Gastroenterology
Volume 136, Issue 7 , Pages 2074-2091 , June 2009

The Role of the Visceral Mesoderm in the Development of the Gastrointestinal Tract

  • Valérie A. McLin

      Affiliations

    • Department of Pediatrics, Section of Gastroenterology, Hepatology and Nutrition, Baylor College of Medicine, Houston, Texas
    • Corresponding Author InformationReprint requests Address requests for reprints to: Valérie A. McLin, MD, Unite de Gastroenterologie, Hepatologie et Nutrition Pediatrique, Hopital des Enfants, CH-1211 Geneva, Switzerland
  • ,
  • Susan J. Henning

      Affiliations

    • Departments of Medicine and Cell and Molecular Physiology, University of North Carolina Chapel Hill, Chapel Hill, North Carolina
  • ,
  • Milan Jamrich

      Affiliations

    • Department of Cellular and Molecular Biology, Baylor College of Medicine, Houston, Texas
    • Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas

Received 19 September 2008 ,Accepted 4 March 2009.

References 

  1. Gilbert SF. Developmental biology. Sunderland, MA: Sinauer Associates, Inc; 2000;
  2. Yasugi S. Role of epithelial-mesenchymal interactions in differentiation of epithelium of vertebrate digestive organs. Dev Growth Differ. 1993;35:1–9
  3. Roberts DJ, Smith DM, Goff DJ, et al. Epithelial-mesenchymal signaling during the regionalization of the chick gut. Development. 1998;125:2791–2801
  4. Ekker SC, McGrew LL, Lai CJ, et al. Distinct expression and shared activities of members of the hedgehog gene family of Xenopus laevis. Development. 1995;121:2337–2347
  5. Roberts DJ, Johnson RL, Burke AC, et al. Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development. 1995;121:3163–3174
  6. Bitgood MJ, McMahon AP. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev Biol. 1995;172:126–138
  7. Echelard Y, Epstein DJ, St-Jacques B, et al. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell. 1993;75:1417–1430
  8. Stolow MA, Shi YB. Xenopus sonic hedgehog as a potential morphogen during embryogenesis and thyroid hormone-dependent metamorphosis. Nucleic Acids Res. 1995;23:2555–2562
  9. Kedinger M, Simon-Assmann P, Lacroix B. [Development of the digestive function: regulation of the maturation of intestinal brush border enzymes]. Reprod Nutr Dev. 1986;26:691–702
  10. Apelqvist A, Ahlgren U, Edlund H. Sonic hedgehog directs specialised mesoderm differentiation in the intestine and pancreas. Curr Biol. 1997;7:801–804
  11. Winnier G, Blessing M, Labosky PA, et al. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 1995;9:2105–2116
  12. Wells JM, Melton DA. Vertebrate endoderm development. Annu Rev Cell Dev Biol. 1999;15:393–410
  13. Zaret KS. Regulatory phases of early liver development: paradigms of organogenesis. Nat Rev Genet. 2002;3:499–512
  14. McLin VA, Zorn AM. Molecular control of liver development. Clin Liver Dis. 2006;10:1–25v
  15. Cano DA, Hebrok M, Zenker M. Pancreatic development and disease. Gastroenterology. 2007;132:745–762
  16. Montgomery RK, Mulberg AE, Grand RJ. Development of the human gastrointestinal tract: twenty years of progress. Gastroenterology. 1999;116:702–731
  17. Joyce NC, Haire MF, Palade GE. Morphologic and biochemical evidence for a contractile cell network within the rat intestinal mucosa. Gastroenterology. 1987;92:68–81
  18. Sappino AP, Dietrich PY, Skalli O, et al. Colonic pericryptal fibroblasts (Differentiation pattern in embryogenesis and phenotypic modulation in epithelial proliferative lesions). Virchows Arch A Pathol Anat Histopathol. 1989;415:551–557
  19. Plateroti M, Rubin DC, Duluc I, et al. Subepithelial fibroblast cell lines from different levels of gut axis display regional characteristics. Am J Physiol. 1998;274:G945–G954
  20. Hall PA, Coates PJ, Ansari B, et al. Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J Cell Sci. 1994;107:3569–3577
  21. Wallace KN, Pack M. Unique and conserved aspects of gut development in zebrafish. Dev Biol. 2003;255:12–29
  22. Smith VV, Milla PJ. Histological phenotypes of enteric smooth muscle disease causing functional intestinal obstruction in childhood. Histopathology. 1997;31:112–122
  23. Hohmann B, Holzwarth M, Saur G, et al. Neonatal necrotizing enterocolitis and co-existing defect of the intestinal musculature. Eur J Pediatr. 1993;152:540–541
  24. Izraeli S, Freud E, Mor C, et al. Neonatal intestinal perforation due to congenital defects in the intestinal muscularis. Eur J Pediatr. 1992;151:300–303
  25. McHugh KM. Molecular analysis of smooth muscle development in the mouse. Dev Dyn. 1995;204:278–290
  26. McHugh KM. Molecular analysis of gastrointestinal smooth muscle development. J Pediatr Gastroenterol Nutr. 1996;23:379–394
  27. Wallace KN, Akhter S, Smith EM, et al. Intestinal growth and differentiation in zebrafish. Mech Dev. 2005;122:157–173
  28. Andrew A. The origin of intramural ganglia. II (The trunk neural crest as a source of enteric ganglion cells). J Anat. 1969;105:89–101
  29. Cochard P, Le Douarin NM. Development of the intrinsic innervation of the gut. Scand J Gastroenterol Suppl. 1982;71:1–14
  30. Gershon MD, Payette RF, Rothman TP. Development of the enteric nervous system. Fed Proc. 1983;42:1620–1625
  31. Rothman TP, Nilaver G, Gershon MD. Colonization of the developing murine enteric nervous system and subsequent phenotypic expression by the precursors of peptidergic neurons. J Comp Neurol. 1984;225:13–23
  32. Henning SJ, Rubin DC, Shulman RJ. Ontogeny of the intestinal mucosa. Raven Press; 1994;
  33. Wells JM, Melton DA. Early mouse endoderm is patterned by soluble factors from adjacent germ layers. Development. 2000;127:1563–1572
  34. Dessimoz J, Opoka R, Kordich JJ, et al. FGF signaling is necessary for establishing gut tube domains along the anterior-posterior axis in vivo. Mech Dev. 2006;123:42–55
  35. Sukegawa A, Narita T, Kameda T, et al. The concentric structure of the developing gut is regulated by Sonic hedgehog derived from endodermal epithelium. Development. 2000;127:1971–1980
  36. Tseng HT, Shah R, Jamrich M. Function and regulation of FoxF1 during Xenopus gut development. Development. 2004;131:3637–3647
  37. Zaffran S, Kuchler A, Lee HH, et al. biniou (FoxF), a central component in a regulatory network controlling visceral mesoderm development and midgut morphogenesis in Drosophila. Genes Dev. 2001;15:2900–2915
  38. Mahlapuu M, Enerback S, Carlsson P. Haploinsufficiency of the forkhead gene Foxf1, a target for sonic hedgehog signaling, causes lung and foregut malformations. Development. 2001;128:2397–2406
  39. Jakobsen JS, Braun M, Astorga J, et al. Temporal ChIP-on-chip reveals Biniou as a universal regulator of the visceral muscle transcriptional network. Genes Dev. 2007;21:2448–2460
  40. Mahlapuu M, Pelto-Huikko M, Aitola M, et al. FREAC-1 contains a cell-type-specific transcriptional activation domain and is expressed in epithelial-mesenchymal interfaces. Dev Biol. 1998;202:183–195
  41. Mahlapuu M, Ormestad M, Enerback S, et al. The forkhead transcription factor Foxf1 is required for differentiation of extra-embryonic and lateral plate mesoderm. Development. 2001;128:155–166
  42. Astorga J, Carlsson P. Hedgehog induction of murine vasculogenesis is mediated by Foxf1 and Bmp4. Development. 2007;134:3753–3761
  43. Kalinichenko VV, Zhou Y, Bhattacharyya D, et al. Haploinsufficiency of the mouse Forkhead Box f1 gene causes defects in gall bladder development. J Biol Chem. 2002;277:12369–12374
  44. Aitola M, Carlsson P, Mahlapuu M, et al. Forkhead transcription factor FoxF2 is expressed in mesodermal tissues involved in epithelio-mesenchymal interactions. Dev Dyn. 2000;218:136–149
  45. Ormestad M, Astorga J, Carlsson P. Differences in the embryonic expression patterns of mouse Foxf1 and -2 match their distinct mutant phenotypes. Dev Dyn. 2004;229:328–333
  46. Ormestad M, Astorga J, Landgren H, et al. Foxf1 and Foxf2 control murine gut development by limiting mesenchymal Wnt signaling and promoting extracellular matrix production. Development. 2006;133:833–843
  47. Sandmann T, Jensen LJ, Jakobsen JS, et al. A temporal map of transcription factor activity: mef2 directly regulates target genes at all stages of muscle development. Dev Cell. 2006;10:797–807
  48. Krauss S, Concordet JP, Ingham PW. A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell. 1993;75:1431–1444
  49. Sakiyama J, Yokouchi Y, Kuroiwa A. HoxA and HoxB cluster genes subdivide the digestive tract into morphological domains during chick development. Mech Dev. 2001;101:233–236
  50. Sakiyama J, Yokouchi Y, Kuroiwa A. Coordinated expression of Hoxb genes and signaling molecules during development of the chick respiratory tract. Dev Biol. 2000;227:12–27
  51. Grapin-Botton A, Melton DA. Endoderm development: from patterning to organogenesis. Trends Genet. 2000;16:124–130
  52. Beck F, Tata F, Chawengsaksophak K. Homeobox genes and gut development. Bioessays. 2000;22:431–441
  53. Yokouchi Y, Sakiyama J, Kuroiwa A. Coordinated expression of Abd-B subfamily genes of the HoxA cluster in the developing digestive tract of chick embryo. Dev Biol. 1995;169:76–89
  54. Stanfel MN, Moses KA, Schwartz RJ, et al. Regulation of organ development by the NKX-homeodomain factors: an NKX code. Cell Mol Biol (Noisy-le-grand). 2005;(Suppl 51):OL785–OL799
  55. Park M, Lewis C, Turbay D, et al. Differential rescue of visceral and cardiac defects in Drosophila by vertebrate tinman-related genes. Proc Natl Acad Sci U S A. 1998;95:9366–9371
  56. Zakany J, Duboule D. Hox genes and the making of sphincters. Nature. 1999;401:761–762
  57. Zacchetti G, Duboule D, Zakany J. Hox gene function in vertebrate gut morphogenesis: the case of the caecum. Development. 2007;134:3967–3973
  58. Warot X, Fromental-Ramain C, Fraulob V, et al. Gene dosage-dependent effects of the Hoxa-13 and Hoxd-13 mutations on morphogenesis of the terminal parts of the digestive and urogenital tracts. Development. 1997;124:4781–4791
  59. Goodman FR, Bacchelli C, Brady AF, et al. Novel HOXA13 mutations and the phenotypic spectrum of hand-foot-genital syndrome. Am J Hum Genet. 2000;67:197–202
  60. Goodman FR, Scambler PJ. Human HOX gene mutations. Clin Genet. 2001;59:1–11
  61. Tennyson VM, Gershon MD, Sherman DL, et al. Structural abnormalities associated with congenital megacolon in transgenic mice that overexpress the Hoxa-4 gene. Dev Dyn. 1993;198:28–53
  62. Aubin J, Dery U, Lemieux M, et al. Stomach regional specification requires Hoxa5-driven mesenchymal-epithelial signaling. Development. 2002;129:4075–4087
  63. Wang Z, Dolle P, Cardoso WV, et al. Retinoic acid regulates morphogenesis and patterning of posterior foregut derivatives. Dev Biol. 2006;297:433–445
  64. Kumar M, Jordan N, Melton D, et al. Signals from lateral plate mesoderm instruct endoderm toward a pancreatic fate. Dev Biol. 2003;259:109–122
  65. Ryan JF, Baxevanis AD. Hox, Wnt, and the evolution of the primary body axis: insights from the early-divergent phyla. Biol Direct. 2007;2:37
  66. Lohnes D. The Cdx1 homeodomain protein: an integrator of posterior signaling in the mouse. Bioessays. 2003;25:971–980
  67. Pilon N, Oh K, Sylvestre JR, et al. Cdx4 is a direct target of the canonical Wnt pathway. Dev Biol. 2006;289:55–63
  68. Pilon N, Oh K, Sylvestre JR, et al. Wnt signaling is a key mediator of Cdx1 expression in vivo. Development. 2007;134:2315–2323
  69. Deschamps J, van Nes J. Developmental regulation of the Hox genes during axial morphogenesis in the mouse. Development. 2005;132:2931–2942
  70. Mandhan P, Quan QB, Beasley S, et al. Sonic hedgehog, BMP4, and Hox genes in the development of anorectal malformations in Ethylenethiourea-exposed fetal rats. J Pediatr Surg. 2006;41:2041–2045
  71. Ramalho-Santos M, Melton DA, McMahon AP. Hedgehog signals regulate multiple aspects of gastrointestinal development. Development. 2000;127:2763–2772
  72. Madison BB, McKenna LB, Dolson D, et al. FoxF1 and FoxL1 link hedgehog signaling and the control of epithelial proliferation in the developing stomach and intestine. J Biol Chem. 2009;284:5936–5944
  73. Iafolla AK, Kahler SG. Megalencephaly in the neonatal period as the initial manifestation of glutaric aciduria type I. J Pediatr. 1989;114:1004–1006
  74. Piekarski DH, Stephens FD. The association and embryogenesis of tracheo-oesophageal and anorectal anomalies. Prog Pediatr Surg. 1976;9:63–76
  75. Nielsen C, Murtaugh LC, Chyung JC, et al. Gizzard formation and the role of Bapx1. Dev Biol. 2001;231:164–174
  76. Yasugi S, Matsushita S, Mizuno T. Gland formation induced in the allantoic and small-intestinal endoderm by the proventricular mesenchyme is not coupled with pepsinogen expression. Differentiation. 1985;30:47–52
  77. Kedinger M, Simon-Assmann P, Bouziges F, et al. Epithelial-mesenchymal interactions in intestinal epithelial differentiation. Scand J Gastroenterol Suppl. 1988;151:62–69
  78. Haffen K, Kedinger M, Simon-Assmann PM, et al. Mesenchyme-dependent differentiation of intestinal brush-border enzymes in the gizzard endoderm of the chick embryo. Prog Clin Biol Res. 1982;85:261–270
  79. Ishizuya-Oka A, Mizuno T. Intestinal cytodifferentiation in vitro of chick stomach endoderm induced by the duodenal mesenchyme. J Embryol Exp Morphol. 1984;82:163–176
  80. Roberts DJ. Molecular mechanisms of development of the gastrointestinal tract. Dev Dyn. 2000;219:109–120
  81. Goldstein AM, Brewer KC, Doyle AM, et al. BMP signaling is necessary for neural crest cell migration and ganglion formation in the enteric nervous system. Mech Dev. 2005;122:821–833
  82. Verzi MP, Stanfel MN, Moses KA, et al. Role of the homeodomain transcription factor Bapx1 in mouse distal stomach development. Gastroenterology. 2009 Jan 14;[Epub ahead of print]
  83. Kim BM, Buchner G, Miletich I, et al. The stomach mesenchymal transcription factor Barx1 specifies gastric epithelial identity through inhibition of transient Wnt signaling. Dev Cell. 2005;8:611–622
  84. Moniot B, Biau S, Faure S, et al. SOX9 specifies the pyloric sphincter epithelium through mesenchymal-epithelial signals. Development. 2004;131:3795–3804
  85. Theodosiou NA, Tabin CJ. Sox9 and Nkx2.5 determine the pyloric sphincter epithelium under the control of BMP signaling. Dev Biol. 2005;279:481–490
  86. Smith DM, Nielsen C, Tabin CJ, et al. Roles of BMP signaling and Nkx2.5 in patterning at the chick midgut-foregut boundary. Development. 2000;127:3671–3681
  87. Henning SJ, Rubin DC, Shulman RJ. Ontogeny of the intestinal mucosa. In:  LR J editors. Physiology of the gastrointestinal tract. New York, NY: Raven Press; 1994;p. 571–610
  88. Lacroix B, Kedinger M, Simon-Assmann PM, et al. Effects of human fetal gastroenteric mesenchymal cells on some developmental aspects of animal gut endoderm. Differentiation. 1984;28:129–135
  89. Ratineau C, Duluc I, Pourreyron C, et al. Endoderm- and mesenchyme-dependent commitment of the differentiated epithelial cell types in the developing intestine of rat. Differentiation. 2003;71:163–169
  90. Hayashi K, Yasugi S, Mizuno T. Pepsinogen gene transcription induced in heterologous epithelial-mesenchymal recombinations of chicken endoderms and glandular stomach mesenchyme. Development. 1988;103:725–731
  91. Rankin CT, Bunton T, Lawler AM, et al. Regulation of left-right patterning in mice by growth/differentiation factor-1. Nat Genet. 2000;24:262–265
  92. Collignon J, Varlet I, Robertson EJ. Relationship between asymmetric nodal expression and the direction of embryonic turning. Nature. 1996;381:155–158
  93. Sampath K, Cheng AM, Frisch A, et al. Functional differences among Xenopus nodal-related genes in left-right axis determination. Development. 1997;124:3293–3302
  94. Yashiro K, Saijoh Y, Sakuma R, et al. Distinct transcriptional regulation and phylogenetic divergence of human LEFTY genes. Genes Cells. 2000;5:343–357
  95. Logan M, Pagan-Westphal SM, Smith DM, et al. The transcription factor Pitx2 mediates situs-specific morphogenesis in response to left-right asymmetric signals. Cell. 1998;94:307–317
  96. Yoshioka H, Meno C, Koshiba K, et al. Pitx2, a bicoid-type homeobox gene, is involved in a lefty-signaling pathway in determination of left-right asymmetry. Cell. 1998;94:299–305
  97. Davis NM, Kurpios NA, Sun X, et al. The chirality of gut rotation derives from left-right asymmetric changes in the architecture of the dorsal mesentery. Dev Cell. 2008;15:134–145
  98. Lipscomb K, Schmitt C, Sablyak A, et al. Role for retinoid signaling in left-right asymmetric digestive organ morphogenesis. Dev Dyn. 2006;235:2266–2275
  99. El-Mounayri O, Triplett JW, Yates CW, et al. Regulation of smooth muscle-specific gene expression by homeodomain proteins, Hoxa10 and Hoxb8. J Biol Chem. 2005;280:25854–25863
  100. Louvard D, Kedinger M, Hauri HP. The differentiating intestinal epithelial cell: establishment and maintenance of functions through interactions between cellular structures. Annu Rev Cell Biol. 1992;8:157–195
  101. Kedinger M, Simon-Assmann PM, Lacroix B, et al. Fetal gut mesenchyme induces differentiation of cultured intestinal endodermal and crypt cells. Dev Biol. 1986;113:474–483
  102. Wang LC, Nassir F, Liu ZY, et al. Disruption of hedgehog signaling reveals a novel role in intestinal morphogenesis and intestinal-specific lipid metabolism in mice. Gastroenterology. 2002;122:469–482
  103. Madison BB, Braunstein K, Kuizon E, et al. Epithelial hedgehog signals pattern the intestinal crypt-villus axis. Development. 2005;132:279–289
  104. Mishina Y. Function of bone morphogenetic protein signaling during mouse development. Front Biosci. 2003;8:d855–d869
  105. Faure S, de Santa Barbara P, Roberts DJ, et al. Endogenous patterns of BMP signaling during early chick development. Dev Biol. 2002;244:44–65
  106. De Santa Barbara P, Williams J, Goldstein AM, et al. Bone morphogenetic protein signaling pathway plays multiple roles during gastrointestinal tract development. Dev Dyn. 2005;234:312–322
  107. Batts LE, Polk DB, Dubois RN, et al. Bmp signaling is required for intestinal growth and morphogenesis. Dev Dyn. 2006;235:1563–1570
  108. He XC, Zhang J, Tong WG, et al. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat Genet. 2004;36:1117–1121
  109. Auclair BA, Benoit YD, Rivard N, et al. Bone morphogenetic protein signaling is essential for terminal differentiation of the intestinal secretory cell lineage. Gastroenterology. 2007;133:887–896
  110. Haramis AP, Begthel H, van den Born M, et al. De novo crypt formation and juvenile polyposis on BMP inhibition in mouse intestine. Science. 2004;303:1684–1686
  111. Ishizuya-Oka A, Hasebe T, Shimizu K, et al. Shh/BMP-4 signaling pathway is essential for intestinal epithelial development during Xenopus larval-to-adult remodeling. Dev Dyn. 2006;235:3240–3249
  112. Ishizuya-Oka A, Ueda S, Amano T, et al. Thyroid-hormone-dependent and fibroblast-specific expression of BMP-4 correlates with adult epithelial development during amphibian intestinal remodeling. Cell Tissue Res. 2001;303:187–195
  113. Pinto D, Clevers H. Wnt control of stem cells and differentiation in the intestinal epithelium. Exp Cell Res. 2005;306:357–363
  114. Pinto D, Clevers H. Wnt, stem cells and cancer in the intestine. Biol Cell. 2005;97:185–196
  115. Pinto D, Gregorieff A, Begthel H, et al. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev. 2003;17:1709–1713
  116. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell. 2006;127:469–480
  117. van Es JH, Jay P, Gregorieff A, et al. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol. 2005;7:381–386
  118. Andoh A, Bamba S, Brittan M, et al. Role of intestinal subepithelial myofibroblasts in inflammation and regenerative response in the gut. Pharmacol Ther. 2007;114:94–106
  119. Gregorieff A, Pinto D, Begthel H, et al. Expression pattern of Wnt signaling components in the adult intestine. Gastroenterology. 2005;129:626–638
  120. Theodosiou NA, Tabin CJ. Wnt signaling during development of the gastrointestinal tract. Dev Biol. 2003;259:258–271
  121. Muncan V, Faro A, Haramis AP, et al. T-cell factor 4 (Tcf7l2) maintains proliferative compartments in zebrafish intestine. EMBO Rep. 2007;8:966–973
  122. Barker N, Huls G, Korinek V, et al. Restricted high level expression of Tcf-4 protein in intestinal and mammary gland epithelium. Am J Pathol. 1999;154:29–35
  123. Booth C, Brady G, Potten CS. Crowd control in the crypt. Nat Med. 2002;8:1360–1361
  124. Kim BM, Mao J, Taketo MM, et al. Phases of canonical Wnt signaling during the development of mouse intestinal epithelium. Gastroenterology. 2007;133:529–538
  125. Cervantes S, Yamaguchi TP, Hebrok M. Wnt5a is essential for intestinal elongation in mice. Dev Biol. 2009;326:285–294
  126. Geske MJ, Zhang X, Patel KK, et al. Fgf9 signaling regulates small intestinal elongation and mesenchymal development. Development. 2008;135:2959–2968
  127. Kaestner KH, Silberg DG, Traber PG, et al. The mesenchymal winged helix transcription factor Fkh6 is required for the control of gastrointestinal proliferation and differentiation. Genes Dev. 1997;11:1583–1595
  128. Perreault N, Sackett SD, Katz JP, et al. Foxl1 is a mesenchymal Modifier of Min in carcinogenesis of stomach and colon. Genes Dev. 2005;19:311–315
  129. Katz JP, Perreault N, Goldstein BG, et al. Foxl1 null mice have abnormal intestinal epithelia, postnatal growth retardation, and defective intestinal glucose uptake. Am J Physiol Gastrointest Liver Physiol. 2004;287:G856–G864
  130. Oka T, Shiojima I, Monzen K, et al. Fibroblast growth factor plays a critical role in SM22alpha expression during Xenopus embryogenesis. Arterioscler Thromb Vasc Biol. 2000;20:907–914
  131. Saint-Jeannet JP, Thiery JP, Koteliansky VE. Effect of an inhibitory mutant of the FGF receptor on mesoderm-derived alpha-smooth muscle actin-expressing cells in Xenopus embryo. Dev Biol. 1994;164:374–382
  132. Li X, Madison BB, Zacharias W, et al. Deconvoluting the intestine: molecular evidence for a major role of the mesenchyme in the modulation of signaling cross talk. Physiol Genomics. 2007;29:290–301
  133. Vidrich A, Buzan JM, Ilo C, et al. Fibroblast growth factor receptor-3 is expressed in undifferentiated intestinal epithelial cells during murine crypt morphogenesis. Dev Dyn. 2004;230:114–123
  134. Zhang X, Stappenbeck TS, White AC, et al. Reciprocal epithelial-mesenchymal FGF signaling is required for cecal development. Development. 2006;133:173–180
  135. Shulman RJ, Schanler RJ, Lau C, et al. Early feeding, antenatal glucocorticoids, and human milk decrease intestinal permeability in preterm infants. Pediatr Res. 1998;44:519–523
  136. Stallmach A, Hahn U, Merker HJ, et al. Differentiation of rat intestinal epithelial cells is induced by organotypic mesenchymal cells in vitro. Gut. 1989;30:959–970
  137. Kedinger M, Simon-Assmann P, Alexandre E, et al. Importance of a fibroblastic support for in vitro differentiation of intestinal endodermal cells and for their response to glucocorticoids. Cell Differ. 1987;20:171–182
  138. Foltzer-Jourdainne C, Kedinger M, Raul F. Perinatal expression of brush-border hydrolases in rat colon: hormonal and tissue regulations. Am J Physiol. 1989;257:G496–G503
  139. Walsh MJ, LeLeiko NS, Sterling KM. Regulation of types I, III, and IV procollagen mRNA synthesis in glucocorticoid-mediated intestinal development. J Biol Chem. 1987;262:10814–10818
  140. Simon-Assmann P, Kedinger M, De Arcangelis A, et al. Extracellular matrix components in intestinal development. Experientia. 1995;51:883–900
  141. Weiser MM, Sykes DE, Killen PD. Rat intestinal basement membrane synthesis: Epithelial versus nonepithelial contributions. Lab Invest. 1990;62:325–330
  142. Simo P, Simon-Assmann P, Arnold C, et al. Mesenchyme-mediated effect of dexamethasone on laminin in cocultures of embryonic gut epithelial cells and mesenchyme-derived cells. J Cell Sci. 1992;101:161–171
  143. Solomon NS, Gartner H, Oesterreicher TJ, Henning SJ. Development of glucocorticoid-responsiveness in mouse intestine. Pediatr Res. 2001;49:782–788
  144. Gartner H, Graul MC, Oesterreicher TJ, et al. Development of the fetal intestine in mice lacking the glucocorticoid receptor (GR). J Cell Physiol. 2003;194:80–87
  145. Fraichard A, Chassande O, Plateroti M, et al. The T3R alpha gene encoding a thyroid hormone receptor is essential for post-natal development and thyroid hormone production. EMBO J. 1997;16:4412–4420
  146. Schreiber AM, Cai L, Brown DD. Remodeling of the intestine during metamorphosis of Xenopus laevis. Proc Natl Acad Sci U S A. 2005;102:3720–3725
  147. Leeper LL, McDonald MC, Heath JP, et al. Sucrase-isomaltase ontogeny: synergism between glucocorticoids and thyroxine reflects increased mRNA and no change in cell migration. Biochem Biophys Res Commun. 1998;246:765–770
  148. McDonald MC, Henning SJ. Synergistic effects of thyroxine and dexamethasone on enzyme ontogeny in rat small intestine. Pediatr Res. 1992;32:306–311
  149. Su Y, Shi Y, Shi YB. Cyclosporin A but not FK506 inhibits thyroid hormone-induced apoptosis in tadpole intestinal epithelium. FASEB J. 1997;11:559–565
  150. Su Y, Shi Y, Stolow MA, et al. Thyroid hormone induces apoptosis in primary cell cultures of tadpole intestine: cell type specificity and effects of extracellular matrix. J Cell Biol. 1997;139:1533–1543
  151. Ishizuya-Oka A, Shi YB. Regulation of adult intestinal epithelial stem cell development by thyroid hormone during Xenopus laevis metamorphosis. Dev Dyn. 2007;236:3358–3368
  152. Quasnichka H, Slater SC, Beeching CA, et al. Regulation of smooth muscle cell proliferation by beta-catenin/T-cell factor signaling involves modulation of cyclin D1 and p21 expression. Circ Res. 2006;99:1329–1337
  153. Karlsson L, Lindahl P, Heath JK, et al. Abnormal gastrointestinal development in PDGF-A and PDGFR-(alpha) deficient mice implicates a novel mesenchymal structure with putative instructive properties in villus morphogenesis. Development. 2000;127:3457–3466
  154. Hirota S, Isozaki K, Moriyama Y, et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science. 1998;279:577–580
  155. Taniguchi M, Nishida T, Hirota S, et al. Effect of c-kit mutation on prognosis of gastrointestinal stromal tumors. Cancer Res. 1999;59:4297–4300
  156. Rubin BP. Gastrointestinal stromal tumours: an update. Histopathology. 2006;48:83–96
  157. Heinrich MC, Rubin BP, Longley BJ, et al. Biology and genetic aspects of gastrointestinal stromal tumors: KIT activation and cytogenetic alterations. Hum Pathol. 2002;33:484–495
  158. Heinrich MC, Corless CL, Duensing A, et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science. 2003;299:708–710
  159. MacDonald RS. The role of insulin-like growth factors in small intestinal cell growth and development. Horm Metab Res. 1999;31:103–113
  160. Michaylira CZ, Simmons JG, Ramocki NM, et al. Suppressor of cytokine signaling-2 limits intestinal growth and enterotrophic actions of IGF-I in vivo. Am J Physiol Gastrointest Liver Physiol. 2006;291:G472–G481
  161. Fukamachi H, Narita T, Yahagi N, et al. Endothelin-3 controls growth of colonic epithelial cells by mediating epithelial-mesenchymal interaction. Dev Growth Differ. 2005;47:573–580
  162. Wang Y, Wang L, Iordanov H, et al. Epimorphin(−/−) mice have increased intestinal growth, decreased susceptibility to dextran sodium sulfate colitis, and impaired spermatogenesis. J Clin Invest. 2006;116:1535–1546
  163. Hirai Y, Takebe K, Takashina M, et al. Epimorphin: a mesenchymal protein essential for epithelial morphogenesis. Cell. 1992;69:471–481
  164. Wallace KN, Dolan AC, Seiler C, et al. Mutation of smooth muscle myosin causes epithelial invasion and cystic expansion of the zebrafish intestine. Dev Cell. 2005;8:717–726
  165. Timpl R, Brown JC. Supramolecular assembly of basement membranes. Bioessays. 1996;18:123–132
  166. Shi YB, Fu L, Hasebe T, et al. Regulation of extracellular matrix remodeling and cell fate determination by matrix metalloproteinase stromelysin-3 during thyroid hormone-dependent post-embryonic development. Pharmacol Ther. 2007;116:391–400
  167. El-Hodiri H, Bhatia-Dey N, Kenyon K, et al. Fox (forkhead) genes are involved in the dorso-ventral patterning of the Xenopus mesoderm. Int J Dev Biol. 2001;45:265–271
  168. Frasch M. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature. 1995;374:464–467
  169. Lee HH, Frasch M. Nuclear integration of positive Dpp signals, antagonistic Wg inputs and mesodermal competence factors during Drosophila visceral mesoderm induction. Development. 2005;132:1429–1442
  170. Stickney HL, Imai Y, Draper B, et al. Zebrafish bmp4 functions during late gastrulation to specify ventroposterior cell fates. Dev Biol. 2007;310:71–84
  171. McMahon JA, Takada S, Zimmerman LB, et al. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 1998;12:1438–1452
  172. Monsoro-Burq AH, Duprez D, Watanabe Y, et al. The role of bone morphogenetic proteins in vertebral development. Development. 1996;122:3607–3616
  173. Xue L, Chen X, Chang Y, et al. Regulatory elements of the EKLF gene that direct erythroid cell-specific expression during mammalian development. Blood. 2004;103:4078–4083
  174. Davidson AJ, Zon LI. Turning mesoderm into blood: the formation of hematopoietic stem cells during embryogenesis. Curr Top Dev Biol. 2000;50:45–60
  175. Dosch R, Gawantka V, Delius H, et al. Bmp-4 acts as a morphogen in dorsoventral mesoderm patterning in Xenopus. Development. 1997;124:2325–2334
  176. Onichtchouk D, Glinka A, Niehrs C. Requirement for Xvent-1 and Xvent-2 gene function in dorsoventral patterning of Xenopus mesoderm. Development. 1998;125:1447–1456
  177. Ault KT, Dirksen ML, Jamrich M. A novel homeobox gene PV.1 mediates induction of ventral mesoderm in Xenopus embryos. Proc Natl Acad Sci U S A. 1996;93:6415–6420
  178. Onichtchouk D, Gawantka V, Dosch R, et al. The Xvent-2 homeobox gene is part of the BMP-4 signalling pathway controlling [correction of controling] dorsoventral patterning of Xenopus mesoderm. Development. 1996;122:3045–3053
  179. Kozmik Z, Holland LZ, Schubert M, et al. Characterization of Amphioxus AmphiVent, an evolutionarily conserved marker for chordate ventral mesoderm. Genesis. 2001;29:172–179
  180. Bienz M, Tremml G. Domain of Ultrabithorax expression in Drosophila visceral mesoderm from autoregulation and exclusion. Nature. 1988;333:576–578
  181. Jagla K, Bellard M, Frasch M. A cluster of Drosophila homeobox genes involved in mesoderm differentiation programs. Bioessays. 2001;23:125–133
  182. Azpiazu N, Frasch M. tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev. 1993;7:1325–1340
  183. Azpiazu N, Lawrence PA, Vincent JP, et al. Segmentation and specification of the Drosophila mesoderm. Genes Dev. 1996;10:3183–3194
  184. Lo PC, Frasch M. bagpipe-Dependent expression of vimar, a novel Armadillo-repeats gene, in Drosophila visceral mesoderm. Mech Dev. 1998;72:65–75
  185. Newman CS, Grow MW, Cleaver O, et al. Xbap, a vertebrate gene related to bagpipe, is expressed in developing craniofacial structures and in anterior gut muscle. Dev Biol. 1997;181:223–233
  186. Newman CS, Krieg PA. The Xenopus bagpipe-related homeobox gene zampogna is expressed in the pharyngeal endoderm and the visceral musculature of the midgut. Dev Genes Evol. 1999;209:132–134
  187. Nieuwkoop D, Faber J. Normal table of Xenopus laevis (Daudin). New York, NY: Garland Publishing Inc; 1994;
  188. Horb ME. Patterning the endoderm: the importance of neighbours. Bioessays. 2000;22:599–602
  189. Horb ME, Slack JM. Endoderm specification and differentiation in Xenopus embryos. Dev Biol. 2001;236:330–343
  190. Swindell EC, Eichele G. Retinoid metabolizing enzymes in development. Biofactors. 1999;10:85–89
  191. McLin VA, Rankin SA, Zorn AM. Repression of Wnt/beta-catenin signaling in the anterior endoderm is essential for liver and pancreas development. Development. 2007;134:2207–2217
  192. Glinka A, Wu W, Onichtchouk D, et al. Head induction by simultaneous repression of Bmp and Wnt signalling in Xenopus. Nature. 1997;389:517–519
  193. Okubo T, Hogan BL. Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J Biol. 2004;3:11
  194. Crosnier C, Stamataki D, Lewis J. Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet. 2006;7:349–359
  195. Lints TJ, Hartley L, Parsons LM, et al. Mesoderm-specific expression of the divergent homeobox gene Hlx during murine embryogenesis. Dev Dyn. 1996;205:457–470
  196. Bates MD, Schatzman LC, Lints T, et al. Structural and functional characterization of the mouse Hlx homeobox gene. Mamm Genome. 2000;11:836–842
  197. Hentsch B, Lyons I, Li R, et al. Hlx homeo box gene is essential for an inductive tissue interaction that drives expansion of embryonic liver and gut. Genes Dev. 1996;10:70–79
  198. Pabst O, Schneider A, Brand T, et al. The mouse Nkx2-3 homeodomain gene is expressed in gut mesenchyme during pre- and postnatal mouse development. Dev Dyn. 1997;209:29–35
  199. Buchberger A, Pabst O, Brand T, et al. Chick NKx-2.3 represents a novel family member of vertebrate homologues to the Drosophila homeobox gene tinman: differential expression of cNKx-2.3 and cNKx-2.5 during heart and gut development. Mech Dev. 1996;56:151–163

 Conflicts of interest The authors disclose no conflicts.

 Funding V.A.M. is supported by the National Institutes of Health (K08DK078656) and a Young Investigator Award from the Children's Digestive Health and Nutrition Foundation, S.J.H. is supported by the National Institutes of Health (R01DK069585), and M.J. is supported by the Retinal Research Foundation.

PII: S0016-5085(09)00370-9

doi: 10.1053/j.gastro.2009.03.001

Gastroenterology
Volume 136, Issue 7 , Pages 2074-2091 , June 2009