Enhanced offspring predisposition to steatohepatitis with maternal high-fat diet is associated with epigenetic and microbiome alterations

PLoS ONE

Volumn 12, Issue 4, 2017, Pages

  Wankhade, Umesh D ^a,b   Zhong, Ying ^b   Kang, Ping ^b   Alfaro, Maria ^c   Chintapalli, Sree V ^a,b   Thakali, Keshari M ^a,b   Shankar, Kartik ^a,b  

^a U S DEPARTMENT OF AGRICULTURE   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c ARKANSAS CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; DNA; EPHRIN RECEPTOR B2; FIBROBLAST GROWTH FACTOR 21; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; RNA; VON WILLEBRAND FACTOR; CHOLINE; METHIONINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIUM; CELL ADHESION; CELL COMMUNICATION; CONTROLLED STUDY; DAM (ANIMAL); DISEASE PREDISPOSITION; DNA METHYLATION; EPHB2 GENE; EPIGENETICS; FEMALE; FGF21 GENE; GENE; GENE EXPRESSION; INTESTINE FLORA; LIPID DIET; LIVER WEIGHT; MALE; MATERNAL OBESITY; METABOLISM; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PATHOGENESIS; PPARGC1 BETA GENE; PROGENY; RNA SEQUENCE; VWF GENE; WEIGHT GAIN; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; COMPLICATION; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETICS; LIVER; MATERNAL NUTRITION; MICROBIOLOGY; NON-ALCOHOLIC FATTY LIVER DISEASE; OVERNUTRITION; PREGNANCY; PRENATAL EXPOSURE; VITAMIN DEFICIENCY;

ANIMALS; CHOLINE; CHOLINE DEFICIENCY; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION PROFILING; LIVER; MALE; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; METHIONINE; MICE; MICE, INBRED C57BL; NON-ALCOHOLIC FATTY LIVER DISEASE; OVERNUTRITION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 85017552415     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0175675     Document Type: Article

References (47)

1. Flegal KM, Carroll MD, Ogden CL, Curtin LR (2010) Prevalence and trends in obesity among US adults, 1999-2008. JAMA 303: 235-241. https://doi.org/10.1001/jama.2009.2014 PMID: 20071471
2. Lawlor DA, Smith GD, O'Callaghan M, Alati R, Mamun AA, et al. (2007) Epidemiologic evidence for the fetal overnutrition hypothesis: findings from the mater-university study of pregnancy and its outcomes. Am J Epidemiol 165: 418-424. https://doi.org/10.1093/aje/kwk030 PMID: 17158475
3. Shankar K, Harrell A, Liu X, Gilchrist JM, Ronis MJ, et al. (2008) Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol 294: R528-538. https://doi.org/10.1152/ajpregu.00316.2007 PMID: 18032473
4. Samuelsson AM, Matthews PA, Argenton M, Christie MR, McConnell JM, et al. (2008) Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension 51: 383-392. https://doi.org/10.1161/HYPERTENSIONAHA.107.101477 PMID: 18086952
5. Bohinc BN, Diehl AM (2012) Mechanisms of disease progression in NASH: new paradigms. Clin Liver Dis 16: 549-565. https://doi.org/10.1016/j.cld.2012.05.002 PMID: 22824480
6. Shankar K, Kang P, Harrell A, Zhong Y, Marecki JC, et al. (2010) Maternal overweight programs insulin and adiponectin signaling in the offspring. Endocrinology 151: 2577-2589. https://doi.org/10.1210/en.2010-0017 PMID: 20371699
7. Borengasser SJ, Faske J, Kang P, Blackburn ML, Badger TM, et al. (2014) In utero exposure to prepregnancy maternal obesity and postweaning high-fat diet impair regulators of mitochondrial dynamics in rat placenta and offspring. Physiol Genomics 46: 841-850. https://doi.org/10.1152/physiolgenomics.00059.2014 PMID: 25336449
8. Borengasser SJ, Zhong Y, Kang P, Lindsey F, Ronis MJ, et al. (2013) Maternal obesity enhances white adipose tissue differentiation and alters genome-scale DNA methylation in male rat offspring. Endocrinology 154: 4113-4125. https://doi.org/10.1210/en.2012-2255 PMID: 23959936
9. Oben JA, Mouralidarane A, Samuelsson AM, Matthews PJ, Morgan ML, et al. (2010) Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice. J Hepatol 52: 913-920. https://doi.org/10.1016/j.jhep.2009.12.042 PMID: 20413174
10. Bruce KD, Cagampang FR, Argenton M, Zhang J, Ethirajan PL, et al. (2009) Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology 50: 1796-1808. https://doi.org/10.1002/hep.23205 PMID: 19816994
11. McCurdy CE, Bishop JM, Williams SM, Grayson BE, Smith MS, et al. (2009) Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest 119: 323-335. https://doi.org/10.1172/JCI32661 PMID: 19147984
12. Brumbaugh DE, Friedman JE (2014) Developmental origins of nonalcoholic fatty liver disease. Pediatr Res 75: 140-147. https://doi.org/10.1038/pr.2013.193 PMID: 24192698
13. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, et al. (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41: 1313-1321. https://doi.org/10.1002/hep.20701 PMID: 15915461
14. Shankar K, Zhong Y, Kang P, Blackburn ML, Soares MJ, et al. (2012) RNA-seq analysis of the functional compartments within the rat placentation site. Endocrinology 153: 1999-2011. https://doi.org/10.1210/en.2011-1833 PMID: 22355068
15. Shankar K, Kang P, Zhong Y, Borengasser SJ, Wingfield C, et al. (2015) Transcriptomic and epigenomic landscapes during cell fusion in BeWo trophoblast cells. Placenta 36: 1342-1351. https://doi.org/10.1016/j.placenta.2015.10.010 PMID: 26515927
16. Delidaki M, Gu M, Hein A, Vatish M, Grammatopoulos DK (2011) Interplay of cAMP and MAPK pathways in hCG secretion and fusogenic gene expression in a trophoblast cell line. Mol Cell Endocrinol 332: 213-220. https://doi.org/10.1016/j.mce.2010.10.013 PMID: 21035520
17. Wu H, Xu T, Feng H, Chen L, Li B, et al. (2015) Detection of differentially methylated regions from whole-genome bisulfite sequencing data without replicates. Nucleic Acids Res 43: e141. https://doi.org/10.1093/nar/gkv715 PMID: 26184873
18. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79: 5112-5120. https://doi.org/10.1128/AEM.01043-13 PMID: 23793624
19. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336. https://doi.org/10.1038/nmeth.f.303 PMID: 20383131
20. Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30: 3123-3124. https://doi.org/10.1093/bioinformatics/btu494 PMID: 25061070
21. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, et al. (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31: 814-821. https://doi.org/10.1038/nbt.2676 PMID: 23975157
22. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, et al. (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12: R60. https://doi.org/10.1186/gb-2011-12-6-r60 PMID: 21702898
23. Borengasser SJ, Lau F, Kang P, Blackburn ML, Ronis MJ, et al. (2011) Maternal obesity during gestation impairs fatty acid oxidation and mitochondrial SIRT3 expression in rat offspring at weaning. PLoS One 6: e24068. https://doi.org/10.1371/journal.pone.0024068 PMID: 21901160
24. Bruce KD, Byrne CD (2009) The metabolic syndrome: common origins of a multifactorial disorder. Postgrad Med J 85: 614-621. https://doi.org/10.1136/pgmj.2008.078014 PMID: 19892897
25. Zhu MJ, Han B, Tong J, Ma C, Kimzey JM, et al. (2008) AMP-activated protein kinase signalling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. J Physiol 586: 2651-2664. https://doi.org/10.1113/jphysiol.2007.149633 PMID: 18372306
26. Ainge H, Thompson C, Ozanne SE, Rooney KB (2011) A systematic review on animal models of maternal high fat feeding and offspring glycaemic control. Int J Obes (Lond) 35: 325-335.
27. Bayol SA, Simbi BH, Stickland NC (2005) A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol 567: 951-961. https://doi.org/10.1113/jphysiol.2005.088989 PMID: 16020464
28. Khan I, Dekou V, Hanson M, Poston L, Taylor P (2004) Predictive adaptive responses to maternal highfat diet prevent endothelial dysfunction but not hypertension in adult rat offspring. Circulation 110: 1097-1102. https://doi.org/10.1161/01.CIR.0000139843.05436.A0 PMID: 15326063
29. Levin BE, Govek E (1998) Gestational obesity accentuates obesity in obesity-prone progeny. Am J Physiol 275: R1374-1379. PMID: 9756571
30. Mouralidarane A, Soeda J, Sugden D, Bocianowska A, Carter R, et al. (2015) Maternal obesity programs offspring non-alcoholic fatty liver disease through disruption of 24-h rhythms in mice. Int J Obes (Lond) 39: 1339-1348.
31. Mouralidarane A, Soeda J, Visconti-Pugmire C, Samuelsson AM, Pombo J, et al. (2013) Maternal obesity programs offspring nonalcoholic fatty liver disease by innate immune dysfunction in mice. Hepatology 58: 128-138. https://doi.org/10.1002/hep.26248 PMID: 23315950
32. Borengasser SJ, Kang P, Faske J, Gomez-Acevedo H, Blackburn ML, et al. (2014) High fat diet and in utero exposure to maternal obesity disrupts circadian rhythm and leads to metabolic programming of liver in rat offspring. PLoS One 9: e84209. https://doi.org/10.1371/journal.pone.0084209 PMID: 24416203
33. Kulinski A, Vance DE, Vance JE (2004) A choline-deficient diet in mice inhibits neither the CDP-choline pathway for phosphatidylcholine synthesis in hepatocytes nor apolipoprotein B secretion. J Biol Chem 279: 23916-23924. https://doi.org/10.1074/jbc.M312676200 PMID: 15024002
34. Oz HS, Chen TS, Neuman M (2008) Methionine deficiency and hepatic injury in a dietary steatohepatitis model. Dig Dis Sci 53: 767-776. https://doi.org/10.1007/s10620-007-9900-7 PMID: 17710550
35. Itagaki H, Shimizu K, Morikawa S, Ogawa K, Ezaki T (2013) Morphological and functional characterization of non-alcoholic fatty liver disease induced by a methionine-choline-deficient diet in C57BL/6 mice. Int J Clin Exp Pathol 6: 2683-2696. PMID: 24294355
36. Ma J, Prince AL, Bader D, Hu M, Ganu R, et al. (2014) High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat Commun 5: 3889. https://doi.org/10.1038/ncomms4889 PMID: 24846660
37. Niculescu MD, Yamamuro Y, Zeisel SH (2004) Choline availability modulates human neuroblastoma cell proliferation and alters the methylation of the promoter region of the cyclin-dependent kinase inhibitor 3 gene. J Neurochem 89: 1252-1259. https://doi.org/10.1111/j.1471-4159.2004.02414.x PMID: 15147518
38. da Costa KA, Niculescu MD, Craciunescu CN, Fischer LM, Zeisel SH (2006) Choline deficiency increases lymphocyte apoptosis and DNA damage in humans. Am J Clin Nutr 84: 88-94. PMID: 16825685
39. Rushmore TH, Farber E, Ghoshal AK, Parodi S, Pala M, et al. (1986) A choline-devoid diet, carcinogenic in the rat, induces DNA damage and repair. Carcinogenesis 7: 1677-1680. PMID: 3757170
40. Mimche PN, Brady LM, Bray CF, Lee CM, Thapa M, et al. (2015) The receptor tyrosine kinase EphB2 promotes hepatic fibrosis in mice. Hepatology 62: 900-914. https://doi.org/10.1002/hep.27792 PMID: 25784101
41. Mimche PN, Brady LM, Bray CF, Thapa M, King TP, et al. (2016) Deficiency in the receptor tyrosine kinase EphB2 attenuates experimentally-induced liver fibrosis in mice. The Journal of Immunology 194.
42. Lisman T, Bongers TN, Adelmeijer J, Janssen HL, de Maat MP, et al. (2006) Elevated levels of von Willebrand Factor in cirrhosis support platelet adhesion despite reduced functional capacity. Hepatology 44: 53-61. https://doi.org/10.1002/hep.21231 PMID: 16799972
43. Yilmaz Y, Eren F, Yonal O, Kurt R, Aktas B, et al. (2010) Increased serum FGF21 levels in patients with nonalcoholic fatty liver disease. Eur J Clin Invest 40: 887-892. https://doi.org/10.1111/j.1365-2362.2010.02338.x PMID: 20624171
44. Compare D, Coccoli P, Rocco A, Nardone OM, De Maria S, et al. (2012) Gut - liver axis: the impact of gut microbiota on non alcoholic fatty liver disease. Nutr Metab Cardiovasc Dis 22: 471-476. https://doi.org/10.1016/j.numecd.2012.02.007 PMID: 22546554
45. Koleva PT, Bridgman SL, Kozyrskyj AL (2015) The infant gut microbiome: evidence for obesity risk and dietary intervention. Nutrients 7: 2237-2260. https://doi.org/10.3390/nu7042237 PMID: 25835047
46. Zhu L, Baker SS, Gill C, Liu W, Alkhouri R, et al. (2013) Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH. Hepatology 57: 601-609. https://doi.org/10.1002/hep.26093 PMID: 23055155
47. Lemas DJ, Young BE, Baker PR 2nd, Tomczik AC, Soderborg TK, et al. (2016) Alterations in human milk leptin and insulin are associated with early changes in the infant intestinal microbiome. Am J Clin Nutr 103: 1291-1300. https://doi.org/10.3945/ajcn.115.126375 PMID: 27140533