The cytosolic protein G0S2 maintains quiescence in hematopoietic stem cells

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Yamada, Takeshi ^a   Park, Chun Shik ^a   Burns, Audrea ^a   Nakada, Daisuke ^a   Lacorazza, H Daniel ^a  

^a TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CELL PROTEIN; CELL PROTEIN G0S2; GLYCINE; NUCLEOLIN; RETROVIRUS VECTOR; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; G0S2 PROTEIN, MOUSE; PHOSPHOPROTEIN; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL ACTIVITY; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; CELL TRANSPLANTATION; CHIMERA; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; ENDOSOME; FEMUR; GAIN OF FUNCTION MUTATION; GENETIC TRANSCRIPTION; HEMATOPOIETIC STEM CELL; MITOCHONDRION; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; QUIESCENCE; REGULATORY MECHANISM; STEM CELL; ANIMAL; BLOOD CELL; CELL CYCLE; CELL STRAIN 3T3; CELL STRAIN HEK293; CHEMICAL PHENOMENA; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ANIMALS; BLOOD CELLS; CELL CYCLE; CELL CYCLE PROTEINS; CYTOSOL; GENE EXPRESSION REGULATION; HEK293 CELLS; HEMATOPOIETIC STEM CELLS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICE; NIH 3T3 CELLS; PHOSPHOPROTEINS; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOPROTEINS; RNA-BINDING PROTEINS;

EID: 84861664376     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038280     Document Type: Article

References (53)

1. Lacorazza HD, Yamada T, Liu Y, Miyata Y, Sivina M, et al. (2006) The transcription factor MEF/ELF4 regulates the quiescence of primitive hematopoietic cells. Cancer Cell 9: 175-187.
2. Jude CD, Gaudet JJ, Speck NA, Ernst P, (2008) Leukemia and hematopoietic stem cells: balancing proliferation and quiescence. Cell Cycle 7: 586-591.
3. Sandberg ML, Sutton SE, Pletcher MT, Wiltshire T, Tarantino LM, et al. (2005) c-Myb and p300 regulate hematopoietic stem cell proliferation and differentiation. Dev Cell 8: 153-166.
4. Orford KW, Scadden DT, (2008) Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat Rev Genet 9: 115-128.
5. Passegue E, Wagers AJ, (2006) Regulating quiescence: new insights into hematopoietic stem cell biology. Dev Cell 10: 415-417.
6. Russell L, Forsdyke DR, (1991) A human putative lymphocyte G0/G1 switch gene containing a CpG-rich island encodes a small basic protein with the potential to be phosphorylated. DNA Cell Biol 10: 581-591.
7. Cristillo AD, Heximer SP, Russell L, Forsdyke DR, (1997) Cyclosporin A inhibits early mRNA expression of G0/G1 switch gene 2 (G0S2) in cultured human blood mononuclear cells. DNA Cell Biol 16: 1449-1458.
8. Zandbergen F, Mandard S, Escher P, Tan NS, Patsouris D, et al. (2005) The G0/G1 switch gene 2 is a novel PPAR target gene. Biochem J 392: 313-324.
9. Teunissen BE, Smeets PJ, Willemsen PH, De Windt LJ, Van der Vusse GJ, et al. (2007) Activation of PPARdelta inhibits cardiac fibroblast proliferation and the transdifferentiation into myofibroblasts. Cardiovasc Res 75: 519-529.
10. Yang X, Lu X, Lombes M, Rha GB, Chi YI, et al. (2010) The G(0)/G(1) switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase. Cell Metab 11: 194-205.
11. Tokumaru Y, Yamashita K, Osada M, Nomoto S, Sun DI, et al. (2004) Inverse correlation between cyclin A1 hypermethylation and p53 mutation in head and neck cancer identified by reversal of epigenetic silencing. Cancer Res 64: 5982-5987.
12. Kusakabe M, Watanabe K, Emoto N, Aki N, Kage H, et al. (2009) Impact of DNA demethylation of the G0S2 gene on the transcription of G0S2 in squamous lung cancer cell lines with or without nuclear receptor agonists. Biochem Biophys Res Commun 390: 1283-1287.
13. Kao LC, Germeyer A, Tulac S, Lobo S, Yang JP, et al. (2003) Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 144: 2870-2881.
14. Ma Y, Koza-Taylor PH, DiMattia DA, Hames L, Fu H, et al. (2003) Microarray analysis uncovers retinoid targets in human bronchial epithelial cells. Oncogene 22: 4924-4932.
15. Yoon IK, Kim HK, Kim YK, Song IH, Kim W, et al. (2004) Exploration of replicative senescence-associated genes in human dermal fibroblasts by cDNA microarray technology. Exp Gerontol 39: 1369-1378.
16. Nakamura N, Shimaoka Y, Tougan T, Onda H, Okuzaki D, et al. (2006) Isolation and expression profiling of genes upregulated in bone marrow-derived mononuclear cells of rheumatoid arthritis patients. DNA Res 13: 169-183.
17. Kobayashi S, Ito A, Okuzaki D, Onda H, Yabuta N, et al. (2008) Expression profiling of PBMC-based diagnostic gene markers isolated from vasculitis patients. DNA Res 15: 253-265.
18. Koczan D, Guthke R, Thiesen HJ, Ibrahim SM, Kundt G, et al. (2005) Gene expression profiling of peripheral blood mononuclear leukocytes from psoriasis patients identifies new immune regulatory molecules. Eur J Dermatol 15: 251-257.
19. Colmegna I, Diaz-Borjon A, Fujii H, Schaefer L, Goronzy JJ, et al. (2008) Defective proliferative capacity and accelerated telomeric loss of hematopoietic progenitor cells in rheumatoid arthritis. Arthritis Rheum 58: 990-1000.
20. Zhang K, Zhang R, Li X, Yin G, Niu X, (2009) Promoter methylation status of p15 and p21 genes in HPP-CFCs of bone marrow of patients with psoriasis. Eur J Dermatol 19: 141-146.
21. Storck S, Shukla M, Dimitrov S, Bouvet P, (2007) Functions of the histone chaperone nucleolin in diseases. Subcell Biochem 41: 125-144.
22. Mongelard F, Bouvet P, (2007) Nucleolin: a multiFACeTed protein. Trends Cell Biol 17: 80-86.
23. Fahling M, Steege A, Perlewitz A, Nafz B, Mrowka R, et al. (2005) Role of nucleolin in posttranscriptional control of MMP-9 expression. Biochim Biophys Acta 1731: 32-40.
24. Otake Y, Soundararajan S, Sengupta TK, Kio EA, Smith JC, et al. (2007) Overexpression of nucleolin in chronic lymphocytic leukemia cells induces stabilization of bcl2 mRNA. Blood 109: 3069-3075.
25. Abdelmohsen K, Tominaga K, Lee EK, Srikantan S, Kang MJ, et al. (2011) Enhanced translation by Nucleolin via G-rich elements in coding and non-coding regions of target mRNAs. Nucleic Acids Res 39: 8513-8530.
26. Srivastava M, Pollard HB, (1999) Molecular dissection of nucleolin's role in growth and cell proliferation: new insights. FASEB J 13: 1911-1922.
27. Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, Morrison SJ, (2005) SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121: 1109-1121.
28. Juntilla MM, Patil VD, Calamito M, Joshi RP, Birnbaum MJ, et al. (2010) AKT1 and AKT2 maintain hematopoietic stem cell function by regulating reactive oxygen species. Blood 115: 4030-4038.
29. O'Connell RM, Chaudhuri AA, Rao DS, Gibson WS, Balazs AB, et al. (2010) MicroRNAs enriched in hematopoietic stem cells differentially regulate long-term hematopoietic output. Proc Natl Acad Sci U S A 107: 14235-14240.
30. Foudi A, Hochedlinger K, Van Buren D, Schindler JW, Jaenisch R, et al. (2009) Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat Biotechnol 27: 84-90.
31. Lu X, Yang X, Liu J, (2010) Differential control of ATGL-mediated lipid droplet degradation by CGI-58 and G0S2. Cell Cycle 9: 2719-2725.
32. Passegue E, Wagers AJ, Giuriato S, Anderson WC, Weissman IL, (2005) Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J Exp Med 202: 1599-1611.
33. Coller HA, Sang L, Roberts JM, (2006) A new description of cellular quiescence. PLoS Biol 4: e83.
34. Zhang J, Grindley JC, Yin T, Jayasinghe S, He XC, et al. (2006) PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 441: 518-522.
35. Cheng T, Rodrigues N, Shen H, Yang Y, Dombkowski D, et al. (2000) Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science 287: 1804-1808.
36. Hock H, Hamblen MJ, Rooke HM, Schindler JW, Saleque S, et al. (2004) Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells. Nature 431: 1002-1007.
37. Miyamoto K, Araki KY, Naka K, Arai F, Takubo K, et al. (2007) Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1: 101-112.
38. Yuan Y, Shen H, Franklin DS, Scadden DT, Cheng T, (2004) In vivo self-renewing divisions of haematopoietic stem cells are increased in the absence of the early G1-phase inhibitor, p18INK4C. Nat Cell Biol 6: 436-442.
39. Thorsteinsdottir U, Sauvageau G, Humphries RK, (1999) Enhanced in vivo regenerative potential of HOXB4-transduced hematopoietic stem cells with regulation of their pool size. Blood 94: 2605-2612.
40. Antonchuk J, Sauvageau G, Humphries RK, (2002) HOXB4-induced expansion of adult hematopoietic stem cells ex vivo. Cell 109: 39-45.
41. Kitareewan S, Blumen S, Sekula D, Bissonnette RP, Lamph WW, et al. (2008) G0S2 is an all-trans-retinoic acid target gene. Int J Oncol 33: 397-404.
42. Purton LE, Bernstein ID, Collins SJ, (2000) All-trans retinoic acid enhances the long-term repopulating activity of cultured hematopoietic stem cells. Blood 95: 470-477.
43. Wang Z, Li G, Tse W, Bunting KD, (2009) Conditional deletion of STAT5 in adult mouse hematopoietic stem cells causes loss of quiescence and permits efficient nonablative stem cell replacement. Blood 113: 4856-4865.
44. Kitsos CM, Sankar U, Illario M, Colomer-Font JM, Duncan AW, et al. (2005) Calmodulin-dependent protein kinase IV regulates hematopoietic stem cell maintenance. J Biol Chem 280: 33101-33108.
45. Derenzini M, Sirri V, Pession A, Trere D, Roussel P, et al. (1995) Quantitative changes of the two major AgNOR proteins, nucleolin and protein B23, related to stimulation of rDNA transcription. Exp Cell Res 219: 276-282.
46. Borer RA, Lehner CF, Eppenberger HM, Nigg EA, (1989) Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell 56: 379-390.
47. Ugrinova I, Monier K, Ivaldi C, Thiry M, Storck S, et al. (2007) Inactivation of nucleolin leads to nucleolar disruption, cell cycle arrest and defects in centrosome duplication. BMC Mol Biol 8: 66.
48. Grinstein E, Mahotka C, Borkhardt A, (2011) Rb and nucleolin antagonize in controlling human CD34 gene expression. Cell Signal 23: 1358-1365.
49. Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, et al. (2009) IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 458: 904-908.
50. Jerke U, Tkachuk S, Kiyan J, Stepanova V, Kusch A, et al. (2009) Stat1 nuclear translocation by nucleolin upon monocyte differentiation. PLoS One 4: e8302.
51. Bouvet P, Diaz JJ, Kindbeiter K, Madjar JJ, Amalric F, (1998) Nucleolin interacts with several ribosomal proteins through its RGG domain. J Biol Chem 273: 19025-19029.
52. Visalli G, Paiardini M, Chirico C, Cervasi B, Curro M, et al. (2010) Intracellular accumulation of cell cycle regulatory proteins and nucleolin re-localization are associated with pre-lethal ultrastructural lesions in circulating T lymphocytes: The HIV-induced cell cycle dysregulation revisited. Cell Cycle 9: 2130-2140.
53. Pear WS, Miller JP, Xu L, Pui JC, Soffer B, et al. (1998) Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 92: 3780-3792.