Insights Of The Year

Posted on at November 1, 2017
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Insights of the Year 2016-2017

Each year, we recognize the most influential papers in HD research in three categories: basic science, clinical research, and biomarkers and imaging. The winners of the 2015-2016 competition nominated 15 articles for consideration in the 2016-2017 competition. Ten authors provided summaries, included in this edition, and the remaining five are cited. The HD Insights Editorial Board and prior winners then voted to select the three most influential papers, one from each category. The authors of the winning papers will present their research in a panel discussion at the HSG Annual Meeting in Colorado, on November 2, 2017. Congratulations to all the nominees and winners!


Mutant huntingtin accelerates impaired cellular phenotypes

Most influential paper (Basic science)

By Fatima Gasset-Rosa, PhD

The onset of neurodegenerative disorders such as HD is strongly influenced by aging. Hallmarks of aged cells include compromised nuclear envelope integrity; impaired nucleocytoplasmic transport; and accumulation of DNA double-strand breaks.

We show that mHTT markedly accelerates all these cellular phenotypes in a dose- and age-dependent manner in the cortex and striatum of mice. Huntingtin-linked polyglutamine initially accumulates in nuclei, leading to disruption of nuclear envelope architecture; partial sequestration of factors essential for nucleocytoplasmic transport (Gle1 and RanGAP1); and intranuclear accumulation of mRNA. In aged mice, accumulation of RanGAP1, together with polyglutamine, is shifted to perinuclear and cytoplasmic areas.

Consistent with findings in mice, marked alterations in nuclear envelope morphology, abnormal localization of RanGAP1, and nuclear accumulation of mRNA were found in the cortex of HD patients. Overall, our findings identify polyglutamine-dependent inhibition of nucleocytoplasmic transport and alteration of nuclear integrity as a central component of HD.


Gasset-Rosa F, Chillon-Marinas C, Goginashvili A, et al. Polyglutamine-expanded huntingtin exacerbates age-related disruption of nuclear integrity and nucleocytoplasmic transport. Neuron. 2017 Apr 5;94(1):48-57.e4. doi: 10.1016/j.neuron.2017.03.027.

Genetic variants associated with Huntington’s disease progression identified

Most influential paper (Clinical research)

By Davina Hensman Moss, PhD

In this study, we identified a genetic modifier of HD progression, thereby opening up avenues for potential therapeutic development. By using the extensive phenotypic information available from the TRACK-HD studies, we defined a novel multi-dimensional progression score in HD (n = 216). A parallel progression score using 1,773 previously genotyped subjects from the EHDN REGISTRY study was then developed.

Despite use of less phenotypic information to generate the REGISTRY progression score, the TRACK and REGISTRY progression scores were significantly correlated (r = 0·674). These two progression scores were used in genome-wide association studies to look for genetic variants associated with disease progression. Meta-analysis of progression in TRACK-HD and REGISTRY gave a genome-wide significant signal (p = 1.12 x 10 -10) on chromosome 5, spanning 3 genes: MSH3, DHFR, and MTRNR2L2. The lead SNP in TRACK-HD (rs557874766) is genome-wide significant in the meta-analysis (p = 1.58×10 -8), and encodes an amino acid change (Pro67Ala) in MSH3.

Such a strong association in a small sample implies that the progression measure is a sensitive reflection of disease burden, that the effect size is large, or likely both. As knockout of Msh3 reduces somatic expansion in HD mouse models, this highlights somatic expansion as a potential pathogenic modulator.

Genome-wide association analysis of progression score. Manhattan plot of meta-analysis of TRACK and REGISTRY progression analysis yielding a locus on chromosome 5. Significance of SNPs (y axis) is plotted against genomic location (x axis). Green line in: 5×10 -8.

Courtesy: Davina Hensman


Hensman Moss D, Pardiñas A, Langbehn D, et al. Identification of genetic variants associated with Huntington’s disease progression: a genome-wide association study. Lancet: Neurology Online First. doi: http://dx.doi.org/10.1016/S1474-4422(17)30161-8.

Neurofilament light protein as a potential biomarker of neurodegeneration

Most influential paper (Biomarkers and imaging)

By Lauren Byrne, MSc

No blood biomarker candidate studied to date has shown robust association with HD progression, onset and clinical severity. In the TRACK-HD cohort, we investigated neurofilament light protein (NfL) in blood as a potential prognostic marker of neurodegeneration in HD patients.

We found that mean concentrations of NfL in plasma at baseline were significantly higher in HTT mutation carriers than in controls, and the difference increased with disease stage (Fig. A). There was a striking CAG-dependent genetic dose-response relationship of plasma NfL level at a given age (Fig. B). Premanifest individuals with higher levels of NfL at baseline were more likely to progress to manifest HD during the period of study. Baseline levels of plasma NfL were strongly associated with subsequent cognitive decline and brain atrophy, independent of age and CAG, suggesting that plasma NfL may have predictive value above that of other predictors of HD progression. In a separate cohort, we showed that CSF and plasma levels of NfL were highly correlated, indicating that plasma levels have a CNS-derived origin. We conclude that plasma NfL is a promising potential biomarker of neurodegeneration in HD.

(A) NfL concentrations in plasma increase with disease stage. (B) The CAG-dependent genetic dose-response relationship of plasma NfL level at a given age. The lines show quadratic fit for all participants with a given CAG repeat count or all controls. Each increase in CAG repeat count was associated with higher and more steeply rising NfL concentrations in plasma. (Data were log transformed for comparisons.)

Courtesy: Lauren Byrne


Byrne L, Rodrigues F, Blennow K. Neurofilament light protein in blood as a potential biomarker of neurodegeneration in Huntington’s disease: A retrospective cohort analysis. Lancet Neurol. 2017 Aug;16(8):601-609. doi: 10.1016/S1474-4422(17)30124-2. Epub 2017 Jun 7.

Huntington’s disease accelerates epigenetic aging of brain and blood tissue

Nominee (Basic science)

By Steve Horvath, PhD, ScD

The patient’s age at HD motoric onset is strongly related to the number of CAG trinucleotide repeats in the huntingtin gene, suggesting that biological tissue age plays an important role in disease etiology. Recently, a DNA methylation – based biomarker of tissue age has been advanced as an epigenetic clock, which is arguably the most accurate molecular biomarker of aging.

Using large-scale human brain and blood data sets, we have found that HD is associated with an accelerated epigenetic age of blood and brain tissue. Further, HD has a genome-wide significant effect on the DNA methylation levels of many CpGs, but the effect appears to be tissue-specific. Overall, our results demonstrate that HD is associated with accelerated epigenetic age and has profound effects on DNA methylation levels. Future research in mouse models and in longitudinal human cohort studies will help elucidate cause and effect relationships.


Horvath S, Langfelder P, Kwak S, et al. Huntington’s disease accelerates epigenetic aging of human brain and disrupts DNA methylation levels. Aging. 2016 Jul;8(7): 1485-1504. doi: 10.18632/aging.101005. 

CRISPR/Cas9 permanently inactivates Huntington’s disease mutation

Nominee (Basic science)

By Jong-Min Lee, PhD

All cases of HD are due to expansion of the CAG trinucleotide repeat in the first exon of HTT. However, expanded and normal CAG repeats sit on very diverse HTT haplotype backbones that carry numerous genetic variations. Some variants create or eliminate the CRISPR/Cas9 protospacer adjacent motif (PAM) site, which is required for Cas9 endonuclease. Such PAM-altering SNPs (PASs) provide opportunities for distinguishing the mutant allele from the normal allele in allele-specific CRISPR/Cas9 targeting. 

To identify mutant allele-specific CRISPR/Cas9 targets in a given HD subject, PAM sites generated by SNPs were mapped to HTT haplotypes, and two haplotypes were compared. Then, CRISPR/Cas9 strategies can be designed based on mutant allele-specific CRISPR/Cas9 PAM sites for a given HD subject. For example, a CRISPR/Cas9 strategy simultaneously using gRNA1 and gRNA2, chosen based on PAM sites on the mutant allele, is predicted to excise the promotor region, transcription start site, and CAG repeat from the mutant allele, leading to prevention of the production of mHTT. Our allele-specific strategy does not target the CAG expansion mutation, but rather the haplotype harboring the mutation. Therefore, other CAG repeat-containing genes will not be influenced, making our strategy safe for therapeutic applications.

A CRISPR/Cas9 strategy simultaneously using gRNA1 and gRNA2, chosen based on PAM sites on the mutant allele, is predicted to excise the promotor region, transcription start site, and CAG repeat from the mutant allele, leading to prevention of the production of mutant HTT.

Courtesy: Jong-Min Lee


Shin J, Kim K, Chao M. Permanent inactivation of Huntington’s disease mutation by personalized allele-specific CRISPR/Cas9. Hum Mol Genet. 2016 Oct 15;25(20):4566-4576. doi: 10.1093/hmg/ddw286.

Nuclear pore complex is disrupted by mHTT

Nominee (Basic science)

By Jonathan Grima, PhD

HD is caused by an expanded CAG repeat in the huntingtin gene (HTT). The mechanisms by which mHTT causes disease are unclear. Nucleocytoplasmic transport – the trafficking of macromolecules between the nucleus and cytoplasm – is tightly regulated by nuclear pore complexes (NPCs) made up of nucleoporins (NUPs). Previous studies offered clues that mHTT may disrupt nucleocytoplasmic transport, and a mutation of an NUP can cause HD-like pathology. Therefore, we evaluated the NPC and nucleocytoplasmic transport in multiple models of HD, including mouse and fly models, neurons transfected with mHTT, HD iPSC-derived neurons, and human HD brain regions.

These studies revealed severe mislocalization and aggregation of NUPs and defective nucleocytoplasmic transport. HD repeat – associated non-ATG (RAN) translation proteins also disrupted nucleocytoplasmic transport. Additionally, overexpression of NUPs and treatment with drugs that prevent aberrant NUP biology also mitigated this transport defect and neurotoxicity, providing future novel therapy targets.

Nuclear transport protein RanGAP1 (red) clumps up with mutant huntingtin protein (green) in neurons.

Courtesy: Jonathan Grima


Grima J, Daigle J, Arbez N. Mutant huntingtin disrupts the nuclear pore complex. Neuron. 2017 Apr 5:94(1): 93-107. http://dx.doi.org/10.1016/j.neuron.2017.03.023.

An enhanced mouse model of Huntington disease

Nominee (Basic science)

By Amber Southwell, PhD

Considering the vast majority of Huntington disease (HD) patients are heterozygous, heterozygous HD mice are highly relevant for research. The zQ175 Knock-in (KI) model of HD arose as a natural expansion from Q140 KI mice, and, unlike its predecessor, exhibited substantial HD-like phenotypes when heterozygous. In an effort to increase severity of disease, we backcrossed zQ175 mice to FVB (Q175F), a strain particularly susceptible to mutant huntingtin (HTT)-induced neurodegeneration.

Interestingly, this introduced sudden, early death by fatal seizures. Seizures are not a feature of adult onset HD, but they are seen in FVB mice. The Q175 KI exacerbated these seizures from mild to fatal. HTT protects against FVB seizures, and the neomycin (neo) cassette used to generate the Q140 KI can reduce gene expression. Thus, we deleted the neo cassette generating Q175FDN mice. Q175FDN mice have about two-fold more KI Htt than Q175F mice and do not have fatal seizures, demonstrating that HD KI mice with an intact neo cassette can model HTT deficiency rather than HD. Q175FDN mice also display reduced survival, but death is preceded by an extended decline of body weight, gait, and activity. Moreover, Q175FDN mice display robust, early onset HD-like phenotypes, several of which are truly dominant, making them a superior preclinical model.


Southwell A, Smith-Dijak A, Kay C. An enhanced Q175 knock-in mouse model of Huntington disease with higher mutant huntingtin levels and accelerated disease phenotypes. Hum. Mol. Genet. 2016 25(17):3654-3675. doi: 10.1093/hmg/ddw212. 

A longitudinal analysis of the intermediate alleles carriers’ clinical manifestations in Huntington’s disease

Nominee (Clinical research)

By Esther Cubo, MD, PhD

After the characterization of the gene mutation, a distinct category of HD genes named intermediate alleles (IAs) has been recognized. IAs have been consensually defined as those with a CAG repeat size between 27 and 35, a range just below the disease threshold of 36 repeats. It has been shown that IAs confer genetic instability, and might broaden into the disease range within one generation through the paternal line and, exceptionally, the maternal line. The prevalence of IAs varies between 1.5–5.8% in both the general population and HD families, showing no significant differences between them, and with similar haplotype distributions. Although IAs are not considered to be associated with the HD phenotype, there has been emerging evidence that some individuals with IAs might develop HD-like clinical and neuropathological manifestations. Our study was designed to establish the clinical manifestations of IA carriers for a prospective European HD registry.

We assessed a cohort of participants at risk with <36 CAG repeats of the HTT gene. Outcome measures were the UHDRS motor, cognitive, and behavior domains; total functional capacity (TFC); and quality of life (SF-36). This cohort was subdivided into IA carriers (27–35 CAG) and controls (<27 CAG), and younger versus older participants. We have analyzed and compared the clinical manifestations in elderly versus young patients, and IAs versus non-expanded controls in terms of UHDRS scores, and by subdividing the UHDRS into chorea, bradykinesia, dystonia, and gait domains. In addition, we analyzed the association of several environmental factors, treatments, and sociodemographics with clinical manifestations.

In this study, 12,190 participants of the European HD registry – 657 (5.38%) with <36 CAG repeats, 76 IAs (11.56%), and 581 controls (88.44%) – were included. After correcting for multiple comparisons, at baseline, IA participants were similar to controls in terms of age, quality of life, TFC, total UHDRS motor, behavior and cognitive scores, use of antidopaminergic drugs, body mass index, education background, tobacco and alcohol exposure, residence, and marital and working status. However, older participants with IAs had higher chorea scores compared to controls (p = 0.001). Linear regression analysis showed that aging was the most contributing factor to increased UHDRS motor scores (p = 0.002). On the other hand, one-year follow-up data analysis showed that IA carrier participants had greater cognitive decline compared to controls (p = 0.002).

The results of this study highlight the need for longitudinal data of IA clinical manifestations, which are classically underrepresented in observational registries. Based on these results and prior observations of IA-associated late-onset HD, the allele ranges might warrant further adjustment so that the category of reduced penetrance extends to include shorter expansion lengths stretching into the IA range. These results have important implications for clinical practice and genetic counseling for those individuals who are IA carriers.


Cubo E, Ramos-Arroyo M, Martinez-Horta S. Clinical manifestations of intermediate allele carriers in Huntington disease. Neurology 2016 87(6):571-8. doi: 10.1212/WNL.0000000000002944.

The CREST-E study for Huntington’s disease

Nominee (Clinical research)

By Steven Hersch, MD, PhD

Our manuscript is the primary report for the CREST-E study (Creatine Safety, Tolerability and Efficacy), which was sponsored by the NIH and the FDA, and conducted by the Huntington Study Group in North America and Australasia. Creatine was previously demonstrated to be neuroprotective in animal models, and to slow progressive brain atrophy in presymptomatic HD patients. CREST-E was designed to assess the efficacy of high-dose creatine (up to 40 grams daily) in early symptomatic HD patients for slowing progressive functional decline.

The study opened for enrollment in 2009, and included more than 550 subjects by the time clinical activity ended in 2014 following a preplanned interim analysis that suggested that the study was very unlikely to show overall benefit of creatine. Lack of benefit was confirmed in the primary analysis, although preplanned secondary analyses raised the possibility of unexpected differential effects in males and females.

The legacy of CREST-E includes the unique clinical experience with high-dose and long-term creatine administration; a large safety database for a widely used supplement; longitudinal outcomes data for early HD that will be applicable to future clinical trials; identification of possible interactions between gender, HD, and creatine; and extensive biological and neuroimaging biomarker data that continue to be analyzed.


Hersch S, Schifitto G, Oakes D, et al. The CREST-E study of creatine for Huntington disease: A randomized controlled trial. Neurology. 2017 Aug 8;89(6):594-601. doi: 10.1212/WNL.0000000000004209. Epub 2017 Jul 1.

Symptom heterogeneity correlates with neuronal degeneration

Nominee (Biomarkers and imaging)

By Nasim Mehrabi, PhD

This study completed the overview of cortical cell degeneration in HD by specifically focusing on loss of inhibitory interneurons in three functionally distinct areas of the human brain (primary sensory cortex, superior frontal cortex, and superior parietal cortex) in HD patients compared to neurologically normal individuals. Based on their predominant symptom, the HD patients were grouped into three different symptom groups (‘motor’, ‘mood’, and ‘mixed’).

The results of this study demonstrated a heterogeneous loss of interneurons in these cortical areas, which correlated with the variable symptom profiles of the HD cases. For example, we observed a significant loss of interneurons in the primary sensory cortex of the ‘motor’ cases, but not in the ‘mood’ cases. We are now extending our research on differential cell loss in HD to other parts of the ‘motor circuitry’, such as the thalamus and cerebellum.


Mehrabi N, Waldvogel H, Tippett L. Symptom heterogeneity in Huntington’s disease correlates with neuronal degeneration in the cerebral cortex. Neurobiol Dis. 2016 Dec;96:67-74. doi: 10.1016/j.nbd.2016.08.015. Epub 2016 Aug 25.

Additional Nominated Papers

Yang S, Chang R, Yang H, et al. CRISPR/Cas9-mediated gene editing ameliorates neurotoxicity in mouse model of Huntington’s disease. J Clin Invest. 2017 127(7):2719-2724. doi: 10.1172/JCI92087.

Carsten S. Identifying modifiers of Huntington’s disease progression. Lancet: Neurology Online First 2017 Sep;16(9):679-680. doi: 10.1016/S1474-4422(17)30179-5.

McGarry A, McDermott M, Kieburtz K. A randomized, double-blind, placebo-controlled trial of coenzyme Q10 in Huntington disease. Neurology 2017 88(2):152-159. doi: 10.1212/WNL.0000000000003478.

Gorges, M, Müller H, Mayer I Intact sensory-motor network structure and function in far from onset premanifest Huntington’s disease. Sci. Rep. 2017 7:43841. doi: 10.1038/srep43841.

Skene D, Middleton B, Fraser C, et al. Metabolic profiling of presymptomatic Huntington’s disease sheep reveals novel biomarkers. Sci. Rep. 2017 7:43030. doi: 10.1038/srep43030.

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