding proteins-2 and -4 in perinatal rat lung. J. Mol. Endocrinol. 1995, 15:105-115.
7. Bellusci S., Grindley J., Emoto H., Itah N., Hogan B.L. Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 1997, 124:4867-4878.
8. Bhatt A.J., Amin S.B., Chess P.R., Watkins R.H., Maniscalco W.M. Expression of vascular endothelial growth factor and Flk-1 in developing and glucocorticoid-treated mouse lung. Pediatr. Res. 2000, 47:606-613.
9. Bird A.D., Tan K.H., Olsson P.F., Zieba M., Flecknoe S.J., Liddicoat D.R., Mollard R., Hooper S.B., Cole T.J. Identification of glucocorticoid-regulated genes that control cell proliferation during murine respiratory development. J. Physiol. 2007, 585:187-201.
10. Boucherat O., Franco-Montoya M., Thibault C., Incitti R., Chailley-Heu B., Delacourt C., Bourbon J.R. Gene expression profiling in lung fibroblasts reveals new players in alveolarization. Physiol. Genomics 2007, 32:128-141.
11. Boyden E.A. The mode of origin of pulmonary acini and respiratory bronchioles in the fetal lung. Am. J. Anat. 1974, 141:317-328.
12. Brent A.E., Tabin C.J. FGF acts directly on the somitic tendon progenitors through the Ets transcription factors Pea3 and Erm to regulate scleraxis expression. Development 2004, 131:3885-3896.
13. Bruce M.C., Honaker C.E., Cross R.J. Lung fibroblasts undergo apoptopsis following alveolarization. Am. J. Respir. Cell Mol. Biol. 1999, 20:228-236.
14. Burri P.H. Structural aspects of prenatal and postnatal development and growth of the lung. Lung Growth and Development 1997, 1-35. Marcel Dekker, Inc, New York. J.A. McDonald (Ed.).
15. Cardoso W.V. Molecular regulation of lung development. Annu. Rev. Physiol. 2001, 63:471-494.
16. Carmeliet P., Ferreira V., Breier G., Pollefeyt S., Kieckens L., Gertsenstein M., Fahrig M., Vandenhoeck A., Harpal K., Eberhardt C., Declercq C., Pawling J., Moons L., Collen D., Risau W., Nagy A. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996, 380:435-439.
17. Celli G., LaRochelle W.J., Mackem S., Sharp R., Merlino G. Soluble dominant-negative receptor uncovers essential roles for fibroblast growth factors in multi-organ induction and patterning. EMBO J. 1998, 17:1642-1655.
18. Cole T.J., Blendy J.A., Monaghan A.P., Krieglstein K., Schmid W., Aguzzi A., Fantuzzi G., Hummler E., Unsicker K., Schutz G. Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev. 1995, 9:1608-1621.
19. Cole T.J., Solomon N.M., Van Driel R., Monk J.A., Bird D., Richardson S.J., Dilley R.J., Hooper S.B. Altered epithelial cell proportions in the fetal lung of glucocorticoid receptor null mice. Am. J. Respir. Cell Mol. Biol. 2004, 30:613-619.
20. Colvin J.S., Feldman B., Nadeau J.H., Goldfarb M., Ornitz D.M. Genomic organization and embryonic expression of the mouse fibroblast growth factor 9 gene. Dev. Dyn. 1999, 216:72-88.
21. Colvin J.S., White A.C., Pratt S.J., Ornitz D.M. Lung hypoplasia and neonatal death in Fgf9-null mice identify this gene as an essential regulator of lung mesenchyme. Development 2001, 128:2095-2106.
22. Crawford H.C., Fingleton B., Gustavson M.D., Kurpios N., Wagenaar R.A., Hassell J.A., Matrisian L.M. The PEA3 subfamily of Ets transcription factors synergizes with beta-catenin-LEF-1 to activate matrilysin transcription in intestinal tumors. Mol. Cell. Biol. 2001, 21:1370-1383.
23. Crawford H.C., Matrisian L.M. Mechanisms controlling the transcription of matrix metalloproteinase genes in normal and neoplastic cells. Enzyme Protein 1996, 49:20-37.
24. Curtis R.K., Oresic M., Vidal-Puig A. Pathways to the analysis of microarray data. Trends Biotechnol. 2005, 23:429-435.
25. Davies G., Reid L. Growth of the alveoli and pulmonary arteries in childhood. Thorax 1970, 25:669-681.
26. Davies P., Reid L., Lister G., Pitt B. Postnatal growth of the sheep lung: a morphometric study. Anat. Rec. 1988, 220:281-286.
27. De Moerlooze L., Spencer-Dene B., Revest J., Hajihosseini M., Rosewell I., Dickson C. An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 2000, 127:483-492.
28. DeLisser H.M., Helmke B.P., Cao G., Egan P.M., Taichman D., Fehrenbach M., Zaman A., Cui Z., Mohan G.S., Baldwin H.S., Davies P.F., Savani R.C. Loss of PECAM-1 function impairs alveolarization. J. Biol. Chem. 2006, 281:8724-8731.
29. Deng C.X., Wynshaw-Boris A., Shen M.M., Daugherty C., Ornitz D.M., Leder P. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 1994, 8:p3045-p3057.
30. Docimo S.G., Crone R.K., Davies P., Reid L., Retik A.B., Mandell J. Pulmonary development in the fetal lamb: quantitative histologic study of the alveolar phase. Anat. Rec. 1991, 229:495-498.
31. Dunnill M.S. Postnatal growth of the lung. Thorax 1962, 17:329-333.
32. Emery J.L., Wilcock P.F. The postnatal development of the lung. Acta Anat. 1966, 65:10-29.
33. Firnberg N., Neubuser A. FGF signaling regulates expression of Tbx2, Erm, Pea3, and Pax3 in the early nasal region. Dev. Biol. 2002, 247:237-250.
34. Frank D.U., Fotheringham L.K., Brewer J.A., Muglia L.J., Tristani-Firouzi M., Capecchi M.R., Moon A.M. An Fgf8 mouse mutant phenocopies human 22q11 deletion syndrome. Development 2002, 129:4591-4603.
35. Galambos C., Ng Y.-S., Ali A., Nogushi A., Lovejoy S., D'Amore P.A., deMello D.E. Defective pulmonary development in the absence of heparin-binding vascular endothelial growth factor isoforms. Am. J. Respir. Cell Mol. Biol. 2002, 27:194-203.
36. Guo L., Degenstein L., Fuchs E. Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev. 1996, 10:165-175.
37. Hokuto I., Perl A.K., Whitsett J.A. Prenatal, but not postnatal, inhibition of fibroblast growth factor receptor signaling causes emphysema. J. Biol. Chem. 2003, 278:415-421.
38. Hu M.C., Qui W.R., Wang Y.P., Hill D., Ring B.D., Scully S., Bolon B., DeRose M., Luethy R., Simonet W.S., Arakawa T., Danilenko D.M. FGF-18, a novel member of the fibroblast growth factor family, stimulates hepatic and intestinal proliferation. Mol. Cell. Biol. 1998, 18:6063-6074.
39. Ilagan R., Abu-Issa R., Brown D., Yang Y.P., Jiao K., Schwartz R.J., Klingensmith J., Meyers E.N. Fgf8 is required for anterior heart field development. Development 2006, 133:2435-2445.
40. Jones J.I., Clemmons D.R. Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 1995, 16:3-34.
41. Kimura S., Hara Y., Pineau T., Fernandez-Salguero P., Fox C.H., Ward J.M., Gonzalez F.J. The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev. 1996, 10:60-69.
42. Langston C., Kida K., Reed M., Thurlbeck W.M. Human lung growth in late gestation and in the neonate. Am. Rev. Respir. Dis. 1984, 129:607-613.
43. Lewandoski M., Sun X., Martin G.R. Fgf8 signalling from the AER is essential for normal limb development. Nat. Genet. 2000, 26:460-463.
44. Li C., Xiao J., Hormi K., Borok Z., Minoo P. Wnt5a participates in distal lung morphogenesis. Dev. Biol. 2002, 248:68-81.
45. Li C., Hu L., Xiao J., Chen H., Li J.T., Bellusci S., Delanghe S., Minoo P. Wnt5a regulates Shh and Fgf10 signaling during lung development. Dev. Biol. 2005, 287:86-97.
46. Lin W., Furthauer M., Thisse B., Thisse C., Jing N., Ang S.L. Cloning of the mouse Sef gene and comparative analysis of its expression with Fgf8 and Spry2 during embryogenesis. Mech. Dev. 2002, 113:163-168.
47. Lindahl P., Karlsson L., Hellstrom M., Gebre-Medhin S., Willetts K., Heath J.K., Betsholtz C. Alveogenesis failure in PDGF-A-deficient mice is coupled to lack of distal spreading of alveolar smooth muscle cell progenitors during lung development. Development 1997, 124:3943-3953.
48. Liu Y., Jiang H., Crawford H.C., Hogan B.L. Role for ETS domain transcription factors Pea3/Erm in mouse lung development. Dev. Biol. 2003, 261:10-24.
49. MacArthur C.A., Lawshe A., Xu J., Santos-Ocampo S., Heikinheimo M., Chellaiah A.T., Ornitz D.M. FGF-8 isoforms activate receptor splice forms that are expressed in mesenchymal regions of mouse development. Development 1995, 121:3603-3613.
50. Macatee T.L., Hammond B.P., Arenkiel B.R., Francis L., Frank D.U., Moon A.M. Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 2003, 130:6361-6374.
51. Metzger R.J., Klein O.D., Martin G.R., Krasnow M.A. The branching programme of mouse lung development. Nature 2008, 453:745-750.
52. Meyers E.N., Lewandoski M., Martin G.R. An Fgf8 allelic mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 1998, 18:136-141.
53. Min H., Danilenko D.M., Scully S.A., Bolon B., Ring B.D., Tarpley J.E., DeRose M., Simonet S.W. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev. 1998, 12:3156-3161.
54. Moon A.M. Mouse models for investigating the developmental basis of human birth defects. Pediatr. Res. 2006, 59:749-755.
55. Moon A.M., Capecchi M.R. FGF8 is required for outgrowth and patterning of the limbs. Nat. Genet. 2000, 26:455-459.
56. Moon A.M., Guris D.L., Seo J.H., Li L., Hammond J., Talbot A., Imamoto A. Crkl deficiency disrupts fgf8 signaling in a mouse model of 22q11 deletion syndromes. Dev. Cell 2006, 10:71-80.
57. Muglia L., Jacobson L., Dikkes P., Majzoub J.A. Corticotropin-releasing hormone deficiency reveals major fetal but not adult glucocorticoid need. Nature 1995, 373:427-432.
58. Muglia L.J., Bae D.S., Brown T.T., Vogt S.K., Alvarez J.G., Sunday M.E., Majzoub J.A. Proliferation and differentiation defects during lung development in corticotropin-releasing hormone-deficient mice. Am. J. Respir. Cell Mol. Biol. 1999, 20:181-188.
59. Olson E.N., Arnold H.H., Rigby P.W., Wold B.J. Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell 1996, 85:1-4.
60. Park E.J., Ogden L.A., Talbot A., Evans S., Cai C.L., Black B.L., Frank D.U., Moon A.M. Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling. Development 2006, 133:2419-2433.
61. Park M., Rieger-Fackeldey E., Schanbacher B.L., Cook A.C., Bauer J.A., Rogers L.K., Hansen T.N., Welty S.E., Smith C.V. Altered expressions of fibroblast growth factor receptors and alveolarization in neonatal mice exposed to 85% oxygen. Pediatr. Res. 2007, 62(6):652-657.
62. Park E.J., Watanabe Y., Smyth G., Miyagawa-Tomita S., Meyers E., Klingensmith J., Camenisch T., Buckingham M., Moon A.M. An FGF autocrine loop initiated in second heart field mesoderm regulates morphogenesis at the arterial pole of the heart. Development 2008, 135:3599-3610.
63. Peinado H., Moreno-Bueno G., Hardisson D., Perez-Gomez E., Santos V., Mendiola M., de Diego J.I., Nistal M., Quintanilla M., Portillo F., Cano A. Lysyl oxidase-like 2 as a new poor prognosis marker of squamous cell carcinomas. Cancer Res. 2008, 68:4541-4550.
64. 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. Natl Acad. Sci. USA 2002, 99:10482-10487.
65. Powell P.P., Wang C.C., Horinouchi H., Shepherd K., Jacobson M., Lipson M., Jones R. Differential expression of fibroblast growth factor receptors 1 to 4 and ligand genes in late fetal and early postnatal rat lung. Am. J. Respir. Cell Mol. Biol. 1998, 19:563-572.
66. Powers C.J., McLeskey S.W., Wellstein A. Fibroblast growth factors, their receptors and signaling. Endocr. Relat. Cancer 2000, 7:165-197.
67. Raible F., Brand M. Tight transcriptional control of the ETS domain factors Erm and Pea3 by Fgf signaling during early zebrafish development. Mech. Dev. 2001, 107:105-117.
68. Rajagopal J., Carroll T.J., Guseh J.S., Bores S.A., Blank L.J., Anderson W.J., Yu J., Zhou Q., McMahon A.P., Melton D.A. Wnt7b stimulates embryonic lung growth by coordinately increasing the replication of epithelium and mesenchyme. Development 2008, 135:1625-1634.
69. Roehl H., Nusslein-Volhard C. Zebrafish pea3 and erm are general targets of FGF8 signaling. Curr. Biol. 2001, 11:503-507.
70. Roman J., Schuyler W., McDonald J.A., Roser S. Heparin inhibits lung branching morphogenesis: potential role of smooth muscle cells in cleft formation. Am. J. Med. Sci. 1998, 316:368-378.
71. Saga Y., Miyagawa-Tomita S., Takagi A., Kitajima S., Miyazaki J., Inoue T. MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 1999, 126:3437-3447.
72. Salnikow K., Aprelikova O., Ivanov S., Tackett S., Kaczmarek M., Karaczyn A., Yee H., Kasprzak K.S., Niederhuber J. Regulation of hypoxia-inducible genes by ETS1 transcription factor. Carcinogenesis 2008, 29:1493-1499.
73. Sannes P.L., Burch K.K., Khosia J. Immunohistochemical localization of epidermal growth factor and acidic and basic fibroblast growth factors in postnatal developing and adult rat lung. Am. J. Respir. Cell Mol. Biol. 1992, 7:230-237.
74. Schittny J.C., Djonov V., Fine A., Burri P.H. Programmed cell death contributes to postnatal lung development. Am. J. Respir. Cell Mol. Biol. 1998, 18:786-793.
75. Schmitt J.F., Hearn M.T., Risbridger G.P. Expression of fibroblast growth factor-8 in adult rat tissues and human prostate carcinoma cells. J. Steroid Biochem. Mol. Biol. 1996, 57:173-178.
76. Schuger L., Varani J., Mitra R., Gilbride K. Retinoic acid stimulates mouse lung development by a mechanism involving epithelial-mesenchymal interaction and regulation of epidermal growth factor receptors. Dev. Biol. 1993, 159:462-473.
77. Schuller A.G., van Neck J.W., Beukenholdt R.W., Zwarthoff E.C., Drop S.L. IGF, type I IGF receptor and IGF-binding protein mRNA expression in the developing mouse lung. J. Mol. Endocrinol. 1995, 14:349-355.
78. Sekine K., Ohuchi H., Fujiwara M., Yamasaki M., Yoshizawa T., Soto 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.
79. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
80. Srisuma S., Bhattacharya S., Simon D.M., Solleti S.K., Tyagi S., Starcher B., Mariani T.J. Fibroblast growth factor receptors control epithelial-mesenchymal interactions necessary for alveolar elastogenesis. Am. J. Resp. Crit. Care Med. 2010, 181(8):838-850.
81. Storm E.E., Rubenstein J.L., Martin G.R. Dosage of Fgf8 determines whether cell survival is positively or negatively regulated in the developing forebrain. Proc. Natl Acad. Sci. USA 2003, 100:1757-1762.
82. Storm E.E., Garel S., Borello U., Hebert J.M., Martinez S., McConnell S.K., Martin G.R., Rubenstein J.L. Dose-dependent functions of Fgf8 in regulating telencephalic patterning centers. Development 2006, 133:1831-1844.
83. Sun X., Meyers E.N., Lewandoski M., Martin G.R. Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev. 1999, 13:1834-1846.
84. Sun X., Mariani F.V., Martin G.R. Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 2002, 418:501-508.
85. Szebenyi G., Fallon J.F. Fibroblast growth factors as multifunctional signaling factors. Int. Rev. Cytol. 1999, 185:45-106.
86. Tai C.C., Sala F.G., Ford H.R., Wang K.S., Li C., Minoo P., Grikscheit T.C., Bellusci S. Wnt5a knock-out mouse as a new model of anorectal malformation. J. Surg. Res. 2009, 156:278-282.
87. Trokovic N., Trokovic R., Mai P., Partanen J. Fgfr1 regulates patterning of the pharyngeal region. Genes Dev. 2003, 17:141-153.
88. Trokovic R., Trokovic N., Hernesniemi S., Pirvola U., Vogt Weisenhorn D.M., Rossant J., McMahon A.P., Wurst W., Partanen J. FGFR1 is independently required in both developing mid- and hindbrain for sustained response to isthmic signals. EMBO J. 2003, 22:1811-1823.
89. Trumpp A., Depew M.J., Rubenstein J.L., Bishop J.M., Martin G.R. Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev. 1999, 13:3136-3148.
90. Usui H., Shibayama M., Ohbayashi N., Konishi M., Takada S., Itoh N. Fgf18 is required for embryonic lung alveolar development. Biochem. Biophys. Res. Commun. 2004, 322:887-892.
91. Warburton D., Zhao J., Berberich M.A., Bernfield M. Molecular embryology of the lung: then, now, and in the future. Am. J. Physiol. Lung Cell. Mol. Physiol. 1999, 276:L697-L704.
92. Warburton D., Schwarz M., Tefft D., Flores-Delgado G., Anderson K.D., Cardoso W.V. The molecular basis of lung morphogenesis. Mech. Dev. 2000, 92:55-81.
93. Watanabe Y., Miyagawa-Tomita S., Vincent S.D., Kelly R.G., Moon A.M., Buckingham M.E. Role of mesodermal FGF8 and FGF10 overlaps in the development of the arterial pole of the heart and pharyngeal arch arteries. Circ. Res. 2009.
94. Weinstein M., Xu X., Ohyama K., Deng C.X. FGFR-3 and FGFR-4 function cooperatively to direct alveogenesis in the murine lung. Development 1998, 125:3615-3623.
95. Wert S.E., Dey C.R., Blair P.A., Kimura S., Whitsett J.A. Increased expression of thyroid transcription factor-1 (TTF-1) in respiratory epithelial cells inhibits alveolarization and causes pulmonary inflammation. Dev. Biol. 2002, 242:75-87.
96. Yamamoto H., Yun E.J., Gerber H.P., Ferrara N., Whitsett J.A., Vu T.H. Epithelial-vascular cross talk mediated by VEGF-A and HGF signaling directs primary septa formation during distal lung morphogenesis. Dev. Biol. 2007, 308:44-53.
97. Yi M., Belcastro R., Shek S., Luo D., Post M., Tanswell A.K. Fibroblast growth factor-2 and receptor-1alpha(IIIc) regulate postnatal rat lung cell apoptosis. Am. J. Respir. Crit. Care Med. 2006, 174:581-589.
98. Zhang X., Ibrahimi O.A., Olsen S.K., Umemori H., Mohammadi M., Ornitz D.M. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J. Biol. Chem. 2006, 281:15694-15700.