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 Ca2+mobilizer. In A...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2001-12, Vol.98 (26), p.14859-14864 |
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| creator | Zocchi, Elena Carpaneto, Armando Cerrano, Carlo Bavestrello, Giorgio Giovine, Marco Bruzzone, Santina Guida, Lucrezia Franco, Luisa Usai, Cesare |
| description | 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 Ca2+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. |
| doi_str_mv | 10.1073/pnas.261448698 |
| format | Article |
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Here we demonstrate that sponges express ADP-ribosyl cyclase activity, which converts NAD+into cyclic ADP-ribose, a potent and universal intracellular Ca2+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.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.261448698</identifier><identifier>PMID: 11752433</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Abscisic Acid - biosynthesis ; Abscisic Acid - physiology ; Acids ; Adenosine Diphosphate Ribose - physiology ; ADP-ribosyl Cyclase ; ADP-ribosyl Cyclase 1 ; Animals ; Antigens, CD ; Antigens, Differentiation - metabolism ; Aquatic life ; Axinella polypoides ; Biological Sciences ; Calcium ; Chromatography, High Pressure Liquid ; Cyclic AMP-Dependent Protein Kinases - metabolism ; Demospongiae ; Enzyme Activation ; Enzymes ; Fluorescence ; Heat ; Heat stress disorders ; Hot Temperature ; Ion Channel Gating ; Ion Channels - metabolism ; Ion Channels - physiology ; Marine ; NAD+ Nucleosidase - metabolism ; Phosphorylation ; Pipettes ; Porifera ; Porifera - enzymology ; Porifera - metabolism ; Proteins ; Signal Transduction ; Spectrometry, Fluorescence ; Sponges ; Syntactical consequents ; Temperature ; Thermoreceptors</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2001-12, Vol.98 (26), p.14859-14864</ispartof><rights>Copyright 1993-2001 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Dec 18, 2001</rights><rights>Copyright © 2001, The National Academy of Sciences 2001</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c520t-3c24e61fdf13fb9ce1a0c2154b359d097c8a008e2caf7fcb33296abd5713b0583</citedby><cites>FETCH-LOGICAL-c520t-3c24e61fdf13fb9ce1a0c2154b359d097c8a008e2caf7fcb33296abd5713b0583</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/98/26.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/3057376$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/3057376$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/11752433$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zocchi, Elena</creatorcontrib><creatorcontrib>Carpaneto, Armando</creatorcontrib><creatorcontrib>Cerrano, Carlo</creatorcontrib><creatorcontrib>Bavestrello, Giorgio</creatorcontrib><creatorcontrib>Giovine, Marco</creatorcontrib><creatorcontrib>Bruzzone, Santina</creatorcontrib><creatorcontrib>Guida, Lucrezia</creatorcontrib><creatorcontrib>Franco, Luisa</creatorcontrib><creatorcontrib>Usai, Cesare</creatorcontrib><title>The Temperature-Signaling Cascade in Sponges Involves a Heat-Gated Cation Channel, Abscisic Acid, and Cyclic ADP-Ribose</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>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 Ca2+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.</description><subject>Abscisic Acid - biosynthesis</subject><subject>Abscisic Acid - physiology</subject><subject>Acids</subject><subject>Adenosine Diphosphate Ribose - physiology</subject><subject>ADP-ribosyl Cyclase</subject><subject>ADP-ribosyl Cyclase 1</subject><subject>Animals</subject><subject>Antigens, CD</subject><subject>Antigens, Differentiation - metabolism</subject><subject>Aquatic life</subject><subject>Axinella polypoides</subject><subject>Biological Sciences</subject><subject>Calcium</subject><subject>Chromatography, High Pressure Liquid</subject><subject>Cyclic AMP-Dependent Protein Kinases - metabolism</subject><subject>Demospongiae</subject><subject>Enzyme Activation</subject><subject>Enzymes</subject><subject>Fluorescence</subject><subject>Heat</subject><subject>Heat stress disorders</subject><subject>Hot Temperature</subject><subject>Ion Channel Gating</subject><subject>Ion Channels - metabolism</subject><subject>Ion Channels - physiology</subject><subject>Marine</subject><subject>NAD+ Nucleosidase - metabolism</subject><subject>Phosphorylation</subject><subject>Pipettes</subject><subject>Porifera</subject><subject>Porifera - enzymology</subject><subject>Porifera - metabolism</subject><subject>Proteins</subject><subject>Signal Transduction</subject><subject>Spectrometry, Fluorescence</subject><subject>Sponges</subject><subject>Syntactical consequents</subject><subject>Temperature</subject><subject>Thermoreceptors</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2001</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqF0U2P0zAQBuAIgdiycOWEIOKAOGzK-COJLXGpCuyutBKILWfLcSatq9QusVPYf4-rlvJxgJMtzzOWPW-WPSUwJVCzN1unw5RWhHNRSXEvmxCQpKi4hPvZBIDWheCUn2WPQlgDgCwFPMzOCKlLyhmbZN8WK8wXuNnioOM4YHFrl0731i3zuQ5Gt5hbl99uvVtiyK_dzve7tNH5FepYXOqIbYLRepfPV9o57C_yWROMDdbkM2Pbi1y7RO5Mvz9496n4bBsf8HH2oNN9wCfH9Tz78uH9Yn5V3Hy8vJ7PbgpTUogFM5RjRbq2I6xrpEGiwVBS8oaVsgVZG6EBBFKju7ozDWNUVrppy5qwBkrBzrO3h3u3Y7PB1qCLg-7VdrAbPdwpr636s-LsSi39TqURcpnaXx3bB_91xBDVxgaDfa8d-jGomrI0SVr-FxJBqaSSJ_jyL7j245BGHhQFwiqgnCY0PSAz-BAG7E4PJqD2uat97uqUe2p4_vs3f_Fj0Am8PoJ948-yFOkORbgoperGvo_4PSb64t80iWcHsQ7RDyfCoKxZXbEfJJjK2w</recordid><startdate>20011218</startdate><enddate>20011218</enddate><creator>Zocchi, Elena</creator><creator>Carpaneto, Armando</creator><creator>Cerrano, Carlo</creator><creator>Bavestrello, Giorgio</creator><creator>Giovine, Marco</creator><creator>Bruzzone, Santina</creator><creator>Guida, Lucrezia</creator><creator>Franco, Luisa</creator><creator>Usai, Cesare</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><general>The National Academy of Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20011218</creationdate><title>The Temperature-Signaling Cascade in Sponges Involves a Heat-Gated Cation Channel, Abscisic Acid, and Cyclic ADP-Ribose</title><author>Zocchi, Elena ; 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Here we demonstrate that sponges express ADP-ribosyl cyclase activity, which converts NAD+into cyclic ADP-ribose, a potent and universal intracellular Ca2+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.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>11752433</pmid><doi>10.1073/pnas.261448698</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Abscisic Acid - biosynthesis Abscisic Acid - physiology Acids Adenosine Diphosphate Ribose - physiology ADP-ribosyl Cyclase ADP-ribosyl Cyclase 1 Animals Antigens, CD Antigens, Differentiation - metabolism Aquatic life Axinella polypoides Biological Sciences Calcium Chromatography, High Pressure Liquid Cyclic AMP-Dependent Protein Kinases - metabolism Demospongiae Enzyme Activation Enzymes Fluorescence Heat Heat stress disorders Hot Temperature Ion Channel Gating Ion Channels - metabolism Ion Channels - physiology Marine NAD+ Nucleosidase - metabolism Phosphorylation Pipettes Porifera Porifera - enzymology Porifera - metabolism Proteins Signal Transduction Spectrometry, Fluorescence Sponges Syntactical consequents Temperature Thermoreceptors |
| title | The Temperature-Signaling Cascade in Sponges Involves a Heat-Gated Cation Channel, Abscisic Acid, and Cyclic ADP-Ribose |
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