Quantitative proteomic analysis of the retina in the rat model of non-arteritic anterior ischemic optic neuropathy_Chinese Journal of Ocular Fundus Diseases

Authors：

Hu Liying , Li Zhiqing , Zhang Yan , Shao Xianfeng , Guo Xiaoxue , Yu Dawei ,  Li Xiaorong

Tianjin Key Laboratory of Retinal Functions and Diseases, Tianjin Branch of National Clinical Research Center for Ocular Disease, Eye Institute and School of Optometry, Tianjin Medical University Eye Hospital, Tianjin 300384, China;

Corresponding author：

Li Xiaorong, Email: xiaorli@163.com

Keywords：

Optic neuropathy, ischemic; Optic nerve; Retina; Proteomics

DOI：

10.3760/cma.j.cn511434-20201124-00522

Video：

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Objective To analyze the protein expression changes in the retina of non-arteritic anterior ischemic optic neuropathy (NAION) in rats.Methods The rat NAION (rNAION) model was established by Rose Bengal and laser. Twenty Sprague-Dawley rats were randomly divided into 4 groups, the normal control group, the laser control group, the RB injection control group, and the rNAION model group, with 5 rats in each group. The right eye was used as the experimental eye. The retina was dissected at the third day after modeling. Enzyme digestion method was used for sample preparation and data collection was performed in a non-dependent collection mode. The data were quantitatively analyzed by SWATH quantitative mass spectrometry, searching for differential proteins and performing function and pathway analysis.Results Compared with the other three control groups, a total of 184 differential proteins were detected in the rNAION group (expression fold greater than 1.5 times and P＜0.05), including 99 up-regulated proteins and 85 down-regulated proteins. The expressions of glial fibrillary acidic protein, guanine nucleotide binding protein 4, laminin 1, 14-3-3γ protein YWHAG were increased. Whereas the expressions of Leucine-rich glioma-inactivated protein 1, secretory carrier-associated membrane protein 5, and Clathrin coat assembly protein AP180 were decreased. The differential proteins are mainly involved in biological processes such as nerve growth, energy metabolism, vesicle-mediated transport, the regulation of synaptic plasticity, apoptosis and inflammation. Pathway enrichment analysis showed that PI3K-Akt signaling pathway and complement and thrombin reaction pathway was related to the disease.Conclusion The protein expressions of energy metabolism, nerve growth, synaptic vesicle transport and PI3K-Akt signaling pathway can regulate the neuronal regeneration and apoptosis in NAION.

Citation： Hu Liying, Li Zhiqing, Zhang Yan, Shao Xianfeng, Guo Xiaoxue, Yu Dawei, Li Xiaorong. Quantitative proteomic analysis of the retina in the rat model of non-arteritic anterior ischemic optic neuropathy. Chinese Journal of Ocular Fundus Diseases, 2021, 37(3): 206-213. doi: 10.3760/cma.j.cn511434-20201124-00522 Copy

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1. Johnson LN, Arnold AC. Incidence of nonarteritic and arteritic anterior ischemic optic neuropathy: population-based study in the state of Missouri and Los Angeles county, California[J]. J Neuroophthalmol, 1994, 14(1): 38-44.
2. Levin LA, Louhab A. Apoptosis of retinal ganglion cells in anterior ischemic optic neuropathy[J]. Arch phthalmol, 1996, 114(4): 488-491. DOI: 10.1001/archopht.1996.01100130484027.
3. Slater BJ, Mehrabian Z, Guo Y, et al. Rodent anterior ischemic optic neuropathy (rAION) induces regional retinal ganglion cell apoptosis with a unique temporal pattern[J]. Invest Ophthalmol Vis Sci, 2008, 49(8): 3671-3676. DOI: 10.1167/iovs.07-0504.
4. Salgado C, Vilson F, Miller NR, et al. Cellular inflammation in nonarteritic anterior ischemic optic neuropathy and its primate model[J]. Arch Ophthalmol, 2011, 129(12): 1583-1591. DOI: 10.1001/archophthalmol.2011.351.
5. Abu-Amero KK, Bosley TM. Increased relative mitochondrial DNA content in leucocytes of patients with NAION[J]. Br J Ophthalmol, 2006, 90(7): 823-825. DOI: 10.1136/bjo.2006.090332.
6. Chen XL, Rao J, Zheng Z, et al. Integrated tear proteome and metabolome reveal panels of inflammatory-related molecules via key regulatory pathways in dry eye syndrome[J]. J Proteome Res, 2019, 18(5): 2321-2330. DOI: 10.1021/acs.jproteome.9b00149.
7. Funke S, Perumal N, Bell K, et al. The potential impact of recent insights into proteomic changes associated with glaucoma[J]. Expert Rev Proteomics, 2017, 14(4): 311-334. DOI: 10.1080/14789450.2017.1298448.
8. 肖静, 张晓敏, 李筱荣. 糖尿病视网膜病变的蛋白质组学研究进展[J]. 中华眼底病杂志, 2018, 34(4): 407-411. DOI: 10.3760/cma.j.issn.1005-1015.2018.04.024.Xiao J, Zhang XM, Li XR. Research progress of proteomic in diabetic retinopathy[J]. Chin J Ocul Fundus Dis, 2018, 34(4): 407-411. DOI: 10.3760/cma.j.issn.1005-1015.2018.04.024.
9. Gillet LC, Navarro P, Tate S, et al. Targeted data extraction of the MS/MS spectra generated by data-independent acquisition: a new concept for consistent and accurate proteome analysis[J/OL]. Mol Cell Proteomics, 2012, 11(6): O111.016717[2012-01-18]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3433915/. DOI: 10.1074/mcp.O111.016717.
10. Selevsek N, Chang CY, Gillet LC, et al. Reproducible and consistent quantification of the Saccharomyces cerevisiae proteome by SWATH-mass spectrometry[J]. Mol Cell Proteomics, 2015, 14(3): 739-749. DOI: 10.1074/mcp.M113.035550.
11. Huang Q, Yang L, Luo J, et al. SWATH enables precise label-free quantification on proteome scale[J]. Proteomics, 2015, 15(7): 1215-1223. DOI: 10.1002/pmic.201400270.
12. Bernstein SL, Guo Y, Kelman SE, et al. Functional and cellular responses in a novel rodent model of anterior ischemic optic neuropathy[J]. Invest Ophthalmol Vis Sci, 2003, 44(10): 4153-4162. DOI: 10.1167/iovs.03-0274.
13. 王一玮, 陈婷, 马瑾, 等. 大鼠非动脉炎性前部缺血性视神经病变模型RGC及视神经损伤的特点[J]. 中华眼科杂志, 2016, 52(12): 918-923. DOI: 10.3760/cma.j.issn.0412-4081.2016.12.009.Wang YW, Chen T, Ma J, et al. Temporal and spatial characteristics of RGC death and axon degeneration in the rat model of nonarteritic anterior ischemic optic neuropathy[J]. Chin J Ophthalmol, 2016, 52(12): 918-923. DOI: 10.3760/cma.j.issn.0412-4081.2016.12.009.
14. Zhang C, Guo Y, Miller NR, et al. Optic nerve infarction and post ischemic inflammation in the rodent model of anterior ischemic optic neuropathy(rAION)[J]. Brain Res, 2009, 1264: 67-75. DOI: 10.1016/j.brainres.2008.12.075.
15. Zhang C, Guo Y, Slater BJ, et al. Axonal degeneration regeneration and ganglion cell death in a rodent model of anterior ischemie optic neuropathy (rAION)[J]. Exp Eye Res, 2010, 91(2): 286-292. DOI: 10.1016/j.exer.2010.05.021.
16. Fard MA, Fakhree S, Ameri A. Posterior pole retinal thickness for detection of structural damage in anterior ischaemic optic neuropathy[J]. Neuroophthalmology, 2013, 37(5): 183-191. DOI: 10.3109/01658107.2013.809462.
17. Cho KJ, Kim JH, Park HY, et al. Glial cell response and iNOS expression in the optic nerve head and retina of the rat following acute high IOP ischemia-reperfusion[J]. Brain Res, 2011, 1403: 67-77. DOI: 10.1016/j.brainres.2011.06.005.
18. Feilchenfeld Z, Yücel YH, Gupta N. Oxidative injury to blood vessels and glia of the pre-laminar optic nerve head in human glaucoma[J]. Exp Eye Res, 2008, 87(5): 409-414. DOI: 10.1016/j.exer.2008.07.011.
19. Tang F, Xu F, Cui L, et al. The expression and role of PIDD in retina after optic nerve crush[J]. J Mol Histol, 2020, 51(1): 89-97. DOI: 10.1007/s10735-020-09860-1.
20. Huang Y, Li Z, Wang N, et al. Roles of PI3K and JAK pathways in viability of retinal ganglion cells after acute elevation of intraocular pressure in rats with different autoimmune backgrounds[J/OL]. BMC Neurosci, 2008, 11(9): 78[2008-08-11]. https://bmcneurosci.biomedcentral.com/articles/10.1186/1471-2202-9-78. DOI: 10.1186/1471-2202-9-78.
21. Luo JM, Cen LP, Zhang XM, et al. PI3K/Akt, JAK/STAT and MEK/ERK pathway inhibition protects retinal ganglion cells via different mechanisms after optic nerve injury[J]. Eur J Neurosci, 2007, 26(4): 828-842. DOI: 10.1111/j.1460-9568.2007.05718.x.
22. Elsherbiny NM, Abdel-Mottaleb Y, Elkazaz AY, et al. Carbamazepine alleviates retinal and optic nerve neural degeneration in diabetic mice via nerve growth factor-induced PI3K/Akt/mTOR activation[J/OL]. Front Neurosci, 2019, 13: 1089[2019-11-01]. http://europepmc.org/article/MED/31736682. DOI: 10.3389/fnins.2019.01089.
23. McKee KK, Yang DH, Patel R, et al. Schwann cell myelination requires integration of laminin activities[J]. J Cell Sci, 2012, 125(Pt 19): 4609-4619. DOI: 10.1242/jcs.107995.
24. Nicolás-Pérez M, Kuchling F, Letelier J, et al. Analysis of cellular behavior and cytoskeletal dynamics reveal a constriction mechanism driving optic cup morphogenesis[J/OL]. E Life, 2016, 5: e15797[2016-10-31]. http://europepmc.org/article/MED/27797321. DOI: 10.7554/eLife.15797.
25. Sun YM, Cooper M, Finch S, et al. Rest-mediated regulation of extracellular matrix is crucial for neural development[J/OL]. PLoS One, 2008, 3(11): e3656[2008-11-06]. http://europepmc.org/article/MED/18987749. DOI: 10.1371/journal.pone.0003656.
26. Ye GX, Qin Y, Wang S, et al. LAMC1 promotes the Warburg effect in hepatocellular carcinoma cells by regulating PKM2 expression through AKT pathway[J]. Cancer Biol Ther, 2019, 20(5): 711-719. DOI: 10.1080/15384047.2018.1564558.
27. Downes GB, Gautam N. The G protein subunit gene families[J]. Genomics, 1999, 62(3): 544-552. DOI: 10.1006/geno.1999.5992.
28. Bouter Y, Kacprowski T, Weissmann R, et al. Deciphering the molecular profile of plaques, memory decline and neuron loss in two mouse models for Alzheimer’s disease by deep sequencing[J/OL]. Front Aging Neurosci, 2014, 6: 75[2014-10-16]. http://europepmc.org/article/MED/24795628. DOI:10.3389/fnagi.2014.00075.
29. Bonham LW, Evans DS, Liu YM, et al. Neurotransmitter pathway genes in cognitive decline during aging: evidence for GNG4 and KCNQ2 genes[J]. Am J Alzheimers Dis Other Demen, 2018, 33(3): 153-165. DOI: 10.1177/1533317517739384.
30. Pal J, Patil V, Mondal B, et al. Epigenetically silenced GNG4 inhibits SDF1α/CXCR4 signaling in mesenchymal glioblastoma[J]. Genes Cancer, 2016, 7(3): 136-147. DOI: 10.18632/genesandcancer.105.
31. Morrison D. 14-3-3: modulators of signaling proteins?[J]. Science, 1994, 266(5182): 56-57. DOI: 10.1126/science.7939645.
32. Horie M, Suzuki M, Takahashi E, et al. Cloning, expression, and chromosomal mapping of the human 14-3-3gamma gene (YWHAG) to 7q11.23[J]. Genomics, 1999, 60(2): 241-243. DOI: 10.1006/geno.1999.5887.
33. Cornell B, Wachi T, Zhukarev V, et al. Overexpression of the 14-3-3gamma protein in embryonic mice results in neuronal migration delay in the developing cerebral cortex[J]. Neurosci Lett, 2016, 628: 40-46. DOI: 10.1016/j.neulet.2016.06.009.
34. Sathe G, Na CH, Renuse S, et al. Quantitative proteomic profiling of cerebrospinal fluid to identify candidate biomarkers for Alzheimer's disease[J/OL]. Proteomics Clin Appl, 2019, 13(4): e1800105[2019-1-25]. http://europepmc.org/article/MED/30578620. DOI: 10.1002/prca.201800105.
35. Fusco C, Micale L, Augello B, et al. Smaller and larger deletions of the Williams Beuren syndrome region implicate genes involved in mild facial phenotype, epilepsy and autistic traits[J]. Eur J Hum Genet, 2014, 22(1): 64-70. DOI: 10.1038/ejhg.2013.101.
36. Ramocki MB, Bartnik M, Szafranski P, et al. Recurrent distal 7q11.23 deletion including HIP1 and YWHAG identified in patients with intellectual disabilities, epilepsy, and neurobehavioral problems[J]. Am J Hum Genet, 2010, 87(6): 857-865. DOI: 10.1016/j.ajhg.2010.10.019.
37. Chu YW, Wang CR, Weng FB, et al. MicroRNA-222 contributed to cell proliferation, invasion and migration via regulating YWHAG in osteosarcoma[J]. Eur Rev Med Pharmacol Sci, 2018, 22(9): 2588-2597. DOI: 10.26355/eurrev_201805_14952.
38. Inamdar SM, Lankford CK, Laird JG, et al. Analysis of 14-3-3 isoforms expressed in photoreceptors[J]. Exp Eye Res, 2018, 170: 108-116. DOI: 10.1016/j.exer.2018.02.022.
39. Zhou YD, Zhang DW, Ozkaynak E, et al. Epilepsy gene LGI1 regulates postnatal developmental remodeling of retinogeniculate synapses[J]. J Neurosci, 2012, 32(3): 903-910. DOI: 10.1523/JNEUROSCI.5191-11.2012.
40. Kegel L, Aunin E, Meijer D, et al. LGI proteins in the nervous system[J]. ASN Neuro, 2013, 5(3): 167-181. DOI: 10.1042/AN20120095.
41. Ishikawa K, Nagase T, Suyama M, et al. Prediction of the coding sequences of unidentified human genes. Ⅹ. The complete sequences of 100 new cDNA clones from brain which can code for large proteins in vitro[J]. DNA Res, 1998, 5(3): 169-176. DOI: 10.1093/dnares/5.3.169.
42. Gonthier B, Nasarre C, Roth L, et al. Functional interaction between matrix metalloproteinase-3 and semaphorin-3C during cortical axonal growth and guidance[J]. Cereb Cortex, 2007, 17(7): 1712-1721. DOI: 10.1093/cercor/bhl082.
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Chinese Journal of Ocular Fundus Diseases

Quantitative proteomic analysis of the retina in the rat model of non-arteritic anterior ischemic optic neuropathy

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