Variable substrate preference among phospholipase D toxins from sicariid spiders

Lajoie, Daniel M.; Roberts, Sue A.; Zobel-Thropp, Pamela A.; Delahaye, Jared L.; Bandarian, Vahe; Binford, Greta J.; Cordes, Matthew H. J.

doi:10.1074/jbc.m115.636951

Title: Variable substrate preference among phospholipase D toxins from sicariid spiders

Journal Article · Mon Mar 09 00:00:00 EDT 2015 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.m115.636951· OSTI ID:1347988

Lajoie, Daniel M. ^[1]; Roberts, Sue A. ^[1]; Zobel-Thropp, Pamela A. ^[2]; Delahaye, Jared L. ^[2]; Bandarian, Vahe ^[1]; Binford, Greta J. ^[2]; Cordes, Matthew H. J. ^[1]

Univ. of Arizona, Tucson, AZ (United States)
Lewis and Clark College, Portland, OR (United States)

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.

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Research Organization:: Stanford Univ., CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-76SF00515; P41GM103393; R15-GM-097676-01; R01 GM72623; IOB 0546858

OSTI ID:: 1347988

Journal Information:: Journal of Biological Chemistry, Vol. 290, Issue 17; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 28 works

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59 BASIC BIOLOGICAL SCIENCES
crystal structure
enzyme mechanism
Loxosceles
Loxoscelism
phospholipase D
sicarius
sphingomyelinase
substrate specificity
toxin

Title: Variable substrate preference among phospholipase D toxins from sicariid spiders

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