Variable substrate preference among phospholipase D toxins from sicariid spiders
Abstract
Venoms of the sicariid spiders contain phospholipase D enzyme toxins that can cause severe dermonecrosis and even death in humans. These enzymes convert sphingolipid and lysolipid substrates to cyclic phosphates by activating a hydroxyl nucleophile present in both classes of lipid. The most medically relevant substrates are thought to be sphingomyelin and/or lysophosphatidylcholine. To better understand the substrate preference of these toxins, we used 31P NMR to compare the activity of three related but phylogenetically diverse sicariid toxins against a diverse panel of sphingolipid and lysolipid substrates. Two of the three showed significantly faster turnover of sphingolipids over lysolipids, and all three showed a strong preference for positively charged (choline and/or ethanolamine) over neutral (glycerol and serine) headgroups. Strikingly, however, the enzymes vary widely in their preference for choline, the headgroup of both sphingomyelin and lysophosphatidylcholine, versus ethanolamine. An enzyme from Sicarius terrosus showed a strong preference for ethanolamine over choline, whereas two paralogous enzymes from Loxosceles arizonica either preferred choline or showed no significant preference. Intrigued by the novel substrate preference of the Sicarius enzyme, we solved its crystal structure at 2.1 Å resolution. Lastly, the evolution of variable substrate specificity may help explain the reduced dermonecrotic potential ofmore »
- Authors:
-
- Univ. of Arizona, Tucson, AZ (United States)
- Lewis and Clark College, Portland, OR (United States)
- Publication Date:
- Research Org.:
- Stanford Univ., CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
- OSTI Identifier:
- 1347988
- Grant/Contract Number:
- AC02-76SF00515; P41GM103393; R15-GM-097676-01; R01 GM72623; IOB 0546858
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 290; Journal Issue: 17; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; crystal structure; enzyme mechanism; Loxosceles; Loxoscelism; phospholipase D; sicarius; sphingomyelinase; substrate specificity; toxin
Citation Formats
Lajoie, Daniel M., Roberts, Sue A., Zobel-Thropp, Pamela A., Delahaye, Jared L., Bandarian, Vahe, Binford, Greta J., and Cordes, Matthew H. J. Variable substrate preference among phospholipase D toxins from sicariid spiders. United States: N. p., 2015.
Web. doi:10.1074/jbc.m115.636951.
Lajoie, Daniel M., Roberts, Sue A., Zobel-Thropp, Pamela A., Delahaye, Jared L., Bandarian, Vahe, Binford, Greta J., & Cordes, Matthew H. J. Variable substrate preference among phospholipase D toxins from sicariid spiders. United States. https://doi.org/10.1074/jbc.m115.636951
Lajoie, Daniel M., Roberts, Sue A., Zobel-Thropp, Pamela A., Delahaye, Jared L., Bandarian, Vahe, Binford, Greta J., and Cordes, Matthew H. J. Mon .
"Variable substrate preference among phospholipase D toxins from sicariid spiders". United States. https://doi.org/10.1074/jbc.m115.636951. https://www.osti.gov/servlets/purl/1347988.
@article{osti_1347988,
title = {Variable substrate preference among phospholipase D toxins from sicariid spiders},
author = {Lajoie, Daniel M. and Roberts, Sue A. and Zobel-Thropp, Pamela A. and Delahaye, Jared L. and Bandarian, Vahe and Binford, Greta J. and Cordes, Matthew H. J.},
abstractNote = {Venoms of the sicariid spiders contain phospholipase D enzyme toxins that can cause severe dermonecrosis and even death in humans. These enzymes convert sphingolipid and lysolipid substrates to cyclic phosphates by activating a hydroxyl nucleophile present in both classes of lipid. The most medically relevant substrates are thought to be sphingomyelin and/or lysophosphatidylcholine. To better understand the substrate preference of these toxins, we used 31P NMR to compare the activity of three related but phylogenetically diverse sicariid toxins against a diverse panel of sphingolipid and lysolipid substrates. Two of the three showed significantly faster turnover of sphingolipids over lysolipids, and all three showed a strong preference for positively charged (choline and/or ethanolamine) over neutral (glycerol and serine) headgroups. Strikingly, however, the enzymes vary widely in their preference for choline, the headgroup of both sphingomyelin and lysophosphatidylcholine, versus ethanolamine. An enzyme from Sicarius terrosus showed a strong preference for ethanolamine over choline, whereas two paralogous enzymes from Loxosceles arizonica either preferred choline or showed no significant preference. Intrigued by the novel substrate preference of the Sicarius enzyme, we solved its crystal structure at 2.1 Å resolution. Lastly, the evolution of variable substrate specificity may help explain the reduced dermonecrotic potential of some natural toxin variants, because mammalian sphingolipids use primarily choline as a positively charged headgroup; it may also be relevant for sicariid predatory behavior, because ethanolamine-containing sphingolipids are common in insect prey.},
doi = {10.1074/jbc.m115.636951},
journal = {Journal of Biological Chemistry},
number = 17,
volume = 290,
place = {United States},
year = {Mon Mar 09 00:00:00 EDT 2015},
month = {Mon Mar 09 00:00:00 EDT 2015}
}
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