Protective effects of the neuropeptides PACAP, substance P and the somatostatin analogue octreotide in retinal ischemia: A metabolomic analysis

Molecular BioSystems

Volumn 10, Issue 6, 2014, Pages 1290-1304

  D'Alessandro, Angelo ^a   Cervia, Davide ^a,b   Catalani, Elisabetta ^a   Gevi, Federica ^a   Zolla, Lello ^a   Casini, Giovanni ^c  

^a UNIVERSITY OF TUSCIA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF PISA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; GLUTAMIC ACID; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; OCTREOTIDE; SUBSTANCE P; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANIMAL; C57BL MOUSE; CELL DEATH; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; ISCHEMIA; MALE; METABOLISM; METABOLOMICS; MOUSE; PATHOLOGY; RETINA;

ANIMALS; CELL DEATH; FEMALE; GENE EXPRESSION REGULATION; GLUTAMIC ACID; ISCHEMIA; MALE; METABOLOMICS; MICE; MICE, INBRED C57BL; NEUROTRANSMITTER AGENTS; OCTREOTIDE; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RETINA; SUBSTANCE P; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84900313303     PISSN: 1742206X     EISSN: 17422051     Source Type: Journal    
DOI: 10.1039/c3mb70362b     Document Type: Article

References (73)

1. G. Minhas R. Morishita A. Anand Preclinical models to investigate retinal ischemia: advances and drawbacks Front. Neurol. Neurosci. 2012 3 75
2. N. N. Osborne R. J. Casson J. P. Wood G. Chidlow M. Graham J. Melena Retinal ischemia: mechanisms of damage and potential therapeutic strategies Prog. Retinal Eye Res. 2004 23 91 147
3. M. Rajappa P. Sexena J. Kaur Ocular angiogenesis: mechanisms and recent advances in therapy Adv. Clin. Chem. 2010 50 103 121
4. P. Sapieha D. Hamel Z. Shao J. C. Rivera K. Zaniolo J. S. Joyal S. Chemtob Proliferative retinopathies: angiogenesis that blinds Int. J. Biochem. Cell Biol. 2010 42 1 5 12
5. E. Catalani D. Cervia D. Martini P. Bagnoli E. Simonetti A. M. Timperio G. Casini Changes in neuronal response to ischemia in retinas with genetic alterations of somatostatin receptor expression Eur. J. Neurosci. 2007 25 1447 1459
6. D. Cervia D. Martini C. Ristori E. Catalani A. M. Timperio P. Bagnoli G. Casini Modulation of the neuronal response to ischaemia by somatostatin analogues in wild-type and knock-out mouse retinas J. Neurochem. 2008 106 2224 2235
7. U. Celiker N. Ilhan I. Ozercan T. Demir H. Celiker Octreotide reduces ischaemia-reperfusion injury in the retina Acta Ophthalmol. Scand. 2002 80 395 400
8. D. Cervia G. Casini The Neuropeptide Systems and their Potential Role in the Treatment of Mammalian Retinal Ischemia: A Developing Story Curr. Neuropharmacol. 2013 11 95 101
9. D. Cervia G. Casini P. Bagnoli Physiology and pathology of somatostatin in the mammalian retina: a current view Mol. Cell. Endocrinol. 2008 286 112 122
10. D. Cervia E. Catalani M. Dal Monte G. Casini Vascular endothelial growth factor in the ischemic retina and its regulation by somatostatin J. Neurochem. 2012 120 818 829
11. D. Kokona I. Mastrodimou I. Pediaditakis H. Charalampopoulos A. Schmid K. ThermosPasireotide (SOM230) protects the retina in animal models of ischemia induced retinopathies Exp. Eye Res. 2012 103 90 98
12. N. Mastrodimou G. N. Lambrou K. Thermos Effect of somatostatin analogues on chemically induced ischaemia in the rat retina Naunyn-Schmiedebergs Arch. Pharmacol. 2005 371 44 53
13. P. McGonigle Peptide therapeutics for CNS indications Biochem. Pharmacol. 2012 83 559 656
14. D. Cervia G. Casini Recent advances in cellular and molecular aspects of mammalian retinal ischemia World J. Pharmacol. 2012 1 30 43
15. T. Nakamachi A. Matkovits T. Seki S. Shioda Distribution and protective function of pituitary adenylate cyclase-activating polypeptide in the retina Front. Endocrinol. 2012 3 145
16. G. Bruno F. Tega A. Bruno U. Graf F. Corelli R. Molfetta M. Barucco The role of substance P in cerebral ischemia Int. J. Immunopathol. Pharmacol. 2003 16 67 72
17. J. H. Yang X. X. Meng L. S. Xie Z. Guo Acute myocardial ischemia up-regulates substance P in the retina of rats Neurosci. Lett. 2008 443 218 222
18. G. J. Patti O. Yanes G. Siuzdak Innovation: Metabolomics: the apogee of the omics trilogy Nat. Rev. Mol. Cell Biol. 2012 13 263 269
19. A. D'Alessandro F. Gevi L. Zolla A robust high resolution reversed-phase HPLC strategy to investigate various metabolic species in different biological models Mol. BioSyst. 2011 7 1024 1032
20. A. D'Alessandro F. Gevi L. Zolla Targeted mass spectrometry-based metabolomic profiling through multiple reaction monitoring of liver and other biological matrices Methods Mol. Biol. 2012 909 279 294
21. A. D'Alessandro G. M. D'Amici S. Vaglio L. Zolla Time-course investigation of SAGM-stored leukocyte-filtered red bood cell concentrates: from metabolism to proteomics Haematologica 2012 97 107 115
22. F. Gevi A. D'Alessandro L. Zolla Alterations of red blood cell metabolome during cold liquid storage of erythrocyte concentrates in CPD-SAGM J. Proteomics 2012 76 168 180
23. R. Polati A. Castagna A. M. Bossi Murine macrophages response to iron J. Proteomics 2012 76 10 27
24. D. Cervia C. Nunn P. Bagnoli Multiple signalling transduction mechanisms differentially coupled to somatostatin receptor subtypes: a current view Curr. Enzyme Inhib. 2005 1 265 279
25. A. Bigiani C. Petrucci V. Ghiaroni M. Dal Monte A. Cozzi H. J. Kreienkamp D. Richter P. Bagnoli Functional correlates of somatostatin receptor 2 overexpression in the retina of mice with genetic deletion of somatostatin receptor 1 Brain Res. 2004 1025 177 185
26. B. Pavan S. Fiorini M. Dal Monte L. Lunghi C. Biondi P. Bagnoli D. Cervia Somatostatin coupling to adenylyl cyclase activity in the mouse retina N.-S. Arch. Pharmacol. 2004 370 91 98
27. T. Hamada S. Shibata The role of GABAergic neuron on NMDA- and SP-induced phase delays in the suprachiasmatic nucleus neuronal activity rhythm in vitro Neurosci. Lett. 2010 468 344 347
28. M. Kouznetsova A. Nistri Modulation by substance P of synaptic transmission in the mouse hippocampal slice Eur. J. Neurosci. 1998 10 3076 3084
29. F. Pena J. M. Ramirez Substance P-mediated modulation of pacemaker properties in the mammalian respiratory network J. Neurosci. 2004 24 7549 7556
30. K. Shoge H. K. Mishima T. Saitoh K. Ishihara Y. Tamura H. Shiomi M. Sasa Attenuation by PACAP of glutamate-induced neurotoxicity in cultured retinal neurons Brain Res. 1999 839 66 73
31. M. S. Silveira M. R. Costa M. Bozza R. Linden Pituitary adenylyl cyclase-activating polypeptide prevents induced cell death in retinal tissue through activation of cyclic AMP-dependent protein kinase J. Biol. Chem. 2002 277 16075 16080
32. K. J. Livak T. D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 2001 25 402 408
33. A. D'Alessandro F. Gevi L. Zolla Red blood cell metabolism under prolonged anaerobic storage Mol. BioSyst. 2013 9 6 1196 1209
34. E. Melamud L. Vastag J. D. Rabinowitz Metabolomic analysis and visualization engine for LC-MS data Anal. Chem. 2011 82 9818 9826
35. M. Kanehisa S. Goto KEGG: kyoto encyclopedia of genes and genomes Nucleic Acids Res. 2000 28 27 30
36. D. Ji T. A. Kamalden S. Olmo-Aguado N. N. Osborne Light- and sodium azide-induced death of RGC-5 cells in culture occurs via different mechanisms Apoptosis 2011 16 425 437
37. N. Mastrodimou F. Kiagiadaki K. Thermos The role of nitric oxide and cGMP in somatostatin's protection against retinal ischemia Invest. Ophthalmol. Visual Sci. 2008 49 342 349
38. F. Dijk W. Kamphuis An immunocytochemical study on specific amacrine cell subpopulations in the rat retina after ischemia Brain Res. 2004 1026 205 317
39. W. K. Ju K. Y. Kim Measuring glutamate receptor activation-induced apoptotic cell death in ischemic rat retina using the TUNEL assay Methods Mol. Biol. 2011 740 149 156
40. O. Oz G. Gürelik N. Akyürek L. Cinel A. Hondur A short duration transient ischemia induces apoptosis in retinal layers: an experimental study in rabbits Eur. J. Ophthalmol. 2005 15 233 238
41. N. Katai N. Yoshimura Apoptotic retinal neuronal death by ischemia-reperfusion is executed by two distinct caspase family proteases Invest. Ophthalmol. Visual Sci. 1999 40 2697 2705
42. L. Tenneti S. A. Lipton Involvement of activated caspase-3-like proteases in N-methyl-D-aspartate-induced apoptosis in cerebrocortical neurons J. Neurochem. 2000 74 134 142
43. S. Mei M. Cammalleri D. Azara G. Casini P. Bagnoli M. Del Monte Mechanisms underlying somatostatin receptor 2 down-regulation of vascular endothelial growth factor expression in response to hypoxia in mouse retinal explants J. Pathol. 2012 226 519 533
44. D. Ribatti M. T. Conconi G. G. Nussdorfer Nonclassic endogenous novel regulators of angiogenesis Pharmacol. Rev. 2007 59 185 205
45. N. Calvo J. Reiriz E. Pérez-Navarro J. Alberch Tachykinins protect cholinergic neurons from quinolinic acid excitotoxicity in striatal cultures Brain Res. 1996 740 323 328
46. K. Endo T. Nakamachi T. Seki N. Kagami Y. Wada K. Nakamura K. Kishimoto M. Hori D. Tsuchikawa N. Shinntani H. Hashimoto A. Baba R. Koide S. Shioda Neuroprotective effect of PACAP against NMDA-induced retinal damage in the mouse J. Mol. Neurosci. 2011 43 22 29
47. N. Dilsiz A. Sahaboglu M. Z. Yildiz A. Reichenbach Protective effects of various antioxidants during ischemia-reperfusion in the rat retina Graefe's Arch. Clin. Exp. Ophthalmol. 2006 244 627 633
48. Z. Zhang X. Qin X. Zhao N. Tong Y. Gong W. Zhang X. Wu Valproic acid regulates antioxidant enzymes and prevents ischemia/reperfusion injury in the rat retina Curr. Eye Res. 2012 37 429 437
49. M. V. Van Hecke J. M. Dekker G. Nijpels T. Teerlink C. Jakobs R. P. Stolk R. J. Heine L. M. Bouter B. C. Polak C. D. Stehouwer Homocysteine, S-adenosylmethionine and S-adenosylhomocysteine are associated with retinal microvascular abnormalities: the Hoorn Study Clin. Sci. 2008 114 479 487
50. S. Y. Li Z. J. Fu A. C. Lo Hypoxia-induced oxidative stress in ischemic retinopathy Oxid. Med. Cell. Longevity 2012 426769
51. S. Cuzzocrea D. P. Riley A. Caputi D. Salvemini Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury Pharmacol. Rev. 2001 53 135 159
52. W. Durante F. K. Johnson R. A. Johnson Arginase: a critical regulator of nitric oxide synthesis and vascular function Clin. Exp. Pharmacol. Physiol. 2007 34 906 911
53. S. P. Narayanan J. Suwanpradid A. Saul Z. Xu A. Still R. W. Caldwell R. B. Caldwell Arginase 2 deletion reduces neuro-glial injury and improves retinal function in a model of retinopathy of prematurity PLoS One 2011 6 e22460
54. A. Vasilaki M. Mouratidou S. Schulz K. Thermos Somatostatin mediates nitric oxide production by activating sst(2) receptors in the rat retina Neuropharmacology 2002 43 899 909
55. K. Szabadfi L. Mester D. Reglodi P. Kiss N. Babai B. Racz K. Kovacs A. Szabo A. Tamas R. Gabriel T. Atlasz Novel neuroprotective strategies in ischemic retinal lesions Int. J. Mol. Sci. 2010 11 544 561
56. H. Kuriyama M. Nakagawa M. Tsuda Intracellular Ca(2+) changes induced by in vitro ischemia in rat retinal slices Exp. Eye Res. 2001 73 365 374
57. C. H. Park Y. S. Kim Y. H. Kim M. Y. Choi J. M. Yoo S. S. Kang W. S. Choi G. J. Cho Calcineurin mediates AKT dephosphorylation in the ischemic rat retina Brain Res. 2008 1234 148 157
58. S. Roth A. R. Shaikh M. M. Hennelly Q. Li V. Bindokas C. E. Graham Mitogen-activated protein kinases and retinal ischemia Invest. Ophthalmol. Visual Sci. 2003 44 5383 5395
59. M. Theodoropoulou J. Zhang S. Laupheimer M. Paez-Pereda C. Erneux T. Florio U. Pagotto G. K. Stalla Octreotide, a somatostatin analogue, mediates its antiproliferative action in pituitary tumor cells by altering phosphatidylinositol 3-kinase signaling and inducing Zac1 expression Cancer Res. 2006 66 1576 1582
60. E. Fabian D. Reglodi L. Mester A. Szabo K. Szabadfi A. Tamas G. Toth K. Kovacs Effects of PACAP on intracellular signaling pathways in human retinal pigment epithelial cells exposed to oxidative stress J. Mol. Neurosci. 2012 48 493 500
61. K. Gross I. Karagiannides T. Thomou H. W. Koon C. Bowe H. Kim N. Giorgadze T. Tchkonia T. Pirtskhalava J. L. Kirkland C. Pothoulakis Substance P promotes expansion of human mesenteric preadipocytes through proliferative and antiapoptotic pathways Am. J. Physiol. 2009 296 G1012 G1019
62. B. S. Winkler M. J. Arnold M. A. Brassell D. R. Sliter Glucose dependence of glycolysis, hexose monophosphate shunt activity, energy status, and the polyol pathway in retinas isolated from normal (nondiabetic) rats Invest. Ophthalmol. Visual Sci. 1997 38 62 71
63. M. Al-Shabrawey M. Bartoli A. B. El-Remessy D. H. Platt S. Matragoon M. A. Behzadian R. W. Caldwell R. B. Caldwell Inhibition of NAD(P)H oxidase activity blocks vascular endothelial growth factor overexpression and neovascularization during ischemic retinopathy Am. J. Pathol. 2005 167 599 607
64. H. Yokota S. P. Narayanan W. Zhang H. Liu M. Rojas Z. Xu T. Lemtalsi T. Nagaoka A. Yoshida S. E. Brooks R. W. Caldwell R. B. Caldwell Neuroprotection from retinal ischemia/reperfusion injury by NOX2 NADPH oxidase deletion Invest. Ophthalmol. Visual Sci. 2011 52 8123 8131
65. A. K. Berner O. Brouwers R. Pringle I. Klaassen L. Colhoun C. McVicar S. Brockbank J. W. Curry T. Miyata M. Brownlee R. O. Schlingemann C. Schalkwijk A. W. Stitt Protection against methylglyoxal-derived AGEs by regulation of glyoxalase 1 prevents retinal neuroglial and vasodegenerative pathology Diabetologia 2012 55 845 854
66. B. Mannervik Molecular enzymology of the glyoxalase system Drug Metab. Drug Interact. 2008 23 13 27
67. J. Frenzel J. Richter K. J. Eschrich Pyruvate protects glucose-deprived Muller cells from nitric oxide-induced oxidative stress by radical scavenging Glia 2005 52 276 288
68. H. Honda P. Korge J. N. Weiss Mitochondria and ischemia/reperfusion injury Ann. N. Y. Acad. Sci. 2005 1047 248 258
69. G. J. Ghiardi J. M. Gidday S. Roth The purine nucleoside adenosine in retinal ischemia-reperfusion injury Vision Res. 1999 39 2519 2535
70. S. Roth S. S. Park C. W. Sikorski J. Osinski R. Chan K. Loomiset Concentrations of adenosine and its metabolites in the rat retina/choroid during reperfusion after ischemia Curr. Eye Res. 1997 16 875 885
71. S. Roth P. S. Rosenbaum J. Osinski S. S. Park A. Y. Toledano B. Li A. A. Moshfeghi Ischemia induces significant changes in purine nucleoside concentration in the retina-choroid in rats Exp. Eye Res. 1997 65 771 779
72. G. S. Sandhu A. C. Burrier D. R. Janero Adenosine deaminase inhibitors attenuate ischemic injury and preserve energy balance in isolated guinea pig heart Am. J. Physiol. 1993 265 H1249 H1256
73. P. Seeeha D. Hamel Z. Shao Proliferative retinopathies: angiogenesis that blinds Int. J. Biochem. Cell Biol. 2010 42 5 12