Food Science and Biotechnology

, Volume 27, Issue 1, pp 147–157 | Cite as

The anti-photoaging and moisturizing effects of Bouea macrophylla extract in UVB-irradiated hairless mice

  • Yongin Cheong
  • Changhee Kim
  • Mi-Bo Kim
  • Jae-Kwan HwangEmail author


Ultraviolet (UV) light, a main cause of photoaging, leads to collapse of skin structure, resulting in wrinkle formation and dehydration. The present study assessed the anti-photoaging and moisturizing effects of Bouea macrophylla extract (BRE). UVB-irradiated hairless mice were orally administered with BME (300 mg/kg/day) for 8 weeks. BME ameliorated wrinkle formation, skin thickening, and inelasticity. BME upregulated COL1A1, COL3A1, COL4A1, and COL7A1 mRNA levels through activation of the transforming growth factor-β (TGF-β)/Smad pathway, thereby recovering the content of collagen reduced by UVB. Further, BME suppressed UVB-induced matrix metalloproteinase (MMP)-3 and MMP-13 expression and inhibited MMP-2 and MMP-9 activity by mediating the mitogen-activated protein kinases (MAPKs)/activator protein-1 (AP-1). BME improved moisture content by stimulating the expression of cornified envelope proteins and filaggrin-processing enzymes. Overall, the results show that BME prevents photoaging and promotes moisturization in UVB-irradiated hairless mice, suggesting its potential as a nutraceutical candidate for anti-photoaging and moisturizing effects.


Bouea macrophylla Matrix metalloproteinase Collagen Anti-photoaging Moisturizing effect 


Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.


  1. 1.
    El-Domyati M, Attia S, Saleh F, Brown D, Birk DE, Gasparro F, Ahmad H, Uitto J. Intrinsic aging vs. photoaging: a comparative histopathological, immunohistochemical, and ultrastructural study of skin. Experi. Dermatol. 11: 398–405 (2002).Google Scholar
  2. 2.
    Kuhn A, Zahn S, Patsinakidis N, Landmann A, Graef M, Sauerland C, Surber C, Wenzel J. Resistance to water and abrasion of a broad-spectrum sunscreen: a prospective, open-label study. Experi. Dermatol. 25: 151–152 (2016).CrossRefGoogle Scholar
  3. 3.
    Bickers DR, Athar M. Oxidative stress in the pathogenesis of skin disease. J. Investig. Dermatol. 126: 2565–2575 (2006).CrossRefGoogle Scholar
  4. 4.
    Passeron T, Ortonne J. Skin ageing and its prevention. Press. Medica. 32: 1474–1482 (2003).Google Scholar
  5. 5.
    Heng MC. Signaling pathways targeted by curcumin in acute and chronic injury: burns and photo-damaged skin. Int. J. Dermatol. 52: 531–543 (2013).CrossRefGoogle Scholar
  6. 6.
    Lu J, Guo JH, Tu XL, Zhang C, Zhao M, Zhang QW, Gao FH. Tiron inhibits UVB-Induced AP-1 binding sites transcriptional activation on MMP-1 and MMP-3 promoters by MAPK signaling pathway in human dermal fibroblasts. PloS ONE 11: e0159998 (2016).CrossRefGoogle Scholar
  7. 7.
    Watson RE, Gibbs NK, Griffiths CE, Sherratt MJ. Damage to skin extracellular matrix induced by UV exposure. Antioxid. Redox. Signal. 21: 1063–1077 (2014).CrossRefGoogle Scholar
  8. 8.
    Chen B, Li R, Yan N, Chen G, Qian W, Jiang HL, Ji C, Bi ZG. Astragaloside IV controls collagen reduction in photoaging skin by improving transforming growth factor-β/Smad signaling suppression and inhibiting matrix metalloproteinase-1. Mol. Med. Rep. 11: 3344–3348 (2015).CrossRefGoogle Scholar
  9. 9.
    Quan T, He T, Kang S, Voorhees JJ, Fisher GJ. Solar ultraviolet irradiation reduces collagen in photoaged human skin by blocking transforming growth factor-β type II receptor/Smad signaling. Am. J. Pathol. 165: 741–751 (2004).CrossRefGoogle Scholar
  10. 10.
    Gilmore TD. Introduction to NF-κB: players, pathways, perspectives. Oncogene 25: 6680–6684 (2006).CrossRefGoogle Scholar
  11. 11.
    Perkins ND. Integrating cell-signalling pathways with NF-κB and IKK function. Nat. Rev. Mol. Cell Biol. 8: 49–62 (2007).CrossRefGoogle Scholar
  12. 12.
    Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature 473: 298–307 (2011).CrossRefGoogle Scholar
  13. 13.
    Oh Y, Lim H-W, Kim K, Lim C-J. Ginsenoside Re improves skin barrier function in HaCaT keratinocytes under normal growth conditions. Biosci. Biotehcnol. Biochem 80: 2165–2167 (2016).CrossRefGoogle Scholar
  14. 14.
    Rinnerthaler M, Duschl J, Steinbacher P, Salzmann M, Bischof J, Schuller M, Wimmer H, Peer T, Bauer JW, Richter K. Age-related changes in the composition of the cornified envelope in human skin. Experi. Dermatol. 22: 329–335 (2013).CrossRefGoogle Scholar
  15. 15.
    Rajan NS, Bhat R. Antioxidant compounds and antioxidant activities in unripe and ripe kundang fruits (Bouea macrophylla Griffith). Fruits 71: 41–47 (2016).CrossRefGoogle Scholar
  16. 16.
    Heck DE, Vetrano AM, Mariano TM, Laskin JD. UVB light stimulates production of reactive oxygen species unexpected role for catalase. J. Biol. Chem. 278: 22432–22436 (2003).CrossRefGoogle Scholar
  17. 17.
    Park JE, Pyun HB, Woo SW, Jeong JH, Hwang JK. The protective effect of Kaempferia parviflora extract on UVB-induced skin photoaging in hairless mice. Photodermatol. Photoimmunol Photomed. 30: 237–245 (2014).CrossRefGoogle Scholar
  18. 18.
    Anggakusuma, Yanti, Hwang JK. Effects of macelignan isolated from Myristica fragrans Houtt. on UVB-induced matrix metalloproteinase-9 and cyclooxygenase-2 in HaCaT cells. J. Dermatol. Sci. 57: 114–122 (2010).CrossRefGoogle Scholar
  19. 19.
    Draelos ZD. The latest cosmeceutical approaches for anti-aging. J. Cosmet. Dermatol. 6: 2–6 (2007).CrossRefGoogle Scholar
  20. 20.
    Kim YJ, Kim HN, Shin MS, Choi BT. Thread embedding acupuncture inhibits ultraviolet B irradiation-induced skin photoaging in hairless mice. Evid. Based Complement. Alternat. Med. 2015 (2015).Google Scholar
  21. 21.
    Shirakata Y. Regulation of epidermal keratinocytes by growth factors. J. Dermatol. Sci. 59: 73–80 (2010).CrossRefGoogle Scholar
  22. 22.
    Kim HK. Garlic supplementation ameliorates UV-induced photoaging in hairless mice by regulating antioxidative activity and MMPs expression. Molecules 21: 70 (2016).CrossRefGoogle Scholar
  23. 23.
    Zhan JYX, Wang XF, Liu YH, Zhang ZB, Wang L, Chen JN, Huang S, Zeng HF, Lai XP. Andrographolide sodium bisulfate prevents UV-induced skin photoaging through inhibiting oxidative stress and inflammation. Mediators Inflamm. 2016: 1–12 (2016).CrossRefGoogle Scholar
  24. 24.
    Pillai S, Oresajo C, Hayward J. Ultraviolet radiation and skin aging: roles of reactive oxygen species, inflammation and protease activation, and strategies for prevention of inflammation-induced matrix degradation—a review. Int. J. Cosmet. Sci. 27: 17–34 (2005).CrossRefGoogle Scholar
  25. 25.
    Tanaka YT, Tanaka K, Kojima H, Hamada T, Masutani T, Tsuboi M, Akao Y. Cynaropicrin from Cynara scolymus L. suppresses photoaging of skin by inhibiting the transcription activity of nuclear factor-kappa B. Bioorg. Med. Chem. Lett. 23: 518–523 (2013).CrossRefGoogle Scholar
  26. 26.
    Amano S, Ogura Y, Akutsu N, Matsunaga Y, Kadoya K, Adachi E, Nishiyama T. Protective effect of matrix metalloproteinase inhibitors against epidermal basement membrane damage: skin equivalents partially mimic photoageing process. Br. J. Dermatol. 153: 37–46 (2005).CrossRefGoogle Scholar
  27. 27.
    Chen T, Hou H, Lu J, Zhang K, Li B. Protective effect of gelatin and gelatin hydrolysate from salmon skin on UV irradiation-induced photoaging of mice skin. J. Ocean U. China 15: 1–8 (2016).CrossRefGoogle Scholar
  28. 28.
    Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 69: 562–573 (2006).CrossRefGoogle Scholar
  29. 29.
    Page-McCaw A, Ewald AJ, Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8: 221–233 (2007).CrossRefGoogle Scholar
  30. 30.
    Pittayapruek P, Meephansan J, Prapapan O, Komine M, Ohtsuki M. Role of matrix metalloproteinases in photoaging and photocarcinogenesis. Int. J. Mol. Sci. 17: 868 (2016).CrossRefGoogle Scholar
  31. 31.
    Kim MS, Oh GH, Kim MJ, Hwang JK. Fucosterol inhibits matrix metalloproteinase expression and promotes type-1 procollagen production in UVB-induced HaCaT cells. Photochem. Photobiol. 89: 911–918 (2013).CrossRefGoogle Scholar
  32. 32.
    Candi E, Schmidt R, Melino G. The cornified envelope: a model of cell death in the skin. Nat. Rev. Mol. Cell Biol. 6: 328–340 (2005).CrossRefGoogle Scholar
  33. 33.
    Yamane M, Sugimura K, Kawasaki H, Tatsukawa H, Hitomi K. Analysis on transglutaminase 1 and its substrates using specific substrate peptide in cultured keratinocytes. Biochem. Biophys. Res. Commun. 478: 343–348 (2016).CrossRefGoogle Scholar
  34. 34.
    Kim H, Lim YJ, Park JH, Cho Y. Dietary silk protein, sericin, improves epidermal hydration with increased levels of filaggrins and free amino acids in NC/Nga mice. Br. J. Nutr. 108: 1726–1735 (2012).CrossRefGoogle Scholar
  35. 35.
    Lai CH, Chang SC, Chen YJ, Wang YJ, Lai YJ, Chang HD, Berens EB, Johnson MD, Wang JK, Lin CY. Matriptase and prostasin are expressed in human skin in an inverse trend over the course of differentiation and are targeted to different regions of the plasma membrane. Biol. Open 5: 1380–1387 (2016).CrossRefGoogle Scholar
  36. 36.
    Descargues P, Sil AK, Sano Y, Korchynskyi O, Han G, Owens P, Wang XJ, Karin M. IKKα is a critical coregulator of a Smad4-independent TGFβ-Smad2/3 signaling pathway that controls keratinocyte differentiation. Proc. Natl. Acad. Sci. 105: 2487–2492 (2008).CrossRefGoogle Scholar
  37. 37.
    Wu N, Sulpice E, Obeid P, Benzina S, Kermarrec F, Combe S, Gidrol X. The miR-17 family links p63 protein to MAPK signaling to promote the onset of human keratinocyte differentiation. PloS ONE, 7: e45761 (2012).CrossRefGoogle Scholar

Copyright information

© The Korean Society of Food Science and Technology and Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  • Yongin Cheong
    • 1
  • Changhee Kim
    • 1
  • Mi-Bo Kim
    • 1
  • Jae-Kwan Hwang
    • 1
    Email author
  1. 1.Department of Biotechnology, College of Life Science and BiotechnologyYonsei UniversitySeoulRepublic of Korea

Personalised recommendations