Structural requirements of human DNase IIα for formation of the active enzyme: The role of the signal peptide, N-glycosylation, and disulphide bridging

Biochemical Journal

Volumn 371, Issue 3, 2003, Pages 867-876

  MacLea, Kyle S ^a   Krieser, Ronald J ^a,b   Eastman, Alan ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Deoxyribonuclease II; DNase II ; DNase II like acid DNase (DLAD); DNASE2 gene; Endonuclease; NUC 1; Peptide N glycosidase (PNGase F)

Indexed keywords

BIOCHEMISTRY; CELLS; DNA; NITROGEN COMPOUNDS; POLYPEPTIDES;

OLIGONUCLEOTIDES;

ENZYMES;

CYSTEINE; DEOXYRIBONUCLEASE; DEOXYRIBONUCLEASE II; DEOXYRIBONUCLEASE II ALPHA; DEOXYRIBONUCLEASE II LIKE ACID DEOXYRIBONUCLEASE; DISULFIDE; ENDONUCLEASE; GLYCOSIDASE; HISTIDINE; MUTANT PROTEIN; N GLYCOSIDASE F; NUC 1 PEPTIDE; PEPTIDE; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; CYSTIC FIBROSIS; DISULFIDE BOND; DNA BINDING; DNA CLEAVAGE; DNASE2 GENE; EMBRYO; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; ENZYME STRUCTURE; ENZYME SYNTHESIS; GENE; GENETIC CONSERVATION; HUMAN; HUMAN CELL; MODEL; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; STRUCTURE ACTIVITY RELATION;

ANIMALS; BASE SEQUENCE; CELL LINE; DISULFIDES; DNA PRIMERS; ENDODEOXYRIBONUCLEASES; GLYCOSYLATION; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION;

ANIMALIA;

EID: 0037907759     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021875     Document Type: Article

References (44)

1. Catcheside, D. G. and Holmes, B. (1947) The action of enzymes on chromosomes. Symp. Soc. Exp. Biol. 1, 225-231
2. Bernardi, G., Appella, E. and Zito, R. (1965) Studies on acid deoxyribonuclease. III. Physical and chemical properties of hog spleen acid deoxyribonuclease. Biochemistry 4, 1725-1729
3. Bernardi, G. and Griffe, M. (1964) Studies on acid deoxyribonuclease. II. Isolation and characterization of spleen-acid deoxyribonuclease. Biochemistry 3, 1419-1426
4. Liao, T.-H., Liao, W.-C., Chang, H.-C. and Lu, K.-S. (1989) Deoxyribonuclease II purified from the isolated lysosomes of porcine spleen and from porcine liver homogenates. Comparison with deoxyribonuclease II purified from porcine spleen homogenates. Biochim. Biophys. Acta 1007, 15-22
5. Barry, M. A. and Eastman, A. (1993) Identification of deoxyribonudease II as an endonuclease involved in apoptosis. Arch. Biochem. Biophys. 300, 440-450
6. Yasuda, T., Nadano, D., Awazu, S. and Kishi, K. (1992) Human urine deoxyribonuclease II (DNase II) isoenzymes: a novel immunoaffinity purification, biochemical multiplicity, genetic heterogeneity and broad distribution among tissues and body fluids. Biochim. Biophys. Acta 1119, 185-193
7. Yasuda, T., Nadano, D., Sawazaki, K. and Kishi, K. (1992) Genetic polymorphism of human deoxyribonuclease II (DNase II): low activity levels in urine and leukocytes are due to an autosomal recessive allele. Ann. Hum. Genet. 56, 1-10
8. Yasuda, T., Sawazaki, K., Nadano, D., Takeshita, H., Nakanaga, M. and Kishi, K. (1993) Human seminal deoxyribonuclease I (BNase I): purification, enzymological and immunological characterization and origin. Clin. Chim. Acta 218, 5-16
9. Krieser, R. J., MacLea, K. S., Longnecker, D. S., Fields, J. L., Fiering, S. and Eastman, A. (2002) Deoxyribonuclease IIα is required for DNA digestion during the phagocytic phase of apoptosis and its loss causes perinatal lethality. Cell Death Differ. 9, 956-962
10. Kawane, K., Fukuyama, H., Kondoh, G., Takeda, J., Ohsawa, Y., Uchiyama, Y. and Nagata, S. (2001) Requirement of DNase II for definitive erythropoiesis in the mouse fetal liver. Science 292, 1546-1549
11. Liao, T.-H. (1985) The subunit structure and active site sequence of porcine spleen deoxyribonuclease. J. Biol. Chem. 260, 10708-10713
12. Oosthuizen, M. M. J., Myburgh, J. A. and Schabort, J. C. (1984) Lysosomal acid deoxyribonuclease from vervet monkey livers - I. Purification and physico-chemical characterization. Int. J. Biochem. 16, 1207-1215
13. Rajagopal, S. V. and Rao, K. S. (1992) Purification and properties of a deoxyribonuclease (acid DNase) from rat brain. Biochem. Arch. 8, 135-142
14. Lesca, P. (1976) Protein inhibitor of acid deoxyribonucleases Improved purification procedure and properties. J. Biol. Chem 251, 116-123
15. Torriglia, A., Perani, P., Brossas, J. Y., Chaudun, E., Treton, J., Courtois, Y. and Counis, M. F. (1998) L-DNase II, a molecule that links proteases and endonucleases in apoptosis, derives from the ubiquitous serpin leukocyte elastase inhibitor. Mol. Cell. Biol. 18, 3612-3619
16. Torriglia, A., Chaudun, E., Chany-Fournier, F., Jeanny, J., Courtois, Y. and Counis, M. (1995) Involvement of DNase II in nuclear degeneration during lens cell differentiation. J. Biol. Chem. 270, 28579-28585
17. Malferrari, G., Mazza, U., Tresoldi, C., Rovida, E., Nissim, M., Mirabella, M., Servidei, S. and Biunno, I. (1999) Molecular characterization of a novel endonuclease (Xib) and possible involvement in lysosomal glycogen storage disorders. Exp. Mol. Pathol. 66, 123-130
18. Shiokawa, D., Ohyama, H., Yamada, T., Takahashi, K. and Tanuma, S. (1994) Identification of an endonuclease responsible for apoptosis in rat thymocytes. Eur. J. Biochem. 226, 23-30
19. Tanuma, S. and Shiokawa, D. (1994) Multiple forms of nuclear deoxyribonuclease in rat thymocytes. Biochem. Biophys. Res. Commun. 203, 789-797
20. Krieser, R. J., MacLea, K. S., Park, J. P. and Eastman, A. (2001) The cloning, genomic structure, localization, and expression of human deoxyribonuclease IIβ. Gene 269, 205-216
21. Krieser, R. J. and Eastman, A. (1998) The cloning and expression of human deoxyribonuclease II: a possible role in apoptosis. J. Biol. Chem. 273, 30909-30914
22. Krieser, R. J. and Eastman, A. (2000) Deoxyribonuclease II: structure and chromosomal localization of the murine gene, and comparison with the genomic structure of the human and three C. elegans homologs. Gene 252, 155-162
23. MacLea, K. S., Krieser, R. J. and Eastman, A. (2003) A family history of deoxyribonuclease II: surprises from Trichinella spiralis and Burkholderia pseudomallei. Gene, in the press
24. Wang, C. C., Lu, S. C., Chen, H. L. and Liao, T. H. (1998) Porcine spleen deoxyribonuclease II. Covalent structure, cDNA sequence, molecular cloning, and gene expression. J. Biol. Chem. 273, 17192-17198
25. Takeshita, H., Yasuda, T., Iida, R., Nakajima, T., Hosomi, O., Nakashima, Y., Mori, S., Nomoto, H. and Kishi, K. (1998) Identification of the three non-identical subunits constituting human deoxyribonuclease II. FEBS Lett. 440, 239-242
26. MacLea, K. S., Krieser, R. J. and Eastman, A. (2002) Revised structure of the active form of human deoxyribonuclease IIα. Biochem. Biophys. Res. Commun. 292, 415-421
27. Eastman, A. and Krieser, R. (2001) Deoxyribonuclease II proteins and cDNAs. U.S. Pat. 6,184,034
28. Shak, S., Capon, D. J., Hellmiss, R., Marsters, S. A. and Baker, C. L. (1990) Recombinant human DNase I reduces the viscosity of cystoic fibrosis sputum. Proc. Natl. Acad. Sci U.S.A. 87, 9188-9192
29. Chou, S. F., Chen, H. L. and Lu, S. C. (2002) Up-regulation of human deoxyribonuclease II gene expression during myelomonocytic differentiation of HL-60 and THP-1 cells. Biochem. Biophys. Res. Commun. 296, 48-53
30. Yasuda, T., Takeshita, H., Nakazato, E., Nakajima, T., Hosomi, O., Nakashima, Y. and Kishi, K. (1998) Activity measurement for deoxyribonucleases I and II with picogram sensitivity based on DNA/SYBR Green I fluorescence. Anal. Biochem. 255, 274-276
31. Sakahira, H., Takemura, Y. and Nagata, S. (2001) Enzymatic active site of caspase-activated DNase (CAD) and its inhibition by inhibitor of CAD. Arch. Biochem. Biophys. 388, 91-99
32. Marshall, R. D. (1972) Glycoproteins. Annu. Rev. Biochem. 41, 673-702
33. Miletich, J. P. and Broze, Jr, G. J. (1990) β Protein C is not glycosylated at asparagine 329. The rate of translation may influence the frequency of usage at asparagine-X-cysteine sites. J. Biol. Chem. 265, 11397-11404
34. Bause, E. (1983) Structural requirements of N-glycosylation of proteins. Studies with proline peptides as conformational probes. Biochem. J. 209, 331-336
35. von Heijne, G. (1990) The signal peptide. J. Membr. Biol. 115, 195-201
36. Nielsen, H., Engelbrecht, J., Brunak, S. and von Heijne, G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10, 1-6
37. Yasuda, T., Takeshita, H., Iida, R., Nakajima, T., Hosomi, O., Nakashima, Y., Mori, S. and Kishi, K. (1999) Structural requirements of a human deoxyribonuclease II for the development of the active enzyme form, revealed by site-directed mutagenesis. Biochem. Biophys. Res. Commun. 256, 591-594
38. Shiokawa, D. and Tanuma, S. I. (1998) Cloning of cDNAs encoding porcine and human DNase II. Biochem. Biophys. Res. Commun. 247, 864-869
39. Shiokawa, D. and Tanuma, S. (1999) DLAD, a novel mammalian divalent cation-independent endonuclease with homology to DNase II. Nucleic Acids Res. 27, 4083-4089
40. Lyon, C. J., Evans, C. J., Bill, B. R., Otsuka, A. J. and Aguilera, R. J. (2000) The C. elegans apoptotic nuclease NUC-1 is related in sequence and activity to mammalian DNase II. Gene 252, 147-154
41. Wu, Y. C., Stanfield, G. M. and Horvitz, H. R. (2000) NUC-1, a Caenorhabditis elegans DNase II homolog, functions in an intermediate step of DNA degradation during apoptosis. Genes Dev. 14, 536-548
42. Ito, K., Akiyama, D. and Minamiura, N. (1994) Evidence for an essential histidine residue on active site of human urinary DNase I: carboxymethylation and carbethoxylation. Arch. Biochem. Biophys. 313, 126-130
43. Friedhoff, P., Kolmes, B., Gimadutdinow, O., Wende, W., Krause, K. L. and Pingoud, A. (1996) Analysis of the mechanism of the Serratia nuclease using site-directed mutagenesis. Nucleic Acids Res. 24, 2632-2639
44. Meiss, G., Scholz, S. R., Korn, C., Gimadutdinow, O. and Pingoud, A. (2001) Identification of functionally relevant histidine residues in the apoptotic nuclease CAD. Nucleic Acids Res. 29, 3901-3909