A novel core fucose-specific lectin from the mushroom Pholiota squarrosa

Journal of Biological Chemistry

Volumn 287, Issue 41, 2012, Pages 33973-33982

  Kobayashi, Yuka ^a   Tateno, Hiroaki ^b   Dohra, Hideo ^c   Moriwaki, Kenta ^d   Miyoshi, Eiji ^d   Hirabayashi, Jun ^b   Kawagishi, Hirokazu ^c  

^a J Oil Mills Inc   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c SHIZUOKA UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL FUNCTIONS; CANCER BIOMARKERS; COLON CANCER; DIFFERENTIAL EXPRESSIONS; FETOPROTEIN; FRONTAL AFFINITY CHROMATOGRAPHIES; FUCOSYLATION; GLYCANS; HEPATOCELLULAR CARCINOMA; INCUBATION TIME; ION-EXCHANGE CHROMATOGRAPHY; ISOELECTRIC FOCUSING; MALDI-TOF MASS SPECTROMETRY; N-GLYCANS; N-TERMINALS; SDS-PAGE;

AFFINITY CHROMATOGRAPHY; AMINO ACIDS; BIOLOGICAL SYSTEMS; BIOMARKERS; DISEASES; ELECTROPHORESIS; LIVING SYSTEMS STUDIES; MASS SPECTROMETRY; PURIFICATION; TISSUE;

OLIGOSACCHARIDES;

AGAROSE; FUCOSE; GLYCAN; LECTIN; OLIGOSACCHARIDE; THYROGLOBULIN; TUMOR MARKER;

ADULT; AFFINITY CHROMATOGRAPHY; AGED; AMINO TERMINAL SEQUENCE; ANION EXCHANGE CHROMATOGRAPHY; ARTICLE; CANCER STAGING; CANCER TISSUE; COLON CANCER; CONTROLLED STUDY; FEMALE; FUCOSYLATION; HUMAN; HUMAN TISSUE; ISOELECTRIC FOCUSING; MAJOR CLINICAL STUDY; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR WEIGHT; MUSHROOM; NONHUMAN; PH; PHOLIOTA SQUARROSA; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STABILITY; SEQUENCE ANALYSIS; TEMPERATURE SENSITIVITY; TISSUE MICROARRAY;

AMINO ACID SEQUENCE; ANTIGENS, NEOPLASM; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; FUCOSE; FUNGAL PROTEINS; HUMANS; LECTINS; LIVER NEOPLASMS; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; PHOLIOTA; PROTEIN BINDING; PROTEIN STABILITY;

EID: 84867243012     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.327692     Document Type: Article

References (51)

1. Miyoshi, E., Moriwaki, K., and Nakagawa, T. (2008) Biological function of fucosylation in cancer biology. J. Biochem. 143, 725-729 (Pubitemid 351918934)
2. Uozumi N, Yanagidani S, Miyoshi E, Ihara Y, Sakuma T, Gao CX, Teshima T, Fujii S, Shiba T, and Taniguchi, N. (1996) Purification and cDNA cloning of porcine brain GDP-L-Fuc:N-acetyl-β-D-glucosaminide α1→ 6fucosyltransferase. J. Biol. Chem. 271, 27810-27817 (Pubitemid 26367356)
3. Tateno, H., Nakamura-Tsuruta, S., and Hirabayashi, J. (2009) Comparative analysis of core-fucose-binding lectins from Lens culinaris and Pisum sativum using frontal affinity chromatography. Glycobiology 19, 527-536
4. Howard, I. K. (1971) Studies on a phytohemagglutinin from the lentil. II. Multiple forms of Lens culinaris hemagglutinin. J. Biol. Chem. 246, 1590-1595
5. Foriers, A., Lebrun, E., Van Rapenbusch, R., de Neve, R., and Strosberg, A. D. (1981) The structure of the lentil (Lens culinaris) lectin. Amino acid sequence determination and prediction of the secondary structure. J. Biol. Chem. 256, 5550-5560
6. Aoyagi, Y. (1995) Carbohydrate-based measurements on α-fetoprotein in the early diagnosis of hepatocellular carcinoma. Glycoconj. J. 12, 194-199
7. Ichikawa, E., Kuriyama, S., Yuji, J., Masaki, T., Uchida, N., Nishioka, M., and Taketa, K. (2006) Further resolution of α-fetoprotein glycoforms by two-dimensional isoelectric focusing and lectin affinity electrophoresis. Electrophoresis 27, 3480-3487 (Pubitemid 44430729)
8. Taketa, K. (1990) α-Fetoprotein. Reevaluation in hepatology. Hepatology 12, 1420-1432
9. Debray, H., Decout, D., Strecker, G., Spik, G., and Montreuil, J. (1981) Specificity of twelve lectins toward oligosaccharides and glycopeptides related to N-glycosylproteins. Eur. J. Biochem. 117, 41-55
10. Amano, J., Osanai, M., Orita, T., Sugahara, D., and Osumi, K. (2009) Structural determination by negative-ion MALDI-QIT-TOF MSn after pyrene derivatization of variously fucosylated oligosaccharides with branched decaose cores from human milk. Glycobiology 19, 601-614
11. Harada, H., Kamei, M., Tokumoto, Y., Yui, S., Koyama, F., Kochibe, N., Endo, T., and Kobata, A. (1987) Systematic fractionation of oligosaccharides of human immunoglobulin G by serial affinity chromatography on immobilized lectin columns. Anal. Biochem. 164, 374-381 (Pubitemid 17129675)
12. Matsumura, K., Higashida, K., Hata, Y., Kominami, J., Nakamura-Tsuruta, S., and Hirabayashi, J. (2009) Comparative analysis of oligosaccharide specificities of fucose-specific lectins from Aspergillus oryzae and Aleuria aurantia using frontal affinity chromatography. Anal. Biochem. 386, 217-221
13. Yamashita, K., Kochibe, N., Ohkura, T., Ueda, I., and Kobata, A. (1985) Fractionation of L-fucose-containing oligosaccharides on immobilized Aleuria aurantia lectin. J. Biol. Chem. 260, 4688-4693 (Pubitemid 15034604)
14. Matsumoto, I., Uehara, Y., Jimbo, A., and Seno, N. (1983) Immunochemical and spectral studies on Vicia faba agglutinin. J. Biochem. 93, 763-769
15. Jordinson, M., El-Hariry, I., Calnan, D., Calam, J., and Pignatelli, M. (1999) Vicia faba agglutinin, the lectin present in broad beans, stimulates differentiation of undifferentiated colon cancer cells. Gut 44, 709-714 (Pubitemid 29195921)
16. Allen, A. K., Desai, N. N., and Neuberger, A. (1976) Purification of the glycoprotein lectin from the broad bean (Vicia faba) and a comparison of its properties with lectins of similar specificity. Biochem. J. 155, 127-135
17. Matsumura, K., Higashida, K., Ishida, H., Hata, Y., Yamamoto, K., Shigeta, M., Mizuno-Horikawa, Y., Wang, X., Miyoshi, E., Gu, J., and Taniguchi, N. (2007) Carbohydrate binding specificity of a fucose-specific lectin from Aspergillus oryzae. A novel probe for core fucose. J. Biol. Chem. 282, 15700-15708 (Pubitemid 47093286)
18. Mun, J. Y., Lee, K. J., Kim, Y. J., Kwon, O., Kim, S. J., Lee, S. G., Park, W. S., Heo, W. D., and Oh, D. B. (2012) Development of fluorescent probes for the detection of fucosylated N-glycans using an Aspergillus oryzae lectin. Appl. Microbiol. Biotechnol. 93, 251-260
19. Matsumoto, H., Shinzaki, S., Narisada, M., Kawamoto, S., Kuwamoto, K., Moriwaki, K., Kanke, F., Satomura, S., Kumada, T., and Miyoshi, E. (2010) Clinical application of a lectin antibody ELISA to measure fucosylated haptoglobin in sera of patients with pancreatic cancer. Clin. Chem. Lab. Med. 48, 505-512
20. Kawagishi, H. (1995) Mushroom lectins. Food Rev. Int. 11, 63-68
21. Kobayashi, Y., Ishizaki, T., and Kawagishi, H. (2004) Screening for lectins in wild and cultivated mushrooms from Japan and their sugar binding specificities. Int. J. Med. Mushr. 6, 113-125
22. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
23. Kawagishi, H., Yamawaki, M., Isobe, S., Usui, T., Kimura, A., and Chiba, S. (1994) Two lectins from the marine sponge Halichondria okadai. An N-acetyl-sugar-specific lectin (HOL-I) and an N-acetyllactosamine-specific lectin (HOL-II). J. Biol. Chem. 269, 1375-1379
24. Kawagishi, H., and Mizuno, T. (1988) Purification and properties of a β-galactosyl-specific lectin from the fruiting bodies of ischnoderma resinosus. FEBS Lett. 227, 99-102
25. Kobayashi, Y., Kobayashi, K., Umehara, K., Dohra, H., Murata, T., Usui, T., and Kawagishi, H. (2004) Purification, characterization, and sugar binding specificity of an N-glycolylneuraminic acid-specific lectin from the mushroom Chlorophyllum molybdites. J. Biol. Chem. 279, 53048-53055 (Pubitemid 40051804)
26. Horibe M, Kobayashi Y, Dohra H, Morita T, Murata T, Usui T, Nakamura-Tsuruta S, Kamei M, Hirabayashi J, Matsuura M, Yamada M, Saikawa Y, Hashimoto K, Nakata M, and Kawagishi, H. (2010) Toxic isolectins from the mushroom Boletus venenatus. Phytochemistry 71, 648-657
27. Hirabayashi, J., Arata, Y., and Kasai, K. (2000) Reinforcement of frontal affinity chromatography for effective analysis of lectin-oligosaccharide interactions. J. Chromatogr. A. 890, 261-271 (Pubitemid 30621566)
28. Tateno, H., Nakamura-Tsuruta, S., and Hirabayashi, J. (2007) Frontal affinity chromatography. Sugar-protein interactions. Nat. Protoc. 2, 2529-2537
29. Nakamura-Tsuruta, S., Uchiyama, N., and Hirabayashi, J. (2006) Highthroughput analysis of lectin-oligosaccharide interactions by automated frontal affinity chromatography. Methods Enzymol. 415, 311-325 (Pubitemid 44751105)
30. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
31. Lundy, F. T., and Wisdom, G. B. (1999) An antibody-lectin sandwich assay for quantifying protein glycoforms. Mol. Biotechnol. 12, 203-206 (Pubitemid 29531809)
32. Nakamura-Tsuruta, S., Kominami, J., Kamei, M., Koyama, Y., Suzuki, T., Isemura, M., and Hirabayashi, J. (2006) Comparative analysis by frontal affinity chromatography of oligosaccharide specificity of GlcNAc-binding lectins, Griffonia simplicifolia lectin-II (GSL-II) and Boletopsis leucomelas lectin (BLL) J. Biochem. 140, 285-291 (Pubitemid 44618915)
33. Oda, Y., Senaha, T., Matsuno, Y., Nakajima, K., Naka, R., Kinoshita, M., Honda, E., Furuta, I., and Kakehi, K. (2003) A new fungal lectin recognizing α(1-6)-linked fucose in the N-glycan. J. Biol. Chem. 278, 32439-32447 (Pubitemid 37048442)
34. Nakagawa, T., Miyoshi, E., Yakushijin, T., Hiramatsu, N., Igura, T., Hayashi, N., Taniguchi, N., and Kondo, A. (2008) Glycomic analysis of α-fetoprotein L3 in hepatoma cell lines and hepatocellular carcinoma patients. J. Proteome Res. 7, 2222-2233
35. Abelev, G. I., Perova, S. D., Khramkova, N. I., Postnikova, Z. A., and Irlin, I. S. (1963) Production of embryonal α-globulin by transplantable mouse hepatomas. Transplantation 1, 174-180
36. Morinaga, T., Sakai, M., Wegmann, T. G., and Tamaoki, T. (1983) Primary structures of human α-fetoprotein and its mRNA. Proc. Natl. Acad. Sci. U.S.A. 80, 4604-4608 (Pubitemid 13030973)
37. Taketa, K., and Hirai, H. (1989) Lectin affinity electrophoresis of α-fetoprotein in cancer diagnosis. Electrophoresis 10, 562-567 (Pubitemid 19219287)
38. Li, D., Mallory, T., and Satomura, S. (2001) AFP-L3. A new generation of tumor marker for hepatocellular carcinoma. Clin. Chim. Acta 313, 15-19 (Pubitemid 33016686)
39. Yamagata, Y., Shimizu, K., Nakamura, K., Henmi, F., Satomura, S., Matsuura, S., and Tanaka, M. (2003) Simultaneous determination of percentage of Lens culinaris agglutinin-reactive α-fetoprotein and α-fetoprotein concentration using the LiBASys clinical auto-analyzer. Clin. Chim. Acta 327, 59-67 (Pubitemid 35447817)
40. Sterling, R. K., Jeffers, L., Gordon, F., Sherman, M., Venook, A. P., Reddy, K. R., Satomura, S., and Schwartz, M. E. (2007) Clinical utility of AFP-L3% measurement in North American patients with HCV-related cirrhosis. Am. J. Gastroenterol. 102, 2196-2205 (Pubitemid 47493844)
41. Kagebayashi, C., Yamaguchi, I., Akinaga, A., Kitano, H., Yokoyama, K., Satomura, M., Kurosawa, T., Watanabe, M., Kawabata, T., Chang, W., Li, C., Bousse, L., Wada, H. G., and Satomura, S. (2009) Automated immunoassay system for AFP-L3% using on-chip electrokinetic reaction and separation by affinity electrophoresis. Anal. Biochem. 388, 306-311
42. Tamura, Y., Igarashi, M., Kawai, H., Suda, T., Satomura, S., and Aoyagi, Y. (2010) Clinical advantage of highly sensitive on-chip immunoassay for fucosylated fraction of α-fetoprotein in patients with hepatocellular carcinoma. Dig. Dis. Sci. 55, 3576-3583
43. Morota, K., Nakagawa, M., Sekiya, R., Hemken, P. M., Sokoll, L. J., Elliott, D., Chan, D. W., and Dowell, B. L. (2011) A comparative evaluation of Golgi protein-73, fucosylated hemopexin, α-fetoprotein, and PIVKA-II in the serum of patients with chronic hepatitis, cirrhosis, and hepatocellular carcinoma. Clin. Chem. Lab. Med. 49, 711-718
44. Norton, P. A., Comunale, M. A., Krakover, J., Rodemich, L., Pirog, N., D'Amelio, A., Philip, R., Mehta, A. S., and Block, T. M. (2008) N-Linked glycosylation of the liver cancer biomarker GP73. J. Cell. Biochem. 104, 136-149
45. Wang, M., Long, R. E., Comunale, M. A., Junaidi, O., Marrero, J., Di Bisceglie, A. M., Block, T. M., and Mehta, A. S. (2009) Novel fucosylated biomarkers for the early detection of hepatocellular carcinoma. Cancer Epidemiol. Biomarkers Prev. 18, 1914-1921
46. Yamamoto, K., Imamura, H., Matsuyama, Y., Kume, Y., Ikeda, H., Norman, G. L., Shums, Z., Aoki, T., Hasegawa, K., Beck, Y., Sugawara, Y., and Kokudo, N. (2010) AFP, AFP-L3, DCP, and GP73 as markers for monitoring treatment response and recurrence and as surrogate markers of clinicopathological variables of HCC. J. Gastroenterol. 45, 1272-1282
47. Comunale, M. A., Rodemich-Betesh, L., Hafner, J., Wang, M., Norton, P., Di Bisceglie, A. M., Block, T., and Mehta, A. (2010) Linkage specific fucosylation of alpha-1-antitrypsin in liver cirrhosis and cancer patients. Implications for a biomarker of hepatocellular carcinoma. PLoS One 5, 12419-12422
48. Fukuda, T., Hashimoto, H., Okayasu, N., Kameyama, A., Onogi, H., Nakagawasai, O., Nakazawa, T., Kurosawa, T., Hao, Y., Isaji, T., Tadano, T., Narimatsu, H., Taniguchi, N., and Gu, J. (2011) α1,6-Fucosyltransferase- deficient mice exhibit multiple behavioral abnormalities associated with a schizophrenia-like phenotype. Importance of the balance between the dopamine and serotonin systems. J. Biol. Chem. 286, 18434-18443
49. Wang, X., Inoue, S., Gu, J., Miyoshi, E., Noda, K., Li, W., Mizuno-Horikawa, Y., Nakano, M., Asahi, M., Takahashi, M., Uozumi, N., Ihara, S., Lee, S. H., Ikeda, Y., Yamaguchi, Y., Aze, Y., Tomiyama, Y., Fujii, J., Suzuki, K., Kondo, A., Shapiro, S. D., Lopez-Otin, C., Kuwaki, T., Okabe, M., Honke, K., and Taniguchi, N. (2005) Dysregulation of TGF-β1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 102, 15791-15796 (Pubitemid 41552821)
50. Moriwaki, K., Noda, K., Furukawa, Y., Ohshima, K., Uchiyama, A., Nakagawa, T., Taniguchi, N., Daigo, Y., Nakamura, Y., Hayashi, N., and Miyoshi, E. (2009) Deficiency of GMDS leads to escape from NK cell-mediated tumor surveillance through modulation of TRAIL signaling. Gastroenterology 137, 188-198
51. Moriwaki, K., Shinzaki, S., and Miyoshi, E. (2011) GDP-mannose-4,6- dehydratase (GMDS) deficiency renders colon cancer cells resistant to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) receptor- and CD95-mediated apoptosis by inhibiting complex II formation. J. Biol. Chem. 286, 43123-43133