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UVB irradiation-induced dysregulation of plasma membrane calcium ATPase1 and intracellular calcium homeostasis in human lens epithelial cells

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Abstract

Ultraviolet B (UVB) could lead to the apoptosis of human lens epithelial cell and be hypothesized to be one of the important factors of cataractogenesis. In the human lens, Ca2+-ATPase is a major determinant of calcium homeostasis. Plasma membrane calcium ATPase1 (PMCA1) is a putative “housekeeping” isoform and is widely expressed in all tissues and cells, which plays an important role in calcium homeostasis. However, the effects of UVB-irradiation on the expression of PMCA1 and the cellular calcium homeostasis are still unclear. In the present study, we cultured human lens epithelial cells (HLE B-3) in vitro and investigated the effects of UVB irradiation on the expression of PMCA1 and the intracellular calcium homeostasis using real-time cell electronic sensing system, flow cytometry, fluo-3/AM probes, real-time quantitative PCR, and enzyme-linked immunosorbent assay techniques. We found that UVB irradiation could induce human lens epithelial cell death, cause intracellular calcium ion (Ca2+) elevation, inhibit Ca2+-ATPase activity and decrease the expression of PMCA1 at gene and protein levels, suggesting that the downregulation of PMCA1 and the disruption of calcium homeostasis may play important roles in UVB-induced HLE B-3 cell apoptosis.

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References

  1. Ayala MN, Michael R, Söderberg PG (2000) Influence of exposure time for UV radiation-induced cataract. Invest Ophthalmol Vis Sci 41:3539–3543

    PubMed  CAS  Google Scholar 

  2. Balasubramanian D (2000) Ultraviolet radiation and cataract. J Ocul Pharmacol Ther 16:285–297

    Article  PubMed  CAS  Google Scholar 

  3. Andley UP, Walsh A, Kochevar IE, Reddan JR (1990) Effect of ultraviolet-B radiation on protein synthesis in cultured lens epithelial cells. Curr Eye Res 9:1099–1106

    Article  PubMed  CAS  Google Scholar 

  4. Andley UP, Malone JP, Townsend RR (2011) Inhibition of lens photodamage by UV-absorbing contact lenses. Invest Ophthalmol Vis Sci 52:8330–8341

    Article  PubMed  CAS  Google Scholar 

  5. Lee DH, Cho KS, Park SG, Kim EK, Joo CK (2005) Cellular death mediated by nuclear factor kappa B (NF-kappaB) translocation in cultured human lens epithelial cells after ultraviolet-B irradiation. J Cataract Refract Surg 31:614–619

    Article  PubMed  Google Scholar 

  6. Yao J, Liu Y, Wang X, Shen Y, Yuan S, Wan Y, Jiang Q (2009) UVB radiation induces human lens epithelial cell migration via NADPH oxidase-mediated generation of reactive oxygen species and up-regulation of matrix metalloproteinases. Int J Mol Med 24:153–159

    PubMed  CAS  Google Scholar 

  7. Li WC, Spector A (1996) Lens epithelial cell apoptosis is an early event in the development of UVB-induced cataract. Free Radic Biol Med 20:301–311

    Article  PubMed  CAS  Google Scholar 

  8. Li WC, Kuszak JR, Dunn K, Wang RR, Ma W, Wang GM, Spector A, Leib M, Cotliar AM, Weiss M et al (1995) Lens epithelial cell apoptosis appears to be a common cellular basis for non-congenital cataract development in humans and animals. J Cell Biol 130:169–181

    Article  PubMed  CAS  Google Scholar 

  9. Jing L, Kumari S, Mendelev N, Li PA (2011) Coenzyme q10 ameliorates ultraviolet B irradiation induced cell death through inhibition of mitochondrial intrinsic cell death pathway. Int J Mol Sci 12:8302–8315

    Article  PubMed  CAS  Google Scholar 

  10. Mendelev N, Witherspoon S, Li PA (2009) Overexpression of human selenoprotein H in neuronal cells ameliorates ultraviolet irradiation-induced damage by modulating cell signaling pathways. Exp Neurol 220:328–334

    Article  PubMed  CAS  Google Scholar 

  11. Ricci JE, Gottlieb RA, Green DR (2003) Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J Cell Biol 160:65–75

    Article  PubMed  CAS  Google Scholar 

  12. Duncan G, Bushell AR (1975) Ion analyses of human cataractous lenses. Exp Eye Res 20:223–230

    Article  PubMed  CAS  Google Scholar 

  13. Rasi V, Costantini S, Moramrco A, Giordano R, Giustolisi R, Balacco Gabrieli C (1992) Inorganic element concentrations in cataract human lens. Ann Ophthalmol 24:459–464

    PubMed  CAS  Google Scholar 

  14. Hightower KR, Duncan G, Dawson A, Wormstone IM, Reddan J, Dziedizc D (1999) Ultraviolet irradiation (UVB) interrupts calcium cell signaling in lens epithelial cells. Photochem Photobiol 69:595–598

    PubMed  CAS  Google Scholar 

  15. Marian MJ, Li H, Borchman D, Paterson CA (2005) Plasma membrane Ca2+-ATPase expression in the human lens. Exp Eye Res 81:57–64

    Article  PubMed  CAS  Google Scholar 

  16. Brini M (2009) Plasma membrane Ca2+-ATPase: from a housekeeping function to a versatile signaling role. Pflugers Arch 457:657–664

    Article  PubMed  CAS  Google Scholar 

  17. Bian L, Zeng J, Borchman D, Paterson CA (2000) Plasma membrane calcium ATPase gene expression in bovine lens epithelium. Ophthalmic Res 32:100–105

    Article  PubMed  CAS  Google Scholar 

  18. Marian MJ, Mukhopadhyay P, Borchman D, Tang D, Paterson CA (2007) Regulation of sarco/endoplasmic and plasma membrane calcium ATPase gene expression by calcium in cultured human lens epithelial cells. Cell Calcium 41:87–95

    Article  PubMed  CAS  Google Scholar 

  19. Paterson CA, Zeng J, Husseini Z, Borchman D, Delamere NA, Garland D, Jimenez-Asensio J (1997) Calcium ATPase activity and membrane structure in clear and cataractous human lenses. Curr Eye Res 16:333–338

    Article  PubMed  CAS  Google Scholar 

  20. Marian MJ, Mukhopadhyay P, Borchman D, Tang D, Paterson CA (2008) The effect of hydrogen peroxide on sarco/endoplasmic and plasma membrane calcium ATPase gene expression in cultured human lens epithelial cells. Open Ophthalmol J 2:123–129

    Article  PubMed  Google Scholar 

  21. Guo D, Wu C, Li J, Guo A, Li Q, Jiang H, Chen B, Wang X (2009) Synergistic effect of functionalized nickel nanoparticles and quercetin on inhibition of the SMMC-7721 cells proliferation. Nanoscale Res Lett 4:1395–1402

    Article  PubMed  CAS  Google Scholar 

  22. Andley UP, Lewis RM, Reddan JR, Kochevar IE (1994) Action spectrum for cytotoxicity in the UVA- and UVB-wavelength region in cultured lens epithelial cells. Invest Ophthalmol Vis Sci 35:367–373

    PubMed  CAS  Google Scholar 

  23. Andley UP, Weber JG (1995) Ultraviolet action spectra for photobiological effects in cultured human lens epithelial cells. Photochem Photobiol 62:840–846

    Article  PubMed  CAS  Google Scholar 

  24. McNulty R, Wang H, Mathias RT, Ortwerth BJ, Truscott RJ, Bassnett S (2004) Regulation of tissue oxygen levels in the mammalian lens. J Physiol 559:883–898

    Article  PubMed  CAS  Google Scholar 

  25. Paz ML, Gonzalez Maglio DH, Weill FS, Bustamante J, Leoni J (2008) Mitochondrial dysfunction and cellular stress progression after ultraviolet B irradiation in human keratinocytes. Photodermatol Photoimmunol Photomed 24:115–122

    Article  PubMed  CAS  Google Scholar 

  26. Huang L, Yappert MC, Jumblatt MM, Borchman D (2008) Hyperoxia and thyroxine treatment and the relationships between reactive oxygen species generation, mitochondrial membrane potential, and cardiolipin in human lens epithelial cell cultures. Curr Eye Res 33:575–586

    Article  PubMed  CAS  Google Scholar 

  27. Godar DE, Lucas AD (1995) Spectral dependence of UV-induced immediate and delayed apoptosis: the role of membrane and DNA damage. Photochem Photobiol 62:108–113

    Article  PubMed  CAS  Google Scholar 

  28. Long AC, Colitz CM, Bomser JA (2004) Apoptotic and necrotic mechanisms of stress-induced human lens epithelial cell death. Exp Biol Med (Maywood) 229:1072–1080

    CAS  Google Scholar 

  29. Hightower K, McCready J (1993) Comparative effect of UVA and UVB on cultured rabbit lens. Photochem Photobiol 58:827–830

    Article  PubMed  CAS  Google Scholar 

  30. Williams MR, Duncan G, Riach RA, Webb SF (1993) Acetylcholine receptors are coupled to mobilization of intracellular calcium in cultured human lens cells. Exp Eye Res 57:381–384

    Article  PubMed  CAS  Google Scholar 

  31. Riach RA, Duncan G, Williams MR, Webb SF (1995) Histamine and ATP mobilize calcium by activation of H1 and P2u receptors in human lens epithelial cells. J Physiol 486:273–282

    PubMed  CAS  Google Scholar 

  32. Ding BX, Wang CB (2003) Inhibitory effect of polypeptides from Chlamys farreri on UVB-induced apoptosis and DNA damage in normal human dermal fibroblasts in vitro. Acta Pharmacol Sin 24:1006–1010

    PubMed  CAS  Google Scholar 

  33. Masaki H, Izutsu Y, Yahagi S, Okano Y (2009) Reactive oxygen species in HaCaT keratinocytes after UVB irradiation are triggered by intracellular Ca(2 +) levels. J Investig Dermatol Symp Proc 14:50–52

    Article  PubMed  CAS  Google Scholar 

  34. Ribeiro CM, Paradiso AM, Livraghi A, Boucher RC (2003) The mitochondrial barriers segregate agonist-induced calcium-dependent functions in human airway epithelia. J Gen Physiol 122:377–387

    Article  PubMed  CAS  Google Scholar 

  35. Spät A, Szanda G, Csordás G, Hajnóczky G (2008) High- and low-calcium dependent mechanisms of mitochondrial calcium signalling. Cell Calcium 44:51–63

    Article  PubMed  Google Scholar 

  36. Duncan G, Webb SF, Dawson AP, Bootman MD, Elliott AJ (1993) Calcium regulation in tissue-cultured human and bovine lens epithelial cells. Invest Ophthalmol Vis Sci 34:2835–2842

    PubMed  CAS  Google Scholar 

  37. Chiesa R, Sredy J, Spector A (1985) Phosphorylated intermediates of two Ca2+-ATPases in membrane preparations from lens epithelial cells. Curr Eye Res 4:897–903

    Article  PubMed  CAS  Google Scholar 

  38. Tang D, Dean WL, Borchman D, Paterson CA (2006) The influence of membrane lipid structure on plasma membrane Ca2+-ATPase activity. Cell Calcium 39:209–216

    Article  PubMed  CAS  Google Scholar 

  39. Yang H, Cui DM, Zeng JW (2011) Plasma membrane calcium ATPase expression in human lens epithelium cell lines. Yan Ke Xue Bao 26:35–43

    PubMed  CAS  Google Scholar 

  40. Marian MJ, Mukhopadhyay P, Borchman D, Paterson CA (2008) Plasma membrane Ca-ATPase isoform expression in human cataractous lenses compared to age-matched clear lenses. Ophthalmic Res 40:86–93

    Article  PubMed  CAS  Google Scholar 

  41. Bi HS, Liu DM, Wang XR, Cai WT, Zhang JH, Ma XH (2006) Expression of Ca2+-ATPase gene in clear and cataractous lens epithelium. Rec Adv Ophthalmol 26:25–28

    CAS  Google Scholar 

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Acknowledgments

This work was supported by the Natural Science Foundation of Shandong province (ZR2010HM032).

Conflict of interest

The authors declare that they have no competing interests.

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Authors and Affiliations

  1. Shandong University of Traditional Chinese Medicine, Jinan, 250002, China

    Qiuxin Wu, Daoguang Wang & Yuxiang Du

  2. Key Laboratory of Integrated Traditional Chinese and Western Medicine for Prevention and Therapy of Ocular Diseases in Universities of Shandong, Eye Institute of Shandong University of Traditional Chinese Medicine, Jinan, 250002, China

    Dadong Guo & Hongsheng Bi

  3. Key Laboratory of Integrated Traditional Chinese and Western Medicine for Prevention and Therapy of Ocular Diseases of Shandong Province, Eye Institute of Shandong University of Traditional Chinese Medicine, Jinan, 250002, China

    Dadong Guo & Hongsheng Bi

  4. Affiliated Eye Hospital of Shandong University of Traditional Chinese Medicine, Jinan, 250002, China

    Hongsheng Bi

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  1. Qiuxin Wu
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  2. Dadong Guo
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  3. Hongsheng Bi
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Correspondence to Hongsheng Bi.

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Wu, Q., Guo, D., Bi, H. et al. UVB irradiation-induced dysregulation of plasma membrane calcium ATPase1 and intracellular calcium homeostasis in human lens epithelial cells. Mol Cell Biochem 382, 263–272 (2013). https://doi.org/10.1007/s11010-013-1743-2

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  • DOI: https://doi.org/10.1007/s11010-013-1743-2

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