Twenty-five-year Research Progress in Hookworm Excretory/secretory Products

Overview

Journal Parasit Vectors

Publisher Biomed Central

Specialties Parasitology
Tropical Medicine

Date 2020 Mar 16

PMID 32171305

Citations 18

Authors

Asmaa M I Abuzeid

Xue Zhou

Yue Huang

Guoqing Li

Affiliations

Soon will be listed here.

Abstract

Hookworm infection is a major public health problem that threatens about 500 million people throughout tropical areas of the world. Adult hookworms survive for many years in the host intestine, where they suck blood, causing iron deficiency anemia and malnutrition. Numerous molecules, named excretory/secretory (ES) products, are secreted by hookworm adults and/or larvae to aid in parasite survival and pathobiology. Although the molecular cloning and characterization of hookworm ES products began 25 years ago, the biological role and molecular nature of many of them are still unclear. Hookworm ES products, with distinct structures and functions, have been linked to many essential events in the disease pathogenesis. These events include host invasion and tissue migration, parasite nourishment and reproduction, and immune modulation. Several of these products represent promising vaccine targets for controlling hookworm disease and therapeutic targets for many inflammatory diseases. This review aims to summarize our present knowledge about hookworm ES products, including their role in parasite biology, host-parasite interactions, and as vaccine and pharmaceutical targets and to identify research gaps and future research directions in this field.

Citing Articles

Hookworm genes encoding intestinal excreted-secreted proteins are transcriptionally upregulated in response to the host's immune system.

Schwarz E, Noon J, Chicca J, Garceau C, Li H, Antoshechkin I bioRxiv. 2025; .

PMID: 39975173 PMC: 11838427. DOI: 10.1101/2025.02.01.636063.

Proteomic characterization and comparison of the infective and adult life stage secretomes from Necator americanus and Ancylostoma ceylanicum.

Wong Y, Rosa B, Becker L, Camberis M, LeGros G, Zhan B PLoS Negl Trop Dis. 2025; 19(1):e0012780.

PMID: 39832284 PMC: 11745416. DOI: 10.1371/journal.pntd.0012780.

Hidden in plain sight: How helminths manage to thrive in host blood.

Dagenais M, Tritten L Front Parasitol. 2025; 2():1128299.

PMID: 39816845 PMC: 11732017. DOI: 10.3389/fpara.2023.1128299.

Secreted and surface proteome and transcriptome of .

Wong Y, Pearson M, Fedorova O, Ivanov V, Khmelevskaya E, Tedla B Front Parasitol. 2025; 2():1195457.

PMID: 39816815 PMC: 11732047. DOI: 10.3389/fpara.2023.1195457.

Pattern of intestinal parasitic infections in children with malnutrition in Somalia.

Osman M, Hussein S, Omar M, Issack M, Hanafi A, Ahmed M IJID Reg. 2024; 13:100431.

PMID: 39391270 PMC: 11466610. DOI: 10.1016/j.ijregi.2024.100431.

References

Zhan B, Liu Y, Badamchian M, Williamson A, Feng J, Loukas A . Molecular characterisation of the Ancylostoma-secreted protein family from the adult stage of Ancylostoma caninum. Int J Parasitol. 2003; 33(9):897-907. DOI: 10.1016/s0020-7519(03)00111-5. View

Hassan A, Pritchard D, Ghaemmaghami A . Human dendritic cell sequestration onto the Necator americanus larval sheath during ex-sheathing: a possible mechanism for immune privilege. Parasitology. 2018; 145(9):1183-1190. DOI: 10.1017/S0031182018000136. View

Brown A, Harrison L, Kapulkin W, Jones B, Sinha A, Savage A . Molecular cloning and characterization of a C-type lectin from Ancylostoma ceylanicum: evidence for a role in hookworm reproductive physiology. Mol Biochem Parasitol. 2006; 151(2):141-7. PMC: 1831819. DOI: 10.1016/j.molbiopara.2006.10.017. View

Rote W, Dempsey E, Maki S, Vlasuk G, Moyle M . The role of CD11/CD18 integrins in the reverse passive Arthus reaction in rat dermal tissue. J Leukoc Biol. 1996; 59(2):254-61. DOI: 10.1002/jlb.59.2.254. View

Chadderdon R, Cappello M . The hookworm platelet inhibitor: functional blockade of integrins GPIIb/IIIa (alphaIIbbeta3) and GPIa/IIa (alpha2beta1) inhibits platelet aggregation and adhesion in vitro. J Infect Dis. 1999; 179(5):1235-41. DOI: 10.1086/314724. View

Tang L, Ou X, Selkirk M . Extracellular and cytoplasmic CuZn superoxide dismutases from Brugia lymphatic filarial nematode parasites. Infect Immun. 1994; 62(3):961-7. PMC: 186210. DOI: 10.1128/iai.62.3.961-967.1994. View

Nwosu A . Age-related changes in esterase and acetylcholinesterase activities of the infective larvae of Ancylostoma tubaeforme. Int J Parasitol. 1978; 8(5):355-8. DOI: 10.1016/0020-7519(78)90032-2. View

Wei J, Damania A, Gao X, Liu Z, Mejia R, Mitreva M . The hookworm Ancylostoma ceylanicum intestinal transcriptome provides a platform for selecting drug and vaccine candidates. Parasit Vectors. 2016; 9(1):518. PMC: 5039805. DOI: 10.1186/s13071-016-1795-8. View

Yang X, Gao X . Role of dendritic cells: a step forward for the hygiene hypothesis. Cell Mol Immunol. 2011; 8(1):12-8. PMC: 4002986. DOI: 10.1038/cmi.2010.51. View

10.

Leng L, Bucala R . Insight into the biology of macrophage migration inhibitory factor (MIF) revealed by the cloning of its cell surface receptor. Cell Res. 2006; 16(2):162-8. DOI: 10.1038/sj.cr.7310022. View

11.

Mendez S, Zhan B, Goud G, Ghosh K, Dobardzic A, Wu W . Effect of combining the larval antigens Ancylostoma secreted protein 2 (ASP-2) and metalloprotease 1 (MTP-1) in protecting hamsters against hookworm infection and disease caused by Ancylostoma ceylanicum. Vaccine. 2005; 23(24):3123-30. DOI: 10.1016/j.vaccine.2004.12.022. View

12.

Gan W, Deng L, Yang C, He Q, Hu J, Yin H . An anticoagulant peptide from the human hookworm, Ancylostoma duodenale that inhibits coagulation factors Xa and XIa. FEBS Lett. 2009; 583(12):1976-80. DOI: 10.1016/j.febslet.2009.05.009. View

13.

Ghosh K, Hawdon J, Hotez P . Vaccination with alum-precipitated recombinant Ancylostoma-secreted protein 1 protects mice against challenge infections with infective hookworm (Ancylostoma caninum) larvae. J Infect Dis. 1996; 174(6):1380-3. DOI: 10.1093/infdis/174.6.1380. View

14.

Wasyl K, Zawistowska-Deniziak A, Baska P, Wedrychowicz H, Wisniewski M . Molecular cloning and expression of the cDNA sequence encoding a novel aspartic protease from Uncinaria stenocephala. Exp Parasitol. 2013; 134(2):220-7. DOI: 10.1016/j.exppara.2013.03.013. View

15.

Fujiwara R, Bethony J, Bueno L, Wang Y, Ahn S, Samuel A . Immunogenicity of the hookworm Na-ASP-2 vaccine candidate: characterization of humoral and cellular responses after vaccination in the Sprague Dawley rat. Hum Vaccin. 2006; 1(3):123-8. DOI: 10.4161/hv.1.3.1924. View

16.

Furmidge B, Horn L, Pritchard D . The anti-haemostatic strategies of the human hookworm Necator americanus. Parasitology. 1996; 112 ( Pt 1):81-7. DOI: 10.1017/s0031182000065100. View

17.

Tribolet L, Cantacessi C, Pickering D, Navarro S, Doolan D, Trieu A . Probing of a human proteome microarray with a recombinant pathogen protein reveals a novel mechanism by which hookworms suppress B-cell receptor signaling. J Infect Dis. 2014; 211(3):416-25. DOI: 10.1093/infdis/jiu451. View

18.

Lo S, Rahman A, Xu N, Zhou M, Nagpala P, Jaffe H . Neutrophil inhibitory factor abrogates neutrophil adhesion by blockade of CD11a and CD11b beta(2) integrins. Mol Pharmacol. 1999; 56(5):926-32. DOI: 10.1124/mol.56.5.926. View

19.

Prociv P . Pathogenesis of human hookworm infection: insights from a 'new' zoonosis. Chem Immunol. 1997; 66:62-98. DOI: 10.1159/000058666. View

20.

Pritchard D, Brown A, Toutant J . The molecular forms of acetylcholinesterase from Necator americanus (Nematoda), a hookworm parasite of the human intestine. Eur J Biochem. 1994; 219(1-2):317-23. DOI: 10.1111/j.1432-1033.1994.tb19943.x. View