Effect of PACAP on MAP kinases, Akt and cytokine expressions in rat retinal hypoperfusion

Neuroscience Letters

Volumn 523, Issue 2, 2012, Pages 93-98

  Szabo, Aliz ^a   Danyadi, Bese ^b   Bognar, Eszter ^a   Szabadfi, Krisztina ^b   Fabian, Eszter ^b   Kiss, Peter ^b   Mester, Laszlo ^a   Manavalan, Sridharan ^b,c   Atlasz, Tamas ^b   Gabriel, Robert ^b   Toth, Gabor ^d   Tamas, Andrea ^b   Reglodi, Dora ^b   Kovacs, Krisztina ^a  

^a UNIVERSITY OF PÉCS   (Hungary)

^b UNIVERSITY OF PÉCS   (Hungary)

^c NATIONAL UNIVERSITY OF HEALTH SCIENCES   (United States)

^d UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Akt; Cytokine array; ERK; JNK; P38MAPK; PACAP; Retinal ischemia

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; CYTOKINE; FRACTALKINE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 6; L SELECTIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; RANTES; TISSUE INHIBITOR OF METALLOPROTEINASE 1; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CAROTID ARTERY OBSTRUCTION; CONTROLLED STUDY; CYTOKINE RELEASE; EYE PROTECTION; MALE; NEUROPROTECTION; NONHUMAN; ORGAN PERFUSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RETINA; RETINA ISCHEMIA; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; CAROTID ARTERY, COMMON; CAROTID STENOSIS; CYTOKINES; ENZYME ACTIVATION; ISCHEMIA; MALE; MITOGEN-ACTIVATED PROTEIN KINASES; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; RETINA; RETINAL VESSELS; SIGNAL TRANSDUCTION;

EID: 84864296954     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2012.06.044     Document Type: Article

References (53)

1. Asaga T., Ueki M., Chujo K., Taie S. JTE-607, an inflammatory cytokine synthesis inhibitor, attenuates ischemia/reperfusion-induced renal injury by reducing neutrophil activation in rats. Journal of Bioscience and Bioengineering 2008, 106:22-26.
2. Atlasz T., Babai N., Kiss P., Reglodi D., Tamas A., Szabadfi K., Toth G., Hegyi O., Lubics A., Gabriel R. Pituitary adenylate cyclase activating polypeptide is protective in bilateral carotid occlusion-induced retinal lesion in rats. General and Comparative Endocrinology 2007, 153:108-114.
3. Atlasz T., Szabadfi K., Kiss P., Babai N., Koszegi Z., Tamas A., Reglodi D., Gabriel R. PACAP-mediated neuroprotection of neurochemically identified cell types in MSG-induced retinal regeneration. Journal of Molecular Neuroscience 2008, 36:97-104.
4. Atlasz T., Szabadfi K., Kiss P., Racz B., Gallyas F., Tamas A., Gaal V., Marton Zs., Gabriel R., Reglodi D. Pituitary adenylate cyclase activating polypeptide in the retina: focus on the retinoprotective effects. Annals of the New York Academy of Sciences 2010, 1200:128-139.
5. Atlasz T., Szabadfi K., Kiss P., Tamas A., Toth G., Reglodi D., Gabriel R. Evaluation of the protective effects of PACAP with cell-specific markers in ischemia-induced retinal degeneration. Brain Research Bulletin 2010, 81:497-504.
6. Atlasz T., Szabadfi K., Kiss P., Marton Zs., Griecs M., Hamza L., Gaal V., Biro Zs., Tamas A., Hild G., Nyitrai M., Toth G., Reglodi D., Gabriel R. Effects of PACAP in UV-A radiation-induced retinal degeneration models in rats. Journal of Molecular Neuroscience 2011, 43:51-57.
7. Borba J.C., Henze I.P., Silveira M.S., Kubrusly R.C., Gardino P.F., de Mello M.C., Hokoç J.N., de Mello F.G. Pituitary adenylate cyclase-activating polypeptide (PACAP) can act as determinant of the tyrosine hydroxylase phenotype of dopaminergic cells during retina development. Developmental Brain Research 2005, 156:193-201.
8. Brenneman D.E., Hauser J.M., Spong C., Phillips T.M. Chemokine release is associated with the protective action of PACAP-38 against HIV envelope protein neurotoxicity. Neuropeptides 2002, 36:271-280.
9. Cervia D., Catalani E., Dal Monte M., Casini G. Vascular endothelial growth factor in the ischemic retina and its regulation by somatostatin. Journal of Neurochemistry 2012, 120:818-829.
10. Crane I.J., Kuppner M.C., McKillop-Smith S., Knott R.M., Forrester J.V. Cytokine regulation of RANTES production by human retinal pigment epithelial cells. Cellular Immunology 1998, 184:37-44.
11. Delgado M., Jonakait G.M., Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit chemokine production in activated microglia. Glia 2002, 39:148-161.
12. Delgado M., Abad C., Martinez C., Juarranz M.G., Leceta J., Ganea D., Gomariz R.P. PACAP in immunity and inflammation. Annals of the New York Academy of Sciences 2003, 992:141-157. Review.
13. Delgado M., Leceta J., Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit the production of inflammatory mediators by activated microglia. Journal of Leukocyte Biology 2003, 73:155-164.
14. Dreixler J.C., Hemmert J.W., Shenoy S.K., Shen Y., Lee H.T., Shaikh A.R., Rosenbaum D.M., Roth S. The role of Akt/protein kinase B subtypes in retinal ischemic preconditioning. Experimental Eye Research 2009, 88:512-521.
15. Dvoriantchikova G., Barakat D.J., Hernandez E., Shestopalov V.I., Ivanov D. Liposome-delivered ATP effectively protects the retina against ischemia-reperfusion injury. Molecular Vision 2010, 16:2882-2890.
16. Endo K., Nakamachi T., Seki T., Kagami N., Wada Y., Nakamura K., Kishimoto K., Hori M., Tsuchikawa D., Shintani N., Hashimoto H., Baba A., Koide R., Shioda S. Neuroprotective effect of PACAP against NMDA-induced retinal damage in the mouse. Journal of Molecular Neuroscience 2011, 43:22-29.
17. Engelund A., Fahrenkrug J., Harrison A., Luuk H., Hannibal J. Altered pupillary light reflex in PACAP receptor 1-deficient mice. Brain Research 2012, 1453:17-25.
18. Farkas E., Luiten P.G., Bari F. Permanent, bilateral common carotid artery occlusion in the rat: a model for chronic cerebral hypoperfusion-related neurodegenerative diseases. Brain Research Reviews 2007, 54:162-180.
19. Ferencz A., Kiss P., Weber Gy., Helyes Zs., Shintani N., Baba A., Reglodi D. Comparison of intestinal warm ischemic injury in PACAP knock-out and wild-type mice. Journal of Molecular Neuroscience 2010, 42:435-442.
20. Gaal V., Mark L., Kiss P., Kustos I., Tamas A., Kocsis B., Lubics A., Nemeth V., Nemeth A., Lujber L., Pytel J., Toth G., Reglodi D. Investigation of the effects of PACAP on the composition of tear and endolymph proteins. Journal of Molecular Neuroscience 2008, 36:321-329.
21. Ghaly A., Marsh D.R. Ischaemia-reperfusion modulates inflammation and fibrosis of skeletal muscle after contusion injury. International Journal of Experimental Pathology 2010, 91:244-255.
22. Gloddek J., Pagotto U., Paez Pereda M., Arzt E., Stalla G.K., Renner U. Pituitary adenylate cyclase-activating polypeptide, interleukin-6 and glucocorticoids regulate the release of vascular endothelial growth factor in pituitary folliculostellate cells. Journal of Endocrinology 1999, 160:483-490.
23. Gustavsson C., Agardh C.D., Hagert P., Agardh E. Inflammatory markers in nondiabetic and diabetic rat retinas exposed to ischemia followed by reperfusion. Retina 2008, 28:645-652.
24. Hannibal J., Fahrenkrug J. Target areas innervated by PACAP-immunoreactive retinal ganglion cells. Cell and Tissue Research 2004, 316:99-113.
25. Ji Q., Zhang L., Lv R., Jia H., Xu J. Pentoxifylline decreases up-regulated nuclear factor kappa B activation and cytokine production in the rat retina following transient ischemia. Ophthalmologica 2006, 220:217-224.
26. Jonas J.B., Tao Y., Neumaier M., Findeisen P. Monocyte chemoattractant protein 1, intercellular adhesion molecule 1, and vascular cell adhesion molecule 1 in exudative age-related macular degeneration. Archives of Ophthalmology 2010, 128:1281-1286.
27. Junnarkar S.P., Tapuria N., Mani A., Dijk S., Fuller B., Seifalian A.M., Davidson B.R. Attenuation of warm ischemia-reperfusion injury in the liver by bucillamine through decreased neutrophil activation and Bax/Bcl-2 modulation. Journal of Gastroenterology and Hepatology 2010, 25:1891-1899.
28. Kiss P., Atlasz T., Szabadfi K., Horvath G., Griecs M., Farkas J., Matkovits A., Toth G., Lubics A., Tamas A., Gabriel R., Reglodi D. Comparison between PACAP- and enriched environment-induced retinal protection in MSG-treated newborn rats. Neuroscience Letters 2011, 487:400-405.
29. Lamoke F., Labazi M., Montemari A., Parisi G., Varano M., Bartoli M. Trans-chalcone prevents VEGF expression and retinal neovascularization in the ischemic retina. Experimental Eye Research 2011, 93:350-354.
30. Mathalone N., Lahat N., Rahat M.A., Bahar-Shany K., Oron Y., Geyer O. The involvement of matrix metalloproteinases 2 and 9 in rat retinal ischemia. Graefes Archive for Clinical and Experimental Ophthalmology 2007, 245:725-732.
31. May V., Lutz E., MacKenzie C., Schutz K.C., Dozark K., Braas K.M. Pituitary adenylate cyclase-activating polypeptide (PACAP)/PAC1HOP1 receptor activation coordinates multiple neurotrophic signaling pathways: Akt activation through phosphatidylinositol 3-kinase gamma and vesicle endocytosis for neuronal survival. Journal of Biological Chemistry 2010, 285:9749-9761.
32. Moody T.W., Leyton J., Casibang M., Pisegna J., Jensen R.T. PACAP-27 tyrosine phosphorylates mitogen activated protein kinase and increases VEGF mRNAs in human lung cancer cells. Regulatory Peptides 2002, 109:135-140.
33. Nenekidis I., Pournaras C.J., Tsironi E., Tsilimingas N. Vision impairment during cardiac surgery and extracorporeal circulation: current understanding and the need for further investigation. Acta Ophthalmologica 2012, 90:168-172.
34. Ohtaki H., Nakamachi T., Dohi K., Shioda S. Role of PACAP in ischemic neural death. Journal of Molecular Neuroscience 2008, 36:16-25.
35. Racz B., Gallyas F., Kiss P., Toth G., Hegyi O., Gasz B., Borsiczky B., Ferencz A., Roth E., Tamas A., Lengvari I., Lubics A., Reglodi D. The neuroprotective effects of PACAP in monosodium glutamate-induced retinal lesion involves inhibition of proapoptotic signaling pathways. Regulatory Peptides 2006, 137:20-26.
36. Racz B., Tamas A., Kiss P., Toth G., Gasz B., Borsiczky B., Ferencz A., Gallyas F., Roth E., Reglodi D. Involvement of ERK and CREB signaling pathways in the protective effect of PACAP in monosodium glutamate-induced retinal lesion. Annals of the New York Academy of Sciences 2006, 1070:507-511.
37. Racz B., Gasz B., Gallyas F., Kiss P., Tamas A., Szanto Z., Lubics A., Lengvari I., Toth G., Hegyi O., Roth E., Reglodi D. PKA-Bad-14-3-3 Akt-Bad-14-3-3 signaling pathways are involved in the protective effects of PACAP against ischemia/reperfusion-induced cardiomyocyte apoptosis. Regulatory Peptides 2008, 145:105-115.
38. Reglodi D., Kiss P., Horvath G., Lubics A., Laszlo E., Tamas A., Racz B., Szakaly P. Effects of pituitary adenylate cyclase activating polypeptide in the urinary system, with special emphasis on its protective effects in the kidney. Neuropeptides 2012, 46:61-70.
39. Sanchez A., Tripathy D., Grammas P. RANTES release contributes to the protective action of PACAP38 against sodium nitroprusside in cortical neurons. Neuropeptides 2009, 43:315-320.
40. Seki T., Nakatani M., Taki C., Shinohara Y., Ozawa M., Nishimura S., Ito H., Shioda S. Neuroprotective effect of PACAP against kainic acid-induced neurotoxicity in rat retina. Annals of the New York Academy of Sciences 2006, 1070:531-534.
41. Somogyvari-Vigh A., Reglodi D. Pituitary adenylate cyclase activating polypeptide: a potential neuroprotective peptide. Current Pharmaceutical Design 2004, 10:2861-2889.
42. Szabadfi K., Mester L., Reglodi D., Kiss P., Babai N., Racz B., Kovacs K., Szabo A., Tamas A., Gabriel R., Atlasz T. Novel neuroprotective strategies in ischemic retinal lesions. International Journal of Molecular Sciences 2010, 11:544-561.
43. Szabadfi K., Atlasz T., Kiss P., Danyadi B., Tamas A., Helyes Zs., Hashimoto H., Shintani N., Baba A., Toth G., Gabriel R., Reglodi D. Mice deficient in pituitary adenylate cyclase activating polypeptide (PACAP) are more susceptible to retinal ischemic injury in vivo. Neurotoxicity Research 2012, 21:41-48.
44. Szabadfi K., Atlasz T., Kiss P., Reglodi D., Szabo A., Kovacs K., Szalontai B., Setalo G., Banki E., Csanaky K., Tamas A., Gabriel R. Protective effects of the neuropeptide PACAP in diabetic retinopathy. Cell and Tissue Research 2012, 348:37-46.
45. K. Szabadfi, B. Danyadi, P. Kiss, A. Tamas, E. Fabian, R. Gabriel, D. Reglodi, Protective effects of vasoactive intestinal peptide (VIP) in ischemic retinal degeneration, Journal of Molecular Neuroscience, PMID: 22544514, in press.
46. Szakaly P., Laszlo E., Kovacs K., Racz B., Horvath G., Ferencz A., Lubics A., Kiss P., Tamas A., Brubel R., Opper B., Baba A., Hashimoto H., Farkas J., Matkovits A., Magyarlaki T., Helyes Z., Reglodi D. Mice deficient in pituitary adenylate cyclase activating polypeptide (PACAP) show increased susceptibility to in vivo renal ischemia/reperfusion injury. Neuropeptides 2011, 45:113-121.
47. Vaudry D., Pamantung T.F., Basille M., Rousselle C., Fournier A., Vaudry H., Beauvillain J.C., Gonzalez B.J. PACAP protects cerebellar granule neurons against oxidative stress-induced apoptosis. European Journal of Neuroscience 2002, 15:1451-1460.
48. Vaudry D., Falluel-Morel A., Basille M., Pamantung T.F., Fontaine M., Fournier A., Vaudry H., Gonzalez B.J. Pituitary adenylate cyclase-activating polypeptide prevents C2-ceramide-induced apoptosis of cerebellar granule cells. Journal of Neuroscience Research 2003, 72:303-316.
49. Vaudry D., Falluel-Morel A., Bourgault A., Basille M., Burel D., Wurtz O., Fournier A., Chow B.K., Hashimoto H., Galas L., Vaudry H. Pituitary adenylate cyclase activating polypeptide and its receptors: 20 years after the discovery. Pharmacological Reviews 2009, 61:283-357.
50. Yoneda S., Tanihara H., Kido N., Honda Y., Goto W., Hara H., Miyawaki N. Interleukin-1beta mediates ischemic injury in the rat retina. Experimental Eye Research 2001, 73:661-667.
51. Yoshida S., Yoshida A., Ishibashi T., Elner S.G., Elner V.M. Role of MCP-1 and MIP-1alpha in retinal neovascularization during postischemic inflammation in a mouse model of retinal neovascularization. Journal of Leukocyte Biology 2003, 73:137-144.
52. Yoshida A., Yoshida S., Hata Y., Khalil A.K., Ishibashi T., Inomata H. The role of NF-kappaB in retinal neovascularization in the rat. Possible involvement of cytokine-induced neutrophil chemoattractant (CINC), a member of the interleukin-8 family. Journal of Histochemistry and Cytochemistry 1998, 46:29-36.
53. Zheng X.R., Zhang S.S., Yin F., Tang J.L., Yang Y.J., Wang X., Zhong L. Neuroprotection of VEGF-expression neural stem cells in neonatal cerebral palsy rats. Behavioural Brain Research 2012, 230:108-115.