Where catabolism meets signalling: Neuraminidase 1 as a modulator of cell receptors

Glycoconjugate Journal

Volumn 28, Issue 7, 2011, Pages 441-452

  Pshezhetsky, Alexey V ^a,b,c   Hinek, Aleksander ^d  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Catabolism; Cell growth factors; Cytokines; Elastin; Exocytosis; Immune response; Lysosome; Muscle differentiation; Neuraminidase; Phagocytosis; Plasma membrane; Secretion; Sialidase

Indexed keywords

CELL RECEPTOR; GALACTOSE; GLYCOLIPID; GLYCOPROTEIN; MEMBRANE PROTEIN; N ACETYLGALACTOSAMINE; N ACETYLGLUCOSAMINE; SIALIC ACID; SIALIDASE; SIALYLTRANSFERASE;

CELL SURFACE; ENDOSOME; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME STRUCTURE; ENZYME SYNTHESIS; EXOCYTOSIS; EXTRACELLULAR MATRIX; GLYCOCALYX; HUMAN; LYSOSOME; MOLECULAR RECOGNITION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; SIALYLATION; SIGNAL TRANSDUCTION;

ANIMALS; B-LYMPHOCYTES; CELL MEMBRANE; GLYCOCALYX; GLYCOCONJUGATES; GLYCOLIPIDS; GLYCOPROTEINS; HUMANS; IMMUNITY; LYSOSOMES; MAMMALS; MICE; MYOCYTES, SMOOTH MUSCLE; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; PHAGOCYTOSIS; SIALYLTRANSFERASES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

MAMMALIA;

EID: 82955240622     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-011-9350-5     Document Type: Review

References (125)

1. Cohen, M., Varki, A.: The sialome-far more than the sum of its parts. OMICS 14, 455-464(2010)
2. Kundra, R., Kornfeld, S.: Asparagine-linked oligosaccharides protect Lamp-1 and Lamp-2 from intracellular proteolysis. J. Biol. Chem. 274, 31039-31046(1999)
3. Varki, A., Angata, T.: Siglecs-the major subfamily of I-type lectins. Glycobiology 16, 1R-27R (2006) (Pubitemid 43009801)
4. Cohen, M., Hurtado-Ziola, N., Varki, A.: ABO blood group glycans modulate sialic acid recognition on erythrocytes. Blood 114, 3668-3676(2009)
5. Hakomori, S.: Structure, organization, and function of glycosphingolipids in membrane. Curr. Opin. Hematol. 10, 16-24(2003) (Pubitemid 36020713)
6. Hakomori, S.: Carbohydrate-to-carbohydrate interaction, through glycosynapse, as a basis of cell recognition and membrane organization. Glycoconj. J. 21, 125-137(2004) (Pubitemid 39382658)
7. Todeschini, A. R., Hakomori, S. I.: Functional role of glycosphingolipids and gangliosides in control of cell adhesion, motility, and growth, through glycosynaptic microdomains. Biochim. Biophys. Acta 1780, 421-433(2008)
8. Jones, C. J., Aplin, J. D., Mulholland, J., Glasser, S. R.: Patterns of sialylation in differentiating rat decidual cells as revealed by lectin histochemistry. J. Reprod. Fertil. 99, 635-645(1993) (Pubitemid 24052014)
9. Kelm, S., Schauer, R.: Sialic acids in molecular and cellular interactions. Int. Rev. Cytol. 175, 137-240(1997) (Pubitemid 27309809)
10. Lehmann, F., Tiralongo, E., Tiralongo, J.: Sialic acid-specific lectins: occurrence, specificity and function. Cell. Mol. Life Sci. 63, 1331-1354(2006) (Pubitemid 43939016)
11. Allende, M. L., Proia, R. L.: Lubricating cell signaling pathways with gangliosides. Curr. Opin. Struct. Biol. 12, 587-592(2002) (Pubitemid 35449065)
12. Takashima, S.: Characterization of mouse sialyltransferase genes: their evolution and diversity. Biosci. Biotechnol. Biochem. 72, 1155-1167(2008) (Pubitemid 351872478)
13. Kreisel, W., Volk, B. A., Büchsel, R., Reutter, W.: Different halflives of the carbohydrate and protein moieties of a 110,000-dalton glycoprotein isolated from plasma membranes of rat liver. Proc. Natl. Acad. Sci. U. S. A. 77, 1828-1831(1980)
14. Tauber, R., Park, C. S., Reutter, W.: Intramolecular heterogeneity of degradation in plasma membrane glycoproteins: evidence for a general characteristic. Proc. Natl. Acad. Sci. U. S. A. 80, 4026-4029(1983)
15. Kopitz, J., von Reitzenstein, C., Sinz, K., Cantz, M.: Selective ganglioside desialylation in the plasma membrane of human neuroblastoma cells. Glycobiology 6, 367-376(1996)
16. Kreisel, W., Hanski, C., Tran-Thi, T. A., Katz, N., Decker, K., Reutter, W., Gerok, W.: Remodeling of a rat hepatocyte plasma membrane glycoprotein. De-and reglycosylation of dipeptidyl peptidase IV. J. Biol. Chem. 263, 11736-11742(1988)
17. Monti, E., Preti, A., Venerando, B., Borsani, G.: Recent development in mammalian sialidase molecular biology. Neurochem. Res. 27, 649-663(2002)
18. Saito, N., Yu, R. K.: Biochemistry and function of sialidases. In: Rosenberg, A. (ed.) Biology of sialic acids, pp. 261-313. Plenum Press, New York (1995)
19. Bonten, E., van der Spoel, A., Fornerod, M., Grosveld, G., D'Azzo, A.: Characterization of human lysosomal neuraminidase defines the molecular basis of the metabolic storage disorder sialidosis. Genes. Dev. 10, 3156-3169(1996) (Pubitemid 27020543)
20. Milner, C. M., Smith, S. V., Carrillo, M. B., Taylor, G. L., Hollinshead, M., Campbell, R. D.: Identification of a sialidase encoded in the human major histocompatibility complex. J. Biol. Chem. 272, 4549-4558(1997) (Pubitemid 27078536)
21. Pshezhetsky, A. V., Richard, C., Michaud, L., Igdoura, S., Wang, S., Elsliger, M. A., Qu, J., Leclerc, D., Gravel, R., Dallaire, L., Potier, M.: Cloning, expression and chromosomal mapping of human lysosomal sialidase and characterization of mutations in sialidosis. Nat. Genet. 15, 316-320(1997) (Pubitemid 27098731)
22. Miyagi, T., Konno, K., Emori, Y., Kawasaki, H., Suzuki, K., Yasui, A., Tsuik, S.: Molecular cloning and expression of cDNA encoding rat skeletal muscle cytosolic sialidase. J. Biol. Chem. 268, 26435-26440(1993) (Pubitemid 23361720)
23. Monti, E., Preti, A., Rossi, E., Ballabio, A., Borsani, G.: Cloning and characterization of NEU2, a human gene homologous to rodent soluble sialidases. Genomics 57, 137-143(1999) (Pubitemid 29187946)
24. Miyagi, T., Wada, T., Iwamatsu, A., Hata, K., Yoshikawa, Y., Tokuyama, S., Sawada, M.: Molecular cloning and characterization of a plasma membrane-associated sialidase specific for gangliosides. J. Biol. Chem. 274, 5004-5011(1999)
25. Wada, T., Yoshikawa, Y., Tokuyama, S., Kuwabara, M., Akita, H., Miyagi, T.: Cloning, expression, and chromosomal mapping of a human ganglioside sialidase. Biochem. Biophys. Res. Commun. 261, 21-27(1999) (Pubitemid 29371612)
26. Monti, E., Bassi, M. T., Papini, N., Riboni, M., Manzoni, M., Venerando, B., Croci, G., Preti, A., Ballabio, A., Tettamanti, G., Borsani, G.: Identification and expression of NEU3, a novel human sialidase associated to the plasma membrane. Biochem. J. 349, 343-351(2000) (Pubitemid 30440200)
27. Comelli, E. M., Amado, M., Lustig, S. R., Paulson, J. C.: Identification and expression of Neu4, a novel murine sialidase. Gene 321, 155-161(2003) (Pubitemid 37421406)
28. Monti, E., Bassi, M. T., Bresciani, R., Civini, S., Croci, G. L., Papini, N., Riboni, M., Zanchetti, G., Ballabio, A., Preti, A., Tettamanti, G., Venerando, B., Borsani, G.: Molecular cloning and characterization of NEU4, the fourth member of the human sialidase gene family. Genomics 83, 445-453(2004) (Pubitemid 38220849)
29. Seyrantepe, V., Landry, K., Trudel, S., Hassan, J. A., Morales, C. R., Pshezhetsky, A. V.: Neu4, a novel human lysosomal lumen sialidase, confers normal phenotype to sialidosis and galactosialidosis cells. J. Biol. Chem. 279, 37021-37029(2004) (Pubitemid 39129052)
30. Miyagi, T., Tsuiki, S.: Purification and characterization of cytosolic sialidase from rat liver. J. Biol. Chem. 260, 6710-6716(1985) (Pubitemid 15005857)
31. Tringali, C., Papini, N., Fusi, P., Croci, G., Borsani, G., Preti, A., Tortora, P., Tettamanti, G., Venerando, B., Monti, E.: Properties of recombinant human cytosolic sialidase HsNEU2. The enzyme hydrolyzes monomerically dispersed GM1 ganglioside molecules. J. Biol. Chem. 279, 3169-1379(2004)
32. Wang, Y., Yamaguchi, K., Wada, T., Hata, K., Zhao, X., Fujimoto, T., Miyagi, T.: A close association of the ganglioside-specific sialidase Neu3 with caveolin in membrane microdomains. J. Biol. Chem. 277, 26252-26259(2002) (Pubitemid 34967114)
33. Zanchetti, G., Colombi, P., Manzoni, M., Anastasia, L., Caimi, L., Borsani, G., Venerando, B., Tettamanti, G., Preti, A., Monti, E., Bresciani, R.: Sialidase NEU3 is a peripheral membrane protein localized on the cell surface and in endosomal structures. Biochem. J. 408, 211-219(2007) (Pubitemid 350206344)
34. Yamaguchi, K., Hata, K., Koseki, K., Shiozaki, K., Akita, H., Wada, T., Moriya, S., Miyagi, T.: Evidence for mitochondrial localization of a novel human sialidase (NEU4). Biochem. J. 390, 85-93(2005) (Pubitemid 41192234)
35. Bigi, A., Morosi, L., Pozzi, C., Forcella, M., Tettamanti, G., Venerando, B., Monti, E., Fusi, P.: Human sialidase NEU4 long and short are extrinsic proteins bound to outer mitochondrial membrane and the endoplasmic reticulum, respectively. Glycobiology 20, 148-157(2010)
36. Monti, E., Bonten, E., D'Azzo, A., Bresciani, R., Venerando, B., Borsani, G., Schauer, R., Tettamanti, G.: Sialidases in vertebrates: a family of enzymes tailored for several cell functions. Adv. Carbohydr. Chem. Biochem. 64, 403-479(2010)
37. Miyagi, T.: Aberrant expression of sialidase and cancer progression. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 84, 407-418(2008)
38. Oohira, T., Nagata, N., Akaboshi, I., Matsuda, I., Naito, S.: The infantile form of SL type II associated with congenital adrenal hyperplasia: possible linkage between HLA and the neuraminidase deficiency gene. Hum. Genet. 70, 341-343(1985) (Pubitemid 16241989)
39. Pshezhetsky, A. V., Ashmarina, M.: Lysosomal multienzyme complex: biochemistry, genetics, and molecular pathophysiology. Prog. Nucleic Acid Res. Mol. Biol. 69, 81-114(2001)
40. Lukong, K. E., Seyrantepe, V., Landry, K., Trudel, S., Ahmad, A., Gahl, W. A., Lefrancois, S., Morales, C. R., Pshezhetsky, A. V.: J. Biol. Chem. 276, 46172-46181(2001)
41. Vinogradova, M. V., Michaud, L., Mezentsev, A. V., Lukong, K. E., El-Alfy, M., Morales, C. R., Potier, M., Pshezhetsky, A. V.: Molecular mechanism of lysosomal sialidase deficiency in galactosialidosis involves its rapid degradation. Biochem. J. 330, 641-650(1998) (Pubitemid 28111957)
42. Cross, A. S., Wright, D. G.: Mobilization of sialidase from intracellular stores to the surface of human neutrophils and its role in stimulated adhesion responses of these cells. J. Clin. Invest. 88, 2067-2076(1991)
43. Liang, F., Seyrantepe, V., Landry, K., Ahmad, R., Ahmad, A., Stamatos, N. M., Pshezhetsky, A. V.: Monocyte differentiation upregulates 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(2006) (Pubitemid 44401779)
44. D'Azzo, A., Andria, G., Strisciuglio, G., Galjaard, H.: Galactosialidosis. In: Scriver, C. R., Beaudet, A. L., Sly, W. S., Valle, D. (eds.) The Metabolic and Molecular Bases of Inherited Disease, pp. 3811-3826. McGraw-Hill, New York (2001)
45. Bonten, E. J., Campos, Y., Zaitsev, V., Nourse, A., Waddell, B., Lewis, W., Taylor, G., D'Azzo, A.: Heterodimerization of the sialidase NEU1 with the chaperone protective protein/cathepsin A prevents its premature oligomerization. J. Biol. Chem. 284, 28430-28441(2009)
46. Michalski, J. C., Strecker, G., Fournet, B., Cantz, M., Spranger, J.: Structures of sialyl-oligosaccharides excreted in the urine of a patient with mucolipidosis I. FEBS Lett. 79, 101-104(1977) (Pubitemid 8163394)
47. Strecker, G., Peers, M. C., Michalski, J. C., Hondi-Assah, T., Fournet, B., Spik, G., Montreuil, J., Farriaux, J. P., Maroteaux, P., Durand, P.: Structure of nine sialyl-oligosaccharides accumulated in urine of eleven patients with three different types of sialidosis. Mucolipidosis II and two new types of mucolipidosis. Eur. J. Biochem. 72, 391-403(1977) (Pubitemid 8119167)
48. Dorland, L., Haverkamp, J., Viliegenthart, J. F., Strecker, G., Michalski, J. C., Fournet, B., Spik, G., Montreuil, J.: 360-MHz nuclear-magnetic-resonance spectroscopy of sialyloligosaccharides from patients with sialidosis (mucolipidosis I and II). Eur. J. Biochem. 87, 323-329(1978) (Pubitemid 8355174)
49. van Pelt, J., Kamerling, J. P., Vliegenthart, J. F. G., Verheijen, F. W., Galjaard, H.: Isolation and structural characterization fof sialic acid-containing storage material from mucolipidosis I (sialidosis) fibroblasts. Biochem. Biophys. Acta. 965, 36-45(1988) (Pubitemid 18099348)
50. Yoshino, H., Miyashita, K., Miyatani, N., Ariga, T., Hashimoto, Y., Tsuji, S., Oyanagi, K., Ohama, E., Ikuta, F., Suzuki, A., et al.: Abnormal glycosphingolipid metabolism in the nervous system of galactosialidosis. J. Neurol. Sci. 97, 53-65(1990) (Pubitemid 20190524)
51. Thomas, G. H.: Disorders of glycoprotein degradation: α-mannosidosis, β-mannosidosis, fucosidosis, and sialidosis. In: Scriver, C. R., Beaudet, A. L., Sly, W. S., Valle, D. (eds.) Metabolic and Molecular Bases of Inherited Disease, pp. 3507-3534. McGraw-Hill, New York (2001)
52. de Geest, N., Bonten, E., Mann, L., de Sousa-Hitzler, J., Hahn, C., D'Azzo, A.: Systemic and neurologic abnormalities distinguish the lysosomal disorders sialidosis and galactosialidosis in mice. Hum. Mol. Genet. 11, 1455-1464(2002)
53. Zhou, X. Y., Morreau, H., Rottier, R., Davis, D., Bonten, E., Gillemans, N., Wenger, D., Grosveld, F. G., Doherty, P., Suzuki, K., Grosveld, G. C., D'Azzo, A.: Mouse model for the lysosomal disorder galactosialidosis and correction of the phenotype with overexpressing erythroid precursor cells. Genes. Dev. 9, 2623-2634(1995)
54. Womack, J. E., Yan, D. L., Potier, M.: Gene for neuraminidase activity on mouse chromosome 17 near h-2: pleiotropic effects on multiple hydrolases. Science 212, 63-65(1981) (Pubitemid 11114681)
55. Carrillo, M. B., Milner, C. M., Ball, S. T., Snock, M., Campbell, R. D.: Cloning and characterization of a sialidase from the murine histocompatibility-2 complex: low levels of mRNA and a single amino acid mutation are responsible for reduced sialidase activity in mice carrying the Neu1a allele. Glycobiology 7, 975-986(1997)
56. Rottier, R. J., Bonten, E., D'Azzo, A.: A point mutation in the neu-1 locus causes the neuraminidase defect in the SM/J mouse. Hum. Mol. Genet. 7, 313-321(1998) (Pubitemid 28048548)
57. Champigny, M. J., Mitchell, M., Fox-Robichaud, A., Trigatti, B. L., Igdoura, S. A.: A point mutation in the neu1 promoter recruits an ectopic repressor, Nkx3.2 and results in a mouse model of sialidase deficiency. Mol. Genet. Metab. 97, 43-52(2009)
58. Stinchcombe, J., Bossi, G., Griffiths, G. M.: Linking albinism and immunity: the secrets of secretory lysosomes. Science 305, 55-59(2004) (Pubitemid 38869367)
59. Holt, O. J., Gallo, F., Griffiths, G. M.: Regulating secretory lysosomes. J. Biochem. 140, 7-12(2006) (Pubitemid 44433540)
60. Yogalingam, G., Bonten, E. J., van de Vlekkert, D., Hu, H., Moshiach, S., Connell, S. A., D'Azzo, A.: Neuraminidase 1 is a negative regulator of lysosomal exocytosis. Dev. Cell. 15, 74-86(2008) (Pubitemid 351895600)
61. Kima, P. E., Burleigh, B., Andrews, N. W.: Surface-targeted lysosomal membrane glycoprotein-1 (Lamp-1) enhances lysosome exocytosis and cell invasion by Trypanosoma cruzi. Cell. Microbiol. 2, 477-486(2000) (Pubitemid 32049319)
62. Wu, X., Steigelman, K. A., Bonten, E., Hu, H., He, W., Ren, T., Zuo, J., D'Azzo, A.: Vacuolization and alterations of lysosomal membrane proteins in cochlear marginal cells contribute to hearing loss in neuraminidase 1-deficient mice. Biochim. Biophys. Acta. 1802, 259-268(2010)
63. Andrejewski, N., Punnonen, E. L., Guhde, G., Tanaka, Y., Lüllmann-Rauch, R., Hartmann, D., von Figura, K., Saftig, P.: Normal lysosomal morphology and function in LAMP-1-deficient mice. J. Biol. Chem. 274, 12692-12701(1999)
64. Gaspar, E. B., Mortara, R. A., Andrade, L. O., da Silva, C. V.: Lysosomal exocytosis: an important event during invasion of lamp deficient cells by extracellular amastigotes of Trypanosoma cruzi. Biochem. Biophys. Res. Commun. 384, 265-269(2009)
65. Babal, P., Janega, P., Cerna, A., Kholova, I., Brabencova, E.: Neoplastic transformation of the thyroid gland is accompanied by changes in cellular sialylation. Acta Histochem. 108, 133-140(2006) (Pubitemid 43870308)
66. Berbec, H., Paszkowska, A., Siwek, B., Gradziel, K., Cybulski, M.: Total serum sialic acid concentration as a supporting marker of malignancy in ovarian neoplasia. Eur. J. Gynaecol. Oncol. 20, 389-392(1999)
67. Brooks, S. A., Leathem, A. J. C.: Expression of N-acetyl galactosaminylated and sialylated glycans by metastases arising from primary breast cancer. Invasion Metastasis 18, 115-121(1999) (Pubitemid 29414511)
68. Feijoo-Carnero, C., Rodriguez-Berrocal, F. J., de la Cadena, M. N., Ayude, D., de Carlos, A., Martinez-Zorzano, V. S.: Clinical significance of preoperative serum sialic acid levels in colorectal cancer: utility in the detection of patients at high risk of tumor recurrence. Int. J. Biol. Markers 19, 38-45(2004) (Pubitemid 38515010)
69. Basoglu, M., Yildirgan, M. I., Taysi, S., Yilmaz, I., Kiziltunc, A., Balik, A. A., Celebi, F., Atamanalp, S. S.: Levels of soluble intercellular adhesion molecule-1 and total sialic acid in serum of patients with colorectal cancer. J. Surg. Oncol. 83, 180-184(2003) (Pubitemid 36807949)
70. Rajpura, K. B., Patel, P. S., Chawda, J. G., Shah, R. M.: Clinical significance of total and lipid bound sialic acid levels in oral precancerous conditions and oral cancer. J. Oral Pathol. Med. 34, 263-267(2005) (Pubitemid 40524965)
71. Romppanen, J., Haapalainen, T., Punonen, K., Penttila, I.: Serum sialic acid and prostate-specific antigen in differential diagnosis of benign prostate hyperplasia and prostate cancer. Anticancer Res. 22, 415-420(2002) (Pubitemid 34475332)
72. Uslu, C., Taysi, S., Akcay, F., Sutbeyaz, M. Y., Bakan, N.: Serum free and bound sialic acid and α-1-acid glycoprotein in patients with laryngeal cancer. Ann. Clin. Lab. Sci. 33, 156-159(2003) (Pubitemid 36705925)
73. Lijima, S., Shiba, K., Kimura, M., Nagai, K., Iwai, T.: Changes of α1-acid glycoprotein microheterogeneity in acute inflammation stages analyzed by isoelectric focusing using serum obtained postoperatively. Electrophoresis 21, 753-759(2000) (Pubitemid 30163399)
74. Herve, F., Duche, J. C., Jaurand, M. C.: Changes in expression and microheterogeneity of the genetic variants of human α1-acid glycoprotein in malignant mesothelioma. J. Chromatogr. B 715, 111-123(1998) (Pubitemid 28403604)
75. Miyagi, T., Wada, T., Yamaguchi, K., Hata, K.: Sialidase and malignancy: a minireview. Glycoconj. J. 20, 189-198(2004) (Pubitemid 39024047)
76. Miyagi, T.: Aberrant expression of sialidase and cancer progression. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 84, 407-418(2008)
77. Miyagi, T., Sato, K., Hata, K., Taniguchi, S.: Metastatic potential of transformed rat 3Y1 cell lines is inversely correlated with lysosomal-type sialidase activity. FEBS Lett. 349, 255-259(1994) (Pubitemid 24263273)
78. Sawada, M., Moriya, S., Saito, S., Shineha, R., Satomi, S., Yamori, T., Tsuruo, T., Kannagi, R., Miyagi, T.: Reduced sialidase expression in highly metastatic variants of mouse colon adenocarcinoma 26 and retardation of their metastatic ability by sialidase overexpression. Int. J. Cancer 97, 180-185(2002) (Pubitemid 34019953)
79. Kato, T., Wang, Y., Yamaguchi, K., Milner, C. M., Shineha, R., Satomi, S., Miyagi, T.: Overexpressing 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(2001) (Pubitemid 32467367)
80. Uemura, T., Shiozaki, K., Yamaguchi, K., Miyazaki, S., Satomi, S., Kato, K., Sakuraba, H., Miyagi, T.: Contribution of sialidase NEU1 to suppression of metastasis of human colon cancer cells through desialylation of integrin beta4. Oncogene 28, 1218-1229(2009)
81. Frohman, M., Cowing, C.: Presentation of antigen by B cells: functional dependence on radiation dose, interleukins, cellular activation, and differential glycosylation. J. Immunol. 134, 2269-2275(1985) (Pubitemid 15106988)
82. Kearse, K. P., Cassatt, D. R., Kaplan, A. M., Cohen, D. A.: The requirement for surface Ig signaling as a prerequisite for T cell:B cell interactions. A possible role for desialylation. J. Immunol. 140, 1770-1778(1988)
83. Krieger, J., Jenis, D. M., Chesnut, R. W., Grey, H. M.: Studies on the capacity of intact cells and purified Ia from different B cell sources to function in antigen presentation to T cells. J. Immunol. 140, 388-394(1988)
84. Baum, L. G., Derbin, K., Perillo, N. L., Wu, T., Pang, M., Uittenbogaart, C.: Characterization of terminal sialic acid linkages on human thymocytes. Correlation between lectin-binding phenotype and sialyltransferase expression. J. Biol. Chem. 271, 10793-10799(1996) (Pubitemid 26145817)
85. Bagriaçik, E. U., Miller, K. S.: Cell surface sialic acid and the regulation of immune cell interactions: the neuraminidase effect reconsidered. Glycobiology 9, 267-275(1999) (Pubitemid 29099712)
86. Watanabe, Y., Shiratsuchi, A., Shimizu, K., Takizawa, T., Nakanishi, Y.: Stimulation of phagocytosis of influenza virusinfected cells through surface desialylation of macrophages by viral neuraminidase. Microbiol. Immunol. 48, 875-881(2004) (Pubitemid 39602044)
87. Landolfi, N. F., Cook, R. G.: Activated T lymphocytes express class I molecules which are hyposialylated compared to other lymphocyte populations. Mol. Immunol. 23, 297-309(1986) (Pubitemid 16128893)
88. Chen, X. P., Enioutina, E. Y., Daynes, R. A.: The control of IL-4 gene expression in activated murine T lymphocytes: a novel role for neu-1 sialidase. J. Immunol. 158, 3070-3080(1997) (Pubitemid 127484019)
89. Chen, X. P., Ding, X., Daynes, R. A.: Ganglioside control over IL-4 priming and cytokine production in activated T cells. Cytokine 12, 972-985(2000) (Pubitemid 30479479)
90. Yamamoto, N., Kumashiro, R.: Conversion of vitamin D3 binding protein (group-specific component) to a macrophage activating factor by the stepwise action of beta-galactosidase of B cells and sialidase of T cells. J. Immunol. 151, 2794-2802(1993) (Pubitemid 23264531)
91. Naraparaju, V. R., Yamamoto, N.: Roles of beta-galactosidase of B lymphocytes and sialidase of T lymphocytes in inflammationprimed activation of macrophages. Immunol. Lett. 43, 143-148(1994)
92. Landolfi, N. F., Leone, J., Womack, J. E., Cook, R. G.: Activation of T lymphocytes results in an increase in H-2-encoded neuraminidase. Immunogenetics 22, 159-167(1985) (Pubitemid 15000619)
93. Nan, X., Carubelli, I., Stamatos, N. M.: Sialidase expression in activated human T lymphocytes influences production of IFN-gamma. J. Leukoc. Biol. 81, 284-296(2007) (Pubitemid 46021278)
94. Stamatos, N. M., Liang, F., Nan, X., Landry, K., Cross, A. S., Wang, L. X., Pshezhetsky, A. V.: Differential expression of endogenous sialidases of human monocytes during cellular differentiation into macrophages. FEBS J. 272, 2545-2556(2005) (Pubitemid 40705074)
95. Seyrantepe, V., Hinek, A., Peng, J., Fedjaev, M., Ernest, S., Kadota, Y., Canuel, M., Itoh, K., Morales, C. R., Lavoie, J., Tremblay, J., Pshezhetsky, A. V.: Circulation 117, 1973-1981(2008)
96. Seyrantepe, V., Iannello, A., Liang, F., Kanshin, E., Jayanth, P., Samarani, S., Szewczuk, M. R., Ahmad, A., Pshezhetsky, A. V.: Regulation of phagocytosis in macrophages by neuraminidase 1. J. Biol. Chem. 285, 206-215(2010)
97. Amith, S. R., Jayanth, P., Franchuk, S., Siddiqui, S., Seyrantepe, V., Gee, K., Basta, S., Beyaert, R., Pshezhetsky, A. V., Szewczuk, M. R.: Dependence of pathogen molecule-induced toll-like receptor activation and cell function on Neu1 sialidase. Glycoconj. J. 26, 1197-1212(2009)
98. Amith, S. R., Jayanth, P., Franchuk, S., Finlay, T., Seyrantepe, V., Beyaert, R., Pshezhetsky, A. V., Szewczuk, M. R.: Neu1 desialylation of sialyl alpha-2, 3-linked beta-galactosyl residues of TOLL-like receptor 4 is essential for receptor activation and cellular signaling. Cell. Signal. 22, 314-324(2010)
99. Hata, K., Koseki, K., Yamaguchi, K., Moriya, S., Suzuki, Y., Yingsakmongkon, S., Hirai, G., Sodeoka, M., von Itzstein, M., Miyagi, T.: Limited inhibitory effects of oseltamivir and zanamivir on human sialidases. Antimicrob. Agents Chemother. 52, 3484-3491(2008)
100. Jayanth, P., Amith, S. R., Gee, K., Szewczuk, M. R.: Neu1 sialidase and matrix metalloproteinase-9 cross-talk is essential for neurotrophin activation of Trk receptors and cellular signaling. Cell. Signal. 22, 1193-1205(2010)
101. Stamatos, N. M., Carubelli, I., van de Vlekkert, D., Bonten, E. J., Papini, N., Feng, C., Venerando, B., D'Azzo, A., Cross, A. S., Wang, L. X., Gomatos, P. J.: LPS-induced cytokine production in human dendritic cells is regulated by sialidase activity. J. Leukoc. Biol. 88, 1227-1239(2010)
102. Gross, N., Balmas, K., Beretta Brognara, C: Role of CD44H carbohydrate structure in neuroblastoma adhesive properties. Med. Pediatr. Oncol. 36, 139-141(2001)
103. Nightingale, T. D., Frayne, M. E., Clasper, S., Banerji, S., Jackson, D. G: A mechanism of sialylation functionally silences the hyaluronan receptor LYVE-1 in lymphatic endothelium. J. Biol. Chem. 284, 3935-3945(2009)
104. Katoh, S., Maeda, S., Fukuoka, H., Wada, T., Moriya, S., Mori, A., Yamaguchi, K., Senda, S., Miyagi, T.: A crucial role of sialidase Neu1 in hyaluronan receptor function of CD44 in T helper type 2-mediated airway inflammation of murine acute asthmatic model. Clin. Exp. Immunol. 161, 233-241(2010)
105. Morreau, H., Galjart, N. J., Gillemans, N., Willemsen, R., van der Horst, G. T., D'Azzo, A.: Alternative splicing of 3'-Galactosidase mRNA generates the classic lysosomal enzyme and a related protein 3-Galactosidase. J. Biol. Chem. 264, 20655-20663(1989) (Pubitemid 20009263)
106. Hinek, A., Wrenn, D. S., Mecham, R. P., Barondes, S. H.: The elastin receptor: a galactoside-binding protein. Science 239, 1539-1541(1988)
107. Hinek, A., Rabinovitch, M., Keeley, F., Okamura, O. Y., Callahan, J. W.: The 67 kD elastin/laminin-binding protein is related to an alternatively spliced β-galactosidase. J. Clin. Invest. 91, 1198-1205(1993) (Pubitemid 23095299)
108. Hinek, A.: Nature and multiple functions of the 67 kD elastin/laminin binding protein. Cell Adhes. Commun. 2, 185-193(1994) (Pubitemid 24282665)
109. Privitera, S., Prody, C. A., Callahan, J. W., Hinek, A.: The 67-kDa enzymatically inactive alternatively spliced variant of β-galactosidase is identical to the elastin/laminin-binding protein. J. Biol. Chem. 273, 6319-6326(1998) (Pubitemid 28144722)
110. Hinek, A., Pshezhetsky, A. V., von Itzstein, M., Starcher, B.: Lysosomal sialidase (neuraminidase-1) is targeted to the cell surface in a multiprotein complex that facilitates elastic fiber assembly. J. Biol. Chem. 281, 3698-3710(2006) (Pubitemid 43845988)
111. Hinek, A., Smith, A. C., Cutiongco, E. M., Callahan, J. W., Gripp, K. W., Weksberg, R.: Decreased elastin deposition and high proliferation of fibroblasts from Costello syndrome are related to functional deficiency in the 67-kD elastin-binding protein. Am. J. Hum. Genet. 66, 859-872(2000) (Pubitemid 30470489)
112. Caciotti, A., Donati, M. A., Bardelli, T., D'Azzo, A., Massai, G., Luciani, L., Zammarchi, E., Morrone, A.: Primary and secondary elastin-binding protein defect leads to impaired elastogenesis in fibroblasts from GM1-gangliosidosis patients. Am. J. Pathol. 167, 1689-1698(2005) (Pubitemid 41713320)
113. Factor, S. M., Biempica, L., Goldfischer, S.: Coronary intimal sclerosis in Morquio's syndrome. Virchows Arch. A Pathol. Anat. Histol. 379, 1-10(1978) (Pubitemid 8396516)
114. Dangel, J. H.: Cardiovascular changes in children with mucopolysaccharide storage diseases and related disorders-clinical and echocardiographic findings in 64 patients. Eur. J. Pediatr. 157, 534-538(1998) (Pubitemid 28311476)
115. Guertl, B., Noehammer, C., Hoefler, G.: Metabolic cardiomyopathies. Int. J. Exp. Pathol. 81, 349-372(2000) (Pubitemid 32291178)
116. Starcher, B., D'Azzo, A., Keller, P. W., Rao, G. K., Nadarajah, D., Hinek, A.: Neuraminidase-1 is required for the normal assembly of elastic fibers. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L637-L647(2008)
117. Hinek, A., Bodnaruk, T. D., Bunda, S., Wang, Y., Liu, K.: 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-II. Am. J. Pathol. 173, 1042-1056(2008)
118. Myllarniemi, M., Calderon, L., Lemstrom, K., Buchdunger, E., Hayry, P.: Inhibition of platelet-derived growth factor receptor tyrosine kinase inhibits vascular smooth muscle cell migration and proliferation. FASEB J. 11, 1119-1126(1997) (Pubitemid 27481435)
119. Bayes-Genis, A., Conover, C. A., Schwartz, R. S.: The insulin-like growth factor axis: A review of atherosclerosis and restenosis. Circ. Res. 86, 125-130(2000) (Pubitemid 30086171)
120. Zaina, S., Pettersson, L., Ahren, B., Branen, L., Hassan, A. B., Lindholm, M., Mattsson, R., Thyberg, J., Nilsson, J.: Insulin-like growth factor II plays a central role in atherosclerosis mouse model. J. Biol. Chem. 277, 4504-4511(2002)
121. Zaina, S., Nilsson, J.: Insulin-like growth factor II and its receptors in atherosclerosis and in conditions predisposing to atherosclerosis. Curr. Opin. Lipidol. 14, 483-489(2003) (Pubitemid 37297303)
122. Tallquist, M., Kazlauskas, A.: PDGF signaling in cells and mice. Cytokine Growth Factor Rev. 15, 205-213(2004) (Pubitemid 38781046)
123. Arabkhari, M., Bunda, S., Wang, Y., Wang, A., Pshezhetsky, A. V., Hinek, A.: Desialylation of insulin receptors and IGF-1 receptors by neuraminidase-1 controls the net proliferative response of L6 myoblasts to insulin. Glycobiology 20, 603-616(2010)
124. Champigny, M. J., Perry, R., Rudnicki, M., Igdoura, S. A.: Overexpression of MyoD-inducible lysosomal sialidase (neu1) inhibits myogenesis in C2C12 cells. Exp. Cell Res. 311, 157-166(2005) (Pubitemid 41528794)
125. Zanoteli, E., van de Vlekkert, D., Bonten, E. J., Hu, H., Mann, L., Gomero, E. M., Harris, A. J., Ghersi, G., D'Azzo, A.: Muscle degeneration in neuraminidase 1-deficient mice results from infiltration of the muscle fibers by expanded connective tissue. Biochim. Biophys. Acta 1802, 659-672(2010)