Advertisement

Hormonal Regulation of Adenylyl Cyclase Activity

  • Howard J. Kirchick
  • Juan Codina
  • John D. Hildebrandt
  • Ravi Iyengar
  • Francisco J. Rojas
  • Joel Abramowitz
  • Mary Hunzicker-Dunn
  • Lutz Birnbaumer
Part of the Biochemical Endocrinology book series (BIOEND, volume 1)

Abstract

Peptide and protein hormones such as glucagon and gonadotropins and neurotransmitters such as chatecholamines exert their action on target cells by binding to their respective receptors (R). These interactions lead to stimulation of cAMP formation by the adenylyl cyclase systems in these cells. In what follows we shall review and present key experimental evidences on functional aspects of cAMP forma- tion by adenylyl cyclases as seen both in the absence and presence of hormonal influence. We shall present current knowledge on the molecular composition and structure of hormone sensitive adenylyl cyclases. Taking structural as well as functional aspects into account we shall discuss current thoughts on how both hormonal stimulation and the ensuing desensitization to hormonal stimulation come about. Finally we shall present some speculations as to other forms of regulation, especially attenuation of cAMP formation and raise some of the most pertinent questions in signal transduction research.

Keywords

Adenylate Cyclase Adenylyl Cyclase Hormonal Regulation Guanine Nucleotide Adenylyl Cyclase Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abramowitz, J., and Birnbaumer, L., 1982, Properties of the hormonally responsive rabbit luteal adenylyl cyclase: effects of guanine nucleotides and magnesium ion on stimulation by gonadotropin and catecholamines, Endocrinology 110:773.PubMedCrossRefGoogle Scholar
  2. Abramowitz, J., Iyengar, R., and Birnbaumer, L., 1980, On the mode of action of catecholamines on the turkey erythrocyte adenylyl cyclase: Evaluation of basic activity states after removal of endogenous GDP and interpretation of nucleotide regulation and hormone activation in terms of a two state model, J. Biol. Chem. 255:8259.PubMedGoogle Scholar
  3. Abramowitz, J., Iyengar, R., and Birnbaumer, L., 1982, Guanine nucleotide and magnesium ion regulation of the interaction of gonadotropic and -adrenergic receptors with their hormones: a comparative study using a single membrane system, Endocrinology 110:336.PubMedCrossRefGoogle Scholar
  4. Aktories, K., and Jakobs, K. H., 1981, Epinephrine inhibits adenylate cyclase and stimulates a GTPase in human platelet membranes via -adrenoceptors, FEBS Letters 130:235.PubMedCrossRefGoogle Scholar
  5. Aktories, K., Schultz, G., and Jakobs, K. H., 1979, Inhibition of hamster fat cell adenylate cyclase by prostaglandin Ei and epinephrine: requirement for GTP and sodium ions, FEBS Letters 107:100.PubMedCrossRefGoogle Scholar
  6. Amsterdam, A., Nimrod, A., Lamprecht, S. A., Bernstein, Y., and Lindner, H. R., 1974, Internalization and degradation of receptor-bound hCG in granulosa cell cultures, Am. J. Physiol. 236:E129.Google Scholar
  7. Anderson, W. B., and Jaworski, C. J., 1979, Isoproteronol induced desensitization of adenylyl cyclase responsiveness in a cell-free system, J. Biol. Chem. 254:4596.PubMedGoogle Scholar
  8. Bird, S. J., and Maguire, M. E., 1978, The agonist-specific effect of magnesium action of magnesium action of GTP and magnesium in adenylate cyclase activation, J. Biol. Chem. 253:8826.PubMedGoogle Scholar
  9. Birnbaumer, L., Pohl, S. L., and Rodbell, M., 1969, Adenyl cyclase in fat cells. I. Properties and effects of adrenocorticotropin and fluoride, J. Biol. Chem. 244:3468.PubMedGoogle Scholar
  10. Birnbaumer, L., Swartz, T. L., Abramowitz, J., Mintz, P. W., and Iyengar, R., 1980, Transient and steady state kenetics of the interaction of nucleotides with the adenylyl cyclase system from rat liver plasma membranes: Interpretation in terms of a simple two-state model, J. Biol. Chem. 255:3542.PubMedGoogle Scholar
  11. Birnbaumer, L., Swartz, T. L., Rojas, F. J., and Garber, A. J., 1983, Synthesis, purification by HPLC and characterization of monoiodoglucagon labeled with carrier-free 125I: use as a glucagon receptor probe, J. Receptor Res, (in press).Google Scholar
  12. Blume, A. J., Lichtstein, D., and Boone, G., 1979, Coupling of opiate receptors to adenylate cyclase: Requirement for Na and GTP, Proc. Natl. Acad. Sci. USA 76:5626.PubMedCrossRefGoogle Scholar
  13. Blockaert, J., Hunzicker-Dunn, M., and Birnbaumer, L., 1976, Hormone-stimulated desensitization of hormone-dependent adenylyl cyclase, J. Biol. Chem. 251:2653.Google Scholar
  14. Brown, M. S., and Goldstein, J. L., 1976, Receptor mediated control of cholesterol metabolism, Science 191:150.PubMedCrossRefGoogle Scholar
  15. Cassel, D., and Pfeuffer, T., 1978, Mechanism of cholera toxin action: covalent modification of the guanyl nucleotidebinding protein of the adenylate cyclase system, Proc. Natl. Acad. Sci. USA 75:2669.PubMedCrossRefGoogle Scholar
  16. Cassel, D., and Selinger, Z., 1976, Catecholamine-stimulated GTPase activity in turkey erythrocyte membranes, Biochim. Biophys. Acta 452:538.PubMedGoogle Scholar
  17. cyclase activation by cholera toxin: inhibition of GTP hydrolysis at the regulatory site, Proc. Natl. Acad. Sci. USA 74:3307.PubMedCrossRefGoogle Scholar
  18. cyclase activation through the beta-adrenergic receptor. Catecholamine-induced displacement of bound GDP by GTP. Proc. Natl. Acad. Sci. USA 75:4155.PubMedCrossRefGoogle Scholar
  19. Conn, P. M., Conti, M., Harwood, J. P., Dufau, M. L., and Catt, K. J., 1978, Internalization of gonadotropin receptor complex in ovarian luteal cells, Nature 274:598.PubMedCrossRefGoogle Scholar
  20. Catt, K. J., 1978, Internalization of gonadotropin receptor and desensitization of adenylate cyclase in the ovary, J. Biol. Chem. 251:7729.Google Scholar
  21. Cooper, D. M. F., 1982, Biomodal regulation of adenylate cyclase, FEBS Letters 138:157.PubMedCrossRefGoogle Scholar
  22. Cooper, D. M. F., Schlegel, W., Lin, M. C., and Rodbell, M.,1979, The fat cell adenylate cyclase system; characteriza-tion and manipulation of its bimodal regulation by GTP, J. Biol. Chem. 254:8927.PubMedGoogle Scholar
  23. Cronin, M. J., Myers, G. A., Dabney, L. G., and Hewlett, E. L., 1982, Pertussis toxin uncouples dopamine receptor-mediated inhibition of prolactin release. 64th Annual Meeting of the Endocrine Society, Abstract, No. 857, p. 294.Google Scholar
  24. Dufau, M. L., Baukal, A. J., and Catt, K. J., 1980, Hormoneinduced guanyl nucleotide binding and activation of aden-ylate cyclase in the Leydig cell, Proc. Natl. Acad. Sci. USA 77:5837.PubMedCrossRefGoogle Scholar
  25. Ezra, E., and Salomon, Y., 1980, Mechanism of desensitization of adenylate cyclase by lutropin. GTP-dependent uncoupling of the receptor, J. Biol. Chem. 255:65.Google Scholar
  26. Ezra, E., and Salomon, Y., 1981, Mechanism of adenylate cyclase by lutropin. Impaired introduction of GTP into the regula-tory site, J. Biol. Chem. 256:5377.PubMedGoogle Scholar
  27. Ferguson, K. M., Northup, J. K., and Gilman, A. G., 1982, Goat antibodies to the regulatory component of adenylate cyclase, Fed. Proc. 41:1407 (Abstract No. 6642).Google Scholar
  28. Fung, B. K.-K., Hurley, J. B., and Stryer, L., 1981, Flow of information in the light-triggered cyclic nucleotide cascade of vision, Proc. Natl. Acad. Sci. 78:152.PubMedCrossRefGoogle Scholar
  29. Gill, P. M., and Meren, R., 1978, ADP-ribosylation of membrane proteins catalyzed by cholera toxin. Basis of the activa-tion of adenylate cyclase, Proc. Natl. Acad. Sci. USA75:3050.PubMedCrossRefGoogle Scholar
  30. Hepatic alpha1-adrenergic receptors show agonist-specific regulation by guanine nucleotides: Loss of nucleotide effect after adrenalectomy, J. Biol. Chem., 257:11577.PubMedGoogle Scholar
  31. Hanski, E., Sternweis, P. C., Northrup, J. K., Domerick, A. W., and Gilman, A. G., 1981, The regulatory component of adenylate cyclase, J. Biol. Chem. 256:12911.PubMedGoogle Scholar
  32. Harwood, J. P., Conti, M., Conn, P. M., Dufau, M. L., and Catt, K. J., 1978, Receptor regulation and target cell responses: studies in the ovarian luteal cell, Mol. Cell. Endocrinol. 11:121.PubMedCrossRefGoogle Scholar
  33. Hazeki, O., and Ui, M., 1980, Modification by islet-activating protein of receptor-mediated regulation of cyclic AMP accumulation in isolated rat heart cells, J. Biol. Chem. 256:2856.Google Scholar
  34. Hildebrandt, J., Hanoune, J., and_Birnbaumer, L., 1982, Guanine nucleotide inhibition of cyc S49 mouse lymphoma cell mem-brane adenylyl cyclase, J. Biol. Chem., 257:14723.PubMedGoogle Scholar
  35. Hoffman, B., Mullikin-Kilpatrick, D., and Lefkowitz, R. J., 1980, Heterogeneity of radioligand binding to -adrenergic receptors; analysis of guanine nucleotide regulation of agonist binding in relation to receptor subtypes, J. Biol. Chem. 255:4645.PubMedGoogle Scholar
  36. Hsueh, A. J. W., Dufau, M. L., and Catt, K. J., 1976, Regulation of luteinzing hormone receptors in testicular interstitial cells by gonadotropin, Biochem. Biophys. Res. Commun. 72:1145.PubMedCrossRefGoogle Scholar
  37. Hsueh, A. J. W., Dufau, M. L., and Catt, K. J., 1977, Gonado-tropin-induced regulation of luteinizing hormone receptors and desensitization of testicular 3’5’-cyclic AMP and tes-tosterone responses, Proc. Natl. Acad. Sci. USA 74:592.PubMedCrossRefGoogle Scholar
  38. Hunzicker-Dunn, M., and Birnbaumer, L., 1976a, Adenylyl cyclase in ovarian tissues. II. Regulation of responsiveness to LH, FSH, and PGEx in the rabbit, Endocrinology 99:185.PubMedCrossRefGoogle Scholar
  39. Hunzicker-Dunn, M., and Birnbaumer, L., 1976b, Adenylyl cyclase activities in ovarian tissues. III. Regulation of respon-siveness to LH, FSH and PGE1 in prepubertal, cycling, pregnant and pseudopregnant rats, Endocrinology 99:198.PubMedCrossRefGoogle Scholar
  40. Hunzieker-Dunn, M., and Birnbaumer, L., 1976C., Adenylyl cyclase activities in ovarian tissues. IV. Gonadotropin-induced desensitization of the luteal adenylyl cyclase throughout pregnancy and pseudopregnancy in the rabbit and the rat, Endocrinology 99:211.CrossRefGoogle Scholar
  41. Hunzicker-Dunn, M., and Birnbaumer, L., 1981, Studies on the mechanism of LH-induced desensitization of the rabbit follicular adenylyl cyclase system in vitro, Endocrilology109:345.CrossRefGoogle Scholar
  42. Hunzicker-Dunn, M., Derda, D., Jungmann, R. A., and Birnbaumer, L., 1979a, Resensitization of the desensitized folli-cular adenylyl cyclase system to LH, Endocrinology104:1785.PubMedCrossRefGoogle Scholar
  43. Hunzicker-Dunn, M., Day, S. L., Abramowitz, J., and Birnbaumer, L., 1979b, Ovarian responses of pregnant mare serum gonadotropin-and human chorionic gonadotropin-primed rats: desensitizing, luteolytic and ovulatory effects of a single dose of human chorionic gonadotropin, Endocrinology105:442.PubMedCrossRefGoogle Scholar
  44. Iyengar, R., 1981, Hysteretic activation of adenylyl cyclases. II. Mg ion regulation of the activation of the regulatory component as seen in reconstitution assays, J. Biol. Chem. 256:11042.PubMedGoogle Scholar
  45. Iyengar, R., and Birnbaumer, L., 1979, GDP promotes coupling and activation of cyclizing activity in the glucagonsensitive adenylate cyclase system of rat liver plasma membranes. Evidence for two levels of regulation in adenylyl cyclase, Proc. Natl. Acad. Sci. USA 76:3189.PubMedCrossRefGoogle Scholar
  46. Iyengar, R., and Birnbaumer, L., 1981, Hysteretic activation of adenylyl cyclases. I. Effects of Mg ion on the rate of activation by guanine nucleotides and fluoride, J. Biol. Chem. 256:11036.PubMedGoogle Scholar
  47. Iyengar, R., and Birnbaumer, L., 1982, Hormone receptor modu-lates the regulatory component of adenylyl cyclase by reducing its requirement for Mg and enhancing its extent of activation, Proc. Natl. Acad. Sci. USA (in press).Google Scholar
  48. Iyengar, R., Abramowitz, J., Bordelon-Riser, M. E., Blume, A. J., and Birnbaumer, L., 1980a, Regulation of hormonereceptor coupling to adenylyl cyclase: effects of GTP and GDP, J. Biol. Chem. 255:10312.PubMedGoogle Scholar
  49. Iyengar, R., Mintz, P. W., Swartz, T. L., and Birnbaumer, L., 1980b, Divalent cation-induced desensitization of glucagon stimulable adenylyl cyclase in rat liver plasma membranes: GTP-dependent stimulation by glucagon, J. Biol. Chem. 255:11875.PubMedGoogle Scholar
  50. Iyengar, R., Bhat, M. K., Riser, M. E., and Birnbaumer, L., 1981, Receptor-specific desensitization of the S49 cell adenylyl cyclase: unaltered behavior of the regulatory component, J. Biol. Chem. 256:4810.PubMedGoogle Scholar
  51. Jakobs, K. H., Actories, K., and Schultz, G., 1979, GTP-dependent inhibition of cardiac adenylate cyclase by muscarinic cholinergic agonists, Naunyn-Achmiedeberg* s Arch. Pharmacol. 310:113.CrossRefGoogle Scholar
  52. Jard, S., Cantau, B., and Jakobs, K. R., 1981, Angiotensin II and -adrenergic agonists inhibit rat liver adenylate cyclase, J. Biol. Chem. 256:2603.PubMedGoogle Scholar
  53. Jonassen, J. A., and Richards, J. S., 1980, Granulosa cell desensitization: effects of gonadotropins in antral and preantral follicles, Endocrinology 106:1786.PubMedCrossRefGoogle Scholar
  54. Kaslow, H. R., Farfel, Z., Johnson, G. L., and Bourne, H. R., 1979, Adenylate cyclase assembled in vitro: cholera toxin substrates determines different patterns of regulation by isoproterenol and guanosine 5’-triphosphate, Mol. Pharmacol. 15:472.PubMedGoogle Scholar
  55. Katada, T., and Ui, M., 1981, Islet-activating protein; a modi-fier of receptor-mediated regulation of rat islet adenylate cyclase, J. Biol. Chem. 256:8310.PubMedGoogle Scholar
  56. Katada, T., and Ui, M., 1982a, ADP ribosylation of the specific membrane protein of C6 cells by islet-activating protein associated with modification of adenylate cyclase activity, J. Biol. Chem. 257:7210.PubMedGoogle Scholar
  57. Katada, T., and Ui, M., 1982b, Direct modification of the membrane adenylate cyclase system by islet-activating protein due to ADP-ribosylation of a membrane protein, Proc. Natl. Acad. Sci. USA 79:3129.PubMedCrossRefGoogle Scholar
  58. Katikineni, M., Davies, T. F., Huhtaniemi, I. T., and Catt, K. J., 1980, Luteinizing hormone-receptor interaction in the testis: progressive decrease in reversibility of the hormone-receptor complex, Endocrinology 107:1980.PubMedCrossRefGoogle Scholar
  59. Kirchick, H. J., and Birnbaumer, L., 1982, hCG-induced desensi-tization of luteal catecholamine-responsive adenylyl cyclase is a result of alterations in the nucleotide binding regulatory (N)-component, Biol. Reprod. 26 (Suppl. # 1), 41A (Abstract #10).Google Scholar
  60. Koch, Y., Zor, U., Pomerantz, S. H., Chobsieng, P., and Lindner, H. R., 1973, Intrinsic stimulatory action of follicle stimulating hormone on ovarian adenylate cyclase, J Endocrinol. 58:677.PubMedCrossRefGoogle Scholar
  61. Lamprecht, S. A., Zor, U., Tsafriri, A., and Lindner, H. R., 1973, Action of prostaglandin E2 and of luteinizing hormone on ovarian adenylate cyclase, protein kinase and ornithine decarboxylase activity during postnatal development and maturity in the rat, J. Endocrinol. 57:217.PubMedCrossRefGoogle Scholar
  62. Limbird, L. E., Gill, D. M., and Lefkowitz, R. J., 1980, Agonist-promoted coupling of the B-adrenergic receptor with the guanine nucleotide protein of the adenylate cyclase system, Proc. Natl. Acad. Sci. 77:775.PubMedCrossRefGoogle Scholar
  63. Londos, C., Cooper, D. M. F., Schlegel, W., and Rodbell, M., 1978, Adenosine analogs inhibit adipocyte adenylate cyclase by a GTP-dependent process: basis for actions of adenosine and methylxanthines on cyclic AMP pro-duction and lipolysis, Proc. Natl. Acad. Sci. USA 75:5362.PubMedCrossRefGoogle Scholar
  64. Marsh, J. M., Mills, T. M., and LeMaire, W. J., 1972, Cyclic AMP synthesis in the rabbit Graafian follicle and the effect of luteinizing hormone, Biochim. Biophys. Acta 273:197.CrossRefGoogle Scholar
  65. Nickols, G. A., and Brooker, G., 1979, Induction of refractor-iness to isoproterenol by prior treatment of C6-2B rat astrocytoma cells with cholera toxin, J. Cyclic Nucleo. Res. 5:435.Google Scholar
  66. Northup, J. K., Sternweis, P. C., Smigel, M. D., Schleifer, L. S., Ross, E. M., and Gilman, A. G., 1980, Purification of the regulatory component of adenylate cyclase, Proc. Natl. Acad. Sci. USA 77:6515.CrossRefGoogle Scholar
  67. Pfeuffer, T., 1977, GTP-binding proteins in membranes and the control of adenylate cyclase activity, J. Biol. Chem. 252:7224.PubMedGoogle Scholar
  68. Pfeuffer, T., 1979, Guanine nucleotide-controlled interactions between components of adenylate cyclase, FEBS Letters101:85.PubMedCrossRefGoogle Scholar
  69. Rao, M. C., Richards, J. S., Midgley, A. R. Jr., and Reichert, L. E., 1977, Regulation of gonadotropin receptors by LH in granulosa cells, Endocrinology 101:512.PubMedCrossRefGoogle Scholar
  70. Rodbell, M., Krans, H. M. J., Pohl, S. L., and Birnbaumer, L., 1971a, The glucagon-sensitive adenyl cyclase system in plasma membranes of rat liver. IV. Effects of guanyl nucleotides on binding of 125I-glucagon, J. Biol. Chem. 246:1872.PubMedGoogle Scholar
  71. Rodbell, M., Birnbaumer, L., Pohl, S. L., and Krans, H. M. J., 1971b, The glucagon-sensitive adenyl cyclase system in plasma membranes of rat liver. V. An obligatory role of guanylnucleotides in glucagon action, J. Biol. Chem. 246:1877.PubMedGoogle Scholar
  72. Rodbell, M., Lin, M. C., and Salomon, Y., 1974, Evidence for interdependent action of glucagon and nucleotides on the hepatic adenylate cyclase system, J. Biol. Chem. 249:59.PubMedGoogle Scholar
  73. Ross, E. M., and Gilman, A. G., 1977, Resolution of some compon-ents of adenylate cyclase necessary for catalytic activity, J. Biol. Chem. 252:6966.PubMedGoogle Scholar
  74. Ross, E. M., Howlett, A. C., Fergusson, K. M., and Gilman, A. G., 1978, Reconstitution of hormone-sensitive adenylate cyclase activity with resolved components of the enzyme, J. Biol. Chem. 253:6401.PubMedGoogle Scholar
  75. Sharma, S. K., Klee, W. A., and Nirenberg, M., 1977, Opiatedependent modulation of adenylate cyclase, Proc. Natl. Acad. Sci. USA 74:3365.PubMedCrossRefGoogle Scholar
  76. Somkuti, S. G., Hildebrandt, J. D., Herberg, J. T., and Iyengar, R., 1982, Divalent cation regulation of adenylyl cyclase; an allosteroic site on the catalytic component, J. Biol. Chem. 257:6387.PubMedGoogle Scholar
  77. Sternweis, P. C., and Gilman, A. G., 1979, Reconstitution of chatecholamine-sensitive adenylate cyclase. Reconstitution of the uncoupled variant of S49 lymphoma cell, J. Biol. Chem. 254:3333.PubMedGoogle Scholar
  78. Sternweis, P. C., Northup, J. K., Smigel, M. D., and Gilman, A. G., 1981, The regulatory component of adenylate cyclase. Purification and properties, J. Biol. Chem. 256:11517.PubMedGoogle Scholar
  79. separated catalytic and regulatory units of brain adenylate cyclase, Proc. Natl. Acad. Sci. USA 77:6344.PubMedCrossRefGoogle Scholar
  80. Su, Y. F., Cubeddu, X. L., and Perkins, J. P., 1976, Regulation of adenosine 3’,5’-monophosphate content in human astrocytoma cells: desensitization to catecholamines and prostaglandins, J. Cycle. Nucleo. Res. 2L257,Google Scholar
  81. Su, Y. P., Harden, T. K., and Perkins, J. P., 1980, Catecholamine-specific desensitization of adenylate cyclase: evidence for multistep process, J. Biol. Chem. 255:7410.PubMedGoogle Scholar
  82. Suter, D. E., Fletcher, P. W., Sluss, P. M., Reichert, L. E. Jr., and Niswender, G. D., 1980, Alterations in the number of ovine luteal receptors for LH and progesterone secretion induced by homologous hormone, Biol. Repro. 22:205.CrossRefGoogle Scholar
  83. Sutherland, E. W., and Rall, T. W., 1962, Adenyl cyclase. I. Distribution, preparation and properties, J. Biol. Chem. 237:1220.PubMedGoogle Scholar
  84. Yamada, S., Yamamura, H., and Roeske, W. R., 1980, The regula-tion of cardiac alphax-adrenergic receptors by guanine nucleotides and muscarinic cholinergic agonists, Eur. J. Pharm. 63:239.CrossRefGoogle Scholar
  85. Wei, J. W., and Sulakhe, P. V., 1980, Requirement for sulfhydryl groups in the differential effects of magnesium ion and GTP on agonist binding of muscarinic cholinergic receptor sites in rat atrial membrane fraction, Naunym-Schmeideberg’s Arch Pharma. 314:51.CrossRefGoogle Scholar
  86. Williams, L. T., Mullikin, D., and Lefkowitz, R. J., 1978, Magnesium dependence of agonist binding to adenylate cyclase-coupled hormone receptors, J. Biol. Chem. 253:2984.PubMedGoogle Scholar
  87. Williams, L. T., Mullikin, D., and Lefkowitz, R. J., 1978, Magnesium dependence of agonist binding to adenylate cyclase-coupled hormone receptors, J. Biol. Chem. 253:2984. Birnbaumer, L., and Swartz, T., 1982, Membrane receptors: criteria and selected methods of study, in: “Laboratory Methods Manual for Hormone action and Molecular Endocrin-ology”, W. T. Schrader and B. W. O’Malley, eds., Chapter 3, Houston Biological Associates.Google Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Howard J. Kirchick
    • 1
  • Juan Codina
    • 1
  • John D. Hildebrandt
    • 1
  • Ravi Iyengar
    • 1
  • Francisco J. Rojas
    • 1
  • Joel Abramowitz
    • 2
  • Mary Hunzicker-Dunn
    • 3
  • Lutz Birnbaumer
    • 1
  1. 1.Department of Cell BiologyBaylor College of MedicineHoustonUSA
  2. 2.Department of ZoologyIowa State UniversityAmes, 10USA
  3. 3.Department of BiochemistryNorthwestern University School of MedicineChicagoUSA

Personalised recommendations