Epigenetic mechanisms and posttranslational modifications in systemic Lupus Erythematosus

The complex physiology of eukaryotic cells is regulated through numerous mechanisms, including epigenetic changes and posttranslational modifications. The wide-ranging diversity of these mechanisms constitutes a way of dynamic regulation of the functionality of proteins, their activity, and their su...

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Autores:
Navarro Quiroz, Elkin
Chavez-Estrada, Valeria
Macias-Ochoa, Karime
Ayala-Navarro, María Fernanda
Flores-Aguilar, Aniyensy Sarai
Morales-Navarrete, Francisco
De la Cruz Lopez, Fernando
Gomez Escorcia, Lorena
G. Musso, Carlos
Aroca Martinez, Gustavo
Gonzales Torres, Henry
Diaz Perez, Anderson
Cadena Bonfanti, Andres
Sarmiento Gutierrez, Joany
Meza, Jainy
Diaz Arroyo, Esperanza
Bello Lemus, Yesit
Ahmad, Mostapha
Navarro Quiroz, Roberto
Tipo de recurso:
Fecha de publicación:
2019
Institución:
Universidad Simón Bolívar
Repositorio:
Repositorio Digital USB
Idioma:
eng
OAI Identifier:
oai:bonga.unisimon.edu.co:20.500.12442/4335
Acceso en línea:
https://hdl.handle.net/20.500.12442/4335
Palabra clave:
Posttranslational modifications
Epigenetic mechanisms
Systemic lupus erythematosus
Ubiquitination
SUMOylation
Glycosylation
Hydroxylation
Phosphorylation
Sulfation
Acetylation
Rights
License
Attribution-NonCommercial-NoDerivatives 4.0 Internacional
id USIMONBOL2_b8aeec2f16f6204ad32d2ed225e4d777
oai_identifier_str oai:bonga.unisimon.edu.co:20.500.12442/4335
network_acronym_str USIMONBOL2
network_name_str Repositorio Digital USB
repository_id_str
dc.title.eng.fl_str_mv Epigenetic mechanisms and posttranslational modifications in systemic Lupus Erythematosus
title Epigenetic mechanisms and posttranslational modifications in systemic Lupus Erythematosus
spellingShingle Epigenetic mechanisms and posttranslational modifications in systemic Lupus Erythematosus
Posttranslational modifications
Epigenetic mechanisms
Systemic lupus erythematosus
Ubiquitination
SUMOylation
Glycosylation
Hydroxylation
Phosphorylation
Sulfation
Acetylation
title_short Epigenetic mechanisms and posttranslational modifications in systemic Lupus Erythematosus
title_full Epigenetic mechanisms and posttranslational modifications in systemic Lupus Erythematosus
title_fullStr Epigenetic mechanisms and posttranslational modifications in systemic Lupus Erythematosus
title_full_unstemmed Epigenetic mechanisms and posttranslational modifications in systemic Lupus Erythematosus
title_sort Epigenetic mechanisms and posttranslational modifications in systemic Lupus Erythematosus
dc.creator.fl_str_mv Navarro Quiroz, Elkin
Chavez-Estrada, Valeria
Macias-Ochoa, Karime
Ayala-Navarro, María Fernanda
Flores-Aguilar, Aniyensy Sarai
Morales-Navarrete, Francisco
De la Cruz Lopez, Fernando
Gomez Escorcia, Lorena
G. Musso, Carlos
Aroca Martinez, Gustavo
Gonzales Torres, Henry
Diaz Perez, Anderson
Cadena Bonfanti, Andres
Sarmiento Gutierrez, Joany
Meza, Jainy
Diaz Arroyo, Esperanza
Bello Lemus, Yesit
Ahmad, Mostapha
Navarro Quiroz, Roberto
dc.contributor.author.none.fl_str_mv Navarro Quiroz, Elkin
Chavez-Estrada, Valeria
Macias-Ochoa, Karime
Ayala-Navarro, María Fernanda
Flores-Aguilar, Aniyensy Sarai
Morales-Navarrete, Francisco
De la Cruz Lopez, Fernando
Gomez Escorcia, Lorena
G. Musso, Carlos
Aroca Martinez, Gustavo
Gonzales Torres, Henry
Diaz Perez, Anderson
Cadena Bonfanti, Andres
Sarmiento Gutierrez, Joany
Meza, Jainy
Diaz Arroyo, Esperanza
Bello Lemus, Yesit
Ahmad, Mostapha
Navarro Quiroz, Roberto
dc.subject.eng.fl_str_mv Posttranslational modifications
Epigenetic mechanisms
Systemic lupus erythematosus
Ubiquitination
SUMOylation
Glycosylation
Hydroxylation
Phosphorylation
Sulfation
Acetylation
topic Posttranslational modifications
Epigenetic mechanisms
Systemic lupus erythematosus
Ubiquitination
SUMOylation
Glycosylation
Hydroxylation
Phosphorylation
Sulfation
Acetylation
description The complex physiology of eukaryotic cells is regulated through numerous mechanisms, including epigenetic changes and posttranslational modifications. The wide-ranging diversity of these mechanisms constitutes a way of dynamic regulation of the functionality of proteins, their activity, and their subcellular localization as well as modulation of the di erential expression of genes in response to external and internal stimuli that allow an organism to respond or adapt to accordingly. However, alterations in these mechanisms have been evidenced in several autoimmune diseases, including systemic lupus erythematosus (SLE). The present review aims to provide an approach to the current knowledge of the implications of these mechanisms in SLE pathophysiology.
publishDate 2019
dc.date.accessioned.none.fl_str_mv 2019-11-13T22:11:08Z
dc.date.available.none.fl_str_mv 2019-11-13T22:11:08Z
dc.date.issued.none.fl_str_mv 2019
dc.type.eng.fl_str_mv article
dc.type.coar.fl_str_mv http://purl.org/coar/resource_type/c_6501
dc.identifier.issn.none.fl_str_mv 14220067
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12442/4335
identifier_str_mv 14220067
url https://hdl.handle.net/20.500.12442/4335
dc.language.iso.eng.fl_str_mv eng
language eng
dc.rights.*.fl_str_mv Attribution-NonCommercial-NoDerivatives 4.0 Internacional
dc.rights.coar.fl_str_mv http://purl.org/coar/access_right/c_abf2
dc.rights.uri.*.fl_str_mv http://creativecommons.org/licenses/by-nc-nd/4.0/
rights_invalid_str_mv Attribution-NonCommercial-NoDerivatives 4.0 Internacional
http://creativecommons.org/licenses/by-nc-nd/4.0/
http://purl.org/coar/access_right/c_abf2
dc.publisher.eng.fl_str_mv Multidisciplinary Digital Publishing Institute (MDPI)
dc.source.eng.fl_str_mv International Journal of Molecular Sciences
dc.source.spa.fl_str_mv Vol. 20, No. 22 (2019)
institution Universidad Simón Bolívar
dc.source.uri.spa.fl_str_mv https://doi.org/10.3390/ijms20225679
dc.source.bibliographicCitation.eng.fl_str_mv Wu, H.; Zhao, M.; Tan, L.; Lu, Q. The key culprit in the pathogenesis of systemic lupus erythematosus: Aberrant DNA methylation. Autoimmun. Rev. 2016, 15, 684–689.
Rhodes, B.; Vyse, T.J. The genetics of SLE: An update in the light of genome-wide association studies. Rheumatology (Oxford) 2008, 47, 1603–1611.
Quddus, J.; Johnson, K.J.; Gavalchin, J.; Amento, E.P.; Chrisp, C.E.; Yung, R.L.; Richardson, B.C. Treating activated CD4+ T cells with either of two distinct DNA methyltransferase inhibitors, 5-azacytidine or procainamide, is su cient to cause a lupus-like disease in syngeneic mice. J. Clin. Invest. 1993, 92, 38–53.
Coit, P.; Yalavarthi, S.; Ognenovski, M.; Zhao, W.; Hasni, S.; Wren, J.D.; Kaplan, M.J.; Sawalha, A.H. Epigenome profiling reveals significantDNAdemethylation of interferon signature genes in lupus neutrophils. J. Autoimmun. 2015, 58, 59–66.
Javierre, B.M.; Richardson, B. A New Epigenetic Challenge: Systemic Lupus Erythematosus. In Epigenetic Contributions in Autoimmune Disease. Advances in Experimental Medicine and Biology; Ballestar, E., Ed.; Springer: Boston, MA, USA, 2011; Volume 711, pp. 117–136.
Zhao, M.; Zhou, Y.; Zhu, B.;Wan, M.; Jiang, T.; Tan, Q.; Liu, Y.; Jiang, J.; Luo, S.; Tan, Y.; et al. IFI44L promoter methylation as a blood biomarker for systemic lupus erythematosus. Ann. Rheum. Dis. 2016, 75, 1998–2006.
Cai, L.; Sutter, B.M.; Li, B.; Tu, B.P. Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol. Cell 2011, 42, 426–437.
Brooks, W.H.; Le Dantec, C.; Pers, J.O.; Youinou, P.; Renaudineau, Y. Epigenetics and autoimmunity. J. Autoimmun. 2010, 34, J207–J219.
Patel, D.R.; Richardson, B.C. Epigenetic mechanisms in lupus. Curr. Opin. Rheumatol. 2010, 22, 478–482.
Zouali, M. Epigenetics in lupus. Ann. N. Y. Acad. Sci. 2011, 1217, 154–165.
Coit, P.; Je ries, M.; Altorok, N.; Dozmorov, M.G.; Koelsch, K.A.; Wren, J.D.; Merrill, J.T.; McCune, W.J.; Sawalha, A.H. Genome-wide DNA methylation study suggests epigenetic accessibility and transcriptional poising of interferon-regulated genes in naive CD4+ T cells from lupus patients. J. Autoimmun. 2013, 43, 78–84.
Pieterse, E.; Hofstra, J.; Berden, J.; Herrmann, M.; Dieker, J.; van der Vlag, J. Acetylated histones contribute to the immunostimulatory potential of neutrophil extracellular traps in systemic lupus erythematosus. Clin. Exp. Immunol. 2015, 179, 68–74.
Sujashvili, R. Advantages of Extracellular Ubiquitin in Modulation of Immune Responses. Mediators Inflamm. 2016, 2016, 1–6.
Téllez Castillo, N.; Siachoque Jara, J.J.; Siachoque Jara, J.S.; Siachoque Jara, M.A.; Siachoque Montañez, H.O. Activación de la célula T, alteraciones en el lupus eritematoso sistémico, una revisión narrativa. Rev. Colomb. Reumatol. 2018, 25, 38–54.
Barrera-Vargas, A.; Gómez-Martín, D.; Carmona-Rivera, C.; Merayo-Chalico, J.; Torres-Ruiz, J.; Manna, Z.; Hasni, S.; Alcocer-Varela, J.; Kaplan, M.J. Differential ubiquitination in NETs regulates macrophage responses in systemic lupus erythematosus. Ann. Rheum. Dis. 2018, 77, 944–950.
Nakasone, M.A.; Livnat-Levanon, N.; Glickman, M.H.; Cohen, R.E.; Fushman, D. Mixed-linkage ubiquitin chains send mixed messages. Structure 2013, 21, 727–740.
Erpapazoglou, Z.; Walker, O.; Haguenauer-Tsapis, R. Versatile roles of k63-linked ubiquitin chains in traffcking. Cells 2014, 3, 1027–1088.
Saavedra Hernández, D. La molécula CD28 y su función en la activación de células T. Rev. Cuba. Hematol. Inmunol. Hemoter. 2013, 29, 359–367.
Ding, X.; Wang, A.; Ma, X.; Demarque, M.; Jin, W.; Xin, H.; Dejean, A.; Dong, C. Protein SUMOylation Is Required for Regulatory T Cell Expansion and Function. Cell Rep. 2016, 16, 1055–1066.
Rider, V.; Abdou, N.I.; Kimler, B.F.; Lu, N.; Brown, S.; Fridley, B.L. Gender bias in human systemic lupus erythematosus: A problem of steroid receptor action? Front. Immunol. 2018, 9, 1–10.
Barry, R.; John, S.W.; Liccardi, G.; Tenev, T.; Jaco, I.; Chen, C.H.; Choi, J.; Kasperkiewicz, P.; Fernandes-Alnemri, T.; Alnemri, E.; et al. SUMO-mediated regulation of NLRP3 modulates inflammasome activity. Nat. Commun. 2018, 9, 3001.
Hernández, A.S. Células colaboradoras (TH1, TH2, TH17) y reguladoras (Treg, TH3, NKT) en la artritis reumatoide. Reumatol. Clin. Supl. 2009, 5 (Suppl. 1), 1–5.
Crabtree, G.R.; Schreiber, S.L. Snapshot: Calcium-calcineurin-NFAT signaling. Cell 2010, 138, 1–4.
Biermann, M.H.; Gri ante, G.; Podolska, M.J.; Boeltz, S.; Stürmer, J.; Muñoz, L.E.; Bilyy, R.; Herrmann, M. Sweet but dangerous–The role of immunoglobulin G glycosylation in autoimmunity and inflammation. Lupus 2016, 25, 934–942.
Magnelli, P.E.; Bielik, A.M.; Guthrie, E.P. Identification and characterization of protein glycosylation using specific endo- and exoglycosidases. J. Vis. Exp. 2011, e3749.
Valliere-Douglass, J.F.; Kodama, P.; Mujacic, M.; Brady, L.J.; Wang, W.; Wallace, A.; Yan, B.; Reddy, P.; Treuheit, M.J.; Balland, A. Asparagine-linked oligosaccharides present on a non-consensus amino acid sequence in the CH1 domain of human antibodies. J. Biol. Chem. 2009, 284, 32493–32506.
Hashii, N.; Kawasaki, N.; Itoh, S.; Nakajima, Y.; Kawanishi, T.; Yamaguchi, T. Alteration of N-glycosylation in the kidney in a mouse model of systemic lupus erythematosus: Relative quantification of N-glycans using an isotope-tagging method. Immunology 2009, 126, 336–345.
Vidarsson, G.; Dekkers, G.; Rispens, T. IgG subclasses and allotypes: From structure to effector functions. Front. Immunol. 2014, 5, 520.
Abès, R.; Teillaud, J.-L. Impact of Glycosylation on Effector Functions of Therapeutic IgG. Pharmaceuticals 2010, 3, 146–157.
Jennewein, M.F.; Alter, G. The Immunoregulatory Roles of Antibody Glycosylation. Trends Immunol. 2017, 38, 358–372.
Reily, C.; Stewart, T.J.; Renfrow, M.B.; Novak, J. Glycosylation in health and disease. Nat. Rev. Nephrol. 2019, 15, 346–366.
Anthony, R.M.; Ravetch, J.V. A Novel Role for the IgG Fc Glycan: The Anti-inflammatory Activity of Sialylated IgG Fcs. J. Clin. Immunol. 2010, 30, 9–14.
Saxena, A.; Wu, D. Advances in Therapeutic Fc Engineering - Modulation of IgG-Associated Effector Functions and Serum Half-life. Front. Immunol. 2016, 7, 580.
Leong, K.W.; Ding, J.L. The unexplored roles of human serum IgA. DNA Cell Biol. 2014, 33, 823–829.
Papista, C.; Berthelot, L.; Monteiro, R.C. Dysfunctions of the Iga system: A common link between intestinal and renal diseases. Cell. Mol. Immunol. 2011, 8, 126–134.
Kawa, I.A.; Masood, A.; Amin, S.; Mustafa, M.F.; Rashid, F. Chapter 2—Clinical Perspective of Posttranslational Modifications. In Protein Modificomics; Dar, T.A., Singh, L.R., Eds.; Academic Press: London, UK, 2019; pp. 37–68.
Zurlo, G.; Guo, J.; Takada, M.;Wei,W.; Zhang, Q. New Insights into Protein Hydroxylation and Its Important Role in Human Diseases. Biochim. Biophys. Acta 2016, 1866, 208–220.
Mansoor, F.; Ali, A.; Ali, R. Binding of circulating SLE autoantibodies to oxygen free radical damage chromatin. Autoimmunity 2005, 38, 431–438.
Lahita, R.G.; Bradlow, L.; Fishman, J.; Kunkel, H.G. Estrogen metabolism in systemic lupus erythematosus. Patients and family members. Arthritis Rheum. 1982, 25, 843–846.
Garg, D.K.; Ali, R. Reactive oxygen species modified polyguanylic acid: Immunogenicity and implications for systemic autoimmunity. J. Autoimmun. 1998, 11, 371–378.
Ardito, F.; Giuliani, M.; Perrone, D.; Troiano, G.; Lo Muzio, L. The crucial role of protein phosphorylation in cell signalingand its use as targeted therapy (Review). Int. J. Mol. Med. 2017, 40, 271–280.
Skourti-Stathaki, K.; Proudfoot, N. Histone 3 S10 Phosphorylation: ‘Caught in the R Loop!’. Mol. Cell 2013, 52, 470–472.
Eichten, S.R.; Schmit, R.J.; Springer, N.M. Epigenetics: Beyond chromatin modifications and complex genetic regulation. Plant Physiol. 2014, 165, 933–947.
Rossetto, D.; Avvakumov, N.; Côté, J. Histone phosphorylation. Epigenetics 2012, 7, 1098–1108.
Rossy, J.; Williamson, D.J.; Gaus, K. How does the kinase Lck phosphorylate the T cell receptor? Spatial organization as a regulatory mechanism. Front. Immunol. 2012, 3, 1–6.
Wu, T.; Xie, C.; Han, J.; Ye, Y.;Weiel, J.; Li, Q.; Blanco, I.; Ahn, C.; Olsen, N.; Putterman, C.; et al. Metabolic disturbances associated with systemic lupus erythematosus. PLoS ONE 2012, 7, e37210.
Hsu, W.; Rosenquist, G.L.; Ansari, A.A.; Gershwin, M.E. Autoimmunity and tyrosine sulfation. Autoimmun. Rev. 2005, 4, 429–435.
Tonks, N.K. Protein tyrosine phosphatases: From genes, to function, to disease. Nat. Rev. Mol. Cell Biol. 2006, 7, 833–834.
Kehoe, J.W.; Bertozzi, C.R. Tyrosine sulfation: A modulator of extracellular protein-protein interactions. Chem. Biol. 2000, 7, 57–61.
Seibert, C.; Sakmar, T.P. Toward a framework for sulfoproteomics: Synthesis and characterization of sulfotyrosine-containing peptides. Biopolym. 2008, 90, 459–477.
Farzan, M.; Mirzabekov, T.; Kolchinsky, P.;Wyatt, R.; Cayabyab, M.; Gerard, N.P.; Gerard, C.; Sodroski, J.; Choe, H. Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 1999, 96, 667–676.
Carvalho, C.; Calvisi, S.L.; Leal, B.; Bettencourt, A.; Marinho, A.; Almeida, I.; Farinha, F.; Costa, P.P.; Silva, B.M.; Vasconcelos, C. CCR5-Delta32: Implications in SLE development. Int. J. Immunogenet. 2014, 41, 236–241.
Ren, J.; Panther, E.; Liao, X.; Grammer, A.C.; Lipsky, P.E.; Reilly, C.M. The Impact of Protein Acetylation/Deacetylation on Systemic Lupus Erythematosus. Int. J. Mol. Sci. 2018, 19, 4007.
Shahbazian, M.D.; Grunstein, M. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 2007, 76, 75–100.
Cheung,W.L.; Briggs, S.D.; Allis, C.D. Acetylation and chromosomal functions. Curr. Opin. Cell Biol. 2000, 12, 326–333.
Wang, Z.; Chang, C.; Peng, M.; Lu, Q. Translating epigenetics into clinic: Focus on lupus. Clin. Epigenetics 2017, 9, 1–15.
Bannister, A.J.; Kouzarides, T. Regulation of chromatin by histone modifications. Cell Res. 2011, 21, 381–395.
Drazic, A.; Myklebust, L.M.; Ree, R.; Arnesen, T. The world of protein acetylation. Biochim. Biophys. Acta 2016, 1864, 1372–1401. [
Parthun, M.R. Hat1: The emerging cellular roles of a type B histone acetyltransferase. Oncogene 2007, 26, 5319–5328.
Leung, Y.T.; Shi, L.; Maurer, K.; Song, L.; Zhang, Z.; Petri, M.; Sullivan, K.E. Interferon regulatory factor 1 and histone H4 acetylation in systemic lupus erythematosus. Epigenetics 2015, 10, 191–199.
Tsai, K.L.; Liao, C.C.; Chang, Y.S.; Huang, C.W.; Huang, Y.C.; Chen, J.H.; Lin, S.H.; Tai, C.C.; Lin, Y.F.; Lin, C.Y. Low Levels of IgM and IgA Recognizing Acetylated C1-Inhibitor Peptides Are Associated with Systemic Lupus Erythematosus in Taiwanese Women. Molecules 2019, 24, 1645.
Nettis, E.; Colanardi, M.C.; Loria, M.P.; Vacca, A. Acquired C1-inhibitor deficiency in a patient with systemic lupus erythematosus: A case report and review of the literature. Eur. J. Clin. Invest. 2005, 35, 781–784.
Dunn, J.; Simmons, R.; Thabet, S.; Jo, H. The role of epigenetics in the endothelial cell shear stress response and atherosclerosis. Int. J. Biochem. Cell Biol. 2015, 67, 167–176.
Rodríguez-Dorantes, M.; Téllez-Ascencio, N.; Cerbón, M.A.; Lez, M.; Cervantes, A. Metilación del ADN: Un fenómeno epigenético de importancia Médica. Rev. Invest. Clin. 2004, 56, 56–71.
Pedroza Díaz, N.J.; Ortiz Reyes, B.L.; Vásquez Duque, G.M. Protein Biomarkers in Neuropsychiatric Lupus. Rev. Colomb. Reumatol. 2012, 19, 158–171.
Godsell, J.; Rudloff, I.; Kandane-Rathnayake, R.; Hoi, A.; Nold, M.F.; Morand, M.F.; Harris, J. Clinical associations of IL-10 and IL-37 in systemic lupus erythematosus. Sci. Rep. 2016, 6, 1–10.
Lu, Q.; Wu, A.; Richardson, B.C. Demethylation of the same promoter sequence increases CD70 expression in lupus T cells and T cells treated with lupus-inducing drugs. J. Immunol. 2005, 174, 6212–6219.
Richardson, B. Epigenetically Altered T Cells Contribute to Lupus Flares. Cells 2019, 8, 127.
Teruel, M.; Sawalha, A.H. Epigenetic Variability in Systemic Lupus Erythematosus: What We Learned from Genome-Wide DNA Methylation Studies. Curr. Rheumatol. Rep. 2017, 19, 32.
Cheung, P.; Lau, P. Epigenetic Regulation by Histone Methylation and Histone Variants. Mol. Endocrinol. 2005, 19, 563–573.
Mondal, S.; Gong, X.; Zhang, X.; Salinger, A.J.; Zheng, L.; Sen, S.;Weerapana, E.; Zhang, X.; Thompson, P.R. Halogen Bonding Increases the Potency and Isozyme-selectivity of Protein Arginine Deiminase 1 Inhibitors. Angew. Chemie 2019, 58, 12476–12480.
Knuckley, B.; Causey, C.P.; Jones, J.E.; Bhatia, M.; Dreyton, C.J.; Osborne, T.C.; Takahara, H.; Thompson, P.R. Substrate specificity and kinetic studies of PADs 1, 3, and 4 identify potent and selective inhibitors of protein arginine deiminase 3. Biochemistry 2010, 49, 4852–4863.
Nakashima, K.; Hagiwara, T.; Yamada, M. Nuclear localization of peptidylarginine deiminase V and histone deimination in granulocytes. J. Biol. Chem. 2002, 277, 49562–49568.
Kakumanu, P.; Sobel, E.S.; Narain, S.; Li, Y.; Akaogi, J.; Yamasaki, Y.; Segal, M.S.; Hahn, P.C.; Chan, E.K.; Reeves, W.H.; et al. Citrulline dependence of anti-cyclic citrullinated peptide antibodies in systemic lupus erythematosus as a marker of deforming/erosive arthritis. J. Rheumatol. 2009, 36, 2682–2690.
Muller, S.; Radic, M. Citrullinated Autoantigens: From Diagnostic Markers to Pathogenetic Mechanisms. Clin. Rev. Allergy Immunol. 2015, 49, 232–239.
Navarro Quiroz, E.; Navarro Quiroz, R.; Pacheco Lugo, L.; Aroca Martínez, G.; Gómez Escorcia, L.; Gonzalez Torres, H.; Cadena Bonfanti, A.; Marmolejo, M.D.C.; Sanchez, E.; Villarreal Camacho, J.L.; et al. Integrated analysis of microRNA regulation and its interaction with mechanisms of epigenetic regulation in the etiology of systemic lupus erythematosus. PLoS ONE 2019, 14, e0218116.
Kronimus, Y.; Dodel, R.; Galuska, S.P.; Neumann, S. IgG Fc N-glycosylation: Alterations in neurologic diseases and potential therapeutic target? J. Autoimmun. 2019, 96, 14–23.
Gruszewska, E.; Chludzinska, A.; Chrostek, L.; Cylwik, B.; Gindzienska-Sieskiewicz, E.; Szmitkowski, M.; Sierakowski, S. Carbohydrate-deficient transferrin depends on disease activity in rheumatoid arthritis and systemic sclerosis. Scand. J. Rheumatol. 2013, 42, 203–206.
dc.source.bibliographicCitation.spa.fl_str_mv Guzmán-Flores, J.M.; Portales-Pérez, D.P. Mecanismos de supresión de las células T reguladoras (Treg). Gac. Med. Mex. 2013, 149, 630–638.
Pretel, M.; Marquès, l.; España, A. Lupus eritematoso inducido por fármacos. Actas Dermosifiliogr. 2012, 105, 18–30.
Díaz, J.P.; Muñoz Vahos, C.H.; Luján Chavarría, T.P.; Vásquez Duque, G.M.; Ortiz Reyes, B.L. Análisis proteómico del líquido cefalorraquídeo de pacientes con lupus neuropsiquiátrico, un abordaje inicial para la búsqueda de biomarcadores. Rev. Colomb. Reumatol. 2014, 21, 115–124.
Pozo, M.C. Inestabilidad Genética y Cambios en la Cromatina en Mutantes del Complejo THO en Mitosis y Meiosis de Eucariotas Modelo. Ph.D. Thesis, Universidad de Sevilla, Seville, Spain, December 2013.
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spelling Navarro Quiroz, Elkind586f4e1-e86b-4364-8aa2-1b1dc7c1bb5eChavez-Estrada, Valeria0fa20917-3656-4d39-b764-e230b87c3f23Macias-Ochoa, Karimecfd0ffb7-7c26-46f9-b536-3afafde819c8Ayala-Navarro, María Fernandaa5323b93-52fa-4bea-a175-a5ae36002623Flores-Aguilar, Aniyensy Saraia7951ecd-0231-4c61-8f86-fe62bfd6aa6eMorales-Navarrete, Franciscob9998165-74aa-447b-bffb-2a25e94b0dfaDe la Cruz Lopez, Fernandocb80443d-3239-4256-a8ce-56a20aa1f910Gomez Escorcia, Lorena0eda4380-18c9-49b2-b09c-a02809a7d505G. Musso, Carlos1558dfd1-c0d4-4a2e-bf43-38a3a1d8ce11Aroca Martinez, Gustavo85796035-bace-4923-8931-ac7730cbd5e7Gonzales Torres, Henryae3fef95-8048-4806-866b-e710bb79524aDiaz Perez, Anderson0bf078d9-6f60-46ea-a589-3bf4f2263adeCadena Bonfanti, Andres72c24732-5739-4168-87d9-1ab282d7aefeSarmiento Gutierrez, Joany6d46181b-18dc-43b8-9e71-2924cd829789Meza, Jainyc049ac0c-0fa3-4751-ade8-bf5e19119d0fDiaz Arroyo, Esperanza4a7166a2-c17a-40ce-8d95-f47693864d9eBello Lemus, Yesit8e7f3dac-a463-4db6-81e5-6d7249682c3bAhmad, Mostaphab2d96cdf-1f82-497f-8a5a-d0351e1b527fNavarro Quiroz, Roberto1246844f-5707-438a-808b-1f8c2761977e2019-11-13T22:11:08Z2019-11-13T22:11:08Z201914220067https://hdl.handle.net/20.500.12442/4335The complex physiology of eukaryotic cells is regulated through numerous mechanisms, including epigenetic changes and posttranslational modifications. The wide-ranging diversity of these mechanisms constitutes a way of dynamic regulation of the functionality of proteins, their activity, and their subcellular localization as well as modulation of the di erential expression of genes in response to external and internal stimuli that allow an organism to respond or adapt to accordingly. However, alterations in these mechanisms have been evidenced in several autoimmune diseases, including systemic lupus erythematosus (SLE). The present review aims to provide an approach to the current knowledge of the implications of these mechanisms in SLE pathophysiology.engMultidisciplinary Digital Publishing Institute (MDPI)Attribution-NonCommercial-NoDerivatives 4.0 Internacionalhttp://creativecommons.org/licenses/by-nc-nd/4.0/http://purl.org/coar/access_right/c_abf2International Journal of Molecular SciencesVol. 20, No. 22 (2019)https://doi.org/10.3390/ijms20225679Wu, H.; Zhao, M.; Tan, L.; Lu, Q. The key culprit in the pathogenesis of systemic lupus erythematosus: Aberrant DNA methylation. Autoimmun. Rev. 2016, 15, 684–689.Rhodes, B.; Vyse, T.J. The genetics of SLE: An update in the light of genome-wide association studies. Rheumatology (Oxford) 2008, 47, 1603–1611.Quddus, J.; Johnson, K.J.; Gavalchin, J.; Amento, E.P.; Chrisp, C.E.; Yung, R.L.; Richardson, B.C. Treating activated CD4+ T cells with either of two distinct DNA methyltransferase inhibitors, 5-azacytidine or procainamide, is su cient to cause a lupus-like disease in syngeneic mice. J. Clin. Invest. 1993, 92, 38–53.Coit, P.; Yalavarthi, S.; Ognenovski, M.; Zhao, W.; Hasni, S.; Wren, J.D.; Kaplan, M.J.; Sawalha, A.H. Epigenome profiling reveals significantDNAdemethylation of interferon signature genes in lupus neutrophils. J. Autoimmun. 2015, 58, 59–66.Javierre, B.M.; Richardson, B. A New Epigenetic Challenge: Systemic Lupus Erythematosus. In Epigenetic Contributions in Autoimmune Disease. Advances in Experimental Medicine and Biology; Ballestar, E., Ed.; Springer: Boston, MA, USA, 2011; Volume 711, pp. 117–136.Zhao, M.; Zhou, Y.; Zhu, B.;Wan, M.; Jiang, T.; Tan, Q.; Liu, Y.; Jiang, J.; Luo, S.; Tan, Y.; et al. IFI44L promoter methylation as a blood biomarker for systemic lupus erythematosus. Ann. Rheum. Dis. 2016, 75, 1998–2006.Cai, L.; Sutter, B.M.; Li, B.; Tu, B.P. Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol. Cell 2011, 42, 426–437.Brooks, W.H.; Le Dantec, C.; Pers, J.O.; Youinou, P.; Renaudineau, Y. Epigenetics and autoimmunity. J. Autoimmun. 2010, 34, J207–J219.Patel, D.R.; Richardson, B.C. Epigenetic mechanisms in lupus. Curr. Opin. Rheumatol. 2010, 22, 478–482.Zouali, M. Epigenetics in lupus. Ann. N. Y. Acad. Sci. 2011, 1217, 154–165.Coit, P.; Je ries, M.; Altorok, N.; Dozmorov, M.G.; Koelsch, K.A.; Wren, J.D.; Merrill, J.T.; McCune, W.J.; Sawalha, A.H. Genome-wide DNA methylation study suggests epigenetic accessibility and transcriptional poising of interferon-regulated genes in naive CD4+ T cells from lupus patients. J. Autoimmun. 2013, 43, 78–84.Pieterse, E.; Hofstra, J.; Berden, J.; Herrmann, M.; Dieker, J.; van der Vlag, J. Acetylated histones contribute to the immunostimulatory potential of neutrophil extracellular traps in systemic lupus erythematosus. Clin. Exp. Immunol. 2015, 179, 68–74.Sujashvili, R. Advantages of Extracellular Ubiquitin in Modulation of Immune Responses. Mediators Inflamm. 2016, 2016, 1–6.Téllez Castillo, N.; Siachoque Jara, J.J.; Siachoque Jara, J.S.; Siachoque Jara, M.A.; Siachoque Montañez, H.O. Activación de la célula T, alteraciones en el lupus eritematoso sistémico, una revisión narrativa. Rev. Colomb. Reumatol. 2018, 25, 38–54.Barrera-Vargas, A.; Gómez-Martín, D.; Carmona-Rivera, C.; Merayo-Chalico, J.; Torres-Ruiz, J.; Manna, Z.; Hasni, S.; Alcocer-Varela, J.; Kaplan, M.J. Differential ubiquitination in NETs regulates macrophage responses in systemic lupus erythematosus. Ann. Rheum. Dis. 2018, 77, 944–950.Nakasone, M.A.; Livnat-Levanon, N.; Glickman, M.H.; Cohen, R.E.; Fushman, D. Mixed-linkage ubiquitin chains send mixed messages. Structure 2013, 21, 727–740.Erpapazoglou, Z.; Walker, O.; Haguenauer-Tsapis, R. Versatile roles of k63-linked ubiquitin chains in traffcking. Cells 2014, 3, 1027–1088.Saavedra Hernández, D. La molécula CD28 y su función en la activación de células T. Rev. Cuba. Hematol. Inmunol. Hemoter. 2013, 29, 359–367.Ding, X.; Wang, A.; Ma, X.; Demarque, M.; Jin, W.; Xin, H.; Dejean, A.; Dong, C. Protein SUMOylation Is Required for Regulatory T Cell Expansion and Function. Cell Rep. 2016, 16, 1055–1066.Rider, V.; Abdou, N.I.; Kimler, B.F.; Lu, N.; Brown, S.; Fridley, B.L. Gender bias in human systemic lupus erythematosus: A problem of steroid receptor action? Front. Immunol. 2018, 9, 1–10.Barry, R.; John, S.W.; Liccardi, G.; Tenev, T.; Jaco, I.; Chen, C.H.; Choi, J.; Kasperkiewicz, P.; Fernandes-Alnemri, T.; Alnemri, E.; et al. SUMO-mediated regulation of NLRP3 modulates inflammasome activity. Nat. Commun. 2018, 9, 3001.Hernández, A.S. Células colaboradoras (TH1, TH2, TH17) y reguladoras (Treg, TH3, NKT) en la artritis reumatoide. Reumatol. Clin. Supl. 2009, 5 (Suppl. 1), 1–5.Crabtree, G.R.; Schreiber, S.L. Snapshot: Calcium-calcineurin-NFAT signaling. Cell 2010, 138, 1–4.Biermann, M.H.; Gri ante, G.; Podolska, M.J.; Boeltz, S.; Stürmer, J.; Muñoz, L.E.; Bilyy, R.; Herrmann, M. Sweet but dangerous–The role of immunoglobulin G glycosylation in autoimmunity and inflammation. Lupus 2016, 25, 934–942.Magnelli, P.E.; Bielik, A.M.; Guthrie, E.P. Identification and characterization of protein glycosylation using specific endo- and exoglycosidases. J. Vis. Exp. 2011, e3749.Valliere-Douglass, J.F.; Kodama, P.; Mujacic, M.; Brady, L.J.; Wang, W.; Wallace, A.; Yan, B.; Reddy, P.; Treuheit, M.J.; Balland, A. Asparagine-linked oligosaccharides present on a non-consensus amino acid sequence in the CH1 domain of human antibodies. J. Biol. Chem. 2009, 284, 32493–32506.Hashii, N.; Kawasaki, N.; Itoh, S.; Nakajima, Y.; Kawanishi, T.; Yamaguchi, T. Alteration of N-glycosylation in the kidney in a mouse model of systemic lupus erythematosus: Relative quantification of N-glycans using an isotope-tagging method. Immunology 2009, 126, 336–345.Vidarsson, G.; Dekkers, G.; Rispens, T. IgG subclasses and allotypes: From structure to effector functions. Front. Immunol. 2014, 5, 520.Abès, R.; Teillaud, J.-L. Impact of Glycosylation on Effector Functions of Therapeutic IgG. Pharmaceuticals 2010, 3, 146–157.Jennewein, M.F.; Alter, G. The Immunoregulatory Roles of Antibody Glycosylation. Trends Immunol. 2017, 38, 358–372.Reily, C.; Stewart, T.J.; Renfrow, M.B.; Novak, J. Glycosylation in health and disease. Nat. Rev. Nephrol. 2019, 15, 346–366.Anthony, R.M.; Ravetch, J.V. A Novel Role for the IgG Fc Glycan: The Anti-inflammatory Activity of Sialylated IgG Fcs. J. Clin. Immunol. 2010, 30, 9–14.Saxena, A.; Wu, D. Advances in Therapeutic Fc Engineering - Modulation of IgG-Associated Effector Functions and Serum Half-life. Front. Immunol. 2016, 7, 580.Leong, K.W.; Ding, J.L. The unexplored roles of human serum IgA. DNA Cell Biol. 2014, 33, 823–829.Papista, C.; Berthelot, L.; Monteiro, R.C. Dysfunctions of the Iga system: A common link between intestinal and renal diseases. Cell. Mol. Immunol. 2011, 8, 126–134.Kawa, I.A.; Masood, A.; Amin, S.; Mustafa, M.F.; Rashid, F. Chapter 2—Clinical Perspective of Posttranslational Modifications. In Protein Modificomics; Dar, T.A., Singh, L.R., Eds.; Academic Press: London, UK, 2019; pp. 37–68.Zurlo, G.; Guo, J.; Takada, M.;Wei,W.; Zhang, Q. New Insights into Protein Hydroxylation and Its Important Role in Human Diseases. Biochim. Biophys. Acta 2016, 1866, 208–220.Mansoor, F.; Ali, A.; Ali, R. Binding of circulating SLE autoantibodies to oxygen free radical damage chromatin. Autoimmunity 2005, 38, 431–438.Lahita, R.G.; Bradlow, L.; Fishman, J.; Kunkel, H.G. Estrogen metabolism in systemic lupus erythematosus. Patients and family members. Arthritis Rheum. 1982, 25, 843–846.Garg, D.K.; Ali, R. Reactive oxygen species modified polyguanylic acid: Immunogenicity and implications for systemic autoimmunity. J. Autoimmun. 1998, 11, 371–378.Ardito, F.; Giuliani, M.; Perrone, D.; Troiano, G.; Lo Muzio, L. The crucial role of protein phosphorylation in cell signalingand its use as targeted therapy (Review). Int. J. Mol. Med. 2017, 40, 271–280.Skourti-Stathaki, K.; Proudfoot, N. Histone 3 S10 Phosphorylation: ‘Caught in the R Loop!’. Mol. Cell 2013, 52, 470–472.Eichten, S.R.; Schmit, R.J.; Springer, N.M. Epigenetics: Beyond chromatin modifications and complex genetic regulation. Plant Physiol. 2014, 165, 933–947.Rossetto, D.; Avvakumov, N.; Côté, J. Histone phosphorylation. Epigenetics 2012, 7, 1098–1108.Rossy, J.; Williamson, D.J.; Gaus, K. How does the kinase Lck phosphorylate the T cell receptor? Spatial organization as a regulatory mechanism. Front. Immunol. 2012, 3, 1–6.Wu, T.; Xie, C.; Han, J.; Ye, Y.;Weiel, J.; Li, Q.; Blanco, I.; Ahn, C.; Olsen, N.; Putterman, C.; et al. Metabolic disturbances associated with systemic lupus erythematosus. PLoS ONE 2012, 7, e37210.Hsu, W.; Rosenquist, G.L.; Ansari, A.A.; Gershwin, M.E. Autoimmunity and tyrosine sulfation. Autoimmun. Rev. 2005, 4, 429–435.Tonks, N.K. Protein tyrosine phosphatases: From genes, to function, to disease. Nat. Rev. Mol. Cell Biol. 2006, 7, 833–834.Kehoe, J.W.; Bertozzi, C.R. Tyrosine sulfation: A modulator of extracellular protein-protein interactions. Chem. Biol. 2000, 7, 57–61.Seibert, C.; Sakmar, T.P. Toward a framework for sulfoproteomics: Synthesis and characterization of sulfotyrosine-containing peptides. Biopolym. 2008, 90, 459–477.Farzan, M.; Mirzabekov, T.; Kolchinsky, P.;Wyatt, R.; Cayabyab, M.; Gerard, N.P.; Gerard, C.; Sodroski, J.; Choe, H. Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 1999, 96, 667–676.Carvalho, C.; Calvisi, S.L.; Leal, B.; Bettencourt, A.; Marinho, A.; Almeida, I.; Farinha, F.; Costa, P.P.; Silva, B.M.; Vasconcelos, C. CCR5-Delta32: Implications in SLE development. Int. J. Immunogenet. 2014, 41, 236–241.Ren, J.; Panther, E.; Liao, X.; Grammer, A.C.; Lipsky, P.E.; Reilly, C.M. The Impact of Protein Acetylation/Deacetylation on Systemic Lupus Erythematosus. Int. J. Mol. Sci. 2018, 19, 4007.Shahbazian, M.D.; Grunstein, M. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 2007, 76, 75–100.Cheung,W.L.; Briggs, S.D.; Allis, C.D. Acetylation and chromosomal functions. Curr. Opin. Cell Biol. 2000, 12, 326–333.Wang, Z.; Chang, C.; Peng, M.; Lu, Q. Translating epigenetics into clinic: Focus on lupus. Clin. Epigenetics 2017, 9, 1–15.Bannister, A.J.; Kouzarides, T. Regulation of chromatin by histone modifications. Cell Res. 2011, 21, 381–395.Drazic, A.; Myklebust, L.M.; Ree, R.; Arnesen, T. The world of protein acetylation. Biochim. Biophys. Acta 2016, 1864, 1372–1401. [Parthun, M.R. Hat1: The emerging cellular roles of a type B histone acetyltransferase. Oncogene 2007, 26, 5319–5328.Leung, Y.T.; Shi, L.; Maurer, K.; Song, L.; Zhang, Z.; Petri, M.; Sullivan, K.E. Interferon regulatory factor 1 and histone H4 acetylation in systemic lupus erythematosus. Epigenetics 2015, 10, 191–199.Tsai, K.L.; Liao, C.C.; Chang, Y.S.; Huang, C.W.; Huang, Y.C.; Chen, J.H.; Lin, S.H.; Tai, C.C.; Lin, Y.F.; Lin, C.Y. Low Levels of IgM and IgA Recognizing Acetylated C1-Inhibitor Peptides Are Associated with Systemic Lupus Erythematosus in Taiwanese Women. Molecules 2019, 24, 1645.Nettis, E.; Colanardi, M.C.; Loria, M.P.; Vacca, A. Acquired C1-inhibitor deficiency in a patient with systemic lupus erythematosus: A case report and review of the literature. Eur. J. Clin. Invest. 2005, 35, 781–784.Dunn, J.; Simmons, R.; Thabet, S.; Jo, H. The role of epigenetics in the endothelial cell shear stress response and atherosclerosis. Int. J. Biochem. Cell Biol. 2015, 67, 167–176.Rodríguez-Dorantes, M.; Téllez-Ascencio, N.; Cerbón, M.A.; Lez, M.; Cervantes, A. Metilación del ADN: Un fenómeno epigenético de importancia Médica. Rev. Invest. Clin. 2004, 56, 56–71.Pedroza Díaz, N.J.; Ortiz Reyes, B.L.; Vásquez Duque, G.M. Protein Biomarkers in Neuropsychiatric Lupus. Rev. Colomb. Reumatol. 2012, 19, 158–171.Godsell, J.; Rudloff, I.; Kandane-Rathnayake, R.; Hoi, A.; Nold, M.F.; Morand, M.F.; Harris, J. Clinical associations of IL-10 and IL-37 in systemic lupus erythematosus. Sci. Rep. 2016, 6, 1–10.Lu, Q.; Wu, A.; Richardson, B.C. Demethylation of the same promoter sequence increases CD70 expression in lupus T cells and T cells treated with lupus-inducing drugs. J. Immunol. 2005, 174, 6212–6219.Richardson, B. Epigenetically Altered T Cells Contribute to Lupus Flares. Cells 2019, 8, 127.Teruel, M.; Sawalha, A.H. Epigenetic Variability in Systemic Lupus Erythematosus: What We Learned from Genome-Wide DNA Methylation Studies. Curr. Rheumatol. Rep. 2017, 19, 32.Cheung, P.; Lau, P. Epigenetic Regulation by Histone Methylation and Histone Variants. Mol. Endocrinol. 2005, 19, 563–573.Mondal, S.; Gong, X.; Zhang, X.; Salinger, A.J.; Zheng, L.; Sen, S.;Weerapana, E.; Zhang, X.; Thompson, P.R. Halogen Bonding Increases the Potency and Isozyme-selectivity of Protein Arginine Deiminase 1 Inhibitors. Angew. Chemie 2019, 58, 12476–12480.Knuckley, B.; Causey, C.P.; Jones, J.E.; Bhatia, M.; Dreyton, C.J.; Osborne, T.C.; Takahara, H.; Thompson, P.R. Substrate specificity and kinetic studies of PADs 1, 3, and 4 identify potent and selective inhibitors of protein arginine deiminase 3. Biochemistry 2010, 49, 4852–4863.Nakashima, K.; Hagiwara, T.; Yamada, M. Nuclear localization of peptidylarginine deiminase V and histone deimination in granulocytes. J. Biol. Chem. 2002, 277, 49562–49568.Kakumanu, P.; Sobel, E.S.; Narain, S.; Li, Y.; Akaogi, J.; Yamasaki, Y.; Segal, M.S.; Hahn, P.C.; Chan, E.K.; Reeves, W.H.; et al. Citrulline dependence of anti-cyclic citrullinated peptide antibodies in systemic lupus erythematosus as a marker of deforming/erosive arthritis. J. Rheumatol. 2009, 36, 2682–2690.Muller, S.; Radic, M. Citrullinated Autoantigens: From Diagnostic Markers to Pathogenetic Mechanisms. Clin. Rev. Allergy Immunol. 2015, 49, 232–239.Navarro Quiroz, E.; Navarro Quiroz, R.; Pacheco Lugo, L.; Aroca Martínez, G.; Gómez Escorcia, L.; Gonzalez Torres, H.; Cadena Bonfanti, A.; Marmolejo, M.D.C.; Sanchez, E.; Villarreal Camacho, J.L.; et al. Integrated analysis of microRNA regulation and its interaction with mechanisms of epigenetic regulation in the etiology of systemic lupus erythematosus. PLoS ONE 2019, 14, e0218116.Kronimus, Y.; Dodel, R.; Galuska, S.P.; Neumann, S. IgG Fc N-glycosylation: Alterations in neurologic diseases and potential therapeutic target? J. Autoimmun. 2019, 96, 14–23.Gruszewska, E.; Chludzinska, A.; Chrostek, L.; Cylwik, B.; Gindzienska-Sieskiewicz, E.; Szmitkowski, M.; Sierakowski, S. Carbohydrate-deficient transferrin depends on disease activity in rheumatoid arthritis and systemic sclerosis. Scand. J. Rheumatol. 2013, 42, 203–206.Guzmán-Flores, J.M.; Portales-Pérez, D.P. Mecanismos de supresión de las células T reguladoras (Treg). Gac. Med. Mex. 2013, 149, 630–638.Pretel, M.; Marquès, l.; España, A. Lupus eritematoso inducido por fármacos. Actas Dermosifiliogr. 2012, 105, 18–30.Díaz, J.P.; Muñoz Vahos, C.H.; Luján Chavarría, T.P.; Vásquez Duque, G.M.; Ortiz Reyes, B.L. Análisis proteómico del líquido cefalorraquídeo de pacientes con lupus neuropsiquiátrico, un abordaje inicial para la búsqueda de biomarcadores. Rev. Colomb. Reumatol. 2014, 21, 115–124.Pozo, M.C. Inestabilidad Genética y Cambios en la Cromatina en Mutantes del Complejo THO en Mitosis y Meiosis de Eucariotas Modelo. Ph.D. Thesis, Universidad de Sevilla, Seville, Spain, December 2013.Posttranslational modificationsEpigenetic mechanismsSystemic lupus erythematosusUbiquitinationSUMOylationGlycosylationHydroxylationPhosphorylationSulfationAcetylationEpigenetic mechanisms and posttranslational modifications in systemic Lupus Erythematosusarticlehttp://purl.org/coar/resource_type/c_6501ORIGINALPDF.pdfPDF.pdfPDFapplication/pdf642813https://bonga.unisimon.edu.co/bitstreams/1f288d5d-aad5-4e3e-ab7c-e5d3c41e1d6d/downloadd207a5378fdd70f6ff0a09245ecdc836MD51CC-LICENSElicense_rdflicense_rdfapplication/rdf+xml; charset=utf-8805https://bonga.unisimon.edu.co/bitstreams/8b9e3a13-10d3-4273-bac8-906552e71cf3/download4460e5956bc1d1639be9ae6146a50347MD52LICENSElicense.txtlicense.txttext/plain; charset=utf-8381https://bonga.unisimon.edu.co/bitstreams/17ab5806-07c2-412c-9ab5-e72f32c1190c/download733bec43a0bf5ade4d97db708e29b185MD53TEXTEpigenetic_Mechanisms.pdf.txtEpigenetic_Mechanisms.pdf.txtExtracted texttext/plain83296https://bonga.unisimon.edu.co/bitstreams/cf91c0b8-8fcf-43bd-bbb6-5956bd4b7877/downloada9c4cfbf65154cb84f653719b3f77019MD54PDF.pdf.txtPDF.pdf.txtExtracted texttext/plain88973https://bonga.unisimon.edu.co/bitstreams/c843a9dd-5231-482e-93df-0facbb883e14/download17d1be2dd3819b0a71ab9cf851468a38MD56THUMBNAILEpigenetic_Mechanisms.pdf.jpgEpigenetic_Mechanisms.pdf.jpgGenerated Thumbnailimage/jpeg19618https://bonga.unisimon.edu.co/bitstreams/63945e09-4f95-4797-9bb5-dad4403d1811/download57cb4df2687556962872a053d0a97cbcMD55PDF.pdf.jpgPDF.pdf.jpgGenerated Thumbnailimage/jpeg5103https://bonga.unisimon.edu.co/bitstreams/83ac15e1-1714-4167-af6d-f3079116caa4/downloadaf44fad428bc2988d2f21d43d521ff36MD5720.500.12442/4335oai:bonga.unisimon.edu.co:20.500.12442/43352024-08-14 21:53:21.399http://creativecommons.org/licenses/by-nc-nd/4.0/Attribution-NonCommercial-NoDerivatives 4.0 Internacionalopen.accesshttps://bonga.unisimon.edu.coRepositorio Digital Universidad Simón Bolívarrepositorio.digital@unisimon.edu.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