Game-changing gene-silencing therapies for HD

Posted on at October 13, 2017
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NAME: Amber Southwell, PhD

TITLE: Assistant Professor of Neuroscience, Burnett School of Biomedical Sciences, University of Central Florida

EDUCATION:  PhD, California Institute of Technology; post-doctoral research fellowship, University of British Columbia

HOBBIES: Scuba diving, sailing, partnered dancing, and cooking

The landscape of therapeutic development for genetic disease is rapidly evolving, and scientists are developing promising therapies to treat HD through gene-silencing therapies. HD Insights spoke with Dr. Amber Southwell about the status of gene-silencing therapies for HD, as well as her own work on a selective antisense oligonucleotide (ASO) therapy.

What are gene-silencing therapies for HD?

Gene-silencing therapies reduce or prevent the expression of mHTT. They usually interfere with transcription or translation of mutant RNA, or cause the degradation of mHTT RNA.

What are the primary gene-silencing therapies under investigation?

The majority of gene-silencing therapies under current investigation are antisense oligonucleotides (ASOs), RNAi (RNA interference)-based reagents, and CRISPR/Cas9 gene-editing systems. ASOs are short, synthetic DNA fragments that bind RNA through base pairing, and modulate its function.

The majority of ASO drugs in development work through the degradative mechanism in which Ribonuclease H (RNase H) is recruited to recognize and cleave huntingtin transcripts. This process frees the ASO, enabling it to catalyze the degradation of multiple RNA molecules, effectively suppressing the gene product.

With their diverse functionality, high target specificity, and suitability for direct CNS delivery through lumbar puncture ASOs are an excellent treatment option for HD. Currently, Ionis Pharmaceuticals has a nonselective ASO in a clinical trial. A nonselective ASO silences both wild-type and mHTT genes. RNAi-based reagents—especially microRNA-based reagents—are also being developed.

These reagents use small RNAs to bind to HTT mRNA molecules in order to silence their activity. RNAi-based reagents are not delivered naked—in other words, without a carrier—as are ASOs. Instead, they are typically delivered by a viral carrier.

Two RNAi reagents that have shown a lot of promise are very close to translation to the clinic, one with Sanofi Genzyme and one with uniQure B.V. (see HD Insights, Vol. 16). One of the groups working on RNAi is doing its preclinical studies in the sheep model of HD, because sheep have a very long spinal cord, and a larger brain than nonhuman primates. That group hopes to maximize the therapeutics distribution in a larger brain and spinal cord. In addition, a number of groups are developing gene-editing approaches to produce gene silencing, using the CRISPR/Cas 9 system.

These approaches aim to completely inactivate the mutant copy of the gene. Currently, gene-editing strategies have low efficiency. Basically, you gene-edit some cells in culture, and then select for the cells in which the genes were actually edited.

Next, you test the edited genes to make sure they did not receive an unwanted edit. Finally, you find that the cells have been changed in the way you want, and you expand those up to create your population. These studies are in very early preclinical stages, and there is a long way to go before efficiency and specificity will be high enough for use in the human brain.

What does your most recent research focus on?

We have been investigating a selective ASO that suppresses only mHTT and leaves wild type HTT expression intact. We ran a preclinical trial that will be published very soon and had excellent results. Basically, our ASO prevents the onset of HD in presymptomatic mice, and in symptomatic mice we saw recovery of motor and psychiatric phenotypes.

Most importantly, we saw a complete rescue of cognitive phenotypes. We have shown that our ASO can not only prevent cognitive decline, but can also restore normal cognition when used post-symptom onset, meaning, after the mice have developed a cognitive deficit. We are very excited about this.

Is your selective ASO better than Ionis’s nonselective ASO?

Our selective ASO was co-developed with Ionis. I think the reason Ionis started with a nonselective ASO for its clinical trial was that it was the fastest way to get a therapy to all HD patients, with the idea that going back and developing selective therapies later would yield drugs that were safer for patients in the long term.

I think that nonselective silencing is going to be preferable to not treating HD, but I also think that selective silencing is going to be better for the patient than nonselective silencing. In an effort to preserve wild-type HTT function, the nonselective ASO is being dosed to induce about 50 percent suppression in the cortex, and to have minimal activity in the basal ganglia.

With a selective ASO, it may be possible to use a higher dose, to induce almost total mHTT suppression in the cortex, and have more activity in the basal ganglia.

Is there competition among scientists to be the first to discover the best therapy?

I think most people would agree with me that we are all on the same team. HD is the adversary. It is an incredibly complicated disease, and one that we need to come at from every angle we can. There is still so much work to do—after all, the gene was identified in 1993, and today, more than 20 years later, we are only just starting the very first huntingtin-lowering clinical trials.

There is enough room for everyone’s work, and there is a lot more collaboration than competition in the field.

Are the patients and families hopeful?

Yes, they are really excited. They often contact me and ask, “When is this going to be available for me?” Sometimes I feel that a single email asks me to be a scientist, a clinician, and a genetic counselor. I have to tell people that it is a really long way between mice and men.

A therapy must go through so many steps, so many points of potential failure, and once it gets to human trials, it can take years to prove its safety and efficacy. We are also hindered by our tools; for example, we do not have enough biomarkers to evaluate these therapies. The excitement is pushing the HD community to think that there is going to be something available for them in 5 to 10 years, but we have no idea if that is the case. Yes, we can at last successfully treat a mouse.

Yes, we have really great preventative and restorative preclinical data. Yes, we finally have a huntingtin-lowering clinical trial that is targeting the root cause of HD—but unfortunately, none of this means there is an effective treatment just over the horizon. We simply do not know yet.

Selected gene-silencing therapies in the pipeline

Developer Type Description Status Source
Ionis Pharmaceuticals and Don Cleveland

Research group

ASO Study found ASO infused into cerebrospinal fluid of symptomatic HD mice delays progression of HD and reverses disease phenotypes. Phase I clinical trial

underway

Kordasiewicz HB, et al.

2012. 1

Genzyme miRNA Research suggests two recombinant adeno-associated viral vectors (AAV), AAV1 and AAV2, successfully target neurons that degenerate in HD. Clinical trial planned

(IND estimated 2018)

Hadaczek P, et al. 2016.2
uniQure miRNA Research demonstrates strong in vitro and in vivo allele-selective silencing of mHTT by miSNP50 and total HTT silencing by miH12. Preclinical research

(IND estimated 2017)

Miniarikova J, et al.

2016. 3

Sangamo Biosciences Zinc finger Research revealed that allele-specific zinc fingers lowered production of mutant protein by more than 90 percent, while reducing normal protein by 10 percent or less. Preclinical research

(IND estimated 2017)

Preclinical research

Zhang HS, et al. 2014.4
Neil Aronin Research

Group

siRNA siRNA infusion is shown to lower mHTT levels in the striatum of

mice without producing a robust immune response.

Preclinical research Johnson E, et al. 2015.5
Ionis Pharmaceuticals

Michael Hayden

Research Group

ASO At a wide range of doses, four ASOs potently and selectively

silence mHTT throughout the central nervous system for 36 weeks or more after a single intracerebroventricular injection.

Preclinical research Southwell AL, et al.

2014.6

WAVE Life Sciences ASO WAVE’s lead compounds are stereopure, allele-specific ASOs that target two difference single nucleotide polymorphisms (SNPs) associated with mutated Huntingtin to enable maximal target engagement with minimal off-target effects. Preclinical research

(INDs expected

2017)

WAVE Life Sciences

2017 Pipeline Update

[press release], 2017.7

David Corey Research

Group

ASO Several ASOs targeted to the CAG repeat of HTT and containing a variety of modifications, such as bridged nucleic acids and phosphorothioate internucleotide linkages, demonstrated alleleselective silencing in patient-derived fibroblasts. Preclinical research Gagnon KT, et al. 2010.8
Beverly Davidson

Research Group

CRISPR/

Cas9

CRISPR/Cas9-based strategy for allele-specific genome editing

reduces expression of mutant HTT alleles in human HD fibroblasts and mouse brain.

Preclinical research Monteys AM, et al.

2017.9

Jong-Min Lee Research

Group

CRISPR/

Cas9

Protospacer Adjacent Motif (PAM)-altering SNPs target patientspecific CRISPR/Cas9 sites, with a goal of allele-specifically inactivating the mutant HTT for a given diplotype. Preclinical research Shin JW, et al. 2016.10
Gary Dunbar

Research group

CRISPR/

Cas9

A CRISPR/Cas9 plasmid reduces the production of mHTT in mesenchymal stem cells from YAC128 mice. Preclinical research

Preclinical research

Kolli N, et al. 2017.11
Mahmoud Pouladi

Research Group

CRISPR/

Cas9

Use of a CRISPR-Cas9 and piggyBac transposon-based approach to correct HD hiPSCs and associated phenotypic abnormalities. Preclinical research Xu, et al. 2017.12

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References

1Kordasiewicz HB, Stanek LM, Wancewicz EV, et al. Sustained Therapeutic Reversal of Huntington’s Disease by Transient Repression of Huntingtin Synthesis. Neuron. 2012;74(6):1031-1044.

2Hadaczek P, Stanek L, Ciesielska A, et al. Widespread AAV1- and AAV2-mediated transgene expression in the nonhuman primate brain: implications for Huntington’s disease. Mol There Methods Clin Dev..2016;3:16037.

3Miniarikova J, Zanella I, Huseinovic A, et al. Design, Characterization, and Lead Selection of Therapeutic miRNAs Targeting Huntingtin for Development of Gene Therapy for Huntington’s Disease. Mol Ther Nucleic Acids. 2016;5:e297.

4Zhang HS, Zeitler B, Froelich S, et al. 769.12. Engineered zinc finger transcriptional repressors selectively inhibit mutant huntingtin expression and reverse disease phenotypes in Huntington’s disease patient-derived neurons and in rodent models. [abstract]. Neuroscience 2014; November, 2014; Washington, DC.

5Yu MS, Johnson E, Chase K, McGowan S, et al. Safety of Striatal Infusion of siRNA in a Transgenic Huntington’s Disease Mouse Model. J Huntington’s Dis. 2015;4(3):219-229.

6Southwell AL, Skotte NH, Kordasiewicz HB, et al. In Vivo Evaluation of Candidate Allele-specific Mutant Huntingtin Gene Silencing Antisense Oligonucleotides. Mol Ther. 2014;22(12):2093-2106.

7WAVE Life Sciences 2017 Pipeline Update [press release]. January 06, 2017; http://www.businesswire.com/news/home/20170106005730/en/ Accessed April 29, 2017.

8Gagnon KT, Pendergraff HM, Deleavey GF, et al. Allele-Selective Inhibition of Mutant Huntingtin Expression with Antisense Oligonucleotides Targeting the Expanded CAG Repeat. Biochemistry. 2010;49(47):10166-10178.

9Monteys AM, Ebanks SA, Keiser MS, Davidson BL. CRISPR/Cas9 Editing of the Mutant Huntingtin Allele In Vitro and In Vivo. Mol Ther. 2017;25(1):12-23.

10Shin JW, Kim K-H, Chao MJ, et al. Permanent inactivation of Huntington’s disease mutation by personalized allele-specific CRISPR/Cas9. Hum Mol Genet. 2016;25(20):4566-4576.

11Kolli N, Lu M, Maiti P, Rossignol J, Dunbar GL. CRISPR-Cas9 Mediated Gene-Silencing of the Mutant Huntingtin Gene in an In Vitro Model of Huntington’s Disease. Int J Mol Sci. 2017;18(4).

12Xu X, Tay Y, Sim B, et al. Reversal of Phenotypic Abnormalities by CRISPR/Cas9-Mediated Gene Correction in Huntington Disease Patient-Derived Induced Pluripotent Stem Cells. Stem Cell Reports. 2017;8(3):619-633.

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