TY - JOUR
T1 - Aspartyl Protease Inhibitors as Anti-Filarial Drugs
AU - Beld, Liana
AU - Jung, Hyeim
AU - Bulman, Christina A.
AU - Rosa, Bruce A.
AU - Fischer, Peter U.
AU - Janetka, James W.
AU - Lustigman, Sara
AU - Sakanari, Judy A.
AU - Mitreva, Makedonka
N1 - Funding Information:
Funding: This research was funded in part by the National Institute of Allergy and Infectious Diseases, grant number 1R01AI159450.
Funding Information:
Acknowledgments: We thank Wandy Beatty from the Molecular Microbiology Imaging Core Facility of Washington University for the TEM immunolabeling of B. malayi sections, and Kerstin Fischer for her expert technical support with the immunolocalization. The immunolocalization was supported by the Foundation of the Barnes Jewish Hospital. We thank John Martin for analytical processing and submission of the RNA-seq data, and Joseph F. Urban from the USDA for providing adult T. muris. The following reagents were provided by the NIH/NIAID Filariasis Research Reagent Resource Center for distribution through BEI Resources, NIAID, NIH: Adult Female Brugia malayi (live), NR-48892 and Adult Female Brugia pahangi (live), NR-48903.
Publisher Copyright:
© 2022 by the authors. Licensee MDPI, Basel, Switzerland.
PY - 2022/6
Y1 - 2022/6
N2 - The current treatments for lymphatic filariasis and onchocerciasis do not effectively kill the adult parasitic nematodes, allowing these chronic and debilitating diseases to persist in millions of people. Thus, the discovery of new drugs with macrofilaricidal potential to treat these filarial diseases is critical. To facilitate this need, we first investigated the effects of three aspartyl protease inhibitors (APIs) that are FDA-approved as HIV antiretroviral drugs on the adult filarial nematode, Brugia malayi and the endosymbiotic bacteria, Wolbachia. From the three hits, nelfinavir had the best potency with an IC50 value of 7.78 µM, followed by ritonavir and lopinavir with IC50 values of 14.3 µM and 16.9 µM, respectively. The three APIs have a direct effect on killing adult B. malayi after 6 days of exposure in vitro and did not affect the Wolbachia titers. Sequence conservation and stage-specific gene expression analysis identified Bm8660 as the most likely primary aspartic protease target for these drug(s). Immunolocalization using antibodies raised against the Bm8660 ortholog of Onchocerca volvulus showed it is strongly expressed in female B. malayi, especially in metabolically active tissues such as lateral and dorsal/ventral chords, hypodermis, and uterus tissue. Global transcriptional response analysis using adult female B. pahangi treated with APIs identified four additional aspartic proteases differentially regulated by the three effective drugs, as well as significant enrichment of various pathways including ubiquitin mediated proteolysis, protein kinases, and MAPK/AMPK/FoxO signaling. In vitro testing against the adult gastro-intestinal nematode Trichuris muris suggested broad-spectrum potential for these APIs. This study suggests that APIs may serve as new leads to be further explored for drug discovery to treat parasitic nematode infections.
AB - The current treatments for lymphatic filariasis and onchocerciasis do not effectively kill the adult parasitic nematodes, allowing these chronic and debilitating diseases to persist in millions of people. Thus, the discovery of new drugs with macrofilaricidal potential to treat these filarial diseases is critical. To facilitate this need, we first investigated the effects of three aspartyl protease inhibitors (APIs) that are FDA-approved as HIV antiretroviral drugs on the adult filarial nematode, Brugia malayi and the endosymbiotic bacteria, Wolbachia. From the three hits, nelfinavir had the best potency with an IC50 value of 7.78 µM, followed by ritonavir and lopinavir with IC50 values of 14.3 µM and 16.9 µM, respectively. The three APIs have a direct effect on killing adult B. malayi after 6 days of exposure in vitro and did not affect the Wolbachia titers. Sequence conservation and stage-specific gene expression analysis identified Bm8660 as the most likely primary aspartic protease target for these drug(s). Immunolocalization using antibodies raised against the Bm8660 ortholog of Onchocerca volvulus showed it is strongly expressed in female B. malayi, especially in metabolically active tissues such as lateral and dorsal/ventral chords, hypodermis, and uterus tissue. Global transcriptional response analysis using adult female B. pahangi treated with APIs identified four additional aspartic proteases differentially regulated by the three effective drugs, as well as significant enrichment of various pathways including ubiquitin mediated proteolysis, protein kinases, and MAPK/AMPK/FoxO signaling. In vitro testing against the adult gastro-intestinal nematode Trichuris muris suggested broad-spectrum potential for these APIs. This study suggests that APIs may serve as new leads to be further explored for drug discovery to treat parasitic nematode infections.
KW - Neglected tropical diseases (NTDs)
KW - Trichuris
KW - anti-filarial drugs
KW - filarial nematodes
KW - gastro-intestinal nematodes
KW - macrofilaricidal
UR - http://www.scopus.com/inward/record.url?scp=85132701967&partnerID=8YFLogxK
U2 - 10.3390/pathogens11060707
DO - 10.3390/pathogens11060707
M3 - Article
C2 - 35745561
AN - SCOPUS:85132701967
SN - 2076-0817
VL - 11
JO - Pathogens
JF - Pathogens
IS - 6
M1 - 707
ER -