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The “syncytial tissue triad”: a model for understanding how gap junctions participate in the local control of penile erection

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Summary

Recent findings from both clinical and experimental studies document the importance of syncytial relaxation and contraction of corporal smooth muscle to penile erection and detumescence, respectively. However, the mechanism(s) permitting coordinated response generation among the vast array of largely inexcitable corporal smooth muscle cells is unclear. In this report the compelling evidence for a major role of intercellular communication through gap junctions to erectile function is reviewed. Moreover, a novel concept is advanced to explain more fully the putative mechanistic basis for integrative erectile tissue biology. Specifically, the presence of gap junctions; in concert with the autonomic nervous system and myogenic intracellular signal transduction mechanisms, is postulated to form a “syncytial tissue triad” that is largely responsible for the local modulation of corporal smooth muscle tone. It is reasonable to assume that the existence of this “syncytial tissue triad” confers a plasticity, adaptability, and flexibility to erectile function that may well account for the observed diversity of mechanisms known to regulate penile erection as well as the multifaceted etiology of erectile dysfunction.

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References

  1. Anderson KE, Wagner G (1995) Physiology of penile erection. Physiol Rev 75: 191–236

    Google Scholar 

  2. Barr L, Dewey MM (1962) Intercellular connection between smooth muscle cells: the nexus. Science 137: 670–672

    Google Scholar 

  3. Barr L, Berger W, Dewey MM (1968) Electrical transmission at the nexus between smooth muscle cells. J Gen Physiol 52: 347–368

    Google Scholar 

  4. Bennett MVL, Barrio L, Bargiello TA, Spray DC, Hertzberg EL, Saez JL (1991) Gap junctions: new tools, new answers, new questions. Neuron 6: 305–320

    PubMed  Google Scholar 

  5. Beny J-L, Pacicca C (1994) Bidirectional electrical communication between smooth muscle and endothelial cells in the pig coronary artery. Am J Physiol 266: H1465-H1472

    PubMed  Google Scholar 

  6. Brink PR, Ramanan SV (1985) A model for the diffusion of flourescent probes in the septate giant axon of earthworm. Biophys J 48: 299–309

    PubMed  Google Scholar 

  7. Brink PR, Ramanan SV, Christ GJ (1996) Human connexin43 gap junction channel gating: evidence for mode shifts and/or heterogeneity. Am J Physiol 271: C321-C331

    PubMed  Google Scholar 

  8. Burnstock G, Relevic V (1993) Neural-endothelial interactions in the control of local vascular tone. R.G. Landes, Austin, Texas

    Google Scholar 

  9. Campos de Carvalho AC, Moreno AP, Christ GJ, Melman A, Roy C, Hertzberg EL, Spray DC (1993) Gap junctions formed of connexin43 interconnect smooth muscle cells of the human corpus cavernosum. J Urol 149: 1568–1575

    PubMed  Google Scholar 

  10. Carrier S, Brock G, Kour KW, Lue TF (1993) Pathophysiology of erectile dysfunction. Urology 42: 468–481

    PubMed  Google Scholar 

  11. Christ GJ (1995) Modulation of α1-adrenergic contractility in isolated vascular tissues by heptanol: a functional demonstration of the potential importance of intercellular communication to vascular response generation. Life Sci 56: 709–721

    PubMed  Google Scholar 

  12. Christ GJ (1995) The penis as a vascular organ: the importance of corporal smooth muscle tone in the control of penile erection. Urol Clin North Am 22: 727–745

    PubMed  Google Scholar 

  13. Christ GJ, Rehman J (1996) Neurophysiology. In: Krane RJ, Siroky MB, Goldstein I (eds) Male sexual dysfunction. Churchill Livingstone, London (in press)

    Google Scholar 

  14. Christ GJ, Maayani S, Valcic M, Melman A (1990) Pharmacological studies of human erectile tissue: characteristics of spontaneous contractions and alterations in alpha-adrenoceptor responsiveness with age and disease in isolated tissues. Br J Pharmacol 10: 375–381

    Google Scholar 

  15. Christ GJ, Moreno A, Parker ME, Gondre CM, Valcic M, Melman A, Spray DC (1991) Intercellular communication through gap junctions: a potential role in pharmacomechanical coupling and syncytial tissue contraction in vascular smooth muscle isolated from the human corpus cavernosum. Life Sci 49: PL195-PL200

    PubMed  Google Scholar 

  16. Christ GJ, Spray DC, Brink PR (1991) Characterization of K currents in cultured human corporal smooth muscle cells. J Androl 14: 319–328

    Google Scholar 

  17. Christ GJ, Moreno AP, Melman A, Spray DC (1992) Gap junction-mediated intercellular diffusion of Ca2+ in cultured human corporal smooth muscle cells. Am J Physiol 263: C373-C383

    PubMed  Google Scholar 

  18. Christ GJ, Zhao W, Moss J, Gondre CM, Roy C, Brink PR, Spray DC (1993) Gap junctions modulate tissue contractility andα 1-adrenergic agonist efficacy in isolated rat aorta. J Pharmacol Exp Ther 266: 1054–1065

    PubMed  Google Scholar 

  19. Christ GJ, Brink PR, Melman A, Spray DC (1993) The role of gap junctions and ion channels in the modulation of electrical and chemical signals in human corpus cavernosum smooth muscle. Int J Impotence Res 5: 77–96

    Google Scholar 

  20. Christ GJ, Brink PR, Ramanan SV (1994) Dynamic gap functional communication: a delimiting model for tissue responses. Biophys J 67: 1335–1344

    PubMed  Google Scholar 

  21. Christ GJ, Brink PR, Ramanan SV (1995) The impact of innervation density on syncytial responses in tissues containing gap junctions (abstract). FASEB J 9: A913

    Google Scholar 

  22. Christ GJ, Brink PR, Ramanan SV (1996) Neuronal innervation, signal transduction and erection. J Urol 155:620A

    Google Scholar 

  23. Christ GJ, Spektor M, Gondre CM, Wen YP, Valcic M, Serels S, Rosenbaum S (1996) Pharmacomechanical coupling, signal transduction and intercellular communication in human vascular smooth muscle (abstract). FASEB J 10: A69

    Google Scholar 

  24. Christ GJ, Spray DC, El-Sabban M, Moore L, Brink PR (1996) Gap junctions in vascular tissues: evaluating the role of intercellular communication to the modulation of vasomotor tone. Circ Res 79: 631–646

    PubMed  Google Scholar 

  25. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ (1990) Glutamate induces calcium waves in cultured astrocytes: long range glial signalling. Science 247: 470–473

    PubMed  Google Scholar 

  26. Dermietzel R, Kessler JA, Hertzberg EL, Spray DC (1991) Gap junctions between cultured astrocytes: immunocytochemical, molecular and electrophysiological analysis. J Neurosci 11: 1421–1432

    PubMed  Google Scholar 

  27. Fan SF, Brink PR, Melman A, Christ GJ (1995) An analysis of the maxi-K+ (Kca) channel in cultured human corporal smooth muscle cells. J Urol 153: 818–825

    PubMed  Google Scholar 

  28. Ganon F, Msghina M, Stjarne L (1993) Kinetics of noradrenaline released by sympathetic nerves. Neuroscience 56: 535–538

    PubMed  Google Scholar 

  29. Gibbins IL, Morris JL, Furness JB, Costa M (1988) Innervation of systemic blood vessels. In: Burnstock G, Griffith SG (eds) Nonadrenergic innervation of blood vessels. CRC, Boca Raton, pp 2–36

    Google Scholar 

  30. Giuliano F, Rampin O, Benoit G, Jardin A (1995) Neural control of penile erection. Urol Clin North Am 22: 747–766

    PubMed  Google Scholar 

  31. Goldstein I (1994) Editorial: impotence. J Urol 151: 1533

    PubMed  Google Scholar 

  32. Hall JE, Zampighi GA, Davis RM (eds) (1993) Gap junctions. (Progress in cell research series, vol 3) Elsevier, Amsterdam

    Google Scholar 

  33. Hermsmeyer K (1973) Multiple pacemaker sites in spontaneously active vascular muscle. Circul Res 33: 244–251

    Google Scholar 

  34. Hirst GDS, Edwards FR (1989) Sympathetic neuroeffector transmission in arteries and arterioles. Physiol Rev 69: 546–604

    PubMed  Google Scholar 

  35. Holman ME, Neild TO, Lang RJ (1990) On the passive properties of smooth muscle. In: Sperelakis N, Wood JD (eds) Frontiers in smooth muscle research. Wiley-Liss, New York, pp 379–398

    Google Scholar 

  36. Johansson B, Ljung B (1967) Spread of excitation in the smooth muscle of the rat portal vein. Acta Physiol Scand 70: 312–322

    PubMed  Google Scholar 

  37. Johansson B, Ljung B (1968) Role of myogenic propagation in vascular smooth muscle response to vasomotor nerve stimulation. Acta Physiol Scand 73: 501–510

    PubMed  Google Scholar 

  38. Johansson B, Somlyo AP (1980) Electrophysiological and excitation-contraction coupling. In: Bohr DF, Somlyo AP, Sparks HV (eds) Handbook of physiology, section 2. The cardiovascular system. Williams & Wilkins, Baltimore, pp 301–323

    Google Scholar 

  39. Kenakin T (1994) Pharmacologic analysis of drug receptor interaction, 2nd edn. Raven, New York, pp 118–136

    Google Scholar 

  40. Lerner SE, Melman A, Christ GJ (1993) A review of erectile dysfunction: new insights and more questions. J Urol 149: 1246–1255

    PubMed  Google Scholar 

  41. Lue TF (1994) Erectile dysfunction associated with cavernous and neurological disorders (editorial). J Urol 151: 890

    PubMed  Google Scholar 

  42. Meyer J-U, Lindbom L, Intaglietta M (1987) Coordinated diameter oscillations at arteriolar bifurcations in skeletal muscle. Am J Physiol 253: H568-H573

    PubMed  Google Scholar 

  43. Moreno AP, Campos de Carvalho AC, Christ GJ, Spray DC (1993) Gap junctional communication between human corpus cavernosum smooth muscle cells in culture: gating behavior and single channel events. Am J Physiol 264: C80-C92

    PubMed  Google Scholar 

  44. Rehman J, Melman A, Brink PR, Grine B, Walcott B, Christ GJ (1996) Neurogenic- but not pharmacologic-induced erections are significantly altered by 3 months of experimental diabetes (abstract). FASEB J 10: A64

    Google Scholar 

  45. Segal SS, Duling BR (1986) Flow control among microvessels coordinated by intercellular conduction. Science 234: 868–870

    PubMed  Google Scholar 

  46. Sneyd J, Charles AC, Sanderson MC (1994) A model for the propagation of intercellular calcium waves. Am J Physiol 266: C293-C302

    PubMed  Google Scholar 

  47. Tomita T (1990) Spread of excitation in smooth muscle. In: Sperelakis N, Wood JD (eds) Frontiers in smooth muscle research. Wiley-Liss, New York, pp 361–373

    Google Scholar 

  48. Xia J, Duling BR (1995) Electromechanical coupling and the conducted vasomotor response. Am J Physiol 269: H2022-H2030

    PubMed  Google Scholar 

  49. Xia J, Duling BR (1995) Cellular pathways of the conducted electrical response in arterioles of hamster cheek pouch in vitro. Am J Physiol 269: H2031-H2038

    PubMed  Google Scholar 

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Christ, G.J. The “syncytial tissue triad”: a model for understanding how gap junctions participate in the local control of penile erection. World J Urol 15, 36–44 (1997). https://doi.org/10.1007/BF01275155

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