Delayed administration of erythropoietin and its non-erythropoietic derivatives ameliorates chronic murine autoimmune encephalomyelitis

Journal of Neuroimmunology

Volumn 172, Issue 1-2, 2006, Pages 27-37

  Savino, Costanza ^a   Pedotti, Rosetta ^b   Baggi, Fulvio ^b   Ubiali, Federica ^b   Gallo, Barbara ^b   Nava, Sara ^b   Bigini, Paolo ^a   Barbera, Sara ^a   Fumagalli, Elena ^a   Mennini, Tiziana ^a   Vezzani, Annamaria ^a   Rizzi, Massimo ^a   Coleman, Thomas ^c   Cerami, Anthony ^c   Brines, Michael ^c   Ghezzi, Pietro ^a,c   Bianchi, Roberto ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b DEPARTMENT OF NEUROSURGERY   (Italy)

^c Kenneth S Warren Institute   (United States)

Author keywords

Asialoerythropoietin; Carbamylated erythropoietin; Cytokine; EAE; Erythropoietin; Inflammation; Multiple sclerosis; Spinal cord

Indexed keywords

ERYTHROPOIETIN RECEPTOR; HEMOGLOBIN; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; RECOMBINANT ERYTHROPOIETIN; TUMOR NECROSIS FACTOR ALPHA;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CLINICAL FEATURE; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG DOSE REGIMEN; DRUG EFFECT; DRUG EFFICACY; FEMALE; HEMATOPOIESIS; HEMOGLOBIN DETERMINATION; HUMAN; LOW DRUG DOSE; MOUSE; MULTIPLE SCLEROSIS; NEUROPROTECTION; NONHUMAN; ONSET AGE; PRIORITY JOURNAL; SPINAL CORD; THERAPY DELAY; UNSPECIFIED SIDE EFFECT;

ANALYSIS OF VARIANCE; ANIMALS; BODY WEIGHT; CHRONIC DISEASE; CYTOKINES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ERYTHROPOIETIN; ERYTHROPOIETIN, RECOMBINANT; FEMALE; GLYCOPROTEINS; HEMATOCRIT; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; PEPTIDE FRAGMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEVERITY OF ILLNESS INDEX; SPINAL CORD; SPLEEN; STATISTICS, NONPARAMETRIC; TIME FACTORS; TREATMENT OUTCOME; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33244474401     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2005.10.016     Document Type: Article

References (63)

1. D. Agnello, P. Bigini, P. Villa, T. Mennini, A. Cerami, M.L. Brines, and P. Ghezzi Erythropoietin exerts an anti-inflammatory effect on the CNS in a model of experimental autoimmune encephalomyelitis Brain Res. 952 2002 128 134
2. S. Amor, J.K. O'Neill, M.M. Morris, R.M. Smith, D.C. Wraith, N. Groome, P.J. Travers, and D. Baker Encephalitogenic epitopes of myelin basic protein, proteolipid protein, myelin oligodendrocyte glycoprotein for experimental allergic encephalomyelitis induction in Biozzi ABH (H-2Ag7) mice share an amino acid motif J. Immunol. 156 1996 3000 3008
3. R. Bianchi, B. Buyukakilli, M. Brines, C. Savino, G. Cavaletti, N. Oggioni, G. Lauria, M. Borgna, R. Lombardi, B. Cimen, U. Comelekoglu, A. Kanik, C. Tataroglu, A. Cerami, and P. Ghezzi Erythropoietin both protects from and reverses experimental diabetic neuropathy Proc. Natl. Acad. Sci. U. S. A. 101 2004 823 828
4. C. Bokemeyer, M.S. Aapro, A. Courdi, J. Foubert, H. Link, A. Osterborg, L. Repetto, and P. Soubeyran EORTC guidelines for the use of erythropoietic proteins in anaemic patients with cancer Eur. J. Cancer 40 2004 2201 2216
5. M. Brines, and A. Cerami Emerging biological roles for erythropoietin in the nervous system Nat. Rev. Neurosci. 6 2005 484 494
6. M.L. Brines, P. Ghezzi, S. Keenan, D. Agnello, N.C. de Lanerolle, C. Cerami, L.M. Itri, and A. Cerami Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury Proc. Natl. Acad. Sci. U. S. A. 97 2000 10526 10531
7. M. Brines, G. Grasso, F. Fiordaliso, A. Sfacteria, P. Ghezzi, M. Fratelli, R. Latini, Q.W. Xie, J. Smart, C.J. Su-Rick, E. Pobre, D. Diaz, D. Gomez, C. Hand, T. Coleman, and A. Cerami Erythropoietin mediates tissue protection through an erythropoietin and common beta-subunit heteroreceptor Proc. Natl. Acad. Sci. U. S. A. 101 2004 14907 14912
8. N. Casadevall, J. Nataf, B. Viron, A. Kolta, J.J. Kiladjian, P. Martin-Dupont, P. Michaud, T. Papo, V. Ugo, I. Teyssandier, B. Varet, and P. Mayeux Pure red-cell aplasia and antierythropoietin antibodies in patients treated with recombinant erythropoietin N. Engl. J. Med. 346 2002 469 475
9. M. Celik, N. Gokmen, S. Erbayraktar, M. Akhisaroglu, S. Konakc, C. Ulukus, S. Genc, K. Genc, E. Sagiroglu, A. Cerami, and M. Brines Erythropoietin prevents motor neuron apoptosis and neurologic disability in experimental spinal cord ischemic injury Proc. Natl. Acad. Sci. U. S. A. 99 2002 2258 2263
10. Y.S. Chang, D. Mu, M. Wendland, R.A. Sheldon, Z.S. Vexler, P.S. McQuillen, and D.M. Ferriero Erythropoietin improves functional and histological outcome in neonatal stroke Pediatr. Res. 58 2005 106 111
11. P. Chomczynski, and N. Sacchi Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal. Biochem. 162 1987 156 159
12. S. Dasgupta, M. Jana, Y. Zhou, Y.K. Fung, S. Ghosh, and K. Pahan Antineuroinflammatory effect of NF-kappaB essential modifier-binding domain peptides in the adoptive transfer model of experimental allergic encephalomyelitis J. Immunol. 173 2004 1344 1354
13. H.E. de Vries, J. Kuiper, A.G. de Boer, T.J. Van Berkel, and D.D. Breimer The blood-brain barrier in neuroinflammatory diseases Pharmacol. Rev. 49 1997 143 155
14. R. Diem, M.B. Sattler, D. Merkler, I. Demmer, K. Maier, C. Stadelmann, H. Ehrenreich, and M. Bahr Combined therapy with methylprednisolone and erythropoietin in a model of multiple sclerosis Brain 128 2005 375 385
15. M. Digicaylioglu, and S.A. Lipton Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades Nature 412 2001 641 647
16. H. Ehrenreich, M. Hasselblatt, C. Dembowski, L. Cepek, P. Lewczuk, M. Stiefel, H.H. Rustenbeck, N. Breiter, S. Jacob, F. Knerlich, M. Bohn, W. Poser, E. Ruther, M. Kochen, O. Gefeller, C. Gleiter, T.C. Wessel, M. De Ryck, L. Itri, H. Prange, A. Cerami, M. Brines, and A.L. Siren Erythropoietin therapy for acute stroke is both safe and beneficial Mol. Med. 8 2002 495 505
17. S. Erbayraktar, G. Grasso, A. Sfacteria, Q.W. Xie, T. Coleman, M. Kreilgaard, L. Torup, T. Sager, Z. Erbayraktar, N. Gokmen, O. Yilmaz, P. Ghezzi, P. Villa, M. Fratelli, S. Casagrande, M. Leist, L. Helboe, J. Gerwein, S. Christensen, M.A. Geist, L.O. Pedersen, C. Cerami-Hand, J.P. Wuerth, A. Cerami, and M. Brines Asialoerythropoietin is a nonerythropoietic cytokine with broad neuroprotective activity in vivo Proc. Natl. Acad. Sci. U. S. A. 100 2003 6741 6746
18. M.N. Fukuda, H. Sasaki, L. Lopez, and M. Fukuda Survival of recombinant erythropoietin in the circulation: the role of carbohydrates Blood 73 1989 84 89
19. R. Furlan, E. Brambilla, F. Ruffini, P.L. Poliani, A. Bergami, P.C. Marconi, D.M. Franciotta, G. Penna, G. Comi, L. Adorini, and G. Martino Intrathecal delivery of IFN-gamma protects C57BL/6 mice from chronic-progressive experimental autoimmune encephalomyelitis by increasing apoptosis of central nervous system-infiltrating lymphocytes J. Immunol. 167 2001 1821 1829
20. P. Ghezzi, and M. Brines Erythropoietin as an antiapoptotic, tissue-protective cytokine Cell Death Differ. 11 2004 S37 S44
21. G.W. Gill, J.K. Frost, and K.A. Miller A new formula for a half-oxidized hematoxylin solution that neither overstains nor requires differentiation Acta Cytol. 18 1974 300 311
22. A. Gorio, N. Gokmen, S. Erbayraktar, O. Yilmaz, L. Madaschi, C. Cichetti, A.M. Di Giulio, E. Vardar, A. Cerami, and M. Brines Recombinant human erythropoietin counteracts secondary injury and markedly enhances neurological recovery from experimental spinal cord trauma Proc. Natl. Acad. Sci. U. S. A. 99 2002 9450 9455
23. U. Graumann, R. Reynolds, A.J. Steck, and N. Schaeren-Wiemers Molecular changes in normal appearing white matter in multiple sclerosis are characteristic of neuroprotective mechanisms against hypoxic insult Brain Pathol. 13 2003 554 573
24. T.U.R.H.E.P.S. Group Double-blind, placebo-controlled study of the therapeutic use of recombinant human erythropoietin for anemia associated with chronic renal failure in predialysis patients. The US Recombinant Human Erythropoietin Predialysis Study Group Am. J. Kidney Dis. 18 1991 50 59
25. B. Hilliard, E.B. Samoilova, T.S. Liu, A. Rostami, and Y. Chen Experimental autoimmune encephalomyelitis in NF-kappa B-deficient mice: roles of NF-kappa B in the activation and differentiation of autoreactive T cells J. Immunol. 163 1999 2937 2943
26. B.A. Hilliard, N. Mason, L. Xu, J. Sun, S.E. Lamhamedi-Cherradi, H.C. Liou, C. Hunter, and Y.H. Chen Critical roles of c-Rel in autoimmune inflammation and helper T cell differentiation J. Clin. Invest. 110 2002 843 850
27. C.R. Houser, R.P. Barber, G.D. Crawford, D.A. Matthews, P.E. Phelps, P.M. Salvaterra, and J.E. Vaughn Species-specific second antibodies reduce spurious staining in immunocytochemistry J. Histochem. Cytochem. 32 1984 395 402
28. N. Imai, M. Higuchi, A. Kawamura, K. Tomonoh, M. Oh-Eda, M. Fujiwara, Y. Shimonaka, and N. Ochi Physicochemical and biological characterization of asialoerythropoietin. Suppressive effects of sialic acid in the expression of biological activity of human erythropoietin in vitro Eur. J. Biochem. 194 1990 457 462
29. W. Jelkmann, and K. Wagner Beneficial and ominous aspects of the pleiotropic action of erythropoietin Ann. Hematol. 83 2004 673 686
30. S. Juul Recombinant erythropoietin as a neuroprotective treatment: in vitro and in vivo models Clin. Perinatol. 31 2004 129 142
31. S.E. Juul, R.J. McPherson, F.X. Farrell, L. Jolliffe, D.J. Ness, and C.A. Gleason Erytropoietin concentrations in cerebrospinal fluid of nonhuman primates and fetal sheep following high-dose recombinant erythropoietin Biol. Neonate 85 2004 138 144
32. S.L. Kirk, and S.J. Karlik VEGF and vascular changes in chronic neuroinflammation J. Autoimmun. 21 2003 353 363
33. H. Lassmann Hypoxia-like tissue injury as a component of multiple sclerosis lesions J. Neurol. Sci. 206 2003 187 191
34. M. Leist, P. Ghezzi, G. Grasso, R. Bianchi, P. Villa, M. Fratelli, C. Savino, M. Bianchi, J. Nielsen, J. Gerwien, P. Kallunki, A.K. Larsen, L. Helboe, S. Christensen, L.O. Pedersen, M. Nielsen, L. Torup, T. Sager, A. Sfacteria, S. Erbayraktar, Z. Erbayraktar, N. Gokmen, O. Yilmaz, C. Cerami-Hand, Q.-w. Xie, T. Coleman, A. Cerami, and M. Brines Derivatives of erythropoietin that are tissue protective but not erythropoietic Science 305 2004 239 242
35. W. Li, Y. Maeda, R.R. Yuan, S. Elkabes, S. Cook, and P. Dowling Beneficial effect of erythropoietin on experimental allergic encephalomyelitis Ann. Neurol. 56 2004 767 777
36. V.S. Lim Recombinant human erythropoietin in predialysis patients Am. J. Kidney Dis. 18 1991 34 37
37. R.A. Linker, M. Maurer, S. Gaupp, R. Martini, B. Holtmann, R. Giess, P. Rieckmann, H. Lassmann, K.V. Toyka, M. Sendtner, and R. Gold CNTF is a major protective factor in demyelinating CNS disease: a neurotrophic cytokine as modulator in neuroinflammation Nat. Med. 8 2002 620 624
38. C. Lock, G. Hermans, R. Pedotti, A. Brendolan, E. Schadt, H. Garren, A. Langer-Gould, S. Strober, B. Cannella, J. Allard, P. Klonowski, A. Austin, N. Lad, N. Kaminski, S.J. Galli, J.R. Oksenberg, C.S. Raine, R. Heller, and L. Steinman Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis Nat. Med. 8 2002 500 508
39. K. Maiese, F. Li, and Z.Z. Chong New avenues of exploration for erythropoietin JAMA 293 2005 90 95
40. O.M. Martinez-Estrada, E. Rodriguez-Millan, E. Gonzalez-De Vicente, M. Reina, S. Vilaro, and M. Fabre Erythropoietin protects the in vitro blood-brain barrier against VEGF-induced permeability Eur. J. Neurosci. 18 2003 2538 2544
41. G. Martino How the brain repairs itself: new therapeutic strategies in inflammatory and degenerative CNS disorders Lancet Neurol. 3 2004 372 378
42. G. Martino, L. Adorini, P. Rieckmann, J. Hillert, B. Kallmann, G. Comi, and M. Filippi Inflammation in multiple sclerosis: the good, the bad, and the complex Lancet Neurol. 1 2002 499 509
43. S. Marusic, J.S. Miyashiro, J. Douhan III, R.F. Konz, D. Xuan, J.W. Pelker, V. Ling, J.P. Leonard, and K.A. Jacobs Local delivery of granulocyte macrophage colony-stimulating factor by retrovirally transduced antigen-specific T cells leads to severe, chronic experimental autoimmune encephalomyelitis in mice Neurosci. Lett. 332 2002 185 189
44. J.L. McQualter, R. Darwiche, C. Ewing, M. Onuki, T.W. Kay, J.A. Hamilton, H.H. Reid, and C.C. Bernard Granulocyte macrophage colony-stimulating factor: a new putative therapeutic target in multiple sclerosis J. Exp. Med. 194 2001 873 882
45. A. Micera, F. Properzi, V. Triaca, and L. Aloe Nerve growth factor antibody exacerbates neuropathological signs of experimental allergic encephalomyelitis in adult Lewis rats J. Neuroimmunol. 104 2000 116 123
46. A. Natali, E. Toschi, S. Baldeweg, A. Casolaro, S. Baldi, A.M. Sironi, J.S. Yudkin, and E. Ferrannini Haematocrit, type 2 diabetes, and endothelium-dependent vasodilatation of resistance vessels Eur. Heart J. 26 2005 464 471
47. F. Nicoletti, F. Patti, R. DiMarco, P. Zaccone, A. Nicoletti, P. Meroni, and A. Reggio Circulating serum levels of IL-1Ra in patients with relapsing remitting multiple sclerosis are normal during remission phases but significantly increased either during exacerbations or in response to IFN-beta treatment Cytokine 8 1996 395 400
48. K. Pahan, and M. Schmid Activation of nuclear factor-κB in the spinal cord of experimental allergic encephalomyelitis Neurosci. Lett. 287 2000 17 20
49. S. Pluchino, A. Quattrini, E. Brambilla, A. Gritti, G. Salani, G. Dina, R. Galli, U. Del Carro, S. Amadio, A. Bergami, R. Furlan, G. Comi, A.L. Vescovi, and G. Martino Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis Nature 422 2003 688 694
50. M.A. Proescholdt, S. Jacobson, N. Tresser, E.H. Oldfield, and M.J. Merrill Vascular endothelial growth factor is expressed in multiple sclerosis plaques and can induce inflammatory lesions in experimental allergic encephalomyelitis rats J. Neuropathol. Exp. Neurol. 61 2002 914 925
51. T. Quaschning, F. Ruschitzka, T. Stallmach, S. Shaw, H. Morawietz, W. Goettsch, M. Hermann, T. Slowinski, F. Theuring, B. Hocher, T.F. Luscher, and M. Gassmann Erythropoietin-induced excessive erythrocytosis activates the tissue endothelin system in mice FASEB J. 17 2003 259 261
52. F.T. Ruschitzka, R.H. Wenger, T. Stallmach, T. Quaschning, C. de Wit, K. Wagner, R. Labugger, M. Kelm, G. Noll, T. Rulicke, S. Shaw, R.L. Lindberg, B. Rodenwaldt, H. Lutz, C. Bauer, T.F. Luscher, and M. Gassmann Nitric oxide prevents cardiovascular disease and determines survival in polyglobulic mice overexpressing erythropoietin Proc. Natl. Acad. Sci. U. S. A. 97 2000 11609 11613
53. M.B. Sattler, D. Merkler, K. Maier, C. Stadelmann, H. Ehrenreich, M. Bahr, and R. Diem Neuroprotective effects and intracellular signaling pathways of erythropoietin in a rat model of multiple sclerosis Cell Death Differ. 11 Suppl 2 2004 S181 S192
54. T. Shingo, S.T. Sorokan, T. Shimazaki, and S. Weiss Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells J. Neurosci. 21 2001 9733 9743
55. L. Steinman Optic neuritis, a new variant of experimental encephalomyelitis, a durable model for all seasons, now in its seventieth year J. Exp. Med. 197 2003 1065 1071
56. L. Steinman Immune therapy for autoimmune diseases Science 305 2004 212 216
57. M. Sugawa, Y. Sakurai, Y. Ishikawa-Ieda, H. Suzuki, and H. Asou Effects of erythropoietin on glial cell development; oligodendrocyte maturation and astrocyte proliferation Neurosci. Res. 44 2002 391 403
58. B. Varet, N. Casadevall, C. Lacombe, and P. Nayeaux Erythropoietin: physiology and clinical experience Semin. Hematol. 27 1990 25 31
59. P. Villa, P. Bigini, T. Mennini, D. Agnello, T. Laragione, A. Cagnotto, B. Viviani, M. Marinovich, A. Cerami, T.R. Coleman, M. Brines, and P. Ghezzi Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis J. Exp. Med. 198 2003 971 975
60. B. Viviani, S. Bartesaghi, E. Corsini, P. Villa, P. Ghezzi, A. Garau, C.L. Galli, and M. Marinovich Erythropoietin protects primary hippocampal neurons increasing the expression of brain-derived neurotrophic factor J. Neurochem. 93 2005 412 421
61. L. Wang, Z. Zhang, Y. Wang, R. Zhang, and M. Chopp Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats Stroke 35 2004 1732 1737
62. D.L. Yao, X. Liu, L.D. Hudson, and H.D. Webster Insulin-like growth factor I treatment reduces demyelination and up-regulates gene expression of myelin-related proteins in experimental autoimmune encephalomyelitis Proc. Natl. Acad. Sci. U. S. A. 92 1995 6190 6194
63. J. Zhang, Y. Li, Y. Cui, J. Chen, M. Lu, S.B. Elias, and M. Chopp Erythropoietin treatment improves neurological functional recovery in EAE mice Brain Res. 1034 2005 34 39