NEU3 activity enhances EGFR activation without affecting EGFR expression and acts on its sialylation levels

Glycobiology

Volumn 25, Issue 8, 2015, Pages 855-868

  Mozzi, Alessandra ^a   Forcella, Matilde ^a   Riva, Alice ^b   Difrancesco, Carlotta ^b   Molinari, Francesca ^b   Martin, Vittoria ^b   Papini, Nadia ^c   Bernasconi, Barbara ^d   Nonnis, Simona ^c,f   Tedeschi, Gabriella ^c,f   Mazzucchelli, Luca ^b   Monti, Eugenio ^e   Fusi, Paola ^a   Frattini, Milo ^b  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b Pathology Institute Canton Ticino   (Switzerland)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF INSUBRIA   (Italy)

^e UNIVERSITY OF BRESCIA   (Italy)

^f Filarete Foundation   (Italy)

Author keywords

Cell lines; Colorectal cancer; EGFR; NEU3; Sialylation

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; MESSENGER RNA; PROTEIN NEU3; SIALIDASE; UNCLASSIFIED DRUG; EGFR PROTEIN, HUMAN; GANGLIOSIDE GM3; NEU3 PROTEIN, HUMAN; SIALIC ACID DERIVATIVE; TUMOR PROTEIN;

ARTICLE; CELL VIABILITY; COLORECTAL CANCER; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SIALYLATION; WESTERN BLOTTING; WILD TYPE; CELL MEMBRANE; CHEMICAL STRUCTURE; COLON; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL MEMBRANE; COLON; EPITHELIAL CELLS; G(M3) GANGLIOSIDE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MODELS, MOLECULAR; NEOPLASM PROTEINS; NEURAMINIDASE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIALIC ACIDS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84938815360     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwv026     Document Type: Article

References (100)

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25. Miyagi T, Wada T, Yamaguchi K, Hata K, Shiozaki K. 2008. Plasma membrane-associated sialidase as a crucial regulator of transmembrane signalling. J Biochem. 144: 279-285.
26. Monti E, Bassi MT, Papini N, Riboni M, Manzoni M, Venerando B, Croci G, Preti A, Ballabio A, Tettamanti G, et al. 2000. Identification and expression of NEU3, a novel human sialidase associated to the plasma membrane. Biochem J. 349: 343-351.
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28. Odintsova E, Butters TD, Monti E, Sprong H, van Meer G, Berditchevski F. 2006. Gangliosides play an important role in the organization of CD82-enriched microdomains. Biochem J. 400: 315-325.
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32. Park JJ, Yi JY, Jin YB, Lee YJ, Lee JS, Lee YS, Ko YG, Lee M. 2012. Sialylation of epidermal growth factor receptor regulates receptor activity and chemo-sensitivity to gefitinib in colon cancer cells. Biochem Pharmacol. 83: 849-857.
33. Saridaki Z, Tzardi M, Papadaki C, Sfakianaki M, Pega F, Kalikaki A, Tsakalaki E, Trypaki M, Messaritakis I, Stathopoulos E, et al. 2011. Impact of KRAS, BRAF, PIK3CA mutations, PTEN, AREG, EREG expression and skin rash in >/=2 line cetuximab-based therapy of colorectal cancer patients. PLoS ONE. 6: e15980.
34. Scaringi R, Piccoli M, Papini N, Cirillo F, Conforti E, Bergante S, Tringali C, Garatti A, Gelfi C, Venerando B, et al. 2013. NEU3 sialidase is activated under hypoxia and protects skeletal muscle cells from apoptosis through the activation of the epidermal growth factor receptor signaling pathway and the hypoxia-inducible factor (HIF)-1alpha. J Biol Chem. 288: 3153-3162.
35. Schauer R. 2009. Sialic acids as regulators of molecular and cellular interactions. Curr Opin Struct Biol. 19: 507-514.
36. Schwede T, Kopp J, Guex N, Peitsch MC. 2003. SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res. 31: 3381-3385.
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38. Shiozaki K, Yamaguchi K, Sato I, Miyagi T. 2009. Plasma membrane-associated sialidase (NEU3) promotes formation of colonic aberrant crypt foci in azoxymethane-treated transgenic mice. Cancer Sci. 100: 588-594.
39. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. 1985. Measurement of protein using bicinchoninic acid. Anal Biochem. 150: 76-85.
40. Taylor G. 1996. Sialidases: Structures, biological significance and therapeutic potential. Curr Opin Struct Biol. 6: 830-837.
41. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTALW: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
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45. Varki A. 2008. Sialic acids in human health and disease. Trends Mol Med. 14: 351-360.
46. Wada T, Hata K, Yamaguchi K, Shiozaki K, Koseki K, Moriya S, Miyagi T. 2007. A crucial role of plasma membrane-associated sialidase in the survival of human cancer cells. Oncogene. 26: 2483-2490.
47. Wu SL, Kim J, Hancock WS, Karger B. 2005. Extended range proteomic analysis (ERPA): A new and sensitive LC-MS platform for high sequence coverage of complex proteins with extensive post-translational modifications-comprehensive analysis of beta-casein and epidermal growth factor receptor (EGFR). J Proteome Res. 4: 1155-1170.
48. Yang HJ, Jung KY, Kwak DH, Lee SH, Ryu JS, Kim JS, Chang KT, Lee JW, Choo YK. 2011. Inhibition of ganglioside GD1a synthesis suppresses the differentiation of human mesenchymal stem cells into osteoblasts. Dev Growth Differ. 53: 323-332.
49. Zanchetti G, Colombi P, Manzoni M, Anastasia L, Caimi L, Borsani G, Venerando B, Tettamanti G, Preti A, Monti E, et al. 2007. Sialidase NEU3 is a peripheral membrane protein localized on the cell surface and in endosomal structures. Biochem J. 408: 211-219.
50. Zhen Y, Caprioli RM, Staros JV. 2003. Characterization of glycosylation sites of the epidermal growth factor receptor. Biochemistry. 42: 5478-5492.
51. Albohy A, Li MD, Zheng RB, Zou C, Cairo CW. 2010. Insight into substrate recognition and catalysis by the human neuraminidase 3 (NEU3) through molecular modeling and site-directed mutagenesis. Glycobiology. 20: 1127-1138.
52. Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics. 22: 195-201.
53. Bos PD, Zhang XH, Nadal C, Shu W, Gomis RR, Nguyen DX, Minn AJ, van de Vijver MJ, Gerald WL, Foekens JA, et al. 2009. Genes that mediate breast cancer metastasis to the brain. Nature. 459: 1005-1009.
54. Bradford MM 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.
55. Buschiazzo A, Alzari PM. 2008. Structural insights into sialic acid enzymology. Curr Opin Chem Biol. 12: 565-572.
56. Chavas LM, Tringali C, Fusi P, Venerando B, Tettamanti G, Kato R, Monti E, Wakatsuki S. 2005. Crystal structure of the human cytosolic sialidase Neu2. Evidence for the dynamic nature of substrate recognition. J Biol Chem. 280: 469-475.
57. Chigorno V, Cardace G, Pitto M, Sonnino S, Ghidoni R, Tettamanti G. 1986. A radiometric assay for ganglioside sialidase applied to the determination of the enzyme subcellular location in cultured human fibroblasts. Anal Biochem. 153: 283-294.
58. Chung KY, Shia J, Kemeny NE, Shah M, Schwartz GK, Tse A, Hamilton A, Pan D, Schrag D, Schwartz L, et al. 2005. Cetuximab shows activity in colorectal cancer patients with tumors that do not express the epidermal growth factor receptor by immunohistochemistry. J Clin Oncol. 23: 1803-1810.
59. Cooper CA, Gasteiger E, Packer NH. 2001. GlycoMod - A software tool for determining glycosylation compositions from mass spectrometric data. Proteomics. 1: 340-349.
60. Dolf G, Meyn RE, Curley D, Prather N, Story MD, Boman BM, Siciliano MJ, Hewitt RR. 1991. Extrachromosomal amplification of the epidermal growth factor receptor gene in a human colon carcinoma cell line. Genes Chromosomes Cancer. 3: 48-54.
61. Guex N, Peitsch MC. 1997. SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis. 18: 2714-2723.
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63. Hakomori SI, Handa K. 2015. GM3 and cancer. Glycoconjugate J. 32: 1-8.
64. Huang X, Li Y, Zhang J, Xu Y, Tian Y, Ma K. 2013. Ganglioside GM3 inhibits hepatoma cell motility via down-regulating activity of EGFR and PI3K/AKT signaling pathway. J Cell Biochem. 114: 1616-1624.
65. Jonker DJ, Karapetis CS, Harbison C, O'Callaghan CJ, Tu D, Simes RJ, Malone DP, Langer C, Tebbutt N, Price TJ, et al. 2014. Epiregulin gene expression as a biomarker of benefit from cetuximab in the treatment of advanced colorectal cancer. Br J Cancer. 110: 648-655.
66. Jorissen RN, Walker F, Pouliot N, Garrett TP, Ward CW, Burgess AW. 2003. Epidermal growth factor receptor: Mechanisms of activation and signalling. Exp Cell Res. 284: 31-53.
67. Kakugawa Y, Wada T, Yamaguchi K, Yamanami H, Ouchi K, Sato I, Miyagi T. 2002. Up-regulation of plasma membrane-associated ganglioside sialidase (Neu3) in human colon cancer and its involvement in apoptosis suppression. Proc Natl Acad Sci USA. 99: 10718-10723.
68. Kato K, Shiga K, Yamaguchi K, Hata K, Kobayashi T, Miyazaki K, Saijo S, Miyagi T. 2006. Plasma-membrane-associated sialidase (NEU3) differentially regulates integrin-mediated cell proliferation through laminin- and fibronectin-derived signalling. Biochem J. 394: 647-656.
69. Kuramochi H, Nakajima G, Kaneko Y, Nakamura A, Inoue Y, Yamamoto M, Hayashi K. 2012. Amphiregulin and epiregulin mRNA expression in primary colorectal cancer and corresponding liver metastases. BMC Cancer. 12: 88.
70. Liu YC, Yen HY, Chen CY, Chen CH, Cheng PF, Juan YH, Chen CH, Khoo KH, Yu CJ, Yang PC, et al. 2011. Sialylation and fucosylation of epidermal growth factor receptor suppress its dimerization and activation in lung cancer cells. Proc Natl Acad Sci USA. 108: 11332-11337.
71. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 25: 402-408.
72. Martin V, Mazzucchelli L, Frattini M. 2009. An overview of the epidermal growth factor receptor fluorescence in situ hybridisation challenge in tumour pathology. J Clin Pathol. 62: 314-324.
73. McKay JA, Murray LJ, Curran S, Ross VG, Clark C, Murray GI, Cassidy J, McLeod HL. 2002. Evaluation of the epidermal growth factor receptor (EGFR) in colorectal tumours and lymph node metastases. Eur J Cancer. 38: 2258-2264.
74. Miyagi T, Takahashi K, Hata K, Shiozaki K, Yamaguchi K. 2012. Sialidase significance for cancer progression. Glycoconjugate J. 29: 567-577.
75. Miyagi T, Wada T, Yamaguchi K, Hata K, Shiozaki K. 2008. Plasma membrane-associated sialidase as a crucial regulator of transmembrane signalling. J Biochem. 144: 279-285.
76. Monti E, Bassi MT, Papini N, Riboni M, Manzoni M, Venerando B, Croci G, Preti A, Ballabio A, Tettamanti G, et al. 2000. Identification and expression of NEU3, a novel human sialidase associated to the plasma membrane. Biochem J. 349: 343-351.
77. Monti E, Miyagi T. 2012. Structure and function of mammalian sialidases. Topics Curr Chem. [Epub ahead of Print].
78. Odintsova E, Butters TD, Monti E, Sprong H, van Meer G, Berditchevski F. 2006. Gangliosides play an important role in the organization of CD82-enriched microdomains. Biochem J. 400: 315-325.
79. Ohtsubo K, Marth JD. 2006. Glycosylation in cellular mechanisms of health and disease. Cell. 126: 855-867.
80. Papini N, Anastasia L, Tringali C, Croci G, Bresciani R, Yamaguchi K, Miyagi T, Preti A, Prinetti A, Prioni S, et al. 2004. The plasma membrane-associated sialidase MmNEU3 modifies the ganglioside pattern of adjacent cells supporting its involvement in cell-to-cell interactions. J Biol Chem. 279: 16989-16995.
81. Papini N, Anastasia L, Tringali C, Dileo L, Carubelli I, Sampaolesi M, Monti E, Tettamanti G, Venerando B. 2012. MmNEU3 sialidase over-expression in C2C12 myoblasts delays differentiation and induces hypertrophic myotube formation. J Cell Biochem. 113: 2967-2978.
82. Park JJ, Yi JY, Jin YB, Lee YJ, Lee JS, Lee YS, Ko YG, Lee M. 2012. Sialylation of epidermal growth factor receptor regulates receptor activity and chemo-sensitivity to gefitinib in colon cancer cells. Biochem Pharmacol. 83: 849-857.
83. Saridaki Z, Tzardi M, Papadaki C, Sfakianaki M, Pega F, Kalikaki A, Tsakalaki E, Trypaki M, Messaritakis I, Stathopoulos E, et al. 2011. Impact of KRAS, BRAF, PIK3CA mutations, PTEN, AREG, EREG expression and skin rash in >/=2 line cetuximab-based therapy of colorectal cancer patients. PLoS ONE. 6: e15980.
84. Scaringi R, Piccoli M, Papini N, Cirillo F, Conforti E, Bergante S, Tringali C, Garatti A, Gelfi C, Venerando B, et al. 2013. NEU3 sialidase is activated under hypoxia and protects skeletal muscle cells from apoptosis through the activation of the epidermal growth factor receptor signaling pathway and the hypoxia-inducible factor (HIF)-1alpha. J Biol Chem. 288: 3153-3162.
85. Schauer R. 2009. Sialic acids as regulators of molecular and cellular interactions. Curr Opin Struct Biol. 19: 507-514.
86. Schwede T, Kopp J, Guex N, Peitsch MC. 2003. SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res. 31: 3381-3385.
87. Shiozaki K, Takahashi K, Hosono M, Yamaguchi K, Hata K, Shiozaki M, Bassi R, Prinetti A, Sonnino S, Nitta K, et al. 2015. Phosphatidic acid-mediated activation and translocation to the cell surface of sialidase NEU3, promoting signaling for cell migration. FASEB J. 29: 2099-2111.
88. Shiozaki K, Yamaguchi K, Sato I, Miyagi T. 2009. Plasma membrane-associated sialidase (NEU3) promotes formation of colonic aberrant crypt foci in azoxymethane-treated transgenic mice. Cancer Sci. 100: 588-594.
89. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. 1985. Measurement of protein using bicinchoninic acid. Anal Biochem. 150: 76-85.
90. Taylor G. 1996. Sialidases: Structures, biological significance and therapeutic potential. Curr Opin Struct Biol. 6: 830-837.
91. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTALW: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
92. Trainer DL, Kline T, McCabe FL, Faucette LF, Feild J, Chaikin M, Anzano M, Rieman D, Hoffstein S, Li DJ, et al. 1988. Biological characterization and oncogene expression in human colorectal carcinoma cell lines. Int J Cancer. 41: 287-296.
93. Tringali C, Lupo B, Silvestri I, Papini N, Anastasia L, Tettamanti G, Venerando B. 2012. The plasma membrane sialidase NEU3 regulates the malignancy of renal carcinoma cells by controlling beta1 integrin internalization and recycling. J Biol Chem. 287: 42835-42845.
94. Varella-Garcia M, Diebold J, Eberhard DA, Geenen K, Hirschmann A, Kockx M, Nagelmeier I, Ruschoff J, Schmitt M, Arbogast S, et al. 2009. EGFR fluorescence in situ hybridisation assay: Guidelines for application to non-small-cell lung cancer. J Clin Pathol. 62: 970-977.
95. Varki A. 2008. Sialic acids in human health and disease. Trends Mol Med. 14: 351-360.
96. Wada T, Hata K, Yamaguchi K, Shiozaki K, Koseki K, Moriya S, Miyagi T. 2007. A crucial role of plasma membrane-associated sialidase in the survival of human cancer cells. Oncogene. 26: 2483-2490.
97. Wu SL, Kim J, Hancock WS, Karger B. 2005. Extended range proteomic analysis (ERPA): A new and sensitive LC-MS platform for high sequence coverage of complex proteins with extensive post-translational modifications-comprehensive analysis of beta-casein and epidermal growth factor receptor (EGFR). J Proteome Res. 4: 1155-1170.
98. Yang HJ, Jung KY, Kwak DH, Lee SH, Ryu JS, Kim JS, Chang KT, Lee JW, Choo YK. 2011. Inhibition of ganglioside GD1a synthesis suppresses the differentiation of human mesenchymal stem cells into osteoblasts. Dev Growth Differ. 53: 323-332.
99. Zanchetti G, Colombi P, Manzoni M, Anastasia L, Caimi L, Borsani G, Venerando B, Tettamanti G, Preti A, Monti E, et al. 2007. Sialidase NEU3 is a peripheral membrane protein localized on the cell surface and in endosomal structures. Biochem J. 408: 211-219.
100. Zhen Y, Caprioli RM, Staros JV. 2003. Characterization of glycosylation sites of the epidermal growth factor receptor. Biochemistry. 42: 5478-5492.