ADP-Ribosylation of Signal-Transducing Guanine Nucleotide-Binding Proteins by Pertussis Toxin

  • P. Gierschik
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 175)

Abstract

The gram-negative bacterium Bordetella pertussis, the causative agent of whooping cough, produces a number of virulence factors, among which pertussis toxin is undoubtedly of major importance (Weiss and Hewlett 1986). Pertussis toxin elicits a myriad of biological effects in patients suffering from whooping cough or infected laboratory animals and has thus received several names, including histamine-sensitizing factor, lymphocytosis-promoting factor, islet-activating protein (IAP), or simply pertussigen.

Keywords

Retina Arginine Disulfide Thiol Glucagon 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ad Hoc Group for the Study of Pertusis Vaccines (1988) Placebo-controlled trial of two acellular pertussis vaccines in Sweden: protective efficacy and adverse effects. Lancet i: 955–960Google Scholar
  2. Antoine R, Locht C (1990) Roles of the disulfide bond and the carboxy-terminal region of the S1 subunit in the assembly and biosynthesis of pertusis toxin. Infect Immun 58:1518–1526PubMedGoogle Scholar
  3. Asano T, Ross EM (1984) Catecholamine-stimulated guanosine 5’-0-(3-thiotriphosphate) binding to the stimulatory GTP-binding protein of adenylate cyclase: kinetic analysis in reconstituted phospholipid vesicles. Biochemistry 23: 5467–5471PubMedGoogle Scholar
  4. Askelof P, Rodmalm K, Wrangsell G, Larsson U, Svenson SB, Cowell JL, Unden A, Bartfai T (1990) Pertussis toxin-catalyzed ADP-ribosylation of guanine nucleotide-binding proteins: effects of in vitro mutagenesis at the carboxyterminus of G. FASEB J 5: A4041 (Abstract)Google Scholar
  5. Avigan J, Murthag JJ Jr, Stevens LA, Angus CW, Moss J, Vaughan M (1991) Requirements for pertussis toxin-catalyzed ADP-ribosylation of guanine nucleotide-binding proteins: effects of in vitro mutagenesis at the carboxyterminus of G. FASEB J 5: A4041 (Abstract)Google Scholar
  6. Backlund PS, Simonds WF, Spiegel AM (1990) Carboxymethylation and COOH-terminal processing of the brain G protein y-subunit. J Biol Chem 265:15572–15576PubMedGoogle Scholar
  7. Barbieri JT, Cortina G (1988) ADP-ribosyltransferase mutations in the catalytic S-1 subunit of pertussis toxin. Infect Immun 56:1934–1941PubMedGoogle Scholar
  8. Barbieri JT, Mende-Mueller LM, Rappuoli R, Collier RJ (1989a) Photolabelling of Glu-129 of the S-1 subunit of pertussis toxin with NAD. Infect Immun 57: 3549–3554PubMedGoogle Scholar
  9. Barbieri JT, Moloney BK, Mende-Mueller LM (1989b) Expression and secretion of the S-1 subunit and C180 peptide of pertussis toxin in Escherichia coli. Infect Immun 171: 4362–4369Google Scholar
  10. Barinaga M (1991) How the nose knows: olfactory receptors cloned. The abundant variety of receptors has powerful implications for the brain’s processing of smells. Science 252: 209–210PubMedGoogle Scholar
  11. Bartoloni A, Pizza M, Bigio M, Nucci D, Ashwort LA, Irons LI, Robinson A, Burns D, Manclark C, Sato H, Rappuoli R (1988) Mapping of a protective epitope of pertussis toxin by in vitro refolding of recombinant fragments. Bio/Technology 6: 709–712Google Scholar
  12. Bertrand P, Sanford J, Rudolph U, Codina J, Birnbaumer L (1990) At least three alternatively spliced mRNAs encoding two a subunits of the G0 GTP-binding protein can be expressed in a single tissue. J Biol Chem 265:18576–18580PubMedGoogle Scholar
  13. Birnbaumer L (1990) G proteins in signal transduction. Ann Rev Pharmacol Toxicol 30: 675–705Google Scholar
  14. Birnbaumer L, Abramowitz J, Brown AM (1990) Receptor-effector coupling by G proteins. Biochim Biophys Acta 1031: 163–224PubMedGoogle Scholar
  15. Black WJ, Munoz JJ, Peacock MG, Schad PA, Cowell JL, Burchall JJ, Lim M, Kent A, Steinman L, Falkow S (1988) ADP-ribosyltransferase activity of pertussis toxin and immunomodulation by Bordeila pertussis. Science 240: 656–659PubMedGoogle Scholar
  16. Bokoch GM, Katada T, Northup JK, Ui M, Gilman AG (1984) Purification and properties of the inhibitory guanine nucleotide-binding regulatory component of adenylate cyclase. J Biol Chem 259: 3560–3567PubMedGoogle Scholar
  17. Bray P, Carter A, Simons C, Guo V, Puckett C, Kamholz J, Spiegel A, Nirenberg M (1986) Human cDNA clones fqr four species of Gas signal transduction protein. Proc Natl Acad Sci USA 83: 8893–8897PubMedGoogle Scholar
  18. Brennan MJ, David JL, Kenimer JG, Manclark CR (1988) Lectin-like binding of pertussis toxin to a 165-kilodalton Chinese hamster ovary cell glycoprotein. J Biol Chem 263: 4895–4899PubMedGoogle Scholar
  19. Burnette WN, Cieplak W, Mar VL, Kaljot KT, Sato H, Keith JM (1988) Pertussis toxin S1 mutant with reduced enzyme activity and a conserved protective epitope. Science 242: 72–74PubMedGoogle Scholar
  20. Burns DL, Hausman SZ, Lindner W, Robey FA, Manclark CR (1987) Structural characterization of pertussis toxin A subunit. J Biol Chem 262:17677–17682PubMedGoogle Scholar
  21. Burns DL, Hausman SZ, Witvliet MH, Brennan MJ, Poolman JT, Manclark CR (1988) Biochemical properties of pertussis toxin. Tok J Exp Clin Med 13: 181–185Google Scholar
  22. Burns DL, Manclark CR, Hausman SZ (1990) Pertussis toxin and its mode of entry into eukaryotic cells. In: Manclark CR (ed) Proceedings of the Sixth International Symposium on Pertussis, Department of Health and Human Services, Bethesda, Maryland, DHHS Publication No. (FDA) 90–1164, pp 53–56Google Scholar
  23. Burns DL, Manclark CR (1986) Adenine nucleotide promote dissociation of pertussis toxin subunits. J Biol Chem 261: 4324–4327PubMedGoogle Scholar
  24. Bums DL, Manclark CR (1989) Role of cysteine 41 of the A subunit of pertussis toxin. J Biol Chem 264: 564–568Google Scholar
  25. Buss JE, Mumby S, Casey PJ, Gilman AG, Sefton BM (1987) Myristoylated a subunits of guanine nucleotide-binding regulatory proteins. Proc Natl Acad Sci USA 84: 7493–7497PubMedGoogle Scholar
  26. Cantiello HF, Patenaude CR, Codina J, Birnbaumer L, Ausiello DA (1990) Gal-3 regulates epithelial Na+ channels by activation of phospholipase A2 and lipoxygenase pathways. J Biol Chem 265: 21624–21628PubMedGoogle Scholar
  27. Capiau C, Petre J, Van Damme J, Puype M, Vandekerkhove J (1986) Protein-chemical analysis of pertussis toxin reveals homology between the subunits S2 and S3, between S1 and the A chains of enterotoxins ofVibrio cholerae and Escherichia coli and identifies S2 as the haptoglobin-binding subunit. FEBS Lett 204: 336–340PubMedGoogle Scholar
  28. Carroll SF, McCloskey JA, Crain PF, Oppenheimer NJ, Marschner TM, Collier RJ (1985) Photoaffinity labeling of diphtheria toxin fragment A with NAD: structure of the photoproduct at position 148. Proc Natl Acad Sci USA 82: 7237–7241PubMedGoogle Scholar
  29. Carroll SF, Collier RJ (1987) Active site ofPseudomonas areuginosa exotoxin A: glumatic acid 553 is photolabeled by NAD and shows functional homology with glutamic acid 148 of diphtheria toxin. J Biol Chem 262: 8707–8711PubMedGoogle Scholar
  30. Carty DJ, Iyengar R (1990) A 43kDA form of the GTP-binding protein G13 in human erythrocytes. FEBS Lett 262: 101–103PubMedGoogle Scholar
  31. Casey PJ, Graziano MP, Gilman AG (1989) G protein βγ subunits from bovine brain and retina: equivalent catalytic support of ADP-ribosylation of α subunits by pertussis toxin but differential interactions with Gsα. Biochemistry 28: 611–616PubMedGoogle Scholar
  32. Cassel D, Selinger Z (1977) Mechanism of adenylate cyclase activation by cholera toxin: inhibition of GTP hydrolysis at the regulatory site. Proc Natl Acad Sci USA 74: 3307–3311PubMedGoogle Scholar
  33. Cassel D, Levkovitz H, Selinger Z (9177) The regulatory GTPase cyclase of turkey erythrocyte adenylate cyclase. J Cyclic Nucleotide Res 3: 393–406Google Scholar
  34. Cerione RA, Codina J, Benovic JL, Lefkowitz RJ, Birnbaumer L, Caron MG (1984) The mammalian β 2-adrenergic receptor: reconstitution of functional interactions between pure receptor and pure stimulatory nucleotide binding protein of the adenylate cyclase system. Biochemistry 23: 4519–4525PubMedGoogle Scholar
  35. Cerione RA, Staniszewski C, Benovic JL, Lefkowitz RJ, Caron MG, Gierschik P, Somers RL, Spiegel AM, Codina J, Birnbaumer L (1985) Specificity of the functional interactions of the β-adrenergic receptor and rhodopsin with guanine nucleotide regulatory proteins reconstituted in phospholipid vesicles. J Biol Chem 260:1493–1500PubMedGoogle Scholar
  36. Cieplak W, Locht C, Mar VL, Burnette WN, Keith JM (1990) Photolabelling of mutant forms of the S1 subunit of pertussis toxin with NAD+. Biochem J 268: 547–551PubMedGoogle Scholar
  37. Cockle SA (1989) Identification of an active-site residue in subunit S1 of pertussis toxin by photocrosslihking to NAD. FEBS Lett 249: 329–332PubMedGoogle Scholar
  38. Codina J, Hildebrandt JD, Brinbaumer L, Sekura RD (1984) Effects of guanine nucleotides and Mg on human erythrocyte N1 and Ns, the regulatory components of adenylyl cyclase. J Biol Chem 259:11408–11418PubMedGoogle Scholar
  39. Cody CL, Baraff LJ, Cherry JD, March SM, Manclark CR (1981) Nature and rates of adverse reactions associated with DTP and DT immunizations in infants and in children. Pediatrics 68: 650–660PubMedGoogle Scholar
  40. Cortina G, Barbieri JT (1989) Role of tryptophan 26 in the NAD glycohydrolase reaction of the S-1 subunit of pertussis toxin. J Biol Chem 264:17322–17328PubMedGoogle Scholar
  41. Cortina G, Barbieri JT (1991) Localization of a region of the S1 subunit of pertussis toxin required for efficient ADP-ribosyltransferase activity. J Biol Chem 266: 3022–3030PubMedGoogle Scholar
  42. Costa T, Herz A (1989) Antagonists with negative intrinsic activity at δ opioid receptors coupled to GTP-binding proteins. Proc Natl Acad Sci USA 86: 7321–7325PubMedGoogle Scholar
  43. Costa T, Lang J, Gless C, Herz A (1990) Spontaneous association between opioid receptors and GTP-binding regulatory proteins in native membranes: specific regulation by antagonists and sodium ions. Mol Pharmacol 37: 383–394PubMedGoogle Scholar
  44. De Magistris MT, Romano M, Bartoloni A, Rappuoli R, Tagiiabue A (1989) Human T cell clones define S1 subunit as the most immunogenic moiety of pertussis toxin and determine its epitope map. J Exp Med 169:1519–1532PubMedGoogle Scholar
  45. Domenighini M, Montecucco C, Ripka WC, Rappuoli R (1991) Computer modelling of the NAD binding site of ADP-ribosylating toxins: active-site structure and mechanism of NAD binding. Mol Microbiol 5: 23–31PubMedGoogle Scholar
  46. Enomoto K, Asakawa T (1986) Inhibition of catalytic unit of adenylate cyclase and activation of GTPase of N, protein by βγ-subunits of GTP-binding proteins. FEBS Lett 202: 63–68PubMedGoogle Scholar
  47. Ferguson KM, Higashijima T, Smigel MD, Gilman AG (1986) The influence of bound GDP on the kinetics of guanine nucleotide binding to G proteins. J Biol Chem 261:7393–7399PubMedGoogle Scholar
  48. Florio VA, Sternweis PC (1985) Reconstitution of resolved muscarinic cholinergic receptors with purified GTP-binding proteins. J Biol Chem 260: 3477–3483PubMedGoogle Scholar
  49. Freissmuth M, Gilman AG (1989) Mutations of Gsα designed to alter the reactivity of the protein with bacterial toxins: substitutions at Arg187 result in loss of GTPase activity. J Biol Chem 264:21907–21914PubMedGoogle Scholar
  50. Fukada Y, Ohguro H, Saito T, Yoshizawa T, Akino T (1989) βγ-subunit of bovine transducin composed of two components with distinctive y-subunits. J Biol Chem 264: 5937–5943PubMedGoogle Scholar
  51. Fukada Y, Takao T, Ohguro H, Yoshizawa T, Akino T, Shimonishi Y (1990) Farnesylated y-subunit of photoreceptor G protein indispensable for GTP-binding. Nature 346: 658–660PubMedGoogle Scholar
  52. Fung BK-K, Yamane HK, Ota IM, Clarke S (1990) The y subunit of brain G-proteins is methyl esterified as a C-terminal cysteine. FEBS Lett 260: 313–317PubMedGoogle Scholar
  53. Gautam N, Northup J, Tamir H, Simon Ml (1990) G protein diversity is increased by associations with a variety of y subunits. Proc Natl Sci USA 87: 7973–7977Google Scholar
  54. Gierschik P, Jakobs KH (1987) Receptor mediated ADP-ribosylation of a phospholipase C-stimulating G protein. FEBS Lett 224: 219–223PubMedGoogle Scholar
  55. Gierschik P, Sidiropoulos D, Spiegel AM, Jakobs KH (1987) Purification and immunochemical characterization of the major pertussis-toxin-sensitive guanine-nucleotide-binding protein of bovine-neutrophil membranes. Eur J Biochem 165:185–194PubMedGoogle Scholar
  56. Gierschik P, Sidiropoulos D, Jakobs KH (1989a) Two distinct G-proteins mediate formyl peptide receptor signal transduction in human leukemia (HL-60) cells. J Biol Chem 264: 21470–21473PubMedGoogle Scholar
  57. Gierschik P, Sidiropoulos D, Steisslinger M, Jakobs KH (1989b) Na+ regulation of formyl peptide receptor-mediated signal transduction in HL-60 cells: evidence that the cation prevents activation of the G-protein by unoccupied receptors. Eur J Pharmacol 172: 481–492PubMedGoogle Scholar
  58. Gierschik P, Sidiropoulos D, Dieterich K, Jakobs KH (1990a) Structure and function of signal-transducing heterotrimeric guanosine triphosphate binding proteins. In: Habenicht A (ed) Growth factors, differentiation factors, and cytokines. Springer, Berlin, Heidelberg, New York, pp 395–413Google Scholar
  59. Gierschik P, Sidiropoulos D, Dieterich K, Jakobs KH (1990b) Transmembrane signalling by G-proteins. In: Nahorski SR (ed) Transmembrane signalling, intracellular, messengers and implications for drug development. Wiley, Chichester, pp 73–89Google Scholar
  60. Gierschik P, Moghtader R, Straub C, Dieterich K, Jakobs KH (1991) Signal amplification in HL-60 granulocytes: evidence that the chemotactic peptide receptor catalytically activates G-proteins in native plasma membranes. Eur J Biochem 197: 725–732PubMedGoogle Scholar
  61. Gordon JI, Duronio RJ, Rudnick DA, Adams SP, Gokel GW (1991) Protein N-myristoylation. J Biol Chem 266: 8647–8650PubMedGoogle Scholar
  62. Haga K, Haga T, Ichiyama A, Katada T, Kurose H, Ui M (1985) Functional reconstitution of purified muscarinic receptors and inhibitory guanine nucleotide regulatory protein. Nature 316:731–733PubMedGoogle Scholar
  63. Hausman SZ, Manclark CR, Burns DL (1990) Binding of ATP by pertussis toxin and isolated subunits. Biochemistry 29: 6128–6131PubMedGoogle Scholar
  64. Higashijima T, Ferguson KM, Sternweis PC, Smigel MD, Gilman AG (1987) Effects of Mg2+ and the βγ-subunit complex on the interactions of guanine nucleotides with G proteins. J Biol Chem 262: 762–766PubMedGoogle Scholar
  65. Hildebrandt JD, Sekura RD, Codina J, Iyengar R, Manclark CR, Birnbaumer L (1983) Stimulation and inhibition of adenylyl cyclase mediated by distinct regulatory proteins. Nature 302: 706–709PubMedGoogle Scholar
  66. Hodges TD, Bailey JC, Fleming JW, Kovacs RJ (1989) Selective parasympathectomy increases the quantity of inhibitory guanine nucleotide-binding proteins in canine cardiac ventricle. Mol Pharmacol 36: 72–77PubMedGoogle Scholar
  67. Hoshino S, Kikkawa S, Takahashi K, Itoh H, Kaziro Y, Kawasaki H, Suzuki K, Katada T, Ui M (1990) Identification of sites for alkylation by N-ethylmaleimde and pertussis toxin-catalyzed ADP-ribosylation on GTP-binding proteins. FEBS Lett 276: 227–231PubMedGoogle Scholar
  68. Hsia JA, Tsai S-C, Adamik R, Yost DA, Hewlett EL, Moss J (1985) Amino acid-specific ADP-ribosylation: sensitivity to hydroxylamine of [cysteine(ADP-ribose)] protein and [arginine-(ADP-ribose)] protein linkages. J Biol Chem 260: 16187–16191PubMedGoogle Scholar
  69. Hsu WH, Rudolph U, Sanford J, Bertrand P, Olate J, Nelson C, Moss LG, Boyd III AE, Codina J, Birnbaumer L (1990) Molecualr cloning of a novel splice variant of the a subunit of the mammalian G0 protein. J Biol Chem 265:11220–11226PubMedGoogle Scholar
  70. Huff RM, Neer EJ (1986) Subunit interactions of native and ADP-ribosylated α39 and α41, two guanine nucleotide-binding proteins from bovine cerebral cortex. J Biol Chem 261:1105–1110PubMedGoogle Scholar
  71. Iiri T, Tohkin M, Morishima N, Ohoka Y, Ui M, Katada T (1989) Chemotactic peptide receptor-supported ADP-ribosylation of a pertussis toxin substrate GTP-binding protein by cholera toxin in neutrophil-type HL-60 cells. J Biol Chem 264: 21394–21400PubMedGoogle Scholar
  72. Iyengar R, Rich KA, Herberg JT, Grenet D, Mumby S, Codina J (1987) Identification of a new GTP-binding protein: a Mr = 43000 substrate for pertussis toxin. J Biol Chem 262:9239–9245PubMedGoogle Scholar
  73. Iyengar R, Rich KA, Herberg JT, Premont RT, Codina J (1988) Glucagon receptor-mediated activation of Gs is accompanied by subunit dissociation. J Biol Chem 263: 15348–15353PubMedGoogle Scholar
  74. Jacobson MK, Loflin PT, Aboul-Ela N, Mingmuang M, Moss J, Jacobson EL (1990) Modification of plasma membrane protein cysteine residues by ADP-ribose in vivo. J Biol Chem 265:10825–10828PubMedGoogle Scholar
  75. Jakobs KH, Aktories K, Schultz G (1984) Mechanism of pertussis toxin action on the adenylate cyclase system: inhibition of the turn-on reaction of the inhibitory regulatory site. Eur J Biochem 140:177–181PubMedGoogle Scholar
  76. Jiang M, Pandey S, Tran VT, Fong HKW (1991) Guanine nucleotide-binding regulatory proteins in retinal pigment epithelial cells. Proc Natl Acad Sci USA 88: 3907–3911PubMedGoogle Scholar
  77. Jones DT, Reed RR (1989) Golf: an olfactory-neuron-specific G protein involved in odorant signal transduction. Science 244: 790–795PubMedGoogle Scholar
  78. Jones DT, Masters SB, Bourne HR, Reed RR (1990) Biochemical characterization of three stimulatory GTP-binding proteins: the large and small forms of Gs and the olfactory-specific G-protein G0f. J Biol Chem 265: 2671–2676PubMedGoogle Scholar
  79. Jones TLZ, Simonds WF, Merendino JJ Jr, Brann MR, Spiegel AM (1990) Myristoylation of an inhibitory GTP-binding protein a subunit is essential for its membrane attachment. Proc Natl Acad Sci USA 87: 568–572PubMedGoogle Scholar
  80. Kahn RA, Goddard C, Newkirk M (1988) Chemical and immunological characterization of the 21-kDa ADP-ribosylation factor of adenylate cyclase. J Biol Chem 263: 8282–8287PubMedGoogle Scholar
  81. Kanaho T, Tsai S-C, Adamik R, Hewlett EL, Moss J, Vaughan M (1984) Rhodopsin-enhanced GTPase activity of the inhibitory GTP-binding protein of adenylate cyclase. J Biol Chem 259: 7378–7381PubMedGoogle Scholar
  82. Kaslow HR, Lesikar DD (1987) Sulfhydryl-alkylating reagents inactive the NAD glycohydrolyase activity of pertussis toxin. Biochemistry 26: 4397–4402PubMedGoogle Scholar
  83. Kaslow HR, Lim LL, Moss J, Lesikar DD (1987) Structure activity analysis of the activation of pertussis toxin. Biochemistry 26: 123–127PubMedGoogle Scholar
  84. Kaslow HR, Schlotterbeck JD, Mar VL, Burnette WN (1989) Alkylation of cysteine 41, but not cysteine 200, decreases the ADP-ribosyltransferase activity of the S1 subunit of pertussis toxin. J Biol Chem 264: 6386–6390PubMedGoogle Scholar
  85. Katada T, Tamura M, Ui M (1983) The A protomer of islet-activating protein, pertussis toxin, as an active peptide catalyzing ADP-ribosylation of a membrane protein. Arch Biochem Biophys 224: 290–298PubMedGoogle Scholar
  86. Katada T, Oinum M, Ui M (1986a) Two guanine nucleotide-binding proteins in rat brain serving as the specific substrate of islet-activating protein, pertussis toxin: interactions of the a-subunits with βγ-subunits in development of their biological activities. J Biol Chem 261: 8182–8191PubMedGoogle Scholar
  87. Katada T, Oinuma M, Ui M (1986b) Mechanisms for inhibition of the catalytic activity of adenylate cyclase by the guanine nucleotide-binding proteins serving as the substrate of islet-activating protein, pertussis toxin. J Biol Chem 261: 5215–5221PubMedGoogle Scholar
  88. Kim KJ, Burnette WN, Sublett RD, Manclark CR, Kenimer JG (1989) Epitopes on the S1 subunit of pertussis toxin recognized by monoclonal antibodies. Infect Immun 57: 944–950PubMedGoogle Scholar
  89. Klinz F-J, Costa T (1989) Cholera toxin ADP-ribosylates the receptor-coupled form of pertussis toxin-sensitive G proteins. Biochem Biophys Res Commun 165: 554–560PubMedGoogle Scholar
  90. Kühn H (1981) Interactions of rod cell proteins with the disk membrane: influence of light, ionic strength, and nucleotides. Curr Top Membr Transp 15:171–201Google Scholar
  91. Lai RK, Perez-Sala D, Canada FJ, Rando RR (1990) The y subunit of transducin is farnesylated. Proc Natl Acad Sci USA 87: 7673–7677PubMedGoogle Scholar
  92. Larea CL, Bunt-Milam AH, Hurley JB (1989) α Transducin is present in blue-, green-, and red-sensitive cone photoreceptors in the human retina. Neuron 3: 367–376Google Scholar
  93. Linder ME, Ewald DA, Miller RJ, Gilman AG (1990) Purification and characterization of G0α and three types of G,a after expression in Escherichia coli. J Biol Chem 265: 8243–8251PubMedGoogle Scholar
  94. Linder ME, Pang I-H, Durinio RJ, Gordon JI, Sternweis PC, Gilman AG (1991) Lipid modifications of G protein subunits: myristoylation of G increases its affinity for ßγ. J Biol Chem 266: 4654–4659PubMedGoogle Scholar
  95. Lobban MD, Van Heyningen S (1988) Thiol reagents are substrates for the ADP-ribosyltransferase activity of pertussis toxin. FEBS Lett 233: 229–232PubMedGoogle Scholar
  96. Lochrie MA, Simon MI (1988) G protein multiplicity in eukaryotic signal transduction systems. Biochemistry 27: 4957–4965PubMedGoogle Scholar
  97. Locht C, Keith JM (1986) Pertussis toxin gene: nucleotide sequence and genetic organization. Science 232: 1258–1264PubMedGoogle Scholar
  98. Locht C, Barstad PA, Coligan JE, Mayer L, Munoz J J, Smith SG, Keith JM (1986) Molecular cloning of pertussis toxin genes. Nucl Acid Res 14: 3251–3261Google Scholar
  99. Locht C, Capiau C, Feron C (1989) Identification of amino acid residues essential for the enzymatic activities of pertussis toxin. Proc Natl Acad Sci USA 86: 3075–3079PubMedGoogle Scholar
  100. Locht C, Lobet Y, Feron C, Cieplak W, Keith JM (1990) The role of cysteine 41 in the enzymatic activities of the pertussis toxin S1 subunit as investigated by site-directed mutagenesis. J Biol Chem 265: 4552–4559PubMedGoogle Scholar
  101. Locht C, Cabezon T (1990) Molecular biological studies on the structure-function relationship of pertussis toxin and filamentous hemagglutinin. In: Manclark CR (ed) Proceedings of the Sixth International Symposium on Pertussis, Department of Health and Human Services, Bethesda, Maryland, DHHS Publication No. (FDA) 90–1164, pp 41–52Google Scholar
  102. Maltese WA (1990) Posttranslational modification of proteins by isoprenoids in mammalian cells. FASEB J 4: 3319–3328PubMedGoogle Scholar
  103. Manclark CR (ed) (1990) Proceedings of the Sixth International Symposium on Pertussis, Department of Health and Human Services, United States Public Health Service, Bethesda, Maryland, DHHS Publication No. (FDA) 90–1164, 1990, pp 1–408.Google Scholar
  104. Mattera R, Codina J, Sekura RD, Birnbaumer L (1986) The interaction of nucleotides with pertussis toxin: direct evidence for a nucleotide binding site on the toxin regulating the rate of ADP-ribosylation of N„ the inhibitory regulatory component of adenylyl cyclase. J Biol Chem 261: 11173–11179PubMedGoogle Scholar
  105. Mattera R, Codina J, Sekura RD, Birnbaumer L (1987) Guanosine 5’-0-(3-thiotriphosphate) reduces ADP-ribosylation of the inhibitory guanine nucleotide-binding regulatory protein of adenylyl cyclase (N) by pertussis toxin without causing dissociation of the subunits of N: evidence of existence of heterotrimeric pt + and pt + conformations of N1. J Biol Chem 262: 11247–11251PubMedGoogle Scholar
  106. Miller DL, Ross EM, Alderslade R, Bellman MH, Brawson NSB (1981) Pertussis immunization and serious acute neurological illness in children. Br Med J 282:1595–1599Google Scholar
  107. Milligan G, McKenzie FR (1988) Opioid peptides promote cholera-toxin-catalysed ADP-ribosylation of the inhibitory guanine-nucleotide-binding protein (G1) in membranes of neuroblastoma x glioma hybrid cells. Biochem J 252: 369–373PubMedGoogle Scholar
  108. Milligan G (1989) Foetal calf serum enhances cholera toxin-catalyzed ADP-ribosylation of the pertussis toxin-sensitive guanine nucleotide binding protein, G12, in rat glioma C6BUI cells. Cell Signal 1: 65–74PubMedGoogle Scholar
  109. Milligan G, Carr C, Gould GW, Mullaney I, Lavan BE (1991) Agonist-dependent, cholera toxin-catalyzed ADP-ribosylation of pertussis toxin-sensitive G-proteins following transfection of the α2-C10 adrenergic receptor into rat 1 fibroblasts: evidence for the direct interaction of a single receptor with two pertussis toxin-sensitive G-proteins, G12 and G13. J Biol Chem 266: 6447–6455PubMedGoogle Scholar
  110. Moss J, Stanley SJ, Morin JE, Dixon JE (1980) Activation of choleragen by thiol: protein disulfide oxidoreductase. J Biol Chem 255: 11085–11087PubMedGoogle Scholar
  111. Moss J, Stanley SJ, Burns DL, Hsia JA, Yost DA, Myers GA, Hewlett EL (1983) Activation by thiol of the latent NAD glycohydrolase and ADP-ribosyltransferase activities ofBordetella pertussis toxin (islet-activating protein). J Biol Chem 158:11879–11882Google Scholar
  112. Moss J, Stanley SJ, Watkins PA, Burns DL, Manclark CR, Kaslow HR, Hewlett EL (1986) Stimulation of the thiol-dependent ADP-ribosyltransferase and NAD glycohydrolase activities ofBrodetella pertussis toxin by adenine nucleotides, phospholipids, and detergents. Biochemistry 25: 2720–2725PubMedGoogle Scholar
  113. Moss J, Vaughan M (1988) ADP-ribosylation of guanyl nucleotide-binding regulatory proteins by bacterial toxins. Adv Enzymol 61: 303–379PubMedGoogle Scholar
  114. Mumby S, Heukeroth RO, Gordon JI, Gilman AG (1990a) G protein a-subunit expression, myristoylation, and membrane association in COS cells. Proc Natl Acad Sci USA 87: 728–732PubMedGoogle Scholar
  115. Mumby SM, Casey PJ, Gilman AG, Gutowski S, Sternweis PC (1990b) G protein γ subunits contain a 20-carbon isoprenoid. Proc Natl Acad Sci USA 87: 5873–5877PubMedGoogle Scholar
  116. Murayama T, Ui M (1984) [3H]GDP release from rat and hamster adipocyte membranes independently linked to receptors involved in activation or inhibition of adenylate cyclase. J Biol Chem 259: 761–769PubMedGoogle Scholar
  117. Navon SE, Fung BK-K (1987) Characterization of transducin from bovine retinal rod outer segments: participation of the amino-terminal region of Ta in subunit interaction. J Biol Chem 262:15746–15751PubMedGoogle Scholar
  118. Neer EJ, Lok JM, Wolf LG (1984) Purification and properties of the inhibitory guanine nucleotide regulatory unit of brain adenylate cyclase. J Biol Chem 259:14222–14229PubMedGoogle Scholar
  119. Neer EJ, Pulsifer L, Wolf LG (1988) The amino terminus of G-protein a-subunits is required for interaction with Py. J Biol Chem 263: 8996–9000PubMedGoogle Scholar
  120. Neer EJ, Clapham DE (1990) Structure and function of G-protein Py subunit. In: Iyengar R, Birnbaumer L (eds) G proteins. Academic, San Diego, pp 41–61Google Scholar
  121. Nicosia, A, Perugini M, Franzini C, Casagli MC, Borri MG, Almoni M, Neri P, Ratti G, Rappuoli R (1986) Cloning and sequencing of the pertussis toxin genes: operon structure and gene duplication. Proc Natl Acad USA 83:4631–4635Google Scholar
  122. Northup JK, Sternweis PC, Gilman AG (1983a) The subunits of the stimulatory regulatory component of adenylate cyclase: resolution, activity, and properties of the 35000-Delton (β) subunit. J Biol Chem 258:11361–11368PubMedGoogle Scholar
  123. Northup JK, Smigel MD, Sternweis PC, Gilman AG (1983b) The subunits of the stimulatory regulatory component of adenylate cyclase: resolution of the activated 45000-dalton (α) subunit. J Biol Chem 258:11369–11376PubMedGoogle Scholar
  124. Ohguro H, Fukada Y, Yoshizawa T, Saito T, Akino T (1990) A specific βγ- subunit of transducin stimulates ADP-ribosylation of the α-subunit by pertussis toxin. Biochem Biophys Res Commun 167:1235–1241PubMedGoogle Scholar
  125. Osawa S, Dhanasekaran N, Woon CW, Johnson GL (1990) Gα1-Gαs chimeras define the function of a chain domains in control of G protein activation and βγ subunit complex interaction. Cell 63: 697–706PubMedGoogle Scholar
  126. Paris S, Pouyssegur J (1987) Further evidence for a phospolipase C-coupled G protein in hamster fibroblasts: induction of inositol phosphate formation by fluoroaluminate and vanadate and inhibition by pertussis toxin. J Biol Chem 262:1970–1976PubMedGoogle Scholar
  127. Pizza M, Bartoloni A, Prugnola A, Silvstri S, Rappuoli R (1988) Subunit S1 of pertussis toxin: mapping of the regions essential for ADP-ribosyltransferase activity. Proc Natl Acad Sci USA 85: 7521–7525PubMedGoogle Scholar
  128. Pizza M, Covacci A, Bartoloni A, Perugini M, Nencioni L, De Magistris MT, Villa L, Nucci D, Manetti R, Bugnoli M, Giovannoni F, Olivieri R, Barbieri JT, Sato H, Rappuoli R (1989) Mutants of pertussis toxin suitable for vaccine development. Science 246: 497–500PubMedGoogle Scholar
  129. Pizza M, Bugnoli M, Manetti R, Covacci A, Rappuoli R (1990) The subunit S1 is important for pertussis toxin secretion. J Biol Chem 265:17759–17763PubMedGoogle Scholar
  130. Pizza M, Bugnoli M, Pucci P, Siciliano R, Marino G, Rappuoli R (1991) Further analysis of the sequence of the S1 subunit of pertussis toxin. Infect Immun 59:1177–1179PubMedGoogle Scholar
  131. Raghavan M, Gotto JW, Scott JV, Schutt CE (1991) Preliminary X-ray crystallographic analysis of holotoxin from Bordetella pertussis. J Mol Biol 213:411–414Google Scholar
  132. Ransnäs LA, Insel PA (1988) Subunit dissociation is the mechanism for hormonal activation of the Gs protein in native membranes. J Biol Chem 263:17239–17242PubMedGoogle Scholar
  133. Ribeiro-Neto FAP, Mattera R, Hildebrandt JD, Codina J, Field JB, Birnbaumer L, Sekura RD (1985) ADP-ribosyfation of membrane components by pertussis and cholera toxin. Methods in Enzymology 109: 566–573PubMedGoogle Scholar
  134. Ribeiro-Neto FAP, Mattera R, Grenet D, Sekura RD, Birnbaumer L, Field JB (1987) Adenosine diphosphate ribosylation of G proteins by pertussis and cholera toxin: different requirements for and effects of guanine nucleotides and Mg2+. Mol Endocrinol 1: 472–481PubMedGoogle Scholar
  135. Sato H, Ito A, Chiba J, Sato Y (1984) Monoclonal antibody against pertussis toxin: effect on toxin activity and pertussis infections. Infect Immun 46: 422–428PubMedGoogle Scholar
  136. Sato H, Sato Y, Ito A, Ohishi I (1987) Effect of monoclonal antibody to pertussis toxin on toxin activity. Infect Immun 55:909–915PubMedGoogle Scholar
  137. Schultz AM, Tsai S-C, Kung H-F, Oroszlan S, Moss J, Vaughan M (1987) Hydroxylamine-stable covalent linkage of myristic acid in G0α, a guanine nucleotide-binding protein of bovine brain. Biochem Biophys Res Commun 146:1234–1239PubMedGoogle Scholar
  138. Sekura RD, Fish F, Manclark CR, Meade B (1983) Pertussis toxin: affinity purification of a new ADP-ribosyltransferase. J Biol Chem 258:14647–14651PubMedGoogle Scholar
  139. Sekura RD, Moss J, Vaughan M (eds) (1985) Pertussis toxin. Academic, Orlando, pp 1–255Google Scholar
  140. Simon MI, Strathmann M, Gautam N (1991) Diversity of G proteins in signal transduction. Science 252: 802–808PubMedGoogle Scholar
  141. Simonds WF, Butrynski JE, Gautam N, Unson CG, Spiegel AM (1991) G-protein βγ-dimers: membrane targeting requires subunit coexpression and intact γ C-A-A-X domain. J Biol Chem 266: 5363–5366PubMedGoogle Scholar
  142. Sixma TK, Pronk SE, Kalk KH, Wartna ES, Van Zanten BAM, Witholt B, Hol WGJ (1991) Crystal structure of a cholera toxin-related heat-labile enterotoxin from E coli. Nature 351: 371–377PubMedGoogle Scholar
  143. Smigel MD, Northup JK, Gilman AG (1982) Characteristics of the guanine nucleotide-binding regulatory component of adenylate cyclase. Recent Progr Horm Res 38: 601–624PubMedGoogle Scholar
  144. Spicher K, Klinz F-J, Nürnberg B, Tychowiecka I, Rosenthal W (1991a) Peptide antibodies distinguish between subtypes of G0 α-subunits. Naunyn-Schmiedeberg’s Arch Pharmacol 343: R37 (Abstract)Google Scholar
  145. Spicher K, Klinz F-J, Rudolph U, Codina J, Birnbaumer L, Schultz G, Rosenthal W (1991b) Identification of the G protein a-subunit encoded by αo2 cDNA as a 39kDa pertussis toxin substrate. Biochem Biophys Res Commun 175:473–479PubMedGoogle Scholar
  146. Storsaeter J, Olin P, Renemar B, Lagergard T, Norberg R, Romanus V, Tiru M (1988) Mortality and morbidity from invasive bacterial infections during a clinical trial of acellular pertussis vaccines in Sweden. Pediater Infect Dis J 7: 637–645Google Scholar
  147. Strathmann M, Wilkie TM, Simon MI (1989) Diversity of the G-protein family: sequences from five additional a subunits in the mouse. Proc Natl Acad Sci USA 86: 7407–7409PubMedGoogle Scholar
  148. Strathmann M, Simon MI (1990) G protein diversity: a distinct class of a subunits is present in vertebrates and invertebrastes. Proc Natl Acad sci USA 87: 9113–9117PubMedGoogle Scholar
  149. Strathmann M, Wilkie TM, Simon MI (1990) Alternative splicing produces transcripts encoding two forms of the a subunit of GTP-binding protein G0. Proc Natl Acad sci USA 87: 6477–6481PubMedGoogle Scholar
  150. Sunyer T, Monastirsky B, Codina J, Birnbaumer L (1989) Studies on nucleotide and receptor regulation of G, proteins: effects of pertussis toxin. Mol Endocrinol 3:1115–1124PubMedGoogle Scholar
  151. Tamir H, Fawzi AB, Tamir A, Evans T, Northup JK (1991) G-protein ßγ-iorms: identity of ß and diversity of γ-subunits. Biochemistry 30: 3929–3936PubMedGoogle Scholar
  152. Tamura M, Nogimori K, Murai S, Yajima M, Ito K, Katada T, Ui M, Ishii S (1982) Subunit structure of islet-activating protein, pertussis toxin, in conformity with the A-B model. Biochemistry 21:5516–5522PubMedGoogle Scholar
  153. Tamura M, Nogimori K, Yajima M, Ase K, Ui M (1983) A role of the B-oligomer moiety of islet-activating protein, pertussis toxin, in development of the biological effects on intact cells. J Biol Chem 258: 6756–6761PubMedGoogle Scholar
  154. Tanuma S, Kawashima K, Endo H (1988) Eukaryotic mono(ADP-ribosyl)transferase that ADP-ribosylates GTP-binding regulatory G, protein. J Biol Chem 263: 5485–5489PubMedGoogle Scholar
  155. Tsuchiya M, Bliziotes MM, Serventi IM, Price SR, Avigan J, Murtagh JJ, Stevens LA, Angus CW, Walker MW, Newman KB, Helpern JL, Tsai SC, Moss J, Vaughan M (1990) Pertussis toxin substrates: characterization of multiple forms of G mRNA and the requirements for toxincatalyzed ADP-ribosylation of G and G. Manclark CR (ed) Proceedings of the Sixth International Symposium on Pertussis, Department of Health and Human Services, Bathesda, Maryland, DHHS Publication No. (FDA) 90–1164, pp 57–65Google Scholar
  156. Tsukamoto T, Toyama R, Itoh H, Matsuoka M, Kaziro Y (1991) Structure of the human gene and two rat cDNAs encoding the a chain of GTP-binding regulatory protein Go: two different mRNAs are generated by alternative splicing. Proc Natl Acad sci USA 88: 2974–2978PubMedGoogle Scholar
  157. Ui M (1984) Islet-activating protein, pertussis toxin: a probe for functions of the inhibitory guanine nucleotide regulatory component of adenylate cyclase. Trends Pharmacol sci 5: 277–279Google Scholar
  158. Ui M (1986) Pertussis toxin as a probe of receptor coupling to inositol lipid metabolism. In: Putney JW (ed) Phosphoinositides and receptor mechanisms. Liss, New York, p 163Google Scholar
  159. Van Dop C, Tsubokawa M, Bourne HR, Ramachandran J (1984a) Amino acid sequence of retinal transducin at the site ADP-ribosylated by cholera toxin. J Biol Chem 259: 696–698PubMedGoogle Scholar
  160. Van Dop C, Yamanaka G, Steinberg F, Sekura RD, Manclark CR, Stryer L, Bourne HR (1984b) ADP-ribosylation of transducin by pertussis toxin blocks the light-stimulated hydrolysis of GTP and cGMP in retinal photoreceptors. J Biol Chem 259: 23–26PubMedGoogle Scholar
  161. Watkins PA, Moss J, Burns DL, Hewlett EL, Vaughan M (1984) Inhibition of bovine rod outer segement GTPase by Bordetella pertussis toxin. J Biol Chem 259:1378–1381PubMedGoogle Scholar
  162. Watkins PA, Burns DL, Kanaho Y, Liu T-Y, Hewlett EL, Moss J (1985) ADP-ribosylation of transducin by pertussis toxin. J Biol Chem 260:13478–13482PubMedGoogle Scholar
  163. West RE Jr, Moss J, Vaughan M, Liu T, Liu T-Y (1985) Pertussis toxin-catalyzed ADP-ribosylation of transducin: cysteine 347 is the ADP-ribose acceptor site. J Biol Chem 260:14428–14430PubMedGoogle Scholar
  164. Weiss AA, Hewlett EL (1986) Virulence factors of Bordetella pertussis. Ann Rev Microbiol 40: 661–686Google Scholar
  165. Winslow JW, Bradley JD, Smith JA, Neer EJ (1987) Reactive sulfhydryl groups of α39, a guanine nucleotide-binding protein from brain: location and function. J Biol Chem. 262: 4501–4507PubMedGoogle Scholar
  166. Witvliet MH, Burns DL, Brennan MJ, Poolman JT, Manclark CR (1989) Binding of pertussis toxin to eucaryotic cells and glycoproteins. Infect Immun 57: 3324–3330PubMedGoogle Scholar
  167. Wong YH, Federman A, Pace AM, Zachary I, Evans T, Pouyssegur J, Bourne HR (1991) Mutant α subunits of Gi2 inhibit cyclic AMP accumulation. Nature 351: 63–65PubMedGoogle Scholar
  168. Yamamoto T, Nakazawa T, Miyata T, Kaji A, Yokata T (1984) Evolution and structure of two ADP-ribosylation enterotoxins, Escherichia coli heat-labile toxin and cholera toxin. FEBS Lett 169: 241–246PubMedGoogle Scholar
  169. Yamane HK, Farnsworth CC, Xie H, Howald W, Fung BK-K, Clarke S, Gelb MH, Glomset JA (1990) Brain G protein γ subunits contain an all-trans-geranylgeranyl-cysteine methyl ester at their carboxyl termini. Proc Natl Acad Sci 87: 5868–5872PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin · Heidelberg 1992

Authors and Affiliations

  • P. Gierschik
    • 1
  1. 1.Pharmakologisches InstitutUniversität HeidelbergHeidelbergGermany

Personalised recommendations