Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-22T15:37:23.479Z Has data issue: false hasContentIssue false

Maternal high-fat diet consumption programs male offspring to mitigate complications in liver regeneration

Published online by Cambridge University Press:  03 December 2021

T. Fante
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
L. A. P. Simino
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Marina Figueiredo Fontana
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Andressa Reginato
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Thomaz Guadagnini Ramalheira
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Hosana Gomes Rodrigues
Affiliation:
Laboratory of Nutrients and Tissue Repair, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Patricia Cristina Lisboa
Affiliation:
Laboratory of Endocrine Physiology, Department of Physiological Sciences, Roberto Alcantara Gomes Biology Institute, State University of Rio de Janeiro, Rio de Janeiro, Brazil
Egberto Gaspar de Moura
Affiliation:
Laboratory of Endocrine Physiology, Department of Physiological Sciences, Roberto Alcantara Gomes Biology Institute, State University of Rio de Janeiro, Rio de Janeiro, Brazil
Leticia Martins Ignácio-Souza
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Marciane Milanski
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Marcio Alberto Torsoni
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Adriana Souza Torsoni*
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
*
Address for correspondence: Adriana Souza Torsoni, 1300, Pedro Zaccaria St. Laboratory of Metabolic Disorders, FCA – UNICAMP, Limeira, São Paulo13484-350, Brazil. Email: [email protected]

Abstract

In the last decades, obesity and nonalcoholic fatty liver disease (NAFLD) have become increasingly prevalent in wide world. Fatty liver can be detrimental to liver regeneration (LR) and offspring of obese dams (HFD-O) are susceptible to NAFLD development. Here we evaluated LR capacity in HFD-O after partial hepatectomy (PHx). HFD-O re-exposed or not to HFD in later life were evaluated for metabolic parameters, inflammation, proliferation, tissue repair markers and survival rate after PHx. Increasing adiposity and fatty liver were observed in HFD-O. Despite lower IL-6 levels, Ki67 labeling, cells in S phase and Ciclin D1/PCNA protein content, a lower impact on survival rate was found after PHx, even when re-exposed to HFD. However, no difference was observed between offspring of control dams (SC-O) and HFD-O after surgery. Although LR impairment is dependent of steatosis development, offspring of obese dams are programmed to be protected from the damage promoted by HFD.

Type
Original Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Marchesini, G, Brizi, M, Blanchi, G, et al. Nonalcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes. 2001; 50(8), 18441850. DOI 10.2337/diabetes.50.8.1844.CrossRefGoogle ScholarPubMed
Heron, M. Deaths: leading causes for 2015. Natl Vital Stat Reports. 2017; 66(5), 1–76.Google ScholarPubMed
Lindenmeyer, CC, McCullough, AJ. The natural history of nonalcoholic fatty liver disease—An evolving view. Clin Liver Dis. 2018; 22(1), 1121. DOI 10.1016/j.cld.2017.08.003.CrossRefGoogle ScholarPubMed
Rinella, ME. Nonalcoholic fatty liver disease a systematic review. JAMA. 2015; 313(22), 22632273. DOI 10.1001/jama.2015.5370.CrossRefGoogle ScholarPubMed
Rodrigues, AA, Andrade, RSSB, Vasconcelos, DFP. Relationship between experimental diet in rats and nonalcoholic hepatic disease: review of literature. Int J Hepatol. 2018; 2018(7), 18. DOI 10.1155/2018/9023027.CrossRefGoogle ScholarPubMed
Kitamori, K, Naito, H, Tamada, H, et al. Development of novel rat model for high-fat and high-cholesterol diet-induced steatohepatitis and severe fibrosis progression in SHRSP5/Dmcr. Environ Health Prev Med. 2012; 17(3), 173182. DOI 10.1007/s12199-011-0235-9.CrossRefGoogle ScholarPubMed
Zou, Y, Li, J, Lu, C, et al. High-fat emulsion-induced rat model of nonalcoholic steatohepatitis. Life Sci. 2006; 79(11), 11001107. DOI 10.1016/j.lfs.2006.03.021.CrossRefGoogle ScholarPubMed
Liu, Y, Meyer, C, Xu, C, et al. Animal models of chronic liver diseases. Am J Physiol Gastrointest Liver Physiol. 2013; 304(5), G449G468. DOI 10.1152/ajpgi.00199.2012.CrossRefGoogle ScholarPubMed
Corbin, KD, Zeisel, SH. Choline metabolism provides novel insights into nonalcoholic fatty liver disease and its progression. Curr Opin Gastroenterol. 2012; 28(2), 159165. DOI 10.1097/MOG.0b013e32834e7b4b.CrossRefGoogle ScholarPubMed
Anstee, QM, Goldin, RD. Mouse models in non-alcoholic fatty liver disease and steatohepatitis research. Int J Exp Pathol. 2006; 87(1), 116. DOI 10.1111/j.0959-9673.2006.00465.x.CrossRefGoogle ScholarPubMed
Kirsch, R, Clarkson, V, Shephard, EG, et al. Rodent nutritional model of non-alcoholic steatohepatitis: species, strain and sex difference studies. J Gastroenterol Hepatol. 2003; 18(11), 12721282. DOI 10.1046/j.1440-1746.2003.03198.x.CrossRefGoogle ScholarPubMed
Lieber, CS, Leo, MA, Mak, KM, et al. Model of nonalcoholic steatohepatitis. Am J Clin Nutr. 2004; 79(3), 502509. DOI 10.1093/ajcn/79.3.502.CrossRefGoogle ScholarPubMed
Kučera, O, Garnol, T, Lotková, H, et al. The effect of rat strain, diet composition and feeding period on the development of a nutritional model of non-alcoholic fatty liver disease in rats. Physiol Res. 2011; 60(2), 317328. DOI 10.33549/physiolres.932022.CrossRefGoogle ScholarPubMed
Pruis, MGM, Lendvai, Á., Bloks, VW, et al. Maternal western diet primes non-alcoholic fatty liver disease in adult mouse offspring. Acta Physiol. 2014; 210(1), 215227. DOI 10.1111/apha.12197.CrossRefGoogle ScholarPubMed
Cao, B, Liu, C, Zhang, Q, Dong, Y. Maternal high-fat diet leads to non-alcoholic fatty liver disease through upregulating hepatic SCD1 expression in neonate rats. Front Nutr. 2020; 7, 547. DOI 10.3389/fnut.2020.581723.CrossRefGoogle ScholarPubMed
McCurdy, CE, Bishop, JM, Williams, SM, et al. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest. 2009; 119(2), 323335. DOI 10.1172/JCI32661.Google ScholarPubMed
Ashino, NG, Saito, KN, Souza, FD, et al. Maternal high-fat feeding through pregnancy and lactation predisposes mouse offspring to molecular insulin resistance and fatty liver. J Nutr Biochem. 2012; 23(4), 341348. DOI 10.1016/j.jnutbio.2010.12.011.CrossRefGoogle ScholarPubMed
Benatti, RO, Melo, AM, Borges, FO, et al. Maternal high-fat diet consumption modulates hepatic lipid metabolism and microRNA-122 (miR-122) and microRNA-370 (miR-370) expression in offspring. Br J Nutr. 2014; 111(12), 21122122. DOI 10.1017/S0007114514000579.CrossRefGoogle ScholarPubMed
de Paula Simino, LA, de Fante, T, Figueiredo Fontana, M, et al. Lipid overload during gestation and lactation can independently alter lipid homeostasis in offspring and promote metabolic impairment after new challenge to high-fat diet. Nutr Metab (Lond). 2017; 14(1), 16. DOI 10.1186/s12986-017-0168-4.CrossRefGoogle ScholarPubMed
de, Fante T, Simino, LA, Reginato, A, et al. Diet-Induced maternal obesity alters insulin signalling in male mice offspring rechallenged with a high-fat diet in adulthood. PLoS One. 2016; 11(8), e0160184. DOI 10.1371/journal.pone.0160184.Google Scholar
Moore, JB. Symposium 1: overnutrition: consequences and solutions Non-alcoholic fatty liver disease: the hepatic consequence of obesity and the metabolic syndrome. Proc Nutr Soc. 2010; 69(2), 211220. DOI 10.1017/S0029665110000030.CrossRefGoogle Scholar
Mao, SA, Glorioso, JM, Nyberg, SL. Liver regeneration. Transl Res. 2014; 163(4), 352362. DOI 10.1016/j.trsl.2014.01.005.CrossRefGoogle ScholarPubMed
Li, W, Liang, X, Leu, JI, Kovalovich, K, Ciliberto, G, Taub, R. Global changes in interleukin-6-dependent gene expression patterns in mouse livers after partial hepatectomy. Hepatology. 2001; 33(6), 13771386. DOI 10.1053/jhep.2001.24431.CrossRefGoogle ScholarPubMed
Veteläinen, R, Van Vliet, AK, Van Gulik, TM. Severe steatosis increases hepatocellular injury and impairs liver regeneration in a rat model of partial hepatectomy. Ann Surg. 2007; 245(1), 4450. DOI 10.1097/01.sla.0000225253.84501.0e.CrossRefGoogle Scholar
Mitchell, C, Willenbring, H. A reproducible and well-tolerated method for 2/3 partial hepatectomy in mice. Nat Protoc. 2008; 3(7), 11671170. DOI 10.1038/nprot.2008.80.CrossRefGoogle ScholarPubMed
Mehlem, A, Hagberg, CE, Muhl, L, Eriksson, U, Falkevall, A. Imaging of neutral lipids by oil red O for analyzing the metabolic status in health and disease. Nat Protoc. 2013; 8(6), 11491154. DOI 10.1038/nprot.2013.055.CrossRefGoogle ScholarPubMed
Severgnini, M, Sherman, J, Sehgal, A, et al. A rapid two-step method for isolation of functional primary mouse hepatocytes: cell characterization and asialoglycoprotein receptor based assay development. Cytotechnology. 2012; 64(2), 187195. DOI 10.1007/s10616-011-9407-0.CrossRefGoogle ScholarPubMed
Russel, W, Burch, R. The principles of humane experimental technique. Med J Aust. 1960; 1(13), 500500. DOI 10.5694/j.1326-5377.1960.tb73127.x.Google Scholar
Yang, SQ, Mandal, AK, Huang, J, Diehl, AM. Disrupted signaling and inhibited regeneration in obese mice with fatty livers: implications for nonalcoholic fatty liver disease pathophysiology. Hepatology. 2001; 34(4 I), 694706. DOI 10.1053/jhep.2001.28054.CrossRefGoogle ScholarPubMed
Rudnick, DA, Davidson, NO. Functional relationships between lipid metabolism and liver regeneration. Int J Hepatol. 2012; 2012(1), 18. DOI 10.1155/2012/549241.CrossRefGoogle ScholarPubMed
Scholzen, T, Gerdes, J. The Ki-67 protein: from the known and the unknown. J Cell Physiol. 2000; 182(3), 311322. DOI 10.1002/(SICI)1097-4652(200003)182:.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
Zheng, B, Wang, G, Gao, W, Wu, Q, Zhu, W, Weng, G. SOX7 is involved in polyphyllin D-induced G0/G1 cell cycle arrest through down-regulation of cyclin D1. Acta Pharm. 2020; 70(2), 191200. DOI 10.2478/acph-2020-0017.CrossRefGoogle ScholarPubMed
Abshagen, K, Degenhardt, B, Liebig, M, et al. Liver-specific Repin1 deficiency impairs transient hepatic steatosis in liver regeneration. Sci Rep. 2018; 8(1), 115. DOI 10.1038/s41598-018-35325-3.CrossRefGoogle ScholarPubMed
Amini, N, Margonis, GA, Buttner, S, et al. Liver regeneration after major liver hepatectomy: impact of body mass index. Surgery. 2016; 160, 8191. DOI 10.1016/j.surg.2016.02.014.CrossRefGoogle ScholarPubMed
Matot, I, Nachmansson, N, Duev, O, et al. Impaired liver regeneration after hepatectomy and bleeding is associated with a shift from hepatocyte proliferation to hypertrophy. FASEB J. 2017; 31(12), 52835295. DOI 10.1096/fj.201700153R.CrossRefGoogle ScholarPubMed
Mebratu, Y, Tesfaigzi, Y. How ERK1/2 activation controls cell proliferation and cell death is subcellular localization the answer? Cell Cycle. 2009; 8(8), 11681175. DOI 10.4161/cc.8.8.8147.CrossRefGoogle Scholar
Wang, XF, Yang, ZG, Xue, B, Shi, H. Activation of the cholinergic antiinflammatory pathway ameliorates obesity-induced inflammation and insulin resistance. Endocrinology. 2011; 152(3), 836846. DOI 10.1210/en.2010-0855.CrossRefGoogle ScholarPubMed
Naseem, S, Hussain, T, Manzoor, S. Interleukin-6: a promising cytokine to support liver regeneration and adaptive immunity in liver pathologies. Cytokine Growth Factor Rev. 2018; 39(15), 3645. DOI 10.1016/j.cytogfr.2018.01.002.CrossRefGoogle ScholarPubMed
Sydor, S, Gu, Y, Schlattjan, M, et al. Steatosis does not impair liver regeneration after partial hepatectomy. Lab Invest. 2013; 93(1), 2030. DOI 10.1038/labinvest.2012.142.CrossRefGoogle Scholar
Tao, Y, Wang, M, Chen, E, Tang, H. Liver regeneration: analysis of the main relevant signaling molecules. Mediators Inflamm. 2017; 2017(5309), 19. DOI 10.1155/2017/4256352.Google ScholarPubMed
Gupta, P, Venugopal, SK. Augmenter of liver regeneration: a key protein in liver regeneration and pathophysiology. Hepatol Res. 2018; 48(8), 587596. DOI 10.1111/hepr.13077.CrossRefGoogle ScholarPubMed
Wedemeyer, H, Thursz, M. The role of different EASL-papers: clinical practice guidelines vs. position papers vs. conference summaries. J Hepatol. 2010; 53(2), 372384. DOI 10.1016/j.jhep.2010.04.008.CrossRefGoogle Scholar
Berardis, S, Sokal, E. Pediatric non-alcoholic fatty liver disease: an increasing public health issue. Eur J Pediatr. 2014; 173(2), 131139. DOI 10.1007/s00431-013-2157-6.CrossRefGoogle Scholar
Alisi, A, Cianfarani, S, Manco, M, Agostoni, C, Nobili, V. Non-alcoholic fatty liver disease and metabolic syndrome in adolescents: pathogenetic role of genetic background and intrauterine environment. Ann Med. 2012; 44(1), 2940. DOI 10.3109/07853890.2010.547869.CrossRefGoogle ScholarPubMed
Ayonrinde, OT, Olynyk, JK, Marsh, JA, et al. Childhood adiposity trajectories and risk of nonalcoholic fatty liver disease in adolescents. J Gastroenterol Hepatol. 2015; 30(1), 163171. DOI 10.1111/jgh.12666.CrossRefGoogle ScholarPubMed
Miller, CN, Morton, HP, Cooney, PT, et al. Acute exposure to high-fat diets increases hepatic expression of genes related to cell repair and remodeling in female rats. Nutr Res. 2014; 34(1), 8593. DOI 10.1016/j.nutres.2013.10.010.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Fante et al. supplementary material

Fante et al. supplementary material

Download Fante et al. supplementary material(Image)
Image 220.4 KB