Top

Published in:

Open Access 01-12-2017 | Research

Nicorandil potentiates sodium butyrate induced preconditioning of neurons and enhances their survival upon subsequent treatment with H₂O₂

Authors: Parisa Tabeshmehr, Haider Kh Husnain, Mahin Salmannejad, Mahsa Sani, Seyed Mojtaba Hosseini, Mohammad Hossein Khorraminejad Shirazi

Published in: Translational Neurodegeneration | Issue 1/2017

Abstract

Background

Extensive loss of donor neural stem cell (NSCs) due to ischemic stress and low rate of differentiation at the site of cell graft are two of the major issues that hamper optimal outcome in NSCs transplantation studies. Given that histone deacetylases (HDACs) modulate various cellular processes by deacetylating histones and non-histone proteins, we hypothesized that combined treatment with small molecules, sodium butyrate (NaB; a known HDAC inhibitor) and nicorandil, will enhance the rate neuronal differentiation of NSCs besides their preconditioning to resist oxidative stress.

Methods

NSCs derived from 14-day old Sprague Dawley rat ganglion eminence were characterized for tri-lineage differentiation. Treatment with 1 mM NaB significantly changed their culture characteristics while continuous treatment for 10 days enhanced their neural differentiation. NaB treatment also preconditioned the cells for their resistance to oxidative stress.

Results

The highest rate of neural differentiation and preconditioning effect was achieved when the NSCs were treated concomitantly with NaB and nicorandil. Cell proliferation assay showed that concomitant treatment with NaB and nicorandil retarded their rate of proliferation.

Conclusion

These data conclude that preconditioning of NSCs with NaB and nicorandil effectively enhances their differentiation capacity besides preconditioning the cells to support their survival under ischemic conditions.

Available only for authorised users

Zhao Y, Zuo Y, Jiang J, Yan H, Wang X, Huo H, et al. Neural stem cell transplantation combined with erythropoietin for the treatment of spinal cord injury in rats. Exp Thera Med. 2016;12(4):2688–94.CrossRef

Lee IH, Huang SS, Chuang CY, Liao KH, Chang LH, Chuang CC, Su YS, Lin HJ, Hsieh JY, Su SH, Lee OK. Delayed epidural transplantation of human induced pluripotent stem cell-derived neural progenitors enhances functional recovery after stroke. Sci Rep. 2017;7(1):1943.CrossRefPubMedPubMedCentral

Bjugstad KB, Rael LT, Levy S, Carrick M, Mains CW, Slone DS, et al. Oxidation-reduction potential as a biomarker for severity and acute outcome in traumatic brain injury. Oxid Med Cell Longev. 2016;2016:9.CrossRef

Lu J, Xie L, Liu C, Zhang Q, Sun S. PTEN/PI3k/AKT regulates macrophage polarization in emphysematous mice. Scand J Immunol. 2017;85(6):395-405. doi:10.1111/sji.12545.

Zhou Q, Dalgard CL, Wynder C, Doughty ML. Histone deacetylase inhibitors SAHA and sodium butyrate block G1-to-S cell cycle progression in neurosphere formation by adult sub-ventricular cells. BMC Neurosci. 2011;12(1):1.CrossRef

Hsing CH, Hung SK, Chen YC, Wei TS, Sun DP, Wang JJ, et al. Histone deacetylase inhibitor trichostatin a ameliorated endotoxin-induced neuro-inflammation and cognitive dysfunction. Mediat Inflamm. 2015;27:2015.

Ziemka-Nalecz M, Jaworska J, Sypecka J, Polowy R, Filipkowski RK, Zalewska T. Sodium butyrate, a Histone Deacetylase inhibitor, exhibits Neuroprotective/Neurogenic effects in a rat model of neonatal hypoxia-ischemia. Mol Neurobiol. 2017;54(7):5300-18.

Siebzehnrubl FA, Buslei R, Eyupoglu IY, Seufert S, Hahnen E, Blumcke I. Histone deacetylase inhibitors increase neuronal differentiation in adult forebrain precursor cells. Exp Brain Res. 2007;176(4):672–8.CrossRefPubMed

Alvarez AA, Field M, Bushnev S, Longo MS, Sugaya K. The effects of histone deacetylase inhibitors on glioblastoma-derived stem cells. J Mol Neurosci. 2015;55(1):7–20.CrossRefPubMed

10.

Fung H, Demple B. A vital role for Ape1/Ref1 protein in repairing spontaneous DNA damage in human cells. Mol Cell. 2005;17:463–70.CrossRefPubMed

11.

Domenis R, Bergamin N, Gianfranceschi G, Vascotto C, Romanello M, Rigo S, et al. The redox function of APE1 is involved in the differentiation process of stem cells toward a neuronal cell fate. PLoS One. 2014;9(2):e89232.CrossRefPubMedPubMedCentral

12.

Poletto M, Vascotto C, Scognamiglio PL, Lirussi L, Marasco D. Role of the unstructured N-terminal domain of the hAPE1 (human apurinic/apyrimidinic endonuclease-1) in the modulation of its interaction with nucleic acids and NPM1 (nucleophosmin). Biochem J. 2013;452:545–57.CrossRefPubMed

13.

Jason M, Kaski JC. Vasodilator therapy: nitrates and Nicorandil. Cardiovasc Drugs Ther. 2016; 10.1007/s10557-016-6668-z.

14.

Georgiadis MM, Chen Q, Meng J, Guo C, Wireman R, Reed A, et al. Small molecule activation of apurinic/apyrimidinic endonuclease 1 reduces DNA damage induced by cisplatin in cultured sensory neurons. DNA Repair (Amst). 2016;41:32–41.CrossRef

15.

Zhou Y, Wang Q, Evers BM, Chung DH. Signal transduction pathways involved in oxidative stress-induced intestinal epithelial cell apoptosis. Pediatric Res. 2005;58(6):1192–7.CrossRef

16.

So EC, Chen YC, Wang SC, Wu CC, Huang MC, Lai MS, et al. Midazolam regulated caspase pathway, endoplasmic reticulum stress, autophagy, and cell cycle to induce apoptosis in MA-10 mouse Leydig tumor cells. Onco Targets Ther. 2016;9:2519.PubMedPubMedCentral

17.

Boland K, Flanagan L, Prehn JH. Paracrine control of tissue regeneration and cell proliferation by Caspase-3. Cell Death Dis. 2013;4(7):e725.CrossRefPubMedPubMedCentral

18.

Amariglio N, Hirshberg A, Scheithauer BW, et al. Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med. 2009;6:e1000029.CrossRefPubMedPubMedCentral

19.

Radtke C, Redeker J, Jokuszies A, et al. In vivo transformation of neural stem cells following transplantation in the injured nervous system. J Reconstr Microsurg. 2010;26:211–2.CrossRefPubMed

20.

Wu W, He Q, Li X, Zhang X, Lu A, Ge R, et al. Long-term cultured human neural stem cells undergo spontaneous transformation to tumor-initiating cells. Int J Biol Sci. 2011;7:892–901.CrossRefPubMedPubMedCentral

21.

Kaus A, Widera D, Kassmer S, Peter J, Zaenker K, Kaltschmidt C, et al. Neural stem cells adopt tumorigenic properties by constitutively activated NF-kappaB and subsequent VEGF up-regulation. Stem Cells Dev. 2010;19(7):999–1015.CrossRefPubMed

22.

Zhao LN, Wang P, Liu YH, Cai H, Ma J, Liu LB, Xi Z, Li ZQ, Liu XB, Xue YX. Mir-383 inhibits proliferation, migration and angiogenesis of glioma-exposed endothelial cells in vitro via vegf-mediated fak and src signaling pathways. Cellular signalling. 2017;30:142-53.

23.

Lange C, Garcia MT, Decimo I, Bifari F, Eelen G, Quaegebeur A, et al. Relief of hypoxia by angiogenesis promotes neural stem cell differentiation by targeting glycolysis. EMBO J. 2016;35(9):924–41.CrossRefPubMedPubMedCentral

24.

Lim S, Kaldis P. Loss of Cdk2 and Cdk4 induces a switch from proliferation to differentiation in neural stem cells. Stem Cells. 2012;30:1509–20.CrossRefPubMed

25.

Dokmanovic M, Clarke C, Marks PA. Histone Deacetylase inhibitors: overview and perspectives. Mol Cancer Res. 2007;5(10):981–9.CrossRefPubMed

26.

Lagger G. O’Carro ll D, Rembold M et al. essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J. 2002;21:2672–81.CrossRefPubMedPubMedCentral

27.

Marks PA, Jiang X. Histone deacetylase inhibitors in programmed cell death and cancer therapy. Cell Cycle. 2005;4(4):549–51.CrossRefPubMed

28.

Marks PA, Xu WS. Histone deacetylase inhibitors: potential in cancer therapy. J Cell Biochem. 2009;107(4):600–8.CrossRefPubMedPubMedCentral

29.

Elmi M, Matsumoto Y, Zeng ZJ, Lakshminarasimhan P, Yang W, Uemura A, et al. TLX activates MASH1 forinduction of neuronal lineage commitment of adult hippocampal neuroprogenitors. Mol Cell Neurosci. 2010;45(2):121–31.CrossRefPubMed

30.

Roth SY, Denu JM, Allis CD. Histone acetyltransferases. Annu Rev Biochem. 2001;70:81–120.CrossRefPubMed

31.

Gregory PD, Wagner K, Horz W. Histone acetylation and chromatin remodeling. Exp Cell Res. 2001;265:195–202.CrossRefPubMed

32.

Thiagalingam S, Cheng KH, Lee HJ, Mineva N, Thiagalingam A, Ponte JF. Histone deacetylases: unique players in shaping the epigenetic histone code. Ann N Y Acad Sci. 2003;983:84–100.CrossRefPubMed

33.

Richon VM, Sandhoff TW, Rifkind RA, Marks PA. Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc Natl Acad Sci U S A. 2000;97:10014–9.CrossRefPubMedPubMedCentral

34.

Hsieh J, Nakashima K, Kuwabara T, Mejia E, Gage FH. Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci U S A. 2004;101(47):16659–64.CrossRefPubMedPubMedCentral

35.

Chu W, Yuan J, Huang L, Xiang X, Zhu H, Chen F, et al. Valproic acid arrests proliferation but promotes neuronal differentiation of adult spinal NSPCs from SCI rats. Neurochem Res. 2015;40(7):1472–86.CrossRefPubMed

36.

Biermann J, Boyle J, Pielen A, Lagrè WA. Histone deacetylase inhibitors sodium butyrate and valproic acid delay spontaneous cell death in purified rat retinal ganglion cells. Mol Vis. 2011;17:395–403.PubMedPubMedCentral

37.

Sun J, Wang F, Li H, Zhang H, Jin J, Chen W, et al. Neuroprotective effect of sodium butyrate against cerebral ischemia/reperfusion injury in mice. Biomed Res Int. 2015 May;7:2015.

38.

Valvassori SS, Dal-Pont GC, Steckert AV, Varela RB, Lopes-Borges J, Mariot E, et al. Sodium butyrate has an antimanic effect and protects the brain against oxidative stress in an animal model of mania induced by ouabain. Psychiatry Res. 2016;235:154–9.CrossRefPubMed

39.

Georgiadis MM, Luo M, Gaur RK, Delaplane S, Li X, Kelley MR. Evolution of the redox function in mammalian apurinic/apyrimidinic endonuclease. Mutat Res. 2008;643:54–63.CrossRefPubMedPubMedCentral

40.

Luo M, Zhang J, He H, Su D, Chen Q, Gross ML, et al. Characterization of the redox activity and disulfide bond formation in apurinic/apyrimidinic endonuclease. Biochemist. 2012;51:695–705.CrossRef

41.

Park MS, Kim CS, Joo HK, Lee YR, Kang G, Kim SJ, et al. Cytoplasmic localization and redox cysteine residue of APE1/Ref-1 are associated with its anti-inflammatory activity in cultured endothelial cells. Mol Cells. 2013;36:439–45.CrossRefPubMedPubMedCentral

42.

Idris NM1, Ashraf M, Ahmed RP, Shujia J, Haider KH. Activation of IL-11/STAT3 pathway in preconditioned human skeletal myoblasts blocks apoptotic cascade under oxidant stress. Regen Med. 2012;7(1):47–57.CrossRefPubMed

43.

Niagara MI, Haider HK, Jiang S, Ashraf M. Pharmacologically preconditioned skeletal myoblasts are resistant to oxidative stress and promote angiomyogenesis via release of paracrine factors in the infarcted heart. Circ Res. 2007;100(4):545–55.CrossRefPubMed

44.

Xiang J, Wan C, Guo R, Guo D. Is hydrogen peroxide a suitable apoptosis inducer for all cell types? Biomed Res Int. Volume 2016, Article ID 7343965, 6-pages. http://dx.doi.org/10.1155/2016/7343965.

Title: Nicorandil potentiates sodium butyrate induced preconditioning of neurons and enhances their survival upon subsequent treatment with H2O2
Authors: Parisa Tabeshmehr
Haider Kh Husnain
Mahin Salmannejad
Mahsa Sani
Seyed Mojtaba Hosseini
Mohammad Hossein Khorraminejad Shirazi
Publication date: 01-12-2017
Publisher: BioMed Central
Published in: Translational Neurodegeneration / Issue 1/2017
Electronic ISSN: 2047-9158
DOI: https://doi.org/10.1186/s40035-017-0097-1

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Nicorandil potentiates sodium butyrate induced preconditioning of neurons and enhances their survival upon subsequent treatment with H₂O₂

Abstract

Background

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 1/2017

The development prospection of HDAC inhibitors as a potential therapeutic direction in Alzheimer’s disease

Rest tremor revisited: Parkinson’s disease and other disorders

Disease modification and Neuroprotection in neurodegenerative disorders

Mild cognitive impairment in Parkinson’s disease: a distinct clinical entity?

Environmental insults: critical triggers for amyotrophic lateral sclerosis

The role of cognitive activity in cognition protection: from Bedside to Bench