Heme oxygenase-1 deficiency alters erythroblastic Island formation, steady-state erythropoiesis and red blood cell lifespan in mice

Haematologica

Volumn 100, Issue 5, 2015, Pages 601-610

  Fraser, Stuart T ^a   Midwinter, Robyn G ^b   Coupland, Lucy A ^c   Kong, Stephanie ^d   Berger, Birgit S ^b,g   Yeo, Jia Hao ^a   Andrade, Osvaldo Cooley ^a   Cromer, Deborah ^e   Suarna, Cacang ^b,d   Lam, Magda ^b,d   Maghzal, Ghassan J ^b,d,e   Chong, Beng H ^f   Parish, Christopher R ^c   Stocker, Roland ^b,d,e  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c Australian National University   (Australia)

^d VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^e UNIVERSITY OF NEW SOUTH WALES   (Australia)

^f UNIVERSITY OF NEW SOUTH WALES   (Australia)

^g GERMAN CANCER RESEARCH CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; HEME; HEME OXYGENASE 1; HOMEODOMAIN PROTEIN; PAIRED RELATED HOMEODOMAIN PROTEIN; PHOSPHATIDYLSERINE; SIALOADHESIN; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; VERY LATE ACTIVATION ANTIGEN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BILIRUBIN BLOOD LEVEL; BONE MARROW DERIVED MACROPHAGE; CELL SIZE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME DEFICIENCY; ERYTHROBLAST; ERYTHROCYTE; ERYTHROPOIESIS; FEMALE; FLOW CYTOMETRY; HEMATOCRIT; HEMOGLOBIN BLOOD LEVEL; MALE; MICROCYTIC ANEMIA; MOUSE; NONHUMAN; OXIDATIVE STRESS; SCANNING ELECTRON MICROSCOPY; SPLEEN WEIGHT; SPLENOMEGALY; ANIMAL; BONE MARROW CELL; CELL COMMUNICATION; CELL DIFFERENTIATION; CYTOLOGY; DEFICIENCY; GENETICS; GROWTH DISORDER; HEMOLYTIC ANEMIA; IMMUNOPHENOTYPING; IRON METABOLISM DISORDER; KNOCKOUT MOUSE; LIVER; MACROPHAGE; MEAN CORPUSCULAR VOLUME; METABOLISM; SPLEEN;

ANEMIA, HEMOLYTIC; ANIMALS; BONE MARROW CELLS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL SURVIVAL; ERYTHROBLASTS; ERYTHROCYTE INDICES; ERYTHROCYTES; ERYTHROPOIESIS; GROWTH DISORDERS; HEME OXYGENASE-1; IMMUNOPHENOTYPING; IRON METABOLISM DISORDERS; LIVER; MACROPHAGES; MICE; MICE, KNOCKOUT; OXIDATIVE STRESS; SPLEEN;

EID: 84929147920     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2014.116368     Document Type: Article

References (50)

1. Chasis JA, Mohandas N. Erythroblastic islands: niches for erythropoiesis. Blood. 2008;112(3):470-478.
2. An X, Mohandas N. Erythroblastic islands, terminal erythroid differentiation and reticulocyte maturation. Int J Hematol. 2011;93(2):139-143.
3. Mohandas N, Chasis JA. The erythroid niche: molecular processes occurring within erythroblastic islands. Transfus Clin Biol. 2010;17(3):110-111.
4. Yoshida H, Kawane K, Koike M, et al. Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature. 2005;437(7059):754-758.
5. Ji P, Murata-Hori M, Lodish HF. Formation of mammalian erythrocytes: chromatin condensation and enucleation. Trends Cell Biol. 2011;21(7):409-415.
6. Coupland LA, Cromer D, Davenport MP, Parish CR. A novel fluorescent-based assay reveals that thrombopoietin signaling and Bcl-X(L) influence, respectively, platelet and erythrocyte lifespans. Exp Hematol. 2010;38(6):453-461.
7. Schroit AJ, Madsen JW, Tanaka Y. In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membranes. J Biol Chem. 1985;260(8): 5131-5138.
8. Miyanishi M, Tada K, Koike M, et al. Identification of Tim4 as a phosphatidylserine receptor. Nature. 2007;450(7168):435-439.
9. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA. 1968;61(2):748-755.
10. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev. 2006;86(2):583-650.
11. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science. 1987;235(4792):1043-1046.
12. Poss KD, Tonegawa S. Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci USA. 1997;94(20):10919-10924.
13. Duckers HJ, Boehm M, True AL, et al. Heme oxygenase-1 protects against vascular constriction and proliferation. Nat Med. 2001;7(6):693-698.
14. Poss KD, Tonegawa S. Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci USA. 1997;94(20):10925-10930.
15. Koizumi S. Human heme oxygenase-1 deficiency: a lesson on serendipity in the discovery of the novel disease. Pediatr Int. 2007;49(2):125-132.
16. Kovtunovych G, Eckhaus MA, Ghosh MC, Ollivierre-Wilson H, Rouault TA. Dysfunction of the heme recycling system in heme oxygenase 1-deficient mice: effects on macrophage viability and tissue iron distribution. Blood. 2010;116(26):6054-6062.
17. Yachie A, Niida Y, Wada T, et al. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest. 1999;103(1):129-135.
18. Kartikasari AE, Wagener FA, Yachie A, et al. Hepcidin suppression and defective iron recycling account for dysregulation of iron homeostasis in heme oxygenase-1 deficiency. J Cell Mol Med. 2009;13(9B):3091-3102.
19. Denschlag D, Marculescu R, Unfried G, et al. The size of a microsatellite polymorphism of the haem oxygenase 1 gene is associated with idiopathic recurrent miscarriage. Mol Hum Reprod. 2004;10(3):211-214.
20. Gil GP, Ananina G, Oliveira MB, et al. Polymorphism in the HMOX1 gene is associated with high levels of fetal hemoglobin in Brazilian patients with sickle cell anemia. Hemoglobin. 2013;37(4):315-324.
21. Kaartokallio T, Klemetti MM, Timonen A, et al. Microsatellite polymorphism in the heme oxygenase-1 promoter is associated with nonsevere and late-onset preeclampsia. Hypertension. 2014;64(1):172-177.
22. Fraser ST, Midwinter RG, Berger BS, Stocker R. A critical link between iron metabolism, erythropoiesis, and development. Adv Hematol. 2011;2011:473709.
23. Stocker R. Induction of haem oxygenase as a defence against oxidative stress. Free Radic Res Commun. 1990;9(2):101-112.
24. Cao YA, Wagers AJ, Karsunky H, et al. Heme oxygenase-1 deficiency leads to disrupted response to acute stress in stem cells and progenitors. Blood. 2008;112(12):4494-4502.
25. Cao YA, Kusy S, Luong R, et al. Heme oxygenase-1 deletion affects stress erythropoiesis. PLoS One. 2011;6(5):e20634.
26. Yet SF, Layne MD, Liu X, et al. Absence of heme oxygenase-1 exacerbates atherosclerotic lesion formation and vascular remodeling. FASEB J. 2003;17(12):1759-1761.
27. Fraser ST, Isern J, Baron MH. Use of transgenic fluorescent reporter mouse lines to monitor hematopoietic and erythroid development during embryogenesis. Methods Enzymol. 2010;476:403-427.
28. Bayer SB, Maghzal G, Stocker R, Hampton MB, Winterbourn CC. Neutrophil-mediated oxidation of erythrocyte peroxiredoxin 2 as a potential marker of oxidative stress in inflammation. FASEB J. 2013;27(8):3315-3322.
29. Beutler E. Red cell metabolism. A manual of biochemical methods. 3rd ed. 1984, New York: Grune & Stratton.
30. Socolovsky M, Nam H, Fleming MD, et al. Ineffective erythropoiesis in Stat5a-/-5b-/-mice due to decreased survival of early erythroblasts. Blood. 2001;98(12):3261-3273.
31. Chen K, Liu J, Heck S, et al. Resolving the distinct stages in erythroid differentiation based on dynamic changes in membrane protein expression during erythropoiesis. Proc Natl Acad Sci USA. 2009;106(41): 17413-17418.
32. Parish CR, Warren HS. Use of the intracellular fluorescent dye CFSE to monitor lymphocyte migration and proliferation. Curr Protoc Immunol. 2002;Chapter 4:Unit 4 9.
33. Garcia-Santos D, Schranzhofer M, Horvathova M, et al. Heme oxygenase 1 is expressed in murine erythroid cells where it controls the level of regulatory heme. Blood. 2014;123(14):2269-2277.
34. Eshghi S, Vogelezang MG, Hynes RO, Griffith LG, Lodish HF. α4β1 integrin and erythropoietin mediate temporally distinct steps in erythropoiesis: integrins in red cell development. J Cell Biol. 2007;177(5):871-880.
35. Sadahira Y, Yoshino T, Monobe Y. Very late activation antigen 4-vascular cell adhesion molecule 1 interaction is involved in the formation of erythroblastic islands. J Exp Med. 1995;181(1):411-415.
36. Jacobsen RN, Forristal CE, Raggatt LJ, et al. Mobilization with granulocyte colony-stimulating factor blocks medullar erythropoiesis by depleting F4/80+VCAM1+ CD169+ERHR3+ Ly6G+ erythroid island macrophages in the mouse. Exp Hematol. 2014;42(7):547-561.
37. Sadahira Y, Mori M, Awai M, Watarai S, Yasuda T. Forssman glycosphingolipid as an immunohistochemical marker for mouse stromal macrophages in hematopoietic foci. Blood. 1988;72(1):42-48.
38. Ulyanova T, Jiang Y, Padilla S, Nakamoto B, Papayannopoulou T. Combinatorial and distinct roles of α5 and α4 integrins in stress erythropoiesis in mice. Blood. 2011;117(3): 975-985.
39. Lee TH, Kim SU, Yu SL, et al. Peroxiredoxin II is essential for sustaining life span of erythrocytes in mice. Blood. 2003;101(12): 5033-5038.
40. Low FM, Hampton MB, Peskin AV, Winterbourn CC. Peroxiredoxin 2 functions as a noncatalytic scavenger of low-level hydrogen peroxide in the erythrocyte. Blood. 2007;109(6):2611-2617.
41. Peskin AV, Dickerhof N, Poynton RA, et al. Hyperoxidation of peroxiredoxins 2 and 3: rate constants for the reactions of the sulfenic acid of the peroxidatic cysteine. J Biol Chem. 2013;288(20):14170-14177.
42. Chow A, Lucas D, Hidalgo A, et al. Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J Exp Med. 2011;208(2):261-271.
43. Ramos P, Casu C, Gardenghi S, et al. Macrophages support pathological erythropoiesis in polycythemia vera and β-thalassemia. Nat Med. 2013;19(4):437-445.
44. Jeney V, Balla J, Yachie A, et al. Pro-oxidant and cytotoxic effects of circulating heme. Blood. 2002;100(3):879-887.
45. McGrath KE, Kingsley PD, Koniski AD, et al. Enucleation of primitive erythroid cells generates a transient population of "pyrenocytes" in the mammalian fetus. Blood. 2008;111(4):2409-2417.
46. Isern J, Fraser ST, He Z, Baron MH. The fetal liver is a niche for maturation of primitive erythroid cells. Proc Natl Acad Sci USA. 2008;105(18):6662-6667.
47. Soares MP, Seldon MP, Gregoire IP, et al. Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J Immunol. 2004;172(6):3553-3563.
48. Belcher JD, Mahaseth H, Welch TE, et al. Heme oxygenase-1 is a modulator of inflammation and vaso-occlusion in transgenic sickle mice. J Clin Invest. 2006;116(3):808-816.
49. Wu BJ, Di Girolamo N, Beck K, et al. Probucol [4,4’-[(1-methylethylidene)bis (thio)]bis-[2,6-bis(1,1-dimethylethyl)phenol]] inhibits compensatory remodeling and promotes lumen loss associated with atherosclerosis in apolipoprotein E-deficient mice. J Pharmacol Exp Ther. 2007;321(2): 477-484.
50. Miharada K, Hiroyama T, Sudo K, Nagasawa T, Nakamura Y. Efficient enucleation of erythroblasts differentiated in vitro from hematopoietic stem and progenitor cells. Nat Biotechnol. 2006;24(10):1255-1256.