Collagens are the most abundant proteins in mammals and form an extracellular matrix (ECM) with other components as the structural support of muscle, skin, corneas and blood vessels etc. Other than providing structural support, the ECM exhibits active communication with cells and influences many cellular processes including migration, wound healing, differentiation and cancer metastasis. Though collagen proteins contain highly repetitive primary sequences and defined tertiary structures, more and more studies have shown that many short peptides/motifs within collagen proteins play key roles in various biological processes. These short sequences are effective within triple helical structures or independently as stand-alone molecules resulting from proteolytic degradation. Besides endogenous ECM-derived peptides, many more functional peptides have been produced by tissue processing, chemical synthesis, and recombinant protein production. In this review, we summarize different peptides/motifs identified in collagen and other ECM proteins and discuss their potential for medical, personal care, and cosmetics applications.
References
[1]
Karsdal, M.A. (2019) Biochemistry of Collagens, Laminins and Elastin: Structure, Function and Biomarkers. 2nd Edition, Academic Press, London.
[2]
Sainio, A. and Jarvelainen, H. (2020) Extracellular Matrix-Cell Interactions: Focus on Therapeutic Applications. Cell Signal, 66, Article ID: 109487.
https://doi.org/10.1016/j.cellsig.2019.109487
[3]
Jariwala, N., Ozols, M., Bell, M., Bradley, E., Gilmore, A., Debelle, L. and Sherratt, M.J. (2022) Matrikines as Mediators of Tissue Remodelling. Advanced Drug Delivery Reviews, 185, Article ID: 114240. https://doi.org/10.1016/j.addr.2022.114240
[4]
Banerjee, P. and Shanthi, C. (2016) Cryptic Peptides from Collagen: A Critical Review. Protein & Peptide Letters, 23, 664-672.
https://doi.org/10.2174/0929866522666160512151313
[5]
Maquart, F.X., Pasco, S., Ramont, L., Hornebeck, W. and Monboisse, J.C. (2004) An Introduction to Matrikines: Extracellular Matrix-Derived Peptides Which Regulate Cell Activity. Implication in Tumor Invasion. Critical Reviews in Oncology/Hematology, 49, 199-202. https://doi.org/10.1016/j.critrevonc.2003.06.007
[6]
Hwang, S.J., Ha, G.H., Seo, W.Y., Kim, C.K., Kim, K. and Lee, S.B. (2020) Human Collagen α-2 Type I Stimulates Collagen Synthesis, Wound Healing, and Elastin Production in Normal Human Dermal Fibroblasts (HDFs). BMB Reports, 53, 539-544. https://doi.org/10.5483/BMBRep.2020.53.10.120
[7]
Aly, N., et al. (2022) Cosmetic Potential of a Recombinant 50 kDa Protein. Cosmetics, 9, Article 8. https://doi.org/10.3390/cosmetics9010008
[8]
Katayama, K., Seyer, J.M., Raghow, R. and Kang, A.H. (1991) Regulation of Extracellular Matrix Production by Chemically Synthesized Subfragments of Type I Collagen Carboxy Propeptide. Biochemistry, 30, 7097-7104.
https://doi.org/10.1021/bi00243a009
[9]
Katayama, K., Armendariz-Borunda, J., Raghow, R., Kang, A.H. and Seyer, J.M. (1993) A Pentapeptide from Type I Procollagen Promotes Extracellular Matrix Production. The Journal of Biological Chemistry, 268, 9941-9944.
https://doi.org/10.1016/S0021-9258(18)82153-6
[10]
Jones, R.R., Castelletto, V., Connon, C.J. and Hamley, I.W. (2013) Collagen Stimulating Effect of Peptide Amphiphile C16-KTTKS on Human Fibroblasts. Molecular Pharmaceutics, 10, 1063-1069. https://doi.org/10.1021/mp300549d
[11]
Abu Samah, N.H. and Heard, C.M. (2011) Topically Applied KTTKS: A Review. International Journal of Cosmetic Science, 33, 483-490.
https://doi.org/10.1111/j.1468-2494.2011.00657.x
[12]
Tsai, W.C., Hsu, C.C., Chung, C.Y., Lin, M.S., Li, S.L. and Pang, J.H. (2007) The Pentapeptide KTTKS Promoting the Expressions of Type I Collagen and Transforming Growth Factor-β of Tendon Cells. Journal of Orthopaedic Research, 25, 1629-1634. https://doi.org/10.1002/jor.20455
[13]
Talalaj, U., Uscinowicz, P., Bruzgo, I., Surazyński, A., Zareba, I. and Markowska, A. (2019) The Effects of a Novel Series of KTTKS Analogues on Cytotoxicity and Proteolytic Activity. Molecules, 24, Article 3698.
https://doi.org/10.3390/molecules24203698
[14]
Choi, Y.L., Park, E.J., Kim, E., Na, D.H. and Shin, Y.H. (2014) Dermal Stability and in vitro Skin Permeation of Collagen Pentapeptides (KTTKS and Palmitoyl-KTTKS). Biomolecules & Therapeutics, 22, 321-327.
https://doi.org/10.4062/biomolther.2014.053
[15]
Palladino, P., Castelletto, V., Dehsorkhi, A., Stetsenko, D. and Hamley, I.W. (2012) Conformation and Self-Association of Peptide Amphiphiles Based on the KTTKS Collagen Sequence. Langmuir, 28, 12209-12215. https://doi.org/10.1021/la302123h
[16]
Akbarian, M., Khani, A., Eghbalpour, S. and Uversky, V.N. (2022) Bioactive Peptides: Synthesis, Sources, Applications, and Proposed Mechanisms of Action. I International Journal of Molecular Sciences, 23, Article 1445.
https://doi.org/10.3390/ijms23031445
[17]
Wise, S.G. and Weiss, A.S. (2009) Tropoelastin. The International Journal of Biochemistry & Cell Biology, 41, 494-497. https://doi.org/10.1016/j.biocel.2008.03.017
[18]
Bradshaw, R.A. and Stahl, P. (2016) Encyclopedia of Cell Biology. Academic Press, Waltham.
[19]
Pickart, L. and Thaler, M.M. (1973) Tripeptide in Human Serum which Prolongs Survival of Normal Liver Cells and Stimulates Growth in Neoplastic Liver. Nature New Biology, 243, 85-87.
[20]
Pickart, L., Freedman, J.H., Loker, W.J., Peisach, J., Perkins, C.M., Stenkamp, R.E. and Weinstein, B. (1980) Growth-Modulating Plasma Tripeptide May Function by Facilitating Copper Uptake into Cells. Nature, 288, 715-717.
https://doi.org/10.1038/288715a0
[21]
Pickart, L. and Margolina, A. (2018) Regenerative and Protective Actions of the GHK-Cu Peptide in the Light of the New Gene Data. International Journal of Molecular Sciences, 19, Article 1987. https://doi.org/10.3390/ijms19071987
[22]
Pickart, L., Vasquez-Soltero, J.M. and Margolina, A. (2015) GHK Peptide as a Natural Modulator of Multiple Cellular Pathways in Skin Regeneration. BioMed Research International, 2015, Article ID: 648108. https://doi.org/10.1155/2015/648108
[23]
Arul, V., Kartha, R. and Jayakumar, R. (2007) A Therapeutic Approach for Diabetic Wound Healing Using Biotinylated GHK Incorporated Collagen Matrices. Life Sciences, 80, 275-284. https://doi.org/10.1016/j.lfs.2006.09.018
[24]
Maquart, F.X., Pickart, L., Laurent, M., Gillery, P., Monboisse, J.C. and Borel, J.P. (1988) Stimulation of Collagen Synthesis in Fibroblast Cultures by the Tripeptide-Copper Complex Glycyl-L-Histidyl-L-Lysine-Cu2+. FEBS Letters, 238, 343-346.
https://doi.org/10.1016/0014-5793(88)80509-X
[25]
Wegrowski, Y., Maquart, F.X. and Borel, J.P. (1992) Stimulation of Sulfated Glycosaminoglycan Synthesis by the Tripeptide-Copper Complex Glycyl-L-Histidyl-L-Lysine-Cu2+. Life Sciences, 51, 1049-1056.
https://doi.org/10.1016/0024-3205(92)90504-I
[26]
Giudici, C., Raynal, N., Wiedemann, H., Cabral, W.A., Marini, J.C., Timpl, R., Bachinger, H.P., Farndale, R.W., Sasaki, T. and Tenni, R. (2008) Mapping of SPARC/BM-40/Osteonectin-Binding Sites on Fibrillar Collagens. Journal of Biological Chemistry, 283, 19551-19560. https://doi.org/10.1074/jbc.M710001200
[27]
Hohenester, E., Sasaki, T., Giudici, C., Farndale, R.W. and Bachinger, H.P. (2008) Structural Basis of Sequence-Specific Collagen Recognition by SPARC. Proceedings of the National Academy of Sciences of the United States of America, 105, 18273-18277. https://doi.org/10.1073/pnas.0808452105
[28]
Lisman, T., Raynal, N., Groeneveld, D., Maddox, B., Peachey, A.R., Huizinga, E.G., de Groot, P.G. and Farndale, R.W. (2006) A Single High-Affinity Binding Site for von Willebrand Factor in Collagen III, Identified Using Synthetic Triple-Helical Peptides. Blood, 108, 3753-3756. https://doi.org/10.1182/blood-2006-03-011965
[29]
Abdulhussein, R., McFadden, C., Fuentes-Prior, P. and Vogel, W.F. (2004) Exploring the Collagen-Binding Site of the DDR1 Tyrosine Kinase Receptor. Journal of Biological Chemistry, 279, 31462-31470. https://doi.org/10.1074/jbc.M400651200
[30]
Konitsiotis, A.D., Raynal, N., Bihan, D., Hohenester, E., Farndale, R.W. and Leitinger, B. (2008) Characterization of High Affinity Binding Motifs for the Discoidin Domain Receptor DDR2 in Collagen. Journal of Biological Chemistry, 283, 6861-6868. https://doi.org/10.1074/jbc.M709290200
[31]
Ferri, N., Carragher, N.O. and Raines, E.W. (2004) Role of Discoidin Domain Receptors 1 and 2 in Human Smooth Muscle Cell-Mediated Collagen Remodeling: Potential Implications in Atherosclerosis and Lymphangioleiomyomatosis. The American Journal of Pathology, 164, 1575-1585.
https://doi.org/10.1016/S0002-9440(10)63716-9
[32]
Hou, G., Vogel, W. and Bendeck, M.P. (2001) The Discoidin Domain Receptor Tyrosine Kinase DDR1 in Arterial Wound Repair. Journal of Clinical Investigation, 107, 727-735. https://doi.org/10.1172/JCI10720
[33]
Chen, E.A. and Lin, Y.S. (2019) Using Synthetic Peptides and Recombinant Collagen to Understand DDR-Collagen Interactions. Biochimica et Biophysica Acta (BBA)—Molecular Cell Research, 1866, Article ID: 118458.
https://doi.org/10.1016/j.bbamcr.2019.03.005
[34]
Vogel, W., Gish, G.D., Alves, F. and Pawson, T. (1997) The Discoidin Domain Receptor Tyrosine Kinases Are Activated by Collagen. Molecular Cell, 1, 13-23.
https://doi.org/10.1016/S1097-2765(00)80003-9
[35]
Leitinger, B. and Kwan, A.P. (2006) The Discoidin Domain Receptor DDR2 Is a Receptor for Type X Collagen. Matrix Biology, 25, 355-364.
https://doi.org/10.1016/j.matbio.2006.05.006
[36]
Leitinger, B., Steplewski, A. and Fertala, A. (2004) The D2 Period of Collagen II Contains a Specific Binding Site for the Human Discoidin Domain Receptor, DDR2. Journal of Molecular Biology, 344, 993-1003.
https://doi.org/10.1016/j.jmb.2004.09.089
[37]
Ichikawa, O., Osawa, M., Nishida, N., Goshima, N., Nomura, N. and Shimada, I. (2007) Structural Basis of the Collagen-Binding Mode of Discoidin Domain Receptor 2. The EMBO Journal, 26, 4168-4176. https://doi.org/10.1038/sj.emboj.7601833
[38]
Pountos, I., Panteli, M., Lampropoulos, A., Jones, E., Calori, G.M. and Giannoudis, P.V. (2016) The Role of Peptides in Bone Healing and Regeneration: A Systematic Review. BMC Medicine, 14, Article No. 103.
https://doi.org/10.1186/s12916-016-0646-y
[39]
Bhatnagar, R.S., Qian, J.J., Wedrychowska, A., Sadeghi, M., Wu, Y.M. and Smith, N. (1999) Design of Biomimetic Habitats for Tissue Engineering with P-15, a Synthetic Peptide Analogue of Collagen. Tissue Engineering, 5, 53-65.
https://doi.org/10.1089/ten.1999.5.53
[40]
Heino, J. (2007) The Collagen Family Members as Cell Adhesion Proteins. Bioessays, 29, 1001-1010. https://doi.org/10.1002/bies.20636
[41]
Boraschi-Diaz, I., Mort, J.S., Bromme, D., Senis, Y.A., Mazharian, A. and Komarova, S.V. (2018) Collagen Type I Degradation Fragments Act through the Collagen Receptor LAIR-1 to Provide a Negative Feedback for Osteoclast Formation. Bone, 117, 23-30. https://doi.org/10.1016/j.bone.2018.09.006
[42]
Meyaard, L. (2008) The Inhibitory Collagen Receptor LAIR-1 (CD305). Journal of Leukocyte Biology, 83, 799-803. https://doi.org/10.1189/jlb.0907609
[43]
Mohan, R.R. and Wilson, S.E. (2001) Discoidin Domain Receptor (DDR) 1 and 2: Collagen-Activated Tyrosine Kinase Receptors in the Cornea. Experimental Eye Research, 72, 87-92. https://doi.org/10.1006/exer.2000.0932
[44]
Peng, D.H., Rodriguez, B.L., Diao, L., Chen, L., Wang, J., Byers, L.A., Wei, Y., Chapman, H.A., Yamauchi, M., Behrens, C., Raso, G., Soto, L.M.S., Cuentes, E.R.P., Wistuba, I.I., Kurie, J.M. and Gibbons, D.L. (2020) Collagen Promotes Anti-PD-1/PD-L1 Resistance in Cancer through LAIR1-Dependent CD8. Nature Communications, 11, Article No. 4520. https://doi.org/10.1038/s41467-020-18298-8
[45]
Vijver, S.V., Singh, A., Mommers-Elshof, E.T.A.M., Meeldijk, J., Copeland, R., Boon, L., Langermann, S., Flies, D., Meyaard, L. and Ramos, M.I.P. (2021) Collagen Fragments Produced in Cancer Mediate T Cell Suppression through Leukocyte-Associated Immunoglobulin-Like Receptor 1. Frontiers in Immunology, 12, Article 733561. https://doi.org/10.3389/fimmu.2021.733561
[46]
Lebbink, R.J., de Ruiter, T., Adelmeijer, J., Brenkman, A.B., van Helvoort, J.M., Koch, M., Farndale, R.W., Lisman, T., Sonnenberg, A., Lenting, P.J. and Meyaard, L. (2006) Collagens Are Functional, High Affinity Ligands for the Inhibitory Immune Receptor LAIR-1. Journal of Experimental Medicine, 203, 1419-1425.
https://doi.org/10.1084/jem.20052554
[47]
Lebbink, R.J., van den Berg, M.C., de Ruiter, T., Raynal, N., van Roon, J.A., Lenting, P.J., Jin, B. and Meyaard, L. (2008) The Soluble Leukocyte-Associated Ig-Like Receptor (LAIR)-2 Antagonizes the Collagen/LAIR-1 Inhibitory Immune Interaction. The Journal of Immunology, 180, 1662-1669.
https://doi.org/10.4049/jimmunol.180.3.1662
[48]
San Antonio, J.D., Lander, A.D., Karnovsky, M.J. and Slayter, H.S. (1994) Mapping the Heparin-Binding Sites on Type I Collagen Monomers and Fibrils. Journal of Cell Biology, 125, 1179-1188. https://doi.org/10.1083/jcb.125.5.1179
[49]
Sweeney, S.M., Guy, C.A., Fields, G.B. and San Antonio, J.D. (1998) Defining the Domains of Type I Collagen Involved in Heparin-Binding and Endothelial Tube Formation. Proceedings of the National Academy of Sciences of the United States of America, 95, 7275-7280. https://doi.org/10.1073/pnas.95.13.7275
[50]
Knight, C.G., Morton, L.F., Peachey, A.R., Tuckwell, D.S., Farndale R.W. and Barnes, M.J. (2000) The Collagen-Binding A-Domains of Integrins α1β1 and α2β1 Recognize the Same Specific Amino Acid Sequence, GFOGER, in Native (Triple-Helical) Collagens. Journal of Biological Chemistry, 275, 35-40.
https://doi.org/10.1074/jbc.275.1.35
[51]
Raynal, N., Hamaia, S.W., Siljander, P.R., Maddox, B., Peachey, A.R., Fernandez, R., Foley, L.J., Slatter, D.A., Jarvis, G.E. and Farndale, R.W. (2006) Use of Synthetic Peptides to Locate Novel Integrin α2β1-Binding Motifs in Human Collagen III. Journal of Biological Chemistry, 281, 3821-3831.
https://doi.org/10.1074/jbc.M509818200
[52]
Staatz, W.D., Fok, K.F., Zutter, M.M., Adams, S.P., Rodriguez, B.A. and Santoro, S.A. (1991) Identification of a Tetrapeptide Recognition Sequence for the α2β1 Integrin in Collagen. The Journal of Biological Chemistry, 266, 7363-7367.
https://doi.org/10.1016/S0021-9258(20)89455-1
[53]
Hennessy, K.M., Pollot, B.E., Clem, W.C., Phipps, M.C., Sawyer, A.A., Culpepper, B.K. and Bellis, S.L. (2009) The Effect of Collagen I Mimetic Peptides on Mesenchymal Stem Cell Adhesion and Differentiation, and on Bone Formation at Hydroxyapatite Surfaces. Biomaterials, 30, 1898-1909.
https://doi.org/10.1016/j.biomaterials.2008.12.053
[54]
Pytela, R., Pierschbacher, M.D., Ginsberg, M.H., Plow, E.F. and Ruoslahti, E. (1986) Platelet Membrane Glycoprotein IIb/IIIa: Member of a Family of Arg-Gly-Asp— Specific Adhesion Receptors. Science, 231, 1559-1562.
https://doi.org/10.1126/science.2420006
[55]
Pytela, R., Pierschbacher, M.D. and Ruoslahti, E. (1985) Identification and Isolation of a 140 kd Cell Surface Glycoprotein with Properties Expected of a Fibronectin Receptor. Cell, 40, 191-198. https://doi.org/10.1016/0092-8674(85)90322-8
[56]
Ruoslahti, E. and Pierschbacher, M.D. (1987) New Perspectives in Cell Adhesion: RGD and Integrins. Science, 238, 491-497. https://doi.org/10.1126/science.2821619
[57]
Orgel, J.P., Eid, A., Antipova, O., Bella, J. and Scott, J.E. (2009) Decorin Core Protein (Decoron) Shape Complements Collagen Fibril Surface Structure and Mediates Its Binding. PLOS ONE, 4, e7028. https://doi.org/10.1371/journal.pone.0007028
[58]
Zhou, L., Hinerman, J.M., Blaszczyk, M., Miller, J.L., Conrady, D.G., Barrow, A.D., Chirgadze, D.Y., Bihan, D., Farndale, R.W. and Herr, A.B. (2016) Structural Basis for Collagen Recognition by the Immune Receptor OSCAR. Blood, 127, 529-537.
https://doi.org/10.1182/blood-2015-08-667055
[59]
Barrow, A.D., Raynal, N., Andersen, T.L., Slatter, D.A., Bihan, D., Pugh, N., Cella, M., Kim, T., Rho, J., Negishi-Koga, T., Delaisse, J.M., Takayanagi, H., Lorenzo, J., Colonna, M., Farndale, R.W., Choi, Y. and Trowsdale, J. (2011) OSCAR Is a Collagen Receptor That Costimulates Osteoclastogenesis in DAP12-Deficient Humans and Mice. Journal of Clinical Investigation, 121, 3505-3516.
https://doi.org/10.1172/JCI45913
[60]
Di Lullo, G.A., Sweeney, S.M., Korkko, J., Ala-Kokko, L. and San Antonio, J.D. (2002) Mapping the Ligand-Binding Sites and Disease-Associated Mutations on the Most Abundant Protein in the Human, Type I Collagen. Journal of Biological Chemistry, 277, 4223-4231. https://doi.org/10.1074/jbc.M110709200
[61]
Parkin, J.D., San Antonio, J.D., Pedchenko, V., Hudson, B., Jensen, S.T. and Savige, J. (2011) Mapping Structural Landmarks, Ligand Binding Sites, and Missense Mutations to the Collagen IV Heterotrimers Predicts Major Functional Domains, Novel Interactions, and Variation in Phenotypes in Inherited Diseases Affecting Basement Membranes. Human Mutation, 32, 127-143. https://doi.org/10.1002/humu.21401
[62]
Parkin, J.D., San Antonio, J.D., Persikov, A.V., Dagher, H., Dalgleish, R., Jensen, S.T., Jeunemaitre, X. and Savige, J. (2017) The Collαgen III Fibril Has a “Flexi-Rod” Structure of Flexible Sequences Interspersed with Rigid Bioactive Domains Including Two with Hemostatic Roles. PLOS ONE, 12, e0175582.
https://doi.org/10.1371/journal.pone.0175582
[63]
An, B., Chang, S.W., Hoop, C., Baum, J., Buehler, M.J. and Kaplan, D.L. (2017) Structural Insights into the Glycine Pair Motifs in Type III Collagen. ACS Biomaterials Science & Engineering, 3, 269-278.
https://doi.org/10.1021/acsbiomaterials.6b00512
[64]
Maurice, P., Legrand, C. and Fauvel-Lafeve, F. (2004) Platelet Adhesion and Signaling Induced by the Octapeptide Primary Binding Sequence (KOGEOGPK) from Type III Collagen. The FASEB Journal, 18, 1339-1347.
https://doi.org/10.1096/fj.03-1151com
[65]
Brisson, B.K., Stewart, D.C., Burgwin, C., Chenoweth, D., Wells, R.G., Adams, S.L. and Volk, S.W. (2022) Cysteine-Rich Domain of Type III Collagen N-Propeptide Inhibits Fibroblast Activation by Attenuating TGFβ Signaling. Matrix Biology, 109, 19-33. https://doi.org/10.1016/j.matbio.2022.03.004
[66]
An, B., Abbonante, V., Yigit, S., Balduini, A., Kaplan, D.L. and Brodsky, B. (2014) Definition of the Native and Denatured Type II Collagen Binding Site for Fibronectin Using a Recombinant Collagen System. Journal of Biological Chemistry, 289, 4941-4951. https://doi.org/10.1074/jbc.M113.530808
[67]
Koliakos, G.G., Kouzi-Koliakos, K., Furcht, L.T., Reger, L.A. and Tsilibary, E.C. (1989) The Binding of Heparin to Type IV Collagen: Domain Specificity with Identification of Peptide Sequences from the α1(IV) and α2(IV) Which Preferentially Bind Heparin. The Journal of Biological Chemistry, 264, 2313-2323.
https://doi.org/10.1016/S0021-9258(18)94178-5
[68]
Ricard-Blum, S. and Salza, R. (2014) Matricryptins and Matrikines: Biologically Active Fragments of the Extracellular Matrix. Experimental Dermatology, 23, 457-463.
https://doi.org/10.1111/exd.12435
[69]
Okada, M. and Yamawaki, H. (2019) A Current Perspective of Canstatin, a Fragment of Type IV Collagen a α2 Chain. Journal of Pharmacological Sciences, 139, 59-64. https://doi.org/10.1016/j.jphs.2018.12.001
[70]
Elango, J., Hou, C., Bao, B., Wang, S., Maté Sánchez de Val, J.E. and Wu, W.H. (2022) The Molecular Interaction of Collagen with Cell Receptors for Biological Function. Polymers, 14, Article 876. https://doi.org/10.3390/polym14050876
[71]
Farndale, R.W., Lisman, T., Bihan, D., Hamaia, S., Smerling, C.S., Pugh, N., Konitsiotis, A., Leitinger, B., de Groot, P.G., Jarvis, G.E. and Raynal, N. (2008) Cell-Collagen Interactions: The Use of Peptide Toolkits to Investigate Collagen-Receptor Interactions. Biochemical Society Transactions, 36, 241-250.
https://doi.org/10.1042/BST0360241
[72]
Calvo, E., Tokumasu, F., Mizurini, D.M., McPhie, P., Narum, D.L., Ribeiro, J.M., Monteiro, R.Q. and Francischetti, I.M. (2010) Aegyptin Displays High-Affinity for the von Willebrand Factor Binding Site (RGQOGVMGF) in Collagen and Inhibits Carotid Thrombus Formation in vivo. FEBS Journal, 277, 413-427.
https://doi.org/10.1111/j.1742-4658.2009.07494.x
[73]
Chiang, T.M., Cole, F. and Woo-Rasberry, V. (2002) Cloning, Characterization, and Functional Studies of a 47-kDa Platelet Receptor for Type III Collagen. Journal of Biological Chemistry, 277, 34896-34901. https://doi.org/10.1074/jbc.M205311200
[74]
Leo, J.C., Elovaara, H., Bihan, D., Pugh, N., Kilpinen, S.K., Raynal, N., Skurnik, M., Farndale, R.W. and Goldman, A. (2010) First Analysis of a Bacterial Collagen-Binding Protein with Collagen Toolkits: Promiscuous Binding of YadA to Collagens May Explain How YadA Interferes with Host Processes. Infection and Immunity, 78, 3226-3236. https://doi.org/10.1128/IAI.01057-09
[75]
Luo, R., Jeong, S.J., Jin, Z., Strokes, N., Li, S. and Piao, X. (2011) G Protein-Coupled Receptor 56 and Collagen III, a Receptor-Ligand Pair, Regulates Cortical Development and Lamination. Proceedings of the National Academy of Sciences of the United States of America, 108, 12925-12930.
https://doi.org/10.1073/pnas.1104821108
[76]
Cauble, M., et al. (2018) Microstructure Dependent Binding of Pigment Epithelium Derived Factor (PEDF) to Type I Collagen Fibrils. Journal of Structural Biology, 199, 132-139. https://doi.org/10.1016/j.jsb.2017.06.001
[77]
Somasundaram, R. and Schuppan, D. (1996) Type I, II, III, IV, V, and VI Collagens Serve as Extracellular Ligands for the Isoforms of Platelet-Derived Growth Factor (AA, BB, and AB). Journal of Biological Chemistry, 271, 26884-26891.
https://doi.org/10.1074/jbc.271.43.26884
[78]
Malinda, K.M., Wysocki, A.B., Koblinski, J.E., Kleinman, H.K. and Ponce, M.L. (2008) Angiogenic Laminin-Derived Peptides Stimulate Wound Healing. The International Journal of Biochemistry & Cell Biology, 40, 2771-2780.
https://doi.org/10.1016/j.biocel.2008.05.025
[79]
Baud, S., Duca, L., Bochicchio, B., Brassart, B., Belloy, N., Pepe, A., Dauchez, M., Martiny, L. and Debelle, L. (2013) Elastin Peptides in Aging and Pathological Conditions. BioMolecular Concepts, 4, 65-76. https://doi.org/10.1515/bmc-2011-0062
[80]
Robinet, A., Fahem, A., Cauchard, J.H., Huet, E., Vincent, L., Lorimier, S., Antonicelli, F., Soria, C., Crepin, M., Hornebeck, W. and Bellon, G. (2005) Elastin-Derived Peptides Enhance Angiogenesis by Promoting Endothelial Cell Migration and Tubulogenesis through Upregulation of MT1-MMP. Journal of Cell Science, 118, 343-356. https://doi.org/10.1242/jcs.01613
[81]
Dhavalikar, P., Robinson, A., Lan, Z., Jenkins, D., Chwatko, M., Salhadar, K., Jose, A., Kar, R., Shoga, E., Kannapiran, A. and Cosgriff-Hernandez, E. (2020) Review of Integrin-Targeting Biomaterials in Tissue Engineering. Advanced Healthcare Materials, 9, e2000795. https://doi.org/10.1002/adhm.202000795
[82]
Feng, Y.Z. and Mrksich, M. (2004) The Synergy Peptide PHSRN and the Adhesion Peptide RGD Mediate Cell Adhesion through a Common Mechanism. Biochemistry, 43, 15811-15821. https://doi.org/10.1021/bi049174+
[83]
Lidén, A, van Wieringen, T., Lannergard, J., Kassner, A., Heinegard, D., Reed, R.K., Guss, B. and Rubin, K. (2008) A Secreted Collagen- and Fibronectin-Binding Streptococcal Protein Modulates Cell-Mediated Collagen Gel Contraction and Interstitial Fluid Pressure. Journal of Biological Chemistry, 283, 1234-1242.
https://doi.org/10.1074/jbc.M704827200
[84]
Wang, B., Wang, Y.M., Chi, C.F., Luo, H.Y., Deng, S.G. and Ma, J.Y. (2013) Isolation and Characterization of Collagen and Antioxidant Collagen Peptides from Scales of Croceine Croaker (Pseudosciaena crocea). Marine Drugs, 11, 4641-4661.
https://doi.org/10.3390/md11114641
[85]
Castillo-Briceno, P., Bihan, D., Nilges, M., Hamaia, S., Meseguer, J., García-Ayala, A., Farndale, R.W. and Mulero, V. (2011) A Role for Specific Collagen Motifs during Wound Healing and Inflammatory Response of Fibroblasts in the Teleost Fish Gilthead Seabream. Molecular Immunology, 48, 826-834.
https://doi.org/10.1016/j.molimm.2010.12.004
[86]
Hu, Z., Yang, P., Zhou, C., Li, S. and Hong, P. (2017) Marine Collagen Peptides from the Skin of Nile Tilapia (Oreochromis niloticus): Characterization and Wound Healing Evaluation. Marine Drugs, 15, Article 102.
https://doi.org/10.3390/md15040102
[87]
Mihardja, S.S., Yu, J. and Lee, R.J. (2011) Extracellular Matrix-Derived Peptides and Myocardial Repair. Cell Adhesion & Migration, 5, 111-113.
https://doi.org/10.4161/cam.5.2.13796
[88]
Volk, S.W., Wang, Y., Mauldin, E.A., Liechty, K.W. and Adams, S.L. (2011) Diminished Type III Collagen Promotes Myofibroblast Differentiation and Increases Scar Deposition in Cutaneous Wound Healing. Cells Tissues Organs, 194, 25-37.
https://doi.org/10.1159/000322399
[89]
Kakoi, C., Udo, H., Matsukawa, T. and Ohnuki, K. (2012) Collagen Peptides Enhance Hippocampal Neurogenesis and Reduce Anxiety Related Behavior in Mice. Biomedical Research, 33, 273-279. https://doi.org/10.2220/biomedres.33.273
[90]
Nogimura, D., Mizushige, T., Taga, Y., Nagai, A., Shoji, S., Azuma, N., Kusubata, M., Adachi, S.I., Yoshizawa, F. and Kabuyama, Y. (2020) Prolyl-Hydroxyproline, a Collagen-Derived Dipeptide, Enhances Hippocampal Cell Proliferation, Which Leads to Antidepressant-Like Effects in Mice. FASEB Journal, 34, 5715-5723.
https://doi.org/10.1096/fj.201902871R
[91]
Koizumi, S., Inoue, N., Sugihara, F. and Igase, M. (2019) Effects of Collagen Hydrolysates on Human Brain Structure and Cognitive Function: A Pilot Clinical Study. Nutrients, 12, Article 50. https://doi.org/10.3390/nu12010050
[92]
Konig, D., Oesser, S., Scharla, S., Zdzieblik, D. and Gollhofer, A. (2018) Specific Collagen Peptides Improve Bone Mineral Density and Bone Markers in Postmenopausal Women-A Randomized Controlled Study. Nutrients, 10, Article 97.
https://doi.org/10.3390/nu10010097
[93]
Liu, J., Wang, J. and Guo, Y. (2020) Effect of Collagen Peptide, Alone and in Combination with Calcium Citrate, on Bone Loss in Tail-Suspended Rats. Molecules, 25, Article 782. https://doi.org/10.3390/molecules25040782
[94]
De Martino, D. and Bravo-Cordero, J.J. (2023) Collagens in Cancer: Structural Regulators and Guardians of Cancer Progression. Cancer Research, 83, 1386-1392.
https://doi.org/10.1158/0008-5472.CAN-22-2034
[95]
Pryce, B.R., Wang, D.J., Zimmers, T.A., Ostrowski, M.C. and Guttridge, D.C. (2023) Cancer Cachexia: Involvement of an Expanding Macroenvironment. Cancer Cell, 41, 581-584. https://doi.org/10.1016/j.ccell.2023.02.007
[96]
Xu, S., Xu, H., Wang, W., Li, S., Li, H., Li, T., Zhang, W., Yu, X. and Liu, L. (2019) The Role of Collagen in Cancer: From Bench to Bedside. Journal of Translational Medicine, 17, Article No. 309. https://doi.org/10.1186/s12967-019-2058-1
[97]
Inoue, N., Sugihara, F. and Wang, X. (2016) 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. Journal of the Science of Food and Agriculture, 96, 4077-4081. https://doi.org/10.1002/jsfa.7606
[98]
Gorouhi, F. and Maibach, H.I. (2009) Role of Topical Peptides in Preventing or Treating Aged Skin. International Journal of Cosmetic Science, 31, 327-345.
https://doi.org/10.1111/j.1468-2494.2009.00490.x
[99]
Reddy, B., Jow, T. and Hantash, B.M. (2012) Bioactive Oligopeptides in Dermatology: Part I. Experimental Dermatology, 21, 563-568.
https://doi.org/10.1111/j.1600-0625.2012.01528.x
[100]
Lintner, K. and Peschard, O. (2000) Biologically Active Peptides: From a Laboratory Bench Curiosity to a Functional Skin Care Product. International Journal of Cosmetic Science, 22, 207-218. https://doi.org/10.1046/j.1467-2494.2000.00010.x
[101]
Blanes-Mira, C., Clemente, J., Jodas, G., Gil, A., Fernández-Ballester, G., Ponsati, B., Gutierrez, L., Pérez-Payá, E. and Ferrer-Montiel, A. (2002) A Synthetic Hexapeptide (Argireline) with Antiwrinkle Activity. International Journal of Cosmetic Science, 24, 303-310. https://doi.org/10.1046/j.1467-2494.2002.00153.x
[102]
Marini, A., Farwick, M., Grether-Beck, S., Brenden, H., Felsner, I., Jaenicke, T., Weber, M., Schild, J., Maczkiewitz, U., Kohler, T., Bonfigli, A., Pagani, V. and Krutmann, J. (2012) Modulation of Skin Pigmentation by the Tetrapeptide PKEK: In vitro and in vivo Evidence for Skin Whitening Effects. Experimental Dermatology, 21, 140-146. https://doi.org/10.1111/j.1600-0625.2011.01415.x
[103]
Fertala, A. (2020) Three Decades of Research on Recombinant Collagens: Reinventing the Wheel or Developing New Biomedical Products? Bioengineering, 7, Article 155. https://doi.org/10.3390/bioengineering7040155
