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Morpholino

Morpholino

Overview
In molecular biology
Molecular biology
Molecular biology is the study of biology at a molecular level. The field overlaps with other areas of biology and chemistry, particularly genetics and biochemistry...

, a Morpholino is a molecule
Molecule
A molecule is defined as an electrically neutral group of at least two atoms in a definite arrangement held together by very strong chemical bonds. Molecules are distinguished from polyatomic ions in this strict sense...

 used to modify gene expression
Gene expression
Gene expression is the process by which information from a gene is used in the synthesis of a functional gene product. These products are often proteins, but in non-protein coding genes such as rRNA genes or tRNA genes, the product is a functional RNA...

. Morpholino oligomer
Oligomer
In chemistry, an oligomer consists of a less than five number of monomer units , in contrast to a polymer that, at least in principle, consists of an unlimited number of monomers. Many oils are oligomeric, such as liquid paraffin. Plasticizers are oligomeric esters widely used to soften...

s (oligos) are an antisense technology used to block access of other molecules to specific sequences within nucleic acid
Nucleic acid
A nucleic acid is a macromolecule composed of chains of monomeric nucleotides. In biochemistry these molecules carry genetic information or form structures within cells. The most common nucleic acids are deoxyribonucleic acid and ribonucleic acid . Nucleic acids are universal in living things, as...

. Morpholinos block small (~25 base) regions of the base-pairing surfaces of ribonucleic acid (RNA
RNA
Ribonucleic acid is a biologically important type of molecule that consists of a long chain of nucleotide units. Each nucleotide consists of a nitrogenous base, a ribose sugar, and a phosphate...

).

This article discusses only the Morpholino antisense oligos, which are nucleic acid analogs
Nucleic acid analogues
Nucleic acid analogues are compounds structurally similar to naturally occurring RNA and DNA, used in medicine and in molecular biology research....

. The word "morpholino" can occur in other chemical names, referring to chemicals containing a six-membered morpholine
Morpholine
Morpholine is an organic chemical compound having the chemical formula O2NH. This heterocycle, pictured at right, features both amine and ether functional groups. Because of the amine, morpholine is a base; its conjugate acid is called morpholinium...

 ring.
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Encyclopedia
In molecular biology
Molecular biology
Molecular biology is the study of biology at a molecular level. The field overlaps with other areas of biology and chemistry, particularly genetics and biochemistry...

, a Morpholino is a molecule
Molecule
A molecule is defined as an electrically neutral group of at least two atoms in a definite arrangement held together by very strong chemical bonds. Molecules are distinguished from polyatomic ions in this strict sense...

 used to modify gene expression
Gene expression
Gene expression is the process by which information from a gene is used in the synthesis of a functional gene product. These products are often proteins, but in non-protein coding genes such as rRNA genes or tRNA genes, the product is a functional RNA...

. Morpholino oligomer
Oligomer
In chemistry, an oligomer consists of a less than five number of monomer units , in contrast to a polymer that, at least in principle, consists of an unlimited number of monomers. Many oils are oligomeric, such as liquid paraffin. Plasticizers are oligomeric esters widely used to soften...

s (oligos) are an antisense technology used to block access of other molecules to specific sequences within nucleic acid
Nucleic acid
A nucleic acid is a macromolecule composed of chains of monomeric nucleotides. In biochemistry these molecules carry genetic information or form structures within cells. The most common nucleic acids are deoxyribonucleic acid and ribonucleic acid . Nucleic acids are universal in living things, as...

. Morpholinos block small (~25 base) regions of the base-pairing surfaces of ribonucleic acid (RNA
RNA
Ribonucleic acid is a biologically important type of molecule that consists of a long chain of nucleotide units. Each nucleotide consists of a nitrogenous base, a ribose sugar, and a phosphate...

).

This article discusses only the Morpholino antisense oligos, which are nucleic acid analogs
Nucleic acid analogues
Nucleic acid analogues are compounds structurally similar to naturally occurring RNA and DNA, used in medicine and in molecular biology research....

. The word "morpholino" can occur in other chemical names, referring to chemicals containing a six-membered morpholine
Morpholine
Morpholine is an organic chemical compound having the chemical formula O2NH. This heterocycle, pictured at right, features both amine and ether functional groups. Because of the amine, morpholine is a base; its conjugate acid is called morpholinium...

 ring. To help avoid confusion with other morpholine-containing molecules, when describing oligos "Morpholino" is often capitalized as a trade name
Trade name
A trade name, also known as a trading name or a business name, is the name which a business trades under for commercial purposes, although its registered, legal name, used for contracts and other formal situations, may be another....

, though this usage is not consistent throughout the scientific literature. Morpholinos are sometimes referred to as PMO (phosphorodiamidate morpholino oligo).

Morpholinos are usually used as a research tool for reverse genetics
Reverse genetics
Reverse genetics is an approach to discovering the function of a gene that proceeds in the opposite direction of so called forward genetic screens of classical genetics...

 by knocking down
Gene knockdown
Gene knockdown refers to techniques by which the expression of one or more of an organism's genes is reduced, either through genetic modification or by treatment with a reagent such as a short DNA or RNA oligonucleotide with a sequence complementary to either an mRNA transcript or a gene...

 gene function. This is achieved by preventing cells from making a targeted protein
Protein
Proteins are organic compounds made of amino acids arranged in a linear chain and folded into a globular form. The amino acids in a polymer chain are joined together by the peptide bonds between the carboxyl and amino groups of adjacent amino acid residues...

 or by modifying the splicing
Splicing (genetics)
In molecular biology, splicing is a modification of an RNA after transcription, in which introns are removed and exons are joined. This is needed for the typical eukaryotic messenger RNA before it can be used to produce a correct protein through translation...

 of pre-mRNA. Knocking down gene expression is a powerful method for learning about the function of a particular protein; similarly, causing a specific exon
Exon
An exon is a nucleic acid sequence that is represented in the mature form of an RNA molecule after either portions of a precursor RNA have been removed by cis-splicing or by two or more precursor RNA molecules have been ligated by trans-splicing. The mature RNA molecule can be a messenger RNA or...

 to be spliced out of a protein can help to determine the function of the protein moiety encoded
Genetic code
The genetic code is the set of rules by which information encoded in genetic material is translated into proteins by living cells. A more precise term for the concept might be "genetic cipher". The code defines a mapping between tri-nucleotide sequences, called codons, and amino acids...

 by that exon. These molecules have been applied to studies in several model organism
Model organism
A model organism is a species that is extensively studied to understand particular biological phenomena, with the expectation that discoveries made in the organism model will provide insight into the workings of other organisms...

s, including mice
Mouse
A mouse is a small mammal belonging to the order of rodents. The best known mouse species is the common house mouse . It is also a popular pet. The American white-footed mouse and the deer mouse also sometimes live in houses. In some places, certain kinds of field mice are also common...

, zebrafish, frog
Xenopus
Xenopus is a genus of highly aquatic frogs native to Sub-Saharan Africa. There are 18 species in the Xenopus genus...

s, and sea urchin
Sea urchin
Sea urchins or urchins are small, spiny, globular animals that compose part of class Echinoidea. They are found in oceans all over the world. Their shell, or "test", is round and spiny, typically from 3 to 10 cm across. Common colors include black and dull shades of green, olive, brown, purple,...

s.

Morpholinos are also in development as pharmaceutical
Pharmacology
Pharmacology is the study of drug action. More specifically, it is the study of the interactions that occur between a living organism and exogenous chemicals that alter normal biochemical function. If substances have medicinal properties, they are considered pharmaceuticals...

 therapeutics targeted against pathogen
Pathogen
A pathogen , infectious agent, or germ, is a biological agent that causes disease or illness to its host....

ic organisms such as bacteria
Bacteria
The bacteria are a large group of unicellular microorganisms. Typically a few micrometres in length, bacteria have a wide range of shapes, ranging from spheres to rods and spirals...

 or virus
Virus
A virus is an infectious agent too small to be seen directly with a light microscope. They are not made of cells and can only replicate inside the cells of another organism . Viruses infect all types of organisms, from animals and plants to bacteria and archaea...

es and for amelioration of genetic diseases
Genetic disorder
A genetic disorder is an illness caused by abnormalities in genes or chromosomes. While some diseases, such as cancer, are due in part to a genetic disorders, they can also be caused by environmental factors. Most disorders are quite rare and affect one person in every several thousands or millions...

. These synthetic oligos were conceived by James E. Summerton (Gene Tools, LLC
Gene Tools
Gene Tools, LLC is a limited liability company located in Philomath, Oregon, United States that manufactures Morpholino antisense oligos and delivery reagents. Gene Tools was founded in 1997 and began regularly shipping custom-sequence Morpholino oligos in 2000. The manager and general partner, Dr...

) and developed in collaboration with Dwight D. Weller (AVI BioPharma Inc.
AVI Bio Pharma
AVI BioPharma Inc. is a medical research and drug development company with corporate offices in Portland, Oregon, United States, and laboratories in Corvallis, Oregon. It was incorporated in 1980...

).

Structure


Morpholinos are synthetic
Chemical synthesis
In chemistry, chemical synthesis is purposeful execution of chemical reactions to get a product, or several products. This happens by physical and chemical manipulations usually involving one or more reactions...

 molecule
Molecule
A molecule is defined as an electrically neutral group of at least two atoms in a definite arrangement held together by very strong chemical bonds. Molecules are distinguished from polyatomic ions in this strict sense...

s which are the product of a redesign of natural nucleic acid structure. Usually 25 bases in length, they bind to complementary sequences of RNA by standard nucleic acid base-pairing
Base pair
In molecular biology, two nucleotides on opposite complementary DNA or RNA strands that are connected via hydrogen bonds are called a base pair . In the canonical Watson-Crick base pairing, adenine forms a base pair with thymine , as does guanine with cytosine in DNA. In RNA, thymine is replaced...

. Structurally, the difference between Morpholinos and DNA
DNA
Deoxyribonucleic acid is a nucleic acid that contains the genetic instructions used in the development and functioning of all known living organisms and some viruses. The main role of DNA molecules is the long-term storage of information...

 is that while Morpholinos have standard nucleic acid bases, those bases are bound to morpholine
Morpholine
Morpholine is an organic chemical compound having the chemical formula O2NH. This heterocycle, pictured at right, features both amine and ether functional groups. Because of the amine, morpholine is a base; its conjugate acid is called morpholinium...

 rings instead of deoxyribose
Deoxyribose
Deoxyribose, also known as D-Deoxyribose and 2-deoxyribose, is an aldopentose — a monosaccharide containing five carbon atoms, and including an aldehyde functional group in its linear structure...

 rings and linked through phosphorodiamidate groups instead of phosphates. This may be easiest to visualize by referring to the first figure and comparing the structures of the two strands depicted there, one of RNA and the other of a Morpholino. Replacement of anionic
Ion
An ion is an atom or molecule where the total number of electrons is not equal to the total number of protons, giving it a net positive or negative electrical charge...

 phosphates with the uncharged phosphorodiamidate groups eliminates ionization in the usual physiological pH
PH
pH is a measure of the acidity or basicity of a solution. It is defined as the cologarithm of the activity of dissolved hydrogen ions . Hydrogen ion activity coefficients cannot be measured experimentally, so they are based on theoretical calculations...

 range, so Morpholinos in organisms or cells are uncharged molecules. The entire backbone of a Morpholino is made from these modified subunits. Morpholinos are most commonly used as single-stranded oligos, though heteroduplex
Heteroduplex
A heteroduplex is a double-stranded molecule of nucleic acid originated through the genetic recombination of single complementary strands derived from different sources, such as from different homologous chromosomes or even from different organisms....

es of a Morpholino strand and a complementary
Complementarity (molecular biology)
In molecular biology, complementarity is a property of double-stranded nucleic acids such as DNA and RNA as well as DNA:RNA duplexes. Each strand is complementary to the other in that the base pairs between them are non-covalently connected via two or three hydrogen bonds.Since there is only one...

 DNA strand may be used in combination with cationic cytosol
Cytosol
The cytosol or intracellular fluid is the liquid found inside cells. In eukaryotes this liquid is separated by cell membranes from the contents of the organelles suspended in the cytosol, such as the mitochondrial matrix inside the mitochondrion...

ic delivery reagents.

Function


Morpholinos do not degrade their target RNA molecules, unlike many antisense structural types (e.g. phosphorothioates, siRNA
Sírna
Sírna Sáeglach , son of Dian, son of Demal, son of Rothechtaid mac Main, was, according to medieval Irish legend and historical tradition, a High King of Ireland...

). Instead, Morpholinos act by "steric blocking", binding to a target sequence within an RNA and simply getting in the way of molecules which might otherwise interact with the RNA.

Morpholino oligos are often used to investigate the role of a specific mRNA transcript in an embryo. Developmental biologists inject Morpholino oligos into eggs or embryos of zebrafish, African clawed frog (Xenopus
Xenopus
Xenopus is a genus of highly aquatic frogs native to Sub-Saharan Africa. There are 18 species in the Xenopus genus...

), and sea urchin
Sea urchin
Sea urchins or urchins are small, spiny, globular animals that compose part of class Echinoidea. They are found in oceans all over the world. Their shell, or "test", is round and spiny, typically from 3 to 10 cm across. Common colors include black and dull shades of green, olive, brown, purple,...

, producing morphant
Morphant
An organism which has been treated with a Morpholino antisense oligo to temporarily knock down expression of a targeted gene is called a Morphant.-Background:...

 embryos, or electroporate Morpholinos into chick
Chicken
The chicken is a domesticated fowl. As one of the most common and widespread domestic animals, and with a population of more than 24 billion in 2003, there are more chickens in the world than any other bird...

 embryos at later stages of development. With appropriate cytosolic delivery systems, Morpholinos are effective in cell culture
Cell culture
Cell culture is the process by which cells are grown under controlled conditions. In practice the term "cell culture" has come to refer to the culturing of cells derived from multicellular eukaryotes, especially animal cells...

.

Morpholinos are being developed as pharmaceuticals under the name "NeuGenes" by AVI BioPharma Inc. They have been used in mammals ranging from mice
Mouse
A mouse is a small mammal belonging to the order of rodents. The best known mouse species is the common house mouse . It is also a popular pet. The American white-footed mouse and the deer mouse also sometimes live in houses. In some places, certain kinds of field mice are also common...

 to humans and some are currently being tested in clinical trial
Clinical trial
Clinical trials are conducted to allow safety and efficacy data to be collected for new drugs or devices. These trials can only take place once satisfactory information has been gathered on the quality of the product and its non-clinical safety, and Health Authority/Ethics Committee approval is...

s for treatment of Duchenne muscular dystrophy
Duchenne muscular dystrophy
Duchenne muscular dystrophy is a severe recessive X-linked form of muscular dystrophy characterized by rapid progression of muscle degeneration, eventually leading to loss of ambulation and death. This affliction affects one in 3500 males, making it the most prevalent of muscular dystrophies. In...

.

Normal gene expression in eukaryotes



In eukaryotic
Eukaryote
A eukaryote is an organism whose cells contain complex structures enclosed within membranes. The defining membrane-bound structure that sets eukaryotic cells apart from prokaryotic cells is the nucleus, or nuclear envelope, within which the genetic material is carried...

 organisms, pre-mRNA is transcribed
Transcription (genetics)
Transcription, or RNA synthesis, is the process of creating an equivalent RNA copy of a sequence of DNA. Both RNA and DNA are nucleic acids, which use base pairs of nucleotides as a complementary language that can be converted back and forth from DNA to RNA in the presence of the correct enzymes...

 in the nucleus, introns are spliced
Splicing (genetics)
In molecular biology, splicing is a modification of an RNA after transcription, in which introns are removed and exons are joined. This is needed for the typical eukaryotic messenger RNA before it can be used to produce a correct protein through translation...

 out, then the mature mRNA is exported from the nucleus
Cell nucleus
In cell biology, the nucleus , also sometimes referred to as the "control center", is a membrane-enclosed organelle found in eukaryotic cells. It contains most of the cell's genetic material, organized as multiple long linear DNA molecules in complex with a large variety of proteins, such as...

 to the cytoplasm
Cytoplasm
The cytoplasm is the part of a cell that is enclosed within the cell membrane. In eukaryotic cells, the cytoplasm contains organelles, such as mitochondria, which are filled with liquid that is kept separate from the rest of the cytoplasm by biological membranes. The contents of the cell nucleus...

. The small subunit of the ribosome
Ribosome
Ribosomes are complexes of RNA and protein that are found in all cells. The ribosome is part of the mechanism that translates the DNA sequence into the protein sequence. Ribosomes from bacteria, archaea and eukaryotes , have significantly different structure and RNA...

 usually starts by binding to one end of the mRNA and is joined there by various other eukaryotic initiation factor
Eukaryotic initiation factor
Eukaryotic initiation factors are proteins used in eukaryotic translation. There exist many more eukaryotic initiation factors than prokaryotic initiation factors due to greater biological complexity...

s, forming the initiation complex. The initiation complex scans along the mRNA strand until it reaches a start codon
Start codon
ATG and AUG denote sequences of DNA and RNA respectively that are the start codon or initiation codon encoding the amino acid methionine in eukaryotes and a modified Met in prokaryotes....

, and then the large subunit of the ribosome attaches to the small subunit and translation of a protein
Protein
Proteins are organic compounds made of amino acids arranged in a linear chain and folded into a globular form. The amino acids in a polymer chain are joined together by the peptide bonds between the carboxyl and amino groups of adjacent amino acid residues...

 begins. This entire process is referred to as gene expression; it is the process by which the information in a gene
Gene
A gene is the basic unit of heredity in a living organism. All living things depend on genes. Genes hold the information to build and maintain their cells and pass genetic traits to offspring...

, encoded as a sequence of bases in DNA
DNA
Deoxyribonucleic acid is a nucleic acid that contains the genetic instructions used in the development and functioning of all known living organisms and some viruses. The main role of DNA molecules is the long-term storage of information...

, is converted into the structure of a protein. A Morpholino can modify splicing or block translation, depending on the Morpholino's base sequence.

Blocking translation



Bound to the 5'-untranslated region of messenger RNA (mRNA), Morpholinos can interfere with progression of the ribosomal
Ribosome
Ribosomes are complexes of RNA and protein that are found in all cells. The ribosome is part of the mechanism that translates the DNA sequence into the protein sequence. Ribosomes from bacteria, archaea and eukaryotes , have significantly different structure and RNA...

 initiation complex from the 5' cap to the start codon. This prevents translation of the coding region of the targeted transcript
Transcript
Transcript may refer to:* An RNA molecule, a type of compound produced directly from genes* Transcript , a copy of a student's permanent academic record* Transcript , the documented medical record of patients...

 (called "knocking down
Gene knockdown
Gene knockdown refers to techniques by which the expression of one or more of an organism's genes is reduced, either through genetic modification or by treatment with a reagent such as a short DNA or RNA oligonucleotide with a sequence complementary to either an mRNA transcript or a gene...

" gene expression
Gene expression
Gene expression is the process by which information from a gene is used in the synthesis of a functional gene product. These products are often proteins, but in non-protein coding genes such as rRNA genes or tRNA genes, the product is a functional RNA...

). This is useful experimentally when an investigator wishes to know the function of a particular protein; Morpholinos provide a convenient means of knocking down expression of the protein and learning how that knockdown changes the cells or organism. Some Morpholinos knock down expression so effectively that, after degradation of preexisting proteins, the targeted proteins become undetectable by Western blot
Western blot
The western blot is an analytical technique used to detect specific proteins in a given sample of tissue homogenate or extract. It uses gel electrophoresis to separate native or denatured proteins by the length of the polypeptide or by the 3-D structure of the protein...

 (e.g. figure 1 in:).

Modifying pre-mRNA splicing



Morpholinos can interfere with pre-mRNA processing steps either by preventing splice-directing small nuclear ribonucleoproteins (snRNP
SnRNP
snRNPs , or small nuclear ribonucleoproteins, are particles that combine with pre-mRNA and various proteins to form spliceosomes . SnRNPs "recognize" the places along a strand of pre-mRNA and are essential in the removal of introns...

) complexes from binding to their targets at the borders of introns on a strand of pre-mRNA, or by blocking the nucleophilic
Nucleophile
In chemistry, a nucleophile is a reagent that forms a chemical bond to its reaction partner by donating both bonding electrons. Because nucleophiles donate electrons, they are by definition Lewis bases . All molecules or ions with a free pair of electrons can act as nucleophiles...

 adenine base and preventing it from forming the splice lariat structure, or by interfering with the binding of splice regulatory proteins such as splice silencers and splice enhancers
Exonic splicing enhancer
An exonic splicing enhancer is a DNA sequence motif consisting of 6 bases within an exon that directs, or enhances, accurate splicing of hetero-nuclear RNA or pre-mRNA into messenger RNA .- The Basics :...

. Preventing the binding of snRNP U1 (at the donor site) or U2/U5 (at the polypyrimidine moiety and acceptor site) can cause modified splicing
Splicing (genetics)
In molecular biology, splicing is a modification of an RNA after transcription, in which introns are removed and exons are joined. This is needed for the typical eukaryotic messenger RNA before it can be used to produce a correct protein through translation...

, commonly excluding exon
Exon
An exon is a nucleic acid sequence that is represented in the mature form of an RNA molecule after either portions of a precursor RNA have been removed by cis-splicing or by two or more precursor RNA molecules have been ligated by trans-splicing. The mature RNA molecule can be a messenger RNA or...

s from the mature mRNA. Targeting some splice targets results in intron
Intron
An intron is a DNA region within a gene that is not translated into protein. These non-coding sections are transcribed to precursor mRNA and some other RNAs , and subsequently removed by a process called splicing during the processing to mature RNA. After intron splicing An intron is a DNA region...

 inclusions, while activation of cryptic splice sites can lead to partial inclusions or exclusions. Targets of U11/U12 snRNPs can also be blocked. Splice modification can be conveniently assayed by reverse-transcriptase polymerase chain reaction (RT-PCR) and is seen as a band shift after gel electrophoresis
Gel electrophoresis
Gel electrophoresis is a technique used for the separation of deoxyribonucleic acid , ribonucleic acid , or protein molecules using an electric field applied to a gel matrix...

 of RT-PCR products.

Blocking other mRNA sites


Morpholinos have been used to block miRNA
Mirna
Mirna may refer to:people* Mirna * Mirna Jukić, a bronze medal winner in swimming* Mirna Khayat, a Lebanese music video director* Mirna Macur, a Slovenian social researcherplaces* Mirna , a river in Istria, Croatia...

 activity and maturation. They can block ribozyme
Ribozyme
A ribozyme is an RNA molecule that catalyzes a chemical reaction...

 activity. U2 and U12 snRNP functions have been inhibited by Morpholinos. Morpholinos targeted to "slippery" mRNA sequences within protein coding regions can induce translational frameshifts
Frameshift mutation
A frameshift mutation is a genetic mutation caused by indels, ie. insertion or deletion of a number of nucleotides that is not evenly divisible by three from a DNA sequence...

. Activities of Morpholinos against this variety of targets suggest that Morpholinos can be used as a general-purpose tool for blocking interactions of proteins or nucleic acids with mRNA.

Specificity, stability and non-antisense effects


Morpholinos have become a standard knockdown tool in animal embryo
Embryo
An embryo is a multicellular diploid eukaryote in its earliest stage of development, from the time of first cell division until birth, hatching, or germination...

nic systems, which have a broader range of gene expression than adult cell
Cell (biology)
The cell is the basic structural and functional unit of all known living organisms. It is the smallest unit of an organism that is classified as living, and is often called the building block of life. The Alberts text discusses how the "cellular building blocks" move to shape developing embryos...

s and can be strongly affected by an off-target interaction. Following initial injections into frog or fish embryos at the single-cell or few-cell stages, Morpholino effects can often be measured five days later, after most of the processes of organogenesis
Organogenesis
In animal development, organogenesis is the process by which the ectoderm, endoderm, and mesoderm develop into the internal organs of the organism. Internal organs initiate development in humans within the 3rd to 8th weeks in utero...

 and differentiation
Cellular differentiation
In developmental biology, cellular differentiation is the process by which a less specialized cell becomes a more specialized cell type. Differentiation occurs numerous times during the development of a multicellular organism as the organism changes from a single zygote to a complex system of...

 are past, with observed phenotype
Phenotype
A phenotype is any observable characteristic or trait of an organism: such as its morphology, development, biochemical or physiological properties, or behavior. Phenotypes result from the expression of an organism's genes as well as the influence of environmental factors and possible interactions...

s consistent with target-gene knockdown. Control oligos with irrelevant sequences usually produce no change in embryonic phenotype, evidence of the Morpholino oligo's sequence-specificity and lack of non-antisense effects.

mRNA rescue experiments can often restore the wild-type phenotype to the embryos and provide evidence for the specificity of a Morpholino. In an mRNA rescue, a Morpholino is co-injected with an mRNA that codes for the same protein that the Morphlino is targeted to knock down. However, the rescue mRNA has a modified 5'-UTR
Five prime untranslated region
The five prime untranslated region , also known as the leader sequence, is a particular section of messenger RNA and the DNA that codes for it. It starts at the +1 position and ends just before the start codon of the coding region...

 (untranslated region) so that the rescue mRNA contains no target for the Morpholino but the rescue mRNA's coding region
Coding region
Coding region, depending on context, can refer to an organism or a geneThe coding region of a gene is that portion of a gene's DNA or RNA that is composed of exons....

 encodes the protein of interest. Translation of the rescue mRNA replaces production of the protein which was knocked down by the Morpholino. Since the rescue mRNA would not affect phenotypic changes due to modulation of off-target gene expression by the Morpholino, this return to wild-type phenotype is further evidence of Morpholino specificity.

Because of their completely unnatural backbones, Morpholinos are not recognized by cellular proteins. Nuclease
Nuclease
A nuclease is an enzyme capable of cleaving the phosphodiester bonds between the nucleotide subunits of nucleic acids. Older publications may use terms such as "polynucleotidase" or "nucleodepolymerase"....

s do not degrade Morpholinos, nor are they degraded in serum or in cells. Morpholinos do not activate toll-like receptor
Toll-like receptor
Toll-like receptors are a class of proteins that play a key role in the innate immune system. They are single membrane-spanning non-catalytic receptors that recognize structurally conserved molecules derived from microbes...

s and so they do not activate innate immune responses
Innate immune system
The innate immune system comprises the cells and mechanisms that defend the host from infection by other organisms, in a non-specific manner. This means that the cells of the innate system recognize and respond to pathogens in a generic way, but unlike the adaptive immune system, it does not confer...

 such as interferon
Interferon
Interferons are natural cell-signaling proteins produced by the cells of the immune system of most vertebrates in response to challenges such as viruses, parasites and tumor cells. They belong to the large class of glycoproteins known as cytokines and are produced by a wide variety of cells in...

 induction or the NF-κB
NF-kB
NF-κB is a protein complex that controls the transcription of DNA. NF-κB is found in almost all animal cell types and is involved in cellular responses to stimuli such as stress, cytokines, free radicals, ultraviolet irradiation, oxidized LDL, and bacterial or viral antigens...

 mediated inflammation
Inflammation
Inflammation is the complex biological response of vascular tissues to harmful stimuli, such as pathogens, damaged cells, or irritants. Inflammation is a protective attempt by the organism to remove the injurious stimuli as well as initiate the healing process for the tissue. Inflammation is not a...

 response. Morpholinos are not known to modify methylation of DNA
DNA methylation
DNA methylation is a type of chemical modification of DNA that can be inherited and subsequently removed without changing the original DNA sequence...

.

A cause for concern in the use of Morpholinos is the potential for "off target" effects. Up to 18% of Morpholinos appear to have non-target related phenotypes including cell death in the central nervous system and somite
Somite
A somite is a division of the body of an animal. In vertebrates this is mainly discernible in the embryo stage, in arthropods it is a characteristic of a hypothetical ancestor.-In vertebrates:...

 tissues of zebrafish embryos. Most of these effects have been shown to be due to activation of p53
P53
p53 , is a transcription factor which in humans is encoded by the TP53 gene. p53 is important in multicellular organisms, where it regulates the cell cycle and thus functions as a tumor suppressor that is involved in preventing cancer...

-mediated apoptosis
Apoptosis
Apoptosis is the process of programmed cell death that may occur in multicellular organisms. Programmed cell death involves a series of biochemical events leading to a characteristic cell morphology and death; in more specific terms, a series of biochemical events that lead to a variety of...

, and can be suppressed by co-injection of an anti-p53 Morpholino along with the experimental Morpholino. It appears that these effects are sequence specific, as in most cases if a Morpholino is associated with non-target effects, the 4-base mismatch Morpholino will not trigger these effects. The question of whether an observed morphant
Morphant
An organism which has been treated with a Morpholino antisense oligo to temporarily knock down expression of a targeted gene is called a Morphant.-Background:...

 phenotype is due to the intended knockdown or an off-target interaction can often be addressed by running another experiment to confirm that the observed morphant phenotype results from the knockdown of the expected target. This can be done by recapitulating the morphant phenotype with a second, non-overlapping Morpholino targeting the same mRNA or by confirmation of the observed phenotypes by use of a mutant strain or dominant negative methods. As mentioned above, rescue of observed phenotypes by coinjecting a rescue mRNA is, when feasible, a reliable test of specificity of a Morpholino.

Delivery


For a Morpholino to be effective, it must be delivered past the cell membrane
Cell membrane
The cell membrane is the biological membrane separating the interior of a cell from the outside environment....

 into the cytosol of a cell. Once in the cytosol, Morpholinos freely diffuse between the cytosol and nucleus, as demonstrated by the nuclear splice-modifying activity of Morpholinos observed after microinjection into the cytosol of cells. Different methods are used for delivery into embryos, into cultured cells or into adult animals. A microinjection
Microinjection
Microinjection refers to the process of using a glass micropipette to insert substances at a microscopic or borderline macroscopic level into a single living cell. It is a simple mechanical process in which a needle roughly 0.5 to 5 micrometers in diameter penetrates the cell membrane and/or the...

 apparatus is usually used for delivery into an embryo, with injections most commonly performed at the single-cell or few-cell stage; an alternative method for embryonic delivery is electroporation
Electroporation
Electroporation, or electropermeabilization, is a significant increase in the electrical conductivity and permeability of the cell plasma membrane caused by an externally applied electrical field...

, which can deliver oligos into tissues of later embryonic stages. Common techniques for delivery into cultured cells include the Endo-Porter peptide (which causes the Morpholino to be released from endosome
Endosome
In biology, an endosome is a membrane-bound compartment inside cells, roughly 500 nm in diameter when fully mature.-Function:Many endocytotic vesicles, derived from the plasma membrane, are either transported to a pre-existing endosome and fuse with it or are acidified via proton pump to become an...

s), the Special Delivery system (using a Morpholino-DNA heteroduplex
Heteroduplex
A heteroduplex is a double-stranded molecule of nucleic acid originated through the genetic recombination of single complementary strands derived from different sources, such as from different homologous chromosomes or even from different organisms....

 and an ethoxylated polyethylenimine delivery reagent), electroporation or scrape loading. Delivery into adult tissues is usually difficult, though there are a few systems allowing useful uptake of unmodified Morpholino oligos (including the inherently leaky muscle
Muscle
Muscle is the contractile tissue of the body and is derived from the mesodermal layer of embryonic germ cells. Muscle cells contain contractile filaments that move past each other and change the size of the cell. They are classified as skeletal, cardiac, or smooth muscles. Their function is to...

 cells caused by Duchenne muscular dystrophy
Duchenne muscular dystrophy
Duchenne muscular dystrophy is a severe recessive X-linked form of muscular dystrophy characterized by rapid progression of muscle degeneration, eventually leading to loss of ambulation and death. This affliction affects one in 3500 males, making it the most prevalent of muscular dystrophies. In...

 or the vascular endothelial
Endothelium
The endothelium is the thin layer of cells that line the interior surface of blood vessels, forming an interface between circulating blood in the lumen and the rest of the vessel wall. Endothelial cells line the entire circulatory system, from the heart to the smallest capillary...

 cells stressed during balloon angioplasty
Angioplasty
Angioplasty is the technique of mechanically widening a narrowed or obstructed blood vessel; typically as a result of atherosclerosis. Tightly folded balloons are passed into the narrowed locations and then inflated to a fixed size using water pressures some 75 to 500 times normal blood pressure...

). Though they permeate through intercellular spaces in tissues effectively, unconjugated PMOs have limited distribution into the cytosol & nuclear spaces within healthy tissues following iv administration. Systemic delivery into many cells in adult organisms can be accomplished by using covalent conjugates of Morpholino oligos with cell penetrating peptide
Cell penetrating peptide
Cell penetrating peptides are short peptides that facilitate cellular uptake of various molecular cargo . The "cargo" is associated with the peptides either through chemical linkage via covalent bonds or through non-covalent interactions...

s, and while toxicity has been associated with moderate doses of the peptide conjugates they have been used in vivo for effective oligo delivery at doses below those causing observed toxicity. An octa-guanidinium dendrimer attached to the end of a Morpholino can deliver the modified oligo (called a Vivo-Morpholino) from the blood to the cytosol. Delivery-enabled Morpholinos, such as peptide conjugates and Vivo-Morpholinos, show promise as therapeutics for viral and genetic diseases.

Intellectual property


Gene Tools, LLC
Gene Tools
Gene Tools, LLC is a limited liability company located in Philomath, Oregon, United States that manufactures Morpholino antisense oligos and delivery reagents. Gene Tools was founded in 1997 and began regularly shipping custom-sequence Morpholino oligos in 2000. The manager and general partner, Dr...

 and AVI BioPharma Inc.
AVI Bio Pharma
AVI BioPharma Inc. is a medical research and drug development company with corporate offices in Portland, Oregon, United States, and laboratories in Corvallis, Oregon. It was incorporated in 1980...

 claim intellectual property
Intellectual property
Intellectual property is a number of distinct types of legal monopolies over creations of the mind, both artistic and commercial, and the corresponding fields of law...

on aspects of Morpholino oligo.

Further reading