COLLAGEN: STRUCTURE, METABOLISM, PRODUCTION AND INDUSTRIAL APPLICATION A. K. Gulevsky, I. I. Shcheniavsky

Details: Hits: 988

ISSN 2410-7751 (Print)
ISSN 2410-776X (Online)

Biotechnologia Acta V. 13, No 5, 2020
Р. 42-61, Bibliography 122, English
Universal Decimal Classification: 547.982
https://doi.org/10.15407/biotech13.05.042

COLLAGEN: STRUCTURE, METABOLISM, PRODUCTION AND INDUSTRIAL APPLICATION

A. K. Gulevsky, I. I. Shcheniavsky

Institute for Problems of Cryobiology and Cryomedicine of the National Academy of Sciences of Ukraine, Kharkiv

This review presents the current scientific literature data about structure, properties, and functions of collagen, which is known as one of the most abundant human and animal proteins. The building of collagen molecule from the primary structure to submolecular formations, the main stages of its synthesis and biodegradation are briefly described. The information about collagen diversity, its features and metabolic ways in various tissues, including skin, tendons, bones, etc. is presented. The problems of pathologies caused by collagen synthesis and breakdown disorders as well as age-related changes in collagen properties and their causes are discussed.

A comparative analysis of the advantages and disadvantages of collagen and its derivatives obtaining from various sources (animals, marine, and recombinant) is given. The most productive methods for collagen extraction from various tissues are shown. The concept of collagen hydrolysis conditions influence on the physicochemical properties and biological activity of the obtained products is described.

The applications of collagen and its products in various fields of industrial activity, such as pharmaceutical, cosmetic industry and medicine, are discussed. Further prospective directions of fundamental and applied investigations in this area of research are outlined.

Key words: collagen types, collagen metabolism, sources of collagen production, collagen hydrolysis, application of collagen.

References

1. Mienaltowski M. J., Birk D. E. Structure, physiology, and biochemistry of collagens. Adv. Exp. Med. Biol. 2014, V. 802, P. 5–29. https://doi.org/10.1007/978-94-007-7893-1_2

2. Potekhina Y. Collagen Structure and Function. Russian Osteopathic J. 2016, N 1?2, P. 87–99. https://doi.org/10.32885/2220-0975-2016-1-2-87-99

3. Nikitin V. N., Perskii E. E., Utevskaya L. A. Essays about triple helix. Kyiv: Naukova dumka. 1984, 167 р. (In Russian).

4. Kadler K. E. Fell Muir Lecture: Collagen fibril formation in vitro and in vivo. Int. J. Exp. Pathol. 2017, 98 (1), 4–16. https://doi.org/10.1111/iep.12224

5. Kirkness M. W., Lehmann K., Forde N. R. Mechanics and structural stability of the collagen triple helix. Curr. Opin. Chem. Biol. 2019, V. 53, P. 98–105. https://doi.org/10.1016/j.cbpa.2019.08.001

6. Cisneros D. A., Hung C., Franz C. M., Muller D. J. Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy. J. Structural Biol. 2006, 154 (3), 232–245. https://doi.org/10.1016/j.jsb.2006.02.006

7. Kamrani P., Marston G., Jan A. Anatomy, Connective Tissue. [Updated 2020 Aug 13]. In: Stat Pearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2020 Jan. Available from: https://www.ncbi.nlm.nih.gov/books/NBK538534/

8. Gatseva A., Sin Y. Y., Brezzo G., Van Agtmael T. Basal membrane collagens and disease mechanisms. Essays Biochem. 2019, 63 (3), 297–312. https://doi.org/10.1042/EBC20180071

9. Ricard-Blum S. The collagen family. Cold Spring Harb. Perspect. Biol. 2011, 3 (1), a004978. https://doi.org/10.1101/cshperspect.a004978

10. Sorushanova A., Delgado L. M., Wu Z., Shologu N., Kshirsagar A., Raghunath R., Mullen A. M., Bayon Y., Pandit A., Raghunath M., Zeugolis D. I. The Collagen Suprafamily: From Biosynthesis to Advanced Biomaterial Development. Adv. Mater. 2019, 31 (1), e1801651. https://doi.org/10.1002/adma.201801651

11. Hulmes D. J. Building collagen molecules, fibrils, and suprafibrillar structures. J. Struct. Biol. 2002, 137 (1?2), 2?10. https://doi.org/10.1006/jsbi.2002.4450

12. Rappu P., Salo A. M., Myllyharju J., Heino J. Role of prolyl hydroxylation in the molecular interactions of collagens. Essays Biochem. 2019, 63 (3), 325–335. https://doi.org/10.1042/EBC20180053

13. Yamauchi M., Terajima M., Shiiba M. Lysine Hydroxylation and Cross-Linking of Collagen. Methods Mol. Biol. 2019, V. 1934, P. 309–324. https://doi.org/10.1007/978-1-4939-9055-9_19

14. Van Doren S. R. Matrix metalloproteinase interactions with collagen and elastin. Matrix Biol. 201, V. 44?46, P. 224–231. https://doi.org/10.1016/j.matbio.2015.01.005

15. Bishop J. E. Increased collagen synthesis and decreased collagen degradation in right ventricular by pressure over load. Cardiovasc. Res. 1994, 28 (10), 1501–1505. https://doi.org/10.1093/cvr/28.10.1581

16. Slutskij L. I. Biochemistry of normal and pathologically changed connective tissue. Leningrad: Medicine. 1969, 367 р.

17. Persky E. E., Utevskaya L. A. About age-related changes in physicochemical properties of collagen fibers. Ontogenesis. 1971, 2 (2), 188–192. (In Russian).

18. Thomas J. T., Ayad S., Grant M. E. Cartilage collagens: strategies for the study of their haracteriza and expression in the extracellular matrix. Ann. Rheum. Dis. 1994, 53 (8), 488–496. https://doi.org/10.1136/ard.53.8.488

19. Serov V. V., Shekhter A. B. Connective tissue. Functional morphology and General pathology. Moskva: Medicine. 1981, 312 р.

20. Genovese F., Karsdal M. A. Protein degradation fragments as diagnostic and prognostic biomarkers of connective tissue diseases: understanding the extracellular matrix message and implication for current and future serological biomarkers. Expert Rev. Proteomics. 2016, 13 (2), 213–225. https://doi.org/10.1586/14789450.2016.1134327

21. Chalikias G. K., Tziakas D. N. Biomarkers of the extracellular matrix and of collagen fragments. Clin. Chim. Acta. 2015, V. 443, P. 39–47. https://doi.org/10.1016/j.cca.2014.06.028

22. Gorres K. L., Raines R. T. Prolyl 4-hydroxylase. Crit. Rev. Biochem. Mol. Biol. 2010, 45 (2), 106–124. https://doi.org/10.3109/10409231003627991

23. Cheah K. S. Collagen genes and inherited connective tissue disease. Biochem. J. 1985, 229 (2), 287–303. https://doi.org/10.1042/bj2290287

24. Bateman J. F., Hannagan M., Chan D., Cole W. G. Characterization of a type I collagen alpha 2(I) glycine-586 to valine substitution in osteogenesis imperfecta type IV. Detection of the mutation and prenatal diagnosis by a chemical cleavage method. Biochem. J. 1991, 276 (3), 765–770. https://doi.org/10.1042/bj2760765

25. Cole W. G., Chan D., Chow C. W., Rogers J. G., Bateman J. F. Disrupted growth plates and progressive deformities in osteogenesis imperfecta as a result of the substitution of glycine 585 by valine in the alpha 2 (I) chain of type I collagen. J. Med. Genet. 1996, 33 (11), 968?971. https://doi.org/10.1136/jmg.33.11.968

26. Galicka A. Mutations of noncollagen genes in osteogenesis imperfecta-implications of the gene products in collagen biosynthesis and pathogenesis of disease. Postepy Hig. Med. Dosw. 2012, V. 66, P. 359–371. (In Polish) https://doi.org/10.5604/17322693.1000336

27. Chang W., Barnes A. M., Cabral W. A., Bodurtha J. N., Marini J. C. Prolyl 3-hydroxylase 1 and CRTAP are mutually stabilizing in the endoplasmic reticulum collagen prolyl 3-hydroxylation complex. Hum. Mol. Genet. 2010, 9 (2), 223–234. https://doi.org/10.1093/hmg/ddp481

28. Valli M., Barnes A. M., Gallanti A., Cabral W. A., Viglio S., Weis M. A., Makareeva E., Eyre D., Leikin S., Antoniazzi F., Marini J. C., Mottes M. Deficiency of CRTAP in non-lethal recessive osteogenesis imperfecta reduces collagen deposition into matrix. Clin. Genet. 2012, 82 (5), 453–459. https://doi.org/10.1111/j.1399-0004.2011.01794.x

29. Uzel M. I., Shih S. D., Gross H., Kessler E., Gerstenfeld L. C., Trackman P. C. Molecular events that contribute to lysyl oxidase enzyme activity and insoluble collagen accumulation in osteosarcoma cell clones. J. Bone Miner. Res. 2000, 15 (6), 1189–1197. https://doi.org/10.1359/jbmr.2000.15.6.1189

30. Nikitin V. N., Perskii E. E., Utevskaya L. A. Age-Related and Evolutionary Biochemistry of Collagen Structures. Kyiv: Naukova dumka. 1977, P. 242. (In Russian).

31. Quaglino D., Fornieri C., Nanney L. B., Davidson J. M. Extracellular matrix modifications in rat tissues of different ages. Correlations between elastin and collagen type I mRNA expression and lysyl-oxidase activity. Matrix. 1993, 13 (6), 481?490. https://doi.org/10.1016/S0934-8832(11)80114-9

32. Halme T., Peltonen J., Sims T. J., Vihersaari T., Penttinen R. Collagen in human aorta. Changes in the type III/I ratio and concentration of the reducible crosslink, dehydrohydroxylysinonorleucine in ascending aorta from healthy subjects of different age and patients with annulo-aortic ectasia. Biochim. Biophys. Acta. 1986, 881 (2), 222?228. https://doi.org/10.1016/0304-4165(86)90007-3

33. Shin J. W., Kwon S. H., Choi J. Y., Na J. I., Huh C. H., Choi H. R., Park K. C. Molecular Mechanisms of Dermal Aging and Antiaging Approaches. Int. J. Mol. Sci. 2019, 20 (9), 2126. https://doi.org/10.3390/ijms20092126

34. Sipil? K. H., Drushinin K., Rappu P., Jokinen J., Salminen T. A., Salo A. M., K?pyl? J., Myllyharju J., Heino J. Proline hydroxylation in collagen supports integrin binding by two distinct mechanisms. J. Biol. Chem. 2018, 293 (20), 7645–7658. https://doi.org/10.1074/jbc.RA118.002200

35. Davison P. F., Brennan M. The organization of cross-linking in collagen fibrils. Connect Tissue Res. 1983, 11 (2?3), 135–151. https://doi.org/10.3109/03008208309004850

36. El-ta’alu A. B., Persky E. E., Bulankina N. I., Kot Y. G., Kot E. V., Ponomarenko A. N., Kostinoi T. V. The Role of Collagen Processing in Age-related Changes in the Thermo-stability of Connective Tissue Macromolecule. Webmed Central Biochemistry 2011, 2 (10), WMC002385. https://doi/org/10.9754/journal.wmc.2011.002385

37. Behmoaras J., Slove S., Seve S., Vranckx R., Sommer P., Jacob M. P. Differential expression of lysyl oxidases LOXL1 and LOX during growth and aging suggests specific roles in elastin and collagen fiber remodeling in rat aorta. Rejuvenation Res. 2008, 11 (5), 883?889. https://doi.org/10.1089/rej.2008.0760

38. Saleem A., Rajput S. J. Insights from the in silico structural, functional and phylogenetic characterization of canine lysyl oxidase protein. Genet. Eng. Biotechnol. 2020, 18 (1), 20. https://doi.org/10.1186/s43141-020-00034-w

39. Panwar P., Lamour G., Mackenzie N. C., Yang H., Ko F., Li H., Br?mme D. Changes in Structural-Mechanical Properties and Degradability of Collagen during Aging-associated Modifications. J. Biol. Chem. 2015, 290 (38), 23291?23306. https://doi.org/10.1074/jbc.M115.644310

40. Hudson D. M., Archer M., King K. B., Eyre D. R. Glycation of type I collagen selectively targets the same helical domain lysine sites as lysyl oxidase-mediated cross-linking. J. Biol. Chem. 2018, 293 (40), 15620?15627. https://doi.org/10.1074/jbc.RA118.004829

41. Behmoaras J., Slove S., Seve S., Vranckx R., Sommer P., Jacob M. P. Differential expression of lysyl oxidases LOXL1 and LOX during growth and aging suggests specific roles in elastin and collagen fiber remodeling in rat aorta. Rejuvenation Res. 2008, 11 (5), 883?889. https://doi.org/10.1089/rej.2008.0760

42. Gaar J., Naffa R. Brimble M. Enzymatic and non-enzymatic crosslinks found in collagen and elastin and their chemical synthesis (Review Article) Org. Chem. Front. 2020, 7 (18), 2789?2814. https://doi.org/10.1039/D0QO00624F

43. Zullo A., Fleckenstein J., Schleip R., Hoppe K., Wearing S., Klingler W. Structural and Functional Changes in the Coupling of Fascial Tissue, Skeletal Muscle, and Nerves During Aging. Front Physiol. 2020, V. 11, P. 592. https://doi.org/10.3389/fphys.2020.00592

44. Lee D. H., Oh J. H., Chung J. H. Glycosaminoglycan and proteoglycan in skin aging. J. Dermatol. Sci. 2016, 83 (3), 174?181. https://doi.org/10.1016/j.jdermsci.2016.05.016

45. Stammers M., Ivanova I. M., Niewczas I. S., Segonds-Pichon A., Streeter M., Spiegel D. A., Clark J. Age-related changes in the physical properties, cross-linking, and glycation of collagen from mouse tail tendon. J. Biol. Chem. 2020, 295 (31), 10562?10571. https://doi.org/10.1074/jbc.RA119.011031

46. Verz?r F., Strittmatter-Ackerschott E. Studies on ageing of collagen by perchlorate reactions. Experientia. 1975, 15, 31 (10), 1183?1186. https://doi.org/10.1007/BF02326783

47. Chattopadhyay S., Raines R. T. Review collagen-based biomaterials for wound healing. Biopolymers. 2014, 101 (8), 821?833. https://doi.org/10.1002/bip.22486

48. Field F. K., Kerstein M. D. Overview of wound healing in a moist environment. Am. J. Surg. 1994, 167 (1A), 2S?6S. https://doi.org/10.1016/0002-9610(94)90002-7

49. Patino M. G., Neiders M. E., Andreana S., Noble B., Cohen R. E. Collagen as an implantable material in medicine and dentistry. J. Oral. Implantol. 2002, 28 (5), 220?225. https://doi.org/10.1563/1548-1336(2002)028<0220:CAAIMI>2.3.CO;2

50. Storublevtsev S. A., Popov V. I., Antipova L. V., Stukalo O. G., Bolgova S. B. Evaluation of the bacteriostatic effect of immobilized on collagen carrier antibiotics and silver ions in provision of the aseptic state of the tissue wounds]. Gig. Sanit. 2015, 94 (9), 54?57. (In Russian).

51. Mousavi S., Khoshfetrat A. B., Khatami N., Ahmadian M., Rahbarghazi R. Comparative study of collagen and gelatin in chitosan-based hydrogels for effective wound dressing: Physical properties and fibroblastic cell behavior. Biochem. Biophys. Res. Commun. 2019, 518 (4), 625?631. https://doi.org/10.1016/j.bbrc.2019.08.102

52. Boyd M., Flasza M., Johnson P. A., Roberts J. S., Kemp P. Integration and persistence of an investigational human living skin equivalent (ICX-SKN) in human surgical wounds. Regen. Med. 2007, 2 (4), 363?370. https://doi.org/10.2217/17460751.2.4.363

53. Caball?-Serrano J., Zhang S., Sculean A., Staehli A., Bosshardt D. D. Tissue Integration and Degradation of a Porous Collagen-Based Scaffold Used for Soft Tissue Augmentation. Materials (Basel). 2020, 13 (10), 2420. https://doi.org/10.3390/ma13102420

54. Weinberg C. B., Bell E. A blood vessel model constructed from collagen and cultured vascular cells. Science. 1986, 231 (4736), 397–400. https://doi.org/10.1126/science.2934816

55. Berglund J. D., Mohseni M. M., Nerem R. M., Sambanis A. A biological hybrid model for collagen-based tissue engineered vascular constructs. Biomaterials. 2003, 24 (7), 1241–1254. https://doi.org/10.1016/S0142-9612(02)00506-9

56. Copes F., Pien N., Van Vlierberghe S., Boccafoschi F., Mantovani D. Collagen-Based Tissue Engineering Strategies for Vascular Medicine. Front Bioeng. Biotechnol. 2019, V. 7, P. 166. https://doi.org/10.3389/fbioe.2019.00166

57. Avila Rodr?guez M. I., Rodr?guez Barroso L. G., S?nchez M. L. Collagen: A review on its sources and potential cosmetic applications. Cosmet. Dermatol. 2018, 17 (1), 20?26. https://doi.org/10.1111/jocd.12450

58. Udhayakumar S., Shankar K. G., Sowndarya S., Rose C. Novel fibrous collagen-based cream accelerates fibroblast growth for wound healing applications: in vitro and in vivo evaluation. Biomater. Sci. 2017, 5 (9), 1868?1883. https://doi/org/10.1039/c7bm00331e

59. Antipova L. V., Storublevtsev S. A., Bolgova S. B., Sukhov I. V. Obtaining, identification and comparative analysis of fish collagens with analogues of animal origin. Fundamental res. 2015, 8 (1), 9?13. (In Russian).

60. Baumann L., Kaufman J., Saghari S. Collagen fillers. Dermatol. Ther. 2006, 19 (3), 134–140. https://doi.org/10.1111/j.1529-8019.2006.00067.x

61. Cho K. H., Uthaman S., Park I. K., Cho C. S. Injectable Biomaterials in Plastic and Reconstructive Surgery: A Review of the Current Status. Tissue Eng. Regen. Med. 2018, 15 (5), 559–574. https://doi.org/10.1007/s13770-018-0158-2

62. Reddy B., Jow T., Hantash B. M. Bioactive oligopeptides in dermatology: Part I. Exp Dermatol. 2012, 21 (8), 563?568. https://doi.org/10.1111/j.1600-0625.2012.01528.x

63. Abu Samah N. H., Heard C. M. Topically applied KTTKS: a review. Int. J. Cosmet. Sci. 2011, 33 (6), 483?490. https://doi.org/10.1111/j.1468-2494.2011.00657.x

64. Katayama K., Seyer J. M., Raghow R., Kang A. H. Regulation of extracellular matrix production by chemically synthesized subfragments of type I collagen carboxy propeptide. Biochemistry. 1991, 30 (29), 7097?7104. https://doi.org/10.1021/bi00243a009

65. Katayama K., Armendariz-Borunda J., Raghow R., Kang A. H., Seyer J. M. A pentapeptide from type I procollagen promotes extracellular matrix production. J. Biol. Chem. 1993, 268 (14), 9941?9944.

66. Robinson L. R., Fitzgerald N. C., Doughty D. G., Dawes N. C., Berge C. A., Bissett D. L. Topical palmitoyl pentapeptide provides improvement in photoaged human facial skin. Int. J. Cosmet. Sci. 2005, 27 (3), 155?160. https://doi.org/10.1111/j.1467-2494.2005.00261.x

67. Farwick M., Grether-Beck S., Marini A., Maczkiewitz U., Lange J., K?hler T., Lersch P., Falla T., Felsner I., Brenden H., Jaenicke T., Franke S., Krutmann J. Bioactive tetrapeptide GEKG boosts extracellular matrix formation: in vitro and in vivo molecular and clinical proof. Exp. Dermatol. 2011, 20 (7), 602?604. https://doi.org/10.1111/j.1600-0625.2011.01307.x

68. Lintner K., Peschard O. Biologically active peptides: from a laboratory bench curiosity to a functional skin care product. Int. J. Cosmet. Sci. 2000, 22 (3), 207?218. https://doi.org/10.1046/j.1467-2494.2000.00010.x

69. Le?n-L?pez A., Morales-Pe?aloza A., Mart?nez-Ju?rez V. M., Vargas-Torres A., Zeugolis D. I., Aguirre-?lvarez G. Hydrolyzed Collagen-Sources and Applications. Molecules. 2019, 24 (22), 4031. https://doi.org/10.3390/molecules24224031

70. Silva T. H., Moreira-Silva J., Marques A. L., Domingues A., Bayon Y., Reis R. L. Marine origin collagens and its potential applications. Mar. Drugs. 2014, 12 (12), 5881?5901. https://doi.org/10.3390/md12125881

71. Casalone C., Hope J. Atypical and classic bovine spongiform encephalopathy. Handb. Clin. Neurol. 2018, V. 153, P. 121?134. https://doi.org/10.1016/B978-0-444-63945-5.00007-6

72. Kumar V. A., Taylor N. L., Jalan A. A., Hwang L. K., Wang B. K., Hartgerink J. D. A nanostructured synthetic collagen mimic for hemostasis. Biomacromolecules. 2014, 15 (4), 1484?1490. https://doi.org/10.1021/bm500091e

73. Geddis A. E., Prockop D. J. Expression of human COL1A1 gene in stably transfected HT1080 cells: the production of a thermostable homotrimer of type I collagen in a recombinant system. Matrix. 1993, 13 (5), 399–405. https://doi.org/10.1016/S0934-8832(11)80045-4

74. Myllyharju J., Lamberg A., Notbohm H., Fietzek P. P., Pihlajaniemi T., Kivirikko K. I. Expression of wild-type and modified proalpha chains of human type I procollagen in insect cells leads to the formation of stable [alpha1(I)]2alpha2(I) collagen heterotrimers and [alpha1(I)]3 homotrimers but not [alpha2(I)]3 homotrimers. J. Biol. Chem. 1997, 272 (35), 21824?21830. https://doi.org/10.1074/jbc.272.35.21824

75. Tomita M., Kitajima T., Yoshizato K. Formation of recombinant human procollagen I heterotrimers in a baculovirus expression system. J. Biochem. (Tokyo) 1997, 121 (6), 1061–1069. https://doi.org/10.1093/oxfordjournals.jbchem.a021695

76. Veijola J., Pihlajaniemi T., Kivirikko K. I. Co-expression of the alpha subunit of human prolyl 4-hydroxylase with BiP polypeptide in insect cells leads to the formation of soluble and insoluble complexes: soluble alpha-subunit-BiP complexes have no prolyl 4-hydroxylase activity. Biochem. J. 1996, 35 (Pt 2), 613–618. https://doi.org/10.1042/bj3150613

77. Vaughn P. R., Galanis M., Richards K. M., Tebb T. A., Ramshaw J. A., Werkmeister J. A. Production of recombinant hydroxylated human type III collagen fragment in Saccharomyces cerevisiae. DNA Cell Biol. 1998, 17 (6), 511?518. https://doi.org/10.1089/dna.1998.17.511

78. Olsen D. R., Leigh S. D., Chang R., McMullin H., Ong W., Tai E., Chisholm G., Birk D. E., Berg R. A., Hitzeman R. A., Toman P. D. Production of human type I collagen in yeast reveals unexpected new insights into the molecular assembly of collagen trimers. J. Biol. Chem. 2001, 276 (26), 24038?24043. https://doi.org/10.1074/jbc.M101613200

79. de Bruin E. C., Werten M. W. T., Laane C., de Wolf F. A. Endogenous prolyl 4-hydroxylation in Hansenula polymorpha and its use for the production of hydroxylated recombinant gelatin. FEMS Yeast Res. 2002, 1 (4), 291–298. https://doi.org/10.1111/j.1567-1364.2002.tb00047.x

80. Nokelainen M., Tu H., Vuorela A., Notbohm H., Kivirikko K. I., Myllyharju J. High-level production of human type I collagen in the yeast Pichia pastoris. Yeast. 2001, 18 (9), 797?806. https://doi.org/10.1002/yea.730

81. Toman P. D., Chisholm G., McMullin H., Giere L. M., Olsen D. R., Kovach R. J., Leigh S. D., Fong B. E., Chang R., Daniels G. A., Berg R. A., Hitzeman R. A. Production of recombinant human type I procollagen trimers using a four-gene expression system in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 2000, 275 (30), 23303?23309. https://doi.org/10.1074/jbc.M002284200

82. Werten M. W., Wisselink W. H., Jansen-van den Bosch T. J., de Bruin E. C., de Wolf F. A. Secreted production of a custom-designed, highly hydrophilic gelatin in Pichia pastoris. Protein Eng. 2001, 14 (6), 447?454. https://doi.org/10.1093/protein/14.6.447

83. Bulleid N. J., John D. C., Kadler K. E. Recombinant expression systems for the production of collagen. Biochem. Soc. Trans. 2000, 28 (4), 350?353. https://doi.org/10.1042/bst0280350

84. John D. C., Watson R., Kind A. J., Scott A. R., Kadler K. E., Bulleid N. J. Expression of an engineered form of recombinant procollagen in mouse milk. Nat. Biotechnol. 1999, 17 (4), 385?389. https://doi.org/10.1038/7945

85. Tomita M., Munetsuna H., Sato T., Adachi T., Hino R., Hayashi M., Shimizu K., Nakamura N., Tamura T., Yoshizato K. Transgenic silkworms produce recombinant human type III procollagen in cocoons. Nat. Biotechnol. 2003, 21 (1), 52?56. https://doi.org/10.1038/nbt771

86. Olsen D., Yang C., Bodo M., Chang R., Leigh S., Baez J., Carmichael D., Per?l? M., H?m?l?inen E. R., Jarvinen M., Polarek J. Recombinant collagen and gelatin for drug delivery. Adv. Drug. Deliv. Rev. 2003, 55 (12), 1547?1567. https://doi.org/10.1016/j.addr.2003.08.008

87. Merle C., Perret S., Lacour T., Jonval V., Hudaverdian S., Garrone R., Ruggiero F., Theisen M. Hydroxylated human homotrimeric collagen I in Agrobacterium tumefaciens-mediated transient expression and in transgenic tobacco plant. FEBS Lett. 2002, 515 (1?3), 114?118. https://doi.org/10.1016/S0014-5793(02)02452-3

88. Ruggiero F., Exposito J. Y., Bournat P., Gruber V., Perret S., Comte J., Olagnier B., Garrone R., Theisen M. Triple helix assembly and processing of human collagen produced in transgenic tobacco plants. FEBS Lett. 2000, 469 (1), 132?136. https://doi.org/10.1016/S0014-5793(00)01259-X

89. Pihlajaniemi T., Myllyla R., Kivirikko K. I. Prolyl 4-hydroxylase and its role in collagen synthesis. J. Hepatol. 1991, 13 (Suppl. 3), S2–7. https://doi.org/10.1016/0168-8278(91)90002-S

90. Yang C., Hillas P. J., B?ez J. A., Nokelainen M., Balan J., Tang J., Spiro R., Polarek J. W. The application of recombinant human collagen in tissue engineering. BioDrugs. 2004, 18 (2), 103?119. https://doi.org/10.2165/00063030-200418020-00004

91. Shoseyov O., Posen Y., Grynspan F. Human recombinant type I collagen produced in plants. Tissue Eng. Part A. 2013, 19 (13?14), 1527–1533. https://doi.org/10.1089/ten.tea.2012.0347

92. Wainwright D., Madden M., Luterman A., HuntJ., Monafo W., Heimbach D., Kagan R., Sittig K., Dimick A., Herndon D. Clinical evaluation of an acellular allograft dermal matrix in full-thickness burns. J. Burn. Care Rehabil. 1996, 17 (2), 124?136. https://doi.org/10.1097/00004630-199603000-00006

93. Karami A., Tebyanian H., Sayyad Soufdoost R., Motavallian E., Barkhordari A., Nourani M. R. Extraction and Characterization of Collagen with Cost-Effective Method from Human Placenta for Biomedical Applications. World J. Plast. Surg. 2019, 8 (3), 352?358. https://doi/org/10.29252/wjps.8.3.352

94. Shah V., Manekar A. Isolation and characterization of collagen from the placenta of buffalo (Bovidae bubalus bubalis) for the biomaterial applications. Trend in Life Sci. 2012, 1 (4), 26–32.

95. Gushhina Ju. Ju., Plokhov R. A., Zeveke A. V. Research of infl uence of irrigation, pH and modulators of proteoglycans on the morphology of the fi brils and collagen subfi brils. Bull. Nizhny Novgorod University. N. I. Lobachevsky. 2007, N 1, P. 114–118. (In Russian).

96. Lepetit J. Collagen contribution to meat toughness: Theoretical aspects. Meat. Sci. 2008, 80 (4), 960–967. https://doi.org/10.1016/j.meatsci.2008.06.016

97. Rizk M. A., Mostafa N. Y. Extraction and Characterization of Collagen from Buffalo Skin for Biomedical Applications. Orient. J. Chem. 2016, 32 (3). https://doi.org/10.13005/ojc/320336

98. Wallace D. G., Condell R. A., Donovan J. W., Paivinen A., Rhee W. M., Wade S. B. Multiple denaturational transitions in haracteri collagen. Biopolymers. 1986, 25 (10), 1875?1895. https://doi.org/10.1002/bip.360251006

99. Latorrea M. E., Lifschitzb A. L., Purslowc P. P. New recommendations for measuring collagen solubility. Meat. Sci. 2016, V. 118, 78–81.https://doi.org/10.1016/j.meatsci.2016.03.019

100. Mikhailov А. N. Chemistry and physics of skin collagen. Мoskva: Leg. Industrija. 1980, 232 р. (In Russian).

101. Zaides А. L. Collagen structure and its changes during processing. Мoskva: Leg. Industrija. 1972, 168 р. (In Russian).

102. Ignatieva N. Yu. Collagen – the main protein of the connective tissue (a review). Esteticheskaya medicina. 2005, 6 (3), 247–256.

103. Sarbon N. M., Cheow C. S., Kyaw Z. W., Howell N. K. Effects of different types and concentration of salt on the rheological and thermal properties of sin croaker and shortfin scad skin gelatin. Inter. Food Res. J. 2014, 21 (1), 317–324.

104. Vojdani F. Solubility. Methods of Testing Protein Functionality. Hall G. M. (Ed). London: St. Edmundsbury Press. 1996, Р. 11?60. https://doi.org/10.1007/978-1-4613-1219-2_2

105. Veeruraj A., Arumugam M., Balasubramanian T. Isolation and characterization of thermostable collagen from the marine eelfish (Evenchelys macrura). Process Biochem. 2013, 48 (10), 1592?1602. https://doi.org/10.1016/j.procbio.2013.07.011

106. Kittiphattanabawon P., Benjakul S., Visessanguan W., Kishimura H., Shahidi F. Isolation and haracterization of collagen from the skin of brownbanded bamboo shark (Chiloscyllium punctatum). Food Chem. 2010, 119 (4), 1519?1526. https://doi.org/10.1016/j.foodchem.2009.09.037

107. Zavareze E. R., Silva C. M., Mellado M. S., Hernandez C. P. Functionality of bluewing searobin (Prionotus punctatus) protein hydrolysates obtained from different microbial proteases. Qu?m. Nova. 2009, V. 32, P. 1739?1743. https://doi.org/10.1590/S0100-40422009000700011

108. Chakraborty P. D., De D., Bandyopadhyay S., Bhattacharyya D. Human aqueous placental extract as a wound healer. J. Wound. Care. 2009, 18 (11), 462?467.https://doi.org/10.12968/jowc.2009.18.11.44987

109. Datta P., Bhattacharyya D. In vitro growth inhibition of microbes by human placental extract. Curr. Sci. 2005, 88 (5), 782–786. Available from: http://www.jstor.org/stable/24111266

110. Metzmacher I., Ruth P., Abel M., Friess W. In vitro binding of matrix metalloproteinase-2 (MMP-2), MMP- 9, and bacterial collagenase on collagenous wound dressings. Wound Repair Regen. 2007, 15 (4), 549?555. https://doi.org/10.1111/j.1524-475X.2007.00263.x

111. Lund L. R., Romer J., Bugge T. H., Nielsen B. S., Frandsen T. L., Degen J. L., Stephens R. W., Dan? K. Functional overlap between two classes of matrix-degrading proteases in wound healing. EMBO J. 1999, 18 (17), 4645?4656. https://doi.org/10.1093/emboj/18.17.4645

112. Trengove N. J., Stacey M. C., MacAuley S., Bennett N., Gibson J., Burslem F., Murphy G., Schultz G. Analysis of the acute and chronic wound environments: the role of proteases and their inhibitors. Wound Repair Regen. 1999, 7 (6), 442?452. https://doi.org/10.1046/j.1524-475X.1999.00442.x

113. De D., Datta Chakraborty P., Mitra J., Sharma K., Mandal S., Das A., Chakrabarti S., Bhattacharyya D. Ubiquitin-like protein from human placental extract exhibits collagenase activity. PloS One. 2013, 8 (3), e59585. https://doi.org/10.1371/journal.pone.0059585

114. Kivirikko K. I. Biosynthesis of Collagen. In: Fricke R., Hartmann F. (eds) Connective Tissues. Springer, Berlin, Heidelberg. 1974, P. 107?121. https://doi.org/10.1007/978-3-642-61932-8_14

115. Myllyl? R., Tuderman L., Kivirikko K. I. Mechanism of the prolyl hydroxylase reaction. 2. Kinetic analysis of the reaction sequence. Eur. J. Biochem. 1977, 80 (2), 349?357. https://doi.org/10.1111/j.1432-1033.1977.tb11889.x

116. Tuderman L., Kivirikko K. I., Prockop D. J. Partial purification and characterization of a neutral protease which cleaves the N-terminal propeptides from procollagen. Biochemistry. 1978, 17 (15), 2948–2954. https://doi.org/10.1021/bi00608a002

117. Repin N. V., Chizh Yu. A., Marchenko L. N., Govorukha T. P. Morphological Characteristics of Aortal Endothelium in Rats with Renal Insufficiency after Allogenic Placental Cryoextract Correction. JMBS. 2020, 5 (4), 379–338. https://doi.org/10.26693/jmbs05.04.379

118. Vaskovych A. M., Repin M. V., Marchenk L. M., Govorukha T. P., Pasieshvili N. M. Nephroprotective Effect of Placental Cryoextract When Simulating Acute Renal Failure in Rats. Probl. Cryobiol. Cryomed. 2019, 29 (2), 183. https://doi.org/10.15407/cryo29.02.183

119. Rozanova S., Cherkashina Y., Repina S., Rozanova K., Nardid O. Protective effect of placenta extracts against nitrite-induced oxidative stress in human erythrocytes. Cell Mol. Biol. Lett. 2012, 17 (2), 240–248. https://doi.org/10.2478/s11658-012-0007-6

120. Moiseyeva N. N., Gorina O. L., Nikolchenko A. Yu., Shchenyavsky I. I. Comparative Evaluation of Biological Activity of Fraction Below 5 kDa from Cattle Cord Blood After Low-Temperature Storage (at -80 °C) or Lyophilization to Treat Burn Wounds in Rats. Probl. Cryobiol. Cryomed. 2020, 30 (1), 47–57. https://doi.org/10.15407/cryo30.01.047

121. Gulevsky O. K., Schenyavsky I. I. Antihypoxant Activity of Low Molecular Weight Fraction Bovine Blood Cryohemolysate at Different Stages of Ontogenesis. Probl. Cryobiol. Cryomed. 2017, 27 (1), 41–50. https://doi.org/10.15407/cryo27.01.041

122. Gulevsky A. K., Abakumowa E. S., Shenyavsky I. I. Biological activity of low molecular weight fraction obtained from cord and peripheral blood in cows of different ages. Fiziol. Zh. 2017, 63 (2), 73–79. (In Ukrainian). https://doi.org/10.15407/fz63.02.073