Salmon and human thrombin differentially regulate radicular pain, glial-induced inflammation and spinal neuronal excitability through protease-activated receptor-1

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Smith, Jenell R ^a   Syre, Peter P ^a   Oake, Shaina A ^a   Nicholson, Kristen J ^a   Weisshaar, Christine L ^a   Cruz, Katrina ^b   Bucki, Robert ^b   Baumann, Bethany C ^a   Janmey, Paul A ^a,b   Winkelstein, Beth A ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BASE SEQUENCE; BLOOD COAGULATION; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EVOKED POTENTIALS; HUMANS; INFLAMMATION; KINETICS; NEURONS; PAIN; RADICULOPATHY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, PAR-1; SALMON; SPINAL CORD; THROMBIN;

EID: 84894281339     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080006     Document Type: Article

References (79)

1. Côté P, Cassidy D, Carroll LJ, Kristman V (2004) The annual incidence and course of neck pain in the general population: a population-based cohort study. Pain 112: 267-273. (Pubitemid 39550726)
2. Haldeman DC, Carroll L, Cassidy D, Schubert J, Nygren A (2008) The bone and joint decade 2000-2010 task force on neck pain and its associated disorders. Spine 33: S5-S7. (Pubitemid 351155753)
3. Strine TW, Hootman JM (2007) US national prevalence and correlates of low back and neck pain among adults. Arthritis Rheum 57: 656-665. (Pubitemid 46764057)
4. Scholz J, Woolf CJ (2007) The neuropathic triad: neurons, immune cells and glia. Nat Neurosci 10: 1361-1368. (Pubitemid 350014681)
5. Woolf CJ, Mannion RJ (1999) Neuropathic pain: aetiology, symptoms, mechanisms, and management. Pain 353: 1959-1999.
6. Abbed KM, Coumans J (2007) Cervical radiculopathy: pathophysiology, presentation, and clinical evaluation. Neurosurgery 60: S28-S34.
7. Caridi JM, Pumberger M, Hughes AP (2011) Cervical radiculopathy: a review. HSS J 7: 265-272.
8. Hubbard RD, Winkelstein BA (2005) Transient cervical nerve root compression in the rat induces bilateral forepaw allodynia and spinal glial activation: mechanical factors in painful neck injuries. Spine 30: 1924-1932. (Pubitemid 41292215)
9. Nicholson KJ, Quindlen JC, Winkelstein BA (2011) Development of a duration threshold for modulating evoked neuronal responses after nerve root compression injury. Stapp Car Crash J 55: 1-24.
10. Nicholson KJ, Guarino BB, Winkelstein BA (2012) Transient nerve root compression load and duration differentially mediate behavioral sensitivity and associated spinal astrocyte activation and mGluR5 expression. Neuroscience 209: 187-195.
11. Wall P, Melzack R (1994) Textbook of Pain. 3rd edition. London: Churchill Livingstone.
12. Chang YW, Winkelstein BA (2011) Schwann cell proliferation and macrophage infiltration are evident at day 14 after painful cervical nerve root compression in the rat. J Neurotrauma 28: 2429-2438.
13. Hubbard RD, Quinn KP, Martínz JJ, Winkelstein BA (2008) The role of graded nerve root compression on axonal damage, neuropeptides changes, and pain-related behaviors. Stapp Car Crash J 52: 33-58.
14. Rothman SM, Huang Z, Lee KE, Weisshaar CL, Winkelstein BA (2009) Cytokine mRNA expression in painful radiculopathy. J Pain 10: 90-99.
15. Winkelstein BA, DeLeo JA (2002) Nerve root severity differentially modulates spinal glial activation in a rat lumbar radiculopathy model: considerations for persistent pain. Brain Res 956: 294-301. (Pubitemid 35351396)
16. Rothman SM, Winkelstein BA (2010) Cytokine antagonism reduces pain and modulates spinal astrocytic reactivity after cervical nerve root compression. Ann Biomed Eng 38: 2563-2576.
17. Rothman SM, Winkelstein BA (2007) Chemical and mechanical nerve root insults induce differential behavioral sensitivity and glial activation that are enhanced in combination. Brain Res 1181: 30-43. (Pubitemid 350050907)
18. Hubbard RD, Winkelstein BA (2008) Dorsal root compression produces myelinated axonal degeneration near the biomechanical thresholds for mechanical behavioral hypersensitivity. Exp Neurol 212: 482-489.
19. Kangrga I, Randic M (1990) Tachykinins and calcitonin gene-related peptide enhance release of endogenous glutamate and aspartate from the rat spinal dorsal horn slice. J Neurosci 10: 2026-2038.
20. Smulin DH, Skilling SR, Larson AA (1990) Interaction between substance P, calcitonin gene-related peptide, taurine and excitatory amino acids in the spinal cord. Pain 42: 93-101. (Pubitemid 20231781)
21. Nicholson KJ, Gilliland TM, Winkelstein BA (2013) Upregulation of GLT-1 by treatment with ceftriaxone alleviates radicular pain by reducing spinal astrocyte activation and neuronal hyperexcitability. J Neurosci Res: doi: 10.1002/jnr.23295.
22. Arnér S, Meyerson BA (1988) Lack of analgesic effect of opioids on neuropathic and idiopathic forms of pain. Pain 22: 11-23.
23. Dworkin RH, Backonja M, Rowbotham MC, Allen RR, Argoff CR, et al. (2003) Advances in neuropatic pain: diagnosis, mechanisms, and treatment recommendations. Arch Neurol 60: 1524-1534. (Pubitemid 37443116)
24. McNicol E, Horowicz-Mehler N, Fisk RA, Bennett K, Gialeli-Goudas M, et al. Management of opioid side effects in cancer-related and chronic noncancer pain: a systematic review. J Pain 4: 231-256.
25. Vranken JH (2009) Mechanisms and treatment of neuropathic pain. Cent Nerv Syst Agents Med Chem 9: 71-78.
26. Garcia P, Gulati A, and Levy JH (2010) The role of thrombin and protease activated receptors in pain mechanisms. Thromb Haemost 103: 1145-1151.
27. Narita M, Usui A, Narita M, Niikura K, Nozaki H, et al. (2005) Protease-activated receptor-1 and platelet-derived growth factor in spinal cord neurons are implicated in neuropathic pain after nerve injury. J Neurosci 25: 10000-10009. (Pubitemid 41528038)
28. Neigo B, Samson AL, Petersen K, Medcalf RL (2011) Thrombin-induced activation of astrocytes in mixed rat hippocampal cultures is inhibited by soluble thrombomodulin. Brain Res 1381: 31-51.
29. Nishino A, Suzuki M, Ohtani H, Motohashi O, Umezawa K, et al. (1993) Thrombin may contribute to the pathophysiology of central nervous system injury. J Neurotrauma 10: 167-179. (Pubitemid 23209482)
30. Asfaha S, Brussee V, Chapman K, Zochodne DW, Vergnolle N (2002) Proteinase-activated receptor-1 agonists attenuate nociception in response to noxious stimuli. Brit J Pharmacol 135: 1101-1106. (Pubitemid 34259109)
31. Fang M, Kovács KJ, Fisher LL, Larson AA (2003) Thrombin inhibits NMDA-mediated nociceptive activity in the mouse: possible mediation by endothelin. J Physiol 549: 903-917. (Pubitemid 36889778)
32. Weisshaar CL, Winer JP, Guarino BB, Janmey PA, Winkelstein BA (2011) The potential for salmon fibrin and thrombin to mitigate pain subsequent to cervical nerve root injury. Biomaterials 32: 9738-9746.
33. Sharp KG, Dickson AR, Marchenko SA, Yee KM, Emery PN, et al. (2012) Salmon fibrin treatment of spinal cord injury promotes functional recovery and density of serotonergic innervation. Exp Neurol 235: 345-356.
34. Coughlin SR (2000) Thrombin signaling and protease-activated receptors. Nature 407: 258-264.
35. Jaques S, LeMasurier M, Sheridan PJ, Seeley SK, Kuliopulos A (2000) Substrate-assisted catalysis of the PAR1 thrombin receptor. J Biol Chem 275: 40671-40678.
36. Luo W, Wang Y, Reiser G (2007) Protease-activated receptors in the brain: receptor expression, activation, and functions in neurodegeneration and neuroprotection. Brain Res 56: 331-345. (Pubitemid 350176599)
37. Bunnett NW (2006) Protease-activated receptors: how proteases signal to cells to cause inflammation and pain. Semin Thromb Hemost 32: 39-47.
38. Junge CE, Lee CJ, Hubbard KB, Zhang A, Olson JJ, et al. (2004) Protease-activated receptor-1 in human brain: localization and functional expression in astrocytes. Exp Neurol 188: 94-103. (Pubitemid 38748808)
39. Pompili E, Fabrizi C, Nori AL, Panetta B, Geloso MC, et al. (2011) Protease-activated receptor-1 expression in rat microglia after trimethyltin treatment. J Histochem Cytochem 59: 302-311.
40. Vellani V, Kinsey AM, Prandini M, Hechtfischer SC, Reeh P, et al. (2010) Protease activated receptors 1 and 4 sensitize TRPV1 in nociceptive neurones. Mol Pain 6: 61.
41. Vergnolle N, Hollenberg MD, Wallace JL (1999) Pro- and anti-inflammatory actions of thrombin: a distinct role for proteinase-activated receptor-1 (PAR1). Britt J Pharmacol 126: 1262-1268. (Pubitemid 29123764)
42. Wang H, Ubl JJ, Reiser G (2002) Four subtypes of protease-activated receptors, co-expressed in rat astrocytes, evoke different physiological signaling. Glia 37: 53-63. (Pubitemid 34103094)
43. Dong L, Smith JR, Winkelstein BA (2013) Ketorolac reduces spinal astrocytic activation and PAR1 expression associated with attenuation of pain after facet joint injury. J Neurotrauma 30: 818-825.
44. Boven LA, Vergnolle N, Henry AD, Silva C, Imai Y, et al. (2003) Up-regulation of proteinase-activated receptor 1 expression in astrocytes during HIV encephalitis. J Immunol 170: 2638-2646. (Pubitemid 36245656)
45. Fan Y, Zhang W, Mulholland M (2005) Thrombin and PAR-1-AP increase proinflammatory cytokine expression in C6 cells. J Surg Res 129: 196-201. (Pubitemid 41797055)
46. Nicole O, Goldshmidt A, Hamill CE, Sorensen SD, Sastre A, et al. (2005) Activation of protease-activated receptor-1 triggers astrogliosis after brain injury. J Neurosci 25: 4319-4329. (Pubitemid 40628776)
47. Simmons A, Lee RV, Möller T, Weinstein JR (2013) Thrombin induces release of proinflammatory chemokines interleukin-8 and interferon-γ- induced protein-10 from cultured human fetal astrocytes. Neuroreport 24: 36-40.
48. Zimmermann M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16: 109-110.
49. Michaud SE, Wang LZ, Korde N, Bucki R, Randhawa PK, et al. (2002) Purification of salmon thrombin and its potential as an alternative to mammalian thrombins in fibrin sealants. Thomb Res 107: 245-254. (Pubitemid 35435384)
50. Winer JP, Oake S, Janmey PA (2009) Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation. PLoS One 4: e6382.
51. Brummel KE, Paradis SG, Butenas S, Mann KG (2002) Thrombin functions during tissue factor-induced blood coagulation. Blood 100: 148-152. (Pubitemid 35177440)
52. Ignjatovic V (2013) Thrombin clotting time. Methods Mol Biol 992: 131-138.
53. Quinn KP, Dong L, Golder FJ, Winkelstein BA (2010) Neuronal hyperexcitability in the dorsal horn after painful facet joint injury. Pain 151: 414-421.
54. Miller WJ, Leventhal I, Scarsella D, Haydon PG, Janmey PA, et al. (2009) Mechanically induced reactive gliosis causes ATP-mediated alterations in astrocyte stiffness. J Neurotrauma 26: 789-797.
55. Seeley S, Covic L, Jaques SL, Sudmeier J, Baleja JD, et al. (2003) Structural basis for thrombin activation of a protease-activated receptor: inhibition of intramolecular liganding. Chem Biol 10: 1033-1041. (Pubitemid 37496433)
56. Latremoliere A, Woolf CJ (2009) Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 10: 895-926.
57. DeLeo JA (2006) Basic science of pain. J Bone Joint Surg Am S2: 58-62.
58. Inoue K (2006) The function of microglia through purinergic receptors: neuropathic pain and cytokine release. Pharmacol Therapeut 109: 210-226.
59. Milligan ED, Watkins LR (2009) Pathological and protective roles of glia in chronic pain. Nat Rev Neursoci 10: 23-36.
60. Vallejo R, Tille DM, Vogel L, Benyamin R (2010) The role of glia and the immune system in the development and maintenance of neuropathic pain. Pain Pract 10: 167-184.
61. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6: 626-640. (Pubitemid 41059337)
62. Watkins LR, Milligan ED, Maier SF (2001) Glial activation: a driving force for pathological pain. Trends Neurosci 24: 450-455. (Pubitemid 32695356)
63. Winkelstein BA, Rutkowski MD, Sweitzer SM, Pahl JL, DeLeo JA (2001) Nerve injury proximal or distal to the DRG induces similar spinal glial activation and selective cytokine expression fur differential behavioral responses to pha rmacological treatment. J Comp Neurol 439: 127-139. (Pubitemid 32906017)
64. Ju YE, Janmey PA, McCormick ME, Sawyer ES, Flanagan LA (2007) Enhanced neurite growth from mammalian neurons in three-dimensional salmon fibrin gels. Biomaterials 28: 2097-2108. (Pubitemid 46198924)
65. Uibo R, Laidmäe I, Sawyer ES, Flanagan LA, Georges PC, et al. (2009) Soft materials to treat central nervous system injuries: evaluation of the suitability of non-mammalian fibrin gels. Biomaterials 1793: 924-930.
66. Martin L, Augé C, Boué J, Buresi MC, Chapman K, et al. (2009) Thrombin receptor: an endogenous inhibitor of inflammatory pain, activating opioid pathways. Pain 146: 121-129.
67. Chang YW, Tan A, Saab C, Waxman S (2009) Unilateral focal burn injury is followed by long-lasting bilateral allodynia and neuronal hyperexcitability in spinal cord dorsal horn. J Pain 11: 119-130.
68. Crosby ND, Weisshaar CL, Winkelstein BA (2013) Spinal neuronal plasticity is evident within 1 day after a painful cervical facet capsule injury. Neurosci Lett 542: 102-106.
69. Palecek J, Dougherty PM, Kim SH, Paleckova V, Lekan H, et al. (1992) Responses of spinothalamic tract neurons to mechanical and thermal stimuli in an experimental model of peripheral neuropathy in primates. J Neurophysiol 68: 1951-1966. (Pubitemid 23015499)
70. Choi MS, Kim YE, Lee WJ, Choi JW, Park GH, et al. (2007) Activation of protease-activated receptor 1 mediates induction of matrix metalloproteinase-9 by thrombin in rat primary astrocytes. Brain Res Bull 76: 368-375.
71. Jha MK, Jeon S, Suk K (2012) Glia as a link between neuroinflammation and neuropathic pain. Immune Netw 12: 41-47.
72. McMahon SB, Cafferty WBJ, Marchand F (2005) Immune and glial cell factors as pain mediators and modulators. Exp Neurol 192: 444-462. (Pubitemid 40341688)
73. Dale C, Vergnolle N (2008) Protease signaling to G protein-coupled receptors: implications for inflammation and pain. J Recept Signal Transduct Res 28: 29-37. (Pubitemid 351588074)
74. Ma L, Dorling A (2012) The roles of thrombin and protease-activated receptors in inflammation. Semin Immunopathol 34: 63-72.
75. Gao YJ, Ji RR (2009) c-Fos or pERK, which is a better marker for neuronal activation and central sensitization after noxious stimulation and tissue injury? Open Pain J 2: 11-17.
76. Shavit E, Michaelson DM, Chapman J (2011) Anatomical localization of protease-activated receptor-1 and protease-mediated neuroglial crosstalk on peri-synaptic astrocytic endfeet. J Neurochem 119: 460-473.
77. Asfaha S, Cenac N, Houle S, Altier C, Papez MD, et al. (2007) Protease-activated receptor-4: a novel mechanism of inflammatory pain modulation. Britt J Pharmacol 150: 176-185. (Pubitemid 46160607)
78. Gosalia DN, Salisbury CM, Maly DJ, Ellman JA, Diamond SL (2005) Profiling serine protease substrate specificity with solution phase fluorogenic peptide microarrays. Proteomics 5: 1292-1298.
79. Manseth E, Skjervold PO, Flengsrud R (2004) Sample displacement chromatography of atlantic salmon (salmo salar) thrombin. J Biochem Biophys Methods 60: 39-47. (Pubitemid 38952851)