The heterotaxy gene GALNT11 glycosylates Notch to orchestrate cilia type and laterality

Nature

Volumn 504, Issue 7480, 2013, Pages 456-459

  Boskovski, Marko T ^a,c   Yuan, Shiaulou ^a   Pedersen, Nis Borbye ^b   Goth, Christoffer Knak ^b   Makova, Svetlana ^a   Clausen, Henrik ^b   Brueckner, Martina ^a   Khokha, Mustafa K ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM PROTEIN; ADAM17 PROTEIN; BIOLOGICAL MARKER; COCO PROTEIN; EPIDERMAL GROWTH FACTOR; GLYCOSYLATED PROTEIN; N ACETYLGALACTOSAMINE TYPE O GLYCOSYLATION ENZYME; NOTCH INTRACELLULAR DOMAIN; NOTCH1 RECEPTOR; PITX2C PROTEIN; POLYCYSTIN 2; PROTEIN; UNCLASSIFIED DRUG;

CILIATE; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; PEPTIDE; SENSORY SYSTEM; SPATIAL DISTRIBUTION;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; CILIARY DYSKINESIA; CILIARY MOTILITY; CONTROLLED STUDY; EMBRYO; EUKARYOTIC FLAGELLUM; FEMALE; GALNT11 GENE; GENE FUNCTION; GENE OVEREXPRESSION; GENE SILENCING; HEMISPHERIC DOMINANCE; HETEROTAXY SYNDROME; HUMAN; IN VITRO STUDY; INTRACELLULAR SIGNALING; MARKER GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; XENOPUS TROPICALIS;

ADAM PROTEINS; AMINO ACID SEQUENCE; ANIMALS; BODY PATTERNING; CILIA; EMBRYO, NONMAMMALIAN; GLYCOSYLATION; HETEROTAXY SYNDROME; HUMANS; MICE; MOLECULAR SEQUENCE DATA; N-ACETYLGALACTOSAMINYLTRANSFERASES; PEPTIDE FRAGMENTS; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; XENOPUS; XENOPUS PROTEINS;

VERTEBRATA; XENOPUS TROPICALIS;

EID: 84890557385     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12723     Document Type: Article

References (40)

1. Sutherland, M. J. & Ware, S. M. Disorders of left-right asymmetry: heterotaxy and situs inversus. Am. J. Med. Genet. C. Semin. Med. Genet. 151C, 307-317 (2009).
2. Nonaka, S. et al. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95, 829-837 (1998).
3. McGrath, J. , Somlo, S. , Makova, S. , Tian, X. & Brueckner, M. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114, 61-73 (2003).
4. Yoshiba, S. et al. Cilia at the node of mouse embryos sense fluid flow for left-right determination via Pkd2. Science 338, 226-231 (2012).
5. Schweickert, A. et al. Cilia-driven leftward flow determines laterality in Xenopus. Curr. Biol. 17, 60-66 (2007).
6. Kramer-Zucker, A. G. et al. Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 132, 1907-1921 (2005).
7. Fakhro, K. A. et al. Rare copynumber variations in congenital heart disease patients identify unique genes in left-right patterning. Proc. Natl Acad. Sci. USA 108, 2915-2920 (2011).
8. Greenway, S. C. et al. De novo copy number variants identify new genes and loci in isolated sporadic tetralogy of Fallot. Nature Genet. 41, 931-935 (2009).
9. Zaidi, S. et al. De novo mutations in histone-modifying genes in congenital heart disease. Nature 498, 220-223 (2013).
10. Bennett, E. P. et al. Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology 22, 736-756 (2012).
11. Schweickert, A. et al. The nodal inhibitor Coco is a critical target of leftward flow in Xenopus. Curr. Biol. 20, 738-743 (2010).
12. Deblandre, G. A. , Wettstein, D. A. , Koyano-Nakagawa, N. & Kintner, C. A two-step mechanism generates the spacing pattern of the ciliated cells in the skin of Xenopus embryos. Development 126, 4715-4728 (1999).
13. Artavanis-Tsakonas, S. & Muskavitch, M. A. Notch: the past, the present, and the future. Curr. Top. Dev. Biol. 92, 1-29 (2010).
14. Wettstein, D. A. , Turner, D. L. & Kintner, C. The Xenopus homolog of Drosophila Suppressor of Hairless mediates Notch signaling during primary neurogenesis. Development 124, 693-702 (1997).
15. Rana, N. A. & Haltiwanger, R. S. Fringe benefits: functional and structural impacts of O-glycosylation on the extracellular domain of Notch receptors. Curr. Opin. Struct. Biol. 21, 583-589 (2011).
16. Schwientek, T. et al. Functional conservation of subfamilies of putative UDP-Nacetylgalactosamine: polypeptide N-acetylgalactosaminyltransferases in Drosophila, Caenorhabditis elegans, and mammals. One subfamily composed of l(2)35Aa is essential in Drosophila. J. Biol. Chem. 277, 22623-22638 (2002).
17. Brou, C. et al. A novel proteolytic cleavage involved in Notch signaling: the role of the disintegrin-metalloprotease TACE. Mol. Cell 5, 207-216 (2000).
18. Gram Schjoldager, K. T. et al. A systematic study of site-specific GalNAc-type O-glycosylation modulating proprotein convertase processing. J. Biol. Chem. 286, 40122-40132 (2011).
19. Kato, Y. Themultiple roles of Notch signaling during left-right patterning. Cell. Mol. Life Sci. 68, 2555-2567 (2011).
20. Lopes, S. S. et al. Notch signalling regulates left-right asymmetry through ciliary length control. Development 137, 3625-3632 (2010).
21. Krebs, L. T. et al. Notch signaling regulates left-right asymmetry determination by inducing Nodal expression. Genes Dev. 17, 1207-1212 (2003).
22. Pennekamp, P. et al. The ion channel polycystin-2 is required for left-right axis determination in mice. Curr. Biol. 12, 938-943 (2002).
23. Duldulao, N. A. , Lee, S. & Sun, Z. Cilia localization is essential for in vivo functions of the Joubert syndrome protein Arl13b/Scorpion. Development 136, 4033-4042 (2009).
24. Raya, A. et al. Notch activity acts as a sensor for extracellular calcium during vertebrate left-right determination. Nature 427, 121-128 (2004).
25. Stubbs, J. L. , Oishi, I. , Izpisua Belmonte, J. C. & Kintner, C. The forkhead protein Foxj1 specifies node-like cilia in Xenopus and zebrafishembryos. NatureGenet. 40, 1454-1460 (2008).
26. Bisgrove, B. W. , Makova, S. , Yost, H. J. & Brueckner, M. RFX2 is essential in the ciliated organ of asymmetry and an RFX2 transgene identifies a population of ciliated cells sufficient for fluid flow. Dev. Biol. 363, 166-178 (2012).
27. Chung, M. I. et al. RFX2 is broadly required for ciliogenesis during vertebrate development. Dev. Biol. 363, 155-165 (2012).
28. Shinohara, K. et al. Two rotating cilia in the node cavity are sufficient to break leftright symmetry in the mouse embryo. Nature Commun. 3, 622 (2012).
29. Kamura, K. et al. Pkd1l1 complexes with Pkd2 on motile cilia and functions to establish the left-right axis. Development 138, 1121-1129 (2011).
30. Vick, P. et al. Flow on the right side of the gastrocoel roof plate is dispensable for symmetry breakage in the frog Xenopus laevis. Dev. Biol. 331, 281-291 (2009).
31. del Viso, F. & Khokha, M. Generating diploid embryos from Xenopus tropicalis. Methods Mol. Biol. 917, 33-41 (2012).
32. Nieuwkoop, P. D. &Faber, J. Normal Table of Xenopus laevis (Daudin): a Systematical and Chronological Survey of the Development from the Fertilized Egg Till the End of Metamorphosis (Garland, 1994).
33. Khokha, M. K. et al. Techniques and probes for the study of Xenopus tropicalis development. Dev. Dyn. 225, 499-510 (2002).
34. Vonica, A. &Brivanlou, A. H. The left-right axis is regulated by the interplay of Coco, Xnr1 and derriere in Xenopus embryos. Dev. Biol. 303, 281-294 (2007).
35. Caspary, T. , Larkins, C. E. & Anderson, K. V. The graded response to Sonic Hedgehog depends on cilia architecture. Dev. Cell 12, 767-778 (2007).
36. Piperno, G. & Fulller, M. T. Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms. J. Cell Biol. 101, 2085-2094 (1985).
37. Pedersen, J. W. et al. Lectin domains of polypeptide GalNAc transferases exhibit glycopeptide binding specificity. J. Biol. Chem. 286, 32684-32696 (2011).
38. Walentek, P. , Beyer, T. , Thumberger, T. , Schweickert, A. & Blum, M. ATP4a is required for Wnt-dependent Foxj1 expression and leftward flow in Xenopus leftright development. Cell Rep. 1, 516-527 (2012).
39. Steentoft, C. et al. Mining the O-glycoproteome using zinc-finger nucleaseglycoengineered SimpleCell lines. Nature Methods 8, 977-982 (2011).
40. Steentoft, C. et al. Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. EMBO J. 32, 1478-1488 (2013).