Mechanical strain enhances survivability of collagen micronetworks in the presence of collagenase: implications for load-bearing matrix growth and stability

Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences

Volumn 367, Issue 1902, 2009, Pages 3339-3362

  Bhole, Amit P ^a   Flynn, Brendan P ^a   Liles, Melody ^a   Saeidi, Nima ^a   Dimarzio, Charles A ^b   Ruberti, Jeffrey W ^a  

^a Department of Mechanical and Industrial Engineering ^*  (United States)

^b Northeastern University   (United States)

Author keywords

Collagen; Degradation; Extracellular matrix; Tension

Indexed keywords

ANIMALS; BEARINGS (MACHINE PARTS); BEARINGS (STRUCTURAL); BUILDING MATERIALS; CELL CULTURE; DEGRADATION; ELECTRIC DISCHARGE MACHINING; MOLECULES; TISSUE;

COLLAGEN FIBRILS; COLLAGEN MOLECULES; COLLAGENASE; COLLAGENOUS TISSUES; DIFFERENTIAL INTERFERENCE CONTRAST IMAGING; EXTRACELLULAR MATRICES; EXTRACELLULAR MATRIX; FIBROBLASTIC CELLS; LOAD-BEARING; LOAD-BEARING TISSUES; MATRIX GROWTH; MECHANICAL FORCE; MECHANICAL STRAIN; MICRONETWORKS; STRUCTURAL MATERIALS; TENSION;

COLLAGEN;

COLLAGEN; COLLAGENASE; MULTIPROTEIN COMPLEX;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIOMECHANICS; CATTLE; CHEMISTRY; IN VITRO STUDY; MECHANICAL STRESS; PHASE CONTRAST MICROSCOPY; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; BIOMECHANICS; CATTLE; COLLAGEN; COLLAGENASES; MICROSCOPY, INTERFERENCE; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; STRESS, MECHANICAL;

EID: 69649102613     PISSN: 1364503X     EISSN: None     Source Type: Journal    
DOI: 10.1098/rsta.2009.0093     Document Type: Article

References (65)

1. Altman, G. H., Horan, R. L., Martin, I., Farhadi, J., Stark, P. R., Volloch, V., Richmond, J. C., Vunjak-Novakovic, G. & Kaplan, D. L. 2002 Cell differentiation by mechanical stress. FASEB J. 16, 270-272.
2. Arokoski, J. P., Jurvelin, J. S., Vaatainen, U. & Helminen, H. J. 2000 Normal and pathological adaptations of articular cartilage to joint loading. Scand. J. Med. Sci. Sports 10, 186-198.(doi:10.1034/j,1600838.2000. 010004186.x)
3. Baneyx, G. & Vogel, V. 1999 Self-assembly of fibronectin into fibrillar networks underneath dipalmitoyl phosphatidylcholine monolayers: Role of lipid matrix and tensile forces. Proc. Natl Acad. Sci. USA 96, 12 518-12 523. (doi:10.1073/pnas.96.22.12518) (Pubitemid 29513534)
4. Barocas, V. H. & Tranquillo, R. T. 1997 An anisotropic biphasic theory of tissue-equivalent mechanics: the interplay among cell traction, fibrillar network deformation, fibril alignment, and cell contact guidance. J. Biomech. Eng. 119, 137-145. (doi:10.1115/l.2796072)
5. Barocas, V. H., Moon, A. G. & Tranquillo, R. T. 1995 The fibroblast-populated collagen microsphere assay of cell traction force-part 2: measurement of the cell traction parameter. J. Biomech. Eng. 117, 161-170. (doi:10.1115/1.2795998)
6. Bass, E. C., Wistrom, E. V., Diederich, C. J., Nau, W. H., Pellegrino, R., Ruberti, J. & Lotz, J. C. 2004 Heat-induced changes in porcine annulus fibrosus biomechanics. J. Biomech. 37, 233-240. (doi:10.1016/j.jbiomech.2003.07. 002) (Pubitemid 38050054)
7. Bell, E., Ivarsson, B. & Merrill, C. 1979 Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Natl Acad. Sci. USA 76, 1274-1278. (doi:10.1073/pnas.76.3.1274) (Pubitemid 9143722)
8. Birk, D. E. & Trelstad, R. L. 1984 Extracellular compartments in matrix morphogenesis: collagen fibril, bundle, and lamellar formation by corneal fibroblasts. J. Cell Biol. 99, 2024-2033. (doi:10.1083/jcb.99.6.2024)
9. Birk, D. E., Silver, F. H. & Trelstad, R. L. 1991 Matrix assembly. In Cell biology of extracellular matrix (ed. E. D. Hay), pp. 221-254. New York, NY; London, UK: Plenum Press.
10. Bishop, J. E. & Lindahl, G. 1999 Regulation of cardiovascular collagen synthesis by mechanical load. Cardiovasc. Res. 42, 27-44. (doi:10.1016/S0008-6363(99)00021-8) (Pubitemid 29167067)
11. Blain, E. J., Gilbert, S. J., Wardale, R. J., Capper, S. J., Mason, D. J. & Duance, V. C. 2001 Up-regulation of matrix metalloproteinase expression and activation following cyclical compressive loading of articular cartilage in vitro. Arch. Biochem. Biophys. 396, 49-55. (doi:10.1006/abbi.2001.2575)
12. Bohren, C. F. & Huffman, D. R. 1983 Absorption and scattering of light by small particles. New York, NY: Wiley.
13. Buckwalter, J. A., Saltzman, C. & Brown, T. 2004 The impact of osteoarthritis: implications for research. Clin. Orthop. Relat. Res. 427, S6-S15.
14. Burke, K. E., Naughton, G., Waldo, E. & Cassai, N. 1983 Bovine collagen implant: histologic chronology in pig dermis. J. Dermatol. Surg. Oncol. 9, 889-895. (Pubitemid 14232748)
15. Burke, K. E., Naughton, G. & Cassai, N. 1985 A histological, immunological, and electron microscopic study of bovine collagen implants in the human. Ann. Plast. Surg. 14, 515-522. (doi:10.1097/00000637-198506000-00004) (Pubitemid 15071821)
16. Canty, E. G. & Kadler, K. E. 2005 Procollagen trafficking, processing and fibrillogenesis. J. Cell Sci. 118, 1341-1353. (doi:10.1242/jcs.01731)
17. Carter, D. & Beaupre, G. 2001 Skeletal form and function: mechanobiology of skeletal development, aging and regeneration. Cambridge, UK: Press Syndicate of the University of Cambridge.
18. Carter, D. R. & Orr, T. E. 1992 Skeletal development and bone functional adaptation. J. Bone Miner. Res. 7(Suppl. 2), S389-S395.
19. Chalmers, J. & Ray, R. 1962 The growth of transplanted foetal bones in different immunological environments. J. Bone Joint Surg. 44B, 149-164.
20. Cintron, C., Covington, H. & Kublin, C. L. 1983 Morphogenesis of rabbit corneal stroma. Invest. Ophthalmol. Vis. Sci. 24, 543-556.
21. Donald, P. J. 1986 Collagen grafts-here today and gone tomorrow. Otolaryngol. Head Neck Surg. 95, 607-614.
22. Duty, A. O., Oest, M. E. & Guldberg, R. E. 2007 Cyclic mechanical compression increases mineralization of cell-seeded polymer scaffolds in vivo. J. Biomech. Eng. 129, 531-539. (doi:10.1115/1.2746375)
23. Expósito, J., Cluzel, C., Lethias, C. & Garrone, R. 2000 Tracing the evolution of vertebrate fibrillar collagens from an ancestral alpha chain. Matrix Biol. 19, 275-279. (doi:10.1016/S0945053X(00)00067-6) (Pubitemid 30601760)
24. Exposito, J. Y., Cluzel, C., Garrone, R. & Lethias, C. 2002 Evolution of collagens. Anat. Rec. 268, 302-316. (doi:10.1002/ar.l.0162)
25. Gelles, J., Schnapp, B. J. & Sheetz, M. P. 1988 Tracking kinesin-driven movements with nanometrescale precision. Nature 331, 450-453. (doi:10.1038/331450a0) (Pubitemid 18064370)
26. Giraud-Guille, M. M. 1996 Twisted liquid crystalline supramolecular arrangements in morphogenesis. Int. Rev. Cytol. 166, 59-101. (doi:10.1016/S0074-7696(08)62506-l)
27. Giraud-Guille, M. M., Besseau, L. & Martin, R. 2003 Liquid crystalline assemblies of collagen in bone and in vitro systems. J. Biomech. 36, 1571-1579. (doi:10.1016/S0021-9290(03)00134-9) (Pubitemid 37117362)
28. Hay, E. D. & Revel, J. P. 1969 Fine structure of the developing avian cornea. Monogr. Dev. Biol. 1, 1-144.
29. He, Y., Macarak, E. J., Korostoff, J. M. & Howard, P. S. 2004 Compression and tension: differential effects on matrix accumulation by periodontal ligament fibroblasts in vitro. Connect. Tissue Res. 45, 28-39. (doi:10.1080/03008200490278124) (Pubitemid 38489341)
30. Huang, C. & Yannas, I. V. 1977 Mechanochemical studies of enzymatic degradation of insoluble collagen fibers. J. Biomed. Mater. Res. 11, 137-154. (doi:10.1002/jbm.820110113) (Pubitemid 8059844)
31. Isenberg, B. C. & Tranquillo, R. T. 2003 Long-term cyclic distention enhances the mechanical properties of collagen-based media-equivalents. Ann. Biomed. Eng. 31, 937-949. (doi:10.1114/1.1590662)
32. Jeffrey, J. J. 1998 Interstitial collagenases. In Matrix metalloproteases, pp. 15-42. San Diego, CA: Academic Press.
33. Jester, J. V., Petroll, W. M. & Cavanagh, H. D. 1999 Corneal stromal wound healing in refractive surgery: the role of myofibroblasts. Prog. Retin. Eye Res. 18, 311-356. (doi:10.1016/S13509462(98)00021-4)
34. Juncosa-Melvin, N., Shearn, J. T., Boivin, G. P., Gooch, C., Galloway, M. T., West, J. R., Nirmalanandhan, V. S., Bradica, G. & Butler, D. L. 2006 Effects of mechanical stimulation on the biomechanics and histology of stem cell-collagen sponge constructs for rabbit patellar tendon repair. Tissue Eng. 12, 2291-2300. (doi:10.1089/ten.2006.12.2291) (Pubitemid 44734987)
35. Koskinen, S. O., Heinemeier, K. M., Olesen, J. L., Langberg, H. & Kjaer, M. 2004 Physical exercise can influence local levels of matrix metalloproteinases and their inhibitors in tendon-related connective tissue. J. Appl. Physiol. 96, 861-864. (doi:10.1152/japplphysiol.00489.2003) (Pubitemid 38248655)
36. Krishnan, L., Weiss, J. A., Wessman, M. D. & Hoying, J. B. 2004 Design and application of a test system for viscoelastic characterization of collagen gels. Tissue Eng. 10, 241-252. (doi: 10.1089/107632704322791880) (Pubitemid 38199379)
37. Langille, R. M. & Hall, B. K. 1989 Developmental processes, developmental sequences and early vertebrate phylogeny. Biol. Rev. Camb. Philos. Soc. 64, 73-91. (doi:10.1Hl/j.l469185X.1989.tb00672.x)
38. Leikina, E., Mertts, M. V., Kuznetsova, N. & Leikin, S. 2002 Type I collagen is thermally unstable at body temperature. Proc. Natl Acad. Sci. USA 99, 1314-1318. (doi:10.1073/pnas.032307099) (Pubitemid 34136490)
39. Lotz, J. C., Hadi, T., Bratton, C., Reiser, K. M. & Hsieh, A. H. 2008 Anulus fibrosus tension inhibits degenerative structural changes in lamellar collagen. Eur. Spine J. 17, 1149-1159. (doi:10.1007/s00586-008-0721-y)
40. Lyons, G., Eisenstein, S. M. Sweet, M. B. 1981 Biochemical changes in intervertebral disc degeneration. Biochim. Biophys. Acta 673, 443-453. (Pubitemid 11103744)
41. Majima, T., Marchuk, L. L., Sciore, P., Shrive, N. G., Frank, C. B. & Hart, D. A. 2000a Compressive compared with tensile loading of medial collateral ligament scar in vitro uniquely influences mRNA levels for aggrecan, collagen type ii, and collagenase. J. Orthop. Res. 18, 524-531. (doi:10.1002/jor.H00180403) (Pubitemid 30786584)
42. Majima, T., Marchuk, L. L., Shrive, N. G., Frank, C. B. & Hart, D. A. 2000b In-vitro cyclic tensile loading of an immobilized and mobilized ligament autograft selectively inhibits mrna levels for collagenase (MMP-I). J. Orthop. Sci. 5, 503-510. (doi:10.1007/s007760070030) (Pubitemid 30797424)
43. Maroudas, A. 1972 Physical chemistry and the structure of cartilage. J. Physiol. 223, 21-22.
44. Miles, C. A. & Ghelashvili, M. 1999 Polymer-in-a-box mechanism for the thermal stabilization of collagen molecules in fibers. Biophys. J. 76, 3243-3252. (doi:10.1016/S0006-3495(99)77476-X) (Pubitemid 29269471)
45. Moses, M. A., Marikovsky, M., Harper, J. W., Vogt, P., Eriksson, E., Klagsbrun, M. & Langer, R. 1996 Temporal study of the activity of matrix metalloproteinases and their endogenous inhibitors during wound healing. J. Cell Biochem. 60, 379-386. (doi:10.1002/ (SICI)1097-4644(19960301)60:3<379::AID- JCB9>3.0.CO;2-T) (Pubitemid 26090505)
46. Nabeshima, Y., Grood, E. S., Sakurai, A. & Herman, J. H. 1996 Uniaxial tension inhibits tendon collagen degradation by collagenase in vitro. J. Orthop. Res. 14, 123-130. (doi: 10.1002/jor.1100140120) (Pubitemid 26091612)
47. Neath, P., Roche, S. M. & Bee, J. A. 1991 Intraocular pressure-dependent and -independent phases of growth of the embryonic chick eye and cornea. Invest. Ophthalmol. Vis. Sci. 32, 2483-2491.
48. Ozerdem, B. & Tozeren, A. 1995 Physical response of collagen gels to tensile strain. J. Biomech. Eng. 117, 397-401. (doi: 10.1115/1.2794198)
49. Parsons, M., Kessler, E., Laurent, G. J., Brown, R. A. & Bishop, J. E. 1999 Mechanical load enhances procollagen processing in dermal fibroblasts by regulating levels of procollagen c-proteinase. Exp. Cell Res. 252, 319-331. (doi:10.1006/excr.1999.4618) (Pubitemid 29530262)
50. Petroll, W. M. & Ma, L. 2003 Direct, dynamic assessment of cell-matrix interactions inside fibrillar collagen lattices. Cell Motil. Cytoskeleton 55, 254-264. (doi:10.1002/cm.l0126) (Pubitemid 36897530)
51. Prajapati, R. T., Chavally-Mis, B., Herbage, D., Eastwood, M. & Brown, R. A. 2000 Mechanical loading regulates protease production by fibroblasts in three-dimensional collagen substrates. Wound Repair Regen. 8, 226-237. (doi:10.1046/j.l524-475x.2000.00226.x) (Pubitemid 30421525)
52. Riley, G. P., Curry, V., DeGroot, J., van El, B., Verzijl, N., Hazleman, B. L. & Bank, R. A. 2002 Matrix metalloproteinase activities and their relationship with collagen remodelling in tendon pathology. Matrix Biol. 21, 185-195. (doi:10.1016/S0945-053X(01)00196-2) (Pubitemid 34145243)
53. Robbins, J. R., Evanko, S. P. & Vogel, K. G. 1997 Mechanical loading and TGF-beta regulate proteoglycan synthesis in tendon. Arch. Biochem. Biophys. 342, 203-211. (doi:10.1006/abbi.l997.0102)
54. Ruberti, J. W. & Hallab, N. J. 2005 Strain-controlled enzymatic cleavage of collagen in loaded matrix. Biochem. Biophys. Res. Commun. 336, 483-489. (doi:10.1016/j.bbrc.2005.08.128)
55. Ruberti, J. W. & Zieske, J. D. 2008 Prelude to corneal tissue engineering-gaining control of collagen organization. Prog. Retin. Eye Res. 27, 549-577. (doi:10.1016/j.preteyeres.2008.08.001)
56. Schnapp, B.J., Gelles, J. & Sheetz, M.P. 1988 Nanometer-scale measurements using video light microscopy. Cell Motil. Cytoskeleton 10, 47-53. (doi:10.1002/cm.970100'109) (Pubitemid 18193306)
57. Sutter, N.B. et al. 2007 A single IGF1 allele is a major determinant of small size in dogs. Science 316, 112-115. (doi:10.1126/science.1137045)
58. Tiktopulo, E. I. & Kajava, A. V. 1998 Denaturation of type I collagen fibrils is an endothermic process accompanied by a noticeable change in the partial heat capacity. Biochemistry 37, 8147-8152. (doi:10.1021/bi980360n)
59. Trelstad, R. L. 1982 The bilaterally asymmetrical architecture of the submammalian corneal stroma resembles a cholesteric liquid crystal. Dev. Biol. 92, 133-134. (doi:10.1016/00121606(82)90157-9)
60. Tzafriri, A. R., Bercovier, M. Parnas, H. 2002 Reaction diffusion model of the enzymatic erosion of insoluble fibrillar matrices. Biophys. J. 83, 776-793. (doi:10.1016/S0006-3495(02)75208-9) (Pubitemid 34803616)
61. Urban, J. P. & Roberts, S. 2003 Degeneration of the intervertebral disc. Arthritis Res. Ther. 5, 120-130. (doi:10.1186/ar629)
62. Vailas, A. C., Zernicke, R. F., Grindeland, R. E. & Li, K. C. 1990 Suspension effects on rat femur-medial collateral ligament-tibia unit. Am. J. Physiol. 258, R724-R728.
63. Wolff, J. 1891 Das gesetz der transformation der knochen. Berlin, Germany: A. Hirschwald.
64. Zerath, E. 1998 Effects of microgravity on bone and calcium homeostasis. Adv. Space Res. 21, 1049-1058. (doi:10.1016/S0273-1177(98)00026-X) (Pubitemid 128369729)
65. Zhong, C., Chrzanowska-Wodnicka, M., Brown, J., Shaub, A., Belkin, A. M. & Burridge, K. 1998 Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J. Cell Biol. 141, 539-551. (doi:10.1083/jcb.l41.2.539) (Pubitemid 28237100)