Current Research Projects

1.) Understanding the role of lyosomal activities in neurodegenerative diseases and targeted therapies

From Redox Biology 1:19-13

Parkinson’s disease is associated with not only intracellular accumulation of α-synuclein, but also propagation of its intracellular damage, and transmission to neighboring cells.  We will use a novel transgenic mouse overexpressing lysosomal cathepsin D to test the hypothesis that enhancing specific lysosomal activities decreases α-synuclein spreading and attenuating α-synuclein-induced neurodegeneration. Success of this study may bring significant benefit to patients who are affected by this disease.

2.) Autophagy, mitophagy, bioenergetics, and aging

Redox Biology 4: 242-259

We have effectively used a systems biology approach to understand the mechanisms of transcription in the nervous system and apoptosis.  We extended this concept to autophagy with a system biology paper which revealed some previously unknown interactions and regulation of autophagy genes, lipid metabolism and calcium regulated proteases.  Ongoing work is examining regulation of autophagy in disease models both in vitro and in vivo.

3.) Understanding the role of protein O-GlcNAcylation in neurodegenerative diseases

Physiology Review 2021

Alzheimer’s disease (AD) and related dementia affects more than 5 million Americans, and the number is expected to nearly triple by 2050.  Therapeutic development faces diverse and significant challenges, including those faced by BACE inhibitors, anti-oxidants, and neutralizing antibodies. A better understanding of the fundamental biology in neurodegeneration and neuropathology in AD and related diseases is important.  O-GlcNAcylation, a nutrient and stress sensing protein post-translational modification pathway, may regulate key processes in neuronal function and survival and play an important role in human AD. The pathway is controlled by the action of O-GlcNAcase (OGA), which removes O-GlcNAc from modified proteins, and is currently explored as a therapeutic target.  Supporting inhibition of OGA as a therapeutic strategy are the observations that an oral pharmacologic OGA inhibitor thiamet G (TG) decreases tau phosphorylation in the brain in transgenic mice overexpressing tau.  Considering the potential of putting this strategy into human treatment, it is important to understand the broad pleiotropic impact of elevation of O-GlcNAcylation on neuronal functions and determine the underlying mechanisms.  Our laboratories have a long-term interest in O-GlcNAc biology, regulation of autophagy-endolysosomal pathways in neurodegenerative disease models.

4.) Circadian regulation of mitophagy in cardiovascular and neurodegenerative diseases

Annual Rev Physiology 82:79-101

Recent studies from our group and collaborators suggest that the circadian clock governs daily turnover of cellular constituents in the heart.  We will substantiate our study on circadian regulation of fundamental mechanisms including mitophagy and mitochondrial function in the heart and the brain, in the context of cardiovascular and Alzheimer’s Disease (AD). 

Representative Citations

  • Qiao L, Hamamichi S, Caldwell KA, Caldwell GA, Yacoubian TA, Wilson S, Xie ZL, Speake LD, Parks R, Crabtree D, Liang Q, Crimmins S, Schneider L, Uchiyama Y, Iwatsubo T, Zhou Y, Peng L, Lu YM, Standaert DG. Walls KC, Shacka JJ, Roth KA, Zhang J (2008) Lysosomal enzyme cathepsin D protects against α-synuclein aggregation and toxicity. Molecular Brain 1:17. PMCID:PMC2600785
  • Shacka J, Roth K, Zhang J (2008) The autophagy-lysosomal degradation pathway: role in neurodegenerative disease and therapy.  Frontiers in Bioscience 13:718-36
  • Qiao L, Zhang J (2009) Inhibition of lysosomal functions reduces proteasomal activity. Neurosci Lett 456:15-19
  • Schneider L, Zhang J (2010) Lysosomal function in macromolecular homeostasis and bioenergetics in Parkinson’s disease.  Molecular Neurodegeneration 5:14.  PMCID: PMC2867960
  • Walls KC, Ghosh AP, Franklin AL, Klocke BJ, Ballestas M, Shacka JJ,Zhang J, Roth KA (2010) Lysosome dysfunction triggers Atg7-dependent neural apoptosis. J Biol Chem 285:10497-507.  PMCID:PMC2856257
  • Jegga A, Schneider L, Ouyang X, Zhang J (2011) Systems biology of the autophagy-lysosomal pathway.  Autophagy 7:5, 1-13.  PMCID:PMC3127210
  • Liang Q, Ouyang X, Schneider L, Zhang J (2011) Reduction of mutant huntingtin accumulation and toxicity by lysosomal cathepsins D and B in neurons.  Molecular Neurodegeneration 6:37. PMCID:PMC3164227
  • Dranka BP, Benavides GA, Diers AR, Giordano S, Zelickson BR, Reily C, Zou L, Chatham J, Hill BG, Zhang J, Landar A, and Darley-Usmar VM(2011)Assessing bioenergetic function in response to oxidative stress by metabolic profiling.  Free Radical Biology and Medicine 51:1622-1635 PMCID:PMC3548422
  • Schneider L, Giordano S, Zelickson BR, Johnson MA, Benavides GA, Ouyang X, Fineberg N, Darley-Usmar VM, Zhang J (2011) Differentiation of SH-SY5Y cells to a neuronal phenotype changes cellular bioenergetics and the response to oxidative stress. Free Radical Biology and Medicine 51:2007-2017. PMCID:PMC3208787
  • Giordano S, Lee J, Darley-Usmar VM, Zhang J (2012) Distinct effects of rotenone, 1-methyl-4-phenylpyridinium and 6-hydroxydopamine on cellular bioenergetics and cell death. PlosOne 7(9):e44610. PMCID:PMC3435291
  • Crabtree D, Zhang J (2012) Genetically engineered mouse models for Parkinson’s diseases.  Brain Research Bulletin 88:13-32. PMCID:PMC3244549
  • Crabtree D, Boyer-Guittaut M, Ouyang X, Fineberg N, Zhang J (2013) Dopamine and its metabolites in cathepsin D heterozygous mice before and after MPTP administration. Neuroscience Letters 538: 3-8 PMCID: PMC3645893
  • Crabtree D, Dodson M, Ouyang X, Boyer-Guittaut M, Liang Q, Ballestas M, Fineberg N, Zhang J (2014) Overexpression of an inactive mutant cathepsin D increases endogenous alpha-synuclein and cathepsin B activity in SH-SY5Y cells. J Neurochem 128:950-61.  PMCID:PMC3951679
  • Giordano S, Dodson M, Ravi S, Ouyang X, Redmann M, Darley-Usmar V, Zhang J (2014) Bioenergetic adaptation in response to autophagy regulators during rotenone exposure.  J Neurochem 131:625-33 PMCID:PMC4454361
  • Redmann M, Wani W, Volpicelli-Daley L, Darley-Usmar V, Zhang J (2017) Trehalose does not improve neuronal survival on exposure to alpha-synuclein pre-formed fibrils.  Redox Biology 11:429-437 PMCID:PMC5220183
  • Cheng S, Wani WY, Hottman DA, Jeong A, Cao D, LeBlanc KJ, Saftig P, Zhang J*, Li L* (2017) Haplodeficiency of Cathepsin Ddoes not affect cerebral amyloidosis and autophagy in APP/PS1 transgenic mice.  J Neurochem 142(2):297-304 *Co-corresponding author PMCID:PMC5499660
  • Nelson M, Boutin M, Tse T, Lu H, Haley EM, Ouyang X, Zhang J, Auray-Blais C, Shacka JJ (2017) The lysosomal enzyme alpha-Galactosidase A is deficient in Parkinson’s disease brain in association with the pathologic accumulation of alpha-synuclein. Neurobiology of Disease 110:68-81 PMCID:PMC5747987
  • *Zhang J, Culp ML, Craver JG, Darley-Usmar V (2018) Mitochondrial function and autophagy: integrating proteotoxic, redox, and metabolic stress in Parkinson’s disease. *corresponding author. J Neurochem 144(6):691-709, PMCID:PMC5897151
  • Hossain MI, Marcus JM, Lee JH, Garcia PL, Singh VL, Shacka JJ, Zhang J, Gropen TI, Falany CN, Andrabi SA (2020) Restoration of cathepsin D and lysosomal function in stroke is neuroprotective. Autophagy (IF11)
  • Shacka J, Roth K, Zhang J (2008) The autophagy-lysosomal degradation pathway: role in neurodegenerative disease and therapy.  Frontiers in Bioscience 13:718-36
  • Jegga A, Schneider L, Ouyang X, Zhang J (2011) Systems biology of the autophagy-lysosomal pathway.  Autophagy 7:5, 1-13.  PMCID:PMC3127210
  • Dranka BP, Benavides GA, Diers AR, Giordano S, Zelickson BR, Reily C, Zou L, Chatham J, Hill BG, Zhang J, Landar A, and Darley-Usmar VM(2011)Assessing bioenergetic function in response to oxidative stress by metabolic profiling.  Free Radical Biology and Medicine 51:1622-1635 PMCID:PMC3548422
  • Jaber N, Dou Z, Chen JS, Catanzaro J, Jiang YP, Ballou LM, Selinger E, Ouyang X, Lin R, Zhang J, Zong WX (2012) The Class III PI3K Vps34 plays an essential role in autophagy and in the heart and liver function. Proc Nat Acad Sci USA 109:2003-2008. Co-corresponding author. PMCID: PMC3277541
  • Jaber N, Dou Z, Lin RZ, Zhang J, Zong WX (2012) Mammalian PIK3C3/VPS34: The key to autophagic processing in liver and heart. Autophagy 8:4, 707-708
  • Higdon AN, Benavides GA, Chacko B, Ouyang X, Johnson MS, Landar A, Zhang J, Darley-Usmar VM (2012)Hemin causes mitochondrial dysfunction in endothelial cells throughpromoting lipid peroxidation: the protective role of autophagy. American Journal of Physiology 302(7):H1394-409. PMCID:PMC3330785
  • Klionsky et al (Zhang J as one of 1270 co-authors) (2012) Guidelines for the Use and Interpretation of Assays for Monitoring Autophagy in Higher Eukaryotes. Autophagy 8:4, 445-544. PMCID:PMC3404883
  • Lee J, Giordano S, Zhang J (2012) Autophagy, mitochondrial and oxidative stress: cross-talk and redox signaling.  Biochemical Journal 441:523-540. PMCID:PMC3258656
  • Hill B, Benavides G, Lancaster J, Ballinger S, Dell’Italia L, Zhang J, Darley-Usmar VM (2012) Integration of cellular bioenergetics with mitochondrial quality control and autophagy.  Biological Chemistry 393:1485-1512. PMCID:PMC3594552
  • Mitchell T, Chacko B, Ballinger SW, Bailey SM, Zhang J, Darley-Usmar VM (2013) Convergent mechanisms for mitochondrial dysfunction in metabolic disease; insights from mitochondrial therapeutics.  Biochemical Society Transactions 41:127-133 PMCID:PMC3582193
  • Zhang J (2013) Autophagy and mitophagy in cellular damage control.  Redox Biology 1:19-23. PMCID:PMC3740586
  • Dodson M, Darley-Usmar V, Zhang J (2013) Cellular metabolic and autophagic pathways: traffic control by redox signaling.  Free Radical Biology and Medicine 63:207-221 PMCID:PMC3729625
  • Giordano S, Darley-Usmar V, Zhang J (2013) Autophagy as an essential cellular antioxidant pathway in neurodegenerative disease.  Redox Biology 2:82–90. PMCID:PMC3909266
  • Parekh VV, Wu L, Boyd KL, Williams, JA, Gaddy JA, Olivares-Villagomez D, Cover TL, Zong WX, Zhang J, Van Kaer L (2013) Impaired autophagy, defective T cell homeostasis and a wasting syndrome in mice with a T cell-specific deletion of Vps34. Journal of Immunity 190(10):5086-101. PMCID:PMC3646937
  • Le Grand JN, Bon K, Fraichard A, Zhang J, Jouvenot M, Risold P-Y, Boyer-Guittaut M, Delage-Mourroux R (2013) Specific distribution of the autophagic protein GABARAPL1/GEC1 in the developing and adult mouse brain and identification of neuronal populations expressing GABARAPL1/GEC1. PlosOne 8(5):e63133 PMCID:PMC3655077
  • Mitchell T, Johnson MS, Ouyang X, Chacko BK, Mitra K, Lei X, Gai Y, Moore DR, Barnes S, Zhang J, Koizumi A, Ramanadham S,Darley-Usmar VM (2013) Dysfunctional mitochondrial bioenergetics and oxidative stress in Akita+/Ins2-derived β-cells.  American J of Physiology 305(5):E585-99. PMCID:PMC3761167
  • Liang Q,Benavides G, Vasilopoulos A, Gius D, Darley-Usmar V, Zhang J (2013)Bioenergetic and autophagic control by Sirt3 in response to nutrient deprivation in mouse embryonic fibroblasts. Biochemical Journal 454:249-257 PMCID:PMC3927421
  • Benavides GA, Liang Q, Dodson M, Darley-Usmar V, Zhang J (2013) Inhibition of autophagy and glycolysis by nitric oxide during hypoxia-reoxygenation impairs cellular bioenergetics and promotes cell death in primary neurons. Free Radical Biology and Medicine 65:1215-1228 PMCID:PMC3859859
  • Dodson M, Liang Q, Johnson M, Redmann M, Fineberg N, Darley-Usmar V, Zhang J (2013)Inhibition of glycolysis attenuates 4-hydroxynonenal-dependent autophagy and exacerbates apoptosis in differentiated SH-SY5Y neuroblastoma cells. Autophagy 9:1996-2008. PMCID:PMC4028343
  • Boyer-Guittaut M, Poillet L, Liang Q, Bôle-Richard E, Ouyang X, Benavides GA, Chakrama F-Z, Fraichard A, Darley-Usmar VM, Despouy G, Jouvenot M, Delage-Mourroux R,Zhang J (2014) The role of GABARAPL1 (GEC1) in autophagic flux and mitochondrial quality control in MDA-MB-436 breast cancer cells.  Autophagy 10:6,986-1003 PMCID:PMC4091181
  • Chacko B, Kramer P, Ravi S, Benavides G, Mitchell T, Dranka BP, Ferrick D, Singal A, Ballinger S, Bailey SM, Hardy R, Zhang J, Zhi D, Darley-Usmar VM (2014) The Bioenergetic Health Index: A new concept in translational research.  Clinical Science 127:367-373 PMCID:PMC4202728
  • Giordano S, Dodson M, Ravi S, Ouyang X, Redmann M, Darley-Usmar V, Zhang J (2014) Bioenergetic adaptation in response to autophagy regulators during rotenone exposure.  J Neurochem 131:625-33 PMCID:PMC4454361
  • Levonen AL, Hill BG, Kansanen E, Zhang J, Darley-Usmar VM (2014) Redox regulation of antioxidants, autophagy and the response to stress; implications for electrophile therapeutics. Free Radical Biology and Medicine 71:196–207. PMCID:PMC4042208
  • Redmann M, Dodson M, Boyer-Guittaut M, Darley-Usmar VM, Zhang J (2014) Mitophagy mechanisms and role in human diseases. International Journal of Biochemistry and Cell biology 53C:127-133. PMCID:PMC4111979
  • Allison D, Antoine L, Ballinger S, Bamman M, Biga P, Darley-Usmar V, Fisher G, Gohlke J, Halade G, Hartman J, Hunter G, Messina J, Nagy T, Plaisance E, Roth K, Sandel M, Schwartz T, Smith D, Sweatt JD, Tollefsbol T, Watts S, Yang Y, Zhang J, Austad S (2014) Aging and Energetics’ ‘Top 40’ Future Research Opportunities 2010-2013.  F1000Research 12;3:219 PMCID:PMC4197746
  • Zhang J (2015) Teaching the basics of autophagy and mitophagy to redox biologists—mechanisms and experimental approaches. Redox Biology 4:242-259 PMCID:PMC4803799
  • Dodson M, Redmann M, Rajasekaran, NS, Darley-Usmar V, Zhang J (2015) KEAP1-NRF2 signaling and autophagy in protection against oxidative and reductive proteotoxicity. Biochem Journal 469:347-355. PMCID:PMC5514546
  • Jurkuvenaite A, Benavides GA, Komarova S, Doaran SF, Johnson M, Aggarwal S, Zhang J, Darley-Usmar VM, Matalon S (2015) Upregulation of autophagy decreases chlorine gas induced mitochondrial injury and lung inflammation. Free Radical Biology and Medicine 85:83-94 PMCID:PMC4508227
  • Rangarajan S, Kurundkar A, KurundkarD, Bernard K, Sanders Y, Ding Q,Antony VB, Zhang J, Zmijewski J, Thannickal VJ (2016) Novel mechanisms for the anti-fibrotic action of Nintedanib. American Journal of Respiratory Cell and Molecular Biology (AJRCMB) 54:51-59 PMCID: PMC4742925
  • Klionsky et al (Zhang J as one of ~2000 co-authors) (2016) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes.  Autophagy 12:1, 1-222 PMCID:PMC4835977
  • Radhakrishnan RK, Narasimhan M, Shanmugam G, Devarajan A, Palaniappan S, Zhang J, Halade G, Darley-Usmar VM, Hoidal JR, Rajasekaran NS (2016) Abrogation of Nrf2 impairs antioxidant signaling and promotes atrial hypertrophy in response to high-Intensity exercise stress. Journal of Translational Medicine 14:86 PMCID:PMC4822244
  • Redmann M, Darley-Usmar V, Zhang J (2016) The role of autophagy, mitophagy and lysosomal functions in modulating cellular bioenergetics and survival in the context of redox and proteotoxic damage: implications for age dependent neurodegenerative diseases. Aging and Disease 7:150-162 PMCID:PMC4809607
  • Hjelmeland A, Zhang J (2016) Metabolic, autophagic and mitophagic activities in cancer initiation and progression. Biomedical Journal 39:98-106 PMCID:PMC5514543
  • Wende AR, Young M, Chatham J, Zhang J, Rajasekaran NS, Darley-Usmar VM (2016) Redox biology and the interface between bioenergetics, autophagy and circadian control of metabolism. Free Radical Biology and Medicine 100:94-107PMCID:PMC5124549
  • Aggarwal S, Mannam P, Zhang J (2016) Autophagy and mitophagy in pulmonary diseases. Am J of Physiol Lung Cell Mol Physiol 311:L433-L452. PMCID:PMC5504426
  • Redmann M, Benavides GA, Berryhill TF, Wani WY, Ouyang X, Johnson MS, Ravi S, Barnes S, Darley-Usmar VM, Zhang J (2017) Inhibition of autophagy with bafilomycin and chloroquine decreases mitochondrial quality and bioenergetic function in primary neurons. Redox Biology 11:73-81 PMCID:PMC5124357
  • BernardK, Logsdon NJ, Herranz VM, Benavides GA, Zhang J, Darley-Usmar VM, Thannickal VJ (2017) NADPH Oxidase 4 (Nox4) Suppresses Mitochondrial Biogenesis in Lung Fibroblasts via a Nuclear Factor Erythroid- Derived 2-like 2 (Nrf2)-Dependent Pathway. J Biol Chem 292:3029-3038 PMCID:PMC5314196
  • Parakh VV, Pabbisetty SK, Wu L, Sebzda E, Martinez J, Zhang J, Van Kaer L (2017) The autophagy-related protein Vps34 controls the homeostasis and function of antigen cross-presenting CD8α+ dendritic cells. Proc Nat Acad Sci USA 114(31):E6371-E6380. PMCID:PMC5547642
  • McGinnis GR, Tang Y, Brewer R, Brahma M, Stanley HL, Shanmugam G, Rajasekaran NS, Row GC, Frank SJ, Wende AR, Abel ED, Taegtmeyer H, Litovsky S, Darley-Usmar V, Zhang J, Chatham JC, Young ME (2017) Genetic disruption of the cardiomyocyte circadian clock differentially influences insulin-mediated processes in the heart. Journal of Molecular and Cellular Cardiology 110:80-95 PMCID:PMC5586500
  • Wu P, Yuan X, Li F, Zhang J, Zhu W, Wei M, Li J, Wang X (2017) Myocardial upregulation of cathepsin D by ischemic heart disease promotes autophagic flux and protects against cardiac remodeling and heart failure.Circ Heart Fail 10:e004044 PMCID:PMC5535800
  • Dodson M, Benavides G, Johnson M, Redmann M, Wani WY, Ouyang X, Cofield SS, Mitra K, Darley-Usmar V, Zhang J (2017) Regulation of autophagy, mitochondrial dynamics and cellular bioenergetics by 4-hydroxynonenal in primary neurons. Autophagy 13(11):1828-1840 PMCID:PMC5788494
  • Bernard K, Logsdon NJ, Benavides GA, Sanders Y, Zhang J, Darley-Usmar VM, Thannickal VJ (2018) Glutaminolysis is required for TGF-β1-induced myofibroblast differentiation and activation. J Biol Chem 293(4):1218-1228 PMCID:PMC5787800
  • Brewer RA, Collins HE, Berry RD, Brahma MK, Tirado B, Stanley HL, Wende AR, Taegtmeyer H, Rajasekaran NS, Darley-Usmar V, Zhang J, Frank SJ, Chatham JC, Young ME (2018) Temporal partitioning of adaptive responses of the murine heart to fasting: a guide for experimental design. Life Sciences 197:30-39 PMCID:PMC5837814
  • Hough KP, Trevor JL, Strenkowski JG, Wang Y, Chacko BK, Tousif S, Chanda D, Steele C, Antony VB, Dokeland T, Ouyang X, Zhang J, Duncan SR, Thannickal VK, Darley-Usmar VM, Deshane JS (2018) Exosomal Transfer of Mitochondria from Airway Myeloid-Derived Regulatory Cells to T cells. Redox Biology 18:54-64 PMCID:PMC6031096
  • Libby CJ, Zhang S, Benavides GA, Scott SE, Li Y, Redmann M, Tran AN, Otamias A, Darley-Usmar V, Napieralo M, Zhang J, Augelli-Szafran CE, Zhang W, Hjelmeland A (2018) Identification of Compounds That Decrease Glioblastoma Growth and Glucose Uptake in Vitro. ACS Chemical Biology 13 (8), pp 2048–2057 PMCID:PMC6425477
  • Wright JN, Benavides GA, Johnson MS, Wani W, Ouyang X, Zou L, Collins H, Zhang J, Darley-Usmar V, Chatham JC (2019) Acute increases in O-GlcNAc indirectly impair mitochondrial bioenergetics through dysregulation of LonP1-mediated mitochondrial protein complex turnover.  American Journal of Physiology-Cell Physiology 316: C862-C875. PMCID: PMC6620580
  • Hill BG, Shiva S, Ballinger B, Zhang J, Darley-Usmar V (2019) Bioenergetics and translational metabolism: Implications for physiology and precision medicine. Biol Chem 401:3-29 PMCID: PMC6944318
  • Zhang J, Chatham JC, Young M (2020) Circadian regulation of cardiac biology: rhythms that keep the heart beating.   Annual Review of Physiology 82:5.1–5.23 PMCID:PMC7012667 (IF14) 
  • Ouyang X, Ahmad I, Johnson M, Redmann M, Craver J, Wani WY, Gloria A Benavides, Chacko B, Li P, Young M, Jegga A, Darley-Usmar V, Zhang J (2020) A novel function of nuclear receptor binding factor 2 (NRBF2) in learning and memory. Lab Inv 100:1238–1251 (IF4.25)
  • Chatham J, Young ME, Zhang J (2020) Role of O-linked N-acetylglucosamine (O-GlcNAc) modification of proteins in diabetic cardiovascular complications. Current Opinions in Pharmacology 57:1-12 (IF5.203)
  • Kim S, Song J, Ernst P, Latimer MN, Goh KY, Ha C-M, Ma W, Rajasekaran NS, Zhang J, Liu X, Prabhu SD, Qin G, Wende AR, Young ME, Zhou L (2020) MitoQ regulates redox-related non-coding RNAs to preserve mitochondrial network integrity in pressure overload heart failure.  AJP-Heart and Circulatory Physiology 318: H682–H695 (IF4.048)
  • Yang G, Song W, Postoak JL, Chen J, Martinez J, Zhang J, Wu L, Van Kaer L (2020) Autophagy-related protein Vps34 controls T cell metabolism and function.  Autophagy (IF11)
  • Ma X, McKeen T, Zhang J, Ding WX (2020) Role and mechanisms of mitophagy in liver diseases. Cells.
  • Mia S, Kane M, Latimer M, Reitz C, Sonkar R, Benavides G, Smith S, Frank S, Martino T, Zhang J, Darley-Usmar V, Young M (2020) Differential Effects of REV-ERBa/b Agonism on Cardiac Gene Expression, Metabolism, and Contractile Function in a Mouse Model of Circadian Disruption. Am J Physiol Heart Circ Physiol318:H1487–H1508 (IF4.048)
  • Fill D, Chacko BK, Conley R, Ouyang X, Zhang J, Darley-Usmar VM, Zuberi A, Lutz CM, Napierala M, Napierala JS (2020) Expression of FxnG127V causes hallmark FRDA pathological features. Disease Models and Mechanisms PMCID: PMC7406325 (IF4.028)
  • Zhang J (2020) The Promise of a Golden Era for Exploring the Frontiers of Aging, Metabolism and Redox Biology. Frontier in Aging 1:4.
  • Yang G, Song W, Xu J, Postoak JL, Cheng F, Martinez J, Zhang J, Wu L, Van Kaer L (2020) Pik3c3-deficiency in myeloid cells imparts partial resistance to experimental autoimmune encephalomyelitis associated with reduced IL-1β production. Cellular & Molecular Immunology (IF8.2)
  • Klionsky et al (Zhang J as one of ~3000 co-authors) (2021) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes (4th edition).  Autophagy (IF11)
  • Mueller T, Ouyang X, Johnson M, Qian W-J, Chatham JC, Darley-Usmar V, Zhang J (2021) New Insights into the Biology of Protein O-GlcNAcylation: Approaches and Observations. Frontier in Aging 1:5
  • Collins H, Kane MS, Hill B, Litovsky S, Darley-Usmar V, Young ME, Chatham JC, Zhang J (2021) Mitochondrial morphology and mitophagy in heart diseases: qualitative and quantitative analyses using transmission electron microscopy (TEM) Frontier in Aging
  • Scott SE, Libby CJ, Ayokanmbi A, Otamias A, Redmann M, Li Y, Griguer C, Zhang J, Napierala M, Ananthan A, Hjelmeland A (2021) Novel dopamine receptor 3 antagonists inhibit the growth of primary and temozolomide resistant glioblastoma. PlosOne (IF2.776)
  • Yang G, Postoak JL, Song W, Martinez J, Zhang J, Wu L, Van Kaer L (2021) Dendritic cell PIK3C3/VPS34 controls the pathogenicity of CNS autoimmunity independently of LC3-associated phagocytosis Autophagy (IF11)
  • Austad SN, Ballinger S, Buford TW, Carter CS, Smith Jr DL, Darley-Usmar V, Zhang J (2021) Targeting whole body metabolism and mitochondrial bioenergetics in the drug development for Alzheimer’s disease. Acta Pharmaceutica Sinica B (APSB)  Special Issue (IF11.4)
  • Benavides G, Mueller T, Darley-UsmarV, ZhangJ (2022) Optimization of measurement of mitochondrial electron transport activity in postmortem human brain samples and measurement of susceptibility to rotenone and 4-hydroxynonenal inhibition. Redox Biology 50:102241 (IF16)
  • Wani W, Boyer-Guittaut M, Dodson M, Chatham J, Darley-Usmar V, Zhang J (2015) Regulation of autophagy by protein post-translational modification.  Laboratory Investigation 95:14-25. PMCID:PMC4454381
  • Wani W, Chatham J, Darley-Usmar V, McMahon L, Zhang J (2017) O-GlcNAcylation and neurodegeneration.  Brain Res Bulletin 133:80-87 PMCID:PMC5292095
  • Wani WY, Ouyang X, Benavides GA, Redmann M, Cofield JS, Shacka JJ, Darley-Usmar V, Chatham JC, Zhang J (2017) O-GlcNAc regulation of autophagy and α-synuclein homeostasis; implications for Parkinson’s disease. Molecular Brain 10:32 PMCID:PMC5517830
  • Zhang J, Chatham JC, Young M (2020) Circadian regulation of cardiac biology: rhythms that keep the heart beating.   Annual Review of Physiology 82:5.1–5.23 PMCID:PMC7012667 (IF14) 
  • Chatham J, Young ME, Zhang J (2020) Role of O-linked N-acetylglucosamine (O-GlcNAc) modification of proteins in diabetic cardiovascular complications. Current Opinions in Pharmacology 57:1-12 (IF5.203)
  • Chatham JC, Zhang J, Wende AR (2020)Role of O-linked N-acetylglucosamine (O-GlcNAc) protein modification in cellular (patho)physiology. Physiology Review (IF24)
  • Mueller T, Ouyang X, Johnson M, Qian W-J, Chatham JC, Darley-Usmar V, Zhang J (2020) New Insights into the Biology of Protein O-GlcNAcylation: Approaches and Observations. Frontier in Aging.
  • Huynh VN, Wang S, Ouyang X, Wani WY, Johnson M, Chacko B,  Jegga AG, Qian W-J, Chatham J, Darley-Usmar V, ZhangJ (2021) Defining the dynamic regulation of O-GlcNAc proteome in the mouse cortex — The O-GlcNAcylation of synaptic and trafficking proteins related to neurodegenerative diseases. Frontier in Aging2:757801. doi: 10.3389/fragi.2021.757801
    • Huynh VN*, Benavides G*, Johnson M, Chacko BK, Ouyang X, Osuma E, Mueller T, Chatham J, Darley-Usmar V, ZhangJ (2022) Association of bioenergetic and nutrient sensing machineries in mice exposed to saline versus thiamet G in both sexes. Molecular Brain 15: 22 PMCID: PMC8898497 (IF3.627)
  • Wende AR, Young M, Chatham J, Zhang J, Rajasekaran NS, Darley-Usmar VM (2016) Redox biology and the interface between bioenergetics, autophagy and circadian control of metabolism. Free Radical Biology and Medicine 100:94-107PMCID:PMC5124549
  • McGinnis GR, Tang Y, Brewer R, Brahma M, Stanley HL, Shanmugam G, Rajasekaran NS, Row GC, Frank SJ, Wende AR, Abel ED, Taegtmeyer H, Litovsky S, Darley-Usmar V, Zhang J, Chatham JC, Young ME (2017) Genetic disruption of the cardiomyocyte circadian clock differentially influences insulin-mediated processes in the heart. Journal of Molecular and Cellular Cardiology 110:80-95 PMCID:PMC5586500
  • Brewer RA, Collins HE, Berry RD, Brahma MK, Tirado B, Stanley HL, Wende AR, Taegtmeyer H, Rajasekaran NS, Darley-Usmar V, Zhang J, Frank SJ, Chatham JC, Young ME (2018) Temporal partitioning of adaptive responses of the murine heart to fasting: a guide for experimental design. Life Sciences 197:30-39 PMCID:PMC5837814
  • Hill BG, Shiva S, Ballinger B, Zhang J, Darley-Usmar V (2019) Bioenergetics and translational metabolism: Implications for physiology and precision medicine. Biol Chem 401:3-29 PMCID: PMC6944318
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  • Chatham J, Young ME, Zhang J (2020) Role of O-linked N-acetylglucosamine (O-GlcNAc) modification of proteins in diabetic cardiovascular complications. Current Opinions in Pharmacology 57:1-12 (IF5.203)
  • Mia S, Kane M, Latimer M, Reitz C, Sonkar R, Benavides G, Smith S, Frank S, Martino T, Zhang J, Darley-Usmar V, Young M (2020) Differential Effects of REV-ERBa/b Agonism on Cardiac Gene Expression, Metabolism, and Contractile Function in a Mouse Model of Circadian Disruption. Am J Physiol Heart Circ Physiol318:H1487–H1508 (IF4.048)
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