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Cited by 87Collagen: Extraction and CharacterizationCellular Mechanics and InteractionsConnective tissue disorders research

Mechanochemistry of collagen

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Siadat, Seyed Mohammad, Ruberti, Jeffrey W.·2023·Acta Biomaterialia
DOI 10.1016/j.actbio.2023.01.025PMC PMC13270376
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Abstract

The collagen molecular family is the result of nearly one billion years of evolution. It is a unique family of proteins, the majority of which provide general mechanical support to biological tissues. Fibril forming collagens are the most abundant collagens in vertebrate animals and are generally found in positions that resist tensile loading. In animals, cells produce fibril-forming collagen molecules that self-assemble into larger structures known as collagen fibrils. Collagen fibrils are the fundamental, continuous, load-bearing elements in connective tissues, but are often further aggregated into larger load-bearing structures, fascicles in tendon, lamellae in cornea and in intervertebral disk. We know that failure to form fibrillar collagen is embryonic lethal, and excessive collagen formation/growth (fibrosis) or uncontrolled enzymatic remodeling (type II collagen: osteoarthritis) is pathological. Collagen is thus critical to vertebrate viability and instrumental in maintaining efficient mechanical structures. However, despite decades of research, our understanding of collagen matrix formation is not complete, and we know still less about the detailed mechanisms that drive collagen remodeling, growth, and pathology. In this perspective, we examine the known role of mechanical force on the formation and development of collagenous structure. We then discuss a mechanochemical mechanism that has the potential to unify our understanding of collagenous tissue assembly dynamics, which preferentially deposits and grows collagen fibrils directly in the path of mechanical force, where the energetics should be dissuasive and where collagen fibrils are most required. We term this mechanism: Mechanochemical force-structure causality. STATEMENT OF SIGNIFICANCE: Our mechanochemical-force structure causality postulate suggests that collagen molecules are components of mechanochemically-sensitive and dynamically-responsive fibrils. Collagen molecules assemble preferentially in the path of applied strain, can be grown in place by mechanical extension, and are retained in the path of force through strain-stabilization. The mechanisms that drive this behavior operate at the level of the molecules themselves and are encoded into the structure of the biomaterial. The concept might change our understanding of structure formation, enhance our ability to treat injuries, and accelerate the development of therapeutics to prevent pathologies such as fibrosis. We suggest that collagen is a mechanochemically responsive dynamic element designed to provide a substantial "material assist" in the construction of adaptive carriers of mechanical signals.

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  1. [1]Gross J, Highberger JH, Schmitt FO, Some factors involved in the fibrogenesis of collagen in vitro, Proc. Soc. Exp. Biol. Med 80 (3) (1952) 462– 465. 14949085
  2. [2]Highberger JH, Gross J, Schmitt FO, The interaction of mucoprotein with soluble collagen; an electron microscope study, Proc. Natl. Acad. Sci. U. S. A 37 (5) (1951) 286– 291. 14834152 PMC1063355
  3. [3]Gross J, Lapiere CM, Collagenolytic activity in amphibian tissues: a tissue culture assay, Proc. Natl. Acad. Sci. U. S. A 48 (1962) 1014– 1022. 13902219 PMC220898
  4. [4]Gross J, Nagai Y, Specific degradation of the collagen molecule by tadpole collagenolytic enzyme, Proc. Natl. Acad. Sci. U. S. A 54 (4) (1965) 1197– 1204. 4286832 PMC219836
  5. [5]Weiner S, Traub W, Bone structure: from angstroms to microns, FASEB J. 6 (3) (1992) 879– 885. 1740237
  6. [6]Benjamin M, Qin S, Ralphs JR, Fibrocartilage associated with human tendons and their pulleys, J. Anat 187 (Pt 3) (1995) 625– 633. 8586561 PMC1167465
  7. [7]Basser PJ, Schneiderman R, Bank RA, Wachtel E, Maroudas A, Mechanical properties of the collagen network in human articular cartilage as measured by osmotic stress technique, Arch. Biochem. Biophys 351 (2) (1998) 207– 219. 9515057
  8. [8]Maroudas A, Bannon C, Measurement of swelling pressure in cartilage and comparison with the osmotic pressure of constituent proteoglycans, Biorheology 18 (3–6) (1981) 619– 632. 6799013
  9. [9]Clark JM, The organisation of collagen fibrils in the superficial zones of articular cartilage, J. Anat 171 (1990) 117– 130. 2081698 PMC1257132
  10. [10]Pearson OM, Lieberman DE, The aging of Wolff’s ?law?: Ontogeny and responses to mechanical loading in cortical bone, Am. J. Phys. Anthropol 125 (S39) (2004) 63– 99. 15605390
  11. [11]Frost HM, Wolff’s law and bone’s structural adaptations to mechanical usage: an overview for clinicians, Angle Orthod. 64 (3) (1994) 175– 188. 8060014
  12. [12]Frost HM, New targets for fascial, ligament and tendon research: a perspective from the Utah paradigm of skeletal physiology, J. Musculoskelet. Neuronal Interact 3 (3) (2003) 201– 209. 15758342
  13. [13]Subramanian A, Kanzaki LF, Galloway JL, Schilling TF, Mechanical force regulates tendon extracellular matrix organization and tenocyte morphogenesis through TGFbeta signaling, eLife 7 (2018). PMC6345564 30475205
  14. [14]Zeng D, Ferrari A, Ulmer J, Veligodskiy A, Fischer P, Spatz J, Ventikos Y, Poulikakos D, Kroschewski R, Three-dimensional modeling of mechanical forces in the extracellular matrix during epithelial lumen formation, Biophys. J 90 (12) (2006) 4380– 4391. 16565042 PMC1471864
  15. [15]Malandrino A, Trepat X, Kamm RD, Mak M, Dynamic filopodial forces induce accumulation, damage, and plastic remodeling of 3D extracellular matrices, PLoS Comput. Biol 15 (4) (2019) e1006684. 30958816 PMC6472805
  16. [17]Abhilash AS, Trappmann Brendon B, Vivek Christopher, Remodeling of Fibrous Extracellular Matrices by Contractile Cells: Predictions from Discrete Fiber Network Simulations, Biophys. J 107 (8) (2014) 1829– 1840. 25418164 PMC4213674
  17. [18]Topol H, Demirkoparan H, Pence TJ, On collagen fiber morphoelasticity and homeostatic remodeling tone, J. Mech. Behav. Biomed. Mater 113 (2021) 104154. 33158790
  18. [20]Musiime M, Chang J, Hansen U, Kadler KE, Zeltz C, Gullberg D, Collagen assembly at the cell surface: dogmas revisited 10 (3) (2021) 662. PMC8002325 33809734
  19. [21]Kalson NS, Lu Y, Taylor SH, Starborg T, Holmes DF, Kadler KE, A structure-based extracellular matrix expansion mechanism of fibrous tissue growth, Elife 4 (2015). PMC4438642 25992598
  20. [22]Koudouna E, Mikula E, Brown DJ, Young RD, Quantock AJ, Jester JV, Cell regulation of collagen fibril macrostructure during corneal morphogenesis, Acta Biomater. 79 (2018) 96– 112. 30170195 PMC6163070
  21. [23]Young RD, Knupp C, Koudouna E, Ralphs JR, Ma Y, Lwigale PY, Jester JV, Quantock AJ, Cell-independent matrix configuration in early corneal development, Exp. Eye Res 187 (2019) 107772. 31445001 PMC6892249
  22. [24]Trelstad RL, The bilaterally asymmetrical architecture of the submammalian corneal stroma resembles a cholesteric liquid crystal, Dev. Biol 92 (1) (1982) 133– 134. 7106374
  23. [25]Giraud-Guille MM, Twisted plywood architecture of collagen fibrils in human compact bone osteons, Calcif. Tissue Int 42 (3) (1988) 167– 180. 3130165
  24. [26]Giraud-Guille MM, Liquid crystalline phases of sonicated type I collagen, Biol. Cell 67 (1) (1989) 97– 101. 2605377
  25. [27]Giraud-Guille MM, Liquid crystallinity in condensed type I collagen solutions. A clue to the packing of collagen in extracellular matrices, J. Mol. Biol 224 (3) (1992) 861– 873. 1569562
  26. [28]Giraud-Guille MM, Twisted liquid crystalline supramolecular arrangements in morphogenesis, Int. Rev. Cytol 166 (1996) 59– 101. 8881773
  27. [29]Giraud-Guille MM, Besseau L, Banded patterns in liquid crystalline phases of type I collagen: relationship with crimp morphology in connective tissue architecture, Connect. Tissue Res 37 (3–4) (1998) 183– 193. 9862220
  28. [30]Giraud-Guille MM, Besseau L, Martin R, Liquid crystalline assemblies of collagen in bone and in vitro systems, J. Biomech 36 (10) (2003) 1571– 1579. 14499304
  29. [31]Gobeaux F, Belamie E, Mosser G, Davidson P, Panine P, Giraud-Guille MM, Cooperative ordering of collagen triple helices in the dense state, Langmuir ACS J. Surf. Colloids 23 (11) (2007) 6411– 6417. 17441743
  30. [32]Gobeaux F, Mosser G, Anglo A, Panine P, Davidson P, Giraud-Guille MM, Belamie D, Fibrillogenesis in dense collagen solutions: a physicochemical study, J. Mol. Biol 376 (5) (2008) 1509– 1522. 18234220
  31. [33]Saeidi N, Karmelek KP, Paten JA, Zareian R, DiMasi E, Ruberti JW, Molecular crowding of collagen: a pathway to produce highly-organized collagenous structures, Biomaterials 33 (30) (2012) 7366– 7374. 22846420 PMC3757096
  32. [34]Exposito J-Y, Cluzel C, Garrone R, Lethias C, Evolution of collagens, Anat. Rec 268 (3) (2002) 302– 316. 12382326
  33. [35]Bhole AP, Flynn BP, Liles M, Saeidi N, Dimarzio CA, Ruberti JW, Mechanical strain enhances survivability of collagen micronetworks in the presence of collagenase: implications for load-bearing matrix growth and stability, Philos. Trans. A Math. Phys. Eng Sci 367 (1902) (2009) 3339– 3362. 19657003 PMC2865878
  34. [36]Camp RJ, Liles M, Beale J, Saeidi N, Flynn BP, Moore E, Murthy SK, Ruberti JW, Molecular mechanochemistry: low force switch slows enzymatic cleavage of human type I collagen monomer, J. Am. Chem. Soc 133 (11) (2011) 4073– 4078. 21348512 PMC3299535
  35. [37]Flynn BP, Bhole AP, Saeidi N, Liles M, Dimarzio CA, Ruberti JW, Mechanical strain stabilizes reconstituted collagen fibrils against enzymatic degradation by mammalian collagenase matrix metalloproteinase 8 (MMP-8), PLoS One 5 (8) (2010) e12337. 20808784 PMC2925882
  36. [38]Flynn BP, Tilburey GE, Ruberti JW, Highly sensitive single-fibril erosion assay demonstrates mechanochemical switch in native collagen fibrils, Biomech. Model. Mechanobiol 12 (2) (2013) 291– 300. 22584606 PMC3773243
  37. [39]Huang C, Yannas IV, Mechanochemical studies of enzymatic degradation of insoluble collagen fibers, J. Biomed. Mater. Res 11 (1) (1977) 137– 154. 14968
  38. [40]Nabeshima Y, Grood ES, Sakurai A, Herman JH, Uniaxial tension inhibits tendon collagen degradation by collagenase in vitro, J. Orthop. Res 14 (1) (1996) 123– 130. 8618154
  39. [41]Ruberti JW, Hallab NJ, Strain-controlled enzymatic cleavage of collagen in loaded matrix, Biochem. Biophys. Res. Commun 336 (2) (2005) 483– 489. 16140272
  40. [42]Wyatt KEK, Bourne JW, Torzilli PA, Deformation-dependent enzyme mechanokinetic cleavage of type I collagen, J. Biomech. Eng 131 (5) (2009) 051004. 19388774 PMC2766525
  41. [43]Zareian R, Church KP, Saeidi N, Flynn BP, Beale JW, Ruberti JW, Probing collagen/enzyme mechanochemistry in native tissue with dynamic, enzyme-induced creep, Langmuir ACS J. Surf. Colloids 26 (12) (2010) 9917– 9926. PMC3712121 20429513
  42. [47]Baitsell GA, The origin and structure of a fibrous tissue which appears in living cultures of adult frog tissues, J. Exp. Med 21 (5) (1915) 455– 478. 19867883 PMC2125327
  43. [49]Wolbach SB, Controlled formation of collagen and reticulum. A study of the source of intercellular substance in recovery from experimental scorbutus, Am. J. Pathol 9 (Suppl) (1933) 689– 700 5. 19970104 PMC2062765
  44. [52]Kalson NS, Starborg T, Lu Y, Mironov A, Humphries SM, Holmes DF, Kadler KE, Nonmuscle myosin II powered transport of newly formed collagen fibrils at the plasma membrane, Proc. Natl. Acad. Sci. U. S. A 110 (49) (2013) E4743– E4752. 24248360 PMC3856828
  45. [54]Paten JA, Siadat SM, Susilo ME, Ismail EN, Stoner JL, Rothstein JP, Ruberti JW, Flow-induced crystallization of collagen: a potentially critical mechanism in early tissue formation, ACS Nano 10 (5) (2016) 5027– 5040. 27070851 PMC6037489
  46. [56]Porter KR, Vanamee P, Observations on the formation of connective tissue fibers, Proc. Soc. Exp. Biol. Med 71 (4) (1949) 513– 516. 18139799
  47. [57]Godman GC, Porter KR, Chondrogenesis, studied with the electron microscope, J. Biophys. Biochem. Cytol 8 (1960) 719– 760. 13706207 PMC2224963
  48. [58]Chapman JA, Morphological and chemical studies of collagen formation. I. The fine structure of guinea pig granulomata, J. Biophys. Biochem. Cytol 9 (1961) 639– 651. 13692398 PMC2225033
  49. [59]Ross R, Benditt EP, Wound healing and collagen formation. I. Sequential changes in components of guinea pig skin wounds observed in the electron microscope, J. Biophys. Biochem. Cytol 11 (1961) 677– 700. 14494202 PMC2225131
  50. [60]Revel JP, Hay ED, An autoradiographic and electron microscopic study of collagen synthesis in differentiating cartilage, Z. Zellforsch. Mikrosk. Anat 61 (1963) 110– 144. 14095095
  51. [61]Porter KR, Cell fine structure and biosynthesis of intercellular macro-molecules, Biophys. J 4 (1964) SUPPL167– 201. 14104076 PMC1367623
  52. [62]Marchi F, Leblond CP, Collagen biogenesis and assembly into fibrils as shown by ultrastructural and 3H-proline radioautographic studies on the fibroblasts of the rat food pad, Am. J. Anat 168 (2) (1983) 167– 197. 6650434
  53. [63]Marchi F, Leblond CP, Radioautographic characterization of successive compartments along the rough endoplasmic reticulum-Golgi pathway of collagen precursors in foot pad fibroblasts of [3H]proline-injected rats, J. Cell Biol 98 (5) (1984) 1705– 1709. 6725395 PMC2113191
  54. [64]Revell CK, Jensen OE, Shearer T, Lu Y, Holmes DF, Kadler KE, Collagen fibril assembly: New approaches to unanswered questions, Matrix Biology Plus 12 (2021) 100079. 34381990 PMC8334717
  55. [65]Wassermann F, Fibrillogenesis in the regenerating rat tendon with special reference to growth and composition of the collagenous fibril, Am. J. Anat 94 (3) (1954) 399– 437. 13171341
  56. [66]Goldberg B, Green H, An analysis of collagen secretion by established mouse fibroblast lines, J. Cell Biol 22 (1964) 227– 258. 14195613 PMC2106491
  57. [67]Kadler KE, Holmes DF, Trotter JA, Chapman JA, Collagen fibril formation, Biochem. J 316 (Pt 1) (1996) 1– 11. 8645190 PMC1217307
  58. [68]Welsh RA, Intracytoplasmic collagen formations in desmoid fibromatosis, Am. J. Pathol 49 (3) (1966) 515– 535. 5920328 PMC1916474
  59. [69]Dyer RF, Peppler RD, Intracellular collagen in the nonpregnant and IUD-containing rat uterus, Anat. Rec 187 (2) (1977) 241– 247. 557912
  60. [70]Gotjamanos T, Intracellular collagen in recurrent ameloblastic fibroma, J. Oral Pathol 8 (5) (1979) 277– 283. 119840
  61. [71]Michna H, Intracellular collagen fibrils: evidence of an intracellular source from experiments with tendon fibroblasts and fibroblastic tumour cells, J. Anat 158 (1988) 1– 12. 3225213 PMC1261972
  62. [72]Trelstad RL, Hayashi K, Tendon collagen fibrillogenesis: intracellular sub-assemblies and cell surface changes associated with fibril growth, Dev. Biol 71 (2) (1979) 228– 242. 499658
  63. [73]Birk DE, Trelstad RL, Extracellular compartments in matrix morphogenesis: collagen fibril, bundle, and lamellar formation by corneal fibroblasts, J. Cell Biol 99 (6) (1984) 2024– 2033. 6542105 PMC2113579
  64. [74]Birk DE, Trelstad RL, Extracellular compartments in tendon morphogenesis: collagen fibril, bundle, and macroaggregate formation, J. Cell Biol 103 (1) (1986) 231– 240. 3722266 PMC2113791
  65. [75]Yang GC, Birk DE, Topographies of extracytoplasmic compartments in developing chick tendon fibroblasts, J. Ultrastruct. Mol. Struct. Res 97 (1–3) (1986) 238– 248. 3453371
  66. [76]Canty EG, Lu Y, Meadows RS, Shaw MK, Holmes DF, Kadler KE, Coalignment of plasma membrane channels and protrusions (fibripositors) specifies the parallelism of tendon, J. Cell Biol 165 (4) (2004) 553– 563. 15159420 PMC2172348
  67. [77]Lu Y, Kamel-El Sayed SA, Wang K, Tiede-Lewis LM, Grillo MA, Veno PA, Dusevich V, Phillips CL, Bonewald LF, Dallas SL, Live imaging of type I collagen assembly dynamics in osteoblasts stably expressing GFP and mCherry-tagged collagen constructs, J. Bone Miner. Res 33 (6) (2018) 1166– 1182. 29461659 PMC6425932
  68. [78]Fessler JH, Fessler LI, Biosynthesis of procollagen, Annu. Rev. Biochem 47 (1978) 129– 162. 354493
  69. [79]Prockop DJ, Kivirikko KI, Tuderman L, Guzman NA, The biosynthesis of collagen and its disorders (first of two parts), N. Engl. J. Med 301 (1) (1979) 13– 23. 449904
  70. [80]Prockop DJ, Kivirikko KI, Tuderman L, Guzman NA, The biosynthesis of collagen and its disorders (second of two parts), N. Engl. J. Med 301 (2) (1979) 77– 85. 36559
  71. [81]N’Diaye E-N, Cook R, Wang H, Wu P, LaCanna R, Wu C, Ye Z, Seshasayee D, Hazen M, Lin W, Extracellular BMP1 is the major proteinase for COOH-terminal proteolysis of type I procollagen in lung fibroblasts, Am. J. Physiol. Cell Physiol 320 (2) (2021) C162– C174. 33206546
  72. [82]Li S, Van Den Diepstraten C, D’Souza SJ, Chan BM, Pickering JG, Vascular smooth muscle cells orchestrate the assembly of type I collagen via alpha2beta1 integrin, RhoA, and fibronectin polymerization, Am. J. Pathol 163 (3) (2003) 1045– 1056. 12937145 PMC1868248
  73. [83]Sottile J, Hocking DC, Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions, Mol. Biol. Cell 13 (10) (2002) 3546– 3559. 12388756 PMC129965
  74. [84]McDonald JA, Kelley DG, Broekelmann TJ, Role of fibronectin in collagen deposition: Fab’ to the gelatin-binding domain of fibronectin inhibits both fibronectin and collagen organization in fibroblast extracellular matrix, J. Cell Biol 92 (2) (1982) 485– 492. 7061591 PMC2112086
  75. [86]Barczyk M, Carracedo S, Gullberg D, Integrins, Cell Tissue Res. 339 (1) (2010) 269– 280. 19693543 PMC2784866
  76. [87]Gullberg D, Turner DC, Borg TK, Terracio L, Rubin K, Different beta 1-integrin collagen receptors on rat hepatocytes and cardiac fibroblasts, Exp. Cell. Res 190 (2) (1990) 254– 264. 2170154
  77. [88]Johnson C, Galis ZS, Quantitative assessment of collagen assembly by live cells, J. Biomed. Mater. Res. A 67 (3) (2003) 775– 784. 14613225
  78. [89]Harris AK, Stopak D, Wild P, Fibroblast traction as a mechanism for collagen morphogenesis, Nature 290 (5803) (1981) 249– 251. 7207616
  79. [90]Stopak D, Harris AK, Connective tissue morphogenesis by fibroblast traction. I. Tissue culture observations, Dev. Biol 90 (2) (1982) 383– 398. 7075867
  80. [91]Schnieke A, Harbers K, Jaenisch R, Embryonic lethal mutation in mice induced by retrovirus insertion into the α1(I) collagen gene, Nature 304 (5924) (1983) 315– 320. 6308457
  81. [92]Zeltz C, Orgel J, Gullberg D, Molecular composition and function of integrin-based collagen glues—introducing COLINBRIs, Biochimica et Biophysica Acta (BBA)-General Subjects 1840 (8) (2014) 2533– 2548. 24361615
  82. [93]Siadat SM, Zamboulis DE, Thorpe CT, Ruberti JW, Connizzo BK, Tendon Extracellular Matrix Assembly, Maintenance and Dysregulation Throughout Life, Adv. Exp. Med. Biol 1348 (2021) 45– 103. 34807415
  83. [94]Porter KR, Pappas GD, Collagen formation by fibroblasts of the chick embryo dermis, J. Biophys. Biochem. Cytol 5 (1) (1959) 153– 166. 13630947 PMC2224637
  84. [95]Jackson SF, Smith RH, Studies on the biosynthesis of collagen. I. The growth of fowl osteoblasts and the formation of collagen in tissue culture, J. Biophys. Biochem. Cytol 3 (6) (1957) 897– 912. 13481024 PMC2224126
  85. [96]Ross R, Benditt EP, Wound healing and collagen formation. III. A quantitative radioautographic study of the utilization of proline-H3 in wounds from normal and scorbutic guinea pigs, J. Cell Biol 15 (1962) 99– 108. 13975120 PMC2106131
  86. [97]Young RD, Knupp C, Pinali C, Png KM, Ralphs JR, Bushby AJ, Starborg T, Kadler KE, Quantock AJ, Three-dimensional aspects of matrix assembly by cells in the developing cornea, Proc. Natl. Acad. Sci. U. S. A 111 (2) (2014) 687– 692. 24385584 PMC3896168
  87. [98]Bradbury S, Meek G, The fine structure of the adipose cell of the leech Glossiphonia complanata, J. Cell Biol 4 (5) (1958) 603– 608. PMC2224550 13587556
  88. [100]Hill TL, Linear Aggregation Theory, Springer-Verlag, New York, 1987.
  89. [101]Shemesh T, Bershadsky AD, Kozlov MM, Force-driven polymerization in cells: actin filaments and focal adhesions, J. Phys. Condens. Matter 17 (47) (2005) S3913– S3928. 21690732
  90. [102]Brown RA, Blunn GW, Ejim OS, Preparation of orientated fibrous mats from fibronectin: composition and stability, Biomaterials 15 (6) (1994) 457– 464. 8080937
  91. [103]Ejim OS, Blunn GW, Brown RA, Production of artificial-orientated mats and strands from plasma fibronectin: a morphological study, Biomaterials 14 (10) (1993) 743– 748. 8218723
  92. [104]Legant WR, Chen CS, Vogel V, Force-induced fibronectin assembly and matrix remodeling in a 3D microtissue model of tissue morphogenesis, Integr. Biol 4 (10) (2012) 1164. PMC3586566 22961409
  93. [105]Singh P, Carraher C, Schwarzbauer JE, Assembly of Fibronectin Extracellular Matrix, Annu. Rev. Cell Dev. Biol 26 (1) (2010) 397– 419. 20690820 PMC3628685
  94. [106]Keller A, Kolnaar H, Flow-induced orientation and structure formation, Materials Science and Technology, VCH Verlagsgessellschaft mbH 1997, pp. 187– 268.
  95. [110]Kubow KE, Vukmirovic R, Zhe L, Klotzsch E, Smith ML, Gourdon D, Luna S, Vogel V, Mechanical forces regulate the interactions of fibronectin and collagen I in extracellular matrix, Nat. Commun 6 (1) (2015) 8026. 26272817 PMC4539566
  96. [111]Birk DE, Zycband EI, Winkelmann DA, Trelstad RL, Collagen fibrillogenesis in situ: fibril segments are intermediates in matrix assembly, Proc. Natl. Acad. Sci. U. S. A 86 (12) (1989) 4549– 4553. 2734306 PMC287308
  97. [112]Peterson BE, Rolfe RA, Kunselman A, Murphy P, Szczesny SE, Mechanical stimulation via muscle activity is necessary for the maturation of tendon multiscale mechanics during embryonic development, Front. Cell Dev. Biol 9 (2021) 725563. 34540841 PMC8446456
  98. [113]Birk DE, Southern JF, Zycband EI, Fallon JT, Trelstad RL, Collagen fibril bundles: a branching assembly unit in tendon morphogenesis, Development 107 (3) (1989) 437– 443. 2612371
  99. [114]Humphrey JD, Remodeling of a collagenous tissue at fixed lengths, J. Biomech. Eng 121 (6) (1999) 591– 597. 10633258
  100. [115]Laurent GJ, Dynamic state of collagen: pathways of collagen degradation in vivo and their possible role in regulation of collagen mass, Am. J. Physiol 252 (1 Pt 1) (1987) C1– C9. 3544859
  101. [116]Nissen R, Cardinale GJ, Udenfriend S, Increased turnover of arterial collagen in hypertensive rats, Proc. Natl. Acad. Sci. U. S. A 75 (1) (1978) 451– 453. 272662 PMC411267
  102. [117]Basser PJ, Schneiderman R, Bank RA, Wachtel E, Maroudas A, Mechanical properties of the collagen network in human articular cartilage as measured by osmotic stress technique, Arch. Biochem. Biophys 351 (2) (1998) 207– 219. 9515057
  103. [118]Bischoff JE, Arruda EM, Grosh K, Finite element modeling of human skin using an isotropic, nonlinear elastic constitutive model, J. Biomech 33 (6) (2000) 645– 652. 10807984
  104. [119]Brown NA, Pandy MG, Kawcak CE, McIlwraith CW, Force-and moment–generating capacities of muscles in the distal forelimb of the horse, J. Anat 203 (1) (2003) 101– 113. 12892409 PMC1571149
  105. [120]Harrison SM, Whitton RC, Kawcak CE, Stover SM, Pandy MG, Relationship between muscle forces, joint loading and utilization of elastic strain energy in equine locomotion, J. Exp. Biol 213 (23) (2010) 3998– 4009. 21075941
  106. [121]Maroudas A, Palla G, Gilav E, Racemization of aspartic acid in human articular cartilage, Connect. Tissue Res 28 (3) (1992) 161– 169. 1468204
  107. [122]Polga DJ, Beaubien BP, Kallemeier PM, Schellhas KP, Lew WD, Buttermann GR, Wood KB, Measurement of in vivo intradiscal pressure in healthy thoracic intervertebral discs, Spine 29 (12) (2004) 1320– 1324. 15187632
  108. [123]Riley GP, Curry V, DeGroot J, van El B, Verzijl N, Hazleman BL, Bank RA, Matrix metalloproteinase activities and their relationship with collagen remodelling in tendon pathology, Matrix Biol. 21 (2) (2002) 185– 195. 11852234
  109. [124]Sivan S-S, Wachtel E, Tsitron E, Sakkee N, van der Ham F, DeGroot J, Roberts S, Maroudas A, Collagen turnover in normal and degenerate human intervertebral discs as determined by the racemization of aspartic acid, J. Biol. Chem 283 (14) (2008) 8796– 8801. 18250164
  110. [125]Thorpe CT, Streeter I, Pinchbeck GL, Goodship AE, Clegg PD, Birch HL, Aspartic acid racemization and collagen degradation markers reveal an accumulation of damage in tendon collagen that is enhanced with aging, J. Biol. Chem 285 (21) (2010) 15674– 15681. 20308077 PMC2871433
  111. [126]Verzijl N, DeGroot J, Thorpe SR, Bank RA, Shaw JN, Lyons TJ, Bijlsma JW, Lafeber FP, Baynes JW, TeKoppele JM, Effect of collagen turnover on the accumulation of advanced glycation end products, J. Biol. Chem 275 (50) (2000) 39027– 39031. 10976109
  112. [127]Wilke HJ, Neef P, Caimi M, Hoogland T, Claes LE, New in vivo measurements of pressures in the intervertebral disc in daily life, Spine 24 (8) (1999) 755– 762. 10222525
  113. [128]Saini K, Cho S, Dooling LJ, Discher DE, Tension in fibrils suppresses their enzymatic degradation - a molecular mechanism for ’use it or lose it’, Matrix Biol. 85–86 (2020) 34– 46. PMC6906264 31201857
  114. [129]Heinemeier KM, Schjerling P, Heinemeier J, Magnusson SP, Kjaer M, Lack of tissue renewal in human adult Achilles tendon is revealed by nuclear bomb (14)C, FASEB J. 27 (5) (2013) 2074– 2079. 23401563 PMC3633810
  115. [130]Vaben C, Heinemeier KM, Schjerling P, Olsen J, Petersen MM, Kjaer M, Krogsgaard MR, No detectable remodelling in adult human menisci: an analysis based on the C(14) bomb pulse, Br. J. Sports Med 54 (23) (2020) 1433– 1437. 32409517 PMC7677461
  116. [131]Heinemeier KM, Schjerling P, Heinemeier J, Moller MB, Krogsgaard MR, Grum-Schwensen S, Petersen MM, Kjaer M, Radiocarbon dating reveals minimal collagen turnover in both healthy and osteoarthritic human cartilage, Sci. Transl. Med 8 (346) (2016) 346ra90. 27384346
  117. [132]Heinemeier KM, Schjerling P, Ohlenschlaeger TF, Eismark C, Olsen J, Kjaer M, Carbon-14 bomb pulse dating shows that tendinopathy is preceded by years of abnormally high collagen turnover, FASEB J. 32 (9) (2018) 4763– 4775. 29570396
  118. [133]Leikina E, Mertts MV, Kuznetsova N, Leikin S, Type I collagen is thermally unstable at body temperature, Proc. Natl. Acad. Sci 99 (3) (2002) 1314– 1318. 11805290 PMC122187
  119. [134]Miles CA, Ghelashvili M, Polymer-in-a-box mechanism for the thermal stabilization of collagen molecules in fibers, Biophys. J 76 (6) (1999) 3243– 3252. 10354449 PMC1300293
  120. [136]Adhikari AS, Glassey E, Dunn AR, Conformational dynamics accompanying the proteolytic degradation of trimeric collagen I by collagenases, J. Am. Chem. Soc 134 (32) (2012) 13259– 13265. 22720833 PMC4800024
  121. [137]Kirkness MWH, Forde NR, Single-molecule assay for proteolytic susceptibility: force-induced collagen destabilization, Biophys. J 114 (3) (2018) 570– 576. 29414702 PMC5985029
  122. [138]Minond D, Lauer-Fields JL, Nagase H, Fields GB, Matrix metalloproteinase triple-helical peptidase activities are differentially regulated by substrate stability, Biochemistry 43 (36) (2004) 11474– 11481. 15350133
  123. [139]Chang SW, Flynn BP, Ruberti JW, Buehler MJ, Molecular mechanism of force induced stabilization of collagen against enzymatic breakdown, Biomaterials 33 (15) (2012) 3852– 3859. 22401852 PMC3309414
  124. [140]Dittmore A, Silver J, Sarkar SK, Marmer B, Goldberg GI, Neuman KC, Internal strain drives spontaneous periodic buckling in collagen and regulates remodeling, Proc. Natl. Acad. Sci. U. S. A 113 (30) (2016) 8436– 8441. 27402741 PMC4968713
  125. [141]Birk DE, Fitch JM, Babiarz JP, Doane KJ, Linsenmayer TF, Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter, J. Cell Sci 95 (Pt 4) (1990) 649– 657. 2384532
  126. [142]Birk DE, Nurminskaya MV, Zycband EI, Collagen fibrillogenesis in situ: fibril segments undergo post-depositional modifications resulting in linear and lateral growth during matrix development, Dev. Dyn 202 (3) (1995) 229– 243. 7780173
  127. [143]Scott JE, The periphery of the developing collagen fibril. Quantitative relationships with dermatan sulphate and other surface-associated species, Biochem. J 218 (1) (1984) 229– 233. 6712611 PMC1153328
  128. [144]Benedek GB, Theory of transparency of the eye, Appl. Opt 10 (3) (1971) 459– 473. 20094474
  129. [145]Meek KM, Corneal collagen—its role in maintaining corneal shape and transparency, Biophys. Rev 1 (2) (2009) 83– 93. 28509987 PMC5425665
  130. [146]Maurice DM, The structure and transparency of the cornea, J. Physiol 136 (2) (1957) 263– 286. 13429485 PMC1358888
  131. [147]Chakravarti S, Petroll WM, Hassell JR, Jester JV, Lass JH, Paul J, Birk DE, Corneal opacity in lumican-null mice: defects in collagen fibril structure and packing in the posterior stroma, Invest. Ophthalmol. Vis. Sci 41 (11) (2000) 3365– 3373. 11006226 PMC4318236
  132. [148]Vogel KG, Trotter JA, The effect of proteoglycans on the morphology of collagen fibrils formed in vitro, Coll. Relat. Res 7 (2) (1987) 105– 114. 3621881
  133. [149]Brown AI, Kreplak L, Rutenberg AD, An equilibrium double-twist model for the radial structure of collagen fibrils, Soft Matter 10 (42) (2014) 8500– 8511. 25238208
  134. [150]Svensson RB, Herchenhan A, Starborg T, Larsen M, Kadler KE, Qvortrup K, Magnusson SP, Evidence of structurally continuous collagen fibrils in tendons, Acta Biomater. 50 (2017) 293– 301. 28063986
  135. [151]Graham HK, Holmes DF, Watson RB, Kadler KE, Identification of collagen fibril fusion during vertebrate tendon morphogenesis. The process relies on unipolar fibrils and is regulated by collagen-proteoglycan interaction, J. Mol. Biol 295 (4) (2000) 891– 902. 10656798
  136. [152]Kadler KE, Holmes DF, Graham H, Starborg T, Tip-mediated fusion involving unipolar collagen fibrils accounts for rapid fibril elongation, the occurrence of fibrillar branched networks in skin and the paucity of collagen fibril ends in vertebrates, Matrix Biol. 19 (4) (2000) 359– 365. 10963997
  137. [153]Christiansen DL, Huang EK, Silver FH, Assembly of type I collagen: fusion of fibril subunits and the influence of fibril diameter on mechanical properties, Matrix Biol. 19 (5) (2000) 409– 420. 10980417
  138. [154]Ambrosi D, Ben Amar M, Cyron CJ, DeSimone A, Goriely A, Humphrey JD, Kuhl E, Growth and remodelling of living tissues: perspectives, challenges and opportunities, J. R. Soc. Interface 16 (157) (2019) PMC6731508 31431183
  139. [155]Herchenhan A, Uhlenbrock F, Eliasson P, Weis M, Eyre D, Kadler KE, Magnusson SP, Kjaer M, Lysyl oxidase activity is required for ordered collagen fibrillogenesis by tendon cells, J. Biol. Chem 290 (26) (2015) 16440– 16450. 25979340 PMC4481240
  140. [156]Kalson NS, Holmes DF, Herchenhan A, Lu Y, Starborg T, Kadler KE, Slow stretching that mimics embryonic growth rate stimulates structural and mechanical development of tendon-like tissue in vitro, Dev. Dyn 240 (11) (2011) 2520– 2528. 22012594 PMC3505797
  141. [157]Pan XS, Li J, Brown EB, Kuo CK, Embryo movements regulate tendon mechanical property development, Philos. Trans. R. Soc. B Biol. Sci 373 (1759) (2018) PMC6158208 30249775
  142. [158]Sutter NB, Bustamante CD, Chase K, Gray MM, Zhao K, Zhu L, Padhukasahasram B, Karlins E, Davis S, Jones PG, Quignon P, Johnson GS, Parker HG, Fretwell N, Mosher DS, Lawler DF, Satyaraj E, Nordborg M, Lark KG, Wayne RK, Ostrander EA, A single IGF1 allele is a major determinant of small size in dogs, Science 316 (5821) (2007) 112– 115. 17412960 PMC2789551
  143. [159]Ilizarov GA, The tension-stress effect on the genesis and growth of tissues: part II. The influence of the rate and frequency of distraction, Clin. Orthop. Relat. Res 239 (1989) 263– 285. 2912628
  144. [160]Ilizarov GA, The tension-stress effect on the genesis and growth of tissues. Part I. The influence of stability of fixation and soft-tissue preservation, Clin. Orthop. Relat. Res 238 (1989) 249– 281. 2910611
  145. [161]Bonnel F, Peruchon E, Baldet P, Dimeglio A, Rabischong P, Effects of compression on growth plates in the rabbit, Acta Orthop. Scand 54 (5) (1983) 730– 733. 6670489
  146. [162]Yoo WJ, Cheon J-E, Lee HR, Cho T-J, Choi IH, Physeal growth arrest by excessive compression: histological, biochemical, and Micro-CT observations in rabbits, Clin. Orthopedic Surg 3 (4) (2011) 309. PMC3232359 22162794
  147. [164]Coulombre AJ, The role of intraocular pressure in the development of the chick eye. II. Control of corneal size, AMA Arch. Ophthalmol 57 (2) (1957) 250– 253. 13393895
  148. [165]Coulombre AJ, Coulombre JL, The role of intraocular pressure in the development of the chick eye. IV. Corneal curvature, AMA Arch. Ophthalmol 59 (4) (1958) 502– 506. 13519969
  149. [166]Allen DB, Goldberg BD, Stimulation of collagen synthesis and linear growth by growth hormone in glucocorticoid-treated children, Pediatrics 89 (3) (1992) 416– 421. 1741214
  150. [167]Doessing S, Heinemeier KM, Holm L, Mackey AL, Schjerling P, Rennie M, Smith K, Reitelseder S, Kappelgaard AM, Rasmussen MH, Flyvbjerg A, Kjaer M, Growth hormone stimulates the collagen synthesis in human tendon and skeletal muscle without affecting myofibrillar protein synthesis, J. Physiol 588 (Pt 2) (2010) 341– 351. 19933753 PMC2821728
  151. [169]Zitnay JL, Li Y, Qin Z, San BH, Depalle B, Reese SP, Buehler MJ, Yu SM, Weiss JA, Molecular level detection and localization of mechanical damage in collagen enabled by collagen hybridizing peptides, Nat. Commun 8 (1) (2017) 14913. 28327610 PMC5364439
  152. [170]Siadat SM, Silverman AA, Susilo ME, Paten JA, DiMarzio CA, Ruberti JW, Development of fluorescently labeled, functional type I collagen molecules, Macromol. Biosci 22 (3) (2022) 2100144. 34856056
  153. [171]Konda SS, Brantley JN, Varghese BT, Wiggins KM, Bielawski CW, Makarov DE, Molecular catch bonds and the anti-Hammond effect in polymer mechanochemistry, J. Am. Chem. Soc 135 (34) (2013) 12722– 12729. 23905836

Cited by

Sorted by citations

Authors
Siadat, S. M., & Ruberti, J. W.
Affiliations
Northeastern University (US)
Corresponding author
Ruberti, Jeffrey W.
ORCID
Venue
Acta Biomaterialia
Publisher
Elsevier BV
Published
2023-06
Volume
163
Pages
50-62
ISSN
1742-7061 (ISSN-L)
DOI
10.1016/j.actbio.2023.01.025
PMC
PMC13270376
OpenAlex
W4316804348
Cited by
87
References
1
Citations by year
2026: 27 · 2025: 28 · 2024: 20 · 2023: 12
FWCI
1.48
Type
journal article
Language
en
Open access
Licence
Locations
  • Acta Biomaterialia (publishedVersion)
  • SSRN Electronic Journal (acceptedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (publishedVersion)
Funders
National Eye Institute (R01EY015500, R21EY029167, R01EY034124)
Topics
  • Physical Sciences › Materials Science › Biomaterials › Collagen: Extraction and Characterization
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Connective tissue disorders research
Keywords
collagen, mechanochemistry, collagen fibril formation, mechanical forces, collagen self-assembly, collagen remodeling, fibrosis, type II collagen, osteoarthritis, connective tissue mechanics, mechanobiology
MeSH terms
Animals, Collagen, Extracellular Matrix, Tendons, Fibrillar Collagens, Collagen Type II

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