{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,6]],"date-time":"2026-03-06T01:28:52Z","timestamp":1772760532982,"version":"3.50.1"},"reference-count":35,"publisher":"Springer Science and Business Media LLC","issue":"1","funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["Go 2158\/3-1"],"award-info":[{"award-number":["Go 2158\/3-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["Bi 1567\/2-1"],"award-info":[{"award-number":["Bi 1567\/2-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Neuroinflammation"],"published-print":{"date-parts":[[2017,12]]},"DOI":"10.1186\/s12974-017-0905-7","type":"journal-article","created":{"date-parts":[[2017,6,27]],"date-time":"2017-06-27T07:52:22Z","timestamp":1498549942000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":30,"title":["The Carbon monoxide releasing molecule ALF-186 mediates anti-inflammatory and neuroprotective effects via the soluble guanylate cyclase \u00df1 in rats\u2019 retinal ganglion cells after ischemia and reperfusion injury"],"prefix":"10.1186","volume":"14","author":[{"given":"Felix","family":"Ulbrich","sequence":"first","affiliation":[]},{"given":"Claus","family":"Hagmann","sequence":"additional","affiliation":[]},{"given":"Hartmut","family":"Buerkle","sequence":"additional","affiliation":[]},{"given":"Carlos C.","family":"Romao","sequence":"additional","affiliation":[]},{"given":"Nils","family":"Schallner","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9991-3226","authenticated-orcid":false,"given":"Ulrich","family":"Goebel","sequence":"additional","affiliation":[]},{"given":"Julia","family":"Biermann","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2017,6,27]]},"reference":[{"key":"905_CR1","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.ejphar.2012.12.007","volume":"700","author":"NRD Costa","year":"2013","unstructured":"Costa NRD, Silva RO, Nicolau LAD, Lucetti LT, Santana APM, Arag\u00e3o KS, et al. Role of soluble guanylate cyclase activation in the gastroprotective effect of the HO-1\/CO pathway against alendronate-induced gastric damage in rats. Eur J Pharmacol. 2013;700:51\u20139.","journal-title":"Eur J Pharmacol"},{"key":"905_CR2","doi-asserted-by":"crossref","first-page":"1587","DOI":"10.1016\/S0002-9440(10)63515-8","volume":"163","author":"A Nakao","year":"2003","unstructured":"Nakao A, Kimizuka K, Stolz DB, Neto JS, Kaizu T, Choi AMK, et al. Carbon monoxide inhalation protects rat intestinal grafts from ischemia\/reperfusion injury. Am J Pathol. 2003;163:1587\u201398.","journal-title":"Am J Pathol"},{"key":"905_CR3","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1097\/01.tp.0000188637.80695.7f","volume":"81","author":"A Nakao","year":"2006","unstructured":"Nakao A, Toyokawa H, Abe M, Kiyomoto T, Nakahira K, Choi AMK, et al. Heart Allograft Protection with Low-Dose Carbon Monoxide Inhalation: Effects on Inflammatory Mediators and Alloreactive T-cell Responses. Transplantation. 2006;81:220\u201330.","journal-title":"Transplantation"},{"key":"905_CR4","doi-asserted-by":"crossref","first-page":"F979","DOI":"10.1152\/ajprenal.00158.2004","volume":"287","author":"JS Neto","year":"2004","unstructured":"Neto JS. Protection of transplant-induced renal ischemia-reperfusion injury with carbon monoxide. Am J Physiol Renal Physiol. 2004;287:F979\u201389.","journal-title":"Am J Physiol Renal Physiol"},{"key":"905_CR5","doi-asserted-by":"crossref","unstructured":"Qin W, Zhang J, Lv W, Wang X, Sun B. Effect of carbon monoxide-releasing molecules II-liberated CO on suppressing inflammatory response in sepsis by interfering with nuclear factor kappa B activation. Gao H, editor. PloS ONE. Public Library of Science; 2013;8:e75840.","DOI":"10.1371\/journal.pone.0075840"},{"key":"905_CR6","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1016\/j.jss.2005.11.130","volume":"130","author":"J Kohmoto","year":"2006","unstructured":"Kohmoto J, Nakao A, KAIZU T, TSUNG A, Ikeda A, TOYOKAWA H, et al. Low dose carbon monoxide inhalation prevents ischemia\/reperfusion injury of transplanted rat lung grafts via inhibition of ERK1\/2. J Surg Res. 2006;130:208.","journal-title":"J Surg Res"},{"key":"905_CR7","doi-asserted-by":"crossref","unstructured":"Kaizu T, Ikeda A, Nakao A, Tsung A, Toyokawa H, Ueki S, et al. Protection of transplant-induced hepatic ischemia\/reperfusion injury with carbon monoxide via MEK\/ERK1\/2 pathway downregulation. American Journal of Physiology-Gastrointestinal and Liver Physiology. American Physiological Society; 2008;294:G236\u201344.","DOI":"10.1152\/ajpgi.00144.2007"},{"key":"905_CR8","first-page":"L688","volume":"276","author":"LE Otterbein","year":"1999","unstructured":"Otterbein LE, Mantell LL, Choi AMK. Carbon monoxide provides protection against hyperoxic lung injury. Am J Physiol. 1999;276:L688\u201394.","journal-title":"Am J Physiol"},{"key":"905_CR9","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1038\/74680","volume":"6","author":"LE Otterbein","year":"2000","unstructured":"Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med. 2000;6:422\u20138.","journal-title":"Nat Med"},{"key":"905_CR10","doi-asserted-by":"crossref","first-page":"L312","DOI":"10.1152\/ajplung.2000.278.2.L312","volume":"278","author":"I Petrache","year":"2000","unstructured":"Petrache I, Otterbein LE, Alam J, Wiegand GW, Choi AM. Heme oxygenase-1 inhibits TNF-alpha-induced apoptosis in cultured fibroblasts. Am J Physiol Lung Cell Mol Physiol. 2000;278:L312\u20139.","journal-title":"Am J Physiol Lung Cell Mol Physiol"},{"key":"905_CR11","doi-asserted-by":"crossref","unstructured":"Frost RB, Farrer TJ, Primosch M, Hedges DW. Prevalence of traumatic brain injury in the general adult population: a meta-analysis. Neuroepidemiology. Karger Publishers; 2013;40:154\u20139.","DOI":"10.1159\/000343275"},{"key":"905_CR12","doi-asserted-by":"crossref","first-page":"1747","DOI":"10.1016\/S0140-6736(06)68770-9","volume":"367","author":"AD Lopez","year":"2006","unstructured":"Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJL. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet. 2006;367:1747\u201357.","journal-title":"Lancet"},{"key":"905_CR13","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1097\/00001199-200609000-00001","volume":"21","author":"JA Langlois","year":"2006","unstructured":"Langlois JA, Rutland-Brown W, Wald MM. The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil. 2006;21:375\u20138.","journal-title":"J Head Trauma Rehabil"},{"key":"905_CR14","doi-asserted-by":"crossref","unstructured":"Queiroga CSF, Tomasi S, Wideroe M, Alves PM, Vercelli A, Vieira HLA. Preconditioning triggered by carbon monoxide (CO) provides neuronal protection following perinatal hypoxia-ischemia. Borlongan CV, editor. PloS ONE. Public Library of Science; 2012;7:e42632.","DOI":"10.1371\/journal.pone.0042632"},{"key":"905_CR15","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1002\/cpt.10","volume":"97","author":"A Dasgupta","year":"2015","unstructured":"Dasgupta A, Bowman L, D\u2019Arsigny CL, Archer SL. Soluble Guanylate Cyclase: A New Therapeutic Target for Pulmonary Arterial Hypertension and Chronic Thromboembolic Pulmonary Hypertension. Clin Pharmacol Ther. 2015;97:88\u2013102.","journal-title":"Clin Pharmacol Ther"},{"key":"905_CR16","unstructured":"Biermann J, Lagr\u00e8ze WA, Dimitriu C, Stoykow C, Goebel U. Preconditioning with inhalative carbon monoxide protects rat retinal ganglion cells from ischemia\/reperfusion injury. Invest. Ophthalmol Vis Sci. The Association for Research in Vision and Ophthalmology; 2010;51:3784\u201391."},{"key":"905_CR17","unstructured":"Tomiyama K, Ikeda A, Ueki S, Nakao A, Stolz DB, Koike Y, et al. Inhibition of Kupffer Cell-mediated early proinflammatory response with carbon monoxide in transplant-induced hepatic ischemia\/reperfusion injury in rats. Hepatology. Wiley Subscription Services, Inc., A Wiley Company; 2008;48:1608\u201320."},{"key":"905_CR18","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1038\/ki.2014.80","volume":"86","author":"Y Ruan","year":"2014","unstructured":"Ruan Y, Wang L, Zhao Y, Yao Y, Chen S, Li J, et al. Carbon monoxide potently prevents ischemia-induced high-mobility group box 1 translocation and release and protects against lethal renal ischemia-reperfusion injury. Kidney Int. 2014;86:525\u201337.","journal-title":"Kidney Int"},{"key":"905_CR19","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/j.yjmcc.2011.11.005","volume":"52","author":"AB Stein","year":"2012","unstructured":"Stein AB, Bolli R, Dawn B, Sanganalmath SK, Zhu Y, Wang O-L, et al. Carbon monoxide induces a late preconditioning-mimetic cardioprotective and antiapoptotic milieu in the myocardium. J Mol Cell Cardiol. 2012;52:228\u201336.","journal-title":"J Mol Cell Cardiol"},{"key":"905_CR20","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1111\/j.1471-4159.2008.05610.x","volume":"107","author":"HLA Vieira","year":"2008","unstructured":"Vieira HLA, Queiroga CSF, Alves PM. Pre-conditioning induced by carbon monoxide provides neuronal protection against apoptosis. J Neurochem. 2008;107:375\u201384.","journal-title":"J Neurochem"},{"key":"905_CR21","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1111\/jnc.13653","volume":"138","author":"AS Almeida","year":"2016","unstructured":"Almeida AS, Sonnewald U, Alves PM, Vieira HLA. Carbon monoxide improves neuronal differentiation and yield by increasing the functioning and number of mitochondria. J Neurochem. 2016;138:423\u201335.","journal-title":"J Neurochem"},{"key":"905_CR22","unstructured":"Fujimoto H, Ohno M, Ayabe S, Kobayashi H, Ishizaka N, Kimura H, et al. Carbon monoxide protects against cardiac ischemia\u2014reperfusion injury in vivo via MAPK and Akt--eNOS pathways. Arterioscler Thromb Vasc Biol. American Heart Association, Inc; 2004;24:1848\u201353."},{"key":"905_CR23","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1038\/sj.ki.5000016","volume":"69","author":"A Sandouka","year":"2006","unstructured":"Sandouka A, Fuller BJ, Mann BE, Green CJ, Foresti R, Motterlini R. Treatment with CO-RMs during cold storage improves renal function at reperfusion. Kidney Int. 2006;69:239\u201347.","journal-title":"Kidney Int"},{"key":"905_CR24","doi-asserted-by":"crossref","first-page":"2605","DOI":"10.1161\/STROKEAHA.110.607101","volume":"42","author":"B Wang","year":"2011","unstructured":"Wang B, Cao W, Biswal S, Dor\u00e9 S. Carbon Monoxide-Activated Nrf2 Pathway Leads to Protection Against Permanent Focal Cerebral Ischemia. Stroke. 2011;42:2605\u2013U369.","journal-title":"Stroke"},{"key":"905_CR25","doi-asserted-by":"crossref","unstructured":"Mahan VL, Zurakowski D, Otterbein LE, Pigula FA. Inhaled carbon monoxide provides cerebral cytoprotection in pigs. Meisel A, editor. PloS ONE. Public Library of Science; 2012;7.","DOI":"10.1371\/journal.pone.0041982"},{"key":"905_CR26","doi-asserted-by":"publisher","unstructured":"Wei Y, Chen P, de Bruyn M, Zhang W, Bremer E, Helfrich W. Carbon monoxide-Releasing Molecule-2 (CORM-2) attenuates acute hepatic ischemia reperfusion injury in rats. BMC Gastroenterol. BioMed Central. 2010;10:42. doi: 10.1186\/1471-230X-10-42 . PMID:20444253. PMCID:PMC2873601.","DOI":"10.1186\/1471-230X-10-42"},{"key":"905_CR27","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1196\/annals.1344.007","volume":"1053","author":"MA Yenari","year":"2005","unstructured":"Yenari MA, Liu JL, Zheng Z, Vexler ZS, Lee JE, Giffard RG. Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection. Ann N Y Acad Sci. 2005;1053:74\u201383.","journal-title":"Ann N Y Acad Sci"},{"key":"905_CR28","doi-asserted-by":"crossref","first-page":"s55","DOI":"10.1185\/030079902125000732","volume":"18","author":"S Kelly","year":"2002","unstructured":"Kelly S, Yenari MA. Neuroprotection: Heat Shock Proteins. Curr Med Res Opin. 2002;18:s55\u201360.","journal-title":"Curr Med Res Opin"},{"key":"905_CR29","doi-asserted-by":"crossref","first-page":"379","DOI":"10.18388\/abp.2014_1910","volume":"61","author":"Z Banecka-Majkutewicz","year":"2014","unstructured":"Banecka-Majkutewicz Z, Grabowski M, Kadzinski L, Papkov A, Wegrzyn A, Banecki B. Increased levels of antibodies against heat shock proteins in stroke patients. Acta Biochim Pol. 2014;61:379\u201383.","journal-title":"Acta Biochim Pol"},{"key":"905_CR30","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.brainres.2014.12.019","volume":"1599","author":"D He","year":"2015","unstructured":"He D, Song X, Li L. Geranylgeranylacetone protects against cerebral ischemia and reperfusion injury: HSP90 and eNOS phosphorylation involved. Brain Res. 2015;1599:150\u20137.","journal-title":"Brain Res"},{"key":"905_CR31","unstructured":"Meng J-L, Mei W-Y, Dong Y-F, Wang J-H, Zhao C-M, Lan A-P, et al. Heat shock protein 90 mediates cytoprotection by H2S against chemical hypoxia-induced injury in PC12 cells. Clin Exp Pharmacol Physiol. Blackwell Publishing Ltd; 2011;38:42\u20139."},{"key":"905_CR32","first-page":"1275","volume":"17","author":"J Biermann","year":"2011","unstructured":"Biermann J, Lagr\u00e8ze WA, Schallner N, Schwer CI, Goebel U. Inhalative preconditioning with hydrogen sulfide attenuated apoptosis after retinal ischemia\/reperfusion injury. Mol Vis. 2011;17:1275\u201386.","journal-title":"Mol Vis"},{"key":"905_CR33","unstructured":"Kim N, Kim JY, Yenari MA. Anti-inflammatory properties and pharmacological induction of Hsp70 after brain injury. Inflammopharmacology. SP Birkh\u00e4user Verlag Basel; 2012;20:177\u201385."},{"key":"905_CR34","doi-asserted-by":"crossref","unstructured":"Bettaga N, Jaeger R, Duennes S, Groneberg D, Friebe A. Cell-specific impact of nitric oxide-dependent guanylyl cyclase on arteriogenesis and angiogenesis in mice. Angiogenesis. Springer Netherlands; 2015;18:245\u201354.","DOI":"10.1007\/s10456-015-9463-8"},{"key":"905_CR35","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/j.ejphar.2015.07.009","volume":"764","author":"A Mori","year":"2015","unstructured":"Mori A, Namekawa R, Hasebe M, Saito M, Sakamoto K, Nakahara T, et al. Involvement of prostaglandin I-2 in nitric oxide-induced vasodilation of retinal arterioles in rats. Eur J Pharmacol. 2015;764:249\u201355.","journal-title":"Eur J Pharmacol"}],"container-title":["Journal of Neuroinflammation"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12974-017-0905-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,9,27]],"date-time":"2019-09-27T02:00:08Z","timestamp":1569549608000},"score":1,"resource":{"primary":{"URL":"http:\/\/jneuroinflammation.biomedcentral.com\/articles\/10.1186\/s12974-017-0905-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,6,27]]},"references-count":35,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2017,12]]}},"alternative-id":["905"],"URL":"https:\/\/doi.org\/10.1186\/s12974-017-0905-7","relation":{},"ISSN":["1742-2094"],"issn-type":[{"value":"1742-2094","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,6,27]]},"article-number":"130"}}