The 10th International Conference on cGMP 2022: recent trends in cGMP research and development-meeting report.
Guanylyl cyclases
Mosliciguat
NO-GC
Natriuretic peptides
Nitric oxide
Phosphodiesterases
Praliciguat
Riociguat
Runcaciguat
Vericiguat
cGMP
sGC activators
sGC stimulators
Journal
Naunyn-Schmiedeberg's archives of pharmacology
ISSN: 1432-1912
Titre abrégé: Naunyn Schmiedebergs Arch Pharmacol
Pays: Germany
ID NLM: 0326264
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
received:
10
01
2023
accepted:
31
03
2023
medline:
14
7
2023
pubmed:
20
4
2023
entrez:
20
04
2023
Statut:
ppublish
Résumé
Increasing cGMP is a unique therapeutic principle, and drugs inhibiting cGMP-degrading enzymes or stimulating cGMP production are approved for the treatment of various diseases such as erectile dysfunction, coronary artery disease, pulmonary hypertension, chronic heart failure, irritable bowel syndrome, or achondroplasia. In addition, cGMP-increasing therapies are preclinically profiled or in clinical development for quite a broad set of additional indications, e.g., neurodegenerative diseases or different forms of dementias, bone formation disorders, underlining the pivotal role of cGMP signaling pathways. The fundamental understanding of the signaling mediated by nitric oxide-sensitive (soluble) guanylyl cyclase and membrane-associated receptor (particulate) guanylyl cyclase at the molecular and cellular levels, as well as in vivo, especially in disease models, is a key prerequisite to fully exploit treatment opportunities and potential risks that could be associated with an excessive increase in cGMP. Furthermore, human genetic data and the clinical effects of cGMP-increasing drugs allow back-translation into basic research to further learn about signaling and treatment opportunities. The biannual international cGMP conference, launched nearly 20 years ago, brings all these aspects together as an established and important forum for all topics from basic science to clinical research and pivotal clinical trials. This review summarizes the contributions to the "10th cGMP Conference on cGMP Generators, Effectors and Therapeutic Implications," which was held in Augsburg in 2022 but will also provide an overview of recent key achievements and activities in the field of cGMP research.
Identifiants
pubmed: 37079081
doi: 10.1007/s00210-023-02484-8
pii: 10.1007/s00210-023-02484-8
pmc: PMC10338386
doi:
Substances chimiques
Guanylate Cyclase
EC 4.6.1.2
Soluble Guanylyl Cyclase
EC 4.6.1.2
Cyclic GMP
H2D2X058MU
Nitric Oxide
31C4KY9ESH
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1669-1686Informations de copyright
© 2023. The Author(s).
Références
Armstrong PW, Roessig L, Patel MJ, Anstrom KJ, Butler J, Voors AA, Lam CSP, Ponikowski P, Temple T, Pieske B, Ezekowitz J, Hernandez AF, Koglin J, O’Connor CM (2018) A multicenter, randomized, double-blind, placebo-controlled trial of the efficacy and safety of the oral soluble guanylate cyclase stimulator: the VICTORIA trial. JACC Heart Fail 6:96–104
pubmed: 29032136
doi: 10.1016/j.jchf.2017.08.013
Armstrong PW, Lam CSP, Anstrom KJ, Ezekowitz J, Hernandez AF, O’Connor CM, Pieske B, Ponikowski P, Shah SJ, Solomon SD, Voors AA, She L, Vlajnic V, Carvalho F, Bamber L, Blaustein RO, Roessig L, Butler J, Group VI-HS (2020) Effect of vericiguat vs placebo on quality of life in patients with heart failure and preserved ejection fraction: the VITALITY-HFpEF randomized clinical trial. JAMA 324:1512–1521
pubmed: 33079152
doi: 10.1001/jama.2020.15922
Aslam MI, Hahn VS, Jani V, Hsu S, Sharma K, Kass DA (2021) Reduced right ventricular sarcomere contractility in heart failure with preserved ejection fraction and severe obesity. Circulation 143:965–967
pubmed: 33370156
doi: 10.1161/CIRCULATIONAHA.120.052414
Barret DCA, Kaupp UB, Marino J (2022) The structure of cyclic nucleotide-gated channels in rod and cone photoreceptors. Trends Neurosci 45:763–776
pubmed: 35934530
doi: 10.1016/j.tins.2022.07.001
Becker-Pelster EM, Hahn MG, Delbeck M, Dietz L, Huser J, Kopf J, Kraemer T, Marquardt T, Mondritzki T, Nagelschmitz J, Nikkho SM, Pires PV, Tinel H, Weimann G, Wunder F, Sandner P, Schuhmacher J, Stasch JP, Truebel HKF (2022) Inhaled mosliciguat (BAY 1237592): targeting pulmonary vasculature via activating apo-sGC. Respir Res 23:272
pubmed: 36183104
pmcid: 9526466
doi: 10.1186/s12931-022-02189-1
Benardeau A, Kahnert A, Schomber T, Meyer J, Pavkovic M, Kretschmer A, Lawrenz B, Hartmann E, Mathar I, Hueser J, Kraehling JR, Eitner F, Hahn MG, Stasch JP, Sandner P (2021) Runcaciguat, a novel soluble guanylate cyclase activator, shows renoprotection in hypertensive, diabetic, and metabolic preclinical models of chronic kidney disease. Naunyn Schmiedebergs Arch Pharmacol 394:2363–2379
pubmed: 34550407
pmcid: 8592982
doi: 10.1007/s00210-021-02149-4
Beuve A, Wu C, Cui C, Liu T, Jain MR, Huang C, Yan L, Kholodovych V, Li H (2016) Identification of novel S-nitrosation sites in soluble guanylyl cyclase, the nitric oxide receptor. J Proteomics 138:40–47
pubmed: 26917471
pmcid: 5066868
doi: 10.1016/j.jprot.2016.02.009
Bork NI, Kuret A, Cruz Santos M, Molina CE, Reiter B, Reichenspurner H, Friebe A, Skryabin BV, Rozhdestvensky TS, Kuhn M, Lukowski R, Nikolaev VO (2021) Rise of cGMP by partial phosphodiesterase-3A degradation enhances cardioprotection during hypoxia. Redox Biol 48:102179
pubmed: 34763298
pmcid: 8590074
doi: 10.1016/j.redox.2021.102179
Butler J, Lam CSP, Anstrom KJ, Ezekowitz J, Hernandez AF, O’Connor CM, Pieske B, Ponikowski P, Shah SJ, Solomon SD, Voors AA, Wu Y, Carvalho F, Bamber L, Blaustein RO, Roessig L, Armstrong PW (2019) Rationale and design of the VITALITY-HFpEF trial. Circ Heart Fail 12:e005998
pubmed: 31096775
doi: 10.1161/CIRCHEARTFAILURE.119.005998
Calamaras TD, Pande S, Baumgartner RA, Kim SK, McCarthy JC, Martin GL, Tam K, McLaughlin AL, Wang GR, Aronovitz MJ, Lin W, Aguirre JI, Baca P, Liu P, Richards DA, Davis RJ, Karas RH, Jaffe IZ, Blanton RM (2021) MLK3 mediates impact of PKG1alpha on cardiac function and controls blood pressure through separate mechanisms. JCI Insight 6(18):e149075. https://doi.org/10.1172/jci.insight.149075
Ceddia RP, Liu D, Shi F, Crowder MK, Mishra S, Kass DA, Collins S (2021) Increased energy expenditure and protection from diet-induced obesity in mice lacking the cgmp-specific phosphodiesterase PDE9. Diabetes 70:2823–2836
pubmed: 34620617
pmcid: 8660992
doi: 10.2337/db21-0100
Correia SS, Iyengar RR, Germano P, Tang K, Bernier SG, Schwartzkopf CD, Tobin J, Lee TW, Liu G, Jacobson S, Carvalho A, Rennie GR, Jung J, Renhowe PA, Lonie E, Winrow CJ, Hadcock JR, Jones JE, Currie MG (2021a) The CNS-penetrant soluble guanylate cyclase stimulator CY6463 reveals its therapeutic potential in neurodegenerative diseases. Front Pharmacol 12:656561
pubmed: 34108877
pmcid: 8181742
doi: 10.3389/fphar.2021.656561
Correia SS, Liu G, Jacobson S, Bernier SG, Tobin JV, Schwartzkopf CD, Atwater E, Lonie E, Rivers S, Carvalho A, Germano P, Tang K, Iyengar RR, Currie MG, Hadcock JR, Winrow CJ, Jones JE (2021b) The CNS-penetrant soluble guanylate cyclase stimulator CYR119 attenuates markers of inflammation in the central nervous system. J Neuroinflammation 18:213
pubmed: 34537066
pmcid: 8449877
doi: 10.1186/s12974-021-02275-z
Cui C, Wu C, Shu P, Liu T, Li H, Beuve A (2022) Soluble guanylyl cyclase mediates noncanonical nitric oxide signaling by nitrosothiol transfer under oxidative stress. Redox Biol 55:102425
pubmed: 35961098
pmcid: 9372771
doi: 10.1016/j.redox.2022.102425
Dai Y, Faul EM, Ghosh A, Stuehr DJ (2022) NO rapidly mobilizes cellular heme to trigger assembly of its own receptor. Proc Natl Acad Sci U S A 119(4):e2115774119. https://doi.org/10.1073/pnas.2115774119
de la Fuente-Alonso A, Toral M, Alfayate A, Ruiz-Rodriguez MJ, Bonzon-Kulichenko E, Teixido-Tura G, Martinez-Martinez S, Mendez-Olivares MJ, Lopez-Maderuelo D, Gonzalez-Valdes I, Garcia-Izquierdo E, Mingo S, Martin CE, Muino-Mosquera L, De Backer J, Nistal JF, Forteza A, Evangelista A, Vazquez J, Campanero MR, Redondo JM (2021) Aortic disease in Marfan syndrome is caused by overactivation of sGC-PRKG signaling by NO. Nat Commun 12:2628
pubmed: 33976159
pmcid: 8113458
doi: 10.1038/s41467-021-22933-3
Egbert JR, Uliasz TF, Lowther KM, Kaback D, Wagner BM, Healy CL, O’Connell TD, Potter LR, Jaffe LA, Yee SP (2022) Epitope-tagged and phosphomimetic mouse models for investigating natriuretic peptide-stimulated receptor guanylyl cyclases. Front Mol Neurosci 15:1007026
pubmed: 36340689
pmcid: 9627482
doi: 10.3389/fnmol.2022.1007026
Emdin M, Aimo A, Castiglione V, Vergaro G, Georgiopoulos G, Saccaro LF, Lombardi CM, Passino C, Cerbai E, Metra M, Senni M (2020) Targeting cyclic guanosine monophosphate to treat heart failure: JACC Review Topic of the Week. J Am Coll Cardiol 76:1795–1807
pubmed: 33032741
doi: 10.1016/j.jacc.2020.08.031
Follmann M, Ackerstaff J, Redlich G, Wunder F, Lang D, Kern A, Fey P, Griebenow N, Kroh W, Becker-Pelster EM, Kretschmer A, Geiss V, Li V, Straub A, Mittendorf J, Jautelat R, Schirok H, Schlemmer KH, Lustig K, Gerisch M, Knorr A, Tinel H, Mondritzki T, Trubel H, Sandner P, Stasch JP (2017) Discovery of the soluble guanylate cyclase stimulator vericiguat (BAY 1021189) for the treatment of chronic heart failure. J Med Chem 60:5146–5161
pubmed: 28557445
doi: 10.1021/acs.jmedchem.7b00449
Frankenreiter S, Groneberg D, Kuret A, Krieg T, Ruth P, Friebe A, Lukowski R (2018) Cardioprotection by ischemic postconditioning and cyclic guanosine monophosphate-elevating agents involves cardiomyocyte nitric oxide-sensitive guanylyl cyclase. Cardiovasc Res 114:822–829
pubmed: 29438488
doi: 10.1093/cvr/cvy039
Friebe A, Voussen B, Groneberg D (2018) NO-GC in cells “off the beaten track.” Nitric Oxide Biol Chem 77:12–18
doi: 10.1016/j.niox.2018.03.020
Garthwaite J (2019) NO as a multimodal transmitter in the brain: discovery and current status. Br J Pharmacol 176:197–211
pubmed: 30399649
doi: 10.1111/bph.14532
Gheorghiade M, Greene SJ, Butler J, Filippatos G, Lam CS, Maggioni AP, Ponikowski P, Shah SJ, Solomon SD, Kraigher-Krainer E, Samano ET, Muller K, Roessig L, Pieske B, Investigators S-R, Coordinators, (2015) Effect of Vericiguat, a soluble guanylate cyclase stimulator, on natriuretic peptide levels in patients with worsening chronic heart failure and reduced ejection fraction: the SOCRATES-REDUCED randomized trial. JAMA 314:2251–2262
pubmed: 26547357
doi: 10.1001/jama.2015.15734
Ghosh A, Stasch JP, Papapetropoulos A, Stuehr DJ (2014) Nitric oxide and heat shock protein 90 activate soluble guanylate cyclase by driving rapid change in its subunit interactions and heme content. J Biol Chem 289:15259–15271
pubmed: 24733395
pmcid: 4140884
doi: 10.1074/jbc.M114.559393
Giesen J, Mergia E, Koesling D, Russwurm M (2022) Hippocampal AMPA- and NMDA-induced cGMP signals are mainly generated by NO-GC2 and are under tight control by PDEs 1 and 2. Eur J Neurosci 55:18–31
pubmed: 34902209
doi: 10.1111/ejn.15564
Goetz KR, Sprenger JU, Perera RK, Steinbrecher JH, Lehnart SE, Kuhn M, Gorelik J, Balligand JL, Nikolaev VO (2014) Transgenic mice for real-time visualization of cGMP in intact adult cardiomyocytes. Circ Res 114:1235–1245
doi: 10.1161/CIRCRESAHA.114.302437
Habek N, Dobrivojevic Radmilovic M, Kordic M, Ilic K, Grgic S, Farkas V, Bagaric R, Skokic S, Svarc A, Dugandzic A (2020) Activation of brown adipose tissue in diet-induced thermogenesis is GC-C dependent. Pflugers Arch 472:405–417
pubmed: 31940065
doi: 10.1007/s00424-020-02347-8
Hahn MG, Lampe T, El Sheikh S, Griebenow N, Woltering E, Schlemmer KH, Dietz L, Gerisch M, Wunder F, Becker-Pelster EM, Mondritzki T, Tinel H, Knorr A, Kern A, Lang D, Hueser J, Schomber T, Benardeau A, Eitner F, Truebel H, Mittendorf J, Kumar V, van den Akker F, Schaefer M, Geiss V, Sandner P, Stasch JP (2021) Discovery of the soluble guanylate cyclase activator runcaciguat (BAY 1101042). J Med Chem 64:5323–5344
pubmed: 33872507
doi: 10.1021/acs.jmedchem.0c02154
Hochheiser J, Haase T, Busker M, Sommer A, Kreienkamp HJ, Behrends S (2016) Heterodimerization with the beta1 subunit directs the alpha2 subunit of nitric oxide-sensitive guanylyl cyclase to calcium-insensitive cell-cell contacts in HEK293 cells: Interaction with Lin7a. Biochem Pharmacol 122:23–32
pubmed: 27793718
doi: 10.1016/j.bcp.2016.10.008
Hofmann F (2020) The cGMP system: components and function. Biol Chem 401:447–469
pubmed: 31747372
doi: 10.1515/hsz-2019-0386
Horiuchi Y, Villacorta H, Maisel AS (2022) Natriuretic peptide-guided therapy for heart failure. Heart Int 16:112–116
pubmed: 36741100
pmcid: 9872778
doi: 10.17925/HI.2022.16.2.112
Horst BG, Yokom AL, Rosenberg DJ, Morris KL, Hammel M, Hurley JH, Marletta MA (2019) Allosteric activation of the nitric oxide receptor soluble guanylate cyclase mapped by cryo-electron microscopy. eLife 8:e50634. https://doi.org/10.7554/eLife.50634
Ichiki T, Jinno A, Tsuji Y (2022) Natriuretic peptide-based novel therapeutics: long journeys of drug developments optimized for disease states. Biology (Basel) 11(6):859. https://doi.org/10.3390/biology11060859
Kalyanaraman H, Pal China S, Cabriales JA, Moininazeri J, Casteel DE, Garcia JJ, Wong VW, Chen A, Sah RL, Boss GR, Pilz RB (2022) Protein kinase G2 is essential for skeletal homeostasis and adaptation to mechanical loading in male but not female mice. J Bone Miner Res 38(1):171–185. https://doi.org/10.1002/jbmr.4746
Kamynina A, Guttzeit S, Eaton P, Cuello F (2022) Nitroxyl Donor CXL-1020 Lowers blood pressure by targeting C195 in cyclic guanosine-3’,5’-monophosphate-dependent protein kinase I. Hypertension 79:946–956
pubmed: 35168371
doi: 10.1161/HYPERTENSIONAHA.122.18756
Kang Y, Liu R, Wu JX, Chen L (2019) Structural insights into the mechanism of human soluble guanylate cyclase. Nature 574:206–210
pubmed: 31514202
doi: 10.1038/s41586-019-1584-6
Kim SM, Yuen T, Iqbal J, Rubin MR, Zaidi M (2021) The NO-cGMP-PKG pathway in skeletal remodeling. Ann N Y Acad Sci 1487:21–30
pubmed: 32860248
doi: 10.1111/nyas.14486
Kuhn M (2016) Molecular physiology of membrane guanylyl cyclase receptors. Physiol Rev 96:751–804
pubmed: 27030537
doi: 10.1152/physrev.00022.2015
Leineweber K, Moosmang S, Paulson D (2017) Genetics of NO deficiency. Am J Cardiol 120:S80–S88
pubmed: 29025574
doi: 10.1016/j.amjcard.2017.06.013
Liu R, Kang Y, Chen L (2021) Activation mechanism of human soluble guanylate cyclase by stimulators and activators. Nat Commun 12(1):5492. https://doi.org/10.1038/s41467-021-25617-0
Liu PW, Martin GL, Lin W, Huang W, Pande S, Aronovitz MJ, Davis RJ, Blanton RM (2022) Mixed lineage kinase 3 requires a functional CRIB domain for regulation of blood pressure, cardiac hypertrophy, and left ventricular function. Am J Physiol Heart Circ Physiol 323:H513–H522
pubmed: 35867711
doi: 10.1152/ajpheart.00660.2021
Lukowski R, Feil R (2022) Recent developments in cGMP research: from mechanisms to medicines and back. Br J Pharmacol 179:2321–2327
pubmed: 35332531
doi: 10.1111/bph.15824
Lundberg JO, Weitzberg E (2022) Nitric oxide signaling in health and disease. Cell 185:2853–2878
pubmed: 35931019
doi: 10.1016/j.cell.2022.06.010
Ly OT, Chen H, Brown GE, Hong L, Wang X, Han YD, Pavel MA, Sridhar A, Maienschein-Cline M, Chalazan B, Ong SG, Abdelhady K, Massad M, Rizkallah LE, Rehman J, Khetani SR, Darbar D (2022) Mutant ANP induces mitochondrial and ion channel remodeling in a human iPSC-derived atrial fibrillation model. JCI Insight 7(7):e155640. https://doi.org/10.1172/jci.insight.155640
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 (2022) CNP regulates cardiac contractility and increases cGMP near both SERCA and TnI: difference from BNP visualized by targeted cGMP biosensors. Cardiovasc Res 118:1506–1519
pubmed: 33970224
doi: 10.1093/cvr/cvab167
Markham A, Duggan S (2021) Vericiguat: first approval. Drugs 81:721–726
pubmed: 33770393
doi: 10.1007/s40265-021-01496-z
McMurray JJV, Jackson AM, Lam CSP, Redfield MM, Anand IS, Ge J, Lefkowitz MP, Maggioni AP, Martinez F, Packer M, Pfeffer MA, Pieske B, Rizkala AR, Sabarwal SV, Shah AM, Shah SJ, Shi VC, van Veldhuisen DJ, Zannad F, Zile MR, Cikes M, Goncalvesova E, Katova T, Kosztin A, Lelonek M, Sweitzer N, Vardeny O, Claggett B, Jhund PS, Solomon SD (2020) Effects of sacubitril-valsartan versus valsartan in women compared with men with heart failure and preserved ejection fraction: insights from PARAGON-HF. Circulation 141:338–351
pubmed: 31736337
doi: 10.1161/CIRCULATIONAHA.119.044491
Menges L, Krawutschke C, Fuchtbauer EM, Fuchtbauer A, Sandner P, Koesling D, Russwurm M (2019) Mind the gap (junction): cGMP induced by nitric oxide in cardiac myocytes originates from cardiac fibroblasts. Br J Pharmacol 176:4696–4707
pubmed: 31423565
pmcid: 6965686
doi: 10.1111/bph.14835
Mergia E, Russwurm M, Zoidl G, Koesling D (2003) Major occurrence of the new alpha2beta1 isoform of NO-sensitive guanylyl cyclase in brain. Cell Signal 15:189–195
pubmed: 12464390
doi: 10.1016/S0898-6568(02)00078-5
Michalakis S, Becirovic E, Biel M (2018) Retinal cyclic nucleotide-gated channels: from pathophysiology to therapy. Int J Mol Sci 19(3):749. https://doi.org/10.3390/ijms19030749
Michalakis S, Gerhardt M, Rudolph G, Priglinger S, Priglinger C (2022) Achromatopsia: genetics and gene therapy. Mol Diagn Ther 26:51–59
pubmed: 34860352
doi: 10.1007/s40291-021-00565-z
Mishra S, Sadagopan N, Dunkerly-Eyring B, Rodriguez S, Sarver DC, Ceddia RP, Murphy SA, Knutsdottir H, Jani VP, Ashok D, Oeing CU, O'Rourke B, Gangoiti JA, Sears DD, Wong GW, Collins S, Kass DA (2021) Inhibition of phosphodiesterase type 9 reduces obesity and cardiometabolic syndrome in mice. J Clin Investig 131(21):e148798
Mohan IK, Baba K, Iyyapu R, Thirumalasetty S, Satish OS (2023) Advances in congestive heart failure biomarkers. Adv Clin Chem 112:205–248
pubmed: 36642484
doi: 10.1016/bs.acc.2022.09.005
Monica FZ, Bian K, Murad F (2016) The endothelium-dependent nitric oxide-cGMP pathway. Adv Pharmacol 77:1–27
pubmed: 27451093
doi: 10.1016/bs.apha.2016.05.001
Moyes AJ, Hobbs AJ (2019) C-type natriuretic peptide: a multifaceted paracrine regulator in the heart and vasculature. Int J Mol Sci 20(9):2281. https://doi.org/10.3390/ijms20092281
Nelissen E, Argyrousi EK, Van Goethem NP, Zhao F, Hines CDG, Swaminath G, Gerisch M, Hueser J, Sandner P, Prickaerts J (2021) Soluble guanylate cyclase stimulator vericiguat enhances long-term memory in rats without altering cerebral blood volume. Biomedicines 9(8):1047. https://doi.org/10.3390/biomedicines9081047
Nelissen E, Possemis N, Van Goethem NP, Schepers M, Mulder-Jongen DAJ, Dietz L, Janssen W, Gerisch M, Huser J, Sandner P, Vanmierlo T, Prickaerts J (2022) The sGC stimulator BAY-747 and activator runcaciguat can enhance memory in vivo via differential hippocampal plasticity mechanisms. Sci Rep 12:3589
pubmed: 35246566
pmcid: 8897390
doi: 10.1038/s41598-022-07391-1
Oller J, Mendez-Barbero N, Ruiz EJ, Villahoz S, Renard M, Canelas LI, Briones AM, Alberca R, Lozano-Vidal N, Hurle MA, Milewicz D, Evangelista A, Salaices M, Nistal JF, Jimenez-Borreguero LJ, De Backer J, Campanero MR, Redondo JM (2017) Nitric oxide mediates aortic disease in mice deficient in the metalloprotease Adamts1 and in a mouse model of Marfan syndrome. Nat Med 23:200–212
pubmed: 28067899
doi: 10.1038/nm.4266
Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315–424
pubmed: 17237348
doi: 10.1152/physrev.00029.2006
Pavlou M, Schon C, Occelli LM, Rossi A, Meumann N, Boyd RF, Bartoe JT, Siedlecki J, Gerhardt MJ, Babutzka S, Bogedein J, Wagner JE, Priglinger SG, Biel M, Petersen-Jones SM, Buning H, Michalakis S (2021) Novel AAV capsids for intravitreal gene therapy of photoreceptor disorders. EMBO Mol Med 13:e13392
pubmed: 33616280
pmcid: 8033523
doi: 10.15252/emmm.202013392
Pearson GD, Devereux R, Loeys B, Maslen C, Milewicz D, Pyeritz R, Ramirez F, Rifkin D, Sakai L, Svensson L, Wessels A, Van Eyk J, Dietz HC, National Heart L, Blood I, Working NMF, G, (2008) Report of the National Heart, Lung, and Blood Institute and National Marfan Foundation Working Group on research in Marfan syndrome and related disorders. Circulation 118:785–791
pubmed: 18695204
pmcid: 2909440
doi: 10.1161/CIRCULATIONAHA.108.783753
Peixoto CA, Nunes AK, Garcia-Osta A (2015) Phosphodiesterase-5 inhibitors: action on the signaling pathways of neuroinflammation, neurodegeneration, and cognition. Mediators Inflamm 2015:940207
pubmed: 26770022
pmcid: 4681825
doi: 10.1155/2015/940207
Perez-Ternero C, Aubdool AA, Makwana R, Sanger GJ, Stimson RH, Chan LF, Moyes AJ, Hobbs AJ (2022) C-type natriuretic peptide is a pivotal regulator of metabolic homeostasis. Proc Natl Acad Sci USA 119:e2116470119
pubmed: 35333648
pmcid: 9060477
doi: 10.1073/pnas.2116470119
Peters S, Paolillo M, Mergia E, Koesling D, Kennel L, Schmidtko A, Russwurm M, Feil R (2018) cGMP imaging in brain slices reveals brain region-specific activity of NO-sensitive guanylyl cyclases (NO-GCs) and NO-GC stimulators. Int J Mol Sci 19(8):2313
Petersen J, Mergia E, Kennel L, Drees O, Steubing RD, Real CI, Kallenborn-Gerhardt W, Lu R, Friebe A, Koesling D, Schmidtko A (2019) Distinct functions of soluble guanylyl cyclase isoforms NO-GC1 and NO-GC2 in inflammatory and neuropathic pain processing. Pain 160:607–618
pubmed: 30422870
doi: 10.1097/j.pain.0000000000001440
Petraina A, Nogales C, Krahn T, Mucke H, Luscher TF, Fischmeister R, Kass DA, Burnett JC, Hobbs AJ, Schmidt H (2022) Cyclic GMP modulating drugs in cardiovascular diseases: mechanism-based network pharmacology. Cardiovasc Res 118:2085–2102
pubmed: 34270705
doi: 10.1093/cvr/cvab240
Pieske B, Butler J, Filippatos G, Lam C, Maggioni AP, Ponikowski P, Shah S, Solomon S, Kraigher-Krainer E, Samano ET, Scalise AV, Muller K, Roessig L, Gheorghiade M, Investigators S, Coordinators (2014) Rationale and design of the SOluble guanylate Cyclase stimulatoR in heArT failurE Studies (SOCRATES). Eur J Heart Fail 16:1026–1038
pubmed: 25056511
doi: 10.1002/ejhf.135
Pieske B, Maggioni AP, Lam CSP, Pieske-Kraigher E, Filippatos G, Butler J, Ponikowski P, Shah SJ, Solomon SD, Scalise AV, Mueller K, Roessig L, Gheorghiade M (2017) Vericiguat in patients with worsening chronic heart failure and preserved ejection fraction: results of the SOluble guanylate Cyclase stimulatoR in heArT failurE patientS with PRESERVED EF (SOCRATES-PRESERVED) study. Eur Heart J 38:1119–1127
pubmed: 28369340
pmcid: 5400074
doi: 10.1093/eurheartj/ehw593
Potter LR (2011a) Guanylyl cyclase structure, function and regulation. Cell Signal 23:1921–1926
pubmed: 21914472
pmcid: 4856045
doi: 10.1016/j.cellsig.2011.09.001
Potter LR (2011b) Regulation and therapeutic targeting of peptide-activated receptor guanylyl cyclases. Pharmacol Ther 130:71–82
pubmed: 21185863
doi: 10.1016/j.pharmthera.2010.12.005
Reichel FF, Seitz I, Wozar F, Dimopoulos S, Jung R, Kempf M, Kohl S, Kortum FC, Ott S, Pohl L, Stingl K, Bartz-Schmidt KU, Stingl K, Fischer MD (2022) Development of retinal atrophy after subretinal gene therapy with voretigene neparvovec. Br J Ophthalmol. https://doi.org/10.1136/bjophthalmol-2021-321023
Reverte-Salisa L, Sanyal A, Pfeifer A (2019) Role of cAMP and cGMP signaling in brown fat. Handb Exp Pharmacol 251:161–182
pubmed: 29633180
doi: 10.1007/164_2018_117
Ros O, Zagar Y, Ribes S, Baudet S, Loulier K, Couvet S, Ladarre D, Aghaie A, Louail A, Petit C, Mechulam Y, Lenkei Z, Nicol X (2019) SponGee: a genetic tool for subcellular and cell-specific cGMP manipulation. Cell Rep 27(4003–4012):e4006
Rubin AF, Green P (2007) Comment on “The consensus coding sequences of human breast and colorectal cancers.” Science 317:1500
pubmed: 17872429
doi: 10.1126/science.1138956
Russwurm M, Behrends S, Harteneck C, Koesling D (1998) Functional properties of a naturally occurring isoform of soluble guanylyl cyclase. Biochem J 335(Pt 1):125–130
pubmed: 9742221
pmcid: 1219760
doi: 10.1042/bj3350125
Russwurm M, Wittau N, Koesling D (2001) Guanylyl cyclase/PSD-95 interaction: targeting of the nitric oxide-sensitive alpha2beta1 guanylyl cyclase to synaptic membranes. J Biol Chem 276:44647–44652
pubmed: 11572861
doi: 10.1074/jbc.M105587200
Russwurm M, Mullershausen F, Friebe A, Jäger R, Russwurm C, Koesling D (2007) Design of fluorescence resonance energy transfer (FRET)-based cGMP indicators: a systematic approach. Biochem J 407:69–77
pubmed: 17516914
pmcid: 2267402
doi: 10.1042/BJ20070348
Sabbatini AR, Kararigas G (2020) Menopause-related estrogen decrease and the pathogenesis of HFpEF: JACC Review Topic of the Week. J Am Coll Cardiol 75:1074–1082
pubmed: 32138968
doi: 10.1016/j.jacc.2019.12.049
Sandner P (2018) From molecules to patients: exploring the therapeutic role of soluble guanylate cyclase stimulators. Biol Chem 399(7):679–690. https://doi.org/10.1515/hsz-2018-0155
Sandner P, Vakalopoulos A, Hahn MG, Stasch JP, Follmann M (2021) Soluble guanylate cyclase stimulators and their potential use: a patent review. Expert Opin Ther Pat 31(3):203–222
Savitska D, Hess M, Calis D, Marchetta P, Harasztosi C, Fink S, Eckert P, Ruth P, Ruttiger L, Knipper M, Singer W (2022) Stress affects central compensation of neural responses to cochlear synaptopathy in a cGMP-dependent way. Front Neurosci 16:864706
pubmed: 35968392
pmcid: 9372611
doi: 10.3389/fnins.2022.864706
Sayed N, Baskaran P, Ma X, van den Akker F, Beuve A (2007) Desensitization of soluble guanylyl cyclase, the NO receptor, by S-nitrosylation. Proc Natl Acad Sci USA 104:12312–12317
pubmed: 17636120
pmcid: 1940331
doi: 10.1073/pnas.0703944104
Schmidt H, Bottcher A, Gross T, Schmidtko A (2022) cGMP signalling in dorsal root ganglia and the spinal cord: various functions in development and adulthood. Br J Pharmacol 179:2361–2377
pubmed: 33939841
doi: 10.1111/bph.15514
Seifert R, Schirmer B (2022) cCMP and cUMP come into the spotlight, finally. Trends Biochem Sci 47:461–463
pubmed: 35031198
doi: 10.1016/j.tibs.2021.12.008
Sjoblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, Mandelker D, Leary RJ, Ptak J, Silliman N, Szabo S, Buckhaults P, Farrell C, Meeh P, Markowitz SD, Willis J, Dawson D, Willson JK, Gazdar AF, Hartigan J, Wu L, Liu C, Parmigiani G, Park BH, Bachman KE, Papadopoulos N, Vogelstein B, Kinzler KW, Velculescu VE (2006) The consensus coding sequences of human breast and colorectal cancers. Science 314:268–274
pubmed: 16959974
doi: 10.1126/science.1133427
Stehle D, Xu MZ, Schomber T, Hahn MG, Schweda F, Feil S, Kraehling JR, Eitner F, Patzak A, Sandner P, Feil R, Bénardeau A (2021) Novel sGC activators increase glomerular cGMP, induce vasodilation, and improve blood flow in the murine kidney. Br J Pharmacol 179(11):2476–2489. https://doi.org/10.1111/bph.15586
Straczynska P, Papis K, Morawiec E, Czerwinski M, Gajewski Z, Olejek A, Bednarska-Czerwinska A (2022) Signaling mechanisms and their regulation during in vivo or in vitro maturation of mammalian oocytes. Reprod Biol Endocrinol 20:37
pubmed: 35209923
pmcid: 8867761
doi: 10.1186/s12958-022-00906-5
Sumi MP, Ghosh A (2022) Hsp90 in Human Diseases: Molecular Mechanisms to Therapeutic Approaches. Cells 11(6):976. https://doi.org/10.3390/cells11060976
Szczurkowska J, Guo A, Martin J, Lee SI, Martinez E, Chien CT, Khan TA, Singh R, Dadson D, Tran TS, Pautot S, Shelly M (2022) Semaphorin3A/PlexinA3 association with the Scribble scaffold for cGMP increase is required for apical dendrite development. Cell Rep 38:110483
pubmed: 35294878
pmcid: 8994670
doi: 10.1016/j.celrep.2022.110483
Tal N, Morehouse BR, Millman A, Stokar-Avihail A, Avraham C, Fedorenko T, Yirmiya E, Herbst E, Brandis A, Mehlman T, Oppenheimer-Shaanan Y, Keszei AFA, Shao S, Amitai G, Kranzusch PJ, Sorek R (2021) Cyclic CMP and cyclic UMP mediate bacterial immunity against phages. Cell 184(23):5728–5739.e16
Thoonen R, Cauwels A, Decaluwe K, Geschka S, Tainsh RE, Delanghe J, Hochepied T, De Cauwer L, Rogge E, Voet S, Sips P, Karas RH, Bloch KD, Vuylsteke M, Stasch JP, Van de Voorde J, Buys ES, Brouckaert P (2015) Cardiovascular and pharmacological implications of haem-deficient NO-unresponsive soluble guanylate cyclase knock-in mice. Nat Commun 6:8482
pubmed: 26442659
doi: 10.1038/ncomms9482
Tolone A, Belhadj S, Rentsch A, Schwede F, Paquet-Durand F (2019) The cGMP pathway and inherited photoreceptor degeneration: targets, compounds, and biomarkers. Genes (Basel) 10(6):453. https://doi.org/10.3390/genes10060453
Udelson JE, Lewis GD, Shah SJ, Zile MR, Redfield MM, Burnett J Jr, Parker J, Seferovic JP, Wilson P, Mittleman RS, Profy AT, Konstam MA (2020) Effect of praliciguat on peak rate of oxygen consumption in patients with heart failure with preserved ejection fraction: the CAPACITY HFpEF randomized clinical trial. JAMA 324:1522–1531
pubmed: 33079154
pmcid: 7576408
doi: 10.1001/jama.2020.16641
van Haastert PJM, Keizer-Gunnink I, Pots H, Ortiz-Mateos C, Veltman D, van Egmond W, Kortholt A (2021) Forty-five years of cGMP research in Dictyostelium: understanding the regulation and function of the cGMP pathway for cell movement and chemotaxis. Mol Biol Cell 32:ar8
pubmed: 34347507
pmcid: 8684759
doi: 10.1091/mbc.E21-04-0171
Velagic A, Li JC, Qin CX, Li M, Deo M, Marshall SA, Anderson D, Woodman OL, Horowitz JD, Kemp-Harper BK, Ritchie RH (2022) Cardioprotective actions of nitroxyl donor Angeli’s salt are preserved in the diabetic heart and vasculature in the face of nitric oxide resistance. Br J Pharmacol 179:4117–4135
pubmed: 35365882
doi: 10.1111/bph.15849
Wagner BM, Robinson JW, Lin YW, Lee YC, Kaci N, Legeai-Mallet L, Potter LR (2021a) Prevention of guanylyl cyclase-B dephosphorylation rescues achondroplastic dwarfism. JCI insight 6(9):e147832. https://doi.org/10.1172/jci.insight.147832
Wagner JE, Zobel L, Gerhardt MJ, O’Riordan CR, Frederick A, Petersen-Jones SM, Biel M, Michalakis S (2021b) In vivo potency testing of subretinal rAAV5.hCNGB1 gene therapy in the Cngb1 knockout mouse model of retinitis pigmentosa. Hum Gene Ther 32:1158–1170
pubmed: 34376057
pmcid: 8819509
doi: 10.1089/hum.2021.121
Wagner BM, Robinson JW, Healy CL, Gauthier M, Dickey DM, Yee SP, Osborn JW, O’Connell TD, Potter LR (2022) Guanylyl cyclase-A phosphorylation decreases cardiac hypertrophy and improves systolic function in male, but not female, mice. FASEB J 36:e22069
pubmed: 34859913
doi: 10.1096/fj.202100600RRR
Wittenborn EC, Marletta MA (2021) Structural perspectives on the mechanism of soluble guanylate cyclase activation. Int J Mol Sci 22(11):5439. https://doi.org/10.3390/ijms22115439
Wobst J, Schunkert H, Kessler T (2018) Genetic alterations in the NO-cGMP pathway and cardiovascular risk. Nitric Oxide Biol Chem 76:105–112
doi: 10.1016/j.niox.2018.03.019
Wu G, Sharina I, Martin E (2022) Soluble guanylyl cyclase: molecular basis for ligand selectivity and action in vitro and in vivo. Front Mol Biosci 9:1007768
pubmed: 36304925
pmcid: 9592903
doi: 10.3389/fmolb.2022.1007768
Zhang Z, Yang D, Xiang J, Zhou J, Cao H, Che Q, Bai Y, Guo J, Su Z (2021) Non-shivering thermogenesis signalling regulation and potential therapeutic applications of brown adipose tissue. Int J Biol Sci 17:2853–2870
pubmed: 34345212
pmcid: 8326120
doi: 10.7150/ijbs.60354
Zheng X, Hu Z, Li H, Yang J (2022a) Structure of the human cone photoreceptor cyclic nucleotide-gated channel. Nat Struct Mol Biol 29:40–46
pubmed: 34969976
doi: 10.1038/s41594-021-00699-y
Zheng X, Li H, Hu Z, Su D, Yang J (2022b) Structural and functional characterization of an achromatopsia-associated mutation in a phototransduction channel. Commun Biol 5:190
pubmed: 35233102
pmcid: 8888761
doi: 10.1038/s42003-022-03120-6