Matrix Metalloproteinases on Skin Photoaging.
MMP inhibitors
extracellular matrix breakdown
matrix metalloproteinase (MMP)
skin aging
Journal
Journal of cosmetic dermatology
ISSN: 1473-2165
Titre abrégé: J Cosmet Dermatol
Pays: England
ID NLM: 101130964
Informations de publication
Date de publication:
04 Sep 2024
04 Sep 2024
Historique:
revised:
31
07
2024
received:
21
05
2024
accepted:
20
08
2024
medline:
4
9
2024
pubmed:
4
9
2024
entrez:
4
9
2024
Statut:
aheadofprint
Résumé
Skin aging is characterized by an imbalance between the generation and degradation of extracellular matrix molecules (ECM). Matrix metalloproteinases (MMPs) are the primary enzymes responsible for ECM breakdown. Intrinsic and extrinsic stimuli can induce different MMPs. However, there is limited literature especially on the summary of skin MMPs and potential inhibitors. We aim to focus on the upregulation of MMP expression or activity in skin cells following exposure to UV radiation. We also would like to offer valuable insights into potential clinical applications of MMP inhibitors for mitigating skin aging. This article presents the summary of prior research, which involved an extensive literature search across diverse academic databases including Web of Science and PubMed. Our findings offer a comprehensive insight into the effects of MMPs on skin aging after UV irradiation, including their substrate preferences and distinct roles in this process. Additionally, a comprehensive list of natural plant and animal extracts, proteins, polypeptides, amino acids, as well as natural and synthetic compounds that serve as inhibitors for MMPs is compiled. Skin aging is a complex process influenced by environmental factors and MMPs. Research focuses on UV-induced skin damage and the formation of Advanced Glycosylation End Products (AGEs), leading to wrinkles and impaired functionality. Inhibiting MMPs is crucial for maintaining youthful skin. Natural sources of MMP inhibitor substances, such as extracts from plants and animals, offer a safer approach to obtain inhibitors through dietary supplements. Studying isolated active ingredients can contribute to developing targeted MMP inhibitors.
Sections du résumé
BACKGROUND
BACKGROUND
Skin aging is characterized by an imbalance between the generation and degradation of extracellular matrix molecules (ECM). Matrix metalloproteinases (MMPs) are the primary enzymes responsible for ECM breakdown. Intrinsic and extrinsic stimuli can induce different MMPs. However, there is limited literature especially on the summary of skin MMPs and potential inhibitors.
OBJECTIVE
OBJECTIVE
We aim to focus on the upregulation of MMP expression or activity in skin cells following exposure to UV radiation. We also would like to offer valuable insights into potential clinical applications of MMP inhibitors for mitigating skin aging.
METHODS
METHODS
This article presents the summary of prior research, which involved an extensive literature search across diverse academic databases including Web of Science and PubMed.
RESULTS
RESULTS
Our findings offer a comprehensive insight into the effects of MMPs on skin aging after UV irradiation, including their substrate preferences and distinct roles in this process. Additionally, a comprehensive list of natural plant and animal extracts, proteins, polypeptides, amino acids, as well as natural and synthetic compounds that serve as inhibitors for MMPs is compiled.
CONCLUSION
CONCLUSIONS
Skin aging is a complex process influenced by environmental factors and MMPs. Research focuses on UV-induced skin damage and the formation of Advanced Glycosylation End Products (AGEs), leading to wrinkles and impaired functionality. Inhibiting MMPs is crucial for maintaining youthful skin. Natural sources of MMP inhibitor substances, such as extracts from plants and animals, offer a safer approach to obtain inhibitors through dietary supplements. Studying isolated active ingredients can contribute to developing targeted MMP inhibitors.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024 The Author(s). Journal of Cosmetic Dermatology published by Wiley Periodicals LLC.
Références
F. H. Silver, L. M. Siperko, and G. P. Seehra, “Mechanobiology of Force Transduction in Dermal Tissue,” Skin Research and Technology 9, no. 1 (2003): 3–23.
J. Krutmann, A. Bouloc, G. Sore, B. A. Bernard, and T. Passeron, “The Skin Aging Exposome,” Journal of Dermatological Science 85, no. 3 (2017): 152–161.
A. M. Kligman, “Early Destructive Effect of Sunlight on Human Skin,” JAMA 210, no. 13 (1969): 2377–2380.
N. Cui, M. Hu, and R. A. Khalil, “Biochemical and Biological Attributes of Matrix Metalloproteinases,” Progress in Molecular Biology and Translational Science 147 (2017): 1–73.
F. H. Silver, Y. P. Kato, M. Ohno, and A. J. Wasserman, “Analysis of Mammalian Connective Tissue: Relationship Between Hierarchical Structures and Mechanical Properties,” Journal of Long‐Term Effects of Medical Implants 2, no. 2–3 (1992): 165–198.
J. Gross and C. M. Lapiere, “Collagenolytic Activity in Amphibian Tissues: A Tissue Culture Assay,” Proceedings of the National Academy of Sciences of the United States of America 48, no. 6 (1962): 1014–1022.
C. Amălinei, I. D. Căruntu, S. E. Giuşcă, and R. A. Bălan, “Matrix Metalloproteinases Involvement in Pathologic Conditions,” Romanian Journal of Morphology and Embryology 51, no. 2 (2010): 215–228.
V. M. Kähäri and U. Saarialho‐Kere, “Matrix Metalloproteinases in Skin,” Experimental Dermatology 6, no. 5 (1997): 199–213.
X. Wang and R. A. Khalil, “Matrix Metalloproteinases, Vascular Remodeling, and Vascular Disease,” Advances in Pharmacology 81 (2018): 241–330.
Y. Nakagami, K. Abe, N. Nishiyama, and N. Matsuki, “Laminin Degradation by Plasmin Regulates Long‐Term Potentiation,” Journal of Neuroscience 20, no. 5 (2000): 2003–2010.
A. Uemura, M. Nakamura, S. Kachi, et al., “Effect of Plasmin on Laminin and Fibronectin During Plasmin‐Assisted Vitrectomy,” Archives of Ophthalmology 123, no. 2 (2005): 209–213.
E. I. Deryugina and J. P. Quigley, “Cell Surface Remodeling by Plasmin: A New Function for an Old Enzyme,” Journal of Biomedicine and Biotechnology 2012 (2012): 1–21.
C. Tu, C. F. Ortega‐Cava, G. Chen, et al., “Lysosomal Cathepsin B Participates in the Podosome‐Mediated Extracellular Matrix Degradation and Invasion via Secreted Lysosomes in v‐Src Fibroblasts,” Cancer Research 68, no. 22 (2008): 9147–9156.
Z. Jevnikar, B. Mirković, U. P. Fonović, N. Zidar, U. Švajger, and J. Kos, “Three‐Dimensional Invasion of Macrophages Is Mediated by Cysteine Cathepsins in Protrusive Podosomes,” European Journal of Immunology 42, no. 12 (2012): 3429–3441.
H. Steinbrenner, M. C. Ramos, D. Stuhlmann, H. Sies, and P. Brenneisen, “UVA‐Mediated Downregulation of MMP‐2 and MMP‐9 in Human Epidermal Keratinocytes,” Biochemical and Biophysical Research Communications 308, no. 3 (2003): 486–491.
F. T. Vicentini, T. He, Y. Shao, et al., “Quercetin Inhibits UV Irradiation‐Induced Inflammatory Cytokine Production in Primary Human Keratinocytes by Suppressing NF‐κB Pathway,” Journal of Dermatological Science 61, no. 3 (2011): 162–168.
M. J. Petersen, C. Hansen, and S. Craig, “Ultraviolet A Irradiation Stimulates Collagenase Production in Cultured Human Fibroblasts,” Journal of Investigative Dermatology 99, no. 4 (1992): 440–444.
P. Brenneisen, J. Oh, M. Wlaschek, et al., “Ultraviolet B Wavelength Dependence for the Regulation of Two Major Matrix‐Metalloproteinases and Their Inhibitor TIMP‐1 in Human Dermal Fibroblasts,” Photochemistry and Photobiology 64, no. 4 (1996): 649–657.
J. Kim, C. W. Lee, E. K. Kim, et al., “Inhibition Effect of Gynura Procumbens Extract on UV‐B‐Induced Matrix‐Metalloproteinase Expression in Human Dermal Fibroblasts,” Journal of Ethnopharmacology 137, no. 1 (2011): 427–433.
H.‐M. Chiang, H. C. Chen, H. H. Chiu, C. W. Chen, S. M. Wang, and K. C. Wen, “Neonauclea reticulata (Havil.) Merr Stimulates Skin Regeneration After UVB Exposure via ROS Scavenging and Modulation of the MAPK/MMPs/Collagen Pathway,” Evidence‐Based Complementary and Alternative Medicine 2013 (2013): 1–9.
J. E. Park, H. B. Pyun, S. W. Woo, J. H. Jeong, and J. K. Hwang, “The Protective Effect of K Aempferia Parviflora Extract on UVB‐Induced Skin Photoaging in Hairless Mice,” Photodermatology, Photoimmunology & Photomedicine 30, no. 5 (2014): 237–245.
G. Imokawa and K. Ishida, “Biological Mechanisms Underlying the Ultraviolet Radiation‐Induced Formation of Skin Wrinkling and Sagging I: Reduced Skin Elasticity, Highly Associated With Enhanced Dermal Elastase Activity, Triggers Wrinkling and Sagging,” International Journal of Molecular Sciences 16, no. 4 (2015): 7753–7775.
H. Nakajima, Y. Ezaki, T. Nagai, R. Yoshioka, and G. Imokawa, “Epithelial–Mesenchymal Interaction During UVB‐Induced Up‐Regulation of Neutral Endopeptidase,” Biochemical Journal 443, no. 1 (2012): 297–305.
A. Tewari, K. Grys, J. Kollet, R. Sarkany, and A. R. Young, “Upregulation of MMP12 and Its Activity by UVA1 in Human Skin: Potential Implications for Photoaging,” Journal of Investigative Dermatology 134, no. 10 (2014): 2598–2609.
C.‐H. Park, M. J. Lee, J. Ahn, et al., “Heat Shock‐Induced Matrix Metalloproteinase (MMP)‐1 and MMP‐3 Are Mediated Through ERK and JNK Activation and via an Autocrine Interleukin‐6 Loop,” Journal of Investigative Dermatology 123, no. 6 (2004): 1012–1019.
Z. Chen, J. Y. Seo, Y. K. Kim, et al., “Heat Modulation of Tropoelastin, Fibrillin‐1, and Matrix Metalloproteinase‐12 in Human Skin In Vivo,” Journal of Investigative Dermatology 124, no. 1 (2005): 70–78.
P. Pittayapruek, J. Meephansan, O. Prapapan, M. Komine, and M. Ohtsuki, “Role of Matrix Metalloproteinases in Photoaging and Photocarcinogenesis,” International Journal of Molecular Sciences 17, no. 6 (2016): 868.
H. Nagase, R. Visse, and G. Murphy, “Structure and Function of Matrix Metalloproteinases and TIMPs,” Cardiovascular Research 69, no. 3 (2006): 562–573.
M. D. Sternlicht and Z. Werb, “How Matrix Metalloproteinases Regulate Cell Behavior,” Annual Review of Cell and Developmental Biology 17, no. 1 (2001): 463–516.
G. Imokawa, H. Nakajima, and K. Ishida, “Biological Mechanisms Underlying the Ultraviolet Radiation‐Induced Formation of Skin Wrinkling and Sagging II: Over‐Expression of Neprilysin Plays an Essential Role,” International Journal of Molecular Sciences 16, no. 4 (2015): 7776–7795.
M. Brennan, H. Bhatti, K. C. Nerusu, et al., “Matrix Metalloproteinase‐1 Is the Major Collagenolytic Enzyme Responsible for Collagen Damage in UV‐Irradiated Human Skin,” Photochemistry and Photobiology 78, no. 1 (2003): 43–48.
J. A. Urı́a, M. G. Jiménez, M. Balbı́n, J. M. P. Freije, and C. López‐Otı́n, “Differential Effects of Transforming Growth Factor‐β on the Expression of Collagenase‐1 and Collagenase‐3 in Human Fibroblasts,” Journal of Biological Chemistry 273, no. 16 (1998): 9769–9777.
D. Sbardella, G. F. Fasciglione, M. Gioia, et al., “Human Matrix Metalloproteinases: An Ubiquitarian Class of Enzymes Involved in Several Pathological Processes,” Molecular Aspects of Medicine 33, no. 2 (2012): 119–208.
V. Fortino, E. Maioli, C. Torricelli, P. Davis, and G. Valacchi, “Cutaneous MMPs Are Differently Modulated by Environmental Stressors in Old and Young Mice,” Toxicology Letters 173, no. 2 (2007): 73–79.
A. Y. Strongin, I. Collier, G. Bannikov, B. L. Marmer, G. A. Grant, and G. I. Goldberg, “Mechanism of Cell Surface Activation of 72‐kDa Type IV Collagenase: Isolation of the Activated Form of the Membrane Metalloprotease,” Journal of Biological Chemistry 270, no. 10 (1995): 5331–5338.
V. W. Wong, R. K. Garg, M. Sorkin, et al., “Loss of Keratinocyte Focal Adhesion Kinase Stimulates Dermal Proteolysis Through Upregulation of MMP9 in Wound Healing,” Annals of Surgery 260, no. 6 (2014): 1138–1146.
S.‐n. Xue, J. Lei, D. Z. Lin, C. Yang, and L. Yan, “Changes in Biological Behaviors of Rat Dermal Fibroblasts Induced by High Expression of MMP9,” World Journal of Emergency Medicine 5, no. 2 (2014): 139–143.
H. F. Bigg, A. D. Rowan, M. D. Barker, and T. E. Cawston, “Activity of Matrix Metalloproteinase‐9 Against Native Collagen Types I and III,” FEBS Journal 274, no. 5 (2007): 1246–1255.
I. E. Collier, W. Legant, B. Marmer, et al., “Diffusion of MMPs on the Surface of Collagen Fibrils: The Mobile Cell Surface–Collagen Substratum Interface,” PLoS One 6, no. 9 (2011): e24029.
M. D. Sternlicht, A. Lochter, C. J. Sympson, et al., “The Stromal Proteinase MMP3/Stromelysin‐1 Promotes Mammary Carcinogenesis,” Cell 98, no. 2 (1999): 137–146.
R. Visse and H. Nagase, “Matrix Metalloproteinases and Tissue Inhibitors of Metalloproteinases: Structure, Function, and Biochemistry,” Circulation Research 92, no. 8 (2003): 827–839.
C. Piperi and A. G. Papavassiliou, “Molecular Mechanisms Regulating Matrix Metalloproteinases,” Current Topics in Medicinal Chemistry 12, no. 10 (2012): 1095–1112.
M. Bashir, M. Sharma, and V. Werth, “TNF‐α Production in the Skin,” Archives of Dermatological Research 301 (2009): 87–91.
M. S. Ågren, R. Schnabel, L. H. Christensen, and U. Mirastschijski, “Tumor Necrosis Factor‐α‐Accelerated Degradation of Type I Collagen in Human Skin Is Associated With Elevated Matrix Metalloproteinase (MMP)‐1 and MMP‐3 Ex Vivo,” European Journal of Cell Biology 94, no. 1 (2015): 12–21.
M. Steenport, K. M. F. Khan, B. du, S. E. Barnhard, A. J. Dannenberg, and D. J. Falcone, “Matrix Metalloproteinase (MMP)‐1 and MMP‐3 Induce Macrophage MMP‐9: Evidence for the Role of TNF‐α and Cyclooxygenase‐2,” Journal of Immunology 183, no. 12 (2009): 8119–8127.
B. Wielockx, K. Lannoy, S. D. Shapiro, et al., “Inhibition of Matrix Metalloproteinases Blocks Lethal Hepatitis and Apoptosis Induced by Tumor Necrosis Factor and Allows Safe Antitumor Therapy,” Nature Medicine 7, no. 11 (2001): 1202–1208.
J. P. Witty, J. H. Wright, and L. M. Matrisian, “Matrix Metalloproteinases Are Expressed During Ductal and Alveolar Mammary Morphogenesis, and Misregulation of Stromelysin‐1 in Transgenic Mice Induces Unscheduled Alveolar Development,” Molecular Biology of the Cell 6, no. 10 (1995): 1287–1303.
U. Mirastschijski, B. Lupše, K. Maedler, et al., “Matrix Metalloproteinase‐3 Is Key Effector of TNF‐α‐Induced Collagen Degradation in Skin,” International Journal of Molecular Sciences 20, no. 20 (2019): 5234.
M. Madlener and S. Werner, “cDNA Cloning and Expression of the Gene Encoding Murine Stromelysin‐2 (MMP‐10),” Gene 202, no. 1–2 (1997): 75–81.
B. Quantin, G. Murphy, and R. Breathnach, “Pump‐1 cDNA Codes for a Protein With Characteristics Similar to Those of Classical Collagenase Family Members,” Biochemistry 28, no. 13 (1989): 5327–5334.
H. I. Park, J. Ni, F. E. Gerkema, D. Liu, V. E. Belozerov, and Q. X. A. Sang, “Identification and Characterization of Human Endometase (Matrix Metalloproteinase‐26) From Endometrial Tumor,” Journal of Biological Chemistry 275, no. 27 (2000): 20540–20544.
J. A. Uría and C. López‐Otín, “Matrilysin‐2, a New Matrix Metalloproteinase Expressed in Human Tumors and Showing the Minimal Domain Organization Required for Secretion, Latency, and Activity,” Cancer Research 60, no. 17 (2000): 4745–4751.
M. S. Ågren, T. Litman, J. O. Eriksen, P. Schjerling, M. Bzorek, and L. M. R. Gjerdrum, “Gene Expression Linked to Reepithelialization of Human Skin Wounds,” International Journal of Molecular Sciences 23, no. 24 (2022): 15746.
M. Seiki, “Membrane‐Type 1 Matrix Metalloproteinase: A Key Enzyme for Tumor Invasion,” Cancer Letters 194, no. 1 (2003): 1–11.
P. Zigrino, J. Brinckmann, A. Niehoff, et al., “Fibroblast‐Derived MMP‐14 Regulates Collagen Homeostasis in Adult Skin,” Journal of Investigative Dermatology 136, no. 8 (2016): 1575–1583.
F. Sabeh, I. Ota, K. Holmbeck, et al., “Tumor Cell Traffic Through the Extracellular Matrix Is Controlled by the Membrane‐Anchored Collagenase MT1‐MMP,” Journal of Cell Biology 167, no. 4 (2004): 769–781.
B. Zheng, Z. Zhang, C. M. Black, B. de Crombrugghe, and C. P. Denton, “Ligand‐Dependent Genetic Recombination in Fibroblasts: A Potentially Powerful Technique for Investigating Gene Function in Fibrosis,” American Journal of Pathology 160, no. 5 (2002): 1609–1617.
A. Gutierrez‐Fernandez, C. Soria‐Valles, F. G. Osorio, et al., “Loss of MT1‐MMP Causes Cell Senescence and Nuclear Defects Which Can be Reversed by Retinoic Acid,” EMBO Journal 34, no. 14 (2015): 1875–1888.
Y. Itoh and M. Seiki, “MT1‐MMP: A Potent Modifier of Pericellular Microenvironment,” Journal of Cellular Physiology 206, no. 1 (2006): 1–8.
I. Ivanova, B. Kurz, K. Lang, T. Maisch, M. Berneburg, and Y. Kamenisch, “Investigation of the HelioVital Filter Foil Revealed Protective Effects Against UVA1 Irradiation‐Induced DNA Damage and Against UVA1‐Induced Expression of Matrixmetalloproteinases (MMP) MMP1, MMP2, MMP3 and MMP15,” Photochemical & Photobiological Sciences 21, no. 3 (2022): 361–372.
S. Taddese, A. S. Weiss, G. Jahreis, R. H. H. Neubert, and C. E. H. Schmelzer, “In Vitro Degradation of Human Tropoelastin by MMP‐12 and the Generation of Matrikines From Domain 24,” Matrix Biology 28, no. 2 (2009): 84–91.
J. H. Chung, J. Y. Seo, M. K. Lee, et al., “Ultraviolet Modulation of Human Macrophage Metalloelastase in Human Skin In Vivo,” Journal of Investigative Dermatology 119, no. 2 (2002): 507–512.
S. Taddese, A. S. Weiss, R. H. H. Neubert, and C. E. H. Schmelzer, “Mapping of Macrophage Elastase Cleavage Sites in Insoluble Human Skin Elastin,” Matrix Biology 27, no. 5 (2008): 420–428.
E. Lenci, L. Cosottini, and A. Trabocchi, “Novel Matrix Metalloproteinase Inhibitors: An Updated Patent Review (2014–2020),” Expert Opinion on Therapeutic Patents 31, no. 6 (2021): 509–523.
H. Yuan, Q. Ma, L. Ye, and G. Piao, “The Traditional Medicine and Modern Medicine From Natural Products,” Molecules 21, no. 5 (2016): 559.
S. Costa, S. Schwaiger, R. Cervellati, H. Stuppner, E. Speroni, and M. C. Guerra, “In Vitro Evaluation of the Chemoprotective Action Mechanisms of Leontopodic Acid Against Aflatoxin B1 and Deoxynivalenol‐Induced Cell Damage,” Journal of Applied Toxicology 29, no. 1 (2009): 7–14.
I.‐E. Pralea, R. C. Moldovan, A. B. Țigu, et al., “Profiling of Polyphenolic Compounds of Leontopodium Alpinum Cass Callus Cultures Using UPLC/IM‐HRMS and Screening of In Vitro Effects,” Plants 11, no. 1 (2021): 100.
U. Reisinger, S. Schwaiger, I. Zeller, et al., “Leoligin, the Major Lignan From Edelweiss, Inhibits Intimal Hyperplasia of Venous Bypass Grafts,” Cardiovascular Research 82, no. 3 (2009): 542–549.
M. J. Dobner, S. Sosa, S. Schwaiger, et al., “Anti‐Inflammatory Activity of Leontopodium alpinum and Its Constituents,” Planta Medica 70, no. 06 (2004): 502–508.
E. Speroni, S. Schwaiger, P. Egger, et al., “In Vivo Efficacy of Different Extracts of Edelweiss (Leontopodium alpinum Cass.) in Animal Models,” Journal of Ethnopharmacology 105, no. 3 (2006): 421–426.
X. Meng, M. Guo, Z. Geng, et al., “Effects and Mechanism of the Leontopodium alpinum Callus Culture Extract on Blue Light Damage in Human Foreskin Fibroblasts,” Molecules 28, no. 5 (2023): 2172.
E. Son, Y. M. Lee, S. H. Kim, and D. S. Kim, “Photoprotective Effects of Processed Ginseng Leaf Administration Against UVB‐Induced Skin Damage in Hairless Mice,” Molecules 28, no. 18 (2023): 6734.
Q. Meng, Y. Niu, X. Niu, R. H. Roubin, and J. R. Hanrahan, “Ethnobotany, Phytochemistry and Pharmacology of the Genus Caragana Used in Traditional Chinese Medicine,” Journal of Ethnopharmacology 124, no. 3 (2009): 350–368.
S. R. Lee, J. H. Kwak, H. J. Kim, and S. Pyo, “Neuroprotective Effects of Kobophenol Against the Withdrawal of Tropic Support, Nitrosative Stress, and Mitochondrial Damage in SH‐SY5Y Neuroblastoma Cells,” Bioorganic & Medicinal Chemistry Letters 17, no. 7 (2007): 1879–1882.
B. Zhao, J. Q. Liu, Z. Zheng, et al., “Human Amniotic Epithelial Stem Cells Promote Wound Healing by Facilitating Migration and Proliferation of Keratinocytes via ERK, JNK and AKT Signaling Pathways,” Cell and Tissue Research 365 (2016): 85–99.
M.‐S. Kim, Y. K. Kim, H. C. Eun, K. H. Cho, and J. H. Chung, “All‐Trans Retinoic Acid Antagonizes UV‐Induced VEGF Production and Angiogenesis via the Inhibition of ERK Activation in Human Skin Keratinocytes,” Journal of Investigative Dermatology 126, no. 12 (2006): 2697–2706.
H.‐E. Kim, H. Cho, A. Ishihara, B. Kim, and O. Kim, “Cell Proliferation and Migration Mechanism of Caffeoylserotonin and Serotonin via Serotonin 2B Receptor in Human Keratinocyte HaCaT Cells,” BMB Reports 51, no. 4 (2018): 188–193.
J. Kang, W. Chen, J. Xia, et al., “Extracellular Matrix Secreted by Senescent Fibroblasts Induced by UVB Promotes Cell Proliferation in HaCaT Cells Through PI3K/AKT and ERK Signaling Pathways,” International Journal of Molecular Medicine 21, no. 6 (2008): 777–784.
L. Su, L. Fu, X. Li, et al., “Loss of CAR Promotes Migration and Proliferation of HaCaT Cells and Accelerates Wound Healing in Rats via Src‐p38 MAPK Pathway,” Scientific Reports 6, no. 1 (2016): 19735.
J. Zhang, L. Li, Q. Zhang, et al., “Microtubule‐Associated Protein 4 Phosphorylation Regulates Epidermal Keratinocyte Migration and Proliferation,” International Journal of Biological Sciences 15, no. 9 (2019): 1962–1976.
A. Gazel, R. I. Nijhawan, R. Walsh, and M. Blumenberg, “Transcriptional Profiling Defines the Roles of ERK and p38 Kinases in Epidermal Keratinocytes,” Journal of Cellular Physiology 215, no. 2 (2008): 292–308.
M. Schüppel, U. Kürschner, U. Kleuser, M. Schäfer‐Korting, and B. Kleuser, “Sphingosine 1‐Phosphate Restrains Insulin‐Mediated Keratinocyte Proliferation via Inhibition of Akt Through the S1P2 Receptor Subtype,” Journal of Investigative Dermatology 128, no. 7 (2008): 1747–1756.
M. J. Kim, K. J. Won, D. Y. Kim, et al., “Skin Wound Healing and Anti‐Wrinkle‐Promoting In Vitro Biological Activities of Caragana sinica Flower Absolute and Its Chemical Composition,” Pharmaceuticals 16, no. 2 (2023): 235.
E. J. Jeong, L. Hwang, M. Lee, K. Y. Lee, M. J. Ahn, and S. H. Sung, “Neuroprotective Biflavonoids of Chamaecyparis obtusa Leaves Against Glutamate‐Induced Oxidative Stress in HT22 Hippocampal Cells,” Food and Chemical Toxicology 64 (2014): 397–402.
K. Madhuri and P. R. Naik, “Ameliorative Effect of Borneol, a Natural Bicyclic Monoterpene Against Hyperglycemia, Hyperlipidemia and Oxidative Stress in Streptozotocin‐Induced Diabetic Wistar Rats,” Biomedicine & Pharmacotherapy 96 (2017): 336–347.
C. M. Park and H. S. Yoon, “Anti‐Bacterial Effects of Lavender and Peppermint Oils on Streptococcus mutans,” Journal of Korean Academy of Oral Health 42, no. 4 (2018): 210–215.
Y.‐A. Jang, S. G. Kim, H. K. Kim, and J. T. Lee, “Biological Activity and Component Analyses of Chamaecyparis obtusa Leaf Extract: Evaluation of Antiwrinkle and Cell Protection Effects in UVA‐Irradiated Cells,” Medicina 59, no. 4 (2023): 755.
J. M. Choi, S. I. Lee, and E. J. Cho, “Effect of Vigna angularis on High‐Fat Diet‐Induced Memory and Cognitive Impairments,” Journal of Medicinal Food 23, no. 11 (2020): 1155–1162.
S. Oh, S. Zheng, M. Fang, et al., “Anti‐Photoaging Effect of Phaseolus angularis L. Extract on UVB‐Exposed HaCaT Keratinocytes and Possibilities as Cosmetic Materials,” Molecules 28, no. 3 (2023): 1407.
H. Bunawan, S. N. Baharum, S. N. Bunawan, N. M. Amin, and N. M. Noor, “Cosmos caudatus Kunth: A Traditional Medicinal Herb,” Global Journal of Pharmacology 8, no. 3 (2014): 420–426.
S.‐H. Cheng, M. Y. Barakatun‐Nisak, J. Anthony, and A. Ismail, “Potential Medicinal Benefits of Cosmos caudatus (Ulam Raja): A Scoping Review,” Journal of Research in Medical Sciences: The Official Journal of Isfahan University of Medical Sciences 20, no. 10 (2015): 1000–1006.
Y. C. Loo, H. C. Hu, S. Y. Yu, et al., “Development on Potential Skin Anti‐Aging Agents of Cosmos caudatus Kunth via Inhibition of Collagenase, MMP‐1 and MMP‐3 Activities,” Phytomedicine 110 (2023): 154643.
Y.‐J. Park, M. Kim, and S.‐J. Bae, “Enhancement of Anticarcinogenic Effect by Combination of Lycii fructus With Vitamin C,” Journal‐Korean Society of Food Science and Nutrition 31, no. 1 (2002): 143–148.
J.‐S. Park, J. D. Park, B. C. Lee, K.‐J. Choi, S.‐W. Ra, and K.‐W. Chang, “Effects of Extracts From Various Parts of Lycium chinense Mill. on the Proliferation of Mouse Spleen Cells,” Korean Journal of Medicinal Crop Science 8, no. 4 (2000): 291–296.
K.‐I. Kang, J.‐Y. Jung, K.‐H. Koh, and C.‐H. Lee, “Hepatoprotective Effects of Lycium chinense Mill. Fruit Extracts and Fresh Fruit Juice,” Korean Journal of Food Science and Technology 38, no. 1 (2006): 99–103.
H.‐B. Deng, D. P. Cui, J. M. Jiang, Y. C. Feng, N. S. Cai, and D. D. Li, “Inhibiting Effects of Achyranthes bidentata Polysaccharide and Lycium barbarum Polysaccharide on Nonenzyme Glycation in D‐Galactose Induced Mouse Aging Model,” Biomedical and Environmental Sciences: BES 16, no. 3 (2003): 267–275.
A. Debib, M. Dueñas, M. Boumediene, R. A. Mothana, A. Latifa, and M. A. Tir‐Touil, “Synergetic Hepatoprotective Effect of Phenolic Fractions Obtained From Ficus carica Dried Fruit and Extra Virgin Olive Oil on CCL4‐Induced Oxidative Stress and Hepatotoxicity in Rats,” Journal of Food Biochemistry 40, no. 4 (2016): 507–516.
H. Seo, C. Kim, M. B. Kim, and J. K. Hwang, “Anti‐Photoaging Effect of Korean Mint (Agastache rugosa Kuntze) Extract on UVB‐Irradiated Human Dermal Fibroblasts,” Preventive Nutrition and Food Science 24, no. 4 (2019): 442–448.
M.‐S. Yun, C. Kim, and J.‐K. Hwang, “Agastache rugosa Kuntze Attenuates UVB‐Induced Photoaging in Hairless Mice Through the Regulation of MAPK/AP‐1 and TGF‐β/Smad Pathways,” Journal of Microbiology and Biotechnology 29, no. 9 (2019): 1349–1360.
J. H. Yoo, J. S. Lee, J. H. Jang, J. I. Jung, E. J. Kim, and S. Y. Choi, “AGEs Blocker™(Goji Berry, fig, and Korean Mint Mixed Extract) Inhibits Skin Aging Caused by Streptozotocin‐Induced Glycation in Hairless Mice,” Preventive Nutrition and Food Science 28, no. 2 (2023): 134–140.
J. Jung, Y. J. Choi, J. H. Yoo, S. Y. Choi, and E. J. Kim, “Antiphotoaging Effect of AGEs Blocker™ in UVB‐Irradiated Cells and Skh: HR‐1 Hairless Mice,” Current Issues in Molecular Biology 45, no. 5 (2023): 4181–4199.
S. M. Ulven, B. Kirkhus, A. Lamglait, et al., “Metabolic Effects of Krill Oil Are Essentially Similar to Those of Fish Oil but at Lower Dose of EPA and DHA, in Healthy Volunteers,” Lipids 46, no. 1 (2011): 37–46.
J. Kim, N. Lee, Y. S. Chun, S. H. Lee, and S. K. Ku, “Krill Oil's Protective Benefits Against Ultraviolet B‐Induced Skin Photoaging in Hairless Mice and In Vitro Experiments,” Marine Drugs 21, no. 9 (2023): 479.
B. K. Patel, K. H. Patel, R. Y. Huang, C. N. Lee, and S. M. Moochhala, “The Gut‐Skin Microbiota Axis and Its Role in Diabetic Wound Healing—A Review Based on Current Literature,” International Journal of Molecular Sciences 23, no. 4 (2022): 2375.
S.‐Y. Lee, E. Lee, Y. M. Park, and S. J. Hong, “Microbiome in the Gut‐Skin Axis in Atopic Dermatitis,” Allergy, Asthma & Immunology Research 10, no. 4 (2018): 354–362.
J.‐Y. Park, J. Y. Lee, Y. G. Kim, and C. H. Kang, “Latilactobacillus sakei Wikim0066 Protects Skin Through MMP Regulation on UVB‐Irradiated In Vitro and In Vivo Model,” Nutrients 15, no. 3 (2023): 726.
X. Zhang, J. Xu, M. Ma, et al., “Heat‐Killed Lactobacillus rhamnosus ATCC 7469 Improved UVB‐Induced Photoaging via Antiwrinkle and Antimelanogenesis Impacts,” Photochemistry and Photobiology 99 (2023): 1318–1331.
M. Hamayun, S. A. Khan, S. EunYoung, S. EunYoung, and L. I. J. L. InJung, “Folk Medicinal Knowledge and Conservation Status of Some Economically Valued Medicinal Plants of District Swat, Pakistan,” Lyonia 11, no. 2 (2006): 101–113.
M. Hamayun, “Ethnobotanical Studies of Some Useful Shrubs and Trees of District Buner, NWFP, Pakistan,” Ethnobotanical Leaflets 2003, no. 1 (2003): 12.
P. A. Cohen, J. C. Travis, P. H. J. Keizers, F. E. Boyer, and B. J. Venhuis, “The Stimulant Higenamine in Weight Loss and Sports Supplements,” Clinical Toxicology 57, no. 2 (2019): 125–130.
D. Kim, J. H. Yun, E. Roh, H. S. Shin, and J. E. Kim, “Higenamine Reduces Fine‐Dust‐Induced Matrix Metalloproteinase (MMP)‐1 in Human Keratinocytes,” Plants 12, no. 13 (2023): 2479.
F. Chen, X. Guo, and Y. Wu, “Skin Antiaging Effects of a Multiple Mechanisms Hyaluronan Complex,” Skin Research and Technology 29, no. 6 (2023): e13350.
Y. Guo, Y. Zhang, Y. S. Wang, L. Y. Ma, H. Liu, and W. Gao, “Protective Effect of Salvia plebeia R. Br Ethanol Extract on UVB‐Induced Skin Photoaging In Vitro and In Vivo,” Photodermatology, Photoimmunology & Photomedicine 39 (2023): 466–477.
R. K. Pandey, L. N. Goswami, Y. Chen, et al., “Nature: A Rich Source for Developing Multifunctional Agents. Tumor‐Imaging and Photodynamic Therapy,” Lasers in Surgery and Medicine: The Official Journal of the American Society for Laser Medicine and Surgery 38, no. 5 (2006): 445–467.
X. Liu, R. Zhang, H. Shi, et al., “Protective Effect of Curcumin Against Ultraviolet A Irradiation‐Induced Photoaging in Human Dermal Fibroblasts,” Molecular Medicine Reports 17, no. 5 (2018): 7227–7237.
L. Zhang, J. Q. Gan, and H. Wang, “Neurocognitive Mechanisms of Mathematical Giftedness: A Literature Review,” Applied Neuropsychology: Child 6, no. 1 (2017): 79–94.
S. S. Jalde, A. K. Chauhan, J. H. Lee, P. K. Chaturvedi, J. S. Park, and Y. W. Kim, “Synthesis of Novel Chlorin e6‐Curcumin Conjugates as Photosensitizers for Photodynamic Therapy Against Pancreatic Carcinoma,” European Journal of Medicinal Chemistry 147 (2018): 66–76.
T. B. Thapa Magar, S. K. Mallik, P. Gurung, et al., “Chlorin E6‐Curcumin‐Mediated Photodynamic Therapy Promotes an Anti‐Photoaging Effect in UVB‐Irradiated Fibroblasts,” International Journal of Molecular Sciences 24, no. 17 (2023): 13468.
F. C. Ip, Y. P. Ng, H. J. An, et al., “Cycloastragenol Is a Potent Telomerase Activator in Neuronal Cells: Implications for Depression Management,” Neurosignals 22, no. 1 (2014): 52–63.
Y. Yu, L. Zhou, Y. Yang, and Y. Liu, “Cycloastragenol: An Exciting Novel Candidate for Age‐Associated Diseases,” Experimental and Therapeutic Medicine 16, no. 3 (2018): 2175–2182.
M. H. Yang, S. T. Hwang, J. Y. Um, and K. S. Ahn, “Cycloastragenol Exerts Protective Effects Against UVB Irradiation in Human Dermal Fibroblasts and HaCaT Keratinocytes,” Journal of Dermatological Science 111, no. 2 (2023): 60–67.
H. J. Lee, A. R. Im, S. M. Kim, H. S. Kang, J. D. Lee, and S. Chae, “The Flavonoid Hesperidin Exerts Anti‐Photoaging Effect by Downregulating Matrix Metalloproteinase (MMP)‐9 Expression via Mitogen Activated Protein Kinase (MAPK)‐Dependent Signaling Pathways,” BMC Complementary and Alternative Medicine 18 (2018): 1–9.
Y. S. Sheen, H. Y. Huang, and Y. H. Liao, “The Efficacy and Safety of an Antiaging Topical Serum Containing Hesperetin and Sodium Cyclic Lysophosphatidic Acid: A Single‐Center Clinical Trial,” Journal of Cosmetic Dermatology 20, no. 12 (2021): 3960–3967.
H. Pageon, A. Azouaoui, H. Zucchi, S. Ricois, C. Tran, and D. Asselineau, “Potentially Beneficial Effects of Rhamnose on Skin Ageing: An In Vitro and In Vivo Study,” International Journal of Cosmetic Science 41, no. 3 (2019): 213–220.
R. Novotná, D. Škařupová, J. Hanyk, et al., “Hesperidin, Hesperetin, Rutinose, and Rhamnose Act as Skin Anti‐Aging Agents,” Molecules 28, no. 4 (2023): 1728.
Q. Hong, S. Wang, S. Liu, X. Chen, and G. Cai, “LRG1 May Accelerate the Progression of ccRCC via the TGF‐β Pathway,” BioMed Research International 2020 (2020): 1–9.
H. N. Park, M. J. Song, Y. E. Choi, D. H. Lee, J. H. Chung, and S. T. Lee, “LRG1 Promotes ECM Integrity by Activating the TGF‐β Signaling Pathway in Fibroblasts,” International Journal of Molecular Sciences 24, no. 15 (2023): 12445.
S. M. Ham, M. J. Song, H. S. Yoon, D. H. Lee, J. H. Chung, and S. T. Lee, “SPARC Is Highly Expressed in Young Skin and Promotes Extracellular Matrix Integrity in Fibroblasts via the TGF‐β Signaling Pathway,” International Journal of Molecular Sciences 24, no. 15 (2023): 12179.
Y. Zhou, R. Bai, Y. Huang, et al., “The Anti‐Photoaging Effect of C‐Phycocyanin on Ultraviolet B‐Irradiated BALB/c‐Nu Mouse Skin,” Frontiers in Bioengineering and Biotechnology 11 (2023): 1229387.
W. Cho, J. Park, M. Lee, et al., “Gly‐Pro‐Val‐Gly‐Pro‐Ser Peptide Fish Collagen Improves Skin Moisture and Wrinkles With Ameliorated the Oxidative Stress and Pro‐Inflammatory Factors in Skin Photoaging Mimic Models,” Preventive Nutrition and Food Science 28, no. 1 (2023): 50–60.
R. Olsen and T. DeLorey, “GABA and Glycine,” in Basic Neurochemistry: Molecular, Cellular and Medical Aspects, eds. G. J. Siegel, B. W. Agranoff, R. W. Albers, S. K. Fisher, and M. D. Uhler (Philadelphia, PA: Lippincott, Williams & Wilkins, 1999), 335–346.
U. Warskulat, A. Reinen, S. Grether‐Beck, J. Krutmann, and D. Häussinger, “The Osmolyte Strategy of Normal Human Keratinocytes in Maintaining Cell Homeostasis,” Journal of Investigative Dermatology 123, no. 3 (2004): 516–521.
K. Ito, K. Tanaka, Y. Nishibe, J. Hasegawa, and H. Ueno, “GABA‐Synthesizing Enzyme, GAD67, From Dermal Fibroblasts: Evidence for a New Skin Function,” Biochimica et Biophysica Acta (BBA)—General Subjects 1770, no. 2 (2007): 291–296.
H. Zhao, B. Park, M. J. Kim, et al., “The Effect of γ‐Aminobutyric Acid Intake on UVB‐Induced Skin Damage in Hairless Mice,” Biomolecules & Therapeutics 31, no. 6 (2023): 640–647.
L. T. T. Le, B. K. Kim, P. N. Chien, et al., “Investigating the Anti‐Aging Effects of Caviar Oil on Human Skin,” In Vivo 37, no. 5 (2023): 2078–2091.
M. Essendoubi, C. Gobinet, R. Reynaud, J. F. Angiboust, M. Manfait, and O. Piot, “Human Skin Penetration of Hyaluronic Acid of Different Molecular Weights as Probed by Raman Spectroscopy,” Skin Research and Technology 22, no. 1 (2016): 55–62.
S. Gariboldi, M. Palazzo, L. Zanobbio, et al., “Low Molecular Weight Hyaluronic Acid Increases the Self‐Defense of Skin Epithelium by Induction of β‐Defensin 2 via TLR2 and TLR4,” Journal of Immunology 181, no. 3 (2008): 2103–2110.
M. Meunier, A. Scandolera, E. Chapuis, et al., “The Anti‐Wrinkles Properties of Sodium Acetylated Hyaluronate,” Journal of Cosmetic Dermatology 21, no. 7 (2022): 2749–2762.
Y.‐R. Song, W. C. Lim, A. Han, et al., “Rose Petal Extract (Rosa gallica) Exerts Skin Whitening and Anti‐Skin Wrinkle Effects,” Journal of Medicinal Food 23, no. 8 (2020): 870–878.
T. Miura, H. Ichiki, N. Iwamoto, et al., “Antidiabetic Activity of the Rhizoma of Anemarrhena Asphodeloides and Active Components, Mangiferin and Its Glucoside,” Biological and Pharmaceutical Bulletin 24, no. 9 (2001): 1009–1011.
Y. Wang, Y. Dan, D. Yang, et al., “The Genus Anemarrhena Bunge: A Review on Ethnopharmacology, Phytochemistry and Pharmacology,” Journal of Ethnopharmacology 153, no. 1 (2014): 42–60.
A. R. Im, Y. K. Seo, S. H. Cho, K. H. O, K. M. Kim, and S. Chae, “Clinical Evaluation of the Safety and Efficacy of a Timosaponin A‐III‐Based Antiwrinkle Agent Against Skin Aging,” Journal of Cosmetic Dermatology 19, no. 2 (2020): 423–436.
R. Du and T. Lei, “Effects of Autologous Platelet‐Rich Plasma Injections on Facial Skin Rejuvenation,” Experimental and Therapeutic Medicine 19, no. 4 (2020): 3024–3030.
S. Hu, Z. Li, J. Cores, et al., “Needle‐Free Injection of Exosomes Derived From Human Dermal Fibroblast Spheroids Ameliorates Skin Photoaging,” ACS Nano 13, no. 10 (2019): 11273–11282.
J. Molinari, E. Ruszova, V. Velebny, and L. Robert, “Effect of Advanced Glycation Endproducts on Gene Expression Profiles of Human Dermal Fibroblasts,” Biogerontology 9 (2008): 177–182.
L. Rittié, A. Berton, J. C. Monboisse, W. Hornebeck, and P. Gillery, “Decreased Contraction of Glycated Collagen Lattices Coincides With Impaired Matrix Metalloproteinase Production,” Biochemical and Biophysical Research Communications 264, no. 2 (1999): 488–492.
G. B. Fields, “The Rebirth of Matrix Metalloproteinase Inhibitors: Moving Beyond the Dogma,” Cells 8, no. 9 (2019): 984.
E. Hadler‐Olsen, J.‐O. Winberg, and L. Uhlin‐Hansen, “Matrix Metalloproteinases in Cancer: Their Value as Diagnostic and Prognostic Markers and Therapeutic Targets,” Tumor Biology 34 (2013): 2041–2051.
G. S. Butler and C. M. Overall, “Updated Biological Roles for Matrix Metalloproteinases and New “Intracellular” Substrates Revealed by Degradomics,” Biochemistry 48, no. 46 (2009): 10830–10845.
R. P. Beckett and M. Whittaker, “Matrix Metalloproteinase Inhibitors 1998,” Expert Opinion on Therapeutic Patents 8, no. 3 (1998): 259–282.
M. Whittaker, C. D. Floyd, P. Brown, and A. J. H. Gearing, “Design and Therapeutic Application of Matrix Metalloproteinase Inhibitors. (Chem. Rev. 1999, 99, 2735–2776. Published on the Web September 8, 1999),” Chemical Reviews 101, no. 7 (2001): 2205–2206.
J. Martel‐Pelletier, D. J. Welsch, and J.‐P. Pelletier, “Metalloproteases and Inhibitors in Arthritic Diseases,” Best Practice & Research. Clinical Rheumatology 15, no. 5 (2001): 805–829.
P. Burrage and C. Brinckerhoff, “Molecular Targets in Osteoarthritis: Metalloproteinases and Their Inhibitors,” Current Drug Targets 8, no. 2 (2007): 293–303.
S. Chopra, C. M. Overall, and A. Dufour, “Matrix Metalloproteinases in the CNS: Interferons Get Nervous,” Cellular and Molecular Life Sciences 76, no. 16 (2019): 3083–3095.
R. Khokha, A. Murthy, and A. Weiss, “Metalloproteinases and Their Natural Inhibitors in Inflammation and Immunity,” Nature Reviews Immunology 13, no. 9 (2013): 649–665.
M. Gao, T. T. Nguyen, M. A. Suckow, et al., “Acceleration of Diabetic Wound Healing Using a Novel Protease–Anti‐Protease Combination Therapy,” Proceedings of the National Academy of Sciences of the United States of America 112, no. 49 (2015): 15226–15231.
M. P. Caley, V. L. Martins, and E. A. O'Toole, “Metalloproteinases and Wound Healing,” Advances in Wound Care 4, no. 4 (2015): 225–234.
G. B. Fields, “Mechanisms of Action of Novel Drugs Targeting Angiogenesis‐Promoting Matrix Metalloproteinases,” Frontiers in Immunology 10 (2019): 1278.