Selective inhibition of JNK with a peptide inhibitor attenuates pain hypersensitivity and tumor growth in a mouse skin cancer pain model

Experimental Neurology

Volumn 219, Issue 1, 2009, Pages 146-155

  Gao, Yong Jing ^a   Cheng, Jen Kun ^a,b,c,d   Zeng, Qing ^a   Xu, Zhen Zhong ^a   Decosterd, Isabelle ^e,f   Xu, Xiaoyin ^a   Ji, Ru Rong ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b MACKAY MEMORIAL HOSPITAL   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d NURSING AND MANAGEMENT COLLEGE   (Taiwan)

^e LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^f UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; ANTINEOPLASTIC AGENT; MORPHINE; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1 INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER PAIN; CONTROLLED STUDY; DRUG EFFICACY; DRUG RESPONSE; ENZYME ACTIVATION; ENZYME INHIBITION; EVENING DOSAGE; IN VITRO STUDY; IN VIVO STUDY; MELANOMA; MORNING DOSAGE; MOUSE; NERVE FIBER; NONHUMAN; PAIN ASSESSMENT; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SPINAL CORD; SPINAL GANGLION; TREATMENT DURATION; TUMOR GROWTH;

ACTIVATING TRANSCRIPTION FACTOR 3; ANALGESICS, OPIOID; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; HYPERALGESIA; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MELANOMA; MICE; MICE, INBRED C57BL; MORPHINE; PAIN; PAIN MEASUREMENT; PEPTIDES; PERIPHERAL NERVOUS SYSTEM DISEASES; SENSORY RECEPTOR CELLS; SKIN NEOPLASMS;

EID: 68549125155     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.05.006     Document Type: Article

References (52)

1. Alexaki V.I., Javelaud D., and Mauviel A. JNK supports survival in melanoma cells by controlling cell cycle arrest and apoptosis. Pigment Cell Melanoma Res. 21 (2008) 429-438
2. Andoh T., Sugiyama K., Fujita M., Iida Y., Nojima H., Saiki I., and Kuraishi Y. Pharmacological evaluation of morphine and non-opioid analgesic adjuvants in a mouse model of skin cancer pain. Biol. Pharm. Bull. 31 (2008) 520-522
3. Borsello T., and Bonny C. Use of cell-permeable peptides to prevent neuronal degeneration. Trends Mol. Med. 10 (2004) 239-244
4. Bulka A., Plesan A., Xu X.J., and Wiesenfeld-Hallin Z. Reduced tolerance to the anti-hyperalgesic effect of methadone in comparison to morphine in a rat model of mononeuropathy. Pain 95 (2002) 103-109
5. Cain D.M., Wacnik P.W., Turner M., Wendelschafer-Crabb G., Kennedy W.R., Wilcox G.L., and Simone D.A. Functional interactions between tumor and peripheral nerve: changes in excitability and morphology of primary afferent fibers in a murine model of cancer pain. J. Neurosci. 21 (2001) 9367-9376
6. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., and Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods 53 (1994) 55-63
7. Constantin C.E., Mair N., Sailer C.A., Andratsch M., Xu Z.Z., Blumer M.J., Scherbakov N., Davis J.B., Bluethmann H., Ji R.R., and Kress M. Endogenous tumor necrosis factor alpha (TNFalpha) requires TNF receptor type 2 to generate heat hyperalgesia in a mouse cancer model. J. Neurosci. 28 (2008) 5072-5081
8. Craft N., Bruhn K.W., Nguyen B.D., Prins R., Liau L.M., Collisson E.A., De A., Kolodney M.S., Gambhir S.S., and Miller J.F. Bioluminescent imaging of melanoma in live mice. J. Invest. Dermatol. 125 (2005) 159-165
9. Eferl R., Ricci R., Kenner L., Zenz R., David J.P., Rath M., and Wagner E.F. Liver tumor development. c-Jun antagonizes the proapoptotic activity of p53. Cell 112 (2003) 181-192
10. Einspahr J.G., Thomas T.L., Saboda K., Nickolof B.J., Warneke J., Curiel-Lewandrowski C., Ranger-Moore J., Duckett L., Bangert J., Fruehauf J.P., and Alberts D.S. Expression of vascular endothelial growth factor in early cutaneous melanocytic lesion progression. Cancer 110 (2007) 2519-2527
11. Ennis B.W., Fultz K.E., Smith K.A., Westwick J.K., Zhu D., Boluro-Ajayi M., Bilter G.K., and Stein B. Inhibition of tumor growth, angiogenesis, and tumor cell proliferation by a small molecule inhibitor of c-Jun N-terminal kinase. J. Pharmacol. Exp. Ther. 313 (2005) 325-332
12. Gao Y.J., Zhang L., Samad O.A., Suter M.R., Yasuhiko K., Xu Z.Z., Park J.Y., Lind A.L., Ma Q., and Ji R.R. JNK-induced MCP-1 production in spinal cord astrocytes contributes to central sensitization and neuropathic pain. J. Neurosci. 29 (2009) 4096-4108
13. Gurzov E.N., Bakiri L., Alfaro J.M., Wagner E.F., and Izquierdo M. Targeting c-Jun and JunB proteins as potential anticancer cell therapy. Oncogene 27 (2008) 641-652
14. Honore P., Rogers S.D., Schwei M.J., Salak-Johnson J.L., Luger N.M., Sabino M.C., Clohisy D.R., and 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 98 (2000) 585-598
15. Jemal A., Devesa S.S., Hartge P., and Tucker M.A. Recent trends in cutaneous melanoma incidence among whites in the United States. J. Natl. Cancer Inst. 93 (2001) 678-683
16. Ji R.R., Befort K., Brenner G.J., and Woolf C.J. ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J. Neurosci. 22 (2002) 478-485
17. Ji R.R., Kawasaki Y., Zhuang Z.Y., Wen Y.R., and Zhang Y.Q. Protein kinases as potential targets for the treatment of pathological pain. Handb. Exp. Pharmacol. (2007) 359-389
18. Jin S.X., Zhuang Z.Y., Woolf C.J., and Ji R.R. 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. 23 (2003) 4017-4022
19. Jorgensen K., Davidson B., and Florenes V.A. Activation of c-jun N-terminal kinase is associated with cell proliferation and shorter relapse-free period in superficial spreading malignant melanoma. Mod. Pathol. 19 (2006) 1446-1455
20. Krejsgaard T., Vetter-Kauczok C.S., Woetmann A., Lovato P., Labuda T., Eriksen K.W., Zhang Q., Becker J.C., and Odum N. Jak3- and JNK-dependent vascular endothelial growth factor expression in cutaneous T-cell lymphoma. Leukemia 20 (2006) 1759-1766
21. Leach B.C., Kulbersh J.S., Day T.A., and Cook J. Cranial neuropathy as a presenting sign of recurrent aggressive skin cancer. Dermatol. Surg. 34 (2008) 483-497
22. Lehembre S., Carvalho P., Young P., Josset V., Hacpille L., and Joly P. Palliative care management of patients in a dermatology department. Ann. Dermatol. Venereol. 133 (2006) 967-970
23. Lewis J.W., Shavit Y., Terman G.W., Gale R.P., and Liebeskind J.C. Stress and morphine affect survival of rats challenged with a mammary ascites tumor (MAT 13762B). Nat. Immun. Cell Growth Regul. 3 (1983) 43-50
24. Lopez-Bergami P., Huang C., Goydos J.S., Yip D., Bar-Eli M., Herlyn M., Smalley K.S., Mahale A., Eroshkin A., Aaronson S., and Ronai Z. Rewired ERK-JNK signaling pathways in melanoma. Cancer Cell 11 (2007) 447-460
25. Luger N.M., Sabino M.A., Schwei M.J., Mach D.B., Pomonis J.D., Keyser C.P., Rathbun M., Clohisy D.R., Honore P., Yaksh T.L., and Mantyh P.W. Efficacy of systemic morphine suggests a fundamental difference in the mechanisms that generate bone cancer vs inflammatory pain. Pain 99 (2002) 397-406
26. Malmberg A.B., Chen C., Tonegawa S., and Basbaum A.I. Preserved acute pain and reduced neuropathic pain in mice lacking PKCgamma. Science 278 (1997) 279-283
27. Mantyh P.W. Cancer pain and its impact on diagnosis, survival and quality of life. Nat. Rev. Neurosci. 7 (2006) 797-809
28. Mao-Ying Q.L., Cui K.M., Liu Q., Dong Z.Q., Wang W., Wang J., Sha H., Wu G.C., and Wang Y.Q. Stage-dependent analgesia of electro-acupuncture in a mouse model of cutaneous cancer pain. Eur. J. Pain 10 (2006) 689-694
29. Mao J. Opioid-induced abnormal pain sensitivity: implications in clinical opioid therapy. Pain 100 (2002) 213-217
30. McNicol E., Horowicz-Mehler N., Fisk R.A., Bennett K., Gialeli-Goudas M., Chew P.W., Lau J., and Carr D. Management of opioid side effects in cancer-related and chronic noncancer pain: a systematic review. J. Pain 4 (2003) 231-256
31. Menendez L., Lastra A., Fresno M.F., Llames S., Meana A., Hidalgo A., and Baamonde A. Initial thermal heat hypoalgesia and delayed hyperalgesia in a murine model of bone cancer pain. Brain Res. 969 (2003) 102-109
32. Mercadante S. Malignant bone pain: pathophysiology and treatment. Pain 69 (1997) 1-18
33. Nateri A.S., Spencer-Dene B., and Behrens A. Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature 437 (2005) 281-285
34. Negin B.P., Riedel E., Oliveria S.A., Berwick M., Coit D.G., and Brady M.S. Symptoms and signs of primary melanoma: important indicators of Breslow depth. Cancer 98 (2003) 344-348
35. Obata K., and Noguchi K. MAPK activation in nociceptive neurons and pain hypersensitivity. Life Sci. 74 (2004) 2643-2653
36. Obata K., Yamanaka H., Kobayashi K., Dai Y., Mizushima T., Katsura H., Fukuoka T., Tokunaga A., and Noguchi K. 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 (2004) 10211-10222
37. Raghavendra V., Rutkowski M.D., and DeLeo J.A. The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats. J. Neurosci. 22 (2002) 9980-9989
38. Sasamura T., Nakamura S., Iida Y., Fujii H., Murata J., Saiki I., Nojima H., and Kuraishi Y. Morphine analgesia suppresses tumor growth and metastasis in a mouse model of cancer pain produced by orthotopic tumor inoculation. Eur. J. Pharmacol. 441 (2002) 185-191
39. Schafers M., Svensson C.I., Sommer C., and Sorkin L.S. Tumor necrosis factor-alpha induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons. J. Neurosci. 23 (2003) 2517-2521
40. Schwei M.J., Honore P., Rogers S.D., Salak-Johnson J.L., Finke M.P., Ramnaraine M.L., Clohisy D.R., and Mantyh P.W. Neurochemical and cellular reorganization of the spinal cord in a murine model of bone cancer pain. J. Neurosci. 19 (1999) 10886-10897
41. Suckfuell M., Canis M., Strieth S., Scherer H., and Haisch A. Intratympanic treatment of acute acoustic trauma with a cell-permeable JNK ligand: a prospective randomized phase I/II study. Acta Otolaryngol. 127 (2007) 938-942
42. Svensson C.I., Marsala M., Westerlund A., Calcutt N.A., Campana W.M., Freshwater J.D., Catalano R., Feng Y., Protter A.A., Scott B., and Yaksh T.L. Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing. J. Neurochem. 86 (2003) 1534-1544
43. Svensson C.I., Medicherla S., Malkmus S., Jiang Y., Ma J.Y., Kerr I., Brainin-Mattos J., Powell H.C., Luo Z.D., Chakravarty S., Dugar S., Higgins L.S., Protter A.A., and Yaksh T.L. Role of p38 mitogen activated protein kinase in a model of osteosarcoma-induced pain. Pharmacol. Biochem. Behav. 90 4 (2008) 664-675
44. Tawfik V.L., LaCroix-Fralish M.L., Nutile-McMenemy N., and DeLeo J.A. Transcriptional and translational regulation of glial activation by morphine in a rodent model of neuropathic pain. J. Pharmacol. Exp. Ther. 313 (2005) 1239-1247
45. Tsujino H., Kondo E., Fukuoka T., Dai Y., Tokunaga A., Miki K., Yonenobu K., Ochi T., and Noguchi K. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol. Cell. Neurosci. 15 (2000) 170-182
46. Wacnik P.W., Eikmeier L.J., Ruggles T.R., Ramnaraine M.L., Walcheck B.K., Beitz A.J., and Wilcox G.L. Functional interactions between tumor and peripheral nerve: morphology, algogen identification, and behavioral characterization of a new murine model of cancer pain. J. Neurosci. 21 (2001) 9355-9366
47. Wang Z., Gardell L.R., Ossipov M.H., Vanderah T.W., Brennan M.B., Hochgeschwender U., Hruby V.J., Malan Jr. T.P., Lai J., and Porreca F. Pronociceptive actions of dynorphin maintain chronic neuropathic pain. J. Neurosci. 21 (2001) 1779-1786
48. Xia H.H., He H., De Wang J., Gu Q., Lin M.C., Zou B., Yu L.F., Sun Y.W., Chan A.O., Kung H.F., and Wong B.C. Induction of apoptosis and cell cycle arrest by a specific c-Jun NH2-terminal kinase (JNK) inhibitor, SP-600125, in gastrointestinal cancers. Cancer Lett. 241 (2006) 268-274
49. Yoshino Y., Aoyagi M., Tamaki M., Duan L., Morimoto T., and Ohno K. Activation of p38 MAPK and/or JNK contributes to increased levels of VEGF secretion in human malignant glioma cells. Int. J. Oncol. 29 (2006) 981-987
50. Zhang H.W., Iida Y., Andoh T., Nojima H., Murata J., Saiki I., and Kuraishi Y. Mechanical hypersensitivity and alterations in cutaneous nerve fibers in a mouse model of skin cancer pain. J. Pharmacol. Sci. 91 (2003) 167-170
51. Zhang R.X., Liu B., Wang L., Ren K., Qiao J.T., Berman B.M., and Lao L. Spinal glial activation in a new rat model of bone cancer pain produced by prostate cancer cell inoculation of the tibia. Pain 118 (2005) 125-136
52. Zhuang Z.Y., Wen Y.R., Zhang D.R., Borsello T., Bonny C., Strichartz G.R., Decosterd I., and Ji R.R. 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. 26 (2006) 3551-3560