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J. Biol. Chem., Vol. 279, Issue 25, 26082-26089, June 18, 2004

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Multiple Fatty Acid Sensing Mechanisms Operate in Enteroendocrine Cells

NOVEL EVIDENCE FOR DIRECT MOBILIZATION OF STORED CALCIUM BY CYTOSOLIC FATTY ACID^*

Tohru Hira, Austin C. Elliott, David G. Thompson¶, R. Maynard Case, and John T. McLaughlin¶||

From the School of Biological Sciences, G.38 Stopford Building, University of Manchester, Oxford Road, Manchester M13 9PT, United Kingdom, the Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University, Kita-9, Nishi-9, Kita-ku, Sapporo, 060-8589, Japan, and ^¶Gastrointestinal Sciences, Clinical Sciences Building, Hope Hospital, Stott Lane, Salford M6 8HD, United Kingdom

Fatty acids (FA) with at least 12 carbon atoms increase intracellular Ca²⁺ ([Ca²⁺]_i) to stimulate cholecystokinin release from enteroendocrine cells. Using the murine enteroendocrine cell line STC-1, we investigated whether candidate intracellular pathways transduce the FA signal, or whether FA themselves act within the cell to release Ca²⁺ directly from the intracellular store. STC-1 cells loaded with fura-2 were briefly (3 min) exposed to saturated FA above and below the threshold length (C₈, C₁₀, and C₁₂). C₁₂, but not C₈ or C₁₀, induced a dose-dependent increase in [Ca²⁺]_i, in the presence or absence of extracellular Ca²⁺. Various signaling inhibitors, including D-myo-inositol 1,4,5-triphosphate receptor antagonists, all failed to block FA-induced Ca²⁺ responses. To identify direct effects of cytosolic FA on the intracellular Ca²⁺ store, [Ca²⁺]_i was measured in STC-1 cells loaded with the lower affinity Ca²⁺ dye magfura-2, permeabilized by streptolysin O. In permeabilized cells, again C₁₂ but not C₈ or C₁₀, induced release of stored Ca²⁺. Although C₁₂ released Ca²⁺ in other permeabilized cell lines, only intact STC-1 cells responded to C₁₂ in the presence of extracellular Ca²⁺. In addition, 30 min exposure to C₁₂ induced a sustained elevation of [Ca²⁺]_i in the presence of extracellular Ca²⁺, but only a transient response in the absence of extracellular Ca²⁺. These results suggest that at least two FA sensing mechanisms operate in enteroendocrine cells: intracellularly, FA (C₁₂) transiently induce Ca²⁺ release from intracellular Ca²⁺ stores. However, they also induce sustained Ca²⁺ entry from the extracellular medium to maintain an elevated [Ca²⁺]_i.

Received for publication, January 6, 2004 , and in revised form, March 19, 2004.

^* This work was supported by the Digestive Disorders Foundation, UK, and the Japan Society for the Promotion of Science. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^|| To whom correspondence should be addressed. Tel.: 44-161-206-4362; Fax: 44-161-206-1495; E-mail: john.mclaughlin{at}man.ac.uk.

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