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Review

Erythropoietin and the use of a transgenic model of erythropoietin-deficient mice

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Pages 29-39 | Published online: 07 Apr 2016

References

  • Semenza GL. Oxygen homeostasis. Wiley Interdiscip Rev Syst Biol Med. 2010;2(3):336–361.
  • Gassmann M, Soliz J. Erythropoietin modulates the neural control of hypoxic ventilation. Cell Mol Life Sci. 2009;66(22):3575–3582.
  • Fandrey J, Gorr TA, Gassmann M. Regulating cellular oxygen sensing by hydroxylation. Cardiovasc Res. 2006;71(4):642–651.
  • Yeo EJ, Chun YS, Park JW. New anticancer strategies targeting HIF-1. Biochem Pharmacol. 2004;68(6):1061–1069.
  • Forsythe JA, Jiang BH, Iyer NV, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol. 1996;16(9):4604–4613.
  • Franke K, Gassmann M, Wielockx B. Erythrocytosis: the HIF pathway in control. Blood. 2013;122(7):1122–1128.
  • Favret F, Richalet JP, Henderson KK, Germack R, Gonzalez NC. Myocardial adrenergic and cholinergic receptor function in hypoxia: correlation with O(2) transport in exercise. Am J Physiol Regul Integr Comp Physiol. 2001;280(3):R730–R738.
  • Gonzalez NC, Clancy RL, Moue Y, Richalet JP. Increasing maximal heart rate increases maximal O2 uptake in rats acclimatized to simulated altitude. J Appl Physiol. 1998;84(1):164–168.
  • Robach P, Fulla Y, Westerterp KR, Richalet JP. Comparative response of EPO and soluble transferrin receptor at high altitude. Med Sci Sports Exerc. 2004;36(9):1493–1498. [discussion 1492].
  • Wu H, Liu X, Jaenisch R, Lodish HF. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell. 1995;83(1):59–67.
  • Ogunshola OO, Bogdanova AY. Epo and non-hematopoietic cells: what do we know? Methods Mol Biol. 2013;982:13–41.
  • Gassmann M, Heinicke K, Soliz J, Ogunshola OO. Non-erythroid functions of erythropoietin. Adv Exp Med Biol. 2003;543:323–330.
  • Binley K, Askham Z, Iqball S, et al. Long-term reversal of chronic anemia using a hypoxia-regulated erythropoietin gene therapy. Blood. 2002;100(7):2406–2413.
  • Wiessner C, Allegrini PR, Ekatodramis D, Jewell UR, Stallmach T, Gassmann M. Increased cerebral infarct volumes in polyglobulic mice overexpressing erythropoietin. J Cereb Blood Flow Metab. 2001;21(7):857–864.
  • Fisher JW. Erythropoietin: physiology and pharmacology update. Exp Biol Med. 2003;228(1):1–14.
  • Masuda S, Okano M, Yamagishi K, Nagao M, Ueda M, Sasaki R. A novel site of erythropoietin production. Oxygen-dependent production in cultured rat astrocytes. J Biol Chem. 1994;269(30):19488–19493.
  • Marti HH, Gassmann M, Wenger RH, et al. Detection of erythropoietin in human liquor: intrinsic erythropoietin production in the brain. Kidney Int. 1997;51(2):416–418.
  • Bernaudin M, Marti HH, Roussel S, et al. A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab. 1999;19(6):643–651.
  • Ammarguellat F, Gogusev J, Drueke TB. Direct effect of erythropoietin on rat vascular smooth-muscle cell via a putative erythropoietin receptor. Nephrol Dial Transplant. 1996;11(4):687–692.
  • El Hasnaoui-Saadani R, Marchant D, Pichon A, et al. Epo deficiency alters cardiac adaptation to chronic hypoxia. Respir Physiol Neurobiol. 2013;186(2):146–154.
  • Tan CC, Eckardt KU, Firth JD, Ratcliffe PJ. Feedback modulation of renal and hepatic erythropoietin mRNA in response to graded anemia and hypoxia. Am J Physiol. 1992;263(3 pt 2):F474–F481.
  • Digicaylioglu M, Bichet S, Marti HH, et al. Localization of specific erythropoietin binding sites in defined areas of the mouse brain. Proc Natl Acad Sci USA. 1995;92(9):3717–3720.
  • Marti HH. Erythropoietin and the hypoxic brain. J Exp Biol. 2004;207(pt 18):3233–3242.
  • Soliz J, Joseph V, Soulage C, et al. Erythropoietin regulates hypoxic ventilation in mice by interacting with brainstem and carotid bodies. J Physiol. 2005;568(pt 2):559–571.
  • Siren AL, Knerlich F, Poser W, Gleiter CH, Brück W, Ehrenreich H. Erythropoietin and erythropoietin receptor in human ischemic/hypoxic brain. Acta Neuropathol. 2001;101(3):271–276.
  • Bernaudin M, Bellail A, Marti HH, et al. Neurons and astrocytes express EPO mRNA: oxygen-sensing mechanisms that involve the redox-state of the brain. Glia. 2000;30(3):271–278.
  • Brines ML, Ghezzi P, Keenan S, et al. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci USA. 2000;97(19):10526–10531.
  • Juul S. Neuroprotective role of erythropoietin in neonates. J Matern Fetal Neonatal Med. 2012;25(suppl 4):105–107.
  • Almaguer-Melian W, Merceron-Martinez D, Pavon-Fuentes N, et al. Erythropoietin promotes neural plasticity and spatial memory recovery in fimbria-fornix-lesioned rats. Neurorehabil Neural Repair. 2015;29(10):979–988.
  • Miskowiak KW, Vinberg M, Harmer CJ, Ehrenreich H, Kessing LV. Erythropoietin: a candidate treatment for mood symptoms and memory dysfunction in depression. Psychopharmacology. 2012; 219(3):687–698.
  • Osborn M, Rustom N, Clarke M, et al. Antidepressant-like effects of erythropoietin: a focus on behavioural and hippocampal processes. PLoS One. 2013;8(9):e72813.
  • Yu X, Shacka JJ, Eells JB, et al. Erythropoietin receptor signalling is required for normal brain development. Development. 2002;129(2):505–516.
  • Chen ZY, Asavaritikrai P, Prchal JT, Noguchi CT. Endogenous erythropoietin signaling is required for normal neural progenitor cell proliferation. J Biol Chem. 2007;282(35):25875–25883.
  • Sola A, Rogido M, Lee BH, Genetta T, Wen TC. Erythropoietin after focal cerebral ischemia activates the Janus kinase-signal transducer and activator of transcription signaling pathway and improves brain injury in postnatal day 7 rats. Pediatr Res. 2005;57(4):481–487.
  • Silva M, Grillot D, Benito A, Richard C, Nuñez G, Fernández-Luna JL. Erythropoietin can promote erythroid progenitor survival by repressing apoptosis through Bcl-XL and Bcl-2. Blood. 1996;88(5):1576–1582.
  • Jelkmann W. Effects of erythropoietin on brain function. Curr Pharm Biotechnol. 2005;6(1):65–79.
  • Wang L, Zhang Z, Wang Y, Zhang R, Chopp M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke. 2004;35(7):1732–1737.
  • Ribatti D, Vacca A, Roccaro AM, Crivellato E, Presta M. Erythropoietin as an angiogenic factor. Eur J Clin Invest. 2003;33(10):891–896.
  • Marti HH, Bernaudin M, Petit E, Bauer C. Neuroprotection and angiogenesis: dual role of erythropoietin in brain ischemia. News Physiol Sci. 2000;15:225–229.
  • Jaquet K, Krause K, Tawakol-Khodai M, Geidel S, Kuck KH. Erythropoietin and VEGF exhibit equal angiogenic potential. Microvasc Res. 2002;64(2):326–333.
  • Roubille F, Prunier F, Barrere-Lemaire S, et al. What is the role of erythropoietin in acute myocardial infarct? Bridging the gap between experimental models and clinical trials. Cardiovasc Drugs Ther. 2013; 27(4):315–331.
  • Bin-Jaliah I, Ammar HI, Mikhailidis DP, et al. Cardiac adaptive responses after hypoxia in an experimental model. Angiology. 2010;61(2):145–156.
  • Cai Z, Manalo DJ, Wei G, et al. Hearts from rodents exposed to intermittent hypoxia or erythropoietin are protected against ischemia-reperfusion injury. Circulation. 2003;108(1):79–85.
  • Cai Z, Semenza GL. Phosphatidylinositol-3-kinase signaling is required for erythropoietin-mediated acute protection against myocardial ischemia/reperfusion injury. Circulation. 2004;109(17):2050–2053.
  • Hoch M, Fischer P, Stapel B, et al. Erythropoietin preserves the endothelial differentiation capacity of cardiac progenitor cells and reduces heart failure during anticancer therapies. Cell Stem Cell. 2011;9(2):131–143.
  • Miro-Murillo M, Elorza A, Soro-Arnaiz I, et al. Acute Vhl gene inactivation induces cardiac HIF-dependent erythropoietin gene expression. PLoS One. 2011;6(7):e22589.
  • Zafiriou MP, Noack C, Unsold B, et al. Erythropoietin responsive cardiomyogenic cells contribute to heart repair post myocardial infarction. Stem Cells. 2014;32(9):2480–2491.
  • Kertesz N, Wu J, Chen TH, Sucov HM, Wu H. The role of erythropoietin in regulating angiogenesis. Dev Biol. 2004;276(1):101–110.
  • Marzo F, Lavorgna A, Coluzzi G, et al. Erythropoietin in heart and vessels: focus on transcription and signalling pathways. J Thromb Thrombolysis. 2008;26(3):183–187.
  • Sanchis-Gomar F, Garcia-Gimenez JL, Pareja-Galeano H, Romagnoli M, Perez-Quilis C, Lippi G. Erythropoietin and the heart: physiological effects and the therapeutic perspective. Int J Cardiol. 2014;171(2):116–125.
  • Burger D, Xenocostas A, Feng QP. Molecular basis of cardioprotection by erythropoietin. Curr Mol Pharmacol. 2009;2(1):56–69.
  • Ong SB, Hall AR, Dongworth RK, et al. Akt protects the heart against ischaemia-reperfusion injury by modulating mitochondrial morphology. Thromb Haemost. 2015;113(3):513–521.
  • Carraway MS, Suliman HB, Jones WS, Chen CW, Babiker A, Piantadosi CA. Erythropoietin activates mitochondrial biogenesis and couples red cell mass to mitochondrial mass in the heart. Circ Res. 2010;106(11):1722–1730.
  • Qin C, Zhou S, Xiao Y, Chen L. Erythropoietin enhances mitochondrial biogenesis in cardiomyocytes exposed to chronic hypoxia through Akt/eNOS signalling pathway. Cell Biol Int. 2014;38(3):335–342.
  • Borovnik-Lesjak V, Whitehouse K, Baetiong A, Artin B, Radhakrishnan J, Gazmuri RJ. High-dose erythropoietin during cardiac resuscitation lessens postresuscitation myocardial stunning in swine. Trans Res. 2013;162(2):110–121.
  • Vasileiou PV, Xanthos T, Barouxis D, et al. Erythropoietin administration facilitates return of spontaneous circulation and improves survival in a pig model of cardiac arrest. Am J Emerg Med. 2014;32(8):871–877.
  • Ogilvie M, Yu X, Nicolas-Metral V, et al. Erythropoietin stimulates proliferation and interferes with differentiation of myoblasts. J Biol Chem. 2000;275(50):39754–39761.
  • Rundqvist H, Rullman E, Sundberg CJ, et al. Activation of the erythropoietin receptor in human skeletal muscle. Eur J Endocrinol. 2009;161(3):427–434.
  • Lundby C, Olsen NV. Effects of recombinant human erythropoietin in normal humans. J Physiol. 2011;589(pt 6):1265–1271.
  • Lundby C, Hellsten Y, Jensen MB, Munch AS, Pilegaard H. Erythropoietin receptor in human skeletal muscle and the effects of acute and long-term injections with recombinant human erythropoietin on the skeletal muscle. J Appl Physiol. 2008;104(4):1154–1160.
  • Contaldo C, Meier C, Elsherbiny A, et al. Human recombinant erythropoietin protects the striated muscle microcirculation of the dorsal skinfold from postischemic injury in mice. Am J Physiol Heart Circ Physiol. 2007;293(1):H274–H283.
  • Launay T, Hagstrom L, Lottin-Divoux S, et al. Blunting effect of hypoxia on the proliferation and differentiation of human primary and rat L6 myoblasts is not counteracted by Epo. Cell Prolif. 2010;43(1):1–8.
  • Lamon S, Zacharewicz E, Stephens AN, Russell AP. EPO-receptor is present in mouse C2C12 and human primary skeletal muscle cells but EPO does not influence myogenesis. Physiol Rep. 2014;2(3):e00256.
  • Rotter R, Menshykova M, Winkler T, et al. Erythropoietin improves functional and histological recovery of traumatized skeletal muscle tissue. J Orthop Res. 2008;26(12):1618–1626.
  • Cayla JL, Maire P, Duvallet A, Wahrmann JP. Erythropoietin induces a shift of muscle phenotype from fast glycolytic to slow oxidative. Int J Sports Med. 2008;29(6):460–465.
  • Hojman P, Brolin C, Gissel H, et al. Erythropoietin over-expression protects against diet-induced obesity in mice through increased fat oxidation in muscles. PLoS One. 2009;4(6):e5894.
  • Nouette-Gaulain K, Bellance N, Prevost B, et al. Erythropoietin protects against local anesthetic myotoxicity during continuous regional analgesia. Anesthesiology. 2009;110(3):648–659.
  • Jia Y, Warin R, Yu X, Epstein R, Noguchi CT. Erythropoietin signaling promotes transplanted progenitor cell survival. FASEB J. 2009;23(9):3089–3099.
  • Mille-Hamard L, Billat VL, Henry E, et al. Skeletal muscle alterations and exercise performance decrease in erythropoietin-deficient mice: a comparative study. BMC Med Genomics. 2012;5:29.
  • Lamon S, Russell AP. The role and regulation of erythropoietin (EPO) and its receptor in skeletal muscle: how much do we really know? Front Physiol. 2013;4:176.
  • Bunn HF. Erythropoietin. Cold Spring Harb Perspect Med. 2013;3(3): a011619.
  • Means RT Jr. Clinical application of recombinant erythropoietin in the anemia of chronic disease. Hematol Oncol Clin North Am. 1994;8(5):933–944.
  • Miller CB, Jones RJ, Piantadosi S, Abeloff MD, Spivak JL. Decreased erythropoietin response in patients with the anemia of cancer. N Engl J Med. 1990;322(24):1689–1692.
  • Spivak JL. Recombinant human erythropoietin and the anemia of cancer. Blood. 1994;84(4):997–1004.
  • Fischl M, Galpin JE, Levine JD, et al. Recombinant human erythropoietin for patients with AIDS treated with zidovudine. N Engl J Med. 1990;322(21):1488–1493.
  • Caro J, Brown S, Miller O, Murray T, Erslev AJ. Erythropoietin levels in uremic nephric and anephric patients. J Lab Clin Med. 1979;93(3):449–458.
  • Cotes PM. Physiological studies of erythropoietin in plasma. In: Jelkmann W, Gross AJ, editors. Erythropoietin. Berlin: Springer; 1989:57–79.
  • Bosman DR, Winkler AS, Marsden JT, Macdougall IC, Watkins PJ. Anemia with erythropoietin deficiency occurs early in diabetic nephropathy. Diabetes Care. 2001;24(3):495–499.
  • Singh A, Eckardt KU, Zimmermann A, et al. Increased plasma viscosity as a reason for inappropriate erythropoietin formation. J Clin Invest. 1993;91(1):251–256.
  • Maxwell PH, Osmond MK, Pugh CW, et al. Identification of the renal erythropoietin-producing cells using transgenic mice. Kidney Int. 1993;44(5):1149–1162.
  • Macarlupu JL, Buvry A, Morel OE, León-Velarde F, Richalet JP, Favret F. Time course of ventilatory acclimatisation to hypoxia in a model of anemic transgenic mice. Respir Physiol Neurobiol. 2006;153(1):14–22.
  • Macarlupu JL, Buvry A, Morel OE, León-Velarde F, Richalet JP, Favret F. Characterisation of the ventilatory response to hypoxia in a model of transgenic anemic mice. Respir Physiol Neurobiol. 2006;150(1):19–26.
  • El Hasnaoui-Saadani R, Pichon A, Marchant D, et al. Cerebral adaptations to chronic anemia in a model of erythropoietin-deficient mice exposed to hypoxia. Am J Physiol Regul Integr Comp Physiol. 2009;296(3):R801–R811.
  • Pichon A, Lamarre Y, Voituron N, et al. Red blood cell deformability is very slightly decreased in erythropoietin deficient mice. Clin Hemorheol Microcirc. 2014;56(1):41–46.
  • Hagstrom L, Agbulut O, El-Hasnaoui-Saadani R, et al. Epo is relevant neither for microvascular formation nor for the new formation and maintenance of mice skeletal muscle fibres in both normoxia and hypoxia. J Biomed Biotechnol. 2010;2010:137817.
  • Deem S, Hedges RG, McKinney S, Polissar NL, Alberts MK, Swenson ER. Mechanisms of improvement in pulmonary gas exchange during isovolemic hemodilution. J Appl Physiol. 1999;87(1):132–141.
  • Lopez TV, Lappin TR, Maxwell P, et al. Autocrine/paracrine erythropoietin signalling promotes JAK/STAT-dependent proliferation of human cervical cancer cells. Int J Cancer. 2011;129(11):2566–2576.
  • Schoch HJ, Fischer S, Marti HH. Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain. 2002;125(pt 11):2549–2557.
  • Favret F, Henderson KK, Clancy RL, Richalet JP, Gonzalez NC. Exercise training alters the effect of chronic hypoxia on myocardial adrenergic and muscarinic receptor number. J Appl Physiol. 2001;91(3):1283–1288.
  • Voituron N, Jeton F, Cholley Y, et al. Catalyzing role of erythropoietin on the nitric oxide central pathway during the ventilatory responses to hypoxia. Physiol Rep. 2014;2(2):e00223.
  • D’Amato FR, Zanettini C, Lampis V, et al. Unstable maternal environment, separation anxiety, and heightened CO2 sensitivity induced by gene-by-environment interplay. PLoS One. 2011;6(4):e18637.
  • Ivy CM, Scott GR. Control of breathing and the circulation in high-altitude mammals and birds. Comp Biochem Physiol A Mol Integr Physiol. 2015;186:66–74.
  • Gregg SG, Willis WT, Brooks GA. Interactive effects of anemia and muscle oxidative capacity on exercise endurance. J Appl Physiol. 1989;67(2):765–770.
  • Hogan MC, Bebout DE, Wagner PD. Effect of hemoglobin concentration on maximal O2 uptake in canine gastrocnemius muscle in situ. J Appl Physiol. 1991;70(3):1105–1112.
  • Koskolou MD, Roach RC, Calbet JA, Rådegran G, Saltin B. Cardiovascular responses to dynamic exercise with acute anemia in humans. Am J Physiol. 1997;273(4 pt 2):H1787–H1793.
  • Teppema LJ, Dahan A. The ventilatory response to hypoxia in mammals: mechanisms, measurement, and analysis. Physiol Rev. 2010;90(2):675–754.
  • Maxova H, Vizek M. Biphasic ventilatory response to hypoxia in unanesthetized rats. Physiol Res. 2001;50(1):91–96.
  • Powell FL, Milsom WK, Mitchell GS. Time domains of the hypoxic ventilatory response. Respir Physiol. 1998;112(2):123–134.
  • Olson EB Jr, Dempsey JA. Rat as a model for humanlike ventilatory adaptation to chronic hypoxia. J Appl Physiol. 1978;44(5):763–769.
  • Bisgard GE, Neubauer LA. Peripheral and central effects of hypoxia. In: Dempsey JA, Pack AI, editors. Regulation of Breathing. New York, NY: Dekker; 1995:617–618.
  • Powell FL, Huey KA, Dwinell MR. Central nervous system mechanisms of ventilatory acclimatization to hypoxia. Respir Physiol. 2000;121(2–3):223–236.
  • LaManna JC, Chavez JC, Pichiule P. Structural and functional adaptation to hypoxia in the rat brain. J Exp Biol. 2004;207(pt 18):3163–3169.
  • Liu J, Narasimhan P, Yu F, Chan PH. Neuroprotection by hypoxic preconditioning involves oxidative stress-mediated expression of hypoxia-inducible factor and erythropoietin. Stroke. 2005;36(6):1264–1269.
  • Hagstrom L, Canon F, Agbulut O, et al. Skeletal muscle intrinsic functional properties are preserved in a model of erythropoietin deficient mice exposed to hypoxia. Pflugers Arch. 2010;459(5):713–723.
  • Mouly V, Edom F, Decary S, Vicart P, Barbert JP, Butler-Browne GS. SV40 large T antigen interferes with adult myosin heavy chain expression, but not with differentiation of human satellite cells. Exp Cell Res. 1996;225(2):268–276.
  • Rosario R, Epstein M. Relationship between erythropoietin administration and alterations of renin-angiotensin-aldosterone. J Renin Angiotensin Aldosterone Syst. 2006;7(3):135–138.
  • Rocha J, Eduardo-Figueira M, Barateiro A, et al. Erythropoietin reduces acute lung injury and multiple organ failure/dysfunction associated to a scald-burn inflammatory injury in the rat. Inflammation. 2015;38(1):312–326.