Subarachnoid Hemorrhage Increases Level of Heme Oxygenase-1 and Biliverdin Reductase in the Choroid Plexus

. 2020 ; 14 () : 593305. [epub] 20201126

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33328892

Subarachnoid hemorrhage is a specific, life-threatening form of hemorrhagic stroke linked to high morbidity and mortality. It has been found that the choroid plexus of the brain ventricles forming the blood-cerebrospinal fluid barrier plays an important role in subarachnoid hemorrhage pathophysiology. Heme oxygenase-1 and biliverdin reductase are two of the key enzymes of the hemoglobin degradation cascade. Therefore, the aim of present study was to investigate changes in protein levels of heme oxygenase-1 and biliverdin reductase in the rat choroid plexus after experimental subarachnoid hemorrhage induced by injection of non-heparinized autologous blood to the cisterna magna. Artificial cerebrospinal fluid of the same volume as autologous blood was injected to mimic increased intracranial pressure in control rats. Immunohistochemical and Western blot analyses were used to monitor changes in the of heme oxygenase-1 and biliverdin reductase levels in the rat choroid plexus after induction of subarachnoid hemorrhage or artificial cerebrospinal fluid application for 1, 3, and 7 days. We found increased levels of heme oxygenase-1 and biliverdin reductase protein in the choroid plexus over the entire period following subarachnoid hemorrhage induction. The level of heme oxygenase-1 was the highest early (1 and 3 days) after subarachnoid hemorrhage indicating its importance in hemoglobin degradation. Increased levels of heme oxygenase-1 were also observed in the choroid plexus epithelial cells at all time points after application of artificial cerebrospinal fluid. Biliverdin reductase protein was detected mainly in the choroid plexus epithelial cells, with levels gradually increasing during subarachnoid hemorrhage. Our results suggest that heme oxygenase-1 and biliverdin reductase are involved not only in hemoglobin degradation but probably also in protecting choroid plexus epithelial cells and the blood-cerebrospinal fluid barrier from the negative effects of subarachnoid hemorrhage.

Zobrazit více v PubMed

Almeida A. S., Queiroga C. S. F., Sousa M. F. Q., Alves P. M., Vieira H. L. A. (2012). Carbon monoxide modulates apoptosis by reinforcing oxidative metabolism in astrocytes: role of Bcl-2. PubMed DOI PMC

Baranano D. E., Rao M., Ferris C. D., Snyder S. H. (2002). Biliverdin reductase: a major physiologic cytoprotectant. PubMed DOI PMC

Basiglio C. L., Arriaga S. M., Pelusa F., Almará A. M., Kapitulnik J., Mottino A. D. (2010). Complement activation and disease: protective effects of hyperbilirubinaemia. PubMed DOI

Blackburn S. L., Kumar P. T., McBride D., Zeineddine H. A., Leclerc J., Choi H. A., et al. (2018). Unique contribution of haptoglobin and haptoglobin genotype in aneurysmal subarachnoid hemorrhage. PubMed DOI PMC

Brazda V., Muller P., Brozkova K., Vojtesek B. (2006). Restoring wild-type conformation and DNA-binding activity of mutant p53 is insufficient for restoration of transcriptional activity. PubMed DOI

Buehler P. W., Humar R., Schaer D. J. (2020). Haptoglobin therapeutics and compartmentalization of cell-Free hemoglobin toxicity. PubMed DOI

Chang E. F., Claus C. P., Vreman H. J., Wong R. J., Noble-Haeusslein L. J. (2005). Heme regulation in traumatic brain injury: relevance to the adult and developing brain. PubMed DOI

Chen W., Maghzal G. J., Ayer A., Suarna C., Dunn L. L., Stocker R. (2018). Absence of the biliverdin reductase-a gene is associated with increased endogenous oxidative stress. PubMed DOI

Conzen C., Becker K., Albanna W., Weiss M., Bach A., Lushina N., et al. (2019). The acute phase of experimental subarachnoid hemorrhage: intracranial pressure dynamics and their effect on cerebral blood flow and autoregulation. PubMed DOI

d’Avella D., Cicciarello R., Zuccarello M., Albiero F., Romano A., Angileri F. F., et al. (1996). Brain energy metabolism in the acute stage of experimental subarachnoid haemorrhage: local changes in cerebral glucose utilization. PubMed DOI

Dijkstra C. D., Damoiseaux J. G. (1993). Macrophage heterogeneity established by immune-cytochemistry. PubMed DOI

Dubový P., Brázda V., Klusáková I., Hradilová-Svíženská I. (2013). Bilateral elevation of interleukin-6 protein and mRNA in both lumbar and cervical dorsal root ganglia following unilateral chronic compression injury of the sciatic nerve. PubMed DOI PMC

Dubový P., Klusáková I., Svíženská I. (2002). A quantitative immunohistochemical study of the endoneurium in the rat dorsal and ventral spinal roots. PubMed DOI

Etminan N., Chang H.-S., Hackenberg K., de Rooij N. K., Vergouwen M. D. I., Rinkel G. J. E., et al. (2019). Worldwide incidence of aneurysmal subarachnoid hemorrhage according to region, time period, blood pressure, and smoking prevalence in the population: a systematic review and meta-analysis. PubMed DOI PMC

Ewing J. F., Weber C. M., Maines M. D. (1993). Biliverdin reductase is heat resistant and coexpressed with constitutive and heat shock forms of heme oxygenase in brain. PubMed DOI

Fabriek B. O., Dijkstra C. D., van den Berg T. K. (2005). The macrophage scavenger receptor CD163. PubMed DOI

Galea J., Cruickshank G., Teeling J. L., Boche D., Garland P., Perry V. H., et al. (2012). The intrathecal CD163-haptoglobin-hemoglobin scavenging system in subarachnoid hemorrhage: hemoglobin scavenging in subarachnoid hemorrhage. PubMed DOI PMC

Garton T., Hua Y., Xiang J., Xi G., Keep R. F. (2017a). Challenges for intraventricular hemorrhage research and emerging therapeutic targets. PubMed DOI PMC

Garton T., Keep R. F., Hua Y., Xi G. (2017b). CD163, a hemoglobin/haptoglobin scavenger receptor, after intracerebral hemorrhage: functions in microglia/macrophages versus neurons. PubMed DOI

Germanò A. F., Dixon C. E., d’Avella D., Hayes R. L., Tomasello F. (1994). Behavioral deficits following experimental subarachnoid hemorrhage in the rat. PubMed DOI

Gram M., Sveinsdottir S., Cinthio M., Sveinsdottir K., Hansson S. R., Mörgelin M., et al. (2014). Extracellular hemoglobin - mediator of inflammation and cell death in the choroid plexus following preterm intraventricular hemorrhage. PubMed DOI PMC

Gram M., Sveinsdottir S., Ruscher K., Hansson S. R., Cinthio M., Åkerström B., et al. (2013). Hemoglobin induces inflammation after preterm intraventricular hemorrhage by methemoglobin formation. PubMed DOI PMC

Hernangómez M., Klusáková I., Joukal M., Hradilová-Svíženská I., Guaza C., Dubový P. (2016). CD200R1 agonist attenuates glial activation, inflammatory reactions, and hypersensitivity immediately after its intrathecal application in a rat neuropathic pain model. PubMed DOI PMC

Hosoya Y., Fujita T. (1973). Scanning electron microscope observation of intraventricular macrophages (Kolmer cells) in the rat brain. PubMed DOI

Hugelshofer M., Buzzi R. M., Schaer C. A., Richter H., Akeret K., Anagnostakou V., et al. (2019). Haptoglobin administration into the subarachnoid space prevents hemoglobin-induced cerebral vasospasm. PubMed DOI PMC

Hylden J. L., Wilcox G. L. (1980). Intrathecal morphine in mice: a new technique. PubMed DOI

Jansen S., Kress E., Fragoulis A., Wruck C. H. J., Wolf R., Grotzinger J., et al. (2017). Psoriasin has divergent effects on the innate immune responses of murine glial cells. PubMed DOI

Jansen T., Daiber A. (2012). Direct antioxidant properties of bilirubin and biliverdin. Is there a role for biliverdin reductase? PubMed DOI PMC

Kapitulnik J. (2004). Bilirubin: an endogenous product of heme degradation with both cytotoxic and cytoprotective properties. PubMed DOI

Karimy J. K., Zhang J., Kurland D. B., Theriault B. C., Duran D., Stokum J. A., et al. (2017). Inflammation-dependent cerebrospinal fluid hypersecretion by the choroid plexus epithelium in posthemorrhagic hydrocephalus. PubMed DOI

Kikuchi A., Park S.-Y., Miyatake H., Sun D., Sato M., Yoshida T., et al. (2001). Crystal structure of rat biliverdin reductase. PubMed DOI

Kwon M., Woo S., Kurland D., Yoon S., Palmer A., Banerjee U., et al. (2015). Methemoglobin is an endogenous toll-like receptor 4 ligand –relevance to subarachnoid hemorrhage. PubMed DOI PMC

Ling E.-A., Kaur C., Lu J. (1998). Origin, nature, and some functional considerations of intraventricular macrophages, with special reference to the epiplexus cells. PubMed DOI

Liszczak T. M., Black P. M., Tzouras A., Foley L., Zervas N. T. (1984). Morphological changes of the basilar artery, ventricles, and choroid plexus after experimental SAH. PubMed DOI

Lucke-Wold B., Logsdon A., Manoranjan B., Turner R., McConnell E., Vates G., et al. (2016). Aneurysmal subarachnoid hemorrhage and neuroinflammation: a comprehensive review. PubMed DOI PMC

Maines M. D. (2005). New insights into biliverdin reductase functions: linking heme metabolism to cell signaling. PubMed DOI

Matz P., Turner C., Weinstein P. R., Massa S. M., Panter S. S., Sharp F. R. (1996). Heme-oxygenase-1 induction in glia throughout rat brain following experimental subarachnoid hemorrhage. PubMed DOI

McDonagh A. F. (2001). Turning green to gold. PubMed DOI

McDonagh A. F. (2010). The biliverdin–bilirubin antioxidant cycle of cellular protection: missing a wheel? PubMed DOI

McMenamin P. G., Wealthall R. J., Deverall M., Cooper S. J., Griffin B. (2003). Macrophages and dendritic cells in the rat meninges and choroid plexus: three-dimensional localisation by environmental scanning electron microscopy and confocal microscopy. PubMed DOI

Mendez N. V., Wharton J. A., Leclerc J. L., Blackburn S. L., Douglas-Escobar M. V., Weiss M. D., et al. (2013). Clinical implications of bilirubin-associated neuroprotection and neurotoxicity. PubMed PMC

Morita T., Perrella M. A., Lee M. E., Kourembanas S. (1995). Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. PubMed DOI PMC

Nakaso K., Kitayama M., Mizuta E., Fukuda H., Ishii T., Nakashima K., et al. (2000). Co-induction of heme oxygenase-1 and peroxiredoxin I in astrocytes and microglia around hemorrhagic region in the rat brain. PubMed DOI

Nitti M., Piras S., Brondolo L., Marinari U., Pronzato M., Furfaro A. (2018). Heme oxygenase 1 in the nervous system: does it favor neuronal cell survival or induce neurodegeneration? PubMed DOI PMC

Noguchi M., Yoshida T., Kikuchi G. (1979). Specific requirement of NADPH-cytochrome c reductase for the microsomal heme oxygenase reaction yielding biliverdin IXα. PubMed DOI

Polfliet M. M. J., Fabriek B. O., Daniëls W. P., Dijkstra C. D., van den Berg T. K. (2006). The rat macrophage scavenger receptor CD163: expression, regulation and role in inflammatory mediator production. PubMed DOI

Prunell G. F., Mathiesen T., Diemer N. H., Svendgaard N.-A. (2003). Experimental subarachnoid hemorrhage: subarachnoid blood volume, mortality rate, neuronal death, cerebral blood flow, and perfusion pressure in three different rat models. PubMed DOI

Prunell G. F., Mathiesen T., Svendgaard N.-A. (2002). A new experimental model in rats for study of the pathophysiology of subarachnoid hemorrhage. PubMed DOI

Regan R. F., Panter S. S. (1993). Neurotoxicity of hemoglobin in cortical cell culture. PubMed DOI

Sadrzadeh S. M., Anderson D. K., Panter S. S., Hallaway P. E., Eaton J. W. (1987). Hemoglobin potentiates central nervous system damage. PubMed DOI PMC

Schallner N., Pandit R., LeBlanc R., Thomas A. J., Ogilvy C. S., Zuckerbraun B. S., et al. (2015). Microglia regulate blood clearance in subarachnoid hemorrhage by heme oxygenase-1. PubMed DOI PMC

Sedlak T. W., Saleh M., Higginson D. S., Paul B. D., Juluri K. R., Snyder S. H. (2009). Bilirubin and glutathione have complementary antioxidant and cytoprotective roles. PubMed DOI PMC

Sehba F. A., Pluta R. M., Zhang J. H. (2011). Metamorphosis of subarachnoid hemorrhage research: from delayed vasospasm to early brain injury. PubMed DOI PMC

Sharma N., Tramutola A., Lanzillotta C., Arena A., Blarzino C., Cassano T. (2019). Loss of biliverdin reductase-A favors tau hyper-phosphorylation in Alzheimer’s disease. PubMed DOI

Shibahara S., Kitamuro T., Takahashi K. (2002). Heme degradation and human disease: diversity is the soul of life. PubMed DOI

Simard P. F., Tosun C., Melnichenko L., Ivanova S., Gerzanich V., Simard J. M. (2011). Inflammation of the choroid plexus and ependymal layer of the ventricle following intraventricular hemorrhage. PubMed DOI PMC

Solár P., Klusáková I., Jančálek R., Dubový P., Joukal M. (2020a). Subarachnoid hemorrhage induces dynamic immune cell reactions in the choroid plexus. PubMed DOI PMC

Solár P., Zamani A., Kubíčková L., Dubový P., Joukal M. (2020b). Choroid plexus and the blood–cerebrospinal fluid barrier in disease. PubMed DOI PMC

Solomon R. A., Antunes J. L., Chen R. Y., Bland L., Chien S. (1985). Decrease in cerebral blood flow in rats after experimental subarachnoid hemorrhage: a new animal model. PubMed DOI

Stec D. E., Gordon D. M., Nestor-Kalinoski A. L., Donald M. C., Mitchell Z. L., Creeden J. F. (2020). Biliverdin reductase A (BVRA) knockout in adipocytes induces hypertrophy and reduces mitochondria in white fat of obese mice. PubMed DOI PMC

Suzuki H., Kanamaru K., Tsunoda H., Inada H., Kuroki M., Sun H., et al. (1999). Heme oxygenase-1 gene induction as an intrinsic regulation against delayed cerebral vasospasm in rats. PubMed DOI PMC

Suzuki H., Muramatsu M., Kojima T., Taki W. (2003). Intracranial heme metabolism and cerebral vasospasm after aneurysmal subarachnoid hemorrhage. PubMed DOI

Turner C. P., Panter S. S., Sharp F. R. (1999). Anti-oxidants prevent focal rat brain injury as assessed by induction of heat shock proteins (HSP70, HO-1/HSP32, HSP47) following subarachnoid injections of lysed blood. PubMed DOI

Vermeulen M., Hasan D., Blijenberg B. G., Hijdra A., van Gijn J. (1989). Xanthochromia after subarachnoid haemorrhage needs no revisitation. PubMed DOI PMC

Wd L., Wj X., Sh A. (1999). Protective role of heme oxygenase-1 in oxidative stress-induced neuronal injury. PubMed DOI

Wegiel B., Otterbein L. E. (2012). Go green: the anti-inflammatory effects of biliverdin reductase. PubMed DOI PMC

Willis D., Moore A. R., Frederick R., Willoughby D. A. (1996). Heme oxygenase: a novel target for the modulation of inflammatory response. PubMed DOI

Wolburg H., Paulus W. (2010). Choroid plexus: biology and pathology. PubMed DOI

Xu X., Zhi T., Chao H., Jiang K., Liu Y., Bao Z., et al. (2018). ERK1/2/mTOR/Stat3 pathway-mediated autophagy alleviates traumatic brain injury-induced acute lung injury. PubMed DOI

Yeo N., Terrett L., Gupta A. K. (2019). Contemporary management of aneurysmal subarachnoid hemorrhage: a literature review. DOI

Zamboni L., DeMartino C. (1967). Buffered picric-acid formaldehyde: a new rapid fixation for electron microscopy.

Zhang L., Zhang Z., Liu B., Jin Y., Tian Y., Xin Y., et al. (2017). The protective effect of heme oxygenase-1 against intestinal barrier dysfunction in cholestatic liver injury is associated with NF-κB inhibition. PubMed DOI PMC

Zhang Y., Ding Y., Lu T., Zhang Y., Xu N., Yu L., et al. (2018). Biliverdin reductase-A improves neurological function in a germinal matrix hemorrhage rat model. PubMed DOI PMC

Zoerle T., Lombardo A., Colombo A., Longhi L., Zanier E. R., Rampini P., et al. (2015). Intracranial pressure after subarachnoid hemorrhage. PubMed DOI

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...