Phosphatidylinositol 3-kinase mediates pain behaviors induced by activation of peripheral ephrinBs/EphBs signaling in mice

Pharmacology Biochemistry and Behavior

Volumn 95, Issue 3, 2010, Pages 315-324

  Guan, Xue Hai ^b   Lu, Xian Fu ^b   Zhang, Hong Xing ^b   Wu, Jing Ru ^b   Yuan, Yan ^b   Bao, Qi ^b   Ling, Di Yang ^b   Cao, Jun Li ^a,b  

^a XUZHOU MEDICAL UNIVERSITY   (China)

^b Jiangsu Institute of Anesthesiology   (China)

Author keywords

EphB; EphrinB; Extracellular signal regulated kinase; Fos; Hyperalgesia; Peripheral sensitization; Phosphatidylinositol 3 kinase

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; EPHRIN B1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN FOS; WORTMANNIN; ANDROSTANE DERIVATIVE; EPHRIN; EPHRIN RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DOSE RESPONSE; DRUG ADMINISTRATION ROUTE; DRUG PROTEIN BINDING; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; INTRAPLANTAR DRUG ADMINISTRATION; MALE; MOUSE; NERVE ENDING; NONHUMAN; PAIN; PERIPHERAL NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPONSE TIME; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; COMPARATIVE STUDY; DRUG EFFECTS; METABOLISM; PAIN MEASUREMENT; PHYSIOLOGY; PROCEDURES; PSYCHOLOGY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANDROSTADIENES; ANIMALS; EPHRINS; MALE; MICE; PAIN; PAIN MEASUREMENT; RECEPTORS, EPH FAMILY; SIGNAL TRANSDUCTION; PHOSPHATIDYLINOSITOL 3-KINASES;

MUS;

EID: 77950457499     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2010.02.007     Document Type: Article

References (59)

1. Albanesi C., Scarponi C., Giustizieri M.L., Girolomoni G. Keratinocytes in inflammatory skin diseases. Curr Drug Targets Inflamm Allergy 2005, 4:329-334.
2. Amaya F., Shimosato G., Nagano M., Ueda M., Hashimoto S., Tanaka Y., et al. NGF and GDNF differentially regulate TRPV1 expression that contributes to development of inflammatory thermal hyperalgesia. Eur J NeuroSci 2004, 20:2303-2310.
3. Bogen O., Joseph E.K., Chen X., Levine J.D. GDNF hyperalgesia is mediated by PLCgamma, MAPK/ERK, PI3K, CDK5 and Src family kinase signaling and dependent on the IB4-binding protein versican. Eur J NeuroSci 2008, 28:12-19.
4. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
5. Bundesen L.Q., Scheel T.A., Bregman B.S., Kromer L.F. Ephrin-B2 and EphB2 regulation of astrocyte-meningeal fibroblast interactions in response to spinal cord lesions in adult rats. J Neurosci 2003, 23:7789-7800.
6. Cakir M., Grossman A.B. Targeting MAPK (Ras/ERK) and PI3K/Akt pathways in pituitary tumorigenesis. Expert Opin Ther Targets 2009, 13:1121-1134.
7. Camps M., Rückle T., Ji H., Ardissone V., Rintelen F., Shaw J., et al. Blockade of PI3Kgamma suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat Med 2005, 11:936-943.
8. Cao J.L., Ruan J.P., Ling D.Y., Guan X.H., Bao Q., Yuan Y., et al. Activation of peripheral ephrinBs/EphBs signaling induces hyperalgesia through a MAPKs-mediated mechanism in mice. Pain 2008, 139:617-631.
9. Castellino R.C., Durden D.L. Mechanisms of disease: the PI3K-Akt-PTEN signaling node-an intercept point for the control of angiogenesis in brain tumors. Nat Clin Pract Neurol 2007, 3:682-693.
10. Chandler L.J., Sutton G., Dorairaj N.R., Norwood D. N-methyl-Daspartate receptor-mediated bidirectional control of extracellular signalregulated kinase activity in cortical neuronal cultures. J Biol Chem 2001, 276:2627-2636.
11. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., Yaksh T.J. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53:55-63.
12. Coggeshall R.E. Fos, nociception and the dorsal horn. Prog Neurobiol 2005, 77:299-352.
13. Endersby R., Baker S.J. PTEN signaling in brain: neuropathology and tumorigenesis. Oncogene 2008, 27:5416-5430.
14. Fecker L.F., Stockfleth E., Nindl I., Ulrich C., Forschner T., Eberle J. The role of apoptosis in therapy and prophylaxis of epithelial tumours by nonsteroidal anti-inflammatory drugs (NSAIDs). Br J Dermatol 2007, 156:25-33.
15. Fitsialos G., Chassot A.A., Turchi L., Dayem M.A., LeBrigand K., Moreilhon C., et al. Transcriptional signature of epidermal keratinocytes subjected to in vitro scratch wounding reveals selective roles for ERK1/2, p38, and phosphatidylinositol 3-kinase signaling pathways. J Biol Chem 2007, 282:15090-15102.
16. Gerlai R. Eph receptors and neural plasticity. Nat Rev Neurosci 2001, 2:205-209.
17. Goldshmit Y., McLenachan S., Turnley A. Roles of Eph receptors and ephrins in the normal and damaged adult CNS. Brain Res Rev 2006, 52:327-345.
18. 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.
19. Holen H.L., Shadidi M., Narvhus K., Kjøsnes O., Tierens A., Aasheim H.C. Signaling through ephrin-A ligand leads to activation of Src-family kinases, Akt phosphorylation, and inhibition of antigen receptor-induced apoptosis. J Leukoc Biol 2008, 84:1183-1191.
20. Jones D.M., Tucker B.A., Rahimtula M., Mearow K.M. The synergistic effects of NGF and IGF-1 on neurite growth in adult sensory neurons: convergence on the PI 3-kinase signaling pathway. J Neurochem 2003, 86:1116-1128.
21. Kim M.S., Rådinger M., Gilfillan A.M. The multiple roles of phosphoinositide 3-kinase in mast cell biology. Trends Immunol 2008, 29:493-501.
22. Klein R. Eph/ephrin signaling in morphogenesis, neural development and plasticity. Curr Opin Cell Biol 2004, 16:580-589.
23. Klein R. Bidirectional modulation of synaptic functions by Eph/ephrin signaling. Nat Neurosci 2009, 12:15-20.
24. Lee H., Caterina M.J. TRPV channels as thermosensory receptors in epithelial cells. Pflugers Arch 2005, 451:160-167.
25. Malik-Hall M., Dina O.A., Levine J.D. Primary afferent nociceptor mechanisms mediating NGF-induced mechanical hyperalgesia. Eur J NeuroSci 2005, 21:3387-3394.
26. Menges C.W., McCance D.J. Constitutive activation of the Raf-MAPK pathway causes negative feedback inhibition of Ras-PI3K-AKT and cellular arrest through the EphA2 receptor. Oncogene 2008, 27:2934-2940.
27. Moss A., Alvares D., Meredith-Middleton J., Robinson M., Slater R., Hunt S.P., et al. Ephrin-A4 inhibits sensory neurite outgrowth and is regulated by neonatal skin wounding. Eur J NeuroSci 2005, 22:2413-2421.
28. Müller E.J., Williamson L., Kolly C., Suter M.M. Outside-in signaling through integrins and cadherins: a central mechanism to control epidermal growth and differentiation?. J Invest Dermatol 2008, 128:501-516.
29. Munglani R., Fleming B.G., Hunt S.P. Remembrance of times past: the significance of c-fos in pain. Br J Anaesth 1996, 76:1-4.
30. Nicol G.D., Vasko M.R. Unraveling the story of NGF-mediated sensitization of nociceptive sensory neurons: ON or OFF the Trks?. Mol Interv 2007, 7:26-41.
31. Pankow S., Bamberger C., Klippel A., Werner S. Regulation of epidermal homeostasis and repair by phosphoinositide 3-kinase. J Cell Sci 2006, 119:4033-4046.
32. Pasquale E.B. Eph-ephrin bidirectional signaling in physiology and disease. Cell 2008, 133:38-52.
33. Perkinton M.S., Ip J.K., Wood G.L., Crossthwaite A.J., Williams R.J. Phosphatidylinositol 3-kinase is a central mediator of NMDA receptor signaling to MAP kinase (Erk1/2), Akt/PKB and CREB in striatal neurones. J Neurochem 2002, 80:239-254.
34. Pezet S., McMahon S.B. Neurotrophins: mediators and modulators of pain. Annu Rev Neurosci 2006, 29:507-538.
35. Pezet S., Marchand F., D'Mello R., Grist J., Clark A.K., Malcangio M., et al. Phosphatidylinositol 3-kinase is a key mediator of central sensitization in painful inflammatory conditions. J Neurosci 2008, 28:4261-4270.
36. Russo S.J., Mazei-Robison M.S., Ables J.L., Nestler E.J. Neurotrophic factors and structural plasticity in addiction. Neuropharmacology 2009, 56:73-82.
37. Sammons M.J., Raval P., Davey P.T., Rogers D., Parsons A.A., Bingham S. Carrageenan-induced thermal hyperalgesia in the mouse: role of nerve growth factor and the mitogen-activated protein kinase pathway. Brain Res 2000, 876:48-54.
38. Sánchez-Pérez A.M., Llansola M., Felipo V. Modulation of NMDA receptors by AKT kinase. Neurochem Int 2006, 49:351-358.
39. Sayama K., Yamasaki K., Hanakawa Y., Shirakata Y., Tokumaru S., Ijuin T., et al. Phosphatidylinositol 3-kinase is a key regulator of early phase differentiation in keratinocytes. J Biol Chem 2002, 277:40390-40396.
40. Song X.J., Cao J.L., Li H.C., Zheng J.H., Song X.S., Xiong L.Z. Upregulation and redistribution of ephrinB and EphB receptor in dorsal root ganglion and spinal dorsal horn neurons after peripheral nerve injury and dorsal rhizotomy. Eur J Pain 2008, 12:1031-1039.
41. Song X.J., Zheng J.H., Cao J.L., Liu W.T., Song X.S., Huang Z.J. EphrinB-EphB receptor signaling contributes to neuropathic pain by regulating neural excitability and spinal synaptic plasticity in rats. Pain 2008, 139:168-180.
42. Southall M.D., Li T., Gharibova L.S., Pei Y., Nicol G.D., Travers J.B. Activation of epidermal vanilloid receptor-1 induces release of proinflammatory mediators in human keratinocytes. J Pharmacol Exp Ther 2003, 304:217-222.
43. Stein A.T., Ufret-Vincenty C.A., Hua L., Santana L.F., Gordon S.E. Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J Gen Physiol 2006, 128:509-522.
44. Steinle J.J., Meininger C.J., Forough R., Wu G., Wu M.H., Granger H.J. Eph B4 receptor signaling mediates endothelial cell migration and proliferation via the phosphatidylinositol 3-kinase pathway. J Biol Chem 2002, 277:43830-43835.
45. Steinle J.J., Meininger C.J., Chowdhury U., Wu G., Wu M.H., Granger H.J. Role of ephrin B2 in human retinal endothelial cell proliferation and migration. Cell Signal 2003, 15:1011-1017.
46. Sun R.Q., Tu Y.J., Yan J.Y., Willis W.D. Activation of protein kinase B/Akt signaling pathway contributes to mechanical hypersensitivity induced by capsaicin. Pain 2006, 120:86-96.
47. Sun R., Yan J., Willis W.D. Activation of protein kinase B/Akt in the periphery contributes to pain behavior induced by capsaicin in rats. Neuroscience 2007, 144:286-294.
48. Tessier-Lavigne M. Eph receptor tyrosine kinases, axon repulsion, and the development of topographic maps. Cell 1995, 82:345-348.
49. Tüzün Y., Antonov M., Dolar N., Wolf R. Keratinocyte cytokine and chemokine receptors. Dermatol Clin 2007, 25:467-476.
50. Umeda J., Sano S., Kogawa K., Motoyama N., Yoshikawa K., Itami S., et al. In vivo cooperation between Bcl-xL and the phosphoinositide 3-kinase-Akt signaling pathway for the protection of epidermal keratinocytes from apoptosis. FASEB J 2003, 17:610-620.
51. Willson C.A., Irizarry-Ramirez M., Gaskins H.E., Cruz-Orengo L., Figueroa J.D., Whittemore S.R., Miranda J.D. Upregulation of EphA receptor expression in the injured adult rat spinal cord. Cell Transplant 2002, 11:229-239.
52. Willson C.A., Miranda J.D., Foster R.D., Onifer S.M., Whittemore S.R. Transection of the adult rat spinal cord upregulates EphB3 receptor and ligand expression. Cell Transplant 2003, 12:279-290.
53. Xu J.T., Tu H.Y., Xin W.J., Liu X.G., Zhang G.H., Zhai C.H. Activation of phosphatidylinositol 3-kinase and protein kinase B/Akt in dorsal root ganglia and spinal cord contributes to the neuropathic pain induced by spinal nerve ligation in rats. Exp Neurol 2007, 206:269-279.
54. Yamaguchi Y., Pasquale E.B. Eph receptors in the adult brain. Curr Opin Neurobiol 2004, 14:288-296.
55. Zhao J., Seereeram A., Nassar M.A., Levato A., Pezet S., Hathaway G., Morenilla-Palao C., Stirling C., Fitzgerald M., McMahon S.B., Rios M., Wood J.N. Nociceptor-derived brain-derived neurotrophic factor regulates acute and inflammatory but not neuropathic pain. Mol Cell Neurosci 2006, 31:539-548. London Pain Consortium.
56. Zhao P., Barr T.P., Hou Q., Dib-Hajj S.D., Black J.A., Albrecht P.J., et al. Voltage-gated sodium channel expression in rat and human epidermal keratinocytes: evidence for a role in pain. Pain 2008, 139:90-105.
57. Zhu W., Oxford G.S. Phosphoinositide-3-kinase and mitogen activated protein kinase signaling pathways mediate acute NGF sensitization of TRPV1. Mol Cell Neurosci 2007, 34:689-700.
58. Zhu W., Xu P., Cuascut F.X., Hall A.K., Oxford G.S. Activin acutely sensitizes dorsal root ganglion neurons and induces hyperalgesia via PKC-mediated potentiation of transient receptor potential vanilloid I. J Neurosci 2007, 27:13770-13780.
59. Zhuang Z.Y., Xu H., Clapham D.E., Ji R.R. Phosphatidylinositol 3-kinase activates ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPV1 sensitization. J Neurosci 2004, 24:8300-8309.