Ginsberg Lab

Head of Lab

Stephen D. Ginsberg, PhD

Ginsberg Lab Members

Melissa J. Alldred, PhD Research Scientist/NKI; Research Assistant Professor, Dept of Psychiatry/NYULMC [email]

Amanda Labuza Postdoctoral Fellow [email]

Megan Gautier, PhD Student [email]

Arthur Saltzman, MS Research Technician [email]

Gisele Ferrari, Administrator [email]


All publications


About the Ginsberg Lab

The Vulnerability of Neuronal Cell Types to Brain Disease

The Ginsberg Lab , led by Stephen D. Ginsberg, PhD , aims to understand mechanisms underlying selective vulnerability associated with AD. Our researchers extensively characterize individual populations of neurons from AD and Down syndrome models and postmortem brains using high-throughput gene assays. Individuals with Down syndrome develop neuropathological changes seen in early AD.

We are currently profiling selectively vulnerable neurons and comparing them with relatively spared neurons during AD onset and progression. We are also analyzing selective vulnerability in the hippocampus by evaluating several different hippocampal neuron subtypes simultaneously. Animal studies suggest that specific gene pathways associated with neuron survival and intracellular trafficking are important for normal neuron function, partially explaining why some neurons are vulnerable and others resilient. Parallel studies in the postmortem brain indicate that individual genes and their encoded proteins in these critical pathways are disrupted in AD, especially within vulnerable neurons early in the disease.

Our translational research is directed toward reversing the dysregulation of genetic pathways in vulnerable neurons. One project employs a chronic dietary restriction approach in adult AD mice. Another uses an early development dietary supplementation in Down syndrome mice to positively affect vulnerable hippocampal neurons as adults. We then evaluate treatment benefits using the single-population profiling procedure for potential therapeutic development.

The hippocampal formation and cholinergic basal forebrain, brain regions critical for learning and memory, are the main structures analyzed, with particular emphasis given to identifying mechanisms that underlie changes within specific cell types, including cholinergic basal forebrain (CBF) neurons, dentate gyrus granule cells, CA1 & CA3 pyramidal neurons, and entorhinal cortex stellate cells. Experiments are conducted on animal and cellular models of neurodegeneration, including mouse models of amyloid overexpression, Down syndrome (DS), and tauopathy. The Ginsberg lab also conducts parallel studies on postmortem human brain tissues accrued from subjects diagnosed with Alzheimer’s disease (AD), DS, mild cognitive impairment (MCI), and nondemented controls with no cognitive impairment (NCI). Dr. Ginsberg is also spearheading a program to investigate selective vulnerability of specific pyramidal neurons and GABAergic interneurons in schizophrenia (SZ) and major depressive disorder (MDD).

The Ginsberg Laboratory has provided essential data in human and relevant mouse models that compare and contrast cells that degenerate (e.g., CBF neurons, CA1 hippocampal pyramidal neurons, and glutamatergic neocortical pyramidal neurons) versus cells that are relatively spared within these specific paradigms (e.g., dentate gyrus granule cells). Dr. Ginsberg is one of the relatively few neuroscientists that conduct expression profiling research at the single cell level consistently. Dr. Ginsberg developed his own RNA amplification technology termed terminal continuation (TC) RNA amplification which is employed in conjunction with microarray and qPCR based investigations of gene expression at the single cell level. The Ginsberg laboratory has just developed a new technology for the amplification of microRNAs termed miRNA signature sequence amplification (SSAM) for biomarker discovery science. miRNAs are a short 17-25 nucleotide class of non-protein coding RNAs (ncRNAs) that have been shown to have critical functions in a wide variety of biological processes. One major obstacle when profiling miRNAs is their low expression level. miRNAs are estimated to constitute only 0.01% of total RNA. As a result, large quantities of starting materials were required for miRNA profiling until the advent of the developing SSAM technology.

Recent research achievements include:
Postmortem single cell gene expression analyses in hippocampal CA1 pyramidal neurons demonstrating up regulation of endosomal markers (including rab GTPases rab5 and rab7) with concomitant down regulation of the BDNF receptor TrkB in AD and mild cognitive impairment (MCI). Based on these postmortem human microarray, qPCR, and protein-based observations, we were able to determine in vitro that rab5 down regulates TrkB expression, providing a potential mechanism for lack of neurotrophic support during the progression of AD.

Postmortem single cell gene expression analyses in cholinergic basal forebrain (CBF) neurons demonstrating down regulation of nerve growth factor receptor TrkA, BDNF receptor TrkB, and neurotrophin-3 receptor TrkC, but not the pan-nerve growth factor receptor p75 in AD and MCI.

Correlation of antemortem cognitive decline with postmortem down regulation of TrkB and up regulation of rab5 and rab7 expression within individual CBF and CA1 neurons in normal control, MCI, and AD patients.

Identifying a shift in the expression of 3-repeat tau (3Rtau) relative to 4-repeat tau (4Rtau) within individual CBF neurons and CA1 pyramidal cells in MCI and AD as compared to normal controls.

Characterizing transcripts and proteins in adult mice that are differentially regulated in the dentate gyrus (granule cells as well as granule cell dendrites) following perforant path lesions over a 6 month postlesion time course including specific NMDA receptors and AMPA glutamate receptors.

Demonstrating specific transcripts are differentially regulated in hippocampal CA1 neurons that bear neurofibrillary tangles (NFTs) in AD versus non-tangle bearing CA1 neurons in normal control brains.

Illustrating that classes of transcripts within single CA1 pyramidal neurons tended to be genes related to neuronal communication, whereas glial-associated markers were under represented in CA1 pyramidal neurons relative to regional hippocampal dissections. These observations highlight a dilution effect that is likely to occur in conventional regional microarray and qPCR studies.

Current research endeavors include:
Expression profiling of neocortical pyramidal neurons as well as calbindin-immunoreactive and parvalbumin-immunoreactive interneurons within the auditory cortex of schizophrenics compared to age-matched normal controls.

Molecular fingerprinting of hippocampal CA1 pyramidal neurons throughout the lifespan of a mouse model of tauopathy (hTau mice).

Expression profiling of hippocampal and basal forebrain circuits at time points before and following cholinergic neurodegeneration a mouse model of Down’s syndrome and AD (Ts65Dn mice).

Assessment of hippocampal pyramidal neurons and entorhinal cortex stellate cells in mouse models of AD and DS (Tg2576 mouse and Ts65Dn mouse) following caloric restriction.

Single cell expression profiling of the six isoforms of tau as well as truncated tau isoforms within vulnerable cell types in postmortem human brains in AD and related tauopathies as well as tauopathy animal models.

Future endeavors include:
Nanotechnology development of RNA amplification to facilitate expression profiling of processes (including dendritic spines and developing axonal profiles) and subcellular elements (including mitochondria and lysosomes) that can test the overriding hypothesis of selective vulnerability within specific forebrain circuits.

Subcellular fractionation (including synaptic, postsynaptic density, and mitochondrial fractions) of tissue homogenates for discrete proteomic evaluations including tandem MS/MS and MALDI-TOF assessments in postmortem hippocampus in normal, MCI, and AD as well as analysis of subcellular fractions in normal mice and transgenic models subjected to perforant path transections.

Ginsberg Lab TC RNA Amplification Protocol
Click here to view protocol or click the icon to download as a PDF PDF

Selected publications since 2008 (from a total of 75 peer-reviewed manuscripts and 23 book chapters)

Ginsberg, S.D.: Transcriptional profiling of small samples in the central nervous system. Methods Mol. Biol., 439: 147-158, 2008. PMID: 18370101. PMCID: PMC2648843.

Levine, S., Saltzman, A., and Ginsberg, S.D.: Different inflammatory reactions to vitamin D(3) among the lateral, third and fourth ventricular choroid plexuses of the rat. Exp. Mol. Pathol., 85: 117-121, 2008. PMID: 18675267.

Mufson, E.J., Counts, S.E., Perez, S., and Ginsberg, S.D.: Cholinergic system during the progression of Alzheimer’s disease: therapeutic implications. Expert Rev. Neurother., 8: 1703-1718, 2008. PMID: 18986241. PMCID: PMC2631573.

Alldred, M.J., Che, S., and Ginsberg, S.D.: Terminal continuation (TC) RNA amplification enables expression profiling using minute RNA input obtained from mouse brain. Int. J. Mol. Sci., 9: 2091-2104, 2008. PMID: 19165351. PMCID: PMC2629436.

Ginsberg, S.D., Che, S., Counts, S.E., and Mufson, E.J.: Gene expression abnormalities mark the progression of Alzheimer's disease. In Sun, M.K. (ed): Research Progress in Alzheimer's Disease and Dementia, Volume 3, Hauppauge: Nova Science Publishing, pp. 25-58, 2008. ISBN-13: 978-1-60021-960-3.

Ginsberg, S.D.: Single and rare cell analysis-amplification methods. T7 based amplification protocols. In Bosio, A. and Gerstmayer, B. (eds): Microarrays in Inflammation. Progress in Inflammation Research, Basel: Birkhäuser-Verlag, pp. 81-94, 2008. ISBN-13: 978-3-7643-8333-6.

Altar, C.A., Vawter, M., and Ginsberg, S.D.: Target identification for CNS diseases by transcriptional profiling. Neuropsychopharmacology, 34: 18-54, 2009. PMID: 18923405. PMCID: PMC2675576.

Alldred, M.J., Che, S., and Ginsberg, S.D.: Terminal continuation (TC) RNA amplification without second strand synthesis. J. Neurosci. Meth., 177: 381-385, 2009. PMID: 19026688. PMCID: PMC2659495.

Levine, S., Saltzman, A., Levy, E., and Ginsberg, S.D.: Systemic pathology in aged mouse models of Down's syndrome and Alzheimer's disease. Exp. Mol. Pathol., 86: 18-22, 2009. PMID: 19041304. PMCID: PMC2659493.

Choi, J.H.K., Berger, J.D., Mazzella, M.J., Morales-Corraliza, J., Nixon, R.A., Ginsberg, S.D., Levy, E., and Mathews, P.M.: Age-dependent dysregulation of brain amyloid precursor protein in the Ts65Dn Down syndrome mouse model. J. Neurochem., 110: 1818-1827, 2009. PMID: 19619138. PMCID: PMC2744432.

Jiang, Y., Mullaney, K.A., Peterhoff, C.M., Che, S., Schmidt, S.D., Boyer-Boiteau, A., Ginsberg, S.D., Cataldo, A.M., Mathews, P.M., and Nixon, R.A.: Alzheimer’s-related endosome dysfunction in Down syndrome is Abeta-independent but requires APP and is reversed by BACE-1 inhibition. Proc. Natl. Acad. Sci. USA, 107: 1630-1635, 2010. PMID: 20080541. PMCID: PMC2824382.

Ginsberg, S.D.: Alterations in discrete glutamate receptor subunits in adult mouse dentate gyrus granule cells following perforant path transection. Anal. Bioanal. Chem., 397: 3349-3358, 2010. PMID: 20577723. PMCID: PMC3149099.

Levine, S., Saltzman, A., and Ginsberg, S.D.: Mitotic figures in the median eminence of the hypothalamus. Neurochem. Res., 35: 1743-1746, 2010. PMID: 20680457. PMCID: PMC3148030.

Haskew-Layton, R.E., Payappilly, J.B., Smirnova, N.A., Ma, T.C., Chan, K.K., Murphy, T.H., Guo, H., Langley, B., Sultana, R., Butterfield, D.A., Santagata, S., Alldred, M.J., Gazaryan, I.G., Bell, G.W., Ginsberg, S.D., and Ratan, R.R.: Controlled enzymatic production of astrocytic hydrogen peroxide protects neurons from oxidative stress via an Nrf2 independent pathway. Proc. Natl. Acad. Sci. USA, 107: 17385-17390, 2010. PMID: 20855618. PMCID: PMC2951414.

Ginsberg, S.D., Alldred, M.J., Counts, S.E., Cataldo, A.M., Neve, R.L., Jiang, Y., Wuu, J., Chao, M.V., Mufson, E.J., Nixon, R.A., and Che, S.: Microarray analysis of hippocampal CA1 neurons implicates early
 endosomal dysfunction during Alzheimer’s disease progression. Biol. Psychiatry, 68: 885-893, 2010. PMID: 20655510. PMCID: PMC2965820.

Kaur, G., Mohan, P., Pawlik, M., DeRosa, S., Fajiculay, J., Che, S., Grubb, A., Ginsberg, S.D., Nixon, R.A., and Levy, E: Cystatin C rescues degenerating neurons in a cystatin B-knockout mouse model of progressive myoclonus epilepsy. Am. J. Pathol., 177: 2256-2267, 2010. PMID: 20889561. PMCID: PMC2966785.

Ginsberg, S.D.: Microarray use for the analysis of the CNS. In Squire, L.R. (ed): Encyclopedia of Neuroscience, Volume 5, Oxford: Academic Press, pp. 835-841, 2009. ISBN-13: 978-0-08-045046-9.

Ginsberg, S.D.: Gene microarrays. In Kompoliti, K., and Verhagen Metman, L. (eds): Encyclopedia of Movement Disorders. Oxford: Academic Press, pp. 538-540, 2010. ISBN: 978-0-12-374101-1.

Mufson, E.J., Counts, S.E., Perez, S.E., and Ginsberg, S.D.: Cholinergic systems in aging and Alzheimer’s disease: neurotrophic and molecular analysis. In Koob, G.F., Le Moal, M., and Thompson, R.F. (eds): Encyclopedia of Behavioral Neuroscience, Volume 1, Oxford: Academic Press, pp. 249-256, 2010. ISBN-13: 978-0-08-044732-2.

Devi, L., Alldred, M.J., Ginsberg, S.D., and Ohno, M.: Sex- and brain region-specific acceleration of beta-amyloidogenesis following behavioral stress in a mouse model of Alzheimer's disease. Molecular Brain, 3: 34, 2010. PMID: 21059265. PMCID: PMC2988063.

Ginsberg, S.D., Mufson, E.J., Counts, S.E., Wuu, J., Alldred, M.J., Nixon, R.A., and Che, S.: Regional selectivity of rab5 and rab7 protein upregulation in mild cognitive impairment and Alzheimer’s disease. J. Alzheimers Dis., 22: 631-639, 2010. PMID: 20847427. PMCID: PMC3031860.

Counts, S.E., Perez, S.E., Ginsberg, S.D., and Mufson, E.J.: Neuroprotective role for galanin in Alzheimer’s disease. EXS, 102: 143-162, 2010. PMID: 21299067. PMCID: PMC3117305.

Levine, S., Saltzman, A., and Ginsberg, S.D.: Vacuolar pathology in the median eminence of the hypothalamus after hyponatremia. J. Neuropathol. Exp. Neurol., 70: 151-156, 2011. PMID: 21343884. PMCID: PMC3074179.

Ginsberg, S.D., Mufson, E.J., Alldred, M.J., Counts, S.E., Wuu, J., Nixon, R.A., and Che, S.: Upregulation of select rab GTPases in cholinergic basal forebrain neurons in mild cognitive impairment and Alzheimer's disease. J. Chem. Neuroanat., 42: 102-110, 2011. PMID: 21669283. PMCID: PMC3163754.

Counts, S.E., Che, S., Ginsberg, S.D., and Mufson, E.J.: Gender differences in neurotrophin and glutamate receptor expression in cholinergic nucleus basalis neurons during the progression of Alzheimer's disease. J. Chem. Neuroanat., 42: 111-117, 2011. PMID: 21397006. PMCID: PMC3155625.

Ginsberg, S.D., Che, S., Hashim, A., Zavadil, J., Cancro, R., Lee, S.H., Petkova, E., Sershen, H.W., and Volavka, J.: Differential regulation of catechol-O-methyltransferase expression in a mouse model of aggression. Brain Struct. Funct., 216(4):347-56, 2011. PMID: 21512897. PMCID: PMC3199365.

Mufson, E.J., Perez, S., Kelley, C.M., Chu, S., Galarza, A., Blakely, S., and Ginsberg, S.D.: Fixation protocols for neurohistology: neurons to genes. In Walz, C.M., and Doucette, R. (eds): Neurohistology and Imaging: Basic Techniques, Totowa: Humana Press, in press.

Ginsberg, S.D., Alldred, M.J., and Che, S.: Gene expression profiling using the terminal continuation (TC) RNA amplification method for small input samples in neuroscience. In Karamanos, Y. (ed): Expression Profiling in Neuroscience, Neuromethods, Volume 64. New York: Humana Press, 2012. ISBN 978-1-61779-447-6.

Ginsberg, S.D., Alldred, M.J., and Che, S.: Gene expression levels assessed by CA1 pyramidal neuron and regional hippocampal dissections in Alzheimer's disease. Neurobiol. Dis., 45(1):99-107, 2012. PMID: 21821124. PMCID: PMC3220746.

Ginsberg, S.D., Hemby, S.E. and Smiley, J.F.: Expression profiling in neuropsychiatric disorders: emphasis on glutamate receptors in bipolar disorder. Pharmacol. Biochem. Behav., 100: 705-711, 2012. PMID:22005598. PMCID:PMC3253885.

Alldred, M.J,. Duff, K ., and Gindberg, S.D: Microarray analysis of CAI pyramidal neurons in a mouse model of tuopathy reveals progressive synaptic dysfunction. Neurobiol. Dis., 45: 751-762, 2012. PMID: 22079237. PMCID:PMC3259262.

Mufson, E.J., Binder, L., Counts, S.E., DeKosky, S.T., deToledo-Morrell, L., Ginsberg, S.D., Ikonomovic, M., Perez, S.E., and Scheff, S.W.: Mild cognitive impairment: pathology and mechanisms. Acta Neuropathol., 123: 13-30, 2012. PMID:22101321. PMCID:PMC3282485.

Perez, S.E., Getova, D.P., He, B., Counts, S.E. Geula, C., Coutadeur, S, Peillon., Desire, L., Ginsberg, S.D., and Mufson, EJ.: Rac1b increases with progressive tau pathology with cholinergic nucleus basalis neurons in Alzhiemer's disease. Am. J. Pathol., 180: 526-540, 2012. PMID:22142809. PMC3349868.

Devi, L., Alldred, MJ., Ginsberg, S.D., and Ohno, M.: Mechanisms underlying insulin deficiency-induced acceleration of β-amyloidosis in a mouse model of Alzheimer's disease. PLoS One, 7: e32792, 2012. PMID: 22403710. PMCID:PMC3293895.

Zhang, Y.Q., Henderson, M.X., Colangelo, C.M., Ginsberg, S.D., Bruce, C., Wu, T., and Chandra, S.S.: Identification of CSPα clients reveals a role in dynamin 1 regualtion. Neuron, 74: 136-150, 2012 PMID:22500636. PMCID:PMC3328141.

Pillai, A., Bruno, D., Sarreal, A.S., Hernando, R.T., Saint-Louis, L.A., Nierenberg, J., Ginsberg, S.D., Pomara, N., Mehta, P.D., Zetterberg, H., Blennow, K., and Buckley, P.F.: Plasma BDNF levels vary in relation to body weight in females. PLoS One, 7: e39358, 2012. PMID: 227768299. PMCID: PMC3388065.

Mufson, E.J., He, B., Nadeem, M., Perez, S.E., Counts, S.E., Leurgans, S., Fritz, J., Lah, J., Ginsberg, S.D., Wuu, J., and Scheff, S.W.: Hippocampal proNGF signaling pathways and β-amyloid levels in mild cognitive impairment and Alzheimer's disease. J.Neuropathol. Exp. Neurol., 71: 1018-1029, 2012. PMID:23095849. PMCID:PMC3481187.

Velazquez, R., Ash, J.A., Powers, B.E., Kelley, C.M., Strawderman, M., Luscher, Z.I., Ginsberg, S.D., Mufson, E.J,, and Strupp, B.J.: Maternal choline supplementation improves spatial learning and adult hippocampal neurogenesis in the Ts65Dn mouse model of Down Syndrome. Neurobiol. Dis., 58: 92-101, 2013. PMID: 23643842. PMCID:PMC4029409.

Kelley, C.M., Powers, B.E., Velazquez, R., Ash, J.A., Ginsberg, S.D., Strupp, B.J., and Mufson, E.J.: Sex differences in the cholinergic basal forebrain in the Ts65Dn mouse model of Down syndrome and Alzheimer's disease. Brain Pathol., 24:33-44, 2014. PMID:23802663. PMCID:PMC4220609.

Kelley, C.M., Powers, B.E., Velazquez, R., Ash, J.A., Ginsberg, S.D., Strupp, B.J., and Mufson, E.J.: Maternal choline supplementation differentially alters the basal forebrain cholinergic systemof youg-adult Ts65Dn and disomic mice. J. Comp. Neurol., 522: 1390-1410, 2014. PMID: 24178831. PMCID: PMC3959592.

Counts, S.E., Alldred, M.J., Che, S., Ginsberg, S.D., and Mufson, EJ.: Synaptic gene dysregulation within hippocampal CA1 pyramidal neurons in mild cognitive impairment. Neuropharmacology, 79: 172-179, 2014. PMID:24445080. PMCID: PMC3951099.

Kaur, K., Sharma A., Xu, W., Gerum, S., Alldred, M.J.,Shivkumar, S., Basavarajappa, B.S., Pawlik, M., Ohno, M., Ginsberg, S.D., Wilson, D.A., Guilfoyle, D.N., and Levy, E: Glutamatergic transmission aberration: a major cause of behavioral deficits in a murine model of Down's syndrome. J.Neurosci., 34: 5099-5106, 2014. PMID:24719089. PMCID:PMC3983795.

Ash, J.A., Velazquez, R., Kelley, C.M., Powers, B.E., Ginsberg, S.D., Mufson, E.J., and Strupp, B.J.: Maternal choline supplementation improves spatial mapping and increases basal forebrain cholinergic neuron number and size in aged Ts65Dn mice. Neurobiol. Dis., 70: 32-42, 2014. PMID: 24932939. PMCID: PMC4133151.

Yan, J., Ginsberg, S>D., Powers, B., Alldred, M.J., Saltzman, A., Strupp, BJ., and Caudill, M>A.: Maternal choline supplementation programs greater activity of the phosphotidylethanolamine N-methyltransferase(PEMT) pathway in adult Ts65Dn trisomic mice. FASEB J., 28: 4312-423,2014. PMID: 24963152. PMCID:PMC4202107.

Alldred, M.J., Lee, S.H., Petkova, E., and Ginsberg, S.D.: Expression profile analysis of hippocampal CA1 pyramidal neurons in aged Ts65Dn mice, a model of Down syndrome(DS) and Alzheimer's disease(AD). Brain Struc. Funct., 220:2983-2996, 2015. PMID:25031177. PMCID: PMC4297601.

Mariga, A., Zavadil, J., Ginsberg, S.D., and Chao, M.V.: Withdrawal of BDNF from hippocampal cultures leads to chages in genes involved in synaptic function. Dev.Neurobiol., 75: 173-192, 2015. PMID: 25059794. PMCID PMC4329925.

Alldred, M.J., Lee, S.H., Petkova, E., and Ginsberg, S.D.: Expression profile analysis of vulnerable CA1 pyramidal neurons in young-middle aged Ts65Dn mice. J. Comp. Neurol., 523:61-74, 2015. PMID:25131634. PMCID:PMCC4232465.

Schafer, M.J., Alldred, M.J., Lee, S.H., Calhoun, M.E., Petkova, E., Mathews, P.M., and Ginsberg, S.D.: Female-specific reduction of β-amyloid and γ-secretase by caloric restriction in Tg2576 mice. Neurobiol Aging, 36: 1293-1302, 2015. PMID:25556162. PMCID:PMC4346433.

Ginsberg, S.D., and Che, S.: Methods and compositions for amplification and detection of microRNAs(miRNAs) and noncoding RNAs(ncRNAs) using the signature sequence amplification method(SSAM). Recent Adv. DNA Gene Seq., 8: 2-9, 2015.PMID:25564022. PMCID:PMC4321964.

Perez, S.E., Hi, B., Nadeem., M., Wuu, J., Ginsberg, S.D., Ikonomovic, M.D., and Mufson, E.J.: Hippocampal endosomal,lysosomal and autophagic dysregulation in mild cognitive impairment: correlation with Aβ and tau pathology. J.Neuropathol. Exp. Neurol., 74: 345-358, 2015. PMID: 25756588. PMCID: PMC4366294.

Mufson, E.J., Mahady, L., Waters, D., Counts, S.E., Prez, S.E., DeKosky, S.T., Ginsberg, S.D., Ikonomovic, M.D, Scheff, S.W., aand Binder, L.:Hippocampal plasticity during the progression of Alzheimer's disease. Neuroscience, 309: 51-67, 2015. PMID: 25772787. PMCID: PMC4567973.

Schafer, M.J., Dolgalev, I., Alldred, M.J., Heguy, A., and Ginsberg, S.D.: Calorie restriction suppresses age dependent hippocampal CA1 transcritional signatures. PLoS One,10: e0133923, 2015. PMID: 26221964. PMCID:PMC4519125.

Strupp, B.J., Powers, B.E., Velazquez, R., Ash, J.A., Kelley, C.M., Alldred, M.J., Strawderman, M.S., Caudill, M.A., Mufson, E.J., and Ginsberg, S.D.: Maternal choline supplementation: A potential prenatal treatment for Down syndrome and Alzheimer's disease. Curr. Alzheimer Res., 13: 97-106, 2016. PMID:26391045. PMCID:PMC4733524.

Kelley, C.M., Ash, J.A., Powers, BE., Velazquez, R., Alldred, M.J., Ikonomovic, M.D., Ginsberg, S.D., Strupp, B.J., and Mufson, E.J.: Effects of maternal choline supplementation on the septohippocampal cholinergic system in teh Ts65Dn mouse model of Down Syndrome. Curr. Alzheimer Res., 13: 84-96, 2016. PMID: 26391046. PMCID: PMC4733527.

Henderson, M.X., Wirak, G.S., Zhang, Y-Q., Dai, F., Ginsberg, S.D., Dolzhanskaya, N, Staropoli, J.F., Nijssen, P.C.G., Lam, T.K.T., Roth, A.F., Davis, N.G., Dawson, G., Velinov, M., and Chandra, S.S.: Neuronal ceroid lipofuscinosis with DNAJC5/CSPα mutation has PPT1 pathology and exhibit aberrant protein palmitoylation. Acta Neuropathol., 131: 621-637, 2016. PMID: 26659577. PMCID: PMC4791186.

Powers, B.E., Velazquez, R., Kelley, C.M., Ash, J.A., Strawderman, M.S., Alldred, M.J.,Ginsberg, S.D., Mufson E.J., and Strupp, B.J.: Attentional function and basal forebrain cholinergic neuron morphology during aging in the Ts65Dn mouse model of Down syndrome. Brain Struct. Funct., 221:4337-4352, 2016. PMID: 26719290. PMCID: PMC4929047.

Jiang, Y.,Rigoglioso, A., Peterhoff, C.M., Pawlik, M., Sato, Y., Bleiwas, C., Stavrides, P., Smiley, J.F., Ginsberg, S.D., Mathwes, P.M., Levy, E., and Nixon, R.A.: Partial BACE1 reduction in a Down syndrome mouse model blocks Alzheimer-related endosomal anomalies and cholinergic neurodegeneration: role of APP-CTF. Neurobiol Aging, 39: 90-98, 2016. PMID:26923405. PMCID: PMC4773919.

Morales-Corraliza, J., Wong, H., Mazzella, M.J., Che, S., Lee, S.H., Petkova, E., Wagner, J.D., Hemby, S.E., Ginsberg, S.D., and Mathews, P.M.: Brain-wide insulin resistance, tau phosphorylation changes, and hippocampal neprilysin and amyloid-β alterations in a monkey model of type 1 diabetes. J. Neurosci., 36: 4248-4258, 2016, PMID: 27076423. PMCID:PMC4829649.

Tiernan, C.T., Ginsberg, S.D., Guillozet-Bongaatrs, A.L., S.M., He, B., Kanaan, N.M., Mufson, E.J., Binder, L.I., and Counts, S.E.: Protein homeostasis gene dysregulation in pretangle-bearing nucleus basalis neurons during the progression of Alzheimer's disease. Neurobiol Aging, 42: 80-90. PMID:27143424. PMCID:PMC4973891.

Mufson,E.J., Ikonomovic, M.D., Counts, S.E., Perez, S.E., Malek-Ahmadi, M., Scheff, S.W., and Ginsberg, S.D. Molecular and cellular pathophysiology of preclinical Alzheimer's disease. Bhav. Brain Res, 311: 54-69,2016. PMID: 27185734. PMCID:PMC4931948.

Campanari, M.L., Navarrete, F., Ginsberg, S.D., Manzanares, J., Saez-Valero, J., and Garcia-Ayllon, M.S.: Increased expression of readthrough acetylcholinesterase variants in the brains of Alzheimer's disease patients. J. Alzheimers Dis., 53: 831-841, 2016. PMID: 27258420. PMCID: PMC5013723.

Rosa, E., Mahendram, S., Ke, Y., Ittner, L., Gindberg, S.D., and Fahnestock, M.: Tau modulates BDNF expression and mediates Aβ-induced BDNF down-regulation in animal and cellular models od Alzheimer's disease. Neurobiol Aging, 48: 135-142, 2016. PMID: 27676333. PMCID: PMC5159317.

Bordi, M., Berg, M.J., Mohan, P.S., Peterhoff, C.M., Alldred, M.J., Che, S., Ginsberg, S.D., and Nixon, R.A.: Autophagy flux in CA1 neurons of Alzheimer hippocampus: increased induction overburdens failing lysosomes to propel neuritic dystrophy. Autophagy, 12:2467-2484, 2016. PMID:27813694. PMCID: PMC5173282.

Powers, B.E., Kelley, C.M., Velazquez, R., Ash, J.A., Strawderman, M.S., Alldred, M.J., Ginsberg, S.D., Mufson E.J., and Strupp, B.J.: Maternal choline supplementation in a mouse model of Downn syndrome: effects on attention and nucleus basalis/substantia innominata neuron morphology in adult offsping. Neuroscience, 340: 501-514, 2017. PMID: 27840230. PMCID: PMC5177989.

Arango-Lievano, M., Peguet, C., Catteau, M., Parmentier, M.L., Wu, S., Chao, M.V., Ginsberg, S.D., and Jeanneteau, F.: Deletion of beurotrophin signaling through the glucocorticoid receptor pathway causes tau neuropathology, Sci. Rep., 6:37231, 2016. PMID:27849045. PMCID: PMC5110980.

Kelly, S.C., He, B., S.E., Ginsberg, S.D., Mufson, EJ., and Counts, E.E.: Locus coeruleus cellular and molecular pathology during the progression of Alzheimer's disease. Acta Neuropathol Commun, %: 8, 2017. PMID: 28109312. PMCID: PMC5251221.

Gauthier, S.A., Perez-Gonzalez, R., Sharma, A., Huang, F.K., Alldred, M.J., Pawlik, M., Kaur, G., Ginsberg, S.D., Neubert, T.A., and Levy, E.: Enhanced exosome secretion in Down syndrome brain - a protective mechanism to alleviate neuronal endosomal abnormalities. Acta Neuropathol Commun., 5: 65, 2017. PMID:28851452. PMCID:PMC5576289.

Ginsberg, S.D., Malek-Ahmadi, M.H., Alldred, M.J., Che, S., Elarova, I., Chen, Y., Keanneteau, F., Kranz, T.M., Chao, M.V., Counts, S.E., and Mufson, E.J.: Selective decline of neurotrophin receptor genes within CA1 pyramidal neurons and hippocampus proper: correlation with cognitive performance and neeuropathology in mild cognitive impairment and Alzheimer's disease. Hippocampus, 2017 Sep 9. [Epub ahead of print]. PMID: 28888073.

Jeanneteau F, Barrere C, Vos M, De Vries CJM, Rouillard C, Levesque D, Dromard Y, Moisan MP, Duric V, Franklin TC, Duman RS, Lewis DA, Ginsberg SD, Arango-Lievano M. The Stress-Induced Transcription Factor NR4A1 adjusts Mitochondrial Function and Synapse Number in Prefrontal Cortex. J Neurosci. 2018 28(6):1335-1350 PMID: 29295823.

Ginsberg SD, Alldred MJ, Gunnam SM, Schiroli C, Lee SH, Morgello S, Fischer T. Expression profiling suggests microglial impairment in human immunodeficiency virus neuropathogenesis. Ann Neurol 2018 83(2):406-417 PMID: 29369399 .

Alldred MJ, Chao HM, Lee SH, Beilin J, Powers BE, Petkova E, Strupp BJ, Ginsberg SD. CA1 pyramidal neuron gene expression mosaics in the Ts65Dn murine model of Down syndrome amd Alzheimer's disease following maternal choline supplementation. Hippocampus. 2018 28(4):251-268 PMID: 29394516.

Tiernan CT, Ginsberg SD, He B, Ward SM, Guillozet-Bongaarts AL, Kanaan NM, Mufson EJ, Counts SE. Pretangle pathology within cholinergic nucleus basalis neurons coincides with neurotrophic and neurotransmitter receptor gene dysregulation during the progression of Alzheimer's disease. Neurobiol Dis. 2018 117:125-136 PMID: 29859871.

Mufson EJ, He B, Ginsberg SD, Carper BA, Bieler GS, Crawford F, Alvarez VE, Huber BR, Stein TD, McKee AC, Perez SE. Gene Profiling of Nucleus Basalis Tau Containing Neurons in Chronic Traumatic Encephalopathy: A Chronic Effects of Neurotrama Consortium Study. J Neurotrauma. 2018 35(11):1260-1271 PMID: 29338612.

Peng KY, Perez-Gonzalez R, Alldred MJ, Goulbourne CN, Morales-Corraliza J, Saito M, Saito M, Ginsberg SD, Mathews PM, Levy E. Apoliprotein E4 compromises brain exosome production. Brain 2019 142(1):163-175 doi: 10.1093/brain/awy289 PMID:30496349

Perez SE, Miguel JC, He B, Malek-Ahmadi M, Abrahamson EE, Ikonomovic MD, Lott I, Doran E, Alldred MJ, Ginsberg SD, Mufson EJ. Frontal cortex and striatal cellular and molecular pathobiology in individuals with Down syndrome with and without dementia. Acta Neuropathol. 2019 137: 413-436 PMID:30734106.

Kelley CM, Ginsberg SD, Alldred MJ, Strupp BJ, Mufson EJ. Maternal choline supplementation alters basal forebrain cholinergic neuron gene expression in the Ts65Dn mouse model of Down syndrome. Dev Neurobiol 2019. PMID: 31120189 PMCID: In Process. doi:10.1002/neu.22700.

Ginsberg SD, Malek-Ahmadi MH, Alldred MJ, Che S, Elarova, I, Chen Y, Jeanneteau F, Kranz TM, Chao MV, Counts SE, Mufson EJ. Selective decline of neurotrophin and neurotrophin receptor genes within CA1 pyramidal neurons and hippocampus proper: correlation with cognitive performance and neuropathology in mild cognitive impairment and Alzheimer's disease. Hippocampus 2019 29: 422-439 PMID:28888073. PMCID:PMC5844851 doi: 10.1002/hipo.22802.

Alldred MJ, Chao HM, Lee SH, Beilin J, Powers BE, Petkova E, Strupp BJ, Ginsberg SD. Long-term effects of maternal choline supplementation on CA1 pyramidal neuron gene expression in the Ts65Dn mouse model of Down syndrome and Alzheimer's disease. 2019 FASEB J. 33: 9871-9884. PMID:31180719.

Mufson EJ, Counts SE, Ginsberg SD, Mahady L, Perez SE, Massa SM, Longo FM, Ikonomovic MD. Nerve growth factor pathobiology during the progression of Alzheimer's disease. 2019 Front Neurosci. 13: 533. PMID:31312116.

Ginsberg SD, Malek-Ahmadi MH, Alldred MJ, Chen Y, Chen K, Chao MV, Counts SE, Mufson EJ. Brain-derived neurotrophic factor (BDNF) and TrKB hippocampal gene expression are putative predictors of neuritic plaque and neurofibrillary tangle pathology. 2019 Neurobiol Dis. Jul 23, 2019:104540 [Epub ahead of print]. PMID: 31349032.

Mufson, E.J., Counts, S.E., Ginsberg, S.D., Mahady, L., Perez, S.E., Massa, S.M., Longo, F.M., and Ikonomovic, M.D. Nerve growth factor pathobiology during the progression of Alzheimer’s disease. Front. Neurosci., 13: 533, 2019. PMID: 31312116. PMCID: PMC6613497. doi: 10.3389/fnins.2019.00533.

Kelley, C.M., Ginsberg, S.D., Alldred, M.J., Strupp, B.J., and Mufson, E.J. Maternal choline supplementation alters basal forebrain cholinergic neuron gene expression in the Ts65Dn mouse model of Down syndrome. Dev. Neurobiol., 79: 664-683, 2019. PMID: 31120189. PMCID: PMC6756931. doi: 10.1002/dneu.22700.

Ginsberg, S.D., Malek-Ahmadi, M.H., Alldred, M.J., Chen, Y., Chen, K., Chao, M.V., Counts, S.E., and Mufson, E.J. Brain-derived neurotrophic factor (BDNF) and TrkB hippocampal gene expression are putative predictors of neuritic plaque and neurofibrillary tangle pathology. Neurobiol. Dis., 132: 104540, 2019. PMID: 31349032. PMCID: PMC6834890. doi: 10.1016/j.nbd.2019.104540.

Cox, L.M. Schafer, M.J, Sohn, J., Vincentini, J., Weiner, H.L., Ginsberg, S.D., and Blaser, M.J. Calorie restriction slows age-related microbiota changes in an Alzheimer’s disease model in female mice. Sci. Rep., 9: 17904, 2019. PMID: 31784610. PMCID: PMC6884494. doi: 10.1038/s41598-019-54187-x.

Inda, M.C., Joshi, S., Wang, T., Bolaender, A., Gandu, S., Koren III, J., Che, A.Y., Taldone, T., Yan, P., Sun, W., Uddin, M., Panchal, P., Riolo, M., Shah, S., Barlas, A., Xu, K., Chan, L.Y.L., Gruzinova, A., Kishinevsky, S., Studer, L., Fossati, V., Noggle, S.A., White, J.R., de Stanchina, E., Sequeira, S., Anthoney, K.H., Steele, J.W., Manova-Todorova, K., Patil, S., Dunphy, M.P., Pillarsetty, N.V.K., Pereira, A.C., Erdjument-Bromage, H., Neubert, T.A., Rodina, A., Ginsberg, S.D., De Marco Garcia, N., Luo, W., and Chiosis, G.The epichaperome is a mediator of toxic hippocampal stress and leads to protein connectivity-based dysfunction. Nat. Commun., 11: 319, 2020. PMID: 31949159. PMCID: PMC6965647. doi: 10.1038/s41467-019-14082-5.

Roy, E.R., Wang, B., Wan, Y.W., Chiu, G.S., Cole, A.L., Yin, Z., Propson, N.E., Xu, Y., Jankowsky, J.L., Liu, Z., Lee, V.M., Trojanowski, J.Q., Ginsberg, S.D., Butovsky, O., Zheng, H., and Cao, W.: Type I interferon response drives neuroinflammation and synapse loss in Alzheimer disease. J. Clin. Invest., 130: 1912-1930, 2020. PMID: 31917687. PMCID: PMC7108898. doi: 10.1172/JCI133737.

Balla A, Ginsberg SD, Abbas AI, Sershen H, Javitt DC. Translational neurophysiological biomarkers of N-methyl-d-aspartate receptor dysfunction in serine racemase knockout mice. Biomark Neuropsychiatry. 2020 Jun;2:100019. doi: 10.1016/j.bionps.2020.100019. Epub 2020 Jun 18. PMID: 34308374; PMCID: PMC8301266.

He, B., Perez, S.E., Lee, S.H., Ginsberg, S.D., Malek-Ahmadi, M.H., and Mufson, E.J.: Expression profiling of precuneus layer III cathepsin D-immunopositive pyramidal neurons in mild cognitive impairment and Alzheimer's disease: Evidence for neuronal signaling vulnerability. J Comp Neurol., 528: 2748-2766, 2020. PMID: 32323319. PMCID: PMC7492791. doi: 10.1002/cne.24929.

D'Acunzo P, Pérez-González R, Kim Y, Hargash T, Miller C, Alldred MJ, Erdjument-Bromage H, Penikalapati SC, Pawlik M, Saito M, Saito M, Ginsberg SD, Neubert TA, Goulbourne CN, Levy E. Mitovesicles are a novel population of extracellular vesicles of mitochondrial origin altered in Down syndrome. Sci Adv. 2021 Feb 12;7(7):eabe5085. doi: 10.1126/sciadv.abe5085. PMID: 33579698; PMCID: PMC7880603.

Gautier MK, Ginsberg SD. A method for quantification of vesicular compartments within cells using 3D reconstructed confocal z-stacks: Comparison of ImageJ and Imaris to count early endosomes within basal forebrain cholinergic neurons. J Neurosci Methods. 2021 Feb 15;350:109038. doi: 10.1016/j.jneumeth.2020.109038. Epub 2020 Dec 15. PMID: 33338543; PMCID: PMC8026492.

Alldred MJ, Penikalapati SC, Lee SH, Heguy A, Roussos P, Ginsberg SD. Profiling Basal Forebrain Cholinergic Neurons Reveals a Molecular Basis for Vulnerability Within the Ts65Dn Model of Down Syndrome and Alzheimer's Disease. Mol Neurobiol. 2021 Oct;58(10):5141-5162. doi: 10.1007/s12035-021-02453-3. Epub 2021 Jul 14. PMID: 34263425.

[last updated 10.06.21]