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Title: A redox-active, compact molecule for cross-linking amyloidogenic peptides into nontoxic, off-pathway aggregates: In vitro and in vivo efficacy and molecular mechanisms

Abstract

Chemical reagents targeting and controlling amyloidogenic peptides have received much attention for helping identify their roles in the pathogenesis of protein-misfolding disorders. In this paper, we report a novel strategy for redirecting amyloidogenic peptides into nontoxic, off-pathway aggregates, which utilizes redox properties of a small molecule (DMPD, N,N-dimethyl-p-phenylenediamine) to trigger covalent adduct formation with the peptide. In addition, for the first time, biochemical, biophysical, and molecular dynamics simulation studies have been performed to demonstrate a mechanistic understanding for such an interaction between a small molecule (DMPD) and amyloid-β (Aβ) and its subsequent anti-amyloidogenic activity, which, upon its transformation, generates ligand–peptide adducts via primary amine-dependent intramolecular cross-linking correlated with structural compaction. Furthermore, in vivo efficacy of DMPD toward amyloid pathology and cognitive impairment was evaluated employing 5xFAD mice of Alzheimer’s disease (AD). Such a small molecule (DMPD) is indicated to noticeably reduce the overall cerebral amyloid load of soluble Aβ forms and amyloid deposits as well as significantly improve cognitive defects in the AD mouse model. Altogether our in vitro and in vivo studies of DMPD toward Aβ with the first molecular-level mechanistic investigations present the feasibility of developing new, innovative approaches that employ redox-active compounds without the structural complexity asmore » next-generation chemical tools for amyloid management.« less

Authors:
 [1];  [2];  [1];  [3];  [4];  [5];  [3];  [6];  [7];  [2];  [2];  [7];  [5];  [6];  [8];  [2];  [1]
+ Show Author Affiliations
  1. Ulsan National Institute of Science and Technology (UNIST), Ulsan (Korea)
  2. Univ. of Michigan, Ann Arbor, MI (United States)
  3. Asan Medical Center, Seoul (Korea)
  4. Ulsan National Institute of Science and Technology (UNIST), Ulsan (Korea); Univ. of Michigan, Ann Arbor, MI (United States)
  5. Univ. of Cincinnati, Cincinnati, OH (United States)
  6. Univ. of Nevada, Reno, NV (United States)
  7. Univ. of Miami, Coral Gables, FL (United States)
  8. Asan Medical Center, Seoul (Korea); Univ. of Ulsan College of Medicine, Seoul (Korea)
Publication Date:
Research Org.:
Univ. of Michigan, Ann Arbor, MI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1345989
Grant/Contract Number:  
AC02-98CH10886
Resource Type:
Accepted Manuscript
Journal Name:
Journal of the American Chemical Society
Additional Journal Information:
Journal Volume: 137; Journal Issue: 46; Journal ID: ISSN 0002-7863
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Derrick, Jeffrey S., Kerr, Richard A., Nam, Younwoo, Oh, Shin Bi, Lee, Hyuck Jin, Earnest, Kaylin G., Suh, Nayoung, Peck, Kristy L., Ozbil, Mehmet, Korshavn, Kyle J., Ramamoorthy, Ayyalusamy, Prabhakar, Rajeev, Merino, Edward J., Shearer, Jason, Lee, Joo -Yong, Ruotolo, Brandon T., and Lim, Mi Hee. A redox-active, compact molecule for cross-linking amyloidogenic peptides into nontoxic, off-pathway aggregates: In vitro and in vivo efficacy and molecular mechanisms. United States: N. p., 2015. Web. doi:10.1021/jacs.5b10043.
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Derrick, Jeffrey S., Kerr, Richard A., Nam, Younwoo, Oh, Shin Bi, Lee, Hyuck Jin, Earnest, Kaylin G., Suh, Nayoung, Peck, Kristy L., Ozbil, Mehmet, Korshavn, Kyle J., Ramamoorthy, Ayyalusamy, Prabhakar, Rajeev, Merino, Edward J., Shearer, Jason, Lee, Joo -Yong, Ruotolo, Brandon T., & Lim, Mi Hee. A redox-active, compact molecule for cross-linking amyloidogenic peptides into nontoxic, off-pathway aggregates: In vitro and in vivo efficacy and molecular mechanisms. United States. https://doi.org/10.1021/jacs.5b10043
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Derrick, Jeffrey S., Kerr, Richard A., Nam, Younwoo, Oh, Shin Bi, Lee, Hyuck Jin, Earnest, Kaylin G., Suh, Nayoung, Peck, Kristy L., Ozbil, Mehmet, Korshavn, Kyle J., Ramamoorthy, Ayyalusamy, Prabhakar, Rajeev, Merino, Edward J., Shearer, Jason, Lee, Joo -Yong, Ruotolo, Brandon T., and Lim, Mi Hee. Tue . "A redox-active, compact molecule for cross-linking amyloidogenic peptides into nontoxic, off-pathway aggregates: In vitro and in vivo efficacy and molecular mechanisms". United States. https://doi.org/10.1021/jacs.5b10043. https://www.osti.gov/servlets/purl/1345989.
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@article{osti_1345989,
title = {A redox-active, compact molecule for cross-linking amyloidogenic peptides into nontoxic, off-pathway aggregates: In vitro and in vivo efficacy and molecular mechanisms},
author = {Derrick, Jeffrey S. and Kerr, Richard A. and Nam, Younwoo and Oh, Shin Bi and Lee, Hyuck Jin and Earnest, Kaylin G. and Suh, Nayoung and Peck, Kristy L. and Ozbil, Mehmet and Korshavn, Kyle J. and Ramamoorthy, Ayyalusamy and Prabhakar, Rajeev and Merino, Edward J. and Shearer, Jason and Lee, Joo -Yong and Ruotolo, Brandon T. and Lim, Mi Hee},
abstractNote = {Chemical reagents targeting and controlling amyloidogenic peptides have received much attention for helping identify their roles in the pathogenesis of protein-misfolding disorders. In this paper, we report a novel strategy for redirecting amyloidogenic peptides into nontoxic, off-pathway aggregates, which utilizes redox properties of a small molecule (DMPD, N,N-dimethyl-p-phenylenediamine) to trigger covalent adduct formation with the peptide. In addition, for the first time, biochemical, biophysical, and molecular dynamics simulation studies have been performed to demonstrate a mechanistic understanding for such an interaction between a small molecule (DMPD) and amyloid-β (Aβ) and its subsequent anti-amyloidogenic activity, which, upon its transformation, generates ligand–peptide adducts via primary amine-dependent intramolecular cross-linking correlated with structural compaction. Furthermore, in vivo efficacy of DMPD toward amyloid pathology and cognitive impairment was evaluated employing 5xFAD mice of Alzheimer’s disease (AD). Such a small molecule (DMPD) is indicated to noticeably reduce the overall cerebral amyloid load of soluble Aβ forms and amyloid deposits as well as significantly improve cognitive defects in the AD mouse model. Altogether our in vitro and in vivo studies of DMPD toward Aβ with the first molecular-level mechanistic investigations present the feasibility of developing new, innovative approaches that employ redox-active compounds without the structural complexity as next-generation chemical tools for amyloid management.},
doi = {10.1021/jacs.5b10043},
journal = {Journal of the American Chemical Society},
number = 46,
volume = 137,
place = {United States},
year = {Tue Nov 17 00:00:00 EST 2015},
month = {Tue Nov 17 00:00:00 EST 2015}
}
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https://doi.org/10.1021/jacs.5b10043
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