Proteomic analysis of chick retina during early recovery from lens‑induced myopia

Zhou,Yun  Yun; Chun,Rachel  Ka Man; Wang,Jian  Chao; Zuo,Bing; Li,King  Kit; Lam,Thomas  Chuen; Liu,Quan; To,Chi‑Ho

doi:10.3892/mmr.2018.8954

Proteomic analysis of chick retina during early recovery from lens‑induced myopia

Authors:
- Yun Yun Zhou
- Rachel Ka Man Chun
- Jian Chao Wang
- Bing Zuo
- King Kit Li
- Thomas Chuen Lam
- Quan Liu
- Chi‑Ho To
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Affiliations: Refractive Surgery Department, State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat‑sen University, Guangzhou, Guangdong 510060, P.R. China, Laboratory of Experimental Optometry, Centre for Myopia Research, School of Optometry, Hong Kong Polytechnic University, Hong Kong 999077, SAR, P.R. China, Department of Ophthalmology, The Second Affiliated Hospital of Xi'an Jiaotong University, Xi'an, Shanxi 710049, P.R. China
Published online on: May 3, 2018 https://doi.org/10.3892/mmr.2018.8954
Pages: 59-66
Copyright : © Zhou et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY 4.0].

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Abstract

Myopia development has been extensively studied from different perspectives. Myopia recovery is also considered important for understanding the development of myopia. However, despite several previous studies, retinal proteomics during recovery from myopia is still relatively unknown. Therefore, the aim of the present study was to investigate the changes in protein profiles of chicken retinas during early recovery from lens‑induced myopia to evaluate the signals involved in the adjustment of this refractive disorder. Three‑day old chickens wore glasses for 7 days (‑10D lens over the right eye and a plano lens as control over the left eye), followed by 24 h without lenses. Protein expression in the retina was measured by two‑dimensional fluorescence difference gel electrophoresis (2D‑DIGE). Pro‑Q Diamond phosphoprotein staining 2D gel electrophoresis was used to analyze phosphoprotein profiles. Protein spots with significant differences (P<0.05) were analyzed by mass spectrometry. The minus lens‑treated eye became myopic, however following 24 h recovery, less myopia was observed. 2D‑DIGE proteomic analysis demonstrated that three identified protein spots were upregulated at least 1.2‑fold in myopic recovery retinas compared with those of the controls, Ras related protein Rab‑11B, S‑antigen retina and pineal gland and 26S proteasome non‑ATPase regulatory subunit 14. Pro‑Q Diamond images further revealed three protein spots with significant changes (at least 1.8‑fold): β‑tubulin was downregulated, while peroxiredoxin 4 and ubiquitin carboxyl‑terminal hydrolase‑L1 were upregulated in the recovery retinas compared with the control eye retinas. The present study detected previously unreported protein changes in recovering eyes, therefore revealing their potential involvement in retinal remodeling during eye ball reforge.

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1	Norton TT, Amedo AO and Siegwart JT Jr: The effect of age on compensation for a negative lens and recovery from lens-induced myopia in tree shrews (Tupaia glis belangeri). Vision Res. 50:564–576. 2010. View Article : Google Scholar : PubMed/NCBI
2	Smith EL III, Hung LF, Arumugam B and Huang J: Negative lens-induced myopia in infant monkeys: Effects of high ambient lighting. Invest Ophthalmol Vis Sci. 54:2959–2969. 2013. View Article : Google Scholar : PubMed/NCBI
3	Zhou X, Ye J, Willcox MD, Xie R, Jiang L, Lu R, Shi J, Bai Y and Qu J: Changes in protein profiles of guinea pig sclera during development of form deprivation myopia and recovery. Mol Vis. 16:2163–2174. 2010.PubMed/NCBI
4	Shen W and Sivak JG: Eyes of a lower vertebrate are susceptible to the visual environment. Invest Ophthalmol Vis Sci. 48:4829–4837. 2007. View Article : Google Scholar : PubMed/NCBI
5	Wallman J and Winawer J: Homeostasis of eye growth and the question of myopia. Neuron. 43:447–468. 2004. View Article : Google Scholar : PubMed/NCBI
6	Zee BM and Garcia BA: Discovery of lysine post-translational modifications through mass spectrometric detection. Essays Biochem. 52:147–163. 2012. View Article : Google Scholar : PubMed/NCBI
7	Eichler J and Maupin-Furlow J: Post-translation modification in Archaea: Lessons from Haloferax volcanii and other haloarchaea. FEMS Microbiol Rev. 37:583–606. 2013. View Article : Google Scholar : PubMed/NCBI
8	Mann M and Jensen ON: Proteomic analysis of post-translational modifications. Nat Biotechnol. 21:255–261. 2003. View Article : Google Scholar : PubMed/NCBI
9	Petrov D, Margreitter C, Grandits M, Oostenbrink C and Zagrovic B: A systematic framework for molecular dynamics simulations of protein post-translational modifications. PLoS Comput Biol. 9:e10031542013. View Article : Google Scholar : PubMed/NCBI
10	Zolnierowicz S and Bollen M: Protein phosphorylation and protein phosphatases. De Panne, Belgium, September 19–24, 1999. EMBO J. 19:483–488. 2000. View Article : Google Scholar : PubMed/NCBI
11	Zhu X, McBrien NA, Smith EL III, Troilo D and Wallman J: Eyes in various species can shorten to compensate for myopic defocus. Invest Ophthalmol Vis Sci. 54:2634–2644. 2013. View Article : Google Scholar : PubMed/NCBI
12	Frost MR and Norton TT: Differential protein expression in tree shrew sclera during development of lens-induced myopia and recovery. Mol Vis. 13:1580–1588. 2007.PubMed/NCBI
13	Frost MR and Norton TT: Alterations in protein expression in tree shrew sclera during development of lens-induced myopia and recovery. Invest Ophthalmol Vis Sci. 53:322–336. 2012. View Article : Google Scholar : PubMed/NCBI
14	Amedo AO and Norton TT: Visual guidance of recovery from lens-induced myopia in tree shrews (Tupaia glis belangeri). Ophthalmic Physiol Opt. 32:89–99. 2012. View Article : Google Scholar : PubMed/NCBI
15	Wang JC, Chun RK, Zhou YY, Zuo B, Li KK, Liu Q and To CH: Both the central and peripheral retina contribute to myopia development in chicks. Ophthalmic Physiol Opt. 35:652–662. 2015. View Article : Google Scholar : PubMed/NCBI
16	Chun RK, Shan SW, Lam TC, Wong CL, Li KK, Do CW and To CH: Cyclic adenosine monophosphate activates retinal apolipoprotein A1 expression and inhibits myopic eye growth. Invest Ophthalmol Vis Sci. 56:8151–8157. 2015. View Article : Google Scholar : PubMed/NCBI
17	Lam TC, Li KK, Lo SC, Guggenheim JA and To CH: A chick retinal proteome database and differential retinal protein expressions during early ocular development. J Proteome Res. 5:771–784. 2006. View Article : Google Scholar : PubMed/NCBI
18	Lam TC, Li KK, Lo SC, Guggenheim JA and To CH: Application of fluorescence difference gel electrophoresis technology in searching for protein biomarkers in chick myopia. J Proteome Res. 6:4135–4149. 2007. View Article : Google Scholar : PubMed/NCBI
19	Wu Y, Liu Q, To C, Li K, Chun R, Yu J and Lam T: Differential retinal protein expressions during form deprivation myopia in albino guinea pigs. Curr Proteomics. 11:37–47. 2014. View Article : Google Scholar
20	Liebler DC and Zimmerman LJ: Targeted quantitation of proteins by mass spectrometry. Biochemistry. 52:3797–3806. 2013. View Article : Google Scholar : PubMed/NCBI
21	Tu C, Beharry KD, Shen X, Li J, Wang L, Aranda JV and Qu J: Proteomic profiling of the retinas in a neonatal rat model of oxygen-induced retinopathy with a reproducible ion-current-based MS1 approach. J Proteome Res. 14:2109–2120. 2015. View Article : Google Scholar : PubMed/NCBI
22	Hung LF, Wallman J and Smith EL III: Vision-dependent changes in the choroidal thickness of macaque monkeys. Invest Ophthalmol Vis Sci. 41:1259–1269. 2000.PubMed/NCBI
23	Liang H, Crewther SG, Crewther DP and Junghans BM: Structural and elemental evidence for edema in the retina, retinal pigment epithelium, and choroid during recovery from experimentally induced myopia. Invest Ophthalmol Vis Sci. 45:2463–2474. 2004. View Article : Google Scholar : PubMed/NCBI
24	Lu F, Zhou X, Jiang L, Fu Y, Lai X, Xie R and Qu J: Axial myopia induced by hyperopic defocus in guinea pigs: A detailed assessment on susceptibility and recovery. Exp Eye Res. 89:101–108. 2009. View Article : Google Scholar : PubMed/NCBI
25	Nickla DL, Zhu X and Wallman J: Effects of muscarinic agents on chick choroids in intact eyes and eyecups: Evidence for a muscarinic mechanism in choroidal thinning. Ophthalmic Physiol Opt. 33:245–256. 2013. View Article : Google Scholar : PubMed/NCBI
26	Rada JA and Palmer L: Choroidal regulation of scleral glycosaminoglycan synthesis during recovery from induced myopia. Invest Ophthalmol Vis Sci. 48:2957–2966. 2007. View Article : Google Scholar : PubMed/NCBI
27	Wildsoet C: Neural pathways subserving negative lens-induced emmetropization in chicks-insights from selective lesions of the optic nerve and ciliary nerve. Curr Eye Res. 27:371–385. 2003. View Article : Google Scholar : PubMed/NCBI
28	Ferrin G, Ranchal I, Llamoza C, Rodríguez-Perálvarez ML, Romero-Ruiz A, Aguilar-Melero P, López-Cillero P, Briceño J, Muntané J, Montero-Álvarez JL and De la Mata M: Identification of candidate biomarkers for hepatocellular carcinoma in plasma of HCV-infected cirrhotic patients by 2-D DIGE. Liver Int. 34:438–446. 2014. View Article : Google Scholar : PubMed/NCBI
29	Knowles MR, Cervino S, Skynner HA, Hunt SP, de Felipe C, Salim K, Meneses-Lorente G, McAllister G and Guest PC: Multiplex proteomic analysis by two-dimensional differential in-gel electrophoresis. Proteomics. 3:1162–1171. 2003. View Article : Google Scholar : PubMed/NCBI
30	Marouga R, David S and Hawkins E: The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal Bioanal Chem. 382:669–678. 2005. View Article : Google Scholar : PubMed/NCBI
31	Wu TL: Two-dimensional difference gel electrophoresis. Methods Mol Biol. 328:71–95. 2006.PubMed/NCBI
32	Fukuda M: Regulation of secretory vesicle traffic by Rab small GTPases. Cell Mol Life Sci. 65:2801–2813. 2008. View Article : Google Scholar : PubMed/NCBI
33	Khvotchev MV, Ren M, Takamori S, Jahn R and Südhof TC: Divergent functions of neuronal Rab11b in Ca²⁺-regulated versus constitutive exocytosis. J Neurosci. 23:10531–10539. 2003. View Article : Google Scholar : PubMed/NCBI
34	Alone DP, Tiwari AK, Mandal L, Li M, Mechler BM and Roy JK: Rab11 is required during Drosophila eye development. Int J Dev Biol. 49:873–879. 2005. View Article : Google Scholar : PubMed/NCBI
35	Pelissier A, Chauvin JP and Lecuit T: Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Curr Biol. 13:1848–1857. 2003. View Article : Google Scholar : PubMed/NCBI
36	Muto A, Aoki Y and Watanabe S: Mouse Rab11-FIP4 regulates proliferation and differentiation of retinal progenitors in a Rab11-independent manner. Dev Dyn. 236:214–225. 2007. View Article : Google Scholar : PubMed/NCBI
37	Muto A, Arai K and Watanabe S: Rab11-FIP4 is predominantly expressed in neural tissues and involved in proliferation as well as in differentiation during zebrafish retinal development. Dev Biol. 292:90–102. 2006. View Article : Google Scholar : PubMed/NCBI
38	Ng EL and Tang BL: Rab GTPases and their roles in brain neurons and glia. Brain Res Rev. 58:236–246. 2008. View Article : Google Scholar : PubMed/NCBI
39	Zhu X, Li A, Brown B, Weiss ER, Osawa S and Craft CM: Mouse cone arrestin expression pattern: Light induced translocation in cone photoreceptors. Mol Vis. 8:462–471. 2002.PubMed/NCBI
40	Palczewski K, Pulvermüller A, Buczyłko J and Hofmann KP: Phosphorylated rhodopsin and heparin induce similar conformational changes in arrestin. J Biol Chem. 266:18649–18654. 1991.PubMed/NCBI
41	Zipfel B, Schmid HA and Meissl H: Photoendocrine signal transduction in pineal photoreceptors of the trout. Role of cGMP and nitric oxide. Adv Exp Med Biol. 460:79–82. 1999. View Article : Google Scholar : PubMed/NCBI
42	Palczewski K, McDowell JH, Jakes S, Ingebritsen TS and Hargrave PA: Regulation of rhodopsin dephosphorylation by arrestin. J Biol Chem. 264:15770–15773. 1989.PubMed/NCBI
43	Finley D: Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem. 78:477–513. 2009. View Article : Google Scholar : PubMed/NCBI
44	Murata S, Yashiroda H and Tanaka K: Molecular mechanisms of proteasome assembly. Nat Rev Mol Cell Biol. 10:104–115. 2009. View Article : Google Scholar : PubMed/NCBI
45	Tanaka K: The proteasome: Overview of structure and functions. Proc Jpn Acad Ser B Phys Biol Sci. 85:12–36. 2009. View Article : Google Scholar : PubMed/NCBI
46	Kominami K, DeMartino GN, Moomaw CR, Slaughter CA, Shimbara N, Fujimuro M, Yokosawa H, Hisamatsu H, Tanahashi N, Shimizu Y, et al: Nin1p, a regulatory subunit of the 26S proteasome, is necessary for activation of Cdc28p kinase of Saccharomyces cerevisiae. EMBO J. 14:3105–3115. 1995.PubMed/NCBI
47	Lee S: Post-translational modification of proteins in toxicological research: Focus on lysine acylation. Toxicol Res. 29:81–86. 2013. View Article : Google Scholar : PubMed/NCBI
48	Xu Y, Wang X, Wang Y, Tian Y, Shao X, Wu LY and Deng N: Prediction of posttranslational modification sites from amino acid sequences with kernel methods. J Theor Biol. 344:78–87. 2014. View Article : Google Scholar : PubMed/NCBI
49	Axelsen LN, Calloe K, Holstein-Rathlou NH and Nielsen MS: Managing the complexity of communication: Regulation of gap junctions by post-translational modification. Front Pharmacol. 4:1302013. View Article : Google Scholar : PubMed/NCBI
50	Bertrand E, Fritsch C, Diether S, Lambrou G, Müller D, Schaeffel F, Schindler P, Schmid KL, van Oostrum J and Voshol H: Identification of apolipoprotein A-I as a ‘STOP’ signal for myopia. Mol Cell Proteomics. 5:2158–2166. 2006. View Article : Google Scholar : PubMed/NCBI
51	McKerracher L, Essagian C and Aguayo AJ: Marked increase in beta-tubulin mRNA expression during regeneration of axotomized retinal ganglion cells in adult mammals. J Neurosci. 13:5294–5300. 1993. View Article : Google Scholar : PubMed/NCBI
52	Nielsen K, Birkenkamp-Demtröder K, Ehlers N and Orntoft TF: Identification of differentially expressed genes in keratoconus epithelium analyzed on microarrays. Invest Ophthalmol Vis Sci. 44:2466–2476. 2003. View Article : Google Scholar : PubMed/NCBI
53	Sharma RK, O'Leary TE, Fields CM and Johnson DA: Development of the outer retina in the mouse. Brain Res Dev Brain Res. 145:93–105. 2003. View Article : Google Scholar : PubMed/NCBI
54	Wagner E, Luche S, Penna L, Chevallet M, Van Dorsselaer A, Leize-Wagner E and Rabilloud T: A method for detection of overoxidation of cysteines: Peroxiredoxins are oxidized in vivo at the active-site cysteine during oxidative stress. Biochem J. 366:777–785. 2002. View Article : Google Scholar : PubMed/NCBI
55	Wong CM, Chun AC, Kok KH, Zhou Y, Fung PC, Kung HF, Jeang KT and Jin DY: Characterization of human and mouse peroxiredoxin IV: Evidence for inhibition by Prx-IV of epidermal growth factor- and p53-induced reactive oxygen species. Antioxid Redox Signal. 2:507–518. 2000. View Article : Google Scholar : PubMed/NCBI
56	Wood ZA, Schröder E, Harris Robin J and Poole LB: Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci. 28:32–40. 2003. View Article : Google Scholar : PubMed/NCBI
57	Day IN and Thompson RJ: UCHL1 (PGP 9.5): Neuronal biomarker and ubiquitin system protein. Prog Neurobiol. 90:327–362. 2010. View Article : Google Scholar : PubMed/NCBI
58	Pan Y, Appukuttan B, Mohs K, Ashander LM and Smith JR: Ubiquitin carboxyl-terminal esterase L1 promotes proliferation of human choroidal and retinal endothelial cells. Asia Pac J Ophthalmol (Phila). 4:51–55. 2015. View Article : Google Scholar : PubMed/NCBI
59	Yu FJ, Lam TC, Liu LQ, Chun RK, Cheung JK, Li KK and To CH: Isotope-coded protein label based quantitative proteomic analysis reveals significant up-regulation of apolipoprotein A1 and ovotransferrin in the myopic chick vitreous. Sci Rep. 7:126492017. View Article : Google Scholar : PubMed/NCBI
60	Summers JA, Harper AR, Feasley CL, Van-Der-Wel H, Byrum JN, Hermann M and West CM: Identification of apolipoprotein A-I as a retinoic acid-binding protein in the eye. J Biol Chem. 291:18991–19005. 2016. View Article : Google Scholar : PubMed/NCBI
61	Aebersold R, Burlingame AL and Bradshaw RA: Western blots versus selected reaction monitoring assays: Time to turn the tables? Mol Cell Proteomics. 12:2381–2382. 2013. View Article : Google Scholar : PubMed/NCBI
62	Lundberg E, Fagerberg L, Klevebring D, Matic I, Geiger T, Cox J, Algenäs C, Lundeberg J, Mann M and Uhlen M: Defining the transcriptome and proteome in three functionally different human cell lines. Mol Syst Biol. 6:4502010. View Article : Google Scholar : PubMed/NCBI
63	Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W and Selbach M: Global quantification of mammalian gene expression control. Nature. 473:337–342. 2011. View Article : Google Scholar : PubMed/NCBI
64	Vogel C, Silva GM and Marcotte EM: Protein expression regulation under oxidative stress. Mol Cell Proteomics. 10(M111): 0092172011.PubMed/NCBI
65	Hannis JC, Manalili SM, Hall TA, Ranken R, White N, Sampath R, Blyn LB, Ecker DJ, Mandrell RE, Fagerquist CK, et al: High-resolution genotyping of Campylobacter species by use of PCR and high-throughput mass spectrometry. J Clin Microbiol. 46:1220–1225. 2008. View Article : Google Scholar : PubMed/NCBI