The Streptococcus pyogenesNAD+ glycohydrolase modulates epithelial cell PARylation and HMGB1 release

Cellular Microbiology

Volumn 17, Issue 9, 2015, Pages 1376-1390

  Chandrasekaran, Sukantha ^a   Caparon, Michael G ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 8; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE NUCLEOSIDASE; TUMOR NECROSIS FACTOR ALPHA; HMGB1 PROTEIN, HUMAN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PARP1 PROTEIN, HUMAN; POLY(ADENOSINE DIPHOSPHATE RIBOSE);

APOPTOSIS; ARTICLE; BACTERIAL STRAIN; CELL DIVISION; CELL STRESS; CHANNEL GATING; CONTROLLED STUDY; CYTOKINE RESPONSE; ENZYME ACTIVITY; EPITHELIUM CELL; FEMALE; HELA CELL LINE; HOST CELL; HUMAN; HUMAN CELL; MEMBRANE PERMEABILITY; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOCOCCUS PYOGENES; TRANSCRIPTION INITIATION; CELL LINE; ENZYMOLOGY; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

STREPTOCOCCUS; STREPTOCOCCUS PYOGENES;

CELL LINE; EPITHELIAL CELLS; HMGB1 PROTEIN; HOST-PATHOGEN INTERACTIONS; HUMANS; NAD+ NUCLEOSIDASE; POLY (ADP-RIBOSE) POLYMERASE-1; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; STREPTOCOCCUS PYOGENES;

EID: 84940437862     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12442     Document Type: Article

References (59)

1. Abdelkarim, G.E., Gertz, K., Harms, C., Katchanov, J., Dirnagl, U., Szabo, C., and Endres, M. (2001) Protective effects of PJ34, a novel, potent inhibitor of poly(ADP-ribose) polymerase (PARP) in in vitro and in vivo models of stroke. Int J Mol Med 7: 255-260.
2. Altman, B.J., and Rathmell, J.C. (2012) Metabolic stress in autophagy and cell death pathways. Cold Spring Harb Perspect Biol 4: a008763.
3. Alvarez-Gonzalez, R., and Althaus, F.R. (1989) Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA-damaging agents. Mutat Res 218: 67-74.
4. Ato, M., Ikebe, T., Kawabata, H., Takemori, T., and Watanabe, H. (2008) Incompetence of neutrophils to invasive group A streptococcus is attributed to induction of plural virulence factors by dysfunction of a regulator. PLoS ONE 3: e3455.
5. Boulares, A.H., Yakovlev, A.G., Ivanova, V., Stoica, B.A., Wang, G., Iyer, S., and Smulson, M. (1999) Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. J Biol Chem 274: 22932-22940.
6. Bricker, A.L., Cywes, C., Ashbaugh, C.D., and Wessels, M.R. (2002) NAD+-glycohydrolase acts as an intracellular toxin to enhance the extracellular survival of group A streptococci. Mol Microbiol 44: 257-269.
7. Burgos, E.S. (2011) NAMPT in regulated NAD biosynthesis and its pivotal role in human metabolism. Curr Med Chem 18: 1947-1961.
8. Carlson, A.S., Kellner, A., Bernheimer, A.W., and Freeman, E.B. (1957) A streptococcal enzyme that acts specifically upon diphosphopyridine nucleotide: characterization of the enzyme and its separation from streptolysin O. J Exp Med 106: 15-26.
9. Chandrasekaran, S., Ghosh, J., Port, G.C., Koh, E., and Caparon, M.G. (2013) Analysis of polymorphic residues reveals distinct enzymatic and cytotoxic activities of the streptococcus pyogenes NAD+ glycohydrolase. J Biol Chem 288: 20064-20075.
10. Chavakis, T., Bierhaus, A., Al-Fakhri, N., Schneider, D., Witte, S., Linn, T., etal. (2003) The pattern recognition receptor (RAGE) is a counterreceptor for leukocyte integrins: a novel pathway for inflammatory cell recruitment. J Exp Med 198: 1507-1515.
11. Cunningham, M.W. (2000) Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13: 470-511.
12. Cywes Bentley, C., Hakansson, A., Christianson, J., and Wessels, M.R. (2005) Extracellular group A Streptococcus induces keratinocyte apoptosis by dysregulating calcium signalling. Cell Microbiol 7: 945-955.
13. Davis, K., Banerjee, S., Friggeri, A., Bell, C., Abraham, E., and Zerfaoui, M. (2012) Poly(ADP-ribosyl)ation of high mobility group box 1 (HMGB1) protein enhances inhibition of efferocytosis. Mol Med 18: 359-369.
14. D'Amours, D., Desnoyers, S., D'Silva, I., and Poirier, G.G. (1999) Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342: 249-268.
15. Ditsworth, D., Zong, W.X., and Thompson, C.B. (2007) Activation of poly(ADP)-ribose polymerase (PARP-1) induces release of the pro-inflammatory mediator HMGB1 from the nucleus. J Biol Chem 282: 17845-17854.
16. Fink, S.L., and Cookson, B.T. (2005) Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 73: 1907-1916.
17. Garcia Soriano, F., Virag, L., Jagtap, P., Szabo, E., Mabley, J.G., Liaudet, L., etal. (2001) Diabetic endothelial dysfunction: the role of poly(ADP-ribose) polymerase activation. Nat Med 7: 108-113.
18. Ghosh, J., and Caparon, M.G. (2006) Specificity of Streptococcus pyogenes NAD(+) glycohydrolase in cytolysin-mediated translocation. Mol Microbiol 62: 1203-1214.
19. Ghosh, J., Anderson, P.J., Chandrasekaran, S., and Caparon, M.G. (2010) Characterization of Streptococcus pyogenes beta-NAD+ glycohydrolase: re-evaluation of enzymatic properties associated with pathogenesis. J Biol Chem 285: 5683-5694.
20. Gibson, B.A., and Kraus, W.L. (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol 13: 411-424.
21. Goldmann, O., Sastalla, I., Wos-Oxley, M., Rohde, M., and Medina, E. (2009) Streptococcus pyogenes induces oncosis in macrophages through the activation of an inflammatory programmed cell death pathway. Cell Microbiol 11: 138-155.
22. Grushoff, P.S., Shany, S., and Bernheimer, A.W. (1975) Purification and properties of streptococcal nicotinamide adenine dinucleotide glycohydrolase. J Bacteriol 122: 599-605.
23. Harder, J., Franchi, L., Munoz-Planillo, R., Park, J.H., Reimer, T., and Nunez, G. (2009) Activation of the Nlrp3 inflammasome by Streptococcus pyogenes requires streptolysin O and NF-kappa B activation but proceeds independently of TLR signaling and P2X7 receptor. J Immunol 183: 5823-5829.
24. Hassa, P.O., and Hottiger, M.O. (1999) A role of poly (ADP-ribose) polymerase in NF-kappaB transcriptional activation. Biol Chem 380: 953-959.
25. Jayaram, H.N., Kusumanchi, P., and Yalowitz, J.A. (2011) NMNAT expression and its relation to NAD metabolism. Curr Med Chem 18: 1962-1972.
26. Johansson, L., Snall, J., Sendi, P., Linner, A., Thulin, P., Linder, A., etal. (2014) HMGB1 in severe soft tissue infections caused by Streptococcus pyogenes. Front Cell Infect Microbiol 4: 4.
27. Koch-Nolte, F., Fischer, S., Haag, F., and Ziegler, M. (2011) Compartmentation of NAD+-dependent signalling. FEBS Lett 585: 1651-1656.
28. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
29. Langelier, M.F., Planck, J.L., Roy, S., and Pascal, J.M. (2011) Crystal structures of poly(ADP-ribose) polymerase-1 (PARP-1) zinc fingers bound to DNA: structural and functional insights into DNA-dependent PARP-1 activity. J Biol Chem 286: 10690-10701.
30. Leckman, J.F., King, R.A., Gilbert, D.L., Coffey, B.J., Singer, H.S., Dure, L.S.T., etal. (2011) Streptococcal upper respiratory tract infections and exacerbations of tic and obsessive-compulsive symptoms: a prospective longitudinal study. J Am Acad Child Adolesc Psychiatry 50: 108-118.e3.
31. Los, F.C., Randis, T.M., Aroian, R.V., and Ratner, A.J. (2013) Role of pore-forming toxins in bacterial infectious diseases. Microbiol Mol Biol Rev 77: 173-207.
32. Luo, X., and Kraus, W.L. (2012) On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev 26: 417-432.
33. Madden, J.C., Ruiz, N., and Caparon, M. (2001) Cytolysin-mediated translocation (CMT): a functional equivalent of type III secretion in gram-positive bacteria. Cell 104: 143-152.
34. Magassa, N., Chandrasekaran, S., and Caparon, M.G. (2010) Streptococcus pyogenes cytolysin-mediated translocation does not require pore formation by streptolysin O. EMBO Rep 11: 400-405.
35. Meehl, M.A., Pinkner, J.S., Anderson, P.J., Hultgren, S.J., and Caparon, M.G. (2005) A novel endogenous inhibitor of the secreted streptococcal NAD-glycohydrolase. PLoS Pathog 1: e35.
36. Mendoza-Alvarez, H., and Alvarez-Gonzalez, R. (1993) Poly(ADP-ribose) polymerase is a catalytic dimer and the automodification reaction is intermolecular. J Biol Chem 268: 22575-22580.
37. Messmer, D., Yang, H., Telusma, G., Knoll, F., Li, J., Messmer, B., etal. (2004) High mobility group box protein 1: an endogenous signal for dendritic cell maturation and Th1 polarization. J Immunol 173: 307-313.
38. Michos, A., Gryllos, I., Hakansson, A., Srivastava, A., Kokkotou, E., and Wessels, M.R. (2006) Enhancement of streptolysin O activity and intrinsic cytotoxic effects of the group A streptococcal toxin, NAD-glycohydrolase. J Biol Chem 281: 8216-8223.
39. Nossa, C.W., Jain, P., Tamilselvam, B., Gupta, V.R., Chen, L.F., Schreiber, V., etal. (2009) Activation of the abundant nuclear factor poly(ADP-ribose) polymerase-1 by Helicobacter pylori. Proc Natl Acad Sci USA 106: 19998-20003.
40. Radin, J.N., Gonzalez-Rivera, C., Ivie, S.E., McClain, M.S., and Cover, T.L. (2011) Helicobacter pylori VacA induces programmed necrosis in gastric epithelial cells. Infect Immun 79: 2535-2543.
41. Ratner, A.J., Hippe, K.R., Aguilar, J.L., Bender, M.H., Nelson, A.L., and Weiser, J.N. (2006) Epithelial cells are sensitive detectors of bacterial pore-forming toxins. J Biol Chem 281: 12994-12998.
42. Riddle, D.J., Bessen, D.E., and Caparon, M.G. (2010) Variation in Streptococcus pyogenes NAD+ glycohydrolase is associated with tissue tropism. J Bacteriol 192: 3735-3746.
43. Samal, B., Sun, Y., Stearns, G., Xie, C., Suggs, S., and McNiece, I. (1994) Cloning and characterization of the cDNA encoding a novel human pre-B-cell colony-enhancing factor. Mol Cell Biol 14: 1431-1437.
44. Scaffidi, P., Misteli, T., and Bianchi, M.E. (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418: 191-195.
45. Shepard, L.A., Heuck, A.P., Hamman, B.D., Rossjohn, J., Parker, M.W., Ryan, K.R., etal. (1998) Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens perfringolysin O: an alpha-helical to beta-sheet transition identified by fluorescence spectroscopy. Biochemistry 37: 14563-14574.
46. Stevens, D.L., Salmi, D.B., McIndoo, E.R., and Bryant, A.E. (2000) Molecular epidemiology of nga and NAD glycohydrolase/ADP-ribosyltransferase activity among Streptococcus pyogenes causing streptococcal toxic shock syndrome. J Infect Dis 182: 1117-1128.
47. Sumby, P., Porcella, S.F., Madrigal, A.G., Barbian, K.D., Virtaneva, K., Ricklefs, S.M., etal. (2005) Evolutionary origin and emergence of a highly successful clone of serotype M1 group a Streptococcus involved multiple horizontal gene transfer events. J Infect Dis 192: 771-782.
48. Tatsuno, I., Sawai, J., Okamoto, A., Matsumoto, M., Minami, M., Isaka, M., etal. (2007) Characterization of the NAD-glycohydrolase in streptococcal strains. Microbiology 153: 4253-4260.
49. Timmer, A.M., Timmer, J.C., Pence, M.A., Hsu, L.C., Ghochani, M., Frey, T.G., etal. (2009) Streptolysin O promotes group A Streptococcus immune evasion by accelerated macrophage apoptosis. J Biol Chem 284: 862-871.
50. Virag, L., Robaszkiewicz, A., Vargas, J.M., and Javier Oliver, F. (2013) Poly(ADP-ribose) signaling in cell death. Mol Aspects Med 34: 1153-1167.
51. Walev, I., Hombach, M., Bobkiewicz, W., Fenske, D., Bhakdi, S., and Husmann, M. (2002) Resealing of large transmembrane pores produced by streptolysin O in nucleated cells is accompanied by NF-kappaB activation and downstream events. FASEB J 16: 237-239.
52. Walker, M.J., Barnett, T.C., McArthur, J.D., Cole, J.N., Gillen, C.M., Henningham, A., etal. (2014) Disease manifestations and pathogenic mechanisms of group a Streptococcus. Clin Microbiol Rev 27: 264-301.
53. Wang, Y., Kim, N.S., Haince, J.F., Kang, H.C., David, K.K., Andrabi, S.A., etal. (2011) Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase-1-dependent cell death (parthanatos). Sci Signal 4: ra20.
54. Weerasinghe, P., and Buja, L.M. (2012) Oncosis: an important non-apoptotic mode of cell death. Exp Mol Pathol 93: 302-308.
55. Yang, W.S., Park, S.O., Yoon, A.R., Yoo, J.Y., Kim, M.K., Yun, C.O., and Kim, C.W. (2006) Suicide cancer gene therapy using pore-forming toxin, streptolysin O. Mol Cancer Ther 5: 1610-1619.
56. Yu, Z., Kuncewicz, T., Dubinsky, W.P., and Kone, B.C. (2006) Nitric oxide-dependent negative feedback of PARP-1 trans-activation of the inducible nitric-oxide synthase gene. J Biol Chem 281: 9101-9109.
57. Yuan, J., Adamski, R., and Chen, J. (2010) Focus on histone variant H2AX: to be or not to be. FEBS Lett 584: 3717-3724.
58. Zhang, S., Lin, Y., Kim, Y.S., Hande, M.P., Liu, Z.G., and Shen, H.M. (2007) c-Jun N-terminal kinase mediates hydrogen peroxide-induced cell death via sustained poly(ADP-ribose) polymerase-1 activation. Cell Death Differ 14: 1001-1010.
59. Zhang, T., Berrocal, J.G., Yao, J., DuMond, M.E., Krishnakumar, R., Ruhl, D.D., etal. (2012) Regulation of poly(ADP-ribose) polymerase-1-dependent gene expression through promoter-directed recruitment of a nuclear NAD+ synthase. J Biol Chem 287: 12405-12416.