New approaches to treatment of anemia of chronic disease
Keywords:
anemia of chronic disease, hepcidin, erythroferrone, Gs-heparins
Abstract
Anemia of chronic disease is often associated with multiple chronic infectious diseases (infectious endocarditis, osteomyelitis, tuberculosis), cancer, rheumatic diseases (rheumatoid arthritis, systemic lupus erythematosus, vasculitis), and chronic renal failure. The pathogenesis of this anemia is rather complex, diverse, and poorly understood. Hepcidin is an important peptide that regulates iron absorption in the intestine. Many upstream and downstream signaling pathways regulate expression of hepcidin. A genetic defect in one of them may lead to deficiency, excess or redistribution of iron in the body. Timely detection and correction of anemia can improve the quality of life and survival of patients. Modern methods for correction of anemia of chronic disease are usually limited to the uncontrolled use of iron supplements. The recombinant erythropoietin treatment is most commonly used in patients with chronic renal failure. These therapeutic tactics are usually explained by depression of erythropoietin synthesis by proinflammatory cytokines. Currently, a number of drugs is being developed, which inhibit hepcidin synthesis directly or indirectly by regulating expression of hepcidin inhibitors and stimulators. Some drugs have already been approved for clinical use and can be successfully used for treatment of anemia. In this review, we presented a new, pathogenetically well-grounded approach to the treatment of anemia of chronic disease.
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References
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26. Andriopoulos B., Corradini E., Xia Y., Faasse S.A., Chen S., Grgurevic L. et al. BMP6 is a key endogenous regulator of hepcidin expression and iron metabolism. Nature Genetics. 2009; 41(4): 482-7.
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28. Pak M., Lopez M.A., Gabayan V., Ganz T., Rivera S. Suppression of hepcidin during anemia requires erythropoietic activity. Blood. 2006; 108(12): 3730-5.
29. Tanno T., Bhanu N.V., Oneal P.A. et al. High levels of GDF15 in thalassemia suppress expression of the iron regulatory protein hepcidin. Nature Medicine. 2007; 13(9): 1096-101.
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33. Poli M., Asperti M., Naggi A., Campostrini N., Girelli D., Corbella M. et al. Glycol-split nonanticoagulant heparins are inhibitors of hepcidin expression in vitro and in vivo. Blood. 2014; 123(10): 1564-73.
34. Ritchie J.P., Ramani V.C., Ren Y., Naggi A., Torri G., Casu B. et al. SST0001, a chemically modified heparin, inhibits myeloma growth and angiogenesis via disruption of the heparanase/syndecan-1 axis. Clinical Cancer Research. 2011; 17(6): 1382-93.
35. Naggi A., Casu B., Perez M., Torri G., Cassinelli G., Penco S. et al. Modulation of the heparanase-inhibiting activity of heparin through selective desulfation, graded N-acetylation, and glycol splitting. The Journal of Biological Chemistry. 2005; 280(13): 12103-13.
36. Silvestri L., Pagani A. Camaschella C. Furin-mediated release of soluble hemojuvelin: a new link between hypoxia and iron homeostasis. Blood. 2008; 111(2): 924-31.
37. Steinbicker A.U., Sachidanandan C., Vonner A.J., Yusuf R.Z., Deng D.Y., Lai C.S. et al. Inhibition of bone morphogenetic protein signaling attenuates anemia associated with inflammation. Blood. 2011; 117(18): 4915-23.
38. Peterson P.W. Targeting cancer-induced anemia with hepcidin lowering ALK2 inhibitors. Clinical Cancer Researsh. 2015; 75(15): 3647.
39. Boser P., Seemann D., Liguori M.J., Fan L., Huang L., Hafner M. et al. Anti-repulsive guidance molecule C (RGMc) antibodies increases serum iron in rats and cynomolgus monkeys by hepcidindownregulation. The AAPS Journal. 2015; 17(4): 930-8.
40. Akinc A., Chan-Daniels A., Sehgal A. Targeting the hepcidin pathway with RNAi therapeutics for the treatment of anemia. Blood. 2011; 118(21): 315.
41. Nair J.K, Willoughby J.L., Chan A., Charisse K., Alam M.R., Wang Q. et al. Multivalent N-acetylgalactosamine-conjugated siRNA localizes in hepatocytes and elicits robust RNAi-mediated gene silencing. Journal of the American Chemical Society. 2014; 136(49): 16958-61.
42. Kurzrock R., Voorhees P.M., Casper C., Furman R.R., Fayad L., Lonial S. et al. A phase I, open-label study of siltuximab, an anti-IL-6 monoclonal antibody, in patients with B-cell non-Hodgkin lymphoma, multiple myeloma, or Castleman disease. Clinical Cancer Research. 2013; 19(13): 3659-70.
43. Casper C., Chaturvedi S., Munshi N., Wong R., Qi M., Schaffer M. et al. Analysis of inflammatory and anemia-related biomarkers in a randomized, double-blind, placebo-controlled study of siltuximab (anti-IL6 monoclonal antibody) in patients with multicentriccastleman disease. Clinical Cancer Research. 2015; 21(19): 4294-304.
44. Angevin E., Tabernero J., Elez E, Cohen S.J., Bahleda R., van Laethem J.L. et al. A phase I/II, multipledose, dose-escalation study of siltuximab, an anti-interleukin- 6 monoclonal antibody, in patients with advanced solid tumors. Clinical Cancer Research. 2014; 20(8): 2192-204.
45. Schipperus M., Rijnbeek B., Reddy M., Qin X., Cornfield M.J. CNTO328 (anti- IL-6 mAb) treatment is associated with an increase inhemoglobin (Hb) and decrease in hepcidin levels in renal cell carcinoma (RCC). Blood. 2009; 114(22): 4045.
46. Song S.N., Tomosugi N., Kawabata H., Ishikawa T., Nishikawa T., Yoshizaki K. et al. Down-regulation of hepcidin resulting from long-term treatment with an anti-IL-6 receptor antibody (tocilizumab) improves anemia of inflammation in multicentric Castleman disease. Blood. 2010; 116(18): 3627-34.
47. Song S.N., Iwahashi M., Tomosugi N., Uno K., Yamana J., Yamana S. et al. Comparative evaluation of the effects of treatment with tocilizumab and TNF-alpha inhibitors on serum hepcidin, anemia response and disease activity in rheumatoid arthritis patients. Arthritis Research and Therapy. 2013; 15(5): 141.
48. Isaacs J.D., Harari O., Kobold U., Lee J.S., Bernasconi C. et al. Effect of tocilizumab on haematological markers implicates interleukin-6 signalling in the anaemia of rheumatoid arthritis. Arthritis Research and Therapy. 2013; 15(6): 204.
49. De Vos J., Jourdan M., Tarte K., Jasmin C., Klein B. JAK2 tyrosine kinase inhibitor tyrphostin AG490 downregulates the mitogenactivated protein kinase (MAPK) and signal transducer and activator of transcription (STAT) pathways and induces apoptosis in myeloma cells. British Journal of Haemotology. .2000; 109(4): 823-8.
50. Fatih N., Camberlein E., Island M.L., Corlu A., Abgueguen E., Dеtivaud L. et al. Natural and synthetic STAT3 inhibitors reduce hepcidin expression in differentiated mouse hepatocytes expressing the active phosphorylated STAT3 form. Journal of Molecular Medicine. 2010; 88(5): 477-86.
51. McMurray J.S., Mandal P.K., Liao W.S., Klostergaard J., Robertson F.M. The consequences of selective inhibition of signal transducer and activator of transcription 3 (STAT3) tyrosine705 phosphorylation by phosphopeptide mimetic prodrugs targeting the Src. homology 2 (SH2) domain. Jakstat. 2012; 1(4): 263-347.
52. Groopman J.E., Itri L.M. Chemotherapy-induced anemia in adults: incidence and treatment. Journal of the National Cancer Institute. 1999; 91(19): 1616-34.
53. Georgiev P., Lazaroiu M., Ocroteala L., Grudeva-Popova J., Gheorghita E., Vasilica M. et al. The anti-hepcidinSpiegelmer® LexaptepidPegol (NOX-H94) as treatment of anemia of chronic disease in patients with multiple myeloma, low grade lymphoma, and CLL: a phase II pilot study. Cancer Research. 2014; 74 (19): 3847.
54. Cooke K.S., Hinkle B., Salimi-Moosavi H., Foltz I., King C. A fully human anti-hepcidin antibody modulates iron metabolism in both mice and nonhuman primates. Blood. 2013; 122(17): 3054-61.
2. Melnikova I. Anaemia therapies. Nature Reviews Drug Discovery. 2006; 5(8): 627-8.
3. McClellan W., Aronoff S.L., Bolton W.K. The prevalence of anaemia in patients with chronic kidney disease. Current Medical Research and Opinion. 2004; 20: 1501-10.
4. Meyer T.E. Anemia in heart failure. Current Cardiology Reports. 2003; 5(3): 213-14.
5. Saravana S., Rai А. Anemia of chronic disease in patients with rheumatoid arthritis-use of zinc protoporphyrin (ZPP) levels. The Journal of Rheumatology. 2007; 34(2): 446.
6. Giannouli S., Voulgarelis М., Ziakas P.D., Tzioufas A.G. Anaemia in systemic lupus erythematosus: from pathophysiology to clinical assessment. Annals of the Rheumatic Diseases. 2006; 65(2): 144-8.
7. Ellegala D.B., Alden T.D. Couture Anemia, testosterone, and pituitary adenoma in men. Journal of Neurosurgurgery. 2003; 98(5): 974-7.
8. Thomas М.С., Tsalamandris С., Macisaac R. Functional erythropoietin deficiency in patients with Type 2 diabetes and anaemia. Diabetic Medicine. 2006; 23(5): 502-9.
9. Roy C.N. Anemia of inflammation. Hematology. American Society of Hematology. Education Program. 2010; 2010: 276-80.
10. Margetic S., Topic Е., Ruzic D.F. Soluble transferrin receptor and transferrin receptor-ferritin index in iron deficiency anemia and anemia in rheumatoid arthritis. Clinical Chemistry and Laboratory Medicine. 2005; 43(3): 326-31.
11. Fitzsimons E.J., Brock J.H. The anaemia of chronic disease: Remains hard to distinguish from iron deficiency anaemia in some cases. The BMJ. 2001; 322(7290): 811-12.
12. Arndt U., Kaltwasser J.P., Gottschalk R. Correction of iron-deficient erythropoiesis in the treatment of anemia of chronic disease with recombinant human erythropoietin. Annals of Hematology. 2005; 84(3): 159-66.
13. Ruiz-Arguelles G.J., Diaz-Hernandez А., Manzano С. Ineffectiveness of oral iron hydroxide polymaltose in iron-deficiency anemia. Hematology. 2007; 12(3): 255-6.
14. Reynoso-Gоmez Е., Salinas-Rojas V., Lazo-Langner А. Safety and efficacy of total dose intravenous iron infusion in the treatment of iron-deficiency anemia in adult non-pregnant patients. Revista De Investigacion Clinica. 2002; 54(1): 12-20.
15. Andrews P.A. Disorders of iron metabolism. New England Journal of Medicine. 2000; 342 (17): 1293.
16. Wally J., Halbrooks P.J., Vonrhein C, Rould M.A., Everse S.J., Mason A.B., Buchanan S.K. The crystal structure of iron-free human serum transferrin provides insight intointer-lobe communication and receptor binding. The Journal of Biological Chemistry. 2006; 281(34): 24934-44.
17. Cheng Y., Zak O., Aisen P., Harrison S.C., Walz T. Structure of the human transferrin receptor-transferrin complex. Cell. 2004; 116(4): 565-76.
18. Fleming M.D., Romano M.A., Su M.A., Garrick L.M., Garrick M.D., Andrews N.C. Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron F transport. Proceedings of the National Academy of Sciences. USA. 1998; 95(3): 1148-53.
19. Torti F.M., Torti S.V. Regulation of ferritin genes and protein. Blood. 2002; 99(10): 3505-16. ISSN 0031-2991
20. Hentze M.W., Muckenthaler M.U., Andrews N.C. Balancing acts: molecular control of mammalian iron metabolism. Cell. 2004; 117(3): 285-97.
21. Ludwiczek S., Aigner E., Theurl I., Weiss G. Cytokine-mediatedregulation of iron transport in human monocytic cells. Blood. 2003; 101(10): 4148-54.
22. Sakamori R., Takehara T., Tatsumi T., Shigekawa M., Hikita H., Hiramatsu N., Kanto T., Hayashi N. STAT3 signaling withinhepatocytes is required for anemia of inflammation in vivo. Journal of Gastroenterology. 2010; 45(2): 244-8.
23. Mayeur C., Lohmeyer L.K., Leyton P., Kao S.M., Pappas A.E., Kolodziej S.A. et al. The type I BMP receptorAlk3 is required for the induction of hepatic hepcidin gene expressionby interleukin-6. Blood. 2014; 123(14): 2261-8.
24. Theurl I., Schroll A., Sonnweber T., Nairz M., Theurl M., Willenbacher W. et al. Pharmacologic inhibition of hepcidin expression reverses anemia of chronic inflammation in rats. Blood. 2011; 118(18): 4977-84.
25. Nicolas G., Bennoun M., Devaux I., ., Grandchamp B., Kahn A. et al. Lack of hepcidin geneexpression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proceedings of the National Academy of Sciences. USA. 2001; 98(15): 8780-5.
26. Andriopoulos B., Corradini E., Xia Y., Faasse S.A., Chen S., Grgurevic L. et al. BMP6 is a key endogenous regulator of hepcidin expression and iron metabolism. Nature Genetics. 2009; 41(4): 482-7.
27. Babitt J.L., Huang F.W., Wrighting D.M., Xia Y., Sidis Y., Samad T.A. et al. Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nature Genetics. 2006; 38(5): 531-9.
28. Pak M., Lopez M.A., Gabayan V., Ganz T., Rivera S. Suppression of hepcidin during anemia requires erythropoietic activity. Blood. 2006; 108(12): 3730-5.
29. Tanno T., Bhanu N.V., Oneal P.A. et al. High levels of GDF15 in thalassemia suppress expression of the iron regulatory protein hepcidin. Nature Medicine. 2007; 13(9): 1096-101.
30. Tanno T., Porayette P., Sripichai O. et al. Identification of TWSG1 as a second novel erythroid regulator of hepcidin expression in murinend human cells. Blood. 2009; 114(1): 181-6.
31. Kautz L., Jung G., Valore E.V., Rivella S., Nemeth E., Ganz T. Identification of erythroferrone as an erythroid regulator of iron metabolism. Nature Genetics. 2014; 46(7): 678-84.
32. Poli M., Girelli D., Campostrini N., Maccarinelli F., Finazzi D., Luscieti S. et al. Heparin: a potent inhibitor of hepcidin expression in vitro and in vivo. Blood. 2011; 117(3): 997-1004.
33. Poli M., Asperti M., Naggi A., Campostrini N., Girelli D., Corbella M. et al. Glycol-split nonanticoagulant heparins are inhibitors of hepcidin expression in vitro and in vivo. Blood. 2014; 123(10): 1564-73.
34. Ritchie J.P., Ramani V.C., Ren Y., Naggi A., Torri G., Casu B. et al. SST0001, a chemically modified heparin, inhibits myeloma growth and angiogenesis via disruption of the heparanase/syndecan-1 axis. Clinical Cancer Research. 2011; 17(6): 1382-93.
35. Naggi A., Casu B., Perez M., Torri G., Cassinelli G., Penco S. et al. Modulation of the heparanase-inhibiting activity of heparin through selective desulfation, graded N-acetylation, and glycol splitting. The Journal of Biological Chemistry. 2005; 280(13): 12103-13.
36. Silvestri L., Pagani A. Camaschella C. Furin-mediated release of soluble hemojuvelin: a new link between hypoxia and iron homeostasis. Blood. 2008; 111(2): 924-31.
37. Steinbicker A.U., Sachidanandan C., Vonner A.J., Yusuf R.Z., Deng D.Y., Lai C.S. et al. Inhibition of bone morphogenetic protein signaling attenuates anemia associated with inflammation. Blood. 2011; 117(18): 4915-23.
38. Peterson P.W. Targeting cancer-induced anemia with hepcidin lowering ALK2 inhibitors. Clinical Cancer Researsh. 2015; 75(15): 3647.
39. Boser P., Seemann D., Liguori M.J., Fan L., Huang L., Hafner M. et al. Anti-repulsive guidance molecule C (RGMc) antibodies increases serum iron in rats and cynomolgus monkeys by hepcidindownregulation. The AAPS Journal. 2015; 17(4): 930-8.
40. Akinc A., Chan-Daniels A., Sehgal A. Targeting the hepcidin pathway with RNAi therapeutics for the treatment of anemia. Blood. 2011; 118(21): 315.
41. Nair J.K, Willoughby J.L., Chan A., Charisse K., Alam M.R., Wang Q. et al. Multivalent N-acetylgalactosamine-conjugated siRNA localizes in hepatocytes and elicits robust RNAi-mediated gene silencing. Journal of the American Chemical Society. 2014; 136(49): 16958-61.
42. Kurzrock R., Voorhees P.M., Casper C., Furman R.R., Fayad L., Lonial S. et al. A phase I, open-label study of siltuximab, an anti-IL-6 monoclonal antibody, in patients with B-cell non-Hodgkin lymphoma, multiple myeloma, or Castleman disease. Clinical Cancer Research. 2013; 19(13): 3659-70.
43. Casper C., Chaturvedi S., Munshi N., Wong R., Qi M., Schaffer M. et al. Analysis of inflammatory and anemia-related biomarkers in a randomized, double-blind, placebo-controlled study of siltuximab (anti-IL6 monoclonal antibody) in patients with multicentriccastleman disease. Clinical Cancer Research. 2015; 21(19): 4294-304.
44. Angevin E., Tabernero J., Elez E, Cohen S.J., Bahleda R., van Laethem J.L. et al. A phase I/II, multipledose, dose-escalation study of siltuximab, an anti-interleukin- 6 monoclonal antibody, in patients with advanced solid tumors. Clinical Cancer Research. 2014; 20(8): 2192-204.
45. Schipperus M., Rijnbeek B., Reddy M., Qin X., Cornfield M.J. CNTO328 (anti- IL-6 mAb) treatment is associated with an increase inhemoglobin (Hb) and decrease in hepcidin levels in renal cell carcinoma (RCC). Blood. 2009; 114(22): 4045.
46. Song S.N., Tomosugi N., Kawabata H., Ishikawa T., Nishikawa T., Yoshizaki K. et al. Down-regulation of hepcidin resulting from long-term treatment with an anti-IL-6 receptor antibody (tocilizumab) improves anemia of inflammation in multicentric Castleman disease. Blood. 2010; 116(18): 3627-34.
47. Song S.N., Iwahashi M., Tomosugi N., Uno K., Yamana J., Yamana S. et al. Comparative evaluation of the effects of treatment with tocilizumab and TNF-alpha inhibitors on serum hepcidin, anemia response and disease activity in rheumatoid arthritis patients. Arthritis Research and Therapy. 2013; 15(5): 141.
48. Isaacs J.D., Harari O., Kobold U., Lee J.S., Bernasconi C. et al. Effect of tocilizumab on haematological markers implicates interleukin-6 signalling in the anaemia of rheumatoid arthritis. Arthritis Research and Therapy. 2013; 15(6): 204.
49. De Vos J., Jourdan M., Tarte K., Jasmin C., Klein B. JAK2 tyrosine kinase inhibitor tyrphostin AG490 downregulates the mitogenactivated protein kinase (MAPK) and signal transducer and activator of transcription (STAT) pathways and induces apoptosis in myeloma cells. British Journal of Haemotology. .2000; 109(4): 823-8.
50. Fatih N., Camberlein E., Island M.L., Corlu A., Abgueguen E., Dеtivaud L. et al. Natural and synthetic STAT3 inhibitors reduce hepcidin expression in differentiated mouse hepatocytes expressing the active phosphorylated STAT3 form. Journal of Molecular Medicine. 2010; 88(5): 477-86.
51. McMurray J.S., Mandal P.K., Liao W.S., Klostergaard J., Robertson F.M. The consequences of selective inhibition of signal transducer and activator of transcription 3 (STAT3) tyrosine705 phosphorylation by phosphopeptide mimetic prodrugs targeting the Src. homology 2 (SH2) domain. Jakstat. 2012; 1(4): 263-347.
52. Groopman J.E., Itri L.M. Chemotherapy-induced anemia in adults: incidence and treatment. Journal of the National Cancer Institute. 1999; 91(19): 1616-34.
53. Georgiev P., Lazaroiu M., Ocroteala L., Grudeva-Popova J., Gheorghita E., Vasilica M. et al. The anti-hepcidinSpiegelmer® LexaptepidPegol (NOX-H94) as treatment of anemia of chronic disease in patients with multiple myeloma, low grade lymphoma, and CLL: a phase II pilot study. Cancer Research. 2014; 74 (19): 3847.
54. Cooke K.S., Hinkle B., Salimi-Moosavi H., Foltz I., King C. A fully human anti-hepcidin antibody modulates iron metabolism in both mice and nonhuman primates. Blood. 2013; 122(17): 3054-61.
Published
2018-10-05
How to Cite
Budnevskiy A. V., Ovsyannikov E. S., Voronina E. V., Labzhaniya N. B., Zhusina Y. G. New approaches to treatment of anemia of chronic disease // Patologicheskaya Fiziologiya i Eksperimental’naya Terapiya (Pathological physiology and experimental therapy). 2018. VOL. 62. № 3. PP. 106–112.
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Section
Reviews
