FGF10 is required for cell proliferation and gland formation in the stomach epithelium of the chicken embryo

Developmental Biology

Volumn 294, Issue 1, 2006, Pages 11-23

  Shin, Masahiro ^a   Noji, Sumihare ^b   Neubüser, Annette ^c   Yasugi, Sadao ^a  

^a TOKYO METROPOLITAN UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

cSP; Digestive tract; ECPg; Epithelial mesenchymal interactions; FGF10; FGFR1b; FGFR2b; Proventricular gland; sFGFR2b; Stomach

Indexed keywords

FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 2B; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; VIRUS VECTOR;

ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; CHICKEN; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIUM CELL; EXPRESSION VECTOR; GENE OVEREXPRESSION; MESENCHYME; MORPHOGENESIS; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; STOMACH EPITHELIUM; STOMACH GLAND; STOMACH GLAND DEVELOPMENT;

ANIMALIA; VERTEBRATA;

EID: 33645989377     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2005.12.019     Document Type: Article

References (74)

1. Alvarez Y., Alonso M.T., Vendrell V., Zelarayan L.C., Chamero P., Theil T., Bosl M.R., Kato S., Maconochie M., Riethmacher D., et al. Requirements for FGF3 and FGF10 during inner ear formation. Development 130 (2003) 6329-6338
2. Amaya E., Musci T.J., and Kirschner M.W. Expression of a dominant-negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell 66 (1991) 257-270
3. Asaki T., Konishi M., Miyake A., Kato S., Tomizawa M., and Itoh N. Roles of fibroblast growth factor 10 (Fgf10) in adipogenesis in vivo. Mol. Cell. Endocrinol. 218 (2004) 119-128
4. Basilico C., and Moscatelli D. The FGF family of growth factors and oncogenes. Adv. Cancer Res. 59 (1992) 115-165
5. Beauchamp R.D., Barnard J.A., McCutchen C.M., Cherner J.A., and Coffey Jr. R.J. Localization of transforming growth factor alpha and its receptor in gastric mucosal cells. Implications for a regulatory role in acid secretion and mucosal renewal. J. Clin. Invest. 84 (1989) 1017-1023
6. Beer H.D., Vindevoghel L., Gait M.J., Revest J.M., Duan D.R., Mason I., Dickson C., and Werner S. Fibroblast growth factor (FGF) receptor 1-IIIb is a naturally occurring functional receptor for FGFs that is preferentially expressed in the skin and the brain. J. Biol. Chem. 275 (2000) 16091-16607
7. Bellot F., Crumley G., Kaplow J.M., Schlessinger J., Jaye M., and Dionne C.A. Ligand-induced transphosphorylation between different FGF receptors. EMBO J. 10 (1991) 2849-2854
8. Bennett C., Paterson I.M., Corbishley C.M., and Luqmani Y.A. Expression of growth factor and epidermal growth factor receptor encoded transcripts in human gastric tissues. Cancer Res. 49 (1989) 2104-2111
9. Bhushan A., Itoh N., Kato S., Thiery J.P., Czernichow P., Bellusci S., and Scharfmann R. Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 128 (2001) 5109-5117
10. Bockman D.E., Sharp R., and Merlino G. Regulation of terminal differentiation of zymogenic cells by transforming growth factor alpha in transgenic mice. Gastroenterology 108 (1995) 447-454
11. Burns R.C., Fairbanks T.J., Sala F., De Langhe S., Mailleux A., Thiery J.P., Dickson C., Itoh N., Warburton D., Anderson K.D., et al. Requirement for fibroblast growth factor 10 or fibroblast growth factor receptor 2-IIIb signaling for cecal development in mouse. Dev. Biol. 265 (2004) 61-74
12. Celli G., LaRochelle W.J., Mackem S., Sharp R., and Merlino G. Soluble dominant-negative receptor uncovers essential roles for fibroblast growth factors in multi-organ induction and patterning. EMBO J. 17 (1998) 1642-1655
13. De Moerlooze L., Spencer-Dene B., Revest J., Hajihosseini M., Rosewell I., and Dickson C. An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127 (2000) 483-492
14. Eswarakumar V.P., Lax I., and Schlessinger J. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev. 16 (2005) 139-149
15. Fukuda K., Ishii Y., Saiga H., Shiokawa K., and Yasugi S. Mesenchymal regulation of epithelial gene expression in developing avian stomach: 5′-flanking region of pepsinogen gene can mediate mesenchymal influence on its expression. Development 120 (1994) 3487-3495
16. Fukuda K., Kameda T., Saitoh K., Iba H., and Yasugi S. Down-regulation of endodermal Shh is required for gland formation in chicken stomach. Mech. Dev. 120 (2003) 801-809
17. Haffen K., Kedinger M., and Simon-Assmann P. Mesenchyme-dependent differentiation of epithelial progenitor cells in the gut. J. Pediatr. Gastroenterol. Nutr. 6 (1987) 14-23
18. Harada H., Toyono T., Toyoshima K., Yamasaki M., Itoh N., Kato S., Sekine K., and Ohuchi H. FGF10 maintains stem cell compartment in developing mouse incisors. Development 129 (2002) 1533-1541
19. Hayashi K., Yasugi S., and Mizuno T. Isolation and structural analysis of embryonic chicken pepsinogen gene: avian homologue of prochymosin gene. Biochem. Biophys. Res. Commun. 152 (1988) 776-782
20. Hebrok M., Kim S.K., and Melton D.A. Notochord repression of endodermal Sonic hedgehog permits pancreas development. Genes Dev. 12 (1998) 1705-1713
21. Iba H. Gene transfer into chicken embryos by retrovirus vectors. Dev. Growth Differ. 42 (2000) 213-218
22. Igarashi M., Finch P.W., and Aaronson S.A. Characterization of recombinant human fibroblast growth factor (FGF)-10 reveals functional similarities with keratinocyte growth factor (FGF-7). J. Biol. Chem. 273 (1998) 13230-13235
23. Ishii Y., Fukuda K., Saiga H., Matsushita S., and Yasugi S. Early specification of intestinal epithelium in the chicken embryo: a study on the localization and regulation of CdxA expression. Dev. Growth Differ. 39 (1997) 643-653
24. Ishii Y., Rex M., Scotting P.J., and Yasugi S. Region-specific expression of chicken Sox2 in the developing gut and lung epithelium: regulation by epithelial-mesenchymal interactions. Dev. Dyn 213 (1998) 464-475
25. Itoh N., and Ornitz D.M. Evolution of the Fgf and Fgfr gene families. Trends Genet. 20 (2004) 563-569
26. Jackson D., Bresnick J., Rosewell I., Crafton T., Poulsom R., Stamp G., and Dickson C. Fibroblast growth factor receptor signalling has a role in lobuloalveolar development of the mammary gland. J. Cell Sci. 110 (1997) 1261-1268
27. Jacobsen C.M., Narita N., Bielinska M., Syder A.J., Gordon J.I., and Wilson D.B. Genetic mosaic analysis reveals that GATA-4 is required for proper differentiation of mouse gastric epithelium. Dev. Biol. 241 (2002) 34-46
28. Jin D.Y., Ishii Y., and Yasugi S. Localization of DNA-synthesizing cells and cell proliferation pattern in developing proventricular (glandular stomach) epithelium of embryonic and hatched chickens. Dev. Growth Differ. 38 (1996) 1-8
29. Kim S.K., Hebrok M., and Melton D.A. Notochord to endoderm signaling is required for pancreas development. Development 124 (1997) 4243-4252
30. Koike T., and Yasugi S. In vitro analysis of mesenchymal influences on the differentiation of stomach epithelial cells of the chicken embryo. Differentiation 65 (1999) 13-25
31. Laufer E., Nelson C.E., Johnson R.L., Morgan B.A., and Tabin C. Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 79 (1994) 993-1003
32. Le Douarin N.M. An experimental analysis of liver development. Med. Biol. 53 (1975) 427-455
33. Mailleux A.A., Spencer-Dene B., Dillon C., Ndiaye D., Savona-Baron C., Itoh N., Kato S., Dickson C., Thiery J.P., and Bellusci S. Role of FGF10/FGFR2b signaling during mammary gland development in the mouse embryo. Development 129 (2002) 53-60
34. Makarenkova H.P., Ito M., Govindarajan V., Faber S.C., Sun L., McMahon G., Overbeek P.A., and Lang R.A. FGF10 is an inducer and Pax6 a competence factor for lacrimal gland development. Development 127 (2000) 2563-2572
35. Mandler M., and Neubuser A. FGF signaling is required for initiation of feather placode development. Development 131 (2004) 3333-3343
36. Marcelle C., Eichmann A., Halevy O., Breant C., and Le Douarin N.M. Distinct developmental expression of a new avian fibroblast growth factor receptor. Development 120 (1994) 683-694
37. Marics I., Padilla F., Guillemot J.F., Scaal M., and Marcelle C. FGFR4 signaling is a necessary step in limb muscle differentiation. Development 129 (2002) 4559-4569
38. Matsuda Y., Wakamatsu Y., Kohyama J., Okano H., Fukuda K., and Yasugi S. Notch signaling functions as a binary switch for the determination of glandular and luminal fates of endodermal epithelium during chicken stomach development. Development 132 (2005) 2783-2793
39. Matsumoto K., Saitoh K., Koike C., Narita T., Yasugi S., and Iba H. Differential expression of fos and jun family members in the developing chicken gastrointestinal tract. Oncogene 16 (1998) 1611-1616
40. Miki T., Bottaro D.P., Fleming T.P., Smith C.L., Burgess W.H., Chan A.M., and Aaronson S.A. Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 246-250
41. Mizuno T., and Yasugi S. Susceptibility of epithelia to directive influences of mesenchymes during organogenesis: uncoupling of morphogenesis and cytodifferentiation. Cell Differ. Dev. 31 (1990) 151-159
42. Narita T., Ishii Y., Nohno T., Noji S., and Yasugi S. Sonic hedgehog expression in developing chicken digestive organs is regulated by epithelial-mesenchymal interactions. Dev. Growth Differ. 40 (1998) 67-74
43. Narita T., Saitoh K., Kameda T., Kuroiwa A., Mizutani M., Koike C., Iba H., and Yasugi S. BMPs are necessary for stomach gland formation in the chicken embryo: a study using virally induced BMP-2 and Noggin expression. Development 127 (2000) 981-988
44. Nohno T., Kawakami Y., Ohuchi H., Fujiwara A., Yoshioka H., and Noji S. Involvement of the Sonic hedgehog gene in chick feather formation. Biochem. Biophys. Res. Commun. 206 (1995) 33-39
45. Ohuchi H., Nakagawa T., Yamamoto A., Araga A., Ohata T., Ishimaru Y., Yoshioka H., Kuwana T., Nohno T., Yamasaki M., et al. The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development 124 (1997) 2235-2244
46. Ohuchi H., Hori Y., Yamasaki M., Harada H., Sekine K., Kato S., and Itoh N. FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development. Biochem. Biophys. Res. Commun. 277 (2000) 643-649
47. Ohuchi H., Tao H., Ohata K., Itoh N., Kato S., Noji S., and Ono K. Fibroblast growth factor 10 is required for proper development of the mouse whiskers. Biochem. Biophys. Res. Commun. 302 (2003) 562-567
48. Ornitz D.M., Xu J., Colvin J.S., McEwen D.G., MacArthur C.A., Coulier F., Gao G., and Goldfarb M. Receptor specificity of the fibroblast growth factor family. J. Biol. Chem. 271 (1996) 15292-15297
49. Peters K.G., Werner S., Chen G., and Williams L.T. Two FGF receptor genes are differentially expressed in epithelial and mesenchymal tissues during limb formation and organogenesis in the mouse. Development 114 (1992) 233-243
50. Powers C.J., McLeskey S.W., and Wellstein A. Fibroblast growth factors, their receptors and signaling. Endocr. Relat. Cancer 7 (2000) 165-197
51. Robinson M.L., MacMillan-Crow L.A., Thompson J.A., and Overbeek P.A. Expression of a truncated FGF receptor results in defective lens development in transgenic mice. Development 121 (1995) 3959-3967
52. Romanoff A.L. The Avian Embryo (1960), Macmillan, New York
53. Sakamoto N., Fukuda K., Watanuki K., Sakai D., Komano T., Scotting P.J., and Yasugi S. Role for cGATA-5 in transcriptional regulation of the embryonic chicken pepsinogen gene by epithelial-mesenchymal interactions in the developing chicken stomach. Dev. Biol. 223 (2000) 103-113
54. Sato K., and Yasugi S. Chicken keratin-19: cloning of cDNA and analysis of expression in thechicken embryonic gut. Dev. Growth Differ. 39 (1997) 751-761
55. Sharp R., Babyatsky M.W., Takagi H., Tagerud S., Wang T.C., Bockman D.E., Brand S.J., and Merlino G. Transforming growth factor alpha disrupts the normal program of cellular differentiation in the gastric mucosa of transgenic mice. Development 121 (1995) 149-161
56. Shin M., Watanuki K., and Yasugi S. Expression of Fgf10 and Fgf receptors during development of the embryonic chicken stomach. Gene Expression Patterns 5 (2005) 511-516
57. Sukegawa A., Narita T., Kameda T., Saitoh K., Nohno T., Iba H., Yasugi S., and Fukuda K. The concentric structure of the developing gut is regulated by Sonic hedgehog derived from endodermal epithelium. Development 127 (2000) 1971-1980
58. Suzuki K., Yamanishi K., Mori O., Kamikawa M., Andersen B., Kato S., Toyoda T., and Yamada G. Defective terminal differentiation and hypoplasia of the epidermis in mice lacking the Fgf10 gene. FEBS Lett. 481 (2000) 53-56
59. Szebenyi G., and Fallon J.F. Fibroblast growth factors as multifunctional signaling factors. Int. Rev. Cytol. 185 (1999) 45-106
60. Tabata H., and Yasugi S. Tissue interaction regulates expression of a spasmolytic polypeptide gene in chicken stomach epithelium. Dev. Growth Differ. 40 (1998) 519-526
61. Takeda J., Tabata H., Fukuda K., and Yasugi S. Involvement of the signal transduction pathway mediated by epidermal growth factor receptor in the differentiation of chicken glandular stomach. Dev. Growth Differ. 44 (2002) 501-508
62. Takiguchi K., Yasugi S., and Mizuno T. Gizzard epithelium of chick embryo can express embryonic pepsinogen antigen, a marker protein of proventriculus. Roux's Arch. Dev. Biol. 195 (1986) 475-483
63. Ueno H., Gunn M., Dell K., Tseng Jr. A., and Williams L. A truncated form of fibroblast growth factor receptor 1 inhibits signal transduction by multiple types of fibroblast growth factor receptor. J. Biol. Chem. 267 (1992) 1470-1476
64. Urase K., and Yasugi S. Induction and inhibition of epithelial differentiation by the mixed cell aggregates of mesenchymes from the chicken embryonic digestive tract. Dev. Growth Differ. 35 (1993) 33-40
65. Urase K., Mukasa T., Igarashi H., Ishii Y., Yasugi S., Momoi M.Y., and Momoi T. Spatial expression of Sonic hedgehog in the lung epithelium during branching morphogenesis. Biochem. Biophys. Res. Commun. 225 (1996) 161-166
66. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., and Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273 (1996) 613-622
67. Werner S., Peters K.G., Longaker M.T., Fuller-Pace F., Banda M.J., and Williams L.T. Large induction of keratinocyte growth factor expression in the dermis during wound healing. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 6896-6900
68. Werner S., Smola H., Liao X., Longaker M.T., Krieg T., Hofschneider P.H., and Williams L.T. The function of KGF in morphogenesis of epithelium and reepithelialization of wounds. Science 266 (1994) 819-822
69. Wessels N.K. Tissue Interaction and Development (1977), W.A. Benjamin, California
70. Wright T.J., and Mansour S.L. Fgf3 and Fgf10 are required for mouse otic placode induction. Development 130 (2003) 3379-3390
71. Yang J., Richards J., Bowman P., Guzman R., Enami J., McCormick K., Hamamoto S., Pitelka D., and Nandi S. Sustained growth and three-dimensional organization of primary mammary tumor epithelial cells embedded in collagen gels. Proc. Natl. Acad. Sci. U. S. A. 76 (1979) 3401-3405
72. Yasugi S. Role of epithelial-mesenchymal interactions in differentiation of epithelium of vertebrate digestive organs. Dev. Growth Differ. 35 (1993) 1-9
73. Yasugi S. The role of mesenchymal tissue in the development of the gut. Connect. Tissue 32 (2000) 273-278
74. Yasugi S., and Fukuda K. The mesenchymal factor regulating epithelial morphogenesis and differentiation of the chicken stomach. Zool. Sci. 17 (2000) 1-9