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Article ; Online: Astrocytes Drive Divergent Metabolic Gene Expression in Humans and Chimpanzees.

Zintel, Trisha M / Pizzollo, Jason / Claypool, Christopher G / Babbitt, Courtney C

2023 Volume 16, Issue 1

Abstract: The human brain utilizes ∼20% of all of the body's metabolic resources, while chimpanzee brains use <10%. Although previous work shows significant differences in metabolic gene expression between the brains of primates, we have yet to fully resolve the ... ...

Abstract	The human brain utilizes ∼20% of all of the body's metabolic resources, while chimpanzee brains use <10%. Although previous work shows significant differences in metabolic gene expression between the brains of primates, we have yet to fully resolve the contribution of distinct brain cell types. To investigate cell type-specific interspecies differences in brain gene expression, we conducted RNA-seq on neural progenitor cells, neurons, and astrocytes generated from induced pluripotent stem cells from humans and chimpanzees. Interspecies differential expression analyses revealed that twice as many genes exhibit differential expression in astrocytes (12.2% of all genes expressed) than neurons (5.8%). Pathway enrichment analyses determined that astrocytes, rather than neurons, diverged in expression of glucose and lactate transmembrane transport, as well as pyruvate processing and oxidative phosphorylation. These findings suggest that astrocytes may have contributed significantly to the evolution of greater brain glucose metabolism with proximity to humans.
MeSH term(s)	Animals ; Humans ; Astrocytes/metabolism ; Pan troglodytes/genetics ; Neurons/metabolism ; Brain/metabolism ; Gene Expression
Language	English
Publishing date	2023-12-30
Publishing country	England
Document type	Journal Article
ZDB-ID	2495328-3
ISSN	1759-6653 ; 1759-6653
ISSN (online)	1759-6653
ISSN	1759-6653
DOI	10.1093/gbe/evad239
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Article ; Online: Differentially Active and Conserved Neural Enhancers Define Two Forms of Adaptive Noncoding Evolution in Humans.

Pizzollo, Jason / Zintel, Trisha M / Babbitt, Courtney C

Genome biology and evolution

2022 Volume 14, Issue 8

Abstract: The human and chimpanzee genomes are strikingly similar, but our neural phenotypes are very different. Many of these differences are likely driven by changes in gene expression, and some of those changes may have been adaptive during human evolution. Yet, ...

Abstract	The human and chimpanzee genomes are strikingly similar, but our neural phenotypes are very different. Many of these differences are likely driven by changes in gene expression, and some of those changes may have been adaptive during human evolution. Yet, the relative contributions of positive selection on regulatory regions or other functional regulatory changes are unclear. Where are these changes located throughout the human genome? Are functional regulatory changes near genes or are they in distal enhancer regions? In this study, we experimentally combined both human and chimpanzee cis-regulatory elements (CREs) that showed either (1) signs of accelerated evolution in humans or (2) that have been shown to be active in the human brain. Using a massively parallel reporter assay, we tested the ability of orthologous human and chimpanzee CREs to activate transcription in induced pluripotent stem-cell-derived neural progenitor cells and neurons. With this assay, we identified 179 CREs with differential activity between human and chimpanzee; in contrast, we found 722 CREs with signs of positive selection in humans. Selection and differentially expressed CREs strikingly differ in level of expression, size, and genomic location. We found a subset of 69 CREs in loci with genetic variants associated with neuropsychiatric diseases, which underscores the consequence of regulatory activity in these loci for proper neural development and function. By combining CREs that either experienced recent selection in humans or CREs that are functional brain enhancers, presents a novel way of studying the evolution of noncoding elements that contribute to human neural phenotypes.
MeSH term(s)	Enhancer Elements, Genetic ; Genome ; Genomics ; Humans ; Regulatory Sequences, Nucleic Acid
Language	English
Publishing date	2022-07-22
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2495328-3
ISSN	1759-6653 ; 1759-6653
ISSN (online)	1759-6653
ISSN	1759-6653
DOI	10.1093/gbe/evac108
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Article ; Online: Metabolic changes in human brain evolution.

Bauernfeind, Amy L / Babbitt, Courtney C

Evolutionary anthropology

2020 Volume 29, Issue 4, Page(s) 201–211

Abstract: Because the human brain is considerably larger than those of other primates, it is not surprising that its energy requirements would far exceed that of any of the species within the order. Recently, the development of stem cell technologies and single- ... ...

Abstract	Because the human brain is considerably larger than those of other primates, it is not surprising that its energy requirements would far exceed that of any of the species within the order. Recently, the development of stem cell technologies and single-cell transcriptomics provides novel ways to address the question of what specific genomic changes underlie the human brain's unique phenotype. In this review, we consider what is currently known about human brain metabolism using a variety of methods from brain imaging and stereology to transcriptomics. Next, we examine novel opportunities that stem cell technologies and single-cell transcriptomics provide to further our knowledge of human brain energetics. These new experimental approaches provide the ability to elucidate the functional effects of changes in genetic sequence and expression levels that potentially had a profound impact on the evolution of the human brain.
MeSH term(s)	Biological Evolution ; Brain/metabolism ; Gene Expression Profiling/methods ; Humans ; Neuroimaging/methods ; Phenotype ; Single-Cell Analysis/methods ; Stem Cell Research
Language	English
Publishing date	2020-04-24
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	1131718-8
ISSN	1520-6505 ; 1060-1538
ISSN (online)	1520-6505
ISSN	1060-1538
DOI	10.1002/evan.21831
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Article ; Online: Genetic diversity underlying behavioral plasticity in human adaptation.

Bauernfeind, Amy L / Babbitt, Courtney C

Progress in brain research

2019 Volume 250, Page(s) 41–58

Abstract: The human brain is notably different from that of other primate species by its size and structure, in addition to its behavioral output. As we seek to understand how the human brain has evolved, many researchers have turned to genomics to help elucidate ... ...

Abstract	The human brain is notably different from that of other primate species by its size and structure, in addition to its behavioral output. As we seek to understand how the human brain has evolved, many researchers have turned to genomics to help elucidate the biological basis for uniqueness of the human brain. When considering the molecular evolution of the human brain, a common misconception is that molecular evolution should be "unidirectional"-progressing along a single trajectory with the human brain as the ultimate goal. This outlook fails to acknowledge the importance of variability in the evolutionary process. In this review, we review what we know about inter- and intraspecific molecular diversity in the human brain arising from heritable and non-heritable sources. We note that genetic substitutions may not be optimal in brain evolution due to pleiotropic effects. Instead, we focus on other sources of molecular diversity including gene duplications, copy number variations, and transcriptional regulation. With recent advancements in the field of single-cell genomics, we explore what is currently known about gene expression at the cellular level and highlight opportunities to advance our understanding of human uniqueness at the neuronal level.
MeSH term(s)	Adaptation, Physiological ; Adaptation, Psychological ; Animals ; Brain ; Gene Expression ; Genetic Variation ; Humans ; Neuronal Plasticity
Language	English
Publishing date	2019-07-23
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ISSN	1875-7855 ; 0079-6123
ISSN (online)	1875-7855
ISSN	0079-6123
DOI	10.1016/bs.pbr.2019.06.002
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Article ; Online: Immune System Promiscuity in Human and Nonhuman Primate Evolution.

Brinkworth, Jessica F / Babbitt, Courtney C

Human biology

2019 Volume 90, Issue 4, Page(s) 251–269

Abstract: Many genes that respond to infection have functions outside of immunity and have been found to be under natural selection. Pathogens may therefore incidentally alter nonimmune physiology through engagement with immune system genes. This raises a logical ... ...

Abstract	Many genes that respond to infection have functions outside of immunity and have been found to be under natural selection. Pathogens may therefore incidentally alter nonimmune physiology through engagement with immune system genes. This raises a logical question of how genetically promiscuous the immune system is, here defined as how heavily cross-referenced the immune system is into other physiological systems. This work examined immune gene promiscuity across physiological systems in primates by assessing the baseline (unperturbed) expression of key tissue and cell types for differences, and primate genomes for signatures of selection. These efforts revealed "immune" gene expression to be cross-referenced extensively in other physiological systems in primates. When immune and nonimmune tissues diverge in expression, the differentially expressed genes at baseline are enriched for cell biological activities not immediately identifiable as immune function based. Individual comparisons of immune and nonimmune tissues in primates revealed low divergence in gene expression between tissues, with the exception of whole blood. Immune gene promiscuity increases over evolutionary time, with hominoids exhibiting the most cross-referencing of such genes among primates. An assessment of genetic sequences also found positive selection in the coding regions of differentially expressed genes between tissues functionally associated with immunity. This suggests that, with increasing promiscuity, divergent gene expression between the immune system and other physiological systems tends to be adaptive and enriched for immune functions in hominoids.
MeSH term(s)	Animals ; Evolution, Molecular ; Humans ; Immune System ; Phylogeny ; Primates/genetics ; Selection, Genetic
Language	English
Publishing date	2019-11-12
Publishing country	United States
Document type	Journal Article
ZDB-ID	1116-2
ISSN	1534-6617 ; 0018-7143
ISSN (online)	1534-6617
ISSN	0018-7143
DOI	10.13110/humanbiology.90.4.01
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Article ; Online: White-throated sparrow (

Elowe, Cory R / Babbitt, Courtney / Gerson, Alexander R

Physiological genomics

2023 Volume 55, Issue 11, Page(s) 544–556

Abstract: Migratory songbirds undertake challenging journeys to reach their breeding grounds each spring. They accomplish these nonstop flapping feats of endurance through a suite of physiological changes, including the development of substantial fat stores and ... ...

Abstract	Migratory songbirds undertake challenging journeys to reach their breeding grounds each spring. They accomplish these nonstop flapping feats of endurance through a suite of physiological changes, including the development of substantial fat stores and flight muscle hypertrophy and an increased capacity for fat catabolism. In addition, migratory birds may show large reductions in organ masses during flight, including the flight muscle and liver, which they must rapidly rebuild during their migratory stopover before replenishing their fat stores. However, the molecular basis of this capacity for rapid tissue remodeling and energetic output has not been thoroughly investigated. We performed RNA-sequencing analysis of the liver and pectoralis flight muscle of captive white-throated sparrows in experimentally photostimulated migratory and nonmigratory condition to explore the mechanisms of seasonal change to metabolism and tissue mass regulation that may facilitate these migratory journeys. Based on transcriptional changes, we propose that tissue-specific adjustments in preparation for migration may alleviate the damaging effects of long-duration activity, including a potential increase to the inflammatory response in the muscle. Furthermore, we hypothesize that seasonal hypertrophy balances satellite cell recruitment and apoptosis, while little evidence appeared in the transcriptome to support myostatin-, insulin-like growth factor 1-, and mammalian target of rapamycin-mediated pathways for muscle growth. These findings can encourage more targeted molecular studies on the unique integration of pathways that we find in the development of the migratory endurance phenotype in songbirds.
MeSH term(s)	Animals ; Sparrows/genetics ; Sparrows/metabolism ; Transcriptome/genetics ; Liver ; Muscles ; Hypertrophy ; Seasons ; Mammals/genetics
Language	English
Publishing date	2023-09-11
Publishing country	United States
Document type	Journal Article
ZDB-ID	2038823-8
ISSN	1531-2267 ; 1094-8341
ISSN (online)	1531-2267
ISSN	1094-8341
DOI	10.1152/physiolgenomics.00018.2023
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Zs.A 5697: Show issues

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Article ; Online: Tempo and mode of gene expression evolution in the brain across primates.

Rickelton, Katherine / Zintel, Trisha M / Pizzollo, Jason / Miller, Emily / Ely, John J / Raghanti, Mary Ann / Hopkins, William D / Hof, Patrick R / Sherwood, Chet C / Bauernfeind, Amy L / Babbitt, Courtney C

eLife

2024 Volume 13

Abstract: Primate evolution has led to a remarkable diversity of behavioral specializations and pronounced brain size variation among species (Barton, 2012; DeCasien and Higham, 2019; Powell et al., 2017). Gene expression provides a promising opportunity for ... ...

Abstract	Primate evolution has led to a remarkable diversity of behavioral specializations and pronounced brain size variation among species (Barton, 2012; DeCasien and Higham, 2019; Powell et al., 2017). Gene expression provides a promising opportunity for studying the molecular basis of brain evolution, but it has been explored in very few primate species to date (e.g. Khaitovich et al., 2005; Khrameeva et al., 2020; Ma et al., 2022; Somel et al., 2009). To understand the landscape of gene expression evolution across the primate lineage, we generated and analyzed RNA-seq data from four brain regions in an unprecedented eighteen species. Here, we show a remarkable level of variation in gene expression among hominid species, including humans and chimpanzees, despite their relatively recent divergence time from other primates. We found that individual genes display a wide range of expression dynamics across evolutionary time reflective of the diverse selection pressures acting on genes within primate brain tissue. Using our samples that represent a 190-fold difference in primate brain size, we identified genes with variation in expression most correlated with brain size. Our study extensively broadens the phylogenetic context of what is known about the molecular evolution of the brain across primates and identifies novel candidate genes for the study of genetic regulation of brain evolution.
MeSH term(s)	Humans ; Animals ; Phylogeny ; Primates/genetics ; Brain/physiology ; Evolution, Molecular ; Pan troglodytes/genetics ; Gene Expression ; Biological Evolution
Language	English
Publishing date	2024-01-26
Publishing country	England
Document type	Journal Article
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.70276
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Article ; Online: The predictive nature of transcript expression levels on protein expression in adult human brain.

Bauernfeind, Amy L / Babbitt, Courtney C

BMC genomics

2017 Volume 18, Issue 1, Page(s) 322

Abstract: Background: Next generation sequencing methods are the gold standard for evaluating expression of the transcriptome. When determining the biological implications of such studies, the assumption is often made that transcript expression levels correspond ... ...

Abstract	Background: Next generation sequencing methods are the gold standard for evaluating expression of the transcriptome. When determining the biological implications of such studies, the assumption is often made that transcript expression levels correspond to protein levels in a meaningful way. However, the strength of the overall correlation between transcript and protein expression is inconsistent, particularly in brain samples. Results: Following high-throughput transcriptomic (RNA-Seq) and proteomic (liquid chromatography coupled with tandem mass spectrometry) analyses of adult human brain samples, we compared the correlation in the expression of transcripts and proteins that support various biological processes, molecular functions, and that are located in different areas of the cell. Although most categories of transcripts have extremely weak predictive value for the expression of their associated proteins (R Conclusions: The predictive value of transcript expression for corresponding proteins is variable in human brain samples, reflecting the complex regulation of protein expression. However, we found that transcriptomic analyses are appropriate for assessing the expression levels of certain classes of proteins, including those that modify proteins, such as kinases and phosphatases, regulate metabolic and synaptic activity, or are associated with a cellular membrane. These findings can be used to guide the interpretation of gene expression results from primate brain samples.
Language	English
Publishing date	2017-04-24
Publishing country	England
Document type	Journal Article
ISSN	1471-2164
ISSN (online)	1471-2164
DOI	10.1186/s12864-017-3674-x
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Article ; Online: TATA-binding associated factors have distinct roles during early mammalian development.

He, Xinjian Doris / Phillips, Shelby / Hioki, Kaito / Majhi, Prabin Dhangada / Babbitt, Courtney / Tremblay, Kimberly D / Pobezinsky, Leonid A / Mager, Jesse

Developmental biology

2024 Volume 511, Page(s) 53–62

Abstract: Early embryonic development is a finely orchestrated process that requires precise regulation of gene expression coordinated with morphogenetic events. TATA-box binding protein-associated factors (TAFs), integral components of transcription initiation ... ...

Abstract	Early embryonic development is a finely orchestrated process that requires precise regulation of gene expression coordinated with morphogenetic events. TATA-box binding protein-associated factors (TAFs), integral components of transcription initiation coactivators like TFIID and SAGA, play a crucial role in this intricate process. Here we show that disruptions in TAF5, TAF12 and TAF13 individually lead to embryonic lethality in the mouse, resulting in overlapping yet distinct phenotypes. Taf5 and Taf12 mutant embryos exhibited a failure to implant post-blastocyst formation, and Taf5 mutants have aberrant lineage specification within the inner cell mass. In contrast, Taf13 mutant embryos successfully implant and form egg-cylinder stages but fail to initiate gastrulation. Strikingly, we observed a depletion of pluripotency factors in TAF13-deficient embryos, including OCT4, NANOG and SOX2, highlighting an indispensable role of TAF13 in maintaining pluripotency. Transcriptomic analysis revealed distinct gene targets affected by the loss of TAF5, TAF12 and TAF13. Thus, we propose that TAF5, TAF12 and TAF13 convey locus specificity to the TFIID complex throughout the mouse genome.
Language	English
Publishing date	2024-04-07
Publishing country	United States
Document type	Journal Article
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2024.04.002
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Zs.B 508: Show issues

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Article ; Online: The appropriation of glucose through primate neurodevelopment.

Bauernfeind, Amy L / Babbitt, Courtney C

Journal of human evolution

2014 Volume 77, Page(s) 132–140

Abstract: The human brain is considerably larger and more energetically costly than that of other primate species. As such, discovering how human ancestors were able to provide sufficient energy to their brains is a central theme in the study of hominin evolution. ...

Abstract	The human brain is considerably larger and more energetically costly than that of other primate species. As such, discovering how human ancestors were able to provide sufficient energy to their brains is a central theme in the study of hominin evolution. However, many discussions of metabolism frequently omit the different ways in which energy, primarily glucose, is used once made available to the brain. In this review, we discuss two glucose metabolic pathways, oxidative phosphorylation and aerobic glycolysis, and their respective contributions to the energetic and anabolic budgets of the brain. While oxidative phosphorylation is a more efficient producer of energy, aerobic glycolysis contributes essential molecules for the growth of the brain and maintaining the structure of its cells. Although both pathways occur in the brain throughout the lifetime, aerobic glycolysis is a critical pathway during development, and oxidative phosphorylation is highest during adulthood. We outline how elevated levels of aerobic glycolysis may support the protracted neurodevelopmental sequence of humans compared with other primates. Finally, we review the genetic evidence for differences in metabolic function in the brains of primates and explore genes that may provide insight into how glucose metabolism may differ across species.
MeSH term(s)	Animals ; Biological Evolution ; Brain/metabolism ; Glucose/metabolism ; Glycolysis/physiology ; Humans ; Macaca/physiology ; Oxidative Phosphorylation ; Pan troglodytes/physiology
Chemical Substances	Glucose (IY9XDZ35W2)
Language	English
Publishing date	2014-12
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	120141-4
ISSN	1095-8606 ; 0047-2484
ISSN (online)	1095-8606
ISSN	0047-2484
DOI	10.1016/j.jhevol.2014.05.016
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