Abstract
Cyclic 3′,5′-guanylyl and adenylyl nucleotides function as second messengers in eukaryotic signal transduction pathways and as sensory transducers in prokaryotes. The nucleotidyl cyclases (NCs) that catalyze the synthesis of these molecules comprise several evolutionarily distinct groups, of which class III is the largest. The domain structures of prokaryotic and eukaryotic class III NCs are diverse, including a variety of regulatory and transmembrane modules. Yet all members of this family contain one or two catalytic domains, characterized by an evolutionarily ancient topological motif (βααββαβ) that is preserved in several other enzymes that catalyze the nucleophilic attack of a 3′-hydroxyl upon a 5′ nucleotide phosphate. Two dyad-related catalytic domains compose one catalytic unit, with the catalytic sites formed at the domain interface. The catalytic domains of mononucleotidyl cyclases (MNCs) and diguanylate cyclases (DGCs) are called cyclase homology domains (CHDs) and GGDEF domains, respectively. Prokaryotic NCs usually contain only one catalytic domain and are catalytically active as intermolecular homodimers. The different modes of dimerization in class III NCs probably evolved concurrently with their mode of binding substrate. The catalytic mechanism of GGDEF domain homodimers is not completely understood, but they are expected to have a single active site with each subunit contributing equivalent determinants to bind one GTP molecule or half a c-diGMP molecule. CHD dimers have two potential dyad-related active sites, with both CHDs contributing determinants to each site. Homodimeric class III MNCs have two equivalent catalytic sites, although such enzymes may show half-of-sites reactivity. Eukaryotic class III MNCs often contain two divergent CHDs, with only one catalytically competent site. All CHDs appear to use a common catalytic mechanism, which requires the participation of two magnesium or manganese ions for binding polyphosphate groups and nucleophile activation. In contrast, mechanisms for purine recognition and specificity are more diverse. Class III NCs are subject to regulation by small molecule effectors, endogenous domains, or exogenous protein partners. Many of these regulators act by altering the interface of the catalytic domains and therefore the integrity of the catalytic site(s). This review focuses on both conserved and divergent mechanisms of class III NC function and regulation.
References
Artymiuk PJ, Poirette AR, Rice DW, Willett P (1997) A polymerase I palm in adenylyl cyclase? Nature 388:33–34
Barton GJ (1993) ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng 6:37–40
Barzu O, Danchin A (1994) Adenylyl cyclases: a heterogeneous class of ATP-utilizing enzymes. Prog Nucleic Acid Res Mol Biol 49:241–283
Beese LS, Steitz TA (1991) Structural basis for the 3′-5′ exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism. EMBO J 10:25–33
Beuve A (1999) Conversion of a guanylyl cyclase to an adenylyl cyclase. Methods 19:545–550
Beuve A, Krin E, Danchin A (1993) Rhizobium meliloti adenylate cyclase: probing of a NTP-binding site common to cyclases and cation transporters. C R Acad Sci III 316:533–539
Bieger B, Essen LO (2001) Structural analysis of adenylate cyclases from Trypanosoma brucei in their monomeric state. EMBO J 20:433–445
Brautigam CA, Steitz TA (1998) Structural and functional insights provided by crystal structures of DNA polymerases and their substrate complexes. Curr Opin Struct Biol 8:54–63
Buck J, Sinclair ML, Schapal L, Cann MJ, Levin LR (1999) Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc Natl Acad Sci USA 96:79–84
Cann MJ, Hammer A, Zhou J, Kanacher T (2003) A defined subset of adenylyl cyclases is regulated by bicarbonate ion. J Biol Chem 278:35033–35038
Chan C, Paul R, Samoray D, Amiot NC, Giese B, Jenal U, Schirmer T (2004) Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci USA 101:17084–17089
Chen Y, Weng G, Li J, Harry A, Pieroni J, Dingus J, Hildebrandt JD, Guarnieri F, Weinstein H, Iyengar R (1997) A surface on the G protein beta-subunit involved in interactions with adenylyl cyclases. Proc Natl Acad Sci USA 94:2711–2714
Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J (2000) Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289:625–628
Cooper D (2005) Compartmentalization of adenylate cyclase and cAMP signalling. Biochem Soc Trans 33:1319–1322
Cooper DM, Mons N, Fagan K (1994) Ca(2+)-sensitive adenylyl cyclases. Cell Signal 6:823–840
Cooper DM, Mons N, Karpen JW (1995) Adenylyl cyclases and the interaction between calcium and cAMP signalling. Nature 374:421–424
Cooper DM, Schell MJ, Thorn P, Irvine RF (1998) Regulation of adenylyl cyclase by membrane potential. J Biol Chem 273:27703–27707
Cooper DMF (2003) Regulation and organization of adenylyl cyclases and cAMP. Biochem J 375:517–529
Cotta M, Whitehead T, Wheeler M (1998) Identification of a novel adenylate cyclase in the ruminal anaerobe, Prevotella ruminicola D31d. FEMS Microbiol Lett 164:257–260
Coudart-Cavalli MP, Sismeiro O, Danchin A (1997) Bifunctional structure of two adenylyl cyclases from the myxobacterium Stigmatella aurantiaca. Biochimie 79:757–767
Dessauer CW, Gilman AG (1997) The catalytic mechanism of mammalian adenylyl cyclase. Equilibrium binding and kinetic analysis of P-site inhibition. J Biol Chem 272:27787–27795
Dessauer CW, Scully TT, Gilman AG (1997) Interactions of forskolin and ATP with the cytosolic domains of mammalian adenylyl cyclase. J Biol Chem 272:22272–22277
Dessauer CW, Tesmer JJ, Sprang SR, Gilman AG (1998) Identification of a Gia binding site on type V adenylyl cyclase. J Biol Chem 273:25831–25839
Dessauer CW, Tesmer JJ, Sprang SR, Gilman AG (1999) The interactions of adenylate cyclases with P-site inhibitors. Trends Pharmacol Sci 20:205–210
Doublié S, Ellenberger T (1998) The mechanism of action of T7 DNA polymerase. Curr Opin Struct Biol 8:704–712
Drum CL, Yan SZ, Bard J, Shen YQ, Lu D, Soelaiman S, Grabarek Z, Bohm A, Tang WJ (2002) Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415:396–402
Eckstein F, Romaniuk PJ, Heideman W, Storm DR (1981) Stereochemistry of the mammalian adenylate cyclase reaction. J Biol Chem 256:9118–9120
Feng Q, Zhang Y, Li Y, Liu Z, Zuo J, Fang F (2005) Two domains are critical for the nuclear localization of soluble adenylyl cyclase. Biochimie 88:319–328
Gallagher DT, Smith NN, Kim SK, Heroux A, Robinson H, Reddy PT (2006) Structure of the Class IV Adenylyl Cyclase Reveals a Novel Fold. J Mol Biol. 2006 Aug 11; [Epub ahead of print]
Geng W, Wang Z, Zhang J, Reed BY, Pak CYC, Moe OW (2005) Cloning and characterization of the human soluble adenylyl cyclase. Am J Physiol Cell Physiol 288:C1305–1316
Gu C, Cali JJ, Cooper DM (2002) Dimerization of mammalian adenylate cyclases. Eur J Biochem 269:413–421
Guo Q, Shen Y, Zhukovskaya NL, Florian J, Tang WJ (2004) Structural and kinetic analyses of the interaction of anthrax adenylyl cyclase toxin with reaction products cAMP and pyrophosphate. J Biol Chem 279:29427–29435
Guo Q, Shen Y, Lee YS, Gibbs CS, Mrksich M, Tang WJ (2005) Structural basis for the interaction of Bordetella pertussis adenylyl cyclase toxin with calmodulin. EMBO J 24:3190–3201
Guo YL, Seebacher T, Kurz U, Linder JU, Schultz JE (2001) Adenylyl cyclase Rv1625c of Mycobacterium tuberculosis: a progenitor of mammalian adenylyl cyclases. EMBO J 20:3667–3675
Hanoune J, Defer N (2001) Regulation and role of adenylyl cyclase isoforms. Annu Rev Pharmacol Toxicol 41:145–174
Holland MM, Leib TK, Gerlt JA (1988) Isolation and characterization of a small catalytic domain released from the adenylate cyclase from Escherichia coli by digestion with trypsin. J Biol Chem 263:14661–14668
Hu B, Nakata H, Gu C, De Beer T, Cooper DM (2002) A critical interplay between Ca2+ inhibition and activation by Mg2+ of AC5 revealed by mutants and chimeric constructs. J Biol Chem 277:33139–33147
Hurley J (1998) The adenylyl and guanylyl cyclase superfamily. Curr Opin Struct Biol 8:770–777
Hurley JH (1999) Structure, mechanism, and regulation of mammalian adenylyl cyclase. J Biol Chem 274:7599–7602
Hyne RV, Garbers DL (1979) Regulation of guinea pig sperm adenylate cyclase by calcium. Biol Reprod 21:1135–1142
Jaiswal BS, Conti M (2001) Identification and functional analysis of splice variants of the germ cell soluble adenylyl cyclase. J Biol Chem 276:31698–31708
Jaiswal BS, Conti M (2003) Calcium regulation of the soluble adenylyl cyclase expressed in mammalian spermatozoa. Proc Natl Acad Sci USA 100:10676–10681
Kasahara M, Unno T, Yashiro K, Ohmori M (2001) CyaG, a novel cyanobacterial adenylyl cyclase and a possible ancestor of mammalian guanylyl cyclases. J Biol Chem 276:10564–10569
Ketkar A, Shenoya A, Ramagopal UA, Visweswariaha SS, Sugun K (2006) A structural basis for the role of nucleotide specifying residues in regulating the oligomerization of the Rv1625c adenylyl cyclase from M. tuberculosis. J Mol Biol 356:904–916
Ketkar AD, Shenoy AR, Kesavulu MM, Visweswariah SS, Suguna K (2004) Purification, crystallization and preliminary X-ray diffraction analysis of the catalytic domain of adenylyl cyclase Rv1625c from Mycobacterium tuberculosis. Acta Crystallogr D Biol Crystallogr 60:371–373
Kimura Y, Vassylyev DG, Matsushima M, Mitsuoka K, Murata K, Hiral T, Fujiyoshi Y (1997) Surface of bacteriorhodopsin revealed by high-resolution electron crystallography. Nature 389:206–211
Krupinski J, Cali JJ (1998) Molecular diversity of the adenylyl cyclases. Adv Second Messenger Phosphoprotein Res 32:53–79
Ladant D, Ullmann A (1999) Bordetella pertussis adenylate cyclase: a toxin with multiple talents. Trends Microbiol 7:172–176
Leppla SH (1982) Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc Natl Acad Sci USA 79:3162–3166
Linder JU (2005) Substrate selection by class III adenylyl cyclases and guanylyl cyclases. IUBMB Life 57:797–803
Linder JU, Schultz JE (2003) The class III adenylyl cyclases: multi-purpose signalling modules. Cell Signal 15:1081–1089
Linder JU, Engel P, Reimer A, Kruger T, Plattner H, Schultz A, Schultz JE (1999) Guanylyl cyclases with the topology of mammalian adenylyl cyclases and an N-terminal P-type ATPase-like domain in Paramecium, Tetrahymena and Plasmodium. EMBO J 18:4222–4232
Linder JU, Hoffmann T, Kurz U, Schultz JE (2000) A guanylyl cyclase from Paramecium with 22 transmembrane spans. Expression of the catalytic domains and formation of chimeras with the catalytic domains of mammalian adenylyl cyclases. J Biol Chem 275:11235–11240
Linder JU, Schultz A, Schultz JE (2002) Adenylyl cyclase Rv1264 from Mycobacterium tuberculosis has an autoinhibitory N-terminal domain. J Biol Chem 277:15271–15276
Linder JU, Hammer A, Schultz JE (2004) The effect of HAMP domains on class IIIb adenylyl cyclases from Mycobacterium tuberculosis. Eur J Biochem 271:2446–2451
Litvin NT, Kamenetsky M, Zarifyan A, Buck J, Levin LR (2003) Kinetic properties of “soluble” adenylyl cyclase. Synergism between calcium and bicarbonate. J Biol Chem 278:15922–15926
Liu Y, Ruoho AE, Rao VD, Hurley JH (1997) Catalytic mechanism of the adenylyl and guanylyl cyclases: modeling and mutational analysis. Proc Natl Acad Sci USA 94:13414–13419
Masuda S, Ono TA (2005) Adenylyl cyclase activity of Cya1 from the cyanobacterium Synechocystis sp. strain PCC 6803 is inhibited by bicarbonate. J Bacteriol 187:5032–5035
McCue LA, McDonough KA, Lawrence CE (2000) Functional classification of cNMP-binding proteins and nucleotide cyclases with implications for novel regulatory pathways in Mycobacterium tuberculosis. Genome Res 10:204–219
Mons N, Decorte L, Jaffard R, Cooper DM (1998) Ca2+-sensitive adenylyl cyclases, key integrators of cellular signalling. Life Sci 62:1647–1652
Mou TC, Gille A, Fancy DA, Seifert R, Sprang SR (2005) Structural basis for the inhibition of mammalian membrane adenylyl cyclase by 2 ′(3′)-O-(N-methylanthraniloyl)-guanosine 5′-triphosphate. J Biol Chem 280:7253–7261
Murzin AG (1998) How far divergent evolution goes in proteins. Curr Opin Struct Biol 8:380–387
Noyama K, Maekawa S (2003) Localization of cyclic nucleotide phosphodiesterase 2 in the brain-derived Triton-insoluble low-density fraction (raft). Neurosci Res 45:141–148
Ochoa de Alda JAG, Ajlani G, Houmard J (2000) Synechocystis strain PCC 6803 cya2, a prokaryotic gene that encodes a guanylyl cyclase. J Bacteriol 182:3839–3842
Pei J, Grishin N (2001) GGDEF domain is homologous to adenylyl cyclase. Proteins 42:210–216
Reddy P, Hoskins J, McKenney K (1995a) Mapping domains in proteins: dissection and expression of Escherichia coli adenylyl cyclase. Anal Biochem 231:282–286
Reddy R, Smith D, Wayman G, Wu Z, Villacres EC, Storm DR (1995b) Voltage-sensitive adenylyl cyclase activity in cultured neurons. A calcium-independent phenomenon. J Biol Chem 270:14340–14346
Roelofs J, Van Haastert PJM (2002) Deducing the origin of soluble adenylyl cyclase, a gene lost in multiple lineages. Mol Biol Evol 19:2239–2246
Romling U, Gomelsky M, Galperin MY (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57:629–639
Scholich K, Barbier AJ, Mullenix JB, Patel TB (1997a) Characterization of soluble forms of nonchimeric type V adenylyl cyclase. Proc Natl Acad Sci USA 94:2915–2920
Scholich K, Wittpoth C, Barbier AJ, Mullenix JB, Patel TB (1997b) Identification of an intramolecular interaction between small regions in type V adenylyl cyclase that influences stimulation of enzyme activity by Gsalpha. Proc Natl Acad Sci USA 94:9602–9607
Seebacher T, Linder JU, Schultz JE (2001) An isoform-specific interaction of the membrane anchors affects mammalian adenylyl cyclase type V activity. Eur J Biochem 268:105–110
Shen Y, Zhukovskaya NL, Guo Q, Florián J, Tang WJ (2005) Calcium-independent calmodulin binding and two-metal-ion catalytic mechanism of anthrax edema factor. EMBO J 24:929–941
Shenoy A, Visweswariah S (2004) Class III nucleotide cyclases in bacteria and archaebacteria: lineage-specific expansion of adenylyl cyclases and a dearth of guanylyl cyclases. FEBS Lett 561:11–21
Shenoy AR, Srinivasan N, Subramaniam M, Visweswariah SS (2003) Mutational analysis of the Mycobacterium tuberculosis Rv1625c adenylyl cyclase: residues that confer nucleotide specificity contribute to dimerization. FEBS Lett 545:253–259
Shenoy AR, Sreenath NP, Mahalingam M, Visweswariah SS (2005) Characterization of phylogenetically distant members of the adenylate cyclase family from mycobacteria: Rv1647 from Mycobacterium tuberculosis and its orthologue ML1399 from M. leprae. Biochem J 387:541–551
Simonds WF (1999) G protein regulation of adenylate cyclase. Trends Pharmacol Sci 20:66–73
Sinha SC, Wetterer M, Sprang SR, Schultz JE, Linder JU (2005) Origin of asymmetry in adenylyl cyclases: structures of Mycobacterium tuberculosis Rv1900c. EMBO J 24:663–673
Sismeiro O, Trotot P, Biville F, Vivares C, Danchin A (1998) Aeromonas hydrophila adenylyl cyclase2: a new class of adenylyl cyclases with thermophilic properties and sequence similarities to proteins from hyperthermophilic archaebacteria. J Bacteriol 180:3339–3344
Smit MJ, Iyengar R (1998) Mammalian adenylyl cyclases. Adv Second Messenger Phosphoprotein Res 32:1–21
Steegborn C, Litvin TN, Hess KC, Capper AB, Taussig R, Buck J, Levin LR, Wu H (2005a) A novel mechanism for adenylyl cyclase inhibition from the crystal structure of its complex with catechol estrogen. J Biol Chem 280:31754–31759
Steegborn C, Litvin TN, Levin LR, Buck J, Wu H (2005b) Bicarbonate activation of adenylyl cyclase via promotion of catalytic active site closure and metal recruitment. Nat Struct Mol Biol 12:32–37
Steitz TA (1993) DNA- and RNA-dependent DNA polymerases. Curr Opin Struct Biol 3:31–38
Steitz TA (1999) DNA polymerases: structural diversity and common mechanisms. J Biol Chem 274:17395–17398
Steitz TA, Steitz JA (1993) A general two-metal-ion mechanism for catalytic RNA. Proc Natl Acad Sci USA 90:6498–6502
Steitz TA, Smerdon SJ, Jäger J, Joyce CM (1994) A unified polymerase mechanism for nonhomologous DNA and RNA polymerases. Science 266:2022–2025
Süsstrunk U, Pidoux J, Taubert S, Ullmann A, CJ T (1998) Pleiotropic effects of cAMP on germination, antibiotic biosynthesis and morphological development in Streptomyces coelicolor. Mol Microbiol 30:33–46
Sunahara RK, Taussig R (2002) Isoforms of mammalian adenylyl cyclase: multiplicities of signaling. Mol Interv 2:168–184
Sunahara RK, Dessauer CW, Gilman AG (1996) Complexity and diversity of mammalian adenylyl cyclases. Annu Rev Pharmacol Toxicol 36:461–480
Sunahara RK, Dessauer CW, Whisnant RE, Kleuss C, Gilman AG (1997) Interaction of Gsa with the cytosolic domains of mammalian adenylyl cyclase. J Biol Chem 272:22265–22271
Sunahara RK, Beuve A, Tesmer JJG, Sprang SR, Garbers DL, Gilman AG (1998) Exchange of substrate and inhibitor specificities between adenylyl and guanylyl cyclases. J Biol Chem 273:16332–16338
Tang WJ, Gilman AG (1995) Construction of a soluble adenylyl cyclase activated by Gs alpha and forskolin. Science 268:1769–1772
Tang WJ, Stanzel M, Gilman AG (1995) Truncation and alanine-scanning mutants of type I adenylyl cyclase. Biochemistry 34:14563–14572
Tang WJ, Yan S, Drum CL (1998) Class III adenylyl cyclases: regulation and underlying mechanisms. Adv Second Messenger Phosphoprotein Res 32:137–151
Taussig R, Zimmermann G (1998) Type-specific regulation of mammalian adenylyl cyclases by G protein pathways. Adv Second Messenger Phosphoprotein Res 32:81–98
Taussig R, Iniguez-Lluhi JA, Gilman AG (1993) Inhibition of adenylyl cyclase by Gi alpha. Science 261:218–221
Taussig R, Tang WJ, Hepler JR, Gilman AG (1994) Distinct patterns of bidirectional regulation of mammalian adenylyl cyclases. J Biol Chem 269:6093–6100
Tellez-Sosa J, Soberon N, Vega-Segura A, Torres-Marquez ME, Cevallos MA (2002) The rhizobium etli cyaC product: characterization of a novel adenylate cyclase class. J Bacteriol 184:3560–3568
Tesmer JJ, Sprang SR (1998) The structure, catalytic mechanism and regulation of adenylyl cyclase. Curr Opin Struct Biol 8:713–719
Tesmer JJ, Dessauer CW, Sunahara RK, Murray LD, Johnson RA, Gilman AG, Sprang SR (2000) Molecular basis for P-site inhibition of adenylyl cyclase. Biochemistry 39:14464–14471
Tesmer JJG, Sunahara RK, Gilman AG, Sprang SR (1997) Crystal structure of the catalytic domains of adenylyl cyclase in a complex with Gsa_GTPgS. Science 278:1907–1916
Tesmer JJG, Sunahara RK, Johnson RA, Gilman AG, Sprang SR (1999) Two metal ion catalysis in adenylyl cyclase. Science 285:756–760
Tews I, Findeisen F, Sinning I, Schultz A, Schultz JE, Linder JU (2005) The structure of a pH-sensing mycobacterial adenylyl cyclase holoenzyme. Science 308:1020–1023
Tucker CL, Hurley JH, Miller TR, Hurley JB (1998) Two amino acid substitutions convert a guanylyl cyclase, RetGC-1, into an adenylyl cyclase. Proc Natl Acad Sci USA 95:5993–5997
Weber JH, Vishnyakov A, Hambach K, Schultz A, Schultz JE, Linder JU (2004) Adenylyl cyclases from plasmodium, paramecium and tetrahymena are novel ion channel/enzyme fusion proteins. Cell Signal 16:115–125
Whisnant RE, Gilman AG, Dessauer CW (1996) Interaction of the two cytosolic domains of mammalian adenylyl cyclase. Proc Natl Acad Sci USA 93:6621–6625
Wittpoth C, Scholich K, Yigzaw Y, Stringfield TM, Patel TB (1999) Regions on adenylyl cyclase that are necessary for inhibition of activity by beta gamma and G(ialpha) subunits of heterotrimeric G proteins. Proc Natl Acad Sci USA 96:9551–9556
Yahr TL, Vallis AJ, Hancock MK, Barbieri JT, Frank DW (1998) ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc Natl Acad Sci USA 95:13899–13904
Yan SZ, Hahn D, Huang ZH, Tang WJ (1996) Two cytoplasmic domains of mammalian adenylyl cyclase form a Gsa- and forskolin-activated enzyme in vitro. J Biol Chem 271:10941–10945
Yan SZ, Huang ZH, Rao VD, Hurley JH, Tang WJ (1997a) Three discrete regions of mammalian adenylyl cyclase form a site for Gsalpha activation. J Biol Chem 272:18849–18854
Yan SZ, Huang ZH, Shaw RS, Tang WJ (1997b) The conserved asparagine and arginine are essential for catalysis of mammalian adenylyl cyclase. J Biol Chem 272:12342–12349
Zehmer JK, Hazel JR (2003) Plasma membrane rafts of rainbow trout are subject to thermal acclimation. J Exp Biol 206:1657–1667
Zhang G, Liu Y, Ruoho AE, Hurley JH (1997) Structure of the adenylyl cyclase catalytic core. Nature 386:247–253
Zimmermann G, Zhou D, Taussig R (1998) Mutations uncover a role for two magnesium ions in the catalytic mechanism of adenylyl cyclase. J Biol Chem 273:19650–19655
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We acknowledge support from the Howard Hughes Medical Institute, NIH grant DK46371 (SRS), Welch Foundation grant I-1229 (SRS) and the John W. and Rhonda K. Pate Professorship to SRS.
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Sinha, S.C., Sprang, S.R. (2006). Structures, mechanism, regulation and evolution of class III nucleotidyl cyclases. In: Reviews of Physiology Biochemistry and Pharmacology. Reviews of Physiology Biochemistry and Pharmacology, vol 157. Springer, Berlin, Heidelberg. https://doi.org/10.1007/112_0603
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