CURRENT SITUATION AND PROSPECT OF Tenomodulin IN TENDON TISSUE ENGINEERING_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

GUAN Cewen , LEI Xing , SONG Yang , QU Yanlong.

Department of Orthopedics, the 1st Affiliated Hospital of Harbin Medical University, Harbin Heilongjiang, 150001, P.R.China. Corresponding author: QU Yanlong, E-mail: xytowner@163.com;

Corresponding author：

Keywords：

Tissue engineered tendon; Tenomodulin; Cytokine; Scaffold material

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Objective To review the latest researches of Tenomodulin in tendon tissue engineering, to predict the progress of research and application of Tenomodulin. Methods The literature concerning Tenomodulin in tendon tissue engineering was collected and analyzed. Results Tenomodulin is a type II transmembrane glycoprotein that can regulate growth of tendon and contains a C-terminal anti-angiogenic domain. The human Tenomodulin gene spans approximately 1 360 bp and is mapped to Xq22.1. The expression of Tenomodulin is regulated by various biological factors, especially Scleraxis; and the nature and structure of scaffold material as well as the stain loading and cell passage, can modulate the expression of Tenomodulin. Conclusion Tenomodulin, as relatively specific molecule makers for tendon and containing a C-terminal anti-angiogenic domain, is expected to play a significant role in tendon tissue engineering.

Citation： GUAN Cewen,LEI Xing,SONG Yang,QU Yanlong.. CURRENT SITUATION AND PROSPECT OF Tenomodulin IN TENDON TISSUE ENGINEERING. Chinese Journal of Reparative and Reconstructive Surgery, 2013, 27(1): 101-105. doi: Copy

1.	Rui YF, Lui PP, Li G, et al. Isolation and characterization of multipotent rat tendon-derived stem cells. Tissue Eng Part A, 2010, 16(5): 1549-1558.
2.	Tan Q, Lui PP, Rui YF, et al. Comparison of potentials of stem cells isolated from tendon and bone marrow for musculoskeletal tissue engineering. Tissue Eng Part A, 2012, 18(7-8): 840-851.
3.	Alberton P, Popov C, Prägert M, et al. Conversion of human bone marrow-derived mesenchymal stem cells into tendon progenitor cells by ectopic expression of scleraxis. Stem Cells Dev, 2012, 21(6): 846-858.
4.	Yukata K, Matsui Y, Shukunami C, et al. Differential expression of Tenomodulin and Chondromodulin-1 at the insertion site of the tendon reflects a phenotypic transition of the resident cells. Tissue Cell, 2010, 42(2): 116-120.
5.	Backman LJ, Fong G, Andersson G, et al. Substance P is a mechanoresponsive, autocrine regulator of human tenocyte proliferation. PLoS One, 2011, 6(11): e27209.
6.	Kishore V, Bullock W, Sun X, et al. Tenogenic differentiation of human MSCs induced by the topography of electrochemically aligned collagen threads. Biomaterials, 2012, 33(7): 2137-2144.
7.	Shukunami C, Oshima Y, Hiraki Y. Molecular cloning of tenomodulin, a novel chondromodulin-I related gene. Biochem Biophys Res Commun, 2001, 280(5): 1323-1327.
8.	Oshima Y, Sato K, Tashiro F, et al. Anti-angiogenic action of the C-terminal domain of tenomodulin that shares homology with chondromodulin-I. J Cell Sci, 2004, 117(Pt 13): 2731-2744.
9.	Sánchez-Pulido L, Devos D, Valencia A. BRICHOS: a conserved domain in proteins associated with dementia, respiratory distress and cancer. Trends Biochem Sci, 2002, 27(7): 329-332.
10.	Aslan H, Kimelman-Bleich N, Pelled G, et al. Molecular targets for tendon neoformation. J Clin Invest, 2008, 118(2): 439-444.
11.	Shukunami C, Takimoto A, Miura S, et al. Chondromodulin-I and tenomodulin are differentially expressed in the avascular mesenchyme during mouse and chick development. Cell Tissue Res, 2008, 332(1): 111-122.
12.	Shukunami C, Takimoto A, Oro M, et al. Scleraxis positively regulates the expression of tenomodulin, a differentiation marker of tenocytes. Dev Biol, 2006, 298(1): 234-247.
13.	Docheva D, Hunziker EB, Fässler R, et al. Tenomodulin is necessary for tenocyte proliferation and tendon maturation. Mol Cell Biol, 2005, 25(2): 699-705.
14.	Watahiki J, Yamaguchi T, Enomoto A, et al. Identification of differentially expressed genes in mandibular condylar and tibial growth cartilages using laser microdissection and fluorescent differential display: chondromodulin-I (ChM-1) and tenomodulin (TeM) are differentially expressed in mandibular condylar and other growth cartilages. Bone, 2008, 42(6): 1053-1060.
15.	Pisani DF, Pierson PM, Massoudi A, et al. Myodulin is a novel potential angiogenic factor in skeletal muscle. Exp Cell Res, 2004, 292(1): 40-50.
16.	Shukunami C, Hiraki Y. Chondromodulin-I and tenomodulin: the negative control of angiogenesis in connective tissue. Curr Pharm Des, 2007, 13(20): 2101-2112.
17.	Kimura N, Shukunami C, Hakuno D, et al. Local tenomodulin absence, angiogenesis, and matrix metalloproteinase activation are associated with the rupture of the chordae tendineae cordis. Circulation, 2008, 118(17): 1737-1747.
18.	Hiraki Y, Shukunami C. Angiogenesis inhibitors localized in hypovascular mesenchymal tissues: chondromodulin-I and tenomodulin. Connect Tissue Res, 2005, 46(1): 3-11.
19.	Lorda-Diez CI, Montero JA, Martinez-Cue C, et al. Transforming growth factors beta coordinate cartilage and tendon differentiation in the developing limb mesenchyme. J Biol Chem, 2009, 284(43): 29988-29996.
20.	Schneider PR, Buhrmann C, Mobasheri A, et al. Three-dimensional high-density co-culture with primary tenocytes induces tenogenic differentiation in mesenchymal stem cells. J Orthop Res, 2011, 29(9): 1351-1360.
21.	Liu W, Watson SS, Lan Y, et al. The atypical homeodomain transcription factor Mohawk controls tendon morphogenesis. Mol Cell Biol, 2010, 30(20): 4797-4807.
22.	Inoue M, Ebisawa K, Itaya T, et al. Effect of GDF-5 and BMP-2 on the expression of tendo/ligamentogenesis-related markers in human PDL-derived cells. Oral Dis, 2012, 18(2): 206-212.
23.	Park A, Hogan MV, Kesturu GS, et al. Adipose-derived mesenchymal stem cells treated with growth differentiation factor-5 express tendon-specific markers. Tissue Eng Part A, 2010, 16(9): 2941-2951.
24.	Haddad-Weber M, Prager P, Kunz M, et al. BMP12 and BMP13 gene transfer induce ligamentogenic differentiation in mesenchymal progenitor and anterior cruciate ligament cells. Cytotherapy, 2010, 12(4): 505-513.
25.	Violini S, Ramelli P, Pisani LF, et al. Horse bone marrow mesenchymal stem cells express embryo stem cell markers and show the ability for tenogenic differentiation by in vitro exposure to BMP-12. BMC Cell Biol, 2009, 10: 29.
26.	倪明, 芮云峰, 陈启明, 等. 生长分化因子7体外促进BMSCs向肌腱细胞分化的研究. 中国修复重建外科杂志, 2011, 25(9): 1103-1109.
27.	Lee JY, Zhou Z, Taub PJ, et al. BMP-12 treatment of adult mesenchymal stem cells in vitro augments tendon-like tissue formation and defect repair in vivo. PloS One, 2011, 6(3): e17531.
28.	Mendias CL, Bakhurin KI, Faulkner JA. Tendons of myostatin-deficient mice are small, brittle, and hypocellular. Proc Natl Acad Sci U S A, 2008, 105(1): 388-393.
29.	Engler AJ, Sen S, Sweeney HL, et al. Matrix elasticity directs stem cell lineage specification. Cell, 2006, 126(4): 677-689.
30.	Kilian KA, Bugarija B, Lahn BT, et al. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci U S A, 2010, 107(11): 4872-4877.
31.	Kishore V, Bullock W, Sun X, et al. Tenogenic differentiation of human MSCs induced by the topography of electrochemically aligned collagen threads. Biomaterials, 2012, 33(7): 2137-2144.
32.	Omae H, Zhao C, Sun YL, et al. Multilayer tendon slices seeded with bone marrow stromal cells: a novel composite for tendon engineering. J Orthop Res, 2009, 27(7): 937-942.
33.	Omae H, Sun YL, An KN, et al. Engineered tendon with decellularized xenotendon slices and bone marrow stromal cells: an in vivo animal study. J Tissue Eng Regen Med, 2012, 6(3): 238-244.
34.	Bashur CA, Shaffer RD, Dahlgren LA, et al. Effect of fiber diameter and alignment of electrospun polyurethane meshes on mesenchymal progenitor cells. Tissue Eng Part A, 2009, 15(9): 2435-2445.
35.	Zhu J, Li J, Wang B, et al. The regulation of phenotype of cultured tenocytes by microgrooved surface structure. Biomaterials, 2010, 31(27): 6952-6958.
36.	Eliasson P, Andersson T, Aspenberg P. Rat Achilles tendon healing: mechanical loading and gene expression. J Appl Physiol, 2009, 107(2): 399-407.
37.	Mendias CL, Gumucio JP, Bakhurin KI, et al. Physiological loading of tendons induces scleraxis expression in epitenon fibroblasts. J Orthop Res, 2012, 30(4): 606-612.
38.	廖梅旭, 宁良菊, 陈晓禾, 等. 应变诱导BMSCs腱向分化的实验研究. 中国修复重建外科杂志, 2010, 24(7): 817-821.
39.	Tan Q, Lui PP, Rui YF. Effect of in vitro passaging on the stem cell-related properties of tendon-derived stem cells-implications in tissue engineering. Stem Cells Dev, 2012, 21(5): 790-800.
40.	Mazzocca AD, Chowaniec D, McCarthy MB, et al. In vitro changes in human tenocyte cultures obtained from proximal biceps tendon: multiple passages result in changes in routine cell markers. Knee Surg Sports Traumatol Arthrosc, 2012, 20(9): 1666-1672.

1. Rui YF, Lui PP, Li G, et al. Isolation and characterization of multipotent rat tendon-derived stem cells. Tissue Eng Part A, 2010, 16(5): 1549-1558.
2. Tan Q, Lui PP, Rui YF, et al. Comparison of potentials of stem cells isolated from tendon and bone marrow for musculoskeletal tissue engineering. Tissue Eng Part A, 2012, 18(7-8): 840-851.
3. Alberton P, Popov C, Prägert M, et al. Conversion of human bone marrow-derived mesenchymal stem cells into tendon progenitor cells by ectopic expression of scleraxis. Stem Cells Dev, 2012, 21(6): 846-858.
4. Yukata K, Matsui Y, Shukunami C, et al. Differential expression of Tenomodulin and Chondromodulin-1 at the insertion site of the tendon reflects a phenotypic transition of the resident cells. Tissue Cell, 2010, 42(2): 116-120.
5. Backman LJ, Fong G, Andersson G, et al. Substance P is a mechanoresponsive, autocrine regulator of human tenocyte proliferation. PLoS One, 2011, 6(11): e27209.
6. Kishore V, Bullock W, Sun X, et al. Tenogenic differentiation of human MSCs induced by the topography of electrochemically aligned collagen threads. Biomaterials, 2012, 33(7): 2137-2144.
7. Shukunami C, Oshima Y, Hiraki Y. Molecular cloning of tenomodulin, a novel chondromodulin-I related gene. Biochem Biophys Res Commun, 2001, 280(5): 1323-1327.
8. Oshima Y, Sato K, Tashiro F, et al. Anti-angiogenic action of the C-terminal domain of tenomodulin that shares homology with chondromodulin-I. J Cell Sci, 2004, 117(Pt 13): 2731-2744.
9. Sánchez-Pulido L, Devos D, Valencia A. BRICHOS: a conserved domain in proteins associated with dementia, respiratory distress and cancer. Trends Biochem Sci, 2002, 27(7): 329-332.
10. Aslan H, Kimelman-Bleich N, Pelled G, et al. Molecular targets for tendon neoformation. J Clin Invest, 2008, 118(2): 439-444.
11. Shukunami C, Takimoto A, Miura S, et al. Chondromodulin-I and tenomodulin are differentially expressed in the avascular mesenchyme during mouse and chick development. Cell Tissue Res, 2008, 332(1): 111-122.
12. Shukunami C, Takimoto A, Oro M, et al. Scleraxis positively regulates the expression of tenomodulin, a differentiation marker of tenocytes. Dev Biol, 2006, 298(1): 234-247.
13. Docheva D, Hunziker EB, Fässler R, et al. Tenomodulin is necessary for tenocyte proliferation and tendon maturation. Mol Cell Biol, 2005, 25(2): 699-705.
14. Watahiki J, Yamaguchi T, Enomoto A, et al. Identification of differentially expressed genes in mandibular condylar and tibial growth cartilages using laser microdissection and fluorescent differential display: chondromodulin-I (ChM-1) and tenomodulin (TeM) are differentially expressed in mandibular condylar and other growth cartilages. Bone, 2008, 42(6): 1053-1060.
15. Pisani DF, Pierson PM, Massoudi A, et al. Myodulin is a novel potential angiogenic factor in skeletal muscle. Exp Cell Res, 2004, 292(1): 40-50.
16. Shukunami C, Hiraki Y. Chondromodulin-I and tenomodulin: the negative control of angiogenesis in connective tissue. Curr Pharm Des, 2007, 13(20): 2101-2112.
17. Kimura N, Shukunami C, Hakuno D, et al. Local tenomodulin absence, angiogenesis, and matrix metalloproteinase activation are associated with the rupture of the chordae tendineae cordis. Circulation, 2008, 118(17): 1737-1747.
18. Hiraki Y, Shukunami C. Angiogenesis inhibitors localized in hypovascular mesenchymal tissues: chondromodulin-I and tenomodulin. Connect Tissue Res, 2005, 46(1): 3-11.
19. Lorda-Diez CI, Montero JA, Martinez-Cue C, et al. Transforming growth factors beta coordinate cartilage and tendon differentiation in the developing limb mesenchyme. J Biol Chem, 2009, 284(43): 29988-29996.
20. Schneider PR, Buhrmann C, Mobasheri A, et al. Three-dimensional high-density co-culture with primary tenocytes induces tenogenic differentiation in mesenchymal stem cells. J Orthop Res, 2011, 29(9): 1351-1360.
21. Liu W, Watson SS, Lan Y, et al. The atypical homeodomain transcription factor Mohawk controls tendon morphogenesis. Mol Cell Biol, 2010, 30(20): 4797-4807.
22. Inoue M, Ebisawa K, Itaya T, et al. Effect of GDF-5 and BMP-2 on the expression of tendo/ligamentogenesis-related markers in human PDL-derived cells. Oral Dis, 2012, 18(2): 206-212.
23. Park A, Hogan MV, Kesturu GS, et al. Adipose-derived mesenchymal stem cells treated with growth differentiation factor-5 express tendon-specific markers. Tissue Eng Part A, 2010, 16(9): 2941-2951.
24. Haddad-Weber M, Prager P, Kunz M, et al. BMP12 and BMP13 gene transfer induce ligamentogenic differentiation in mesenchymal progenitor and anterior cruciate ligament cells. Cytotherapy, 2010, 12(4): 505-513.
25. Violini S, Ramelli P, Pisani LF, et al. Horse bone marrow mesenchymal stem cells express embryo stem cell markers and show the ability for tenogenic differentiation by in vitro exposure to BMP-12. BMC Cell Biol, 2009, 10: 29.
26. 倪明, 芮云峰, 陈启明, 等. 生长分化因子7体外促进BMSCs向肌腱细胞分化的研究. 中国修复重建外科杂志, 2011, 25(9): 1103-1109.
27. Lee JY, Zhou Z, Taub PJ, et al. BMP-12 treatment of adult mesenchymal stem cells in vitro augments tendon-like tissue formation and defect repair in vivo. PloS One, 2011, 6(3): e17531.
28. Mendias CL, Bakhurin KI, Faulkner JA. Tendons of myostatin-deficient mice are small, brittle, and hypocellular. Proc Natl Acad Sci U S A, 2008, 105(1): 388-393.
29. Engler AJ, Sen S, Sweeney HL, et al. Matrix elasticity directs stem cell lineage specification. Cell, 2006, 126(4): 677-689.
30. Kilian KA, Bugarija B, Lahn BT, et al. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci U S A, 2010, 107(11): 4872-4877.
31. Kishore V, Bullock W, Sun X, et al. Tenogenic differentiation of human MSCs induced by the topography of electrochemically aligned collagen threads. Biomaterials, 2012, 33(7): 2137-2144.
32. Omae H, Zhao C, Sun YL, et al. Multilayer tendon slices seeded with bone marrow stromal cells: a novel composite for tendon engineering. J Orthop Res, 2009, 27(7): 937-942.
33. Omae H, Sun YL, An KN, et al. Engineered tendon with decellularized xenotendon slices and bone marrow stromal cells: an in vivo animal study. J Tissue Eng Regen Med, 2012, 6(3): 238-244.
34. Bashur CA, Shaffer RD, Dahlgren LA, et al. Effect of fiber diameter and alignment of electrospun polyurethane meshes on mesenchymal progenitor cells. Tissue Eng Part A, 2009, 15(9): 2435-2445.
35. Zhu J, Li J, Wang B, et al. The regulation of phenotype of cultured tenocytes by microgrooved surface structure. Biomaterials, 2010, 31(27): 6952-6958.
36. Eliasson P, Andersson T, Aspenberg P. Rat Achilles tendon healing: mechanical loading and gene expression. J Appl Physiol, 2009, 107(2): 399-407.
37. Mendias CL, Gumucio JP, Bakhurin KI, et al. Physiological loading of tendons induces scleraxis expression in epitenon fibroblasts. J Orthop Res, 2012, 30(4): 606-612.
38. 廖梅旭, 宁良菊, 陈晓禾, 等. 应变诱导BMSCs腱向分化的实验研究. 中国修复重建外科杂志, 2010, 24(7): 817-821.
39. Tan Q, Lui PP, Rui YF. Effect of in vitro passaging on the stem cell-related properties of tendon-derived stem cells-implications in tissue engineering. Stem Cells Dev, 2012, 21(5): 790-800.
40. Mazzocca AD, Chowaniec D, McCarthy MB, et al. In vitro changes in human tenocyte cultures obtained from proximal biceps tendon: multiple passages result in changes in routine cell markers. Knee Surg Sports Traumatol Arthrosc, 2012, 20(9): 1666-1672.

Chinese Journal of Reparative and Reconstructive Surgery

CURRENT SITUATION AND PROSPECT OF Tenomodulin IN TENDON TISSUE ENGINEERING

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