Effects of hydrostatic pressure on leporine meniscus cell-seeded PLLA scaffolds.

Hydrostatic pressure (HP) is an important component of the loading environment of the knee joint. Studies with articular chondrocytes and TMJ disc fibrochondrocytes have identified certain benefits of HP for tissue engineering purposes. However, similar studies with meniscus cells are lacking. Thus, in this experiment, the effects of applying 10 MPa of HP at three different frequencies (0, 0.1, and 1 Hz) to leporine meniscus cell-seeded PLLA scaffolds were examined. HP was applied once every 3 days for 1 h for a period of 28 days. Constructs were analyzed for cellular, biochemical, and biomechanical properties. At t = 4 weeks, total collagen/scaffold was found to be significantly higher in the 10 MPa, 0 Hz group when compared with other groups. This despite the fact that the cell numbers/scaffold were found to be lower in all HP groups when compared with the culture control. Additionally, the total GAG/scaffold, instantaneous modulus, and relaxation modulus were significantly increased in the 10 MPa, 0 Hz group when compared with the culture control. In summary, this experiment provides evidence for the benefit of a 10 MPa, 0 Hz stimulus, on both biochemical and biomechanical aspects, for the purposes of meniscus tissue engineering using PLLA scaffolds.

[1]  P. Saldiva,et al.  Histochemical and ultrastructural study of the extracellular matrix fibers in patellar tendon donor site scars and normal controls. , 1996, Journal of submicroscopic cytology and pathology.

[2]  Farshid Guilak,et al.  Regulation of matrix turnover in meniscal explants: role of mechanical stress, interleukin-1, and nitric oxide. , 2003, Journal of applied physiology.

[3]  L. Rosenberg Chemical basis for the histological use of safranin O in the study of articular cartilage. , 1971, The Journal of bone and joint surgery. American volume.

[4]  Jerry C. Hu,et al.  The effects of intermittent hydrostatic pressure on self-assembled articular cartilage constructs. , 2006, Tissue engineering.

[5]  Kyriacos A Athanasiou,et al.  Effects of temporal hydrostatic pressure on tissue-engineered bovine articular cartilage constructs. , 2009, Tissue engineering. Part A.

[6]  M. Ochi,et al.  Changes in the Permeability and Histologic Findings of Rabbit Menisci After Immobilization , 1997, Clinical orthopaedics and related research.

[7]  Nobuhiko Yui,et al.  Electrospun PLGA nanofiber scaffolds for articular cartilage reconstruction: mechanical stability, degradation and cellular responses under mechanical stimulation in vitro , 2006, Journal of biomaterials science. Polymer edition.

[8]  J. Rada,et al.  Visual deprivation upregulates extracellular matrix synthesis by chick scleral chondrocytes. , 1994, Investigative ophthalmology & visual science.

[9]  Kyriacos A Athanasiou,et al.  Effects of growth factors on meniscal fibrochondrocytes. , 2005, Tissue engineering.

[10]  A. Grodzinsky,et al.  Tissue shear deformation stimulates proteoglycan and protein biosynthesis in bovine cartilage explants. , 2001, Archives of biochemistry and biophysics.

[11]  K. Athanasiou,et al.  Biodegradable Materials in Arthroscopy , 2006, Sports medicine and arthroscopy review.

[12]  Kyriacos A Athanasiou,et al.  Comparison of scaffolds and culture conditions for tissue engineering of the knee meniscus. , 2005, Tissue engineering.

[13]  Lutz Claes,et al.  A three-dimensional collagen matrix as a suitable culture system for the comparison of cyclic strain and hydrostatic pressure effects on intervertebral disc cells. , 2005, Journal of neurosurgery. Spine.

[14]  Wasim S Khan,et al.  The matrix-forming phenotype of cultured human meniscus cells is enhanced after culture with fibroblast growth factor 2 and is further stimulated by hypoxia , 2006, Arthritis research & therapy.

[15]  W C Hutton,et al.  The effect of hydrostatic pressure on intervertebral disc metabolism. , 1999, Spine.

[16]  K. Athanasiou,et al.  Mechanical Stimulation Toward Tissue Engineering of the Knee Meniscus , 2004, Annals of Biomedical Engineering.

[17]  D. Schurman,et al.  Mechanoregulation of human articular chondrocyte aggrecan and type II collagen expression by intermittent hydrostatic pressure in vitro , 2003, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[18]  E H Burger,et al.  Mechanical loading stimulates the release of transforming growth factor‐β activity by cultured mouse calvariae and periosteal cells , 1995, Journal of cellular physiology.

[19]  S. Collier,et al.  Effects of transforming growth factor beta on proteoglycan synthesis by cell and explant cultures derived from the knee joint meniscus. , 1995, Osteoarthritis and cartilage.

[20]  D. R. Carter,et al.  In vitro stimulation of articular chondrocyte mRNA and extracellular matrix synthesis by hydrostatic pressure , 1996, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[21]  P. Heinrich,et al.  Transforming Growth Factor β1 Regulates Tissue Inhibitor of Metalloproteinases—1 Expression in Differentiated Human Articular Chondrocytes , 1994 .

[22]  Byung-Soo Kim,et al.  Regeneration of whole meniscus using meniscal cells and polymer scaffolds in a rabbit total meniscectomy model. , 2006, Journal of biomedical materials research. Part A.

[23]  A. Grodzinsky,et al.  Biosynthetic response of cartilage explants to dynamic compression , 1989, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[24]  R. Waters,et al.  Energy‐speed relationship of walking: Standard tables , 1988, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[25]  J. Vacanti,et al.  Tissue engineered meniscus: a potential new alternative to allogeneic meniscus transplantation. , 1997, Transplantation proceedings.

[26]  P. Walker,et al.  The role of the menisci in force transmission across the knee. , 1975, Clinical orthopaedics and related research.

[27]  P. Heinrich,et al.  Transforming growth factor beta 1 regulates tissue inhibitor of metalloproteinases-1 expression in differentiated human articular chondrocytes. , 1994, Arthritis and rheumatism.

[28]  P. Pirttiniemi,et al.  Comparison of Amounts and Properties of Collagen and Proteoglycans in Condylar, Costal and Nasal Cartilages , 1999, Cells Tissues Organs.

[29]  Andrés J. García,et al.  Oscillatory tension differentially modulates matrix metabolism and cytoskeletal organization in chondrocytes and fibrochondrocytes. , 2004, Journal of biomechanics.

[30]  K. Athanasiou,et al.  Design Characteristics for the Tissue Engineering of Cartilaginous Tissues , 2004, Annals of Biomedical Engineering.

[31]  W C Hutton,et al.  Contact pressures in the human hip joint. , 1987, The Journal of bone and joint surgery. British volume.

[32]  C. M. Agrawal,et al.  Intraspecies and Interspecies Comparison of the Compressive Properties of the Medial Meniscus , 2004, Annals of Biomedical Engineering.

[33]  K. Athanasiou,et al.  Toward tissue engineering of the knee meniscus. , 2001, Tissue engineering.

[34]  H. Helminen,et al.  Effects of cyclic hydrostatic pressure on proteoglycan synthesis in cultured chondrocytes and articular cartilage explants. , 1993, Archives of biochemistry and biophysics.

[35]  Hiroshi Ohshima,et al.  Muscle atrophy and bone loss after 90 days' bed rest and the effects of flywheel resistive exercise and pamidronate: results from the LTBR study. , 2005, Bone.

[36]  A. Grodzinsky,et al.  Combined effects of dynamic tissue shear deformation and insulin-like growth factor I on chondrocyte biosynthesis in cartilage explants. , 2003, Archives of biochemistry and biophysics.

[37]  J. Hassenpflug,et al.  Combination of reduced oxygen tension and intermittent hydrostatic pressure: a useful tool in articular cartilage tissue engineering. , 2001, Journal of biomechanics.

[38]  C. Frank,et al.  Menisci of the rabbit knee require mechanical loading to maintain homeostasis: cyclic hydrostatic compression in vitro prevents derepression of catabolic genes , 2005, Journal of orthopaedic science : official journal of the Japanese Orthopaedic Association.

[39]  S. Nicoll,et al.  Hydrostatic Pressure Differentially Regulates Outer and Inner Annulus Fibrosus Cell Matrix Production in 3D Scaffolds , 2008, Annals of Biomedical Engineering.

[40]  J. F. Woessner,et al.  The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. , 1961, Archives of biochemistry and biophysics.

[41]  K. Allen,et al.  A Surface–Regional and Freeze–Thaw Characterization of the Porcine Temporomandibular Joint Disc , 2005, Annals of Biomedical Engineering.

[42]  B. Seedhom,et al.  Upregulation of aggrecan and type II collagen mRNA expression in bovine chondrocytes by the application of hydrostatic pressure. , 2003, Biorheology.

[43]  F. Guilak,et al.  Simultaneous changes in the mechanical properties, quantitative collagen organization, and proteoglycan concentration of articular cartilage following canine meniscectomy , 2000, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[44]  K. Hasty,et al.  Chondrocyte response to cyclic hydrostatic pressure in alginate versus pellet culture , 2006, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[45]  S. Elder,et al.  Influence of Cyclic Hydrostatic Pressure on Fibrocartilaginous Metaplasia of Achilles Tendon Fibroblasts , 2006, Biomechanics and modeling in mechanobiology.

[46]  B. F. Morrey,et al.  Growth Factors and Fibrochondrocytes in Scaffolds , 2006 .

[47]  D R Carter,et al.  Time-dependent effects of intermittent hydrostatic pressure on articular chondrocyte type II collagen and aggrecan mRNA expression. , 2000, Journal of rehabilitation research and development.

[48]  A. Hall,et al.  Differential effects of hydrostatic pressure on cation transport pathways of isolated articular chondrocytes , 1999, Journal of cellular physiology.

[49]  C W Hutton,et al.  Knee Meniscus: Basic and Clinical Foundations , 1993 .

[50]  R. Wilkins,et al.  The cellular physiology of articular cartilage , 1996, Experimental physiology.

[51]  E. Thonar,et al.  Chondrocyte extracellular matrix synthesis and turnover are influenced by static compression in a new alginate disk culture system. , 2000, Archives of biochemistry and biophysics.

[52]  K. Athanasiou,et al.  Passage and reversal effects on gene expression of bovine meniscal fibrochondrocytes , 2007, Arthritis research & therapy.

[53]  Y. Toyama,et al.  Hydrostatic pressure modulates mRNA expressions for matrix proteins in human meniscal cells. , 2006, Biorheology.

[54]  Kyriacos A Athanasiou,et al.  Viscoelastic characterization of the porcine temporomandibular joint disc under unconfined compression. , 2006, Journal of biomechanics.

[55]  W. A. Hodge,et al.  Contact pressures in the human hip joint measured in vivo. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[56]  K. Athanasiou,et al.  Effects of hydrostatic pressure on TMJ disc cells. , 2006, Tissue engineering.

[57]  J. Steinmeyer,et al.  Proteoglycan metabolism and viability of articular cartilage explants as modulated by the frequency of intermittent loading. , 2003, Osteoarthritis and cartilage.

[58]  Stacy M. Imler,et al.  Combined effects of growth factors and static mechanical compression on meniscus explant biosynthesis. , 2004, Osteoarthritis and cartilage.

[59]  Georg Kemmler,et al.  Osteoarthritis After Arthroscopic Partial Meniscectomy , 1995, The American journal of sports medicine.