C-mannosylation of human hyaluronidase 1: Possible roles for secretion and enzymatic activity

International Journal of Oncology

Volumn 45, Issue 1, 2014, Pages 344-350

  Goto, Yuki ^a   Niwa, Yuki ^a   Suzuki, Takehiro ^b   Dohmae, Naoshi ^b   Umezawa, Kazuo ^c   Simizu, Siro ^a  

^a KEIO UNIVERSITY   (Japan)

^b RIKEN   (Japan)

^c AICHI MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

C mannosylation; Glycosylation; Hyaluronidase; Mass spectrometry

Indexed keywords

GLUTAMIC ACID; HYALURONIC ACID; HYALURONIDASE; HYALURONIDASE 1; MANNOSE; TRYPTOPHAN; UNCLASSIFIED DRUG; CULTURE MEDIUM; HYALURONOGLUCOSAMINIDASE;

ARTICLE; C MANNOSYLATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR DOCKING; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN SECRETION; PROTEIN STRUCTURE; CHEMICAL STRUCTURE; CHEMISTRY; CULTURE MEDIUM; ENZYME ACTIVE SITE; GLYCOSYLATION; METABOLISM; PROTEIN PROCESSING; PROTEIN SECONDARY STRUCTURE; SECRETION (PROCESS); TUMOR CELL LINE;

CATALYTIC DOMAIN; CELL LINE, TUMOR; CULTURE MEDIA, CONDITIONED; GLYCOSYLATION; HUMANS; HYALURONIC ACID; HYALURONOGLUCOSAMINIDASE; MANNOSE; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY;

EID: 84902595137     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2014.2438     Document Type: Article

References (33)

1. Furmanek A and Hofsteenge J: Protein C-mannosylation: facts and questions. Acta Biochim Pol 47: 781-789, 2000.
2. Doucey MA, Hess D, Cacan R and Hofsteenge J: Protein C-mannosylation is enzyme-catalysed and uses dolichylphosphate-mannose as a precursor. Mol Biol Cell 9: 291-300, 1998.
3. Krieg J, Hartmann S, Vicentini A, Gläsner W, Hess D and Hofsteenge J: Recognition signal for C-mannosylation of Trp-7 in RNase 2 consists of sequence Trp-x-x-Trp. Mol Biol Cell 9: 301-309, 1998.
4. Julenius K: NetCGlyc 1.0: prediction of mammalian C-mannosylation sites. Glycobiology 17: 868-876, 2007.
5. Hofsteenge J, Müller DR, de Beer T, Löffler A, Richter WJ and Vliegenthart JF: New type of linkage between a carbohydrate and a protein: C-glycosylation of a specific tryptophan residue in human RNase Us. Biochemistry 33: 13524-13530, 1994.
6. Gonzalez de Peredo A, Klein D, Macek B, Hess D, Peter-Katalinic J and Hofsteenge J: C-mannosylation and o-fucosylation of thrombospondin type 1 repeats. Mol Cell Proteomics 1: 11-18, 2002.
7. Hofsteenge J, Huwiler KG, Macek B, Hess D, Lawler J, Mosher DF and Peter-Katalinic J: C-mannosylation and O-fucosylation of the thrombospondin type 1 module. J Biol Chem 276: 6485-6498, 2001.
8. Wang LW, Leonhard-Melief C, Haltiwanger RS and Apte SS: Post-translational modification of thrombospondin type-1 repeats in ADAMTS-like 1/punctin-1 by C-mannosylation of tryptophan. J Biol Chem 284: 30004-30015, 2009.
9. Hamming OJ, Kang L, Svensson A, Karlsen JL, Rahbek-Nielsen H, Paludan SR, Hjorth SA, Bondensgaard K and Hartmann R: Crystal structure of interleukin-21 receptor (IL-21R) bound to IL-21 reveals that sugar chain interacting with WSXWS motif is integral part of IL-21R. J Biol Chem 287: 9454-9460, 2012.
10. Buettner FF, Ashikov A, Tiemann B, Lehle L and Bakker H: C. elegans DPY-19 is a C-mannosyltransferase glycosylating thrombospondin repeats. Mol Cell 50: 295-302, 2013.
11. Ihara Y, Manabe S, Ikezaki M, Inai Y, Matsui I-SL, Ohta Y, Muroi E and Ito Y: C-mannosylated peptides derived from the thrombospondin type 1 repeat interact with Hsc70 to modulate its signaling in RAW264.7 cells. Glycobiology 20: 1298-1310, 2010.
12. Muroi E, Manabe S, Ikezaki M, Urata Y, Sato S, Kondo T, Ito Y and Ihara Y: C-mannosylated peptides derived from the thrombospondin type 1 repeat enhance lipopolysaccharide-induced signaling in macrophage-like RAW264.7 cells. Glycobiology 17: 1015-1028, 2007.
13. Overall CM and Lopez-Otin C: Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer 2: 657-672, 2002.
14. Simizu S, Ishida K, Wierzba MK and Osada H: Secretion of heparanase protein is regulated by glycosylation in human tumor cell lines. J Biol Chem 279: 2697-2703, 2004.
15. Simizu S and Niwa Y: Practical molecular targets for suppression of metastasis. For Immunopathol Dis Therap 4: 43-51, 2013.
16. Chao KL, Muthukumar L and Herzberg O: Structure of human hyaluronidase-1, a hyaluronan hydrolyzing enzyme involved in tumor growth and angiogenesis. Biochemistry 46: 6911-6920, 2007.
17. Tan JX, Wang XY, Su XL, Li HY, Shi Y, Wang L and Ren GS: Upregulation of HYAL1 expression in breast cancer promoted tumor cell proliferation, migration, invasion and angiogenesis. PLoS One 6: e22836, 2011.
18. Tan JX, Wang XY, Li HY, Su XL, Wang L, Ran L, Zheng K and Ren GS: HYAL1 overexpression is correlated with the malignant behavior of human breast cancer. Int J Cancer 128: 1303-1315, 2011.
19. Imundo L, Leduc CA, Guha S, Brown M, Perino G, Gushulak L, Triggs-Raine B and Chung WK: A complete deficiency of hyaluronoglucosaminidase 1 (HYAL1) presenting as familial juvenile idiopathic arthritis. J Inherit Metab Dis 34: 1013-1022, 2011.
20. Kuroda M, Funasaki S, Saitoh T, Sasazawa Y, Nishiyama S, Umezawa K and Simizu S: Determination of topological structure of ARL6ip1 in cells: identification of the essential binding region of ARL6ip1 for conophylline. FEBS Lett 587: 3656-3660, 2013.
21. Yasukagawa T, Niwa Y, Simizu S and Umezawa K: Suppression of cellular invasion by glybenclamide through inhibited secretion of platelet-derived growth factor in ovarian clear cell carcinoma ES-2 cells. FEBS Lett 586: 1504-1509, 2012.
22. Miyazaki I, Simizu S, Okumura H, Takagi S and Osada H: A small-molecule inhibitor shows that pirin regulates migration of melanoma cells. Nat Chem Biol 6: 667-673, 2010.
23. Simizu S, Umezawa K, Takada M, Arber N and Imoto M: Induction of hydrogen peroxide production and Bax expression by caspase-3(-like) proteases in tyrosine kinase inhibitorinduced apoptosis in human small cell lung carcinoma cells. Exp Cell Res 238: 197-203, 1998.
24. Simizu S, Suzuki T, Muroi M, Lai NS, Takagi S, Dohmae N and Osada H: Involvement of disulfide bond formation in the activation of heparanase. Cancer Res 67: 7841-7849, 2007.
25. Niwa Y, Suzuki T, Dohmae N, Umezawa K and Simizu S: Determination of cathepsin V activity and intracellular trafficking by N-glycosylation. FEBS Lett 586: 3601-3607, 2012.
26. Guntenhöner MW, Pogrel MA and Stern R: A substrate-gel assay for hyaluronidase activity. Matrix 12: 388-396, 1992.
27. Zhang L, Bharadwaj AG, Casper A, Barkley J, Barycki JJ and Simpson MA: Hyaluronidase activity of human Hyal1 requires active site acidic and tyrosine residues. J Biol Chem 284: 9433-9442, 2009.
28. Yamaguchi H, Kidachi Y, Kamiie K, Noshita T and Uetsu H: Structural insight into the ligand-receptor interaction between glycyrrhetinic acid (GA) and the high-mobility group protei B1 (HMGB1)-DNA complex. Bioinformation 23: 1147-1153, 2012.
29. Susana DL, Lídia MG, Teresa AFC, Henrique FC, Rui M and Rita CG: Structure based virtual screening for discovery of novel human neutrophil elastase inhibitors. Med Chem Comm 3: 1299-1304, 2012.
30. Wilkins MR, Gasteiger E, Gooley AA, Herbert BR, Molloy MP, Binz PA, Ou K, Sanchez JC, Bairoch A, Williams KL and Hochstrasser DF: High-throughput mass spectrometric discovery of protein post-translational modifications. J Mol Biol 289: 645-657, 1999.
31. Frost GI, Csóka AB, Wong T, Stern R and Csóka TB: Purification, cloning, and expression of human plasma hyaluronidase. Biochem Biophys Res Commun 236: 10-15, 1997.
32. Azuma M, Kabe Y, Kuramori C, Kodo M, Yamaguchi Y and Handa H: Adenine nucleotide translocator transports haem precursors into mitochondria. PLoS One 3: e3070, 2008.
33. Fukiage C, Nakajima E, Ma H, Azuma M and Shearer TR: Characterization and regulation of lens-specific calpain Lp82. J Biol Chem 277: 20678-20685, 2002.