Resurrection of ancestral effector caspases identifies novel networks for evolution of substrate specificity

Grinshpon, Robert D.; Shrestha, Suman; Titus-McQuillan, James; Hamilton, Paul T.; Swartz, Paul D.; Clark, A. Clay

doi:10.1042/bcj20190625

Title: Resurrection of ancestral effector caspases identifies novel networks for evolution of substrate specificity

Journal Article · Thu Nov 21 00:00:00 EST 2019 · Biochemical Journal

DOI:https://doi.org/10.1042/bcj20190625· OSTI ID:1577159

Grinshpon, Robert D. ^[1]; Shrestha, Suman ^[2]; Titus-McQuillan, James ^[2]; Hamilton, Paul T. ^[3]; Swartz, Paul D. ^[3];

^[2]

North Carolina State Univ., Raleigh, NC (United States); Univ. of Texas, Arlington, TX (United States)
Univ. of Texas, Arlington, TX (United States)
North Carolina State Univ., Raleigh, NC (United States)

Apoptotic caspases evolved with metazoans more than 950 million years ago (MYA), and a series of gene duplications resulted in two subfamilies consisting of initiator and effector caspases. The effector caspase genes (caspases-3, -6, and -7) were subsequently fixed into the Chordata phylum more than 650 MYA when the gene for a common ancestor (CA) duplicated, and the three effector caspases have persisted throughout mammalian evolution. All caspases prefer an aspartate residue at the P1 position of substrates, so each caspase evolved discrete cellular roles through changes in substrate recognition at the P4 position combined with allosteric regulation. We examined the evolution of substrate specificity in caspase-6, which prefers valine at the P4 residue, compared with caspases-3 and -7, which prefer aspartate, by reconstructing the CA of effector caspases (AncCP-Ef1) and the CA of caspase-6 (AncCP-6An). We show that AncCP-Ef1 is a promiscuous enzyme with little distinction between Asp, Val, or Leu at P4. The specificity of caspase-6 was defined early in its evolution, where AncCP-6An demonstrates a preference for Val over Asp at P4. Structures of AncCP-Ef1 and of AncCP-6An show a network of charged amino acids near the S4 pocket that, when combined with repositioning a flexible active site loop, resulted in a more hydrophobic binding pocket in AncCP-6An. The ancestral protein reconstructions show that the caspase-hemoglobinase fold has been conserved for over 650 million years and that only three substitutions in the scaffold are necessary to shift substrate selection toward Val over Asp.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Contributing Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Grant/Contract Number:: W-31-109-ENG-38

OSTI ID:: 1577159

Journal Information:: Biochemical Journal, Vol. 476, Issue 22; ISSN 0264-6021

Publisher:: Biochemical SocietyCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 12 works

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59 BASIC BIOLOGICAL SCIENCES
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ancestral protein reconstruction
caspase
computational biology
functional divergence
protein evolution

Title: Resurrection of ancestral effector caspases identifies novel networks for evolution of substrate specificity

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References (91)

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