The role of hyaluronic acid in biomineralization

Abstract

Hyaluronic acid has been extensively investigated due to intrinsic properties of natural origin and strong ability to bind ions in water. Hyaluronic acid is an excellent crystal modifier because its abundant negatively charged carboxyl groups can bind the cations protruding from the crystal lattice. In this review, we mainly present the latest work focus on the role of hyaluronic acid in controlling the crystallization, breaking the symmetry of crystal, and the surface funtionalization of nanocrystals.

Keywords

hyaluronic acid / biomineralization / crystal growth / extracellular matrix / bone and cartilage repair

References

[1] Ropes M W, Robertson W V B, Rossmeisl E C, . Synovial fluid mucin. Acta Medica Scandinavica , 1947, 128(s196): 700–744
[2] Meyer K, Smyth E M, Dawson M H. The isolation of a mucopolysaccharide form synovial fluid. Journal of Biological Chemistry , 1939, 128: 319–327
[3] Meyer K, Palmer J W. The polysaccharide of the vitreous humour. Journal of Biological Chemistry , 1934, 107: 629–634
[4] Ropes M W, Bauer W. Synovial Fluid Changes in Joint Disease. Canbridge MA: Harvard University Press, 1953
[5] Sunblad L. Studies on hyaluronic acid in synovial fluids. Acta Societatis Medicorum Upsaliensis , 1953, 58(3–4): 113–238
[6] Sundblad L. Glycosaminoglycans and glycoproteins in synovial fluid. In: Balazs E A, Jeanloz R W, eds. The Amino Sugars . New York, London: Academic Press, 1964, 229–250
[7] Coleman P J, Scott D, Mason R M, . Characterization of the effect of high molecular weight hyaluronan on trans-synovial flow in rabbit knees. The Journal of Physiology , 1999, 514(1): 265–282
[8] Blumberg B S, Ogston A G. Physicochemical studies on hyaluronic acid. In: Chemistry and Biology Mucopolysaccha-rides (Ciba Foundation Symposium ). London: Churchill, 1953, 22–37
[9] Balazs E A. Physical chemistry of hyaluronic acid. Federation Proceedings , 1958, 17(4): 1086–1093
[10] Almond A, Sheehan J K, Brass A. Molecular dynamics simulations of the two disaccharides of hyaluronan in aqueous solution. Glycobiology , 1997, 7(5): 597–604
[11] Almond A, Brass A, Sheehan J K. Dynamic exchange between stabilized conformations predicted for hyaluronan tetrasacchari-des: comparison of molecular dynamics simulations with available NMR data. Glycobiology , 1998, 8(10): 973–980
[12] Almond A, Brass A, Sheehan J K. Oligosaccharides as model systems for understanding water-biopolymer interaction: hydrated dynamics of a hyaluronan decamer. Journal of Physical Chemistry B , 2000, 104(23): 5634–5640
[13] Almond A, Brass A, Sheehan J K. Deducing polymeric structure from aqueous molecular dynamics simulations of oligosaccha-rides: predictions from simulations of hyaluronan tetrasaccha-rides compared with hydrodynamic and X-ray fibre diffraction data. Journal of Molecular Biology , 1998, 284(5): 1425–1437
[14] Toole B P. Hyaluronan: from extracellular glue to pericellular cue. Nature Reviews Cancer , 2004, 4(7): 528–539
[15] Sutherland I W. Novel and established applications of microbial polysaccharides. Trends in Biotechnology , 1998, 16(1): 41–46
[16] Morimoto K, Yamaguchi H, Iwakura Y, . Effects of viscous hyaluronate-sodium solutions on the nasal absorption of vasopressin and an analogue. Pharmaceutical Research , 1991, 8(4): 471–474
[17] Luo Y, Ziebell M R, Prestwich G D. A hyaluronic acid-taxol antitumor bioconjugate targeted to cancer cells. Biomacromolecules , 2000, 1(2): 208–218
[18] Adams M E. Viscosupplementation: a treatment for osteoarthritis. Journal of Rheumatology , 1993, 20(s39): 1–24
[19] Han S Y, Han H S, Lee S C, . Mineralized hyaluronic acid nanoparticles as a robust drug carrier. Journal of Materials Chemistry , 2011, 21(22): 7996–8001
[20] Chen Z H, Zhou H H, Wang X L, . Controlled mineralization by extracellular matrix: monodisperse, colloidally stable calcium phosphate-hyaluronan hybrid nanospheres. Chemical Communications , 2010, 46(8): 1278–1280
[21] Chen Z H, Wang C H, Zhou H H, . Biomimetic crystallization of toplike calcite single crystals with an extensive (00.1) face in the presence of sodium hyaluronate. Crystal Growth & Design , 2010, 10(11): 4722–4727
[22] Chen Z H, Wang C H, Zhou H H, . Modulation of calcium oxalate crystallization by commonly consumed green tea. CrystEngComm , 2010, 12(3): 845–852
[23] Hou S, Xu Q, Tian W, . The repair of brain lesion by implantation of hyaluronic acid hydrogels modified with laminin. Journal of Neuroscience Methods , 2005, 148(1): 60–70
[24] Ren Y J, Zhou Z Y, Cui F Z, . Hyaluronic acid/polylysine hydrogel as a transfer system for transplantation of neural stem cells. Journal of Bioactive and Compatible Polymers , 2009, 24(1): 56–62
[25] Hardingham T E, Muir H. The specific interaction of hyaluronic acid with cartillage proteoglycans. Biochimica et Biophysica Acta , 1972, 279(2): 401–405
[26] Huang L, Cheng Y Y, Koo P L, . The effect of hyaluronan on osteoblast proliferation and differentiation in rat calvarial-derived cell cultures. Journal of Biomedical Materials Research Part A , 2003, 66A(4): 880–884
[27] Fraser J R E, Laurent T C, Laurent U B G. Hyaluronan: its nature, distribution, functions and turnover. Journal of Internal Medicine , 1997, 242(1): 27–33
[28] Laurent T C, Fraser J R. Hyaluronan. FASEB Journal , 1992, 6(7): 2397–2404
[29] Lowenstam H A, Weiner S. On Biomineralization. Oxford: Oxford University Press, 1989, 324
[30] Mann S, Webb J, Williams R J P. Biomineralization. Weinheim: VCH, 1989, 490
[31] Simkiss K, Wilbur K M. Biomineralization. San Diego, CA: Academic Press, 1989, 337
[32] Baeuerlein E. Biomineralization.Weinheim: Wiley-VCH, 2000, 294
[33] Mann S. Biomineralization. Oxford: Oxford University Press, 2001, 198
[34] Baeuerlein E. Handbook of Biomineralization. Biological Aspects and Structure Formation . Weinheim: Wiley-VCH, 2007, 440
[35] Arias J L, Fernandez M S. Biomineralization: From Paleontology to Materials Science. Santiago, Chile: Editorial Universitaria, 2007, 534
[36] Dorozhkin S V, Epple M. Biological and medical significance of calcium phosphates. Angewandte Chemie International Edition , 2002, 41(17): 3130–3146
[37] LeGeros R Z. In: Brown P W, Constantz B, eds. Hydroxyapatite and Related Materials. Boca Raton, FL: CRC, 1994, 3–28
[38] Rueger J M. Bone substitution materials. Current status and prospects. Der Orthopade , 1998, 27(2): 72–79
[39] LeGeros R Z, LeGeros J P. In: Schnettler R, Markgraf E, eds. Knochenersatzmaterialien und wachstumsfaktoren . Stuttgart: Thieme, 1997, 180 (in German)
[40] Choi J S, K?ller M, Müller D, . Verbesserung der biokompatibilit?t von Ni-Ti-Formged?chtnislegierungen (“Nitinol”) durch beschichtung mit calciumphosphaten aus l?sung. Biomedizinische Technik , 2001, 46(s1): 226–227 (in German)
[41] Ambard A J, Mueninghoff L. Calcium phosphate cement: review of mechanical and biological properties. Journal of Prosthodontics , 2006, 15(5): 321–328
[42] Saha S, Pal S. Mechanical properties of bone cement: a review. Journal of Biomedical Materials Research , 1984, 18(4): 435–462
[43] Gisep A, Wieling R, Bohner M, . Resorption patterns of calcium-phosphate cements in bone. Journal of Biomedical Materials Research Part A , 2003, 66A(3): 532–540
[44] Morejón-Alonso L, Ferreira O J B, Carrodeguas R G, . Bioactive composite bone cement based on α-tricalcium phosphate/tricalcium silicate. Journal of Biomedical Materials Research Part B: Applied Biomaterials , 2012, 100B(1): 94–102
[45] Brunner T J, Grass R N, Bohner M, . Effect of particle size, crystal phase and crystallinity on the reactivity of tricalcium phosphate cements for bone reconstruction. Journal of Materials Chemistry , 2007, 17(38): 4072–4078
[46] Henslee A M, Gwak D-H, Mikos A G, . Development of a biodegradable bone cement for craniofacial applications. Journal of Biomedical Materials Research Part A , 2012, 100A(9): 2252–2259
[47] James R, Deng M, Laurencin C T, . Nanocomposites and bone regeneration. Frontier of Materials Science , 2011, 5(4): 342–357
[48] Cui F Z, Wen H B, Su X W, . Microstructures of external periosteal callus of repaired femoral fracture in children. Journal of Structural Biology , 1996, 117(3): 204–208
[49] Zhang W, Liao S S, Cui F Z. Hierarchical self-assembly of nano-fibrils in mineralized collagen. Chemistry of Materials , 2003, 15(16): 3221–3226
[50] Zhang W, Huang Z L, Liao S S, . Nucleation sites of calcium phosphate crystals during collagen mineralization. Journal of the American Ceramic Society , 2003, 86(6): 1052–1054
[51] Cui F-Z, Li Y, Ge J. Self-assembly of mineralized collagen composites. Materials Science and Engineering R: Reports , 2007, 57(1–6): 1–27
[52] Cai Y, Liu Y, Yan W, . Role of hydroxyapatite nanoparticle size in bone cell proliferation. Journal of Materials Chemistry , 2007, 17(36): 3780–3787
[53] Bako? D, Soldán M, Hernández-Fuentes I. Hydroxyapatite–collagen–hyaluronic acid composite. Biomaterials , 1999, 20(2): 191–195
[54] Solchaga L A, Dennis J E, Goldberg V M, . Hyaluronic acid-based polymers as cell carriers for tissue-engineered repair of bone and cartilage. Journal of Orthopaedic Research , 1999, 17(2): 205–213
[55] Aebli N, Stich H, Schawalder P, . Effects of bone morphogenetic protein-2 and hyaluronic acid on the osseointegration of hydroxyapatite-coated implants: an experimental study in sheep. Journal of Biomedical Materials Research Part A , 2005, 73A(3): 295–302
[56] Yoshikawa M, Tsuji N, Toda T, . Osteogenic effect of hyaluronic acid sodium salt in the pores of a hydroxyapatite scaffold. Materials Science and Engineering C , 2007, 27(2): 220–226
[57] Ishikawa Y, Komotori J, Senna M. Properties of hydroxyapatite-hyaluronic acid nano-composite sol and its interaction with natural bones and collagen fibers. Current Nanoscience , 2006, 2(3): 191–196
[58] Shen H, Tan J, Saltzman W M. Surface-mediated gene transfer from nanocomposites of controlled texture. Nature Materials , 2004, 3(8): 569–574
[59] Maitra A. Calcium phosphate nanoparticles: second-generation nonviral vectors in gene therapy. Expert Review of Molecular Diagnostics , 2005, 5(6): 893–905
[60] Sokolova V, Epple M. Inorganic nanoparticles as carriers of nucleic acids into cells. Angewandte Chemie International Edition , 2008, 47(8): 1382–1395
[61] Sokolova V V, Radtke I, Heumann R, . Effective transfection of cells with multi-shell calcium phosphate–DNA nanoparticles. Biomaterials , 2006, 27(16): 3147–3153
[62] Chowdhury E H, Kutsuzawa K, Akaike T. Designing smart nano-apatite composites: the emerging era of non-viral gene delivery. Gene Therapy & Molecular Biology , 2005, 9: 301–315
[63] Sokolova V, Kovtun A, Prymak O, . Functionalisation of calcium phosphate nanoparticles by oligonucleotides and their application for gene silencing. Journal of Materials Chemistry , 2007, 17(8): 721–727
[64] Pedraza C E, Bassett D C, McKee M D, . The importance of particle size and DNA condensation salt for calcium phosphate nanoparticle transfection. Biomaterials , 2008, 29(23): 3384–3392
[65] Kakizawa Y, Miyata K, Furukawa S, . Size-controlled formation of a calcium phosphate-based organic–inorganic hybrid vector for gene delivery using poly(ethylene glycol)-block-poly(aspartic acid). Advanced Materials , 2004, 16(8): 699–702
[66] Welzel T, Radtke I, Meyer-Zaika W, . Transfection of cells with custom-made calcium phosphate nanoparticles coated with DNA. Journal of Materials Chemistry , 2004, 14(14): 2213–2217
[67] Donners J J J M, Nolte R J M, Sommerdijk N A J M. Dendrimer-based hydroxyapatite composites with remarkable materials. Advanced Materials , 2003, 15(4): 313–316
[68] Shkilnyy A, Friedrich A, Tiersch B, . Poly(ethylene imine)-controlled calcium phosphate mineralization. Langmuir , 2008, 24(5): 2102–2109
[69] Schmidt H T, Gray B L, Wingert P A, . Assembly of aqueous-cored calcium phosphate nanoparticles for drug deli-very. Chemistry of Materials , 2004, 16(24): 4942–4947
[70] Sauer M, Haefele T, Graff A, . Ion-carrier controlled precipitation of calcium phosphate in giant ABA triblock copolymer vesicles. Chemical Communications , 2001, 23(23): 2452–2453
[71] Sugawara A, Yamane S, Akiyoshi K. Nanogel-templated mineralization: polymer-calcium phosphate hybrid nanomaterials. Macromolecular Rapid Communications , 2006, 27(6): 441–446
[72] Perkin K K, Turner J L, Wooley K L, . Fabrication of hybrid nanocapsules by calcium phosphate mineralization of shell cross-linked polymer micelles and nanocages. Nano Letters , 2005, 5(7): 1457–1461
[73] Ethirajan A, Ziener U, Chuvilin A, . Biomimetic hydroxyapatite crystallization in gelatin nanoparticles synthesized using a miniemulsion process. Advanced Functional Materials , 2008, 18(15): 2221–2227
[74] Wang X, Zhuang J, Peng Q, . Liquid-solid-solution synthesis of biomedical hydroxyapatite nanorods. Advanced Materials , 2006, 18(15): 2031–2034
[75] Antonietti M, Breulmann M, G?ltner C G, . Inorganic/organic mesostructures with complex architectures: precipitation of calcium phosphate in the presence of double-hydrophilic block copolymers. Chemistry- A European Journal , 1998, 4(12): 2493–2500
[76] Song R Q, Xu A W, Antonietti M, . Calcite crystals with platonic shapes and minimal surfaces. Angewandte Chemie International Edition , 2009, 48(2): 395–399
[77] Han S, Han H S, Lee S C, . Mineralized hyaluronic acid nanoparticles as a robust drug carrier. Journal of Materials Chemistry , 2011, 21(22): 7996–8001
[78] Furth G, Knierim R, Buss V, . Binding of bivalent cations by hyaluronate in aqueous solution. International Journal of Biological Macromolecules , 2008, 42(1): 33–40
[79] Scott J E, Heatley F. Hyaluronan forms specific stable tertiary structures in aqueous solution: a ¹³C NMR study. Proceedings of the National Academy of Sciences of the United States of America , 1999, 96(9): 4850–4855
[80] Lippmann F. Sedimentary Carbonate Minerals. Berlin: Springer-Verlag, 1973
[81] Orme C A, Noy A, Wierzbicki A, . Formation of chiral morphologies through selective binding of amino acids to calcite surface steps. Nature , 2001, 411(6839): 775–779
[82] Fu G, Qiu S R, Orme C A, . Acceleration of calcite kinetics by abalone nacre proteins. Advanced Materials , 2005, 17(22): 2678–2683
[83] Kulp E A, Switzer J A. Electrochemical biomineralization: the deposition of calcite with chiral morphologies. Journal of the American Chemical Society , 2007, 129(49): 15120–15121
[84] Huang Y X, Buder J, Cardoso-Gil R, . Shape development and structure of a complex (otoconia-like?) calcite–gelatine composite. Angewandte Chemie International Edition , 2008, 47(43): 8280–8284
[85] Weissbuch I, Addadi L, Leiserowitz L. Molecular recognition at crystal interfaces. Science , 1991, 253(5020): 637–645
[86] Wolf S E, Loges N, Mathiasch B, . Phase selection of calcium carbonate through the chirality of adsorbed amino acids. Angewandte Chemie International Edition , 2007, 46(29): 5618–5623
[87] Lahav M, Leiserowitz L. Comments on “Mirror symmtry breaking” of the centrosymmetric CaCO₃ crystals with amino acids. Angewandte Chemie International Edition , 2008, 47(20): 3680–3682
[88] Loges N, Wolf S E, Panth?fer M, . Reply to “Mirror symmetry breaking” of the centrosymmetric CaCO₃ crystals with amino acids. Angewandte Chemie International Edition , 2008, 47(20): 3683–3686
[89] Wang T X, C?lfen H, Antonietti M. Nonclassical crystallization: mesocrystals and morphology change of CaCO₃ crystals in the presence of a polyelectrolyte additive. Journal of the American Chemical Society , 2005, 127(10): 3246–3247
[90] Wang T X, Antonietti M, C?lfen H. Calcite mesocrystals: “morphing” crystals by a polyelectrolyte. Chemistry- A European Journal , 2006, 12(22): 5722–5730
[91] Pastero L, Aquilano D. CaCO₃ (calcite)/Li₂CO₃ (zabuyelite) anomalous mixed crystals. Sector zoning and growth mecha-nisms. Crystal Growth & Design , 2008, 8(9): 3451–3460
[92] Rajam S, Mann S. Selective stabilization of the (001) face of calcite in the presence of lithium. Journal of the Chemical Society: Chemical Communications , 1990, 24(24): 1789–1791
[93] Pastero L, Costa E, Bruno M, . Morphology of calcite (CaCO₃) crystals growing from aqueous solutions in the presence of Li⁺ ions. Surface behavior of the {0001} form. Crystal Growth & Design , 2004, 4(3): 485–490
[94] Arias J L, Neira-Carrillo A, Arias J I, . Sulfated polymers in biological mineralization: a plausible source for bio-inspired engineering. Journal of Materials Chemistry , 2004, 14(14): 2154–2160
[95] Arias J L, Fernández M S. Polysaccharides and proteoglycans in calcium carbonate-based biomineralization. Chemical Reviews , 2008, 108(11): 4475–4482
[96] Chen Z H, Chen J Z, Li X D, . Unpublished work
[97] Yu H, Sheikholeslami R, Doherty W O S. The effects of silica and sugar on the crystallographic and morphological properties of calcium oxalate. Journal of Crystal Growth , 2004, 265(3–4): 592–603
[98] Grases F, García-Ferragut L, S?hnel O, . Study on calcium oxalate monohydrate renal uroliths I. Qualitative properties. Scandinavian Journal of Urology and Nephrology , 1995, 29(4): 413–419
[99] Demadis K D. In: Shah R K, ed. Compact Heat Exchangers and Enhancement Technology for the Process Industries . New York: Begell House Inc., 2003, 483–490
[100] Ak?n B, ?ner M, Bayram Y, . Effects of carboxylate-modified, “green” inulin biopolymers on the crystal growth of calcium oxalate. Crystal Growth & Design , 2008, 8(6): 1997–2005
[101] Millan A. Crystal growth shape of whewellite polymorphs: Influence of structure distortions on crystal shape. Crystal Growth & Design , 2001, 1(3): 245–254
[102] Wesson J A, Worcester E M, Kleinman J G. Role of anionic proteins in kidney stone formation: interaction between model anionic polypeptides and calcium oxalate crystals. Journal of Urology , 2000, 163(4): 1343–1348
[103] Joshi V S, Parekh B B, Joshi M J, . Herbal extracts of tribulus terrestris and bergenia ligulata inhibit growth of calcium oxalate monohydrate crystals in vitro. Journal of Crystal Growth , 2005, 275(1–2): e1403–e1408
[104] Li X, Zhang D, Lynch-Holm V J, . Isolation of a crystal matrix protein associated with calcium oxalate precipitation in vacuoles of specialized cells. Plant Physiology , 2003, 133(2): 549–559
[105] Backov R, Lee C M, Khan S R, . Calcium oxalate monohydrate precipitation at phosphatidylglycerol Langmuir monolayers. Langmuir , 2000, 16(14): 6013–6019
[106] Ouyang J M, Deng S P, Zhou N, . Effect of tartrates with various counterions on the precipitation of calcium oxalate in vesicle solutions. Colloids and Surfaces A: Physicochemical and Engineering Aspects , 2005, 256(1): 21–27
[107] Skrti? D, Filipovi?-Vincekovi? N, Babi?-Ivan?i? V, . Influence of sodium cholate on the crystallization of calcium oxalate. Journal of Crystal Growth , 1993, 133(3–4): 189–195
[108] Weaver M L, Qiu S R, Hoyer J R, . Inhibition of calcium oxalate monohydrate growth by citrate and the effect of the background electrolyte. Journal of Crystal Growth , 2007, 306(1): 135–145
[109] Jung T, Sheng X, Choi C K, . Probing crystallization of calcium oxalate monohydrate and the role of macromolecule additives with in situ atomic force microscopy. Langmuir , 2004, 20(20): 8587–8596
[110] Guo S, Ward M D, Wesson J A. Direct visualization of calcium oxalate monohydrate crystallization and dissolution with atomic force microscopy and the role of polymeric additives. Langmuir , 2002, 18(11): 4284–4291
[111] Akyol E, Bozkurt A, ?ner M. The effects of polyelectrolytes on the inhibition and aggregation of calcium oxalate crystallization. Polymers for Advanced Technologies , 2006, 17(1): 58–65
[112] Akyol E, ?ner M. Inhibition of calcium oxalate monohydrate crystal growth using polyelectrolytes. Journal of Crystal Growth , 2007, 307(1): 137–144
[113] Wang L, Qiu S R, Zachowicz W, . Modulation of calcium oxalate crystallization by linear aspartic acid-rich peptides. Langmuir , 2006, 22(17): 7279–7285
[114] Wesson J A, Worcester E M, Wiessner J H, . Control of calcium oxalate crystal structure and cell adherence by urinary macromolecules. Kidney International , 1998, 53(4): 952–957
[115] Sallis J D, Lumley M F. On the possible role of glycosaminoglycans as natural inhibitors of calcium oxalate stones. Investigative Urology , 1979, 16(4): 296–299
[116] Nishio S, Abe Y, Wakatsuki A, . Matrix glycosaminoglycan in urinary stones. Journal of Urology , 1985, 134(3): 503–505
[117] Angell A H, Resnick M I. Surface interaction between glycosaminoglycans and calcium oxalate. Journal of Urology , 1989, 141(5): 1255–1258
[118] Asselman M, Verhulst A, De Broe M E, . Calcium oxalate crystal adherence to hyaluronan-, osteopontin-, and CD44-expressing injured/regenerating tubular epithelial cells in rat kidneys. Journal of the American Society of Nephrology , 2003, 14(12): 3155–3166
[119] Coe F L, Evan A P, Worcester E M, . Three pathways for human kidney stone formation. Urological Research , 2010, 38(3): 147–160
[120] Verkoelen C F. Crystal retention in renal stone disease: a crucial role for the glycosaminoglycan hyaluronan? Journal of the American Society of Nephrology , 2006, 17(6): 1673–1687
[121] Asselman M, Williams J C, Evan A P, . Hyaluronan and stone disease. AIP Conference Proceedings , 2008, 1049: 133–144
[122] Jonassen J A, Cao L C, Honeyman T, . Intracellular events in the initiation of calcium oxalate stones. Nephron Experimental Nephrology , 2004, 98(2): e61–e64
[123] Ratkalkar V N, Kleinman J G. Mechanisms of stone formation. Clinical Reviews in Bone and Mineral Metabolism , 2011, 9(3–4): 187–197
[124] Khan S R, Kok D J. Modulators of urinary stone formation. Frontiers in Bioscience , 2004, 9(1–3): 1450–1482
[125] Khan S R. Role of renal epithelial cells in the initiation of calcium oxalate stones. Nephron Experimental Nephrology , 2004, 98(2): e55–e60
[126] Basavaraj D R, Biyani C S, Browning A J, . The role of urinary kidney stone inhibitors and promoters in the pathogenesis of calcium containing renal stones. EAU-EBU Update Series , 2007, 5(3): 126–136
[127] Schepers M S J, van der Boom B G, Romijn J C, . Urinary crystallization inhibitors do not prevent crystal binding. The Journal of Urology , 2002, 167(4): 1844–1847
[128] Knepper M A, Saidel G M, Hascall V C, . Concentration of solutes in the renal inner medulla: interstitial hyaluronan as a mechano-osmotic transducer. American Journal of Physiology- Renal Physiology , 2003, 284(3): F433–F446
[129] Hautmann R, Lehmann A, Komor S. Calcium and oxalate concentrations in human renal tissue: the key to the pathogenesis of stone formation? The Journal of Urology , 1980, 123(3): 317–319
[130] Verkoelen C F, Van Der Boom B G, Romijn J C. Identification of hyaluronan as a crystal-binding molecule at the surface of migrating and proliferating MDCK cells. Kidney International , 2000, 58(3): 1045–1054
[131] Niemeyer C M, Mirkin C A. Nanobiotechnology . Weinheim: Wiley-VCH, 2004
[132] Lee H, Choi S H, Park T G. Direct visualization of hyaluronic acid polymer chain by self-assembled one-dimensional array of gold nanoparticles. Macromolecules , 2006, 39(1): 23–25
[133] Jeong Y I, Kim S T, Jin S G, . Cisplatin-incorporated hyaluronic acid nanoparticles based on ion-complex formation. Journal of Pharmaceutical Sciences , 2008, 97(3): 1268–1276
[134] Kumar A, Sahoo B, Montpetit A, . Development of hyaluronic acid–Fe₂O₃ hybrid magnetic nanoparticles for targeted delivery of peptides. Nanomedicine: Nanotechnology, Biology and Medicine , 2007, 3(2): 132–137
[135] Lee Y, Lee H, Kim Y B, . Bioinspired surface immobilization of hyaluronic acid on monodisperse magnetite nanocrystals for targeted cancer imaging. Advanced Materials , 2008, 20(21): 4154–4157
[136] Laroui H, Grossin L, Léonard M, . Hyaluronate-covered nanoparticles for the therapeutic targeting of cartilage. Biomacromolecules , 2007, 8(12): 3879–3885
[137] Mendes R M, Silva G A B, Caliari M V, . Effects of single wall carbon nanotubes and its functionalization with sodium hyaluronate on bone repair. Life Sciences , 2010, 87(7–8): 215–222
[138] Kim J, Park K, Hahn S K. Effect of hyaluronic acid molecular weight on the morphology of quantum dot-hyaluronic acid conjugates. International Journal of Biological Macromolecules , 2008, 42(1): 41–45
[139] Bhang S H, Won N, Lee T J, . Hyaluronic acid-quantum dot conjugates for in vivo lymphatic vessel imaging. ACS Nano , 2009, 3(6): 1389–1398
[140] Erathodiyil N, Ying J Y. Functionalization of inorganic nanoparticles for bioimaging applications. Accounts of Chemical Research , 2011, 44(10): 925–935
[141] Cao M-R, Hou J, Zhang Q, . Preparation of hyaluronic acid-quantum dot conjugate and its application in tumor imaging. Chemical Journal of Chinese Universities , 2012, 33(03): 437–441
[142] Stadlinger B, Hintze V, Bierbaum S, . Biological functionalization of dental implants with collagen and glycosaminoglycans — A comparative study. Journal of Biomedical Materials Research Part B: Applied Biomaterials , 2012, 100B(2): 331–341