Cellular distribution and gene expression profile during flexor tendon graft repair: A novel tissue engineering approach

Journal of Tissue Engineering

Volumn 4, Issue 1, 2013, Pages 1-16

  Juneja, Subhash C ^a,b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b TORONTO WESTERN HOSPITAL   (Canada)

Author keywords

Adhesion formation; Flexor tendon; Graft healing; Scars

Indexed keywords

ADAMTS1 PROTEIN; COLLAGEN TYPE 1; MESSENGER RNA; NEUTROPHIL COLLAGENASE; PROTEIN LYSINE 6 OXIDASE; SOMATOMEDIN; THROMBOSPONDIN 2; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; VERSICAN;

ALLOGRAFT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELLULAR DISTRIBUTION; FLEXOR TENDON INJURY; GENE; GENE EXPRESSION; HISTOLOGY; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA EXTRACTION; SCAR FORMATION; SKELETAL MUSCLE; TENDON GRAFT; TISSUE ADHESION; TISSUE ENGINEERING; WOUND CONTRACTION; WOUND HEALING;

EID: 84890193444     PISSN: None     EISSN: 20417314     Source Type: Journal    
DOI: 10.1177/2041731413492741     Document Type: Article

References (91)

1. Taras JS and Lamb MJ. Treatment of flexor tendon injuries: surgeons' perspective. J Hand Ther 1999; 12: 141-148.
2. Lilly SI and Messer TM. Complications after treatment of flexor tendon injuries. J Am Acad Orthop Surg 2006; 14: 387-396.
3. Stark HH, Anderson DR, Zemel NP, et al. Bridge flexor tendon grafts. Clin Orthop Relat Res 1989; 242: 51-59.
4. Seiler JG. 3rd, Chu CR, Amiel D, et al. The Marshall R. Urist Young Investigator Award. Autogenous flexor tendon grafts. Biologic mechanisms for incorporation. Clin Orthop Relat Res 1997; 345: 239-247.
5. Boyer MI. Flexor tendon biology. Hand Clin 2005; 21: 159-166.
6. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999; 21: 70-71.
7. Hasslund S, Jacobson JA, Dadali T, et al. Adhesions in a murine flexor tendon graft model: autograft versus allograft reconstruction. J Orthop Res 2008; 26: 824-833.
8. Wu YF, Chen CH, Cao Y, et al. Molecular events of cellular apoptosis and proliferation in the early tendon healing period. J Hand Surg Am 2010; 35: 2-10.
9. Wong JK, Lui YH, Kapacee Z, et al. The cellular biology of flexor tendon adhesion formation: an old problem in a new paradigm. Am J Pathol 2009; 175: 1938-1951.
10. Kobayashi M, Watanabe N, Oshima Y, et al. The fate of host and graft cells in early healing of bone tunnel after tendon graft. Am J Sports Med 2005; 33: 1892-1897.
11. Crippa MP. Urokinase-type plasminogen activator. Int J Biochem Cell Biol 2007; 39: 690-694.
12. Smith PC and Martínez J. Differential uPA expression by TGF-beta1 in gingival fibroblasts. J Dent Res 2006; 85: 150-155.
13. Xia W, De Bock C, Murrell GA, et al. Expression of urokinase-type plasminogen activator and its receptor is up-regulated during tendon healing. J Orthop Res 2003; 21: 819-825.
14. Chan JC, Duszczyszyn DA, Castellino FJ, et al. Accelerated skin wound healing in plasminogen activator inhibitor-1-deficient mice. Am J Pathol 2001; 159: 1681-1688.
15. Weiler A, Unterhauser FN, Bail HJ, et al. Alpha-smooth muscle actin is expressed by fibroblastic cells of the ovine anterior cruciate ligament and its free tendon graft during remodeling. J Orthop Res 2002; 20: 310-317.
16. Menetrey J, Laumonier T, Garavaglia G, et al. α-smooth muscle actin and TGF-β receptor I expression in the healing rabbit medial collateral and anterior cruciate ligaments. Injury 2011; 42: 735-741.
17. O'Malley Y, Zhao W, Barcellos-Hoff MH, et al. Radiation-induced alterations in rat mesangial cell Tgfb1 and Tgfb3 gene expression are not associated with altered secretion of active Tgfb isoforms. Radiation Res 1999; 152: 622-628.
18. Frank S, Madlener M and Werner S. Transforming growth factors beta1, beta2, and beta3 and their receptors are differentially regulated during normal and impaired wound healing. J Biol Chem 1996; 271: 10188-10193.
19. Douglas HE. Tgf-β in wound healing: a review. J Wound Care 2010; 19: 403-406.
20. Massague J. How cells read TGF-β signals. Nat Rev Mol Cell Biol 2000; 1: 169-178.
21. Lebrin F, Deckers M, Bertolino P, et al. TGF-beta receptor function in the endothelium. Cardiovasc Res 2005; 65: 599-608.
22. Marchuk DA. The molecular genetics of hereditary hemorrhagic telangiectasia. Chest 1997; 111: 79S-82S.
23. Seki T, Hong KH, Yun J, et al. Isolation of a regulatory region of activin receptor-like kinase1gene sufficient for arterial endothelium-specific expression. Circ Res 2004; 94: e72-e77.
24. Ngo M, Pham H, Longaker MT, et al. Differential expression of transforming growth factor-beta receptors in a rabbit zone II flexor tendon wound healing model. Plast Reconstr Surg 2001; 108: 1260-1267.
25. Sciore P, Boykiw R and Hart DA. Semiquantitative reverse transcription-polymerase chain reaction analysis of mRNA for growth factors and growth factor receptors from normal and healing rabbit medial collateral ligament tissue. J Orthop Res 1998; 16: 429-437.
26. Tsubone T, Moran SL, Amadio PC, et al. Expression of growth factors in canine flexor tendon after laceration in vivo. Ann Plast Surg 2004; 53: 393-397.
27. Berglund ME, Hart DA, Reno C, et al. Growth factor and protease expression during different phases of healing after rabbit deep flexor tendon repair. J Orthop Res 2011; 29: 886-892.
28. Itoh N and Ornitz DM. Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J Biochem 2011; 149: 121-130.
29. Ortega S, Ittmann M, Tsang SH, et al. Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor-2. Proc Natl Acad Sci U S A 1998; 95: 5672-5677.
30. Thomopoulos S, Das R, Sakiyama-Elbert S, et al. bFGF and PDGF-BB for tendon repair: controlled release and biologic activity by tendon fibroblasts in vitro. Ann Biomed Eng 2010; 38: 225-234.
31. Tang JB, Cao Y, Zhu B, et al. Adeno-associated virus-2-mediated bFGF gene transfer to digital flexor tendons significantly increases healing strength. An in vivo study. J Bone Joint Surg Am 2008; 90: 1078-1089.
32. Chen D, Zhao M and Mundy GR. Bone morphogenetic proteins. Growth Factors 2004; 22: 233-241.
33. Wolfman NM, Hattersley G, Cox K, et al. Ectopic induction of tendon and ligament in rats by growth and differentiation factors 5, 6, and 7, members of the TGF-beta gene family. J Clin Invest 1997; 100: 321-330.
34. Mikic B. Multiple effects of GDF-5 deficiency on skeletal tissues: implications for therapeutic bioengineering. Ann Biomed Eng 2004; 32: 466-476.
35. Aspenberg P and Forslund C. Enhanced tendon healing with GDF 5 and 6. Acta Orthop Scand 1999; 70: 51-54.
36. Chhabra A, Tsou D, Clark RT, et al. GDF-5 deficiency in mice delays Achilles tendon healing. J Orthop Res 2003; 21: 826-835.
37. Oshiro W, Lou J, Xing X, et al. Flexor tendon healing in the rat: a histologic and gene expression study. J Hand Surg Am 2003; 28: 814-823.
38. Dahlgren LA, Mohammed HO and Nixon AJ. Temporal expression of growth factors and matrix molecules in healing tendon lesions. J Orthop Res 2005; 23: 84-92.
39. Fushida-Takemura H, Fukuda M, Maekawa N, et al. Detection of lysyl oxidase gene expression in rat skin during wound healing. Arch Dermatol Res 1996; 288: 7-10.
40. Ritzenthaler JD, Goldstein RH, Fine A, et al. Transforming-growth-factor-β activation elements in the distal promoter regions of the rat α1 type I collagen gene. Biochem J 1991; 280: 157-162.
41. Rossi P, Karsenty G, Roberts AB, et al. A nuclear factor 1 binding site mediates the transcriptional activation of a type I collagen promoter by transforming growth factor-β. Cell 1988; 52: 405-414.
42. Juneja SC, Reynolds D, Awad HA, et al. Tendon/ligament defect in Mds1 knockout mouse. In: Orthopedic Research Society (ORS) meeting, Long Beach CA, USA, 13-16 January 2011, poster no. 1620. Rosemont, IL: ORS.
43. Wight TN. Versican: a versatile extracellular matrix proteoglycan in cell biology. Curr Opin Cell Biol 2002; 14: 617-623.
44. Scott A, Lian Ø, Roberts CR, et al. Increased versican content is associated with tendinosis pathology in the patellar tendon of athletes with jumper's knee. Scand J Med Sci Sports 2008; 18: 427-435.
45. Järveläinen H, Puolakkainen P, Pakkanen S, et al. A role for decorin in cutaneous wound healing and angiogenesis. Wound Repair Regen 2006; 14: 443-452.
46. Toeda K, Nakamura K, Hirohata S, et al. Versican is induced in infiltrating monocytes in myocardial infarction. Mol Cell Biochem 2005; 280: 47-56.
47. Schönherr E, Hausser H, Beavan L, et al. Decorin-type I collagen interaction. Presence of separate core protein-binding domains. J Biol Chem 1995; 270: 8877-8883.
48. Kalamajski S, Aspberg A and Oldberg A. The decorin sequence SYIRIADTNIT binds collagen type I. J Biol Chem 2007; 282: 16062-16067.
49. Zhang G, Ezura Y, Chervoneva I, et al. Decorin regulates assembly of collagen fibrils and acquisition of biomechanical properties during tendon development. J Cell Biochem 2006; 98: 1436-1449.
50. Robbins JR, Evanko SP and Vogel KG. Mechanical loading and TGF-beta regulate proteoglycan synthesis in tendon. Arch Biochem Biophys 1997; 342: 203-211.
51. Simeon A, Wegrowski A, Bontemps Y, et al. Expression of glycosaminoglycans and small proteoglycans in wounds: modulation by the tripeptide-copper complex glycyl-l-histidyl-l-lysine-Cu(2+). J Invest Dermatol 2000; 115: 962-968.
52. Corsi A, Xu T, Chen XD, et al. Phenotypic effects of biglycan deficiency are linked to collagen fibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers-Danlos-like changes in bone and other connective tissues. J Bone Miner Res 2002; 17: 1180-1189.
53. Hiroyuki Y, Hiromichi F, Wataru A, et al. Patellar tendon strength of a specific protein-knockout mouse. Effects of biglycan on the mechanical property of biological fibrous tissues. Nihon Kikai Gakkai Kanto Shibu Sokai Koen Ronbunshu 2005; 11: 475-476.
54. Danielson KG, Baribault H, Holmes DF, et al. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 1997; 136: 729-743.
55. Ilkhani-Pour S, Voleti PB, Buckley MR, et al. Achilles tendon repair response to injury is enhanced by the absence of decorin. In: Orthopedic Research Society (ORS), annual meeting, San Antonio, TX, 26-29 January 2013, poster no. 0616. Rosemont, IL: ORS.
56. Moustakas A, Pardali K, Gaal A, et al. Mechanisms of TGF-beta signaling in regulation of cell growth and differentiation. Immunol Lett 2002; 82: 85-91.
57. Comalada M, Cardó M, Xaus J, et al. Decorin reverses the repressive effect of autocrine-produced TGF-beta on mouse macrophage activation. J Immunol 2003; 170: 4450-4456.
58. Border WA, Noble NA, Yamamoto T, et al. Natural inhibitor of transforming growth factor-beta protects against scarring in experimental kidney disease. Nature 1992; 360: 361-364.
59. Rapraeger AC, Krufka A and Olwin BB. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 1991; 252: 1705-1708.
60. Olwin BB and Rapraeger A. Repression of myogenic differentiation by aFGF, bFGF, and K-FGF is dependent on cellular heparan sulfate. J Cell Biol 1992; 118: 631-639.
61. Hosaka Y, Kirisawa R, Mafune N, et al. Downregulation of decorin and transforming growth factor-beta1 by decorin gene suppression in tendinocytes. Connect Tissue Res 2005; 46: 18-26.
62. Hamilton DW. Functional role of periostin in development and wound. J Cell Commun Signal 2008; 2: 9-17.
63. Norris RA, Damon B, Mironov V, et al. Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. J Cell Biochem 2007; 101: 695-711.
64. Chiquet-Ehrismann R and Tucker RP. Tenascins and the importance of adhesion modulation. Cold Spring Harb Perspect Biol 2011; 10: 7-19.
65. Järvinen TA, Józsa L, Kannus P, et al. Mechanical loading regulates the expression of tenascin-C in the myotendinous junction and tendon but does not induce de novo synthesis in the skeletal muscle. J Cell Sci 2003; 116: 857-866.
66. Chiquet M and Fambrough DM. Chick myotendinous antigen. II. A novel extracellular glycoprotein complex consisting of large disulfide-linked subunits. J Cell Biol 1984; 98: 1937-1946.
67. Kannus P, Jozsa L, Jarvinen TA, et al. Location and distribution of non-collagenous matrix proteins in musculoskeletal tissues of rat. Histochem J 1998; 30: 799-810.
68. Järvinen TA, Jozsa L, Kannus P, et al. Mechanical loading regulates tenascin-C expression in the osteotendinous junction. J Cell Sci 1999; 112: 3157-3166.
69. Riley GP, Harrall RL, Cawston TE, et al. Tenascin-C and human tendon degeneration. Am J Pathol 1996; 149: 933-943.
70. Ireland D, Harrall R, Curry V, et al. Multiple changes in gene expression in chronic human Achilles tendinopathy. Matrix Biol 2001; 20: 159-169.
71. Mokone GG, Gajjar M, September AV, et al. The guanine-thymine dinucleotide repeat polymorphism within the tenascin-C gene is associated with Achilles tendon injuries. Am J Sports Med 2005; 33: 1016-1021.
72. Carey WA, Taylor GD, Dean WB, et al. Tenascin-C deficiency attenuates TGF-β-mediated fibrosis following murine lung injury. Am J Physiol Lung Cell Mol Physiol 2010; 299: L785-L793.
73. Chuong CM and Chen HM. Enhanced expression of neural cell adhesion molecules and tenascin (cytotactin) during wound healing. Am J Pathol 1991; 138: 427-440.
74. Bornstein P. Thrombospondins as matricellular modulators of cell function. J Clin Invest 2001; 107: 929-934.
75. Iruela-Arispe ML, Liska DJ and Sage EH. Differential expression of thrombospondin 1, 2, and 3 during murine development. Dev Dyn 1993; 197: 40-56.
76. Kyriakides TR, Zhu YH, Smith LT, et al. Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis. J Cell Biol 1998; 140: 419-430.
77. Bornstein P, Kyriakides TR, Yang Z, et al. Thrombospondin 2 modulates collagen fibrillogenesis and angiogenesis. J Investig Dermatol Symp Proc 2000; 5: 61-66.
78. Lee NV, Sato M, Annis DS, et al. ADAMTS1 mediates the release of antiangiogenic polypeptides from TSP1 and 2. EMBO J 2006; 25: 5270-5283.
79. Nwomeh BC, Liang HX, Cohen IK, et al. MMP-8 is the predominant collagenase in healing wounds and nonhealing ulcers. J Surg Res 1999; 81: 189-195.
80. Gutiérrez-Fernández A, Inada M, Balbín M, et al. Increased inflammation delays wound healing in mice deficient in collagenase-2 (MMP-8). FASEB J 2007; 21: 2580-2591.
81. Wu N, Jansen ED and Davidson JM. Comparison of mouse matrix metalloproteinase 13 expression in free-electron laser and scalpel incisions during wound healing. J Invest Dermatol 2003; 121: 926-932.
82. Pasternak B. Towards surgical use of matrix metalloproteinase biology. Medical Dissertations, Linkoping University, Sweden, 2008.
83. Holmbeck K, Bianco P, Caterina J, et al. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 1999; 99: 81-92.
84. Hoffmann A, Pelled G, Turgeman G, et al. Neotendon formation induced by manipulation of the Smad8 signalling pathway in mesenchymal stem cells. J Clin Invest 2006; 116: 940-952.
85. Ramcharan M, Li Z, Lee JY, et al. Smad8 activation: common signaling pathway that may be required for BMP12 and mechanical loading induced mesenchymal stem cell teno-differentiation. In: Orthopedic Research Society (ORS) meeting, New Orleans, LA, USA, 6-9 March, 2010, poster no. 1097. Rosemont, IL: ORS.
86. Schweitzer R, Chyung JH and Murtaugh LC. Analysis of the tendon cell fate using Scleraxis, a specific marker for tendons and ligaments. Development 2001; 128: 3855-3866.
87. Gulotta LV, Kovacevic D, Packer JD, et al. Bone marrow-derived mesenchymal stem cells transduced with Scleraxis improve rotator cuff healing in a rat model. Am J Sports Med 2011; 39: 1282-1289.
88. Scott A, Sampaio A, Abraham T, et al. Scleraxis expression is coordinately regulated in a murine model of patellar tendon injury. J Orthop Res 2011; 29: 289-296.
89. Ito Y, Toriuchi N, Yoshitaka T, et al. The Mohawk homeobox gene is a critical regulator of tendon differentiation. Proc Natl Acad Sci U S A 2010; 107: 10538-10542.
90. Liu W, Watson SS, Lan Y, et al. The atypical homeodomain transcription factor Mohawk controls tendon morphogenesis. Mol Cell Biol 2010; 30: 4797-4807.
91. Staverosky JA, Pryce BA, Watson SS, et al. Tubulin polymerization-promoting protein family member 3, Tppp3, is a specific marker of the differentiating tendon sheath and synovial joints. Dev Dyn 2009; 238: 685-692.