Role of Adenosine Kinase in Sphingosine-1-Phosphate Receptor 1-Induced Mechano-Hypersensitivities.
Adenosine kinase
Adenosine receptor subtype 3
Mechano-hypersensitivities
Neuroinflammation
Sphingosine-1-phosphate receptor 1
Journal
Cellular and molecular neurobiology
ISSN: 1573-6830
Titre abrégé: Cell Mol Neurobiol
Pays: United States
ID NLM: 8200709
Informations de publication
Date de publication:
Nov 2022
Nov 2022
Historique:
received:
26
08
2021
accepted:
22
10
2021
pubmed:
14
11
2021
medline:
18
10
2022
entrez:
13
11
2021
Statut:
ppublish
Résumé
Emerging evidence implicates the sphingosine-1-phosphate receptor subtype 1 (S1PR1) in the development of neuropathic pain. Continued investigation of the signaling pathways downstream of S1PR1 are needed to support development of S1PR1 antagonists. In rodents, intrathecal (i.th.) injection of SEW2871, a selective S1PR1 agonist, activates the nod-like receptor family, pyrin domain containing 3 inflammasome, increases interleukin-1β (IL-1β) and causes behavioral hypersensitivity. I.th. injection of a IL-1β receptor antagonist blocks SEW2871-induced hypersensitivity, suggesting that IL-1β contributes to S1PR1's actions. Interestingly, previous studies have suggested that IL-1β increases the expression/activity of adenosine kinase (ADK), a key regulator of adenosine signaling at its receptors (ARs). Increased ADK expression reduces adenosine signaling whereas inhibiting ADK restores the action of adenosine. Here, we show that SEW287-induced behavioral hypersensitivity is associated with increased expression of ADK in astrocytes of the dorsal horn of the spinal cord. Moreover, the ADK inhibitor, ABT702, blocks SEW2871-induced hypersensitivity. These findings link ADK activation to S1PR1. If SEW2871-induced pain is mediated by IL-1β, which in turn activates ADK and leads to mechano-allodynia, then blocking ADK should attenuate IL-1β effects. In support of this idea, recombinant rat (rrIL-1β)-induced allodynia was blocked by at least 90% with ABT702, functionally linking ADK to IL-1β. Moreover, the selective A
Identifiants
pubmed: 34773542
doi: 10.1007/s10571-021-01162-8
pii: 10.1007/s10571-021-01162-8
pmc: PMC9098694
mid: NIHMS1759817
doi:
Substances chimiques
Inflammasomes
0
Interleukin-1beta
0
NLR Proteins
0
Oxadiazoles
0
S1PR1 protein, rat
0
SEW2871
0
Sphingosine-1-Phosphate Receptors
0
Thiophenes
0
Adenosine Kinase
EC 2.7.1.20
Adenosine
K72T3FS567
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2909-2918Subventions
Organisme : NIDA NIH HHS
ID : R01 DA043543
Pays : United States
Organisme : Saint Louis University
ID : Start Up Fund
Organisme : NIGMS NIH HHS
ID : T32 GM008306
Pays : United States
Organisme : NIH HHS
ID : T32GM008306-28
Pays : United States
Organisme : NIDA NIH HHS
ID : R01DA043543
Pays : United States
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Andrews NA, Latremoliere A, Basbaum AI, Mogil JS, Porreca F, Rice ASC, Woolf CJ, Currie GL, Dworkin RH, Eisenach JC, Evans S, Gewandter JS, Gover TD, Handwerker H, Huang W, Iyengar S, Jensen MP, Kennedy JD, Lee N, Levine J, Lidster K, Machin I, McDermott MP, McMahon SB, Price TJ, Ross SE, Scherrer G, Seal RP, Sena ES, Silva E, Stone L, Svensson CI, Turk DC, Whiteside G (2016) Ensuring transparency and minimization of methodologic bias in preclinical pain research: PPRECISE considerations. Pain 157(4):901–909. https://doi.org/10.1097/j.pain.0000000000000458
doi: 10.1097/j.pain.0000000000000458
pubmed: 26683237
Aronica E, Zurolo E, Iyer A, de Groot M, Anink J, Carbonell C, van Vliet EA, Baayen JC, Boison D, Gorter JA (2011) Upregulation of adenosine kinase in astrocytes in experimental and human temporal lobe epilepsy. Epilepsia 52(9):1645–1655. https://doi.org/10.1111/j.1528-1167.2011.03115.x
doi: 10.1111/j.1528-1167.2011.03115.x
pubmed: 21635241
pmcid: 3169746
Aronica E, Sandau US, Iyer A, Boison D (2013) Glial adenosine kinase—a neuropathological marker of the epileptic brain. Neurochem Int 63(7):688–695. https://doi.org/10.1016/j.neuint.2013.01.028
doi: 10.1016/j.neuint.2013.01.028
pubmed: 23385089
Bennett GJ, Xie YK (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33(1):87–107
doi: 10.1016/0304-3959(88)90209-6
Bigaud M, Guerini D, Billich A, Bassilana F, Brinkmann V (2014) Second generation S1P pathway modulators: research strategies and clinical developments. Biochim Biophys Acta 1841(5):745–758. https://doi.org/10.1016/j.bbalip.2013.11.001
doi: 10.1016/j.bbalip.2013.11.001
pubmed: 24239768
Boison D (2013) Adenosine kinase: exploitation for therapeutic gain. Pharmacol Rev 65(3):906–943. https://doi.org/10.1124/pr.112.006361
doi: 10.1124/pr.112.006361
pubmed: 23592612
pmcid: 3698936
Boison D, Chen JF, Fredholm BB (2010) Adenosine signaling and function in glial cells. Cell Death Differ 17(7):1071–1082. https://doi.org/10.1038/cdd.2009.131
doi: 10.1038/cdd.2009.131
pubmed: 19763139
Brinkmann V, Billich A, Baumruker T, Heining P, Schmouder R, Francis G, Aradhye S, Burtin P (2010) Fingolimod (FTY720): discovery and development of an oral drug to treat multiple sclerosis. Nat Rev Drug Discov 9(11):883–897. https://doi.org/10.1038/nrd3248
doi: 10.1038/nrd3248
pubmed: 21031003
Byers SL, Wiles MV, Dunn SL, Taft RA (2012) Mouse estrous cycle identification tool and images. PLoS ONE 7(4):e35538. https://doi.org/10.1371/journal.pone.0035538
doi: 10.1371/journal.pone.0035538
pubmed: 22514749
pmcid: 3325956
Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53(1):55–63
doi: 10.1016/0165-0270(94)90144-9
Chen Z, Doyle TM, Luongo L, Largent-Milnes TM, Giancotti LA, Kolar G, Squillace S, Boccella S, Walker JK, Pendleton A, Spiegel S, Neumann WL, Vanderah TW, Salvemini D (2019) Sphingosine-1-phosphate receptor 1 activation in astrocytes contributes to neuropathic pain. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.1820466116
doi: 10.1073/pnas.1820466116
pubmed: 31888991
pmcid: 6969507
Chua KC, Xiong C, Ho C, Mushiroda T, Jiang C, Mulkey F, Lai D, Schneider BP, Rashkin SR, Witte JS, Friedman PN, Ratain MJ, McLeod HL, Rugo HS, Shulman LN, Kubo M, Owzar K, Kroetz DL (2020) Genomewide meta-analysis validates a role for S1PR1 in microtubule targeting agent-induced sensory peripheral neuropathy. Clin Pharmacol Ther 108(3):625–634. https://doi.org/10.1002/cpt.1958
doi: 10.1002/cpt.1958
pubmed: 32562552
Dahlhamer J, Lucas J, Zelaya C, Nahin R, Mackey S, DeBar L, Kerns R, Von Korff M, Porter L, Helmick C (2018) Prevalence of chronic pain and high-impact chronic pain among adults—United States. Morb Mortal Wkly Rep 67(36):1001–1006. https://doi.org/10.15585/mmwr.mm6736a2
doi: 10.15585/mmwr.mm6736a2
Davis BK, Wen H, Ting JP (2011) The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol 29:707–735. https://doi.org/10.1146/annurev-immunol-031210-101405
doi: 10.1146/annurev-immunol-031210-101405
pubmed: 21219188
pmcid: 4067317
Dixon WJ (1980) Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20:441–462. https://doi.org/10.1146/annurev.pa.20.040180.002301
doi: 10.1146/annurev.pa.20.040180.002301
pubmed: 7387124
Doolen S, Iannitti T, Donahue RR, Shaw BC, Grachen CM, Taylor BK (2018) Fingolimod reduces neuropathic pain behaviors in a mouse model of multiple sclerosis by a sphingosine-1 phosphate receptor 1-dependent inhibition of central sensitization in the dorsal horn. Pain 159(2):224–238. https://doi.org/10.1097/j.pain.0000000000001106
doi: 10.1097/j.pain.0000000000001106
pubmed: 29140922
pmcid: 6287931
Doyle TM, Chen Z, Durante M, Salvemini D (2019) Activation of sphingosine-1-phosphate receptor 1 in the spinal cord produces mechanohypersensitivity through the activation of inflammasome and IL-1beta pathway. J Pain 20(8):956–964. https://doi.org/10.1016/j.jpain.2019.02.007
doi: 10.1016/j.jpain.2019.02.007
pubmed: 30802544
pmcid: 6933942
Doyle TM, Janes K, Chen Z, Grace PM, Esposito E, Cuzzocrea S, Largent-Milnes TM, Neumann WL, Watkins LR, Spiegel S, Vanderah TW, Salvemini D (2020a) Activation of sphingosine-1-phosphate receptor subtype 1 in the central nervous system contributes to morphine-induced hyperalgesia and antinociceptive tolerance in rodents. Pain. https://doi.org/10.1097/j.pain.0000000000001888
doi: 10.1097/j.pain.0000000000001888
pubmed: 32301840
pmcid: 7554181
Doyle TM, Largent-Milnes TM, Chen Z, Staikopoulos V, Esposito E, Dalgarno R, Fan C, Tosh DK, Cuzzocrea S, Jacobson KA, Trang T, Hutchinson MR, Bennett GJ, Vanderah TW, Salvemini D (2020b) Chronic morphine-induced changes in signaling at the A3 adenosine receptor contribute to morphine-induced hyperalgesia, tolerance, and withdrawal. J Pharmacol Exp Ther 374(2):331–341. https://doi.org/10.1124/jpet.120.000004
doi: 10.1124/jpet.120.000004
pubmed: 32434943
pmcid: 7372916
Franchi L, Eigenbrod T, Munoz-Planillo R, Nunez G (2009) The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol 10(3):241–247. https://doi.org/10.1038/ni.1703
doi: 10.1038/ni.1703
pubmed: 19221555
pmcid: 2820724
Fujii Y, Hirayama T, Ohtake H, Ono N, Inoue T, Sakurai T, Takayama T, Matsumoto K, Tsukahara N, Hidano S, Harima N, Nakazawa K, Igarashi Y, Goitsuka R (2012a) Amelioration of collagen-induced arthritis by a novel S1P1 antagonist with immunomodulatory activities. J Immunol 188(1):206–215. https://doi.org/10.4049/jimmunol.1101537
doi: 10.4049/jimmunol.1101537
pubmed: 22131329
Fujii Y, Ueda Y, Ohtake H, Ono N, Takayama T, Nakazawa K, Igarashi Y, Goitsuka R (2012b) Blocking S1P interaction with S1P(1) receptor by a novel competitive S1P(1)-selective antagonist inhibits angiogenesis. Biochem Biophys Res Commun 419(4):754–760. https://doi.org/10.1016/j.bbrc.2012.02.096
doi: 10.1016/j.bbrc.2012.02.096
pubmed: 22387544
Grenald SA, Doyle TM, Zhang H, Slosky LM, Chen Z, Largent-Milnes TM, Spiegel S, Vanderah TW, Salvemini D (2017) Targeting the S1P/S1PR1 axis mitigates cancer-induced bone pain and neuroinflammation. Pain 158(9):1733–1742. https://doi.org/10.1097/j.pain.0000000000000965
doi: 10.1097/j.pain.0000000000000965
pubmed: 28570482
pmcid: 5580091
Healy LM, Antel JP (2016) Sphingosine-1-Phosphate Receptors in the Central Nervous and Immune Systems. Curr Drug Targets 17(16):1841–1850. https://doi.org/10.2174/1389450116666151001112710
doi: 10.2174/1389450116666151001112710
pubmed: 26424391
Hylden JL, Wilcox GL (1980) Intrathecal morphine in mice: a new technique. Eur J Pharmacol 67(2–3):313–316. https://doi.org/10.1016/0014-2999(80)90515-4
doi: 10.1016/0014-2999(80)90515-4
pubmed: 6893963
Jacobson KA, Giancotti LA, Lauro F, Mufti F, Salvemini D (2020) Treatment of chronic neuropathic pain: purine receptor modulation. Pain. https://doi.org/10.1097/j.pain.0000000000001857
doi: 10.1097/j.pain.0000000000001857
pubmed: 32379223
pmcid: 8272921
Janes K, Little JW, Li C, Bryant L, Chen C, Chen Z, Kamocki K, Doyle T, Snider A, Esposito E, Cuzzocrea S, Bieberich E, Obeid L, Petrache I, Nicol G, Neumann WL, Salvemini D (2014) The development and maintenance of paclitaxel-induced neuropathic pain require activation of the sphingosine 1-phosphate receptor subtype 1. J Biol Chem 289(30):21082–21097. https://doi.org/10.1074/jbc.M114.569574
doi: 10.1074/jbc.M114.569574
pubmed: 24876379
pmcid: 4110312
Kim YK, Shin JS, Nahm MH (2016) NOD-like receptors in infection, immunity, and diseases. Yonsei Med J 57(1):5–14. https://doi.org/10.3349/ymj.2016.57.1.5
doi: 10.3349/ymj.2016.57.1.5
pubmed: 26632377
Kowaluk EA, Mikusa J, Wismer CT, Zhu CZ, Schweitzer E, Lynch JJ, Lee CH, Jiang M, Bhagwat SS, Gomtsyan A, McKie J, Cox BF, Polakowski J, Reinhart G, Williams M, Jarvis MF (2000) ABT-702 (4-amino-5-(3-bromophenyl)-7-(6-morpholino-pyridin- 3-yl)pyrido[2,3-d]pyrimidine), a novel orally effective adenosine kinase inhibitor with analgesic and anti-inflammatory properties. II. In vivo characterization in the rat. J Pharmacol Exp Ther 295(3):1165–1174
pubmed: 11082454
Little JW, Ford A, Symons-Liguori AM, Chen Z, Janes K, Doyle T, Xie J, Luongo L, Tosh DK, Maione S, Bannister K, Dickenson AH, Vanderah TW, Porreca F, Jacobson KA, Salvemini D (2015) Endogenous adenosine A3 receptor activation selectively alleviates persistent pain states. Brain 138(Pt 1):28–35. https://doi.org/10.1093/brain/awu330
doi: 10.1093/brain/awu330
pubmed: 25414036
Lopez-Castejon G, Brough D (2011) Understanding the mechanism of IL-1beta secretion. Cytokine Growth Factor Rev 22(4):189–195. https://doi.org/10.1016/j.cytogfr.2011.10.001
doi: 10.1016/j.cytogfr.2011.10.001
pubmed: 22019906
pmcid: 3714593
Muscoli C, Doyle T, Dagostino C, Bryant L, Chen Z, Watkins LR, Ryerse J, Bieberich E, Neumman W, Salvemini D (2010) Counter-regulation of opioid analgesia by glial-derived bioactive sphingolipids. J Neurosci 30(46):15400–15408. https://doi.org/10.1523/JNEUROSCI.2391-10.2010
doi: 10.1523/JNEUROSCI.2391-10.2010
pubmed: 21084596
pmcid: 3000610
Petucci C, Culver JA, Kapoor N, Sessions EH, Divlianska D, Gardell SJ (2019) Measurement of pyridine nucleotides in biological samples using LC-MS/MS. In: Bhattacharya SK (ed) Metabolomics, methods and protocols. Springer, New York, pp 61–73. https://doi.org/10.1007/978-1-4939-9488-5
doi: 10.1007/978-1-4939-9488-5
Ren K, Torres R (2009) Role of interleukin-1beta during pain and inflammation. Brain Res Rev 60(1):57–64. https://doi.org/10.1016/j.brainresrev.2008.12.020
doi: 10.1016/j.brainresrev.2008.12.020
pubmed: 19166877
Rossi S, Motta C, Studer V, Macchiarulo G, Volpe E, Barbieri F, Ruocco G, Buttari F, Finardi A, Mancino R, Weiss S, Battistini L, Martino G, Furlan R, Drulovic J, Centonze D (2014) Interleukin-1beta causes excitotoxic neurodegeneration and multiple sclerosis disease progression by activating the apoptotic protein p53. Mol Neurodegener 9:56. https://doi.org/10.1186/1750-1326-9-56
doi: 10.1186/1750-1326-9-56
pubmed: 25495224
pmcid: 4292815
Sanna MG, Liao J, Jo E, Alfonso C, Ahn MY, Peterson MS, Webb B, Lefebvre S, Chun J, Gray N, Rosen H (2004) Sphingosine 1-phosphate (S1P) receptor subtypes S1P1 and S1P3, respectively, regulate lymphocyte recirculation and heart rate. J Biol Chem 279(14):13839–13848. https://doi.org/10.1074/jbc.M311743200
doi: 10.1074/jbc.M311743200
pubmed: 14732717
Squillace S, Spiegel S, Salvemini D (2020) Targeting the sphingosine-1-phosphate axis for developing non-narcotic pain therapeutics. Trends Pharmacol Sci 41(11):851–867. https://doi.org/10.1016/j.tips.2020.09.006
doi: 10.1016/j.tips.2020.09.006
pubmed: 33010954
pmcid: 8491165
Stockstill K, Doyle TM, Yan X, Chen Z, Janes K, Little JW, Braden K, Lauro F, Giancotti LA, Harada CM, Yadav R, Xiao WH, Lionberger JM, Neumann WL, Bennett GJ, Weng HR, Spiegel S, Salvemini D (2018) Dysregulation of sphingolipid metabolism contributes to bortezomib-induced neuropathic pain. J Exp Med 215(5):1301–1313. https://doi.org/10.1084/jem.20170584
doi: 10.1084/jem.20170584
pubmed: 29703731
pmcid: 5940258
Stockstill K, Wahlman C, Braden K, Chen Z, Yosten GL, Tosh DK, Jacobson KA, Doyle TM, Samson WK, Salvemini D (2020) Sexually dimorphic therapeutic response in bortezomib-induced neuropathic pain reveals altered pain physiology in female rodents. Pain 161(1):177–184. https://doi.org/10.1097/j.pain.0000000000001697
doi: 10.1097/j.pain.0000000000001697
pubmed: 31490328
pmcid: 6923586
Tsuchiya K, Hara H (2014) The inflammasome and its regulation. Crit Rev Immunol 34(1):41–80. https://doi.org/10.1615/critrevimmunol.2013008686
doi: 10.1615/critrevimmunol.2013008686
pubmed: 24579701
Van Doorn R, Van Horssen J, Verzijl D, Witte M, Ronken E, Van Het Hof B, Lakeman K, Dijkstra CD, Van Der Valk P, Reijerkerk A, Alewijnse AE, Peters SL, De Vries HE (2010) Sphingosine 1-phosphate receptor 1 and 3 are upregulated in multiple sclerosis lesions. Glia 58(12):1465–1476. https://doi.org/10.1002/glia.21021
doi: 10.1002/glia.21021
pubmed: 20648639
Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, Binaglia M, Corsini E, Di Luca M, Galli CL, Marinovich M (2003) Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 23(25):8692–8700
doi: 10.1523/JNEUROSCI.23-25-08692.2003
Voet S, Srinivasan S, Lamkanfi M, van Loo G (2019) Inflammasomes in neuroinflammatory and neurodegenerative diseases. EMBO Mol Med 11(6):e10248. https://doi.org/10.15252/emmm.201810248
doi: 10.15252/emmm.201810248
pubmed: 31015277
pmcid: 6554670
Wahlman C, Doyle TM, Little JW, Luongo L, Janes K, Chen Z, Esposito E, Tosh DK, Cuzzocrea S, Jacobson KA, Salvemini D (2018) Chemotherapy-induced pain is promoted by enhanced spinal adenosine kinase levels through astrocyte-dependent mechanisms. Pain 159(6):1025–1034. https://doi.org/10.1097/j.pain.0000000000001177
doi: 10.1097/j.pain.0000000000001177
pubmed: 29419652
pmcid: 5955834
Walsh JG, Muruve DA, Power C (2014) Inflammasomes in the CNS. Nat Rev Neurosci 15(2):84–97. https://doi.org/10.1038/nrn3638
doi: 10.1038/nrn3638
pubmed: 24399084