Article

You have full text access to this OnlineOpen article

BMP4 modulates fibroblast growth factor–mediated induction of proximal and distal lung differentiation in mouse embryonic tracheal epithelium in mesenchyme-free culture

  1. Brian A. Hyatt*,
  2. Xiaofei Shangguan,
  3. John M. Shannon

Article first published online: 5 SEP 2002

DOI: 10.1002/dvdy.10145

Issue

Developmental Dynamics

Developmental Dynamics

Volume 225, Issue 2, pages 153–165, October 2002

Additional Information

How to Cite

Hyatt, B. A., Shangguan, X. and Shannon, J. M. (2002), BMP4 modulates fibroblast growth factor–mediated induction of proximal and distal lung differentiation in mouse embryonic tracheal epithelium in mesenchyme-free culture. Dev. Dyn., 225: 153–165. doi: 10.1002/dvdy.10145

Author Information

  1. Division of Pulmonary Biology, Children's Hospital Medical Center, Cincinnati, Ohio

*Children's Hospital Medical Center, Division of Pulmonary Biology, 3333 Burnet Avenue, Cincinnati, OH 45229-3039

Publication History

  1. Issue published online: 19 SEP 2002
  2. Article first published online: 5 SEP 2002
  3. Manuscript Accepted: 11 JUL 2002
  4. Manuscript Received: 12 APR 2002

Funded by

  • NHLBI. Grant Numbers: SCOR HL56387, T32 HL07752
  • March of Dimes. Grant Number: 19-FY99-712

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (820K)

REFERENCES

  • Alescio T, Cassini A. 1962. Induction in vitro of tracheal buds by pulmonary mesenchyme grafted on tracheal epithelium. J Exp Zool 150: 83–94.
    Direct Link:
  • Arman E, Haffner-Krausz R, Gorivodsky M, Lonai P. 1999. Fgfr2 is required for limb outgrowth and lung-branching morphogenesis. Proc Natl Acad Sci U S A 96: 11895–11899.
  • Bellusci S, Henderson R, Winnier G, Oikawa T, Hogan BLM. 1996. Evidence from normal expression and targeted misexpression that Bone Morphogenetic Protein-4 (Bmp-4) plays a role in mouse embryonic lung morphogenesis. Development 122: 1693–1702.
  • Bellusci S, Furuta Y, Rush MG, Henderson R, Winnier G, Hogan BLM. 1997a. Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 124: 53–63.
  • Bellusci S, Grindley J, Emoto H, Itoh N, Hogan BL. 1997b. Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 124: 4867–4878.
  • Bitgood MJ, McMahon AP. 1995. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev Biol 1: 126–138.
  • Bragg AD, Moses HL, Serra R. 2001. Signaling to the epithelium is not sufficient to mediate all of the effects of transforming growth factor beta and bone morphogenetic protein 4 on murine embryonic lung development. Mech Dev 109: 13–26.
  • Cardoso WV, Itoh A, Nogawa H, Mason I, Brody JS. 1997. FGF-1 and FGF-7 induce distinct patterns of growth and differentiation in embryonic lung epithelium. Dev Dyn 208: 398–405.
    Direct Link:
  • Celli G, LaRochelle WJ, Mackem S, Sharp R, Merlino G. 1998. Soluble dominant-negative receptor uncovers essential roles for fibroblast growth factors in multi-organ induction and patterning. EMBO J 17: 1642–1655.
  • Colvin JS, Feldman B, Nadeau JH, Goldfarb M, Ornitz DM. 1999. Genomic organization and embryonic expression of the mouse fibroblast growth factor 9 gene. Dev Dyn 216: 72–88.
    Direct Link:
  • Colvin JS, White AC, Pratt SJ, Ornitz DM. 2001. Lung hypoplasia and neonatal death in Fgf9-null mice identify this gene as an essential regulator of lung mesenchyme. Development 128: 2095–2106.
  • De Moerlooze L, Spencer-Dene B, Revest J, Hajihosseini M, Rosewell I, Dickson C. 2000. An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127: 483–492.
  • Deterding RR, Shannon JM. 1995. Proliferation and differentiation of fetal rat pulmonary epithelium in the absence of mesenchyme. J Clin Invest 95: 2963–2972.
  • Deterding RR, Jacoby CR, Shannon JM. 1996. Acidic fibroblast growth factor and keratinocyte growth factor stimulate fetal rat pulmonary epithelial growth. Am J Physiol 271: L495–L505.
  • Dewulf N, Verschueren K, Lonnoy O, Moren A, Grimsby S, Vande Spiegle K, Miyazono K, Huylebroeck D, Ten Dijke P. 1995. Distinct spatial and temporal expression patterns of two type I receptors for bone morphogenetic proteins during mouse embryogenesis. Endocrinology 136: 2652–2663.
  • Finch PW, Cunha GR, Rubin JS, Wong J, Ron D. 1995. Pattern of keratinocyte growth factor and keratinocyte growth factor receptor expression during mouse fetal development suggests a role in mediating morphogenetic mesenchymal-epithelial interactions. Dev Dyn 203: 223–240.
  • Fisher JH, Shannon JM, Hoffman T, Mason RJ. 1989. Nucleotide and deduced amino acid sequence of the hydrophobic surfactant protein SP-C from the rat: expression in alveolar type II cells and homology with SP-C from other species. Biochim Biophys Acta 995: 225–230.
  • Fu YM, Spirito P, Yu ZX, Biro S, Sasse J, Lei J, Ferrans VJ, Epstein SE, Casscells W. 1991. Acidic fibroblast growth factor in the developing rat embryo. J Cell Biol 114: 1261–1273.
  • Gonzalez A-M, Buscaglia M, Ong M, Baird A. 1990. Distribution of basic fibroblast growth factor in the 18-day rat fetus: localization in the basement membranes of diverse tissues. J Cell Biol 110: 753–765.
  • Guo L, Degenstein L, Fuchs E. 1996. Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev 10: 165–175.
  • Hackett BP, Brody SL, Liang M, Zeitz ID, Bruns LA, Gitlin JD. 1995. Primary structure of hepatocyte nuclear factor/forkhead homologue 4 and characterization of gene expression in the developing respiratory and reproductive epithelium. Proc Natl Acad Sci U S A 92: 4249–4253.
  • Han RNN, Liu J, Tanswell AK, Post M. 1992. Expression of basic fibroblast growth factor and receptor: immunolocalization studies in developing rat fetal lung. Pediatr Res 31: 435–440.
  • Hu MC, Qiu WR, Wang YP, Hill D, Ring BD, Scully S, Bolon B, DeRose M, Luethy R, Simonet WS, Arakawa T, Danilenko DM. 1998. FGF-18, a novel member of the fibroblast growth factor family, stimulates hepatic and intestinal proliferation. Mol Cell Biol 18: 6063–6074.
  • Kalina M, Mason RJ, Shannon JM. 1992. Surfactant protein C is expressed in alveolar type II cells but not in Clara cells of rat lung. Am J Respir Cell Mol Biol 6: 595–600.
  • Lebeche D, Malpel S, Cardoso WV. 1999. Fibroblast growth factor interactions in the developing lung. Mech Dev 86: 125–136.
  • Liu Z, Xu J, Colvin JS, Ornitz DM. 2002. Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18. Genes Dev 16: 859–869.
  • Lu MM, Yang H, Zhang L, Shu W, Blair DG, Morrisey EE. 2001. The bone morphogenic protein antagonist gremlin regulates proximal-distal patterning of the lung. Dev Dyn 222: 667–680.
    Direct Link:
  • Mason IJ, Fuller-Pace F, Smith R, Dickson C. 1994. FGF-7 (keratinocyte growth factor) expression during mouse development suggests roles in myogenesis, forebrain regionalization and epithelial-mesenchymal interactions. Mech Dev 45: 15–30.
  • Masters JRW. 1976. Epithelial-mesenchymal interaction during lung development: the effect of mesenchymal mass. Dev Biol 51: 98–108.
  • Matsui R, Brody JS, Yu Q. 1999. FGF-2 induces surfactant protein gene expression in foetal rat lung epithelial cells through a MAPK-independent pathway. Cell Signal 11: 221–228.
  • Miller DL, Ortega S, Bashayan O, Basch R, Basilico C. 2000. Compensation by fibroblast growth factor 1 (FGF1) does not account for the mild phenotypic defects observed in FGF2 null mice (published erratum appears in Mol Cell Biol 2000;20:3752). Mol Cell Biol 20: 2260–2268.
  • Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, DeRose M, Simonet WS. 1998. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev 12: 3156–3161.
  • Miralles F, Czernichow P, Ozaki K, Itoh N, Scharfmann R. 1999. Signaling through fibroblast growth factor receptor 2b plays a key role in the development of the exocrine pancreas. Proc Natl Acad Sci U S A 96: 6267–6272.
  • Neubuser A, Peters H, Balling R, Martin GR. 1997. Antagonistic interactions between FGF and BMP signaling pathways: a mechanism for positioning the sites of tooth formation. Cell 90: 247–255.
  • Nogawa H, Ito T. 1995. Branching morphogenesis of embryonic mouse lung epithelium in mesenchyme-free culture. Development 121: 1015–1022.
  • Nogawa H, Morita K, Cardoso WV. 1998. Bud formation precedes the appearance of differential cell proliferation during branching morphogenesis of mouse lung epithelium in vitro. Dev Dyn 213: 228–235.
    Direct Link:
  • Ohbayashi N, Hoshikawa M, Kimura S, Yamasaki M, Fukui S, Itoh N. 1998. Structure and expression of the mRNA encoding a novel fibroblast growth factor, FGF-18. J Biol Chem 273: 18161–18164.
  • Ohbayashi N, Shibayama M, Kurotaki Y, Imanishi M, Fujimori T, Itoh N, Takada S. 2002. FGF18 is required for normal cell proliferation and differentiation during osteogenesis and chondrogenesis. Genes Dev 16: 870–879.
  • Ohtsuka N, Urase K, Momoi T, Nogawa H. 2001. Induction of bud formation of embryonic mouse tracheal epithelium by fibroblast growth factor plus transferrin in mesenchyme-free culture. Dev Dyn 222: 263–272.
    Direct Link:
  • Ornitz DM, Itoh N. 2001. Fibroblast growth factors. Genome Biol 2:REVIEWS3005.
  • Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, Gao G, Goldfarb M. 1996. Receptor specificity of the fibroblast growth factor family. J Biol Chem 271: 15292–15297.
  • Ortega S, Ittmann M, Tsang SH, Ehrlich M, Basilico C. 1998. Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc Natl Acad Sci U S A 95: 5672–5677.
  • Park WY, Miranda B, Lebeche D, Hashimoto G, Cardoso WV. 1998. FGF-10 is a chemotactic factor for distal epithelial buds during lung development. Dev Biol 201: 125–134.
  • Pepicelli CV, Lewis PM, McMahon AP. 1998. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr Biol 8: 1083–1086.
  • Peters H, Balling R. 1999. Teeth. Where and how to make them. Trends Genet 15: 59–65.
  • Peters K, Werner S, Liao X, Wert S, Whitsett J, Williams L. 1994. Targeted expression of a dominant negative FGF receptor blocks branching morphogenesis and epithelial differentiation of the mouse lung. EMBO J 13: 3296–3301.
  • Piscione TD, Phan T, Rosenblum ND. 2001. BMP7 controls collecting tubule cell proliferation and apoptosis via Smad1-dependent and -independent pathways. Am J Physiol Renal Physiol 280: F19–F33.
  • Pizette S, Niswander L. 1999. BMPs negatively regulate structure and function of the limb apical ectodermal ridge. Development 126: 883–894.
  • Post M, Souza P, Liu J, Tseu I, Wang J, Kuliszewski M, Tanswell AK. 1996. Keratinocyte growth factor and its receptor are involved in regulating early lung branching. Development 122: 3107–3115.
  • Rossi JM, Dunn NR, Hogan BL, Zaret KS. 2001. Distinct mesodermal signals, including BMPs from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm. Genes Dev 15: 1998–2009.
  • Sekine K, Ohuchi H, Fujiwara M, Yamasaki M, Yoshizawa T, Sato T, Yagishita N, Matsui D, Koga Y, Itoh N, Kato S. 1999. Fgf10 is essential for limb and lung formation. Nat Genet 21: 138–141.
  • Shannon JM. 1994. Induction of alveolar type II cell differentiation in fetal tracheal epithelium by grafted distal lung mesenchyme. Dev Biol 166: 600–614.
  • Shannon JM. 1996. Epithelial-mesenchymal interactions in lung development. J Jpn Med Soc Biol 26: 47–65.
  • Shannon JM, Nielsen LD, Gebb SA, Randell SH. 1998. Mesenchyme specifies epithelial differentiation in reciprocal recombinants of embryonic lung and trachea. Dev Dyn 212: 482–494.
    Direct Link:
  • Shannon JM, Gebb SA, Nielsen LD. 1999. Induction of alveolar type II cell differentiation in embryonic tracheal epithelium in mesenchyme-free culture. Development 126: 1675–1688.
  • Shi W, Zhao J, Anderson KD, Warburton D. 2001. Gremlin negatively modulates BMP-4 induction of embryonic mouse lung branching morphogenesis. Am J Physiol Lung Cell Mol Physiol 280: L1030–L1039.
  • Shiratori M, Oshika E, Ung LP, Singh G, Shinozuka H, Warburton D, Michalopoulos G, Katyal SL. 1996. Keratinocyte growth factor and embryonic rat lung morphogenesis. Am J Respir Cell Mol Biol 15: 328–338.
  • Strum JM, Compton RS, Katyal SL, Singh G. 1992. The regulated expression of mRNA for Clara cell protein in the developing airways of the rat, as revealed by tissue in situ hybridization. Tissue Cell 24: 461–471.
  • Taderera JT. 1967. Control of lung differentiation in vitro. Dev Biol 16: 489–512.
  • Tichelaar JW, Wert SE, Costa RH, Kimura S, Whitsett JA. 1999. HNF-3/forkhead homologue-4 (HFH-4) is expressed in ciliated epithelial cells in the developing mouse lung. J Histochem Cytochem 47: 823–832.
  • Weaver M, Yingling JM, Dunn NR, Bellusci S, Hogan BL. 1999. Bmp signaling regulates proximal-distal differentiation of endoderm in mouse lung development. Development 126: 4005–4015.
  • Weaver M, Dunn NR, Hogan BL. 2000. Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 127: 2695–2704.
  • Weinstein M, Xu X, Ohyama K, Deng CX. 1998. FGFR-3 and FGFR-4 function cooperatively to direct alveogenesis in the murine lung. Development 125: 3615–3623.
  • Wert SE, Glasser SW, Korfhagen TR, Whitsett JA. 1993. Transcriptional elements from the human SP-C gene direct expression in the primordial respiratory epithelium of transgenic mice. Dev Biol 156: 426–443.
  • Wessells N. 1970. Mammalian lung development: interactions in formation and morphogenesis of tracheal buds. J Exp Zool 175: 455–466.
    Direct Link:
  • Whitsett JA, Clark JC, Picard L, Tichelaar JW, Wert SE, Itoh N, Perl AK, Stahlman MT. 2002. FGF-18 influences proximal programing during lung morphogenesis. J Biol Chem 277: 22743–22749.
  • Wilkinson DG. 1992. Whole mount in situ hybridization of vertebrate embryos. In: WilkinsonDG, editor. In situ hybridization, a practical approach. New York: IRL Press. p 75–83.
  • Yamasaki M, Miyake A, Tagashira S, Itoh N. 1996. Structure and expression of the rat mRNA encoding a novel member of the fibroblast growth factor family. J Biol Chem 271: 15918–15921.
  • Zimmerman LB, De Jesus-Escobar JM, Harland RM. 1996. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86: 599–606.
View Full Article (HTML) Get PDF (820K)