Sterilization and low temperature effects on regenerative potential of hyaluronic acid
DOI:
https://doi.org/10.15407/cryo35.02.068Keywords:
hyaluronic acid, low temperature exposure, preservation of regenerative properties, sterilizationAbstract
Due to its physical properties and pharmacological activity, hyaluronic acid (HA) has considerable potential for use in cryobiology and cryomedicine. The aim of the study was to create a method for sterilizing aqueous solutions of HA that does not reduce its regenerative properties, and to study the effect of low temperatures on their preservation. For the sterilization of aqueous solutions of HA, a gentle sterilization regimen — tyndallization — was proposed, which at the same time ensures the sterility of the solutions and does not affect their regenerative properties. The effects of tyndallization and low temperatures on the preservation of the regenerative properties of 1 and 2% aqueous solutions of HA of different molecular weights: low molecular weight (LMW HA) (<100 kDa) and high molecular weight (HMW HA) (>2000 kDa) was studied in an animal model of excision wound healing. It has been shown that low temperatures do not change the regenerative properties of HMW HA and LMW HA (even in the thermocycling mode), which opens up wide possibilities for use in cryobiology and cryomedicine.
Probl Cryobiol Cryomed 2025; 35(2):68–75
References
Asadpour R, Aminirad M, Rahbar M, et al. Effects of hyaluronic acid on sperm parameters, mitochondrial function and apoptosis of spermatozoa in Simmental bulls with good and poor freezing ability. J Anim Physiol Anim Nutr (Berl). 2024; 108(2): 383-94. CrossRef
Bohaumilitzky L, Huber AK, Stork EM, et al. Trickster in disguise: Hyaluronan's ambivalent roles in the matrix. Front Oncol [Internet]. 2017 Oct 9 [cited 2024 Jul 2]; 7: 242. Available from: https://www.frontiersin.org/journals/oncology/articles/10.3389/fonc.2017.00242/full CrossRef
Bukhari SNA, Roswandi NL, Waqas M, et al. Hyaluronic acid, a promising skin rejuvenating biomedicine: A review of recent updates and pre-clinical and clinical investigations on cosmetic and nutricosmetic effects. Int J Biol Macromol. 2018; 120(Pt B): 1682-95. CrossRef
Collins MN, Birkinshaw C. Comparison of the effectiveness of four different crosslinking agents with hyaluronic acid hydrogel films for tissue-culture applications. J Appl Polym Sci. 2007; 104(5): 3183-91. CrossRef
Cui N, Qian J, Liu T, et al. Hyaluronic acid hydrogel scaffolds with a triple degradation behavior for bone tissue engineering. Carbohydr Polym. 2015; 126: 192-8. CrossRef
Cyphert JM, Trempus CS, Garantziotis S. Size matters: molecular weight specificity of hyaluronan effects in cell biology. Int J Cell Biol [Internet]. 2015 Sep 10 [cited 2024 Aug 4]; 2015: 563818. Available from: https://onlinelibrary.wiley.com/doi/epdf/10.1155/2015/563818 CrossRef
Dong Y, Cui M, Qu J, et al. Conformable hyaluronic acid hydrogel delivers adipose-derived stem cells and promotes regeneration of burn injury. Acta Biomater. 2020; 108: 56-66. CrossRef
Evanko SP, Wight TN. Intracellular localization of hyaluronan in proliferating cells. J Histochem Cytochem. 1999; 47(10): 1331-42. CrossRef
Fallacara A, Baldini E, Manfredini S, Vertuani S. Hyaluronic acid in the third millennium. Polymers [Internet]. 2018 Jun 25 [cited 2024 Jul 4]; 10: 701. Available from: https://www.mdpi.com/2073-4360/10/7/701 CrossRef
Gallorini M, Antonetti Lamorgese Passeri C, Cataldi A, et al. Hyaluronic acid alleviates oxidative stress and apoptosis in human tenocytes via Caspase 3 and 7. Int J Mol Sci [Internet]. 2022 Aug 8 [cited 2024 Jul 2]; 23(15): 8817. Available from: https://www.mdpi.com/1422-0067/23/15/8817 CrossRef
Gupta RC, Lall R, Srivastava A, Sinha A. Hyaluronic acid: molecular mechanisms and therapeutic trajectory. Front Vet Sci [Internet]. 2019 Jun 25 [cited 2024 Jul 12]; 6: 192. Available from: https://www.frontiersin.org/journals/veterinary-science/articles/10.3389/fvets.2019.00192/full CrossRef
Hascall VC, Majors AK, De La Motte CA, et al. Intracellular hyaluronan: a new frontier for inflammation? Biochim Biophys Acta. 2004; 1673(1-2): 3-12. CrossRef
Hauck S, Zager P, Halfter N, et al. Collagen/hyaluronan based hydrogels releasing sulfated hyaluronan improve dermal wound healing in diabetic mice via reducing inflammatory macrophage activity. Bioact Mater. 2021; 6(12): 4342-59. CrossRef
Huang G, Huang H. Application of hyaluronic acid as carriers in drug delivery. Drug Deliv. 2018; 25(1): 766-72. CrossRef
Hwang HS, Lee CS. Recent progress in hyaluronic-acid-based hydrogels for bone tissue engineering. Gels [Internet]. 2023 Jul 21 [cited 2024 Aug 12]; 9(7): 588. Available from: https://www.mdpi.com/2310-2861/9/7/588 CrossRef
Knudson W, Ishizuka S, Terabe K, et al. The pericellular hyaluronan of articular chondrocytes. Matrix Biol. 2019; 78-79: 32-46. CrossRef
Kwon MY, Wang C, Galarraga JH, et al. Influence of hyaluronic acid modification on CD44 binding towards the design of hydrogel biomaterials. Biomaterials [Internet]. 2019 Nov [cited 2024 Sep 2]; 222: 119451. Available from: https://www.sciencedirect.com/science/article/abs/pii/S0142961219305502 CrossRef
Litwiniuk M, Krejner A, Speyrer MS, et al. Hyaluronic Acid in Inflammation and Tissue Regeneration. Wounds. 2016; 28(3): 78-88. PubMed
Long C, Peng H, Yang W, et al. Targeted delivery of gemcitabine for precision therapy of cholangiocarcinoma using hyaluronic acid-modified metal-organic framework nanoparticles. ACS Omega. 2024; 9(10): 11998-2005. CrossRef
Luo Y, Prestwich GD. Synthesis and selective cytotoxicity of a hyaluronic acid-antitumor bioconjugate. Bioconjug Chem. 1999; 10(5): 755-63. CrossRef
Marcotti S, Maki K, Reilly GC, et al. Hyaluronic acid selective anchoring to the cytoskeleton: An atomic force microscopy study. PLoS One [Internet]. 2018 Oct 25 [cited 2024 Sep 2]; 13(10): e0206056. Available from: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0206056 CrossRef
Marei WFA, Raheem KA, Salavati M, et al. Hyaluronan and hyaluronidase, which is better for embryo development? Theriogenology. 2016; 86(4): 940-48. CrossRef
Marinho A, Nunes C, Reis S. Hyaluronic acid: a key ingredient in the therapy of inflammation. Biomolecules [Internet]. 2021 Oct 15 [cited 2024 Sep 3]; 11(10): 1518. Available from: https://www.mdpi.com/2218-273X/11/10/1518 CrossRef
Mondek J, Kalina M, Simulescu V, et al. Thermal degradation of high molar mass hyaluronan in solution and in powder; comparison with BSA. Polym. Degrad. Stabil. 2015; 120: 107-13. CrossRef
Munesada D, Sakai D, Nakamura Y, et al. Investigation of the mitigation of dmso-induced cytotoxicity by hyaluronic acid following cryopreservation of human nucleus pulposus cells. Int J Mol Sci [Internet]. 2023 Jul 31 [cited 2024 Sep 6]; 24(15): 12289. Available from: https://www.mdpi.com/1422-0067/24/15/12289 CrossRef
Papakonstantinou E, Roth M, Karakiulakis G. Hyaluronic acid: A key molecule in skin aging. Dermatoendocrinol. 2012; 4(3): 253-8. CrossRef
Pilbauerova N, Schmidt J, Soukup T, et al. Innovative approach in the cryogenic freezing medium for mesenchymal stem cells. Biomolecules [Internet]. 2022 Apr 20 [cited 2024 Sep 3]; 12(5): 610. Available from: https://www.mdpi.com/2218-273X/12/5/610 CrossRef
Sanchez DC, Ocampo BRY, Chirino, CAE. Use of hyaluronic acid as an alternative for reconstruction of interdental papilla. Rev. Odontol. Mex. 2017; 21(3): 199-207. CrossRef
Sapudom J, Müller CD, Nguyen KT, et al. Matrix remodeling and hyaluronan production by myofibroblasts and cancer-associated fibroblasts in 3D collagen matrices. Gels [Internet]. 2020 Sep 30 [cited 2024 Sep 4]; 6(4): 33. Available from: https://www.mdpi.com/2310-2861/6/4/33 CrossRef
Sharma S, Kishen A. Bioarchitectural design of bioactive biopolymers: structure-function paradigm for diabetic wound healing. Biomimetics (Basel) [Internet]. 2024 May 4 [cited 2024 Sep 4]; 9(5): 275. Available from: https://www.mdpi.com/2313-7673/9/5/275 CrossRef
Singampalli KL, Balaji S, Wang X, et al. The Role of an IL-10/hyaluronan axis in dermal wound healing. Front Cell Dev Biol [Internet]. 2020 Jul 17 [cited 2024 Sep 2]; 8: 636. Available from: https://www.frontiersin.org/journals/cell-and-developmental-biology/articles/10.3389/fcell.2020.00636/full CrossRef
Snetkov P, Zakharova K, Morozkina S, et al. Hyaluronic acid: the influence of molecular weight on structural, physical, physico-chemical, and degradable properties of biopolymer. Polymers (Basel) [Internet]. 2020 Aug 20 [cited 2024 Sep 2]; 12(8): 1800. Available from: https://www.mdpi.com/2073-4360/12/8/1800 CrossRef
Stern R, Asari AA, Sugahara KN. Hyaluronan fragments: an information-rich system. Eur J Cell Biol. 2006; 85(8): 699-715. CrossRef
Stern R, Kogan G, Jedrzejas MJ, et al. The many ways to cleave hyaluronan. Biotechnol Adv. 2007; 25(6): 537-57. CrossRef
Sudhakar K, Ji SM, Kummara MR, Han SS. Recent progress on hyaluronan-based products for wound healing applications. Pharmaceutics [Internet]. 2022 Oct 19 [cited 2024 Aug 4]; 14(10): 2235. Available from: https://www.mdpi.com/1999-4923/14/10/2235 CrossRef
Takeo M, Lee W, Ito M. Wound healing and skin regeneration. Cold Spring Harb Perspect Med [Internet]. 2015 Jan 5 [cited 2024 Sep 3]; 5(1): a023267. Available from: https://pubmed.ncbi.nlm.nih.gov/25561722/ CrossRef
Trabucchi E, Pallotta S, Morini M, et al. Low molecular weight hyaluronic acid prevents oxygen free radical damage to granulation tissue during wound healing. Int J Tissue React. 2002; 24(2): 65-71.
Yang G, Guo X, Luan Y. The application on different molecular weight of sodium hyaluronate. Food Drug. 2005; 12: 1-3.
Ye J, Zhang H, Wu H, et al. Cytoprotective effect of hyaluronic acid and hydroxypropyl methylcellulose against DNA damage induced by thimerosal in Chang conjunctival cells. Graefes Arch Clin Exp Ophthalmol. 2012; 250(10): 1459-66. CrossRef
Yu CJ, Ko CJ, Hsieh CH, et al. Proteomic analysis of osteoarthritic chondrocyte reveals the hyaluronic acid-regulated proteins involved in chondroprotective effect under oxidative stress. J Proteomics. 2014; 99: 40-53. CrossRef
Zerbinati N, Sommatis S, Maccario C, et al. In vitro hair growth promoting effect of a noncrosslinked hyaluronic acid in human dermal papilla cells. Biomed Res Int [Internet]. 2021 Oct 21 [cited 2024 Aug 4]; 2021: 5598110. Available from: https://onlinelibrary.wiley.com/doi/10.1155/2021/5598110 CrossRef
Zhai P, Peng X, Li B, et al. The application of hyaluronic acid in bone regeneration. Int J Biol Macromol. 2020; 151: 1224-39. CrossRef
Ziegelaar BW, Aigner J, Staudenmaier R, et al. The characterisation of human respiratory epithelial cells cultured on resorbable scaffolds: first steps towards a tissue engineered tracheal replacement. Biomaterials. 2002; 23(6): 1425-38. CrossRef
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