Key Role of the Cdx2 Homeobox Gene in Extracellular Matrix-mediated Intestinal Cell Differentiation

doi:10.1083/jcb.139.6.1553

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© The Rockefeller University Press, 0021-9525/1997//1553 $5.00
The Journal of Cell Biology, Volume 139, Number 6, , 1997 1553-1565

Article

Key Role of the Cdx2 Homeobox Gene in Extracellular Matrix–mediated Intestinal Cell Differentiation

Olivier Lorentz, Isabelle Duluc, Adèle De Arcangelis, Patricia Simon-Assmann, Michèle Kedinger, and Jean-Noël Freund

Institut National de la Santé et de la Recherche Médicale, Unité 381, 67200 Strasbourg, France

To explore the role of homeobox genes in the intestine, thehuman colon adenocarcinoma cell line Caco2-TC7 has been stablytransfected with plasmids synthesizing Cdx1 and Cdx2 senseand antisense RNAs. Cdx1 overexpression or inhibition by antisenseRNA does not markedly modify the cell differentiation markersanalyzed in this study. In contrast, Cdx2 overexpression stimulatestwo typical markers of enterocytic differentiation: sucrase-isomaltaseand lactase. Cells in which the endogenous expression of Cdx2is reduced by antisense RNA attach poorly to the substratum.Conversely, Cdx2 overexpression modifies the expression ofmolecules involved in cell–cell and cell–substratum interactions and in transduction process: indeed, E-cadherin,integrin-β4 subunit, laminin- ${gamma}$ 2 chain, hemidesmosomal protein,APC, and ${alpha}$ -actinin are upregulated. Interestingly, most of thesemolecules are preferentially expressed in vivo in the differentiatedvilli enterocytes rather than in crypt cells. Cdx2 overexpressionalso results in the stimulation of HoxA-9 mRNA expression, an homeobox gene selectively expressed in the colon. In contrast,Cdx2-overexpressing cells display a decline of Cdx1 mRNA, whichis mostly found in vivo in crypt cells. When implanted in nudemice, Cdx2-overexpressing cells produce larger tumors than controlcells, and form glandular and villus-like structures.

Laminin-1 is known to stimulate intestinal cell differentiationin vitro. In the present study, we demonstrate that the differentiatingeffect of laminin-1 coatings on Caco2-TC7 cells is accompaniedby an upregulation of Cdx2. To further document this observation,we analyzed a series of Caco2 clones in which the production of laminin- ${alpha}$ 1 chain is differentially inhibited by antisenseRNA. We found a positive correlation between the level of Cdx2expression, that of endogenous laminin- ${alpha}$ 1 chain mRNA and thatof sucrase-isomaltase expression in these cell lines.

Taken together, these results suggest (a) that Cdx1 and Cdx2homeobox genes play distinct roles in the intestinal epithelium,(b) that Cdx2 provokes pleiotropic effects triggering cellstowards the phenotype of differentiated villus enterocytes,and (c) that Cdx2 expression is modulated by basement membranecomponents. Hence, we conclude that Cdx2 plays a key role inthe extracellular matrix–mediated intestinal cell differentiation.

Abbreviations used in this paper: EHS, Engelbreth-Holms-Swarm; FAK, focal adhesion kinase; HD1, component of hemidesmosome; LPH, lactase-phlorizin hydrolase; RT-PCR, reverse transcriptase-polymerase chain reaction; SI, sucrase-isomaltase.

Address all correspondence to Dr. Jean-Noël Freund, INSERM,Unité 381, 3 avenue Molière, 67200 Strasbourg,France. Tel.: (33) 388 27 77 27. Fax: (33) 388 26 35 38. E-mail:jean-noel.freund{at}inserm.u-strasbg.fr

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