Embryonic expression of endothelins and their receptors in lamprey and frog reveals stem vertebrate origins of complex Endothelin signaling.
Neural crest cells (NCCs) are highly patterned embryonic cells that migrate along stereotyped routes to give rise to a diverse array of adult tissues and cell types. Modern NCCs are thought to have evolved from migratory neural precursors with limited developmental potential and patterning. How this occurred is poorly understood. Endothelin signaling regulates several aspects of NCC development, including their migration, differentiation, and patterning. In jawed vertebrates, Endothelin signaling involves multiple functionally distinct ligands (Edns) and receptors (Ednrs) expressed in various NCC subpopulations. To test the potential role of endothelin signaling diversification in the evolution of modern, highly patterned NCC, we analyzed the expression of the complete set of endothelin ligands and receptors in the jawless vertebrate, the sea lamprey (Petromyzon marinus). To better understand ancestral features of gnathostome edn and ednr expression, we also analyzed all known Endothelin signaling components in the African clawed frog (Xenopus laevis). We found that the sea lamprey has a gnathsotome-like complement of edn and ednr duplicates, and these genes are expressed in patterns highly reminiscent of their gnathostome counterparts. Our results suggest that the duplication and specialization of vertebrate Endothelin signaling coincided with the appearance of highly patterned and multipotent NCCs in stem vertebrates.
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA.
Tyler
T
Square
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA.|Department of Zoology, Faculty of Natural Sciences, Comenius University in Bratislava, Bratislava, 84215, Slovakia.
David
D
Jandzik
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA.
Maria
M
Cattell
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA.
Andrew
A
Hansen
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA.
Daniel Meulemans
DM
Medeiros
Mech Dev. 2006 Feb;123(2):124-34
16412618
Br J Pharmacol. 1993 Aug;109(4):1024-8
8401914
Development. 2000 Sep;127(17):3815-28
10934026
Development. 2007 Jan;134(2):335-45
17166927
Dev Cell. 2004 Sep;7(3):291-9
15363405
J Clin Invest. 1998 Jul 1;102(1):22-33
9649553
Development. 2014 Feb;141(3):629-38
24449839
J Biol Chem. 1993 Apr 25;268(12):8547-53
8473300
Eur J Pharmacol. 1988 Aug 2;152(3):373-4
3065091
Mol Biol Evol. 2016 Sep;33(9):2337-44
27288344
Development. 2009 Jun;136(12):1987-94
19439494
Proteins. 2002 Jun 1;47(4):481-8
12001226
Q Rev Biol. 1983 Mar;58(1):1-28
6346380
Mol Biol Evol. 2009 Apr;26(4):783-99
19174480
Science. 1983 Apr 15;220(4594):268-73
17732898
Dev Biol. 2015 Jan 15;397(2):293-304
25446275
Dev Biol. 2011 Feb 1;350(1):217-27
21035440
J Biol Chem. 1993 Sep 5;268(25):19126-33
8360195
Biochim Biophys Acta. 1994 Sep 8;1223(2):202-8
8086489
J Biol Chem. 1995 Jun 23;270(25):15262-8
7797512
Proc Natl Acad Sci U S A. 2008 Dec 2;105(48):18806-11
19017795
Eur J Biochem. 1994 Feb 15;220(1):37-43
8119297
BMC Evol Biol. 2008 Jan 23;8:16
18215274
Development. 2015 Dec 1;142(23):4180-7
26511928
J Cardiovasc Pharmacol. 1998;31 Suppl 1:S13-5
9595387
Dev Dyn. 2011 Jun;240(6):1454-66
21538684
Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9645-50
8790384
Nature. 1999 Dec 2;402(6761):496-501
10591209
Nature. 2012 Dec 6;492(7427):104-7
23135395
Mech Dev. 1998 Jul;75(1-2):145-9
9739130
Development. 2012 Feb;139(4):720-30
22241841
Proc Natl Acad Sci U S A. 2010 Oct 5;107(40):17262-7
20855630
Biochem Soc Trans. 2000;28(4):426-30
10961933
Development. 2003 Jun;130(11):2317-27
12702647
Int J Dev Biol. 2003 Jun;47(5):315-25
12895026
FEBS Lett. 1988 Apr 25;231(2):440-4
3282927
Development. 2008 Feb;135(4):755-65
18199583
Methods Enzymol. 1995;248:183-228
7674922
Dev Biol. 2010 May 1;341(1):315-23
20171204
Cell Signal. 2010 Nov;22(11):1615-25
20466059
Cell. 1994 Dec 30;79(7):1277-85
8001160
Development. 1998 Dec;125(24):4931-41
9811577
Dev Biol. 2008 Nov 1;323(1):114-29
18775422
Nature. 1988 Mar 31;332(6163):411-5
2451132
Arch Biochem Biophys. 2002 Feb 15;398(2):240-8
11831855
Dev Cell. 2007 Sep;13(3):405-20
17765683
Am J Med Genet A. 2010 Dec;152A(12):2962-73
20684004
Circulation. 1994 Mar;89(3):1320-2
8124823
Development. 2015 Jan 15;142(2):242-57
25564621
Evol Dev. 2000 Jan-Feb;2(1):3-5
11256415
Genet Med. 2010 Jan;12(1):39-43
20009762
Genes Dev. 2005 Mar 15;19(6):744-55
15769946
Nature. 2015 Nov 19;527(7578):371-4
26524532
J Clin Invest. 2000 May;105(10):1373-82
10811845
Biol Open. 2014 May 23;3(6):503-9
24857848
Dev Biol. 2014 Jan 15;385(2):396-404
24252777
Gen Comp Endocrinol. 2014 Dec 1;209:21-34
25010382
Dev Genes Evol. 2008 Dec;218(11-12):723-7
18773220
Nature. 2006 Jun 8;441(7094):750-2
16760978
Biochem Biophys Res Commun. 1988 Aug 15;154(3):868-75
3044368
Genesis. 2013 Jul;51(7):457-70
23712931
Dev Biol. 2006 Feb 1;290(1):92-104
16364284
Development. 1998 Mar;125(5):813-24
9449664
Dev Biol. 2003 Dec 15;264(2):339-51
14651922
Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3024-9
9501209
Philos Trans R Soc Lond B Biol Sci. 2001 Oct 29;356(1414):1615-32
11604127