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Article ; Online: Long-Chain Acylcholines Link Butyrylcholinesterase to Regulation of Non-neuronal Cholinergic Signaling.

Kinchen, Jason M / Mohney, Robert P / Pappan, Kirk L

2021 Volume 21, Issue 3, Page(s) 599–611

Abstract: Acylcholines are comprised of an acyl chain esterified to a choline moiety; acetylcholine is the best-characterized member of this class, functioning as a neurotransmitter in the central and peripheral nervous systems as well as an inhibitor of cytokine ... ...

Abstract	Acylcholines are comprised of an acyl chain esterified to a choline moiety; acetylcholine is the best-characterized member of this class, functioning as a neurotransmitter in the central and peripheral nervous systems as well as an inhibitor of cytokine production by macrophages and other innate immune cells. Acylcholines are metabolized by a class of cholinesterases, including acetylcholinesterase (a specific regulator of acetylcholine levels) and butyrylcholinesterase (BChE, an enigmatic enzyme whose function has not been resolved by genetic knockout models). BChE provides reserve capacity to hydrolyze acetylcholine, but its importance is arguable given acetylcholinesterase is the most catalytically efficient enzyme characterized to date. While known to be substrates of BChE in vitro, endogenous production of long-chain acylcholines is a recent discovery enabled by untargeted metabolomics. Compared to acetylcholine, long-chain acylcholines show greater stability in circulation with homeostatic levels-dictated by synthesis and clearance-suggested to impact cholinergic receptor sensitivity of acetylcholine with varying levels of antagonism. Acylcholines then provide a link between BChE and non-neuronal acetylcholine signaling, filling a gap in understanding around how imbalances between acylcholines and BChE could modulate inflammatory disease, such as the "cytokine storm" identified in severe COVID-19. Areas for further research, development, and clinical testing are outlined.
MeSH term(s)	Acetylcholinesterase/genetics ; Acetylcholinesterase/metabolism ; Butyrylcholinesterase/genetics ; Butyrylcholinesterase/metabolism ; COVID-19 ; Cholinergic Agents ; Humans ; SARS-CoV-2
Chemical Substances	Cholinergic Agents ; Acetylcholinesterase (EC 3.1.1.7) ; Butyrylcholinesterase (EC 3.1.1.8)
Language	English
Publishing date	2021-11-10
Publishing country	United States
Document type	Journal Article
ZDB-ID	2078618-9
ISSN	1535-3907 ; 1535-3893
ISSN (online)	1535-3907
ISSN	1535-3893
DOI	10.1021/acs.jproteome.1c00538
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Article: Long-Chain Acylcholines Link Butyrylcholinesterase to Regulation of Non-neuronal Cholinergic Signaling

Kinchen, Jason M. / Mohney, Robert P. / Pappan, Kirk L.

Journal of proteome research. 2021 Nov. 11, v. 21, no. 3

2021

Abstract	Acylcholines are comprised of an acyl chain esterified to a choline moiety; acetylcholine is the best-characterized member of this class, functioning as a neurotransmitter in the central and peripheral nervous systems as well as an inhibitor of cytokine production by macrophages and other innate immune cells. Acylcholines are metabolized by a class of cholinesterases, including acetylcholinesterase (a specific regulator of acetylcholine levels) and butyrylcholinesterase (BChE, an enigmatic enzyme whose function has not been resolved by genetic knockout models). BChE provides reserve capacity to hydrolyze acetylcholine, but its importance is arguable given acetylcholinesterase is the most catalytically efficient enzyme characterized to date. While known to be substrates of BChE in vitro, endogenous production of long-chain acylcholines is a recent discovery enabled by untargeted metabolomics. Compared to acetylcholine, long-chain acylcholines show greater stability in circulation with homeostatic levels–dictated by synthesis and clearance–suggested to impact cholinergic receptor sensitivity of acetylcholine with varying levels of antagonism. Acylcholines then provide a link between BChE and non-neuronal acetylcholine signaling, filling a gap in understanding around how imbalances between acylcholines and BChE could modulate inflammatory disease, such as the “cytokine storm” identified in severe COVID-19. Areas for further research, development, and clinical testing are outlined.
Keywords	COVID-19 infection ; acetylcholine ; acetylcholinesterase ; antagonism ; choline ; cholinesterase ; cytokines ; macrophages ; metabolomics ; moieties ; neurotransmitters ; proteome ; research
Language	English
Dates of publication	2021-1111
Size	p. 599-611.
Publishing place	American Chemical Society
Document type	Article
ZDB-ID	2078618-9
ISSN	1535-3907 ; 1535-3893
ISSN (online)	1535-3907
ISSN	1535-3893
DOI	10.1021/acs.jproteome.1c00538
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Article ; Online: A model to die for: signaling to apoptotic cell removal in worm, fly and mouse.

Kinchen, Jason M

Apoptosis : an international journal on programmed cell death

2010 Volume 15, Issue 9, Page(s) 998–1006

Abstract: Programmed cell death is used during developmental morphogenesis to eliminate superfluous cells or cells with inappropriate developmental potential (e.g., self-reactive immune cells, tumorigenic cells). Recent work in genetic models has led to a number ... ...

Abstract	Programmed cell death is used during developmental morphogenesis to eliminate superfluous cells or cells with inappropriate developmental potential (e.g., self-reactive immune cells, tumorigenic cells). Recent work in genetic models has led to a number of key observations, revealing signal transduction pathways and identifying new roles for genes previously studied in corpse removal (e.g., removal of broken synapses in the nervous system). Further, studies using mouse models have suggested a role for removal of apoptotic cells in the establishment or maintenance of immune tolerance. In this review, we survey current knowledge of phagocytic pathways derived from studies in the nematode (Caenorhabditis elegans), the fly (Drosophila melanogaster), and mouse (Mus musculus) model systems.
MeSH term(s)	Animals ; Apoptosis ; Caenorhabditis elegans/cytology ; Caenorhabditis elegans/immunology ; Caenorhabditis elegans/metabolism ; Drosophila melanogaster/cytology ; Drosophila melanogaster/immunology ; Drosophila melanogaster/metabolism ; Humans ; Mice ; Models, Animal ; Phagocytosis ; Signal Transduction
Language	English
Publishing date	2010-09
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1452360-7
ISSN	1573-675X ; 1360-8185
ISSN (online)	1573-675X
ISSN	1360-8185
DOI	10.1007/s10495-010-0509-5
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Article ; Online: A procession of metabolic alterations accompanying muscle senescence in Manduca sexta.

Wone, Bernard W M / Kinchen, Jason M / Kaup, Elana R / Wone, Beate

Scientific reports

2018 Volume 8, Issue 1, Page(s) 1006

Abstract: ... the progression of muscle aging, as well as to evaluate the utility of the M. sexta system for molecular ...

Abstract	Biological aging profoundly impairs muscle function, performance, and metabolism. Because the progression of metabolic alterations associated with aging muscle has not been chronicled, we tracked the metabolic profiles of flight muscle from middle to advanced age in Manduca sexta to identify key molecules during the progression of muscle aging, as well as to evaluate the utility of the M. sexta system for molecular dissection of muscle aging. We identified a number of differences between Diel Time, Sexes, and Muscle Ages, including changes in metabolites related to energetics, extracellular matrix turnover, and glutathione metabolism. Increased abundances of glycolytic metabolites suggest a shift toward increased glycolysis with advancing age, whereas decreased abundances in lysolipids and acylcarnitines reflect decreasing beta-oxidation. We also observed a shift towards decreased polyamine metabolism with age, which might result in an age-related decline in lipid metabolism possibly due to regulation of energy metabolism by polyamines. Collectively, our findings demonstrate the feasibility of our system and approach and provide a deeper understanding of lepidopteran aging. More importantly, the results identify the key altered metabolic pathways that collectively contribute to the muscle aging phenotype and thereby improve our understanding of muscle senescence.
MeSH term(s)	Aging/metabolism ; Animals ; Female ; Flight, Animal/physiology ; Glutathione/metabolism ; Glycolysis/physiology ; Lipid Metabolism/physiology ; Male ; Manduca/growth & development ; Manduca/metabolism ; Metabolome ; Muscle Development/physiology ; Muscles/metabolism ; Oxidative Phosphorylation ; Polyamines/metabolism
Chemical Substances	Polyamines ; Glutathione (GAN16C9B8O)
Language	English
Publishing date	2018-01-17
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-018-19630-5
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Article ; Online: Author Correction: Metabolomics analysis of follicular fluid coupled with oocyte aspiration reveals importance of glucocorticoids in primate periovulatory follicle competency.

Ravisankar, Sweta / Hanna, Carol B / Brooks, Kelsey E / Murphy, Melinda J / Redmayne, Nash / Ryu, Junghyun / Kinchen, Jason M / Chavez, Shawn L / Hennebold, Jon D

Scientific reports

2021 Volume 11, Issue 1, Page(s) 16968

Language	English
Publishing date	2021-08-16
Publishing country	England
Document type	Published Erratum
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-021-96473-7
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Article: A model to die for: signaling to apoptotic cell removal in worm, fly and mouse

Kinchen, Jason M

Apoptosis. 2010 Sept., v. 15, no. 9

2010

Abstract	Programmed cell death is used during developmental morphogenesis to eliminate superfluous cells or cells with inappropriate developmental potential (e.g., self-reactive immune cells, tumorigenic cells). Recent work in genetic models has led to a number of key observations, revealing signal transduction pathways and identifying new roles for genes previously studied in corpse removal (e.g., removal of broken synapses in the nervous system). Further, studies using mouse models have suggested a role for removal of apoptotic cells in the establishment or maintenance of immune tolerance. In this review, we survey current knowledge of phagocytic pathways derived from studies in the nematode (Caenorhabditis elegans), the fly (Drosophila melanogaster), and mouse (Mus musculus) model systems.
Keywords	apoptosis ; phagocytosis
Language	English
Dates of publication	2010-09
Size	p. 998-1006.
Publisher	Springer US
Publishing place	Boston
Document type	Article
ZDB-ID	1452360-7
ISSN	1360-8185
ISSN	1360-8185
DOI	10.1007/s10495-010-0509-5
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Article: Metabolomic Predictors of Non-alcoholic Steatohepatitis and Advanced Fibrosis in Children.

Kordy, Kattayoun / Li, Fan / Lee, David J / Kinchen, Jason M / Jew, Michael H / La Rocque, Maria Eduarda / Zabih, Sara / Saavedra, Monica / Woodward, Cora / Cunningham, Nicole J / Tobin, Nicole H / Aldrovandi, Grace M

Frontiers in microbiology

2021 Volume 12, Page(s) 713234

Abstract: Non-alcoholic fatty liver disease (NAFLD) is the leading cause of chronic liver disease in western countries both in children and adults. Metabolic dysregulation associated with gut microbial dysbiosis may influence disease progression from hepatic ... ...

Abstract	Non-alcoholic fatty liver disease (NAFLD) is the leading cause of chronic liver disease in western countries both in children and adults. Metabolic dysregulation associated with gut microbial dysbiosis may influence disease progression from hepatic steatosis to inflammation and subsequent fibrosis. Using a multi-omics approach, we profiled the oral and fecal microbiome and plasma metabolites from 241 predominantly Latino children with non-alcoholic steatohepatitis (NASH), non-alcoholic fatty liver (NAFL), and controls. Children with more severe liver pathology were dysbiotic and had increased gene content associated with lipopolysaccharide biosynthesis and lipid, amino acid and carbohydrate metabolism. These changes were driven by increases in Bacteroides and concomitant decreases of
Language	English
Publishing date	2021-08-12
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2587354-4
ISSN	1664-302X
ISSN	1664-302X
DOI	10.3389/fmicb.2021.713234
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Article ; Online: Metabolomics analysis of follicular fluid coupled with oocyte aspiration reveals importance of glucocorticoids in primate periovulatory follicle competency.

Ravisankar, Sweta / Hanna, Carol B / Brooks, Kelsey E / Murphy, Melinda J / Redmayne, Nash / Ryu, Junghyun / Kinchen, Jason M / Chavez, Shawn L / Hennebold, Jon D

Scientific reports

2021 Volume 11, Issue 1, Page(s) 6506

Abstract: Gonadotropin administration during infertility treatment stimulates the growth and development of multiple ovarian follicles, yielding heterogeneous oocytes with variable capacity for fertilization, cleavage, and blastocyst formation. To determine how ... ...

Abstract	Gonadotropin administration during infertility treatment stimulates the growth and development of multiple ovarian follicles, yielding heterogeneous oocytes with variable capacity for fertilization, cleavage, and blastocyst formation. To determine how the intrafollicular environment affects oocyte competency, 74 individual rhesus macaque follicles were aspirated and the corresponding oocytes classified as failed to cleave, cleaved but arrested prior to blastulation, or those that formed blastocysts following in vitro fertilization. Metabolomics analysis of the follicular fluid (FF) identified 60 unique metabolites that were significantly different between embryo classifications, of which a notable increase in the intrafollicular ratio of cortisol to cortisone was observed in the blastocyst group. Immunolocalization of the glucocorticoid receptor (GR, NR3C1) revealed translocation from the cytoplasm to nucleus with oocyte maturation in vitro and, correlation to intrafollicular expression of the 11-hydroxy steroid dehydrogenases that interconvert these glucocorticoids was detected upon an ovulatory stimulus in vivo. While NR3C1 knockdown in oocytes had no effect on their maturation or fertilization, expansion of the associated cumulus granulosa cells was inhibited. Our findings indicate an important role for NR3C1 in the regulation of follicular processes via paracrine signaling. Further studies are required to define the means through which the FF cortisol:cortisone ratio determines oocyte competency.
MeSH term(s)	Animals ; Blastocyst/cytology ; Female ; Fertilization in Vitro/methods ; Follicular Fluid/metabolism ; Glucocorticoids/metabolism ; In Vitro Oocyte Maturation Techniques/methods ; Macaca mulatta ; Male ; Metabolome ; Oocyte Retrieval/methods ; Oocytes/cytology ; Oocytes/metabolism ; Ovulation ; Receptors, Glucocorticoid/metabolism
Chemical Substances	Glucocorticoids ; Receptors, Glucocorticoid
Language	English
Publishing date	2021-03-22
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-021-85704-6
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Article ; Online: Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells.

Kinchen, Jason M / Ravichandran, Kodi S

Nature

2010 Volume 464, Issue 7289, Page(s) 778–782

Abstract: Engulfment of apoptotic cells occurs throughout life in multicellular organisms. Impaired apoptotic cell clearance (due to defective recognition, internalization or degradation) results in autoimmune disease. One fundamental challenge in understanding ... ...

Abstract	Engulfment of apoptotic cells occurs throughout life in multicellular organisms. Impaired apoptotic cell clearance (due to defective recognition, internalization or degradation) results in autoimmune disease. One fundamental challenge in understanding how defects in corpse removal translate into diseased states is the identification of critical components orchestrating the different stages of engulfment. Here we use genetic, cell biological and molecular studies in Caenorhabditis elegans and mammalian cells to identify SAND-1 and its partner CCZ-1 as new factors in corpse removal. In worms deficient in either sand-1 or ccz-1, apoptotic cells are internalized and the phagosomes recruit the small GTPase RAB-5 but fail to progress to the subsequent RAB-7(+) stage. The mammalian orthologues of SAND-1, namely Mon1a and Mon1b, were similarly required for phagosome maturation. Mechanistically, Mon1 interacts with GTP-bound Rab5, identifying Mon1 as a previously unrecognized Rab5 effector. Moreover, a Mon1-Ccz1 complex (but not either protein alone) could bind Rab7 and could also influence Rab7 activation, suggesting Mon1-Ccz1 as an important link in progression from the Rab5-positive stage to the Rab7-positive stage of phagosome maturation. Taken together, these data identify SAND-1 (Mon1) and CCZ-1 (Ccz1) as critical and evolutionarily conserved components regulating the processing of ingested apoptotic cell corpses.
MeSH term(s)	Animals ; Animals, Genetically Modified ; Apoptosis/genetics ; Caenorhabditis elegans/cytology ; Caenorhabditis elegans/genetics ; Caenorhabditis elegans Proteins/genetics ; Caenorhabditis elegans Proteins/metabolism ; Carrier Proteins/genetics ; Carrier Proteins/metabolism ; Cell Line ; Conserved Sequence/genetics ; Disorders of Sex Development ; Evolution, Molecular ; Gonads/cytology ; Gonads/metabolism ; Guanine Nucleotide Dissociation Inhibitors/metabolism ; Hydrogen-Ion Concentration ; Intracellular Signaling Peptides and Proteins ; Mice ; Multiprotein Complexes/chemistry ; Multiprotein Complexes/metabolism ; NIH 3T3 Cells ; Phagocytosis/genetics ; Phagosomes/genetics ; Phagosomes/metabolism ; Protein Binding ; Thymus Gland/cytology ; Two-Hybrid System Techniques ; Vesicular Transport Proteins/genetics ; Vesicular Transport Proteins/metabolism ; rab GTP-Binding Proteins/metabolism ; rab5 GTP-Binding Proteins/metabolism
Chemical Substances	CCZ-1 protein, C elegans ; Caenorhabditis elegans Proteins ; Carrier Proteins ; Guanine Nucleotide Dissociation Inhibitors ; Intracellular Signaling Peptides and Proteins ; Mon1a protein, mouse ; Mon1b protein, mouse ; Multiprotein Complexes ; SAND-1 protein, C elegans ; Vesicular Transport Proteins ; rab7 protein (152989-05-4) ; rab GTP-Binding Proteins (EC 3.6.5.2) ; rab5 GTP-Binding Proteins (EC 3.6.5.2)
Language	English
Publishing date	2010-03-21
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	120714-3
ISSN	1476-4687 ; 0028-0836
ISSN (online)	1476-4687
ISSN	0028-0836
DOI	10.1038/nature08853
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Article ; Online: Head and Neck Squamous Cell Carcinoma Metabolism Draws on Glutaminolysis, and Stemness Is Specifically Regulated by Glutaminolysis via Aldehyde Dehydrogenase.

Kamarajan, Pachiyappan / Rajendiran, Thekkelnaycke M / Kinchen, Jason / Bermúdez, Mercedes / Danciu, Theodora / Kapila, Yvonne L

Journal of proteome research

2017 Volume 16, Issue 3, Page(s) 1315–1326

Abstract: Cancer cells use alternate energetic pathways; however, cancer stem cell (CSC) metabolic energetic pathways are unknown. The purpose of this study was to define the metabolic characteristics of head and neck cancer at different points of its pathogenesis ...

Abstract	Cancer cells use alternate energetic pathways; however, cancer stem cell (CSC) metabolic energetic pathways are unknown. The purpose of this study was to define the metabolic characteristics of head and neck cancer at different points of its pathogenesis with a focus on its CSC compartment. UPLC-MS/MS-profiling and GC-MS-validation studies of human head and neck cancer tissue, saliva, and plasma were used in conjunction with in vitro and in vivo models to carry out this investigation. We identified metabolite biomarker panels that distinguish head and neck cancer from healthy controls, and confirmed involvement of glutamate and glutaminolysis. Glutaminase, which catalyzes glutamate formation from glutamine, and aldehyde dehydrogenase (ALDH), a stemness marker, were highly expressed in primary and metastatic head and neck cancer tissues, tumorspheres, and CSC versus controls. Exogenous glutamine induced stemness via glutaminase, whereas inhibiting glutaminase suppressed stemness in vitro and tumorigenesis in vivo. Head and neck CSC (CD44
MeSH term(s)	Adult ; Aged ; Aged, 80 and over ; Aldehyde Dehydrogenase/metabolism ; Carcinoma, Squamous Cell/metabolism ; Case-Control Studies ; Female ; Gas Chromatography-Mass Spectrometry ; Glutamic Acid ; Glutaminase ; Glutamine/metabolism ; Head and Neck Neoplasms/metabolism ; Humans ; Male ; Middle Aged ; Neoplastic Stem Cells/metabolism ; Neoplastic Stem Cells/pathology ; Tandem Mass Spectrometry
Chemical Substances	Glutamine (0RH81L854J) ; Glutamic Acid (3KX376GY7L) ; Aldehyde Dehydrogenase (EC 1.2.1.3) ; Glutaminase (EC 3.5.1.2)
Language	English
Publishing date	2017-03-03
Publishing country	United States
Document type	Journal Article
ZDB-ID	2078618-9
ISSN	1535-3907 ; 1535-3893
ISSN (online)	1535-3907
ISSN	1535-3893
DOI	10.1021/acs.jproteome.6b00936
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