The erythropoietin-derived peptide MK-X and erythropoietin have neuroprotective effects against ischemic brain damage

Cell Death and Disease

Volumn 8, Issue 8, 2017, Pages

  Yoo, Seung Jun ^a   Cho, Bongki ^a   Lee, Deokho ^a   Son, Gowoon ^a   Lee, Yeong Bae ^b   Han, Hyung Soo ^c   Kim, Eunjoo ^a   Moon, Chanil ^d   Moon, Cheil ^a  

^a Daegu Gyeongbuk Institute of Science and Technology   (South Korea)

^b Gachon University   (South Korea)

^c Kyungpook National University School of Medicine   (South Korea)

^d GemVax   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CASP3 PROTEIN, MOUSE; CASPASE 3; ERYTHROPOIETIN; GLUTAMIC ACID; JAK2 PROTEIN, MOUSE; JANUS KINASE 2; NEUROPROTECTIVE AGENT; PEPTIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ANIMAL; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN ISCHEMIA; C57BL MOUSE; CELL DEATH; CEREBROVASCULAR ACCIDENT; CEREBROVASCULAR DISEASE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MAMMALIAN EMBRYO; MAPK SIGNALING; METABOLISM; MIDDLE CEREBRAL ARTERY; MITOCHONDRION; MOUSE; NERVE CELL; PATHOLOGY; PERMEABILITY; PRIMARY CELL CULTURE; RAT; SPRAGUE DAWLEY RAT; SURGERY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN ISCHEMIA; CASPASE 3; CELL DEATH; CEREBRAL CORTEX; CEREBROVASCULAR DISORDERS; EMBRYO, MAMMALIAN; ERYTHROPOIETIN; GENE EXPRESSION REGULATION; GLUTAMIC ACID; JANUS KINASE 2; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MIDDLE CEREBRAL ARTERY; MITOCHONDRIA; NEURONS; NEUROPROTECTIVE AGENTS; PEPTIDES; PERMEABILITY; PHOSPHATIDYLINOSITOL 3-KINASES; PRIMARY CELL CULTURE; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; STROKE;

EID: 85045777932     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/CDDIS.2017.381     Document Type: Article

References (60)

1. Adams HP Jr., Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke 1993; 24: 35–41.
2. Abreu TT, Mateus S, Correia J. Therapy implications of transthoracic echocardiography in acute ischemic stroke patients. Stroke 2005; 36: 1565–1566.
3. Li D, Shao Z, Vanden Hoek TL, Brorson JR. Reperfusion accelerates acute neuronal death induced by simulated ischemia. Exp neurol 2007; 206: 280–287.
4. Mehta A, Prabhakar M, Kumar P, Deshmukh R, Sharma PL. Excitotoxicity: bridge to various triggers in neurodegenerative disorders. Eur j pharmacol 2013; 698: 6–18.
5. Sims NR, Muyderman H. Mitochondria, oxidative metabolism and cell death in stroke. Biochim Biophys Acta 2010; 1802: 80–91.
6. Luo T, Wang J, Hao S, Guo T, Ren P, Cheng Z et al. Brain drug delivery systems for the stroke intervention and recovery. Curr Pharm Des 2017, 23: 2258–2267.
7. Lai TW, Zhang S, Wang YT. Excitotoxicity and stroke: identifying novel targets for neuroprotection. Prog Neurobiol 2014; 115: 157–188.
8. Brines M, Cerami A. Emerging biological roles for erythropoietin in the nervous system. Nat rev Neurosci 2005; 6: 484–494.
9. Grasso G, Sfacteria A, Cerami A, Brines M. Erythropoietin as a tissue-protective cytokine in brain injury: what do we know and where do we go? Neuroscientist 2004; 10: 93–98.
10. Noguchi CT, Asavaritikrai P, Teng R, Jia Y. Role of erythropoietin in the brain. Crit rev oncol/ hematol 2007; 64: 159–171.
11. Liu C, Shen K, Liu Z, Noguchi CT. Regulated human erythropoietin receptor expression in mouse brain. J Biol Chem 1997; 272: 32395–32400.
12. Tsai PT, Ohab JJ, Kertesz N, Groszer M, Matter C, Gao J et al. A critical role of erythropoietin receptor in neurogenesis and post-stroke recovery. J neurosci 2006; 26: 1269–1274.
13. Fu A, Hui EK, Lu JZ, Boado RJ, Pardridge WM. Neuroprotection in experimental stroke in the rat with an IgG-erythropoietin fusion protein. Brain Res 2010; 1360: 193–197.
14. Rodriguez Cruz Y, Mengana Tamos Y, Munoz Cernuda A, Subiros Martines N, Gonzalez-Quevedo A, Sosa Teste I et al. Treatment with nasal neuro-EPO improves the neurological, cognitive, and histological state in a gerbil model of focal ischemia. Scientific World J 2010; 10: 2288–2300.
15. Arcasoy MO. The non-haematopoietic biological effects of erythropoietin. Br j haematol 2008; 141: 14–31.
16. Lipsic E, Schoemaker RG, van der Meer P, Voors AA, van Veldhuisen DJ, van Gilst WH. Protective effects of erythropoietin in cardiac ischemia: from bench to bedside. J Am Coll Cardiol 2006; 48: 2161–2167.
17. Rangarajan V, Juul SE. Erythropoietin: emerging role of erythropoietin in neonatal neuroprotection. Pediatr neurol 2014; 51: 481–488.
18. Zhou TF, Yu JG. Recombinant human erythropoietin attenuates neuronal apoptosis and cognitive defects via JAK2/STAT3 signaling in experimental endotoxemia. J surg res 2013; 183: 304–312.
19. Zaman K, Ryu H, Hall D, O'Donovan K, Lin KI, Miller MP et al. Protection from oxidative stress-induced apoptosis in cortical neuronal cultures by iron chelators is associated with enhanced DNA binding of hypoxia-inducible factor-1 and ATF-1/CREB and increased expression of glycolytic enzymes, p21(waf1/cip1), and erythropoietin. J neurosci 1999; 19: 9821–9830.
20. Ehrenreich H, Weissenborn K, Prange H, Schneider D, Weimar C, Wartenberg K et al. Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke 2009; 40: e647–e656.
21. Unger EF, Thompson AM, Blank MJ, Temple R. Erythropoiesis-stimulating agents – time for a reevaluation. N Engl j med 2010; 362: 189–192.
22. Steinbrook R. Erythropoietin, the FDA, and oncology. N Engl j med 2007; 356: 2448–2451.
23. Yoo SJ, Cho B, Moon C, Yu SW. Neuroprotective effects of an erythropoietin-derived peptide in PC1 2 cells under oxidative stress. CNS Neurol Disord Drug Targets 2016; 15:927–934.
24. Enblad P, Frykholm P, Valtysson J, Silander HC, Andersson J, Fasth KJ et al. Middle cerebral artery occlusion and reperfusion in primates monitored by microdialysis and sequential positron emission tomography. Stroke 2001; 32: 1574–1580.
25. Singhal AB, Dijkhuizen RM, Rosen BR, Lo EH. Normobaric hyperoxia reduces MRI diffusion abnormalities and infarct size in experimental stroke. Neurology 2002; 58: 945–952.
26. Zhou X, Hollern D, Liao J, Andrechek E, Wang H. NMDA receptor-mediated excitotoxicity depends on the coactivation of synaptic and extrasynaptic receptors. Cell death dis 2013; 4: e560.
27. Vergun O, Keelan J, Khodorov BI, Duchen MR. Glutamate-induced mitochondrial depolarisation and perturbation of calcium homeostasis in cultured rat hippocampal neurones. J physiol 1999; 519(Pt 2): 451–466.
28. Abramov AY, Duchen MR. Mechanisms underlying the loss of mitochondrial membrane potential in glutamate excitotoxicity. Biochim Biophys Acta 2008; 1777: 953–964.
29. Zhang Y, Bhavnani BR. Glutamate-induced apoptosis in neuronal cells is mediated via caspase-dependent and independent mechanisms involving calpain and caspase-3 proteases as well as apoptosis inducing factor (AIF) and this process is inhibited by equine estrogens. BMC neurosci 2006; 7: 49.
30. Elmore S. Apoptosis: a review of programmed cell death. Toxicol pathol 2007; 35: 495–516.
31. Porter AG, Janicke RU. Emerging roles of caspase-3 in apoptosis. Cell Death Differ 1999; 6: 99–104.
32. Kuhrt D, Wojchowski DM. Emerging EPO and EPO receptor regulators and signal transducers. Blood 2015; 125: 3536–3541.
33. Kapralova K, Horvathova M, Pecquet C, Fialova Kucerova J, Pospisilova D, Leroy E et al. Cooperation of germ line JAK2 mutations E846D and R1063H in hereditary erythrocytosis with megakaryocytic atypia. Blood 2016; 128: 1418–1423.
34. Brines M, Cerami A. Discovering erythropoietin's extra-hematopoietic functions: biology and clinical promise. Kidney int 2006; 70: 246–250.
35. Bond WS, Rex TS. Evidence that erythropoietin modulates neuroinflammation through differential action on neurons, astrocytes, and microglia. Front Immunol 2014; 5: 523.
36. Vauzour D, Vafeiadou K, Rice-Evans C, Williams RJ, Spencer JP. Activation of pro-survival Akt and ERK1/2 signalling pathways underlie the anti-apoptotic effects of flavanones in cortical neurons. J neurochem 2007; 103: 1355–1367.
37. Siren AL, Fratelli M, Brines M, Goemans C, Casagrande S, Lewczuk P et al. Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci USA 2001; 98: 4044–4049.
38. Quast MJ, Wei J, Huang NC, Brunder DG, Sell SL, Gonzalez JM et al. Perfusion deficit parallels exacerbation of cerebral ischemia/reperfusion injury in hyperglycemic rats. J cereb blood flow metab 1997; 17: 553–559.
39. Candelario-Jalil E, Gonzalez-Falcon A, Garcia-Cabrera M, Leon OS, Fiebich BL. Wide therapeutic time window for nimesulide neuroprotection in a model of transient focal cerebral ischemia in the rat. Brain Res 2004; 1007: 98–108.
40. Williams AJ, Dave JR, Phillips JB, Lin Y, McCabe RT, Tortella FC. Neuroprotective efficacy and therapeutic window of the high-affinity N-methyl-D-aspartate antagonist conantokin-G: in vitro (primary cerebellar neurons) and in vivo (rat model of transient focal brain ischemia) studies. J pharmacol exp therapeut 2000; 294: 378–386.
41. Bennett CL, Silver SM, Djulbegovic B, Samaras AT, Blau CA, Gleason KJ et al. Venous thromboembolism and mortality associated with recombinant erythropoietin and darbepoetin administration for the treatment of cancer-associated anemia. Jama 2008; 299: 914–924.
42. Minnerup J, Wersching H, Schabitz WR. EPO for stroke therapy-Is there a future for further clinical development? Exp transl stroke med 2010; 2: 10.
43. Torup L. Neuroprotection with or without erythropoiesis; sometimes less is more. Br j pharmacol 2007; 151: 1141–1142.
44. Fischer K, McDonough V. Stroke care within the golden hour. JAMA neurol 2015; 72: 475–476.
45. Iqbal A. The 'golden hour' treatment of acute ischemic stroke. Med health 2011; 94: 378–379.
46. Assandri R, Egger M, Gassmann M, Niggli E, Bauer C, Forster I et al. Erythropoietin modulates intracellular calcium in a human neuroblastoma cell line. J physiol 1999; 516 (Pt 2): 343–352.
47. Chu X, Tong Q, Cheung JY, Wozney J, Conrad K, Mazack V et al. Interaction of TRPC2 and TRPC6 in erythropoietin modulation of calcium influx. J Biol Chem 2004; 279: 10514–10522.
48. Cheung JY, Zhang XQ, Bokvist K, Tillotson DL, Miller BA. Modulation of calcium channels in human erythroblasts by erythropoietin. Blood 1997; 89: 92–100.
49. Tringali G, Pozzoli G, Lisi L, Navarra P. Erythropoietin inhibits basal and stimulated corticotropin-releasing hormone release from the rat hypothalamus via a nontranscriptional mechanism. Endocrinology 2007; 148: 4711–4715.
50. Xiong Y, Chopp M, Lee CP. Erythropoietin improves brain mitochondrial function in rats after traumatic brain injury. Neurol res 2009; 31: 496–502.
51. Broughton BR, Reutens DC, Sobey CG. Apoptotic mechanisms after cerebral ischemia. Stroke 2009; 40: e331–e339.
52. Broker LE, Kruyt FA, Giaccone G. Cell death independent of caspases: a review. Clin cancer res 2005; 11: 3155–3162.
53. Kilic E, Kilic U, Soliz J, Bassetti CL, Gassmann M, Hermann DM. Brain-derived erythropoietin protects from focal cerebral ischemia by dual activation of ERK-1/-2 and Akt pathways. FASEB J 2005; 19: 2026–2028.
54. Ruscher K, Freyer D, Karsch M, Isaev N, Megow D, Sawitzki B et al. Erythropoietin is a paracrine mediator of ischemic tolerance in the brain: evidence from an in vitro model. J neurosci 2002; 22: 10291–10301.
55. Byts N, Samoylenko A, Fasshauer T, Ivanisevic M, Hennighausen L, Ehrenreich H et al. Essential role for Stat5 in the neurotrophic but not in the neuroprotective effect of erythropoietin. Cell Death Differ 2008; 15: 783–792.
56. Brines ML, Ghezzi P, Keenan S, Agnello D, de Lanerolle NC, Cerami C et al. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci USA 2000; 97: 10526–10531.
57. Bickel U. How to measure drug transport across the blood-brain barrier. NeuroRx 2005; 2: 15–26.
58. Siren AL, Knerlich F, Poser W, Gleiter CH, Bruck W, Ehrenreich H. Erythropoietin and erythropoietin receptor in human ischemic/hypoxic brain. Acta neuropathol 2001; 101: 271–276.
59. Saver JL, Smith EE, Fonarow GC, Reeves MJ, Zhao X, Olson DM et al. The ‘golden hour’ and acute brain ischemia: presenting features and lytic therapy in 430,000 patients arriving within 60 minutes of stroke onset. Stroke 2010; 41: 1431–1439.
60. Ebinger M, Audebert HJ. Stroke care within the golden hour–in reply. JAMA neurol 2015; 72: 476–477.