Dissociations in the Effects of β2-Adrenergic Receptor Agonists on cAMP Formation and Superoxide Production in Human Neutrophils: Support for the Concept of Functional Selectivity

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Brunskole Hummel, Irena ^a,b   Reinartz, Michael T ^a   Kälble, Solveig ^a   Burhenne, Heike ^a   Schwede, Frank ^c   Buschauer, Armin ^b   Seifert, Roland ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c BIOLOG Life Science Institute   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENALIN; BETA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYTOCHROME C; DICHLORISOPRENALINE; DOBUTAMINE; EPHEDRINE; FORMYLMETHIONYLLEUCYLPHENYLALANINE; ISOPRENALINE; OXYGEN; SALBUTAMOL; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ARTICLE; CONTROLLED STUDY; DISSOCIATION; DRUG EFFICACY; DRUG POTENCY; DRUG SELECTIVITY; ENZYME INHIBITION; GENETIC MANIPULATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; LIGAND BINDING; NEUTROPHIL; PROTEIN CONFORMATION; PROTEIN SYNTHESIS; RECEPTOR POTENTIAL; RECOMBINANT DNA TECHNOLOGY; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

ADRENERGIC AGONISTS; ALBUTEROL; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EPHEDRINE; EPINEPHRINE; FEMALE; HUMANS; ISOPROTERENOL; KINETICS; MALE; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NEUTROPHILS; PRIMARY CELL CULTURE; PROTEIN CONFORMATION; RECEPTORS, ADRENERGIC, BETA-2; SIGNAL TRANSDUCTION; SUPEROXIDES;

EID: 84878573306     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064556     Document Type: Article

References (84)

1. Selvatici R, Falzarano S, Mollica A, Spisani S, (2006) Signal transduction pathways triggered by selective formylpeptide analogues in human neutrophils. Eur J Pharmacol 534: 1-11.
2. Seifert R, Schultz G, (1991) The superoxide-forming NADPH oxidase of phagocytes. An enzyme system regulated by multiple mechanisms. Rev Physiol Biochem Pharmacol 117: 1-338.
3. Morel F, Doussiere J, Vignais PV, (1991) The superoxide-generating oxidase of phagocytic cells. Physiological, molecular and pathological aspects. Eur J Biochem 201: 523-546.
4. El-Benna J, Dang PM, Perianin A, (2010) Peptide-based inhibitors of the phagocyte NADPH oxidase. Biochem Pharmacol 80: 778-785.
5. Arruda MA, Barja-Fidalgo C, (2009) NADPH oxidase activity: In the crossroad of neutrophil life and death. Front Biosci 14: 4546-4556.
6. Burde R, Seifert R, Buschauer A, Schultz G, (1989) Histamine inhibits activation of human neutrophils and HL-60 leukemic cells via H2 receptors. Naunyn-Schmiedeberg's Arch Pharmacol 340: 671-678.
7. Gierschik P, Sidiropoulos D, Jakobs KH, (1989) Two distinct Gi proteins mediate formyl peptide receptor signal transduction in human leukemia (HL-60) cells. J Biol Chem 264: 21470-21473.
8. Wenzel-Seifert K, Arthur JM, Liu HY, Seifert R, (1999) Quantitative analysis of formyl peptide receptor coupling to Gαi1, Gαi2, and Gαi3. J Biol Chem 274: 33259-33266.
9. Wenzel-Seifert K, Ervens J, Seifert R, (1991) Differential inhibition and potentiation by cell-permeant analogues of cyclic AMP and cyclic GMP and NO-containing compounds of exocytosis in human neutrophils. Naunyn Schmiedebergs Arch Pharmacol 344: 396-402.
10. Mirza ZN, Kato M, Kimura H, Tachibana A, Fujiu T, et al. (2002) Fenoterol inhibits superoxide anion generation by human polymorphonuclear leukocytes via β-adrenoceptor-dependent and-independent mechanisms. Ann Allergy Asthma Immunol 88: 494-500.
11. Mitsuyama T, Takeshige K, Furuno T, Tanaka T, Hidaka K, et al. (1995) An inhibitor of cyclic AMP-dependent protein kinase enhances the superoxide production of human neutrophils stimulated by N-formyl-methionyl-leucyl-phenylalanine. Mol Cell Biochem 145: 19-24.
12. Mueller H, Motulsky HJ, Sklar LA, (1988) The potency and kinetics of the β-adrenergic receptors on human neutrophils. Mol Pharmacol 34: 347-353.
13. Wong K, Freund K, (1981) Inhibition of the N-formylmethionyl-leucyl-phenylalanine induced respiratory burst in human neutrophils by adrenergic agonists and prostaglandins of the E series. Can J Physiol Pharmacol 59: 915-920.
14. Lad PM, Goldberg BJ, Smiley PA, Olson CV, (1985) Receptor-specific threshold effects of cyclic AMP are involved in the regulation of enzyme release and superoxide production from human neutrophils. Biochim Biophys Acta 846: 286-295.
15. Wenzel-Seifert K, Seifert R, (2000) Molecular analysis of β2-adrenoceptor coupling to Gs, Gi, and Gq proteins. Mol Pharmacol 58: 954-966.
16. Evans BA, Sato M, Sarwar M, Hutchinson DS, Summers RJ, (2010) Ligand-directed signalling at β-adrenoceptors. Br J Pharmacol 159: 1022-1038.
17. Drake MT, Violin JD, Whalen EJ, Wisler JW, Shenoy SK, et al. (2008) β-Arrestin-biased agonism at the β2-adrenergic receptor. J Biol Chem 283: 5669-5676.
18. Audet M, Bouvier M, (2008) Insights into signaling from the β2-adrenergic receptor structure. Nat Chem Biol 4: 397-403.
19. Rosenbaum DM, Rasmussen SG, Kobilka BK, (2009) The structure and function of G-protein-coupled receptors. Nature 459: 356-363.
20. Seifert R, Wenzel-Seifert K, (2002) Constitutive activity of G protein-coupled receptors: cause of disease and common property of wild-type receptors. Naunyn Schmiedebergs Arch Pharmacol 366: 381-416.
21. Neubig RR, Spedding M, Kenakin T, Christopoulos A, (2003) International Union of Pharmacology Committee on Receptor Nomenclature and Drug Classification. XXXVIII. Update on terms and symbols in quantitative pharmacology. Pharmacol Rev 55: 597-606.
22. Kenakin T, (2004) Principles: receptor theory in pharmacology. Trends Pharmacol Sci 25: 186-192.
23. Gether U, Lin S, Kobilka BK, (1995) Fluorescent labeling of purified β2-adrenergic receptor. Evidence for ligand-specific conformational changes. J Biol Chem 270: 28268-28275.
24. Seifert R, Gether U, Wenzel-Seifert K, Kobilka BK, (1999) Effects of guanine, inosine, and xanthine nucleotides on β2-adrenergic receptor/Gs interactions: evidence for multiple receptor conformations. Mol Pharmacol 56: 348-358.
25. Sternini C, Spann M, Anton B, Keith DE Jr, Bunnett NW, et al. (1996) Agonist-selective endocytosis of μ opioid receptor by neurons in vivo. Proc Natl Acad Sci USA 93: 9241-9246.
26. Galandrin S, Bouvier M, (2006) Distinct signaling profiles of β1- and β2-adrenergic receptor ligands toward adenylyl cyclase and mitogen-activated protein kinase reveals the pluridimensionality of efficacy. Mol Pharmacol 70: 1575-1584.
27. Rajagopal S, Rajagopal K, Lefkowitz RJ, (2010) Teaching old receptors new tricks: biasing seven-transmembrane receptors. Nat Rev Drug Discov 9: 373-386.
28. Kobilka BK, Deupi X, (2007) Conformational complexity of G protein-coupled receptors. Trends Pharmacol Sci 28: 397-406.
29. Kenakin T, (1995) Agonist-receptor efficacy. II. Agonist trafficking of receptor signals. Trends Pharmacol Sci 16: 232-238.
30. Tucek S, (1997) Is the R and R dichotomy real? Trends Pharmacol Sci 18: 414-416.
31. Liu JJ, Horst R, Katritch V, Stevens RC, Wüthrich K, (2012) Biased signaling pathways in β2-adrenergic receptor characterized by 19F-NMR. Science 335: 1106-1110.
32. Galandrin S, Oligny-Longpré G, Bouvier M, (2007) The evasive nature of drug efficacy: implications for drug discovery. Trends Pharmacol Sci 28: 423-430.
33. Kenakin T, Miller LJ, (2010) Seven transmembrane receptors as shapeshifting proteins: the impact of allosteric modulation and functional selectivity on new drug discovery. Pharmacol Rev 62: 265-304.
34. Rosethorne EM, Charlton SJ, (2011) Agonist-biased signaling at the histamine H4 receptor: JNJ7777120 recruits β-arrestin without activating G proteins. Mol Pharmacol 79: 749-757.
35. Azzi M, Charest PG, Angers S, Rousseau G, Kohout T, et al. (2003) β-arrestin-mediated activation of MAPK by inverse agonists reveals distinct active conformations for G protein-coupled receptors. Proc Natl Acad Sci USA 100: 11406-11411.
36. Thomas RL, Mistry R, Langmead CJ, Wood MD, Challiss RA, (2008) G protein coupling and signaling pathway activation by M1 muscarinic acetylcholine receptor orthosteric and allosteric agonists. J Pharmacol Exp Ther 327: 365-374.
37. Swaminath G, Deupi X, Lee TW, Zhu W, Thian FS, et al. (2005) Probing the β2-adrenoceptor binding site with catechol reveals differences in binding and activation by agonists and partial agonists. J Biol Chem 280: 22165-22171.
38. Kahsai AW, Xiao K, Rajagopal S, Ahn S, Shukla AK, et al. (2011) Multiple ligand-specific conformations of the β2-adrenergic receptor. Nat Chem Biol 7: 692-700.
39. Granier S, Kim S, Shafer AM, Ratnala VR, Fung JJ, et al. (2007) Structure and conformational changes in the C-terminal domain of the β2-adrenoceptor: insights from fluorescence resonance energy transfer studies. J Biol Chem 282: 13895-13905.
40. Reher TM, Brunskole I, Neumann D, Seifert R, (2012) Evidence for ligand-specific conformations of the histamine H2-receptor in human eosinophils and neutrophils. Biochem Pharmacol 84: 1175-1185.
41. Beste KY, Burhenne H, Kaever V, Stasch JP, Seifert R, (2012) Nucleotidyl cyclase activity of soluble guanylyl cyclase α1β1. Biochemistry 51: 194-204.
42. Kinast L, von der Ohe J, Burhenne H, Seifert R, (2012) Impairment of adenylyl cyclase 2 function and expression in hypoxanthine phosphoribosyltransferase-deficient rat B103 neuroblastoma cells as model for Lesch-Nyhan disease: BODIPY-forskolin as pharmacological tool. Naunyn Schmiedebergs Arch Pharmacol 385: 671-683.
43. Weitl N, Seifert R, (2008) Distinct interactions of human β1- and β2-adrenoceptors with isoproterenol, epinephrine, norepinephrine, and dopamine. J Pharmacol Exp Ther 327: 760-769.
44. Cheng Y, Prusoff WH, (1973) Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem Pharmacol 22: 3099-3108.
45. Seifert R, Wenzel-Seifert K, Lee TW, Gether U, Sanders-Bush E, et al. (1998) Different effects of Gsα splice variants on β2-adrenoreceptor-mediated signaling. The β2-adrenoreceptor coupled to the long splice variant of Gsα has properties of a constitutively active receptor. J Biol Chem 273: 5109-5116.
46. Seifert R, Hilgenstock G, Fassbender M, Distler A, (1991) Regulation of the superoxide-forming NADPH oxidase of human neutrophils is not altered in essential hypertension. J Hypertens 9: 147-153.
47. Hill SJ, (2006) G protein-coupled receptors: past, present and future. Br J Pharmacol 147Suppl 1: S27-37.
48. Baker JG, Hall IP, Hill SJ, (2003) Influence of agonist efficacy and receptor phosphorylation on antagonist affinity measurements: differences between second messenger and reporter gene responses. Mol Pharmacol 64: 679-688.
49. Appl H, Holzammer T, Dove S, Haen E, Strasser A, et al. (2011) Interactions of recombinant human histamine H1, H2, H3 and H4 receptors with 34 antidepressants and antipsychotics. Naunyn Schmiedebergs Arch Pharmacol 385: 145-170.
50. Gibson-Berry KL, Whitin JC, Cohen HJ, (1993) Modulation of the respiratory burst in human neutrophils by isoproterenol and dibutyryl cyclic AMP. J Neuroimmunol 43: 59-68.
51. Barnett CC Jr, Moore EE, Partrick DA, Silliman CC, (1997) Beta-adrenergic stimulation down-regulates neutrophil priming for superoxide generation, but not elastase release. J Surg Res 70: 166-170.
52. Hidaka H, Inagaki M, Kawamoto S, Sasaki Y, (1984) Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry. 23: 5036-5041.
53. Rothermel JD, Jastorff B, Botelho LH, (1984) Inhibition of glucagon-induced glycogenolysis in isolated rat hepatocytes by the Rp diastereomer of adenosine cyclic 3′,5′-phosphorothioate. J Biol Chem 259: 8151-8155.
54. Lazarovici P, Rasouly D, Friedman L, Tabekman R, Ovadia H, et al. (1996) K252a and staurosporine microbial alkaloid toxins as prototype of neurotropic drugs. Adv Exp Med Biol 391: 367-377.
55. Uemura T, Ohta Y, Nakao Y, Manaka T, Nakamura H, et al. (2010) Epinephrine accelerates osteoblastic differentiation by enhancing bone morphogenetic protein signaling through a cAMP/protein kinase A signaling pathway. Bone 47: 756-765.
56. Kellenberger S, Muller K, Richener H, Bilbe G, (1998) Formoterol and isoproterenol induce c-fos gene expression in osteoblast-like cells by activating β2-adrenergic receptors. Bone 22: 471-478.
57. Hoogland TM, Saggau P, (2004) Facilitation of L-type Ca2+ channels in dendritic spines by activation of β2 adrenergic receptors. J Neurosci 24: 8416-8427.
58. Madden KS, Szpunar MJ, Brown EB, (2011) β-Adrenergic receptors (β-AR) regulate VEGF and IL-6 production by divergent pathways in high β-AR-expressing breast cancer cell lines. Breast Cancer Res Treat 130: 747-758.
59. Dostmann WRG, Taylor SS, Genieser HG, Jastorff B, Døskeland SO, et al. (1990) Probing cyclic nucleotide binding sites of cAMP-dependent protein kinase I and II with analogs of adenosine 3′,5′-cyclic phosphorothioates. J Biol Chem 265: 10484-10491.
60. Hourani SM, Boon K, Fooks HM, Prentice DJ, (2001) Role of cyclic nucleotides in vasodilations of the rat thoracic aorta induced by adenosine analogues. Br J Pharmacol 2001 133: 833-40.
61. Seifert R, Lushington GH, Mou TC, Gille A, Sprang SR, (2012) Inhibitors of membranous adenylyl cyclases. Trends Pharmacol Sci 33: 64-78.
62. Kaukel E, Mundhenk K, Hilz H, (1972) N6-monobutyryladenosine 3′:5′-monophosphate is the biologically active derivative of dibutyryladenosine 3′:5′-monophosphate in HeLa S3 cells. Eur J Biochem 27: 197-200.
63. Jackson EK, Raghvendra DK, (2004) The extracellular cyclic AMP-adenosine pathway in renal physiology. Annu Rev Physiol 66: 571-599.
64. Russel FG, Koenderink JB, Masereeuw R, (2008) Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol Sci 29: 200-207.
65. Gloerich M, Bos JL, (2010) Epac: defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol 50: 355-375.
66. Seifert R, Dove S, (2009) Functional selectivity of GPCR ligand stereoisomers: new pharmacological opportunities. Mol Pharmacol 75: 13-18.
67. Mukhopadhyay S, Howlett AC, (2005) Chemically distinct ligands promote differential CB1 cannabinoid receptor-Gi protein interactions. Mol Pharmacol 67: 2016-2024.
68. Reher TM, Neumann D, Buschauer A, Seifert R, (2012) Incomplete activation of human eosinophils via the histamine H4-receptor: Evidence for ligand-specific receptor conformations. Biochem Pharmacol 84: 192-203.
69. Woo AY, Wang TB, Zeng X, Zhu W, Abernethy DR, et al. (2009) Stereochemistry of an agonist determines coupling preference of β2-adrenoceptor to different G proteins in cardiomyocytes. Mol Pharmacol 75: 158-165.
70. Carbonetti NH, (2010) Pertussis toxin and adenylate cyclase toxin: key virulence factors of Bordetella pertussis and cell biology tools. Future Microbiol 5: 455-469.
71. Orlic T, Loomis WH, Shreve A, Namiki S, Junger WG, (2002) Hypertonicity increases cAMP in PMN and blocks oxidative burst by PKA-dependent and-independent mechanisms. Am J Physiol Cell Physiol 282: C1261-C1269.
72. Sedgwick JB, Berube ML, Zurier RB, (1985) Stimulus-dependent inhibition of superoxide generation by prostaglandins. Clin Immunol Immunopathol 34: 205-215.
73. Cronstein BN, Kramer SB, Rosenstein ED, Korchak HM, Weissmann G, et al. (1988) Occupancy of adenosine receptors raises cyclic AMP alone and in synergy with occupancy of chemoattractant receptors and inhibits membrane depolarization. Biochem J 252: 709-715.
74. Costantini TW, Deree J, Peterson CY, Putnam JG, Woon T, et al. (2010) Pentoxifylline modulates p47phox activation and downregulates neutrophil oxidative burst through PKA-dependent and-independent mechanisms. Immunopharmacol Immunotoxicol 32: 82-91.
75. Costa T, Klinz FJ, Vachon L, Herz A, (1988) Opioid receptors are coupled tightly to G proteins but loosely to adenylate cyclase in NG108-15 cell membranes. Mol Pharmacol 34: 744-7454.
76. Werner K, Schwede F, Genieser HG, Geiger J, Butt E, (2011) Quantification of cAMP and cGMP analogs in intact cells: pitfalls in enzyme immunoassays for cyclic nucleotides. Naunyn Schmiedebergs Arch Pharmacol 384: 169-176.
77. Brodde OE, Michel MC, (1995) Adrenergic and muscarinic receptors in the human heart. Pharmacol Rev 51: 651-690.
78. Stallaert W, Dorn JF, van der Westhuizen E, Audet M, Bouvier M, (2012) Impedance responses reveal β2-adrenergic receptor signaling pluridimensionality and allow classification of ligands with distinct signaling profiles. PLoS One 7: e29420.
79. Liao CH, Lin SZ, Tseng CP, Day YJ, Chang CS, et al. (2008) A benzodiazepines derived compound, 4-(3-chlorophenyl)-1,3-dihydronaphtho 2,3-b]1,4]diazepin-2-one (ND700C), inhibits fMLP-induced superoxide anion release by activating protein phosphatase 2A in human neutrophils. Biochem Pharmacol 76: 1728-1739.
80. Liu FC, Day YJ, Liou JT, Yu HP, Liao HR, (2012) Splitomicin inhibits fMLP-induced superoxide anion production in human neutrophils by activate cAMP/PKA signaling inhibition of ERK pathway. Eur J Pharmacol 688: 68-75.
81. Kaya AI, Onaran HO, Ozcan G, Ambrosio C, Costa T, et al. (2012) Cell contact-dependent functional selectivity of β2-adrenergic receptor ligands in stimulating cAMP accumulation and extracellular signal-regulated kinase phosphorylation. J Biol Chem 287: 6362-6374.
82. Beste KY, Seifert R, (2013) cCMP, cUMP, cTMP, cIMP and cXMP as possible second messengers: development of a hypothesis based on studies with soluble guanylyl cyclase α1β1. Biol Chem 394: 261-270.
83. Uzkeser H, Cadirci E, Halici Z, Odabasoglu F, Polat B, et al. (2012) Anti-inflammatory and antinociceptive effects of salbutamol on acute and chronic models of inflammation in rats: involvement of an antioxidant mechanism. Mediators Inflamm 2012: 438912.
84. Sun Y, Huang J, Xiang Y, Bastepe M, Juppner H, et al. (2007) Dosage-dependent switch from G protein-coupled to G protein-independent signaling by a GPCR. EMBO J 26: 53-64.