Hyaluronan and synovial joint: function, distribution and healing

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ABSTRACT

Synovial fluid is a viscous solution found in the cavities of synovial joints. The principal role of synovial fluid is to reduce friction between the articular cartilages of synovial joints during movement. The presence of high molar mass hyaluronan (HA) in this fluid gives it the required viscosity for its function as lubricant solution. Inflammation oxidation stress enhances normal degradation of hyaluronan causing several diseases related to joints. This review describes hyaluronan properties and distribution, applications and its function in synovial joints, with short review for using thiol compounds as antioxidants preventing HA degradations under inflammation conditions.

Abeydeera LR. (2002). In vitro production of embryos in swine. Theriogenology57: 257-273.

Adams ME. (1993). Viseosupplementation: A treatment for osteoarthritis. JRheumatol 20: Suppl. 39: 1-24.

Altman RD. (2000). Intra-articular sodium hyaluronate in osteoarthritis of the knee. Semin Arthritis Rheum 30: 11-18.

Aruoma OI, Halliwell B, Hoey BM, Butler J. (1989). The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radic Biol Med 6: 593.

Ashhurst DE, Bland YS, Levick JR. (1991). An immunohistochemical study of the collagens of rabbit synovial interstitium. J Rheumatol 18: 1669-1672.

Athanasou NA, Quinn J. (1991). Immunocytochemical analysis of human synovial lining cells: phenotypic relation to other marrow derived cells. AnnRheum Dis 50: 311-315.

Balazs EA, Denlinger JL. (1989). Clinical uses of hyaluronan. Ciba Found Symp143: 265-280.

Balazs EA, Laurent TC, Jeanloz RW. (1986). Nomencla ture of hyaluronic acid. Biochemical Journal 235: 903.

Balazs EA. (2003). Analgesic eff ect of elastoviscous hyaluronan solutions and the treatment of arthritic pain. Cells Tissues Organs 174: 49-62.

Balazs EA, Denlinger JL. (1993). Viscosupplementation: a new concept in the treatment of osteoarthritis. J Rheumatol 20: 3-9.

Banasova M, Valachova K, Juranek I, Soltes L. (2012). Eff ect of thiol compounds on oxidative degradation of high molar hyaluronan in vitro. InterdiscipToxicol 5(Suppl. 1): 25-26.

Banasova M, Valachova K, Juranek I, Soltes L. (2013b). Aloevera and methylsulfonylmethane as dietary supplements: Their potential benefi ts for arthritic patients with diabetic complications. Journal of Information Intelligenceand Knowledge 5: 51-68.

Banasova M, Valachova K, Rychly J, Priesolova E, Nagy M, Juranek I, Soltes L. (2011). Scavenging and chain breaking activity of bucillamine on free-radical mediated degradation of high molar mass hyaluronan. ChemZi 7: 205-206.

Baňasova M, Valachova K, Hrabarova E, Priesolova E, Nagy M, Juranek I, Šoltes L. (2011). Early stage of the acute phase of joint infl ammation. In vitro testing of bucillamine and its oxidized metabolite SA981 in the function of antioxidants. 16th Interdisciplinary Czech-Slovak Toxicological Conference in Prague. Interdiscip Toxicol 4(2): 22.

Barrett J P, Siviero P. (2002). Retrospective study of outcomes in Hyalgan(R)- treated patients with osteoarthritis of the knee. Clin Drug Invest 22: 87-97.

Bergeret-Galley C, Latouche X, Illouz Y G.(2001). The value of a new fi ller material in corrective and cosmetic surgery: DermaLive and DermaDeep. AestheticPlast Surg 25: 249-255. 0 60 120 180 240 300 7 8 9 10 Dynamic viscosity [mPa·s] Time [min] 10050250 0 60 120 .

Betts WH, Cleland LG. (1982): Eff ect of metal chelators and antiinfl ammatory drugs on the degradation of hyaluronic acid. Arthritis Rheum 25: 1469-1476.

Blake DR, Hall ND, Treby DA. (1981). Protection against superoxide and hydrogen peroxide in synovial fl uid from rheumatoid patients. Clin Sci 61: 483-486.

Blewis ME, Nugent-Derfus GE, Schmidt TA, Schumacher BL, Sah RL. (2007). A model of synovial fl uid lubricant composition in normal and injured. Europeancells and materials 13: 26-39.

Bothner H, Wik O. (1987). Rheology of hyaluronate. Acta Otolaryngol Suppl442: 25-30.

Brandt K. (1970). Modifi cation of chemotaxis by synovial fl uid hyaluronate. Arthritis Rheum 13: 308-309.

Brown MB, Jones SA. (2005). Hyaluronic acid: a unique topical vehicle for the localized delivery of drugs to the skin. J Eur Acad Dermatol Venereol 19: 308-318.

Brown TJ, Laurent UBG, Fraser JRE. (1991). Turnover of hyaluronan in synovial joints: elimination of labelled hyaluronan from the knee joints of the rabbit. Exp Physiol 76: 125-34.

Bucolo C, Mangiafi co P. (1999). Pharmacological profi le of a new topical pilocarpine formulation. J Ocul Pharmacol Ther 15: 567-573.

Bucolo C, Spadaro A, Mangiafi co S. (1998). Pharmacological evaluation of a new timolol/pilocarpine formulation. Ophthalmic Res 30: 101-106.

Camber O, Edman P, Gurny R. (1987). Infl uence of sodium hyaluronate on the meiotic eff ect of pilocarpine in rabbits. Curr Eye Res 6: 779-784.

Camber O, Edman P. (1989). Sodium hyaluronate as an ophthalmic vehicle - some factors governing its eff ect on the ocular absorption of pilocarpine. Curr Eye Res 8: 563-567.

Cantor JO, Cerreta JM, Armand G, Turino GM. (1998). Aerosolized hyaluronic acid decreases alveolar injury induced by human neutrophil elastase. ProcSoc Exp Biol Med 217: 471-475.

Chabrecek P, Soltes L, Kallay Z, Fugedi A. (1990). Isolation and characterization of high molecular weight (3H) hyaluronic acid. J Label Compd Radiopharm28: 1121-1125.

Chabrecek P, Soltes L, Kallay Z, Novak I. (1990). Gel permeation chromatographic characterization of sodium hyaluronate and its reactions prepared by ultrasonic degradation. Chromatographia 30: 201-204.

Chen FH, Rousche KT, Tuan RS. (2006). Technology Insight: adult stem cells in cartilage regeneration and tissue engineering. Nat Clin Pract Rheumatol2(7): 373-82.

Coleman P, Kavanagh E, Mason RM, Levick JR, Ashhurst DE. (1998). The proteoglycans and glycosaminoglycan chains of rabbit synovium. HistochemJ 30: 519-524.

Comper WD, Laurent TC. (1978). Physiological function of connective tissue polysaccharidcs. Physiol Rev 58: 255-315.

Cowman MK, Matsuoka S. (2005). Experimental ap proaches to hyaluronan structure. Carbohydrate Re search 340: 791-809.

Dahl LB, Dahl IM, Engstrom-Laurent A, Granath K. (1985). Concentration and molecular weight of sodium hyaluronate in synovial fl uid from patients with rheumatoid arthritis and other arthropathies. Ann Rheum Dis 44: 817-822.

Dobbie JW, Hind C, Meijers P, Bodart C, Tasiaux N, Perret J, Anderson JD. (1995). Lamellar body secretion: ultrastructural analysis of an unexplored function of synoviocytes. Br J Rheumatol 34: 13-23.

Dougados M. (2000). Sodium hyaluronate therapy in osteoarthritis: arguments for a potential benefi cial structural eff ect. Semin Arthritis Rheum 30: 19-25.

Drafi F, Valachova K, Hrabarova E, Juranek I, Bauerova K, Šoltes L. (2010). Study of methotrexate and β-alanyl-L-histidine in comparison with L-glutathione on high-molar-mass hyaluronan degradation induced by ascorbate plus Cu (II) ions via rotational viscometry. 60th Pharmacological Days in Hradec Kralove. Acta Medica 53(3): 170.

Drobnik J. (1991). Hyaluronan in drug delivery. Adv Drug Dev Rev 7: 295-308.

Duranti F, Salti G, Bovani B, Calandra M, Rosati ML. (1998). Injectable hyaluronic acid gel for soft tissue augmentation - a clinical and histological study. Dermatol Surg 24: 1317-1325.

Edwards JCW, Wilkinson LS, Jones HM. (1994). The formation of human synovial cavities: a possible role for hyaluronan and CD44 in altered interzone cohesion. J Anat 185: 355-67.

Edwards JCW (1995). Consensus statement. Second international meeting on synovium. Cell biology, physiology and pathology. Ann Rheum Dis 54: 389-91.

Eliaz RE, Szoka FC. (2001). Liposome-encapsulated doxorubicin targeted to CD44: a strategy to kill CD44-overexpressing tumor cells. Cancer Res 61: 2592-2601.

Figueiredo F, Jones GM, Thouas GA, Trounson AO. (2002). The eff ect of extracellular matrix molecules on mouse preimplantation embryo development in vitro. Reprod Fertil Dev 14: 443-451.

Fisher AE, Naughton ODP. (2005). Therapeutic chelators for the twenty fi rst century: new treatments for iron and copper mediated infl ammatory and neurological disorders. Curr Drug Delivery 2: 261-268.

Fraser JRE, Foo WK, Maritz JS. (1972). Viscous interactions of hyaluronic acid with some proteins and neutral saccharides. Ann Rheum Dis 31: 513-20.

Fraser JRE, Kimpton WG, Pierscionek BK, Cahill RNP. (1993). The kinetics of hyaluronan in normal and acutely infl amed synovial joints - observations with experimental arthritis in sheep. Semin Arthritis Rheum 22: 9-17.

Furnus CC, de Matos DG, Martinez AG. (1998). Eff ect of hyaluronic acid on development of in vitro produced bovine embryos. Theriogenology 49: 1489-99.

Gandolfi SA, Massari A, Orsoni JG. (1992). Low-molecular-weight sodium hyaluronate in the treatment of bacterial corneal ulcers. Graefes Arch Clin ExpOphthalmol 230: 20-23.

Gardner DK, Lane M, Stevens J, Schoolcraft WB. (2003). Changing the start temperature and cooling rate in a slow-freezing protocol increases human blastocyst viability. Fertil Steril 79: 407-410.

Gardner DK, Rodriegez-Martinez H, Lane M. (1999). Fetal development after transfer is increased by replacing protein with the glycosaminoglycan hyaluronan for mouse embryo culture and transfer. Hum Reprod 14: 2575-2580.

Ghosh P, Guidolin D. (2002). Potential mechanism of action of intraarticular hyaluronan therapy in osteoarthritis: are the eff ects molecular weight dependent? Semin Arthritis Rheum 32: 10-37.

Ghosh S, Jassal M. (2002). Use of polysaccharide fi bres for modem wound dressings. Indian J Fibre Textile Res 27: 434-450.

Gibbs DA, Merrill EW, Smith KA, Balazs EA. (1968). Rheology of hyaluronic acid. Biopolymers 6: 777-91.

Glogau RG. (2000). The risk of progression to invasive disease. J Am Acad Dermatol42: S23-S24.

Grootveld M, Henderson EB, Farrell A, Blake DR, Parkes HG, Haycock P. (1991). Oxidative damage to hyaluronate and glucose in synovial fl uid during exercise of the infl amed rheumatoid joint. Detection of abnormal low-molecular- mass metabolites by proton-N.M.R. spectroscopy. Biochem J 273: 459-467.

Guidolin DD, Ronchetti IP, Lini E. (2001). Morphological analysis of articular cartilage biopsies from a randomized. clinical study comparing the eff ects of 500-730 kDa sodium hyaluronate Hyalgan(R) and methylprednisolone acetate on primary osteoarthritis of the knee. Osteoarthritis Cartilage 9: 371-381.

Gurny R, Ibrahim H, Aebi A. (1987). Design and evaluation of controlled release systems for the eye. J Control Release 6: 367-373.

Haddad JJ, Harb HL. (2005). L-gamma-Glutamyl-L-cysteinyl-glycine (glutathione; GSH) and GSH-related enzymes in the regulation of pro- and anti-infl ammatory cytokines: a signaling transcriptional scenario for redox(y) immunologic sensor(s). Mol Immunol 42: 987-1014.

Hamburger MI, Lakhanpal S, Mooar PA, Oster D. (2003). Intra-articular hyaluronans: a review of product-specifi c safety profi les. Semin Arthritis Rheum32: 296-309.

Haubeck HD, Kock R, Fischer DC, van de Leur E, Hoff meister K, Greiling H. (1995). Transforming growth factor s1, a major stimulator of hyaluronan synthesis in human synovial lining cells. Arthritis Rheum 38: 669-677.

Herrero-Vanrell R, Fernandez-Carballido A, Frutos G, Cadorniga R. (2000). Enhancement of the mydriatic response to tropicamide by bioadhesive polymers. J Ocul Pharmacol Ther 16: 419-428.

Hills BA, Crawford RW. (2003) Normal and prosthetic synovial joints are lubricated by surface-active phospholipid: a hypothesis. J Arthroplasty 18: 499-505.

Hlavacek M. (1993). The role of synovial fl uid fi ltration by cartilage in lubrication of synovial joints. J Biomech 26(10): 1145-50.

Hochberg MC. (2000). Role of intra-articular hyaluronic acid preparations in medical management of osteoarthritis of the knee. Semin Arthritis Rheum30: 2-10. Hrabarova E, Valachova K, Rapta P, Soltes L. (2010). An alternative standard for trolox-equivalent antioxidant-capacity estimation based on thiol antioxidants. Comparative 2,2’-azinobis[3-ethylbenzothiazoline-6-sulfonic acid] decolorization and rotational viscometry study regarding hyaluronan degradation. Chemistry & Biodiversity 7(9): 2191-2200.

Hrabarova E, Valachova K, Rychly J, Rapta P, Sasinkova V, Malikova M, Soltes L. (2009). High-molar-mass hyaluronan degradation by Weissberger’s system: Pro- and anti-oxidative eff ects of some thiol compounds. Polymer Degradationand Stability 94: 1867-1875.

Hrabarova E, Valachova K, Juranek I, Soltes L. (2012). Free-radical degradation of high-molar-mass hyaluronan induced by ascorbate plus cupric ions: evaluation of antioxidative eff ect of cysteine-derived compounds. Chemistry& Biodiversity 9: 309-317.

Hrabarova E, Gemeiner P, Soltes L. (2007). Peroxynitrite: In vivo and in vitro synthesis and oxidant degradative action on biological systems regarding biomolecular injury and infl ammatory processes. Chem Pap 61: 417-437.

Hrabarova E, Valachova K, Juranek I, Šoltes L. (2011). Free-radical degradationof high-molar-mass hyaluronan induced by ascorbate plus cupric ions. Antioxidativeproperties of the Piešťany-spa curative waters from healing peloidand maturation pool. In: “Kinetics, Catalysis and Mechanism of Chemical Reactions” G. E. Zaikov (eds), Nova Science Publishers, New York, pp. 29-36.

Hrabarova E, Valachova K, Rychly J, Rapta P, Sasinkova V, Gemeiner P, Šoltes L. (2009). High-molar-mass hyaluronan degradation by the Weissberger´s system: pro- and antioxidative eff ects of some thiol compounds. Polym DegradStab 94: 1867-1875.

Hultberg M, Hultberg B. (2006). The eff ect of diff erent antioxidants on glutathione turnover in human cell lines and their interaction with hydrogen peroxide. Chem Biol Interact 163(3): 192-198.

Hutadilok N. Ghosh P, Brooks PM. (1988). Binding of haptoglobin. inter-α- trypsin inhibitor, and l proteinase inhibitor to synovial fl uid hyaluronate and the infl uence of these proteins on its degradation byoxygen derived free radicals. Ann Rheum Dis 47: 377-85.

Inoue M, Katakami C. (1993). The eff ect of hyaluronic-acid on corneal epithelial- cell proliferation. Invest Ophthalmol Vis Sci 34: 2313-2315.

Itano N, Kimata K. (2002). Mammalian hyaluronan synthases. IUBMB Life 54: 195-199.

Jaakma U, Zhang B R, Larsson B. (1997). Eff ects of sperm treatments on the invitro development of bovine oocytes in semidefi ned and defi ned media. Theriogenology 48: 711-720.

Jang G, Lee BC, Kang SK, Hwang WS. (2003). Eff ect of glycosaminoglycans on the preimplantation development of embryos derived from in vitro fertilization and somatic cell nuclear transfer. Reprod Fertil Dev 15: 179-185.

Jarvinen K, Jarvinen T, Urtti A. (1995). Ocular absorption following topical delivery.Adv Drug Dev Rev 16: 3-19.

Jay GD, Britt DE, Cha DJ. (2000). Lubricin is a product of megakaryocyte stimulating factor gene expression by human synovial fi broblasts. J Rheumatol27: 594-600.

Joly T, Nibart M, Thibier M. (1992). Hyaluronic-acid as a substitute for proteins in the deep-freezing of embryos from mice and sheep - an in vitro investigation. Theriogenology 37: 473-480.

Juranek I, Soltes L. (2012). Reactive oxygen species in joint physiology: Possiblemechanism of maintaining hypoxia to protect chondrocytes from oxygen excessvia synovial fl uid hyaluronan peroxidation. In: “Kinetics, Catalysis and Mechanism of Chemical Reactions: From Pure to Applied Science. Volume 2 - Tomorrow and Perspectives” R.M. Islamova, S.V. Kolesov, G.E. Zaikov (eds), Nova Science Publishers, New York pp. 1-10

Kano K, Miyano T, Kato S. (1998). Eff ects of glycosaminoglycans on the development of in vitro matured and fertilized porcine oocytes to the blastocyst stage in vitro. Biol Reprod 58: 1226-1232.

Kelly MA, Goldberg VM, Healy WL. (2003). Osteoarthritis and beyond: a consensus on the past, present, and future of hyaluronans in orthopedics. Orthopedics26: 1064-1079.

Kemmann E. (1998). Creutzfeldt-Jakob disease (CJD) and assisted reproductive technology (ART) - quantifi cation of risks as part of informed consent. Hum Reprod 13: 1777.

Kessler A, Biasibetti M, da Silva Melo DA, Wajner M, Dutra-Filho CS, de Souza Wyse AT, Wannmacher CMD. (2008). Antioxidant eff ect of cysteamine in brain cortex of young rats. Neurochem Res 33: 737-44.

Kim A, Checkla DM, Dehazya P, Chen WL. (2003). Characterization of DNAhyaluronan matrix for sustained gene transfer. J Control Release 90: 81-95.

Kirwan J. (2001). Is there a place for intra-articular hyaluronate in osteoarthritis of the knee? Knee 8: 93-101.

Knight AD, Levick JR. (1984). Morphometry of the ultrastructure of the bloodjoint barrier in the rabbit knee. Q J Exp Physiol 69: 271-288.

Kogan G. (2010). Hyaluronan - A High Molar mass messenger reporting on thestatus of synovial joints: part 1. Physiological status In: New Steps in Chemical and Biochemical Physics. ISBN: 97 8-1-61668-923 -0. pp. 121-133.

Kogan G, Soltes L, Stern R, Mendichi R. (2007a). Hyaluronic acid: A biopolymerwith versatile physico-chemical and biological properties. Chapter 31 - in: Handbook of Polymer Research: Monomers, Oligomers, Polymers and Composites. Pethrick R. A, Ballada A, Zaikov G. E. (eds.), Nova Science Publishers, New York, pp. 393-439.

Kogan G, Soltes L, Stern R, Gemeiner P. (2007). Hyaluronic acid: A natural biopolymer with a broad range of biomedical and industrial applications. BiotechnolLett 29: 17-25.

Kreil G. (1995). Hyaluronidases-A group of neglected enzymes. Protein Sciences4: 1666-1669.

Lane M, Maybach JM, Hooper K. (2003). Cryo-survival and development of bovine blastocysts are enhanced by culture with recombinant albumin and hyaluronan. Mol Reprod Dev 64: 70-78.

Langer K, Mutschler E, Lambrecht G. (1997). Methylmethacrylate sulfopropylmethacrylate copolymer nanoparticles for drug delivery - Part III. Evaluation as drug delivery system for ophthalmic applications. Int J Pharm 158: 219-231.

Lath D, Csomorova K, Kollarikova G, Stankovska M, Soltes L. (2005). Molar mass-intrinsic viscosity relationship of high-molar-mass yaluronans: Involvement of shear rate. Chem Pap 59: 291-293.

Laurent TC, Laurent UBG, Fraser JRE. (1996). The structure and function of hyaluronan: An over view. Immunology and Cell Biology 74: A1-A7.

Laurent TC. (1989). The biology of hyaluronan. In: Ciba Foundation Symposium.John Wiley and Sons, New York. 143: 1-298.

Laurent TC, Fraser JRE. (1992). Hyaluronan. FASEB J 6: 2397-2404.

Laurent TC. Laurent UBG, Fraser JRE. (1995). Functions of hyaluronan. AnnRheum Dis 54: 429-32.

Laurent TC, Ryan M, Pictruszkiewicz A. (1960). Fractionation of hyaluronic acid. The polydispersity of hyaluronic acid from the vitreous body. BiochimBiophys Acta 42: 476-85.

Levick JR. (1994). An analysis of the interaction between interstitial plasma protein, interstitial fl ow, and fenestral fi ltration and its application to synovium. Microvasc Res 47: 90-125.

Leyden J, Narins RS, Brandt F. (2003). A randomized, double-blind, multicenter comparison of the effi cacy and tolerability of Restylane versus Zyplast for the correction of nasolabial folds. Dermatol Surg 29: 588-595.

Lim ST, Forbes B, Berry DJ, Martin GP, Brown MB. (2002). In vivo evaluation of novel hyaluronan/chitosan microparticulate delivery systems for the nasal delivery of gentamicin in rabbits. Int J Pharm 231: 73-82.

Luo Y, Prestwich GD. (1999). Synthesis and selective cytotoxicity of a hyaluronic acid-antitumor bioconjugate. Bioconjug Chem 10: 755-763.

Luo Y, Ziebell MR, Prestwich GD. (2000). A hyaluronic acid-taxol antitumor bioconjugate targeted to cancer cells. Biomacromolecules 1: 208-218.

Maheu E, Ayral X, Dougados M. (2002). A hyaluronan preparation (500-730 kDa) in the treatment of osteoarthritis: a review of clinical trials with Hyalgan(R). Int J Clin Pract 56: 804-813.

Manuskiatti W, Maibach HI. (1996). Hyaluronic acid and skin: wound healing and aging. Int J Dermatol 35: 539-544.

Mazzucco D, Scott R, Spector M. (2004). Composition of joint fl uid in patients undergoing total knee replacement and revision arthroplasty: correlation with fl ow properties. Biomaterials 25: 4433-4445.

McCord JM. (1974). Free radicals and infl ammation: protection of synovial fl uid by superoxide dismutase. Science 185: 529-531.

McDonald JN, Levick JR. (1988). Morphology of surface synoviocytes in situ at normal and raised joint pressure, studied by scanning electron microscopy. Ann Rheum Dis 47: 232-240.

McDonald JN, Leviek JR. (1995). Eff ect of intra-articular hyaluronan on pressure- fl ow relation across synovium in anaesthetized rabbits. J Physiol485(Pt.1): 179-93.

Mendichi R, Soltes L. (2002). Hyaluronan molecular weight and polydispersity in some commercial intra-articular injectable preparations and in synovial fl uid Infl amm Res 51: 115-116.

Meyer K, Palmer JW. (1934). The polysaccharide of the vitreous humor. Journalof Biology and Chemistry 107: 629-634. Miltner O, Schneider U, Siebert CH. (2002). Effi cacy of intraarticular hyaluronic acid in patients with osteoarthritis-a prospective clinical trial. OsteoarthritisCartilage 10: 680-686.

Miyano T, Hirooka RE, Kano K. (1994). Eff ects of hyaluronic-acid on the development of 1-cell and 2-cell porcine embryos to the blastocyst stage invitro. Theriogenology 41: 1299-1305.

Miyazaki M, Sato S, Yamaguchi T. (1983). Analgesic and antiinfl ammatory actionof hyaluronic sodium, Japan Pharmacological Conference. Tokyo, April 4, 1983.

Miyazaki T, Miyauchi S, Nakamura T. (1996). The eff ect of sodium hyaluronate on the growth of rabbit cornea epithelial cells in vitro. J Ocul PharmacolTher 12: 409-415.

Momberger TS, Levick JR, Mason RM. (2005). Hyaluronan secretion by synoviocytes is mechanosensitive. Matrix Biol 24: 510-519.

Moreira CA, Armstrong DK, Jelliff e RW. (1991). Sodium hyaluronate as a carrier for intravitreal gentamicin - an experimental study. Acta Ophthalmol(Copenh) 69: 45-49.

Moreira CA, Moreira AT, Armstrong DK. (1991). In vitro and in vivo studies with sodium hyaluronate as a carrier for intraocular gentamicin. Acta Ophthalmol(Copenh) 69: 50-56.

Morimoto K, Metsugi K, Katsumata H. (2001). Eff ects of lowviscosity sodium hyaluronate preparation on the pulmonary absorption of rh-insulin in rats. Drug Dev Ind Pharm 27: 365-371.

Morimoto K, Yamaguchi H, Iwakura Y. (1991). Eff ects of viscous hyaluronatesodium solutions on the nasal absorption of vasopressin and an analog. Pharmacol Res 8: 471-474.

Morris ER, Rees DA, Welsh EJ. (1980). Conformation and dynamic interactions in hyaluronate solutions. J Mol Biol 138: 383-400.

Myint P. (1987). The reactivity of various free radicals with hyaluronic acid steady-state and pulse radiolysis studies. Biochim Biophys-Aeta 925: 194-202.

Necas J, Bartosikova L, Brauner P, Kolar J. (2008). Hyaluronic acid (hyaluronan): a review. Veterinarni Medicina 53(8): 397-411.

Niwa Y, Sakane T, Shingu M, Yokoyama MM. (1983). Eff ect of stimulated neutrophils from the synovial fl uid of patients with rheumatoid arthritis on lymphocytes: a possible role of increased oxygen radicals generated by the neutrophils. J Clin Immunol 3: 228-240.

Noble PW. (2002). Hyaluronan and its catabolic products in tissue injury and repair. Matrix Biol 21: 25-29.

Oates KMN, Krause WE, Colby RH. (2002). Using rheology to probe the mechanism of joint lubrication: polyelectrolyte/protein interactions in synovial fl uid. Mat Res Soc Syrnp Proc 711: 53-58.

Ogston AG, Stanier JE. (1953). The physiological function of hyaluronic acid in synovial fl uid viscous, elastic and lubricant properties. J Physiol 199: 244-52.

Ortonne JP. (1996). A controlled study of the activity of hyaluronic acid in the treatment of venous leg ulcers. J Dermatol Treatment 7: 75-81.

Orvisky E, Soltes L, Chabrecek P, Novak I, Kery V, Stancikova M, Vins I. (1992). The determination of hyaluronan molecular weight distribution by means of high perfeormance size exclusion chromatography. J Liq Chromatogr 15: 3203-3218.

Parsons BJ, Al-Assaf S, Navaratnam S, Phillips GO. (2002). Comparison of thereactivity of diff erent oxidative species (ROS) towards hyaluronan, in: Kennedy JF, Phillips GO, Williams PA, Hascall VC (Eds.), Hyaluronan: Chemical, Biochemical and Biological Aspects, Woodhead, Publishing Ltd, Cambridge, MA, pp. 141-150.

Peer D, Florentin A, Margalit R. (2003). Hyaluronan is a key component in cryoprotection and formulation of targeted unilamellar liposomes. BiochimBiophys Acta-Biomembranes 1612: 76-82.

Peer D, Margalit R. (2000). Physicochemical evaluation of a stability-driven approach to drug entrapment in regular and in surface-modifi ed liposomes. Arch Biochem Biophys 383: 185-190.

Poli A, Mason RM, Levick JR. (2004). Eff ects of Arg- Gly-Asp sequence peptide and hyperosmolarity on the permeability of interstitial matrix and fenestrated endothelium in joints. Microcirculation 11: 463-476.

Praest BM, Greiling H, Kock R. (1997). Eff ects of oxygen-derived free radicals on the molecular weight and the polydispersity of hyaluronan solutions. Carbohydr Res 303 :153-157 .

Price FM, Levick JR, Mason RM. (1996). Glycosaminoglycan concentration in synovium and other tissues of rabbit knee in relation to synovial hydraulic resistance. J Physiol (Lond) 495: 803-820.

Prisell PT, Camber O, Hiselius J, Norstedt G. (1992). Evaluation of hyaluronan as a vehicle for peptide growth factors. Int J Pharm 85: 51-56.

Radin EL, Swann DA, Weisser PA. (1970). Separation of a hyaluronate-frec lubricating fraction from synovial fl uid. Nature 228: 377-8.

Rapta P, Valachova K, Gemeiner P, Soltes L. (2009). High-molar-mass hyaluronan behavior during testing its radical scavenging capacity in organic and aqueous media: Eff ects of the presence of Manganese (II) ions. Chem Biodivers6: 162-169.

Rapta P, Valachova K, Gemeiner P, Šoltes L. (2009). High-molar-mass hyaluronan behavior during testing its antioxidant properties in organic and aqueous media: eff ects of the presence of Mn(II) ions. Chem Biodivers 6: 162-169.

Rapta P, Valachova K, Zalibera M, Šnirc V, Šoltes L. (2010). Hyaluronan degradationby reactive oxygen species: scavenging eggect of the hexapyridoindole stobadineand two of its derivatives. In Monomers, Oligomers, Polymers, Composites, and Nanocomposites, Ed: R. A. Pethrick P. Petkov, A. Zlatarov G. E.

Zaikov, S. K. Rakovsky, Nova Science Publishers, N.Y, Chapter 7, pp. 113-126.

Rees MD, Kennett EC, Whitelock JM, Davies MJ. (2008). Oxidative damage to extracellular matrix and its role in human pathologies. Free Radical Biol. Med 44: 1973-2001.

Revell PA. (1989). Synovial lining cells. Rheumatol Int 9: 49-51.

Risberg B. (1997). Adhesions: preventive strategies. Eur J Surg 163: 32-39.

Rittig M, Tittor F, Lutjen-Drecoll E, Mollenhauer J, Rauterberg J. (1992). Immunohistochemical study of extracellular material in the aged human synovial membrane. Mech Ageing Dev 64: 219-234.

Rychly J, Soltes L, Stankovska M, Janigova I, Csomorova K, Sasinkova V, Kogan G, Gemeiner P. (2006). Unexplored capabilities of chemiluminescence and thermoanalytical methods in characterization of intact and degraded hyaluronans. Polym Degrad Stab 91(12): 3174-3184.

Saettone MF, Giannaccini B, Chetoni P, et al. (1991). Evaluation of highmolecular- weight and low-molecular-weight fractions of sodium hyaluronate and an ionic complex as adjuvants for topical ophthalmic vehicles containing pilocarpine. Int J Pharm 72: 131-139.

Saettone MF, Monti D, Torracca MT, Chetoni P. (1994). Mucoadhesive ophthalmic vehicles - evaluation polymeric low-viscosity formulations. J OculPharmacol 10: 83-92.

Sakurai K, Miyazaki K, Kodera Y. (1997). Anti-infl ammatory activity of superoxide dismutase conjugated with sodium hyaluronate. Glycoconj J 14: 723-728.

Sasaki H, Yamamura K, Nishida K. (1996). Delivery of drugs to the eye by topical application. Prog Retinal Eye Res 15: 583-620.

Sattar A, Kumar S, West DC. (1992). Does hyaluronan have a role in endothelial cell proliferation ofthe synovium. Semin. Arthritis Rheum 22: 37-43.

Schartz RA. (1997). The actinic keratoses. A perspective and update. DermatolSurg 23: 1009-1019.

Schiller J, Volpi N, Hrabarova E, Soltes L. (2011). Hyaluronic acid: a natural biopolymer In: Handbook of Biopolymers and Their ApplicationsS. Kalia and L. Averous (eds), Wiley & Scrivener Publishing, USA pp. 3-34.

Schmid T, Lindley K, Su J, Soloveychik V, Block J, Kuettner K, Schumacher B. (2001a). Superfi cial zone protein (SZP) is an abundant glycoprotein in human synovial fl uid and serum. Trans Orthop Res Soc 26: 82.

Schmid T, Soloveychik V, Kuettner K, Schumacher B. (2001b). Superfi cial zone protein (SZP) from human cartilage has lubrication activity. Trans OrthopRes Soc 26: 178.

Schumacher BL, Block JA, Schmid TM, Aydelotte MB, Kuettner KE. (1994). A novel proteoglycan synthesized and secreted by chondrocytes of the superfi cial zone of articular cartilage. Arch Biochem Biophys 311: 144-152.

Schumacher BL, Hughes CE, Kuettner KE, Caterson B, Aydelotte MB. (1999). Immunodetection and partial c DNA sequence of the proteoglycan, superfi cial zone protein, synthesized by cells lining synovial joints. J Orthop Res17: 110-120.

Schumacher BL, Schmidt TA, Voegtline MS, Chen AC, Sah RL. (2005). Proteoglycan 4 (PRG4) synthesis and immunolocalization in bovine meniscus. JOrthop Res 23: 562-568.

Schwarz IM, Hills BA. (1996). Synovial surfactant: lamellar bodies in type B synoviocytes and proteolipid in synovial fl uid and the articular lining. Br JRheumatol 35: 821-827.

Schwarz IM, Hills BA. (1998). Surface-active phospholipids as the lubricating component of lubricin. Br J Rheumatol 37: 21-26.

Scott DL, Shipley M, Dawson A, Edwards S, Symmons DP, Woolf AD. (1998).

The clinical management of rheumatoid arthritis and osteoarthritis: strategies for improving clinical eff ectiveness. Br J Rheumatol 37: 546-554. Scott JE, Cummings C, Brass A, Chen Y. (1991). Secondary and tertiary structures of hyaluronan in aqueous solution, investigated by rotary shadowingelectron microscopy and computer simulation. Biochem J 274: 600-705.

Servaty R, Schiller J, Binder H, Arnold K. (2000). Hydration of polymeric components of the cartilage - An infrared spectroscopic study on hyaluronic acid and chondroitin sulfate. Int J Biol Macromol 28: 123-129.

Simkovic I, Hricovini M, Soltes L, Mendichi R, Cosentino C. (2000). Preparation of water soluble/insoluble derivatives of Hyaluronic acid by cross linking with epichlorohydrin in aqueous NaOH/NH4OH solution. Carbohydr Polym41: 9-14.

Simon A, Safran A, Revel A. (2003). Hyaluronic acid can successfully replace albumin as the sole macromolecule in a human embryo transfer medium. Fertil Steril 79: 1434-1438.

Soldati D, Rahm F, Pasche P. (1999). Mucosal wound healing after nasal surgery. A controlled clinical trial on the effi cacy of hyaluronic acid containing cream. Drugs Exp Clin Res 25: 253-261.

Soloveva ME, Solovev VV, Faskhutdinova AA, Kudryavtsev AA, Akatov VS. (2007). Prooxidant and cytotoxic action of N-acetylcysteine and glutathione in combinations with vitamin B12b. Cell Tissue Biol 1: 40-49.

Soltes L, Kogan G. (2009). Impact of transition metals in the free-radical degradationof hyaluronan biopolymer In: “Kinetics & Thermodynamics for Chemistry & Biochemistry: Vol. 2” E. M. Pearce, G. E. Zaikov, G. Kirshenbaum (eds), Nova Science Publishers, New York (181-199).

Soltes L, Mendichi R, Kogan G, Mach M. (2004). Associating Hyaluronan Derivatives: A Novel Horizon in Viscosupplementation of Osteoarthritic Joints. Chem Biodivers 1: 468-472.

Soltes L, Brezova V, Stankovska M, Kogan G, Gemeiner P. (2006a). Degradation of high-molecular-weight hyaluronan by hydrogen peroxide in the presence of cupric ions. Carbohydr Res 341: 639-644.

Soltes L, Mendichi R, Kogan G, Schiller J, Stankovska M, Arnhold J. (2006b) Degradative action of reactive oxygen species on hyaluronan. Biomacromolecules7: 659-668.

Soltes L, Stankovska M, Brezova V, Schiller J, Arnhold J, Kogan G, Gemeiner P. (2006c). Hyaluronan degradation by copper (II) chloride and ascorbate: rotational viscometric, EPR spin-trapping, and MALDI-TOF mass spectrometric investigations Carbohydr Res 341: 2826-2834.

Soltes L, Stankovska M, Kogan G, Germeiner P, Stern R. (2005). Contribution of oxidative reductive reations to high molecular weight hyaluronan catabolism. Chem Biodivers 2: 1242-1245.

Soltes L, Valachova K, Mendichi R, Kogan G, Arnhold J, Gemeiner P. (2007). Solution properties of high-molar-mass hyaluronans: the biopolymer degradation by ascorbate. Carbohydr Res 342: 1071-1077.

Soltes L. (2010). Hyaluronan - A High-Molar-Mass Messenger Reporting on theStatus of Synovial Joints: Part II. Pathophysiological Status In: New Steps in Chemical and Biochemical Physics. Pure and Applied ScienceE. M. Pearce, G. Kirshenbaum, G. E. Zaikov (eds), Nova Science Publishers, New York pp. 137-152.

Stankovska M, Arnhold J, Rychly J, Spalteholz H, Gemeiner P, Soltes L. (2007). In vitro screening of the action of non-steroidal anti-infl ammatory drugs on hypochlorous acid-induced hyaluronan degradation. Polym Degrad Stabil92: 644-652.

Stankovska M, Soltes L, Vikartovska A, Mendichi r, Lath D, Molnarova M, Gemeiner P. (2004). Study of hyaluronan degradation by means of rotational Viscometry: Contribution of the material of viscometer. Chem Pap 58: 348-352.

Stankovska M, Hrabarova E, Valachova K, Molnarova M, Gemeiner P, Soltes L. (2006). The degradative action of peroxynitrite on high-molecular-weight hyaluronan . Neuroendocrinol Lett 27(Suppl. 2): 31-34.

Stankovska M, Soltes L, Vikartovska A, Gemeiner P, Kogan G, Bakos D. (2005). Degradation of high-molecular-weight hyaluronan: a rotational viscometry study. Biologia 60(Suppl. 17): 149-152.

Stern R, Kogan G, Jedrzejas M. J, Soltes L. (2007). The many ways to cleave hyaluronan. Biotechnol Adv 25: 537-557.

Stiebel-Kalish H, Gaton DD, Weinberger D. (1998). A comparison of the eff ect of hyaluronic acid versus gentamicin on corneal epithelial healing. Eye 12: 829-833.

Suchanek E, Simunic V, Juretic D, Grizelj V. (1994). Follicular-fl uid contents of hyaluronic-acid, follicle-stimulating-hormone and steroids relative to the success of in-vitro fertilization of human oocytes. Fertil Steril 62: 347-352.

Surendrakumar K, Martyn GP, Hodgers ECM. (2003). Sustained release of insulin from sodium hyaluronate based dry powder formulations after pulmonary delivery to beagle dogs. J Control Release 91: 385-394.

Surini S, Akiyama H, Morishita M. (2003). Polyion complex of chitosan and sodium hyaluronate as an implant device for insulin delivery. STP Pharm Sci13: 265-268.

Surovcikova L, Valachova K, Banasova M, Snirc V, Priesolova E, Nagy M, Juranek I, Soltes L. (2012). Free-radical degradation of high-molar-mass hyaluronan induced by ascorbate plus cupric ions: Testing of stobadine and its two derivatives in function as antioxidants. General Physiol Biophys 31: 57-64.

Swann DA, Silver FH, Slayter HS, Staff ord W, Shore E. (1985). The molecular structure and lubricating activity of lubricin isolated from bovine and human synovial fl uids. Biochem J 225: 195-201.

Takayama K, Hirata M, Machida Y. (1990). Eff ect of interpolymer complex-formation on bioadhesive property and drug release phenomenon of compressed tablet consisting of chitosan and sodium hyaluronate. Chem PharmaceutBull 38: 1993-1997.

Tani E, Katakami C, Negi A (2002). Eff ects of various eye drops on corneal wound healing after superfi cial keratectomy in rabbits. Jpn J Ophthalmol46: 488-495.

Tascioglu F, Oner C. (2003). Effi cacy of intra-articular sodium hyaluronate in the treatment of knee osteoarthritis. Clin Rheumatol 22: 112-117.

Thibodeau PA, Kocsis-Bedard S, Courteau J, Niyonsenga T, Paquette B. (2001).

Thiols can either enhance or suppress DNA damage induction by catecholestrogens. Free Radic Biol Med 30: 62-73.

Turino GM, Cantor JO. (2003). Hyaluronan in respiratory injury and repair. AmJ Respir Crit Care Med 167: 1169-1175.

Uthman I, Raynauld JP, Haraoui B. (2003). Intra-articular therapy in osteoarthritis. Postgrad Med J 79: 449-453.

Valachova K, Vargova A, Rapta P, Hrabarova E, Drafi F, Bauerova K, Juranek I, Soltes L. (2011). Aurothiomalate as preventive and chain-breaking antioxidant in radical degradation of high-molar-mass hyaluronan. Chemistry& Biodiversity 8: 1274-1283.

Valachova K, Banasova M, Machova L, Juranek I, Bezek S, Soltes L. (2013b). Antioxidant activity of various hexahydropyridoindoles. Journal of InformationIntelligence and Knowledge 5: 15-32.

Valachova K, Hrabarova E, Priesolova E, Nagy M, Banasova M, Juranek I, Soltes L. (2011). Free-radical degradation of high-molecular-weight hyaluronan induced by ascorbate plus cupric ions. Testing of bucillamine and its SA981- metabolite as antioxidants. J Pharma & Biomedical Analysis 56: 664-670.

Valachova K, Hrabarova E, Drafi F, Juranek I, Bauerova K, Priesolova E, Nagy M, Šoltes L. (2010a). Ascorbate and Cu(II) induced oxidative degradation of high-molar-mass hyaluronan. Pro- and antioxidative eff ects of some thiols. Neuroendocrinol Lett 31(2): 101-104.

Valachova K, Hrabarova E, Gemeiner P, Šoltes L. (2008). Study of pro- and anti-oxidative properties of d-penicillamine in a system comprising highmolar- mass hyaluronan, ascorbate, and cupric ions. Neuroendocrinol Lett29: 697-701.

Valachova K, Hrabarova E, Juranek I, Šoltes L. (2011b). Radical degradation of high-molar-mass hyaluronan induced by Weissberger oxidative system.

Testing of thiol compounds in the function of antioxidants. 16th Interdisciplinary Slovak-Czech Toxicological Conference in Prague. Interdiscip Toxicol4(2): 65.

Valachova K, Kogan G, Gemeiner P, Šoltes L. (2008b). Hyaluronan degradation by ascorbate: Protective eff ects of manganese (II). Cellulose Chem. Technol 42(9-10): 473−483.

Valachova K, Kogan G, Gemeiner P, Šoltes L. (2009b). Hyaluronan degradationby ascorbate: protective eff ects of manganese (II) chloride. In: Progress in Chemistry and Biochemistry. Kinetics, Thermodynamics, Synthesis, Properties and Application, Nova Science Publishers, N.Y, Chapter 20, pp. 201-215.

Valachova K, Mendichi R, Šoltes L. (2010c). Eff ect of L-glutathione on high-molar-mass hyaluronan degradation by oxidative system Cu(II) plus ascorbate. In: Monomers, Oligomers, Polymers, Composites, and Nanocomposites, Ed: R. A. Pethrick P. Petkov, A. Zlatarov G. E. Zaikov, S. K. Rakovsky, Nova Science Publishers, N.Y, Chapter 6, pp. 101-111.

Valachova K, Rapta P, Kogan G, Hrabarova E, Gemeiner P, Šoltes L. (2009a). Degradation of high-molar-mass hyaluronan by ascorbate plus cupric ions: eff ects of D-penicillamine addition. Chem Biodivers 6: 389-395.

Valachova K, Rapta P, Slovakova M, Priesolova E, Nagy M, Mislovičova D, Drafi F, Bauerova K, Šoltes L. (2013a). Radical degradation of high-molar-mass hyaluronaninduced by ascorbate plus cupric ions. Testing of arbutin in the functionof antioxidant. In: Advances in Kinetics and Mechanism of Chemical Reactions, G. E. Zaikov, A. J. M. Valente, A. L. Iordanskii (eds), Apple Academic Press, Waretown, NJ, USA, pp. 1-19. Valachova K, Šoltes L. (2010b). Eff ects of biogenic transition metal ions Zn(II)and Mn(II) on hyaluronan degradation by action of ascorbate plus Cu(II) ions. In: New Steps in Chemical and Biochemical Physics. Pure and Applied Science, Nova Science Publishers, Ed: E. M. Pearce, G. Kirshenbaum, G.E. Zaikov, Nova Science Publishers, N.Y, Chapter 10, pp. 153-160.

Valachova K, Vargova A, Rapta P, Hrabarova E, Drafi F, Bauerova K, Juranek I, Šoltes L. (2011a). Aurothiomalate in function of preventive and chainbreaking antioxidant at radical degradation of high-molar-mass hyaluronan. Chem Biodivers 8: 1274-1283.

Vanos HC, Drogendijk AC, Fetter WPF. (1991). The infl uence of contamination of culture-medium with hepatitis-B virus on the outcome of in vitro fertilization pregnancies. Am J Obstet Gynecol 165: 152-159.

Vazquez JR, Short B, Findlow AH. (2003). Outcomes of hyaluronan therapy in diabetic foot wounds. Diabetes Res Clin Pract 59: 123-127.

Weigel PH, Hascall VC, Tammi M. (1997). Hyaluronan synthases. J Biol Chem272: 13997-14000.

West DC, Hampson IN, Arnold F, Kumar S. (1985). Angiogenesis induced by degradation products of hyaluronic acid. Science 228: 1324-1326.

Wilkinson LS, Pitsillides AA, Worrall JG, Edwards JC. (1992). Light microscopic characterization of the fi broblastlike synovial intimal cell (synoviocyte). ArthritisRheum 35: 1179-1184.

Worrall JG, Bayliss MT, Edwards JC. (1991). Morphological localization of hyaluronan in normal and diseased synovium. J Rheumatol 18: 1466-1472.

Worrall JG, Wilkinson LS, Bayliss MT, Edwards JC. (1994). Zonal distribution of chondroitin-4-sulphate/ dermatan sulphate and chondroitin-6-sulphate in normal and diseased human synovium. Ann Rheum Dis 53: 35-38.

Yerushalmi N, Arad A, Margalit R. (1994). Molecular and cellular studies of hyaluronic acid-modifi ed liposomes as bioadhesive carriers for topical drugdelivery in wound-healing. Arch Biochem Biophys 313: 267-273.

Yerushalmi N, Margalit R. (1998). Hyaluronic acid-modifi ed bioadhesive liposomes as local drug depots: eff ects of cellular and fl uid dynamics on liposome retention at target sites. Arch Biochem Biophys 349: 21-26.

Yun YH, Goetz DJ, Yellen P, Chen W. (2004). Hyaluronan microspheres for sustained gene delivery and site-specifi c targetting. Biomaterials 25: 147-157.

Zhu YX, Granick S. (2003). Biolubrication: hyaluronic acid and the infl uence on its interfacial viscosity of an antiinfl ammatory drug. Macromolecules 36: 973-976.

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