Linked production of pyroglutamate-modified proteins via self-cleavage of fusion tags with TEV protease and autonomous N-terminal cyclization with glutaminyl cyclase in Vivo

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Shih, Yan Ping ^a   Chou, Chi Chi ^a   Chen, Yi Ling ^a   Huang, Kai Fa ^a   Wang, Andrew H J ^a  

^a INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; GLUTAMINYL CYCLASE; LYASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEINASE; PYROGLUTAMIC ACID; TOBACCO ETCH VIRUS PROTEASE; UNCLASSIFIED DRUG; AMINOACYLTRANSFERASE; GLUTAMINYL-PEPTIDE CYCLOTRANSFERASE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN; TEV PROTEASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CATALYSIS; CONTROLLED STUDY; CYCLIZATION; GENE EXPRESSION; GENE INSERTION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOLECULAR CLONING; POLYMERASE CHAIN REACTION; PROTEIN CLEAVAGE; PROTEIN TARGETING; CELL MOTION; GENE VECTOR; LIQUID CHROMATOGRAPHY; METABOLISM; NANOTECHNOLOGY; PROTEIN DEGRADATION; TANDEM MASS SPECTROMETRY;

AMINOACYLTRANSFERASES; CELL MOVEMENT; CHROMATOGRAPHY, LIQUID; CYCLIZATION; ENDOPEPTIDASES; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HUMANS; MONOCYTE CHEMOATTRACTANT PROTEINS; NANOTECHNOLOGY; PROTEOLYSIS; PYRROLIDONECARBOXYLIC ACID; RECOMBINANT FUSION PROTEINS; TANDEM MASS SPECTROMETRY;

EID: 84899646534     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094812     Document Type: Article

References (57)

1. Van Coillie E, Proost P, Van Aelst I, Struyf S, Polfliet M, et al. (1998) Functional comparison of two human monocyte chemotactic protein-2 isoforms, role of the amino-terminal pyroglutamic acid and processing by CD26/dipeptidyl peptidase IV. Biochemistry 37: 12672-12680. (Pubitemid 28427552)
2. Goren HJ, Bauce LG, Vale W (1977) Forces and structural limitations of binding of thyrotrophin-releasing factor to the thyrotrophin-releasing receptor: the pyroglutamic acid moiety. Mol Pharmacol 13: 606-614 (Pubitemid 8148877)
3. Morty RE, Bulau P, Pellé R, Wilk S, Abe K (2006) Pyroglutamyl peptidase type I from Trypanosoma brucei: a new virulence factor from African trypanosomes that de-blocks regulatory peptides in the plasma of infected hosts. Biochem J 394: 635-645.
4. Kitabgi P, De Nadai F, Rovère C, Bidard JN (1992) Biosynthesis, maturation, release, and degradation of neurotensin and neuromedin N. Ann N Y Acad Sci 668: 30-42. (Pubitemid 23025844)
5. Smith AM, Watson SA (2000) Review article: gastrin and colorectal cancer. Aliment Pharmacol Ther 14: 1231-1247.
6. Holst J, Ørskov C (1994) in Gut Peptides: Biochemistry and Physiology, eds Walsh J., Dockray G. (Raven Press, New York), pp. 305-340.
7. Sozzani S, Locati M, Allavena P, Van Damme J, Mantovani A (1996) Chemokines: a superfamily of chemotactic cytokines. Int J Clin Lab Res 26: 69-82. (Pubitemid 26310342)
8. Dick LW Jr, Kim C, Qiu D, Cheng KC (2007) Determination of the origin of the N-terminal pyro-glutamate variation in monoclonal antibodies using model peptides. Biotechnol Bioeng 97: 544-553. (Pubitemid 46848069)
9. Liao YD, Huang HC, Leu YJ, Wei CW, Tang PC, et al. (2000) Purification and cloning of cytotoxic ribonucleases from Rana catesbeiana (bullfrog). Nucleic Acids Res 28: 4097-4104.
10. Schilling S, Lauber T, Schaupp M, Manhart S, Scheel E, et al. (2006) On the seeding and oligomerization of pGlu-amyloid peptides (in vitro). Biochemistry 45: 12393-12399. (Pubitemid 44583682)
11. Fischer WH, Spiess J (1987) Identification of a mammalian glutaminyl cyclase converting glutaminyl into pyroglutamyl peptides. Proc Natl Acad Sci USA 84: 3628-3632. (Pubitemid 17088334)
12. Busby WH Jr, Quackenbush GE, Humm J, Youngblood WW, Kizer JS (1987) An enzyme(s) that converts glutaminyl-peptides into pyroglutamyl-peptides. Presence in pituitary, brain, adrenal medulla, and lymphocytes. J Biol Chem 262: 8532-8536.
13. Oberg KA, Ruysschaert JM, Azarkan M, Smolders N, Zerhouni S, et al. (1998) Papaya glutamine cyclase, a plant enzyme highly resistant to proteolysis, adopts an all-b conformation. Eur J Biochem 258: 214-222. (Pubitemid 28538328)
14. Schilling S, Wasternack C, Demuth HU (2008) Glutaminyl cyclases from animals and plants: a case of functionally convergent protein evolution. Biol Chem 389: 983-991.
15. Wintjens R, Belrhali H, Clantin B, Azarkan M, Bompard C, et al. (2006) Crystal structure of papaya glutaminyl cyclase, an archetype for plant and bacterial glutaminyl cyclases. J Mol Biol 357: 457-470. (Pubitemid 43290747)
16. Guevara T, Mallorqú-Fernández N, Garcá-Castellanos R, Garcá-Piqué S, Ebert Petersen G, et al. (2006) Papaya glutamine cyclotransferase shows a singular five-fold b-propeller architecture that suggests a novel reaction mechanism. Biol Chem 387: 1479-1486. (Pubitemid 44691430)
17. Huang WL, Wang YR, Ko TP, Chia CY, Huang KF, et al. (2010) Crystal structure and functional analysis of the glutaminyl cyclase from Xanthomonas campestris. J Mol Biol 401: 374-88.
18. Böckers TM, Kreutz MR, Pohl T (1995) Glutaminyl-cyclase expression in the bovine/porcine hypothalamus and pituitary. J Neuroendocrinol 7: 445-453.
19. Sykes PA, Watson SJ, Temple JS, Bateman RC Jr. (1999) Evidence for tissuespecific forms of glutaminyl cyclase. FEBS Lett 455: 159-161. (Pubitemid 29322801)
20. Huang KF, Liu YL, Cheng WJ, Ko TP, Wang AH (2005) Crystal structures of human glutaminyl cyclase, an enzyme responsible for protein N-terminal pyroglutamate formation. Proc Natl Acad Sci USA 102: 13117-13122. (Pubitemid 41324988)
21. Cynis H, Rahfeld JU, Stephan A, Kehlen A, Koch B, et al. (2008) Isolation of an isoenzyme of human glutaminyl cyclase: retention in the Golgi complex suggests involvement in the protein maturation machinery. J Mol Biol 379: 966-980.
22. Huang KF, Liaw SS, Huang WL, Chia CY, Lo YC, et al. (2011) Structures of human Golgi-resident glutaminyl cyclase and its complexes with inhibitors reveal a large loop movement upon inhibitor binding. J Biol Chem 286: 12439-12449.
23. Flanagan T, Taylor L, Poulter L, Viveros OH, Diliberto EJ Jr. (1990) A novel 1745-dalton pyroglutamyl peptide derived from chromogranin B is in the bovine adrenomedullary chromaffin vesicle. Cell Mol Neurobiol 10: 507-523.
24. Schilling S, Manhart S, Hoffmann T, Ludwig HH, Wasternack C, et al. (2003) Substrate specificity of glutaminyl cyclases from plants and animals. Biol Chem 384: 1583-1592. (Pubitemid 38054881)
25. Chen YL, Huang KF, Kuo WC, Lo YC, Lee YM, et al. (2012) Inhibition of glutaminyl cyclase attenuates cell migration modulated by monocyte chemoattractant proteins. Biochem J 442: 403-412.
26. Welker E, Hathaway L, Xu G, Narayan M, Pradeep L, et al. (2007) Oxidative folding and N-terminal cyclization of onconase. Biochemistry 46: 5485-5493. (Pubitemid 46717272)
27. Shih YP, Wu HC, Hu SM, Wang TF, Wang AH (2005) Self-cleavage of fusion protein in vivo using TEV protease to yield native protein. Protein Science 14: 936-941. (Pubitemid 40389363)
28. Dougherty WG, Cary SM, Parks TD (1989) Molecular genetic analysis of a plant virus polyprotein cleavage site: a model. Virology 171: 356-364.
29. Kapust RB, Tözsér J, Copeland TD, Waugh DS (2002) The P1' specificity of tobacco etch virus protease. Biochem Biophys Res Commun 294: 949-955. (Pubitemid 34687141)
30. Phan J, Zdanov A, Evdokimov AG, Tropea JE, Peters HK 3rd, et al. (2002) Structural basis for the substrate specificity of tobacco etch virus protease. J Biol Chem 277: 50564-50572. (Pubitemid 36042215)
31. Kapust RB, Waugh DS (2000) Controlled intracellular processing of fusion proteins by TEV protease. Protein Expr Purif 19: 312-318. (Pubitemid 30446312)
32. Oppenheim J, Fujiwara H (1996) The role of cytokines in cancer. Cytokine Growth Factor Rev 7: 279-288. (Pubitemid 27200312)
33. Kuhlmann MT, Klocke R, Nikol S (2007) Therapeutic angiogenesis for peripheral artery disease: cytokine therapy. Vasa 36: 253-260. (Pubitemid 350260419)
34. Ardelt W, Shogen K, Darzynkiewicz Z (2008) Onconase and amphinase, the antitumor ribonucleases from Rana pipiens oocytes. Curr Pharm Biotechnol 9: 215-225. (Pubitemid 352024698)
35. Ardelt W, Ardelt B, Darzynkiewicz Z (2009) Ribonucleases as potential modalities in anticancer therapy. Eur J Pharmacol 625: 181-189.
36. Zeng G (1998) Sticky-end PCR: New method for subcloning. Biotechniques 25: 206-208. (Pubitemid 28371406)
37. Shih YP, Kung WM, Chen JC, Yeh CH, Wang AH, et al. (2002) Highthroughput screening of soluble recombinant proteins. Protein Science 11: 1714-1719. (Pubitemid 34663551)
38. Wang TF, Wang AH (2004) High-throughput screening of soluble recombinant proteins. In Purifying proteins for proteomics: A laboratory manual (ed. R.J. Simpson), pp. 111-119. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Kapust RB, Tözsér J, Fox JD, Anderson DE, Cherry S, et al. (2001) Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency. Protein Eng 14: 993-1000. (Pubitemid 34137240)
40. Mosimann SC, Ardelt W, James MN (1994) Refined 1.7 A X-ray crystallographic structure of P-30 protein, an amphibian ribonuclease with anti-tumor activity. J Mol Biol 236: 1141-1153.
41. Chang CF, Chen C, Chen YC, Hom K, Huang RF, et al. (1998) The solution structure of a cytotoxic ribonuclease from the oocytes of Rana catesbeiana (bullfrog). J Mol Biol 283: 231-244. (Pubitemid 28466652)
42. Blaszczyk J, Coillie EV, Proost P, Damme JV, Opdenakker G, et al. (2000) Complete crystal structure of monocyte chemotactic protein-2, a CC chemokine that interacts with multiple receptors. Biochemistry 39: 14075-14081.
43. Awadé AC, Cleuziat P, Gonzalès T, Robert-Baudouy J (1994) Pyrrolidone carboxyl peptidase (Pcp): an enzyme that removes pyroglutamic acid (pGlu) from pGlu-peptides and pGlu-proteins. Proteins 20: 34-51. (Pubitemid 24308148)
44. Cynis H, Hoffmann T, Friedrich D, Kehlen A, Gans K, et al. (2011) The isoenzyme of glutaminyl cyclase is an important regulator of monocyte infiltration under inflammatory conditions. EMBO Mol Med 3: 545-558.
45. Schilling S, Zeitschel U, Hoffmann T, Heiser U, Francke M, et al. (2008) Glutaminyl cyclase inhibition attenuates pyroglutamate Ab and Alzheimer's disease-like pathology. Nat Med 14: 1106-1111.
46. Nussbaum JM, Schilling S, Cynis H, Silva A, Swanson E, et al. (2012) Prion-like behaviour and tau-dependent cytotoxicity of pyroglutamylated amyloid-b. Nature 485: 651-655.
47. Becker A, Kohlmann S, Alexandru A, Jagla W, Canneva F, et al. (2013) Glutaminyl cyclase-mediated toxicity of pyroglutamate-b amyloid induces striatal neurodegeneration. BMC Neurosci 14: 108.
48. Ezura Y, Kajita M, Ishida R, Yoshida S, Yoshida H, et al. (2004) Association of multiple nucleotide variations in the pituitary glutaminyl cyclase gene (QPCT) with low radial BMD in adult women. J Bone Miner Res 19: 1296-1301. (Pubitemid 41094371)
49. Huang QY, Kung AW (2007) The association of common polymorphisms in the QPCT gene with bone mineral density in the Chinese population. J Hum Genet 52: 757-762. (Pubitemid 47389624)
50. Cynis H, Kehlen A, Haegele M, Hoffmann T, Heiser U, et al. (2013) Inhibition of Glutaminyl Cyclases alleviates CCL2-mediated inflammation of non-alcoholic fatty liver disease in mice. Int J Exp Pathol 94: 217-725.
51. Iwasaki H, Emi M, Ezura Y, Ishida R, Kajita M, et al. (2003) Association of a Trp16Ser variation in the gonadotropin releasing hormone signal peptide with bone mineral density, revealed by SNP-dependent PCR typing. Bone 32: 185-190. (Pubitemid 36299147)
52. Pavlakis N, Vogelzang NJ (2006) Ranpirnase-an antitumour ribonuclease: its potential role in malignant mesothelioma. Expert Opin Biol Ther 6: 391-399.
53. Lou YC, Huang YC, Pan YR, Chen C, Liao YD (2006) Roles of N-terminal pyroglutamate in maintaining structural integrity and pKa values of catalytic histidine residues in bullfrog ribonuclease 3. J Mol Biol 355: 409-421. (Pubitemid 41785746)
54. Liao YD, Wang SC, Leu YJ, Wang CF, Chang ST, et al. (2003) The structural integrity exerted by N-terminal pyroglutamate is crucial for the cytotoxicity of frog ribonuclease from Rana pipiens. Nucleic Acids Res 31: 5247-5255.
55. Wang H, Piatkov KI, Brower CS, Varshavsky A (2009) Glutamine-specific Nterminal amidase, a component of the N-end rule pathway. Mol Cell 34: 686-695.
56. Ingrosso D, Fowler AV, Bleibaum J, Clarke S (1989) Specificity of endoproteinase Asp-N (Pseudomonas fragi): cleavage at glutamyl residues in two proteins. Biochem Biophys Res Commun 162: 1528-1534. (Pubitemid 19214757)
57. Lee J, Feldman AR, Delmas B, Paetzel M (2007) Crystal structure of the VP4 protease from infectious pancreatic necrosis virus reveals the acyl-enzyme complex for an intermolecular self-cleavage reaction. J Biol Chem 282: 24928-24937. (Pubitemid 47347508)