Journal of Molecular Neuroscience

, Volume 37, Issue 2, pp 97–110 | Cite as

Electroacupuncture Induced Spinal Plasticity is Linked to Multiple Gene Expressions in Dorsal Root Deafferented Rats

  • Xu-Yang Wang
  • Xiao-Li Li
  • Sun-Quan Hong
  • Yan-Bin Xi-Yang
  • Ting-Hua Wang


The underlying mechanism for electroacupuncture (EA) associated functional improvement in patients suffering from spinal cord injury (SCI) is largely unknown. Collateral sprouting is one plausible factor, where the cord microenvironment may contribute greatly. The present study evaluated the effects of EA on collateral sprouting from spared dorsal root ganglion (DRG), sensory functional restorations, and differential gene expressions in spinal cord after partial DRG removal in the rat. Following EA, N1 waveform latencies for cortical somatosensory evoked potential significantly shortened. The densities of terminal sprouting from the spared DRG significantly increased on the EA versus the non-EA side. Microarray analysis revealed that several genes were upregulated on the acupunctured side at different time points; they were ciliary neurotrophic factor (CNTF) at 1 day postoperation (dpo), fibroblast growth factor (FGF)-1, insulin-like growth factor (IGF) 1 receptor, neuropeptide Y, and FGF-13 at 7 dpo, and CNTF and calcitonin gene-related polypeptide-alpha at 14 dpo, respectively. Meanwhile, five genes (CNTF, p75-like apoptosis-inducing death domain protein, IGF-1, transforming growth factor-beta 2, and FGF-4) were downregulated at 7 dpo. Furthermore, reverse transcriptase polymerase chain reaction results supported the gene chip analysis. It was concluded that the EA induced sensory functional restorations following partial DRG ganglionectomies could be brought about by intraspinal sprouting from the spared DRG, as well as multiple differential gene expressions in the spinal cord. The results could have clinical application in EA treatment of patients after spinal injury.


Electroacupuncture Dorsal root ganglionectomies Sprouting Genes Rat 


  1. Abdulla, F. A., & Smith, P. A. (1999). Nerve injury increases an excitatory action of neuropeptide Y and Y2-agonists on dorsal root ganglion neurons. Neuroscience, 89, 43–60. doi:10.1016/S0306-4522(98)00443-6.PubMedCrossRefGoogle Scholar
  2. Bird, G. C., Han, J. S., Fum, Y., Adwanikar, H., Willis, W. D., & Neugebauer, V. (2006). Pain-related synaptic plasticity in spinal dorsal horn neurons: role of CGRP. Molecular Pain, 2, 31. doi:10.1186/1744-8069-2-31.PubMedCrossRefGoogle Scholar
  3. Blesch, A., & Tuszynski, M. H. (2003). Cellular GDNF delivery promotes growth of motor and dorsal column sensory axons after partial and complete spinal cord transections and induces remyelination. Journal of Comparative Neurology, 467, 403–417. doi:10.1002/cne.10934.PubMedCrossRefGoogle Scholar
  4. Brazma, A., Hingamp, P., Quackenbush, J., et al. (2001). Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nature Genetics, 29, 365–371. doi:10.1038/ng1201-365.PubMedCrossRefGoogle Scholar
  5. Buldyrev, I., Tanner, N. M., Hsieh, H. Y., Dodd, E. G., Nguyen, L. T., & Balkowiec, A. (2006). Calcitonin gene-related peptide enhances release of native brain-derived neurotrophic factor from trigeminal ganglion neurons. Journal of Neurochemistry, 99, 1338–1350. doi:10.1111/j.1471-4159.2006.04161.x.PubMedCrossRefGoogle Scholar
  6. Chen, J., Huang, C., Xiao, D., Chen, H. P., & Cheng, J. S. (2003). Expression of interleukin-6 mRNA in ischemic rat brain after electroacupuncture stimulation. Acupuncture & Electro-therapeutics Research, 28, 157–166.Google Scholar
  7. Cheng, B., & Mattson, M. P. (1992). IGF-I and IGF-II protect cultured hippocampal and septal neurons against calcium-mediated hypoglycemic damage. Journal of Neuroscience, 12, 1558–1566.PubMedGoogle Scholar
  8. Coulpier, M., & Ibanez, C. F. (2004). Retrograde propagation of GDNF-mediated signals in sympathetic neurons. Molecular and Cellular Neurosciences, 27, 132–139. doi:10.1016/j.mcn.2004.06.001.PubMedCrossRefGoogle Scholar
  9. Dong, Z. Q., Ma, F., Xie, H., Wang, Y. Q., & Wu, G. C. (2005). Changes of expression of glial cell line-derived neurotrophic factor and its receptor in dorsal root ganglions and spinal dorsal horn during electroacupuncture treatment in neuropathic pain rats. Neuroscience Letters, 376, 143–148. doi:10.1016/j.neulet.2004.11.044.PubMedCrossRefGoogle Scholar
  10. Dong, H. X., Wu, L. F., & Bao, T. R. (1994). The effect of acupuncture on plasticity in lamina II of cat spinal cord after partial deafferentation—a quantitative electron microscopic study. Chinese Journal of Neuroanatomy, 10, 6–11.Google Scholar
  11. Duggan, A. W., Hope, P. J., & Lang, C. W. (1991). Microinjection of neuropeptide Y into the superficial dorsal horn reduces stimulus-evoked release of immunoreactive substance P in the anaesthetized cat. Neuroscience, 44, 733–740. doi:10.1016/0306-4522(91)90092-3.PubMedCrossRefGoogle Scholar
  12. Emson, P. C., & De Quidt, M. E. (1984). NPY a new member of the pancreatic polypeptide family. Trends in Neuroscience, 7, 31–35. DOI 10.1016/S0166-2236(84)80271-4.CrossRefGoogle Scholar
  13. Everitt, B. J., Hockfelt, T., Terenius, L., Tatemoto, K., Mutt, V., & Goldstein, M. (1984). Differential coexistence of neuropeptide Y (NPY)-like immunoreactivity with catecholamines in the central nervous system of the rat. Neuroscience, 11, 443–462. doi:10.1016/0306-4522(84)90036-8.PubMedCrossRefGoogle Scholar
  14. Fields, R. D., Yu, C., & Nelson, P. G. (1991). Calcium, network activity, and the role of NMDA channels in synaptic plasticity in vitro. Journal of Neuroscience, 11, 134–146.PubMedGoogle Scholar
  15. Fukuyama, N., Tanaka, E., Tabata, Y., et al. (2007). Intravenous injection of phagocytes transfected ex vivo with FGF-4 DNA/biodegradable gelatin complex promotes angiogenesis in a rat myocardial ischemia/reperfusion injury model. Basic Research in Cardiology, 102, 209–216. doi:10.1007/s00395-006-0629-9.PubMedCrossRefGoogle Scholar
  16. Gouin, A., Bloch-Gallego, E., Tanaka, H., Rosenthal, A., & Henderson, C. E. (1996). Transforming growth factor-beta 3, glial cell line-derived neurotrophic factor, and fibroblast growth factor-2, act in different manners to promote motoneuron survival in vitro. Journal of Neuroscience Research, 43, 454–464. doi:10.1002/(SICI)1097-4547(19960215)43:4<454::AID-JNR6>3.0.CO;2-E.PubMedCrossRefGoogle Scholar
  17. Guo, J. C., Gao, H. M., Chen, J., et al. (2004). Modulation of the gene expression in the protective effects of electroacupuncture against cerebral ischemia: a cDNA microarray study. Acupuncture & Electro-therapeutics Research, 29, 173–186.Google Scholar
  18. Guo, Y., Guo, H., Zhang, L., et al. (2005). Genomic analysis of anti-hepatitis B virus (HBV) activity by small interfering RNA and lamivudine in stable HBV-producing cells. Journal of Virology, 79, 14392–14403. doi:10.1128/JVI.79.22.14392-14403.2005.PubMedCrossRefGoogle Scholar
  19. Guo, H. F., Tian, J., Wang, X., Fang, Y., Hou, Y., & Han, J. (1996a). Brain substrates activated by electroacupuncture of different frequencies (I): comparative study on the expression of oncogene c-fos and genes coding for three opioid peptides. Brain Research. Molecular Brain Research, 43, 157–166. doi:10.1016/S0169-328X(96)00170-2.PubMedCrossRefGoogle Scholar
  20. Guo, H. F., Tian, J., Wang, X., Fang, Y., Hou, Y., & Han, J. (1996b). Brain substrates activated by electroacupuncture (EA) of different frequencies (II): role of Fos/Jun proteins in EA-induced transcription of preproenkephalin and preprodynorphingenes. Brain Research. Molecular Brain Research, 43, 167–173. doi:10.1016/S0169-328X(96)00171-4.PubMedCrossRefGoogle Scholar
  21. Hammarberg, H., Risling, M., Hökfelt, T., Cullheim, S., & Piehl, F. (1998). Expression of insulin-like growth factors and corresponding binding proteins (IGFBP 1–6) in rat spinal cord and peripheral nerve after axonal injuries. Journal of Comparative Neurology, 400, 57–72. doi:10.1002/(SICI)1096-9861(19981012)400:1<57::AID-CNE4>3.0.CO;2-S.PubMedCrossRefGoogle Scholar
  22. Hartung, H., Feldman, B., Lovec, H., Coulier, F., Birnbaum, D., & Goldfarb, M. (1997). Murine FGF-12 and FGF-13: expression in embryonic nervous system, connective tissue and heart. Mechanisms of Development, 64, 31–39. doi:10.1016/S0925-4773(97)00042-7.PubMedCrossRefGoogle Scholar
  23. Henderson, C. E., Phillips, H. S., Pollock, R. A., et al. (1994). GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science, 266, 1062–1064. doi:10.1126/science.7973664.PubMedCrossRefGoogle Scholar
  24. Horvat, J. C., Affane-Boulaid, F., Baillet-Derbin, C., et al. (1997). Post-traumatic reconnection of the cervical spinal cord with skeletal striated muscles. Study in adult rats and marmosets. Comptes Rendus des Séances de la Société de Biologie et de ses Filiales, 191, 717–729.PubMedGoogle Scholar
  25. Hossain, M. A., Fielding, K. E., Trescher, W. H., Ho, T., Wilson, M. A., & Laterra, J. (1998). Human FGF-1 gene delivery protects against quinolinate-induced striatal and hippocampal injury in neonatal rats. European Journal of Neuroscience, 10, 2490–2499. doi:10.1046/j.1460-9568.1998.00259.x.PubMedCrossRefGoogle Scholar
  26. Hung, K. S., Tsai, S. H., Lee, T. C., Lin, J. W., Chang, C. K., & Chiu, W. T. (2007). Gene transfer of insulin-like growth factor-I providing neuroprotection after spinal cord injury in rats. Journal of Neurosurgery. Spine, 6, 35–46. doi:10.3171/spi.2007.6.1.35.PubMedCrossRefGoogle Scholar
  27. Ikeda, O., Murakami, M., Ino, H., et al. (2002). Effects of brain-derived neurotrophic factor (BDNF) on compression-induced spinal cord injury: BDNF attenuates down-regulation of superoxide dismutase expression and promotes up-regulation of myelin basic protein expression. Journal of Neuropathology and Experimental Neurology, 61, 142–153.PubMedGoogle Scholar
  28. Institute of Laboratory Animal Resources Commission on Life Sciences National Research Council (1996) Guide for the care and use of laboratory animals. National Academy Press: Washington, D.C.Google Scholar
  29. Ishihara, A., Saito, H., & Abe, K. (1994). Transforming growth factor-beta 1 and -beta 2 promote neurite sprouting and elongation of cultured rat hippocampal neurons. Brain Research, 639, 21–25. doi:10.1016/0006-8993(94)91759-0.PubMedCrossRefGoogle Scholar
  30. Johnston, P., Nam, M., Hossain, M. A., et al. (1996). Delivery of human fibroblast growth factor-1 gene to brain by modified rat brain endothelial cells. Journal of Neurochemistry, 67, 1643–1652.PubMedCrossRefGoogle Scholar
  31. Koshinaga, M., Sanon, H. R., & Whittemore, S. R. (1993). Altered acidic and basic fibroblast growth factor expression following spinal cord injury. Experimental Neurology, 120, 32–48. doi:10.1006/exnr.1993.1038.PubMedCrossRefGoogle Scholar
  32. Krieglstein, K., Henheik, P., Farkas, L., et al. (1998). GDNF requires TGF-β for establishing its neurotrophic activity. Journal of Neuroscience, 18, 9822–9834.PubMedGoogle Scholar
  33. Krieglstein, K., & Unsicker, K. (1996). Distinct modulatory actions of TGF-beta and LIF on neurotrophin-mediated survival of developing sensory neurons. Neurochemical Research, 21, 843–850. doi:10.1007/BF02532308.PubMedCrossRefGoogle Scholar
  34. Lacroix, J. S., Anggård, A., Hökfelt, T., O’Hare, M. M., Fahrenkrug, J., & Lundberg, J. M. (1990). Neuropeptide Y: presence in sympathetic and parasympathetic innervation of the nasal mucosa. Cell & Tissue Research, 259, 119–128. doi:10.1007/BF00571436.CrossRefGoogle Scholar
  35. Lee, T. H., & Beitz, A. J. (1992). Electroacupuncture modifies the expression of c-fos in the spinal cord induced by noxious stimulation. Brain Research, 577, 80–91. doi:10.1016/0006-8993(92)90540-P.PubMedCrossRefGoogle Scholar
  36. Lee, M. Y., Kim, C. J., Shin, S. L., Moon, S. H., & Chun, M. H. (1998). Increased ciliary neurotrophic factor expression in reactive astrocytes following spinal cord injury in the rat. Neuroscience Letters, 255, 79–82. doi:10.1016/S0304-3940(98)00710-1.PubMedCrossRefGoogle Scholar
  37. Liang, X. B., Liu, X. Y., Li, F. Q., et al. (2002). Long-term high-frequency electroacupuncture stimulation prevents neuronal degeneration and up-regulates BDNF mRNA in the substantia nigra and ventral tegmental area following medial forebrain bundle axotomy. Brain Research. Molecular Brain Research, 108, 51–59. doi:10.1016/S0169-328X(02)00513-2.PubMedCrossRefGoogle Scholar
  38. Liang, X. B., Luo, Y., Liu, X. Y., et al. (2003). Electroacupuncture improves behavior and upregulates GDNF mRNA in MFB transected rats. Neuroreport, 14, 1177–1181. doi:10.1097/00001756-200306110-00015.PubMedCrossRefGoogle Scholar
  39. Liang, F. Y., & Wan, X. C. (1989). Improvement of the tetramethyl benzidine reaction with ammonium molybdate as a stabilizer for light and electron microscopic ligand-HRP neurohistochemistry, immunocytochemistry and double-labelling. Journal of Neuroscience Methods, 28, 155–162. doi:10.1016/0165-0270(89)90031-9.PubMedCrossRefGoogle Scholar
  40. Liu, C. N., & Chambers, W. W. (1958). Intraspinal sprouting of dorsal root axon. Archives of Neurology and Psychiatr, 79, 46–61.Google Scholar
  41. Liu, F., Wang, T. H., Zhang, Y., Hong, S. Q., & Song, X. B. (2006). Impact of acupuncture to IGF-I expression in spared dorsal root ganglion of cats. Sichuan Da Xue Xue Bao Yi Xue Ban, 37, 384–386.PubMedGoogle Scholar
  42. Long, S. L., Liu, F., Wang, T. H., Wang, T. W., Ke, Q., & Yuan, Y. (2005). Influence of acupuncture on NT-4 expression in spared root ganglion and spinal cord. Sichuan Da Xue Xue Bao Yi Xue Ban, 36, 625–629.PubMedGoogle Scholar
  43. Mantyh, P. W., Allen, C. J., Rogers, S., et al. (1994). Some sensory neurons express neuropeptide Y receptors: potential paracrine inhibition of primary afferent nociceptors following peripheral nerve injury. Journal of Neuroscience, 14, 3958–3968.PubMedGoogle Scholar
  44. Mark, M. A., Colvin, L. A., & Duggan, A. W. (1998). Spontaneous release of immunoreactive neuropeptide Y from the central terminals of large diameter primary afferents of rats with peripheral nerve injury. Neuroscience, 83, 581–589. doi:10.1016/S0306-4522(97)00402-8.PubMedCrossRefGoogle Scholar
  45. McNeill, D. L., Carlton, S. M., & Hulsebosch, C. E. (1991). Intraspinal sprouting of calcitonin gene-related peptide containing primary afferents after deafferentation in the rat. Experimental Neurology, 114, 321–329. doi:10.1016/0014-4886(91)90158-9.PubMedCrossRefGoogle Scholar
  46. Murray, M., & Goldberger, M. E. (1986). Replacement of synaptic terminals in lamina II and Clarke's nucleus after unilateral lumbosacral dorsal rhizotomy in adult cats. Journal of Neuroscience, 6, 3205–3217.PubMedGoogle Scholar
  47. Niswander, L., Tickle, C., Vogel, A., Booth, I., & Martin, G. R. (1993). FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell, 75, 579–587. doi:10.1016/0092-8674(93)90391-3.PubMedCrossRefGoogle Scholar
  48. Noguchi, K., De Leon, M., Nahin, R. L., Senba, E., & Ruda, M. A. (1993). Quantification of axotomy-induced alteration of neuropeptide mRNAs in dorsal root ganglion neurons with special reference to neuropeptide Y mRNA and the effects of neonatal capsaicin treatment. Journal of Neuroscience Research, 35, 54–66. doi:10.1002/jnr.490350108.PubMedCrossRefGoogle Scholar
  49. Nuwer, M. R. (1990). Electrophysiologic evaluation and monitoring of spinal cord and root function. Neurosurgery Clinics of North America, 1, 533–549.PubMedGoogle Scholar
  50. Ohara, S., Roth, K. A., Beaudet, L. N., & Schmidt, R. E. (1994). Transganglionic neuropeptide Y response to sciatic nerve injury in young and aged rats. Journal of Neuropathology and Experimental Neurology, 53, 646–662.PubMedCrossRefGoogle Scholar
  51. Ohara, S., Tantuwaya, V., DiStefano, P. S., & Schmidt, R. E. (1995). Exogenous NT-3 mitigates the transganglionic neuropeptide Y response to sciatic nerve injury. Brain Research, 699, 143–148. doi:10.1016/0006-8993(95)01021-M.PubMedCrossRefGoogle Scholar
  52. Ou, Y. W., Han, L., Da, C. D., Huang, Y. L., & Cheng, J. S. (2001). Influence of acupuncture upon expressing levels of basic fibroblast growth factor in rat brain following focal cerebral ischemia—evaluated by time-resolved fluorescence immunoassay. Neurological Research, 23, 47–50. doi:10.1179/016164101101198271.PubMedCrossRefGoogle Scholar
  53. Oyesiku, N. M., Wilcox, J. N., & Wigston, D. J. (1997). Changes in expression of ciliary neurotrophic factor (CNTF) and CNTF-receptor alpha after spinal cord injury. Journal of Neurobiology, 32, 251–261. doi:10.1002/(SICI)1097-4695(199703)32:3<251::AID-NEU1>3.0.CO;2-6.PubMedCrossRefGoogle Scholar
  54. Patterson, T. A., Lobenhofer, E. K., Fulmer-Smentek, S. B., et al. (2006). Performance comparison of one-color and two-color platforms within the MicroArray Quality Control (MAQC) project. Nature Biotechnology, 24, 1140–1150. doi:10.1038/nbt1242.PubMedCrossRefGoogle Scholar
  55. Rodin, B. E., Sampogna, S. L., & Kruger, L. (1982). An examination of intraspinal sprouting in dorsal root axons with the tracer horseradish peroxidase. Journal of Comparative Neurology, 215, 187–198. DOI 10.1002/cne.902150206.CrossRefGoogle Scholar
  56. Romano, G. (2003). The complex biology of the receptor for the insulin-like growth factor-1. Drug News & Perspectives, 16, 525–531. doi:10.1358/dnp.2003.16.8.829351.CrossRefGoogle Scholar
  57. Russell, J. C., Szuflita, N., Khatri, R., Laterra, J., & Hossain, M. A. (2006). Transgenic expression of human FGF-1 protects against hypoxic-ischemic injury in perinatal brain by intervening at caspase-XIAP signaling cascades. Neurobiology of Disease, 22, 677–690. doi:10.1016/j.nbd.2006.01.016.PubMedCrossRefGoogle Scholar
  58. Sendtner, M., Carroll, P., Holtmann, B., Hughes, R. A., & Thoenen, H. (1994). Ciliary neurotrophic factor. Journal of Neurobiology, 25, 1436–1453. doi:10.1002/neu.480251110.PubMedCrossRefGoogle Scholar
  59. Sizonenko, S. V., Sirimanne, E. S., Williams, C. E., & Gluckman, P. D. (2001). Neuroprotective effects of the N-terminal tripeptide of IGF-1, glycine-proline-glutamate, in the immature rat brain after hypoxic-ischemic injury. Brain Research, 922, 42–50. doi:10.1016/S0006-8993(01)03148-1.PubMedCrossRefGoogle Scholar
  60. Sterne, G. D., Brown, R. A., Green, C. J., & Terenghi, G. (1998). NT-3 modulates NPY expression in primary sensory neurons following peripheral nerve injury. Journal of Anatomy, 193, 273–281. doi:10.1046/j.1469-7580.1998.19320273.x.PubMedCrossRefGoogle Scholar
  61. Tarabal, O., Calderó, J., Ribera, J., et al. (1996). Regulation of motoneuronal calcitonin gene-related peptide (CGRP) during axonal growth and neuromuscular synaptic plasticity induced by botulinum toxin in rats. European Journal of Neuroscience, 8, 829–836. doi:10.1111/j.1460-9568.1996.tb01269.x.PubMedCrossRefGoogle Scholar
  62. Tinazzi, M., Zanette, G., Manganotti, P., et al. (1997). Amplitude changes of tibial nerve cortical somatosensory evoked potentials when the ipsilateral or contralateral ear is used as reference. Journal of Clinical Neurophysiology, 14, 217–225. doi:10.1097/00004691-199705000-00006.PubMedCrossRefGoogle Scholar
  63. Tsujimoto, T., & Kuno, M. (1988). Calcitonin gene-related peptide prevents disuse-induced sprouting of rat motor nerve terminals. Journal of Neuroscience, 8, 3951–3957.PubMedGoogle Scholar
  64. Turbes, C. C. (1997). Repair, reconstruction, regeneration and rehabilitation strategies to spinal cord injury. Biomedical Sciences Instrumentation, 34, 351–356.PubMedGoogle Scholar
  65. Unsicker, K., & Krieglstein, K. (2002). TGF-betas and their roles in the regulation of neuron survival. Advances in Experimental Medicine and Biology, 513, 353–374.PubMedGoogle Scholar
  66. van Eden, C. G., & Rinkens, A. (1994). Lesion induced expression of low affinity NGF-binding protein (p75) immunoreactivity after neonatal and adult aspiration lesions of the rat dorsomedial prefrontal cortex. Brain Res Dev Brain Res, 82, 167–174. doi:10.1016/0165-3806(94)90159-7.PubMedGoogle Scholar
  67. Wakisaka, S., Kajander, K. C., & Bennett, G. J. (1992). Effects of peripheral nerve injuries and tissue inflammation on the levels of neuropeptide Y-like immunoreactivity in rat primary afferent neurons. Brain Research, 598, 349–352. doi:10.1016/0006-8993(92)90206-O.PubMedCrossRefGoogle Scholar
  68. Watabe, K., Ohashi, T., Sakamoto, T., et al. (2000). Rescue of adult rat spinal motoneurons by adenoviral gene transfer of lesioned glial cell line-derived neurotrophic factor. Journal of Neuroscience Research, 60, 511–519. doi:10.1002/(SICI)1097-4547(20000515)60:4<511::AID-JNR10>3.0.CO;2-I.PubMedCrossRefGoogle Scholar
  69. Wang, T. H., Wang, X. Y., Li, X. L., Chen, H. M., & Wu, L. F. (2007). Effect of electroacupuncture on neurotrophin expression in cat spinal cord after partial dorsal rhizotomy. Neurochemical Research, 32, 1415–1422. doi:10.1007/s11064-007-9326-9.PubMedCrossRefGoogle Scholar
  70. Wang, T. T., Yuan, Y., Kang, Y., et al. (2005). Effects of acupuncture on the expression of glial cell line-derived neurotrophic factor (GDNF) and basic fibroblast growth factor (FGF-2/bFGF) in the left sixth lumbar dorsal root ganglion following removal of adjacent dorsal root ganglia. Neuroscience Letters, 382, 236–241. doi:10.1016/j.neulet.2005.03.020.PubMedCrossRefGoogle Scholar
  71. Wang, T. T., Yuan, W. L., Ke, Q., et al. (2006). Effects of electroacupuncture on the expression of c-jun and c-fos in spared dorsal root ganglion and associated spinal laminae following removal of adjacent dorsal root ganglia in cats. Neuroscience, 140, 1169–1176. doi:10.1016/j.neuroscience.2006.03.008.PubMedCrossRefGoogle Scholar
  72. Wu, L. F., & Xiao, R. Y. (1992). The effect of acupuncture on plasticity of cat spinal cord: quantitative electron microscopic study. Journal of Chinese Medicine, 3, 1–8.Google Scholar
  73. Xiao, R. Y., Wu, L. F., & Li, G. R. (1989). Influence of acupuncture on the plasticity of lamina II of cat spinal dorsal horn-a quantitative ultrastructure study. Chinese Journal of Neuroanatomy, 5, 149–155.Google Scholar
  74. Yamaguchi, F., Itano, T., Mizobuchi, M., et al. (1990). Insulin-like growth factor I (IGF-I) distribution in the tissue and extracellular compartment in different regions of rat brain. Brain Research, 533, 344–347. doi:10.1016/0006-8993(90)91361-J.PubMedCrossRefGoogle Scholar
  75. Yang, Y. H., Dudoit, S., Luu, P., et al. (2002). Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic acids Research, 30, e15. doi:10.1093/nar/30.4.e15.PubMedCrossRefGoogle Scholar
  76. Yun, S. J., Park, H. J., Yeom, M. J., Hahm, D. H., Lee, H. J., & Lee, E. H. (2002). Effect of electroacupuncture on the stress-induced changes in brain-derived neurotrophic factor expression in rat hippocampus. Neuroscience Letters, 318, 85–88. doi:10.1016/S0304-3940(01)02492-2.PubMedCrossRefGoogle Scholar
  77. Zhou, X. F., Li, W. P., Zhou, F. H., et al. (2005). Differential effects of endogenous brain-derived neurotrophic factor on the survival of axotomized sensory neurons in dorsal root ganglia: a possible role for the p75 neurotrophin receptor. Neuroscience, 132, 591–603. doi:10.1016/j.neuroscience.2004.12.034.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press 2008

Authors and Affiliations

  • Xu-Yang Wang
    • 1
    • 2
  • Xiao-Li Li
    • 2
    • 3
  • Sun-Quan Hong
    • 3
  • Yan-Bin Xi-Yang
    • 3
  • Ting-Hua Wang
    • 1
    • 3
  1. 1.Institute of Neurological Disease, West China HospitalSichuan UniversityChengduChina
  2. 2.Brain Research Centerthe First Affiliated Hospital of Wenzhou Medical CollegeWenzhouChina
  3. 3.Research Institute of NeuroscienceKunming Medical CollegeKunmingChina

Personalised recommendations