Lnx2 ubiquitin ligase is essential for exocrine cell differentiation in the early zebrafish pancreas

被引:12
作者
Won, Minho [1 ]
Ro, Hyunju [2 ]
Dawid, Igor B. [1 ]
机构
[1] NICHHD, Sect Dev Biol, Bethesda, MD 20892 USA
[2] Chungnam Natl Univ, Coll Biosci & Biotechnol, Dept Biol Sci, Daejeon 305764, South Korea
基金
新加坡国家研究基金会; 美国国家卫生研究院;
关键词
pancreas; Numb; Notch; morpholino; TALEN; FAMILY PROTEINS; NUMB; ENDOCRINE; EXPRESSION; DOMAIN; UBIQUITYLATION; MODULATION; PROMOTE; DESIGN; SYSTEM;
D O I
10.1073/pnas.1517033112
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The gene encoding the E3 ubiquitin ligase Ligand of Numb protein-X (Lnx)2a is expressed in the ventral-anterior pancreatic bud of zebrafish embryos in addition to its expression in the brain. Knockdown of Lnx2a by using an exon 2/intron 2 splice morpholino resulted in specific inhibition of the differentiation of ventral bud derived exocrine cell types, with little effect on endocrine cell types. A frame shifting null mutation in lnx2a did not mimic this phenotype, but a mutation that removed the exon 2 splice donor site did. We found that Lnx2b functions in a redundant manner with its paralog Lnx2a. Inhibition of lnx2a exon 2/3 splicing causes exon 2 skipping and leads to the production of an N-truncated protein that acts as an interfering molecule. Thus, the phenotype characterized by inhibition of exocrine cell differentiation requires inactivation of both Lnx2a and Lnx2b. Human LNX1 is known to destabilize Numb, and we show that inhibition of Numb expression rescues the Lnx2a/b-deficient phenotype. Further, Lnx2a/b inhibition leads to a reduction in the number of Notch active cells in the pancreas. We suggest that Lnx2a/b function to fine tune the regulation of Notch through Numb in the differentiation of cell types in the early zebrafish pancreas. Further, the complex relationships among genotype, phenotype, and morpholino effect in this case may be instructive in the ongoing consideration of morpholino use.
引用
收藏
页码:12426 / 12431
页数:6
相关论文
共 45 条
[1]   Notch signalling controls pancreatic cell differentiation [J].
Apelqvist, Å ;
Li, H ;
Sommer, L ;
Beatus, P ;
Anderson, DJ ;
Honjo, T ;
de Angelis, MH ;
Lendahl, U ;
Edlund, H .
NATURE, 1999, 400 (6747) :877-881
[2]   Early appearance of pancreatic hormone-expressing cells in the zebrafish embryo [J].
Argenton, F ;
Zecchin, E ;
Bortolussi, M .
MECHANISMS OF DEVELOPMENT, 1999, 87 (1-2) :217-221
[3]   Numb regulates Notch1, but not Notch3, during myogenesis [J].
Beres, Brian J. ;
George, Rajani ;
Lougher, Eric J. ;
Barton, Michael ;
Verrelli, Brian C. ;
McGlade, C. Jane ;
Rawls, J. Alan ;
Wilson-Rawls, Jeanne .
MECHANISMS OF DEVELOPMENT, 2011, 128 (5-6) :247-257
[4]   Zebrafish Numb and Numblike Are Involved in Primitive Erythrocyte Differentiation [J].
Bresciani, Erica ;
Confalonieri, Stefano ;
Cermenati, Solei ;
Cimbro, Simona ;
Foglia, Efrem ;
Beltrame, Monica ;
Di Fiore, Pier Paolo ;
Cotelli, Franco .
PLOS ONE, 2010, 5 (12)
[5]   Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting [J].
Cermak, Tomas ;
Doyle, Erin L. ;
Christian, Michelle ;
Wang, Li ;
Zhang, Yong ;
Schmidt, Clarice ;
Baller, Joshua A. ;
Somia, Nikunj V. ;
Bogdanove, Adam J. ;
Voytas, Daniel F. .
NUCLEIC ACIDS RESEARCH, 2011, 39 (12) :e82
[6]   Ligand of Numb proteins LNX1p80 and LNX2 interact with the human glycoprotein CD8α and promote its ubiquitylation and endocytosis [J].
D'Agostino, Massimo ;
Tornillo, Giusy ;
Caporaso, Maria Gabriella ;
Barone, Maria Vittoria ;
Ghigo, Eric ;
Bonatti, Stefano ;
Mottola, Giovanna .
JOURNAL OF CELL SCIENCE, 2011, 124 (21) :3545-3556
[7]   Simple Methods for Generating and Detecting Locus-Specific Mutations Induced with TALENs in the Zebrafish Genome [J].
Dahlem, Timothy J. ;
Hoshijima, Kazuyuki ;
Jurynec, Michael J. ;
Gunther, Derrick ;
Starker, Colby G. ;
Locke, Alexandra S. ;
Weis, Allison M. ;
Voytas, Daniel F. ;
Grunwald, David Jonah .
PLOS GENETICS, 2012, 8 (08)
[8]   The mammalian Numb phosphotyrosine-binding domain - Characterization of binding specificity and identification of a novel PDZ domain-containing Numb binding protein, LNX [J].
Dho, SE ;
Jacob, S ;
Wolting, CD ;
French, MB ;
Rohrschneider, LR ;
McGlade, CJ .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1998, 273 (15) :9179-9187
[9]   TAL Effector-Nucleotide Targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction [J].
Doyle, Erin L. ;
Booher, Nicholas J. ;
Standage, Daniel S. ;
Voytas, Daniel F. ;
Brendel, Volker P. ;
VanDyk, John K. ;
Bogdanove, Adam J. .
NUCLEIC ACIDS RESEARCH, 2012, 40 (W1) :W117-W122
[10]   The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene [J].
Duret, L ;
Chureau, C ;
Samain, S ;
Weissenbach, J ;
Avner, P .
SCIENCE, 2006, 312 (5780) :1653-1655