Thrombospondin-4 contributes to spinal sensitization and neuropathic pain states

Journal of Neuroscience

Volumn 32, Issue 26, 2012, Pages 8977-8987

  Kim, Doo Sik ^a,g   Li, Kang Wu ^a   Boroujerdi, Amin ^a   Yu, Yanhui Peter ^a   Zhou, Chun Yi ^a   Deng, Ping ^b   Park, John ^a   Zhang, Xia ^a,h   Lee, Joshua ^a   Corpe, Michael ^a   Sharp, Kelli ^c   Steward, Oswald ^c   Eroglu, Cagla ^d   Barres, Ben ^e   Zaucke, Frank ^f   Xu, Zao C ^b   David Luo, Z ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e STANFORD UNIVERSITY   (United States)

^f UNIVERSITY OF COLOGNE   (Germany)

^g Kosin University   (South Korea)

^h CHINA MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

THROMBOSPONDIN; THROMBOSPONDIN 4; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BEHAVIOR; CENTRAL NERVOUS SYSTEM SENSITIZATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FLUORESCENCE HISTOCHEMISTRY; GENE; HYPERSENSITIVITY; KNOCKOUT MOUSE; LOCOMOTION; MALE; MOUSE; NERVE LIGATION; NERVOUS SYSTEM FUNCTION; NEUROPATHIC PAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL NEURON SENSITIZATION; SPINE INJURY; THROMBOSPONDIN 4 GENE; UPREGULATION; WESTERN BLOTTING;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANALYSIS OF VARIANCE; ANIMALS; ANTIBODIES; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID ANTAGONISTS; GREEN FLUORESCENT PROTEINS; HUMANS; HYPERALGESIA; INHIBITORY POSTSYNAPTIC POTENTIALS; INJECTIONS, SPINAL; MALE; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; NEURALGIA; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; PAIN MEASUREMENT; PAIN THRESHOLD; RATS; RATS, SPRAGUE-DAWLEY; SODIUM CHANNEL BLOCKERS; SPINAL CORD; SPINAL NERVES; TETRODOTOXIN; THROMBOSPONDINS; UP-REGULATION; VALINE;

EID: 84862838135     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6494-11.2012     Document Type: Article

References (46)

1. Adams JC (2001) Thrombospondins: multifunctional regulators of cell interactions. Annu Rev Cell Dev Biol 17:25-51.
2. Adams JC, Lawler J (2004) The thrombospondins. Int J Biochem Cell Biol 36:961-968.
3. Arber S, Caroni P (1995) Thrombospondin-4, an extracellular matrix protein expressed in the developing and adult nervous system promotes neurite outgrowth. J Cell Biol 131:1083-1094.
4. Barlow AL, Macleod A, Noppen S, Sanderson J, Guérin CJ (2010) Colocalization analysis in fluorescence micrographs: verification of a more accurate calculation of Pearson's correlation coefficient. Microsc Microanal 16:710-724.
5. Basso DM, Beattie MS, Bresnahan JC (1995) A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12:1-21.
6. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, Popovich PG (2006) Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 23:635-659.
7. Bornstein P (2001) Thrombospondins as matricellular modulators of cell function. J Clin Invest 107:929-934.
8. Boroujerdi A, Kim HK, Lyu YS, Kim DS, Figueroa KW, Chung JM, Luo ZD (2008) Injury discharges regulate calcium channel alpha-2-delta-1 subunit upregulation in the dorsal horn that contributes to initiation of neuropathic pain. Pain 139:358-366.
9. Boroujerdi A, Zeng J, Sharp K, Kim D, Steward O, Luo ZD (2011) Calcium channel alpha-2-delta-1 protein upregulation in dorsal spinal cord mediates spinal cord injury-induced neuropathic pain states. Pain 152:649-655.
10. Brittain JM, Duarte DB, Wilson SM, Zhu W, Ballard C, Johnson PL, Liu N, Xiong W, Ripsch MS, Wang Y, Fehrenbacher JC, Fitz SD, Khanna M, Park CK, Schmutzler BS, Cheon BM, Due MR, Brustovetsky T, Ashpole NM, Hudmon A, et al. (2011) Suppression of inflammatory and neuropathic pain by uncoupling CRMP-2 from the presynaptic Ca(2) channel complex. Nat Med 17:822-829.
11. Choi BH (1988) Prenatal gliogenesis in the developing cerebrum of the mouse. Glia 1:308-316.
12. Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A, Lawler J, Mosher DF, Bornstein P, Barres BA (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120:421-433.
13. Costigan M, Befort K, Karchewski L, Griffin RS, D'Urso D, Allchorne A, Sitarski J, Mannion JW, Pratt RE, Woolf CJ (2002) Replicate highdensity rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci 3:16.
14. Cserr H (1965) Potassium exchange between cerebrospinal fluid, plasma, and brain. Am J Physiol 209:1219-1226.
15. Dixon WJ (1980) Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20:441-462.
16. Dubový P, Klusáková I, Svízenská I (2002) A quantitative immunohistochemical study of the endoneurium in the rat dorsal and ventral spinal roots. Histochem Cell Biol 117:473-480.
17. Dunkle ET, Zaucke F, Clegg DO (2007) Thrombospondin-4 and matrix three-dimensionality in axon outgrowth and adhesion in the developing retina. Exp Eye Res 84:707-717.
18. Edwards MA, Yamamoto M, Caviness VS Jr (1990) Organization of radial glia and related cells in the developing murine CNS: an analysis based upon a new monoclonal antibody marker. Neuroscience 36:121-144.
19. Eroglu C, Allen NJ, Susman MW, O'Rourke NA, Park CY, Ozkan E, Chakraborty C, Mulinyawe SB, Annis DS, Huberman AD, Green EM, Lawler J, Dolmetsch R, Garcia KC, Smith SJ, Luo ZD, Rosenthal A, Mosher DF, Barres BA (2009) Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell 139:380-392.
20. Fukuoka T, Yamanaka H, Kobayashi K, Okubo M, Miyoshi K, Dai Y, Noguchi K (2012) Re-evaluation of the phenotypic changes in L4 dorsal root ganglion neurons after L5 spinal nerve ligation. Pain 153:68-79.
21. 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.
22. Hoffman JR, O'Shea KS (1999) Thrombospondin expression in nerve regeneration, II: comparison of optic nerve crush in the mouse and goldfish. Brain Res Bull 48:421-427.
23. Jeon SM, Lee KM, Cho HJ (2009) Expression of monocyte chemoattractant protein-1 in rat dorsal root ganglia and spinal cord in experimental models of neuropathic pain. Brain Res 1251:103-111.
24. Katsura H, Obata K, Mizushima T, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Tokunaga A, Sakagami M, Noguchi K (2006) Antisense knock down of TRPA1, but not TRPM8, alleviates cold hyperalgesia after spinal nerve ligation in rats. Exp Neurol 200:112-123.
25. Kim DS, Figueroa KW, Li KW, Boroujerdi A, Yolo T, Luo ZD (2009) Profiling of dynamically changed gene expression in dorsal root ganglia post peripheral nerve injury and a critical role of injury-induced glial fibrillary acidic protein in maintenance of pain behaviors [corrected]. Pain 143:114-122.
26. Kim SH, Chung JM (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363.
27. Li CY, Song YH, Higuera ES, Luo ZD (2004) Spinal dorsal horn calcium channel α2δ-1 subunit upregulation contributes to peripheral nerve injury-induced tactile allodynia. J Neurosci 24:8494-8499.
28. Lo FS, Zhao S, Erzurumlu RS (2011) Astrocytes promote peripheral nerve injury-induced reactive synaptogenesis in the neonatal CNS. J Neurophysiol 106:2876-2887.
29. Luo ZD, Figueroa KW (2008) Multilevel genomic approach in pain research: basic science and clinical implications. Rev Analg 10:45-58.
30. Luo ZD, Chaplan SR, Higuera ES, Sorkin LS, Stauderman KA, Williams ME, Yaksh TL (2001) Upregulation of dorsal root ganglion α2δ calcium channel subunit and its correlation with allodynia in spinal nerve-injured rats. J Neurosci 21:1868-1875.
31. Nguyen D, Deng P, Matthews EA, Kim DS, Feng G, Dickenson AH, Xu ZC, Luo ZD (2009) Enhanced pre-synaptic glutamate release in deep-dorsal horn contributes to calcium channel alpha-2-delta-1 protein-mediated spinal sensitization and behavioral hypersensitivity. Mol Pain 5:6.
32. Obata K, Yamanaka H, Kobayashi K, Dai Y, Mizushima T, Katsura H, Fukuoka T, Tokunaga A, Noguchi K (2004) Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation. J Neurosci 24:10211-10222.
33. Pixley SK, de Vellis J (1984) Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Brain Res 317:201-209.
34. Randall LO, Selitto JJ (1957) A method for measurement of analgesic activity on inflamed tissue. Arch Int Pharmacodyn Ther 111:409-419.
35. 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.
36. Schäfers M, Sorkin LS, Geis C, Shubayev VI (2003) Spinal nerve ligation induces transient upregulation of tumor necrosis factor receptors 1 and 2 in injured and adjacent uninjured dorsal root ganglia in the rat. Neurosci Lett 347:179-182.
37. Shibasaki M, Sasaki M, Miura M, Mizukoshi K, Ueno H, Hashimoto S, Tanaka Y, Amaya F (2010) Induction of high mobility group box-1 in dorsal root ganglion contributes to pain hypersensitivity after peripheral nerve injury. Pain 149:514-521.
38. Shimoyama M, Shimoyama N, Hori Y (2000) Gabapentin affects glutamatergic excitatory neurotransmission in the rat dorsal horn. Pain 85:405-414.
39. Södersten F, Ekman S, Schmitz M, Paulsson M, Zaucke F (2006) Thrombospondin-4 and cartilage oligomeric matrix protein form heterooligomers in equine tendon. Connect Tissue Res 47:85-91.
40. Valder CR, Liu JJ, Song YH, Luo ZD (2003) Coupling gene chip analyses and rat genetic variances in identifying potential target genes that may contribute to neuropathic allodynia development. J Neurochem 87:560-573.
41. Wang H, Sun H, Della Penna K, Benz RJ, Xu J, Gerhold DL, Holder DJ, Koblan KS (2002) Chronic neuropathic pain is accompanied by global changes in gene expression and shares pathobiology with neurodegenerative diseases. Neuroscience 114:529-546.
42. Xu JT, Tu HY, Xin WJ, Liu XG, Zhang GH, Zhai CH (2007) Activation of phosphatidylinositol 3-kinase and protein kinase B/Akt in dorsal root ganglia and spinal cord contributes to the neuropathic pain induced by spinal nerve ligation in rats. Exp Neurol 206:269-279.
43. Xu J, Xiao N, Xia J (2010) Thrombospondin 1 accelerates synaptogenesis in hippocampal neurons through neuroligin 1. Nat Neurosci 13:22-24.
44. Yaksh T, Luo ZD (2007) Anatomy of the pain processing system. In: Pain management (Waldman SD, ed), pp 11-20. Philadelphia: Saunders Elsevier.
45. Yang L, Zhang FX, Huang F, Lu YJ, Li GD, Bao L, Xiao HS, Zhang X (2004) Peripheral nerve injury induces trans-synaptic modification of channels, receptors and signal pathways in rat dorsal spinal cord. Eur J Neurosci 19:871-883.
46. Zeilhofer HU (2005) Synaptic modulation in pain pathways. Rev Physiol Biochem Pharmacol 154:73-100.