Primary cilia modulate Ihh signal transduction in response to hydrostatic loading of growth plate chondrocytes

Bone

Volumn 50, Issue 1, 2012, Pages 79-84

  Shao, Yvonne Y ^a   Wang, Lai ^a   Welter, Jean F ^b   Ballock, R Tracy ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Growth plate chondrocyte; Hydrostatic compression; Indian hedgehog; Primary cilium

Indexed keywords

CHLORAL HYDRATE; LUCIFERASE; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOMECHANICS; CARTILAGE CELL; CELL STRUCTURE; COMPRESSION; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; GENE EXPRESSION; GROWTH PLATE; HYDROSTATIC COMPRESSION; MECHANICAL STRESS; NONHUMAN; PRIMARY CILIA; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CHONDROCYTES; CILIA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH PLATE; HEDGEHOG PROTEINS; HYDROSTATIC PRESSURE; MECHANOTRANSDUCTION, CELLULAR; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; STRESS, MECHANICAL;

EID: 80054742150     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2011.08.033     Document Type: Article

References (54)

1. Wilkins R.J., Browning J.A., Urban J.P. Chondrocyte regulation by mechanical load. Biorheology 2000, 37:67-74.
2. Hall A.C., Urban J.P., Gehl K.A. The effects of hydrostatic pressure on matrix synthesis in articular cartilage. J Orthop Res 1991, 9:1-10.
3. Buschmann M.D., Gluzband Y.A., Grodzinsky A.J., Hunziker E.B. Mechanical compression modulates matrix biosynthesis in chondrocyte/agarose culture. J Cell Sci 1995, 108(Pt 4):1497-1508.
4. Toyoda T., Seedhom B.B., Yao J.Q., Kirkham J., Brookes S., Bonass W.A. Hydrostatic pressure modulates proteoglycan metabolism in chondrocytes seeded in agarose. Arthritis Rheum 2003, 48:2865-2872.
5. Radomisli T.E., Moore D.C., Barrach H.J., Keeping H.S., Ehrlich M.G. Weight-bearing alters the expression of collagen types I and II, BMP 2/4 and osteocalcin in the early stages of distraction osteogenesis. J Orthop Res 2001, 19:1049-1056.
6. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996, 273:613-622.
7. Kobayashi T., Chung U.I., Schipani E., Starbuck M., Karsenty G., Katagiri T., et al. PTHrP and Indian hedgehog control differentiation of growth plate chondrocytes at multiple steps. Development 2002, 129:2977-2986.
8. St-Jacques B., Hammerschmidt M., McMahon A.P. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 1999, 13:2072-2086.
9. Long F., Zhang X.M., Karp S., Yang Y., McMahon A.P. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 2001, 128:5099-5108.
10. Rohatgi R., Milenkovic L., Scott M.P. Patched1 regulates hedgehog signaling at the primary cilium. Science 2007, 317:372-376.
11. Matise M.P., Joyner A.L. Gli genes in development and cancer. Oncogene 1999, 18:7852-7859.
12. Rohatgi R., Scott M.P. Patching the gaps in Hedgehog signalling. Nat Cell Biol 2007, 9:1005-1009.
13. Taipale J., Chen J.K., Cooper M.K., Wang B., Mann R.K., Milenkovic L., et al. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 2000, 406:1005-1009.
14. Chen J.K., Taipale J., Cooper M.K., Beachy P.A. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev 2002, 16:2743-2748.
15. May S.R., Ashique A.M., Karlen M., Wang B., Shen Y., Zarbalis K., et al. Loss of the retrograde motor for IFT disrupts localization of Smo to cilia and prevents the expression of both activator and repressor functions of Gli. Dev Biol 2005, 287:378-389.
16. Song B., Haycraft C.J., Seo H.S., Yoder B.K., Serra R. Development of the post-natal growth plate requires intraflagellar transport proteins. Dev Biol 2007, 305:202-216.
17. McGlashan S.R., Haycraft C.J., Jensen C.G., Yoder B.K., Poole C.A. Articular cartilage and growth plate defects are associated with chondrocyte cytoskeletal abnormalities in Tg737orpk mice lacking the primary cilia protein polaris. Matrix Biol 2007, 26:234-246.
18. Haycraft C.J., Zhang Q., Song B., Jackson W.S., Detloff P.J., Serra R., et al. Intraflagellar transport is essential for endochondral bone formation. Development 2007, 134:307-316.
19. Corbit K.C., Aanstad P., Singla V., Norman A.R., Stainier D.Y., Reiter J.F. Vertebrate Smoothened functions at the primary cilium. Nature 2005, 437:1018-1021.
20. Praetorius H.A., Spring K.R. Removal of the MDCK cell primary cilium abolishes flow sensing. J Membr Biol 2003, 191:69-76.
21. 2+ and cAMP signaling. Gastroenterology 2006, 131:911-920.
22. Pazour G.J., Dickert B.L., Vucica Y., Seeley E.S., Rosenbaum J.L., Witman G.B., et al. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J Cell Biol 2000, 151:709-718.
23. Moyer J.H., Lee-Tischler M.J., Kwon H.Y., Schrick J.J., Avner E.D., Sweeney W.E., et al. Candidate gene associated with a mutation causing recessive polycystic kidney disease in mice. Science 1994, 264:1329-1333.
24. Ballock R.T., Heydemann A., Wakefield L.M., Flanders K.C., Roberts A.B., Sporn M.B. TGF-beta 1 prevents hypertrophy of epiphyseal chondrocytes: regulation of gene expression for cartilage matrix proteins and metalloproteases. Dev Biol 1993, 158:414-429.
25. Rasband W. Image J 1997-2011, U.S. National Institutes of Health, Bethesda, MD.
26. Hueter C. Anatomische Studien an den Extremitätengelenken Neugeborener und Erwachsener. Virchows Arch Pathol Anat Physiol Klin Med 1862, 26:484-519.
27. Ehrlich M.G., Mankin H.J., Treadwell B.V. Biochemical and physiological events during closure of the stapled distal femoral epiphyseal plate in rats. J Bone Joint Surg Am 1972, 54:309-322.
28. Herwig J., Schmidt A., Matthiab H.H., Kleemann H., Buddecke E. Biochemical events during stapling of the proximal tibial epiphyseal plate in pigs. Clin Orthop Relat Res 1987, 283-289.
29. Frost H.M. Skeletal structural adaptations to mechanical usage (SATMU): 3. The hyaline cartilage modeling problem. Anat Rec 1990, 226:423-432.
30. Mankin K.P., Zaleske D.J. Response of physeal cartilage to low-level compression and tension in organ culture. J Pediatr Orthop 1998, 18:145-148.
31. Wilson-MacDonald J., Houghton G.R., Bradley J., Morscher E. The relationship between periosteal division and compression or distraction of the growth plate. An experimental study in the rabbit. J Bone Joint Surg Br 1990, 72:303-308.
32. Alberty A., Peltonen J. Proliferation of the hypertrophic chondrocytes of the growth plate after physeal distraction. An experimental study in rabbits. Clin Orthop Relat Res 1993, 7-11.
33. Farnum C.E., Nixon A., Lee A.O., Kwan D.T., Belanger L., Wilsman N.J. Quantitative three-dimensional analysis of chondrocytic kinetic responses to short-term stapling of the rat proximal tibial growth plate. Cells Tissues Organs 2000, 167:247-258.
34. Reich A., Jaffe N., Tong A., Lavelin I., Genina O., Pines M., et al. Weight loading young chicks inhibits bone elongation and promotes growth plate ossification and vascularization. J Appl Physiol 2005, 98:2381-2389.
35. Yang X., Vezeridis P.S., Nicholas B., Crisco J.J., Moore D.C., Chen Q. Differential expression of type X collagen in a mechanically active 3-D chondrocyte culture system: a quantitative study. J Orthop Surg Res 2006, 1:15.
36. Cassino T.R., Anderson R., Love B.J., Huckle W.R., Seamans D.K., Forsten-Williams K. Design and application of an oscillatory compression device for cell constructs. Biotechnol Bioeng 2007, 98:211-220.
37. Hauselmann H.J., Masuda K., Hunziker E.B., Neidhart M., Mok S.S., Michel B.A., et al. Adult human chondrocytes cultured in alginate form a matrix similar to native human articular cartilage. Am J Physiol 1996, 271:C742-C752.
38. Toyoda T., Seedhom B.B., Kirkham J., Bonass W.A. Upregulation of aggrecan and type II collagen mRNA expression in bovine chondrocytes by the application of hydrostatic pressure. Biorheology 2003, 40:79-85.
39. Ballock R.T., Zhou X., Mink L.M., Chen D.H., Mita B.C. Both retinoic acid and 1,25(OH)2 vitamin D3 inhibit thyroid hormone-induced terminal differentiation of growth plate chondrocytes. J Orthop Res 2001, 19:43-49.
40. Tang G.H., Rabie A.B., Hagg U. Indian hedgehog: a mechanotransduction mediator in condylar cartilage. J Dent Res 2004, 83:434-438.
41. Wu Q., Zhang Y., Chen Q. Indian hedgehog is an essential component of mechanotransduction complex to stimulate chondrocyte proliferation. J Biol Chem 2001, 276:35290-35296.
42. Eggenschwiler J.T., Anderson K.V. Cilia and developmental signaling. Annu Rev Cell Dev Biol 2007, 23:345-373.
43. Christensen S.T., Pedersen L.B., Schneider L., Satir P. Sensory cilia and integration of signal transduction in human health and disease. Traffic 2007, 8:97-109.
44. Oro A.E. The primary cilia, a 'Rab-id' transit system for hedgehog signaling. Curr Opin Cell Biol 2007, 19:691-696.
45. Singla V., Reiter J.F. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 2006, 313:629-633.
46. Haycraft C.J., Banizs B., Aydin-Son Y., Zhang Q., Michaud E.J., Yoder B.K. Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet 2005, 1:e53.
47. Koyama E., Young B., Nagayama M., Shibukawa Y., Enomoto-Iwamoto M., Iwamoto M., et al. Conditional Kif3a ablation causes abnormal hedgehog signaling topography, growth plate dysfunction, and excessive bone and cartilage formation during mouse skeletogenesis. Development 2007, 134:2159-2169.
48. Ruiz-Perez V.L., Blair H.J., Rodriguez-Andres M.E., Blanco M.J., Wilson A., Liu Y.N., et al. Evc is a positive mediator of Ihh-regulated bone growth that localises at the base of chondrocyte cilia. Development 2007, 134:2903-2912.
49. Blair H.J., Tompson S., Liu Y.N., Campbell J., MacArthur K., Ponting C.P., et al. Evc2 is a positive modulator of Hedgehog signalling that interacts with Evc at the cilia membrane and is also found in the nucleus. BMC Biol 2011, 9:14.
50. Jensen C.G., Poole C.A., McGlashan S.R., Marko M., Issa Z.I., Vujcich K.V., et al. Ultrastructural, tomographic and confocal imaging of the chondrocyte primary cilium in situ. Cell Biol Int 2004, 28:101-110.
51. Malone A.M., Anderson C.T., Tummala P., Kwon R.Y., Johnston T.R., Stearns T., et al. Primary cilia mediate mechanosensing in bone cells by a calcium-independent mechanism. Proc Natl Acad Sci USA 2007, 104:13325-13330.
52. McGlashan S.R., Knight M.M., Chowdhury T.T., Joshi P., Jensen C.G., Kennedy S., et al. Mechanical loading modulates chondrocyte primary cilia incidence and length. Cell Biol Int 2010, 34:441-446.
53. McGlashan S.R., Cluett E.C., Jensen C.G., Poole C.A. Primary cilia in osteoarthritic chondrocytes: from chondrons to clusters. Dev Dyn 2008, 237:2013-2020.
54. Kennedy J.R., Brittingham E. Fine structure changes during chloral hydrate deciliation of Paramecium caudatum. J Ultrastruct Res 1968, 22:530-545.