Constitutive excessive erythrocytosis causes inflammation and increased vascular permeability in aged mouse brain

Brain Research

Volumn 1531, Issue , 2013, Pages 48-57

  Ogunshola, O O ^a   Moransard, M ^a   Gassmann, M ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Cell death; Endothelial activation; Endothelium; Erythropoietin

Indexed keywords

BETA CATENIN; ERYTHROPOIETIN; INTERLEUKIN 6; OCCLUDIN; PROTEIN BCL XL; PROTEIN P53; RNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; BRAIN BLOOD VESSEL; BRAIN TISSUE; CELL DEATH; CONTROLLED STUDY; CORRELATION ANALYSIS; ENCEPHALITIS; ERYTHROCYTOSIS; FEMALE; LIFESPAN; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; TRANSGENIC MOUSE;

ANIMALIA; MUS MUSCULUS;

CELL DEATH; ENDOTHELIAL ACTIVATION; ENDOTHELIUM; ERYTHROPOIETIN;

AGING; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CAPILLARY PERMEABILITY; ENDOTHELIUM, VASCULAR; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; POLYCYTHEMIA;

EID: 84883265813     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.07.033     Document Type: Article

References (38)

1. N.J. Abbott Inflammatory mediators and modulation of blood-brain barrier permeability Cell Mol. Neurobiol. 20 2000 131 147
2. J.I. Alvarez, and J.M. Teale Breakdown of the blood-brain barrier and blood-cerebrospinal fluid barrier is associated with differential leukocyte migration in distinct compartments of the CNS during the course of murine NCC J. Neuroimmunol. 173 2006 45 55
3. A.T. Argaw, Y. Zhang, B.J. Snyder, M.L. Zhao, N. Kopp, S.C. Lee, C.S. Raine, C.F. Brosnan, and G.R. John IL-1beta regulates blood-brain barrier permeability via reactivation of the hypoxia-angiogenesis program J. Immunol. 177 2006 5574 5584
4. G. Bertinieri, G. Parati, L. Ulian, C. Santucciu, P. Massaro, R. Cosentini, G. Torgano, A. Morganti, and G. Mancia Hemodilution reduces clinic and ambulatory blood pressure in polycythemic patients Hypertension 31 1998 848 853
5. Z.Y. Chen, P. Asavaritikrai, J.T. Prchal, and C.T. Noguchi Endogenous erythropoietin signaling is required for normal neural progenitor cell proliferation J. Biol. Chem. 282 2007 25875 25883
6. Z.Z. Chong, J.Q. Kang, and K. Maiese Erythropoietin is a novel vascular protectant through activation of Akt1 and mitochondrial modulation of cysteine proteases Circulation 106 2002 2973 2979
7. M. Digicaylioglu, S. Bichet, H.H. Marti, R.H. Wenger, L.A. Rivas, C. Bauer, and M. Gassmann Localization of specific erythropoietin binding sites in defined areas of the mouse brain Proc. Natl. Acad. Sci. USA 92 1995 3717 3720
8. A. Falanga, M. Marchetti, V. Evangelista, A. Vignoli, M. Licini, M. Balicco, S. Manarini, G. Finazzi, C. Cerletti, and T. Barbui Polymorphonuclear leukocyte activation and hemostasis in patients with essential thrombocythemia and polycythemia vera Blood 96 2000 4261 4266
9. J.W. Fisher Erythropoietin: physiology and pharmacology update Exp. Biol. Med. (Maywood) 228 2003 1 14
10. T. Frietsch, M.H. Maurer, J. Vogel, M. Gassmann, W. Kuschinsky, and K.F. Waschke Reduced cerebral blood flow but elevated cerebral glucose metabolic rate in erythropoietin overexpressing transgenic mice with excessive erythrocytosis J. Cereb. Blood Flow Metab. 27 2007 469 476
11. C. Grimm, A. Wenzel, M. Groszer, H. Mayser, M. Seeliger, M. Samardzija, C. Bauer, M. Gassmann, and C.E. Reme HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration Nat. Med. 8 2002 718 724
12. K. Heinicke, O. Baum, O.O. Ogunshola, J. Vogel, T. Stallmach, D.P. Wolfer, S. Keller, K. Weber, P.D. Wagner, M. Gassmann, and V. Djonov Excessive erythrocytosis in adult mice overexpressing erythropoietin leads to hepatic, renal, neuronal, and muscular degeneration Am. J. Physiol. Regul. Integr. Comp. Physiol. 291 2006 R947 R956
13. A.K. Junk, A. Mammis, S.I. Savitz, M. Singh, S. Roth, S. Malhotra, P.S. Rosenbaum, A. Cerami, M. Brines, and D.M. Rosenbaum Erythropoietin administration protects retinal neurons from acute ischemia-reperfusion injury Proc. Natl. Acad. Sci. USA 99 2002 10659 10664
14. C.G. Kevil, H. Pruitt, T.J. Kavanagh, J. Wilkerson, F. Farin, D. Moellering, V.M. Darley-Usmar, D.C. Bullard, and R.P. Patel Regulation of endothelial glutathione by ICAM-1: implications for inflammation Faseb. J. 18 2004 1321 1323
15. S. Korbel, T. Bittorf, E. Siegl, and B. Kollner Recombinant human erythropoietin induces proliferation and Ca(2+)-influx in specific leukocyte subpopulations of rainbow trout (Oncorhynchus mykiss) blood and head kidney cells J. Comp. Physiol. [B] 174 2004 121 128
16. A. Kumral, S. Genc, E. Ozer, O. Yilmaz, N. Gokmen, T.F. Koroglu, N. Duman, K. Genc, and H. Ozkan Erythropoietin downregulates bax and DP5 proapoptotic gene expression in neonatal hypoxic-ischemic brain injury Biol. Neonate. 89 2006 205 210
17. Y. Li, Z.Y. Lu, M. Ogle, and L. Wei Erythropoietin prevents blood brain barrier damage induced by focal cerebral ischemia in mice Neurochem. Res. 32 2007 2132 2141
18. O.M. Martinez-Estrada, E. Rodriguez-Millan, E. Gonzalez-De Vicente, M. Reina, S. Vilaro, and M. Fabre Erythropoietin protects the in vitro blood-brain barrier against VEGF-induced permeability Eur. J. Neurosci. 18 2003 2538 2544
19. S. Masuda, M. Okano, K. Yamagishi, M. Nagao, M. Ueda, and R. Sasaki A novel site of erythropoietin production. Oxygen-dependent production in cultured rat astrocytes J. Biol. Chem. 269 1994 19488 19493
20. T. Neunteufl, S. Heher, T. Stefenelli, I. Pabinger, and H. Gisslinger Endothelial dysfunction in patients with polycythaemia vera Br. J. Haematol. 115 2001 354 359
21. O.O. Ogunshola, V. Djonov, R. Staudt, J. Vogel, and M. Gassmann Chronic excessive erythrocytosis induces endothelial activation and damage in mouse brain Am. J. Physiol. Regul. Integr. Comp. Physiol. 290 2006 R678 R684
22. D. Ribatti, A. Vacca, A.M. Roccaro, E. Crivellato, and M. Presta Erythropoietin as an angiogenic factor Eur. J. Clin. Invest. 33 2003 891 896
23. R. Ross Atherosclerosis-an inflammatory disease N. Engl. J. Med. 340 1999 115 126
24. F.T. Ruschitzka, R.H. Wenger, T. Stallmach, T. Quaschning, C. de Wit, K. Wagner, R. Labugger, M. Kelm, G. Noll, T. Rulicke, S. Shaw, R.L. Lindberg, B. Rodenwaldt, H. Lutz, C. Bauer, T.F. Luscher, and M. Gassmann Nitric oxide prevents cardiovascular disease and determines survival in polyglobulic mice overexpressing erythropoietin Proc. Natl. Acad. Sci. USA 97 2000 11609 11613
25. R. Shurtz-Swirski, B. Kristal, S.M. Shasha, G. Shapiro, R. Geron, and S. Sela Interaction between erythropoietin and peripheral polymorphonuclear leukocytes in continuous ambulatory dialysis patients Nephron 91 2002 759 761
26. J. Soliz, V. Joseph, C. Soulage, C. Becskei, J. Vogel, J.M. Pequignot, O. Ogunshola, and M. Gassmann Erythropoietin regulates hypoxic ventilation in mice by interacting with brainstem and carotid bodies J. Physiol. 2005
27. P.H. Stone, A.U. Coskun, Y. Yeghiazarians, S. Kinlay, J.J. Popma, R.E. Kuntz, and C.L. Feldman Prediction of sites of coronary atherosclerosis progression: in vivo profiling of endothelial shear stress, lumen, and outer vessel wall characteristics to predict vascular behavior Curr. Opin Cardiol. 18 2003 458 470
28. L. Velly, L. Pellegrini, B. Guillet, N. Bruder, and P. Pisano Erythropoietin 2nd cerebral protection after acute injuries: a double-edged sword? Pharmacol. Ther. 128 2010 445 459
29. J. Vogel, I. Kiessling, K. Heinicke, T. Stallmach, P. Ossent, O. Vogel, M. Aulmann, T. Frietsch, H. Schmid-Schonbein, W. Kuschinsky, and M. Gassmann Transgenic mice overexpressing erythropoietin adapt to excessive erythrocytosis by regulating blood viscosity Blood 102 2003 2278 2284
30. J. Vogel, and M. Gassmann Erythropoietic and non-erythropoietic functions of erythropoietin in mouse models J. Physiol. 589 2011 1259 1264
31. K.F. Wagner, D.M. Katschinski, J. Hasegawa, D. Schumacher, B. Meller, U. Gembruch, U. Schramm, W. Jelkmann, M. Gassmann, and J. Fandrey Chronic inborn erythrocytosis leads to cardiac dysfunction and premature death in mice overexpressing erythropoietin Blood 97 2001 536 542
32. T.G. Walsh, R.P. Murphy, P. Fitzpatrick, K.D. Rochfort, A.F. Guinan, A. Murphy, and P.M. Cummins Stabilization of brain microvascular endothelial barrier function by shear stress involves VE-cadherin signaling leading to modulation of pTyr- Occludin levels J. Cell Physiol. 226 2011 3053 3063
33. E. Warabi, Y. Wada, H. Kajiwara, M. Kobayashi, N. Koshiba, T. Hisada, M. Shibata, J. Ando, M. Tsuchiya, T. Kodama, and N. Noguchi Effect on endothelial cell gene expression of shear stress, oxygen concentration, and low-density lipoprotein as studied by a novel flow cell culture system Free Radic Biol. Med. 37 2004 682 694
34. L. Wei, B.H. Han, Y. Li, C.L. Keogh, D.M. Holtzman, and S.P. Yu Cell death mechanism and protective effect of erythropoietin after focal ischemia in the whisker-barrel cortex of neonatal rats J. Pharmacol. Exp. Ther. 317 2006 109 116
35. T.C. Wen, Y. Sadamoto, J. Tanaka, P.X. Zhu, K. Nakata, Y.J. Ma, R. Hata, and M. Sakanaka Erythropoietin protects neurons against chemical hypoxia and cerebral ischemic injury by up-regulating Bcl-xL expression J. Neurosci. Res. 67 2002 795 803
36. C. Wiessner, P.R. Allegrini, D. Ekatodramis, U.R. Jewell, T. Stallmach, and M. Gassmann Increased cerebral infarct volumes in polyglobulic mice overexpressing erythropoietin J. Cereb. Blood Flow Metab. 21 2001 857 864
37. H. Xu, A. Manivannan, K.A. Goatman, H.R. Jiang, J. Liversidge, P.F. Sharp, J.V. Forrester, and I.J. Crane Reduction in shear stress, activation of the endothelium, and leukocyte priming are all required for leukocyte passage across the blood-retina barrier J. Leukoc. Biol. 75 2004 224 232
38. H. Yamawaki, S. Lehoux, and B.C. Berk Chronic physiological shear stress inhibits tumor necrosis factor-induced proinflammatory responses in rabbit aorta perfused ex vivo Circulation 108 2003 1619 1625