Molecular cloning, expression, and characterization of a Ca 2+-dependent, membrane-associated nuclease of Mycoplasma genitalium

Journal of Bacteriology

Volumn 192, Issue 19, 2010, Pages 4876-4884

  Li, Linbo ^a   Krishnan, Manickam ^a   Baseman, Joel B ^a   Kannan, T R ^a  

^a Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; EGTAZIC ACID; MANGANESE; MG 186 ENZYME; TRITON X 114; UNCLASSIFIED DRUG; ZINC; BACTERIAL PROTEIN; ENDONUCLEASE;

APOPTOSIS; ARTICLE; BIOCHEMISTRY; CELL FRACTIONATION; CELL MEMBRANE; CELL NUCLEUS; CELL SURFACE; DNA DEGRADATION; ENDOMETRIUM CELL; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PURIFICATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; MOLECULAR CLONING; MYCOPLASMA GENITALIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS; ZYMOGRAPHY; AMINO ACID SEQUENCE; CELL LINE; CHEMISTRY; DRUG EFFECT; ENZYMOLOGY; GENETICS; IMMUNOBLOTTING; METABOLISM; MOLECULAR GENETICS; POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY;

EUKARYOTA; MYCOPLASMA; MYCOPLASMA GENITALIUM;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CELL LINE; CELL NUCLEUS; ENDONUCLEASES; HUMANS; IMMUNOBLOTTING; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MYCOPLASMA GENITALIUM; POLYMERASE CHAIN REACTION;

EID: 77957331584     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00401-10     Document Type: Article

References (41)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Balasubramanian, S., T. R. Kannan, P. J. Hart, and J. B. Baseman. 2009. Amino acid changes in elongation factor Tu of Mycoplasma pneumoniae and Mycoplasma genitalium influence fibronectin binding. Infect. Immun. 77:3533-3541.
3. Baseman, J. B., S. F. Dallo, J. G. Tully, and D. L. Rose. 1988. Isolation and characterization of Mycoplasma genitalium strains from the human respiratory tract. J. Clin. Microbiol. 26:2266-2269.
4. Baseman, J. B., M. Lange, N. L. Criscimagna, J. A. Giron, and C. A. Thomas. 1995. Interplay between mycoplasmas and host target cells. Microb. Pathog. 19:105-116.
5. Baseman, J. B., and J. G. Tully. 1997. Mycoplasmas: sophisticated, reemerging, and burdened by their notoriety. Emerg. Infect. Dis. 3:21-32.
6. Beagley, K. W., and C. M. Gockel. 2003. Regulation of innate and adaptive immunity by the female sex hormones oestradiol and progesterone. FEMS Immunol. Med. Microbiol. 38:13-22.
7. 2+-dependent endonuclease. J. Bacteriol. 179:2210-2220.
8. Bendjennat, M., A. Blanchard, M. Loutfi, L. Montagnier, and E. Bahraoui. 1999. Role of Mycoplasma penetrans endonuclease P40 as a potential pathogenic determinant. Infect. Immun. 67:4456-4462.
9. Blaylock, M. W., O. Musatovova, J. G. Baseman, and J. B. Baseman. 2004. Determination of infectious load of Mycoplasma genitalium in clinical samples of human vaginal cells. J. Clin. Microbiol. 42:746-752.
10. Bootman, M. D., T. J. Collins, C. M. Peppiatt, L. S. Prothero, L. MacKenzie, P. De Smet, M. Travers, S. C. Tovey, J. T. Seo, M. J. Berridge, F. Ciccolini, and P. Lipp. 2001. Calcium signalling-an overview. Semin. Cell Dev. Biol. 12:3-10.
11. Cotton, F. A., E. E. Hazen, Jr., and M. J. Legg. 1979. Staphylococcal nuclease: proposed mechanism of action based on structure of enzyme-thymidine 3′,5′-bisphosphate-calcium ion complex at 1.5-A resolution. Proc. Natl. Acad. Sci. U. S. A. 76:2551-2555.
12. Cowen, B. S., and S. C. Smith. 1972. Nuclease activities of Mycoplasma gallisepticum as a function of culture age in different media. J. Bacteriol. 109:21-24.
13. Dallo, S. F., and J. B. Baseman. 2000. Intracellular DNA replication and long-term survival of pathogenic mycoplasmas. Microb. Pathog. 29:301-309.
14. Dallo, S. F., T. R. Kannan, M. W. Blaylock, and J. B. Baseman. 2002. Elongation factor Tu and E1 beta subunit of pyruvate dehydrogenase complex act as fibronectin binding proteins in Mycoplasma pneumoniae. Mol. Microbiol. 46:1041-1051.
15. Desai, N. N., E. A. Kennard, D. A. Kniss, and C. I. Friedman. 1994. Novel human endometrial cell line promotes blastocyst development. Fertil. Steril. 61:760-766.
16. Feng, S. H., and S. C. Lo. 1994. Induced mouse spleen B-cell proliferation and secretion of immunoglobulin by lipid-associated membrane proteins of Mycoplasma fermentans incognitus and Mycoplasma penetrans. Infect. Immun. 62:3916-3921.
17. Feng, S. H., and S. C. Lo. 1999. Lipid extract of Mycoplasma penetrans proteinase K-digested lipid-associated membrane proteins rapidly activates NF-κB and activator protein 1. Infect. Immun. 67:2951-2956.
18. Fraser, C. M., J. D. Gocayne, O. White, M. D. Adams, R. A. Clayton, R. D. Fleischmann, C. J. Bult, A. R. Kerlavage, G. Sutton, J. M. Kelley, R. D. Fritchman, J. F. Weidman, K. V. Small, M. Sandusky, J. Fuhrmann, D. Nguyen, T. R. Utterback, D. M. Saudek, C. A. Phillips, J. M. Merrick, J. F. Tomb, B. A. Dougherty, K. F. Bott, P. C. Hu, T. S. Lucier, S. N. Peterson, H. O. Smith, C. A. Hutchison III, and J. C. Venter. 1995. The minimal gene complement of Mycoplasma genitalium. Science 270:397-403.
19. Furr, P. M., and D. Taylor-Robinson. 1993. Factors influencing the ability of different mycoplasmas to colonize the genital tract of hormone-treated female mice. Int. J. Exp. Pathol. 74:97-101.
20. Jarvill-Taylor, K. J., C. VanDyk, and F. C. Minion. 1999. Cloning of mnuA, a membrane nuclease gene of Mycoplasma pulmonis, and analysis of its expression in Escherichia coli. J. Bacteriol. 181:1853-1860.
21. Kannan, T. R., and J. B. Baseman. 2006. ADP-ribosylating and vacuolating cytotoxin of Mycoplasma pneumoniae represents unique virulence determinant among bacterial pathogens. Proc. Natl. Acad. Sci. U. S. A. 103:6724-6729.
22. Kannan, T. R., D. Provenzano, J. R. Wright, and J. B. Baseman. 2005. Identification and characterization of human surfactant protein A binding protein of Mycoplasma pneumoniae. Infect. Immun. 73:2828-2834.
23. Loll, P. J., and E. E. Lattman. 1989. The crystal structure of the ternary complex of staphylococcal nuclease, Ca2+, and the inhibitor pdTp, refined at 1.65 A. Proteins 5:183-201.
24. Mernaugh, G. R., S. F. Dallo, S. C. Holt, and J. B. Baseman. 1993. Properties of adhering and nonadhering populations of Mycoplasma genitalium. Clin. Infect. Dis. 17(Suppl. 1):S69-S78.
25. Minion, F. C., and J. D. Goguen. 1986. Identification and preliminary characterization of external membrane-bound nuclease activities in Mycoplasma pulmonis. Infect. Immun. 51:352-354.
26. Minion, F. C., K. J. Jarvill-Taylor, D. E. Billings, and E. Tigges. 1993. Membrane-associated nuclease activities in mycoplasmas. J. Bacteriol. 175:7842-7847.
27. Mitchell, A., and L. R. Finch. 1977. Pathways of nucleotide biosynthesis in Mycoplasma mycoides subsp. mycoides. J. Bacteriol. 130:1047-1054.
28. Namiki, K., S. Goodison, S. Porvasnik, R. W. Allan, K. A. Iczkowski, C. Urbanek, L. Reyes, N. Sakamoto, and C. J. Rosser. 2009. Persistent exposure to Mycoplasma induces malignant transformation of human prostate cells. PLoS One 4:e6872.
29. Paddenberg, R., A. Weber, S. Wulf, and H. G. Mannherz. 1998. Mycoplasma nucleases able to induce internucleosomal DNA degradation in cultured cells possess many characteristics of eukaryotic apoptotic nucleases. Cell Death Differ. 5:517-528.
30. Paddenberg, R., S. Wulf, A. Weber, P. Heimann, L. A. Beck, and H. G. Mannherz. 1996. Internucleosomal DNA fragmentation in cultured cells under conditions reported to induce apoptosis may be caused by mycoplasma endonucleases. Eur. J. Cell Biol. 71:105-119.
31. Pollack, J. D., and P. J. Hoffmann. 1982. Properties of the nucleases of mollicutes. J. Bacteriol. 152:538-541.
32. Rao, L., D. Perez, and E. White. 1996. Lamin proteolysis facilitates nuclear events during apoptosis. J. Cell Biol. 135:1441-1455.
33. Razin, S., A. Knyszynski, and Y. Lifshitz. 1964. Nucleases of Mycoplasma. J. Gen. Microbiol. 36:323-332.
34. Sasaki, Y., J. Ishikawa, A. Yamashita, K. Oshima, T. Kenri, K. Furuya, C. Yoshino, A. Horino, T. Shiba, T. Sasaki, and M. Hattori. 2002. The complete genomic sequence of Mycoplasma penetrans, an intracellular bacterial pathogen in humans. Nucleic Acids Res. 30:5293-5300.
35. 2+-dependent, sugar-nonspecific exonuclease exposed on the cell surface. J. Bacteriol. 189:3414-3424.
36. Taniuchi, H., C. B. Anfinsen, and A. Sodja. 1967. The amino acid sequence of an extracellular nuclease of Staphylococcus aureus. 3. Complete amino acid sequence. J. Biol. Chem. 242:4752-4758.
37. Taylor-Robinson, D. 2002. Mycoplasma genitalium - an update. Int. J. STD AIDS. 13:145-151.
38. Thomas, A. P., G. S. Bird, G. Hajnoczky, L. D. Robb-Gaspers, and J. W. Putney, Jr. 1996. Spatial and temporal aspects of cellular calcium signaling. FASEB J. 10:1505-1517.
39. Tully, J. G., D. L. Rose, J. B. Baseman, S. F. Dallo, A. L. Lazzell, and C. P. Davis. 1995. Mycoplasma pneumoniae and Mycoplasma genitalium mixture in synovial fluid isolate. J. Clin. Microbiol. 33:1851-1855.
40. Tully, J. G., D. Taylor-Robinson, R. M. Cole, and D. L. Rose. 1981. A newly discovered mycoplasma in the human urogenital tract. Lancet 1:1288-1291.
41. Ueno, P. M., J. Timenetsky, V. E. Centonze, J. J. Wewer, M. Cagle, M. A. Stein, M. Krishnan, and J. B. Baseman. 2008. Interaction of Mycoplasma genitalium with host cells: evidence for nuclear localization. Microbiology 154:3033-3041.