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Article ; Online: Universal NicE-Seq: A Simple and Quick Method for Accessible Chromatin Detection in Fixed Cells.

Chin, Hang Gyeong / Vishnu, Udayakumar S / Sun, Zhiyi / Ponnaluri, V K Chaithanya / Zhang, Guoqiang / Xu, Shuang-Yong / Benoukraf, Touati / Cejas, Paloma / Spracklin, George / Estève, Pierre-Olivier / Long, Henry W / Pradhan, Sriharsa

Methods in molecular biology (Clifton, N.J.)

2023 Volume 2611, Page(s) 39–52

Abstract: Genome-wide accessible chromatin sequencing and identification has enabled deciphering the epigenetic information encoded in chromatin, revealing accessible promoters, enhancers, nucleosome positioning, transcription factor occupancy, and other ... ...

Abstract	Genome-wide accessible chromatin sequencing and identification has enabled deciphering the epigenetic information encoded in chromatin, revealing accessible promoters, enhancers, nucleosome positioning, transcription factor occupancy, and other chromosomal protein binding. The starting biological materials are often fixed using formaldehyde crosslinking. Here, we describe accessible chromatin library preparation from low numbers of formaldehyde-crosslinked cells using a modified nick translation method, where a nicking enzyme nicks one strand of DNA and DNA polymerase incorporates biotin-conjugated dATP, dCTP, and methyl-dCTP. Once the DNA is labeled, it can be isolated for NGS library preparation. We termed this method as universal NicE-seq (nicking enzyme-assisted sequencing). We also demonstrate a single tube method that enables direct NGS library preparation from low cell numbers without DNA purification. Furthermore, we demonstrated universal NicE-seq on FFPE tissue section sample.
MeSH term(s)	Chromatin ; DNA/genetics ; Nucleosomes ; Chromosome Mapping/methods ; Sequence Analysis, DNA/methods ; Formaldehyde ; High-Throughput Nucleotide Sequencing/methods
Chemical Substances	Chromatin ; DNA (9007-49-2) ; Nucleosomes ; Formaldehyde (1HG84L3525)
Language	English
Publishing date	2023-02-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-2899-7_3
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Article ; Online: S-adenosylhomocysteine Hydrolase Participates in DNA Methylation Inheritance.

Ponnaluri, V K Chaithanya / Estève, Pierre-Olivier / Ruse, Cristian I / Pradhan, Sriharsa

Journal of molecular biology

2018 Volume 430, Issue 14, Page(s) 2051–2065

Abstract: DNA (cytosine-5) methyltransferase 1 (DNMT1) is essential for mammalian development and maintenance of DNA methylation following DNA replication in cells. The DNA methylation process generates S-adenosyl-l-homocysteine, a strong inhibitor of DNMT1. Here ... ...

Abstract	DNA (cytosine-5) methyltransferase 1 (DNMT1) is essential for mammalian development and maintenance of DNA methylation following DNA replication in cells. The DNA methylation process generates S-adenosyl-l-homocysteine, a strong inhibitor of DNMT1. Here we report that S-adenosylhomocysteine hydrolase (SAHH/AHCY), the only mammalian enzyme capable of hydrolyzing S-adenosyl-l-homocysteine binds to DNMT1 during DNA replication. SAHH enhances DNMT1 activity in vitro, and its overexpression in mammalian cells led to hypermethylation of the genome, whereas its inhibition by adenosine periodate or siRNA-mediated knockdown resulted in hypomethylation of the genome. Hypermethylation was consistent in both gene bodies and repetitive DNA elements leading to aberrant gene regulation. Cells overexpressing SAHH specifically up-regulated metabolic pathway genes and down-regulated PPAR and MAPK signaling pathways genes. Therefore, we suggest that alteration of SAHH level affects global DNA methylation levels and gene expression.
MeSH term(s)	Adenosylhomocysteinase/genetics ; Adenosylhomocysteinase/metabolism ; Animals ; COS Cells ; Cercopithecus aethiops ; DNA (Cytosine-5-)-Methyltransferase 1/metabolism ; DNA Methylation ; DNA Replication ; Epigenesis, Genetic ; Gene Expression Regulation ; HEK293 Cells ; HeLa Cells ; Humans ; Metabolic Networks and Pathways ; Mutation ; Proteomics/methods ; Repetitive Sequences, Nucleic Acid ; S Phase ; S-Adenosylhomocysteine/metabolism ; Signal Transduction
Chemical Substances	S-Adenosylhomocysteine (979-92-0) ; DNA (Cytosine-5-)-Methyltransferase 1 (EC 2.1.1.37) ; DNMT1 protein, human (EC 2.1.1.37) ; AHCY protein, human (EC 3.3.1.1) ; Adenosylhomocysteinase (EC 3.3.1.1)
Language	English
Publishing date	2018-05-28
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80229-3
ISSN	1089-8638 ; 0022-2836
ISSN (online)	1089-8638
ISSN	0022-2836
DOI	10.1016/j.jmb.2018.05.014
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Article: S-adenosylhomocysteine Hydrolase Participates in DNA Methylation Inheritance

Ponnaluri, V.K. Chaithanya / Estève, Pierre-Olivier / Ruse, Cristian I / Pradhan, Sriharsa

Journal of molecular biology. 2018 July 06, v. 430, no. 14

2018

Abstract	DNA (cytosine-5) methyltransferase 1 (DNMT1) is essential for mammalian development and maintenance of DNA methylation following DNA replication in cells. The DNA methylation process generates S-adenosyl-l-homocysteine, a strong inhibitor of DNMT1. Here we report that S-adenosylhomocysteine hydrolase (SAHH/AHCY), the only mammalian enzyme capable of hydrolyzing S-adenosyl-l-homocysteine binds to DNMT1 during DNA replication. SAHH enhances DNMT1 activity in vitro, and its overexpression in mammalian cells led to hypermethylation of the genome, whereas its inhibition by adenosine periodate or siRNA-mediated knockdown resulted in hypomethylation of the genome. Hypermethylation was consistent in both gene bodies and repetitive DNA elements leading to aberrant gene regulation. Cells overexpressing SAHH specifically up-regulated metabolic pathway genes and down-regulated PPAR and MAPK signaling pathways genes. Therefore, we suggest that alteration of SAHH level affects global DNA methylation levels and gene expression.
Keywords	DNA ; DNA methylation ; DNA replication ; adenosine ; adenosylhomocysteinase ; biochemical pathways ; gene expression ; genes ; mammals ; methyltransferases ; mitogen-activated protein kinase ; peroxisome proliferator-activated receptors ; signal transduction
Language	English
Dates of publication	2018-0706
Size	p. 2051-2065.
Publishing place	Elsevier Ltd
Document type	Article
ZDB-ID	80229-3
ISSN	1089-8638 ; 0022-2836
ISSN (online)	1089-8638
ISSN	0022-2836
DOI	10.1016/j.jmb.2018.05.014
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Article ; Online: Developmentally linked human DNA hypermethylation is associated with down-modulation, repression, and upregulation of transcription.

Baribault, Carl / Ehrlich, Kenneth C / Ponnaluri, V K Chaithanya / Pradhan, Sriharsa / Lacey, Michelle / Ehrlich, Melanie

Epigenetics

2018 Volume 13, Issue 3, Page(s) 275–289

Abstract: DNA methylation can affect tissue-specific gene transcription in ways that are difficult to discern from studies focused on genome-wide analyses of differentially methylated regions (DMRs). To elucidate the variety of associations between differentiation- ...

Abstract	DNA methylation can affect tissue-specific gene transcription in ways that are difficult to discern from studies focused on genome-wide analyses of differentially methylated regions (DMRs). To elucidate the variety of associations between differentiation-related DNA hypermethylation and transcription, we used available epigenomic and transcriptomic profiles from 38 human cell/tissue types to focus on such relationships in 94 genes linked to hypermethylated DMRs in myoblasts (Mb). For 19 of the genes, promoter-region hypermethylation in Mb (and often a few heterologous cell types) was associated with gene repression but, importantly, DNA hypermethylation was absent in many other repressed samples. In another 24 genes, DNA hypermethylation overlapped cryptic enhancers or super-enhancers and correlated with down-modulated, but not silenced, gene expression. However, such methylation was absent, surprisingly, in both non-expressing samples and highly expressing samples. This suggests that some genes need DMR hypermethylation to help repress cryptic enhancer chromatin only when they are actively transcribed. For another 11 genes, we found an association between intergenic hypermethylated DMRs and positive expression of the gene in Mb. DNA hypermethylation/transcription correlations similar to those of Mb were evident sometimes in diverse tissues, such as aorta and brain. Our findings have implications for the possible involvement of methylated DNA in Duchenne's muscular dystrophy, congenital heart malformations, and cancer. This epigenomic analysis suggests that DNA methylation is not simply the inevitable consequence of changes in gene expression but, instead, is often an active agent for fine-tuning transcription in association with development.
MeSH term(s)	Adult ; Aged ; Aged, 80 and over ; Cell Differentiation/genetics ; Child, Preschool ; Chromatin/genetics ; CpG Islands/genetics ; DNA Methylation/genetics ; Epigenesis, Genetic ; Female ; Gene Expression Regulation/genetics ; Heart Defects, Congenital/genetics ; Heart Defects, Congenital/pathology ; Histones/genetics ; Humans ; Male ; Muscle, Skeletal/metabolism ; Muscular Dystrophy, Duchenne/genetics ; Muscular Dystrophy, Duchenne/pathology ; Myoblasts/metabolism ; Neoplasms/genetics ; Neoplasms/pathology ; Organ Specificity ; Promoter Regions, Genetic ; Transcriptional Activation/genetics
Chemical Substances	Chromatin ; Histones
Language	English
Publishing date	2018-04-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1559-2308
ISSN (online)	1559-2308
DOI	10.1080/15592294.2018.1445900
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Article ; Online: A mechanistic overview of TET-mediated 5-methylcytosine oxidation.

Ponnaluri, V K Chaithanya / Maciejewski, Jaroslaw P / Mukherji, Mridul

Biochemical and biophysical research communications

2013 Volume 436, Issue 2, Page(s) 115–120

Abstract: Methylation of DNA at the carbon-5 position of cytosine plays crucial roles in the epigenetic transcriptional silencing during metazoan development. Recent identification of Ten-Eleven Translocation (TET)-family demethylases have added a new dimension to ...

Abstract	Methylation of DNA at the carbon-5 position of cytosine plays crucial roles in the epigenetic transcriptional silencing during metazoan development. Recent identification of Ten-Eleven Translocation (TET)-family demethylases have added a new dimension to dynamic regulation of 5-methylcytosine (5mC), and thus, inheritable and somatic gene silencing. The interest in hematology was particularly stimulated by the recent discovery of TET2 mutations in myeloid malignancies which were proven to be leukemogenic in murine knockout models. The TET-family enzymes are Fe(II), 2-oxoglutarate-dependent oxygenases and catalyze demethylation of 5mC by iterative oxidation reactions. In the last decade results from numerous studies have established a key role for these enzymes in epigenetic transcriptional regulation in eukaryotes primarily by hydroxylation reactions. The TET catalyzed hydroxylation and dehydration reactions in the mammalian system exemplify the diversity of oxidation reactions catalyzed by Fe(II), 2-oxoglutarate-dependent oxygenases, and suggest an existence of other types of oxidation reactions catalyzed by these enzymes in the eukaryotes, which are so far only documented in prokaryotes. Here, we review the TET-mediated 5mC oxidation in light of the putative reaction mechanism of Fe(II), 2-oxoglutarate-dependent oxygenases.
MeSH term(s)	5-Methylcytosine/metabolism ; Animals ; DNA Methylation ; Dioxygenases/genetics ; Dioxygenases/metabolism ; Humans ; Iron/metabolism ; Isoenzymes/genetics ; Isoenzymes/metabolism ; Ketoglutaric Acids/metabolism ; Models, Genetic ; Oxidation-Reduction
Chemical Substances	Isoenzymes ; Ketoglutaric Acids ; 5-Methylcytosine (6R795CQT4H) ; alpha-ketoglutaric acid (8ID597Z82X) ; Iron (E1UOL152H7) ; TET3 protein, human (EC 1.-) ; Dioxygenases (EC 1.13.11.-)
Language	English
Publishing date	2013-06-28
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	205723-2
ISSN	1090-2104 ; 0006-291X ; 0006-291X
ISSN (online)	1090-2104 ; 0006-291X
ISSN	0006-291X
DOI	10.1016/j.bbrc.2013.05.077
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Article ; Online: Evaluation of anti-HIF and anti-angiogenic properties of honokiol for the treatment of ocular neovascular diseases.

Vavilala, Divya Teja / Ponnaluri, V K Chaithanya / Kanjilal, Debolina / Mukherji, Mridul

PloS one

2014 Volume 9, Issue 11, Page(s) e113717

Abstract: Pathological activation of the hypoxia-inducible-factor (HIF) pathway leading to expression of pro-angiogenic genes, such as vascular endothelial growth factor (VEGF), is the fundamental cause of neovascularization in ocular ischemic diseases and cancers. ...

Abstract	Pathological activation of the hypoxia-inducible-factor (HIF) pathway leading to expression of pro-angiogenic genes, such as vascular endothelial growth factor (VEGF), is the fundamental cause of neovascularization in ocular ischemic diseases and cancers. We have shown that pure honokiol inhibits the HIF pathway and hypoxia-mediated expression of pro-angiogenic genes in a number of cancer and retinal pigment epithelial (RPE) cell lines. The crude extracts, containing honokiol, from Magnolia plants have been used for thousands of years in the traditional oriental medicine for a number of health benefits. We have recently demonstrated that daily intraperitoneal injection of honokiol starting at postnatal day (P) 12 in an oxygen induced retinopathy mouse model significantly reduced retinal neovascularization at P17. Here, we evaluate the mechanism of HIF inhibition by honokiol in RPE cells. Using chromatin immunoprecipitation experiments, we demonstrate that honokiol inhibits binding of HIF to hypoxia-response elements present on VEGF promoter. We further show using a number of in vitro angiogenesis assays that, in addition to anti-HIF effect, honokiol manifests potent anti-angiogenic effect on human retinal micro vascular endothelial cells. Our results suggest that honokiol possesses potent anti-HIF and anti-angiogenic properties. These properties of honokiol make it an ideal therapeutic agent for the treatment of ocular neovascular diseases and solid tumors.
MeSH term(s)	Angiogenesis Inhibitors/pharmacology ; Angiogenesis Inhibitors/therapeutic use ; Biphenyl Compounds/pharmacology ; Biphenyl Compounds/therapeutic use ; Cell Line ; Cell Movement/drug effects ; Cell Proliferation/drug effects ; Endothelium, Vascular/drug effects ; Eye Diseases/drug therapy ; HeLa Cells ; Humans ; Hypoxia-Inducible Factor 1/antagonists & inhibitors ; Lignans/pharmacology ; Lignans/therapeutic use ; Luciferases/antagonists & inhibitors ; Neovascularization, Pathologic/drug therapy ; Retinal Pigment Epithelium/cytology
Chemical Substances	Angiogenesis Inhibitors ; Biphenyl Compounds ; Hypoxia-Inducible Factor 1 ; Lignans ; honokiol (11513CCO0N) ; Luciferases (EC 1.13.12.-)
Language	English
Publishing date	2014
Publishing country	United States
Document type	Journal Article
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0113717
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Article ; Online: NicE-seq: high resolution open chromatin profiling.

Ponnaluri, V K Chaithanya / Zhang, Guoqiang / Estève, Pierre-Olivier / Spracklin, George / Sian, Stephanie / Xu, Shuang-Yong / Benoukraf, Touati / Pradhan, Sriharsa

Genome biology

2017 Volume 18, Issue 1, Page(s) 122

Abstract: Open chromatin profiling integrates information across diverse regulatory elements to reveal the transcriptionally active genome. Tn5 transposase and DNase I sequencing-based methods prefer native or high cell numbers. Here, we describe NicE-seq (nicking ...

Abstract	Open chromatin profiling integrates information across diverse regulatory elements to reveal the transcriptionally active genome. Tn5 transposase and DNase I sequencing-based methods prefer native or high cell numbers. Here, we describe NicE-seq (nicking enzyme assisted sequencing) for high-resolution open chromatin profiling on both native and formaldehyde-fixed cells. NicE-seq captures and reveals open chromatin sites (OCSs) and transcription factor occupancy at single nucleotide resolution, coincident with DNase hypersensitive and ATAC-seq sites at a low sequencing burden. OCSs correlate with RNA polymerase II occupancy and active chromatin marks, while displaying a contrasting pattern to CpG methylation. Decitabine-mediated hypomethylation of HCT116 displays higher numbers of OCSs.
Language	English
Publishing date	2017-06-28
Publishing country	England
Document type	Journal Article
ZDB-ID	2040529-7
ISSN	1474-760X ; 1465-6914 ; 1465-6906
ISSN (online)	1474-760X ; 1465-6914
ISSN	1465-6906
DOI	10.1186/s13059-017-1247-6
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Article ; Online: Studies on substrate specificity of Jmjd2a-c histone demethylases.

Ponnaluri, V K Chaithanya / Vavilala, Divya Teja / Mukherji, Mridul

Biochemical and biophysical research communications

2011 Volume 405, Issue 4, Page(s) 588–592

Abstract: Jumonji domain containing iron (II), 2-oxoglutarate (2OG)-dependent dioxygenases from Jmjd2 family demethylate trimethylated histone3-lysine 9 (H3-K9me3), and also H3-K9me2 and H3-K36me3, albeit at lower rates. Recently, we have identified the first non- ... ...

Abstract	Jumonji domain containing iron (II), 2-oxoglutarate (2OG)-dependent dioxygenases from Jmjd2 family demethylate trimethylated histone3-lysine 9 (H3-K9me3), and also H3-K9me2 and H3-K36me3, albeit at lower rates. Recently, we have identified the first non-histone substrates of JmjD2 demethylases. Here, we studied the substrate specificity of Jmjd2a-c demethylases using site-directed mutagenesis and novel non-histone substrates. We identified preference of Arg at -1 position and a smaller amino acid at -2 position using both singly and doubly mutated peptide substrates by Jmjd2a-c demethylases. Our results also identified similarities in substrate selectivity by H3-K9 methyltransferase, G9a and Jmjd2 demethylases despite their distinct reaction mechanisms.
MeSH term(s)	Arginine/chemistry ; Arginine/genetics ; Cloning, Molecular ; Humans ; Jumonji Domain-Containing Histone Demethylases/chemistry ; Jumonji Domain-Containing Histone Demethylases/genetics ; Mutagenesis, Site-Directed ; Substrate Specificity
Chemical Substances	KDM4C protein, human ; Arginine (94ZLA3W45F) ; Jumonji Domain-Containing Histone Demethylases (EC 1.14.11.-) ; KDM4B protein, human (EC 1.14.11.-) ; KDM4A protein, human (EC 1.5.-)
Language	English
Publishing date	2011-02-25
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	205723-2
ISSN	1090-2104 ; 0006-291X ; 0006-291X
ISSN (online)	1090-2104 ; 0006-291X
ISSN	0006-291X
DOI	10.1016/j.bbrc.2011.01.073
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Article ; Online: Hypoxia mediated expression of stem cell markers in VHL-associated hemangioblastomas.

Ponnaluri, V K Chaithanya / Vavilala, Divya Teja / Prakash, Swami / Mukherji, Mridul

Biochemical and biophysical research communications

2013 Volume 438, Issue 1, Page(s) 71–77

Abstract: Hemangioblastomas of the retina, central nervous system, and kidney are observed in patients with mutations in the von Hippel-Lindau (VHL) tumor suppressor gene. Mutations in the VHL lead to constitutive activation of hypoxia-inducible-factor (HIF) ... ...

Abstract	Hemangioblastomas of the retina, central nervous system, and kidney are observed in patients with mutations in the von Hippel-Lindau (VHL) tumor suppressor gene. Mutations in the VHL lead to constitutive activation of hypoxia-inducible-factor (HIF) pathway. HIF-mediated expression of pro-angiogenic genes causes extensive pathological neovascularization in hemangioblastomas. A number of studies have shown coexistence of pro-angiogenic and stem cell markers in 'tumorlet-like stromal cells' in the retinal and optic nerve hemangioblastomas, leading to suggestions that hemangioblastomas originate from developmentally arrested stem cells or embryonic progenitors. Since recent studies have shown that the HIF pathway also plays a role in the maintenance/de-differentiation of normal and cancerous stem cells, we evaluated the role of the HIF pathway in the expression of stem cell markers in VHL-/- renal cell carcinoma cells under normoxia or VHL+/+ retinal pigment epithelial cells under hypoxia. Here we show that the expression of stem cell markers in hemangioblastomas is due to activation of the HIF pathway. Further, we show that honokiol, digoxin, and doxorubicin, three recently identified HIF inhibitors from natural sources, blocks the expression of stem cell markers. Our results show the mechanism for the cytological origin of neoplastic stromal cells in hemangioblastomas, and suggest that inhibition of the HIF pathway is an attractive strategy for the treatment of hemangioblastomas.
MeSH term(s)	Cell Hypoxia ; Cell Line, Tumor ; Gene Expression Regulation, Neoplastic ; Hemangioblastoma/metabolism ; Hemangioblastoma/pathology ; Humans ; Hypoxia-Inducible Factor 1, alpha Subunit/metabolism ; Neoplastic Stem Cells/metabolism ; Neoplastic Stem Cells/pathology ; Von Hippel-Lindau Tumor Suppressor Protein/metabolism
Chemical Substances	HIF1A protein, human ; Hypoxia-Inducible Factor 1, alpha Subunit ; Von Hippel-Lindau Tumor Suppressor Protein (EC 2.3.2.27) ; VHL protein, human (EC 6.3.2.-)
Language	English
Publishing date	2013-08-16
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	205723-2
ISSN	1090-2104 ; 0006-291X ; 0006-291X
ISSN (online)	1090-2104 ; 0006-291X
ISSN	0006-291X
DOI	10.1016/j.bbrc.2013.07.028
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Article ; Online: Enzymatic methyl sequencing detects DNA methylation at single-base resolution from picograms of DNA.

Genome research

2021 Volume 31, Issue 7, Page(s) 1280–1289

Abstract: Bisulfite sequencing detects 5mC and 5hmC at single-base resolution. However, bisulfite treatment damages DNA, which results in fragmentation, DNA loss, and biased sequencing data. To overcome these problems, enzymatic methyl-seq (EM-seq) was developed. ... ...

Abstract	Bisulfite sequencing detects 5mC and 5hmC at single-base resolution. However, bisulfite treatment damages DNA, which results in fragmentation, DNA loss, and biased sequencing data. To overcome these problems, enzymatic methyl-seq (EM-seq) was developed. This method detects 5mC and 5hmC using two sets of enzymatic reactions. In the first reaction, TET2 and T4-BGT convert 5mC and 5hmC into products that cannot be deaminated by APOBEC3A. In the second reaction, APOBEC3A deaminates unmodified cytosines by converting them to uracils. Therefore, these three enzymes enable the identification of 5mC and 5hmC. EM-seq libraries were compared with bisulfite-converted DNA, and each library type was ligated to Illumina adaptors before conversion. Libraries were made using NA12878 genomic DNA, cell-free DNA, and FFPE DNA over a range of DNA inputs. The 5mC and 5hmC detected in EM-seq libraries were similar to those of bisulfite libraries. However, libraries made using EM-seq outperformed bisulfite-converted libraries in all specific measures examined (coverage, duplication, sensitivity, etc.). EM-seq libraries displayed even GC distribution, better correlations across DNA inputs, increased numbers of CpGs within genomic features, and accuracy of cytosine methylation calls. EM-seq was effective using as little as 100 pg of DNA, and these libraries maintained the described advantages over bisulfite sequencing. EM-seq library construction, using challenging samples and lower DNA inputs, opens new avenues for research and clinical applications.
Language	English
Publishing date	2021-06-17
Publishing country	United States
Document type	Journal Article
ZDB-ID	1284872-4
ISSN	1549-5469 ; 1088-9051 ; 1054-9803
ISSN (online)	1549-5469
ISSN	1088-9051 ; 1054-9803
DOI	10.1101/gr.266551.120
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