Skip to main content
SpringerLink
Log in

Expression of gLTP in Sympathetic Ganglia from Stress-hypertensive Rats: Molecular Evidence

  • Published:
Journal of Molecular Neuroscience Aims and scope Submit manuscript

Abstract

We previously reported behavioral and electrophysiological evidence indicating that superior cervical ganglia (SCG) from rats that developed hypertension as a result of chronic psychosocial stress expressed ganglionic long-term potentiation (gLTP) in vivo. In the present study, we present additional supportive evidence by measuring changes in protein levels of essential signaling molecules in ganglia from chronically stressed rats. We compared protein levels of essential, LTP-related signaling molecules in ganglia isolated from chronic stress-hypertensive rats, known to have expressed gLTP, with those of the same molecules in normal ganglia 1h after eliciting gLTP by high frequency stimulation (HFS) in vitro. Immunoblot analysis showed a significant increase in the levels of phosphorylated CaMKII, total CaMKII, nitric oxide synthase (NOS-1), and calmodulin in SCG from both chronically stressed rats and from normal rat ganglia in which gLTP was expressed by HFS in vitro. Additionally, there was a parallel reduction in calcineurin protein levels in ganglia from both groups. The present results confirm that ganglia from stressed rats have expressed gLTP in vivo and that synaptic plasticity in sympathetic ganglia may involve a molecular cascade largely similar to that of LTP in the hippocampal CA1 region.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alkadhi, K. A., & Altememi, G. F. (1997). Nitric oxide mediates long-term potentiation in rat superior cervical ganglion. Brain Research, 753, 315–317.

    Article  PubMed  CAS  Google Scholar 

  • Alkadhi, K. A., Salgado-Commissariat, D., Hogan, Y. H., & Akpaudo, S. B. (1996). Induction and maintenance of ganglionic long-term potentiation require activation of 5-hydroxytryptamine (5-HT3) receptors. Journal of Physiology, 496(Pt 2), 479–489.

    PubMed  CAS  Google Scholar 

  • Alkadhi, K. A., Al-Hijailan, R. S., Malik, K., & Hogan, Y. H. (2001a). Retrograde carbon monoxide is required for induction of long-term potentiation in rat superior cervical ganglion. Journal of Neuroscience, 21, 3515–3520.

    PubMed  CAS  Google Scholar 

  • Alkadhi, K. A., Otoom, S. A., Tanner, F. L., Sockwell, D., & Hogan, Y. H. (2001b). Inhibition of ganglionic long-term potentiation decreases blood pressure in spontaneously hypertensive rats. Experimental Biology and Medicine (Maywood), 226, 1024–1030.

    CAS  Google Scholar 

  • Alkadhi, K. A., Alzoubi, K. H., & Aleisa, A. M. (2005a). Plasticity of sympathetic transmission in autonomic ganglia. Progress in Neurobiology, 75, 83–108.

    Article  PubMed  CAS  Google Scholar 

  • Alkadhi, K. A., Alzoubi, K. H., Abdulaziz, A. M., Tanner, F. L., & Nimer, A. S. (2005b). Psychosocial stress-induced hypertension results from in vivo expression of long-term potentiation in sympathetic ganglia. Neurobiology of Disease, 20, 849–857.

    Article  PubMed  CAS  Google Scholar 

  • Alkadhi, K. A., & Alzoubi, K. H. (2007). Role of long-term potentiation of sympathetic ganglia (gLTP) in hypertension. Clinical and Experimental Hypertension, 29, 267–286.

    Article  PubMed  Google Scholar 

  • Alonso-deFlorida, F., Morales, M. A., & Minzoni, A. A. (1991). Modulated long-term potentiation in the cat superior cervical ganglion in vivo. Brain Research, 544, 203–210.

    Article  PubMed  CAS  Google Scholar 

  • Altememi, G. F., & Alkadhi, K. A. (1999). Nitric oxide is required for the maintenance but not initiation of ganglionic long-term potentiation. Neuroscience, 94, 897–902.

    Article  PubMed  CAS  Google Scholar 

  • Alzoubi, K. H., Aleisa, A. M., & Alkadhi, K. A. (2006). Molecular studies on the protective effect of nicotine in adult-onset hypothyroidism-induced impairment of long-term potentiation. Hippocampus, 16(10), 861–74.

    Article  PubMed  CAS  Google Scholar 

  • Bachoo, M., & Polosa, C. (1991). Long-term potentiation of nicotinic transmission by a heterosynaptic mechanism in the stellate ganglion of the cat. Journal of Neurophysiology, 65, 639–647.

    PubMed  CAS  Google Scholar 

  • Bachoo, M., & Polosa, C. (1992). Preganglionic axons from the third thoracic spinal segment fail to induce long-term potentiation in the superior cervical ganglion of the cat. Canadian Journal of Physiology and Pharmacology, 70(Suppl), S27–31.

    PubMed  Google Scholar 

  • Bachoo, M., Heppner, T., Fiekers, J., & Polosa, C. (1992). A role for protein kinase C in long term potentiation of nicotinic transmission in the superior cervical ganglion of the rat. Brain Research, 585, 299–302.

    Article  PubMed  CAS  Google Scholar 

  • Boone, J. L. (1991). Stress and hypertension. Primary Care, 18, 623–649.

    PubMed  CAS  Google Scholar 

  • Briggs, C. A., Brown, T. H., & McAfee, D. A. (1985). Neurophysiology and pharmacology of long-term potentiation in the rat sympathetic ganglion. Journal of Physiology, 359, 503–521.

    PubMed  CAS  Google Scholar 

  • Briggs, C. A., & McAfee, D. A. (1988). Long-term potentiation at nicotinic synapses in the rat superior cervical ganglion. Journal of Physiology, 404, 129–144.

    PubMed  CAS  Google Scholar 

  • Briggs, C. A., McAfee, D. A., & McCaman, R. E. (1988). Long-term regulation of synaptic acetylcholine release and nicotinic transmission: the role of cyclic AMP. British Journal of Pharmacology, 93, 399–411.

    PubMed  CAS  Google Scholar 

  • Brown, T. H., & McAfee, D. A. (1982). Long-term synaptic potentiation in the superior cervical ganglion. Science, 215, 1411–1413.

    Article  PubMed  CAS  Google Scholar 

  • Cetiner, M., & Bennett, M. R. (1993). Nitric oxide modulation of calcium-activated potassium channels in postganglionic neurones of avian cultured ciliary ganglia. British Journal of Pharmacology, 110, 995–1002.

    PubMed  CAS  Google Scholar 

  • Dore, S., Takahashi, M., Ferris, C. D., Zakhary, R., Hester, L. D., Guastella, D., & Snyder, S. H. (1999). Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proceedings of the National Academy of Sciences of the United States of America, 96, 2445–2450.

    Article  PubMed  CAS  Google Scholar 

  • Esler, M., Julius, S., Zweifler, A., Randall, O., Harburg, E., Gardiner, H., et al. (1977). Mild high-renin essential hypertension. Neurogenic human hypertension? New England Journal of Medicine, 296, 405–411.

    PubMed  CAS  Google Scholar 

  • Gerges, N. Z., Stringer, J. L., & Alkadhi, K. A. (2001). Combination of hypothyroidism and stress abolishes early LTP in the CA1 but not dentate gyrus of hippocampus of adult rats. Brain Research, 922, 250–260.

    Article  PubMed  CAS  Google Scholar 

  • Gerges, N. Z., Aleisa, A. M., Alhaider, A. A., & Alkadhi, K. A. (2002). Reduction of elevated arterial blood pressure in obese Zucker rats by inhibition of ganglionic long-term potentiation. Neuropharmacology, 43, 1070–1076.

    Article  PubMed  CAS  Google Scholar 

  • Gerges, N. Z., Aleisa, A. M., Schwarz, L. A., & Alkadhi, K. A. (2003). Chronic psychosocial stress decreases calcineurin in the dentate gyrus: a possible mechanism for preservation of early ltp. Neuroscience, 117, 869–874.

    Article  PubMed  CAS  Google Scholar 

  • Gerges, N. Z., Aleisa, A. M., Schwarz, L. A., & Alkadhi, K. A. (2004). Reduced basal CaMKII levels in hippocampal CA1 region: possible cause of stress-induced impairment of LTP in chronically stressed rats. Hippocampus, 14, 402–410.

    Article  PubMed  CAS  Google Scholar 

  • Hadjiconstantinou, M., Potter, P. E., & Neff, N. H. (1982). Trans-synaptic modulation via muscarinic receptors of serotonin-containing small intensely fluorescent cells of superior cervical ganglion. Journal of Neuroscience, 2, 1836–1839.

    PubMed  CAS  Google Scholar 

  • Hanson, P. I., Kapiloff, M. S., Lou, L. L., Rosenfeld, M. G., & Schulman, H. (1989). Expression of a multifunctional Ca2+/calmodulin-dependent protein kinase and mutational analysis of its autoregulation. Neuron, 3, 59–70.

    Article  PubMed  CAS  Google Scholar 

  • Hogan, Y. H., Hawkins, R., & Alkadhi, K. A. (1998). Adenosine A1 receptor activation inhibits LTP in sympathetic ganglia. Brain Research, 807, 19–28.

    Article  PubMed  CAS  Google Scholar 

  • Johnston, D., & Wu, S. (1995). Foundations of cellular neurophysiology. Cambridge, MA: MIT Press.

    Google Scholar 

  • Kandel, E. R., & Hawkins, R. D. (1992). The biological basis of learning and individuality. Scientific American, 267, 78–86.

    PubMed  CAS  Google Scholar 

  • Hoyer, D., Waeber, C., Karpf, A., Neijt, H., Palacios, J. M. (1989). [3H]ICS 205-930 labels 5-HT3 recognition sites in membranes of cat and rabbit vagus nerve and superior cervical ganglion. Naunyn Schmiedebergs Archives of Pharmacology, 340(4), 78–86.

    Article  CAS  Google Scholar 

  • Lin, Y. Q., & Bennett, M. R. (1994). Nitric oxide modulation of quantal secretion in chick ciliary ganglia. Journal of Physiology, 481(Pt 2), 385–394.

    PubMed  CAS  Google Scholar 

  • Magee, J. C., & Schofield, G. G. (1992). Neurotransmission through sympathetic ganglia of spontaneously hypertensive rats. Hypertension, 20, 367–373.

    PubMed  CAS  Google Scholar 

  • Maurice, D. H., & Haslam, R. J. (1990). Molecular basis of the synergistic inhibition of platelet function by nitrovasodilators and activators of adenylate cyclase: Inhibition of cyclic AMP breakdown by cyclic GMP. Molecular Pharmacology, 37, 671–681.

    PubMed  CAS  Google Scholar 

  • McEwen, B. S. (1998). Protective and damaging effects of stress mediators. New England Journal of Medicine, 338, 171–179.

    Article  PubMed  CAS  Google Scholar 

  • Minota, S., Kumamoto, E., Kitakoga, O., & Kuba, K. (1991). Long-term potentiation induced by a sustained rise in the intraterminal Ca2+ in bull-frog sympathetic ganglia. Journal of Physiology, 435, 421–438.

    PubMed  CAS  Google Scholar 

  • Morales, M. A., Bachoo, M., Collier, B., & Polosa, C. (1994). Pre- and postsynaptic components of nicotinic long-term potentiation in the superior cervical ganglion of the cat. Journal of Neurophysiology, 72, 819–824.

    PubMed  CAS  Google Scholar 

  • Morales, M., Wang, S. D. (2002). Differential composition of 5-hydroxytryptamine3 receptors synthesized in the rat CNS and peripheral nervous system. Journal of Neuroscience, 22, 6732–6741.

    PubMed  CAS  Google Scholar 

  • Nichols, R. A., & Mollard, P. (1996). Direct observation of serotonin 5-HT3 receptor-induced increases in calcium levels in individual brain nerve terminals. Journal of Neurochemistry, 67, 581–592.

    Article  PubMed  CAS  Google Scholar 

  • Pettit, D. L., Perlman, S., & Malinow, R. (1994). Potentiated transmission and prevention of further LTP by increased CaMKII activity in postsynaptic hippocampal slice neurons. Science, 266, 1881–1885.

    Article  PubMed  CAS  Google Scholar 

  • Scott, T. R., & Bennett, M. R. (1993a). The effect of nitric oxide on the efficacy of synaptic transmission through the chick ciliary ganglion. British Journal of Pharmacology, 110, 627–632.

    PubMed  CAS  Google Scholar 

  • Scott, T. R., & Bennett, M. R. (1993b). The effect of ions and second messengers on long-term potentiation of chemical transmission in avian ciliary ganglia. British Journal of Pharmacology, 110, 461–469.

    PubMed  CAS  Google Scholar 

  • Sheng, H., Gagne, G. D., Matsumoto, T., Miller, M. F., Forstermann, U., & Murad, F. (1993). Nitric oxide synthase in bovine superior cervical ganglion. Journal of Neurochemistry, 61, 1120–1126.

    Article  PubMed  CAS  Google Scholar 

  • Siegrist, J. (2001). [Psychosocial factors influencing development and course of coronary heart disease]. Herz, 26, 316–325.

    Article  PubMed  CAS  Google Scholar 

  • Szilagyi, J. E. (1991). Psychosocial stress elevates blood pressure via an opioid dependent mechanism in normotensive rats. Clinical and Experimental Hypertension Part A, 13, 1383–1394.

    Article  CAS  Google Scholar 

  • Wang, J. H., & Kelly, P. T. (1995). Postsynaptic injection of CA2+/CaM induces synaptic potentiation requiring CaMKII and PKC activity. Neuron, 15, 443–452.

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

Support is contributed by a grant (0255402Y) from AHA-Texas Affiliate.

Author information

Authors and Affiliations

  1. Department of Clinical Pharmacy, College of Pharmacy, Jordan University of Science and Technology, Irbid, Jordan

    K. H. Alzoubi

  2. College of Pharmacy, King Saud University, Riyadh, Saudi Arabia

    A. M. Aleisa

  3. Department of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX, 77204-5515, USA

    K. A. Alkadhi

Authors
  1. K. H. Alzoubi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. M. Aleisa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. A. Alkadhi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. A. Alkadhi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alzoubi, K.H., Aleisa, A.M. & Alkadhi, K.A. Expression of gLTP in Sympathetic Ganglia from Stress-hypertensive Rats: Molecular Evidence. J Mol Neurosci 35, 201–209 (2008). https://doi.org/10.1007/s12031-008-9054-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12031-008-9054-x

Keywords

Search

Navigation