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Effect of Peripheral Axotomy on Gene Expression of NIDD in Rat Neural Tissues

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Abstract

Peripheral nerve lesion-induced production of neuronal nitric oxide synthase (nNOS) was implicated to influence a range of postaxotomy processes necessary for neuronal survival and nerve regeneration (Zochodne et al., Neuroscience, 91:1515–1527, 1999; Keilhoff et al., Journal of Chemical Neuroanatomy, 24:181–187, 2002, Nitric Oxide, 10:101–111, 2004). Protein–protein interactions represent an important mechanism in the control of NOS spatial distribution or activity (Alderton et al., Biochemical Journal, 357:593–615, 2001; Dedio et al., FASEB Journal, 15:79–89, 2001; Zimmermann et al., Proceedings of the National Academy of Sciences, 99:17167–17172, 2002). As one of the nNOS-binding proteins, nNOS-interacting DHHC domain-containing protein with dendritic mRNA (NIDD) has recently been identified to increase nNOS enzyme activity by targeting nNOS to the synaptic plasma membrane in a postsynaptic density protein 95/discs-large/zona occlusens-1 domain dependent manner (Saitoh et al., Journal of Biological Chemistry, 279:29461–29468, 2004). In this paper, we established a rat model with peripheral axotomy to investigate the gene expression patterns of NIDD in neural tissues using TaqMan quantitative real-time polymerase chain reaction and in situ hybridization combined with immunofluorescence. It revealed that NIDD mRNA was upregulated after sciatic nerve transection with the similar expressing styles as that of the nNOS in the injured nerves, corresponding dorsal root ganglia, and lumbar spinal cord. These findings imply that NIDD may be involved in the different pathological conditions including nerve regeneration, neuron loss or survival, and even pain process, possibly via regulating the enzyme nNOS activity.

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References

  • Alderton W. K., Cooper C. E., & Knowles R. G. (2001). Nitric oxide synthases: Structure, function and inhibition. Biochemical Journal, 357, 593–615.

    Article  PubMed  CAS  Google Scholar 

  • Choi Y., Raja S. N., Moore L. C., & Tobin J. R. (1996). Neuropathic pain in rats is associated with altered nitric oxide synthase activity in neural tissue. Journal of the Neurological Sciences, 138, 14–20.

    Article  PubMed  CAS  Google Scholar 

  • Cristino L., Pica A., Della Corte F., & Bentivoglio M. (2000). Coinduction of nitric oxide synthase, BCL-2 and growth-associated protein-43 in spinal motoneurons during axon regeneration in the lizard tail. Neuroscience, 101, 451–458.

    Article  PubMed  CAS  Google Scholar 

  • Dedio J., KÖnig P., Wohlfart P., Schroeder C., Kummer W., & Müller-Esterl W. (2001). NOSIP, a novel modulator of endothelial nitric oxide synthase activity. FASEB Journal, 15, 79–89.

    Article  PubMed  CAS  Google Scholar 

  • Ernst A. F., Gallo G., Letourneau P. C., & McLoon S. C. (2000). Stabilization of growing retinal axons by the combined signaling of nitric oxide and brain-derived neurotrophic factor. Journal of neuroscience, 20, 1458–1469.

    PubMed  CAS  Google Scholar 

  • Fang M., Jaffrey S. R., Sawa A., Ye K., Luo X., & Snyder S. H. (2000). Dexras1: A G protein specifically coupled to neuronal nitric oxide synthase via CAPON. Neuron, 28, 183–193.

    Article  PubMed  CAS  Google Scholar 

  • Guhring H., Gorig M., Ates M., Coste O., Zeilhofer H. U., Pahl A., Rehse K., & Brune K. (2000). Suppressed injury-induced rise in spinal prostaglandin E2 production and reduced early thermal hyperalgesia in iNOS-deficient mice. Journal of Neuroscience, 20, 6714–6720.

    PubMed  CAS  Google Scholar 

  • Haraguchi K., Satoh K., Yanai H., Hamada F., Kawabuchi M., & Akiyama T. (2000). The hDLG-associated protein DAP interacts with dynein light chain and neuronal nitric oxide synthase. Genes Cells, 5, 905–911.

    Article  PubMed  CAS  Google Scholar 

  • Hunt S. P., Mantyh P. W., & Priestley J. V. (1992). The organization of biochemically characterized sensory neurons. In S. A. Scott (Eds.), Sensory neurons: Diversity, development and plasticity (pp. 60–76). New York: Oxford University Press.

    Google Scholar 

  • Jaffrey S. R., Benfenati F., Snowman A. M., Czernik A. J., & Snyder S. H. (2002). Neuronal nitric-oxide synthase localization mediated by a ternary complex with synapsin and CAPON. Proceedings of the National Academy of Sciences, 99, 3199–3204.

    Article  CAS  Google Scholar 

  • Keilhoff G., Fansa H., & Wolf G. (2002). Neuronal nitric oxide synthase is the dominant nitric oxide supplier for the survival of dorsal root ganglia after peripheral nerve axotomy. Journal of Chemical Neuroanatomy, 24, 181–187.

    Article  PubMed  CAS  Google Scholar 

  • Keilhoff G., Fansa H., & Wolf G. (2004). Neuronal NOS deficiency promotes apoptotic cell death of spinal cord neurons after peripheral nerve transection. Nitric Oxide, 10, 101–111.

    Article  PubMed  CAS  Google Scholar 

  • Lefebvre R. A. (1995). Nitric oxide in the peripheral nervous system. Annals of Medicine, 27, 379–388.

    PubMed  CAS  Google Scholar 

  • Levy D., Tal M., Hoke A., & Zochodne D. W. (2000). Transient action of the endothelial constitutive nitric oxide synthase (ecNOS) mediates the development of thermal hypersensitivity following peripheral nerve injury. European journal of Neuroscience, 12, 2323–2332.

    Article  PubMed  CAS  Google Scholar 

  • MaihOfner C., Euchenhofer C., Tegeder I., Beck K. F., Pfeilschifter J., & Geisslinger G. (2000). Regulation and immunohistochemical localization of nitric oxide synthases and soluble guanylyl cyclase in mouse spinal cord following nociceptive stimulation. European journal of Neuroscience, 290, 71–75.

    CAS  Google Scholar 

  • Naik A. K., Tandan S. K., Kumar D., Dudhgaonkar S. P. (2006). Nitric oxide and its modulators in chronic constriction injury-induced neuropathic pain in rats. European Journal of Pharmacology, 530, 59–69.

    Article  PubMed  CAS  Google Scholar 

  • Paakkari I., & Lindsberg P. (1995). Nitric oxide in the central nervous system. Annals of Medicine, 27, 369–377.

    PubMed  CAS  Google Scholar 

  • Prast H., & Philippu A. (2001). Nitric oxide as modulator of neuronal function. Progress in Neurobiology, 64, 51–68.

    Article  PubMed  CAS  Google Scholar 

  • Roczniak A., Levine D. Z., & Burns K. D. (2000). Localization of protein inhibitor of neuronal nitric oxide synthase in rat kidney. American Journal of Physiology Renal Physiol, 278, F702–F707.

    CAS  Google Scholar 

  • Saitoh F., Tian Q. B., Okano A., Sakagami H., Kondo H., & Suzuki T. (2004). NIDD, a novel DHHC-containing protein, targets neuronal nitric-oxide synthase (nNOS) to the synaptic membrane through a PDZ-dependent interaction and regulates nNOS activity. Journal of Biological Chemistry, 279, 29461–29468.

    Article  PubMed  CAS  Google Scholar 

  • Shen A., Wang H., Zhang Y., Yan J., Zhu D., & Gu J. (2002). Expression of β-1,4-galactosyltransferase II and V in rat injured sciatic nerves. European journal of Neuroscience, 327, 45–48.

    CAS  Google Scholar 

  • Shen A., Zhu D., Ding F., Zhu M., Gu X., & Gu J. (2003). Increased gene expression of β-1, 4-galactosyltransferase I in rat injured sciatic nerve. Journal of Molecular Neuroscience, 21, 103–110.

    Article  PubMed  CAS  Google Scholar 

  • Symons N. A., Danielsen N., & Harvey A. R. (2001). Migration of cells into and out of peripheral nerve isografts in the peripheral and central nervous systems of the adult mouse. European Journal of Neuroscience, 14, 522–532.

    Article  PubMed  CAS  Google Scholar 

  • Thippeswamy T., McKay J. S., & Morris R. (2001). Bax and caspases are inhibited by endogenous nitric oxide in dorsal root ganglion neurons in vitro. European journal of Neuroscience, 14, 1229–1236.

    Article  PubMed  CAS  Google Scholar 

  • Van Wangenen S., & Rehder V. (2001). Regulation of neuronal growth cone filopodia by nitric oxide depends on soluble guanylyl cyclase. Journal of Neurobiology, 46, 206–219.

    Article  Google Scholar 

  • Verge V. M. K., Xu Z., Xu X. J., Wiesenfeld-Hallin Z., & Hokfelt T. (1992). Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglion after peripheral axotomy: In situ hybridization and functional studies. Proceedings of the National Academy of Sciences, 89, 11617–11621.

    Article  CAS  Google Scholar 

  • Welch, J. A. (1996). Peripheral nerve injury. Seminars in Veterinary Medicine and Surgery (Small Animal), 11, 273–284.

    CAS  Google Scholar 

  • Zhou L., & Wu W. (2006). Antisense oligos to neuronal nitric oxide synthase aggravate motoneuron death induced by spinal root avulsion in adult rat. Experimental Neurology, 197, 84–92.

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann K., Opitz N., Dedio J., Renne C., Müller-Esterl W., & Oess S. (2002). NOSTRIN: A protein modulating nitric oxide release and subcellular distribution of endothelial nitric oxide synthase. Proceedings of the National Academy of Sciences, 99, 17167–17172.

    Article  CAS  Google Scholar 

  • Zochodne D. W., Levy D., Zwiers H., Sun H., Rubin I., Cheng C., & Lauritzen M. (1999). Evidence for nitric oxide and nitric oxide synthase activity in proximal stumps of transected peripheral nerves. Neuroscience, 91, 1515–1527.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work is supported by the Nature Science Foundation of China (30300099), Jiangsu Province Natural Scientific Grants (BK2003035), and the Grant of the Jiangsu Province Key Lab of Neuroregeneration.

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Authors and Affiliations

  1. The Jiangsu Province Key Laboratory of Neuroregeneration, Nantong University, Nantong, 226001, People’s Republic of China

    Chun Cheng, Mengling Chen, Shuqiong Niu & Aiguo Shen

  2. Department of Microbiology and Immunology, Medical College, Nantong University, Nantong, 226001, People’s Republic of China

    Chun Cheng, Mengling Chen, Shuxian Shi, Shangfeng Gao, Xin Li, Haiou Liu & Yongwei Qin

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  1. Chun Cheng
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  2. Mengling Chen
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  3. Shuxian Shi
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  4. Shangfeng Gao
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  5. Shuqiong Niu
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  6. Xin Li
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  7. Haiou Liu
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  8. Yongwei Qin
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  9. Aiguo Shen
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Correspondence to Aiguo Shen.

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Chun Cheng and Mengling Chen both contributed equally to this work.

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Cheng, C., Chen, M., Shi, S. et al. Effect of Peripheral Axotomy on Gene Expression of NIDD in Rat Neural Tissues. J Mol Neurosci 32, 199–206 (2007). https://doi.org/10.1007/s12031-007-0035-2

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  • DOI: https://doi.org/10.1007/s12031-007-0035-2

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