Extracellular matrix proteoglycan plays a pivotal role in sensitization by low pH of mechanosensitive currents in nociceptive sensory neurones

Journal of Physiology

Volumn 590, Issue 13, 2012, Pages 2995-3007

  Kubo, Asako ^a   Katanosaka, Kimiaki ^a   Mizumura, Kazue ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; AMILORIDE; CALCIUM; CAPSAZEPINE; CHONDROITIN ABC LYASE; ISOLECTIN B4; PROTEOGLYCAN; STAUROSPORINE; VERSICAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL INTERACTION; CELL LABELING; CELL SURFACE; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; EXTRACELLULAR MATRIX; FEMALE; NOCICEPTION; NONHUMAN; PATCH CLAMP; PH; PRIORITY JOURNAL; PROTEIN BINDING; RAT; SENSITIZATION; SENSORY NERVE CELL; SENSORY SYSTEM ELECTROPHYSIOLOGY; SIGNAL TRANSDUCTION; SPINAL GANGLION; WHOLE CELL;

ANIMALS; CELLS, CULTURED; EXTRACELLULAR MATRIX; GANGLIA, SPINAL; GLYCOPROTEINS; HYDROGEN-ION CONCENTRATION; LECTINS; NOCICEPTORS; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; VERSICANS;

EID: 84862983602     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.229153     Document Type: Article

References (40)

1. Alessandri-Haber N, Yeh JJ, Boyd AE, Parada CA, Chen X, Reichling DB & Levine JD (2003). Hypotonicity induces TRPV4-mediated nociception in rat. Neuron 39, 497-511.
2. Barritt AW, Davies M, Marchand F, Hartley R, Grist J, Yip P, McMahon SB & Bradbury EJ (2006). Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J Neurosci 26, 10856-10867.
3. Bennett DL, Averill S, Clary DO, Priestley JV & McMahon SB (1996). Postnatal changes in the expression of the trkA high-affinity NGF receptor in primary sensory neurons. Eur J Neurosci 8, 2204-2208.
4. Bogen O, Dina OA, Gear RW & Levine JD (2009). Dependence of monocyte chemoattractant protein 1 hyperalgesia on the isolectin B4-binding protein versican. Neuroscience 159, 780-786.
5. Bogen O, Dreger M, Gillen C, Schröder W & Hucho F (2005). Identification of versican as an isolectin B4-binding glycoprotein from mammalian spinal cord tissue. FEBS J 272, 1090-1102.
6. Bogen O, Joseph EK, Chen X & Levine JD (2008). GDNF hyperalgesia is mediated by PLCγ, MAPK/ERK, PI3K, CDK5 and Src family kinase signaling and dependent on the IB4-binding protein versican. Eur J Neurosci 28, 12-19.
7. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW & McMahon SB (2002). Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640.
8. Brierley SM, Castro J, Harrington AM, Hughes PA, Page AJ, Rychkov GY & Blackshaw LA (2011). TRPA1 contributes to specific mechanically activated currents and sensory neuron mechanical hypersensitivity. J Physiol 589, 3575-3593.
9. Cavanaugh DJ, Lee H, Lo L, Shields SD, Zylka MJ, Basbaum AI & Anderson DJ (2009). Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc Natl Acad Sci U S A 106, 9075-9080.
10. Coste B, Mathur J, Schmidt M, Earley TJ, Ranade S, Petrus MJ, Dubin AE & Patapoutian A (2010). Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330, 55-60.
11. Dansereau MA, Gosselin RD, Pohl M, Pommier B, Mechighel P, Mauborgne A, Rostene W, Kitabgi P, Beaudet N, Sarret P & Melik-Parsadaniantz S (2008). Spinal CCL2 pronociceptive action is no longer effective in CCR2 receptor antagonist-treated rats. J Neurochem 106, 757-769.
12. de la Peña E, Sala S, Rovira JC, Schmidt RF & Belmonte C (2002). Elastoviscous substances with analgesic effects on joint pain reduce stretch-activated ion channel activity in vitro. Pain 99, 501-508.
13. Di Castro A, Drew LJ, Wood JN & Cesare P (2006). Modulation of sensory neuron mechanotransduction by PKC- and nerve growth factor-dependent pathways. Proc Natl Acad Sci U S A 103, 4699-4704.
14. Drew LJ, Rohrer DK, Price MP, Blaver KE, Cockayne DA, Cesare P & Wood JN (2004). Acid-sensing ion channels ASIC2 and ASIC3 do not contribute to mechanically activated currents in mammalian sensory neurones. J Physiol 556, 691-710.
15. Drew LJ, Wood JN & Cesare P (2002). Distinct mechanosensitive properties of capsaicin-sensitive and -insensitive sensory neurons. J Neurosci 22, RC228.
16. Frey Law LA, Sluka KA, McMullen T, Lee J, Arendt-Nielsen L & Graven-Nielsen T (2008). Acidic buffer induced muscle pain evokes referred pain and mechanical hyperalgesia in humans. Pain 140, 254-264.
17. Hotta N, Taguchi T & Mizumura K (2010). Low pH enhances response of thin muscle afferents to mechanical stimuli. Adv Exp Med Biol 669, 315-318.
18. Hu J & Lewin GR (2006). Mechanosensitive currents in the neurites of cultured mouse sensory neurones. J Physiol 577, 815-828.
19. Huang CW, Tzeng JN, Chen YJ, Tsai WF, Chen CC & Sun WH (2007). Nociceptors of dorsal root ganglion express proton-sensing G-protein-coupled receptors. Mol Cell Neurosci 36, 195-210.
20. Hucho TB, Dina OA & Levine JD (2005). Epac mediates a cAMP-to-PKC signaling in inflammatory pain: an isolectin B4(+) neuron-specific mechanism. J Neurosci 25, 6119-6126.
21. Jin W, Lo TM, Loh HH & Thayer SA (1994). U73122 inhibits phospholipase C-dependent calcium mobilization in neuronal cells. Brain Res 642, 237-243.
22. Jones III RC, Xu L & Gebhart GF (2005). The mechanosensitivity of mouse colon afferent fibers and their sensitization by inflammatory mediators require transient receptor potential vanilloid 1 and acid-sensing ion channel 3. J Neurosci 25, 10981-10989.
23. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, Chan KW, Ciceri P, Davis MI, Edeen PT, Faraoni R, Floyd M, Hunt JP, Lockhart DJ, Milanov ZV, Morrison MJ, Pallares G, Patel HK, Pritchard S, Wodicka LM & Zarrinkar PP (2008). A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 26, 127-132.
24. Kinsella MG, Tran PK, Weiser-Evans MC, Reidy M, Majack RA & Wight TN (2003). Changes in perlecan expression during vascular injury: role in the inhibition of smooth muscle cell proliferation in the late lesion. Arterioscler Thromb Vasc Biol 23, 608-614.
25. Koda H & Mizumura K (2002). Sensitization to mechanical stimulation by inflammatory mediators and by mild burn in canine visceral nociceptors in vitro. J Neurophysiol 87, 2043-2051.
26. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ & Corey DP (2006). TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50, 277-289.
27. Kwok JC, Dick G, Wang D & Fawcett JW (2011). Extracellular matrix and perineuronal nets in CNS repair. Dev Neurobiol 71, 1073-1089.
28. Lechner SG & Lewin GR (2009). Peripheral sensitisation of nociceptors via G-protein-dependent potentiation of mechanotransduction currents. J Physiol 587, 3493-3503.
29. Ludwig MG, Vanek M, Guerini D, Gasser JA, Jones CE, Junker U, Hofstetter H, Wolf RM & Seuwen K (2003). Proton-sensing G-protein-coupled receptors. Nature 425, 93-98.
30. Möller I, Perez M, Monfort J, Benito P, Cuevas J, Perna C, Domenech G, Herrero M, Montell E & Verges J (2010). Effectiveness of chondroitin sulphate in patients with concomitant knee osteoarthritis and psoriasis: a randomized, double-blind, placebo-controlled study. Osteoarthritis Cartilage 18 (Suppl. 1), S32-S40.
31. Murase K, Ryu PD & Randic M (1989). Excitatory and inhibitory amino acids and peptide-induced responses in acutely isolated rat spinal dorsal horn neurons. Neurosci Lett 103, 56-63.
32. Sluka KA, Kalra A & Moore SA (2001). Unilateral intramuscular injections of acidic saline produce a bilateral, long-lasting hyperalgesia. Muscle Nerve 24, 37-46.
33. Steen KH & Reeh PW (1993). Sustained graded pain and hyperalgesia from harmless experimental tissue acidosis in human skin. Neurosci Lett 154, 113-116.
34. Steen KH, Reeh PW, Anton F & Handwerker HO (1992). Protons selectively induce lasting excitation and sensitization to mechanical stimulation of nociceptors in rat skin, in vitro. J Neurosci 12, 86-95.
35. Stucky CL & Lewin GR (1999). Isolectin B4-positive and -negative nociceptors are functionally distinct. J Neurosci 19, 6497-6505.
36. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI & Julius D (1998). The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21, 531-543.
37. Tsunozaki M & Bautista DM (2009). Mammalian somatosensory mechanotransduction. Curr Opin Neurobiol 19, 362-369.
38. Vilceanu D & Stucky CL (2010). TRPA1 mediates mechanical currents in the plasma membrane of mouse sensory neurons. PLoS One 5, e12177.
39. Waldmann R, Champigny G, Bassilana F, Heurteaux C & Lazdunski M (1997). A proton-gated cation channel involved in acid-sensing. Nature 386, 173-177.
40. Wu YJ, La Pierre DP, Wu J, Yee AJ & Yang BB (2005). The interaction of versican with its binding partners. Cell Res 15, 483-494.