YY1 is indispensable for Lgr5+ intestinal stem cell renewal

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 21, 2014, Pages 7695-7700

  Perekatt, Ansu O ^a   Valdez, Michael J ^a   Davila, Melanie ^a   Hoffman, A ^a   Bonder, Edward M ^b   Gao, Nan ^b   Verzi, Michael P ^a  

^a Life Sciences Building Rutgers University   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Crypt base columnar cell; Mitochondria; Transcriptional regulation

Indexed keywords

BMI1 PROTEIN; CASPASE 3; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 5; HISTONE H2AX; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TRANSCRIPTION FACTOR YY1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL LINEAGE; CELL METABOLISM; CELL POPULATION; CELL PROLIFERATION; CELL RENEWAL; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CRYPT CELL; DNA DAMAGE; ENERGY METABOLISM; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION PROFILING; HOMEOSTASIS; IMMUNOREACTIVITY; INTESTINE CELL; INTESTINE VILLUS; METABOLIC REGULATION; MITOSIS INDEX; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROGENY; PROTEIN BINDING; STEM CELL;

CRYPT BASE COLUMNAR CELL; MITOCHONDRIA; TRANSCRIPTIONAL REGULATION;

ANIMALS; CELL DIVISION; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; INTESTINES; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELLS; YY1 TRANSCRIPTION FACTOR;

EID: 84901659560     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1400128111     Document Type: Article

References (63)

1. Clevers H (2013) The intestinal crypt, a prototype stem cell compartment. Cell 154(2): 274-284.
2. Sangiorgi E, Capecchi MR (2008) Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40(7):915-920. (Pubitemid 351913652)
3. Barker N, van Oudenaarden A, Clevers H (2012) Identifying the stem cell of the intestinal crypt: Strategies and pitfalls. Cell Stem Cell 11(4):452-460.
4. Montgomery RK, et al. (2011) Mouse telomerase reverse transcriptase (mTert) expression marks slowly cycling intestinal stem cells. Proc Natl Acad Sci USA 108(1): 179-184.
5. Takeda N, et al. (2011) Interconversion between intestinal stem cell populations in distinct niches. Science 334(6061):1420-1424.
6. Powell AE, et al. (2012) The pan-ErbB negative regulator Lrig1 is an intestinal stem cell marker that functions as a tumor suppressor. Cell 149(1):146-158.
7. Wong VW, et al. (2012) Lrig1 controls intestinal stem-cell homeostasis by negative regulation of ErbB signalling. Nat Cell Biol 14(4):401-408.
8. Van Landeghem L, et al. (2012) Activation of two distinct Sox9-EGFP-expressing intestinal stem cell populations during crypt regeneration after irradiation. Am J Physiol Gastrointest Liver Physiol 302(10):G1111-G1132.
9. Itzkovitz S, et al. (2012) Single-molecule transcript counting of stem-cell markers in the mouse intestine. Nat Cell Biol 14(1):106-114.
10. Snippert HJ, et al. (2010) Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143(1):134-144.
11. Bravo R, Axelrod DE (2013) A calibrated agent-based computer model of stochastic cell dynamics in normal human colon crypts useful for in silico experiments. Theor Biol Med Model 10(1):66.
12. Barker N, et al. (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457(7229):608-611.
13. O'Brien LE, Soliman SS, Li X, Bilder D (2011) Altered modes of stem cell division drive adaptive intestinal growth. Cell 147(3):603-614.
14. McLeod CJ, Wang L, Wong C, Jones DL (2010) Stem cell dynamics in response to nutrient availability. Curr Biol 20(23):2100-2105.
15. Choi NH, Lucchetta E, Ohlstein B (2011) Nonautonomous regulation of Drosophila midgut stem cell proliferation by the insulin-signaling pathway. Proc Natl Acad Sci USA 108(46):18702-18707.
16. Yilmaz OH, et al. (2012) mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 486(7404):490-495.
17. Stringari C, et al. (2012) Metabolic trajectory of cellular differentiation in small intestine by Phasor Fluorescence Lifetime Microscopy of NADH. Sci Rep 2:568.
18. Myant KB, et al. (2013) ROS production and NF-κB activation triggered by RAC1 facilitate WNT-driven intestinal stem cell proliferation and colorectal cancer initiation. Cell Stem Cell 12(6):761-773.
19. Rera M, et al. (2011) Modulation of longevity and tissue homeostasis by the Dro-sophila PGC-1 homolog. Cell Metab 14(5):623-634.
20. Berns KI, Bohenzky RA (1987) Adeno-associated viruses: An update. Adv Virus Res 32: 243-306.
21. Chang LS, Shi Y, Shenk T (1989) Adeno-associated virus P5 promoter contains an adenovirus E1A-inducible element and a binding site for the major late transcription factor. J Virol 63(8):3479-3488. (Pubitemid 19181410)
22. Shi Y, Seto E, Chang LS, Shenk T (1991) Transcriptional repression by YY1, a human GLI-Krüppel-related protein, and relief of repression by adenovirus E1A protein. Cell 67(2):377-388. (Pubitemid 121001453)
23. Park K, Atchison ML (1991) Isolation of a candidate repressor/activator, NF-E1 (YY-1, delta), that binds to the immunoglobulin kappa 3′ enhancer and the immunoglobulin heavy-chain mu E1 site. Proc Natl Acad Sci USA 88(21):9804-9808. (Pubitemid 21915722)
24. Hariharan N, Kelley DE, Perry RP (1991) Delta, a transcription factor that binds to downstream elements in several polymerase II promoters, is a functionally versatile zinc finger protein. Proc Natl Acad Sci USA 88(21):9799-9803. (Pubitemid 21915721)
25. Gregoire S, et al. (2013) Essential and unexpected role of Yin Yang 1 to promote mesodermal cardiac differentiation. Circ Res 112(6):900-910.
26. Lu L, et al. (2013) Genome-wide survey by ChIP-seq reveals YY1 regulation of lincRNAs in skeletal myogenesis. EMBO J 32(19):2575-2588.
27. Blättler SM, et al. (2012) Yin Yang 1 deficiency in skeletal muscle protects against rapamycin-induced diabetic-like symptoms through activation of insulin/IGF signaling. Cell Metab 15(4):505-517.
28. Blättler SM, et al. (2012) Defective mitochondrial morphology and bioenergetic function in mice lacking the transcription factor Yin Yang 1 in skeletal muscle. Mol Cell Biol 32(16):3333-3346.
29. Lu L, et al. (2012) A novel YY1-miR-1 regulatory circuit in skeletal myogenesis revealed by genome-wide prediction of YY1-miRNA network. PLoS ONE 7(2):e27596.
30. Wang H, et al. (2008) NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myo-genesis and rhabdomyosarcoma. Cancer Cell 14(5):369-381.
31. Pan X, et al. (2013) YY1 controls Igκ repertoire and B-cell development, and localizes with condensin on the Igκ locus. EMBO J 32(8):1168-1182.
32. Zaprazna K, Atchison ML (2012) YY1 controls immunoglobulin class switch recombination and nuclear activation-induced deaminase levels. Mol Cell Biol 32(8): 1542-1554.
33. Liu H, et al. (2007) Yin Yang 1 is a critical regulator of B-cell development. Genes Dev 21(10):1179-1189. (Pubitemid 46789876)
34. Onder TT, et al. (2012) Chromatin-modifying enzymes as modulators of reprogram-ming. Nature 483(7391):598-602.
35. Palacios D, et al. (2010) TNF/p38a/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell 7(4):455-469.
36. Vella P, Barozzi I, Cuomo A, Bonaldi T, Pasini D (2012) Yin Yang 1 extends the Myc-related transcription factors network in embryonic stem cells. Nucleic Acids Res 40(8): 3403-3418.
37. Pan X, et al. (2012) Increased expression of PcG protein YY1 negatively regulates B cell development while allowing accumulation of myeloid cells and LT-HSC cells. PLoS ONE 7(1):e30656.
38. Affar B, et al. (2006) Essential dosage-dependent functions of the transcription factor yin yang 1 in late embryonic development and cell cycle progression. Mol Cell Biol 26(9):3565-3581.
39. el Marjou F, et al. ( 2004) Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39( 3): 186-193. (Pubitemid 39079517)
40. Muncan V, et al. (2006) Rapid loss of intestinal crypts upon conditional deletion of the Wnt/Tcf-4 target gene c-Myc. Mol Cell Biol 26(22):8418-8426. (Pubitemid 44748575)
41. van der Flier LG, et al. (2009) Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 136(5):903-912.
42. Muñoz J, et al. (2012) The Lgr5 intestinal stem cell signature: Robust expression of proposed quiescent '+4' cell markers. EMBO J 31(14):3079-3091.
43. Barker N, et al. (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449(7165):1003-1007. (Pubitemid 350014593)
44. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21(1):70-71. (Pubitemid 29036285)
45. Marshman E, Booth C, Potten CS (2002) The intestinal epithelial stem cell. Bioessays 24(1):91-98. (Pubitemid 34108424)
46. Barker N, van de Wetering M, Clevers H (2008) The intestinal stem cell. Genes Dev 22(14):1856-1864. (Pubitemid 352008634)
47. Zhang F, Fu L, Wang Y (2013) 6-thioguanine induces mitochondrial dysfunction and oxidative DNA damage in acute lymphoblastic leukemia cells. Mol Cell Proteomics 12(12):3803-3811.
48. Liu Y, et al. (2013) Resveratrol protects mouse oocytes from methylglyoxal-induced oxidative damage. PLoS ONE 8(10):e77960.
49. Sharma LK, et al. (2011) Mitochondrial respiratory complex I dysfunction promotes tumorigenesis through ROS alteration and AKT activation. Hum Mol Genet 20(23): 4605-4616.
50. Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120(4): 483-495. (Pubitemid 40269763)
51. Koopman WJ, et al. (2005) Inhibition of complex I of the electron transport chain causes O2-mediated mitochondrial outgrowth. Am J Physiol Cell Physiol 288(6): C1440-C1450. (Pubitemid 40991081)
52. Rosato RR, et al. (2010) Histone deacetylase inhibitors activate NF-kappaB in human leukemia cells through an ATM/NEMO-related pathway. J Biol Chem 285(13): 10064-10077.
53. Woodbine L, Brunton H, Goodarzi AA, Shibata A, Jeggo PA (2011) Endogenously induced DNA double strand breaks arise in heterochromatic DNA regions and require ataxia telangiectasia mutated and Artemis for their repair. Nucleic Acids Res 39(16): 6986-6997.
54. Vilenchik MM, Knudson AG (2003) Endogenous DNA double-strand breaks: Production, fidelity of repair, and induction of cancer. Proc Natl Acad Sci USA 100(22): 12871-12876. (Pubitemid 37339992)
55. Bruskov VI, Malakhova LV, Masalimov ZK, Chernikov AV (2002) Heat-induced formation of reactive oxygen species and 8-oxoguanine, a biomarker of damage to DNA. Nucleic Acids Res 30(6):1354-1363. (Pubitemid 34679713)
56. Assaily W, et al. (2011) ROS-mediated p53 induction of Lpin1 regulates fatty acid oxidation in response to nutritional stress. Mol Cell 44(3):491-501.
57. Li X, May JM (2003) Location and recycling of mitochondrial alpha-tocopherol. Mitochondrion 3(1):29-38.
58. Cunningham JT, et al. (2007) mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 450(7170):736-740. (Pubitemid 350207689)
59. Ito K, et al. (2004) Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431(7011):997-1002. (Pubitemid 39434422)
60. Hua G, et al. (2012) Crypt base columnar stem cells in small intestines of mice are radioresistant. Gastroenterology 143(5):1266-1276.
61. Buczacki SJ, et al. (2013) Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 495(7439):65-69.
62. van Es JH, et al. (2012) Dll1+ secretory progenitor cells revert to stem cells upon crypt damage. Nat Cell Biol 14(10):1099-1104.
63. Madisen L, et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13(1):133-140.