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August 2016; 2 (4) ArticleOpen Access

Trans-pQTL study identifies immune crosstalk between Parkinson and Alzheimer loci

Gail Chan, Charles C. White, Phoebe A. Winn, Maria Cimpean, Joseph M. Replogle, Laura R. Glick, Nicole E. Cuerdon, Katie J. Ryan, Keith A. Johnson, Julie A. Schneider, David A. Bennett, Lori B. Chibnik, Reisa A. Sperling, Philip L. De Jager, Elizabeth M. Bradshaw
First published July 26, 2016, DOI: https://doi.org/10.1212/NXG.0000000000000090
Gail Chan
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Charles C. White
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Phoebe A. Winn
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Maria Cimpean
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Joseph M. Replogle
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Laura R. Glick
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Nicole E. Cuerdon
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Katie J. Ryan
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Keith A. Johnson
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Julie A. Schneider
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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David A. Bennett
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Lori B. Chibnik
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Reisa A. Sperling
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Philip L. De Jager
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Elizabeth M. Bradshaw
From the Ann Romney Center for Neurologic Diseases (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Program in Translational NeuroPsychiatric Genomics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Institute for the Neurosciences, Departments of Neurology and Psychiatry, Center for Alzheimer's Research and Treatment (K.A.J., R.A.S.), Department of Neurology, Brigham and Women's Hospital, Boston, MA; Program in Medical and Population Genetics (G.C., C.C.W., P.A.W., M.C., J.M.R., L.R.G., N.E.C., K.J.R., L.B.C., P.L.D.J., E.M.B.), Broad Institute, Cambridge, MA; Harvard Medical School (G.C., J.M.R., K.J.R., K.A.J., L.B.C., R.A.S., P.L.D.J., E.M.B.), Boston, MA; Department of Neurology (K.A.J., R.A.S.), Massachusetts General Hospital, Boston; and Rush Alzheimer's Disease Center (J.A.S., D.A.B.), Rush University Medical Center, Chicago, IL.
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Full PDF
Citation
Trans-pQTL study identifies immune crosstalk between Parkinson and Alzheimer loci
Gail Chan, Charles C. White, Phoebe A. Winn, Maria Cimpean, Joseph M. Replogle, Laura R. Glick, Nicole E. Cuerdon, Katie J. Ryan, Keith A. Johnson, Julie A. Schneider, David A. Bennett, Lori B. Chibnik, Reisa A. Sperling, Philip L. De Jager, Elizabeth M. Bradshaw
Neurol Genet Aug 2016, 2 (4) e90; DOI: 10.1212/NXG.0000000000000090

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Abstract

Objective: Given evidence from genetic studies, we hypothesized that there may be a shared component to the role of myeloid function in Parkinson and Alzheimer disease (PD and AD) and assessed whether PD susceptibility variants influenced protein expression of well-established AD-associated myeloid genes in human monocytes.

Methods: We repurposed data in which AD-related myeloid proteins CD33, TREM1, TREM2, TREML2, TYROBP, and PTK2B were measured by flow cytometry in monocytes from 176 participants of the PhenoGenetic Project (PGP) and Harvard Aging Brain Study. Linear regression was used to identify associations between 24 PD risk variants and protein expression. The 2 cohorts were meta-analyzed in a discovery analysis, and the 4 most strongly suggestive results were validated in an independent cohort of 50 PGP participants.

Results: We discovered and validated an association between the PD risk allele rs12456492G in the RIT2 locus and increased CD33 expression (pjoint = 3.50 × 10−5) and found strongly suggestive evidence that rs11060180A in the CCDC62/HIP1R locus decreased PTK2B expression (pjoint = 1.12 × 10−4). Furthermore, in older individuals, increased CD33 expression on peripheral monocytes was associated with a greater burden of parkinsonism (p = 0.047), particularly bradykinesia (p = 6.64 × 10−3).

Conclusions: We find that the rs12456492 PD risk variant affects expression of AD-associated protein CD33 in peripheral monocytes, which suggests that genetic factors for these 2 diseases may converge to influence overlapping innate immune-mediated mechanisms that contribute to neurodegeneration. Furthermore, the effect of the rs12456492G PD risk allele on increased CD33 suggests that the inhibition of certain myeloid functions may contribute to PD susceptibility, as is the case for AD.

GLOSSARY

AD=
Alzheimer disease;
DLPFC=
dorsolateral prefrontal cortex;
eQTL=
expression quantitative trait locus;
GWAS=
genome-wide association study;
HABS=
Harvard Aging Brain Study;
PD=
Parkinson disease;
PGP=
PhenoGenetic Project;
pQTL=
protein quantitative trait locus;
ROS-MAP=
Religious Orders Study and Memory and Aging Project;
SNP=
single nucleotide polymorphism

Footnotes

  • ↵* Co-last authors.

  • Funding information and disclosures are provided at the end of the article. Go to Neurology.org/ng for full disclosure forms. The Article Processing Charge was paid by the authors.

  • Supplemental data at Neurology.org/ng

  • Received March 15, 2016.
  • Accepted in final form June 15, 2016.
  • © 2016 American Academy of Neurology

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially.

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Neurology: Genetics | Online ISSN: 2376-7839

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