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Article: Dipeptidyl Peptidase-4 at the Interface Between Inflammation and Metabolism.

Trzaskalski, Natasha A / Fadzeyeva, Evgenia / Mulvihill, Erin E

Clinical medicine insights. Endocrinology and diabetes

2020 Volume 13, Page(s) 1179551420912972

Abstract: Dipeptidyl peptidase-4 (DPP4) is a serine protease that rapidly inactivates the incretin peptides, glucagon-like peptide-1, and glucose-dependent insulinotropic polypeptide to modulate postprandial islet hormone secretion and glycemia. Dipeptidyl ... ...

Abstract	Dipeptidyl peptidase-4 (DPP4) is a serine protease that rapidly inactivates the incretin peptides, glucagon-like peptide-1, and glucose-dependent insulinotropic polypeptide to modulate postprandial islet hormone secretion and glycemia. Dipeptidyl peptidase-4 also has nonglycemic effects by controlling the progression of inflammation, which may be mediated more through direct protein-protein interactions than catalytic activity in the context of nonalcoholic fatty liver disease (NAFLD), obesity, and type 2 diabetes (T2D). Failure to resolve inflammation resulting in chronic subclinical activation of the immune system may influence the development of metabolic dysregulation. Thus, through both its cleavage and regulation of the bioactivity of peptide hormones and its influence on inflammation, DPP4 exhibits a diverse array of effects that can influence the progression of metabolic disease. Here, we highlight our current understanding of the complex biology of DPP4 at the intersection of inflammation, obesity, T2D, and NAFLD. We compare and review new mechanisms identified in basic laboratory and clinical studies, which may have therapeutic application and relevance to the pathogenesis of obesity and T2D.
Language	English
Publishing date	2020-03-20
Publishing country	United States
Document type	Journal Article ; Review
ISSN	1179-5514
ISSN	1179-5514
DOI	10.1177/1179551420912972
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Article ; Online: Thermoneutral housing does not accelerate metabolic dysfunction-associated fatty liver disease in male or female C57Bl/6J mice fed a Western diet.

Nunes, Julia R C / Smith, Tyler K T / Ghorbani, Peyman / O'Dwyer, Conor / Trzaskalski, Natasha A / Dergham, Habiba / Pember, Ciara / Kilgour, Marisa K / Mulvihill, Erin E / Fullerton, Morgan D

American journal of physiology. Endocrinology and metabolism

2023 Volume 325, Issue 1, Page(s) E10–E20

Abstract: Metabolic dysfunction-associated fatty liver disease (MAFLD) represents a growing cause of mortality and morbidity and encompasses a spectrum of liver pathologies. Although dozens of preclinical models have been developed to recapitulate stages of MAFLD, ...

Abstract	Metabolic dysfunction-associated fatty liver disease (MAFLD) represents a growing cause of mortality and morbidity and encompasses a spectrum of liver pathologies. Although dozens of preclinical models have been developed to recapitulate stages of MAFLD, few achieve fibrosis using an experimental design that mimics human pathogenesis. We sought to clarify whether the combination of thermoneutral (T
MeSH term(s)	Humans ; Female ; Male ; Animals ; Mice ; Housing ; Mice, Inbred C57BL ; Diet, Western/adverse effects ; Non-alcoholic Fatty Liver Disease/metabolism ; Liver/metabolism ; Fibrosis
Language	English
Publishing date	2023-05-17
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	603841-4
ISSN	1522-1555 ; 0193-1849
ISSN (online)	1522-1555
ISSN	0193-1849
DOI	10.1152/ajpendo.00124.2023
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Article: Adaptation to short-term extreme fat consumption alters intestinal lipid handling in male and female mice

Morrow, Nadya M. / Locatelli, Cassandra A.A. / Trzaskalski, Natasha A. / Klein, Chelsea T. / Hanson, Antonio A. / Alhadi, Hadeel / Tripathi, Ishika / Clément, Andrew C. / Imran, Sara / Lorenzen-Schmidt, Ilka / Mulvihill, Erin E.

Biochimica et biophysica acta. 2022 Nov., v. 1867, no. 11

2022

Abstract: The small intestine is a highly adaptable organ serving as both a barrier to the external environment and a conduit for nutrient absorption. Enterocytes package dietary triglycerides (TG) into chylomicrons for transport into circulation; the remaining ... ...

Abstract	The small intestine is a highly adaptable organ serving as both a barrier to the external environment and a conduit for nutrient absorption. Enterocytes package dietary triglycerides (TG) into chylomicrons for transport into circulation; the remaining TGs are stored in cytosolic lipid droplets (CLDs). The current study aimed to characterize the impact of diet composition on intestinal lipid handling in male and female wild-type mice. Mice were continued on their grain-based diet (GBD) and switched to either a high-fat, high cholesterol Western-style diet (WD) or a ketogenic diet (KD) for 3 or 5 weeks. KD-fed mice displayed significantly higher plasma TG levels in response to an olive oil gavage than WD- and GBD-fed mice; TG levels were ~2-fold higher in male KD-fed mice than female KD-fed mice. Poloxamer-407 experiments revealed enhanced intestinal-TG secretion rates in male mice fed a KD upon olive oil gavage, whereas secretion rates were unchanged in female mice. Surprisingly, jejunal CLD size and TG mass after oil gavage were similar among the groups. At fasting, TG mass was significantly higher in the jejunum of male KD-fed mice and the duodenum of female KD-fed mice, providing increased substrate for chylomicron formation. In addition to greater fasting intestinal TG stores, KD-fed male mice displayed longer small intestinal lengths, while female mice displayed markedly longer jejunal villi lengths. After 5 weeks of diet, 12 h fasting-2 h refeeding experiments revealed jejunal TG levels were similar between diet groups in male mice; however, in female mice, jejunal TG mass was significantly higher in KD-fed mice compared to GBD- and WD-fed mice. These experiments reveal that KD feeding promotes distinct morphological and functional changes to the murine small intestine compared to the WD diet. Moreover, changes to intestinal lipid handling in response to carbohydrate and protein restriction manifest differently in male and female mice.
Keywords	Western diets ; carbohydrates ; cholesterol ; chylomicrons ; duodenum ; enterocytes ; fasting ; fat intake ; females ; jejunum ; ketogenic diet ; males ; nutrient uptake ; olive oil ; secretion
Language	English
Dates of publication	2022-11
Publishing place	Elsevier B.V.
Document type	Article
ISSN	1388-1981
DOI	10.1016/j.bbalip.2022.159208
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Pancreas-derived DPP4 is not essential for glucose homeostasis under metabolic stress.

Fadzeyeva, Evgenia / Locatelli, Cassandra A A / Trzaskalski, Natasha A / Nguyen, My-Anh / Capozzi, Megan E / Vulesevic, Branka / Morrow, Nadya M / Ghorbani, Peyman / Hanson, Antonio A / Lorenzen-Schmidt, Ilka / Doyle, Mary-Anne / Seymour, Richard / Varin, Elodie M / Fullerton, Morgan D / Campbell, Jonathan E / Mulvihill, Erin E

iScience

2023 Volume 26, Issue 5, Page(s) 106748

Abstract: Mice systemically lacking dipeptidyl peptidase-4 (DPP4) have improved islet health, glucoregulation, and reduced obesity with high-fat diet (HFD) feeding compared to wild-type mice. Some, but not all, of this improvement can be linked to the loss of DPP4 ...

Abstract	Mice systemically lacking dipeptidyl peptidase-4 (DPP4) have improved islet health, glucoregulation, and reduced obesity with high-fat diet (HFD) feeding compared to wild-type mice. Some, but not all, of this improvement can be linked to the loss of DPP4 in endothelial cells (ECs), pointing to the contribution of non-EC types. The importance of intra-islet signaling mediated by α to β cell communication is becoming increasingly clear; thus, our objective was to determine if β cell DPP4 regulates insulin secretion and glucose tolerance in HFD-fed mice by regulating the local concentrations of insulinotropic peptides. Using β cell double incretin receptor knockout mice, β cell- and pancreas-specific
Language	English
Publishing date	2023-04-26
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2023.106748
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Article ; Online: Adaptation to short-term extreme fat consumption alters intestinal lipid handling in male and female mice.

Morrow, Nadya M / Locatelli, Cassandra A A / Trzaskalski, Natasha A / Klein, Chelsea T / Hanson, Antonio A / Alhadi, Hadeel / Tripathi, Ishika / Clément, Andrew C / Imran, Sara / Lorenzen-Schmidt, Ilka / Mulvihill, Erin E

Biochimica et biophysica acta. Molecular and cell biology of lipids

2022 Volume 1867, Issue 11, Page(s) 159208

Abstract	The small intestine is a highly adaptable organ serving as both a barrier to the external environment and a conduit for nutrient absorption. Enterocytes package dietary triglycerides (TG) into chylomicrons for transport into circulation; the remaining TGs are stored in cytosolic lipid droplets (CLDs). The current study aimed to characterize the impact of diet composition on intestinal lipid handling in male and female wild-type mice. Mice were continued on their grain-based diet (GBD) and switched to either a high-fat, high cholesterol Western-style diet (WD) or a ketogenic diet (KD) for 3 or 5 weeks. KD-fed mice displayed significantly higher plasma TG levels in response to an olive oil gavage than WD- and GBD-fed mice; TG levels were ~2-fold higher in male KD-fed mice than female KD-fed mice. Poloxamer-407 experiments revealed enhanced intestinal-TG secretion rates in male mice fed a KD upon olive oil gavage, whereas secretion rates were unchanged in female mice. Surprisingly, jejunal CLD size and TG mass after oil gavage were similar among the groups. At fasting, TG mass was significantly higher in the jejunum of male KD-fed mice and the duodenum of female KD-fed mice, providing increased substrate for chylomicron formation. In addition to greater fasting intestinal TG stores, KD-fed male mice displayed longer small intestinal lengths, while female mice displayed markedly longer jejunal villi lengths. After 5 weeks of diet, 12 h fasting-2 h refeeding experiments revealed jejunal TG levels were similar between diet groups in male mice; however, in female mice, jejunal TG mass was significantly higher in KD-fed mice compared to GBD- and WD-fed mice. These experiments reveal that KD feeding promotes distinct morphological and functional changes to the murine small intestine compared to the WD diet. Moreover, changes to intestinal lipid handling in response to carbohydrate and protein restriction manifest differently in male and female mice.
MeSH term(s)	Animals ; Chylomicrons/metabolism ; Diet, High-Fat ; Enterocytes/metabolism ; Female ; Male ; Mice ; Olive Oil/metabolism ; Triglycerides/metabolism
Chemical Substances	Chylomicrons ; Olive Oil ; Triglycerides
Language	English
Publishing date	2022-08-01
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	60-7
ISSN	1879-2618 ; 1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2650 ; 0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
ISSN (online)	1879-2618 ; 1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2650
ISSN	0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
DOI	10.1016/j.bbalip.2022.159208
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Article ; Online: Quantification of murine myocardial infarct size using 2-D and 4-D high-frequency ultrasound.

Dann, Melissa M / Clark, Sydney Q / Trzaskalski, Natasha A / Earl, Conner C / Schepers, Luke E / Pulente, Serena M / Lennord, Ebonee N / Annamalai, Karthik / Gruber, Joseph M / Cox, Abigail D / Lorenzen-Schmidt, Ilka / Seymour, Richard / Kim, Kyoung-Han / Goergen, Craig J / Mulvihill, Erin E

American journal of physiology. Heart and circulatory physiology

2022 Volume 322, Issue 3, Page(s) H359–H372

Abstract: Ischemic heart disease is the leading cause of death in the United States, Canada, and worldwide. Severe disease is characterized by coronary artery occlusion, loss of blood flow to the myocardium, and necrosis of tissue, with subsequent remodeling of ... ...

Abstract	Ischemic heart disease is the leading cause of death in the United States, Canada, and worldwide. Severe disease is characterized by coronary artery occlusion, loss of blood flow to the myocardium, and necrosis of tissue, with subsequent remodeling of the heart wall, including fibrotic scarring. The current study aims to demonstrate the efficacy of quantitating infarct size via two-dimensional (2-D) echocardiographic akinetic length and four-dimensional (4-D) echocardiographic infarct volume and surface area as in vivo analysis techniques. We further describe and evaluate a new surface area strain analysis technique for estimating myocardial infarction (MI) size after ischemic injury. Experimental MI was induced in mice via left coronary artery ligation. Ejection fraction and infarct size were measured through 2-D and 4-D echocardiography. Infarct size established via histology was compared with ultrasound-based metrics via linear regression analysis. Two-dimensional echocardiographic akinetic length (
MeSH term(s)	Algorithms ; Animals ; Cardiac Output ; Female ; Heart Ventricles/diagnostic imaging ; Heart Ventricles/pathology ; Heart Ventricles/physiopathology ; Imaging, Three-Dimensional/methods ; Imaging, Three-Dimensional/standards ; Male ; Mice ; Myocardial Infarction/diagnostic imaging ; Myocardial Infarction/pathology ; Myocardial Infarction/physiopathology ; Sensitivity and Specificity ; Ultrasonography/methods ; Ultrasonography/standards
Language	English
Publishing date	2022-01-07
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	603838-4
ISSN	1522-1539 ; 0363-6135
ISSN (online)	1522-1539
ISSN	0363-6135
DOI	10.1152/ajpheart.00476.2021
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Article ; Online: Nobiletin Prevents High-Fat Diet-Induced Dysregulation of Intestinal Lipid Metabolism and Attenuates Postprandial Lipemia.

Morrow, Nadya M / Trzaskalski, Natasha A / Hanson, Antonio A / Fadzeyeva, Evgenia / Telford, Dawn E / Chhoker, Sanjiv S / Sutherland, Brian G / Edwards, Jane Y / Huff, Murray W / Mulvihill, Erin E

Arteriosclerosis, thrombosis, and vascular biology

2021 Volume 42, Issue 2, Page(s) 127–144

Abstract: Objective: Nobiletin is a dietary flavonoid that improves insulin resistance and atherosclerosis in mice with metabolic dysfunction. Dysregulation of intestinal lipoprotein metabolism contributes to atherogenesis. The objective of the study was to ... ...

Abstract	Objective: Nobiletin is a dietary flavonoid that improves insulin resistance and atherosclerosis in mice with metabolic dysfunction. Dysregulation of intestinal lipoprotein metabolism contributes to atherogenesis. The objective of the study was to determine if nobiletin targets the intestine to improve metabolic dysregulation in both male and female mice. Approach and Results: Triglyceride-rich lipoprotein (TRL) secretion, intracellular triglyceride kinetics, and intestinal morphology were determined in male and female LDL (low-density lipoprotein) receptor knockout ( Conclusions: Nobiletin opposed the effects of the HFHC diet by normalizing intestinal de novo lipogenesis through improved insulin sensitivity. Nobiletin prevents postprandial lipemia because the enhanced TRL clearance more than compensates for increased TRL secretion.
MeSH term(s)	Animals ; Diet, High-Fat/adverse effects ; Female ; Flavones/pharmacology ; Flavones/therapeutic use ; Hyperlipidemias/blood ; Hyperlipidemias/metabolism ; Hyperlipidemias/prevention & control ; Intestines/drug effects ; Intestines/metabolism ; Lipid Metabolism/drug effects ; Male ; Mice, Inbred C57BL ; Postprandial Period ; Protective Agents/pharmacology ; Protective Agents/therapeutic use ; Triglycerides/blood ; Triglycerides/metabolism ; Mice
Chemical Substances	Flavones ; Protective Agents ; Triglycerides ; nobiletin (D65ILJ7WLY)
Language	English
Publishing date	2021-12-16
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1221433-4
ISSN	1524-4636 ; 1079-5642
ISSN (online)	1524-4636
ISSN	1079-5642
DOI	10.1161/ATVBAHA.121.316896
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Article ; Online: Myeloid deletion and therapeutic activation of AMPK do not alter atherosclerosis in male or female mice.

LeBlond, Nicholas D / Ghorbani, Peyman / O'Dwyer, Conor / Ambursley, Nia / Nunes, Julia R C / Smith, Tyler K T / Trzaskalski, Natasha A / Mulvihill, Erin E / Viollet, Benoit / Foretz, Marc / Fullerton, Morgan D

Journal of lipid research

2020 Volume 61, Issue 12, Page(s) 1697–1706

Abstract: The dysregulation of myeloid-derived cell metabolism can drive atherosclerosis. AMP-activated protein kinase (AMPK) controls various aspects of macrophage dynamics and lipid homeostasis, which are important during atherogenesis. Using LysM-Cre to drive ... ...

Abstract	The dysregulation of myeloid-derived cell metabolism can drive atherosclerosis. AMP-activated protein kinase (AMPK) controls various aspects of macrophage dynamics and lipid homeostasis, which are important during atherogenesis. Using LysM-Cre to drive the deletion of both the α1 and α2 catalytic subunits (MacKO), we aimed to clarify the role of myeloid-specific AMPK signaling in male and female mice made acutely atherosclerotic by injection of AAV vector encoding a gain-of-function mutant PCSK9 (PCSK9-AAV) and WD feeding. After 6 weeks of WD feeding, mice received a daily injection of either the AMPK activator A-769662 or a vehicle control for an additional 6 weeks. Following this (12 weeks total), we assessed myeloid cell populations and differences between genotype or sex were not observed. Similarly, aortic sinus plaque size, lipid staining, and necrotic area did not differ in male and female MacKO mice compared with their littermate floxed controls. Moreover, therapeutic intervention with A-769662 showed no treatment effect. There were also no observable differences in the amount of circulating total cholesterol or triglyceride, and only minor differences in the levels of inflammatory cytokines between groups. Finally, CD68+ area and markers of autophagy showed no effect of either lacking AMPK signaling or AMPK activation. Our data suggest that while defined roles for each catalytic AMPK subunit have been identified, complete deletion of myeloid AMPK signaling does not significantly impact atherosclerosis. Additionally, these findings suggest that intervention with the first-generation AMPK activator A-769662 is not able to stem the progression of atherosclerosis.
MeSH term(s)	AMP-Activated Protein Kinases/metabolism ; Animals ; Atherosclerosis/immunology ; Atherosclerosis/pathology ; Atherosclerosis/therapy ; Enzyme Activation ; Female ; Macrophages/metabolism ; Male ; Mice ; Signal Transduction
Chemical Substances	AMP-Activated Protein Kinases (EC 2.7.11.31)
Language	English
Publishing date	2020-09-25
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80154-9
ISSN	1539-7262 ; 0022-2275
ISSN (online)	1539-7262
ISSN	0022-2275
DOI	10.1194/jlr.RA120001040
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Article ; Online: Hepatocyte-derived DPP4 regulates portal GLP-1 bioactivity, modulates glucose production, and when absent influences NAFLD progression.

Trzaskalski, Natasha A / Vulesevic, Branka / Nguyen, My-Anh / Jeraj, Natasha / Fadzeyeva, Evgenia / Morrow, Nadya M / Locatelli, Cassandra Aa / Travis, Nicole / Hanson, Antonio A / Nunes, Julia Rc / O'Dwyer, Conor / van der Veen, Jelske N / Lorenzen-Schmidt, Ilka / Seymour, Rick / Pulente, Serena M / Clément, Andrew C / Crawley, Angela M / Jacobs, René L / Doyle, Mary-Anne /

Cooper, Curtis L / Kim, Kyoung-Han / Fullerton, Morgan D / Mulvihill, Erin E

JCI insight

2023 Volume 8, Issue 2

Abstract: Elevated circulating dipeptidyl peptidase-4 (DPP4) is a biomarker for liver disease, but its involvement in gluconeogenesis and metabolic associated fatty liver disease progression remains unclear. Here, we identified that DPP4 in hepatocytes but not TEK ...

Abstract	Elevated circulating dipeptidyl peptidase-4 (DPP4) is a biomarker for liver disease, but its involvement in gluconeogenesis and metabolic associated fatty liver disease progression remains unclear. Here, we identified that DPP4 in hepatocytes but not TEK receptor tyrosine kinase-positive endothelial cells regulates the local bioactivity of incretin hormones and gluconeogenesis. However, the complete absence of DPP4 (Dpp4-/-) in aged mice with metabolic syndrome accelerates liver fibrosis without altering dyslipidemia and steatosis. Analysis of transcripts from the livers of Dpp4-/- mice displayed enrichment for inflammasome, p53, and senescence programs compared with littermate controls. High-fat, high-cholesterol feeding decreased Dpp4 expression in F4/80+ cells, with only minor changes in immune signaling. Moreover, in a lean mouse model of severe nonalcoholic fatty liver disease, phosphatidylethanolamine N-methyltransferase mice, we observed a 4-fold increase in circulating DPP4, in contrast with previous findings connecting DPP4 release and obesity. Last, we evaluated DPP4 levels in patients with hepatitis C infection with dysglycemia (Homeostatic Model Assessment of Insulin Resistance > 2) who underwent direct antiviral treatment (with/without ribavirin). DPP4 protein levels decreased with viral clearance; DPP4 activity levels were reduced at long-term follow-up in ribavirin-treated patients; but metabolic factors did not improve. These data suggest elevations in DPP4 during hepatitis C infection are not primarily regulated by metabolic disturbances.
MeSH term(s)	Mice ; Animals ; Non-alcoholic Fatty Liver Disease/metabolism ; Glucose/metabolism ; Glucagon-Like Peptide 1/metabolism ; Dipeptidyl Peptidase 4/metabolism ; Endothelial Cells/metabolism ; Ribavirin/metabolism ; Hepatocytes/metabolism ; Hepatitis C
Chemical Substances	Glucose (IY9XDZ35W2) ; Glucagon-Like Peptide 1 (89750-14-1) ; Dipeptidyl Peptidase 4 (EC 3.4.14.5) ; Ribavirin (49717AWG6K)
Language	English
Publishing date	2023-01-24
Publishing country	United States
Document type	Journal Article
ISSN	2379-3708
ISSN (online)	2379-3708
DOI	10.1172/jci.insight.154314
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