Erythropoietin Contrastingly Affects Bacterial Infection and Experimental Colitis by Inhibiting Nuclear Factor-κB-Inducible Immune Pathways

Immunity

Volumn 34, Issue 1, 2011, Pages 61-74

  Nairz, Manfred ^a   Schroll, Andrea ^a   Moschen, Alexander R ^a   Sonnweber, Thomas ^a   Theurl, Milan ^a   Theurl, Igor ^a   Taub, Nicole ^a   Jamnig, Christina ^a   Neurauter, Daniela ^a   Huber, Lukas A ^a   Tilg, Herbert ^a   Moser, Patrizia L ^b   Weiss, Günter ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b MEDICAL UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; RECOMBINANT ERYTHROPOIETIN; TRANSCRIPTION FACTOR RELA; TRANSFERRIN RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; COLITIS; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; EXPERIMENTAL INFECTION; GENE EXPRESSION; IMMUNOMODULATION; MACROPHAGE ACTIVATION; MALE; MEDIATOR RELEASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SURVIVAL; TISSUE INJURY;

ANIMALS; CELL LINE; COLITIS; DEXTRAN SULFATE; ERYTHROPOIETIN; HUMANS; INFLAMMATION MEDIATORS; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; NITRIC OXIDE; RECEPTORS, ERYTHROPOIETIN; SALMONELLA; SALMONELLA INFECTIONS; SIGNAL TRANSDUCTION; TRINITROBENZENESULFONIC ACID; TUMOR NECROSIS FACTOR-ALPHA;

EID: 78751698162     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2011.01.002     Document Type: Article

References (48)

1. Adembri C., Massagrande A., Tani A., Miranda M., Margheri M., De Gaudio R., Pellegrini-Giampietro D.E. Carbamylated erythropoietin is neuroprotective in an experimental model of traumatic brain injury. Crit. Care Med. 2008, 36:975-978.
2. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
3. Aoshiba K., Onizawa S., Tsuji T., Nagai A. Therapeutic effects of erythropoietin in murine models of endotoxin shock. Crit. Care Med. 2009, 37:889-898.
4. Asquith M.J., Boulard O., Powrie F., Maloy K.J. Pathogenic and protective roles of MyD88 in leukocytes and epithelial cells in mouse models of inflammatory bowel disease. Gastroenterology 2010, 139:519-529. 529, e1-e2.
5. Bohlius J., Schmidlin K., Brillant C., Schwarzer G., Trelle S., Seidenfeld J., Zwahlen M., Clarke M., Weingart O., Kluge S., et al. Recombinant human erythropoiesis-stimulating agents and mortality in patients with cancer: a meta-analysis of randomised trials. Lancet 2009, 373:1532-1542.
6. Bouma G., Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 2003, 3:521-533.
7. Brines M., Cerami A. Emerging biological roles for erythropoietin in the nervous system. Nat. Rev. Neurosci. 2005, 6:484-494.
8. Brines M., Grasso G., Fiordaliso F., Sfacteria A., Ghezzi P., Fratelli M., Latini R., Xie Q.W., Smart J., Su-Rick C.J., et al. Erythropoietin mediates tissue protection through an erythropoietin and common beta-subunit heteroreceptor. Proc. Natl. Acad. Sci. USA 2004, 101:14907-14912.
9. Bunn H.F. New agents that stimulate erythropoiesis. Blood 2007, 109:868-873.
10. Carvalho G., Lefaucheur C., Cherbonnier C., Métivier D., Chapel A., Pallardy M., Bourgeade M.F., Charpentier B., Hirsch F., Kroemer G. Chemosensitization by erythropoietin through inhibition of the NF-kappaB rescue pathway. Oncogene 2005, 24:737-745.
11. Chen J., Connor K.M., Aderman C.M., Smith L.E. Erythropoietin deficiency decreases vascular stability in mice. J. Clin. Invest. 2008, 118:526-533.
12. Corwin H.L., Gettinger A., Fabian T.C., May A., Pearl R.G., Heard S., An R., Bowers P.J., Burton P., Klausner M.A., Corwin M.J. Efficacy and safety of epoetin alfa in critically ill patients. N. Engl. J. Med. 2007, 357:965-976. EPO Critical Care Trials Group.
13. De Maria R., Testa U., Luchetti L., Zeuner A., Stassi G., Pelosi E., Riccioni R., Felli N., Samoggia P., Peschle C. Apoptotic role of Fas/Fas ligand system in the regulation of erythropoiesis. Blood 1999, 93:796-803.
14. Digicaylioglu M., Lipton S.A. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature 2001, 412:641-647.
15. Ehrenreich H., Hasselblatt M., Dembowski C., Cepek L., Lewczuk P., Stiefel M., Rustenbeck H.H., Breiter N., Jacob S., Knerlich F., et al. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol. Med. 2002, 8:495-505.
16. Erbayraktar S., de Lanerolle N., de Lotbinière A., Knisely J.P., Erbayraktar Z., Yilmaz O., Cerami A., Coleman T.R., Brines M. Carbamylated erythropoietin reduces radiosurgically-induced brain injury. Mol. Med. 2006, 12:74-80.
17. Greten F.R., Eckmann L., Greten T.F., Park J.M., Li Z.W., Egan L.J., Kagnoff M.F., Karin M. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004, 118:285-296.
18. Imamura R., Isaka Y., Ichimaru N., Takahara S., Okuyama A. Carbamylated erythropoietin protects the kidneys from ischemia-reperfusion injury without stimulating erythropoiesis. Biochem. Biophys. Res. Commun. 2007, 353:786-792.
19. Jelkmann W. Erythropoietin after a century of research: Younger than ever. Eur. J. Haematol. 2007, 78:183-205.
20. Junk A.K., Mammis A., Savitz S.I., Singh M., Roth S., Malhotra S., Rosenbaum P.S., Cerami A., Brines M., Rosenbaum D.M. Erythropoietin administration protects retinal neurons from acute ischemia-reperfusion injury. Proc. Natl. Acad. Sci. USA 2002, 99:10659-10664.
21. Kaltwasser J.P., Kessler U., Gottschalk R., Stucki G., Möller B. Effect of recombinant human erythropoietin and intravenous iron on anemia and disease activity in rheumatoid arthritis. J. Rheumatol. 2001, 28:2430-2436.
22. Karin M., Ben-Neriah Y. Phosphorylation meets ubiquitination: The control of NF-[kappa]B activity. Annu. Rev. Immunol. 2000, 18:621-663.
23. Karin M., Delhase M. The I kappa B kinase (IKK) and NF-kappa B: Key elements of proinflammatory signalling. Semin. Immunol. 2000, 12:85-98.
24. Kaser A., Zeissig S., Blumberg R.S. Inflammatory bowel disease. Annu. Rev. Immunol. 2010, 28:573-621.
25. Lawrance I.C., Wu F., Leite A.Z., Willis J., West G.A., Fiocchi C., Chakravarti S. A murine model of chronic inflammation-induced intestinal fibrosis down-regulated by antisense NF-kappa B. Gastroenterology 2003, 125:1750-1761.
26. Leist M., Ghezzi P., Grasso G., Bianchi R., Villa P., Fratelli M., Savino C., Bianchi M., Nielsen J., Gerwien J., et al. Derivatives of erythropoietin that are tissue protective but not erythropoietic. Science 2004, 305:239-242.
27. Liu Y., Pop R., Sadegh C., Brugnara C., Haase V.H., Socolovsky M. Suppression of Fas-FasL coexpression by erythropoietin mediates erythroblast expansion during the erythropoietic stress response in vivo. Blood 2006, 108:123-133.
28. Ludwig H., Crawford J., Osterborg A., Vansteenkiste J., Henry D.H., Fleishman A., Bridges K., Glaspy J.A. Pooled analysis of individual patient-level data from all randomized, double-blind, placebo-controlled trials of darbepoetin alfa in the treatment of patients with chemotherapy-induced anemia. J. Clin. Oncol. 2009, 27:2838-2847.
29. Mastroeni P., Vazquez-Torres A., Fang F.C., Xu Y., Khan S., Hormaeche C.E., Dougan G. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo. J. Exp. Med. 2000, 192:237-248.
30. Nairz M., Fritsche G., Crouch M.L., Barton H.C., Fang F.C., Weiss G. Slc11a1 limits intracellular growth of Salmonella enterica sv. Typhimurium by promoting macrophage immune effector functions and impairing bacterial iron acquisition. Cell. Microbiol. 2009, 11:1365-1381.
31. Nairz M., Theurl I., Schroll A., Theurl M., Fritsche G., Lindner E., Seifert M., Crouch M.L., Hantke K., Akira S., et al. Absence of functional Hfe protects mice from invasive Salmonella enterica serovar Typhimurium infection via induction of lipocalin-2. Blood 2009, 114:3642-3651.
32. Neubauer H., Cumano A., Müller M., Wu H., Huffstadt U., Pfeffer K. Jak2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis. Cell 1998, 93:397-409.
33. Neurath M.F., Pettersson S., Meyer zum Büschenfelde K.H., Strober W. Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-kappa B abrogates established experimental colitis in mice. Nat. Med. 1996, 2:998-1004.
34. Parganas E., Wang D., Stravopodis D., Topham D.J., Marine J.C., Teglund S., Vanin E.F., Bodner S., Colamonici O.R., van Deursen J.M., et al. Jak2 is essential for signaling through a variety of cytokine receptors. Cell 1998, 93:385-395.
35. Parsa C.J., Matsumoto A., Kim J., Riel R.U., Pascal L.S., Walton G.B., Thompson R.B., Petrofski J.A., Annex B.H., Stamler J.S., Koch W.J. A novel protective effect of erythropoietin in the infarcted heart. J. Clin. Invest. 2003, 112:999-1007.
36. Pasparakis M. Regulation of tissue homeostasis by NF-kappaB signalling: implications for inflammatory diseases. Nat. Rev. Immunol. 2009, 9:778-788.
37. Pfeffer M.A., Burdmann E.A., Chen C.Y., Cooper M.E., de Zeeuw D., Eckardt K.U., Feyzi J.M., Ivanovich P., Kewalramani R., Levey A.S., et al. A trial of darbepoetin alfa in type 2 diabetes and chronic kidney disease. N. Engl. J. Med. 2009, 361:2019-2032. TREAT Investigators.
38. Schaible U.E., Kaufmann S.H. Iron and microbial infection. Nat. Rev. Microbiol. 2004, 2:946-953.
39. Sepodes B., Maio R., Pinto R., Sharples E., Oliveira P., McDonald M., Yaqoob M., Thiemermann C., Mota-Filipe H. Recombinant human erythropoietin protects the liver from hepatic ischemia-reperfusion injury in the rat. Transpl. Int. 2006, 19:919-926.
40. Sirén A.L., Fratelli M., Brines M., Goemans C., Casagrande S., Lewczuk P., Keenan S., Gleiter C., Pasquali C., Capobianco A., et al. Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc. Natl. Acad. Sci. USA 2001, 98:4044-4049.
41. Suzuki N., Ohneda O., Takahashi S., Higuchi M., Mukai H.Y., Nakahata T., Imagawa S., Yamamoto M. Erythroid-specific expression of the erythropoietin receptor rescued its null mutant mice from lethality. Blood 2002, 100:2279-2288.
42. Theurl I., Mattle V., Seifert M., Mariani M., Marth C., Weiss G. Dysregulated monocyte iron homeostasis and erythropoietin formation in patients with anemia of chronic disease. Blood 2006, 107:4142-4148.
43. Valdez Y., Ferreira R.B., Finlay B.B. Molecular mechanisms of Salmonella virulence and host resistance. Curr. Top. Microbiol. Immunol. 2009, 337:93-127.
44. Weiss G., Goodnough L.T. Anemia of chronic disease. N. Engl. J. Med. 2005, 352:1011-1023.
45. Weiss G., Werner-Felmayer G., Werner E.R., Grünewald K., Wachter H., Hentze M.W. Iron regulates nitric oxide synthase activity by controlling nuclear transcription. J. Exp. Med. 1994, 180:969-976.
46. Weiss G., Houston T., Kastner S., Jöhrer K., Grünewald K., Brock J.H. Regulation of cellular iron metabolism by erythropoietin: Activation of iron-regulatory protein and upregulation of transferrin receptor expression in erythroid cells. Blood 1997, 89:680-687.
47. Zhang Y.L., Radhakrishnan M.L., Lu X., Gross A.W., Tidor B., Lodish H.F. Symmetric signaling by an asymmetric 1 erythropoietin: 2 erythropoietin receptor complex. Mol. Cell 2009, 33:266-274.
48. Zhu B.M., McLaughlin S.K., Na R., Liu J., Cui Y., Martin C., Kimura A., Robinson G.W., Andrews N.C., Hennighausen L. Hematopoietic-specific Stat5-null mice display microcytic hypochromic anemia associated with reduced transferrin receptor gene expression. Blood 2008, 112:2071-2080.