IndraLab

Statements



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"GAS genome harboring an NADase/SLO complex-defective mutation impairs SLO-mediated translocation of NADase and resistance to phagocytic killing in vitro."

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"A specific NADase-SLO interaction contributes to the pathogenesis of GAS in a mouse infection model."

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"The over-length cross-links indicate that domain 4 in SLO is subjected to dynamic movement, where a similar domain movement has recently been reported for the SLO-NADase complex xref ."

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"Emergence of a globally dominant invasive GAS M-type 1 clone in the 1980s was temporally associated with acquisition of DNA sequences encoding enzymatically active NADase and a highly active promoter driving expression of the NADase-SLO operon [ xref , xref ]."

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"A new paradigm for the interaction of NADase and SLO was proposed by Madden et al ., who found that NADase could be translocated into the cytosol of epithelial cells in vitro after its secretion from GAS bound to the cell surface [ xref ]."

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"Translocation required the concomitant expression of SLO, which suggested a model in which NADase associates with SLO on the epithelial cell surface and is transferred across the cell membrane in a process dependent on SLO."

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"Ab initio molecular envelopes were generated to depict the overall architecture of NADase and NADase/SLO complex (Fig. 3c)."

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"To further understand the structural details of how the N-terminal translocation domain of NADase, which is missing in our determined crystal structure, interacts with SLO, we performed SAXS-based atomistic modeling of the full-length NADase and NADase/SLO complex."

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"SLO and NADase physically interact and co-stabilize after secretion xref ."

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"Streptococcal strain emergence and epidemicity has been associated with a high-activity promoter recombination event at the NADaseSLO locus which results in increased expression of the NADase and SLO toxins xref , xref , xref , xref ."

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"How NADase interacts with SLO to synergistically promote GAS cytotoxicity and intracellular survival is a long-standing question."

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"We conclude that binding of NADase to SLO stabilizes both toxins, thereby enhancing GAS virulence."

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"SLO and NADase interact in solution as a heterodimer with 1:1 stoichiometry."

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"This study characterizes the binding interaction between NADase and SLO and reports that the expression of each toxin is crucial for maximal expression and stability of the other."

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"These observations provide an explanation for conservation of full-length NADase expression even when it lacks enzymatic activity and suggest a critical role for binding of NADase to SLO in GAS pathogenesis."

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"Structure-guided studies reveal a salt-bridge interaction between NADase and SLO is important to cytotoxicity and resistance to phagocytic killing during GAS infection."

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"Moreover, it is suggested that direct interaction and mutual stabilization between NADase and SLO are crucial for enhancing GAS virulence xref , signifying the importance of the NADase/SLO complex formation in GAS pathogenesis."

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"However, the manner in which NADase interacts with SLO to exert the synergistic effects is a long-standing question."

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"To reveal atomic interactions between NADase and SLO by X-ray crystallography, initial crystallization screening was performed on mature (signal sequence truncated) full length NADase/SLO and NADase G330D /SLO complexes but failed to yield hits."

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"The overall structure of the NADase 193-451,G330D /SLO 106-574 heterodimer exhibits an elongated shape with the C-terminal domain 4 of SLO bound to the C-terminal enzymatic domain of NADase."

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"The structure of SLO-bound NADase 193-451,G330D superimposes well with the structure of NADase 193-451 in complex with IFS (PDB 4KT6), with a root-mean-square deviation (RMSD) of 0.518 Å for 212 aligned C α atoms, suggesting the common polymorphism G330D does not affect the global structure of the NADase enzymatic domain (Supplementary Fig.  xref )."

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"However, the effect of disrupting specific interactions between NADase and SLO on the pathogenic abilities of GAS has not been tested, and can only be tested in an informed manner when structural information is available."

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"To evaluate the impact of the NADase-SLO interaction on GAS cytotoxicity, we first assessed the contribution of the salt-bridge to NADase translocation into host cells during bacterium-host cell interaction via SLO-mediated translocation known as CMT xref ; an essential step for GAS to exert its full cytotoxic potential."

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"These findings suggested that the NADase-SLO interaction contributes to the survival within phagocytes."

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"Specifically, we studied the interaction of NADase with its cotoxin, SLO."

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"Our data suggested an interaction between SLO and NADase in the culture supernatant, likely after secretion of the toxins, leading to mutual protection from further processing or degradation."

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"NADase-SLO synergism utilized by GAS serves as a unique example that two secreted toxins of Gram-positive bacteria interact and act in a concerted manner."

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"Prior to this work, it was not understood how NADase and SLO assemble into a complex to accomplish these tasks and how NADase-SLO interactions correlate with their synergistic functions."

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"When NADase and pneumolysin were loaded on the column together, no shift in the NADase elution volume was observed, suggesting a lack of interaction with pneumolysin ( xref ) and specificity of NADase binding to SLO."

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"The second phase could represent nonspecific binding, or it could reflect two domains of NADase interacting with SLO or a conformational change induced by the initial interaction ( xref )."

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"In this study, we tested that hypothesis by examining the physical and functional interactions between SLO and NADase."

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"In the present investigation, we used analytical gel filtration to detect binding in solution between SLO and full-length NADase, as well as binding of SLO to the catalytic domain of NADase (190NADase) at micromolar concentrations."

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"We used BLI to investigate in more detail the interaction between NADase and SLO."

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"BLI data for the interaction of full-length NADase with SLO fit a binding model with two phases."

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"We therefore propose that the interaction between SLO and NADase in solution stabilizes both toxins and represents an important early step of CMT."

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"Secreted NADase and SLO interact to stabilize each other in the extracellular environment xref ."

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"Production of both NADase and SLO is associated with augmented host cell injury beyond that produced by SLO alone, but the mechanism of enhanced cytotoxicity is not known."

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"Purified recombinant SLO bound NADase in vitro, supporting a specific, physical interaction of the two proteins."

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"This successful clade is characterized by the absence of the hasABC locus and the presence of an nga-ifs-slo locus variant associated with increased expression of NADase and SLO, possibly acquired from emm 1 or emm 12 strains by horizontal gene transfer ( xref , xref )."

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"The atomic details of the NADase 193-451,G330D /SLO 106-574 complex determined by X-ray crystallography in this study (Figs.  xref and xref ) allow us to design experiments to evaluate the importance of specific NADase-SLO interactions in GAS virulence by introducing point mutations in the GAS genome rather than gene deletion."

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"The relative mobility of the N- and C-terminal domains of NADase and the large dynamic motion of the SLO N-terminus add to the complexity to the NADase-SLO interaction."

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"Our structural information presented here may open up an opportunity for the design of alternative agents to perturb the NADase-SLO interaction to suppress GAS virulence."

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"These findings showed the NADase-SLO salt-bridge interaction contributes to the virulence of GAS during infections."

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"Our data are consistent with a model whereby interactions of the NADase glycohydrolase domain and translocation domain with SLO and the cell surface increase avidity of NADase binding and facilitate toxin-toxin and toxin-cell surface interactions."

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"In human epithelial keratinocytes exposed to GAS in vitro , SLO and NADase production is associated with increased GAS intracellular survival ( xref , xref )."

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"A new paradigm for the interaction of NADase and SLO was proposed by Madden et al., who found that NADase could be translocated into the cytosol of epithelial cells in vitro after its secretion from GAS bound to the cell surface [XREF_BIBR]."

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"Translocation required the concomitant expression of SLO, which suggested a model in which NADase associates with SLO on the epithelial cell surface and is transferred across the cell membrane in a process dependent on SLO."

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"Purified recombinant SLO bound NADase in vitro, supporting a specific, physical interaction of the two proteins."

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"A20 exhibited a higher level of NADase translocation than A20 during GAS-A549 infection (Fig. 4e), demonstrating the salt bridge at the NADase/SLO complex interface plays a key role in NADase translocation.To study the impact of the complex-defective mutation on GAS resistance to phagocytic killing, differentiated U937 cells were infected with A20, A20 , or A20 at an MOI of 50, and the bacterial survival inside phagocytic cells was assessed (Fig. 4f)."

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"To further assess the biological importance of the salt bridge interaction for NADase/SLO complex formation in the pathogenesis of GAS during infections, mice were subjected to an air-pouch model of subcutaneous infection with A20 or A20 (n = 8 for each GAS strain)."

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"Structure-guided studies reveal a salt-bridge interaction between NADase and SLO is important to cytotoxicity and resistance to phagocytic killing during GAS infection."

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"Furthermore, the biological significance of the NADase/SLO complex in GAS virulence is demonstrated in a murine infection model."

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"Overall, this work delivers the structure-functional relationship of the NADase/SLO complex and pinpoints the key interacting residues that are central to the coordinated actions of NADase and SLO in the pathogenesis of GAS infection."

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"Moreover, it is suggested that direct interaction and mutual stabilization between NADase and SLO are crucial for enhancing GAS virulence , signifying the importance of the NADase/SLO complex formation in GAS pathogenesis.NADase and SLO are functionally-interdependent during GAS infection."

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"However, NADase remains a potent virulence factor and is able to interact with SLO similarly to the wild type , suggesting the molecular evolution of NADase has a tendency for preservation of the NADase/SLO complex.The synergistic activities of NADase and SLO through physical association is a unique example among Gram-positive bacteria, as secreted toxins generally function exclusively."

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"Here, the structure of the NADase/SLO complex is presented, obtained using X-ray crystallography and small-angle scattering."

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"The atomic details allow us to identify key interacting residues and demonstrate the biological importance of the NADase/SLO complex to the pathogenesis of GAS infection in vitro and in a mouse model."

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"To reveal atomic interactions between NADase and SLO by X-ray crystallography, initial crystallization screening was performed on mature (signal sequence truncated) full length NADase/SLO and NADase /SLO complexes but failed to yield hits."

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"The overall structure of the NADase /SLO heterodimer exhibits an elongated shape with the C-terminal domain 4 of SLO bound to the C-terminal enzymatic domain of NADase.The structure of SLO-bound NADase superimposes well with the structure of NADase in complex with IFS (PDB 4KT6), with a root-mean-square deviation (RMSD) of 0."

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"To verify the dissociation of NADase/SLO complex was due to the salt-bridge disruption rather than a major structural change of NADase caused by the point mutation, the NADase activity assay was performed."

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"Small-angle scattering studies on the NADase/SLO complex."

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"To gain structural insights into the missing structural elements required for CMT activity, we conducted small-angle X-ray and neutron scattering (SAXS and SANS) on mature full-length NADase and the NADase/SLO complex."

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"SAXS data collected from NADase and the NADase/SLO complex showed a linear behavior in the Guinier region consistent with a monodisperse solution of macromolecules (Fig. 3a; Supplementary Fig. 5a, b and Supplementary Table 1)."

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"Furthermore, we demonstrate that disruption of the NADase-SLO interaction can affect the outcomes of GAS infection in vitro and in our mouse model."

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"For over a decade, the biological relevance of the NADase-SLO interaction in GAS pathogenesis could only be demonstrated by deletion of either toxin or both xref , xref , xref , xref , xref due to the lack of structural information."

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"A recent study suggests that binding of NADase to SLO stabilizes both toxins, thereby increasing host cell toxicity [ xref ]."

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"Here, the structure and dynamic nature of the NADase/SLO complex are elucidated by X-ray crystallography and small-angle scattering, illustrating atomic details of the complex interface and functionally relevant conformations."

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"Overall, SAXS studies reveal functionally-relevant conformations of the NADase/SLO complex and suggest the dynamic interplay between SLO and NADase is fundamental to the functioning of the complex and the molecular clues provided here will be beneficial for future studies to dissect the mechanistic actions of NADase and SLO in CMT.Taken together, this work delivers structural insight into the synergism of NADase and SLO in GAS pathogenesis and fills a current knowledge gap in the literature."

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"In addition to SAXS studies, we attempted to visualize each protein within the NADase/SLO complex by SANS with contrast variation, where the measurements were designed such that SLO would be contrast matched in 42% D O and the deuterium labelled NADase would be contrast matched in 100% D O."

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"We conclude that binding of NADase to SLO stabilizes both toxins, thereby enhancing GAS virulence."

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"The column was calibrated with proteins of standard masses, and the Stokes radius of NADase alone and the NADase and SLO complex were determined to be consistent with globular protein masses of 59.5 kDa (predicted molecular mass, 47.2 kDa) and 136.3 kDa (predicted molecular mass of SLO + NADase, 110kDa), respectively."

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"Thus, the SANS provides additional support that the NADase/SLO complex exhibits dynamic behavior, involving a rigid NADase/SLO core structure with dynamic peripheral domains.The multistate ensemble of the NADase/SLO complex shows two distinct conformations adopted by the SLO N-terminal disordered region and the NADase N-terminal domain."

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"When NADase and pneumolysin were loaded on the column together, no shift in the NADase elution volume was observed, suggesting a lack of interaction with pneumolysin (XREF_FIG) and specificity of NADase binding to SLO."

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"SEC-MALS analysis of the NADase and SLO complex at the same concentrations again revealed a shift in the NADase elution volume and a calculated average mass for the NADase and SLO complex of 83kDa."

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"In this study, we tested that hypothesis by examining the physical and functional interactions between SLO and NADase."

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"We used BLI to investigate in more detail the interaction between NADase and SLO."

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"This structural ensemble of the NADase/SLO complex indicates why the N-terminal translocation domain is dispensable for the complex formation but is required for the maximal binding of NADase to SLO and for the SLO-mediated translocation of NADase."

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"The full-length NADase was combined with the full-length SLO model to build an initial full-length model of NADase/SLO complex for further SAXS-based modeling."

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"The dimensionless Kratky plot of NADase/SLO complex also showed a peak shift to the right with a maxima >1.104 suggestive of flexibility (Supplementary Fig. 5c)."

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"A multistate model with 9% of compact and 53% of extended state, together with 38% of free NADase, fits well with the SAXS data and comprehensively describes the solution state of NADase/SLO complex (Fig. 3a, c)."

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"The presence of free NADase in the structural ensemble is attributed to the known behavior of partial dissociation of NADase/SLO complex in solution ."

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"The dissociation of NADase/SLO was confirmed by multi-angle light scattering coupled with SEC (SEC-MALS) (Supplementary Fig. 6) that showed the molecular weight of the NADase/SLO complex is ~90 kDa, lower than the expected mass of ~110 kDa and consistent with a previous report ."

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"As the dissociation process of a protein complex often occurs through a number of transition events involving low surface area contact interfaces , the compact-to-extended state transition could be interpreted as the first step of the dissociation process of the NADase/SLO complex."

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"This may suggest that the dynamic motions of the N-terminal domain of NADase and the N-terminal disordered region of SLO are functionally linked to the CMT activity which involves the separation of NADase from SLO.Mapping the polymorphic residues of NADase identified from clinical isolates on the full-length structural model of the NADase/SLO complex reveals the polymorphisms are distant from the complex interface (Supplementary Fig. 8a), supporting the notion that the preservation of the NADase/SLO complex plays an important role in the molecular evolution of NADase ."

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"These residues are located at the solvent-exposed area in the NADase/SLO multistate model (Supplementary Fig. 8b), showing the structural ensemble of the NADase/SLO complex is competent for binding to cell surface glycans and is functionally relevant."

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"Taken together, the small-angle scattering studies reveal the dynamic nature and functional conformations of the NADase/SLO complex, and provide molecular insight into the evolution of NADase."

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"However, the effect of disrupting specific interactions between NADase and SLO on the pathogenic abilities of GAS has not been tested, and can only be tested in an informed manner when structural information is available."

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"Additionally, structural analyses on the full-length atomistic models of the NADase/SLO complex suggest that both compact and extended states are competent in NADase-mediated glycan-binding (Supplementary Fig. 8b) and that the interface interaction is conserved in the molecular evolution of NADase (Supplementary Fig. 8a)."

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"Overall, the results from this mouse infection study reveals the significance of the ionic interaction at the NADase/SLO complex interface in GAS pathogenesis."

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"Here, we uncover the molecular structure of the NADase/SLO complex, revealing that a salt bridge formed between NADase D315 and SLO R531 is fundamental for the interface interaction and that conformational dynamics play an important role to the functioning of the complex."

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"Our studies convey the structure-functional relationship of the NADase/SLO complex underpinning the augmented virulence of GAS.For over a decade, the biological relevance of the NADase-SLO interaction in GAS pathogenesis could only be demonstrated by deletion of either toxin or both due to the lack of structural information."

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"Furthermore, the significance of NADase/SLO complex formation on the pathogenesis of GAS infection is directly demonstrated in the murine model of skin infection (Fig. 5)."

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"The compact state displays a physical association between the NADase N-terminal domain and SLO and this larger contact surface area provides a structural basis for strong binding of NADase to SLO ."

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"NADase (12.3 mg/ml) and NADase/SLO complex (15.1 mg/ml) were subjected to SEC-SAXS ."