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54. Gastrointestinal Helminth Infection Improves Insulin Sensitivity, Decreases Systemic Inflammation, and Alters the Composition of Gut Microbiota in Distinct Mouse Models of Type 2 Diabetes

Author

Khudhair, Zainab, primary, Alhallaf, Rafid, additional, Eichenberger, Ramon M., additional, Whan, Jen, additional, Kupz, Andreas, additional, Field, Matt, additional, Krause, Lutz, additional, Wilson, David T., additional, Daly, Norelle L., additional, Giacomin, Paul, additional, Sotillo, Javier, additional, and Loukas, Alex, additional

Published
2021
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55. Liver fluke induces cholangiocarcinoma

Author

Sripa, Banchob, Kaewkes, Sasithorn, Sithithaworn, Paiboon, Mairiang, Eimorn, Laha, Thewarach, Smout, Michael, Pairojkul, Chawalit, Bhudhisawasdi, Vajaraphongsa, Tesana, Smarn, Thinkamrop, Bandit, Bethony, Jeffrey M., Loukas, Alex, and Brindley, Paul J.

Subjects
Fluke infections -- Statistics, Fluke infections -- Risk factors, Fluke infections -- Prevention, Medical research, Medicine, Experimental
Abstract

Opisthorchiasis and Clonorchiasis: Major Regional Public Health Problems Liver fluke infection caused by Opisthorchis viverrini, O. felineus, and Clonorchis sinensis is a major public health problem in East Asia and [...]

Published
2007

56. Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms

Author

Logan, Jayden, Pearson, Mark S., Manda, Srikanth S., Choi, Young Jun, Field, Matthew, Eichenberger, Ramon M., Mulvenna, Jason, Nagaraj, Shivashankar H., Fujiwara, Ricardo T., Gazzinelli-Guimaraes, Pedro, Bueno, Lilian, Mati, Vitor, Bethony, Jeffrey M., Mitreva, Makedonka, Sotillo, Javier, Loukas, Alex, Logan, Jayden, Pearson, Mark S., Manda, Srikanth S., Choi, Young Jun, Field, Matthew, Eichenberger, Ramon M., Mulvenna, Jason, Nagaraj, Shivashankar H., Fujiwara, Ricardo T., Gazzinelli-Guimaraes, Pedro, Bueno, Lilian, Mati, Vitor, Bethony, Jeffrey M., Mitreva, Makedonka, Sotillo, Javier, and Loukas, Alex

Abstract

The human hookworm Necator americanus infects more than 400 million people worldwide, contributing substantially to the poverty in these regions. Adult stage N. americanus live in the small intestine of the human host where they inject excretory/secretory (ES) products into the mucosa. ES products have been characterized at the proteome level for a number of animal hookworm species, but until now, the difficulty in obtaining sufficient live N. ameri-canus has been an obstacle in characterizing the secretome of this important human patho-gen. Herein we describe the ES proteome of N. americanus and utilize this information along with RNA Seq data to conduct the first proteogenomic analysis of a parasitic helminth, significantly improving the available genome and thereby generating a robust description of the parasite secretome. The genome annotation resulted in a revised prediction of 3,425 fewer genes than initially reported, accompanied by a significant increase in the number of exons and introns, total gene length and the percentage of the genome covered by genes. Almost 200 ES proteins were identified by LC-MS/MS with SCP/TAPS proteins, ‘hypotheti-cal’ proteins and proteases among the most abundant families. These proteins were compared to commonly used model species of human parasitic infections, including Ancylostoma caninum, Nippostrongylus brasiliensis and Heligmosomoides polygyrus. SCP/ TAPS proteins are immunogenic in nematode infections, so we expressed four of those identified in this study in recombinant form and showed that they are all recognized to vary-ing degrees by serum antibodies from hookworm-infected subjects from a disease-endemic area of Brazil. Our findings provide valuable information on important families of proteins with both known and unknown functions that could be instrumental in host-parasite interac-tions, including protein families that might be key for parasite survival in the onslaught of robust immune responses, as well as vacc

Published
2020

64. Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms

Author

Logan, Jayden, primary, Pearson, Mark S., additional, Manda, Srikanth S., additional, Choi, Young-Jun, additional, Field, Matthew, additional, Eichenberger, Ramon M., additional, Mulvenna, Jason, additional, Nagaraj, Shivashankar H., additional, Fujiwara, Ricardo T., additional, Gazzinelli-Guimaraes, Pedro, additional, Bueno, Lilian, additional, Mati, Vitor, additional, Bethony, Jeffrey M., additional, Mitreva, Makedonka, additional, Sotillo, Javier, additional, and Loukas, Alex, additional

Published
2020
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68. Hookworms Evade Host Immunity by Secreting a Deoxyribonuclease to Degrade Neutrophil Extracellular Traps

Author

Bouchery, Tiffany, primary, Moyat, Mati, additional, Sotillo, Javier, additional, Silverstein, Solomon, additional, Volpe, Beatrice, additional, Coakley, Gillian, additional, Tsourouktsoglou, Theodora-Dorita, additional, Becker, Luke, additional, Shah, Kathleen, additional, Kulagin, Manuel, additional, Guiet, Romain, additional, Camberis, Mali, additional, Schmidt, Alfonso, additional, Seitz, Arne, additional, Giacomin, Paul, additional, Le Gros, Graham, additional, Papayannopoulos, Venizelos, additional, Loukas, Alex, additional, and Harris, Nicola L., additional

Published
2020
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71. MOESM2 of Safety and tolerability of experimental hookworm infection in humans with metabolic disease: study protocol for a phase 1b randomised controlled clinical trial

Author

Pierce, Doris, Merone, Lea, Lewis, Chris, Rahman, Tony, Croese, John, Loukas, Alex, McDonald, Malcolm, Giacomin, Paul, and McDermott, Robyn

Abstract

Additional file 2. Screening pathology form: The Laboratory Request form used for to assess eligibility of participants following their initial screening visit.

Published
2019
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72. New drugs for an ancient parasite

Author

Loukas, Alex and Bethony, Jeffrey M.

Abstract

Only one drug is widely used to treat schistosomiasis, a chronic, neglected tropical disease caused by parasitic blood flukes. Fears of potential drug resistance have accelerated the search for new classes of antischistosome drugs. A promising candidate has now emerged (pages 407-412)., Schistosomiasis, caused by blood flukes of the genus Schistosoma (Fig. 1), has afflicted humans for thousands of years and is arguably the most important human helminth infection. Schistosomes infect more [...]

Published
2008

73. Vaccination of hamsters with Opisthorchis viverrini extracellular vesicles and vesicle-derived recombinant tetraspanins induces antibodies that block vesicle uptake by cholangiocytes and reduce parasite burden after challenge infection

Author

Chaiyadet, Sujittra, primary, Sotillo, Javier, additional, Krueajampa, Watchara, additional, Thongsen, Sophita, additional, Brindley, Paul J., additional, Sripa, Banchob, additional, Loukas, Alex, additional, and Laha, Thewarach, additional

Published
2019
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74. In-depth proteomic characterization of Schistosoma haematobium: Towards the development of new tools for elimination

Author

Sotillo, Javier, primary, Pearson, Mark S., additional, Becker, Luke, additional, Mekonnen, Gebeyaw G., additional, Amoah, Abena S., additional, van Dam, Govert, additional, Corstjens, Paul L. A. M., additional, Murray, Janice, additional, Mduluza, Takafira, additional, Mutapi, Francisca, additional, and Loukas, Alex, additional

Published
2019
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76. Hookworm-Derived Metabolites Suppress Pathology in a Mouse Model of Colitis and Inhibit Secretion of Key Inflammatory Cytokines in Primary Human Leukocytes

Author

Wangchuk, Phurpa, primary, Shepherd, Catherine, additional, Constantinoiu, Constantin, additional, Ryan, Rachael Y. M., additional, Kouremenos, Konstantinos A., additional, Becker, Luke, additional, Jones, Linda, additional, Buitrago, Geraldine, additional, Giacomin, Paul, additional, Wilson, David, additional, Daly, Norelle, additional, McConville, Malcolm J., additional, Miles, John J., additional, and Loukas, Alex, additional

Published
2019
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77. Programmed knockout mutation of liver fluke granulin attenuates virulence of infection-induced hepatobiliary morbidity

Author

Arunsan, Patpicha, primary, Ittiprasert, Wannaporn, additional, Smout, Michael J, additional, Cochran, Christina J, additional, Mann, Victoria H, additional, Chaiyadet, Sujittra, additional, Karinshak, Shannon E, additional, Sripa, Banchob, additional, Young, Neil David, additional, Sotillo, Javier, additional, Loukas, Alex, additional, Brindley, Paul J, additional, and Laha, Thewarach, additional

Published
2019
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79. Differences in transcription between free-living and CO2-activated third-stage larvae of Haemonchus contortus

Author

Zhong Weiwei, Zawadzki Jodi L, Presidente Paul JA, Hall Ross S, Jex Aaron R, Young Neil D, Campbell Bronwyn E, Cantacessi Cinzia, Aleman-Meza Boanerges, Loukas Alex, Sternberg Paul W, and Gasser Robin B

Subjects
Biotechnology, TP248.13-248.65, Genetics, QH426-470
Abstract

Abstract Background The disease caused by Haemonchus contortus, a blood-feeding nematode of small ruminants, is of major economic importance worldwide. The infective third-stage larva (L3) of this gastric nematode is enclosed in a cuticle (sheath) and, once ingested with herbage by the host, undergoes an exsheathment process that marks the transition from the free-living (L3) to the parasitic (xL3) stage. This study explored changes in gene transcription associated with this transition and predicted, based on comparative analysis, functional roles for key transcripts in the metabolic pathways linked to larval development. Results Totals of 101,305 (L3) and 105,553 (xL3) expressed sequence tags (ESTs) were determined using 454 sequencing technology, and then assembled and annotated; the most abundant transcripts encoded transthyretin-like, calcium-binding EF-hand, NAD(P)-binding and nucleotide-binding proteins as well as homologues of Ancylostoma-secreted proteins (ASPs). Using an in silico-subtractive analysis, 560 and 685 sequences were shown to be uniquely represented in the L3 and xL3 stages, respectively; the transcripts encoded ribosomal proteins, collagens and elongation factors (in L3), and mainly peptidases and other enzymes of amino acid catabolism (in xL3). Caenorhabditis elegans orthologues of transcripts that were uniquely transcribed in each L3 and xL3 were predicted to interact with a total of 535 other genes, all of which were involved in embryonic development. Conclusion The present study indicated that some key transcriptional alterations taking place during the transition from the L3 to the xL3 stage of H. contortus involve genes predicted to be linked to the development of neuronal tissue (L3 and xL3), formation of the cuticle (L3) and digestion of host haemoglobin (xL3). Future efforts using next-generation sequencing and bioinformatic technologies should provide the efficiency and depth of coverage required for the determination of the complete transcriptomes of different developmental stages and/or tissues of H. contortus as well as the genome of this important parasitic nematode. Such advances should lead to a significantly improved understanding of the molecular biology of H. contortus and, from an applied perspective, to novel methods of intervention.

Published
2010
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80. Schistosomiasis vaccine discovery using immunomics

Author

Loukas Alex, Doolan Denise L, Driguez Patrick, Felgner Philip L, and McManus Donald P

Subjects
Infectious and parasitic diseases, RC109-216
Abstract

Abstract The recent publication of the Schistosoma japonicum and S. mansoni genomes has expanded greatly the opportunities for post-genomic schistosomiasis vaccine research. Immunomics protein microarrays provide an excellent application of this new schistosome sequence information, having been utilised successfully for vaccine antigen discovery with a range of bacterial and viral pathogens, and malaria. Accordingly, we have designed and manufactured a Schistosoma immunomics protein microarray as a vaccine discovery tool. The microarray protein selection combined previously published data and in silico screening of available sequences for potential immunogens based on protein location, homology to known protective antigens, and high specificity to schistosome species. Following cloning, selected sequences were expressed cell-free and contact-printed onto nitrocellulose microarrays. The reactivity of microarray proteins with antisera from schistosomiasis-exposed/resistant animals or human patients can be measured with labelled secondary antibodies and a laser microarray scanner; highly reactive proteins can be further assessed as putative vaccines. This highly innovative technology has the potential to transform vaccine research for schistosomiasis and other parasitic diseases of humans and animals.

Published
2010
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81. Gene discovery for the carcinogenic human liver fluke, Opisthorchis viverrini

Author

Gasser Robin B, Smout Michael J, Sripa Manop, Sripa Banchob, Mulvenna Jason, Pinlaor Porntip, Laha Thewarach, Brindley Paul J, and Loukas Alex

Subjects
Biotechnology, TP248.13-248.65, Genetics, QH426-470
Abstract

Abstract Background Cholangiocarcinoma (CCA) – cancer of the bile ducts – is associated with chronic infection with the liver fluke, Opisthorchis viverrini. Despite being the only eukaryote that is designated as a 'class I carcinogen' by the International Agency for Research on Cancer, little is known about its genome. Results Approximately 5,000 randomly selected cDNAs from the adult stage of O. viverrini were characterized and accounted for 1,932 contigs, representing ~14% of the entire transcriptome, and, presently, the largest sequence dataset for any species of liver fluke. Twenty percent of contigs were assigned GO classifications. Abundantly represented protein families included those involved in physiological functions that are essential to parasitism, such as anaerobic respiration, reproduction, detoxification, surface maintenance and feeding. GO assignments were well conserved in relation to other parasitic flukes, however, some categories were over-represented in O. viverrini, such as structural and motor proteins. An assessment of evolutionary relationships showed that O. viverrini was more similar to other parasitic (Clonorchis sinensis and Schistosoma japonicum) than to free-living (Schmidtea mediterranea) flatworms, and 105 sequences had close homologues in both parasitic species but not in S. mediterranea. A total of 164 O. viverrini contigs contained ORFs with signal sequences, many of which were platyhelminth-specific. Examples of convergent evolution between host and parasite secreted/membrane proteins were identified as were homologues of vaccine antigens from other helminths. Finally, ORFs representing secreted proteins with known roles in tumorigenesis were identified, and these might play roles in the pathogenesis of O. viverrini-induced CCA. Conclusion This gene discovery effort for O. viverrini should expedite molecular studies of cholangiocarcinogenesis and accelerate research focused on developing new interventions, drugs and vaccines, to control O. viverrini and related flukes.

Published
2007
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82. The NLRP3 Inflammasome Suppresses Protective Immunity to Gastrointestinal Helminth Infection

Author

Alhallaf, Rafid, Agha, Zainab, Miller, Catherine M, Robertson, Avril, Sotillo, Javier, Croese, John, Cooper, Matthew A., Masters, Seth, Kupz, Andreas, Smith, Nicholas, Loukas, Alex, Alhallaf, Rafid, Agha, Zainab, Miller, Catherine M, Robertson, Avril, Sotillo, Javier, Croese, John, Cooper, Matthew A., Masters, Seth, Kupz, Andreas, Smith, Nicholas, and Loukas, Alex

Abstract

Inflammasomes promote immunity to microbial pathogens by regulating the function of IL-1-family cytokines such as IL-18 and IL-1 beta. However, the roles for inflammasomes during parasitic helminth infections remain unclear. We demonstrate that mice and humans infected with gastrointestinal nematodes display increased IL-18 secretion, which in Trichuris-infected or worm antigen-treated mice and in macrophages co-cultured with Trichuris antigens or exosome-like vesicles was dependent on the NLRP3 inflammasome. NLRP3-deficient mice displayed reduced pro-inflammatory type 1 cytokine responses and augmented protective type 2 immunity, which was reversed by IL-18 administration. NLRP3-dependent suppression of immunity partially required CD4(+) cells but was apparent even in Rag1(-/-) mice that lack adaptive immune cells, suggesting that NLRP3 influences both innate and adaptive immunity. These data highlight a role for NLRP3 in limiting protective immunity to helminths, suggesting that targeting the NLRP3 inflammasome may be an approach for limiting the disease burden associated with helminth infections.

Published
2018

83. Characterization of SR3 reveals abundance of non-LTR retrotransposons of the RTE clade in the genome of the human blood fluke, Schistosoma mansoni

Author

Brindley Paul J, Loukas Alex, Kewgrai Nonglack, and Laha Thewarach

Subjects
Biotechnology, TP248.13-248.65, Genetics, QH426-470
Abstract

Abstract Background It is becoming apparent that perhaps as much as half of the genome of the human blood fluke Schistosoma mansoni is constituted of mobile genetic element-related sequences. Non-long terminal repeat (LTR) retrotransposons, related to the LINE elements of mammals, comprise much of this repetitive component of the schistosome genome. Of more than 12 recognized clades of non-LTR retrotransposons, only members of the CR1, RTE, and R2 clades have been reported from the schistosome genome. Results Inspection of the nucleotide sequence of bacterial artificial chromosome number 49_J_14 from chromosome 1 of the genome of Schistosoma mansoni (GenBank AC093105) revealed the likely presence of several RTE-like retrotransposons. Among these, a new non-LTR retrotransposon designated SR3 was identified and is characterized here. Analysis of gene structure and phylogenetic analysis of both the reverse transcriptase and endonuclease domains of the mobile element indicated that SR3 represented a new family of RTE-like non-LTR retrotransposons. Remarkably, two full-length copies of SR3-like elements were present in BAC 49-J-14, and one of 3,211 bp in length appeared to be intact, indicating SR3 to be an active non-LTR retrotransposon. Both were flanked by target site duplications of 10–12 bp. Southern hybridization and bioinformatics analyses indicated the presence of numerous copies (probably >1,000) of SR3 interspersed throughout the genome of S. mansoni. Bioinformatics analyses also revealed SR3 to be transcribed in both larval and adult developmental stages of S. mansoni and to be also present in the genomes of the other major schistosome parasites of humans, Schistosoma haematobium and S. japonicum. Conclusion Numerous copies of SR3, a novel non-LTR retrotransposon of the RTE clade are present in the genome of S. mansoni. Non-LTR retrotransposons of the RTE clade including SR3 appear to have been remarkably successful in colonizing, and proliferation within the schistosome genome.

Published
2005
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86. Hookworm Secreted Extracellular Vesicles Interact With Host Cells and Prevent Inducible Colitis in Mice

Author

Eichenberger, Ramon M., primary, Ryan, Stephanie, additional, Jones, Linda, additional, Buitrago, Geraldine, additional, Polster, Ramona, additional, Montes de Oca, Marcela, additional, Zuvelek, Jennifer, additional, Giacomin, Paul R., additional, Dent, Lindsay A., additional, Engwerda, Christian R., additional, Field, Matthew A., additional, Sotillo, Javier, additional, and Loukas, Alex, additional

Published
2018
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87. The NLRP3 Inflammasome Suppresses Protective Immunity to Gastrointestinal Helminth Infection

Author

Alhallaf, Rafid, primary, Agha, Zainab, additional, Miller, Catherine M., additional, Robertson, Avril A.B., additional, Sotillo, Javier, additional, Croese, John, additional, Cooper, Matthew A., additional, Masters, Seth L., additional, Kupz, Andreas, additional, Smith, Nicholas C., additional, Loukas, Alex, additional, and Giacomin, Paul R., additional

Published
2018
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88. A novel blood-feeding detoxification pathway in Nippostrongylus brasiliensis L3 reveals a potential checkpoint for arresting hookworm development

Author

Bouchery, Tiffany, primary, Filbey, Kara, additional, Shepherd, Amy, additional, Chandler, Jodie, additional, Patel, Deepa, additional, Schmidt, Alfonso, additional, Camberis, Mali, additional, Peignier, Adeline, additional, Smith, Adam A. T., additional, Johnston, Karen, additional, Painter, Gavin, additional, Pearson, Mark, additional, Giacomin, Paul, additional, Loukas, Alex, additional, Bottazzi, Maria-Elena, additional, Hotez, Peter, additional, and LeGros, Graham, additional

Published
2018
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93. Sertraline, Paroxetine, and Chlorpromazine Are Rapidly Acting Anthelmintic Drugs Capable of Clinical Repurposing

Author

Weeks, Janis C., primary, Roberts, William M., additional, Leasure, Caitlyn, additional, Suzuki, Brian M., additional, Robinson, Kristin J., additional, Currey, Heather, additional, Wangchuk, Phurpa, additional, Eichenberger, Ramon M., additional, Saxton, Aleen D., additional, Bird, Thomas D., additional, Kraemer, Brian C., additional, Loukas, Alex, additional, Hawdon, John M., additional, Caffrey, Conor R., additional, and Liachko, Nicole F., additional

Published
2018
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94. Polypyridylruthenium(II) complexes exert anti-schistosome activity and inhibit parasite acetylcholinesterases

Author

Sundaraneedi, Madhu K., primary, Tedla, Bemnet A., additional, Eichenberger, Ramon M., additional, Becker, Luke, additional, Pickering, Darren, additional, Smout, Michael J., additional, Rajan, Siji, additional, Wangchuk, Phurpa, additional, Keene, F. Richard, additional, Loukas, Alex, additional, Collins, J. Grant, additional, and Pearson, Mark S., additional

Published
2017
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95. The parasite’s new clothes

Author

Pearson, Mark S and Loukas, Alex

Subjects
0301 basic medicine, QH301-705.5, Science, Population, Short Report, parasitic diseases, Bioinformatics, General Biochemistry, Genetics and Molecular Biology, Host-Parasite Interactions, 03 medical and health sciences, stem cells, Parasite hosting, Animals, Humans, Parasites, S. mansoni, Biology (General), education, Flatworm, education.field_of_study, Microbiology and Infectious Disease, General Immunology and Microbiology, biology, General Neuroscience, General Medicine, Schistosoma mansoni, 030108 mycology & parasitology, biology.organism_classification, Virology, Schistosomiasis mansoni, Adult Stem Cells, 030104 developmental biology, Developmental Biology and Stem Cells, Infectious disease (medical specialty), Medicine, Other, Stem cell, Insight, Developmental biology
Abstract

Schistosomes infect more than 200 million of the world's poorest people. These parasites live in the vasculature, producing eggs that spur a variety of chronic, potentially life-threatening, pathologies exacerbated by the long lifespan of schistosomes, that can thrive in the host for decades. How schistosomes maintain their longevity in this immunologically hostile environment is unknown. Here, we demonstrate that somatic stem cells in Schistosoma mansoni are biased towards generating a population of cells expressing factors associated exclusively with the schistosome host-parasite interface, a structure called the tegument. We show cells expressing these tegumental factors are short-lived and rapidly turned over. We suggest that stem cell-driven renewal of this tegumental lineage represents an important strategy for parasite survival in the context of the host vasculature. DOI: http://dx.doi.org/10.7554/eLife.12473.001, eLife digest Schistosomes are parasitic worms that infect and cause chronic disease in hundreds of millions of people in the developing world. A major reason these parasites are so damaging is that they are capable of living and reproducing in the human bloodstream for decades. Previous research had shown that schistosomes have a population of stem cells that are proposed to promote the parasite’s survival inside the host’s bloodstream. However, it was not clear what role these cells play in the worms. Collins et al. have now found that, in a parasitic worm called Schistosoma mansoni, a large number of these stem cells are destined to become cells that generate the parasite’s skin. This unique tissue is known as the tegument, and had long been thought to have evolved in parasitic flatworms to help them survive in their host and evade its immune defenses. Therefore, Collins et al.’s findings suggest a new mechanism by which stem cells can promote the survival of a parasite inside its host. In the long-term, these findings could lead to new treatments for parasitic infections and may shed light on the evolution of parasitic flatworms. An important future challenge will be to determine if disrupting these parasites’ stem cells, and their ability to generate new tegumental cells, has any effect on the parasite inside its host. DOI: http://dx.doi.org/10.7554/eLife.12473.002

Published
2016

97. Suppression of mRNAs encoding CD63 family tetraspanins from the carcinogenic liver fluke Opisthorchis viverrini results in distinct tegument phenotypes

Author

Chaiyadet, Sujittra, primary, Krueajampa, Watchara, additional, Hipkaeo, Wiphawi, additional, Plosan, Yada, additional, Piratae, Supawadee, additional, Sotillo, Javier, additional, Smout, Michael, additional, Sripa, Banchob, additional, Brindley, Paul J., additional, Loukas, Alex, additional, and Laha, Thewarach, additional

Published
2017
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