Dynamic transcription programs during ES cell differentiation towards mesoderm in serum versus serum-freeBMP4 culture

BMC Genomics

Volumn 8, Issue , 2007, Pages

  Bruce, Stephen J ^a,b   Gardiner, Brooke B ^a,c,d   Burke, Les J ^a,d   Milena, M Milena ^a,c   Grimmond, Sean M ^a,c,d   Perkins, Andrew C ^a,b,c,d  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b Wesley Research Institute   (Australia)

^c Ritchie Research Laboratories   (Australia)

^d Australian Stem Cell Centre   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CELL DNA; KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 2; OCTAMER TRANSCRIPTION FACTOR 4; UNCLASSIFIED DRUG; BONE MORPHOGENETIC PROTEIN;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; CELL CULTURE; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CULTURE MEDIUM; DEVELOPMENTAL GENETICS; DNA MICROARRAY; DOWN REGULATION; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; INTERMETHOD COMPARISON; MESODERM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DNA BINDING; PROTEIN LOCALIZATION; UNINDEXED SEQUENCE; AMINO ACID SEQUENCE; ANIMAL; CLUSTER ANALYSIS; COMPARATIVE STUDY; CULTURE TECHNIQUE; DRUG EFFECT; ERYTHROPOIESIS; GENETICS; HEART MUSCLE CELL; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; TIME;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BONE MORPHOGENETIC PROTEINS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CLUSTER ANALYSIS; CULTURE MEDIA, SERUM-FREE; EMBRYONIC STEM CELLS; ERYTHROPOIESIS; GENE EXPRESSION PROFILING; MESODERM; MICE; MOLECULAR SEQUENCE DATA; MYOCYTES, CARDIAC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 38349126303     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-8-365     Document Type: Article

References (152)

1. Evans MJ Kaufman MH Establishment in culture of pluripotential cells from mouse embryos Nature 1981, 292(5819):154-156 10.1038/292154a0 7242681
2. Keller G Kennedy M Papayannopoulou T Wiles MV Hematopoietic commitment during embryonic stem cell differentiation in culture Mol Cell Biol 1993, 13(1):473-486 358927 8417345
3. Vittet D Prandini MH Berthier R Schweitzer A Martin-Sisteron H Uzan G Dejana E Embryonic stem cells differentiate in vitro to endothelial cells through successive maturation steps Blood 1996, 88(9):3424-3431 8896407
4. Bain G Kitchens D Yao M Huettner JE Gottlieb DI Embryonic stem cells express neuronal properties in vitro Dev Biol 1995, 168(2):342-357 10.1006/dbio.1995.1085 7729574
5. Rohwedel J Maltsev V Bober E Arnold HH Hescheler J Wobus AM Muscle cell differentiation of embryonic stem cells reflects myogenesis in vivo: developmentally regulated expression of myogenic determination genes and functional expression of ionic currents Dev Biol 1994, 164(1):87-101 10.1006/dbio.1994.1182 8026639
6. Ramalho-Santos M Yoon S Matsuzaki Y Mulligan RC Melton DA "Stemness": Transcriptional profiling of embryonic and adult stem cells Science 2002, 298(5593):597-600 10.1126/science.1072530 12228720
7. Ivanova NB Dimos JT Schaniel C Hackney JA Moore KA Lemischka IR A stem cell molecular signature Science 2002, 298(5593):601-604 10.1126/ science.1073823 12228721
8. Tanaka TS Kunath T Kimber WL Jaradat SA Stagg CA Usuda M Yokota T Niwa H Rossant J Ko MS Gene expression profiling of embryo-derived stem cells reveals candidate genes associated with pluripotency and lineage specificity Genome Res 2002, 12(12):1921-1928 187571 12466296 10.1101/ gr.670002
9. Vogel G Stem cells. 'Stemness' genes still elusive Science 2003, 302(5644):371 10.1126/science.302.5644.371a 14563977
10. Hirst CE Ng ES Azzola L Voss AK Thomas T Stanley EG Elefanty AG Transcriptional profiling of mouse and human ES cells identifies SLAIN1, a novel stem cell gene Dev Biol 2006, 293(1):90-103 10.1016/ j.ydbio.2006.01.023 16546155
11. Bouhon IA Kato H Chandran S Allen ND Neural differentiation of mouse embryonic stem cells in chemically defined medium Brain Res Bull 2005, 68(1-2):62-75 10.1016/j.brainresbull.2005.08.022 16325006
12. Richards M Tan SP Tan JH Chan WK Bongso A The transcriptome profile of human embryonic stem cells as defined by SAGE Stem Cells 2004, 22(1):51-64 10.1634/stemcells.22-1-51 14688391
13. Kuhn K Baker SC Chudin E Lieu MH Oeser S Bennett H Rigault P Barker D McDaniel TK Chee MS A novel, high-performance random array platform for quantitative gene expression profiling Genome Res 2004, 14(11):2347-2356 525694 15520296 10.1101/gr.2739104
14. Okazaki Y Furuno M Kasukawa T Adachi J Bono H Kondo S Nikaido I Osato N Saito R Suzuki H Yamanaka I Kiyosawa H Yagi K Tomaru Y Hasegawa Y Nogami A Schonbach C Gojobori T Baldarelli R Hill DP Bult C Hume DA Quackenbush J Schriml LM Kanapin A Matsuda H Batalov S Beisel KW Blake JA Bradt D Brusic V Chothia C Corbani LE Cousins S Dalla E Dragani TA Fletcher CF Forrest A Frazer KS Gaasterland T Gariboldi M Gissi C Godzik A Gough J Grimmond S Gustincich S Hirokawa N Jackson IJ Jarvis ED Kanai A Kawaji H Kawasawa Y Kedzierski RM King BL Konagaya A Kurochkin IV Lee Y Lenhard B Lyons PA Maglott DR Maltais L Marchionni L McKenzie L Miki H Nagashima T Numata K Okido T Pavan WJ Pertea G Pesole G Petrovsky N Pillai R Pontius JU Qi D Ramachandran S Ravasi T Reed JC Reed DJ Reid J Ring BZ Ringwald M Sandelin A Schneider C Semple CA Setou M Shimada K Sultana R Takenaka Y Taylor MS Teasdale RD Tomita M Verardo R Wagner L Wahlestedt C Wang Y Watanabe Y Wells C Wilming LG Wynshaw-Boris A Yanagisawa M Yang I Yang L Yuan Z Zavolan M Zhu Y Zimmer A Carninci P Hayatsu N Hirozane-Kishikawa T Konno H Nakamura M Sakazume N Sato K Shiraki T Waki K Kawai J Aizawa K Arakawa T Fukuda S Hara A Hashizume W Imotani K Ishii Y Itoh M Kagawa I Miyazaki A Sakai K Sasaki D Shibata K Shinagawa A Yasunishi A Yoshino M Waterston R Lander ES Rogers J Birney E Hayashizaki Y Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs Nature 2002, 420(6915):563-573 10.1038/nature01266 12466851
15. Verdugo RA Medrano JF Comparison of gene coverage of mouse oligonucleotide microarray platforms BMC Genomics 2006, 7(58):1440853-16551360 10.1186/1471-2164-7-58
16. Perkins AC Enrichment of blood from embryonic stem cells in vitro Reprod Fertil Dev 1998, 10(7-8):563-572 10.1071/RD98104 10612462
17. Wiles MV Johansson BM Embryonic stem cell development in a chemically defined medium Exp Cell Res 1999, 247(1):241-248 10.1006/excr.1998.4353 10047466
18. Bhattacharya B Miura T Brandenberger R Mejido J Luo Y Yang AX Joshi BH Ginis I Thies RS Amit M Lyons I Condie BG Itskovitz-Eldor J Rao MS Puri RK Gene expression in human embryonic stem cell lines: Unique molecular signature Blood 2004, 103(8):2956-2964 10.1182/blood-2003-09-3314 15070671
19. Ivanova N Dobrin R Lu R Kotenko I Levorse J DeCoste C Schafer X Lun Y Lemischka IR Dissecting self-renewal in stem cells with RNA interference Nature 2006, 442(7102):533-538 10.1038/nature04915 16767105
20. Nilsson SK Johnston HM Whitty GA Williams B Webb RJ Denhardt DT Bertoncello I Bendall LJ Simmons PJ Haylock DN Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells Blood 2005, 106(4):1232-1239 10.1182/blood-2004-11-4422 15845900
21. Botquin V Hess H Fuhrmann G Anastassiadis C Gross MK Vriend G Scholer HR New POU dimer configuration mediates antagonistic control of an osteopontin preimplantation enhancer by Oct-4 and Sox-2 Genes Dev 1998, 12(13):2073-2090 316977 9649510
22. Jin J Cardozo T Lovering RC Elledge SJ Pagano M Harper JW Systematic analysis and nomenclature of mammalian F-box proteins Genes Dev 2004, 18(21):2573-2580 525538 15520277 10.1101/gad.1255304
23. Tokuzawa Y Kaiho E Maruyama M Takahashi K Mitsui K Maeda M Niwa H Yamanaka S Fbx15 is a novel target of Oct3/4 but is dispensable for embryonic stem cell self-renewal and mouse development Mol Cell Biol 2003, 23(8):2699-2708 152544 12665572 10.1128/MCB.23.8.2699-2708.2003
24. Takahashi K Yamanaka S Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 2006, 126(4):663-676 10.1016/j.cell.2006.07.024 16904174
25. Nichols J Zevnik B Anastassiadis K Niwa H Klewe-Nebenius D Chambers I Scholer H Smith A Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4 Cell 1998, 95(3):379-391 10.1016/S0092-8674(00)81769-9 9814708
26. Avilion AA Nicolis SK Pevny LH Perez L Vivian N Lovell-Badge R Multipotent cell lineages in early mouse development depend on SOX2 function Genes Dev 2003, 17(1):126-140 195970 12514105 10.1101/gad.224503
27. Chambers I Colby D Robertson M Nichols J Lee S Tweedie S Smith A Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells Cell 2003, 113(5):643-655 10.1016/ S0092-8674(03)00392-1 12787505
28. Rosner MH Vigano MA Ozato K Timmons PM Poirier F Rigby PW Staudt LM A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo Nature 1990, 345(6277):686-692 10.1038/345686a0 1972777
29. Wilkinson DG Bhatt S Herrmann BG Expression pattern of the mouse T gene and its role in mesoderm formation Nature 1990, 343(6259):657-659 10.1038/343657a0 1689462
30. Hart AH Hartley L Sourris K Stadler ES Li R Stanley EG Tam PP Elefanty AG Robb L Mixl1 is required for axial mesendoderm morphogenesis and patterning in the murine embryo Development 2002, 129(15):3597-3608 12117810
31. Tsang TE Shawlot W Kinder SJ Kobayashi A Kwan KM Schughart K Kania A Jessell TM Behringer RR Tam PP Lim1 activity is required for intermediate mesoderm differentiation in the mouse embryo Dev Biol 2000, 223(1):77-90 10.1006/dbio.2000.9733 10864462
32. Treichel D Becker MB Gruss P The novel transcription factor gene Sp5 exhibits a dynamic and highly restricted expression pattern during mouse embryogenesis Mech Dev 2001, 101(1-2):175-179 10.1016/ S0925-4773(00)00544-X 11231070
33. Ciruna BG Rossant J Expression of the T-box gene Eomesodermin during early mouse development Mech Dev 1999, 81(1-2):199-203 10.1016/ S0925-4773(98)00243-3 10330500
34. Peifer M Berg S Reynolds AB A repeating amino acid motif shared by proteins with diverse cellular roles Cell 1994, 76(5):789-791 10.1016/ 0092-8674(94)90353-0 7907279
35. Haub O Goldfarb M Expression of the fibroblast growth factor-5 gene in the mouse embryo Development 1991, 112(2):397-406 1794310
36. Gofflot F Hall M Morriss-Kay GM Genetic patterning of the developing mouse tail at the time of posterior neuropore closure Dev Dyn 1997, 210(4):431-445 10.1002/ (SICI)1097-0177(199712)210:4<431::AID-AJA7>3.0.CO;2-H 9415428
37. Okano M Bell DW Haber DA Li E DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development Cell 1999, 99(3):247-257 10.1016/S0092-8674(00)81656-6 10555141
38. Chen Y Amende I Hampton TG Yang Y Ke Q Min JY Xiao YF Morgan JP Vascular endothelial growth factor promotes cardiomyocyte differentiation of embryonic stem cells Am J Physiol Heart Circ Physiol 2006, 291(4):H1653-8 10.1152/ajpheart.00363.2005 16699073
39. Black BL Transcriptional pathways in second heart field development Semin Cell Dev Biol 2007, 18(1):67-76 10.1016/j.semcdb.2007.01.001 17276708
40. Andrews NC Kotkow KJ Ney PA Erdjument-Bromage H Tempst P Orkin SH The ubiquitous subunit of erythroid transcription factor NF-E2 is a small basic-leucine zipper protein related to the v-maf oncogene Proc Natl Acad Sci U S A 1993, 90(24):11488-11492 48009 8265578 10.1073/ pnas.90.24.11488
41. Kihm AJ Kong Y Hong W Russell JE Rouda S Adachi K Simon MC Blobel GA Weiss MJ An abundant erythroid protein that stabilizes free alpha-haemoglobin Nature 2002, 417(6890):758-763 10.1038/nature00803 12066189
42. Miller IJ Bieker JJ A novel, erythroid cell-specific murine transcription factor that binds to the CACCC element and is related to the Kruppel family of nuclear proteins Mol Cell Biol 1993, 13(5):2776-2786 359658 7682653
43. Shaw GC Cope JJ Li L Corson K Hersey C Ackermann GE Gwynn B Lambert AJ Wingert RA Traver D Trede NS Barut BA Zhou Y Minet E Donovan A Brownlie A Balzan R Weiss MJ Peters LL Kaplan J Zon LI Paw BH Mitoferrin is essential for erythroid iron assimilation Nature 2006, 440(7080):96-100 10.1038/nature04512 16511496
44. Philipsen S Suske G A tale of three fingers: The family of mammalian Sp/ XKLF transcription factors Nucleic Acids Res 1999, 27(15):2991-3000 148522 10454592 10.1093/nar/27.15.2991
45. Perkins A Erythroid Kruppel like factor: From fishing expedition to gourmet meal Int J Biochem Cell Biol 1999, 31(10):1175-1192 10.1016/ S1357-2725(99)00083-7 10582346
46. Suske G Bruford E Philipsen S Mammalian SP/KLF transcription factors: bring in the family Genomics 2005, 85(5):551-556 10.1016/ j.ygeno.2005.01.005 15820306
47. Anderson KP Kern CB Crable SC Lingrel JB Isolation of a gene encoding a functional zinc finger protein homologous to erythroid Kruppel-like factor: Identification of a new multigene family Mol Cell Biol 1995, 15(11):5957-5965 230847 7565748
48. Shields JM Christy RJ Yang VW Identification and characterization of a gene encoding a gut-enriched Kruppel-like factor expressed during growth arrest J Biol Chem 1996, 271(33):20009-20017 10.1074/jbc.271.33.20009 8702718
49. Kuo CT Veselits ML Barton KP Lu MM Clendenin C Leiden JM The LKLF transcription factor is required for normal tunica media formation and blood vessel stabilization during murine embryogenesis Genes Dev 1997, 11(22):2996-3006 316695 9367982
50. Segre JA Bauer C Fuchs E Klf4 is a transcription factor required for establishing the barrier function of the skin Nat Genet 1999, 22(4):356-360 10.1038/11926 10431239
51. Li Y McClintick J Zhong L Edenberg HJ Yoder MC Chan RJ Murine embryonic stem cell differentiation is promoted by SOCS-3 and inhibited by the zinc finger transcription factor Klf4 Blood 2005, 105(2):635-637 10.1182/ blood-2004-07-2681 15358627
52. Crossley M Whitelaw E Perkins A Williams G Fujiwara Y Orkin SH Isolation and characterization of the cDNA encoding BKLF/TEF-2, a major CACCC-box-binding protein in erythroid cells and selected other cells Mol Cell Biol 1996, 16(4):1695-1705 231156 8657145
53. Turner J Crossley M Cloning and characterization of mCtBP2, a co-repressor that associates with basic Kruppel-like factor and other mammalian transcriptional regulators Embo J 1998, 17(17):5129-5140 1170841 9724649 10.1093/emboj/17.17.5129
54. Shields JM Yang VW Identification of the DNA sequence that interacts with the gut-enriched Kruppel-like factor Nucleic Acids Res 1998, 26(3):796-802 147321 9443972 10.1093/nar/26.3.796
55. Pavletich NP Pabo CO Zinc finger-DNA recognition: Crystal structure of a Zif268-DNA complex at 2.1 A Science 1991, 252(5007):809-817 10.1126/ science.2028256 2028256
56. Oka S Shiraishi Y Yoshida T Ohkubo T Sugiura Y Kobayashi Y NMR structure of transcription factor Sp1 DNA binding domain Biochemistry 2004, 43(51):16027-16035 10.1021/bi048438p 15609997
57. Feng WC Southwood CM Bieker JJ Analyses of beta-thalassemia mutant DNA interactions with erythroid Kruppel-like factor (EKLF), an erythroid cell-specific transcription factor J Biol Chem 1994, 269(2):1493-1500 8288615
58. van Vliet J Crofts LA Quinlan KG Czolij R Perkins AC Crossley M Human KLF17 is a new member of the Sp/KLF family of transcription factors Genomics 2006, 87(4):474-482 10.1016/j.ygeno.2005.12.011 16460907
59. Fu Y Frith MC Haverty PM Weng Z MotifViz: An analysis and visualization tool for motif discovery Nucleic Acids Res 2004, 32(Web Server issue):W420-3 441564 15215422 10.1093/nar/gkh426
60. Loh YH Wu Q Chew JL Vega VB Zhang W Chen X Bourque G George J Leong B Liu J Wong KY Sung KW Lee CW Zhao XD Chiu KP Lipovich L Kuznetsov VA Robson P Stanton LW Wei CL Ruan Y Lim B Ng HH The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells Nat Genet 2006, 38(4):431-440 10.1038/ng1760 16518401
61. Perkins AC Sharpe AH Orkin SH Lethal beta-thalassaemia in mice lacking the erythroid CACCC- transcription factor EKLF Nature 1995, 375(6529):318-322 10.1038/375318a0 7753195
62. Ben-Shushan E Thompson JR Gudas LJ Bergman Y Rex-1, a gene encoding a transcription factor expressed in the early embryo, is regulated via Oct-3/4 and Oct-6 binding to an octamer site and a novel protein, Rox-1, binding to an adjacent site Mol Cell Biol 1998, 18(4):1866-1878 121416 9528758
63. Wu DY Yao Z Functional analysis of two Sp1/Sp3 binding sites in murine Nanog gene promoter Cell Res 2006, 16(3):319-322 10.1038/sj.cr.7310040 16541131
64. Pesce M Marin Gomez M Philipsen S Scholer HR Binding of Sp1 and Sp3 transcription factors to the Oct-4 gene promoter Cell Mol Biol (Noisy-le-grand) 1999, 45(5):709-716 10512200
65. Nakatake Y Fukui N Iwamatsu Y Masui S Takahashi K Yagi R Yagi K Miyazaki J Matoba R Ko MS Niwa H Klf4 cooperates with Oct3/4 and Sox2 to activate the Lefty1 core promoter in embryonic stem cells Mol Cell Biol 2006, 26(20):7772-7782 1636862 16954384 10.1128/MCB.00468-06
66. Hosler BA Rogers MB Kozak CA Gudas LJ An octamer motif contributes to the expression of the retinoic acid-regulated zinc finger gene Rex-1 (Zfp-42) in F9 teratocarcinoma cells Mol Cell Biol 1993, 13(5):2919-2928 359685 8474450
67. Johansson BM Wiles MV Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development Mol Cell Biol 1995, 15(1):141-151 231923 7799920
68. Hubner K Fuhrmann G Christenson LK Kehler J Reinbold R De La Fuente R Wood J Strauss JF 3rd Boiani M Scholer HR Derivation of oocytes from mouse embryonic stem cells Science 2003, 300(5623):1251-1256 10.1126/ science.1083452 12730498
69. Clark AT Bodnar MS Fox M Rodriquez RT Abeyta MJ Firpo MT Pera RA Spontaneous differentiation of germ cells from human embryonic stem cells in vitro Hum Mol Genet 2004, 13(7):727-739 10.1093/hmg/ddh088 14962983
70. Lacham-Kaplan O Chy H Trounson A Testicular cell conditioned medium supports differentiation of embryonic stem cells into ovarian structures containing oocytes Stem Cells 2006, 24(2):266-273 10.1634/ stemcells.2005-0204 16109761
71. Schultheiss TM Burch JB Lassar AB A role for bone morphogenetic proteins in the induction of cardiac myogenesis Genes Dev 1997, 11(4):451-462 10.1101/gad.11.4.451 9042859
72. Schultheiss TM Xydas S Lassar AB Induction of avian cardiac myogenesis by anterior endoderm Development 1995, 121(12):4203-4214 8575320
73. Sugi Y Lough J Anterior endoderm is a specific effector of terminal cardiac myocyte differentiation of cells from the embryonic heart forming region Dev Dyn 1994, 200(2):155-162 7919501
74. Zhang H Bradley A Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development Development 1996, 122(10):2977-2986 8898212
75. Tzahor E Lassar AB Wnt signals from the neural tube block ectopic cardiogenesis Genes Dev 2001, 15(3):255-260 312627 11159906 10.1101/ gad.871501
76. Kawai T Takahashi T Esaki M Ushikoshi H Nagano S Fujiwara H Kosai K Efficient cardiomyogenic differentiation of embryonic stem cell by fibroblast growth factor 2 and bone morphogenetic protein 2 Circ J 2004, 68(7):691-702 10.1253/circj.68.691 15226637
77. Hosseinkhani M Hosseinkhani H Khademhosseini A Bolland F Kobayashi H Prat Gonzalez S Bone morphogenetic protein-4 enhances cardiomyocyte differentiation of cynomolgus monkey ES cells in Knockout Serum Replacement medium Stem Cells 2006 17138962
78. Nishii K Shibata Y Mode and determination of the initial contraction stage in the mouse embryo heart Anat Embryol (Berl) 2006, 211(2):95-100 10.1007/s00429-005-0065-x 16320070
79. Zandstra PW Bauwens C Yin T Liu Q Schiller H Zweigerdt R Pasumarthi KB Field LJ Scalable production of embryonic stem cell-derived cardiomyocytes Tissue Eng 2003, 9(4):767-778 10.1089/107632703768247449 13678453
80. Kouskoff V Lacaud G Schwantz S Fehling HJ Keller G Sequential development of hematopoietic and cardiac mesoderm during embryonic stem cell differentiation Proc Natl Acad Sci U S A 2005, 102(37):13170-13175 1201570 16141334 10.1073/pnas.0501672102
81. Drissen R von Lindern M Kolbus A Driegen S Steinlein P Beug H Grosveld F Philipsen S The erythroid phenotype of EKLF-null mice: Defects in hemoglobin metabolism and membrane stability Mol Cell Biol 2005, 25(12):5205-5214 1140573 15923635 10.1128/MCB.25.12.5205-5214.2005
82. Hodge D Coghill E Keys J Maguire T Hartmann B McDowall A Weiss M Grimmond S Perkins A A global role for EKLF in definitive and primitive erythropoiesis Blood 2006, 107(8):3359-3370 1895762 16380451 10.1182/ blood-2005-07-2888
83. Adelman CA Chattopadhyay S Bieker JJ The BMP/BMPR/Smad pathway directs expression of the erythroid-specific EKLF and GATA1 transcription factors during embryoid body differentiation in serum-free media Development 2002, 129(2):539-549 11807044
84. Shie JL Chen ZY O'Brien MJ Pestell RG Lee ME Tseng CC Role of gut-enriched Kruppel-like factor in colonic cell growth and differentiation Am J Physiol Gastrointest Liver Physiol 2000, 279(4):G806-14 11005769
85. Wani MA Means RT Jr. Lingrel JB Loss of LKLF function results in embryonic lethality in mice Transgenic Res 1998, 7(4):229-238 10.1023/ A:1008809809843 9859212
86. Kuo CT Veselits ML Leiden JM LKLF: A transcriptional regulator of single-positive T cell quiescence and survival Science 1997, 277(5334):1986-1990 10.1126/science.277.5334.1986 9302292
87. Meno C Shimono A Saijoh Y Yashiro K Mochida K Ohishi S Noji S Kondoh H Hamada H lefty-1 is required for left-right determination as a regulator of lefty-2 and nodal Cell 1998, 94(3):287-297 10.1016/ S0092-8674(00)81472-5 9708731
88. Ghaleb AM Nandan MO Chanchevalap S Dalton WB Hisamuddin IM Yang VW Kruppel-like factors 4 and 5: The yin and yang regulators of cellular proliferation Cell Res 2005, 15(2):92-96 1317089 15740636 10.1038/ sj.cr.7290271
89. Funnell AP Maloney CA Thompson LJ Keys J Tallack M Perkins AC Crossley M Erythroid Kruppel-like Factor Directly Activates the Basic Kruppel-like Factor Gene in Erythroid Cells Mol Cell Biol 2007 1899893 17283065
90. Wei D Kanai M Huang S Xie K Emerging role of KLF4 in human gastrointestinal cancer Carcinogenesis 2006, 27(1):23-31 10.1093/carcin/ bgi243 16219632
91. Bateman NW Tan D Pestell RG Black JD Black AR Intestinal tumor progression is associated with altered function of KLF5 J Biol Chem 2004, 279(13):12093-12101 10.1074/jbc.M311532200 14726538
92. Heyer LJ Kruglyak S Yooseph S Exploring expression data: Identification and analysis of coexpressed genes Genome Res 1999, 9(11):1106-1115 310826 10568750 10.1101/gr.9.11.1106
93. Stepchenko AG Luchina NN Polanovsky OL Conservative Val47 residue of POU homeodomain: Role in DNA recognition FEBS Lett 1997, 412(1):5-8 10.1016/ S0014-5793(97)00508-5 9257679
94. Merika M Orkin SH DNA-binding specificity of GATA family transcription factors Mol Cell Biol 1993, 13(7):3999-4010 359949 8321207
95. Ovcharenko I Nobrega MA Loots GG Stubbs L ECR Browser: A tool for visualizing and accessing data from comparisons of multiple vertebrate genomes Nucleic Acids Res 2004, 32(Web Server issue):W280-6 441493 15215395 10.1093/nar/gkh355
96. Liaw L Birk DE Ballas CB Whitsitt JS Davidson JM Hogan BL Altered wound healing in mice lacking a functional osteopontin gene (spp1) J Clin Invest 1998, 101(7):1468-1478 508725 9525990
97. Luo J Sladek R Bader JA Matthyssen A Rossant J Giguere V Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-beta Nature 1997, 388(6644):778-782 10.1038/42022 9285590
98. Rodda S Sharma S Scherer M Chapman G Rathjen P CRTR-1, a developmentally regulated transcriptional repressor related to the CP2 family of transcription factors J Biol Chem 2001, 276(5):3324-3332 10.1074/ jbc.M008167200 11073954
99. Rogers MB Hosler BA Gudas LJ Specific expression of a retinoic acid-regulated, zinc-finger gene, Rex-1, in preimplantation embryos, trophoblast and spermatocytes Development 1991, 113(3):815-824 1821852
100. Shi W Wang H Pan G Geng Y Guo Y Pei D Regulation of the pluripotency marker rex-1 by nanog and sox2 J Biol Chem 2006, 281(33):23319-23325 10.1074/jbc.M601811200 16714766
101. Edgar AJ Molecular cloning and tissue distribution of mammalian L-threonine 3-dehydrogenases BMC Biochem 2002, 3:19 117216 12097150 10.1186/1471-2091-3-19
102. Arima T Hata K Tanaka S Kusumi M Li E Kato K Shiota K Sasaki H Wake N Loss of the maternal imprint in Dnmt3Lmat-/- mice leads to a differentiation defect in the extraembryonic tissue Dev Biol 2006, 297(2):361-373 10.1016/j.ydbio.2006.05.003 16920095
103. Yoshikawa T Piao Y Zhong J Matoba R Carter MG Wang Y Goldberg I Ko MS High-throughput screen for genes predominantly expressed in the ICM of mouse blastocysts by whole mount in situ hybridization Gene Expr Patterns 2006, 6(2):213-224 1850761 16325481 10.1016/j.modgep.2005.06.003
104. Franz WM Breves D Klingel K Brem G Hofschneider PH Kandolf R Heart-specific targeting of firefly luciferase by the myosin light chain-2 promoter and developmental regulation in transgenic mice Circ Res 1993, 73(4):629-638 8370121
105. Tonini GP Casalaro A Cara A Di Martino D Inducible expression of calcyclin, a gene with strong homology to S-100 protein, during neuroblastoma cell differentiation and its prevalent expression in Schwann-like cell lines Cancer Res 1991, 51(6):1733-1737 1998963
106. Wang PJ McCarrey JR Yang F Page DC An abundance of X-linked genes expressed in spermatogonia Nat Genet 2001, 27(4):422-426 10.1038/86927 11279525
107. Wulf P Suter U Embryonic expression of epithelial membrane protein 1 in early neurons Brain Res Dev Brain Res 1999, 116(2):169-180 10.1016/ S0165-3806(99)00092-9 10521561
108. Ko MS Kitchen JR Wang X Threat TA Hasegawa A Sun T Grahovac MJ Kargul GJ Lim MK Cui Y Sano Y Tanaka T Liang Y Mason S Paonessa PD Sauls AD DePalma GE Sharara R Rowe LB Eppig J Morrell C Doi H Large-scale cDNA analysis reveals phased gene expression patterns during preimplantation mouse development Development 2000, 127(8):1737-1749 10725249
109. Meno C Takeuchi J Sakuma R Koshiba-Takeuchi K Ohishi S Saijoh Y Miyazaki J ten Dijke P Ogura T Hamada H Diffusion of nodal signaling activity in the absence of the feedback inhibitor Lefty2 Dev Cell 2001, 1(1):127-138 10.1016/S1534-5807(01)00006-5 11703930
110. Sakaguchi T Nishimoto M Miyagi S Iwama A Morita Y Iwamori N Nakauchi H Kiyonari H Muramatsu M Okuda A Putative "stemness" gene jam-B is not required for maintenance of stem cell state in embryonic, neural, or hematopoietic stem cells Mol Cell Biol 2006, 26(17):6557-6570 1592844 16914739 10.1128/MCB.00729-06
111. Scott LM Mueller L Collins SJ E3, a hematopoietic-specific transcript directly regulated by the retinoic acid receptor alpha Blood 1996, 88(7):2517-2530 8839844
112. Vogel W Gish GD Alves F Pawson T The discoidin domain receptor tyrosine kinases are activated by collagen Mol Cell 1997, 1(1):13-23 10.1016/ S1097-2765(00)80003-9 9659899
113. Mootha VK Bunkenborg J Olsen JV Hjerrild M Wisniewski JR Stahl E Bolouri MS Ray HN Sihag S Kamal M Patterson N Lander ES Mann M Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria Cell 2003, 115(5):629-640 10.1016/ S0092-8674(03)00926-7 14651853
114. Wassarman KM Lewandoski M Campbell K Joyner AL Rubenstein JL Martinez S Martin GR Specification of the anterior hindbrain and establishment of a normal mid/hindbrain organizer is dependent on Gbx2 gene function Development 1997, 124(15):2923-2934 9247335
115. Ikonomidis JS Gibson WC Butler JE McClister DM Sweterlitsch SE Thompson RP Mukherjee R Spinale FG Effects of deletion of the tissue inhibitor of matrix metalloproteinases-1 gene on the progression of murine thoracic aortic aneurysms Circulation 2004, 110(11 Suppl 1):II268-73 15364874
116. Katz JP Perreault N Goldstein BG Lee CS Labosky PA Yang VW Kaestner KH The zinc-finger transcription factor Klf4 is required for terminal differentiation of goblet cells in the colon Development 2002, 129(11):2619-2628 12015290
117. Shindo T Manabe I Fukushima Y Tobe K Aizawa K Miyamoto S Kawai-Kowase K Moriyama N Imai Y Kawakami H Nishimatsu H Ishikawa T Suzuki T Morita H Maemura K Sata M Hirata Y Komukai M Kagechika H Kadowaki T Kurabayashi M Nagai R Kruppel-like zinc-finger transcription factor KLF5/BTEB2 is a target for angiotensin II signaling and an essential regulator of cardiovascular remodeling Nat Med 2002, 8(8):856-863 12101409
118. Falender AE Lanz R Malenfant D Belanger L Richards JS Differential expression of steroidogenic factor-1 and FTF/LRH-1 in the rodent ovary Endocrinology 2003, 144(8):3598-3610 10.1210/en.2002-0137 12865342
119. Vasseur S Hoffmeister A Garcia-Montero A Barthet M Saint-Michel L Berthezene P Fiedler F Closa D Dagorn JC Iovanna JL Mice with targeted disruption of p8 gene show increased sensitivity to lipopolysaccharide and DNA microarray analysis of livers reveals an aberrant gene expression response BMC Gastroenterol 2003, 3:25 212298 12959645 10.1186/ 1471-230X-3-25
120. Xu H Gonzalo JA St Pierre Y Williams IR Kupper TS Cotran RS Springer TA Gutierrez-Ramos JC Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice J Exp Med 1994, 180(1):95-109 10.1084/jem.180.1.95 7911822
121. Kobayashi K Hernandez LD Galan JE Janeway CA Jr. Medzhitov R Flavell RA IRAK-M is a negative regulator of Toll-like receptor signaling Cell 2002, 110(2):191-202 10.1016/S0092-8674(02)00827-9 12150927
122. McGowan KM Coulombe PA Onset of keratin 17 expression coincides with the definition of major epithelial lineages during skin development J Cell Biol 1998, 143(2):469-486 10.1083/jcb.143.2.469 9786956
123. Schubart UK Yu J Amat JA Wang Z Hoffmann MK Edelmann W Normal development of mice lacking metablastin (P19), a phosphoprotein implicated in cell cycle regulation J Biol Chem 1996, 271(24):14062-14066 10.1074/jbc.271.24.14062 8662897
124. Takahashi Y Dominici M Swift J Nagy C Ihle JN Trophoblast stem cells rescue placental defect in SOCS3-deficient mice J Biol Chem 2006, 281(17):11444-11445 10.1074/jbc.C600015200 16517610
125. Jin W Broedl UC Monajemi H Glick JM Rader DJ Lipase H, a new member of the triglyceride lipase family synthesized by the intestine Genomics 2002, 80(3):268-273 10.1006/geno.2002.6837 12213196
126. Ishiguro H Furukawa Y Daigo Y Miyoshi Y Nagasawa Y Nishiwaki T Kawasoe T Fujita M Satoh S Miwa N Fujii Y Nakamura Y Isolation and characterization of human NBL4, a gene involved in the beta-catenin/tcf signaling pathway Jpn J Cancer Res 2000, 91(6):597-603 10874211
127. Jiang N Wang X Jhanwar-Uniyal M Darzynkiewicz Z Dai W Polo box domain of Plk3 functions as a centrosome localization signal, overexpression of which causes mitotic arrest, cytokinesis defects, and apoptosis J Biol Chem 2006, 281(15):10577-10582 10.1074/jbc.M513156200 16478733
128. Kim M Geum D Khang I Park YM Kang BM Lee KA Kim K Expression pattern of HSP25 in mouse preimplantation embryo: Heat shock responses during oocyte maturation Mol Reprod Dev 2002, 61(1):3-13 10.1002/mrd.1125 11774370
129. Zhu M Lovell KL Patterson JS Saunders TL Hughes ED Friderici KH Beta-mannosidosis mice: A model for the human lysosomal storage disease Hum Mol Genet 2006, 15(3):493-500 10.1093/hmg/ddi465 16377659
130. Sato M Kimura T Kurokawa K Fujita Y Abe K Masuhara M Yasunaga T Ryo A Yamamoto M Nakano T Identification of PGC7, a new gene expressed specifically in preimplantation embryos and germ cells Mech Dev 2002, 113(1):91-94 10.1016/S0925-4773(02)00002-3 11900980
131. Maki JM Rasanen J Tikkanen H Sormunen R Makikallio K Kivirikko KI Soininen R Inactivation of the lysyl oxidase gene Lox leads to aortic aneurysms, cardiovascular dysfunction, and perinatal death in mice Circulation 2002, 106(19):2503-2509 10.1161/01.CIR.0000038109.84500.1E 12417550
132. Sitzmann J Noben-Trauth K Kamano H Klempnauer KH Expression of B-Myb during mouse embryogenesis Oncogene 1996, 12(9):1889-1894 8649849
133. Tang CJ Lin CY Tang TK Dynamic localization and functional implications of Aurora-C kinase during male mouse meiosis Dev Biol 2006, 290(2):398-410 10.1016/j.ydbio.2005.11.036 16386730
134. Beer HD Bittner M Niklaus G Munding C Max N Goppelt A Werner S The fibroblast growth factor binding protein is a novel interaction partner of FGF-7, FGF-10 and FGF-22 and regulates FGF activity: Implications for epithelial repair Oncogene 2005, 24(34):5269-5277 10.1038/sj.onc.1208560 15806171
135. Razani B Engelman JA Wang XB Schubert W Zhang XL Marks CB Macaluso F Russell RG Li M Pestell RG Di Vizio D Hou H Jr. Kneitz B Lagaud G Christ GJ Edelmann W Lisanti MP Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities J Biol Chem 2001, 276(41):38121-38138 11457855
136. Beddington RS Rashbass P Wilson V Brachyury - a gene affecting mouse gastrulation and early organogenesis Dev Suppl 1992:157-165 1299362
137. Sun X Meyers EN Lewandoski M Martin GR Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo Genes Dev 1999, 13(14):1834-1846 316887 10421635
138. Saga Y Hata N Kobayashi S Magnuson T Seldin MF Taketo MM MesP1: A novel basic helix-loop-helix protein expressed in the nascent mesodermal cells during mouse gastrulation Development 1996, 122(9):2769-2778 8787751
139. Behrens J Jerchow BA Wurtele M Grimm J Asbrand C Wirtz R Kuhl M Wedlich D Birchmeier W Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta Science 1998, 280(5363) 596-599 10.1126/science.280.5363.596 9554852
140. Bouckson-Castaing V Moudjou M Ferguson DJ Mucklow S Belkaid Y Milon G Crocker PR Molecular characterisation of ninein, a new coiled-coil protein of the centrosome J Cell Sci 1996, 109(Pt 1):179-190 8834802
141. Fehling HJ Swat W Laplace C Kuhn R Rajewsky K Muller U von Boehmer H MHC class I expression in mice lacking the proteasome subunit LMP-7 Science 1994, 265(5176):1234-1237 10.1126/science.8066463 8066463
142. Cole TB Wenzel HJ Kafer KE Schwartzkroin PA Palmiter RD Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene Proc Natl Acad Sci U S A 1999, 96(4):1716-1721 15571 9990090 10.1073/pnas.96.4.1716
143. Meissner A Zilles O Varona R Jozefowski K Ritter U Marquez G Hallmann R Korner H CC chemokine ligand 20 partially controls adhesion of naive B cells to activated endothelial cells under shear stress Blood 2003, 102(8):2724-2727 10.1182/blood-2003-01-0007 12816871
144. Li Y Chambers J Pang J Ngo K Peterson PA Leung WP Yang Y Characterization of the mouse proteasome regulator PA28b gene Immunogenetics 1999, 49(3):149-157 10.1007/s002510050476 9914329
145. Ridley SH Ktistakis N Davidson K Anderson KE Manifava M Ellson CD Lipp P Bootman M Coadwell J Nazarian A Erdjument-Bromage H Tempst P Cooper MA Thuring JW Lim ZY Holmes AB Stephens LR Hawkins PT FENS-1 and DFCP1 are FYVE domain-containing proteins with distinct functions in the endosomal and Golgi compartments J Cell Sci 2001, 114(Pt 22):3991-4000 11739631
146. Ossendorp F Fu N Camps M Granucci F Gobin SJ van den Elsen PJ Schuurhuis D Adema GJ Lipford GB Chiba T Sijts A Kloetzel PM Ricciardi-Castagnoli P Melief CJ Differential expression regulation of the alpha and beta subunits of the PA28 proteasome activator in mature dendritic cells J Immunol 2005, 174(12):7815-7822 15944286
147. Mohan WS Jr. Scheer E Wendling O Metzger D Tora L TAF10 (TAF(II)30) is necessary for TFIID stability and early embryogenesis in mice Mol Cell Biol 2003, 23(12):4307-4318 156135 12773572 10.1128/ MCB.23.12.4307-4318.2003
148. Wagner DS Gan L Klein WH Identification of a differentially expressed RNA helicase by gene trapping Biochem Biophys Res Commun 1999, 262(3):677-684 10.1006/bbrc.1999.1208 10471385
149. Shah GN Ulmasov B Waheed A Becker T Makani S Svichar N Chesler M Sly WS Carbonic anhydrase IV and XIV knockout mice: Roles of the respective carbonic anhydrases in buffering the extracellular space in brain Proc Natl Acad Sci U S A 2005, 102(46):16771-16776 1283849 16260723 10.1073/ pnas.0508449102
150. Lau YF Chan KM Sparkes R Male-enhanced antigen gene is phylogenetically conserved and expressed at late stages of spermatogenesis Proc Natl Acad Sci U S A 1989, 86(21):8462-8466 298302 2813404 10.1073/pnas.86.21.8462
151. Kusumi K Sun ES Kerrebrock AW Bronson RT Chi DC Bulotsky MS Spencer JB Birren BW Frankel WN Lander ES The mouse pudgy mutation disrupts Delta homologue Dll3 and initiation of early somite boundaries Nat Genet 1998, 19(3):274-278 10.1038/961 9662403
152. Spencer JA Eliazer S Ilaria RL Jr. Richardson JA Olson EN Regulation of microtubule dynamics and myogenic differentiation by MURF, a striated muscle RING-finger protein J Cell Biol 2000, 150(4):771-784 10.1083/ jcb.150.4.771 10953002