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Cited by 1Connexins and lens biologyAdvanced Proteomics Techniques and ApplicationsHeat shock proteins research

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Comparative proteomics in captive giant pandas to identify proteins involved in age-related cataract formation

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You, Yuyan, Bai, Chao, Wang, Wei, Zhan, Tongtong, Hu, Xin, Hao, Feier, Xia, Maohua, Liu, Yan, Ma, Tao, Liu, Yanhui, Zheng, Changming, Pu, Tianchun, Zhang, Yizhuo, Lu, Yanping, Ding, Nan, Li, Jing, Yin, Yanqiang, Chen, Yucun, Wang, Liqin, Zhou, Jun, Niu, Lili, Xiu, Yunfang, Lu, Yan, Jia, Ting, Liu, Xuefeng, Zhang, Chenglin·2023·Scientific Reports
DOI 10.1038/s41598-023-40003-0PMC PMC10404263

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Abstract

Approximately 20% of aged captive giant pandas ( Ailuropoda melanoleuca ) have cataracts that impair their quality of life. To identify potential biomarkers of cataract formation, we carried out a quantitative proteomics analysis of 10 giant pandas to find proteins differing in abundance between healthy and cataract-bearing animals. We identified almost 150 proteins exceeding our threshold for differential abundance, most of which were associated with GO categories related to extracellular localization. The most significant differential abundance was associated with components of the proteasome and other proteins with a role in proteolysis or its regulation, most of which were depleted in pandas with cataracts. Other modulated proteins included components of the extracellular matrix or cytoskeleton, as well as associated signaling proteins and regulators, but we did not find any differentially expressed transcription factors. These results indicate that the formation of cataracts involves a complex post-transcriptional network of signaling inside and outside lens cells to drive stress responses as a means to address the accumulation of protein aggregates triggered by oxidative damage. The modulated proteins also indicate that it should be possible to predict the onset of cataracts in captive pandas by taking blood samples and testing them for the presence or absence of specific protein markers.

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Research works printed but not linked: 38

  1. Truscott, R. J. W. Age-related nuclear cataract: Oxidation is the key. Exp. Eye Res. 80, 709–725. https://doi.org/10.1016/j.exer.2004.12.007 (2005). · DOI
  2. Urfer, S. R., Greer, K. & Wolf, N. S. Age-related cataract in dogs: A biomarker for life span and its relation to body size. Age 33, 451–460. https://doi.org/10.1007/s11357-010-9158-4 (2011). · DOI
  3. Jin, Y. et al. Dental abnormalities in eight captive giant pandas (Ailuropoda melanoleuca) in China. J. Comp. Pathol. 146, 357–364. https://doi.org/10.1016/j.jcpa.2011.08.001 (2012). · DOI
  4. Jin, Y. et al. Dental abnormalities of eight wild Qinling giant pandas (Ailuropoda melanoleuca qinlingensis), Shaanxi Province, China. J. Wildlife Dis. 51, 849–859. https://doi.org/10.7589/2014-12-289 (2015). · DOI
  5. Hammond, C. J. et al. The heritability of age-related cortical cataract: The twin eye study. Invest. Ophthalmol. Vis. Sci. 42, 601–605 (2001).
  6. Ottonello, S., Foroni, C., Carta, A., Petrucco, S. & Maraini, G. Oxidative stress and age-related cataract. Ophthalmologica 214, 78–85. https://doi.org/10.1159/000027474 (2000). · DOI
  7. Ho, M., Peng, Y., Chen, S. & Chiou, S. J. J. Senile cataracts and oxidative stress. J. Clin. Gerontol. Geriatr. 1, 17–21. https://doi.org/10.1016/j.jcgg.2010.10.006 (2010). · DOI
  8. Asbell, P. A. et al. Age-related cataract. Lancet 365, 599–609. https://doi.org/10.1016/s0140-6736(05)17911-2 (2005). · DOI
  9. Tinaztepe, O. E., Ay, M. & Eser, E. Nuclear and mitochondrial DNA of age-related cataract patients are susceptible to oxidative damage. Curr. Eye Res. 42, 583–588. https://doi.org/10.1080/02713683.2016.1200100 (2017). · DOI
  10. Uno, H. Age-related pathology and biosenescent markers in captive rhesus macaques. Age 20, 1–13. https://doi.org/10.1007/s11357-997-0001-5 (1997). · DOI
  11. Billingsley, G. et al. CRYBA4, a novel human cataract gene, is also involved in microphthalmia. Am. J. Hum. Genet. 79, 702–709. https://doi.org/10.1086/507712 (2006). · DOI
  12. Hasanova, N., Kubo, E., Kumamoto, Y., Takamura, Y. & Akagi, Y. Age-related cataracts and Prdx6: Correlation between severity of lens opacity, age and the level of Prdx 6 expression. Br. J. Ophthalmol. 93, 1081–1084. https://doi.org/10.1136/bjo.2008.152272 (2009). · DOI
  13. Zhang, Y. et al. Genetic polymorphisms of superoxide dismutases, catalase, and glutathione peroxidase in age-related cataract. Mol. Vis. 17, 2325–2332 (2011).
  14. Liu, X., Luo, Y., Zhou, P. & Lu, Y. DNA methylation mediated and oxidative stress related genes CRYAA and GJA3 in nuclear age-related cataract (ARC) and its mechanism. Invest. Ophthalmol. Vis. Sci. 56, 5877 (2015).
  15. Zhou, P., Luo, Y., Liu, X., Fan, L. & Lu, Y. Down-regulation and CpG island hypermethylation of CRYAA in age-related nuclear cataract. FASEB J. 26, 4897–4902. https://doi.org/10.1096/fj.12-213702 (2012). · DOI
  16. Wang, Y. et al. Altered DNA methylation and expression profiles of 8-oxoguanine DNA glycosylase 1 in lens tissue from age-related cataract patients. Curr. Eye Res. 40, 815–821. https://doi.org/10.3109/02713683.2014.957778 (2015). · DOI
  17. You, Y. Y. et al. Genome-wide analysis of methylation in giant pandas with cataract by methylation-dependent restriction-site associated DNA sequencing (MethylRAD). PLoS ONE 14, e0222292. https://doi.org/10.1371/journal.pone.0222292 (2019). · DOI
  18. You, Y. Y. et al. RNA-Seq analysis in giant pandas reveals the differential expression of multiple genes involved in cataract formation. BMC Genomic Data 22, 44. https://doi.org/10.1186/s12863-021-00996-x (2021). · DOI
  19. Erde, J., Loo, R. & Loo, J. A. Enhanced FASP (eFASP) to increase proteome coverage and sample recovery for quantitative proteomic experiments. J. Proteome Res. 13, 1885–1895. https://doi.org/10.1021/pr4010019 (2014). · DOI
  20. Kanehisa, M. & Goto, S. KEGG kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30. https://doi.org/10.1093/nar/27.1.29 (2000). · DOI · Paper page
  21. Kanehisa, M. Toward understanding the origin and evolution of cellular organisms. Protein Sci. 28, 1947–1951. https://doi.org/10.1002/pro.3715 (2019). · DOI · Paper page
  22. Kanehisa, M., Furumichi, M., Sato, Y., Kawashima, M. & Ishiguro-Watanabe, M. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res. 51, D587–D592. https://doi.org/10.1093/nar/gks1239 (2023). · DOI
  23. Doshna, C. W. et al. Investigation of the role of apoptosis in drug-induced cataract formation. Invest. Ophthalmol. Vis. Sci. 43, 2377 (2002).
  24. Galichanin, K., Svedlund, J. & Soderberg, P. Kinetics of GADD45α, TP53 and CASP3 gene expression in the rat lens in vivo in response to exposure to double threshold dose of UV-B radiation. Exp. Eye Res. 97, 19–23. https://doi.org/10.1016/j.exer.2012.02.003 (2012). · DOI
  25. Li, B. et al. Relationship between the altered expression and epigenetics of GSTM3 and age-related cataract. Invest. Ophthalmol. Vis. Sci. 57, 4721–4732. https://doi.org/10.1167/iovs.16-19242 (2016). · DOI
  26. Liu, P. et al. Long-lived metabolic enzymes in the crystalline lens identified by pulse-labeling of mice and mass spectrometry. Elife 8, e50170. https://doi.org/10.7554/elife.50170 (2019). · DOI
  27. Peters, J. M., Franke, W. W. & Kleinschmidt, J. A. Distinct 19 S and 20 S subcomplexes of the 26 S proteasome and their distribution in the nucleus and the cytoplasm. J. Biol. Chem. 269, 7709–7718 (1994). · DOI
  28. Hernebring, M., Adelöf, J., Wiseman, J., Petersen, A. & Zetterberg, M. H2O2-induced cataract as a model of age-related cataract: Lessons learned from overexpressing the proteasome activator PA28αβ in mouse eye lens. Exp. Eye Res. 203, 108395. https://doi.org/10.1016/j.exer.2020.108395 (2021). · DOI
  29. Zetterberg, M., Petersen, A., Sjöstrand, J. & Karlsson, J. Proteasome activity in human lens nuclei and correlation with age, gender and severity of cataract. Curr. Eye Res. 27, 45–53. https://doi.org/10.1076/ceyr.27.2.45.15457 (2003). · DOI
  30. Zhang, T. et al. [Comparison of proteasome activity in the epithelium of human age-related cataract and normal lens] (Chinese). Yan Ke Xue Bao 22, 89–91 (2006).
  31. Rowan, S., Bejarano, E. & Taylor, A. Mechanistic targeting of advanced glycation end-products in age-related diseases. Biochim. Biophys. Acta Mol. Basis Dis. 1864, 3631–3643. https://doi.org/10.1016/j.bbadis.2018.08.036 (2018). · DOI
  32. Nahomi, R. B., Oya-Ito, T. & Nagaraj, R. H. The combined effect of acetylation and glycation on the chaperone and anti-apoptotic functions of human α-crystallin. Biochim. Biophys. Acta 1832, 195–203. https://doi.org/10.1016/j.bbadis.2012.08.015 (2013). · DOI
  33. Raghavan, C. T. et al. AGEs in human lens capsule promote the TGFβ2-mediated EMT of lens epithelial cells: implications for age-associated fibrosis. Aging Cell 15, 465–476. https://doi.org/10.1111/acel.12450 (2016). · DOI
  34. Shigemitsu, T. et al. Immunocytochemical features of lens after cataract tissue: Signalling molecules (growth factors, cytokines, other signalling molecules), cytoskeleton proteins, cellular and extracellular matrix proteins. Int. Ophthalmol. 23, 137–144. https://doi.org/10.1023/a:1010640118852 (1999). · DOI
  35. Wederell, E. D. & de Iongh, R. U. Extracellular matrix and integrin signaling in lens development and cataract. Semin. Cell Dev. Biol. 17, 759–776. https://doi.org/10.1016/j.semcdb.2006.10.006 (2006). · DOI
  36. Walker, J. & Menko, A. S. Integrins in lens development and disease. Exp. Eye Res. 88, 216–225. https://doi.org/10.1016/j.exer.2008.06.020 (2009). · DOI
  37. Petricoin, E. F. & Liotta, L. A. SELDI-TOF-based serum proteomic pattern diagnostics for early detection of cancer. Curr. Opin. Biotechnol. 15, 24–30. https://doi.org/10.1016/j.copbio.2004.01.005 (2004). · DOI
  38. Ray, S. et al. Proteomic technologies for the identification of disease biomarkers in serum: Advances and challenges ahead. Proteomics 11, 2139–2161. https://doi.org/10.1002/pmic.201000460 (2011). · DOI

Metadata

Authors
You, Y., Bai, C., Wang, W., Zhan, T., Hu, X., Hao, F., Xia, M., Liu, Y., Ma, T., Liu, Y., Zheng, C., Pu, T., Zhang, Y., Lu, Y., Ding, N., Li, J., Yin, Y., Chen, Y., Wang, L., Zhou, J., Niu, L., Xiu, Y., Lu, Y., Jia, T., Liu, X., & Zhang, C.
Affiliations
Beijing Planetarium (CN)
Corresponding author
  • You, Yuyan
  • Liu, Yan
  • Liu, Yanhui
  • Lu, Yanping
  • Lu, Yan
  • Jia, Ting
  • Liu, Xuefeng
  • Zhang, Chenglin
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2023-08-05
Volume
13
Issue
1
Pages
12722-12722
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/s41598-023-40003-0
PMC
PMC10404263
OpenAlex
W4385606475
Cited by
1
References
3
Citations by year
2023: 1
FWCI
0.09
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
National Natural Science Foundation of China (NSFC 31872257)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connexins and lens biology
  • Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
Keywords
giant panda, senile cataract, lens proteins, proteasome, proteolysis, extracellular matrix, cytoskeleton, oxidative damage, protein aggregates, biomarkers, captive animals
MeSH terms
Animals, Ursidae, Cataract, Quality of Life, Proteomics

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