Neuroglobin Expression in the Brain: a Story of Tissue Homeostasis Preservation

Overview

Journal Mol Neurobiol

Specialties Molecular Biology
Neurology

Date 2018 Jul 12

PMID 29992530

Citations 21

Authors

Zoe P Van Acker

Evi Luyckx

Sylvia Dewilde

Affiliations

Soon will be listed here.

Abstract

After its discovery in 2000, the notion grew that neuroglobin, a neuronal specific heme protein, is involved in cytoprotection. To date, neuroglobin levels have been positively correlated with a beneficial outcome in a plethora of neurotoxic insults, e.g., ischemic and traumatic brain injuries and Alzheimer's disease. The first part of this review goes further into these changes of neuroglobin expression upon different neuronal insults as well as the underlying regulation. In the second part, we shed light on the mechanisms by which neuroglobin contributes to neuroprotection, being (i) the scavenging and detoxification of reactive oxygen/nitrogen species, (ii) the augmentation of the threshold for apoptosis initiation, (iii) its contribution to an anti-inflammatory milieu, and (iv) tissue regeneration. We also consider different neuroglobin models to address as yet unanswered questions. Based on the recent findings and progress in the field, we invigorate the avenues of neuroglobin in neurological ailments to increase in the coming years.

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References

Burmester T, Hankeln T . Function and evolution of vertebrate globins. Acta Physiol (Oxf). 2014; 211(3):501-14. DOI: 10.1111/apha.12312. View

Jayaraman T, Tejero J, Chen B, Blood A, Frizzell S, Shapiro C . 14-3-3 binding and phosphorylation of neuroglobin during hypoxia modulate six-to-five heme pocket coordination and rate of nitrite reduction to nitric oxide. J Biol Chem. 2011; 286(49):42679-42689. PMC: 3234913. DOI: 10.1074/jbc.M111.271973. View

Emara M, Salloum N, Allalunis-Turner J . Expression and hypoxic up-regulation of neuroglobin in human glioblastoma cells. Mol Oncol. 2009; 3(1):45-53. PMC: 5527870. DOI: 10.1016/j.molonc.2008.11.002. View

Yu Z, Zhang Y, Liu N, Yuan J, Lin L, Zhuge Q . Roles of Neuroglobin Binding to Mitochondrial Complex III Subunit Cytochrome c1 in Oxygen-Glucose Deprivation-Induced Neurotoxicity in Primary Neurons. Mol Neurobiol. 2015; 53(5):3249-3257. DOI: 10.1007/s12035-015-9273-4. View

Fabrizius A, Andre D, Laufs T, Bicker A, Reuss S, Porto E . Critical re-evaluation of neuroglobin expression reveals conserved patterns among mammals. Neuroscience. 2016; 337:339-354. DOI: 10.1016/j.neuroscience.2016.07.042. View

Khan A, Mao X, Banwait S, DerMardirossian C, Bokoch G, Jin K . Regulation of hypoxic neuronal death signaling by neuroglobin. FASEB J. 2008; 22(6):1737-47. PMC: 2746758. DOI: 10.1096/fj.07-100784. View

Chen X, Liu Y, Zhang L, Zhu P, Zhu H, Yang Y . Long-term neuroglobin expression of human astrocytes following brain trauma. Neurosci Lett. 2015; 606:194-9. DOI: 10.1016/j.neulet.2015.09.002. View

Wawrowski A, Gerlach F, Hankeln T, Burmester T . Changes of globin expression in the Japanese medaka (Oryzias latipes) in response to acute and chronic hypoxia. J Comp Physiol B. 2010; 181(2):199-208. DOI: 10.1007/s00360-010-0518-2. View

Tian J, Cai T, Yuan Z, Wang H, Liu L, Haas M . Binding of Src to Na+/K+-ATPase forms a functional signaling complex. Mol Biol Cell. 2005; 17(1):317-26. PMC: 1345669. DOI: 10.1091/mbc.e05-08-0735. View

10.

Baez-Jurado E, Vega G, Aliev G, Tarasov V, Esquinas P, Echeverria V . Blockade of Neuroglobin Reduces Protection of Conditioned Medium from Human Mesenchymal Stem Cells in Human Astrocyte Model (T98G) Under a Scratch Assay. Mol Neurobiol. 2017; 55(3):2285-2300. DOI: 10.1007/s12035-017-0481-y. View

11.

Paltrinieri L, Di Rocco G, Battistuzzi G, Borsari M, Sola M, Ranieri A . Computational evidence support the hypothesis of neuroglobin also acting as an electron transfer species. J Biol Inorg Chem. 2017; 22(4):615-623. DOI: 10.1007/s00775-017-1455-2. View

12.

Ye Q, Sun Y, Wu Y, Gao Y, Li Z, Li W . Pichia pastoris Production of Tat-NGB and Its Neuroprotection on Rat Pheochromocytoma Cells. Mol Biotechnol. 2015; 58(1):22-9. DOI: 10.1007/s12033-015-9898-6. View

13.

Di Giulio C, Zara S, Cataldi A, Porzionato A, Pokorski M, De Caro R . Human carotid body HIF and NGB expression during human development and aging. Adv Exp Med Biol. 2012; 758:265-71. DOI: 10.1007/978-94-007-4584-1_36. View

14.

Cardinale A, Fusco F, Paldino E, Giampa C, Marino M, Nuzzo M . Localization of neuroglobin in the brain of R6/2 mouse model of Huntington's disease. Neurol Sci. 2017; 39(2):275-285. DOI: 10.1007/s10072-017-3168-2. View

15.

Yu Z, Liu N, Li Y, Xu J, Wang X . Neuroglobin overexpression inhibits oxygen-glucose deprivation-induced mitochondrial permeability transition pore opening in primary cultured mouse cortical neurons. Neurobiol Dis. 2013; 56:95-103. PMC: 3674158. DOI: 10.1016/j.nbd.2013.04.015. View

16.

Van Acker Z, Luyckx E, Van Leuven W, Geuens E, De Deyn P, Van Dam D . Impaired hypoxic tolerance in APP23 mice: a dysregulation of neuroprotective globin levels. FEBS Lett. 2017; 591(10):1321-1332. PMC: 5518225. DOI: 10.1002/1873-3468.12651. View

17.

Li R, Pouranfar F, Lee S, Morris M, Wang Y, Gozal D . Neuroglobin protects PC12 cells against beta-amyloid-induced cell injury. Neurobiol Aging. 2007; 29(12):1815-22. PMC: 2586918. DOI: 10.1016/j.neurobiolaging.2007.05.001. View

18.

Ye S, Zhou X, Lai X, Zheng L, Chen X . Silencing neuroglobin enhances neuronal vulnerability to oxidative injury by down-regulating 14-3-3gamma. Acta Pharmacol Sin. 2009; 30(7):913-8. PMC: 4006654. DOI: 10.1038/aps.2009.70. View

19.

Ma Y, Freitag P, Zhou J, Brune B, Frede S, Fandrey J . Thyroid hormone induces erythropoietin gene expression through augmented accumulation of hypoxia-inducible factor-1. Am J Physiol Regul Integr Comp Physiol. 2004; 287(3):R600-7. DOI: 10.1152/ajpregu.00115.2004. View

20.

Vinay D, Ryan E, Pawelec G, Talib W, Stagg J, Elkord E . Immune evasion in cancer: Mechanistic basis and therapeutic strategies. Semin Cancer Biol. 2015; 35 Suppl:S185-S198. DOI: 10.1016/j.semcancer.2015.03.004. View