The erythropoietin-derived peptide ARA290 reverses mechanical allodynia in the neuritis model

Neuroscience

Volumn 233, Issue , 2013, Pages 174-183

  Pulman, K G T ^a   Smith, M ^a   Mengozzi, M ^a   Ghezzi, P ^a   Dilley, A ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

Allodynia; Chemokine (CC motif) ligand 2; Erythropoietin; Hyperalgesia; Neuritis; Tumor necrosis factor

Indexed keywords

ARA 290; ERYTHROPOIETIN; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUROPROTECTIVE AGENT; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG MECHANISM; HYPERALGESIA; MALE; NEURITIS; NEUROPATHIC PAIN; NEUROPROTECTION; NONHUMAN; PAIN ASSESSMENT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; CHEMOKINE CCL2; DISEASE MODELS, ANIMAL; ERYTHROPOIETIN; HYPERALGESIA; MALE; NEURALGIA; NEURITIS; NEUROPROTECTIVE AGENTS; OLIGOPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SCIATIC NERVE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84873749267     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.12.022     Document Type: Article

References (59)

1. Aley K.O., McCarter G., Levine J.D. Nitric oxide signaling in pain and nociceptor sensitization in the rat. J Neurosci 1998, 18:7008-7014.
2. Bennett G.J. A neuroimmune interaction in painful peripheral neuropathy. Clin J Pain 2000, 16:S139-S143.
3. Bennett G.J., Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988, 33:87-107.
4. Bernaudin M., Marti H.H., Roussel S., Divoux D., Nouvelot A., MacKenzie E.T., Petit E. A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab 1999, 19:643-651.
5. Bove G.M. Focal nerve inflammation induces neuronal signs consistent with symptoms of early complex regional pain syndromes. Exp Neurol 2009, 219:223-227.
6. Bove G.M., Weissner W., Barbe M.F. Long lasting recruitment of immune cells and altered epi-perineurial thickness in focal nerve inflammation induced by complete Freund's adjuvant. J Neuroimmunol 2009, 213:26-30.
7. Bove G.M., Dilley A. The conundrum of sensitization when recording from nociceptors. J Neurosci Methods 2010, 188:213-218.
8. Bove G.M., Ransil B.J., Lin H.C., Leem J.G. Inflammation induces ectopic mechanical sensitivity in axons of nociceptors innervating deep tissues. J Neurophysiol 2003, 90:1949-1955.
9. Brines M.L., Ghezzi P., Keenan S., Agnello D., de Lanerolle N.C., Cerami C., Itri L.M., Cerami A. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci U S A 2000, 97:10526-10531.
10. Brines M., Cerami A. Erythropoietin-mediated tissue protection: reducing collateral damage from the primary injury response. J Intern Med 2008, 264:405-432.
11. Brines M., Patel N.S., Villa P., Brines C., Mennini T., De Paola M., Erbayraktar Z., Erbayraktar S., Sepodes B., Thiemermann C., Ghezzi P., Yamin M., Hand C.C., Xie Q.W., Coleman T., Cerami A. Nonerythropoietic, tissue-protective peptides derived from the tertiary structure of erythropoietin. Proc Natl Acad Sci U S A 2008, 105:10925-10930.
12. Calapai G., Marciano M.C., Corica F., Allegra A., Parisi A., Frisina N., Caputi A.P., Buemi M. Erythropoietin protects against brain ischemic injury by inhibition of nitric oxide formation. Eur J Pharmacol 2000, 401:349-356.
13. Campana W.M., Li X., Shubayev V.I., Angert M., Cai K., Myers R.R. Erythropoietin reduces Schwann cell TNF-alpha, Wallerian degeneration and pain-related behaviors after peripheral nerve injury. Eur J Neurosci 2006, 23:617-626.
14. Campana W.M., Myers R.R. Exogenous erythropoietin protects against dorsal root ganglion apoptosis and pain following peripheral nerve injury. Eur J Neurosci 2003, 18:1497-1506.
15. Campana W.M., Myers R.R. Erythropoietin and erythropoietin receptors in the peripheral nervous system: changes after nerve injury. FASEB J 2001, 15:1804-1806.
16. Campbell J.N., Meyer R.A. Mechanisms of neuropathic pain. Neuron 2006, 52:77-92.
17. Chacur M., Milligan E.D., Gazda L.S., Armstrong C., Wang H., Tracey K.J., Maier S.F., Watkins L.R. A new model of sciatic inflammatory neuritis (SIN): induction of unilateral and bilateral mechanical allodynia following acute unilateral peri-sciatic immune activation in rats. Pain 2001, 94:231-244.
18. Chen Y., Boettger M.K., Reif A., Schmitt A., Uçeyler N., Sommer C. Nitric oxide synthase modulates CFA-induced thermal hyperalgesia through cytokine regulation in mice. Mol Pain 2010, 6:13.
19. Contaldo C., Lindenblatt N., Elsherbiny A., Högger D.C., Borozadi M.K., Vetter S.T., Lang K.S., Handschin A.E., Giovanoli P. Erythropoietin requires endothelial nitric oxide synthase to counteract TNF-[alpha]-induced microcirculatory dysfunction in murine striated muscle. Shock 2011, 35:315-321.
20. 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.
21. De Alba J., Clayton N.M., Collins S.D., Colthup P., Chessell I., Knowles R.G. GW274150, a novel and highly selective inhibitor of the inducible isoform of nitric oxide synthase (iNOS), shows analgesic effects in rat models of inflammatory and neuropathic pain. Pain 2006, 120:170-181.
22. Decosterd I., Woolf C.J. Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 2000, 87:149-158.
23. Dilley A. MRI signal hyper-intensity of neural tissues in diffuse chronic pain syndromes - a pilot study. Muscle Nerve 2011, 44:981-984.
24. Dilley A., Bove G.M. Resolution of inflammation-induced axonal mechanical sensitivity and conduction slowing in C-fiber nociceptors. J Pain 2008, 9:185-192.
25. Dilley A., Lynn B., Pang S.J. Pressure and stretch mechanosensitivity of peripheral nerve fibres following local inflammation of the nerve trunk. Pain 2005, 117:462-472.
26. Eliav E., Benoliel R., Herzberg U., Kalladka M., Tal M. The role of IL-6 and IL-1beta in painful perineural inflammatory neuritis. Brain Behav Immun 2009, 23:474-484.
27. Eliav E., Benoliel R., Tal M. Inflammation with no axonal damage of the rat saphenous nerve trunk induces ectopic discharge and mechanosensitivity in myelinated axons. Neurosci Lett 2001, 311:49-52.
28. Eliav E., Herzberg U., Ruda M.A., Bennett G.J. Neuropathic pain from an experimental neuritis of the rat sciatic nerve. Pain 1999, 83:169-182.
29. Gracely R.H., Lynch S.A., Bennett G.J. Painful neuropathy: altered central processing maintained dynamically by peripheral input. Pain 1992, 51:175-194.
30. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
31. Hoheisel U., Unger T., Mense S. Excitatory and modulatory effects of inflammatory cytokines and neurotrophins on mechanosensitive group IV muscle afferents in the rat. Pain 2005, 114:168-176.
32. Holthusen H. Involvement of the NO/cyclic GMP pathway in bradykinin evoked pain from veins in humans. Pain 1997, 69:87-92.
33. Jia H., Feng X., Li W., Hu Y., Zeng Q., Liu J., Xu J. Recombinant human erythropoietin attenuates spinal neuroimmune activation of neuropathic pain in rats. Ann Clin Lab Sci 2009, 39:84-91.
34. Jia H.B., Jin Y., Ji Q., Hu Y.F., Zhou Z.Q., Xu J.G., Yang J.J. Effects of recombinant human erythropoietin on neuropathic pain and cerebral expressions of cytokines and nuclear factor-kappa B. Can J Anaesth 2009, 56:597-603.
35. Kajander K.C., Bennett G.J. Onset of a painful peripheral neuropathy in rat: a partial and differential deafferentation and spontaneous discharge in A beta and A delta primary afferent neurons. J Neurophysiol 1992, 68:734-744.
36. Keswani S.C., Buldanlioglu U., Fischer A., Reed N., Polley M., Liang H., Zhou C., Jack C., Leitz G.J., Hoke A. A novel endogenous erythropoietin mediated pathway prevents axonal degeneration. Ann Neurol 2004, 56:815-826.
37. Kilic E., Kilic U., Soliz J., Bassetti C.L., Gassmann M., Hermann D.M. Brain-derived erythropoietin protects from focal cerebral ischemia by dual activation of ERK-1/-2 and Akt pathways. FASEB J 2005, 19:2026-2028.
38. Kim S.H., Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50:355-363.
39. Kim K.H., Kim J.I., Han J.A., Choe M.A., Ahn J.H. Upregulation of neuronal nitric oxide synthase in the periphery promotes pain hypersensitivity after peripheral nerve injury. Neuroscience 2011, 190:367-378.
40. Koshimura K., Murakami Y., Sohmiya M., Tanaka J., Kato Y. Effects of erythropoietin on neuronal activity. J Neurochem 1999, 72:2565-2572.
41. LaMotte R.H., Shain C.N., Simone D.A., Tsai E.P. Neurogenic hyperalgesia: psychophysical studies of underlying mechanisms. J Neurophysiol 1991, 66:190-211.
42. Leem J.G., Bove G.M. Mid-axonal tumor necrosis factor-alpha induces ectopic activity in a subset of slowly conducting cutaneous and deep afferent neurons. J Pain 2002, 3:45-49.
43. Mengozzi M., Cervellini I., Villa P., Erbayraktar Z., Gokmen N., Yilmaz O., Erbayraktar S., Manohasandra M., Van Hummelen P., Vandenabeele P., Chernajovsky Y., Annenkov A., Ghezzi P. Erythropoietin-induced changes in brain gene expression reveal induction of synaptic plasticity genes in experimental stroke. Proc Natl Acad Sci U S A 2012, 109:9617-9622.
44. Ozaktay A.C., Kallakuri S., Takebayashi T., Cavanaugh J.M., Asik I., DeLeo J.A., Weinstein J.N. Effects of interleukin-1 beta, interleukin-6, and tumor necrosis factor on sensitivity of dorsal root ganglion and peripheral receptive fields in rats. Eur Spine J 2006, 15:1529-1537.
45. Oztürk E., Demirbilek S., Köroglu A., But A., Begec Z.O., Gülec M., Akyol O., Ersoy M.O. Propofol and erythropoietin antioxidant properties in rat brain injured tissue. Prog Neuropsychopharmacol Biol Psychiatry 2008, 32:81-86.
46. Pregi N., Wenker S., Vittori D., Leirós C.P., Nesse A. TNF-alpha-induced apoptosis is prevented by erythropoietin treatment on SH-SY5Y cells. Exp Cell Res 2009, 315:419-431.
47. Richards N., Batty T., Dilley A. CCL2 has similar excitatory effects to TNF-{alpha} in a subgroup of inflamed C-fiber axons. J Neurophysiol 2011, 106:2838-2848.
48. Sakanaka M., Wen T.C., Matsuda S., Masuda S., Morishita E., Nagao M., Sasaki R. In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc Natl Acad Sci U S A 1998, 95:4635-4640.
49. Schafers M., Lee D.H., Brors D., Yaksh T.L., Sorkin L.S. Increased sensitivity of injured and adjacent uninjured rat primary sensory neurons to exogenous tumor necrosis factor-alpha after spinal nerve ligation. J Neurosci 2003, 23:3028-3038.
50. Sirén A.L., Fratelli M., Brines M., Goemans C., Casagrande S., Lewczuk P., Keenan S., Gleiter C., Pasquali C., Capobianco A., Mennini T., Heumann R., Cerami A., Ehrenreich H., Ghezzi P. Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci U S A 2001, 98:4044-4049.
51. Sommer C., Lindenlaub T., Teuteberg P., Schafers M., Hartung T., Toyka K.V. Anti-TNF-neutralizing antibodies reduce pain-related behavior in two different mouse models of painful mononeuropathy. Brain Res 2001, 913:86-89.
52. Sommer C., Marziniak M., Myers R.R. The effect of thalidomide treatment on vascular pathology and hyperalgesia caused by chronic constriction injury of rat nerve. Pain 1998, 74:83-91.
53. Sorkin L.S., Xiao W.H., Wagner R., Myers R.R. Tumour necrosis factor-alpha induces ectopic activity in nociceptive primary afferent fibres. Neuroscience 1997, 81:255-262.
54. Swartjes M., Morariu A., Niesters M., Brines M., Cerami A., Aarts L., Dahan A. ARA290, a peptide derived from the tertiary structure of erythropoietin, produces long-term relief of neuropathic pain: an experimental study in rats and beta-common receptor knockout mice. Anesthesiology 2011, 115:1084-1092.
55. Tal M., Bennett G.J. Extra-territorial pain in rats with a peripheral mononeuropathy: mechano-hyperalgesia and mechano-allodynia in the territory of an uninjured nerve. Pain 1994, 57:375-382.
56. Tal M., Eliav E. Abnormal discharge originates at the site of nerve injury in experimental constriction neuropathy (CCI) in the rat. Pain 1996, 64:511-518.
57. Toth C., Martinez J.A., Liu W.Q., Diggle J., Guo G.F., Ramji N., Mi R., Hoke A., Zochodne D.W. Local erythropoietin signaling enhances regeneration in peripheral axons. Neuroscience 2008, 154:767-783.
58. Villa P., Bigini P., Mennini T., Agnello D., Laragione T., Cagnotto A., Viviani B., Marinovich M., Cerami A., Coleman T.R., Brines M., Ghezzi P. Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis. J Exp Med 2003, 198:971-975.
59. Woolf C.J. Central sensitization: implications for the diagnosis and treatment of pain. Pain 2011, 152:S2-15.