Intrathecal delivery of PDGF produces tactile allodynia through its receptors in spinal microglia

Molecular Pain

Volumn 5, Issue , 2009, Pages

  Masuda, Junya ^a   Tsuda, Makoto ^a   Tozaki Saitoh, Hidetoshi ^a   Inoue, Kazuhide ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; GLIAL FIBRILLARY ACIDIC PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; MINOCYCLINE; NEURON SPECIFIC NUCLEAR PROTEIN; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN CC1; PROTEIN OX 42; UNCLASSIFIED DRUG; PLATELET DERIVED GROWTH FACTOR;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL COUNT; CELL STRUCTURE; CONTROLLED STUDY; IMMUNOFLUORESCENCE; MALE; MICROGLIA; NERVE INJURY; NEUROPATHIC PAIN; NONHUMAN; OLIGODENDROGLIA; PATHOGENESIS; PRIORITY JOURNAL; RAT; SPINAL CORD DORSAL HORN; TACTILE ALLODYNIA; WITHDRAWAL REFLEX; ANIMAL; CYTOLOGY; DISEASE MODEL; DRUG ADMINISTRATION ROUTE; HYPERALGESIA; INJURY; METABOLISM; PAIN; PAIN ASSESSMENT; PATHOLOGY; PHYSIOLOGY; SPINAL NERVE; TOUCH; WISTAR RAT;

ANIMALS; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION ROUTES; HYPERALGESIA; MALE; MICROGLIA; PAIN; PAIN MEASUREMENT; PLATELET-DERIVED GROWTH FACTOR; RATS; RATS, WISTAR; SPINAL NERVES; TOUCH;

EID: 67449118510     PISSN: 17448069     EISSN: None     Source Type: Journal    
DOI: 10.1186/1744-8069-5-23     Document Type: Article

References (47)

1. Woolf CJ Mannion RJ Neuropathic pain: Aetiology, symptoms, mechanisms, and management Lancet 1999, 353:1959-1964. 10.1016/S0140-6736(99)01307-0 10371588
2. Nicholson B Differential diagnosis: Nociceptive and neuropathic pain Am J Manag Care 2006, 12:S256-262. 16774457
3. Scholz J Woolf CJ Can we conquer pain? Nat Neurosci 2002, 5(Suppl):1062-1067. 10.1038/nn942 12403987
4. Woolf CJ Evidence for a central component of post-injury pain hypersensitivity Nature 1983, 306:686-688. 10.1038/306686a0 6656869
5. Pol van den AN Obrietan K Chen G Excitatory actions of GABA after neuronal trauma J Neurosci 1996, 16:4283-4292. 8753889
6. Moore KA Kohno T Karchewski LA Scholz J Baba H Woolf CJ Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord J Neurosci 2002, 22:6724-6731. 12151551
7. Obata K Noguchi K MAPK activation in nociceptive neurons and pain hypersensitivity Life Sci 2004, 74:2643-2653. 10.1016/j.lfs.2004.01.007 15041446
8. Zhou XF Deng YS Chie E Xue Q Zhong JH McLachlan EM Rush RA Xian CJ Satellite-cell-derived nerve growth factor and neurotrophin-3 are involved in noradrenergic sprouting in the dorsal root ganglia following peripheral nerve injury in the rat Eur J Neurosci 1999, 11:1711-1722. 10.1046/j.1460-9568.1999.00589.x 10215925
9. Tsuda M Inoue K Salter MW Neuropathic pain and spinal microglia: A big problem from molecules in "small" glia Trends Neurosci 2005, 28:101-107. 10.1016/j.tins.2004.12.002 15667933
10. Watkins LR Milligan ED Maier SF Glial activation: A driving force for pathological pain Trends Neurosci 2001, 24:450-455. 10.1016/ S0166-2236(00)01854-3 11476884
11. Tsuda M Mizokoshi A Shigemoto-Mogami Y Koizumi S Inoue K Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury Glia 2004, 45:89-95. 10.1002/glia.10308 14648549
12. Tsuda M Shigemoto-Mogami Y Koizumi S Mizokoshi A Kohsaka S Salter MW Inoue K P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury Nature 2003, 424:778-783. 10.1038/ nature01786 12917686
13. Tozaki-Saitoh H Tsuda M Miyata H Ueda K Kohsaka S Inoue K P2Y12 receptors in spinal microglia are required for neuropathic pain after peripheral nerve injury J Neurosci 2008, 28:4949-4956. 10.1523/ JNEUROSCI.0323-08.2008 18463248
14. Zhuang ZY Kawasaki Y Tan PH Wen YR Huang J Ji RR Role of the CX3CR1/p38 MAPK pathway in spinal microglia for the development of neuropathic pain following nerve injury-induced cleavage of fractalkine Brain Behav Immun 2007, 21:642-651. 2084372 17174525 10.1016/j.bbi.2006.11.003
15. Jin SX Zhuang ZY Woolf CJ Ji RR p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain J Neurosci 2003, 23:4017-4022. 12764087
16. Li X Ponten A Aase K Karlsson L Abramsson A Uutela M Backstrom G Hellstrom M Bostrom H Li H et al. PDGF-C is a new protease-activated ligand for the PDGF alpha-receptor Nat Cell Biol 2000, 2:302-309. 10.1038/35010579 10806482
17. LaRochelle WJ Jeffers M McDonald WF Chillakuru RA Giese NA Lokker NA Sullivan C Boldog FL Yang M Vernet C et al. PDGF-D, a new protease-activated growth factor Nat Cell Biol 2001, 3:517-521. 10.1038/ 35074593 11331882
18. Claesson-Welsh L Eriksson A Westermark B Heldin CH cDNA cloning and expression of the human A-type platelet-derived growth factor (PDGF) receptor establishes structural similarity to the B-type PDGF receptor Proc Natl Acad Sci USA 1989, 86:4917-4921. 297526 2544881 10.1073/ pnas.86.13.4917
19. Matsui T Heidaran M Miki T Popescu N La Rochelle W Kraus M Pierce J Aaronson S Isolation of a novel receptor cDNA establishes the existence of two PDGF receptor genes Science 1989, 243:800-804. 10.1126/ science.2536956 2536956
20. Yarden Y Escobedo JA Kuang WJ Yang-Feng TL Daniel TO Tremble PM Chen EY Ando ME Harkins RN Francke U et al. Structure of the receptor for platelet-derived growth factor helps define a family of closely related growth factor receptors Nature 1986, 323:226-232. 10.1038/323226a0 3020426
21. Andrae J Gallini R Betsholtz C Role of platelet-derived growth factors in physiology and medicine Genes Dev 2008, 22:1276-1312. 10.1101/ gad.1653708 18483217
22. Heldin CH Ostman A Ronnstrand L Signal transduction via platelet-derived growth factor receptors Biochim Biophys Acta 1998, 1378:F79-113. 9739761
23. Hoch RV Soriano P Roles of PDGF in animal development Development 2003, 130:4769-4784. 10.1242/dev.00721 12952899
24. Narita M Usui A Niikura K Nozaki H Khotib J Nagumo Y Yajima Y Suzuki T Protease-activated receptor-1 and platelet-derived growth factor in spinal cord neurons are implicated in neuropathic pain after nerve injury J Neurosci 2005, 25:10000-10009. 10.1523/JNEUROSCI.2507-05.2005 16251448
25. Oya T Zhao YL Takagawa K Kawaguchi M Shirakawa K Yamauchi T Sasahara M Platelet-derived growth factor-b expression induced after rat peripheral nerve injuries Glia 2002, 38:303-312. 10.1002/glia.10074 12007143
26. Sasahara M Fries JW Raines EW Gown AM Westrum LE Frosch MP Bonthron DT Ross R Collins T PDGF B-chain in neurons of the central nervous system, posterior pituitary, and in a transgenic model Cell 1991, 64:217-227. 10.1016/0092-8674(91)90223-L 1986868
27. Kitadai Y Sasaki T Kuwai T Nakamura T Bucana CD Hamilton SR Fidler IJ Expression of activated platelet-derived growth factor receptor in stromal cells of human colon carcinomas is associated with metastatic potential Int J Cancer 2006, 119:2567-2574. 10.1002/ijc.22229 16988946
28. Bowen-Pope DF Malpass TW Foster DM Ross R Platelet-derived growth factor in vivo: Levels, activity, and rate of clearance Blood 1984, 64:458-469. 6331547
29. Ledeboer A Sloane EM Milligan ED Frank MG Mahony JH Maier SF Watkins LR Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation Pain 2005, 115:71-83. 10.1016/j.pain.2005.02.009 15836971
30. Tikka T Fiebich BL Goldsteins G Keinanen R Koistinaho J Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia J Neurosci 2001, 21:2580-2588. 11306611
31. Hua XY Svensson CI Matsui T Fitzsimmons B Yaksh TL Webb M Intrathecal minocycline attenuates peripheral inflammation-induced hyperalgesia by inhibiting p38 MAPK in spinal microglia Eur J Neurosci 2005, 22:2431-2440. 10.1111/j.1460-9568.2005.04451.x 16307586
32. Piao ZG Cho IH Park CK Hong JP Choi SY Lee SJ Lee S Park K Kim JS Oh SB Activation of glia and microglial p38 MAPK in medullary dorsal horn contributes to tactile hypersensitivity following trigeminal sensory nerve injury Pain 2006, 121:219-231. 10.1016/j.pain.2005.12.023 16495005
33. Kobayashi K Yamanaka H Fukuoka T Dai Y Obata K Noguchi K P2Y12 receptor upregulation in activated microglia is a gateway of p38 signaling and neuropathic pain J Neurosci 2008, 28:2892-2902. 10.1523/ JNEUROSCI.5589-07.2008 18337420
34. Chessell IP Hatcher JP Bountra C Michel AD Hughes JP Green P Egerton J Murfin M Richardson J Peck WL et al. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain Pain 2005, 114:386-396. 10.1016/j.pain.2005.01.002 15777864
35. Smits A Kato M Westermark B Nister M Heldin CH Funa K Neurotrophic activity of platelet-derived growth factor (PDGF): Rat neuronal cells possess functional PDGF beta-type receptors and respond to PDGF Proc Natl Acad Sci USA 1991, 88:8159-8163. 52466 1654560 10.1073/ pnas.88.18.8159
36. Yeh HJ Silos-Santiago I Wang YX George RJ Snider WD Deuel TF Developmental expression of the platelet-derived growth factor alpha-receptor gene in mammalian central nervous system Proc Natl Acad Sci USA 1993, 90:1952-1956. 45998 8446614 10.1073/pnas.90.5.1952
37. Oumesmar BN Vignais L Baron-Van Evercooren A Developmental expression of platelet-derived growth factor alpha-receptor in neurons and glial cells of the mouse CNS J Neurosci 1997, 17:125-139. 8987742
38. Raff MC Glial cell diversification in the rat optic nerve Science 1989, 243:1450-1455. 10.1126/science.2648568 2648568
39. Reeve AJ Patel S Fox A Walker K Urban L Intrathecally administered endotoxin or cytokines produce allodynia, hyperalgesia and changes in spinal cord neuronal responses to nociceptive stimuli in the rat Eur J Pain 2000, 4:247-257. 10.1053/eujp.2000.0177 10985868
40. Viviani B Bartesaghi S Gardoni F Vezzani A Behrens MM Bartfai T Binaglia M Corsini E Di Luca M Galli CL Marinovich M Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases J Neurosci 2003, 23:8692-8700. 14507968
41. Wang S Cheng Q Malik S Yang J Interleukin-1beta inhibits gamma-aminobutyric acid type A (GABA(A)) receptor current in cultured hippocampal neurons J Pharmacol Exp Ther 2000, 292:497-504. 10640285
42. Ikeda H Tsuda M Inoue K Murase K Long-term potentiation of neuronal excitation by neuron-glia interactions in the rat spinal dorsal horn Eur J Neurosci 2007, 25:1297-1306. 10.1111/j.1460-9568.2007.05386.x 17425556
43. Kawasaki Y Zhang L Cheng JK Ji RR Cytokine mechanisms of central sensitization: Distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord J Neurosci 2008, 28:5189-5194. 2408767 18480275 10.1523/JNEUROSCI.3338-07.2008
44. Nakajima K Shimojo M Hamanoue M Ishiura S Sugita H Kohsaka S Identification of elastase as a secretory protease from cultured rat microglia J Neurochem 1992, 58:1401-1408. 10.1111/ j.1471-4159.1992.tb11356.x 1548474
45. Kim SH Chung JM An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat Pain 1992, 50:355-363. 10.1016/0304-3959(92)90041-9 1333581
46. Chaplan SR Bach FW Pogrel JW Chung JM Yaksh TL Quantitative assessment of tactile allodynia in the rat paw J Neurosci Methods 1994, 53:55-63. 10.1016/0165-0270(94)90144-9 7990513
47. Park CS Schneider IC Haugh JM Kinetic analysis of platelet-derived growth factor receptor/phosphoinositide 3-kinase/Akt signaling in fibroblasts J Biol Chem 2003, 278:37064-37072. 10.1074/jbc.M304968200 12871957