Expression of heparan sulfate sulfotransferases in Kluyveromyces lactis and preparation of 3′-phosphoadenosine-5′-phosphosulfate

Glycobiology

Volumn 21, Issue 6, 2011, Pages 771-780

  Zhou, Xianxuan ^a   Chandarajoti, Kasemsiri ^a   Pham, Truong Quang ^a   Liu, Renpeng ^a   Liu, Jian ^a  

^a University of North Carolina   (United States)

Author keywords

heparan sulfate; heparin; K. lactis; PAPS; sulfotransferase

Indexed keywords

2 O SULFOTRANSFERASE; 3 O SULFOTRANSFERASE 1; 6 O SULFOTRANSFERASE 1; 6 O SULFOTRANSFERASE 3; ADENOSINE 3' PHOSPHATE 5' PHOSPHOSULFATE; ESTROGEN SULFOTRANSFERASE; FUNGAL PROTEIN; HEPARAN SULFATE; HEPARIN; POLYSACCHARIDE; SULFOTRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME SYNTHESIS; KLUYVEROMYCES LACTIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; THERMOSTABILITY; YEAST CELL;

CARBOHYDRATE CONFORMATION; GENE EXPRESSION; KLUYVEROMYCES; PHOSPHOADENOSINE PHOSPHOSULFATE; POLYSACCHARIDES; SULFOTRANSFERASES;

BACTERIA (MICROORGANISMS); KLUYVEROMYCES LACTIS; SUIDAE;

EID: 79956095975     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwr001     Document Type: Article

References (32)

1. Abdel-Banat BMA, Nonklang S, Hoshida H, Akada R. 2010. Random and targeted gene integrations through the control of non-homologous end joining in the yeast Kluyveromyces marxianus. Yeast. 27:29-39.
2. Aquino RS, Pereira MS, Vairo BC, Cinelli LP, Santos GR, Fonseca RJ, Mourao PA. 2010. Heparins from procine and bovine intestinal mucosa: Are they similar drugs? Thromb Haemost. 103:1005-1015.
3. Arepally G, Ortel TL. 2006. Heparin-induced thrombocytopenia. N Engl J Med. 355:809-817. (Pubitemid 44285586)
4. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 68:729-777. (Pubitemid 29449208)
5. Blom N, Sicheritz-Pontén T, Gupta R, Gammeltoft S, Brunak S. 2004. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics. 4:1633-1649. (Pubitemid 38738322)
6. Bonekamp FJ, Oosterom J. 1994. On the safety of Kluyveromyces lactis- a review. Appl Microbiol Biotechnol. 41:1-3.
7. Borgenstrom M, Jalkanen M, Salmivirta M. 2003. Sulfated derivatives of Escherichia coli K5 polysaccharides as modulators of fibroblast growth factor signaling. J Biol Chem. 278:49882-49889. (Pubitemid 37548823)
8. Burkart MD, Izumi M, Chapman E, Lin CH, Wong CH. 2000. Regeneration of PAPS for the enzymatic synthesis of sulfated oligosaccharides. J Org Chem. 65:5565-5574.
9. Chen J, Avci FY, Munoz EM, McDowell LM, Chen M, Pedersen LC, Zhang L, Linhardt RJ, Liu J. 2005. Enzymatic redesigning of biologically active heparan sulfate. J Biol Chem. 280:42817-42825. (Pubitemid 43049243)
10. Chen J, Jones CL, Liu J. 2007. Using an enzymatic combinatorial approach to identify anticoagulant heparan sulfate structures. Chem Biol. 14:986-993. (Pubitemid 47404901)
11. Colussi PA, Specht CA, Taron CH. 2005. Characterization of a nucleus-encoded chitinase from the yeast Kluyveromyces lactis. Appl Environ Microbiol. 71:2862-2869. (Pubitemid 40807187)
12. Copeland R, Balasubramaniam A, Tiwari V, Zhang F, Bridges A, Linhardt RJ, Shukla D, Liu J. 2008. Using a 3-O-sulfated heparin octasaccharide to inhibit the entry of herpes simplex virus type 1. Biochemistry (Mosc). 47:5774-5783. (Pubitemid 351747056)
13. Edavettal SC, Carrick K, Shah RR, Pedersen LC, Tropsha A, Pope RM, Liu J. 2004. A conformational change in heparan sulfate 3-O-sulfotransferase-1 is induced by binding to heparan sulfate. Biochemistry (Mosc). 43:4680-4688. (Pubitemid 38509088)
14. Esko JD, Selleck SB. 2002. Order out of chaos: Assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem. 71:435-471. (Pubitemid 34800227)
15. Flores MV, Cuellas A, Voget CE. 1999. The proteolytic system of the yeast Kluyveromyces lactis. Yeast. 15:1437-1448. (Pubitemid 29472156)
16. Habuchi H, Habuchi O, Kimata K. 1995. Purification and characterization of heparan sulfate 6-sulfotransferase from the culture medium of Chinese hamster ovary cells. J Biol Chem. 270:4172.
17. Hong F, Meinander NQ, Jonsson LJ. 2002. Fermentation strategies for improved heterologous expression of laccase in Pichia pastoris. Biotechnol Bioeng. 79:438-449. (Pubitemid 34847321)
18. Kakuta Y, Sueyoshi T, Negishi M, Pedersen LC. 1999. Crystal structure of the sulfotransferase domain of human heparan sulfate N-deacetylase/N- sulfotransferase 1. J Biol Chem. 274:10673-10676.
19. Klabunde J, Kleebank S, Piontek M, Hollenberg CP, Hellwig S, Degelmann A. 2007. Increase of calnexin gene dosage boosts the secretion of heterologous proteins by Hansenula polymorpha. FEMS Yeast Res. 7:1168-1180. (Pubitemid 47390292)
20. Kobayashi M, Habuchi H, Habuchi O, Saito M, Kimata K. 1996. Purification and characterization of heparan sulfate 2-sulfotransferase from cultured Chinese hamster ovary cells. J Biol Chem. 271:7645-7653. (Pubitemid 26107045)
21. Kuberan B, Lech MZ, Beeler DL, Wu ZL, Rosenberg RD. 2003. Enzymatic synthesis of antithrombin III-binding heparan sulfate pentasaccharide. Nat Biotechnol. 21:1343-1346. (Pubitemid 37356620)
22. Lindahl U, Li JP, Kusche-Gullberg M, Salmivirta M, Alaranta S, Veromaa T, Emeis J, Roberts I, Taylor C, Oreste P, et al. 2005. Generation of "neohe-parin" from E. coli K5 capsular polysaccharide. J Med Chem. 48:349-352. (Pubitemid 40139778)
23. Liu J, Shworak NW, Fritze LMS, Edelberg JM, Rosenberg RD. 1996. Purification of heparan sulfate D-glucosaminyl 3-O-sulfotransferase. J Biol Chem. 271:27072-27082. (Pubitemid 26359127)
24. Liu H, Zhang Z, Linhardt RJ. 2009. Lessons learned from the contamination of heparin. Nat Prod Rep. 26:313-321.
25. Macauley-Patrick S, Fazenda ML, McNeil B, Harvey LM. 2005. Heterologous protein production using the Pichia pastoris expression system. Yeast. 22:249-270. (Pubitemid 40528349)
26. MacRae IJ, Rose AB, Segel IH. 1998. Adenosine 5'-phosphosulfate kinase from Penicillium chrysogenum. J Biol Chem. 273:28583-28589.
27. Orellana A, Hirschberg CB, Wei Z, Swiedler SJ, Ishihara M. 1994. Molecular cloning and expression of a glycosaminoglycan N-acetylglucosaminyl N-deacetylase/N-sulfotransferase from a heparin producing cell line. J Biol Chem. 269:2270-2276.
28. Peterson S, Frick A, Liu J. 2009. Design of biologically active heparan sulfate and heparin using an enzyme-based approach. Nat Prod Rep. 26:610-627.
29. Petitou M, van Boeckel CAA. 2004. A synthetic antithrombin III binding pentasaccharide is now a drug! What comes next? Angew Chem Int Ed Engl. 43:3118-3133. (Pubitemid 39257600)
30. Saribas AS, Mobasseri A, Pristatsky P, Chen X, Barthelson R, Hakes D, Wang J. 2004. Production of N-sulfated polysaccharides using yeast-expressed N-deacetylase/N-sulfotransferase-1 (NDST-1). Glycobiology. 14:1217-1228. (Pubitemid 39585356)
31. Stanley P. 1992. Glycosylation engineering. Glycobiology. 2:99-107.
32. Van Ooyen AJJ, Dekker P, Huang M, Olsthoorn MMA, Jacobs DI, Colussi PA, Taron CH. 2006. Heterologous protein production in the yeast Kluyveromyces lactis. FEMS Yeast Res. 6:381-392.