Sterical hindrance promotes selectivity of the autophagy cargo receptor NDP52 for the danger receptor galectin-8 in antibacterial autophagy - PubMed (original) (raw)
Sterical hindrance promotes selectivity of the autophagy cargo receptor NDP52 for the danger receptor galectin-8 in antibacterial autophagy
Sai Li et al. Sci Signal. 2013.
Abstract
Autophagy, the process of lysosome-dependent degradation of cytosolic components, is a mechanism by which cells selectively engulf invading pathogens to protect themselves against infection. Galectin-8, a cytosolic protein with specificity for β-galactoside-containing glycans, binds endosomal and lysosomal membranes that have been damaged, for example, by pathogens, and selectively recruits the autophagy cargo receptor NDP52 to induce autophagy. We solved the crystal structure of the NDP52-galectin-8 complex to show how NDP52 exclusively binds galectin-8 and, consequently, why other galectins do not restrict the growth of Salmonella in human cells.
Figures
Figure 1. The molecular basis of the interaction between Gal8C-CRD and NDP52368-381
(A) Cartoon representation of Gal8C-CRD (yellow and grey) in complex with NDP52368-381 (cyan). F1-F5, S1-S6 numbering of β-strands. (B) Hydrophobic contacts between Gal8C-CRD and NDP52368-381. Residues of Gal8C-CRD involved in hydrophobic interaction are colored yellow and labeled in black. NDP52 in cyan. (C) ITC data for the interaction of NDP52368-381and Gal8C-CRD at the indicated peptide versus protein molar ratios. Top, raw data; bottom, integrated heat data. Kd, dissociation constant; N, reaction stoichiometry. (D) Hydrogen bonds between Gal8C-CRD (yellow) and NDP52368-381 (cyan) with distances measured in Ångströms (Å). (E) Dissociation constants for the indicated interactions obtained through ITC. . NB: binding not detectable. (F) Scheme of interactions between NDP52 (blue) and galectin-8 (yellow). Single letter abbreviations indicate mutations tested in this study with colors indicating affinity (red: Kd >120 μM, blue: 27< Kd <41 μM, black: Kd <12 μM). Circled residues occur in human galectin CRDs, squared residues are experimental mutations.
Figure 2. Functional importance of the NDP52 binding site in galectin-8 for anti-bacterial autophagy
(A) LUMIER binding assay. Normalized ratio of luciferase activity bound to anti-Flag beads to luciferase activity in lysates from 293ET cells co-expressing NDP52 fused to luciferase and the indicated Flag-tagged wild-type (WT) or mutated (I312A, A323Y) galectin-8 proteins. (B-C) Percentage of S. Typhimurium exhibiting NDP52 (B) or galectin-8 (C) recruitment at 1 hour post-infection in Hela cells expressing the indicated siRNA-resistant WT or mutated galectin-8 alleles fused to mCherry as determined by fluorescence microscopy. Cells were treated with control siRNA (siControl) or siRNA against galectin-8 (siGal8) (B) or only siGal8 (C).. Mean and s.d. were quantified from quadruplicate cultures (n>200 bacteria per coverslip), and representative confocal images from siGal8-treated cells are shown (D).
Figure 3. The molecular basis for the specificity of NDP52 for galectin-8
(A) For galectins containing two CRDs, N- and C-terminal domains are indicated. Red dots and black triangles indicate residues in Gal8C-CRD that, if mutated, prevented or impaired binding to NDP52368-381, respectively. (B) Close-up view of Gal8 Ala323 (yellow) in contact with the γ-carbon of the NDP52 Pro379 and the ε-carbon and hydroxyl oxygen of the NDP52 Tyr380 side chain (blue and red). Van der Waals volumes of key atoms rendered as transparent spheres. (C) Dissociation constants for the interaction of NDP52368-381 with the indicated Gal8C-CRD variants obtained ITC. NB: binding not detectable.
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References
- Mizushima N, Yoshimori T, Ohsumi Y. The role of atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 2011;27:107–132. - PubMed
- Thurston TLM, Ryzhakov G, Bloor S, von Muhlinen N, Randow F. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat Immunol. 2009;10:1215–1221. - PubMed
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