N-glycosylation Does Not Affect the Catalytic Activity of Ricin A Chain but Stimulates Cytotoxicity by Promoting Its Transport Out of the Endoplasmic Reticulum

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Volumn 13, Issue 11, 2012, Pages 1508-1521

  Yan, Qing ^a   Li, Xiao Ping ^a   Tumer, Nilgun E ^a  

^a Rutgers University   (United States)

Author keywords

Endoplasmic reticulum dislocation; N glycosylation; Ribosome depurination; Ricin; Vacuole transport

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; RICIN A;

ARTICLE; CELL TRANSPORT; CELL VACUOLE; CYTOSOL; CYTOTOXICITY; ENDOPLASMIC RETICULUM; GLYCOSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBOSOME; SACCHAROMYCES CEREVISIAE; YEAST;

AMINO ACID MOTIFS; CATALYTIC DOMAIN; CYTOSOL; ENDOPLASMIC RETICULUM; GLYCOSYLATION; GREEN FLUORESCENT PROTEINS; POINT MUTATION; PROTEIN PRECURSORS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; RICIN; SACCHAROMYCES CEREVISIAE; VACUOLES;

EID: 84867229684     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2012.01404.x     Document Type: Article

References (45)

1. Endo Y, Tsurugi K. RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. J Biol Chem 1987;262:8128-8130.
2. Sandvig K, Grimmer S, Lauvrak SU, Torgersen ML, Skretting G, van Deurs B, Iversen TG. Pathways followed by ricin and Shiga toxin into cells. Histochem Cell Biol 2002;117:131-141.
3. Halling KC, Halling AC, Murray EE, Ladin BF, Houston LL, Weaver RF. Genomic cloning and characterization of a ricin gene from Ricinus communis. Nucleic Acids Res 1985;13:8019-8033.
4. Lappi DA, Kapmeyer W, Beglau JM, Kaplan NO. The disulfide bond connecting the chains of ricin. Proc Natl Acad Sci U S A 1978;75:1096-1100.
5. Lord JM. Precursors of ricin and Ricinus communis agglutinin. Glycosylation and processing during synthesis and intracellular transport. Eur J Biochem 1985;146:411-416.
6. Van Deurs B, Tonnessen TI, Petersen OW, Sandvig K, Olsnes S. Routing of internalized ricin and ricin conjugates to the Golgi complex. J Cell Biol 1986;102:37-47.
7. Wright HT, Robertus JD. The intersubunit disulfide bridge of ricin is essential for cytotoxicity. Arch Biochem Biophys 1987;256:280-284.
8. Bellisola G, Fracasso G, Ippoliti R, Menestrina G, Rosen A, Solda S, Udali S, Tomazzolli R, Tridente G, Colombatti M. Reductive activation of ricin and ricin A-chain immunotoxins by protein disulfide isomerase and thioredoxin reductase. Biochem Pharmacol 2004;67:1721-1731.
9. Spooner RA, Watson PD, Marsden CJ, Smith DC, Moore KA, Cook JP, Lord JM, Roberts LM. Protein disulphide-isomerase reduces ricin to its A and B chains in the endoplasmic reticulum. Biochem J 2004;383:285-293.
10. Wesche J, Rapak A, Olsnes S. Dependence of ricin toxicity on translocation of the toxin A-chain from the endoplasmic reticulum to the cytosol. J Biol Chem 1999;274:34443-34449.
11. Gillece P, Pilon M, Romisch K. The protein translocation channel mediates glycopeptide export across the endoplasmic reticulum membrane. Proc Natl Acad Sci U S A 2000;97:4609-4614.
12. Spooner RA, Lord JM. How ricin and Shiga toxin reach the cytosol of target cells: retrotranslocation from the endoplasmic reticulum. Curr Top Microbiol Immunol 2012;357:19-40.
13. Rapak A, Falnes PO, Olsnes S. Retrograde transport of mutant ricin to the endoplasmic reticulum with subsequent translocation to cytosol. Proc Natl Acad Sci U S A 1997;94:3783-3788.
14. Slominska-Wojewodzka M, Gregers TF, Walchli S, Sandvig K. EDEM is involved in retrotranslocation of ricin from the endoplasmic reticulum to the cytosol. Mol Biol Cell 2006;17:1664-1675.
15. Li S, Spooner RA, Allen SC, Guise CP, Ladds G, Schnoder T, Schmitt MJ, Lord JM, Roberts LM. Folding-competent and folding-defective forms of ricin A chain have different fates after retrotranslocation from the endoplasmic reticulum. Mol Biol Cell 2010;21:2543-2554.
16. Redmann V, Oresic K, Tortorella LL, Cook JP, Lord M, Tortorella D. Dislocation of ricin toxin A chains in human cells utilizes selective cellular factors. J Biol Chem 2011;286:21231-21238.
17. Hosomi A, Tanabe K, Hirayama H, Kim I, Rao H, Suzuki T. Identification of an Htm1 (EDEM)-dependent, Mns1-independent Endoplasmic Reticulum-associated Degradation (ERAD) pathway in Saccharomyces cerevisiae: application of a novel assay for glycoprotein ERAD. J Biol Chem 2010;285:24324-24334.
18. Rutenber E, Katzin BJ, Ernst S, Collins EJ, Mlsna D, Ready MP, Robertus JD. Crystallographic refinement of ricin to 2.5 Å. Proteins 1991;10:240-250.
19. Schlossman D, Withers D, Welsh P, Alexander A, Robertus J, Frankel A. Role of glutamic acid 177 of the ricin toxin A chain in enzymatic inactivation of ribosomes. Mol Cell Biol 1989;9:5012-5021.
20. Soler-Rodriguez AM, Uhr JW, Richardson J, Vitetta ES. The toxicity of chemically deglycosylated ricin A-chain in mice. Int J Immunopharmacol 1992;14:281-291.
21. Sehgal P, Kumar O, Kameswararao M, Ravindran J, Khan M, Sharma S, Vijayaraghavan R, Prasad GB. Differential toxicity profile of ricin isoforms correlates with their glycosylation levels. Toxicology 2011;282:56-67.
22. Parikh BA, Coetzer C, Tumer NE. Pokeweed antiviral protein regulates the stability of its own mRNA by a mechanism that requires depurination but can be separated from depurination of the α-sarcin/ricin loop of rRNA. J Biol Chem 2002;277:41428-41437.
23. Faulhammer F, Konrad G, Brankatschk B, Tahirovic S, Knodler A, Mayinger P. Cell growth-dependent coordination of lipid signaling and glycosylation is mediated by interactions between Sac1p and Dpm1p. J Cell Biol 2005;168:185-191.
24. Vida TA, Emr SD. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 1995;128:779-792.
25. Maley F, Trimble RB, Tarentino AL, Plummer TH Jr. Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal Biochem 1989;180:195-204.
26. +-ATPase. J Biol Chem 1992;267:447-454.
27. Pierce M, Kahn JN, Chiou J, Tumer NE. Development of a quantitative RT-PCR assay to examine the kinetics of ribosome depurination by ribosome inactivating proteins using Saccharomyces cerevisiae as a model. RNA 2011;17:201-210.
28. Jolliffe NA, Di Cola A, Marsden CJ, Lord JM, Ceriotti A, Frigerio L, Roberts LM. The N-terminal ricin propeptide influences the fate of ricin A-chain in tobacco protoplasts. J Biol Chem 2006;281:23377-23385.
29. Simpson JC, Lord JM, Roberts LM. Point mutations in the hydrophobic C-terminal region of ricin A chain indicate that Pro250 plays a key role in membrane translocation. Eur J Biochem 1995;232:458-463.
30. Li XP, Baricevic M, Saidasan H, Tumer NE. Ribosome depurination is not sufficient for ricin-mediated cell death in Saccharomyces cerevisiae. Infect Immun 2007;75:417-428.
31. Parikh BA, Tortora A, Li XP, Tumer NE. Ricin inhibits activation of the unfolded protein response by preventing splicing of the HAC1 mRNA. J Biol Chem 2008;283:6145-6153.
32. Mulholland J, Botstein D. Immunoelectron microscopy of aldehyde-fixed yeast cells. In: Guthrie C, Fink GR, editors. Methods in Enzymology, Volume 351. San Diego: Academic Press; 2002, pp. 50-81.
33. Lehrman MA. Oligosaccharide-based information in endoplasmic reticulum quality control and other biological systems. J Biol Chem 2001;276:8623-8626.
34. Helenius A. How N-linked oligosaccharides affect glycoprotein folding in the endoplasmic reticulum. Mol Biol Cell 1994;5:253-265.
35. Parodi AJ. Protein glucosylation and its role in protein folding. Annu Rev Biochem 2000;69:69-93.
36. Spiro RG. Glucose residues as key determinants in the biosynthesis and quality control of glycoproteins with N-linked oligosaccharides. J Biol Chem 2000;275:35657-35660.
37. Banerjee S, Vishwanath P, Cui J, Kelleher DJ, Gilmore R, Robbins PW, Samuelson J. The evolution of N-glycan-dependent endoplasmic reticulum quality control factors for glycoprotein folding and degradation. Proc Natl Acad Sci U S A 2007;104:11676-11681.
38. Sokolowska I, Walchli S, Wegrzyn G, Sandvig K, Slominska-Wojewodzka M. A single point mutation in ricin A-chain increases toxin degradation and inhibits EDEM1-dependent ER retrotranslocation. Biochem J 2011;436:371-385.
39. Winther JR, Stevens TH, Kielland-Brandt MC. Yeast carboxypeptidase Y requires glycosylation for efficient intracellular transport, but not for vacuolar sorting, in vivo stability, or activity. Eur J Biochem 1991;197:681-689.
40. Wilkins TA, Bednarek SY, Raikhel NV. Role of propeptide glycan in post-translational processing and transport of barley lectin to vacuoles in transgenic tobacco. Plant Cell 1990;2:301-313.
41. Parikh BA, Baykal U, Di R, Tumer NE. Evidence for retro-translocation of pokeweed antiviral protein from endoplasmic reticulum into cytosol and separation of its activity on ribosomes from its activity on capped RNA. Biochemistry 2005;44:2478-2490.
42. Baykal U, Tumer NE. The C-terminus of pokeweed antiviral protein has distinct roles in transport to the cytosol, ribosome depurination and cytotoxicity. Plant J 2007;49:995-1007.
43. Cabrera M, Ungermann C. Purification and in vitro analysis of yeast vacuoles. In: Klionsky DJ, editor. Methods in Enzymology, Volume 451. San Diego: Academic Press; 2008, pp. 177-196.
44. Chiou JC, Li XP, Remacha M, Ballesta JP, Tumer NE. Shiga toxin 1 is more dependent on the P proteins of the ribosomal stalk for depurination activity than Shiga toxin 2. Int J Biochem Cell Biol 2011;43:1792-1801.
45. Li XP, Chiou JC, Remacha M, Ballesta JP, Tumer NE. A two-step binding model proposed for the electrostatic interactions of ricin A chain with ribosomes. Biochemistry 2009;48:3853-3863.