The mouse ileal lipid-binding protein gene: a model for studying axial patterning during gut morphogenesis

doi:10.1083/jcb.126.6.1547

This Article

	Full Text (PDF, 9407K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Crossman, M. W.
	Articles by Gordon, J. I.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Crossman, M. W.
	Articles by Gordon, J. I.


Social Bookmarking

	What's this?

ARTICLES

The mouse ileal lipid-binding protein gene: a model for studying axial patterning during gut morphogenesis

MW Crossman, SM Hauft and JI Gordon
Department of Molecular Biology, and Pharmacology, Washington University School of Medicine, St. Louis, Missouri 63110.

Normal, chimeric-transgenic, and transgenic mice have been used to study the axial patterns of ileal lipid-binding protein gene (Ilbp) expression during and after completion of gut morphogenesis. Ilbp is initially activated in enterocytes in bidirectional wave that expands proximally in the ileum and distally to the colon during late gestation and the first postnatal week. This activation occurs at the same time that a wave of cytodifferentiation of the gut endoderm is completing its unidirectional journey from duodenum to colon. The subsequent contraction of Ilbp's expression domain, followed by its reexpansion from the distal to proximal ileum, coincides with a critical period in gut morphogenesis (postnatal days 7-28) when its proliferative units (crypts) form, establish their final stem cell hierarchy, and then multiply through fission. The wave of reactivation is characterized by changing patterns of Ilbp expression: (a) at the proximal most boundary of the wave, villi contain a mixed population of scattered ileal lipid- binding protein (ILBP)-positive and ILBP-negative enterocytes derived from the same monoclonal crypt; (b) somewhat more distally, villi contain vertical coherent stripes of wholly ILBP-positive enterocytes derived from monoclonal crypts and adjacent, wholly ILBP-negative stripes of enterocytes emanating from other monoclonal crypts; and (c) more distally, all the enterocytes on a villus support Ilbp expression. Functional mapping studies of Ilbp's promoter in transgenic mice indicate that nucleotides -145 to +48 contain cis-acting elements sufficient to produce an appropriately directed distal-to-proximal wave of Ilbp activation in the ileum, to maintain an appropriate axial distribution of monophenotypic wholly reporter-positive villi in the distal portion of the ileum, as well as striped and speckled villi in the proximal portion of its expression domain, and to correctly support reporter production in villus-associated ileal enterocytes. Nucleotides -417 to -146 of Ilbp contain a "temporal" suppressor that delays initial ileal activation of the gene until the second postnatal week. Nucleotides -913 to -418 contain a temporal suppressor that further delays initial activation of the gene until the third to fourth postnatal week, a spatial suppressor that prohibits gene expression in the proximal quarter of the ileum and in the proximal colon, and a cell lineage suppressor that prohibits expression in goblet cells during the first two postnatal weeks.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Bosse, T., Piaseckyj, C. M., Burghard, E., Fialkovich, J. J., Rajagopal, S., Pu, W. T., Krasinski, S. D. (2006). Gata4 Is Essential for the Maintenance of Jejunal-Ileal Identities in the Adult Mouse Small Intestine. Mol. Cell. Biol. 26: 9060-9070 [Abstract] [Full Text]
Chen, X., Chen, F., Liu, S., Glaeser, H., Dawson, P. A., Hofmann, A. F., Kim, R. B., Shneider, B. L., Pang, K. S. (2006). Transactivation of Rat Apical Sodium-Dependent Bile Acid Transporter and Increased Bile Acid Transport by 1{alpha},25-Dihydroxyvitamin D3 via the Vitamin D Receptor. Mol. Pharmacol. 69: 1913-1923 [Abstract] [Full Text]
Bettess, M. D., Dubois, N., Murphy, M. J., Dubey, C., Roger, C., Robine, S., Trumpp, A. (2005). c-Myc Is Required for the Formation of Intestinal Crypts but Dispensable for Homeostasis of the Adult Intestinal Epithelium. Mol. Cell. Biol. 25: 7868-7878 [Abstract] [Full Text]
Vidrich, A., Buzan, J. M., Barnes, S., Reuter, B. K., Skaar, K., Ilo, C., Cominelli, F., Pizarro, T., Cohn, S. M. (2005). Altered Epithelial Cell Lineage Allocation and Global Expansion of the Crypt Epithelial Stem Cell Population Are Associated with Ileitis in SAMP1/YitFc Mice. Am. J. Pathol. 166: 1055-1067 [Abstract] [Full Text]
Campbell, S. J., Henderson, C. J., Anthony, D. C., Davidson, D., Clark, A. J., Wolf, C. R. (2005). The Murine Cyp1a1 Gene Is Expressed in a Restricted Spatial and Temporal Pattern during Embryonic Development. J. Biol. Chem. 280: 5828-5835 [Abstract] [Full Text]
Sauvaget, D., Chauffeton, V., Citadelle, D., Chatelet, F.-P., Cywiner-Golenzer, C., Chambaz, J., Pincon-Raymond, M., Cardot, P., Le Beyec, J., Ribeiro, A. (2002). Restriction of Apolipoprotein A-IV Gene Expression to the Intestine Villus Depends on a Hormone-responsive Element and Parallels Differential Expression of the Hepatic Nuclear Factor 4alpha and gamma Isoforms. J. Biol. Chem. 277: 34540-34548 [Abstract] [Full Text]
Madison, B. B., Dunbar, L., Qiao, X. T., Braunstein, K., Braunstein, E., Gumucio, D. L. (2002). cis Elements of the Villin Gene Control Expression in Restricted Domains of the Vertical (Crypt) and Horizontal (Duodenum, Cecum) Axes of the Intestine. J. Biol. Chem. 277: 33275-33283 [Abstract] [Full Text]
Lee, S. Y., Wang, Z., Lin, C.-K., Contag, C. H., Olds, L. C., Cooper, A. D., Sibley, E. (2002). Regulation of Intestine-specific Spatiotemporal Expression by the Rat Lactase Promoter. J. Biol. Chem. 277: 13099-13105 [Abstract] [Full Text]
Chen, F., Ma, L., Al-Ansari, N., Shneider, B. (2001). The Role of AP-1 in the Transcriptional Regulation of the Rat Apical Sodium-dependent Bile Acid Transporter. J. Biol. Chem. 276: 38703-38714 [Abstract] [Full Text]
Hwang, S. T., Henning, S. J. (2001). Ontogenic Regulation of Components of Ileal Bile AcidAbsorption. Exp. Biol. Med. 226: 674-680 [Abstract] [Full Text]
Hwang, S. T., Henning, S. J. (2000). Hormonal regulation of expression of ileal bile acid binding protein in suckling rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278: R1555-R1563 [Abstract] [Full Text]
WALTERS, J R F (2000). Bile acids are physiological ligands for a nuclear receptor. Gut 46: 308-309 [Full Text]
Xu, G., Shneider, B. L., Shefer, S., Nguyen, L. B., Batta, A. K., Tint, G. S., Arrese, M., Thevananther, S., Ma, L., Stengelin, S., Kramer, W., Greenblatt, D., Pcolinsky, M., Salen, G. (2000). Ileal bile acid transport regulates bile acid pool, synthesis, and plasma cholesterol levels differently in cholesterol-fed rats and rabbits. J. Lipid Res. 41: 298-304 [Abstract] [Full Text]
Saam, J. R., Gordon, J. I. (1999). Inducible Gene Knockouts in the Small Intestinal and Colonic Epithelium. J. Biol. Chem. 274: 38071-38082 [Abstract] [Full Text]
Grober, J., Zaghini, I., Fujii, H., Jones, S. A., Kliewer, S. A., Willson, T. M., Ono, T., Besnard, P. (1999). Identification of a Bile Acid-responsive Element in the Human Ileal Bile Acid-binding Protein Gene. INVOLVEMENT OF THE FARNESOID X RECEPTOR/9-cis-RETINOIC ACID RECEPTOR HETERODIMER. J. Biol. Chem. 274: 29749-29754 [Abstract] [Full Text]
Makishima, M., Okamoto, A. Y., Repa, J. J., Tu, H., Learned, R. M., Luk, A., Hull, M. V., Lustig, K. D., Mangelsdorf, D. J., Shan, B. (1999). Identification of a Nuclear Receptor for Bile Acids. Science 284: 1362-1365 [Abstract] [Full Text]
Pinto, D., Robine, S., Jaisser, F., Marjou, F. E., Louvard, D. (1999). Regulatory Sequences of the Mouse Villin Gene That Efficiently Drive Transgenic Expression in Immature and Differentiated Epithelial Cells of Small and Large Intestines. J. Biol. Chem. 274: 6476-6482 [Abstract] [Full Text]
Le Beyec, J., Chauffeton, V., Kan, H.-Y., Janvier, P.-L., Cywiner-Golenzer, C., Chatelet, F.-P., Kalopissis, A. D., Zannis, V., Chambaz, J., Pincon-Raymond, M., Cardot, P. (1999). The -700/-310 Fragment of the Apolipoprotein A-IV Gene Combined with the -890/-500 Apolipoprotein C-III Enhancer Is Sufficient to Direct a Pattern of Gene Expression Similar to That for the Endogenous Apolipoprotein A-IV Gene. J. Biol. Chem. 274: 4954-4961 [Abstract] [Full Text]
Slorach, E., Campbell, F., Dorin, J. (1999). A mouse model of intestinal stem cell function and regeneration. J. Cell Sci. 112: 3029-3038 [Abstract]
Falk, P. G., Hooper, L. V., Midtvedt, T., Gordon, J. I. (1998). Creating and Maintaining the Gastrointestinal Ecosystem: What We Know and Need To Know from Gnotobiology. Microbiol. Mol. Biol. Rev. 62: 1157-1170 [Abstract] [Full Text]
Colnot, S., Romagnolo, B., Lambert, M., Cluzeaud, F., Porteu, A., Vandewalle, A., Thomasset, M., Kahn, A., Perret, C. (1998). Intestinal Expression of the Calbindin-D9K Gene in Transgenic Mice. REQUIREMENT FOR A Cdx2-BINDING SITE IN A DISTAL ACTIVATOR REGION. J. Biol. Chem. 273: 31939-31946 [Abstract] [Full Text]
Nielsen, L. B., McCormick, S. P.�A., Pierotti, V., Tam, C., Gunn, M. D., Shizuya, H., Young, S. G. (1997). Human Apolipoprotein B Transgenic Mice Generated with 207-�and 145-Kilobase Pair Bacterial Artificial Chromosomes. EVIDENCE THAT A DISTANT 5'-ELEMENT CONFERS APPROPRIATE TRANSGENE EXPRESSION IN THE INTESTINE. J. Biol. Chem. 272: 29752-29758 [Abstract] [Full Text]
Simon, T. C., Cho, A., Tso, P., Gordon, J. I. (1997). Suppressor and Activator Functions Mediated by a Repeated Heptad Sequence in the Liver Fatty Acid-binding Protein Gene (Fabpl). EFFECTS ON RENAL, SMALL INTESTINAL, AND COLONIC EPITHELIAL CELL GENE EXPRESSION IN TRANSGENIC MICE. J. Biol. Chem. 272: 10652-10663 [Abstract] [Full Text]
Duluc, I, Lorentz, O, Fritsch, C, Leberquier, C, Kedinger, M, Freund, J. (1997). Changing intestinal connective tissue interactions alters homeobox gene expression in epithelial cells. J. Cell Sci. 110: 1317-1324 [Abstract]
Romagnolo, B., Cluzeaud, F., Lambert, M., Colnot, S., Porteu, A., Molina, T., Tomasset, M., Vandewalle, A., Kahn, A., Perret, C. (1996). Tissue-specific and Hormonal Regulation of Calbindin-D9K Fusion Genes in Transgenic Mice. J. Biol. Chem. 271: 16820-16826 [Abstract] [Full Text]
Hermiston, M L, Wong, M H, Gordon, J I (1996). Forced expression of E-cadherin in the mouse intestinal epithelium slows cell migration and provides evidence for nonautonomous regulation of cell fate in a self-renewing system.. Genes Dev. 10: 985-996 [Abstract]
Bisaha, J. G., Simon, T. C., Gordon, J. I., Breslow, J. L. (1995). Characterization of an Enhancer Element in the Human Apolipoprotein C-III Gene That Regulates Human Apolipoprotein A-I Gene Expression in the Intestinal Epithelium. J. Biol. Chem. 270: 19979-19988 [Abstract] [Full Text]
Kramer, W., Sauber, K., Baringhaus, K.-H., Kurz, M., Stengelin, S., Lange, G., Corsiero, D., Girbig, F., Konig, W., Weyland, C. (2001). Identification of the Bile Acid-binding Site of the Ileal Lipid-binding Protein by Photoaffinity Labeling, Matrix-assisted Laser Desorption Ionization-Mass Spectrometry, and NMR Structure. J. Biol. Chem. 276: 7291-7301 [Abstract] [Full Text]
Lu, T. T., Repa, J. J., Mangelsdorf, D. J. (2001). Orphan Nuclear Receptors as eLiXiRs and FiXeRs of Sterol Metabolism. J. Biol. Chem. 276: 37735-37738 [Full Text]