Synthesis of Lipid-Linked Oligosaccharides (LLOs) and Their Phosphonate Analogues as Probes To Study Protein Glycosylation Enzymes

Abstract

Here we review chemical and chemoenzymatic methods for the synthesis of lipid-linked oligosaccharides (LLOs) and their phosphonate analogues, which serve as substrates and inhibitors to investigate the structure and mechanism of protein N-glycosylation enzymes. We emphasize how to overcome the challenges pertaining to the instability and difficult physicochemical properties of this class of compounds.

1 Introduction

2 LLO Syntheses

2.1 Glycosyl Phosphate Syntheses

2.2 Glycosyl Phosphonates

2.3 Lipid Elongation

2.4 Lipid Phosphates

2.5 Coupling Reaction Strategies

3 Chemoenzymatic Synthesis of Elongated LLOs

4 Biological Properties of Synthetic LLOs

5 Conclusion

Key words

carbohydrates - polyprenols - diphosphates - phosphonates - glycosides - lipid-linked oligosaccharides

• References

• 1 Siberstein S. Gilmore R. FASEB J. 1996; 10: 849
• 2 Knauer R. Lehle L. J. Biol. Chem. 1999; 274: 17249
• 3 Kelleher DJ. Gilmore R. Glycobiology 2006; 16: 47
• 4 Larkin A. Imperiali B. Biochemistry 2011; 50: 4411
• 5 Dempski RE. Imperiali B. Curr. Opin. Chem. Biol. 2002; 6: 844
• 6 Yan A. Lennarz WJ. J. Biol. Chem. 2005; 280: 3121
• 7 Schwarz F. Aebi M. Curr. Opin. Struct. Biol. 2011; 21: 576
• 8 Shrimal S. Cherepanova NA. Gilmore R. Semin. Cell Dev. Biol. 2015; 41: 71
• 9 Welply JK. Shenbagamurthi P. Lennarz WJ. Naider F. J Biol Chem. 1983; 258: 11856
• 10 Gerber S. Lizak C. Michaud G. Bucher M. Darbre T. Aebi M. Reymond JL. Locher KP. J. Biol. Chem. 2013; 288: 8849
• 11 Imperiali B. O’Connor SE. Curr. Opin. Chem. Biol. 1999; 3: 643
• 12 Patterson MC. Semin. Pediatr. Neurol. 2005; 12: 144
• 13 Lizak C. Gerber S. Numao S. Aebi M. Locher KP. Nature 2011; 474: 350
• 14 Sharon N. Glycobiology 2007; 17: 1150
• 15 Wild R. Kowal J. Eyring J. Ngwa EM. Aebi M. Locher KP. Science 2018; DOI: in press; 10.1126/science.aar5140.
• 16 Bai L. Wang T. Zhao G. Kovach A. Li H. Nature 2018; 555: 328
• 17 Kowarik M. Numao S. Feldman MF. Schulz BL. Callewaert N. Kiermaier E. Catrein I. Aebi M. Science 2006; 314: 1148
• 18 Zufferey R. Knauer R. Burda P. Stagljar I. te Heesen S. Lehle L. Aebi M. EMBO J. 1995; 14: 4949
• 19 Ramírez AS. Boilevin J. Biswas R. Gan BH. Janser D. Aebi M. Darbre T. Reymond JL. Locher KP. Glycobiology 2017; 27: 525
• 20 Liu F. Vijayakrishnan B. Faridmoayer A. Taylor TA. Parsons TB. Bernardes GJ. L. Kowarik M. Davis BG. J. Am. Chem. Soc. 2014; 136: 566
• 21 Sharma CB. Lehle L. Tanner W. Eur. J. Biochem. 1981; 116: 101
• 22 Breuer W. Bause E. Eur. J. Biochem. 1995; 228: 689
• 23 Fang X. Gibbs BS. Coward JK. Bioorg. Med. Chem. Lett. 1995; 5: 2701
• 24 Xu Z. Bioorg. Med. Chem. Lett. 2015; 25: 3777
• 25 Warren CD. Konami Y. Jeanloz RW. Carbohydr. Res. 1973; 30: 257
• 26 Wedgwoodt JF. Warren CD. Jeanloz RW. Stromingert JL. Proc. Natl. Acad. Sci. U. S. A. 1974; 71: 5022
• 27 Khorlin AY. Zurabyan SE. Antonenko TS. Tetrahedron Lett. 1970; 55: 4803
• 28 Matta KL. Bahl OP. Carbohydr. Res. 1972; 21: 460
• 29 Srivastava VK. Carbohydr. Res. 1982; 103: 286
• 30 Lemieux RU. Morgan AR. Can. J. Chem. 1965; 43: 2214
• 31 Warren CD. Milat M.-L. Augé C. Jeanloz RW. Carbohydr. Res. 1984; 126: 61
• 32 Lemieux RU. Driguez H. J. Am. Chem. Soc. 1975; 97: 4063
• 33 Nashed MA. Slife CW. Kiso M. Anderson L. Carbohydr. Res. 1980; 82: 237
• 34 Napiórkowska M. Boilevin J. Sovdat T. Darbre T. Reymond J.-L. Aebi M. Locher KP. Nat. Struct. Mol. Biol. 2017; 24: 1100
• 35 Graczyk PP. Mikolajczyk M. Anomeric Effect: Origin and ­Consequences. In Topics in Stereochemistry. Vol. 21. Eliel EL. Wilen SH. John Wiley & Sons; New York: 1994: 159
• 36 Freitas MP. Org. Biomol. Chem. 2013; 11: 2885
• 37 Bauerfeldt GF. Cardozo TM. Pereira MS. da Silva CO. Org. Biomol. Chem. 2013; 11: 299
• 38 Nakabayashi S. Warren CD. Jeanloz RW. Carbohydr. Res. 1986; 150: 7
• 39 Lee J. Coward JK. J. Org. Chem. 1992; 57: 4126
• 40 Warren CD. Herscovics A. Jeanloz RW. Carbohydr. Res. 1978; 61: 181
• 41 Nishimura S.-I. Kuzuhara H. Takiguchi Y. Shimahara K. ­Carbohydr. Res. 1989; 194: 223
• 42 Excoffier G. Gagnaire D. Utille JP. Carbohydr. Res. 1975; 39: 368
• 43 Itoh T. Takamura H. Watanabe K. Araki Y. Ishido Y. Carbohydr. Res. 1986; 156: 241
• 44 Nudelman A. Herzig J. Gottlieb HE. Keinan E. Sterling J. Carbohydr. Res. 1987; 162: 145
• 45 Watanabe K. Itoh K. Araki Y. Ishido Y. Carbohydr. Res. 1986; 154: 165
• 46 Chang R. Yeager AR. Finney NS. Org. Biomol. Chem. 2003; 1: 39
• 47 Flitsch SL. Pinches HL. Taylor JP. Turner NJ. J. Chem. Soc., Perkin Trans. 1 1992; 2087
• 48 Sabesan S. Neira S. Carbohydr. Res. 1992; 223: 169
• 49 Nikolaev AV. Botvinko IV. Ross AJ. Carbohydr. Res. 2007; 342: 297
• 50 Arlt M. Hindsgaul O. J. Org. Chem. 1995; 60: 14
• 51 Zhang Q. Liu HW. J. Am. Chem. Soc. 2000; 122: 9065
• 52 Hardré R. Khaled A. Willemetz A. Dupré T. Moore S. Gravier-Pelletier C. Le Merrer Y. Bioorg. Med. Chem. Lett. 2007; 17: 152
• 53 Crich D. Dudkin V. Org. Lett. 2000; 2: 3941
• 54 Veeneman GH. Broxterman HJ. G. van der Marel GA. van Boom JH. Tetrahedron Lett. 1991; 32: 6175
• 55 Schmidt RR. Wegmann B. Jung K. Liebigs Ann. Chem. 1991; 121
• 56 Hoch M. Heinz E. Schmidt RR. Carbohydr. Res. 1989; 191: 21
• 57 Tsai YH. Götze S. Azzouz N. Hahm HS. Seeberger PH. Varon Silva D. Angew. Chem. Int. Ed. 2011; 50: 9961
• 58 Dohi H. Périon R. Durka M. Bosco M. Roué Y. Moreau F. Grizot S. Ducruix A. Escaich S. Vincent SP. Chem. Eur. J. 2008; 14: 9530
• 59 Dinev Z. Wardak AZ. Brownlee RT. C. Williams SJ. Carbohydr. Res. 2006; 341: 1743
• 60 Cudic P. Behenna DC. Yu MK. Kruger RG. Szewczuk LM. McCafferty DG. Bioorg. Med. Chem. Lett. 2001; 11: 3107
• 61 Sim MM. Kondo H. Wong CH. J. Am. Chem. Soc. 1993; 115: 2260
• 62 Kakinuma H. Yuasa H. Hashimoto H. Carbohydr. Res. 1998; 312: 103
• 63 Wolf S. Zismann T. Lunau N. Meier C. Chem. Eur. J. 2009; 15: 7656
• 64 Bosco M. Massarweh A. Iatmanen-Harbi S. Bouhss A. Chantret I. Busca P. Moore SE. H. Gravier-Pelletier C. Eur. J. Med. Chem. 2017; 125: 952
• 65 Kondo H. Ichikawa Y. Wong CH. J. Am. Chem. Soc. 1992; 114: 8748
• 66 Cheon HS. Lian Y. Kishi Y. Org. Lett. 2007; 9: 3323
• 67 Crich D. Sun S. Tetrahedron 1998; 54: 8321
• 68 van Summeren RP. Moody DB. Feringa BL. Minnaard AJ. J. Am. Chem. Soc. 2006; 128: 4546
• 69 Li T. Tikad A. Pan W. Vincent SP. Org. Lett. 2014; 16: 5628
• 70 Seeman JI. Chem. Rev. 1983; 83: 83
• 71 Schäfer A. Thiem J. J. Org. Chem. 2000; 65: 24
• 72 Gordon RD. Sivarajah P. Satkunarajah M. Ma D. Tarling CA. Vizitiu D. Withers SG. Rini JM. J. Mol. Biol. 2006; 360: 67
• 73 Hajduch J. Nam G. Kim EJ. Fröhlich R. Hanover JA. Kirk KL. Carbohydr. Res. 2008; 343: 189
• 74 Pougny JR. Nassr MA. M. Sinaÿ P. J. Chem. Soc., Chem. Commun. 1981; 375
• 75 Nicotra F. Ronchetti F. Russo G. J. Chem. Soc., Chem. Commun. 1982; 470
• 76 Henbest HB. Nicholls B. J. Chem. Soc. 1959; 227
• 77 Arbuzov BA. Pure Appl. Chem. 1964; 9: 307
• 78 Qiao L. Vederad C. J. Org. Chem. 1993; 58: 3480
• 79 Garneau S. Qiao L. Chen L. Walker S. Vederas JC. Bioorg. Med. Chem. 2004; 12: 6473
• 80 Casero F. Cipolla L. Lay L. Nicotra F. Panza L. Russo G. J. Org. Chem. 1996; 61: 3428
• 81 Chang R. Vo TT. Finney NS. Carbohydr. Res. 2006; 341: 1998
• 82 Cui J. Horton D. Carbohydr. Res. 1998; 309: 319
• 83 Bouvet VR. Ben RN. J. Org. Chem. 2006; 71: 3619
• 84 Giese B. Angew. Chem. Int. Ed. 1989; 28: 969
• 85 Dupuis J. Giese B. Rüegge D. Fischer H. Korth H.-G. Sustmann R. Angew. Chem. Int. Ed. 1984; 23: 896
• 86 Korth H. Sustmann R. Dupuis J. Giese B. J. Chem. Soc., Perkin Trans. 2 1986; 1453
• 87 Giese B. Pure Appl. Chem. 1988; 60: 1655
• 88 McGarvey GJ. Schmidtmann FW. Benedum TE. Kizer DE. Tetrahedron Lett. 2003; 44: 3775
• 89 Patnam R. Juárez-Ruiz JM. Roy R. Org. Lett. 2006; 8: 2691
• 90 Lin CK. Chen KT. Hu CM. Yun WY. Cheng WC. Chem. Eur. J. 2015; 21: 7511
• 91 Dolan SC. MacMillan J. J. Chem. Soc., Chem. Commun. 1985; 1588
• 92 Barton DH. R. McCombie SW. J. Chem. Soc., Perkin Trans. 1 1975; No. 16, 1574
• 93 Babič A. Gobec S. Gravier-Pelletier C. Le Merrer Y. Pečar S. Tetrahedron 2008; 64: 9093
• 94 Lu W. Navidpour L. Taylor SD. Carbohydr. Res. 2005; 340: 1213
• 95 Debenham SD. Toone EJ. Tetrahedron: Asymmetry 2000; 11: 385
• 96 DeNinno MP. Etienne JB. Duplantier KC. Tetrahedron Lett. 1995; 36: 669
• 97 Barroca N. Jacquinet JC. Carbohydr. Res. 2002; 337: 673
• 98 Dullenkopf W. Castro-Palomino JC. Manzoni L. Schmidt RR. Carbohydr. Res. 1996; 296: 135
• 99 Kamkhachorn T. Parameswar AR. Demchenko AV. Org. Lett. 2010; 12: 3078
• 100 Kobertz WR. Bertozzi CR. Bednarski MD. Tetrahedron Lett. 1992; 33: 737
• 101 Dondoni A. Marra A. Pasti C. Tetrahedron: Asymmetry 2000; 11: 305
• 102 Stolz F. Reiner M. Blume A. Reutter W. Schmidt RR. J. Org. Chem. 2004; 69: 665
• 103 Borodkin VS. Ferguson MA. J. Nikolaev AV. Tetrahedron Lett. 2001; 42: 5305
• 104 Veleti SK. Lindenberger JJ. Ronning DR. Sucheck SJ. Bioorg. Med. Chem. 2014; 22: 1404
• 105 Chernyak AY. Levinsky AB. Dmitriev BA. Kochetkov AK. Carbohydr. Res. 1984; 128: 269
• 106 Dorfmueller HC. Borodkin VS. Blair DE. Pathak S. Navratilova I. Van Aalten DM. F. Amino Acids 2011; 40: 781
• 107 Knapp S. Myers DS. J. Org. Chem. 2001; 66: 3636
• 108 Knapp S. Gonzalez S. Myers DS. Eckman LL. Bewley CA. Org. Lett. 2002; 4: 4337
• 109 Knapp S. Ajayi K. Tetrahedron Lett. 2007; 48: 1945
• 110 Searle GD. Curr. Opin. Struct. Biol. 1995; 5: 605
• 111 Lillelund VH. Jensen HH. Liang X. Bols M. Chem. Rev. 2002; 102: 515
• 112 Sinnott ML. Chem. Rev. 1990; 90: 1171
• 113 Rye CS. Withers SG. Curr. Opin. Chem. Biol. 2000; 4: 573
• 114 Bols M. Acc. Chem. Res. 1998; 31: 1
• 115 Bouix C. Bisseret P. Eustache J. Tetrahedron Lett. 1998; 39: 825
• 116 Bosco M. Bisseret P. Bouix-Peter C. Eustache J. Tetrahedron Lett. 2001; 42: 7949
• 117 Godin G. Compain P. Masson G. Martin OR. J. Org. Chem. 2002; 67: 6960
• 118 La Ferla B. Bugada P. Nicotra F. J. Carbohydr. Chem. 2006; 25: 151
• 119 Blériot Y. Auberger N. Jagadeesh Y. Gauthier C. Prencipe G. Tran AT. Marrot J. Désiré J. Yamamoto A. Kato A. Sollogoub M. Org. Lett. 2014; 16: 5512
• 120 Hsu C. Schelwies M. Enck S. Huang L. Huang S. Chang Y. Cheng TR. Cheng W. Wong C. J. Org. Chem. 2014; 79: 8629
• 121 Hoffmann M. Burkhart F. Hessler G. Kessler H. Helv. Chim. Acta 1996; 79: 1519
• 122 Chojnacki T. Jankowski W. Mankowski T. Sasak W. Anal. Biochem. 1975; 69: 114
• 123 Ibata K. Mizuno M. Takigawa T. Tanaka Y. Biochem. J. 1983; 213: 305
• 124 Eggens I. Chojnacki T. Kenne L. Dallner G. Biochim. Biophys. Acta 1983; 751: 355
• 125 Bizri M. Bouhours J.-F. Bizri Y. Got R. Comp. Biochem. Physiol., Part B: Comp. Biochem. 1986; 84: 565
• 126 Rip JW. Carroll KK. Anal. Biochem. 1987; 160: 350
• 127 Crick DC. Carroll KK. Lipids 1987; 22: 1045
• 128 Sato K. Miyamoto O. Inoue S. Furusawa F. Matsuhashi Y. Chem. Lett. 1983; 725
• 129 Sato K. Seiichi I. Onishi A. Uchida N. Minowa N. J. Chem. Soc., Perkin Trans. 1 1981; 761
• 130 Hesek D. Lee M. Zajicek J. Fisher JF. Mobashery S. J. Am. Chem. Soc. 2012; 134: 13881
• 131 Jaenicke L. Siegmund HU. Biol. Chem. Hoppe-Seyler 1986; 367: 787
• 132 Inoue S. Kaneko T. Takahashi Y. Miyamoto O. Sato K. J. Chem. Soc., Chem. Commun. 1987; 1036
• 133 Jaenicke L. Siegmund H. Chem. Phys. Lipids 1989; 51: 159
• 134 Grassi D. Lippuner V. Aebi M. Brunner J. Vasella A. J. Am. Chem. Soc. 1997; 119: 10992
• 135 Wu B. Woodward R. Wen L. Wang X. Zhao G. Wang PG. Eur. J. Org. Chem. 2013; 8162
• 136 Amslinger S. Kis K. Hecht S. Adam P. Rohdich F. Arigoni D. Bacher A. Eisenreich W. J. Org. Chem. 2002; 67: 4590
• 137 Kocovsky P. Ahmed G. Srogl J. Malkov AV. Steele J. J. Org. Chem. 1999; 64: 2765
• 138 Takaya H. Ohta T. Sayo N. Kumobayashi H. Akutagawa S. Inoue S. Kasahara I. Noyori R. J. Am. Chem. Soc. 1987; 109: 1596
• 139 Imperiali B. Zimmerman JW. Tetrahedron Lett. 1988; 29: 5343
• 140 Chang YF. Liu CY. Guo CW. Wang YC. Fang JM. Cheng WC. J. Org. Chem. 2008; 73: 7197
• 141 Khwaja TA. Reese CB. Stewart JC. M. J. Chem. Soc. 1970; 2092
• 142 Warren CD. Jeanloz RW. Biochemistry 1972; 11: 2565
• 143 Michelson AM. Biochim. Biophys. Acta, Spec. Sect. Nucleic Acids Relat. Subj. 1964; 91: 1
• 144 Imperiali B. Zimmerman JW. Tetrahedron Lett. 1990; 31: 6485
• 145 Wedgwood JF. Strominger JL. Warren CD. J. Biol. Chem. 1974; 249: 6316
• 146 Popjak G. Cornforth JW. Cornforth RH. Ryhage R. Goodman DS. J. Biol. Chem. 1962; 237: 56
• 147 Rupar CA. Carroll KK. Chem. Phys. Lipids 1976; 17: 193
• 148 Brody EP. Gutsche CD. Tetrahedron 1977; 33: 723
• 149 Julia M. Mestdagh H. Rolando C. Tetrahedron 1986; 42: 3841
• 150 Danilov LL. Druzhinina TN. Kalinchuk NA. Maltsev SD. Shibaev VN. Chem. Phys. Lipids 1989; 51: 191
• 151 Cramer F. Rittersdorf W. Tetrahedron 1967; 23: 3015
• 152 Danilov LL. Chojnacki T. FEBS Lett. 1981; 131: 310
• 153 Warren CD. Jeanloz RW. Carbohydr. Res. 1974; 37: 252
• 154 Khorana HG. Todd AR. J. Chem. Soc. 1953; 2257
• 155 Hoard DE. Ott DG. J. Am. Chem. Soc. 1965; 87: 1785
• 156 Bernardes GJ. L. Kikkeri R. Maglinao M. Laurino P. Collot M. Hong SY. Lepenies B. Seeberger PH. Org. Biomol. Chem. 2010; 8: 4987
• 157 Perez C. Gerber S. Boilevin J. Bucher M. Darbre T. Aebi M. Reymond J.-L. Locher KP. Nature 2015; 524: 433
• 158 Zhang J. Angala SK. Pramanik PK. Li K. Crick DC. Liav A. Jozwiak A. Swiezewska E. Jackson M. Chatterjee D. ACS Chem. Biol. 2011; 6: 819
• 159 Lee YJ. Ishiwata A. Ito Y. Tetrahedron 2009; 65: 6310
• 160 Schoenhofen IC. McNally DJ. Vinogradov E. Whitfield D. Young NM. Dick S. Wakarchuk WW. Brisson JR. Logan SM. J. Biol. Chem. 2006; 281: 723
• 161 Olivier NB. Chen MM. Behr JR. Imperial B. Biochemistry 2006; 45: 13659
• 162 Glover KJ. Weerapana E. Chen MM. Imperiali B. Biochemistry 2006; 45: 5343
• 163 Weerapana E. Glover KJ. Chen MM. Imperiali B. J. Am. Chem. Soc. 2005; 127: 13766
• 164 Troutman JM. Imperiali B. Biochemistry 2009; 48: 2807
• 165 Matta KL. Johnson EA. Barlow JJ. Carbohydr. Res. 1973; 26: 215
• 166 Glover KJ. Weerapana E. Imperiali B. Proc. Natl. Acad. Sci. U. S. A. 2005; 102: 14255
• 167 Woodward R. Yi W. Li L. Zhao G. Eguchi H. Sridhar PR. Guo H. Song JK. Motari E. Cai L. Kelleher P. Liu X. Han W. Zhang W. Ding Y. Li M. Wang PG. Nat. Chem. Biol. 2010; 6: 418
• 168 Nishimoto M. Kitaoka M. Appl. Environ. Microbiol. 2007; 73: 6444
• 169 Cai L. Guan W. Kitaoka M. Shen J. Xia C. Chen W. Wang PG. Chem. Commun. 2009; No. 20, 2944
• 170 Cai L. Guan W. Wang W. Zhao W. Kitaoka M. Shen J. O’Neil C. Wang PG. Bioorg. Med. Chem. Lett. 2009; 19: 5433
• 171 Kukuruzinska MA. Apekin V. Lamkin MS. Hiltz A. Rodriguez A. Lin CC. Paz MA. Oppenheim FG. Biochem. Biophys. Res. Commun. 1994; 198: 1248
• 172 Gao XD. Moriyama S. Miura N. Dean N. Nishimura SI. J. Biol. Chem. 2008; 283: 32534
• 173 Lu J. Takahashi T. Ohoka A. Nakajima KI. Hashimoto R. Miura N. Tachikawa H. Gao XD. Glycobiology 2012; 22: 504
• 174 Gao XD. Nishikawa A. Dean N. Glycobiology 2004; 14: 559
• 175 Couto JR. Huffaker TC. Robbins PW. J. Biol. Chem. 1984; 259: 378
• 176 Yamazaki H. Shiraishi N. Takeuchi K. Ohnishi Y. Horinouchi S. Gene 1998; 221: 179
• 177 Kämpf M. Absmanner B. Schwarz M. Lehle L. J. Biol. Chem. 2009; 284: 11900
• 178 Cipollo JF. Trimble RB. Chi JH. Yan Q. Dean N. J. Biol. Chem. 2001; 276: 21828
• 179 O’Reilly MK. Zhang G. Imperiali B. Biochemistry 2006; 45: 9593
• 180 Absmanner B. Schmeiser V. Kämpf M. Lehle L. Biochem. J. 2010; 426: 205
• 181 Burda P. Aebi M. Biochim. Biophys. Acta, Gen. Subj. 1999; 1426: 239
• 182 Tai VW. Reilly MK. O. Imperiali B. Bioorg. Med. Chem. 2001; 9: 1133
• 183 Watt GM. Revers L. Webberley MC. Wilson IB. H. Flitsch SL. Carbohydr. Res. 1997; 305: 533
• 184 Li ST. Wang N. Xu S. Yin J. Nakanishi H. Dean N. Gao XD. Biochim. Biophys. Acta, Gen. Subj. 2017; 1861: 2934
• 185 Rexer TF. T. Schildbach A. Klapproth J. Schierhorn A. Mahour R. Pietzsch M. Rapp E. Reichl U. Biotechnol. Bioeng. 2018; 115: 192
• 186 Li S.-T. Wang N. Xu X.-X. Fujita M. Nakanishi H. Kitajima T. Dean N. Gao X.-D. FASEB J. 2018; 32 DOI: in press; 10.1096/fj.201701267R.
• 187 Wang N. Li S. Lu T. Nakanishi H. Gao X. Chin. Chem. Lett. 2017; 29: 35
• 188 Ramírez AS. Boilevin J. Lin C.-W. Gan BH. Janser D. Aebi M. Darbre T. Reymond J.-L. Locher KP. Glycobiology 2017; 27: 726
• 189 Roy SK. Chiba Y. Jigami Y. Biotechnol. Bioprocess Eng. 2000; 5: 219
• 190 Sethuraman N. Stadheim TA. Curr. Opin. Biotechnol. 2006; 17: 341
• 191 Chiba Y. Akeboshi H. Biol. Pharm. Bull. 2009; 32: 786
• 192 Dalziel M. Crispin M. Scanlan CN. Zitzmann N. Dwek RA. Science 2014; 343: 38
• 193 Lalonde ME. Durocher Y. J. Biotechnol. 2017; 251: 128
• 194 Dagan R. Poolman J. Siegrist CA. Vaccine 2010; 28: 5513
• 195 Borrow R. Dagan R. Zepp F. Hallander H. Poolman J. Expert Rev. Vaccines 2011; 10: 1621
• 196 Vella M. Pace D. Expert Opin. Biol. Ther. 2014; 15: 529
• 197 Chen MM. Weerapana E. Ciepichal E. Stupak J. Reid CW. Swiezewska E. Imperiali B. Biochemistry 2007; 46: 14342
• 198 Lizak C. Gerber S. Michaud G. Schubert M. Fan Y.-Y. Bucher M. Darbre T. Aebi M. Reymond J.-L. Locher KP. Nat. Commun. 2013; 4: 2627
• 199 Naegeli A. Michaud G. Schubert M. Lin CW. Lizak C. Darbre T. Reymond JL. Aebi M. J. Biol. Chem. 2014; 289: 24521
• 200 Lizak C. Gerber S. Zinne D. Michaud G. Schubert M. Chen F. Bucher M. Darbre T. Zenobi R. Reymond JL. Locher KP. J. Biol. Chem. 2014; 289: 735
• 201 Ramírez AS. Boilevin J. Mehdipour AR. Hummer G. Darbre T. Reymond J.-L. Locher KP. Nat. Commun. 2018; 9: 445