Y Chromosome Missing Protein, TBL1Y, May Play an Important Role in Cardiac Differentiation

Journal of Proteome Research

Volumn 16, Issue 12, 2017, Pages 4391-4402

  Meyfour, Anna ^a,b   Ansari, Hassan ^a   Pahlavan, Sara ^a   Mirshahvaladi, Shahab ^a   Rezaei Tavirani, Mostafa ^b   Gourabi, Hamid ^a   Baharvand, Hossein ^a,c   Salekdeh, Ghasem Hosseini ^a,d  

^a ROYAN INSTITUTE FOR REPRODUCTIVE BIOMEDICINE   (Iran)

^b SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c UNIVERSITY OF SCIENCE AND CULTURE   (Iran)

^d AGRICULTURAL BIOTECHNOLOGY RESEARCH INSTITUTE OF IRAN   (Iran)

Author keywords

cardiac differentiation; Chromosome Centric Human Proteome Project (C HPP); human embryonic stem cell; TBL1Y; Y chromosome

Indexed keywords

BCORP1 PROTEIN; CHROMOSOME PROTEIN; DDX3Y PROTEIN; HSFY PROTEIN; KDM5D PROTEIN; MESSENGER RNA; PCDH11Y PROTEIN; PRY PROTEIN; RBMY PROTEIN; RPS4Y1 PROTEIN; SMALL INTERFERING RNA; TBL1Y PROTEIN; UNCLASSIFIED DRUG; USP9Y PROTEIN; UTY PROTEIN; XKRY PROTEIN; ZFY PROTEIN; PROTEIN; TBL1Y PROTEIN, HUMAN; TRANSDUCIN;

ARTICLE; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; GENE SILENCING; HEART DEVELOPMENT; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; X CHROMOSOME; Y CHROMOSOME; CARDIAC MUSCLE; CYTOLOGY; EMBRYONIC STEM CELL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEART; METABOLISM; PHYSIOLOGY;

CELL DIFFERENTIATION; CHROMOSOMES, HUMAN, Y; EMBRYONIC STEM CELLS; HEART; HUMANS; MALE; MYOCARDIUM; PROTEINS; RNA, MESSENGER; TRANSDUCIN;

EID: 85034826714     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.7b00391     Document Type: Article

References (51)

1. Jangravi, Z.; Alikhani, M.; Arefnezhad, B.; Sharifi Tabar, M.; Taleahmad, S.; Karamzadeh, R.; Jadaliha, M.; Mousavi, S. A.; Ahmadi Rastegar, D.; Parsamatin, P.; Vakilian, H.; Mirshahvaladi, S.; Sabbaghian, M.; Mohseni Meybodi, A.; Mirzaei, M.; Shahhoseini, M.; Ebrahimi, M.; Piryaei, A.; Moosavi-Movahedi, A. A.; Haynes, P. A.; Goodchild, A. K.; Nasr-Esfahani, M. H.; Jabbari, E.; Baharvand, H.; Sedighi Gilani, M. A.; Gourabi, H.; Salekdeh, G. H. A fresh look at the male-specific region of the human Y chromosome J. Proteome Res. 2013, 12 (1) 6-22 10.1021/pr300864k
2. Bellott, D. W.; Hughes, J. F.; Skaletsky, H.; Brown, L. G.; Pyntikova, T.; Cho, T. J.; Koutseva, N.; Zaghlul, S.; Graves, T.; Rock, S.; Kremitzki, C.; Fulton, R. S.; Dugan, S.; Ding, Y.; Morton, D.; Khan, Z.; Lewis, L.; Buhay, C.; Wang, Q.; Watt, J.; Holder, M.; Lee, S.; Nazareth, L.; Alfoldi, J.; Rozen, S.; Muzny, D. M.; Warren, W. C.; Gibbs, R. A.; Wilson, R. K.; Page, D. C. Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators Nature 2014, 508 (7497) 494-9 10.1038/nature13206
3. Ahmadi Rastegar, D.; Sharifi Tabar, M.; Alikhani, M.; Parsamatin, P.; Sahraneshin Samani, F.; Sabbaghian, M.; Sadighi Gilani, M. A.; Mohammad Ahadi, A.; Mohseni Meybodi, A.; Piryaei, A.; Ansari-Pour, N.; Gourabi, H.; Baharvand, H.; Salekdeh, G. H. Isoform-Level Gene Expression Profiles of Human Y Chromosome Azoospermia Factor Genes and Their X Chromosome Paralogs in the Testicular Tissue of Non-Obstructive Azoospermia Patients J. Proteome Res. 2015, 14 (9) 3595-605 10.1021/acs.jproteome.5b00520
4. Vangompel, M. J.; Xu, E. Y. The roles of the DAZ. family in spermatogenesis: More than just translation? Spermatogenesis 2011, 1 (1) 36-46 10.4161/spmg.1.1.14659
5. Foresta, C.; Moro, E.; Ferlin, A. Y chromosome microdeletions and alterations of spermatogenesis Endocr. Rev. 2001, 22 (2) 226-39 10.1210/edrv.22.2.0425
6. Vakilian, H.; Mirzaei, M.; Sharifi Tabar, M.; Pooyan, P.; Habibi Rezaee, L.; Parker, L.; Haynes, P. A.; Gourabi, H.; Baharvand, H.; Salekdeh, G. H. DDX3Y, a Male-Specific Region of Y Chromosome Gene, May Modulate Neuronal Differentiation J. Proteome Res. 2015, 14 (9) 3474-83 10.1021/acs.jproteome.5b00512
7. Jangravi, Z.; Tabar, M. S.; Mirzaei, M.; Parsamatin, P.; Vakilian, H.; Alikhani, M.; Shabani, M.; Haynes, P. A.; Goodchild, A. K.; Gourabi, H.; Baharvand, H.; Salekdeh, G. H. Two Splice Variants of Y Chromosome-Located Lysine-Specific Demethylase 5D Have Distinct Function in Prostate Cancer Cell Line (DU-145) J. Proteome Res. 2015, 14 (9) 3492-502 10.1021/acs.jproteome.5b00333
8. Skuse, D. H. Imprinting, the X-chromosome, and the male brain: explaining sex differences in the liability to autism Pediatr. Res. 2000, 47 (1) 9-16 10.1203/00006450-200001000-00006
9. Serajee, F. J.; Mahbubul Huq, A. H. Association of Y chromosome haplotypes with autism J. Child Neurol 2009, 24 (10) 1258-61 10.1177/0883073809333530
10. Goulmy, E.; Termijtelen, A.; Bradley, B. A.; van Rood, J. J. Y-antigen killing by T cells of women is restricted by HLA Nature 1977, 266 (5602) 544-5 10.1038/266544a0
11. Wang, W.; Meadows, L. R.; den Haan, J. M.; Sherman, N. E.; Chen, Y.; Blokland, E.; Shabanowitz, J.; Agulnik, A. I.; Hendrickson, R. C.; Bishop, C. E. et al. Human H-Y: a male-specific histocompatibility antigen derived from the SMCY protein Science 1995, 269 (5230) 1588-90 10.1126/science.7667640
12. Sandberg, A. A. Chromosomal abnormalities and related events in prostate cancer Hum. Pathol. 1992, 23 (4) 368-80 10.1016/0046-8177(92)90083-F
13. Lau, Y. F.; Zhang, J. Expression analysis of thirty one Y chromosome genes in human prostate cancer Mol. Carcinog. 2000, 27 (4) 308-21 10.1002/(SICI)1098-2744(200004)27:4<308::AID-MC9>3.0.CO;2-R
14. Vergnaud, G.; Page, D. C.; Simmler, M. C.; Brown, L.; Rouyer, F.; Noel, B.; Botstein, D.; de la Chapelle, A.; Weissenbach, J. A deletion map of the human Y chromosome based on DNA hybridization Am. J. Hum. Genet. 1986, 38 (2) 109-24
15. Isensee, J.; Witt, H.; Pregla, R.; Hetzer, R.; Regitz-Zagrosek, V.; Noppinger, P. R. Sexually dimorphic gene expression in the heart of mice and men J. Mol. Med. (Heidelberg, Ger.) 2008, 86 (1) 61-74 10.1007/s00109-007-0240-z
16. Schocken, D. D.; Arrieta, M. I.; Leaverton, P. E.; Ross, E. A. Prevalence and mortality rate of congestive heart failure in the United States J. Am. Coll. Cardiol. 1992, 20 (2) 301-6 10.1016/0735-1097(92)90094-4
17. Fairweather, D.; Cooper, L. T., Jr.; Blauwet, L. A. Sex and gender differences in myocarditis and dilated cardiomyopathy Curr. Probl Cardiol 2013, 38 (1) 7-46 10.1016/j.cpcardiol.2012.07.003
18. Cocker, M. S.; Abdel-Aty, H.; Strohm, O.; Friedrich, M. G. Age and gender effects on the extent of myocardial involvement in acute myocarditis: a cardiovascular magnetic resonance study Heart 2009, 95 (23) 1925-30 10.1136/hrt.2008.164061
19. Cooper, L. T.; Mather, P. J.; Alexis, J. D.; Pauly, D. F.; Torre-Amione, G.; Wittstein, I. S.; Dec, G. W.; Zucker, M.; Narula, J.; Kip, K.; McNamara, D. M. Investigators, I., Myocardial recovery in peripartum cardiomyopathy: prospective comparison with recent onset cardiomyopathy in men and nonperipartum women J. Card. Failure 2012, 18 (1) 28-33 10.1016/j.cardfail.2011.09.009
20. Fermini, B.; Fossa, A. A. The impact of drug-induced QT interval prolongation on drug discovery and development Nat. Rev. Drug Discovery 2003, 2 (6) 439-47 10.1038/nrd1108
21. Haddad, G. E.; Saunders, L. J.; Crosby, S. D.; Carles, M.; del Monte, F.; King, K.; Bristow, M. R.; Spinale, F. G.; Macgillivray, T. E.; Semigran, M. J.; Dec, G. W.; Williams, S. A.; Hajjar, R. J.; Gwathmey, J. K. Human cardiac-specific cDNA array for idiopathic dilated cardiomyopathy: sex-related differences Physiol. Genomics 2008, 33 (2) 267-77 10.1152/physiolgenomics.00265.2007
22. Heidecker, B.; Lamirault, G.; Kasper, E. K.; Wittstein, I. S.; Champion, H. C.; Breton, E.; Russell, S. D.; Hall, J.; Kittleson, M. M.; Baughman, K. L.; Hare, J. M. The gene expression profile of patients with new-onset heart failure reveals important gender-specific differences Eur. Heart J. 2010, 31 (10) 1188-96 10.1093/eurheartj/ehp549
23. Prelle, K.; Zink, N.; Wolf, E. Pluripotent stem cells - model of embryonic development, tool for gene targeting, and basis of cell therapy Anat Histol Embryol 2002, 31 (3) 169-86 10.1046/j.1439-0264.2002.00388.x
24. Kelleher, N. L. A cell-based approach to the human proteome project J. Am. Soc. Mass Spectrom. 2012, 23 (10) 1617-24 10.1007/s13361-012-0469-9
25. Larijani, M. R.; Seifinejad, A.; Pournasr, B.; Hajihoseini, V.; Hassani, S. N.; Totonchi, M.; Yousefi, M.; Shamsi, F.; Salekdeh, G. H.; Baharvand, H. Long-term maintenance of undifferentiated human embryonic and induced pluripotent stem cells in suspension Stem Cells Dev. 2011, 20 (11) 1911-23 10.1089/scd.2010.0517
26. Fonoudi, H.; Ansari, H.; Abbasalizadeh, S.; Larijani, M. R.; Kiani, S.; Hashemizadeh, S.; Zarchi, A. S.; Bosman, A.; Blue, G. M.; Pahlavan, S.; Perry, M.; Orr, Y.; Mayorchak, Y.; Vandenberg, J.; Talkhabi, M.; Winlaw, D. S.; Harvey, R. P.; Aghdami, N.; Baharvand, H. A Universal and Robust Integrated Platform for the Scalable Production of Human Cardiomyocytes From Pluripotent Stem Cells Stem Cells Transl. Med. 2015, 4 (12) 1482-94 10.5966/sctm.2014-0275
27. Perissi, V.; Scafoglio, C.; Zhang, J.; Ohgi, K. A.; Rose, D. W.; Glass, C. K.; Rosenfeld, M. G. TBL1 and TBLR1 phosphorylation on regulated gene promoters overcomes dual CtBP and NCoR/SMRT transcriptional repression checkpoints Mol. Cell 2008, 29 (6) 755-66 10.1016/j.molcel.2008.01.020
28. Wamstad, J. A.; Alexander, J. M.; Truty, R. M.; Shrikumar, A.; Li, F.; Eilertson, K. E.; Ding, H.; Wylie, J. N.; Pico, A. R.; Capra, J. A.; Erwin, G.; Kattman, S. J.; Keller, G. M.; Srivastava, D.; Levine, S. S.; Pollard, K. S.; Holloway, A. K.; Boyer, L. A.; Bruneau, B. G. Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage Cell 2012, 151 (1) 206-20 10.1016/j.cell.2012.07.035
29. Takeuchi, T.; Watanabe, Y.; Takano-Shimizu, T.; Kondo, S. Roles of jumonji and jumonji family genes in chromatin regulation and development Dev. Dyn. 2006, 235 (9) 2449-59 10.1002/dvdy.20851
30. Walport, L. J.; Hopkinson, R. J.; Vollmar, M.; Madden, S. K.; Gileadi, C.; Oppermann, U.; Schofield, C. J.; Johansson, C. Human UTY(KDM6C) is a male-specific N-methyl lysyl demethylase J. Biol. Chem. 2014, 289 (26) 18302-13 10.1074/jbc.M114.555052
31. Lee, S.; Lee, J. W.; Lee, S. K. UTX, a histone H3-lysine 27 demethylase, acts as a critical switch to activate the cardiac developmental program Dev. Cell 2012, 22 (1) 25-37 10.1016/j.devcel.2011.11.009
32. Wang, C.; Lee, J. E.; Cho, Y. W.; Xiao, Y.; Jin, Q.; Liu, C.; Ge, K. UTX regulates mesoderm differentiation of embryonic stem cells independent of H3K27 demethylase activity Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (38) 15324-9 10.1073/pnas.1204166109
33. Eriksson, M.; Jokinen, E.; Sistonen, L.; Leppa, S. Heat shock factor 2 is activated during mouse heart development Int. J. Dev Biol. 2000, 44 (5) 471-7
34. Hilton, E.; Johnston, J.; Whalen, S.; Okamoto, N.; Hatsukawa, Y.; Nishio, J.; Kohara, H.; Hirano, Y.; Mizuno, S.; Torii, C.; Kosaki, K.; Manouvrier, S.; Boute, O.; Perveen, R.; Law, C.; Moore, A.; Fitzpatrick, D.; Lemke, J.; Fellmann, F.; Debray, F. G.; Dastot-Le-Moal, F.; Gerard, M.; Martin, J.; Bitoun, P.; Goossens, M.; Verloes, A.; Schinzel, A.; Bartholdi, D.; Bardakjian, T.; Hay, B.; Jenny, K.; Johnston, K.; Lyons, M.; Belmont, J. W.; Biesecker, L. G.; Giurgea, I.; Black, G. BCOR analysis in patients with OFCD and Lenz microphthalmia syndromes, mental retardation with ocular anomalies, and cardiac laterality defects Eur. J. Hum. Genet. 2009, 17 (10) 1325-35 10.1038/ejhg.2009.52
35. Ng, D.; Thakker, N.; Corcoran, C. M.; Donnai, D.; Perveen, R.; Schneider, A.; Hadley, D. W.; Tifft, C.; Zhang, L.; Wilkie, A. O.; van der Smagt, J. J.; Gorlin, R. J.; Burgess, S. M.; Bardwell, V. J.; Black, G. C.; Biesecker, L. G. Oculofaciocardiodental and Lenz microphthalmia syndromes result from distinct classes of mutations in BCOR Nat. Genet. 2004, 36 (4) 411-6 10.1038/ng1321
36. Zhu, X.; Dai, F. R.; Wang, J.; Zhang, Y.; Tan, Z. P.; Zhang, Y. Novel BCOR mutation in a boy with Lenz microphthalmia/oculo-facio-cardio-dental (OFCD) syndrome Gene 2015, 571 (1) 142-4 10.1016/j.gene.2015.07.061
37. Li, J.; Wang, J.; Wang, J.; Nawaz, Z.; Liu, J. M.; Qin, J.; Wong, J. Both corepressor proteins SMRT and N-CoR exist in large protein complexes containing HDAC3 EMBO J. 2000, 19 (16) 4342-50 10.1093/emboj/19.16.4342
38. Guenther, M. G.; Barak, O.; Lazar, M. A. The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3 Mol. Cell. Biol. 2001, 21 (18) 6091-101 10.1128/MCB.21.18.6091-6101.2001
39. Tomita, A.; Buchholz, D. R.; Shi, Y. B. Recruitment of N-CoR/SMRT-TBLR1 corepressor complex by unliganded thyroid hormone receptor for gene repression during frog development Mol. Cell. Biol. 2004, 24 (8) 3337-46 10.1128/MCB.24.8.3337-3346.2004
40. Perissi, V.; Aggarwal, A.; Glass, C. K.; Rose, D. W.; Rosenfeld, M. G. A corepressor/coactivator exchange complex required for transcriptional activation by nuclear receptors and other regulated transcription factors Cell 2004, 116 (4) 511-26 10.1016/S0092-8674(04)00133-3
41. Omenn, G. S.; Lane, L.; Lundberg, E. K.; Beavis, R. C.; Nesvizhskii, A. I.; Deutsch, E. W. Metrics for the Human Proteome Project 2015: progress on the human proteome and guidelines for high-confidence protein identification J. Proteome Res. 2015, 14 (9) 3452-3460 10.1021/acs.jproteome.5b00499
42. Perissi, V.; Jepsen, K.; Glass, C. K.; Rosenfeld, M. G. Deconstructing repression: evolving models of co-repressor action Nat. Rev. Genet. 2010, 11 (2) 109-23 10.1038/nrg2736
43. Oswald, F.; Winkler, M.; Cao, Y.; Astrahantseff, K.; Bourteele, S.; Knochel, W.; Borggrefe, T. RBP-Jkappa/SHARP recruits CtIP/CtBP corepressors to silence Notch target genes Mol. Cell. Biol. 2005, 25 (23) 10379-90 10.1128/MCB.25.23.10379-10390.2005
44. Lai, E. C. Notch signaling: control of cell communication and cell fate Development 2004, 131 (5) 965-73 10.1242/dev.01074
45. Tung, J. C.; Paige, S. L.; Ratner, B. D.; Murry, C. E.; Giachelli, C. M. Engineered biomaterials control differentiation and proliferation of human-embryonic-stem-cell-derived cardiomyocytes via timed Notch activation Stem Cell Rep. 2014, 2 (3) 271-81 10.1016/j.stemcr.2014.01.011
46. Ding, R.; Jiang, X.; Ha, Y.; Wang, Z.; Guo, J.; Jiang, H.; Zheng, S.; Shen, Z.; Jie, W. Activation of Notch1 signalling promotes multi-lineage differentiation of c-Kit(POS)/NKX2.5(POS) bone marrow stem cells: implication in stem cell translational medicine Stem Cell Res. Ther. 2015, 6, 91 10.1186/s13287-015-0085-2
47. D'Amato, G.; Luxan, G.; de la Pompa, J. L. Notch signalling in ventricular chamber development and cardiomyopathy FEBS J. 2016, 283 (23) 4223-4237 10.1111/febs.13773
48. D'Amato, G.; Luxan, G.; del Monte-Nieto, G.; Martinez-Poveda, B.; Torroja, C.; Walter, W.; Bochter, M. S.; Benedito, R.; Cole, S.; Martinez, F.; Hadjantonakis, A. K.; Uemura, A.; Jimenez-Borreguero, L. J.; de la Pompa, J. L. Sequential Notch activation regulates ventricular chamber development Nat. Cell Biol. 2015, 18 (1) 7-20 10.1038/ncb3280
49. Tagariello, A.; Breuer, C.; Birkner, Y.; Schmidt, S.; Koch, A. M.; Cesnjevar, R.; Ruffer, A.; Dittrich, S.; Schneider, H.; Winterpacht, A.; Sticht, H.; Dotsch, J.; Toka, O. Functional null mutations in the gonosomal homologue gene TBL1Y are associated with non-syndromic coarctation of the aorta Curr. Mol. Med. 2012, 12 (2) 199-205 10.2174/156652412798889027
50. Urbanek, K.; Cabral-da-Silva, M. C.; Ide-Iwata, N.; Maestroni, S.; Delucchi, F.; Zheng, H.; Ferreira-Martins, J.; Ogorek, B.; D'Amario, D.; Bauer, M.; Zerbini, G.; Rota, M.; Hosoda, T.; Liao, R.; Anversa, P.; Kajstura, J.; Leri, A. Inhibition of notch1-dependent cardiomyogenesis leads to a dilated myopathy in the neonatal heart Circ. Res. 2010, 107 (3) 429-41 10.1161/CIRCRESAHA.110.218487
51. Legrain, P.; Aebersold, R.; Archakov, A.; Bairoch, A.; Bala, K.; Beretta, L.; Bergeron, J.; Borchers, C. H.; Corthals, G. L.; Costello, C. E.; Deutsch, E. W.; Domon, B.; Hancock, W.; He, F.; Hochstrasser, D.; Marko-Varga, G.; Salekdeh, G. H.; Sechi, S.; Snyder, M.; Srivastava, S.; Uhlen, M.; Wu, C. H.; Yamamoto, T.; Paik, Y. K.; Omenn, G. S. The human proteome project: current state and future direction Mol. Cell. Proteomics 2011, 10 (7) M111.009993 10.1074/mcp.M111.009993