Tif1γ regulates the TGF-β1 receptor and promotes physiological aging of hematopoietic stem cells

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

Volumn 111, Issue 29, 2014, Pages 10592-10597

  Quéré, Ronan ^a,b   Saint Paul, Laetitia ^a,b   Carmignac, Virginie ^b   Martin, Romain Z ^a,b   Chret́ien, Marie Lorraine ^a,b,c   Largeot, Anne ^a,b   Hammann, Arlette ^b   Pais De Barros, Jean Paul ^b   Bastie, Jean Noël ^a,b,c   Delva, Laurent ^a,b  

^a Institut Médical de Génétique et d Immunologie   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c DIJON UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION INTERMEDIARY FACTOR 1GAMMA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1 RECEPTOR; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BONE MARROW CELL; CELL AGING; CONTROLLED STUDY; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; MOUSE; NONHUMAN; PREMATURE AGING; PRIORITY JOURNAL; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TELOMERE SHORTENING; TRANSCRIPTION REGULATION;

AGING; ANIMALS; ANTIGENS, CD; CELL AGING; CELL SEPARATION; GENE EXPRESSION REGULATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; MICE; MYELOID CELLS; PHENOTYPE; POLYUBIQUITIN; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA1; UBIQUITINATION;

EID: 84904642596     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1405546111     Document Type: Article

References (45)

1. Venturini L, et al. (1999) TIF1gamma, a novel member of the transcriptional intermediary factor 1 family. Oncogene 18(5):1209-1217. (Pubitemid 29085994)
2. Yan KP, et al. (2004) Molecular cloning, genomic structure, and expression analysis of the mouse transcriptional intermediary factor 1 gamma gene. Gene 334:3-13. (Pubitemid 38902710)
3. Kusy S, et al. (2011) Adult hematopoiesis is regulated by TIF1γ, a repressor of TAL1 and PU.1 transcriptional activity. Cell Stem Cell 8(4):412-425.
4. He W, et al. (2006) Hematopoiesis controlled by distinct TIF1gamma and Smad4 branches of the TGFbeta pathway. Cell 125(5):929-941. (Pubitemid 43795187)
5. Ransom DG, et al. (2004) The zebrafish moonshine gene encodes transcriptional intermediary factor 1gamma, an essential regulator of hematopoiesis. PLoS Biol 2(8):E237.
6. Aucagne R, et al. (2011) Transcription intermediary factor 1γ is a tumor suppressor in mouse and human chronic myelomonocytic leukemia. J Clin Invest 121(6):2361-2370.
7. Bai X, et al. (2013) TiF1-gamma plays an essential role in murine hematopoiesis and regulates transcriptional elongation of erythroid genes. Dev Biol 373(2):422-430.
8. Henry CJ, Marusyk A, DeGregori J (2011) Aging-associated changes in hematopoiesis and leukemogenesis: what' s the connection? (Translated from eng). Aging (Albany, NY Online) 3(6):643-656.
9. de Haan G, Van Zant G (1999) Dynamic changes in mouse hematopoietic stem cell numbers during aging. Blood 93(10):3294-3301.
10. Rossi DJ, et al. (2005) Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci USA 102(26):9194-9199. (Pubitemid 40923540)
11. Sudo K, Ema H, Morita Y, Nakauchi H (2000) Age-associated characteristics of murine hematopoietic stem cells. J Exp Med 192(9):1273-1280.
12. Geiger H, de Haan G, Florian MC (2013) The ageing haematopoietic stem cell compartment. Nat Rev Immunol 13(5):376-389.
13. Benz C, et al. (2012) Hematopoietic stem cell subtypes expand differentially during development and display distinct lymphopoietic programs. Cell Stem Cell 10(3):273-283.
14. Dykstra B, et al. (2007) Long-term propagation of distinct hematopoietic differentiation programs in vivo. Cell Stem Cell 1(2):218-229. (Pubitemid 47215588)
15. Xi Q, et al. (2011) A poised chromatin platform for TGF-β access to master regulators. Cell 147(7):1511-1524.
16. Dupont S, et al. (2009) FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell 136(1):123-135.
17. Dupont S, et al. (2005) Germ-layer specification and control of cell growth by Ectodermin, a Smad4 ubiquitin ligase. Cell 121(1):87-99.
18. Morsut L, et al. (2010) Negative control of Smad activity by ectodermin/Tif1gamma patterns the mammalian embryo. Development 137(15):2571-2578.
19. Yamazaki S, et al. (2009) TGF-beta as a candidate bone marrow niche signal to induce hematopoietic stem cell hibernation. Blood 113(6):1250-1256.
20. Fortunel N, et al. (2000) Release from quiescence of primitive human hematopoietic stem/progenitor cells by blocking their cell-surface TGF-beta type II receptor in a short-term in vitro assay. Stem Cells 18(2):102-111. (Pubitemid 30176804)
21. Yamazaki S, et al. (2006) Cytokine signals modulated via lipid rafts mimic niche signals and induce hibernation in hematopoietic stem cells. EMBO J 25(15):3515-3523. (Pubitemid 44264862)
22. Challen GA, Boles NC, Chambers SM, Goodell MA (2010) Distinct hematopoietic stem cell subtypes are differentially regulated by TGF-beta1. Cell Stem Cell 6(3):265-278.
23. Rossi DJ, et al. (2007) Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 447(7145):725-729. (Pubitemid 46889729)
24. Nijnik A, et al. (2007) DNA repair is limiting for haematopoietic stem cells during ageing. Nature 447(7145):686-690. (Pubitemid 46889732)
25. Morrison SJ, Wandycz AM, Akashi K, Globerson A, Weissman IL (1996) The aging of hematopoietic stem cells. Nat Med 2(9):1011-1016. (Pubitemid 26306840)
26. Pang WW, et al. (2011) Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age. Proc Natl Acad Sci USA 108(50):20012-20017.
27. Blasco MA (2007) Telomere length, stem cells and aging. Nat Chem Biol 3(10):640-649. (Pubitemid 47417712)
28. Ding H, et al. (2004) Regulation of murine telomere length by Rtel: an essential gene encoding a helicase-like protein. Cell 117(7):873-886. (Pubitemid 38798854)
29. Köhler A, et al. (2009) Altered cellular dynamics and endosteal location of aged early hematopoietic progenitor cells revealed by time-lapse intravital imaging in long bones. Blood 114(2):290-298.
30. Ramos CA, et al. (2006) Evidence for diversity in transcriptional profiles of single hematopoietic stem cells. PLoS Genet 2(9):e159.
31. Blank U, Karlsson G, Karlsson S (2008) Signaling pathways governing stem-cell fate. Blood 111(2):492-503.
32. Yamazaki S, et al. (2011) Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 147(5):1146-1158.
33. Beerman I, et al. (2010) Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proc Natl Acad Sci USA 107(12):5465-5470.
34. Cho RH, Sieburg HB, Muller-Sieburg CE (2008) A new mechanism for the aging of hematopoietic stem cells: aging changes the clonal composition of the stem cell compartment but not individual stem cells. Blood 111(12):5553-5561.
35. Fortunel N, et al. (1998) High proliferative potential-quiescent cells: a working model to study primitive quiescent hematopoietic cells. J Cell Sci 111(Pt 13):1867-1875. (Pubitemid 28370531)
36. Jacobsen SE, et al. (1991) Transforming growth factor-beta trans-modulates the expression of colony stimulating factor receptors on murine hematopoietic progenitor cell lines. Blood 77(8):1706-1716.
37. Lee YJ, et al. (1997) TGF-beta suppresses IFN-gamma induction of class II MHC gene expression by inhibiting class II transactivator messenger RNA expression. J Immunol 158(5):2065-2075.
38. Nandan D, Reiner NE (1997) TGF-beta attenuates the class II transactivator and reveals an accessory pathway of IFN-gamma action. J Immunol 158(3):1095-1101. (Pubitemid 127469929)
39. Gekas C, Graf T (2013) CD41 expression marks myeloid-biased adult hematopoietic stem cells and increases with age. Blood 121(22):4463-4472.
40. Stirewalt DL, et al. (2009) Decreased IRF8 expression found in aging hematopoietic progenitor/stem cells. Leukemia 23(2):391-393.
41. Wang H, et al. (2008) IRF8 regulates B-cell lineage specification, commitment, and differentiation. Blood 112(10):4028-4038.
42. Blank U, Karlsson S (2011) The role of Smad signaling in hematopoiesis and translational hematology. Leukemia 25(9):1379-1388.
43. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL (2003) Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 5(5):410-421. (Pubitemid 36592263)
44. Kavsak P, et al. (2000) Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol Cell 6(6):1365-1375. (Pubitemid 32045929)
45. Kulkarni A, Oza J, Yao M, et al. Tripartite Motif-containing 33 (TRIM33) protein functions in the poly(ADP-ribose) polymerase (PARP)-dependent DNA damage response through interaction with Amplified in Liver Cancer 1 (ALC1) protein. J Biol Chem. 2013;288(45):32357-32369.