Journal Home > Volume 7 , Issue 2
Food Science and Human Wellness 2018, 7(2): 138-147 https://doi.org/10.1016/j.fshw.2018.02.002
Research Article | Open Access | Issue | Published: 24 February 2018

Chicken collagen hydrolysates differentially mediate anti-inflammatory activity and type I collagen synthesis on human dermal fibroblasts

Show Author's Information Marina Offengenden1,  Subhadeep Chakrabarti1,  Jianping Wu( )
Department of Agricultural, Food & Nutritional Science and the Cardiovascular Research Centre, University of Alberta, Edmonton, AB, Canada

1 Both authors contributed equally.

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

Keywords:
Antioxidant activity, Collagen peptides, Chicken collagen, Anti-inflammatory activity, Human dermal fibroblasts
Cite this article:
Offengenden M, Chakrabarti S, Wu J. Chicken collagen hydrolysates differentially mediate anti-inflammatory activity and type I collagen synthesis on human dermal fibroblasts. Food Science and Human Wellness, 2018, 7(2): 138-147. https://doi.org/10.1016/j.fshw.2018.02.002
Download citation
EndNote(RIS)
BibTeX

389

Views

9

Downloads

Citations

46

Crossref

N/A

WoS

47

Scopus

0

CSCD

Abstract Full text About this article

Collagen is a major extracellular matrix protein. Given the potential anti-inflammatory and antioxidant profiles of these bioactive compounds, there has been increasing interest in using collagen derived peptides and peptide-rich collagen hydrolysates for skin health, due to their immunomodulatory, antioxidant and proliferative effects on dermal fibroblasts. However, all hydrolysates are not equally effective in exerting the beneficial effects; hence, further research is needed to determine the factors that improve the therapeutic applicability of such preparations. We used different enzymatic conditions to generate a number of different collagen hydrolysates with distinct peptide profiles. We found that the use of two rather than one enzyme for hydrolysis generates a greater abundance of low molecular weight peptides with consequent improvement in bioactive properties. Testing these hydrolysates on human dermal fibroblasts showed distinct actions on inflammatory changes, oxidative stress, type I collagen synthesis and cellular proliferation. Our findings suggest that different enzymatic conditions affect the peptide profile of hydrolysates and differentially regulate their biological activities and potential protective responses on dermal fibroblasts.


menu
Abstract
Full text
Outline
About this article

Chicken collagen hydrolysates differentially mediate anti-inflammatory activity and type I collagen synthesis on human dermal fibroblasts

Show Author's information Marina Offengenden1, Subhadeep Chakrabarti1, Jianping Wu( )
Department of Agricultural, Food & Nutritional Science and the Cardiovascular Research Centre, University of Alberta, Edmonton, AB, Canada

1 Both authors contributed equally.

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

Abstract

Collagen is a major extracellular matrix protein. Given the potential anti-inflammatory and antioxidant profiles of these bioactive compounds, there has been increasing interest in using collagen derived peptides and peptide-rich collagen hydrolysates for skin health, due to their immunomodulatory, antioxidant and proliferative effects on dermal fibroblasts. However, all hydrolysates are not equally effective in exerting the beneficial effects; hence, further research is needed to determine the factors that improve the therapeutic applicability of such preparations. We used different enzymatic conditions to generate a number of different collagen hydrolysates with distinct peptide profiles. We found that the use of two rather than one enzyme for hydrolysis generates a greater abundance of low molecular weight peptides with consequent improvement in bioactive properties. Testing these hydrolysates on human dermal fibroblasts showed distinct actions on inflammatory changes, oxidative stress, type I collagen synthesis and cellular proliferation. Our findings suggest that different enzymatic conditions affect the peptide profile of hydrolysates and differentially regulate their biological activities and potential protective responses on dermal fibroblasts.

Keywords: Antioxidant activity, Collagen peptides, Chicken collagen, Anti-inflammatory activity, Human dermal fibroblasts

References(54)

[1]

M.C. Gomez-Guillen, B. Gimenez, M.E. Lopez-Caballero, M.P. Montero, Functional and bioactive properties of collagen and gelatin from alternative sources: a review, Food Hydrocolloids 25 (8) (2011) 1813-1827.
DOI Google Scholar
[2]

H. Ohara, H. Iida, K. Ito, Y. Takeuchi, Y. Nomura, Effects of Pro-Hyp, a collagen hydrolysate-derived peptide, on hyaluronic acid synthesis using in vitro cultured synovium cells and oral ingestion of collagen hydrolysates in a guinea pig model of osteoarthritis, Biosci. Biotechnol. Biochem. 74 (10) (2010) 2096-2099.
DOI Google Scholar
[3]

A. Saiga, K. Iwai, T. Hayakawa, Y. Takahata, S. Kitamura, T. Nishimura, et al., Angiotensin I-converting enzyme-inhibitory peptides obtained from chicken collagen hydrolysate, J. Agric. Food Chem. 56 (20) (2008) 9586-9591.
DOI Google Scholar
[4]

Y. Zhang, T. Kouguchi, K. Shimizu, M. Sato, Y. Takahata, F. Morimatsu, Chicken collagen hydrolysate reduces proinflammatory cytokine production in C57BL/6: KOR-ApoEshl mice, J. Nutr. Sci. Vitaminol. (Tokyo) 56 (3) (2010) 208-210.
DOI Google Scholar
[5]

J. Ao, B. Li, Amino acid composition and antioxidant activities of hydrolysates and peptide fractions from porcine collagen, Food Sci. Technol. Int. 18 (5) (2012) 425-434.
DOI Google Scholar
[6]

E. Mendis, N. Rajapakse, S.K. Kim, Antioxidant properties of a radical-scavenging peptide purified from enzymatically prepared fish skin gelatin hydrolysate, J. Agric. Food Chem. 53 (3) (2005) 581-587.
DOI Google Scholar
[7]

Y. Nomura, K. Oohashi, M. Watanabe, S. Kasugai, Increase in bone mineral density through oral administration of shark gelatin to ovariectomized rats, Nutrition 21 (11–12) (2005) 1120-1126.
DOI Google Scholar
[8]

Y. Wang, C.L. Zhang, Q. Zhang, P. Li, Composite electrospun nanomembranes of fish scale collagen peptides/chito-oligosaccharides: antibacterial properties and potential for wound dressing, Int. J. Nanomed. 6 (2011) 667-676.
DOI Google Scholar
[9]

R.W. Moskowitz, Role of collagen hydrolysate in bone and joint disease, Semin. Arthritis Rheum. 30 (2) (2000) 87-99.
DOI Google Scholar
[10]

G.Y. Li, S. Fukunaga, K. Takenouchi, F. Nakamura, Comparative study of the physiological properties of collagen, gelatin and collagen hydrolysate as cosmetic materials, Int. J. Cosmet. Sci. 27 (2) (2005) 101-106.
DOI Google Scholar
[11]

M. Faria, E.L. da Costa, J.A. Gontijo, F.M. Netto, Evaluation of the hypotensive potential of bovine and porcine collagen hydrolysates, J. Med. Food 11 (3) (2008) 560-567.
DOI Google Scholar
[12]

S. Oesser, J. Seifert, Stimulation of type II collagen biosynthesis and secretion in bovine chondrocytes cultured with degraded collagen, Cell Tissue Res. 311 (3) (2003) 393-399.
DOI Google Scholar
[13]

L. Boudjennah, V. Dalet-Fumeron, M. Pagano, Expression of collagenase/gelatinase activity from basement-membrane fibronectin–isolation after limited proteolysis of a bovine lens capsule and molecular definition of this thiol-dependent zinc metalloproteinase, Eur. J. Biochem. 255 (1) (1998) 46-54.
DOI Google Scholar
[14]

K.H. Leem, S. Lee, A. Jang, H.K. Kim, Porcine skin gelatin hydrolysate promotes longitudinal bone growth in adolescent rats, J. Med. Food 16 (5) (2013) 447-453.
DOI Google Scholar
[15]

Y. Zhang, T. Kouguchi, M. Shimizu, T. Ohmori, Y. Takahata, F. Morimatsu, Chicken collagen hydrolysate protects rats from hypertension and cardiovascular damage, J. Med. Food 13 (2) (2010) 399-405.
DOI Google Scholar
[16]

T. Kouguchi, T. Ohmori, M. Shimizu, Y. Takahata, Y. Maeyama, T. Suzuki, et al., Effects of a chicken collagen hydrolysate on the circulation system in subjects with mild hypertension or high-normal blood pressure, Biosci. Biotechnol. Biochem. 77 (4) (2013) 691-696.
DOI Google Scholar
[17]

A. Saiga-Egusa, K. Iwai, T. Hayakawa, Y. Takahata, F. Morimatsu, Antihypertensive effects and endothelial progenitor cell activation by intake of chicken collagen hydrolysate in pre- and mild-hypertension, Biosci. Biotechnol. Biochem. 73 (2) (2009) 422-424.
DOI Google Scholar
[18]

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.
DOI Google Scholar
[19]

J. Liang, X. Pei, Z. Zhang, N. Wang, J. Wang, Y. Li, The protective effects of long-term oral administration of marine collagen hydrolysate from chum salmon on collagen matrix homeostasis in the chronological aged skin of Sprague-Dawley male rats, J. Food Sci. 75 (8) (2010) H230-H238.
DOI Google Scholar
[20]

A. Firooz, F. Gorouhi, P. Davari, M. Atarod, S. Hekmat, M. Rashighi-Firoozabadi, et al., Comparison of hydration, sebum and pH values in clinically normal skin of patients with atopic dermatitis and healthy controls, Clin. Exp. Dermatol. 32 (3) (2007) 321-322.
DOI Google Scholar
[21]

C. Oresajo, S. Pillai, M. Manco, M. Yatskayer, D. McDaniel, Antioxidants and the skin: understanding formulation and efficacy, Dermatol. Ther. 25 (3) (2012) 252-259.
DOI Google Scholar
[22]

J. Doles, M. Storer, L. Cozzuto, G. Roma, W.M. Keyes, Age-associated inflammation inhibits epidermal stem cell function, Gene Dev. 26 (19) (2012) 2144-2153.
DOI Google Scholar
[23]

T. Akase, T. Nagase, L.J. Huang, A. Ibuki, T. Minematsu, G. Nakagami, et al., Aging-like skin changes induced by ultraviolet irradiation in an animal model of metabolic syndrome, Biol. Res. Nurs. 14 (2) (2012) 180-187.
DOI Google Scholar
[24]

J.H. Chung, J.Y. Seo, H.R. Choi, M.K. Lee, C.S. Youn, G. Rhie, et al., Modulation of skin collagen metabolism in aged and photoaged human skin in vivo, J. Invest. Dermatol. 117 (5) (2001) 1218-1224.
DOI Google Scholar
[25]

J. Kim, J.S. Hwang, Y.K. Cho, Y.K. Han, Y.J. Jeon, K.H. Yang, Protective effects of (−)-epigallocatechin-3-gallate on UVA- and UVB-induced skin damage, Skin Pharmacol. Appl. 14 (1) (2001) 11-19.
DOI Google Scholar
[26]

H.M. Park, E. Hwang, K.G. Lee, S.M. Han, Y. Cho, S.Y. Kim, Royal jelly protects against ultraviolet B-induced photoaging in human skin fibroblasts via enhancing collagen production, J. Med. Food 14 (9) (2011) 899-906.
DOI Google Scholar
[27]

V. Zague, V. de Freitas, M. da Costa Rosa, G.A. de Castro, R.G. Jaeger, G.M. Machado-Santelli, Collagen hydrolysate intake increases skin collagen expression and suppresses matrix metalloproteinase 2 activity, J. Med. Food 14 (6) (2011) 618-624.
DOI Google Scholar
[28]

Y. Zhuang, H. Hou, X. Zhao, Z. Zhang, B. Li, Effects of collagen and collagen hydrolysate from jellyfish (Rhopilema esculentum) on mice skin photoaging induced by UV irradiation, J. Food Sci. 74 (6) (2009) H183-8.
DOI Google Scholar
[29]

F. Gorouhi, H.I. Maibach, Role of topical peptides in preventing or treating aged skin, Int. J. Cosmet. Sci. 31 (5) (2009) 327-345.
DOI Google Scholar
[30]

Y. Shigemura, K. Iwai, F. Morimatsu, T. Iwamoto, T. Mori, C. Oda, 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.
DOI Google Scholar
[31]

S. Ichikawa, M. Morifuji, H. Ohara, H. Matsumoto, Y. Takeuchi, K. Sato, Hydroxyproline-containing dipeptides and tripeptides quantified at high concentration in human blood after oral administration of gelatin hydrolysate, Int. J. Food Sci. Nutr. 61 (1) (2010) 52-60.
DOI Google Scholar
[32]

S. Schadow, H.C. Siebert, G. Lochnit, J. Kordelle, M. Rickert, J. Steinmeyer, Collagen metabolism of human osteoarthritic articular cartilage as modulated by bovine collagen hydrolysates, PLoS One 8 (1) (2013) e53955.
DOI Google Scholar
[33]

S. Chakrabarti, S.T. Davidge, High glucose-induced oxidative stress alters estrogen effects on ERalpha and ERbeta in human endothelial cells: reversal by AMPK activator, J. Steroid Biochem. Mol. Biol. 117 (4–5) (2009) 99-106.
DOI Google Scholar
[34]

W. Huang, S. Chakrabarti, K. Majumder, Y. Jiang, S.T. Davidge, J. Wu, Egg-derived peptide IRW inhibits TNF-alpha-induced inflammatory response and oxidative stress in endothelial cells, J. Agric. Food Chem. 58 (20) (2010) 10840-10846.
DOI Google Scholar
[35]

P.C. Trackman, Diverse biological functions of extracellular collagen processing enzymes, J. Cell Biochem. 96 (5) (2005) 927-937.
DOI Google Scholar
[36]

D.H. Kim, Y.J. Je, C.D. Kim, Y.H. Lee, Y.J. Seo, J.H. Lee, et al., Can platelet-rich plasma be used for skin rejuvenation? Evaluation of effects of platelet-rich plasma on human dermal fibroblast, Ann. Dermatol. 23 (4) (2011) 424-431.
DOI Google Scholar
[37]

E. Jung, J. Lee, J. Baek, K. Jung, S. Huh, S. Kim, et al., Effect of Camellia japonica oil on human type I procollagen production and skin barrier function, J. Ethnopharmacol. 112 (1) (2007) 127-131.
DOI Google Scholar
[38]

B. Ma, K.Z. Zhang, C. Hendrie, C.Z. Liang, M. Li, A. Doherty-Kirby, et al., PEAKS: powerful software for peptide de novo sequencing by tandem mass spectrometry, Rapid Commun. Mass Spectrom. 17 (20) (2003) 2337-2342.
DOI Google Scholar
[39]

A.E. Bello, S. Oesser, Collagen hydrolysate for the treatment of osteoarthritis and other joint disorders: a review of the literature, Curr. Med. Res. Opin. 22 (11) (2006) 2221-2232.
DOI Google Scholar
[40]

S.H. Elder, A. Borazjani, Effect of collagen hydrolysate on chondrocyte-seeded agarose constructs, Biomed. Mater. Eng. 19 (6) (2009) 409-414.
DOI Google Scholar
[41]

C. Oba, H. Ohara, M. Morifuji, K. Ito, S. Ichikawa, K. Kawahata, 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 (4) (2013) 204-211.
DOI Google Scholar
[42]

V. Zague, A new view concerning the effects of collagen hydrolysate intake on skin properties, Arch. Dermatol. Res. 300 (9) (2008) 479-483.
DOI Google Scholar
[43]

H. Ohara, S. Ichikawa, H. Matsumoto, M. Akiyama, N. Fujimoto, T. Kobayashi, 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.
DOI Google Scholar
[44]

C. Helary, M. Zarka, M.M. Giraud-Guille, Fibroblasts within concentrated collagen hydrogels favour chronic skin wound healing, J. Tissue Eng. Regen. Med. 6 (3) (2012) 225-237.
DOI Google Scholar
[45]

R. Song, H.N. Bian, W. Lai, H.D. Chen, K.S. Zhao, Normal skin and hypertrophic scar fibroblasts differentially regulate collagen and fibronectin expression as well as mitochondrial membrane potential in response to basic fibroblast growth factor, Braz. J. Med. Biol. Res. 44 (5) (2011) 402-410.
DOI Google Scholar
[46]

H.M. Chiang, H.C. Chen, T.J. Lin, I.C. Shih, K.C. Wen, Michelia alba extract attenuates UVB-induced expression of matrix metalloproteinases via MAP kinase pathway in human dermal fibroblasts, Food Chem. Toxicol. 50 (12) (2012) 4260-4269.
DOI Google Scholar
[47]

Y. Fang, X.H. Hu, Z.G. Jia, M.H. Xu, Z.Y. Guo, F.H. Gao, Tiron protects against UVB-induced senescence-like characteristics in human dermal fibroblasts by the inhibition of superoxide anion production and glutathione depletion, Australas. J. Dermatol. 53 (3) (2012) 172-180.
DOI Google Scholar
[48]

P.E. Lazzerini, M. Natale, E. Gianchecchi, P.L. Capecchi, C. Montilli, S. Zimbone, et al., Adenosine A2A receptor activation stimulates collagen production in sclerodermic dermal fibroblasts either directly and through a cross-talk with the cannabinoid system, J. Mol. Med. (Berl.) 90 (3) (2012) 331-342.
DOI Google Scholar
[49]

A.M. Rezakhanlou, C. Miller, B. McMullin, A. Ghaffari, R. Garcia, A. Ghahary, Gaseous nitric oxide exhibits minimal effect on skin fibroblast extracellular matrix gene expression and immune cell viability, Cell Biol. Int. 35 (4) (2011) 407-415.
DOI Google Scholar
[50]

J.I. Silverberg, M. Patel, N. Brody, J. Jagdeo, Caffeine protects human skin fibroblasts from acute reactive oxygen species-induced necrosis, J. Drugs Dermatol. 11 (11) (2012) 1342-1346.
Google Scholar
[51]

G.M. Campo, A. Avenoso, A. D'Ascola, V. Prestipino, M. Scuruchi, G. Nastasi, et al., Inhibition of hyaluronan synthesis reduced inflammatory response in mouse synovial fibroblasts subjected to collagen-induced arthritis, Arch. Biochem. Biophys. 518 (1) (2012) 42-52.
DOI Google Scholar
[52]

I.S. An, S. An, S.M. Kang, T.B. Choe, S.N. Lee, H.H. Jang, et al., Titrated extract of Centella asiatica provides a UVB protective effect by altering microRNA expression profiles in human dermal fibroblasts, Int. J. Mol. Med. 30 (5) (2012) 1194-1202.
DOI Google Scholar
[53]

F. Giampieri, J.M. Alvarez-Suarez, S. Tulipani, A.M. Gonzales-Paramas, C. Santos-Buelga, S. Bompadre, et al., Photoprotective potential of strawberry (Fragaria x ananassa) extract against uv-a irradiation damage on human fibroblasts, J. Agric. Food Chem. 60 (9) (2012) 2322-2327.
DOI Google Scholar
[54]

Y. Tokudome, K. Nakamura, M. Kage, H. Todo, K. Sugibayashi, F. Hashimoto, Effects of soybean peptide and collagen peptide on collagen synthesis in normal human dermal fibroblasts, Int. J. Food Sci. Nutr. 63 (6) (2012) 689-695.
DOI Google Scholar
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 03 December 2017
Revised: 26 January 2018
Accepted: 17 February 2018
Published: 24 February 2018
Issue date: June 2018

Copyright

© 2018 “Society information”.

Acknowledgements

Acknowledgements

This study was funded by grants from Alberta Livestock and Meat Agency (ALMA) and the Natural Sciences and Engineering Research Council (NSERC) of Canada to JW. The funders had no role in the study design, data collection and analysis, decision to publish or preparation of this manuscript.

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