Vascular signal transducer and activator of transcription-3 promotes angiogenesis and neuroplasticity long-term after stroke

Circulation

Volumn 131, Issue 20, 2015, Pages 1772-1782

  Hoffmann, Christian J ^a   Harms, Ulrike ^a   Rex, Andre ^a   Szulzewsky, Frank ^b   Wolf, Susanne A ^b   Grittner, Ulrike ^a   Lättig Tünnemann, Gisela ^a   Sendtner, Michael ^c   Kettenmann, Helmut ^a,b   Dirnagl, Ulrich ^a,d,e   Endres, Matthias ^a,d,e   Harms, Christoph ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^e German Cancer Consortium (DKTK)   (Germany)

Author keywords

Angiogenesis effect; Brain ischemia; Endothelial cells; Inflammation; Microarray analysis

Indexed keywords

ADAMTS1 PROTEIN; ADAMTS9 PROTEIN; CD11B ANTIGEN; CD31 ANTIGEN; CD45 ANTIGEN; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN; UNCLASSIFIED DRUG; ADAM PROTEIN; ADAMTS9 PROTEIN, MOUSE; SCLEROPROTEIN; STAT3 PROTEIN, MOUSE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; BRAIN DAMAGE; BRAIN HISTOLOGY; BRAIN ISCHEMIA; CELL LOSS; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; IMMUNOFLUORESCENCE; KNOCKOUT MOUSE; LONG TERM SURVIVAL; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE REGENERATION; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WILD TYPE; ANIMAL; BIOSYNTHESIS; BRAIN; BRAIN CIRCULATION; CEREBRAL ARTERY DISEASE; CONVALESCENCE; DEFICIENCY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MICROGLIA; NERVE FIBER; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; VASCULAR ENDOTHELIUM;

ADAM PROTEINS; ANIMALS; AXONS; BRAIN; CELLULAR MICROENVIRONMENT; CEREBROVASCULAR CIRCULATION; CONVALESCENCE; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION PROFILING; INFARCTION, MIDDLE CEREBRAL ARTERY; MICE; MICE, KNOCKOUT; MICROGLIA; NEOVASCULARIZATION, PHYSIOLOGIC; NEURONAL PLASTICITY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOVERY OF FUNCTION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84935420116     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.114.013003     Document Type: Article

References (34)

1. Beck H, Plate KH. Angiogenesis after cerebral ischemia. Acta Neuropathol (Berl). 2009;117:481-496. doi: 10.1007/s00401-009-0483-6.
2. Young CC, Brooks KJ, Buchan AM, Szele FG. Cellular and molecular determinants of stroke-induced changes in subventricular zone cell migration. Antioxid Redox Signal. 2011;14:1877-1888. doi: 10.1089/ars.2010.3435.
3. Adams RH, Eichmann A. Axon guidance molecules in vascular patterning. Cold Spring Harb Perspect Biol. 2010;2:a001875. doi: 10.1101/cshperspect.a001875.
4. Ohab JJ, Fleming S, Blesch A, Carmichael ST. A neurovascular niche for neurogenesis after stroke. J Neurosci. 2006;26:13007-13016. doi: 10.1523/JNEUROSCI.4323-06.2006.
5. Funamoto M, Fujio Y, Kunisada K, Negoro S, Tone E, Osugi T, Hirota H, Izumi M, Yoshizaki K, Walsh K, Kishimoto T, Yamauchi-Takihara K. Signal transducer and activator of transcription 3 is required for glycoprotein 130-mediated induction of vascular endothelial growth factor in cardiac myocytes. J Biol Chem. 2000;275:10561-10566.
6. Yahata Y, Shirakata Y, Tokumaru S, Yamasaki K, Sayama K, Hanakawa Y, Detmar M, Hashimoto K. Nuclear translocation of phosphorylated STAT3 is essential for vascular endothelial growth factor-induced human dermal microvascular endothelial cell migration and tube formation. J Biol Chem. 2003;278:40026-40031. doi: 10.1074/jbc.M301866200.
7. Paulin R, Meloche J, Bonnet S. STAT3 signaling in pulmonary arterial hypertension. JAKSTAT. 2012;1:223-233. doi: 10.4161/jkst.22366.
8. Suzuki S, Tanaka K, Nogawa S, Dembo T, Kosakai A, Fukuuchi Y. Phosphorylation of signal transducer and activator of transcription-3 (Stat3) after focal cerebral ischemia in rats. Exp Neurol. 2001;170:63-71. doi: 10.1006/exnr.2001.7701.
9. Loddick SA, Turnbull AV, Rothwell NJ. Cerebral interleukin-6 is neuroprotective during permanent focal cerebral ischemia in the rat. J Cereb Blood Flow Metab. 1998;18:176-179. doi: 10.1097/00004647-199802000-00008.
10. Battle TE, Frank DA. The role of STATs in apoptosis. Curr Mol Med. 2002;2:381-392.
11. Jung JE, Kim GS, Narasimhan P, Song YS, Chan PH. Regulation of Mn-superoxide dismutase activity and neuroprotection by STAT3 in mice after cerebral ischemia. J Neurosci. 2009;29:7003-7014. doi: 10.1523/JNEUROSCI.1110-09.2009.
12. Yamashita T, Sawamoto K, Suzuki S, Suzuki N, Adachi K, Kawase T, Mihara M, Ohsugi Y, Abe K, Okano H. Blockade of interleukin-6 signaling aggravates ischemic cerebral damage in mice: possible involvement of Stat3 activation in the protection of neurons. J Neurochem. 2005;94:459-468. doi: 10.1111/j.1471-4159.2005.03227.x.
13. Dziennis S, Jia T, Rønnekleiv OK, Hurn PD, Alkayed NJ. Role of signal transducer and activator of transcription-3 in estradiol-mediated neuroprotection. J Neurosci. 2007;27:7268-7274. doi: 10.1523/JNEUROSCI.1558-07.2007.
14. Satriotomo I, Bowen KK, Vemuganti R. JAK2 and STAT3 activation contributes to neuronal damage following transient focal cerebral ischemia. J Neurochem. 2006;98:1353-1368. doi: 10.1111/j.1471-4159.2006.04051.x.
15. Gertz K, Kronenberg G, Kälin RE, Baldinger T, Werner C, Balkaya M, Eom GD, Hellmann-Regen J, Kröber J, Miller KR, Lindauer U, Laufs U, Dirnagl U, Heppner FL, Endres M. Essential role of interleukin-6 in post-stroke angiogenesis. Brain. 2012;135(pt 6):1964-1980. doi: 10.1093/brain/aws075.
16. Takeda K, Kaisho T, Yoshida N, Takeda J, Kishimoto T, Akira S. Stat3 activation is responsible for IL-6-dependent T cell proliferation through preventing apoptosis: generation and characterization of T cell-specific Stat3-deficient mice. J Immunol. 1998;161:4652-4660.
17. Forde A, Constien R, Gröne HJ, Hämmerling G, Arnold B. Temporal Cremediated recombination exclusively in endothelial cells using Tie2 regulatory elements. Genesis. 2002;33:191-197. doi: 10.1002/gene.10117.
18. Endres M, Gertz K, Lindauer U, Katchanov J, Schultze J, Schröck H, Nickenig G, Kuschinsky W, Dirnagl U, Laufs U. Mechanisms of stroke protection by physical activity. Ann Neurol. 2003;54:582-590. doi: 10.1002/ana.10722.
19. Gubern C, Hurtado O, Rodríguez R, Morales JR, Romera VG, Moro MA, Lizasoain I, Serena J, Mallolas J. Validation of housekeeping genes for quantitative real-time PCR in in-vivo and in-vitro models of cerebral ischaemia. BMC Mol Biol. 2009;10:57. doi: 10.1186/1471-2199-10-57.
20. Olah M, Amor S, Brouwer N, Vinet J, Eggen B, Biber K, Boddeke HW. Identification of a microglia phenotype supportive of remyelination. Glia. 2012;60:306-321. doi: 10.1002/glia.21266.
21. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4:249-264. doi: 10.1093/biostatistics/4.2.249.
22. Reid MJ, Cross AK, Haddock G, Allan SM, Stock CJ, Woodroofe MN, Buttle DJ, Bunning RA. ADAMTS-9 expression is up-regulated following transient middle cerebral artery occlusion (tMCAo) in the rat. Neurosci Lett. 2009;452:252-257. doi: 10.1016/j.neulet.2009.01.058.
23. Yiu G, He Z. Glial inhibition of CNS axon regeneration. Nat Rev Neurosci. 2006;7:617-627. doi: 10.1038/nrn1956.
24. Bogen O, Dreger M, Gillen C, Schröder W, Hucho F. Identification of versican as an isolectin B4-binding glycoprotein from mammalian spinal cord tissue. FEBS J. 2005;272:1090-1102. doi: 10.1111/j.1742-4658.2005.04543.x.
25. Jung JE, Kim GS, Chan PH. Neuroprotection by interleukin-6 is mediated by signal transducer and activator of transcription 3 and antioxidative signaling in ischemic stroke. Stroke. 2011;42:3574-3579. doi: 10.1161/STROKEAHA.111.626648.
26. Kinouchi T, Kitazato KT, Shimada K, Yagi K, Tada Y, Matsushita N, Sumiyoshi M, Satomi J, Kageji T, Nagahiro S. Activation of signal transducer and activator of transcription-3 by a peroxisome proliferator-activated receptor γ agonist contributes to neuroprotection in the peri-infarct region after ischemia in oophorectomized rats. Stroke. 2012;43:478-483. doi: 10.1161/STROKEAHA.111.618926.
27. Ali C, Nicole O, Docagne F, Lesne S, MacKenzie ET, Nouvelot A, Buisson A, Vivien D. Ischemia-induced interleukin-6 as a potential endogenous neuroprotective cytokine against NMDA receptor-mediated excitotoxicity in the brain. J Cereb Blood Flow Metab. 2000;20:956-966. doi: 10.1097/00004647-200006000-00008.
28. Lin TN, Wang PY, Chi SI, Kuo JS. Differential regulation of ciliary neurotrophic factor (CNTF) and CNTF receptor α (CNTFR α) expression following focal cerebral ischemia. Brain Res Mol Brain Res. 1998;55:71-80.
29. Suzuki S, Tanaka K, Nogawa S, Ito D, Dembo T, Kosakai A, Fukuuchi Y. Immunohistochemical detection of leukemia inhibitory factor after focal cerebral ischemia in rats. J Cereb Blood Flow Metab. 2000;20:661-668. doi: 10.1097/00004647-200004000-00003.
30. Chen Z, Han ZC. STAT3: a critical transcription activator in angiogenesis. Med Res Rev. 2008;28:185-200. doi: 10.1002/med.20101.
31. Kadler KE, Baldock C, Bella J, Boot-Handford RP. Collagens at a glance. J Cell Sci. 2007;120(pt 12):1955-1958. doi: 10.1242/jcs.03453.
32. Koo BH, Coe DM, Dixon LJ, Somerville RP, Nelson CM, Wang LW, Young ME, Lindner DJ, Apte SS. ADAMTS9 is a cell-autonomously acting, antiangiogenic metalloprotease expressed by microvascular endothelial cells. Am J Pathol. 2010;176:1494-1504. doi: 10.2353/ajpath.2010.090655.
33. Lemarchant S, Pruvost M, Montaner J, Emery E, Vivien D, Kanninen K, Koistinaho J. ADAMTS proteoglycanases in the physiological and pathological central nervous system. J Neuroinflammation. 2013;10:133. doi: 10.1186/1742-2094-10-133.
34. Zimmermann DR, Dours-Zimmermann MT. Extracellular matrix of the central nervous system: from neglect to challenge. Histochem Cell Biol. 2008;130:635-653. doi: 10.1007/s00418-008-0485-9.