The temperature-signaling cascade in sponges involves a heat-gated cation channel, abscisic acid, and cyclic ADP-ribose.
Sponges (phylum Porifera) are the phylogenetically oldest metazoan animals, their evolution dating back to 600 million years ago. Here we demonstrate that sponges express ADP-ribosyl cyclase activity, which converts NAD(+) into cyclic ADP-ribose, a potent and universal intracellular Ca(2+) mobilizer. In Axinella polypoides (Demospongiae, Axinellidae), ADP-ribosyl cyclase was activated by temperature increases by means of an abscisic acid-induced, protein kinase A-dependent mechanism. The thermosensor triggering this signaling cascade was a heat-activated cation channel. Elucidation of the complete thermosensing pathway in sponges highlights a number of features conserved in higher organisms: (i) the cation channel thermoreceptor, sensitive to heat, mechanical stress, phosphorylation, and anesthetics, shares all of the functional characteristics of the mammalian heat-activated background K(+) channel responsible for central and peripheral thermosensing; (ii) involvement of the phytohormone abscisic acid and cyclic ADP-ribose as its second messenger is reminiscent of the drought stress signaling pathway in plants. These results suggest an ancient evolutionary origin of this stress-signaling cascade in a common precursor of modern Metazoa and Metaphyta.
Zocchi
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E
Dipartimento di Medicina Sperimentale, Sezione Biochimica, University of Genova, Viale Benedetto XV no. 1, 16132 Genova, Italy. ezocchi@unige.it
Carpaneto
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A
Cerrano
C
C
Bavestrello
G
G
Giovine
M
M
Bruzzone
S
S
Guida
L
L
Franco
L
L
Usai
C
C
D036541:ADP-ribosyl Cyclase; D051997:ADP-ribosyl Cyclase 1; D000040:Abscisic Acid / Q000096:biosynthesis / Q000502:physiology*; D000246:Adenosine Diphosphate Ribose / Q000502:physiology*; D000818:Animals; D015703:Antigens, CD; D000943:Antigens, Differentiation / Q000378:metabolism; D002851:Chromatography, High Pressure Liquid; D017868:Cyclic AMP-Dependent Protein Kinases / Q000378:metabolism; D004789:Enzyme Activation; D006358:Hot Temperature; D015640:Ion Channel Gating; D007473:Ion Channels / Q000378:metabolism / Q000502:physiology*; D009244:NAD+ Nucleosidase / Q000378:metabolism; D011161:Porifera / Q000201:enzymology / Q000378:metabolism*; D015398:Signal Transduction; D013050:Spectrometry, Fluorescence
D015703:Antigens, CD; D000943:Antigens, Differentiation; D007473:Ion Channels; D000246:Adenosine Diphosphate Ribose; D000040:Abscisic Acid; D017868:Cyclic AMP-Dependent Protein Kinases; D036541:ADP-ribosyl Cyclase; D009244:NAD+ Nucleosidase; D051997:ADP-ribosyl Cyclase 1