Central or peripheral delivery of an adenosine A1 receptor agonist improves mechanical allodynia in a mouse model of painful diabetic neuropathy

Neuroscience

Volumn 285, Issue , 2015, Pages 312-323

  Katz, N K ^a   Ryals, J M ^a   Wright, D E ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Adenosine A1 receptor; Diabetes; Mechanical allodynia; Neuropathy; Pain

Indexed keywords

5' IODOTUBERCIDIN; 6 N CYCLOPENTYLADENOSINE; ACID PHOSPHATASE PROSTATE ISOENZYME; ADENOSINE; ADENOSINE A1 RECEPTOR; ADENOSINE KINASE INHIBITOR; ADENOSINE PHOSPHATE; ECTO 5' NUCLEOTIDASE; GLUCOSE; HUMAN PROSTATIC ACID PHOSPHATASE; MESSENGER RNA; PHOSPHATASE; UNCLASSIFIED DRUG; ADENOSINE A1 RECEPTOR AGONIST; ANALGESIC AGENT; N(6)-CYCLOPENTYLADENOSINE;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CENTRAL DRUG DELIVERY; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVITY; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HISTOCHEMISTRY; HYDROLYSIS; IN VIVO STUDY; INTRAPLANTAR DRUG ADMINISTRATION; MALE; MECHANICAL ALLODYNIA; MECHANICAL WITHDRAWAL THRESHOLD; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PAIN PARAMETERS; PERIPHERAL DRUG DELIVERY; PH; PROTEIN EXPRESSION; SINGLE DRUG DOSE; SPINAL CORD; SPINAL GANGLION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; STREPTOZOTOCIN-INDUCED DIABETIC NEUROPATHY; ANALOGS AND DERIVATIVES; ANIMAL; DIABETIC NEUROPATHIES; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; FOOT; HINDLIMB; HYPERALGESIA; INTRASPINAL DRUG ADMINISTRATION; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TOUCH;

ADENOSINE; ADENOSINE A1 RECEPTOR AGONISTS; ADENOSINE MONOPHOSPHATE; ANALGESICS, NON-NARCOTIC; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; FOOT; GANGLIA, SPINAL; HINDLIMB; HYDROLYSIS; HYPERALGESIA; INJECTIONS, SPINAL; MALE; MICE; NEURONS; RECEPTOR, ADENOSINE A1; SPINAL CORD; TOUCH;

EID: 84916631340     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.10.065     Document Type: Article

References (66)

1. Abbracchio M.P., Burnstock G., Verkhratsky A., Zimmermann H. Purinergic signalling in the nervous system: an overview. Trends Neurosci 2009, 32:19-29.
2. Akkina S.K., Patterson C.L., Wright D.E. GDNF rescues nonpeptidergic unmyelinated primary afferents in streptozotocin-treated diabetic mice. Exp Neurol 2001, 167:173-182.
3. Aley K.O., Green P.G., Levine J.D. Opioid and adenosine peripheral antinociception are subject to tolerance and withdrawal. J Neurosci 1995, 15:8031-8038.
4. Argoff C.E. Topical analgesics in the management of acute and chronic pain. Mayo Clin Proc 2013, 88:195-205.
5. Bantel C., Childers S.R., Eisenach J.C. Role of adenosine receptors in spinal G-protein activation after peripheral nerve injury. Anesthesiology 2002, 96:1443-1449.
6. Baron R., Mayoral V., Leijon G., Binder A., Steigerwald I., Serpell M. Efficacy and safety of combination therapy with 5% lidocaine medicated plaster and pregabalin in post-herpetic neuralgia and diabetic polyneuropathy. Curr Med Res Opin 2009, 25:1677-1687.
7. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 2007, 87:659-797.
8. Burnstock G. Purinergic signalling and disorders of the central nervous system. Nat Rev Drug Discov 2008, 7:575-590.
9. Callaghan B.C., Cheng H.T., Stables C.L., Smith A.L., Feldman E.L. Diabetic neuropathy: clinical manifestations and current treatments. Lancet Neurol 2012, 11:521-534.
10. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53:55-63.
11. 2 receptors of the substantia gelatinosa are located predominantly on intrinsic neurons: an autoradiography study. J Pharmacol Exp Ther 1988, 247:757-764.
12. Cole B.E. Diabetic peripheral neuropathic pain: recognition and management. Pain Med 2007, 8(suppl. 2):S27-32.
13. Corder G., Siegel A., Intondi A.B., Zhang X., Zadina J.E., Taylor B.K. A novel method to quantify histochemical changes throughout the mediolateral axis of the substantia gelatinosa after spared nerve injury: characterization with TRPV1 and substance P. J Pain 2010, 11:388-398.
14. Cui J.G., Sollevi A., Linderoth B., Meyerson B.A. Adenosine receptor activation suppresses tactile hypersensitivity and potentiates spinal cord stimulation in mononeuropathic rats. Neurosci Lett 1997, 223:173-176.
15. Curros-Criado M.M., Herrero J.F. The antinociceptive effects of the systemic adenosine A1 receptor agonist CPA in the absence and in the presence of spinal cord sensitization. Pharmacol Biochem Behav 2005, 82:721-726.
16. DeLander G.E., Hopkins C.J. Involvement of A2 adenosine receptors in spinal mechanisms of antinociception. Eur J Pharmacol 1987, 139:215-223.
17. Deuchars S.A., Brooke R.E., Deuchars J. Adenosine A1 receptors reduce release from excitatory but not inhibitory synaptic inputs onto lateral horn neurons. J Neurosci 2001, 21:6308-6320.
18. Duby J.J., Campbeell R.K., Setter S.M., White J.R., Rasmussen K.A. Diabetic neuropathy: an intense review. Am J Health Syst Pharm 2004, 61:160-173.
19. Dworkin R.H., O'Connor A.B., Audette J., Baron R., Gourlay G.K., Haanpaa M.L., Kent J.L., Krane E.J., Lebel A.A., Levy R.M., Mackey S.C., Mayer J., Miaskowski C., Raja S.N., Rice A.S., Schmader K.E., Stacey B., Stanos S., Treede R.D., Turk D.C., Walco G.A., Wells C.D. Recommendations for the pharmacological management of neuropathic pain: an overview and literature update. Mayo Clin Proc 2010, 85:S3-14.
20. Fairbanks C.A. Spinal delivery of analgesics in experimental models of pain and analgesia. Adv Drug Deliv Rev 2003, 55:1007-1041.
21. Fredholm B.B., AP I.J., Jacobson K.A., Linden J., Muller C.E. International Union of Basic and Clinical Pharmacology. LXXXI. Nomenclature and classification of adenosine receptors - an update. Pharmacol Rev 2011, 63:1-34.
22. Fredholm B.B., Ijzerman A.P., Jacobson K.A., Klotz K.N., Linden J. International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol Rev 2001, 53:527-552.
23. Gan M.J., Albanese-O'Neill A., Haller M.J. Type 1 diabetes: current concepts in epidemiology, pathophysiology, clinical care, and research. Curr Prob Pediatr Adolesc Health Care 2012, 42:269-291.
24. Goding J.W. Ecto-enzymes: physiology meets pathology. J Leukoc Biol 2000, 67:285-311.
25. Guieu R., Peragut J.C., Roussel P., Hassani H., Sampieri F., Bechis G., Gola R., Rochat H. Adenosine and neuropathic pain. Pain 1996, 68:271-274.
26. Horiuchi H., Ogata T., Morino T., Yamamoto H. Adenosine A1 receptor agonists reduce hyperalgesia after spinal cord injury in rats. Spinal Cord 2010, 48:685-690.
27. Hurt J.K., Zylka M.J. PAPupuncture has long-lasting antinociceptive effects in mouse models of acute and chronic pain. Mol Pain 2012, 8:28.
28. Irving G.A., Backonja M.M., Dunteman E., Blonsky E.R., Vanhove G.F., Lu S.P., Tobias J., Group N-.C.S. A multicenter, randomized, double-blind, controlled study of NGX-4010, a high-concentration capsaicin patch, for the treatment of postherpetic neuralgia. Pain Med 2011, 12:99-109.
29. Karlsten R., Gordh T., Post C. Local antinociceptive and hyperalgesic effects in the formalin test after peripheral administration of adenosine analogues in mice. Pharmacol Toxicol 1992, 70:434-438.
30. Krein S.L. The effect of chronic pain in diabetes patients' self-management. Diabetes Care 2005, 28:65-70.
31. Lee-Kubli C.A., Mixcoatl-Zecuatl T., Jolivalt C.G., Calcutt N.A. Animal models of diabetes-induced neuropathic pain. Curr Top Behav Neurosci 2014.
32. Lee Y.-W., Yaksh T.L. Pharmacology of the spinal adenosine receptor which mediates antiallodynic action of intrathecal adenosine agonists. JPET 1996, 277:1642-1648.
33. Li J., Perl E.R. Adenosine inhibition of synaptic transmission in the substantia gelatinosa. J Neurophysiol 1994, 72:1611-1621.
34. Lima F.O., Souza G.R., Verri W.A., Parada C.A., Ferreira S.H., Cunha F.Q., Cunha T.M. Direct blockade of inflammatory hypernociception by peripheral A1 adenosine receptors: involvement of the NO/cGMP/PKG/KATP signaling pathway. Pain 2010, 151:506-515.
35. Longhi M.S., Robson S.C., Bernstein S.H., Serra S., Deaglio S. Biological functions of ecto-enzymes in regulating extracellular adenosine levels in neoplastic and inflammatory disease states. J Mol Med 2013, 91:165-172.
36. McGreevy K., Williams K.A. Contemporary insights into painful diabetic neuropathy and treatment with spinal cord stimulation. Curr Pain Headache Rep 2012, 16:43-49.
37. Quintero I.B., Araujo C.L., Pulkka A.E., Wirkkala R.S., Herrala A.M., Eskelinen E.L., Jokitalo E., Hellstrom P.A., Tuominen H.J., Hirvikoski P.P., Vihko P.T. Prostatic acid phosphatase is not a prostate specific target. Cancer Res 2007, 67:6549-6554.
38. Said G. Diabetic neuropathy - a review. Nat Clin Pract Neurol 2007, 3:331-340.
39. Sawynok J. Adenosine receptor activation and nociception. Eur J Pharmacol 1998, 317:1-11.
40. Sawynok J. Topical and peripherally acting analgesics. Pharmacol Rev 2003, 55:1-20.
41. Sawynok J. Adenosine and ATP receptors. HEP 2006, 177:309-328.
42. Sawynok J., Liu X.J. Adenosine in the spinal cord and periphery: release and regulation of pain. Prog Neurobiol 2003, 69:313-340.
43. Sawynok J., Zarrindast M.R., Reid A.R., Doak G.J. Adenosine A3 receptor activation produces nociceptive behaviour and edema by release of histamine and 5-hydroxytryptamine. Eur J Pharmacol 1997, 333:1-7.
44. Schulte G., Robertson B., Fredholm B.B., DeLander G.E., Shortland P., Molander C. Distribution of antinociceptive adenosine a1 receptors in the spinal cord dorsal horn, and relationship to primary afferents and neuronal subpopulations. Neuroscience 2003, 121:907-916.
45. Simpson D.M., Brown S., Tobias J., Grp N.C.S. Controlled trial of high-concentration capsaicin patch for treatment of painful HIV neuropathy. Neurology 2008, 70:2305-2313.
46. Sjolund K.F., von Heijne M., Hao J.X., Xu X.J., Sollevi A., Weisenfeld-Hallin Z. Intrathecal administration of the adenosine A1 receptor agonist R-phenylisopropyl adenosine reduces presumed pain behavior in a rat model of central pain. Neurosci Lett 1998, 243:89-92.
47. Smith H.S., Argoff C.E. Pharmacological treatment of diabetic neuropathic pain. Drugs 2011, 71:557-589.
48. Snedecor S.J., Sudharshan L., Cappelleri J.C., Sadosky A., Mehta S., Botteman M. Systematic review and meta-analysis of pharmacological therapies for painful diabetic peripheral neuropathy. Pain Pract 2013.
49. Sowa N.A., Street S.E., Vihko P., Zylka M.J. Prostatic acid phosphatase reduces thermal sensitivity and chronic pain sensitization by depleting phosphatidylinositol 4,5-bisphosphate. J Neurosci 2010, 30:10282-10293.
50. Sowa N.A., Taylor-Blake B., Zylka M.J. Ecto-5'-nucleotidase (CD73) inhibits nociception by hydrolyzing AMP to adenosine in nociceptive circuits. J Neurosci 2010, 30:2235-2244.
51. 1-adenosine receptors to mediate antinociception. PloS One 2009, 4:e4248.
52. Sowa N.A., Voss M.K., Zylka M.J. Recombinant ecto-5'-nucleotidase (CD73) has long lasting antinociceptive effects that are dependent on adenosine A1 receptor activation. Mol Pain 2010, 6:20.
53. Spallone V., Lacerenza M., Rossi A., Sicuteri R., Marchettini P. Painful diabetic polyneuropathy: approach to diagnosis and management. Clin J Pain 2012, 28:726-743.
54. Street S.E., Walsh P.L., Sowa N.A., Taylor-Blake B., Guillot T.S., Vihko P., Wightman R.M., Zylka M.J. PAP and NT5E inhibit nociceptive neurotransmission by rapidly hydrolyzing nucleotides to adenosine. Mol Pain 2011, 7:80.
55. Taiwo Y.O., Levine J.D. Direct cutaneous hyperalgesia induced by adenosine. Neuroscience 1990, 38:757-762.
56. Taylor-Blake B., Zylka M.J. Prostatic acid phosphatase is expressed in peptidergic and nonpeptidergic nociceptive neurons of mice and rats. PloS One 2010, 5:e8674.
57. Tian L., Ji G., Wang C., Bai X., Lu Y., Xiong L. Excitatory synaptic transmission in the spinal substantia gelatinosa is under an inhibitory tone of endogenous adenosine. Neurosci Lett 2010, 477:28-32.
58. Ulugol A., Karadag H.C., Tamer M., FIrat Z., Aslantas A., Dokmeci I. Involvement of adenosine in the anti-antiallodynic effect of amitriptyline in streptozocin-induced diabetic rats. Neurosci Lett 2002, 328:129-132.
59. Van Belle T.L., Coppieters K.T., Von Herrath M.G. Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol Rev 2011, 91:79-118.
60. Veves A., Backonja M., Malik R.A. Painful diabetic neuropathy: epidemiology, natural history, early diagnosis, and treatment options. Pain Med 2008, 9:660-674.
61. Yegutkin G.G. Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochim Biophys Acta 2008, 1783:673-694.
62. 2a receptor agonist reduces hyperalgesia caused by a surgical incision in rats. Anesthesiology 2007, 107:797-806.
63. Ziegler D. Painful diabetic neuropathy: treatment and future aspects. Diabetes/metabolism research and reviews 2008, 24(suppl. 1):S52-S57.
64. Zimmermann H. New insights into molecular structure and function of ectonucleotidases in the nervous system. Neurochem Int 1998, 32:421-425.
65. Zochodne D.W. Diabetes mellitus and the peripheral nervous system: manifestations and mechanisms. Muscle Nerve 2007, 36:144-166.
66. Zylka M.J., Sowa N.A., Taylor-Blake B., Twomey M.A., Herrala A., Voikar V., Vihko P. Prostatic acid phosphatase is an ectonucleotidase and suppresses pain by generating adenosine. Neuron 2008, 60:111-122.