Program specificity for ptf1a in pancreas versus neural tube development correlates with distinct collaborating cofactors and chromatin accessibility

Molecular and Cellular Biology

Volumn 33, Issue 16, 2013, Pages 3166-3179

  Meredith, David M ^a,b,c   Borromeo, Mark D ^a   Deering, Tye G ^a,b,d   Casey, Bradford H ^a   Savage, Trisha K ^a   Mayer, Paul R ^a   Hoang, Chinh ^b   Tung, Kuang Chi ^a   Kumar, Manonmani ^b   Shen, Chengcheng ^a,b,e   Swift, Galvin H ^b   MacDonald, Raymond J ^b   Johnsona, Jane E ^a  

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

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

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d HemoShear LLC   (United States)

^e NONE

Author keywords

[No Author keywords available]

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOX; TRANSCRIPTION FACTOR SOX; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BINDING SITE; BRANCHING MORPHOGENESIS; CELL PROLIFERATION; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DIFFERENTIATION; DNA BINDING; DNA FLANKING REGION; DNA SEQUENCE; EMBRYO; ENDOPLASMIC RETICULUM; ENHANCER REGION; GENE EXPRESSION; MOUSE; MULTIGENE FAMILY; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PANCREAS; PANCREAS DEVELOPMENT; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SIGNAL NOISE RATIO; SIGNAL TRANSDUCTION; SPINAL CORD; TISSUE SPECIFICITY; TRANSCRIPTION INITIATION;

ANIMALS; BASE SEQUENCE; CELL LINE; CHROMATIN; CONSENSUS SEQUENCE; DNA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPATOCYTE NUCLEAR FACTOR 3-BETA; HUMANS; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; MICE; MICE, TRANSGENIC; NEURAL TUBE; PANCREAS; PROTEIN BINDING; SOXB1 TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS;

EID: 84881292705     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00364-13     Document Type: Article

References (55)

1. Mann RS, Lelli KM, Joshi R. 2009. Hox specificity unique roles for cofactors and collaborators. Curr. Top. Dev. Biol. 88:63-101.
2. Kondoh H, Kamachi Y. 2010. SOX-partner code for cell specification: regulatory target selection and underlying molecular mechanisms. Int. J. Biochem. Cell Biol. 42:391-399.
3. Biggin MD. 2011. Animal transcription networks as highly connected, quantitative continua. Dev. Cell 21:611-626.
4. Liu X, Lee CK, Granek JA, Clarke ND, Lieb JD. 2006. Whole-genome comparison of Leu3 binding in vitro and in vivo reveals the importance of nucleosome occupancy in target site selection. Genome Res. 16:1517- 1528.
5. Li XY, Thomas S, Sabo PJ, Eisen MB, Stamatoyannopoulos JA, Biggin MD. 2011. The role of chromatin accessibility in directing the widespread, overlapping patterns of Drosophila transcription factor binding. Genome Biol. 12:R34.
6. Fong AP, Yao Z, Zhong JW, Cao Y, Ruzzo WL, Gentleman RC, Tapscott SJ. 2012. Genetic and epigenetic determinants of neurogenesis and myogenesis. Dev. Cell. 22:721-735.
7. Biddie SC, John S, Sabo PJ, Thurman RE, Johnson TA, Schiltz RL, Miranda TB, Sung MH, Trump S, Lightman SL, Vinson C, Stamatoyannopoulos JA, Hager GL. 2011. Transcription factor AP1 potentiates chromatin accessibility and glucocorticoid receptor binding. Mol. Cell 43:145-155.
8. John S, Sabo PJ, Thurman RE, Sung MH, Biddie SC, Johnson TA, Hager GL, Stamatoyannopoulos JA. 2011. Chromatin accessibility predetermines glucocorticoid receptor binding patterns. Nat. Genet. 43:264- 268.
9. Beres TM, Masui T, Swift GH, Shi L, Henke RM, MacDonald RJ. 2006. PTF1 is an organ-specific and Notch-independent basic helix-loop-helix complex containing the mammalian Suppressor of Hairless (RBP-J) or its paralogue, RBP-L. Mol. Cell. Biol. 26:117-130.
10. Masui T, Long Q, Beres TM, Magnuson MA, MacDonald RJ. 2007. Early pancreatic development requires the vertebrate Suppressor of Hairless (RBPJ) in the PTF1 bHLH complex. Genes Dev. 21:2629-2643.
11. Hori K, Cholewa-Waclaw J, Nakada Y, Glasgow SM, Masui T, Henke RM, Wildner H, Martarelli B, Beres TM, Epstein JA, Magnuson MA, Macdonald RJ, Birchmeier C, Johnson JE. 2008. A nonclassical bHLH Rbpj transcription factor complex is required for specification of GABAergic neurons independent of Notch signaling. Genes Dev. 22: 166 -178.
12. Masui T, Swift GH, Deering T, Shen C, Coats WS, Long Q, Elsasser HP, Magnuson MA, MacDonald RJ. 2010. Replacement of Rbpj with Rbpjl in the PTF1 complex controls the final maturation of pancreatic acinar cells. Gastroenterology 139:270-280.
13. Cockell M, Stevenson BJ, Strubin M, Hagenbuchle O, Wellauer PK. 1989. Identification of a cell-specific DNA-binding activity that interacts with a transcriptional activator of genes expressed in the acinar pancreas. Mol. Cell. Biol. 9:2464-2476.
14. Masui T, Swift GH, Hale MA, Meredith DM, Johnson JE, Macdonald RJ. 2008. Transcriptional autoregulation controls pancreatic Ptf1a expression during development and adulthood. Mol. Cell. Biol. 28:5458- 5468.
15. Henke RM, Savage TK, Meredith DM, Glasgow SM, Hori K, Dumas J, MacDonald RJ, Johnson JE. 2009. Neurog2 is a direct downstream target of the Ptf1a-Rbpj transcription complex in dorsal spinal cord. Development 136:2945-2954.
16. Meredith DM, Masui T, Swift GH, MacDonald RJ, Johnson JE. 2009. Multiple transcriptional mechanisms control Ptf1a levels during neural development including autoregulation by the PTF1-J complex. J. Neurosci. 29:11139-11148.
17. Thompson N, Gesina E, Scheinert P, Bucher P, Grapin-Botton A. 2012. RNA profiling and chromatin immunoprecipitation-sequencing reveal that PTF1a stabilizes pancreas progenitor identity via the control of MNX1/HLXB9 and a network of other transcription factors. Mol. Cell. Biol. 32:1189-1199.
18. Krapp A, Knofler M, Ledermann B, Burki K, Berney C, Zoerkler N, Hagenbuchle O, Wellauer PK. 1998. The bHLH protein PTF1-p48 is essential for the formation of the exocrine and the correct spatial organization of the endocrine pancreas. Genes Dev. 12:3752-3763.
19. Glasgow SM, Henke RM, Macdonald RJ, Wright CV, Johnson JE. 2005. Ptf1a determines GABAergic over glutamatergic neuronal cell fate in the spinal cord dorsal horn. Development 132:5461-5469.
20. Hoshino M, Nakamura S, Mori K, Kawauchi T, Terao M, Nishimura YV, Fukuda A, Fuse T, Matsuo N, Sone M, Watanabe M, Bito H, Terashima T, Wright CV, Kawaguchi Y, Nakao K, Nabeshima Y. 2005. Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 47:201-213.
21. Fujitani Y, Fujitani S, Luo H, Qiu F, Burlison J, Long Q, Kawaguchi Y, Edlund H, MacDonald RJ, Furukawa T, Fujikado T, Magnuson MA, Xiang M, Wright CV. 2006. Ptf1a determines horizontal and amacrine cell fates during mouse retinal development. Development 133:4439- 4450.
22. Pascual M, Abasolo I, Mingorance-Le Meur A, Martinez A, Del Rio JA, Wright CV, Real FX, Soriano E. 2007. Cerebellar GABAergic progenitors adopt an external granule cell-like phenotype in the absence of Ptf1a transcription factor expression. Proc. Natl. Acad. Sci. U. S. A. 104:5193-5198.
23. Kawaguchi Y, Cooper B, Gannon M, Ray M, MacDonald RJ, Wright CV. 2002. The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat. Genet. 32:128-134.
24. Storm R, Cholewa-Waclaw J, Reuter K, Brohl D, Sieber M, Treier M, Muller T, Birchmeier C. 2009. The bHLH transcription factor Olig3 marks the dorsal neuroepithelium of the hindbrain and is essential for the development of brainstem nuclei. Development 136:295-305.
25. Rose SD, Swift GH, Peyton MJ, Hammer RE, MacDonald RJ. 2001. The role of PTF1-P48 in pancreatic acinar gene expression. J. Biol. Chem. 276:44018-44026.
26. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111.
27. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38:576-589.
28. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J. 2003. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374-378.
29. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28:511-515.
30. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G. 2010. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28:495-501.
31. Megason SG, McMahon AP. 2002. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129:2087-2098.
32. Ong CT, Corces VG. 2011. Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat. Rev. Genet. 12:283-293.
33. Ladewig J, Koch P, Brustle O. 2013. Leveling Waddington: the emergence of direct programming and the loss of cell fate hierarchies. Nat. Rev. Mol. Cell Biol. 14:225-236.
34. 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.
35. Nishida K, Hoshino M, Kawaguchi Y, Murakami F. 2010. Ptf1a directly controls expression of immunoglobulin superfamily molecules Nephrin and Neph3 in the developing central nervous system. J. Biol. Chem. 285: 373-380.
36. Mizuhara E, Minaki Y, Nakatani T, Kumai M, Inoue T, Muguruma K, Sasai Y, Ono Y. 2010. Purkinje cells originate from cerebellar ventricular zone progenitors positive for Neph3 and E-cadherin. Dev. Biol. 338:202- 214.
37. Volker LA, Petry M, Abdelsabour-Khalaf M, Schweizer H, Yusuf F, Busch T, Schermer B, Benzing T, Brand-Saberi B, Kretz O, Hohne M, Kispert A. 2012. Comparative analysis of Neph gene expression in mouse and chicken development. Histochem. Cell Biol. 137:355-366.
38. Minaki Y, Mizuhara E, Morimoto K, Nakatani T, Sakamoto Y, Inoue Y, Satoh K, Imai T, Takai Y, Ono Y. 2005. Migrating postmitotic neural precursor cells in the ventricular zone extend apical processes and form adherens junctions near the ventricle in the developing spinal cord. Neurosci. Res. 52:250-262.
39. Putaala H, Soininen R, Kilpelainen P, Wartiovaara J, Tryggvason K. 2001. The murine nephrin gene is specifically expressed in kidney, brain and pancreas: inactivation of the gene leads to massive proteinuria and neonatal death. Hum. Mol. Genet. 10:1-8.
40. van Beest M, Dooijes D, van De Wetering M, Kjaerulff S, Bonvin A, Nielsen O, Clevers H. 2000. Sequence-specific high mobility group box factors recognize 10-12-base pair minor groove motifs. J. Biol. Chem. 275:27266-27273.
41. Maruyama M, Ichisaka T, Nakagawa M, Yamanaka S. 2005. Differential roles for Sox15 and Sox2 in transcriptional control in mouse embryonic stem cells. J. Biol. Chem. 280:24371-24379.
42. Pellerin I, Schnabel C, Catron KM, Abate C. 1994. Hox proteins have different affinities for a consensus DNA site that correlate with the positions of their genes on the hox cluster. Mol. Cell. Biol. 14:4532-4545.
43. Benayoun BA, Caburet S, Dipietromaria A, Bailly-Bechet M, Batista F, Fellous M, Vaiman D, Veitia RA. 2008. The identification and characterization of a FOXL2 response element provides insights into the pathogenesis of mutant alleles. Hum. Mol. Genet. 17:3118-3127.
44. Gao N, LeLay J, Vatamaniuk MZ, Rieck S, Friedman JR, Kaestner KH. 2008. Dynamic regulation of Pdx1 enhancers by Foxa1 and Foxa2 is essential for pancreas development. Genes Dev. 22:3435-3448.
45. Lee CS, Sund NJ, Behr R, Herrera PL, Kaestner KH. 2005. Foxa2 is required for the differentiation of pancreatic alpha-cells. Dev. Biol. 278: 484-495.
46. Sathira N, Yamashita R, Tanimoto K, Kanai A, Arauchi T, Kanematsu S, Nakai K, Suzuki Y, Sugano S. 2010. Characterization of transcription start sites of putative non-coding RNAs by multifaceted use of massively paralleled sequencer. DNA Res. 17:169-183.
47. Xuan S, Borok MJ, Decker KJ, Battle MA, Duncan SA, Hale MA, Macdonald RJ, Sussel L. 2012. Pancreas-specific deletion of mouse Gata4 and Gata6 causes pancreatic agenesis. J. Clin. Invest. 122:3516 - 3528.
48. Bergsland M, Werme M, Malewicz M, Perlmann T, Muhr J. 2006. The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev. 20:3475-3486.
49. Lodato MA, Ng CW, Wamstad JA, Cheng AW, Thai KK, Fraenkel E, Jaenisch R, Boyer LA. 2013. SOX2 co-occupies distal enhancer elements with distinct POU factors in ESCs and NPCs to specify cell state. PLoS Genet. 9:e1003288. doi:10.1371/journal.pgen.1003288.
50. Xu CR, Cole PA, Meyers DJ, Kormish J, Dent Zaret SKS. 2011. Chromatin "prepattern" and histone modifiers in a fate choice for liver and pancreas. Science 332:963-966.
51. Bailey PJ, Klos JM, Andersson E, Karlen M, Kallstrom M, Ponjavic J, Muhr J, Lenhard B, Sandelin A, Ericson J. 2006. A global genomic transcriptional code associated with CNS-expressed genes. Exp. Cell Res. 312:3108-3119.
52. Corbo JC, Lawrence KA, Karlstetter M, Myers CA, Abdelaziz M, Dirkes W, Weigelt K, Seifert M, Benes V, Fritsche LG, Weber BH, Langmann T. 2010. CRX ChIP-seq reveals the cis-regulatory architecture of mouse photoreceptors. Genome Res. 20:1512-1525.
53. Hong JW, Hendrix DA, Levine MS. 2008. Shadow enhancers as a source of evolutionary novelty. Science 321:1314.
54. Frankel N, Davis GK, Vargas D, Wang S, Payre F, Stern DL. 2010. Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 466:490-493.
55. Zaret KS, Carroll JS. 2011. Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 25:2227-2241.