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Calcium puffs are generic InsP₃-activated elementary calcium signals and are downregulated by prolonged hormonal stimulation to inhibit cellular calcium responses

Stephen C. Tovey^1,*, Patrick de Smet^2,*, Peter Lipp^1,, David Thomas¹, Kenneth W. Young³, Ludwig Missiaen², Humbert De Smedt², Jan B. Parys², Michael J. Berridge¹, Jan Thuring⁴, Andrew Holmes⁴ and Martin D. Bootman^1,5

¹ Laboratory of Molecular Signalling, The Babraham Institute, Babraham, Cambridge, CB2 4AT, UK
² Laboratory of Physiology, K.U. Leuven Campus Gasthuisberg O/N, Herestraat 49, B-3000 Leuven, Belgium
³ Department of Cell Physiology and Pharmacology, Medical Sciences Building, University of Leicester, University Road, Leicester, LE1 9HN, UK
⁴ Department of Chemistry, University of Cambridge, Lensfield Road, Cambridge, CB2 1EW, UK
⁵ Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK
^* These authors contributed equally to this study

Author for correspondence (e-mail: peter.lipp{at}bbsrc.ac.uk)

Accepted August 7, 2001

Elementary Ca²⁺ signals, such as ‘Ca²⁺ puffs’, which arise from the activation of inositol 1,4,5-trisphosphate receptors, are building blocks for local and global Ca²⁺ signalling. We characterized Ca²⁺ puffs in six cell types that expressed differing ratios of the three inositol 1,4,5-trisphosphate receptor isoforms. The amplitudes, spatial spreads and kinetics of the events were similar in each of the cell types. The resemblance of Ca²⁺ puffs in these cell types suggests that they are a generic elementary Ca²⁺ signal and, furthermore, that the different inositol 1,4,5-trisphosphate isoforms are functionally redundant at the level of subcellular Ca²⁺ signalling. Hormonal stimulation of SH-SY5Y neuroblastoma cells and HeLa cells for several hours downregulated inositol 1,4,5-trisphosphate expression and concomitantly altered the properties of the Ca²⁺ puffs. The amplitude and duration of Ca²⁺ puffs were substantially reduced. In addition, the number of Ca²⁺ puff sites active during the onset of a Ca²⁺ wave declined. The consequence of the changes in Ca²⁺ puff properties was that cells displayed a lower propensity to trigger regenerative Ca²⁺ waves. Therefore, Ca²⁺ puffs underlie inositol 1,4,5-trisphosphate signalling in diverse cell types and are focal points for regulation of cellular responses.

Key words: Calcium, Signalling, Inositol 1,4,5-trisphosphate

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