Glycosylation Genes Essential for Mouse Embryonic Development

Michael Pierce; Pamela Stanley

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Varki A, Cummings RD, Esko JD, et al., editors. Essentials of Glycobiology [Internet]. 3rd edition. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2015-2017.

Essentials of Glycobiology [Internet]. 3rd edition.

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Online Appendix 27AGlycosylation Genes Essential for Mouse Embryonic Development

Michael Pierce and Pamela Stanley.

Published online: September 5, 2017.

Table 1

Gene	Glycan substrate accumulated	Glycan(s) not generated	Stage of death	Reference(s)
N-glycans
Mpi	fructose-6-P	Man-6-P	~E11.5	DeRossi et al. 2006
Pmm2	Man-6-P	Man-1-P	~E3.5	Thiel et al. 2006
Dpagt1	Dol-P	GlcNAc-P-P-Dol	E4-5	Marek et al. 1999
Mgat1	Man₅GlcNAc₂Asn	GlcNAc-Man₅GlcNAc₂Asn	~E9.5	Ioffe and Stanley 1994; Metzler et al. 1994
Man2a1+ Man2a2	GlcNAcMan₅GlcNAc₂Asn	GlcNAc-Man₃GlcNAc₂Asn	E15.5-18.5-P0	Akama et al. 2006
GPI-anchors
Piga	naked GPI-anchor	GlcNAc-GPI-anchor	E7.5-9.5	Nozaki et al. 1999
O-GalNAc glycans
C1galt1	GalNAc-O-Ser/Thr	Gal-GalNAc-Ser/Thr	~E13.5	Xia et al. 2004
C1galt1c1	GalNAc-O-Ser/Thr	Gal-GalNAc-Ser/Thr	~E13.5	Wang et al. 2010
O-fucose glycans
Pofut1	C₂XXXXS/TC₃ EGF repeats	Fuc-O-EGF	~E9.5	Shi and Stanley 2003
Lfng	Fuc-O-EGF	GlcNAc-Fuc-O-EGF	≤P0	Evrard et al. 1998; Zhang and Gridley 1998
Pofut2	TSR type 1 repeats	Fuc-O-TSR type 1	~E6.5	Du et al. 2010
O-mannose glycans
Pomt1	unmodified Ser/Thr	Man-O-Ser/Thr	E7.5-9.5	Willer et al. 2004
Pomt2	unmodified Ser/Thr	Man-O-Ser/Thr	~E9.5	Hu et al. 2011
B4gat1	Xyl-Rbo5P-Rbo5P-GalNAc-GlcNAc-Man(P)-O-Ser/Thr	priming GlcA for XlyGlcA matriglycan added by LARGE	~E9.5	Wright et al. 2012; Willer et al. 2014; Kanagawa et al. 2016
O-glucose glycans
Poglut1	C₁XSXPTC₂ EGF repeats	Glc-O-EGF repeat	~E10.5	Fernandez-Valdivia et al. 2011
Glycosamino-glycans (GAGs)
Ext1	core GAG lacks HS	HS	E6.5-8.5	Lin et al. 2000
Ext2	core GAG lacks HS	HS	E6.5-8.5	Stickens et al. 2005
Ndst1+Ndst2	no N sulfation of HS	HS with GlcNS	~E12.5	Holmborn et al. 2004
Hs6st1	reduced 6-O-sulfation GlcN in HS	HS with GlcN6S	≥E15.5	Habuchi et al. 2007
Hs6st1+Hs2st	very reduced 2-O- and 6-O-sulfation GlcN in HS	HS with GlcN-O-2S and GlcN-O-6S	<E15,5	Conway et al. 2011
Chst11	reduced 4-O-sulfation of GalN in CS	CS with GalN-O-4S	~P0	Bian et al. 2011
Glycolipids
Ugcg	Ceramide lacks Glc	Glc-Cer	≤E9.5	Yamashita et al. 1999
B3gnt5	GalGlc-Cer	GlcNAc-Gal-Glc-Cer	~E3.5	Biellmann et al. 2008
B4galt5	GlcNAcGalGlc-Cer	Gal-GlcNAc-Gal-Glc-Cer	~E10.5	Kumagai et al. 2009; Nishie et al. 2010
Nucleotide sugars
Gne	Mannosamine	GCs without sialic acid	~E9.5	Schwarzkopf et al. 2002
Ugdh	UDP-Glc	UDP-GlcA	~E4.5	Garcia-Garcia and Anderson 2003
Slc35c1	GDP-Fuc	GCs with little Fuc	~P0	Hellbusch et al. 2007
Slc35d1	high UDP-GlcA and UDP-GalNAc in cytoplasm	CS GAGs	~P0	Hiraoka et al. 2007

: Modified, with permission, from Stanley P. 2016. What have we learned from glycosyltransferase knockouts in mice? J Mol Biol 2016 Aug 14;428(16):3166-82. doi: 10.1016/j.jmb.2016.03.025.
: TSR, thrombospondin repeat; EGF, epidermal growth factor; LARGE, like-acetylglucosaminyltransferase; GC, glycoconjugate; HS, heparan sulfate; CS, chondroitin sulfate; KS, keratan sulfate.

Reference List

Akama TO, Nakagawa H, Wong NK, Sutton-Smith M, Dell A, Morris HR, Nakayama J, Nishimura S, Pai A, Moremen KW, et al. Essential and mutually compensatory roles of α-mannosidase II and α-mannosidase IIx in N-glycan processing in vivo in mice. Proc Natl Acad Sci. 2006;103:8983–8988. [PMC free article: PMC1474017] [PubMed: 16754854]
Bian S, Akyuz N, Bernreuther C, Loers G, Laczynska E, Jakovcevski I, Schachner M. Dermatan sulfotransferase Chst14/D4st1, but not chondroitin sulfotransferase Chst11/C4st1, regulates proliferation and neurogenesis of neural progenitor cells. J Cell Sci. 2011;124:4051–4063. [PubMed: 22159417]
Biellmann F, Hulsmeier AJ, Zhou D, Cinelli P, Hennet T. The Lc3-synthase gene B3gnt5 is essential to pre-implantation development of the murine embryo. BMC Dev Biol. 2008;8:109. [PMC free article: PMC2596124] [PubMed: 19014510]
Conway CD, Price DJ, Pratt T, Mason JO. Analysis of axon guidance defects at the optic chiasm in heparan sulphate sulphotransferase compound mutant mice. J Anat. 2011;219:734–742. [PMC free article: PMC3237881] [PubMed: 21951307]
DeRossi C, Bode L, Eklund EA, Zhang F, Davis JA, Westphal V, Wang L, Borowsky AD, Freeze HH. Ablation of mouse phosphomannose isomerase (Mpi) causes mannose 6-phosphate accumulation, toxicity, and embryonic lethality. J Biol Chem. 2006;281:5916–5927. [PubMed: 16339137]
Du J, Takeuchi H, Leonhard-Melief C, Shroyer KR, Dlugosz M, Haltiwanger RS, Holdener BC. O-fucosylation of thrombospondin type 1 repeats restricts epithelial to mesenchymal transition (EMT) and maintains epiblast pluripotency during mouse gastrulation. Dev Biol. 2010;346:25–38. [PMC free article: PMC2937101] [PubMed: 20637190]
Evrard YA, Lun Y, Aulehla A, Gan L, Johnson RL. lunatic fringe is an essential mediator of somite segmentation and patterning. Nature. 1998;394:377–381. [PubMed: 9690473]
Fernandez-Valdivia R, Takeuchi H, Samarghandi A, Lopez M, Leonardi J, Haltiwanger RS, Jafar-Nejad H. Regulation of mammalian Notch signaling and embryonic development by the protein O-glucosyltransferase Rumi. Development. 2011;138:1925–1934. [PMC free article: PMC3082299] [PubMed: 21490058]
Garcia-Garcia MJ, Anderson KV. Essential role of glycosaminoglycans in Fgf signaling during mouse gastrulation. Cell. 2003;114:727–737. [PubMed: 14505572]
Habuchi H, Nagai N, Sugaya N, Atsumi F, Stevens RL, Kimata K. Mice deficient in heparan sulfate 6-O-sulfotransferase-1 exhibit defective heparan sulfate biosynthesis, abnormal placentation, and late embryonic lethality. J Biol Chem. 2007;282:15578–15588. [PubMed: 17405882]
Hellbusch CC, Sperandio M, Frommhold D, Yakubenia S, Wild MK, Popovici D, Vestweber D, Grone HJ, von Figura K, Lubke T, et al. Golgi GDP-fucose transporter-deficient mice mimic congenital disorder of glycosylation IIc/leukocyte adhesion deficiency II. J Biol Chem. 2007;282:10762–10772. [PubMed: 17276979]
Hiraoka S, Furuichi T, Nishimura G, Shibata S, Yanagishita M, Rimoin DL, Superti-Furga A, Nikkels PG, Ogawa M, Katsuyama K, et al. Nucleotide-sugar transporter SLC35D1 is critical to chondroitin sulfate synthesis in cartilage and skeletal development in mouse and human. Nat Med. 2007;13:1363–1367. [PubMed: 17952091]
Holmborn K, Ledin J, Smeds E, Eriksson I, Kusche-Gullberg M, Kjellen L. Heparan sulfate synthesized by mouse embryonic stem cells deficient in NDST1 and NDST2 is 6-O-sulfated but contains no N-sulfate groups. J Biol Chem. 2004;279:42355–42358. [PubMed: 15319440]
Hu H, Li J, Gagen CS, Gray NW, Zhang Z, Qi Y, Zhang P. Conditional knockout of protein O-mannosyltransferase 2 reveals tissue-specific roles of O-mannosyl glycosylation in brain development. J Comp Neurol. 2011;519:1320–1337. [PMC free article: PMC3634366] [PubMed: 21452199]
Ioffe E, Stanley P. Mice lacking N-acetylglucosaminyltransferase I activity die at mid-gestation, revealing an essential role for complex or hybrid N-linked carbohydrates. Proc Natl Acad Sci. 1994;91:728–732. [PMC free article: PMC43022] [PubMed: 8290590]
Kanagawa M, Kobayashi K, Tajiri M, Manya H, Kuga A, Yamaguchi Y, Akasaka-Manya K, Furukawa J, Mizuno M, Kawakami H, Shinohara Y, Wada Y, Endo T, Toda T. Identification of a post-translational modification with ribitol-phosphate and its defect in muscular dystrophy. Cell Reports. 2016;14:2209–2223. [PubMed: 26923585]
Kumagai T, Tanaka M, Yokoyama M, Sato T, Shinkai T, Furukawa K. Early lethality of β-1,4-galactosyltransferase V-mutant mice by growth retardation. Biochem Biophys Res Commun. 2009;379:456–459. [PubMed: 19114028]
Lin X, Wei G, Shi Z, Dryer L, Esko JD, Wells DE, Matzuk MM. Disruption of gastrulation and heparan sulfate biosynthesis in EXT1-deficient mice. Dev Biol. 2000;224:299–311. [PubMed: 10926768]
Marek KW, Vijay IK, Marth JD. A recessive deletion in the GlcNAc-1-phosphotransferase gene results in peri-implantation embryonic lethality. Glycobiology. 1999;9:1263–1271. [PubMed: 10536042]
Metzler M, Gertz A, Sarkar M, Schachter H, Schrader JW, Marth JD. Complex asparagine-linked oligosaccharides are required for morphogenic events during post-implantation development. EMBO J. 1994;13:2056–2065. [PMC free article: PMC395055] [PubMed: 8187759]
Nishie T, Hikimochi Y, Zama K, Fukusumi Y, Ito M, Yokoyama H, Naruse C, Ito M, Asano M. β4-galactosyltransferase-5 is a lactosylceramide synthase essential for mouse extra-embryonic development. Glycobiology. 2010;20:1311–1322. [PubMed: 20574042]
Nozaki M, Ohishi K, Yamada N, Kinoshita T, Nagy A, Takeda J. Developmental abnormalities of glycosylphosphatidylinositol-anchor-deficient embryos revealed by Cre/loxP system. Lab Invest. 1999;79:293–299. [PubMed: 10092065]
Schwarzkopf M, Knobeloch KP, Rohde E, Hinderlich S, Wiechens N, Lucka L, Horak I, Reutter W, Horstkorte R. Sialylation is essential for early development in mice. Proc Natl Acad Sci. 2002;99:5267–5270. [PMC free article: PMC122758] [PubMed: 11929971]
Shi S, Stanley P. Protein O-fucosyltransferase 1 is an essential component of Notch signaling pathways. Proc Natl Acad Sci. 2003;100:5234–5239. [PMC free article: PMC154328] [PubMed: 12697902]
Stickens D, Zak BM, Rougier N, Esko JD, Werb Z. Mice deficient in Ext2 lack heparan sulfate and develop exostoses. Development. 2005;132:5055–5068. [PMC free article: PMC2767329] [PubMed: 16236767]
Thiel C, Lubke T, Matthijs G, von Figura K, Korner C. Targeted disruption of the mouse phosphomannomutase 2 gene causes early embryonic lethality. Mol Cell Biol. 2006;26:5615–5620. [PMC free article: PMC1592760] [PubMed: 16847317]
Wang Y, Ju T, Ding X, Xia B, Wang W, Xia L, He M, Cummings RD. Cosmc is an essential chaperone for correct protein O-glycosylation. Proc Natl Acad Sci U S A. 2010;107:9228–9233. [PMC free article: PMC2889116] [PubMed: 20439703]
Willer T, Prados B, Falcon-Perez JM, Renner-Muller I, Przemeck GK, Lommel M, Coloma A, Valero MC, de Angelis MH, Tanner W, et al. Targeted disruption of the Walker–Warburg syndrome gene Pomt1 in mouse results in embryonic lethality. Proc Natl Acad Sci. 2004;101:14126–14131. [PMC free article: PMC521095] [PubMed: 15383666]
Willer T, Inamori KI, Venzke D, Harvey C, Morgensen G, Hara Y, Beltran Valero de Bernabe D, Yu L, Wright KM, Campbell KP. The glucuronyltransferase B4GAT1 is required for initiation of LARGE-mediated α-dystroglycan functional glycosylation. eLife. 2014;3 [PMC free article: PMC4227050] [PubMed: 25279699] [CrossRef]
Wright KM, Lyon KA, Leung H, Leahy DJ, Ma L, Ginty DD. Dystroglycan organizes axon guidance cue localization and axonal pathfinding. Neuron. 2012;76:931–944. [PMC free article: PMC3526105] [PubMed: 23217742]
Xia L, Ju T, Westmuckett A, An G, Ivanciu L, McDaniel JM, Lupu F, Cummings RD, McEver RP. Defective angiogenesis and fatal embryonic hemorrhage in mice lacking core 1-derived O-glycans. J Cell Biol. 2004;164:451–459. [PMC free article: PMC2172228] [PubMed: 14745002]
Yamashita T, Wada R, Sasaki T, Deng C, Bierfreund U, Sandhoff K, Proia RL. A vital role for glycosphingolipid synthesis during development and differentiation. Proc Natl Acad Sci. 1999;96:9142–9147. [PMC free article: PMC17746] [PubMed: 10430909]
Zhang N, Gridley T. Defects in somite formation in lunatic fringe-deficient mice. Nature. 1998;394:374–377. [PubMed: 9690472]

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Pierce M, Stanley P. Glycosylation Genes Essential for Mouse Embryonic Development. 2017 Sep 5. In: Varki A, Cummings RD, Esko JD, et al., editors. Essentials of Glycobiology [Internet]. 3rd edition. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2015-2017. Online Appendix 27A.
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