Ablating hedgehog signaling in tenocytes during development impairs biomechanics and matrix organization of the adult murine patellar tendon enthesis

Journal of Orthopaedic Research

Volumn 33, Issue 8, 2015, Pages 1142-1151

  Breidenbach, Andrew P ^a   Aschbacher Smith, Lindsey ^b   Lu, Yinhui ^c   Dyment, Nathaniel A ^d   Liu, Chia Feng ^e   Liu, Han ^b   Wylie, Chris ^b   Rao, Marepalli ^a   Shearn, Jason T ^a   Rowe, David W ^d   Kadler, Karl E ^c   Jiang, Rulang ^b   Butler, David L ^a  

^a 705 Engineering Research Center   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF CONNECTICUT   (United States)

^e LERNER RESEARCH INSTITUTE   (United States)

Author keywords

enthesis; fibrocartilage; hedgehog; mineralization; serial block face scanning electron microscopy; tendon mechanics

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BONE MINERALIZATION; CELLS BY BODY ANATOMY; COLLAGEN FIBER; CONTROLLED STUDY; FIBROCARTILAGE; FRACTURE HEALING; HEDGEHOG PATHWAY; MALE; MOUSE; NONHUMAN; PATELLA LIGAMENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TENOCYTE; ANIMAL; CONNECTIVE TISSUE; CYTOLOGY; KNOCKOUT MOUSE; PATELLA; PHYSIOLOGY; TENDON;

SONIC HEDGEHOG PROTEIN;

ANIMALS; BIOMECHANICAL PHENOMENA; CONNECTIVE TISSUE; HEDGEHOG PROTEINS; MALE; MICE; MICE, KNOCKOUT; PATELLA; SIGNAL TRANSDUCTION; TENDONS;

EID: 84936846054     PISSN: 07360266     EISSN: 1554527X     Source Type: Journal    
DOI: 10.1002/jor.22899     Document Type: Article

References (40)

1. Salmon L, Russell V, Musgrove T, Pinczewski L, Refshauge K,. 2005. Incidence and risk factors for graft rupture and contralateral rupture after anterior cruciate ligament reconstruction. Arthroscopy 21: 948-957.
2. Juncosa-Melvin N, Shearn JT, Boivin GP, et al., 2006. Effects of mechanical stimulation on the biomechanics and histology of stem cell-collagen sponge constructs for rabbit patellar tendon repair. Tissue Eng A 12: 2291-2300.
3. Kinneberg KRC, Galloway MT, Butler DL, et al., 2012. The native cell population does not contribute to central-third graft healing at 6, 12, or 26 weeks in the rabbit patellar tendon. J Orthop Res 31: 638-644.
4. Kinneberg KRC, Galloway MT, Butler DL, et al., 2011. Effect of implanting a soft tissue autograft in a central-third patellar tendon defect: biomechanical and histological comparisons. J Biomech Eng 133: 091002.
5. Benjamin M, Kaiser E, Milz S,. 2008. Structure-function relationships in tendons: a review. J Anat 212: 211-228.
6. Woo SL, Buckwalter JA,. 1988. Injury and repair of the musculoskeletal soft tissues. Savannah, Georgia, June 18-20, 1987. J Orthop Res 6: 907-931.
7. Thomopoulos S, Williams GR, Gimbel JA, et al., 2003. Variation of biomechanical, structural, and compositional properties along the tendon to bone insertion site. J Orthop Res 21: 413-419.
8. Schwartz AG, Pasteris JD, Genin GM, et al., 2012. Mineral distributions at the developing tendon enthesis. PLoS ONE 7: e48630.
9. Thomopoulos S, Marquez JP, Weinberger B, et al., 2006. Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations. J Biomech 39: 1842-1851.
10. Dyment NA, Kazemi N, Aschbacher-Smith L, et al., 2012. The relationships among spatiotemporal collagen gene expression, histology, and biomechanics following full-length injury in the murine patellar tendon. J Orthop Res 30: 28-36.
11. Silva MJ, Thomopoulos S, Kusano N, et al., 2006. Early healing of flexor tendon insertion site injuries: tunnel repair is mechanically and histologically inferior to surface repair in a canine model. J Orthop Res 24: 990-1000.
12. Gilday SD, Chris Casstevens E, Kenter K, et al., 2014. Murine patellar tendon biomechanical properties and regional strain patterns during natural tendon-to-bone healing after acute injury. J Biomech 47: 2035-2042.
13. Liu C, Aschbacher-Smith L, Bathelery NJ, et al., 2012. Spatial and temporal expression of molecular markers and cell signals during normal development of the mouse patellar tendon. Tissue Eng A 18: 598-608.
14. Liu C, Breidenbach A, Aschbacher-Smith L, et al., 2013. A role for hedgehog signaling in the differentiation of the insertion site of the patellar tendon in the mouse. PLoS ONE 8: e65411.
15. Xie J, Murone M, Luoh SM, et al., 1998. Activating smoothened mutations in sporadic basal-cell carcinoma. Nature 391: 90-92.
16. Pryce BA, Watson SS, Murchison ND, et al., 2009. Recruitment and maintenance of tendon progenitors by TGFbeta signaling are essential for tendon formation. Development 136: 1351-1361.
17. Schweitzer R, Chyung JH, Murtaugh LC, et al., 2001. Analysis of the tendon cell fate using scleraxis, a specific marker for tendons and ligaments. Development 128: 3855-3866.
18. Dyment NA, Liu C, Kazemi N, et al., 2013. The paratenon contributes to scleraxis-expressing cells during patellar tendon healing. PLoS ONE 8: e59944.
19. Dourte LM, Pathmanathan L, Jawad AF, et al., 2012. Influence of decorin on the mechanical, compositional, and structural properties of the mouse patellar tendon. J Biomech Eng 134: 031005.
20. R Core Team,. 2013. R: a language and environment for statistical computing. http://www.R-project.org/
21. Chambers JM, Hastie TJ,. 1993. Chapter 7: generalized additive models. Statistical models in S. New York: Chapman & Hall.
22. Ushiku C, Adams DJ, Jiang X, et al., 2010. Long bone fracture repair in mice harboring GFP reporters for cells within the osteoblastic lineage. J Orthop Res 28: 1338-1347.
23. Chen X, Nadiarynkh O, Plotnikov S, et al., 2012. Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure. Nat Protoc 7: 654-669.
24. Schindelin J, Arganda-Carreras I, Frise E, et al., 2012. Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676-682.
25. Starborg T, Kalson NS, Lu Y, et al., 2013. Using transmission electron microscopy and 3View to determine collagen fibril size and three-dimensional organization. Nat Protoc 8: 1433-1448.
26. Kremer JR, Mastronarde DN, McIntosh JR,. 1996. Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71-76.
27. Starborg T, Lu Y, Kadler KE, et al., 2008. Chapter 17 electron microscopy of collagen fibril structure in vitro and in vivo including three-dimensional reconstruction. pp 319-345.
28. Korvick DL, Cummings JF, Grood ES, et al., 1996. The use of an implantable force transducer to measure patellar tendon forces in goats. J Biomech 29: 557-561.
29. Juncosa N, West JR, Galloway MT, et al., 2003. In vivo forces used to develop design parameters for tissue engineered implants for rabbit patellar tendon repair. J Biomech 36: 483-488.
30. Jiang J, Leong NL, Mung JC, et al., 2008. Interaction between zonal populations of articular chondrocytes suppresses chondrocyte mineralization and this process is mediated by PTHrP. Osteoarthr Cartil 16: 70-82.
31. Chen X, Macica CM, Nasiri A, et al., 2008. Regulation of articular chondrocyte proliferation and differentiation by indian hedgehog and parathyroid hormone-related protein in mice. Arthritis Rheum 58: 3788-3797.
32. Lenton K, James AW, Manu A, et al., 2011. Indian hedgehog positively regulates calvarial ossification and modulates bone morphogenetic protein signaling. Genesis 49: 784-796.
33. St-Jacques B, Hammerschmidt M, McMahon AP,. 1999. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 13: 2072-2086.
34. Kobayashi T, Chung U, Schipani E, et al., 2002. PTHrP and indian hedgehog control differentiation of growth plate chondrocytes at multiple steps. Development 129: 2977-2986.
35. Mak KK, Kronenberg HM, Chuang P, et al., 2008. Indian hedgehog signals independently of PTHrP to promote chondrocyte hypertrophy. Development 135: 1947-1956.
36. Mackie EJ, Ahmed YA, Tatarczuch L, et al., 2008. Endochondral ossification: how cartilage is converted into bone in the developing skeleton. Int J Biochem Cell Biol 40: 46-62.
37. Chen X, Macica CM, Dreyer BE, et al., 2006. Initial characterization of PTH-related protein gene-driven lacZ expression in the mouse. J Bone Miner Res 21: 113-123.
38. Wang M, VanHouten JN, Nasiri AR, et al., 2013. PTHrP regulates the modeling of cortical bone surfaces at fibrous insertion sites during growth. J Bone Miner Res 28: 598-607.
39. Benjamin M, Rufai A, Ralphs JR,. 2000. The mechanism of formation of bony spurs (enthesophytes) in the achilles tendon. Arthritis Rheum 43: 576-583.
40. Breidenbach AP, Gilday SD, Lalley AL, et al., 2013. Functional tissue engineering of tendon: establishing biological success criteria for improving tendon repair. J Biomech 47: 1941-1948.