Persistent mechanical allodynia positively correlates with an increase in activated microglia and increased P-p38 mitogen-activated protein kinase activation in streptozotocin-induced diabetic rats

European Journal of Pain (United Kingdom)

Volumn 18, Issue 2, 2014, Pages 162-173

  Cheng, K I ^a,b   Wang, H C ^a,c   Chuang, Y T ^d   Chou, C W ^a   Tu, H P ^e   Yu, Y C ^b   Chang, L L ^a   Lai, C S ^a,b  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHANG GUNG UNIVERSITY   (Taiwan)

^d KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^e KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; MITOGEN ACTIVATED PROTEIN KINASE P38; SODIUM CHANNEL NAV1.3; SODIUM CHANNEL NAV1.8; SODIUM CHLORIDE; STREPTOZOCIN;

ADULT; ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CELL ACTIVATION; CHRONIC PAIN; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EXPERIMENTAL BEHAVIORAL TEST; FEMORAL VEIN; GLIA CELL; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; HYPERSENSITIVITY; IMMUNOFLUORESCENCE; MALE; MECHANICAL STIMULATION; MICROGLIA; NERVE CELL; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD DORSAL HORN; SPINAL GANGLION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; THERMAL STIMULATION; UPREGULATION;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; HYPERALGESIA; MALE; MICROGLIA; NAV1.3 VOLTAGE-GATED SODIUM CHANNEL; NEURALGIA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; UP-REGULATION;

EID: 84896749717     PISSN: 10903801     EISSN: 15322149     Source Type: Journal    
DOI: 10.1002/j.1532-2149.2013.00356.x     Document Type: Article

References (56)

1. Abbott, C. A., Malik, R. A., Van Ross, E. R., Kulkarni, J., Boulton, A. J. (2011). Prevalence and characteristics of painful diabetic neuropathy in a large community-based diabetic population in the U. K. Diabetes Care 34, 2220-2224.
2. Afsari, Z. H., Renno, W. M., Abd-El-Basset, E. (2008). Alteration of glial fibrillary acidic proteins immunoreactivity in astrocytes of the spinal cord diabetic rats. Anat Rec (Hoboken) 291, 390-399.
3. Berta, T., Poirot, O., Pertin, M., Ji, R. R., Kellenberger, S., Decosterd, I. (2008). Transcriptional and functional profiles of voltage-gated Na (+) channels in injured and non-injured DRG neurons in the SNI model of neuropathic pain. Mol Cell Neurosci 37, 196-208. (Pubitemid 351173844)
4. Bierhaus, A., Fleming, T., Stoyanov, S., Leffler, A., Babes, A., Neacsu, C., Sauer, S. K., Eberhardt, M., Schnolzer, M., Lasitschka, F., Neuhuber, W. L., Kichko, T. I., Konrade, I., Elvert, R., Mier, W., Pirags, V., Lukic, I. K., Morcos, M., Dehmer, T., Rabbani, N., Thornalley, P. J., Edelstein, D., Nau, C., Forbes, J., Humpert, P. M., Schwaninger, M., Ziegler, D., Stern, D. M., Cooper, M. E., Haberkorn, U., Brownlee, M., Reeh, P. W., Nawroth, P. P. (2012). Methylglyoxal modification of Nav1.8 facilitates nociceptive neuron firing and causes hyperalgesia in diabetic neuropathy. Nat Med 18, 926-933.
5. Black, J. A., Nikolajsen, L., Kroner, K., Jensen, T. S., Waxman, S. G. (2008). Multiple sodium channel isoforms and mitogen-activated protein kinases are present in painful human neuromas. Ann Neurol 64, 644-653.
6. Boulton, A. J., Malik, R. A. (1998). Diabetic neuropathy. Med Clin North Am 82, 909-929. (Pubitemid 28350788)
7. Brownlee, M. (2005). The pathobiology of diabetic complications: A unifying mechanism. Diabetes 54, 1615-1625. (Pubitemid 40770750)
8. Cheng, K. I., Wang, H. C., Chang, L. L., Wang, F. Y., Lai, C. S., Chou, C. W., Tsai, H. P., Kwan, A. L. (2012). Pretreatment with intrathecal amitriptyline potentiates anti-hyperalgesic effects of post-injury intraperitoneal amitriptyline following spinal nerve ligation. BMC Neurol 12, 44.
9. Colburn, R. W., Rickman, A. J., De Leo, J. A. (1999). The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior. Exp Neurol 157, 289-304. (Pubitemid 29260737)
10. Craner, M. J., Klein, J. P., Renganathan, M., Black, J. A., Waxman, S. G. (2002). Changes of sodium channel expression in experimental painful diabetic neuropathy. Ann Neurol 52, 786-792. (Pubitemid 35403189)
11. Crown, E. D. (2012). The role of mitogen activated protein kinase signaling in microglia and neurons in the initiation and maintenance of chronic pain. Exp Neurol 234, 330-339.
12. Dauch, J. R., Yanik, B. M., Hsieh, W., Oh, S. S., Cheng, H. T. (2012). Neuron-astrocyte signaling network in spinal cord dorsal horn mediates painful neuropathy of type 2 diabetes. Glia 60, 1301-1315.
13. Dib-Hajj, S., Black, J. A., Felts, P., Waxman, S. G. (1996). Down-regulation of transcripts for Na channel alpha-SNS in spinal sensory neurons following axotomy. Proc Natl Acad Sci U S A 93, 14950-14954. (Pubitemid 26419076)
14. Dobretsov, M., Hastings, S. L., Romanovsky, D., Stimers, J. R., Zhang, J. M. (2003). Mechanical hyperalgesia in rat models of systemic and local hyperglycemia. Brain Res 960, 174-183. (Pubitemid 36044574)
15. Fox, A., Eastwood, C., Gentry, C., Manning, D., Urban, L. (1999). Critical evaluation of the streptozotocin model of painful diabetic neuropathy in the rat. Pain 81, 307-316. (Pubitemid 29257901)
16. Gao, Y. J., Zhang, L., Ji, R. R. (2010). Spinal injection of TNF-alpha-activated astrocytes produces persistent pain symptom mechanical allodynia by releasing monocyte chemoattractant protein-1. Glia 58, 1871-1880.
17. Gonzalez-Clemente, J. M., Mauricio, D., Richart, C., Broch, M., Caixas, A., Megia, A., Gimenez-Palop, O., Simon, I., Martinez-Riquelme, A., Gimenez-Perez, G., Vendrell, J. (2005). Diabetic neuropathy is associated with activation of the TNF-alpha system in subjects with type 1 diabetes mellitus. Clin Endocrinol (Oxf) 63, 525-529. (Pubitemid 41626747)
18. Gwak, Y. S., Kang, J., Unabia, G. C., Hulsebosch, C. E. (2012). Spatial and temporal activation of spinal glial cells: Role of gliopathy in central neuropathic pain following spinal cord injury in rats. Exp Neurol 234, 362-372.
19. Hains, B. C., Klein, J. P., Saab, C. Y., Craner, M. J., Black, J. A., Waxman, S. G. (2003). Upregulation of sodium channel Nav1.3 and functional involvement in neuronal hyperexcitability associated with central neuropathic pain after spinal cord injury. J Neurosci 23, 8881-8892. (Pubitemid 37210901)
20. He, X. H., Zang, Y., Chen, X., Pang, R. P., Xu, J. T., Zhou, X., Wei, X. H., Li, Y. Y., Xin, W. J., Qin, Z. H., Liu, X. G. (2010). TNF-alpha contributes to up-regulation of Nav1.3 and Nav1.8 in DRG neurons following motor fiber injury. Pain 151, 266-279.
21. Hong, S., Morrow, T. J., Paulson, P. E., Isom, L. L., Wiley, J. W. (2004). Early painful diabetic neuropathy is associated with differential changes in tetrodotoxin-sensitive and -resistant sodium channels in dorsal root ganglion neurons in the rat. J Biol Chem 279, 29341-29350. (Pubitemid 38915812)
22. Huang, L., Gao, Y. J., Wang, J., Strichartz, G. (2011). Shifts in cell-type expression accompany a diminishing role of spinal p38-mapkinase activation over time during prolonged postoperative pain. Anesthesiology 115, 1281-1290.
23. Ji, R. R., Strichartz, G. (2004). Cell signaling and the genesis of neuropathic pain. Sci STKE 2004, reE14.
24. Jin, S. X., Zhuang, Z. Y., Woolf, C. J., Ji, R. R. (2003). 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, 4017-4022. (Pubitemid 36958419)
25. Julius, D., Basbaum, A. I. (2001). Molecular mechanisms of nociception. Nature 413, 203-210. (Pubitemid 32867885)
26. Kawamura, N., Dyck, P. J., Schmeichel, A. M., Engelstad, J. K., Low, P. A. (2008). Inflammatory mediators in diabetic and non-diabetic lumbosacral radiculoplexus neuropathy. Acta Neuropathol 115, 231-239.
27. Kerr, B. J., Souslova, V., McMahon, S. B., Wood, J. N. (2001). A role for the TTX-resistant sodium channel Nav 1.8 in NGF-induced hyperalgesia, but not neuropathic pain. Neuroreport 12, 3077-3080. (Pubitemid 32907008)
28. Kim, S. H., Chung, J. M. (1992). An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50, 355-363.
29. Kim, S. H., Kwon, J. K., Kwon, Y. B. (2012). Pain modality and spinal glia expression by streptozotocin induced diabetic peripheral neuropathy in rats. Lab Anim Res 28, 131-136.
30. Kim, S. Y., Bae, J. C., Kim, J. Y., Lee, H. L., Lee, K. M., Kim, D. S., Cho, H. J. (2002). Activation of p38 MAP kinase in the rat dorsal root ganglia and spinal cord following peripheral inflammation and nerve injury. Neuroreport 13, 2483-2486.
31. Li, F., Obrosova, I. G., Abatan, O., Tian, D., Larkin, D., Stuenkel, E. L., Stevens, M. J. (2005). Taurine replacement attenuates hyperalgesia and abnormal calcium signaling in sensory neurons of STZ-D rats. Am J Physiol Endocrinol Metab 288, E29-E36. (Pubitemid 40023787)
32. Lindia, J. A., Kohler, M. G., Martin, W. J., Abbadie, C. (2005). Relationship between sodium channel NaV1.3 expression and neuropathic pain behavior in rats. Pain 117, 145-153. (Pubitemid 41764782)
33. Ma, W., Quirion, R. (2002). Partial sciatic nerve ligation induces increase in the phosphorylation of extracellular signal-regulated kinase (ERK) and c-Jun. N-terminal kinase (JNK) in astrocytes in the lumbar spinal dorsal horn and the gracile nucleus. Pain 99, 175-184. (Pubitemid 35247540)
34. Malcangio, M., Tomlinson, D. R. (1998). A pharmacologic analysis of mechanical hyperalgesia in streptozotocin/diabetic rats. Pain 76, 151-157. (Pubitemid 28304951)
35. Mo, G., Grant, R., O'Donnell, D., Ragsdale, D. S., Cao, C. Q., Seguela, P. (2011). Neuropathic Nav1.3-mediated sensitization to P2X activation is regulated by protein kinase C. Mol Pain 7, 14.
36. Naseri, K., Saghaei, E., Abbaszadeh, F., Afhami, M., Haeri, A., Rahimi, F., Jorjani, M. (2013). Role of microglia and astrocyte in central pain syndrome following electrolytic lesion at the spinothalamic tract in rats. J Mol Neurosci 49, 470-479.
37. Nassar, M. A., Levato, A., Stirling, L. C., Wood, J. N. (2005). Neuropathic pain develops normally in mice lacking both Na (v) 1.7 and Na (v) 1.8. Mol Pain 1, 24.
38. Obrosova, I. G. (2009). Diabetic painful and insensate neuropathy: Pathogenesis and potential treatments. Neurother 6, 638-647.
39. Piercy, V., Banner, S. E., Bhattacharyya, A., Parsons, A. A., Sanger, G. J., Smith, S. A., Bingham, S. (1999). Thermal, but not mechanical, nociceptive behavior is altered in the Zucker Diabetic Fatty rat and is independent of glycemic status. J Diabetes Complications 13, 163-169. (Pubitemid 29430217)
40. Renno, W. M., Alkhalaf, M., Afsari, Z., Abd-El-Basset, E., Mousa, A. (2008). Consumption of green tea alters glial fibriliary acidic protein immunoreactivity in the spinal cord astrocytes of STZ-diabetic rats. Nutr Neurosci 11, 32-40. (Pubitemid 351864131)
41. Rush, A. M., Cummins, T. R., Waxman, S. G. (2007). Multiple sodium channels and their roles in electrogenesis within dorsal root ganglion neurons. J Physiol 579, 1-14.
42. Scholz, J., Abele, A., Marian, C., Haussler, A., Herbert, T. A., Woolf, C. J., Tegeder, I. (2008). Low-dose methotrexate reduces peripheral nerve injury-evoked spinal microglial activation and neuropathic pain behavior in rats. Pain 138, 130-142.
43. Shaw, J. E., Sicree, R. A., Zimmet, P. Z. (2010). Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 87, 4-14.
44. Suzuki, N., Hasegawa-Moriyama, M., Takahashi, Y., Kamikubo, Y., Sakurai, T., Inada, E. (2011). Lidocaine attenuates the development of diabetic-induced tactile allodynia by inhibiting microglial activation. Anesth Analg 113, 941-946.
45. Sweitzer, S. M., Medicherla, S., Almirez, R., Dugar, S., Chakravarty, S., Shumilla, J. A., Yeomans, D. C., Protter, A. A. (2004). Antinociceptive action of a p38alpha MAPK inhibitor, SD-282, in a diabetic neuropathy model. Pain 109, 409-419. (Pubitemid 38638718)
46. Tesfaye, S., Vileikyte, L., Rayman, G., Sindrup, S., Perkins, B., Baconja, M., Vinik, A., Boulton, A. (2011). Painful diabetic peripheral neuropathy: Consensus recommendations on diagnosis, assessment and management. Diabetes Metab Res Rev. doi: 10.1002/dmrr.1225.
47. Toth, C. C., Jedrzejewski, N. M., Ellis, C. L., Frey, W. H., 2nd. (2010). Cannabinoid-mediated modulation of neuropathic pain and microglial accumulation in a model of murine type I diabetic peripheral neuropathic pain. Mol Pain 6, 16.
48. Tsuda, M., Ueno, H., Kataoka, A., Tozaki-Saitoh, H., Inoue, K. (2008). Activation of dorsal horn microglia contributes to diabetes-induced tactile allodynia via extracellular signal-regulated protein kinase signaling. Glia 56, 378-386. (Pubitemid 351212947)
49. Veves, A., Backonja, M., Malik, R. A. (2008). Painful diabetic neuropathy: Epidemiology, natural history, early diagnosis, and treatment options. Pain Med 9, 660-674.
50. Wen, Y. R., Suter, M. R., Kawasaki, Y., Huang, J., Pertin, M., Kohno, T., Berde, C. B., Decosterd, I., Ji, R. R. (2007). Nerve conduction blockade in the sciatic nerve prevents but does not reverse the activation of p38 mitogen-activated protein kinase in spinal microglia in the rat spared nerve injury model. Anesthesiology 107, 312-321. (Pubitemid 47196496)
51. Wodarski, R., Clark, A. K., Grist, J., Marchand, F., Malcangio, M. (2009). Gabapentin reverses microglial activation in the spinal cord of streptozotocin-induced diabetic rats. Eur J Pain 13, 807-811.
52. Wood, J. N., Boorman, J. P., Okuse, K., Baker, M. D. (2004). Voltage-gated sodium channels and pain pathways. J Neurobiol 61, 55-71. (Pubitemid 39287770)
53. Wu, Q. H., Chen, W. S., Chen, Q. X., Wang, J. H., Zhang, X. M. (2010). Changes in the expression of platelet-derived growth factor in astrocytes in diabetic rats with spinal cord injury. Chin Med J (Engl) 123, 1577-1581.
54. Xu, J. T., Xin, W. J., Wei, X. H., Wu, C. Y., Ge, Y. X., Liu, Y. L., Zang, Y., Zhang, T., Li, Y. Y., Liu, X. G. (2007). p38 activation in uninjured primary afferent neurons and in spinal microglia contributes to the development of neuropathic pain induced by selective motor fiber injury. Exp Neurol 204, 355-365. (Pubitemid 46330283)
55. Zhang, J., Shi, X. Q., Echeverry, S., Mogil, J. S., De Koninck, Y., Rivest, S. (2007). Expression of CCR2 in both resident and bone marrow-derived microglia plays a critical role in neuropathic pain. J Neurosci 27, 12396-12406. (Pubitemid 350085465)
56. Zhuang, Z. Y., Gerner, P., Woolf, C. J., Ji, R. R. (2005). ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114, 149-159. (Pubitemid 40279096)