The Knee Meniscus: A Complex Tissue of Diverse Cells

Article

Abstract

This review describes the knee meniscus and its diverse cell populations. Situated between the femur and tibia, the meniscus acts to transmit loads within the knee while maintaining joint stability. Not only does this tissue display complex geometry and anatomy, its cellular profile ranges from fibroblast-like to chondrocyte-like. When the tissue first begins to develop in the body, its cells are similar in shape and morphology, but as it matures, these cells take on distinct characteristics. The spindle-shaped cells of the outer meniscus are well-suited to maintaining a fibrous extracellular matrix rich in collagen type I. The round, inner meniscus cells produce both collagen types I and II, and glycosaminoglycans, giving rise to a hyaline-like inner portion of the tissue. Cells intermediately located display characteristics of both cell types. Fibrochondrocytes are also known to be highly dependent on mechanical stimulation to maintain healthy tissue, and display regional variation in response to different biomolecular cues. Investigating this cell population under a variety of conditions can lead to a better understanding of the pathophysiology and regenerative processes of the meniscus.

Keywords

Fibrochondrocytes Mechanosensitivity Growth factors Gene expression Development Anatomy 

References

  1. 1.
    Ahluwalia, S., M. Fehm, M. M. Murray, S. D. Martin, and M. Spector. Distribution of smooth muscle actin-containing cells in the human meniscus. J. Orthop. Res. 19(4):659–664, 2001.CrossRefGoogle Scholar
  2. 2.
    Aufderheide, A. C., and K. A. Athanasiou. Assessment of a bovine co-culture, scaffold-free method for growing meniscus-shaped constructs. Tissue Eng. 13(9):2195–2205, 2007.CrossRefGoogle Scholar
  3. 3.
    Bhargava, M. M., E. T. Attia, G. A. Murrell, M. M. Dolan, R. F. Warren, and J. A. Hannafin. The effect of cytokines on the proliferation and migration of bovine meniscal cells. Am. J. Sports Med. 27(5):636–643, 1999.Google Scholar
  4. 4.
    Brindle, T., J. Nyland, and D. L. Johnson. The meniscus: review of basic principles with application to surgery and rehabilitation. J. Athl. Train. 36(2):160–169, 2001.Google Scholar
  5. 5.
    Cao, M., M. Stefanovic-Racic, H. I. Georgescu, L. A. Miller, and C. H. Evans. Generation of nitric oxide by lapine meniscal cells and its effect on matrix metabolism: stimulation of collagen production by arginine. J. Orthop. Res. 16(1):104–111, 1998.CrossRefGoogle Scholar
  6. 6.
    Cheung, H. S. Distribution of type i, ii, iii and v in the pepsin solubilized collagens in bovine menisci. Connect. Tissue Res. 16(4):343–356, 1987.CrossRefMathSciNetGoogle Scholar
  7. 7.
    Clark, C. R., and J. A. Ogden. Development of the menisci of the human knee joint. Morphological changes and their potential role in childhood meniscal injury. J. Bone Joint Surg. Am. 65(4):538–547, 1983.Google Scholar
  8. 8.
    Collier, S., and P. Ghosh. Effects of transforming growth factor beta on proteoglycan synthesis by cell and explant cultures derived from the knee joint meniscus. Osteoarthr. Cartil. 3(2):127–138, 1995.CrossRefGoogle Scholar
  9. 9.
    Djurasovic, M., J. W. Aldridge, R. Grumbles, M. P. Rosenwasser, D. Howell, and A. Ratcliffe. Knee joint immobilization decreases aggrecan gene expression in the meniscus. Am. J. Sports Med. 26(3):460–466, 1998.Google Scholar
  10. 10.
    Fink, C., B. Fermor, J. B. Weinberg, D. S. Pisetsky, M. A. Misukonis, and F. Guilak. The effect of dynamic mechanical compression on nitric oxide production in the meniscus. Osteoarthr. Cartil. 9(5):481–487, 2001.CrossRefGoogle Scholar
  11. 11.
    Gemmiti, C. V., and R. E. Guldberg. Fluid flow increases type ii collagen deposition and tensile mechanical properties in bioreactor-grown tissue-engineered cartilage. Tissue Eng. 12(3):469–479, 2006.CrossRefGoogle Scholar
  12. 12.
    Ghadially, F. N., I. Thomas, N. Yong, and J. M. Lalonde. Ultrastructure of rabbit semilunar cartilages. J. Anat. 125(Pt 3):499–517, 1978.Google Scholar
  13. 13.
    Greis, P. E., D. D. Bardana, M. C. Holmstrom, and R. T. Burks. Meniscal injury: I. Basic science and evaluation. J. Am. Acad. Orthop. Surg. 10(3):168–176, 2002.Google Scholar
  14. 14.
    Gruber, H. E., D. Mauerhan, Y. Chow, J. A. Ingram, H. J. Norton, E. N. Hanley, Jr., and Y. Sun. Three-dimensional culture of human meniscal cells: extracellular matrix and proteoglycan production. BMC Biotechnol. 8:54, 2008.CrossRefGoogle Scholar
  15. 15.
    Gunja, N. J., R. K. Uthamanthil, and K. A. Athanasiou. Effects of tgf-beta1 and hydrostatic pressure on meniscus cell-seeded scaffolds. Biomaterials 30(4):565–573, 2009.Google Scholar
  16. 16.
    Hellio Le Graverand, M. P., Y. Ou, T. Schield-Yee, L. Barclay, D. Hart, T. Natsume, and J. B. Rattner. The cells of the rabbit meniscus: their arrangement, interrelationship, morphological variations and cytoarchitecture. J. Anat. 198(Pt 5):525–535, 2001.CrossRefGoogle Scholar
  17. 17.
    Hoben, G. M., and K. A. Athanasiou. Creating a spectrum of fibrocartilages through different cell sources and biochemical stimuli. Biotechnol. Bioeng. 100(3):587–598, 2008.CrossRefGoogle Scholar
  18. 18.
    Kambic, H. E., and C. A. McDevitt. Spatial organization of types i and ii collagen in the canine meniscus. J. Orthop. Res. 23(1):142–149, 2005.CrossRefGoogle Scholar
  19. 19.
    Marsano, A., D. Wendt, T. M. Quinn, T. J. Sims, J. Farhadi, M. Jakob, M. Heberer, and I. Martin. Bi-zonal cartilaginous tissues engineered in a rotary cell culture system. Biorheology 43(3–4):553–560, 2006.Google Scholar
  20. 20.
    McAlinden, A., J. Dudhia, M. C. Bolton, P. Lorenzo, D. Heinegard, and M. T. Bayliss. Age-related changes in the synthesis and mRNA expression of decorin and aggrecan in human meniscus and articular cartilage. Osteoarthr. Cartil. 9(1):33–41, 2001.CrossRefGoogle Scholar
  21. 21.
    Melrose, J., S. Smith, M. Cake, R. Read, and J. Whitelock. Comparative spatial and temporal localisation of perlecan, aggrecan and type i, ii and iv collagen in the ovine meniscus: an ageing study. Histochem. Cell Biol. 124(3–4):225–235, 2005.CrossRefGoogle Scholar
  22. 22.
    Mikic, B., T. L. Johnson, A. B. Chhabra, B. J. Schalet, M. Wong, and E. B. Hunziker. Differential effects of embryonic immobilization on the development of fibrocartilaginous skeletal elements. J. Rehabil. Res. Dev. 37(2):127–133, 2000.Google Scholar
  23. 23.
    Miller, R. R., and P. A. Rydell. Primary culture of microvascular endothelial cells from canine meniscus. J. Orthop. Res. 11(6):907–911, 1993.CrossRefGoogle Scholar
  24. 24.
    Moon, M. S., J. M. Kim, and I. Y. Ok. The normal and regenerated meniscus in rabbits. Morphologic and histologic studies. Clin. Orthop. Relat. Res. 182:264–269, 1984.Google Scholar
  25. 25.
    Mueller, S. M., T. O. Schneider, S. Shortkroff, H. A. Breinan, and M. Spector. Alpha-smooth muscle actin and contractile behavior of bovine meniscus cells seeded in type i and type ii collagen-gag matrices. J. Biomed. Mater. Res. 45(3):157–166, 1999.CrossRefGoogle Scholar
  26. 26.
    Mueller, S. M., S. Shortkroff, T. O. Schneider, H. A. Breinan, I. V. Yannas, and M. Spector. Meniscus cells seeded in type i and type ii collagen-gag matrices in vitro. Biomaterials 20(8):701–709, 1999.CrossRefGoogle Scholar
  27. 27.
    Nakata, K., K. Shino, M. Hamada, T. Mae, T. Miyama, H. Shinjo, S. Horibe, K. Tada, T. Ochi, and H. Yoshikawa. Human meniscus cell: characterization of the primary culture and use for tissue engineering. Clin. Orthop. Relat. Res. 391(Suppl):S208–218, 2001.CrossRefGoogle Scholar
  28. 28.
    Natsu-Ume, T., T. Majima, C. Reno, N. G. Shrive, C. B. Frank, and D. A. Hart. Menisci of the rabbit knee require mechanical loading to maintain homeostasis: Cyclic hydrostatic compression in vitro prevents derepression of catabolic genes. J. Orthop. Sci. 10(4):396–405, 2005.CrossRefGoogle Scholar
  29. 29.
    Neves, A. A., N. Medcalf, and K. M. Brindle. Tissue engineering of meniscal cartilage using perfusion culture. Ann. N Y Acad. Sci. 961:352–355, 2002.CrossRefGoogle Scholar
  30. 30.
    O’Reilly, M. S., T. Boehm, Y. Shing, N. Fukai, G. Vasios, W. S. Lane, E. Flynn, J. R. Birkhead, B. R. Olsen, and J. Folkman. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88(2):277–285, 1997.CrossRefGoogle Scholar
  31. 31.
    Ochi, K., Y. Daigo, T. Katagiri, A. Saito-Hisaminato, T. Tsunoda, Y. Toyama, H. Matsumoto, and Y. Nakamura. Expression profiles of two types of human knee-joint cartilage. J. Hum.Genet. 48(4):177–182, 2003.CrossRefGoogle Scholar
  32. 32.
    Ochi, M., T. Kanda, Y. Sumen, and Y. Ikuta. Changes in the permeability and histologic findings of rabbit menisci after immobilization. Clin. Orthop. Relat. Res. 334:305–315, 1997.CrossRefGoogle Scholar
  33. 33.
    Pangborn, C. A., and K. A. Athanasiou. Effects of growth factors on meniscal fibrochondrocytes. Tissue Eng. 11(7–8):1141–1148, 2005.CrossRefGoogle Scholar
  34. 34.
    Pangborn, C. A., and K. A. Athanasiou. Growth factors and fibrochondrocytes in scaffolds. J. Orthop. Res. 23(5):1184–1190, 2005.CrossRefGoogle Scholar
  35. 35.
    Park, L. S., J. A. Jacobson, D. A. Jamadar, E. Caoili, M. Kalume-Brigido, and E. Wojtys. Posterior horn lateral meniscal tears simulating meniscofemoral ligament attachment in the setting of ACL tear: MRI findings. Skeletal Radiol. 36(5):399–403, 2007.CrossRefGoogle Scholar
  36. 36.
    Pufe, T., W. J. Petersen, N. Miosge, M. B. Goldring, R. Mentlein, D. J. Varoga, and B. N. Tillmann. Endostatin/collagen xviii—an inhibitor of angiogenesis—is expressed in cartilage and fibrocartilage. Matrix Biol. 23(5):267–276, 2004.CrossRefGoogle Scholar
  37. 37.
    Spindler, K. P., C. E. Mayes, R. R. Miller, A. K. Imro, and J. M. Davidson. Regional mitogenic response of the meniscus to platelet-derived growth factor (pdgf-ab). J. Orthop. Res. 13(2):201–207, 1995.CrossRefGoogle Scholar
  38. 38.
    Tanaka, T., K. Fujii, and Y. Kumagae. Comparison of biochemical characteristics of cultured fibrochondrocytes isolated from the inner and outer regions of human meniscus. Knee Surg. Sports Traumatol. Arthrosc. 7(2):75–80, 1999.CrossRefGoogle Scholar
  39. 39.
    Upton, M. L., J. Chen, F. Guilak, and L. A. Setton. Differential effects of static and dynamic compression on meniscal cell gene expression. J. Orthop. Res. 21(6):963–969, 2003.CrossRefGoogle Scholar
  40. 40.
    Upton, M. L., F. Guilak, T. A. Laursen, and L. A. Setton. Finite element modeling predictions of region-specific cell-matrix mechanics in the meniscus. Biomech. Model Mechanobiol. 5(2–3):140–149, 2006.CrossRefGoogle Scholar
  41. 41.
    Upton, M. L., A. Hennerbichler, B. Fermor, F. Guilak, J. B. Weinberg, and L. A. Setton. Biaxial strain effects on cells from the inner and outer regions of the meniscus. Connect. Tissue Res. 47(4):207–214, 2006.CrossRefGoogle Scholar
  42. 42.
    Verdonk, P. C., R. G. Forsyth, J. Wang, K. F. Almqvist, R. Verdonk, E. M. Veys, and G. Verbruggen. Characterisation of human knee meniscus cell phenotype. Osteoarthr. Cartil. 13(7):548–560, 2005.CrossRefGoogle Scholar
  43. 43.
    Webber, R. J., M. G. Harris, and A. J. Hough, Jr. Cell culture of rabbit meniscal fibrochondrocytes: proliferative and synthetic response to growth factors and ascorbate. J. Orthop. Res. 3(1):36–42, 1985.CrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2009

Authors and Affiliations

  • Johannah Sanchez-Adams
    • 1
  • Kyriacos A. Athanasiou
    • 1
  1. 1.Department of BioengineeringRice UniversityHoustonUSA

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