Cloning, expression, and characterization of an alternatively spliced variant of human heparanase

Biochemical and Biophysical Research Communications

Volumn 354, Issue 1, 2007, Pages 33-38

  Nasser, Nicola J ^a,b   Avivi, Aaron ^a   Shushy, Moran ^b   Vlodavsky, Israel ^b   Nevo, Eviatar ^a  

^a UNIVERSITY OF HAIFA   (Israel)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Alternative splicing; Extracellular matrix; Heparan sulfate; Heparanase

Indexed keywords

COMPLEMENTARY DNA; ENZYME VARIANT; HEPARANASE;

ALTERNATIVE RNA SPLICING; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME DEGRADATION; ENZYME LOCALIZATION; EXON; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN VARIANT; SEQUENCE ANALYSIS; TUMOR CELL CULTURE;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; CLONING, MOLECULAR; GENETIC VARIATION; GLIOMA; GLUCURONIDASE; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION;

EID: 33846280793     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2006.12.189     Document Type: Article

References (32)

1. Kjellen L., and Lindahl U. Proteoglycans: structures and interactions. Annu. Rev. Biochem. 60 (1991) 443-475
2. Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., and Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68 (1999) 729-777
3. Iozzo R.V. Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67 (1998) 609-652
4. Vlodavsky I., Friedmann Y., Elkin M., Aingorn H., Atzmon R., Ishai-Michaeli R., Bitan M., Pappo O., Peretz T., Michal I., Spector L., and Pecker I. Mammalian heparanase: gene cloning, expression and function in tumor progression and metastasis. Nat. Med. 5 (1999) 793-802
5. Hulett M.D., Freeman C., Hamdorf B.J., Baker R.T., Harris M.J., and Parish C.R. Cloning of mammalian heparanase, an important enzyme in tumor invasion and metastasis. Nat. Med. 5 (1999) 803-809
6. Kussie P.H., Hulmes J.D., Ludwig D.L., Patel S., Navarro E.C., Seddon A.P., Giorgio N.A., and Bohlen P. Cloning and functional expression of a human heparanase gene. Biochem. Biophys. Res. Commun. 261 (1999) 183-187
7. Toyoshima M., and Nakajima M. Human heparanase. Purification, characterization, cloning, and expression. J. Biol. Chem. 274 (1999) 24153-24160
8. Nasser N.J., Nevo E., Shafat I., Ilan N., Vlodavsky I., and Avivi A. Adaptive evolution of heparanase in hypoxia-tolerant Spalax: gene cloning and identification of a unique splice variant. Proc. Natl. Acad. Sci. USA 102 (2005) 15161-15166
9. Ast G. How did alternative splicing evolve?. Nat. Rev. Genet. 5 (2004) 773-782
10. Ast G. The alternative genome. Sci. Am. 292 (2005) 40-77
11. Goldshmidt O., Zcharia E., Aingorn H., Guatta-Rangini Z., Atzmon R., Michal I., Pecker I., Mitrani E., and Vlodavsky I. Expression pattern and secretion of human and chicken heparanase are determined by their signal peptide sequence. J. Biol. Chem. 276 (2001) 29178-29187
12. Zetser A., Levy-Adam F., Kaplan V., Gingis-Velitski S., Bashenko Y., Schubert S., Flugelman M.Y., Vlodavsky I., and Ilan N. Processing and activation of latent heparanase occurs in lysosomes. J. Cell Sci. 117 (2004) 2249-2258
13. Zetser A., Bashenko Y., Edovitsky E., Levy-Adam F., Vlodavsky I., and Ilan N. Heparanase induces vascular endothelial growth factor expression: correlation with p38 phosphorylation levels and Src activation. Cancer Res. 66 (2006) 1455-1463
14. Levy-Adam F., Abboud-Jarrous G., Guerrini M., Beccati D., Vlodavsky I., and Ilan N. Identification and characterization of heparin/heparan sulfate binding domains of the endoglycosidase heparanase. J. Biol. Chem. 280 (2005) 20457-20466
15. Kelly T., Suva L.J., Huang Y., Macleod V., Miao H.Q., Walker R.C., and Sanderson R.D. Expression of heparanase by primary breast tumors promotes bone resorption in the absence of detectable bone metastases. Cancer Res. 65 (2005) 5778-5784
16. Vlodavsky I., Fuks Z., Bar-Ner M., Ariav Y., and Schirrmacher V. Lymphoma cell-mediated degradation of sulfated proteoglycans in the subendothelial extracellular matrix: relationship to tumor cell metastasis. Cancer Res. 43 (1983) 2704-2711
17. Goldshmidt O., Nadav L., Aingorn H., Irit C., Feinstein N., Ilan N., Zamir E., Geiger B., Vlodavsky I., and Katz B.Z. Human heparanase is localized within lysosomes in a stable form. Exp. Cell Res. 281 (2002) 50-62
18. Brett D., Pospisil H., Valcarcel J., Reich J., and Bork P. Alternative splicing and genome complexity. Nat. Genet. 30 (2002) 29-30
19. Boue S., Letunic I., and Bork P. Alternative splicing and evolution. Bioessays 25 (2003) 1031-1034
20. Modrek B., and Lee C. A genomic view of alternative splicing. Nat. Genet. 30 (2002) 13-19
21. Modrek B., Resch A., Grasso C., and Lee C. Genome-wide detection of alternative splicing in expressed sequences of human genes. Nucleic Acids Res. 29 (2001) 2850-2859
22. Magen A., and Ast G. The importance of being divisible by three in alternative splicing. Nucleic Acids Res. 33 (2005) 5574-5582
23. Carmel I., Tal S., Vig I., and Ast G. Comparative analysis detects dependencies among the 5′ splice-site positions. RNA 10 (2004) 828-840
24. Kondrashov F.A., and Koonin E.V. Evolution of alternative splicing: deletions, insertions and origin of functional parts of proteins from intron sequences. Trends Genet. 19 (2003) 115-119
25. Pagani F., and Baralle F.E. Genomic variants in exons and introns: identifying the splicing spoilers. Nat. Rev. Genet. 5 (2004) 389-396
26. Cartegni L., Chew S.L., and Krainer A.R. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat. Rev. Genet. 3 (2002) 285-298
27. Baek D., and Green P. Sequence conservation, relative isoform frequencies, and nonsense-mediated decay in evolutionarily conserved alternative splicing. Proc. Natl. Acad. Sci. USA 102 (2005) 12813-12818
28. Dong J., Kukula A.K., Toyoshima M., and Nakajima M. Genomic organization and chromosome localization of the newly identified human heparanase gene. Gene 253 (2000) 171-178
29. Abboud-Jarrous G., Rangini-Guetta Z., Aingorn H., Atzmon R., Elgavish S., Peretz T., and Vlodavsky I. Site-directed mutagenesis, proteolytic cleavage, and activation of human proheparanase. J. Biol. Chem. 280 (2005) 13568-13575
30. Hashimoto Y., Kondo C., Kojima T., Nagata H., Moriyama A., Hayakawa T., and Katunuma N. Significance of 32-kDa cathepsin L secreted from cancer cells. Cancer Biother. Radiopharm. 21 (2006) 217-224
31. Klose A., Zigrino P., Dennhofer R., Mauch C., and Hunzelmann N. Identification and discrimination of extracellularly active cathepsins B and L in high-invasive melanoma cells. Anal. Biochem. 353 (2006) 57-62
32. Gingis-Velitski S., Zetser A., Flugelman M.Y., Vlodavsky I., and Ilan N. Heparanase induces endothelial cell migration via protein kinase B/Akt activation. J. Biol. Chem. 279 (2004) 23536-23541