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June 2015; 1 (1) ArticleOpen Access

Phenotypic and molecular analyses of primary lateral sclerosis

Hiroshi Mitsumoto, Peter L. Nagy, Chris Gennings, Jennifer Murphy, Howard Andrews, Raymond Goetz, Mary Kay Floeter, Jonathan Hupf, Jessica Singleton, Richard J. Barohn, Sharon Nations, Christen Shoesmith, Edward Kasarskis, Pam Factor-Litvak
First published April 16, 2015, DOI: https://doi.org/10.1212/01.NXG.0000464294.88607.dd
Hiroshi Mitsumoto
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Peter L. Nagy
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Chris Gennings
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Jennifer Murphy
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Howard Andrews
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Raymond Goetz
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Mary Kay Floeter
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Jonathan Hupf
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Jessica Singleton
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Richard J. Barohn
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Sharon Nations
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Christen Shoesmith
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Edward Kasarskis
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Pam Factor-Litvak
From the Department of Neurology (H.M., J.H., J.S.), Eleanor and Lou Gehrig MDA/ALS Research Center, Columbia University Medical Center (CUMC), New York, NY; Department of Pathology and Cell Biology (P.L.N.), Personalized Genomic Medicine Laboratory, CUMC, New York, NY; Department of Biostatistics (C.G.), Virginia Commonwealth University, Richmond, VA; Department of Neurology (J.M.), University of California, San Francisco, CA; Departments of Biostatistics and Psychiatry (H.A., R.G.), Mailman School of Medicine, CUMC, New York, NY; Clinical Neuroscience Program (M.K.F.), NINDS, NIH, Bethesda, MD; Department of Neurology (R.J.B.), University of Kansas, Lawrence, KS; Department of Neurology (S.N.), University of Texas Southwestern Medical Center, Dallas, TX; Department of Neurology (C.S.), Western University, London, Ontario, Canada; Department of Neurology (E.K.), University of Kentucky, Lexington, KY; and Department of Epidemiology (P.F.-L), Mailman School of Public Health, CUMC, New York, NY.
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Citation
Phenotypic and molecular analyses of primary lateral sclerosis
Hiroshi Mitsumoto, Peter L. Nagy, Chris Gennings, Jennifer Murphy, Howard Andrews, Raymond Goetz, Mary Kay Floeter, Jonathan Hupf, Jessica Singleton, Richard J. Barohn, Sharon Nations, Christen Shoesmith, Edward Kasarskis, Pam Factor-Litvak
Neurol Genet Jun 2015, 1 (1) e3; DOI: 10.1212/01.NXG.0000464294.88607.dd

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Abstract

Objective: To understand phenotypic and molecular characteristics of patients with clinically “definite” primary lateral sclerosis (PLS) in a prospective study.

Methods: Six sites enrolled 41 patients who had pure upper motor neuron dysfunction, bulbar symptoms, a normal EMG done within 12 months of enrollment, and onset of symptoms ≥5 years before enrollment. For phenotypic analyses, 27 demographic, clinical, and cognitive variables were analyzed using the k-means clustering method. For molecular studies, 34 available DNA samples were tested for the C9ORF72 mutation, and exome sequencing was performed to exclude other neurologic diseases with known genetic cause.

Results: K-means clustering using the 25 patients with complete datasets suggested that patients with PLS can be classified into 2 groups based on clinical variables, namely dysphagia, objective bulbar signs, and urinary urgency. Secondary analyses performed in all 41 patients and including only variables with complete data corroborated the results from the primary analysis. We found no evidence that neurocognitive variables are important in classifying patients with PLS. Molecular studies identified C9ORF72 expansion in one patient. Well-characterized pathogenic mutations were identified in SPG7, DCTN1, and PARK2. Most cases showed no known relevant mutations.

Conclusions: Cluster analyses based on clinical variables indicated at least 2 subgroups of clinically definite PLS. Molecular analyses further identified 4 cases with mutations associated with amyotrophic lateral sclerosis, Parkinson disease, and possibly hereditary spastic paraplegia. Phenotypic and molecular characterization is the first step in investigating biological clues toward the definition of PLS. Further studies with larger numbers of patients are essential.

GLOSSARY

ALS=
amyotrophic lateral sclerosis;
ALS-CBS=
Amyotrophic Lateral Sclerosis-Cognitive Behavioral Screen;
COWAT=
Controlled Oral Word Association Test;
HSP=
hereditary spastic paraplegia;
IRB=
Institutional Review Board;
LMN=
lower motor neuron;
LPGM=
Laboratory of Personalized Genomic Medicine;
MND=
motor neuron disease;
PD=
Parkinson disease;
PLS=
primary lateral sclerosis;
SNP=
single nucleotide polymorphism;
UMN=
upper motor neuron

Footnotes

  • PLS Study COSMOS Group coinvestigators are listed at Neurology.org/ng

  • 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 Columbia University.

  • Supplemental data at Neurology.org/ng

  • Received February 9, 2015.
  • Accepted in final form March 17, 2015.
  • © 2015 American Academy of Neurology

This is an open access article distributed under the terms of the Creative Commons Attribution-Noncommercial No Derivative 3.0 License, 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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