{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T04:45:02Z","timestamp":1789965902819,"version":"4.0.1"},"reference-count":53,"publisher":"Public Library of Science (PLoS)","issue":"2","license":[{"start":{"date-parts":[[2018,2,21]],"date-time":"2018-02-21T00:00:00Z","timestamp":1519171200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Research Funding of the Medical Faculty (FoRUM), Ruhr University Bochum (DE)","award":["F720-2011"],"award-info":[{"award-number":["F720-2011"]}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0192322","type":"journal-article","created":{"date-parts":[[2018,2,23]],"date-time":"2018-02-23T15:51:43Z","timestamp":1519401103000},"page":"e0192322","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":20,"title":["Soluble adenylyl cyclase: A novel player in cardiac hypertrophy induced by isoprenaline or pressure overload"],"prefix":"10.1371","volume":"13","author":[{"given":"Ilona","family":"Schirmer","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tippaporn","family":"Bualeong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heidi","family":"Budde","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Diana","family":"Cimiotti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Avinash","family":"Appukuttan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicole","family":"Klein","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Philip","family":"Steinwascher","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Reusch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andreas","family":"M\u00fcgge","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rainer","family":"Meyer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yury","family":"Ladilov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2706-6109","authenticated-orcid":true,"given":"Kornelia","family":"Jaquet","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2018,2,21]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1093\/cvr\/cvs249","article-title":"\u03b2-Adrenergic receptor stimulation causes cardiac hypertrophy via G\u03b2\u03b3\/Erk-dependent pathway","volume":"96","author":"M Vidal","year":"2012","journal-title":"Cardiovasc Res"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"9760","DOI":"10.1074\/jbc.274.14.9760","article-title":"Both G<sub>s<\/sub> and G<sub>i<\/sub> proteins are critically involved in Isoproterenol-induced cardiomyocyte hypertrophy","volume":"274","author":"Y Zou","year":"1999","journal-title":"J Biol Chem"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1073\/pnas.96.1.79","article-title":"Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals","volume":"96","author":"J Buck","year":"1991","journal-title":"Proc Natl Acad Sci USA"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/S0026-895X(25)14397-6","article-title":"Forskolin does not activate sperm adenylate cyclase","volume":"24","author":"LR Forte","year":"1983","journal-title":"Mol Pharmacol"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"343","DOI":"10.3389\/fphys.2013.00343","article-title":"pH sensing via bicarbonate regulated \u201esoluble\u201dadenylyl cyclase (sAC)","volume":"4","author":"N Rahman","year":"2013","journal-title":"Front Physiol"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"33283","DOI":"10.1074\/jbc.M113.510073","article-title":"CO<sub>2<\/sub>\/HCO<sub>3<\/sub>- and calcium regulated soluble adenylyl cyclase as a physiological ATP sensor","volume":"288","author":"JH Zippin","year":"2013","journal-title":"J Biol Chem"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"1097","DOI":"10.1073\/pnas.72.3.1097","article-title":"Development of a Mn-2+-sensitive, \u2018soluble\u2019 adenylate cyclase in rat testis","volume":"72","author":"T Braun","year":"1975","journal-title":"Proc Natl Acad Sci USA"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"15922","DOI":"10.1074\/jbc.M212475200","article-title":"Kinetic properties of soluble adenylyl cyclase. Synergism between calcium and bicarbonate","volume":"278","author":"TN Litvin","year":"2003","journal-title":"J Biol Chem"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"4151","DOI":"10.1111\/febs.12913","article-title":"Structural analysis of human soluble adenylyl cyclase and crystal structures of its nucleotide complexes \u2013 implications for cyclase catalysis and evolution","volume":"281","author":"S Kleinboelting","year":"2014","journal-title":"FEBS J"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1126\/science.289.5479.625","article-title":"Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor","volume":"289","author":"Y Chen","year":"2000","journal-title":"Science"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"e3251","DOI":"10.1371\/journal.pone.0003251","article-title":"Somatic soluble adenylyl cyclase isoforms are unaffected in SACY<sup>TM1Lex<\/sup>\/SACY<sup>TM1Lex<\/sup> knockout mice","volume":"3","author":"J Farell","year":"2008","journal-title":"PLoS ONE"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"750","DOI":"10.1165\/rcmb.2013-0542OC","article-title":"A soluble adenylyl cyclase form targets to axonemes and rescues beat regulation in soluble adenylyl cyclase knock-out mice","volume":"51","author":"X Chen","year":"2014","journal-title":"Am J Resp Cell and Mol Biol"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1096\/fj.02-0598fje","article-title":"Compartmentalization of bicarbonate-sensitive adenylyl cyclase in distinct signaling microdomains","volume":"17","author":"JH Zippin","year":"2003","journal-title":"FASEB J"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"5808","DOI":"10.1016\/S0021-9258(17)30340-X","article-title":"Physical and functional properties of adenylate cyclase from mature rat testis","volume":"253","author":"EJ Neer","year":"1978","journal-title":"J Biol Chem"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/0076-6879(91)95160-L","article-title":"Purification of soluble form of adenylate cyclase from testes","volume":"195","author":"T Braun","year":"1991","journal-title":"Methods Enzymol"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1016\/j.cmet.2013.05.003","article-title":"Mitochondrial Ca<sup>2+<\/sup> uptake induces cyclic AMP generation in the matrix and modulates organelle ATP levels","volume":"17","author":"G Di Benedetto","year":"2013","journal-title":"Cell Metabolism"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"953","DOI":"10.1007\/s00424-010-0865-6","article-title":"Physiological carbon dioxide, bicarbonate and pH sensing","volume":"460","author":"M Tresguerres","year":"2010","journal-title":"Pflugers Archiv\u2014Eur J Physiol"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"1277","DOI":"10.1038\/ki.2011.95","article-title":"Intracellular cAMP signaling by soluble adenylyl cyclase","volume":"79","author":"M Tresguerres","year":"2011","journal-title":"Kidney Int"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"3126","DOI":"10.1074\/jbc.M112.403279","article-title":"Type 10 soluble adenylyl cyclase is overexpressed in prostate carcinoma and controls proliferation of prostate cancer cells","volume":"288","author":"JP Flacke","year":"2013","journal-title":"J Biol Chem"},{"key":"ref20","article-title":"Introducing a novel mechanism to control heart rate in the ancestral pacific hagfish","author":"CM Wilson","year":"2016","journal-title":"J Exp Biol"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1093\/cvr\/cvr306","article-title":"Type 10 adenylyl cyclase mediates mitochondrial Bax translocation and apoptosis of adult rat cardiomyocytes under simulated ischaemia\/reperfusion","volume":"93","author":"A Appukuttan","year":"2012","journal-title":"Cardiovasc Res"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"14760","DOI":"10.1074\/jbc.M900925200","article-title":"Soluble adenylyl cyclase controls mitochondria-dependent apoptosis in coronary endothelial cells","volume":"284","author":"S Kumar","year":"2009","journal-title":"J Biol Chem"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"2646","DOI":"10.1016\/j.bbadis.2014.06.034","article-title":"Role of soluble adenylyl cyclase in cell death and growth","volume":"1842","author":"Y Ladilov","year":"2014","journal-title":"Biochim Biophys Acta"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"2656","DOI":"10.1016\/j.bbadis.2014.09.008","article-title":"Inhibition of soluble adenylyl cyclase increases the radiosensitivity of prostate cancer cells","volume":"1842","author":"A Appukuttan","year":"2014","journal-title":"Biochim Biophys Acta"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1083\/jcb.200311119","article-title":"Bicarbonate-responsible \u201csoluble\u201d adenylyl cyclase defines a nuclear AMP microdomain","volume":"164","author":"JH Zippin","year":"2004","journal-title":"J Cell Biol"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"1884","DOI":"10.1096\/fj.06-7915com","article-title":"Cardiomyocyte-specific inactivation of transcription factor CREB in mice","volume":"21","author":"M Matus","year":"2007","journal-title":"FASEB J"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/s00424-008-0487-4","article-title":"Expression of cTnI-R145G affects shortening properties of adult rat cardiomyocytes","volume":"457","author":"S Reis","year":"2008","journal-title":"Pflugers Arch\u2013Eur J Physiol"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"C495","DOI":"10.1152\/ajpcell.2000.279.2.C495","article-title":"Hypertrophic effect of selective beta1-adrenoceptor stimulation on ventricular cardiomyocytes from adult rat","volume":"279","author":"M Sch\u00e4fer","year":"2000","journal-title":"Am J Physiol"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1124\/jpet.113.208496","article-title":"Pharmacological distinction between soluble and transmembrane adenylyl cyclases","volume":"347","author":"JL Bitterman","year":"2013","journal-title":"J Pharmacol Exp Therapeutics"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/j.cmet.2009.01.012","article-title":"Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation","volume":"9","author":"R Acin-Perez","year":"2009","journal-title":"Cell Metab"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"2509","DOI":"10.1073\/pnas.95.5.2509","article-title":"A simplified system for generating recombinant adenoviruses","volume":"95","author":"T-C He","year":"1998","journal-title":"Proc Natl Acad Sci USA"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1007\/s00395-006-0597-0","article-title":"Myocardial injury modulates the innate immune system and changes myocardial sensitivity","volume":"101","author":"G Baumgarten","year":"2006","journal-title":"Basic Res Cardiol"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1007\/s10741-008-9132-8","article-title":"Beta-adrenergic stimulation and myocardial function in the failing heart","volume":"14","author":"A El-Armouche","year":"2009","journal-title":"Heart Fail Rev"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1186\/1756-0500-3-307","article-title":"Mice lacking the C\u03b2 subunit of PKA are resistant to angiotensin II-induced cardiac hypertrophy and dysfunction","volume":"16","author":"LC Enns","year":"2010","journal-title":"BMC Res Notes"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"15467","DOI":"10.1073\/pnas.1000462107","article-title":"PKA phosphorylates histone deacetylase 5 and prevents its nuclear export, leading to the inhibition of gene transcription and cardiomyocyte hypertrophy","volume":"107","author":"CH Ha","year":"2010","journal-title":"Proc Natl Acad SCI USA"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1161\/CIRCRESAHA.114.305892","article-title":"Cardiac hypertrophy is inhibited by a local pool of cAMP generated by phosphodiesterase 2","volume":"117","author":"A Zoccarato","year":"2015","journal-title":"Circ Res"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/j.pharmthera.2014.03.008","article-title":"cAMP signaling in subcellular compartments","volume":"143","author":"K Lefkimmiatis","year":"2014","journal-title":"Pharmacol Ther"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.bbamcr.2003.10.008","article-title":"Endothelin-1 promotes phosphorylation of CREB transcription factor in primary cultures of neonatal rat cardiomyocytes: implications for the regulation of c-jun expression","volume":"1644","author":"JG Harrison","year":"2004","journal-title":"Biochim Biophys Acta"},{"key":"ref39","first-page":"1527","article-title":"CREB: a Ca2+-regulated transcription factor phosphorylated by calmodulin-dependent kinases","volume":"251","author":"M Sheng","year":"1991","journal-title":"Science"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1126\/science.273.5277.959","article-title":"Coupling of the ras-MAPK pathway to the gene activation by RSK2, a growth factor regulated CREB kinase","volume":"273","author":"J Xing","year":"1996","journal-title":"Science"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"476","DOI":"10.1016\/j.cardiores.2004.04.026","article-title":"Role of Ca2+\/calmodulin-dependent kinase II in cardiac hypertrophy and heart failure","volume":"63","author":"T Zhang","year":"2004","journal-title":"Cardiovascular Res"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"844","DOI":"10.1172\/JCI46399","article-title":"Ras signaling pathway mutations and cardiac hypertrophy: getting into and out of the thick of it","volume":"121","author":"BD Gelb","year":"2011","journal-title":"JCI"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1172\/JCI200316326","article-title":"Linkage of \u03b21-adrenergic stimulation to apoptotic heart cell death through protein kinase A-independent activation of Ca2+\/calmodulin kinase II","volume":"111","author":"W-Z Zhu","year":"2003","journal-title":"JCI"},{"key":"ref44","doi-asserted-by":"crossref","DOI":"10.1161\/CIRCULATIONAHA.110.942268","article-title":"Molecular pathways underlying cardiac remodelling during pathophysiologic stimulation","volume":"122","author":"I Kehat","year":"2010","journal-title":"Circulation"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"C1305","DOI":"10.1152\/ajpcell.00584.2004","article-title":"Cloning and characterization of the human soluble adenylyl cyclase","volume":"288","author":"W Geng","year":"2005","journal-title":"Am J Physiol Cell Physiol"},{"key":"ref46","doi-asserted-by":"crossref","DOI":"10.1161\/CIRCRESAHA.107.164947","article-title":"Epac mediates \u00df adrenergic receptor-induced cardiomyocyte hypertrophy","volume":"102","author":"M Metrich","year":"2008","journal-title":"Circ Res"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1073\/pnas.231619298","article-title":"Activated glycogen synthase kinase 3\u00df suppresses cardiac hypertrophy in vivo","volume":"22","author":"CL Antos","year":"2002","journal-title":"PNAS"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"e14227","DOI":"10.1371\/journal.pone.0014227","article-title":"Concerted regulation of cGMP and cAMP phosphodiesterases in early cardiac hypertrophy induced by angiotensin II","volume":"5","author":"W Mokni","year":"2010","journal-title":"PLoSOne"},{"issue":"4","key":"ref49","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1016\/j.cardfail.2007.01.004","article-title":"Hypertrophy and heart failure in mice overexpressing the cardiac sodium-calcium exchanger","volume":"13","author":"KP Roos","year":"2007","journal-title":"J Card Fail"},{"issue":"2","key":"ref50","doi-asserted-by":"crossref","first-page":"e89559","DOI":"10.1371\/journal.pone.0089559","article-title":"Effect of transverse aortic constriction on cardiac structure, function and gene expression in pregnant rats","volume":"9","author":"NT Songstad","year":"2014","journal-title":"PLoS One"},{"issue":"5","key":"ref51","doi-asserted-by":"crossref","first-page":"H1703","DOI":"10.1152\/ajpheart.00238.2001","article-title":"Echocardiographic assessment of LV hypertrophy and function in aortic-banded mice: necropsy validation","volume":"282","author":"Y Liao","year":"2002","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"ref52","first-page":"506","article-title":"Natriuretic peptides and cardiac hypertrophy","volume":"48","author":"B London","year":"2006","journal-title":"JACC"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/j.yjmcc.2014.03.002","article-title":"Targeted deletion of ERK2 in cardiomyocytes attenuates hypertrophic response but provokes provokes pathological stress induced cardiac dysfunction","volume":"72","author":"S Ulm","year":"2014","journal-title":"J Mol Cell Cardio"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0192322","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,7,2]],"date-time":"2025-07-02T00:17:57Z","timestamp":1751415477000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0192322"}},"subtitle":[],"editor":[{"given":"Harald HHW","family":"Schmidt","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2018,2,21]]},"references-count":53,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2018,2,21]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0192322","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,2,21]]}}}