|
|
Mitochondrial control of hematopoietic stem cell balance and hematopoiesis |
Massimo Bonora1,2,Paolo Pinton1,Keisuke Ito2,*( ) |
1. Department of Morphology, Surgery, Experimental Medicine University of Ferrara, Section of Pathology Oncology, Experimental Biology Laboratory for Technologies of Advanced Therapies (LTTA), Ferrara, Italy 2. Ruth L. and David S. Gottesman Institute for Stem Cell and Regenerative Medicine Research, Departments of Cell Biology and Medicine, Albert Einstein Cancer Center and Einstein-Sinai Diabetes Research Center, Albert Einstein College of Medicine, Bronx, NY 10461, USA |
|
|
Abstract Hematopoietic stem cells (HSCs) are stem cells from mesodermal derivation that reside in bone marrow and provide blood cells for the whole life of an adult individual, through a process called hematopoiesis. The long lasting support of HSCs for hematopoiesis is permitted by the fine regulation of quiescence and division output. Exit from the quiescent state is to produce a committed and/or stem daughter cells, in an event defined asymmetric or symmetric division. A deregulation in the proportion between asymmetric and symmetric divisions is critical in the appearance of hematological disorders ranging from bone marrow failure to hematological malignancies. Over the past years, several studies have indicated how the metabolism of HSCs is determinant in the regulation of HSC quiescence and commitment process. A metabolism shifted to the glycolytic pathway promotes HSCs quiescence and sustainment of hematopoiesis. Boosting mitochondrial respiration promotes the stem cell commitment followed by stem pool exhaustion, and minimal mitochondrial activity is required to maintain the HSCs quiescence. In the present review are discussed the most recent advances in comprehension of the roles of mitochondria in the hematopoiesis and in the division balance.
|
Keywords
mitochondria
division balance
hypoxia inducible factor 1 alpha (Hif-1α)
metabolism
hematopoiesis
hematopoietic stem cells
|
Corresponding Author(s):
Keisuke Ito
|
Issue Date: 06 May 2015
|
|
1 |
Arruda A P, Pers B M, Parlakgül G, Güney E, Inouye K, Hotamisligil G S (2014). Chronic enrichment of hepatic endoplasmic reticulum-mitochondria contact leads to mitochondrial dysfunction in obesity. Nat Med, 20(12): 1427–1435
https://doi.org/10.1038/nm.3735
pmid: 25419710
|
2 |
Beckmann J, Scheitza S, Wernet P, Fischer J C, Giebel B (2007). Asymmetric cell division within the human hematopoietic stem and progenitor cell compartment: identification of asymmetrically segregating proteins. Blood, 109(12): 5494–5501
https://doi.org/10.1182/blood-2006-11-055921
pmid: 17332245
|
3 |
Bononi A, Bonora M, Marchi S, Missiroli S, Poletti F, Giorgi C, Pandolfi P P, Pinton P (2013). Identification of PTEN at the ER and MAMs and its regulation of Ca(2+) signaling and apoptosis in a protein phosphatase-dependent manner. Cell Death Differ, 20(12): 1631–1643
https://doi.org/10.1038/cdd.2013.77
pmid: 23811847
|
4 |
Bononi A, Missiroli S, Poletti F, Suski J M, Agnoletto C, Bonora M, De Marchi E, Giorgi C, Marchi S, Patergnani S, Rimessi A, Wieckowski M R, Pinton P (2012). Mitochondria-associated membranes (MAMs) as hotspot Ca(2+) signaling units. Adv Exp Med Biol, 740: 411–437
https://doi.org/10.1007/978-94-007-2888-2_17
pmid: 22453952
|
5 |
Bonora M, De Marchi E, Patergnani S, Suski J M, Celsi F, Bononi A, Giorgi C, Marchi S, Rimessi A, Duszyński J, Pozzan T, Wieckowski M R, Pinton P (2014). Tumor necrosis factor-α impairs oligodendroglial differentiation through a mitochondria-dependent process. Cell Death Differ, 21(8): 1198–1208
https://doi.org/10.1038/cdd.2014.35
pmid: 24658399
|
6 |
Bonora M, Patergnani S, Rimessi A, De Marchi E, Suski J M, Bononi A, Giorgi C, Marchi S, Missiroli S, Poletti F, Wieckowski M R, Pinton P (2012). ATP synthesis and storage. Purinergic Signal, 8(3): 343–357
https://doi.org/10.1007/s11302-012-9305-8
pmid: 22528680
|
7 |
Bonora M, Pinton P (2014). The mitochondrial permeability transition pore and cancer: molecular mechanisms involved in cell death. Front Oncol, 4: 302
https://doi.org/10.3389/fonc.2014.00302
pmid: 25478322
|
8 |
Carracedo A, Cantley L C, Pandolfi P P (2013). Cancer metabolism: fatty acid oxidation in the limelight. Nat Rev Cancer, 13(4): 227–232
https://doi.org/10.1038/nrc3483
pmid: 23446547
|
9 |
Chen C, Liu Y, Liu R, Ikenoue T, Guan K L, Liu Y, Zheng P (2008). TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J Exp Med, 205(10): 2397–2408
https://doi.org/10.1084/jem.20081297
pmid: 18809716
|
10 |
Dalton C M, Carroll J (2013). Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte. J Cell Sci, 126(Pt 13): 2955–2964
https://doi.org/10.1242/jcs.128744
pmid: 23659999
|
11 |
Galluzzi L, Pietrocola F, Levine B, Kroemer G (2014). Metabolic control of autophagy. Cell, 159(6): 1263–1276
https://doi.org/10.1016/j.cell.2014.11.006
pmid: 25480292
|
12 |
Gan B, Hu J, Jiang S, Liu Y, Sahin E, Zhuang L, Fletcher-Sananikone E, Colla S, Wang Y A, Chin L, Depinho R A (2010). Lkb1 regulates quiescence and metabolic homeostasis of haematopoietic stem cells. Nature, 468(7324): 701–704
https://doi.org/10.1038/nature09595
pmid: 21124456
|
13 |
Giebel B, Zhang T, Beckmann J, Spanholtz J, Wernet P, Ho A D, Punzel M (2006). Primitive human hematopoietic cells give rise to differentially specified daughter cells upon their initial cell division. Blood, 107(5): 2146–2152
https://doi.org/10.1182/blood-2005-08-3139
pmid: 16249381
|
14 |
Giorgi C, Bonora M, Missiroli S, Poletti F, Ramirez F G, Morciano G, Morganti C, Pandolfi P P, Mammano F, Pinton P (2014). Intravital imaging reveals p53-dependent cancer cell death induced by phototherapy via calcium signaling. Oncotarget, 6(3): 1435–1445
|
15 |
Giorgi C, Bonora M, Sorrentino G, Missiroli S, Poletti F, Suski J M, Ramirez G, Rizzuto R, Di Virgilio F, Zito E, Pandolfi P P, Wieckowski M R, Mammano F, Del Sal G, Pinton P (2015). p53 at the endoplasmic reticulum regulates apoptosis in a Ca2+-dependent manner. Proc Natl Acad Sci, 112(6): 1779–1784
|
16 |
Green D R, Galluzzi L, Kroemer G (2014). Cell biology. Metabolic control of cell death. Science, 345(6203): 1250256
https://doi.org/10.1126/science.1250256
pmid: 25237106
|
17 |
Gurumurthy S, Xie S Z, Alagesan B, Kim J, Yusuf R Z, Saez B, Tzatsos A, Ozsolak F, Milos P, Ferrari F, Park P J, Shirihai O S, Scadden D T, Bardeesy N (2010). The Lkb1 metabolic sensor maintains haematopoietic stem cell survival. Nature, 468(7324): 659–663
https://doi.org/10.1038/nature09572
pmid: 21124451
|
18 |
Higuchi R, Vevea J D, Swayne T C, Chojnowski R, Hill V, Boldogh I R, Pon L A (2013). Actin dynamics affect mitochondrial quality control and aging in budding yeast. Curr Biol, 23(23): 2417–2422
https://doi.org/10.1016/j.cub.2013.10.022
pmid: 24268413
|
19 |
Inoue S, Noda S, Kashima K, Nakada K, Hayashi J, Miyoshi H (2010). Mitochondrial respiration defects modulate differentiation but not proliferation of hematopoietic stem and progenitor cells. FEBS Lett, 584(15): 3402–3409
https://doi.org/10.1016/j.febslet.2010.06.036
pmid: 20600007
|
20 |
Ito K, Bernardi R, Morotti A, Matsuoka S, Saglio G, Ikeda Y, Rosenblatt J, Avigan D E, Teruya-Feldstein J, Pandolfi P P (2008). PML targeting eradicates quiescent leukaemia-initiating cells. Nature, 453(7198): 1072–1078
https://doi.org/10.1038/nature07016
pmid: 18469801
|
21 |
Ito K, Carracedo A, Weiss D, Arai F, Ala U, Avigan D E, Schafer Z T, Evans R M, Suda T, Lee C H, Pandolfi P P (2012). A PML–PPAR-δ pathway for fatty acid oxidation regulates hematopoietic stem cell maintenance. Nat Med, 18(9): 1350–1358
https://doi.org/10.1038/nm.2882
pmid: 22902876
|
22 |
Ito K, Suda T (2014). Metabolic requirements for the maintenance of self-renewing stem cells. Nat Rev Mol Cell Biol, 15(4): 243–256
https://doi.org/10.1038/nrm3772
pmid: 24651542
|
23 |
Kunisaki Y, Bruns I, Scheiermann C, Ahmed J, Pinho S, Zhang D, Mizoguchi T, Wei Q, Lucas D, Ito K, Mar J C, Bergman A, Frenette P S (2013). Arteriolar niches maintain haematopoietic stem cell quiescence. Nature, 502(7473): 637–643
https://doi.org/10.1038/nature12612
pmid: 24107994
|
24 |
Leary A G, Strauss L C, Civin C I, Ogawa M (1985). Disparate differentiation in hemopoietic colonies derived from human paired progenitors. Blood, 66(2): 327–332
pmid: 4016276
|
25 |
Liu F, Lee J Y, Wei H, Tanabe O, Engel J D, Morrison S J, Guan J L (2010). FIP200 is required for the cell-autonomous maintenance of fetal hematopoietic stem cells. Blood, 116(23): 4806–4814
https://doi.org/10.1182/blood-2010-06-288589
pmid: 20716775
|
26 |
Mantel C, Messina-Graham S, Broxmeyer H E (2010). Upregulation of nascent mitochondrial biogenesis in mouse hematopoietic stem cells parallels upregulation of CD34 and loss of pluripotency: a potential strategy for reducing oxidative risk in stem cells. Cell Cycle, 9(10): 2008–2017
https://doi.org/10.4161/cc.9.10.11733
pmid: 20495374
|
27 |
Marchi S, Patergnani S, Pinton P (2014). The endoplasmic reticulum-mitochondria connection: one touch, multiple functions. Biochim Biophys Acta, 1837(4): 461–469
https://doi.org/10.1016/j.bbabio.2013.10.015
pmid: 24211533
|
28 |
McKenzie J L, Takenaka K, Gan O I, Doedens M, Dick J E (2007). Low rhodamine 123 retention identifies long-term human hematopoietic stem cells within the Lin-CD34+CD38- population. Blood, 109(2): 543–545
https://doi.org/10.1182/blood-2006-06-030270
pmid: 16990597
|
29 |
Mendelson A, Frenette P S (2014). Hematopoietic stem cell niche maintenance during homeostasis and regeneration. Nat Med, 20(8): 833–846
https://doi.org/10.1038/nm.3647
pmid: 25100529
|
30 |
Morrison S J, Kimble J (2006). Asymmetric and symmetric stem-cell divisions in development and cancer. Nature, 441(7097): 1068–1074
https://doi.org/10.1038/nature04956
pmid: 16810241
|
31 |
Mortensen M, Ferguson D J, Edelmann M, Kessler B, Morten K J, Komatsu M, Simon A K (2010). Loss of autophagy in erythroid cells leads to defective removal of mitochondria and severe anemia in vivo. Proc Natl Acad Sci USA, 107(2): 832–837
https://doi.org/10.1073/pnas.0913170107
pmid: 20080761
|
32 |
Nakada D, Saunders T L, Morrison S J (2010). Lkb1 regulates cell cycle and energy metabolism in haematopoietic stem cells. Nature, 468(7324): 653–658
https://doi.org/10.1038/nature09571
pmid: 21124450
|
33 |
Pagliarini D J, Wiley S E, Kimple M E, Dixon J R, Kelly P, Worby C A, Casey P J, Dixon J E (2005). Involvement of a mitochondrial phosphatase in the regulation of ATP production and insulin secretion in pancreatic beta cells. Mol Cell, 19(2): 197–207
https://doi.org/10.1016/j.molcel.2005.06.008
pmid: 16039589
|
34 |
Patergnani S, Pinton P (2015). Mitophagy and mitochondrial balance. Methods Mol Biol, 1241: 181–194
https://doi.org/10.1007/978-1-4939-1875-1_15
pmid: 25308497
|
35 |
Piccoli C, Ria R, Scrima R, Cela O, D’Aprile A, Boffoli D, Falzetti F, Tabilio A, Capitanio N (2005). Characterization of mitochondrial and extra-mitochondrial oxygen consuming reactions in human hematopoietic stem cells. Novel evidence of the occurrence of NAD(P)H oxidase activity. J Biol Chem, 280(28): 26467–26476
https://doi.org/10.1074/jbc.M500047200
pmid: 15883163
|
36 |
Ploemacher R E, Brons N H (1988a). In vivo proliferative and differential properties of murine bone marrow cells separated on the basis of rhodamine-123 retention. Exp Hematol, 16(11): 903–907
pmid: 3181339
|
37 |
Ploemacher R E, Brons N H (1988b). Isolation of hemopoietic stem cell subsets from murine bone marrow: II. Evidence for an early precursor of day-12 CFU-S and cells associated with radioprotective ability. Exp Hematol, 16(1): 27–32
pmid: 2891557
|
38 |
Prowse A B, Chong F, Elliott D A, Elefanty A G, Stanley E G, Gray P P, Munro T P, Osborne G W (2012). Analysis of mitochondrial function and localisation during human embryonic stem cell differentiation in vitro. PLoS ONE, 7(12): e52214
https://doi.org/10.1371/journal.pone.0052214
pmid: 23284940
|
39 |
Rehman J (2010). Empowering self-renewal and differentiation: the role of mitochondria in stem cells. J Mol Med (Berl), 88(10): 981–986
https://doi.org/10.1007/s00109-010-0678-2
pmid: 20809088
|
40 |
Rimessi A, Bonora M, Marchi S, Patergnani S, Marobbio C M, Lasorsa F M, Pinton P (2013). Perturbed mitochondrial Ca2+ signals as causes or consequences of mitophagy induction. Autophagy, 9(11): 1677–1686
https://doi.org/10.4161/auto.24795
pmid: 24121707
|
41 |
Romero-Moya D, Bueno C, Montes R, Navarro-Montero O, Iborra F J, López L C, Martin M, Menendez P (2013). Cord blood-derived CD34+ hematopoietic cells with low mitochondrial mass are enriched in hematopoietic repopulating stem cell function. Haematologica, 98(7): 1022–1029
https://doi.org/10.3324/haematol.2012.079244
pmid: 23349299
|
42 |
Schroeder T (2007). Asymmetric cell division in normal and malignant hematopoietic precursor cells. Cell Stem Cell, 1(5): 479–481
https://doi.org/10.1016/j.stem.2007.10.016
pmid: 18938740
|
43 |
Simsek T, Kocabas F, Zheng J, Deberardinis R J, Mahmoud A I, Olson E N, Schneider J W, Zhang C C, Sadek H A (2010). The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell, 7(3): 380–390
https://doi.org/10.1016/j.stem.2010.07.011
pmid: 20804973
|
44 |
Spencer J A, Ferraro F, Roussakis E, Klein A, Wu J, Runnels J M, Zaher W, Mortensen L J, Alt C, Turcotte R, Yusuf R, C?té D, Vinogradov S A, Scadden D T, Lin C P (2014). Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature, 508(7495): 269–273
https://doi.org/10.1038/nature13034
pmid: 24590072
|
45 |
Staiber W (2007). Asymmetric distribution of mitochondria and of spindle microtubules in opposite directions in differential mitosis of germ line cells in Acricotopus. Cell Tissue Res, 329(1): 197–203
https://doi.org/10.1007/s00441-007-0400-z
pmid: 17372767
|
46 |
Suda T, Suda J, Ogawa M (1984). Disparate differentiation in mouse hemopoietic colonies derived from paired progenitors. Proc Natl Acad Sci USA, 81(8): 2520–2524 (Research Support, U.S. Gov’t, Non-P.H.S. Research Support, U.S. Gov’t, P.H.S.)
https://doi.org/10.1073/pnas.81.8.2520
pmid: 6585813
|
47 |
Takahashi S, Tanaka T, Sakai J (2007). New therapeutic target for metabolic syndrome: PPARdelta. Endocr J, 54(3): 347–357
https://doi.org/10.1507/endocrj.KR-99
pmid: 17409576
|
48 |
Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, Shima H, Johnson R S, Hirao A, Suematsu M, Suda T (2010). Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell, 7(3): 391–402
https://doi.org/10.1016/j.stem.2010.06.020
pmid: 20804974
|
49 |
Takubo K, Nagamatsu G, Kobayashi C I, Nakamura-Ishizu A, Kobayashi H, Ikeda E, Goda N, Rahimi Y, Johnson R S, Soga T, Hirao A, Suematsu M, Suda T (2013). Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell, 12(1): 49–61
https://doi.org/10.1016/j.stem.2012.10.011
pmid: 23290136
|
50 |
Ting S B, Deneault E, Hope K, Cellot S, Chagraoui J, Mayotte N, Dorn J F, Laverdure J P, Harvey M, Hawkins E D, Russell S M, Maddox P S, Iscove N N, Sauvageau G (2012). Asymmetric segregation and self-renewal of hematopoietic stem and progenitor cells with endocytic Ap2a2. Blood, 119(11): 2510–2522
https://doi.org/10.1182/blood-2011-11-393272
pmid: 22174158
|
51 |
Vance J E (2014). MAM (mitochondria-associated membranes) in mammalian cells: lipids and beyond. Biochim Biophys Acta, 1841(4): 595–609
https://doi.org/10.1016/j.bbalip.2013.11.014
pmid: 24316057
|
52 |
Vega-Naredo I, Loureiro R, Mesquita K A, Barbosa I A, Tavares L C, Branco A F, Erickson J R, Holy J, Perkins E L, Carvalho R A, Oliveira P J (2014). Mitochondrial metabolism directs stemness and differentiation in P19 embryonal carcinoma stem cells. Cell Death Differ, 21(10): 1560–1574
https://doi.org/10.1038/cdd.2014.66
pmid: 24832466
|
53 |
Wallace D C, Chalkia D (2013). Mitochondrial DNA genetics and the heteroplasmy conundrum in evolution and disease. Cold Spring Harb Perspect Biol, 5(11): a021220
https://doi.org/10.1101/cshperspect.a021220
pmid: 24186072
|
54 |
Wanet A, Remacle N, Najar M, Sokal E, Arnould T, Najimi M, Renard P (2014). Mitochondrial remodeling in hepatic differentiation and dedifferentiation. Int J Biochem Cell Biol, 54: 174–185
https://doi.org/10.1016/j.biocel.2014.07.015
pmid: 25084555
|
55 |
Wang Y H, Israelsen W J, Lee D, Yu V W, Jeanson N T, Clish C B, Cantley L C, Vander Heiden M G, Scadden D T (2014). Cell-state-specific metabolic dependency in hematopoiesis and leukemogenesis. Cell, 158(6): 1309–1323
https://doi.org/10.1016/j.cell.2014.07.048
pmid: 25215489
|
56 |
Weissman I L, Anderson D J, Gage F (2001). Stem and progenitor cells: origins, phenotypes, lineage commitments, and transdifferentiations. Annu Rev Cell Dev Biol, 17(1): 387–403
https://doi.org/10.1146/annurev.cellbio.17.1.387
pmid: 11687494
|
57 |
Wu M, Kwon H Y, Rattis F, Blum J, Zhao C, Ashkenazi R, Jackson T L, Gaiano N, Oliver T, Reya T (2007). Imaging hematopoietic precursor division in real time. Cell Stem Cell, 1(5): 541–554
https://doi.org/10.1016/j.stem.2007.08.009
pmid: 18345353
|
58 |
Yu W M, Liu X, Shen J, Jovanovic O, Pohl E E, Gerson S L, Finkel T, Broxmeyer H E, Qu C K (2013). Metabolic regulation by the mitochondrial phosphatase PTPMT1 is required for hematopoietic stem cell differentiation. Cell Stem Cell, 12(1): 62–74
https://doi.org/10.1016/j.stem.2012.11.022
pmid: 23290137
|
59 |
Zhang H, Gao P, Fukuda R, Kumar G, Krishnamachary B, Zeller K I, Dang C V, Semenza G L (2007). HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell, 11(5): 407–420
https://doi.org/10.1016/j.ccr.2007.04.001
pmid: 17482131
|
60 |
Zhang Y, Marsboom G, Toth P T, Rehman J (2013). Mitochondrial respiration regulates adipogenic differentiation of human mesenchymal stem cells. PLoS ONE, 8(10): e77077
https://doi.org/10.1371/journal.pone.0077077
pmid: 24204740
|
61 |
Zimdahl B, Ito T, Blevins A, Bajaj J, Konuma T, Weeks J, Koechlein C S, Kwon H Y, Arami O, Rizzieri D, Broome H E, Chuah C, Oehler V G, Sasik R, Hardiman G, Reya T (2014). Lis1 regulates asymmetric division in hematopoietic stem cells and in leukemia. Nat Genet, 46(3): 245–252
https://doi.org/10.1038/ng.2889
pmid: 24487275
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|