Selective inhibition of extracellular signal-regulated kinases 1/2 blocks nerve growth factor to brain-derived neurotrophic factor signaling and suppresses the development of and reverses already established pain behavior in rats

Neuroscience

Volumn 206, Issue , 2012, Pages 224-236

  Matsuoka, Y ^a   Yang, J ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

AZD6244; Drug therapy; MEK inhibitor; Neuropathic pain; NGF BDNF signaling

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 7; NERVE GROWTH FACTOR; SELUMETINIB; SMALL INTERFERING RNA;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MALE; NERVE COMPRESSION; NERVE INJURY; NEUROPATHIC PAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN INDUCTION; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN; SPINAL GANGLION; UPREGULATION;

ANIMALS; BENZIMIDAZOLES; BLOTTING, WESTERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; ENZYME INHIBITORS; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MALE; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASE 7; NERVE GROWTH FACTOR; NEURALGIA; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84862785495     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.01.002     Document Type: Article

References (47)

1. Adjei A.A., Cohen R.B., Franklin W., Morris C., Wilson D., Molina J.R., Hanson L.J., Gore L., Chow L., Leong S., Maloney L., Gordon G., Simmons H., Marlow A., Litwiler K., Brown S., Poch G., Kane K., Haney J., Eckhardt S.G. Phase I pharmacokinetic and pharmacodynamic study of the oral, small-molecule mitogen-activated protein kinase kinase 1/2 inhibitor AZD6244 (ARRY-142886) in patients with advanced cancers. J Clin Oncol 2008, 26:2139-2146.
2. Alter B.J., Zhao C., Karim F., Landreth G.E., Gereau R.W. Genetic targeting of ERK1 suggests a predominant role for ERK2 in murine pain models. J Neurosci 2010, 30:11537-11547.
3. Apfel S.C., Wright D.E., Wiideman A.M., Dormia C., Snider W.D., Kessler J.A. Nerve growth factor regulates the expression of brain-derived neurotrophic factor mRNA in the peripheral nervous system. Mol Cell Neurosci 1996, 7:134-142.
4. Bennett G.J., Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988, 33:87-107.
5. Bennouna J., Lang I., Valladares-Ayerbes M., Boer K., Adenis A., Escudero P., Kim T.Y., Pover G.M., Morris C.D., Douillard J.Y. A phase II, open-label, randomised study to assess the efficacy and safety of the MEK1/2 inhibitor AZD6244 (ARRY-142886) versus capecitabine monotherapy in patients with colorectal cancer who have failed one or two prior chemotherapeutic regimens. Invest New Drugs 2011, 29:1021-1028.
6. Cameron S.J., Malik S., Akaike M., Lerner-Marmarosh N., Yan C., Lee J.D., Abe J., Yang J. Regulation of epidermal growth factor-induced connexin 43 gap junction communication by big mitogen-activated protein kinase1/ERK5 but not ERK1/2 kinase activation. J Biol Chem 2003, 278:18682-18688.
7. Cao X.H., Byun H.S., Chen S.R., Cai Y.Q., Pan H.L. Reduction in voltage-gated K+ channel activity in primary sensory neurons in painful diabetic neuropathy: role of brain-derived neurotrophic factor. J Neurochem 2010, 114:1460-1475.
8. Cho H.J., Kim J.K., Zhou X.F., Rush R.A. Increased brain-derived neurotrophic factor immunoreactivity in rat dorsal root ganglia and spinal cord following peripheral inflammation. Brain Res 1997, 764:269-272.
9. Chow S., Hedley D., Grom P., Magari R., Jacobberger J.W., Shankey T.V. Whole blood fixation and permeabilization protocol with red blood cell lysis for flow cytometry of intracellular phosphorylated epitopes in leukocyte subpopulations. Cytometry A 2005, 67:4-17.
10. Coull J.A., Beggs S., Boudreau D., Boivin D., Tsuda M., Inoue K., Gravel C., Salter M.W., De Koninck Y. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 2005, 438:1017-1021.
11. Cui J.G., Holmin S., Mathiesen T., Meyerson B.A., Linderoth B. Possible role of inflammatory mediators in tactile hypersensitivity in rat models of mononeuropathy. Pain 2000, 88:239-248.
12. Decosterd I., Woolf C.J. Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 2000, 87:149-158.
13. Denton C.L., Gustafson D.L. Pharmacokinetics and pharmacodynamics of AZD6244 (ARRY-142886) in tumor-bearing nude mice. Cancer Chemother Pharmacol 2011, 67:349-360.
14. Geng S.J., Liao F.F., Dang W.H., Ding X., Liu X.D., Cai J., Han J.S., Wan Y., Xing G.G. Contribution of the spinal cord BDNF to the development of neuropathic pain by activation of the NR2B-containing NMDA receptors in rats with spinal nerve ligation. Exp Neurol 2010, 222:256-266.
15. Ha S.O., Kim J.K., Hong H.S., Kim D.S., Cho H.J. Expression of brain-derived neurotrophic factor in rat dorsal root ganglia, spinal cord and gracile nuclei in experimental models of neuropathic pain. Neuroscience 2001, 107:301-309.
16. Huynh H., Soo K.C., Chow P.K., Tran E. Targeted inhibition of the extracellular signal-regulated kinase kinase pathway with AZD6244 (ARRY-142886) in the treatment of hepatocellular carcinoma. Mol Cancer Ther 2007, 6:138-146.
17. Ji R.R., Gereau R.W., Malcangio M., Strichartz G.R. MAP kinase and pain. Brain Res Rev 2009, 60:135-148.
18. Kamakura S., Moriguchi T., Nishida E. Activation of the protein kinase ERK5/BMK1 by receptor tyrosine kinases. Identification and characterization of a signaling pathway to the nucleus. J Biol Chem 1999, 274:26563-26571.
19. Kimura T.E., Jin J., Zi M., Prehar S., Liu W., Oceandy D., Abe J., Neyses L., Weston A.H., Cartwright E.J., Wang X. Targeted deletion of the extracellular signal-regulated protein kinase 5 attenuates hypertrophic response and promotes pressure overload-induced apoptosis in the heart. Circ Res 2010, 106:961-970.
20. Kleinschnitz C., Hofstetter H.H., Meuth S.G., Braeuninger S., Sommer C., Stoll G. T cell infiltration after chronic constriction injury of mouse sciatic nerve is associated with interleukin-17 expression. Exp Neurol 2006, 200:480-485.
21. Li C.Q., Xu J.M., Liu D., Zhang J.Y., Dai R.P. Brain derived neurotrophic factor (BDNF) contributes to the pain hypersensitivity following surgical incision in the rats. Mol Pain 2008, 4:27.
22. Lu V.B., Ballanyi K., Colmers W.F., Smith P.A. Neuron type-specific effects of brain-derived neurotrophic factor in rat superficial dorsal horn and their relevance to "central sensitization". J Physiol 2007, 584:543-563.
23. Lu V.B., Biggs J.E., Stebbing M.J., Balasubramanyan S., Todd K.G., Lai A.Y., Colmers W.F., Dawbarn D., Ballanyi K., Smith P.A. Brain-derived neurotrophic factor drives the changes in excitatory synaptic transmission in the rat superficial dorsal horn that follow sciatic nerve injury. J Physiol 2009, 587:1013-1032.
24. Matsuoka Y., Yokoyama M., Kobayashi H., Omori M., Itano Y., Morita K., Mori H., Nakanishi T. Expression profiles of BDNF splice variants in cultured DRG neurons stimulated with NGF. Biochem Biophys Res Commun 2007, 362:682-688.
25. Merighi A., Salio C., Ghirri A., Lossi L., Ferrini F., Betelli C., Bardoni R. BDNF as a pain modulator. Prog Neurobiol 2008, 85:297-317.
26. Michael G.J., Averill S., Nitkunan A., Rattray M., Bennett D.L., Yan Q., Priestley J.V. Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J Neurosci 1997, 17:8476-8490.
27. Miletic G., Miletic V. Increases in the concentration of brain derived neurotrophic factor in the lumbar spinal dorsal horn are associated with pain behavior following chronic constriction injury in rats. Neurosci Lett 2002, 319:137-140.
28. Obara Y., Yamauchi A., Takehara S., Nemoto W., Takahashi M., Stork P.J., Nakahata N. ERK5 activity is required for nerve growth factor-induced neurite outgrowth and stabilization of tyrosine hydroxylase in PC12 cells. J Biol Chem 2009, 284:23564-23573.
29. Obata K., Katsura H., Mizushima T., Sakurai J., Kobayashi K., Yamanaka H., Dai Y., Fukuoka T., Noguchi K. Roles of extracellular signal-regulated protein kinases 5 in spinal microglia and primary sensory neurons for neuropathic pain. J Neurochem 2007, 102:1569-1584.
30. Obata K., Noguchi K. BDNF in sensory neurons and chronic pain. Neurosci Res 2006, 55:1-10.
31. Obata K., Yamanaka H., Dai Y., Mizushima T., Fukuoka T., Tokunaga A., Noguchi K. Differential activation of MAPK in injured and uninjured DRG neurons following chronic constriction injury of the sciatic nerve in rats. Eur J Neurosci 2004, 20:2881-2895.
32. Obata K., Yamanaka H., Dai Y., Tachibana T., Fukuoka T., Tokunaga A., Yoshikawa H., Noguchi K. Differential activation of extracellular signal-regulated protein kinase in primary afferent neurons regulates brain-derived neurotrophic factor expression after peripheral inflammation and nerve injury. J Neurosci 2003, 23:4117-4126.
33. Park S.Y., Lee J.Y., Choi J.Y., Park M.J., Kim D.S. Nerve growth factor activates brain-derived neurotrophic factor promoter IV via extracellular signal-regulated protein kinase 1/2 in PC12 cells. Mol Cells 2006, 21:237-243.
34. Radtke C., Vogt P.M., Devor M., Kocsis J.D. Keratinocytes acting on injured afferents induce extreme neuronal hyperexcitability and chronic pain. Pain 2010, 148:94-102.
35. Stirling L.C., Forlani G., Baker M.D., Wood J.N., Matthews E.A., Dickenson A.H., Nassar M.A. Nociceptor-specific gene deletion using heterozygous NaV1.8-Cre recombinase mice. Pain 2005, 113:27-36.
36. Storek B., Reinhardt M., Wang C., Janssen W.G., Harder N.M., Banck M.S., Morrison J.H., Beutler A.S. Sensory neuron targeting by self-complementary AAV8 via lumbar puncture for chronic pain. Proc Natl Acad Sci U S A 2008, 105:1055-1060.
37. Sturgill T.W. MAP kinase: it's been longer than fifteen minutes. Biochem Biophys Res Commun 2008, 371:1-4.
38. Suter M.R., Wen Y.R., Decosterd I., Ji R.R. Do glial cells control pain?. Neuron Glia Biol 2007, 3:255-268.
39. Vaudry D., Stork P.J., Lazarovici P., Eiden L.E. Signaling pathways for PC12 cell differentiation: making the right connections. Science 2002, 296:1648-1649.
40. Wang X., Ratnam J., Zou B., England P.M., Basbaum A.I. TrkB signaling is required for both the induction and maintenance of tissue and nerve injury-induced persistent pain. J Neurosci 2009, 29:5508-5515.
41. Wu C., Boustany L., Liang H., Brennan T.J. Nerve growth factor expression after plantar incision in the rat. Anesthesiology 2007, 107:128-135.
42. Wu C., Erickson M.A., Xu J., Wild K.D., Brennan T.J. Expression profile of nerve growth factor after muscle incision in the rat. Anesthesiology 2009, 110:140-149.
43. Xiao C., Zhang L., Cheng Q.P., Zhang L.C. The activation of extracellular signal-regulated protein kinase 5 in spinal cord and dorsal root ganglia contributes to inflammatory pain. Brain Res 2008, 1215:76-86.
44. Yajima Y., Narita M., Usui A., Kaneko C., Miyatake M., Yamaguchi T., Tamaki H., Wachi H., Seyama Y., Suzuki T. Direct evidence for the involvement of brain-derived neurotrophic factor in the development of a neuropathic pain-like state in mice. J Neurochem 2005, 93:584-594.
45. Yeh T.C., Marsh V., Bernat B.A., Ballard J., Colwell H., Evans R.J., Parry J., Smith D., Brandhuber B.J., Gross S., Marlow A., Hurley B., Lyssikatos J., Lee P.A., Winkler J.D., Koch K., Wallace E. Biological characterization of ARRY-142886 (AZD6244), a potent, highly selective mitogen-activated protein kinase kinase 1/2 inhibitor. Clin Cancer Res 2007, 13:1576-1583.
46. Zhuang Z.Y., Gerner P., Woolf C.J., Ji R.R. ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 2005, 114:149-159.
47. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.