Identification of a vesicular ATP release inhibitor for the treatment of neuropathic and inflammatory pain

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 31, 2017, Pages E6297-E6305

  Kato, Yuri ^a,b   Hiasa, Miki ^b   Ichikawa, Reiko ^c   Hasuzawa, Nao ^d   Kadowaki, Atsushi ^b   Iwatsuki, Ken ^c,e   Shima, Kazuhiro ^f   Endo, Yasuo ^f   Kitahara, Yoshiro ^c   Inoue, Tsuyoshi ^b   Nomura, Masatoshi ^d   Omote, Hiroshi ^b   Moriyama, Yoshinori ^a,b,g   Miyaji, Takaaki ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c AJINOMOTO CO INC   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

^e TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^f TOHOKU UNIVERSITY   (Japan)

^g MATSUMOTO DENTAL UNIVERSITY   (Japan)

Author keywords

Analgesic effect; Antiinflammatory effect; Clodronate; Purinergic chemical transmission; Vesicular nucleotide transporter

Indexed keywords

ADENOSINE TRIPHOSPHATE; CARRIER PROTEIN; CHLORIDE ION; CLODRONIC ACID; DICLOFENAC; ETIDRONIC ACID; GABAPENTIN; HYDROCORTISONE; INTERLEUKIN 6; PARACETAMOL; PREDNISOLONE; PREGABALIN; TRAMADOL; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; VESICULAR NEUROTRANSMITTER TRANSPORTER; VESICULAR NUCLEOTIDE TRANSPORTER;

ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CHRONIC PAIN; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG MECHANISM; DRUG POTENCY; DRUG SELECTIVITY; HUMAN; HUMAN CELL; IC50; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY PAIN; MALE; MICROGLIA; MOUSE; NERVE CELL; NEUROPATHIC PAIN; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; PAW EDEMA; PRIORITY JOURNAL; VON FREY TEST;

EID: 85026674452     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1704847114     Document Type: Article

References (47)

1. Gold MS, Gebhart GF (2010) Nociceptor sensitization in pain pathogenesis. Nat Med 16:1248–1257.
2. Ren K, Dubner R (2010) Interactions between the immune and nervous systems in pain. Nat Med 16:1267–1276.
3. Dworkin RH, et al. (2003) Advances in neuropathic pain: Diagnosis, mechanisms, and treatment recommendations. Arch Neurol 60:1524–1534.
4. Tsuda M, Inoue K, Salter MW (2005) Neuropathic pain and spinal microglia: A big problem from molecules in “small” glia. Trends Neurosci 28:101–107.
5. Harirforoosh S, Asghar W, Jamali F (2013) Adverse effects of nonsteroidal antiinflammatory drugs: An update of gastrointestinal, cardiovascular and renal complications. J Pharm Pharm Sci 16:821–847.
6. Woolf CJ (2009) μ and δ opioid receptors diverge. Cell 137:987–988.
7. Porreca F, Ossipov MH (2009) Nausea and vomiting side effects with opioid analgesics during treatment of chronic pain: Mechanisms, implications, and management options. Pain Med 10:654–662.
8. Jensen TS, Madsen CS, Finnerup NB (2009) Pharmacology and treatment of neuropathic pains. Curr Opin Neurol 22:467–474.
9. Burnstock G (2008) Purinergic signalling and disorders of the central nervous system. Nat Rev Drug Discov 7:575–590.
10. Sawada K, et al. (2008) Identification of a vesicular nucleotide transporter. Proc Natl Acad Sci USA 105:5683–5686.
11. Miyaji T, Sawada K, Omote H, Moriyama Y (2011) Divalent cation transport by vesicular nucleotide transporter. J Biol Chem 286:42881–42887.
12. Sakamoto S, et al. (2014) Impairment of vesicular ATP release affects glucose metabolism and increases insulin sensitivity. Sci Rep 4:6689.
13. Masuda T, et al. (2016) Dorsal horn neurons release extracellular ATP in a VNUT-dependent manner that underlies neuropathic pain. Nat Commun 7:12529.
14. Nishida K, Nomura Y, Kawamori K, Moriyama Y, Nagasawa K (2014) Expression profile of vesicular nucleotide transporter (VNUT, SLC17A9) in subpopulations of rat dorsal root ganglion neurons. Neurosci Lett 579:75–79.
15. Jung J, Shin YH, Konishi H, Lee SJ, Kiyama H (2013) Possible ATP release through lysosomal exocytosis from primary sensory neurons. Biochem Biophys Res Commun 430: 488–493.
16. Brunner F, Schmid A, Kissling R, Held U, Bachmann LM (2009) Biphosphonates for the therapy of complex regional pain syndrome I–Systematic review. Eur J Pain 13:17–21.
17. Costa L, Major PP (2009) Effect of bisphosphonates on pain and quality of life in patients with bone metastases. Nat Clin Pract Oncol 6:163–174.
18. Kim S, et al. (2013) Analgesic effects of the non-nitrogen-containing bisphosphonates etidronate and clodronate, independent of anti-resorptive effects on bone. Eur J Pharmacol 699:14–22.
19. Rogers MJ, Crockett JC, Coxon FP, Mönkkönen J (2011) Biochemical and molecular mechanisms of action of bisphosphonates. Bone 49:34–41.
20. Pazianas M, Abrahamsen B (2011) Safety of bisphosphonates. Bone 49:103–110.
21. Muratore M, Quarta E, Grimaldi A, Calcagnile F, Quarta L (2011) Clinical utility of clodronate in the prevention and management of osteoporosis in patients intolerant of oral bisphosphonates. Drug Des Devel Ther 5:445–454.
22. Leviatan S, Sawada K, Moriyama Y, Nelson N (2010) Combinatorial method for over-expression of membrane proteins in Escherichia coli. J Biol Chem 285:23548–23556.
23. Juge N, et al. (2010) Metabolic control of vesicular glutamate transport and release. Neuron 68:99–112.
24. Hiasa M, et al. (2014) Essential role of vesicular nucleotide transporter in vesicular storage and release of nucleotides in platelets. Physiol Rep 2:e12034.
25. Larsson M, et al. (2012) Functional and anatomical identification of a vesicular transporter mediating neuronal ATP release. Cereb Cortex 22:1203–1214.
26. Oya M, et al. (2013) Vesicular nucleotide transporter is involved in ATP storage of secretory lysosomes in astrocytes. Biochem Biophys Res Commun 438:145–151.
27. Imura Y, et al. (2013) Microglia release ATP by exocytosis. Glia 61:1320–1330.
28. Shinozaki Y, et al. (2014) Microglia trigger astrocyte-mediated neuroprotection via purinergic gliotransmission. Sci Rep 4:4329.
29. Sahni M, Guenther HL, Fleisch H, Collin P, Martin TJ (1993) Bisphosphonates act on rat bone resorption through the mediation of osteoblasts. J Clin Invest 91:2004–2011.
30. Forster IC, Hernando N, Biber J, Murer H (2013) Phosphate transporters of the SLC20 and SLC34 families. Mol Aspects Med 34:386–395.
31. Marchand F, Perretti M, McMahon SB (2005) Role of the immune system in chronic pain. Nat Rev Neurosci 6:521–532.
32. Sakaki H, Tsukimoto M, Harada H, Moriyama Y, Kojima S (2013) Autocrine regulation of macrophage activation via exocytosis of ATP and activation of P2Y11 receptor. PLoS One 8:e59778.
33. Schäcke H, Döcke WD, Asadullah K (2002) Mechanisms involved in the side effects of glucocorticoids. Pharmacol Ther 96:23–43.
34. Rogers MJ, et al. (1996) Bisphosphonates induce apoptosis in mouse macrophage-like cells in vitro by a nitric oxide-independent mechanism. J Bone Miner Res 11: 1482–1491.
35. Kumamaru H, et al. (2012) Liposomal clodronate selectively eliminates microglia from primary astrocyte cultures. J Neuroinflammation 9:116.
36. Cao Q, et al. (2014) SLC17A9 protein functions as a lysosomal ATP transporter and regulates cell viability. J Biol Chem 289:23189–23199.
37. Miyaji T, et al. (2015) AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis. Nat Commun 6:5928.
38. Tokunaga A, Tsukimoto M, Harada H, Moriyama Y, Kojima S (2010) Involvement of SLC17A9-dependent vesicular exocytosis in the mechanism of ATP release during T cell activation. J Biol Chem 285:17406–17416.
39. Cekic C, Linden J (2016) Purinergic regulation of the immune system. Nat Rev Immunol 16:177–192.
40. Gerstein HC, et al.; Action to Control Cardiovascular Risk in Diabetes Study Group (2008) Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med 358: 2545–2559.
41. Xu ZZ, et al. (2010) Resolvins RvE1 and RvD1 attenuate inflammatory pain via central and peripheral actions. Nat Med 16:592–597.
42. Dixon WJ (1980) Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20:441–462.
43. Dominguez LJ, Di Bella G, Belvedere M, Barbagallo M (2011) Physiology of the aging bone and mechanisms of action of bisphosphonates. Biogerontology 12:397–408.
44. Kato Y, Omote H, Miyaji T (2013) Inhibitors of ATP release inhibit vesicular nucleotide transporter. Biol Pharm Bull 36:1688–1691.
45. Shimada-Shimizu N, Hisamitsu T, Nakamura TY, Wakabayashi S (2013) Evidence that Na+/H+ exchanger 1 is an ATP-binding protein. FEBS J 280:1430–1442.
46. Seltzer Z, Dubner R, Shir Y (1990) A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43:205–218.
47. Banker GA, Cowan WM (1977) Rat hippocampal neurons in dispersed cell culture. Brain Res 126:397–442.