NFIB regulates transcriptional networks that control the development of prostatic hyperplasia

Endocrinology

Volumn 157, Issue 3, 2016, Pages 1094-1109

  Grabowska, Magdalena M ^a   Kelly, Stephen M ^c   Reese, Amy L ^c   Cates, Justin M ^a   Case, Tom C ^a   Zhang, Jianghong ^a   Degraff, David J ^d   Strand, Douglas W ^e   Miller, Nicole L ^a   Clark, Peter E ^a,b   Hayward, Simon W ^a,f   Gronostajski, Richard M ^g   Anderson, Philip D ^c   Matusik, Robert J ^a,b,h  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

^c SALISBURY UNIVERSITY   (United States)

^d PENN STATE COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^f NorthShore University HealthSystems Research Institute   (United States)

^g UNIVERSITY AT BUFFALO   (United States)

^h VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; ANDROSTANOLONE; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; NUCLEAR FACTOR I; PROTEIN; PROTEIN NFIB; UNCLASSIFIED DRUG; FOXA1 PROTEIN, HUMAN; NFIB PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CASTRATION; CELL CYCLE; CELL DIVISION; CELL EXPANSION; CELL POPULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA SEQUENCE; EMBRYO; ENGRAFTMENT; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IN VIVO STUDY; KIDNEY CAPSULE; LNCAP CELL LINE; LOWER URINARY TRACT SYMPTOM; MALE; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE HYPERTROPHY; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; ANIMAL; CELL PROLIFERATION; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENE SILENCING; GENETICS; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; PROSTATE; PROSTATE TUMOR; SEQUENCE ANALYSIS; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GENE REGULATORY NETWORKS; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, KNOCKOUT; NFI TRANSCRIPTION FACTORS; PROSTATE; PROSTATIC HYPERPLASIA; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, RNA;

EID: 84960538933     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-1312     Document Type: Article

References (64)

1. Marker PC, Donjacour AA, Dahiya R, Cunha GR. Hormonal, cellular, and molecular control of prostatic development. Dev Biol. 2003;253:165-174.
2. Gao N, Ishii K, Mirosevich J, et al. Forkhead box A1 regulates prostate ductal morphogenesis and promotes epithelial cell maturation. Development. 2005;132:3431-3443.
3. De Graff DJ, Grabowska MM, Case TC, et al. FOXA1 deletion in luminal epithelium causes prostatic hyperplasia and alteration of differentiated phenotype. Lab Investig. 2014;94:726-739.
4. Gao N, Zhang J, Rao MA, et al. The role of hepatocyte nuclear factor-3 α (forkhead box A1) and androgen receptor in transcriptional regulation of prostatic genes. Mol Endocrinol. 2003;17:1484-1507.
5. Cirillo LA, Lin FR, Cuesta I, Friedman D, Jarnik M, Zaret KS. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell. 2002;9:279-289.
6. Sun Q, Yu X, Degraff DJ, Matusik RJ. Upstream stimulatory factor 2, a novel FoxA1-interacting protein, is involved in prostate-specific gene expression. Mol Endocrinol. 2009;23:2038-2047.
7. Jia L, Berman BP, Jariwala U, et al. Genomic androgen receptoroccupied regions with different functions, defined by histone acetylation, coregulators and transcriptional capacity. PLoS One. 2008;3:e3645.
8. Grabowska MM, Elliott AD, De Graff DJ, et al. NFI transcription factors interact with FOXA1 to regulate prostate-specific gene expression. Mol Endocrinol. 2014;28:949-964.
9. Kruse U, Sippel AE. Transcription factor nuclear factor I proteins form stable homo- and heterodimers. FEBS Lett. 1994;348:46-50.
10. Chaudhry AZ, Lyons GE, Gronostajski RM. Expression patterns of the four nuclear factor I genes during mouse embryogenesis indicate a potential role in development. Dev Dyn. 1997;208:313-325.
11. Gründer A, Ebel TT, Mallo M, et al. Nuclear factor I-B (Nfib) deficient mice have severe lung hypoplasia. Mech Dev. 2002;112:69-77.
12. Murtagh J, Martin F, Gronostajski RM. The nuclear factor I (NFI) gene family in mammary gland development and function. J Mammary Gland Biol Neoplasia. 2003;8:241-254.
13. Steele-Perkins G, Butz KG, Lyons GE, et al. Essential role for NFI-C/CTF transcription-replication factor in tooth root development. Mol Cell Biol. 2003;23:1075-1084.
14. Steele-Perkins G, Plachez C, Butz KG, et al. The transcription factor gene Nfib is essential for both lung maturation and brain development. Mol Cell Biol. 2005;25:685-698.
15. Driller K, Pagenstecher A, Uhl M, etal. Nuclear factor IX deficiency causes brainmalformationand severe skeletal defects. Mol Cell Biol. 2007;27:3855-3867.
16. Campbell CE, Piper M, Plachez C, et al. The transcription factor Nfix is essential for normal brain development. BMC Dev Biol. 2008;8:52.
17. Messina G, Biressi S, Monteverde S, et al. Nfix regulates fetal-specific transcription in developing skeletal muscle. Cell. 2010;140:554-566.
18. Harris L, Genovesi LA, Gronostajski RM, Wainwright BJ, Piper M. Nuclear factor one transcription factors: divergent functions in developmental versus adult stem cell populations. Dev Dyn 2015;244:227-238.
19. Hsu, YC, Osinski J, Campbell CE, et al. Mesenchymal Nuclear factor I B regulates cell proliferation and epithelial differentiation during lung maturation. Dev Biol. 2011;354:242-252.
20. Waki H, Nakamura M, Yamauchi T, et al. Global mapping of cell type-specific open chromatin by FAIRE-seq reveals the regulatory role of the NFI family in adipocyte differentiation. PLoS Genet 2011;7:e1002311.
21. Betancourt J, Katzman S, Chen B. Nuclear factor one B regulates neuralstem cell differentiation and axonal projectionofcorticofugal neurons. J Comp Neurol 2014;522:6-35.
22. Piper M, Moldrich R, Lindwall C, et al. Multiple non-cell-autonomous defects underlie neocortical callosal dysgenesis in Nfib-deficient mice. Neural Dev. 2009;4:43.
23. Piper M, Barry G, Harvey TJ, et al. NFIB-mediated repression of the epigenetic factor Ezh2 regulates cortical development. J Neurosci. 2014;34:2921-2930.
24. Chang CY, Pasolli HA, Giannopoulou EG, et al. NFIB is a governor of epithelial-melanocyte stem cell behaviour in a shared niche. Nature. 2013;495:98-102.
25. Wang Y, Hayward S, Cao M, Thayer K, Cunha G. Cell differentiation lineage in the prostate. Differentiation. 2001;68:270-279.
26. Hudson DL, Guy AT, Fry P, et al. Epithelial cell differentiation pathways in the human prostate: identification of intermediate phenotypes by keratin expression. J Histochem Cytochem. 2001;49:271-278.
27. Verhagen AP, Aalders TW, Ramaekers FC, et al. Differential expression of keratins in the basal and luminal compartments of rat prostatic epithelium during degeneration and regeneration. Prostate. 1988;13:25-38.
28. Ousset M, Van Keymeulen A, Bouvencourt G, etal. Multipotent and unipotent progenitors contribute to prostate postnatal development. Nat Cell Biol. 2012;14:1131-1138.
29. Sugimura Y, Cunha GR, Donjacour AA. Morphogenesis of ductal networks in the mouse prostate. Biol Reprod. 1986;34:961-971.
30. Sinha AA, Bentley MD. The relationshipofepithelial cell typesinthe ventral prostate glands of castrated mice treated with testosterone. Anat Rec. 1984;208:533-544.
31. Wang ZA, Mitrofanova A, Bergren SK, et al. Lineage analysis of basal epithelial cells reveals their unexpected plasticity and supports a cell-of-origin model for prostate cancer heterogeneity. Nat Cell Biol. 2013;15:274-283.
32. Kwon O-J, Zhang L, Ittmann MM, Xin L. Prostatic inflammation enhances basal-to-luminal differentiation and accelerates initiation of prostate cancer with a basal cell origin. Proc Natl Acad Sci USA. 2014;111:E592-E600.
33. Song CS, Jung MH, Supakar PC, Chatterjee B, Roy AK. Negative regulation of the androgen receptor gene promoter by NFI and an adjacently located multiprotein-binding site. Mol Endocrinol. 1999;13:1487-1496.
34. Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data. Cambridge, UK: Babraham Institute; 2010.
35. Langmead B, Trapnell C, Pop M, Salzberg S. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25.
36. Langmead B. Aligning short sequencing reads with Bowtie. Curr Protoc Bioinformatics. 2010; Chapter 11:Unit 11.7.
37. Heinz S, Benner C, Spann N, et al. Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and Bcell identities. Mol Cell. 2010;38:576-589.
38. Chen H, Butros PC. VennDiagram: Generate high-resolution Venn and Euler plots. BMC Bioinformatics. 2011;12:35.
39. Zhang J, Gao N, De Graff DJ, et al. Characterization of cis elements of the probasin promoter necessary for prostate-specific gene expression. Prostate. 2010;70:934-951.
40. Chen Z, Lan X, Thomas-Ahner JM, et al. Agonist and antagonist switchDNAmotifsrecognizedbyhumanandrogenreceptorinprostate cancer. EMBO J 2015;34:502-516.
41. Pages H, Carlson M, Falcon S, Li N. AnnotationDbi: Annotation Database Interface. R package version 1.28.1.
42. Carlson M. org. Hs.eg.db: Genome wide annotation for human. R package version 1.10.1.
43. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37:1-13.
44. Huangda W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2008;4:44-57.
45. Nickols NG, Dervan PB. Suppression of androgen receptor-mediated gene expression by a sequence-specific DNA-binding polyamide. Proc Natl Acad Sci USA. 2007;104:10418-10423.
46. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics. 2004;20:307-315.
47. Gentleman R. Annotate: Annotation of Microarrays. R package version 1.43.4.
48. Carlson M. Affymetrix Human Genome U133 Plus 2.0 Array annotation data (chip hgu133plus2). R package version 3.0.0.
49. Staack A, Donjacour AA, Brody J, Cunha GR, Carroll P. Mouse urogenital development: a practical approach. Differentiation. 2003;71:402-413.
50. Trapnell C, Roberts A, Goff L, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7:562-578.
51. Lin-Tsai O, Clark PE, Miller NL, et al. Surgical intervention for symptomatic benign prostatic hyperplasia is correlated with expression of the AP-1 transcription factor network. Prostate. 2014;74:669-679.
52. Oudes AJ, Campbell DS, Sorensen CM, Walashek LS, True LD, Liu AY. Transcriptomes of human prostate cells. BMC Genomics. 2006;7:92.
53. Mirosevich J, Bentel JM, Zeps N, Redmond SL, D'Antuono MF, Dawkins HJ. Androgen receptor expression of proliferating basal and luminal cells in adult murine ventral prostate. J Endocrinol. 1999;162:341-350.
54. Signoretti S, Waltregny D, Dilks J, et al. p63 Is a prostate basal cell marker and is required for prostate development. Am J Pathol. 2000;157:1769-1775.
55. Kaplan SA. Update on the American Urological Association guidelines for the treatment of benign prostatic hyperplasia. Rev Urol. 2006;8:S10-S17.
56. Engelen E, Akinci U, Bryne JC, et al. Sox2 cooperates with Chd7 to regulate genes that are mutated in human syndromes. Nat Genet. 2011;43:607-611.
57. Norquay LD, Yang X, Sheppard P, et al. RFX1 and NF-1 associate with P sequences of the human growth hormone locus in pituitary chromatin. Mol Endocrinol. 2003;17:1027-1038.
58. Yu X, Cates JM, Morrissey C, et al. SOX2 expression in the developing, adult, as well as, diseased prostate. Prostate Cancer Prostatic Dis. 2014;17:301-309.
59. Gandaglia G, Briganti A, Gontero P, et al. The role of chronic prostatic inflammation in the pathogenesis and progression of benign prostatic hyperplasia (BPH). BJU Int. 2013;112:432-441.
60. Fujita S, Ito T, Mizutani T, et al. miR-21 gene expression triggered by AP-1 is sustained through a double-negative feedback mechanism. J Mol Biol. 2008;378:492-504.
61. Shin VY, Jin H, Ng EK, et al. NF-κB targets miR-16 and miR-21 in gastric cancer: involvement of prostaglandin E receptors. Carcinogenesis. 2011;32:240-245.
62. Ribas J, Ni X, Haffner M, et al. miR-21: an androgen receptorregulated microRNA that promotes hormone-dependent and hormone-independent prostate cancer growth. Cancer Res. 2009;69:7165-7169.
63. Danielsen JM, Sylvestersen KB, Bekker-Jensen S, et al. Mass spectrometric analysis of lysine ubiquitylation reveals promiscuity at site level. Mol Cell Proteomics 2011;10:M110.003590.
64. Grant M. Identification of SUMOylated proteins in neuroblastoma cells after treatment with hydrogen peroxide or ascorbate. BMB Rep. 2010;43:720-725.