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MNase-seq

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Mnase based sequencing

MNase-seq (Micrococcal Nuclease sequencing), short for micrococcal nuclease digestion with deep sequencing[1], is a molecular biological technique that has been used since 2008 to measure nucleosome occupancy in the human genome[2]. Though, the term ‘MNase-seq’ had not been coined until a year later, in 2009[3]. Briefly, this technique relies on the use of the non-specific endo-exonuclease micrococcal nuclease, an enzyme derived from the bacteria Staphylococcus aureus, to bind and cleave protein-unbound regions of DNA on chromatin. DNA bound to histones or other chromatin-bound proteins may remain undigested. The uncut DNA is then purified from the proteins and sequenced through one or more of the various Next-Generation sequencing methods[4].
MNase-seq is one of four classes of methods used for assessing the status of the epigenome through analysis of chromatin accessibility. The other three techniques are DNase-seq, FAIRE-seq, and ATAC-seq[1]. While MNase-seq is primarily used to sequence regions of DNA bound by nucleosomes or other chromatin-bound proteins[2], the other three are commonly used for: mapping Deoxyribonuclease I hypersensitive sites (DHSs)[5], sequencing the DNA unbound to chromatin proteins[6], and sequencing regions of loosely packaged chromatin through transposition of markers[7],[8], respectively[1].

History

Micrococcal nuclease (MNase) was first discovered in Staphylococcus aureus in 1956[9], protein crystallized in 1966[10], and characterized in 1967[11]. MNase digestion of chromatin was key to early studies of chromatin studies; being used to determine that each nucleosomal unit of chromatin was composed of approximately 200bp of DNA[12]. This, alongside Olins’ and Olins’ “beads on a string” model[13], confirmed Kornberg’s ideas regarding the basic chromatin structure[14]. Upon additional studies, it was found that MNase could not degrade histone-bound DNA shorter than ~140bp and that DNase I and II could degrade the bound DNA to as low as 10bp[15],[16]. This ultimately elucidated that ~146bp of DNA wrap around the nucleosome core[17], ~50bp linker DNA connect each nucleosome[18], and that 10 continuous base-pairs of DNA tightly bind to the nucleosome core in intervals[16].
In addition to being used to study chromatin structure, micrococcal nuclease digestion had been used in oligonucleotide sequencing experiments since its characterization in 1967[19]. MNase digestion was additionally used in several studies to analyze chromatin-free sequences, such as yeast (S. cerevisiae) mitochondrial DNA[20] as well as bacteriophage DNA[21],[22] through its preferential digestion of adenine and thymine-rich regions[23]. In the early 1980s, MNase digestion was used to determine the nucleosomal phasing and associated DNA for chromosomes from mature SV40[24], fruit flies (D. melanogaster)[25], yeast[26], and monkeys[27], among others. The first study to use this digestion to study the relevance of chromatin accessibility to gene expression in humans was in 1985, where the nuclease was used to study the association of certain oncogenic sequences with chromatin and nuclear proteins[28]. Studies utilizing MNase digestion to determine nucleosome positioning without sequencing or array information continued into the early 2000’s[29].
With the advent of whole genome sequencing in the late 1990s and early 2000s, it became possible to compare purified DNA sequences to the eukaryotic genomes of S. cerevisiae[30], C. elegans[31], D. melanogaster[32], A. thaliana[33], M. musculus[34], and H. sapiens[35]. MNase digestion was first applied to genome-wide nucleosome occupancy studies in S. cerevisiae[36] and C. elegans[37], accompanied by analyses through microarrays to determine which DNA regions were enriched with MNase-resistant nucleosomes. MNase-based microarray analyses were often utilized at genome-wide scales for yeast[38],[39] and in limited genomic regions in humans[40],[41] to determine nucleosome positioning, which could be used as an inference for transcriptional inactivation.
It was not until 2008, around the time Next-Generation sequencing was being developed when MNase digestion was combined with high-throughput sequencing, namely Solexa/Illumina sequencing, to study nucleosomal positioning at a genome-wide scale in humans[2]. A year later, the terms “MNase-Seq” and “MNase-ChIP”, for micrococcal nuclease digestion with chromatin immunoprecipitation, were finally coined[3]. Since its initial application in 2008[2], MNase-seq has been utilized to deep sequence DNA associated with nucleosome occupancy and epigenomics across eukaryotes[4]. As of February 2020, MNase-seq is still applied to assay accessibility in chromatin[42].

Description

MNase-seq uses the endo-exonuclease micrococcal nuclease to bind and cleave protein-unbound regions of DNA of eukaryotic chromatin, which is optionally crosslinked with formaldehyde[43], first cleaving and excising one strand, then cleaving the antiparallel strand as well[3]. To have activity, MNase requires a buffer containing Ca2+ ions, typically with a final concentration of 1mM[4],[11]. If a region of DNA is bound by the nucleosome core (i.e. histone proteins) or other chromatin-bound proteins (e.g. transcription factors), then MNase is unable to bind and cleave the DNA. Nucleosomes or the chromatin-bound proteins can be purified from the sample using immunoprecipitation and the bound DNA can be subsequently purified via gel electrophoresis. The purified DNA is typically ~150bp, if purified from nucleosomes[2], or shorter, if from another protein (e.g. transcription factors)[44], making short-read high-throughput sequencing ideal for MNase-Seq as reads for these technologies are highly accurate but can only cover a couple hundred continuous base-pairs in length[45]. Once sequenced, the reads can be aligned to a reference genome to determine which DNA regions are bound by nucleosomes or proteins of interest, with tools such as Bowtie (sequence analysis) [1]. The positioning of nucleosomes elucidated, through MNase-seq, can then be used to predict genomic expression[46] and regulation[47] at the time of digestion, as chromatin is dynamic and the positioning of nucleosomes on DNA changes through the activity of various transcription factors and complexes, approximately reflecting transcriptional activity at these sites[48].

Comparison to other Accessibility Assays

MNase-seq is one of four major methods (DNase-seq, MNase-seq, FAIRE-seq, and ATAC-seq) for more direct determination of chromatin accessibility and the subsequent consequences for gene transcription[49]. All four techniques are contrasted with ChIP-seq, which relies on the inference that certain marks on histone tails are indicative of gene activation or repression[50], not directly assessing nucleosome positioning, but instead being valuable for the assessment of histone modifier enzymatic function[1].

DNase-seq

As with MNase-seq[2], DNase-seq was developed from an existing DNA footprinting technology[5] and was later combined with Next-Generation sequencing technology to assay chromatin accessibility[51]. Both techniques have been used across several eukaryotes to ascertain information on nucleosome positioning in the respective organisms[1] and both rely on the same principle of digesting open DNA to isolate ~140bp bands of DNA from nucleosomes[2],[52] or shorter bands if ascertaining transcription factor information[44],[52]. Both techniques have recently been optimized for single-cell sequencing, which corrects for one of the major disadvantages of both techniques; that being the requirement for high cell input[53],[54].
At sufficient concentrations, DNase I is capable of digesting nucleosome-bound DNA to 10bp, whereas micrococcal nuclease cannot[16]. Additionally, DNase-seq is used to identify DHSs, which are regions of DNA that are hypersensitive to DNase treatment and are often indicative of regulatory regions (e.g. promoters or enhancers)[55]. An equivalent effect is not found with MNase. As a result of this distinction, DNase-seq is primarily utilized to directly identify regulatory regions, whereas MNase-seq is used to identify transcription factor and nucleosomal occupancy to indirectly infer effects on gene expression[1].

FAIRE-seq

FAIRE-seq differs more from MNase-seq than does DNase-seq[1]. FAIRE-seq was developed in 2007[6] and combined with next-generation sequencing three years later to study DHSs[56]. FAIRE-seq relies on the use of formaldehyde to crosslink target proteins with DNA and then subsequent sonication and phenol-chloroform extraction to separate non-crosslinked DNA and crosslinked DNA. The non-crosslinked DNA is sequenced and analyzed, allowing for direct observation of open chromatin[57].
MNase-seq does not measure chromatin accessibility as directly as FAIRE-seq. However, unlike FAIRE-seq, it does necessarily require crosslinking[4], nor does it rely on sonication[1], but it may require phenol and chloroform extraction[4]. Two major disadvantages of FAIRE-seq are the minimum input of 100,000 cells and the reliance on crosslinking[6], which may also bind other chromatin-bound proteins to the DNA, hence limiting the amount of non-crosslinked DNA that can be recovered and assayed from the aqueous phase[49]. Thus, the overall resolution obtained from FAIRE-seq can be relatively lower than that of DNase-seq or MNase-seq[49] and with the 100,000 cell requirement[6], the single-cell equivalents of DNase-seq[53] or MNase-seq[54] make them far more appealing alternatives[1].

ATAC-seq

ATAC-seq is the most recently developed chromatin accessibility assay[7]. ATAC-seq uses a hyperactive transposase to insert transposable markers with specific adapters used for sequencing into open regions of chromatin. PCR can be used to amplify sequences adjacent to the inserted transposons, allowing for determination of open chromatin sequences without causing a shift in chromatin structure[7],[8]. ATAC-seq has been proven effective in humans, amongst other eukaryotes, including in frozen samples[58]. As with DNase-seq[53] and MNase-seq[54], a successful single-cell version of ATAC-seq has also been developed[59].
ATAC-seq has several advantages over MNase-seq. ATAC-seq does not rely on the variable digestion of the micrococcal nuclease, nor crosslinking or phenol-chloroform extraction[4],[8]. It generally maintains chromatin structure, so results from ATAC-seq can be used to directly assess chromatin accessibility, rather than indirectly as with MNase-seq. ATAC-seq can also be completed within a few hours[8], whereas the other techniques typically require overnight incubation periods[4],[5],[6]. The two major disadvantages to ATAC-seq, in comparison to MNase-seq, are the requirement for higher sequencing coverage and the prevalence of mitochondrial contamination due to non-specific insertion of DNA into both mitochondrial DNA and nuclear DNA[1],[7],[8].


Applications and Technique

MNase digestion coupled with high-throughput sequencing (MNase-seq) is used primarily for mapping nucleosome positioning [60]. Mnase activity does not target Nucleosome associated with DNA making it the ideal enzyme for understanding nucleosome occupancy[61]. As seen in figure one , Mnase induces doubles strand break in regions free of histones[61]. Mnase also exhibits exonuclease activity digestion the digesting the cut DNA until an histone is reached. The histones are then removed leaving behind DNA binding histone regions[61].


Recently Mnase-seq has also been implemented in determining regions of transcription factors binding)[62]. The advantaged of Mnase digesting prior to sequencing for analyses of transcription factors is due to the weak link between transcription factor and chromatin[62]. Unlike histone or nucleosome binding, transcription factors rely on a weak cross link for binding DNA. Other methods such as sonification which require the use of increased temperatures and detergents will interrupt this binding leading to loss of the transcription factor. The use of micrococcal nuclease digesting does not require high temperatures or high a concentrations detergent.



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<refrences /> Category:Molecular biology techniques

MNase-seq

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