Hyaluronic Acid: The Reason for Its Variety of Physiological and Biochemical Functional Properties

Author(s): Rami Al-Khateeb*, Jelena Prpic.

Journal Name: Applied Clinical Research, Clinical Trials and Regulatory Affairs

Volume 6 , Issue 2 , 2019

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Abstract:

Introduction: Many physicians may be unfamiliar with the importance of hyaluronic acid (HA) and its physiological and biochemical functions at cellular level. Despite the vast number of published studies using HA in medical treatments, it is still difficult for the reader to clearly distinguish the different types of HA employed in different medical applications. In addition, published studies do not mention the exact type of HA used or its biochemical properties. Usually, a study mentions only its molecular weight and concentration, which are insufficient to know its exact designed properties or to make a comparison with other types of HA.

Methodology: This article is intended to summarise the information about native and modified HAs with a focus on explaining their different physiological and biochemical functions in the human body, their different commercially available types, and how they affect the associated medical applications. The goal is to provide a basis to researchers and physicians for distinguishing different types of HA and their properties in order to enhance physicians’ clinical practice in terms of application of different types of HA to treatments and to help the international research community to change the reporting of HA characteristics in published papers. This is necessary to enhance future acquisition of data, with the ability to create an HA data bank for further research and as a reference for different HA types and their medical applications.

Conclusion: These developments should enhance the scientific and clinical knowledge about HA. Furthermore, the overall approach in this paper can be applied to other similar substances.

Keywords: Hyaluronic acid, hyaluronan, hyaluronan cross-linking, hyaluronan hydrogel, hyaluronan molecular weight, hyaluronan synthesis, hyaluronan degradation, hyaluronidase, extracellular matrix, glycosaminoglycan, hyaluronan modification, hyaluronan medical applications, hyaluronan production, hyaluronan cellular functions, hyaluronan physiochemical functions.

[1]
Chong B, Blank L, Mclaughlin R, Nielsen L. Microbial hyaluronic acid production. App Microbiol Biotechnol 2004; 66(4): 341-51.
[2]
Boeriu C, Springer J, Kooy F, van den Broek L, Eggink G. Production methods for hyaluronan. Int J Carbohyd Chem 2013; 2013: 1-14.
[3]
Taylor S. Advances in food and nutrition research. 1st ed. Saint Louis: Elsevier Science 2014.
[4]
Kuo J, Prestwich GD. Hyaluronic acid. In: Ducheyne P, Healey KE, Hutmacher DW, Grainger DW, Kirkpatrick CJ, Eds. Comprehensive Biomaterials Amsterdem. Boston: Elsevier 2011; pp. 239-59.
[5]
Garg H, Hales C. Chemistry and biology of hyaluronan. 1st ed. Amsterdam: Elsevier 2008.
[6]
Necas J, Bartosikova L, Brauner P, Kolar J. Hyaluronic acid (hyaluronan): A review. Vet Med 2008; 53(8): 397-411.
[7]
Bradshaw R, Stahl P. Encyclopedia of cell biology. Oxford: Elsevier Inc. 2016.
[8]
Collins M, Birkinshaw C. Hyaluronic acid based scaffolds for tissue engineering- A review. Carbohyd Poly 2013; 92(2): 1262-79.
[9]
Vigier S, Fülöp T. Exploring the extracellular matrix to create biomaterials. In: Travascio F, Ed. Composition and function of the extracellular matrix in the human body. IntechOpen 2016.
[10]
Wight T. Provisional matrix: A role for versican and hyaluronan. Matrix Biol 2017; 60-61: 38-56.
[11]
DeAngelis P. Evolution of glycosaminoglycans and their glycosyltransferases: Implications for the extracellular matrices of animals and the capsules of pathogenic bacteria. Anat Rec 2002; 268(3): 317-26.
[12]
Pollard T, Earnshaw W, Johnson G, Lippincott-Schwartz J. Cell biology. 3rd ed. Philadelphia: Elsevier Inc. 2016.
[13]
Hubbard T, Murzin A, Brenner S, Chothia C. SCOP: A structural classification of Proteins database. Nucleic Acids Res 1997; 25(1): 236-9.
[14]
Yella J, Yaddanapudi S, Wang Y, Jegga A. Changing trends in computational drug repositioning. Pharmaceuticals 2018; 11(2): 57.
[15]
Thul P, Lindskog C. The human protein atlas: A spatial map of the human proteome. Protein Sci 2017; 27(1): 233-44.
[16]
Thul P, Åkesson L, Wiking M, et al. A subcellular map of the human proteome. Science 2017; 356(6340)eaal3321
[17]
Kogan G, Šoltés L, Stern R, Gemeiner P. Hyaluronic acid: A natural biopolymer with a broad range of biobiomedical and industrial applications. Biotechnol Lett 2006; 29(1): 17-25.
[18]
Stern R, Jedrzejas M. Hyaluronidases: Their genomics, structures, and mechanisms of action. Chem Rev 2006; 106(3): 818-39.
[19]
Fraser J, Laurent T, Laurent U. Hyaluronan: Its nature, distribution, functions and turnover. J Intern Med 1997; 242(1): 27-33.
[20]
Fakhari A, Berkland C. Applications and emerging trends of hyaluronic acid in tissue engineering, as a dermal filler and in osteoarthritis treatment. Acta Biomaterialia 2013; 9(7): 7081-92.
[21]
Becker L, Bergfeld W, Belsito D, et al. Final report of the safety assessment of hyaluronic acid, potassium hyaluronate, and sodium hyaluronate. Int J Toxicol 2009; 28((4_suppl)): 5-67.
[22]
Cowman M, Lee H, Schwertfeger K, McCarthy J, Turley E. The content and size of hyaluronan in biological fluids and tissues. Front Immunol 2015; 6: 261.
[23]
Sasaki E, Matsuo K, Iida A, et al. A Novel mouse model for phenytoin-induced liver injury: Involvement of immune-related factors and P450-mediated metabolism. Toxicol Sci 2013; 136(1): 250-63.
[24]
Kalcheim C, Duksin D, Bachar E, Vogel Z. Collagen-stimulating factor from embryonic brain has ascorbate-like activity and stimulates prolyl hydroxylation in cultured muscle cells. Eur J Biochem 1985; 146(1): 227-32.
[25]
Binninger E, Schachtschabel D. Stimulatory effects of ascorbic acid on hyaluronic acid synthesis of in vitro cultured normal and glaucomatous trabecular meshwork cells of the human eye. Z Gerontol 1993; 26(4): 243-6.
[26]
Swann D. The degradation of hyaluronic acid by ascorbic acid. Biochem J 1967; 102(3): 42C-4C.
[27]
Aleksiewicz R, Lutnicki K, Komsta R, Kostro K. Application of hyaluronic acid sodium salt and vitamin C in the therapy of dogs with hypertrophic osteodystrophy. J Vet Res 2013; 57(2): 249-55.
[28]
Botzki A, Rigden D, Braun S, et al. l-ascorbic acid 6-hexadecanoate, a potent hyaluronidase inhibitor. J Biol Chem 2004; 279(44): 45990-7.
[29]
Kano M, Haga K, Miyazaki K, Ishikawa F. Daily consumption of fermented soymilk helps to improve facial wrinkles in healthy postmenopausal women in a randomized, parallel-group, open-label trial. Func Foods Health Dis 2018; 8(2): 107-21.
[30]
Südel K, Venzke K, Mielke H, et al. Novel aspects of intrinsic and extrinsic aging of human skin: Beneficial effects of soy extract. Photochem Photobiol 2005; 81(3): 581.
[31]
Parashar P, Rathor M, Dwivedi M, Saraf S. Hyaluronic acid decorated naringenin nanoparticles: Appraisal of chemopreventive and curative potential for lung cancer. Pharmaceutics 2018; 10(1): 33.
[32]
Karim S, Alexandrine F, Gaston G. Magnesium and connective tissue. Magnesium Res 2003; 16(1): 70-4.
[33]
Campo R. Effects of cations on cartilage structure: Swelling of growth plate and degradation of proteoglycans induced by chelators of divalent cations. Calcified Tissue Int 1988; 43(2): 108-21.
[34]
Wang X, Ackermann M, Tolba E, et al. Artificial cartilage bio-matrix formed of hyaluronic acid and Mg2+-polyphosphate. Eur Cell Mat 2016; 32: 271-83.
[35]
Lee J, Spicer A. Hyaluronan: A multifunctional, megaDalton, stealth molecule. Curr Opin Cell Biol 2000; 12(5): 581-6.
[36]
Stern R, Asari A, Sugahara K. Hyaluronan fragments: An information-rich system. Eur J Cell Biol 2006; 85(8): 699-715.
[37]
Tsepilov R, Beloded A. Hyaluronic acid- an “old” molecule with “new” functions: Biosynthesis and depolymerization of hyaluronic acid in bacteria and vertebrate tissues including during carcinogenesis. Biochemistry (Moscow) 2015; 80(9): 1093-108.
[38]
Vigetti D, Viola M, Karousou E, De Luca G, Passi A. Metabolic control of hyaluronan synthases. Matrix Biol 2014; 35: 8-13.
[39]
Dicker K, Gurski L, Pradhan-Bhatt S, Witt R, Farach-Carson M, Jia X. Hyaluronan: A simple polysaccharide with diverse biological functions. Acta Biomater 2014; 10(4): 1558-70.
[40]
Tammi R, Passi A, Rilla K, et al. Transcriptional and post-translational regulation of hyaluronan synthesis. FEBS J 2011; 278(9): 1419-28.
[41]
Tammi M, Day A, Turley E. Hyaluronan and homeostasis: A balancing act. J Biol Chem 2001; 277(7): 4581-4.
[42]
Toole B. Hyaluronan: From extracellular glue to pericellular cue. Nat Rev Cancer 2004; 4(7): 528-39.
[43]
Laurent T, Laurent U, Fraser J. Functions of hyaluronan. Annal Rheumatic Dis 1995; 54(5): 429-32.
[44]
Borzacchiello A, Mayol L, Ambrosio L, Gärskog O, Dahlqvist Å. Rheological characterization of vocal folds after injection augmentation in a preliminary animal study. J Bioact Compat Pol 2004; 19(4): 331-41.
[45]
David I. Hyaluronan for knee OA, facts vs. myths. In: Casebook of Orthopedic Rehabilitation. Berlin, Heidelberg: Springer 2008; pp. 99-101.
[46]
Mathias A, Antos L, Lovisa R, Johanna M, Victor S. Mapping the intrinsic viscosity of hyaluronic acid at high concentration of OH Uppsala Universitet; 2017 Available from: http://www.diva-portal.org/smash/ get/diva2:1114201/FULL TEXT01.pdf
[47]
Huang L, Grammatikakis N, Yoneda M, Banerjee S, Toole B. Molecular characterization of a novel intracellular hyaluronan-binding protein. J Biol Chem 2000; 275(38): 29829-39.
[48]
Shimoda M, Yoshida H, Mizuno S, et al. Hyaluronan-binding protein involved in hyaluronan depolymerization controls endochondral ossification through hyaluronan metabolism. Am J Pathol 2017; 187(5): 1162-76.
[49]
Siódmiak J, Bełdowski P, Augé W, Ledziński D, Śmigiel S, Gadomski A. Molecular dynamic analysis of hyaluronic acid and phospholipid interaction in tribological surgical adjuvant design for osteoarthritis. Molecules 2017; 22(9): 1436.
[50]
Ishikawa M, Sawada Y, Yoshitomi T. Structure and function of the interphotoreceptor matrix surrounding retinal photoreceptor cells. Exp Eye Res 2015; 133: 3-18.
[51]
Hollyfield J, Rayborn M, Tammi M, Tammi R. Hyaluronan in the interphotoreceptor matrix of the eye: Species differences in content, distribution, ligand binding and degradation. Exp Eye Res 1998; 66(2): 241-8.
[52]
Jiang D, Liang J, Noble P. Hyaluronan as an immune regulator in human diseases. Physiol Rev 2011; 91(1): 221-64.
[53]
Bertl K, Bruckmann C, Isberg P, Klinge B, Gotfredsen K, Stavropoulos A. Hyaluronan in non-surgical and surgical periodontal therapy: A systematic review. J Clin Periodontol 2015; 42(3): 236-46.
[54]
Dahiya P, Kamal R. Hyaluronic acid: A boon in periodontal therapy. N Am J Med Sci 2013; 5(5): 309.
[55]
Pogrel M, Lowe M, Stern R. Hyaluronan (hyaluronic acid) in human saliva. Arch Oral Biol 1996; 41(7): 667-71.
[56]
Yıldırım S, Özener H, Doğan B, Kuru B. Effect of topically-applied hyaluronic-acid on pain and palatal epithelial wound healing: An examiner-blind, randomized, controlled clinical trial. J Periodontol 2018; 89(1): 36-45.
[57]
Hancock J. Cell signalling. 4th ed. Oxford University Press 2017.
[58]
Naish J, Syndercombe CD. Medical sciences. Edinburgh: Saunders/Elsevier 2015.
[59]
Lucas K, Pitari G, Kazerounian S, et al. Guanyly cyclases and signaling by cyclic GMP. Pharmacol Rev 2000; 52(3): 375-414.
[60]
Xu Y, Fisher G. Receptor type protein tyrosine phosphatases (RPTPs)- roles in signal transduction and human disease. J Cell Commun Signal 2012; 6(3): 125-38.
[61]
Kahmann J, O’Brien R, Werner J, et al. Localization and characterization of the hyaluronan-binding site on the link module from human TSG-6. Structure 2000; 8(7): 763-74.
[62]
Day A, Prestwich G. Hyaluronan-binding proteins: Tying up the giant. J Biol Chem 2001; 277(7): 4585-8.
[63]
Karamanos N, Piperigkou Z, Theocharis A, et al. Proteoglycan chemical diversity drives multifunctional cell regulation and therapeutics. Chem Rev 2018; 118(18): 9152-232.
[64]
Kent W. The human genome browser at UCSC. Genome Res 2002; 12(6): 996-1006.
[65]
Funahashi A, Matsuoka Y, Jouraku A, Morohashi M, Kikuchi N, Kitano H. CellDesigner 3.5: A versatile modeling tool for biochemical networks. Proc IEEE 2008; 96(8): 1254-65.
[66]
Oda K, Kitano H. A comprehensive map of the toll-like receptor signaling network. Mol Syst Biol 2006; 2: 2006.0015.
[67]
Cosic I, Cosic D, Lazar K. environmental light and its relationship with electromagnetic resonances of biomolecular interactions, as predicted by the resonant recognition model. Int J Environ Res Public Health 2016; 13(7): 647.
[68]
Cosic I, Cosic D, Lazar K. Is it possible to predict electromagnetic resonances in proteins, DNA and RNA? EPJ Nonlinear Biomedical Physics 2015; 3(1): 5.
[69]
Zwinkels J. Light, electromagnetic spectrum. In: Encyclopedia of Color Science and Technology. New York: Springer 2015; pp. 1-8.
[70]
Chen W, Abatangelo G. Functions of hyaluronan in wound repair. Wound Repair Regen 1999; 7(2): 79-89.
[71]
David-Raoudi M, Tranchepain F, Deschrevel B, et al. Differential effects of hyaluronan and its fragments on fibroblasts: Relation to wound healing. Wound Repair Regen 2008; 16(2): 274-87.
[72]
Aya K, Stern R. Hyaluronan in wound healing: Rediscovering a major player. Wound Repair Regen 2014; 22(5): 579-93.
[73]
Scotti L, Kumar SR, Mitsugu IH, et al. Recent advancement in natural hyaluronidase inhibitors. Curr Topics in Med Chem 2016; 16(23): 2525-31.
[74]
Sze J, Brownlie J, Love C. Biotechnological production of hyaluronic acid: A mini review. 3 Biotech 2016; 6(1): 67.
[75]
Liu L, Liu Y, Li J, Du G, Chen J. Microbial production of hyaluronic acid: Current state, challenges, and perspectives. Microb Cell Fact 2011; 10(1): 99.
[76]
Ardizzoni A, Neglia R, Baschieri M, et al. Influence of hyaluronic acid on bacterial and fungal species, including clinically relevant opportunistic pathogens. ‎. J Mater Sci Mater Med 2011; 22(10): 2329-38.
[77]
Kuo J. Practical aspects of hyaluronan based medical products. Boca Raton: CRC/Taylor & Francis 2006.
[78]
Khabarov V, Boykov P, Selyanin M, Polyak F. Hyaluronic acid: Production, properties, application in biology and medicine. 1st ed. John Wiley & Sons 2015; pp. 97-119.
[79]
Collins M. Hyaluronic acid for biomedical and pharmaceutical applications. Smithers Rapra 2014.
[80]
Schanté C, Zuber G, Herlin C, Vandamme T. Chemical modifications of hyaluronic acid for the synthesis of derivatives for a broad range of biomedical applications. Carbohydr Poly 2011; 85(3): 469-89.
[81]
Burdick J, Prestwich G. Hyaluronic acid hydrogels for biomedical applications. Adv Mater 2011; 23(12): H41-56.
[82]
Yang R, Tan L, Cen L, Zhang Z. An injectable scaffold based on crosslinked hyaluronic acid gel for tissue regeneration. RSC Adv 2016; 6(20): 16838-50.
[83]
Hertegård S, Dahlqvist Å, Laurent C, Borzacchiello A, Ambrosio L. Viscoelastic properties of rabbit vocal folds after augmentation. J Otolaryngol Head Neck Surg 2003; 128(3): 401-6.
[84]
Borzacchiello A, Russo L, Malle B, Schwach-Abdellaoui K, Ambrosio L. Hyaluronic acid based hydrogels for regenerative medicine applications. BioMed Res Int 2015; 2015: 1-12.
[85]
Gřundělová L, Gregorova A, Mráček A, Vícha R, Smolka P, Minařík A. Viscoelastic and mechanical properties of hyaluronan films and hydrogels modified by carbodiimide. Carbohydr Polym 2015; 119: 142-8.
[86]
Mendez-Vilas A, Solano A. Polymer science: Research advances, practical applications and educational aspects. 1st ed. Formatex Research Center 2016.[Cited: 9 March 2019]. Available from:. http://www.formatex.org/polymerscience1/
[87]
Chiara S, Annalisa La G, Mario De R. Biotechnological production and application of hyaluronan. INTECH Open Access Publisher 2010.
[88]
Salzillo R, Schiraldi C, Corsuto L, et al. Optimization of hyaluronan-based eye drop formulations. Carbohydr Polym 2016; 153: 275-83.
[89]
Liu J, Zheng H, Poh P, Machens H, Schilling A. Hydrogels for engineering of perfusable vascular networks. International J Mol Sci 2015; 16(7): 15997-6016.
[90]
Chun K, Choi H, Lee J. Comparison of mechanical property and role between enamel and dentin in the human teeth. J Dental Biomech 2014; 5
[http://dx.doi.org/10.1177/1758736014520809]
[91]
Carter F, Frank T, Davies P, McLean D, Cuschieri A. Measurements and modelling of the compliance of human and porcine organs. Med Image Anal 2001; 5(4): 231-6.
[92]
Seedhom B, Berry E, Ostell A, Cuppone M. The longitudinal youngs modulus of cortical bone in the midshaft of human femur and its correlation with CT scanning data. Calcified Tissue Int 2004; 74(3): 302-9.
[93]
Boschetti F, Pennati G, Gerraso F, Peretti G, Dubini G. Biomechanical properties of human articular cartilage under compressive loads. Biorheology 2004; 41(3-4): 159-66.


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Article Details

VOLUME: 6
ISSUE: 2
Year: 2019
Page: [112 - 159]
Pages: 48
DOI: 10.2174/2213476X06666190405094637

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