A proline-rich loop mediates specific functions of human sialidase NEU4 in SK-N-BE neuronal differentiation

Glycobiology

Volumn 23, Issue 12, 2013, Pages 1499-1509

  Bigi, Alessandra ^b   Tringali, Cristina ^c,d   Forcella, Matilde ^b   Mozzi, Alessandra ^b   Venerando, Bruno ^c,d   Monti, Eugenio ^e   Fusi, Paola ^a,b  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c IRCCS POLICLINICO SAN DONATO   (Italy)

^d UNIVERSITY OF BRESCIA   (Italy)

^e EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

Akt signaling pathway; NEU4; Neuronal differentiation; Proline rich region; Sialidase

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROLINE; PROTEIN KINASE B; RETINOIC ACID; SIALIDASE; SIALIDASE NEU4 ENZYME; UNCLASSIFIED DRUG; NEU4 PROTEIN, HUMAN;

AMINO ACID SEQUENCE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DELETION MUTANT; HUMAN; MOLECULAR MODEL; NERVE CELL DIFFERENTIATION; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; CELL DIFFERENTIATION; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; METABOLISM; NEUROBLASTOMA; PATHOLOGY; TUMOR CELL CULTURE;

CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; MODELS, MOLECULAR; NEURAMINIDASE; NEUROBLASTOMA; PROLINE; TRETINOIN; TUMOR CELLS, CULTURED;

EID: 84887889225     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwt078     Document Type: Article

References (41)

1. Bigi A, Morosi L, Pozzi C., Forcella M, Tettamanti G, Venerando B., Monti E, Fusi P. 2010. Human sialidase NEU4 long and short are extrinsic proteins bound to outer mitochondrial membrane and the endoplasmic reticulum, respectively. Glycobiology. 20:148-157.
2. Blouin C, Butt D, Roger AJ 2004. Rapid evolution in conformational space: A study of loop regions in a ubiquitous GTP binding domain. Protein Sci. 13:608-616.
3. 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.
4. Castro-Palomino J.C., Simon B, Speer O., Leist M, Schmidt RR 2001. Synthesis of ganglioside GD3 and its comparison with bovine GD3 with regard to oligodendrocyte apoptosis mitochondrial damage. Chemistry. 7:2178-2184.
5. 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.
6. Comelli EM, Amado M, Lustig S.R., Paulson JC 2003. Identification and expression of Neu4, a novel murine sialidase. Gene. 321:155-161.
7. Da Silva J.S., Hasegawa T, Miyagi T., Dotti CG, Abad-Rodriguez J. 2005. Asymmetric membrane ganglioside sialidase activity specifies axonal fate. Nat Neurosci. 8:606-615.
8. De Maria R., Lenti L, Malisan F., d'Agostino F, Tomassini B, Zeuner A., Rippo MR, Testi R. 1997. Requirement for GD3 ganglioside in CD95- and ceramide-induced apoptosis. Science. 277:1652-1655.
9. Ellman GL, Courtney KD, Andres V, Jr, Feather-Stone RM. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol. 7:88-95.
10. Finlay TM, Abdulkhalek S, Gilmour A., Guzzo C, Jayanth P, Amith S.R., Gee K., Beyaert R, Szewczuk MR 2010. Thymoquinone-induced Neu4 sialidase activates NFkappaB in macrophage cells and pro-inflammatory cytokines in vivo. Glycoconj J. 27:583-600.
11. Finlay TM, Jayanth P, Amith S.R., Gilmour A., Guzzo C, Gee K, Beyaert R., Szewczuk MR 2010. Thymoquinone from nutraceutical black cumin oil activates Neu4 sialidase in live macrophage, dendritic, and normal and type I sialidosis human fibroblast cells via GPCR Galphai proteins and matrix metalloproteinase-9. Glycoconj J. 27:329-348.
12. Fuster MM, Esko JD 2005. The sweet and sour of cancer: Glycans as novel therapeutic targets. Nat Rev Cancer. 5:526-542.
13. Giacopuzzi E, Barlati S, Preti A., Venerando B, Monti E, Borsani G., Bresciani R. 2011. Gallus gallus NEU3 sialidase as model to study protein evolution mechanism based on rapid evolving loops. BMC Biochemistry. 12:1-15.
14. Giacopuzzi E, Bresciani R, Schauer R., Monti E, Borsani G. 2012. New insights on the sialidase protein family revealed by a phylogenetic analysis in metazoa. PLoS One. 7:e44193.
15. Gu W, Helms V. 2005. Dynamical binding of proline-rich peptides to their recognition domains. Biochim Biophys Acta. 1754:232-238.
16. Hasegawa T, Sugeno N, Takeda A., Matsuzaki-Kobayashi M, Kikuchi A, Furukawa K., Miyagi T, Itoyama Y. 2007. Role of Neu4L sialidase and its substrate ganglioside GD3 in neuronal apoptosis induced by catechol metabolites. FEBS Lett. 581:406-412.
17. Hasegawa T, Yamaguchi K, Wada T., Takeda A, Itoyama Y, Miyagi T. 2000. Molecular cloning of mouse ganglioside sialidase and its increased expression in Neuro2a cell differentiation. J Biol Chem. 275:8007-8015.
18. Jiang H, Blouin C. 2007. Insertions and the emergence of novel protein structure: A structure-based phylogenetic study of insertions. BMC Bioinformatics. 8:444.
19. Layer PG. 1990. Cholinesterases preceding major tracts in vertebrate neurogen-esis. Bioessays. 12:415-420.
20. Lopez-Carballo G., Moreno L, Masia S., Perez P, Barettino D. 2002. Activation of the phosphatidylinositol 3-kinase/Akt signaling pathway by retinoic acid is required for neural differentiation of SH-SY5Y human neuroblastoma cells. J Biol Chem. 277:25297-25304.
21. Malisan F, Testi R. 2002. GD3 Ganglioside and apoptosis. Biochim Biophys Acta. 1585:179-187.
22. Masia S, Alvarez S, de Lera AR, Barettino D. 2007. Rapid, nongenomic actions of retinoic acid on phosphatidylinositol-3-kinase signaling pathway mediated by the retinoic acid receptor. Mol Endocrinol. 21:2391-2402.
23. Monti E, Bassi MT, Bresciani R, Civini S., Croci GL, Papini N, Riboni M, Zanchetti G., Ballabio A, Preti A, et al 2004. Molecular cloning and characterization of NEU4, the fourth member of the human sialidase gene family. Genomics. 83:445-453.
24. Nakamura Y, Ozaki T, Ichimiya S., Nakagawara A, Sakiyama S. 1998. Ectopic expression of DAN enhances the retinoic acid-induced neuronal differentiation in human neuroblastoma cell lines. Biochem Biophys Res Commun. 243:722-726.
25. Pawson T, Nash P. 2003. Assembly of cell regulatory systems through protein interaction domains. Science. 300:445-452.
26. Pawson T, Scott JD 1997. Signaling through scaffold, anchoring, and adaptor proteins. Science. 278:2075-2080.
27. Proshin S, Yamaguchi K, Wada T., Miyagi T. 2002. Modulation of neuritogen-esis by ganglioside-specific sialidase (Neu 3) in human neuroblastoma NB-1 cells. Neurochem Res. 27:841-846.
28. Rodriguez JA, Piddini E, Hasegawa T., Miyagi T, Dotti CG 2001. Plasma membrane ganglioside sialidase regulates axonal growth and regeneration in hip-pocampal neurons in culture. J Neurosci. 21:8387-8395.
29. Schwab M. 1994. Human neuroblastoma: Amplification of the N-myc onco-gene and loss of a putative cancer-preventing gene on chromosome 1p. Recent Results Cancer Res. 135:7-16.
30. Schwab M, Varmus HE, Bishop JM 1985. Human N-myc gene contributes to neoplastic transformation of mammalian cells in culture. Nature. 316:160-162.
31. Shiozaki K, Koseki K, Yamaguchi K., Shiozaki M, Narimatsu H, Miyagi T. 2009. Developmental change of sialidase neu4 expression in murine brain and its involvement in the regulation of neuronal cell differentiation. J Biol Chem. 284:21157-21164.
32. Shiozaki K, Yamaguchi K, Takahashi K., Moriya S, Miyagi T. 2011. Regulation of sialyl lewis antigen expression in colon cancer cells by sialidase NEU4. J Biol Chem. 286:21052-21061.
33. Soding J, Biegert A, Lupas AN 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33: W244-W248.
34. Songyang Z. 1999. Recognition and regulation of primary-sequence motifs by signaling modular domains. Prog Biophys Mol Biol. 71:359-372.
35. Takahashi K, Mitoma J, Hosono M., Shiozaki K, Sato C, Yamaguchi K., Kitajima K, Higashi H, Nitta K., Shima H, et al 2012. Sialidase NEU4 hydrolyzes polysialic acids of neural cell adhesion molecules and negatively regulates neurite formation by hippocampal neurons. J Biol Chem. 287:14816-14826.
36. Taylor G. 1996. Sialidases: Structures, biological significance and therapeutic potential. Curr Opin Struct Biol. 6:830-837.
37. Tringali C, Cirillo F, Lamorte G., Papini N, Anastasia L, Lupo B., Silvestri I, Tettamanti G, Venerando B. 2012. NEU4L sialidase overexpression promotes beta-catenin signaling in neuroblastoma cells, enhancing stem-like malignant cell growth. Int J Cancer. 131:1768-1778.
38. Williamson MP. 1994. The structure and function of proline-rich regions in proteins. Biochem J. 297(Pt 2):249-260.
39. Yamaguchi K, Hata K, Koseki K., Shiozaki K, Akita H, Wada T., Moriya S, Miyagi T. 2005. Evidence for mitochondrial localization of a novel human sialidase (NEU4). Biochem J. 390:85-93.
40. Yamanami H, Shiozaki K, Wada T., Yamaguchi K, Uemura T, Kakugawa Y., Hujiya T, Miyagi T. 2007. Down-regulation of sialidase NEU4 may contribute to invasive properties of human colon cancers. Cancer Sci. 98:299-307.
41. Yanagisawa M, Yu RK 2007. The expression and functions of glycoconjugates in neural stem cells. Glycobiology. 17:57R-74R.