Background & Aims: Intestinal lactase activity declines during childhood in some humans. This phenotypic polymorphism of lactase persistence or nonpersistence into adult life has been shown in a recent study to be 100% associated with a T/C nucleotide polymorphism at position −13910 and approximately 97% with an A/G nucleotide polymorphism at position −22018. The aim of this study was to investigate the role of these nucleotide polymorphisms for lactase-phlorizin hydrolase (LPH) gene expression. Methods: The −13910 and −22018 regions were cloned from lactase-persistent and -nonpersistent individuals, and the regions were analyzed for gene regulatory activity of a luciferase reporter gene by transfection experiments using the intestinal cell line Caco-2. Electrophoretic mobility shift assays (EMSAs) were used to investigate protein/DNA interactions with the −13910 sequence. Results: We show that the −13910 region contains a strong enhancer. The −13910 regions from both lactase persistent (−13910T variant) and lactase nonpersistent (−13910C variant) have enhancer activity. However, the −13910T variant enhances the LPH promoter approximately 4 times more than the −13910C variant when analyzed in differentiated Caco-2 cells. A nuclear factor from both an intestinal and a nonintestinal extract binds strongly to the −13910T variant whereas the binding to the −13910C variant is much weaker. Conclusions: The discovery of a functional difference between the 2 alleles at position −13910 supports the notion that the molecular difference between lactase persistence and nonpersistence is caused by the mutation at position −13910.
Two phenotypes exist in the human population with regard to expression of lactase in adults. Lactase non-persistence (adult-type hypolactasia and lactose intolerance) is characterized by a decline in the expression of lactase-phlorizin hydrolase (LPH) after weaning. In contrast, lactase-persistent individuals have a high LPH throughout their lifespan. Lactase persistence and non-persistence are associated with a T/C polymorphism at position −13 910 upstream the lactase gene. A nuclear factor binds more strongly to the T −13 910 variant associated with lactase persistence than the C −13 910 variant associated with lactase non-persistence. Oct-1 and glyceraldehyde-3-phosphate dehydrogenase were co-purified by DNA affinity purification using the sequence of the T −13 910 variant. Supershift analyses show that Oct-1 binds directly to the T −13 910 variant, and we suggest that GAPDH is co-purified due to interactions with Oct-1. Expression of Oct-1 stimulates reporter gene expression from the T and the C −13 910 variant/LPH promoter constructs only when it is co-expressed with HNF1 α. Binding sites for other intestinal transcription factors (GATA-6, HNF4 α, Fox and Cdx-2) were identified in the region of the −13 910 T/C polymorphism. Three of these sites are required for the enhancer activity of the −13 910 region. The data suggest that the binding of Oct-1 to the T −13 910 variant directs increased lactase promoter activity and this might provide an explanation for the lactase persistence phenotype in the human population.
Lactase–phlorizin hydrolase is exclusively expressed in the small intestine and is often used as a marker for the differentiation of enterocytes. The cis-element CE-LPH1 found in the lactase–phlorizin hydrolase promoter has previously been shown to bind an intestinal-specific nuclear factor. By electrophoretic mobility-shift assay it was shown that the factor Cdx-2 (a homoeodomain-protein related to caudal) binds to a TTTAC sequence in the CE-LPH1. Furthermore it was demonstrated that Cdx-2 is able to activate reporter gene transcription by binding to CE-LPH1. A mutation in CE-LPH1, which does not affect Cdx-2 binding, results in a higher transcriptional activity, indicating that the CE-LPH1 site contains other binding site(s) in addition to the Cdx-2-binding site.