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Inhibition of Soluble Guanylate Cyclase by ODQ

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Department of Biological Chemistry, School of Medicine, Howard Hughes Medical Institute, and Department of Medicinal Chemistry, College of Pharmacy, The University of Michigan, Ann Arbor, Michigan 48109-0606, Department of Chemistry, Michigan State University, East Lansing, Michigan 48824-1322
Cite this: Biochemistry 2000, 39, 35, 10848–10854
Publication Date (Web):August 8, 2000
https://doi.org/10.1021/bi9929296
Copyright © 2000 American Chemical Society

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    Abstract

    The heme in soluble guanylate cyclases (sGC) as isolated is ferrous, high-spin, and 5-coordinate. [1H-[1,2,4]oxadiazolo-[4,3-a]quinoxalin-1-one] (ODQ) has been used extensively as a specific inhibitor for sGC and as a diagnostic tool for identifying a role for sGC in signal transduction events. Addition of ODQ to ferrous sGC leads to a Soret shift from 431 to 392 nm and a decrease in nitric oxide (NO)-stimulated sGC activity. This Soret shift is consistent with oxidation of the ferrous heme to ferric heme. The results reported here further define the molecular mechanism of inhibition of sGC by ODQ. Addition of ODQ to the isolated sGC heme domain [β1(1−385)] gave the same spectral changes as when sGC was treated with ODQ. EPR and resonance Raman spectroscopy was used to show that the heme in ODQ-treated β1(1−385) is indeed ferric. Inhibition of the NO-stimulated sGC activity by ODQ is due to oxidation of the sGC heme and not to perturbation of the catalytic site, since the ODQ-treated sGC has the same basal activity as untreated sGC (68 ± 12 nmol min-1 mg-1). In addition, ODQ-oxidized sGC can be re-reduced by dithionite, and this re-reduced sGC has identical NO-stimulated activity as the original ferrous sGC. Oxidation of the sGC heme by ODQ is fast with a second-order rate constant of 8.5 × 103 M-1 s-1. ODQ can also oxidize hemoglobin, indicating that the reaction is not specific for the heme in sGC versus that in other hemoproteins.

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     The studies were supported by Howard Hughes Medical Institute, Predoctoral Fellowship from the Graduate School of the University of Michigan and NIH Grant GM25480.

     Department of Biological Chemistry.

    §

     Department of Chemistry, Michigan State University.

    *

     To whom correspondence should be addressed.

     Howard Hughes Medical Institute.

     Division of Medicinal Chemistry.

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    11. Liqian Chen, Xinghong Zhou, Yijian Deng, Ying Yang, Xiaohu Chen, Qinghong Chen, Yanyan Liu, Xiuqiong Fu, Hiu Yee Kwan, Yanting You, Wen Jin, Xiaoshan Zhao. Zhenwu decoction ameliorates cardiac hypertrophy through activating sGC (soluble guanylate cyclase) - cGMP (cyclic guanosine monophosphate) - PKG (protein kinase G) pathway. Journal of Ethnopharmacology 2023, 300 , 115705. https://doi.org/10.1016/j.jep.2022.115705
    12. Zhenyu Hu, Bo Zhang, Leon Jian Ying Lim, Wei Zhern Kelvin Loh, Dejie Yu, Bryce Wei Quan Tan, Mui Cheng Liang, Zhongwei Huang, Chen Huei Leo, Hua Huang, Tuck Wah Soong. S-Nitrosylation-Mediated Reduction of Ca V 1.2 Surface Expression and Open Probability Underlies Attenuated Vasoconstriction Induced by Nitric Oxide. Hypertension 2022, 79 (12) , 2854-2866. https://doi.org/10.1161/HYPERTENSIONAHA.122.19103
    13. Jun Guo, Xi Yu, Yanping Liu, Likui Lu, Dan Zhu, Yingying Zhang, Lingjun Li, Pengjie Zhang, Qinqin Gao, Xiyuan Lu, Miao Sun. Prenatal hypothyroidism diminished exogenous NO-mediated diastolic effects in fetal rat thoracic aorta smooth muscle via increased oxidative stress. Reproductive Toxicology 2022, 113 , 52-61. https://doi.org/10.1016/j.reprotox.2022.08.009
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    15. Minze Xu, Falk-Bach Lichtenberger, Cem Erdoǧan, Enyin Lai, Pontus B. Persson, Andreas Patzak, Pratik H. Khedkar. Nitric Oxide Signalling in Descending Vasa Recta after Hypoxia/Re-Oxygenation. International Journal of Molecular Sciences 2022, 23 (13) , 7016. https://doi.org/10.3390/ijms23137016
    16. Yue Dai, Dennis J. Stuehr. Inactivation of soluble guanylyl cyclase in living cells proceeds without loss of haem and involves heterodimer dissociation as a common step. British Journal of Pharmacology 2022, 179 (11) , 2505-2518. https://doi.org/10.1111/bph.15527
    17. Josean Reyes-Rivera, Yang Wu, Benjamin G.H. Guthrie, Michael A. Marletta, Nicole King, Thibaut Brunet. Nitric oxide signaling controls collective contractions in a colonial choanoflagellate. Current Biology 2022, 32 (11) , 2539-2547.e5. https://doi.org/10.1016/j.cub.2022.04.017
    18. Daniela Giordano, Cinzia Verde, Paola Corti. Nitric Oxide Production and Regulation in the Teleost Cardiovascular System. Antioxidants 2022, 11 (5) , 957. https://doi.org/10.3390/antiox11050957
    19. Aleksey V. Shchulkin, Yulia V. Abalenikhina, Elena A. Sudakova, Pavel Yu. Mylnikov, Elena N. Yakusheva. Mechanisms of Regulation of the P-Glycoprotein Transporter Protein Functioning under the Action of Nitric Oxide. Biochemistry (Moscow) 2022, 87 (4) , 366-379. https://doi.org/10.1134/S000629792204006X
    20. Mohammed Al-Chawishly, Oliver Loveland, Alison M. Gurney. Kv7 Channels in Cyclic-Nucleotide Dependent Relaxation of Rat Intra-Pulmonary Artery. Biomolecules 2022, 12 (3) , 429. https://doi.org/10.3390/biom12030429
    21. Airlla Laana de Medeiros Cavalcanti, Patrícia Keytth Lins Rocha, Zhengbing Zhuge, Marcelo F. Montenegro, Luciano Leite Paulo, Leônidas das Graças Mendes-Júnior, Maria Cláudia Rodrigues Brandão, Petrônio F. Athayde-Filho, Jon O. Lundberg, Eddie Weitzberg, Mattias Carlström, Valdir de Andrade Braga. Cardiovascular characterization of the novel organic mononitrate NDIBP in rats. Nitric Oxide 2022, 119 , 50-60. https://doi.org/10.1016/j.niox.2021.12.007
    22. Rui Liu, Yunlu Kang, Lei Chen. Activation mechanism of human soluble guanylate cyclase by stimulators and activators. Nature Communications 2021, 12 (1) https://doi.org/10.1038/s41467-021-25617-0
    23. Tristan H. J. Lewis, Paulina M. Getsy, John F. Peroni, Rita M. Ryan, Michael W. Jenkins, Stephen J. Lewis. Characterization of endothelium-dependent and -independent processes in occipital artery of the rat: relevance to control of blood flow to nodose sensory cells. Journal of Applied Physiology 2021, 131 (3) , 1067-1079. https://doi.org/10.1152/japplphysiol.00221.2021
    24. Dennis J. Stuehr, Saurav Misra, Yue Dai, Arnab Ghosh. Maturation, inactivation, and recovery mechanisms of soluble guanylyl cyclase. Journal of Biological Chemistry 2021, 296 , 100336. https://doi.org/10.1016/j.jbc.2021.100336
    25. Hubert Dabiré, Fatou Dramé, Nelly Cita, Bijan Ghaleh. The hypertensive effect of sorafenib is abolished by sildenafil. Cardio-Oncology 2020, 6 (1) https://doi.org/10.1186/s40959-020-00064-w
    26. Mirko Gastreich-Seelig, Marcel Jimenez, Ervice Pouokam. Mechanisms Associated to Nitroxyl (HNO)-Induced Relaxation in the Intestinal Smooth Muscle. Frontiers in Physiology 2020, 11 https://doi.org/10.3389/fphys.2020.00438
    27. Petra Muenzner, Christof R. Hauck. Neisseria gonorrhoeae Blocks Epithelial Exfoliation by Nitric-Oxide-Mediated Metabolic Cross Talk to Promote Colonization in Mice. Cell Host & Microbe 2020, 27 (5) , 793-808.e5. https://doi.org/10.1016/j.chom.2020.03.010
    28. Amanda Roggia Ruviaro, Paula de Paula Menezes Barbosa, Eduardo Costa Alexandre, Alberto Fernando Oliveira Justo, Edson Antunes, Gabriela Alves Macedo. Aglycone-rich extracts from citrus by-products induced endothelium-independent relaxation in isolated arteries. Biocatalysis and Agricultural Biotechnology 2020, 23 , 101481. https://doi.org/10.1016/j.bcab.2019.101481
    29. Cheng Xue Qin, Jarryd Anthonisz, Chen Huei Leo, Nicola Kahlberg, Anida Velagic, Mandy Li, Edwina Jap, Owen L. Woodman, Laura J. Parry, John D. Horowitz, Barbara K. Kemp-Harper, Rebecca H. Ritchie. Nitric Oxide Resistance, Induced in the Myocardium by Diabetes, Is Circumvented by the Nitric Oxide Redox Sibling, Nitroxyl. Antioxidants & Redox Signaling 2020, 32 (1) , 60-77. https://doi.org/10.1089/ars.2018.7706
    30. Christopher M. Adams, Julien P. N. Papillon. Recent Developments for the Treatment of Glaucoma. 2020, 189-256. https://doi.org/10.1007/7355_2019_92
    31. Yunlu Kang, Rui Liu, Jing-Xiang Wu, Lei Chen. Structural insights into the mechanism of human soluble guanylate cyclase. Nature 2019, 574 (7777) , 206-210. https://doi.org/10.1038/s41586-019-1584-6
    32. Hae Jin Kim, Ji Hyun Jang, Yin Hua Zhang, Hae Young Yoo, Sung Joon Kim. Fast relaxation and desensitization of angiotensin II contraction in the pulmonary artery via AT1R and Akt-mediated phosphorylation of muscular eNOS. Pflügers Archiv - European Journal of Physiology 2019, 471 (10) , 1317-1330. https://doi.org/10.1007/s00424-019-02305-z
    33. Francesc X. Guix, Carmem L. Sartório, Gerard ILL-Raga. BACE1 Translation: At the Crossroads Between Alzheimer’s Disease Neurodegeneration and Memory Consolidation. Journal of Alzheimer's Disease Reports 2019, 3 (1) , 113-148. https://doi.org/10.3233/ADR-180089
    34. Christin Elgert, Anne Rühle, Peter Sandner, Sönke Behrends. A novel soluble guanylyl cyclase activator, BR 11257, acts as a non-stabilising partial agonist of sGC. Biochemical Pharmacology 2019, 163 , 142-153. https://doi.org/10.1016/j.bcp.2019.02.007
    35. Alice V. Araújo, Fernanda A. Andrade, Michele Paulo, Tiago D. de Paula, Simone R. Potje, Amanda C. Pereira, Lusiane M. Bendhack. NO donors induce vascular relaxation by different cellular mechanisms in hypertensive and normotensive rats. Nitric Oxide 2019, 86 , 12-20. https://doi.org/10.1016/j.niox.2019.02.004
    36. Alencar Kolinski Machado, Francine Carla Cadoná, Charles Elias Assmann, Ana Cristina Andreazza, Marta Maria Medeiros Frescura Duarte, Cátia dos Santos Branco, Xinyang Zhou, Diulie Valente de Souza, Euler Esteves Ribeiro, Ivana Beatrice Mânica da Cruz. Açaí (Euterpe oleracea Mart.) has anti-inflammatory potential through NLRP3-inflammasome modulation. Journal of Functional Foods 2019, 56 , 364-371. https://doi.org/10.1016/j.jff.2019.03.034
    37. Michael A. Hollas, Manel Ben Aissa, Sue H. Lee, Jesse M. Gordon-Blake, Gregory R.J. Thatcher. Pharmacological manipulation of cGMP and NO/cGMP in CNS drug discovery. Nitric Oxide 2019, 82 , 59-74. https://doi.org/10.1016/j.niox.2018.10.006
    38. Zhanneta Zalutskaya, Lidiya Kochemasova, Elena Ermilova. Dual positive and negative control of Chlamydomonas PII signal transduction protein expression by nitrate/nitrite and NO via the components of nitric oxide cycle. BMC Plant Biology 2018, 18 (1) https://doi.org/10.1186/s12870-018-1540-x
    39. Sandhya S. Visweswariah, Natasha Jaiswal. Guanylyl Cyclase Receptors. 2018, 2308-2315. https://doi.org/10.1007/978-3-319-67199-4_434
    40. William L. Dees, Jill K. Hiney, Vinod K. Srivastava. Complimentary Methods for Assessing Hypothalamic Actions of Manganese During Pubertal Development. 2018https://doi.org/10.1007/7653_2018_10
    41. Makoto Ando, Takayuki Matsumoto, Kumiko Taguchi, Tsuneo Kobayashi. Poly (I:C) impairs NO donor-induced relaxation by overexposure to NO via the NF-kappa B/iNOS pathway in rat superior mesenteric arteries. Free Radical Biology and Medicine 2017, 112 , 553-566. https://doi.org/10.1016/j.freeradbiomed.2017.08.027
    42. Angel Josabad Alonso‐Castro, Marco Martin González‐Chávez, Juan Ramón Zapata‐Morales, Alexia Karina Verdinez‐Portales, Amanda Sánchez‐Recillas, Rolffy Ortiz‐Andrade, Mario Isiordia‐Espinoza, Fidel Martínez‐Gutiérrez, Marco Antonio Ramírez‐Morales, Fabiola Domínguez, María Elizabeth Juache‐Flores, Roberto Martínez. Antinociceptive Activity of Ent‐Dihydrotucumanoic Acid Isolated from Gymnosperma glutinosum Spreng Less. Drug Development Research 2017, 78 (7) , 340-348. https://doi.org/10.1002/ddr.21397
    43. Shao-Rui Chen, Xiao-Gao Jin, Hui-Lin Pan. Endogenous nitric oxide inhibits spinal NMDA receptor activity and pain hypersensitivity induced by nerve injury. Neuropharmacology 2017, 125 , 156-165. https://doi.org/10.1016/j.neuropharm.2017.07.023
    44. Liwei He, Fangtian Fan, Xianbang Hou, Cuixiang Gao, Li Meng, Shu Meng, Shiwen Huang, Hongyan Wu. Resveratrol suppresses pulmonary tumor metastasis by inhibiting platelet-mediated angiogenic responses. Journal of Surgical Research 2017, 217 , 113-122. https://doi.org/10.1016/j.jss.2017.05.009
    45. Mizanur M. Rahaman, Anh T. Nguyen, Megan P. Miller, Scott A. Hahn, Courtney Sparacino-Watkins, Soma Jobbagy, Nolan T. Carew, Nadiezhda Cantu-Medellin, Katherine C. Wood, Catherine J. Baty, Francisco J. Schopfer, Eric E. Kelley, Mark T. Gladwin, Emil Martin, Adam C. Straub. Cytochrome b5 Reductase 3 Modulates Soluble Guanylate Cyclase Redox State and cGMP Signaling. Circulation Research 2017, 121 (2) , 137-148. https://doi.org/10.1161/CIRCRESAHA.117.310705
    46. Evelien Van Rymenant, John Van Camp, Bart Pauwels, Charlotte Boydens, Laura Vanden Daele, Katrijn Beerens, Peter Brouckaert, Guy Smagghe, Asimina Kerimi, Gary Williamson, Charlotte Grootaert, Johan Van de Voorde. Ferulic acid-4- O -sulfate rather than ferulic acid relaxes arteries and lowers blood pressure in mice. The Journal of Nutritional Biochemistry 2017, 44 , 44-51. https://doi.org/10.1016/j.jnutbio.2017.02.018
    47. Huafeng Zhang, Bingwei Sun. Pleiotropic regulations of neutrophil receptors response to sepsis. Inflammation Research 2017, 66 (3) , 197-207. https://doi.org/10.1007/s00011-016-0993-3
    48. Nádia J. Almeida Cardelli, M. Elisa Lopes-Pires, Pedro H.L. Bonfitto, Heloisa H. Ferreira, Edson Antunes, Sisi Marcondes. Cross-talking between lymphocytes and platelets and its regulation by nitric oxide and peroxynitrite in physiological condition and endotoxemia. Life Sciences 2017, 172 , 2-7. https://doi.org/10.1016/j.lfs.2016.12.013
    49. Eduardo Henrique Silva Sousa, Luiz Gonzaga de França Lopes, Gonzalo Gonzalez, Marie-Alda Gilles-Gonzalez. Drug discovery targeting heme-based sensors and their coupled activities. Journal of Inorganic Biochemistry 2017, 167 , 12-20. https://doi.org/10.1016/j.jinorgbio.2016.11.022
    50. Arnab Ghosh, Dennis J. Stuehr. Regulation of sGC via hsp90, Cellular Heme, sGC Agonists, and NO: New Pathways and Clinical Perspectives. Antioxidants & Redox Signaling 2017, 26 (4) , 182-190. https://doi.org/10.1089/ars.2016.6690
    51. Doris Koesling, Michael Russwurm, Evanthia Mergia. Regulation and Physiological Functions of NO-Sensitive Guanylyl Cyclase. 2017, 107-116. https://doi.org/10.1016/B978-0-12-804273-1.00008-9
    52. Lai Wen, Susanne Feil, Robert Feil. cGMP Signaling in Platelets. 2017, 231-252. https://doi.org/10.1007/978-3-319-66224-4_15
    53. Cristina La Torre, Benedetta Cinque, Francesca Lombardi, Gianfranca Miconi, Paola Palumbo, Zoran Evtoski, Giuseppe Placidi, Donatella Fanini, Anna Maria Cimini, Elisabetta Benedetti, Maurizio Giuliani, Maria Grazia Cifone. Nitric Oxide Chemical Donor Affects the Early Phases of In Vitro Wound Healing Process. Journal of Cellular Physiology 2016, 231 (10) , 2185-2195. https://doi.org/10.1002/jcp.25331
    54. Jagamya Vijayaraghavan, Kristopher Kramp, Michael E. Harris, Focco van den Akker. Inhibition of soluble guanylyl cyclase by small molecules targeting the catalytic domain. FEBS Letters 2016, 590 (20) , 3669-3680. https://doi.org/10.1002/1873-3468.12427
    55. Andrew W. Holt, Danielle N. Martin, Patti R. Shaver, Shaquria P. Adderley, Joshua D. Stone, Chintamani N. Joshi, Jake T. Francisco, Robert M. Lust, Douglas A. Weidner, Brian M. Shewchuk, David A. Tulis. Soluble guanylyl cyclase-activated cyclic GMP-dependent protein kinase inhibits arterial smooth muscle cell migration independent of VASP-serine 239 phosphorylation. Cellular Signalling 2016, 28 (9) , 1364-1379. https://doi.org/10.1016/j.cellsig.2016.06.012
    56. Xian-xia Zhang, Li-min Lu, Li Wang. Vitamin K3 inhibits mouse uterine contraction in vitro via interference with the calcium transfer and the potassium channels. Biochemical and Biophysical Research Communications 2016, 476 (4) , 393-399. https://doi.org/10.1016/j.bbrc.2016.05.132
    57. Lihui Zou, Xiaomao Xu, Zhenguo Zhai, Ting Yang, Junhua Jin, Fei Xiao, Chen Wang. Identification of downstream target genes regulated by the nitric oxide–soluble guanylate cyclase–cyclic guanosine monophosphate signal pathway in pulmonary hypertension. Journal of International Medical Research 2016, 44 (3) , 508-519. https://doi.org/10.1177/0300060516636751
    58. Jie Pan, Xiaoxue Zhang, Hong Yuan, Qiming Xu, Huijuan Zhang, Yajun Zhou, Zhong-Xian Huang, Xiangshi Tan. The molecular mechanism of heme loss from oxidized soluble guanylate cyclase induced by conformational change. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 2016, 1864 (5) , 488-500. https://doi.org/10.1016/j.bbapap.2016.02.012
    59. A S Leitão Junior, R M Campos, J B G Cerqueira, M C Fonteles, C F Santos, G de Nucci, E H S Sousa, L G F Lopes, L F Gonzaga-Silva, N R F Nascimento. Relaxant effect of a metal-based drug in human corpora cavernosa and its mechanism of action. International Journal of Impotence Research 2016, 28 (1) , 20-24. https://doi.org/10.1038/ijir.2015.27
    60. Sandhya S. Visweswariah, Natasha Jaiswal. Guanylyl Cyclase Receptors. 2016, 1-8. https://doi.org/10.1007/978-1-4614-6438-9_434-1
    61. M. Elisa Lopes-Pires, Ana C. Antunes Naime, Nádia J. Almeida Cardelli, Débora J. Anjos, Edson Antunes, Sisi Marcondes, . PKC and AKT Modulate cGMP/PKG Signaling Pathway on Platelet Aggregation in Experimental Sepsis. PLOS ONE 2015, 10 (9) , e0137901. https://doi.org/10.1371/journal.pone.0137901
    62. Filipa Mota, Paul Gane, Kathryn Hampden-Smith, Charles K. Allerston, John Garthwaite, David L. Selwood. A new small molecule inhibitor of soluble guanylate cyclase. Bioorganic & Medicinal Chemistry 2015, 23 (17) , 5303-5310. https://doi.org/10.1016/j.bmc.2015.07.074
    63. Marija Marinko, Aleksandra Novakovic, Dragoslav Nenezic, Ivan Stojanovic, Predrag Milojevic, Miomir Jovic, Nenad Ugresic, Vladimir Kanjuh, Qin Yang, Guo-Wei He. Nicorandil directly and cyclic GMP-dependently opens K+ channels in human bypass grafts. Journal of Pharmacological Sciences 2015, 128 (2) , 59-64. https://doi.org/10.1016/j.jphs.2015.03.003
    64. Guangshuo Zhu, Dieter Groneberg, Gautam Sikka, Daijiro Hori, Mark J. Ranek, Taishi Nakamura, Eiki Takimoto, Nazareno Paolocci, Dan E. Berkowitz, Andreas Friebe, David A. Kass. Soluble Guanylate Cyclase Is Required for Systemic Vasodilation But Not Positive Inotropy Induced by Nitroxyl in the Mouse. Hypertension 2015, 65 (2) , 385-392. https://doi.org/10.1161/HYPERTENSIONAHA.114.04285
    65. William L. Dees, Jill K. Hiney, Vinod K. Srivastava. The Effects of Manganese on Female Pubertal Development. 2014, 437-458. https://doi.org/10.1039/9781782622383-00437
    66. Fabiane Sônego, José Carlos Alves-Filho, Fernando Queiróz Cunha. Targeting neutrophils in sepsis. Expert Review of Clinical Immunology 2014, 10 (8) , 1019-1028. https://doi.org/10.1586/1744666X.2014.922876
    67. Edward A. Pankey, Modar Kassan, Soo-Kyoung Choi, Khalid Matrougui, Bobby D. Nossaman, Albert L. Hyman, Philip J. Kadowitz. Vasodilator responses to acetylcholine are not mediated by the activation of soluble guanylate cyclase or TRPV4 channels in the rat. American Journal of Physiology-Heart and Circulatory Physiology 2014, 306 (11) , H1495-H1506. https://doi.org/10.1152/ajpheart.00978.2013
    68. Natasha M. Rogers, Franziska Seeger, Elsa D. Garcin, David D. Roberts, Jeffrey S. Isenberg. Regulation of soluble guanylate cyclase by matricellular thrombospondins: implications for blood flow. Frontiers in Physiology 2014, 5 https://doi.org/10.3389/fphys.2014.00134
    69. Syamantak Majumder, Swaraj Sinha, Jamila H. Siamwala, Ajit Muley, Himabindu Reddy Seerapu, Gopi Krishna Kolluru, Vimal Veeriah, Shunmugam Nagarajan, Sree Rama Chaitanya Sridhara, Mani Krishna Priya, Maniselvan Kuppusamy, Sundaramoorthy Srinivasan, Salini Konikkat, Gowrishankar Soundararajan, S. Venkataraman, Uttara Saran, Suvro Chatterjee. A comparative study of NONOate based NO donors: Spermine NONOate is the best suited NO donor for angiogenesis. Nitric Oxide 2014, 36 , 76-86. https://doi.org/10.1016/j.niox.2013.12.002
    70. Denise Cazzato, Emma Assi, Claudia Moscheni, Silvia Brunelli, Clara De Palma, Davide Cervia, Cristiana Perrotta, Emilio Clementi. Nitric oxide drives embryonic myogenesis in chicken through the upregulation of myogenic differentiation factors. Experimental Cell Research 2014, 320 (2) , 269-280. https://doi.org/10.1016/j.yexcr.2013.11.006
    71. Ahmed El-Sehemy, Alex C. Chang, Abul Kalam Azad, Nidhi Gupta, Zhihua Xu, Helen Steed, Aly Karsan, YangXin Fu. Notch activation augments nitric oxide/soluble guanylyl cyclase signaling in immortalized ovarian surface epithelial cells and ovarian cancer cells. Cellular Signalling 2013, 25 (12) , 2780-2787. https://doi.org/10.1016/j.cellsig.2013.09.008
    72. Hong Wang, Aileen X. Wang, Kevin Aylor, Eugene J. Barrett. Nitric Oxide Directly Promotes Vascular Endothelial Insulin Transport. Diabetes 2013, 62 (12) , 4030-4042. https://doi.org/10.2337/db13-0627
    73. Shyamali Mandal, Amelia Stanco, Emmanuel S. Buys, Grigori Enikolopov, John L. R. Rubenstein. Soluble Guanylate Cyclase Generation of cGMP Regulates Migration of MGE Neurons. The Journal of Neuroscience 2013, 33 (43) , 16897-16914. https://doi.org/10.1523/JNEUROSCI.1871-13.2013
    74. Constantinos Glynos, Lisa L. Dupont, Theodoros Vassilakopoulos, Andreas Papapetropoulos, Peter Brouckaert, Athanassios Giannis, Guy F. Joos, Ken R. Bracke, Guy G. Brusselle. The Role of Soluble Guanylyl Cyclase in Chronic Obstructive Pulmonary Disease. American Journal of Respiratory and Critical Care Medicine 2013, 188 (7) , 789-799. https://doi.org/10.1164/rccm.201210-1884OC
    75. Barbara Lies, Dieter Groneberg, Stepan Gambaryan, Andreas Friebe. Lack of effect of ODQ does not exclude cGMP signalling via NO ‐sensitive guanylyl cyclase. British Journal of Pharmacology 2013, 170 (2) , 317-327. https://doi.org/10.1111/bph.12275
    76. Emanuel Sanz-Luque, Francisco Ocaña-Calahorro, Angel Llamas, Aurora Galvan, Emilio Fernandez. Nitric oxide controls nitrate and ammonium assimilation in Chlamydomonas reinhardtii. Journal of Experimental Botany 2013, 64 (11) , 3373-3383. https://doi.org/10.1093/jxb/ert175
    77. Bobby D Nossaman, George F Lasker, Edward A Pankey, Raj D Parikh, Philip J Kadowitz. Stimulators and activators of soluble guanylate cyclase: potential therapeutic indications. 2013, 74-87. https://doi.org/10.2217/ebo.13.290
    78. George F. Lasker, Edward A. Pankey, Philip J. Kadowitz. Modulation of Soluble Guanylate Cyclase for the Treatment of Erectile Dysfunction. Physiology 2013, 28 (4) , 262-269. https://doi.org/10.1152/physiol.00001.2013
    79. George F. Lasker, Edward A. Pankey, Terrence J. Frink, Jonathan R. Zeitzer, Korey A. Walter, Philip J. Kadowitz. The sGC activator BAY 60-2770 has potent erectile activity in the rat. American Journal of Physiology-Heart and Circulatory Physiology 2013, 304 (12) , H1670-H1679. https://doi.org/10.1152/ajpheart.00062.2013
    80. Ali Alshehri, Marie-Pierre Bourguignon, Nicolas Clavreul, Cécile Badier-Commander, Willy Gosgnach, Serge Simonet, Christine Vayssettes-Courchay, Alex Cordi, Jean-Noël Fabiani, Tony J. Verbeuren, Michel Félétou. Mechanisms of the vasorelaxing effects of CORM-3, a water-soluble carbon monoxide-releasing molecule: interactions with eNOS. Naunyn-Schmiedeberg's Archives of Pharmacology 2013, 386 (3) , 185-196. https://doi.org/10.1007/s00210-012-0829-9
    81. Robrecht Thoonen, Patrick Y. Sips, Kenneth D. Bloch, Emmanuel S. Buys. Pathophysiology of Hypertension in the Absence of Nitric Oxide/Cyclic GMP Signaling. Current Hypertension Reports 2013, 15 (1) , 47-58. https://doi.org/10.1007/s11906-012-0320-5
    82. George F. Lasker, Edward A. Pankey, Alexander V. Allain, Subramanyam N. Murthy, Johannes-Peter Stasch, Philip J. Kadowitz. The Selective Rho-kinase Inhibitor Azaindole-1 Has Long-lasting Erectile Activity in the Rat. Urology 2013, 81 (2) , 465.e7-465.e14. https://doi.org/10.1016/j.urology.2012.10.039
    83. E.S. Underbakke, N.B. Surmeli, B.C. Smith, S.L. Wynia-Smith, M.A. Marletta. Nitric Oxide Signaling. 2013, 241-262. https://doi.org/10.1016/B978-0-08-097774-4.00320-X
    84. Nicholas Peake, Nyan Su, Manoj Ramachandran, Pramod Achan, Donald M Salter, Dan L Bader, Amie J Moyes, Adrian J Hobbs, Tina T Chowdhury. Natriuretic peptide receptors regulate cytoprotective effects in a human ex vivo 3D/bioreactor model. Arthritis Research & Therapy 2013, 15 (4) , R76. https://doi.org/10.1186/ar4253
    85. Mariarosaria Bucci, Andreas Papapetropoulos, Valentina Vellecco, Zongmin Zhou, Altaany Zaid, Panagiotis Giannogonas, Anna Cantalupo, Sandeep Dhayade, Katia P. Karalis, Rui Wang, Robert Feil, Giuseppe Cirino, . cGMP-Dependent Protein Kinase Contributes to Hydrogen Sulfide-Stimulated Vasorelaxation. PLoS ONE 2012, 7 (12) , e53319. https://doi.org/10.1371/journal.pone.0053319
    86. Nathaniel B. Fernhoff, Emily R. Derbyshire, Eric S. Underbakke, Michael A. Marletta. Heme-assisted S-Nitrosation Desensitizes Ferric Soluble Guanylate Cyclase to Nitric Oxide. Journal of Biological Chemistry 2012, 287 (51) , 43053-43062. https://doi.org/10.1074/jbc.M112.393892
    87. Zhibo An, Jason J. Winnick, Mary C. Moore, Ben Farmer, Marta Smith, Jose M. Irimia, Peter J. Roach, Alan D. Cherrington. A Cyclic Guanosine Monophosphate–Dependent Pathway Can Regulate Net Hepatic Glucose Uptake in Vivo. Diabetes 2012, 61 (10) , 2433-2441. https://doi.org/10.2337/db11-1816
    88. A. N. Meints, J. G. Pemberton, J. P. Chang. Nitric Oxide and Guanylate Cyclase Signalling are Differentially Involved in Gonadotrophin (LH) Release Responses to Two Endogenous GnRHs from Goldfish Pituitary Cells. Journal of Neuroendocrinology 2012, 24 (8) , 1166-1181. https://doi.org/10.1111/j.1365-2826.2012.02323.x
    89. Hongyan Wang, Fangfang Zhong, Jie Pan, Wei Li, Jihu Su, Zhong-Xian Huang, Xiangshi Tan. Structural and functional insights into the heme-binding domain of the human soluble guanylate cyclase α2 subunit and heterodimeric α2β1. JBIC Journal of Biological Inorganic Chemistry 2012, 17 (5) , 719-730. https://doi.org/10.1007/s00775-012-0891-2
    90. Nur Basak Surmeli, Michael A. Marletta. Insight into the Rescue of Oxidized Soluble Guanylate Cyclase by the Activator Cinaciguat. ChemBioChem 2012, 13 (7) , 977-981. https://doi.org/10.1002/cbic.201100809
    91. Bobby D. Nossaman, Edward A. Pankey, Adeleke R. Badejo, David B. Casey, Satvika Uppu, Subramanyam N. Murthy, Philip J. Kadowitz. Analysis of responses to glyceryl trinitrate and sodium nitrite in the intact chest rat. Nitric Oxide 2012, 26 (4) , 223-228. https://doi.org/10.1016/j.niox.2012.03.009
    92. Fabíola Z. Mónica, Julio Rojas-Moscoso, Marcovan Porto, André A. Schenka, Edson Antunes, José Carlos Cogo, Gilberto De Nucci. Immunohistochemical and functional characterization of nitric oxide signaling pathway in isolated aorta from Crotalus durissus terrificus. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 2012, 155 (3) , 433-439. https://doi.org/10.1016/j.cbpc.2011.11.003
    93. Felipe C. Munhoz, Simone R. Potje, Amanda C. Pereira, Marcella G. Daruge, Roberto S. da Silva, Lusiane M. Bendhack, Cristina Antoniali. Hypotensive and vasorelaxing effects of the new NO-donor [Ru(terpy)(bdq)NO+]3+ in spontaneously hypertensive rats. Nitric Oxide 2012, 26 (2) , 111-117. https://doi.org/10.1016/j.niox.2011.12.008
    94. Bobby Nossaman, Edward Pankey, Philip Kadowitz. Stimulators and Activators of Soluble Guanylate Cyclase: Review and Potential Therapeutic Indications. Critical Care Research and Practice 2012, 2012 , 1-12. https://doi.org/10.1155/2012/290805
    95. Zhan-Qing Wang, Jing-Feng Xu, Jin-Ping Wang, Wei-Juan Zhao, Ming Zeng. Involvement of Guanylate Cyclase and K+ Channels in Relaxation Evoked by Ferulate Nitrate in Rat Aorta Artery. Journal of Pharmacological Sciences 2012, 118 (4) , 521-530. https://doi.org/10.1254/jphs.11179FP
    96. Calvin K. Y. Chan, Judith Mak, Yuansheung Gao, Ricky Y. K. Man, Paul M. Vanhoutte. Endothelium-derived NO, but not cyclic GMP, is required for hypoxic augmentation in isolated porcine coronary arteries. American Journal of Physiology-Heart and Circulatory Physiology 2011, 301 (6) , H2313-H2321. https://doi.org/10.1152/ajpheart.00258.2011
    97. Daniella Bonaventura, Renata Galvão de Lima, Roberto Santana da Silva, Lusiane Maria Bendhack. NO donors-relaxation is impaired in aorta from hypertensive rats due to a reduced involvement of K+ channels and sarcoplasmic reticulum Ca2+-ATPase. Life Sciences 2011, 89 (17-18) , 595-602. https://doi.org/10.1016/j.lfs.2011.07.022
    98. Xiao-Gao Jin, Shao-Rui Chen, Xue-Hong Cao, Li Li, Hui-Lin Pan. Nitric Oxide Inhibits Nociceptive Transmission by Differentially Regulating Glutamate and Glycine Release to Spinal Dorsal Horn Neurons. Journal of Biological Chemistry 2011, 286 (38) , 33190-33202. https://doi.org/10.1074/jbc.M111.270967
    99. Linda S. Hoffmann, Peter M. Schmidt, Yvonne Keim, Carsten Hoffmann, Harald H. H. W. Schmidt, Johannes-Peter Stasch, . Fluorescence Dequenching Makes Haem-Free Soluble Guanylate Cyclase Detectable in Living Cells. PLoS ONE 2011, 6 (8) , e23596. https://doi.org/10.1371/journal.pone.0023596
    100. Dean L. Kellogg, Joan L. Zhao, Yubo Wu, John M. Johnson. Antagonism of soluble guanylyl cyclase attenuates cutaneous vasodilation during whole body heat stress and local warming in humans. Journal of Applied Physiology 2011, 110 (5) , 1406-1413. https://doi.org/10.1152/japplphysiol.00702.2010
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