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J. Biol. Chem., Vol. 277, Issue 35, 32258-32267, August 30, 2002

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Induction of MUC2 and MUC5AC Mucins by Factors of the Epidermal Growth Factor (EGF) Family Is Mediated by EGF Receptor/Ras/Raf/Extracellular Signal-regulated Kinase Cascade and Sp1^*

Michaël Perrais^§, Pascal Pigny^¶, Marie-Christine Copin, Jean-Pierre Aubert^**, and Isabelle Van Seuningen

From the  Unité INSERM 560, Place de Verdun, 59045 Lille Cedex, ^** Laboratoires de Biochimie et de Biologie Moléculaire and ^¶ d'Endocrinologie de l'Hôpital Claude Huriez, Centre Hospitalier et Universitaire de Lille, 59037 Lille Cedex, and  Service d'Anatomie et Cytologie Pathologiques de l'Hôpital A. Calmette, Centre Hospitalier et Universitaire de Lille, 59037 Lille Cedex, France

The 11p15 mucin genes (MUC2, MUC5AC, MUC5B and MUC6) possess a cell-specific pattern of expression in normal lung that is altered during carcinogenesis. Growth factors of the epidermal growth factor family are known to target key genes that in turn may affect the homeostasis of lung mucosae. Our aim was to study the regulation of the 11p15 mucin genes both at the promoter and protein levels to assess whether their altered expression may represent a key event during lung carcinogenesis. Studies were performed in the mucoepidermoid NCI-H292 lung cancer cell line. Cell treatment with epidermal growth factor (EGF), transforming growth factor  (TGF-), or tumor necrosis factor  (TNF-) resulted in a dramatic increase of MUC2 and MUC5AC mRNAs levels, promoter activity, and apomucin expression, whereas those of MUC5B and MUC6 were unchanged. pGL3 deletion mutants of MUC2, MUC5AC, and MUC5B promoters were constructed and used in transient transfection assays to characterize EGF- and TGF--responsive regulatory regions within the promoters. They were located in the 2627/2097 and 202/1 regions of MUC2 and MUC5AC promoters, respectively. Finally, we demonstrate that transcription factor Sp1 not only binds and activates MUC2 and MUC5AC promoters but also participates to their EGF- and TGF--mediated up-regulation. We also show that Sp3 is a strong inhibitor of 11p15 mucin gene transcription. In conclusion, MUC2 and MUC5AC are two target genes of EGFR ligands in lung cancer cells, and up-regulation of these two genes goes through concomitant activation of the EGFR/Ras/Raf/Extracellular Signal-regulated Kinase-signaling pathway and Sp1 binding to their promoters.

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