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Structural characterisation of ligand-binding determinants in human lung surfactant protein D: influence of Asp325.

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Shrive AK, Martin C, Burns I, Paterson JM, Martin JD, Townsend JP, Waters P, Clark HW, Kishore U, Reid KB, Greenhough TJ
OpenAccess logo J Mol Biol 394 776-88 (2009)
Related entries: 1pw9, 1pwb, 3ikn, 3ikp, 3ikr

Cited: 20 times
EuropePMC logo PMID: 19799916

Abstract

The crystal structures of a biologically and therapeutically active recombinant homotrimeric fragment of human lung surfactant protein D with a series of bound ligands have been determined. While the structures reveal various different binding modes, all utilise a similarly positioned pair of mannose-type O3' and O4' hydroxyls with no direct interaction between any non-terminal sugar and protein. The orientation, position, and interactions of the bound terminal sugar depend on the sugar itself, the presence and form of glycosidic linkage, and the environment in the crystal, which, via Asp325, places stereochemical and electronic constraints, different for the three different subunits in the homotrimer, on the ligand-binding site. As a direct consequence of this influence, the other binding-pocket flanking residue, Arg343, exhibits variable conformation and variable interactions with bound ligand and leaves open to question which orientation of terminal mannobiose, and of other terminal disaccharides, may be present in extended physiological ligands. The combined structural evidence shows that there is significant flexibility in recognition; that Asp325, in addition to Arg343, is an important determinant of ligand selectivity, recognition, and binding; and that differences in crystal contact interfaces exert, through Asp325, significant influence on preferred binding modes.

Articles - 3ikq mentioned but not cited (3)

  1. Structural characterisation of ligand-binding determinants in human lung surfactant protein D: influence of Asp325. Shrive AK, Martin C, Burns I, Paterson JM, Martin JD, Townsend JP, Waters P, Clark HW, Kishore U, Reid KB, Greenhough TJ. J Mol Biol 394 776-788 (2009)
  2. Predicting binding sites from unbound versus bound protein structures. Clark JJ, Orban ZJ, Carlson HA. Sci Rep 10 15856 (2020)
  3. Elucidating the enhanced binding affinity of a double mutant SP-D with trimannose on the influenza A virus using molecular dynamics. Li D, Minkara MS. Comput Struct Biotechnol J 20 4984-5000 (2022)


Reviews citing this publication (3)

  1. Review: Structural determinants of pattern recognition by lung collectins. Seaton BA, Crouch EC, McCormack FX, Head JF, Hartshorn KL, Mendelsohn R. Innate Immun 16 143-150 (2010)
  2. The carbohydrate recognition domain of collectins. Veldhuizen EJ, van Eijk M, Haagsman HP. FEBS J 278 3930-3941 (2011)
  3. Surfactant Proteins A and D: Trimerized Innate Immunity Proteins with an Affinity for Viral Fusion Proteins. Watson A, Phipps MJS, Clark HW, Skylaris CK, Madsen J. J Innate Immun 11 13-28 (2019)

Articles citing this publication (14)

  1. Mechanism of pathogen recognition by human dectin-2. Feinberg H, Jégouzo SAF, Rex MJ, Drickamer K, Weis WI, Taylor ME. J Biol Chem 292 13402-13414 (2017)
  2. Mutagenesis of surfactant protein D informed by evolution and x-ray crystallography enhances defenses against influenza A virus in vivo. Crouch E, Nikolaidis N, McCormack FX, McDonald B, Allen K, Rynkiewicz MJ, Cafarella TM, White M, Lewnard K, Leymarie N, Zaia J, Seaton BA, Hartshorn KL. J Biol Chem 286 40681-40692 (2011)
  3. Molecular basis of sugar recognition by collectin-K1 and the effects of mutations associated with 3MC syndrome. Venkatraman Girija U, Furze CM, Gingras AR, Yoshizaki T, Ohtani K, Marshall JE, Wallis AK, Schwaeble WJ, El-Mezgueldi M, Mitchell DA, Moody PC, Wakamiya N, Wallis R. BMC Biol 13 27 (2015)
  4. Molecular mechanisms of inhibition of influenza by surfactant protein D revealed by large-scale molecular dynamics simulation. Goh BC, Rynkiewicz MJ, Cafarella TR, White MR, Hartshorn KL, Allen K, Crouch EC, Calin O, Seeberger PH, Schulten K, Seaton BA. Biochemistry 52 8527-8538 (2013)
  5. Research Support, Non-U.S. Gov't Antibody equivalent molecules of the innate immune system: parallels between innate and adaptive immune proteins. Palaniyar N. Innate Immun 16 131-137 (2010)
  6. Computational and experimental prediction of human C-type lectin receptor druggability. Aretz J, Wamhoff EC, Hanske J, Heymann D, Rademacher C. Front Immunol 5 323 (2014)
  7. Crystallographic complexes of surfactant protein A and carbohydrates reveal ligand-induced conformational change. Shang F, Rynkiewicz MJ, McCormack FX, Wu H, Cafarella TM, Head JF, Seaton BA. J Biol Chem 286 757-765 (2011)
  8. Crystal Structure of a Complex of Surfactant Protein D (SP-D) and Haemophilus influenzae Lipopolysaccharide Reveals Shielding of Core Structures in SP-D-Resistant Strains. Clark HW, Mackay RM, Deadman ME, Hood DW, Madsen J, Moxon ER, Townsend JP, Reid KBM, Ahmed A, Shaw AJ, Greenhough TJ, Shrive AK. Infect Immun 84 1585-1592 (2016)
  9. Structural definition of hSP-D recognition of Salmonella enterica LPS inner core oligosaccharides reveals alternative binding modes for the same LPS. Littlejohn JR, da Silva RF, Neale WA, Smallcombe CC, Clark HW, Mackay RA, Watson AS, Madsen J, Hood DW, Burns I, Greenhough TJ, Shrive AK. PLoS One 13 e0199175 (2018)
  10. Surfactant Protein D as a Potential Biomarker and Therapeutic Target in Ovarian Cancer. Kumar J, Murugaiah V, Sotiriadis G, Kaur A, Jeyaneethi J, Sturniolo I, Alhamlan FS, Chatterjee J, Hall M, Kishore U, Karteris E. Front Oncol 9 542 (2019)
  11. Surfactant protein D delays Fas- and TRAIL-mediated extrinsic pathway of apoptosis in T cells. Djiadeu P, Kotra LP, Sweezey N, Palaniyar N. Apoptosis 22 730-740 (2017)
  12. Surfactant protein D induces immune quiescence and apoptosis of mitogen-activated peripheral blood mononuclear cells. Pandit H, Thakur G, Koippallil Gopalakrishnan AR, Dodagatta-Marri E, Patil A, Kishore U, Madan T. Immunobiology 221 310-322 (2016)
  13. Biomarkers for lung epithelium injury in occupational hexavalent chromium-exposed workers. Li P, Li Y, Zhang J, Yu SF, Tong W, Hu X, Jia G. J Occup Environ Med 57 e45-50 (2015)
  14. Atomic-resolution crystal structures of the immune protein conglutinin from cow reveal specific interactions of its binding site with N-acetylglucosamine. Paterson JM, Shaw AJ, Burns I, Dodds AW, Prasad A, Reid KB, Greenhough TJ, Shrive AK. J Biol Chem 294 17155-17165 (2019)


Related citations provided by authors (1)

  1. High-resolution structural insights into ligand binding and immune cell recognition by human lung surfactant protein D.. Shrive AK, Tharia HA, Strong P, Kishore U, Burns I, Rizkallah PJ, Reid KB, Greenhough TJ J Mol Biol 331 509-23 (2003)

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