Microglial cathepsin B contributes to the initiation of peripheral inflammation-induced chronic pain

Journal of Neuroscience

Volumn 32, Issue 33, 2012, Pages 11330-11342

  Sun, Li ^a   Wu, Zhou ^a   Hayashi, Yoshinori ^a   Peters, Christoph ^b   Tsuda, Makoto ^a   Inoue, Kazuhide ^a,c   Nakanishi, Hiroshi ^a,c  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF FREIBURG   (Germany)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN B; CD11B ANTIGEN; CD4 ANTIGEN; CRYOPYRIN; CYCLOOXYGENASE 2; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NEURON SPECIFIC NUCLEAR PROTEIN;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC PAIN; CONTROLLED STUDY; HYPERALGESIA; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INFLAMMATORY PAIN; LYSOSOME; MALE; MICROGLIA; MOTOR ACTIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADENOSINE TRIPHOSPHATE; AMINO ACID CHLOROMETHYL KETONES; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD4; CALCIUM-BINDING PROTEINS; CARRIER PROTEINS; CATHEPSIN B; CELLS, CULTURED; CHROMOGRANIN A; CHRONIC PAIN; CYCLOOXYGENASE 2; DIPEPTIDES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; FREUND'S ADJUVANT; FUNCTIONAL LATERALITY; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; HYPERALGESIA; INFLAMMATION; INTERLEUKIN-18; INTERLEUKIN-1BETA; LYSOPHOSPHOLIPIDS; LYSOSOMES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MICROGLIA; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; PAIN THRESHOLD; RNA, SMALL INTERFERING; SPINAL CORD; TRANSFECTION;

EID: 84865013141     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0677-12.2012     Document Type: Article

References (59)

1. Broom DC, Samad TA, Kohno T, Tegeder I, Geisslinger G, Woolf CJ (2004) Cyclooxygenase 2 expression in the spared nerve injury model of neuropathic pain. Neuroscience 124:891-900.
2. Cardona A, Saalfeld S, Arganda I, Pereanu W, Schindelin J, Hartenstein V (2010) Identifying neuronal lineages of Drosophila by sequence analysis of axon tracts. J Neurosci 30:7538-7553.
3. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63.
4. Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, De Koninck Y (2005) BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438:1017-1021.
5. Di Comite G, Rossi CM, Marinosci A, Lolmede K, Baldissera E, Aiello P, Mueller RB, Herrmann M, Voll RE, Rovere-Querini P, Sabbadini MG, Corti A, Manfredi AA (2009) Circulating chromogranin A reveals extraarticular involvement in patients with rheumatoid arthritis and curbs TNF--elicited endothelial activation. J Leukoc Biol 85:81-87.
6. Dinarello CA (1998) Interleukin-1, interleukin-18, and the interleukin-1 converting enzyme. Ann N Y Acad Sci 856:1-11.
7. Donnelly-Roberts DL, Jarvis MF (2007) Discovery of P2X7 receptor-selective antagonists offers new insights into P2X7 receptor function and indicates a role in chronic pain states. Br J Pharmacol 151:571-579.
8. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, Bauernfeind FG, Abela GS, Franchi L, Nuñez G, Schnurr M, Espevik T, Lien E, Fitzgerald KA, Rock KL, Moore KJ, Wright SD, Hornung V, Latz E (2010) NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464:1357-1361.
9. Fantuzzi G, Dinarello CA (1999) Interleukin-18 and interleukin-1: two cytokine substrates for ICE (caspase-1). J Clin Immunol 19:1-11.
10. Fiorentino PM, Tallents RH, Miller JN, Brouxhon SM, O'Banion MK, Puzas JE, Kyrkanides S (2008) Spinal interleukin-1 in a mouse model of arthritis and joint pain. Arthritis Rheum 58:3100-3109.
11. Fujita R, Ma Y, Ueda H (2008) Lysophosphatidic acid-induced membrane ruffling and brain-derived neurotrophic factor gene expression are mediated by ATP release in primary microglia. J Neurochem 107:152-160.
12. Funk CD, FitzGerald GA (2007) COX-2 inhibitors and cardiovascular risk. J Cardiovasc Pharmacol 50:470-479.
13. Guo W, Wang H, Watanabe M, Shimizu K, Zou S, LaGraize SC, Wei F, Dubner R, Ren K (2007) Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain. J Neurosci 27:6006-6018.
14. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG, Reinheckel T, Fitzgerald KA, Latz E, Moore KJ, Golenbock DT (2008) The NALP3 inflammasome is involved in the innate immune response to amyloid-Nat Immunol 9:857-865.
15. Hargreaves K, Dubner R, Brown F, Flores C, Joris J (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88.
16. Hayashi Y, Yoshida M, Yamato M, Ide T, Wu Z, Ochi-Shindou M, Kanki T, Kang D, Sunagawa K, Tsutsui H, Nakanishi H (2008) Reverse of age dependent memory impairment and mitochondrial DNA damage in microglia by an overexpression of human mitochondrial transcription factor A in mice. J Neurosci 28:8624-8634.
17. 2-activated K channels are possible molecular targets for the analgesic effects of S-ketamine on neuropathic pain. J Neurosci 31:17370-17382.
18. Hentze H, Lin XY, Choi MS, Porter AG (2003) Critical role for cathepsin B in mediating caspase-1-dependent interleukin-18 maturation and caspase-1 independent necrosis triggered by the microbial toxin nigericin. Cell Death Differ 10:956-968.
19. Hooper C, Fry VA, Sevastou IG, Pocock JM (2009) Scavenger receptor control of chromogranin A-induced microglial stress and neurotoxic cascades. FEBS Lett 583:3461-3466.
20. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, Fitzgerald KA, Latz E (2008) Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9:847-856.
21. Hua XY, Svensson CI, Matsui T, Fitzsimmons B, Yaksh TL, Webb M (2005) Intrathecal minocycline attenuates peripheral inflammation-induced hyperalgesia by inhibiting p38 MAPK in spinal microglia. Eur J Neurosci 22:2431-2440.
22. Inoue M, Rashid MH, Fujita R, Contos JJ, Chun J, Ueda H (2004) Initiation of neuropathic pain requires lysophosphatidic acid receptor signaling. Nat Med 10:712-718.
23. Jarvis MF (2010) The neural-glial purinergic receptor ensemble in chronic pain states. Trends Neurosci 33:48-57.
24. Kang SJ, Wang S, Hara H, Peterson EP, Namura S, Amin-Hanjani S, Huang Z, Srinivasan A, Tomaselli KJ, Thornberry NA, Moskowitz MA, Yuan J (2000) Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions. J Cell Biol 149:613-622.
25. Kanno T, Yaguchi T, Nishizaki T (2010) Noradrenaline stimulates ATP release from DRG neurons by targeting 3 adrenoceptors as a factor of neuropathic pain. J Cell Physiol 224:345-351.
26. Kawasaki Y, Xu ZZ, Wang X, Park JY, Zhuang ZY, Tan PH, Gao YJ, Roy K, Corfas G, Lo EH, Ji RR (2008) Distinct roles of matrix metalloproteases in the early and late-phase development of neuropathic pain. Nat Med 14:331-336.
27. Kingham PJ, Cuzner ML, Pocock JM (1999) Apoptotic pathway mobilized in microglia and neurones as a consequence of chromogranin A-induced microglial activation. J Neurochem 73:538-547.
28. Koike M, Shibata M, Ohsawa Y, Nakanishi H, Koga T, Kametaka S, Waguri S, Momoi T, Kominami E, Peters C, Figura K, Saftig P, Uchiyama Y (2003) Involvement of two different cell death pathways in retinal atrophy of cathepsin D-deficient mice. Mol Cell Neurosci 22:146-1461.
29. Lee KM, Kang BS, Lee HL, Son SJ, Hwang SH, Kim DS, Park JS, Cho HJ (2004) Spinal NFB activation induces COX-2 upregulation and contributes to inflammatory pain hypersensitivity. Eur J Neurosci 19:3375-3381.
30. Mangoni AA, Woodman RJ, Gaganis P, Gilbert AL, Knights KM (2010) Use of non-steroidal anti-inflammatory drugs and risk of incident myocardial infarction and heart failure, and all-cause mortality in the Australian veteran community. Br J Clin Pharmacol 69:689-700.
31. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, Roose-Girma M, Lee WP, Weinrauch Y, Monack DM, Dixit VM (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440:228-232.
32. Matsuka Y, Ono T, Iwase H, Mitrirattanakul S, Omoto KS, Cho T, Lam YY, Snyder B, Spigelman I (2008) Altered ATP release and metabolism in dorsal root ganglia of neuropathic rats. Mol Pain 4:66.
33. Miyoshi K, Obata K, Kondo T, Okamura H, Noguchi K (2008) Interleukin-18-mediated microglia/astrocyte interaction in the spinal cord enhances neuropathic pain processing after nerve injury. J Neurosci 28:12775-12787.
34. Nakamichi K, Saiki M, Kitani H, Kuboyama Y, Morimoto K, Takayama-Ito M, Kurane I (2006) Suppressive effect of simvastatin on interferon-induced expression of CC chemokine ligand 5 in microglia. Neurosci Lett 407:205-210.
35. Raghavendra V, Tanga FY, DeLeo JA (2004) Complete Freunds adjuvant induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. Eur J Neurosci 20:467-473.
36. Ren K, Torres R (2009) Role of interleukin-1 during pain and inflammation. Brain Res Rev 60:57-64.
37. Rigaud M, Gemes G, Barabas ME, Chernoff DI, Abram SE, Stucky CL, Hogan QH (2008) Species and strain differences in rodent sciatic nerve anatomy: implications for studies of neuropathic pain. Pain 136:188-201.
38. Samad TA, Moore KA, Sapirstein A, Billet S, Allchorne A, Poole S, Bonventre JV, Woolf CJ (2001) Interleukin-1-mediated induction of COX-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410:471-475.
39. Sastradipura DF, Nakanishi H, Tsukuba T, Nishishita K, Sakai H, Kato Y, Gotow T, Uchiyama Y, Yamamoto K (1998) Identification of cellular compartments involved in processing of cathepsin E in primary cultures of rat microglia. J Neurochem 70:2045-2056.
40. Scholz J, Woolf CJ (2007) The neuropathic pain triad: Neurons, immune cells and glia. Nat Neurosci 10:1361-1368.
41. Schotte P, Van Criekinge W, Van de Craen M, Van Loo G, Desmedt M, Grooten J, Cornelissen M, De Ridder L, Vandekerckhove J, Fiers W, Vandenabeele P, Beyaert R (1998) Cathepsin B-mediated activation of the proinflammatory caspase-11. Biochem Biophys Res Commun 251:379-387.
42. Shan S, Qi-Liang MY, Hong C, Tingting L, Mei H, Haili P, Yan-Qing W, Zhi-Qi Z, Yu-Qiu Z (2007) Is functional state of spinal microglia involved in the anti-allodynic and anti-hyperalgesic effects of electroacupuncture in rat model of monoarthritis? Neurobiol Dis 26:558-568.
43. Stutz A, Golenbock DT, Latz E (2009) Inflammasomes: too big to miss. J Clin Invest 119:3502-3511.
44. Sun L, Wu Z, Baba M, Peters C, Uchiyama Y, Nakanishi H (2010) Cathepsin B-dependent motor neuron death after nerve injury in the adult mouse. Biochem Biophys Res Commun 399:391-395.
45. Suter MR, Wen YR, Decosterd I, Ji RR (2007) Do glial cells control pain? Neuron Glia Biol 3:255-268.
46. Svensson CI, Marsala M, Westerlund A, Calcutt NA, Campana WM, Freshwater JD, Catalano R, Feng Y, Protter AA, Scott B, Yaksh TL (2003) Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing. J Neurochem 86:1534-1544.
47. Sweitzer S, Martin D, DeLeo JA (2001) Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibits an anti-allodynic action in a rat model of neuropathic pain. Neuroscience 103:529-539.
48. 2 influx and pore formation induced by the activation of P2X7 nucleotide receptors on mouse microglial cell line. Biochim Biophys Acta 1726:177-186.
49. Terada K, Yamada J, Hayashi Y, Wu Z, Uchiyama Y, Peters C, Nakanishi H (2010) Involvement of cathepsin B in the processing and secretion of interleukin-1 in chromogranin A-stimulated microglia. Glia 58:114-124.
50. Thiele DL, Lipsky PE (1985) Regulation of cellular function by products of lysosomal enzyme activity: elimination of human natural killer cells by a dipeptide methyl ester generated from L-leucine methyl ester by monocytes or polymorphonuclear leukocytes. Proc Natl Acad Sci U S A 82:2468-2472.
51. Thiele DL, Lipsky PE (1990) Mechanism of L-leucyl-L-leucine methyl estermediated killing of cytotoxic lymphocytes: dependence on a lysosomal thiol protease, dipeptidyl peptidase I, that is enriched in these cells. Proc Natl Acad Sci U S A 87:83-87.
52. Triantafyllou K, Vlachogiannakos J, Ladas SD (2010) Gastrointestinal and liver side effects of drugs in elderly patients. Best Pract Res Clin Gastro-enterol 24:203-215.
53. Tschopp J, Schroder K (2010) NLRP3 inflammasome activation: the convergence of multiple signaling pathways on ROS production? Nat Rev Immunol 10:210-215.
54. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K (2003) P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424:778-783.
55. Tsuda M, Inoue K, Salter MW (2005) Neuropathic pain and spinal microglia: a big program from molecules in "small" glia. Trends Neurosci 28:101-107.
56. Vancompernolle K, Van Herreweghe F, Pynaert G, Van de Craen M, De Vos K, Totty N, Sterling A, Fiers W, Vandenabeele P, Grooten J (1998) Atractyloside-induced release of cathepsin B, a protease with caspaseprocessing activity. FEBS Lett 438:150-158.
57. Vardeh D, Wang D, Costigan M, Lazarus M, Saper CB, Woolf CJ, Fitzgerald GA, Samad TA (2009) COX2 in CNS neural cells mediates mechanical inflammatory pain hypersensitivity in mice. J Clin Invest 119:287-294.
58. Verri WA Jr, Cunha TM, Parada CA, Poole S, Liew FY, Ferreira SH, Cunha FQ (2007) Antigen-induced inflammatory mechanical hypernociception in mice is mediated by IL-18. Brain Behav Immun 21:535-543.
59. Watkins LR, Milligan ED, Maier SF (2001) Glial activation: a driving force for pathological pain. Trends Neurosci 24:450-455.