Phosphodiesterase 2A localized in the spinal cord contributes to inflammatory pain processing

Anesthesiology

Volumn 121, Issue 2, 2014, Pages 372-382

  Kallenborn Gerhardt, Wiebke ^a   Lu, Ruirui ^a   Bothe, Aaron ^a,c   Thomas, Dominique ^a   Schlaudraff, Jessica ^b   Lorenz, Jana E ^a   Lippold, Nancy ^a   Real, Catherine I ^a   Ferreirós, Nerea ^a   Geisslinger, Gerd ^a   Del Turco, Domenico ^b   Schmidtko, Achim ^a  

^a UNIVERSITY OF WITTEN HERDECKE   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BAY 607550; CYCLIC AMP; CYCLIC GMP; ESTERASE; MESSENGER RNA; PHOSPHODIESTERASE 2A; PHOSPHODIESTERASE 2A INHIBITOR; PHOSPHODIESTERASE INHIBITOR; UNCLASSIFIED DRUG; ZYMOSAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; HYPERSENSITIVITY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INFLAMMATORY PAIN; LASER MICRODISSECTION; LIQUID CHROMATOGRAPHY; MALE; MOUSE; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD DORSAL HORN; TANDEM MASS SPECTROMETRY; ZYMOSAN INDUCED HYPERSENTIVITY;

ANIMALS; BEHAVIOR, ANIMAL; CYCLIC AMP; CYCLIC GMP; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 2; DRUG HYPERSENSITIVITY; IMIDAZOLES; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INJECTIONS, SPINAL; MALE; MICE; MICE, INBRED C57BL; MICRODISSECTION; NEURALGIA; PAIN; PAIN MEASUREMENT; PHOSPHODIESTERASE INHIBITORS; POSTERIOR HORN CELLS; REAL-TIME POLYMERASE CHAIN REACTION; SPINAL CORD; TRIAZINES; UP-REGULATION; ZYMOSAN;

EID: 84905050115     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0000000000000270     Document Type: Article

References (51)

1. Basbaum AI, Bautista DM, Scherrer G, Julius D: Cellular and molecular mechanisms of pain. Cell 2009; 139:267-84
2. Malmberg AB, Brandon EP, Idzerda RL, Liu H, McKnight GS, Basbaum AI: Diminished inflammation and nociceptive pain with preservation of neuropathic pain in mice with a targeted mutation of the type I regulatory subunit of cAMPdependent protein kinase. J Neurosci 1997; 17:7462-70
3. Aley KO, Levine JD: Role of protein kinase A in the maintenance of inflammatory pain. J Neurosci 1999; 19:2181-6
4. Ahmadi S, Lippross S, Neuhuber WL, Zeilhofer HU: PGE(2) selectively blocks inhibitory glycinergic neurotransmission onto rat superficial dorsal horn neurons. Nat Neurosci 2002; 5:34-40
5. Bhave G, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW IV: cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 2002; 35:721-31
6. Hucho TB, Dina OA, Levine JD: Epac mediates a cAMP-to-PKC signaling in inflammatory pain: An isolectin B4(+) neuron-specific mechanism. J Neurosci 2005; 25:6119-26
7. Eijkelkamp N, Linley JE, Torres JM, Bee L, Dickenson AH, Gringhuis M, Minett MS, Hong GS, Lee E, Oh U, Ishikawa Y, Zwartkuis FJ, Cox JJ, Wood JN: A role for Piezo2 in EPAC1-dependent mechanical allodynia. Nat Commun 2013; 4:1682
8. Tao YX, Johns RA: Activation of cGMP-dependent protein kinase Iα is required for N-methyl-D-aspartate-or nitric oxide-produced spinal thermal hyperalgesia. Eur J Pharmacol 2000; 392:141-5
9. Tegeder I, Del Turco D, Schmidtko A, Sausbier M, Feil R, Hofmann F, Deller T, Ruth P, Geisslinger G: Reduced inflammatory hyperalgesia with preservation of acute thermal nociception in mice lacking cGMP-dependent protein kinase I. Proc Natl Acad Sci U S A 2004; 101:3253-7
10. Schmidtko A, Ruth P, Geisslinger G, Tegeder I: Inhibition of cyclic guanosine 5-monophosphate-dependent protein kinase I (PKG-I) in lumbar spinal cord reduces formalin-induced hyperalgesia and PKG upregulation. Nitric Oxide 2003; 8:89-94
11. Luo C, Gangadharan V, Bali KK, Xie RG, Agarwal N, Kurejova M, Tappe-Theodor A, Tegeder I, Feil S, Lewin G, Polgar E, Todd AJ, Schlossmann J, Hofmann F, Liu DL, Hu SJ, Feil R, Kuner T, Kuner R: Presynaptically localized cyclic GMPdependent protein kinase 1 is a key determinant of spinal synaptic potentiation and pain hypersensitivity. PLoS Biol 2012; 10:e1001283
12. Heine S, Michalakis S, Kallenborn-Gerhardt W, Lu R, Lim HY, Weiland J, Del Turco D, Deller T, Tegeder I, Biel M, Geisslinger G, Schmidtko A: CNGA3: A target of spinal nitric oxide/cGMP signaling and modulator of inflammatory pain hypersensitivity. J Neurosci 2011; 31:11184-92
13. Emery EC, Young GT, Berrocoso EM, Chen L, McNaughton PA: HCN2 ion channels play a central role in inflammatory and neuropathic pain. Science 2011; 333:1462-6
14. Schmidtko A, Tegeder I, Geisslinger G: No NO, no pain? The role of nitric oxide and cGMP in spinal pain processing. Trends Neurosci 2009; 32:339-46
15. Pierre S, Eschenhagen T, Geisslinger G, Scholich K: Capturing adenylyl cyclases as potential drug targets. Nat Rev Drug Discov 2009; 8:321-35
16. Francis SH, Blount MA, Corbin JD: Mammalian cyclic nucleotide phosphodiesterases: Molecular mechanisms and physiological functions. Physiol Rev 2011; 91:651-90
17. Stephenson DT, Coskran TM, Kelly MP, Kleiman RJ, Morton D, ONeill SM, Schmidt CJ, Weinberg RJ, Menniti FS: The distribution of phosphodiesterase 2A in the rat brain. Neuroscience 2012; 226:145-55
18. Bender AT, Beavo JA: Cyclic nucleotide phosphodiesterases: Molecular regulation to clinical use. Pharmacol Rev 2006; 58:488-520
19. Boess FG, Hendrix M, van der Staay FJ, Erb C, Schreiber R, van Staveren W, de Vente J, Prickaerts J, Blokland A, Koenig G: Inhibition of phosphodiesterase 2 increases neuronal cGMP, synaptic plasticity and memory performance. Neuropharmacology 2004; 47:1081-92
20. Hunskaar S, Fasmer OB, Hole K: Formalin test in mice, a useful technique for evaluating mild analgesics. J Neurosci Methods 1985; 14:69-76
21. Kallenborn-Gerhardt W, Schröder K, Del Turco D, Lu R, Kynast K, Kosowski J, Niederberger E, Shah AM, Brandes RP, Geisslinger G, Schmidtko A: NADPH oxidase-4 maintains neuropathic pain after peripheral nerve injury. J Neurosci 2012; 32:10136-45
22. Lu R, Schmidtko A: Direct intrathecal drug delivery in mice for detecting in vivo effects of cGMP on pain processing. Methods Mol Biol 2013; 1020:215-21
23. Decosterd I, Woolf CJ: Spared nerve injury: An animal model of persistent peripheral neuropathic pain. Pain 2000; 87:149-58
24. Schnell SA, Staines WA, Wessendorf MW: Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J Histochem Cytochem 1999; 47:719-30
25. Schmidtko A, Gao W, Sausbier M, Rauhmeier I, Sausbier U, Niederberger E, Scholich K, Huber A, Neuhuber W, Allescher HD, Hofmann F, Tegeder I, Ruth P, Geisslinger G: Cysteinerich protein 2, a novel downstream effector of cGMP/cGMPdependent protein kinase I-mediated persistent inflammatory pain. J Neurosci 2008; 28:1320-30
26. Taqatqeh F, Mergia E, Neitz A, Eysel UT, Koesling D, Mittmann T: More than a retrograde messenger: Nitric oxide needs two cGMP pathways to induce hippocampal long-term potentiation. J Neurosci 2009; 29:9344-50
27. Vardeh D, Wang D, Costigan M, Lazarus M, Saper CB, Woolf CJ, Fitzgerald GA, Samad TA: COX2 in CNS neural cells mediates mechanical inflammatory pain hypersensitivity in mice. J Clin Invest 2009; 119:287-94
28. Masood A, Huang Y, Hajjhussein H, Xiao L, Li H, Wang W, Hamza A, Zhan CG, ODonnell JM: Anxiolytic effects of phosphodiesterase-2 inhibitors associated with increased cGMP signaling. J Pharmacol Exp Ther 2009; 331:690-9
29. Rodefer JS, Saland SK, Eckrich SJ: Selective phosphodiesterase inhibitors improve performance on the ED/ID cognitive task in rats. Neuropharmacology 2012; 62:1182-90
30. Meller ST, Gebhart GF: Intraplantar zymosan as a reliable, quantifiable model of thermal and mechanical hyperalgesia in the rat. Eur J Pain 1997; 1:43-52
31. Schmidtko A, Gao W, König P, Heine S, Motterlini R, Ruth P, Schlossmann J, Koesling D, Niederberger E, Tegeder I, Friebe A, Geisslinger G: cGMP produced by NO-sensitive guanylyl cyclase essentially contributes to inflammatory and neuropathic pain by using targets different from cGMP-dependent protein kinase I. J Neurosci 2008; 28:8568-76
32. Stephenson DT, Coskran TM, Wilhelms MB, Adamowicz WO, ODonnell MM, Muravnick KB, Menniti FS, Kleiman RJ, Morton D: Immunohistochemical localization of phosphodiesterase 2A in multiple mammalian species. J Histochem Cytochem 2009; 57:933-49
33. van Donkelaar EL, Rutten K, Blokland A, Akkerman S, Steinbusch HW, Prickaerts J: Phosphodiesterase 2 and 5 inhibition attenuates the object memory deficit induced by acute tryptophan depletion. Eur J Pharmacol 2008; 600:98-104
34. Rutten K, Van Donkelaar EL, Ferrington L, Blokland A, Bollen E, Steinbusch HW, Kelly PA, Prickaerts JH: Phosphodiesterase inhibitors enhance object memory independent of cerebral blood flow and glucose utilization in rats. Neuropsychopharmacology 2009; 34:1914-25
35. Schmidt CJ: Phosphodiesterase inhibitors as potential cognition enhancing agents. Curr Top Med Chem 2010; 10:222-30
36. Fischmeister R, Castro LR, Abi-Gerges A, Rochais F, Jurevicius J, Leroy J, Vandecasteele G: Compartmentation of cyclic nucleotide signaling in the heart: The role of cyclic nucleotide phosphodiesterases. Circ Res 2006; 99:816-28
37. Mika D, Leroy J, Vandecasteele G, Fischmeister R: PDEs create local domains of cAMP signaling. J Mol Cell Cardiol 2012; 52:323-9
38. Seybold J, Thomas D, Witzenrath M, Boral S, Hocke AC, B?rger A, Hatzelmann A, Tenor H, Schudt C, Kr?ll M, Sch?tte H, Hippenstiel S, Suttorp N: Tumor necrosis factor-α-dependent expression of phosphodiesterase 2: Role in endothelial hyperpermeability. Blood 2005; 105:3569-76
39. Surapisitchat J, Jeon KI, Yan C, Beavo JA: Differential regulation of endothelial cell permeability by cGMP via phosphodiesterases 2 and 3. Circ Res 2007; 101:811-8
40. Diebold I, Djordjevic T, Petry A, Hatzelmann A, Tenor H, Hess J, Görlach A: Phosphodiesterase 2 mediates redox-sensitive endothelial cell proliferation and angiogenesis by thrombin via Rac1 and NADPH oxidase 2. Circ Res 2009; 104:1169-77
41. Gresele P, Momi S, Falcinelli E: Anti-platelet therapy: Phosphodiesterase inhibitors. Br J Clin Pharmacol 2011; 72:634-46
42. MacFarland RT, Zelus BD, Beavo JA: High concentrations of a cGMP-stimulated phosphodiesterase mediate ANP-induced decreases in cAMP and steroidogenesis in adrenal glomerulosa cells. J Biol Chem 1991; 266:136-42
43. Nikolaev VO, Gambaryan S, Engelhardt S, Walter U, Lohse MJ: Real-time monitoring of the PDE2 activity of live cells: Hormone-stimulated cAMP hydrolysis is faster than hormonestimulated cAMP synthesis. J Biol Chem 2005; 280:1716-9
44. Shi X, Li X, Clark JD: Formalin injection causes a coordinated spinal cord CO/NO-cGMP signaling system response. Mol Pain 2005; 1:33
45. Witwicka H, Kobia?ka M, Siednienko J, Mitkiewicz M, Gorczyca WA: Expression and activity of cGMP-dependent phosphodiesterases is up-regulated by lipopolysaccharide (LPS) in rat peritoneal macrophages. Biochim Biophys Acta 2007; 1773:209-18
46. Kallenborn-Gerhardt W, Lu R, Syhr KM, Heidler J, von Melchner H, Geisslinger G, Bangsow T, Schmidtko A: Antioxidant activity of sestrin 2 controls neuropathic pain after peripheral nerve injury. Antioxid Redox Signal 2013; 19:2013-23
47. Xu Q, Yaksh TL: A brief comparison of the pathophysiology of inflammatory versus neuropathic pain. Curr Opin Anaesthesiol 2011; 24:400-7
48. Ellis A, Bennett DL: Neuroinflammation and the generation of neuropathic pain. Br J Anaesth 2013; 111:26-37
49. Plummer MS, Cornicelli J, Roark H, Skalitzky DJ, Stankovic CJ, Bove S, Pandit J, Goodman A, Hicks J, Shahripour A, Beidler D, Lu XK, Sanchez B, Whitehead C, Sarver R, Braden T, Gowan R, Shen XQ, Welch K, Ogden A, Sadagopan N, Baum H, Miller H, Banotai C, Spessard C, Lightle S: Discovery of potent selective bioavailable phosphodiesterase 2 (PDE2) inhibitors active in an osteoarthritis pain model. Part II: Optimization studies and demonstration of in vivo efficacy. Bioorg Med Chem Lett 2013; 23:3443-7
50. Sierksma AS, Rutten K, Sydlik S, Rostamian S, Steinbusch HW, van den Hove DL, Prickaerts J: Chronic phosphodiesterase type 2 inhibition improves memory in the APPswe/PS1dE9 mouse model of Alzheimers disease. Neuropharmacology 2013; 64:124-36
51. Reneerkens OA, Rutten K, Bollen E, Hage T, Blokland A, Steinbusch HW, Prickaerts J: Inhibition of phoshodiesterase type 2 or type 10 reverses object memory deficits induced by scopolamine or MK-801. Behav Brain Res 2013; 236:16-22