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News Article | November 3, 2016
Site: www.eurekalert.org

LA JOLLA -- (Nov. 3, 2016) We can tell when plants need water: their leaves droop and they start to look dry. But what's happening on a molecular level? Scientists at the Salk Institute have made a leap forward in answering that question, which could be critical to helping agriculture adapt to drought and other climate-related stressors. The new research suggests that in the face of environmental hardship, plants employ a small group of proteins that act as conductors to manage their complex responses to stress. The results, which are detailed in the November 4 issue of Science, may help in developing new technologies to optimize water use in plants. "A plant's response to a stressor is a highly complex process at the molecular level, with hundreds of genes involved," says senior author Joseph Ecker, a Howard Hughes Medical Institute Investigator, professor and director of Salk's Genomic Analysis Laboratory and holder of the Salk International Council Chair in Genetics. "We've discovered key conductors in this molecular symphony, which may offer clues to helping plants better tolerate stressors such as drought in the face of climate change. If you can control one of these conductors, you control all of the genes that follow its lead." How well a plant responds to stress can determine whether it survives and thrives or succumbs to a threat. Just as humans have hormones such as adrenaline that help us cope with threats, plants have a few key hormones that allow them to respond to stressors in their environment. One of these is abscisic acid (ABA), a plant hormone involved in seed development and water optimization. When water is scarce or salinity is high, roots and leaves produce ABA. Although the hormone is understood to impact a plant's stress response, scientists have known very little about what happens globally after it is released. "Just a few dozen regulatory proteins dictate the expression of hundreds if not thousands of genes," says Liang Song, a research associate in Salk's Plant Biology Laboratory and the paper's first author. "By understanding what those master regulators are and how they work, we can better understand, and potentially modulate, the stress response." In their study, the Salk team tracked real-time changes in plant genetic activity in response to ABA and identified a handful of these master proteins that govern responses to a wide range of external stressors, including drought. Using a technique that maps where these regulatory proteins bind to DNA, the team defined key factors that coordinate gene expression, allowing for an efficient cellular response to changing conditions. The Salk team focused on candidate regulatory proteins known to respond to ABA. They exposed 3-day-old seedlings of the reference plant Arabidopsis thaliana to abscisic acid and checked gene expression at regular time points over 60 hours. In the process, they amassed 122 datasets involving 33,602 genes, 3,061 of which were expressed at differing levels for at least one time point. Analysis of the data revealed a hierarchy of control, with some regulatory proteins ranking as top contributors to gene expression. Intriguingly, a snapshot of protein binding patterns at a particular time point can largely explain gene expression over a large span of time. Together, these dynamics suggest a coordinated genome-wide response to environmental triggers. "With this network view, we can see that some of these components are targeted by the same master regulator proteins, which suggests precise and coordinated genetic control," says Song. "This could be important for agricultural purposes because regulating one gene could in turn stimulate or suppress another whole set of genes, allowing for a comprehensive design of interventions." The results mirror those of a 2013 study by the Ecker lab on the plant hormone ethylene, suggesting that such coordinated and hierarchical control of genetic activity may be common to flowering plants. Other authors on the paper include: Shao-shan Carol Huang, Rosa Castanon, Joseph R. Nery, Huaming Chen, Marina Watanabe and Jerushah Thomas of the Salk Institute; and Aaron Wise and Ziv Bar-Joseph of Carnegie Mellon University. The work was funded by the Howard Hughes Medical Institute, the Gordon and Betty Moore Foundation (GBMF 3034), the National Science Foundation (MCB-1024999 and DBI-1356505), the National Institutes of Health (U01 HL122626-01) and by a Salk Pioneer Postdoctoral Fellowship. Song is also supported by a Salk Women & Science award. About the Salk Institute for Biological Studies Every cure has a starting point. The Salk Institute embodies Jonas Salk's mission to dare to make dreams into reality. Its internationally renowned and award-winning scientists explore the very foundations of life, seeking new understandings in neuroscience, genetics, immunology and more. The Institute is an independent nonprofit organization and architectural landmark: small by choice, intimate by nature and fearless in the face of any challenge. Be it cancer or Alzheimer's, aging or diabetes, Salk is where cures begin. Learn more at: salk.edu.


News Article | December 20, 2016
Site: www.eurekalert.org

LA JOLLA -- (Dec. 20, 2016) When you build models, whether ships or cars, you want them to be as much like the real deal as possible. This quality is even more crucial for building model organs, because disease treatments developed from these models have to be safe and effective for humans. Now, scientists at the Salk Institute have studied a 3D "mini-brain" grown from human stem cells and found it to be structurally and functionally more similar to real brains than the 2D models in widespread use. The discovery, appearing in the December 20, 2016, issue of Cell Reports, indicates that the new model could better help scientists understand brain development as well as neurological diseases like Alzheimer's or schizophrenia. "Being able to grow human brain cells as miniature three-dimensional organs was a real breakthrough," says senior author Joseph Ecker, a Howard Hughes Medical Institute Investigator and professor and director of Salk's Genomic Analysis Laboratory. "Now that we have a structurally realistic model, we can start to ask whether it is also functionally realistic, by looking at its genetic and epigenetic features." For years, cell biologists have been chemically prompting embryonic stem cells in petri dishes to develop ("differentiate") into various types of brain cells. While researchers are able to glean a tremendous amount of information from these single layers of cells, the obvious limitation is that real brain tissue isn't two-dimensional. In 2013, European investigators developed a method to grow embryonic brain cells in 3D gels, where they begin to differentiate into realistic layers like an actual brain. However, it was unknown how faithfully these lab-grown mini-brains, called cerebral organoids (COs), look and behave like real brains until now. Collaborating with the European lab that developed the protocol for growing COs, Ecker's lab compared COs in early stages of brain development to real brain tissue at the same developmental stage. "Our work demonstrates the remarkable degree to which human brain development can be recapitulated in a dish in cerebral organoids," says Juergen Knoblich, co-senior author of the new paper and head of the European lab. To create COs for analysis, the teams used a human embryonic cell line called H9, adding the right chemicals to induce the cells down a neurodevelopmental pathway for 60 days. They then analyzed the COs' epigenetics, the pattern of chemical markers on DNA responsible for activating or silencing genes. Cells' epigenomes -- which are influenced by environmental factors like diet or stress--have been increasingly tied to development and disease (like schizophrenia). "No one has done epigenome sequencing for cerebral organoids before," says Chongyuan Luo, a Salk research associate and first author of the paper. "This kind of assessment is so important for understanding brain development, especially if we're eventually going to use these tissues for neurological therapies." The team compared their results both to age-matched real tissue from the National Institutes of Health NeuroBioBank and other researchers' 2D brain-model data. They found that COs were much more like real brain tissue than 2D models in the degree of differentiation the cells achieved and in their gene expression; in other words, COs develop along very similar early-developmental timelines as real brains, although they do not mature to the same level. When it came to epigenetics, however, both 3D and 2D models had similar aberrant patterns, which seem to be common to all cells grown in culture versus inside the brain. What this difference means is not entirely clear but, because it is so striking, Ecker suggests it could be a useful measure of how similar a model is to the real brain. "Our findings show that cerebral organoids as a 3D model of brain function are getting closer to a real brain than 2D models, so perhaps by using the epigenetic pattern as a gauge we can get even closer," says Ecker, who also holds the Salk International Council Chair in Genetics. Other authors included: Rosa Castanon and Joseph R. Nery of the Salk Institute, and Madeline A. Lancaster of the Institute of Molecular Biotechnology of the Austrian Academy of Science. The work was funded by the Howard Hughes Medical Institute, the Gordon and Betty Moore Foundation, the Austrian Academy of Sciences, the Austrian Science Fund, the European Research Council, a Marie Curie postdoctoral fellowship and the Medical Research Council. About the Salk Institute for Biological Studies: Every cure has a starting point. The Salk Institute embodies Jonas Salk's mission to dare to make dreams into reality. Its internationally renowned and award-winning scientists explore the very foundations of life, seeking new understandings in neuroscience, genetics, immunology, plant biology and more. The Institute is an independent nonprofit organization and architectural landmark: small by choice, intimate by nature and fearless in the face of any challenge. Be it cancer or Alzheimer's, aging or diabetes, Salk is where cures begin. Learn more at: salk.edu.


News Article | November 10, 2016
Site: www.eurekalert.org

PORTLAND, Ore, and LA JOLLA, Calif. - Families struggling with infertility or a genetic predisposition for debilitating mitochondrial diseases may someday benefit from a new breakthrough led by scientists at OHSU and the Salk Institute for Biological Studies. In a study to be published Thursday, Nov. 10 in the journal Cell Stem Cell, researchers discovered it's possible to regenerate human eggs or oocytes - the cellular beginning of an embryo - by making use of genetic material that normally goes to waste. This DNA comes from small cells called polar bodies that form off of eggs and contain the same genetic material as in a woman's egg nucleus. Until now, polar bodies had never been shown to be potentially useful for generating functional human eggs for fertility treatments. In the study, scientists successfully transplanted a polar body from a woman's developing oocyte into the cytoplasm of a donor oocyte stripped of its nucleus. Though the technique could be years away from progressing to clinical trials, the advancement eventually could be significant for women of advanced maternal age. One recent survey showed that the average age of first-time mothers increased in the United States from 21.4 years in 1970 to 25.0 years in 2006. "We know that fertility declines as women get older," said Shoukhrat Mitalipov, Ph.D., co- senior author and director of the OHSU Center for Embryonic Cell and Gene Therapy. "This is potentially a way to double the number of eggs we're able to get from one session of in vitro fertilization." "Although it was only possible to examine a limited number of lines, from the point of view of epigenomic profiles, the quality of polar body-derived embryonic cells looks quite promising," says co-senior author Joseph Ecker, Ph.D., Salk professor and director of the Genomic Analysis Laboratory. By rescuing polar bodies that would otherwise simply bud off the developing oocyte, researchers were able to form additional oocytes genetically related to the mother through nuclear transfer. When fertilized with sperm, the new oocytes developed into viable embryos. None of the embryos were implanted to carry out an actual pregnancy. "Normally, polar bodies disintegrate and disappear during egg development," said co-first author Hong Ma, M.D., Ph.D., with OHSU's Center for Embryonic Cell and Gene Therapy. "We were able to recycle them. We hope that by doing this, we can double the number of patient eggs available for in vitro fertilization." "This is the first investigation into the surprising viability of human polar bodies and it reveals a new source of previously discarded genetic material to study," says Ryan O'Neil, co-first author and Salk researcher. In addition to potentially benefitting women of advanced maternal age, the technique may present another opportunity to help women known to have mutations in their mitochondria, the tiny powerhouses inside nearly every cell of the body. Mutations in mitochondria can result in debilitating forms of disease in children. "This new technique maximizes the chances of families having a child through in vitro fertilization free of genetic mutations," Mitalipov said. Mitalipov previously developed a mitochondrial replacement therapy involving the implantation of patient's egg nucleus - or spindle - into a healthy donated egg stripped of its original nucleus. Mitalipov also has successfully demonstrated the spindle-transfer technique in the healthy offspring of rhesus macaque monkeys. In addition to Mitalipov, Ecker, Ma and O'Neil, authors of the study include Ryan C. O'Neil and Yupeng He, of the Genomic Analysis Laboratory at the Salk Institute and the Bioinformatics Program at the University of California and San Diego; Joseph R. Ecker, Ph.D., of the Salk Institute and Howard Hughes Medical Institute; Nuria Marti Gutierrez, Eunju Kang, Yeonmi Lee, Tomonari Hayama, M.D., Ph.D., Amy Koski, Rebecca Tippner-Hedges, Riffat Ahmed, Crystal Van Dyken, Ying Li, and Don P. Wolf, Ph.D., of the OHSU Center for Embryonic Cell and Gene Therapy; Manoj Hariharan, Ph.D., Zhuzhu Z. Zhang, Ph.D., Joseph Nery and Rosa Castanon, of the Salk Institute; Susan Olson, Ph.D., of the OHSU Department of Molecular and Medical Genetics; David Battaglia, Ph.D., H.C.L.D., David M. Lee, M.D., Diana H. Wu, M.D., and Paula Amato, M.D., of the OHSU Department of Obstetrics and Gynecology; and Cengiz Cinnioglu, Ph.D., and Refik Kayali, Ph.D., of IviGen Los Angeles.


Kurihara Y.,Plant Biology Laboratory | Schmitz R.J.,Plant Biology Laboratory | Schmitz R.J.,Genomic Analysis Laboratory | Nery J.R.,Genomic Analysis Laboratory | And 9 more authors.
G3: Genes, Genomes, Genetics | Year: 2012

Eukaryotes possess several RNA surveillance mechanisms that prevent undesirable aberrant RNAs from accumulating. Arabidopsis XRN2, XRN3, and XRN4 are three orthologs of the yeast 59-to-39 exoribonuclease, Rat1/Xrn2, that function in multiple RNA decay pathways. XRN activity is maintained by FIERY1 (FRY1), which converts the XRN inhibitor, adenosine 39, 59-bisphosphate (PAP), into 59AMP. To identify the roles of XRNs and FRY1 in suppression of non-coding RNAs, strand-specific genome-wide tiling arrays and deep strand-specific RNA-Seq analyses were carried out in fry1 and xrn single and double mutants. In fry1-6, about 2000 new transcripts were identified that extended the 39 end of specific mRNAs; many of these were also observed in genotypes that possess the xrn3-3 mutation, a partial loss-of-function allele. Mutations in XRN2 and XRN4 in combination with xrn3-3 revealed only a minor effect on 39 extensions, indicating that these genes may be partially redundant with XRN3. We also observed the accumulation of 39 remnants of many DCL1-processed microRNA (miRNA) precursors in fry1-6 and xrn3-3. These findings suggest that XRN3, in combination with FRY1, is required to prevent the accumulation of 39 extensions that arise from thousands of mRNA and miRNA precursor transcripts. © 2012 Kurihara et al.


News Article | November 3, 2016
Site: phys.org

Scientists at the Salk Institute have made a leap forward in answering that question, which could be critical to helping agriculture adapt to drought and other climate-related stressors. The new research suggests that in the face of environmental hardship, plants employ a small group of proteins that act as conductors to manage their complex responses to stress. The results, which are detailed in the November 4 issue of Science, may help in developing new technologies to optimize water use in plants. "A plant's response to a stressor is a highly complex process at the molecular level, with hundreds of genes involved," says senior author Joseph Ecker, a Howard Hughes Medical Institute Investigator, professor and director of Salk's Genomic Analysis Laboratory and holder of the Salk International Council Chair in Genetics. "We've discovered key conductors in this molecular symphony, which may offer clues to helping plants better tolerate stressors such as drought in the face of climate change. If you can control one of these conductors, you control all of the genes that follow its lead." How well a plant responds to stress can determine whether it survives and thrives or succumbs to a threat. Just as humans have hormones such as adrenaline that help us cope with threats, plants have a few key hormones that allow them to respond to stressors in their environment. One of these is abscisic acid (ABA), a plant hormone involved in seed development and water optimization. When water is scarce or salinity is high, roots and leaves produce ABA. Although the hormone is understood to impact a plant's stress response, scientists have known very little about what happens globally after it is released. "Just a few dozen regulatory proteins dictate the expression of hundreds if not thousands of genes," says Liang Song, a research associate in Salk's Plant Biology Laboratory and the paper's first author. "By understanding what those master regulators are and how they work, we can better understand, and potentially modulate, the stress response." In their study, the Salk team tracked real-time changes in plant genetic activity in response to ABA and identified a handful of these master proteins that govern responses to a wide range of external stressors, including drought. Using a technique that maps where these regulatory proteins bind to DNA, the team defined key factors that coordinate gene expression, allowing for an efficient cellular response to changing conditions. The Salk team focused on candidate regulatory proteins known to respond to ABA. They exposed 3-day-old seedlings of the reference plant Arabidopsis thaliana to abscisic acid and checked gene expression at regular time points over 60 hours. In the process, they amassed 122 datasets involving 33,602 genes, 3,061 of which were expressed at differing levels for at least one time point. Analysis of the data revealed a hierarchy of control, with some regulatory proteins ranking as top contributors to gene expression. Intriguingly, a snapshot of protein binding patterns at a particular time point can largely explain gene expression over a large span of time. Together, these dynamics suggest a coordinated genome-wide response to environmental triggers. "With this network view, we can see that some of these components are targeted by the same master regulator proteins, which suggests precise and coordinated genetic control," says Song. "This could be important for agricultural purposes because regulating one gene could in turn stimulate or suppress another whole set of genes, allowing for a comprehensive design of interventions." The results mirror those of a 2013 study by the Ecker lab on the plant hormone ethylene, suggesting that such coordinated and hierarchical control of genetic activity may be common to flowering plants. Explore further: Study reveals which genes are critical to a plant's response to drought


News Article | November 4, 2016
Site: www.sciencedaily.com

We can tell when plants need water: their leaves droop and they start to look dry. But what's happening on a molecular level? Scientists at the Salk Institute have made a leap forward in answering that question, which could be critical to helping agriculture adapt to drought and other climate-related stressors. The new research suggests that in the face of environmental hardship, plants employ a small group of proteins that act as conductors to manage their complex responses to stress. The results, which are detailed in the November 4 issue of Science, may help in developing new technologies to optimize water use in plants. "A plant's response to a stressor is a highly complex process at the molecular level, with hundreds of genes involved," says senior author Joseph Ecker, a Howard Hughes Medical Institute Investigator, professor and director of Salk's Genomic Analysis Laboratory and holder of the Salk International Council Chair in Genetics. "We've discovered key conductors in this molecular symphony, which may offer clues to helping plants better tolerate stressors such as drought in the face of climate change. If you can control one of these conductors, you control all of the genes that follow its lead." How well a plant responds to stress can determine whether it survives and thrives or succumbs to a threat. Just as humans have hormones such as adrenaline that help us cope with threats, plants have a few key hormones that allow them to respond to stressors in their environment. One of these is abscisic acid (ABA), a plant hormone involved in seed development and water optimization. When water is scarce or salinity is high, roots and leaves produce ABA. Although the hormone is understood to impact a plant's stress response, scientists have known very little about what happens globally after it is released. "Just a few dozen regulatory proteins dictate the expression of hundreds if not thousands of genes," says Liang Song, a research associate in Salk's Plant Biology Laboratory and the paper's first author. "By understanding what those master regulators are and how they work, we can better understand, and potentially modulate, the stress response." In their study, the Salk team tracked real-time changes in plant genetic activity in response to ABA and identified a handful of these master proteins that govern responses to a wide range of external stressors, including drought. Using a technique that maps where these regulatory proteins bind to DNA, the team defined key factors that coordinate gene expression, allowing for an efficient cellular response to changing conditions. The Salk team focused on candidate regulatory proteins known to respond to ABA. They exposed 3-day-old seedlings of the reference plant Arabidopsis thaliana to abscisic acid and checked gene expression at regular time points over 60 hours. In the process, they amassed 122 datasets involving 33,602 genes, 3,061 of which were expressed at differing levels for at least one time point. Analysis of the data revealed a hierarchy of control, with some regulatory proteins ranking as top contributors to gene expression. Intriguingly, a snapshot of protein binding patterns at a particular time point can largely explain gene expression over a large span of time. Together, these dynamics suggest a coordinated genome-wide response to environmental triggers. "With this network view, we can see that some of these components are targeted by the same master regulator proteins, which suggests precise and coordinated genetic control," says Song. "This could be important for agricultural purposes because regulating one gene could in turn stimulate or suppress another whole set of genes, allowing for a comprehensive design of interventions." The results mirror those of a 2013 study by the Ecker lab on the plant hormone ethylene, suggesting that such coordinated and hierarchical control of genetic activity may be common to flowering plants.


News Article | January 19, 2016
Site: phys.org

Now, researchers at the Salk Institute and Cambridge University have used this ancient practice, combined with modern genetic research, to show that grafted plants can share epigenetic traits, according to a new paper published the week of January 18, 2016 in the Proceedings of the National Academy of Sciences. "Grafting is something done often in the commercial world, and yet, we really don't completely understand the consequences for the two plants," says Joseph Ecker, one of the senior authors of the paper and director of Salk's Genomic Analysis Laboratory. "Our study showed genetic information is actually flowing from one plant to the other. That's the surprise to me." That genetic information shared between plants isn't DNA—the two grafted plants keep their original genomes—but epigenetic information is being communicated within the plant. In epigenetics, chemical markers act on existing genes in a plant or animal's DNA to turn genes on or off. Epigenetics can determine whether a cell becomes muscle cell or a skin cell and determine how a plant reacts to different soils, climates and disease. "In the future, this research might allow growers to exploit epigenetic information to improve crops and yields," says Mathew Lewsey, one of the first authors of the paper and a Salk research associate. To track the flow of epigenetic information, the Salk and Cambridge teams focused on tiny molecules called small RNAs, or sRNAs. There are various types of epigenetic processes, but sRNAs contribute to a gene silencing process called DNA methylation. In DNA methylation, molecular markers bind along the top of DNA to block the cell's machinery from reading or expressing the genes under the molecular markers. Previous studies by the Cambridge members of this research group have shown that sRNAs can move across grafted plants from the shoots to the roots. So the researchers designed a grafting experiment with three variations of the plant Arabidopsis thaliana (thale cress). Two varieties were wild-type thale cress, while the third variety was a mutant bred to lack sRNAs of any kind. After performing each graft, the researchers analyzed shoot and root tissue to look for changes in DNA methylation along the plants' different genomes. They also confirmed whether the sRNAs were moving from the wild-type plants into the mutant variety that lacked sRNAs. "This set-up allowed us to observe something quite unique: they were actually transmitting the epigenetic equivalent of alleles, called epialleles," says Lewsey. An allele is a gene that is shared within a species, but may differ from individual to individual, such as the allele for developing Huntington's disease. In this case, the researchers were searching for sites along the epigenome of the plants that were alleles altered by the epigenetic process. In other words: epialleles. "Because the two wild-type plants varied in their epigenetics along their genomes, we could observe how grafting a shoot onto roots can actually transmit epialleles from one plant to another," says Lewsey. David Baulcombe, a senior author on the paper, acknowledges that the new findings were not totally unexpected. Previous smaller scale work had indicated that sRNAs could move and mediate epigenetic change in the recipient tissue. "What was unexpected, however, was the scale of the changes due to the mobile RNA," says Baulcombe, of the Department of Plant Sciences at the University of Cambridge. Thousands of sites along the thale cress genome were silenced by sRNAs. By examining the location of these epialleles, the researchers could start to find clues to their purpose. The epialleles observed in the experiment were often silencing areas of the genome called transposable elements, or transposons. Transposons make up part of the so-called dark DNA, or the vast portion of a genome that does not code for genes. Originally called "jumping genes," transposons can move from up and down the genome to influence the expression of genes nearby. Many of the transposons targeted by the sRNAs in the experiment were very close in location to active genes. Despite this silencing of transposons, there were only small changes in gene expression between the wild-type plants and the mutant plant that lacked sRNAs. "We think this is because of the compact nature of the A. thaliana genome," says Lewsey. "It's likely that moving to a species with a larger genome and transposons that are more active will show more of a difference." Thanks to new gene editing tools, it will be possible to run similar grafting experiments with the more complicated genomes of popular crops. "In other plants with more complex genomes, these effects are going to be magnified by many hundred-fold," says Ecker, who is also a Howard Hughes Medical Institute and Gordon and Betty Moore Foundation investigator. Baulcombe agrees that the epigenetic effects of the mobile RNA are likely to be much greater with crop plants than in the models species used in the present work. The two research groups are now planning an extended collaboration to explore these effects in tomatoes and other crops. "There are already thousands of other epigenetic differences between the roots and the shoots of a single plants—and two grafted plants are also genetically different," says Ecker. "So creating that epiallele difference in the roots is something really new for the plant."


He Y.,University of California at San Diego | He Y.,Genomic Analysis Laboratory | Ecker J.R.,Genomic Analysis Laboratory | Ecker J.R.,Salk Institute for Biological Studies
Annual Review of Genomics and Human Genetics | Year: 2015

DNA methylation is a chemical modification that occurs predominantly on CG dinucleotides in mammalian genomes. However, recent studies have revealed that non-CG methylation (mCH) is abundant and nonrandomly distributed in the genomes of pluripotent cells and brain cells, and is present at lower levels in many other human cells and tissues. Surprisingly, mCH in pluripotent cells is distinct from that in brain cells in terms of sequence specificity and association with transcription, indicating the existence of different mCH pathways. In addition, several recent studies have begun to reveal the biological significance of mCH in diverse cellular processes. In reprogrammed somatic cells, mCH marks megabase-scale regions that have failed to revert to the pluripotent epigenetic state. In myocytes, promoter mCH accumulation is associated with the transcriptional response to environmental factors. In brain cells, mCH accumulates during the establishment of neural circuits and is associated with Rett syndrome. In this review, we summarize the current understanding of mCH and its possible functional consequences in different biological contexts. Copyright © 2015 by Annual Reviews. All rights reserved.

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