The intraflagellar transport protein IFT80 is required for cilia formation and osteogenesis

Bone

Volumn 51, Issue 3, 2012, Pages 407-417

  Yang, Shuying ^a   Wang, Changdong ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Cilia; Hedgehog signaling; Intraflagellar transport; Osteoblast differentiation; Skeleton development

Indexed keywords

ALKALINE PHOSPHATASE; ARL13B PROTEIN; CARRIER PROTEIN; GUANOSINE TRIPHOSPHATASE; IFT80 PROTEIN; INTRAFLAGELLAR TRANSPORT PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI2; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EUKARYOTIC FLAGELLUM; GENE; GENE SILENCING; HUMAN; HUMAN CELL; IFT80 GENE; LONG BONE; MESENCHYMAL STEM CELL; MINERALIZATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PROTEIN EXPRESSION; RNA INTERFERENCE; SKULL; STROMA CELL;

ADP-RIBOSYLATION FACTORS; ALKALINE PHOSPHATASE; ANIMALS; BONE AND BONES; CALCIFICATION, PHYSIOLOGIC; CARRIER PROTEINS; CELL DIFFERENTIATION; CILIA; GENE EXPRESSION REGULATION; GENE SILENCING; HEDGEHOG PROTEINS; HEK293 CELLS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, INBRED C57BL; OSTEOBLASTS; OSTEOGENESIS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; STEM CELLS; TUBULIN;

EID: 84864066860     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2012.06.021     Document Type: Article

References (85)

1. Serra R. Intraflagellar transport in skeletal development. J Musculoskelet Neuronal Interact 2007, 7:302-303.
2. Bisgrove B.W., Yost H.J. The roles of cilia in developmental disorders and disease. Development 2006, 133:4131-4143.
3. Davenport J.R., Yoder B.K. An incredible decade for the primary cilium: a look at a once-forgotten organelle. Am J Physiol Renal Physiol 2005, 289:F1159-F1169.
4. Pan J., Wang Q., Snell W.J. Cilium-generated signaling and cilia-related disorders. Lab Invest 2005, 85:452-463.
5. Mykytyn K., Mullins R.F., Andrews M., Chiang A.P., Swiderski R.E., Yang B., et al. Bardet-Biedl syndrome type 4 (Bbs4)-null mice implicate bbs4 in flagella formation but not global cilia assembly. Proc Natl Acad Sci U S A 2004, 101:8664-8669.
6. Mykytyn K., Sheffield V.C. Establishing a connection between cilia and Bardet-Biedl syndrome. Trends Mol Med 2004, 10:106-109.
7. 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.
8. 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.
9. Kolpakova-Hart E., Jinnin M., Hou B., Fukai N., Olsen B.R. Kinesin-2 controls development and patterning of the vertebrate skeleton by Hedgehog- and Gli3-dependent mechanisms. Dev Biol 2007, 309:273-284.
10. Liu A., Wang B., Niswander L.A. Mouse intraflagellar transport proteins regulate both the activator and repressor functions of gli transcription factors. Development 2005, 132:3103-3111.
11. 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.
12. 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.
13. Zhang Q., Murcia N.S., Chittenden L.R., Richards W.G., Michaud E.J., Woychik R.P., et al. Loss of the Tg737 protein results in skeletal patterning defects. Dev Dyn 2003, 227:78-90.
14. Haycraft C.J., Serra R. Cilia involvement in patterning and maintenance of the skeleton. Curr Top Dev Biol 2008, 85:303-332.
15. Chang C.F., Ramaswamy G., Serra R. Depletion of primary cilia in articular chondrocytes results in reduced gli3 repressor to activator ratio, increased hedgehog signaling, and symptoms of early osteoarthritis. Osteoarthritis Cartilage 2012, 20:152-161.
16. Serra R. Role of intraflagellar transport and primary cilia in skeletal development. Anat Rec (Hoboken) 2008, 291:1049-1061.
17. Martins A.A., Paiva A., Morgado J.M., Gomes A., Pais M.L. Quantification and immunophenotypic characterization of bone marrow and umbilical cord blood mesenchymal stem cells by multicolor flow cytometry. Transplant Proc 2009, 41:943-946.
18. Berbari N.F., O'connor A.K., Haycraft C.J., Yoder B.K. The primary cilium as a complex signaling center. Curr Biol 2009, 19:R526-R535.
19. Xiao Z., Dallas M., Qiu N., Nicolella D., Cao L., Johnson M., et al. Conditional deletion of Pkd1 in osteocytes disrupts skeletal mechanosensing in mice. FASEB J 2011, 25:2418-2432.
20. Kalogeropoulos M., Varanasi S.S., Olstad O.K., Sanderson P., Gautvik V.T., Reppe S., et al. Zic1 transcription factor in bone: neural developmental protein regulates mechanotransduction in osteocytes. FASEB J 2010, 24:2893-2903.
21. Xiao Z., Zhang S., Cao L., Qiu N., David V., Quarles L.D. Conditional disruption of pkd1 in osteoblasts results in osteopenia due to direct impairment of bone formation. J Biol Chem 2010, 285:1177-1187.
22. 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.
23. Kimura H., Ng J.M., Curran T. Transient inhibition of the hedgehog pathway in young mice causes permanent defects in bone structure. Cancer Cell 2008, 13:249-260.
24. Mcmahon A.P., Ingham P.W., Tabin C.J. Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol 2003, 53:1-114.
25. Wang B., Fallon J.F., Beachy P.A. Hedgehog-regulated processing of gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 2000, 100:423-434.
26. Marigo V., Johnson R.L., Vortkamp A., Tabin C.J. Sonic hedgehog differentially regulates expression of gli and gli3 during limb development. Dev Biol 1996, 180:273-283.
27. 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.
28. 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.
29. Shahangian A., Chow E.K., Tian X., Kang J.R., Ghaffari A., Liu S.Y., et al. Type I Ifns mediate development of postinfluenza bacterial pneumonia in mice. J Clin Invest 2009, 119:1910-1920.
30. Huang W., Kane J.K., Li M.D. Identification and characterization of a long isoform of human Ift80, Ift80-L. Biochem Biophys Res Commun 2008, 373:653-658.
31. Beales P.L., Bland E., Tobin J.L., Bacchelli C., Tuysuz B., Hill J., et al. Ift80, which encodes a conserved intraflagellar transport protein, is mutated in jeune asphyxiating thoracic dystrophy. Nat Genet 2007, 39:727-729.
32. Cavalcanti D.P., Huber C., Le Quan Sang K.H., Baujat G., Collins F., Delezoide A.L., et al. Mutation In Ift80 gene in a foetus with a phenotype of Verma-Naumoff provides molecular evidence for the Jeune-Verma-Naumoff dysplasia spectrum. J Med Genet 2011, 48:88-92.
33. Dagoneau N., Goulet M., Genevieve D., Sznajer Y., Martinovic J., Smithson S., et al. Dync2h1 mutations cause asphyxiating thoracic dystrophy and short rib-polydactyly syndrome, Type III. Am J Hum Genet 2009, 84:706-711.
34. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
35. D'Souza S., Kurihara N., Shiozawa Y., Joseph J., Taichman R., Galson D.L., Roodman G.D. Annexin II interactions with the annexin II receptor enhance multiple myeloma cell adhesion and growth in the bone marrow microenvironment. Blood 2012, 119:1888-1896.
36. Yang S., Li Y.P. Rgs12 is essential for Rankl-evoked signaling for terminal differentiation of osteoclasts in vitro. J Bone Miner Res 2007, 22:45-54.
37. Stewart S.A., Dykxhoorn D.M., Palliser D., Mizuno H., Yu E.Y., An D.S., et al. Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA 2003, 9:493-501.
38. Yang S., Li Y.P. Rgs10-null mutation impairs osteoclast differentiation resulting from the loss of [Ca2+]I oscillation regulation. Genes Dev 2007, 21:1803-1816.
39. Vandesompele J., De Paepe A., Speleman F. Elimination of primer-dimer artifacts and genomic coamplification using a two-Step Sybr green I real-time Rt-Pcr. Anal Biochem 2002, 303:95-98.
40. Schneider G.B., Whitson S.W., Cooper L.F. Restricted and coordinated expression of Beta3-integrin and bone sialoprotein during cultured osteoblast differentiation. Bone 1999, 24:321-327.
41. Ovchinnikov D. Alcian blue/Alizarin red staining of cartilage and bone in mouse. Cold Spring Harb Protoc 2009, 2009. [Pdb Prot5170].
42. Yamakawa K., Iwasaki H., Masuda I., Ohjimi Y., Honda I., Saeki K., et al. The utility of Alizarin Red S staining in calcium pyrophosphate dihydrate crystal deposition disease. J Rheumatol 2003, 30:1032-1035.
43. Reinholz G.G., Getz B., Pederson L., Sanders E.S., Subramaniam M., Ingle J.N., et al. Bisphosphonates directly regulate cell proliferation, differentiation, and gene expression in human osteoblasts. Cancer Res 2000, 60:6001-6007.
44. Rungby J., Kassem M., Eriksen E.F., Danscher G. The Von Kossa reaction for calcium deposits: silver lactate staining increases sensitivity and reduces background. Histochem J 1993, 25:446-451.
45. Mccauley L.K., Koh A.J., Beecher C.A., Cui Y., Decker J.D., Franceschi R.T. Effects of differentiation and transforming growth factor Beta 1 On Pth/Pthrp Receptor mRNA levels In Mc3t3-E1 cells. J Bone Miner Res 1995, 10:1243-1255.
46. Yang S., Wei D., Wang D., Phimphilai M., Krebsbach P.H., Franceschi R.T. In vitro and in vivo synergistic interactions between the Runx2/Cbfa1 transcription factor and bone morphogenetic protein-2 in stimulating osteoblast differentiation. J Bone Miner Res 2003, 18:705-715.
47. Rosenbaum J.L., Witman G.B. Intraflagellar transport. Nat Rev Mol Cell Biol 2002, 3:813-825.
48. Pedersen L.B., Rosenbaum J.L. Intraflagellar transport (Ift) role in ciliary assembly, resorption and signalling. Curr Top Dev Biol 2008, 85:23-61.
49. Mukhopadhyay S., Lu Y., Qin H., Lanjuin A., Shaham S., Sengupta P. Distinct Ift mechanisms contribute to the generation of ciliary structural diversity in C. elegans. EMBO J 2007, 26:2966-2980.
50. Gu Y., Liang X., Wu W., Liu M., Song S., Cheng L., et al. Multicenter contraceptive efficacy trial of injectable testosterone undecanoate in Chinese men. J Clin Endocrinol Metab 2009, 94:1910-1915.
51. Orimo H. The mechanism of mineralization and the role of alkaline phosphatase in health and disease. J Nihon Med Sch 2010, 77:4-12.
52. Huangfu D., Liu A., Rakeman A.S., Murcia N.S., Niswander L., Anderson K.V. Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 2003, 426:83-87.
53. Huangfu D., Anderson K.V. Cilia and hedgehog responsiveness in the mouse. Proc Natl Acad Sci U S A 2005, 102:11325-11330.
54. Eggenschwiler J.T., Anderson K.V. Cilia and developmental signaling. Annu Rev Cell Dev Biol 2007, 23:345-373.
55. Jemtland R., Divieti P., Lee K., Segre G.V. Hedgehog promotes primary osteoblast differentiation and increases Pthrp mRNA expression and Ipthrp secretion. Bone 2003, 32:611-620.
56. Joeng K.S., Long F. The Gli2 transcriptional activator is a crucial effector for ihh signaling in osteoblast development and cartilage vascularization. Development 2009, 136:4177-4185.
57. Kesper D.A., Didt-Koziel L., Vortkamp A. Gli2 activator function in preosteoblasts is sufficient to mediate Ihh-dependent osteoblast differentiation, whereas the repressor function of Gli2 is dispensable for endochondral ossification. Dev Dyn 2010, 239:1818-1826.
58. Kinsella T.M., Nolan G.P. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum Gene Ther 1996, 7:1405-1413.
59. Yang S., Delgado R., King S.R., Woffendin C., Barker C.S., Yang Z.Y., et al. Generation of retroviral vector for clinical studies using transient transfection. Hum Gene Ther 1999, 10:123-132.
60. Rohatgi R., Milenkovic L., Scott M.P. Patched1 regulates hedgehog signaling at the primary cilium. Science 2007, 317:372-376.
61. Wang Y., Zhou Z., Walsh C.T., Mcmahon A.P. Selective translocation of intracellular smoothened to the primary cilium in response to hedgehog pathway modulation. Proc Natl Acad Sci U S A 2009, 106:2623-2628.
62. Rohatgi R., Milenkovic L., Corcoran R.B., Scott M.P. Hedgehog signal transduction by smoothened: pharmacologic evidence for a 2-step activation process. Proc Natl Acad Sci U S A 2009, 106:3196-3201.
63. Cavalcanti D.P., Huber C., Sang K.H., Baujat G., Collins F., Delezoide A.L., et al. Mutation in Ift80 in a fetus with the phenotype of verma-naumoff provides molecular evidence for Jeune-Verma-Naumoff dysplasia spectrum. J Med Genet 2011, 48:88-92.
64. Pazour G.J., Baker S.A., Deane J.A., Cole D.G., Dickert B.L., Rosenbaum J.L., et al. The intraflagellar transport protein, Ift88, is essential for vertebrate photoreceptor assembly and maintenance. J Cell Biol 2002, 157:103-113.
65. 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.
66. Rix S., Calmont A., Scambler P.J., Beales P.L. An Ift80 mouse model of short rib polydactyly syndromes shows defects in hedgehog signalling without loss or malformation of cilia. Hum Mol Genet 2011, 20:1306-1314.
67. Scholey J.M. Intraflagellar transport. Annu Rev Cell Dev Biol 2003, 19:423-443.
68. Hudak L.M., Lunt S., Chang C.H., Winkler E., Flammer H., Lindsey M., et al. The intraflagellar transport protein Ift80 is essential for photoreceptor survival in a zebrafish model of Jeune asphyxiating thoracic dystrophy. Invest Ophthalmol Vis Sci 2010, 51:3792-3799.
69. Oberklaid F., Danks D.M., Mayne V., Campbell P. Asphyxiating thoracic dysplasia. clinical, radiological, and pathological information on 10 patients. Arch Dis Child 1977, 52:758-765.
70. Caspary T., Larkins C.E., Anderson K.V. The graded response to sonic hedgehog depends on cilia architecture. Dev Cell 2007, 12:767-778.
71. Ocbina P.J., Anderson K.V. Intraflagellar transport, cilia, and mammalian hedgehog signaling: analysis in mouse embryonic fibroblasts. Dev Dyn 2008, 237:2030-2038.
72. Hui C.C., Angers S. Gli proteins in development and disease. Annu Rev Cell Dev Biol 2011, 27:513-537.
73. Persson M., Stamataki D., Te Welscher P., Andersson E., Bose J., Ruther U., et al. Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity. Genes Dev 2002, 16:2865-2878.
74. Litingtung Y., Chiang C. Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat Neurosci 2000, 3:979-985.
75. Bai C.B., Joyner A.L. Gli1 can rescue the in vivo function of Gli2. Development 2001, 128:5161-5172.
76. Park H.L., Bai C., Platt K.A., Matise M.P., Beeghly A., Hui C.C., et al. Mouse Gli1 mutants are viable but have defects in Shh signaling in combination with a Gli2 mutation. Development 2000, 127:1593-1605.
77. Shimoyama A., Wada M., Ikeda F., Hata K., Matsubara T., Nifuji A., et al. Ihh/Gli2 signaling promotes osteoblast differentiation by regulating Runx2 expression and function. Mol Biol Cell 2007, 18:2411-2418.
78. Hojo H., Ohba S., Yano F., Saito T., Ikeda T., Nakajima K., et al. Gli1 protein participates in hedgehog-mediated specification of osteoblast lineage during endochondral ossification. J Biol Chem 2012, 287:17860-17869.
79. Chen M.H., Wilson C.W., Li Y.J., Law K.K., Lu C.S., Gacayan R., et al. Cilium-independent regulation of Gli protein function by Sufu in hedgehog signaling is evolutionarily conserved. Genes Dev 2009, 23:1910-1928.
80. Spinella-Jaegle S., Rawadi G., Kawai S., Gallea S., Faucheu C., Mollat P., et al. Sonic hedgehog increases the commitment of pluripotent mesenchymal cells into the osteoblastic lineage and abolishes adipocytic differentiation. J Cell Sci 2001, 114:2085-2094.
81. Van Der Horst G., Farih-Sips H., Lowik C.W., Karperien M. Hedgehog stimulates only osteoblastic differentiation of undifferentiated Ks483 cells. Bone 2003, 33:899-910.
82. Kawai S., Sugiura T. Characterization of human bone morphogenetic protein (Bmp)-4 And -7 gene promoters: activation of bmp promoters by Gli, a sonic hedgehog mediator. Bone 2001, 29:54-61.
83. Krishnan V., Ma Y., Moseley J., Geiser A., Friant S., Frolik C. Bone anabolic effects of Sonic/Indian hedgehog are mediated by Bmp-2/4-Dependent pathways in the neonatal rat metatarsal model. Endocrinology 2001, 142:940-947.
84. Zhao M., Qiao M., Harris S.E., Chen D., Oyajobi B.O., Mundy G.R. The zinc finger transcription factor Gli2 mediates bone morphogenetic protein 2 expression in osteoblasts in response to hedgehog signaling. Mol Cell Biol 2006, 26:6197-6208.
85. Xiao Z.S., Quarles L.D. Role of the polycytin-primary cilia complex in bone development and mechanosensing. Ann N Y Acad Sci 2010, 1192:410-421.