Sense (molecular biology)

Last updated December 04, 2023

In molecular biology and genetics, the sense of a nucleic acid molecule, particularly of a strand of DNA or RNA, refers to the nature of the roles of the strand and its complement in specifying a sequence of amino acids.^{[ citation needed ]} Depending on the context, sense may have slightly different meanings. For example, the negative-sense strand of DNA is equivalent to the template strand, whereas the positive-sense strand is the non-template strand whose nucleotide sequence is equivalent to the sequence of the mRNA transcript.

DNA sense

Because of the complementary nature of base-pairing between nucleic acid polymers, a double-stranded DNA molecule will be composed of two strands with sequences that are reverse complements of each other. To help molecular biologists specifically identify each strand individually, the two strands are usually differentiated as the "sense" strand and the "antisense" strand. An individual strand of DNA is referred to as positive-sense (also positive (+) or simply sense) if its nucleotide sequence corresponds directly to the sequence of an RNA transcript which is translated or translatable into a sequence of amino acids (provided that any thymine bases in the DNA sequence are replaced with uracil bases in the RNA sequence). The other strand of the double-stranded DNA molecule is referred to as negative-sense (also negative (−) or antisense), and is reverse complementary to both the positive-sense strand and the RNA transcript. It is actually the antisense strand that is used as the template from which RNA polymerases construct the RNA transcript, but the complementary base-pairing by which nucleic acid polymerization occurs means that the sequence of the RNA transcript will look identical to the positive-sense strand, apart from the RNA transcript's use of uracil instead of thymine.

Sometimes the phrases coding strand and template strand are encountered in place of sense and antisense, respectively, and in the context of a double-stranded DNA molecule the usage of these terms is essentially equivalent. However, the coding/sense strand need not always contain a code that is used to make a protein; both protein-coding and non-coding RNAs may be transcribed.

The terms "sense" and "antisense" are relative only to the particular RNA transcript in question, and not to the DNA strand as a whole. In other words, either DNA strand can serve as the sense or antisense strand. Most organisms with sufficiently large genomes make use of both strands, with each strand functioning as the template strand for different RNA transcripts in different places along the same DNA molecule. In some cases, RNA transcripts can be transcribed in both directions (i.e. on either strand) from a common promoter region, or be transcribed from within introns on either strand (see "ambisense" below).^[1]^[2]^[3]

Sense DNA

The DNA sense strand looks like the messenger RNA (mRNA) transcript, and can therefore be used to read the expected codon sequence that will ultimately be used during translation (protein synthesis) to build an amino acid sequence and then a protein. For example, the sequence "ATG" within a DNA sense strand corresponds to an "AUG" codon in the mRNA, which codes for the amino acid methionine. However, the DNA sense strand itself is not used as the template for the mRNA; it is the DNA antisense strand that serves as the source for the protein code, because, with bases complementary to the DNA sense strand, it is used as a template for the mRNA. Since transcription results in an RNA product complementary to the DNA template strand, the mRNA is complementary to the DNA antisense strand.

Hence, a base triplet 3′-TAC-5′ in the DNA antisense strand (complementary to the 5′-ATG-3′ of the DNA sense strand) is used as the template which results in a 5′-AUG-3′ base triplet in the mRNA. The DNA sense strand will have the triplet ATG, which looks similar to the mRNA triplet AUG but will not be used to make methionine because it will not be directly used to make mRNA. The DNA sense strand is called a "sense" strand not because it will be used to make protein (it won't be), but because it has a sequence that corresponds directly to the RNA codon sequence. By this logic, the RNA transcript itself is sometimes described as "sense".

Example with double-stranded DNA

DNA strand 1: antisense strand (transcribed to) → RNA strand (sense)

DNA strand 2: sense strand

Some regions within a double-stranded DNA molecule code for genes, which are usually instructions specifying the order in which amino acids are assembled to make proteins, as well as regulatory sequences, splicing sites, non-coding introns, and other gene products. For a cell to use this information, one strand of the DNA serves as a template for the synthesis of a complementary strand of RNA. The transcribed DNA strand is called the template strand, with antisense sequence, and the mRNA transcript produced from it is said to be sense sequence (the complement of antisense). The untranscribed DNA strand, complementary to the transcribed strand, is also said to have sense sequence; it has the same sense sequence as the mRNA transcript (though T bases in DNA are substituted with U bases in RNA).

`3′CGCTATAGCGTTT 5′`	DNA antisense strand (template/noncoding)	Used as a template for transcription.
`5′GCGATATCGCAAA 3′`	DNA sense strand (nontemplate/coding)	Complementary to the template strand.
`5′GCGAUAUCGCAAA 3′`	mRNA sense transcript	RNA strand that is transcribed from the noncoding (template/antisense) strand. Note¹: Except for the fact that all thymines are now uracils (`T → U`), it is complementary to the noncoding (template/antisense) DNA strand and identical to the coding (nontemplate/sense) DNA strand.
`3′CGCUAUAGCGUUU 5′`	mRNA antisense transcript	RNA strand that is transcribed from the coding (nontemplate/sense) strand. Note: Except for the fact that all thymines are now uracils (`T → U`), it is complementary to the coding (nontemplate/sense) DNA strand and identical to the noncoding (template/antisense) DNA strand.

The names assigned to each strand actually depend on which direction you are writing the sequence that contains the information for proteins (the "sense" information), not on which strand is depicted as "on the top" or "on the bottom" (which is arbitrary). The only biological information that is important for labeling strands is the relative locations of the terminal 5′ phosphate group and the terminal 3′ hydroxyl group (at the ends of the strand or sequence in question), because these ends determine the direction of transcription and translation. A sequence written 5′-CGCTAT-3′ is equivalent to a sequence written 3′-TATCGC-5′ as long as the 5′ and 3′ ends are noted. If the ends are not labeled, convention is to assume that both sequences are written in the 5′-to-3′ direction. The "Watson strand" refers to 5′-to-3′ top strand (5′→3′), whereas the "Crick strand" refers to the 5′-to-3′ bottom strand (3′←5′).^[4] Both Watson and Crick strands can be either sense or antisense strands depending on the specific gene product made from them.

For example, the notation "YEL021W", an alias of the URA3 gene used in the National Center for Biotechnology Information (NCBI) database, denotes that this gene is in the 21st open reading frame (ORF) from the centromere of the left arm (L) of Yeast (Y) chromosome number V (E), and that the expression coding strand is the Watson strand (W). "YKL074C" denotes the 74th ORF to the left of the centromere of chromosome XI and that the coding strand is the Crick strand (C). Another confusing term referring to "Plus" and "Minus" strand is also widely used. Whether the strand is sense (positive) or antisense (negative), the default query sequence in NCBI BLAST alignment is "Plus" strand.

Ambisense

A single-stranded genome that is used in both positive-sense and negative-sense capacities is said to be ambisense. Some viruses have ambisense genomes. Bunyaviruses have three single-stranded RNA (ssRNA) fragments, some of them containing both positive-sense and negative-sense sections; arenaviruses are also ssRNA viruses with an ambisense genome, as they have three fragments that are mainly negative-sense except for part of the 5′ ends of the large and small segments of their genome.

Antisense RNA

An RNA sequence that is complementary to an endogenous mRNA transcript is sometimes called "antisense RNA". In other words, it is a non-coding strand complementary to the coding sequence of RNA; this is similar to negative-sense viral RNA. When mRNA forms a duplex with a complementary antisense RNA sequence, translation is blocked. This process is related to RNA interference. Cells can produce antisense RNA molecules naturally, called microRNAs, which interact with complementary mRNA molecules and inhibit their expression. The concept has also been exploited as a molecular biology technique, by artificially introducing a transgene coding for antisense RNA in order to block the expression of a gene of interest. Radioactively or fluorescently labelled antisense RNA can be used to show the level of transcription of genes in various cell types.

Some alternative antisense structural types have been experimentally applied as antisense therapy. In the United States, the Food and Drug Administration (FDA) has approved the phosphorothioate antisense oligonucleotides fomivirsen (Vitravene)^[5] and mipomersen (Kynamro)^[6] for human therapeutic use.

RNA sense in viruses

In virology, the term "sense" has a slightly different meaning. The genome of an RNA virus can be said to be either positive-sense, also known as a "plus-strand", or negative-sense, also known as a "minus-strand". In most cases, the terms "sense" and "strand" are used interchangeably, making terms such as "positive-strand" equivalent to "positive-sense", and "plus-strand" equivalent to "plus-sense". Whether a viral genome is positive-sense or negative-sense can be used as a basis for classifying viruses.

Positive-sense

Positive-sense (5′-to-3′) viral RNA signifies that a particular viral RNA sequence may be directly translated into viral proteins (e.g., those needed for viral replication). Therefore, in positive-sense RNA viruses, the viral RNA genome can be considered viral mRNA, and can be immediately translated by the host cell. Unlike negative-sense RNA, positive-sense RNA is of the same sense as mRNA. Some viruses (e.g. Coronaviridae) have positive-sense genomes that can act as mRNA and be used directly to synthesize proteins without the help of a complementary RNA intermediate. Because of this, these viruses do not need to have an RNA polymerase packaged into the virion—the RNA polymerase will be one of the first proteins produced by the host cell, since it is needed in order for the virus's genome to be replicated.

Negative-sense

Negative-sense (3′-to-5′) viral RNA is complementary to the viral mRNA, thus a positive-sense RNA must be produced by an RNA-dependent RNA polymerase from it prior to translation. Like DNA, negative-sense RNA has a nucleotide sequence complementary to the mRNA that it encodes; also like DNA, this RNA cannot be translated into protein directly. Instead, it must first be transcribed into a positive-sense RNA that acts as an mRNA. Some viruses (e.g. influenza viruses) have negative-sense genomes and so must carry an RNA polymerase inside the virion.

Antisense oligonucleotides

Gene silencing can be achieved by introducing into cells a short "antisense oligonucleotide" that is complementary to an RNA target. This experiment was first done by Zamecnik and Stephenson in 1978^[7] and continues to be a useful approach, both for laboratory experiments and potentially for clinical applications (antisense therapy).^[8] Several viruses, such as influenza viruses^[9]^[10]^[11]^[12] Respiratory syncytial virus (RSV)^[9] and SARS coronavirus (SARS-CoV),^[9] have been targeted using antisense oligonucleotides to inhibit their replication in host cells.

If the antisense oligonucleotide contains a stretch of DNA or a DNA mimic (phosphorothioate DNA, 2′F-ANA, or others) it can recruit RNase H to degrade the target RNA. This makes the mechanism of gene silencing catalytic. Double-stranded RNA can also act as a catalytic, enzyme-dependent antisense agent through the RNAi/siRNA pathway, involving target mRNA recognition through sense-antisense strand pairing followed by target mRNA degradation by the RNA-induced silencing complex (RISC). The R1 plasmid hok/sok system provides yet another example of an enzyme-dependent antisense regulation process through enzymatic degradation of the resulting RNA duplex.

Other antisense mechanisms are not enzyme-dependent, but involve steric blocking of their target RNA (e.g. to prevent translation or to induce alternative splicing). Steric blocking antisense mechanisms often use oligonucleotides that are heavily modified. Since there is no need for RNase H recognition, this can include chemistries such as 2′-O-alkyl, peptide nucleic acid (PNA), locked nucleic acid (LNA), and Morpholino oligomers.

Related Research Articles

Ribonucleic acid (RNA) is a polymeric molecule that is essential for most biological functions, either by performing the function itself or by forming a template for the production of proteins. RNA and deoxyribonucleic acid (DNA) are nucleic acids. The nucleic acids constitute one of the four major macromolecules essential for all known forms of life. RNA is assembled as a chain of nucleotides. Cellular organisms use messenger RNA (mRNA) to convey genetic information that directs synthesis of specific proteins. Many viruses encode their genetic information using an RNA genome.

An RNA virus is a virus—other than a retrovirus—that has ribonucleic acid (RNA) as its genetic material. The nucleic acid is usually single-stranded RNA (ssRNA) but it may be double-stranded (dsRNA). Notable human diseases caused by RNA viruses include the common cold, influenza, SARS, MERS, COVID-19, Dengue Virus, hepatitis C, hepatitis E, West Nile fever, Ebola virus disease, rabies, polio, mumps, and measles.

A reverse transcriptase (RT) is an enzyme used to generate complementary DNA (cDNA) from an RNA template, a process termed reverse transcription. Reverse transcriptases are used by viruses such as HIV and hepatitis B to replicate their genomes, by retrotransposon mobile genetic elements to proliferate within the host genome, and by eukaryotic cells to extend the telomeres at the ends of their linear chromosomes. Contrary to a widely held belief, the process does not violate the flows of genetic information as described by the classical central dogma, as transfers of information from RNA to DNA are explicitly held possible.

Transcription is the process of copying a segment of DNA into RNA. The segments of DNA transcribed into RNA molecules that can encode proteins are said to produce messenger RNA (mRNA). Other segments of DNA are copied into RNA molecules called non-coding RNAs (ncRNAs). mRNA comprises only 1–3% of total RNA samples. Less than 2% of the human genome can be transcribed into mRNA, while at least 80% of mammalian genomic DNA can be actively transcribed, with the majority of this 80% considered to be ncRNA.

Oligonucleotides are short DNA or RNA molecules, oligomers, that have a wide range of applications in genetic testing, research, and forensics. Commonly made in the laboratory by solid-phase chemical synthesis, these small fragments of nucleic acids can be manufactured as single-stranded molecules with any user-specified sequence, and so are vital for artificial gene synthesis, polymerase chain reaction (PCR), DNA sequencing, molecular cloning and as molecular probes. In nature, oligonucleotides are usually found as small RNA molecules that function in the regulation of gene expression, or are degradation intermediates derived from the breakdown of larger nucleic acid molecules.

A nucleic acid sequence is a succession of bases within the nucleotides forming alleles within a DNA or RNA (GACU) molecule. This succession is denoted by a series of a set of five different letters that indicate the order of the nucleotides. By convention, sequences are usually presented from the 5' end to the 3' end. For DNA, with its double helix, there are two possible directions for the notated sequence; of these two, the sense strand is used. Because nucleic acids are normally linear (unbranched) polymers, specifying the sequence is equivalent to defining the covalent structure of the entire molecule. For this reason, the nucleic acid sequence is also termed the primary structure.

When referring to DNA transcription, the coding strand is the DNA strand whose base sequence is identical to the base sequence of the RNA transcript produced. It is this strand which contains codons, while the non-coding strand contains anticodons. During transcription, RNA Pol II binds to the non-coding template strand, reads the anti-codons, and transcribes their sequence to synthesize an RNA transcript with complementary bases.

In molecular biology, a reading frame is a way of dividing the sequence of nucleotides in a nucleic acid molecule into a set of consecutive, non-overlapping triplets. Where these triplets equate to amino acids or stop signals during translation, they are called codons.

Antisense RNA (asRNA), also referred to as antisense transcript, natural antisense transcript (NAT) or antisense oligonucleotide, is a single stranded RNA that is complementary to a protein coding messenger RNA (mRNA) with which it hybridizes, and thereby blocks its translation into protein. The asRNAs have been found in both prokaryotes and eukaryotes, and can be classified into short and long non-coding RNAs (ncRNAs). The primary function of asRNA is regulating gene expression. asRNAs may also be produced synthetically and have found wide spread use as research tools for gene knockdown. They may also have therapeutic applications.

<span class="mw-page-title-main">Primary transcript</span> RNA produced by transcription

A primary transcript is the single-stranded ribonucleic acid (RNA) product synthesized by transcription of DNA, and processed to yield various mature RNA products such as mRNAs, tRNAs, and rRNAs. The primary transcripts designated to be mRNAs are modified in preparation for translation. For example, a precursor mRNA (pre-mRNA) is a type of primary transcript that becomes a messenger RNA (mRNA) after processing.

Viral replication is the formation of biological viruses during the infection process in the target host cells. Viruses must first get into the cell before viral replication can occur. Through the generation of abundant copies of its genome and packaging these copies, the virus continues infecting new hosts. Replication between viruses is greatly varied and depends on the type of genes involved in them. Most DNA viruses assemble in the nucleus while most RNA viruses develop solely in cytoplasm.

Baltimore classification is a system used to classify viruses based on their manner of messenger RNA (mRNA) synthesis. By organizing viruses based on their manner of mRNA production, it is possible to study viruses that behave similarly as a distinct group. Seven Baltimore groups are described that take into consideration whether the viral genome is made of deoxyribonucleic acid (DNA) or ribonucleic acid (RNA), whether the genome is single- or double-stranded, and whether the sense of a single-stranded RNA genome is positive or negative.

In genetics, a sense strand, or coding strand, is the segment within double-stranded DNA that carries the translatable code in the 5′ to 3′ direction, and which is complementary to the antisense strand of DNA, or template strand, which does not carry the translatable code in the 5′ to 3′ direction. The sense strand is the strand of DNA that has the same sequence as the mRNA, which takes the antisense strand as its template during transcription, and eventually undergoes translation into a protein. The antisense strand is thus responsible for the RNA that is later translated to protein, while the sense strand possesses a nearly identical makeup to that of the mRNA.

Directionality, in molecular biology and biochemistry, is the end-to-end chemical orientation of a single strand of nucleic acid. In a single strand of DNA or RNA, the chemical convention of naming carbon atoms in the nucleotide pentose-sugar-ring means that there will be a 5′ end, which frequently contains a phosphate group attached to the 5′ carbon of the ribose ring, and a 3′ end, which typically is unmodified from the ribose -OH substituent. In a DNA double helix, the strands run in opposite directions to permit base pairing between them, which is essential for replication or transcription of the encoded information.

RNA-based evolution is a theory that posits that RNA is not merely an intermediate between Watson and Crick model of the DNA molecule and proteins, but rather a far more dynamic and independent role-player in determining phenotype. By regulating the transcription in DNA sequences, the stability of RNA, and the capability of messenger RNA to be translated, RNA processing events allow for a diverse array of proteins to be synthesized from a single gene. Since RNA processing is heritable, it is subject to natural selection suggested by Darwin and contributes to the evolution and diversity of most eukaryotic organisms.

In molecular biology, complementarity describes a relationship between two structures each following the lock-and-key principle. In nature complementarity is the base principle of DNA replication and transcription as it is a property shared between two DNA or RNA sequences, such that when they are aligned antiparallel to each other, the nucleotide bases at each position in the sequences will be complementary, much like looking in the mirror and seeing the reverse of things. This complementary base pairing allows cells to copy information from one generation to another and even find and repair damage to the information stored in the sequences.

Polypurine reverse-Hoogsteen hairpins (PPRHs) are non-modified oligonucleotides containing two polypurine domains, in a mirror repeat fashion, linked by a pentathymidine stretch forming double-stranded DNA stem-loop molecules. The two polypurine domains interact by intramolecular reverse-Hoogsteen bonds allowing the formation of this specific hairpin structure.

Monodnaviria is a realm of viruses that includes all single-stranded DNA viruses that encode an endonuclease of the HUH superfamily that initiates rolling circle replication of the circular viral genome. Viruses descended from such viruses are also included in the realm, including certain linear single-stranded DNA (ssDNA) viruses and circular double-stranded DNA (dsDNA) viruses. These atypical members typically replicate through means other than rolling circle replication.

This glossary of genetics is a list of definitions of terms and concepts commonly used in the study of genetics and related disciplines in biology, including molecular biology, cell biology, and evolutionary biology. It is intended as introductory material for novices; for more specific and technical detail, see the article corresponding to each term. For related terms, see Glossary of evolutionary biology.

This glossary of cell and molecular biology is a list of definitions of terms and concepts commonly used in the study of cell biology, molecular biology, and related disciplines, including genetics, microbiology, and biochemistry. It is split across two articles:

References

↑ Anne-Lise Haenni (2003). "Expression strategies of ambisense viruses". Virus Research. 93 (2): 141–150. doi:10.1016/S0168-1702(03)00094-7. PMID 12782362.
↑ Kakutani T; Hayano Y; Hayashi T; Minobe Y. (1991). "Ambisense segment 3 of rice stripe virus: the first instance of a virus containing two ambisense segments". J Gen Virol. 72 (2): 465–8. doi: 10.1099/0022-1317-72-2-465 . PMID 1993885.
↑ Zhu Y; Hayakawa T; Toriyama S; Takahashi M. (1991). "Complete nucleotide sequence of RNA 3 of rice stripe virus: an ambisense coding strategy". J Gen Virol. 72 (4): 763–7. doi: 10.1099/0022-1317-72-4-763 . PMID 2016591.
↑ Cartwright, Reed; Dan Graur (Feb 8, 2011). "The multiple personalities of Watson and Crick strands". Biology Direct. 6: 7. doi: 10.1186/1745-6150-6-7 . PMC 3055211 . PMID 21303550.
↑ "FDA approves fomivirsen for CMV". healio. 1 October 1998. Retrieved 18 September 2020.
↑ "FDA approves orphan drug for inherited cholesterol disorder". Drug Topics. 30 January 2013. Retrieved 18 September 2020.
↑ Zamecnik, P.C.; Stephenson, M.L. (1978). "Inhibition of Rous sarcoma Virus Replication and Cell Transformation by a Specific Oligodeoxynucleotide". Proc. Natl. Acad. Sci. USA. 75 (1): 280–284. Bibcode:1978PNAS...75..280Z. doi: 10.1073/pnas.75.1.280 . PMC 411230 . PMID 75545.
↑ Watts, J.K.; Corey, D.R. (2012). "Silencing Disease Genes in the Laboratory and in the Clinic". J. Pathol. 226 (2): 365–379. doi:10.1002/path.2993. PMC 3916955 . PMID 22069063.
1 2 3 Kumar, Binod; Khanna, Madhu; Meseko, Clement A.; Sanicas, Melvin; Kumar, Prashant; Asha, Kumari; Asha, Kumari; Kumar, Prashant; Sanicas, Melvin (January 2019). "Advancements in Nucleic Acid Based Therapeutics against Respiratory Viral Infections". Journal of Clinical Medicine. 8 (1): 6. doi: 10.3390/jcm8010006 . PMC 6351902 . PMID 30577479.
↑ Kumar, Binod; Asha, Kumari; Khanna, Madhu; Ronsard, Larance; Meseko, Clement Adebajo; Sanicas, Melvin (2018-01-10). "The emerging influenza virus threat: status and new prospects for its therapy and control". Archives of Virology. 163 (4): 831–844. doi:10.1007/s00705-018-3708-y. ISSN 0304-8608. PMC 7087104 . PMID 29322273.
↑ Kumar, Prashant; Kumar, Binod; Rajput, Roopali; Saxena, Latika; Banerjea, Akhil C.; Khanna, Madhu (2013-06-02). "Cross-Protective Effect of Antisense Oligonucleotide Developed Against the Common 3′ NCR of Influenza A Virus Genome". Molecular Biotechnology. 55 (3): 203–211. doi:10.1007/s12033-013-9670-8. ISSN 1073-6085. PMID 23729285. S2CID 24496875.
↑ Kumar, B.; Khanna, Madhu; Kumar, P.; Sood, V.; Vyas, R.; Banerjea, A. C. (2011-07-09). "Nucleic Acid-Mediated Cleavage of M1 Gene of Influenza A Virus Is Significantly Augmented by Antisense Molecules Targeted to Hybridize Close to the Cleavage Site". Molecular Biotechnology. 51 (1): 27–36. doi:10.1007/s12033-011-9437-z. ISSN 1073-6085. PMID 21744034. S2CID 45686564.

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[1] Anne-Lise Haenni (2003). "Expression strategies of ambisense viruses". Virus Research. 93 (2): 141–150. doi:10.1016/S0168-1702(03)00094-7. PMID 12782362.

[2] Kakutani T; Hayano Y; Hayashi T; Minobe Y. (1991). "Ambisense segment 3 of rice stripe virus: the first instance of a virus containing two ambisense segments". J Gen Virol. 72 (2): 465–8. doi: 10.1099/0022-1317-72-2-465 . PMID 1993885.

[3] Zhu Y; Hayakawa T; Toriyama S; Takahashi M. (1991). "Complete nucleotide sequence of RNA 3 of rice stripe virus: an ambisense coding strategy". J Gen Virol. 72 (4): 763–7. doi: 10.1099/0022-1317-72-4-763 . PMID 2016591.

[4] Cartwright, Reed; Dan Graur (Feb 8, 2011). "The multiple personalities of Watson and Crick strands". Biology Direct. 6: 7. doi: 10.1186/1745-6150-6-7 . PMC 3055211 . PMID 21303550.

[5] "FDA approves fomivirsen for CMV". healio. 1 October 1998. Retrieved 18 September 2020.

[6] "FDA approves orphan drug for inherited cholesterol disorder". Drug Topics. 30 January 2013. Retrieved 18 September 2020.

[7] Zamecnik, P.C.; Stephenson, M.L. (1978). "Inhibition of Rous sarcoma Virus Replication and Cell Transformation by a Specific Oligodeoxynucleotide". Proc. Natl. Acad. Sci. USA. 75 (1): 280–284. Bibcode:1978PNAS...75..280Z. doi: 10.1073/pnas.75.1.280 . PMC 411230 . PMID 75545.

[8] Watts, J.K.; Corey, D.R. (2012). "Silencing Disease Genes in the Laboratory and in the Clinic". J. Pathol. 226 (2): 365–379. doi:10.1002/path.2993. PMC 3916955 . PMID 22069063.

[:0-9] 1 2 3 Kumar, Binod; Khanna, Madhu; Meseko, Clement A.; Sanicas, Melvin; Kumar, Prashant; Asha, Kumari; Asha, Kumari; Kumar, Prashant; Sanicas, Melvin (January 2019). "Advancements in Nucleic Acid Based Therapeutics against Respiratory Viral Infections". Journal of Clinical Medicine. 8 (1): 6. doi: 10.3390/jcm8010006 . PMC 6351902 . PMID 30577479.

[10] Kumar, Binod; Asha, Kumari; Khanna, Madhu; Ronsard, Larance; Meseko, Clement Adebajo; Sanicas, Melvin (2018-01-10). "The emerging influenza virus threat: status and new prospects for its therapy and control". Archives of Virology. 163 (4): 831–844. doi:10.1007/s00705-018-3708-y. ISSN 0304-8608. PMC 7087104 . PMID 29322273.

[11] Kumar, Prashant; Kumar, Binod; Rajput, Roopali; Saxena, Latika; Banerjea, Akhil C.; Khanna, Madhu (2013-06-02). "Cross-Protective Effect of Antisense Oligonucleotide Developed Against the Common 3′ NCR of Influenza A Virus Genome". Molecular Biotechnology. 55 (3): 203–211. doi:10.1007/s12033-013-9670-8. ISSN 1073-6085. PMID 23729285. S2CID 24496875.

[12] Kumar, B.; Khanna, Madhu; Kumar, P.; Sood, V.; Vyas, R.; Banerjea, A. C. (2011-07-09). "Nucleic Acid-Mediated Cleavage of M1 Gene of Influenza A Virus Is Significantly Augmented by Antisense Molecules Targeted to Hybridize Close to the Cleavage Site". Molecular Biotechnology. 51 (1): 27–36. doi:10.1007/s12033-011-9437-z. ISSN 1073-6085. PMID 21744034. S2CID 45686564.

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