Sfrp1, Sfrp2, and Sfrp5 regulate the Wnt/β-catenin and the planar cell polarity pathways during early trunk formation in mouse

Genesis

Volumn 46, Issue 2, 2008, Pages 92-103

  Satoh, Wataru ^a,b   Matsuyama, Makoto ^a   Takemura, Hiromasa ^a,b,c   Aizawa, Shinichi ^a   Shimono, Akihiko ^a  

^a RIKEN   (Japan)

^b NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

Convergent extension; Planar cell polarity pathway; Sfrp; Somitogenesis; Wnt catenin pathway

Indexed keywords

BETA CATENIN; SECRETED FRIZZLED RELATED PROTEIN 1; SECRETED FRIZZLED RELATED PROTEIN 2; SECRETED FRIZZLED RELATED PROTEIN 5; UNCLASSIFIED DRUG; WNT PROTEIN; MEMBRANE PROTEIN; SFRP1 PROTEIN, MOUSE; SFRP2 PROTEIN, MOUSE; SFRP5 PROTEIN, MOUSE; SIGNAL PEPTIDE;

ARTICLE; CELL POLARITY; CONTROLLED STUDY; EMBRYO DEVELOPMENT; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; EMBRYO (ANATOMY); GENETICS; METABOLISM; MORPHOGENESIS; MOUSE MUTANT; SOMITE;

MUS;

ANIMALS; BETA CATENIN; BODY PATTERNING; CELL POLARITY; EMBRYO, MAMMALIAN; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; SOMITES; WNT PROTEINS;

EID: 39549107806     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.20369     Document Type: Article

References (67)

1. Aulehla A, Herrmann BG. 2004. Segmentation in vertebrates: Clock and gradient finally joined. Genes Dev 18:2060-2067.
2. Aulehla A, Wehrte C, Brand-Saberi B, Kemler R, Gossler A, Kanzler B, Herrmann BG. 2003. Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev Cell 4:395-406.
3. Axelrod JD. 2001. Unipolar membrane association of Dishevelled mediates Frizzled planar cell polarity signaling. Genes Dev 15:1182-1187.
4. Bettenhausen B, Hrabe de Angelis M, Simon D, Guenet JL, Gossler A. 1995. Transient and restricted expression during mouse embryogenesis of Dll1, a murine gene closely related to Drosophila Delta. Development 121:2407-2418.
5. Capdevila J, Tabin C, Johnson RL. 1998. Control of dorsoventral somite patterning by Wnt-1 and beta-catenin. Dev Biol 193:182-194.
6. Carreira-Barbosa F, Concha ML, Takeuchi M, Ueno N, Wilson SW, Tada M. 2003. Prickle 1 regulates cell movements during gastrulation and neuronal migration in zebrafish. Development 130:4037-4046.
7. Carter M, Chen X, Slowinska B, Minnerath S, Glickstein S, Shi L, Campagne F, Weinstein H, Ross ME. 2005. Crooked tail (Cd) model of human folate-responsive neural tube defects is mutated in Wnt coreceptor lipoprotein receptor-related protein 6. Proc Natl Acad Sci USA 102:12843-12848.
8. Chapman DL, Agulnik I, Hancock S, Silver LM, Papaioannou VE. 1996. Tbx6, a mouse T-Box gene implicated in paraxial mesoderm formation at gastrulation. Dev Biol 180:534-542.
9. Cole SE, Levorse JM, Tilghman SM, Vogt TF. 2002. Clock regulatory elements control cyclic expression of Lunatic fringe during somitogenesis. Dev Cell 3:75-84.
10. Cox S, Smith L, Bogani D, Cheeseman M, Siggers P, Greenfield A. 2006. Sexually dimorphic expression of secreted frizzled-related (SFRP) genes in the developing mouse Mullerian duct. Mol Reprod Dev 73:1008-1016.
11. Dale JK, Maroto M, Dequeant ML, Malapert P, McGrew M, Pourquie O. 2003. Periodic notch inhibition by lunatic fringe underlies the chick segmentation clock. Nature 421:275-278.
12. Dequeant ML, Glynn E, Gaudenz K, Wahl M, Chen J, Mushegian A, Pourquie O. 2006. A complex oscillating network of signaling genes underlies the mouse segmentation clock. Science 314:1595-1598.
13. Downs MK, Davies T. 1993. Staging of gastrulating embryos by morphological landmark in the dissecting microscope. Development 118:1255-1266.
14. Echelard Y, Epstein DJ, St-Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP. 1993. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75:1417-1430.
15. Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, Nishida H, Yap CC, Suzuki M, Kawai J, Suzuki H, Carninci P, Hayashizaki Y, Wells C, Frith M, Ravasi T, Pang KC, Hallinan J, Mattick J, Hume DA, Lipovich L, Batalov S, Engström PG, Mizuno Y, Faghihi MA, Sandelin A, Chalk AM, Mottagui-Tabar S, Liang Z, Lenhard B, Wahlestedt C; RIKEN Genome Exploration Research Group; Genome Science Group (Genome Network Project Core Group); FANTOM Consortium. 2005. Antisense transcription in the mammalian transcriptome. Science 309:1564-1566.
16. Finley KR, Tennessen J, Shawlot W. 2003. The mouse secreted frizzled-related protein 5 gene is expressed in the anterior visceral endoderm and foregut endoderm during early post-implantation development. Gene Expr Patterns 3:681-684.
17. Furushima K, Yamamoto A, Naganom T, Shibata M, Miyachi H, Abe T, Ohshima N, Kiyonari H, Aizawa S. 2007. Mouse homologues of Shisa antagonistic to Wnt and Fgf signalings. Dev Biol 306:480-492.
18. Galceran J, Sustmann C, Hsu SC, Folberth S, Grosschedl R. 2004. LEF1-mediated regulation of Delta-like 1 links Wnt and Notch signaling in somitogenesis. Genes Dev 18:2718-2723.
19. Galli LM, Barnes T, Cheng T, Acosta L, Anglade A, Willert K, Nusse R, Burrus LW. 2006. Differential inhibition of Wnt-3a by Sfrp-1. Sfrp-2, and Sfrp-3. Dev Dyn 235:681-690.
20. Goulding MD, Chalepakis G, Deutsch U, Erselius JR, Grass P. 1991. Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J 10:1135-1147.
21. Henry CA, Hall LA, Burr Hille M, Solnica-Krezel L, Cooper MS. 2000. Somites in zebrafish doubly mutant for knypek and trilobite form without internal mesenchymal cells or compaction. Curr Biol 10:1063-1066.
22. Heisenberg CP, Tada M, Rauch GJ, Saude L, Concha ML, Geisler R, Stemple DL, Smith JC, Wilson SW. 2000. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405:76-81.
23. Hoang BH, Thomas JT, Abdul-Karim FW, Correia KM, Conlon RA, Luvten FP, Ballock RT. 1998. Expression pattern of two Frizzled-related genes. Frzb-1 and Sfrp-1, during mouse embryogenesis suggests a role for modulating action of Wnt family members. Dev Dyn 212:364-372.
24. Hofmann M, Schuster-Gossler K, Watabe-Rudolph M, Aulehla A, Herrmann BG, Gossler A. 2004. WNT signaling, in synergy with T/TBX6, controls Notch signaling by regulating Dili expression in the presomitic mesoderm of mouse embryos. Genes Dev 18:2712-2717.
25. Jenny A, Darken RS, Wilson PA, Mlodzik M. 2003. Prickle and Strabismus form a functional complex to generate a correct axis during planar cell polarity signaling. EMBO J 22:4409-4420.
26. Jones SE, Jomary C. 2002. Secreted Frizzled-related proteins: Searching for relationships and patterns. Bioessays 24:811-820.
27. Kawano Y, Kypta R. 2003. Secreted antagonists of the Wnt signaling pathway. J Cell Sci 116:2627-2634.
28. Keller R. 2002. Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298:1950-1954.
29. Kinder SJ, Tsang TE, Quinlan GA, Hadjantonakis AK, Nagy A, Tam PP. 1999. The orderly allocation of mesodermal cells to the extraembryonic structures and the anteroposterior axis during gastrulation of the mouse embryo. Development 126:4691-4701.
30. Kinder SJ, Tsang TE, Wakamiya M, Sasaki H, Behringer RR, Nagy A, Tam PP. 2001. The organizer of the mouse gastrula is composed of a dynamic population of progenitor cells for the axial mesoderm. Development 128:3623-3634.
31. Leaf I, Tennessen J, Mukhopadhyay M, Westphal H, Shawlot W. 2006. Sfrp5 is not essential for axis formation in the mouse. Genesis 44:573-578.
32. Leimeister C, Bach A, Gessler M. 1998. Developmental expression patterns of mouse sFRP genes encoding members of the secreted frizzled related protein family. Mech Dev 75:29-42.
33. Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, Bradley A. 1999. Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22:361-365.
34. Lu X, Borchers AG, Jolicoeur C, Rayburn H, Baker JC, Tessier-Lavigne M. 2004. PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430:93-98.
35. MacDonald BT, Adamska M, Meisler MH. 2004. Hypomorphic expression of Dkk1 in the doubleridge mouse: Dose dependence and compensatory interactions with Lrp6. Development 131:2543-2552.
36. Mansouri A, Yokota Y, Wehr R, Copeland NG, Jenkins NA, Grass P. 1997. Paired-related murine homeobox gene expressed in the developing sclerotome, kidney, and nervous system. Dev Dyn 210:53-65.
37. Merrill BJ, Pasolli HA, Polak L, Rendl M, Garcia-Garcia MJ, Anderson KV, Fuchs E. 2004. Tcf3: A transcriptional regulator of axis induction in the early embryo. Development 131:263-274.
38. Mikels AJ, Nusse R. 2006. Purified Wnt5a protein activates or inhibits β-catenin-TCF signaling depending on receptor context. PLoS Biol 4:570-582.
39. Morales AV, Yasuda Y, Ish-Horowicz D. 2002. Periodic lunatic fringe expression is controlled during segmentation by a cyclic transcriptional enhancer responsive to notch signaling. Dev Cell 3:63-74.
40. Morimoto M, Takahashi Y, Endo M, Saga Y. 2005. The Mesp2 transcription factor establishes segmental borders by suppressing Notch activity. Nature 435:354-459.
41. Mukhopadhyay M, Shtrom S, Rodriguez-Esteban C, Chen L, Tsukui T, Gomer L, Dorward DW, Glinka A, Grinberg A, Huang SP, Niehrs C, Belmonte JC, Westphal H. 2001. Dickkopfl is required for embryonic head induction and limb morphogenesis in the mouse. Dev Cell 1:423-434.
42. Mukhopadhyay M, Teufel A, Yamashita T, Agulnick AD, Chen L, Downs KM, Schindler A, Grinberg A, Huang SP, Dorward D, Westphal H. 2003. Functional ablation of the mouse Ldb1 gene results in severe patterning defects during gastrulation. Development 130:495-505.
43. Niehrs C. 2006. Function and biological roles of the Dickkopf family of Wnt modulators. Oncogene 25:7469-7481.
44. Oishi I, Suzuki H, Onishi N, Takada R, Kani S, Ohkawara B, Koshida I, Suzuki K, Yamada G, Schwabe GC, Mundlos S, Shibuya H, Takada S, Minami Y. 2003. The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 8:645-654.
45. Park M, Moon TR. 2002. The planar cell-polarity gene stbm regulates cell behaviour and cell fate in vertebrate embryos. Nat Cell Biol 4:20-25.
46. Prud'homme B, Lartillot N, Balavoine G, Adoutte AVervoort M. 2002. Phylogenetic analysis of the Wnt gene family. Insights from lophotrochozoan members. Curr Biol 12:1395-1400.
47. Qian D, Jones C, Rzadzinska A, Mark S, Zhang X, Steel KP, Dai X, Chen P. 2007. Wnt5a functions in planar cell polarity regulation in mice. Dev Biol 306:121-33.
48. Robert B, Sassoon D, Jacq B, Gehring W, Buckingham M. 1989. Hox-7, a mouse homeobox gene with a novel pattern of expression during embryogenesis. EMBO J 8:91-100.
49. Satoh W, Gotoh T, Tsunematsu Y, Aizawa S, Shimono A. 2006. Sfrp1 and Sfrp2 regulate anteroposterior axis elongation and somite segmentation during mouse embryogenesis. Development 133:989-999.
50. Schambony A, Wedlich D. 2007. Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. Dev Cell 12:779-792.
51. Seifert JR, Mlodzik M. 2007. Frizzled/PCP signalling: A conserved mechanism regulating cell polarity and directed motility. Nat Rev Genet 8:126-138.
52. Shimono A, Behringer RR. 1999. Isolation of novel cDNAs by subtractions between the anterior mesendoderm of single mouse gastrula stage embryos. Dev Biol 209:369-380.
53. Shimono A, Behringer RR. 2003. Angiomotin regulates visceral endoderm movements during mouse embryogenesis. Curr Biol 13:613-617.
54. Suzuki H, Watkins DN, Jair KW, Schuebel KE, Markowitz SD, Chen WD, Pretlow TP, Yang B, Akiyama Y, Van Engeland M, Toyota M, Tokino T, Hinoda Y, Imai K, Herman JG, Baylin SB. 2004. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet 36:417-422.
55. Torban E, Kor C, Gros P. 2004. Van Gogh-like2 (Strabismus) and its role in planar cell polarity and convergent extension in vertebrates. Trends Genet 20:570-577.
56. Tree DR, Shulman JM, Rousset R, Scott MP, Gubb D, Axelrod JD. 2002. Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109:371-381.
57. Wang J, Hamblet NS, Mark S, Dickinson ME, Brinkman BC, Segil N, Fraser SE, Chen P, Wallingford JB, Wynshaw-Boris A. 2006. Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation. Development 133:1767-1778.
58. Widelitz R. 2005. Wnt signaling through canonical and non-canonical pathways: recent progress. Growth Factors 23:111-116.
59. Wilkinson DG. 1992. Whole mount in situ hybridization of vertebrate embryos. In: Wilkinson DG, editor. In situ hybridization. Oxford: IRL. pp 75-83.
60. Wilkinson DG, Bhatt S, Herrmann BG. 1990. Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343:657-659.
61. Wilson V, Rashbass P, Beddington RS. 1993. Chimeric analysis of T (Brachyury) gene function. Development 117:1321-131.
62. Yagi T, Nada S, Watanabe N, Tamemoto H, Kohmura N, Ikawa Y, Aizawa S. 1993. A novel negative selection for homologous recombinants using diphtheria toxin A fragment gene. Anal Biochem 214:77-86.
63. Yamaguchi TP, Takada S, Yoshikawa Y, Wu N, McMahon AP. 1999a. T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev 13:3185-3190.
64. Yamaguchi TP, Bradley A, McMahon AP, Jones S. 1999b. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126:1211-1223.
65. Yamamoto A, Kemp C, Bachiller D, Geissen D, De Robertis EM. 2000. Mouse paraxial protocadherin is expressed in trunk mesoderm and is not essential for mouse development. Genesis 27:49-57.
66. Ybot-Gonzalez P, Savery D, Gerrelli D, Signore M, Mitchell CE, Faux CH, Greene ND, Copp AJ. 2007. Convergent extension, planar-cell-polarity signalling and initiation of mouse neural tube closure. Development 134:789-799.
67. Zeng L, Fagotto F, Zhang T, Hsu W, Vasicek TJ, Perry WL III, Lee JJ, Tilghman SM, Gumbiner BM, Costantini F. 1997. The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90:181-192.