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Structural characterization of carbohydrate binding by LMAN1 protein provides new insight into the endoplasmic reticulum export of factors V (FV) and VIII (FVIII).

Zheng C, Page RC, Das V, Nix JC, Wigren E, Misra S, Zhang B
J Biol Chem 288 20499-509 (2013)
Cited: 33 times
EuropePMC logo PMID: 23709226

Abstract

LMAN1 (ERGIC-53) is a key mammalian cargo receptor responsible for the export of a subset of glycoproteins from the endoplasmic reticulum. Together with its soluble coreceptor MCFD2, LMAN1 transports coagulation factors V (FV) and VIII (FVIII). Mutations in LMAN1 or MCFD2 cause the genetic bleeding disorder combined deficiency of FV and FVIII (F5F8D). The LMAN1 carbohydrate recognition domain (CRD) binds to both glycoprotein cargo and MCFD2 in a Ca(2+)-dependent manner. To understand the biochemical basis and regulation of LMAN1 binding to glycoprotein cargo, we solved crystal structures of the LMAN1-CRD bound to Man-α-1,2-Man, the terminal carbohydrate moiety of high mannose glycans. Our structural data, combined with mutagenesis and in vitro binding assays, define the central mannose-binding site on LMAN1 and pinpoint histidine 178 and glycines 251/252 as critical residues for FV/FVIII binding. We also show that mannobiose binding is relatively independent of pH in the range relevant for endoplasmic reticulum-to-Golgi traffic, but is sensitive to lowered Ca(2+) concentrations. The distinct LMAN1/MCFD2 interaction is maintained at these lowered Ca(2+) concentrations. Our results suggest that compartmental changes in Ca(2+) concentration regulate glycoprotein cargo binding and release from the LMAN1·MCFD2 complex in the early secretory pathway.

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Articles - 4gkx mentioned but not cited (3)

  1. Structural characterization of carbohydrate binding by LMAN1 protein provides new insight into the endoplasmic reticulum export of factors V (FV) and VIII (FVIII). Zheng C, Page RC, Das V, Nix JC, Wigren E, Misra S, Zhang B. J Biol Chem 288 20499-20509 (2013)
  2. Structural basis for disparate sugar-binding specificities in the homologous cargo receptors ERGIC-53 and VIP36. Satoh T, Suzuki K, Yamaguchi T, Kato K. PLoS One 9 e87963 (2014)
  3. HumanLectome, an update of UniLectin for the annotation and prediction of human lectins. Schnider B, M'Rad Y, El Ahmadie J, de Brevern AG, Imberty A, Lisacek F. Nucleic Acids Res 52 D1683-D1693 (2024)


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  1. Convergent and divergent mechanisms of sugar recognition across kingdoms. Taylor ME, Drickamer K. Curr Opin Struct Biol 28 14-22 (2014)
  2. Combined deficiency of coagulation factors V and VIII: an update. Zheng C, Zhang B. Semin Thromb Hemost 39 613-620 (2013)
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  4. Membrane Transport at an Organelle Interface in the Early Secretory Pathway: Take Your Coat Off and Stay a While: Evolution of the metazoan early secretory pathway. Hanna MG, Peotter JL, Frankel EB, Audhya A. Bioessays 40 e1800004 (2018)
  5. Missing links in antibody assembly control. Anelli T, van Anken E. Int J Cell Biol 2013 606703 (2013)
  6. Human Lectins, Their Carbohydrate Affinities and Where to Find Them. Raposo CD, Canelas AB, Barros MT. Biomolecules 11 188 (2021)
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  1. Onion-like glycodendrimersomes from sequence-defined Janus glycodendrimers and influence of architecture on reactivity to a lectin. Xiao Q, Zhang S, Wang Z, Sherman SE, Moussodia RO, Peterca M, Muncan A, Williams DR, Hammer DA, Vértesy S, André S, Gabius HJ, Klein ML, Percec V. Proc Natl Acad Sci U S A 113 1162-1167 (2016)
  2. LMAN1 (ERGIC-53) promotes trafficking of neuroreceptors. Fu YL, Zhang B, Mu TW. Biochem Biophys Res Commun 511 356-362 (2019)
  3. Brg1 coordinates multiple processes during retinogenesis and is a tumor suppressor in retinoblastoma. Aldiri I, Ajioka I, Xu B, Zhang J, Chen X, Benavente C, Finkelstein D, Johnson D, Akiyama J, Pennacchio LA, Dyer MA. Development 142 4092-4106 (2015)
  4. Analysis of MCFD2- and LMAN1-deficient mice demonstrates distinct functions in vivo. Zhu M, Zheng C, Wei W, Everett L, Ginsburg D, Zhang B. Blood Adv 2 1014-1021 (2018)
  5. Dimeric sorting code for concentrative cargo selection by the COPII coat. Nie C, Wang H, Wang R, Ginsburg D, Chen XW. Proc Natl Acad Sci U S A 115 E3155-E3162 (2018)
  6. Systems-wide analysis unravels the new roles of CCM signal complex (CSC). Abou-Fadel J, Vasquez M, Grajeda B, Ellis C, Zhang J. Heliyon 5 e02899 (2019)
  7. Hepatitis B Virus Exploits ERGIC-53 in Conjunction with COPII to Exit Cells. Zeyen L, Döring T, Prange R. Cells 9 E1889 (2020)
  8. Isoform-selective oligomer formation of Saccharomyces cerevisiae p24 family proteins. Hirata R, Nihei C, Nakano A. J Biol Chem 288 37057-37070 (2013)
  9. ARL15 modulates magnesium homeostasis through N-glycosylation of CNNMs. Zolotarov Y, Ma C, González-Recio I, Hardy S, Franken GAC, Uetani N, Latta F, Kostantin E, Boulais J, Thibault MP, Côté JF, Díaz-Moreno I, Quintana AD, Hoenderop JGJ, Martínez-Cruz LA, Tremblay ML, de Baaij JHF. Cell Mol Life Sci 78 5427-5445 (2021)
  10. Analysis of COPII Vesicles Indicates a Role for the Emp47-Ssp120 Complex in Transport of Cell Surface Glycoproteins. Margulis NG, Wilson JD, Bentivoglio CM, Dhungel N, Gitler AD, Barlowe C. Traffic 17 191-210 (2016)
  11. Molecular mechanisms of missense mutations that generate ectopic N-glycosylation sites in coagulation factor VIII. Wei W, Misra S, Cannon MV, Yang R, Zhu X, Gilmore R, Zhu M, Zhang B. Biochem J 475 873-886 (2018)
  12. Suppression of the IgM Response by Aryl Hydrocarbon Receptor Activation in Human Primary B Cells Involves Impairment of Immunoglobulin Secretory Processes. Zhou J, Henriquez J, Crawford R, Kaminski N. Toxicol Sci 163 319-329 (2018)
  13. Amino Groups of Chitosan Are Crucial for Binding to a Family 32 Carbohydrate Binding Module of a Chitosanase from Paenibacillus elgii. Das SN, Wagenknecht M, Nareddy PK, Bhuvanachandra B, Niddana R, Balamurugan R, Swamy MJ, Moerschbacher BM, Podile AR. J Biol Chem 291 18977-18990 (2016)
  14. Factor VIII and vWF deficiency in STT3A-CDG. Chang IJ, Byers HM, Ng BG, Merritt JL, Gilmore R, Shrimal S, Wei W, Zhang Y, Blair AB, Freeze HH, Zhang B, Lam C. J Inherit Metab Dis 42 325-332 (2019)
  15. Crystallographic snapshots of the EF-hand protein MCFD2 complexed with the intracellular lectin ERGIC-53 involved in glycoprotein transport. Satoh T, Nishio M, Suzuki K, Yagi-Utsumi M, Kamiya Y, Mizushima T, Kato K. Acta Crystallogr F Struct Biol Commun 76 216-221 (2020)
  16. Altered phenotype in LMAN1-deficient mice with low levels of residual LMAN1 expression. Everett LA, Khoriaty RN, Zhang B, Ginsburg D. Blood Adv 4 5635-5643 (2020)
  17. Separate roles of LMAN1 and MCFD2 in ER-to-Golgi trafficking of FV and FVIII. Zhang Y, Liu Z, Zhang B. Blood Adv 7 1286-1296 (2023)
  18. Crystal structure of the legume lectin-like domain of an ERGIC-53-like protein from Entamoeba histolytica. Khan F, Suguna K. Acta Crystallogr F Struct Biol Commun 75 197-204 (2019)
  19. LMAN1 is a receptor for house dust mite allergens. Miller MH, Swaby LG, Vailoces VS, LaFratta M, Zhang Y, Zhu X, Hitchcock DJ, Jewett TJ, Zhang B, Tigno-Aranjuez JT. Cell Rep 42 112208 (2023)


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