Expression genetics identifies spinal mechanisms supporting formalin late phase behaviors

Molecular Pain

Volumn 6, Issue , 2010, Pages

  Li, Xiangqi ^a,b   Sahbaie, Peyman ^a,b   Zheng, Ming ^b   Ritchie, Jennifer ^c   Peltz, Gary ^b   Mogil, Jeffrey S ^c   Clark, J David ^a,b  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; FORMALDEHYDE; MESSENGER RNA; STRESS ACTIVATED PROTEIN KINASE 1; ANTHRA(1,9 CD)PYRAZOL 6(2H) ONE; ANTHRA(1,9-CD)PYRAZOL-6(2H)-ONE; ANTHRACENE DERIVATIVE; ENZYME INHIBITOR; FIXATIVE; STRESS ACTIVATED PROTEIN KINASE;

ANALGESIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC DATABASE; LICKING; MOUSE; MOUSE STRAIN; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD; STRAIN DIFFERENCE; ANIMAL; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETICS; INTRASPINAL DRUG ADMINISTRATION; METABOLISM; NOCICEPTIVE RECEPTOR; PAIN; PAIN ASSESSMENT; PATHOPHYSIOLOGY; PHYSIOLOGY; REACTION TIME; SPECIES DIFFERENCE;

ANIMALS; ANTHRACENES; BEHAVIOR, ANIMAL; ENZYME INHIBITORS; FIXATIVES; FORMALDEHYDE; GENE EXPRESSION REGULATION; GENOME-WIDE ASSOCIATION STUDY; INJECTIONS, SPINAL; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; MICE, INBRED STRAINS; NOCICEPTORS; PAIN; PAIN MEASUREMENT; REACTION TIME; RNA, MESSENGER; SPECIES SPECIFICITY; SPINAL CORD;

EID: 77949456126     PISSN: 17448069     EISSN: None     Source Type: Journal    
DOI: 10.1186/1744-8069-6-11     Document Type: Article

References (45)

1. Mogil JS, Ritchie J, Sotocinal SG, Smith SB, Croteau S, Levitin DJ, Naumova AK. Screening for pain phenotypes: analysis of three congenic mouse strains on a battery of nine nociceptive assays. Pain 2006, 126:24-34. 10.1016/j.pain.2006.06.004, 16842916.
2. Dubuisson D, Dennis SG. The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats. Pain 1977, 4:161-174. 10.1016/0304-3959(77)90130-0, 564014.
3. Hunskaar S, Hole K. The formalin test in mice: dissociation between inflammatory and non-inflammatory pain. Pain 1987, 30:103-114. 10.1016/0304-3959(87)90088-1, 3614974.
4. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, Zhao M, Hayward NJ, Chong JA, Julius D, Moran MM, Fanger CM. TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci USA 2007, 104:13525-13530. 10.1073/pnas.0705924104, 1941642,1941642, 17686976.
5. Clavelou P, Pajot J, Dallel R, Raboisson P. Application of the formalin test to the study of orofacial pain in the rat. Neurosci Lett 1989, 103:349-353. 10.1016/0304-3940(89)90125-0, 2812522.
6. Ossipov MH, Jerussi TP, Ren K, Sun H, Porreca F. Differential effects of spinal (R)-ketoprofen and (S)-ketoprofen against signs of neuropathic pain and tonic nociception: evidence for a novel mechanism of action of (R)-ketoprofen against tactile allodynia. Pain 2000, 87:193-199. 10.1016/S0304-3959(00)00280-3, 10924812.
7. Moore PK, Babbedge RC, Wallace P, Gaffen ZA, Hart SL. 7-Nitro indazole, an inhibitor of nitric oxide synthase, exhibits anti-nociceptive activity in the mouse without increasing blood pressure. Br J Pharmacol 1993, 108:296-297. 1907983, 7680591.
8. Munro G. Pharmacological assessment of the rat formalin test utilizing the clinically used analgesic drugs gabapentin, lamotrigine, morphine, duloxetine, tramadol and ibuprofen: influence of low and high formalin concentrations. Eur J Pharmacol 2009, 605:95-102. 10.1016/j.ejphar.2009.01.004, 19168051.
9. Abram SE, Yaksh TL. Systemic lidocaine blocks nerve injury-induced hyperalgesia and nociceptor-driven spinal sensitization in the rat. Anesthesiology 1994, 80:383-391.
10. Ji RR, Baba H, Brenner GJ, Woolf CJ. Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 1999, 2:1114-1119. 10.1038/16040, 10570489.
11. Vissers KC, Geenen F, Biermans R, Meert TF. Pharmacological correlation between the formalin test and the neuropathic pain behavior in different species with chronic constriction injury. Pharmacol Biochem Behav 2006, 84:479-486. 10.1016/j.pbb.2006.06.011, 16860855.
12. Lacroix-Fralish ML, Mogil JS. Progress in genetic studies of pain and analgesia. Annu Rev Pharmacol Toxicol 2009, 49:97-121. 10.1146/annurev-pharmtox-061008-103222, 2730377, 18834308.
13. Mogil JS, Wilson SG, Bon K, Lee SE, Chung K, Raber P, Pieper JO, Hain HS, Belknap JK, Hubert L, Elmer GI, Chung JM, Devor M. Heritability of nociception I: responses of 11 inbred mouse strains on 12 measures of nociception. Pain 1999, 80:67-82. 10.1016/S0304-3959(98)00197-3, 10204719.
14. Wilson SG, Chesler EJ, Hain H, Rankin AJ, Schwarz JZ, Call SB, Murray MR, West EE, Teuscher C, Rodriguez-Zas S, Belknap JK, Mogil JS. Identification of quantitative trait loci for chemical/inflammatory nociception in mice. Pain 2002, 96:385-391. 10.1016/S0304-3959(01)00489-4, 11973013.
15. LaCroix-Fralish ML, Mo G, Smith SB, Sotocinal SG, Ritchie J, Austin JS, Melmed K, Schorscher-Petcu A, Laferriere AC, Lee TH, Romanovsky D, Liao G, Behlke MA, Clark DJ, Peltz G, Séguéla P, Dobretsov M, Mogil JS. The beta3 subunit of the Na+, K+-ATPase mediates variable nociceptive sensitivity in the formalin test. Pain 2009, 144:294-302. 10.1016/j.pain.2009.04.028, 19464798.
16. Gibson G, Weir B. The quantitative genetics of transcription. Trends Genet 2005, 21:616-623. 10.1016/j.tig.2005.08.010, 16154229.
17. Li X, Shi X, Liang DY, Clark JD. Spinal CK2 regulates nociceptive signaling in models of inflammatory pain. Pain 2005, 115:182-190. 10.1016/j.pain.2005.02.025, 15836981.
18. Frazer KA, Eskin E, Kang HM, Bogue MA, Hinds DA, Beilharz EJ, Gupta RV, Montgomery J, Morenzoni MM, Nilsen GB, Pethiyagoda CL, Stuve LL, Johnson FM, Daly MJ, Wade CM, Cox DR. A sequence-based variation map of 8.27 million SNPs in inbred mouse strains. Nature 2007, 448:1050-1053. 10.1038/nature06067, 17660834.
19. Wang J, Liao G, Usuka J, Peltz G. Computational genetics: from mouse to human?. Trends Genet 2005, 21:526-532. 10.1016/j.tig.2005.06.010, 16009447.
20. Yang L, Zhang FX, Huang F, Lu YJ, Li GD, Bao L, Xiao HS, Zhang X. Peripheral nerve injury induces trans-synaptic modification of channels, receptors and signal pathways in rat dorsal spinal cord. Eur J Neurosci 2004, 19:871-883. 10.1111/j.0953-816X.2004.03121.x, 15009134.
21. Zhuang ZY, Wen YR, Zhang DR, Borsello T, Bonny C, Strichartz GR, Decosterd I, Ji RR. A peptide c-Jun N-terminal kinase (JNK) inhibitor blocks mechanical allodynia after spinal nerve ligation: respective roles of JNK activation in primary sensory neurons and spinal astrocytes for neuropathic pain development and maintenance. J Neurosci 2006, 26:3551-3560. 10.1523/JNEUROSCI.5290-05.2006, 16571763.
22. Daulhac L, Mallet C, Courteix C, Etienne M, Duroux E, Privat AM, Eschalier A, Fialip J. Diabetes-induced mechanical hyperalgesia involves spinal mitogen-activated protein kinase activation in neurons and microglia via N-methyl-D-aspartate-dependent mechanisms. Mol Pharmacol 2006, 70:1246-1254. 10.1124/mol.106.025478, 16868181.
23. Cao FL, Liu MG, Hao J, Li Z, Lu ZM, Chen J. Different roles of spinal p38 and c-Jun N-terminal kinase pathways in bee venom-induced multiple pain-related behaviors. Neurosci Lett 2007, 427:50-54. 10.1016/j.neulet.2007.09.005, 17923327.
24. Gao YJ, Ji RR. Activation of JNK pathway in persistent pain. Neurosci Lett 2008, 437:180-183. 10.1016/j.neulet.2008.03.017, 2486445, 18455869.
25. Katsura H, Obata K, Miyoshi K, Kondo T, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Sakagami M, Noguchi K. Transforming growth factor-activated kinase 1 induced in spinal astrocytes contributes to mechanical hypersensitivity after nerve injury. Glia 2008, 56:723-733. 10.1002/glia.20648, 18293403.
26. Gao YJ, Zhang L, Samad OA, Suter MR, Yasuhiko K, Xu ZZ, Park JY, Lind AL, Ma Q, Ji RR. JNK-induced MCP-1 production in spinal cord astrocytes contributes to central sensitization and neuropathic pain. J Neurosci 2009, 29:4096-4108. 10.1523/JNEUROSCI.3623-08.2009, 2682921, 19339605.
27. Hassanzadeh P, Ahmadiani A. Nitric oxide and c-Jun N-terminal kinase are involved in the development of dark neurons induced by inflammatory pain. Synapse 2006, 59:101-106. 10.1002/syn.20219, 16284960.
28. Qin M, Wang JJ, Cao R, Zhang H, Duan L, Gao B, Xiong YF, Chen LW, Rao ZR. The lumbar spinal cord glial cells actively modulate subcutaneous formalin induced hyperalgesia in the rat. Neurosci Res 2006, 55:442-450. 10.1016/j.neures.2006.04.017, 16759728.
29. Groppo R, Richter JD. Translational control from head to tail. Curr Opin Cell Biol 2009, 21:444-451. 10.1016/j.ceb.2009.01.011, 19285851.
30. Karin M, Gallagher E. From JNK to pay dirt: jun kinases, their biochemistry, physiology and clinical importance. IUBMB Life 2005, 57:283-295. 10.1080/15216540500097111, 16036612.
31. Gao M, Labuda T, Xia Y, Gallagher E, Fang D, Liu YC, Karin M. Jun turnover is controlled through JNK-dependent phosphorylation of the E3 ligase Itch. Science 2004, 306:271-275. 10.1126/science.1099414, 15358865.
32. Ahn YH, Kurie JM. MKK4/SEK1 is negatively regulated through a feedback loop involving the E3 ubiquitin ligase itch. J Biol Chem 2009,
33. Burke JE, Dennis EA. Phospholipase A2 structure/function, mechanism, and signaling. J Lipid Res 2009, 50(Suppl):S237-242. 10.1194/jlr.R800033-JLR200, 19011112.
34. Sung B, Wang S, Zhou B, Lim G, Yang L, Zeng Q, Lim JA, Wang JD, Kang JX, Mao J. Altered spinal arachidonic acid turnover after peripheral nerve injury regulates regional glutamate concentration and neuropathic pain behaviors in rats. Pain 2007, 131:121-131. 10.1016/j.pain.2006.12.020, 2478515, 17267128.
35. Kim DH, Fitzsimmons B, Hefferan MP, Svensson CI, Wancewicz E, Monia BP, Hung G, Butler M, Marsala M, Hua XY, Yaksh TL. Inhibition of spinal cytosolic phospholipase A(2) expression by an antisense oligonucleotide attenuates tissue injury-induced hyperalgesia. Neuroscience 2008, 154:1077-1087. 10.1016/j.neuroscience.2008.04.033, 2640426, 18511207.
36. Lucas KK, Svensson CI, Hua XY, Yaksh TL, Dennis EA. Spinal phospholipase A2 in inflammatory hyperalgesia: role of group IVA cPLA2. Br J Pharmacol 2005, 144:940-952. 10.1038/sj.bjp.0706116, 1576074, 15685208.
37. Catterall WA. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 2000, 26:13-25. 10.1016/S0896-6273(00)81133-2, 10798388.
38. Lopez-Santiago LF, Pertin M, Morisod X, Chen C, Hong S, Wiley J, Decosterd I, Isom LL. Sodium channel beta2 subunits regulate tetrodotoxin-sensitive sodium channels in small dorsal root ganglion neurons and modulate the response to pain. J Neurosci 2006, 26:7984-7994. 10.1523/JNEUROSCI.2211-06.2006, 16870743.
39. Drenth JP, Waxman SG. Mutations in sodium-channel gene SCN9A cause a spectrum of human genetic pain disorders. J Clin Invest 2007, 117:3603-3609. 10.1172/JCI33297, 2096434, 18060017.
40. Guo Y, Lu P, Farrell E, Zhang X, Weller P, Monshouwer M, Wang J, Liao G, Zhang Z, Hu S, Allard J, Shafer S, Usuka J, Peltz G. In silico and in vitro pharmacogenetic analysis in mice. Proc Natl Acad Sci USA 2007, 104:17735-17740. 10.1073/pnas.0700724104, 2077071, 17978195.
41. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy--analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 2004, 20:307-315. 10.1093/bioinformatics/btg405, 14960456.
42. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003, 31:e15. 10.1093/nar/gng015, 150247, 12582260.
43. Rodgers JL, Nicewander WA. Thirteen ways to look at the correlation coefficient. The American Statistician 1988, 42:59-66.
44. Liang D, Li X, Clark JD. Increased expression of Ca2+/calmodulin-dependent protein kinase II alpha during chronic morphine exposure. Neuroscience 2004, 123:769-775. 10.1016/j.neuroscience.2003.10.007, 14706789.
45. Liang DY, Shi X, Li X, Li J, Clark JD. The beta2 adrenergic receptor regulates morphine tolerance and physical dependence. Behav Brain Res 2007, 181:118-126. 10.1016/j.bbr.2007.03.037, 1989675, 17498818.