Skip to main content

Advertisement

SpringerLink
Log in

SCY1-Like 1-Binding Protein 1 (SCYL1BP1) Suppressed Sciatic Nerve Regeneration by Enhancing the RhoA Pathway

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

SCY1-like 1-binding protein 1 (SCYL1BP1) is first identified as an interacting protein with SCYL1. Since SCYL1BP1 is a soluble protein with coiled-coil domains known to be relevant with transcriptional regulation, it has been found to activate the transcription of murine double minute 2 (MDM2) and participate in neurite outgrowth and regeneration. However, the role and mechanism of SCYL1BP1 in peripheral nerve system lesion and repair are still unknown. Here in vitro, our work demonstrated that SCYL1BP1 inhibited cAMP-induced primary Schwann cell differentiation and suppressed nerve growth factor-mediated neurite outgrowth in PC12 cells by enhancing the RhoA pathway. Furthermore, we found that pretreatment with a Rho kinase inhibitor Y-27632 resulted in partial rescue of Schwann cell differentiation and neurite outgrowth. In vivo experiments showed that SCYL1BP1 could also suppress nerve fiber regeneration. In conclusion, we speculated that SCYL1BP1 participated in Schwann cell (SC) differentiation and neurite outgrowth in the sciatic nerve after crush by regulating the RhoA pathway.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Hokfelt T, Zhang X, Wiesenfeld-Hallin Z (1994) Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci 17(1):22–30

    Article  CAS  PubMed  Google Scholar 

  2. Fricker FR, Bennett DL (2011) The role of neuregulin-1 in the response to nerve injury. Future Neurol 6(6):809–822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Fawcett JW, Keynes RJ (1990) Peripheral nerve regeneration. Annu Rev Neurosci 13:43–60

    Article  CAS  PubMed  Google Scholar 

  4. Zhao ZS, Manser E (2005) PAK and other Rho-associated kinases—effectors with surprisingly diverse mechanisms of regulation. Biochem J 386(Pt 2):201–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Govek EE, Newey SE, Van Aelst L (2005) The role of the Rho GTPases in neuronal development. Genes Dev 19(1):1–49

    Article  CAS  PubMed  Google Scholar 

  6. Pedersen E, Brakebusch C (2012) Rho GTPase function in development: how in vivo models change our view. Exp Cell Res 318(14):1779–1787

    Article  CAS  PubMed  Google Scholar 

  7. McKerracher L, Higuchi H (2006) Targeting Rho to stimulate repair after spinal cord injury. J Neurotrauma 23(3-4):309–317

    Article  PubMed  Google Scholar 

  8. Dergham P, Ellezam B, Essagian C, Avedissian H, Lubell WD, McKerracher L (2002) Rho signaling pathway targeted to promote spinal cord repair. J Neurosci Off J Soc Neurosci 22(15):6570–6577

    CAS  Google Scholar 

  9. Ahmed Z, Douglas MR, Read ML, Berry M, Logan A (2011) Citron kinase regulates axon growth through a pathway that converges on cofilin downstream of RhoA. Neurobiol Dis 41(2):421–429

    Article  CAS  PubMed  Google Scholar 

  10. Da Silva JS, Medina M, Zuliani C, Di Nardo A, Witke W, Dotti CG (2003) RhoA/ROCK regulation of neuritogenesis via profilin IIa-mediated control of actin stability. J Cell Biol 162(7):1267–1279

    Article  PubMed  PubMed Central  Google Scholar 

  11. Wang Y, Teng HL, Huang ZH (2013) Repulsive migration of Schwann cells induced by Slit-2 through Ca2+-dependent RhoA-myosin signaling. Glia 61(5):710–723

    Article  PubMed  Google Scholar 

  12. Del Debbio CB, Santos MF, Yan CY, Ahmad I, Hamassaki DE (2014) Rho GTPases control ciliary epithelium cells proliferation and progenitor profile induction in vivo. Invest Ophthalmol Vis Sci 55(4):2631–2641

    Article  PubMed  Google Scholar 

  13. Sun Y, Lim Y, Li F, Liu S, Lu JJ, Haberberger R, Zhong JH, Zhou XF (2012) ProBDNF collapses neurite outgrowth of primary neurons by activating RhoA. PLoS One 7(4):e35883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chacon PJ, Garcia-Mejias R, Rodriguez-Tebar A (2011) Inhibition of RhoA GTPase and the subsequent activation of PTP1B protects cultured hippocampal neurons against amyloid beta toxicity. Mol Neurodegener 6(1):14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Talens-Visconti R, Peris B, Guerri C, Guasch RM (2010) RhoE stimulates neurite-like outgrowth in PC12 cells through inhibition of the RhoA/ROCK-I signalling. J Neurochem 112(4):1074–1087

    Article  CAS  PubMed  Google Scholar 

  16. Hu X, Hu J, Dai L, Trapp B, Yan R (2015) Axonal and Schwann cell BACE1 is equally required for remyelination of peripheral nerves. J Neurosci Off J Soc Neurosci 35(9):3806–3814

    Article  CAS  Google Scholar 

  17. Li Z, Gu X, Sun L, Wu S, Liang L, Cao J, Lutz BM, Bekker A et al (2015) Dorsal root ganglion myeloid zinc finger protein 1 contributes to neuropathic pain after peripheral nerve trauma. Pain 156(4):711–721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hung HA, Sun G, Keles S, Svaren J (2015) Dynamic regulation of Schwann cell enhancers after peripheral nerve injury. J Biol Chem 290(11):6937–6950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Zhang L, Li J, Wang C, Ma Y, Huo K (2005) A new human gene hNTKL-BP1 interacts with hPirh2. Biochem Biophys Res Commun 330(1):293–297

    Article  CAS  PubMed  Google Scholar 

  20. Hennies HC, Kornak U, Zhang H, Egerer J, Zhang X, Seifert W, Kuhnisch J, Budde B et al (2008) Gerodermia osteodysplastica is caused by mutations in SCYL1BP1, a Rab-6 interacting golgin. Nat Genet 40(12):1410–1412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Di Y, Li J, Fang J, Xu Z, He X, Zhang F, Ling J, Li X et al (2003) Cloning and characterization of a novel gene which encodes a protein interacting with the mitosis-associated kinase-like protein NTKL. J Hum Genet 48(6):315–321

    CAS  PubMed  Google Scholar 

  22. Liu Y, Chen Y, Lu X, Wang Y, Duan Y, Cheng C, Shen A (2012) SCYL1BP1 modulates neurite outgrowth and regeneration by regulating the Mdm2/p53 pathway. Mol Biol Cell 23(23):4506–4514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zhu L, Yan Y, Ke K, Wu X, Gao Y, Shen A, Li J, Kang L et al (2012) Dynamic change of Numbl expression after sciatic nerve crush and its role in Schwann cell differentiation. J Neurosci Res 90(8):1557–1565

    Article  CAS  PubMed  Google Scholar 

  24. Cheng X, Zhou Z, Xu G, Zhao J, Wu H, Long L, Wen H, Gu X et al (2013) Dynamic changes of Jab1 and p27kip1 expression in injured rat sciatic nerve. J Mol Neurosci MN 51(1):148–158

    Article  CAS  PubMed  Google Scholar 

  25. Zhu X, Yao L, Guo A, Li A, Sun H, Wang N, Liu H, Duan Z et al (2014) CAP1 was associated with actin and involved in Schwann cell differentiation and motility after sciatic nerve injury. J Mol Histol 45(3):337–348

    Article  CAS  PubMed  Google Scholar 

  26. Yao L, Liu YH, Li X, Ji YH, Yang XJ, Hang XT, Ding ZM, Liu F, Wang YH, Shen AG (2014) CRMP1 interacted with Spy1 during the collapse of growth cones induced by Sema3A and acted on regeneration after sciatic nerve crush. Mol Neurobiol

  27. Zhu X, Yao L, Yang X, Sun H, Guo A, Li A, Yang H (2014) Spatiotemporal expression of KHSRP modulates Schwann cells and neuronal differentiation after sciatic nerve injury. Int J Biochem Cell Biol 48:1–10

    Article  CAS  PubMed  Google Scholar 

  28. Cao L, Zhu YL, Su Z, Lv B, Huang Z, Mu L, He C (2007) Olfactory ensheathing cells promote migration of Schwann cells by secreted nerve growth factor. Glia 55(9):897–904

    Article  PubMed  Google Scholar 

  29. Yuan Y, Shen H, Yao J, Hu N, Ding F, Gu X (2010) The protective effects of Achyranthes bidentata polypeptides in an experimental model of mouse sciatic nerve crush injury. Brain Res Bull 81(1):25–32

    Article  CAS  PubMed  Google Scholar 

  30. Doddrell RD, Dun XP, Moate RM, Jessen KR, Mirsky R, Parkinson DB (2012) Regulation of Schwann cell differentiation and proliferation by the Pax-3 transcription factor. Glia 60(9):1269–1278

    Article  PubMed  Google Scholar 

  31. Wang Y, Wu X, Zhong Y, Shen J, Wu X, Ju S, Wang X (2014) Effects of histone deacetylase inhibition on the survival, proliferation and migration of Schwann cells, as well as on the expression of neurotrophic factors and genes associated with myelination. Int J Mol Med 34(2):599–605

    PubMed  Google Scholar 

  32. Zorick TS, Lemke G (1996) Schwann cell differentiation. Curr Opin Cell Biol 8(6):870–876

    Article  CAS  PubMed  Google Scholar 

  33. Tang X, Wang Y, Zhou S, Qian T, Gu X (2013) Signaling pathways regulating dose-dependent dual effects of TNF-alpha on primary cultured Schwann cells. Mol Cell Biochem 378(1-2):237–246

    Article  CAS  PubMed  Google Scholar 

  34. Schafers M, Geis C, Brors D, Yaksh TL, Sommer C (2002) Anterograde transport of tumor necrosis factor-alpha in the intact and injured rat sciatic nerve. J Neurosci Off J Soc Neurosci 22(2):536–545

    Google Scholar 

  35. Jessen KR, Mirsky R (2005) The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6(9):671–682

    Article  CAS  PubMed  Google Scholar 

  36. Bhatheja K, Field J (2006) Schwann cells: origins and role in axonal maintenance and regeneration. Int J Biochem Cell Biol 38(12):1995–1999

    Article  CAS  PubMed  Google Scholar 

  37. Ceci ML, Mardones-Krsulovic C, Sanchez M, Valdivia LE, Allende ML (2014) Axon-Schwann cell interactions during peripheral nerve regeneration in zebrafish larvae. Neural Dev 9(1):22

    Article  PubMed  PubMed Central  Google Scholar 

  38. Lehmann HC, Hoke A (2010) Schwann cells as a therapeutic target for peripheral neuropathies. CNS Neurol Disord Drug Targets 9(6):801–806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Akassoglou K, Yu WM, Akpinar P, Strickland S (2002) Fibrin inhibits peripheral nerve remyelination by regulating Schwann cell differentiation. Neuron 33(6):861–875

    Article  CAS  PubMed  Google Scholar 

  40. Solecki DJ, Trivedi N, Govek EE, Kerekes RA, Gleason SS, Hatten ME (2009) Myosin II motors and F-actin dynamics drive the coordinated movement of the centrosome and soma during CNS glial-guided neuronal migration. Neuron 63(1):63–80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hu L, Liu M, Chen L, Chan TH, Wang J, Huo KK, Zheng BJ, Xie D et al (2012) SCYL1 binding protein 1 promotes the ubiquitin-dependent degradation of Pirh2 and has tumor-suppressive function in the development of hepatocellular carcinoma. Carcinogenesis 33(8):1581–1588

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 81171140, No. 81471258, No. 31300902, No. 31270802), the National Basic Research Program of China (973 Program, No. 2012CB822104),, the Colleges and Universities in Natural Science Research Project of Jiangsu Province (No. 13KJB31009), and a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institution (PAPD).

Author information

Author notes

    Authors and Affiliations

    1. Department of Orthopaedics, Affiliated Hospital of Nantong University, Nantong, 226001, Jiangsu, People’s Republic of China

      Weidong Zhang, Yi Cao, Yang Liu, Xingxing Mao & Youhua Wang

    2. Jiangsu Province Key Laboratory for Inflammation and Molecular Drug Target, Medical College of Nantong University, Nantong, Jiangsu, 226001, People’s Republic of China

      Yonghua Liu & Aiguo Shen

    3. Department of Pathogen Biology, Medical College, Nantong University, Nantong, 226001, Jiangsu, People’s Republic of China

      Yang Liu

    4. Department of Orthopaedics, Affiliated Jiangyin Hospital of Nantong University, Nantong, Jiangsu, 226001, People’s Republic of China

      Huiguang Yang & Zhengming Zhou

    5. Medical College, Nantong University, 19 Qi-Xiu Road, Nantong, 226001, Jiangsu Province, People’s Republic of China

      Xudong Zhu

    Authors
    1. Weidong Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Yonghua Liu
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Xudong Zhu
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Yi Cao
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Yang Liu
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Xingxing Mao
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Huiguang Yang
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Zhengming Zhou
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Youhua Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    10. Aiguo Shen
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Youhua Wang or Aiguo Shen.

    Ethics declarations

    Experiments were performed according to the guidelines published in the NIH Guiding for the Care and Use of Laboratory Animals and approved by the Chinese National Committee for the Use of Experimental Animals for Medical Purposes (Jiangsu Branch).

    Conflict of Interest

    The authors declare that they have no competing interests.

    Additional information

    Weidong Zhang and Yonghua Liu contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Zhang, W., Liu, Y., Zhu, X. et al. SCY1-Like 1-Binding Protein 1 (SCYL1BP1) Suppressed Sciatic Nerve Regeneration by Enhancing the RhoA Pathway. Mol Neurobiol 53, 6342–6354 (2016). https://doi.org/10.1007/s12035-015-9531-5

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s12035-015-9531-5

    Keywords

    Search

    Navigation