Cell-specific occupancy of an extended repertoire of CREM and CREB binding loci in male germ cells

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Martianov, Igor ^a   Choukrallah, Mohamed Amin ^a   Krebs, Arnaud ^a   Ye, Tao ^a   Legras, Stephanie ^a   Rijkers, Erikjan ^b   Van Ijcken, Wilfred ^b   Jost, Bernard ^a   Sassone Corsi, Paolo ^c   Davidson, Irwin ^a  

^a INSERM   (France)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT MODULATOR; HISTONE H3; RNA POLYMERASE II; HISTONE; LYSINE; MESSENGER RNA; MICRORNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL SHAPE; CELL SPECIFICITY; CELL TYPE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; GENE TARGETING; GERM CELL; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDE MAPPING; PROMOTER REGION; PROTEIN METHYLATION; SPERMATID; SPERMATOGENESIS; SPERMATOGONIUM; TESTIS; TRANSCRIPTION REGULATION; ANIMAL; ANTIBODY SPECIFICITY; CELL LINE; CHROMOSOME; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HAPLOIDY; METABOLISM; METHYLATION; SPERMATOZOON;

ANIMALIA; MURINAE;

ANIMALS; BINDING SITES; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMES, MAMMALIAN; CYCLIC AMP RESPONSE ELEMENT MODULATOR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; GENE EXPRESSION REGULATION; GENETIC LOCI; HAPLOIDY; HISTONES; LYSINE; MALE; METHYLATION; MICE; MICRORNAS; ORGAN SPECIFICITY; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; SPERMATIDS; SPERMATOZOA; TESTIS;

EID: 77957115669     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-530     Document Type: Article

References (48)

1. Sassone-Corsi P. Transcription factors responsive to cAMP. Annu Rev Cell Dev Biol 1995, 11:355-377. 10.1146/annurev.cb.11.110195.002035, 8689562.
2. Hummler E, Cole TJ, Blendy JA, Ganss R, Aguzzi A, Schmid W, Beermann F, Schutz G. Targeted mutation of the CREB gene: compensation within the CREB/ATF family of transcription factors. Proc Natl Acad Sci USA 1994, 91(12):5647-5651. 10.1073/pnas.91.12.5647, 44053, 8202542.
3. Johannessen M, Delghandi MP, Moens U. What turns CREB on?. Cell Signal 2004, 16(11):1211-1227. 10.1016/j.cellsig.2004.05.001, 15337521.
4. Bannister AJ, Kouzarides T. The CBP co-activator is a histone acetyltransferase. Nature 1996, 384:641-643. 10.1038/384641a0, 8967953.
5. Conkright MD, Canettieri G, Screaton R, Guzman E, Miraglia L, Hogenesch JB, Montminy M. TORCs: transducers of regulated CREB activity. Mol Cell 2003, 12(2):413-423. 10.1016/j.molcel.2003.08.013, 14536081.
6. Screaton RA, Conkright MD, Katoh Y, Best JL, Canettieri G, Jeffries S, Guzman E, Niessen S, Yates JR, Takemori H, et al. The CREB coactivator TORC2 functions as a calcium- and cAMP-sensitive coincidence detector. Cell 2004, 119(1):61-74. 10.1016/j.cell.2004.09.015, 15454081.
7. Koo SH, Flechner L, Qi L, Zhang X, Screaton RA, Jeffries S, Hedrick S, Xu W, Boussouar F, Brindle P, et al. The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism. Nature 2005, 437(7062):1109-1111. 10.1038/nature03967, 16148943.
8. Altarejos JY, Goebel N, Conkright MD, Inoue H, Xie J, Arias CM, Sawchenko PE, Montminy M. The Creb1 coactivator Crtc1 is required for energy balance and fertility. Nat Med 2008, 14(10):1112-1117. 10.1038/nm.1866, 2667698, 18758446.
9. Wang B, Goode J, Best J, Meltzer J, Schilman PE, Chen J, Garza D, Thomas JB, Montminy M. The insulin-regulated CREB coactivator TORC promotes stress resistance in Drosophila. Cell Metab 2008, 7(5):434-444. 10.1016/j.cmet.2008.02.010, 18460334.
10. Foulkes NS, Sassone-Corsi P. More is better: activators and repressors from the same gene. Cell 1992, 68(3):411-414. 10.1016/0092-8674(92)90178-F, 1739963.
11. Foulkes NS, Mellstrom B, Benusiglio E, Sassone-Corsi P. Developmental switch of CREM function during spermatogenesis: from antagonist to activator. Nature 1992, 355(6355):80-84. 10.1038/355080a0, 1370576.
12. Foulkes NS, Schlotter F, Pevet P, Sassone-Corsi P. Pituitary hormone FSH directs the CREM functional switch during spermatogenesis. Nature 1993, 362(6417):264-267. 10.1038/362264a0, 7681549.
13. Fimia GM, De Cesare D, Sassone-Corsi P. CBP-independent activation of CREM and CREB by the LIM-only protein ACT. Nature 1999, 398(6723):165-169. 10.1038/18237, 10086359.
14. Nantel F, Monaco L, Foulkes NS, Masquilier D, LeMeur M, Henriksen K, Dierich A, Parvinen M, Sassone-Corsi P. Spermiogenesis deficiency and germ-cell apoptosis in CREM-mutant mice. Nature 1996, 380(6570):159-162. 10.1038/380159a0, 8600390.
15. Blendy JA, Kaestner KH, Weinbauer GF, Nieschlag E, Schutz G. Severe impairment of spermatogenesis in mice lacking the CREM gene. Nature 1996, 380(6570):162-165. 10.1038/380162a0, 8600391.
16. Nantel F, Sassone-Corsi P. CREM: A transcriptional master switch during the spermatogenesis differentiation program. Front Biosci 1996, 1:d266-269.
17. Zhou Y, Sun Z, Means AR, Sassone-Corsi P, Bernstein KE. cAMP-response element modulator tau is a positive regulator of testis angiotensin converting enzyme transcription. Proc Natl Acad Sci USA 1996, 93(22):12262-12266. 10.1073/pnas.93.22.12262, 37978, 8901568.
18. Bailey T. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology 1994, 28-36. AAAI Press, Menlo Park, California.
19. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 2007, 14(11):1025-1040. 10.1038/nsmb1338, 17984965.
20. Chalmel F, Rolland AD, Niederhauser-Wiederkehr C, Chung SS, Demougin P, Gattiker A, Moore J, Patard JJ, Wolgemuth DJ, Jegou B, et al. The conserved transcriptome in human and rodent male gametogenesis. Proc Natl Acad Sci USA 2007, 104(20):8346-8351. 10.1073/pnas.0701883104, 1864911, 17483452.
21. Hofmann MC, Narisawa S, Hess RA, Millan JL. Immortalization of germ cells and somatic testicular cells using the SV40 large T antigen. Exp Cell Res 1992, 201(2):417-435. 10.1016/0014-4827(92)90291-F, 1322317.
22. Montminy MR, Sevarino KA, Wagner JA, Mandel G, Goodman RH. Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc Natl Acad Sci USA 1986, 83(18):6682-6686. 10.1073/pnas.83.18.6682, 386573, 2875459.
23. Beissbarth T, Borisevich I, Horlein A, Kenzelmann M, Hergenhahn M, Klewe-Nebenius A, Klaren R, Korn B, Schmid W, Vingron M, et al. Analysis of CREM-dependent gene expression during mouse spermatogenesis. Mol Cell Endocrinol 2003, 212(1-2):29-39. 10.1016/j.mce.2003.09.023, 14654248.
24. Conkright MD, Guzman E, Flechner L, Su AI, Hogenesch JB, Montminy M. Genome-wide analysis of CREB target genes reveals a core promoter requirement for cAMP responsiveness. Mol Cell 2003, 11(4):1101-1108. 10.1016/S1097-2765(03)00134-5, 12718894.
25. Carninci P, Sandelin A, Lenhard B, Katayama S, Shimokawa K, Ponjavic J, Semple CA, Taylor MS, Engstrom PG, Frith MC, et al. Genome-wide analysis of mammalian promoter architecture and evolution. Nat Genet 2006, 38(6):626-635. 10.1038/ng1789, 16645617.
26. Hinoi E, Ueshima T, Hojo H, Iemata M, Takarada T, Yoneda Y. Up-regulation of per mRNA expression by parathyroid hormone through a protein kinase A-CREB-dependent mechanism in chondrocytes. J Biol Chem 2006, 281(33):23632-23642. 10.1074/jbc.M512362200, 16777848.
27. Cheng HY, Papp JW, Varlamova O, Dziema H, Russell B, Curfman JP, Nakazawa T, Shimizu K, Okamura H, Impey S, et al. microRNA modulation of circadian-clock period and entrainment. Neuron 2007, 54(5):813-829. 10.1016/j.neuron.2007.05.017, 2590749, 17553428.
28. Vo N, Klein ME, Varlamova O, Keller DM, Yamamoto T, Goodman RH, Impey S. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc Natl Acad Sci USA 2005, 102(45):16426-16431. 10.1073/pnas.0508448102, 1283476, 16260724.
29. Wu J, Xie X. Comparative sequence analysis reveals an intricate network among REST, CREB and miRNA in mediating neuronal gene expression. Genome Biol 2006, 7(9):R85. 10.1186/gb-2006-7-9-r85, 1794552, 17002790.
30. Zhang X, Odom DT, Koo SH, Conkright MD, Canettieri G, Best J, Chen H, Jenner R, Herbolsheimer E, Jacobsen E, et al. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci USA 2005, 102(12):4459-4464. 10.1073/pnas.0501076102, 555478, 15753290.
31. Impey S, McCorkle SR, Cha-Molstad H, Dwyer JM, Yochum GS, Boss JM, McWeeney S, Dunn JJ, Mandel G, Goodman RH. Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 2004, 119(7):1041-1054.
32. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 2007, 130(1):77-88. 10.1016/j.cell.2007.05.042, 17632057.
33. Core LJ, Waterfall JJ, Lis JT. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008, 322(5909):1845-1848. 10.1126/science.1162228, 2833333, 19056941.
34. Wilusz JE, Freier SM, Spector DL. 3' end processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell 2008, 135(5):919-932. 10.1016/j.cell.2008.10.012, 2722846, 19041754.
35. Sunwoo H, Dinger ME, Wilusz JE, Amaral PP, Mattick JS, Spector DL. MEN epsilon/beta nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles. Genome Res 2009, 19(3):347-359. 10.1101/gr.087775.108, 2661813, 19106332.
36. Bellora N, Farre D, Alba MM. Positional bias of general and tissue-specific regulatory motifs in mouse gene promoters. BMC Genomics 2007, 8:459. 10.1186/1471-2164-8-459, 2249607, 18078513.
37. Yamashita A, Goto N, Nishiguchi S, Shimada K, Yamanishi H, Yasunaga T. Computational search for over-represented 8-mers within the 5'-regulatory regions of 634 mouse testis-specific genes. Gene 2008, 427(1-2):93-98. 10.1016/j.gene.2008.08.018, 18817858.
38. Euskirchen G, Royce TE, Bertone P, Martone R, Rinn JL, Nelson FK, Sayward F, Luscombe NM, Miller P, Gerstein M, et al. CREB binds to multiple loci on human chromosome 22. Mol Cell Biol 2004, 24(9):3804-3814. 10.1128/MCB.24.9.3804-3814.2004, 387762, 15082775.
39. Cha-Molstad H, Keller DM, Yochum GS, Impey S, Goodman RH. Cell-type-specific binding of the transcription factor CREB to the cAMP-response element. Proc Natl Acad Sci USA 2004, 101(37):13572-13577. 10.1073/pnas.0405587101, 518796, 15342915.
40. Kimmins S, Kotaja N, Davidson I, Sassone-Corsi P. Testis-specific transcription mechanisms promoting male germ-cell differentiation. Reproduction 2004, 128(1):5-12. 10.1530/rep.1.00170, 15232059.
41. Kimmins S, Sassone-Corsi P. Chromatin remodelling and epigenetic features of germ cells. Nature 2005, 434(7033):583-589. 10.1038/nature03368, 15800613.
42. Kolthur-Seetharam U, Martianov I, Davidson I. Specialization of the general transcriptional machinery in male germ cells. Cell Cycle 2008, 7(22):3493-3498.
43. Schmidt EE, Schibler U. High accumulation of components of the RNA polymerase II transcription machinery in rodent spermatids. Development 1995, 121:2373-2383.
44. Schmidt EE, Ohbayashi T, Makino Y, Tamura T, Schibler U. Spermatid-specific overexpression of the TATA-binding protein gene involves recruitment of two potent testis-specific promoters. JBiolChem 1997, 272:5326-5334.
45. Martianov I, Brancorsini S, Catena R, Gansmuller A, Kotaja N, Parvinen M, Sassone-Corsi P, Davidson I. Polar nuclear localization of H1T2, a histone H1 variant, required for spermatid elongation and DNA condensation during spermiogenesis. Proc Natl Acad Sci USA 2005, 102(8):2808-2813. 10.1073/pnas.0406060102, 549447, 15710904.
46. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nussbaum C, Myers RM, Brown M, Li W, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008, 9(9):R137. 10.1186/gb-2008-9-9-r137, 2592715, 18798982.
47. Krebs A, Frontini M, Tora L. GPAT: retrieval of genomic annotation from large genomic position datasets. BMC Bioinformatics 2008, 9:533. 10.1186/1471-2105-9-533, 2654044, 19077303.
48. Delmas V, van der Hoorn F, Mellstrom B, Jegou B, Sassone-Corsi P. Induction of CREM activator proteins in spermatids: down-stream targets and implications for haploid germ cell differentiation. Mol Endocrinol 1993, 7(11):1502-1514. 10.1210/me.7.11.1502, 8114765.