1932

Abstract

Chemogenetics refers to experimental systems that dynamically regulate the activity of a recombinant protein by providing or withholding the protein's specific biochemical stimulus. Chemogenetic tools permit precise dynamic control of specific signaling molecules to delineate the roles of those molecules in physiology and disease. Yeast -amino acid oxidase (DAAO) enables chemogenetic manipulation of intracellular redox balance by generating hydrogen peroxide only in the presence of -amino acids. Advances in biosensors have allowed the precise quantitation of these signaling molecules. The combination of chemogenetic approaches with biosensor methodologies has opened up new lines of investigation, allowing the analysis of intracellular redox pathways that modulate physiological and pathological cell responses. We anticipate that newly developed transgenic chemogenetic models will permit dynamic modulation of cellularredox balance in diverse cells and tissues and will facilitate the identification and validation of novel therapeutic targets involved in both physiological redox pathways and pathological oxidative stress.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-pharmtox-012221-082339
2022-01-06
2024-12-09
Loading full text...

Full text loading...

/deliver/fulltext/pharmtox/62/1/annurev-pharmtox-012221-082339.html?itemId=/content/journals/10.1146/annurev-pharmtox-012221-082339&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Cui H, Kong Y, Zhang H. 2012. Oxidative stress, mitochondrial dysfunction, and aging. J. Signal Transduct. 2012:646354
    [Google Scholar]
  2. 2. 
    Leopold JA, Loscalzo J 2005. Oxidative enzymopathies and vascular disease. Arterioscler. Thromb. Vasc. Biol. 25:1332–40
    [Google Scholar]
  3. 3. 
    Kattoor AJ, Pothineni NVK, Palagiri D, Mehta JL 2017. Oxidative stress in atherosclerosis. Curr. Atheroscler. Rep. 19:1142
    [Google Scholar]
  4. 4. 
    Forrester SJ, Booz GW, Sigmund CD, Coffman TM, Kawai T et al. 2018. Angiotensin II signal transduction: an update on mechanisms of physiology and pathophysiology. Physiol. Rev. 98:31627–738
    [Google Scholar]
  5. 5. 
    Wang X, Wang W, Li L, Perry G, Lee H, Zhu X 2014. Oxidative stress and mitochondrial dysfunction in Alzheimer's disease. Biochim. Biophys. Acta Mol. Basis Dis. 1842:81240–47
    [Google Scholar]
  6. 6. 
    Emini Veseli B, Perrotta P, De Meyer GRA, Roth L, Van der Donckt C et al. 2017. Animal models of atherosclerosis. Eur. J. Pharmacol. 816:3–13
    [Google Scholar]
  7. 7. 
    Lindsey ML, Bolli R, Canty JM, Du X-J, Frangogiannis NG et al. 2018. Guidelines for experimental models of myocardial ischemia and infarction. Am. J. Physiol. Circ. Physiol. 314:4H812–38
    [Google Scholar]
  8. 8. 
    Houser SR, Margulies KB, Murphy AM, Spinale FG, Francis GS et al. 2012. Animal models of heart failure: a scientific statement from the American Heart Association. Circ. Res. 111:1131–50
    [Google Scholar]
  9. 9. 
    Schiattarella GG, Altamirano F, Tong D, French KM, Villalobos E et al. 2019. Nitrosative stress drives heart failure with preserved ejection fraction. Nature 568:7752351–56
    [Google Scholar]
  10. 10. 
    Cardinale D, Iacopo F, Cipolla CM 2020. Cardiotoxicity of anthracyclines. Front. Cardiovasc. Med 7:26
    [Google Scholar]
  11. 11. 
    Jenkins DJA, Kitts D, Giovannucci EL, Sahye-Pudaruth S, Paquette M et al. 2020. Selenium, antioxidants, cardiovascular disease, and all-cause mortality: a systematic review and meta-analysis of randomized controlled trials. Am. J. Clin. Nutr. 112:61642–52
    [Google Scholar]
  12. 12. 
    Bjelakovic G, Nikolova D, Gluud C 2013. Antioxidant supplements to prevent mortality. JAMA 310:111178–79
    [Google Scholar]
  13. 13. 
    Sies H. 2017. Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: oxidative eustress. Redox. Biol. 11:613–19
    [Google Scholar]
  14. 14. 
    Nathan C, Cunningham-Bussel A. 2013. Beyond oxidative stress: an immunologist's guide to reactive oxygen species. Nat. Rev. Immunol. 13:5349–61
    [Google Scholar]
  15. 15. 
    Waypa GB, Marks JD, Guzy RD, Mungai PT, Schriewer JM et al. 2013. Superoxide generated at mitochondrial complex III triggers acute responses to hypoxia in the pulmonary circulation. Am. J. Respir. Crit. Care Med. 187:4424–32
    [Google Scholar]
  16. 16. 
    Weinberg SE, Singer BD, Steinert EM, Martinez CA, Mehta MM et al. 2019. Mitochondrial complex III is essential for suppressive function of regulatory T cells. Nature 565:495–99
    [Google Scholar]
  17. 17. 
    Kalwa H, Sartoretto JL, Martinelli R, Romero N, Steinhorn BS et al. 2014. Central role for hydrogen peroxide in P2Y1 ADP receptor-mediated cellular responses in vascular endothelium. PNAS 111:93383–88
    [Google Scholar]
  18. 18. 
    Sartoretto JL, Kalwa H, Shiroto T, Sartoretto SM, Pluth MD et al. 2012. Role of Ca2+ in the control of H2O2-modulated phosphorylation pathways leading to eNOS activation in cardiac myocytes. PLOS ONE 7:9e44627
    [Google Scholar]
  19. 19. 
    Sartoretto JL, Kalwa H, Pluth MD, Lippard SJ, Michel T et al. 2011. Hydrogen peroxide differentially modulates cardiac myocyte nitric oxide synthesis. PNAS 108:3815792–97
    [Google Scholar]
  20. 20. 
    Hsieh H-J, Liu C-A, Huang B, Tseng AH, Wang DL. 2014. Shear-induced endothelial mechanotransduction: the interplay between reactive oxygen species (ROS) and nitric oxide (NO) and the pathophysiological implications. J. Biomed. Sci. 21:3
    [Google Scholar]
  21. 21. 
    Huang ZM, Gao E, Fonseca F, Hayashi H, Shang X et al. 2013. Convergence of G protein-coupled receptor and nitric oxide pathways determines the outcome to cardiac ischemic injury. Sci. Signal. 6:299ra95
    [Google Scholar]
  22. 22. 
    Jian Z, Han H, Zhang T, Puglisi J, Izu LT et al. 2014. Mechanochemotransduction during cardiomyocyte contraction is mediated by localized nitric oxide signaling. Sci. Signal. 7:317ra27
    [Google Scholar]
  23. 23. 
    Steinhorn B, Sartoretto JL, Sorrentino A, Romero N, Kalwa H et al. 2017. Insulin-dependent metabolic and inotropic responses in the heart are modulated by hydrogen peroxide from NADPH-oxidase isoforms NOX2 and NOX4.. Free Radic. Biol. Med. 113:16–25
    [Google Scholar]
  24. 24. 
    Goldstein BJ, Mahadev K, Wu X, Zhu L, Motoshima H. 2005. Role of insulin-induced reactive oxygen species in the insulin signaling pathway. Antioxid. Redox Signal. 7:7–81021–31
    [Google Scholar]
  25. 25. 
    Sies H. 2014. Role of metabolic H2O2 generation: redox signaling and oxidative stress. J. Biol. Chem. 289:138735–41
    [Google Scholar]
  26. 26. 
    Ushio-Fukai M. 2009. Compartmentalization of redox signaling through NADPH oxidase-derived ROS. Antioxid. Redox Signal. 11:61289–99
    [Google Scholar]
  27. 27. 
    Netto LES, Antunes F. 2016. The roles of peroxiredoxin and thioredoxin in hydrogen peroxide sensing and in signal transduction. Mol. Cells 39:165–71
    [Google Scholar]
  28. 28. 
    Ferguson GD, Bridge WJ. 2019. The glutathione system and the related thiol network in Caenorhabditis elegans. Redox Biol 24:101171
    [Google Scholar]
  29. 29. 
    Maron BA, Michel T. 2012. Subcellular localization of oxidants and redox modulation of endothelial nitric oxide synthase. Circ. J. 76:112497–512
    [Google Scholar]
  30. 30. 
    Bedard K, Krause K-H. 2007. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87:1245–313
    [Google Scholar]
  31. 31. 
    Li J-M. 2002. Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells. J. Biol. Chem. 277:2219952–60
    [Google Scholar]
  32. 32. 
    Saravi SSS, Eroglu E, Waldeck-Weiermair M, Sorrentino A, Steinhorn B et al. 2020. Differential endothelial signaling responses elicited by chemogenetic H2O2 synthesis. Redox Biol 36:101605
    [Google Scholar]
  33. 33. 
    Montiel V, Bella R, Michel LYM, Esfahani H, De Mulder D et al. 2020. Inhibition of aquaporin-1 prevents myocardial remodeling by blocking the transmembrane transport of hydrogen peroxide. Sci. Transl. Med. 12:564eaay2176
    [Google Scholar]
  34. 34. 
    Granger DN, Kvietys PR. 2015. Reperfusion injury and reactive oxygen species: the evolution of a concept. Redox Biol 6:524–51
    [Google Scholar]
  35. 35. 
    Furuhashi M. 2020. New insights into purine metabolism in metabolic diseases: role of xanthine oxidoreductase activity. Am. J. Physiol. Endocrinol. Metab. 319:5E827–34
    [Google Scholar]
  36. 36. 
    Kaludercic N, Mialet-Perez J, Paolocci N, Parini A, Di Lisa F. 2014. Monoamine oxidases as sources of oxidants in the heart. J. Mol. Cell. Cardiol. 73:34–42
    [Google Scholar]
  37. 37. 
    Holmström KM, Finkel T. 2014. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat. Rev. Mol. Cell Biol. 15:6411–21
    [Google Scholar]
  38. 38. 
    Finkel T. 2011. Signal transduction by reactive oxygen species. J. Cell Biol. 194:17–15
    [Google Scholar]
  39. 39. 
    Murphy MP. 2009. How mitochondria produce reactive oxygen species. Biochem. J. 417:11–13
    [Google Scholar]
  40. 40. 
    Oestreicher J, Morgan B. 2019. Glutathione: subcellular distribution and membrane transport. Biochem. Cell Biol. 97:3270–89
    [Google Scholar]
  41. 41. 
    Yoon E, Babar A, Choudhary M, Kutner M, Pyrsopoulos N. 2016. Acetaminophen-induced hepatotoxicity: a comprehensive update. J. Clin. Transl. Hepatol. 4:2131–42
    [Google Scholar]
  42. 42. 
    Fomenko DE, Koc A, Agisheva N, Jacobsen M, Kaya A et al. 2011. Thiol peroxidases mediate specific genome-wide regulation of gene expression in response to hydrogen peroxide. PNAS 108:72729–34
    [Google Scholar]
  43. 43. 
    Kil IS, Lee SK, Ryu KW, Woo HA, Hu MC et al. 2012. Feedback control of adrenal steroidogenesis via H2O2-dependent, reversible inactivation of peroxiredoxin III in mitochondria. Mol. Cell 46:5584–94
    [Google Scholar]
  44. 44. 
    Van Laer K, Dick TP. 2016. Utilizing natural and engineered peroxiredoxins as intracellular peroxide reporters. Mol. Cells 39:146–52
    [Google Scholar]
  45. 45. 
    Zhang J, Duan D, Osama A, Fang J 2021. Natural molecules targeting thioredoxin system and their therapeutic potentials. Antioxid. Redox Signal. 34:141083–107
    [Google Scholar]
  46. 46. 
    Fan Y, Makar M, Wang MX, Ai H-W. 2017. Monitoring thioredoxin redox with a genetically encoded red fluorescent biosensor. Nat. Chem. Biol. 13:91045–52
    [Google Scholar]
  47. 47. 
    Lo Conte M, Carroll KS. 2013. The redox biochemistry of protein sulfenylation and sulfinylation. J. Biol. Chem. 288:3726480–88
    [Google Scholar]
  48. 48. 
    Qin F, Rounds NK, Mao W, Kawai K, Liang CS 2001. Antioxidant vitamins prevent cardiomyocyte apoptosis produced by norepinephrine infusion in ferrets. Cardiovasc. Res. 51:4736–48
    [Google Scholar]
  49. 49. 
    Zimmer HG. Regulation of and intervention into the oxidative pentose phosphate pathway and adenine nucleotide metabolism in the heart. Mol. Cell. Biochem160–161–101–9
    [Google Scholar]
  50. 50. 
    Ashoka AH, Ali F, Tiwari R, Kumari R, Pramanik SK, Das A. 2020. Recent advances in fluorescent probes for detection of HOCl and HNO. ACS Omega 5:41730–42
    [Google Scholar]
  51. 51. 
    Jiang X, Wang L, Carroll SL, Chen J, Wang MC, Wang J 2018. Challenges and opportunities for small-molecule fluorescent probes in redox biology applications. Antioxid. Redox Signal. 29:6518–40
    [Google Scholar]
  52. 52. 
    Winterbourn CC. 2014. The challenges of using fluorescent probes to detect and quantify specific reactive oxygen species in living cells. Biochim. Biophys. Acta 1840:2730–38
    [Google Scholar]
  53. 53. 
    Zhu H, Fan J, Du J, Peng X 2016. Fluorescent probes for sensing and imaging within specific cellular organelles. Acc. Chem. Res. 49:102115–26
    [Google Scholar]
  54. 54. 
    Fujikawa Y, Roma LP, Sobotta MC, Rose AJ, Diaz MB et al. 2016. Mouse redox histology using genetically encoded probes. Sci. Signal. 9:419rs1
    [Google Scholar]
  55. 55. 
    Bilan DS, Belousov VV. 2016. HyPer family probes: state of the art. Antioxid. Redox Signal. 24:13731–51
    [Google Scholar]
  56. 56. 
    Braissant O, McLin VA, Cudalbu C. 2013. Ammonia toxicity to the brain. J. Inherit. Metab. Dis. 36:4595–612
    [Google Scholar]
  57. 57. 
    Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS et al. 2006. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 3:4281–86
    [Google Scholar]
  58. 58. 
    Bilan DS, Belousov VV. 2016. New tools for redox biology: from imaging to manipulation. Free Radic. Biol. Med. 109:167–88
    [Google Scholar]
  59. 59. 
    Matlashov ME, Bogdanova YA, Ermakova GV, Mishina NM, Ermakova YG et al. 2015. Fluorescent ratiometric pH indicator SypHer2: applications in neuroscience and regenerative biology. Biochim. Biophys. Acta 1850:112318–28
    [Google Scholar]
  60. 60. 
    Pak VV, Ezeriņa D, Lyublinskaya OG, Pedre B, Tyurin-Kuzmin PA et al. 2020. Ultrasensitive genetically encoded indicator for hydrogen peroxide identifies roles for the oxidant in cell migration and mitochondrial function. Cell Metab 31:3642–53.e6
    [Google Scholar]
  61. 61. 
    Steinhorn B, Sartoretto JL, Sorrentino A, Romero N, Kalwa H et al. 2017. Insulin-dependent metabolic and inotropic responses in the heart are modulated by hydrogen peroxide from NADPH-oxidase isoforms NOX2 and NOX4. Free Radic. Biol. Med. 113:August16–25
    [Google Scholar]
  62. 62. 
    Waypa GB, Marks JD, Guzy RD, Mungai PT, Schriewer JM et al. 2013. Superoxide generated at mitochondrial complex III triggers acute responses to hypoxia in the pulmonary circulation. Am. J. Respir. Crit. Care Med. 187:4424–32
    [Google Scholar]
  63. 63. 
    Waypa GB, Marks JD, Guzy R, Mungai PT, Schriewer J et al. 2010. Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells. Circ. Res. 106:3526–35
    [Google Scholar]
  64. 64. 
    Ezeriņa D, Morgan B, Dick TP 2014. Imaging dynamic redox processes with genetically encoded probes. J. Mol. Cell. Cardiol. 73:43–49
    [Google Scholar]
  65. 65. 
    Zou Y, Wang A, Shi M, Chen X, Liu R et al. 2018. Analysis of redox landscapes and dynamics in living cells and in vivo using genetically encoded fluorescent sensors. Nat. Protoc. 13:102362–86
    [Google Scholar]
  66. 66. 
    Hung YP, Albeck JG, Tantama M, Yellen G. 2011. Imaging cytosolic NADH-NAD+ redox state with a genetically encoded fluorescent biosensor. Cell Metab 14:4545–54
    [Google Scholar]
  67. 67. 
    Bubb KJ, Drummond GR, Figtree GA. 2020. New opportunities for targeting redox dysregulation in cardiovascular disease. Cardiovasc. Res. 116:3532–44
    [Google Scholar]
  68. 68. 
    Waypa GB, Smith KA, Schumacker PT. 2016. O2 sensing, mitochondria and ROS signaling: The fog is lifting. Mol. Aspects Med.47–4876–89
    [Google Scholar]
  69. 69. 
    Santolini J, Wootton SA, Jackson AA, Feelisch M 2019. The redox architecture of physiological function. Curr. Opin. Physiol. 9:34–47
    [Google Scholar]
  70. 70. 
    Stefanska J, Pawliczak R. 2008. Apocynin: molecular aptitudes. Mediators Inflamm 2008.106507
    [Google Scholar]
  71. 71. 
    Zhang M, Brewer AC, Schröder K, Santos CXC, Grieve DJ et al. 2010. NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. PNAS 107:4218121–26
    [Google Scholar]
  72. 72. 
    Zhang M, Prosser BL, Bamboye MA, Gondim ANS, Santos CX et al. 2015. Contractile function during angiotensin-II activation: Increased Nox2 activity modulates cardiac calcium handling via phospholamban phosphorylation. J. Am. Coll. Cardiol. 66:3261–72
    [Google Scholar]
  73. 73. 
    Rapti K, Diokmetzidou A, Kloukina I, Milner DJ, Varela A et al. 2017. Opposite effects of catalase and MnSOD ectopic expression on stress induced defects and mortality in the desmin deficient cardiomyopathy model. Free Radic. Biol. Med. 110:June206–18
    [Google Scholar]
  74. 74. 
    Leskovac V, Trivić S, Wohlfahrt G, Kandrac J, Pericin D 2005. Glucose oxidase from Aspergillus niger: the mechanism of action with molecular oxygen, quinones, and one-electron acceptors. Int. J. Biochem. Cell Biol. 37:4731–50
    [Google Scholar]
  75. 75. 
    Vlasov K, Van Dort CJ, Solt K 2018. Optogenetics and chemogenetics. Chemical and Biochemical Approaches for the Study of Anesthetic Function Part B RG Eckenhoff, IJ Dmochowski 603181–96 Cambridge, MA: Academic
    [Google Scholar]
  76. 76. 
    Kim CK, Adhikari A, Deisseroth K 2017. Integration of optogenetics with complementary methodologies in systems neuroscience. Nat. Rev. Neurosci. 18:4222–35
    [Google Scholar]
  77. 77. 
    Urban DJ, Roth BL. 2015. DREADDs (designer receptors exclusively activated by designer drugs): chemogenetic tools with therapeutic utility. Annu. Rev. Pharmacol. Toxicol. 55:399–417
    [Google Scholar]
  78. 78. 
    Wang L, Zhu L, Meister J, Bone DBJ, Pydi SP et al. 2021. Use of DREADD technology to identify novel targets for antidiabetic drugs. Annu. Rev. Pharmacol. Toxicol. 61:421–40
    [Google Scholar]
  79. 79. 
    Dimidschstein J, Chen Q, Tremblay R, Rogers SL, Saldi G-A et al. 2016. A viral strategy for targeting and manipulating interneurons across vertebrate species. Nat. Neurosci. 19:121743–49
    [Google Scholar]
  80. 80. 
    Steinhorn B, Sorrentino A, Badole S, Bogdanova Y, Belousov V, Michel T. 2018. Chemogenetic generation of hydrogen peroxide in the heart induces severe cardiac dysfunction. Nat. Commun. 9:14044
    [Google Scholar]
  81. 81. 
    Sahoo S, Aurich MK, Jonsson JJ, Thiele I. 2014. Membrane transporters in a human genome-scale metabolic knowledgebase and their implications for disease. Front. Physiol. 5:91
    [Google Scholar]
  82. 82. 
    Sorrentino A, Michel T. 2020. Redox à la carte: novel chemogenetic models of heart failure. Br. J. Pharmacol. 177:143162–67
    [Google Scholar]
  83. 83. 
    Manvich DF, Webster KA, Foster SL, Farrell MS, Ritchie JC et al. 2018. The DREADD agonist clozapine N-oxide (CNO) is reverse-metabolized to clozapine and produces clozapine-like interoceptive stimulus effects in rats and mice. Sci. Rep. 8:13840
    [Google Scholar]
  84. 84. 
    Sorrentino A, Steinhorn B, Troncone L, Saravi SSS, Badole S et al. 2019. Reversal of heart failure in a chemogenetic model of persistent cardiac redox stress. Am. J. Physiol. Heart Circ. Physiol. 317:3H617–26
    [Google Scholar]
  85. 85. 
    Magnus CJ, Lee PH, Bonaventura J, Zemla R, Gomez JL et al. 2019. Ultrapotent chemogenetics for research and potential clinical applications. Science 364:6436eaav5282
    [Google Scholar]
  86. 86. 
    Kaiser E, Tian Q, Wagner M, Barth M, Xian W et al. 2019. DREADD technology reveals major impact of Gq signalling on cardiac electrophysiology. Cardiovasc. Res. 115:61052–66
    [Google Scholar]
  87. 87. 
    Ferrantini C, Coppini R, Sacconi L 2019. Cardiomyocyte-specific Gq signalling and arrhythmias: novel insights from DREADD technology. Cardiovasc. Res. 115:6992–94
    [Google Scholar]
  88. 88. 
    Krebs HA. 1935. Metabolism of amino-acids: deamination of amino-acids. Biochem. J. 29:71620–44
    [Google Scholar]
  89. 89. 
    Pollegioni L, Sacchi S, Murtas G 2018. Human D-amino acid oxidase: structure, function, and regulation. Front. Mol. Biosci 5:November107
    [Google Scholar]
  90. 90. 
    Liu Y-L, Wang S-C, Hwu H-G, Fann CS-J, Yang U-C et al. 2016. Haplotypes of the D-amino acid oxidase gene are significantly associated with schizophrenia and its neurocognitive deficits. PLOS ONE 11:3e0150435
    [Google Scholar]
  91. 91. 
    Abou El-Magd RM, Park HK, Kawazoe T, Iwana S, Ono K et al. 2010. The effect of risperidone on D-amino acid oxidase activity as a hypothesis for a novel mechanism of action in the treatment of schizophrenia. J. Psychopharmacol. 24:71055–67
    [Google Scholar]
  92. 92. 
    Sasabe J, Miyoshi Y, Rakoff-Nahoum S, Zhang T, Mita M et al. 2016. Interplay between microbial d-amino acids and host d-amino acid oxidase modifies murine mucosal defence and gut microbiota. Nat. Microbiol. 1:July16125
    [Google Scholar]
  93. 93. 
    Nagano T, Yamao S, Terachi A, Yarimizu H, Itoh H et al. 2019. d-amino acid oxidase promotes cellular senescence via the production of reactive oxygen species. Life Sci. Alliance 2:1e201800045
    [Google Scholar]
  94. 94. 
    Pollegioni L, Langkau B, Tischer W, Ghisla S, Pilone MS 1993. Kinetic mechanism of d-amino acid oxidases from Rhodotorula gracilis and Trigonopsis variabilis. J. Biol. Chem. 268:1913850–57
    [Google Scholar]
  95. 95. 
    Sacchi S, Lorenzi S, Molla G, Pilone MS, Rossetti C, Pollegioni L 2002. Engineering the substrate specificity of d-amino-acid oxidase. J. Biol. Chem. 277:3027510–16
    [Google Scholar]
  96. 96. 
    Matlashov ME, Belousov VV, Enikolopov G. 2014. How much H2O2 is produced by recombinant D-amino acid oxidase in mammalian cells?. Antioxid. Redox Signal. 20:71039–44
    [Google Scholar]
  97. 97. 
    Rosini E, Pollegioni L, Ghisla S, Orru R, Molla G. 2009. Optimization of d-amino acid oxidase for low substrate concentrations—towards a cancer enzyme therapy. FEBS J 276:174921–32
    [Google Scholar]
  98. 98. 
    Pollegioni L, Molla G. 2011. New biotech applications from evolved D-amino acid oxidases. Trends Biotechnol 29:6276–83
    [Google Scholar]
  99. 99. 
    Chai Q, Lu T, Wang XL, Lee HC 2014. Hydrogen sulfide impairs shear stress-induced vasodilation in mouse coronary arteries. Pflügers Arch. 467:2329–40
    [Google Scholar]
  100. 100. 
    Zhang H, Bai Z, Zhu L, Liang Y, Fan X et al. 2020. Hydrogen sulfide donors: therapeutic potential in anti-atherosclerosis. Eur. J. Med. Chem. 205:112665
    [Google Scholar]
  101. 101. 
    Cheng Z, Kishore R. 2020. Potential role of hydrogen sulfide in diabetes-impaired angiogenesis and ischemic tissue repair. Redox Biol 37:101704
    [Google Scholar]
  102. 102. 
    Ngowi EE, Sarfraz M, Afzal A, Khan NH, Khattak S et al. 2020. Roles of hydrogen sulfide donors in common kidney diseases. Front. Pharmacol. 11:1706
    [Google Scholar]
  103. 103. 
    Ngowi EE, Afzal A, Sarfraz M, Khattak S, Zaman SU et al. 2021. Role of hydrogen sulfide donors in cancer development and progression. Int. J. Biol. Sci. 17:73–88
    [Google Scholar]
  104. 104. 
    San Martín A, Ceballo S, Baeza-Lehnert F, Lerchundi R, Valdebenito R et al. 2014. Imaging mitochondrial flux in single cells with a FRET sensor for pyruvate. PLOS ONE 9:1e85780
    [Google Scholar]
  105. 105. 
    Merhi A, Delree P, Marini AM. 2017. The metabolic waste ammonium regulates mTORC2 and mTORC1 signaling. Sci. Rep. 7:44602
    [Google Scholar]
  106. 106. 
    Skowrońska M, Albrecht J. 2013. Oxidative and nitrosative stress in ammonia neurotoxicity. Neurochem. Int. 62:5731–37
    [Google Scholar]
  107. 107. 
    Adeva-Andany M, López-Ojén M, Funcasta-Calderón R, Ameneiros-Rodríguez E, Donapetry-García C et al. 2014. Comprehensive review on lactate metabolism in human health. Mitochondrion 17:76–100
    [Google Scholar]
  108. 108. 
    Huang BK, Stein KT, Sikes HD. 2016. Modulating and measuring intracellular H2O2 using genetically encoded tools to study its toxicity to human cells. ACS Synth. Biol. 5:121389–95
    [Google Scholar]
  109. 109. 
    Shibuya N, Kimura H. 2013. Production of hydrogen sulfide from d-cysteine and its therapeutic potential. Front. Endocrinol. 4:87
    [Google Scholar]
  110. 110. 
    Kanagy NL, Szabo C, Papapetropoulos A. 2017. Vascular biology of hydrogen sulfide. Am. J. Physiol. Cell Physiol. 312:5C537–49
    [Google Scholar]
  111. 111. 
    Bełtowski J 2019. Synthesis, metabolism, and signaling mechanisms of hydrogen sulfide: an overview. Vascular Effects of Hydrogen Sulfide: Methods and Protocols J Bełtowski 1–8 New York: Humana
    [Google Scholar]
  112. 112. 
    Huang BK, Sikes HD. 2014. Quantifying intracellular hydrogen peroxide perturbations in terms of concentration. Redox Biol 2:1955–62
    [Google Scholar]
  113. 113. 
    Huang BK, Stein KT, Sikes HD. 2016. Modulating and measuring intracellular H2O2 using genetically encoded tools to study its toxicity to human cells. ACS Synth. Biol. 5:121389–95
    [Google Scholar]
  114. 114. 
    Stein KT, Moon SJ, Sikes HD. 2018. Mitochondrial H2O2 generation using a tunable chemogenetic tool to perturb redox homeostasis in human cells and induce cell death. ACS Synth. Biol. 7:92037–44
    [Google Scholar]
  115. 115. 
    Mishina NM, Bogdanova YA, Ermakova YG, Panova AS, Kotova DA et al. 2019. Which antioxidant system shapes intracellular H2O2 gradients?. Antioxid. Redox Signal. 31:9664–70
    [Google Scholar]
  116. 116. 
    Eroglu E, Saravi SSS, Sorrentino A, Steinhorn B, Michel T. 2019. Discordance between eNOS phosphorylation and activation revealed by multispectral imaging and chemogenetic methods. PNAS 116:4020210–17
    [Google Scholar]
  117. 117. 
    Samulski RJ, Muzyczka N. 2014. AAV-mediated gene therapy for research and therapeutic purposes. Annu. Rev. Virol. 1:427–51
    [Google Scholar]
  118. 118. 
    Grimm D, Lee JS, Wang L, Desai T, Akache B et al. 2008. In vitro and in vivo gene therapy vector evolution via multispecies interbreeding and retargeting of adeno-associated viruses. J. Virol. 82:125887–911
    [Google Scholar]
  119. 119. 
    Grimm M, Brown JH. 2010. β-Adrenergic receptor signaling in the heart: role of CaMKII. J. Mol. Cell. Cardiol. 48:2322–30
    [Google Scholar]
  120. 120. 
    Mattiazzi A, Mundiña-Weilenmann C, Guoxiang C, Vittone L, Kranias E. 2005. Role of phospholamban phosphorylation on Thr17 in cardiac physiological and pathological conditions. Cardiovasc. Res. 68:3366–75
    [Google Scholar]
  121. 121. 
    Sulakhe PV, Vo XT. 1995. Regulation of phospholamban and troponin-I phosphorylation in the intact rat cardiomyocytes by adrenergic and cholinergic stimuli: roles of cyclic nucleotides, calcium, protein kinases and phosphatases and depolarization. Mol. Cell. Biochem149–150–103–26
    [Google Scholar]
  122. 122. 
    McMurray JJV, Packer M, Desai AS, Gong J, Lefkowitz MP et al. 2014. Angiotensin-neprilysin inhibition versus enalapril in heart failure. N. Engl. J. Med. 371:11993–1004
    [Google Scholar]
  123. 123. 
    Kong Q, Lin CG. 2010. Oxidative damage to RNA: mechanisms, consequences, and diseases. Cell. Mol. Life Sci. 67:111817–29
    [Google Scholar]
  124. 124. 
    Ziaeian B, Fonarow GC. 2016. Epidemiology and aetiology of heart failure. Nat. Rev. Cardiol. 13:6368–78
    [Google Scholar]
  125. 125. 
    Lerman LO, Kurtz TW, Touyz RM, Ellison DH, Chade AR et al. 2019. Animal models of hypertension: a scientific statement from the American Heart Association. Hypertension 73:6e87–120
    [Google Scholar]
  126. 126. 
    Bugger H, Abel ED. 2009. Rodent models of diabetic cardiomyopathy. Dis. Model. Mech. 2:9–10454–66
    [Google Scholar]
/content/journals/10.1146/annurev-pharmtox-012221-082339
Loading
/content/journals/10.1146/annurev-pharmtox-012221-082339
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error