Alteration of imprinted genes and offspring organ development caused by environmental factors
Received date: 2021-10-01
Revised date: 2021-12-21
Online published: 2021-12-22
Supported by
Supported by the Key Project of National Key R&D Program of China No(2020YFA0803900)
Imprinted genes are a special subset of about 100 genes, which are mainly expressed in the form of parental monoallelic genes, and play important roles in the growth and development of embryos. In recent years, it has been found that epigenetic modification of imprinted genes induced by environmental factors can cause fetal multi-organ dysplasia and even susceptibility to multiple diseases in adulthood, which also exhibit multi-generational inheritance. In this review, we summarize the effects of expression changes of imprinted genes on ontogenetic development and organ functions in late stage of life, and propose that abnormal epigenetic modification and expression of imprinted genes caused by environmental deleterious factors are important mechanisms for explaining the multi-organ dysplasia in offspring. Such mechanisms are greatly significant for understanding the phenotypic changes caused by alteration of imprinted gene expression during ontogeny and exploring early prevention and treatment strategies of diseases.
Hui Qu, Yi Liu, Yawen Chen, Hui Wang . Alteration of imprinted genes and offspring organ development caused by environmental factors[J]. Hereditas(Beijing), 2022 , 44(2) : 107 -116 . DOI: 10.16288/j.yczz.21-302
| [1] | Zoghbi HY, Beaudet AL. Epigenetics and human disease. Cold Spring Harb Perspect Biol, 2016, 8(2):a019497. |
| [2] | Moon YS, Smas CM, Lee K, Villena JA, Kim KH, Yun EJ, Sul HS. Mice lacking paternally expressed Pref-1/Dlk1 display growth retardation and accelerated adiposity. Mol Cell Biol, 2002, 22(15):5585-5592. |
| [3] | Azzi S, Brioude F, Le Bouc Y, Netchine I. Human imprinting anomalies in fetal and childhood growth disorders: clinical implications and molecular mechanisms. Curr Pharm Des, 2014, 20(11):1751-1763. |
| [4] | Perez JD, Rubinstein ND, Dulac C. New perspectives on genomic imprinting, an essential and multifaceted mode of epigenetic control in the developing and adult brain. Annu Rev Neurosci, 2016, 39:347-384. |
| [5] | Charalambous M, Da Rocha ST, Ferguson-Smith AC. Genomic imprinting, growth control and the allocation of nutritional resources: consequences for postnatal life. Curr Opin Endocrinol Diabetes Obes, 2007, 14(1):3-12. |
| [6] | Wu Y, Feng X, Gao L, Jiao BW. Imprinted genes: important regulators in development. Hereditas (Beijing), 2016, 38(6):508-522. |
| [6] | 吴瑜, 冯旭, 高岚, 焦保卫. 印记基因:发育中的重要调节因子. 遗传, 2016, 38(6):508-522. |
| [7] | Wang L, Zhang J, Duan JL, Gao XX, Zhu W, Lu XY, Yang L, Zhang J, Li GQ, Ci WM, Li W, Zhou Q, Aluru N, Tang FC, He C, Huang XX, Liu J. Programming and inheritance of parental DNA methylomes in mammals. Cell, 2014, 157(7):979-991. |
| [8] | Bartolomei MS, Tilghman SM. Genomic imprinting in mammals. Annu Rev Genet, 1997, 31:493-525. |
| [9] | Leseva M, Knowles BB, Messerschmidt DM, Solter D. Erase-maintain-establish: natural reprogramming of the mammalian epigenome. Cold Spring Harb Symp Quant Biol, 2015, 80:155-163. |
| [10] | Van Otterdijk SD, Michels KB. Transgenerational epigenetic inheritance in mammals: how good is the evidence? FASEB J, 2016, 30(7):2457-2465. |
| [11] | Weaver JR, Susiarjo M, Bartolomei MS. Imprinting and epigenetic changes in the early embryo. Mamm Genome, 2009, 20(9-10):532-543. |
| [12] | Pintican D, Strilciuc Ş, Armean SM, Mihu D. Effects of ethanol, nicotine and caffeine gestational exposure of female rats on lung and brain tissues in fetuses: morphological and biological study. Rom J Morphol Embryol, 2019, 60(2):643-651. |
| [13] | He B, Wen YX, Hu SW, Wang GH, Hu W, Magdalou J, Chen LB, Wang H. Prenatal caffeine exposure induces liver developmental dysfunction in offspring rats. J Endocrinol, 2019, 242(3):211-226. |
| [14] | Niller HH, Minarovits J. Patho-epigenetics of infectious diseases caused by intracellular bacteria. Adv Exp Med Biol, 2016, 879:107-130. |
| [15] | Costa LG, Cole TB, Dao K, Chang YC, Coburn J, Garrick JM. Effects of air pollution on the nervous system and its possible role in neurodevelopmental and neurodegenerative disorders. Pharmacol Ther, 2020, 210:107523. |
| [16] | Kitsiou-Tzeli S, Tzetis M. Maternal epigenetics and fetal and neonatal growth. Curr Opin Endocrinol Diabetes Obes, 2017, 24(1):43-46. |
| [17] | Mani S, Ghosh J, Coutifaris C, Sapienza C, Mainigi M. Epigenetic changes and assisted reproductive technologies. Epigenetics, 2020, 15(1-2):12-25. |
| [18] | Qin JB, Sheng XQ, Wu D, Gao SY, You YP, Yang TB, Wang H. Adverse obstetric outcomes associated with in vitro fertilization in singleton pregnancies. Reprod Sci, 2017, 24(4):595-608. |
| [19] | Chen M, Heilbronn LK. The health outcomes of human offspring conceived by assisted reproductive technologies (ART).[J]Dev Orig Health Dis, 2017, 8(4):388-402. |
| [20] | Pothineni NV, Kovelamudi S, Kantipudi S. Assisted reproductive techniques and cardiovascular risk. J Am Coll Cardiol, 2019, 73(1):117-118. |
| [21] | Heber MF, Ptak GE. The effects of assisted reproduction technologies on metabolic health and disease. Biol Reprod, 2021, 104(4):734-744. |
| [22] | Portha B, Grandjean V, Movassat J. Mother or father: who is in the front line? Mechanisms underlying the non-genomic transmission of obesity/diabetes via the maternal or the paternal line. Nutrients, 2019, 11(2):233. |
| [23] | Potabattula R, Dittrich M, Schorsch M, Hahn T, Haaf T, El Hajj N. Male obesity effects on sperm and next- generation cord blood DNA methylation. PLoS One, 2019, 14(6):e0218615. |
| [24] | Szyf M. DNA methylation, behavior and early life adversity. J Genet Genomics, 2013, 40(7):331-338. |
| [25] | Kim J, Frey WD, He HZ, Kim H, Ekram MB, Bakshi A, Faisal M, Perera BPU, Ye A, Teruyama R. Peg3 mutational effects on reproduction and placenta-specific gene families. PLoS One, 2013, 8(12):e83359. |
| [26] | Lei JZ, Nie Q, Chen DB. A single-cell epigenetic model for paternal psychological stress-induced transgenerational reprogramming in offspring. Biol Reprod, 2018, 98(6):846-855. |
| [27] | O'neill RJ, Vrana PB, Rosenfeld CS. Maternal methyl supplemented diets and effects on offspring health. Front Genet, 2014, 5:289. |
| [28] | Liang F, Diao L, Liu J, Jiang N, Zhang J, Wang HJ, Zhou WH, Huang GY, Ma D. Paternal ethanol exposure and behavioral abnormities in offspring: associated alterations in imprinted gene methylation. Neuropharmacology, 2014, 81:126-133. |
| [29] | Zhang XL, Ji MM, Tan XM, Yu KL, Xu LJ, Chen GY, Yu ZL. Role of epigenetic regulation of Igf2 and H19 in 2,3,7,8- tetrachlorobenzo-p-dioxin (TCDD)-induced ovarian toxicity in offspring rats. Toxicol Lett, 2019, 311:98-104. |
| [30] | Zhu B, Huang XH, Chen DJ, Lu YC, Chen Y, Zhao JY. Methylation changes of H19 gene in sperms of X-irradiated mouse and maintenance in offspring. Biochem Biophys Res Commun, 2006, 340(1):83-89. |
| [31] | De WE, Mak W, Calhoun S, Stein P, Ord T, Krapp C, Coutifaris C, Schultz RM, Bartolomei MS. In vitro culture increases the frequency of stochastic epigenetic errors at imprinted genes in placental tissues from mouse concepti produced through assisted reproductive technologies. Biol Reprod, 2014, 90(2):22. |
| [32] | Yan Z, Li Q, Zhang L, Kang BJ, Fan W, Deng T, Zhu J, Wang Y. The growth and development conditions in mouse offspring derived from ovarian tissue cryopreservation and orthotopic transplantation. J Assist Reprod Genet, 2020, 37(4):923-932. |
| [33] | Nomura Y, John RM, Janssen AB, Davey C, Finik J, Buthmann J, Glover V, Lambertini L. Neurodevelopmental consequences in offspring of mothers with preeclampsia during pregnancy: underlying biological mechanism via imprinting genes. Arch Gynecol Obstet, 2017, 295(6):1319-1329. |
| [34] | Janssen AB, Capron LE, O'donnell K, Tunster SJ, Ramchandani PG, Heazell AEP, Glover V, John RM. Maternal prenatal depression is associated with decreased placental expression of the imprinted gene peg3. Psychol Med, 2016, 46(14):2999-3011. |
| [35] | Ghasemi M, Heidari Nia M, Hashemi M, Keikha N, Fazeli K, Taji O, Naghavi A. An association study of polymorphisms in the H19 imprinted gene in an Iranian population with the risk of polycystic ovary syndrome. Biol Reprod, 2020, 103(5):978-985. |
| [36] | Soubry A, Murphy SK, Wang F, Huang Z, Vidal AC, Fuemmeler BF, Kurtzberg J, Murtha A, Jirtle RL, Schildkraut JM, Hoyo C. Newborns of obese parents have altered DNA methylation patterns at imprinted genes. Int J Obes (Lond), 2015, 39(4):650-657. |
| [37] | Wu L, Lu Y, Jiao Y, Liu B, Li SG, Li Y, Xing FY, Chen DB, Liu X, Zhao JJ, Xiong XL, Gu YY, Lu JL, Chen XJ, Li XY. Paternal psychological stress reprograms hepatic gluconeogenesis in offspring. Cell Metab, 2016, 23(4):735-743. |
| [38] | Charalambous M, Cowley M, Geoghegan F, Smith FM, Radford EJ, Marlow BP, Graham CF, Hurst LD, Ward A. Maternally-inherited Grb10 reduces placental size and efficiency. Dev Biol, 2010, 337(1):1-8. |
| [39] | Wang LX, Balas B, Christ-Roberts CY, Kim RY, Ramos FJ, Kikani CK, Li CL, Deng CX, Reyna S, Musi N, Dong LQ, Defronzo RA, Liu F. Peripheral disruption of the Grb10 gene enhances insulin signaling and sensitivity in vivo. Mol Cell Biol, 2007, 27(18):6497-6505. |
| [40] | Kent LN, Ohboshi S, Soares MJ. Akt1 and insulin-like growth factor 2 (Igf2) regulate placentation and fetal/ postnatal development. Int J Dev Biol, 2012, 56(4):255-261. |
| [41] | Forbes BE, Blyth AJ, Wit JM. Disorders of IGFs and IGF-1R signaling pathways. Mol Cell Endocrinol, 2020, 518:111035. |
| [42] | Cao XY, Hua X, Wang XL, Chen L. Exposure of pregnant mice to triclosan impairs placental development and nutrient transport. Sci Rep, 2017, 7:44803. |
| [43] | Jedynak P, Tost J, Calafat AM, Bourova-Flin E, Busato F, Forhan A, Heude B, Jakobi M, Rousseaux S, Schwartz J, Slama R, Vaiman D, Philippat C, Lepeule J. Pregnancy exposure to synthetic phenols and placental DNA methylation - an epigenome-wide association study in male infants from the EDEN cohort. Environ Pollut, 2021, 290:118024. |
| [44] | Chen XJ, Chen F, Lv PP, Zhang D, Ding GL, Hu XL, Feng C, Sheng JZ, Huang HF. Maternal high estradiol exposure alters CDKN1C and IGF2 expression in human placenta. Placenta, 2018, 61:72-79. |
| [45] | Choux C, Petazzi P, Sanchez-Delgado M, Hernandez Mora JR, Monteagudo A, Sagot P, Monk D, Fauque P. The hypomethylation of imprinted genes in IVF/ICSI placenta samples is associated with concomitant changes in histone modifications. Epigenetics, 2020, 15(12):1386-1395. |
| [46] | Yamamoto Y, Nishikawa Y, Tokairin T, Omori Y, Enomoto K. Increased expression of H19 non-coding mRNA follows hepatocyte proliferation in the rat and mouse. J Hepatol, 2004, 40(5):808-814. |
| [47] | Chang S, Hur SK, Naveh NSS, Thorvaldsen JL, French DL, Gagne AL, Jobaliya CD, Anguera MC, Bartolomei MS, Kalish JM. Derivation and investigation of the first human cell-based model of beckwith-wiedemann syndrome. Epigenetics, 2020: 1-11. |
| [48] | Yoshimura H, Matsuda Y, Yamamoto M, Kamiya S, Ishiwata T. Expression and role of long non-coding RNA H19 in carcinogenesis. Front Biosci Landmark, 2018, 23:614-625. |
| [49] | Deng J, Mueller M, Geng TT, Shen YY, Liu Y, Hou P, Ramillapalli R, Taylor HS, Paidas M, Huang YQ. H19 lncRNA alters methylation and expression of Hnf4α in the liver of metformin-exposed fetuses. Cell Death Dis, 2017, 8(12):e3175. |
| [50] | Nyirenda MJ, Dean S, Lyons V, Chapman KE, Seckl JR. Prenatal programming of hepatocyte nuclear factor 4alpha in the rat: A key mechanism in the 'foetal origins of hyperglycaemia'?. Diabetologia, 2006, 49(6):1412-1420. |
| [51] | Zhu X, Wu YB, Zhou J, Kang DM. Upregulation of lncRNA Meg3 promotes hepatic insulin resistance via increasing FoxO1 expression. Biochem Biophys Res Commun, 2016, 469(2):319-325. |
| [52] | Zhu X, Li HQ, Wu YB, Zhou J, Yang GW, Wang WD. lncRNA MEG3 promotes hepatic insulin resistance by serving as a competing endogenous RNA of miR-214 to regulate ATF4 expression. Int J Mol Med, 2019, 43(1):345-357. |
| [53] | Wu L, Lu Y, Jiao Y, Liu B, Li SG, Li Y, Xing FY, Chen DB, Liu X, Zhao JJ, Xiong XL, Gu YY, Lu JL, Chen XJ, Li XY. Paternal psychological stress reprograms hepatic gluconeogenesis in offspring. Cell Metab, 2016, 23(4):735-743. |
| [54] | Copping NA, Christian SGB, Ritter DJ, Islam MS, Buscher N, Zolkowska D, Pride MC, Berg EL, Lasalle JM, Ellegood J, Lerch JP, Reiter LT, Silverman JL, Dindot SV. Neuronal overexpression of Ube3a isoform 2 causes behavioral impairments and neuroanatomical pathology relevant to 15q11.2-q13.3 duplication syndrome. Hum Mol Genet, 2017, 26(20):3995-4010. |
| [55] | Sun JD, Liu Y, Moreno S, Baudry M, Bi XN. Imbalanced mechanistic target of rapamycin C1 and C2 activity in the cerebellum of angelman syndrome mice impairs motor function. J Neurosci, 2015, 35(11):4706-4718. |
| [56] | Tang GM, Gudsnuk K, Kuo SH, Cotrina ML, Rosoklija G, Sosunov A, Sonders MS, Kanter E, Castagna C, Yamamoto A, Yue ZY, Arancio O, Peterson BS, Champagne F, Dwork AJ. Loss of mTOR-dependent macroautophagy causes autistic-like synaptic pruning deficits. Neuron, 2014, 83(5):1131-1143. |
| [57] | Dunaway KW, Islam MS, Coulson RL, Lopez SJ, Vogel Ciernia A, Chu RG, Yasui DH, Pessah IN, Lott P, Mordaunt C, Meguro-Horike M, Horike SI, Korf I, Lasalle JM. Cumulative impact of polychlorinated biphenyl and large chromosomal duplications on DNA methylation, chromatin, and expression of autism candidate genes. Cell Rep, 2016, 17(11):3035-3048. |
| [58] | Yang Y, Jiang WD, Yang S, Qi FL, Zhao RQ. Transgenerational inheritance of betaine-induced epigenetic alterations in estrogen-responsive IGF-2/IGFBP2 genes in rat hippocampus. Mol Nutr Food Res, 2020, 64(8):e1900823. |
| [59] | Baumgarten SC, Convissar SM, Zamah AM, Fierro MA, Winston NJ, Scoccia B, Stocco C. FSH regulates IGF-2 expression in human granulosa cells in an AKT-dependent manner. J Clin Endocrinol Metab, 2015, 100(8):E1046-E1055. |
| [60] | Zhang XL, Ji MM, Tan XM, Yu KL, Xu LJ, Chen GY, Yu ZL. Role of epigenetic regulation of Igf2 and H19 in 2,3,7,8- tetrachlorobenzo-p-dioxin (TCDD)-induced ovarian toxicity in offspring rats. Toxicol Lett, 2019, 311:98-104. |
| [61] | Song PY, Li DY, Wang XD, Zhong XH. Effects of perfluorooctanoic acid exposure during pregnancy on the reproduction and development of male offspring mice. Andrologia, 2018, 50(8):e13059. |
| [62] | He Z, Zhang JZ, Chen GH, Cao JG, Chen YW, Ai C, Wang H. H19/let-7 axis mediates caffeine exposure during pregnancy induced adrenal dysfunction and its multi- generation inheritance. Sci Total Environ, 2021, 792:148440. |
| [63] | Busada JT, Cidlowski JA. Mechanisms of glucocorticoid action during development. Curr Top Dev Biol, 2017, 125:147-170. |
| [64] | Watkins AJ, Sirovica S, Stokes B, Isaacs M, Addison O, Martin RA. Paternal low protein diet programs preimplantation embryo gene expression, fetal growth and skeletal development in mice. Biochim Biophys Acta Mol Basis Dis, 2017, 1863(6):1371-1381. |
| [65] | Cleaton MA, Dent CL, Howard M, Corish JA, Gutteridge I, Sovio U, Gaccioli F, Takahashi N, Bauer SR, Charnock- Jones DS, Powell TL, Smith GCS, Ferguson-Smith AC, Charalambous M. Fetus-derived DLK1 is required for maternal metabolic adaptations to pregnancy and is associated with fetal growth restriction. Nat Genet, 2016, 48(12):1473-1480. |
| [66] | Traustadottir GÁ, Lagoni LV, Ankerstjerne LBS, Bisgaard HC, Jensen CH, Andersen DC. The imprinted gene delta like non-canonical notch ligand 1 (Dlk1) is conserved in mammals, and serves a growth modulatory role during tissue development and regeneration through notch dependent and independent mechanisms. Cytokine Growth Factor Rev, 2019, 46:17-27. |
| [67] | Charalambous M, Da Rocha ST, Radford EJ, Medina- Gomez G, Curran S, Pinnock SB, Ferron SR, Vidal-Puig A, Ferguson-Smith AC. DLK1/PREF1 regulates nutrient metabolism and protects from steatosis. Proc Natl Acad Sci USA, 2014, 111(45):16088-16093. |
| [68] | Matsuzaki H, Kuramochi D, Okamura E, Hirakawa K, Ushiki A, Tanimoto K. Recapitulation of gametic DNA methylation and its post-fertilization maintenance with reassembled DNA elements at the mouse Igf2/H19 locus. Epigenetics Chromatin, 2020, 13(1):2. |
| [69] | Zhang WP, Yang J, Lv Y, Li SL, Qiang M. Paternal benzo[a]pyrene exposure alters the sperm DNA methylation levels of imprinting genes in F0 generation mice and their unexposed F1-2 male offspring. Chemosphere, 2019, 228:586-594. |
| [70] | Legoff L, Dali O, D'cruz SC, Suglia A, Gely-Pernot A, Hémery C, Kernanec PY, Demmouche A, Kervarrec C, Tevosian S, Multigner L, Smagulova F. Ovarian dysfunction following prenatal exposure to an insecticide, chlordecone, associates with altered epigenetic features. Epigenetics Chromatin, 2019, 12(1):29. |
| [71] | Xu RM, Li C, Liu XY, Gao SR. Insights into epigenetic patterns in mammalian early embryos. Protein Cell, 2021, 12(1):7-28. |
| [72] | Short AK, Fennell KA, Perreau VM, Fox A, O'bryan MK, Kim JH, Bredy TW, Pang TY, Hannan AJ. Elevated paternal glucocorticoid exposure alters the small noncoding RNA profile in sperm and modifies anxiety and depressive phenotypes in the offspring. Transl Psychiatry, 2016, 6(6):e837. |
| [73] | Tammen SA, Friso S, Choi SW. Epigenetics: the link between nature and nurture. Mol Aspects Med, 2013, 34(4):753-764. |
/
| 〈 |
|
〉 |