Epithelial/mesenchymal interactions and branching morphogenesis of the lung

Current Opinion in Genetics and Development

Volumn 8, Issue 4, 1998, Pages 481-486

  Hogan, Brigid L M ^a   Yingling, Jonathan M ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR;

ARTICLE; CELL INTERACTION; DROSOPHILA; EMBRYO; EPITHELIUM CELL; GENETIC CONSERVATION; LUNG DEVELOPMENT; MESENCHYME CELL; MORPHOGENESIS; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRACHEA; VERTEBRATE;

VERTEBRATA;

EID: 0031693463     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(98)80121-4     Document Type: Article

References (46)

1. Samakovlis C, Hacohen N, Manning G, Sutherland DC, Guillemin K, Krasnow MA: Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 1996, 122:1395-1407.
2. Isaac DD, Andrew DJ: Tubulogenesis in Drosophila: a requirement for the trachealess gene product. Genes Dev 1996, 10:103-117.
3. Wilk R, Weizman I, Shilo BZ: trachealess encodes a bHIh-Pas protein that is an inducer of tracheal cell fates in Drosophila. Genes Dev 1996, 10:93-102.
4. de Celis JF, Llimargas M, Casanova J: Ventral veinless, the gene encoding the Cf1a transcription factor, links positional information and cell differentiation during embryonic and imaginal development in Drosophila melanogaster. Development 1995, 121:3405-3416.
5. Anderson MG, Perkins GL, Chittick P, Shrigley RJ, Johnson WA: drifter, a Drosophila Pou-domain transcription factor, is required for correct differentiation and migration of tracheal cells and midline glia. Genes Dev 1995, 9:123-137.
6. Sonnenfeld M, Ward M, Nystrom G, Mosher J, Stahl S, Crews S: The Drosophila tango gene encodes a bHLH-PAS protein that is orthologous to mammalian Arnt and controls CNS midline and tracheal development. Development 1997, 124:4571-4582. A recent paper in which a heterodimeric partner of trachealess is cloned. Tango mutants have tracheal defects and gene-dosage experiments demonstrate in vivo interactions between trh and tango.
7. Ohshiro T, Saigo K: Transcriptional regulation of breathless FGF receptor gene by binding of TRACHEALESS/dARNT heterodimers to three central midline elements in Drosophila developing trachea. Development 1997, 124:3975-3986. An excellent paper describing the cloning of dARNT (Tango), a heterodimeric partner for trachealess. The minimal enhancer region of the breathless gene contains three CMEs (central midline elements). A bHLH-PAS/hARNT (human ARNT) heterodimeric complex (SIM/hARNT) was known to bind these sites in vitro. The authors reasoned that the Drosophila ARNT homolog may be a heterodimeric binding partner for TRH and that this complex may regulate BTL expression in the trachea. The experiments clearly demonstrate that TRH/dARNT heterodimers indeed regulate BTL expression via CME sites in the promoter.
8. Anderson MG, Certel SJ, Certel K, Lee T, Montell DJ, Johnson WA: Function of the Drosophila POU domain transcription factor drifter as an upstream regulator of breathless receptor tyrosine kinase expression in developing trachea. Development 1996, 122:4169-4178.
9. Llimargas M, Casanova J: ventral veinless, a Pou domain transcription factor, regulates different transduction pathways required for tracheal branching in Drosophila. Development 1997, 124:3273-3281. These authors investigate the possibility that Ventral veinless (Vvl), also known as Drifter (Dfr), regulates tracheal system development beyond its role in maintaining breathless expression. An elegant series of genetic experiments demonstrate a role for Vvl in tracheal expression of thick veins (tkv) and rhomboid (rho), two genes essential for Dpp and Spitz signaling, respectively. An activated form of the Tkv receptor is capable of changing the migratory fate of specific tracheal cells, firmly establishing a role for Dpp signaling in tracheal system development.
10. Sutherland D, Samakovlis C, Krasnow MA: branchless encodes a Drosophila Fgf homolog that controls tracheal cell migration and the pattern of branching. Cell 1996, 87:1091-1101.
11. Lee T, Hacohen N, Krasnow M, Montell DJ: Regulated Breathless receptor tyrosine kinase activity required to pattern cell migration and branching in the Drosophila tracheal system. Genes Dev 1996, 10:2912-2921.
12. Klambt C, Glazer L, Shilo BZ: breathless, a Drosophila Fgf receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev 1992, 6:1668-1678.
13. Glazer L, Shilo BZ: The Drosophila FGF-R homolog is expressed in the embryonic tracheal system and appears to be required for directed tracheal cell extension. Genes Dev 1991, 5:697-705.
14. Reichman-Fried M, Shilo BZ: Breathless, a Drosophila FGF receptor homolog, is required for the onset of tracheal cell migration and tracheole formation. Mech Dev 1995, 52:265-273.
15. Vincent S, Ruberte E, Grieder NC, Chen CK, Haerry T, Schuh R, Affolter M: DPP controls tracheal cell migration along the dorsoventral body axis of the Drosophila embryo. Development 1997, 124:2741-2750. A strong genetics paper firmly establishing a role for Dpp signaling in tracheal system development. Activated and dominant negative Dpp receptors were used to demonstrate that Dpp signaling is required to 'program' tracheal cells to migrate dorsoventrally. Moreover, Dpp signaling was shown to change the migratory fate of anteroposterior branch cells to dorsoventrally migrating cells. Dorsal expression of Branchless was also shown to require dpp activity.
16. Bier E, Jan LY, Jan YN: rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev 1990, 4:190-203.
17. Wappner P, Gabay L, Shilo BZ: Interactions between the EGF receptor and DPP pathways establish distinct cell fates in the tracheal placodes. Development 1997, 124:4707-4716. Another excellent paper that examines the mechanisms responsible for establishing tracheal cell migratory fate before the initiation of migration in response to the Bnl/Btl pathway. Using an antibody against the double phosphorylated form of ERK (dp-ERK), localized Spitz activation is shown to be required for anteroposterior migration. Dpp is responsible for dorsoventral migration. Importantly, both pathways are shown to be instructive as elimination of both signals eliminates tracheal cell migration entirely. Antagonistic interactions between these two pathways is also demonstrated.
18. Newfeld SJ, Chartoff EH, Graff JM, Melton DA, Gelbart WM: Mothers against dpp encodes a conserved cytoplasmic protein required in DPP/TGF-beta responsive cells. Development 1996, 122:2099-2108.
19. Newfeld SJ, Mehra A, Singer MA, Wrana JL, Attisano L, Gelbart WM: Mothers against dpp participates in a DDP/TGF-beta responsive serine-threonine kinase signal transduction cascade. Development 1997, 124:3167-3176.
20. Tsuneizumi K, Nakayama T, Kamoshida Y, Kornberg TB, Christian JL, Tabata T: Daughters against dpp modulates dpp organizing activity in Drosophila wing development. Nature 1997, 389:627-631.
21. Kretzschmar M, Doody J, Massagué J: Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1. Nature 1997, 389:618-622.
22. Affolter M, Nellen D, Nussbaumer U, Basler K: Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TGF beta homologs during Drosophila embryogenesis. Development 1994, 120:3105-3117.
23. Stark KA, Yee GH, Roote CE, Williams EL, Zusman S, Hynes RO: A novel alpha integrin subunit associates with betaPS and functions in tissue morphogenesis and movement during Drosophila development. Development 1997, 124:4583-4594.
24. Uemura T, Oda H, Kraut R, Hayashi S, Kotaoka Y, Takeichi M: Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev 1996, 10:659-671.
25. Eulenberg KG, Schuh R: The tracheae defective gene encodes a bZIP protein that controls tracheal cell movement during Drosophila embryogenesis. EMBO J 1997, 16:7156-7165. Molecular characterization of the tdf gene which is involved in a wide variety of migratory events during embryogenesis, including tracheal system migration, tdf is shown to be regulated by trachealess and to be required for general cell migration. It functions in parallel to the Dpp and Bnl/Btl pathways which govern directed cell migration.
26. Hacohen N, Kramer S, Sutherland D, Hiromi Y, Krasnow MA: sprouty encodes a novel antagonist of Fgf signaling that patterns apical branching of the Drosophila airways. Cell 1998, 92:253-263. An important paper describing a novel gene, sprouty that encodes a secreted FGF signaling antagonist. Imprecise excision of a silent P-transposon insertion in the sprouty locus produces ectopic branch formation. Mutations in sprouty result in hyperactivation of the Bnl/Btl signaling pathway and genetic mosaic analysis demonstrates that this gene acts nonautonomously in tracheal tip cells to inhibit branching in nearby stalk cells. Transcription of sprouty was found to be induced by activation of the Bnl/Btl pathway to establish a negative feedback loop to limit the range of Bnl/Btl signaling. Finally, a BLAST search identified three human homologs of Sprouty.
27. Holley SA, Jackson PD, Sasai Y, Lu B, De Robertis EM, Hoffmann FM, Ferguson EL: A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 1995, 376:249-253.
28. Bogue CW, Lou LJ, Vasavada H, Wilson CM, Jacobs HC: Expression of HoxB genes in the developing mouse foregut and lung. Am J Respir Cell Mol Biol 1996, 15:163-171.
29. Mollard R, Dziadek M: Homeobox genes from clusters A and B demonstrate characteristics of temporal colinearity and differential restrictions in spatial expression domains in the branching mouse lung. Int J Dev Biol 1997, 41:655-666. A systematic study of the expression of HoxA and HoxB genes during branching morphogenesis of the embryonic mouse lung using RT-PCR. The temporal and colinear activation of Hox genes suggests a potential role for Hox genes during all three stages of embryonic lung development.
30. Ten Have-Opbroek AAW: The development of the lung in mammals: an analysis of concepts and findings. Am J Anat 1981, 162:201-219.
31. Wessells NK: Mammalian lung development: interactions in formation and morphogenesis of tracheal buds. J Exp Zool 1970, 175:455-466.
32. Wert SE, Glasser SW, Korfhagen TR, Whitsett JA: Transcriptional elements from the human SP-C gene direct expression in the primordial respiratory epithelium of transgenic mice. Dev Biol 1993, 156:426-443.
33. Peters K, Werner S, Liao X, Wert S, Whitsett J, Williams L: Targeted expression of a dominant negative FGF receptor blocks branching morphogenesis and epithelial differentiation of the mouse lung. EMBO J 1994, 13:3296-3301.
34. Post M, Souza P, Liu J, Tseu I, Wang J, Kuliszewski M, Tanswell AK: Keratinocyte growth factor and its receptor are involved in regulating early lung branching. Development 1996, 122:3107-3115.
35. Shiratori M, Oshika E, Ung LP, Singh G, Shinozuka H, Warburton D, Michalopoulos G, Katyal SL: Keratinocyte growth factor and embryonic rat lung morphogenesis. Am J Respir Cell Mol Biol 1996, 15:328-338.
36. Cardoso WV, Itoh A, Nogawa H, Mason I, Brody JS: FGF-1 and FGF-7 induce distinct patterns of growth and differentiation in embryonic lung epithelium. Dev Dyn 1997, 208:398-405. Mesenchyme-free lung epithelial cultures are used to examine the biological effects of FGF1 and FGF7 on murine lung development. FGF1 is shown to promote epithelial proliferation, bud formation and expression of surfactant protein-B (SP-B); whereas FGF7 induces epithelial proliferation without bud formation resulting in cyst-like structures. FGF7 induces both SP-A and SP-B. The observed effects correlate with the distribution of the FGF receptors, FGFR2-IIIb (KGFR) and FGFR4.
37. Ohmichi H, Koshimizu U, Matsumoto K, Nakamura T: Hepatocyte growth factor (HGF) acts as a mesenchyme-derived morphogenic factor during fetal lung development. Development 1998, 125:1315-1324. A detailed analysis of the role of HGF and c-met/HGF-R in lung development. RT-PCR is used to determine that expression of HGF is confined to the lung mesenchyme, whereas HGF-R is expressed in the adjacent endoderm, predicting involvement of this pathway in epithelial/mesenchymal interactions during lung development. In vitro organ cultures demonstrate the ability of HGF to stimulate branching morphogenesis and anti-sense or neutralizing antibody studies against HGF inhibit branching. Most importantly, evidence is presented for the synergistic activities of HGF and FGF in mediating branching morphogenesis of the lung in organ culture.
38. Bellusci S, Grindley J, Emoto H, Itoh N, Hogan BL: Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 1997, 124:4867-4878. A detailed analysis of the expression and activity of FGF10 in mediating branching morphogenesis of the lung. FGF10 is demonstrated to be dynamically expressed in pulmonary mesenchyme from the earliest stages of lung development. Addition of FGF10 to in vitro organ cultures results in extensive branching morphogenesis. Comparison of the in vivo expression of FGF10, FGF1 and FGF7 indicates that FGF10 is the most likely endogenous FGF responsible for early epithelial proliferation and outgrowth.
39. Miettinen PJ, Warburton D, Bu D, Zhao JS, Berger JE, Minoo P, Koivisto T, Allen L, Dobbs L, Werb Z et al.: Impaired lung branching morphogenesis in the absence of functional EGF receptor. Dev Biol 1997, 186:224-236. A detailed analysis of the pulmonary defect present in EGF receptor deficient mice. Histology, electron microscopy, organ culture and RT-PCR are used to characterize the immature lung phenotype of these mice.
40. Kimura S, Hara Y, Pineau T, Fernandez-Salguero P, Fox CH, Ward JM, Gonzalez FJ: 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.
41. Bellusci S, Henderson R, Winnier G, Oikawa T, Hogan BL: Evidence from normal expression and targeted misexpression that bone morphogenetic protein (Bmp-4) plays a role in mouse embryonic lung morphogenesis. Development 1996, 122:1693-1702.
42. Bellusci S, Furuta Y, Rush MG, Henderson R, Winnier G, Hogan BL: Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 1997, 124:53-63. A second paper from this group (see [41]) utilizing a transgenic approach to analyze the role of a potentially important signaling molecule in lung organogenesis. The phenotype of these transgenic lungs suggests that Shh normally stimulates mesenchymal proliferation in vivo. The expression profile of a number of potentially important signaling molecules in lung development is presented (Wnt-2, SHH, BMP4, BMP7). A model for the involvement of these signaling molecules in lung development is discussed.
43. Goodrich LV, Johnson RL, Milenkovic L, McMahon JA, Scott MP: Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev 1996, 10:301-312.
44. Marigo V, Scott MP, Johnson RL, Goodrich LV, Tabin CJ: Conservation in hedgehog signaling: induction of a chicken patched homolog by Sonic hedgehog in the developing limb. Development 1996, 122:1225-1233.
45. Alexandre C, Jacinto A, Ingham PW: Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev 1996, 10:2003-2013.
46. Grindley JC, Bellusci S, Perkins D, Hogan BL: Evidence for the involvement of the Gli gene family in embryonic mouse lung development. Dev Biol 1997, 188:337-348. The expression pattern of three vertebrate Gli genes during the pseudoglandular stage of lung development is examined. All three were found to be strongly expressed in distinct but overlapping domains of the mesoderm. The role of the Gli genes in regulating patched expression via the Shh pathway is discussed and evidence from Gli3XtJ embryos, homozygous for deletion of the Gli3 gene, implicate this gene in normal lung development.