Abstract
Epigenetic modifications, reversibly controlling gene expression, are crucial for interpreting the genome under the influence of physiological factors. The basic processes (DNA methylation and histone modification, DNA accessibility, and chromatin structure) which characterize epigenetics are regulated by an orchestrated series of events. The spectrum of these events is becoming wider and wider, increasing the complexity of the interplay between the basic processes and the multiple side mechanisms responsive to environmental stimuli. The “histone code hypothesis” suggests that combinations of different histone modifications may regulate chromatin structure and transcriptional activity. Among these modifications, a crucial role is played by poly(ADP-ribosyl)ation, the reaction catalyzed by poly(ADP-ribose)polymerase-1 widely recognized as a “genome guardian” for driving the repair of damaged DNA. Increasing evidence indicates also that alterations in membrane phospholipid composition and lipid metabolism may play a role in epigenetics. Moreover, a “lipid code” has been proposed since in the nucleus a lipid fraction is present that seems tightly bound to DNA.
This review will analyze these topics and their possible interplay in epigenetic regulation and discuss the relative role of nutritional and environmental challenges.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsAbbreviations
- 4-HNE:
-
4-Hydroxynonenale
- ADP-ribose:
-
Adenosine diphosphate ribose
- AMPK:
-
5′-Adenosine monophosphate-activated protein kinase
- COX:
-
Cyclooxygenase
- DHA:
-
Docosahexaenoic acid
- EPA:
-
Eicosapentaenoic acid
- ER:
-
Estrogen receptor
- FASN:
-
Fatty acid synthase
- FOXO1:
-
Forkhead box protein O1
- HDAC:
-
Histone deacetylase
- LOX:
-
Lipoxygenase
- MCF-7:
-
Michigan cancer foundation-7
- mtDNA:
-
Mitochondrial DNA
- mTOR:
-
Mammalian target of rapamycin
- NAD+:
-
Nicotinamide adenine dinucleotide
- ncRNA:
-
Noncoding RNA
- NF-κB:
-
Nuclear factor-κB
- PAR:
-
Poly(ADP-ribose)
- PARP:
-
poly(ADP-ribose)polymerase
- PKCζ:
-
Protein kinase C ζ
- PPAR:
-
Peroxisome proliferator-activating receptor
- PUFA:
-
Polyunsaturated fatty acid
- RAF:
-
Rapidly accelerated fibrosarcoma
- ROS:
-
Reactive oxygen species
- SIRT1:
-
Sirtuin 1
- SREBP:
-
Sterol regulatory element-binding protein
- STAT3:
-
Signal transducer and activator of transcription 3
References
Albi E, Viola Magni MP (2004) The role of intranuclear lipids. Biol Cell 96(8):657–667
Altmeyer M, Hottiger MO (2009) Poly(ADP-ribose) polymerase 1 at the crossroad of metabolic stress and inflammation in aging. Aging (Albany NY) 1(5):458–469
Baenke F, Peck B, Miess H, Schulze A (2013) Hooked on fat: the role of lipid synthesis in cancer metabolism and tumor development. Dis Model Mech 6(6):1353–1363
Bai P, Cantò C (2012) The role of PARP-1 and PARP-2 enzymes in metabolic regulation and disease. Cell Metab 16(3):290–295
Balla T (2016) Cell biology: lipid code for membrane recycling. Nature 529(7586):292–293
Beneke S (2012) Regulation of chromatin structure by poly(ADP-ribosyl)ation. Front Genet 3:169
Beneke S, Bürkle A (2007) Poly(ADP-ribosyl)ation in mammalian aging. Nucl Ac Res 35(22):7456–7465
Bianchi AR, Ferreri C, Ruggiero S, Deplano S et al (2016) Automodification of PARP and fatty acid-based membrane lipidome as a promising integrated biomarker panel in molecular medicine. Biomark Med 10(3):229–242
Bolognesi A, Chatgilialoglu A, Polito L, Ferreri C (2013) Membrane lipidome reorganization correlates with the fate of neuroblastoma cells supplemented with fatty acids. PLoS One 8(2):e55537
Caiafa P (2000–2013) PARP and epigenetic regulation. In: Madame Curie bioscience database. Landes Bioscience, Austin
Calder PC (2001) Polyunsaturated fatty acids, inflammation, and immunity. Lipids 36:1007–1024
Cantó C, Sauve AA, Bai P (2013) Crosstalk between poly(ADP-ribose) polymerase and sirtuin enzymes. Mol Asp Med 34(6). https://doi.org/10.1016/j.mam.2013.01.004
Caron A, Richard D, Laplante M (2015) The roles of mTOR complexes in lipid metabolism. Annu Rev Nutr 35:321–348
Choi SW, Friso S (2010) Epigenetics: a new bridge between nutrition and health. Adv Nutr 1:8–16
Comerford SA, Huang Z, Du X, Wang Y, Cai L, Witkiewicz A et al (2014) Acetate dependence of tumors. Cell 159(7):1591–1602
Davie JR (2003) Inhibition of histone deacetylase activity by Butyrate. J Nutr 133(7):2485S–2493S
Deckelbaum RJ, Worgall TS, Seo T (2006) n-3 fatty acids and gene expression. Am J Clin Nutr 83:1520S–1525S
Erener S, Hesse M, Kostadinova R, Hottiger MO (2012) PARP1 controls adipogenic gene expression and adipocyte function. Mol Endocrinol 26(1):79–86
Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free RadicBiol Med 11:81–128
Faraone Mennella MR (2011) Mammalian spermatogenesis, DNA repair, Poly(ADP-ribose) turnover: the state of the art. In: Storici F (ed) On the pathways to fixing DNA damage and errors. InTech, pp 235–254. https://doi.org/10.5772/23337
Faraone-Mennella MR (2015) A new facet of ADP-ribosylation reactions: SIRTs and PARPs interplay. Front Biosc (Landmark Edition) 20:458–473
Ferreri C, Chatgilialoglu C (2012) Role of fatty acid-based functional lipidomics in the development of molecular diagnostic tools. Expert Rev Mol Diagn 12:767–780
Ferreri C, Chatgilialoglu C (2015) Membrane lipidomics for personalized health. Wiley, New York
Ferreri C, Masi A, Sansone A, Giacometti G, Larocca AV, Menounou G, Scanferlato R, Tortorella S, Rota D, Conti M, Deplano S, Louka M, Maranini AR, Salat A, Sunda V, Chatgilialoglu C (2017) Fatty acids in membranes as homeostatic, metabolic and nutritional biomarkers: recent advancements in analytics and diagnostics. Diagnostics 7:1. https://doi.org/10.3390/diagnostics7010001
Hottiger MO (2015) Nuclear ADP-Ribosylation and its role in chromatin plasticity, cell differentiation, and epigenetics. Annu Rev Biochem 84:227–263
Kaliman P, Parrizas M (2011) Obesity and systemic inflammation: insights into epigenetic mechanisms. In: Croniger C (ed) Role of the adipocyte in development of type 2 diabetes. InTech, pp 65–88. ISBN: 978-953-307-598-3
Kassan M, Choi SK, Galan M, Bishop A, Umezawa K, Trebak M et al (2013) Enhanced NFkappaB activity impairs vascular function through PARP-1, SP-1 and COX2-dependent mechanisms in type 2 diabetes. Diabetes 62(6):2078–2087
Keating ST, El-Osta A (2015) Epigenetics and metabolism. Circ Res 116:715–736
Kiss B, Szántó M, Szklenár M, Brunyánszki A, Marosvölgyi T, Sárosi E et al (2015) Poly(ADP-ribose) polymerase-1 ablation alters eicosanoid and docosanoid signaling and metabolism in a murine model of contact hypersensitivity. Mol Med Rep 11(4):2861–2867
Kristjuhan A, Walker J, Suka N, Grunstein M et al (2002) Transcriptional inhibition of genes with severe histone H3 hypoacetylation in the coding region. Mol Cell 10(4):925–933
Lands WE (1958) Metabolism of glycerolipides; a comparison of lecithin and triglyceride synthesis. J Biol Chem 231:883–888
Lapucci A, Pittelli M, Rapizzi E, Felici R, Moroni F, Chiarugi A (2011) PARP1 is a nuclear epigenetic regulator of mitochondrial DNA repair and transcription. Mol Pharmacol 79:932–940
Latham T, Mackay L, Sproul D, Karim M, Culley J et al (2012) Lactate, a product of glycolytic metabolism, inhibits histone deacetylase activity and promotes changes in gene expression. Nucl Ac Res 40(11):4794–4803
Lazzarini A, Macchiarulo A, Floridi A, Coletti A et al (2015) Very-long-chain fatty acid sphingomyelin in nuclear lipid microdomains of hepatocytes and hepatoma cells: can the exchange from C24:0 to C16:0 affect signal proteins and vitamin D receptor? Mol Biol Cell 26(13):2418–2425
Lichtenberg D, Goñi FM, Heerklotz H (2005) Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem Sci 30(8):430–436
Lopez S, Bermudez B, Montserrat-de la Paz S, Jaramillo S et al (2014) Membrane composition and dynamics: a target of bioactive virgin olive oil constituents. Biochim Biophys Acta Biomembr 1838(6):1638–1656. ISSN 0005-2736
Luo X, Kraus WL (2012) On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev 26(5):417–432
Maraldi NM, Capitani S, Caramelli E, Cocco L et al (1984) Conformational changes of nuclear chromatin related to phospholipid induced modifications of the template availability. Adv Enzym Regul 22:447–464
Mouritsen OG (2005) Life – as a matter of fat. The emerging science of lipidomics. The frontiers collection. Springer, Berlin
Ohanna M, Giuliano S, Bonet C, Imbert V et al (2011) Senescent cells develop a PARP-1 and nuclear factor-κB-associated secretome (PNAS). Genes Dev 25(12):1245–1261
Pégorier JP, Le May C, Girard J (2004) Control of gene expression by fatty acids. J Nutr 134:2444S–2449S
Pfluger PT, Herranz D, Velasco-Miguel S, Serrano M, Tscho MH (2008) Sirt1 protects against high-fat diet-induced metabolic damage. Proc Natl Acad Sci U S A 105(28):9793–9798
Pirrotta V (2003) Transcription. Puffing with PARP. Science 299(5606):528–529
Raghavan V, Vijayaraghavalu S, Peetla C, Yamada M et al (2015) Sustained epigenetic drug delivery depletes cholesterol-sphingomyelin rafts from resistant breast cancer cells, influencing biophysical characteristics of membrane lipids. Langmuir 31(42):11564–11573
Rodríguez-Vargas JM, Ruiz-Magaña MJ, Ruiz-Ruiz C, Majuelos-Melguizo J et al (2012 Jul) ROS-induced DNA damage and PARP-1 are required for optimal induction of starvation-induced autophagy. Cell Res 22(7):1181–1198
Sadli N, Ahmed N, Ackland ML, Sinclair A et al (2011) Effect of zinc and DHA on expression levels and post-translational modifications of histones H3 and H4 in human neuronal cells. In: Dr Chang RCC (ed) Neurodegenerative diseases – processes, prevention, protection and monitoring. InTech, Rijeka, pp 141–164
Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7:517–528
Ventura R, Mordec K, Waszczuk J, Wang Z et al (2015) Inhibition of de novo palmitate synthesis by fatty acid synthase induces apoptosis in tumor cells by remodeling cell membranes, inhibiting signaling pathways, and reprogramming Gene expression. EBio Med 2(8):808–824
Virág L, Szabó C (2002) The therapeutic potential of PARP inhibitors. Pharmacol Rev 54:375–429
Waterland RA, Jirtle RL (2003) Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23(15):5293–5300
Wu X, Dong Z, Wang CJ, Barlow LJ et al (2016) FASN regulates cellular response to genotoxic treatments by increasing PARP-1 expression and DNA repair activity via NF-κB and SP1. Proc Natl Acad Sci U S A 113(45):E6965–EE973
Xu S, Bai P, Little J, Liu P (2014) PARP1 in atherosclerosis: from molecular mechanisms to therapeutic implications. Med Res Rev 34(3):644–675
Zerfaoui M, Errami Y, Naura AS, Suzuki Y et al (2010) PARP1 is a determining factor in Crm1-mediated nuclear export and retention of p65 NF-kappa B upon TLR4 stimulation. J Immunol 185(3):1894–1902
Zhao S, Xu W, Jiang W, Yu W et al (2010) Regulation of cellular metabolism by protein lysine acetylation. Science 327(5968):1000–1004
Zhdanov R, Schirmer EC, Venkatasubramani AV, Kerr ARV et al (2015) Lipids contribute to epigenetic control via chromatin structure and functions. Sci Open Res. https://doi.org/10.14293/S2199-1006.1.SOR-LIFE.AUXYTR.v1
Author information
Authors and Affiliations
Corresponding authors
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this entry
Cite this entry
Faraone-Mennella, M.R., Masi, A., Ferreri, C. (2019). Regulatory Roles of PARP-1 and Lipids in Epigenetic Mechanisms. In: Patel, V., Preedy, V. (eds) Handbook of Nutrition, Diet, and Epigenetics. Springer, Cham. https://doi.org/10.1007/978-3-319-55530-0_37
Download citation
DOI: https://doi.org/10.1007/978-3-319-55530-0_37
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-55529-4
Online ISBN: 978-3-319-55530-0
eBook Packages: MedicineReference Module Medicine