[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.5483/BMBRep.2013.46.2.272

Transduced PEP-1-FK506BP ameliorates corneal injury in Botulinum toxin A-induced dry eye mouse model

Kim, Dae Won (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University)
Lee, Sung Ho (R&D Center, Lumieye Genetics Co., Ltd.)
Ku, Sae Kwang (Department of Anatomy and Histology, College of Korean Medicine, Daegu Haany University)
Cho, Soo Hyun (Department of Anatomy and Histology, College of Korean Medicine, Daegu Haany University)
Cho, Sung-Woo (Department of Biochemistry and Molecular Biology, University of Ulsan College of Medicine)
Yoon, Ga Hyeon (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University)
Hwang, Hyun Sook (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University)
Park, Jinseu (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University)
Eum, Won Sik (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University)
Kwon, Oh-Shin (School of Life Sciences and Biotechnology, College of Natural Sciences, Kyungpook National University)
Choi, Soo Young (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University)

Publication Information

BMB Reports / v.46, no.2, 2013 , pp. 124-129 More about this Journal

Abstract

FK506 binding protein 12 (FK506BP) belongs to a family of immunophilins, and is involved in multiple biological processes. However, the function of FK506BP in corneal disease remains unclear. In this study, we examined the protective effects on dry eye disease in a Botulinum toxin A (BTX-A) induced mouse model, using a cell-permeable PEP-1-FK506BP protein. PEP-1-FK506BP efficiently transduced into human corneal epithelial cells in a time- and dose-dependent manner, and remained stable in the cells for 48 h. In addition, we demonstrated that topical application of PEP-1-FK506BP was transduced into mouse cornea and conjunctiva by immunohistochemistry. Furthermore, topical application of PEP-1-FK506BP to BTX-A-induced mouse model markedly inhibited expression levels of pro-inflammatory cytokines such as interleukin- $1{\beta}$ (IL- $1{\beta}$ ), tumor necrosis factor- ${\alpha}$ (TNF- ${\alpha}$ ) and macrophage inhibitory factor (MIF) in corneal and conjunctival epithelium. These results suggest PEP-1-FK506BP as a potential therapeutic agent for dry eye diseases.

Keywords

Cytokines; Dry eye disease; Inflammation; PEP-1-FK506BP; Protein therapy;

Citations & Related Records

Times Cited By KSCI : 2 (Citation Analysis)

Reference
Cited By KSCI

1	Stern, M. E. and Pflugfelder, S. C. (2004) Inflammation in dry eye. Ocul. Surf. 2, 124-130. DOI ScienceOn
2	Lee, S. H., Kim, D. W., Eom, S. A., Jun, S. Y., Park, M., Kim, D. S., Kwon, H. J., Kwon, H. Y., Han, K. H., Park, J., Hwang, H. S., Eum, W. S. and Choi, S. Y. (2012) Suppression of 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced skin inflammation in mice by transduced Tat-Annexin protein. BMB Rep. 45, 354-359. 과학기술학회마을 DOI ScienceOn
3	Kubo, E., Fatma, N., Akagi, Y., Beier, D. R., Singh, S. P. and Singh, D. P. (2008) TAT-mediated PRDX6 protein transduction protects against eye lens epithelial cell death and delays lens opacity. Am. J. Physiol. Cell Physiol. 294, C842-C855. DOI ScienceOn
4	Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254. DOI ScienceOn
5	Suwan-apichon, O., Rizen, M., Rangsin, R., Herretes, S., Reyes, J. M., Lekhanont, K. and Chuck, R. S. (2006) Botulium toxin B-induced mouse model of keratoconjunctivitis sicca. Invest. Ophthalmol. Vis. Sci. 47, 133-139. DOI ScienceOn
6	Lekhanont, K., Ilya, L., Suwan-apichon, O., Rangsin, R. and Chuck, R. S. (2007) Comparison of topical dry eye medications for the treatment of keratoconjunctivitis sicca in a botulium toxin B-induced mouse model. Cornea 26, 84-89. DOI ScienceOn
7	Wang, H., Zhong, C. Y., Wu, J. F., Huang, Y. B. and Liu, C. B. (2010) Enhancement of TAT cell membrane penetration efficiency by dimethyl sulphoxide. J. Con. Rel. 143, 64-70. DOI ScienceOn
8	Liu, X., Lin, Z., Zhou, T., Zong, R., He, H., Liu, Z., Ma, J. X., Liu, Z. and Zhou, Y. (2011) Anti-angiogenic and anti-inflammatory effects of SERPINA3K on corneal injury. PLoS ONE 6, e16712. DOI ScienceOn
9	Zhu, L., Shen, J., Zhang, C., Park, C. Y., Kohanim, S., Yew, M., Parker, J. S. and Chuck, R. S. (2009) Inflammatory cytokine expression on the ocular surface in the Botulium toxin B induced murine dry eye model. Mol. Vis. 15, 250-258.
10	Jiang, W., Cazacu, S., Xiang, C., Zenklusen, J. C., Fine, H. A., Berens, M., Armstrong, B., Brodie, C. and Mikkelsen, T. (2008) FK506 binding protein mediates glioma cell growth and sensitivity to rapamycin treatment by regulating NF- ${\kappa}B$ signaling pathway. Neoplasis 10, 235-243. DOI
11	Kim, S. Y., Jeong, H. J., Kim, D. W., Kim, M. J., An, J. J., Sohn, E. J., Kang, H. W., Shin, M. J., Ahn, E. H., Kwon, S. W., Kim, D. S., Cho, S. W., Park, J., Eum, W. S. and Choi, S. Y. (2011) Transduced PEP-1-FK506BP inhibits the inflammatory response in the Raw 264.7 cells and mouse models. Immunobiol. 216, 771-781. DOI ScienceOn
12	Kim, S. Y., Sohn, E. J., Kim, D. W., Jeong, H. J., Kim, M. J., Kang, H. W., Shin, M. J., Ahn, E. H., Kwon, S. W., Kim, Y. N., Kwon, H. J., Kim, T. Y., Lee, K. S., Park, J., Eum, W. S. and Choi, S. Y. (2011) Transduced PEP-1-FK506BP ameliorates atopic dermatitis in NC/Nga mice. J. Invest. Dermatol. 131, 1477-1485. DOI ScienceOn
13	Dietz, G. P. (2010) Cell-penetrating peptide technology to deliver chaperones and associated factors in diseases and basic research. Curr. Pharm. Biotechol. 11, 167-174. DOI ScienceOn
14	Wadia, J. S. and Dowdy, S. F. (2002) Protein transduction technology. Curr. Opin. Biotechnol. 13, 52-56. DOI ScienceOn
15	Ahn, E. H., Kim, D. W., Kang, H. W., Shin, M. J., Won, M. H., Kim, J., Kim, D. S., Kwon, O. S., Kang, T. C., Han, K. H., Park, J., Eum, W. S. and Choi, S. Y. (2010) Transduced PEP-1-ribosomal protein S3 (rpS3) ameliorates 12-O-tetradecanoyl phorbol-13-acetate-induced inflammation in mice. Toxicol. 276, 192-197. DOI ScienceOn
16	Lim, K. S., Won, Y. W., Park, Y. S. and Kim, Y. H. (2010) Preparation and functional analysis of recombinant protein transduction domain-metallothionein fusion proteins. Biochimie 92, 964-970. DOI ScienceOn
17	Shin, M. J., Lee, Y. P., Kim, D. W., An, J. J., Jang, S. H., Cho, S. M., Sheen, S. H., Lee, H. R., Kweon, H. Y., Kang, S. W., Lee, K. G., Park, J., Eum, W. S., Cho, Y. J. and Choi, S. Y. (2010) Transduced PEP-1-AMPK inhibits LPS-induced COX-2 and iNOS expression in Raw264.7 cells. BMB Rep. 43, 40-45. DOI ScienceOn
18	Eum, W. S., Kim, D. W., Hwang, I. K., Yoo, K. Y., Kang, T. C., Jang, S. H., Choi, H. S., Choi, S. H., Kim, Y. H., Kim, S. Y., Kwon, H. Y., Kang, J. H., Kwon, O. S., Cho, S. W., Lee, K. S., Park, J., Won, M. H. and Choi, S. Y. (2004) In vivo protein transduction: Biologically active intact PEP-1-superoxide dismutase fusion protein efficiently protects against ischemic insult. Free Radic. Biol. Med. 37, 1656-1669. DOI ScienceOn
19	Kwon, S. W., Sohn, E. J., Kim, D. W., Jeong, H. J., Kim, M. J., Ahn, E. H., Kim, Y. N., Dutta, S., Kim, D. S., Park, J., Eum, W. S., Hwang, H. S. and Choi, S. Y. (2011) Anti-inflammatory effect of transduced PEP-1-heme oxygenase-1 in Raw 264.7 cells and a mouse edema model. Biochem. Biophys. Res. Commun. 411, 354-359. DOI ScienceOn
20	Schaumberg, D. A., Sullivan, D. A., Buring, J. E. and Dana, M. R. (2003) Prevalence of dry eye syndrome among US women. Am. J. Ophthalmol. 136, 318-326. DOI ScienceOn
21	Schaumberg, D. A., Sullivan, D. A. and Dana, M. R. (2002) Epidemiology of dry eye syndrome. Ade. Exp. Med. Biol. 506, 989-998. DOI
22	Behrens, A., Doyle, J. J., Stern, L., Chuck, R. S., McDonnell, P. J., Azar, D. T., Dua, H. S., Hom, M., Karpecki, P. M., Laibson, P. R., Lemp, M. A., Meisler, D. M., Del Castillo, J. M., O'Brien, T. P., Pflugfelder, S. C., Rolando, M., Schein, O. D., Seitz, B., Tseng, S. C., van Setten, G., Wilson, S. E. and Yiu, S. C. (2006) Dysfunctional tear syndrome study group. Dysfunctional tear syndrome: a Delphi approach to treatment recommendations. Cornea 25, 900-907. DOI ScienceOn
23	Schaumberg, D. A., Buring, J. E., Sullivan, D. A. and Dana, M. R. (2001) Hormone replacement therapy and dry eye syndrome. JAMA 286, 2114-2119. DOI ScienceOn
24	Gupta, H., Jain, S., Mathur, R., Mishra, P., Mishra, A. K. and Velpandian, T. (2007) Sustained ocular drug delivery from a temperature and pH triggered novel in situ gel system. Drug Deliv. 14, 507-515. DOI ScienceOn
25	Khaw, P. T., Shah, P. and Elkington, A. R. (2004) Injury to the eye. BMJ 328, 36-38. DOI ScienceOn
26	Hosseini, H. and Nejabat, M. (2007) A potential therapeutic strategy for inhibition of corneal neovascularization with new anti-VEGF agents. Med. Hypotheses 68, 799-801. DOI ScienceOn
27	Narayanan, S., Miller, W. L. and McDermott, A. M. (2006) Conjunctival cytokine expression in symptomatic moderate dry eye subjects. Invest. Ophthalmol. Vis. Sci. 47, 2445-2450. DOI ScienceOn
28	Luo, L., Li, D.Q., Doshi, A., Farley, W., Corrales, R. M. and Pflugfelder, S. C. (2004) Experimental dry eye stimulates production of inflammatory cytokines and MMP-9 and activates MAPK signaling pathways on the ocular surface. Invest. Ophthalmol. Vis. Sci. 45, 4293-4301. DOI ScienceOn
29	Dana, M. R. and Hamrah, P. (2002) Role of immunity and inflammation in corneal and ocular surface diseases associated with dry eye. Ade. Exp. Med. Biol. 506, 729-738. DOI
30	Gulati, A., Sacchetti, M., Bonini, S. and Dana, R. (2006) Chemokine receptor CCR5 expression in conjunctival epithelium of patients with dry eye syndrome. Arch. Ophthalmol. 124, 710-716. DOI ScienceOn
31	Solomon, A., Dursun, D., Liu, Z., Xie, Y., Macri A. and Pflugfelder, S. C. (2001) Pro- and anti-inflammatory forms of inerleukin-1 in the tear fluid and conjunctiva of patients with dry eye diseases. Invest. Ophthalmol. Vis. Sci. 42, 2283-2293.
32	Hongyok, T., Chae, J. J., Shin, Y. J., Na, D., Li, L. and Chuck, R. S. (2009) Effect of chitosan-N-acetylcysteine conjugate in a mouse model of Botulium toxin B-induced dry eye. Arch. Ophthalmol. 127, 525-532. DOI ScienceOn
33	Perry, H. D., Solomon, R., Donnenfeld, E. D., Perry, A. R., Wittpenn, J. R., Greenman, H. E. and Savage, H. E. (2008) Evaluation of topical cyclosporine for the treatment of dry eye diseases. Arch. Ophthalmol. 126, 1046-1050. DOI ScienceOn
34	De Paiva, C. S., Corrales, R. M. and Villarrea, A. L. (2006) Corticosteroid and doxycycline suppress MMP-9 and inflammatory cytokine expression, MAPK activation in the corneal epithelium in experimental dry eye. Exp. Eye Res. 83, 526-535. DOI ScienceOn
35	Li, N., He, J., Schwartz, C. E., Gjorstrup, P. and Bazan, H. E. (2010) Resolvin E1 improves tear production and decreases inflammation in a dry eye mouse model. J. Ocul. Pharmacol. Ther. 26, 431-439. DOI ScienceOn

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	Rahel Zulliger. (2015) Journal of Controlled Release Non-viral therapeutic approaches to ocular diseases: An overview and future directions / 219 , 471
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