HIF-mediated increased ROS from reduced mitophagy and decreased catalase causes neocytolysis

Journal of Molecular Medicine

Volumn 93, Issue 8, 2015, Pages 857-866

  Song, Jihyun ^a   Yoon, Donghoon ^a,e   Christensen, Robert D ^b   Horvathova, Monika ^c   Thiagarajan, Perumal ^d   Prchal, Josef T ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b INTERMOUNTAIN HEALTHCARE   (United States)

^c PALACKÝ UNIVERSITY   (Czech Republic)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Catalase; HIFs; Hypoxia; Mitochondria; Neocytolysis; Reactive oxygen species (ROS)

Indexed keywords

CATALASE; HYPOXIA INDUCIBLE FACTOR; OXYGEN; PROTEIN BNIP3; REACTIVE OXYGEN METABOLITE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MICRORNA; MIRN-21 MICRORNA, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOLYSIS; ENZYME ACTIVITY; ERYTHROCYTE; EXPOSURE; HEMATOCRIT; HUMAN; HYPOXIA; INFANT; MITOCHONDRION; MITOPHAGY; MOUSE; MURINE MODEL; NEOCYTOLYSIS; NEWBORN; NONHUMAN; NORMAL HUMAN; PROTEIN EXPRESSION; RETICULOCYTE; ANIMAL; ANOXIA; C57BL MOUSE; CELL LINE; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; POLYCYTHEMIA;

ANIMALS; ANOXIA; CATALASE; CELL LINE; ERYTHROCYTES; GENE DELETION; GENE EXPRESSION REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICE, INBRED C57BL; MICRORNAS; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; POLYCYTHEMIA; REACTIVE OXYGEN SPECIES; RETICULOCYTES;

EID: 84937972798     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-015-1294-y     Document Type: Article

References (36)

1. Alfrey CP, Rice L, Udden MM, Driscoll TB (1997) Neocytolysis: physiological down-regulator of red-cell mass. Lancet 349(9062):1389–1390
2. Alfrey CP, Udden MM, Huntoon CL, Driscoll T (1996) Destruction of newly released red blood cells in space flight. Med Sci Sports Exerc 28(10 Suppl):S42–S44
3. Rice L, Ruiz W, Driscoll T, Whitley CE, Tapia R, Hachey DL, Gonzales GF, Alfrey CP (2001) Neocytolysis on descent from altitude: a newly recognized mechanism for the control of red cell mass. Ann Intern Med 134(8):652–656
4. Risso A, Turello M, Biffoni F, Antonutto G (2007) Red blood cell senescence and neocytolysis in humans after high altitude acclimatization. Blood Cells Mol Dis 38(2):83–92
5. Sivilotti ML (2004) Oxidant stress and haemolysis of the human erythrocyte. Toxicol Rev 23(3):169–188
6. Ghaffari S (2008) Oxidative stress in the regulation of normal and neoplastic hematopoiesis. Antioxid Redox Signal 10(11):1923–1940
7. Rogers SC, Said A, Corcuera D, McLaughlin D, Kell P, Doctor A (2009) Hypoxia limits antioxidant capacity in red blood cells by altering glycolytic pathway dominance. FASEB J 23(9):3159–3170
8. Baillie K (2011) Altitude air pressure calculator. http://www.altitude.org/air_pressure.php. Accessed 10 Jan 2012
9. Sanchez C, Merino C, Figallo M (1970) Simultaneous measurement of plasma volume and cell mass in polycythemia of high altitude. J Appl Physiol 28(6):775–778
10. Evans GO (2008) Animal hematotoxicology: a practical guide for toxicologists and biomedical researchers, illustrated edn. CRC Press, Boca Raton
11. Hickey MM, Lam JC, Bezman NA, Rathmell WK, Simon MC (2007) von Hippel-Lindau mutation in mice recapitulates Chuvash polycythemia via hypoxia-inducible factor-2alpha signaling and splenic erythropoiesis. J Clin Invest 117(12):3879–3889
12. Ang SO, Chen H, Hirota K, Gordeuk VR, Jelinek J, Guan Y, Liu E, Sergueeva AI, Miasnikova GY, Mole D et al (2002) Disruption of oxygen homeostasis underlies congenital Chuvash polycythemia. Nat Genet 32(4):614–621
13. Hams E, Saunders SP, Cummins EP, O’Connor A, Tambuwala MT, Gallagher WM, Byrne A, Campos-Torres A, Moynagh PM, Jobin C et al (2011) The hydroxylase inhibitor dimethyloxallyl glycine attenuates endotoxic shock via alternative activation of macrophages and IL-10 production by B1 cells. Shock 36(3):295–302
14. Sandoval H, Thiagarajan P, Dasgupta SK, Schumacher A, Prchal JT, Chen M, Wang J (2008) Essential role for Nix in autophagic maturation of erythroid cells. Nature 454(7201):232–235
15. Aerbajinai W, Giattina M, Lee YT, Raffeld M, Miller JL (2003) The proapoptotic factor Nix is coexpressed with Bcl-xL during terminal erythroid differentiation. Blood 102(2):712–717
16. Fei P, Wang W, Kim SH, Wang S, Burns TF, Sax JK, Buzzai M, Dicker DT, McKenna WG, Bernhard EJ et al (2004) Bnip3L is induced by p53 under hypoxia, and its knockdown promotes tumor growth. Cancer Cell 6(6):597–609
17. Bakker WJ, Harris IS, Mak TW (2007) FOXO3a is activated in response to hypoxic stress and inhibits HIF1-induced apoptosis via regulation of CITED2. Mol Cell 28(6):941–953
18. Marinkovic D, Zhang X, Yalcin S, Luciano JP, Brugnara C, Huber T, Ghaffari S (2007) Foxo3 is required for the regulation of oxidative stress in erythropoiesis. J Clin Invest 117(8):2133–2144
19. Scortegagna M, Ding K, Oktay Y, Gaur A, Thurmond F, Yan LJ, Marck BT, Matsumoto AM, Shelton JM, Richardson JA et al (2003) Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1-/- mice. Nat Genet 35(4):331–340
20. Muratsu-Ikeda S, Nangaku M, Ikeda Y, Tanaka T, Wada T, Inagi R (2012) Downregulation of miR-205 modulates cell susceptibility to oxidative and endoplasmic reticulum stresses in renal tubular cells. PLoS One 7(7):e41462
21. Haque R, Chun E, Howell JC, Sengupta T, Chen D, Kim H (2012) MicroRNA-30b-mediated regulation of catalase expression in human ARPE-19 cells. PLoS One 7(8):e42542
22. Yu D, dos Santos CO, Zhao G, Jiang J, Amigo JD, Khandros E, Dore LC, Yao Y, D’Souza J, Zhang Z et al (2010) miR-451 protects against erythroid oxidant stress by repressing 14-3-3zeta. Genes Dev 24(15):1620–1633
23. Zhang X, Ng WL, Wang P, Tian L, Werner E, Wang H, Doetsch P, Wang Y (2012) MicroRNA-21 modulates the levels of reactive oxygen species by targeting SOD3 and TNFalpha. Cancer Res 72(18):4707–4713
24. Jopling J, Henry E, Wiedmeier SE, Christensen RD (2009) Reference ranges for hematocrit and blood hemoglobin concentration during the neonatal period: data from a multihospital health care system. Pediatrics 123(2):e333–e337
25. Prchal JT (ed) (2010) Secondary polycythemia (Erythrocytosis). Williams hematology, 8th edn. McGraw Hill, New York
26. Christensen RD, Lambert DK, Henry E, Eggert LD, Yaish HM, Reading NS, Prchal JT (2012) Unexplained extreme hyperbilirubinemia among neonates in a multihospital healthcare system. Blood Cells Mol Dis. doi:10.1016/j.bcmd.2012.10.004
27. Fasjena GJ, Bates HH, Reid AF (1950) Changes in blood volume in neonatal period. Am J Dis Child 79:510–511
28. Maisels MJ, Kring E (2006) The contribution of hemolysis to early jaundice in normal newborns. Pediatrics 118(1):276–279
29. Christensen RD, Lambert DK, Henry E, Yaish HM, Prchal JT (2014) End-tidal carbon monoxide as an indicator of the hemolytic rate. Blood Cells Mol Dis. doi:10.1016/j.bcmd.2014.11.018
30. Alfrey CP, Fishbane S (2007) Implications of neocytolysis for optimal management of anaemia in chronic kidney disease. Nephron Clin Pract 106(4):149–156
31. Emerling BM, Weinberg F, Liu JL, Mak TW, Chandel NS (2008) PTEN regulates p300-dependent hypoxia-inducible factor 1 transcriptional activity through Forkhead transcription factor 3a (FOXO3a). Proc Natl Acad Sci U S A 105(7):2622–2627
32. Holmstrom KM, Finkel T (2014) Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat Rev Mol Cell Biol 15(6):411–421
33. Hyoudou K, Nishikawa M, Kobayashi Y, Kuramoto Y, Yamashita F, Hashida M (2007) Analysis of in vivo nuclear factor-kappaB activation during liver inflammation in mice: prevention by catalase delivery. Mol Pharmacol 71(2):446–453
34. Mock DM, Lankford GL, Widness JA, Burmeister LF, Kahn D, Strauss RG (1999) Measurement of red cell survival using biotin-labeled red cells: validation against 51Cr-labeled red cells. Transfusion 39(2):156–162
35. Vogel J, Kiessling I, Heinicke K, Stallmach T, Ossent P, Vogel O, Aulmann M, Frietsch T, Schmid-Schonbein H, Kuschinsky W et al (2003) Transgenic mice overexpressing erythropoietin adapt to excessive erythrocytosis by regulating blood viscosity. Blood 102(6):2278–2284
36. Yoon D, Pastore YD, Divoky V, Liu E, Mlodnicka AE, Rainey K, Ponka P, Semenza GL, Schumacher A, Prchal JT (2006) Hypoxia-inducible factor-1 deficiency results in dysregulated erythropoiesis signaling and iron homeostasis in mouse development. J Biol Chem 281(35):25703–25711