Erythropoietin treatment leads to reduced blood glucose levels and body mass: Insights from murine models

Journal of Endocrinology

Volumn 205, Issue 1, 2010, Pages 87-95

  Katz, Odelia ^a   Stuible, Matthew ^b   Golishevski, Nathalia ^a   Lifshitz, Lilach ^a   Tremblay, Michel L ^b   Gassmann, Max ^c   Mittelman, Moshe ^a   Neumann, Drorit ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; HEMOGLOBIN A1C; PROTEIN TYROSINE PHOSPHATASE 1B; RECOMBINANT ERYTHROPOIETIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; BODY MASS; BODY WEIGHT; C57BL 6 MOUSE; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE PREDISPOSITION; EXPERIMENTAL MODEL; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; INJECTION; INTROSPECTION; MALE; METABOLIC DISORDER; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; TRANSGENIC MOUSE; WEIGHT GAIN;

ANIMALS; BLOOD GLUCOSE; BODY MASS INDEX; BODY WEIGHT; ERYTHROPOIETIN; FEMALE; HEMOGLOBIN A, GLYCOSYLATED; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, ANIMAL; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1;

EID: 77949523583     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1677/JOE-09-0425     Document Type: Article

References (68)

1. Allegra V, Mengozzi G, Martimbianco L & Vasile A 1996 Early and late effects of erythropoietin on glucose metabolism in maintenance hemodialysis patients. American Journal of Nephrology 16 304-308.
2. Allegra V, Martimbianco L & Vasile A 1997 Lipid and apolipoprotein patterns during erythropoietin therapy: roles of erythropoietin, route of administration, and diet. Nephrology, Dialysis, Transplantation 12 924-932.
3. Arcasoy MO 2008 The non-haematopoietic biological effects of erythropoietin. British Journal of Haematology 141 14-31.
4. Beleslin-Cokic BB, Cokic VP, Yu X, Weksler BB, Schechter AN & Noguchi CT 2004 Erythropoietin and hypoxia stimulate erythropoietin receptor and nitric oxide production by endothelial cells. Blood 104 2073-2080.
5. Bloomgarden ZT 2006 Glycemic treatment in type 1 and type 2 diabetes. Diabetes Care 29 2549-2555.
6. Bogdanova A, Mihov D, Lutz H, Saam B, Gassmann M & Vogel J 2007 Enhanced erythro-phagocytosis in polycythemic mice overexpressing erythropoietin. Blood 110 762-769.
7. Borissova AM, Djambazova A, Todorov K, Dakovska L, Tankova T & Kirilov G 1993 Effect of erythropoietin on the metabolic state and peripheral insulin sensitivity in diabetic patients on haemodialysis. Nephrology, Dialysis, Transplantation 8 93.
8. Boute N, Boubekeur S, Lacasa D & Issad T 2003 Dynamics of the interaction between the insulin receptor and protein tyrosine-phosphatase 1B in living cells. EMBO Reports 4 313-319.
9. Brines M, Grasso G, Fiordaliso F, Sfacteria A, Ghezzi P, Fratelli M, Latini R, Xie QW, Smart J, Su-Rick CJ et al. 2004 Erythropoietin mediates tissue protection through an erythropoietin and common beta-subunit heteroreceptor. PNAS 101 14907-14912.
10. Brown JN, Kemp DW& Brice KR 2009 Class effect of erythropoietin therapy on hemoglobin A(1c) in a patient with diabetes mellitus and chronic kidney disease not undergoing hemodialysis. Pharmacotherapy 29 468-472.
11. Callero MA, Perez GM, Vittori DC, Pregi N & Nesse AB 2007 Modulation of protein tyrosine phosphatase 1B by erythropoietin in UT-7 cell line. Cellular Physiology and Biochemistry 20 319-328.
12. Camici GG, Stallmach T, Hermann M, Hassink R, Doevendans P, Grenacher B, Hirschy A, Vogel J, Luscher TF, Ruschitzka F et al. 2007 Constitutively overexpressed erythropoietin reduces infarct size in a mouse model of permanent coronary artery ligation. Methods in Enzymology 435 147-155.
13. Cayla J, Lavoie C, Gareau R & Duvallet A 1999 Effects of recombinant erythropoietin (r-HuEPO) on plasma glucose concentration in endurance-trained rats. Acta Physiologica Scandinavica 166 247-249.
14. Chew GT, Gan SK & Watts GF 2006 Revisiting the metabolic syndrome. Medical Journal of Australia 185 445-449.
15. Chong ZZ, Shang YC & Maiese K 2007 Vascular injury during elevated glucose can be mitigated by erythropoietin and Wnt signaling. Current Neurovascular Research 4 194-204.
16. Cilloni D, Messa F, Carturan S, Arruga F, Defilippi I, Messa E, Gottardi E & Saglio G 2004 Myelodysplastic syndromes. Annals of the New York Academy of Sciences 1028 400-408.
17. Cohen J, Oren-Young L, Klingmuller U & Neumann D 2004 Protein tyrosine phosphatase 1B participates in the down-regulation of erythropoietin receptor signalling. Biochemical Journal 377 517-524.
18. Elchebly M, Payette P, Michaliszyn E, Cromlish W, Collins S, Loy AL, Normandin D, Cheng A, Himms-Hagen J, Chan CC et al. 1999 Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 283 1544-1548.
19. Eschbach JW, Kelly MR, Haley NR, Abels RI & Adamson JW 1989 Treatment of the anemia of progressive renal failure with recombinant human erythropoietin. New England Journal of Medicine 321 158-163.
20. Feldeisen SE & Tucker KL 2007 Nutritional strategies in the prevention and treatment of metabolic syndrome. Applied Physiology, Nutrition, and Metabolism 32 46-60.
21. Fenjves ES, Ochoa MS, Cabrera O, Mendez AJ, Kenyon NS, Inverardi L & Ricordi C 2003 Human, nonhuman primate, and rat pancreatic islets express erythropoietin receptors. Transplantation 75 1356-1360.
22. Fiordaliso F, Chimenti S, Staszewsky L, Bai A, Carlo E, Cuccovillo I, Doni M, Mengozzi M, Tonelli R, Ghezzi P et al. 2005 A nonerythropoietic derivative of erythropoietin protects the myocardium from ischemiareperfusion injury. PNAS 102 2046-2051.
23. Galeano M, Altavilla D, Cucinotta D, Russo GT, Calo M, Bitto A, Marini H, Marini R, Adamo EB, Seminara P et al. 2004 Recombinant human erythropoietin stimulates angiogenesis and wound healing in the genetically diabetic mouse. Diabetes 53 2509-2517.
24. Ghezzi P & Mengozzi M 2007 Activities of erythropoietin on tumors: an immunological perspective. European Journal of Immunology 37 1427-1430.
25. Giugliano D, Ceriello A & Esposito K 2008 Glucose metabolism and hyperglycemia. American Journal of Clinical Nutrition 87 217S-222S.
26. Hackett RH, Wang YD & Larner AC 1995 Mapping of the cytoplasmic domain of the human growth hormone receptor required for the activation of Jak2 and Stat proteins. Journal of Biological Chemistry 270 21326-21330.
27. -/- mice. Journal of Biological Chemistry 280 15038-15046.
28. Heinicke K, Baum O, Ogunshola OO, Vogel J, Stallmach T, Wolfer DP, Keller S, Weber K, Wagner PD, Gassmann M et al. 2006 Excessive erythrocytosis in adult mice overexpressing erythropoietin leads to hepatic, renal, neuronal, and muscular degeneration. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 291 R947-R956.
29. Hojman P, Brolin C, Gissel H, Brandt C, Zerahn B, Pedersen BK & Gehl J 2009 Erythropoietin over-expression protects against diet-induced obesity in mice through increased fat oxidation in muscles. PLoS ONE 4 e5894.
30. Houseknecht KL & Portocarrero CP 1998 Leptin and its receptors: regulators of whole-body energy homeostasis. Domestic Animal Endocrinology 15 457-475.
31. Issad T, Boute N, Boubekeur S & Lacasa D 2005 Interaction of PTPB with the insulin receptor precursor during its biosynthesis in the endoplasmic reticulum. Biochimie 87 111-116.
32. Katz O, Barzilay E, Skaat A, Herman A, Mittelman M & Neumann D 2005 Erythropoietin induced tumour mass reduction in murine lymphoproliferative models. Acta Haematologica 114 177-179.
33. Katz O, Gil L, Lifshitz L, Prutchi-Sagiv S, Gassmann M, Mittelman M & Neumann D 2007 Erythropoietin enhances immune responses in mice. European Journal of Immunology 37 1584-1593.
34. Keller U 2006 From obesity to diabetes. International Journal for Vitamin and Nutrition Research 76 172-177.
35. Klaman LD, Boss O, Peroni OD, Kim JK, Martino JL, Zabolotny JM, Moghal N, Lubkin M, Kim YB, Sharpe AH et al. 2000 Increased energy expenditure, decreased adiposity, and tissue-specific insulin sensitivity in protein-tyrosine phosphatase 1B-deficient mice. Molecular and Cellular Biology 20 5479-5489.
36. Kolonin MG, Saha PK, Chan L, Pasqualini R & Arap W 2004 Reversal of obesity by targeted ablation of adipose tissue. Nature Medicine 10 625-632.
37. Krantz SB 1991 Erythropoietin. Blood 77 419-434.
38. Lifshitz L, Prutchi-Sagiv S, Avneon M, Gassmann M, Mittelman M & Neumann D 2009 Non-erythroid activities of erythropoietin: functional effects on murine dendritic cells. Molecular Immunology 46 713-721.
39. Marzo F, Lavorgna A, Coluzzi G, Santucci E, Tarantino F, Rio T, Conti E, Autore C, Agati L & Andreotti F 2008 Erythropoietin in heart and vessels: focus on transcription and signalling pathways. Journal of Thrombosis and Thrombolysis 26 183-187.
40. Mittelman M 1996 Anemia of cancer: pathogenesis and treatment with recombinant erythropoietin. Israel Journal of Medical Sciences 32 1201-1206.
41. Mittelman M, Neumann D, Peled A, Kanter P & Haran-Ghera N 2001 Erythropoietin induces tumor regression and antitumor immune responses in murine myeloma models. PNAS 98 5181-5186.
42. Montel-Hagen A, Sitbon M & Taylor N 2009 Erythroid glucose transporters. Current Opinion in Hematology 16 165-172.
43. Muzzin P, Eisensmith RC, Copeland KC & Woo SL 1996 Correction of obesity and diabetes in genetically obese mice by leptin gene therapy. PNAS 93 14804-14808.
44. Pelleymounter MA, Cullen MJ, Baker MB, Hecht R, Winters D, Boone T & Collins F 1995 Effects of the obese gene product on body weight regulation in ob/ob mice. Science 269 540-543.
45. Pinto JP, Ribeiro S, Pontes H, Thowfeequ S, Tosh D, Carvalho F & Porto G 2008 Erythropoietin mediates hepcidin expression in hepatocytes through EPOR signaling and regulation of C/EBPalpha. Blood 111 5727-5733.
46. Pothiwala P, Jain SK & Yaturu S 2009 Metabolic syndrome and cancer. Metabolic Syndrome and Related Disorders 7 279-288.
47. Prutchi-Sagiv S, Golishevski N, Katz O, Oster HS, Naparstek E, Hoffman M, Neumann D & Mittelman M 2006a T-cell abnormalities in patients with myelodysplastic syndromes: improved immunological functionsin patietns treated with recombinant erythropoietin. Blood, The American Society of Hematology - 48th Annual Meeting, Abstract #2675.
48. Prutchi-Sagiv S, Golishevsky N, Oster HS, Katz O, Cohen A, Naparstek E, Neumann D & Mittelman M 2006b Erythropoietin treatment in advanced multiple myeloma is associated with improved immunological functions: could it be beneficial in early disease? British Journal of Haematology 135 660-672.
49. Prutchi-Sagiv S, Lifshitz L, Orkin R, Mittelman M & Neumann D 2008 Erythropoietin effects on dendritic cells: potential mediators in its function as an immunomodulator? Experimental Hematology 36 1682-1690.
50. Rasic-Milutinovic Z, Perunicic-Pekovic G, Cavala A, Gluvic Z, Bokan L & Stankovic S 2008 The effect of recombinant human erythropoietin treatment on insulin resistance and inflammatory markers in non-diabetic patients on maintenance hemodialysis. Hippokratia 12 157-161.
51. Rohlfing CL, Wiedmeyer HM, Little RR, England JD, Tennill A & Goldstein DE 2002 Defining the relationship between plasma glucose and HbA(1c): analysis of glucose profiles and HbA(1c) in the diabetes control and complications trial. Diabetes Care 25 275-278.
52. Rondinone CM, Trevillyan JM, Clampit J, Gum RJ, Berg C, Kroeger P, Frost L, Zinker BA, Reilly R, Ulrich R et al. 2002 Protein tyrosine phosphatase 1B reduction regulates adiposity and expression of genes involved in lipogenesis. Diabetes 51 2405-2411.
53. Rosen ED & Spiegelman BM 2006 Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444 847-853.
54. Ruschitzka FT, Wenger RH, Stallmach T, Quaschning T, de Wit C, Wagner K, Labugger R, Kelm M, Noll G, Rulicke T et al. 2000 Nitric oxide prevents cardiovascular disease and determines survival in polyglobulic mice overexpressing erythropoietin. PNAS 97 11609-11613.
55. Schiffer M, Park JK, Tossidou I, Bartels J, Shushakova N, Menne J & Fliser D 2008 Erythropoietin prevents diabetes-induced podocyte damage. Kidney & Blood Pressure Research 31 411-415.
56. Silverberg DS, Wexler D, Blum M, Tchebiner J, Sheps D, Keren G, Schwartz D, Baruch R, Yachnin T, Shaked M et al. 2002 The correction of anemia in severe resistant heart failure with erythropoietin and intravenous iron prevents the progression of both the heart and the renal failure and markedly reduces hospitalization. Clinical Nephrology 58 S37-S45.
57. Soliz J, Gassmann M & Joseph V 2007 Soluble erythropoietin receptor is present in the mouse brain and is required for the ventilatory acclimatization to hypoxia. Journal of Physiology 583 329-336.
58. Soliz J, Thomsen JJ, Soulage C, Lundby C & Gassmann M 2009 Sex-dependent regulation of hypoxic ventilation in mice and humans is mediated by erythropoietin. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 296 R1837-R1846.
59. Spaia S, Pangalos M, Askepidis N, Pazarloglou M, Mavropoulou E, Theodoridis S, Dimitrakopoulos K, Milionis A & Vayonas G 2000 Effect of short-term rHuEPO treatment on insulin resistance in haemodialysis patients. Nephron 84 320-325.
60. Spivak JL 1994 Recombinant human erythropoietin and the anemia of cancer [editorial]. Blood 84 997-1004.
61. Spivak JL, Pham T, Isaacs M & Hankins WD 1991 Erythropoietin is both a mitogen and a survival factor. Blood 77 1228-1233.
62. Tuzcu A, Bahceci M, Yilmaz E, Bahceci S & Tuzcu S 2004 The comparison of insulin sensitivity in non-diabetic hemodialysis patients treated with and without recombinant human erythropoietin. Hormone and Metabolic Research 36 716-720.
63. 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 2278-2284.
64. Wang ND, Finegold MJ, Bradley A, Ou CN, Abdelsayed SV, Wilde MD, Taylor LR, Wilson DR & Darlington GJ 1995 Impaired energy homeostasis in C/EBPalpha knockout mice. Science 269 1108-1112.
65. Waring JF, Ciurlionis R,Clampit JE, Morgan S, Gum RJ, Jolly RA, Kroeger P, Frost L, Trevillyan J, Zinker BA et al. 2003 PTP1B antisense-treated mice show regulation of genes involved in lipogenesis in liver and fat. Molecular and Cellular Endocrinology 203 155-168.
66. Wickler SJ & Gleeson TT 1993 Lactate and glucose metabolism in mouse (Mus musculus) and reptile (Anolis carolinensis) skeletal muscle. American Journal of Physiology 264 R487-R491.
67. Winearls CG, Oliver DO, Pippard MJ, Reid C, Downing MR & Cotes PM 1986 Effect of human erythropoietin derived from recombinant DNA on the anaemia of patients maintained by chronic haemodialysis. Lancet 2 1175-1178.
68. Zhang DE, Zhang P, Wang ND, Hetherington CJ, Darlington GJ & Tenen DG 1997 Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAATenhancer binding protein alpha-deficient mice. PNAS 94 569-574.