Epigenetic targeting of transforming growth factor β receptor II and implications for cancer therapy

Molecular and Cellular Pharmacology

Volumn 1, Issue 1, 2009, Pages 57-70

  Chowdhury, Sanjib ^a   Ammanamanchi, Sudhakar ^b   Howell, Gillian M ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Epigenetics; HDAC inhibitors; Histone deacetylases; Histone modifications; TGF RII; Therapy

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; APICIDIN; BUTYRIC ACID; DESMOCOLLIN; DNA METHYLTRANSFERASE INHIBITOR; HISTONE; HISTONE DEACETYLASE INHIBITOR; N (2 AMINOPHENYL) 4 (3 PYRIDINYLMETHOXYCARBONYLAMINOMETHYL)BENZAMIDE; NUCLEAR FACTOR Y; TAMOXIFEN; TRANSCRIPTION FACTOR SP1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; TRICHOSTATIN A; VALPROIC ACID;

ACETYLATION; CANCER CHEMOTHERAPY; CANCER RESEARCH; CARCINOGENESIS; COLON CANCER; COLON CARCINOMA; DNA METHYLATION; DNA REPAIR; DNA SEQUENCE; DRUG INHIBITION; DRUG TARGETING; EPIGENETICS; GENE MUTATION; GENE SILENCING; GROWTH INHIBITION; HEAD AND NECK CARCINOMA; HUMAN; LUNG CANCER; NONHUMAN; PANCREAS CANCER; PHENOTYPE; PROGNOSIS; PROSTATE CANCER; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; TUMOR GROWTH;

EID: 77953406722     PISSN: None     EISSN: 19381247     Source Type: Journal    
DOI: 10.4255/mcpharmacol.09.07     Document Type: Review

References (106)

1. Massague J. The transforming growth factor-beta family. Annu Rev Cell Biol 1990;6:597-641.
2. Derynck R, Akhurst RJ, Balmain A. TGF-beta signaling in tumor suppression and cancer progression. Nat Genet 2001;29:117-29.
3. Jakowlew SB. Transforming growth factor-beta in cancer and metastasis. Cancer Metastasis Rev 2006;25:435-57.
4. Pardali K, Moustakas A. Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochim Biophys Acta 2007;1775:21-62.
5. Gobbi H, Dupont WD, Simpson JF, et al. Transforming growth factor-beta and breast cancer risk in women with mammary epithelial hyperplasia. J Natl Cancer Inst 1999;91:2096-101.
6. Gobbi H, Arteaga CL, Jensen RA, et al. Loss of expression of transforming growth factor beta type II receptor correlates with high tumour grade in human breast in-situ and invasive carcinomas. Histopathology 2000;36:168-77.
7. Attisano L, Wrana JL. Signal transduction by the TGF-beta superfamily. Science 2002;296:1646-7.
8. Miyazono K. TGF-beta signaling by Smad proteins. Cytokine Growth Factor Rev 2000;11:15-22.
9. Liu F. Receptor-regulated Smads in TGF-beta signaling. Front Biosci 2003;8:s1280-303.
10. Feng XH, Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol 2005;21:659-93.
11. Feinberg AP, Tycko B. The history of cancer epigenetics. Nat Rev 2004;4:143-53.
12. Baylin SB. Mechanisms underlying epigenetically mediated gene silencing in cancer. Semin Cancer Biol 2002;12:331-7.
13. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. New Engl J Med 2003;349:2042-54.
14. Allfrey VG, Faulkner R, Mirsky AE. Acetylation and Methylation of Histones and Their Possible Role in the Regulation of Rna Synthesis. Proc Natl Acad Sci USA 1964;51:786-94.
15. Luger K, Richmond TJ. The histone tails of the nucleosome. Curr Opin Genet Dev 1998;8:140-6.
16. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000;403:41-5.
17. Fischle W, Wang Y, Allis CD. Binary switches and modification cassettes in histone biology and beyond. Nature 2003;425:475-9.
18. Wang Y, Fischle W, Cheung W, Jacobs S, Khorasanizadeh S, Allis CD. Beyond the double helix: writing and reading the histone code. Novartis Found Symp 2004;259:3-17; discussion -21, 163-9.
19. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature 1997;389:349-52.
20. Mai A, Massa S, Rotili D, et al. Histone deacetylation in epigenetics: an attractive target for anticancer therapy. Med Res Rev 2005;25:261-309.
21. Jenuwein T, Laible G, Dorn R, Reuter G. SET domain proteins modulate chromatin domains in eu- and heterochromatin. Cell Mol Life Sci 1998;54:80-93.
22. Rea S, Eisenhaber F, O'Carroll D, et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 2000;406:593-9.
23. Jenuwein T. Re-SET-ting heterochromatin by histone methyltransferases. Trends in cell biology 2001;11:266-73.
24. Lachner M, Jenuwein T. The many faces of histone lysine methylation. Curr Opin Cell Biol 2002;14:286-98.
25. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 2001;410:116-20.
26. Peters AH, Mermoud JE, O'Carroll D, et al. Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nat Gen 2002;30:77-80.
27. Fraga MF, Ballestar E, Villar-Garea A, et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Gen 2005;37:391-400.
28. Stewart MD, Li J, Wong J. Relationship between histone H3 lysine 9 methylation, transcription repression, and heterochromatin protein 1 recruitment. Mol Cell Biol 2005;25:2525-38.
29. Tachibana M, Nozaki M, Takeda N, Shinkai Y. Functional dynamics of H3K9 methylation during meiotic prophase progression. EMBO J 2007;26:3346-59.
30. Patnaik D, Chin HG, Esteve PO, Benner J, Jacobsen SE, Pradhan S. Substrate specificity and kinetic mechanism of mammalian G9a histone H3 methyltransferase. J Biol Chem 2004;279:53248-58.
31. Milner CM, Campbell RD. The G9a gene in the human major histocompatibility complex encodes a novel protein containing ankyrin-like repeats. Biochem J 1993;290 ( Pt 3):811-8.
32. Brown SE, Campbell RD, Sanderson CM. Novel NG36/G9a gene products encoded within the human and mouse MHC class III regions. Mamm Genome 2001;12:916-24.
33. Tachibana M, Ueda J, Fukuda M, et al. Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes Dev 2005;19:815-26.
34. Tachibana M, Matsumura Y, Fukuda M, Kimura H, Shinkai Y. G9a/GLP complexes independently mediate H3K9 and DNA methylation to silence transcription. EMBO J 2008;27:2681-90.
35. Martin C, Zhang Y. The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 2005;6:838-49.
36. Wang H, Cao R, Xia L, et al. Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase. Mol Cell 2001;8:1207-17.
37. Malik S, Roeder RG. Epigenetics? Mediator does that too! Mol Cell 2008;31:305-6.
38. Cloos PA, Christensen J, Agger K, Helin K. Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev 2008;22:1115-40.
39. Nguyen CT, Weisenberger DJ, Velicescu M, et al. Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5-aza-2′-deoxycytidine. Cancer Res 2002;62:6456-61.
40. Wozniak RJ, Klimecki WT, Lau SS, Feinstein Y, Futscher BW. 5-Aza-2′-deoxycytidine-mediated reductions in G9A histone methyltransferase and histone H3 K9 di-methylation levels are linked to tumor suppressor gene reactivation. Oncogene 2007;26:77-90.
41. Coombes MM, Briggs KL, Bone JR, Clayman GL, El-Naggar AK, Dent SY. Resetting the histone code at CDKN2A in HNSCC by inhibition of DNA methylation. Oncogene 2003;22:8902-11.
42. Bartova E, Pachernik J, Harnicarova A, et al. Nuclear levels and patterns of histone H3 modification and HP1 proteins after inhibition of histone deacetylases. Journal Cell Sci 2005;118(Pt 21):5035-46.
43. Wu LP, Wang X, Li L, et al. Histone deacetylase inhibitor depsipeptide activates silenced genes through decreasing both CpG and H3K9 methylation on the promoter. Mol Cell Biol 2008;28:3219-35.
44. McGarvey KM, Fahrner JA, Greene E, Martens J, Jenuwein T, Baylin SB. Silenced tumor suppressor genes reactivated by DNA demethylation do not return to a fully euchromatic chromatin state. Cancer Res 2006;66:3541-9.
45. Sun L, Wu G, Willson JK, et al. Expression of transforming growth factor beta type II receptor leads to reduced malignancy in human breast cancer MCF-7 cells. J Biol Chem 1994;269:26449-55.
46. Brattain MG, Markowitz SD, Willson JK. The type II transforming growth factor-beta receptor as a tumor-suppressor gene. Curr Opin Oncol 1996;8:49-53.
47. Markowitz SD, Roberts AB. Tumor suppressor activity of the TGF-beta pathway in human cancers. Cytokine Growth Factor Rev 1996;7:93-102.
48. Wang J, Han W, Zborowska E, et al. Reduced expression of transforming growth factor beta type I receptor contributes to the malignancy of human colon carcinoma cells. J Biol Chem 1996;271:17366-71.
49. Ko Y, Koli KM, Banerji SS, et al. A kinase-defective transforming growth factor-beta receptor type II is a dominant-negative regulator for human breast carcinoma MCF-7 cells. Int J Oncol 1998;12:87-94.
50. Biswas S, Chytil A, Washington K, et al. Transforming growth factor beta receptor type II inactivation promotes the establishment and progression of colon cancer. Cancer Res 2004;64:4687-92.
51. Kim SJ, Im YH, Markowitz SD, Bang YJ. Molecular mechanisms of inactivation of TGF-beta receptors during carcinogenesis. Cytokine Growth Factor Rev 2000;11:159-68.
52. Park K, Kim SJ, Bang YJ, et al. Genetic changes in the transforming growth factor beta (TGF-beta) type II receptor gene in human gastric cancer cells: correlation with sensitivity to growth inhibition by TGF-beta. Proc Natl Acad Sci USA 1994;91:8772-6.
53. Markowitz S, Wang J, Myeroff L, et al. Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability. Science 1995;268:1336-8.
54. Parsons R, Myeroff LL, Liu B, et al. Microsatellite instability and mutations of the transforming growth factor beta type II receptor gene in colorectal cancer. Cancer Res 1995;55:5548-50.
55. Wang J, Sun L, Myeroff L, et al. Demonstration that mutation of the type II transforming growth factor beta receptor inactivates its tumor suppressor activity in replication error-positive colon carcinoma cells. J Biol Chem 1995;270:22044-9.
56. Grady WM, Myeroff LL, Swinler SE, et al. Mutational inactivation of transforming growth factor beta receptor type II in microsatellite stable colon cancers. Cancer Res 1999;59:320-4.
57. Markowitz S. TGF-beta receptors and DNA repair genes, coupled targets in a pathway of human colon carcinogenesis. Biochim Biophys Acta 2000;1470:M13-20.
58. Pinto M, Oliveira C, Cirnes L, et al. Promoter methylation of TGFbeta receptor I and mutation of TGFbeta receptor II are frequent events in MSI sporadic gastric carcinomas. J Pathol 2003;200:32-8.
59. Schmitt FC, Soares R, Gobbi H, et al. Microsatellite instability in medullary breast carcinomas. Int J Cancer 1999;82:644-7.
60. Hougaard S, Norgaard P, Abrahamsen N, Moses HL, Spang-Thomsen M, Skovgaard Poulsen H. Inactivation of the transforming growth factor beta type II receptor in human small cell lung cancer cell lines. Br J Cancer 1999;79:1005-11.
61. Schmidt WM, Sedivy R, Forstner B, Steger GG, Zochbauer-Muller S, Mader RM. Progressive up-regulation of genes encoding DNA methyltransferases in the colorectal adenoma-carcinoma sequence. Mol Carcinog 2007;46:766-72.
62. Ogino S, Kawasaki T, Ogawa A, Kirkner GJ, Loda M, Fuchs CS. TGFBR2 mutation is correlated with CpG island methylator phenotype in microsatellite instability-high colorectal cancer. Hum Pathol 2007;38(4):614-20.
63. Teodoridis JM, Hardie C, Brown R. CpG island methylator phenotype (CIMP) in cancer: causes and implications. Cancer Lett 2008;268:177-86.
64. Di Bartolo DL, Cannon M, Liu YF, et al. KSHV LANA inhibits TGF-beta signaling through epigenetic silencing of the TGF-beta type II receptor. Blood 2008;111:4731-
65. Hinshelwood RA, Huschtscha LI, Melki J, et al. Concordant epigenetic silencing of transforming growth factor-beta signaling pathway genes occurs early in breast carcinogenesis. Cancer Res 2007;67:11517-27.
66. Osada H, Tatematsu Y, Sugito N, Horio Y, Takahashi T. Histone modification in the TGFbetaRII gene promoter and its significance for responsiveness to HDAC inhibitor in lung cancer cell lines. Mol Carcinog 2005;44:233-41.
67. Yamashita S, Takahashi S, McDonell N, et al. Methylation silencing of transforming growth factor-beta receptor type II in rat prostate cancers. Cancer Res 2008;68:2112-21.
68. Hemavathy KC, Chang TH, Zhang H, et al. Reduced expression of TGF beta1RII in agnogenic myeloid metaplasia is not due to mutation or methylation. Leuk Res 2006;30:47-53.
69. Osada H, Tatematsu Y, Sugito N, Horio Y, Takahashi T. Histone modification in the TGFbetaRII gene promoter and its significance for responsiveness to HDAC inhibitor in lung cancer cell lines. Mol Carcinog 2005;44:233-41.
70. Bae HW, Geiser AG, Kim DH, et al. Characterization of the promoter region of the human transforming growth factor-beta type II receptor gene. J Biol Chem 1995;270:29460-8.
71. Suske G. The Sp-family of transcription factors. Gene 1999;238:291-300.
72. Ammanamanchi S, Kim SJ, Sun LZ, Brattain MG. Induction of transforming growth factor-beta receptor type II expression in estrogen receptor-positive breast cancer cells through SP1 activation by 5-aza-2'-deoxycytidine. J Biol Chem 1998;273:16527-34.
73. Periyasamy S, Ammanamanchi S, Tillekeratne MP, Brattain MG. Repression of transforming growth factor-beta receptor type I promoter expression by Sp1 deficiency. Oncogene 2000;19:4660-7.
74. Ammanamanchi S, Brattain MG. Sp3 is a transcriptional repressor of transforming growth factor-beta receptors. J Biol Chem 2001a;276:3348-52.
75. Ammanamanchi S, Brattain MG. 5-azaC treatment enhances expression of transforming growth factor-beta receptors through down-regulation of Sp3. The Journal of biological chemistry 2001b;276:32854-9.
76. Ammanamanchi S, Freeman JW, Brattain MG. Acetylated sp3 is a transcriptional activator. J Biol Chem 2003;278:35775-80.
77. Spengler ML, Brattain MG. Sumoylation inhibits cleavage of Sp1 N-terminal negative regulatory domain and inhibits Sp1-dependent transcription. J Biol Chem 2006;281:5567-74.
78. Venkatasubbarao K, Ammanamanchi S, Brattain MG, Mimari D, Freeman JW. Reversion of transcriptional repression of Sp1 by 5 aza-2′ deoxycytidine restores TGF-beta type II receptor expression in the pancreatic cancer cell line MIA PaCa-2. Cancer Res 2001;61:6239-47.
79. Huang W, Zhao S, Ammanamanchi S, Brattain M, Venkatasubbarao K, Freeman JW. Trichostatin A induces transforming growth factor beta type II receptor promoter activity and acetylation of Sp1 by recruitment of PCAF/p300 to a Sp1.NF-Y complex. J Biol Chem 2005;280:10047-54.
80. Zhao S, Venkatasubbarao K, Li S, Freeman JW. Requirement of a specific Sp1 site for histone deacetylase-mediated repression of transforming growth factor beta Type II receptor expression in human pancreatic cancer cells. Cancer Res 2003;63:2624-30.
81. Thiagalingam S, Cheng KH, Lee HJ, Mineva N, Thiagalingam A, Ponte JF. Histone deacetylases: unique players in shaping the epigenetic histone code. Ann N Y Acad Sci 2003;983:84-100.
82. Carew JS, Giles FJ, Nawrocki ST. Histone deacetylase inhibitors: mechanisms of cell death and promise in combination cancer therapy. Cancer Lett 2008;269:7-17.
83. Glaser KB. HDAC inhibitors: clinical update and mechanism-based potential. Biochem Pharmacol 2007;74:659-71.
84. Glozak MA, Seto E. Histone deacetylases and cancer. Oncogene 2007;26:5420-32.
85. Mehnert JM, Kelly WK. Histone deacetylase inhibitors: biology and mechanism of action. Cancer J 2007;13:23-9.
86. Sigalotti L, Fratta E, Coral S, et al. Epigenetic drugs as pleiotropic agents in cancer treatment: biomolecular aspects and clinical applications. J Cell Physiol 2007;212:330-44.
87. Ishihama K, Yamakawa M, Semba S, et al. Expression of HDAC1 and CBP/p300 in human colorectal carcinomas. J Clin Pathol 2007;60:1205-10.
88. Mariadason JM. HDACs and HDAC inhibitors in colon cancer. Epigenetics 2008;3:28-37.
89. Weichert W, Denkert C, Noske A, et al. Expression of class I histone deacetylases indicates poor prognosis in endometrioid subtypes of ovarian and endometrial carcinomas. Neoplasia 2008;10:1021-7.
90. Weichert W, Denkert C, Noske A, et al. Expression of class I histone deacetylases indicates poor prognosis in endometrioid subtypes of ovarian and endometrial carcinomas. Neoplasia 2008;10:1021-7.
91. Weichert W, Roske A, Niesporek S, et al. Class I histone deacetylase expression has independent prognostic impact in human colorectal cancer: specific role of class I histone deacetylases in vitro and in vivo. Clin Cancer Res 2008;14:1669-77.
92. Song J, Noh JH, Lee JH, et al. Increased expression of histone deacetylase 2 is found in human gastric cancer. Apmis 2005;113:264-8.
93. Weichert W, Roske A, Gekeler V, et al. Histone deacetylases 1, 2 and 3 are highly expressed in prostate cancer and HDAC2 expression is associated with shorter PSA relapse time after radical prostatectomy. Br J Cancer 2008;98:604-10.
94. Osada H, Tatematsu Y, Saito H, Yatabe Y, Mitsudomi T, Takahashi T. Reduced expression of class II histone deacetylase genes is associated with poor prognosis in lung cancer patients. Int J Cancer 2004;112:26-32.
95. Dejligbjerg M, Grauslund M, Litman T, et al. Differential effects of class I isoform histone deacetylase depletion and enzymatic inhibition by belinostat or valproic acid in HeLa cells. Mol Cancer 2008;7:70.
96. Khan N, Jeffers M, Kumar S, et al. Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem J 2008;409:581-9.
97. Wang J, Yang L, Yang J, et al. Transforming growth factor beta induces apoptosis through repressing the phosphoinositide 3-kinase/AKT/survivin pathway in colon cancer cells. Cancer Res 2008;68:3152-60.
98. Hostetter CL, Licata LA, Keen JC. Timing is everything: Order of administration of 5-aza 2′ deoxycytidine, trichostatin A and tamoxifen changes estrogen receptor mRNA expression and cell sensitivity. Cancer Lett 2008. Article in press.
99. Li F, Ling X, Huang H, et al. Differential regulation of survivin expression and apoptosis by vitamin D3 compounds in two isogenic MCF-7 breast cancer cell sublines. Oncogene 2005;24:1385-95.
100. Yang L, Yang J, Venkateswarlu S, Ko T, Brattain MG. Autocrine TGFbeta signaling mediates vitamin D3 analog-induced growth inhibition in breast cells. J Cell Physiol 2001;188:383-93.
101. Anumanthan G, Halder SK, Osada H, et al. Restoration of TGF-beta signalling reduces tumorigenicity in human lung cancer cells. Br J Cancer 2005;93:1157-67.
102. Chinnaiyan P, Allen GW, Harari PM. Radiation and new molecular agents, part II: targeting HDAC, HSP90, IGF-1R, PI3K, and Ras. Semin Radiat Oncol 2006;16:59-64.
103. Yoshikawa M, Hishikawa K, Marumo T, Fujita T. Inhibition of histone deacetylase activity suppresses epithelial-to-mesenchymal transition induced by TGF-beta1 in human renal epithelial cells. J Am Soc Nephrol 2007;18:58-65.
104. Kumagai T, Wakimoto N, Yin D, et al. Histone deacetylase inhibitor, suberoylanilide hydroxamic acid (Vorinostat, SAHA) profoundly inhibits the growth of human pancreatic cancer cells. Int J Cancer 2007;121:656-65.
105. Witta SE, Gemmill RM, Hirsch FR, et al. Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res 2006;66:944-50.
106. Digel W, Lubbert M. DNA methylation disturbances as novel therapeutic target in lung cancer: preclinical and clinical results. Crit Rev Oncol Hematol 2005;55:1-11.