Acta Biologica Hungarica

, Volume 55, Issue 1–4, pp 143–148 | Cite as

Estradiol-Stimulated Nitric Oxide Release In Nervous Tissue, Vasculature, and Gonads of the Giant Cockroach Blaberus Craniifer

  • F. E. Nieto-FernandezEmail author
  • F. Ianuzzi
  • Adriana Ruiz
  • Lilian Nodimele


The vertebrate system of steroid hormones appears to have been conserved widely throughout the animal kingdom. The sex hormone estrogen, 17-β-estradiol (E2), long considered to be exclusively a vertebrate hormone, is found also in invertebrates related to reproductive and developmental processes such as spawning, vitellogenesis and molting. These processes are affected by estrogen induced changes at the genomic level and take place at a large time scale. The discovery of surface membrane receptors for E2 has opened new possibilities for the involvement of estrogen in biological functions other than reproductive. These processes take place within a few seconds to minutes and involve sudden cytosolic calcium transients, activation of adenylate cyclase or activation of phospholipase C (PLC). E2 can modulate the production of nitric oxide (NO) in endotheliar and other cells. A similar mechanism linking estrogen to cNOS catalized nitric oxide (NO) release is reported herein for the first time in several tissues of the giant cockroach Blaberus craniifer. This process has been identified in the brain, nerve cord, vasculature and ovaries. This effect is concentration dependent and is inhibited by tamoxifen an estrogen receptor blocker.


Estradiol estrogen receptors nitric oxide invertebrate insect 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Bidmon, H. J., Stumpf, W. E. (1991) Uptake, distribution and binding of vertebrate and invertebrate steroid hormones and time-dependence of ponasterone A. binding in Calliphora vicina. Comparisons among cholesterol, corticosterone, Cortisol, dexamethasone, 5 alpha-dihydrotestosterone, 1,25-dihy-droxyvitamin D3, ecdysone, estradiol-17 beta, ponasterone A., progesterone, and testosterone. Histochemistry 96, 419–434.CrossRefGoogle Scholar
  2. 2.
    Goetz, R. M., Thatte, H. S., Prabhakar, R., Cho, M. R., Michel, T., Golan, D. E. (1999) Estradiol induces the calcium-dependent translocation of endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. USA 96, 2788–2793.CrossRefGoogle Scholar
  3. 3.
    Gonzales, R. J., Kanagy N. L. (1999) Endothelium-independent relaxation of vascular smooth muscle by 17beta-estradiol. J. Cardiovasc. Pharmacol. Ther 4, 227–234.CrossRefGoogle Scholar
  4. 4.
    Gonzales, R. J., Walker, B. R., Kanagy, N. L. (2001) 17beta-estradiol increases nitric oxide-dependent dilation in rat pulmonary arteries and thoracic aorta. Am. J. Physiol. Lung Cell Mol. Physiol. 280, 555–564.CrossRefGoogle Scholar
  5. 5.
    Kelly, M. J., Levin, E. R. (2001) Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol. Metab. 12, 152–156.CrossRefGoogle Scholar
  6. 6.
    Keshan, B., Ray, A. K. (2000) Estradiol-17beta in Bombyx mori: possible significance and its effect on silk production. J. Insect. Physiol. 46, 1061–1068.CrossRefGoogle Scholar
  7. 7.
    Keshan, B., Ray, A. K. (2001) Effect of estradiol-17beta on cell area, lumen area and trehalase activity of posterior silk gland of Bombyx mori L. Indian J. Exp. Biol. 39, 1096–1102.PubMedGoogle Scholar
  8. 8.
    Keshan, B., Ray, A. K. (2001) The presence of estradiol-17beta and its specific binding sites in posterior silk gland of Bombyx mori. Gen. Comp. Endocrinol. 123, 23–30.Google Scholar
  9. 9.
    Kirkbride-Smith, A. E., Bell, H. A., Edwards, J. P. (2001) Effects of three vertebrate hormones on the growth, development, and reproduction of the tomato moth, Lacanobia oleracea L. (Lepidoptera: Noctuidae). Environ. Toxicol. Chem. 20, 1838–1845.CrossRefGoogle Scholar
  10. 10.
    Krukoff T. L., Khalili, P. (1997) Stress-induced activation of nitric oxide-producing neurons in the rat brain. J. Comp. Neurol. 377, 509–519.CrossRefGoogle Scholar
  11. 11.
    Levin, E. R. (2001) Cell localization, physiology, and nongenomic actions of estrogen receptors. J. Appl. Physiol. 91, 1860–1867.CrossRefGoogle Scholar
  12. 12.
    Levin, E. R. (2002) Cellular functions of plasma membrane estrogen receptors. Steroids 67, 471–475.CrossRefGoogle Scholar
  13. 13.
    Levin, E. R. (2003) Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Mo/. Endocrinol. 17, 309–317.Google Scholar
  14. 14.
    Ogiso, M., Ohnishi, E. (1986) Does estradiol play a. role in ovarian maturation or embryonic development of the silkworm? Gen. Comp. Endocrinol. 61, 82–86.Google Scholar
  15. 15.
    Pedram, A., Razandi, M., Aitkenhead, M., Hughes, C. C., Levin, E. R. (2002) Integration of the nongenomic and genomic actions of estrogen. Membrane-initiated signaling by steroid to transcription and cell biology. J. Biol. Chem. 277, 50768–50775.CrossRefGoogle Scholar
  16. 16.
    Prevot, V., Bouret, S., Stefano, G. B., Beauvillain, J. (2000) Median eminence nitric oxide signaling. Brain. Res. Rev. 34, 27–41.CrossRefGoogle Scholar
  17. 17.
    Prevot, V., Croix, D., Rialas, C. M., Poulain, P., Fricchione, G. L., Stefano, G. B., Beauvillain, J. C. (1999) Estradiol coupling to endothelial nitric oxide stimulates gonadotropin-releasing hormone release from rat median eminence via a. membrane receptor. Endocrinology 140, 652–659.CrossRefGoogle Scholar
  18. 18.
    Stefano, G. B., Cadet, P., Breton, C., Goumon, Y., Prevot, V., Dessaint, J. P., Beauvillain, J. C., Roumier, A. S., Welters, I., Salzet, M. (2000) Estradiol-stimulated nitric oxide release in human granulocytes is dependent on intracellular calcium transients: evidence of a. cell surface estrogen receptor. Blood 95, 3951–3958.CrossRefGoogle Scholar
  19. 19.
    Stefano, G. B., Cadet, P., Mantione, K., Cho, J. J., Jones, D., Zhu, W. (2003) Estrogen signaling at the cell surface coupled to nitric oxide release in Mytilus edulis nervous system. Endocrinology 144, 1234–1240.CrossRefGoogle Scholar
  20. 20.
    Stefano, G. B., Goumon, Y., Bilfmger, T. V., Welters, I. D., Cadet, P. (2000) Basal nitric oxide limits immune, nervous and cardiovascular excitation: human endothelia express a. mu opiate receptor. Prog. Neurobiol. 60, 513–530.CrossRefGoogle Scholar
  21. 21.
    Stefano, G. B., Prevot, V., Beauvillain, J. C., Cadet, P., Fimiani, C., Welters, I., Fricchione, G. L., Breton, C., Lassalle, P., Salzet, M., Bilfmger, T. V. (2000) Cell-surface estrogen receptors mediate calcium-dependent nitric oxide release in human endothelia. Circulation 101, 1594–1597.CrossRefGoogle Scholar
  22. 22.
    Stefano, G. B., Salzet, B., Rialas, C. M., Pope, M., Kustka, A., Neenan, K., Pryor, S., Salzet, M. (1997) Morphine- and anandamide-stimulated nitric oxide production inhibits presynaptic dopamine release. Brain Res. 763, 63–68.CrossRefGoogle Scholar
  23. 23.
    Swevers, L., Lambert, J. G., De Loof A. (1991) Synthesis and metabolism of vertebrate-type steroids by tissues of insects: a. critical evaluation. Experientia 47, 687–698.CrossRefGoogle Scholar
  24. 24.
    Tarrant, A. M., Atkinson, S., Atkinson, M. J. (1999) Estrone and estradiol-17 beta concentration in tissue of the scleractinian coral, Montipora verrucosa. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 122, 85–92.CrossRefGoogle Scholar
  25. 25.
    Warrier, S. R., Tirumalai, R., Subramoniam, T. (2001) Occurrence of vertebrate steroids, estradiol 17beta and progesterone in the reproducing females of the mud crab Scylla serrata. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 130, 283–294.CrossRefGoogle Scholar
  26. 26.
    Yocum, L. B., Denlinger, D. L., Katlic, N. E., Brueggemeier, R. W., Mechoulam, R. (1987) A. developmental profile of estrogen and androgen radioimmunoactive substances in the flesh fly, Sarcophaga crassipalpis. Insect Biochemistry 17, 1149–1153.CrossRefGoogle Scholar
  27. 27.
    You, H. J., Kim, J. Y., Jeong, H. G. (2003) 17 beta-estradiol increases inducible nitric oxide synthase expression in macrophages. Biochem. Biophys. Res. Commun. 303, 1129–1134.CrossRefGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2004

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • F. E. Nieto-Fernandez
    • 1
    Email author
  • F. Ianuzzi
    • 1
  • Adriana Ruiz
    • 1
  • Lilian Nodimele
    • 1
  1. 1.SUNY College at Old WestburyNeuroscience Research Institute (NRI)Old WestburyUSA

Personalised recommendations