Skip to main content
Log in

Agonistic Behavior of PACAP6-38 on Sensory Nerve Terminals and Cytotrophoblast Cells

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

Abstract

The effects of pituitary adenylate cyclase activating polypeptide (PACAP) are mediated through G-protein-coupled receptors, the specific PAC1 receptor and VPAC1 and VPAC2 receptors which bind vasoactive intestinal peptide with similar affinity. Based on binding affinity studies, PACAP6-38 was discovered as a potent antagonist of PAC1 and it has been used by hundreds of studies as a PACAP antagonist. Recently, we have found that in certain cells/tissues, PACAP6-38 does not antagonize PACAP-induced effects, but surprisingly, it exerts similar actions to PACAP1-38, behaving as an agonist. In the present study, we report on the agonistic behavior of PACAP6-38 on neuropeptide release from sensory nerves of the isolated rat trachea and on the MAPK signaling pathways in cytotrophoblast cells. In isolated rat tracheae, PACAP6-38, similarly to PACAP1-38, induced significant inhibitory effects on the release of three simultaneously measured sensory neuropeptides, substance P, calcitonin gene-related peptide, and somatostatin evoked by both chemical excitation and electrical field stimulation of capsaicin-sensitive afferents. Effects of PACAP6-38 were the same as those of PACAP1-38 on MAPK signaling in human cytotrophoblast cells. Western blot analysis showed that both peptide forms stimulated ERK1/2 and JNK phosphorylation, while they both inhibited p38 MAPK phosphorylation. The most pronounced effects were observed when both peptides were present. In summary, our results show that PACAP6-38, which is a PACAP receptor antagonist in most cells/tissues, can behave as an agonist in other systems. The increasing interest in the effects of PACAP requires further studies on the pharmacological properties of the peptide and its analogues.

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

Access this article

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

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • Abad, C., Gomariz, R. P., & Waschek, J. A. (2006). Neuropeptide mimetics and antagonists in the treatment of inflammatory disease: focus on VIP and PACAP. Current Topics in Medicinal Chemistry, 6, 151–163. doi:10.2174/156802606775270288.

    Article  PubMed  CAS  Google Scholar 

  • Alexandre, D., Vaudry, H., Grumolato, L., et al. (2002). Novel splice variants of type I pituitary adenylate cyclase activating polypeptide receptor in frog exhibit altered adenylate cyclase stimulation and differential relative abundance. Endocrinology, 143, 2680–2692. doi:10.1210/en.143.7.2680.

    Article  PubMed  CAS  Google Scholar 

  • Arimura, A. (1998). Perspectives on pituitary adenylate cyclase activating polypeptide (PACAP) in the neuroendocrine, endocrine, and nervous systems. Japanese Journal of Physiology, 48, 301–331. doi:10.2170/jjphysiol.48.301.

    Article  PubMed  CAS  Google Scholar 

  • Arimura, A. (2007). PACAP: The road to discovery. Peptides, 28, 1617–1619. doi:10.1016/j.peptides.2007.06.006.

    Article  PubMed  CAS  Google Scholar 

  • Beebe, X., Darczak, D., Davis-Taber, R. A., et al. (2008). Discovery and SAR of hydrazide antagonists of the pituitary adenylate cyclase activating polypeptide (PACAP) receptor type 1 (PAC1-R). Bioorganic & Medicinal Chemistry Letters, 18, 2162–2166. doi:10.1016/j.bmcl.2008.01.052.

    Article  CAS  Google Scholar 

  • Boronkai, A., Nemeth, J., Tamas, A., et al. (2007). Occurrence of PACAP in human placenta and its effects on MAP kinases in human trophoblast cells. Journal of Molecular Neuroscience, 33, 344.

    Google Scholar 

  • Bourgault, S., Vaudry, D., Botia, B., et al. (2008). Novel stable PACAP analogs with potent activity towards the PAC1 receptor. Peptides, 29, 919–932.

    Article  PubMed  CAS  Google Scholar 

  • Brenneman, D. E. (2007). Neuroprotection: A comparative view of vasoactive intestinal peptide and pituitary adenylate cyclase activating polypeptide. Peptides, 28, 1720–1726. doi:10.1016/j.peptides.2007.04.002.

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee, T. K., Sharma, R. V., & Fisher, R. A. (1996). Molecular cloning of a novel variant of the pituitary adenylate cyclase activating polypeptide (PACAP) receptor that stimulates calcium influx by activation of L-type calcium channels. Journal of Biological Chemistry, 271, 32226–32232. doi:10.1074/jbc.271.50.32226.

    Article  PubMed  CAS  Google Scholar 

  • Chen, Y. D., Zhou, Z. G., Wang, Z., et al. (2005). Pituitary adenylate cyclase activating peptide and its receptor antagonist in development of acute pancreatitis in rats. World Journal of Gastroenterology, 11, 538–544.

    PubMed  CAS  Google Scholar 

  • Daniel, P. B., Kieffer, T. J., Leech, C. A., & Habener, J. F. (2001). Novel alternatively spliced exon in the extracellular ligand-binding domain of the pituitary adenylate cyclase activating polypeptide (PACAP) type 1 receptor (PAC1R) selectively increases ligand affinity and alters signal transduction coupling during spermatogenesis. Journal of Biological Chemistry, 276, 12938–12944. doi:10.1074/jbc.M009941200.

    Article  PubMed  CAS  Google Scholar 

  • Desai, B. J., & Burrin, J. M. (1994). PACAP-38 positively regulates glycoprotein hormone alpha-gene expression in placental cells. Molecular and Cellular Endocrinology, 99, 31–37. doi:10.1016/0303-7207(94)90143-0.

    Article  PubMed  CAS  Google Scholar 

  • DiCicco-Bloom, E., Lu, N., Pintar, J. E., & Zhang, J. (1998). The PACAP ligand-receptor system regulates cerebral cortical neurogenesis. Annals of the New York Academy of Sciences, 865, 274–289. doi:10.1111/j.1749-6632.1998.tb11188.x.

    Article  PubMed  CAS  Google Scholar 

  • Ekblad, E. (1999). Pharmacological evidence for both neuronal and smooth muscular PAC1 receptors and a VIP-specific receptor in rat colon. Regulatory Peptides, 85, 87–92. doi:10.1016/S0167-0115(99)00080-4.

    Article  PubMed  CAS  Google Scholar 

  • Freson, K., Peeters, K., De Vos, R., et al. (2008). PACAP and its receptor VPAC1 regulate megakaryocyte maturation: Therapeutic implications. Blood, 111, 1885–1893. doi:10.1182/blood-2007-06-098558.

    Article  PubMed  CAS  Google Scholar 

  • Gasz, B., Racz, B., Roth, E., et al. (2006). PACAP inhibits oxidative stress-induced activation of MAP kinase dependent apoptotic pathway in cultured cardiomyocytes. Annals of the New York Academy of Sciences, 1070, 293–297. doi:10.1196/annals.1317.029.

    Article  PubMed  CAS  Google Scholar 

  • Gomariz, R. P., Juarranz, Y., Abad, C., Arranz, A., Leceta, J., & Martinez, C. (2006). VIP-PACAP system in immunity. New insights for multitarget therapy. Annals of the New York Academy of Sciences, 1070, 51–74. doi:10.1196/annals.1317.031.

    Article  PubMed  CAS  Google Scholar 

  • Helyes, Z., Nemeth, J., Pinter, E., & Szolcsanyi, J. (1997). Inhibition by nociceptin of neurogenic inflammation and the release of SP and CGRP from sensory nerve terminals. British Journal of Pharmacology, 121, 613–615. doi:10.1038/sj.bjp.0701209.

    Article  PubMed  CAS  Google Scholar 

  • Hernandez, M., Barahona, M. V., Recio, P., et al. (2004). Heterogeneity of neuronal and smooth muscle receptors involved in the VIP- and PACAP-induced relaxations of the pig intravesical ureter. British Journal of Pharmacology, 141, 123–131. doi:10.1038/sj.bjp.0705582.

    Article  PubMed  CAS  Google Scholar 

  • Hollosy, T., Jozsa, R., Jakab, B., Nemeth, J., Lengvari, I., & Reglodi, D. (2004). Effects of in ovo treatment with PACAP antagonist on general activity, motor and social behavior in chickens. Regulatory Peptides, 123, 99–106. doi:10.1016/j.regpep.2004.05.018.

    Article  PubMed  CAS  Google Scholar 

  • Ichinose, M., Asai, M., Imai, K., & Sawada, M. (1995). Enhancement of phagocytosis in mouse macrophages by pituitary adenylate cyclase activating polypeptide (PACAP) and related peptides. Immunopharmacology, 30, 217–224. doi:10.1016/0162-3109(95)00025-O.

    Article  PubMed  CAS  Google Scholar 

  • Jozsa, R., Hollosy, T., Tamas, A., Toth, G., Lengvari, I., & Reglodi, D. (2005). Pituitary adenylate cyclase activating polypeptide plays a role in olfactory memory formation in chicken. Peptides, 26, 2344–2350. doi:10.1016/j.peptides.2005.03.054.

    Article  PubMed  CAS  Google Scholar 

  • Kiss, P., Hauser, D., Tamas, A., Horvath, Z., Lengvari, I., & Reglodi, D. (2007). Effects of perinatal PACAP and PACAP antagonist treatment on novelty-seeking behavior in adolescent rats. Journal of Molecular Neuroscience, 33, 340.

    Google Scholar 

  • Koh, P. O., Won, C. K., Noh, H. S., Cho, G. J., & Choi, W. S. (2005). Expression of pituitary adenylate cyclase activating polypeptide and its type I receptor mRNAs in human placenta. Journal of Veterinary Science, 6, 1–5.

    PubMed  Google Scholar 

  • Laburthe, M., & Couvineau, A. (2002). Molecular pharmacology and structure of VPAC receptors for VIP and PACAP. Regulatory Peptides, 108, 165–173. doi:10.1016/S0167-0115(02)00099-X.

    Article  PubMed  CAS  Google Scholar 

  • Laburthe, M., Couvineau, A., & Tan, V. (2007). Class II G protein-coupled receptors for VIP and PACAP: Structure, models of activation and pharmacology. Peptides, 28, 1631–1639. doi:10.1016/j.peptides.2007.04.026.

    Article  PubMed  CAS  Google Scholar 

  • Le, S. V., Yamaguchi, D. J., McArdle, C. A., Tachiki, K., Pisegna, J. R., & Germano, P. (2002). PAC1 and PACAP expression, signaling, and effect on the growth of HCT8, human colonic tumor cells. Regulatory Peptides, 109, 115–125.

    Article  PubMed  CAS  Google Scholar 

  • Lelievre, V., Hu, Z., Byun, J. Y., Ioffe, Y., & Waschek, J. A. (2002). Fibroblast growth factor-2 converts PACAP growth action on embryonic hindbrain precursors from stimulation to inhibition. Journal of Neuroscience Research, 67, 566–573. doi:10.1002/jnr.10153.

    Article  PubMed  CAS  Google Scholar 

  • Li, M., Maderdrut, J. L., Lertora, J. J., & Batuman, V. (2007). Intravenous infusion of pituitary adenylate cyclase activating polypeptide (PACAP) in a patient with multiple myeloma and myeloma kidney: a case study. Peptides, 28, 1891–1895. doi:10.1016/j.peptides.2007.05.002.

    Article  PubMed  CAS  Google Scholar 

  • Lutz, E. M., MacKenzie, C. J., Johnson, M., et al. (1999). Domains determining agonist selectivity in chimaeric VIP2 (VPAC2)/PACAP (PAC1) receptors. British Journal of Pharmacology, 128, 934–940. doi:10.1038/sj.bjp.0702872.

    Article  PubMed  CAS  Google Scholar 

  • Lutz, E. M., Ronaldson, E., Shaw, P., Jonhson, M. S., Holland, P. J., & Mitchell, R. (2006). Characterization of novel splice variants of the PAC1 receptor in human neuroblastoma cells: Consequences for signaling by VIP and PACAP. Molecular and Cellular Neurosciences, 31, 193–209. doi:10.1016/j.mcn.2005.09.008.

    Article  PubMed  CAS  Google Scholar 

  • Lyu, R. M., Germano, P. M., Choi, J. K., Le, S. V., & Pisegna, J. R. (2000). Identification of an essential amino acid motif within the C terminus of the pituitary adenylate cyclase activating polypeptide type I receptor that is critical for signal transduction but not for receptor internalization. Journal of Biological Chemistry, 275, 36134–36142. doi:10.1074/jbc.M004612200.

    Article  PubMed  CAS  Google Scholar 

  • McDougall, J. J., & Barin, A. K. (2005). The role of joint nerves and mast cells in the alteration of vasoactive intestinal peptide (VIP) sensitivity during inflammation progression in rats. British Journal of Pharmacology, 145, 104–113. doi:10.1038/sj.bjp.0706169.

    Article  PubMed  CAS  Google Scholar 

  • Miyata, A., Arimura, A., Dahl, R. R., et al. (1989). Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochemical and Biophysical Research Communications, 164, 567–574. doi:10.1016/0006-291X(89)91757-9.

    Article  PubMed  CAS  Google Scholar 

  • Monaghan, T. K., MacKenzie, C. J., Plevin, R., & Lutz, E. M. (2008). PACAP-38 induces neuronal differentiation of human SH-SY5Y neuroblastoma cells via cAMP-mediated activation of ERK and p38 MAP kinases. Journal of Neurochemistry, 104, 74–88.

    PubMed  CAS  Google Scholar 

  • Muller, J. M., Debaigt, C., Goursaud, S., et al. (2007). Unconventional binding sites and receptors for VIP and related peptides PACAP and PHI/PHM: An update. Peptides, 28, 1655–1666. doi:10.1016/j.peptides.2007.04.006.

    Article  PubMed  CAS  Google Scholar 

  • Mustafa, T., Grimaldi, M., & Eiden, L. E. (2007). The hop cassette of the PAC1 receptor confers coupling to Ca2+ elevation required for pituitary adenylate cyclase activating polypeptide-evoked neurosecretion. Journal of Biological Chemistry, 282, 8079–8091. doi:10.1074/jbc.M609638200.

    Article  PubMed  CAS  Google Scholar 

  • Nemeth, J., Reglodi, D., Pozsgai, G., et al. (2006). Effect of PACAP-38 on sensory neuropeptide release and neurogenic inflammation in rats and mice. Neuroscience, 143, 223–230. doi:10.1016/j.neuroscience.2006.07.028.

    Article  PubMed  CAS  Google Scholar 

  • Nicot, A., & DiCicco-Bloom, E. (2001). Regulation of neuroblast mitosis is determined by PACAP receptor isoform expression. Proceedings of the National Academy of Sciences of the United States of America, 98, 4758–4763. doi:10.1073/pnas.071465398.

    Article  PubMed  CAS  Google Scholar 

  • Nielsen, K. M., Chaverra, M., Hapner, S. J., et al. (2004). PACAP promotes sensory neuron differentiation: Blockade by neurotrophic factors. Molecular and Cellular Neurosciences, 25, 629–641. doi:10.1016/j.mcn.2003.12.004.

    Article  PubMed  CAS  Google Scholar 

  • Ohno, F., Watanabe, J., Sekihara, S., et al. (2005). Pituitary adenylate cyclase activating polypeptide promotes differentiation of mouse neural stem cells into astrocytes. Regulatory Peptides, 126, 115–122. doi:10.1016/j.regpep.2004.08.028.

    Article  PubMed  CAS  Google Scholar 

  • Pantaloni, C., Brabet, P., Bilanges, B., et al. (1996). Alternative splicing in the N-terminal extracellular domain of the pituitary adenylate cyclase activating polypeptide (PACAP) receptor modulates receptor selectivity and relative potencies of PACAP-27 and PACAP-38 in phospholipase C activation. Journal of Biological Chemistry, 271, 22146–22151. doi:10.1074/jbc.271.36.22146.

    Article  PubMed  CAS  Google Scholar 

  • Pisegna, J. R., & Oh, D. S. (2007). Pituitary adenylate cyclase activating polypeptide: A novel peptide with protean implications. Current Opinion on Endocrinology, Diabetes and Obesity, 14, 58–62.

    CAS  Google Scholar 

  • Pisegna, J. R., & Wank, S. A. (1996). Cloning and characterization of the signal transduction of four splice variants of the human pituitary adenylate cyclase activating polypeptide receptor. Journal of Biological Chemistry, 271, 17267–17274. doi:10.1074/jbc.271.29.17267.

    Article  PubMed  CAS  Google Scholar 

  • Racz, B., Gallyas Jr., F., Kiss, P., et al. (2006). The neuroprotective effects of PACAP in monosodium glutamate-induced retinal lesion involves inhibition of proapoptotic signaling pathways. Regulatory Peptides, 137, 20–26. doi:10.1016/j.regpep.2006.02.009.

    Article  PubMed  CAS  Google Scholar 

  • Racz, B., Gallyas Jr, F., Kiss, P., et al. (2007). Effects of pituitary adenylate cyclase activating polypeptide (PACAP) on the PKA-Bad-14-3-3 signaling pathway in glutamate-induced retinal injury in neonatal rats. Neurotoxicity Research, 12, 95–104.

    Article  PubMed  CAS  Google Scholar 

  • Racz, B., Gasz, B., Gallyas Jr., F., et al. (2008). PKA-Bad-14-3-3 and Akt-Bad-14-3-3 signaling pathways are involved in the protective effects of PACAP against ischemia/reperfusion-induced cardiomyocyte apoptosis. Regulatory Peptides, 145, 105–115. doi:10.1016/j.regpep.2007.09.015.

    Article  PubMed  CAS  Google Scholar 

  • Reglodi, D., Kiss, P., Tamas, A., & Lengvari, I. (2003). The effects of PACAP and PACAP antagonist on the neurobehavioral development of newborn rats. Behavioural Brain Research, 140, 131–139. doi:10.1016/S0166-4328(02)00289-9.

    Article  PubMed  CAS  Google Scholar 

  • Robberecht, P., Gourlet, P., De Neef, P., et al. (1992a). Structural requirements for the occupancy of pituitary adenylate cyclase activating peptide (PACAP) receptors and adenylate cyclase activation in human neuroblastoma NB-OK-1 cell membranes. Discovery of PACAP(6-38) as a potent antagonist. European Journal of Biochemistry, 207, 239–246. doi:10.1111/j.1432-1033.1992.tb17043.x.

    Article  PubMed  CAS  Google Scholar 

  • Robberecht, P., Gourlet, P., De Neef, P., et al. (1992b). Receptor occupancy and adenylate cyclase activation in AR 4-2J rat pancreatic acinar cell membranes by analogs of pituitary adenylate cyclase activating peptides amino-terminally shortened or modified at position 1, 2, 3, 20, or 21. Molecular Pharmacology, 42, 347–355.

    PubMed  CAS  Google Scholar 

  • Scaldaferri, M. L., Modesti, A., Palumbo, C., et al. (2000). Pituitary adenylate cyclase activating polypeptide (PACAP) and PACAP-receptor type 1 expression in rat and human placenta. Endocrinology, 141, 1158–1167. doi:10.1210/en.141.3.1158.

    Article  PubMed  CAS  Google Scholar 

  • Sherwood, N. M., Krueckl, S. L., & McRory, J. E. (2000). The origin and function of the pituitary adenylate cyclase activating polypeptide (PACAP)/glucagon superfamily. Endocrine Reviews, 21, 619–670. doi:10.1210/er.21.6.619.

    Article  PubMed  CAS  Google Scholar 

  • Shintani, N., Suetake, S., Hashimoto, H., et al. (2005). Neuroprotective action of endogenous PACAP in cultured rat cortical neurons. Regulatory Peptides, 126, 123–128. doi:10.1016/j.regpep.2004.08.014.

    Article  PubMed  CAS  Google Scholar 

  • Shioda, S., Ohtaki, H., Nakamachi, T., et al. (2006). Pleiotropic functions of PACAP in the CNS. Neuroprotection and neurodevelopment. Annals of the New York Academy of Sciences, 1070, 550–560. doi:10.1196/annals.1317.080.

    Article  PubMed  CAS  Google Scholar 

  • Sun, C., Song, D., Davis-Traber, R. A., et al. (2007). Solution structure and mutational analysis of pituitary adenylate cyclase activating polypeptide binding to the extracellular domain of PAC1-Rs. Proceedings of the National Academy of Sciences of the United States of America, 104, 7875–7880. doi:10.1073/pnas.0611397104.

    Article  PubMed  CAS  Google Scholar 

  • Szolcsanyi, J., & Bartho, L. (1982). Capsaicin-sensitive non-cholinergic excitatory innervation of the guinea-pig tracheobronchial smooth muscle. Neuroscience Letters, 34, 247–251. doi:10.1016/0304-3940(82)90183-5.

    Article  PubMed  CAS  Google Scholar 

  • Takeba, Y., Suzuki, N., Kaneko, A., Asai, T., & Sakane, T. (1999). Evidence for neural regulation of inflammatory synovial cell functions by secreting calcitonin gene-related peptide and vasoactive intestinal peptide in patients with rheumatoid arthritis. Arthritis and Rheumatism, 42, 2418–2429. doi:10.1002/1529-0131(199911)42:11<2418::AID-ANR21>3.0.CO;2-7.

    Article  PubMed  CAS  Google Scholar 

  • Tohei, A., Matsuzaki, M., & Kogo, H. (2001). Antagonist of pituitary adenylate cyclase activating polypeptide suppresses prolactin secretion without changing the activity of dopamine neurons in lactating rats. Neuroendocrinology, 73, 68–74.

    Article  PubMed  CAS  Google Scholar 

  • Vandermeers, A., Vandenborre, S., Hou, X., et al. (1992). Antagonistitc properties are shifted back to agonistic properties by further N-terminal shortening of pituitary adenylate cyclase activating peptides in human neuroblastoma NB-OK-1 cell membranes. European Journal of Biochemistry, 208, 815–819. doi:10.1111/j.1432-1033.1992.tb17252.x.

    Article  PubMed  CAS  Google Scholar 

  • Vaudry, D., Gonzalez, B. J., Basille, M., Pamantung, T. F., Fournier, A., & Vaudry, H. (2000a). PACAP acts as a neurotrophic factor during histogenesis of the rat cerebellar cortex. Annals of the New York Academy of Sciences, 921, 293–299.

    Article  PubMed  CAS  Google Scholar 

  • Vaudry, D., Gonzalez, B. J., Basille, M., Yon, L., Fournier, A., & Vaudry, H. (2000b). Pituitary adenylate cyclase activating polypeptide and its receptors: from structure to functions. Pharmacological Reviews, 52, 269–324.

    PubMed  CAS  Google Scholar 

  • Vaudry, D., Pamantung, T. F., Basille, M., et al. (2002). PACAP protects cerebellar granule neurons against oxidative stress-induced apoptosis. European Journal of Neuroscience, 15, 1451–1460. doi:10.1046/j.1460-9568.2002.01981.x.

    Article  PubMed  CAS  Google Scholar 

  • Winzell, M. S., & Ahren, B. (2007). G-protein-coupled receptors and islet function—Implications for treatment of type 2 diabetes. Pharmacology & Therapeutics, 116, 437–448.

    Article  CAS  Google Scholar 

  • Wong, A. O., Leung, M. Y., Shea, W. L., Tse, L. Y., Chang, J. P., & Chow, B. K. (1998). Hypophysiotropic action of pituitary adenylate cyclase activating polypeptide (PACAP) in the goldfish: Immunohistochemical demonstration of PACAP in the pituitary, PACAP stimulation of growth hormone release from pituitary cells, and molecular cloning of pituitary type I PACAP receptor. Endocrinology, 139, 3465–3479. doi:10.1210/en.139.8.3465.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, C. J., Kikuyama, S., Nakajo, S., Hirabayashi, T., Mizushima, H., & Shioda, S. (2000). Splice variants of PAC1 receptor during early neuronal development of rats. Peptides, 21, 1177–1183. doi:10.1016/S0196-9781(00)00257-6.

    Article  PubMed  CAS  Google Scholar 

  • Zia, F., Fagarasan, M., Bitar, K., et al. (1995). Pituitary adenylate cyclase activating peptide receptors regulate the growth of non-small cell lung cancer cells. Cancer Research, 55, 4886–4891.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was sponsored by Hungarian Grants: T046589, K72592, K73044, F67830, NRDP1A/005/2004, RET-008/2005, ETT-06-348/2006, ETT-06-284/2006 and Bolyai Postdoctoral Research Fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Z Helyes.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reglodi, D., Borzsei, R., Bagoly, T. et al. Agonistic Behavior of PACAP6-38 on Sensory Nerve Terminals and Cytotrophoblast Cells. J Mol Neurosci 36, 270–278 (2008). https://doi.org/10.1007/s12031-008-9089-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12031-008-9089-z

Keywords

Navigation