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Mitochondrial dysfunction and epigenetics underlying the link between early-life nutrition and non-alcoholic fatty liver disease

Published online by Cambridge University Press:  24 January 2022

Anabela La Colla ,
Carolina Anahí Cámara ,
Sabrina Campisano  and
Andrea Nancy Chisari Open the ORCID record for Andrea Nancy Chisari [Opens in a new window]
Anabela La Colla*
Affiliation:
Departamento de Química y Bioquímica, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, 7600 Mar del Plata, Argentina
Carolina Anahí Cámara
Affiliation:
Departamento de Química y Bioquímica, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, 7600 Mar del Plata, Argentina
Sabrina Campisano
Affiliation:
Departamento de Química y Bioquímica, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, 7600 Mar del Plata, Argentina
Andrea Nancy Chisari*
Affiliation:
Departamento de Química y Bioquímica, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, 7600 Mar del Plata, Argentina
*
*Co-corresponding authors: Dr. Andrea N. Chisari, email: achisari@mdp.edu.ar; Dr. Anabela La Colla, email: analacolla@mdp.edu.ar
*Co-corresponding authors: Dr. Andrea N. Chisari, email: achisari@mdp.edu.ar; Dr. Anabela La Colla, email: analacolla@mdp.edu.ar
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Abstract

Early-life malnutrition plays a critical role in foetal development and predisposes to metabolic diseases later in life, according to the concept of ‘developmental programming’. Different types of early nutritional imbalance, including undernutrition, overnutrition and micronutrient deficiency, have been related to long-term metabolic disorders. Accumulating evidence has demonstrated that disturbances in nutrition during the period of preconception, pregnancy and primary infancy can affect mitochondrial function and epigenetic mechanisms. Moreover, even though multiple mechanisms underlying non-alcoholic fatty liver disease (NAFLD) have been described, in the past years, special attention has been given to mitochondrial dysfunction and epigenetic alterations. Mitochondria play a key role in cellular metabolic functions. Dysfunctional mitochondria contribute to oxidative stress, insulin resistance and inflammation. Epigenetic mechanisms have been related to alterations in genes involved in lipid metabolism, fibrogenesis, inflammation and tumorigenesis. In accordance, studies have reported that mitochondrial dysfunction and epigenetics linked to early-life nutrition can be important contributing factors in the pathogenesis of NAFLD. In this review, we summarise the current understanding of the interplay between mitochondrial dysfunction, epigenetics and nutrition during early life, which is relevant to developmental programming of NAFLD.

Keywords

Early-life nutritionEpigeneticsMitochondriaDevelopmental programmingNAFLD
Type
Review Article
Information
Nutrition Research Reviews , Volume 36 , Issue 2 , December 2023 , pp. 281 - 294
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Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of The Nutrition Society

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References

Friedman, SL, Neuschwander-Tetri, BA, Rinella, M, et al. (2018) Mechanisms of NAFLD development and therapeutic strategies. Nat Med 24, 908–922.CrossRefGoogle ScholarPubMed
Campisano, S, La Colla, A, Echarte, SM, et al. (2019) Interplay between early-life malnutrition, epigenetic modulation of the immune function and liver diseases. Nutr Res Rev 32, 128–145.CrossRefGoogle ScholarPubMed
Picard, M & Turnbull, DM (2013) Linking the metabolic state and mitochondrial DNA in chronic disease, health, and aging. Diabetes 62, 672–678.CrossRefGoogle ScholarPubMed
Calcaterra, V, Cena, H, Verduci, E, et al. (2020) Nutritional surveillance for the best start in life, promoting health for neonates, infants and children. Nutrients 12, 3386.CrossRefGoogle ScholarPubMed
Brumbaugh, DE & Friedman, JE (2014) Developmental origins of nonalcoholic fatty liver disease. Pediatr Res 75, 140–147.CrossRefGoogle ScholarPubMed
Kim, J-A, Wei, Y & Sowers, JR (2008) Role of mitochondrial dysfunction in insulin resistance. Circ Res 102, 401–414.CrossRefGoogle ScholarPubMed
Xu, L, Nagata, N & Ota, T (2019) Impact of glucoraphanin-mediated activation of Nrf2 on non-alcoholic fatty liver disease with a focus on mitochondrial dysfunction. Int J Mol Sci 20, 5920.CrossRefGoogle ScholarPubMed
Wiederkehr, A & Wollheim, CB (2006) Minireview: implication of mitochondria in insulin secretion and action. Endocrinology 147, 2643–2649.CrossRefGoogle ScholarPubMed
Del Campo, JA, Gallego-Durán, R, Gallego, P, et al. (2018) Genetic and epigenetic regulation in nonalcoholic fatty liver disease (NAFLD). Int J Mol Sci 19, 911.CrossRefGoogle ScholarPubMed
Xu, F & Guo, W (2020) The progress of epigenetics in the development and progression of non-alcoholic fatty liver disease. Liver Res 4, 118–123.CrossRefGoogle Scholar
Black, RE, Victora, CG, Walker, SP, et al. (2013) Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 382, 427–451.CrossRefGoogle ScholarPubMed
Li, M, Reynolds, CM, Segovia, SA, et al. (2015) Developmental programming of nonalcoholic fatty liver disease: The effect of early life nutrition on susceptibility and disease severity in later life. Biomed Res Int 2015, 437107.Google ScholarPubMed
Ross, MG & Beall, MH (2008) Adult sequelae of intrauterine growth restriction. Semin Perinatol 32, 213–218.CrossRefGoogle ScholarPubMed
Thompson, MD (2020) Developmental programming of NAFLD by parental obesity. Hepatol Commun 4, 1392–1403.CrossRefGoogle ScholarPubMed
Barker, DJP (2007) The origins of the developmental origins theory. J Intern Med 261, 412–417.CrossRefGoogle ScholarPubMed
Gluckman, PD & Hanson, MA (2004) The developmental origins of the metabolic syndrome. Trends Endocrinol Metab 15, 183–187.CrossRefGoogle ScholarPubMed
McCurdy, CE, Bishop, JM, Williams, SM, et al. (2009) Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest 119, 323–335.Google ScholarPubMed
Bruce, KD, Cagampang, FR, Argenton, M, 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.CrossRefGoogle ScholarPubMed
Gregorio, BM, Souza-Mello, V, Carvalho, JJ, et al. (2010) Maternal high-fat intake predisposes nonalcoholic fatty liver disease in C57BL/6 offspring. Am J Obstet Gynecol 203, 495.e1-8.CrossRefGoogle ScholarPubMed
Souza-Mello, V, Mandarim-de-Lacerda, CA & Aguila, MB (2007) Hepatic structural alteration in adult programmed offspring (severe maternal protein restriction) is aggravated by post-weaning high-fat diet. Br J Nutr 98, 1159–1169.CrossRefGoogle ScholarPubMed
Sanchez-Blanco, C, Amusquivar, E, Bispo, K, et al. (2016) Influence of cafeteria diet and fish oil in pregnancy and lactation on pups’ body weight and fatty acid profiles in rats. Eur J Nutr 55, 1741–1753.CrossRefGoogle ScholarPubMed
Sánchez-Blanco, C, Amusquivar, E, Bispo, K, et al. (2019) Dietary fish oil supplementation during early pregnancy in rats on a cafeteria-diet prevents fatty liver in adult male offspring. Food Chem Toxicol 123, 546–552.CrossRefGoogle ScholarPubMed
Bayol, SA, Simbi, BH, Fowkes, RC, et al. (2010) Maternal ‘junk food’ diet in pregnancy and lactation promotes nonalcoholic fatty liver disease in rat offspring. Endocrinology 151, 1451–1461.CrossRefGoogle ScholarPubMed
Pruis, MGM, Lendvai, A, Bloks, VW, et al. (2014) Maternal western diet primes non-alcoholic fatty liver disease in adult mouse offspring. Acta Physiol (Oxf) 210, 215–227.CrossRefGoogle ScholarPubMed
Campisano, SE, Echarte, SM, Podaza, E, et al. (2017) Protein malnutrition during fetal programming induces fatty liver in adult male offspring rats. J Physiol Biochem 73, 275–285.CrossRefGoogle ScholarPubMed
Erhuma, A, Salter, AM, Sculley, DV, et al. (2007) Prenatal exposure to a low-protein diet programs disordered regulation of lipid metabolism in the aging rat. Am J Physiol Endocrinol Metab 292, 1702–1714.CrossRefGoogle ScholarPubMed
Deshmukh, U, Katre, P & Yajnik, CS (2013) Influence of maternal vitamin B12 and folate on growth and insulin resistance in the offspring. Nestle Nutr Inst Workshop Ser 74, 145–54.CrossRefGoogle ScholarPubMed
Khaire, A, Rathod, R, Kale, A, et al. (2015) Vitamin B and omega-3 fatty acids together regulate lipid metabolism in Wistar rats. Prostaglandins Leukot Essent Fatty Acids 99, 7–17.CrossRefGoogle ScholarPubMed
Ahmad, S, Kumar, KA, Basak, T, et al. (2013) PPAR signaling pathway is a key modulator of liver proteome in pups born to vitamin B(12) deficient rats. J Proteomics 91, 297–308.CrossRefGoogle ScholarPubMed
Pooya, S, Blaise, S, Moreno Garcia, M, et al. (2012) Methyl donor deficiency impairs fatty acid oxidation through PGC-1α hypomethylation and decreased ER-α, ERR-α, and HNF-4α in the rat liver. J Hepatol 57, 344–351.CrossRefGoogle ScholarPubMed
Sharma, SS, Jangale, NM, Harsulkar, AM, et al. (2017) Chronic maternal calcium and 25-hydroxyvitamin D deficiency in Wistar rats programs abnormal hepatic gene expression leading to hepatic steatosis in female offspring. J Nutr Biochem 43, 36–46.CrossRefGoogle ScholarPubMed
Spinelli, JB & Haigis, MC (2018) The multifaceted contributions of mitochondria to cellular metabolism. Nat Cell Biol 20, 745–754.CrossRefGoogle ScholarPubMed
Walsh, CT, Tu, BP & Tang, Y (2018) Eight kinetically stable but thermodynamically activated molecules that power cell metabolism. Chem Rev 118, 1460–1494.CrossRefGoogle ScholarPubMed
Zhao, R-Z, Jiang, S, Zhang, L, et al. (2019) Mitochondrial electron transport chain, ROS generation and uncoupling (Review). Int J Mol Med 44, 3–15.Google ScholarPubMed
Sazanov, LA (2015) A giant molecular proton pump: structure and mechanism of respiratory complex I. Nat Rev Mol Cell Biol 16, 375–388.CrossRefGoogle ScholarPubMed
Watt, IN, Montgomery, MG, Runswick, MJ, et al. (2010) Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. Proc Natl Acad Sci U S A 107, 16823–16827.CrossRefGoogle ScholarPubMed
Murphy, MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417, 1–13.CrossRefGoogle ScholarPubMed
Brand, MD (2010) The sites and topology of mitochondrial superoxide production. Exp Gerontol 45, 466–472.CrossRefGoogle ScholarPubMed
Schieber, M & Chandel, NS (2014) ROS function in redox signaling and oxidative stress. Curr Biol 24, 453–462.CrossRefGoogle ScholarPubMed
Sena, LA & Chandel, NS (2012) Physiological roles of mitochondrial reactive oxygen species. Mol Cell 48, 158–167.CrossRefGoogle ScholarPubMed
Cox, AG, Winterbourn, CC & Hampton, MB (2009) Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem J 425, 313–325.CrossRefGoogle ScholarPubMed
Winterbourn, CC & Hampton, MB (2008) Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45, 549–561.CrossRefGoogle ScholarPubMed
Ray, PD, Huang, B-W & Tsuji, Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24, 981–990.CrossRefGoogle ScholarPubMed
Betteridge, DJ (2000) What is oxidative stress? Metabolism 49, Suppl. 1, S3–S8.CrossRefGoogle ScholarPubMed
Wang, B, Van Veldhoven, PP, Brees, C, et al. (2013) Mitochondria are targets for peroxisome-derived oxidative stress in cultured mammalian cells. Free Radic Biol Med 65, 882–894.CrossRefGoogle ScholarPubMed
Radi, R, Cassina, A, Hodara, R, et al. (2002) Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 33, 1451–1464.CrossRefGoogle ScholarPubMed
Trujillo, M, Ferrer-Sueta, G & Radi, R (2008) Peroxynitrite detoxification and its biologic implications. Antioxid Redox Signal 10, 1607–1620.CrossRefGoogle ScholarPubMed
Simões, ICM, Fontes, A, Pinton, P, et al. (2018) Mitochondria in non-alcoholic fatty liver disease. Int J Biochem Cell Biol 95, 93–99.CrossRefGoogle ScholarPubMed
Petrosillo, G, Portincasa, P, Grattagliano, I, et al. (2007) Mitochondrial dysfunction in rat with nonalcoholic fatty liver Involvement of complex I, reactive oxygen species and cardiolipin. Biochim Biophys Acta 1767, 1260–1267.CrossRefGoogle ScholarPubMed
Pérez-Carreras, M, Del Hoyo, P, Martín, MA, et al. (2003) Defective hepatic mitochondrial respiratory chain in patients with nonalcoholic steatohepatitis. Hepatology 38, 999–1007.CrossRefGoogle ScholarPubMed
Besse-Patin, A, Leveille, M, Oropeza, D, et al. (2017) Estrogen signals through peroxisome proliferator-activated receptor-γ coactivator 1α to reduce oxidative damage associated with diet-induced fatty liver disease. Gastroenterology 152, 243–256 CrossRefGoogle ScholarPubMed
Onyango, IG, Lu, J, Rodova, M, et al. (2010) Regulation of neuron mitochondrial biogenesis and relevance to brain health. Biochim Biophys Acta 1802, 228–234.CrossRefGoogle ScholarPubMed
Scarpulla, RC, Vega, RB & Kelly, DP (2012) Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol Metab 23, 459–466.CrossRefGoogle ScholarPubMed
Wallace, DC (2018) Mitochondrial genetic medicine. Nat Genet 50, 1642–1649.CrossRefGoogle ScholarPubMed
Irrcher, I, Adhihetty, PJ, Sheehan, T, et al. (2003) PPARγ coactivator-1α expression during thyroid hormone- and contractile activity-induced mitochondrial adaptations. Am J Physiol Cell Physiol 284, 1669–1677.CrossRefGoogle ScholarPubMed
Virbasius, JV & Scarpulla, RC (1994) Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc Natl Acad Sci U S A 91, 1309–1313.CrossRefGoogle ScholarPubMed
Jornayvaz, FR & Shulman, GI (2010) Regulation of mitochondrial biogenesis. Essays Biochem 47, 69–84.Google ScholarPubMed
Vega, RB, Huss, JM & Kelly, DP (2000) The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor α in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol Cell Biol 20, 1868–1876.CrossRefGoogle ScholarPubMed
Giguère, V (2008) Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr Rev 29, 677–696.CrossRefGoogle ScholarPubMed
Winder, WW, Holmes, BF, Rubink, DS, et al (2000) Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J Appl Physiol 88, 2219–2226.CrossRefGoogle ScholarPubMed
Rodgers, JT, Lerin, C, Haas, W, et al. (2005) Nutrient control of glucose homeostasis through a complex of PGC-1α and SIRT1. Nature 434, 113–118.CrossRefGoogle ScholarPubMed
Kong, X, Wang, R, Xue, Y, et al. (2010) Sirtuin 3, a new target of PGC-1α, plays an important role in the suppression of ROS and mitochondrial biogenesis. PLoS One 5, e11707.CrossRefGoogle ScholarPubMed
Lin, J, Handschin, C & Spiegelman, BM (2005) Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 1, 361–370.CrossRefGoogle ScholarPubMed
Ritov, VB, Menshikova, EV, He, J, et al. (2005) Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54, 8–14.CrossRefGoogle ScholarPubMed
Lowell, BB & Shulman, GI (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307, 384–387.CrossRefGoogle ScholarPubMed
Delettre, C, Lenaers, G, Griffoin, JM, et al. (2000) Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26, 207–210.CrossRefGoogle ScholarPubMed
Cipolat, S, Martins de Brito, O, Dal Zilio, B, et al. (2004) OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc Natl Acad Sci U S A 101, 15927–15932.CrossRefGoogle ScholarPubMed
Smirnova, E, Griparic, L, Shurland, D-L, et al. (2001) Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol Biol Cell 12, 2245–2256.CrossRefGoogle ScholarPubMed
Otera, H, Wang, C, Cleland, MM, et al. (2010) Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J Cell Biol 191, 1141–1158.CrossRefGoogle ScholarPubMed
James, DI, Parone, PA, Mattenberger, Y, et al. (2003) hFis1, a novel component of the mammalian mitochondrial fission machinery. J Biol Chem 278, 36373–36379.CrossRefGoogle ScholarPubMed
Palmer, CS, Osellame, LD, Laine, D, et al. (2011) MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep 12, 565–573.CrossRefGoogle ScholarPubMed
Losón, OC, Song, Z, Chen, H, et al. (2013) Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol Biol Cell 24, 659–667.CrossRefGoogle ScholarPubMed
Nasrallah, CM & Horvath, TL (2014) Mitochondrial dynamics in the central regulation of metabolism. Nat Rev Endocrinol 10, 650–658.CrossRefGoogle ScholarPubMed
Molina, AJA, Wikstrom, JD, Stiles, L, et al. (2009) Mitochondrial networking protects beta-cells from nutrient-induced apoptosis. Diabetes 58, 2303–2315.CrossRefGoogle ScholarPubMed
Gomes, LC, Di Benedetto, G & Scorrano, L (2011) During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 13, 589–598.CrossRefGoogle ScholarPubMed
Jheng, H-F, Tsai, P-J, Guo, S-M, et al. (2012) Mitochondrial fission contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle. Mol Cell Biol 32, 309–319.CrossRefGoogle ScholarPubMed
Schrepfer, E & Scorrano, L (2016) Mitofusins, from mitochondria to metabolism. Mol Cell 61, 683–694.CrossRefGoogle ScholarPubMed
Mansouri, A, Gattolliat, C-H & Asselah, T (2018) Mitochondrial dysfunction and signaling in chronic liver diseases. Gastroenterology 55, 629–647.CrossRefGoogle Scholar
Peverill, W, Powell, LW & Skoien, R (2014) Evolving concepts in the pathogenesis of NASH: beyond steatosis and inflammation. Int J Mol Sci 15, 8591–8638.CrossRefGoogle ScholarPubMed
Buzzetti, E, Pinzani, M & Tsochatzis, EA (2016) The multiple-hit pathogenesis of non-alcoholic fatty liver disease (NAFLD). Metabolism 65, 1038–1048.CrossRefGoogle ScholarPubMed
Cusi, K (2009) Role of insulin resistance and lipotoxicity in non-alcoholic steatohepatitis. Clin Liver Dis 13, 545–563.CrossRefGoogle ScholarPubMed
Satapati, S, Kucejova, B, Duarte, JAG, et al. (2016) Mitochondrial metabolism mediates oxidative stress and inflammation in fatty liver. J Clin Invest 125, 4447–4462.CrossRefGoogle Scholar
Rector, RS, Thyfault, JP, Uptergrove, GM, et al. (2010) Mitochondrial dysfunction precedes insulin resistance and hepatic steatosis and contributes to the natural history of non-alcoholic fatty liver disease in an obese rodent model. J Hepatol 52, 727–736.CrossRefGoogle Scholar
Sanyal, AJ, Campbell-Sargent, C, Mirshahi, F, et al. (2001) Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology 120,1183–1192.CrossRefGoogle ScholarPubMed
Koliaki, C, Szendroedi, J, Kaul, K, et al. (2015) Adaptation of hepatic mitochondrial function in humans with non-alcoholic fatty liver is lost in steatohepatitis. Cell Metab 21, 739–746.CrossRefGoogle ScholarPubMed
Liesa, M & Shirihai, OS (2013) Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab 17, 491–506.CrossRefGoogle ScholarPubMed
Westermann, B (2010) Mitochondrial fusion and fission in cell life and death. Nat Rev Mol Cell Biol 11, 872–884.CrossRefGoogle ScholarPubMed
Boudoures, AL, Saben, J, Drury, A, et al. (2017) Obesity-exposed oocytes accumulate and transmit damaged mitochondria due to an inability to activate mitophagy. Dev Biol 426, 126–138.CrossRefGoogle Scholar
Saben, JL, Boudoures, AL, Asghar, Z, et al. (2016) Maternal metabolic syndrome programs mitochondrial dysfunction via germline changes across three generations. Cell Rep 16, 1–8.CrossRefGoogle ScholarPubMed
Cheng, Z & Almeida, FA (2014) Mitochondrial alteration in type 2 diabetes and obesity: an epigenetic link. Cell Cycle 13, 890–897.CrossRefGoogle ScholarPubMed
Lee, J, Kim, Y, Friso, S, et al. (2017) Epigenetics in non-alcoholic fatty liver disease. Mol Aspects Med 54, 78–88.CrossRefGoogle ScholarPubMed
Alfaradhi, MZ, Fernandez-Twinn, DS, Martin-Gronert, MS, et al. (2014) Oxidative stress and altered lipid homeostasis in the programming of offspring fatty liver by maternal obesity. Am J Physiol Regul Integr Comp Physiol 307, R26–R34.CrossRefGoogle ScholarPubMed
Keleher, MR, Zaidi, R, Shah, S, et al. (2018) Maternal high-fat diet associated with altered gene expression, DNA methylation, and obesity risk in mouse offspring. PLoS One 13, e0192606.CrossRefGoogle ScholarPubMed
Burgueño, AL, Cabrerizo, R, Gonzales Mansilla, N, et al (2013). Maternal high-fat intake during pregnancy programs metabolic-syndrome-related phenotypes through liver mitochondrial DNA copy number and transcriptional activity of liver PPARGC1A. J Nutr Biochem 24, 6–13.CrossRefGoogle ScholarPubMed
Borengasser, SJ, Lau, F, Kang, P, et al. (2011) Maternal obesity during gestation impairs fatty acid oxidation and mitochondrial SIRT3 expression in rat offspring at weaning. PLoS One 6, e24068.CrossRefGoogle ScholarPubMed
De Velasco, PC, Chicaybam, G, Ramos-Filho, DM, et al. (2017) Maternal intake of trans-unsaturated or interesterified fatty acids during pregnancy and lactation modifies mitochondrial bioenergetics in the liver of adult offspring in mice. Br J Nutr 118, 41–52.CrossRefGoogle ScholarPubMed
Wankhade, UD, Zhong, Y, Kang, P, et al. (2017) Enhanced offspring predisposition to steatohepatitis with maternal high-fat diet is associated with epigenetic and microbiome alterations. PLoS One. 12, e0175675.CrossRefGoogle ScholarPubMed
Zheng, J, Xiao, X, Zhang, Q, et al. (2014) DNA methylation: the pivotal interaction between early-life nutrition and glucose metabolism in later life. Br J Nutr 112, 1850–1857.CrossRefGoogle ScholarPubMed
Ramaiyan, B & Talahalli, RR (2018) Dietary unsaturated fatty acids modulate maternal dyslipidemia-induced DNA methylation and histone acetylation in placenta and fetal liver in rats. Lipids 53, 581–588.CrossRefGoogle ScholarPubMed
Seki, Y, Suzuki, M, Guo, X, et al. (2017) In utero exposure to a high-fat diet programs hepatic hypermethylation and gene dysregulation and development of metabolic syndrome in male mice. Endocrinology 158, 2860–2872.CrossRefGoogle ScholarPubMed
Zhang, J, Zhang, F, Didelot, X, et al. (2009) Maternal high fat diet during pregnancy and lactation alters hepatic expression of insulin like growth factor-2 and key microRNAs in the adult offspring. BMC Genomics 10, 478.CrossRefGoogle ScholarPubMed
Petropoulos, S, Guillemin, C, Ergaz, Z, et al. (2015) Gestational diabetes alters offspring DNA methylation profiles in human and rat: Identification of key pathways involved in endocrine system disorders, insulin signaling, diabetes signaling, and ILK signaling. Endocrinology 156, 2222e2238.CrossRefGoogle ScholarPubMed
Chen, HC, Chen, YZ, Wang, CH, et al. (2020) The nonalcoholic fatty liver disease-like phenotype and lowered serum VLDL are associated with decreased expression and DNA hypermethylation of hepatic ApoB in male offspring of ApoE deficient mothers fed a with Western diet. J Nutr Biochem 77, 108319.CrossRefGoogle ScholarPubMed
Gutierrez Sanchez, LH, Tomita, K, Guo, Q, et al. (2018) Perinatal nutritional reprogramming of the epigenome promotes subsequent development of nonalcoholic steatohepatitis. Hepatol Commun 2, 1493–1512.CrossRefGoogle ScholarPubMed
Du, JE, You, YA, Kwon, EJ, et al. (2020) Maternal malnutrition affects hepatic metabolism through decreased hepatic taurine levels and changes in HNF4A methylation. Int J Mol Sci 21, 9060.CrossRefGoogle ScholarPubMed
Vo, TX, Revesz, A, Sohi, G, et al. (2013) Maternal protein restriction leads to enhanced hepatic gluconeogenic gene expression in adult male rat offspring due to impaired expression of the liver X receptor. J Endocrinol 218, 85–97.CrossRefGoogle ScholarPubMed
Sohi, G, Marchand, K, Revesz, A, et al. (2011) Maternal protein restriction elevates cholesterol in adult rat offspring due to repressive changes in histone modifications at the cholesterol 7α-hydroxylase promoter. Mol Endocrinol 25, 785–798.CrossRefGoogle ScholarPubMed
Suter, MA, Chen, A, Burdine, MS, et al. (2012) A maternal high-fat diet modulates fetal SIRT1 histone and protein deacetylase activity in nonhuman primates. FASEB J 26, 5106–5114.CrossRefGoogle ScholarPubMed
Puppala, S, Li, C, Glenn, JP, et al. (2018) Primate fetal hepatic responses to maternal obesity: epigenetic signalling pathways and lipid accumulation. J Physiol 596, 5823–5837.CrossRefGoogle ScholarPubMed
Burger, GCE, Drummond, JC & Sandstead, HR (1948) Malnutrition and Starvation in Western Netherlands, September 1944 July 1945 parts I and 11. ‘s-Gravenhage: Staatsuit to geverij.Google Scholar
Roseboom, T, de Rooij, S & Painter, R (2006) The Dutch famine and its long-term consequences for adult health. Early Hum Dev 82, 485–491.CrossRefGoogle ScholarPubMed
Lumey, LH (1992) Decreased birthweights in infants after maternal in utero exposure to the Dutch famine of 1944–1945. Paediatr Perinat Epidemiol 6, 240–253.CrossRefGoogle Scholar
Ravelli, GP, Stein, ZA & Susser, MW (1976) Obesity in young men after famine exposure in utero and early infancy. N Engl J Med 295, 349–353.CrossRefGoogle ScholarPubMed
Wang, N, Chen, Y, Ning, Z, et al. (2016) Exposure to famine in early life and non-alcoholic fatty liver disease in adulthood. J Clin Endocrinol Metab 101, 2218–2225.CrossRefGoogle ScholarPubMed
Qi, H, Hu, C, Wang, S, et al. (2020) Early life famine exposure, adulthood obesity patterns and the risk of nonalcoholic fatty liver disease. Liver Int 40, 2694–2705.CrossRefGoogle ScholarPubMed
Wang, B, Cheng, J, Wan, H, et al. (2021) Early-life exposure to the Chinese famine, genetic susceptibility and the risk of type 2 diabetes in adulthood. Diabetologia 64, 1766–1774.CrossRefGoogle Scholar
Liu, D, Yu, DM, Zhao, LY, et al. (2019) Exposure to famine during early life and abdominal obesity in adulthood: Findings from the Great Chinese Famine During 1959–1961. Nutrients 11, 903.CrossRefGoogle ScholarPubMed
Li, Y, Jaddoe, VW, Qi, L, et al. (2011) Exposure to the Chinese Famine in early life and the risk of metabolic syndrome in adulthood. Diabetes Care 34, 1014–1018.CrossRefGoogle Scholar
Heijmans, BT, Tobi, EW, Stein, AD, et al. (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A 105, 17046–17049.CrossRefGoogle ScholarPubMed
Saini, SK, Mangalhara, KC, Prakasam, G, et al. (2017) DNA Methyltransferase1 (DNMT1) Isoform3 methylates mitochondrial genome and modulates its biology. Sci Rep 7, 1525.CrossRefGoogle ScholarPubMed
Mposhi, A, Van der Wijst, MG, Faber, KN, et al. (2017) Regulation of mitochondrial gene expression, the epigenetic enigma. Front Biosci (Landmark Ed) 22, 1099–1113.Google ScholarPubMed
Sharma, N, Pasala, MS & Prakash, A (2019) Mitochondrial DNA: epigenetics and environment. Environ Mol Mutagen 60, 668–682.CrossRefGoogle ScholarPubMed
Jang, HS, Shin, WJ, Lee, JE, et al. (2017) CpG and non-CpG methylation in epigenetic gene regulation and brain function. Genes (Basel) 8, 148.CrossRefGoogle ScholarPubMed
Oestreich, AK & Moley, KH (2017) Developmental and transmittable origins of obesity-associated health disorders. Trends Genet 33, 399–407.CrossRefGoogle ScholarPubMed
Bellizzi, D, D’Aquila, P, Scafone, T, et al. (2013) The control region of mitochondrial DNA shows an unusual CpG and non-CpG methylation pattern. DNA Res 20, 537–547.CrossRefGoogle ScholarPubMed
Koh, CWQ, Goh, YT, Toh, JDW, et al. (2018) Single-nucleotide-resolution sequencing of human N6-methyldeoxyadenosine reveals strand-asymmetric clusters associated with SSBP1 on the mitochondrial genome. Nucleic Acids Res 46, 11659–11670.CrossRefGoogle ScholarPubMed
Jia, Y, Li, R, Cong, R, et al. (2013) Maternal low-protein diet affects epigenetic regulation of hepatic mitochondrial DNA transcription in a sex-specific manner in newborn piglets associated with GR binding to its promoter. PLoS One 8, e63855.CrossRefGoogle Scholar
Nicholls, TJ & Gustafsson, CM (2018). Separating and segregating the human mitochondrial genome. Trends Biochem Sci 43, 869–881.CrossRefGoogle ScholarPubMed
King, GA, Hashemi Shabestari, M, Taris, K-KH, et al. (2018) Acetylation and phosphorylation of human TFAM regulate TFAM–DNA interactions via contrasting mechanisms. Nucleic Acids Res 46, 3633–3642.CrossRefGoogle ScholarPubMed
Lu, B, Lee, J, Nie, X, et al. (2013) Phosphorylation of human TFAM in mitochondria impairs DNA binding and promotes degradation by the AAA+ Lon protease. Mol Cell 49, 121–132.CrossRefGoogle ScholarPubMed
Dong, Z, Pu, L & Cui, H. (2020) Mitoepigenetics and its emerging roles in cancer. Front Cell Dev Biol 8, 4.CrossRefGoogle ScholarPubMed
Mercer, TR, Neph, S, Dinger, ME, et al. (2011) The human mitochondrial transcriptome. Cell 146, 645–58.CrossRefGoogle ScholarPubMed
Zhao, Y, Sun, L, Wang, RR, et al. (2018) The effects of mitochondria-associated long noncoding RNAs in cancer mitochondria: new players in an old arena. Crit Rev Oncol Hematol 131, 76–82.CrossRefGoogle Scholar
Wang, K, Gan, T-Y, Li, N, et al. (2017) Circular RNA mediates cardiomyocyte death via miRNA-dependent upregulation of MTP18 expression. Cell Death Differ 24, 1111–1120.CrossRefGoogle ScholarPubMed
Villota, C, Campos, A, Vidaurre, S, et al. (2012) Expression of mitochondrial non-coding RNAs (ncRNAs) is modulated by high risk human papillomavirus (HPV) oncogenes. J Biol Chem 287, 21303–21315.CrossRefGoogle ScholarPubMed