Large propeptides of fungal β-N-acetylhexosaminidases are novel enzyme regulators that must be intracellularly processed to control activity, dimerization, and secretion into the extracellular environment

Biochemistry

Volumn 46, Issue 10, 2007, Pages 2719-2734

  Plíhal, Ondřej ^a   Sklenář, Jan ^a   Hofbauerová, Kateřina ^a,b   Novák, Petr ^a   Man, Petr ^a   Pompach, Petr ^a   Kavan, Daniel ^a,b   Ryšlavá, Helena ^b   Weignerová, Lenka ^a   Charvátová Pišvejcová, Andrea ^a   Křen, Vladimír ^a   Bezouška, Karel ^a,b  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

DIMERIZATION; ENZYME KINETICS; GROWTH KINETICS; METABOLISM; PEPTIDES; REACTION KINETICS;

BINARY CHITINOLYTIC SYSTEMS; ENDOPLASMIC RETICULUM; ENZYME PRECURSOR; HYPHENATION;

FUNGI;

BETA N ACETYLHEXOSAMINIDASE; PEPTIDASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CATALYSIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIMERIZATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME RELEASE; ENZYME SUBUNIT; FUNGUS; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FOLDING; REGULATORY MECHANISM;

ACETYLGLUCOSAMINE; AMINO ACID SEQUENCE; BETA-N-ACETYLHEXOSAMINIDASE; BIOLOGICAL TRANSPORT; CATALYSIS; DIMERIZATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME PRECURSORS; ENZYME STABILITY; FUNGI; FURIN; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID; THIAZOLES; TRANSCRIPTION, GENETIC;

FUNGI;

EID: 33947254889     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061828m     Document Type: Article

References (42)

1. Weignerová, L., Vavrušková, P., Piš vejcová, A., Thiem, J., and Křen, V. (2003) Fungal β-N-acetylhexosaminidases with high β-N- acetylgalactosaminidase activity and their use for synthesis of β-GalNAc-containing oligosaccharides, Carbohydr. Res. 338, 1003-1008.
2. Korneluk, R. G., Mahuran, D. J., Noete, K., Klavins, M. H., O'Dowd, B. F., Tropak, M., Willard, H. F., Anderson, M. J., Lowden, J. A., and Gravel, R. A. (1986) Isolation of sDNA coding for the α-subunit of human β-hexosaminidase. Extensive homology between the α- and β-subunits and studies on Tay-Sachs disease, J. Biol. Chem. 261, 8407-8413.
3. Proia, R. L. (1988) Gene encoding the human β-hexosaminidase chain: extensive homology of intron placement in the α- and β-chain genes, Proc. Natl. Acad. Sci. U.S.A. 85, 1883-1887.
4. Tews, I., Perrakis, A., Oppenheim A., Dauter, Z., Wilson, K. S., and Vorgias, C. E. (1996) Bacterial chitobiase structure provides insight into catalytic mechanism and the basis of Tay-Sachs disease, Nat. Struct. Biol. 3, 638-648.
5. Huňková, Z., Křen, V., Śč igelová, M., Weignerová, L., Scheel, O., and Thiem, J. (1996) Induction of β-N-acetylhexosaminidases in Aspergillus oryzae, Biotechnol. Lett. 18, 725-730.
6. Huňková, Z., Kubátová, A., Weignerová, L., and Křen, V. (1999) Induction of extracellular glycosidases in filamentous fungi and their potential use in chemotaxonomy, Czech. Mycol. 51, 71-87.
7. Reyes, F., Calatayud, J., Vazquez, M. J., and Martinez, J. (1989) β-N-Acetylglucosaminidase from Aspergillus nidulans which degrades chitin oligomers during autolysis, FEMS Microbiol. Lett. 53, 83-87.
8. Gooday, G. W., Zhu, W.-Y., and O'Donell, R. W. (1992) What are the roles of chitinases in the growing fungus? FEMS Microbiol. Lett. 100, 387-392.
9. Peterbauer, C. K., Brunner, K., Mach, R. L., and Kubicek, C. P. (2002) Identification of the N-acetyl-D-glucosamine-inducible element in the promoter of the Trichoderma atroviride nag1 gene encoding N-acetyl-glucosaminidase, Mol. Genet. Genomics 267, 162-167.
10. Plíhal, O., Sklenář, J., Kmoníč ková, J., Man, P., Pompach, P., Havlíček, V., Křen, V., and Bezouška, K. (2004) N-Glycosylated catalytic unit meets O-glycosylated propeptide: complex protein architecture in a fungal hexosaminidase, Biochem. Soc. Trans. 32, 764-765.
11. Hušáková, L., Herkommerová-Rajnochová, E., Semeňuk, T., Kuzma, M., Rauvolfová, J., Př ikrylová, V., Ettrich, R., Plíhal, O., Bezouška, K., and Křen, V. (2003) Enzymatic discrimination of 2-acetamido-2-deoxy-D- mannopyranose-containing disaccharides using β-N-acetylhexosa-minidases, Adv. Synth. Catal. 345, 735-742.
12. Angliker, H., Wikstrom, P., Shaw, E., Brenner, C., and Fuller, R. S. (1993) The synthesis of inhibitors for processing proteinases and their action on the Kex-2 proteinase of yeast. Biochem. J. 293, 75-81.
13. Altschul, S. F., and Lipman, D. J. (1990) Protein database searches for multiple alignments. Proc. Natl. Acad. Sci. U.S.A. 87, 5509-5513.
14. Harlow, E., and Lane, D. (1988) Antibodies: A Laboratory Manual, 2nd ed., pp 23-56, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
15. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
16. Bezouška, K., Sklenář, J., Novák, P., Halada, P., Havlíček, V., Kraus, M., Tichá, M., and Jonáková, V. (1999) Determination of the complete covalent structure of the major glycoform of DQH sperm surface protein, a novel trypsin-resistant boar seminal plasma O-glycoprotein related to pB1 protein, Protein Sci. 8, 1551-1556.
17. Knapp, S., Vocadlo, D., Gao, Z., Kirk, B., Lou, J., and Withers, S. G. (1996) NAG-thiazoline, an N-acetyl-β-hexosaminidase inhibitor that implicates acetamido participation, J. Am. Chem. Soc. 118, 6804-6805.
18. Jalving, R., van de Vondervoort, P. J. I., Visser, J., and Schaap, P. J. (2000) Characterization of the kexin-like maturase of Aspergillus niger, Appl. Environ. Microbiol. 66, 363-368.
19. Li, Y. T., and Li, S. C. (1980) α-Mannosidase, β-N- acetylhexosaminidase and β-galactosidase from jack bean meal, Methods Enzymol. 90, 702-713.
20. Brumer, H., Sims, P. F. G., and Sinnott, M. L. (1999) Lignocellulose degradation by Phanerochaete chrysosporium: purification and characterization of the main α-galactosidase. Biochem. J. 339, 43-63.
21. Schagger, H. and Von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form, Anal. Biochem. 199, 223-231.
22. Machida, M., Asai, K., Sano, M., Tanaka, T., Kumagai, T., Terai, G., Kusumoto, K., Arima, T., Akita, O., Kashiwagi, Y., Abe, K., Gomi, K., Horiuchi, H., Kitamoto, K., Kobayashi, T., Takeuchi, M., Denning, D. W., Galagan, J. E., Nierman, W. C., Yu, J., Archer, D. B., Bennett, J. W., Bhatnagar, D., Cleveland, T. E., Fedorova, N. D., Gotoh, O., Horikawa, H., Hosoyama, A., Ichinomiya, M., Igarashi, R., Iwashita, K., Juvvadi, P. R., Kato, M., Kato, Y., Kin, T., Kokubun, A., Maeda, H., Maeyama, N., Maruyama, J., Nagasaki, H., Nakajima, T., Oda, K., Okada, K., Paulsen, I., Sakamoto, K., Sawano, T., Takahashi, M., Takase, K., Terabayashi, Y., Wortman, J. R., Yamada, O., Yamagata, Y., Anazawa, H., Hata, Y., Koide, Y., Komori, T., Koyama, Y., Minetoki, T., Suharnan, S., Tanaka, A., Isono, K., Kuhara, S., Ogasawara, N., and Kikuchi, H. (2005) Genome sequencing and analysis of Aspergillus oryzae, Nature 438, 1157-1161.
23. Diez, B., Rodriguez-Saiz, M., de la Fuente, J. L., Moreno, A. M., and Barredo, J. L. (2005) The nagA gene of Penicillium chrysogenum encoding β-N-acetylglucosaminidase, FEMS Microbiol. Lett. 242, 257-264.
24. Sagherian, C., Thorner, P., and Mahuran, D. (1994) The propeptide of the pro/b/polypeptide chain of human β-hexosaminidase is necessary for proper protein folding and exit from the endoplasmic reticulum, Biochem. Biophys. Res. Commun. 204, 135-141.
25. Rhodes, C. J., Brennan, S. O., and Hutton, J. C. (1989) Proalbumin to albumin conversion by a proinsulin processing endopeptidase of insulin secretory granules, J. Biol. Chem. 264, 14240-14245.
26. Redding, K., Holcomb, C., and Fuller, R. S. (1991) Immunolocalization of Kex2 protease identifies a putative late Golgi compartment in the yeast Saccharomyces cerevisiae, J. Cell Biol. 113, 527-538.
27. Cooper, A., and Bussey, H. (1989) Characterization of the yeast KEXI gene product: a carboxypeptidase involved in processing secreted precursor proteins, Mol. Cell. Biol. 9, 2706-2714.
28. Davey, J., Davis, K., Imai, Y., Yamamoto, M., and Matthews, G. (1994) Isolation and characterization of krp, a dibasic endopeptidase required for cell viability in the fission yeast Schizosaccharomyces pombe, EMBO J. 13, 5910-5921.
29. Cain, B. M., Vishnuvardhan, D., Wang, W., Foulon, T., Cadel, S., Cohen, P., and Beinfeld, M. C. (2002) Production, purification and characterization of recombinant prohormone convertase 5 from baculovirus-infected insect cells, Protein Expression Purif. 24, 227-233.
30. Dal Degan, F., Child, R., Svendsen, I., and Ulvskov, P. (2001) The cleavable N-terminal domain of plant endopolygalacturonases from clade B may be involved in a regulated secretion mechanism, J. Biol. Chem. 276, 35297-35304.
31. Shinde, U., and Inouye, M. (2000) Intramolecular cliuperones: polypeptide extensions that modulate protein folding. Semin. Cell Dev. Biol 11, 35-44.
32. Siezen, R. J., and Leunissen, J. A. M. (1997) Subtilases: the superfamily of subtilisin-like proteases, Protein Sci. 6, 501-523.
33. Kjeldsen, T. (2000) Yeast secretory expression of insulin precursors, Appl. Microbiol. Biotechnol. 54, 277-286.
34. Jalving, R., van de Vondervoort, P. J. I., Visser, J., and Schaap, P. J. (2000) Characterization of the kexin-like maturase of Aspergillus niger, Appl. Environ. Microbiol. 66, 363-368.
35. Gagnon-Arsenault, I., Tremblay, J., and Bourbonnais, Y. (2006) Fungal yapsins and cell wall: a unique family of aspartic peptidases for a distinctive cellular function, FEMS Yeast Res. 6, 966-978.
36. Lehner, P. J., and Cresswell, P. (2004) Recent developments in MHC-class-1-mediated antigen presentation, Curr. Opin. Immunol. 16, 82-89.
37. Wubbolts, R., and Neefjes, J. (1999) Intracellular transport and peptide loading of MHC class II molecules: regulation by chaperones and motors, Immunol. Rev. 172, 189-208.
38. Cresswell, P., Bangia, N., Dick, T., and Diedrich, G. (1999) The nature of the MHC class I peptide loading complex, Immunol. Rev. 172, 21-28.
39. Sadasivan, B., Lehner, P. J., Ortmann, B., Spies, T., and Cresswell, P. (1996) Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP, Immunity 5, 103-114.
40. Hughes, E. A., and Cresswell, P. (1998) The thiol oxidoreductase Erp57 is a component of the MHC class I peptide-loading complex, Curr. Biol. 8, 709-712.
41. Jensen, P. E., Weber, D. A., Thayer, W. P., Westerman, L. E., and Dao, C. T. (1999) Peptide exchange in MHC molecules, Immunol. Rev. 172, 229-238.
42. Princiotta, M. F., Finzi, D., Qian, B. S., Gibbs, J., Schuchmann, S., Buttgereit, F., Bennink, J. R., and Yewdell, J. W. (2003) Quantitating protein synthesis, degradation, and endogenous antigen processing, Immunity 18, 343-354.