Integrative analysis of blood and gut microbiota data suggests a non-alcoholic fatty liver disease (NAFLD)-related disorder in French SLA


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
14 01 2020
Historique:
received: 13 08 2019
accepted: 18 12 2019
entrez: 16 1 2020
pubmed: 16 1 2020
medline: 11 11 2020
Statut: epublish

Résumé

Minipigs are a group of small-sized swine lines, which show a broad range of phenotype variation and which often tend to be obese. The SLA

Identifiants

pubmed: 31937803
doi: 10.1038/s41598-019-57127-x
pii: 10.1038/s41598-019-57127-x
pmc: PMC6959234
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

234

Références

McAnulty, P. et al. Minipig in Biomedical Research. Minipig in Biomedical Research, https://doi.org/10.1201/b11356-38 (RC Press, Boca Raton, 2012).
doi: 10.1201/b11356-38
Larzul, C. Pig genetics: insight in minipigs. Bilater. Symp. Miniat. Pigs Biomed. Res. Taiwan Fr. 1–6 (2013).
Bourneuf, E. et al. New susceptibility loci for cutaneous melanoma risk and progression revealed using a porcine model. Oncotarget 9, 27682–27697 (2018).
pubmed: 29963229 pmcid: 6021234 doi: 10.18632/oncotarget.25455
Sachs, D. H. The pig as a potential xenograft donor. Vet. Immunol. Immunopathol. 43, 185–191 (1994).
pubmed: 7856051 doi: 10.1016/0165-2427(94)90135-X pmcid: 7856051
Byrne, C. D. & Targher, G. NAFLD: A multisystem disease. J. Hepatol. 62, S47–S64 (2015).
pubmed: 25920090 doi: 10.1016/j.jhep.2014.12.012 pmcid: 25920090
van Koppen, A. et al. Uncovering a Predictive Molecular Signature for the Onset of NASH-Related Fibrosis in a Translational NASH Mouse Model. Cell. Mol. Gastroenterol. Hepatol. 5, 83–98 (2017).
pubmed: 29276754 pmcid: 5738456 doi: 10.1016/j.jcmgh.2017.10.001
Ryaboshapkina, M. & Hammar, M. Human hepatic gene expression signature of non-alcoholic fatty liver disease progression, a meta-analysis. Sci. Rep. 7 (2017).
Greco, D. et al. Gene expression in human NAFLD. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G1281–7 (2008).
pubmed: 18388185 doi: 10.1152/ajpgi.00074.2008 pmcid: 18388185
Fabbrini, E., Sullivan, S. & Klein, S. Obesity and nonalcoholic fatty liver disease: Biochemical, metabolic, and clinical implications. Hepatology 51, 679–689 (2010).
pubmed: 20041406 pmcid: 20041406 doi: 10.1002/hep.23280
Patil, R. & Sood, G. K. Non-alcoholic fatty liver disease and cardiovascular risk. World J. Gastrointest. Pathophysiol. 8, 51–58 (2017).
pubmed: 28573067 pmcid: 5437502 doi: 10.4291/wjgp.v8.i2.51
Berlanga, A., Guiu-Jurado, E., Porras, J. A. & Auguet, T. Molecular pathways in non-alcoholic fatty liver disease. Clin. Exp. Gastroenterol. 7, 221–239 (2014).
pubmed: 25045276 pmcid: 4094580
Paschos, P. & Paletas, K. Non alcoholic fatty liver disease and metabolic syndrome. Hippokratia 13, 9–19 (2009).
pubmed: 19240815 pmcid: 2633261
Baciu, C. et al. Systematic integrative analysis of gene expression identifies HNF4A as the central gene in pathogenesis of non-alcoholic steatohepatitis. PLoS One 12, 1–14 (2017).
doi: 10.1371/journal.pone.0189223
Zhu, R. et al. Systematic transcriptome analysis reveals elevated expression of alcohol-metabolizing genes in NAFLD livers. J. Pathol. 238, 531–542 (2016).
pubmed: 26415102 doi: 10.1002/path.4650 pmcid: 26415102
Xia, J. et al. Transcriptome analysis on the inflammatory cell infiltration of nonalcoholic steatohepatitis in Bama minipigs induced by a long-term high-fat, high-sucrose diet. PLoS One 9 (2014).
pubmed: 25415189 pmcid: 4240652 doi: 10.1371/journal.pone.0113724
Matz-Soja, M. et al. Hedgehog signaling is a potent regulator of liver lipid metabolism and reveals a GLI-code associated with steatosis. Elife 5, 1–28 (2016).
doi: 10.7554/eLife.13308
Spurlock, M. E. & Gabler, N. K. The development of porcine models of obesity and the metabolic syndrome. J. Nutr. 138, 397–402 (2008).
pubmed: 18203910 doi: 10.1093/jn/138.2.397 pmcid: 18203910
Kanuri, G. & Bergheim, I. In vitro and in vivo models of non-alcoholic fatty liver disease (NAFLD). Int. J. Mol. Sci. 14, 11963–11980 (2013).
pubmed: 23739675 pmcid: 3709766 doi: 10.3390/ijms140611963
Lunney, J. K. Advances in swine biomedical model genomics. Int. J. Biol. Sci. 3, 179–184 (2007).
pubmed: 17384736 pmcid: 1802015 doi: 10.7150/ijbs.3.179
Kogelman, L. J. A. & Kadarmideen, H. N. Applications of Systems Genetics and Biology for Obesity Using Pig Models. in Systems Biology in Animal Production and Health, Vol. 1 1, 25–43 (2016).
Lee, L. et al. Nutritional model of steatohepatitis and metabolic syndrome in the Ossabaw miniature swine. Hepatology 50, 56–67 (2009).
pubmed: 19434740 pmcid: 3254146 doi: 10.1002/hep.22904
Pedersen, R. et al. Characterisation of Gut Microbiota in Ossabaw and Göttingen Minipigs as Models of Obesity and Metabolic Syndrome. PLoS One 8, 1–10 (2013).
doi: 10.1371/annotation/51bc9350-b475-4b46-88b4-8bc1586d9d42
Bollen, P. J. A., Madsen, L. W., Meyer, O. & Ritskes-Hoitinga, J. Growth differences of male and female Gottingen minipigs during ad libitum feeding: a pilot study. Lab. Anim. 39, 80–93 (2005).
pubmed: 15703128 doi: 10.1258/0023677052886565 pmcid: 15703128
Ho, C. S. et al. Nomenclature for factors of the SLA system, update 2008. Tissue Antigens 73, 307–315 (2009).
pubmed: 19317739 doi: 10.1111/j.1399-0039.2009.01213.x pmcid: 19317739
Bovo, S. et al. Genome-wide association studies for 30 haematological and blood clinical-biochemical traits in Large White pigs reveal genomic regions affecting intermediate phenotypes. Sci. Rep. 9, 1–17 (2019).
doi: 10.1038/s41598-019-43297-1
Riordan, J. D. & Nadeau, J. H. Modeling progressive non-alcoholic fatty liver disease in the laboratory mouse. Mamm. Genome 25, 473–486 (2014).
pubmed: 24802098 pmcid: 4164843 doi: 10.1007/s00335-014-9521-3
Nassir, F. & Ibdah, J. A. Sirtuins and nonalcoholic fatty liver disease. World J. Gastroenterol. 22, 10084–10092 (2016).
pubmed: 28028356 pmcid: 5155167 doi: 10.3748/wjg.v22.i46.10084
Bindea, G. et al. ClueGO: A Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25, 1091–1093 (2009).
pubmed: 19237447 pmcid: 19237447 doi: 10.1093/bioinformatics/btp101
Subramanian, A. et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. 102, 15545–15550 (2005).
pubmed: 16199517 doi: 10.1073/pnas.0506580102 pmcid: 16199517
Liberzon, A. et al. The Molecular Signatures Database Hallmark Gene Set Collection. Cell Syst. 1, 417–425 (2015).
pubmed: 26771021 pmcid: 4707969 doi: 10.1016/j.cels.2015.12.004
Mach, N. et al. The Effects of Weaning Methods on Gut Microbiota Composition and Horse Physiology. Front Physiol. (2017).
Panasevich, M. R. et al. High-fat, high-fructose, high-cholesterol feeding causes severe NASH and cecal microbiota dysbiosis in juvenile Ossabaw swine. Am J. Physiol Endocrinol Metab 314 (2017).
pubmed: 28899857 doi: 10.1152/ajpendo.00015.2017 pmcid: 28899857
Lê Cao, K. A., Martin, P. G. P., Robert-Granié, C. & Besse, P. Sparse canonical methods for biological data integration: Application to a cross-platform study. BMC Bioinformatics 10, 1–17 (2009).
doi: 10.1186/1471-2105-10-34
González, I., Cao, K. A. L., Davis, M. J. & Déjean, S. Visualising associations between paired ‘omics’ data sets. BioData Min. 5, 1–23 (2012).
doi: 10.1186/1756-0381-5-19
Alfonso, L., Mourot, J., Insausti, K., Mendizabal, J. A. & Arana, A. Comparative description of growth, fat deposition, carcass and meat quality characteristics of Basque and Large White pigs. Anim. Res. 54, 33–42 (2005).
doi: 10.1051/animres:2005001
Rayis, D. A., Abdelmageed, R. E., Adam, I., Elmugabil, A. & Gasim, G. I. High level of hemoglobin, white blood cells and obesity among Sudanese women in early pregnancy: a cross-sectional study. Futur. Sci. OA 3, FSO182 (2017).
doi: 10.4155/fsoa-2016-0096
Guiraudou, M., Varlet-Marie, E., Raynaud De Mauverger, E. & Brun, J. F. Obesity-related increase in whole blood viscosity includes different profiles according to fat localization. Clin. Hemorheol. Microcirc. 55, 63–73 (2013).
pubmed: 23455838 doi: 10.3233/CH-131690
Giorgio, V. et al. Elevated Hemoglobin Level Is Associated with Advanced Fibrosis in Pediatric Nonalcoholic Fatty Liver Disease. J. Pediatr. Gastroenterol. Nutr. 65, 150–155 (2017).
pubmed: 28737569 doi: 10.1097/MPG.0000000000001614 pmcid: 28737569
Bai, C. H. et al. Relationship between hemoglobin levels and risk for suspected non-alcoholic fatty liver in taiwanese adults. Chin. J. Physiol. 57, 286–294 (2014).
pubmed: 25241989 doi: 10.4077/CJP.2014.BAD280 pmcid: 25241989
Vinci, P. et al. The Association between Hematological Parameters and Insulin Resistance Is Modified by Body Mass Index – Results from the North-East Italy MoMa Population Study. PLoS One 9, e101590 (2014).
pubmed: 25000394 pmcid: 4085001 doi: 10.1371/journal.pone.0101590
Das, S., Mukherjee, S., Vasudevan, D. & Balakrishnan, V. Comparison of haematological parameters in patients with non-alcoholic fatty liver disease and alcoholic liver disease. Singapore Med. J. 53, 175–181 (2011).
Milovanovic Alempijevic, T. et al. Diagnostic Accuracy of Platelet Count and Platelet Indices in Noninvasive Assessment of Fibrosis in Nonalcoholic Fatty Liver Disease Patients. Can. J. Gastroenterol. Hepatol. 2017, 1–5 (2017).
doi: 10.1155/2017/6070135
Ozhan, H. et al. Mean platelet volume in patients with non-alcoholic fatty liver disease. Platelets 21, 29–32 (2010).
pubmed: 19947902 doi: 10.3109/09537100903391023 pmcid: 19947902
Celikbilek, M. Letter: increased platelet activation in chronic liver disease - hit two targets with a single shot. Aliment. Pharmacol. Ther. 43, 1023–1023 (2016).
pubmed: 27040172 doi: 10.1111/apt.13582 pmcid: 27040172
Chauhan, A., Adams, D. H., Watson, S. P. & Lalor, P. F. Platelets: No longer bystanders in liver disease. Hepatology 64, 1774–1784 (2016).
pubmed: 26934463 pmcid: 5082495 doi: 10.1002/hep.28526
Bekler, A. et al. Increased Platelet Distribution Width Is Associated with Severity of Coronary Artery Disease in Patients with Acute Coronary Syndrome. Angiology 66, 638–643 (2015).
pubmed: 25112777 doi: 10.1177/0003319714545779 pmcid: 25112777
Antoniades, C. G., Wendon, J. & Vergani, D. Paralysed monocytes in acute on chronic liver disease. J. Hepatol. 42, 163–165 (2005).
pubmed: 15664238 doi: 10.1016/j.jhep.2004.12.005 pmcid: 15664238
Harmon, R. C., Tiniakos, D. G. & Argo, C. K. Inflammation in nonalcoholic steatohepatitis. Expert Rev. Gastroenterol. Hepatol. 5, 189–200 (2011).
pubmed: 21476914 doi: 10.1586/egh.11.21 pmcid: 21476914
Mitsumoto, K. et al. Time-course microarrays reveal early activation of the immune transcriptome in a choline-deficient mouse model of liver injury. Life Sci. 184, 103–111 (2017).
pubmed: 28711489 doi: 10.1016/j.lfs.2017.07.009 pmcid: 28711489
Kirpich, I. A. et al. Integrated hepatic transcriptome and proteome analysis of mice with high-fat diet-induced nonalcoholic fatty liver disease. J. Nutr. Biochem. 22, 38–45 (2011).
pubmed: 20303728 doi: 10.1016/j.jnutbio.2009.11.009 pmcid: 20303728
Qi, S., Wang, C., Li, C., Wang, P. & Liu, M. Candidate genes investigation for severe nonalcoholic fatty liver disease based on bioinformatics analysis. Medicine (Baltimore). 96, e7743 (2017).
pubmed: 28796060 pmcid: 5556226 doi: 10.1097/MD.0000000000007743
Hart, K. M. et al. Type 2 immunity is protective in metabolic disease but exacerbates NAFLD collaboratively with TGF-b. Sci. Transl. Med. 9 (2017).
pubmed: 28659437 doi: 10.1126/scitranslmed.aal3694 pmcid: 28659437
Chung, G. E. et al. Associations between White Blood Cell Count and the Development of Incidental Nonalcoholic Fatty Liver Disease. Gastroenterol. Res. Pract. 2016, 1–6 (2016).
doi: 10.1155/2016/7653689
Ley, R., Turnbaugh, P., Klein, S. & Gordon, J. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–3 (2006).
doi: 10.1038/4441022a
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting Linear Mixed-Effects Models using lme4. J. Stat. Softw. 67 (2015).
Lê, S., Josse, J. & Husson, F. FactoMineR: An R Package for Multivariate Analysis. J. Stat. Softw. 25, 1–18 (2008).
doi: 10.18637/jss.v025.i01
Jacquier, V. et al. Genome-wide immunity studies in the rabbit: Transcriptome variations in peripheral blood mononuclear cells after in vitro stimulation by LPS or PMA-Ionomycin. BMC Genomics 16 (2015).
pubmed: 25613284 pmcid: 4326531 doi: 10.1186/s12864-015-1218-9
Smyth, G. K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3 (2004).
doi: 10.2202/1544-6115.1027
Kauffmann, A., Gentleman, R. & Huber, W. arrayQualityMetrics - A bioconductor package for quality assessment of microarray data. Bioinformatics 25, 415–416 (2009).
pubmed: 19106121 doi: 10.1093/bioinformatics/btn647 pmcid: 19106121
Younossi, Z. M. et al. Hepatic gene expression in patients with obesity-related non-alcoholic steatohepatitis. Liver Int. 25, 760–771 (2005).
pubmed: 15998427 doi: 10.1111/j.1478-3231.2005.01117.x pmcid: 15998427
Arendt, B. M. et al. Altered hepatic gene expression in nonalcoholic fatty liver disease is associated with lower hepatic n-3 and n-6 polyunsaturated fatty acids. Hepatology 61, 1565–78 (2015).
pubmed: 25581263 doi: 10.1002/hep.27695 pmcid: 25581263
Almanza, D. RNA Seq Analysis of Non-Alcoholic Fatty Liver Disease (NAFLD) Induced by Metabolic Syndrome in a Mouse Model. Honor. Coll. Thesis Univ. Massachussets Bost (2016).
Wang, R., Wang, X. & Zhuang, L. Gene expression profiling reveals key genes and pathways related to the development of non-alcoholic fatty liver disease. Ann. Hepatol. 15, 190–199 (2016).
pubmed: 26845596 doi: 10.1016/S0168-8278(16)00132-X pmcid: 26845596
Hui, S. T. et al. The genetic architecture of NAFLD among inbred strains of mice. Elife 4, 1–28 (2015).
doi: 10.7554/eLife.05607
Moylan, C. A. et al. Hepatic gene expression profiles differentiate presymptomatic patients with mild versus severe nonalcoholic fatty liver disease. Hepatology 59, 471–482 (2014).
pubmed: 23913408 doi: 10.1002/hep.26661 pmcid: 23913408
Wruck, W. et al. Multi-omic profiles of human non-alcoholic fatty liver disease tissue highlight heterogenic phenotypes. Sci. Data 2, 1–10 (2015).
doi: 10.1038/sdata.2015.68
Gawrieh, S. et al. Hepatic gene networks in morbidly obese patients with nonalcoholic fatty liver disease. Obes. Surg. 20, 1698–1709 (2010).
pubmed: 20473581 doi: 10.1007/s11695-010-0171-6 pmcid: 20473581
Carazo, A. et al. Hepatic expression of adiponectin receptors increases with non-alcoholic fatty liver disease progression in morbid obesity in correlation with glutathione peroxidase 1. Obes. Surg. 21, 492–500 (2011).
pubmed: 21240660 doi: 10.1007/s11695-010-0353-2 pmcid: 21240660
Teufel, A. et al. Comparison of Gene Expression Patterns Between Mouse Models of Nonalcoholic Fatty Liver Disease and Liver Tissues From Patients. Gastroenterology 151, 513–525.e0 (2016).
pubmed: 27318147 doi: 10.1053/j.gastro.2016.05.051 pmcid: 27318147
Lepage, P. et al. Biodiversity of the mucosa-associated microbiota is stable along the distal digestive tract in healthy individuals and patients with IBD. Inflamm. Bowel Dis. 11, 473–480 (2005).
pubmed: 15867587 doi: 10.1097/01.MIB.0000159662.62651.06 pmcid: 15867587
Mach, N. et al. Early-life establishment of the swine gut microbiome and impact on host phenotypes. Environ. Microbiol. Rep. 7, 554–569 (2015).
pubmed: 25727666 doi: 10.1111/1758-2229.12285 pmcid: 25727666
Caporaso, J. G. et al. correspondence QIIME allows analysis of high- throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing. Nat. Publ. Gr. 7, 335–336 (2010).
McMurdie, P. J. & Holmes, S. Phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS One 8 (2013).
Philip, D. Computer program review VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).
doi: 10.1111/j.1654-1103.2003.tb02228.x
Paulson, J. N., Colin Stine, O., Bravo, H. C. & Pop, M. Differential abundance analysis for microbial marker-gene surveys. Nat. Methods 10, 1200–1202 (2013).
pubmed: 24076764 pmcid: 4010126 doi: 10.1038/nmeth.2658
Escofier, B. & Pagès, J. Multiple factor analysis (AFMULT package). Comput. Stat. Data Anal. 18, 121–140 (1994).
doi: 10.1016/0167-9473(94)90135-X
Rohart, F., Gautier, B., Singh, A. & Lê Cao, K.-A. mixOmics: An R package for ‘omics feature selection and multiple data integration. PLOS Comput. Biol. 13, e1005752 (2017).
pubmed: 29099853 pmcid: 5687754 doi: 10.1371/journal.pcbi.1005752

Auteurs

Marco Moroldo (M)

Université Paris Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France. marco.moroldo@inra.fr.

Peris Mumbi Munyaka (PM)

Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Canada.

Jérôme Lecardonnel (J)

Université Paris Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France.

Gaëtan Lemonnier (G)

Université Paris Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France.

Eric Venturi (E)

INRAE, PAO, 37380, Nouzilly, France.

Claire Chevaleyre (C)

Université de Tours, INRAE, ISP, 37380, Nouzilly, France.

Isabelle P Oswald (IP)

Université de Toulouse, INRAE, ENVT, INP-Purpan, UPS, Toxalim, 31027, Toulouse, France.

Jordi Estellé (J)

Université Paris Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France.

Claire Rogel-Gaillard (C)

Université Paris Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France.

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