TGFβ and BMP Dependent Cell Fate Changes Due to Loss of Filamin B Produces Disc Degeneration and Progressive Vertebral Fusions

PLoS Genetics

Volumn 12, Issue 3, 2016, Pages

  Zieba, Jennifer ^a   Forlenza, Kimberly Nicole ^a   Khatra, Jagteshwar Singh ^a   Sarukhanov, Anna ^a   Duran, Ivan ^a   Rigueur, Diana ^b   Lyons, Karen M ^a,b   Cohn, Daniel H ^a,b   Merrill, Amy E ^c,d   Krakow, Deborah ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; COLLAGEN TYPE 10; CONNECTIVE TISSUE GROWTH FACTOR; FILAMIN; FILAMIN B; PROTEIN P21; RNA; SMAD2 PROTEIN; SMAD3 PROTEIN; SYNAPTOPHYSIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; CTGF PROTEIN, MOUSE; SMAD PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANNULUS FIBROSUS; APOPTOSIS; ARTICLE; CARTILAGE CELL; CELL FATE; CONTROLLED STUDY; CTGF GENE; FIBROBLAST; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERVERTEBRAL DISK DEGENERATION; KNOCKOUT MOUSE; MORPHOLOGY; MOUSE; NONHUMAN; P21 GENE; PHENOTYPE; POSTNATAL DEVELOPMENT; PROTEIN DEPLETION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPINE FUSION; UPREGULATION; WESTERN BLOTTING; ABNORMALITIES; ANIMAL; CHONDROCYTE; DISEASE MODEL; EPIPHYSIS PLATE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; LUMBAR VERTEBRA; METABOLISM; MULTIPLE MALFORMATION SYNDROME; MUSCULOSKELETAL DISEASE; PATHOLOGY; SCOLIOSIS; SPINE; SYNOSTOSIS; THORACIC VERTEBRA;

ABNORMALITIES, MULTIPLE; ACTIN CYTOSKELETON; ANIMALS; BONE MORPHOGENETIC PROTEINS; CHONDROCYTES; CONNECTIVE TISSUE GROWTH FACTOR; DISEASE MODELS, ANIMAL; FILAMINS; GROWTH PLATE; HUMANS; INTERVERTEBRAL DISC DEGENERATION; LUMBAR VERTEBRAE; MICE; MICE, KNOCKOUT; MUSCULOSKELETAL DISEASES; SCOLIOSIS; SIGNAL TRANSDUCTION; SMAD PROTEINS; SPINE; SYNOSTOSIS; THORACIC VERTEBRAE; TRANSFORMING GROWTH FACTOR BETA;

EID: 84962477021     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005936     Document Type: Article

References (42)

1. Krakow D, Rimoin DL, The skeletal dysplasias. Genetics in medicine: official journal of the American College of Medical Genetics. 2010;12(6):327–41. doi: 10.1097/GIM.0b013e3181daae9b20556869.
2. Mitter D, Krakow D, Farrington-Rock C, Meinecke P, Expanded clinical spectrum of spondylocarpotarsal synostosis syndrome and possible manifestation in a heterozygous father. American journal of medical genetics Part A. 2008;146A(6):779–83. doi: 10.1002/ajmg.a.3223018257094.
3. Al Kaissi A, Ghachem MB, Nassib N, Ben Chehida F, Kozlowski K, Spondylocarpotarsal synostosis syndrome (with a posterior midline unsegmented bar). Skeletal radiology. 2005;34(6):364–6. doi: 10.1007/s00256-004-0869-415891931.
4. Lories RJ, Luyten FP, Bone morphogenetic protein signaling in joint homeostasis and disease. Cytokine & growth factor reviews. 2005;16(3):287–98. doi: 10.1016/j.cytogfr.2005.02.00915993360.
5. Yang X, Chen L, Xu X, Li C, Huang C, Deng CX, TGF-beta/Smad3 signals repress chondrocyte hypertrophic differentiation and are required for maintaining articular cartilage. The Journal of cell biology. 2001;153(1):35–46. 11285272; PubMed Central PMCID: PMC2185521.
6. Shi Y, Massague J, Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell. 2003;113(6):685–700. 12809600.
7. Miyazono K, Kusanagi K, Inoue H, Divergence and convergence of TGF-beta/BMP signaling. Journal of cellular physiology. 2001;187(3):265–76. doi: 10.1002/jcp.108011319750.
8. Sohn P, Cox M, Chen D, Serra R, Molecular profiling of the developing mouse axial skeleton: a role for Tgfbr2 in the development of the intervertebral disc. BMC developmental biology. 2010;10:29. doi: 10.1186/1471-213X-10-2920214815; PubMed Central PMCID: PMC2848151.
9. Harradine KA, Akhurst RJ, Mutations of TGFbeta signaling molecules in human disease. Annals of medicine. 2006;38(6):403–14. doi: 10.1080/0785389060091991117008304.
10. Li J, Yoon ST, Hutton WC, Effect of bone morphogenetic protein-2 (BMP-2) on matrix production, other BMPs, and BMP receptors in rat intervertebral disc cells. Journal of spinal disorders & techniques. 2004;17(5):423–8. 15385883.
11. Wang EA, Rosen V, D'Alessandro JS, Bauduy M, Cordes P, Harada T, et al. Recombinant human bone morphogenetic protein induces bone formation. Proceedings of the National Academy of Sciences of the United States of America. 1990;87(6):2220–4. 2315314; PubMed Central PMCID: PMC53658.
12. Sugimoto Y, Takimoto A, Akiyama H, Kist R, Scherer G, Nakamura T, et al. Scx+/Sox9+ progenitors contribute to the establishment of the junction between cartilage and tendon/ligament. Development. 2013;140(11):2280–8. doi: 10.1242/dev.09635423615282.
13. Stossel TP, Condeelis J, Cooley L, Hartwig JH, Noegel A, Schleicher M, et al. Filamins as integrators of cell mechanics and signalling. Nature reviews Molecular cell biology. 2001;2(2):138–45. doi: 10.1038/3505208211252955.
14. Sasaki A, Masuda Y, Ohta Y, Ikeda K, Watanabe K, Filamin associates with Smads and regulates transforming growth factor-beta signaling. The Journal of biological chemistry. 2001;276(21):17871–7. doi: 10.1074/jbc.M00842220011278410.
15. Zheng L, Baek HJ, Karsenty G, Justice MJ, Filamin B represses chondrocyte hypertrophy in a Runx2/Smad3-dependent manner. The Journal of cell biology. 2007;178(1):121–8. doi: 10.1083/jcb.20070311317606870; PubMed Central PMCID: PMC2064428.
16. Krakow D, Robertson SP, King LM, Morgan T, Sebald ET, Bertolotto C, et al. Mutations in the gene encoding filamin B disrupt vertebral segmentation, joint formation and skeletogenesis. Nature genetics. 2004;36(4):405–10. doi: 10.1038/ng131914991055.
17. Farrington-Rock C, Kirilova V, Dillard-Telm L, Borowsky AD, Chalk S, Rock MJ, et al. Disruption of the Flnb gene in mice phenocopies the human disease spondylocarpotarsal synostosis syndrome. Human molecular genetics. 2008;17(5):631–41. doi: 10.1093/hmg/ddm18817635842; PubMed Central PMCID: PMC2680151.
18. Langer LO, Jr.Gorlin RJ, Donnai D, Hamel BC, Clericuzio C, Spondylocarpotarsal synostosis syndrome (with or without unilateral unsegmented bar). American journal of medical genetics. 1994;51(1):1–8. doi: 10.1002/ajmg.13205101028030662.
19. Seaver LH, Boyd E, Spondylocarpotarsal synostosis syndrome and cervical instability. American journal of medical genetics. 2000;91(5):340–4. 10766994.
20. Dahia CL, Mahoney EJ, Durrani AA, Wylie C, Postnatal growth, differentiation, and aging of the mouse intervertebral disc. Spine. 2009;34(5):447–55. doi: 10.1097/BRS.0b013e3181990c6419247165.
21. Pryce BA, Brent AE, Murchison ND, Tabin CJ, Schweitzer R, Generation of transgenic tendon reporters, ScxGFP and ScxAP, using regulatory elements of the scleraxis gene. Developmental dynamics: an official publication of the American Association of Anatomists. 2007;236(6):1677–82. doi: 10.1002/dvdy.2117917497702.
22. Lee MK, Pardoux C, Hall MC, Lee PS, Warburton D, Qing J, et al. TGF-beta activates Erk MAP kinase signalling through direct phosphorylation of ShcA. The EMBO journal. 2007;26(17):3957–67. doi: 10.1038/sj.emboj.760181817673906; PubMed Central PMCID: PMC1994119.
23. Ivkovic S, Yoon BS, Popoff SN, Safadi FF, Libuda DE, Stephenson RC, et al. Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development. 2003;130(12):2779–91. 12736220; PubMed Central PMCID: PMC3360973.
24. Leivonen SK, Hakkinen L, Liu D, Kahari VM, Smad3 and extracellular signal-regulated kinase 1/2 coordinately mediate transforming growth factor-beta-induced expression of connective tissue growth factor in human fibroblasts. The Journal of investigative dermatology. 2005;124(6):1162–9. doi: 10.1111/j.0022-202X.2005.23750.x15955090.
25. Pardali K, Kowanetz M, Heldin CH, Moustakas A, Smad pathway-specific transcriptional regulation of the cell cycle inhibitor p21(WAF1/Cip1). Journal of cellular physiology. 2005;204(1):260–72. doi: 10.1002/jcp.2030415690394.
26. Liu C, Goswami M, Talley J, Chesser-Martinez PL, Lou CH, Sater AK, TAK1 promotes BMP4/Smad1 signaling via inhibition of erk MAPK: a new link in the FGF/BMP regulatory network. Differentiation; research in biological diversity. 2012;83(4):210–9. doi: 10.1016/j.diff.2011.12.00722387344.
27. Brugger SM, Merrill AE, Torres-Vazquez J, Wu N, Ting MC, Cho JY, et al. A phylogenetically conserved cis-regulatory module in the Msx2 promoter is sufficient for BMP-dependent transcription in murine and Drosophila embryos. Development. 2004;131(20):5153–65. doi: 10.1242/dev.0139015459107.
28. Hu J, Lu J, Lian G, Zhang J, Hecht JL, Sheen VL, Filamin B regulates chondrocyte proliferation and differentiation through Cdk1 signaling. PloS one. 2014;9(2):e89352. doi: 10.1371/journal.pone.008935224551245; PubMed Central PMCID: PMC3925234.
29. Stickens D, Behonick DJ, Ortega N, Heyer B, Hartenstein B, Yu Y, et al. Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development. 2004;131(23):5883–95. doi: 10.1242/dev.0146115539485; PubMed Central PMCID: PMC2771178.
30. Tachi K, Takami M, Sato H, Mochizuki A, Zhao B, Miyamoto Y, et al. Enhancement of bone morphogenetic protein-2-induced ectopic bone formation by transforming growth factor-beta1. Tissue engineering Part A. 2011;17(5–6):597–606. doi: 10.1089/ten.TEA.2010.009420874259.
31. Harper JW, Elledge SJ, Keyomarsi K, Dynlacht B, Tsai LH, Zhang P, et al. Inhibition of cyclin-dependent kinases by p21. Molecular biology of the cell. 1995;6(4):387–400. 7626805; PubMed Central PMCID: PMC301199.
32. Stewart MC, Farnum CE, MacLeod JN, Expression of p21CIP1/WAF1 in chondrocytes. Calcified tissue international. 1997;61(3):199–204. 9262510.
33. O'Rahilly R, Müller F, Human embryology & teratology. 3rd ed.New York: Wiley-Liss; 2001. xii, 505 p. p.
34. Blitz E, Viukov S, Sharir A, Shwartz Y, Galloway JL, Pryce BA, et al. Bone ridge patterning during musculoskeletal assembly is mediated through SCX regulation of Bmp4 at the tendon-skeleton junction. Developmental cell. 2009;17(6):861–73. doi: 10.1016/j.devcel.2009.10.01020059955; PubMed Central PMCID: PMC3164485.
35. Tolonen J, Gronblad M, Vanharanta H, Virri J, Guyer RD, Rytomaa T, et al. Growth factor expression in degenerated intervertebral disc tissue. An immunohistochemical analysis of transforming growth factor beta, fibroblast growth factor and platelet-derived growth factor. European spine journal: official publication of the European Spine Society, the European Spinal Deformity Society, and the European Section of the Cervical Spine Research Society. 2006;15(5):588–96. doi: 10.1007/s00586-005-0930-615980999; PubMed Central PMCID: PMC3489346.
36. Colombier P, Clouet J, Hamel O, Lescaudron L, Guicheux J, The lumbar intervertebral disc: from embryonic development to degeneration. Joint, bone, spine: revue du rhumatisme. 2014;81(2):125–9. doi: 10.1016/j.jbspin.2013.07.01223932724.
37. Smith LJ, Nerurkar NL, Choi KS, Harfe BD, Elliott DM, Degeneration and regeneration of the intervertebral disc: lessons from development. Disease models & mechanisms. 2011;4(1):31–41. doi: 10.1242/dmm.00640321123625; PubMed Central PMCID: PMC3008962.
38. Clouet J, Pot-Vaucel M, Grimandi G, Masson M, Lesoeur J, Fellah BH, et al. Characterization of the age-dependent intervertebral disc changes in rabbit by correlation between MRI, histology and gene expression. BMC musculoskeletal disorders. 2011;12:147. doi: 10.1186/1471-2474-12-14721726455; PubMed Central PMCID: PMC3150337.
39. van de Laar IM, Oldenburg RA, Pals G, Roos-Hesselink JW, de Graaf BM, Verhagen JM, et al. Mutations in SMAD3 cause a syndromic form of aortic aneurysms and dissections with early-onset osteoarthritis. Nature genetics. 2011;43(2):121–6. doi: 10.1038/ng.74421217753.
40. Hadjipavlou AG, Tzermiadianos MN, Bogduk N, Zindrick MR, The pathophysiology of disc degeneration: a critical review. The Journal of bone and joint surgery British volume. 2008;90(10):1261–70. doi: 10.1302/0301-620X.90B10.2091018827232.
41. McLeod MJ, Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology. 1980;22(3):299–301. doi: 10.1002/tera.14202203066165088.
42. Meller M, Vadachkoria S, Luthy DA, Williams MA, Evaluation of housekeeping genes in placental comparative expression studies. Placenta. 2005;26(8–9):601–7. doi: 10.1016/j.placenta.2004.09.00916085039.