Cdc42 is required for chondrogenesis and interdigital programmed cell death during limb development

Mechanisms of Development

Volumn 129, Issue 1-4, 2012, Pages 38-50

  Aizawa, Ryo ^a   Yamada, Atsushi ^a   Suzuki, Dai ^a   Iimura, Tadahiro ^b   Kassai, Hidetoshi ^c,d   Harada, Takeshi ^c,d   Tsukasaki, Masayuki ^a   Yamamoto, Gou ^a   Tachikawa, Tetsuhiko ^a   Nakao, Kazuki ^d,e   Yamamoto, Matsuo ^a   Yamaguchi, Akira ^b   Aiba, Atsu ^c,d   Kamijo, Ryutaro ^a  

^a SHOWA UNIVERSITY   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

Cdc42; Chondrogenesis; Conditional knockout mice; Limb development; Programmed cell death

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; COLLAGENASE 3; PROTEIN CDC42; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR MSX2; TRANSCRIPTION FACTOR SOX9;

ANATOMICAL VARIATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE DEFECT; BONE GROWTH; BONE MINERALIZATION; CARTILAGE; CARTILAGE CELL; CELL DIFFERENTIATION; CHONDROGENESIS; CLEFT PALATE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; IN SITU HYBRIDIZATION; LIMB DEVELOPMENT; LONG BONE; MOUSE; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SKULL; STERNUM; SYNDACTYLY;

ANIMALS; APOPTOSIS; BODY PATTERNING; BONE MORPHOGENETIC PROTEIN 2; CDC42 GTP-BINDING PROTEIN; CELL DIFFERENTIATION; CHONDROGENESIS; FEMALE; FOOT; FOOT DEFORMITIES, CONGENITAL; GENE EXPRESSION; GROWTH PLATE; LIMB BUDS; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, INBRED ICR; MICE, TRANSGENIC; MSX1 TRANSCRIPTION FACTOR;

MAMMALIA; MUS;

EID: 84861344070     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2012.02.002     Document Type: Article

References (50)

1. Bandyopadhyay A., Tsuji K., Cox K., Harfe B.D., Rosen V., Tabin C.J. Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS Genet. 2006, 2:e216.
2. Bastida M.F., Sheth R., Ros M.A. A BMP-Shh negative-feedback loop restricts Shh expression during limb development. Development 2009, 136:3779-3789.
3. Bishop A.L., Hall A. Rho GTPases and their effector proteins. Biochem. J. 2000, 348(Pt 2):241-255.
4. Burridge K., Wennerberg K. Rho and Rac take center stage. Cell 2004, 116:167-179.
5. Capdevila J., Izpisua Belmonte J.C. Patterning mechanisms controlling vertebrate limb development. Annu. Rev. Cell Dev. Biol. 2001, 17:87-132.
6. Chai Y., Jiang X., Ito Y., Bringas P., Han J., Rowitch D.H., Soriano P., McMahon A.P., Sucov H.M. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 2000, 127:1671-1679.
7. Chen F., Ma L., Parrini M.C., Mao X., Lopez M., Wu C., Marks P.W., Davidson L., Kwiatkowski D.J., Kirchhausen T., Orkin S.H., Rosen F.S., Mayer B.J., Kirschner M.W., Alt F.W. Cdc42 is required for PIP(2)-induced actin polymerization and early development but not for cell viability. Curr. Biol. 2000, 10:758-765.
8. Chen Y., Zhao X. Shaping limbs by apoptosis. J. Exp. Zool. 1998, 282:691-702.
9. DeLise A.M., Fischer L., Tuan R.S. Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage 2000, 8:309-334.
10. Erlebacher A., Filvaroff E.H., Gitelman S.E., Derynck R. Toward a molecular understanding of skeletal development. Cell 1995, 80:371-378.
11. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
12. Fernandez-Teran M.A., Hinchliffe J.R., Ros M.A. Birth and death of cells in limb development: a mapping study. Dev. Dyn. 2006, 235:2521-2537.
13. Francis-West P.H., Antoni L., Anakwe K. Regulation of myogenic differentiation in the developing limb bud. J. Anat. 2003, 202:69-81.
14. Furusawa T., Lim J.H., Catez F., Birger Y., Mackem S., Bustin M. Down-regulation of nucleosomal binding protein HMGN1 expression during embryogenesis modulates Sox9 expression in chondrocytes. Mol. Cell. Biol. 2006, 26:592-604.
15. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998, 279:509-514.
16. Hall B.K., Miyake T. All for one and one for all: condensations and the initiation of skeletal development. BioEssays 2000, 22:138-147.
17. Hattori T., Muller C., Gebhard S., Bauer E., Pausch F., Schlund B., Bosl M.R., Hess A., Surmann-Schmitt C., von der Mark H., de Crombrugghe B., von der Mark K. SOX9 is a major negative regulator of cartilage vascularization, bone marrow formation and endochondral ossification. Development 2010, 137:901-911.
18. Heasman S.J., Ridley A.J. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 2008, 9:690-701.
19. Hernandez-Martinez R., Covarrubias L. Interdigital cell death function and regulation: new insights on an old programmed cell death model. Dev. Growth Differ. 2011, 53:245-258.
20. Houzelstein D., Cohen A., Buckingham M.E., Robert B. Insertional mutation of the mouse Msx1 homeobox gene by an nlacZ reporter gene. Mech. Dev. 1997, 65:123-133.
21. Ito Y., Teitelbaum S.L., Zou W., Zheng Y., Johnson J.F., Chappel J., Ross F.P., Zhao H. Cdc42 regulates bone modeling and remodeling in mice by modulating RANKL/M-CSF signaling and osteoclast polarization. J. Clin. Invest. 2010, 120:1981-1993.
22. Karsenty G. The complexities of skeletal biology. Nature 2003, 423:316-318.
23. Kronenberg H.M. Developmental regulation of the growth plate. Nature 2003, 423:332-336.
24. LaLonde D.P., Grubinger M., Lamarche-Vane N., Turner C.E. CdGAP associates with actopaxin to regulate integrin-dependent changes in cell morphology and motility. Curr. Biol. 2006, 16:1375-1385.
25. Logan M., Martin J.F., Nagy A., Lobe C., Olson E.N., Tabin C.J. Expression of Cre recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 2002, 33:77-80.
26. Maatouk D.M., Choi K.S., Bouldin C.M., Harfe B.D. In the limb AER Bmp2 and Bmp4 are required for dorsal-ventral patterning and interdigital cell death but not limb outgrowth. Dev. Biol. 2009, 327:516-523.
27. Macias D., Ganan Y., Sampath T.K., Piedra M.E., Ros M.A., Hurle J.M. Role of BMP-2 and OP-1 (BMP-7) in programmed cell death and skeletogenesis during chick limb development. Development 1997, 124:1109-1117.
28. Melendez J., Grogg M., Zheng Y. Signaling role of Cdc42 in regulating mammalian physiology. J. Biol. Chem. 2011, 286:2375-2381.
29. Merino R., Macias D., Ganan Y., Economides A.N., Wang X., Wu Q., Stahl N., Sampath K.T., Varona P., Hurle J.M. Expression and function of Gdf-5 during digit skeletogenesis in the embryonic chick leg bud. Dev. Biol. 1999, 206:33-45.
30. Niswander L. Pattern formation: old models out on a limb. Nat. Rev. Genet. 2003, 4:133-143.
31. Oldfield S.F., Evans D.J. Tendon morphogenesis in the developing avian limb: plasticity of fetal tendon fibroblasts. J. Anat. 2003, 202:153-164.
32. Ovchinnikov D.A., Selever J., Wang Y., Chen Y.T., Mishina Y., Martin J.F., Behringer R.R. BMP receptor type IA in limb bud mesenchyme regulates distal outgrowth and patterning. Dev. Biol. 2006, 295:103-115.
33. Pizette S., Abate-Shen C., Niswander L. BMP controls proximodistal outgrowth, via induction of the apical ectodermal ridge, and dorsoventral patterning in the vertebrate limb. Development 2001, 128:4463-4474.
34. Robert B. Bone morphogenetic protein signaling in limb outgrowth and patterning. Dev. Growth Differ. 2007, 49:455-468.
35. Rodriguez C.I., Buchholz F., Galloway J., Sequerra R., Kasper J., Ayala R., Stewart A.F., Dymecki S.M. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 2000, 25:139-140.
36. Sagai T., Hosoya M., Mizushina Y., Tamura M., Shiroishi T. Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 2005, 132:797-803.
37. Shaheen R., Faqeih E., Sunker A., Morsy H., Al-Sheddi T., Shamseldin H.E., Adly N., Hashem M., Alkuraya F.S. Recessive mutations in DOCK6, encoding the guanidine nucleotide exchange factor DOCK6, lead to abnormal actin cytoskeleton organization and Adams-Oliver syndrome. Am. J. Hum. Genet. 2011, 89:328-333.
38. Shapiro I.M., Adams C.S., Freeman T., Srinivas V. Fate of the hypertrophic chondrocyte: microenvironmental perspectives on apoptosis and survival in the epiphyseal growth plate. Birth Defects Res. C Embryo Today 2005, 75:330-339.
39. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
40. Southgate L., Machado R.D., Snape K.M., Primeau M., Dafou D., Ruddy D.M., Branney P.A., Fisher M., Lee G.J., Simpson M.A., He Y., Bradshaw T.Y., Blaumeiser B., Winship W.S., Reardon W., Maher E.R., Fitzpatrick D.R., Wuyts W., Zenker M., Lamarche-Vane N., Trembath R.C. Gain-of-function mutations of ARHGAP31, a Cdc42/Rac1 GTPase regulator, cause syndromic cutis aplasia and limb anomalies. Am. J. Hum. Genet. 2011, 88:574-585.
41. Spagnoli A., O'Rear L., Chandler R.L., Granero-Molto F., Mortlock D.P., Gorska A.E., Weis J.A., Longobardi L., Chytil A., Shimer K., Moses H.L. TGF-beta signaling is essential for joint morphogenesis. J. Cell Biol. 2007, 177:1105-1117.
42. Suzuki D., Yamada A., Amano T., Yasuhara R., Kimura A., Sakahara M., Tsumaki N., Takeda S., Tamura M., Nakamura M., Wada N., Nohno T., Shiroishi T., Aiba A., Kamijo R. Essential mesenchymal role of small GTPase Rac1 in interdigital programmed cell death during limb development. Dev. Biol. 2009, 335:396-406.
43. Tickle C. Molecular basis of vertebrate limb patterning. Am. J. Med. Genet. 2002, 112:250-255.
44. Wang G., Beier F. Rac1/Cdc42 and RhoA GTPases antagonistically regulate chondrocyte proliferation, hypertrophy, and apoptosis. J. Bone Miner. Res. 2005, 20:1022-1031.
45. Woods A., Wang G., Beier F. Regulation of chondrocyte differentiation by the actin cytoskeleton and adhesive interactions. J. Cell. Physiol. 2007, 213:1-8.
46. Woods A., Wang G., Dupuis H., Shao Z., Beier F. Rac1 signaling stimulates N-cadherin expression, mesenchymal condensation, and chondrogenesis. J. Biol. Chem. 2007, 282:23500-23508.
47. Yamada A., Sheikh F., Niimi T., DeMayo F.J., Keegan A.D., Donnelly R.P., Kimura S. Induction of uteroglobin-related protein 2 (Ugrp2) gene expression by the Th2 cytokines IL-4 and IL-13. J. Immunol. 2005, 175:5708-5715.
48. Zanetti N.C., Solursh M. Induction of chondrogenesis in limb mesenchymal cultures by disruption of the actin cytoskeleton. J. Cell Biol. 1984, 99:115-123.
49. Zhang X., Siclari V.A., Lan S., Zhu J., Koyama E., Dupuis H.L., Enomoto-Iwamoto M., Beier F., Qin L. The critical role of the epidermal growth factor receptor in endochondral ossification. J. Bone Miner. Res. 2011, 26:2622-2633.
50. Zou H., Wieser R., Massague J., Niswander L. Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev. 1997, 11:2191-2203.