Angiotensin II type-2 receptor stimulation induces neuronal VEGF synthesis after cerebral ischemia

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1862, Issue 7, 2016, Pages 1297-1308

  Mateos, Laura ^a,b   Perez Alvarez, Maria Jose ^b,c   Wandosell, Francisco ^b,d  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

AT2 receptor; Ischemic stroke; MCAO; Oxygen glucose deprivation and VEGF

Indexed keywords

ANGIOTENSIN 2 RECEPTOR; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROTEIN KINASE B; VASCULOTROPIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN ISCHEMIA; BRAIN LEVEL; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; IN VITRO STUDY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL CULTURE; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REPERFUSION; SIGNAL TRANSDUCTION; TRANSIENT ISCHEMIC ATTACK; UPREGULATION;

EID: 84963944142     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2016.03.013     Document Type: Article

References (50)

1. Dirnagl U., Iadecola C., Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 1999, 22(9):391-397.
2. Hacke W., Kaste M., Bluhmki E., Brozman M., Davalos A., Guidetti D., Larrue V., Lees K.R., Medeghri Z., Machnig T., Schneider D., von Kummer R., Wahlgren N., Toni D. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N. Engl. J. Med. 2008, 359(13):1317-1329. 10.1056/NEJMoa0804656.
3. Perez-Alvarez M.J., Maza Mdel C., Anton M., Ordonez L., Wandosell F. Post-ischemic estradiol treatment reduced glial response and triggers distinct cortical and hippocampal signaling in a rat model of cerebral ischemia. J. Neuroinflammation 2012, 9:157. 10.1186/1742-2094-9-157.
4. Casals J.B., Pieri N.C.G., Feitosa M.L.T., Ercolin A.C.M., Roballo K.C.S., Barreto R.S.N., Bressan F.F., Martins D.S., Miglino M.A., Ambrosio C.E. The use of animal models for stroke research: a review. Commun. Med. 2011, 61(4):305-313.
5. Mogi M., Kawajiri M., Tsukuda K., Matsumoto S., Yamada T., Horiuchi M. Serum levels of renin-angiotensin system components in acute stroke patients. Geriatr. Gerontol. Int. 2014, 14(4):793-798. 10.1111/ggi.12167.
6. Grobe J.L., Xu D., Sigmund C.D. An intracellular renin-angiotensin system in neurons: fact, hypothesis, or fantasy. Physiology 2008, 23:187-193. 10.1152/physiol.00002.2008.
7. Chapman N., Huxley R., Anderson C., Bousser M.G., Chalmers J., Colman S., Davis S., Donnan G., MacMahon S., Neal B., Warlow C., Woodward M. Effects of a perindopril-based blood pressure-lowering regimen on the risk of recurrent stroke according to stroke subtype and medical history: the PROGRESS trial. Stroke 2004, 35(1):116-121. 10.1161/01.STR.0000106480.76217.6F.
8. Mateos L., Ismail M.A., Gil-Bea F.J., Schule R., Schols L., Heverin M., Folkesson R., Bjorkhem I., Cedazo-Minguez A. Side chain-oxidized oxysterols regulate the brain renin-angiotensin system through a liver X receptor-dependent mechanism. J. Biol. Chem. 2011, 286(29):25574-25585. 10.1074/jbc.M111.236877.
9. Li J., Culman J., Hortnagl H., Zhao Y., Gerova N., Timm M., Blume A., Zimmermann M., Seidel K., Dirnagl U., Unger T. Angiotensin AT2 receptor protects against cerebral ischemia-induced neuronal injury. FASEB J. 2005, 19(6):617-619. 10.1096/fj.04-2960fje.
10. Iwai M., Liu H.W., Chen R., Ide A., Okamoto S., Hata R., Sakanaka M., Shiuchi T., Horiuchi M. Possible inhibition of focal cerebral ischemia by angiotensin II type 2 receptor stimulation. Circulation 2004, 110(7):843-848. 10.1161/01.CIR.0000138848.58269.80.
11. de Gasparo M., Catt K.J., Inagami T., Wright J.W., Unger T. The angiotensin II receptors. Pharmacol. Rev. 2000, 52(3):415-472.
12. McCarthy C.A., Vinh A., Callaway J.K., Widdop R.E. Angiotensin AT2 receptor stimulation causes neuroprotection in a conscious rat model of stroke. Stroke 2009, 40(4):1482-1489. 10.1161/STROKEAHA.108.531509.
13. Dorrance A.M. Angiotensin II type 2 receptor agonists as therapies for ischemic stroke. Hypertension 2012, 60(6):1391-1392. 10.1161/HYPERTENSIONAHA.112.200956.
14. Alhusban A., Fouda A.Y., Pillai Bindu, Ishrat T., Soliman S., Fagan S.C. Compound 21 is pro-angiogenic in the brain and results in sustained recovery after ischemic stroke. J. Hypertens. 2015, 33(1):170-180. 10.1097/hjh.0000000000000364.
15. Rosenstein J.M., Krum J.M., Ruhrberg C. VEGF in the nervous system. Organogenesis 2010, 6(2):107-114.
16. Mackenzie F., Ruhrberg C. Diverse roles for VEGF-A in the nervous system. Development 2012, 139(8):1371-1380. 10.1242/dev.072348.
17. Ogunshola O.O., Antic A., Donoghue M.J., Fan S.Y., Kim H., Stewart W.B., Madri J.A., Ment L.R. Paracrine and autocrine functions of neuronal vascular endothelial growth factor (VEGF) in the central nervous system. J. Biol. Chem. 2002, 277(13):11410-11415. 10.1074/jbc.M111085200.
18. Krum J.M., Khaibullina A. Inhibition of endogenous VEGF impedes revascularization and astroglial proliferation: roles for VEGF in brain repair. Exp. Neurol. 2003, 181(2):241-257. 10.3201/eid0906.020485.
19. Leker R.R., Teichner A., Ovadia H., Keshet E., Reinherz E., Ben-Hur T. Expression of endothelial nitric oxide synthase in the ischemic penumbra: relationship to expression of neuronal nitric oxide synthase and vascular endothelial growth factor. Brain Res. 2001, 909(1-2):1-7.
20. Hayashi T., Abe K., Suzuki H., Itoyama Y. Rapid induction of vascular endothelial growth factor gene expression after transient middle cerebral artery occlusion in rats. Stroke 1997, 28(10):2039-2044.
21. Sun Y., Jin K., Xie L., Childs J., Mao X.O., Logvinova A., Greenberg D.A. VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J. Clin. Invest. 2003, 111(12):1843-1851. 10.1172/JCI17977.
22. Jin K.L., Mao X.O., Greenberg D.A. Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc. Natl. Acad. Sci. U. S. A. 2000, 97(18):10242-10247.
23. Zan L., Zhang X., Xi Y., Wu H., Song Y., Teng G., Li H., Qi J., Wang J. Src regulates angiogenic factors and vascular permeability after focal cerebral ischemia-reperfusion. Neuroscience 2014, 262:118-128. 10.1016/j.neuroscience.2013.12.060.
24. Zhang Z.G., Zhang L., Tsang W., Soltanian-Zadeh H., Morris D., Zhang R., Goussev A., Powers C., Yeich T., Chopp M. Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2002, 22(4):379-392. 10.1097/00004647-200204000-00002.
25. Wan Y., Wallinder C., Plouffe B., Beaudry H., Mahalingam A.K., Wu X., Johansson B., Holm M., Botoros M., Karlen A., Pettersson A., Nyberg F., Fandriks L., Gallo-Payet N., Hallberg A., Alterman M. Design, synthesis, and biological evaluation of the first selective nonpeptide AT2 receptor agonist. J. Med. Chem. 2004, 47(24):5995-6008. 10.1021/jm049715t.
26. Kaschina E., Grzesiak A., Li J., Foryst-Ludwig A., Timm M., Rompe F., Sommerfeld M., Kemnitz U.R., Curato C., Namsolleck P., Tschope C., Hallberg A., Alterman M., Hucko T., Paetsch I., Dietrich T., Schnackenburg B., Graf K., Dahlof B., Kintscher U., Unger T., Steckelings U.M. Angiotensin II type 2 receptor stimulation: a novel option of therapeutic interference with the renin-angiotensin system in myocardial infarction?. Circulation 2008, 118(24):2523-2532. 10.1161/CIRCULATIONAHA.108.784868.
27. Yrjanheikki J., Koistinaho J., Kettunen M., Kauppinen R.A., Appel K., Hull M., Fiebich B.L. Long-term protective effect of atorvastatin in permanent focal cerebral ischemia. Brain Res. 2005, 1052(2):174-179. 10.1016/j.brainres.2005.06.004.
28. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2007, Academic Press, San Diego, California. sixth ed.
29. Türeyen K., Vemuganti R., Sailor K.A., Dempsey R.J. Infarct volume quantification in mouse focal cerebral ischemia: a comparison of triphenyltetrazolium chloride and cresyl violet staining techniques. J. Neurosci. Methods 2004, 139(2):203-207. 10.1016/j.jneumeth.2004.04.029.
30. Mateos L., Akterin S., Gil-Bea F.J., Spulber S., Rahman A., Bjorkhem I., Schultzberg M., Flores-Morales A., Cedazo-Minguez A. Activity-regulated cytoskeleton-associated protein in rodent brain is down-regulated by high fat diet in vivo and by 27-hydroxycholesterol in vitro. Brain Pathol. 2009, 19(1):69-80. 10.1111/j.1750-3639.2008.00174.x.
31. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001, 25(4):402-408. 10.1006/meth.2001.1262.
32. Perez-Alvarez M.J., Mateos L., Alonso A., Wandosell F. Estradiol and progesterone administration after pMCAO stimulates the neurological recovery and reduces the detrimental effect of ischemia mainly in hippocampus. Mol. Neurobiol. 2014, 10.1007/s12035-014-8963-7.
33. Jing F., Mogi M., Sakata A., Iwanami J., Tsukuda K., Ohshima K., Min L.J., Steckelings U.M., Unger T., Dahlof B., Horiuchi M. Direct stimulation of angiotensin II type 2 receptor enhances spatial memory. J. Cereb. Blood Flow Metab. 2012, 32(2):248-255. 10.1038/jcbfm.2011.133.
34. Sun Y.Y., Lin S.H., Lin H.C., Hung C.C., Wang C.Y., Lin Y.C., Hung K.S., Lien C.C., Kuan C.Y., Lee Y.H. Cell type-specific dependency on the PI3K/Akt signaling pathway for the endogenous Epo and VEGF induction by baicalein in neurons versus astrocytes. PLoS One 2013, 8(7). 10.1371/journal.pone.0069019.
35. Ruggero D., Sonenberg N. The Akt of translational control. Oncogene 2005, 24(50):7426-7434. 10.1038/sj.onc.1209098.
36. Wang Y., Jin K., Mao X.O., Xie L., Banwait S., Marti H.H., Greenberg D.A. VEGF-overexpressing transgenic mice show enhanced post-ischemic neurogenesis and neuromigration. J. Neurosci. Res. 2007, 85(4):740-747.
37. Lennmyr F., Ata K.A., Funa K., Olsson Y., Terent A. Expression of vascular endothelial growth factor (VEGF) and its receptors (Flt-1 and Flk-1) following permanent and transient occlusion of the middle cerebral artery in the rat. J. Neuropathol. Exp. Neurol. 1998, 57(9):874-882.
38. Joseph J.P., Mecca A.P., Regenhardt R.W., Bennion D.M., Rodriguez V., Desland F., Patel N.A., Pioquinto D.J., Unger T., Katovich M.J., Steckelings U.M., Sumners C. The angiotensin type 2 receptor agonist compound 21 elicits cerebroprotection in endothelin-1 induced ischemic stroke. Neuropharmacology 2014, 81:134-141. 10.1016/j.neuropharm.2014.01.044.
39. Alhusban A., Fouda A.Y., Bindu P., Ishrat T., Soliman S., Fagan S.C. Compound 21 is pro-angiogenic in the brain and results in sustained recovery after ischemic stroke. J. Hypertens. 2014, 10.1097/HJH.0000000000000364.
40. Min L.J., Mogi M., Tsukuda K., Jing F., Ohshima K., Nakaoka H., Kan-No H., Wang X.L., Chisaka T., Bai H.Y., Iwanami J., Horiuchi M. Direct stimulation of angiotensin II type 2 receptor initiated after stroke ameliorates ischemic brain damage. Am. J. Hypertens. 2014, 27(8):1036-1044. 10.1093/ajh/hpu015.
41. McCarthy C.A., Vinh A., Miller A.A., Hallberg A., Alterman M., Callaway J.K., Widdop R.E. Direct angiotensin AT2 receptor stimulation using a novel AT2 receptor agonist, compound 21, evokes neuroprotection in conscious hypertensive rats. PLoS One 2014, 9(4). 10.1371/journal.pone.0095762.
42. Adams H.P., del Zoppo G., Alberts M.J., Bhatt D.L., Brass L., Furlan A., Grubb R.L., Higashida R.T., Jauch E.C., Kidwell C., Lyden P.D., Morgenstern L.B., Qureshi A.I., Rosenwasser R.H., Scott P.A., Wijdicks E.F. Guidelines for the early management of adults with ischemic stroke: a guideline from the American Heart Association/American Stroke Association Stroke Council, Clinical Cardiology Council, Cardiovascular Radiology and Intervention Council, and the Atherosclerotic Peripheral Vascular Disease and Quality of Care Outcomes in Research Interdisciplinary Working Groups: the American Academy of Neurology affirms the value of this guideline as an educational tool for neurologists. Stroke 2007, 38(5):1655-1711. 10.1161/STROKEAHA.107.181486.
43. Benicky J., Hafko R., Sanchez-Lemus E., Aguilera G., Saavedra J.M. Six commercially available angiotensin II AT1 receptor antibodies are non-specific. Cell. Mol. Neurobiol. 2012, 32(8):1353-1365. 10.1007/s10571-012-9862-y.
44. Hafko R., Villapol S., Nostramo R., Symes A., Sabban E.L., Inagami T., Saavedra J.M. Commercially available angiotensin II At(2) receptor antibodies are nonspecific. PLoS One 2013, 8(7). 10.1371/journal.pone.0069234.
45. Reinecke K., Lucius R., Reinecke A., Rickert U., Herdegen T., Unger T. Angiotensin II accelerates functional recovery in the rat sciatic nerve in vivo: role of the AT2 receptor and the transcription factor NF-kappaB. FASEB J. 2003, 17(14):2094-2096. 10.1096/fj.02-1193fje.
46. Shraim N., Mertens B., Clinckers R., Sarre S., Michotte Y., Van Eeckhaut A. Microbore liquid chromatography with UV detection to study the in vivo passage of compound 21, a non-peptidergic AT(2) receptor agonist, to the striatum in rats. J. Neurosci. Methods 2011, 202(2):137-142. 10.1016/j.jneumeth.2011.06.009.
47. Kondo T., Reaume A.G., Huang T.T., Carlson E., Murakami K., Chen S.F., Hoffman E.K., Scott R.W., Epstein C.J., Chan P.H. Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J. Neurosci. 1997, 17(11):4180-4189.
48. Ohashi H., Takagi H., Oh H., Suzuma K., Suzuma I., Miyamoto N., Uemura A., Watanabe D., Murakami T., Sugaya T., Fukamizu A., Honda Y. Phosphatidylinositol 3-kinase/Akt regulates angiotensin II-induced inhibition of apoptosis in microvascular endothelial cells by governing survivin expression and suppression of caspase-3 activity. Circ. Res. 2004, 94(6):785-793. 10.1161/01.RES.0000121103.03275.EC.
49. Li Y.N., Pan R., Qin X.J., Yang W.L., Qi Z., Liu W., Liu K.J. Ischemic neurons activate astrocytes to disrupt endothelial barrier via increasing VEGF expression. J. Neurochem. 2014, 129(1):120-129. 10.1111/jnc.12611.
50. Rosenstein J.M., Mani N., Khaibullina A., Krum J.M. Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons. J. Neurosci. 2003, 23(35):11036-11044.