Sensitivity of the Natriuretic Peptide/cGMP System to Hyperammonaemia in Rat C6 Glioma Cells and GPNT Brain Endothelial Cells
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Cell Culture
2.3. Crystal Violet Cell Proliferation Assays
2.4. Cyclic GMP Enzyme Immunoassay
2.5. Tissue Collection, RNA Extraction and Multiplex GeXP RT-qPCR Assay
2.6. Reactive Oxygen Species (ROS) Assays
2.7. Extracellular Vesicle Preparation and Flow Cytometry
2.8. Data Presentation and Statistical Analysis
3. Results
3.1. Molecular and Functional Characterisation of Natriuretic Peptides in Rat C6 Glioma Cells
3.2. Effects of Hyperammonaemia and CNP on Cell Proliferation in Rat C6 Cells
3.3. Effects of Hyperammonaemia on CNP-Stimulated and Sodium Nitroprusside-Stimulated cGMP Accumulation in Rat C6 Cells
3.4. Effects of Hyperammonaemia on CNP-Stimulated cGMP Efflux from Rat C6 Cells
3.5. Effects of Hyperammonaemia on Expression of Genes Associated with cGMP Regulation in Rat C6 Cells
3.6. Effects of Hyperammonaemia on Reactive Oxygen Species (ROS) Production in Rat C6 Cells
3.7. Effects of Hyperammonaemia on the Natriuretic Peptide System in Rat GPNT Brain Endothelial Cells
3.8. Effects of Hyperammonaemia on Extracellular Vesicle Production from C6 Cells and Their Functional Effects on Natriuretic Peptide Signalling in GPNT Cells
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Potter, L.R.; Abbey-Hosch, S.; Dickey, D.M. Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr. Rev. 2005, 27, 47–72. [Google Scholar] [CrossRef]
- Kuhn, M. Molecular physiology of membrane guanylyl cyclase receptors. Physiol. Rev. 2016, 96, 751–804. [Google Scholar] [CrossRef]
- Fowkes, R.C.; McArdle, C.A. C-type natriuretic peptide: An important neuroendocrine regulator? Trends Endocrinol. Metab. 2000, 11, 333–338. [Google Scholar] [CrossRef]
- Rose, R.A.; Giles, W.R. Natriuretic peptide C receptor signalling in the heart and vasculature. J. Physiol. 2008, 586, 353–366. [Google Scholar] [CrossRef] [PubMed]
- Moyes, A.J.; Khambata, R.S.; Villar, I.; Bubb, K.J.; Baliga, R.S.; Lumsden, N.G.; Xiao, F.; Gane, P.J.; Rebstock, A.-S.; Worthington, R.J.; et al. Endothelial C-type natriuretic peptide maintains vascular homeostasis. J. Clin. Investig. 2014, 124, 4039–4051. [Google Scholar] [CrossRef] [PubMed]
- Goncalves, J.; Grove, K.L.; Deschepper, C.F. Generation of cyclic guanosine monophosphate in brain slices incubated with atrial or C-type natriuretic peptides: Comparison of the amplitudes and cellular distribution of the responses. Regul. Pept. 1995, 57, 55–63. [Google Scholar] [CrossRef]
- Olcese, J.; Middendorff, R.; Münker, M.; Schmidt, C.; McArdle, C.A. Natriuretic peptides stimulate cyclic GMP production in an immortalized LHRH neuronal cell line. J. Neuroendocr. 1994, 6, 127–130. [Google Scholar] [CrossRef]
- Tsang, D.; Tung, C.S.; Yeung, V.T.; Cockram, C.S. Endothelin-3 reduces C-type natriuretic peptide-induced cyclic GMP formation in C6 glioma cells. Regul. Pept. 1997, 70, 91–96. [Google Scholar] [CrossRef]
- Chusho, H.; Tamura, N.; Ogawa, Y.; Yasoda, A.; Suda, M.; Miyazawa, T.; Nakamura, K.; Nakao, K.; Kurihara, T.; Komatsu, Y.; et al. Dwarfism and early death in mice lacking C-type natriuretic peptide. Proc. Natl. Acad. Sci. USA 2001, 98, 4016–4021. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Legeai-Mallet, L. C-type natriuretic peptide analog as therapy for achondroplasia. Endocr. Dev. 2015, 30, 98–105. [Google Scholar] [CrossRef] [PubMed]
- Ueda, Y.; Yasoda, A.; Hirota, K.; Yamauchi, I.; Yamashita, T.; Kanai, Y.; Sakane, Y.; Fujii, T.; Inagaki, N. Exogenous C-type natriuretic peptide therapy for impaired skeletal growth in a murine model of glucocorticoid treatment. Sci. Rep. 2019, 9, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Zhang, M.; Su, Y.-Q.; Sugiura, K.; Xia, G.; Eppig, J.J. Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 2010, 330, 366–369. [Google Scholar] [CrossRef] [Green Version]
- Zhao, Z.; Ma, L. Regulation of axonal development by natriuretic peptide hormones. Proc. Natl. Acad. Sci. USA 2009, 106, 18016–18021. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schmidt, H.; Dickey, D.M.; Dumoulin, A.; Octave, M.; Robinson, J.W.; Kühn, R.; Feil, R.; Potter, L.R.; Rathjen, F.G. Regulation of the natriuretic peptide receptor 2 (Npr2) by phosphorylation of juxtamembrane serine and threonine residues is essential for bifurcation of sensory axons. J. Neurosci. 2018, 38, 9768–9780. [Google Scholar] [CrossRef] [PubMed]
- Schmidt, H.; Stonkute, A.; Jüttner, R.; Koesling, R.; Friebe, A.; Rathjen, F.G. C-type natriuretic peptide (CNP) is a bifurcation factor for sensory neurons. Proc. Natl. Acad. Sci. USA 2009, 106, 16847–16852. [Google Scholar] [CrossRef] [Green Version]
- Barmashenko, G.; Buttgereit, J.; Herring, N.; Bader, M.; Ozcelik, C.; Manahan-Vaughan, D.; Braunewell, K.H. Regulation of hippocampal synaptic plasticity thresholds and changes in exploratory and learning behavior in dominant negative NPR-B mutant rats. Front. Mol. Neurosci. 2014, 7, 95. [Google Scholar] [CrossRef] [Green Version]
- Muüller, D.; Hida, B.; Guidone, G.; Speth, R.C.; Michurina, T.V.; Enikolopov, G.; Middendorff, R. Expression of guanylyl cyclase (GC)-A and GC-B during brain development: Evidence for a role of GC-B in perinatal neurogenesis. Endocrinology 2009, 150, 5520–5529. [Google Scholar] [CrossRef] [Green Version]
- Ma, Q.; Zhang, L. C-type natriuretic peptide functions as an innate neuroprotectant in neonatal hypoxic-ischemic brain injury in mouse via natriuretic peptide receptor 2. Exp. Neurol. 2018, 304, 58–66. [Google Scholar] [CrossRef] [PubMed]
- Espiner, E.A.; Dalrymple-Alford, J.C.; Prickett, T.C.R.; Alamri, Y.; Anderson, T.J. C-type natriuretic peptide in Parkinson’s disease: Reduced secretion and response to deprenyl. J. Neural Transm. 2014, 121, 371–378. [Google Scholar] [CrossRef]
- Ceylan, M.; Yalcin, A.; Bayraktutan, O.F.; Laloglu, E. Serum NT-pro CNP levels in epileptic seizure, psychogenic non-epileptic seizure, and healthy subjects. Neurol. Sci. 2018, 39, 2135–2139. [Google Scholar] [CrossRef]
- Bohara, M.; Kambe, Y.; Nagayama, T.; Tokimura, H.; Arita, K.; Miyata, A. C-type natriuretic peptide modulates permeability of the blood–brain barrier. J. Cereb. Blood Flow Metab. 2014, 34, 589–596. [Google Scholar] [CrossRef] [Green Version]
- Bélanger, M.; Magistretti, P.J. The role of astroglia in neuroprotection. Dialogues Clin. Neurosci. 2009, 11, 281–295. [Google Scholar]
- Felipo, V.; Butterworth, R.F. Neurobiology of ammonia. Prog. Neurobiol. 2002, 67, 259–279. [Google Scholar] [CrossRef]
- AdliMoghaddam, A.; Sabbir, M.G.; Albensi, B.C. Ammonia as a potential neurotoxic factor in Alzheimer’s disease. Front. Mol. Neurosci. 2016, 9, 57. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tivers, M.S.; Handel, I.; Gow, A.G.; Lipscomb, V.J.; Jalan, R.; Mellanby, R.J. Hyperammonemia and systemic inflammatory response syndrome predicts presence of hepatic encephalopathy in dogs with congenital portosystemic shunts. PLoS ONE 2014, 9, e82303. [Google Scholar] [CrossRef] [PubMed]
- Jayakumar, A.; Norenberg, M.D. Hyperammonemia in hepatic encephalopathy. J. Clin. Exp. Hepatol. 2018, 8, 272–280. [Google Scholar] [CrossRef] [PubMed]
- Felipo, V. Hepatic encephalopathy: Effects of liver failure on brain function. Nat. Rev. Neurosci. 2013, 14, 851–858. [Google Scholar] [CrossRef]
- Kornerup, L.S.; Gluud, L.L.; Vilstrup, H.; Dam, G. Update on the therapeutic management of hepatic encephalopathy. Curr. Gastroenterol. Rep. 2018, 20, 21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rockey, N.C.; Rahimi, R.S. Hepatic encephalopathy: Pharmacological therapies targeting ammonia. Semin. Liver Dis. 2016, 36, 048–055. [Google Scholar] [CrossRef] [Green Version]
- Zacharias, H.D.; Zacharias, A.P.; Gluud, L.L.; Morgan, M.Y. Pharmacotherapies that specifically target ammonia for the prevention and treatment of hepatic encephalopathy in adults with cirrhosis. Cochrane Database Syst. Rev. 2019, 6, CD012334. [Google Scholar] [CrossRef]
- Leone, A.M.; Kao, L.M.; McMillian, M.K.; Nie, A.Y.; Parker, J.B.; Kelley, M.F.; Usuki, E.; Parkinson, A.; Lord, P.G.; Johnson, M.D. Evaluation of felbamate and other antiepileptic drug toxicity potential based on hepatic protein covalent binding and gene expression. Chem. Res. Toxicol. 2007, 20, 600–608. [Google Scholar] [CrossRef]
- Konopacka, A.; Fręśko, I.; Piaskowski, S.; Albrecht, J.; Zielinska, M. Ammonia affects the activity and expression of soluble and particulate GC in cultured rat astrocytes. Neurochem. Int. 2006, 48, 553–558. [Google Scholar] [CrossRef]
- Zielinska, M.; Fręśko, I.; Konopacka, A.; Felipo, V.; Albrecht, J. Hyperammonemia inhibits the natriuretic peptide receptor 2 (NPR-2)-mediated cyclic GMP synthesis in the astrocytic compartment of rat cerebral cortex slices. Neurotoxicology 2007, 28, 1260–1263. [Google Scholar] [CrossRef] [PubMed]
- Konopacka, A.; Zielinska, M.; Albrecht, J. Ammonia inhibits the C-type natriuretic peptide-dependent cyclic GMP synthesis and calcium accumulation in a rat brain endothelial cell line. Neurochem. Int. 2008, 52, 1160–1166. [Google Scholar] [CrossRef] [PubMed]
- Agusti, A.; Hernández-Rabaza, V.; Balzano, T.; Taoro-Gonzalez, L.; Ibañez-Grau, A.; Cabrera-Pastor, A.; Fustero, S.; Llansola, M.; Montoliu, C.; Felipo, V. Sildenafil reduces neuroinflammation in cerebellum, restores GABAergic tone, and improves motor in-coordination in rats with hepatic encephalopathy. CNS Neurosci. Ther. 2017, 23, 386–394. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De França, M.E.R.; Peixoto, C.A. cGMP signaling pathway in hepatic encephalopathy neuroinflammation and cognition. Int. Immunopharmacol. 2020, 79, 106082. [Google Scholar] [CrossRef]
- Bollen, E.; Prickaerts, J. Phosphodiesterases in neurodegenerative disorders. IUBMB Life 2012, 64, 965–970. [Google Scholar] [CrossRef]
- Liu, L.; Xu, H.; Ding, S.; Wang, D.; Song, G.; Huang, X. Phosphodiesterase 5 inhibitors as novel agents for the treatment of Alzheimer’s disease. Brain Res. Bull. 2019, 153, 223–231. [Google Scholar] [CrossRef]
- VerPlank, J.J.S.; Tyrkalska, S.D.; Fleming, A.; Rubinsztein, D.C.; Goldberg, A.L. cGMP via PKG activates 26S proteasomes and enhances degradation of proteins, including ones that cause neurodegenerative diseases. Proc. Natl. Acad. Sci. USA 2020, 117, 14220–14230. [Google Scholar] [CrossRef] [PubMed]
- Reierson, G.W.; Guo, S.; Mastronardi, C.; Licinio, J.; Wong, M.-L. cGMP signaling, phosphodiesterases and major depressive disorder. Curr. Neuropharmacol. 2011, 9, 715–727. [Google Scholar] [CrossRef] [Green Version]
- Lorget, F.; Kaci, N.; Peng, J.; Benoist-Lasselin, C.; Mugniery, E.; Oppeneer, T.; Wendt, D.J.; Bell, S.M.; Bullens, S.; Bunting, S.; et al. Evaluation of the therapeutic potential of a CNP analog in a Fgfr3 mouse model recapitulating achondroplasia. Am. J. Hum. Genet. 2012, 91, 1108–1114. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Breinholt, V.M.; Rasmussen, C.E.; Mygind, P.H.; Kjelgaard-Hansen, M.; Faltinger, F.; Bernhard, A.; Zettler, J.; Hersel, U. TransCon CNP, a sustained-release C-type natriuretic peptide prodrug, a potentially safe and efficacious new therapeutic modality for the treatment of comorbidities associated with fibroblast growth factor receptor 3–related skeletal dysplasias. J. Pharmacol. Exp. Ther. 2019, 370, 459–471. [Google Scholar] [CrossRef] [PubMed]
- Day, A.; Jameson, Z.; Hyde, C.; Simbi, B.; Fowkes, R.; Lawson, C. C-type natriuretic peptide (CNP) inhibition of interferon-γ-mediated gene expression in human endothelial cells in vitro. Biosensors 2018, 8, 86. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bae, C.-R.; Hino, J.; Hosoda, H.; Miyazato, M.; Kangawa, K. C-type natriuretic peptide (CNP) in endothelial cells attenuates hepatic fibrosis and inflammation in non-alcoholic steatohepatitis. Life Sci. 2018, 209, 349–356. [Google Scholar] [CrossRef] [PubMed]
- Tomasiuk, R.; Szlufik, S.; Friedman, A.; Koziorowski, D. Ropinirole treatment in Parkinson’s disease associated with higher serum level of inflammatory biomarker NT-proCNP. Neurosci. Lett. 2014, 566, 147–150. [Google Scholar] [CrossRef]
- Tanabe, K.; Matsushima-Nishiwaki, R.; Kozawa, O.; Iida, H. Dexmedetomidine suppresses interleukin-1β-induced interleukin-6 synthesis in rat glial cells. Int. J. Mol. Med. 2014, 34, 1032–1038. [Google Scholar] [CrossRef] [Green Version]
- Tanabe, K.; Matsushima-Nishiwaki, R.; Yamaguchi, S.; Iida, H.; Dohi, S.; Kozawa, O. Mechanisms of tumor necrosis factor-α-induced interleukin-6 synthesis in glioma cells. J. Neuroinflammation 2010, 7, 16. [Google Scholar] [CrossRef] [Green Version]
- De Souza, D.F.; Wartchow, K.; Hansen, F.; Lunardi, P.; Guerra, M.C.; Nardin, P.; Gonçalves, C.-A. Interleukin-6-induced S100B secretion is inhibited by haloperidol and risperidone. Prog. Neuropsychopharmacol. Biol. Psychiatry 2013, 43, 14–22. [Google Scholar] [CrossRef] [Green Version]
- Neary, J.; Woodson, C.; Blicharska, J.; Norenberg, L.; Norenberg, M. Effect of ammonia on calcium homeostasis in primary astrocyte cultures. Brain Res. 1990, 524, 231–235. [Google Scholar] [CrossRef]
- Blanco, V.M.; Márquez, M.S.; Alvarez-Leefmans, F.J. Parallel changes in intracellular water volume and pH induced by NH3/NH4+exposure in single neuroblastoma cells. Cell. Physiol. Biochem. 2013, 32, 57–76. [Google Scholar] [CrossRef] [Green Version]
- Hilgier, W.; Węgrzynowicz, M.; Ruszkiewicz, J.; Oja, S.S.; Saransaari, P.; Albrecht, J. Direct exposure to ammonia and hyperammonemia increase the extracellular accumulation and degradation of astroglia-derived glutathione in the rat prefrontal cortex. Toxicol. Sci. 2010, 117, 163–168. [Google Scholar] [CrossRef] [Green Version]
- Yang, C.Z.; Li, H.L.; Zhou, Y.; Chai, R.C.; Zhao, R.; Dong, Y.; Xu, Z.Y.; Lau, L.T.; Yingge, Z.; Teng, J.; et al. A new specialization in astrocytes: Glutamate- and ammonia-induced nuclear size changes. J. Neurosci. Res. 2011, 89, 2041–2051. [Google Scholar] [CrossRef]
- Laemmle, A.; Gallagher, R.C.; Keogh, A.; Stricker, T.; Gautschi, M.; Nuoffer, J.-M.; Baumgartner, M.R.; Haberle, J. Frequency and pathophysiology of acute liver failure in Ornithine Transcarbamylase Deficiency (OTCD). PLoS ONE 2016, 11, e0153358. [Google Scholar] [CrossRef] [Green Version]
- Kondo, T.; Setoguchi, T.; Taga, T. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc. Natl. Acad. Sci. USA 2004, 101, 781–786. [Google Scholar] [CrossRef] [Green Version]
- Régina, A.; Romero, I.A.; Greenwood, J.; Adamson, P.; Bourre, J.M.; Couraud, P.O.; Roux, F. Dexamethasone regulation of P-glycoprotein activity in an immortalized rat brain endothelial cell line, GPNT. J. Neurochem. 1999, 73. [Google Scholar]
- Thompson, I.R.; Chand, A.N.; Jonas, K.C.; Burrin, J.M.; Steinhelper, M.E.; Wheeler-Jones, C.P.; McArdle, C.A.; Fowkes, R.C. Molecular characterisation and functional interrogation of a local natriuretic peptide system in rodent pituitaries, αT3-1 and LβT2 gonadotroph cells. J. Endocrinol. 2009, 203, 215–229. [Google Scholar] [CrossRef]
- Mirczuk, S.M.; Lessey, A.J.; Catterick, A.R.; Perrett, R.M.; Scudder, C.J.; Read, J.E.; Lipscomb, V.J.; Niessen, S.J.; Childs, A.J.; McArdle, C.A.; et al. Regulation and function of C-type natriuretic peptide (CNP) in gonadotrope-derived cell lines. Cells 2019, 8, 1086. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Heinrich, L.F.; Andersen, D.K.; Cleasby, M.E.; Lawson, C. Long-term high fat feeding of rats results in increased numbers of circulating microvesicles with pro-inflammatory effects on endothelial cells. Br. J. Nutr. 2015, 113, 1704–1711. [Google Scholar] [CrossRef] [Green Version]
- Thiriet, N.; Esteve, L.; Aunis, D.; Zwiller, J. Immediate early gene induction by natriuretic peptides in PC12 phaeochromocytoma and C6 glioma cells. NeuroReport 1997, 8, 399–402. [Google Scholar] [CrossRef] [PubMed]
- Sorci, G.; Spreca, A.; Donato, R.; Rambotti, M.G. Detection of membrane-bound guanylate cyclase activity in rat C6 glioma cells at different growth states following activation by natriuretic peptides. Brain Res. 1995, 683, 51–58. [Google Scholar] [CrossRef]
- Hesse, R.; Lausser, L.; Gummert, P.; Schmid, F.; Wahler, A.; Schnack, C.; Kroker, K.S.; Otto, M.; Tumani, H.; Kestler, H.A.; et al. Reduced cGMP levels in CSF of AD patients correlate with severity of dementia and current depression. Alzheimer’s Res. Ther. 2017, 9, 17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peake, N.J.; Pavlov, A.M.; D’Souza, A.; Pingguan-Murphy, B.; Sukhorukov, G.B.; Hobbs, A.J.; Chowdhury, T.T. Controlled release of C-type natriuretic peptide by microencapsulation dampens proinflammatory effects induced by IL-1β in cartilage explants. Biomacromolecules 2015, 16, 524–531. [Google Scholar] [CrossRef] [PubMed]
- Görg, B.; Qvartskhava, N.; Bidmon, H.-J.; Palomero-Gallagher, N.; Kircheis, G.; Zilles, K.; Häussinger, D. Oxidative stress markers in the brain of patients with cirrhosis and hepatic encephalopathy. Hepatology 2010, 52, 256–265. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Saint-Pol, J.; Gosselet, F.; Duban-Deweer, S.; Pottiez, G.; Karamanos, Y. Targeting and crossing the blood-brain barrier with extracellular vesicles. Cells 2020, 9, 851. [Google Scholar] [CrossRef] [Green Version]
- Lawson, C.; Vicencio, J.M.; Yellon, D.M.; Davidson, S.M. Microvesicles and exosomes: New players in metabolic and cardiovascular disease. J. Endocrinol. 2016, 228, R57–R71. [Google Scholar] [CrossRef]
- Taheri, B.; Soleimani, M.; Aval, S.F.; Memari, F.; Zarghami, N. C6 glioma-derived microvesicles stimulate the proliferative and metastatic gene expression of normal astrocytes. Neurosci. Lett. 2018, 685, 173–178. [Google Scholar] [CrossRef]
- Ma, C.; Chen, H.; Zhang, S.; Yan, Y.; Wu, R.; Wang, Y.; Liu, Y.; Yang, L.; Liu, M. Exosomal and extracellular HMGB1 have opposite effects on SASH1 expression in rat astrocytes and glioma C6 cells. Biochem. Biophys. Res. Commun. 2019, 518, 325–330. [Google Scholar] [CrossRef]
- Izquierdo-Altarejos, P.; Cabrera-Pastor, A.; Gonzalez-King, H.; Montoliu, C.; Felipo, V. Extracellular vesicles from hyperammonemic Rats Induce Neuroinflammation and Motor Incoordination in Control Rats. Cells 2020, 9, 572. [Google Scholar] [CrossRef] [Green Version]
- Roux, F.; Couraud, P.-O. Rat brain endothelial cell lines for the study of blood–brain barrier permeability and transport functions. Cell. Mol. Neurobiol. 2005, 25, 41–57. [Google Scholar] [CrossRef] [Green Version]
- Parkinson, F.E.; Ferguson, J.; Zamzow, C.R.; Xiong, W. Gene expression for enzymes and transporters involved in regulating adenosine and inosine levels in rat forebrain neurons, astrocytes and C6 glioma cells. J. Neurosci. Res. 2006, 84, 801–808. [Google Scholar] [CrossRef]
- Galland, F.; Seady, M.; Taday, J.; Smaili, S.S.; Gonçalves, C.A.; Leite, M.C. Astrocyte culture models: Molecular and function characterization of primary culture, immortalized astrocytes and C6 glioma cells. Neurochem. Int. 2019, 131, 104538. [Google Scholar] [CrossRef] [PubMed]
- Portais, J.-C.; Schuster, R.; Merle, M.; Canioni, P. Metabolic flux determination in C6 glioma cells using carbon-13 distribution upon [1-13C]glucose incubation. Eur. J. Biochem. 1993, 217, 457–468. [Google Scholar] [CrossRef] [PubMed]
- Lie, S.; Wang, T.; Forbes, B.; Proud, C.G.; Petersen, J. The ability to utilise ammonia as nitrogen source is cell type specific and intricately linked to GDH, AMPK and mTORC1. Sci. Rep. 2019, 9, 1–15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Görg, B.; Karababa, A.; Shafigullina, A.; Bidmon, H.J.; Häussinger, D. Ammonia-induced senescence in cultured rat astrocytes and in human cerebral cortex in hepatic encephalopathy. Glia 2015, 63, 37–50. [Google Scholar] [CrossRef] [PubMed]
- Bodega, G.; Segura, B.; Ciordia, S.; Mena, M.D.C.; López-Fernández, L.A.; García, M.I.; Trabado, I.; Suárez, I. Ammonia affects astroglial proliferation in culture. PLoS ONE 2015, 10, e0139619. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Buzańska, L.; Zabłocka, B.; Dybel, A.; Domańska-Janik, K.; Albrecht, J. Delayed induction of apoptosis by ammonia in C6 glioma cells. Neurochem. Int. 2000, 37, 287–297. [Google Scholar] [CrossRef]
- Thompson, I.R.; Mirczuk, S.M.; Smith, L.; Lessey, A.J.; Simbi, B.; Sunters, A.; Baxter, G.F.; Lipscomb, V.J.; McGonnell, I.M.; Wheeler-Jones, C.P.; et al. Homologous and heterologous desensitization of guanylyl cyclase-B signaling in GH3 somatolactotropes. Cell Tissue Res. 2014, 355, 425–436. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fowkes, R.C.; Forrest-Owen, W.; McArdle, C.A. C-type natriuretic peptide (CNP) effects in anterior pituitary cell lines: Evidence for homologous desensitisation of CNP-stimulated cGMP accumulation in alpha T3-1 gonadotroph-derived cells. J. Endocrinol. 2000, 166, 195–203. [Google Scholar] [CrossRef]
- Wang, H.-M.; Zhang, T.; Li, Q.; Huang, J.-K.; Chen, R.-F.; Sun, X.-J. Inhibition of glycogen synthase kinase-3β by lithium chloride suppresses 6-hydroxydopamine-induced inflammatory response in primary cultured astrocytes. Neurochem. Int. 2013, 63, 345–353. [Google Scholar] [CrossRef]
- Wang, L.; Hagemann, T.L.; Kalwa, H.; Michel, T.; Messing, A.; Feany, M.B. Nitric oxide mediates glial-induced neurodegeneration in Alexander disease. Nat. Commun. 2015, 6, 8966. [Google Scholar] [CrossRef] [Green Version]
- Loughney, K.; Hill, T.R.; Florio, V.A.; Uher, L.; Rosman, G.J.; Wolda, S.L.; Jones, B.A.; Howard, M.L.; McAllister-Lucas, L.M.; Sonnenburg, W.K.; et al. Isolation and characterization of cDNAs encoding PDE5A, a human cGMP-binding, cGMP-specific 3′,5′-cyclic nucleotide phosphodiesterase. Gene 1998, 216, 139–147. [Google Scholar] [CrossRef]
- Fawcett, L.; Baxendale, R.; Stacey, P.; McGrouther, C.; Harrow, I.; Soderling, S.; Hetman, J.; Beavo, J.A.; Phillips, S.C. Molecular cloning and characterization of a distinct human phosphodiesterase gene family: PDE11A. Proc. Natl. Acad. Sci. USA 2000, 97, 3702–3707. [Google Scholar] [CrossRef]
- Sager, G.; Ravna, A.W. Cellular efflux of cAMP and cGMP—a question about selectivity. Mini Rev. Med. Chem. 2009, 9, 1009–1013. [Google Scholar] [CrossRef]
- Jördens, M.S.; Keitel, V.; Karababa, A.; Zemtsova, I.; Bronger, H.; Häussinger, D.; Görg, B. Multidrug resistance-associated protein 4 expression in ammonia-treated cultured rat astrocytes and cerebral cortex of cirrhotic patients with hepatic encephalopathy. Glia 2015, 63, 2092–2105. [Google Scholar] [CrossRef]
- Neary, J.T.; Whittemore, S.R.; Zhu, Q.; Norenberg, M.D. Destabilization of glial fibrillary acidic protein mRNA in astrocytes by ammonia and protection by extracellular ATP. J. Neurochem. 1994, 63, 2021–2027. [Google Scholar] [CrossRef] [PubMed]
- Norenberg, M.D.; Neary, J.T.; Norenberg, L.-O.B.; McCarthy, M. Ammonia induced decrease in glial fibrillary acidic protein in cultured astrocytes. J. Neuropathol. Exp. Neurol. 1990, 49, 399–405. [Google Scholar] [CrossRef]
- Galland, F.; Negri, E.; Da Ré, C.; Fróes, F.; Strapazzon, L.; Guerra, M.C.; Tortorelli, L.S.; Gonçalves, C.-A.; Leite, M.C. Hyperammonemia compromises glutamate metabolism and reduces BDNF in the rat hippocampus. NeuroToxicology 2017, 62, 46–55. [Google Scholar] [CrossRef] [PubMed]
- Probst, J.; Kölker, S.; Okun, J.G.; Kumar, A.; Gursky, E.; Posset, R.; Hoffmann, G.F.; Peravali, R.; Zielonka, M. Chronic hyperammonemia causes a hypoglutamatergic and hyperGABAergic metabolic state associated with neurobehavioral abnormalities in zebrafish larvae. Exp. Neurol. 2020, 331, 113330. [Google Scholar] [CrossRef]
- Santos, C.L.; Bobermin, L.D.; Souza, D.G.; Bellaver, B.; Bellaver, G.; Arús, B.A.; Souza, D.O.; Gonçalves, C.-A.; Quincozes-Santos, A. Lipoic acid and N-acetylcysteine prevent ammonia-induced inflammatory response in C6 astroglial cells: The putative role of ERK and HO1 signaling pathways. Toxicol. Vitr. 2015, 29, 1350–1357. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Delpech, J.-C.; Herron, S.; Botros, M.B.; Ikezu, T. Neuroimmune crosstalk through extracellular vesicles in health and disease. Trends Neurosci. 2019, 42, 361–372. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Regan, J.T.; Mirczuk, S.M.; Scudder, C.J.; Stacey, E.; Khan, S.; Worwood, M.; Powles, T.; Dennis-Beron, J.S.; Ginley-Hidinger, M.; McGonnell, I.M.; et al. Sensitivity of the Natriuretic Peptide/cGMP System to Hyperammonaemia in Rat C6 Glioma Cells and GPNT Brain Endothelial Cells. Cells 2021, 10, 398. https://doi.org/10.3390/cells10020398
Regan JT, Mirczuk SM, Scudder CJ, Stacey E, Khan S, Worwood M, Powles T, Dennis-Beron JS, Ginley-Hidinger M, McGonnell IM, et al. Sensitivity of the Natriuretic Peptide/cGMP System to Hyperammonaemia in Rat C6 Glioma Cells and GPNT Brain Endothelial Cells. Cells. 2021; 10(2):398. https://doi.org/10.3390/cells10020398
Chicago/Turabian StyleRegan, Jacob T., Samantha M. Mirczuk, Christopher J. Scudder, Emily Stacey, Sabah Khan, Michael Worwood, Torinn Powles, J. Sebastian Dennis-Beron, Matthew Ginley-Hidinger, Imelda M. McGonnell, and et al. 2021. "Sensitivity of the Natriuretic Peptide/cGMP System to Hyperammonaemia in Rat C6 Glioma Cells and GPNT Brain Endothelial Cells" Cells 10, no. 2: 398. https://doi.org/10.3390/cells10020398
APA StyleRegan, J. T., Mirczuk, S. M., Scudder, C. J., Stacey, E., Khan, S., Worwood, M., Powles, T., Dennis-Beron, J. S., Ginley-Hidinger, M., McGonnell, I. M., Volk, H. A., Strickland, R., Tivers, M. S., Lawson, C., Lipscomb, V. J., & Fowkes, R. C. (2021). Sensitivity of the Natriuretic Peptide/cGMP System to Hyperammonaemia in Rat C6 Glioma Cells and GPNT Brain Endothelial Cells. Cells, 10(2), 398. https://doi.org/10.3390/cells10020398