Epigenetic regulation of glycosylation is the quantum mechanics of biology

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 1, 2014, Pages 65-70

  Lauc, Gordan ^a,b   Vojta, Aleksandar ^c   Zoldoš, Vlatka ^c  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b GENOS GLYCOSCIENCE RESEARCH LABORATORY   (Croatia)

^c UNIVERSITY OF ZAGREB   (Croatia)

Author keywords

Adaptation; Epigenetics; Evolution; Glycosylation

Indexed keywords

GLYCOSIDASE; GLYCOSYLTRANSFERASE; PROTEOME;

BIOCHEMICAL COMPOSITION; DNA METHYLATION; EPIGENETICS; GENE; GENE EXPRESSION REGULATION; GENOME ANALYSIS; GLYCOBIOLOGY; GLYCOSIDASE GENE; GLYCOSYLATION; GLYCOSYLTRANSFERASE GENE; HUMAN; LINKAGE ANALYSIS; METABOLOMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; QUANTUM MECHANICS; REVIEW; STRUCTURE ANALYSIS;

EUKARYOTA;

ADAPTATION; EPIGENETICS; EVOLUTION; GLYCOSYLATION;

BIOLOGICAL EVOLUTION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GENES; GLYCOSYLATION; HUMANS; QUANTUM THEORY;

EID: 84884992503     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.08.017     Document Type: Review

References (75)

1. I.H.G.S. Consortium Finishing the euchromatic sequence of the human genome Nature 431 2004 931 945
2. E. Pennisi Genomics. ENCODE project writes eulogy for junk DNA Science 337 2012 1159 1161
3. L.D. Ward, and M. Kellis Evidence of abundant purifying selection in humans for recently acquired regulatory functions Science 337 2012 1675 1678
4. A. Hintze, and C. Adami Evolution of complex modular biological networks PLoS Comput. Biol. 4 2008 e23
5. G.W. Hart, and R.J. Copeland Glycomics hits the big time Cell 143 2010 672 676
6. K.W. Moremen, M. Tiemeyer, and A.V. Nairn Vertebrate protein glycosylation: diversity, synthesis and function Nat. Rev. Mol. Cell Biol. 13 2012 448 462
7. R.T. Lee, G. Lauc, and Y.C. Lee Glycoproteomics: protein modifications for versatile functions EMBO Rep. 6 2005 1018 1022 (Pubitemid 41637644)
8. V. Zoldos, M. Novokmet, I. Beceheli, and G. Lauc Genomics and epigenomics of the human glycome Glycoconj. J. 30 2013 41 50
9. V. Zoldoš, S. Grgurević, and G. Lauc Epigenetic regulation of protein glycosylation Biomol. Concepts 1 2010 253 261
10. K.S. Lau, E.A. Partridge, A. Grigorian, C.I. Silvescu, V.N. Reinhold, M. Demetriou, and J.W. Dennis Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation Cell 129 2007 123 134 (Pubitemid 46507588)
11. A. Hassinen, F.M. Pujol, N. Kokkonen, C. Pieters, M. Kihlstrom, K. Korhonen, and S. Kellokumpu Functional organization of Golgi N- and O-glycosylation pathways involves pH-dependent complex formation that is impaired in cancer cells J. Biol. Chem. 286 2011 38329 38340
12. A. Rivinoja, A. Hassinen, N. Kokkonen, A. Kauppila, and S. Kellokumpu Elevated Golgi pH impairs terminal N-glycosylation by inducing mislocalization of Golgi glycosyltransferases J. Cell. Physiol. 220 2009 144 154
13. J.P. Kunkel, D.C. Jan, J.C. Jamieson, and M. Butler Dissolved oxygen concentration in serum-free continuous culture affects N-linked glycosylation of a monoclonal antibody J. Biotechnol. 62 1998 55 71 (Pubitemid 28403594)
14. K. Ohtsubo, and J.D. Marth Glycosylation in cellular mechanisms of health and disease Cell 126 2006 855 867 (Pubitemid 44310784)
15. G. Lauc, I. Rudan, H. Campbell, and P.M. Rudd Complex Genetic Regulation of Protein Glycosylation Mol. Biosyst. 6 2010 329 335
16. J.E. Huffman, A. Knezevic, V. Vitart, J. Kattla, B. Adamczyk, M. Novokmet, W. Igl, M. Pucic, L. Zgaga, A. Johannson, I. Redzic, O. Gornik, T. Zemunik, O. Polasek, I. Kolcic, M. Pehlic, C.A. Koeleman, S. Campbell, S.H. Wild, N.D. Hastie, H. Campbell, U. Gyllensten, M. Wuhrer, J.F. Wilson, C. Hayward, I. Rudan, P.M. Rudd, A.F. Wright, and G. Lauc Polymorphisms in B3GAT1, SLC9A9 and MGAT5 are associated with variation within the human plasma N-glycome of 3533 European adults Hum. Mol. Genet. 20 2011 5000 5011
17. G. Lauc, A. Essafi, J.E. Huffman, C. Hayward, A. Knežević, J.J. Kattla, O. Polašek, O. Gornik, V. Vitart, J.L. Abrahams, M. Pučić, M. Novokmet, I. Redžić, S. Campbell, S.H. Wild, F. Borovečki, W. Wang, I. Kolčić, L. Zgaga, U. Gyllensten, J.F. Wilson, A.F. Wright, N.D. Hastie, H. Campbell, P.M. Rudd, and I. Rudan Genomics meets glycomics - the first GWAS study of human N-glycome identifies HNF1alpha as a master regulator of plasma protein fucosylation PLoS Genet. 6 2010 e1001256
18. G. Lauc, J.E. Huffman, M. Pucic, L. Zgaga, B. Adamczyk, A. Muzinic, M. Novokmet, O. Polasek, O. Gornik, J. Kristic, T. Keser, V. Vitart, B. Scheijen, H.W. Uh, M. Molokhia, A.L. Patrick, P. McKeigue, I. Kolcic, I.K. Lukic, O. Swann, F.N. van Leeuwen, L.R. Ruhaak, J.J. Houwing-Duistermaat, P.E. Slagboom, M. Beekman, A.J. de Craen, A.M. Deelder, Q. Zeng, W. Wang, N.D. Hastie, U. Gyllensten, J.F. Wilson, M. Wuhrer, A.F. Wright, P.M. Rudd, C. Hayward, Y. Aulchenko, H. Campbell, and I. Rudan Loci associated with N-glycosylation of human immunoglobulin g show pleiotropy with autoimmune diseases and haematological cancers PLoS Genet. 9 2013 e1003225
19. V. Zoldos, T. Horvat, and G. Lauc Glycomics meets genomics, epigenomics and other high throughput omics for system biology studies Curr. Opin. Chem. Biol. 17 2013 34 40
20. R. Jaenisch, and A. Bird Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals Nat. Genet. 33 Suppl. 2003 245 254 (Pubitemid 36278835)
21. G. Lauc, and V. Zoldoš Protein glycosylation - an evolutionary crossroad between genes and environment Mol. Biosyst. 6 2010 2373 2379
22. O. Gornik, T. Pavic, and G. Lauc Alternative glycosylation modulates function of IgG and other proteins - implications on evolution and disease Biochim. Biophys. Acta 1820 2012 1318 1326
23. J.W. Dennis, K.S. Lau, M. Demetriou, and I.R. Nabi Adaptive regulation at the cell surface by N-glycosylation Traffic 10 2009 1569 1578
24. P. Stanley Regulation of Notch signaling by glycosylation Curr. Opin. Struct. Biol. 17 2007 530 535 (Pubitemid 350019017)
25. A. Knežević, O. Polašek, O. Gornik, I. Rudan, H. Campbell, C. Hayward, A. Wright, I. Kolčić, N. O'Donoghue, J. Bones, P.M. Rudd, and G. Lauc Variability, heritability and environmental determinants of human plasma N-glycome J. Proteome Res. 8 2009 694 701
26. M. Pucic, A. Knezevic, J. Vidic, B. Adamczyk, M. Novokmet, O. Polasek, O. Gornik, S. Supraha-Goreta, M.R. Wormald, I. Redzic, H. Campbell, A. Wright, N.D. Hastie, J.F. Wilson, I. Rudan, M. Wuhrer, P.M. Rudd, D. Josic, and G. Lauc High throughput isolation and glycosylation analysis of IgG-variability and heritability of the IgG glycome in three isolated human populations Mol. Cell Proteomics 10 2011 (M111 010090)
27. O. Gornik, J. Wagner, M. Pučić, A. Knežević, I. Redžić, and G. Lauc Stability of N-glycan profiles in human plasma Glycobiology 19 2009 1547 1553
28. M. Pučić, S. Pinto, M. Novokmet, A. Knežević, O. Gornik, O. Polašek, K. Vlahoviček, W. Wei, P.M. Rudd, A.F. Wright, H. Campbell, I. Rudan, and G. Lauc Common aberrations from normal human N-glycan plasma profile Glycobiology 20 2010 970 975
29. A. Knežević, O. Gornik, O. Polašek, M. Pučić, M. Novokmet, I. Redžić, P.M. Rudd, A.F. Wright, H. Campbell, I. Rudan, and G. Lauc Effects of aging, body mass index, plasma lipid profiles, and smoking on human plasma N-glycans Glycobiology 20 2010 959 969
30. A.V. Probst, E. Dunleavy, and G. Almouzni Epigenetic inheritance during the cell cycle Nat. Rev. Mol. Cell Biol. 10 2009 192 206
31. Z.M. Thayer, and C.W. Kuzawa Biological memories of past environments: epigenetic pathways to health disparities Epigenetics 6 2011 798 803
32. C. Faulk, and D.C. Dolinoy Timing is everything: the when and how of environmentally induced changes in the epigenome of animals Epigenetics 6 2011 791 797
33. J.E. Cropley, C.M. Suter, K.B. Beckman, and D.I. Martin Germ-line epigenetic modification of the murine A vy allele by nutritional supplementation Proc. Natl. Acad. Sci. U.S.A. 103 2006 17308 17312 (Pubitemid 44788965)
34. Z. Migicovsky, and I. Kovalchuk Epigenetic memory in mammals Front. Genet. 2 2011 28
35. O. Rechavi, G. Minevich, and O. Hobert Transgenerational inheritance of an acquired small RNA-based antiviral response in C. elegans Cell 147 2011 1248 1256
36. R.J. Schmitz, M.D. Schultz, M.G. Lewsey, R.C. O'Malley, M.A. Urich, O. Libiger, N.J. Schork, and J.R. Ecker Transgenerational epigenetic instability is a source of novel methylation variants Science 334 2011 369 373
37. D. Crews, R. Gillette, S.V. Scarpino, M. Manikkam, M.I. Savenkova, and M.K. Skinner Epigenetic transgenerational inheritance of altered stress responses Proc. Natl. Acad. Sci. U.S.A. 109 2012 9143 9148
38. B.R. Carone, L. Fauquier, N. Habib, J.M. Shea, C.E. Hart, R. Li, C. Bock, C. Li, H. Gu, P.D. Zamore, A. Meissner, Z. Weng, H.A. Hofmann, N. Friedman, and O.J. Rando Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals Cell 143 2010 1084 1096
39. M. Zeybel, T. Hardy, Y.K. Wong, J.C. Mathers, C.R. Fox, A. Gackowska, F. Oakley, A.D. Burt, C.L. Wilson, Q.M. Anstee, M.J. Barter, S. Masson, A.M. Elsharkawy, D.A. Mann, and J. Mann Multigenerational epigenetic adaptation of the hepatic wound-healing response Nat. Med. 18 2012 1369 1377
40. M.K. Skinner, M. Mohan, M.M. Haque, B. Zhang, and M.I. Savenkova Epigenetic transgenerational inheritance of somatic transcriptomes and epigenetic control regions Genome Biol. 13 2012 R91
41. E. Jablonka, and G. Raz Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution Q. Rev. Biol. 84 2009 131 176
42. H.D. Morgan, F. Santos, K. Green, W. Dean, and W. Reik Epigenetic reprogramming in mammals Hum. Mol. Genet. 14 2005 R47 R58
43. H.D. Morgan, H.G.E. Sutherland, D.I.K. Martin, and E. Whitelaw Epigenetic inheritance at the agouti locus in the mouse Nat. Genet. 23 1999 314 318 (Pubitemid 29526429)
44. M.D. Anway, A.S. Cupp, M. Uzumcu, and M.K. Skinner Epigenetic transgenerational actions of endocrine disruptors and male fertility Science 308 2005 1466 1469 (Pubitemid 40791300)
45. C. Popp, W. Dean, S.H. Feng, S.J. Cokus, S. Andrews, M. Pellegrini, S.E. Jacobsen, and W. Reik Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency Nature 463 2010 U1101 U1126
46. S. Feng, S.E. Jacobsen, and W. Reik Epigenetic reprogramming in plant and animal development Science 330 2010 622 627
47. G.W. van der Heijden, A.A.H.A. Derijck, L. Ramos, M. Giele, J. van der Vlag, and P. de Boer Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin Dev. Biol. 298 2006 458 469 (Pubitemid 44441186)
48. D.K. Palmer, K. Oday, and R.L. Margolis The Centromere Specific Histone Cenp-a Is Selectively Retained in Discrete Foci in Mammalian Sperm Nuclei Chromosoma 100 1990 32 36
49. F. Johannes, E. Porcher, F.K. Teixeira, V. Saliba-Colombani, M. Simon, N. Agier, A. Bulski, J. Albuisson, F. Heredia, P. Audigier, D. Bouchez, C. Dillmann, P. Guerche, F. Hospital, and V. Colot Assessing the impact of transgenerational epigenetic variation on complex traits PLoS Genet. 5 2009 e1000530
50. J. Reinders, B.B.H. Wulff, M. Mirouze, A. Mari-Ordonez, M. Dapp, W. Rozhon, E. Bucher, G. Theiler, and J. Paszkowski Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes Gene Dev. 23 2009 939 950
51. F.K. Teixeira, F. Heredia, A. Sarazin, F. Roudier, M. Boccara, C. Ciaudo, C. Cruaud, J. Poulain, M. Berdasco, M.F. Fraga, O. Voinnet, P. Wincker, M. Esteller, and V. Colot A role for RNAi in the selective correction of DNA methylation defects Science 323 2009 1600 1604
52. P.D. Gluckman, M.A. Hanson, and A.S. Beedle Non-genomic transgenerational inheritance of disease risk Bioessays 29 2007 145 154 (Pubitemid 46340249)
53. M. Rassoulzadegan, V. Grandjean, P. Gounon, S. Vincent, I. Gillot, and F. Cuzin RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse Nature 441 2006 469 474 (Pubitemid 44050143)
54. E. Beyret, N. Liu, and H. Lin piRNA biogenesis during adult spermatogenesis in mice is independent of the ping-pong mechanism Cell Res. 22 2012 1429 1439
55. T. Watanabe, Y. Totoki, A. Toyoda, M. Kaneda, S. Kuramochi-Miyagawa, Y. Obata, H. Chiba, Y. Kohara, T. Kono, T. Nakano, M.A. Surani, Y. Sakaki, and H. Sasaki Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes Nature 453 2008 539 543 (Pubitemid 351733315)
56. U. Syrbe, S. Jennrich, A. Schottelius, A. Richter, A. Radbruch, and A. Hamann Differential regulation of P-selectin ligand expression in naive versus memory CD4 + T cells: evidence for epigenetic regulation of involved glycosyltransferase genes Blood 104 2004 3243 3248 (Pubitemid 39507142)
57. Y. Kizuka, S. Kitazume, M. Yoshida, and N. Taniguchi Brain-specific expression of N-acetylglucosaminyltransferase IX (GnT-IX) is regulated by epigenetic histone modifications J. Biol. Chem. 286 2011 31875 31884
58. F. Dall'Olio, N. Malagolini, M. Trinchera, and M. Chiricolo Mechanisms of cancer-associated glycosylation changes, Frontiers in bioscience Front. Biosci. 17 2012 670 699
59. Y.S. Kim, and G. Deng Aberrant expression of carbohydrate antigens in cancer: the role of genetic and epigenetic regulation Gastroenterology 135 2008 305 309 (Pubitemid 351899050)
60. K. Moriwaki, M. Narisada, T. Imai, S. Shinzaki, and E. Miyoshi The effect of epigenetic regulation of fucosylation on TRAIL-induced apoptosis Glycoconj. J. 27 2010 649 659
61. A. Caretti, S.M. Sirchia, S. Tabano, A. Zulueta, F. Dall'OlioM, and M. Trinchera DNA methylation and histone modifications modulate the beta1,3 galactosyltransferase beta3Gal-T5 native promoter in cancer cells Int. J. Biochem. Cell Biol. 44 2012 84 90
62. Y.I. Kawamura, M. Toyota, R. Kawashima, T. Hagiwara, H. Suzuki, K. Imai, Y. Shinomura, T. Tokino, R. Kannagi, and T. Dohi DNA hypermethylation contributes to incomplete synthesis of carbohydrate determinants in gastrointestinal cancer Gastroenterology 135 2008 142 151
63. A. Yusa, K. Miyazaki, N. Kimura, M. Izawa, and R. Kannagi Epigenetic silencing of the sulfate transporter gene DTDST induces sialyl Lewisx expression and accelerates proliferation of colon cancer cells Cancer Res. 70 2010 4064 4073
64. Y. Chihara, K. Sugano, A. Kobayashi, Y. Kanai, H. Yamamoto, M. Nakazono, H. Fujimoto, T. Kakizoe, K. Fujimoto, S. Hirohashi, and Y. Hirao Loss of blood group A antigen expression in bladder cancer caused by allelic loss and/or methylation of the ABO gene Lab. Invest. 85 2005 895 907 (Pubitemid 41021298)
65. R. Saldova, E. Dempsey, M. Perez-Garay, K. Marino, J.A. Watson, A. Blanco-Fernandez, W.B. Struwe, D.J. Harvey, S.F. Madden, R. Peracaula, A. McCann, and P.M. Rudd 5-AZA-2′-deoxycytidine induced demethylation influences N-glycosylation of secreted glycoproteins in ovarian cancer Epigenetics 6 2011 1362 1372
66. Y. Ide, E. Miyoshi, T. Nakagawa, J. Gu, M. Tanemura, T. Nishida, T. Ito, H. Yamamoto, Y. Kozutsumi, and N. Taniguchi Aberrant expression of N-acetylglucosaminyltransferase-IVa and IVb (GnT-IVa and b) in pancreatic cancer Biochem. Biophys. Res. Commun. 341 2006 478 482 (Pubitemid 43152129)
67. V. Zoldoš, T. Horvat, M. Novokmet, C. Cuenin, A. Mužinić, M. Pučić, J.E. Huffman, O. Gornik, O. Polašek, H. Campbell, C. Hayward, A.F. Wright, I. Rudan, K. Owen, M.I. McCarthy, Z. Herceg, and G. Lauc Epigenetic silencing of HNF1A associates with changes in the composition of the human plasma N-glycome Epigenetics 7 2012 164 172
68. T. Horvat, M. Dezeljin, I. Redzic, D. Barisic, M. Herak Bosnar, G. Lauc, and V. Zoldos Reversibility of membrane N-glycome of HeLa cells upon treatment with epigenetic inhibitors PLoS One 8 2013 e54672
69. T. Horvat, A. Mužinić, D. Barišić, M.H. Bosnar, and V. Zoldoš Epigenetic modulation of the HeLa cell membrane N-glycome Biochim. Biophys. Acta 1820 2012 1412 1419
70. J.R. Bishop, and P. Gagneux Evolution of carbohydrate antigens - microbial forces shaping host glycomes? Glycobiology 17 2007 23R 34R (Pubitemid 47053737)
71. L.V. Hooper, T. Midtvedt, and J.I. Gordon How host-microbial interactions shape the nutrient environment of the mammalian intestine Annu. Rev. Nutr. 22 2002 283 307 (Pubitemid 35221463)
72. D. Joralemon New World depopulation and the case of disease J. Anthropol. Res. 38 1982 108 127
73. L.M. Chen, O. Blixt, J. Stevens, A.S. Lipatov, C.T. Davis, B.E. Collins, N.J. Cox, J.C. Paulson, and R.O. Donis In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity Virology 422 2012 105 113
74. K. Miyazaki, K. Ohmori, M. Izawa, T. Koike, K. Kumamoto, K. Furukawa, T. Ando, M. Kiso, T. Yamaji, Y. Hashimoto, A. Suzuki, A. Yoshida, M. Takeuchi, and R. Kannagi Loss of disialyl Lewis(a), the ligand for lymphocyte inhibitory receptor sialic acid-binding immunoglobulin-like lectin-7 (Siglec-7) associated with increased sialyl Lewis(a) expression on human colon cancers Cancer Res. 64 2004 4498 4505 (Pubitemid 38856921)
75. J. Serpa, P. Mesquita, N. Mendes, C. Oliveira, R. Almeida, F. Santos-Silva, C.A. Reis, J. LePendu, and L. David Expression of Lea in gastric cancer cell lines depends on FUT3 expression regulated by promoter methylation Cancer Lett. 242 2006 191 197 (Pubitemid 44485309)