Manuela Zaccolo - Selected Publications#

Total number of publications: 180; citations: .8500; H-index: 50 (Web of Science)

Tomek J, Zaccolo M. Compartmentalized cAMP signalling and control of cardiac rhythm. Philos Trans R Soc Lond B Biol Sci. 2023 Jun 19;378(1879):20220172. doi: 10.1098/rstb.2022.0172.

Kovanich D, Low TY, Zaccolo M. Using the Proteomics Toolbox to Resolve Topology and Dynamics of Compartmentalized cAMP Signaling. Int J Mol Sci. 2023 Feb 28;24(5):4667. doi: 10.3390/ijms24054667.

Varley A, Koschinski A, Johnson MR, Zaccolo M. cAMP Compartmentalisation in Human Myometrial Cells. Cells. 2023 Feb 24;12(5):718. doi: 10.3390/cells12050718.

Subramaniam G, Schleicher K, Kovanich D, Zerio A, Folkmanaite M, Chao YC, Surdo NC, Koschinski A, Hu J, Scholten A, Heck AJR, Ercu M, Sholokh A, Park KC, Klussmann E, Meraviglia V, Bellin M, Zanivan S, Hester S, Mohammed S, Zaccolo M. Integrated Proteomics Unveils Nuclear PDE3A2 as a Regulator of Cardiac Myocyte Hypertrophy. Circ Res. 2023 Mar 31;132(7):828-848. doi: 10.1161/CIRCRESAHA.122.321448.

Folkmanaite M, Zaccolo M. Regulation of cardiac function by cAMP nanodomains.Biosci Rep. 2023 Feb 7:BSR20220953. doi: 10.1042/BSR20220953.

Ren L, Thai PN, Gopireddy RR, Timofeyev V, Ledford HA, Woltz RL, Park S, Puglisi JL, Moreno CM, Santana LF, Conti AC, Kotlikoff MI, Xiang YK, Yarov-Yarovoy V, Zaccolo M, Zhang XD, Yamoah EN, Navedo MF, Chiamvimonvat N. Adenylyl cyclase isoform 1 contributes to sinoatrial node automaticity via functional microdomains. JCI Insight. 2022 Nov 22;7(22):e162602. doi: 10.1172/jci.insight.162602.

Bose SJ, Read MJ, Akerman E, Capel RA, Ayagama T, Russell A, Terrar DA, Zaccolo M, Burton RAB. Inhibition of adenylyl cyclase 1 by ST034307 inhibits IP3-evoked changes in sino-atrial node beat rate. Front Pharmacol. 2022 Aug 29;13:951897. doi: 10.3389/fphar.2022.951897

Li D, Liu K, Davis H, Robertson C, Neely OC, Tarafdar A, Li N, Lefkimmiatis K, Zaccolo M, Paterson DJ. Abnormal Cyclic Nucleotide Signaling at the Outer Mitochondrial Membrane In Sympathetic Neurons During the Early Stages of Hypertension. Hypertension. 2022 Jul;79(7):1374-1384. doi: 10.1161/HYPERTENSIONAHA.121.18882.

Anton SE, Kayser C, Maiellaro I, Nemec K, Möller J, Koschinski A, Zaccolo M, Annibale P, Falcke M, Lohse MJ, Bock A. Receptor-associated independent cAMP nanodomains mediate spatiotemporal specificity of GPCR signalling. Cell. 2022 Mar 31;185(7):1130-1142.e11. doi: 10.1016/j.cell.2022.02.011.

Schleicher K, Hester S, Stegmann M, Zaccolo M. Quantitative Phosphoproteomics to Study cAMP Signaling. Methods Mol Biol. 2022;2483:281-296. doi: 10.1007/978-1-0716-2245-2_18.

Koschinski A, Zaccolo M. Micro-2D Cell Culture for cAMP Measurements Using FRET Reporters in Human iPSC-Derived Cardiomyocytes. Methods Mol Biol. 2022;2483:141-165. doi: 10.1007/978-1-0716-2245-2_9.

Ren L, Thai P, Gopireddy R, Timofeyev V, Ledford H, Woltz R, Park S, Puglisi J, Moreno Moreno C, Santana F, Conti A, Kotlikoff M, Xiang Y, Yarov-Yarovoy V, Zaccolo M, Zhang X-D, Yamoah E, Navedo M and Chiamvimonvat N. Adenylyl Cyclase Isoform 1 Contributes to Sinoatrial Node Automaticity via Functional Microdomains. iScience. 2021 Dec 25;25(1):103693. doi: 10.1016/j.isci.2021.103693.

Kar P, Barak P, Zerio A, Lin YP, Parekh AJ, Watts VJ, Cooper DMF, Zaccolo M, Kramer H, Parekh AB. AKAP79 Orchestrates a Cyclic AMP Signalosome Adjacent to Orai1 Ca2+ Channels. Function (Oxf). 2021 Jul 29;2(5):zqab036. doi: 10.1093/function/zqab036.

Manfra O, Calamera G, Froese A, Arunthavarajah D, Surdo NC, Meier S, Melleby AO, Aasrum M, Aronsen JM, Nikolaev VO, Zaccolo M, Moltzau LR, Levy FO, Andressen KW. CNP regulates cardiac contractility and increases cGMP near both SERCA and TnI: difference from BNP visualized by targeted cGMP biosensors. Cardiovasc Res. 2022 May 6;118(6):1506-1519. doi: 10.1093/cvr/cvab167.

Zaccolo M. cAMP Buffering via Liquid-Liquid Phase Separation. Function. 2020 Dec 26;2(1):zqaa048. doi: 10.1093/function/zqaa048.

Zaccolo M, Zerio A, Lobo MJ. Subcellular Organization of the cAMP Signaling Pathway. Pharmacol Rev. 2021 Jan;73(1):278-309. doi: 10.1124/pharmrev.120.000086.

As of April 2022, this paper received enough citations to place it in the top 1% of the field (Web of Science)

Simon JN, Vrellaku B, Monterisi S, Chu SM, Rawlings N, Lomas O, Marchal GA, Waithe D, Syeda F, Gajendragadkar PR, Jayaram R, Sayeed R, Channon KM, Fabritz L, Swietach P, Zaccolo M, Eaton P, Casadei B. Oxidation of Protein Kinase A Regulatory Subunit PKARIα Protects Against Myocardial Ischemia-Reperfusion Injury by Inhibiting Lysosomal-Triggered Calcium Release. Circulation. 2021 Feb 2;143(5):449-465. doi: 10.1161/CIRCULATIONAHA.120.046761.

Lobo MJ, Reverte-Salisa L, Chao YC, Koschinski A, Gesellchen F, Subramaniam G, Jiang H, Pace S, Larcom N, Paolocci E, Pfeifer A, Zanivan S, Zaccolo M. Phosphodiesterase 2A2 regulates mitochondria clearance through Parkin-dependent mitophagy. Commun Biol. 2020 Oct 21;3(1):596. doi: 10.1038/s42003-020-01311-7

Capel RA, Bose SJ, Collins TP, Rajasundaram S, Ayagama T, Zaccolo M, Burton RB, Terrar DA. IP3-mediated Ca2+ release regulates atrial Ca2+ transients and pacemaker function by stimulation of adenylyl cyclases. Am J Physiol Heart Circ Physiol. 2021 Jan 1;320(1):H95-H107. doi: 10.1152/ajpheart.00380.2020.

20. Brescia M, Chao YC, Koschinski A, Tomek J, Zaccolo M. Multi-Compartment, Early Disruption of cGMP and cAMP Signalling in Cardiac Myocytes from the mdx Model of Duchenne Muscular Dystrophy. Int J Mol Sci. 2020 Sep 25;21(19):7056. doi: 10.3390/ijms21197056

Santos JD, Pinto FR, Ferreira JF, Amaral MD, Zaccolo M, Farinha CM. Cytoskeleton regulators CAPZA2 and INF2 associate with CFTR to control its plasma membrane levels under EPAC1 activation. Biochem J. 2020 Jul 17;477(13):2561-2580. doi: 10.1042/BCJ20200287.

Schleicher K, Zaccolo M. Axelrod Symposium 2019: Phosphoproteomic Analysis of G-Protein-Coupled Pathways. Mol Pharmacol. 2021 May;99(5):383-391. doi: 10.1124/mol.119.118869.

Dai Y, Amenov A, Ignatyeva N, Koschinski A, Xu H, Soong PL, Tiburcy M, Linke WA, Zaccolo M, Hasenfuss G, Zimmermann WH, Ebert A. Troponin destabilization impairs sarcomere-cytoskeleton interactions in iPSC-derived cardiomyocytes from dilated cardiomyopathy patients. Sci Rep. 2020 Jan 14;10(1):209. doi: 10.1038/s41598-019-56597-3.

Chao YC, Surdo NC, Pantano S, Zaccolo M. Imaging cAMP nanodomains in the heart. Biochem Soc Trans. 2019 Oct 31;47(5):1383-1392. doi: 10.1042/BST20190245.

Bers DM, Xiang YK, Zaccolo M. Whole-Cell cAMP and PKA Activity are Epiphenomena, Nanodomain Signaling Matters. Physiology (Bethesda). 2019 Jul 1;34(4):240-249. doi: 10.1152/physiol.00002.2019

Koschinski A, Zaccolo M. Quantification and Comparison of Signals Generated by Different FRET-Based cAMP Reporters. Methods Mol Biol. 2019;1947:217-237. doi: 10.1007/978-1-4939-9121-1_12.

Brown P; RELISH Consortium, Zhou Y. Large expert-curated database for benchmarking document similarity detection in biomedical literature search. Database (Oxford). 2019 Jan 1;2019:baz085. doi: 10.1093/database/baz085.

Musheshe N, Lobo MJ, Schmidt M, Zaccolo M. Targeting FRET-Based Reporters for cAMP and PKA Activity Using AKAP79. Sensors (Basel). 2018 Jul 5;18(7):2164. doi: 10.3390/s18072164.

Burdyga A, Surdo NC, Monterisi S, Di Benedetto G, Grisan F, Penna E, Pellegrini L, Zaccolo M, Bortolozzi M, Swietach P, Pozzan T, Lefkimmiatis K. Phosphatases control PKA-dependent functional microdomains at the outer mitochondrial membrane. Proc Natl Acad Sci U S A. 2018 Jul 10;115(28):E6497-E6506. doi: 10.1073/pnas.1806318115

Liu K, Li D, Hao G, McCaffary D, Neely O, Woodward L, Ioannides D, Lu CJ, Brescia M, Zaccolo M, Tandri H, Ajijola OA, Ardell JL, Shivkumar K, Paterson DJ. Phosphodiesterase 2A as a therapeutic target to restore cardiac neurotransmission during sympathetic hyperactivity. JCI Insight. 2018 May 3;3(9):e98694. doi: 10.1172/jci.insight.98694.

Wright PT, Bhogal NK, Diakonov I, Pannell LMK, Perera RK, Bork NI, Schobesberger S, Lucarelli C, Faggian G, Alvarez-Laviada A, Zaccolo M, Kamp TJ, Balijepalli RC, Lyon AR, Harding SE, Nikolaev VO, Gorelik J. Cardiomyocyte Membrane Structure and cAMP Compartmentation Produce Anatomical Variation in β2AR-cAMP Responsiveness in Murine Hearts. Cell Rep. 2018 Apr 10;23(2):459-469. doi: 10.1016/j.celrep.2018.03.053

Bruche S, Zaccolo M. FRET-ting about RhoA signalling in heart and vasculature: a new tool in our cardiovascular toolbox. Cardiovasc Res. 2018 Apr 1;114(5):e25-e27. doi: 10.1093/cvr/cvy032.

Hamilton A, Zhang Q, Salehi A, Willems M, Knudsen JG, Ringgaard AK, Chapman CE, Gonzalez-Alvarez A, Surdo NC, Zaccolo M, Basco D, Johnson PRV, Ramracheya R, Rutter GA, Galione A, Rorsman P, Tarasov AI Adrenaline Stimulates Glucagon Secretion by Tpc2-Dependent Ca2+ Mobilization From Acidic Stores in Pancreatic α-Cells. Diabetes. 2018 Jun;67(6):1128-1139. doi: 10.2337/db17-1102.

Schleicher K, Zaccolo M. Using cAMP Sensors to Study Cardiac Nanodomains. J Cardiovasc Dev Dis. 2018 Mar 13;5(1):17. doi: 10.3390/jcdd5010017.

Musheshe N, Schmidt M, Zaccolo M. cAMP: From Long-Range Second Messenger to Nanodomain Signalling.Trends Pharmacol Sci. 2018 Feb;39(2):209-222. doi: 10.1016/j.tips.2017.11.006.

Rodrigues AL, Brescia M, Koschinski A, Moreira TH, Cameron RT, Baillie G, Beirão PSL, Zaccolo M, Cruz JS. Increase in Ca2+ current by sustained cAMP levels enhances proliferation rate in GH3 cells. Life Sci. 2018 Jan 1;192:144-150. doi: 10.1016/j.lfs.2017.11.040.

Koschinski A, Zaccolo M. Activation of PKA in cell requires higher concentration of cAMP than in vitro: implications for compartmentalization of cAMP signalling. Sci Rep. 2017 Oct 26;7(1):14090. doi: 10.1038/s41598-017-13021-y.

Monterisi S, Lobo MJ, Livie C, Castle JC, Weinberger M, Baillie G, Surdo NC, Musheshe N, Stangherlin A, Gottlieb E, Maizels R, Bortolozzi M, Micaroni M, Zaccolo M. PDE2A2 regulates mitochondria morphology and apoptotic cell death via local modulation of cAMP/PKA signalling. Elife. 2017 May 2;6:e21374. doi: 10.7554/eLife.21374.

Surdo NC, Berrera M, Koschinski A, Brescia M, Machado MR, Carr C, Wright P, Gorelik J, Morotti S, Grandi E, Bers DM, Pantano S, Zaccolo M. FRET biosensor uncovers cAMP nano-domains at β-adrenergic targets that dictate precise tuning of cardiac contractility. Nat Commun. 2017 Apr 20;8:15031. doi: 10.1038/ncomms15031.

Monterisi S, Zaccolo M. Components of the mitochondrial cAMP signalosome. Biochem Soc Trans. 2017 Feb 8;45(1):269-274. doi: 10.1042/BST20160394.

Brescia M, Zaccolo M. Modulation of Compartmentalised Cyclic Nucleotide Signalling via Local Inhibition of Phosphodiesterase Activity. Int J Mol Sci. 2016 Oct 2;17(10):1672. doi: 10.3390/ijms17101672

Zoccarato A, Fields LH, Zaccolo M. Response to Wagner et al.: phosphodiesterase-2-anti-adrenergic friend or hypertrophic foe in heart disease? Naunyn Schmiedebergs Arch Pharmacol. 2016 Nov;389(11):1143-1145. doi: 10.1007/s00210-016-1301-z.

Ivan T, Enkvist E, Viira B, Manoharan GB, Raidaru G, Pflug A, Alam KA, Zaccolo M, Engh RA, Uri A. Bifunctional Ligands for Inhibition of Tight-Binding Protein-Protein Interactions. Bioconjug Chem. 2016 Aug 17;27(8):1900-10. doi: 10.1021/acs.bioconjchem.6b00293.

Lobo MJ, Amaral MD, Zaccolo M, Farinha CM EPAC1 activation by cAMP stabilizes CFTR at the membrane by promoting its interaction with NHERF1. J Cell Sci. 2016 Jul 1;129(13):2599-612. doi: 10.1242/jcs.185629.

Chay A, Zamparo I, Koschinski A, Zaccolo M, Blackwell KT. Control of βAR- and N-methyl-D-aspartate (NMDA) Receptor-Dependent cAMP Dynamics in Hippocampal Neurons. PLoS Comput Biol. 2016 Feb 22;12(2):e1004735. doi: 10.1371/journal.pcbi.1004735.

Abbattiscianni AC, Favia M, Mancini MT, Cardone RA, Guerra L, Monterisi S, Castellani S, Laselva O, Di Sole F, Conese M, Zaccolo M^, Casavola V^. Correctors of mutant CFTR enhance subcortical cAMP-PKA signaling through modulating ezrin phosphorylation and cytoskeleton organization. J Cell Sci. 2016 Mar 15;129(6):1128-40. doi: 10.1242/jcs.177907

^Joint corresponding authors

Shigeto M, Ramracheya R, Tarasov AI, Cha CY, Chibalina MV, Hastoy B, Philippaert K, Reinbothe T, Rorsman N, Salehi A, Sones WR, Vergari E, Weston C, Gorelik J, Katsura M, Nikolaev VO, Vennekens R, Zaccolo M, Galione A, Johnson PR, Kaku K, Ladds G, Rorsman. PGLP-1 stimulates insulin secretion by PKC-dependent TRPM4 and TRPM5 activation. J Clin Invest. 2015 Dec;125(12):4714-28. doi: 10.1172/JCI81975.

Fields LA, Koschinski A, Zaccolo M. Sustained exposure to catecholamines affects cAMP/PKA compartmentalised signalling in adult rat ventricular myocytes. Cell Signal. 2016 Jul;28(7):725-32. doi: 10.1016/j.cellsig.2015.10.003.

Zoccarato A, Surdo NC, Aronsen JM, Fields LA, Mancuso L, Dodoni G, Stangherlin A, Livie C, Jiang H, Sin YY, Gesellchen F, Terrin A, Baillie GS, Nicklin SA, Graham D, Szabo-Fresnais N, Krall J, Vandeput F, Movsesian M, Furlan L, Corsetti V, Hamilton G, Lefkimmiatis K, Sjaastad I, Zaccolo M. Cardiac Hypertrophy Is Inhibited by a Local Pool of cAMP Regulated by Phosphodiesterase 2. Circ Res. 2015 Sep 25;117(8):707-19. doi: 10.1161/CIRCRESAHA.114.305892

Recommended in F1000Prime as being of special significance in its field by F1000 Faculty

Li D, Lu CJ, Hao G, Wright H, Woodward L, Liu K, Vergari E, Surdo NC, Herring N, Zaccolo M, Paterson DJ. Efficacy of B-Type Natriuretic Peptide Is Coupled to Phosphodiesterase 2A in Cardiac Sympathetic Neurons. Hypertension. 2015 Jul;66(1):190-8. doi: 10.1161/HYPERTENSIONAHA.114.05054.

Parnell E, Koschinski A, Zaccolo M, Cameron RT, Baillie GS, Baillie GL, Porter A, McElroy SP, Yarwood SJ. Phosphorylation of ezrin on Thr567 is required for the synergistic activation of cell spreading by EPAC1 and protein kinase A in HEK293T cells. Biochim Biophys Acta. 2015 Jul;1853(7):1749-58. doi: 10.1016/j.bbamcr.2015.04.009.

Lomas O, Brescia M, Carnicer R, Monterisi S, Surdo NC, Zaccolo M. Adenoviral transduction of FRET-based biosensors for cAMP in primary adult mouse cardiomyocytes. Methods Mol Biol. 2015;1294:103-15. doi: 10.1007/978-1-4939-2537-7_8.

Koschinski A, Zaccolo M. A novel approach combining real-time imaging and the patch-clamp technique to calibrate FRET-based reporters for cAMP in their cellular microenvironment. Methods Mol Biol. 2015;1294:25-40. doi: 10.1007/978-1-4939-2537-7_3.

Maléth J, Balázs A, Pallagi P, Balla Z, Kui B, Katona M, Judák L, Németh I, Kemény LV, Rakonczay Z Jr, Venglovecz V, Földesi I, Pető Z, Somorácz Á, Borka K, Perdomo D, Lukacs GL, Gray MA, Monterisi S, Zaccolo M, Sendler M, Mayerle J, Kühn JP, Lerch MM, Sahin-Tóth M, Hegyi PAlcohol disrupts levels and function of the cystic fibrosis transmembrane conductance regulator to promote development of pancreatitis. Gastroenterology. 2015 Feb;148(2):427-39.e16. doi: 10.1053/j.gastro.2014.11.002

Lefkimmiatis K, Zaccolo M. cAMP signaling in subcellular compartments. Pharmacol Ther. 2014 Sep;143(3):295-304. doi: 10.1016/j.pharmthera.2014.03.008.

Lomas O, Zaccolo M. Phosphodiesterases maintain signaling fidelity via compartmentalization of cyclic nucleotides. Physiology (Bethesda). 2014 Mar;29(2):141-9. doi: 10.1152/physiol.00040.2013.

Stangherlin A, Koschinski A, Terrin A, Zoccarato A, Jiang H, Fields LA, Zaccolo M. Analysis of compartmentalized cAMP: a method to compare signals from differently targeted FRET reporters. Methods Mol Biol. 2014;1071:59-71. doi: 10.1007/978-1-62703-622-1_5

Monterisi S, Casavola V, Zaccolo M. Local modulation of cystic fibrosis conductance regulator: cytoskeleton and compartmentalized cAMP signalling. Br J Pharmacol. 2013 May;169(1):1-9. doi: 10.1111/bph.12017.

Terrin A, Monterisi S, Stangherlin A, Zoccarato A, Koschinski A, Surdo NC, Mongillo M, Sawa A, Jordanides NE, Mountford JC, Zaccolo M. PKA and PDE4D3 anchoring to AKAP9 provides distinct regulation of cAMP signals at the centrosome. J Cell Biol. 2012 Aug 20;198(4):607-21. doi: 10.1083/jcb.201201059.

Röder IV, Strack S, Reischl M, Dahley O, Khan MM, Kassel O, Zaccolo M, Rudolf R. Participation of myosin Va and Pka type I in the regeneration of neuromuscular junctions. PLoS One. 2012;7(7):e40860. doi: 10.1371/journal.pone.0040860.

Choi KR, Berrera M, Reischl M, Strack S, Albrizio M, Röder IV, Wagner A, Petersen Y, Hafner M, Zaccolo M, Rudolf R. Rapsyn mediates subsynaptic anchoring of PKA type I and stabilisation of acetylcholine receptor in vivo. J Cell Sci. 2012 Feb 1;125(Pt 3):714-23. doi: 10.1242/jcs.092361

Monterisi S, Favia M, Guerra L, Cardone RA, Marzulli D, Reshkin SJ, Casavola V, Zaccolo M. CFTR regulation in human airway epithelial cells requires integrity of the actin cytoskeleton and compartmentalized cAMP and PKA activity. J Cell Sci. 2012 Mar 1;125(Pt 5):1106-17. doi: 10.1242/jcs.089086.

Stangherlin A, Zaccolo M. cGMP-cAMP interplay in cardiac myocytes: a local affair with far-reaching consequences for heart function. Biochem Soc Trans. 2012 Feb;40(1):11-4. doi: 10.1042/BST20110655.

Parnell E, Smith BO, Palmer TM, Terrin A, Zaccolo M, Yarwood SJ. Regulation of the inflammatory response of vascular endothelial cells by EPAC1. Br J Pharmacol. 2012 May;166(2):434-46. doi: 10.1111/j.1476-5381.2011.01808.x.

Stangherlin A, Zaccolo M. Phosphodiesterases and subcellular compartmentalized cAMP signaling in the cardiovascular system. Am J Physiol Heart Circ Physiol. 2012 Jan;302(2):H379-90. doi: 10.1152/ajpheart.00766.2011.

Miller CL, Cai Y, Oikawa M, Thomas T, Dostmann WR, Zaccolo M, Fujiwara K, Yan C. Cyclic nucleotide phosphodiesterase 1A: a key regulator of cardiac fibroblast activation and extracellular matrix remodeling in the heart. Basic Res Cardiol. 2011 Nov;106(6):1023-39. doi: 10.1007/s00395-011-0228-2.

Zaccolo M. Spatial control of cAMP signalling in health and disease. Curr Opin Pharmacol. 2011 Dec;11(6):649-55. doi: 10.1016/j.coph.2011.09.014

Mohamed TMA, Oceandy D, Zi M, Prehar S, Alatwi N, Wang Y, Shaheen MA, Abou-Leisa R, Schelcher C, Hegab Z, Baudoin F, Emerson M, Mamas M, Di Benedetto G, Zaccolo M, Lei M, Cartwright EJ, Neyses L. Plasma membrane calcium pump (PMCA4)-neuronal nitric-oxide synthase complex regulates cardiac contractility through modulation of a compartmentalized cyclic nucleotide microdomain. J Biol Chem. 2011 Dec 2;286(48):41520-41529. doi: 10.1074/jbc.M111.290411

Stangherlin A, Zaccolo M. Local termination of 3'-5'-cyclic adenosine monophosphate signals: the role of A kinase anchoring protein-tethered phosphodiesterases. J Cardiovasc Pharmacol. 2011 Oct;58(4):345-53. doi: 10.1097/FJC.0b013e3182214f2b

Gesellchen F, Stangherlin A, Surdo N, Terrin A, Zoccarato A, Zaccolo M. Measuring spatiotemporal dynamics of cyclic AMP signaling in real-time using FRET-based biosensors. Methods Mol Biol. 2011;746:297-316. doi: 10.1007/978-1-61779-126-0_16.

Wilson LS, Baillie GS, Pritchard LM, Umana B, Terrin A, Zaccolo M, Houslay MD, Maurice DH. A phosphodiesterase 3B-based signaling complex integrates exchange protein activated by cAMP 1 and phosphatidylinositol 3-kinase signals in human arterial endothelial cells. J Biol Chem. 2011 May 6;286(18):16285-96. doi: 10.1074/jbc.M110.217026.

Sin YY, Edwards HV, Li X, Day JP, Christian F, Dunlop AJ, Adams DR, Zaccolo M, Houslay MD, Baillie GS. Disruption of the cyclic AMP phosphodiesterase-4 (PDE4)-HSP20 complex attenuates the β-agonist induced hypertrophic response in cardiac myocytes. J Mol Cell Cardiol. 2011 May;50(5):872-83. doi: 10.1016/j.yjmcc.2011.02.006.

Stangherlin A, Gesellchen F, Zoccarato A, Terrin A, Fields LA, Berrera M, Surdo NC, Craig MA, Smith G, Hamilton G, Zaccolo M. cGMP signals modulate cAMP levels in a compartment-specific manner to regulate catecholamine-dependent signaling in cardiac myocytes. Circ Res. 2011 Apr 15;108(8):929-39. doi: 10.1161/CIRCRESAHA.110.230698

Diskar M, Zenn HM, Kaupisch A, Kaufholz M, Brockmeyer S, Sohmen D, Berrera M, Zaccolo M, Boshart M, Herberg FW, Prinz A. Regulation of cAMP-dependent protein kinases: the human protein kinase X (PrKX) reveals the role of the catalytic subunit alphaH-alphaI loop. J Biol Chem. 2010 Nov 12;285(46):35910-8. doi: 10.1074/jbc.M110.155150.

Oliveira RF, Terrin A, Di Benedetto G, Cannon RC, Koh W, Kim M, Zaccolo M, Blackwell KT. The role of type 4 phosphodiesterases in generating microdomains of cAMP: large scale stochastic simulations. PLoS One. 2010 Jul 22;5(7):e11725. doi: 10.1371/journal.pone.0011725.

Vaasa A, Lust M, Terrin A, Uri A, Zaccolo M. Small-molecule FRET probes for protein kinase activity monitoring in living cells. Biochem Biophys Res Commun. 2010 Jul 9;397(4):750-5. doi: 10.1016/j.bbrc.2010.06.026.

Röder IV, Choi KR, Reischl M, Petersen Y, Diefenbacher ME, Zaccolo M, Pozzan T, Rudolf R. Myosin Va cooperates with PKA RIalpha to mediate maintenance of the endplate in vivo. Proc Natl Acad Sci U S A. 2010 Feb 2;107(5):2031-6. doi: 10.1073/pnas.0914087107.

Zaccolo M. cAMP signal transduction in the heart: understanding spatial control for the development of novel therapeutic strategies. Br J Pharmacol. 2009 Sep;158(1):50-60. doi: 10.1111/j.1476-5381.2009.00185.x.

Röder IV, Lissandron V, Martin J, Petersen Y, Di Benedetto G, Zaccolo M, Rudolf R. PKA microdomain organisation and cAMP handling in healthy and dystrophic muscle in vivo. Cell Signal. 2009 May;21(5):819-26. doi: 10.1016/j.cellsig.2009.01.029.

Maritan M, Monaco G, Zamparo I, Zaccolo M, Pozzan T, Lodovichi C. Odorant receptors at the growth cone are coupled to localized cAMP and Ca2+ increases. Proc Natl Acad Sci U S A. 2009 Mar 3;106(9):3537-42. doi: 10.1073/pnas.0813224106.Recommended in F1000Prime as being of special significance in its field by F1000 Faculty

Dal Molin F, Zornetta I, Puhar A, Tonello F, Zaccolo M, Montecucco C. cAMP imaging of cells treated with pertussis toxin, cholera toxin, and anthrax edema toxin. Biochem Biophys Res Commun. 2008 Nov 14;376(2):429-33. doi: 10.1016/j.bbrc.2008.09.012

Di Benedetto G, Zoccarato A, Lissandron V, Terrin A, Li X, Houslay MD, Baillie GS, Zaccolo M. Protein kinase A type I and type II define distinct intracellular signaling compartments. Circ Res. 2008 Oct 10;103(8):836-44. doi: 10.1161/CIRCRESAHA.108.174813.

Moll D, Prinz A, Brendel CM, Berrera M, Guske K, Zaccolo M, Genieser HG, Herberg FW. Biochemical characterization and cellular imaging of a novel, membrane permeable fluorescent cAMP analog. BMC Biochem. 2008 Jun 25;9:18. doi: 10.1186/1471-2091-9-1

Space and time-resolved gene expression experiments on cultured mammalian cells by a single-cell electroporation microarray. Vassanelli S, Bandiera L, Borgo M, Cellere G, Santoni L, Bersani C, Salamon M, Zaccolo M, Lorenzelli L, Girardi S, Maschietto M, Dal Maschio M, Paccagnella A. N Biotechnol. 2008 Jun;25(1):55-67. doi: 10.1016/j.nbt.2008.03.002

Berrera M, Dodoni G, Monterisi S, Pertegato V, Zamparo I, Zaccolo M. A toolkit for real-time detection of cAMP: insights into compartmentalized signaling. Handb Exp Pharmacol. 2008;(186):285-98. doi: 10.1007/978-3-540-72843-6_12

Ferlin A, Pepe A, Gianesello L, Garolla A, Feng S, Giannini S, Zaccolo M, Facciolli A, Morello R, Agoulnik AI, Foresta C. Mutations in the insulin-like factor 3 receptor are associated with osteoporosis. J Bone Miner Res. 2008 May;23(5):683-93. doi: 10.1359/jbmr.080204.

Webb RJ, Tinworth L, Thomas GM, Zaccolo M, Carroll J. Developmentally acquired PKA localisation in mouse oocytes and embryos. Dev Biol. 2008 May 1;317(1):36-45. doi: 10.1016/j.ydbio.2008.01.045.

Fanelli T, Cardone RA, Favia M, Guerra L, Zaccolo M, Monterisi S, De Santis T, Riccardi SM, Reshkin SJ, Casavola V. Beta-oestradiol rescues DeltaF508CFTR functional expression in human cystic fibrosis airway CFBE41o- cells through the up-regulation of NHERF1. Biol Cell. 2008 Jul;100(7):399-412. doi: 10.1042/BC20070095.

Li C, Krishnamurthy PC, Penmatsa H, Marrs KL, Wang XQ, Zaccolo M, Jalink K, Li M, Nelson DJ, Schuetz JD, Naren AP Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell. 2007 Nov 30;131(5):940-51. doi: 10.1016/j.cell.2007.09.037

Beffagna G, De Bortoli M, Nava A, Salamon M, Lorenzon A, Zaccolo M, Mancuso L, Sigalotti L, Bauce B, Occhi G, Basso C, Lanfranchi G, Towbin JA, Thiene G, Danieli GA, Rampazzo A. Missense mutations in desmocollin-2 N-terminus, associated with arrhythmogenic right ventricular cardiomyopathy, affect intracellular localization of desmocollin-2 in vitro. BMC Med Genet. 2007 Oct 26;8:65. doi: 10.1186/1471-2350-8-65

Lygren B, Carlson CR, Santamaria K, Lissandron V, McSorley T, Litzenberg J, Lorenz D, Wiesner B, Rosenthal W, Zaccolo M, Taskén K, Klussmann E. AKAP complex regulates Ca2+ re-uptake into heart sarcoplasmic reticulum. EMBO Rep. 2007 Nov;8(11):1061-7. doi: 10.1038/sj.embor.7401081

Lissandron V, Rossetto MG, Erbguth K, Fiala A, Daga A, Zaccolo M. Transgenic fruit-flies expressing a FRET-based sensor for in vivo imaging of cAMP dynamics. Cell Signal. 2007 Nov;19(11):2296-303. doi: 10.1016/j.cellsig.2007.07.004

Recommended in F1000Prime as being of special significance in its field by F1000 Faculty

Zaccolo M, Movsesian MA. cAMP and cGMP signaling cross-talk: role of phosphodiesterases and implications for cardiac pathophysiology. Circ Res. 2007 Jun 8;100(11):1569-78. doi: 10.1161/CIRCRESAHA.106.144501.

Hernandez VH, Bortolozzi M, Pertegato V, Beltramello M, Giarin M, Zaccolo M, Pantano S, Mammano F. Unitary permeability of gap junction channels to second messengers measured by FRET microscopy. Nat Methods. 2007 Apr;4(4):353-8. doi: 10.1038/nmeth1031

Dunn TA, Wang CT, Colicos MA, Zaccolo M, DiPilato LM, Zhang J, Tsien RY, Feller MB. Imaging of cAMP levels and protein kinase A activity reveals that retinal waves drive oscillations in second-messenger cascades. J Neurosci. 2006 Dec 6;26(49):12807-15. doi: 10.1523/JNEUROSCI.3238-06.2006.

Tocchetti CG, Wang W, Froehlich JP, Huke S, Aon MA, Wilson GM, Di Benedetto G, O'Rourke B, Gao WD, Wink DA, Toscano JP, Zaccolo M, Bers DM, Valdivia HH, Cheng H, Kass DA, Paolocci N. Nitroxyl improves cellular heart function by directly enhancing cardiac sarcoplasmic reticulum Ca2+ cycling. Circ Res. 2007 Jan 5;100(1):96-104. doi: 10.1161/01.RES.0000253904.53601.c9

Terrin A, Di Benedetto G, Pertegato V, Cheung YF, Baillie G, Lynch MJ, Elvassore N, Prinz A, Herberg FW, Houslay MD, Zaccolo M. PGE(1) stimulation of HEK293 cells generates multiple contiguous domains with different [cAMP]]: role of compartmentalized phosphodiesterases. J Cell Biol. 2006 Nov 6;175(3):441-51. doi: 10.1083/jcb.200605050

Dal Molin F, Tonello F, Ladant D, Zornetta I, Zamparo I, Di Benedetto G, Zaccolo M, Montecucco C. Cell entry and cAMP imaging of anthrax edema toxin. EMBO J. 2006 Nov 15;25(22):5405-13. doi: 10.1038/sj.emboj.7601408.

Schmid A, Bai G, Schmid N, Zaccolo M, Ostrowski LE, Conner GE, Fregien N, Salathe M. Real-time analysis of cAMP-mediated regulation of ciliary motility in single primary human airway epithelial cells. J Cell Sci. 2006 Oct 15;119(Pt 20):4176-86. doi: 10.1242/jcs.03181

Lissandron V, Zaccolo M. Compartmentalized cAMP/PKA signalling regulates cardiac excitation-contraction coupling. J Muscle Res Cell Motil. 2006;27(5-7):399-403. doi: 10.1007/s10974-006-9077-2.

Mongillo M, Zaccolo M. A complex phosphodiesterase system controls beta-adrenoceptor signalling in cardiomyocytes. Biochem Soc Trans. 2006 Aug;34(Pt 4):510-1. doi: 10.1042/BST0340510.

Zaccolo M, Di Benedetto G, Lissandron V, Mancuso L, Terrin A, Zamparo I. Restricted diffusion of a freely diffusible second messenger: mechanisms underlying compartmentalized cAMP signalling. Biochem Soc Trans. 2006 Aug;34(Pt 4):495-7. doi: 10.1042/BST0340495.

Zaccolo M. Phosphodiesterases and compartmentalized cAMP signalling in the heart. Eur J Cell Biol. 2006 Jul;85(7):693-7. doi: 10.1016/j.ejcb.2006.01.002.

Mongillo M, Tocchetti CG, Terrin A, Lissandron V, Cheung YF, Dostmann WR, Pozzan T, Kass DA, Paolocci N, Houslay MD, Zaccolo M. Compartmentalized phosphodiesterase-2 activity blunts beta-adrenergic cardiac inotropy via an NO/cGMP-dependent pathway. Circ Res. 2006 Feb 3;98(2):226-34. doi: 10.1161/01.RES.0000200178.34179.93.

Lissandron V, Terrin A, Collini M, D'alfonso L, Chirico G, Pantano S, Zaccolo M. Improvement of a FRET-based indicator for cAMP by linker design and stabilization of donor-acceptor interaction. J Mol Biol. 2005 Dec 2;354(3):546-55. doi: 10.1016/j.jmb.2005.09.089.

Gerbino A, Ruder WC, Curci S, Pozzan T, Zaccolo M, Hofer AM. Termination of cAMP signals by Ca2+ and G(alpha)i via extracellular Ca2+ sensors: a link to intracellular Ca2+ oscillations. J Cell Biol. 2005 Oct 24;171(2):303-12. doi: 10.1083/jcb.200507054.

Zaccolo M, Cesetti T, Di Benedetto G, Mongillo M, Lissandron V, Terrin A, Zamparo I Imaging the cAMP-dependent signal transduction pathway. Biochem Soc Trans. 2005 Dec;33(Pt 6):1323-6. doi: 10.1042/BST20051323.

Mongillo M, Terrin A, Evellin S, Lissandron V, Zaccolo M. Study of cyclic adenosine monophosphate microdomains in cells. Methods Mol Biol. 2005;307:1-13. doi: 10.1385/1-59259-839-0:001.

Pantano S, Zaccolo M, Carloni P Molecular basis of the allosteric mechanism of cAMP in the regulatory PKA subunit. FEBS Lett. 2005 May 9;579(12):2679-85. doi: 10.1016/j.febslet.2005.02.084.

Cardone RA, Bagorda A, Bellizzi A, Busco G, Guerra L, Paradiso A, Casavola V, Zaccolo M, Reshkin SJ. Protein kinase A gating of a pseudopodial-located RhoA/ROCK/p38/NHE1 signal module regulates invasion in breast cancer cell lines. Mol Biol Cell. 2005 Jul;16(7):3117-27. doi: 10.1091/mbc.e04-10-0945.

Warrier S, Belevych AE, Ruse M, Eckert RL, Zaccolo M, Pozzan T, Harvey RD. Beta-adrenergic- and muscarinic receptor-induced changes in cAMP activity in adult cardiac myocytes detected with FRET-based biosensor. Am J Physiol Cell Physiol. 2005 Aug;289(2):C455-61. doi: 10.1152/ajpcell.00058.2005.

Caccia M, Camozzi E, Collini M, Zaccolo M, Chirico G. Photon moment analysis in cells in the presence of photo-bleaching. Appl Spectrosc. 2005 Feb;59(2):227-36. doi: 10.1366/0003702053084981.

Takimoto E, Champion HC, Belardi D, Moslehi J, Mongillo M, Mergia E, Montrose DC, Isoda T, Aufiero K, Zaccolo M, Dostmann WR, Smith CJ, Kass DA cGMP catabolism by phosphodiesterase 5A regulates cardiac adrenergic stimulation by NOS3-dependent mechanism. Circ Res. 2005 Jan 7;96(1):100-9. doi: 10.1161/01.RES.0000152262.22968.72.

Ponsioen B, Zhao J, Riedl J, Zwartkruis F, van der Krogt G, Zaccolo M, Moolenaar WH, Bos JL, Jalink K. Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep. 2004 Dec;5(12):1176-80. doi: 10.1038/sj.embor.7400290.

Abrahamsen H, Baillie G, Ngai J, Vang T, Nika K, Ruppelt A, Mustelin T, Zaccolo M, Houslay M, Taskén K. TCR- and CD28-mediated recruitment of phosphodiesterase 4 to lipid rafts potentiates TCR signaling. J Immunol. 2004 Oct 15;173(8):4847-58. doi: 10.4049/jimmunol.173.8.4847.

Mongillo M, McSorley T, Evellin S, Sood A, Lissandron V, Terrin A, Huston E, Hannawacker A, Lohse MJ, Pozzan T, Houslay MD, Zaccolo M. Fluorescence resonance energy transfer-based analysis of cAMP dynamics in live neonatal rat cardiac myocytes reveals distinct functions of compartmentalized phosphodiesterases. Circ Res. 2004 Jul 9;95(1):67-75. doi: 10.1161/01.RES.0000134629.84732.11

Evellin S, Mongillo M, Terrin A, Lissandron V, Zaccolo M. Measuring dynamic changes in cAMP using fluorescence resonance energy transfer. Methods Mol Biol. 2004;284:259-70. doi: 10.1385/1-59259-816-1:259.

Zaccolo M. Use of chimeric fluorescent proteins and fluorescence resonance energy transfer to monitor cellular responses. Circ Res. 2004 Apr 16;94(7):866-73. doi: 10.1161/01.RES.0000123825.83803.CD.

Salamon M, Millino C, Raffaello A, Mongillo M, Sandri C, Bean C, Negrisolo E, Pallavicini A, Valle G, Zaccolo M, Schiaffino S, Lanfranchi G. Human MYO18B, a novel unconventional myosin heavy chain expressed in striated muscles moves into the myonuclei upon differentiation. J Mol Biol. 2003 Feb 7;326(1):137-49. doi: 10.1016/s0022-2836(02)01335-9.

Zaccolo M, Pozzan T. cAMP and Ca2+ interplay: a matter of oscillation patterns. Trends Neurosci. 2003 Feb;26(2):53-5. doi: 10.1016/s0166-2236(02)00017-6.

Zaccolo M. Selection of functional antibodies on the basis of valency. Methods Mol Biol. 2002;178:255-8. doi: 10.1385/1-59259-240-6:255.

Zaccolo M, Magalhães P, Pozzan T. Compartmentalisation of cAMP and Ca(2+) signals. Curr Opin Cell Biol. 2002 Apr;14(2):160-6. doi: 10.1016/s0955-0674(02)00316-2.

Zaccolo M^, Pozzan T^. Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science. 2002 Mar 1;295(5560):1711-5. doi: 10.1126/science.1069982. ^Joint corresponding authors

Bastianutto C, Bestard JA, Lahnakoski K, Broere D, De Visser M, Zaccolo M, Pozzan T, Ferlini A, Muntoni F, Patarnello T, Klamut HJ. Dystrophin muscle enhancer 1 is implicated in the activation of non-muscle isoforms in the skeletal muscle of patients with X-linked dilated cardiomyopathy. Hum Mol Genet. 2001 Nov 1;10(23):2627-35. doi: 10.1093/hmg/10.23.2627.

Zaccolo M, Filippin L, Magalhães P, Pozzan T. Heterogeneity of second messenger levels in living cells. Novartis Found Symp. 2001;239:85-93; discussion 93-5, 150-9. doi: 10.1002/0470846674.ch8.

Zaccolo M, Pozzan T. Imaging signal transduction in living cells with GFP-based probes. IUBMB Life. 2000 May;49(5):375-9. doi: 10.1080/152165400410218.

Zaccolo M, De Giorgi F, Cho CY, Feng L, Knapp T, Negulescu PA, Taylor SS, Tsien RY, Pozzan T. A genetically encoded, fluorescent indicator for cyclic AMP in living cells. Nat Cell Biol. 2000 Jan;2(1):25-9. doi: 10.1038/71345.

Zaccolo M, Gherardi E. The effect of high-frequency random mutagenesis on in vitro protein evolution: a study on TEM-1 beta-lactamase. J Mol Biol. 1999 Jan 15;285(2):775-83. doi: 10.1006/jmbi.1998.2262.

Zaccolo M, Griffiths AP, Prospero TD, Winter G, Gherardi E. Dimerization of Fab fragments enables ready screening of phage antibodies that affect hepatocyte growth factor/scatter factor activity on target cells. Eur J Immunol. 1997 Mar;27(3):618-23. doi: 10.1002/eji.1830270307.

Zaccolo M, Williams DM, Brown DM, Gherardi E. An approach to random mutagenesis of DNA using mixtures of triphosphate derivatives of nucleoside analogues. J Mol Biol. 1996 Feb 2;255(4):589-603. doi: 10.1006/jmbi.1996.0049.

Vola R, Lombardi A, Tarditi L, Zaccolo M, Neri D, Björck L, Mariani M. Recombinant proteins L and LG. Two new tools for purification of murine antibody fragments. Cell Biophys. 1994;24-25:27-36. doi: 10.1007/BF02789212.

Zaccolo M, Malavasi F. From cells to genes: how to make antibodies useful in human diagnosis and therapy. Int J Clin Lab Res. 1993;23(4):192-8. doi: 10.1007/BF02592308.

Zaccolo M, Roggero S, Armellini D, Pegoraro L, Rappuoli R, Malavasi F. Generation of human monoclonal antibodies that confer protection against pertussis toxin. Infect Immun. 1992 Mar;60(3):1258-60. doi: 10.1128/iai.60.3.1258-1260.1992.

Funaro A, Spagnoli GC, Ausiello CM, Alessio M, Roggero S, Delia D, Zaccolo M, Malavasi F Involvement of the multilineage CD38 molecule in a unique pathway of cell activation and proliferation. J Immunol. 1990 Oct 15;145(8):2390-6. PMID: 1976692

Alessio M, Bellone G, Funaro A, De Monte LB, Roggero S, Peruzzi L, Zaccolo M, Momo M, Cappa AP, Malavasi F. Characterization by monoclonal antibody of a highly conserved antigenic determinant expressed on human platelet membranes and intermediate filament type III. Scand J Immunol. 1990 May;31(5):609-17. doi: 10.1111/j.1365-3083.1990.tb02812.x.

Peruzzi L, Melioli G, De Monte LB, Alessio M, Zaccolo M, Roggero S, Bellone G, Funaro A, Malavasi F. Microplate selection technique (MPST). A new method for selecting mouse transfectants expressing human gene products. J Immunol Methods. 1989 Sep 29;123(1):113-21. doi: 10.1016/0022-1759(89)90035-5.

Genzano F, Funaro A, Alessio M, De Monte LB, Bellone G, Peruzzi L, Zaccolo M, Caligari-Cappino F, Malavasi F Generation and characterization of a murine monoclonal antibody specific for the human T1-CD5 molecule. Int J Biol Markers. 1987 Sep-Dec;2(3):143-50. PMID: 3330108