Protein O-Glucosyltransferase 1 (POGLUT1) Promotes Mouse Gastrulation through Modification of the Apical Polarity Protein CRUMBS2

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Post-translational addition of sugar chains is essential for normal activity of many secreted and transmembrane proteins and dozens of human genetic diseases are associated with congenital disorders of glycosylation. Protein O-glucosyltransferase 1 (POGLUT1), which is essential for early mouse development, catalyzes the addition of O-glucose to extracellular EGF repeats of proteins, including NOTCH1. Here we show that mouse POGLUT1 modifies NOTCH1 in vivo; however, the essential role of POGLUT1 in gastrulation is due to POGLUT1-dependent glycosylation of EGF repeats in the apical polarity protein CRUMBS2. In contrast to findings in Drosophila, where modification of Crumbs by POGLUT1 is not required, mouse POGLUT1 is required for the activity of CRUMBS2: the unmodified protein fails to localize to the apical membrane and the gastrulation defects of Poglut1 mutants are indistinguishable from those of Crumbs2 mutants. Human mutations in POGLUT1 cause Dowling-Degos Disease type 4; the hyperpigmentation associated with this autosomal dominant disease was previously attributed to altered Notch signaling, but our results suggest that this disease and other POGLUT1-associated phenotypes may be due to altered activity of CRUMBS proteins.

Vyšlo v časopise: Protein O-Glucosyltransferase 1 (POGLUT1) Promotes Mouse Gastrulation through Modification of the Apical Polarity Protein CRUMBS2. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005551
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005551

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1. Ishio A, Sasamura T, Ayukawa T, Kuroda J, Ishikawa HO, Aoyama N, Matsumoto K, Gushiken T, Okajima T, Yamakawa T, Matsuno K. O-fucose monosaccharide of Drosophila Notch has a temperature-sensitive function and cooperates with O-glucose glycan in Notch transport and Notch signaling activation. J Biol Chem. 2015 Jan 2;290(1):505–19. doi: 10.1074/jbc.M114.616847 Epub 2014 Nov 5. 25378397; PubMed Central PMCID: PMC4281752.

2. Moremen KW, Molinari M. N-linked glycan recognition and processing: the molecular basis of endoplasmic reticulum quality control. Curr Opin Struct Biol. 2006 Oct; 16(5): 592–9. Epub 2006 Aug 30. Review. 16938451; PubMed Central PMCID: PMC3976202.

3. Imperiali B, Rickert KW. Conformational implications of asparagine-linked glycosylation. Proc Natl Acad Sci U S A. 1995 Jan 3; 92(1): 97–101. 7816856; PubMed Central PMCID: PMC42824.

4. Panin VM, Papayannopoulos V, Wilson R, Irvine KD. Fringe modulates Notch-ligand interactions. Nature. 1997 Jun 26; 387(6636): 908–12. 9202123.

5. Okajima T, Xu A, Irvine KD. Modulation of notch-ligand binding by protein O-fucosyltransferase 1 and fringe. J Biol Chem. 2003 Oct 24; 278(43): 42340–5. Epub 2003 Aug 8. 12909620.

6. Bruckner K, Perez L, Clausen H, Cohen S. Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature. 2000 Jul 27; 406(6794): 411–5. Erratum in: Nature 2000 Oct 5;407(6804):654. 10935637.

7. Okajima T, Reddy B, Matsuda T, Irvine KD. Contributions of chaperone and glycosyltransferase activities of O-fucosyltransferase 1 to Notch signaling. BMC Biol. 2008; 6 : 1. doi: 10.1186/1741-7007-6-1 10.1186/1741-7007-6-1. 18194540; PubMed Central PMCID: PMC2242781.

8. Schachter H, Freeze HH. Glycosylation diseases: quo vadis? Biochim Biophys Acta. 2009 Sep; 1792(9):925–30. doi: 10.1016/j.bbadis.2008.11.002 Epub 2008 Nov 13. Review. 19061954; PubMed Central PMCID: PMC3927646.

9. Freeze HH. Understanding human glycosylation disorders: biochemistry leads the charge. J Biol Chem. 2013 Mar 8;288(10):6936–45. doi: 10.1074/jbc.R112.429274 Epub 2013 Jan 17. Review. 23329837; PubMed Central PMCID: PMC3591604.

10. Freeze HH, Aebi M. Altered glycan structures: the molecular basis of congenital disorders of glycosylation. Curr Opin Struct Biol. 2005 Oct; 15(5): 490–8. Review. 16154350.

11. Okamura Y, Saga Y. Pofut1 is required for the proper localization of the Notch receptor during mouse development. Mech Dev. 2008 Aug; 125(8): 663–73. doi: 10.1016/j.mod.2008.04.007 Epub 2008 May 4. 18547789.

12. Du J, Takeuchi H, Leonhard-Melief C, Shroyer KR, Dlugosz M, Haltiwanger RS, et al. O-fucosylation of thrombospondin type 1 repeats restricts epithelial to mesenchymal transition (EMT) and maintains epiblast pluripotency during mouse gastrulation. Dev Biol. 2010 Oct 1; 346(1): 25–38. doi: 10.1016/j.ydbio.2010.07.008 Epub 2010 Jul 14. 20637190; PubMed Central PMCID: PMC2937101.

13. Fernandez-Valdivia R, Takeuchi H, Samarghandi A, Lopez M, Leonardi J, Haltiwanger RS, et al. Regulation of mammalian Notch signaling and embryonic development by the protein O-glucosyltransferase Rumi. Development. 2011 May;138(10):1925–34. doi: 10.1242/dev.060020 Epub 2011 Apr 13. 21490058; PubMed Central PMCID: PMC3082299.

14. Willer T, Prados B, Falcon-Perez JM, Renner-Muller I, Przemeck GK, Lommel M, et al. Targeted disruption of the Walker-Warburg syndrome gene Pomt1 in mouse results in embryonic lethality. Proc Natl Acad Sci U S A. 2004 Sep 28; 101(39): 14126–31. Epub 2004 Sep 21. 15383666; PubMed Central PMCID: PMC521095.

15. Garcia-Garcia MJ, Anderson KV. Essential role of glycosaminoglycans in Fgf signaling during mouse gastrulation. Cell. 2003 Sep 19; 114(6): 727–37. 14505572.

16. Stahl M, Uemura K, Ge C, Shi S, Tashima Y, Stanley P. Roles of Pofut1 and O-fucose in mammalian Notch signaling. J Biol Chem. 2008 May 16;283(20):13638–51. doi: 10.1074/jbc.M802027200 Epub 2008 Mar 17. 18347015; PubMed Central PMCID: PMC2376238.

17. Yao D, Huang Y, Huang X, Wang W, Yan Q, Wei L, Xin W, Gerson S, Stanley P, Lowe JB, Zhou L. Protein O-fucosyltransferase 1 (Pofut1) regulates lymphoid and myeloid homeostasis through modulation of Notch receptor ligand interactions. Blood. 2011 May 26;117(21):5652–62. doi: 10.1182/blood-2010-12-326074 Epub 2011 Apr 4. 21464368; PubMed Central PMCID: PMC3110024.

18. Wang W, Yu S, Zimmerman G, Wang Y, Myers J, Yu VW, Huang D, Huang X, Shim J, Huang Y, Xin W, Qiao P, Yan M, Xin W, Scadden DT, Stanley P, Lowe JB, Huang AY,Siebel CW, Zhou L. Notch Receptor-Ligand Engagement Maintains Hematopoietic Stem Cell Quiescence and Niche Retention. Stem Cells. 2015 Jul;33(7):2280–93. doi: 10.1002/stem.2031 Epub 2015 May 13. 25851125; PubMed Central PMCID: PMC4478168.

19. Shao L, Moloney DJ, Haltiwanger R. Fringe modifies O-fucose on mouse Notch1 at epidermal growth factor-like repeats within the ligand-binding site and the Abruptex region. J Biol Chem. 2003 Mar 7; 278(10): 7775–82. Epub 2002 Dec 16. 12486116.

20. Alfaro JF, Gong CX, Monroe ME, Aldrich JT, Clauss TR, Purvine SO, et al. Tandem mass spectrometry identifies many mouse brain O-GlcNAcylated proteins including EGF domain-specific O-GlcNAc transferase targets. Proc Natl Acad Sci U S A. 2012 May 8; 109(19): 7280–5. doi: 10.1073/pnas.1200425109 Epub 2012 Apr 19. 22517741; PubMed Central PMCID: PMC3358849.

21. Rana NA, Nita-Lazar A, Takeuchi H, Kakuda S, Luther KB, Haltiwanger RS. O-glucose trisaccharide is present at high but variable stoichiometry at multiple sites on mouse Notch1. J Biol Chem. 2011 Sep 9; 286(36): 31623–37. doi: 10.1074/jbc.M111.268243 Epub 2011 Jul 8. 21757702; PubMed Central PMCID: PMC3173066.

22. Wang Y, Shao L, Shi S, Harris RJ, Spellman MW, Stanley P, et al. Modification of epidermal growth factor-like repeats with O-fucose. Molecular cloning and expression of a novel GDP-fucose protein O-fucosyltransferase. J Biol Chem. 2001 Oct 26; 276(43): 40338–45. Epub 2001 Aug 27. 11524432.

23. Sakaidani Y, Ichiyanagi N, Saito C, Nomura T, Ito M, Nishio Y, et al. O-linked-N-acetylglucosamine modification of mammalian Notch receptors by an atypical O-GlcNAc transferase Eogt1. Biochem Biophys Res Commun. 2012 Mar 2;419(1):14–9. doi: 10.1016/j.bbrc.2012.01.098 Epub 2012 Jan 28. 22310717.

24. Acar M, Jafar-Nejad H, Takeuchi H, Rajan A, Ibrani D, Rana NA, et al. Rumi is a CAP10 domain glycosyltransferase that modifies Notch and is required for Notch signaling. Cell. 2008 Jan 25; 132(2): 247–58. doi: 10.1016/j.cell.2007.12.016 18243100; PubMed Central PMCID: PMC2275919.

25. Okajima T, Irvine KD. Regulation of notch signaling by O-linked fucose. Cell. 2002 Dec 13; 111(6): 893–904. 12526814.

26. Shi S, Stanley P. Protein O-fucosyltransferase 1 is an essential component of Notch signaling pathways. Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5234–9. Epub 2003 Apr 15. 12697902; PubMed Central PMCID: PMC154328.

27. Teng Y, Liu Q, Ma J, Liu F, Han Z, Wang Y, et al. Cloning, expression and characterization of a novel human CAP10-like gene hCLP46 from CD34(+) stem/progenitor cells. Gene. 2006 Apr 12; 371(1): 7–15. Epub 2006 Mar 9. 16524674.

28. Wang Y, Chang N, Zhang T, Liu H, Ma W, Chu Q, et al. Overexpression of human CAP10-like protein 46 KD in T-acute lymphoblastic leukemia and acute myelogenous leukemia. Genet Test Mol Biomarkers. 2010 Feb; 14(1): 127–33. doi: 10.1089/gtmb.2009.0145 20143914.

29. Takeuchi H, Fernandez-Valdivia RC, Caswell DS, Nita-Lazar A, Rana NA, Garner TP, et al. Rumi functions as both a protein O-glucosyltransferase and a protein O-xylosyltransferase. Proc Natl Acad Sci U S A. 2011 Oct 4;108(40):16600–5. doi: 10.1073/pnas.1109696108 21949356

30. van de Pavert SA, Kantardzhieva A, Malysheva A, Meuleman J, Versteeg I, Levelt C, et al. Crumbs homologue 1 is required for maintenance of photoreceptor cell polarization and adhesion during light exposure. J Cell Sci. 2004 Aug 15; 117(Pt 18): 4169–77. 15316081.

31. Whiteman EL, Fan S, Harder JL, Walton KD, Liu CJ, Soofi A, et al. Crumbs3 is essential for proper epithelial development and viability. Mol Cell Biol. 2014 Jan; 34(1): 43–56. doi: 10.1128/MCB.00999-13 Epub 2013 Oct 28. 24164893; PubMed Central PMCID: PMC3911272.

32. Xiao Z, Patrakka J, Nukui M, Chi L, Niu D, Betsholtz C, et al. Deficiency in Crumbs homolog 2 (Crb2) affects gastrulation and results in embryonic lethality in mice. Dev Dyn. 2011 Dec; 240(12): 2646–56. doi: 10.1002/dvdy.22778 Erratum in: Dev Dyn. 2012 Feb;241(2):431. Pikkarainan, Timo [corrected to Pikkarainen, Timo]. 22072575.

33. Kasarskis A, Manova K, Anderson KV. A phenotype-based screen for embryonic lethal mutations in the mouse. Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7485–90. 9636176; PubMed Central PMCID: PMC22659.

34. Gosens I, Sessa A, den Hollander AI, Letteboer SJ, Belloni V, Arends ML, et al. FERM protein EPB41L5 is a novel member of the mammalian CRB-MPP5 polarity complex. Exp Cell Res. 2007 Nov 15; 313(19): 3959–70. Epub 2007 Sep 7. 17920587.

35. Laprise P, Beronja S, Silva-Gagliardi NF, Pellikka M, Jensen AM, McGlade CJ, Tepass U. The FERM protein Yurt is a negative regulatory component of the Crumbs complex that controls epithelial polarity and apical membrane size. Dev Cell. 2006 Sep; 11(3): 363–74. 16950127; PubMed Central PMCID: PMC2834949.

36. Lee JD, Silva-Gagliardi NF, Tepass U, McGlade CJ, Anderson KV. The FERM protein Epb4.1l5 is required for organization of the neural plate and for the epithelial-mesenchymal transition at the primitive streak of the mouse embryo. Development. 2007 Jun; 134(11): 2007–16. 17507402.

37. Garcia-Garcia MJ, Eggenschwiler JT, Caspary T, Alcorn HL, Wyler MR, Huangfu D, et al. Analysis of mouse embryonic patterning and morphogenesis by forward genetics. Proc Natl Acad Sci U S A. 2005 Apr 26;102(17):5913–9. Epub 2005 Mar 8. 15755804; PubMed Central PMCID: PMC1087930.

38. Hayashi S, Lewis P, Pevny L, McMahon AP. Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech Dev. 2002 Dec; 119 Suppl 1: S97–S101. 14516668.

39. Schroeter EH, Kisslinger JA, Kopan R. Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature. 1998 May 28; 393(6683): 382–6. 9620803.

40. Del Monte G, Grego-Bessa J, González-Rajal A, Bolós V, De La Pompa JL. Monitoring Notch1 activity in development: evidence for a feedback regulatory loop. Dev Dyn. 2007 Sep;236(9):2594–614. 17685488.

41. Oka C, Nakano T, Wakeham A, de la Pompa JL, Mori C, Sakai T, et al. Disruption of the mouse RBP-J kappa gene results in early embryonic death. Development. 1995 Oct; 121(10): 3291–301. 7588063.

42. Donoviel DB, Hadjantonakis AK, Ikeda M, Zheng H, Hyslop PS, Bernstein A. Mice lacking both presenilin genes exhibit early embryonic patterning defects. Genes & development. 1999 Nov 1; 13(21): 2801–10. 10557208; PubMed Central PMCID: PMC317124.

43. Haltom AR, Lee TV, Harvey BM, Leonardi J, Chen YJ, Hong Y, et al. The protein O-glucosyltransferase Rumi modifies eyes shut to promote rhabdomere separation in Drosophila. PLoS Genet. 2014 Nov;10(11):e1004795. doi: 10.1371/journal.pgen.1004795 eCollection 2014 Nov. 25412384; PubMed Central PMCID: PMC4238978.

44. Silva J, Barrandon O, Nichols J, Kawaguchi J, Theunissen TW, Smith A. Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol. 2008 Oct 21;6(10):e253. doi: 10.1371/journal.pbio.0060253 18942890; PubMed Central PMCID: PMC2570424.

45. Kakuda S, Haltiwanger RS. Analyzing the posttranslational modification status of Notch using mass spectrometry. Methods Mol Biol. 2014; 1187 : 209–21. doi: 10.1007/978-1-4939-1139-4_16 25053492.

46. Harris RJ, Spellman MW. O-linked fucose and other post-translational modifications unique to EGF modules. Glycobiology. 1993 Jun; 3(3): 219–24. Review. 8358148.

47. Wahi K, Bochter MS, Cole SE. The many roles of Notch signaling during vertebrate somitogenesis. Semin Cell Dev Biol. 2014 Dec 4. pii: S1084-9521(14)00320-6. doi: 10.1016/j.semcdb.2014.11.010 [Epub ahead of print] Review. 25483003.

48. Sigrist CJ, de Castro E, Cerutti L, Cuche BA, Hulo N, Bridge A, et al. New and continuing developments at PROSITE. Nucleic acids research. 2013 Jan;41(Database issue):D344–7. doi: 10.1093/nar/gks1067 Epub 2012 Nov 17. 23161676; PubMed Central PMCID: PMC3531220.

49. den Hollander AI, Davis J, van der Velde-Visser SD, Zonneveld MN, Pierrottet CO, Koenekoop RK, et al. CRB1 mutation spectrum in inherited retinal dystrophies. Hum Mutat. 2004 Nov; 24(5): 355–69. Review. 15459956.

50. Li S, Shen T, Xiao X, Guo X, Zhang Q. Detection of CRB1 mutations in families with retinal dystrophy through phenotype-oriented mutational screening. Int J Mol Med. 2014 Apr; 33(4): 913–8. doi: 10.3892/ijmm.2014.1655 Epub 2014 Feb 12. 24535598.

51. Jalkh N, Guissart C, Chouery E, Yammine T, El Ali N, Farah HA, et al. Report of a novel mutation in CRB1 in a Lebanese family presenting retinal dystrophy. Ophthalmic Genet. 2014 Mar; 35(1): 57–62. doi: 10.3109/13816810.2013.763995 Epub 2013 Jan 30. 23362850.

52. van de Pavert SA, Meuleman J, Malysheva A, Aartsen WM, Versteeg I, Tonagel F, et al. A single amino acid substitution (Cys249Trp) in Crb1 causes retinal degeneration and deregulates expression of pituitary tumor transforming gene Pttg1. J Neurosci. 2007 Jan 17; 27(3): 564–73. 17234588.

53. Slavotinek A, Kaylor J, Pierce H, Cahr M, DeWard SJ, Schneidman-Duhovny D, et al. CRB2 mutations produce a phenotype resembling congenital nephrosis, Finnish type, with cerebral ventriculomegaly and raised alpha-fetoprotein. Am J Hum Genet. 2015 Jan 8; 96(1): 162–9. doi: 10.1016/j.ajhg.2014.11.013 Epub 2014 Dec 31. 25557780; PubMed Central PMCID: PMC4289687.

54. Ebarasi L, Ashraf S, Bierzynska A, Gee HY, McCarthy HJ, Lovric S, et al. Defects of CRB2 cause steroid-resistant nephrotic syndrome. Am J Hum Genet. 2015 Jan 8; 96(1): 153–61. doi: 10.1016/j.ajhg.2014.11.014 Epub 2014 Dec 31. 25557779; PubMed Central PMCID: PMC4289689.

55. Basmanav FB, Oprisoreanu AM, Pasternack SM, Thiele H, Fritz G, Wenzel J, et al. Mutations in POGLUT1, encoding protein O-glucosyltransferase 1, cause autosomal-dominant Dowling-Degos disease. Am J Hum Genet. 2014 Jan 2; 94(1): 135–43. doi: 10.1016/j.ajhg.2013.12.003 24387993; PubMed Central PMCID: PMC3882728.

56. Chu Q, Liu L, Wang W. Overexpression of hCLP46 enhances Notch activation and regulates cell proliferation in a cell type-dependent manner. Cell Prolif. 2013 Jun; 46(3): 254–62. doi: 10.1111/cpr.12037 23692084.

57. Gao Y, Liu T, Huang Y. MicroRNA-134 suppresses endometrial cancer stem cells by targeting POGLUT1 and Notch pathway proteins. FEBS Lett. 2015 Jan 16; 589(2): 207–14. doi: 10.1016/j.febslet.2014.12.002 Epub 2014 Dec 17. 25528443.

58. Jin G, Cao Z, Sun X, Wang K, Huang T, Shen B. Protein O-glucosyltransferase 1 overexpression downregulates p16 in BT474 human breast cancer cells. Oncol Lett. 2014 Aug; 8(2): 594–600. Epub 2014 May 28. 25009645; PubMed Central PMCID: PMC4081438.

59. Rodriguez CI, Buchholz F, Galloway J, Sequerra R, Kasper J, Ayala R, et al. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat Genet. 2000 Jun; 25(2): 139–40. 10835623.

60. Sakai K, Miyazaki J. A transgenic mouse line that retains Cre recombinase activity in mature oocytes irrespective of the cre transgene transmission. Biochem Biophys Res Commun. 1997 Aug 18; 237(2): 318–24. 9268708.

61. Alves CH, Sanz AS, Park B, Pellissier LP, Tanimoto N, Beck SC, et al. Loss of CRB2 in the mouse retina mimics human retinitis pigmentosa due to mutations in the CRB1 gene. Hum Mol Genet. 2013 Jan 1; 22(1): 35–50. doi: 10.1093/hmg/dds398 23001562

62. Mehalow AK, Kameya S, Smith RS, Hawes NL, Denegre JM, Young JA, et al. CRB1 is essential for external limiting membrane integrity and photoreceptor morphogenesis in the mammalian retina. Hum Mol Genet. 2003 Sep 1; 12(17): 2179–89. doi: 10.1093/hmg/dds398 Epub 2012 Sep 21. 23001562.

63. Collignon J, Varlet I, Robertson EJ. Relationship between asymmetric nodal expression and the direction of embryonic turning. Nature. 1996 May 9; 381(6578): 155–8. 8610012.

64. DasGupta R, Fuchs E. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development. 1999 Oct; 126(20): 4557–68. 10498690.

65. Rumble SM, Lacroute P, Dalca AV, Fiume M, Sidow A, Brudno M. SHRiMP: accurate mapping of short color-space reads. PLoS Comput Biol. 2009 May; 5(5):e1000386. doi: 10.1371/journal.pcbi.1000386 Epub 2009 May 22. 19461883; PubMed Central PMCID: PMC2678294.

66. Laprise P, Beronja S, Silva-Gagliardi NF, Pellikka M, Jensen AM, McGlade CJ, et al. The FERM protein Yurt is a negative regulatory component of the Crumbs complex that controls epithelial polarity and apical membrane size. Dev Cell. 2006 Sep; 11(3): 363–74. 16950127; PubMed Central PMCID: PMC2834949.

67. Makarova O, Roh MH, Liu CJ, Laurinec S, Margolis B. Mammalian Crumbs3 is a small transmembrane protein linked to protein associated with Lin-7 (Pals1). Gene. 2003 Jan 2; 302(1–2): 21–9. 12527193.

68. Tucker KL, Beard C, Dausmann J, Jackson-Grusby L, Laird PW, Lei H, et al. Germ-line passage is required for establishment of methylation and expression patterns of imprinted but not of nonimprinted genes. Genes Dev. 1996 Apr 15; 10(8): 1008–20. 8608936.

69. Hadjantonakis AK, Gertsenstein M, Ikawa M, Okabe M, Nagy A. Generating green fluorescent mice by germline transmission of green fluorescent ES cells. Mech Dev. 1998 Aug; 76(1–2): 79–90. 9867352.

70. Kwan EM, Boraston AB, McLean BW, Kilburn DG, Warren RA. N-Glycosidase-carbohydrate-binding module fusion proteins as immobilized enzymes for protein deglycosylation. Protein Eng Des Sel. 2005 Oct; 18(10): 497–501. Epub 2005 Sep 9. 16155117.