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Metabolic Brain Disease

, Volume 34, Issue 5, pp 1243–1251 | Cite as

Long non-coding RNAs and cell death following ischemic stroke

  • Masoumeh Alishahi
  • Farhoodeh Ghaedrahmati
  • Tannaz Akbari Kolagar
  • William Winlow
  • Negin Nikkar
  • Maryam Farzaneh
  • Seyed Esmaeil KhoshnamEmail author
Review Article

Abstract

Stroke is a major cause of morbidity and mortality worldwide, and extensive efforts have focused on the improvement of therapeutic strategies to reduce cell death following ischemic stroke. Uncovering the cellular and molecular pathophysiological processes in ischemic stroke have been a top priority. Long noncoding RNAs (lncRNAs) are endogenous molecules that play key roles in the pathophysiology of cerebral ischemia, and involved in the neuronal cell death during ischemic stroke. In recent years, a bulk of aberrantly expressed lncRNAs have been screened out in ischemic stroke insulted animals. LncRNAs along with their targets could affect the genetic machinery at molecular levels, and exploring their functions and mechanisms may be a promising option for ischemic stroke treatment. In this review, we summarize the current knowledge for lncRNAs in ischemic stroke, focusing on the role of specific lncRNAs that may underlie cell death to find possible therapeutic targets.

Keywords

Long non-coding RNA Ischemic stroke Cell death 

Notes

References

  1. Aliaga E, Silhol M, Bonneau N, Maurice T, Arancibia S, Tapia-Arancibia L (2010) Dual response of BDNF to sublethal concentrations of β-amyloid peptides in cultured cortical neurons. Neurobiol Dis 37:208–217CrossRefGoogle Scholar
  2. Alishahi M, Farzaneh M, Ghaedrahmati F, Nejabatdoust A, Sarkaki A, Khoshnam SE (2019) NLRP3 inflammasome in ischemic stroke: as possible therapeutic target. Int J Stroke 1747493019841242Google Scholar
  3. Bao M-H, Szeto V, Yang BB, Zhu S-z, Sun H-S, Feng Z-P (2018) Long non-coding RNAs in ischemic stroke. Cell Death Dis 9:281CrossRefGoogle Scholar
  4. Baucum AJ, Shonesy BC, Rose KL, Colbran RJ (2015) Quantitative proteomics analysis of CaMKII phosphorylation and the CaMKII interactome in the mouse forebrain. ACS Chem Neurosci 6:615–631CrossRefGoogle Scholar
  5. Bhattarai S, Pontarelli F, Prendergast E, Dharap A (2017) Discovery of novel stroke-responsive lncRNAs in the mouse cortex using genome-wide. RNA-seq. Neurobiol Dis 108:204–212CrossRefGoogle Scholar
  6. Boon RA, Jaé N, Holdt L, Dimmeler S (2016) Long noncoding RNAs: from clinical genetics to therapeutic targets? J Am Coll Cardiol 67:1214–1226CrossRefGoogle Scholar
  7. Broadbent NJ, Squire LR, Clark RE (2004) Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci U S A 101:14515–14520CrossRefGoogle Scholar
  8. Brunkow ME, Tilghman S (1991) Ectopic expression of the H19 gene in mice causes prenatal lethality. Genes Dev 5:1092–1101CrossRefGoogle Scholar
  9. Cai H et al (2017) Long non-coding RNA taurine upregulated 1 enhances tumor-induced angiogenesis through inhibiting microRNA-299 in human glioblastoma. Oncogene 36:318CrossRefGoogle Scholar
  10. Carpenter S et al (2013) A long noncoding RNA mediates both activation and repression of immune response genes. science 341:789–792CrossRefGoogle Scholar
  11. Cesana M et al (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous. RNA. Cell 147:358–369CrossRefGoogle Scholar
  12. Chen S et al (2017) LncRNA TUG1 sponges microRNA-9 to promote neurons apoptosis by up-regulated Bcl2l11 under ischemia. Biochem Biophys Res Commun 485:167–173CrossRefGoogle Scholar
  13. Conway E, Healy E, Bracken AP (2015) PRC2 mediated H3K27 methylations in cellular identity and cancer. Curr Opin Cell Biol 37:42–48CrossRefGoogle Scholar
  14. Dharap A, Nakka VP, Vemuganti R (2012) Effect of focal ischemia on long noncoding RNAs. Stroke 43:2800–2802CrossRefGoogle Scholar
  15. Dharap A, Pokrzywa C, Vemuganti R (2013) Increased binding of stroke-induced long non-coding RNAs to the transcriptional corepressors Sin3A and coREST. ASN Neuro 5:AN20130029CrossRefGoogle Scholar
  16. Donkor ES (2018) Stroke in the century: a snapshot of the burden, epidemiology, and quality of life stroke research and treatment 2018Google Scholar
  17. Duan L-J, Ding M, Hou L-J, Cui Y-T, Li C-J, Yu D-M (2017) Long noncoding RNA TUG1 alleviates extracellular matrix accumulation via mediating microRNA-377 targeting of PPARγ in diabetic nephropathy. Biochem Biophys Res Commun 484:598–604CrossRefGoogle Scholar
  18. Dykstra-Aiello C et al (2016) Altered expression of long noncoding RNAs in blood after ischemic stroke and proximity to putative stroke risk loci. Stroke 47:2896–2903CrossRefGoogle Scholar
  19. Ebert MS, Neilson JR, Sharp PA (2007) MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4:721CrossRefGoogle Scholar
  20. Feigin VL, Norrving B, Mensah GA (2017) Global burden of stroke. Circ Res 120:439–448CrossRefGoogle Scholar
  21. Gilgun-Sherki Y, Rosenbaum Z, Melamed E, Offen D (2002) Antioxidant therapy in acute central nervous system injury: current state. Pharmacol Rev 54:271–284CrossRefGoogle Scholar
  22. Gong C, Maquat LE (2011) lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3′ UTRs via Alu elements. Nature 470:284CrossRefGoogle Scholar
  23. Gray CBB, Heller Brown J (2014) CaMKIIdelta subtypes: localization and function. Front Pharmacol 5:15Google Scholar
  24. Group I-C (2012) The benefits and harms of intravenous thrombolysis with recombinant tissue plasminogen activator within 6 h of acute ischaemic stroke (the third international stroke trial [IST-3]): a randomised controlled trial. Lancet 379:2352–2363CrossRefGoogle Scholar
  25. Han X, Yang F, Cao H, Liang Z (2015) Malat1 regulates serum response factor through miR-133 as a competing endogenous RNA in myogenesis. FASEB J 29:3054–3064CrossRefGoogle Scholar
  26. Hawkins KE et al (2017) Targeting resolution of neuroinflammation after ischemic stroke with a lipoxin A4 analog: protective mechanisms and long-term effects on neurological recovery. Brain and behavior 7:e00688CrossRefGoogle Scholar
  27. Hu W, Alvarez-Dominguez JR, Lodish HF (2012) Regulation of mammalian cell differentiation by long non-coding RNAs. EMBO Rep 13:971–983CrossRefGoogle Scholar
  28. Huang H-L, Lin C-C, Jeng K-CG, Yao P-W, Chuang L-T, Kuo S-L, Hou C-W (2012) Fresh green tea and gallic acid ameliorate oxidative stress in kainic acid-induced status epilepticus. J Agric Food Chem 60:2328–2336CrossRefGoogle Scholar
  29. Hudmon A, Kim SA, Kolb SJ, Stoops JK, Waxham MN (2001) Light scattering and transmission electron microscopy studies reveal a mechanism for calcium/calmodulin-dependent protein kinase II self-association. J Neurochem 76:1364–1375CrossRefGoogle Scholar
  30. Iadecola C, Anrather J (2011) The immunology of stroke: from mechanisms to translation. Nat Med 17:796CrossRefGoogle Scholar
  31. Ji T-T, Huang X, Jin J, Pan S-H, Zhuge X-J (2016) Inhibition of long non-coding RNA TUG1 on gastric cancer cell transference and invasion through regulating and controlling the expression of miR-144/c-met axis. Asian Pac J Trop Med 9:508–512CrossRefGoogle Scholar
  32. Ji Y, Guo X, Zhang Z, Huang Z, Zhu J, Chen Q-H, Gui L (2017) CaMKIIδ meditates phenylephrine induced cardiomyocyte hypertrophy through store-operated Ca2+ entry. Cardiovasc Pathol 27:9–17CrossRefGoogle Scholar
  33. Jung JE, Karatas H, Liu Y, Yalcin A, Montaner J, Lo EH, Van Leyen K (2015) STAT-dependent upregulation of 12/15-lipoxygenase contributes to neuronal injury after stroke. J Cereb Blood Flow Metab 35:2043–2051CrossRefGoogle Scholar
  34. Karreth FA et al (2011) In vivo identification of tumor-suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell 147:382–395CrossRefGoogle Scholar
  35. Khalil AM et al (2009) Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci 106:11667–11672CrossRefGoogle Scholar
  36. Khoshnam SE, Sarkaki A, Khorsandi L, Winlow W, Badavi M, Moghaddam HF, Farbooda Y (2017a) Vanillic acid attenuates effects of transient bilateral common carotid occlusion and reperfusion in rats. Biomed Pharmacother 96:667–674CrossRefGoogle Scholar
  37. Khoshnam SE, Winlow W, Farbood Y, Moghaddam HF, Farzaneh M (2017b) Emerging roles of microRNAs in ischemic stroke: as possible therapeutic agents. J Stroke 19:166CrossRefGoogle Scholar
  38. Khoshnam SE, Winlow W, Farzaneh M (2017c) The interplay of MicroRNAs in the inflammatory mechanisms following ischemic stroke. J Neuropathol Exp Neurol 76:548–561CrossRefGoogle Scholar
  39. Khoshnam SE, Winlow W, Farzaneh M, Farbood Y, Moghaddam HF (2017d) Pathogenic mechanisms following ischemic stroke. Neurol Sci 38:1167–1186CrossRefGoogle Scholar
  40. Khoshnam SE, Farbood Y, Moghaddam HF, Sarkaki A, Badavi M, Khorsandi L (2018a) Vanillic acid attenuates cerebral hyperemia, blood-brain barrier disruption and anxiety-like behaviors in rats following transient bilateral common carotid occlusion and reperfusion. Metab Brain Dis:1–9Google Scholar
  41. Khoshnam SE, Sarkaki A, Rashno M, Farbood Y (2018b) Memory deficits and hippocampal inflammation in cerebral hypoperfusion and reperfusion in male rats: Neuroprotective role of vanillic acid Life sciencesGoogle Scholar
  42. Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP (2010) Noncoding RNA gas5 is a growth arrest–and starvation-associated repressor of the glucocorticoid receptor. Sci Signal 3:ra8Google Scholar
  43. Kumar G, Goyal MK, Sahota PK, Jain R (2010) Penumbra, the basis of neuroimaging in acute stroke treatment: current evidence. J Neurol Sci 288:13–24CrossRefGoogle Scholar
  44. Li L et al. (2016) Long noncoding RNA MALAT1 promotes aggressive pancreatic cancer proliferation and metastasis via the stimulation of autophagy. Mol Cancer TherGoogle Scholar
  45. Li Z, Li J, Tang N (2017) Long noncoding RNA Malat1 is a potent autophagy inducer protecting brain microvascular endothelial cells against oxygen-glucose deprivation/reoxygenation-induced injury by sponging miR-26b and upregulating ULK2 expression. Neuroscience 354:1–10CrossRefGoogle Scholar
  46. Liu X, Hou L, Huang W, Gao Y, Lv X, Tang J (2016) The mechanism of long non-coding RNA MEG3 for neurons apoptosis caused by hypoxia: mediated by miR-181b-12/15-LOX signaling pathway. Front Cell Neurosci 10:201Google Scholar
  47. Lorenzen JM, Martino F, Thum T (2012) Epigenetic modifications in cardiovascular disease. Basic Res Cardiol 107:245CrossRefGoogle Scholar
  48. Lu K-h et al (2013) Long non-coding RNA MEG3 inhibits NSCLC cells proliferation and induces apoptosis by affecting p53 expression. BMC Cancer 13:461CrossRefGoogle Scholar
  49. Ma X, Shao C, Jin Y, Wang H, Meng Y (2014) Long non-coding RNAs: a novel endogenous source for the generation of dicer-like 1-dependent small RNAs in Arabidopsis thaliana. RNA Biol 11:373–390CrossRefGoogle Scholar
  50. Ma F, Wang S-h, Cai Q, L-y J, Zhou D, Ding J, Z-w Q (2017) Long non-coding RNA TUG1 promotes cell proliferation and metastasis by negatively regulating miR-300 in gallbladder carcinoma. Biomed Pharmacother 88:863–869CrossRefGoogle Scholar
  51. Mattingsdal M et al (2013) Pathway analysis of genetic markers associated with a functional MRI faces paradigm implicates polymorphisms in calcium responsive pathways. Neuroimage 70:143–149CrossRefGoogle Scholar
  52. Mehta SL, Kim T, Vemuganti R (2015) Long noncoding RNA FosDT promotes ischemic brain injury by interacting with REST-associated chromatin-modifying proteins. J Neurosci 35:16443–16449CrossRefGoogle Scholar
  53. Mercer TR, Mattick JS (2013) Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 20:300CrossRefGoogle Scholar
  54. Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10:155CrossRefGoogle Scholar
  55. Michalik KM et al (2014) Long noncoding RNA MALAT1 regulates endothelial cell function and vessel growth. Circ Res 114:1389–1397CrossRefGoogle Scholar
  56. Mondal T et al (2015) MEG3 long noncoding RNA regulates the TGF-β pathway genes through formation of RNA–DNA triplex structures. Nat Commun 6:7743CrossRefGoogle Scholar
  57. Moran A, Forouzanfar M, Sampson U, Chugh S, Feigin V, Mensah G (2013) The epidemiology of cardiovascular diseases in sub-Saharan Africa: the global burden of diseases, injuries and risk factors 2010 study. Prog Cardiovasc Dis 56:234–239CrossRefGoogle Scholar
  58. Moskowitz MA, Lo EH, Iadecola C (2010) The science of stroke: mechanisms in search of treatments. Neuron 67:181–198CrossRefGoogle Scholar
  59. Ng SY, Johnson R, Stanton LW (2012) Human long non-coding RNAs promote pluripotency and neuronal differentiation by association with chromatin modifiers and transcription factors. EMBO J 31:522–533CrossRefGoogle Scholar
  60. Noh K-M et al (2012) Repressor element-1 silencing transcription factor (REST)-dependent epigenetic remodeling is critical to ischemia-induced neuronal death. Proc Natl Acad Sci:201121568Google Scholar
  61. Paonessa F et al (2016) Regulation of neural gene transcription by optogenetic inhibition of the RE1-silencing transcription factor. Proc Natl Acad Sci 113:E91–E100CrossRefGoogle Scholar
  62. Peng W et al (2015) Long non-coding RNA MEG3 functions as a competing endogenous RNA to regulate gastric cancer progression. J Exp Clin Cancer Res 34:79CrossRefGoogle Scholar
  63. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP (2011) A ceRNA hypothesis: the Rosetta stone of a hidden RNA language? Cell 146:353–358CrossRefGoogle Scholar
  64. Schaukowitch K, Kim T-K (2014) Emerging epigenetic mechanisms of long non-coding RNAs. Neuroscience 264:25–38CrossRefGoogle Scholar
  65. Srinivasan M, Edman CF, Schulman H (1994) Alternative splicing introduces a nuclear localization signal that targets multifunctional CaM kinase to the nucleus. J Cell Biol 126:839–852CrossRefGoogle Scholar
  66. Sun H-s, Feng Z-p (2013) Neuroprotective role of ATP-sensitive potassium channels in cerebral ischemia. Acta Pharmacol Sin 34:24CrossRefGoogle Scholar
  67. Sun H-S et al (2008) Effectiveness of PSD95 inhibitors in permanent and transient focal ischemia in the rat. Stroke 39:2544–2553CrossRefGoogle Scholar
  68. Sun H-S et al (2009) Suppression of hippocampal TRPM7 protein prevents delayed neuronal death in brain ischemia. Nat Neurosci 12:1300CrossRefGoogle Scholar
  69. Sun H-S et al (2015) Neuronal KATP channels mediate hypoxic preconditioning and reduce subsequent neonatal hypoxic–ischemic brain injury. Exp Neurol 263:161–171CrossRefGoogle Scholar
  70. Szcześniak MW, Makałowska I (2016) lncRNA-RNA interactions across the human transcriptome. PLoS One 11:e0150353CrossRefGoogle Scholar
  71. Tan Z et al (2014) Combination treatment of r-tPA and an optimized human apyrase reduces mortality rate and hemorrhagic transformation 6 h after ischemic stroke in aged female rats. Eur J Pharmacol 738:368–373CrossRefGoogle Scholar
  72. Tang Y, Jin X, Xiang Y, Chen Y, Shen C-x, Zhang Y-c, Li Y-g (2015) The lncRNA MALAT1 protects the endothelium against ox-LDL-induced dysfunction via upregulating the expression of the miR-22-3p target genes CXCR2 and AKT. FEBS Lett 589:3189–3196CrossRefGoogle Scholar
  73. Tekle WG et al (2012) Intravenous thrombolysis in expanded time window (3-4.5 hours) in general practice with concurrent availability of endovascular treatment. J Vasc Interv Neurol 5:22Google Scholar
  74. Thangavelu K, Kannan R, Kumar NS, Rethish E, Sabitha S, Sayeeganesh N (2012) Significance of localization of mandibular foramen in an inferior alveolar nerve block. J Nat Sci Biol Med 3:156CrossRefGoogle Scholar
  75. Tripathi V et al (2010) The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 39:925–938CrossRefGoogle Scholar
  76. Vakili A, Mojarrad S, Akhavan MM, Rashidy-Pour A (2011) Pentoxifylline attenuates TNF-α protein levels and brain edema following temporary focal cerebral ischemia in rats. Brain Res 1377:119–125CrossRefGoogle Scholar
  77. Van der Worp H et al (2002) The effect of tirilazad mesylate on infarct volume of patients with acute ischemic stroke. Neurology 58:133–135CrossRefGoogle Scholar
  78. Velayatzadeh M, ASKARY SA, Beheshti M, Mahjob S, Hoseini M (2014) Measurement of heavy metals (HG, CD, SN, ZN, NI, FE) in canned tuna fish product in central cities, IranGoogle Scholar
  79. Wang P, Ren Z, Sun P (2012) Overexpression of the long non-coding RNA MEG3 impairs in vitro glioma cell proliferation. J Cell Biochem 113:1868–1874CrossRefGoogle Scholar
  80. Wang SH et al (2016) The lnc RNA MALAT 1 functions as a competing endogenous RNA to regulate MCL-1 expression by sponging miR-363-3p in gallbladder cancer. J Cell Mol Med 20:2299–2308CrossRefGoogle Scholar
  81. Wang Y, Yang T, Zhang Z, Lu M, Zhao W, Zeng X, Zhang W (2017) Long non-coding RNA TUG 1 promotes migration and invasion by acting as a ce RNA of miR-335-5p in osteosarcoma cells. Cancer Sci 108:859–867CrossRefGoogle Scholar
  82. Wang H, Liao S, Yu J (2019) Abstract WP347: long non-coding RNA TUG1 contributes to microglial activation after oxygen glucose deprivation stroke 50:AWP347-AWP347Google Scholar
  83. Williams AB, Schumacher B (2016) p53 in the DNA-damage-repair process. Cold Spring Harbor perspectives in medicine a026070Google Scholar
  84. Wilusz JE, Sunwoo H, Spector DL (2009) Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 23:1494–1504CrossRefGoogle Scholar
  85. Wu Z et al (2017) LncRNA-N1LR enhances neuroprotection against ischemic stroke probably by inhibiting p53 phosphorylation. Mol Neurobiol 54:7670–7685CrossRefGoogle Scholar
  86. Xiao H et al (2015) LncRNA MALAT1 functions as a competing endogenous RNA to regulate ZEB2 expression by sponging miR-200s in clear cell kidney carcinoma. Oncotarget 6:38005Google Scholar
  87. Xu Q et al (2016) Long non-coding RNA C2dat1 regulates CaMKIIδ expression to promote neuronal survival through the NF-κB signaling pathway following cerebral ischemia. Cell Death Dis 7:e2173CrossRefGoogle Scholar
  88. Yan H, Yuan J, Gao L, Rao J, Hu J (2016) Long noncoding RNA MEG3 activation of p53 mediates ischemic neuronal death in stroke. Neuroscience 337:191–199CrossRefGoogle Scholar
  89. Yang F, Bi J, Xue X, Zheng L, Zhi K, Hua J, Fang G (2012) Up-regulated long non-coding RNA H19 contributes to proliferation of gastric cancer cells. FEBS J 279:3159–3165CrossRefGoogle Scholar
  90. Ye J et al. (2018) Ischemic injury-induced CaMKIIδ and CaMKIIγ confer neuroprotection through the NF-κB signaling pathway. Mol Neurobiol 1–14Google Scholar
  91. Yoon J-H et al (2012) LincRNA-p21 suppresses target mRNA translation. Mol Cell 47:648–655CrossRefGoogle Scholar
  92. Young T, Matsuda T, Cepko C (2005) The noncoding RNA taurine upregulated gene 1 is required for differentiation of the murine retina. Curr Biol 15:501–512CrossRefGoogle Scholar
  93. Yu G, Wu F, Wang E-S (2015) BQ-869, a novel NMDA receptor antagonist, protects against excitotoxicity and attenuates cerebral ischemic injury in stroke. Int J Clin Exp Pathol 8:1213Google Scholar
  94. Yuan L, Zhang J, Chen YE, Yin K-J (2015) Long non-coding RNAs mediate cerebrovascular endothelial pathologies in ischemic stroke. Stroke 46:A72–A72Google Scholar
  95. Yuan P, Cao W, Zang Q, Li G, Guo X, Fan J (2016) The HIF-2α-MALAT1-miR-216b axis regulates multi-drug resistance of hepatocellular carcinoma cells via modulating autophagy. Biochem Biophys Res Commun 478:1067–1073CrossRefGoogle Scholar
  96. Zhang X et al. (2010) Maternally expressed gene 3, an imprinted noncoding RNA gene, is associated with meningioma pathogenesis and progression. Cancer research:0008-5472. CAN-0009-3885Google Scholar
  97. Zhang J et al (2016) Altered long non-coding RNA transcriptomic profiles in brain microvascular endothelium after cerebral ischemia. Exp Neurol 277:162–170CrossRefGoogle Scholar
  98. Zhang X, Tang X, Liu K, Hamblin MH, Yin K-J (2017) Long non-coding RNA Malat1 regulates cerebrovascular pathologies in ischemic stroke. J Neurosci:3389–3316Google Scholar
  99. Zhang X, Hamblin MH, Yin K-J (2018) Noncoding RNAs and stroke the neuroscientist 1073858418769556Google Scholar
  100. Zhao F et al (2015) Microarray profiling and co-expression network analysis of LncRNAs and mRNAs in neonatal rats following hypoxic-ischemic brain damage. Sci Rep 5:13850CrossRefGoogle Scholar
  101. Zhou Y, Zhang X, Klibanski A (2012) MEG3 non-coding RNA: a tumor suppressor. J Mol Endocrinol: JME-12-0008Google Scholar
  102. Zhuo H et al (2016) The aberrant expression of MEG3 regulated by UHRF1 predicts the prognosis of hepatocellular carcinoma. Mol Carcinog 55:209–219CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Masoumeh Alishahi
    • 1
  • Farhoodeh Ghaedrahmati
    • 2
  • Tannaz Akbari Kolagar
    • 1
  • William Winlow
    • 3
    • 4
  • Negin Nikkar
    • 5
  • Maryam Farzaneh
    • 6
  • Seyed Esmaeil Khoshnam
    • 7
    Email author
  1. 1.Department of Biology, Tehran North BranchIslamic Azad UniversityTehranIran
  2. 2.Department of Immunology, Medical SchoolShiraz University of Medical SciencesShirazIran
  3. 3.Dipartimento di BiologiaUniversità degli Studi di NapoliNaplesItaly
  4. 4.Honorary Research Fellow, Institute of Ageing and Chronic DiseasesUniversity of LiverpoolLiverpoolUK
  5. 5.Department of Biology, Faculty of SciencesAlzahra UniversityTehranIran
  6. 6.Department of Stem Cells and Developmental Biology, Cell Science Research CenterRoyan Institute for Stem Cell Biology and Technology, ACECRTehranIran
  7. 7.Physiology Research CenterAhvaz Jundishapur University of Medical SciencesAhvazIran

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