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Structural basis for binding of Drosophila Smaug to the GPCR Smoothened and to the germline inducer Oskar

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Kubíková, Jana, Ubartaitė, Gabrielė, Metz, Jutta, Jeske, Mandy·2023·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.2304385120PMC PMC10410706

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Abstract

Drosophila Smaug and its orthologs comprise a family of mRNA repressor proteins that exhibit various functions during animal development. Smaug proteins contain a characteristic RNA-binding sterile-α motif (SAM) domain and a conserved but uncharacterized N-terminal domain (NTD). Here, we resolved the crystal structure of the NTD of the human SAM domain-containing protein 4A (SAMD4A, a.k.a. Smaug1) to 1.6 Å resolution, which revealed its composition of a homodimerization D subdomain and a subdomain with similarity to a pseudo-HEAT-repeat analogous topology (PHAT) domain. Furthermore, we show that Drosophila Smaug directly interacts with the Drosophila germline inducer Oskar and with the Hedgehog signaling transducer Smoothened through its NTD. We determined the crystal structure of the NTD of Smaug in complex with a Smoothened α-helical peptide to 2.0 Å resolution. The peptide binds within a groove that is formed by both the D and PHAT subdomains. Structural modeling supported by experimental data suggested that an α-helix within the disordered region of Oskar binds to the NTD of Smaug in a mode similar to Smoothened. Together, our data uncover the NTD of Smaug as a peptide-binding domain.

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Figures

Fig. 1. Crystal structure of the NTD of human SAMD4A. (A) Domain organization of Drosophila Smaug and human SAMD4A proteins. SSR, Smaug similarity region; NTD, N-terminal domain. The horizontal orange or yellow lines below the protein schemes indicate insertions into the respective PHAT domains. (B) Crystal structure of the NTD dimer of the human SAMD4A. The D subdomain, the PHAT1 subdomain, and the linker α-helix are indicated. (C) Structural superimposition of the D subdomains of SAMD4A onto the D domain of β-TrCP1 (Left) and of the PHAT1 domain of SAMD4A onto the PHAT2 domain of Smaug (Right). PDB codes are indicated in parentheses. (D) Details of the D subdomain dimer interface of SAMD4A. Amino acid residues are labeled for one protein chain only. Residues in bold are 100% conserved across animals. The orientation of the structure is relative to the one depicted in the Upper panel of Fig. 1B. (E) Details of the interface formed by the D and the PHAT1 subdomains. Residues in bold are 100% conserved across animals. The orientation of the structure is relative to the one depicted in the Upper panel of Fig. 1B. (F) Structural comparison between the D-PHAT1 domain of SAMD4A and the SAM-PHAT2 domain of Smaug. SRE, Smaug recognition elements. The model of the SAM-PHAT2 domain–SRE complex was prepared by superimposition of the two crystal structures indicated by the PDB codes in parenthesis. (G) Structural detail indicating the position of the H86 residue, which is mutated in spmd mice.
Fig. 1. Crystal structure of the NTD of human SAMD4A. (A) Domain organization of Drosophila Smaug and human SAMD4A proteins. SSR, Smaug similarity region; NTD, N-terminal domain. The horizontal orange or yellow lines below the protein schemes indicate insertions into the respective PHAT domains. (B) Crystal structure of the NTD dimer of the human SAMD4A. The D subdomain, the PHAT1 subdomain, and the linker α-helix are indicated. (C) Structural superimposition of the D subdomains of SAMD4A onto the D domain of β-TrCP1 (Left) and of the PHAT1 domain of SAMD4A onto the PHAT2 domain of Smaug (Right). PDB codes are indicated in parentheses. (D) Details of the D subdomain dimer interface of SAMD4A. Amino acid residues are labeled for one protein chain only. Residues in bold are 100% conserved across animals. The orientation of the structure is relative to the one depicted in the Upper panel of Fig. 1B. (E) Details of the interface formed by the D and the PHAT1 subdomains. Residues in bold are 100% conserved across animals. The orientation of the structure is relative to the one depicted in the Upper panel of Fig. 1B. (F) Structural comparison between the D-PHAT1 domain of SAMD4A and the SAM-PHAT2 domain of Smaug. SRE, Smaug recognition elements. The model of the SAM-PHAT2 domain–SRE complex was prepared by superimposition of the two crystal structures indicated by the PDB codes in parenthesis. (G) Structural detail indicating the position of the H86 residue, which is mutated in spmd mice.CC BY-NC-ND · PubMed Central
Fig. 2. The Smaug–Smoothened interaction. (A) Domain organization of Drosophila Smaug and Smoothened proteins. DR, disordered region; TM, transmembrane; SBR, Smaug-binding region. (B) ReLo assays showed a colocalization between Smaug and Smoothened. Controls are plasmids without an insert. (The scale bar is 10 µm.) (C) Of the four Smaug fragments indicated, only the NTD (Smaug 1-281) interacted with the Smoothened cytotail (Smo 556-1036) in the ReLo assay. (The scale bar is 10 µm.) (D) The Smoothened deletion and the Smaug deletion were unable to interact with Smaug and Smoothened, respectively, in the ReLo assay. (The scale bar is 10 µm.) (E) ITC using Smaug NTD (aa 70-281, His-tag removed) and a Smoothened peptide (Smo 970-1003).
Fig. 2. The Smaug–Smoothened interaction. (A) Domain organization of Drosophila Smaug and Smoothened proteins. DR, disordered region; TM, transmembrane; SBR, Smaug-binding region. (B) ReLo assays showed a colocalization between Smaug and Smoothened. Controls are plasmids without an insert. (The scale bar is 10 µm.) (C) Of the four Smaug fragments indicated, only the NTD (Smaug 1-281) interacted with the Smoothened cytotail (Smo 556-1036) in the ReLo assay. (The scale bar is 10 µm.) (D) The Smoothened deletion and the Smaug deletion were unable to interact with Smaug and Smoothened, respectively, in the ReLo assay. (The scale bar is 10 µm.) (E) ITC using Smaug NTD (aa 70-281, His-tag removed) and a Smoothened peptide (Smo 970-1003).CC BY-NC-ND · PubMed Central
Fig. 3. Crystal structure of Smaug-NTD in complex with Smoothened. (A) Crystal structure of the NTD of Drosophila Smaug in complex with a Smoothened peptide (colored deep teal). (B) Structural detail of the Smaug–Smoothened interface. (C) Sequence alignment of the Smaug-binding region of Smoothened. Orange triangles indicate central residues involved in the Smaug interaction. (D) GST pull-down assay using 1 nmol GST-Smoothened 970-1003 (SBR) wild-type (WT) or L978E/L984E/L985E mutant (MUT) proteins and 2 nmol Smaug 70-281 (His-tag removed). Protein markers in kDa are indicated on the left. Input and pull-down samples originated from one experiment; the gel was split as it contained also the data shown in SI Appendix, Fig. S6D. (E) Mutant Smoothened SBR (MUT; L978E/L984E/L985E) did not interact with the NTD of Smaug, and mutant Smaug NTD (MUT; S250E/L253E) did not interact with the Smoothened cytotail in the ReLo assay. (The scale bar is 10 µm.) (F) GST pull-down assay using 1 nmol GST or GST-Smoothened SBR (970-1003) and 1 nmol Smaug NTD (70-281) wild-type or S250E/L253E mutant proteins (His-tag removed). Protein markers in kDa are indicated on the left. Input and pull-down samples originated from one experiment but were loaded onto two gels.
Fig. 3. Crystal structure of Smaug-NTD in complex with Smoothened. (A) Crystal structure of the NTD of Drosophila Smaug in complex with a Smoothened peptide (colored deep teal). (B) Structural detail of the Smaug–Smoothened interface. (C) Sequence alignment of the Smaug-binding region of Smoothened. Orange triangles indicate central residues involved in the Smaug interaction. (D) GST pull-down assay using 1 nmol GST-Smoothened 970-1003 (SBR) wild-type (WT) or L978E/L984E/L985E mutant (MUT) proteins and 2 nmol Smaug 70-281 (His-tag removed). Protein markers in kDa are indicated on the left. Input and pull-down samples originated from one experiment; the gel was split as it contained also the data shown in SI Appendix, Fig. S6D. (E) Mutant Smoothened SBR (MUT; L978E/L984E/L985E) did not interact with the NTD of Smaug, and mutant Smaug NTD (MUT; S250E/L253E) did not interact with the Smoothened cytotail in the ReLo assay. (The scale bar is 10 µm.) (F) GST pull-down assay using 1 nmol GST or GST-Smoothened SBR (970-1003) and 1 nmol Smaug NTD (70-281) wild-type or S250E/L253E mutant proteins (His-tag removed). Protein markers in kDa are indicated on the left. Input and pull-down samples originated from one experiment but were loaded onto two gels.CC BY-NC-ND · PubMed Central
Fig. 4. The Smaug–Short Oskar interaction. (A) Domain organization of Drosophila Smaug and Oskar. The Short Oskar isoform is generated by alternate translation from M139 onward. NTD, N-terminal domain; DR, disordered region; SBR, Smaug-binding region. (B) Smaug interacted with Short Oskar but not Long Oskar in the ReLo assay. Plasmids lacking an insert served as controls. (The scale bar is 10 µm.) (C) Oskar (only the short isoform was tested) and Smaug interacted in split-ubiquitin yeast two-hybrid (Y2H) assays (Upper). Short Oskar binding mapped to the NTD of Smaug (Lower). Ten-fold dilutions are shown. Selection plates lacked adenine and histidine as compared to control plates. (D) The NTD of Smaug bound to the DR of Short Oskar in Y2H assays. Ten-fold dilutions are shown. Selection plates lacked adenine and histidine as compared to control plates. (E) Oskar 292-352 (SBR) was necessary and sufficient for Smaug-NTD binding in Y2H assays. Ten-fold dilutions are shown. Selection plates lacked adenine and histidine as compared to control plates. (F) MBP pull-down assay using 1 nmol His-MBP-Oskar 292-325 and 5 nmol Smaug NTD (37 to 281; His-tag removed). Input and pull-down samples originated from one experiment; the gel was split into two panels as it contained additional data irrelevant to the study.
Fig. 4. The Smaug–Short Oskar interaction. (A) Domain organization of Drosophila Smaug and Oskar. The Short Oskar isoform is generated by alternate translation from M139 onward. NTD, N-terminal domain; DR, disordered region; SBR, Smaug-binding region. (B) Smaug interacted with Short Oskar but not Long Oskar in the ReLo assay. Plasmids lacking an insert served as controls. (The scale bar is 10 µm.) (C) Oskar (only the short isoform was tested) and Smaug interacted in split-ubiquitin yeast two-hybrid (Y2H) assays (Upper). Short Oskar binding mapped to the NTD of Smaug (Lower). Ten-fold dilutions are shown. Selection plates lacked adenine and histidine as compared to control plates. (D) The NTD of Smaug bound to the DR of Short Oskar in Y2H assays. Ten-fold dilutions are shown. Selection plates lacked adenine and histidine as compared to control plates. (E) Oskar 292-352 (SBR) was necessary and sufficient for Smaug-NTD binding in Y2H assays. Ten-fold dilutions are shown. Selection plates lacked adenine and histidine as compared to control plates. (F) MBP pull-down assay using 1 nmol His-MBP-Oskar 292-325 and 5 nmol Smaug NTD (37 to 281; His-tag removed). Input and pull-down samples originated from one experiment; the gel was split into two panels as it contained additional data irrelevant to the study.CC BY-NC-ND · PubMed Central
Fig. 5. Predicted structure of Smaug-NTD in complex with the Oskar SBR. (A) Structural model of the Drosophila Smaug-NTD in complex with the Oskar-SBR (blue) generated using AlphaFold2-multimer-version3 (58–60). The model contains the Drosophila-specific insertion (aa 156-196) of the Smaug-NTD. (B) Predicted aligned error plot generated from the prediction run, showing a low positional error of the N-terminal part of the Oskar-SBR relative to the Smaug-NTD. (C) Sequence alignment of Oskar covering the SBR. Orange triangles indicate Oskar residues that are critical for Smaug binding based on the predicted structural model. (D) OST4-EGFP and mCherry fusions to the proteins indicated were coexpressed in S2R+ cells, and their localization was analyzed by microscopy. The Smaug MUT (S250E, L253E) and the deletion of the SBR of Oskar (295-352) prevented the Smaug–Oskar interaction. (Scale bar is 10 µm.) (E and F) Yeast two-hybrid assays showing that the Smaug NTD MUT (S250E, L253E) or the deletion of aa 292-306 from the SBR (292-352) of Oskar prevented the Smaug–Oskar interaction. Selection medium lacked adenine and histidine. (G) GST pull-down assay using 1 nmol GST-Smaug 1-281 and 2 nmol His-MBP or His-MBP-Oskar. In addition, 45 nmol of a Smo 907-1003 synthetic peptide with wild-type (W) sequence or carrying the L978E/L984E/L985E point mutations (M) were present during the experiment as indicated above the gel image. Protein markers in kDa are indicated on the left. Input and pull-down samples originated from one experiment but were loaded onto two gels. (H) Surface representation of the Smaug NTD colored according to residue conservation (61) considering sequences of Smaug orthologs from various animals (Left) or Drosophilids only (Right).
Fig. 5. Predicted structure of Smaug-NTD in complex with the Oskar SBR. (A) Structural model of the Drosophila Smaug-NTD in complex with the Oskar-SBR (blue) generated using AlphaFold2-multimer-version3 (58–60). The model contains the Drosophila-specific insertion (aa 156-196) of the Smaug-NTD. (B) Predicted aligned error plot generated from the prediction run, showing a low positional error of the N-terminal part of the Oskar-SBR relative to the Smaug-NTD. (C) Sequence alignment of Oskar covering the SBR. Orange triangles indicate Oskar residues that are critical for Smaug binding based on the predicted structural model. (D) OST4-EGFP and mCherry fusions to the proteins indicated were coexpressed in S2R+ cells, and their localization was analyzed by microscopy. The Smaug MUT (S250E, L253E) and the deletion of the SBR of Oskar (295-352) prevented the Smaug–Oskar interaction. (Scale bar is 10 µm.) (E and F) Yeast two-hybrid assays showing that the Smaug NTD MUT (S250E, L253E) or the deletion of aa 292-306 from the SBR (292-352) of Oskar prevented the Smaug–Oskar interaction. Selection medium lacked adenine and histidine. (G) GST pull-down assay using 1 nmol GST-Smaug 1-281 and 2 nmol His-MBP or His-MBP-Oskar. In addition, 45 nmol of a Smo 907-1003 synthetic peptide with wild-type (W) sequence or carrying the L978E/L984E/L985E point mutations (M) were present during the experiment as indicated above the gel image. Protein markers in kDa are indicated on the left. Input and pull-down samples originated from one experiment but were loaded onto two gels. (H) Surface representation of the Smaug NTD colored according to residue conservation (61) considering sequences of Smaug orthologs from various animals (Left) or Drosophilids only (Right).CC BY-NC-ND · PubMed Central

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Metadata

Authors
Kubíková, J., Ubartaitė, G., Metz, J., & Jeske, M.
Affiliations
Heidelberg University (DE)
Corresponding author
Jeske, Mandy
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2023-07-31
Volume
120
Issue
32
Pages
e2304385120-e2304385120
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.2304385120
PMC
PMC10410706
OpenAlex
W4385409666
Cited by
18
References
2
Citations by year
2026: 1 · 2025: 7 · 2024: 9 · 2023: 1
FWCI
1.60
Type
journal article
Language
en
Open access
Licence
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Desy Publications Database (Deutsches Elektronen-Synchrotron DESY) (submittedVersion, other-oa)
  • DESY Publication Database (PUBDB) (Deutsches Elektronen-Synchrotron)
Funders
Deutsche Forschungsgemeinschaft (JE827/1-1)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
Keywords
Smaug, sterile alpha motif domain, N-terminal domain, Smoothened, Oskar, Hedgehog signaling, peptide binding, protein-protein interaction, Drosophila, crystal structure
MeSH terms
Smoothened Receptor, Animals, Drosophila, Germ Cells, Humans, Repressor Proteins, RNA, Messenger, RNA-Binding Proteins, Drosophila Proteins, Receptors, G-Protein-Coupled, Hedgehog Proteins

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CoChat. (2026). Citation check: Structural basis for binding of Drosophila Smaug to the GPCR Smoothened and to the germline inducer Oskar. https://app.cochat.ai/papers/10.1073/pnas.2304385120
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Kubíková, J., Ubartaitė, G., Metz, J., & Jeske, M. (2023). Structural basis for binding of Drosophila Smaug to the GPCR Smoothened and to the germline inducer Oskar. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.2304385120