Advertisement

Neurochemical Research

, Volume 42, Issue 4, pp 1084–1095 | Cite as

Upregulated Expression of TRIM32 Is Involved in Schwann Cell Differentiation, Migration and Neurite Outgrowth After Sciatic Nerve Crush

  • Yonghua Liu
  • Weijie Wu
  • Huiguang Yang
  • Zhengming Zhou
  • Xiaojian Zhu
  • Chi Sun
  • Yuxi Liu
  • Zhaohui Yu
  • Yuyan Chen
  • Youhua WangEmail author
Original Paper

Abstract

Tripartite motif containing 32 (TRIM32), a member of the tripartite motif (TRIM) family, plays an indispensable role in myoblast proliferation. It also regulates neuron and skeletal muscle stem cell differentiation. Although it is of great importance, we know little about the roles of TRIM32 during peripheral nervous system injury. Here, we examined the dynamic changes of TRIM32 in acute sciatic nerve crush (SNC) model. After crush, TRIM32 rapidly increased and reached the climax at 1 week but then gradually declined to the normal level at 4 weeks post-injury. Meanwhile, we observed similar changes of Oct-6. What is more, we found co-localization of TRIM32 with S100 and Oct-6 in 1-week-injured tissues using double immunofluorescent staining. In further vitro experiments, enhancive expression of TRIM32 was detected during the process of cyclic adenosine monophosphate (cAMP)-induced Schwann cell differentiation and nerve growth factor (NGF)-induced PC12 cell neurite outgrowth. More interestingly, specific si-TRIM32-transfected RSC96 cells exhibited obvious reduction in the ability of migration. Taken together, we inferred that upregulated TRIM32 was not only involved in the differentiation and migration of Schwann cells but the neurite elongation after SNC.

Keywords

TRIM32 Schwann cell Differentiation PC12 cell Neurite outgrowth Sciatic nerve crush 

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 81471258, No. 31300902) and the Applied Basic Research Project of Nantong City (No. MS12015099).

Compliance with Ethical Standards

Conflict of interest

None.

References

  1. 1.
    Zhang W, Liu Y, Zhu X, Cao Y, Liu Y, Mao X, Yang H, Zhou Z, Wang Y, Shen A (2015) SCY1-like 1-binding protein 1 (SCYL1BP1) suppressed sciatic nerve regeneration by enhancing the rhoa pathway. Mol Neurobiol. doi: 10.1007/s12035-015-9531-5 Google Scholar
  2. 2.
    Fricker FR, Bennett DL (2011) The role of neuregulin-1 in the response to nerve injury. Fut Neurol 6(6):809–822CrossRefGoogle Scholar
  3. 3.
    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. doi: 10.1007/s12035-014-9049-2 Google Scholar
  4. 4.
    Fu SY, Gordon T (1997) The cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol 14(1–2):67–116. doi: 10.1007/BF02740621 CrossRefPubMedGoogle Scholar
  5. 5.
    Kury P, Stoll G, Muller HW (2001) Molecular mechanisms of cellular interactions in peripheral nerve regeneration. Curr Opin Neurol 14(5):635–639CrossRefPubMedGoogle Scholar
  6. 6.
    Fawcett JW, Keynes RJ (1990) Peripheral nerve regeneration. Annu Rev Neurosci 13:43–60. doi: 10.1146/annurev.ne.13.030190.000355 CrossRefPubMedGoogle Scholar
  7. 7.
    Napolitano LM, Jaffray EG, Hay RT, Meroni G (2011) Functional interactions between ubiquitin E2 enzymes and TRIM proteins. Biochem J 434(2):309–319. doi: 10.1042/BJ20101487 CrossRefPubMedGoogle Scholar
  8. 8.
    Mokhonova EI, Avliyakulov NK, Kramerova I, Kudryashova E, Haykinson MJ, Spencer MJ (2015) The E3 ubiquitin ligase TRIM32 regulates myoblast proliferation by controlling turnover of NDRG2. Hum Mol Genet 24(10):2873–2883. doi: 10.1093/hmg/ddv049 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Meroni G (2012) Genomics and evolution of the TRIM gene family. Adv Exp Med Biol 770:1–9CrossRefPubMedGoogle Scholar
  10. 10.
    Cambiaghi V, Giuliani V, Lombardi S, Marinelli C, Toffalorio F, Pelicci PG (2012) TRIM proteins in cancer. Adv Exp Med Biol 770:77–91CrossRefPubMedGoogle Scholar
  11. 11.
    Liu J, Zhang C, Wang XL, Ly P, Belyi V, Xu-Monette ZY, Young KH, Hu W, Feng Z (2014) E3 ubiquitin ligase TRIM32 negatively regulates tumor suppressor p53 to promote tumorigenesis. Cell Death Differ 21(11):1792–1804. doi: 10.1038/cdd.2014.121 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Kano S, Miyajima N, Fukuda S, Hatakeyama S (2008) Tripartite motif protein 32 facilitates cell growth and migration via degradation of Abl-interactor 2. Cancer Res 68(14):5572–5580. doi: 10.1158/0008-5472.CAN-07-6231 CrossRefPubMedGoogle Scholar
  13. 13.
    Nicklas S, Otto A, Wu X, Miller P, Stelzer S, Wen Y, Kuang S, Wrogemann K, Patel K, Ding H, Schwamborn JC (2012) TRIM32 regulates skeletal muscle stem cell differentiation and is necessary for normal adult muscle regeneration. PLoS One 7(1):e30445. doi: 10.1371/journal.pone.0030445 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Hillje AL, Pavlou MA, Beckmann E, Worlitzer MM, Bahnassawy L, Lewejohann L, Palm T, Schwamborn JC (2013) TRIM32-dependent transcription in adult neural progenitor cells regulates neuronal differentiation. Cell Death Dis 4:e976. doi: 10.1038/cddis.2013.487 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Sato T, Okumura F, Kano S, Kondo T, Ariga T, Hatakeyama S (2011) TRIM32 promotes neural differentiation through retinoic acid receptor-mediated transcription. J Cell Sci 124 (Pt 20):3492–3502. doi: 10.1242/jcs.088799 CrossRefPubMedGoogle Scholar
  16. 16.
    Kudryashova E, Wu J, Havton LA, Spencer MJ (2009) Deficiency of the E3 ubiquitin ligase TRIM32 in mice leads to a myopathy with a neurogenic component. Hum Mol Genet 18(7):1353–1367. doi: 10.1093/hmg/ddp036 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Chen Z, Zhang W, Ni L, Wang G, Cao Y, Wu W, Sun C, Yuan D, Ni H, Wang Y, Yang H (2015) Spatiotemporal expression of poly(rC)-binding protein PCBP2 modulates Schwann cell proliferation after sciatic nerve injury. Cell Mol Neurobiol. doi: 10.1007/s10571-015-0253-z Google Scholar
  18. 18.
    Wang Y, Long L, Yang J, Wu Y, Wu H, Wei H, Deng X, Cheng X, Lou D, Chen H, Wen H (2013) Spatiotemporal expression of SKIP after rat sciatic nerve crush. Neurochem Res 38(4):857–865. doi: 10.1007/s11064-013-0990-7 CrossRefPubMedGoogle Scholar
  19. 19.
    Liu Y, Liu Y, Nie X, Cao J, Zhu X, Zhang W, Liu Z, Mao X, Yan S, Ni Y, Wang Y (2014) Up-regulation of HDAC4 is associated with Schwann cell proliferation after sciatic nerve crush. Neurochem Res 39(11):2105–2117. doi: 10.1007/s11064-014-1401-4 CrossRefPubMedGoogle Scholar
  20. 20.
    Izumi H, Kaneko Y (2014) Trim32 facilitates degradation of MYCN on spindle poles and induces asymmetric cell division in human neuroblastoma cells. Cancer Res 74(19):5620–5630. doi: 10.1158/0008-5472.CAN-14-0169 CrossRefPubMedGoogle Scholar
  21. 21.
    Horn EJ, Albor A, Liu Y, El-Hizawi S, Vanderbeek GE, Babcock M, Bowden GT, Hennings H, Lozano G, Weinberg WC, Kulesz-Martin M (2004) RING protein Trim32 associated with skin carcinogenesis has anti-apoptotic and E3-ubiquitin ligase properties. Carcinogenesis 25(2):157–167. doi: 10.1093/carcin/bgh003 CrossRefPubMedGoogle Scholar
  22. 22.
    Yokota T, Mishra M, Akatsu H, Tani Y, Miyauchi T, Yamamoto T, Kosaka K, Nagai Y, Sawada T, Heese K (2006) Brain site-specific gene expression analysis in Alzheimer’s disease patients. Eur J Clin Invest 36(11):820–830. doi: 10.1111/j.1365-2362.2006.01722.x CrossRefPubMedGoogle Scholar
  23. 23.
    Locke M, Tinsley CL, Benson MA, Blake DJ (2009) TRIM32 is an E3 ubiquitin ligase for dysbindin. Hum Mol Genet 18(13):2344–2358. doi: 10.1093/hmg/ddp167 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Albor A, Kulesz-Martin M (2007) Novel initiation genes in squamous cell carcinomagenesis: a role for substrate-specific ubiquitylation in the control of cell survival. Mol Carcinog 46(8):585–590. doi: 10.1002/mc.20344 CrossRefPubMedGoogle Scholar
  25. 25.
    Schwamborn JC, Berezikov E, Knoblich JA (2009) The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136(5):913–925. doi: 10.1016/j.cell.2008.12.024 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Ide C (1996) Peripheral nerve regeneration. Neurosci Res 25(2):101–121CrossRefPubMedGoogle Scholar
  27. 27.
    Chen ZL, Yu WM, Strickland S (2007) Peripheral regeneration. Annu Rev Neurosci 30:209–233. doi: 10.1146/annurev.neuro.30.051606.094337 CrossRefPubMedGoogle Scholar
  28. 28.
    Akassoglou K, Yu WM, Akpinar P, Strickland S (2002) Fibrin inhibits peripheral nerve remyelination by regulating Schwann cell differentiation. Neuron 33(6):861–875CrossRefPubMedGoogle Scholar
  29. 29.
    Sato T, Okumura F, Iguchi A, Ariga T, Hatakeyama S (2012) TRIM32 promotes retinoic acid receptor alpha-mediated differentiation in human promyelogenous leukemic cell line HL60. Biochem Biophys Res Commun 417(1):594–600. doi: 10.1016/j.bbrc.2011.12.012 CrossRefPubMedGoogle Scholar
  30. 30.
    Bahnassawy L, Perumal TM, Gonzalez-Cano L, Hillje AL, Taher L, Makalowski W, Suzuki Y, Fuellen G, del Sol A, Schwamborn JC (2015) TRIM32 modulates pluripotency entry and exit by directly regulating Oct4 stability. Sci Rep 5:13456. doi: 10.1038/srep13456 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Huang C (2010) Roles of E3 ubiquitin ligases in cell adhesion and migration. Cell Adhes Migr 4 (1):10–18CrossRefGoogle Scholar
  32. 32.
    Hokfelt T, Zhang X, Wiesenfeld-Hallin Z (1994) Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci 17(1):22–30CrossRefPubMedGoogle Scholar
  33. 33.
    Eser F, Aktekin LA, Bodur H, Atan C (2009) Etiological factors of traumatic peripheral nerve injuries. Neurol India 57(4):434–437. doi: 10.4103/0028-3886.55614 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Yonghua Liu
    • 1
    • 2
    • 3
  • Weijie Wu
    • 2
  • Huiguang Yang
    • 4
  • Zhengming Zhou
    • 4
  • Xiaojian Zhu
    • 5
  • Chi Sun
    • 2
  • Yuxi Liu
    • 2
  • Zhaohui Yu
    • 2
  • Yuyan Chen
    • 6
  • Youhua Wang
    • 2
    Email author
  1. 1.Jiangsu Province Key Laboratory for Inflammation and Molecular Drug TargetNantong UniversityNantongPeople’s Republic of China
  2. 2.Department of Orthopaedics, Affiliated Hospital of Nantong UniversityNantong UniversityNantongPeople’s Republic of China
  3. 3.Department of Pathogen Biology, Medical CollegeNantong UniversityNantongPeople’s Republic of China
  4. 4.Department of Orthopaedics, Affiliated Jiangyin Hospital of Nantong UniversityNantong UniversityNantongPeople’s Republic of China
  5. 5.Department of Orthopaedics, Affiliated Mental Health Center of Nantong UniversityNantong UniversityNantongPeople’s Republic of China
  6. 6.Class 2, Grade 13, Clinical Medicine, Medical CollegeNantong UniversityNantongPeople’s Republic of China

Personalised recommendations