Thrombospondin-4 and excitatory synaptogenesis promote spinal sensitization after painful mechanical joint injury

Experimental Neurology

Volumn 264, Issue , 2015, Pages 111-120

  Crosby, Nathan D ^a   Zaucke, Frank ^b   Kras, Jeffrey V ^a   Dong, Ling ^a   Luo, Z David ^c   Winkelstein, Beth A ^a,d  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; GABAPENTIN; THROMBOSPONDIN; THROMBOSPONDIN 4; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID; AMINE; ANALGESIC AGENT; CYCLOHEXANECARBOXYLIC ACID DERIVATIVE; GLIAL FIBRILLARY ACIDIC PROTEIN; TUBULIN;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; EXCITABILITY; JOINT INJURY; LOAD CARRYING CAPACITY; MALE; MECHANOTRANSDUCTION; NERVE CELL PLASTICITY; NEUROPATHIC PAIN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT; SENSITIZATION; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL GANGLION; SPINAL SENSITIZATION; SYNAPTOGENESIS; ACTION POTENTIAL; ANIMAL; ARTHRALGIA; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENE EXPRESSION REGULATION; GENETICS; HYPERALGESIA; JOINT CAPSULE; METABOLISM; NERVE CELL; PAIN MEASUREMENT; PATHOLOGY; PHYSIOLOGY; SYNAPSE; TIME FACTOR; ZYGAPOPHYSEAL JOINT;

ACTION POTENTIALS; AMINES; ANALGESICS; ANIMALS; ARTHRALGIA; CYCLOHEXANECARBOXYLIC ACIDS; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; HYPERALGESIA; JOINT CAPSULE; MALE; NEURONS; PAIN MEASUREMENT; RATS; SPINAL CORD; SYNAPSES; THROMBOSPONDINS; TIME FACTORS; TUBULIN; ZYGAPOPHYSEAL JOINT;

EID: 84919724898     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.11.015     Document Type: Article

References (52)

1. Adams J.C. Thrombospondins: multifunctional regulators of cell interactions. Annu. Rev. Cell Dev. Biol. 2001, 17:25-51.
2. Adams J.C., Lawler J. The thrombospondins. Int. J. Biochem. Cell B 2004, 36:961-968.
3. Arber S., Caroni P. Thrombospondin-4, an extracellular matrix protein expressed in the developing and adult nervous system promotes neurite outgrowth. J. Cell Biol. 1995, 131:1083-1094.
4. Basbaum A.I., Bautista D.M., Scherrer G., Julius D. Cellular and molecular mechanisms of pain. Cell 2009, 139:267-284.
5. Bove S.E., Laemont K.D., Brooker R.M., Osborn M.N., Sanchez B.M., Guzman R.E., Hook K.E., Juneau P.L., Connor J.R., Kilgore K.S. Surgically induced osteoarthritis in the rat results in the development of both osteoarthritis-like joint pain and secondary hyperalgesia. Osteoarthr. Cartil. 2006, 14:1041-1048.
6. Brakeman P.R., Lanahan A.A., O'Brien R., Roche K., Barnes C.A., Huganir R.L., Worley P.F. Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 1997, 386:284-288.
7. Chen Y.W., Zhao P., Borup R., Hoffman E.P. Expression profiling in the muscular dystrophies: identification of novel aspects of molecular pathophysiology. J. Cell Biol. 2000, 151:1321-1336.
8. Christopherson K.S., Ullian E.M., Stokes C.C.A., Mullowney C.E., Hell J.W., Agah A., Lawler J., Mosher D.F., Bornstein P., Barres B.A. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 2005, 120:421-433.
9. Crosby N.D., Weisshaar C.L., Winkelstein B.A. Spinal neuronal plasticity is evident within 1day after a cervical facet joint injury. Neurosci. Lett. 2013, 542:102-106.
10. Crosby N.D., Gilliland T.M., Winkelstein B.A. Early afferent activity from the facet joint after painful trauma to its capsule potentiates neuronal excitability and glutamate signaling in the spinal cord. Pain 1878-1887, 155:2014.
11. De Camilli P., Cameron R., Greengard P. Synapsin 1, a nerve terminal specific phosphoprotein: its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections. J. Cell Biol. 1983, 96:1337-1354.
12. Dong L., Winkelstein B.A. Simulated whiplash modulates expression of the glutamatergic system in the spinal cord suggesting spinal plasticity is associated with painful dynamic cervical facet loading. J. Neurotrauma 2010, 27:163-174.
13. Dong L., Quindlen J.C., Lipschutz D.E., Winkelstein B.A. Whiplash-like facet joint loading initiates glutamatergic responses in the DRG and spinal cord associated with behavioral hypersensitivity. Brain Res. 2012, 1461:51-63.
14. Dong L., Crosby N.D., Winkelstein B.A. Gabapentin alleviates facet-mediated pain in the rat through reduced neuronal hyperexcitability and astrocytic activation in the spinal cord. J. Pain 2013, 14:1564-1572.
15. Dong L., Smith J.R., Winkelstein B.A. Ketorolac reduces spinal astrocytic activation and PAR1 expression associated with attenuation of pain following facet joint injury. J. Neurotrauma 2013, 30:818-825.
16. Dunkle E.T., Zaucke F., Clegg D.O. Thrombospondin-4 and matrix three-dimensionality in axon growth and adhesion in the developing retina. Exp. Eye Res. 2007, 84:707-717.
17. Duquette M., Nadler M., Okuhara D., Thompson J., Shuttleworth T., Lawler J. Members of the Thrombospondin Gene Family Bind Stromal Interaction Molecule 1 and Regulate Calcium Channel Activity 2014, (Matrix Biol in press).
18. Eroglu C., Allen N.J., Susman M.W., O'Rourke N.A., Park C.Y., Ozkan E., Chakraborty C., Mulinyawe S.B., Annis D.S., Huberman A.D., Green E.M., Lawler J., Dolmetsch R., Garcia K.C., Smith S.J., Luo Z.D., Rosenthal A., Mosher D.F., Barres B.A. Gabapentin receptor a2d-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell 2009, 139:380-392.
19. Field M.J., Holloman E.F., McCleary S., Hughes J., Singh L. Evaluation of gabapentin and S-(+)-3-isobutylgaba in a rat model of postoperative pain. JPET 1997, 282:1242-1246.
20. Hains B.C., Johnson K.M., Eaton M.J., Willis W.D., Hulsebosch C.E. Serotonergic neural precursor cell grafts attenuate bilateral hyperexcitability of dorsal horn neurons after spinal hemisection in rat. Neuroscience 2003, 116:1097-1110.
21. Hansen U., Platz N., Becker A., Bruckner P., Paulsson M., Zaucke F. A secreted variant of cartilage oligomeric matrix protein carrying a chondrodysplasia-causing mutation (p.H587R) disrupts collagen fibrillogenesis. Arthritis Rheum. 2011, 63:159-167.
22. Hogg-Johnson S., van der Velde G., Carroll L.J., Holm L.W., Cassidy J.D., Guzman J., Cote P., Halderman S., Ammendolia C., Carragee E., Hurwitz E., Nordin M., Peloso P. The burden and determinants of neck pain in the general population. Eur. Spine J. 2008, 17:S39-S51.
23. Honore P., Rogers S.D., Schwei M.J., Salak-Johnson J.L., Luger N.M., Sabino M.C., Clohisy D.R., Mantyh P.W. Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons. Neuroscience 2000, 98:585-598.
24. Hubbard R.D., Chen Z., Winkelstein B.A. Transient cervical nerve root compression modulates pain: load thresholds for allodynia and sustained changes in spinal neuropeptide expression. J. Biomech. 2008, 41(3):677-685.
25. Ippolito D.M., Eroglu C. Quantifying synapses: an immunohistochemistry-based assay to quantify synapse number. J. Vis. Exp. 2010, 45:2270.
26. Jaken R.J.P., Joosten E.A.J., Knuwer M., Miller R., ven der Meulen I., Marcus M.A.E., Deumens R. Synaptic plasticity in the substantia gelatinosa in a model of chronic neuropathic pain. Neurosci. Lett. 2010, 469:30-33.
27. Kallakuri S., Singh A., Lu Y., Chen C., Patwardhan A., Cavanaugh J.M. Tensile stretching of cervical facet joint capsule and related axonal changes. Eur. Spine J. 2008, 17:556-563.
28. Kim D.S., Li K.W., Boroujerdi A., Yu Y.P., Zhou C.Y., Deng P., Park J., Zhang X., Lee J., Corpe M., Sharp K., Steward O., Eroglu C., Barres B., Zaucke F., Xu Z.C., Luo Z.D. Thrombospondin-4 contributes to spinal sensitization and neuropathic pain states. J. Neurosci. 2012, 32:8977-8987.
29. Kras J.V., Weisshaar C.L., Quindlen J.A., Winkelstein B.A. Brain-derived neurotrophic factor is upregulated in the cervical DRG & spinal cord and contributes to the maintenance of pain from facet joint injury. J. Neurosci. Res. 2013, 91:1312-1321.
30. Kras J.V., Dong L., Winkelstein B.A. Increased interleukin-1a and prostaglandin E2 expression in the spinal cord at day 1 after painful facet joint injury: evidence of early spinal inflammation. Spine 2014, 39:207-212.
31. Latremoliere A., Woolf C.J. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J. Pain 2009, 10:895-926.
32. Lee K.E., Winkelstein B.A. Joint distraction magnitude is associated with different behavioral outcomes and substance P levels for cervical facet joint loading in the rat. J. Pain 2009, 10:436-445.
33. Lee K.E., Davis M.B., Mejilla R.M., Winkelstein B.A. In vivo cervical facet capsule distraction: mechanical implications for whiplash and neck pain. Stapp Car Crash J. 2004, 48:373-395.
34. Lee K.E., Davis M.B., Winkelstein B.A. Capsular ligament involvement in the development of mechanical hyperalgesia after facet joint loading: behavioral and inflammatory outcomes in a rodent model of pain. J. Neurotrauma 2008, 25:1383-1393.
35. Li K.W., Kim D.S., Zaucke F., Luo Z.D. Trigeminal nerve injury-induced thrombospondin-4 upregulation contributes to orofacial neuropathic pain states in a rat model. Eur. J. Pain 2014, 18:489-495.
36. Li K.W., Yu Y.P., Zhou C., Kim D.S., Lin B., Sharp K., Steward O., Luo Z.D. Calcium channel α2δ1 proteins mediate trigeminal neuropathic pain states associated with aberrant excitatory synaptogenesis. J. Biol. Chem. 2014, 289:7025-7037.
37. Lin J.Y., Peng B., Yang Z.W., Min S. Number of synapses increased in the rat spinal dorsal horn after sciatic nerve transection: a stereological study. Brain Res. Bull. 2011, 84:430-433.
38. Lo F.S., Zhao S., Erzurumlu R.S. Astrocytes promote peripheral nerve injury-induced reactive synaptogenesis in the neonatal CNS. J. Neurophysiol. 2011, 106:2876-2887.
39. Lu Y., Chen C., Kallakuri S., Patwardhan A., Cavanaugh J.M. Neural response of cervical facet joint capsule to stretch: a study of whiplash pain mechanisms. Stapp Car Crash 2005, 49:49-65.
40. Luo Z.D., Calcutt N.A., Higuera E.S., Valder C.R., Song Y.H., Svensson C.I., Myers R.R. Injury type-specific calcium channel a2d-1 subunit upregulation in rat neuropathic pain models correlates with antiallodynic effects of gabapentin. JPET 2002, 303:1199-1205.
41. Neher E., Sakaba T. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 2008, 59:861-872.
42. Pan B., Yu H., Park J., Yu Y.P., Luo Z.D., Hogan Q.H. Painful nerve injury upregulates thrombospondin-4 expression in dorsal root ganglia. J. Neurosci. Res. 2014, 10.1002/jnr.23498.
43. Pearson A.M., Ivancic P.C., Ito S., Panjabi M.M. Facet joint kinematics and injury mechanisms during simulated whiplash. Spine 2004, 29:390-397.
44. Peng B., Lin J.Y., Shang Y., Yang Z.W., Wang Y.P. Plasticity in the synaptic number associated with neuropathic pain in the rat spinal dorsal horn: a stereological study. Neurosci. Lett. 2010, 486:24-28.
45. Quinn K.P., Dong L., Golder F.J., Winkelstein B.A. Neuronal hyperexcitability in the dorsal horn after painful facet joint injury. Pain 2010, 151:414-421.
46. Rose M.A., Kam P.C.A. Gabapentin: pharmacology and its use in pain management. Anaesthesia 2002, 57:451-462.
47. Rothman S.M., Hubbard R.D., Lee K.E., Winkelstein B.A. Detection, transmission, and perception of pain. Interventional Spine: An Algorithmic Approach 2008, 29-38. Saunders, Philadelphia. C.W. Slipman, R. Derby, F.A. Simeone, T.G. Mayer (Eds.).
48. Siegmund G.P., Winkelstein B.A., Ivancic P.C. The anatomy and biomechanics of acute and chronic whiplash injury. Traffic Inj. Prev. 2009, 10:101-112.
49. Stenina O.I., Desai S.Y., Krukovets I., Kight K., Janigro D., Topol E.J., Plow E.F. Thrombospondin-4 and its variants: expression and differential effects on endothelial cells. Circulation 2003, 108:1514-1519.
50. Ullian E.M., Sapperstein S.K., Christopherson K.S., Barres B.A. Control of synapse number by glia. Science 2001, 291:657-661.
51. Woolf C.J., Shortland P., Coggeshall R.E. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 1992, 355:75-78.
52. Zeng J., Kim D., Li K.W., Sharp K., Steward O., Zaucke F., Luo Z.D. Thrombospondin-4 contributes to spinal cord injury-induced changes in nociception. Eur. J. Pain 2013, 17:1458-1464.