A Role for Hedgehog Signaling in the Differentiation of the Insertion Site of the Patellar Tendon in the Mouse

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Liu, Chia Feng ^a   Breidenbach, Andrew ^b   Aschbacher Smith, Lindsey ^a   Butler, David ^b   Wylie, Christopher ^a  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b 705 Engineering Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULAR MARKER; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; CARTILAGE; CELL CULTURE; CELL POPULATION; CHONDROGENESIS; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FIBROCARTILAGINOUS INSERTION SITE; GENE EXPRESSION; GENE TARGETING; GENETIC RECOMBINATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MINERALIZATION; MOUSE; MUSCLE RIGIDITY; NONHUMAN; PATELLA TENDON; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SMO GENE; TENDON DISEASE; TISSUE DIFFERENTIATION; TISSUE STRUCTURE; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOSKELETAL PROTEINS; FEMALE; FIBROCARTILAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; IMMUNOENZYME TECHNIQUES; INTEGRASES; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MICE; MICE, KNOCKOUT; MUSCLE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN CULTURE TECHNIQUES; PATELLAR LIGAMENT; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION;

ERINACEIDAE; MURINAE;

EID: 84878885793     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065411     Document Type: Article

References (40)

1. Sharma P, Maffulli N, (2006) Biology of tendon injury: healing, modeling and remodeling. Journal of musculoskeletal & neuronal interactions 6: 181-190.
2. Benjamin M, McGonagle D, (2009) Entheses: tendon and ligament attachment sites. Scand J Med Sci Sports 19: 520-527.
3. Wang M, Vanhouten JN, Nasiri AR, Johnson RL, Broadus AE (2012) PTHrP regulates the modeling of cortical bone surfaces at fibrous insertion sites during growth. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research.
4. Liu CF, Aschbacher-Smith L, Barthelery NJ, Dyment N, Butler D, et al. (2012) Spatial and temporal expression of molecular markers and cell signals during normal development of the mouse patellar tendon. Tissue engineering Part A 18: 598-608.
5. Ingham PW, McMahon AP, (2001) Hedgehog signaling in animal development: paradigms and principles. Genes & development 15: 3059-3087.
6. Ehlen HW, Buelens LA, Vortkamp A, (2006) Hedgehog signaling in skeletal development. Birth defects research Part C, Embryo today: reviews 78: 267-279.
7. Ahn S, Joyner AL, (2004) Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 118: 505-516.
8. Bai CB, Auerbach W, Lee JS, Stephen D, Joyner AL, (2002) Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129: 4753-4761.
9. Gu Y, Runyan C, Shoemaker A, Surani A, Wylie C, (2009) Steel factor controls primordial germ cell survival and motility from the time of their specification in the allantois, and provides a continuous niche throughout their migration. Development 136: 1295-1303.
10. Gu Y, Runyan C, Shoemaker A, Surani MA, Wylie C, (2011) Membrane-bound steel factor maintains a high local concentration for mouse primordial germ cell motility, and defines the region of their migration. PloS one 6: e25984.
11. Krull CE, Kulesa PM, (1998) Embryonic explant and slice preparations for studies of cell migration and axon guidance. Current topics in developmental biology 36: 145-159.
12. Molyneaux KA, Stallock J, Schaible K, Wylie C, (2001) Time-lapse analysis of living mouse germ cell migration. Developmental biology 240: 488-498.
13. Dahia CL, Mahoney E, Wylie C, (2012) Shh signaling from the nucleus pulposus is required for the postnatal growth and differentiation of the mouse intervertebral disc. PloS one 7: e35944.
14. Benjamin M, Ralphs JR, (2000) The cell and developmental biology of tendons and ligaments. Int Rev Cytol 196: 85-130.
15. Berman DM, Karhadkar SS, Hallahan AR, Pritchard JI, Eberhart CG, et al. (2002) Medulloblastoma growth inhibition by hedgehog pathway blockade. Science 297: 1559-1561.
16. Pacifici M, Iwamoto M, Golden EB, Leatherman JL, Lee YS, et al. (1993) Tenascin is associated with articular cartilage development. Developmental dynamics: an official publication of the American Association of Anatomists 198: 123-134.
17. Roughley PJ, Melching LI, Recklies AD, (1994) Changes in the expression of decorin and biglycan in human articular cartilage with age and regulation by TGF-beta. Matrix biology: journal of the International Society for Matrix Biology 14: 51-59.
18. Chiquet-Ehrismann R, Tucker RP, (2004) Connective tissues: signalling by tenascins. The international journal of biochemistry & cell biology 36: 1085-1089.
19. Eliasson P, Andersson T, Aspenberg P, (2009) Rat Achilles tendon healing: mechanical loading and gene expression. Journal of applied physiology 107: 399-407.
20. Waggett AD, Ralphs JR, Kwan AP, Woodnutt D, Benjamin M, (1998) Characterization of collagens and proteoglycans at the insertion of the human Achilles tendon. Matrix biology: journal of the International Society for Matrix Biology 16: 457-470.
21. Butler DL, Sheh MY, Stouffer DC, Samaranayake VA, Levy MS, (1990) Surface strain variation in human patellar tendon and knee cruciate ligaments. Journal of biomechanical engineering 112: 38-45.
22. Koyama E, Leatherman JL, Noji S, Pacifici M, (1996) Early chick limb cartilaginous elements possess polarizing activity and express hedgehog-related morphogenetic factors. Developmental dynamics: an official publication of the American Association of Anatomists 207: 344-354.
23. Vortkamp A, Lee K, Lanske B, Segre GV, Kronenberg HM, et al. (1996) Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273: 613-622.
24. St-Jacques B, Hammerschmidt M, McMahon AP, (1999) Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes & development 13: 2072-2086.
25. Karp SJ, Schipani E, St-Jacques B, Hunzelman J, Kronenberg H, et al. (2000) Indian hedgehog coordinates endochondral bone growth and morphogenesis via parathyroid hormone related-protein-dependent and-independent pathways. Development 127: 543-548.
26. Pamela K Levangie, Norkin CC (2005) Joint Structure & Function. Philadelphia: F.A.Davis Company.
27. Lin AC, Seeto BL, Bartoszko JM, Khoury MA, Whetstone H, et al. (2009) Modulating hedgehog signaling can attenuate the severity of osteoarthritis. Nature medicine 15: 1421-1425.
28. Dwyer JR, Sever N, Carlson M, Nelson SF, Beachy PA, et al. (2007) Oxysterols are novel activators of the hedgehog signaling pathway in pluripotent mesenchymal cells. The Journal of biological chemistry 282: 8959-8968.
29. Chang CF, Ramaswamy G, Serra R, (2012) Depletion of primary cilia in articular chondrocytes results in reduced Gli3 repressor to activator ratio, increased Hedgehog signaling, and symptoms of early osteoarthritis. Osteoarthritis and cartilage/OARS, Osteoarthritis Research Society 20: 152-161.
30. Steinert AF, Weissenberger M, Kunz M, Gilbert F, Ghivizzani SC, et al. (2012) Indian hedgehog gene transfer is a chondrogenic inducer of human mesenchymal stem cells. Arthritis research & therapy 14: R168.
31. Liu CF, Aschbacher-Smith L, Barthelery NJ, Dyment N, Butler D, et al. (2011) What we should know before using tissue engineering techniques to repair injured tendons: a developmental biology perspective. Tissue engineering Part B, Reviews 17: 165-176.
32. Kronenberg HM, (2003) Developmental regulation of the growth plate. Nature 423: 332-336.
33. Blitz E, Viukov S, Sharir A, Shwartz Y, Galloway JL, et al. (2009) Bone ridge patterning during musculoskeletal assembly is mediated through SCX regulation of Bmp4 at the tendon-skeleton junction. Dev Cell 17: 861-873.
34. Jeong J, Mao J, Tenzen T, Kottmann AH, McMahon AP, (2004) Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes & development 18: 937-951.
35. Xie J, Murone M, Luoh SM, Ryan A, Gu Q, et al. (1998) Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 391: 90-92.
36. Pryce BA, Brent AE, Murchison ND, Tabin CJ, Schweitzer R, (2007) Generation of transgenic tendon reporters, ScxGFP and ScxAP, using regulatory elements of the scleraxis gene. Dev Dyn 236: 1677-1682.
37. Kwan KM, (2002) Conditional alleles in mice: practical considerations for tissue-specific knockouts. Genesis 32: 49-62.
38. Lazarenko OP, Rzonca SO, Suva LJ, Lecka-Czernik B, (2006) Netoglitazone is a PPAR-gamma ligand with selective effects on bone and fat. Bone 38: 74-84.
39. Dyment NA, Kazemi N, Aschbacher-Smith LE, Barthelery NJ, Kenter K, et al. (2012) The relationships among spatiotemporal collagen gene expression, histology, and biomechanics following full-length injury in the murine patellar tendon. Journal of orthopaedic research: official publication of the Orthopaedic Research Society 30: 28-36.
40. Brunskill EW, Potter SS, (2012) RNA-Seq defines novel genes, RNA processing patterns and enhancer maps for the early stages of nephrogenesis: Hox supergenes. Developmental biology 368: 4-17.