Cited by 134Bone Metabolism and DiseasesConnective tissue disorders researchGenomics and Rare Diseases

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Bi-allelic CSF1R Mutations Cause Skeletal Dysplasia of Dysosteosclerosis-Pyle Disease Spectrum and Degenerative Encephalopathy with Brain Malformation

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Guo, Long, Bertola, Débora Romeo, Takanohashi, Asako, Saito, Asuka, Segawa, Yuko, Yokota, Takanori, Ishibashi, Satoru, Nishida, Yoichiro, Yamamoto, Guilherme Lopes, Franco, José Francisco da Silva, Honjo, Rachel Sayuri, Kim, Chong Ae, Musso, Camila Manso, Timmons, Margaret, Pizzino, Amy, Taft, Ryan J., Lajoie, Bryan, Knight, Melanie A., Fischbeck, Kenneth H., Singleton, Andrew B., Ferreira, Carlos R., Wang, Zheng, Yan, Li, Garbern, James Y., Simsek-Kiper, Pelin O., Ohashi, Hirofumi, Robey, Pamela G., Boyde, Alan, Matsumoto, Naomichi, Miyake, Noriko, Spranger, Jürgen, Schiffmann, Raphael, Vanderver, Adeline, Nishimura, Gen, Passos-Bueno, Maria Rita dos Santos, Simons, Cas, Ishikawa, Kinya, Ikegawa, Shiro·2019·The American Journal of Human Genetics

DOI 10.1016/j.ajhg.2019.03.004PMC PMC6507048

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Abstract

Colony stimulating factor 1 receptor (CSF1R) plays key roles in regulating development and function of the monocyte/macrophage lineage, including microglia and osteoclasts. Mono-allelic mutations of CSF1R are known to cause hereditary diffuse leukoencephalopathy with spheroids (HDLS), an adult-onset progressive neurodegenerative disorder. Here, we report seven affected individuals from three unrelated families who had bi-allelic CSF1R mutations. In addition to early-onset HDLS-like neurological disorders, they had brain malformations and skeletal dysplasia compatible to dysosteosclerosis (DOS) or Pyle disease. We identified five CSF1R mutations that were homozygous or compound heterozygous in these affected individuals. Two of them were deep intronic mutations resulting in abnormal inclusion of intron sequences in the mRNA. Compared with Csf1r-null mice, the skeletal and neural phenotypes of the affected individuals appeared milder and variable, suggesting that at least one of the mutations in each affected individual is hypomorphic. Our results characterized a unique human skeletal phenotype caused by CSF1R deficiency and implied that bi-allelic CSF1R mutations cause a spectrum of neurological and skeletal disorders, probably depending on the residual CSF1R function.

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Authors: Guo, L., Bertola, D. R., Takanohashi, A., Saito, A., Segawa, Y., Yokota, T., Ishibashi, S., Nishida, Y., Yamamoto, G. L., Franco, J. F. D. S., Honjo, R. S., Kim, C. A., Musso, C. M., Timmons, M., Pizzino, A., Taft, R. J., Lajoie, B., Knight, M. A., Fischbeck, K. H., Singleton, A. B., Ferreira, C. R., Wang, Z., Yan, L., Garbern, J. Y., Simsek-Kiper, P. O., Ohashi, H., Robey, P. G., Boyde, A., Matsumoto, N., Miyake, N., Spranger, J., Schiffmann, R., Vanderver, A., Nishimura, G., Passos-Bueno, M. R. D. S., Simons, C., Ishikawa, K., & Ikegawa, S.
Affiliations: RIKEN Center for Integrative Medical Sciences (JP)
Universidade de São Paulo (BR)
Children's Hospital of Philadelphia (US)
Tokyo Medical and Dental University (JP)
Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo (BR)
National Institutes of Health (US)
Illumina (United States) (US)
Chinese Academy of Medical Sciences & Peking Union Medical College (CN)
Wayne State University (US)
Saitama Children's Medical Center (JP)
Queen Mary University of London (GB)
Yokohama City University (JP)
Greenwood Genetic Center (US)
Baylor Scott & White Research Institute (US)
Saitama University (JP)
Royal Children's Hospital (AU)
Corresponding author: Bertola, Débora Romeo
Ikegawa, Shiro
ORCID: Guo, Long
Bertola, Débora Romeo
Takanohashi, Asako
Yokota, Takanori
Ishibashi, Satoru
Nishida, Yoichiro
Yamamoto, Guilherme Lopes
Honjo, Rachel Sayuri
Kim, Chong Ae
Musso, Camila Manso
Pizzino, Amy
Taft, Ryan J.
Lajoie, Bryan
Fischbeck, Kenneth H.
Singleton, Andrew B.
Ferreira, Carlos R.
Wang, Zheng
Ohashi, Hirofumi
Robey, Pamela G.
Boyde, Alan
Matsumoto, Naomichi
Miyake, Noriko
Spranger, Jürgen
Schiffmann, Raphael
Vanderver, Adeline
Nishimura, Gen
Simons, Cas
Ishikawa, Kinya
Ikegawa, Shiro
Venue: The American Journal of Human Genetics
Publisher: Elsevier BV
Published: 2019-05
Volume: 104
Issue: 5
Pages: 925-935
ISSN: 0002-9297 (ISSN-L)
DOI: 10.1016/j.ajhg.2019.03.004
PMC: PMC6507048
OpenAlex: W2937350838
Cited by: 133
References: 36
Citations by year: 2026: 16 · 2025: 13 · 2024: 17 · 2023: 11 · 2022: 21 · 2021: 21 · 2020: 25 · 2019: 9
FWCI: 6.28
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 185 d)
Locations: The American Journal of Human Genetics (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Queen Mary Research Online (Queen Mary University of London) (submittedVersion, cc-by-nc-nd)
Funders: National Health and Medical Research Council (NHMRC 1068278)
Japan Agency for Medical Research and Development (14525125)
Fundação de Amparo à Pesquisa do Estado de São Paulo (2015/21783-9/CEPID 2013/08028-1)
Japan Society for the Promotion of Science (17K16710)
Conselho Nacional de Desenvolvimento Científico e Tecnológico (304130/2016-8)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Connective tissue disorders research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomics and Rare Diseases
Keywords: CSF1R, biallelic variants, compound heterozygosity, skeletal dysplasia, hereditary diffuse leukoencephalopathy with spheroids, brain malformations, intronic variants, hypomorphic mutation, osteoclasts, microglia, monocyte/macrophage lineage, genotype-phenotype correlation
MeSH terms: Adolescent, Adult, Alleles, Animals, Brain, Child, Preschool, Female, Humans, Male, Mutation, Osteochondrodysplasias, Osteosclerosis, Phenotype, Receptor, Macrophage Colony-Stimulating Factor, Receptors, Granulocyte-Macrophage Colony-Stimulating Factor, Mice, Knockout, Mice, Young Adult, Leukoencephalopathies

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Bi-allelic CSF1R Mutations Cause Skeletal Dysplasia of Dysosteosclerosis-Pyle Disease Spectrum and Degenerative Encephalopathy with Brain Malformation

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