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Structural analysis for glycolipid recognition by the C-type lectins Mincle and MCL.

Furukawa A, Kamishikiryo J, Mori D, Toyonaga K, Okabe Y, Toji A, Kanda R, Miyake Y, Ose T, Yamasaki S, Maenaka K
Proc Natl Acad Sci U S A 110 17438-43 (2013)
Related entries: 3wh3, 3whd

Cited: 84 times
EuropePMC logo PMID: 24101491

Abstract

Mincle [macrophage inducible Ca(2+)-dependent (C-type) lectin; CLEC4E] and MCL (macrophage C-type lectin; CLEC4D) are receptors for the cord factor TDM (trehalose-6,6'-dimycolate), a unique glycolipid of mycobacterial cell-surface components, and activate immune cells to confer adjuvant activity. Although it is known that receptor-TDM interactions require both sugar and lipid moieties of TDM, the mechanisms of glycolipid recognition by Mincle and MCL remain unclear. We here report the crystal structures of Mincle, MCL, and the Mincle-citric acid complex. The structures revealed that these receptors are capable of interacting with sugar in a Ca(2+)-dependent manner, as observed in other C-type lectins. However, Mincle and MCL uniquely possess shallow hydrophobic regions found adjacent to their putative sugar binding sites, which reasonably locate for recognition of fatty acid moieties of glycolipids. Functional studies using mutant receptors as well as glycolipid ligands support this deduced binding mode. These results give insight into the molecular mechanism of glycolipid recognition through C-type lectin receptors, which may provide clues to rational design for effective adjuvants.

Articles - 3wh2 mentioned but not cited (9)

  1. Structural analysis for glycolipid recognition by the C-type lectins Mincle and MCL. Furukawa A, Kamishikiryo J, Mori D, Toyonaga K, Okabe Y, Toji A, Kanda R, Miyake Y, Ose T, Yamasaki S, Maenaka K. Proc Natl Acad Sci U S A 110 17438-17443 (2013)
  2. Human Mincle Binds to Cholesterol Crystals and Triggers Innate Immune Responses. Kiyotake R, Oh-Hora M, Ishikawa E, Miyamoto T, Ishibashi T, Yamasaki S. J Biol Chem 290 25322-25332 (2015)
  3. Defining the conformation of human mincle that interacts with mycobacterial trehalose dimycolate. Jégouzo SA, Harding EC, Acton O, Rex MJ, Fadden AJ, Taylor ME, Drickamer K. Glycobiology 24 1291-1300 (2014)
  4. Induction of Mincle by Helicobacter pylori and consequent anti-inflammatory signaling denote a bacterial survival strategy. Devi S, Rajakumara E, Ahmed N. Sci Rep 5 15049 (2015)
  5. Inflammasome NLRP3 activation induced by Convulxin, a C-type lectin-like isolated from Crotalus durissus terrificus snake venom. Rego CMA, Francisco AF, Boeno CN, Paloschi MV, Lopes JA, Silva MDS, Santana HM, Serrath SN, Rodrigues JE, Lemos CTL, Dutra RSS, da Cruz JN, Dos Santos CBR, da S Setúbal S, Fontes MRM, Soares AM, Pires WL, Zuliani JP. Sci Rep 12 4706 (2022)
  6. Aryl Trehalose Derivatives as Vaccine Adjuvants for Mycobacterium tuberculosis. Ryter KT, Ettenger G, Rasheed OK, Buhl C, Child R, Miller SM, Holley D, Smith AJ, Evans JT. J Med Chem 63 309-320 (2020)
  7. MAGA: A Supervised Method to Detect Motifs From Annotated Groups in Alignments. Mier P, Andrade-Navarro MA. Evol Bioinform Online 16 1176934320916199 (2020)
  8. CLEC4E upregulation in gastric cancer: A potential therapeutic target correlating with tumor-associated macrophages. Jiang Q, Xiao D, Wang A, Yu Q, Yin Y, Wu J, Zhang Y, Jin T, Kuang B, Jia Y. Heliyon 10 e27172 (2024)
  9. Characterisation of the bovine C-type lectin receptor Mincle and potential evidence for an endogenous ligand. Holder A, Kolakowski J, Rosentreter C, Knuepfer E, Jégouzo SAF, Rosenwasser O, Harris H, Baumgaertel L, Gibson A, Werling D. Front Immunol 14 1189587 (2023)


Reviews citing this publication (23)

  1. Recent insights into structures and functions of C-type lectins in the immune system. Drickamer K, Taylor ME. Curr Opin Struct Biol 34 26-34 (2015)
  2. MCL and Mincle: C-Type Lectin Receptors That Sense Damaged Self and Pathogen-Associated Molecular Patterns. Richardson MB, Williams SJ. Front Immunol 5 288 (2014)
  3. Recognition of Mycobacterial Lipids by Immune Receptors. Ishikawa E, Mori D, Yamasaki S. Trends Immunol 38 66-76 (2017)
  4. Natural and synthetic carbohydrate-based vaccine adjuvants and their mechanisms of action. Pifferi C, Fuentes R, Fernández-Tejada A. Nat Rev Chem 5 197-216 (2021)
  5. Contact, Collaboration, and Conflict: Signal Integration of Syk-Coupled C-Type Lectin Receptors. Ostrop J, Lang R. J Immunol 198 1403-1414 (2017)
  6. Macrophage Inducible C-Type Lectin As a Multifunctional Player in Immunity. Patin EC, Orr SJ, Schaible UE. Front Immunol 8 861 (2017)
  7. Mincle: 20 years of a versatile sensor of insults. Lu X, Nagata M, Yamasaki S. Int Immunol 30 233-239 (2018)
  8. Sweet complementarity: the functional pairing of glycans with lectins. Gabius HJ, Manning JC, Kopitz J, André S, Kaltner H. Cell Mol Life Sci 73 1989-2016 (2016)
  9. The molecular biology of mycobacterial trehalose in the quest for advanced tuberculosis therapies. Nobre A, Alarico S, Maranha A, Mendes V, Empadinhas N. Microbiology (Reading) 160 1547-1570 (2014)
  10. Pathogenicity and virulence of Mycobacterium tuberculosis. Rahlwes KC, Dias BRS, Campos PC, Alvarez-Arguedas S, Shiloh MU. Virulence 14 2150449 (2023)
  11. Host Responses to Malassezia spp. in the Mammalian Skin. Sparber F, LeibundGut-Landmann S. Front Immunol 8 1614 (2017)
  12. Sensing Lipids with Mincle: Structure and Function. Williams SJ. Front Immunol 8 1662 (2017)
  13. International Union of Basic and Clinical Pharmacology. XCVI. Pattern recognition receptors in health and disease. Bryant CE, Orr S, Ferguson B, Symmons MF, Boyle JP, Monie TP. Pharmacol Rev 67 462-504 (2015)
  14. Human Lectins, Their Carbohydrate Affinities and Where to Find Them. Raposo CD, Canelas AB, Barros MT. Biomolecules 11 188 (2021)
  15. The adaptor protein CARD9, from fungal immunity to tumorigenesis. Wang Y, Zhang D, Hou Y, Shen S, Wang T. Am J Cancer Res 10 2203-2225 (2020)
  16. Identification and Biological Activity of Synthetic Macrophage Inducible C-Type Lectin Ligands. Braganza CD, Teunissen T, Timmer MSM, Stocker BL. Front Immunol 8 1940 (2017)
  17. From structure to function - Ligand recognition by myeloid C-type lectin receptors. Fischer S, Stegmann F, Gnanapragassam VS, Lepenies B. Comput Struct Biotechnol J 20 5790-5812 (2022)
  18. Immune sensing of microbial glycolipids and related conjugates by T cells and the pattern recognition receptors MCL and Mincle. Smith DG, Williams SJ. Carbohydr Res 420 32-45 (2016)
  19. Medicinal chemistry of the myeloid C-type lectin receptors Mincle, Langerin, and DC-SIGN. Cramer J. RSC Med Chem 12 1985-2000 (2021)
  20. Synthetic agonists of NOD-like, RIG-I-like, and C-type lectin receptors for probing the inflammatory immune response. Nielsen AE, Hantho JD, Mancini RJ. Future Med Chem 9 1345-1360 (2017)
  21. DectiSomes: C-type lectin receptor-targeted liposomes as pan-antifungal drugs. Meagher RB, Lewis ZA, Ambati S, Lin X. Adv Drug Deliv Rev 196 114776 (2023)
  22. Biosynthesis, structure and biological function of cholesterol glucoside in Helicobacter pylori: A review. Zhang L, Xie J. Medicine (Baltimore) 102 e34911 (2023)
  23. The Dectin-1 and Dectin-2 clusters: C-type lectin receptors with fundamental roles in immunity. Malamud M, Brown GD. EMBO Rep (2024)

Articles citing this publication (52)



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