Atomic force microscopy reveals age-dependent changes in nanomechanical properties of the extracellular matrix of native human menisci: Implications for joint degeneration and osteoarthritis

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 10, Issue 8, 2014, Pages 1777-1785

  Kwok, Jeanie ^a,b,d   Grogan, Shawn ^d   Meckes, Brian ^c   Arce, Fernando ^a,c   Lal, Ratnesh ^a,b,c   D'Lima, Darryl ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d SCRIPPS CLINIC   (United States)

Author keywords

Atomic force microscopy; Meniscus; Nanomechanics; Osteoarthritis

Indexed keywords

ATOMIC FORCE MICROSCOPY; ELASTIC MODULI; ELASTICITY; NANOMECHANICS; STRESSES;

AGE-RELATED CHANGES; BIMODAL DISTRIBUTION; EXTRACELLULAR MATRICES; JOINT DEGENERATIONS; MECHANICAL HETEROGENEITY; MENISCUS; NANOMECHANICAL PROPERTY; OSTEOARTHRITIS;

TISSUE;

ADULT; AGED; AGING; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; ELASTICITY; EXTRACELLULAR MATRIX; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; JOINT DEGENERATION; KNEE MENISCUS; KNEE OSTEOARTHRITIS; MIDDLE AGED; MOLECULAR MECHANICS; VERY ELDERLY; YOUNG ADULT; YOUNG MODULUS; JOINT DISEASES; MECHANICAL STRESS; METABOLISM; OSTEOARTHRITIS; PHYSIOLOGY; PROCEDURES;

ADULT; AGED; AGED, 80 AND OVER; AGING; EXTRACELLULAR MATRIX; HUMANS; JOINT DISEASES; MICROSCOPY, ATOMIC FORCE; MIDDLE AGED; OSTEOARTHRITIS; STRESS, MECHANICAL; YOUNG ADULT;

EID: 84908575616     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2014.06.010     Document Type: Article

References (50)

1. Ahmed A., Burke D. in-vitro of measurement of static pressure distribution in synovial joints-part I: tibial surface of the knee. J Biomech Eng 1983, 105:216-225.
2. Mow V.C., Ratcliffe A. Structure and function of articular cartilage and meniscus. Basic orthop biomech 1997, 2:113-177.
3. Proctor C., Schmidt M., Whipple R., Kelly M., Mow V. Material properties of the normal medial bovine meniscus. J Orthop Res 1989, 7:771-782.
4. Radin E.L., de Lamotte F., Maquet P. Role of the menisci in the distribution of stress in the knee. Clin Orthop Relat Res 1984, 185:290-294.
5. Seedhom B., Hargreaves D. Transmission of the load in the knee joint with special reference to the role of the menisci part II: experimental results. Discussion and conclusions. Eng Med 1979, 8:220-228.
6. Shoemaker S., Markolf K. The role of the meniscus in the anterior-posterior stability of the loaded anterior cruciate-deficient knee. Effects of partial versus total excision. J Bone Joint Surg 1986, 68:71-79.
7. Shrive N., O'connor J., Goodfellow J. Load-bearing in the knee joint. Clin Orthop Relat Res 1978, 131:279-287.
8. Fairbank T. Knee joint changes after meniscectomy. J Bone Joint Surg Br 1948, 30:664-670.
9. Krause W., Pope M., Johnson R., Wilder D. Mechanical changes in the knee after meniscectomy. J Bone Joint Surg Am 1976, 58:599-604.
10. Lohmander L.S., Englund P.M., Dahl L.L., Roos E.M. The long-term consequence of anterior cruciate ligament and meniscus injuries osteoarthritis. Am J Sports Med 2007, 35:1756-1769.
11. Arnoczky S.P., Warren R.F. Microvasculature of the human meniscus. Am J Sports Med 1982, 10:90-95.
12. Day B., Mackenzie W., Shim S.S., Leung G. The vascular and nerve supply of the human meniscus. Arthroscopy 1985, 1:58-62.
13. Aspden R., Yarker Y., Hukins D. Collagen orientations in the meniscus of the knee joint. J Anat 1985, 140:371-380.
14. McDevitt C.A., Webber R.J. The ultrastructure and biochemistry of meniscal cartilage. Clin Orthop Relat Res 1990, 252:8-18.
15. Adams M.E., Billingham M.E., Muir H. The glycosaminoglycans in menisci in experimental and natural osteoarthritis. Arthritis Rheum 1983, 26:69-76.
16. Hellio Le Graverand M.-P., Vignon E., Otterness I., Hart D. Early changes in lapine menisci during osteoarthritis development: part I: cellular and matrix alterations. Osteoarthr Cartil 2001, 9:56-64.
17. Hellio Le Graverand M.-P., Vignon E., Otterness I., Hart D. Early changes in lapine menisci during osteoarthritis development Part II: molecular alterations. Osteoarthr Cartil 2001, 9:65-72.
18. Herwig J., Egner E., Buddecke E. Chemical changes of human knee joint menisci in various stages of degeneration. Ann Rheum Dis 1984, 43:635-640.
19. Ishihara G., Kojima T., Saito Y., Ishiguro N. Roles of metalloproteinase-3 and aggrecanase 1 and 2 in aggrecan cleavage during human meniscus degeneration. Orthop Rev 2009, 1:10-16.
20. Pauli C., Grogan S., Patil S., et al. Macroscopic and histopathologic analysis of human knee menisci in aging and osteoarthritis. Osteoarthr Cartil 2011, 19:1132-1141.
21. Binnig G., Quate C.F., Gerber C. Atomic force microscope. Phys Rev Lett 1986, 56:930-933.
22. McLeod M.A., Wilusz R.E., Guilak F. Depth-dependent anisotropy of the micromechanical properties of the extracellular and pericellular matrices of articular cartilage evaluated via atomic force microscopy. J Biomech 2013, 46:586-592.
23. Sanchez-Adams J., Wilusz R.E., Guilak F. Atomic force microscopy reveals regional variations in the micromechanical properties of the pericellular and extracellular matrices of the meniscus. J Orthop Res 2013, 31:1218-1225.
24. Rosenberg L. Chemical basis for the histological use of safranin O in the study of articular cartilage. J Bone Joint Surg 1971, 53:69-82.
25. Pauli C., Whiteside R., Heras F., et al. Comparison of cartilage histopathology assessment systems on human knee joints at all stages of osteoarthritis development. Osteoarthr Cartil 2012, 20:476-485.
26. Burman M.S., Sutro C.J. A study of the degenerative changes of the menisci of the knee joint, and the clinical significance thereof. J Bone Joint Surg 1933, 15:835-861.
27. Englund M. The role of the meniscus in osteoarthritis genesis. Med Clin N Am 2009, 93:37-43.
28. Loeser R.F. Age-related changes in the musculoskeletal system and the development of osteoarthritis. Clin Geriatr Med 2010, 26:371-386.
29. Bhattacharyya T., Gale D., Dewire P., et al. The clinical importance of meniscal tears demonstrated by magnetic resonance imaging in osteoarthritis of the knee*. J Bone Joint Surg 2003, 85:4-9.
30. Englund M., Guermazi A., Gale D., et al. Incidental meniscal findings on knee MRI in middle-aged and elderly persons. N Engl J Med 2008, 359:1108-1115.
31. Makris E.A., Hadidi P., Athanasiou K.A. The knee meniscus: structure-function, pathophysiology, current repair techniques, and prospects for regeneration. Biomaterials 2011, 32:7411-7431.
32. Arnoczky S.P., Warren R.F. The microvasculature of the meniscus and its response to injury. An experimental study in the dog. Am J Sports Med 1983, 11:131-141.
33. Cox J.S., Nye C.E., Schaefer W.W., Woodstein I.J. The degenerative effects of partial and total resection of the medial meniscus in dogs' knees. Clin Orthop Relat Res 1975, 109:178-183.
34. McDevitt C., MuIR H. Biochemical changes in the cartilage of the knee in experimental and natural osteoarthritis in the dog. J Bone Joint Surg Br 1976, 58:94-101.
35. Nakano T., Dodd C.M., Scott P.G. Glycosaminoglycans and proteoglycans from different zones of the porcine knee meniscus. J Orthop Res 1997, 15:213-220.
36. Joshi M.D., Suh J.K., Marui T., Woo S.L.Y. Interspecies variation of compressive biomechanical properties of the meniscus. J Biomed Mater Res 1995, 29:823-828.
37. Driban J.B., Sitler M.R., Barbe M.F., Balasubramanian E. Is osteoarthritis a heterogeneous disease that can be stratified into subsets?. Clin Rheumatol 2010, 29:123-131.
38. Felson D.T., Lawrence R.C., Dieppe P.A., et al. Osteoarthritis: new insights. Part 1: the disease and its risk factors. Ann Intern Med 2000, 133:635-646.
39. Wang X., Shen X., Li X., Mauli Agrawal C. Age-related changes in the collagen network and toughness of bone. Bone 2002, 31:1-7.
40. Verzijl N., Degroot J., Oldehinkel E., et al. Age-related accumulation of Maillard reaction products in human articular cartilage collagen. Biochem J 2000, 350:381-387.
41. Verzijl N., DeGroot J., Zaken C.B., et al. Crosslinking by advanced glycation end products increases the stiffness of the collagen network in human articular cartilage: a possible mechanism through which age is a risk factor for osteoarthritis. Arthritis Rheum 2002, 46:114-123.
42. Ingber D.E. Tensegrity: the architectural basis of cellular mechanotransduction. Annu Rev Physiol 1997, 59:575-599.
43. Ingber D.E. Mechanobiology and diseases of mechanotransduction. Ann Med 2003, 35:564-577.
44. Wang N., Butler J.P., Ingber D.E. Mechanotransduction across the cell surface and through the cytoskeleton. Science 1993, 260:1124-1127.
45. Wang N., Tytell J.D., Ingber D.E. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 2009, 10:75-82.
46. Discher D.E., Janmey P., Wang Y.-l. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
47. Fink C., Fermor B., Weinberg J., Pisetsky D., Misukonis M., Guilak F. The effect of dynamic mechanical compression on nitric oxide production in the meniscus. Osteoarthr Cartil 2001, 9:481-487.
48. Fermor B., Jeffcoat D., Hennerbichler A., Pisetsky D.S., Weinberg J.B., Guilak F. The effects of cyclic mechanical strain and tumor necrosis factor alpha on the response of cells of the meniscus. Osteoarthr Cartil 2004, 12:956-962.
49. Upton M.L., Chen J., Guilak F., Setton L.A. Differential effects of static and dynamic compression on meniscal cell gene expression. J Orthop Res 2003, 21:963-969.
50. Upton M.L., Guilak F., Laursen T.A., Setton L.A. Finite element modeling predictions of region-specific cell-matrix mechanics in the meniscus. Biomech Model Mechanobiol 2006, 5:140-149.