PBX1 genomic pioneer function drives ERα signaling underlying progression in breast cancer

PLoS Genetics

Volumn 7, Issue 11, 2011, Pages

  Magnani, Luca ^a   Ballantyne, Elizabeth B ^a   Zhang, Xiaoyang ^a   Lupien, Mathieu ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR ALPHA; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; TRANSCRIPTION FACTOR PBX1;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER PATIENT; CELL PROLIFERATION; CHROMATIN; CONTROLLED STUDY; EPIGENETICS; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENOME; HUMAN; HUMAN CELL; METASTASIS; PROGNOSIS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

BINDING SITES; BREAST NEOPLASMS; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; DISEASE PROGRESSION; DNA-BINDING PROTEINS; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HUMANS; KAPLAN-MEIER ESTIMATE; PROTO-ONCOGENE PROTEINS; RNA, SMALL INTERFERING; TRANSCRIPTIONAL ACTIVATION; TREATMENT OUTCOME;

EID: 81755160905     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002368     Document Type: Article

References (103)

1. Barrero MJ, Boue S, Izpisua Belmonte JC, (2010) Epigenetic mechanisms that regulate cell identity. Cell Stem Cell 7: 565-570.
2. Meissner A, (2010) Epigenetic modifications in pluripotent and differentiated cells. Nature Biotechnology 28: 1079-1088.
3. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
4. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, et al. (2008) Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454: 766-770.
5. Mikkelsen TS, Hanna J, Zhang X, Ku M, Wernig M, et al. (2008) Dissecting direct reprogramming through integrative genomic analysis. Nature 454: 49-55.
6. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, et al. (2008) FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 132: 958-970.
7. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, et al. (2006) Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38: 1289-1297.
8. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, et al. (2005) Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122: 33-43.
9. Hurtado A, Holmes KA, Geistlinger TR, Hutcheson IR, Nicholson RI, et al. (2008) Regulation of ERBB2 by oestrogen receptor-PAX2 determines response to tamoxifen. Nature 456: 663-U693.
10. Lin CY, Vega VB, Thomsen JS, Zhang T, Kong SL, et al. (2007) Whole-genome cartography of estrogen receptor alpha binding sites. PLoS Genet 3: e87 doi:10.1371/journal.pgen.0030087.
11. Liu Y, Gao H, Marstrand TT, Strom A, Valen E, et al. (2008) The genome landscape of ER alpha- and ER beta-binding DNA regions. Proceedings of the National Academy of Sciences of the United States of America 105: 2604-2609.
12. Hua S, Kallen CB, Dhar R, Baquero MT, Mason CE, et al. (2008) Genomic analysis of estrogen cascade reveals histone variant H2A.Z associated with breast cancer progression. Mol Syst Biol 4: 188.
13. Laganiere J, Deblois G, Lefebvre C, Bataille AR, Robert F, et al. (2005) From the Cover: Location analysis of estrogen receptor alpha target promoters reveals that FOXA1 defines a domain of the estrogen response. Proc Natl Acad Sci U S A 102: 11651-11656.
14. Eeckhoute J, Briche I, Kurowska M, Formstecher P, Laine B, (2006) Hepatocyte nuclear factor 4 alpha ligand binding and F domains mediate interaction and transcriptional synergy with the pancreatic islet LIM HD transcription factor Isl1. Journal of Molecular Biology 364: 567-581.
15. Magnani L, Eeckhoute J, Lupien M, (2011) Pioneer factors: directing transcriptional regulators within the chromatin environment. Trends in Genetics In Press.
16. Cuesta I, Zaret KS, Santisteban P, (2007) The forkhead factor FoxE1 binds to the thyroperoxidase promoter during thyroid cell differentiation and modifies compacted chromatin structure. Mol Cell Biol 27: 7302-7314.
17. Cirillo LA, Lin FR, Cuesta I, Friedman D, Jarnik M, et al. (2002) Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell 9: 279-289.
18. Zaret KS, Watts J, Xu J, Wandzioch E, Smale ST, et al. (2008) Pioneer factors, genetic competence, and inductive signaling: programming liver and pancreas progenitors from the endoderm. Cold Spring Harb Symp Quant Biol 73: 119-126.
19. Smale ST, (2010) Pioneer factors in embryonic stem cells and differentiation. Curr Opin Genet Dev 20: 519-526.
20. Weigel D, Jackle H, (1990) The fork head domain: a novel DNA binding motif of eukaryotic transcription factors? Cell 63: 455-456.
21. Specchia G, Lo Coco F, Vignetti M, Avvisati G, Fazi P, et al. (2001) Extramedullary involvement at relapse in acute promyelocytic leukemia patients treated or not with all-trans retinoic acid: a report by the Gruppo Italiano Malattie Ematologiche dell'Adulto. J Clin Oncol 19: 4023-4028.
22. Selleri L, Depew MJ, Jacobs Y, Chanda SK, Tsang KY, et al. (2001) Requirement for Pbx1 in skeletal patterning and programming chondrocyte proliferation and differentiation. Development 128: 3543-3557.
23. Kim SK, Selleri L, Lee JS, Zhang AY, Gu X, et al. (2002) Pbx1 inactivation disrupts pancreas development and in Ipf1-deficient mice promotes diabetes mellitus. Nat Genet 30: 430-435.
24. Schnabel CA, Selleri L, Cleary ML, (2003) Pbx1 is essential for adrenal development and urogenital differentiation. Genesis 37: 123-130.
25. Schnabel CA, Godin RE, Cleary ML, (2003) Pbx1 regulates nephrogenesis and ureteric branching in the developing kidney. Dev Biol 254: 262-276.
26. Kamps MP, Murre C, Sun XH, Baltimore D, (1990) A new homeobox gene contributes the DNA binding domain of the t(1;19) translocation protein in pre-B ALL. Cell 60: 547-555.
27. Park JT, Shih Ie M, Wang TL, (2008) Identification of Pbx1, a potential oncogene, as a Notch3 target gene in ovarian cancer. Cancer Res 68: 8852-8860.
28. Yeh HY, Cheng SW, Lin YC, Yeh CY, Lin SF, et al. (2009) Identifying significant genetic regulatory networks in the prostate cancer from microarray data based on transcription factor analysis and conditional independency. BMC Med Genomics 2: 70.
29. Liu DB, Gu ZD, Cao XZ, Liu H, Li JY, (2005) Immunocytochemical detection of HoxD9 and Pbx1 homeodomain protein expression in Chinese esophageal squamous cell carcinomas. World J Gastroenterol 11: 1562-1566.
30. Kikugawa T, Kinugasa Y, Shiraishi K, Nanba D, Nakashiro K, et al. (2006) PLZF regulates Pbx1 transcription and Pbx1-HoxC8 complex leads to androgen-independent prostate cancer proliferation. Prostate 66: 1092-1099.
31. Crijns AP, de Graeff P, Geerts D, Ten Hoor KA, Hollema H, et al. (2007) MEIS and PBX homeobox proteins in ovarian cancer. Eur J Cancer 43: 2495-2505.
32. Mann RS, Chan SK, (1996) Extra specificity from extradenticle: the partnership between HOX and PBX/EXD homeodomain proteins. Trends Genet 12: 258-262.
33. Moens CB, Selleri L, (2006) Hox cofactors in vertebrate development. Dev Biol 291: 193-206.
34. Laurent A, Bihan R, Omilli F, Deschamps S, Pellerin I, (2008) PBX proteins: much more than Hox cofactors. Int J Dev Biol 52: 9-20.
35. Laurent A, Bihan R, Deschamps S, Guerrier D, Dupe V, et al. (2007) Identification of a new type of PBX1 partner that contains zinc finger motifs and inhibits the binding of HOXA9-PBX1 to DNA. Mech Dev 124: 364-376.
36. Berkes CA, Bergstrom DA, Penn BH, Seaver KJ, Knoepfler PS, et al. (2004) Pbx marks genes for activation by MyoD indicating a role for a homeodomain protein in establishing myogenic potential. Mol Cell 14: 465-477.
37. Wang Y, Yin L, Hillgartner FB, (2001) The homeodomain proteins PBX and MEIS1 are accessory factors that enhance thyroid hormone regulation of the malic enzyme gene in hepatocytes. J Biol Chem 276: 23838-23848.
38. Subramaniam N, Cairns W, Okret S, (1998) Glucocorticoids repress transcription from a negative glucocorticoid response element recognized by two homeodomain-containing proteins, Pbx and Oct-1. J Biol Chem 273: 23567-23574.
39. Eeckhoute J, Lupien M, Meyer CA, Verzi MP, Shivdasani RA, et al. (2009) Cell-type selective chromatin remodeling defines the active subset of FOXA1-bound enhancers. Genome Res 19: 372-380.
40. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, et al. (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10: 515-527.
41. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, et al. (2009) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10: R130.
42. van de Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, et al. (2002) A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 347: 1999-2009.
43. Wang Q, Li W, Zhang Y, Yuan X, Xu K, et al. (2009) Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 138: 245-256.
44. Hurtado A, Holmes KA, Ross-Innes CS, Schmidt D, Carroll JS, (2011) FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nature Genetics 43: 27-U42.
45. Schmidt D, Schwalie PC, Ross-Innes CS, Hurtado A, Brown GD, et al. (2010) A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res 20: 578-588.
46. Welboren WJ, van Driel MA, Janssen-Megens EM, van Heeringen SJ, Sweep FCGJ, et al. (2009) ChIP-Seq of ER alpha and RNA polymerase II defines genes differentially responding to ligands. Embo Journal 28: 1418-1428.
47. Cicatiello L, Mutarelli M, Grober OM, Paris O, Ferraro L, et al. (2010) Estrogen receptor alpha controls a gene network in luminal-like breast cancer cells comprising multiple transcription factors and microRNAs. Am J Pathol 176: 2113-2130.
48. Tsai WW, Wang Z, Yiu TT, Akdemir KC, Xia W, et al. (2010) TRIM24 links a non-canonical histone signature to breast cancer. Nature 468: 927-932.
49. Hu M, Yu J, Taylor JM, Chinnaiyan AM, Qin ZS, (2010) On the detection and refinement of transcription factor binding sites using ChIP-Seq data. Nucleic Acids Res 38: 2154-2167.
50. Joseph R, Orlov YL, Huss M, Sun W, Kong SL, et al. (2010) Integrative model of genomic factors for determining binding site selection by estrogen receptor-alpha. Mol Syst Biol 6: 456.
51. Hua SJ, Kittler R, White KP, (2009) Genomic Antagonism between Retinoic Acid and Estrogen Signaling in Breast Cancer. Cell 137: 1259-1271.
52. Richardson AL, Wang ZGC, De Nicolo A, Lu X, Brown M, et al. (2006) X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 9: 121-132.
53. Butt AJ, McNeil CM, Musgrove EA, Sutherland RL, (2005) Downstream targets of growth factor and oestrogen signalling and endocrine resistance: the potential roles of c-Myc, cyclin D1 and cyclin E. Endocr Relat Cancer 12 (Suppl 1): S47-59.
54. Duan R, Porter W, Safe S, (1998) Estrogen-induced c-fos protooncogene expression in MCF-7 human breast cancer cells: role of estrogen receptor Sp1 complex formation. Endocrinology 139: 1981-1990.
55. Inoue A, Omoto Y, Yamaguchi Y, Kiyama R, Hayashi SI, (2004) Transcription factor EGR3 is involved in the estrogen-signaling pathway in breast cancer cells. J Mol Endocrinol 32: 649-661.
56. Stack G, Kumar V, Green S, Ponglikitmongkol M, Berry M, et al. (1988) Structure and function of the pS2 gene and estrogen receptor in human breast cancer cells. Cancer Treat Res 40: 185-206.
57. Giresi PG, Kim J, McDaniell RM, Iyer VR, Lieb JD, (2007) FAIRE (Formaldehyde-Assisted Isolation of Regulatory Elements) isolates active regulatory elements from human chromatin. Genome Res 17: 877-885.
58. Brykczynska U, Hisano M, Erkek S, Ramos L, Oakeley EJ, et al. (2010) Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nature Structural & Molecular Biology 17: 679-U647.
59. Bhandare R, Schug J, Le Lay J, Fox A, Smirnova O, et al. (2010) Genome-wide analysis of histone modifications in human pancreatic islets. Genome Research 20: 428-433.
60. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108-112.
61. Orford K, Kharchenko P, Lai W, Dao MC, Worhunsky DJ, et al. (2008) Differential H3K4 methylation identifies developmentally poised hematopoietic genes. Developmental Cell 14: 798-809.
62. Serandour AA, Avner S, Percevault F, Demay F, Bizot M, et al. (2011) Epigenetic switch involved in activation of pioneer factor FOXA1-dependent enhancers. Genome Res 21: 555-565.
63. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, et al. (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 98: 10869-10874.
64. Payne SJ, Bowen RL, Jones JL, Wells CA, (2008) Predictive markers in breast cancer-the present. Histopathology 52: 82-90.
65. Badve S, Turbin D, Thorat MA, Morimiya A, Nielsen TO, et al. (2007) FOXA1 expression in breast cancer-correlation with luminal subtype A and survival. Clin Cancer Res 13: 4415-4421.
66. Thorat MA, Marchio C, Morimiya A, Savage K, Nakshatri H, et al. (2008) Forkhead box A1 expression in breast cancer is associated with luminal subtype and good prognosis. J Clin Pathol 61: 327-332.
67. Habashy HO, Powe DG, Rakha EA, Ball G, Paish C, et al. (2008) Forkhead-box A1 (FOXA1) expression in breast cancer and its prognostic significance. Eur J Cancer 44: 1541-1551.
68. Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, et al. (2010) An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat 123: 725-731.
69. Choe SK, Lu P, Nakamura M, Lee J, Sagerstrom CG, (2009) Meis cofactors control HDAC and CBP accessibility at Hox-regulated promoters during zebrafish embryogenesis. Dev Cell 17: 561-567.
70. Hoffman BG, Robertson G, Zavaglia B, Beach M, Cullum R, et al. (2010) Locus co-occupancy, nucleosome positioning, and H3K4me1 regulate the functionality of FOXA2-, HNF4A-, and PDX1-bound loci in islets and liver. Genome Research 20: 1037-1051.
71. Jacobs Y, Schnabel CA, Cleary ML, (1999) Trimeric association of hox and TALE homeodomain proteins mediates Hoxb2 hindbrain enhancer activity. Molecular and Cellular Biology 19: 5134-5142.
72. Chang CP, Shen WF, Rozenfeld S, Lawrence HJ, Largman C, et al. (1995) Pbx Proteins Display Hexapeptide-Dependent Cooperative DNA-Binding with a Subset of Hox Proteins. Genes & Development 9: 663-674.
73. Burda P, Laslo P, Stopka T, (2010) The role of PU.1 and GATA-1 transcription factors during normal and leukemogenic hematopoiesis. Leukemia 24: 1249-1257.
74. Korkola JE, Blaveri E, DeVries S, Moore DH 2nd, Hwang ES, et al. (2007) Identification of a robust gene signature that predicts breast cancer outcome in independent data sets. BMC Cancer 7: 61.
75. Kao KJ, Chang KM, Hsu HC, Huang AT, (2011) Correlation of microarray-based breast cancer molecular subtypes and clinical outcomes: implications for treatment optimization. BMC Cancer 11: 143.
76. Allison KH, Kandalaft PL, Sitlani CM, Dintzis SM, Gown AM, (2011) Routine pathologic parameters can predict Oncotype DX(TM) recurrence scores in subsets of ER positive patients: who does not always need testing? Breast Cancer Res Treat.
77. Toi M, Iwata H, Yamanaka T, Masuda N, Ohno S, et al. (2010) Clinical Significance of the 21-Gene Signature (Oncotype DX) in Hormone Receptor-Positive Early Stage Primary Breast Cancer in the Japanese Population. Cancer 116: 3112-3118.
78. Swanton C, Downward J, (2008) Unraveling the complexity of endocrine resistance in breast cancer by functional genomics. Cancer Cell 13: 83-85.
79. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, et al. (2010) Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol Chapter 19: Unit 19 10: 11-21.
80. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, et al. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
81. Wang K, Sengupta S, Magnani L, Wilson CA, Henry RW, et al. (2010) Brg1 is required for Cdx2-mediated repression of Oct4 expression in mouse blastocysts. PLoS ONE 5: e10622 doi:10.1371/journal.pone.0010622.
82. Lupien M, Meyer CA, Bailey ST, Eeckhoute J, Cook J, et al. (2010) Growth factor stimulation induces a distinct ER(alpha) cistrome underlying breast cancer endocrine resistance. Genes Dev 24: 2219-2227.
83. Ross-Innes CS, Stark R, Holmes KA, Schmidt D, Spyrou C, et al. (2010) Cooperative interaction between retinoic acid receptor-alpha and estrogen receptor in breast cancer. Genes Dev 24: 171-182.
84. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137.
85. Loi S, Haibe-Kains B, Desmedt C, Lallemand F, Tutt AM, et al. (2007) Definition of clinically distinct molecular subtypes in estrogen receptor-positive breast carcinomas through genomic grade. J Clin Oncol 25: 1239-1246.
86. van 't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, et al. (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415: 530-536.
87. Desmedt C, Piette F, Loi S, Wang Y, Lallemand F, et al. (2007) Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin Cancer Res 13: 3207-3214.
88. Loi S, Haibe-Kains B, Desmedt C, Wirapati P, Lallemand F, et al. (2008) Predicting prognosis using molecular profiling in estrogen receptor-positive breast cancer treated with tamoxifen. BMC Genomics 9: 239.
89. Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, et al. (2005) Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 365: 671-679.
90. Sotiriou C, Neo SY, McShane LM, Korn EL, Long PM, et al. (2003) Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proc Natl Acad Sci U S A 100: 10393-10398.
91. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, et al. (2005) Genes that mediate breast cancer metastasis to lung. Nature 436: 518-524.
92. Pawitan Y, Bjohle J, Amler L, Borg AL, Egyhazi S, et al. (2005) Gene expression profiling spares early breast cancer patients from adjuvant therapy: derived and validated in two population-based cohorts. Breast Cancer Research 7: R953-R964.
93. Bittner M, (2005) Expression Project for Oncology- Breast Samples not published.
94. Ivshina AV, George J, Senko O, Mow B, Putti TC, et al. (2006) Genetic reclassification of histologic grade delineates new clinical subtypes of breast cancer. Cancer Research 66: 10292-10301.
95. Schmidt M, Bohm D, von Torne C, Steiner E, Puhl A, et al. (2008) The humoral immune system has a key prognostic impact in node-negative breast cancer. Cancer Research 68: 5405-5413.
96. Zhao HJ, Langerod A, Ji Y, Nowels KW, Nesland JM, et al. (2004) Different gene expression patterns in invasive lobular and ductal carcinomas of the breast. Molecular Biology of the Cell 15: 2523-2536.
97. Lu XS, Lu X, Wang ZCG, Iglehart JD, Zhang XG, et al. (2008) Predicting features of breast cancer with gene expression patterns. Breast Cancer Research and Treatment 108: 191-201.
98. Yu K, Ganesan K, Miller LD, Tan P, (2006) A modular analysis of breast cancer reveals a novel low-grade molecular signature in estrogen receptor- Positive tumors. Clinical Cancer Research 12: 3288-3296.
99. Hess KR, Anderson K, Symmans WF, Valero V, Ibrahim N, et al. (2006) Pharmacogenomic predictor of sensitivity to preoperative chemotherapy with paclitaxel and fluorouracil, doxorubicin, and cyclophosphamide in breast cancer. J Clin Oncol 24: 4236-4244.
100. Kreike B, Halfwerk H, Kristel P, Glas A, Peterse H, et al. (2006) Gene expression profiles of primary breast carcinomas from patients at high risk for local recurrence after breast-conserving therapy. Clin Cancer Res 12: 5705-5712.
101. Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, et al. (2003) Repeated observation of breast tumor subtypes in independent gene expression data sets. Proceedings of the National Academy of Sciences of the United States of America 100: 8418-8423.
102. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, et al. (2000) Molecular portraits of human breast tumours. Nature 406: 747-752.
103. Julka PK, Chacko RT, Nag S, Parshad R, Nair A, et al. (2008) A phase II study of sequential neoadjuvant gemcitabine plus doxorubicin followed by gemcitabine plus cisplatin in patients with operable breast cancer: prediction of response using molecular profiling. British Journal of Cancer 98: 1327-1335.