Semi-permeable membrane retention of synovial fluid lubricants hyaluronan and proteoglycan 4 for a biomimetic bioreactor

Biotechnology and Bioengineering

Volumn 106, Issue 1, 2010, Pages 149-160

  Blewis, Megan E ^a   Lao, Brian J ^a   Jadin, Kyle D ^b   McCarty, William J ^a   Bugbee, William D ^c   Firestein, Gary S ^d   Sah, Robert L ^a,e  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b W L GORE AND ASSOCIATES   (United States)

^c School of Medicine ^*  (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Expanded polytetrafluoroethylene (ePTFE); Hyaluronan; Proteoglycan 4; Semi permeable membrane; Synovial fluid; Synoviocytes

Indexed keywords

EXPANDED POLYTETRAFLUOROETHYLENE (EPTFE); HYALURONAN; PROTEOGLYCANS; SEMI-PERMEABLE MEMBRANES; SYNOVIAL FLUID; SYNOVIOCYTES;

BIOCONVERSION; BIOMIMETICS; BIOREACTORS; BODY FLUIDS; CAPILLARITY; CELL CULTURE; EXPERIMENTS; FLUIDS; HYDROXYLATION; LUBRICANTS; THERMAL CONDUCTIVITY; TISSUE CULTURE;

MEMBRANES;

BIOMIMETIC MATERIAL; HYALURONIC ACID; INTERLEUKIN 1BETA; POLITEF; PROTEOGLYCAN; PROTEOGLYCAN 4; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; BIOENGINEERING; BIOREACTOR; BIOREACTOR DESIGN; BIOSYNTHESIS; CELL ADHESION; CELL CULTURE; CHANNEL GATING; CONTROLLED STUDY; HUMAN; HUMAN CELL; MEMBRANE PERMEABILITY; MEMBRANE TRANSPORT; MOLECULAR WEIGHT; NUTRIENT; SYNOVIAL FLUID; SYNOVIOCYTE;

BIOMIMETICS; BIOREACTORS; HYALURONIC ACID; LUBRICANTS; MEMBRANES; PERMEABILITY; PROTEOGLYCANS; SYNOVIAL FLUID; ULTRAFILTRATION;

EID: 77951554563     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.22645     Document Type: Article

References (65)

1. Afify A, Lynne LC, Howell L. 2007. Correlation of cytologic examination with ELISA assays for hyaluronan and soluble CD44v6 levels in evaluation of effusions. Diagn Cytopathol 35(2):105-110. (Pubitemid 46247142)
2. Albelda SM, Sampson PM, Haselton FR, McNiff JM, Mueller SN, Williams SK, Fishman AP, Levine EM. 1988. Permeability characteristics of cultured endothelial cell monolayers. J Appl Physiol 64(1):308-322. (Pubitemid 18042249)
3. Alvaro-Gracia JM, Zvaifler NJ, Firestein GS. 1990. Cytokines in chronic inflammatory arthritis. V. Mutual antagonism between interferongamma and tumor necrosis factor-alpha on HLA-DR expression, proliferation, collagenase production, and granulocyte macrophage colony-stimulating factor production by rheumatoid arthritis synoviocytes. J Clin Invest 86(6):1790-1798.
4. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS. 1988. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31(3):315-324.
5. Asari A, Miyauchi S, Matsuzaka S, Ito T, Kominami E, Uchiyama Y. 1998. Molecular weight-dependent effects of hyaluronate on the arthritic synovium. Arch Histol Cytol 61(2):125-135. (Pubitemid 28287656)
6. Balazs EA. 1974. The physical properties of synovial fluid and the special role of hyaluronic acid. In: Helfet AJ, editor. Disorders of the knee. Philadelphia: Lippincott Co. p 63-75.
7. Bartok B, Firestein GS. 2009. Fibroblast-like synoviocytes: Key effector cells in rheumatoid arthritis. Immunol Rev (in press).
8. Bellon JM, Bujan J, Honduvilla NG, Hernando A, Navlet J. 1993. Endothelial cell seeding of polytetrafluoroethylene vascular prostheses coated with a fibroblastic matrix. Ann Vasc Surg 7(6):549-555. (Pubitemid 24024998)
9. Bertone AL, Palmer JL, Jones J. 2001. Synovial fluid cytokines and eicosanoids as markers of joint disease in horses. Vet Surg 30(6):528-538. (Pubitemid 33601975)
10. Blewis ME, Nugent-Derfus GE, Schmidt TA, Schumacher BL, Sah RL. 2007. A model of synovial fluid lubricant composition in normal and injured joints. Eur Cell Mater 13:26-39.
11. Blewis ME, Lao BJ, Schumacher BL, Bugbee WD, Firestein GS, Sah RL. 2009. Interactive cytokine regulation of synoviocyte lubricant secretion. Tissue Eng (Epub ahead of print).
12. Charcosset C. 2006. Membrane processes in biotechnology: An overview. Biotechnol Adv 24(5):482-492.
13. Coleman PJ, Scott D, Ray J, Mason RM, Levick JR. 1997. Hyaluronan secretion into the synovial cavity of rabbit knees and comparison with albumin turnover. J Physiol 503(Pt 3):645-656. (Pubitemid 27496675)
14. Coleman PJ, Scott D, Abiona A, Ashhurst DE, Mason RM, Levick JR. 1998. Effect of depletion of interstitial hyaluronan on hydraulic conductance in rabbit knee synovium. J Physiol 509(Pt 3):695-710. (Pubitemid 28306134)
15. Coleman PJ, Scott D, Mason RM, Levick JR. 2000. Role of hyaluronan chain length in buffering interstitial flow across synovium in rabbits. J Physiol 526(Pt 2):425-434. (Pubitemid 30599292)
16. Dahl LB, Dahl IM, Engstrom-Laurent A, Granath K. 1985. Concentration and molecular weight of sodium hyaluronate in synovial fluid from patients with rheumatoid arthritis and other arthropathies. Ann Rheum Dis 44(12):817-822. (Pubitemid 16222234)
17. Fell HB, Jubb RW. 1977. The effect of synovial tissue on the breakdown of articular cartilage in organ culture. Arthritis Rheum 20(7):1359-1371.
18. Firestein GS. 1996. Invasive fibroblast-like synoviocytes in rheumatoid arthritis. Passive responders or transformed aggressors? Arthritis Rheum 39(11):1781-1790.
19. Flory PJ. 1971. Principles of polymer chemistry. Ithaca, NY, USA: Cornell University Press.
20. Fraser JR, Kimpton WG, Pierscionek BK, Cahill RN. 1993. The kinetics of hyaluronan in normal and acutely inflamed synovial joints: Observations with experimental arthritis in sheep. Semin Arthritis Rheum 22(6 Suppl 1):9-17.
21. Geiler T, Kriegsmann J, Keyszer GM, Gay RE, Gay S. 1994. A new model for rheumatoid arthritis generated by engraftment of rheumatoid synovial tissue and normal human cartilage into SCID mice. Arthritis Rheum 37(11):1664-1671. (Pubitemid 24345815)
22. Grad S, Gogolewski S, Alini M, Wimmer MA. 2006. Effects of simple and complex motion patterns on gene expression of chondrocytes seeded in 3D scaffolds. Tissue Eng 12(11):3171-3179. (Pubitemid 44846421)
23. Granger HJ, Taylor AE. 1975. Permeability of connective tissue linings isolated from implanted capsules; implications for interstitial pressure measurements. Circ Res 36(1):222-228.
24. Gribbon P, Heng BC, Hardingham TE. 1999. The molecular basis of the solution properties of hyaluronan investigated by confocal fluorescence recovery after photobleaching. Biophys J 77(4):2210-2216. (Pubitemid 29463181)
25. Jay GD, Lane BP, Sokoloff L. 1992. Characterization of a bovine synovial fluid lubricating factor III. The interaction with hyaluronic acid. Connect Tissue Res 28(4):245-255.
26. Jensen LT, Henriksen JH, Olesen HP, Risteli J, Lorenzen I. 1993. Lymphatic clearance of synovial fluid in conscious pigs: The aminoterminal propeptide of type III procollagen. Eur J Clin Invest 23(12):778-784. (Pubitemid 24015619)
27. Jo H, Dull RO, Hollis TM, Tarbell JM. 1991. Endothelial albumin permeability is shear dependent, time dependent, and reversible. Am J Physiol 260(6 Pt 2):H1992-H1996.
28. Joosten LA, Netea MG, Kim SH, Yoon DY, Oppers-Walgreen B, Radstake TR, Barrera P, van de Loo FA, Dinarello CA, van den Berg WB. 2006. IL-32, a proinflammatory cytokine in rheumatoid arthritis. Proc Natl Acad Sci USA 103(9):3298-3303.
29. Kiener HP, Lee DM, Agarwal SK, Brenner MB. 2006. Cadherin-11 induces rheumatoid arthritis fibroblast-like synoviocytes to form lining layers in vitro. Am J Pathol 168(5):1486-1499.
30. Kim YJ, Sah RLY, Doong JYH, Grodzinsky AJ. 1988. Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 174(1):168-176.
31. Knight AD, Levick JR. 1984. Morphometry of the ultrastructure of the blood-joint barrier in the rabbit knee. Q J Exp Physiol 69(2):271-288.
32. Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, Ishiyama S, Saito S, Inoue K, Kamatani N, Gillespie MT, Martin TJ, Suda T. 1999. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103(9):1345-1352.
33. Laurent UB, Fraser JR, Engstrom-Laurent A, Reed RK, Dahl LB, Laurent TC. 1992. Catabolism of hyaluronan in the knee joint of the rabbit. Matrix 12(2):130-136.
34. Lee HG, Cowman MK. 1994. An agarose gel electrophoretic method for analysis of hyaluronan molecular weight distribution. Anal Biochem 219(2):278-287.
35. Levick JR. 1980. Contributions of the lymphatic and microvascular systems to fluid absorption from the synovial cavity of the rabbit knee. J Physiol 306:445-461.
36. Marks PH, Donaldson ML. 2005. Inflammatory cytokine profiles associated with chondral damage in the anterior cruciate ligament-deficient knee. Arthroscopy 21(11):1342-1347.
37. 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(3):232-240.
38. McGowan KB, Kurtis MS, Lottman LM, Watson D, Sah RL. 2002. Biochemical quantification of DNA in human articular and septal cartilage using PicoGreen and Hoechst 33258. Osteoarthritis Cartilage 10(7):580-587.
39. Nixon AJ, Haupt JL, Frisbie DD, Morisset SS, McIlwraith CW, Robbins PD, Evans CH, Ghivizzani S. 2005. Gene-mediated restoration of cartilage matrix by combination insulin-like growth factor-I/interleukin-1 receptor antagonist therapy. Gene Ther 12(2):177-186.
40. Noh I, Choi YJ, Son Y, Kim CH, Hong SH, Hong CM, Shin IS, Park SN, Park BY. 2006. Diffusion of bioactive molecules through the walls of the medial tissue-engineered hybrid ePTFE grafts for applications in designs of vascular tissue regeneration. J Biomed Mater Res A 79(4):943-953.
41. Nugent-Derfus GE, Takara T, O'Neill JK, Cahill SB, Gortz S, Pong T, Inoue H, Aneloski NM, Wang WW, Vega KI, Klein TJ, Hsieh-Bonassera ND, Bae WC, Burke JD, Bugbee WD, Sah RL. 2007. Continuous passive motion applied to whole joints stimulates chondrocyte biosynthesis of PRG4. Osteoarthritis Cartilage 15(5):566-574.
42. Ozturk AM, Yam A, Chin SI, Heong TS, Helvacioglu F, Tan A. 2008. Synovial cell culture and tissue engineering of a tendon synovial cell biomembrane. J Biomed Mater Res A 84(4):1120-1126.
43. Sabaratnam S, Mason RM, Levick JR. 2004. Filtration rate dependence of hyaluronan reflection by joint-to-lymph barrier: Evidence for concentration polarisation. J Physiol 557(Pt 3):909-922. (Pubitemid 38961625)
44. Sabaratnam S, Arunan V, Coleman PJ, Mason RM, Levick JR. 2005. Size selectivity of hyaluronan molecular sieving by extracellular matrix in rabbit synovial joints. J Physiol 567(Pt 2):569-581. (Pubitemid 41301052)
45. Sahagun G, Moore SA, Hart MN. 1990. Permeability of neutral vs. anionic dextrans in cultured brain microvascular endothelium. Am J Physiol 259(1 Pt 2):H162-H166. (Pubitemid 20247729)
46. Sakamoto T, Mizono S, Miyazaki K, Yamaguchi T, Toyoshima H, Namiki O. 1984. Biological fate of sodium hyaluronate (SPH): Studies on the distribution, metabolism, and excretion of 14C-SPH in rabbits after intra-articular administration. Pharmacometrics 28:375-387. (Pubitemid 14009384)
47. Saxena A, Tripathi BP, Kumar M, Shahi VK. 2009. Membrane-based techniques for the separation and purification of proteins: An overview. Adv Colloid Interface Sci 145(1-2):1-22.
48. Schmid T, Lindley K, Su J, Soloveychik V, Block J, Kuettner K, Schumacher B. 2001. Superficial zone protein (SZP) is an abundant glycoprotein in human synovial fluid and serum. Trans Orthop Res Soc 26:82.
49. Schmidt TA, Gastelum NS, Nguyen QT, Schumacher BL, Sah RL. 2007. Boundary lubrication of articular cartilage: Role of synovial fluid constituents. Arthritis Rheum 56(3):882-891. (Pubitemid 46399436)
50. Schmidt TA, Gastelum NS, Han EH, Nugent-Derfus GE, Schumacher BL, Sah RL. 2008. Differential regulation of proteoglycan 4 metabolism in cartilage by IL-1a, IGF-I, and TGF-b1. Osteoarthritis Cartilage 16(1):90-97.
51. Schmidt TA, Plaas AH, Sandy JD. 2009. Disulfide-bonded multimers of proteoglycan 4 (PRG4) are present in normal synovial fluids. Biochim Biophys Acta 1790:375-384.
52. Schumacher BL, Block JA, Schmid TM, Aydelotte MB, Kuettner KE. 1994. A novel proteoglycan synthesized and secreted by chondrocytes of the superficial zone of articular cartilage. Arch Biochem Biophys 311:144-152.
53. Scott D, Coleman PJ, Abiona A, Ashhurst DE, Mason RM, Levick JR. 1998. Effect of depletion of glycosaminoglycans and non-collagenous proteins on interstitial hydraulic permeability in rabbit synovium. J Physiol 511(Pt 2):629-643. (Pubitemid 28444629)
54. Scott D, Coleman PJ, Mason RM, Levick JR. 2000a. Concentration dependence of interstitial flow buffering by hyaluronan in synovial joints. Microvasc Res 59(3):345-353. (Pubitemid 30322261)
55. Scott D, Coleman PJ, Mason RM, Levick JR. 2000b. Interaction of intra-articular hyaluronan and albumin in the attenuation of fluid drainage from joints. Arthritis Rheum 43(5):1175-1182. (Pubitemid 30368197)
56. Smith MM, Ghosh P. 1987. The synthesis of hyaluronic acid by human synovial fibroblasts is influenced by the nature of the hyaluronate in the extracellular environment. Rheumatol Int 7(3):113-122. (Pubitemid 17139714)
57. Sokal RR, Rohlf FJ. 1995. Biometry. New York:WHFreeman and Co. 887 p.
58. Su J-L, Schumacher BL, Lindley KM, Soloveychik V, Burkhart W, Triantafillou JA, Kuettner KE, Schmid TM. 2001. Detection of superficial zone protein in human and animal body fluids by cross-species monoclonal antibodies specific to superficial zone protein. Hybridoma 20(3):149-157. (Pubitemid 32881309)
59. Sundarrajan M, Boyle DL, Chabaud-Riou M, Hammaker D, Firestein GS. 2003. Expression of the MAPK kinases MKK-4 and MKK-7 in rheumatoid arthritis and their role as key regulators of JNK. Arthritis Rheum 48(9):2450-2460. (Pubitemid 37129422)
60. Swann DA, Slayter HS, Silver FH. 1981. The molecular structure of lubricating glycoprotein-I, the boundary lubricant for articular cartilage. J Biol Chem 256(11):5921-5925.
61. Swann DA, Silver FH, Slayter HS, Stafford W, Shore E. 1985. The molecular structure and lubricating activity of lubricin isolated from bovine and human synovial fluids. Biochem J 225(1):195-201.
62. Thibault M, Poole AR, Buschmann MD. 2002. Cyclic compression of cartilage/bone explants in vitro leads to physical weakening, mechanical breakdown of collagen and release of matrix fragments. J Orthop Res 20(6):1265-1273. (Pubitemid 35363984)
63. Vickers SM, Johnson LL, Zou LQ, Yannas IV, Gibson LJ, Spector M. 2004. Expression of alpha-smooth muscle actin by and contraction of cells derived from synovium. Tissue Eng 10(7):1214-1223. (Pubitemid 39223799)
64. Visser NA, van Kampen GPJ, Dekoning MHMT, van der Korst JK. 1994. The effects of loading on the synthesis of biglycan and decorin in intact mature articular cartilage in vitro. Connect Tissue Res 30(4):241-250.
65. Walluscheck KP, Steinhoff G, Kelm S, Haverich A. 1996. Improved endothelial cell attachment on ePTFE vascular grafts pretreated with synthetic RGD-containing peptides. Eur J Vasc Endovasc Surg 12(3):321-330. (Pubitemid 26379148)