Abstract
Intrauterine growth restriction (IUGR) remains a major problem in swine production since the associated low birth weight leads to high rates of pre-weaning morbidity and mortality, and permanent retardation of growth and development. The underlying regulatory mechanisms from the aspects of epigenetic modification has received widespread attention. Studies explore the changes in genome wide methylation in small intestine (SI), liver and longissimus dorsi muscle (LDM) between IUGR and normal birth weight (NBW) newborn piglets using a methylated DNA immunoprecipitation-sequencing (MeDIP-Seq) approach. The data demonstrated that methylated peaks were prominently distributed in distal intergenic regions and the quantities of peaks in IUGR piglets were more than that of NBW piglets. IUGR piglets had relatively high methylated level in promoters, introns and coding exons in all the three tissues. Through KEGG pathway analysis of differentially methylated genes found that 33, 54 and 5 differentially methylated genes in small intestine, liver and longissimus dorsi muscle between NBW and IUGR piglets, respectively, which are related to development and differentiation, carbohydrate and energy metabolism, lipid metabolism, protein turnover, immune response, detoxification, oxidative stress and apoptosis pathway. The objective of this review is to assess the impact of differentially methylation status on developmental delay, metabolic disorders and immune deficiency of IUGR piglets.
Keywords: IUGR, piglet, MeDIP-Seq, small intestine, liver, muscle.
Graphical Abstract
[1]
Wu, G.; Bazer, F.W.; Wallace, J.M.; Spencer, T.E. BOARD-INVITED REVIEW: Intrauterine growth retardation: Implications for the animal sciences. J. Anim. Sci., 2006, 84, 2316-2337.
[2]
Berard, J.; Kreuzer, M.; Bee, G. Effect of litter size and birth weight on growth, carcass and pork quality, and their relationship to postmortem proteolysis. J. Anim. Sci., 2008, 86, 2357-2368.
[3]
He, Z.X.; Wu, D.Q.; Sun, Z.H.; Tan, Z.L.; Qiao, J.Y.; Ran, T.; Tang, S.X.; Zhou, C.S.; Han, X.F.; Wang, M.; Kang, J.H.; Beauchemin, K.A. Protein or energy restriction during late gestation alters fetal growth and visceral organ mass: An evidence of intrauterine programming in goats. Anim. Reprod. Sci., 2013, 137, 177-182.
[4]
Lin, G.; Liu, C.; Feng, C.; Fan, Z.; Dai, Z.; Lai, C.; Li, Z.; Wu, G.; Wang, J. Metabolomic analysis reveals differences in umbilical vein plasma metabolites between normal and growth-restricted fetal pigs during late gestation. J. Nutr., 2012, 142, 990-998.
[5]
Wang, X.; Wu, W.; Lin, G.; Li, D.; Wu, G.; Wang, J. Temporal proteomic analysis reveals continuous impairment of intestinal development in neonatal piglets with intrauterine growth restriction. J. Proteome Res., 2010, 9, 924-935.
[6]
Liu, C.; Lin, G.; Wang, X.; Wang, T.; Wu, G.; Li, D.; Wang, J. Intrauterine growth restriction alters the hepatic proteome in fetal pigs. J. Nutr. Biochem., 2013, 24, 954-959.
[7]
Wang, J.; Chen, L.; Li, D.; Yin, Y.; Wang, X.; Li, P.; Dangott, L.J.; Hu, W.; Wu, G. Intrauterine growth restriction affects the proteomes of the small intestine, liver, and skeletal muscle in newborn pigs. J. Nutr., 2008, 138, 60-66.
[8]
Wang, T.; Liu, C.; Feng, C.; Wang, X.; Lin, G.; Zhu, Y.; Yin, J.; Li, D.; Wang, J. IUGR alters muscle fiber development and proteome in fetal pigs. Front. Biosci., 2013, 18, 598-607.
[10]
Busslinger, M.; Flavell, R.A. DNA methylation and the regulation of globin gene expression. Prog. Clin. Biol. Res., 1983, 134, 193-203.
[11]
Mohandas, T.; Sparkes, R.S.; Shapiro, L.J. Reactivation of an inactive human X chromosome: evidence for X inactivation by DNA methylation. Science, 1981, 211, 393-396.
[12]
Li, M.; Wu, H.; Luo, Z.; Xia, Y.; Guan, J.; Wang, T.; Gu, Y.; Chen, L.; Zhang, K.; Ma, J.; Liu, Y.; Zhong, Z.; Nie, J.; Zhou, S.; Mu, Z.; Wang, X.; Qu, J.; Jing, L.; Wang, H.; Huang, S.; Yi, N.; Wang, Z. An atlas of DNA methylomes in porcine adipose and muscle tissues. Nat. Commun., 2012, 3, 850.
[13]
Li, Q.; Li, N.; Hu, X.; Li, J.; Du, Z.; Chen, L.; Yin, G.; Duan, J.; Zhang, H.; Zhao, Y.; Wang, J.; Li, N. Genome-wide mapping of DNA methylation in chicken. PLoS One, 2011, 6(5)e19428
[14]
Kwak, W.; Kim, J.N.; Kim, D.; Hong, J.S.; Jeong, J.H.; Kim, H.; Cho, S.; Kim, Y.Y. Genome-wide DNA methylation profiles of small intestine and liver in fast-growing and slow-growing weaning piglets. Asian. Austral. J. Anim., 2014, 27, 1532-1539.
[15]
Thomas, R.M.; Sai, H.; Wells, A.D. Conserved intergenic elements and DNA methylation cooperate to regulate transcription at the il17 locus. J. Biol. Chem., 2012, 287, 25049-25059.
[16]
Doerfler, W.; Kruczek, I.; Eick, D.; Vardimon, L.; Kron, B. DNA methylation and gene activity: the adenovirus system as a model. Cold. Spring. Harb. Sym., 1983, 47(Pt 2), 593-603.
[17]
Aw, T.Y. Intestinal glutathione: Determinant of mucosal peroxide transport, metabolism, and oxidative susceptibility. Toxicol. Appl. Pharmacol., 2005, 204, 320-328.
[18]
Kellett, G.L.; Brot-Laroche, E. Apical GLUT2 - A major pathway of intestinal sugar absorption. Diabetes, 2005, 54, 3056-3062.
[19]
Thorn, S.R.; Rozance, P.J.; Brown, L.D.; Hay, W.W., Jr The intrauterine growth restriction phenotype: Fetal adaptations and potential implications for later life insulin resistance and diabetes. Semin. Reprod. Med., 2011, 29, 225-236.
[20]
Harmel, E.; Bendjoudi, A.; Elchebly, M.; Viollet, B.; Ziv, E.; Delvin, E.; Laville, M.; Levy, E. Disorders in AMPK and insulin signalling pathways in the intestine of insulin-resistant and diabetic psammomys obesus. Gasteroenterology, 2011, 140, S544-S544.
[21]
Sandor, N.; Pap, D.; Prechl, J.; Erdei, A.; Bajtay, Z. A novel, complement-mediated way to enhance the interplay between macrophages, dendritic cells and T lymphocytes. Mol. Immunol., 2009, 47, 438-448.
[22]
Ghannam, A.; Pernollet, M.; Fauquert, J.L.; Monnier, N.; Ponard, D.; Villiers, M.B.; Peguet-Navarro, J.; Tridon, A.; Lunardi, J.; Gerlier, D.; Drouet, C. Human C3 deficiency associated with impairments in dendritic cell differentiation, memory B cells, and regulatory T cells. J. Immunol., 2008, 181, 5158-5166.
[23]
Kosinski, C.; Li, V.S.; Chan, A.S.; Zhang, J.; Ho, C.; Tsui, W.Y.; Chan, T.L.; Mifflin, R.C.; Powell, D.W.; Yuen, S.T.; Leung, S.Y.; Chen, X. Gene expression patterns of human colon tops and basal crypts and BMP antagonists as intestinal stem cell niche factors. Proc. Natl. Acad. Sci. USA, 2007, 104, 15418-15423.
[24]
Sinha, P.; Singh, K.; Sachan, M. High resolution methylation analysis of the HoxA5 regulatory region in different somatic tissues of laboratory mouse during development. Gene Expr. Patterns, 2017, 23-24, 59-69.
[25]
Fu, J.; Bian, M.; Jiang, Q.; Zhang, C. Roles of aurora kinases in mitosis and tumorigenesis. Mol. Cancer Res., 2007, 5, 1-10.
[26]
Schuendeln, M.M.; Piekorz, R.P.; Wichmann, C.; Lee, Y.; McKinnon, P.J.; Boyd, K.; Takahashi, Y.; Ihle, J.N. The centrosomal, putative tumor suppressor protein TACC2 is dispensable for normal development, and deficiency does not lead to cancer. Mol. Cell. Biol., 2004, 24, 6403-6409.
[27]
Karin, M.; Greten, F.R. NF kappa B: Linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol., 2005, 5, 749-759.
[28]
Xiao, H.; Han, B.; Lodyga, M.; Bai, X.H.; Wang, Y.; Liu, M. The actin-binding domain of actin filament-associated protein (AFAP) is involved in the regulation of cytoskeletal structure. Cell. Mol. Life Sci., 2012, 69, 1137-1151.
[29]
Takahashi, R.; Nagayama, S.; Furu, M.; Kajita, Y.; Jin, Y.; Kato, T.; Imoto, S.; Sakai, Y.; Toguchida, J. AFAP1L1, a novel associating partner with vinculin, modulates cellular morphology and motility, and promotes the progression of colorectal cancers. Cancer Med., 2014, 3, 759-774.
[30]
Kobori, T.; Harada, S.; Nakamoto, K.; Tokuyama, S. Changes in PtdIns(4,5)P2 induced by etoposide treatment modulates small intestinal p-glycoprotein via radixin. Biol. Pharm. Bull., 2014, 37, 1124-1131.
[31]
Scandroglio, F.; Tortora, V.; Radi, R.; Castro, L. Metabolic control analysis of mitochondrial aconitase: Influence over respiration and mitochondrial superoxide and hydrogen peroxide production. Free Radic. Res., 2014, 48, 684-693.
[32]
Nabokina, S.M.; Valle, J.E.; Said, H.M. Characterization of the human mitochondrial thiamine pyrophosphate transporter SLC25A19 minimal promoter: A role for NF-Y in regulating, basal transcription. Gene, 2013, 528, 248-255.
[33]
Bing, Peng. J.; Zhu, Q.; Zhong Ying, L.; Xu Shi, H.; Wang, Z. Chlorogenic acid maintains glucose homeostasis through modulating the expression of SGLT-1, GLUT-2, and PLG in different intestinal segments of sprague-dawley rats fed a high-fat diet. Biomed. Environ. Sci., 2015, 28, 894-903.
[34]
Thoden, J.B.; Timson, D.J.; Reece, R.J.; Holden, H.M. Molecular structure of human galactose mutarotase. J. Biol. Chem., 2004, 279, 23431-23437.
[35]
Sane, A.; Seidman, E.; Spahis, S.; Lamantia, V.; Garofalo, C.; Montoudis, A.; Marcil, V.; Levy, E. New insights in intestinal Sar1B GTPase regulation and role in cholesterol homeostasis. J. Cell. Biochem., 2015, 116, 2270-2282.
[36]
Runyon, S.T.; Zhang, Y.; Appleton, B.A.; Sazinsky, S.L.; Wu, P.; Pan, B.; Wiesmann, C.; Skelton, N.J.; Sidhu, S.S. Structura and functional analysis of the PDZ domains of human HtrA1 and HtrA3. Protein Sci., 2007, 16, 2454-2471.
[37]
Hu, H.; Eggers, K.; Chen, W.; Garshasbi, M.; Motazacker, M.M.; Wrogemann, K.; Kahrizi, K.; Tzschach, A.; Hosseini, M.; Bahman, I.; Hucho, T.; Muehlenhoff, M.; Gerardy-Schahn, R.; Najmabadi, H.; Ropers, H.H.; Kuss, A.W. ST3GAL3 mutations impair the development of higher cognitive functions. Am. J. Hum. Genet., 2011, 89, 407-414.
[38]
Anderson, K.; Peng, Q.; Li, K.; Zhou, W.; Sacks, S. Exploration of mechanisms by which production of C3 by dendritic cells (DCs) modulates their function of antigen presentation. Mol. Immunol., 2007, 44, 3992-3992.
[39]
Pondman, K.M.; Tsolaki, A.G.; Paudyal, B.; Shamji, M.H.; Switzer, A.; Pathan, A.A.; Abozaid, S.M.; Ten Haken, B.; Stenbeck, G.; Sim, R.B.; Kishore, U. Complement deposition on nanoparticles can modulate immune responses by macrophage, B and T cells. J. Biomed. Nanotechnol., 2016, 12, 197-216.
[40]
Berin, M.C.; Dwinell, M.B.; Eckmann, L.; Kagnoff, M.F. Production
of MDC/CCL22 by human intestinal epithelial cells. Am. J.
Physiol-Gastr. L., 2001. 280, G1217-G1226
[41]
Wu, G.; Zhou, W.; Zhao, J.; Pan, X.; Sun, Y.; Xu, H.; Shi, P.; Geng, C.; Gao, L.; Tian, X. Matrine alleviates lipopolysaccharide-induced intestinal inflammation and oxidative stress via CCR7 signal. Oncotarget, 2017, 8, 11621-11628.
[42]
Round, J.L.; Mazmanian, S.K. Inducible Foxp(3+) regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl. Acad. Sci. USA, 2010, 107, 12204-12209.
[43]
Laforenza, U.; Gastaldi, G.; Polimeni, M.; Tritto, S.; Tosco, M.; Ventura, U.; Scaffino, M.F.; Yasui, M. Aquaporin-6 is expressed along the rat gastrointestinal tract and upregulated by feeding in the small intestine. BMC Physiol., 2009, 9, 18-18.
[44]
Ikpa, P.T.; Sleddens, H.F.B.M.; Steinbrecher, K.A.; Peppelenbosch, M.P.; de Jonge, H.R.; Smits, R.; Bijvelds, M.J.C. Guanylin and uroguanylin are produced by mouse intestinal epithelial cells of columnar and secretory lineage. Histochem. Cell Biol., 2016, 146, 445-455.
[45]
Schwabe, K.; Cetin, Y. Guanylin and functional coupling proteins in the hepatobiliary system of rat and guinea pig. Histochem. Cell Biol., 2012, 137, 589-597.
[47]
Limesand, S.W.; Rozance, P.J.; Smith, D.; Hay, W.W. Jr. Increased
insulin sensitivity and maintenance of glucose utilization
rates in fetal sheep with placental insufficiency and intrauterine
growth restriction. Am. J. Physiol-Endoc. M., 2007. 293, E1716-
E1725
[48]
Gentili, S.; Morrison, J.L.; McMillen, I.C. Intrauterine growth restriction and differential patterns of hepatic growth and expression of IGF1, PCK2, and HSDL1 mRNA in the sheep fetus in late gestation. Biol. Reprod., 2009, 80, 1121-1127.
[49]
Vuguin, P.; Raab, E.; Liu, B.; Barzilai, N.; Simmons, R. Hepatic insulin resistance precedes the development of diabetes in a model of intrauterine growth retardation. Diabetes, 2004, 53, 2617-2622.
[50]
Schmidt, M.; Dekker, F.J.; Maarsingh, H. Exchange protein directly activated by cAMP (epac): A multidomain cAMP mediator in the regulation of diverse biological functions. Pharmacol. Rev., 2013, 65, 670-709.
[51]
Thorn, S.R.; Regnault, T.R.H.; Brown, L.D.; Rozance, P.J.; Keng, J.; Roper, M.; Wilkening, R.B.; Hay, W.W. Jr. Friedman, J.E. Intrauterine growth restriction increases fetal hepatic gluconeogenic capacity and reduces messenger ribonucleic acid translation initiation and nutrient sensing in fetal liver and skeletal muscle. Endocrinology, 2009, 150, 3021-3030.
[52]
Narayanan, A.; Amaya, M.; Voss, K.; Chung, M.; Benedict, A.; Sampey, G.; Kehn-Hall, K.; Luchini, A.; Liotta, L.; Bailey, C.; Kumar, A.; Bavari, S.; Hakami, R.M.; Kashanchi, F. Reactive oxygen species activate NF kappa B (p65) and p53 and induce apoptosis in RVFV infected liver cells. Virology, 2014, 449, 270-286.
[53]
Derdak, Z.; Lang, C.H.; Villegas, K.A.; Tong, M.; Mark, N.M.; de la Monte, S.M.; Wands, J.R. Activation of p53 enhances apoptosis and insulin resistance in a rat model of alcoholic liver disease. J. Hepatol., 2011, 54, 164-172.
[54]
Huang, L.; Heinloth, A.N.; Zeng, Z.B.; Paules, R.S.; Bushel, P.R. Genes related to apoptosis predict necrosis of the liver as a phenotype observed in rats exposed to a compendium of hepatotoxicants. BMC Genomics, 2008, 9, 288.
[55]
Magliarelli, H.D.F.; Matondo, M.; Meszaros, G.; Goginashvili, A.; Erbs, E.; Zhang, Z.; Mihlan, M.; Wolfrum, C.; Aebersold, R.; Sumara, I.; Ricci, R. Liver ubiquitome uncovers nutrient-stress-mediated trafficking and secretion of complement C3. Cell Death Dis., 2016, 7(10)e2411
[56]
Bavia, L.; Cogliati, B.; Dettoni, J.B.; Ferreira Alves, V.A.; Isaac, L. The complement component C5 promotes liver steatosis and inflammation in murine non-alcoholic liver disease model. Immunol. Lett., 2016, 177, 53-61.
[57]
Min, J.S.; DeAngelis, R.A.; Reis, E.S.; Gupta, S.; Maurya, M.R.; Evans, C.; Das, A.; Burant, C.; Lambris, J.D.; Subramaniam, S. Systems analysis of the complement-induced priming phase of liver regeneration. J. Immunol., 2016, 197, 2500-2508.
[58]
Paulikova, S.; Petera, J.; Sirak, I.; Vosmik, M.; Drastikova, M.; Dusek, L.; Cvanova, M.; Soumarova, R.; Spacek, J.; Beranek, M. ATM and TGFB1 genes polymorphisms in prediction of late complications of chemoradiotherapy in patients with locally advanced cervical cancer. Neoplasma, 2014, 61, 70-76.
[59]
Walesky, C.; Apte, U. Role of hepatocyte nuclear factor 4 alpha (HNF4 alpha) in Cell proliferation and cancer. Gene Expr., 2015, 16, 101-108.
[60]
He, X.C.; Zhang, H.W.; Li, L.H. Cellular and molecular regulation of hematopoietic and intestinal stem cell behavior. In: Stem Cell
Biology: Development and Plasticity, Ourednik, J.; Ourednik, V.;
Sakaguchi, D.S.; NilsenHamilton, M.; Eds; , 2005; Vol. 1049,, pp. 28-38.
[61]
Jones, C.N.; Tuleuova, N.; Lee, J.Y.; Ramanculov, E.; Reddi, A.H.; Zern, M.A.; Revzin, A. Cultivating hepatocytes on printed arrays of HGF and BMP7 to characterize protective effects of these growth factors during in vitro alcohol injury. Biomaterials, 2010, 31, 5936-5944.
[62]
Xu, K.; Gao, J.; Yang, X.; Yao, Y.; Liu, Q. Cytohesin-2 as a novel prognostic marker for hepatocellular carcinoma. Oncol. Rep., 2013, 29, 2211-2218.
[63]
Desbuquois, B.; Carre, N.; Burnol, A.F. Regulation of insulin and type 1 insulin-like growth factor signaling and action by the Grb10/14 and SH2B1/B2 adaptor proteins. FEBS J., 2013, 280, 794-816.
[64]
Shin, J.Y.; Chung, Y.S.; Kang, B.; Jiang, H.L.; Yu, D.Y.; Han, K.; Chae, C.; Moon, J.H.; Jang, G.; Cho, M.H. Co-delivery of LETM1 and CTMP synergistically inhibits tumor growth in H-ras12V liver cancer model mice. Cancer Gene Ther., 2013, 20, 186-194.
[65]
He, Y.; Wu, Y.T.; Huang, C.; Meng, X.M.; Ma, T.T.; Wu, B.M.; Xu, F.Y.; Zhang, L.; Lv, X.W.; Li, J. Inhibitory effects of long noncoding RNA MEG3 on hepatic stellate cells activation and liver fibrogenesis. BBA-Mol. Basis Dis., 2014, 1842, 2204-2215.
[66]
Zhang, J.; Luo, H.; Du, J.; Liu, Y. MicroRNA-300 plays as oncogene by promoting proliferation and reducing apoptosis of liver cancer cells by targeting MDC1. Int. J. Clin. Exp. Pathol., 2016, 9, 1231-1239.
[67]
Schwaderer, J.; Gaiser, A.K.; Phan, T.S.; Delgado, M.; Brunner, T. Liver receptor homolog-1 (NR5a2) regulates CD95/Fas ligand transcription and associated T-cell effector functions. Cell Death Dis., 2017, 8, e2745-e2745.
[68]
Feng, T.; Dzieran, J.; Gu, X.; Marhenke, S.; Vogel, A.; Machida, K.; Weiss, T.S.; Ruemmele, P.; Kollmar, O.; Hoffmann, P.; Graesser, F.; Allgayer, H.; Fabian, J.; Weng, H.L.; Teufel, A.; Maass, T.; Meyer, C.; Lehmann, U.; Zhu, C.; Mertens, P.R.; Gao, C.F.; Dooley, S.; Meindl-Beinker, N.M. Smad7 regulates compensatory hepatocyte proliferation in damaged mouse liver and positively relates to better clinical outcome in human hepatocellular carcinoma. Clin. Sci. , 2015, 128, 761-774.
[69]
Hellgren, G.; Jansson, J.O.; Carlsson, L.M.S.; Carlsson, B. The growth hormone receptor associates with Jak1, Jak2 and Tyk2 in human liver. Growth Horm. IGF Res., 1999, 9, 212-218.
[70]
Hong, S.; Hur, W.; Choi, J.E.; Kim, J.H.; Hwang, D.; Yoon, S.K. Role of ADAM17 in invasion and migration of CD133-expressing liver cancer stem cells after irradiation. Oncotarget, 2016, 7, 23482-23497.
[71]
Xie, B.; Lin, W.; Ye, J.; Wang, X.; Zhang, B.; Xiong, S.; Li, H.; Tan, G. DDR2 facilitates hepatocellular carcinoma invasion and metastasis via activating ERK signaling and stabilizing SNAIL1. J. Exp. Clin. Cancer Res., 2015, 34, 101.
[72]
Avadanei, R.; Caruntu, I.D.; Amalinei, C.; Lozneanu, L.; Balan, R.; Grigoras, A.; Apostol, D.C.; Giusca, S.E. High variability in MMP2/TIMP2 and MMP9/TIMP1 expression in secondary liver tumors. Rom. J. Morphol. Embryol., 2013, 54, 479-485.
[73]
Sambrotta, M.; Strautnieks, S.; Papouli, E.; Rushton, P.; Clark, B.E.; Parry, D.A.; Logan, C.V.; Newbury, L.J.; Kamath, B.M.; Ling, S.; Grammatikopoulos, T.; Wagner, B.E.; Magee, J.C.; Sokol, R.J.; Mieli-Vergani, G.; Smith, J.D.; Johnson, C.A.; McClean, P.; Simpson, M.A.; Knisely, A.S.; Bull, L.N.; Thompson, R.J.; Univ Washington Ctr Mendelian, G. Mutations in TJP2 cause progressive cholestatic liver disease. Nat. Genet., 2014, 46(4), 326-328.
[74]
Untereiner, A.A.; Wang, R.; Ju, Y.; Wu, L. Decreased gluconeogenesis in the absence of cystathionine gamma-lyase and the underlying mechanisms. Antioxid. Redox Signal., 2016, 24, 129-140.
[75]
Cheng, K.M. Hepatic glycogen metabolism in normal developing and intrauterine growth-retarded rat fetuses. Nippon Sanka Fujinka Gakkai Zasshi, 1988, 40, 781-788.
[76]
Vieira, P.; Cameron, J.; Rahikkala, E.; Keski-Filppula, R.; Zhang, L.H.; Santra, S.; Matthews, A.; Myllynen, P.; Nuutinen, M.; Moilanen, J.S.; Rodenburg, R.J.; Rolfs, A.; Uusimaa, J.; van Karnebeek, C.D.M. Novel homozygous PCK1 mutation causing cytosolic phosphoenolpyruvate carboxykinase deficiency presenting as childhood hypoglycemia, an abnormal pattern of urine metabolites and liver dysfunction. Mol. Genet. Metab., 2017, 120, 337-341.
[77]
Nemazanyy, I.; Panasyuk, G.; Zhyvoloup, A.; Panayotou, G.; Gout, I.T.; Filonenko, V. Specific interaction between S6K1 and CoA synthase: A potential link between the mTOR/S6K pathway, CoA biosynthesis and energy metabolism. FEBS Lett., 2004, 578, 357-362.
[78]
Mello, T.; Zanieri, F.; Materozzi, M.; Bereshchenko, O.; Ceni, E.; Tarocchi, M.; Marroncini, G.; Polvani, S.; Tempesti, S.; Nerlov, C.; Milani, S.; Galli, A. Ruvbl1 regulates liver glucose metabolism via the Akt/mTOR pathway: Implications for hepatocellular carcinoma progression. Dig. Liver Dis., 2016, 48, E8-E9.
[79]
Hayhurst, G.P.; Lee, Y.H.; Lambert, G.; Ward, J.M.; Gonzalez, F.J. Hepatocyte nuclear factor 4 alpha (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol. Cell. Biol., 2001, 21, 1393-1403.
[80]
Inoue, Y.; Yu, A.M.; Yim, S.H.; Ma, X.C.; Krausz, K.W.; Inoue, J.; Xiang, C.C.; Brownstein, M.J.; Eggertsen, G.; Bjorkhem, I.; Gonzalez, F.J. Regulation of bile acid biosynthesis by hepatocyte nuclear factor 4 alpha. J. Lipid Res., 2006, 47, 215-227.
[81]
Xu, J.; Xu, Y.; Li, Y.; Jadhav, K.; You, M.; Yin, L.; Zhang, Y. Carboxylesterase 1 is regulated by hepatocyte nuclear factor 4 alpha and protects against alcohol- and MCD diet-induced liver injury. Sci. Rep., 2016, 6, 24277.
[82]
Yoshinari, K.; Ohno, H.; Benoki, S.; Yamazoe, Y. Constitutive androstane receptor transactivates the hepatic expression of mouse Dhcr24 and human DHCR24 encoding a cholesterogenic enzyme 24-dehydrocholesterol reductase. Toxicol. Lett., 2012, 208, 185-191.
[83]
Vluggens, A.; Andreoletti, P.; Viswakarma, N.; Jia, Y.; Matsumoto, K.; Kulik, W.; Khan, M.; Huang, J.; Guo, D.; Yu, S.; Sarkar, J.; Singh, I.; Rao, M.S.; Wanders, R.J.; Reddy, J.K.; Cherkaoui-Malki, M. Functional significance of the two ACOX1 isoforms and their crosstalks with PPAR alpha and RXR alpha. Lab. Invest., 2010, 90, 808-818.
[84]
Reardon, H.T.; Hsieh, A.T.; Jung Park, W.; Kothapalli, K.S.D.; Anthony, J.C.; Nathanielsz, P.W.; Thomas Brenna, J. Dietary long-chain polyunsaturated fatty acids upregulate expression of FADS3 transcripts. PLEFA, 2013, 88, 15-19.
[85]
Lopez-Vicario, C.; Alcaraz-Quiles, J.; Garcia-Alonso, V.; Rius, B.; Hwang, S.H.; Titos, E.; Lopategi, A.; Hammock, B.D.; Arroyo, V.; Claria, J. Inhibition of soluble epoxide hydrolase modulates inflammation and autophagy in obese adipose tissue and liver: Role for omega-3 epoxides. Proc. Natl. Acad. Sci. USA, 2015, 112, 536-541.
[86]
Suelzle, A.; Hirche, F.; Eder, K. Thermally oxidized dietary fat upregulates the expression of target genes of PPARa in rat liver. J. Nutr., 2004, 134, 1375-1383.
[87]
Bykov, I.; Junnikkala, S.; Pekna, M.; Lindros, K.O.; Meri, S. Complement C3 contributes to ethanol-induces liver steatosis in mice. Ann. Med., 2006, 38, 280-286.
[88]
Markiewski, M.M.; DeAngelis, R.A.; Strey, C.W.; Foukas, P.G.; Gerard, C.; Gerard, N.; Wetsel, R.A.; Lambris, J.D. The regulation of liver cell survival by complement. J. Immunol., 2009, 182, 5412-5418.
[89]
Doronin, K.; Flatt, J.W.; Di Paolo, N.C.; Khare, R.; Kalyuzhniy, O.; Acchione, M.; Sumida, J.P.; Ohto, U.; Shimizu, T.; Akashi-Takamura, S.; Miyake, K.; MacDonald, J.W.; Bammler, T.K.; Beyer, R.P.; Farin, F.M.; Stewart, P.L.; Shayakhmetov, D.M. Coagulation factor X activates innate immunity to human species C adenovirus. Science, 2012, 338, 795-798.
[90]
Delgado, M.; Gomariz, R.P.; Martinez, C.; Abad, C.; Leceta, J. Anti-inflammatory properties of the type 1 and type 2 vasoactive intestinal peptide receptors: Role in lethal endotoxic shock. Eur. J. Immunol., 2000, 30, 3236-3246.
[91]
Liu, Y.M.; Chen, Y.; Li, J.Z.; Gong, J.P. Up-regulation of Galectin-9 in vivo results in immunosuppressive effects and prolongs survival of liver allograft in rats. Immunol. Lett., 2014, 162, 217-222.
[92]
Faustino, L.C.; Pires, R.M.; Lima, A.C.; Cordeiro, A.; Souza, L.L.; Ortiga-Carvalho, T.M. Liver glutathione S-transferase alpha expression is decreased by 3,5,3 '-triiodothyronine in hypothyroid but not in euthyroid mice. Exp. Physiol., 2011, 96, 790-800.
[93]
Vinchi, F.; Gastaldi, S.; Silengo, L.; Altruda, F.; Tolosano, E. Hemopexin prevents endothelial damage and liver congestion in a mouse model of heme overload. Am. J. Pathol., 2008, 173, 289-299.
[94]
Xie, Y.; Liu, Y.; Zhao, Y.; Wang, H.; Liu, Y.; Wang, H.; Li, M.; Zhao, H.; Zhou, Q.; Lv, X. Gulo acts as a de novo marker for pronephric tubules in Xenopus laevis. Kidney Blood Press. Res., 2016, 41, 794-801.
[95]
Wang, Y.D.; Chen, W.D.; Li, C.; Guo, C.; Li, Y.; Qi, H.; Shen, H.; Kong, J.; Long, X.; Yuan, F.; Wang, X.; Huang, W. D Farnesoid X receptor antagonizes JNK signaling pathway in liver carcinogenesis by activating SOD3. Mol. Endocrinol., 2015, 29, 322-331.
[96]
Aromataris, E.C.; Castro, J.; Rychkov, G.Y.; Barritt, G.J. Store-operated Ca2+ channels and Stromal Interaction Molecule 1 (STIM1) are targets for the actions of bile acids on liver cells. BBA-Mol. Cell Res., 2008, 1783, 874-885.
[97]
Leu, J.I.J.; George, D.L. Hepatic IGFBP1 is a prosurvival factor that binds to BAK, protects the liver from apoptosis, and antagonizes the proapoptotic actions of p53 at mitochondria. Genes Dev., 2007, 21, 3095-3109.
[98]
Ladha, J.S.; Tripathy, M.K.; Mitra, D. Mitochondrial complex I activity is impaired during HIV-1-induced T-cell apoptosis. Cell Death Differ., 2005, 12, 1417-1428.
[99]
Greenwood, P.L.; Hunt, A.S.; Hermanson, J.W.; Bell, A.W. Effects of birth weight and postnatal nutrition on neonatal sheep: II. Skeletal muscle growth and development. J. Anim. Sci., 2000, 78, 50-61.
[100]
Tilley, R.E.; McNeil, C.J.; Ashworth, C.J.; Page, K.R.; McArdle, H.J. Altered muscle development and expression of the insulin-like growth factor system in growth retarded fetal pigs. Domest. Anim. Endocrinol., 2007, 32, 167-177.
[101]
Tasseva, G.; van der Veen, J.N.; Lingrell, S.; Jacobs, R.L.; Vance, D.E.; Vance, J.E. Lack of phosphatidylethanolamine N-methyltransferase in mice does not promote fatty acid oxidation in skeletal muscle. Biochim. Biophys. Acta, 2016, 1861, 119-129.
[102]
Wei, H.; Li, Z.; Wang, X.; Wang, J.; Pang, W.; Yang, G.; Shen, Q.W. microRNA-151-3p regulates slow muscle gene expression by targeting ATP2a2 in skeletal muscle cells. J. Cell. Physiol., 2015, 230, 1003-1012.
[103]
Salam, R.A.; Das, J.K.; Bhutta, Z.A. Impact of intrauterine growth restriction on long-term health. Curr. Opin. Clin. Nutr., 2014, 17, 249-254.
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