Changes in structural-mechanical properties and degradability of collagen during aging-associated modifications

Journal of Biological Chemistry

Volumn 290, Issue 38, 2015, Pages 23291-23306

  Panwar, Preety ^a   Lamour, Guillaume ^a   Mackenzie, Neil C W ^a   Yang, Heejae ^a   Ko, Frank ^a   Li, Hongbin ^a   Brömme, Dieter ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; ELASTIC MODULI; MAMMALS; MECHANICAL STABILITY; TISSUE;

ADVANCED GLYCATION END PRODUCTS; BONE RESORPTION; COLLAGEN NETWORKS; DEGRADABILITY; EXTRACELLULAR MATRICES; FIBRILLAR COLLAGENS; PROTEOLYTIC DEGRADATION; TYPE I COLLAGEN;

COLLAGEN;

ADVANCED GLYCATION END PRODUCT; CATHEPSIN K; COLLAGEN; COLLAGEN TYPE 1; CTSK PROTEIN, MOUSE;

AGING; ANALYSIS OF VARIANCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CARBOXY TERMINAL SEQUENCE; CENTRIFUGATION; COLORIMETRY; CONTROLLED STUDY; CORRELATION ANALYSIS; ELASTICITY; EXTRACELLULAR MATRIX; HYDROLYSIS; IN VITRO STUDY; MINERALIZATION; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN MODIFICATION; PROTEIN STABILITY; SCANNING ELECTRON MICROSCOPY; SPECTROPHOTOMETRY; YOUNG MODULUS; ANIMAL; BOVINE; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING;

AGING; ANIMALS; BONE RESORPTION; CATHEPSIN K; CATTLE; COLLAGEN; ELASTIC MODULUS; MICE; OSTEOCLASTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS;

EID: 84942867447     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.644310     Document Type: Article

References (76)

1. Fratzl, P. (ed) (2008) Collagen: Structure and Mechanics, pp. 1-505. Springer Science and Business Media, LLC, New York
2. Engel, J., and Bächinger, H. P. (2005) Structure, stability and folding of the collagen triple helix. Top. Curr. Chem. 247, 7-33
3. Orgel, J. P., Irving, T. C., Miller, A., and Wess, T. J. (2006) Microfibrillar structure of type I collagen in situ. Proc. Natl. Acad. Sci. U.S.A. 103, 9001-9005
4. Zhang, G., Ezura, Y., Chervoneva, I., Robinson, P. S., Beason, D. P., Carine, E. T., Soslowsky, L. J., Iozzo, R. V., and Birk, D. E. (2006) Decorin regulates assembly of collagen fibrils and acquisition of biomechanical properties during tendon development. J. Cell Biochem. 98, 1436-1449
5. Kalamajski, S., and Oldberg, A. (2010) The role of small leucine-rich proteoglycans in collagen fibrillogenesis. Matrix Biol. 29, 248-253
6. Gautieri, A., Vesentini, S., Redaelli, A., and Buehler, M. J. (2011) Hierarchical structure and nanomechanics of collagen microfibrils from the atomistic scale up. Nano. Lett. 11, 757-766
7. Connizzo, B. K., Sarver, J. J., Birk, D. E., Soslowsky, L. J., and Iozzo, R. V (2013) Effect of age and proteoglycan deficiency on collagen fiber re-alignment and mechanical properties in mouse supraspinatus tendon. J. Biomech. Eng. 135, 021019
8. Ameye, L., and Young, M. F. (2002) Mice deficient in small leucine-rich proteoglycans: novel in vivo models for osteoporosis, osteoarthritis, Ehlers-Danlos syndrome, muscular dystrophy, and corneal diseases. Glycobiology 12, 107-116
9. Cavalcante, F. S., Ito, S., Brewer, K., Sakai, H., Alencar, A. M., Almeida, M. P., Andrade, J. S., Jr., Majumdar, A., Ingenito, E. P., and Suki, B. (2005) Mechanical interactions between collagen and proteoglycans: implications for the stability of lung tissue. J. Appl. Physiol. 98, 672-679
10. Mays, P. K., McAnulty, R. J., Campa, J. S., and Laurent, G. J. (1991) Agerelated changes in collagen synthesis and degradation in rat tissues. Importance of degradation of newly synthesized collagen in regulating collagen production. Biochem. J. 276, 307-313
11. Rolewska, P., Al-Robaiy, S., Navarrete Santos, A., Simm, A., Silber, R.-E., and Bartling, B. (2013) Age-related expression, enzymatic solubility and modification with advanced glycation end products of fibrillar collagens in mouse lung. Exp. Gerontol. 48, 29-37
12. Varani, J., Dame, M. K., Rittie, L., Fligiel, S. E., Kang, S., Fisher, G. J., and Voorhees, J. J. (2006) Decreased collagen production in chronologically aged skin: roles of age-dependent alteration in fibroblast function and defective mechanical stimulation. Am. J. Pathol. 168, 1861-1868
13. Hofbauer, L. C., Brueck, C. C., Shanahan, C. M., Schoppet, M., and Dobnig, H. (2007) Vascular calcification and osteoporosis-from clinical observation towards molecular understanding. Osteoporos Int. 18, 251-259
14. Tang, S. Y., and Vashishth, D. (2011) The relative contributions of nonenzymatic glycation and cortical porosity on the fracture toughness of aging bone. J. Biomech. 44, 330-336
15. Sell, D. R., and Monnier, V. M. (2012) Molecular basis of arterial stiffening: role of glycation-a mini-review. Gerontology 58, 227-237
16. Verzijl, N., DeGroot, J., Ben, Z. C., Brau-Benjamin, O., Maroudas, A., Bank, R. A., Mizrahi, J., Schalkwijk, C. G., Thorpe, S. R., Baynes, J. W., Bijlsma, J. W., Lafeber, F. P., and TeKoppele, J. M. (2002) 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. 46, 114-123
17. Verzijl, N., DeGroot, J., Thorpe, S. R., Bank, R. A., Shaw, J. N., Lyons, T. J., Bijlsma, J. W., Lafeber, F. P., Baynes, J. W., and TeKoppele, J. M. (2000) Effect of collagen turnover on the accumulation of advanced glycation end products. J. Biol. Chem. 275, 39027-39031
18. Fuerst, M., Bertrand, J., Lammers, L., Dreier, R., Echtermeyer, F., Nitschke, Y., Rutsch, F., Schäfer, F. K., Niggemeyer, O., Steinhagen, J., Lohmann, C. H., Pap, T., and Rüther, W. (2009) Calcification of articular cartilage in human osteoarthritis. Arthritis Rheum. 60, 2694-2703
19. Johnson, R. C., Leopold, J. A., and Loscalzo, J. (2006) Vascular calcification: pathobiological mechanisms and clinical implications. Circ. Res. 99, 1044-1059
20. Rodriguez, K. J., Piechura, L. M., Porras, A. M., and Masters, K. S. (2014) Manipulation of valve composition to elucidate the role of collagen in aortic valve calcification. BMC Cardiovasc. Disord. 14, 29
21. Martin, K. J., and González, E. A. (2007) Metabolic bone disease in chronic kidney disease. J. Am. Soc. Nephrol. 18, 875-885
22. Basta, G., Schmidt, A. M., and De Caterina, R. (2004) Advanced glycation end products and vascular inflammation: implications for accelerated atherosclerosis in diabetes. Cardiovasc. Res. 63, 582-592
23. Noordzij, M. J., Lefrandt, J. D., and Smit, A. J. (2008) Advanced glycation end products in renal failure: an overview. J. Ren. Care 34, 207-212
24. Avery, N. C., and Bailey, A. J. (2006) The effects of the Maillard reaction on the physical properties and cell interactions of collagen. Pathol. Biol. 54, 387-395
25. Garnero, P. (2012) The contribution of collagen crosslinks to bone strength. Bonekey Rep. 1, 182
26. Cox, T. R., and Erler, J. T. (2011) Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis. Models Mech. 4, 165-178
27. Lu, P., Takai, K., Weaver, V. M., and Werb, Z. (2011) Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb. Perspect. Biol. 3, a005058
28. Everts, V., Korper, W., Hoeben, K. A., Jansen, I. D., Bromme, D., Cleutjens, K. B., Heeneman, S., Peters, C., Reinheckel, T., Saftig, P., and Beertsen, W. (2006) Osteoclastic bone degradation and the role of different cysteine proteinases and matrix metalloproteinases: differences between calvaria and long bone. J. Bone Miner. Res. 21, 1399-1408
29. Hu, L., Cheng, X. W., Song, H., Inoue, A., Jiang, H., Li, X., Shi, G.-P., Kozawa, E., Okumura, K., and Kuzuya, M. (2014) Cathepsin K activity controls injury-related vascular repair in mice. Hypertension 63, 607-615
30. Cheng, X. W., Huang, Z., Kuzuya, M., Okumura, K., and Murohara, T. (2011) Cysteine protease cathepsins in atherosclerosis-based vascular disease and its complications. Hypertension 58, 978-986
31. Cheng, X. W., Kikuchi, R., Ishii, H., Yoshikawa, D., Hu, L., Takahashi, R., Shibata, R., Ikeda, N., Kuzuya, M., Okumura, K., and Murohara, T. (2013) Circulating cathepsin K as a potential novel biomarker of coronary artery disease. Atherosclerosis 228, 211-216
32. Duong, L. T. (2013) Inhibition of cathepsin K: blocking osteoclast bone resorption and more. IBMS Bonekey. 10.1038/bonekey.2013.130
33. Papazafiropoulou, A., and Tentolouris, N. (2009) Matrix metalloproteinases and cardiovascular diseases. Hippokratia 13, 76-82
34. Malemud, C. J. (2006) Matrix metalloproteinases (MMPs) in health and disease: an overview. Front. Biosci. 11, 1696-1701
35. Linnevers, C. J., McGrath, M. E., Armstrong, R., Mistry, F. R., Barnes, M. G., Klaus, J. L., Palmer, J. T., Katz, B. A., and Brömme, D. (1997) Expression of human cathepsin K in Pichia pastoris and preliminary crystallographic studies of an inhibitor complex. Protein Sci. 6, 919-921
36. Kokubo, T., and Takadama, H. (2006) How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 27, 2907-2915
37. Oyane, A., Kim, H.-M., Furuya, T., Kokubo, T., Miyazaki, T., and Nakamura, T. (2003) Preparation and assessment of revised simulated body fluids. J. Biomed. Mater. Res. A 65, 188-195
38. Monnier, V. M., Kohn, R. R., and Cerami, A. (1984) Accelerated agerelated browning of human collagen in diabetes mellitus. Proc. Natl. Acad. Sci. U.S.A. 81, 583-587
39. Farndale, R. W., Sayers, C. A., and Barrett, A. J. (1982) A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures. Connect. Tissue Res. 9, 247-248
40. Lamour, G., Yip, C. K., Li, H., and Gsponer, J. (2014) High intrinsic mechanical flexibility of mouse prion nanofibrils revealed by measurements of axial and radial Young's moduli. ACS Nano 8, 3851-3861
41. Lamour, G., Kirkegaard, J. B., Li, H., Knowles, T. P., and Gsponer, J. (2014) Easyworm: an open-source software tool to determine the mechanical properties of worm-like chains. Source Code Biol. Med. 9, 16
42. Knowles, T. P., Fitzpatrick, A. W., Meehan, S., Mott, H. R., Vendruscolo, M., Dobson, C. M., and Welland, M. E. (2007) Role of intermolecular forces in defining material properties of protein nanofibrils. Science 318, 1900-1903
43. Valle, F., Favre, M., De Los Rios, P., Rosa, A., and Dietler, G. (2005) Scaling exponents and probability distributions of DNA end-to-end distance. Phys. Rev. Lett. 95, 158105
44. Panwar, P., Du, X., Sharma, V., Lamour, G., Castro, M., Li, H., and Brömme, D. (2013) Effects of cysteine proteases on the structural and mechanical properties of collagen fibers. J. Biol. Chem. 288, 5940-5950
45. Tan, E. P., Ng, S. Y., and Lim, C. T. (2005) Tensile testing of a single ultrafine polymeric fiber. Biomaterials 26, 1453-1456
46. Søe, K., and Delaissé, J.-M. (2010) Glucocorticoids maintain human osteoclasts in the active mode of their resorption cycle. J. Bone Miner. Res. 25, 2184-2192
47. Smith, J. F., Knowles, T. P., Dobson, C. M., Macphee, C. E., and Welland, M. E. (2006) Characterization of the nanoscale properties of individual amyloid fibrils. Proc. Natl. Acad. Sci. U.S.A. 103, 15806-15811
48. Knowles, T. P., Smith, J. F., Craig, A., Dobson, C. M., and Welland, M. E. (2006) Spatial persistence of angular correlations in amyloid fibrils. Phys. Rev. Lett. 96, 238301
49. Schmid, K., McSharry, W. O., Pameijer, C. H., and Binette, J. P. (1980) Chemical and physicochemical studies on the mineral deposits of the human atherosclerotic aorta. Atherosclerosis 37, 199-210
50. Olsson, L. F., Odselius, R., Ribbe, E., and Hegbrant, J. (2001) Evidence of calcium phosphate depositions in stenotic arteriovenous fistulas. Am. J. Kidney Dis. 38, 377-383
51. Bertazzo, S., Gentleman, E., Cloyd, K. L., Chester, A. H., Yacoub, M. H., and Stevens, M. M. (2013) Nano-analytical electron microscopy reveals fundamental insights into human cardiovascular tissue calcification. Nat. Mater. 12, 576-583
52. Huebschmann, A. G., Regensteiner, J. G., Vlassara, H., and Reusch, J. E. (2006) Diabetes and advanced glycoxidation end products. Diabetes Care 29, 1420-1432
53. Demer, L. L., and Tintut, Y. (2008) Vascular calcification: pathobiology of a multifaceted disease. Circulation 117, 2938-2948
54. Stirban, A., Gawlowski, T., and Roden, M. (2014) Vascular effects of advanced glycation end products: Clinical effects and molecular mechanisms. Mol. Metab. 3, 94-108
55. Nudelman, F., Pieterse, K., George, A., Bomans, P. H., Friedrich, H., Brylka, L. J., Hilbers, P. A., de With, G., and Sommerdijk, N. A. (2010) The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat. Mater. 9, 1004-1009
56. Aguda, A. H., Panwar, P., Du, X., Nguyen, N. T., Brayer, G. D., and Brömme, D. (2014) Structural basis of collagen fiber degradation by cathepsin K. Proc. Natl. Acad. Sci. U.S.A. 111, 17474-17479
57. Wheater, G., Elshahaly, M., Tuck, S. P., Datta, H. K., and van Laar, J. M. (2013) The clinical utility of bone marker measurements in osteoporosis. J. Transl. Med. 11, 201
58. Ebenstein, D. M., Coughlin, D., Chapman, J., Li, C., and Pruitt, L. A. (2009) Nanomechanical properties of calcification, fibrous tissue, and hematoma from atherosclerotic plaques. J. Biomed. Mater. Res. A 91, 1028-1037
59. Ferguson, V. L., Bushby, A. J., and Boyde, A. (2003) Nanomechanical properties and mineral concentration in articular calcified cartilage and subchondral bone. J. Anat. 203, 191-202
60. Koester, K. J., Ager, J. W., 3rd, and Ritchie, R. O. (2008) The true toughness of human cortical bone measured with realistically short cracks. Nat. Mater. 7, 672-677
61. Nair, A. K., Gautieri, A., Chang, S.-W., and Buehler, M. J. (2013) Molecular mechanics of mineralized collagen fibrils in bone. Nat. Commun. 4, 1724
62. Thiam, S., Tracy, R. E., Robinson, J. W., and Warner, I. M. (2004) Determination of elements in native and bypass human coronary artery plaque deposits from the same heart using inductively coupled plasma-mass spectrometry. J. Environ. Sci. Health. A Tox. Hazard Subst. Environ. Eng. 39, 1497-1503
63. Goh, K. L., Holmes, D. F., Lu, H.-Y., Richardson, S., Kadler, K. E., Purslow, P. P., and Wess, T. J. (2008) Ageing changes in the tensile properties of tendons: influence of collagen fibril volume fraction. J. Biomech. Eng. 130, 021011
64. Ebrahimi, A. P. (2009) Mechanical properties of normal and diseased cerebrovascular system. J. Vasc. Interv. Neurol. 2, 155-162
65. Reddy, G. K. (2004) AGE-related cross-linking of collagen is associated with aortic wall matrix stiffness in the pathogenesis of drug-induced diabetes in rats. Microvasc. Res. 68, 132-142
66. Haus, J. M., Carrithers, J. A., Trappe, S. W., and Trappe, T. A. (2007) Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle. J. Appl. Physiol. 103, 2068-2076
67. Buehler, M. J. (2008) Nanomechanics of collagen fibrils under varying cross-link densities: atomistic and continuum studies. J. Mech. Behav. Biomed. Mater. 1, 59-67
68. Yanagishita, M. (1993) Function of proteoglycans in the extracellular matrix. Acta Pathol. Jpn. 43, 283-293
69. Li, Y., Liu, Y., Xia, W., Lei, D., Voorhees, J. J., and Fisher, G. J. (2013) Age-dependent alterations of decorin glycosaminoglycans in human skin. Sci. Rep. 3, 2422
70. Ernst, S., Langer, R., Cooney, C. L., and Sasisekharan, R. (1995) Enzymatic degradation of glycosaminoglycans. Crit. Rev. Biochem. Mol. Biol. 30, 387-444
71. Li, Z., Hou, W.-S., Escalante-Torres, C. R., Gelb, B. D., and Bromme, D. (2002) Collagenase activity of cathepsin K depends on complex formation with chondroitin sulfate. J. Biol. Chem. 277, 28669-28676
72. Paiva, K. B., and Granjeiro, J. M. (2014) Bone tissue remodeling and development: focus on matrix metalloproteinase functions. Arch. Biochem. Biophys. 561, 74-87
73. Lutgens, S. P., Cleutjens, K. B., Daemen, M. J., and Heeneman, S. (2007) Cathepsin cysteine proteases in cardiovascular disease. FASEB J. 21, 3029-3041
74. Gineyts, E., Cloos, P. A., Borel, O., Grimaud, L., Delmas, P. D., and Garnero, P. (2000) Racemization and isomerization of type I collagen C-telopeptides in human bone and soft tissues: assessment of tissue turnover. Biochem. J. 345, 481-485
75. Jaffer, F. A., Kim, D.-E., Quinti, L., Tung, C.-H., Aikawa, E., Pande, A. N., Kohler, R. H., Shi, G.-P., Libby, P., and Weissleder, R. (2007) Optical visualization of cathepsin K activity in atherosclerosis with a novel, proteaseactivatable fluorescence sensor. Circulation 115, 2292-2298
76. Crockett, J. C., Rogers, M. J., Coxon, F. P., Hocking, L. J., and Helfrich, M. H. (2011) Bone remodelling at a glance. J. Cell Sci. 124, 991-998