Longitudinal multi-omics of host–microbe dynamics in prediabetes
Type 2 diabetes mellitus (T2D) is a growing health problem, but little is known about its early disease stages, its effects on biological processes or the transition to clinical T2D. To understand the earliest stages of T2D better, we obtained samples from 106 healthy individuals and individuals wit...
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| Published in | Nature (London) Vol. 569; no. 7758; pp. 663 - 671 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.05.2019
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0028-0836 1476-4687 1476-4687 |
| DOI | 10.1038/s41586-019-1236-x |
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| Abstract | Type 2 diabetes mellitus (T2D) is a growing health problem, but little is known about its early disease stages, its effects on biological processes or the transition to clinical T2D. To understand the earliest stages of T2D better, we obtained samples from 106 healthy individuals and individuals with prediabetes over approximately four years and performed deep profiling of transcriptomes, metabolomes, cytokines, and proteomes, as well as changes in the microbiome. This rich longitudinal data set revealed many insights: first, healthy profiles are distinct among individuals while displaying diverse patterns of intra- and/or inter-personal variability. Second, extensive host and microbial changes occur during respiratory viral infections and immunization, and immunization triggers potentially protective responses that are distinct from responses to respiratory viral infections. Moreover, during respiratory viral infections, insulin-resistant participants respond differently than insulin-sensitive participants. Third, global co-association analyses among the thousands of profiled molecules reveal specific host–microbe interactions that differ between insulin-resistant and insulin-sensitive individuals. Last, we identified early personal molecular signatures in one individual that preceded the onset of T2D, including the inflammation markers interleukin-1 receptor agonist (IL-1RA) and high-sensitivity C-reactive protein (CRP) paired with xenobiotic-induced immune signalling. Our study reveals insights into pathways and responses that differ between glucose-dysregulated and healthy individuals during health and disease and provides an open-access data resource to enable further research into healthy, prediabetic and T2D states.
Deep profiling of transcriptomes, metabolomes, cytokines, and proteomes, alongside changes in the microbiome, in samples from individuals with and without prediabetes reveal insights into inter-individual variability and associations between changes in the microbiome and other factors. |
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| AbstractList | Type 2 diabetes mellitus (T2D) is a growing health problem, but little is known about its early disease stages, its effects on biological processes or the transition to clinical T2D. To understand the earliest stages of T2D better, we obtained samples from 106 healthy individuals and individuals with prediabetes over approximately four years and performed deep profiling of transcriptomes, metabolomes, cytokines, and proteomes, as well as changes in the microbiome. This rich longitudinal data set revealed many insights: first, healthy profiles are distinct among individuals while displaying diverse patterns of intra- and/or inter-personal variability. Second, extensive host and microbial changes occur during respiratory viral infections and immunization, and immunization triggers potentially protective responses that are distinct from responses to respiratory viral infections. Moreover, during respiratory viral infections, insulin-resistant participants respond differently than insulin-sensitive participants. Third, global co-association analyses among the thousands of profiled molecules reveal specific host–microbe interactions that differ between insulin-resistant and insulin-sensitive individuals. Last, we identified early personal molecular signatures in one individual that preceded the onset of T2D, including the inflammation markers interleukin-1 receptor agonist (IL-1RA) and high-sensitivity C-reactive protein (CRP) paired with xenobiotic-induced immune signalling. Our study reveals insights into pathways and responses that differ between glucose-dysregulated and healthy individuals during health and disease and provides an open-access data resource to enable further research into healthy, prediabetic and T2D states. Type 2 diabetes mellitus (T2D) is a growing health problem, but little is known about its early disease stages, its effects on biological processes or the transition to clinical T2D. To understand the earliest stages of T2D better, we obtained samples from 106 healthy individuals and individuals with prediabetes over approximately four years and performed deep profiling of transcriptomes, metabolomes, cytokines, and proteomes, as well as changes in the microbiome. This rich longitudinal data set revealed many insights: first, healthy profiles are distinct among individuals while displaying diverse patterns of intra- and/or inter-personal variability. Second, extensive host and microbial changes occur during respiratory viral infections and immunization, and immunization triggers potentially protective responses that are distinct from responses to respiratory viral infections. Moreover, during respiratory viral infections, insulin-resistant participants respond differently than insulin-sensitive participants. Third, global co-association analyses among the thousands of profiled molecules reveal specific host-microbe interactions that differ between insulin-resistant and insulin-sensitive individuals. Last, we identified early personal molecular signatures in one individual that preceded the onset of T2D, including the inflammation markers interleukin-1 receptor agonist (IL-1RA) and high-sensitivity C-reactive protein (CRP) paired with xenobiotic-induced immune signalling. Our study reveals insights into pathways and responses that differ between glucose-dysregulated and healthy individuals during health and disease and provides an open-access data resource to enable further research into healthy, prediabetic and T2D states. Type 2 diabetes mellitus (T2D) is a growing health problem, but little is known about its early disease stages, its effects on biological processes or the transition to clinical T2D. To understand the earliest stages of T2D better, we obtained samples from 106 healthy individuals and individuals with prediabetes over approximately four years and performed deep profiling of transcriptomes, metabolomes, cytokines, and proteomes, as well as changes in the microbiome. This rich longitudinal data set revealed many insights: first, healthy profiles are distinct among individuals while displaying diverse patterns of intra- and/or inter-personal variability. Second, extensive host and microbial changes occur during respiratory viral infections and immunization, and immunization triggers potentially protective responses that are distinct from responses to respiratory viral infections. Moreover, during respiratory viral infections, insulin-resistant participants respond differently than insulin-sensitive participants. Third, global co-association analyses among the thousands of profiled molecules reveal specific host–microbe interactions that differ between insulin-resistant and insulin-sensitive individuals. Last, we identified early personal molecular signatures in one individual that preceded the onset of T2D, including the inflammation markers interleukin-1 receptor agonist (IL-1RA) and high-sensitivity C-reactive protein (CRP) paired with xenobiotic-induced immune signalling. Our study reveals insights into pathways and responses that differ between glucose-dysregulated and healthy individuals during health and disease and provides an open-access data resource to enable further research into healthy, prediabetic and T2D states. Deep profiling of transcriptomes, metabolomes, cytokines, and proteomes, alongside changes in the microbiome, in samples from individuals with and without prediabetes reveal insights into inter-individual variability and associations between changes in the microbiome and other factors. Type 2 diabetes mellitus (T2D) is a growing health problem, but little is known about its early disease stages, its effects on biological processes or the transition to clinical T2D. To understand the earliest stages of T2D better, we obtained samples from 106 healthy individuals and individuals with prediabetes over approximately four years and performed deep profiling of transcriptomes, metabolomes, cytokines, and proteomes, as well as changes in the microbiome. This rich longitudinal data set revealed many insights: first, healthy profiles are distinct among individuals while displaying diverse patterns of intra- and/or inter-personal variability. Second, extensive host and microbial changes occur during respiratory viral infections and immunization, and immunization triggers potentially protective responses that are distinct from responses to respiratory viral infections. Moreover, during respiratory viral infections, insulin-resistant participants respond differently than insulin-sensitive participants. Third, global co-association analyses among the thousands of profiled molecules reveal specific host-microbe interactions that differ between insulin-resistant and insulin-sensitive individuals. Last, we identified early personal molecular signatures in one individual that preceded the onset of T2D, including the inflammation markers interleukin-1 receptor agonist (IL-1RA) and high-sensitivity C-reactive protein (CRP) paired with xenobiotic-induced immune signalling. Our study reveals insights into pathways and responses that differ between glucose-dysregulated and healthy individuals during health and disease and provides an open-access data resource to enable further research into healthy, prediabetic and T2D states. Deep profiling of transcriptomes, metabolomes, cytokines, and proteomes, alongside changes in the microbiome, in samples from individuals with and without prediabetes reveal insights into inter-individual variability and associations between changes in the microbiome and other factors. Type 2 diabetes mellitus (T2D) is a growing health problem, but little is known about its early disease stages, its effects on biological processes or the transition to clinical T2D. To understand the earliest stages of T2D better, we obtained samples from 106 healthy individuals and individuals with prediabetes over approximately four years and performed deep profiling of transcriptomes, metabolomes, cytokines, and proteomes, as well as changes in the microbiome. This rich longitudinal data set revealed many insights: first, healthy profiles are distinct among individuals while displaying diverse patterns of intra- and/or inter-personal variability. Second, extensive host and microbial changes occur during respiratory viral infections and immunization, and immunization triggers potentially protective responses that are distinct from responses to respiratory viral infections. Moreover, during respiratory viral infections, insulin-resistant participants respond differently than insulin-sensitive participants. Third, global co-association analyses among the thousands of profiled molecules reveal specific host-microbe interactions that differ between insulin-resistant and insulin-sensitive individuals. Last, we identified early personal molecular signatures in one individual that preceded the onset of T2D, including the inflammation markers interleukin-1 receptor agonist (IL-1RA) and high-sensitivity C-reactive protein (CRP) paired with xenobiotic-induced immune signalling. Our study reveals insights into pathways and responses that differ between glucose-dysregulated and healthy individuals during health and disease and provides an open-access data resource to enable further research into healthy, prediabetic and T2D states.Type 2 diabetes mellitus (T2D) is a growing health problem, but little is known about its early disease stages, its effects on biological processes or the transition to clinical T2D. To understand the earliest stages of T2D better, we obtained samples from 106 healthy individuals and individuals with prediabetes over approximately four years and performed deep profiling of transcriptomes, metabolomes, cytokines, and proteomes, as well as changes in the microbiome. This rich longitudinal data set revealed many insights: first, healthy profiles are distinct among individuals while displaying diverse patterns of intra- and/or inter-personal variability. Second, extensive host and microbial changes occur during respiratory viral infections and immunization, and immunization triggers potentially protective responses that are distinct from responses to respiratory viral infections. Moreover, during respiratory viral infections, insulin-resistant participants respond differently than insulin-sensitive participants. Third, global co-association analyses among the thousands of profiled molecules reveal specific host-microbe interactions that differ between insulin-resistant and insulin-sensitive individuals. Last, we identified early personal molecular signatures in one individual that preceded the onset of T2D, including the inflammation markers interleukin-1 receptor agonist (IL-1RA) and high-sensitivity C-reactive protein (CRP) paired with xenobiotic-induced immune signalling. Our study reveals insights into pathways and responses that differ between glucose-dysregulated and healthy individuals during health and disease and provides an open-access data resource to enable further research into healthy, prediabetic and T2D states. |
| Audience | Academic |
| Author | Liang, Liang Albright, Brandon Rost, Hannes Hornburg, Daniel Weinstock, George M. Leopold, Benjamin Perelman, Dalia Zhang, Martin J. Spakowicz, Daniel Limcaoco, Patricia Dunn, Jessilyn Hanson, Blake Sodergren, Erica Colbert, Elizabeth Lee-McMullen, Brittany McLaughlin, Tracey Chen, Lei Allister, Candice Zhou, Xin Snyder, Michael Johnson, Jethro Rao, Varsha Petersen, Lauren Craig, Colleen Metwally, Ahmed A. Tse, David Dagan-Rosenfeld, Orit Ashland, Melanie Leopold, Shana R. Sailani, M. Reza Zhou, Wenyu Avina, Monika Hong, Bo-Young Tran, Thi Dong Binh Bautista, Eddy Piening, Brian Nguyen, Hoan Zhou, Yanjiao Rego, Shannon Ahadi, Sara Mishra, Tejaswini Wei, Eric Kukurba, Kim Rose, Sophia Miryam Schüssler-Fiorenza Contrepois, Kévin Chen, Songjie Bahmani, Amir Chaib, Hassan Salins, Denis |
| Author_xml | – sequence: 1 givenname: Wenyu surname: Zhou fullname: Zhou, Wenyu organization: Department of Genetics, Stanford University School of Medicine – sequence: 2 givenname: M. Reza surname: Sailani fullname: Sailani, M. Reza organization: Department of Genetics, Stanford University School of Medicine – sequence: 3 givenname: Kévin surname: Contrepois fullname: Contrepois, Kévin organization: Department of Genetics, Stanford University School of Medicine – sequence: 4 givenname: Yanjiao surname: Zhou fullname: Zhou, Yanjiao organization: The Jackson Laboratory for Genomic Medicine, Department of Medicine, UConn Health – sequence: 5 givenname: Sara surname: Ahadi fullname: Ahadi, Sara organization: Department of Genetics, Stanford University School of Medicine – sequence: 6 givenname: Shana R. surname: Leopold fullname: Leopold, Shana R. organization: The Jackson Laboratory for Genomic Medicine – sequence: 7 givenname: Martin J. surname: Zhang fullname: Zhang, Martin J. organization: Department of Electrical Engineering, Stanford University – sequence: 8 givenname: Varsha surname: Rao fullname: Rao, Varsha organization: Department of Genetics, Stanford University School of Medicine – sequence: 9 givenname: Monika surname: Avina fullname: Avina, Monika organization: Department of Genetics, Stanford University School of Medicine – sequence: 10 givenname: Tejaswini surname: Mishra fullname: Mishra, Tejaswini organization: Department of Genetics, Stanford University School of Medicine – sequence: 11 givenname: Jethro surname: Johnson fullname: Johnson, Jethro organization: The Jackson Laboratory for Genomic Medicine – sequence: 12 givenname: Brittany surname: Lee-McMullen fullname: Lee-McMullen, Brittany organization: Department of Genetics, Stanford University School of Medicine – sequence: 13 givenname: Songjie surname: Chen fullname: Chen, Songjie organization: Department of Genetics, Stanford University School of Medicine – sequence: 14 givenname: Ahmed A. surname: Metwally fullname: Metwally, Ahmed A. organization: Department of Genetics, Stanford University School of Medicine – sequence: 15 givenname: Thi Dong Binh surname: Tran fullname: Tran, Thi Dong Binh organization: The Jackson Laboratory for Genomic Medicine – sequence: 16 givenname: Hoan surname: Nguyen fullname: Nguyen, Hoan organization: The Jackson Laboratory for Genomic Medicine – sequence: 17 givenname: Xin surname: Zhou fullname: Zhou, Xin organization: The Jackson Laboratory for Genomic Medicine – sequence: 18 givenname: Brandon surname: Albright fullname: Albright, Brandon organization: The Jackson Laboratory for Genomic Medicine – sequence: 19 givenname: Bo-Young surname: Hong fullname: Hong, Bo-Young organization: The Jackson Laboratory for Genomic Medicine – sequence: 20 givenname: Lauren surname: Petersen fullname: Petersen, Lauren organization: The Jackson Laboratory for Genomic Medicine – sequence: 21 givenname: Eddy surname: Bautista fullname: Bautista, Eddy organization: The Jackson Laboratory for Genomic Medicine – sequence: 22 givenname: Blake surname: Hanson fullname: Hanson, Blake organization: The Jackson Laboratory for Genomic Medicine – sequence: 23 givenname: Lei surname: Chen fullname: Chen, Lei organization: The Jackson Laboratory for Genomic Medicine – sequence: 24 givenname: Daniel surname: Spakowicz fullname: Spakowicz, Daniel organization: The Jackson Laboratory for Genomic Medicine – sequence: 25 givenname: Amir surname: Bahmani fullname: Bahmani, Amir organization: Stanford Center for Genomics and Personalized Medicine – sequence: 26 givenname: Denis surname: Salins fullname: Salins, Denis organization: Department of Genetics, Stanford University School of Medicine – sequence: 27 givenname: Benjamin surname: Leopold fullname: Leopold, Benjamin organization: The Jackson Laboratory for Genomic Medicine – sequence: 28 givenname: Melanie surname: Ashland fullname: Ashland, Melanie organization: Department of Genetics, Stanford University School of Medicine – sequence: 29 givenname: Orit surname: Dagan-Rosenfeld fullname: Dagan-Rosenfeld, Orit organization: Department of Genetics, Stanford University School of Medicine – sequence: 30 givenname: Shannon surname: Rego fullname: Rego, Shannon organization: Department of Genetics, Stanford University School of Medicine – sequence: 31 givenname: Patricia surname: Limcaoco fullname: Limcaoco, Patricia organization: Department of Genetics, Stanford University School of Medicine – sequence: 32 givenname: Elizabeth surname: Colbert fullname: Colbert, Elizabeth organization: Division of Endocrinology, Stanford University School of Medicine – sequence: 33 givenname: Candice surname: Allister fullname: Allister, Candice organization: Division of Endocrinology, Stanford University School of Medicine – sequence: 34 givenname: Dalia surname: Perelman fullname: Perelman, Dalia organization: Division of Endocrinology, Stanford University School of Medicine – sequence: 35 givenname: Colleen surname: Craig fullname: Craig, Colleen organization: Division of Endocrinology, Stanford University School of Medicine – sequence: 36 givenname: Eric surname: Wei fullname: Wei, Eric organization: Department of Genetics, Stanford University School of Medicine, Stanford Center for Genomics and Personalized Medicine – sequence: 37 givenname: Hassan surname: Chaib fullname: Chaib, Hassan organization: Department of Genetics, Stanford University School of Medicine, Stanford Center for Genomics and Personalized Medicine, Stanford Diabetes Research Center – sequence: 38 givenname: Daniel surname: Hornburg fullname: Hornburg, Daniel organization: Department of Genetics, Stanford University School of Medicine – sequence: 39 givenname: Jessilyn surname: Dunn fullname: Dunn, Jessilyn organization: Department of Genetics, Stanford University School of Medicine – sequence: 40 givenname: Liang surname: Liang fullname: Liang, Liang organization: Department of Genetics, Stanford University School of Medicine – sequence: 41 givenname: Sophia Miryam Schüssler-Fiorenza surname: Rose fullname: Rose, Sophia Miryam Schüssler-Fiorenza organization: Spinal Cord Injury Service, Veteran Affairs Palo Alto Health Care System, Department of Neurosurgery, Stanford University School of Medicine – sequence: 42 givenname: Kim surname: Kukurba fullname: Kukurba, Kim organization: Department of Genetics, Stanford University School of Medicine – sequence: 43 givenname: Brian surname: Piening fullname: Piening, Brian organization: Earle A Chiles Research Institute, Providence Cancer Center – sequence: 44 givenname: Hannes surname: Rost fullname: Rost, Hannes organization: Donnelly Centre for Cellular & Biomolecular Research, University of Toronto – sequence: 45 givenname: David surname: Tse fullname: Tse, David organization: Department of Electrical Engineering, Stanford University – sequence: 46 givenname: Tracey surname: McLaughlin fullname: McLaughlin, Tracey organization: Division of Endocrinology, Stanford University School of Medicine, Stanford Diabetes Research Center – sequence: 47 givenname: Erica surname: Sodergren fullname: Sodergren, Erica organization: The Jackson Laboratory for Genomic Medicine – sequence: 48 givenname: George M. surname: Weinstock fullname: Weinstock, George M. email: George.Weinstock@jax.org organization: The Jackson Laboratory for Genomic Medicine – sequence: 49 givenname: Michael surname: Snyder fullname: Snyder, Michael email: mpsnyder@stanford.edu organization: Department of Genetics, Stanford University School of Medicine, Stanford Center for Genomics and Personalized Medicine, Stanford Diabetes Research Center |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31142858$$D View this record in MEDLINE/PubMed |
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| Title | Longitudinal multi-omics of host–microbe dynamics in prediabetes |
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