Autonomous and non-autonomous roles of DNase II during cell death in C. elegans embryos

Bioscience Reports

Volumn 35, Issue 3, 2015, Pages

  Yu, Hsiang ^a   Lai, Huey Jen ^a,b   Lin, Tai Wei ^a   Lo, Szecheng J ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Caenorhabditis elegans; DNase II; Exocytosis; Fluorescence probes; Lysosome

Indexed keywords

DEOXYRIBONUCLEASE II; DNA FRAGMENT; NUC 1 PROTEIN; NUCLEASE; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; CED-1 PROTEIN, C ELEGANS; DEOXYRIBONUCLEASE; FLUORESCENT DYE; MEMBRANE PROTEIN;

ANALYTIC METHOD; APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CELL DEATH; CONTROLLED STUDY; DNA DEGRADATION; DNA STRAND BREAKAGE; EMBRYO; ENZYME ACTIVITY; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; TOPOISOMERASE LIGATION FLUORESCENCE PROBE; TUNEL ASSAY; WILD TYPE; ANIMAL; BLASTOMA; CHEMISTRY; CYTOLOGY; EMBRYOLOGY; GENETICS; METABOLISM; MUTATION; NONMAMMALIAN EMBRYO; PHYSIOLOGY; TRANSGENIC ANIMAL;

CAENORHABDITIS ELEGANS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; BLASTOMERES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL DEATH; EMBRYO, NONMAMMALIAN; ENDODEOXYRIBONUCLEASES; FLUORESCENT DYES; MEMBRANE PROTEINS; MUTATION;

EID: 84935020238     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20150055     Document Type: Article

References (39)

1. Elliott, M.R. and Ravichandran, K.S. (2010) Clearance of apoptotic cells: implications in health and disease. J. Cell Biol. 189, 1059-1070 CrossRef PubMed
2. Wickman, G., Julian, L. and Olson, M.F. (2012) How apoptotic cells aid in the removal of their own cold dead bodies. Cell Death Differ. 19, 735-742 CrossRef PubMed
3. Conradt, B. and Xue, D. (2005) Programmed cell death. WormBook: The Online Review of C. elegans Biology, NCBI Bookshelf, Pasadena 1-13
4. Widlak, P. and Garrard, W.T. (2009) Roles of the major apoptotic nuclease-DNA fragmentation factor-in biology and disease. Cell. Mol. Life Sci. 66, 263-274 CrossRef PubMed
5. Widlak, P. and Garrard, W.T. (2001) Ionic and cofactor requirements for the activity of the apoptotic endonuclease DFF40/CAD. Mol. Cell. Biochem. 218, 125-130 CrossRef PubMed
6. Gavrieli, Y., Sherman, Y. and Ben-Sasson, S.A. (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501 CrossRef PubMed
7. Wyllie, A.H. (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284, 555-556 CrossRef PubMed
8. Counis, M.F. and Torriglia, A. (2006) Acid DNases and their interest among apoptotic endonucleases. Biochimie 88, 1851-1858 CrossRef PubMed
9. Kawane, K., Fukuyama, H., Yoshida, H., Nagase, H., Ohsawa, Y., Uchiyama, Y., Okada, K., Iida, T. and Nagata, S. (2003) Impaired thymic development in mouse embryos deficient in apoptotic DNA degradation. Nat. Immunol. 4, 138-144 CrossRef PubMed
10. 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 PubMed
11. Evans, C.J. and Aguilera, R.J. (2003) DNase II: genes, enzymes and function. Gene 322, 1-15 CrossRef PubMed
12. Harosh, I., Binninger, D.M., Harris, P.V., Mezzina, M. and Boyd, J.B. (1991) Mechanism of action of deoxyribonuclease II from human lymphoblasts. Eur. J. Biochem. 202, 479-484 CrossRef PubMed
13. 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 CrossRef PubMed
14. Krieser, R.J., MacLea, K.S., Longnecker, D.S., Fields, J.L., Fiering, S. and Eastman, A. (2002) Deoxyribonuclease IIalpha is required during the phagocytic phase of apoptosis and its loss causes perinatal lethality. Cell Death Differ. 9, 956-962 CrossRef PubMed
15. 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 CrossRef PubMed
16. Barry, M.A., Reynolds, J.E. and Eastman, A. (1993) Etoposide-induced apoptosis in human HL-60 cells is associated with intracellular acidification. Cancer Res. 53, 2349-2357 PubMed
17. Barry, M.A. and Eastman, A. (1993) Identification of deoxyribonuclease II as an endonuclease involved in apoptosis. Arch. Biochem. Biophys. 300, 440-450 CrossRef PubMed
18. Samejima, K. and Earnshaw, W.C. (2005) Trashing the genome: the role of nucleases during apoptosis. Nat. Rev. Mol. Cell Biol. 6, 677-688 CrossRef PubMed
19. Bass, B.P., Tanner, E.A., Mateos San Martin, D., Blute, T., Kinser, R.D., Dolph, P.J. and McCall, K. (2009) Cell-autonomous requirement for DNaseII in nonapoptotic cell death. Cell Death Differ. 16, 1362-1371 CrossRef PubMed
20. Aruscavage, P.J., Hellwig, S. and Bass, B.L. (2010) Small DNA pieces in C. elegans are intermediates of DNA fragmentation during apoptosis. PLoS One 5, e11217 CrossRef PubMed
21. Lai, H.J., Lo, S.J., Kage-Nakadai, E., Mitani, S. and Xue, D. (2009) The roles and acting mechanism of Caenorhabditis elegans DNase II genes in apoptotic dna degradation and development. PLoS One 4, e7348 CrossRef PubMed
22. Minchew, C.L. and Didenko, V.V. (2011) Fluorescent probes detecting the phagocytic phase of apoptosis: enzyme-substrate complexes of topoisomerase and DNA. Molecules 16, 4599-4614 CrossRef PubMed
23. Didenko, V.V. (2011) 5'OH DNA breaks in apoptosis and their labeling by topoisomerase-based approach. Methods Mol. Biol. 682, 77-87 CrossRef PubMed
24. Minchew, C.L. and Didenko, V.V. (2012) In vitro assembly of semi-artificial molecular machine and its use for detection of DNA damage. J. Vis. Exp. 59, e3628 PubMed
25. Minchew, C.L. and Didenko, V.V. (2014) Assessing phagocytic clearance of cell death in experimental stroke by ligatable fluorescent probes. J. Vis. Exp., doi: 10.3791/51261
26. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94 PubMed
27. Gengyo-Ando, K. and Mitani, S. (2000) Characterization of mutations induced by ethyl methanesulfonate, UV, and trimethylpsoralen in the nematode Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 269, 64-69 CrossRef PubMed
28. Lee, M.H. and Schedl, T. (2006) RNA in situ hybridization of dissected gonads. WormBook: The Online Review of C. elegans Biology, NCBI Bookshelf, Pasadena 1-7
29. Chen, W.J., Lai, P.J., Lai, Y.S., Huang, P.T., Lin, C.C. and Liao, T.H. (2007) Probing the catalytic mechanism of bovine pancreatic deoxyribonuclease I by chemical rescue. Biochem. Biophys. Res. Commun. 352, 689-696 CrossRef PubMed
30. Kostich, M., Fire, A. and Fambrough, D.M. (2000) Identification and molecular-genetic characterization of a LAMP/CD68-like protein from Caenorhabditis elegans. J. Cell Sci. 113 Pt 14, 2595-2606 PubMed
31. Huang, R.T., Liao, T.H. and Lu, S.C. (2009) Proteolytic processing of porcine deoxyribonuclease II occurs in lysosomes but is not required for enzyme activation. FEBS J. 276, 1891-1899 CrossRef PubMed
32. Ohkouchi, S., Shibata, M., Sasaki, M., Koike, M., Safig, P., Peters, C., Nagata, S. and Uchiyama, Y. (2013) Biogenesis and proteolytic processing of lysosomal DNase II. PLoS One 8, e59148 CrossRef PubMed
33. 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 CrossRef PubMed
34. Craig, A.L., Moser, S.C., Bailly, A.P. and Gartner, A. (2012) Methods for studying the DNA damage response in the Caenorhabdatis elegans germ line. Methods Cell Biol. 107, 321-352 CrossRef PubMed
35. Liao, C., Liu, M., Bai, X., Liu, P., Wang, X., Li, T., Tang, B., Gao, H., Sun, Q., Liu, X. et al. (2014) Characterisation of a plancitoxin-1-like DNase II gene in Trichinella spiralis. PLoS Negl. Trop. Dis. 8, e3097 CrossRef PubMed
36. MacLea, K.S., Krieser, R.J. and Eastman, A. (2002) Revised structure of the active form of human deoxyribonuclease IIalpha. Biochem. Biophys. Res. Commun. 292, 415-421 CrossRef PubMed
37. MacLea, K.S., Krieser, R.J. and Eastman, A. (2003) Structural requirements of human DNase II alpha for formation of the active enzyme: the role of the signal peptide, N-glycosylation, and disulphide bridging. Biochem. J. 371, 867-876 CrossRef PubMed
38. Xu, M., Liu, Y., Zhao, L., Gan, Q., Wang, X. and Yang, C. (2014) The lysosomal cathepsin protease CPL-1 plays a leading role in phagosomal degradation of apoptotic cells in Caenorhabditis elegans. Mol. Biol. Cell 25, 2071-2083 CrossRef PubMed
39. Lettre, G. and Hengartner, M.O. (2006) Developmental apoptosis in C. elegans: a complex CEDnario. Nat. Rev. Mol. Cell Biol. 7, 97-108 CrossRef PubMed