Characterization of Excretory/Secretory Antigen (ES-15) and Its Modulatory Functions on Goat Immune Cells In Vitro

Overview

Journal Pathogens

Date 2020 Mar 4

PMID 32120801

Citations 9

Authors

Muhammad Ehsan

Javaid Ali Gadahi

Muhammad Waqqas Hasan

Muhammad Haseeb

Haider Ali

Ruofeng Yan

Lixin Xu

Xiaokai Song

Xing-Quan Zhu

Xiangrui Li

Affiliations

Soon will be listed here.

Abstract

Small size excretory/secretory (ES) antigens of the parasite have intense interest among researchers for understanding the molecular basis of helminths immune regulation in term of control strategies. Immunomodulatory roles of ES-15 kDa (HcES-15) on host immune cells during host-parasite interactions are unknown. In this study, the HcES-15 gene was cloned and expression of recombinant protein (rHcES-15) was induced by isopropyl-ß-D-thiogalactopyranoside (IPTG). Binding activity of rHcES-15 to goat peripheral blood mononuclear cells (PBMCs) was confirmed by immunofluorescence assay (IFA) and immunohistochemical analysis showed that 15 kDa protein localized in the outer and inner structure of the adult worm, clearly indicated as the parasite's ES antigen. The immunoregulatory role on cytokines production, cell proliferation, cell migration, nitric oxide (NO) production, apoptosis, and phagocytosis were observed by co-incubation of rHcES-15 with goat PBMCs. The results showed that cytokines IL-4, IL-10, IL-17, the production of nitric oxide (NO), PBMCs apoptosis, and monocytes phagocytosis were all elevated after cells incubated with rHcES-15 at differential protein concentrations. We also found that IFN-γ, TGF-β1, cells proliferation and migration were significantly suppressed with the interaction of rHcES-15 protein. Our findings indicated that low molecular ES antigens of possessed discrete immunoregulatory roles, which will help to understand the mechanisms involved in immune evasion by the parasite during host-parasite interactions.

Citing Articles

Excreted/Secreted 15-kDa Proteins and Serine Protease Peptides from Act as Immune-Response Enhancers in Lambs.

Camas-Pereyra R, Bautista-Garcia G, Perez-Anzurez G, Duran-Cortes Z, Reyes-Guerrero D, Maza-Lopez J Pathogens. 2024; 13(7).

PMID: 39057830 PMC: 11280362. DOI: 10.3390/pathogens13070604.

PLGA-Encapsulated Antigen ES-15 Augments Immune Responses in a Murine Model.

Hasan M, Ehsan M, Wang Q, Haseeb M, Lakho S, Haider A Vaccines (Basel). 2023; 11(12).

PMID: 38140198 PMC: 10748113. DOI: 10.3390/vaccines11121794.

Helminth-associated changes in host immune phenotype connect top-down and bottom-up interactions during co-infection.

Seguel M, Budischak S, Jolles A, Ezenwa V Funct Ecol. 2023; 37(4):860-872.

PMID: 37214767 PMC: 10195069. DOI: 10.1111/1365-2435.14237.

The 22nd Chromatography Component of the Excretory-Secretory Products Decreased the Proliferation of Peripheral Blood Mononuclear Cells from Buffalo.

Yuan X, Han X, Kong X, Hou L, Wei K, Chen M Animals (Basel). 2023; 13(4).

PMID: 36830351 PMC: 9951737. DOI: 10.3390/ani13040564.

Communication is key: Innate immune cells regulate host protection to helminths.

Peng J, Federman H, Hernandez C, Siracusa M Front Immunol. 2022; 13:995432.

PMID: 36225918 PMC: 9548658. DOI: 10.3389/fimmu.2022.995432.

References

Miljkovic D, Cvetkovic I, Vuckovic O, Stosic-Grujicic S, Mostarica Stojkovic M, Trajkovic V . The role of interleukin-17 in inducible nitric oxide synthase-mediated nitric oxide production in endothelial cells. Cell Mol Life Sci. 2003; 60(3):518-25. PMC: 11138561. DOI: 10.1007/s000180300043. View

Ehsan M, Gao W, Gadahi J, Lu M, Liu X, Wang Y . Arginine kinase from Haemonchus contortus decreased the proliferation and increased the apoptosis of goat PBMCs in vitro. Parasit Vectors. 2017; 10(1):311. PMC: 5485575. DOI: 10.1186/s13071-017-2244-z. View

Shakya K, Miller J, Horohov D . A Th2 type of immune response is associated with increased resistance to Haemonchus contortus in naturally infected Gulf Coast Native lambs. Vet Parasitol. 2009; 163(1-2):57-66. DOI: 10.1016/j.vetpar.2009.03.052. View

Smith T, Munn E, Graham M, Tavernor A, Greenwood C . Purification and evaluation of the integral membrane protein H11 as a protective antigen against Haemonchus contortus. Int J Parasitol. 1993; 23(2):271-80. DOI: 10.1016/0020-7519(93)90150-w. View

Wang W, Wang S, Zhang H, Yuan C, Yan R, Song X . Galectin Hco-gal-m from Haemonchus contortus modulates goat monocytes and T cell function in different patterns. Parasit Vectors. 2014; 7:342. PMC: 4117971. DOI: 10.1186/1756-3305-7-342. View

Morissette R, Schoenhoff F, Xu Z, Shilane D, Griswold B, Chen W . Transforming growth factor-β and inflammation in vascular (type IV) Ehlers-Danlos syndrome. Circ Cardiovasc Genet. 2014; 7(1):80-8. DOI: 10.1161/CIRCGENETICS.113.000280. View

Yatsuda A, Eysker M, Vieira-Bressan M, de Vries E . A family of activation associated secreted protein (ASP) homologues of Cooperia punctata. Res Vet Sci. 2002; 73(3):297-306. DOI: 10.1016/s0034-5288(02)00125-x. View

Brunet L . Nitric oxide in parasitic infections. Int Immunopharmacol. 2001; 1(8):1457-67. DOI: 10.1016/s1567-5769(01)00090-x. View

Schallig H, van Leeuwen M, Hendrikx W . Immune responses of Texel sheep to excretory/secretory products of adult Haemonchus contortus. Parasitology. 1994; 108 ( Pt 3):351-7. DOI: 10.1017/s0031182000076198. View

10.

Chen L, Rao K, He Y, Ramaswamy K . Skin-stage schistosomula of Schistosoma mansoni produce an apoptosis-inducing factor that can cause apoptosis of T cells. J Biol Chem. 2002; 277(37):34329-35. PMC: 2742670. DOI: 10.1074/jbc.M201344200. View

11.

Schallig H, van Leeuwen M, Cornelissen A . Protective immunity induced by vaccination with two Haemonchus contortus excretory secretory proteins in sheep. Parasite Immunol. 1998; 19(10):447-53. DOI: 10.1046/j.1365-3024.1997.d01-148.x. View

12.

Uchikawa R, Matsuda S, Arizono N . Suppression of gamma interferon transcription and production by nematode excretory-secretory antigen during polyclonal stimulation of rat lymph node T cells. Infect Immun. 2000; 68(11):6233-9. PMC: 97704. DOI: 10.1128/IAI.68.11.6233-6239.2000. View

13.

Gadahi J, Ehsan M, Wang S, Zhang Z, Yan R, Song X . Recombinant protein of small GTPase ADP-ribosylation factor 1 (HcARF1) modulate the cell mediated immune response . Oncotarget. 2018; 8(68):112211-112221. PMC: 5762504. DOI: 10.18632/oncotarget.22662. View

14.

Craig H, Wastling J, Knox D . A preliminary proteomic survey of the in vitro excretory/secretory products of fourth-stage larval and adult Teladorsagia circumcincta. Parasitology. 2006; 132(Pt 4):535-43. DOI: 10.1017/S0031182005009510. View

15.

Chen H, Weng I, Li C, Wan L, Liu F . Examination of galectins in phagocytosis. Methods Mol Biol. 2014; 1207:201-13. PMC: 4596061. DOI: 10.1007/978-1-4939-1396-1_13. View

16.

Jasmer D, McGuire T . Protective immunity to a blood-feeding nematode (Haemonchus contortus) induced by parasite gut antigens. Infect Immun. 1991; 59(12):4412-7. PMC: 259057. DOI: 10.1128/iai.59.12.4412-4417.1991. View

17.

Babu S, Blauvelt C, Nutman T . Filarial parasites induce NK cell activation, type 1 and type 2 cytokine secretion, and subsequent apoptotic cell death. J Immunol. 2007; 179(4):2445-56. DOI: 10.4049/jimmunol.179.4.2445. View

18.

Lightowlers M, Rickard M . Excretory-secretory products of helminth parasites: effects on host immune responses. Parasitology. 1988; 96 Suppl:S123-66. DOI: 10.1017/s0031182000086017. View

19.

Bradford M . A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72:248-54. DOI: 10.1016/0003-2697(76)90527-3. View

20.

SMITH W, Smith S, Murray J . Protection studies with integral membrane fractions of Haemonchus contortus. Parasite Immunol. 1994; 16(5):231-41. DOI: 10.1111/j.1365-3024.1994.tb00345.x. View