Transforming growth factor-β1 impairs neuropathic pain through pleiotropic effects

Molecular Pain

Volumn 5, Issue , 2009, Pages

  Echeverry, Stefania ^a   Shi, Xiang Qun ^a   Haw, Alexandra ^a   Liu, Hong ^b   Zhang, Zhong Wei ^b   Zhang, Ji ^a  

^a MCGILL UNIVERSITY   (Canada)

^b JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; MONOCYTE CHEMOTACTIC PROTEIN 1; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA1; ANTIINFLAMMATORY AGENT; NEUROPROTECTIVE AGENT; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENCY; DRUG TARGETING; HISTOPATHOLOGY; MALE; MICROENVIRONMENT; MICROGLIA; MYELITIS; NEUROPATHIC PAIN; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ANIMAL; CELL PROLIFERATION; DRUG EFFECT; HYPERALGESIA; INFLAMMATION; INTRASPINAL DRUG ADMINISTRATION; METABOLISM; NERVE CELL; PAIN; PATHOLOGY; PERIPHERAL NERVE; SIGNAL TRANSDUCTION; SPINAL CORD; SPRAGUE DAWLEY RAT;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ASTROCYTES; CELL PROLIFERATION; HYPERALGESIA; INFLAMMATION; INJECTIONS, SPINAL; MALE; MICROGLIA; NEURONS; NEUROPROTECTIVE AGENTS; PAIN; PERIPHERAL NERVES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD PROTEINS; SPINAL CORD; TRANSFORMING GROWTH FACTOR BETA1;

EID: 65349147156     PISSN: 17448069     EISSN: None     Source Type: Journal    
DOI: 10.1186/1744-8069-5-16     Document Type: Article

References (47)

1. Sindrup SH Jensen TS Efficacy of pharmacological treatments of neuropathic pain: An update and effect related to mechanism of drug action Pain 1999, 83:389-400. 10.1016/S0304-3959(99)00154-2 10568846
2. Watson CP The treatment of neuropathic pain: Antidepressants and opioids Clin J Pain 2000, 16:S49-S55. 10870740
3. Scholz J Woolf CJ The neuropathic pain triad: Neurons, immune cells and glia Nat Neurosci 2007, 10:1361-1368. 10.1038/nn1992 17965656
4. Colburn RW Rickman AJ DeLeo JA The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior Exp Neurol 1999, 157:289-304. 10.1006/exnr.1999.7065 10364441
5. Zhang J Hoffert C Vu HK Groblewski T Ahmad S O'Donnell D Induction of CB2 receptor expression in the rat spinal cord of neuropathic but not inflammatory chronic pain models Eur J Neurosci 2003, 17:2750-2754. 10.1046/j.1460-9568.2003.02704.x 12823482
6. Fu KY Light AR Matsushima GK Maixner W Microglial reactions after subcutaneous formalin injection into the rat hind paw Brain Res 1999, 825:59-67. 10.1016/S0006-8993(99)01186-5 10216173
7. Echeverry S Shi XQ Zhang J Characterization of cell proliferation in rat spinal cord following peripheral nerve injury and the relationship with neuropathic pain Pain 2008, 135:37-47. 10.1016/j.pain.2007.05.002 17560721
8. Zhang J Shi XQ Echeverry S Mogil JS De Koninck Y Rivest S Expression of CCR2 in both resident and bone marrow-derived microglia plays a critical role in neuropathic pain J Neurosci 2007, 27:12396-12406. 10.1523/ JNEUROSCI.3016-07.2007 17989304
9. Zhang J De Koninck Y Spatial and temporal relationship between monocyte chemoattractant protein-1 expression and spinal glial activation following peripheral nerve injury J Neurochem 2006, 97:772-783. 10.1111/ j.1471-4159.2006.03746.x 16524371
10. Nesic O Lee J Johnson KM Ye Z Xu GY Unabia GC Wood TG McAdoo DJ Westlund KN Hulsebosch CE Regino Perez-Polo J Transcriptional profiling of spinal cord injury-induced central neuropathic pain J Neurochem 2005, 95:998-1014. 10.1111/j.1471-4159.2005.03462.x 16219025
11. Mantyh PW Clohisy DR Koltzenburg M Hunt SP Molecular mechanisms of cancer pain Nat Rev Cancer 2002, 2:201-209. 10.1038/nrc747 11990856
12. Scholz J Woolf CJ The neuropathic pain triad: Neurons, immune cells and glia Nat Neurosci 2007, 10:1361-1368. 10.1038/nn1992 17965656
13. Milligan ED Watkins LR Pathological and protective roles of glia in chronic pain Nat Rev Neurosci 2009, 10:23-36. 10.1038/nrn2533 19096368
14. Suter MR Wen YR Decosterd I Ji RR Do glial cells control pain? Neuron Glia Biol 2007, 3:255-268. 2394739 18504511 10.1017/S1740925X08000100
15. Blobe GC Schiemann WP Lodish HF Role of transforming growth factor beta in human disease N Engl J Med 2000, 342:1350-1358. 10.1056/ NEJM200005043421807 10793168
16. Bottner M Krieglstein K Unsicker K The transforming growth factor-betas: structure, signaling, and roles in nervous system development and functions J Neurochem 2000, 75:2227-2240. 10.1046/ j.1471-4159.2000.0752227.x 11080174
17. Dennler S Goumans MJ ten DP Transforming growth factor beta signal transduction J Leukoc Biol 2002, 71:731-740. 11994497
18. Flanders KC Ren RF Lippa CF Transforming growth factor-betas in neurodegenerative disease Prog Neurobiol 1998, 54:71-85. 10.1016/ S0301-0082(97)00066-X 9460794
19. Lippa CF Smith TW Flanders KC Transforming growth factor-beta: Neuronal and glial expression in CNS degenerative diseases Neurodegeneration 1995, 4:425-432. 10.1006/neur.1995.0051 8846236
20. Krieglstein K Henheik P Farkas L Jaszai J Galter D Krohn K Unsicker K Glial cell line-derived neurotrophic factor requires transforming growth factor-beta for exerting its full neurotrophic potential on peripheral and CNS neurons J Neurosci 1998, 18:9822-9834. 9822741
21. Suzumura A Sawada M Yamamoto H Marunouchi T Transforming growth factor-beta suppresses activation and proliferation of microglia in vitro J Immunol 1993, 151:2150-2158. 8345199
22. Benveniste EN Tang LP Law RM Differential regulation of astrocyte TNF-alpha expression by the cytokines TGF-beta, IL-6 and IL-10 Int J Dev Neurosci 1995, 13:341-349. 10.1016/0736-5748(94)00061-7 7572286
23. Vodovotz Y Geiser AG Chesler L Letterio JJ Campbell A Lucia MS Sporn MB Roberts AB Spontaneously increased production of nitric oxide and aberrant expression of the inducible nitric oxide synthase in vivo in the transforming growth factor beta 1 null mouse J Exp Med 1996, 183:2337-2342. 2192554 8642342 10.1084/jem.183.5.2337
24. Seltzer Z Dubner R Shir Y A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury Pain 1990, 43:205-218. 10.1016/0304-3959(90)91074-S 1982347
25. Livak KJ Schmittgen TD Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 2001, 25:402-408. 10.1006/meth.2001.1262 11846609
26. Dunker N Schuster N Krieglstein K TGF-beta modulates programmed cell death in the retina of the developing chick embryo Development 2001, 128:1933-1942. 11493517
27. Krieglstein K Richter S Farkas L Schuster N Dunker N Oppenheim RW Unsicker K Reduction of endogenous transforming growth factors beta prevents ontogenetic neuron death Nat Neurosci 2000, 3:1085-1090. 10.1038/80598 11036264
28. Krieglstein K Strelau J Schober A Sullivan A Unsicker K TGF-beta and the regulation of neuron survival and death J Physiol Paris 2002, 96:25-30. 10.1016/S0928-4257(01)00077-8 11755780
29. Tesseur I Wyss-Coray T A role for TGF-beta signaling in neurodegeneration: Evidence from genetically engineered models Curr Alzheimer Res 2006, 3:505-513. 10.2174/156720506779025297 17168649
30. Tesseur I Zou K Esposito L Bard F Berber E Can JV Lin AH Crews L Tremblay P Mathews P Mucke L Masliah E Wyss-Coray T Deficiency in neuronal TGF-beta signaling promotes neurodegeneration and Alzheimer's pathology J Clin Invest 2006, 116:3060-3069. 1626127 17080199 10.1172/ JCI27341
31. Krieglstein K Suter-Crazzolara C Fischer WH Unsicker K TGF-beta superfamily members promote survival of midbrain dopaminergic neurons and protect them against MPP+ toxicity EMBO J 1995, 14:736-742. 398139 7882977
32. Brionne TC Tesseur I Masliah E Wyss-Coray T Loss of TGF-beta 1 leads to increased neuronal cell death and microgliosis in mouse brain Neuron 2003, 40:1133-1145. 10.1016/S0896-6273(03)00766-9 14687548
33. Tsujino H Kondo E Fukuoka T Dai Y Tokunaga A Miki K Yonenobu K Ochi T Noguchi K Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: A novel neuronal marker of nerve injury Mol Cell Neurosci 2000, 15:170-182. 10.1006/mcne.1999.0814 10673325
34. Kataoka K Kanje M Dahlin LB Induction of activating transcription factor 3 after different sciatic nerve injuries in adult rats Scand J Plast Reconstr Surg Hand Surg 2007, 41:158-166. 10.1080/02844310701318288 17701728
35. Luo MC Zhang DQ Ma SW Huang YY Shuster SJ Porreca F Lai J An efficient intrathecal delivery of small interfering RNA to the spinal cord and peripheral neurons Mol Pain 2005, 1:29. 1253531 16191203 10.1186/ 1744-8069-1-29
36. Xiao BG Bai XF Zhang GX Link H Transforming growth factor-beta1 induces apoptosis of rat microglia without relation to bcl-2 oncoprotein expression Neurosci Lett 1997, 226:71-74. 10.1016/S0304-3940(97)00234-6 9159492
37. Toru-Delbauffe D Baghdassarian-Chalaye D Gavaret JM Courtin F Pomerance M Pierre M Effects of transforming growth factor beta 1 on astroglial cells in culture J Neurochem 1990, 54:1056-1061. 10.1111/ j.1471-4159.1990.tb02357.x 1968087
38. Morganti-Kossmann MC Kossmann T Brandes ME Mergenhagen SE Wahl SM Autocrine and paracrine regulation of astrocyte function by transforming growth factor-beta J Neuroimmunol 1992, 39:163-173. 10.1016/ 0165-5728(92)90185-N 1320057
39. Makwana M Jones LL Cuthill D Heuer H Bohatschek M Hristova M Friedrichsen S Ormsby I Bueringer D Koppius A Bauer K Doetschman T Raivich G Endogenous transforming growth factor beta 1 suppresses inflammation and promotes survival in adult CNS J Neurosci 2007, 27:11201-11213. 10.1523/JNEUROSCI.2255-07.2007 17942715
40. 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
41. Samad TA Moore KA Sapirstein A Billet S Allchorne A Poole S Bonventre JV Woolf CJ Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity Nature 2001, 410:471-475. 10.1038/35068566 11260714
42. Ji RR Suter MR p38 MAPK, microglial signaling, and neuropathic pain Mol Pain 2007, 3:33. 2186318 17974036 10.1186/1744-8069-3-33
43. 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
44. Dixon WJ Efficient analysis of experimental observations Annu Rev Pharmacol Toxicol 1980, 20:441-462. 10.1146/annurev.pa.20.040180.002301 7387124
45. Hargreaves K Dubner R Brown F Flores C Joris J A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia Pain 1988, 32:77-88. 10.1016/0304-3959(88)90026-7 3340425
46. Yaksh TL Rudy TA Chronic catheterization of the spinal subarachnoid space Physiol Behav 1976, 17:1031-1036. 10.1016/0031-9384(76)90029-9 14677603
47. Zhang J Rivest S Distribution, regulation and colocalization of the genes encoding the EP2- and EP4-PGE2 receptors in the rat brain and neuronal responses to systemic inflammation Eur J Neurosci 1999, 11:2651-2668. 10.1046/j.1460-9568.1999.00682.x 10457163