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Article ; Online: Structural variants identified using non-Mendelian inheritance patterns advance the mechanistic understanding of autism spectrum disorder

David Kainer / Alan R. Templeton / Erica T. Prates / Daniel Jacboson / Euan R.O. Allan / Sharlee Climer / Michael R. Garvin

HGG Advances, Vol 4, Iss 1, Pp 100150- (2023)

1480

Abstract: Summary: The heritability of autism spectrum disorder (ASD), based on 680,000 families and five countries, is estimated to be nearly 80%, yet heritability reported from SNP-based studies are consistently lower, and few significant loci have been ... ...

Abstract	Summary: The heritability of autism spectrum disorder (ASD), based on 680,000 families and five countries, is estimated to be nearly 80%, yet heritability reported from SNP-based studies are consistently lower, and few significant loci have been identified with genome-wide association studies. This gap in genomic information may reside in rare variants, interaction among variants (epistasis), or cryptic structural variation (SV) and may provide mechanisms that underlie ASD. Here we use a method to identify potential SVs based on non-Mendelian inheritance patterns in pedigrees using parent-child genotypes from ASD families and demonstrate that they are enriched in ASD-risk genes. Most are in non-coding genic space and are over-represented in expression quantitative trait loci, suggesting that they affect gene regulation, which we confirm with their overlap of differentially expressed genes in postmortem brain tissue of ASD individuals. We then identify an SV in the GRIK2 gene that alters RNA splicing and a regulatory region of the ACMSD gene in the kynurenine pathway as significantly associated with a non-verbal ASD phenotype, supporting our hypothesis that these currently excluded loci can provide a clearer mechanistic understanding of ASD. Finally, we use an explainable artificial intelligence approach to define subgroups demonstrating their use in the context of precision medicine.
Keywords	Genomic structural variation ; missing heritability ; autism spectrum disorder ; Mendelian inheritance ; artificial intelligence ; precision medicine ; Genetics ; QH426-470
Language	English
Publishing date	2023-01-01T00:00:00Z
Publisher	Elsevier
Document type	Article ; Online
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Article ; Online: Structural variants identified using non-Mendelian inheritance patterns advance the mechanistic understanding of autism spectrum disorder.

Kainer, David / Templeton, Alan R / Prates, Erica T / Jacboson, Daniel / Allan, Euan R O / Climer, Sharlee / Garvin, Michael R

HGG advances

2022 Volume 4, Issue 1, Page(s) 100150

Abstract: The heritability of autism spectrum disorder (ASD), based on 680,000 families and five countries, is estimated to be nearly 80%, yet heritability reported from SNP-based studies are consistently lower, and few significant loci have been identified with ... ...

Abstract	The heritability of autism spectrum disorder (ASD), based on 680,000 families and five countries, is estimated to be nearly 80%, yet heritability reported from SNP-based studies are consistently lower, and few significant loci have been identified with genome-wide association studies. This gap in genomic information may reside in rare variants, interaction among variants (epistasis), or cryptic structural variation (SV) and may provide mechanisms that underlie ASD. Here we use a method to identify potential SVs based on non-Mendelian inheritance patterns in pedigrees using parent-child genotypes from ASD families and demonstrate that they are enriched in ASD-risk genes. Most are in non-coding genic space and are over-represented in expression quantitative trait loci, suggesting that they affect gene regulation, which we confirm with their overlap of differentially expressed genes in postmortem brain tissue of ASD individuals. We then identify an SV in the GRIK2 gene that alters RNA splicing and a regulatory region of the
MeSH term(s)	Humans ; Autism Spectrum Disorder/genetics ; Genome-Wide Association Study/methods ; Artificial Intelligence ; Quantitative Trait Loci/genetics ; Inheritance Patterns/genetics
Language	English
Publishing date	2022-10-06
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural
ISSN	2666-2477
ISSN (online)	2666-2477
DOI	10.1016/j.xhgg.2022.100150
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Article ; Online: Characterization of aromatic acid/proton symporters in Pseudomonas putida KT2440 toward efficient microbial conversion of lignin-related aromatics.

Wada, Ayumu / Prates, Érica T / Hirano, Ryo / Werner, Allison Z / Kamimura, Naofumi / Jacobson, Daniel A / Beckham, Gregg T / Masai, Eiji

Metabolic engineering

2021 Volume 64, Page(s) 167–179

Abstract: Pseudomonas putida KT2440 (hereafter KT2440) is a well-studied platform bacterium for the production of industrially valuable chemicals from heterogeneous mixtures of aromatic compounds obtained from lignin depolymerization. KT2440 can grow on lignin- ... ...

Abstract	Pseudomonas putida KT2440 (hereafter KT2440) is a well-studied platform bacterium for the production of industrially valuable chemicals from heterogeneous mixtures of aromatic compounds obtained from lignin depolymerization. KT2440 can grow on lignin-related monomers, such as ferulate (FA), 4-coumarate (4CA), vanillate (VA), 4-hydroxybenzoate (4HBA), and protocatechuate (PCA). Genes associated with their catabolism are known, but knowledge about the uptake systems remains limited. In this work, we studied the KT2440 transporters of lignin-related monomers and their substrate selectivity. Based on the inhibition by protonophores, we focused on five genes encoding aromatic acid/H
MeSH term(s)	Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Lignin/metabolism ; Protons ; Pseudomonas putida/genetics ; Pseudomonas putida/metabolism ; Symporters
Chemical Substances	Bacterial Proteins ; Protons ; Symporters ; Lignin (9005-53-2)
Language	English
Publishing date	2021-02-04
Publishing country	Belgium
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1470383-x
ISSN	1096-7184 ; 1096-7176
ISSN (online)	1096-7184
ISSN	1096-7176
DOI	10.1016/j.ymben.2021.01.013
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Article ; Online: Catalytic Mechanism of Aryl-Ether Bond Cleavage in Lignin by LigF and LigG.

Prates, Erica Teixeira / Crowley, Michael F / Skaf, Munir S / Beckham, Gregg T

The journal of physical chemistry. B

2019 Volume 123, Issue 48, Page(s) 10142–10151

Abstract: Given the abundance of lignin in nature, multiple enzyme systems have been discovered to cleave the β-O-4 bonds, the most prevalent intermonomer linkage. In particular, stereospecific cleavage of lignin oligomers by ... ...

Abstract	Given the abundance of lignin in nature, multiple enzyme systems have been discovered to cleave the β-O-4 bonds, the most prevalent intermonomer linkage. In particular, stereospecific cleavage of lignin oligomers by glutathione
MeSH term(s)	Bacterial Proteins/chemistry ; Bacterial Proteins/metabolism ; Biocatalysis ; Catalytic Domain ; Coenzymes/chemistry ; Coenzymes/metabolism ; Glutathione/chemistry ; Glutathione/metabolism ; Glycoconjugates/chemistry ; Glycoconjugates/metabolism ; Hydrolysis ; Kinetics ; Lignin/chemistry ; Lignin/metabolism ; Lyases/chemistry ; Lyases/metabolism ; Molecular Dynamics Simulation ; Oxidoreductases/chemistry ; Oxidoreductases/metabolism ; Protein Binding ; Protein Interaction Domains and Motifs ; Protein Structure, Secondary ; Quantum Theory ; Sphingomonas/chemistry ; Sphingomonas/enzymology ; Stereoisomerism ; Substrate Specificity ; Thermodynamics
Chemical Substances	Bacterial Proteins ; Coenzymes ; Glycoconjugates ; Lignin (9005-53-2) ; Oxidoreductases (EC 1.-) ; aryl ether cleaving enzyme (EC 1.-) ; Lyases (EC 4.-) ; Glutathione (GAN16C9B8O)
Language	English
Publishing date	2019-11-19
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1520-5207
ISSN (online)	1520-5207
DOI	10.1021/acs.jpcb.9b06243
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Article: Catalytic Mechanism of Aryl-Ether Bond Cleavage in Lignin by LigF and LigG

Prates, Erica Teixeira / Crowley, Michael F / Skaf, Munir S / Beckham, Gregg T

Journal of physical chemistry. 2019 Nov. 05, v. 123, no. 48

2019

Abstract	Given the abundance of lignin in nature, multiple enzyme systems have been discovered to cleave the β-O-4 bonds, the most prevalent intermonomer linkage. In particular, stereospecific cleavage of lignin oligomers by glutathione S-transferases (GSTs) has been reported in several sphingomonads. Here, we apply quantum mechanics/molecular mechanics simulations to study the mechanism of two glutathione-dependent enzymes in the β-aryl ether catabolic pathway of Sphingomonas sp. SYK-6, namely, LigF, a β-etherase, and LigG, a lyase. For LigF, the free-energy landscape supports a SN2 reaction mechanism, with the monoaromatic leaving group being promptly neutralized upon release. Specific interactions with conserved residues are responsible for stereoselectivity and for activation of the cofactor as a nucleophile. A glutathione conjugate is also released by LigF and serves the substrate of LigG, undergoing a SN2-like reaction, in which Cys15 acts as the nucleophile, to yield the second monoaromatic product. The simulations suggest that the electron-donating substituent at the para-position found in lignin-derived aromatics and the interaction with Tyr217 are essential for reactivity in LigG. Overall, this work deepens the understanding of the stereospecific enzymatic mechanisms in the β-aryl ether cleavage pathway and reveals key structural features underpinning the ligninolytic activity detected in several sphingomonad GSTs.
Keywords	Gibbs free energy ; Lewis bases ; Sphingomonas ; aromatic compounds ; biochemical pathways ; catalytic activity ; cleavage (chemistry) ; glutathione ; glutathione transferase ; lignin ; neutralization ; physical chemistry ; quantum mechanics ; reaction mechanisms ; stereoselectivity ; stereospecificity
Language	English
Dates of publication	2019-1105
Size	p. 10142-10151.
Publishing place	American Chemical Society
Document type	Article
ISSN	1520-5207
DOI	10.1021/acs.jpcb.9b06243
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Article: Characterization of aromatic acid/proton symporters in Pseudomonas putida KT2440 toward efficient microbial conversion of lignin-related aromatics

Wada, Ayumu / Prates, Érica T / Hirano, Ryo / Werner, Allison Z / Kamimura, Naofumi / Jacobson, Daniel A / Beckham, Gregg T / Masai, Eiji

International Metabolic Engineering Society Metabolic engineering. 2021 Mar., v. 64

2021

Abstract	Pseudomonas putida KT2440 (hereafter KT2440) is a well-studied platform bacterium for the production of industrially valuable chemicals from heterogeneous mixtures of aromatic compounds obtained from lignin depolymerization. KT2440 can grow on lignin-related monomers, such as ferulate (FA), 4-coumarate (4CA), vanillate (VA), 4-hydroxybenzoate (4HBA), and protocatechuate (PCA). Genes associated with their catabolism are known, but knowledge about the uptake systems remains limited. In this work, we studied the KT2440 transporters of lignin-related monomers and their substrate selectivity. Based on the inhibition by protonophores, we focused on five genes encoding aromatic acid/H⁺ symporter family transporters categorized into major facilitator superfamily that uses the proton motive force. The mutants of PP_1376 (pcaK) and PP_3349 (hcnK) exhibited significantly reduced growth on PCA/4HBA and FA/4CA, respectively, while no change was observed on VA for any of the five gene mutants. At pH 9.0, the conversion of these compounds by hcnK mutant (FA/4CA) and vanK mutant (VA) was dramatically reduced, revealing that these transporters are crucial for the uptake of the anionic substrates at high pH. Uptake assays using ¹⁴C-labeled substrates in Escherichia coli and biosensor-based assays confirmed that PcaK, HcnK, and VanK have ability to take up PCA, FA/4CA, and VA/PCA, respectively. Additionally, analyses of the predicted protein structures suggest that the size and hydropathic properties of the substrate-binding sites of these transporters determine their substrate preferences. Overall, this study reveals that at physiological pH, PcaK and HcnK have a major role in the uptake of PCA/4HBA and FA/4CA, respectively, and VanK is a VA/PCA transporter. This information can contribute to the engineering of strains for the efficient conversion of lignin-related monomers to value-added chemicals.
Keywords	4-hydroxybenzoic acid ; Escherichia coli ; Pseudomonas putida ; bacteria ; catabolism ; depolymerization ; genes ; lignin ; mutants ; pH ; proton-motive force ; symporters ; value added
Language	English
Dates of publication	2021-03
Size	p. 167-179.
Publishing place	Elsevier Inc.
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	1470383-x
ISSN	1096-7184 ; 1096-7176
ISSN (online)	1096-7184
ISSN	1096-7176
DOI	10.1016/j.ymben.2021.01.013
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Article ; Online: Potential Pathogenicity Determinants Identified from Structural Proteomics of SARS-CoV and SARS-CoV-2.

Prates, Erica T / Garvin, Michael R / Pavicic, Mirko / Jones, Piet / Shah, Manesh / Demerdash, Omar / Amos, B Kirtley / Geiger, Armin / Jacobson, Daniel

Molecular biology and evolution

2020 Volume 38, Issue 2, Page(s) 702–715

Abstract: Despite SARS-CoV and SARS-CoV-2 being equipped with highly similar protein arsenals, the corresponding zoonoses have spread among humans at extremely different rates. The specific characteristics of these viruses that led to such distinct outcomes remain ...

Abstract	Despite SARS-CoV and SARS-CoV-2 being equipped with highly similar protein arsenals, the corresponding zoonoses have spread among humans at extremely different rates. The specific characteristics of these viruses that led to such distinct outcomes remain unclear. Here, we apply proteome-wide comparative structural analysis aiming to identify the unique molecular elements in the SARS-CoV-2 proteome that may explain the differing consequences. By combining protein modeling and molecular dynamics simulations, we suggest nonconservative substitutions in functional regions of the spike glycoprotein (S), nsp1, and nsp3 that are contributing to differences in virulence. Particularly, we explain why the substitutions at the receptor-binding domain of S affect the structure-dynamics behavior in complexes with putative host receptors. Conservation of functional protein regions within the two taxa is also noteworthy. We suggest that the highly conserved main protease, nsp5, of SARS-CoV and SARS-CoV-2 is part of their mechanism of circumventing the host interferon antiviral response. Overall, most substitutions occur on the protein surfaces and may be modulating their antigenic properties and interactions with other macromolecules. Our results imply that the striking difference in the pervasiveness of SARS-CoV-2 and SARS-CoV among humans seems to significantly derive from molecular features that modulate the efficiency of viral particles in entering the host cells and blocking the host immune response.
MeSH term(s)	Animals ; Humans ; Molecular Dynamics Simulation ; Protein Domains ; Proteomics ; SARS Virus/chemistry ; SARS Virus/metabolism ; SARS Virus/pathogenicity ; SARS-CoV-2/chemistry ; SARS-CoV-2/metabolism ; SARS-CoV-2/pathogenicity ; Species Specificity ; Viral Proteins/chemistry ; Viral Proteins/metabolism
Chemical Substances	Viral Proteins
Keywords	covid19
Language	English
Publishing date	2020-09-17
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	998579-7
ISSN	1537-1719 ; 0737-4038
ISSN (online)	1537-1719
ISSN	0737-4038
DOI	10.1093/molbev/msaa231
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Article ; Online: Structural and functional characterization of NEMO cleavage by SARS-CoV-2 3CLpro.

Hameedi, Mikhail A / T Prates, Erica / Garvin, Michael R / Mathews, Irimpan I / Amos, B Kirtley / Demerdash, Omar / Bechthold, Mark / Iyer, Mamta / Rahighi, Simin / Kneller, Daniel W / Kovalevsky, Andrey / Irle, Stephan / Vuong, Van-Quan / Mitchell, Julie C / Labbe, Audrey / Galanie, Stephanie / Wakatsuki, Soichi / Jacobson, Daniel

Nature communications

2022 Volume 13, Issue 1, Page(s) 5285

Abstract: In addition to its essential role in viral polyprotein processing, the SARS-CoV-2 3C-like protease (3CLpro) can cleave human immune signaling proteins, like NF-κB Essential Modulator (NEMO) and deregulate the host immune response. Here, in vitro assays ... ...

Abstract	In addition to its essential role in viral polyprotein processing, the SARS-CoV-2 3C-like protease (3CLpro) can cleave human immune signaling proteins, like NF-κB Essential Modulator (NEMO) and deregulate the host immune response. Here, in vitro assays show that SARS-CoV-2 3CLpro cleaves NEMO with fine-tuned efficiency. Analysis of the 2.50 Å resolution crystal structure of 3CLpro C145S bound to NEMO
MeSH term(s)	Antiviral Agents/chemistry ; COVID-19 ; Cysteine Endopeptidases/metabolism ; Humans ; Peptide Hydrolases ; Proteins ; SARS-CoV-2
Chemical Substances	Antiviral Agents ; Proteins ; Peptide Hydrolases (EC 3.4.-) ; Cysteine Endopeptidases (EC 3.4.22.-)
Language	English
Publishing date	2022-09-08
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-022-32922-9
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Article: Exploring the role of plant lysin motif receptor-like kinases in regulating plant-microbe interactions in the bioenergy crop

Cope, Kevin R / Prates, Erica T / Miller, John I / Demerdash, Omar N A / Shah, Manesh / Kainer, David / Cliff, Ashley / Sullivan, Kyle A / Cashman, Mikaela / Lane, Matthew / Matthiadis, Anna / Labbé, Jesse / Tschaplinski, Timothy J / Jacobson, Daniel A / Kalluri, Udaya C

Computational and structural biotechnology journal

2022 Volume 21, Page(s) 1122–1139

Abstract: For plants, distinguishing between mutualistic and pathogenic microbes is a matter of survival. All microbes contain microbe-associated molecular patterns (MAMPs) that are perceived by plant pattern recognition receptors (PRRs). Lysin motif receptor-like ...

Abstract	For plants, distinguishing between mutualistic and pathogenic microbes is a matter of survival. All microbes contain microbe-associated molecular patterns (MAMPs) that are perceived by plant pattern recognition receptors (PRRs). Lysin motif receptor-like kinases (LysM-RLKs) are PRRs attuned for binding and triggering a response to specific MAMPs, including chitin oligomers (COs) in fungi, lipo-chitooligosaccharides (LCOs), which are produced by mycorrhizal fungi and nitrogen-fixing rhizobial bacteria, and peptidoglycan in bacteria. The identification and characterization of LysM-RLKs in candidate bioenergy crops including
Language	English
Publishing date	2022-12-31
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	2694435-2
ISSN	2001-0370
ISSN	2001-0370
DOI	10.1016/j.csbj.2022.12.052
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Article ; Online: Antiviral Strategies Against SARS-CoV-2: A Systems Biology Approach.

Prates, Erica T / Garvin, Michael R / Jones, Piet / Miller, J Izaak / Sullivan, Kyle A / Cliff, Ashley / Gazolla, Joao Gabriel Felipe Machado / Shah, Manesh B / Walker, Angelica M / Lane, Matthew / Rentsch, Christopher T / Justice, Amy / Pavicic, Mirko / Romero, Jonathon / Jacobson, Daniel

Methods in molecular biology (Clifton, N.J.)

2022 Volume 2452, Page(s) 317–351

Abstract: The unprecedented scientific achievements in combating the COVID-19 pandemic reflect a global response informed by unprecedented access to data. We now have the ability to rapidly generate a diversity of information on an emerging pathogen and, by using ... ...

Abstract	The unprecedented scientific achievements in combating the COVID-19 pandemic reflect a global response informed by unprecedented access to data. We now have the ability to rapidly generate a diversity of information on an emerging pathogen and, by using high-performance computing and a systems biology approach, we can mine this wealth of information to understand the complexities of viral pathogenesis and contagion like never before. These efforts will aid in the development of vaccines, antiviral medications, and inform policymakers and clinicians. Here we detail computational protocols developed as SARS-CoV-2 began to spread across the globe. They include pathogen detection, comparative structural proteomics, evolutionary adaptation analysis via network and artificial intelligence methodologies, and multiomic integration. These protocols constitute a core framework on which to build a systems-level infrastructure that can be quickly brought to bear on future pathogens before they evolve into pandemic proportions.
MeSH term(s)	Antiviral Agents/pharmacology ; Antiviral Agents/therapeutic use ; Artificial Intelligence ; COVID-19/drug therapy ; Humans ; Pandemics/prevention & control ; SARS-CoV-2 ; Systems Biology
Chemical Substances	Antiviral Agents
Language	English
Publishing date	2022-05-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-2111-0_19
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