NEU1 sialidase expressed in human airway epithelia regulates epidermal growth factor receptor (EGFR) and MUC1 protein signaling

Journal of Biological Chemistry

Volumn 287, Issue 11, 2012, Pages 8214-8231

  Lillehoj, Erik P ^a   Hyun, Sang Won ^a   Feng, Chiguang ^b   Zhang, Lei ^b   Liu, Anguo ^a   Guang, Wei ^a   Nguyen, Chinh ^a   Luzina, Irina G ^a   Atamas, Sergei P ^a   Passaniti, Antonino ^a   Twaddell, William S ^a   Puché, Adam C ^a   Wang, Lai Xi ^a   Cross, Alan S ^a,b   Goldblum, Simeon E ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b University of Maryland School of Medicine Center for Vaccine Development   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHOSPHORYLATION; BACTERIAL ADHESION; DANGER SIGNALS; EPIDERMAL GROWTH FACTOR RECEPTORS; EPITHELIAL CELLS; EXTERNAL ENVIRONMENTS; HUMAN AIRWAY; IN-VIVO; OVER-EXPRESSION; PEANUT AGGLUTININ; PROTECTIVE BARRIER; PROTEIN LEVEL; PROTEIN SIGNALING; PSEUDOMONAS AERUGINOSA; REPAIR PROGRAM; SIALIDASES; SIALYLATION; SMALL AIRWAYS;

CATALYST ACTIVITY; RESPIRATORY SYSTEM; RNA;

ADHESION;

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; FLAGELLIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MUCIN 1; NEURAMINIDASE 1; SIALIDASE; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHOSPHORYLATION; BACTERIUM ADHERENCE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME SUBSTRATE; EPITHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; REGULATORY MECHANISM; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION;

CELL LINE, TRANSFORMED; EPIDERMAL GROWTH FACTOR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUCIN-1; NEURAMINIDASE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RESPIRATORY MUCOSA;

ARACHIS HYPOGAEA; BACTERIA (MICROORGANISMS); MAACKIA AMURENSIS; PSEUDOMONAS AERUGINOSA;

EID: 84863272837     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.292888     Document Type: Article

References (80)

1. Burgel, P. R., and Nadel, J. A. (2004) Roles of epidermal growth factor receptor activation in epithelial cell repair and mucin production in airway epithelium. Thorax 59, 992-996
2. Varki, A. (2008) Sialic acids in human health and disease. Trends Mol. Med. 14, 351-360
3. Schauer, R. (2009) Sialic acids as regulators of molecular and cellular interactions. Curr. Opin. Struct. Biol. 19, 507-514
4. Gagneux, P., Cheriyan, M., Hurtado-Ziola, N., van der Linden, E. C., Anderson, D., McClure, H., Varki, A., and Varki, N. M. (2003) Human-specific regulation of α2-6-linked sialic acids. J. Biol. Chem. 278, 48245-48250 (Pubitemid 37523279)
5. Rose, M. C., and Voynow, J. A. (2006) Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol. Rev. 86, 245-278
6. Yoon, S. J., Nakayama, K., Hikita, T., Handa, K., and Hakomori, S. I. (2006) Epidermal growth factor receptor tyrosine kinase is modulated by GM3 interaction with N-linked GlcNAc termini of the receptor. Proc. Natl. Acad. Sci. U.S.A. 103, 18987-18991 (Pubitemid 350002815)
7. Kawashima, N., Yoon, S. J., Itoh, K., and Nakayama, K. (2009) Tyrosine kinase activity of epidermal growth factor receptor is regulated by GM3 binding through carbohydrate to carbohydrate interactions. J. Biol. Chem. 284, 6147-6155
8. Li, R., Liu, Y., and Ladisch, S. (2001) Enhancement of epidermal growth factor signaling and activation of SRC kinase by gangliosides. J. Biol. Chem. 276, 42782-42792
9. Hattrup, C. L., and Gendler, S. J. (2008) Structure and function of the cell surface (tethered) mucins. Annu. Rev. Physiol. 70, 431-457 (Pubitemid 351738187)
10. Schroeder, J. A., Thompson, M. C., Gardner, M. M., and Gendler, S. J. (2001) Transgenic MUC1 interacts with epidermal growth factor receptor and correlates with mitogen-activated protein kinase activation in the mouse mammary gland. J. Biol. Chem. 276, 13057-13064
11. Hayashi, F., Smith, K. D., Ozinsky, A., Hawn, T. R., Yi, E. C., Goodlett, D. R., Eng, J. K., Akira, S., Underhill, D. M., and Aderem, A. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099-1103 (Pubitemid 32391041)
12. Adamo, R., Sokol, S., Soong, G., Gomez, M. I., and Prince, A. (2004) Pseudomonas aeruginosa flagella activate airway epithelial cells through asialoGM1 and toll-like receptor 2 as well as toll-like receptor 5. Am. J. Respir. Cell Mol. Biol. 30, 627-634 (Pubitemid 38591213)
13. Imberty, A., and Varrot, A. (2008) Microbial recognition of human cell surface glycoconjugates. Curr. Opin. Struct. Biol. 18, 567-576
14. Trappetti, C., Kadioglu, A., Carter, M., Hayre, J., Iannelli, F., Pozzi, G., Andrew, P. W., and Oggioni, M. R. (2009) Sialic acid: a preventable signal for pneumococcal biofilm formation, colonization, and invasion of the host. J. Infect. Dis. 199, 1497-1505
15. Harduin-Lepers, A., Vallejo-Ruiz, V., Krzewinski-Recchi, M. A., Samyn- Petit, B., Julien, S., and Delannoy, P. (2001) The human sialyltransferase family. Biochimie 83, 727-737 (Pubitemid 32821237)
16. Monti, E., Preti, A., Venerando, B., and Borsani, G. (2002) Recent development in mammalian sialidase molecular biology. Neurochem. Res. 27, 649-663
17. Miyagi, T., Wada, T., Iwamatsu, A., Hata, K., Yoshikawa, Y., Tokuyama, S., and Sawada, M. (1999) Molecular cloning and characterization of a plasma membrane-associated sialidase specific for gangliosides. J. Biol. Chem. 274, 5004-5011
18. Monti, E., Preti, A., Nesti, C., Ballabio, A., and Borsani, G. (1999) Expression of a novel human sialidase encoded by the NEU2 gene. Glycobiology 9, 1313-1321 (Pubitemid 30011511)
19. Pshezhetsky, A. V., Richard, C., Michaud, L., Igdoura, S., Wang, S., Elsliger, M. A., Qu, J., Leclerc, D., Gravel, R., Dallaire, L., and Potier, M. (1997) Cloning, expression and chromosomal mapping of human lysosomal sialidase and characterization of mutations in sialidosis. Nat. Genet. 15, 316-320 (Pubitemid 27098731)
20. Bonten, E. J., and d'Azzo, A. (2000) Lysosomal neuraminidase. Catalytic activation in insect cells is controlled by the protective protein/cathepsin A. J. Biol. Chem. 275, 37657-37663 (Pubitemid 32004878)
21. Comelli, E. M., Amado, M., Lustig, S. R., and Paulson, J. C. (2003) Identification and expression of Neu4, a novel murine sialidase. Gene 321, 155-161 (Pubitemid 37421406)
22. Hyun, S. W., Anglin, I. E., Liu, A., Yang, S., Sorkin, J. D., Lillehoj, E., Tonks, N. K., Passaniti, A., and Goldblum, S. E. (2011) Diverse injurious stimuli reduce protein tyrosine phosphatase-μ expression and enhance epidermal growth factor receptor signaling in human airway epithelia. Exp. Lung Res. 37, 327-343
23. Cross, A. S., Sakarya, S., Rifat, S., Held, T. K., Drysdale, B. E., Grange, P. A., Cassels, F. J., Wang, L. X., Stamatos, N., Farese, A., Casey, D., Powell, J., Bhattacharjee, A. K., Kleinberg, M., and Goldblum, S. E. (2003) Recruitment of murine neutrophils in vivo through endogenous sialidase activity. J. Biol. Chem. 278, 4112-4120 (Pubitemid 36801147)
24. Sakarya, S., Rifat, S., Zhou, J., Bannerman, D. D., Stamatos, N. M., Cross, A. S., and Goldblum, S. E. (2004) Mobilization of neutrophil sialidase activity desialylates the pulmonary vascular endothelial surface and increases resting neutrophil adhesion to and migration across the endothelium. Glycobiology 14, 481-494 (Pubitemid 38868263)
25. Guang, W., Ding, H., Czinn, S. J., Kim, K. C., Blanchard, T. G., and Lillehoj, E. P. (2010) Muc1 cell surface mucin attenuates epithelial inflammation in response to a common mucosal pathogen. J. Biol. Chem. 285, 20547-20557
26. Gong, P., Angelini, D. J., Yang, S., Xia, G., Cross, A. S., Mann, D., Bannerman, D. D., Vogel, S. N., and Goldblum, S. E. (2008) TLR4 signaling is coupled to SRC family kinase activation, tyrosine phosphorylation of zonula adherens proteins, and opening of the paracellular pathway in human lung microvascular endothelia. J. Biol. Chem. 283, 13437-13449
27. Achyuthan, K. E., and Achyuthan A. M. (2001) Comparative enzymology, biochemistry and pathophysiology of human exo-α-sialidases (neuraminidases). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 129, 29-64 (Pubitemid 32401124)
28. Angelini, D. J., Hyun, S. W., Grigoryev, D. N., Garg, P., Gong, P., Singh, I. S., Passaniti, A., Hasday, J. D., and Goldblum, S. E. (2006) TNF-α increases tyrosine phosphorylation of vascular endothelial cadherin and opens the paracellular pathway through fyn activation in human lung endothelia. Am. J. Physiol. Lung Cell. Mol. Physiol. 291, L1232-L1245 (Pubitemid 44904530)
29. Liu, A., Garg, P., Yang, S., Gong, P., Pallero, M. A., Annis, D. S., Liu, Y., Passaniti, A., Mann, D., Mosher, D. F., Murphy-Ullrich, J. E., and Goldblum, S. E. (2009) Epidermal growth factor-like repeats of thrombospondins activate phospholipase Cγ and increase epithelial cell migration through indirect epidermal growth factor receptor activation. J. Biol. Chem. 284, 6389-6402
30. Lillehoj, E. P., Hyun, S. W., Kim, B. T., Zhang, X. G., Lee, D. I., Rowland, S., and Kim, K. C. (2001) Muc1 mucins on the cell surface are adhesion sites for Pseudomonas aeruginosa. Am. J. Physiol. Lung Cell. Mol. Physiol. 280, L181-L187
31. Lindorfer, M. A., Nardin, A., Foley, P. L., Solga, M. D., Bankovich, A. J., Martin, E. N., Henderson, A. L., Price, C. W., Gyimesi, E., Wozencraft, C. P., Goldberg, J. B., Sutherland, W. M., and Taylor, R. P. (2001) Targeting of Pseudomonas aeruginosa in the bloodstream with bispecific monoclonal antibodies. J. Immunol. 167, 2240-2249 (Pubitemid 32747536)
32. Lillehoj, E. P., Kim, B. T., and Kim, K. C. (2002) Identification of Pseudomonas aeruginosa flagellin as an adhesin for Muc1 mucin. Am. J. Physiol. Lung Cell. Mol. Physiol. 282, L751-L756 (Pubitemid 34665591)
33. Lillehoj, E. P., Kim, H., Chun, E. Y., and Kim, K. C. (2004) Pseudomonas aeruginosa stimulates phosphorylation of the airway epithelial membrane glycoprotein Muc1 and activates MAP kinase. Am. J. Physiol. Lung Cell. Mol. Physiol. 287, L809-L815 (Pubitemid 39249394)
34. Wang, P., Zhang, J., Bian, H., Wu, P., Kuvelkar, R., Kung, T. T., Crawley, Y., Egan, R. W., and Billah, M. M. (2004) Induction of lysosomal and plasma membrane-bound sialidases in human T-cells via T-cell receptor. Biochem. J. 380, 425-433 (Pubitemid 38788114)
35. Bonten, E., van der Spoel, A., Fornerod, M., Grosveld, G., and d'Azzo, A. (1996) Characterization of human lysosomal neuraminidase defines the molecular basis of the metabolic storage disorder sialidosis. Genes Dev. 10, 3156-3169 (Pubitemid 27020543)
36. Amith, S. R., Jayanth, P., Franchuk, S., Finlay, T., Seyrantepe, V., Beyaert, R., Pshezhetsky, A. V., and Szewczuk, M. R. (2010) Neu1 desialylation of sialyl α-2,3-linked β-galactosyl residues of TOLL-like receptor 4 is essential for receptor activation and cellular signaling. Cell. Signal. 22, 314-324
37. Duca, L., Blanchevoye, C., Cantarelli, B., Ghoneim, C., Dedieu, S., Delacoux, F., Hornebeck, W., Hinek, A., Martiny, L., and Debelle, L. (2007) The elastin receptor complex transduces signals through the catalytic activity of its Neu-1 subunit. J. Biol. Chem. 282, 12484-12491 (Pubitemid 47100624)
38. Antonicelli, F., Bellon, G., Lorimier, S., and Hornebeck, W. (2009) Role of the elastin receptor complex (S-Gal/Cath-A/Neu-1) in skin repair and regeneration. Wound Repair Regen. 17, 631-638
39. Jayanth, P., Amith, S. R., Gee, K., and Szewczuk, M. R. (2010) Neu1 sialidase and matrix metalloproteinase-9 cross-talk is essential for neurotrophin activation of Trk receptors and cellular signaling. Cell. Signal. 22, 1193-1205
40. Hinek, A., Bodnaruk, T. D., Bunda, S., Wang, Y., and Liu, K. (2008) Neuraminidase-1, a subunit of the cell surface elastin receptor, desialylates and functionally inactivates adjacent receptors interacting with the mitogenic growth factors PDGF-BB and IGF-2. Am. J. Pathol. 173, 1042-1056
41. Liu, Y. C., Yen, H. Y., Chen, C. Y., Chen, C. H., Cheng, P. F., Juan, Y. H., Chen, C. H., Khoo, K. H., Yu, C. J., Yang, P. C., Hsu, T. L., and Wong, C. H. (2011) Sialylation and fucosylation of epidermal growth factor receptor suppress its dimerization and activation in lung cancer cells. Proc. Natl. Acad. Sci. U.S.A. 108, 11332-11337
42. Kawaguchi, T., Matsumoto, I., and Osawa, T. (1974) Studies on hemagglutinins from Maackia amurensis seeds. J. Biol. Chem. 249, 2786-2792
43. Wu, W., Punt, J. A., Granger, L., Sharrow, S. O., and Kearse, K. P. (1997) Developmentally regulated expression of peanut agglutinin (PNA)-specific glycans on murine thymocytes. Glycobiology 7, 349-356 (Pubitemid 27187440)
44. Morreau, H., Galjart, N. J., Willemsen, R., Gillemans, N., Zhou, X. Y., and d'Azzo, A. (1992) Human lysosomal protective protein. Glycosylation, intracellular transport, and association with β-galactosidase in the endoplasmic reticulum. J. Biol. Chem. 267, 17949-17956
45. Beguinot, L., Lyall, R. M., Willingham, M. C., and Pastan, I. (1984) Down-regulation of the epidermal growth factor receptor in KB cells is due to receptor internalization and subsequent degradation in lysosomes. Proc. Natl. Acad. Sci. U.S.A. 81, 2384-2388 (Pubitemid 14148263)
46. Kato, K., Lillehoj, E. P., Kai, H., and Kim, K. C. (2010) MUC1 expression by human airway epithelial cells mediates Pseudomonas aeruginosa adhesion. Front. Biosci. 2, 68-77
47. Liang, F., Seyrantepe, V., Landry, K., Ahmad, R., Ahmad, A., Stamatos, N. M., and Pshezhetsky, A. V. (2006) Monocyte differentiation up-regulates the expression of the lysosomal sialidase, Neu1, and triggers its targeting to the plasma membrane via major histocompatibility complex class II-positive compartments. J. Biol. Chem. 281, 27526-27538 (Pubitemid 44401779)
48. Lukong, K. E., Seyrantepe, V., Landry, K., Trudel, S., Ahmad, A., Gahl, W. A., Lefrancois, S., Morales, C. R., and Pshezhetsky, A. V. (2001) Intracellular distribution of lysosomal sialidase is controlled by the internalization signal in its cytoplasmic tail. J. Biol. Chem. 276, 46172-46181
49. Nan, X., Carubelli, I., and Stamatos, N. M. (2007) Sialidase expression in activated human T lymphocytes influences production of IFN-γ. J. Leukoc. Biol. 81, 284-296 (Pubitemid 46021278)
50. Hanisch, F. G., Stadie, T., and Bosslet, K. (1995) Monoclonal antibody BW835 defines a site-specific Thomsen-Friedenreich disaccharide linked to threonine within the VTSA motif of MUC1 tandem repeats. Cancer Res. 55, 4036-4040
51. Uehara, F., and Ohba, N. (2002) MUC1 and sialoglycan expression associated with cytotoxic T lymphocyte infiltration in eyelid malignant tumors. Jpn. J. Ophthalmol. 46, 237-243 (Pubitemid 34626630)
52. Meuillet, E. J., Kroes, R., Yamamoto, H., Warner, T. G., Ferrari, J., Mania-Farnell, B., George, D., Rebbaa, A., Moskal, J. R., and Bremer, E. G. (1999) Sialidase gene transfection enhances epidermal growth factor receptor activity in an epidermoid carcinoma cell line, A431. Cancer Res. 59, 234-240 (Pubitemid 29062983)
53. Monti, E., Bassi, M. T., Papini, N., Riboni, M., Manzoni, M., Venerando, B., Croci, G., Preti, A., Ballabio, A., Tettamanti, G., and Borsani, G. (2000) Identification and expression of NEU3, a novel human sialidase associated to the plasma membrane. Biochem. J. 349, 343-351 (Pubitemid 30440200)
54. Yamaguchi, K., Hata, K., Wada, T., Moriya, S., and Miyagi, T. (2006) Epidermal growth factor-induced mobilization of a ganglioside-specific sialidase (NEU3) to membrane ruffles. Biochem. Biophys. Res. Commun. 346, 484-490 (Pubitemid 43902710)
55. Beachey, E. H. (1981) Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surface. J. Infect. Dis. 143, 325-345
56. Saiman, L., and Prince, A. (1993) Pseudomonas aeruginosa pili bind to asialo GM1 which is increased on the surface of cystic fibrosis epithelial cells. J. Clin. Investig. 92, 1875-1880 (Pubitemid 23304555)
57. Gupta, S. K., Masinick, S., Garrett, M., and Hazlett, L. D. (1997) Pseudomonas aeruginosa lipopolysaccharide binds galectin-3 and other human corneal epithelial proteins. Infect. Immun. 65, 2747-2753 (Pubitemid 27264103)
58. Schroeder, T. H., Lee, M. M., Yacono, P. W., Cannon, C. L., Gerçeker, A. A., Golan, D. E., and Pier, G. B. (2002) CFTR is a pattern recognition molecule that extracts Pseudomonas aeruginosa LPS from the outer membrane into epithelial cells and activates NF-κB translocation. Proc. Natl. Acad. Sci. U.S.A. 99, 6907-6912 (Pubitemid 34526231)
59. Zhang, J., Xu, K., Ambati, B., and Yu, F. S. (2003) Toll-like receptor 5-mediated corneal epithelial inflammatory responses to Pseudomonas aeruginosa flagellin. Invest. Ophthalmol. Vis. Sci. 44, 4247-4254 (Pubitemid 37186258)
60. Soong, G., Reddy, B., Sokol, S., Adamo, R., and Prince, A. (2004) TLR2 is mobilized into an apical lipid raft receptor complex to signal infection in airway epithelial cells. J. Clin. Investig. 113, 1482-1489 (Pubitemid 39071704)
61. Pastoriza Gallego, M., and Hulen, C. (2006) Influence of sialic acid and bacterial sialidase on differential adhesion of Pseudomonas aeruginosa to epithelial cells. Colloids Surf. B Biointerfaces 52, 154-156 (Pubitemid 44428157)
62. McAuley, J. L., Linden, S. K., Png, C. W., King, R. M., Pennington, H. L., Gendler, S. J., Florin, T. H., Hill, G. R., Korolik, V., and McGuckin, M. A. (2007) MUC1 cell surface mucin is a critical element of the mucosal bar- rier to infection. J. Clin. Investig. 117, 2313-2324 (Pubitemid 47219576)
63. Costa, N. R., Mendes, N., Marcos, N. T., Reis, C. A., Caffrey, T., Hollingsworth, M. A., and Santos-Silva, F. (2008) Relevance of MUC1 mucin variable number of tandem repeats polymorphism in H. pylori adhesion to gastric epithelial cells. World J. Gastroenterol. 14, 1411-1414 (Pubitemid 351425223)
64. Parker, P., Sando, L., Pearson, R., Kongsuwan, K., Tellam, R. L., and Smith, S. (2010) Bovine Muc1 inhibits binding of enteric bacteria to Caco-2 cells. Glycoconj. J. 27, 89-97
65. Varki, A. (1997) Sialic acids as ligands in recognition phenomena. FASEB J. 11, 248-255
66. Bremer, E. G., Schlessinger, J., and Hakomori, S. (1986) Ganglioside-mediated modulation of cell growth. Specific effects of GM3 on tyrosine phosphorylation of the epidermal growth factor receptor. J. Biol. Chem. 261, 2434-2440 (Pubitemid 17205183)
67. Li, Y., Ren, J., Yu, W., Li, Q., Kuwahara, H., Yin, L., Carraway, K. L, 3rd, and Kufe, D. (2001) The epidermal growth factor receptor regulates interaction of the human DF3/MUC1 carcinoma antigen with c-Src and β-catenin. J. Biol. Chem. 276, 35239-35242
68. Pochampalli, M. R., el Bejjani, R. M., and Schroeder, J. A. (2007) MUC1 is a novel regulator of ErbB1 receptor trafficking. Oncogene 26, 1693-1701 (Pubitemid 46426203)
69. Amith, S. R., Jayanth, P., Franchuk, S., Siddiqui, S., Seyrantepe, V., Gee, K., Basta, S., Beyaert, R., Pshezhetsky, A. V., and Szewczuk, M. R. (2009) Dependence of pathogen molecule-induced toll-like receptor activation and cell function on Neu1 sialidase. Glycoconj. J. 26, 1197-1212
70. d'Azzo, A., and Bonten, E. (2010) Molecular mechanisms of pathogenesis in a glycosphingolipid and a glycoprotein storage disease. Biochem. Soc. Trans. 38, 1453-1457
71. Buccoliero, R., Palmeri, S., Ciarleglio, G., Collodoro, A., De Santi, M. M., and Federico, A. (2007) Increased lung surfactant phosphatidylcholine in patients affected by lysosomal storage diseases. J. Inherit. Metab. Dis. 30, 983
72. Starcher, B., d'Azzo, A., Keller, P. W., Rao, G. K., Nadarajah, D., and Hinek, A. (2008) Neuraminidase-1 is required for the normal assembly of elastic fibers. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L637-L647
73. Champigny, M. J., Johnson M., and Igdoura, S. A. (2003) Characterization of the mouse lysosomal sialidase promoter. Gene 319, 177-187 (Pubitemid 37346212)
74. Olayioye, M. A., Neve, R. M., Lane, H. A., and Hynes, N. E. (2000) The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J. 19, 3159-3167 (Pubitemid 30428195)
75. Kato, T., Wang, Y., Yamaguchi, K., Milner, C. M., Shineha, R., Satomi, S., and Miyagi, T. (2001) Overexpression of lysosomal-type sialidase leads to suppression of metastasis associated with reversion of malignant phenotype in murine B16 melanoma cells. Int. J. Cancer 92, 797-804 (Pubitemid 32467367)
76. Uemura, T., Shiozaki, K., Yamaguchi, K., Miyazaki, S., Satomi, S., Kato, K., Sakuraba, H., and Miyagi, T. (2009) Contribution of sialidase NEU1 to suppression of metastasis of human colon cancer cells through desialylation of integrin β4. Oncogene 28, 1218-1229
77. Ram, S., Sharma, A. K., Simpson, S. D., Gulati, S., McQuillen, D. P., Pangburn, M. K., and Rice, P. A. (1998) A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J. Exp. Med. 187, 743-752 (Pubitemid 28115190)
78. Anthony, R. M., and Ravetch, J. V. (2010) A novel role for the IgG Fc glycan: the anti-inflammatory activity of sialylated IgG Fcs. J. Clin. Immunol. 30, S9-S14
79. Yoshimura, M., Ihara, Y., Matsuzawa, Y., and Taniguchi, N. (1996) Aberrant glycosylation of E-cadherin enhances cell-cell binding to suppress metastasis. J. Biol. Chem. 271, 13811-13815 (Pubitemid 26185425)
80. Steelant, W. F., Recchi, M. A., Noë, V. T., Boilly-Marer, Y., Bruyneel, E. A., Verbert, A., Mareel, M. M., and Delannoy, P. (1999) Sialylation of E-cadherin does not change the spontaneous or ET-18-OMe-mediated aggregation of MCF-7 human breast cancer cells. Clin. Exp. Metastasis 17, 245-253 (Pubitemid 29360903)