Prokineticins are neuroprotective in models of cerebral ischemia and ischemic tolerance in vitro

Neuropharmacology

Volumn 108, Issue , 2016, Pages 39-48

  Landucci, Elisa ^a   Lattanzi, Roberta ^b   Gerace, Elisabetta ^a   Scartabelli, Tania ^a   Balboni, Gianfranco ^c   Negri, Lucia ^b   Pellegrini Giampietro, Domenico E ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Bv8; Ischemic tolerance; Neuroprotection; Oxygen glucose deprivation; Preconditioning; Prokineticins

Indexed keywords

CASPASE 3; ENDOCRINE GLAND DERIVED VASCULAR ENDOTHELIAL GROWTH FACTOR; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUROPEPTIDE; PROKINETICIN 2; UNCLASSIFIED DRUG; GASTROINTESTINAL HORMONE; NEUROPROTECTIVE AGENT; PROK2 PROTEIN, RAT; PROKINETICIN 2, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN CELL; BRAIN ISCHEMIA; ENZYME RELEASE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; IN VITRO STUDY; NERVE CELL LESION; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; UPREGULATION; ANIMAL; ANURA; BIOSYNTHESIS; BRAIN CORTEX; CELL CULTURE; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; MOUSE; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; RAT;

ANIMALS; ANURA; APOPTOSIS; BRAIN ISCHEMIA; CELLS, CULTURED; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; GASTROINTESTINAL HORMONES; HIPPOCAMPUS; MICE; NEUROPEPTIDES; NEUROPROTECTIVE AGENTS; ORGAN CULTURE TECHNIQUES; RATS;

EID: 84975886650     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2016.04.043     Document Type: Article

References (43)

1. Abou-Hamdan, M., Costanza, M., Fontana, E., Di Dario, M., Musio, S., Congiu, C., Onnis, V., Lattanzi, R., Radaelli, M., Martinelli, V., Salvadori, S., Negri, L., Poliani, P.L., Farina, C., Balboni, G., Steinman, L., Pedotti, R., Critical role for prokineticin 2 in CNS autoimmunity. Neurol. Neuroimmunol. Neuroinflamm., 2, 2015, e95.
2. Boulberdaa, M., Urayama, K., Nebigil, C.G., Prokineticin receptor 1 (PKR1) signalling in cardiovascular and kidney functions. Cardiovasc. Res. 92 (2011), 191–198.
3. Cheng, M.Y., Lee, A.G., Culbertson, C., Sun, G.H., Talati, R.K., Manley, N.C., Li, X.H., Zhao, H., Lyons, D.M., Zhou, Q.Y., Steinberg, G.K., Sapolsky, R.M., Prokineticin 2 is an endangering mediator of cerebral ischemic injury. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 5475–5480.
4. Cheng, M.Y., Leslie, F.M., Zhou, Q.Y., Expression of prokineticins and their receptors in the adult mouse brain. J. Comp. Neurol. 498 (2006), 796–809.
5. Congiu, C., Onnis, V., Deplano, A., Salvadori, S., Marconi, V., Maftei, D., Negri, L., Lattanzi, R., Balboni, G., A new convenient synthetic method and preliminary pharmacological characterization of triazinediones as prokineticin receptor antagonists. Eur. J. Med. Chem. 81 (2014), 334–340.
6. Conti, P., Pinto, A., Tamborini, L., Madsen, U., Nielsen, B., Brauner-Osborne, H., Hansen, K.B., Landucci, E., Pellegrini-Giampietro, D.E., De Sarro, G., Di Paola, E.D., De Micheli, C., Novel 3-carboxy- and 3-phosphonopyrazoline amino acids as potent and selective NMDA receptor antagonists: design, synthesis, and pharmacological characterization. ChemMedChem 5 (2010), 1465–1475.
7. Dirnagl, U., Becker, K., Meisel, A., Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol. 8 (2009), 398–412.
8. Gasser, A., Brogi, S., Urayama, K., Nishi, T., Kurose, H., Tafi, A., Ribeiro, N., Desaubry, L., Nebigil, C.G., Discovery and cardioprotective effects of the first non-peptide agonists of the G protein-coupled prokineticin receptor-1. PLoS One, 10, 2015, e0121027.
9. George, P.M., Steinberg, G.K., Novel stroke therapeutics: unraveling stroke pathophysiology and its impact on clinical treatments. Neuron 87 (2015), 297–309.
10. Gerace, E., Landucci, E., Scartabelli, T., Moroni, F., Chiarugi, A., Pellegrini-Giampietro, D.E., Interplay between histone acetylation/deacetylation and poly(ADP-ribosyl)ation in the development of ischemic tolerance in vitro. Neuropharmacology 92 (2015), 125–134.
11. Gerace, E., Landucci, E., Scartabelli, T., Moroni, F., Pellegrini-Giampietro, D.E., Rat hippocampal slice culture models for the evaluation of neuroprotective agents. Methods Mol. Biol. 846 (2012), 343–354.
12. Gerace, E., Scartabelli, T., Formentini, L., Landucci, E., Moroni, F., Chiarugi, A., Pellegrini-Giampietro, D.E., Mild activation of poly(ADP-ribose) polymerase (PARP) is neuroprotective in rat hippocampal slice models of ischemic tolerance. Eur. J. Neurosci. 36 (2012), 1993–2005.
13. Giannini, E., Lattanzi, R., Nicotra, A., Campese, A.F., Grazioli, P., Screpanti, I., Balboni, G., Salvadori, S., Sacerdote, P., Negri, L., The chemokine Bv8/prokineticin 2 is up-regulated in inflammatory granulocytes and modulates inflammatory pain. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 14646–14651.
14. Gidday, J.M., Cerebral preconditioning and ischaemic tolerance. Nat. Rev. Neurosci. 7 (2006), 437–448.
15. Green, A.R., Shuaib, A., Therapeutic strategies for the treatment of stroke. Drug Discov. Today 11 (2006), 681–693.
16. Koyama, Y., Kiyo-oka, M., Osakada, M., Horiguchi, N., Shintani, N., Ago, Y., Kakuda, M., Baba, A., Matsuda, T., Expression of prokineticin receptors in mouse cultured astrocytes and involvement in cell proliferation. Brain Res. 1112 (2006), 65–69.
17. Landucci, E., Scartabelli, T., Gerace, E., Moroni, F., Pellegrini-Giampietro, D.E., CB1 receptors and post-ischemic brain damage: studies on the toxic and neuroprotective effects of cannabinoids in rat organotypic hippocampal slices. Neuropharmacology 60 (2011), 674–682.
18. Lattanzi, R., Maftei, D., Marconi, V., Florenzano, F., Franchi, S., Borsani, E., Rodella, L.F., Balboni, G., Salvadori, S., Sacerdote, P., Negri, L., Prokineticin 2 upregulation in the peripheral nervous system has a major role in triggering and maintaining neuropathic pain in the chronic constriction injury model. Biomed. Res. Int., 2015, 2015.
19. LeCouter, J., Ferrara, N., EG-VEGF and Bv8: a novel family of tissue-selective mediators of angiogenesis, phenotype, endothelial and function. Trends Cardiovasc. Med. 13 (2003), 276–282.
20. LeCouter, J., Kowalski, J., Foster, J., Hass, P., Zhang, Z.M., Dillard-Telm, L., Frantz, G., Rangell, L., DeGuzman, L., Keller, G.A., Peale, F., Gurney, A., Hillan, K.J., Ferrara, N., Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 412 (2001), 877–884.
21. LeCouter, J., Zlot, C., Tejada, M., Peale, F., Ferrara, N., Bv8 and endocrine gland-derived vascular endothelial growth factor stimulate hematopoiesis and hematopoietic cell mobilization. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 16813–16818.
22. Lin, D.C., Bullock, C.M., Ehlert, F.J., Chen, J.L., Tian, H., Zhou, Q.Y., Identification and molecular characterization of two closely related G protein-coupled receptors activated by prokineticins/endocrine gland vascular endothelial growth factor. J. Biol. Chem. 277 (2002), 19276–19280.
23. Martucci, C., Franchi, S., Giannini, E., Tian, H., Melchiorri, P., Negri, L., Sacerdote, P., Bv8, the amphibian homologue of the mammalian prokineticins, induces a proinflammatory phenotype of mouse macrophages. Brit. J. Pharmacol. 147 (2006), 225–234.
24. Masuda, Y., Takatsu, Y., Terao, Y., Kumano, S., Ishibashi, Y., Suenaga, M., Abe, M., Fukusumi, S., Watanabe, T., Shintani, Y., Yamada, T., Hinuma, S., Inatomi, N., Ohtaki, T., Onda, H., Fujino, M., Isolation and identification of EG-VEGF/prokineticins as cognate ligands for two orphan G-protein-coupled receptors. Biochem. Biophys. Res. Commun. 293 (2002), 396–402.
25. Melchiorri, D., Bruno, V., Besong, G., Ngomba, R., Cuomo, L., Copani, A., Nicoletti, F., Passarelli, F., The mammalian homologue of the novel peptide BV8 is expressed in the central nervous system and supports neuronal survival by activating the MAP kinase/PI-3-kinase pathways. Brit. J. Pharmacol., 133, 2001, U26.
26. Mollay, C., Wechselberger, C., Mignogna, G., Negri, L., Melchiorri, P., Barra, D., Kreil, G., Bv8, a small protein from frog skin and its homologue from snake venom induce hyperalgesia in rats. Eur. J. Pharmacol. 374 (1999), 189–196.
27. Monnier, J., Samson, M., Prokineticins in angiogenesis and cancer. Cancer Lett. 296 (2010), 144–149.
28. Moroni, F., Meli, E., Peruginelli, F., Chiarugi, A., Cozzi, A., Picca, R., Romagnoli, P., Pellicciari, R., Pellegrini-Giampietro, D.E., Poly(ADP-ribose) polymerase inhibitors attenuate necrotic but not apoptotic neuronal death in experimental models of cerebral ischemia. Cell Death Differ. 8 (2001), 921–932.
29. Negri, L., Lattanzi, R., Bv8-prokineticins and their receptors: modulators of pain. Curr. Pharm. Biotechnol. 12 (2011), 1720–1727.
30. Negri, L., Lattanzi, R., Giannini, E., Colucci, M., Margheriti, F., Melchiorri, P., Vellani, V., Tian, H., De Felice, M., Porreca, F., Impaired nociception and inflammatory pain sensation in mice lacking the prokineticin receptor PKR1: focus on interaction between PKR1 and the capsaicin receptor TRPV1 in pain behavior. J. Neurosci. 26 (2006), 6716–6727.
31. Negri, L., Lattanzi, R., Giannini, E., Colucci, M.A., Mignogna, G., Barra, D., Grohovaz, F., Codazzi, F., Kaiser, A., Kreil, G., Melchiorri, P., Biological activities of Bv8 analogues. Brit. J. Pharmacol. 146 (2005), 625–632.
32. Negri, L., Lattanzi, R., Giannini, E., Melchiorri, P., Bv8/Prokineticin proteins and their receptors. Life Sci. 81 (2007), 1103–1116.
33. Ng, K.L., Li, J.D., Cheng, M.Y., Leslie, F.M., Lee, A.G., Zhou, Q.Y., Dependence of olfactory bulb neurogenesis on prokineticin 2 signaling. Science 308 (2005), 1923–1927.
34. Pellegrini-Giampietro, D.E., Cozzi, A., Peruginelli, F., Leonardi, P., Meli, E., Pellicciari, R., Moroni, F., 1-Aminoindan-1,5-dicarboxylic acid and (S)-(+)-2-(3’-carboxybicyclo[1.1.1]pentyl)-glycine, two mGlu1 receptor-preferring antagonists, reduce neuronal death in in vitro and in vivo models of cerebral ischemia. Eur. J. Neurosci. 11 (1999), 3637–3647.
35. Pellegrini-Giampietro, D.E., Peruginelli, F., Meli, E., Cozzi, A., Albani Torregrossa, S., Pellicciari, R., Moroni, F., Protection with metabotropic glutamate 1 receptor antagonists in models of ischemic neuronal death: time-course and mechanisms. Neuropharmacology 38 (1999), 1607–1619.
36. Pellicciari, R., Marinozzi, M., Costantino, G., Natalini, B., Moroni, F., Pellegrini-Giampietro, D., (2R,1’S,2’R,3’S)-2-(2’-Carboxy-3’-phenylcyclopropyl)glycine (PCCG-13), the first potent and selective competitive antagonist of phospholipase D-coupled metabotropic glutamate receptors: asymmetric synthesis and preliminary biological properties. J. Med. Chem. 42 (1999), 2716–2720.
37. Pitteloud, N., Zhang, C., Pignatelli, D., Li, J.D., Raivio, T., Cole, L.W., Plummer, L., Jacobson-Dickman, E.E., Mellon, P.L., Zhou, Q.Y., Crowley, W.F. Jr., Loss-of-function mutation in the prokineticin 2 gene causes Kallmann syndrome and normosmic idiopathic hypogonadotropic hypogonadism. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 17447–17452.
38. Severini, C., Lattanzi, R., Maftei, D., Marconi, V., Ciotti, M.T., Petrocchi, P.P., Florenzano, F., Del Duca, E., Caioli, S., Zona, C., Balboni, G., Salvadori, S., Nistico, R., Negri, L., Bv8/prokineticin 2 is involved in Aß-induced neurotoxicity. Sci. Rep., 5, 2015, 15301.
39. Soga, T., Matsumoto, S., Oda, T., Saito, T., Hiyama, H., Takasaki, J., Kamohara, M., Ohishi, T., Matsushime, H., Furuichi, K., Molecular cloning and characterization of prokineticin receptors. Biochim. Biophys. Acta 1579 (2002), 173–179.
40. Urayama, K., Guilini, C., Turkeri, G., Takir, S., Kurose, H., Messaddeq, N., Dierich, A., Nebigil, C.G., Prokineticin receptor-1 induces neovascularization and epicardial-derived progenitor cell differentiation. Arterioscler. Thromb. Vasc. Biol. 28 (2008), 841–849.
41. Wang, Y., Reis, C., Applegate, R., Stier, G., Martin, R., Zhang, J.H., Ischemic conditioning-induced endogenous brain protection: applications pre-, per- or post-stroke. Exp. Neurol. 272 (2015), 26–40.
42. Wechselberger, C., Puglisi, R., Engel, E., Lepperdinger, G., Boitani, C., Kreil, G., The mammalian homologues of frog Bv8 are mainly expressed in spermatocytes. FEBS Lett. 462 (1999), 177–181.
43. Werner, C.G., Scartabelli, T., Pancani, T., Landucci, E., Moroni, F., Pellegrini-Giampietro, D.E., Differential role of mGlu1 and mGlu5 receptors in rat hippocampal slice models of ischemic tolerance. Eur. J. Neurosci. 25 (2007), 3597–3604.