Punctuated actin contractions during convergent extension and their permissive regulation by the non-canonical Wnt-signaling pathway.
Actomyosin networks linked to the micro-environment through the plasma membrane are thought to be key players in regulating cell behaviors within multicellular tissues, such as converging and extending mesoderm. Here, we observe the dynamics of actin contractions called 'punctuated actin contractions' in the mid-cell body of embryonic mesenchymal cells in the mesoderm. These contraction dynamics are a common feature of Xenopus embryonic tissues and are important for cell shape changes during morphogenesis. Quantitative morphological analysis of these F-actin dynamics indicates that frequent and aligned movements of multiple actin contractions accompany mesoderm cells as they intercalate and elongate. Using inhibitors combined with fluorescence recovery after photobleaching (FRAP) analysis, we find that the dynamics of actin contractions are regulated by both myosin contractility and F-actin polymerization. Furthermore, we find that the non-canonical Wnt-signaling pathway permissively regulates levels of punctuated actin contractions. Overexpression of Xfz7 (Fzd7) can induce early maturation of actin contractions in mesoderm and produce mesoderm-like actin contractions in ectoderm cells. By contrast, expression of the dominant-negative Xenopus disheveled construct Xdd1 blocks the progression of actin contractions into their late mesoderm dynamics but has no effect in ectoderm. Our study reveals punctuated actin contractions within converging and extending mesoderm and uncovers a permissive role for non-canonical Wnt-signaling, myosin contractility and F-actin polymerization in regulating these dynamics.
Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA 15260, USA.
Hye Young
HY
Kim
Lance A
LA
Davidson
D000199:Actins / Q000235:genetics / Q000378:metabolism*; D000818:Animals; D018507:Gene Expression Regulation, Developmental; D008648:Mesoderm / Q000196:embryology / Q000378:metabolism*; D015398:Signal Transduction; D051153:Wnt Proteins / Q000235:genetics / Q000378:metabolism*; D029867:Xenopus Proteins / Q000235:genetics / Q000378:metabolism*; D014982:Xenopus laevis / Q000196:embryology / Q000235:genetics / Q000378:metabolism*
D000199:Actins; D051153:Wnt Proteins; D029867:Xenopus Proteins
EMBO J. 2008 Feb 20;27(4):606-17
18256687
Cell Cycle. 2007 Jan 1;6(1):30-5
17245114
Dev Cell. 2004 Sep;7(3):413-24
15363415
J Biochem. 2009 Feb;145(2):137-50
19008261
Development. 2008 Aug;135(14):2435-44
18550716
Dev Cell. 2009 Mar;16(3):421-32
19289087
Cell Motil Cytoskeleton. 2007 Nov;64(11):822-32
17685442
Curr Biol. 2001 Nov 27;11(23):1847-57
11728307
Methods Cell Biol. 1991;36:679-81
1811160
Development. 2002 Dec;129(24):5815-25
12421719
J Microsc. 2008 Sep;231(3):466-78
18755002
Development. 1996 Sep;122(9):2873-83
8787760
J Cell Biol. 1996 Sep;134(5):1271-81
8794867
J Cell Sci. 2007 Dec 15;120(Pt 24):4332-44
18042624
Development. 2005 Oct;132(20):4599-610
16176947
Development. 1992 Dec;116(4):915-30
1295744
BMC Cell Biol. 2000;1:1
11112983
Curr Biol. 2008 Apr 8;18(7):471-80
18372178
Dev Dyn. 2008 Oct;237(10):2684-92
18629871
Proc Natl Acad Sci U S A. 2010 Jun 1;107(22):9944-9
20463286
Curr Opin Cell Biol. 2007 Aug;19(4):453-8
17616384
Proc Natl Acad Sci U S A. 2008 Jan 8;105(1):210-5
18162551
Dev Biol. 2002 Feb 15;242(2):109-29
11820810
J Cell Biol. 2005 Jan 31;168(3):429-39
15684032
J Cell Biol. 2007 Sep 24;178(7):1207-21
17893245
Dev Cell. 2006 Jul;11(1):69-79
16824954
Nat Cell Biol. 2008 Jan;10(1):61-9
18084283
Biophys J. 1976 Sep;16(9):1055-69
786399
Nat Cell Biol. 2010 Jul;12(7):696-702
20543839
Nature. 2010 Dec 23;468(7327):1110-4
21068726
J Cell Biol. 1996 Jul;134(1):227-40
8698817
Dev Cell. 2006 Jul;11(1):2-4
16824946
J Cell Biol. 1986 Mar;102(3):1074-84
3949874
Development. 2009 Feb;136(4):677-88
19168681
Development. 2010 Aug;137(16):2785-94
20630946
Nature. 2009 Jan 22;457(7228):495-9
19029882
Development. 2009 Dec;136(24):4123-32
19906848
Development. 2000 Jul;127(14):3091-100
10862746
Development. 2001 Aug;128(16):3209-20
11688569
Dev Biol. 2009 Aug 15;332(2):396-406
19523939
Cell. 1996 Feb 9;84(3):359-69
8608589
J Biol Chem. 1999 Apr 16;274(16):11352-61
10196227
Nature. 2001 Oct 25;413(6858):856-60
11677610
Development. 1992 Dec;116(4):901-14
1295743
Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10277-10282
16801551
Dev Dyn. 2004 Nov;231(3):576-81
15376320
Annu Rev Biophys Biomol Struct. 2006;35:361-87
16689641
Curr Biol. 2005 Apr 26;15(8):787-93
15854914
Int J Dev Biol. 1996 Feb;40(1):305-11
8735942
Development. 2006 Nov;133(21):4219-31
17021034
Nat Rev Mol Cell Biol. 2009 Jan;10(1):34-43
19197330
Cell Motil Cytoskeleton. 1989;13(3):127-44
2776221
Dev Cell. 2004 Mar;6(3):343-55
15030758
J Cell Biol. 2009 Sep 7;186(5):693-702
19720875
Nature. 2002 Oct 17;419(6908):726-9
12384700
Nature. 2000 May 4;405(6782):81-5
10811222
Development. 2005 Jun;132(12):2825-36
15930112
Development. 2010 Aug;137(16):2743-52
20663818
Nature. 2004 Jul 15;430(6997):364-7
15254540
BMC Dev Biol. 2007 Dec 24;7:142
18157918
J Biomech. 2010 Jan 5;43(1):63-70
19815213