N-glycome and N-glycoproteome of a Hematophagous Parasitic Nematode

Overview

Journal Comput Struct Biotechnol J

Specialty Biotechnology

Date 2021 May 24

PMID 34025939

Citations 10

Authors

Chunqun Wang

Wenjie Gao

Shi Yan

Xing-Quan Zhu

Xun Suo

Xin Liu

Nishith Gupta

Min Hu

Affiliations

Soon will be listed here.

Abstract

N-glycosylation is a physiologically vital post-translational modification of proteins in eukaryotic organisms. Initial work on - a blood-sucking nematode of ruminants with a broad geographical distribution - has shown that this parasite harbors N-glycans with exclusive chitobiose modifications. Besides, several immunogenic proteins (, amino- and metallo-peptidases) are known to be N-glycosylated in adult worms. However, an informative atlas of N-glycosylation in is not yet available. Herein, we report 291 N-glycosylated proteins with a total of 425 modification sites in the parasite. Among them, many peptidase families (, peptidase C1 and M1) including potential vaccine targets were enriched. Notably, the glycan-rich conjugates are distributed primarily in the intestine and gonads of adult worms, and consequently hidden from the host's immune system. Collectively, these data provide a comprehensive atlas of N-glycosylation in a prevalent parasitic nematode while underlining its significance for infection, immunity and prevention.

Citing Articles

Glycan Complexity and Heterogeneity of Glycoproteins in Somatic Extracts and Secretome of the Infective Stage of the Helminth Fasciola hepatica.

De Marco Verissimo C, Cwiklinski K, Nilsson J, Mirgorodskaya E, Jin C, Karlsson N Mol Cell Proteomics. 2023; 22(12):100684.

PMID: 37993102 PMC: 10755494. DOI: 10.1016/j.mcpro.2023.100684.

The Proteome and Lipidome of Extracellular Vesicles from to Underpin Explorations of Host-Parasite Cross-Talk.

Wang T, Koukoulis T, Vella L, Su H, Purnianto A, Nie S Int J Mol Sci. 2023; 24(13).

PMID: 37446130 PMC: 10341815. DOI: 10.3390/ijms241310955.

The role of glycoconjugates as receptors for insecticidal proteins.

Best H, Williamson L, Heath E, Waller-Evans H, Lloyd-Evans E, Berry C FEMS Microbiol Rev. 2023; 47(4).

PMID: 37279443 PMC: 10337751. DOI: 10.1093/femsre/fuad026.

Defining the filarial N-glycoproteome by glycosite mapping in the human parasitic nematode Brugia malayi.

Mersha F, McClung C, Chen M, Ruse C, Foster J Sci Rep. 2023; 13(1):7951.

PMID: 37193733 PMC: 10187950. DOI: 10.1038/s41598-023-34936-9.

Discovery of Novel Effector Protein Candidates Produced in the Dorsal Gland of Adult Female Root-Knot Nematodes.

Rocha R, Hussey R, Pepi L, Azadi P, Mitchum M Mol Plant Microbe Interact. 2023; 36(6):372-380.

PMID: 36847650 PMC: 11321544. DOI: 10.1094/MPMI-11-22-0232-R.

References

Paschinger K, Wilson I . Two types of galactosylated fucose motifs are present on N-glycans of Haemonchus contortus. Glycobiology. 2015; 25(6):585-90. PMC: 4414472. DOI: 10.1093/glycob/cwv015. View

Jang-Lee J, Curwen R, Ashton P, Tissot B, Mathieson W, Panico M . Glycomics analysis of Schistosoma mansoni egg and cercarial secretions. Mol Cell Proteomics. 2007; 6(9):1485-99. DOI: 10.1074/mcp.M700004-MCP200. View

Yan F, Xu L, Liu L, Yan R, Song X, Li X . Immunoproteomic analysis of whole proteins from male and female adult Haemonchus contortus. Vet J. 2009; 185(2):174-9. DOI: 10.1016/j.tvjl.2009.05.021. View

Geldhof P, Newlands G, Nyame K, Cummings R, SMITH W, Knox D . Presence of the LDNF glycan on the host-protective H-gal-GP fraction from Haemonchus contortus. Parasite Immunol. 2005; 27(1-2):55-60. DOI: 10.1111/j.1365-3024.2005.00744.x. View

Yan S, Vanbeselaere J, Jin C, Blaukopf M, Wols F, Wilson I . Core Richness of N-Glycans of Caenorhabditis elegans: A Case Study on Chemical and Enzymatic Release. Anal Chem. 2017; 90(1):928-935. PMC: 5757221. DOI: 10.1021/acs.analchem.7b03898. View

Engle D, Tiriac H, Rivera K, Pommier A, Whalen S, Oni T . The glycan CA19-9 promotes pancreatitis and pancreatic cancer in mice. Science. 2019; 364(6446):1156-1162. PMC: 6705393. DOI: 10.1126/science.aaw3145. View

Ma G, Wang T, Korhonen P, Ang C, Williamson N, Young N . Molecular alterations during larval development of Haemonchus contortus in vitro are under tight post-transcriptional control. Int J Parasitol. 2018; 48(9-10):763-772. DOI: 10.1016/j.ijpara.2018.03.008. View

Kaji H, Saito H, Yamauchi Y, Shinkawa T, Taoka M, Hirabayashi J . Lectin affinity capture, isotope-coded tagging and mass spectrometry to identify N-linked glycoproteins. Nat Biotechnol. 2003; 21(6):667-72. DOI: 10.1038/nbt829. View

SMITH W, Newlands G, Smith S, Pettit D, Skuce P . Metalloendopeptidases from the intestinal brush border of Haemonchus contortus as protective antigens for sheep. Parasite Immunol. 2003; 25(6):313-23. DOI: 10.1046/j.1365-3024.2003.00637.x. View

10.

Cheng A, Grant C, Noble W, Bailey T . MoMo: discovery of statistically significant post-translational modification motifs. Bioinformatics. 2019; 35(16):2774-2782. PMC: 6691336. DOI: 10.1093/bioinformatics/bty1058. View

11.

Hoberg E, Zarlenga D . Evolution and Biogeography of Haemonchus contortus: Linking Faunal Dynamics in Space and Time. Adv Parasitol. 2016; 93:1-30. DOI: 10.1016/bs.apar.2016.02.021. View

12.

Haslam S, Coles G, Munn E, Smith T, Smith H, Morris H . Haemonchus contortus glycoproteins contain N-linked oligosaccharides with novel highly fucosylated core structures. J Biol Chem. 1996; 271(48):30561-70. DOI: 10.1074/jbc.271.48.30561. View

13.

Wang T, Ma G, Ang C, Korhonen P, Xu R, Nie S . Somatic proteome of Haemonchus contortus. Int J Parasitol. 2019; 49(3-4):311-320. DOI: 10.1016/j.ijpara.2018.12.003. View

14.

Rodrigues J, Acosta-Serrano A, Aebi M, Ferguson M, Routier F, Schiller I . Parasite Glycobiology: A Bittersweet Symphony. PLoS Pathog. 2015; 11(11):e1005169. PMC: 4642930. DOI: 10.1371/journal.ppat.1005169. View

15.

Yu N, Wagner J, Laird M, Melli G, Rey S, Lo R . PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics. 2010; 26(13):1608-15. PMC: 2887053. DOI: 10.1093/bioinformatics/btq249. View

16.

Alter G, Ottenhoff T, Joosten S . Antibody glycosylation in inflammation, disease and vaccination. Semin Immunol. 2018; 39:102-110. PMC: 8731230. DOI: 10.1016/j.smim.2018.05.003. View

17.

Smit C, van Diepen A, Nguyen D, Wuhrer M, Hoffmann K, Deelder A . Glycomic Analysis of Life Stages of the Human Parasite Schistosoma mansoni Reveals Developmental Expression Profiles of Functional and Antigenic Glycan Motifs. Mol Cell Proteomics. 2015; 14(7):1750-69. PMC: 4587318. DOI: 10.1074/mcp.M115.048280. View

18.

Williamson A, Brindley P, Knox D, Hotez P, Loukas A . Digestive proteases of blood-feeding nematodes. Trends Parasitol. 2003; 19(9):417-23. DOI: 10.1016/s1471-4922(03)00189-2. View

19.

Kang P, Mechref Y, Novotny M . High-throughput solid-phase permethylation of glycans prior to mass spectrometry. Rapid Commun Mass Spectrom. 2008; 22(5):721-34. DOI: 10.1002/rcm.3395. View

20.

Ruhaak L, Xu G, Li Q, Goonatilleke E, Lebrilla C . Mass Spectrometry Approaches to Glycomic and Glycoproteomic Analyses. Chem Rev. 2018; 118(17):7886-7930. PMC: 7757723. DOI: 10.1021/acs.chemrev.7b00732. View