Dysbiosis in the Gut Microbiota of Patients with Multiple Sclerosis, with a Striking Depletion of Species Belonging to Clostridia XIVa and IV Clusters

The pathogenesis of multiple sclerosis (MS), an autoimmune disease affecting the brain and spinal cord, remains poorly understood. Patients with MS typically present with recurrent episodes of neurological dysfunctions such as blindness, paresis, and sensory disturbances. Studies on experimental aut...

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Veröffentlicht in:	PloS one Jg. 10; H. 9; S. e0137429
Hauptverfasser:	Miyake, Sachiko, Kim, Sangwan, Suda, Wataru, Oshima, Kenshiro, Nakamura, Masakazu, Matsuoka, Takako, Chihara, Norio, Tomita, Atsuko, Sato, Wakiro, Kim, Seok-Won, Morita, Hidetoshi, Hattori, Masahira, Yamamura, Takashi
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States Public Library of Science 14.09.2015 Public Library of Science (PLoS)
Schlagworte:	Adult Allergies Animal models Autoimmune diseases Bacteria Bacteroidetes - genetics Bacteroidetes - metabolism Bioinformatics Biology Blindness Brain Cell culture Clostridia Clostridium - classification Clostridium - genetics Clostridium - metabolism Clusters Dysbacteriosis Dysbiosis - metabolism Dysbiosis - microbiology Experimental allergic encephalomyelitis Female Gastrointestinal Microbiome High-Throughput Nucleotide Sequencing Humans Immunology Immunoregulation Inflammatory bowel disease Intestinal microflora Japan Lymphocytes Lymphocytes T Male Metabolites Microbiota Multiple sclerosis Multiple Sclerosis - microbiology Multiple Sclerosis - physiopathology Neurological diseases Neurosciences Paresis Pathogenesis Patients Phylogenetics Phylogeny Relative abundance Ribonucleic acid RNA RNA, Bacterial - genetics RNA, Ribosomal, 16S - genetics rRNA 16S Sequence Analysis, RNA Species Spinal cord Womens health Japan
ISSN:	1932-6203, 1932-6203
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Abstract	The pathogenesis of multiple sclerosis (MS), an autoimmune disease affecting the brain and spinal cord, remains poorly understood. Patients with MS typically present with recurrent episodes of neurological dysfunctions such as blindness, paresis, and sensory disturbances. Studies on experimental autoimmune encephalomyelitis (EAE) animal models have led to a number of testable hypotheses including a hypothetical role of altered gut microbiota in the development of MS. To investigate whether gut microbiota in patients with MS is altered, we compared the gut microbiota of 20 Japanese patients with relapsing-remitting (RR) MS (MS20) with that of 40 healthy Japanese subjects (HC40) and an additional 18 healthy subjects (HC18). All the HC18 subjects repeatedly provided fecal samples over the course of months (158 samples in total). Analysis of the bacterial 16S ribosomal RNA (rRNA) gene by using a high-throughput culture-independent pyrosequencing method provided evidence of a moderate dysbiosis in the structure of gut microbiota in patients with MS. Furthermore, we found 21 species that showed significant differences in relative abundance between the MS20 and HC40 samples. On comparing MS samples to the 158 longitudinal HC18 samples, the differences were found to be reproducibly significant for most of the species. These taxa comprised primarily of clostridial species belonging to Clostridia clusters XIVa and IV and Bacteroidetes. The phylogenetic tree analysis revealed that none of the clostridial species that were significantly reduced in the gut microbiota of patients with MS overlapped with other spore-forming clostridial species capable of inducing colonic regulatory T cells (Treg), which prevent autoimmunity and allergies; this suggests that many of the clostridial species associated with MS might be distinct from those broadly associated with autoimmune conditions. Correcting the dysbiosis and altered gut microbiota might deserve consideration as a potential strategy for the prevention and treatment of MS.
AbstractList	The pathogenesis of multiple sclerosis (MS), an autoimmune disease affecting the brain and spinal cord, remains poorly understood. Patients with MS typically present with recurrent episodes of neurological dysfunctions such as blindness, paresis, and sensory disturbances. Studies on experimental autoimmune encephalomyelitis (EAE) animal models have led to a number of testable hypotheses including a hypothetical role of altered gut microbiota in the development of MS. To investigate whether gut microbiota in patients with MS is altered, we compared the gut microbiota of 20 Japanese patients with relapsing-remitting (RR) MS (MS20) with that of 40 healthy Japanese subjects (HC40) and an additional 18 healthy subjects (HC18). All the HC18 subjects repeatedly provided fecal samples over the course of months (158 samples in total). Analysis of the bacterial 16S ribosomal RNA (rRNA) gene by using a high-throughput culture-independent pyrosequencing method provided evidence of a moderate dysbiosis in the structure of gut microbiota in patients with MS. Furthermore, we found 21 species that showed significant differences in relative abundance between the MS20 and HC40 samples. On comparing MS samples to the 158 longitudinal HC18 samples, the differences were found to be reproducibly significant for most of the species. These taxa comprised primarily of clostridial species belonging to Clostridia clusters XIVa and IV and Bacteroidetes. The phylogenetic tree analysis revealed that none of the clostridial species that were significantly reduced in the gut microbiota of patients with MS overlapped with other spore-forming clostridial species capable of inducing colonic regulatory T cells (Treg), which prevent autoimmunity and allergies; this suggests that many of the clostridial species associated with MS might be distinct from those broadly associated with autoimmune conditions. Correcting the dysbiosis and altered gut microbiota might deserve consideration as a potential strategy for the prevention and treatment of MS. The pathogenesis of multiple sclerosis (MS), an autoimmune disease affecting the brain and spinal cord, remains poorly understood. Patients with MS typically present with recurrent episodes of neurological dysfunctions such as blindness, paresis, and sensory disturbances. Studies on experimental autoimmune encephalomyelitis (EAE) animal models have led to a number of testable hypotheses including a hypothetical role of altered gut microbiota in the development of MS. To investigate whether gut microbiota in patients with MS is altered, we compared the gut microbiota of 20 Japanese patients with relapsing-remitting (RR) MS (MS20) with that of 40 healthy Japanese subjects (HC40) and an additional 18 healthy subjects (HC18). All the HC18 subjects repeatedly provided fecal samples over the course of months (158 samples in total). Analysis of the bacterial 16S ribosomal RNA (rRNA) gene by using a high-throughput culture-independent pyrosequencing method provided evidence of a moderate dysbiosis in the structure of gut microbiota in patients with MS. Furthermore, we found 21 species that showed significant differences in relative abundance between the MS20 and HC40 samples. On comparing MS samples to the 158 longitudinal HC18 samples, the differences were found to be reproducibly significant for most of the species. These taxa comprised primarily of clostridial species belonging to Clostridia clusters XIVa and IV and Bacteroidetes. The phylogenetic tree analysis revealed that none of the clostridial species that were significantly reduced in the gut microbiota of patients with MS overlapped with other spore-forming clostridial species capable of inducing colonic regulatory T cells (Treg), which prevent autoimmunity and allergies; this suggests that many of the clostridial species associated with MS might be distinct from those broadly associated with autoimmune conditions. Correcting the dysbiosis and altered gut microbiota might deserve consideration as a potential strategy for the prevention and treatment of MS.The pathogenesis of multiple sclerosis (MS), an autoimmune disease affecting the brain and spinal cord, remains poorly understood. Patients with MS typically present with recurrent episodes of neurological dysfunctions such as blindness, paresis, and sensory disturbances. Studies on experimental autoimmune encephalomyelitis (EAE) animal models have led to a number of testable hypotheses including a hypothetical role of altered gut microbiota in the development of MS. To investigate whether gut microbiota in patients with MS is altered, we compared the gut microbiota of 20 Japanese patients with relapsing-remitting (RR) MS (MS20) with that of 40 healthy Japanese subjects (HC40) and an additional 18 healthy subjects (HC18). All the HC18 subjects repeatedly provided fecal samples over the course of months (158 samples in total). Analysis of the bacterial 16S ribosomal RNA (rRNA) gene by using a high-throughput culture-independent pyrosequencing method provided evidence of a moderate dysbiosis in the structure of gut microbiota in patients with MS. Furthermore, we found 21 species that showed significant differences in relative abundance between the MS20 and HC40 samples. On comparing MS samples to the 158 longitudinal HC18 samples, the differences were found to be reproducibly significant for most of the species. These taxa comprised primarily of clostridial species belonging to Clostridia clusters XIVa and IV and Bacteroidetes. The phylogenetic tree analysis revealed that none of the clostridial species that were significantly reduced in the gut microbiota of patients with MS overlapped with other spore-forming clostridial species capable of inducing colonic regulatory T cells (Treg), which prevent autoimmunity and allergies; this suggests that many of the clostridial species associated with MS might be distinct from those broadly associated with autoimmune conditions. Correcting the dysbiosis and altered gut microbiota might deserve consideration as a potential strategy for the prevention and treatment of MS.
Author	Chihara, Norio Oshima, Kenshiro Kim, Sangwan Hattori, Masahira Tomita, Atsuko Matsuoka, Takako Nakamura, Masakazu Sato, Wakiro Yamamura, Takashi Miyake, Sachiko Morita, Hidetoshi Suda, Wataru Kim, Seok-Won
AuthorAffiliation	2 Department of Immunology, Juntendo University School of Medicine, 2-1-1, Hongo, Bunkyo-ku, Tokyo 113–8421, Japan 3 Center for Omics and Bioinformatics, The Department of Computational Biology, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwanoha 5-1-5, Kashiwa, Chiba 277–8561, Japan 1 Department of Immunology, National Institute of Neuroscience, 4-1-1, Ogawa-Higashi, Kodaira, Tokyo 187–8502, Japan 5 School of Veterinary Medicine, Azabu University, 1-17-71 Fuchinobe, Chuo-ku, Sagamihara, Kanagawa 229–8501, Japan 4 Laboratory for Integrated Bioinformatics, RIKEN Center for Integrative Medical Sciences, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230–0045, Japan University of Illinois at Urbana-Champaign, UNITED STATES
AuthorAffiliation_xml	– name: 3 Center for Omics and Bioinformatics, The Department of Computational Biology, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwanoha 5-1-5, Kashiwa, Chiba 277–8561, Japan – name: 4 Laboratory for Integrated Bioinformatics, RIKEN Center for Integrative Medical Sciences, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230–0045, Japan – name: 5 School of Veterinary Medicine, Azabu University, 1-17-71 Fuchinobe, Chuo-ku, Sagamihara, Kanagawa 229–8501, Japan – name: University of Illinois at Urbana-Champaign, UNITED STATES – name: 1 Department of Immunology, National Institute of Neuroscience, 4-1-1, Ogawa-Higashi, Kodaira, Tokyo 187–8502, Japan – name: 2 Department of Immunology, Juntendo University School of Medicine, 2-1-1, Hongo, Bunkyo-ku, Tokyo 113–8421, Japan
Author_xml	– sequence: 1 givenname: Sachiko surname: Miyake fullname: Miyake, Sachiko – sequence: 2 givenname: Sangwan surname: Kim fullname: Kim, Sangwan – sequence: 3 givenname: Wataru surname: Suda fullname: Suda, Wataru – sequence: 4 givenname: Kenshiro surname: Oshima fullname: Oshima, Kenshiro – sequence: 5 givenname: Masakazu surname: Nakamura fullname: Nakamura, Masakazu – sequence: 6 givenname: Takako surname: Matsuoka fullname: Matsuoka, Takako – sequence: 7 givenname: Norio surname: Chihara fullname: Chihara, Norio – sequence: 8 givenname: Atsuko surname: Tomita fullname: Tomita, Atsuko – sequence: 9 givenname: Wakiro surname: Sato fullname: Sato, Wakiro – sequence: 10 givenname: Seok-Won surname: Kim fullname: Kim, Seok-Won – sequence: 11 givenname: Hidetoshi surname: Morita fullname: Morita, Hidetoshi – sequence: 12 givenname: Masahira surname: Hattori fullname: Hattori, Masahira – sequence: 13 givenname: Takashi surname: Yamamura fullname: Yamamura, Takashi
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/26367776$$D View this record in MEDLINE/PubMed
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Copyright	2015 Miyake et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2015 Miyake et al 2015 Miyake et al
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 ObjectType-Article-2 ObjectType-Feature-1 content type line 23 Competing Interests: The authors have declared that no competing interests exist. Conceived and designed the experiments: SM MH TY. Performed the experiments: HM SK W. Suda. Analyzed the data: SK W. Suda KO SWK. Wrote the paper: SM MH TY. Contributed to collecting patient samples and clinical data: MN TM NC AT W. Sato TY.
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Snippet	The pathogenesis of multiple sclerosis (MS), an autoimmune disease affecting the brain and spinal cord, remains poorly understood. Patients with MS typically...
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SubjectTerms	Adult Allergies Animal models Autoimmune diseases Bacteria Bacteroidetes - genetics Bacteroidetes - metabolism Bioinformatics Biology Blindness Brain Cell culture Clostridia Clostridium - classification Clostridium - genetics Clostridium - metabolism Clusters Dysbacteriosis Dysbiosis - metabolism Dysbiosis - microbiology Experimental allergic encephalomyelitis Female Gastrointestinal Microbiome High-Throughput Nucleotide Sequencing Humans Immunology Immunoregulation Inflammatory bowel disease Intestinal microflora Japan Lymphocytes Lymphocytes T Male Metabolites Microbiota Multiple sclerosis Multiple Sclerosis - microbiology Multiple Sclerosis - physiopathology Neurological diseases Neurosciences Paresis Pathogenesis Patients Phylogenetics Phylogeny Relative abundance Ribonucleic acid RNA RNA, Bacterial - genetics RNA, Ribosomal, 16S - genetics rRNA 16S Sequence Analysis, RNA Species Spinal cord Womens health
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Title	Dysbiosis in the Gut Microbiota of Patients with Multiple Sclerosis, with a Striking Depletion of Species Belonging to Clostridia XIVa and IV Clusters
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