Mycoplasma gallisepticum MGA_0676 is a membrane-associated cytotoxic nuclease with a staphylococcal nuclease region essential for nuclear translocation and apoptosis induction in chicken cells
详细信息 查看全文
- 作者：Jian Xu (1) (3)
Da Teng (1) (3)
Fei Jiang (1) (3)
Yuewei Zhang (1) (3)
Saeed A. El-Ashram (3) (5)
Hui Wang (3)
Zhenhong Sun (4)
Jinyan He (1) (3)
Junjun Shen (1) (3)
Wenxue Wu (1) (3)
Jinxiang Li (2) - 关键词：Mycoplasma gallisepticum ; MGA_0676 ; SNc ; Cytotoxic nuclease ; Nuclear translocation ; Apoptosis
- 刊名：Applied Microbiology and Biotechnology
- 出版年：2015
- 出版时间：February 2015
- 年：2015
- 卷：99
- 期：4
- 页码：1859-1871
- 全文大小：2,163 KB
- 参考文献：1. Abolnik C, Gouws J (2014) Extended survival times of / Mycoplasma gallisepticum and / Mycoplasma synoviae on kanekalon synthetic hair fibres. Poult Sci 93:8鈥?1. doi:10.3382/ps.2013-03457 CrossRef
2. Adelman JS, Kirkpatrick L, Grodio JL, Hawley DM (2013) House finch populations differ in early inflammatory signaling and pathogen tolerance at the peak of / Mycoplasma gallisepticum infection. Am Nat 181:674鈥?89. doi:10.1086/670024 CrossRef
3. Amand HL, Fant K, Norden B, Esbjorner EK (2008) Stimulated endocytosis in penetratin uptake: effect of arginine and lysine. Biochem Biophys Res Commun 371:621鈥?25. doi:10.1016/j.bbrc.2008.04.039 CrossRef
4. Berends ET, Horswill AR, Haste NM, Monestier M, Nizet V, Von Kockritz-Blickwede M (2010) Nuclease expression by / Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J Innate Immun 2:576鈥?86. doi:10.1159/000319909 CrossRef
5. Boddapati N, Anbarasu K, Suryaraja R, Tendulkar AV, Mahalingam S (2012) Subcellular distribution of the human putative nucleolar GTPase GNL1 is regulated by a novel arginine/lysine-rich domain and a GTP binding domain in a cell cycle-dependent manner. J Mol Biol 416:346鈥?66. doi:10.1016/j.jmb.2011.12.066 CrossRef
6. Cacciotto C, Addis MF, Coradduzza E, Carcangiu L, Nuvoli AM, Tore G, Dore GM, Pagnozzi D, Uzzau S, Chessa B, Pittau M, Alberti A (2013) / Mycoplasma agalactiae MAG_5040 is a Mg2+-dependent, sugar-nonspecific SNase recognised by the host humoral response during natural infection. PLoS ONE 8:e57775. doi:10.1371/journal.pone.0057775 CrossRef
7. Chambaud I, Wr贸blewski H, Blanchard A (1999) Interactions between / mycoplasma lipoproteins and the host immune system. Trends Microbiol 7:493鈥?99. doi:10.1016/S0966-842X(99)01641-8 CrossRef
8. Chen LL, Chung WC, Lin CP, Kuo CH (2012) Comparative analysis of gene content evolution in / phytoplasmas and / mycoplasmas. PLoS ONE 7:e34407. doi:10.1371/journal.pone.0034407 CrossRef
9. Chimileski S, Dolas K, Naor A, Gophna U, Papke RT (2013) Extracellular DNA metabolism in / Haloferax volcanii. Front Microbiol 5:57. doi:10.3389/fmicb.2014.00057
10. Delaney NF, Balenger S, Bonneaud C, Marx CJ, Hill GE, Ferguson-Noel N, Tsai P, Rodrigo A, Edwards SV (2012) Ultrafast evolution and loss of CRISPRs following a host shift in a novel wildlife pathogen, / Mycoplasma gallisepticum. PLoS Genet 8:e1002511. doi:10.1371/journal.pgen.1002511 CrossRef
11. Elkind E, Vaisid T, Kornspan JD, Barnoy S, Rottem S, Kosower NS (2012) Calpastatin upregulation in / Mycoplasma hyorhinis-infected cells is promoted by the / mycoplasma lipoproteins via the NF-魏B pathway. Cell Microbiol 14:840鈥?51. doi:10.1111/j.1462-5822.2012.01760.x CrossRef
12. Estev茫o S, van der Spek PE, van Rossum AM, Vink C (2014) Uncoupling of the AP endonucleolytic and 3鈥测€夆啋鈥?鈥?exonucleolytic activities of the Nfo protein of / Mycoplasma pneumoniae through mutation of specific amino acid residues. Microbiology 160:1087鈥?100. doi:10.1099/mic. 0.077578-0 CrossRef
13. Fagerlund R, M茅len K, Kinnunen L, Julkunen I (2002) Arginine/lysine-rich nuclear localization signals mediate interactions between dimeric STATs and importin alpha 5. J Biol Chem 277:30072鈥?0078. doi:10.1074/jbc.M202943200 CrossRef
14. Feller JK, Yang S, Mahalingam M (2013) Immunohistochemistry with a mutation specific monoclonal antibody as a screening tool for the BRAFV600 emutational status in primary cutaneous malignant melanoma. Mod Pathol 26:414鈥?20. doi:10.1038/modpathol.2012.168 CrossRef
15. Fu P, Sun Z, Zhang Y, Yu Z, Zhang H, Su D, Jiang F, Wu W (2014) Development of a direct competitive ELISA for the detection of / Mycoplasma bovis infection based on a monoclonal antibody of P48 protein. BMC Vet Res 10:42. doi:10.1186/1746-6148-10-42 CrossRef
16. Gallego P, Planell R, Benach J, Querol E, Perez-Pons JA, Reverter D (2012) Structural characterization of the enzymes composing the arginine deiminase pathway in / Mycoplasma penetrans. PLoS ONE 7:e47886. doi:10.1371/journal.pone.0047886 CrossRef
17. Gharaibeh S, Hailat A (2011) / Mycoplasma gallisepticum experimental infection and tissue distribution in chickens, sparrows and pigeons. Avian Pathol 40:349鈥?54. doi:10.1080/03079457.2011.582480 CrossRef
18. Ghorashi SA, Bradbury JM, Ferguson-Noel NM, Noormohammadi AH (2013) Comparison of multiple genes and 16S-23S rRNA intergenic space region for their capacity in high resolution melt curve analysis to differentiate / Mycoplasma gallisepticum vaccine strain ts-11 from field strains. Vet Microbiol 167:440鈥?47. doi:10.1016/j.vetmic.2013.09.032 CrossRef
19. Hamasaki M, Furuta N, Matsuda A, Nezu A, Yamamoto A, Fujita N, Oomori H, Noda T, Haraguchi T, Hiraoka Y, Amano A, Yoshimori T (2013) Autophagosomes form at ER-mitochondria contact sites. Nature 495:389鈥?93. doi:10.1038/nature11910 CrossRef
20. Heitz F, Morris MC, Divita G (2009) Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics. Br J Pharmacol 157:195鈥?06. doi:10.1111/j.1476-5381.2009.00057.x CrossRef
21. Kaitala V, Heino M, Getz WM (1997) Host-parasite dynamics and the evolution of host immunity and parasite fecundity strategies. Bull Math Biol 59:427鈥?50. doi:10.1016/S0092-8240(96)00090-0 CrossRef
22. Kandasamy P, Zarini S, Chan ED, Leslie CC, Murphy RC, Voelker DR (2011) Pulmonary surfactant phosphatidylglycerol inhibits / Mycoplasma pneumoniae-stimulated eicosanoid production from human and mouse macrophages. J Biol Chem 286:7841鈥?853. doi:10.1074/jbc.M110.170241 CrossRef
23. Kiedrowski MR, Kavanaugh JS, Malone CL, Mootz JM, Voyich JM, Smeltzer MS, Bayles KW, Horswill AR (2011) Nuclease modulates biofilm formation in community-associated methicillin-resistant / Staphylococcus aureus. PLoS ONE 6:e26714. doi:10.1371/journal.pone.0026714 CrossRef
24. Li L, Krishnan M, Baseman JB, Kannan TR (2010) Molecular cloning, expression, and characterization of a Ca2+-dependent, membrane-associated nuclease of / Mycoplasma genitalium. J Bacteriol 192:4876鈥?884. doi:10.1128/JB.00401-10 CrossRef
25. Masukagami Y, Tivendale KA, Mardani K, Ben-Barak I, Markham PF, Browning GF (2013) The / Mycoplasma gallisepticum virulence factor lipoprotein MslA is a novel polynucleotide binding protein. Infect Immun 81:3220鈥?226. doi:10.1128/I AI.00365-13 CrossRef
26. Morita C, Sumioka R, Nakata M, Okahashi N, Wada S, Yamashiro, Hayashi M, Hamada S, Sumitomo T, Kawabata S (2014) Cell wall-anchored nuclease of / Streptococcus sanguinis contributes to escape from neutrophil extracellular trap-mediated bacteriocidal activity. PloS One 8: e103125. doi: 10.1371/journal.pone.0103125
27. Mu HH, Nourian MM, Jiang HH, Tran JW, Cole BC (2014) / Mycoplasma superantigen initiates a TLR4-dependent Th17 cascade that enhances arthritis after blocking B7-1 in / Mycoplasma arthritidis-infected mice. Cell Microbiol 16:896鈥?11. doi:10.1111/cmi.12247 CrossRef
28. Oberto DKJ, Serebryakova M, Gorbachev A, Zhukova Y, Levitskii S, Mazur AK, Govorun V (2011) / Mycoplasma gallisepticum produces a histone-like protein that recognizes base mismatches in DNA. Biochemistry 50:8692鈥?702. doi:10.1021/bi2009097 CrossRef
29. Olson ME, Nygaard TK, Ackermann L, Watkins RL, Zurek OW, Pallister KB, Griffith S, Kiedrowski MR, Flack CE, Kavanaugh JS, Kreiswirth BN, Horswill AR, Voyich JM (2013) / Staphylococcus aureus nuclease is an SaeRS-dependent virulence factor. Infect Immun 4:1316鈥?324. doi:10.1128/IAI. 01242-12 CrossRef
30. Oussenko IA, Sanchez R, Bechhofer DH (2004) / Bacillus subtilis YhcR, a high-molecular -weight, nonspecific endonuclease with a unique domain structure. J Bacteriol 186:5376鈥?383. doi:10.1128/JB.186.16.5376-5383.2004
31. Paddenberg R, Weber A, Wulf S, Mannherz HG (1998) / Mycoplasma nucleases able to induce internucleosomal DNA degradation in cultured cells possess many characteristics of eukaryotic apoptotic nucleases. Cell Death Differ 5:517鈥?28 CrossRef
32. Papayannopoulos V (2014) Infection: microbial nucleases turn immune cells against each other. Curr Biol 24:R123鈥揜125. doi:10.1016/j.cub.2013.12.027 CrossRef
33. Pettigrew MM, Marks LR, Kong Y, Gent JF, Roche-Hakansson H, Hakansson AP (2014) Dynamic changes in the / Streptococcus pneumoniae transcriptome during transition from biofilm formation to invasive disease upon influenza A virus infection. Infect Immun 82:4607鈥?619. doi:10.1128/IAI. 02225-14 CrossRef
34. Peebles ED, Jacob R, Branton SL, Gerard PD (2014) Effects of / Mycoplasma gallisepticum vaccination on serum 伪1-acid glycoprotein concentrations in commercial layer chickens. Poult Sci 93:1396鈥?402. doi:10.3382/ps.2014-03906 CrossRef
35. Prince OA, Krunkosky TM, Krause DC (2014) In vitro spatial and temporal analysis of / Mycoplasma pneumoniae colonization of human airway epithelium. Infect Immun 82:579鈥?86. doi:10.1128/IAI. 01036-13 CrossRef
36. Schmidt JA, Browning GF, Markham PF (2007) / Mycoplasma hyopneumoniae mhp379 is a Ca2+-dependent, sugar-nonspecific exonuclease exposed on the cell surface. J Bacteriol 189:3414鈥?424. doi:10.1128/JB.01835-06 CrossRef
37. Somarajan SR, Kannan TR, Baseman JB (2010) / Mycoplasma pneumoniae Mpn133 is a cytotoxic nuclease with a glutamic acid-, lysine- and serine-rich region essential for binding and internalization but not enzymatic activity. Cell Microbiol 12:1821鈥?831. doi:10.1111/j.1462-5822.2010.01513.x CrossRef
38. Tang J, Zhou R, Shi X, Kang M, Wang H, Chen H (2008) Two thermostable nucleases coexisted in / Staphylococcus aureus, evidence from mutagenesis and in vitro expression. FEMS Microbiol Lett 284:176鈥?83. doi:10.111/j.1574-6968.2008.01194.x CrossRef
39. Takahashi T, Morozumi M, Okada T, Chiba N, Asami R, Murayama SY, Ubukata K (2009) Prolonged / Mycoplasma pneumoniae infection in an elderly patient with community-acquired pneumonia. J Infect Chemother 15:243鈥?47. doi:10.1007/s10156-009-0692-x CrossRef
40. Thammavongsa V, Missiakas DM, Schneewind O (2013) / Staphylococcus aureus degrades neutrophil extracellular traps to promote immune cell death. Science 342:863鈥?66. doi:10.1126/science.1242255 CrossRef
41. Vande VJ, Sabuncuo臒lu S, Noppen S, Hofer A, Ranjbarian F, Fieuws S, Balzarini J, Liekens S (2014) Nucleoside-catabolizing enzymes in / mycoplasma-infected tumor cell cultures compromise the cytostatic activity of the anticancer drug gemcitabine. J Biol Chem 289:13054鈥?3065. doi:10.1074/jbc.M114.558924
42. Vanyushkina AA, Fisunov GY, Gorbachev AY, Kamashev DE, Govorun VM (2014) Metabolomic analysis of three Mollicute species. PLoS ONE 9:e89312. doi:10.1371/journal.pone.0089312 CrossRef
43. Vogl G, Plaickner A, Szathmary S, Stipkovits L, Rosengarten R, Szostak MP (2008) / Mycoplasma gallisepticum invades chicken erythrocytes during infection. Infect Immun 76:71鈥?7. doi:10.1128/IAI. 00871-07 CrossRef
44. Wang D, Ma W, She R, Sun Q, Liu Y, Hu Y, Liu L, Yang Y, Peng K (2009) Effects of swine gut antimicrobial peptides on the intestinal mucosal immunity in specific-pathogen-free chickens. Poult Sci 88:967鈥?74. doi:10.3382/ps.2008-00533 CrossRef
45. Wang M, Gao XJ, Zhao WW, Zhao WJ, Jiang CH, Huang F, Kou JP, Liu BL, Liu K (2013) Opposite effects of genistein on the regulation of insulin-mediated glucose homeostasis in adipose tissue. Br J Pharmacol 170:328鈥?40. doi:10.1111/bph.12276 CrossRef
46. Wood GE, Iverson-Cabral SL, Patton DL, Cummings PK, Cosgrove Sweeney YT, Totten PA (2013) Persistence, immune response, and antigenic variation of / Mycoplasma genitalium in an experimentally infected pig-tailed macaque (Macaca nemestrina). Infect Immun 81:2938鈥?951. doi:10.1128/IAI. 01322-12 CrossRef
47. Zhang LL, Nguyen HC, Chipot L, Piotrowski E, Bertrand C, Thibessard A, Leblond P (2014) The adnAB Locus, encoding a putative helicase-nuclease activity, is essential in / Streptomyces. J Bacteriol 14:2701鈥?708. doi:10.1128/JB.01513-14 CrossRef - 作者单位：Jian Xu (1) (3)
Da Teng (1) (3)
Fei Jiang (1) (3)
Yuewei Zhang (1) (3)
Saeed A. El-Ashram (3) (5)
Hui Wang (3)
Zhenhong Sun (4)
Jinyan He (1) (3)
Junjun Shen (1) (3)
Wenxue Wu (1) (3)
Jinxiang Li (2)
1. Laboratory of Rapid Diagnostic Technology for Animal Disease, College of Veterinary Medicine, China Agricultural University, 100193, Beijing, People鈥檚 Republic of China
3. Key Laboratory of Animal Epidemiology and Zoonosis, Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, 100193, Beijing, People鈥檚 Republic of China
5. Kafrelsheikh University, El-Geish Street, Kafr el-Sheikh, 33516, Kafr el-Sheikh, Egypt
4. Taishan Medical University, Taian, 271000, Shandong, People鈥檚 Republic of China
2. Chinese Academy of Agricultural Sciences, 100081, Beijing, People鈥檚 Republic of China - 刊物类别：Chemistry and Materials Science
- 刊物主题：Chemistry
Biotechnology
Microbiology
Microbial Genetics and Genomics - 出版者：Springer Berlin / Heidelberg
- ISSN：1432-0614
文摘
Mycoplasma gallisepticum can infect a wide variety of birds including the commercial poultry. M. gallisepticum MGA_0676 is a putative lipoprotein, which is similar to bacterial thermostable nucleases. But the possible pathogenic effect of M. gallisepticum MGA_0676 has not been investigated so far. In the present study, we cloned the MGA_0676 gene after deletion of the amino-terminal signal sequence and mutagenesis of the Mycoplasma TGA tryptophan codons to TGG and expressed recombinant MGA_0676 protein in Escherichia coli. We identified and characterized MGA_0676 as a Ca2+-dependent cytotoxic nuclease of M. gallisepticum with a staphylococcal nuclease (SNc) region that displays the hallmarks of nucleases. Membrane protein immunoblot analysis and immunogold electron microscopy revealed that MGA_0676 locates on the membrane surface of M. gallisepticum. Furthermore, apoptosis assay using annexin V-FITC and propidium iodide (annexin V/PI) indicated that MGA_0676 played significant roles in apoptosis induction and pathological damages in chicken cells. Moreover, confocal microscopy showed that MGA_0676 localizes in the nuclei of host cells. Besides, after the SNc region was deleted, MGA_0676 lost its ability of nuclear localization, nuclease activity, and cytotoxicity, which revealed that the SNc region is essential for nuclear translocation and induction of apoptosis in chicken cells. The above results suggest that MGA_0676 is an important virulence factor in cellular pathology and may play a unique role in the life cycle events of M. gallisepticum.