Journal Home > Volume 11 , Issue 2

Ultraviolet (UV)-induced photoaging skin has become an urgent issue. The functional foods and cosmetics aiming to improve skin photoaging are developing rapidly, and the demand is gradually increasing year by year. Collagen peptides have been proven to display diverse physiological activities, such as excellent moisture retention activity, hygroscopicity, tyrosinase inhibitory activity and antioxidant activity, which indicates that they have great potential in amelioration of UV-induced photoaging. The main objective of this article is to recap the main mechanisms to improve photoaging skin by collagen peptides and their physiological activities in photo-protection. Furthermore, the extraction and structural characteristics of collagen peptides are overviewed. More importantly, some clinical trials on the beneficial effect on skin of collagen peptides are also discussed. In addition, prospects and challenges of collagen peptides are emphatically elucidated in this review. This article implies that collagen peptides have great potential as an effective ingredient in food and cosmetics industry with a wide application prospect.


menu
Abstract
Full text
Outline
About this article

Recent progress in preventive effect of collagen peptides on photoaging skin and action mechanism

Show Author's information Chongyang Lia,bYu Fua,b( )Hongjie Daia,bQiang WangcRuichang GaodYuhao Zhanga,b( )
Key Laboratory of Luminescent and Real-Time Analytical Chemistry, Ministry of Education, College of Food Science, Southwest University, Chongqing 400715, China
Biological Science Research Center, Southwest University, Chongqing 400715, China
Institute of Food Science and Technology, Chinese Academy of Agriculture Sciences/Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Beijing 100193, China
School of Food and Biological Engineering, Jiangsu University, Zhenjiang 212013, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Abstract

Ultraviolet (UV)-induced photoaging skin has become an urgent issue. The functional foods and cosmetics aiming to improve skin photoaging are developing rapidly, and the demand is gradually increasing year by year. Collagen peptides have been proven to display diverse physiological activities, such as excellent moisture retention activity, hygroscopicity, tyrosinase inhibitory activity and antioxidant activity, which indicates that they have great potential in amelioration of UV-induced photoaging. The main objective of this article is to recap the main mechanisms to improve photoaging skin by collagen peptides and their physiological activities in photo-protection. Furthermore, the extraction and structural characteristics of collagen peptides are overviewed. More importantly, some clinical trials on the beneficial effect on skin of collagen peptides are also discussed. In addition, prospects and challenges of collagen peptides are emphatically elucidated in this review. This article implies that collagen peptides have great potential as an effective ingredient in food and cosmetics industry with a wide application prospect.

Keywords: Collagen peptides, Photoprotection, MAPK, TGF-β-Smad, Action mechanism

References(122)

[1]

U. Kusebauch, S.A. Cadamuro, H.J. Musiol, et al., Photocontrolled folding and unfolding of a collagen triple helix, Angew. Chem. Int. Ed. Engl. 45(42) (2006) 7015-7018. https://doi.org/10.1002/anie.200601432.

[2]

Y. Zou, L. Wang, P. Cai, et al., Effect of ultrasound assisted extraction on the physicochemical and functional properties of collagen from softshelled turtle calipash, Int. J. Biol. Macromol. 105(Pt 3) (2017) 1602-1610. https://doi.org/10.1016/j.ijbiomac.2017.03.011.

[3]

G.K. Pal, P.V. Suresh, Sustainable valorisation of seafood by-products: recovery of collagen and development of collagen-based novel functional food ingredients, Innov. Food Sci. Emerg. Technol. 37 (2016) 201-215. https://doi.org/10.1016/j.ifset.2016.03.015.

[4]

Y. Fu, M. Therkildsen, R.E. Aluko, et al., Exploration of collagen recovered from animal by-products as a precursor of bioactive peptides: successes and challenges, Crit. Rev. Food Sci. Nutr. 59(13) (2019) 2011-2027. https://doi.org/10.1080/10408398.2018.1436038.

[5]

A. Kammeyer, R.M. Luiten, Oxidation events and skin aging, Ageing Res. Rev. 21 (2015) 16-29. https://doi.org/10.1016/j.arr.2015.01.001.

[6]

D.J. Tobin, Introduction to skin aging, J. Tissue Viability. 26(1) (2017) 37-46. https://doi.org/10.1016/j.jtv.2016.03.002.

[7]

M. Cavinato, P. Jansen-Durr, Molecular mechanisms of UVB-induced senescence of dermal fibroblasts and its relevance for photoaging of the human skin, Exp. Gerontol. 94 (2017) 78-82. https://doi.org/10.1016/j.exger.2017.01.009.

[8]

C.H. Lee, A. Singla, Y.Y. Lee, Biomedical applications of collagen, Int. J. Pharm. 221 (2001) 1-22. https://doi.org/10.1016/s0378-5173(01)00691-3.

[9]

Y. Na, Research on extraction and properties of antler plate collagen protein, Adv. Eng. Softw. 107 (2017) 197-201. https://doi.org/10.2991/meita-16.2017.42.

[10]

D. Dhakal, P. Koomsap, A. Lamichhane, et al., Optimization of collagen extraction from chicken feet by papain hydrolysis and synthesis of chicken feet collagen based biopolymeric fibres, Food Biosci. 23 (2018) 23-30. https://doi.org/10.1016/j.fbio.2018.03.003.

[11]

Y. Zhang, L. Ma, L. Cai, et al., Effect of combined ultrasonic and alkali pretreatment on enzymatic preparation of angiotensin converting enzyme (ACE) inhibitory peptides from native collagenous materials, Ultrason Sonochem. 36 (2017) 88-94. https://doi.org/10.1016/j.ultsonch.2016.11.008.

[12]

M. Abdollahi, M. Rezaei, A. Jafarpour, et al., Sequential extraction of gel-forming proteins, collagen and collagen hydrolysate from gutted silver carp (Hypophthalmichthys molitrix), a biorefinery approach, Food Chem. 242 (2018) 568-578. https://doi.org/10.1016/j.foodchem.2017.09.045.

[13]

B. Wang, Y.M. Wang, C.F. Chi, et al., Isolation and characterization of collagen and antioxidant collagen peptides from scales of croceine croaker (Pseudosciaena crocea), Mar. Drugs 11(11) (2013) 4641-4661. https://doi.org/10.3390/md11114641.

[14]

Z. Barzideh, A.A. Latiff, C.Y. Gan, et al., Functional properties of collagen hydrolysates from the jellyfish (Chrysaora sp.), Agro. Food Industry Hi. Tech. 25(4) (2014) 27-32.

[15]

J. Lu, H. Hou, Y. Fan, et al., Identification of MMP-1 inhibitory peptides from cod skin gelatin hydrolysates and the inhibition mechanism by MAPK signaling pathway, J. Funct. Foods 33 (2017) 251-260. https://doi.org/10.1016/j.jff.2017.03.049.

[16]

L. Nakchum, S.M. Kim, Preparation of squid skin collagen hydrolysate as an antihyaluronidase, antityrosinase, and antioxidant agent, Prep. Biochem. Biotechnol. 46(2) (2016) 123-130. https://doi.org/10.1080/10826068.2014.9 95808.

[17]

N.M. Sarbon, F. Badii, N.K. Howell, Purification and characterization of antioxidative peptides derived from chicken skin gelatin hydrolysate, Food Hydrocoll. 85 (2018) 311-320. https://doi.org/10.1016/j.foodhyd.2018.06.048.

[18]

X.R. Yang, Y.Q. Zhao, Y.T. Qiu, et al., Preparation and characterization of gelatin and antioxidant peptides from gelatin hydrolysate of skipjack tuna (Katsuwonus pelamis) bone stimulated by in vitro gastrointestinal digestion, Mar. Drugs 17(2) (2019) 78. https://doi.org/10.3390/md17020078.

[19]

H. Song, S. Zhang, L. Zhang, et al., Effect of orally administered collagen peptides from bovine bone on skin aging in chronologically aged mice, Nutrients 9(11) (2017) 1209. https://doi.org/10.3390/nu9111209.

[20]

D. Kim, H. Kim, A. Jang, Anti-oxidative activity and fibroblast cell protection effect of donkey bone hydrolysate against ultraviolet B, Annal. Animal Resour. Sci. 30(2) (2019) 59-68. https://doi.org/10.12718/aars.2019.30.2.59.

[21]

H. Song, M. Meng, X. Cheng, et al., The effect of collagen hydrolysates from silver carp (Hypophthalmichthys molitrix) skin on UV-induced photoaging in mice: molecular weight affects skin repair, Food Funct. 8(4) (2017) 1538-1546. https://doi.org/10.1039/c6fo01397j.

[22]

T. Chen, H. Hou, Y. Fan, et al., Protective effect of gelatin peptides from pacific cod skin against photoaging by inhibiting the expression of MMPs via MAPK signaling pathway, J. Photochem. Photobiol. B 165 (2016) 34-41. https://doi.org/10.1016/j.jphotobiol.2016.10.015.

[23]

E. Mendis, N. Rajapakse, H.G. Byun, et al., Investigation of jumbo squid (Dosidicus gigas) skin gelatin peptides for their in vitro antioxidant effects, Life Sci. 77(17) (2005) 2166-2178. https://doi.org/10.1016/j.lfs.2005.03.016.

[24]

T. Chen, H. Hou, J. Lu, et al., Protective effect of gelatin and gelatin hydrolysate from salmon skin on UV irradiation-induced photoaging of mice skin, J. Ocean Univ. China 15(4) (2016) 711-718. https://doi.org/10.1007/s11802-016-2953-5.

[25]

Y. Zhuang, H. Hou, X. Zhao, et al., Effects of collagen and collagen hydrolysate from jellyfish (Rhopilema esculentum) on mice skin photoaging induced by UV irradiation, J. Food Sci. 74(6) (2009) 183-188. https://doi.org/10.1111/j.1750-3841.2009.01236.x.

[26]

M.F. Chen, Y.Y. Zhang, M. D He, et al., Antioxidant peptide purified from enzymatic hydrolysates of Isochrysis zhanjiangensis and its protective effect against ethanol induced oxidative stress of HepG2 cells, Biotechnol. Bioprocess Eng. 24(2) (2019) 308-317. https://doi.org/10.1007/s12257-018-0391-5.

[27]

Y.W. Li, B. Li, J. He, et al., Structure-activity relationship study of antioxidative peptides by QSAR modeling: the amino acid next to C-terminus affects the activity, J. Pept. Sci. 17(6) (2011) 454-462. https://doi.org/10.1002/psc.1345.

[28]

W. Chen, Y. Hong, Z. Jia, et al., Purification and identification of antioxidant peptides from hydrolysates of large yellow croaker (Pseudosciaena crocea) scales, Trans. ASABE 63(2) (2020) 289-294. https://doi.org/10.13031/trans.13693.

[29]

L. Sun, Y. Zhang, Y. Zhuang, Antiphotoaging effect and purification of an antioxidant peptide from tilapia (Oreochromis niloticus) gelatin peptides, J. Funct. Foods 5(1) (2013) 154-162. https://doi.org/10.1016/j.jff.2012.09.006.

[30]

E. Mendis, N. Rajapakse, S.K. Kim, Antioxidant properties of a radicalscavenging peptide purified from enzymatically prepared fish skin gelatin hydrolysate, J. Agric. Food Chem. 53(3) (2005) 581-587. https://doi.org/10.1021/jf048877v.

[31]

T. Quan, T. He, S. Kang, et al., Solar ultraviolet irradiation reduces collagen in photoaged human skin by blocking transforming growth factor-β type Ⅱ receptor/Smad signaling, Am. J. Pathol. 165(3) (2004) 741-751. https://doi.org/10.1016/s0002-9440(10)63337-8.

[32]

P. Pittayapruek, J. Meephansan, O. Prapapan, et al., Role of matrix metalloproteinases in photoaging and photocarcinogenesis, Int. J. Mol. Sci. 17(6) (2016) 868. https://doi.org/10.3390/ijms17060868.

[33]

H. Tanaka, H. Yamaba, N. Kosugi, et al., Fermentable metabolite of Zymomonas mobilis controls collagen reduction in photoaging skin by improving TGF-β/Smad signaling suppression, Arch. Dermatol. Res. 300(Suppl 1) (2008) S57-S64. https://doi.org/10.1007/s00403-007-0805-2.

[34]

Y.I. Kim, K.S. Kim, H.J. Ahn, et al., Reduced matrix metalloproteinase and collagen transcription mediated by the TGF-β/Smad pathway in passaged normal human dermal fibroblasts, J. Cosmet. Dermatol. 19(5) (2019) 1211-1218. https://doi.org/10.1111/jocd.13114.

[35]

N.S. Bora, B. Mazumder, S. Mandal, et al., Amelioration of UV radiationinduced photoaging by a combinational sunscreen formulation via aversion of oxidative collagen degradation and promotion of TGF-β-Smadmediated collagen production, Eur. J. Pharm. Sci. 127 (2019) 261-275. https://doi.org/10.1016/j.ejps.2018.11.004.

[36]

B. Park, E. Hwang, S.A. Seo, et al., Dietary Rosa damascena protects against UVB-induced skin aging by improving collagen synthesis via MMPs reduction through alterations of c-Jun and c-Fos and TGF-β1 stimulation mediated Smad2/3 and Smad7, J. Functi. Foods 36 (2017) 480-489. https://doi.org/10.1016/j.jff.2017.07.028.

[37]

J. Venkatesan, S. Anil, S.K. Kim, et al., Marine fish proteins and peptides for cosmeceuticals: a review, Marine Drugs 15(5) (2017) 143. https://doi.org/10.3390/md15050143.

[38]

D. Singh, S.K. Srivastava, T.K. Chaudhuri, et al., Multifaceted role of matrix metalloproteinases (MMPs), Front. Mol. Biosci. 2 (2015) 19. https://doi.org/10.3389/fmolb.2015.00019.

[39]

R.P. Verma, C. Hansch, Matrix metalloproteinases (MMPs): chemicalbiological functions and (Q)SARs, Bioorganic Med. Chem. Lett. 15(6) (2007) 2223-2268. https://doi.org/10.1016/j.bmc.2007.01.011.

[40]

H. Nagase, R. Visse, G. Murphy, Structure and function of matrix metalloproteinases and TIMPs, Cardiovasc. Res. 69(3) (2006) 562-573. https://doi.org/10.1016/j.cardiores.2005.12.002.

[41]

S.H. Choi, S.I. Choi, T.D. Jung, et al., Anti-photoaging effect of jeju putgyul (unripe citrus) extracts on human dermal fibroblasts and ultraviolet B-induced hairless mouse skin, Int. J. Mol. Sci. 18(10) (2017). https://doi.org/10.3390/ijms18102052.

[42]

K. Tanaka, J. Hasegawa, K. Asamitsu, et al., Magnolia ovovata extract and its active component magnolol prevent skin photoaging via inhibition of nuclear factor κB, Eur. J. Pharmacol. 565(1/3) (2007) 212-219. https://doi.org/10.1016/j.ejphar.2007.01.095.

[43]

J.H. Oh, A. Kim, J.M. Park, et al., Ultraviolet B-induced matrix metalloproteinase-1 and -3 secretions are mediated via PTEN/Akt pathway in human dermal fibroblasts, J. Cell Physiol. 209(3) (2006) 775-785. https://doi.org/10.1002/jcp.20754.

[44]

H. Kaddurah, T.L. Braunberger, G. Vellaichamy, et al., The impact of sunlight on skin aging, Current Geriatr. Rep. 7(4) (2018) 228-237. https://doi.org/10.1007/s13670-018-0262-0.

[45]

N.R. Moon, S. Kang, S. Park, Consumption of ellagic acid and dihydromyricetin synergistically protects against UV-B induced photoaging, possibly by activating both TGF-β1 and Wnt signaling pathways, J. Photochem. Photobiol. B Biol. 178 (2018) 92-100. https://doi.org/10.1016/j.jphotobiol.2017.11.004.

[46]

X. Xu, H.Y. Wang, Y. Zhang, et al., Adipose-derived stem cells cooperate with fractional carbon dioxide laser in antagonizing photoaging a potential role of Wnt and β-catenin signaling, Cell Biosci. 4 (2014) 24-34. https://doi.org/10.1186/2045-3701-4-24.

[47]

T. Shen, K. Gao, Z. Hu, et al., Ciliary mechanism of regulating hedgehog and Wnt/β-catenin signaling modulates ultraviolet B irradiation-induced photodamage in HaCaT cells, J. Biomed. Nanotechnol. 15(1) (2019) 196-203. https://doi.org/10.1166/jbn.2019.2664.

[48]

S.A. Koppes, P. Kemperman, I. Van Tilburg, et al., Determination of natural moisturizing factors in the skin: Raman microspectroscopy versus HPLC, Biomarkers 22(6) (2017) 502-507. https://doi.org/10.1080/135475 0X.2016.1256428.

[49]

D.R. Hoffman, L.M. Kroll, A. Basehoar, et al., Immediate and extended effects of abrasion on stratum corneum natural moisturizing factor, Skin Res. Technol. 21(3) (2015) 366-372. https://doi.org/10.1111/srt.12201.

[50]

J. Fowler, Understanding the role of natural moisturizing factor in skin hydration, Practical Dermatol. 9 (2012) 36-40.

[51]

S. Wu, H. Kang, Advances in research and application of fish scale collagen, Agric. Sci. Technol. 18(12) (2017) 2543-2546;2553.

[52]

P.H. Li, W.C. Lu, Y.J. Chan, et al., Extraction and characterization of collagen from sea cucumber (Holothuria cinerascens) and its potential application in moisturizing cosmetics, Aquaculture 515 (2020) 734590. https://doi.org/10.1016/j.aquaculture.2019.734590.

[53]

H. Hou, B. Li, Z. Zhang, et al., Moisture absorption and retention properties, and activity in alleviating skin photodamage of collagen polypeptide from marine fish skin, Food Chem. 135(3) (2012) 1432-1439. https://doi.org/10.1016/j.foodchem.2012.06.009.

[54]

C. Oba, H. Ohara, M. Morifuji, et al., Collagen hydrolysate intake improves the loss of epidermal barrier function and skin elasticity induced by UVB irradiation in hairless mice, Photodermatol. Photoimmunol. Photomed. 29 (2013) 204-211.

[55]

M. Kang, S. Yumnam, S. Kim, Oral intake of collagen peptide attenuates ultraviolet B irradiation-induced skin dehydration in vivo by regulating hyaluronic acid synthesis, Int. J. Mol. Sci. 19(11) (2018) 3551. https://doi.org/10.3390/ijms19113551.

[56]

S.N.A. Bukhari, N.L. Roswandi, M. Waqas, et al., Hyaluronic acid, a promising skin rejuvenating biomedicine: a review of recent updates and pre-clinical and clinical investigations on cosmetic and nutricosmetic effects, Int. J. Biol. Macromol. 120(Pt B) (2018) 1682-1695. https://doi.org/10.1016/j.ijbiomac.2018.09.188.

[57]

G.A. Gbogouri, M. Linder, J. Fanni, et al., Influence of hydrolysis degree on the functional properties of salmon byproducts hydrolysates, J. Food Sci. 69(8) (2004) 615-622. https://doi.org/10.1111/j.1365-2621.2004.tb09909.x.

[58]

H. Qi, N. Li, X. Zhao, et al., Physicochemical properties and the radical scavenging capacities of pepsin-solubilized collagen from the body wall of starfish (Asterina pectinifera), J. Aquat. Food Prod. T. 26(4) (2016) 376-389. https://doi.org/10.1080/10498850.2016.1186768.

[59]

B.W. Zhu, XP. Dong, D.Y. Zhou, et al., Physicochemical properties and radical scavenging capacities of pepsin-solubilized collagen from sea cucumber Stichopus japonicus, Food Hydrocoll. 28(1) (2012) 182-188. https://doi.org/10.1016/j.foodhyd.2011.12.010.

[60]

Y. Tang, S. Jin, X. Li, et al., Physicochemical properties and biocompatibility evaluation of collagen from the skin of giant croaker (Nibea japonica), Mar. Drugs 16(7) (2018) 222. https://doi.org/10.3390/md16070222.

[61]

M. Brenner, V.J. Hearing, The protective role of melanin against UV damage in human skin, Photochem. Photobiol. 84(3) (2008) 539-549. https://doi.org/10.1111/j.1751-1097.2007.00226.x.

[62]

P. Prakot, N. Chaitanawisuti, P. Sangtanoo, et al., Inhibitory activities of protein hydrolysates from spotted babylon snails on tyrosinase and melanogenesis, J. Aquat. Food Prod. T. 27(7) (2018) 811-829. https://doi.org/10.1080/10498850.2018.1499687.

[63]

M. Schurink, W.J. van Berkel, H.J. Wichers, et al., Novel peptides with tyrosinase inhibitory activity, Peptides 28(3) (2007) 485-495. https://doi.org/10.1016/j.peptides.2006.11.023.

[64]

J. Chen, L. Li, R. Yi, et al., Extraction and characterization of acid-soluble collagen from scales and skin of tilapia (Oreochromis niloticus), LWT-Food Sci. Technol. 66 (2016) 453-459. https://doi.org/10.1016/j.lwt.2015.10.070.

[65]

H. Niu, Z. Wang, H. Hou, et al., Protective effect of cod (Gadus macrocephalus) skin collagen peptides on acetic acid-induced gastric ulcer in rats, J. Food Sci. 81(7) (2016) H1807-H1815. https://doi.org/10.1111/1750- 3841.13332.

[66]

Y. Zhuang, L. Sun, X. Zhao, et al., Antioxidant and melanogenesis-inhibitory activities of collagen peptide from jellyfish (Rhopilema esculentum), J. Sci. Food Agric. 89(10) (2009) 1722-1727. https://doi.org/10.1002/jsfa.3645.

[67]

H. Hou, X. Zhao, B.F. Li, et al., Inhibition of melanogenic activity by gelatin and polypeptides from pacific cod skin in B16 melanoma cells, J. Food Biochem. 35(4) (2011) 1099-1116. https://doi.org/10.1111/j.1745- 4514.2010.00437.x.

[68]

G.P. Hong, S.G. Min, Y.J. Jo, Anti-oxidative and anti-aging activities of porcine by-product collagen hydrolysates produced by commercial proteases: effect of hydrolysis and ultrafiltration, Molecules 24(6) (2019) 1104. https://doi.org/10.3390/molecules24061104.

[69]

J. Wang, Y. Wang, Q. Tang, et al., Antioxidation activities of low-molecularweight gelatin hydrolysate isolated from the sea cucumber Stichopus japonicus, J. Ocean Univ. China 9(1) (2010) 94-98. https://doi.org/10.1007/s11802-010-0094-9.

[70]

Y.P. Chen, H.T. Wu, G.H. Wang, et al., Improvement of skin condition on skin moisture and anti-melanogenesis by collagen peptides from milkfish (Chanos chanos) scales, Mater. Sci. Eng. R Rep. 382 (2018) 022067. https://doi.org/10.1088/1757-899x/382/2/022067.

[71]

S.H. Park, Y.J. Jo, Static hydrothermal processing and fractionation for production of a collagen peptide with anti-oxidative and anti-aging properties, Process Biochem. 83 (2019) 176-182. https://doi.org/10.1016/j.procbio.2019.05.015.

[72]

S.A. D'Mello, G.J. Finlay, B.C. Baguley, et al., Signaling pathways in melanogenesis, Int. J. Mol. Sci. 17(7) (2016) 1144. https://doi.org/10.3390/ijms17071144.

[73]

J.K. Chae, L. Subedi, M. Jeong, et al., Gomisin N inhibits melanogenesis through regulating the PI3K/Akt and MAPK/ERK signaling pathways in melanocytes, Int. J. Mol. Sci. 18(2) (2017) 471-484. https://doi.org/10.3390/ijms18020471.

[74]

L. Cai, X. Wu, Y. Zhang, et al., Purification and characterization of three antioxidant peptides from protein hydrolysate of grass carp (Ctenopharyngodon idella) skin, J. Funct. Foods 16 (2015) 234-242. https://doi.org/10.1016/j.jff.2015.04.042.

[75]

O. Abdelhedi, R. Nasri, L. Mora, et al., Collagenous proteins from black-barred halfbeak skin as a source of gelatin and bioactive peptides, Food Hydrocoll. 70 (2017) 123-133. https://doi.org/10.1016/j.foodhyd.2017.03.030.

[76]

H.M. Chen, K. Muramoto, F. Yamauchi, et al., Antioxidative properties of histidine-containing peptides designed from peptide fragments found in the digests of a soybean protein, J. Agric. Food Chem. 46(1) (1998) 49-53. https://doi.org/10.1021/jf970649w.

[77]

C.F. Chi, Z.H. Cao, B. Wang, et al., Antioxidant and functional properties of collagen hydrolysates from Spanish mackerel skin as influenced by average molecular weight, Molecules 19(8) (2014) 11211-11230. https://doi.org/10.3390/molecules190811211.

[78]

Z. Li, B. Wang, C. Chi, et al., Influence of average molecular weight on antioxidant and functional properties of cartilage collagen hydrolysates from Sphyrna lewini, Dasyatis akjei and Raja porosa, Food Res. Int. 51(1) (2013) 283-293. https://doi.org/10.1016/j.foodres.2012.12.031.

[79]

H.C. Wu, H.M. Chen, C.Y. Shiau, Free amino acids and peptides as related to antioxidant properties in protein hydrolysates of mackerel (Scomber austriasicus), Food Res. Int. 36(9-10) (2003) 949-957. https://doi.org/10.1016/s0963-9969(03)00104-2.

[80]

D. Ding, B. Du, C. Zhang, et al., Isolation and identification of an antioxidant collagen peptide from skipjack tuna (Katsuwonus pelamis) bone, RSC Advances 9(46) (2019) 27032-27041. https://doi.org/10.1039/c9ra04665h.

[81]

C.F. Chi, B. Wang, Y.M. Wang, et al., Isolation and characterization of three antioxidant peptides from protein hydrolysate of bluefin leatherjacket (Navodon septentrionalis) heads, J. Funct. Foods 12 (2015) 1-10. https://doi.org/10.1016/j.jff.2014.10.027.

[82]

S. Bousopha, S. Nalinanon, C. Sriket, Production of collagen hydrolysate with antioxidant activity from pharaoh cuttlefish skin, Chiang Mai Univ. J. Nat. Sci. 15(2) (2016) 151-162. https://doi.org/10.12982/cmujns.2016.00012.

[83]

Y. Wu, J. Wang, L. Li, et al., Purification and identification of an antioxidant peptide from Pinctada fucata muscle, CyTA-J. Food 16(1) (2017) 11-19. https://doi.org/10.1080/19476337.2017.1332099.

[84]

H.X. Jin, H.P. Xu, Y. Li, et al., Preparation and evaluation of peptides with potential antioxidant activity by microwave assisted enzymatic hydrolysis of collagen from sea cucumber Acaudina molpadioides obtained from Zhejiang province in China, Mar. Drugs 17(3) (2019) 169. https://doi.org/10.3390/md17030169.

[85]

L. Wattanasiritham, C. Theerakulkait, S. Wickramasekara, et al., Isolation and identification of antioxidant peptides from enzymatically hydrolyzed rice bran protein, Food Chem. 192 (2016) 156-162. https://doi.org/10.1016/j.foodchem.2015.06.057.

[86]

L. Sun, W. Chang, Q. Ma, et al., Purification of antioxidant peptides by high resolution mass spectrometry from simulated gastrointestinal digestion hydrolysates of alaska pollock (Theragra chalcogramma) skin collagen, Mar. Drugs 14(10) (2016) 186. https://doi.org/10.3390/md14100186.

[87]

Q. Liang, L. Wang, Y. He, et al., Hydrolysis kinetics and antioxidant activity of collagen under simulated gastrointestinal digestion, J. Funct. Foods 11 (2014) 493-499. https://doi.org/10.1016/j.jff.2014.08.004.

[88]

W. Weng, L. Tang, B. Wang, et al., Antioxidant properties of fractions isolated from blue shark (Prionace glauca) skin gelatin hydrolysates, J. Funct. Foods 11 (2014) 342-351. https://doi.org/10.1016/j.jff.2014.10.021.

[89]

Y.T. Qiu, Y.M. Wang, X.R. Yang, et al., Gelatin and antioxidant peptides from gelatin hydrolysate of skipjack tuna (Katsuwonus pelamis) scales: preparation, identification and activity evaluation, Mar. Drugs 17(10) (2019) 565. https://doi.org/10.3390/md17100565.

[90]

Y. Zhang, X. Duan, Y. Zhuang, Purification and characterization of novel antioxidant peptides from enzymatic hydrolysates of tilapia (Oreochromis niloticus) skin gelatin, Peptides 38(1) (2012) 13-21. https://doi.org/10.1016/j.peptides.2012.08.014.

[91]

J.F. Ding, Y.Y. Li, J.J. Xu, et al., Study on effect of jellyfish collagen hydrolysate on anti-fatigue and anti-oxidation, Food Hydrocoll. 25(5) (2011) 1350-1353. https://doi.org/10.1016/j.foodhyd.2010.12.013.

[92]

Z. Wang, Q. Wang, L. Wang, et al., Improvement of skin condition by oral administration of collagen hydrolysates in chronologically aged mice, J. Sci. Food Agri. 97(9) (2017) 2721-2726. https://doi.org/10.1002/jsfa.8098.

[93]

J. Tao, Y.Q. Zhao, C.F. Chi, et al., Bioactive peptides from cartilage protein hydrolysate of spotless smoothhound and their antioxidant activity in vitro, Mar. Drugs 16(4) (2018) 100. https://doi.org/10.3390/md16040100.

[94]

L. Zhang, Y. Zheng, X. Cheng, et al., The anti-photoaging effect of antioxidant collagen peptides from silver carp (Hypophthalmichthys molitrix) skin is preferable to tea polyphenols and casein peptides, Food Funct. 8(4) (2017) 1698-1707. https://doi.org/10.1039/c6fo01499b.

[95]

H.B. Pyun, M. Kim, J. Park, et al., Effects of collagen tripeptide supplement on photoaging and epidermal skin barrier in UVB-exposed hairless mice, Prev. Nutr. Food Sci. 17(4) (2012) 245-253. https://doi.org/10.3746/pnf.2012.17.4.245.

[96]

S. Sibilla, M. Godfrey, S. Brewer, et al., An overview of the beneficial effects of hydrolysed collagen as a nutraceutical on skin properties, scientific background and clinical studies, Open Nutraceuticals J. 8 (2015) 29-42.

[97]

J. Fan, Y. Zhuang, B. Li, Effects of collagen and collagen hydrolysate from jellyfish umbrella on histological and immunity changes of mice photoaging, Nutrients 5(1) (2013) 223-233. https://doi.org/10.3390/nu5010223.

[98]

T. Chen, H. Hou, Protective effect of gelatin polypeptides from Pacific cod (Gadus macrocephalus) against UV irradiation-induced damages by inhibiting inflammation and improving transforming growth factor-beta/Smad signaling pathway, J. Photochem. Photobiol. B. 162 (2016) 633-640. https://doi.org/10.1016/j.jphotobiol.2016.07.038.

[99]

C.A. Lopez-Morales, S. Vazquez-Leyva, L. Vallejo-Castillo, et al., Determination of peptide profile consistency and safety of collagen hydrolysates as quality attributes, J. Food Sci. 84(3) (2019) 430-439. https://doi.org/10.1111/1750-3841.14466.

[100]

J. Liang, X.R. Pei, Z.F. Zhang, et al., A chronic oral toxicity study of marine collagen peptides preparation from chum salmon (Oncorhynchus keta) skin using Sprague-Dawley rat, Mar. Drugs 10(1) (2012) 20-34. https://doi.org/10.3390/md10010020.

[101]

S. Benjakul, S. Karnjanapratum, W. Visessanguan, Hydrolysed collagen from Lates calcarifer skin: its acute toxicity and impact on cell proliferation and collagen production of fibroblasts, Int. J. Food Sci. Tech. 53(8) (2018) 1871-1879. https://doi.org/10.1111/ijfs.13772.

[102]

D.U. Kim, H.C. Chung, J. Choi, et al., Oral intake of low-molecular-weight collagen peptide improves hydration, elasticity, and wrinkling in human skin: a randomized, double-blind, placebo-controlled study, Nutrients 10(7) (2018) 826. https://doi.org/10.3390/nu10070826.

[103]

K. Iwai, T. Hasegawa, Y. Taguchi, et al., Identification of food-derived collagen peptides in human blood after oral ingestion of gelatin hydrolysates, J. Agric. Food Chem. 53(16) (2005) 6531-6536. https://doi.org/10.1021/jf050206p.

[104]

H. Ohara, H. Matsumoto, K. Ito, et al., Comparison of quantity and structures of hydroxyproline-containing peptides in human blood after oral ingestion of gelatin hydrolysates from different sources, J. Agric. Food Chem. 55(4) (2007) 1532-1535. https://doi.org/10.1021/JF062834S.

[105]

L. Wang, Q. Wang, Q. Liang, et al., Determination of bioavailability and identification of collagen peptide in blood after oral ingestion of gelatin, J. Sci. Food Agric. 95 (13) (2015) 2712-2717. https://doi.org/10.1002/jsfa.7008.

[106]

S. Oesser, M. Adam, W. Babel, et al., Oral administration of 14C labeled gelatin hydrolysate leads to an accumulation of radioactivity in cartilage of mice (C57/BL), J. Nutr. 129(10) (1999) 1891-1895. https://doi.org/10.1093/jn/129.10.1891.

[107]

L. Wang, Q. Wang, J. Qian, et al., Bioavailability and bioavailable forms of collagen after oral administration to rats, J. Agric. Food Chem. 63(14) (2015) 3752-3756. https://doi.org/10.1021/jf5057502.

[108]

M. Watanabe-Kamiyama, M. Shimizu, S. Kamiyama, et al., Absorption and effectiveness of orally administered low molecular weight collagen hydrolysate in rats, J. Agric. Food Chem. 58(2) (2010) 835-841. https://doi.org/10.1021/jf9031487.

[109]

M. Yazaki, Y. Ito, M. Yamada, et al., Oral ingestion of collagen hydrolysate leads to the transportation of highly concentrated Gly-Pro-Hyp and its hydrolyzed form of Pro-Hyp into the bloodstream and skin, J. Agric. Food Chem. 65(11) (2017) 2315-2322. https://doi.org/10.1021/acs.jafc.6b05679.

[110]

H. Ohara, S. Ichikawa, H. Matsumoto, et al., Collagen-derived dipeptide, proline-hydroxyproline, stimulates cell proliferation and hyaluronic acid synthesis in cultured human dermal fibroblasts, J. Dermatol. 37(4) (2010) 330-338. https://doi.org/10.1111/j.1346-8138.2010.00827.x.

[111]

Y. Shigemura, K. Iwai, F. Morimatsu, et al., Effect of prolyl-hydroxyproline (Pro-Hyp), a food-derived collagen peptide in human blood, on growth of fibroblasts from mouse skin, J. Agric. Food Chem. 57(2) (2009) 444-449. https://doi.org/10.1021/jf802785h.

[112]

Z. Xiao, P. Liang, J. Chen, et al., A peptide YGDEY from tilapia gelatin hydrolysates inhibits UVB-mediated skin photoaging by regulating MMP-1 and MMP-9 expression in HaCaT cells, Photochem. Photobiol. 95(6) (2019) 1424-1432. https://doi.org/10.1111/php.13135.

[113]

J. Chen, P. Liang, Z. Xiao, et al., Antiphotoaging effect of boiled abalone residual peptide ATPGDEG on UVB-induced keratinocyte HaCaT cells, Food Nutr. Res. 63 (2019). https://doi.org/10.29219/fnr.v63.3508.

[114]

Q. Ma, Q. Liu, L. Yuan, et al., Protective effects of LSGYGP from fish skin gelatin hydrolysates on UVB-induced MEFs by regulation of oxidative stress and matrix metalloproteinase activity, Nutrients 10(4) (2018) 420. https://doi.org/10.3390/nu10040420.

[115]

J.S. Kim, D. Kim, H.J. Kim, et al., Protection effect of donkey hide gelatin hydrolysates on UVB-induced photoaging of human skin fibroblasts, Process Biochem. 67 (2018) 118-126. https://doi.org/10.1016/j.procbio.2018.02.004.

[116]

N. Inoue, F. Sugihara, X. Wang, Ingestion of bioactive collagen hydrolysates enhance facial skin moisture and elasticity and reduce facial ageing signs in a randomised double-blind placebo-controlled clinical study, J. Sci. Food Agric. 96(12) (2016) 4077-4081. https://doi.org/10.1002/jsfa.7606.

[117]

E. Proksch, D. Segger, J. Degwert, et al., Oral supplementation of specific collagen peptides has beneficial effects on human skin physiology: a doubleblind, placebo-controlled study, Skin Pharmacol. Physiol. 27(1) (2014) 47-55. https://doi.org/10.1159/000351376.

[118]

A. Czajka, E.M. Kania, L. Genovese, et al., Daily oral supplementation with collagen peptides combined with vitamins and other bioactive compounds improves skin elasticity and has a beneficial effect on joint and general wellbeing, Nutr. Res. 57 (2018) 97-108. https://doi.org/10.1016/j.nutres.2018.06.001.

[119]

L. Genovese, A. Corbo, S. Sibilla, An insight into the changes in skin texture and properties following dietary intervention with a nutricosmeceutical containing a blend of collagen bioactive peptides and antioxidants, Skin Pharmacol. Physiol. 30(3) (2017) 146-158. https://doi.org/10.1159/000464470.

[120]

S.R. Schwartz, J. Park, Ingestion of BioCell collagen (R), a novel hydrolyzed chicken sternal cartilage extract, enhanced blood microcirculation and reduced facial aging signs, Clin. Interv. Aging 7 (2012) 267-273. https://doi.org/10.2147/CIA.S32836.

[121]

X. Wang, H. Hong, J. Wu, Hen collagen hydrolysate alleviates UVA-induced damage in human dermal fibroblasts, J. Funct. Foods 63 (2019) 103574. https://doi.org/10.1016/j.jff.2019.103574.

[122]

M. Offengenden, S. Chakrabarti, J. Wu, Chicken collagen hydrolysates differentially mediate anti-inflammatory activity and type I collagen synthesis on human dermal fibroblasts, Food Sci. Human Wellness 7 (2) (2018) 138-147. https://doi.org/10.1016/j.fshw.2018.02.002.

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 13 March 2020
Revised: 07 October 2020
Accepted: 18 October 2020
Published: 25 November 2021
Issue date: March 2022

Copyright

© 2022 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.

Acknowledgements

This work was financially supported by National Key R&D Program of China (No. 2016YFD0400200), National Natural Science Foundation of China (No. 31972102, 31671881, and 31901683), Chongqing Research Program of Basic Research and Frontier Technology (No. cstc2018jcyjA0939), Chongqing Technology Innovation and Application Demonstration Project (No. cstc2018jscx-msybX0204), Fundamental Research Funds for the Central Universities (No. XDJK2019B028), Innovation Program for Chongqing's Overseas Returnees (cx2019072), and Fundamental Research Funds for the Central Universities, China (SWU 019009).

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return