HOXC6 Is transcriptionally regulated via coordination of MLL histone methylase and estrogen receptor in an estrogen environment

Journal of Molecular Biology

Volumn 411, Issue 2, 2011, Pages 334-349

  Ansari, Khairul I ^a   Hussain, Imran ^a   Shrestha, Bishakha ^a   Kasiri, Sahba ^a   Mandal, Subhrangsu S ^a  

^a UNIVERSITY OF TEXAS AT ARLINGTON   (United States)

Author keywords

estrogen receptors; gene regulation; HOXC6; MLL histone methylase; steroid signaling

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; HISTONE H3; HOMEOBOX C6; HOMEODOMAIN PROTEIN; METHYLTRANSFERASE; MLL1 ENZYME; MLL2 ENZYME; MLL3 ENZYME; MLL4 ENZYME; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ARTICLE; ESTROGEN RESPONSIVE ELEMENT; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

EID: 79960701056     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.05.050     Document Type: Article

References (74)

1. Lappin T.R.; Grier D.G.; Thompson A.; and Halliday H.L. HOX genes: seductive science, mysterious mechanisms Ulster Med. J. 75 2006 23 31 (Pubitemid 43168878)
2. Yu B.D.; Hess J.L.; Horning S.E.; Brown G.A.; and Korsmeyer S.J. Altered Hox expression and segmental identity in Mll-mutant mice Nature 378 1995 505 508
3. Alexander T.; Nolte C.; and Krumlauf R. Hox genes and segmentation of the hindbrain and axial skeleton Annu. Rev. Cell Dev. Biol. 25 2009 431 456
4. Chen H.; and Sukumar S. HOX genes: emerging stars in cancer Cancer Biol. Ther. 2 2003 524 525
5. Friedmann Y.; Daniel C.A.; Strickland P.; and Daniel C.W. Hox genes in normal and neoplastic mouse mammary gland Cancer Res. 54 1994 5981 5985 (Pubitemid 24375237)
6. Makiyama K.; Hamada J.; Takada M.; Murakawa K.; Takahashi Y.; and Tada M. Aberrant expression of HOX genes in human invasive breast carcinoma Oncol. Rep. 13 2005 673 679
7. Maroulakou I.G.; and Spyropoulos D.D. The study of HOX gene function in hematopoietic, breast and lung carcinogenesis Anticancer Res. 23 2003 2101 2110 (Pubitemid 36897170)
8. Nunes F.D.; de Almeida F.C.; Tucci R.; and de Sousa S.C. Homeobox genes: a molecular link between development and cancer Pesqui. Odontol. Bras. 17 2003 94 98
9. Rhoads K.; Arderiu G.; Charboneau A.; Hansen S.L.; Hoffman W.; and Boudreau N. A role for Hox A5 in regulating angiogenesis and vascular patterning Lymphatic Res. Biol. 3 2005 240 252 (Pubitemid 43115793)
10. Bodey B.; Bodey B. Jr, Siegel S.E.; and Kaiser H.E. Immunocytochemical detection of the homeobox B3, B4, and C6 gene products in breast carcinomas Anticancer Res. 20 2000 3281 3286
11. Castronovo V.; Kusaka M.; Chariot A.; Gielen J.; and Sobel M. Homeobox genes: potential candidates for the transcriptional control of the transformed and invasive phenotype Biochem. Pharmacol. 47 1994 137 143 (Pubitemid 24045826)
12. Garcia-Gasca A.; and Spyropoulos D.D. Differential mammary morphogenesis along the anteroposterior axis in Hoxc6 gene targeted mice Dev. Dyn. 219 2000 261 276
13. McCabe C.D.; Spyropoulos D.D.; Martin D.; and Moreno C.S. Genome-wide analysis of the homeobox C6 transcriptional network in prostate cancer Cancer Res. 68 2008 1988 1996 (Pubitemid 351416586)
14. Miller G.J.; Miller H.L.; van Bokhoven A.; Lambert J.R.; Werahera P.N.; and Schirripa O. Aberrant HOXC expression accompanies the malignant phenotype in human prostate Cancer Res. 63 2003 5879 5888 (Pubitemid 37187488)
15. Ramachandran S.; Liu P.; Young A.N.; Yin-Goen Q.; Lim S.D.; and Laycock N. Loss of HOXC6 expression induces apoptosis in prostate cancer cells Oncogene 24 2005 188 198 (Pubitemid 40143878)
16. Waltregny D.; Alami Y.; Clausse N.; de Leval J.; and Castronovo V. Overexpression of the homeobox gene HOXC8 in human prostate cancer correlates with loss of tumor differentiation Prostate 50 2002 162 186069
17. Ansari K.I.; Mishra B.P.; and Mandal S.S. Human CpG binding protein interacts with MLL1, MLL2 and hSet1 and regulates Hox gene expression Biochim. Biophys. Acta 1779 2008 66 73
18. Guenther M.G.; Jenner R.G.; Chevalier B.; Nakamura T.; Croce C.M.; Canaani E.; and Young R.A. Global and Hox-specific roles for the MLL1 methyltransferase Proc. Natl Acad. Sci. USA 102 2005 8603 8608 (Pubitemid 40862782)
19. Hess J.L. MLL: a histone methyltransferase disrupted in leukemia Trends Mol. Med. 10 2004 500 507 (Pubitemid 39303623)
20. Ernst P.; Mabon M.; Davidson A.J.; Zon L.I.; and Korsmeyer S.J. An Mll-dependent Hox program drives hematopoietic progenitor expansion Curr. Biol. 14 2004 2063 2069 (Pubitemid 39547963)
21. Meyer C.; Kowarz E.; Hofmann J.; Renneville A.; Zuna J.; and Trka J. New insights to the MLL recombinome of acute leukemias Leukemia 23 2009 1490 1499
22. Ansari K.I.; Mishra B.P.; and Mandal S.S. MLL histone methylases in gene expression, hormone signaling and cell cycle Front. Biosci. 14 2009 3483 3495
23. Canaani E.; Nakamura T.; Rozovskaia T.; Smith S.T.; Mori T.; Croce C.M.; and Mazo A. ALL-1/MLL1, a homologue of Drosophila trithorax, modifies chromatin and is directly involved in infant acute leukaemia Br. J. Cancer 90 2004 756 760 (Pubitemid 38406582)
24. Crawford B.D.; and Hess J.L. MLL core components give the green light to histone methylation ACS Chem. Biol. 1 2006 495 498
25. Dou Y.L.; Milne T.A.; Tackett A.J.; Smith E.R.; Fukuda A.; and Wysocka J. Physical association and coordinate function of the H3K4 methyltransferase MLL1 and the H4K16 acetyltransferase MOF Cell 121 2005 873 885 (Pubitemid 40806419)
26. Glaser S.; Schaft J.; Lubitz S.; Vintersten K.; van der Hoeven F.; and Tufteland K.R. Multiple epigenetic maintenance factors implicated by the loss of Mll2 in mouse development Development 133 2006 1423 1432 (Pubitemid 43732956)
27. Hanson R.D.; Hess J.L.; Yu B.D.; Ernst P.; van Lohuizen M.; and Berns A. Mammalian trithorax and polycomb-group homologues are antagonistic regulators of homeotic development Proc. Natl Acad. Sci. USA 96 1999 14372 14377 (Pubitemid 30000657)
28. Hsieh J.J.; Cheng E.H.; and Korsmeyer S.J. Taspase1: a threonine aspartase required for cleavage of MLL and proper HOX gene expression Cell 115 2003 293 303 (Pubitemid 37487703)
29. Issaeva I.; Zonis Y.; Rozovskaia T.; Orlovsky K.; Croce C.M.; and Nakamura T. Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth Mol. Cell. Biol. 27 2007 1889 1903
30. Lee J.; Saha P.K.; Yang Q.H.; Lee S.; Park J.Y.; and Suh Y. Targeted inactivation of MLL3 histone H3-Lys-4 methyltransferase activity in the mouse reveals vital roles for MLL3 in adipogenesis Proc. Natl Acad. Sci. USA 105 2008 19229 19234
31. Lee J.H.; and Skalnik D.G. CpG-binding protein is a nuclear matrix- and euchromatin-associated protein localized to nuclear speckles containing human trithorax. Identification of nuclear matrix targeting signals J. Biol. Chem. 277 2002 42259 42267 (Pubitemid 35257546)
32. Lee S.; Kim D.H.; Goo Y.H.; Lee Y.C.; Lee S.K.; and Lee J.W. Crucial roles for interactions between MLL3/4 and INI1 in nuclear receptor transactivation Mol. Endocrinol. 23 2009 610 619
33. Milne T.A.; Hughes C.M.; Lloyd R.; Yang Z.; Rozenblatt-Rosen O.; and Dou Y. Menin and MLL cooperatively regulate expression of cyclin-dependent kinase inhibitors Proc. Natl Acad. Sci. USA 102 2005 749 754 (Pubitemid 40282737)
34. Mishra B.P.; Ansari K.I.; and Mandal S.S. Dynamic association of MLL1, H3K4 trimethylation with chromatin and Hox gene expression during the cell cycle FEBS J. 276 2009 1629 1640
35. Mo R.; Rao S.M.; and Zhu Y.J. Identification of the MLL2 complex as a coactivator for estrogen receptor alpha J. Biol. Chem. 281 2006 15714 15720 (Pubitemid 43848459)
36. Nakamura T.; Mori T.; Tada S.; Krajewski W.; Rozovskaia T.; and Wassell R. ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation Mol. Cell 10 2002 1119 1128 (Pubitemid 35453829)
37. Ruthenburg A.J.; Wang W.K.; Graybosch D.M.; Li H.T.; Allis C.D.; Patel D.J.; and Verdine G.L. Histone H3 recognition and presentation by the WDR5 module of the MLL1 complex Nat. Struct. Mol. Biol. 13 2006 704 712 (Pubitemid 44175163)
38. Takeda S.; Chen D.Y.; Westergard T.D.; Fisher J.K.; Rubens J.A.; and Sasagawa S. Proteolysis of MLL family proteins is essential for taspase1-orchestrated cell cycle progression Genes Dev. 20 2006 2397 2409 (Pubitemid 44320388)
39. Yokoyama A.; Wang Z.; Wysocka J.; Sanyal M.; Aufiero D.J.; and Kitabayashi I. Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression Mol. Cell. Biol. 24 2004 5639 5649 (Pubitemid 38787950)
40. Cosgrove, M. S. & Patel, A. Mixed lineage leukemia: a structure-function perspective of the MLL1 protein. FEBS J. 277, 1832-1842.
41. Dou Y.; Milne T.A.; Ruthenburg A.J.; Lee S.; Lee J.W.; and Verdine G.L. Regulation of MLL1 H3K4 methyltransferase activity by its core components Nat. Struct. Mol. Biol. 13 2006 713 719 (Pubitemid 44175164)
42. Patel A.; Dharmarajan V.; and Cosgrove M.S. Structure of WDR5 bound to mixed lineage leukemia protein-1 peptide J. Biol. Chem. 283 2008 32158 32161
43. Deng L.W.; Chiu I.; and Strominger J.L. MLL 5 protein forms intranuclear foci, and overexpression inhibits cell cycle progression Proc. Natl Acad. Sci. USA 101 2004 757 762 (Pubitemid 38121031)
44. Hsieh J.J.D.; Ernst P.; Erdjument-Bromage H.; Tempst P.; and Korsmeyer S.J. Proteolytic cleavage of MLL generates a complex of N- and C-terminal fragments that confers protein stability and subnuclear localization Mol. Cell. Biol. 23 2003 186 1914
45. Ansari K.I.; Hussain I.; Das H.K.; and Mandal S.S. Overexpression of human histone methylase MLL1 upon exposure to a food contaminant mycotoxin, deoxynivalenol FEBS J. 276 2009 3299 3307
46. Libura J.; Ward M.; Solecka J.; and Richardson C. Etoposide-initiated MLL rearrangements detected at high frequency in human primitive hematopoietic stem cells with in vitro and in vivo long-term repopulating potential Eur. J. Haematol. 81 2008 185 195
47. Moneypenny C.G.; Shao J.; Song Y.; and Gallagher E.P. MLL rearrangements are induced by low doses of etoposide in human fetal hematopoietic stem cells Carcinogenesis 27 2006 874 881
48. Chantrain C.F.; Sauvage D.; Brichard B.; Dupont S.; Poirel H.A.; and Ameye G. Neonatal acute myeloid leukemia in an infant whose mother was exposed to diethylstilboestrol in utero Pediatr. Blood Cancer 53 2009 220 222
49. Schnyder S.; Du N.T.; Le H.B.; Singh S.; Loredo G.A.; and Vaughan A.T. Estrogen treatment induces MLL aberrations in human lymphoblastoid cells Leuk. Res. 33 2009 1400 1404
50. Dreijerink K.M.; Mulder K.W.; Winkler G.S.; Hoppener J.W.; Lips C.J.; and Timmers H.T. Menin links estrogen receptor activation to histone H3K4 trimethylation Cancer Res. 66 2006 4929 4935
51. Lee S.; Lee D.K.; Dou Y.; Lee J.; Lee B.; and Kwak E. Coactivator as a target gene specificity determinant for histone H3 lysine 4 methyltransferases Proc. Natl Acad. Sci. USA 103 2006 15392 15397 (Pubitemid 44625602)
52. Ansari K.I.; Kasiri S.; Hussain I.; and Mandal S.S. Mixed lineage leukemia histone methylases play critical roles in estrogen-mediated regulation of HOXC13 FEBS J. 276 2009 7400 7411
53. Strauss J.F. III, Martinez F.; and Kiriakidou M. Placental steroid hormone synthesis: unique features and unanswered questions Biol. Reprod. 54 1996 303 311 (Pubitemid 26031398)
54. Wadsack C.; Hrzenjak A.; Hammer A.; Hirschmugl B.; Levak-Frank S.; and Desoye G. Trophoblast-like human choriocarcinoma cells serve as a suitable in vitro model for selective cholesteryl ester uptake from high density lipoproteins Eur. J. Biochem. 270 2003 451 462 (Pubitemid 36177312)
55. Nilsson S.; and Gustafsson J.A. Estrogen receptor action Crit. Rev. Eukaryotic Gene Expression 12 2002 237 257 (Pubitemid 37051498)
56. Nilsson S.; Makela S.; Treuter E.; Tujague M.; Thomsen J.; and Andersson G. Mechanisms of estrogen action Physiol. Rev. 81 2001 1535 1565 (Pubitemid 32951806)
57. Vermeulen M.; Mulder K.W.; Denissov S.; Pijnappel W.W.; van Schaik F.M.; and Varier R.A. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4 Cell 131 2007 58 69 (Pubitemid 47498531)
58. Jiang S.; Meyer R.; Kang K.; Osborne C.K.; Wong J.; and Oesterreich S. Scaffold attachment factor SAFB1 suppresses estrogen receptor alpha-mediated transcription in part via interaction with nuclear receptor corepressor Mol. Endocrinol. 20 2006 311 320 (Pubitemid 43152506)
59. Oesterreich S.; Zhang Q.; Hopp T.; Fuqua S.A.; Michaelis M.; and Zhao H.H. Tamoxifen-bound estrogen receptor (ER) strongly interacts with the nuclear matrix protein HET/SAF-B, a novel inhibitor of ER-mediated transactivation Mol. Endocrinol. 14 2000 369 381 (Pubitemid 32260529)
60. Shibata H.; Spencer T.E.; Onate S.A.; Jenster G.; Tsai S.Y.; Tsai M.J.; and O'Malley B.W. Role of co-activators and co-repressors in the mechanism of steroid/thyroid receptor action Recent Prog. Horm. Res. 52 1997 141 164 discussion, 164-165 (Pubitemid 127470209)
61. Taylor H.S. Endocrine disruptors affect developmental programming of HOX gene expression Fertil. Steril. 89 2008 e57 e58
62. Block K.; Kardana A.; Igarashi P.; and Taylor H.S. In utero diethylstilbestrol (DES) exposure alters Hox gene expression in the developing Mullerian system FASEB J. 14 2000 1101 110138
63. Daftary G.S.; and Taylor H.S. Endocrine regulation of HOX genes Endocr. Rev. 27 2006 331 355 (Pubitemid 43848302)
64. Taylor H.S.; Arici A.; Olive D.; and Igarashi P. HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium J. Clin. Invest. 101 1998 1379 1384 (Pubitemid 28166835)
65. Chen H.; and Sukumar S. Role of homeobox genes in normal mammary gland development and breast tumorigenesis J. Mammary Gland Biol. Neoplasia 8 2003 159 175 (Pubitemid 38129939)
66. Lane D.B.; Rutherford T.J.; and Taylor H.S. HOXA10 expression in endometrial adenocarcinoma Tumour Biol. 25 2004 264 269 (Pubitemid 40082329)
67. Akbas G.E.; Song J.; and Taylor H.S. A HOXA10 estrogen response element (ERE) is differentially regulated by 17 beta-estradiol and diethylstilbestrol (DES) J. Mol. Biol. 340 2004 1013 1023 (Pubitemid 38968699)
68. Lalmansingh A.S.; and Uht R.M. Estradiol regulates corticotropin- releasing hormone gene (crh) expression in a rapid and phasic manner that parallels estrogen receptor-alpha and -beta recruitment to a 3′,5′-cyclic adenosine 5′-monophosphate regulatory region of the proximal crh promoter Endocrinology 149 2008 346 357
69. Lonard D.M.; and O'Malley B.W. Expanding functional diversity of the coactivators Trends Biochem. Sci. 30 2005 126 132 (Pubitemid 40332528)
70. Ansari K.I.; and Mandal S.S. Mixed lineage leukemia: roles in gene expression, hormone signaling and mRNA processing FEBS J. 277 2010 1790 1804
71. Baniahmad A. Nuclear hormone receptor co-repressors J. Steroid Biochem. Mol. Biol. 93 2005 89 97 (Pubitemid 40602480)
72. Bannister A.J.; and Kouzarides T. Histone methylation: recognizing the methyl mark Methods Enzymol. 376 2004 269 288 (Pubitemid 38200185)
73. Duverger O.; and Morasso M.I. Role of homeobox genes in the patterning, specification, and differentiation of ectodermal appendages in mammals J. Cell. Physiol. 216 2008 337 346 (Pubitemid 351898460)
74. Ansari K.I.; Kasiri S.; Grant J.D.; and Mandal S.S. Apoptosis and anti-tumour activities of manganese(III)-salen and -salphen complexes Dalton Trans. 2009 8525 8531