Haemolytic anaemia and alterations in hepatic iron metabolism in aged mice lacking Cu,Zn-superoxide dismutase

Biochemical Journal

Volumn 420, Issue 3, 2009, Pages 383-390

  Starzyński, Rafał R ^a   Canonne Hergaux, François ^b   Willemetz, Alexandra ^b   Gralak, Mikołaj A ^c   Woliński, Jarosław ^d   Stys, Agnieszka ^a   Olszak, Jarosław ^a   Lipiński, Paweł ^a  

^a INSTITUTE OF GENETICS AND ANIMAL BREEDING   (Poland)

^b CNRS   (France)

^c WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

^d KIELANOWSKI INSTITUTE OF ANIMAL PHYSIOLOGY AND NUTRITION   (Poland)

Author keywords

Erythrophagocytosis; Haem oxygenase; Haemolysis; Iron; Kupffer cells; Superoxide dismutase 1

Indexed keywords

ERYTHROPHAGOCYTOSIS; HAEM OXYGENASE; HAEMOLYSIS; KUPFFER CELLS; SUPEROXIDE DISMUTASE 1;

ANTIGEN-ANTIBODY REACTIONS; BLOOD; CELL MEMBRANES; HEMOGLOBIN OXYGEN SATURATION; LIVER; METABOLISM; OXYGEN; PHYSIOLOGY; ZINC;

MACROPHAGES;

COPPER ZINC SUPEROXIDE DISMUTASE; FERROPORTIN; HEME OXYGENASE 1; HEPCIDIN; IRON; MESSENGER RNA;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME DEFICIENCY; ERYTHROPHAGOCYTOSIS; ERYTHROPOIESIS; GENE EXPRESSION REGULATION; HEMOLYSIS; HEMOLYTIC ANEMIA; IRON BALANCE; IRON BLOOD LEVEL; IRON METABOLISM DISORDER; KNOCKOUT MOUSE; KUPFFER CELL; LIVER METABOLISM; LIVER PARENCHYMA; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AGING; ANEMIA, HEMOLYTIC; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BLOTTING, WESTERN; CATION TRANSPORT PROTEINS; ERYTHROCYTES; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HEME; HEME OXYGENASE-1; HEMOGLOBINS; HEMOLYSIS; IRON; LIVER; MALE; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SUPEROXIDE DISMUTASE;

MUS;

EID: 66949174343     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20082137     Document Type: Article

References (45)

1. Okado-Matsumoto, A. and Fridovich, I. (2001) Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu,Zn-SOD in mitochondria. J. Biol. Chem. 276, 38388-38393
2. Reaume, A. G., Elliott, J. L., Hoffman, E. K., Kowall, N. W., Ferrante, R. J., Siwek, D. F., Wilcox, H. M., Flood, D. G., Beal, M. F., Brown, Jr, R. H. et al. (1996) Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat. Genet. 13, 43-47
3. Matzuk, M. M., Dionne, L., Guo, Q., Kumar, T. R. and Lebowitz, R. M. (1998) Ovarian function in superoxide dismutase 1 and 2 knockout mice. Endocrinology 139, 4008-4011
4. Sentman, M. L., Granström, M., Jakobson, H., Reaume, A., Basu, S. and Marklund, S. L. (2006) Phenotypes of mice lacking extracellular superoxide dismutase and copper- and zinc-containing superoxide dismutase. J. Biol. Chem. 281, 6904-6909
5. Rattan, S. I. (2006) Theories of biological aging: genes, proteins, and free radicals. Free Radical Res. 40, 1230-1238
6. Elchuri, S., Oberley, T. D., Qi, W., Eisenstein, R. S., Jackson Roberts, L., Van Remmen, H., Epstein, C. J. and Huang, T. T. (2005) CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 24, 367-380
7. Keithley, E. M., Canto, C., Zheng, Q. Y., Wang, X., Fischel-Ghodsian, N. and Johnson, K. R. (2005) Cu/Zn superoxide dismutase and age-related hearing loss. Hear. Res. 209, 76-85
8. Muller, F. L., Song, W., Liu, Y., Chaudhuri, A., Pieke-Dahl, S., Strong, R., Huang, T. T., Epstein, C. J., Roberts, 2nd, L. J., Csete, M. et al. (2006) Absence of CuZn superoxide dismutase leads to elevated oxidative stress and acceleration of age-dependent skeletal muscle atrophy. Free Radical Biol. Med. 40, 1993-2004
9. Baumbach, G. L., Didion, S. P. and Faraci, F. M. (2006) Hypertrophy of cerebral arterioles in mice deficient in expression of the gene for CuZn superoxide dismutase. Stroke 37, 1850-1855
10. Iuchi, Y., Okada, F., Onuma, K., Onoda, T., Asao, H., Kobayashi, M. and Fuji, J. (2007) Elevated oxidative stress in erythrocytes due to an SOD1 deficiency causes and triggers autoantibody production. Biochem. J. 402, 219-227
11. Hadjur, S., Ung, K., Wadsworth, L., Dimmick, J., Rajcan-Separovic, E., Scott, R. W., Buchwald, M. and Jirik, F. R. (2001) Defective hematopoiesis and hepatic steatosis in mice with combined deficiencies of the genes encoding Fancc and Cu/Zn superoxide dismutase. Blood 98, 10003-10011
12. Starzyłski, R. R., Lipiłski, P., Drapier, J-C., Diet, A., Smuda, E., Bartłomiejczyk, T., Gralak, M. A. and Kruszewski, M. (2005) Down-regulation of iron regulatory protein 1 activities and expression in superoxide dismutase 1 knock-out mice is not associated with alterations in iron metabolism. J. Biol. Chem. 280, 4207-4212
13. Canonne-Hergaux, F., Donovan, A., Delaby, C., Wang, H. J. and Gros, P. (2006) Comparative studies of duodenal and macrophage ferroportin proteins. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G156-G163
14. Torrance, J. D. and Bothwell, T. H. (1980) Iron stores. Methods Hematol. 1, 90-115
15. Delaby, C., Pilard, N., Hetet, G., Driss, F., Grandchamp, B., Beaumont, C. and Canonne-Hergaux, F. (2005) A physiological model to study iron recycling in macrophages. Exp. Cell Res. 310, 43-53
16. Motterlini, R., Foresti, R., Vandegriff, K., Intaglietta, M. and Winslow, R. M. (1995) Oxidative-stress response in vascular endothelial cells exposed to a cellular hemoglobin solutions. Am. J. Physiol. 269, H648-H655
17. Ascenzi, P., Bocedi, A., Visca, P., Altruda, F., Tolosano, E., Beringhelli, T. and Fasano, M. (2005) Hemoglobin and heme scavenging. IUBMB Life 57, 749-759
18. Kristiansen, M., Graversen, J. H., Jacobsen, C., Sonne, O., Hoffman, H. J., Law, S. K. A. and Moestrup, S. K. (2001) Identification of the hemoglobin receptor. Nature 409, 198-201
19. Hvidberg, V., Maniecki, M. B., Jacobsen, C., Højrup, P., Møller, H. J. and Moestrup, S. K. (2005) Identification of the receptor scavenging hemopexin-heme complexes. Blood 106, 2572-2579
20. Madsen, M., Møller, H. J., Nielsen, M. J., Jacobsen, C., Graversen, J. H,, van den Berg, T. and Moestrup, S. K. (2004) Molecular characterization of the haptoglobin/hemoglobin receptor CD163. Ligand binding properties of the scavenger receptor cysteine-rich domain region. J. Biol. Chem. 279, 51561-51567
21. Dhaliwal, G., Cornett, P. A. and Tierney, Jr, L. M. (2004) Hemolytic anemia. Am. Fam. Physician 69, 2599-2606
22. De Domenico, I., Ward, D. M., Langelier, C., Vaughn, M. B., Nemeth, E., Sundquist, W. I., Ganz, T., Musci, G. and Kaplan, J. (2007) The molecular mechanism of hepcidin-mediated ferroportin down-regulation. Mol. Biol. Cell 18, 2569-2578
23. Kumar, S. and Bandyopadhyay, U. (2005) Free heme toxicity and its detoxification systems in human. Toxicol. Lett. 157, 175-188
24. Delanghe, J. R. and Langlois, M. R. (2001) Hemopexin: a review of biological aspects and the role in laboratory medicine. Clin. Chim. Acta 312, 13-23
25. Bratosin, D., Mazurier, J., Tissier, J. P., Estaquier, J., Huart, J. J., Ameisen, J. C., Aminoff, D. and Montreuil, J. (1998) Cellular and molecular mechanisms of senescent erythrocyte phagocytosis by macrophages. Biochimie 80, 173-195
26. Maines, M. D. (2005) The heme oxygenase system: update 2005. Antioxid. Redox Signalling 7, 1761-1766
27. Immenschuh, S., Shan, Y., Kroll, H., Santoso, S., Wossmann, W., Bein, G. and Bonkovsky, H. L. (2007) Marked hyperbilirubinemia associated with the heme oxygenase-1 gene promoter microsatellite polymorphism in a boy with autoimmune hemolytic anemia. Pediatrics 119, e764-e767
28. Tolosano, E., Fagoonee, S., Hirsch, E., Berger, F. G., Baumann, H., Silengo, L. and Altruda, F. (2002) Enhanced splenomegaly and severe liver inflammation in haptoglobin/hemopexin double-null mice after acute hemolysis. Blood 100, 4201-4208
29. Poss, K. D. and Tonegawa, S. (1997) Heme oxygenase 1 is required for mammalian iron utilization. Proc. Natl. Acad. Sci U.S.A. 94, 10919-10924
30. Yachie, A., Niida, Y., Wada, T., Igarashi, N., Kaneda, H., Toma, T., Ohta, K., Kasahara, Y. and Koizumi, S. (1999) Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J. Clin. Invest. 103, 129-135
31. Khan, Z. A., Barbin, Y. P., Cukiernik, M., Adams, P. C. and Chakrabarti, S. (2004) Heme-oxygenase-mediated iron accumulation in the liver. Can. J. Physiol. Pharmacol. 82, 448-456
32. Abboud, S. and Haile, D. J. (2000) A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J. Biol. Chem. 275, 19906-19912
33. McKie, A. T., Marciani, P., Rolfs, A., Brennan, K., Wehr, K., Barrow, D., Miret, S., Bomford, A., Peters, T. J., Farzaneh, F. et al. (2000) A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol. Cell 5, 299-309
34. Donovan, A., Brownlie, A., Zhou, Y., Shepard, J., Pratt, S. J., Moynihan, J., Paw, B. H., Drejer, A., Barut, B., Zapata, A. et al. (2000) Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature 403, 776-781
35. Vokurka, M., Krijt, J., Sulc, K. and Necas, E. (2006) Hepcidin mRNA levels in mouse liver respond to inhibition of erythropoiesis. Physiol. Res. 55, 667-674
36. Canonne-Hergaux, F., Zhang, A. S., Ponka, P. and Gros, P. (2001) Characterization of the iron transporter DMT1 (NRAMP2/DCT1) in red blood cells of normal and anemic mk/mk mice. Blood 98, 3823-3830
37. Knutson, M. D., Vafa, M,R., Haile, D. J. and Wessling-Resnick, M. (2003) Iron loading and erythrophagocytosis increase ferroportin 1 (FPN1) expression in J774 macrophages. Blood 102, 4191-4197
38. Delaby, C., Pilard, N., Gonçalves, A. S., Beaumont, C. and Canonne-Hergaux, F. (2005) Presence of the exporter ferroportin at the plasma membrane of macrophages is enhanced by iron loading and down-regulated by hepcidin. Blood 106, 3979-3984
39. Viatte, L., Lesbordes-Brion, J. C., Lou, D. Q., Bennoun, M., Nicolas, G., Kahn, A., Canonne-Hergaux, F. and Vaulont, S. (2005) Deregulation of proteins involved in iron metabolism in hepcidin-deficient mice. Blood 105, 4861-4864
40. Peyssonnaux, C., Zinkernagel, A. S., Schuepbach, R. A., Rankin, E., Vaulont, S., Haase, V. H., Nizet, V. and Johnson, R. S. (2007) Regulation of iron homeostasis by the hypoxia-inducible transcription factors (HIFs). J. Clin. Invest. 117, 1926-1932
41. Knutson, M. D., Oukka, M., Koss, L. M., Aydemir, F. and Wessling-Resnick, M. (2005) Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and down-regulated by hepcidin. Proc. Natl. Acad. Sci. U.S.A. 102, 1324-1328
42. Doolittle, R. L. and Richter, G. W. (1981) Isoferritins in rat Kupffer cells, hepatocytes, and extrahepatic macrophages. Biosynthesis in cell suspensions and cultures in response to iron. Lab. Invest. 45, 567-574
43. Tran, T. N., Eubanks, S. K., Schaffer, K. J., Zhou, C. Y. J. and Linder, M. C. (1997) Secretion of ferritin by rat hepatoma cells and its regulation by inflammatory cytokines and iron. Blood 12, 4979-4986
44. Zhang, A. S., Xiong, S., Tsukamoto, H. and Enns, C. A. (2004) Localization of iron metabolism-related mRNAs in rat liver indicate that HFE is expressed predominantly in hepatocytes. Blood 103, 1509-1514
45. Nicolas, G., Bennoun, M., Devaux, I., Beaumont, C., Grandchamp, B., Kahn, A. and Vaulont, S. (2001) Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proc. Natl. Acad. Sci. U.S.A. 98, 8780-8785