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.
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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
Fricker FR, Bennett DL (2011) The role of neuregulin-1 in the response to nerve injury. Fut Neurol 6(6):809–822
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
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
Kury P, Stoll G, Muller HW (2001) Molecular mechanisms of cellular interactions in peripheral nerve regeneration. Curr Opin Neurol 14(5):635–639
Fawcett JW, Keynes RJ (1990) Peripheral nerve regeneration. Annu Rev Neurosci 13:43–60. doi:10.1146/annurev.ne.13.030190.000355
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
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
Meroni G (2012) Genomics and evolution of the TRIM gene family. Adv Exp Med Biol 770:1–9
Cambiaghi V, Giuliani V, Lombardi S, Marinelli C, Toffalorio F, Pelicci PG (2012) TRIM proteins in cancer. Adv Exp Med Biol 770:77–91
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Ide C (1996) Peripheral nerve regeneration. Neurosci Res 25(2):101–121
Chen ZL, Yu WM, Strickland S (2007) Peripheral regeneration. Annu Rev Neurosci 30:209–233. doi:10.1146/annurev.neuro.30.051606.094337
Akassoglou K, Yu WM, Akpinar P, Strickland S (2002) Fibrin inhibits peripheral nerve remyelination by regulating Schwann cell differentiation. Neuron 33(6):861–875
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
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
Huang C (2010) Roles of E3 ubiquitin ligases in cell adhesion and migration. Cell Adhes Migr 4 (1):10–18
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
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
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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).
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Yonghua Liu and Weijie Wu contributed equally to this work.
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Liu, Y., Wu, W., Yang, H. et al. Upregulated Expression of TRIM32 Is Involved in Schwann Cell Differentiation, Migration and Neurite Outgrowth After Sciatic Nerve Crush. Neurochem Res 42, 1084–1095 (2017). https://doi.org/10.1007/s11064-016-2142-3
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DOI: https://doi.org/10.1007/s11064-016-2142-3