Digit patterning during limb development as a result of the BMP-receptor interaction

Scientific Reports

Volumn 2, Issue , 2012, Pages

  Badugu, Amarendra ^a   Kraemer, Conradin ^a   Germann, Philipp ^a,b   Menshykau, Denis ^a   Iber, Dagmar ^a,b  

^a ETH ZURICH   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR; FIBROBLAST GROWTH FACTOR; SMAD4 PROTEIN; SOX9 PROTEIN, MOUSE; TRANSCRIPTION FACTOR SOX9;

ALGORITHM; ANIMAL; ANIMAL EMBRYO; ARTICLE; BIOLOGICAL MODEL; ECTODERM; EMBRYO DEVELOPMENT; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; LIMB BUD; METABOLISM; MORPHOGENESIS; MOUSE; PHYSIOLOGY;

ALGORITHMS; ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEIN RECEPTORS; BONE MORPHOGENETIC PROTEINS; ECTODERM; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FIBROBLAST GROWTH FACTORS; LIMB BUDS; MICE; MODELS, BIOLOGICAL; MORPHOGENESIS; SMAD4 PROTEIN; SOX9 TRANSCRIPTION FACTOR;

EID: 84871779767     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep00991     Document Type: Article

References (104)

1. Bénazet, J.-D. & Zeller, R. Vertebrate limb development: moving from classical morphogen gradients to an integrated 4-dimensional patterning system. Cold Spring Harbor perspectives in biology 1, a001339 (2009).
2. Zeller, R., López-Ríos, J. & Zuniga, A. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat Rev Genet 10, 845-858 (2009).
3. Tickle, C. The number of polarizing region cells required to specify additional digits in the developing chick wing. Nature 289, 295-298 (1981). (Pubitemid 11180678)
4. Wolpert, L. Positional information and the spatial pattern of cellular differentiation. Journal of theoretical biology 25, 1-47 (1969).
5. Riddle, R. D., Johnson, R. L., Laufer, E. & Tabin, C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416 (1993). (Pubitemid 24021914)
6. López-Martínez, A. et al. Limb-patterning activity and restricted posterior localization of the amino-terminal product of Sonic hedgehog cleavage. Current biology : CB 5, 791-796 (1995).
7. Harfe, B. D. et al. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118, 517-528 (2004). (Pubitemid 39485670)
8. Kraus, P., Fraidenraich, D. & Loomis, C. A. Some distal limb structures develop in mice lacking Sonic hedgehog signaling. Mechanisms of development 100, 45-58 (2001).
9. Büscher, D., Bosse, B., Heymer, J. & Rüther, U. Evidence for genetic control of Sonic hedgehog by Gli3 in mouse limb development. Mechanisms of development 62, 175-182 (1997). (Pubitemid 27215786)
10. Litingtung, Y., Dahn, R. D., Li, Y., Fallon, J. F. & Chiang, C. Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature 418, 979-983 (2002). (Pubitemid 34976033)
11. Zhu, J. et al. Uncoupling Sonic hedgehog control of pattern and expansion of the developing limb bud. Dev Cell 14, 624-632 (2008). (Pubitemid 351479933)
12. Ahn, S. & Joyner, A. L. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 118, 505-516 (2004). (Pubitemid 39485669)
13. Ede, D. A. & Law, J. T. Computer simulation of vertebrate limb morphogenesis. Nature 221, 244-248 (1969).
14. Boehm, B. et al. The role of spatially controlled cell proliferation in limb bud morphogenesis. PLoS Biol 8, e1000420 (2010).
15. Dillon, R. & Othmer, H. G. A mathematical model for outgrowth and spatial patterning of the vertebrate limb bud. Journal of theoretical biology 197, 295-330 (1999). (Pubitemid 29150142)
16. Morishita, Y. & Iwasa, Y. Growth based morphogenesis of vertebrate limb bud. Bulletin of mathematical biology 70, 1957-1978 (2008).
17. Hirashima, T., Iwasa, Y. & Morishita, Y. Distance between AER and ZPA is defined by feedforward loop and is stabilized by their feedback loop in vertebrate limb bud. Bulletin of mathematical biology 70, 438-459 (2008).
18. Probst, S. et al. SHH propagates distal limb bud development by enhancing CYP26B1-mediated retinoic acid clearance via AER-FGF signalling. Development (Cambridge, England) 138, 1913-1923 (2011).
19. Dillon, R., Gadgil, C. & Othmer, H. G. Short- and long-range effects of Sonic hedgehog in limb development. Proc. Natl. Acad. Sci USA 100, 10152-10157 (2003). (Pubitemid 37071848)
20. Newman, S. A. Limb pattern, physical mechanisms and morphological evolution - an interview with Stuart A. Newman. Interviewed by Chuong, Cheng-Ming. (2009).
21. Alber, M. et al. The morphostatic limit for amodel of skeletal pattern formation in the vertebrate limb. Bulletin of mathematical biology 70, 460-483 (2008).
22. Miura, T., Shiota, K., Morriss-Kay, G. & Maini, P. K. Mixed-mode pattern in Doublefoot mutant mouse limb-Turing reaction-diffusion model on a growing domain during limb development. Journal of theoretical biology 240, 562-573 (2006). (Pubitemid 43765938)
23. Hentschel, H. G. E., Glimm, T., Glazier, J. A. & Newman, S. A. Dynamical mechanisms for skeletal pattern formation in the vertebrate limb. Proc Biol Sci 271, 1713-1722 (2004). (Pubitemid 39107992)
24. Miura, T. & Maini, P. K. Speed of pattern appearance in reaction-diffusion models: implications in the pattern formation of limb bud mesenchyme cells. Bulletin of mathematical biology 66, 627-649 (2004). (Pubitemid 38800942)
25. Oster, G. F., Murray, J. D.&Maini, P. K. Amodel for chondrogenic condensations in the developing limb: the role of extracellular matrix and cell tractions. Journal of embryology and experimental morphology 89, 93-112 (1985). (Pubitemid 16211082)
26. Oster, G. F., Murray, J. D. & Harris, A. K. Mechanical aspects of mesenchymal morphogenesis. Journal of embryology and experimental morphology 78, 83-125 (1983). (Pubitemid 14213256)
27. Izaguirre, J. A. et al. CompuCell, a multi-model framework for simulation of morphogenesis. Bioinformatics (Oxford, England) 20, 1129-1137 (2004). (Pubitemid 38660350)
28. Chaturvedi, R. et al. Onmultiscale approaches to three-dimensional modelling of morphogenesis. J R Soc Interface 2, 237-253 (2005).
29. Christley, S., Alber, M. S.&Newman, S. A. Patterns of mesenchymal condensation in a multiscale, discrete stochastic model. Plos Computational Biology 3, e76 (2007).
30. Maini, P. K. & Solursh, M. Cellular mechanisms of pattern formation in the developing limb. International review of cytology 129, 91-133 (1991).
31. Newman, S. A. et al.Multiscale models for vertebrate limb development. Current topics in developmental biology 81, 311-340 (2008).
32. Turing, A. The chemical basis of morphogenesis. Phil. Trans. Roy. Soc. Lond B237, 37-72 (1952).
33. Kondo, S. & Miura, T. Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329, 1616-1620 (2010).
34. Newman, S. A. & Frisch, H. L. Dynamics of skeletal pattern formation in developing chick limb. Science 205, 662-668 (1979). (Pubitemid 9253853)
35. Zhu, J., Zhang, Y.-T., Alber, M. S. & Newman, S. A. Bare bones pattern formation: a core regulatory network in varying geometries reproduces major features of vertebrate limb development and evolution. PLoS ONE 5, e10892 (2010).
36. Spagnoli, A. et al. TGF-beta signaling is essential for joint morphogenesis. J Cell Biol 177, 1105-1117 (2007). (Pubitemid 46955713)
37. Lewandoski, M., Sun, X. &Martin, G. R. Fgf8 signalling from the AER is essential for normal limb development. Nat Genet 26, 460-463 (2000).
38. Moon, A. M. & Capecchi, M. R. Fgf8 is required for outgrowth and patterning of the limbs. Nat Genet 26, 455-459 (2000).
39. Sun, X. et al. Conditional inactivation of Fgf4 reveals complexity of signalling during limb bud development. Nat Genet 25, 83-86 (2000). (Pubitemid 30257042)
40. Brunet, L. J., McMahon, J. A.,McMahon, A. P. & Harland, R. M. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science 280, 1455-1457 (1998). (Pubitemid 28264842)
41. Xu, J., Krebs, L. T.&Gridley, T. Generation of mice with a conditional null allele of the Jagged2 gene. Genesis (New York, NY : 2000) 48, 390-393 (2010).
42. Nakayama, N. et al. A novel chordin-like BMP inhibitor, CHL2, expressed preferentially in chondrocytes of developing cartilage and osteoarthritic joint cartilage. Development (Cambridge, England) 131, 229-240 (2004). (Pubitemid 38111429)
43. Towers, M. & Tickle, C. Growing models of vertebrate limb development. Development (Cambridge, England) 136, 179-190 (2009).
44. Kawakami, Y. et al. Transcriptional coactivator PGC-1alpha regulates chondrogenesis via association with Sox9. Proc. Natl. Acad. Sci USA 102, 2414-2419 (2005). (Pubitemid 40279390)
45. Stricker, S. & Mundlos, S. Mechanisms of digit formation: Human malformation syndromes tell the story. Developmental dynamics : an official publication of the American Association of Anatomists 240, 990-1004 (2011).
46. Healy, C., Uwanogho, D. & Sharpe, P. T. Regulation and role of Sox9 in cartilage formation. Developmental dynamics : an official publication of the American Association of Anatomists 215, 69-78 (1999). (Pubitemid 29215705)
47. Zehentner, B. K., Haussmann, A. & Burtscher, H. The bone morphogenetic protein antagonist Noggin is regulated by Sox9 during endochondral differentiation. Development, growth & differentiation 44, 1-9 (2002). (Pubitemid 34123318)
48. Zimmerman, L. B., De Jesús-Escobar, J. M. & Harland, R. M. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599-606 (1996). (Pubitemid 26299491)
49. Pereira, R. C., Economides, A. N. & Canalis, E. Bone morphogenetic proteins induce gremlin, a protein that limits their activity in osteoblasts. Endocrinology 141, 4558-4563 (2000). (Pubitemid 32055134)
50. Weatherbee, S. D., Behringer, R. R., Rasweiler, J. J. & Niswander, L. A. Interdigital webbing retention in bat wings illustrates genetic changes underlying amniote limb diversification. Proceedings of the National Academy of Sciences of the United States of America 103, 15103-15107 (2006). (Pubitemid 44583171)
51. Nissim, S., Hasso, S. M., Fallon, J. F. & Tabin, C. J. Regulation of Gremlin expression in the posterior limb bud. Developmental Biology 299, 12-21 (2006). (Pubitemid 44528396)
52. Liu, W. et al. Threshold-specific requirements for Bmp4 in mandibular development. Developmental Biology 283, 282-293 (2005). (Pubitemid 40977949)
53. Pajni-Underwood, S., Wilson, C. P., Elder, C.,Mishina, Y. &Lewandoski, M. BMP signals control limb bud interdigital programmed cell death by regulating FGF signaling. Development (Cambridge, England) 134, 2359-2368 (2007). (Pubitemid 47010024)
54. ten Dijke, P. et al. Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. The Journal of biological chemistry 269, 16985-16988 (1994). (Pubitemid 24204009)
55. Yamaji, N. et al. A mammalian serine/threonine kinase receptor specifically binds BMP-2 and BMP-4. Biochemical and biophysical research communications 205, 1944-1951 (1994).
56. Verschueren, K. et al. Expression of type I and type IB receptors for activin in midgestation mouse embryos suggests distinct functions in organogenesis. Mechanisms of development 52, 109-123 (1995).
57. Greenwald, J. et al. The BMP7/ActRII extracellular domain complex provides new insights into the cooperative nature of receptor assembly. Mol Cell 11, 605-617 (2003). (Pubitemid 36385117)
58. Baur, S. T., Mai, J. J. & Dymecki, S. M. Combinatorial signaling through BMP receptor IB and GDF5: shaping of the distal mouse limb and the genetics of distal limb diversity. Development (Cambridge, England) 127, 605-619 (2000). (Pubitemid 30093408)
59. Montero, J. A., Lorda-Diez, C. I., Gañan, Y., Macias, D. & Hurle, J. M. Activin/TGFbeta and BMP crosstalk determines digit chondrogenesis. Developmental Biology 321, 343-356 (2008).
60. Yoon, B. S. et al. Bmpr1a andBmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proceedings of the National Academy of Sciences of the United States of America 102, 5062-5067 (2005).
61. Kawakami, Y. et al. BMP signaling during bone pattern determination in the developing limb. Development (Cambridge, England) 122, 3557-3566 (1996). (Pubitemid 26395997)
62. Merino, R. et al. Morphogenesis of digits in the avian limb is controlled by FGFs, TGFbetas, and noggin through BMP signaling. Developmental Biology 200, 35-45 (1998). (Pubitemid 28374690)
63. Ovchinnikov, D. A. et al.BMPreceptor type IA in limb bud mesenchyme regulates distal outgrowth and patterning. Developmental Biology 295, 103-115 (2006). (Pubitemid 44041328)
64. Yi, S. E., Daluiski, A., Pederson, R., Rosen, V. & Lyons, K. M. The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb. Development (Cambridge, England) 127, 621-630 (2000). (Pubitemid 30093409)
65. Robert, B. Bone morphogenetic protein signaling in limb outgrowth and patterning. Development, growth & differentiation 49, 455-468 (2007). (Pubitemid 47174209)
66. Bandyopadhyay, A. et al. Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS genetics 2, e216 (2006).
67. Selever, J., Liu, W., Lu, M.-F., Behringer, R. R. & Martin, J. F. Bmp4 in limb bud mesoderm regulates digit pattern by controlling AER development. Developmental Biology 276, 268-279 (2004). (Pubitemid 39592393)
68. Bénazet, J.-D. et al. A self-regulatory system of interlinked signaling feedback loops controls mouse limb patterning. Science 323, 1050-1053 (2009).
69. Bénazet, J.-D. et al. Smad4 is required to induce digit ray primordia and to initiate the aggregation and differentiation of chondrogenic progenitors in mouse limb buds. Development (Cambridge, England) 139, 4250-4260 (2012).
70. Yoon, B. S. et al. BMPs regulate multiple aspects of growth-plate chondrogenesis through opposing actions on FGF pathways. Development (Cambridge, England) 133, 4667-4678 (2006). (Pubitemid 46063079)
71. Verheyden, J. M. & Sun, X. An Fgf/Gremlin inhibitory feedback loop triggers termination of limb bud outgrowth. Nature 454, 638-641 (2008).
72. Zeller, R. The temporal dynamics of vertebrate limb development, teratogenesis and evolution. Curr Opin Genet Dev 20, 384-390 (2010).
73. Zúñiga, A. & Zeller, R. Gli3 (Xt) and formin (ld) participate in the positioning of the polarising region and control of posterior limb-bud identity. Development (Cambridge, England) 126, 13-21 (1999). (Pubitemid 29045896)
74. Glimm, T., Zhang, J., Shen, Y.-Q. & Newman, S. A. Reaction-diffusion systems and external morphogen gradients: the two-dimensional case, with an application to skeletal pattern formation. Bulletin of mathematical biology 74, 666-687 (2012).
75. Kicheva, A. et al. Kinetics of morphogen gradient formation. Science 315, 521-525 (2007). (Pubitemid 46175757)
76. Kumar, M., Mommer, M. S. & Sourjik, V. Mobility of Cytoplasmic, Membrane, and DNA-Binding Proteins in Escherichia coli. Biophysical journal 98, 552-559 (2010).
77. Hebert, B., Costantino, S. & Wiseman, P. Spatiotemporal image correlation Spectroscopy (STICS) theory, verification, and application to protein velocity mapping in living CHO cells. Biophysical journal 88, 3601-3614 (2005). (Pubitemid 40586608)
78. Scheufler, C., Sebald, W. & Hülsmeyer, M. Crystal structure of human bone morphogenetic protein-2 at 2.7 A resolution. Journal of molecular biology 287, 103-115 (1999). (Pubitemid 29134800)
79. Bastida, M. F., Sheth, R. & Ros, M. A. A BMP-Shh negative-feedback loop restricts Shh expression during limb development. Development (Cambridge, England) 136, 3779-3789 (2009).
80. Michos, O. et al. Gremlin-mediated BMP antagonism induces the epithelialmesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development (Cambridge, England) 131, 3401-3410 (2004). (Pubitemid 39139886)
81. Sun, J. et al. BMP4 activation and secretion are negatively regulated by an intracellular gremlin-BMP4 interaction. The Journal of biological chemistry 281, 29349-29356 (2006). (Pubitemid 44507078)
82. Sudo, S., Avsian-Kretchmer, O.,Wang, L. S. & Hsueh, A. J. W. Protein related to DANand cerberus is a bonemorphogenetic protein antagonist that participates in ovarian paracrine regulation. The Journal of biological chemistry 279, 23134-23141 (2004). (Pubitemid 38685618)
83. Yu, S. R. et al. Fgf8 morphogen gradient forms by a source-sink mechanism with freely diffusing molecules. Nature 461, 533-536 (2009).
84. Duprez, D. M., Kostakopoulou, K., Francis-West, P. H., Tickle, C.&Brickell, P. M. Activation of Fgf-4 and HoxD gene expression by BMP-2 expressing cells in the developing chick limb. Development (Cambridge, England) 122, 1821-1828 (1996). (Pubitemid 26192747)
85. Dudley, A. T. & Tabin, C. J. Constructive antagonism in limb development. Curr Opin Genet Dev 10, 387-392 (2000). (Pubitemid 30450041)
86. Kicheva, A. et al. Kinetics of morphogen gradient formation. Science 315, 521-525 (2007). (Pubitemid 46175757)
87. Yu, S. R. et al. Fgf8 morphogen gradient forms by a source-sink mechanism with freely diffusing molecules. Nature 461, 533-537 (2009).
88. Ries, J., Yu, S. R., Burkhardt, M., Brand, M. & Schwille, P. Modular scanning fcs quantifies receptor-ligand interactions in living multicellular organisms. Nat Methods 6, 643-U31 (2009).
89. R, A. Vectors, Tensors and the Basic Equations of Fluid Mechanics. (Dover Publications, 1989).
90. Murray, J. D. Mathematical Biology. 3rd edition in 2 volumes: Mathematical Biology: II. Spatial Models and Biomedical Applications. (Springer, 2003).
91. Pan, Q. et al. Sox9, a key transcription factor of bone morphogenetic protein-2- induced chondrogenesis, is activated through BMP pathway and a CCAAT box in the proximal promoter. Journal of cellular physiology 217, 228-241 (2008).
92. Niswander, L. & Martin, G. R. FGF-4 and BMP-2 have opposite effects on limb growth. Nature 361, 68-71 (1993). (Pubitemid 23020775)
93. Boulet, A. M.,Moon, A. M.,Arenkiel, B. R.&Capecchi, M. R. The roles of Fgf4 and Fgf8 in limb bud initiation and outgrowth. Developmental Biology 273, 361-372 (2004). (Pubitemid 39140909)
94. Moon, A. M., Boulet, A. M. & Capecchi, M. R. Normal limb development in conditional mutants of Fgf4. Development (Cambridge, England) 127, 989-996 (2000). (Pubitemid 30162645)
95. Lu, P., Minowada, G. & Martin, G. R. Increasing Fgf4 expression in the mouse limb bud causes polysyndactyly and rescues the skeletal defects that result from loss of Fgf8 function. Development (Cambridge, England) 133, 33-42 (2006). (Pubitemid 43169318)
96. Menshykau, D., Kraemer, C. & Iber, D. Branch Mode Selection during Early Lung Development. Plos Computational Biology 8, e1002377 (2012).
97. Affolter, M., Zeller, R. & Caussinus, E. Tissue remodelling through branching morphogenesis. Nat Rev Mol Cell Biol 10, 831-842 (2009).
98. Sharpe, J. et al. Optical Projection Tomography as a Tool for 3D Microscopy and Gene Expression Studies. Science 296, 541-545 (2002). (Pubitemid 34408675)
99. Cutress, I. J., Dickinson, E. J. F. & Compton, R. G. Analysis of commercial general engineering finite element software in electrochemical simulations. J Electroanal Chem 638, 76-83 (2010).
100. Carin, M. Numerical Simulation of Moving Boundary Problems with the ALE Method: Validation in the Case of a Free Surface and a Moving Solidification Front. Excert from the Proceedings of the COMSOL Conference (2006).
101. Thummler, V. &Weddemann, A. Computation of Space-Time Patterns via ALE Methods. Excert from the Proceedings of the COMSOL Conference (2007).
102. Weddemann, A. & Thummler, V. Stability Analysis of ALE-Methods for Advection-Diffusion Problems. Excert from the Proceedings of the COMSOL Conference (2008).
103. Germann, P., Menshykau, D., Tanaka, S. & Iber, D. Simulating organogensis in Comsol. Proceedings of COMSOL Conference 2011 (2011).
104. Bangs, F. et al. Generation of mice with functional inactivation of talpid3, a gene first identified in chicken. Development (Cambridge, England) 138, 3261-3272 (2011).