Student or educator? Sign up with your school email and get 6 months of Pro free.
CoChat
Sign Up
Cited by 860

The DOI matches its Crossref record; 8 of the 8 references it cites were found in a registry or an index.

Hyaluronic Acid in the Third Millennium

Open access
Fallacara, Arianna, Baldini, Erika, Manfredini, Stefano, Vertuani, Silvia·2018·Polymers
DOI 10.3390/polym10070701

Published version of a preprint

Open this paper in CoChat — free account

Abstract

Since its first isolation in 1934, hyaluronic acid (HA) has been studied across a variety of research areas. This unbranched glycosaminoglycan consisting of repeating disaccharide units of N-acetyl-d-glucosamine and d-glucuronic acid is almost ubiquitous in humans and in other vertebrates. HA is involved in many key processes, including cell signaling, wound reparation, tissue regeneration, morphogenesis, matrix organization and pathobiology, and has unique physico-chemical properties, such as biocompatibility, biodegradability, mucoadhesivity, hygroscopicity and viscoelasticity. For these reasons, exogenous HA has been investigated as a drug delivery system and treatment in cancer, ophthalmology, arthrology, pneumology, rhinology, urology, aesthetic medicine and cosmetics. To improve and customize its properties and applications, HA can be subjected to chemical modifications: conjugation and crosslinking. The present review gives an overview regarding HA, describing its history, physico-chemical, structural and hydrodynamic properties and biology (occurrence, biosynthesis (by hyaluronan synthases), degradation (by hyaluronidases and oxidative stress), roles, mechanisms of action and receptors). Furthermore, both conventional and recently emerging methods developed for the industrial production of HA and its chemical derivatization are presented. Finally, the medical, pharmaceutical and cosmetic applications of HA and its derivatives are reviewed, reporting examples of HA-based products that currently are on the market or are undergoing further investigations.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/polym10070701

Cites

8 of 8 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 8 references

Research works printed but not linked: 245

  1. Boeriu, 2013, Production methods for hyaluronan, Int. J. Carbohydr. Chem., 2013, 14, 10.1155/2013/624967 · DOI · Paper page
  2. Meyer, 1934, The polysaccharide of the vitrous humor, J. Biol. Chem., 107, 629, 10.1016/S0021-9258(18)75338-6 · DOI · Paper page
  3. Kendall, 1937, A serologically inactive polysaccharide elaborated by mucoid strains of group a hemolytic streptococcus, J. Biol. Chem., 118, 61, 10.1016/S0021-9258(18)74517-1 · DOI · Paper page
  4. Boas, 1949, Isolation of hyaluronic acid from the cock’s comb, J. Biol. Chem., 181, 573, 10.1016/S0021-9258(18)56578-9 · doi:10.1016/s0021-9258(18)56578-9
  5. Kaye, 1950, Observations on the chemistry of hyaluronic acid, Biochem. J., 2, 13
  6. Meyer, 1948, Highly viscous sodium hyaluronate, J. Biol. Chem., 176, 993, 10.1016/S0021-9258(19)52716-8 · doi:10.1016/s0021-9258(19)52716-8
  7. Varga, 1955, Studies on hyaluronic acid prepared from the vitreous body, J. Biol. Chem., 217, 651, 10.1016/S0021-9258(18)65930-7 · DOI
  8. Fletcher, 1955, Viscosity studies on hyaluronic acid of synovial fluid in rheumatoid arthritis and osteoarthritis, Clin. Sci., 14, 653
  9. Blumberg, 1958, Physicochemical properties of hyaluronic acid formed by Streptococcus haemolyticus, Biochem. J., 70, 1, 10.1042/bj0700001 · doi:10.1042/bj0700001
  10. Weissmann, 1954, The structure of hyalobiuronic acid and of hyaluronic acid from umbilical cord, J. Am. Chem. Soc., 76, 1753, 10.1021/ja01636a010 · DOI · Paper page
  11. Meyer, 1947, The biological significance of hyaluronic acid and hyaluronidase, Physiol. Rev., 27, 335, 10.1152/physrev.1947.27.3.335 · DOI
  12. Ogston, 1953, The physiological function of hyaluronic acid in synovial fluid; viscous, elastic and lubricant properties, J. Physiol., 119, 244, 10.1113/jphysiol.1953.sp004842 · DOI · Paper page
  13. Pinkus, 1953, The influence of hyaluronic acid and other substances on tensile strength of healing wounds, J. Investig. Dermatol., 21, 365, 10.1038/jid.1953.116 · doi:10.1038/jid.1953.116
  14. Miller, 1980, Use of Na-hyaluronate in anterior segment eye surgery, J. Am. Intraocul. Implant Soc., 6, 13, 10.1016/S0146-2776(80)80097-8 · DOI
  15. Binkhorst, 1981, Advantages and disadvantages of intracamerular Na-hyaluronate (Healon) in intraocular lens surgery, Doc. Ophthalmol., 50, 233, 10.1007/BF00158003 · doi:10.1007/bf00158003
  16. Binkhorst, 1980, Inflammation and intraocular pressure after the use of Healon in intraocular lens surgery, J. Am. Intraocul. Implant Soc., 6, 340, 10.1016/S0146-2776(80)80031-0 · doi:10.1016/s0146-2776(80)80031-0
  17. Percival, 1985, Results of a clinical trial of sodium hyaluronate in lens implantation surgery, J. Am. Intraocul. Implant Soc., 11, 257, 10.1016/S0146-2776(85)80036-7 · doi:10.1016/s0146-2776(85)80036-7
  18. Graue, 1980, The protective effect of Na-hyaluronate to corneal endothelium, Exp. Eye Res., 31, 119, 10.1016/0014-4835(80)90094-9 · doi:10.1016/0014-4835(80)90094-9
  19. Percival, 1981, Protective role of Healon during lens implantation, Trans. Ophthalmol. Soc. UK, 101, 77
  20. Regnault, 1974, Treatment of severe cases of retinal detachment with highly viscous hyaluronic acid, Mod. Probl. Ophthalmol., 12, 378
  21. Kanski, 1975, Intravitreal hyaluronic acid injection. A long-term clinical evaluation, Br. J. Ophthalmol., 59, 255, 10.1136/bjo.59.5.255 · doi:10.1136/bjo.59.5.255
  22. Auer, 1980, Effect of hyaluronic acid in naturally occurring and experimentally induced osteoarthritis, Am. J. Vet. Res., 41, 568, 10.2460/ajvr.1980.41.04.568 · doi:10.2460/ajvr.1980.41.04.568
  23. Namiki, 1982, Therapeutic effect of intra-articular injection of high molecular weight hyaluronic acid on osteoarthritis of the knee, Int. J. Clin. Pharmacol. Ther. Toxicol., 20, 501
  24. Leardini, 1988, Intra-articular injections of hyaluronic acid in the treatment of painful shoulder, Clin. Ther., 10, 521
  25. Dougados, 1993, High molecular weight sodium hyaluronate (hyalectin) in osteoarthritis of the knee: A 1year placebo-controlled trial, Osteoarthr. Cartil., 1, 97, 10.1016/S1063-4584(05)80024-X · DOI · Paper page
  26. Jones, 1995, Intra-articular hyaluronic acid compared to intra-articular triamcinolone hexacetonide in inflammatory knee osteoarthritis, Osteoarthr. Cartil., 3, 269, 10.1016/S1063-4584(05)80018-4 · DOI
  27. Juhlin, 1997, Hyaluronan in skin, J. Intern. Med., 242, 61, 10.1046/j.1365-2796.1997.00175.x · DOI
  28. Pavicic, 2011, Efficacy of cream-based novel formulations of hyaluronic acid of different molecular weights in anti-wrinkle treatment, J. Drugs Dermatol., 10, 990
  29. Abatangelo, 1983, Healing of hyaluronic acid-enriched wounds: Histological observations, J. Surg. Res., 35, 410, 10.1016/0022-4804(83)90030-6 · DOI
  30. Doillon, 1986, Collagen-based wound dressing: Effects of hyaluronic acid and fibronectin on wound healing, Biomaterials, 7, 3, 10.1016/0142-9612(86)90080-3 · DOI · Paper page
  31. Laurent, 1987, Hyaluronan and healing of tympanic membrane perforations. An experimental study, Acta Otolaryngol. Suppl., 442, 54
  32. King, 1991, Beneficial actions of exogenous hyaluronic acid on wound healing, Surgery, 109, 76
  33. Duranti, 1998, Injectable hyaluronic acid gel for soft tissue augmentation. A clinical and histological study, Dermatol. Surg., 24, 1317, 10.1111/j.1524-4725.1998.tb00007.x · DOI · Paper page
  34. Lin, 1994, Hyaluronic acid-filled mammary implants: An experimental study, Plast. Reconstr. Surg., 94, 306, 10.1097/00006534-199408000-00014 · doi:10.1097/00006534-199408000-00014
  35. Benedetti, 1990, Microspheres of hyaluronic acid esters—Fabrication methods and in vitro hydrocortisone release, J. Control. Release, 13, 33, 10.1016/0168-3659(90)90072-2 · doi:10.1016/0168-3659(90)90072-2
  36. Lim, 2000, Preparation and evaluation of the in vitro drug release properties and mucoadhesion of novel microspheres of hyaluronic acid and chitosan, J. Control. Release, 66, 281, 10.1016/S0168-3659(99)00285-0 · DOI · Paper page
  37. Moreira, 1991, Sodium hyaluronate as a carrier for intravitreal gentamicin. An experimental study, Acta Ophthalmol., 69, 45, 10.1111/j.1755-3768.1991.tb01989.x · DOI
  38. Morimoto, 1991, Effects of viscous hyaluronate-sodium solutions on the nasal absorption of vasopressin and an analogue, Pharm. Res., 8, 471, 10.1023/A:1015894910416 · DOI
  39. Yerushalmi, 1994, Molecular and cellular studies of hyaluronic acid-modified liposomes as bioadhesive carriers for topical drug delivery in wound healing, Arch. Biochem. Biophys., 313, 267, 10.1006/abbi.1994.1387 · DOI
  40. Camber, 1989, Sodium hyaluronate as an ophthalmic vehicle: Some factors governing its effect on the ocular absorption of pilocarpine, Curr. Eye Res., 8, 563, 10.3109/02713688908995755 · doi:10.3109/02713688908995755
  41. Egbu, 2018, Antibody loaded collapsible hyaluronic acid hydrogels for intraocular delivery, Eur. J. Pharm. Biopharm., 124, 95, 10.1016/j.ejpb.2017.12.019 · DOI
  42. Geiger, 2017, Mixtures of hyaluronic acid and liposomes for drug delivery: Phase behavior, microstructure and mobility of liposomes, Int. J. Pharm., 523, 246, 10.1016/j.ijpharm.2017.03.029 · doi:10.1016/j.ijpharm.2017.03.029
  43. Mamelle, 2016, Hyaluronic acid liposomal gel sustains delivery of a corticoid to the inner ear, J. Control. Release, 226, 248, 10.1016/j.jconrel.2016.02.013 · DOI
  44. Xie, 2011, Hyaluronic acid: Evaluation as a potential delivery vehicle for vitronectin: Growth factor complexes in wound healing applications, J. Control. Release, 153, 225, 10.1016/j.jconrel.2011.03.021 · DOI
  45. Pravda, 2016, Hyaluronic Acid and Its Derivatives in Coating and Delivery Systems: Applications in Tissue Engineering, Regenerative Medicine and Immunomodulation, Adv. Healthc. Mater., 5, 2841, 10.1002/adhm.201600316 · DOI · Paper page
  46. Adamia, 2013, Aberrant splicing, hyaluronan synthases and intracellular hyaluronan as drivers of oncogenesis and potential drug targets, Curr. Cancer Drug Targets, 13, 347, 10.2174/1568009611313040001 · DOI
  47. Adamia, 2005, Hyaluronan and hyaluronan synthases: Potential therapeutic targets in cancer, Curr. Drug Targets Cardiovasc. Haematol. Disord., 5, 3, 10.2174/1568006053005056 · DOI · Paper page
  48. Carvalho, 2016, Genetic basis for hyper production of hyaluronic acid in natural and engineered microorganisms, Microb. Cell Fact., 15, 119, 10.1186/s12934-016-0517-4 · DOI
  49. Heldin, P., Lin, C.Y., Kolliopoulos, K., Chen, Y.H., and Skandalis, S.S. (2018). Regulation of hyaluronan biosynthesis and clinical impact of excessive hyaluronan production. Matrix Biol. · DOI
  50. Cyphert, 2015, Size matters: Molecular weight specificity of hyaluronan effects in cell biology, Int. J. Cell Biol., 2015, 563818, 10.1155/2015/563818 · DOI · Paper page
  51. Ebid, 2014, Hyaluronan is not a ligand but a regulator of toll-like receptor signaling in mesangial cells: Role of extracellular matrix in innate immunity, ISRN Nephrol., 2014, 714081, 10.1155/2014/714081 · DOI
  52. Gao, 2008, Hyaluronan oligosaccharides are potential stimulators to angiogenesis via RHAMM mediated signal pathway in wound healing, Clin. Investig. Med., 31, E106, 10.25011/cim.v31i3.3467 · DOI
  53. Mattheolabakis, 2015, Hyaluronic acid targeting of CD44 for cancer therapy: From receptor biology to nanomedicine, J. Drug Target., 23, 605, 10.3109/1061186X.2015.1052072 · DOI · Paper page
  54. Supp, 2014, Inhibition of hyaluronan synthase 2 reduces the abnormal migration rate of keloid keratinocytes, J. Burn Care Res., 35, 84, 10.1097/BCR.0b013e3182a2a9dd · DOI
  55. Fallacara, A., Vertuani, S., Panozzo, G., Pecorelli, A., Valacchi, G., and Manfredini, S. (2017). Novel Artificial Tears Containing Cross-Linked Hyaluronic Acid: An In Vitro Re-Epithelialization Study. Molecules, 22. · doi:10.3390/molecules22122104
  56. Henry, 2018, Synthesis and characterization of hyaluronic acid hydrogels crosslinked using a solvent-free process for potential biomedical applications, Carbohydr. Polym., 181, 1194, 10.1016/j.carbpol.2017.12.015 · DOI · Paper page
  57. Fallacara, 2017, Hyaluronic acid fillers in soft tissue regeneration, Facial Plast. Surg., 33, 87, 10.1055/s-0036-1597685 · doi:10.1055/s-0036-1597685
  58. Fraser, 1997, Hyaluronan: Its nature, distribution, functions and turnover, J. Intern. Med., 242, 27, 10.1046/j.1365-2796.1997.00170.x · DOI · Paper page
  59. Girish, 2007, The magic glue hyaluronan and its eraser hyaluronidase: A biological overview, Life Sci., 80, 1921, 10.1016/j.lfs.2007.02.037 · DOI · Paper page
  60. Laurent, 1992, Hyaluronan, FASEB J., 6, 2397, 10.1096/fasebj.6.7.1563592 · DOI · Paper page
  61. Scott, 1989, Secondary structures in hyaluronan solutions: Chemical and biological implications, Ciba Found. Symp., 143, 6
  62. Scott, 1991, Secondary and tertiary structures of hyaluronan in aqueous solution, investigated by rotary shadowing-electron microscopy and computer simulation. Hyaluronan is a very efficient network-forming polymer, Biochem. J., 274, 699, 10.1042/bj2740699 · DOI · Paper page
  63. Scott, 1999, Hyaluronan forms specific stable tertiary structures in aqueous solution: A 13C NMR study, Proc. Natl. Acad. Sci. USA, 96, 4850, 10.1073/pnas.96.9.4850 · DOI · Paper page
  64. Laurent, 1989, The biology of hyaluronan. Introduction, Ciba Found. Symp., 143, 1
  65. Balazs, 1986, Nomenclature of hyaluronic acid, Biochem. J., 235, 903, 10.1042/bj2350903 · DOI · Paper page
  66. Heatley, 1988, A water molecule participates in the secondary structure of hyaluronan, Biochem. J., 254, 489, 10.1042/bj2540489 · DOI
  67. Scott, 1992, Supramolecular organization of extracellular matrix glycosaminoglycans, in vitro and in the tissues, FASEB J., 6, 2639, 10.1096/fasebj.6.9.1612287 · DOI · Paper page
  68. Kobayashi, 1994, Viscoelasticity of hyaluronic acid with different molecular weights, Biorheology, 31, 235, 10.3233/BIR-1994-31302 · DOI · Paper page
  69. Cleland, 1968, Ionic polysaccharides. II. Comparison of polyelectrolyte behavior of hyaluronate with that of carboxymethyl cellulose, Biopolymers, 6, 1519, 10.1002/bip.1968.360061102 · doi:10.1002/bip.1968.360061102
  70. Helfet, A.J. (1974). The physical properties of synovial fluid and the special role of hyaluronic acid. Disorders of the Knee, J.B. Lippincott Company.
  71. Rwei, 2008, Viscoelasticity and wearability of hyaluronate solutions, Biochem. Eng. J., 40, 211, 10.1016/j.bej.2007.12.021 · doi:10.1016/j.bej.2007.12.021
  72. Demeester, 1998, Hyaluronan: Preparation, Structure, Properties, and Applications, Chem. Rev., 98, 2663, 10.1021/cr941199z · DOI · Paper page
  73. Maleki, 2008, Effect of pH on the behavior of hyaluronic acid in dilute and semidilute aqueous solutions, Macromol. Symp., 274, 131, 10.1002/masy.200851418 · doi:10.1002/masy.200851418
  74. Ghosh, 1993, Conformational contraction and hydrolysis of hyaluronate in sodium hydroxide solutions, Macromolecules, 26, 4685, 10.1021/ma00069a042 · doi:10.1021/ma00069a042
  75. Morris, 1980, Conformation and dynamic interactions in hyaluronate solutions, J. Mol. Biol., 138, 383, 10.1016/0022-2836(80)90294-6 · DOI · Paper page
  76. 1995, Non-Newtonian properties of hyaluronic acid aqueous solution. Colloids Surf. A Physicochem, Eng. Asp., 97, 197, 10.1016/0927-7757(95)03097-W · doi:10.1016/0927-7757(95)03097-w
  77. Gura, 1998, Specific degradation of hyaluronic acid and its rheological properties, Polym. Degrad. Stab., 59, 297, 10.1016/S0141-3910(97)00194-8 · doi:10.1016/s0141-3910(97)00194-8
  78. DeAngelis, 1998, Identification and molecular cloning of a unique hyaluronan synthase from Pasteurella multocida, J. Biol. Chem., 273, 8454, 10.1074/jbc.273.14.8454 · DOI
  79. Volpi, 2003, Purification and characterization of hyaluronic acid from the mollusc bivalve Mytilus galloprovincialis, Biochimie, 85, 619, 10.1016/S0300-9084(03)00083-X · DOI
  80. Kogan, 2007, Hyaluronic acid: A natural biopolymer with a broad range of biomedical and industrial applications, Biotechnol. Lett., 29, 17, 10.1007/s10529-006-9219-z · DOI · Paper page
  81. Volpi, 2009, Role, metabolism, chemical modifications and applications of hyaluronan, Curr. Med. Chem., 16, 1718, 10.2174/092986709788186138 · DOI · Paper page
  82. Sobolewski, 1997, Collagen and glycosaminoglycans of Wharton’s jelly, Biol. Neonate, 71, 11, 10.1159/000244392 · DOI
  83. Robert, 2010, Biological effects of hyaluronan in connective tissues, eye, skin, venous wall. Role in aging, Pathol. Biol., 58, 187, 10.1016/j.patbio.2009.09.010 · doi:10.1016/j.patbio.2009.09.010
  84. Weigel, 1997, Hyaluronan synthases, J. Biol. Chem., 272, 13997, 10.1074/jbc.272.22.13997 · DOI · Paper page
  85. Itano, 2002, Mammalian hyaluronan synthases, IUBMB Life, 54, 195, 10.1080/15216540214929 · DOI · Paper page
  86. Spicer, 1998, Characterization and molecular evolution of a vertebrate hyaluronan synthase gene family, J. Biol. Chem., 273, 1923, 10.1074/jbc.273.4.1923 · DOI · Paper page
  87. Vigetti, 2014, Metabolic control of hyaluronan synthases, Matrix Biol., 35, 8, 10.1016/j.matbio.2013.10.002 · DOI · Paper page
  88. Stuhlmeier, 2004, Differential effect of transforming growth factor beta (TGF-beta) on the genes encoding hyaluronan synthases and utilization of the p38 MAPK pathway in TGF-beta-induced hyaluronan synthase 1 activation, J. Biol. Chem., 279, 8753, 10.1074/jbc.M303945200 · DOI
  89. Vigetti, 2014, Hyaluronan: Biosynthesis and signaling, Biochim. Biophys. Acta, 1840, 2452, 10.1016/j.bbagen.2014.02.001 · DOI · Paper page
  90. Zhang, 2016, Hyaluronan synthase 2 expressed by cancer-associated fibroblasts promotes oral cancer invasion, J. Exp. Clin. Cancer Res., 35, 181, 10.1186/s13046-016-0458-0 · doi:10.1186/s13046-016-0458-0
  91. Zhang, 2016, Hyaluronan synthase 2 is an adverse prognostic marker in androgen receptor-negative breast cancer, J. Clin. Pathol., 69, 1055, 10.1136/jclinpath-2016-203617 · DOI
  92. Stern, 2006, Hyaluronidases: Their genomics, structures, and mechanisms of action, Chem. Rev., 106, 818, 10.1021/cr050247k · DOI · Paper page
  93. Csoka, 2001, The six hyaluronidase-like genes in the human and mouse genomes, Matrix Biol., 20, 499, 10.1016/S0945-053X(01)00172-X · DOI · Paper page
  94. Lokeshwar, 2001, Stromal and epithelial expression of tumor markers hyaluronic acid and HYAL1 hyaluronidase in prostate cancer, J. Biol. Chem., 276, 11922, 10.1074/jbc.M008432200 · DOI · Paper page
  95. Lepperdinger, 1998, HYAL2, a human gene expressed in many cells, encodes a lysosomal hyaluronidase with a novel type of specificity, J. Biol. Chem., 273, 22466, 10.1074/jbc.273.35.22466 · DOI · Paper page
  96. Frost, 1997, Purification, cloning, and expression of human plasma hyaluronidase, Biochem. Biophys. Res. Commun., 236, 10, 10.1006/bbrc.1997.6773 · DOI · Paper page
  97. Csoka, 1997, Purification and microsequencing of hyaluronidase isozymes from human urine, FEBS Lett., 417, 307, 10.1016/S0014-5793(97)01309-4 · DOI
  98. Cherr, 2001, The dual functions of GPI-anchored PH-20: Hyaluronidase and intracellular signaling, Matrix Biol., 20, 515, 10.1016/S0945-053X(01)00171-8 · DOI · Paper page
  99. Mendichi, 2006, Degradative action of reactive oxygen species on hyaluronan, Biomacromolecules, 7, 659, 10.1021/bm050867v · DOI · Paper page
  100. Stern, 2007, The many ways to cleave hyaluronan, Biotechnol. Adv., 25, 537, 10.1016/j.biotechadv.2007.07.001 · DOI · Paper page
  101. Monzon, 2010, Reactive oxygen species and hyaluronidase 2 regulate airway epithelial hyaluronan fragmentation, J. Biol. Chem., 285, 26126, 10.1074/jbc.M110.135194 · DOI
  102. Schiller, 2003, Contribution of reactive oxygen species to cartilage degradation in rheumatic diseases: Molecular pathways, diagnosis and potential therapeutic strategies, Curr. Med. Chem., 10, 2123, 10.2174/0929867033456828 · DOI
  103. Schiller, 1995, Action of hypochlorous acid on polymeric components of cartilage. Use of 13C NMR spectroscopy, Z. Naturforsch. C, 50, 721, 10.1515/znc-1995-9-1020 · doi:10.1515/znc-1995-9-1020
  104. Tamer, 2013, Hyaluronan and synovial joint: Function, distribution and healing, Interdiscip. Toxicol., 6, 111, 10.2478/intox-2013-0019 · DOI · Paper page
  105. Wu, 2015, A novel role of low molecular weight hyaluronan in breast cancer metastasis, FASEB J., 29, 1290, 10.1096/fj.14-259978 · DOI · Paper page
  106. Kim, M.Y., Muto, J., and Gallo, R.L. (2013). Hyaluronic acid oligosaccharides suppress TLR3-dependent cytokine expression in a TLR4-dependent manner. PLoS ONE, 8. · DOI
  107. Misra, 2006, Hyaluronan constitutively regulates activation of multiple receptor tyrosine kinases in epithelial and carcinoma cells, J. Biol. Chem., 281, 34936, 10.1074/jbc.C600138200 · DOI · Paper page
  108. Toole, 2008, Hyaluronan oligosaccharides as a potential anticancer therapeutic, Curr. Pharm. Biotechnol., 9, 249, 10.2174/138920108785161569 · DOI
  109. Campo, 2013, 4-mer hyaluronan oligosaccharides stimulate in ammation response in synovial broblasts in part via TAK-1 and in part via p38-MAPK, Curr. Med. Chem., 20, 1162, 10.2174/0929867311320090005 · DOI
  110. Yang, 2012, The high and low molecular weight forms of hyaluronan have distinct effects on CD44 clustering, J. Biol. Chem., 287, 43094, 10.1074/jbc.M112.349209 · DOI · Paper page
  111. Turley, 2002, Signaling properties of hyaluronan receptors, J. Biol. Chem., 277, 4589, 10.1074/jbc.R100038200 · DOI · Paper page
  112. Research, G.V. (2018, March 08). Hyaluronic Acid Market Size Worth USD 15.4 Billion by 2025|CAGR: 8.8%. Available online: https://www.grandviewresearch.com/press-release/global-hyaluronic-acid-market.
  113. Shiedlin, 2004, Evaluation of hyaluronan from different sources: Streptococcus zooepidemicus, rooster comb, bovine vitreous, and human umbilical cord, Biomacromolecules, 5, 2122, 10.1021/bm0498427 · DOI
  114. Rangaswamy, 2008, An efficient process for production and purification of hyaluronic acid from Streptococcus equi subsp. zooepidemicus, Biotechnol. Lett., 30, 493, 10.1007/s10529-007-9562-8 · DOI
  115. Kim, 1996, Selection of a Streptococcus equi mutant and optimization of culture conditions for the production of high molecular weight hyaluronic acid, Enzyme Microb. Technol., 19, 440, 10.1016/S0141-0229(96)00019-1 · DOI
  116. Liu, L., Liu, Y., Li, J., Du, G., and Chen, J. (2011). Microbial production of hyaluronic acid: Current state, challenges, and perspectives. Microb. Cell Fact., 10. · DOI · Paper page
  117. Kaur, 2016, Hyaluronan production and molecular weight is enhanced in pathway-engineered strains of lactate dehydrogenase-deficient Lactococcus lactis, Metab. Eng. Commun., 3, 15, 10.1016/j.meteno.2016.01.003 · DOI
  118. Chien, 2007, Enhanced hyaluronic acid production in Bacillus subtilis by coexpressing bacterial hemoglobin, Biotechnol. Prog., 23, 1017
  119. Yu, 2008, Metabolic engineering of Escherichia coli for biosynthesis of hyaluronic acid, Metab. Eng., 10, 24, 10.1016/j.ymben.2007.09.001 · DOI · Paper page
  120. Cheng, 2016, High-titer biosynthesis of hyaluronic acid by recombinant Corynebacterium glutamicum, Biotechnol. J., 11, 574, 10.1002/biot.201500404 · DOI
  121. DeAngelis, 1996, Yeast-derived recombinant DG42 protein of Xenopus can synthesize hyaluronan in vitro, J. Biol. Chem., 271, 23657, 10.1074/jbc.271.39.23657 · DOI
  122. Jeong, 2014, Metabolic engineering of Pichia pastoris for production of hyaluronic acid with high molecular weight, J. Biotechnol., 185, 28, 10.1016/j.jbiotec.2014.05.018 · DOI
  123. Rakkhumkaew, 2013, Hyaluronan synthesis in cultured tobacco cells (BY-2) expressing a chlorovirus enzyme: Cytological studies, Biotechnol. Bioeng., 110, 1174, 10.1002/bit.24783 · doi:10.1002/bit.24783
  124. DeAngelis, 2008, Monodisperse hyaluronan polymers: Synthesis and potential applications, Curr. Pharm. Biotechnol., 9, 246, 10.2174/138920108785161550 · doi:10.2174/138920108785161550
  125. Zuber, 2011, Chemical modifications of hyaluronic acid for the synthesis of derivatives for a broad range of biomedical applications, Carbohydr. Polym., 85, 469, 10.1016/j.carbpol.2011.03.019 · DOI · Paper page
  126. Shimojo, 2015, The crosslinking degree controls the mechanical, rheological, and swelling properties of hyaluronic acid microparticles, J. Biomed. Mater. Res. A, 103, 730, 10.1002/jbm.a.35225 · doi:10.1002/jbm.a.35225
  127. Collins, 2008, Physical properties of crosslinked hyaluronic acid hydrogels, J. Mater. Sci. Mater. Med., 19, 3335, 10.1007/s10856-008-3476-4 · DOI · Paper page
  128. Bowman, 2018, Recent advances in hyaluronic acid based therapy for osteoarthritis, Clin. Transl. Med., 7, 6, 10.1186/s40169-017-0180-3 · DOI · Paper page
  129. Nobile, 2014, Anti-aging and filling efficacy of six types hyaluronic acid based dermo-cosmetic treatment: Double blind, randomized clinical trial of efficacy and safety, J. Cosmet. Dermatol., 13, 277, 10.1111/jocd.12120 · DOI
  130. Kaur, 2006, Repair of tympanic membrane perforation by topical application of 1% sodium hyaluronate, Indian J. Otolaryngol. Head Neck Surg., 58, 241, 10.1007/BF03050829 · doi:10.1007/bf03050829
  131. Gelardi, 2013, Intranasal sodium hyaluronate on the nasal cytology of patients with allergic and nonallergic rhinitis, Int. Forum Allergy Rhinol., 3, 807, 10.1002/alr.21193 · DOI
  132. Gelardi, 2013, Effect of sodium hyaluronate on mucociliary clearance after functional endoscopic sinus surgery, Eur. Ann. Allergy Clin. Immunol., 45, 103
  133. Maleki, 2007, Characterization of the chemical degradation of hyaluronic acid during chemical gelation in the presence of different cross-linker agents, Carbohydr. Res., 342, 2776, 10.1016/j.carres.2007.08.021 · doi:10.1016/j.carres.2007.08.021
  134. Bulpitt, 1999, New strategy for chemical modification of hyaluronic acid: Preparation of functionalized derivatives and their use in the formation of novel biocompatible hydrogels, J. Biomed. Mater. Res., 47, 152, 10.1002/(SICI)1097-4636(199911)47:2<152::AID-JBM5>3.0.CO;2-I · DOI · Paper page
  135. Lim, 2018, One-pot synthesis of dopamine-conjugated hyaluronic acid/polydopamine nanocomplexes to control protein drug release, Int. J. Pharm., 542, 288, 10.1016/j.ijpharm.2018.03.007 · DOI
  136. Magnani, 2000, Novel polysaccharide hydrogels: Characterization and properties, Polym. Adv. Technol., 11, 488, 10.1002/1099-1581(200008/12)11:8/12<488::AID-PAT995>3.0.CO;2-5 · DOI
  137. Sigen, 2018, A facile one-pot synthesis of acrylated hyaluronic acid, Chem. Commun., 54, 1081, 10.1039/C7CC08648B · doi:10.1039/c7cc08648b
  138. Felgueiras, 2017, Octadecyl chains immobilized onto hyaluronic acid coatings by thiol-ene “click chemistry” increase the surface antimicrobial properties and prevent platelet adhesion and activation to polyurethane, ACS Appl. Mater. Interfaces, 9, 7979, 10.1021/acsami.6b16415 · DOI
  139. Smith, 2018, Diels-Alder Click-Cross-Linked Hydrogels with Increased Reactivity Enable 3D Cell Encapsulation, Biomacromolecules, 19, 926, 10.1021/acs.biomac.7b01715 · DOI · Paper page
  140. Fu, 2017, Injectable hyaluronic acid/poly(ethylene glycol) hydrogels crosslinked via strain-promoted azide-alkyne cycloaddition click reaction, Carbohydr. Polym., 169, 332, 10.1016/j.carbpol.2017.04.028 · DOI
  141. Shu, 2002, Disulfide cross-linked hyaluronan hydrogels, Biomacromolecules, 3, 1304, 10.1021/bm025603c · DOI · Paper page
  142. Bencherif, 2008, Influence of the degree of methacrylation on hyaluronic acid hydrogels properties, Biomaterials, 29, 1739, 10.1016/j.biomaterials.2007.11.047 · DOI · Paper page
  143. Donnelly, 2017, Photocrosslinked tyramine-substituted hyaluronate hydrogels with tunable mechanical properties improve immediate tissue-hydrogel interfacial strength in articular cartilage, J. Biomater. Sci. Polym. Ed., 28, 582, 10.1080/09205063.2017.1289035 · DOI
  144. Yui, 1992, Inflammation responsive degradation of crosslinked hyaluronic acid gels, J. Control. Release, 22, 105, 10.1016/0168-3659(92)90195-W · DOI
  145. Collins, 2007, Comparison of the effectiveness of four different crosslinking agents with hyaluronic acid hydrogel films for tissue-culture applications, J. Appl. Polym. Sci., 104, 3183, 10.1002/app.25993 · DOI
  146. Serban, 2008, Synthesis, characterization and chondroprotective properties of a hyaluronan thioethyl ether derivative, Biomaterials, 29, 1388, 10.1016/j.biomaterials.2007.12.006 · DOI
  147. Crescenzi, 2003, Synthesis and partial characterization of hydrogels obtained via glutaraldehyde crosslinking of acetylated chitosan and of hyaluronan derivatives, Biomacromolecules, 4, 1045, 10.1021/bm0340669 · DOI
  148. Tomihata, 1997, Crosslinking of hyaluronic acid with glutaraldehyde, J. Polym. Sci. Part A Polym. Chem., 35, 3553, 10.1002/(SICI)1099-0518(19971130)35:16<3553::AID-POLA22>3.0.CO;2-D · doi:10.1002/(sici)1099-0518(19971130)35:16<3553::aid-pola22>3.0.co;2-d
  149. Seidlits, 2010, The effects of hyaluronic acid hydrogels with tunable mechanical properties on neural progenitor cell differentiation, Biomaterials, 31, 3930, 10.1016/j.biomaterials.2010.01.125 · DOI · Paper page
  150. Pravata, 2008, New amphiphilic lactic acid oligomer–hyaluronan conjugates: Synthesis and physicochemical characterization, Biomacromolecules, 9, 340, 10.1021/bm700843m · doi:10.1021/bm700843m
  151. Steiner, 2006, Synthesis and characterization of new biodegradable hyaluronan alkyl derivatives, Biopolymers, 82, 74, 10.1002/bip.20461 · doi:10.1002/bip.20461
  152. Marchal, 2006, New physically and chemically crosslinked hyaluronate (HA)-based hydrogels for cartilage repair, J. Biomed. Mater. Res. A, 76, 416
  153. Hirano, 2005, Preparation of the methyl ester of hyaluronan and its enzymatic degradation, Carbohydr. Res., 340, 2297, 10.1016/j.carres.2005.07.016 · doi:10.1016/j.carres.2005.07.016
  154. Prata, 2010, Complex fluids based on methacrylated hyaluronic acid, Biomacromolecules, 11, 769, 10.1021/bm901373x · DOI
  155. Benedetti, 1993, Biocompatibility and biodegradation of different hyaluronan derivatives (Hyaff) implanted in rats, Biomaterials, 14, 1154, 10.1016/0142-9612(93)90160-4 · DOI · Paper page
  156. Kaczmarek, 2018, New composite materials prepared by calcium phosphate precipitation in chitosan/collagen/hyaluronic acid sponge cross-linked by EDC/NHS, Int. J. Biol. Macromol., 107, 247, 10.1016/j.ijbiomac.2017.08.173 · DOI
  157. Kirk, 2013, Mechanical and biocompatible characterization of a cross-linked collagen-hyaluronic acid wound dressing, Biomatter, 3, pii:E25633, 10.4161/biom.25633 · DOI
  158. Bergman, 2007, Hyaluronic acid derivatives prepared in aqueous media by triazine-activated amidation, Biomacromolecules, 8, 2190, 10.1021/bm0701604 · doi:10.1021/bm0701604
  159. Eglin, 2014, A systematic analysis of DMTMM vs EDC/NHS for ligation of amines to hyaluronan in water, Carbohydr. Polym., 108, 239, 10.1016/j.carbpol.2014.02.070 · DOI · Paper page
  160. Crescenzi, 2002, NMR structural study of hydrogels based on partially deacetylated hyaluronan, Macromol. Biosci., 2, 272, 10.1002/1616-5195(200208)2:6<272::AID-MABI272>3.0.CO;2-V · doi:10.1002/1616-5195(200208)2:6<272::aid-mabi272>3.0.co;2-v
  161. Bhattacharya, 2017, Impact of structurally modifying hyaluronic acid on CD44 interaction, J. Mater. Chem. B., 5, 8183, 10.1039/C7TB01895A · DOI · Paper page
  162. Kong, 2010, Long acting hyaluronate—Exendin 4 conjugate for the treatment of type 2 diabetes, Biomaterials, 31, 4121, 10.1016/j.biomaterials.2010.01.091 · DOI
  163. Mero, 2014, Hyaluronic acid bioconjugates for the delivery of bioactive molecules, Polymers, 6, 346, 10.3390/polym6020346 · DOI · Paper page
  164. Mangano, 2017, Evaluation of hyaluronic acid-P40 conjugated cream in a mouse model of dermatitis induced by oxazolone, Exp. Ther. Med., 14, 2439, 10.3892/etm.2017.4810 · doi:10.3892/etm.2017.4810
  165. Manju, 2011, Conjugation of curcumin onto hyaluronic acid enhances its aqueous solubility and stability, J. Colloid Interface Sci., 359, 318, 10.1016/j.jcis.2011.03.071 · DOI · Paper page
  166. Sharma, 2018, Wound healing activity of curcumin conjugated to hyaluronic acid: In vitro and in vivo evaluation, Artif. Cells Nanomed. Biotechnol., 46, 1009, 10.1080/21691401.2017.1358731 · DOI
  167. Chen, 2018, Conjugation of paclitaxel to C-6 hexanediamine-modified hyaluronic acid for targeted drug delivery to enhance antitumor efficacy, Carbohydr. Polym., 181, 150, 10.1016/j.carbpol.2017.09.017 · doi:10.1016/j.carbpol.2017.09.017
  168. Nguyen, 2017, Nanohybrid magnetic liposome functionalized with hyaluronic acid for enhanced cellular uptake and near-infrared-triggered drug release, Colloids Surf. B. Biointerfaces, 154, 104, 10.1016/j.colsurfb.2017.03.008 · DOI
  169. Hayward, 2016, Hyaluronic acid-conjugated liposome nanoparticles for targeted delivery to CD44 overexpressing glioblastoma cells, Oncotarget, 7, 34158, 10.18632/oncotarget.8926 · DOI
  170. Han, 2016, Hyaluronan-conjugated liposomes encapsulating gemcitabine for breast cancer stem cells, Int. J. Nanomed., 11, 1413, 10.2147/IJN.S95850 · DOI · Paper page
  171. Chi, 2017, Redox-sensitive and hyaluronic acid functionalized liposomes for cytoplasmic drug delivery to osteosarcoma in animal models, J. Control. Release, 261, 113, 10.1016/j.jconrel.2017.06.027 · DOI · Paper page
  172. Negi, 2015, Hyaluronan coated liposomes as the intravenous platform for delivery of imatinib mesylate in MDR colon cancer, Int. J. Biol. Macromol., 73, 222, 10.1016/j.ijbiomac.2014.11.026 · DOI
  173. Moustafa, 2017, Hyalugel-integrated liposomes as a novel ocular nanosized delivery system of fluconazole with promising prolonged effect, Int. J. Pharm., 534, 14, 10.1016/j.ijpharm.2017.10.007 · DOI
  174. Manconi, 2017, Chitosan and hyaluronan coated liposomes for pulmonary administration of curcumin, Int. J. Pharm., 525, 203, 10.1016/j.ijpharm.2017.04.044 · DOI
  175. Hillaireau, 2016, Hyaluronic acid-conjugated lipoplexes for targeted delivery of siRNA in a murine metastatic lung cancer model, Int. J. Pharm., 514, 103, 10.1016/j.ijpharm.2016.06.125 · DOI
  176. Maudens, 2018, Self-assembled thermoresponsive nanostructures of hyaluronic acid conjugates for osteoarthritis therapy, Nanoscale, 10, 1845, 10.1039/C7NR07614B · DOI
  177. Kim, 2013, Bioimaging and pulmonary applications of self-assembled Flt1 peptide-hyaluronic acid conjugate nanoparticles, Biomaterials, 34, 8478, 10.1016/j.biomaterials.2013.07.062 · DOI
  178. Pandey, M., Choudhury, H., Gunasegaran, T.A.P., Nathan, S.S., Md, S., Gorain, B., Tripathy, M., and Hussain, Z. (2018). Hyaluronic acid-modified betamethasone encapsulated polymeric nanoparticles: Fabrication, characterisation, in vitro release kinetics, and dermal targeting. Drug Deliv. Transl. Res. · DOI
  179. Pereira, 2016, Hyaluronate nanoparticles included in polymer films for the prolonged release of vitamin E for the management of skin wounds, Eur. J. Pharm. Sci., 83, 203, 10.1016/j.ejps.2016.01.002 · DOI
  180. Wang, 2017, Hyaluronic acid-coated chitosan nanoparticles induce ROS-mediated tumor cell apoptosis and enhance antitumor efficiency by targeted drug delivery via CD44, J. Nanobiotechnol., 15, 7, 10.1186/s12951-016-0245-2 · DOI · Paper page
  181. Cho, 2011, Self-assembled nanoparticles based on hyaluronic acid-ceramide (HA-CE) and Pluronic® for tumor-targeted delivery of docetaxel, Biomaterials, 32, 7181, 10.1016/j.biomaterials.2011.06.028 · DOI · Paper page
  182. Parashar, P., Rathor, M., Dwivedi, M., and Saraf, S.A. (2018). Hyaluronic acid decorated naringenin nanoparticles: Appraisal of chemopreventive and curative potential for lung cancer. Pharmaceutics, 10. · DOI
  183. Hwang, 2008, Delivery of ofloxacin to the lung and alveolar macrophages via hyaluronan microspheres for the treatment of tuberculosis, J. Control. Release, 129, 100, 10.1016/j.jconrel.2008.04.009 · DOI
  184. Li, 2017, Inhaled hyaluronic acid microparticles extended pulmonary retention and suppressed systemic exposure of a short-acting bronchodilator, Carbohydr. Polym., 172, 197, 10.1016/j.carbpol.2017.05.020 · DOI
  185. Fatnassi, 2014, Optimization of spray-dried hyaluronic acid microspheres to formulate drug-loaded bone substitute materials, Powder Technol., 255, 44, 10.1016/j.powtec.2013.08.027 · doi:10.1016/j.powtec.2013.08.027
  186. Simsolo, 2018, Formulation and evaluation of organogels containing hyaluronan microparticles for topical delivery of caffeine, AAPS PharmSciTech, 19, 1367, 10.1208/s12249-018-0955-x · doi:10.1208/s12249-018-0955-x
  187. Esposito, 2005, Hyaluronan-based microspheres as tools for drug delivery: A comparative study, Int. J. Pharm., 288, 35, 10.1016/j.ijpharm.2004.09.001 · doi:10.1016/j.ijpharm.2004.09.001
  188. Koivusalo, 2018, Hydrazone crosslinked hyaluronan-based hydrogels for therapeutic delivery of adipose stem cells to treat corneal defects, Mater. Sci. Eng. C Mater. Biol. Appl., 85, 68, 10.1016/j.msec.2017.12.013 · DOI
  189. Luo, 2000, Cross-linked hyaluronic acid hydrogel films: New biomaterials for drug delivery, J. Control. Release, 69, 169, 10.1016/S0168-3659(00)00300-X · DOI · Paper page
  190. Kroin, 2016, Intraarticular slow-release triamcinolone acetate reduces allodynia in an experimental mouse knee osteoarthritis model, Gene, 591, 1, 10.1016/j.gene.2016.06.049 · DOI
  191. Pirard, 2005, Three percent diclofenac in 2.5% hyaluronan gel in the treatment of actinic keratoses: A meta-analysis of the recent studies, Arch. Dermatol. Res., 297, 185, 10.1007/s00403-005-0601-9 · doi:10.1007/s00403-005-0601-9
  192. Gao, 2015, Up-regulation of CD44 in the development of metastasis, recurrence and drug resistance of ovarian cancer, Oncotarget, 6, 9313, 10.18632/oncotarget.3220 · DOI
  193. Buffa, 2017, A new unsaturated derivative of hyaluronic acid—Synthesis, analysis and applications, Carbohydr. Polym., 163, 247, 10.1016/j.carbpol.2017.01.071 · DOI
  194. Aya, 2014, Hyaluronan in wound healing: Rediscovering a major player, Wound Repair Regen., 22, 579, 10.1111/wrr.12214 · DOI · Paper page
  195. Tagliagambe, 2017, Hyaluronic Acid Sodium Salt 0.2% Gel in the Treatment of a Recalcitrant Distal Leg Ulcer: A Case Report, J. Clin. Aesthet. Dermatol., 10, 49
  196. Neuman, 2015, Hyaluronic acid and wound healing, J. Pharm. Pharm. Sci., 18, 53, 10.18433/J3K89D · DOI
  197. 2005, Hyaluronic acid: A new trend to cure skin injuries an observational study, Rev. Enferm., 28, 53
  198. Shi, L., Zhao, Y., Xie, Q., Fan, C., Hilborn, J., Dai, J., and Ossipov, D.A. (2018). Moldable Hyaluronan Hydrogel Enabled by Dynamic Metal-Bisphosphonate Coordination Chemistry for Wound Healing. Adv. Healthc. Mater., 7. · DOI · Paper page
  199. Li, 2018, The preparation of hyaluronic acid grafted pullulan polymers and their use in the formation of novel biocompatible wound healing film, Carbohydr. Polym., 188, 92, 10.1016/j.carbpol.2018.01.102 · DOI
  200. Berce, 2018, Cutaneous wound healing using polymeric surgical dressings based on chitosan, sodium hyaluronate and resveratrol. A preclinical experimental study, Colloids Surf. B Biointerfaces, 163, 155, 10.1016/j.colsurfb.2017.12.041 · DOI

200 of 245 shown

Cited by

See all 860

Metadata

Authors
Fallacara, A., Baldini, E., Manfredini, S., & Vertuani, S.
Venue
Polymers
Publisher
MDPI AG
Published
2018-06-25
Volume
10
Issue
7
Pages
701
ISSN
2073-4360 (ISSN-L)
DOI
10.3390/polym10070701
OpenAlex
W2809231499
Cited by
860
References
8
FWCI
23.41
Type
journal article
Language
en
Open access
gold
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
  • IRALAB (2016-2018)
  • AMBROSIALAB srl (2017)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Hyaluronic Acid in the Third Millennium. https://app.cochat.ai/papers/10.3390/polym10070701
The paper
Fallacara, A., Baldini, E., Manfredini, S., & Vertuani, S. (2018). Hyaluronic Acid in the Third Millennium. Polymers. https://doi.org/10.3390/polym10070701

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.