Regulation of mesenchymal-to-epithelial transition by PARAXIS during somitogenesis

Developmental Dynamics

Volumn 242, Issue 11, 2013, Pages 1332-1344

  Rowton, Megan ^a   Ramos, Pilar ^a,d   Anderson, Douglas M ^b   Rhee, Jerry M ^c   Cunliffe, Heather E ^d   Rawls, Alan ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c CHILDREN'S MEMORIAL HOSPITAL   (United States)

^d TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

Author keywords

Daam2; Dmrt2; ECM; Expression; Fap; Meox2; Mesenchymal to epithelial transition; MET; PARAXIS; Somitogenesis; TCF15

Indexed keywords

COLLAGEN FIBER; DIPEPTIDYL PEPTIDASE; FIBRONECTIN; NOTCH RECEPTOR; SEPRASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PARAXIS; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; CELL ADHESION; CELL INTERACTION; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; GENE CONTROL; GENE EXPRESSION; MESODERM; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POSITIVE FEEDBACK; PRIORITY JOURNAL; REGULATORY MECHANISM; SOMATIC EMBRYOGENESIS; SOMITE;

VERTEBRATA;

DAAM2; DMRT2; ECM; EXPRESSION; FAP; MEOX2; MESENCHYMAL-TO-EPITHELIAL TRANSITION; MET; PARAXIS; SOMITOGENESIS; TCF15;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; DNA-BINDING PROTEINS; EPITHELIAL-MESENCHYMAL TRANSITION; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GELATINASES; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MEMBRANE PROTEINS; MICE; SERINE ENDOPEPTIDASES; SOMITES; TRANSCRIPTION FACTORS;

EID: 84886291162     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24033     Document Type: Article

References (71)

1. Aertgeerts K, Levin I, Shi L, Snell GP, Jennings A, Prasad GS, Zhang Y, Kraus ML, Salakian S, Sridhar V, Wijnands R, Tennant MG. 2005. Structural and kinetic analysis of the substrate specificity of human fibroblast activation protein alpha. J Biol Chem 280:19441-19444.
2. Anderson DM, Arredondo J, Hahn K, Valente G, Martin JF, Wilson-Rawls J, Rawls A. 2006. Mohawk is a novel homeobox gene expressed in the developing mouse embryo. Dev Dyn 235:792-801.
3. Araujo M, Nieto MA. 1997. The expression of chick EphA7 during segmentation of the central and peripheral nervous system. Mech Dev 68:173-177.
4. Araujo M, Piedra ME, Herrera MT, Ros MA, Nieto MA. 1998. The expression and regulation of chick EphA7 suggests roles in limb patterning and innervation. Development 125:4195-4204.
5. Artym W, Kindzelskii AL, Chen WT, Petty HR. 2002. Molecular proximity of seprase and the urokinase-type plasminogen activator receptor on malignant melanoma cell membranes: dependence on beta1 integrins and the cytoskeleton. Carcinogenesis 23:1593-1601.
6. Barnes GL, Alexander PG, Hsu CW, Mariani BD, Tuan RS. 1997. Cloning and characterization of chicken Paraxis: a regulator of paraxial mesoderm development and somite formation. Dev Biol 189:95-111.
7. Baum B, Georgiou M. 2011. Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J Cell Biol 192:907-917.
8. Belo JA, Bouwmeester T, Leyns L, Kertesz N, Gallo M, Follettie M, De Robertis EM. 1997. Cerberus-like is a secreted factor with neuralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech Dev 68:45-57.
9. Burgess R, Cserjesi P, Ligon KL, Olson EN. 1995. Paraxis: a basic helix-loop-helix protein expressed in paraxial mesoderm and developing somites. Dev Biol 168:296-306.
10. Burgess R, Rawls A, Brown D, Bradley A, Olson EN. 1996. Requirement of the Paraxis gene for somite formation and musculoskeletal patterning. Nature 384:570-573.
11. Carpio R, Honor SM, Araya C, Mayor R. 2004. Xenopus Paraxis homologue shows novel domains of expression. Dev Dyn 231:609-613.
12. Correia KM, Conlon RA. 2000. Surface ectoderm is necessary for the morphogenesis of somites. Mech Dev 91:19-30.
13. Dear TN, Boehm T. 1999. Diverse mRNA expression patterns of the mouse calpain genes Capn5, Capn6 and Capn11 during development. Mech Dev 89:201-209.
14. Della Gaspera B, Armand AS, Lecolle S, Charbonnier F, Chanoine C. 2012. Mef2d acts upstream of muscle identity genes and couples lateral myogenesis to dermomyotome formation in Xenopus laevis. PLoS One 7:e52359.
15. Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207-210.
16. Frayne J, Hurd EA, Hall L. 2002. Human tMDC III: a sperm protein with a potential role in oocyte recognition. Mol Hum Reprod 8:817-822.
17. Fukui Y, Hashimoto O, Sanui T, Oono T, Koga H, Abe M, Inayoshi A, Noda M, Oike M, Shirai T, Sasazuki T. 2001. Haematopoietic cell-specific CDM family protein DOCK2 is essential for lymphocyte migration. Nature 412:826-831.
18. George EL, Georges-Labouesse EN, Patel-King RS, Rayburn H, Hynes RO. 1993. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119:1079-1091.
19. Gray RS, Bayly RD, Green SA, Agarwala S, Lowe CJ, Wallingford JB. 2009. Diversification of the expression patterns and developmental functions of the dishevelled gene family during chordate evolution. Dev Dyn 238:2044-2057.
20. Hall A. 2005. Rho GTPases and the control of cell behaviour. Biochem Soc Trans 33:891-895.
21. Helfman DM, Kim EJ, Lukanidin E, Grigorian M. 2005. The metastasis associated protein S100A4: role in tumour progression and metastasis. Br J Cancer 92:1955-1958.
22. Johnson J, Rhee J, Parsons SM, Brown D, Olson EN, Rawls A. 2001. The anterior/posterior polarity of somites is disrupted in Paraxis-deficient mice. Dev Biol 229:176-187.
23. Jülich D, Geisler R, Tübingen 2000 Screen Consortium, Holley SA. 2005. Integrinalpha5 and delta/notch signaling have complementary spatiotemporal requirements during zebrafish somitogenesis. Dev Cell 8:575-586.
24. Lackmann M, Oates AC, Dottori M, Smith FM, Do C, Power M, Kravets L, Boyd AW. 1998. Distinct subdomains of the EphA3 receptor mediate ligand binding and receptor dimerization. J Biol Chem 273:20228-20237.
25. Lee HK, Deneen B. 2012. Daam2 is required for dorsal patterning via modulation of canonical Wnt signaling in the developing spinal cord. Dev Cell 22:183-196.
26. Lee HO, Mullins SR, Franco-Barraza J, Valianou M, Cukierman E, Cheng JD. 2011. Fap-overexpressing fibroblasts produce an extracellular matrix that enhances invasive velocity and directionality of pancreatic cancer cells. BMC Cancer 11:245.
27. Leimeister C, Schumacher N, Steidl C, Gessler M. 2000. Analysis of HeyL expression in wild-type and Notch pathway mutant mouse embryos. Mech Dev 98:175-178.
28. Levy MT, McCaughan GW, Abbott CA, Park JE, Cunningham AM, Müller E, Rettig WJ, Gorrell MD. 1999. Fibroblast activation protein: a cell surface dipeptidyl peptidase and gelatinase expressed by stellate cells at the tissue remodeling interface in human cirrhosis. Hepatology 29:1768-1778.
29. Linker C, Lesbros C, Gros J, Burrus LW, Rawls A, Marcelle C. 2005. beta-Catenin-dependent Wnt signalling controls the epithelial organisation of somites through the activation of Paraxis. Development 132:3895-3905.
30. Loebel DA, Tsoi B, Wong N, Tam PP. 2005. A conserved noncoding intronic transcript at the mouse Dnm3 locus. Genomics 85:782-789.
31. Mankoo BS. 2003. The concerted action of Meox homeobox genes is required upstream of genetic pathways essential for the formation, patterning and differentiation of somites. Development 130:4655-4664.
32. Maroto M, Bone RA, Dale JK. 2012. Somitogenesis. Development 139:2453-2456.
33. Mikheeva SA, Mikheev AM, Petit A, Beyer R, Oxford RG, Khorasani L, Maxwell JP, Glackin CA, Wakimoto H, González-Herrero I, Sánchez-García I, Silber JR, Horner PJ, Rostomily RC. 2010. TWIST1 promotes invasion through mesenchymal change in human glioblastoma. Mol Cancer 9:194.
34. Mostafavi-Pour Z, Askari JA, Parkinson SJ, Parker PJ, Ng TT, Humphries MJ. 2003. Integrin-specific signaling pathways controlling focal adhesion formation and cell migration. J Cell Biol 161:155-167.
35. Mueller SC, Ghersi G, Akiyama SK, Sang QX, Howard L, Pineiro-Sanchez M, Nakahara H, Yeh Y, Chen WT. 1999. A novel protease-docking function of integrin at invadopodia. J Biol Chem 274:24947-24952.
36. Nakagawa O, Nakagawa M, Richardson JA, Olson EN, Srivastava D. 1999. HRT1, HRT2, and HRT3: a new subclass of bHLH transcription factors marking specific cardiac, somitic, and pharyngeal arch segments. Dev Biol 1:72-84.
37. Nakaya Y, Kuroda S, Katagiri YT, Kaibuchi K, Takahashi Y. 2004. Mesenchymal-epithelial transition during somitic segmentation is regulated by differential roles of Cdc42 and Rac1. Dev Cell 7:425-438.
38. Niedermeyer J, Garin-Chesa P, Kriz M, Hilberg F, Mueller E, Bamberger U, Rettig WJ, Schnapp A. 2001. Expression of the fibroblast activation protein during mouse embryo development. Int J Dev Biol 45:445-447.
39. Nieto MA. 2011. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol 27:347-376.
40. Noren NK, Pasquale EB. 2004. Eph receptor-ephrin bidirectional signals that target Ras and Rho proteins. Cell 16:655-666.
41. Poliakov A, Cotrina M, Wilkinson DG. 2004. Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly. Cell 7:465-480.
42. Quertermous EE, Hidai H, Blanar MA, Quertermous T. 1994. Cloning and characterization of a basic helix-loop-helix protein expressed in early mesoderm and the developing somites. Proc Natl Acad Sci USA 91:7066-7070.
43. Radice GL, Rayburn H, Matsunami H, Knudsen KA, Takeichi M, Hynes RO. 1997. Developmental defects in mouse embryos lacking N-cadherin. Dev Biol 181:64-78.
44. Rhee J, Takahashi Y, Saga Y, Wilson-Rawls J, Rawls A. 2003. The protocadherin papc is involved in the organization of the epithelium along the segmental border during mouse somitogenesis. Dev Biol 254:248-261.
45. Rifes P, Thorsteinsdottir S. 2012. Extracellular matrix assembly and 3D organization during paraxial mesoderm development in the chick embryo. Dev Biol 368:370-81.
46. Rifes P, Carvalho L, Lopes C, Andrade RP, Rodrigues G, Palmeirim I, Thorsteinsdottir S. 2007. Redefining the role of ectoderm in somitogenesis: a player in the formation of the fibronectin matrix of presomitic mesoderm. Development 134:3155-3165.
47. Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365-386.
48. Saga Y. 2012. The mechanism of somite formation in mice. Curr Opin Genet Dev 22:331-338.
49. Saleem M, Kweon MH, Johnson JJ, Adhami VM, Elcheva I, Khan N, Hafeez BB, Bhat KMR, Sarfaraz S, Reagan-Shaw S, Spiegelman VS, Setaluri V, and Mukhtar H. 2006. S100A4 accelerates tumorigenesis and invasion of human prostate cancer through the transcriptional regulation of matrix metalloproteinase 9. Proc Natl Acad Sci USA 103:14825-14830.
50. Schmidt C, Stoeckelhuber M, McKinnell I, Putz R, Christ B, Patel K. 2004. Wnt 6 regulates the epithelialisation process of the segmental plate mesoderm leading to somite formation. Dev Biol 271:198-209.
51. Schmidt-Hansen B. 2004. Functional significance of metastasis-inducing S100A4(Mts1) in tumor-stroma interplay. J Biol Chem 279:24498-24504.
52. Schneider M, Hansen JL, Sheikh SP. 2008. S100A4: a common mediator of epithelial-mesenchymal transition, fibrosis and regeneration in diseases? J Mol Med 86:507-522.
53. Seo KW, Wang Y, Kokubo H, Kettlewell JR, Zarkower DA, Johnson RL. 2006. Targeted disruption of the DM domain containing transcription factor Dmrt2 reveals an essential role in somite patterning. Dev Biol 290:200-210.
54. Shanmugalingam S, Wilson SW. 1998. Isolation, expression and regulation of a zebrafish Paraxis homologue. Mech Dev 78:85-89.
55. Šošić D, Brand-Saberi B, Schmidt C, Christ B, Olson EN. 1997. Regulation of paraxis expression and somite formation by ectoderm- and neural tube-derived signals. Dev Biol 185:229-243.
56. Takahashi Y, Sato Y, Suetsugu R, Nakaya Y. 2005. Mesenchymal-to-epithelial transition during somitic segmentation: a novel approach to studying the roles of Rho family GTPases in morphogenesis. Cells Tissues Organs 179:36-42.
57. Tan TK, Zheng G, Hsu TT, Wang Y, Lee VW, Tian X, Wang Y, Cao Q, Harris DC. 2010. Macrophage matrix metalloproteinase-9 mediates epithelial-mesenchymal transition in vitro in murine renal tubular cells. Am J Pathol 176:1256-1270.
58. Thiery JP, Sleeman JP. 2006. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7:131-142.
59. Tonami K, Kurihara Y, Arima S, Nishiyama K, Uchijima Y, Asano T, Sorimachi H, Kurihara H. 2011. Calpain-6, a microtubule-stabilizing protein, regulates Rac1 activity and cell motility through interaction with GEF-H1. J Cell Sci 124:1214-1223.
60. Tsang M, Lijam N, Yang Y, Beier DR, Wynshaw-Boris A, Sussman DJ. 1996. Isolation and characterization of mouse Dishevelled-3. Dev Dyn 207:253-262.
61. Van Aelst L, Symons M. 2002. Role of Rho family GTPases in epithelial morphogenesis. Genes Dev 16:1032-1054.
62. Wagner J, Schmidt C, Nikowits W Jr, Christ B. 2000. Compartmentalization of the somite and myogenesis in chick embryos are influenced by Wnt expression. Dev Biol 228:86-94.
63. Watanabe T, Saito D, Tanabe K, Suetsugu R, Nakaya Y, Nakagawa S, Takahashi Y. 2007. Tet-on inducible system combined with in ovo electroporation dissects multiple roles of genes in somitogenesis of chicken embryos. Dev Biol 305:625-636.
64. Weber S, Saftig P. 2012. Ectodomain shedding and ADAMs in development. Development 139:3693-3709.
65. Wehrle-Haller B. 2012. Structure and function of focal adhesions. Curr Opin Cell Biol 24:116-124.
66. Wilson-Rawls J, Rhee JM, Rawls A. 2004. Paraxis is a basic helix-loop-helix protein that positively regulates transcription through binding to specific E-box elements. J Biol Chem 279:37685-37692.
67. Wilson-Rawls J, Hurt CR, Parsons SM, Rawls A. 1999. Differential regulation of epaxial and hypaxial muscle development by Paraxis. Development 126:5217-5229.
68. Woods A, Couchman JR. 2001. Syndecan-4 and focal adhesion function. Curr Opin Cell Biol 13:578-583.
69. Yang J, Weinberg RA. 2008. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 14:818-829.
70. Yang JT, Rayburn H, Hynes RO. 1993. Embryonic mesodermal defects in alpha 5 integrin-deficient mice. Development 119:1093-1105.
71. Yang JT, Bader BL, Kreidberg JA, Ullman-Culleré M, Trevithick JE, Hynes RO. 1999. Overlapping and independent functions of fibronectin receptor integrins in early mesodermal development. Dev Biol 215:264-277.