Function of mitochondrial cytochrome c oxidase is enhanced in human lens epithelial cells at high temperatures

Takeda,Shun; Yamamoto,Naoki; Nagai,Noriaki; Hiramatsu,Noriko; Deguchi,Saori; Hatsusaka,Natsuko; Kubo,Eri; Sasaki,Hiroshi

doi:10.3892/mmr.2022.12906

Function of mitochondrial cytochrome c oxidase is enhanced in human lens epithelial cells at high temperatures

Authors:
- Shun Takeda
- Naoki Yamamoto
- Noriaki Nagai
- Noriko Hiramatsu
- Saori Deguchi
- Natsuko Hatsusaka
- Eri Kubo
- Hiroshi Sasaki
View Affiliations

Affiliations: Division for Vision Research, Kanazawa Medical University Graduate School of Medical Science, Kahoku, Ishikawa 920-0293, Japan, Department of Ophthalmology, Kanazawa Medical University, Kahoku, Ishikawa 920-0293, Japan, Faculty of Pharmacy, Kindai University, Higashi-Osaka, Osaka 577-8502, Japan, Support Office for Bioresource Research, Research Promotion Headquarters, Fujita Health University, Toyoake, Aichi 470-1192, Japan
Published online on: December 2, 2022 https://doi.org/10.3892/mmr.2022.12906
Article Number: 19
Copyright : © Takeda et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY 4.0].

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Enhancement of density via human lens epithelium (HLE) cell proliferation is the underlying cause of nuclear cataracts. Moreover, our previous epidemiological study demonstrated that the risk of nuclear cataract development is significantly higher under elevated environmental temperatures compared with under lower temperatures. The present study investigated the relationship between temperature and cell proliferation in terms of mitochondrial function, which is a nuclear cataract‑inducing risk factor, using two different HLE cell lines, SRA01/04 and immortalized human lens epithelial cells NY2 (iHLEC‑NY2). Cell proliferation was significantly enhanced under the high‑temperature condition (37.5˚C) in both cell lines. The cell growth levels of SRA01/04 and iHLEC‑NY2 cells cultured at 37.5˚C were 1.20‑ and 1.16‑fold those in the low‑temperature cultures (35.0˚C), respectively. Moreover, the levels of cytochrome c oxidase mRNA (mitochondrial genome, cytochrome c oxidase‑1‑3) and its activity in SRA01/04 and iHLEC‑NY2 cells cultured at 37.5˚C were higher compared with those in cells cultured at 35.0˚C. In addition, adenosine‑5'‑triphosphate (ATP) levels in SRA01/04 and iHLEC‑NY2 cells were also significantly higher at 37.5˚C compared with those at 35.0˚C. By contrast, no significant differences in Na⁺/K⁺‑ATPase or Ca²⁺‑ATPase activities were observed between HLE cells cultured at 35.0 and 37.5˚C. These results suggested that expression of the mitochondrial genome was enhanced in high‑temperature culture, resulting in a sufficient ATP content and cell proliferation for lens opacity. Therefore, elevated environmental temperatures may increase the risk of nuclear cataracts caused by HLE cell proliferation via mitochondrial activation.

View Figures

View References

1	World Health Organization (WHO), . Vision 2020: The RIGHT TO SIGHT. Global initiative for the elimination of avoidable blindness. https://www.who.int/blindness/Vision2020_report.pdfWHO; Geneva, Switzerland: December 1–2021
2	Moreau KL and King JA: Protein misfolding and aggregation in cataract disease and prospects for prevention. Trends Mol Med. 18:273–282. 2012. View Article : Google Scholar : PubMed/NCBI
3	Shenoy AM, Kothadia AD, Shabaraya AR, Rajan MS, Viradia UM and Patel NH: Evaluation of cataract preventive action of phycocyanin. Int J Pharm Sci Drug Res. 3:42–44. 2011.
4	GBD 2019 Blindness and Vision Impairment Collaborators and Vision Loss Expert Group of the Global Burden of Disease: Study, . Causes of blindness and vision impairment in 2020 and trends over 30 years, and prevalence of avoidable blindness in relation to VISION 2020: The right to sight: An analysis for the global burden of disease study. Lancet Glob Health. 9:e144–e160. 2021. View Article : Google Scholar : PubMed/NCBI
5	Vashist P, Talwar B, Gogoi M, Maraini G, Camparini M, Ravindran RD, Murthy GV, Fitzpatrick KE, John N, Chakravarthy U, et al: Prevalence of cataract in an older population in India: the India study of age-related eye disease. Ophthalmology. 118:272–278. e271–272. 2011. View Article : Google Scholar : PubMed/NCBI
6	Klein BE, Klein R and Lee KE: Incidence of age-related cataract over a 10-year interval: The Beaver dam eye study. Ophthalmology. 109:2052–2057. 2002. View Article : Google Scholar : PubMed/NCBI
7	Lee J, Kim MJ and Tchah H: Higher-order aberrations induced by nuclear cataract. J Cataract Refract Surg. 34:2104–2109. 2008. View Article : Google Scholar : PubMed/NCBI
8	Miranda MN: The geographic factor in the onset of presbyopia. Trans Am Ophthalmol Soc. 77:603–621. 1979.PubMed/NCBI
9	Sasaki K, Sasaki H, Jonasson F, Kojima M and Cheng HM: Racial differences of lens transparency properties with aging and prevalence of age-related cataract applying a WHO classification system. Ophthalmic Res. 36:332–340. 2004. View Article : Google Scholar : PubMed/NCBI
10	Miyashita H, Hatsusaka N, Shibuya E, Mita N, Yamazaki M, Shibata T, Ishida H, Ukai Y, Kubo E and Sasaki H: Association between ultraviolet radiation exposure dose and cataract in Han people living in China and Taiwan: A cross-sectional study. PLoS One. 14:e02153382019. View Article : Google Scholar : PubMed/NCBI
11	Kodera S, Hirata A, Miura F, Rashed EA, Hatsusaka N, Yamamoto N, Kubo E and Sasaki H: Model-based approach for analyzing prevalence of nuclear cataracts in elderly residents. Comput Biol Med. 126:1040092020. View Article : Google Scholar : PubMed/NCBI
12	Ayaki M, Ohde H and Yokoyama N: Size of the lens nucleus separated by hydrodissection. Ophthalmic Surg. 24:492–493. 1993.PubMed/NCBI
13	Liu X, Liu Y, Zheng J, Huang Q and Zheng H: Lens epithelial cell proliferation and cell density in human age-related cataract. Yan Ke Xue Bao. 16:184–188. 2000.PubMed/NCBI
14	Yan XJ, Yu X, Wang XP, Jiang JF, Yuan ZY, Lu X, Lei F and Xing DM: Mitochondria play an important role in the cell proliferation suppressing activity of berberine. Sci Rep. 7:417122017. View Article : Google Scholar : PubMed/NCBI
15	Sun N, Youle RJ and Finkel T: The mitochondrial basis of aging. Mol Cell. 61:654–666. 2016. View Article : Google Scholar : PubMed/NCBI
16	Kauppila TES, Kauppila JHK and Larsson NG: Mammalian mitochondria and aging: An update. Cell Metab. 25:57–71. 2017. View Article : Google Scholar : PubMed/NCBI
17	Sebastian D, Palacin M and Zorzano A: Mitochondrial dynamics: Coupling mitochondrial fitness with healthy aging. Trends Mol Med. 23:201–215. 2017. View Article : Google Scholar : PubMed/NCBI
18	Lenka N, Vijayasarathy C, Mullick J and Avadhani NG: Structural organization and transcription regulation of nuclear genes encoding the mammalian cytochrome c oxidase complex. Prog Nucleic Acid Res Mol Biol. 61:309–344. 1998. View Article : Google Scholar : PubMed/NCBI
19	Liang HL, Ongwijitwat S and Wong-Riley MT: Bigenomic functional regulation of all 13 cytochrome c oxidase subunit transcripts in rat neurons in vitro and in vivo. Neuroscience. 140:177–190. 2006. View Article : Google Scholar : PubMed/NCBI
20	Nagai N, Mano Y, Otake H, Shibata T, Kubo E and Sasaki H: Changes in mitochondrial cytochrome c oxidase mRNA levels with cataract severity in lens epithelia of Japanese patients. Mol Med Rep. 19:5464–5472. 2019.PubMed/NCBI
21	Ibaraki N, Chen SC, Lin LR, Okamoto H, Pipas JM and Reddy VN: Human lens epithelial cell line. Exp Eye Res. 67:577–585. 1998. View Article : Google Scholar : PubMed/NCBI
22	Yamamoto N, Takeda S, Hatsusaka N, Hiramatsu N, Nagai N, Deguchi S, Nakazawa Y, Takata T, Kodera S, Hirata A, et al: Effect of a lens protein in low-temperature culture of novel immortalized human lens epithelial cells (iHLEC-NY2). Cells. 9:26702020. View Article : Google Scholar : PubMed/NCBI
23	Sasaki H, Jonasson F, Shui YB, Kojima M, Ono M, Katoh N, Cheng HM, Takahashi N and Sasaki K: High prevalence of nuclear cataract in the population of tropical and subtropical areas. Dev Ophthalmol. 35:60–69. 2002. View Article : Google Scholar : PubMed/NCBI
24	Nagai N and Ito Y: Dysfunction in cytochrome c oxidase caused by excessive nitric oxide in human lens epithelial cells stimulated with interferon-gamma and lipopolysaccharide. Curr Eye Res. 37:889–897. 2012. View Article : Google Scholar : PubMed/NCBI
25	Nagai N and Ito Y: Adverse effects of excessive nitric oxide on cytochrome c oxidase in lenses of hereditary cataract UPL rats. Toxicology. 242:7–15. 2007. View Article : Google Scholar : PubMed/NCBI
26	Nagai N, Liu Y, Fukuhata T and Ito Y: Inhibitors of inducible nitric oxide synthase prevent damage to human lens epithelial cells induced by interferon-gamma and lipopolysaccharide. Biol Pharm Bull. 29:2077–2081. 2006. View Article : Google Scholar : PubMed/NCBI
27	IPCC (Intergovernmental Panel on Climate Change): Summary for policymakers, . Climate Change 2013: The Physical Science Basis, Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V and Midgley PM: Cambridge University Press; Cambridge, UK: 2013
28	Nagaoka T, Watanabe S, Sakurai K, Kunieda E, Watanabe S, Taki M and Yamanaka Y: Development of realistic high-resolution whole-body voxel models of Japanese adult males and females of average height and weight, and application of models to radio-frequency electromagnetic-field dosimetry. Phys Med Biol. 49:1–15. 2004. View Article : Google Scholar : PubMed/NCBI
29	Walters EA, Brown JL, Krisher R, Voelkel S and Swain JE: Impact of a controlled culture temperature gradient on mouse embryo development and morphokinetics. Reprod Biomed Online. 40:494–499. 2020. View Article : Google Scholar : PubMed/NCBI
30	Yamamoto N, Kato Y, Sato A, Hiramatsu N, Yamashita H, Ohkuma M, Miyachi EI, Horiguchi M, Hirano K and Kojima H: Establishment of a new immortalized human corneal epithelial cell line (iHCE-NY1) for use in evaluating eye irritancy by in vitro test methods. In Vitro Cell Dev Biol Anim. 52:742–748. 2016. View Article : Google Scholar : PubMed/NCBI
31	Hiramatsu N, Nagai N, Kondo M, Imaizumi K, Sasaki H and Yamamoto N: Morphological comparison between three-dimensional structure of immortalized human lens epithelial cells and Soemmering's ring. Med Mol Morphol. 54:216–226. 2021. View Article : Google Scholar : PubMed/NCBI
32	Kadenbach B, Jarausch J, Hartmann R and Merle P: Separation of mammalian cytochrome c oxidase into 13 polypeptides by a sodium dodecyl sulfate-gel electrophoretic procedure. Anal Biochem. 129:517–521. 1983. View Article : Google Scholar : PubMed/NCBI
33	Kuhn-Nentwig L and Kadenbach B: Isolation and properties of cytochrome c oxidase from rat liver and quantification of immunological differences between isozymes from various rat tissues with subunit-specific antisera. Eur J Biochem. 149:147–158. 1985. View Article : Google Scholar : PubMed/NCBI
34	Afkhami E, Hheidari MM, Khatami M, Ghadamyari F and Dianatpour S: Detection of novel mitochondrial mutations in cytochrome c oxidase subunit 1 (COX1) in patients with familial adenomatous polyposis (FAP). Clin Transl Oncol. 22:908–918. 2020. View Article : Google Scholar : PubMed/NCBI
35	Wangpermtam P, Petmitr S, Punyarit P, Klongnoi B and Sanguansin S: Down-regulation of mitochondrial NADH and cytochrome b gene associated with high tumor stages in head and neck squamous cell carcinoma. Arch Oral Biol. 99:107–112. 2019. View Article : Google Scholar : PubMed/NCBI
36	Nakazawa Y, Donaldson PJ and Petrova RS: Verification and spatial mapping of TRPV1 and TRPV4 expression in the embryonic and adult mouse lens. Exp Eye Res. 186:1077072019. View Article : Google Scholar : PubMed/NCBI
37	McMillan SN and Scarff CA: Cryo-electron microscopy analysis of myosin at work and at rest. Curr Opin Struct Biol. 75:1023912022. View Article : Google Scholar : PubMed/NCBI
38	Maeshima K, Matsuda T, Shindo Y, Imamura H, Tamura S, Imai R, Kawakami S, Nagashima R, Soga T, Noji H, et al: A transient rise in free Mg²⁺ ions released from ATP-Mg hydrolysis contributes to mitotic chromosome condensation. Curr Biol. 28:444–451. 2018. View Article : Google Scholar : PubMed/NCBI
39	Yoshitomi Y, Osada H, Satake H, Kojima M, Saito-Takatsuji H, Ikeda T, Yoshitake Y, Ishigaki Y, Kubo E, Sasaki H and Yonekura H: Ultraviolet B-induced Otx2 expression in lens epithelial cells promotes epithelial-mesenchymal transition. Biol Open. 18:bio0356912019. View Article : Google Scholar
40	Thompson KV and Holliday R: Effect of temperature on the longevity of human fibroblasts in culture. Exp Cell Res. 80:354–360. 1973. View Article : Google Scholar : PubMed/NCBI