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Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front. Biol.    2015, Vol. 10 Issue (2) : 117-124    https://doi.org/10.1007/s11515-015-1356-0
REVIEW
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
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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
 Cite this article:   
Massimo Bonora,Paolo Pinton,Keisuke Ito. Mitochondrial control of hematopoietic stem cell balance and hematopoiesis[J]. Front. Biol., 2015, 10(2): 117-124.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-015-1356-0
https://academic.hep.com.cn/fib/EN/Y2015/V10/I2/117
Fig.1  Simplified interpretation of hematopoiesis and metabolic features in HSC and differentiating cells. Mitochondria are displayed as intracellular brown objects. Levels of different metabolic parameters are displayed by colorized cartoons. Mitochondrial membrane potential (MMP), based on reports about Rhodamine123 measurements.
Fig.2  Schematic representation of mitochondria activity and the consequent cellular respiration on cellular state of a long-term hematopoietic stem cell.
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
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