Erythropoietin improves hypoxic-ischemic encephalopathy in neonatal rats after short-term anoxia by enhancing angiogenesis

Brain Research

Volumn 1651, Issue , 2016, Pages 104-113

  Yan, Fangfang ^a   Zhang, Meimei ^a   Meng, Yan ^a   Li, Huijuan ^a   Yu, Lie ^a   Fu, Xiaojie ^a   Tang, Youcai ^a   Jiang, Chao ^a  

^a ZHENGZHOU UNIVERSITY   (China)

Author keywords

Angiogenesis; Anoxia; Erythropoietin; Neonatal Rats; VEGF

Indexed keywords

ERYTHROPOIETIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; RAF PROTEIN; RECOMBINANT ERYTHROPOIETIN; SEMAXANIB; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; ANGIOGENIC FACTOR; ERYTHROPOIETIN; INDOLE DERIVATIVE; KDR PROTEIN, RAT; PYRROLE DERIVATIVE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, RAT; VASCULOTROPIN A;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOXIA; ARTICLE; BRAIN INJURY; COGNITION; CONTROLLED STUDY; CORPUS CALLOSUM; HIPPOCAMPUS; HISTOPATHOLOGY; HYPOXIC ISCHEMIC ENCEPHALOPATHY; MALE; NEUROPROTECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; WEIGHT GAIN; WHITE MATTER LESION; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; DRUG EFFECTS; HYPOXIA; HYPOXIA-ISCHEMIA, BRAIN; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT; VASCULARIZATION; WHITE MATTER;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; ANIMALS, NEWBORN; COGNITION; DISEASE MODELS, ANIMAL; ERYTHROPOIETIN; HIPPOCAMPUS; HYPOXIA; HYPOXIA-ISCHEMIA, BRAIN; INDOLES; MALE; PYRROLES; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; WHITE MATTER;

EID: 84988910265     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2016.09.024     Document Type: Article

References (72)

1. Adamczak, J., Hoehn, M., Poststroke angiogenesis, con: dark side of angiogenesis. Stroke 46:5 (2015), e103–e104.
2. Bacic, M., Edwards, N.A., Merrill, M.J., Differential expression of vascular endothelial growth factor (vascular permeability factor) forms in rat tissues. Growth Factors 12:1 (1995), 11–15.
3. Bouzat, P., Millet, A., Boue, Y., et al. Changes in brain tissue oxygenation after treatment of diffuse traumatic brain injury by erythropoietin. Crit. Care Med. 41:5 (2013), 1316–1324.
4. Brines, M.L., Ghezzi, P., Keenan, S., et al. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc. Natl. Acad. Sci. USA 97:19 (2000), 10526–10531.
5. Byts, N., Sirén, A.L., Erythropoietin: a multimodal neuroprotective agent. Exp. Transl. Stroke Med., 1, 2009, 4.
6. Cechetti, F., Worm, P.V., Pereira, L.O., et al. The modified 2VO ischemia protocol causes cognitive impairment similar to that induced by the standard method, but with a better survival rate. Braz. J. Med Biol. Res. 43:12 (2010), 1178–1183.
7. Chun, P.T., McPherson, R.J., Marney, L.C., et al. Serial plasma metabolites following hypoxic-ischemic encephalopathy in a nonhuman primate model. Dev. Neurosci. 37:2 (2015), 161–171.
8. Digicaylioglu, M., Bichet, S., Marti, H.H., et al. Localization of specific erythropoietin binding sites in defined areas of the mouse brain. Proc. Natl. Acad. Sci. USA 92:9 (1995), 3717–3720.
9. Dixon, B.J., Reis, C., Ho, W.M., et al. Neuroprotective strategies after neonatal hypoxic ischemic encephalopathy. Int. J. Mol. Sci. 16:9 (2015), 22368–22401.
10. Dobbing, J., Undernutrition and the developing brain: the use of animal models ot elucidate the human problem. Psychiatr. Neurol. Neurochir. 74:6 (1971), 433–442.
11. Fan, X., Heijnen, C.J., van der, K.M., et al. Beneficial effect of erythropoietin on sensorimotor function and white matter after hypoxia-ischemia in neonatal mice. Pediatr. Res. 69:1 (2011), 56–61.
12. Freitag, M.T., Marton, G., Pajer, K., et al. Monitoring of short-term erythropoietin therapy in rats with acute spinal cord injury using manganese-enhanced magnetic resonance imaging. J. Neuroimaging 25:4 (2015), 582–589.
13. Gonzalez, F.F., Larpthaveesarp, A., McQuillen, P., et al. Erythropoietin increases neurogenesis and oligodendrogliosis of subventricular zone precursor cells after neonatal stroke. Stroke 44:3 (2013), 753–758.
14. Grasso, G., Sfacteria, A., Cerami, A., et al. Erythropoietin as a tissue-protective cytokine in brain injury: what do we know and where do we go?. Neuroscientist 10:2 (2004), 93–98.
15. Grojean, S., Schroeder, H., Pourie, G., et al. Histopathological alterations and functional brain deficits after transient hypoxia in the newborn rat pup: a long term follow-up. Neurobiol. Dis. 14:2 (2003), 265–278.
16. Itokawa, T., Nokihara, H., Nishioka, Y., et al. Antiangiogenic effect by SU5416 is partly attributable to inhibition of Flt-1 receptor signaling. Mol. Cancer Ther. 1:5 (2002), 295–302.
17. Iwai, M., Cao, G., Yin, W., et al. Erythropoietin promotes neuronal replacement through revascularization and neurogenesis after neonatal hypoxia/ischemia in rats. Stroke 38:10 (2007), 2795–2803.
18. Juul, S.E., McPherson, R.J., Farrell, F.X., et al. Erytropoietin concentrations in cerebrospinal fluid of nonhuman primates and fetal sheep following high-dose recombinant erythropoietin. Biol. Neonate 85:2 (2004), 138–144.
19. Kaji, T., Yamamoto, C., Oh-i, M., et al. The vascular endothelial growth factor VEGF165 induces perlecan synthesis via VEGF receptor-2 in cultured human brain microvascular endothelial cells. Biochim. Biophys. Acta 1760:9 (2006), 1465–1474.
20. Kellert, B.A., McPherson, R.J., Juul, S.E., A comparison of high-dose recombinant erythropoietin treatment regimens in brain-injured neonatal rats. Pediatr. Res 61:4 (2007), 451–455.
21. Kertesz, N., Wu, J., Chen, T.H., et al. The role of erythropoietin in regulating angiogenesis. Dev. Biol. 276:1 (2004), 101–110.
22. Kertmen, H., Gürer, B., Yilmaz, E.R., et al. Antioxidant and antiapoptotic effects of darbepoetin-α against traumatic brain injury in rats. Arch. Med. Sci. 11:5 (2015), 1119–1128.
23. Kurinczuk, J.J., White-Koning, M., Badawi, N., Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy. Early Hum. Dev. 86:6 (2010), 329–338.
24. Lee, M.S., Ghim, J., Kim, S.J., et al. Functional interaction between CTGF and FPRL1 regulates VEGF-A-induced angiogenesis. Cell. Signal. 27:7 (2015), 1439–1448.
25. Li, W.L., Fraser, J.L., Yu, S.P., et al. The role of VEGF/VEGFR2 signaling in peripheral stimulation-induced cerebral neurovascular regeneration after ischemic stroke in mice. Exp. Brain Res. 214:4 (2011), 503–513.
26. Ma, Q., Zhang, L., Epigenetic programming of hypoxic-ischemic encephalopathy in response to fetal hypoxia. Prog. Neurobiol. 124 (2015), 28–48.
27. Masada, T., et al. Intraventricular infusion of vascular endothelial growth factor promotes cerebral angiogenesis with minimal brain edema. Neurosurgery 50:3 (2002), 589–598.
28. Masuda, S., Okano, M., Yamagishi, K., et al. A novel site of erythropoietin production. Oxygen-dependent production in cultured rat astrocytes. J. Biol. Chem. 269:30 (1994), 19488–19493.
29. Meng, Y., Xiong, Y., Mahmood, A., et al. Dose-dependent neurorestorative effects of delayed treatment of traumatic brain injury with recombinant human erythropoietin in rats. J. Neurosurg. 115:3 (2011), 550–560.
30. Minnerup, J., Heidrich, J., Rogalewski, A., et al. The efficacy of erythropoietin and its analogues in animal stroke models: a meta-analysis. Stroke 40:9 (2009), 3113–3120.
31. Morris, R., Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11:1 (1984), 47–60.
32. Muller, A.J., Marks, J.D., Hypoxic ischemic brain injury: Potential therapeutic interventions for the future. Neoreviews 15:5 (2014), e177–e186.
33. Nagai, A., Nakagawa, E., Choi, H.B., et al. Erythropoietin and erythropoietin receptors in human CNS neurons, astrocytes, microglia, and oligodendrocytes grown in culture. J. Neuropathol. Exp. Neurol. 60:4 (2001), 386–392.
34. Nakano, M., Satoh, K., Fukumoto, Y., et al. Important role of erythropoietin receptor to promote VEGF expression and angiogenesis in peripheral ischemia in mice. Circ. Res. 100:5 (2007), 662–669.
35. Nyakas, C., Buwalda, B., Luiten, P.G., Hypoxia and brain development. Prog. Neurobiol. 49:1 (1996), 1–51.
36. Ogunshola, O.O., Bogdanova, A.Y., Epo and non-hematopoietic cells: what do we know?. Methods Mol. Biol. 982 (2013), 13–41.
37. Okazaki, T., Ebihara, S., Asada, M., et al. Erythropoietin promotes the growth of tumors lacking its receptor and decreases survival of tumor-bearing mice by enhancing angiogenesis. Neoplasia 10:9 (2008), 932–939.
38. Pan, C.H., Lin, W.H., Chien, Y.C., et al. K20E, an oxidative-coupling compound of methyl caffeate, exhibits anti-angiogenic activities through down-regulations of VEGF and VEGF receptor-2. Toxicol. Appl Pharmcol. 282:2 (2015), 215–26.53.
39. Paris, D., Beaulieu-Abdelahad, D., Mullan, M., et al. Amelioration of experimental autoimmune encephalomyelitis by anatabine. PLoS One, 8(1), 2013, e55392.
40. Pulera, M.R., Adams, L.M., Liu, H., et al. Apoptosis in a neonatal rat model of cerebral hypoxia-ischemia. Stroke 29:12 (1998), 2622–2630.
41. Pulsinelli, W.A., Brierley, J.B., Plum, F., Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol. 11:5 (1982), 491–498.
42. Rangarajan, V., Juul, S.E., Erythropoietin: emerging role of erythropoietin in neonatal neuroprotection. Pediatr. Neurol. 51:4 (2014), 481–488.
43. Rice, J.E. 3rd, Vannucci, R.C., Brierley, J.B., The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 9:2 (1981), 131–141.
44. Robertson, R.T., Levine, S.T., Haynes, S.M., et al. Use of labeled tomato lectin for imaging vasculature structures. Histochem. Cell Biol. 143:2 (2015), 225–234.
45. Shea, K.L., Palanisamy, A., What can you do to protect the newborn brain?. Curr. Opin. Anaesthesiol. 28:3 (2015), 261–266.
46. Spandou, E., Papoutsopoulou, S., Soubasi, V., et al. Hypoxia-ischemia affects erythropoietin and erythropoietin receptor expression pattern in the neonatal rat brain. Brain Res. 1021:2 (2004), 167–172.
47. Statler, P.A., McPherson, R.J., Bauer, L.A., et al. Pharmacokinetics of high-dose recombinant erythropoietin in plasma and brain of neonatal rats. Pediatr. Res. 61:6 (2007), 671–675.
48. Sugawa, M., Sakurai, Y., Ishikawa-Ieda, Y., et al. Effects of erythropoietin on glial cell development; oligodendrocyte maturation and astrocyte proliferation. Neurosci. Res. 44:4 (2002), 391–403.
49. Tang, Y., Wang, L., Wang, J., et al. Ischemia-induced angiogenesis is attenuated in aged rats. Aging Dis. 7:4 (2015), 326–335.
50. Thau-Zuchman, O., Shohami, E., Alexandrovich, A.G., et al. Vascular endothelial growth factor increases neurogenesis after traumatic brain injury. J. Cereb. Blood Flow. Metab. 30:5 (2010), 1008–1016.
51. Torun, Y.A., Ozdemir, M.A., Ulger, H., et al. Erythropoietin improves brain development in short-term hypoxia in rat embryo cultures. Brain Dev. 36:10 (2014), 864–869.
52. Traudt, C.M., McPherson, R.J., Bauer, L.A., et al. Concurrent erythropoietin and hypothermia treatment improve outcomes in a term nonhuman primate model of perinatal asphyxia. Dev. Neurosci. 35:6 (2013), 491–503.
53. Trincavelli, M.L., Da Pozzo, E., Ciampi, O., et al. Regulation of erythropoietin receptor activity in Endothelial Cells by Different Erythropoietin (EPO) derivatives: an in vitro study. Int. J. Mol. Sci. 14:2 (2013), 2258–2281.
54. Tsai, P.T., Ohab, J.J., Kertesz, N., et al. A critical role of erythropoietin receptor in neurogenesis and post-stroke recovery. J. Neurosci. 26:4 (2006), 1269–1274.
55. Tsui, A.K., Marsden, P.A., Mazer, C.D., et al. Differential HIF and NOS responses to acute anemia: defining organ-specific hemoglobin thresholds for tissue hypoxia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 307:1 (2014), R13–R25.
56. Tufro, A., Tubular vascular endothelial growth factor-a, erythropoietin, and medullary vessels: a trio linked by hypoxia. J. Am. Soc. Nephrol. 26:5 (2015), 997–998.
57. Wang, J., Fu, X., Jiang, C., et al. Bone marrow mononuclear cell transplantation promotes therapeutic angiogenesis via upregulation of the VEGF-VEGFR2 signaling pathway in a rat model of vascular dementia. Behav. Brain Res. 265 (2014), 171–180.
58. Wang, J., Fu, X., Yu, L., et al. Preconditioning with VEGF enhances angiogenic and neuroprotective effects of bone marrow mononuclear cell transplantation in a rat model of chronic cerebral hypoperfusion. Mol. Neurobiol., 2015 (Epub ahead of print).
59. Wang, L., Chopp, M., Gregg, S.R., et al. Neural progenitor cells treated with EPO induce angiogenesis through the production of VEGF. J. Cereb. Blood Flow. Metab. 28:7 (2008), 1361–1368.
60. Westenbrink, B.D., Ruifrok, W.P., Voors, A.A., et al. Vascular endothelial growth factor is crucial for erythropoietin-induced improvement of cardiac function in heart failure. Cardiovasc. Res. 87:1 (2010), 30–39.
61. Wu, H., Wu, T., Li, M., et al. Efficacy of the lipid-soluble iron chelator 2,2′-dipyridyl against hemorrhagic brain injury. Neurobiol. Dis. 45:1 (2012), 388–394.
62. Wu, Y.W., Gonzalez, F.F., Erythropoietin: a novel therapy for hypoxic-ischaemic encephalopathy?. Dev. Med. Child Neurol. 57:Suppl 3 (2015), S34–S39.
63. Wu, Y.W., Bauer, L.A., Ballard, R.A., et al. Erythropoietin for neuroprotection in neonatal encephalopathy: safety and pharmacokinetics. Pediatrics 130:4 (2012), 683–691.
64. Xiong, Y., Mahmood, A., Meng, Y., et al. Delayed administration of erythropoietin reducing hippocampal cell loss, enhancing angiogenesis and neurogenesis, and improving functional outcome following traumatic brain injury in rats: comparison of treatment with single and triple dose. J. Neurosurg. 113:3 (2010), 598–608.
65. Xiong, Y., Mahmood, A., Qu, C., et al. Erythropoietin improves histological and functional outcomes after traumatic brain injury in mice in the absence of the neural erythropoietin receptor. J. Neurotrauma 27:1 (2010), 205–215.
66. Xiong, Y., Zhang, Y., Mahmood, A., et al. Erythropoietin mediates neurobehavioral recovery and neurovascular remodeling following traumatic brain injury in rats by increasing expression of vascular endothelial growth factor. Transl. Stroke Res. 2:4 (2011), 619–632.
67. Yang, Z., Wang, H., Jiang, Y., et al. VEGFA activates erythropoietin receptor and enhances VEGFR2-mediated pathological angiogenesis. Am. J. Pathol. 184:4 (2014), 1230–1239.
68. Yeganeh, F., Nikbakht, F., Bahmanpour, S., et al. (Neuroprotective effects of NMDA and group) I metabotropic glutamate receptor antagonists against neurodegeneration induced by homocysteine in rat hippocampus: in vivo study. J. Mol. Neurosci. 50:3 (2013), 551–557.
69. Zacharias, R., Schmidt, M., Kny, J., Sifringer, M., et al. Dose-dependent effects of erythropoietin in propofol anesthetized neonatal rats. Brain Res. 1343 (2010), 14–19.
70. Zhang, Z.G., Zhang, L., Jiang, Q., et al. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J. Clin. Investig. 106:7 (2000), 829–838.
71. Zhao, J., Chen, Y., Xu, Y., et al. Effect of intrauterine infection on brain development and injury. Int. J. Dev. Neurosci. 31:7 (2013), 543–549.
72. Zhu, C., Kang, W., Xu, F., et al. Erythropoietin improved neurologic outcomes in newborns with hypoxic-ischemic encephalopathy. Pediatrics 124:2 (2009), e218–e226.