Possible role of Sox11 in a rat model of surgical brain injury

Document Type : Original Article

Authors

1 Department of Rehabilitation, Zhangjiagang TCM Hospital Affiliated to Nanjing University of Chinese Medicine, Zhangjiagang, China

2 Department of Anesthesiology, Zhangjiagang TCM Hospital Affiliated to Nanjing University of Chinese Medicine, Zhangjiagang, China

Abstract

Objective(s): Sox11, one of the SoxC family members, is an important transcription factor during neural development and neurogenesis. However, there is no report about its function in neural apoptosis. This research aims to examine the function of Sox11 in surgical brain injury (SBI).
Materials and Methods: We used 90 Sprague-Dawley rats to develop the SBI models and the siRNA of Sox11 to study the roles of Sox11. Western blot, real-time PCR, immunofluorescence, neuron apoptosis and necrosis, brain edema, and neurological score were determined.
Results: The gene and protein amount of Sox11, compared with the Sham group, were increased after SBI, which reached a peak at 12 hr. In addition, following the application of siRNAs, the amount of Sox11 protein was significantly less than that in the SBI group. On the other hand, neuronal apoptosis, necrosis, and brain edema were significantly increased, while neurological scores were decreased.
Conclusion: These findings demonstrate the role of Sox11 following nerve injury induced by SBI. Inhibition of Sox11 with siRNA may lead to neuronal injury and cell death, aggravating secondary brain injury after SBI.

Keywords

Main Subjects

References

1. Kim CH, McBride DW, Sherchan P, Person CE, Gren ECK, Kelln W, et al. Crotalus helleri venom preconditioning reduces postoperative cerebral edema and improves neurological outcomes after surgical brain injury. Neurobiol Dis 2017; 107:66-72.
2. Huang L, Woo W, Sherchan P, Khatibi NH, Krafft P, Rolland W, et al. Valproic acid pretreatment reduces brain edema in a rat model of surgical brain injury. Acta Neurochir Suppl 2016; 121:305-310.
3. Jadhav V, Ostrowski RP, Tong W, Matus B, Jesunathadas R, Zhang JH. Cyclo-oxygenase-2 mediates hyperbaric oxygen preconditioning-induced neuroprotection in the mouse model of surgical brain injury. Stroke 2009; 40:3139-3142.
4. Wu MY, Gao F, Tang JF, Shen JC, Gao R, Dang BQ, et al. Possible mechanisms of the PERK pathway on neuronal apoptosis in a rat model of surgical brain injury. Am J Transl Res 2021; 13:732-742.
5. Reiprich S, Wegner M. From CNS stem cells to neurons and glia: Sox for everyone. Cell Tissue Res 2015; 359:111-124.
6. Kavyanifar A, Turan S, Lie DC. SoxC transcription factors: Multifunctional regulators of neurodevelopment. Cell Tissue Res 2018; 371:91-103.
7. Bhattaram P, Penzo-Mendez A, Sock E, Colmenares C, Kaneko KJ, Vassilev A, et al. Organogenesis relies on SoxC transcription factors for the survival of neural and mesenchymal progenitors. Nat Commun 2010; 1:9-20.
8. Dy P, Penzo-Mendez A, Wang H, Pedraza CE, Macklin WB, Lefebvre V. The three SoxC proteins--Sox4, Sox11 and Sox12--exhibit overlapping expression patterns and molecular properties. Nucleic Acids Res 2008; 36:3101-3117.
9. Fang M, Fan S, Yao X, Liu N, Gao J, Wang Z, et al. Transfection of Sox11 plasmid alleviates ventilator-induced lung injury via Sox11 and FAK. Biochem Biophys Res Commun 2019; 512:182-188.
10. Neirijnck Y, Reginensi A, Renkema KY, Massa F, Kozlov VM, Dhib H, et al. Sox11 gene disruption causes congenital anomalies of the kidney and urinary tract (CAKUT). Kidney Int 2018; 93:1142-1153.
11. Muralidharan B, Khatri Z, Maheshwari U, Gupta R, Roy B, Pradhan SJ, et al. LHX2 interacts with the NuRD complex and regulates cortical neuron subtype determinants Fezf2 and Sox11. J Neurosci 2017; 37:194-203.
12. Li Y, Wang J, Zheng Y, Zhao Y, Guo M, Li Y, et al. Sox11 modulates neocortical development by regulating the proliferation and neuronal differentiation of cortical intermediate precursors. Acta Biochim Biophys Sin (Shanghai) 2012; 44:660-668.
13. Sun W, Park KW, Choe J, Rhyu IJ, Kim IH, Park SK, et al. Identification of novel electroconvulsive shock-induced and activity-dependent genes in the rat brain. Biochem Biophys Res Commun 2005; 327:848-856.
14. Jankowski MP, McIlwrath SL, Jing X, Cornuet PK, Salerno KM, Koerber HR, et al. Sox11 transcription factor modulates peripheral nerve regeneration in adult mice. Brain Res 2009; 1256:43-54.
15. Kim DK, Han SB, Hong ST, Choi YJ, Sun W, Geum D, et al. Expression of Sox11 and Brn transcription factors during development and following transient forebrain ischemia in the rat. Neurosci Lett 2008; 433:259-264.
16. Sciences CAfLA. Laboratory animal-guideline for using animals in the education. 2017.
17. Zakhary G, Sherchan P, Li Q, Tang J, Zhang JH. Modification of kynurenine pathway via inhibition of kynurenine hydroxylase attenuates surgical brain injury complications in a male rat model. J Neurosci Res 2020; 98:155-167.
18. Shen H, Chen Z, Wang Y, Gao A, Li H, Cui Y, et al. Role of Neurexin-1beta and Neuroligin-1 in Cognitive Dysfunction After Subarachnoid Hemorrhage in Rats. Stroke 2015; 46:2607-2615.
19. Sherchan P, Huang L, Akyol O, Reis C, Tang J, Zhang JH. Recombinant Slit2 reduces surgical brain injury induced blood brain barrier disruption via Robo4 dependent Rac1 activation in a rodent Model. Sci Rep 2017; 7:746-756.
20. Shi M, Gong Y, Wu M, Gu H, Yu J, Gao F, et al. Downregulation of TREM2/NF-кB signaling may damage the blood-brain barrier and aggravate neuronal apoptosis in experimental rats with surgically injured brain. Brain Res Bull 2022; 183:116-126.
21. Li J, Wu M, Gong Y, Tang J, Shen J, Xu L, et al. Inhibition of LRRK2-Rab10 pathway improves secondary brain injury after surgical brain injury in rats. Front Surg 2021; 8:749310-749320.
22. Gong Y, Wu M, Shen J, Tang J, Li J, Xu J, et al. Inhibition of the NKCC1/NF-kappaB signaling pathway decreases inflammation and improves brain edema and nerve cell apoptosis in an SBI rat model. Front Mol Neurosci 2021; 14:641993-6411007.
23. Wu MY, Gao F, Yang XM, Qin X, Chen GZ, Li D, et al. Matrix metalloproteinase-9 regulates the blood brain barrier via the hedgehog pathway in a rat model of traumatic brain injury. Brain Res 2020; 1727:146553.
24. McBride DW, Wang Y, Adam L, Oudin G, Louis JS, Tang J, et al. Correlation between subacute sensorimotor deficits and brain edema in rats after surgical brain injury. Acta Neurochir Suppl 2016; 121:317-321.
25. Gao F, Li D, Rui Q, Ni H, Liu H, Jiang F, et al. Annexin A7 levels increase in rats with traumatic brain injury and promote secondary brain injury. Front Neurosci 2018; 12:357-364.
26. Xu S, Yu J, Wang Z, Ni C, Xia L, Tang T. SOX11 promotes osteoarthritis through induction of TNF-alpha. Pathol Res Pract 2019; 215:152442.
27. Balta EA, Wittmann MT, Jung M, Sock E, Haeberle BM, Heim B, et al. Phosphorylation modulates the subcellular localization of SOX11. Front Mol Neurosci 2018; 11:211-223.
28. Wang X, Asplund AC, Porwit A, Flygare J, Smith CI, Christensson B, et al. The subcellular Sox11 distribution pattern identifies subsets of mantle cell lymphoma: Correlation to overall survival. Br J Haematol 2008; 143:248-252.
29. Beekman R, Amador V, Campo E. SOX11, a key oncogenic factor in mantle cell lymphoma. Curr Opin Hematol 2018; 25:299-306.
30. Thein DC, Thalhammer JM, Hartwig AC, Crenshaw EB, 3rd, Lefebvre V, Wegner M, et al. The closely related transcription factors Sox4 and Sox11 function as survival factors during spinal cord development. J Neurochem 2010; 115:131-141.
31. Waldron-Roby E, Hoerauf J, Arbez N, Zhu S, Kulcsar K, Ross CA. Sox11 reduces Caspase-6 cleavage and activity. PLoS One 2015; 10:e0141439-141456.
32. Fang M, Xu T, Fan S, Liu N, Li L, Gao J, et al. SOX11 and FAK participate in the stretchinduced mechanical injury to alveolar type 2 epithelial cells. Int J Mol Med 2021; 47:361-373.
33. Norsworthy MW, Bei F, Kawaguchi R, Wang Q, Tran NM, Li Y, et al. Sox11 expression promotes regeneration of some retinal ganglion cell types but kills others. Neuron 2017; 94:1112-1120.
34. Jing X, Wang T, Huang S, Glorioso JC, Albers KM. The transcription factor Sox11 promotes nerve regeneration through activation of the regeneration-associated gene Sprr1a. Exp Neurol 2012; 233:221-232.
35. Guo Y, Liu S, Zhang X, Wang L, Zhang X, Hao A, et al. Sox11 promotes endogenous neurogenesis and locomotor recovery in mice spinal cord injury. Biochem Biophys Res Commun 2014; 446:830-835.
36. Salerno KM, Jing X, Diges CM, Cornuet PK, Glorioso JC, Albers KM. Sox11 modulates brain-derived neurotrophic factor expression in an exon promoter-specific manner. J Neurosci Res 2012; 90:1011-1019.
Iranian Journal of Basic Medical Sciences
Volume 27, Issue 7
July 2024
Pages 888-894

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