Black Rice (Oryza sativa L. var. japonica) Hydrolyzed Peptides Induce Expression of Hyaluronan Synthase 2 Gene in HaCaT Keratinocytes

  • Published : 2007.02.28

Abstract

Black rice (Oryza sativa L. var. japonica) has been used in folk medicine in Asia. To understand the effects of black rice hydrolyzed peptides (BRP) from germinated black rice, we assessed the expression levels of about 20,000 transcripts in BRP-treated HaCaT keratinocytes using human 1A oligo microarray analysis. As a result, the BRP treatment showed a differential expression ratio of more than 2-fold: 745 were activated and 1,011 were repressed. One of the most interesting findings was a 2-fold increase in hyaluronan synthase 2 (HAS2) gene expression by BRP. Semiquantitative RT-PCR showed that BRP increased HAS2 mRNA in dose-dependent manners. ELISA showed that BRP effectively increased hyaluronan (HA) production in HaCaT keratinocytes.

Keywords

References

  1. Boukamp, P., R. T. Petrussevska, D. Breitkreutz, J. Hornung, A. Markham, and N. E. Fusenig. 1988. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106: 761-771 https://doi.org/10.1083/jcb.106.3.761
  2. Brinck, J. and P. Heldin. 1999. Expression of recombinant hyaluronan synthase (HAS) isoforms in CHO cells reduces cell migration and cell surface CD44. Exp. Cell Res. 252: 342-351 https://doi.org/10.1006/excr.1999.4645
  3. Brown, P. O. and D. Botetein. 1999. Exploring the new world of the genome with DNA microarrays. Nat. Genet. 21(Suppl. 1): 33-37 https://doi.org/10.1038/4462
  4. Clarke P. A., R. te Poele, R. Wooster, and R. Workman. 2001. Gene expression microarray analysis in cancer biology, pharmacology, and drug development: Progress and potential. Biochem. Pharmacol. 62: 1311-1336
  5. Dunn, L. B., M. Damesyn, A. A. Moore, D. B. Reuben, and G. A. Greendale. 1997. Does estrogen prevent skin aging? Results from the First National Health and Nutrition Examination Survey (NHANES I). Arch. Dermatol. 133: 339-342 https://doi.org/10.1001/archderm.133.3.339
  6. Feusi, E., L. Sun, A. Sibalic, B. Beck-Schimmer, B. Oertli, and R. P. Wuthrich. 1999. Enhanced hyaluronan synthesis in the MRL-Fas(lpr) kidney: Role of cytokines. Nephron 83: 66-73 https://doi.org/10.1159/000045475
  7. Fleischmajer, R., J. S. Perlish, and R. I. Bashey. 1972. Human dermal glycosaminoglycans and aging. Biochim. Biophys. Acta 279: 265-275 https://doi.org/10.1016/0304-4165(72)90142-0
  8. Fülöp, C., A. Salustri, and V. C. Hascall. 1997. Coding sequence of a hyaluronan synthase homologue expressed during expansion of the mouse cumulus-oocyte complex. Arch. Biochem. Biophys. 337: 261-266 https://doi.org/10.1006/abbi.1996.9793
  9. Ghersetich, I., T. Lotti, G. Campanile, C. Grappone, and G. Dini. 1994. Hyaluronic acid in cutaneous intrinsic aging. Int. J. Dermatol. 33: 119-122 https://doi.org/10.1111/j.1365-4362.1994.tb01540.x
  10. Heldin, P., T. C. Laurent, and C. H. Heldin. 1989. Effect of growth factors on hyaluronan synthesis in cultured human fibroblasts. Biochem. J. 258: 919-922 https://doi.org/10.1042/bj2580919
  11. Itano, N., T. Sawai, M. Yoshida, P. Lenas, Y. Yamada, M. Imagawa, T. Shinomura, M. Hamaguchi, Y. Yoshida, Y. Ohnuki, S. Miyauchi, A. P. Spicer, J. A. McDonald, and K. Kimata. 1999. Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J. Biol. Chem. 274: 25085-25092 https://doi.org/10.1074/jbc.274.35.25085
  12. Juhlin, L. 1997. Hyaluronan in skin. J. Intern. Med. 242: 61-66 https://doi.org/10.1046/j.1365-2796.1997.00175.x
  13. Kaback, L. A. and T. J. Smith. 1999. Expression of hyaluronan synthase messenger ribonucleic acids and their induction by interleukin-1$\beta$ in human orbital fibroblasts: Potential insight into the molecular pathogenesis of thyroidassociated ophthalmopathy. J. Clin. Endocrinol. Metab. 84: 4079-4084 https://doi.org/10.1210/jc.84.11.4079
  14. Kim, B. S., S. J. Kang, S. B. Lee, W. Hwang, and K. S. Kim. 2005. Simple method to correct gene-specific dye bias from partial dye swap information of a DNA microarray experiment. J. Microbiol. Biotechnol. 15: 1377-1383
  15. Kim, H. M., C. S. Kang, E. H. Lee, and T. Y. Shin. 1999. The evaluation of the antianaphylactic effect of Oryza sativa L. subsp. Hsien ting in rats. Pharmacol. Res. 40: 31-36 https://doi.org/10.1006/phrs.1998.0386
  16. Laurent, T. C. and J. R. Fraser. 1992. Hyaluronan. FASEB J. 6: 2397-2404 https://doi.org/10.1096/fasebj.6.7.1563592
  17. Lee, J. Y. and N. G. Lee. 2004. Transcriptional responses of human respiratory epithelial cells to nontypeable Haemophilus influenzae infection analyzed by high density cDNA microarray. J. Microbiol. Biotechnol. 14: 836-843
  18. Lipshutz R. J., S. P. Fodor, T. R. Gingeras, and D. J. Lockhart. 1999. High density synthetic oligonucleotide arrays. Nat. Genet. 21(Suppl. 1): 20-24 https://doi.org/10.1038/4447
  19. Longas, M. O., C. S. Russell, and X. Y. He. 1987. Evidence for structural changes in dermatan sulfate and hyaluronic acid with aging. Carbohydr. Res. 159: 127-136 https://doi.org/10.1016/S0008-6215(00)90010-7
  20. Manuskiatti, W. and H. I. Maibach. 1996. Hyaluronic acid and skin: Wound healing and aging. Int. J. Dermatol. 35: 539-544 https://doi.org/10.1111/j.1365-4362.1996.tb03650.x
  21. Mian, N. 1986. Analysis of cell-growth-phase-related variations in hyaluronate synthase activity of isolated plasma-membrane fractions of cultured human skin fibroblasts. Biochem. J. 237: 333-342 https://doi.org/10.1042/bj2370333
  22. Nishida, Y., C. B. Knudson, W. Eger, K. E. Kuettner, and W. Knudson. 2000. Osteogenic protein 1 stimulates cellsassociated matrix assembly by normal human articular chondrocytes: Up-regulation of hyaluronan synthase, CD44, and aggrecan. Arthritis Rheum. 43: 206-214 https://doi.org/10.1002/1529-0131(200001)43:1<206::AID-ANR25>3.0.CO;2-1
  23. Oh, M. K., M. J. Cha, S. G. Lee, L. Rohlin, and J. C. Liao. 2006. Dynamic gene expression profiling of Escherichia coli in carbon source transition from glucose to acetate. J. Microbiol. Biotechnol. 16: 543-549
  24. Pasonen-Seppanen, S., S. Karvinen, K. Torronen, J. M. Hyttinen, T. Jokela, M. J. Lammi, M. I. Tammi, and R. Tammi. 2003. EGF upregulates, whereas TGF-beta downregulates, the hyaluronan synthases Has2 and Has3 in organotypic keratinocyte cultures: Correlations with epidermal proliferation and differentiation. J. Invest. Dermatol. 120: 1038-1044 https://doi.org/10.1046/j.1523-1747.2003.12249.x
  25. Pienimaki, J. P., K. Rilla, C. Fulop, R. K. Sironen, S. Karvinen, S. Pasonen, M. J. Lammi, R. Tammi, V. C. Hascall, and M. I. Tammi. 2001. Epidermal growth factor activates hyaluronan synthase 2 in epidermal keratinocytes and increases pericellular and intracellular hyaluronan. J. Biol. Chem. 276: 20428-20435 https://doi.org/10.1074/jbc.M007601200
  26. Rilla, K., M. J. Lammi, R. Sironen, K. Torronen, M. Luukkonen, V. C. Hascall, R. J. Midura, M. Hyttinen, J. Pelkonen, M. Tammi, and R. Tammi. 2002. Changed lamellipodial extension, adhesion plaques and migration in epidermal keratinocytes containing constitutively expressed sense and antisense hyaluronan synthase 2 (Has2) genes. J. Cell Sci. 115: 3633-3643 https://doi.org/10.1242/jcs.00042
  27. Sampson, P. M., C. L. Rochester, B. Freundlich, and J. A. Elias. 1992. Cytokine regulation of human lung fibroblast hyaluronan (hyaluronic acid) production. Evidence for cytokine-regulated hyaluronan (hyaluronic acid) degradation and human lung fibroblast-derived hyaluronidase. J. Clin. Invest. 90: 1492-1503 https://doi.org/10.1172/JCI116017
  28. Schmidt, J. B., M. Binder, G. Demschik, C. Bieglmayer, and A. Reiner. 1996. Treatment of skin aging with topical estrogens. Int. J. Dermatol. 35: 669-674 https://doi.org/10.1111/j.1365-4362.1996.tb03701.x
  29. Sobel, H. and R. A. Cohen. 1970. Effect of estradiol on hyaluronic acid in the skin of aging mice. Steroids 16: 1-3 https://doi.org/10.1016/S0039-128X(70)80090-3
  30. Tammi, M. I., A. J. Day, and E. A. Turley. 2002. Hyaluronan and homeostasis: A balancing act. J. Biol. Chem. 277: 4581-4584 https://doi.org/10.1074/jbc.R100037200
  31. Tammi, R., J. A. Ripellino, R. U. Margolis, H. I. Maibach, and M. Tammi. 1989. Hyaluronate accumulation in human epidermis treated with retinoic acid in skin organ culture. J. Invest. Dermatol. 92: 326-332 https://doi.org/10.1111/1523-1747.ep12277125
  32. Tiedemann, K., A. Malmström, and G. Westergren-Thorsson. 1997. Cytokine regulation of proteoglycan production in fibroblasts: Separate and synergistic effects. Matrix Biol. 15: 469-478 https://doi.org/10.1016/S0945-053X(97)90020-2
  33. Tirone, E., C. D'Alessandris, V. C. Hascall, G. Siracusa, and A. Salustri. 1997. Hyaluronan synthesis by mouse cumulus cells is regulated by interactions between follicle-stimulating hormone (or epidermal growth factor) and a soluble oocyte factor (or transforming growth factor beta). J. Biol. Chem. 272: 4787-4794 https://doi.org/10.1074/jbc.272.8.4787
  34. Tusher, V. G., R. Tibshirani, and G. Chu. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98: 5116-5121
  35. Weigel, P. H., V. C. Hascall, and M. Tammi. 1997. Hyaluronan synthases. J. Biol. Chem. 272: 13997-14000 https://doi.org/10.1074/jbc.272.22.13997
  36. Yang, Y. H., S. Dudoit, P. Luu, D. M. Lin, V. Peng, J. Ngai, and T. P. Speed. 2002. Normalization for cDNA microarray data: A robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30: E15 https://doi.org/10.1093/nar/30.4.e15
  37. Zhang, W., C. E. Watson, C. Liu, K. J. Williams, and V. P. Werth. 2000. Glucocorticoids induce a near-total suppression of hyaluronan synthase mRNA in dermal fibroblasts and in osteoblasts: A molecular mechanism contributing to organ atrophy. Biochem. J. 349: 91-97 https://doi.org/10.1042/0264-6021:3490091