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Horm Metab Res 2005; 37(4): 198-204
DOI: 10.1055/s-2005-861414
Original Basic
© Georg Thieme Verlag KG Stuttgart · New York

Isoproterenol Opens K+ ATP Channels via a β2-Adrenoceptor-linked Mechanism in Sertoli Cells from Immature Rats

A.  P.  Jacobus1 , D.  O.  Rodrigues1 , P.  F.  Borba1 , E.  S.  Loss1 , G.  F.  Wassermann1
  • 1Departamento de Fisiologia ICBS, UFRGS, Porto Alegre, Brazil
Further Information

Publication History

Received 4 August 2004

Accepted after revision 3 November 2004

Publication Date:
13 June 2005 (online)

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Abstract

In the present study, we investigated the mechanism by which isoproterenol hyperpolarises membrane potential (MP) in Sertoli cells from seminiferous tubules of 15-day-old rat testes. Modification of MP and resistance (R0) was analysed using conventional intracellular glass microelectrodes. Isoproterenol (2 × 10 - 6 M) induced an immediate and significant hyperpolarisation in the Sertoli-cell membrane. The β2-AR antagonist, butoxamine (1 × 10 -6 M), nullified isoproterenol action. The effect of the β1 antagonist, metoprolol (1×10 - 6 M), was light and non-significant. Sulphonylurea glibenclamide inhibition of the K+ ATP channels suppressed isoproterenol action, and testosterone, while depolarising Sertoli-cell MP closing the K+ ATP channels through the PLC/PIP2 pathway, reduced β-AR agonist-induced hyperpolarisation. Also, polycations LaCl3 and spermine reversed isoproterenol’s hyperpolarisation effect, probably depolarising the membrane potential through ionic interaction neutralising the action of isoproterenol on K+ ATP channels. Adenylate cyclase agonist forskolin (0.1 µM) rapidly hyperpolarised Sertoli-cell MP, mimicking the isoproterenol effect. These effects indicate that isoproterenol’s action on K+ ATP channel probably involves the known signalling cascade β-AR/Gs/AC/cAMP/PKA. These results suggest that the isoproterenol-induced hyperpolarisation is mediated by the opening of K+ ATP channels in Sertoli cells. This β-adrenergic hyperpolarisation might play a physiological role in the modulation of MP.

Key words

Isoproterenol - K+ ATP channels - Sertoli cells - β2-Adrenoceptor - Membrane potential

References

  • 1 Setchell B P, Maddocks S, Brooks D E. Anatomy, vasculature, innervation, and fluids of the male reproductive tract. In: Knobil E, Neill JD (eds) The Physiology of Reproduction, 2nd ed. Raven Press New York; 1994: 1063-1175
    Google Scholar
  • 2 Campos M B, Vitale M L, Ritta M N, Chioccio S R, Calandra R S. Catecholamine distribution in adult rat testis.  Andrologia. 1990;  22 247-250
    PubMedGoogle Scholar
  • 3 Rauchenwald M, Steers W D, Desjardins C. Efferent innervation of the rat testis.  Biol Reprod. 1995;  52 1136-1143
    PubMedGoogle Scholar
  • 4 Zieher L M, Debeljuk L, Iturriza F, Mancini R E. Biogenic Amine Concentration in testes of rats at different ages.  Endocrinology. 1971;  88 351-354
    PubMedGoogle Scholar
  • 5 Verhoven G, Dierickx P, de Moor P. Stimulation effect of neurotransmitters on the aromatization of testosterone by Sertoli cell-enriched cultures.  Mol Cell Endocrinol. 1979;  13 241-253
    CrossrefPubMedGoogle Scholar
  • 6 Attramadal H, Le Gac F, Jahnsen T, Hansson V. β-Adrenergic regulation of Sertoli cell adenylyl cyclase: desensitization by homologous hormone.  Mol Cell Endocrinol. 1983;  34 1-6
    PubMedGoogle Scholar
  • 7 Troispoux C, Reiter E, Combarnous Y, Guillou F. β2 adrenergic receptors mediate cAMP, tissue-type plasminogen activator and transferrin production in rat Sertoli cells.  Mol Cell Endocrinol. 1998;  142 75-86
    CrossrefPubMedGoogle Scholar
  • 8 Heindel J J, Steinberger A, Strada S J. Identification and characterization of a β1-adrenergic receptor in Sertoli cell.  Mol Cell Endocrinol. 1981;  22 349-358
    CrossrefPubMedGoogle Scholar
  • 9 Eikvar L, Bjornerheim R, Attramadal H, Hansson V. β-Adrenoceptor mediated responses and subtypes of β-adrenoceptor in cultured rat Sertoli cells.  J Steroid Biochem Molec Biol. 1993;  1 85-91
    PubMedGoogle Scholar
  • 10 Wassermann G F, Ludwig M S, Barreto K P. β-adrenergic stimulation of amino acid transport in Sertoli cell-enriched testes of rats is independent of its action on protein synthesis.  Med Sci Res. 1996;  24 149-151
    PubMedGoogle Scholar
  • 11 Tolszczuk M, Follea N, Pelletier G. Characterization and localization of β-adrenergic receptors in control and cryptorchidized rat testis by in vitro autoradiography.  J Androl. 1988;  3 172-177
    PubMedGoogle Scholar
  • 12 Verhoeven G, Cailleau J, de Moor P. Desensitization of cultures rat Sertoli cells by follicle-stimulating hormone and by L-isoproterenol.  Mol Cell Endocrinol. 1980;  20 113-126
    CrossrefPubMedGoogle Scholar
  • 13 Laurent-Cardonet V, Guillou F, Combarnous Y. Heterologous and homologous desensitization of the plasminogen activator response of rat Sertoli cells by FSH and isoproterenol.  Endocrinol J. 1994;  2 805-812
    PubMedGoogle Scholar
  • 14 Loss E S, Barreto K P, Leite L, Wassermann G F. Comparative study of the actions of isoproterenol and retinol on amino acid accumulation, 45Ca2+ uptake and membrane potential in Sertoli cells.  Med Sci Res. 1998;  26 195-199
    PubMedGoogle Scholar
  • 15 Nakashima M, Vanhoutte P M. Isoproterenol causes hyperpolarisation through opening of ATP-sensitive potassium channels in vascular smooth muscle of the canine saphenous vein.  J Pharmacol Exp Ther. 1995;  272 379-384
    PubMedGoogle Scholar
  • 16 Fujii K, Onaka U, Goto K, Abe I, Fujishima M. Impaired isoproterenol induced hyperpolarisation in isolated mesenteric arteries of aged rats.  Hypertension. 1999;  34 222-228
    PubMedGoogle Scholar
  • 17 von Ledebur E ICF, Almeida J P, Loss E S, Wassermann G F. Rapid effect of testosterone on rat Sertoli-cell membrane potential. Relationship with K+ ATP channels.  Horm Metab Res. 2002;  34 550-555
    Article in Thieme ConnectPubMedGoogle Scholar
  • 18 Loss E S, Jacobsen M, Costa Z SM, Jacobus A P, Borelli F, Wassermann G F. Testosterone modulates K+ ATP channels in Sertoli-cell membrane by PLC-PIP2 pathway.  Horm Metab Res. 2004;  36 519-525
    Article in Thieme ConnectPubMedGoogle Scholar
  • 19 Wassermann G F, Loss E S. Testosterone action on the Sertoli-cell membrane: A Kir6.x channel related effect.  Curr Pharm Design. 2004;  10 2649-2656
    PubMedGoogle Scholar
  • 20 Wassermann G F, Monti Bloch L, Grillo M L, Silva F RMB, Loss E S, McConnell L L. Electrophysiological changes of Sertoli cells produced by the acute administration of amino acid and FSH.  Horm Metab Res. 1992;  24 326-328
    Article in Thieme ConnectPubMedGoogle Scholar
  • 21 Baukrowitz T, Fakler B. KATP channels gated by intracellular nucleotides and phospholipids.  Eur J Biochem. 2000;  267 5842-5848
    CrossrefPubMedGoogle Scholar
  • 22 Deutsch N, Matsuoka S, Weiss J N. Surface charge and properties of cardiac ATP-sensitive K+ channels.  J Gen Physiol. 1994;  104 773-800
    CrossrefPubMedGoogle Scholar
  • 23 Jo S H, Leblais V, Wang P H, Crow M T, Xiao R P. Phosphatidylinositol 3-kinase functionally compartimentalized the concurrent Gs signaling during β2-adrenergic stimulation.  Circ Res. 2002;  91 46-56
    CrossrefPubMedGoogle Scholar
  • 24 Xiao R P, Zhang S J, Chakir K, Avdonin P, Zhu W, Bond R A. et al . Enhanced Gi signaling selectively negates β2-adrenergic receptor (AR)- but not β1-AR-mediated positive inotropic effect in myocytes from failing rat hearts.  Circulation. 2003;  108 1633-1639
    CrossrefPubMedGoogle Scholar
  • 25 Xiao R P, Cheng H, Zhou Y Y, Kuschel M, Lakatta E G. Recent Advances in Cardiac β2-adrenergic signal transduction.  Circ. Res.. 1999;  85 1092-1100
    PubMedGoogle Scholar
  • 26 Komori K, Flavahan N A, Miller V M, Vanhoutte P M. Electrophysiological analysis of adrenergic neurotransmission and its modulation by chronic denervation in canine saphenous veins.  J Pharmacol Exp Ther. 1990;  252 1197-1201
    PubMedGoogle Scholar
  • 27 Miyoshi H, Nakaya Y. Activation of ATP-sensitive K+ channels by cyclic AMP-dependent protein kinase in cultured smooth muscle cells of porcine coronary artery.  Biochem Biophys Res Commun. 1993;  193 240-247
    CrossrefPubMedGoogle Scholar
  • 28 Marinissen M J, Gutkind J S. G-protein-coupled receptors and signaling networks: emerging paradigms.  TRENDS Pharmacol Sci. 2001;  22 368-376
    CrossrefPubMedGoogle Scholar
  • 29 Meroni S B, Riera M F, Pellizzari E H, Galardo M N, Cigorraga S B. FSH activates phosphatidylinositol 3-kinase/protein kinase B signaling pathway in 20-day-old Sertoli cells independently of IGF-I.  J Endocrinol. 2004;  180 257-265
    CrossrefPubMedGoogle Scholar
  • 30 Cunnigham M A, Zhu Q, Unterman T G, Hammond J M. Follicle-stimulating hormone promotes nuclear exclusion of the forkhead transcription factor fox01a via phosphatidylinositol 3-kinase in porcine granulosa cell.  Endocrinol. 2003;  144 5585-5594
    CrossrefPubMedGoogle Scholar
  • 31 Babu P S, Krishnamurthy H, Chedrese P J. Activation of extracellular-regulated kinase pathway in ovarian granulosa cells by the novel growth factor type 1 follicle-stimulating hormone receptor.  J Biol Chem. 2000;  275 27 615-27 626
    PubMedGoogle Scholar
  • 32 Wassermann G F, Monti Bloch L, McConnell L L, Grillo M L. FSH-induced rapid hyperpolarization followed by a Ca2+-channel mediated depolarization in rat Sertoli cells.  Med Sci Res. 1990;  18 175-176
    PubMedGoogle Scholar
  • 33 Silva F RMB, Leite L D, Wassermann G F. Rapid signal transduction in Sertoli cells.  Eur J Endocrinol. 2002;  147 425-433
    CrossrefPubMedGoogle Scholar
  • 34 Grasso P, Reichert L E Jr. Follicle-stimulating hormone receptor- mediated uptake of 45Ca2+ by proteoliposomes and cultured rat Sertoli cells: evidence for involvement of voltage-activated and voltage-independent calcium channels.  Endocrinol. 1989;  125 3029-3036
    PubMedGoogle Scholar
  • 35 Grasso P, Reichert L E Jr. Follicle-stimulating hormone receptor-mediated uptake of 45Ca2+ by cultured rat Sertoli cells does not require activation of cholera toxin- or pertussis toxin-sensitive guanine nucleotide binding proteins or adenylate cyclase.  Endocrinol. 1990;  127 949-956
    PubMedGoogle Scholar
  • 36 Sharma O P, Flores J A, Leong D A, Velhuis J D. Cellular basis for follicle-stimulating hormone-stimulation in single rat Sertoli cells: possible dissociation from effects of adenosine 3',5'-monophosphate.  Endocrinology. 1994;  134 1915-1923
    CrossrefPubMedGoogle Scholar
  • 37 Irusta O, Wassermann G F. Factors influencing the uptake of [α-14C] aminoisobutyric acid by rat testes.  J Endocrinol. 1974;  60 463-471
    PubMedGoogle Scholar
  • 38 Spritzer P M, Wassermann G F. Amino acid uptake and protein synthesis in rat testes: stimulation by dissociable factors.  Horm Metabol Res. 1985;  17 237-240
    PubMedGoogle Scholar
  • 39 Wassermann G F, Monti Bloch L, Grillo M L, Silva F RMB, Loss E S, McConnell L L. Biochemical factors involved in the FSH action on amino acid transport in immature rat testes.  Horm Metab Res. 1992;  24 276-279
    PubMedGoogle Scholar
  • 40 Touyz R M, Jiang L, Sairam M R. Follicle-stimulating hormone mediated calcium signaling by the alternatively spliced growth factor type I receptor.  Biol Reprod. 2000;  62 1067-1074
    PubMedGoogle Scholar
  • 41 Babu P S, Danilovich N, Sairam M R. Hormone-induced receptor gene splicing: enhanced expression of the growth factor type I follicle-stimulating hormone receptor motif in the developing mouse ovary as a new paradigm in growth regulation.  Endocrinol. 2001;  142 381-389
    CrossrefPubMedGoogle Scholar
  • 42 Quirk S M, Reichert L E Jr. Regulation of the phosphoinositide pathway in cultured Sertoli cells from immature rats: effects of follicle-stimulating hormone and fluoride.  Endocrinol. 1988;  123 230-237
    PubMedGoogle Scholar
  • 43 Quinn K V, Cui Y, Giblin J P, Clap L H, Tinker A. Do anionic phospholipids serve as cofactors or second messengers for the regulation of activity of cloned ATP-sensitive K+ channels?.  Circ Res. 2003;  93 646-655
    CrossrefPubMedGoogle Scholar

G. F. Wassermann

Departamento de Fisiologia ICBS, UFRGS

Rua Sarmento Leite, 500 · CEP 90050-170 Porto Alegre · RS · Brazil

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Email: gwass@ufrgs.br

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