A complex interplay between PGC-1 co-activators and mTORC1 regulates hematopoietic recovery following 5-fluorouracil treatment

Stem Cell Research

Volumn 12, Issue 1, 2014, Pages 178-193

  Basu, Sunanda ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUOROURACIL; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; RAPAMYCIN;

ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; STEM CELL EXPANSION;

ELECTRON TRANSPORT CHAIN; ETC; HEMATOPOIETIC STEM AND PROGENITOR CELL; HEMATOPOIETIC STEM CELL; HSC; HSPC; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX1; MTORC1; N-ACETYL CYSTEINE; NAC; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA CO-ACTIVATOR-1Α; PGC-1 RELATED COACTIVATOR; PGC-1Α; PRC;

ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; CELL PROLIFERATION; FLUOROURACIL; HEMATOPOIETIC STEM CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MULTIPROTEIN COMPLEXES; REACTIVE OXYGEN SPECIES; SIROLIMUS; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS;

EID: 84887602935     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2013.10.006     Document Type: Article

References (49)

1. Andersson U., Scarpulla R.C. Pgc-1-related coactivator, a novel, serum-inducible coactivator of nuclear respiratory factor 1-dependent transcription in mammalian cells. Mol. Cell. Biol. 2001, 21:3738-3749.
2. Banki K., Hutter E., Gonchoroff N.J., Perl A. Elevation of mitochondrial transmembrane potential and reactive oxygen intermediate levels are early events and occur independently from activation of caspases in Fas signaling. J. Immunol. 1999, 162:1466-1479.
3. + cord blood cells to stromal cell-derived factor-1/CXCL12. Blood 2005, 106:485-493.
4. Basu S., Broxmeyer H.E., Hangoc G. Peroxisome proliferator-activated-gamma coactivator-1alpha-mediated mitochondrial biogenesis is important for hematopoietic recovery in response to stress. Stem Cells Dev. 2013, 22:1678-1692.
5. Brugarolas J., Lei K., Hurley R.L., et al. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 2004, 18:2893-2904.
6. Chance B., Thorell B. Localization and kinetics of reduced pyridine nucleotide in living cells by microfluorometry. J. Biol. Chem. 1959, 234:3044-3050.
7. Chen C., Liu Y., Liu R., et al. TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J. Exp. Med. 2008, 205:2397-2408.
8. Cicalese A., Bonizzi G., Pasi C.E., et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009, 138:1083-1095.
9. Cossarizza A., Salvioli S. Flow cytometric analysis of mitochondrial membrane potential using JC-1. Curr. Protoc. Cytom. 2001, 13:9.14.1-9.14.7.
10. Dennis P.B., Jaeschke A., Saitoh M., et al. Mammalian TOR: a homeostatic ATP sensor. Science 2001, 294:1102-1105.
11. Ellisen L.W., Ramsayer K.D., Johannessen C.M., et al. REDD1, a developmentally regulated transcriptional target of p63 and p53, links p63 to regulation of reactive oxygen species. Mol. Cell 2002, 10:995-1005.
12. Fingar D.C., Blenis J. Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 2004, 23:3151-3171.
13. Gan B., Hu J., Jiang S., et al. Lkb1 regulates quiescence and metabolic homeostasis of haematopoietic stem cells. Nature 2010, 468:701-704.
14. Greenberger J.S. Sensitivity of corticosteroid-dependent insulin-resistant lipogenesis in marrow preadipocytes of obese-diabetic (db/db) mice. Nature 1978, 275:752-754.
15. Gurumurthy S., Xie S.Z., Alagesan B., et al. The Lkb1 metabolic sensor maintains haematopoietic stem cell survival. Nature 2010, 468:659-663.
16. Habib S.L. Mechanism of activation of AMPK and upregulation of OGG1 by rapamycin in cancer cells. Oncotarget 2011, 2:958-959.
17. Hao W., Chang C.P., Tsao C.C., Xu J. Oligomycin-induced bioenergetic adaptation in cancer cells with heterogeneous bioenergetic organization. J. Biol. Chem. 2010, 285:12647-12654.
18. Hardie D.G., Carling D., Carlson M. The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell?. Annu. Rev. Biochem. 1998, 67:821-855.
19. Harrison D.E., Lerner C.P. Most primitive hematopoietic stem cells are stimulated to cycle rapidly after treatment with 5-fluorouracil. Blood 1991, 78:1237-1240.
20. Hay N., Sonenberg N. Upstream and downstream of mTOR. Genes Dev. 2004, 18:1926-1945.
21. Heissig B., Hattori K., Dias S., et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002, 109:625-637.
22. Hodgson G.S., Bradley T.R. Properties of haematopoietic stem cells surviving 5-fluorouracil treatment: evidence for a pre-CFU-S cell?. Nature 1979, 281:381-382.
23. Jansen R., Damia G., Usui N., et al. Effects of recombinant transforming growth factor-beta 1 on hematologic recovery after treatment of mice with 5-fluorouracil. J. Immunol. 1991, 147:3342-3347.
24. Kalaitzidis D., Neel B.G. Flow-cytometric phosphoprotein analysis reveals agonist and temporal differences in responses of murine hematopoietic stem/progenitor cells. PLoS One 2008, 3:e3776.
25. Kelly D.P., Scarpulla R.C. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 2004, 18:357-368.
26. Kopp H.G., Avecilla S.T., Hooper A.T., et al. Tie2 activation contributes to hemangiogenic regeneration after myelosuppression. Blood 2005, 106:505-513.
27. Laplante M., Sabatini D.M. mTOR signaling at a glance. J. Cell Sci. 2009, 122:3589-3594.
28. Larsson N.G., Wang J., Wilhelmsson H., et al. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 1998, 18:231-236.
29. Lee J.Y., Nakada D., Yilmaz O.H., et al. mTOR activation induces tumor suppressors that inhibit leukemogenesis and deplete hematopoietic stem cells after Pten deletion. Cell Stem Cell 2010, 7:593-605.
30. Lerner C., Harrison D.E. 5-Fluorouracil spares hemopoietic stem cells responsible for long-term repopulation. Exp. Hematol. 1990, 18:114-118.
31. Mortensen M., Soilleux E.J., Djordjevic G., et al. The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance. J. Exp. Med. 2011, 208:455-467.
32. Munday M.R. Regulation of mammalian acetyl-CoA carboxylase. Biochem. Soc. Trans. 2002, 30:1059-1064.
33. Nakada D., Saunders T.L., Morrison S.J. Lkb1 regulates cell cycle and energy metabolism in haematopoietic stem cells. Nature 2010, 468:653-658.
34. Pieri C., Recchioni R., Moroni F. Age-dependent modifications of mitochondrial trans-membrane potential and mass in rat splenic lymphocytes during proliferation. Mech. Ageing Dev. 1993, 70:201-212.
35. Puigserver P., Spiegelman B.M. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 2003, 24:78-90.
36. Randall T.D., Weissman I.L. Phenotypic and functional changes induced at the clonal level in hematopoietic stem cells after 5-fluorouracil treatment. Blood 1997, 89:3596-3606.
37. Reiling J.H., Hafen E. The hypoxia-induced paralogs Scylla and Charybdis inhibit growth by down-regulating S6K activity upstream of TSC in Drosophila. Genes Dev. 2004, 18:2879-2892.
38. Rich I.N. The effect of 5-fluorouracil on erythropoiesis. Blood 1991, 77:1164-1170.
39. Sato T., Laver J.H., Ogawa M. Reversible expression of CD34 by murine hematopoietic stem cells. Blood 1999, 94:2548-2554.
40. Scarpulla R.C. Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 2002, 286:81-89.
41. Scarpulla R.C. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol. Rev. 2008, 88:611-638.
42. Sengupta S., Peterson T.R., Sabatini D.M. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol. Cell 2010, 40:310-322.
43. Simsek T., Kocabas F., Zheng J., et al. The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 2010, 7:380-390.
44. Smiley S.T., Reers M., Mottola-Hartshorn C., et al. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:3671-3675.
45. Sofer A., Lei K., Johannessen C.M., Ellisen L.W. Regulation of mTOR and cell growth in response to energy stress by REDD1. Mol. Cell. Biol. 2005, 25:5834-5845.
46. Takubo K., Goda N., Yamada W., et al. Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 2010, 7:391-402.
47. Uldry M., Yang W., St-Pierre J., et al. Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab. 2006, 3:333-341.
48. Wilson A., Laurenti E., Oser G., et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008, 135:1118-1129.
49. Yilmaz O.H., Kiel M.J., Morrison S.J. SLAM family markers are conserved among hematopoietic stem cells from old and reconstituted mice and markedly increase their purity. Blood 2006, 107:924-930.