The growth plate's response to load is partially mediated by mechano-sensing via the chondrocytic primary cilium

Cellular and Molecular Life Sciences

Volumn 72, Issue 3, 2015, Pages 597-615

  Rais, Yoach ^a   Reich, Adi ^a,b   Simsa Maziel, Stav ^a   Moshe, Maya ^a   Idelevich, Anna ^a   Kfir, Tal ^a   Miosge, Nicolai ^c   Monsonego Ornan, Efrat ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Aggrecan; Cartilage; Collagen; IFT88; Osteopontin; PKD

Indexed keywords

PARATHYROID HORMONE RELATED PROTEIN; PRIMER DNA; SONIC HEDGEHOG PROTEIN;

ANALYSIS OF VARIANCE; ANIMAL; BIOMECHANICS; CARTILAGE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CHICKEN; EUKARYOTIC FLAGELLUM; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; GROWTH PLATE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MECHANOTRANSDUCTION; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; STIMULATION; ULTRASTRUCTURE;

ANALYSIS OF VARIANCE; ANIMALS; BIOMECHANICAL PHENOMENA; CELL DIFFERENTIATION; CELL PROLIFERATION; CHICKENS; CHONDROCYTES; CILIA; DNA PRIMERS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GROWTH PLATE; HEDGEHOG PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MECHANOTRANSDUCTION, CELLULAR; MICROSCOPY, ELECTRON, SCANNING; PARATHYROID HORMONE-RELATED PROTEIN; PHYSICAL STIMULATION; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84925032088     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1690-4     Document Type: Article

References (87)

1. Atsumi T, Miwa Y, Kimata K, Ikawa Y (1990) A chondrogenic cell line derived from a differentiating culture of AT805 teratocarcinoma cells. Cell Differ Dev 30(2):109-116
2. Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK (2009) The primary cilium as a complex signaling center. Curr Biol 19(13):R526-R535
3. Berbari NF, Sharma N, Malarkey EB, Pieczynski JN, Boddu R, Gaertig J, Guay-Woodford L, Yoder BK (2013) Microtubule modifications and stability are altered by cilia perturbation and in cystic kidney disease. Cytoskeleton (Hoboken) 70(1):24-31
4. Blain EJ (2009) Involvement of the cytoskeletal elements in articular cartilage homeostasis and pathology. Int J Exp Pathol 90(1):1-15
5. Challa TD, Rais Y, Ornan EM (2010) Effect of adiponectin on ATDC5 proliferation, differentiation and signaling pathways. Mol Cell Endocrinol 323(2):282-291
6. Chen JK, Taipale J, Young KE, Beachy PA (2002) Small molecule modulation of smoothened activity. Proc Natl Acad Sci USA 99(22):14071-14076
7. Dagoneau N, Goulet M, Genevieve D, Sznajer Y, Martinovic J, Smithson S, Huber C, Baujat G, Flori E, Tecco L, Cavalcanti D, Delezoide AL, Serre V, Le Merrer M, Munnich A, Cormier-Daire V (2009) DYNC2H1 mutations cause asphyxiating thoracic dystrophy and short rib-polydactyly syndrome, type III. Am J Hum Genet 84(5):706-711
8. de Andrea CE, Wiweger M, Prins F, Bovee JV, Romeo S, Hogendoorn PC (2010) Primary cilia organization reflects polarity in the growth plate and implies loss of polarity and mosaicism in osteochondroma. Lab Invest 90(7):1091-1101
9. Ehlen HW, Buelens LA, Vortkamp A (2006) Hedgehog signaling in skeletal development. Birth Defects Res C Embryo Today 78(3):267-279
10. Epari DR, Taylor WR, Heller MO, Duda GN (2006) Mechanical conditions in the initial phase of bone healing. Clin Biomech (Bristol, Avon) 21(6):646-655
11. Goodship AE, Lanyon LE, McFie H (1979) Functional adaptation of bone to increased stress: an experimental study. J Bone Joint Surg Am 61(4):539-546
12. Guilak F, Alexopoulos LG, Upton ML, Youn I, Choi JB, Cao L, Setton LA, Haider MA (2006) The pericellular matrix as a transducer of biomechanical and biochemical signals in articular cartilage. Ann N Y Acad Sci 1068:498-512
13. Haraguchi K, Hayashi T, Jimbo T, Yamamoto T, Akiyama T (2006) Role of the kinesin-2 family protein, KIF3, during mitosis. J Biol Chem 281(7):4094-4099
14. Hasky-Negev M, Simsa S, Tong A, Genina O, Monsonego Ornan E (2008) Expression of matrix metalloproteinases during vascularization and ossification of normal and impaired avian growth plate. J Anim Sci 86(6):1306-1315
15. Haycraft CJ, Zhang Q, Song B, Jackson WS, Detloff PJ, Serra R, Yoder BK (2007) Intraflagellar transport is essential for endochondral bone formation. Development 134(2):307-316
16. Haycraft CJ, Serra R (2008) Cilia involvement in patterning and maintenance of the skeleton. Curr Top Dev Biol 85:303-332
17. Hirokawa N (2000) Determination of left-right asymmetry: role of Cilia and KIF3 motor proteins. News Physiol Sci 15:56
18. Hoey DA, Tormey S, Ramcharan S, O'Brien FJ, Jacobs CR (2012) Primary cilia-mediated mechanotransduction in human mesenchymal stem cells. Stem Cells 30(11):2561-2570
19. Hoffman BD, Grashoff C, Schwartz MA (2011) Dynamic molecular processes mediate cellular mechanotransduction. Nature 475(7356):316-323
20. Idelevich A, Rais Y, Monsonego-Ornan E (2012) Bone Gla protein increases HIF-1alpha-dependent glucose metabolism and induces cartilage and vascular calcification. Arterioscler Thromb Vasc Biol 31(9):e55-e71
21. Jacobs CR, Temiyasathit S, Castillo AB (2010) Osteocyte mechanobiology and pericellular mechanics. Annu Rev Biomed Eng 12:369-400
22. Jensen CG, Poole CA, McGlashan SR, Marko M, Issa ZI, Vujcich KV, Bowser SS (2004) Ultrastructural, tomographic and confocal imaging of the chondrocyte primary cilium in situ. Cell Biol Int 28(2):101-110
23. Karp SJ, Schipani E, St-Jacques B, Hunzelman J, Kronenberg H, McMahon AP (2000) Indian hedgehog coordinates endochondral bone growth and morphogenesis via parathyroid hormone related-protein-dependent and -independent pathways. Development 127(3):543-548
24. Kim J, Kato M, Beachy PA (2009) Gli2 trafficking links Hedgehog-dependent activation of Smoothened in the primary cilium to transcriptional activation in the nucleus. Proc Natl Acad Sci USA 106(51):21666-21671
25. Kinumatsu T, Shibukawa Y, Yasuda T, Nagayama M, Yamada S, Serra R, Pacifici M, Koyama E (2011) TMJ development and growth require primary cilia function. J Dent Res 90(8):988-994
26. Kolpakova-Hart E, Nicolae C, Zhou J, Olsen BR (2008) Col2-Cre recombinase is co-expressed with endogenous type II collagen in embryonic renal epithelium and drives development of polycystic kidney disease following inactivation of ciliary genes. Matrix Biol 27(6):505-512
27. Kottgen M, Buchholz B, Garcia-Gonzalez MA, Kotsis F, Fu X, Doerken M, Boehlke C, Steffl D, Tauber R, Wegierski T, Nitschke R, Suzuki M, Kramer-Zucker A, Germino GG, Watnick T, Prenen J, Nilius B, Kuehn EW, Walz G (2008) TRPP2 and TRPV4 form a polymodal sensory channel complex. J Cell Biol 182(3):437-447
28. Koyama E, Young B, Nagayama M, Shibukawa Y, Enomoto-Iwamoto M, Iwamoto M, Maeda Y, Lanske B, Song B, Serra R, Pacifici M (2007) Conditional Kif3a ablation causes abnormal hedgehog signaling topography, growth plate dysfunction, and excessive bone and cartilage formation during mouse skeletogenesis. Development 134(11):2159-2169
29. Li S, Duance VC, Blain EJ (2008) Zonal variations in cytoskeletal element organization, mRNA and protein expression in the intervertebral disc. J Anat 213(6):725-732
30. Li J, Zhao Z, Yang J, Liu J, Wang J, Li X, Liu Y (2009) p38 MAPK mediated in compressive stressinduced chondrogenesis of rat bone marrow MSCs in 3D alginate scaffolds. J Cell Physiol 221(3):609-617
31. Lin F, Hiesberger T, Cordes K, Sinclair AM, Goldstein LS, Somlo S, Igarashi P (2003) Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease. Proc Natl Acad Sci USA 100(9):5286-5291
32. Liu A, Wang B, Niswander LA (2005) Mouse intraflagellar transport proteins regulate both the activator and repressor functions of Gli transcription factors. Development 132(13):3103-3111
33. Luo W, Xiong W, Zhou J, Fang Z, Chen W, Fan Y, Li F (2011) Laminar shear stress delivers cell cycle arrest and anti-apoptosis to mesenchymal stem cells. Acta Biochim Biophys Sin (Shanghai) 43(3):210-216
34. Malone AM, Anderson CT, Tummala P, Kwon RY, Johnston TR, Stearns T, Jacobs CR (2007) Primary cilia mediate mechanosensing in bone cells by a calcium-independent mechanism. Proc Natl Acad Sci USA 104 (33):13325-13330
35. Marszalek JR, Ruiz-Lozano P, Roberts E, Chien KR, Goldstein LS (1999) Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc Natl Acad Sci USA 96(9):5043-5048
36. McGlashan SR, Jensen CG, Poole CA (2006) Localization of extracellular matrix receptors on the chondrocyte primary cilium. J Histochem Cytochem 54(9):1005-1014
37. McGlashan SR, Haycraft CJ, Jensen CG, Yoder BK, Poole CA (2007) Articular cartilage and growth plate defects are associated with chondrocyte cytoskeletal abnormalities in Tg737orpk mice lacking the primary cilia protein polaris. Matrix Biol 26(4):234-246
38. McGlashan SR, Knight MM, Chowdhury TT, Joshi P, Jensen CG, Kennedy S, Poole CA (2010) Mechanical loading modulates chondrocyte primary cilia incidence and length. Cell Biol Inter 34(5):441-446
39. Meier-Vismara E, Walker N, Vogel A (1979) Single cilia in the articular cartilage of the cat. Exp Cell Biol 47(3):161-171
40. Muhammad H, Rais Y, Miosge N, Ornan EM (2012) The primary cilium as a dual sensor of mechanochemical signals in chondrocytes. Cell Mol Life Sci 69(13):2101-2107
41. Murcia NS, Richards WG, Yoder BK, Mucenski ML, Dunlap JR, Woychik RP (2000) The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination. Development 127(11):2347-2355
42. Nauli SM, Zhou J (2004) Polycystins and mechanosensation in renal and nodal cilia. BioEssays 26(8):844-856
43. Ng TC, Chiu KW, Rabie AB, Hagg U (2006) Repeated mechanical loading enhances the expression of Indian hedgehog in condylar cartilage. Front Biosci 11:943-948
44. Olsen B (2005) Nearly all cells in vertebrates and many cells in invertebrates contain primary cilia. Matrix Biol 24(7):449-450
45. Ott CE, Bauer S, Manke T, Ahrens S, Rodelsperger C, Grunhagen J, Kornak U, Duda G, Mundlos S, Robinson PN (2009) Promiscuous and depolarization-induced immediate-early response genes are induced by mechanical strain of osteoblasts. J Bone Miner Res 24(7):1247-1262
46. Papachristou DJ, Papachroni KK, Basdra EK, Papavassiliou AG (2009) Signaling networks and transcription factors regulating mechanotransduction in bone. BioEssays 31(7):794-804
47. Pazour GJ, Witman GB (2003) The vertebrate primary cilium is a sensory organelle. Curr Opin Cell Biol 15(1):105-110
48. Pearson SJ, Cobbold M, Harridge SD (2004) Power output of the lower limb during variable inertial loading: a comparison between methods using single and repeated contractions. Eur J Appl Physiol 92(1-2):176-181
49. Pedersen LB, Veland IR, Schroder JM, Christensen ST (2008) Assembly of primary cilia. Dev Dyn 237(8):1993-2006
50. Plotnikova OV, Golemis EA, Pugacheva EN (2008) Cell cycle-dependent ciliogenesis and cancer. Cancer Res 68(7):2058-2061
51. Poole CA, Flint MH, Beaumont BW (1984) Morphological and functional interrelationships of articular cartilage matrices. J Anat 138(Pt 1):113-138
52. Poole CA, Flint MH, Beaumont BW (1985) Analysis of the morphology and function of primary cilia in connective tissues: a cellular cybernetic probe? Cell Motil 5(3):175-193
53. Poole CA, Zhang ZJ, Ross JM (2001) The differential distribution of acetylated and detyrosinated alpha-tubulin in the microtubular cytoskeleton and primary cilia of hyaline cartilage chondrocytes. J Anat 199 (Pt4):393-405
54. Praetorius HA, Leipziger J (2012) Primary cilium-dependent sensing of urinary flow and paracrine purinergic signaling. Semin Cell Dev Biol 24(1):3-10
55. Praetorius HA, Spring KR (2003) The renal cell primary cilium functions as a flow sensor. Curr Opin Nephrol Hypertens 12(5):517-520
56. Reich A, Jaffe N, Tong A, Lavelin I, Genina O, Pines M, Sklan D, Nussinovitch A, Monsonego-Ornan E (2005) Weight loading young chicks inhibits bone elongation and promotes growth plate ossification and vascularization. J Appl Physiol 98(6):2381-2389
57. Reich A, Sharir A, Zelzer E, Hacker L, Monsonego-Ornan E, Shahar R (2008) The effect of weight loading and subsequent release from loading on the postnatal skeleton. Bone 43(4):766-774
58. Reich A, Maziel SS, Ashkenazi Z, Ornan EM (2010) Involvement of matrix metalloproteinases in the growth plate response to physiological mechanical load. J Appl Physiol 108(1):172-180
59. Rieder CL, Jensen CG, Jensen LC (1979) The resorption of primary cilia during mitosis in a vertebrate (PtK1) cell line. J Ultrastruct Res 68(2):173-185
60. Robert A, Margall-Ducos G, Guidotti JE, Bregerie O, Celati C, Brechot C, Desdouets C (2007) The intraflagellar transport component IFT88/polaris is a centrosomal protein regulating G1-S transition in non-ciliated cells. J Cell Sci 120(Pt 4):628-637
61. Rubin CT, Lanyon LE (1984) Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am 66(3):397-402
62. Ruhlen R, Marberry K (2014) The chondrocyte primary cilium. Osteoarthr Cartil S1063-4584(14):01090-01095
63. Sanz-Ramos P, Mora G, Ripalda P, Vicente-Pascual M, Izal-Azcarate I (2012) Identification of signalling pathways triggered by changes in the mechanical environment in rat chondrocytes. Osteoarthr Cartil 20(8):931-939
64. Scholey JM, Anderson KV (2006) Intraflagellar transport and cilium-based signaling. Cell 125(3):439-442
65. Schulz RM, Bader A (2007) Cartilage tissue engineering and bioreactor systems for the cultivation and stimulation of chondrocytes. Eur Biophys J 36(4-5):539-568
66. Seeger-Nukpezah T, Golemis EA (2012) The extracellular matrix and ciliary signaling. Curr Opin Cell Biol 24(5):652-661
67. Shao YY, Wang L, Welter JF, Ballock RT (2012) Primary cilia modulate Ihh signal transduction in response to hydrostatic loading of growth plate chondrocytes. Bone 50(1):79-84
68. Sharma N, Kosan ZA, Stallworth JE, Berbari NF, Yoder BK (2011) Soluble levels of cytosolic tubulin regulate ciliary length control. Mol Biol Cell 22(6):806-816
69. Simsa-Maziel S, Monsonego-Ornan E (2012) Interleukin-1beta promotes proliferation and inhibits differentiation of chondrocytes through a mechanism involving down-regulation of FGFR-3 and p21. Endocrinology 153(5):2296-2310
70. Simsa S, Ornan EM (2007) Endochondral ossification process of the turkey (Meleagris gallopavo) during embryonic and juvenile development. Poult Sci 86(3):565-571
71. Sloboda RD, Rosenbaum JL (2007) Making sense of cilia and flagella. J Cell Biol 179(4):575-582
72. Song B, Haycraft CJ, Seo HS, Yoder BK, Serra R (2007) Development of the post-natal growth plate requires intraflagellar transport proteins. Dev Biol 305(1):202-216
73. 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(16):2072-2086
74. Tanaka SM, Sun HB, Roeder RK, Burr DB, Turner CH, Yokota H (2005) Osteoblast responses one hour after load-induced fluid flow in a three-dimensional porous matrix. Calcif Tissue Int 76(4):261-271
75. Tang GH, Rabie AB, Hagg U (2004) Indian hedgehog: a mechanotransduction mediator in condylar cartilage. J Dent Res 83(5):434-438
76. Temiyasathit S, Tang WJ, Leucht P, Anderson CT, Monica SD, Castillo AB, Helms JA, Stearns T, Jacobs CR (2012) Mechanosensing by the primary cilium: deletion of Kif3A reduces bone formation due to loading. PLoS One 7(3):e33368
77. Terai K, Takano-Yamamoto T, Ohba Y, Hiura K, Sugimoto M, Sato M, Kawahata H, Inaguma N, Kitamura Y, Nomura S (1999) Role of osteopontin in bone remodeling caused by mechanical stress. J Bone Miner Res 14(6):839-849
78. Thompson CL, Chapple JP, Knight MM (2014) Primary cilia disassembly down-regulates mechanosensitive hedgehog signalling: a feedback mechanism controlling ADAMTS-5 expression in chondrocytes. Osteoarthr Cartil 22(3):490-498
79. Tong A, Reich A, Genin O, Pines M, Monsonego-Ornan E (2003) Expression of chicken 75-kDa gelatinase B-like enzyme in perivascular chondrocytes suggests its role in vascularization of the growth plate. J Bone Miner Res 18(8):1443-1452
80. van der Eerden BC, Karperien M, Gevers EF, Lowik CW, Wit JM (2000) Expression of Indian hedgehog, parathyroid hormone-related protein, and their receptors in the postnatal growth plate of the rat: evidence for a locally acting growth restraining feedback loop after birth. J Bone Miner Res 15(6):1045-1055
81. Vortkamp A (2000) The Indian hedgehog-PTHrP system in bone development. Ernst Schering Res Found Workshop 29:191-209
82. Vortkamp A, Lee K, Lanske B, Segre GV, Kronenberg HM, Tabin CJ (1996) Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273(5275):613-622
83. Wann AK, Zuo N, Haycraft CJ, Jensen CG, Poole CA, McGlashan SR, Knight MM (2012) Primary cilia mediate mechanotransduction through control of ATP-induced Ca2+ signaling in compressed chondrocytes. Faseb J 26(4):1663-1671
84. Wheatley DN, Bowser SS (2000) Length control of primary cilia: analysis of monociliate and multiciliate PtK1 cells. Biol Cell 92(8-9):573-582
85. Wilsman NJ, Farnum CE, Reed-Aksamit DK (1980) Incidence and morphology of equine and murine chondrocytic cilia. Anat Rec 197(3):355-361
86. Wu Q, Zhang Y, Chen Q (2001) Indian hedgehog is an essential component of mechanotransduction complex to stimulate chondrocyte proliferation. J Biol Chem 276(38):35290-35296
87. Wu QQ, Chen Q (2000) Mechanoregulation of chondrocyte proliferation, maturation, and hypertrophy: ion-channel dependent transduction of matrix deformation signals. Exp Cell Res 256(2):383-391