Toxicological Research

Korean Society of Toxicology & Korea Environmental Mutagen Society (한국독성학회)
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Antiphotoaging properties of Zingiber montanum essential oil isolated by solvent-free microwave extraction against ultraviolet B-irradiated human dermal fibroblasts

  • Navabhatra, Abhiruj (Department of Pharmacology, College of Pharmacy, Rangsit University) ;
  • Maniratanachote, Rawiwan (National Science and Technology Development Agency (NSTDA)) ;
  • Yingngam, Bancha (Department of Pharmaceutical Chemistry and Technology, Faculty of Pharmaceutical Sciences, Ubon Ratchathani University)
  • Received : 2021.07.16
  • Accepted : 2021.09.07
  • Published : 2022.04.15
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Abstract

Maintaining youthful skin from photoaging with natural products, including essential oils, is a vital strategy that has piqued the interest of researchers in the pharmaceutical and cosmetic industries. This research aimed to investigate the protective properties of Zingiber montanum (J. Koenig) Link ex A. Dietr. essential oil against ultraviolet B (UVB)-induced skin damage and photoaging in normal human dermal fibroblast (HDFn) cells. The essential oil was extracted from fresh plant rhizomes using solvent-free microwave extraction. Its antiphotoaging properties in HDFn cells were investigated using reactive oxygen species (ROS)-scavenging, wound healing, matrix metalloproteinases (MMP-1, MMP-3, and MMP-9) expression, procollagen synthesis, and elastase and tyrosinase inhibitory assays. The results showed that the test oil exhibited no significant toxicity in HDFn at concentrations up to 10 mg/mL, with cell viability exceeding 90%. Following UVB irradiation at 30 mJ/cm2, Z. montanum oil demonstrated time and concentration-dependent ROS radical scavenging capabilities. In a cell migration assay, the essential oil demonstrated wound-healing properties. Z. montanum oil suppressed the expression of MMPs and enhanced the synthesis of type I procollagen at a concentration of 0.1-1 mg/mL. In addition, 0.1-1 mg/mL Z. montanum oil inhibited elastase activity in a concentration-dependent manner but did not affect tyrosinase activity. From these findings, the essential oil of Z. montanum could have potential applications in developing cosmeceutical products to prevent skin photoaging.

Keywords

Acknowledgement

This work was supported by the Research Fund 2018 [Grant number 12/2018] of the Research Institute, Rangsit University, Thailand, and partly supported by the Research, Development, and Engineering Fund for National Nanotechnology, National Science and Technology Development Agency (NSTDA), Thailand. This manuscript was proofread and edited by Cambridge Proofreading LLC under the support of the Research Institute of Rangsit University.

References

  1. Kang CH, Rhie SJ, Kim YC (2018) Antioxidant and skin antiaging effects of marigold methanol extract. Toxicol Res 34:31-39. https://doi.org/10.5487/TR.2018.34.1.031
  2. Farage MA, Miller KW, Elsner P, Maibach HI (2008) Intrinsic and extrinsic factors in skin ageing: a review. Int J Cosmet Sci 30:87-95. https://doi.org/10.1111/j. 1468-2494. 2007. 00415.x
  3. Krutmann J, Schikowski T, Morita A, Berneburg M (2021) Environmentally- induced (extrinsic) skin aging: exposomal factors and underlying mechanisms. J Investig Dermatol 141:1096-1103. https://doi.org/10.1016/j.jid.2020.12.011
  4. Ichihashi M, Ando H, Yoshida M, Niki Y, Matsui M (2009) Photoaging of the skin. Anti-Aging Med 6:46-59. https://doi.org/10.3793/jaam.6.46
  5. Matsumura Y, Ananthaswamy HN (2004) Toxic effects of ultraviolet radiation on the skin. Toxicol Appl Pharmacol 195:298-308. https://doi.org/10.1016/j.taap.2003.08.019
  6. Monteiro e Silva AS, Michniak-Kohn B, Leonardi RG (2017) An overview about oxidation in clinical practice of skin aging. An Bras Dermatol 92:367-374. https://doi.org/10.1590/abd1806-4841.20175481
  7. Park KH, Kim J, Jung S, Sung KH, Son YK, Bae JM, Kim BH (2019) Alleviation of ultraviolet B-induced photoaging by 7-MEGATM 500 in hairless mouse skin. Toxicol Res 35:353-359. https://doi.org/10.5487/tr.2019.35.4.353
  8. Pittayapruek P, Meephansan J, Prapapan O, Komine M, Ohtsuki M (2016) Role of matrix metalloproteinases in photoaging and photocarcinogenesis. Int J Mol Sci 17:868. https://doi.org/10.3390/ijms17060868
  9. Hwang KA, Yi BR, Chul K (2011) Molecular mechanisms and in vivo mouse models of skin aging associated with dermal matrix alterations. Lab Anim Res 27:1-8. https://doi.org/10.5625/lar.2011.27.1.1
  10. Pillai S, Oresajo C, Hayward J (2005) Ultraviolet radiation and skin aging: roles of reactive oxygen species, inflammation andprotease activation, and strategies for prevention of inflammationinduced matrix degradation -a review. Int J Cosmet Sci 27:17-34. https://doi.org/10.1111/j.1467-2494.2004.00241.x
  11. Chase AJ, Bond M, Crook MF, Newby AC (2002) Role of nuclear factor-κB activation in metalloproteinase-1, -3, and -9 secretion by human macrophages in vitro and rabbit foam cells produced in vivo. Arterioscler Thromb Vasc Biol 22:765-771. https://doi.org/10.1161/01.atv.0000015078.09208.92
  12. Rabe JH, Mamelak AJ, McElgunn PJS, Morison WL, Sauder DN (2006) Photoaging: mechanisms and repair. J Am Acad Dermatol 55:1-19. https://doi.org/10.1016/j.jaad.2005.05.010
  13. Vincenti MP, Brinckerhoff CE (2002) Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res 4:157-164. https://doi.org/10.1186/ar401
  14. Correa D (2021) Global cosmetics market to reach $463.5 billion by 2027: Allied Market Research. https://www.globenewswire.com/news-release/2021/02/04/2170144/0/en/Global-Cosmetics-Market-to-Reach-463-5-Billion-by-2027-Allied-Market-Research.html. Accessed 18 Apr 2021
  15. Cavinato M, Waltenberger B, Baraldo G, Grade CVC, Stuppner H, Jansen-Durr P (2017) Plant extracts and natural compounds used against UVB-induced photoaging. Biogerontology 18:499-516. https://doi.org/10.1007/s10522-017-9715-7
  16. Kostyuk V, Potapovich A, Albuhaydar AR, Mayer W, De Luca C, Korkina L (2018) Natural substances for prevention of skin photoaging: Screening systems in the development of sunscreen and rejuvenation cosmetics. Rejuv Res 21:91-101. https://doi.org/10.1089/rej.2017.1931
  17. Sarkic A, Stappen I (2018) Essential oils and their single compounds in cosmetics-a critical review. Cosmetics 5:11. https://doi.org/10.3390/cosmetics5010011
  18. Chongmelaxme B, Sruamsiri R, Dilokthornsakul P, Dhippayom T, Kongkaew C, Saokaew S, Chuthaputti A, Chaiyakunapruk N (2017) Clinical effects of Zingiber cassumunar (Plai): a systematic review. Complement Ther Med 35:70-77. https://doi.org/10.1016/j.ctim.2017.09.009
  19. Pongprayoon U, Soontornsaratune P, Jarikasem S, Sematong T, Wasuwat S, Claeson P (1997) Topical antiinflammatory activity of the major lipophilic constituents of the rhizome of Zingiber cassumunar. Part I: the essential oil. Phytomedicine 3:319-322. https://doi.org/10.1016/s0944-7113(97)80003-7
  20. Rahman L, Lembang RS, Lallo S, Handayani SR, Usmanengsi Permana AD (2021) Bioadhesive dermal patch as promisingapproach for improved antibacterial activity of bioactive compound of Zingiber cassumunar Roxb in ex vivo Staphylococcusaureus skin infection model. J Drug Deliv Sci Technol 63: https://doi.org/10.1016/j.jddst.2021.102522
  21. Nagano T, Oyama Y, Kajita N, Chikahisa L, Nakata M, Okazaki E, Masuda T (1997) New curcuminoids isolated from Zingiber cassumuar protect cells suffering from oxidative stress: a flowcytometric study using rat thymocytes and H2O2. Jpn J Pharmacol 75:363-370. https://doi.org/10.1254/jjp.75.363
  22. Koontongkaew S, Meesuk L, Aupaphong V, Dechatiwongse Na Ayudhaya T, Poachanukoon O (2013) Inhibitory effect of Zingiber cassumunar extracts on lipopolysaccharide-induced cyclooxygenase- 2 and matrix metalloproteinase expression in human gingival fibroblasts. J Periodontal Res 48:507-516. https://doi.org/10.1111/jre.12033
  23. Jeenapongsa R, Yoovathaworn K, Sriwatanakul KM, Pongprayoon U, Sriwatanakul K (2003) Anti-inflammatory activity of (E)-1-(3,4-dimethoxyphenyl) butadiene from Zingiber cassumunar Roxb. J Ethnopharmacol 87:143-148. https://doi.org/10.1016/s0378-8741(03)00098-9
  24. Jitapunkul K, Poachanukoon O, Hannongbua S, Toochinda P, Lawtrakul L (2017) Simulation study of interactions between two bioactive components from Zingiber cassumunar and 5-lipoxygenase. Cell Mol Bioeng 11:77-89. https://doi.org/10.1007/s12195-017-0515-6
  25. Pongprayoon U, Tuchinda P, Claeson P, Sematong T, Reutrakul V, Soontornsaratune P (1997) Topical antiinflammatoryactivity of the major lipophilic constituents of the rhizome of Zingiber cassumunar. Part II: Hexane extractives. Phytomedicine 3:323-326. https://doi.org/10.1016/s0944-7113(97)80004-9
  26. Nakamura S, Iwami J, Matsuda H, Wakayama H, Pongpiriyadacha Y, Yoshikawa M (2009) Structures of new phenylbutanoids and nitric oxide production inhibitors from the rhizomes of Zingiber cassumunar. Chem Pharm Bull 57:1267-1272. https://doi.org/10.1248/cpb.57.1267
  27. Tewtrakul S, Subhadhirasakul S (2007) Anti-allergic activity of some selected plants in the Zingiberaceae family. J Ethnopharmacol 109:535-538. https://doi.org/10.1016/j.jep.2006.08.010
  28. Poachanukoon O, Meesuk L, Pattanacharoenchai N, Monthanapisut P, Dechatiwongse Na Ayudhya T, Koontongkaew S (2015) Zingiber cassumunar ROXb and its active constituent inhibit MMP-9 direct activation by house dust mite allergens and MMP-9 expression in PMA-stimulated human airway epithelial cells. Asian Pac J Allergy Immunol 33:42-51https://doi.org/10.12932/ap0490.33.1.2015
  29. Chaiwongsa R, Ongchai S, Boonsing P, Kongtawelert P, Panthong A, Reutrakul V (2013) Active compound of Zingiber Cassumunar Roxb. down-regulates the expression of genes involved in joint erosion in a human synovial fibroblast cell line. Afr J Tradit Complement Altern Med 10:40-48. https://doi.org/10.4314/ajtcam.v10i1.7
  30. Li MX, Bai X, Ma YP, Zhang HX, Nama N, Pei SJ, Du ZZ (2019) Cosmetic potentials of extracts and compounds from Zingiber cassumunar Roxb. rhizome. Ind Crops Prod 141:111764. https://doi.org/10.1016/j.indcrop.2019.111764
  31. Leelarungrayub J, Manorsoi J, Manorsoi A (2017) Anti-inflammatory activity of niosomes entrapped with Plai oil (Zingiber cassumunar Roxb.) by therapeutic ultrasound in a rat model. Int J Nanomed 12:2469-2476. https://doi.org/10.2147/ijn.s129131
  32. Yingngam B, Brantner A (2018) Boosting the essential oil yield from the rhizomes of cassumunar ginger by an eco-friendly solvent-free microwave extraction combined with central composite design. J Essent Oil Res 30:409-420. https://doi.org/10.1080/10412905.2018.1503099
  33. Yingngam B, Brantner A, Treichler M, Brugger N, Navabhatra A, Nakonrat P (2021) Optimization of the eco-friendly solvent-free microwave extraction of Limnophila aromatica essential oil. Ind Crops Prod 165:113443. https://doi.org/10.1016/j.indcrop.2021.113443
  34. WebBook, NIST Chemistry (2020) NIST standard reference database number 69. 2018. https://webbook.nist.gov/chemistry. Accessed 9 Mar 2020
  35. Mueller H, Kassack UM, Wiese M (2004) Comparison of the usefulness of the MTT, ATP, and calcein assays to predict the potency of cytotoxic agents in various human cancer cell lines. J Biomol Screen 9:506-515. https://doi.org/10.1177/1087057104265386
  36. Kalyanaraman B, Darley-Usmar V, Davies KJA, Dennery PA, Forman HJ, Grisham MB, Mann GE, Moore K, Roberts LJ, Ischiropoulos H (2012) Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med 52:1-6. https://doi.org/10.1016/j.freeradbiomed.2011.09.030
  37. Suarez-Arnedo A, Torres Figueroa F, Clavijo C, Arbelaez P, Cruz JC, Munoz-Camargo C (2020) An image J plugin for the high throughput image analysis of in vitro scratch wound healing assays. PLoS ONE 15: https://doi.org/10.1371/journal.pone.0232565
  38. Muniandy K, Gothai S, Tan WS, Kumar SS, Mohd Esa N, Chandramohan G, Al-Numair KS, Arulselvan P (2018) In vitro wound healing potential of stem extract of Alternanthera sessilis. J Evid Based Complementary Altern Med 2018:3142073. https://doi.org/10.1155/2018/3142073
  39. Momtaz S, Lall N, Basson A (2008) Inhibitory activities of mushroom tyrosine and DOPA oxidation by plant extracts. S Afr J Bot 74:577-582. https://doi.org/10.1016/j.sajb.2008.02.005
  40. An YA, Hwang JY, Lee JS, Kim YC (2015) Cornus officinalis methanol extract upregulates melanogenesis in Melan-a cells. Toxicol Res 31:165-172. https://doi.org/10.5487/tr.2015.31.2.165
  41. Chang TS (2012) Natural melanogenesis inhibitors acting through the down-regulation of tyrosinase activity. Materials (Basel) 5:1661-1685. https://doi.org/10.3390/ma5091661
  42. Kim SE, Lee CM, Kim YC (2017) Anti-melanogenic effect of Oenothera laciniata methanol extract in Melan-a cells. Toxicol Res 33:55-62. https://doi.org/10.5487/tr.2017.33.1.055
  43. Fisher GJ, Datta S, Wang Z, Li XY, Quan T, Chung JH, Kang S, Voorhees JJ (2000) c-Jun-dependent inhibition of cutaneous procollagen transcription following ultraviolet irradiation is reversed by all-trans retinoic acid. J Clin Investig 106:663-670. https://doi.org/10.1172/jci9362
  44. Kim MS, Kim YK, Cho KH, Chung JH (2006) Regulation of type I procollagen and MMP-1 expression after single or repeated exposure to infrared radiation in human skin. Mech Ageing Dev 127:875-882. https://doi.org/10.1016/j.mad.2006.09.007
  45. Park MA, Sim MJ, Kim YC (2017) Anti-photoaging effects of Angelica acutiloba root ethanol extract in human dermal fibroblasts. Toxicol Res 33:125-134. https://doi.org/10.5487/tr.2017.33.2.125
  46. Sriram G, Bigliardi PL, Bigliardi-Qi M (2015) Fibroblast heterogeneity and its implications for engineering organotypic skin models in vitro. Eur J Cell Biol 94:483-512. https://doi.org/10.1016/j.ejcb.2015.08.001
  47. Wang Y, Wang Y, Cheng C, Wang L, Yang J, Li H, Liu H, Cai L (2016) Establishment of a photoaging model in human dermal fibroblasts and study on photoaging-related biomarkers. Int J Clin Exp Med 9(5):8846-8851http://www.ijcem.com/files/ijcem0015786.pdf
  48. Cooper S, Bowden G (2007) Ultraviolet B regulation of transcription factor families: Roles of nuclear factor-kappa B (NF-κB) and activator protein-1 (AP-1) in UVB-induced skin carcinogenesis. Curr Cancer Drug Targets 7:325-334. https://doi.org/10.2174/156800907780809714
  49. Kwon KR, Alam MB, Park JH, Kim TH, Lee SH (2019) Attenuation of UVB-induced photo-aging by polyphenolic-rich Spatholobus suberectus stem extract via modulation of MAPK/AP-1/MMPs signaling in human keratinocytes. Nutrients 11:1341. https://doi.org/10.3390/nu11061341
  50. Subedi L, Lee TH, Wahedi HM, Baek SH, Kim SY (2017) Resveratrol-enriched rice attenuates UVB-ROS-induced skin aging via downregulation of inflammatory cascades. Oxid Med Cell Longev 2017:8379539. https://doi.org/10.1155/2017/8379539
  51. Fisher GJ, Datta SC, Talwar HS, Wang ZQ, Varani J, Kang S, Voorhees JJ (1996) Molecular basis of sun-induced premature skin ageing and retinoid antagonism. Nature 379:335-339. https://doi.org/10.1038/379335a0
  52. Quan T, Qin Z, Xia W, Shao Y, Voorhees JJ, Fisher GJ (2009) Matrix-degrading metalloproteinases in photoaging. J Investig Dermatol 14:20-24. https://doi.org/10.1038/jidsymp.2009.8
  53. Lee GH, Jin SW, Kim SJ, Pham TH, Choi JH, Jeong HG (2019) Tetrabromobisphenol A induces MMP-9 expression via NADPH oxidase and the activation of ROS, MAPK, and Akt pathways in human breast cancer MCF-7 cells. Toxicol Res 35:93-101. https://doi.org/10.5487/tr.2019.35.1.093
  54. Shin JW, Kwon SH, Choi JY, Na JI, Huh CH, Choi HR, Park KC (2019) Molecular mechanisms of dermal aging and antiaging approaches. Int J Mol Sci 20:2126. https://doi.org/10.3390/ijms20092126
  55. Tu Y, Quan T (2016) Oxidative stress and human skin connective tissue aging. Cosmetics 3:28. https://doi.org/10.3390/cosmetics3030028
  56. Cho JW, Jeong YS, Han JW, Chun YJ, Kim HK, Kim MY, Kim BJ, Park KM, Kim JK, Kim JH, Cho SM (2011) Skin hydration and collagen synthesis of AF-343 in HS68 cell line and NC/Nga mice by filaggrin expression and suppression of matrix metallopreteinase. Toxicol Res 27:225-229. https://doi.org/10.5487/tr.2011.27.4.225
  57. Ha BG, Park MA, Lee CM, Kim YC (2015) Antioxidant activity and anti-wrinkle effects of Aceriphyllum rossii leaf ethanol extract. Toxicol Res 31:363-369. https://doi.org/10.5487/tr.2015.31.4.363
  58. Kim SR, Jung YR, An HJ, Kim DH, Jang EJ, Choi YJ, Moon KM, Park MH, Park CH, Chung KW, Bae HR, Choi YW, Kim ND, Chung HY (2013) Anti-wrinkle and anti-inflammatory effects of active garlic components and the inhibition of MMPs via NF-κB signaling. PLoS ONE 8: https://doi.org/10.1371/journal.pone.0073877
  59. Pham QL, Jang HJ, Kim KB (2017) Anti-wrinkle effect of fermented black ginseng on human fibroblasts. Int J Mol Med 39:681-686. https://doi.org/10.3892/ijmm.2017.2858
  60. Aziz J, Shezali H, Radzi Z, Yahya NA, Abu Kassim NH, Czernuszka J, Rahman MT (2016) Molecular mechanisms of stressresponsive changes in collagen and elastin networks in skin. Skin Pharmacol Physiol 29:190-203. https://doi.org/10.1159/000447017
  61. Minami A, Fujita Y, Goto J, Iuchi A, Fujita K, Mikami Y, Shiratori M, Ishii A, Mitragotri S, Iwao Y, Kanazawa H, Kurebayashi Y, Takahashi T, Otsubo T, Ikeda K, Suzuki T (2021) Enhancement of elastin expression by transdermal administration of sialidase isozyme Neu2. Sci Rep 11:3302. https://doi.org/10.1038/s41598-021-82820-1
  62. Sparavigna A (2020) Role of the extracellular matrix in skin aging and dedicated treatment -state of the art. Plast Aesthet Res 7:14.https://doi.org/10.20517/2347-9264.2019.73
  63. Imokawa G, Ishida K (2015) Biological mechanisms underlying the ultraviolet radiation-induced formation of skin wrinkling and sagging I: Reduced skin elasticity, highly associated with enhanced eermal elastase activity, triggers wrinkling and sagging. Int J Mol Sci 16:7753-7775. https://doi.org/10.3390/ijms16047753
  64. Tsukahara K, Takema Y, Moriwaki S, Tsuji N, Suzuki Y, Fujimura T, Imokawa G (2001) Selective inhibition of skin fibroblast elastase elicits a concentration-dependent prevention of ultraviolet B-induced wrinkle formation. J Investig Dermatol 117:671-677. https://doi.org/10.1046/j.0022-202x.2001.01450.x
  65. Guo S, DiPietro LA (2010) Factors affecting wound healing. J Dent Res 89:219-229. https://doi.org/10.1177/0022034509359125
  66. Makrantonaki E, Wlaschek M, Scharffetter-Kochanek K (2017) Pathogenesis of wound healing disorders in the elderly. J Dtsch Dermatol Ges 15:255-275. https://doi.org/10.1111/ddg.13199
  67. Swain D, Gupta A (2015) Interfacial growth during closure of a cutaneous wound: stress generation and wrinkle formation. Soft Matter 11:6499-6508. https://doi.org/10.1039/c5sm01135c
  68. Zucker S, Mancuso P, DiMassimo B, Lysik RM, Conner C, Wu CL (1994) Comparison of techniques for measurement of gelatinases/type IV collagenases: enzyme-linked immunoassays versus substrate degradation assays. Clin Exp Metast 12:13-23. https://doi.org/10.1007/bf01784329
  69. Heo DH, Choi H, Yeom MY, Song BJ, Oh SJ (2014) Serum levels of matrix metalloproteinase-9 predict lymph nodemetastasis in breast cancer patients. Oncol Rep 31:1567-1572. https://doi.org/10.3892/or.2014.3001
  70. Prescimone T, Tognotti D, Caselli C, Cabiati M, D'Amico A, Ry SD, Giannessi D (2014) Reappraisal of quantitative gelzymography for matrix metalloproteinases. J Clin Lab Anal 28:374-380. https://doi.org/10.1002/jcla.21696
  71. Brenner M, Hearing VJ (2008) The protective role of melanin against UV damage in human skin. Photochem Photobiol 84:539-549. https://doi.org/10.1111/j.1751-1097.2007.00226.x
  72. Cestari TF, Dantas LP, Boza JC (2014) Acquired hyperpigmentations. An Bras Dermatol 89:11-25. https://doi.org/10.1590/abd1806-4841.20142353
  73. Stulberg DL, Clark N Tovey D (2003) Common hyperpigmentation disorders in adults: Part I. Diagnostic approach, Cafeau Lait Macules, diffuse hyperpigmentation, sun exposure, and phototoxic reactions. Am Fam Phys 68:1955-1960. https://pubmed.ncbi.nlm.nih.gov/14655804/
  74. Stulberg DL, Clark N, Tovey D (2003) Common hyperpigmentation disorders in adults: Part II. Melanoma, seborrheickeratoses, acanthosis nigricans, melasma, diabetic dermopathy, tinea versicolor, and postinflammatory hyperpigmentation.Am Fam Phys 68:1963-1968. https://pubmed.ncbi.nlm.nih.gov/14655805/
  75. Park J, Chung H, Bang SH, Han AR, Seo EK, Chang SE, Kang DH, Oh ES (2015) (E)-4-(3,4-Dimethoxyphenyl)but-3-en-1-ol enhances melanogenesis through increasing upstream stimulating factor-1-mediated tyrosinase expression. PLoS ONE 10: https://doi.org/10.1371/journal.pone.0141988
  76. Adam RP (2007) Identification of essential oil components by Gas Chromatography/Mass Spectrometry, 4th edn. Allured Publishing Corporation, Illinois