Planta Med 2020; 86(05): 348-355
DOI: 10.1055/a-1101-9326
Biological and Pharmacological Activity
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Potential Beneficial Effects of Digitaria ciliaris Flower Absolute on the Wound Healing-Linked Activities of Fibroblasts and Keratinocytes

Soo Min Park
1   Department of Cosmetic Science, College of Life and Health Sciences, Hoseo University, Asan, Republic of Korea
,
Kyung Jong Won
3   Department of Physiology and Medical Science, School of Medicine, Konkuk University, Chungju, Republic of Korea
,
Dae Il Hwang
1   Department of Cosmetic Science, College of Life and Health Sciences, Hoseo University, Asan, Republic of Korea
4   Institute of Jinan Red Ginseng, Jinan, Republic of Korea
,
Do Yoon Kim
2   College of Chemistry and Chemical Engineering, Hunan Institute of Science and Technology, Yueyang, Hunan, China
,
Ha Bin Kim
1   Department of Cosmetic Science, College of Life and Health Sciences, Hoseo University, Asan, Republic of Korea
,
Yali Li
1   Department of Cosmetic Science, College of Life and Health Sciences, Hoseo University, Asan, Republic of Korea
,
Hwan Myung Lee
1   Department of Cosmetic Science, College of Life and Health Sciences, Hoseo University, Asan, Republic of Korea
› Author Affiliations
Further Information

Publication History

received 04 August 2019
revised 06 January 2020

accepted 15 January 2020

Publication Date:
11 February 2020 (online)

Abstract

Digitaria ciliaris is widely reported to be a problematic weed in agricultural areas and is mainly used as an indicator plant for the development of herbicides. However, its bioactivities on skin regeneration and wound healing have not been investigated. In the present study, we investigated the effects of D. ciliaris flower absolute on skin wound healing and skin regeneration-related events, that is, proliferation, migration, and collagen biosynthesis, in human fibroblasts and keratinocytes. For this study, we extracted absolute from the D. ciliaris flower by solvent extraction and identified the composition of D. ciliaris flower absolute using GC/MS analysis. We also tested the effect of D. ciliaris flower absolute in CCD986sk fibroblasts and/or HaCaT keratinocytes using the WST assay and 5-bromo-2′-deoxyuridine incorporation assay, Boyden chamber assay, ELISA, sprouting assay, and immunoblotting. GC/MS analysis of D. ciliaris flower absolute revealed that it contained 15 compounds. The absolute increased the proliferations of keratinocytes and fibroblasts and the migration of fibroblasts but did not affect cell viabilities. In addition, it enhanced the syntheses of type I and IV collagen in fibroblasts, but not in keratinocytes. The sprouting assay showed increased sprout outgrowth of fibroblasts. In addition, D. ciliaris flower absolute induced the phosphorylation of extracellular signal-regulated kinase 1/2 and p38 mitogen-activated protein kinase in fibroblasts. These results indicate that D. ciliaris flower absolute may promote skin wound healing/regeneration by inducing the proliferation, migration, and collagen synthesis of fibroblasts, as well as the proliferation of keratinocytes. Therefore, D. ciliaris flower absolute may be a potential natural source for cosmetic or pharmaceutical agents that promote skin wound healing/regeneration.

 
  • References

  • 1 Pazyar N, Yaghoobi R, Rafiee E, Mehrabian A, Feily A. Skin wound healing and phytomedicine: a review. Skin Pharmacol Physiol 2014; 27: 303-310
  • 2 Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev 2003; 83: 835-870
  • 3 Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M. Growth factors and cytokines in wound healing. Wound Repair Regen 2008; 16: 585-601
  • 4 Pastar I, Stojadinovic O, Yin NC, Ramirez H, Nusbaum AG, Sawaya A, Patel SB, Khalid L, Isseroff RR, Tomic-Canic M. Epithelialization in wound healing: a comprehensive review. Adv Wound Care 2014; 3: 445-464
  • 5 Baum CL, Arpey CJ. Normal cutaneous wound healing: clinical correlation with cellular and molecular events. Dermatol Surg 2005; 31: 674-686
  • 6 Tuan TL, Keller LC, Sun D, Nimni ME, Cheung D. Dermal fibroblasts activate keratinocyte outgrowth on collagen gels. J Cell Sci 1994; 107: 2285-2289
  • 7 Li J, Chen J, Kirsner R. Pathophysiology of acute wound healing. Clin Dermatol 2007; 25: 9-18
  • 8 OʼToole EA. Extracellular matrix and keratinocyte migration. Clin Exp Dermatol 2001; 26: 525-530
  • 9 Hwang DI, Won KJ, Kim DY, Kim HB, Li Y, Lee HM. Chemical composition of Patrinia scabiosifolia flower absolute and its migratory and proliferative activities in human keratinocytes. Chem Biodivers 2019; 16: e1900252
  • 10 Brett D. A Review of Collagen and Collagen-based Wound Dressings. Wounds 2008; 20: 347-356
  • 11 Uitto J. Connective tissue biochemistry of the aging dermis. Age-related alterations in collagen and elastin. Dermatol Clin 1986; 4: 433-446
  • 12 Savvas M, Bishop J, Laurent G, Watson N, Studd J. Type III collagen content in the skin of postmenopausal women receiving oestradiol and testosterone implants. Br J Obstet Gynaecol 1993; 100: 154-156
  • 13 Rousselle P, Montmasson M, Garnier C. Extracellular matrix contribution to skin wound re-epithelialization. Matrix Biol 2019; 75 – 76: 12-26
  • 14 Smola H, Stark HJ, Thiekötter G, Mirancea N, Krieg T, Fusenig NE. Dynamics of basement membrane formation by keratinocyte-fibroblast interactions in organotypic skin culture. Exp Cell Res 1998; 239: 399-410
  • 15 Tang L, Sierra JO, Kelly R, Kirsner RS, Li J. Wool-derived keratin stimulates human keratinocyte migration and types IV and VII collagen expression. Exp Dermatol 2012; 21: 458-460
  • 16 Thakur R, Jain N, Pathak R, Sandhu SS. Practices in wound healing studies of plants. Evid Based Complement Alternat Med 2011; 2011: 438056
  • 17 Santema TB, Poyck PP, Ubbink DT. Skin grafting and tissue replacement for treating foot ulcers in people with diabetes. Cochrane Database Syst Rev 2016; (02) CD011255
  • 18 Maver T, Maver U, Stana Kleinschek K, Smrke DM, Kreft S. A review of herbal medicines in wound healing. Int J Dermatol 2015; 54: 740-751
  • 19 Negahdari S, Galehdari H, Kesmati M, Rezaie A, Shariati G. Wound healing activity of extracts and formulations of Aloe vera, Henna, Adiantum capillus-veneris, and Myrrh on mouse dermal fibroblast cells. Int J Prev Med 2017; 8: 18
  • 20 Ogden RK, Coblentz WK, Coffey KP, Turner JE, Scarbrough DA, Jennings JA, Richardson MD. Ruminal in situ disappearance kinetics of dry matter and fiber in growing steers for common crabgrass forages sampled on seven dates in northern Arkansas. J Anim Sci 2005; 83: 1142-1152
  • 21 Rao AN, Johnson DE, Sivaprasad B, Ladha JK, Mortimer AM. Weed management in direct-seeded rice. Adv Agron 2007; 93: 153-255
  • 22 Mokni RE, Verloove F. New records, distribution and taxonomic notes for non-native vascular flora of Tunisia – I. Poaceae. Fl Medit 2019; 29: 45-53
  • 23 Chauhan BS, Johnson E. Germination ecology of Southern crabgrass (Digitaria ciliaris) and India crabgrass (Digitaria longiflora): Two important weeds of rice in tropics. Weed Sci 2008; 56: 722-728
  • 24 Glenn BD, Brecke BJ, Bryan Unruh J, Ferrell JA, Kenworthy KE, Macdonald GE. Evaluation of alternative herbicides for southern crabgrass (Digitaria ciliaris) control in St. Augustinegrass. Weed Technol 2015; 29: 536-543
  • 25 Ma XZ, Pang ZD, Wang JH, Song Z, Zhao LM, Du XJ, Deng XL. The role and mechanism of K(Ca)3.1 channels in human monocyte migration induced by palmitic acid. Exp Cell Res 2018; 369: 208-217
  • 26 Mahmoudi R, Ghareghani M, Zibara K, Tajali Ardakani M, Jand Y, Azari H, Nikbakht J, Ghanbari A. Alyssum homolocarpum seed oil (AHSO), containing natural alpha linolenic acid, stearic acid, myristic acid and β-sitosterol, increases proliferation and differentiation of neural stem cells in vitro . BMC Complement Altern Med 2019; 19: 113
  • 27 Sagayama K, Tanaka N, Fukumoto T, Kashiwada Y. Lanostane-type triterpenes from the sclerotium of Inonotus obliquus (Chaga mushrooms) as proproliferative agents on human follicle dermal papilla cells. J Nat Med 2019; 73: 597-601
  • 28 Cho S, Choi CW, Lee DH, Won CH, Kim SM, Lee S, Lee MJ, Chung JH. High-dose squalene ingestion increases type I procollagen and decreases ultraviolet-induced DNA damage in human skin in vivo but is associated with transient adverse effects. Clin Exp Dermatol 2009; 34: 500-508
  • 29 Magdalon J, Hatanaka E, Romanatto T, Rodrigues HG, Kuwabara WM, Scaife C, Newsholme P, Curi R. A proteomic analysis of the functional effects of fatty acids in NIH 3T3 fibroblasts. Lipids Health Dis 2011; 10: 218
  • 30 Zhou BR, Zhang JA, Zhang Q, Permatasari F, Xu Y, Wu D, Yin ZQ, Luo D. Palmitic acid induces production of proinflammatory cytokines interleukin-6, interleukin-1β, and tumor necrosis factor-α via a NF-κB-dependent mechanism in HaCaT keratinocytes. Mediators Inflamm 2013; 2013: 530429
  • 31 Haase I, Evans R, Pofahl R, Watt FM. Regulation of keratinocyte shape, migration and wound epithelialization by IGF-1- and EGF-dependent signaling pathways. J Cell Sci 2003; 116: 3227-3238
  • 32 Pruniéras M, Régnier M, Fougère S, Woodley D. Keratinocytes synthesize basal-lamina proteins in culture. J Invest Dermatol 1983; 81 (Suppl. 01) 74s-81s
  • 33 Kisling A, Lust RM, Katwa LC. What is the role of peptide fragments of collagen I and IV in health and disease?. Life Sci 2019; 228: 30-34
  • 34 Katz M, Amit I, Yarden Y. Regulation of MAPKs by growth factors and receptor tyrosine kinases. Biochim Biophys Acta 2007; 1773: 1161-1176
  • 35 Yu XY, Qiao SB, Guan HS, Liu SW, Meng XM. Effects of visfatin on proliferation and collagen synthesis in rat cardiac fibroblasts. Horm Metab Res 2010; 42: 507-513
  • 36 Ranzato E, Mazzucco L, Patrone M, Burlando B. Platelet lysate promotes in vitro wound scratch closure of human dermal fibroblasts: different roles of cell calcium, P38, ERK and PI3K/AKT. J Cell Mol Med 2009; 13: 2030-2038
  • 37 Lee TH, Lee GW, Park KH, Mohamed MA, Bang MH, Baek YS, Son Y, Chung DK, Baek NI, Kim J. The stimulatory effects of Stewartia koreana extract on the proliferation and migration of fibroblasts and the wound healing activity of the extract in mice. Int J Mol Med 2014; 34: 145-152
  • 38 Makino T, Jinnin M, Muchemwa FC, Fukushima S, Kogushi-Nishi H, Moriya C, Igata T, Fujisawa A, Johno T, Ihn H. Basic fibroblast growth factor stimulates the proliferation of human dermal fibroblasts via the ERK1/2 and JNK pathways. Br J Dermatol 2010; 162: 717-723
  • 39 Roh SS, Lee MH, Hwang YL, Song HH, Jin MH, Park SG, Lee CK, Kim CD, Yoon TJ, Lee JH. Stimulation of the extracellular matrix production in dermal fibroblasts by velvet antler extract. Ann Dermatol 2010; 22: 173-179
  • 40 He T, Bai X, Yang L, Fan L, Li Y, Su L, Gao J, Han S, Hu D. Loureirin B inhibits hypertrophic scar formation via inhibition of the TGF-β1-ERK/JNK pathway. Cell Physiol Biochem 2015; 37: 666-676
  • 41 Sato M, Shegogue D, Gore EA, Smith EA, McDermott PJ, Trojanowska M. Role of p38 MAPK in transforming growth factor beta stimulation of collagen production by scleroderma and healthy dermal fibroblasts. J Invest Dermatol 2002; 118: 704-711
  • 42 Nagai Y, Miyata K, Sun GP, Rahman M, Kimura S, Miyatake A, Kiyomoto H, Kohno M, Abe Y, Yoshizumi M, Nishiyama A. Aldosterone stimulates collagen gene expression and synthesis via activation of ERK1/2 in rat renal fibroblasts. Hypertension 2005; 46: 1039-1045
  • 43 Lan CC, Fang AH, Wu PH, Wu CS. Tacrolimus abrogates TGF-β1-induced type I collagen production in normal human fibroblasts through suppressing p38 MAPK signalling pathway: implications on treatment of chronic atopic dermatitis lesions. J Eur Acad Dermatol Venereol 2014; 28: 204-215
  • 44 Kovats E. Gas chromatographic characterization of organic substances in the retention index system. Adv Chromatogr 1965; 1: 229-247
  • 45 Adams RP. Identification of essential Oil Components by Gas Chromatography/Mass Spectroscopy. Carol Stream, IL: Allured publishing Co.; 1995