Transcript Slide 1
Gene therapy and immunology
Gene Therapy – an approach designed to treat disease by replacing,
altering or supplementing genes that are defective or missing.
Two immunological factors play important roles in gene therapy:
Immunodeficiency diseases are prime candidates for
therapeutic approaches where genes are introduced into a patient to correct a
gene mutation.
Immune responses against vectors used in gene therapy
can be important for the success or failure of a particular approach.
Correcting an immunodeficiency disease: X-linked SCID
A clinical study in France (1999) sought to cure young patients with Xlinked SCID.
Approach: isolate stem cells from bone marrow, grow in culture,
replace defective gc gene, and reintroduce into patient.
Isolate CD34+ cells
Patient
cells with receptors restored
add gc gene
Ex vivo therapy - cells with defective genes are removed from a
patient for transfection (introduction of genes). The treated cells are then
returned to the patient.
In vivo therapy – direct administration of a gene or packaged gene to
the patient.
Vector - a delivery device for insertion of a gene into cells.
Viral vectors are currently the most common means for
efficient gene transfer.
Retrovirus vector Retroviruses have a small RNA genome that has
three genes coding for structural proteins (Gag, Pol and Env) required for viral
replication surrounded by two long terminal repeats
LTR j
Gag
Pol
Env
LTR
LTRs contain promoter and enhancer functions for viral transcription and
are involved in integration of the virus into the host cell genome.
A short packaging sequence psi (j) is needed for the RNA transcript to
be packaged into a mature virion.
Viruses engineered for therapy lack genes needed for replication, these
are replaced by the therapeutic gene, but retain LTR’s (needed for expression)
and the packaging sequence. The essential functions of gag, pol and env are
provided by stable packaging cell lines that express these proteins and allow the
defective virus to be packaged into a mature virion.
j
cDNA of interest
j neo resistance
cDNA
promoter
Gene of interest can be driven by a viral promoter or by a different
inserted promoter. A selected promoter might be advantageous if someone
wanted tissue-specific expression of a particular gene. Can also include antibiotic
selection marker to select infected cells for ex vivo experiments.
Retroviral vectors have a couple of limitations:
1). they only infect dividing cells
2). they integrate more or less randomly into the host genome. The
right handed LTR can promote and enhance expression of genes adjacent to
it. If one of these is a proto-oncogene, could potentially activate it
inappropriately. Risk of causing cancer?
cellular DNA
proviral DNA
(or transduced gene)
cellular DNA
In the French study, retroviral gene transduction led to successful
restoration of functioning immune systems to 9 of 11 boys with X-SCID.
Boys developed normal numbers of CD4 and CD8 T cells and
responded normally to childhood immunizations.
However, in September of 2002, one of the 11 children developed
leukemia three years after initiation of the project. The leukemia arose from
expansion of a single gd T cell and was due to insertion of the viral vector near a
gene known as LMO2, which is a transcription factor linked previously to
leukemia. It was unclear as to whether or not this was a highly unusual event or
might be more common. Some trials were temporarily suspended.
Then, in December of 2003, a second one of the 11 children developed
leukemia due to expansion of an ab T cell, also due to viral vector insertion near
LMO2.
Unfortunately this year a third child from the original French study also
developed leukemia, but the mechanism appears to be different and not involve
LMO2. This has caused temporary suspensions of related trials on a world-wide
basis.
Adenosine deaminase deficiency
ADA-SCID is a recessive disease that leads to an accumulation of toxic
purine metabolites that affects multiple cell types, but particularly lymphocytes.
This was the very first genetic disease to be treated with a gene therapy
approach in 1990.
Patients with ADA-SCID are best treated with a bone marrow transplant
(not always possible to find good match).
An alternative treatment is to give the patients ADA-PEG, adenosine
deaminase coupled to polyethylene glycol to help stabilize the enzyme. This is
not curative, but does ease symptoms.
The original gene therapy approach was similar to that discussed
above for X-linked SCID except that T cells were isolated and these were
infected with the retrovirus containing the cDNA for adenosine deaminase.
patient
add ADA gene
Isolate T cells
grow in culture in IL-2
patient
cells with enzyme restored
For ethical reasons, the patients were also given ADA-PEG as a backup therapy. Later trials used CD34+ stem cells rather than T cells
The trials suffered from two problems:
1). The percentage of ADA
expressing cells that showed up in the
periphery was very small.
2). it was difficult to evaluate the
effectiveness of the therapy due to the
complicating factor of providing the ADAPEG. Overall improvement in immune
responses was observed. However,
discontinuation of the ADA-PEG did cause
conditions to worsen.
Two adjustments to increase efficacy of approach:
1. Patients no longer given ADA-PEG. The reasoning is that infected
cells re-administered to the patient will have a growth advantage over ADAdeficient cells and will more readily populate the bone marrow. The provision of
ADA-PEG eliminates much of this advantage
2. Patients treated with a low intensity, nonmyeloablative therapy to
partially destroy their immune system to make room in the bone marrow for the
infected cells to expand.
Isolate CD34+ cells
add ADA gene
Patient with partial
depletion of bone marrow cells
cells with enzyme restored
ADA+ cells have a growth
advantage
Adenovirus vectors. Adenoviruses cause infections in humans that are
relatively mild, often causing upper respiratory symptoms. However, as a
consequence, they have the potential to trigger inflammatory responses.
Adenovirus vectors are widely used in gene therapy because they
exhibit the highest transfection efficiencies both ex vivo and in vivo. They can
infect both dividing and nondividing cells of a wide variety of cell types.
In in vitro cell culture, adenoviruses can replicate to very high titers so
that sufficient quantities of vector can be prepared for clinical trials.
The genome of adenoviruses:
Linear, double-stranded DNA. Viral DNA is encapsulated within a
protein coat (non-enveloped virus). Adenovirus DNA does not integrate into
host chromosomal DNA and remains an episome (separate DNA in nucleus) in
cells. Thus, cannot cause insertional mutagenesis.
The virus has two general sets of genes, early and late, which are
expressed either before viral replication (early) or after (late) in a host cell. The
first-generation viruses had one or more early genes (typically E1 or E3) replaced
by the gene of interest. The E1 or E3 gene products could be supplied by
packaging cells to make virus for therapy.
E1a, E1b
ITR promoter
(inverted terminal repeat)
E3
cDNA
Adenovirus vectors can trigger cytotoxic T cell responses directed at
transfected cells expressing adenovirus proteins followed by a humoral
response generating anti-adenoviral antibodies. These two characteristics of
adenovirus vectors permit only transient expression of therapeutic genes and
limit the ability to repeatedly administer virus.
This potential problem really came to light with a recent
incident at the University of Pennsylvania. An 18 year old
patient by the name of Jesse Gelsinger had volunteered
to participate in a clinical gene therapy trial. Jesse
suffered from an ornithine transcarbamylase deficiency (a
urea cycle enzyme) that can lead to elevated blood
ammonia concentrations. Was kept in check relatively
well with a very low protein diet and drug treatment.
Jesse was treated with an adenovirus vector carrying the ornithine
transcarbamylase gene that was injected directly into an artery leading to his
liver (these are the cells that should have OTC). He should have suffered only
mild, flu-like symptoms, but somehow in this patient the adenovirus triggered an
overwhelming systemic inflammatory response causing acute respiratory
distress and death due to lung failure and anoxia. He survived only four days
following the procedure.
Follow-up studies showed that much of the virus failed to infect liver
cells, but either infected liver macrophages or passed through the liver to lymph
nodes, spleen and bone marrow.
More recent versions of adenovirus have been developed that are
termed “gutless” vectors because they are missing most all viral genes, but still
contain inverted terminal repeats and a packaging sequence around the
transgene. All other required genes needed for production of the virus for use in
therapy can be supplied by co-infecting helper viruses. These vectors present
fewer proteins to the immune system and can prolong gene expression. Immune
responses will likely still be problematic with time.
Adeno-associated viruses (AAV) as vectors.
Small parvovirus often found in cells infected
with adenovirus. Has only a single 4.7 kb single-stranded
DNA genome surrounded by a protein coat.
The DNA does integrate into the host genome,
but does so at only a single site on chromosome 19.
Virus can infect many cell types, both dividing and nondividing.
The AAV proteins expressed are nontoxic to cells and do not trigger a
host immune response, so they do not cause inflammation like adenoviruses.
Can remove most of genetic information with exception of two 145 bp
terminal repeats and replace with gene or genes of interest. (however, it can’t be
any larger than the wild-type virus, so this limits the amount of DNA you can
incorporate)
AAV can’t reproduce by itself, but needs help from other viruses like
adenovirus or herpes virus (that’s why it is only seen in cells also infected by other
viruses). This made it tough to figure out how to propagate the virus in culture.
Investigators have identified the required helper genes and put these into
packaging cells to allow production of helper-free AAV.
TR
Rep
Cap
TR
Wild-type virus has two genes: rep and cap. Rep contains information for
replication, expression and integration. Cap has genes for capsid structural
proteins. Surrounded by terminal repeats containing promoter. Replace with
transgene and any regulatory sequences needed.
TR promoter
cDNA
Can get stable expression in infected cells (but virus does not replicate and
spread, would be temporary). Unfortunately, without Rep, the virus tends to
integrate somewhat randomly, but seems to prefer transcribed genes. Could
cause insertional mutagenesis.
Other viral vectors being examined:
Herpes Simplex virus vectors are of interest because HSV has the
capacity to infect neurons. Potentially useful for treatment of brain disorders
like Parkinson’s disease and brain tumors like gliomas.
Lentiviruses are retroviruses, but are much more complex in their
genomes, containing 6 additional genes. HIV is a lentivirus. The packaging
cell line is much more complex due to additional gene requirements. However,
lentiviruses have the advantage that they can infect nondividing cells as well
as dividing cells.
Nonviral vectors for gene therapy-viral vectors all elicit an immune
response to some degree, have potential toxicity issues (e.g., insertional
mutagenesis, inflammatory reactions), and are sometimes difficult to produce in
large amounts. Nonviral delivery systems could potentially circumvent many of
these problems.
Naked DNA –Plasmid is injected or delivered via gene gun. Often
suffers from a low transfection efficiency, especially compared to viruses -of
considerable interest in the vaccine field. New studies suggest that simple iv
injections can deliver to muscle and liver better than anticipated.
Cationic Lipids and Liposomes - When plasmid DNA is mixed with
small liposomes containing cationic lipids, lipid-plasmid DNA complexes form
due to electrostatic interactions between negatively charged phosphate groups
of DNA and positively charged lipid residues. These DNA-cationic lipids can
enter cells through endocytosis. A drawback is low transfection efficiency in
vivo. Most DNA transfected into cells with cationic lipids remains in endosomes.
Can include targeting molecules in the liposomes to deliver them to
specific cell types. Can add polyethylene glycol derivatives to phospholipids at
the liposome surface to produce “stealth liposomes”, which circulate in the
bloodstream for extended periods. Some investigators have tethered antibodies
to the transferrin receptor to the polyethylene glycol covering to allow the
liposomes to cross the blood-brain barrier.
RNA interference
There is a process known as posttranscriptional gene silencing that
was first identified by investigators trying to create a dark purple petunia. Adding
genes for one color tended to turn off other color genes in an odd fashion – it did
so after the genes were transcribed. The intermediate in the process turned out
to be a double-stranded RNA molecule. The process has been found to be
highly conserved in eukaryotes and probably persists in part due to its role in
viral defense.
It was subsequently shown in C. elegans (nematodes) that injection of
a dsRNA corresponding to the mRNA coding for a particular protein could
actually eliminate production of that protein. The dsRNA was processed to form
small 21-23 oligonucleotide fragments by an enzyme known as Dicer. These
fragments bind to a complex known as the RNA-induced silencing complex or
RISC. This complex targets the homologous mRNA and cleaves it.
It was found that this also works in human cells, with the
complication that, if you give a human cell a dsRNA, you will induce the
interferon response and shut off lots of protein synthesis.
However, it was found that if you give the cell only small dsRNA
oligonucleotides, the interferon response does not occur. Thus, it is possible
now to eliminate the transcription of specific proteins form cells. A powerful
tool for experimentalists. The process is called RNA interference or RNAi
and the small oligos are called small, interfering RNAs or siRNA.
It is also possible to express a small hairpin RNA that is processed
by dicer to form the siRNAs. These are referred to as shRNAs or short,
hairpin RNAs. Allows one to use plasmids as vectors or viruses as vectors
for the delivery of these into cells. Consequently, there is considerable
interest in using these as therapeutic agents for the treatment of diseases
where the elimination of a particular protein is sought (e.g., cancer, HIV,
Huntington’s disease).
Interferon response
Gene therapy trials. There are currently on the order of 1000+ clinical
gene trials underway, mostly in the U.S.
1. 66% of these target cancer, about 9.5% target monogenic
diseases (disease caused by single gene mutation), 8% target vascular disease
and 6.6% infectious diseases.
2. The most common gene delivery method being tested is
retrovirus (27%) followed by adenovirus (26%) and naked DNA (15%).
3. The most common transgene being delivered is a cytokine
gene (e.g., lymphocytes transfected to enhance tumor killing power and
replaced) followed by antigens (enhance tumor immunity) and then genes for
tumor suppressors.
4. The most common delivery route is intratumoral followed
by iv. Most are in Phase I trials which test mostly for safety.