Significance: Heme oxygenase-1 (HO-1) converts heme to biliverdin, carbon monoxide, and ferrous ions, but its cellular functions are far beyond heme metabolism. HO-1 via heme removal and degradation products acts as a cytoprotective, anti-inflammatory, immunomodulatory, and proangiogenic protein, regulating also a cell cycle. Additionally, HO-1 can translocate to nucleus and regulate transcription factors, so it can also act independently of enzymatic function. Recent Advances: Recently, a body of evidence has emerged indicating a role for HO-1 in postnatal differentiation of stem and progenitor cells. Maturation of satellite cells, skeletal myoblasts, adipocytes, and osteoclasts is inhibited by HO-1, whereas neurogenic differentiation and formation of cardiomyocytes perhaps can be enhanced. Moreover, HO-1 influences a lineage commitment in pluripotent stem cells and maturation of hematopoietic cells. It may play a role in development of osteoblasts, but descriptions of its exact effects are inconsistent. Critical Issues: In this review we discuss a role of HO-1 in cell differentiation, and possible HO-1-dependent signal transduction pathways. Among the potential mediators, we focused on microRNA (miRNA). These small, noncoding RNAs are critical for cell differentiation. Recently we have found that HO-1 not only influences expression of specific miRNAs but also regulates miRNA processing enzymes. Future Directions: It seems that interplay between HO-1 and miRNAs may be important in regulating fates of stem and progenitor cells and needs further intensive studies. Antioxid. Redox Signal. 20, 1827–1850.
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References
1.
AbdallahBM and KassemM.New factors controlling the balance between osteoblastogenesis and adipogenesis. Bone, 50: 540–545, 2012.
2.
AbrahamNG. Molecular regulation—biological role of heme in hematopoiesis. Blood Rev, 5: 19–28, 1991.
3.
AfonyushkinT, OskolkovaOV, PhilippovaM, ResinkTJ, ErneP, BinderBR, and BochkovVN. Oxidized phospholipids regulate expression of ATF4 and VEGF in endothelial cells via NRF2-dependent mechanism: novel point of convergence between electrophilic and unfolded protein stress pathways. Arterioscler Thromb Vasc Biol, 30: 1007–1013, 2010.
4.
AguiariP, LeoS, ZavanB, VindigniV, RimessiA, BianchiK, FranzinC, CortivoR, RossatoM, VettorR, AbatangeloG, PozzanT, PintonP, and RizzutoR. High glucose induces adipogenic differentiation of muscle-derived stem cells. Proc Natl Acad Sci U S A, 105: 1226–1231, 2008.
5.
AkimotoT, UshidaT, MiyakiS, AkaogiH, TsuchiyaK, YanZ, WilliamsRS, and TateishiT. Mechanical stretch inhibits myoblast-to-adipocyte differentiation through Wnt signaling. Biochem Biophys Res Commun, 329: 381–385, 2005.
6.
AlmeidaM. Unraveling the role of FoxOs in bone—insights from mouse models. Bone, 49: 319–327, 2011.
7.
AlvesLR, CostaES, SorgineMH, Nascimento-SilvaMC, TeodosioC, BarcenaP, Castro-Faria-NetoHC, BozzaPT, OrfaoA, OliveiraPL, and Maya-MonteiroCM. Heme-oxygenases during erythropoiesis in K562 and human bone marrow cells. PLoS One, 6: e21358, 2011.
8.
AmbrosV and ChenX. The regulation of genes and genomes by small RNAs. Development, 134: 1635–1641, 2007.
AsaharaT, KawamotoA, and MasudaH. Concise review: circulating endothelial progenitor cells for vascular medicine. Stem Cells, 29: 1650–1655, 2011.
11.
AsakuraA, KomakiM, and RudnickiM. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation, 68: 245–253, 2001.
12.
AzizA, SebastianS, and DilworthFJ. The origin and fate of muscle satellite cells. Stem Cell Rev, 8: 609–622, 2012.
13.
BarbagalloI, TibulloD, Di RosaM, GiallongoC, PalumboGA, RacitiG, CampisiA, VanellaA, GreenCJ, and MotterliniR. A cytoprotective role for the heme oxygenase-1/CO pathway during neural differentiation of human mesenchymal stem cells. J Neurosci Res, 86: 1927–1935, 2008.
14.
BarbagalloI, VanellaA, PetersonSJ, KimDH, TibulloD, GiallongoC, VanellaL, ParrinelloN, PalumboGA, RaimondoFD, AbrahamNG, and AsprinioD. Overexpression of heme oxygenase-1 increases human osteoblast stem cell differentiation. J Bone Miner Metab, 28: 276–288, 2009.
15.
BarreraLN, RushworthSA, BowlesKM, and MacEwanDJ. Bortezomib induces heme oxygenase-1 expression in multiple myeloma. Cell Cycle, 11: 2248–2252, 2012.
16.
BaruscottiI, BarchiesiF, JacksonEK, ImthurnB, StillerR, KimJH, SchaufelbergerS, RosselliM, HughesCC, and DubeyRK. Estradiol stimulates capillary formation by human endothelial progenitor cells: role of estrogen receptor-{alpha}/{beta}, heme oxygenase 1, and tyrosine kinase. Hypertension, 56: 397–404, 2010.
17.
BeckmanJD, ChenC, NguyenJ, ThayanithyV, SubramanianS, SteerCJ, and VercellottiGM. Regulation of heme oxygenase-1 protein expression by miR-377 in combination with miR-217. J Biol Chem, 286: 3194–3202, 2011.
18.
BellinM, MarchettoMC, GageFH, and MummeryCL. Induced pluripotent stem cells: the new patient?. Nat Rev Mol Cell Biol, 13: 713–726, 2012.
19.
BerardiE, PuesM, ThorrezL, and SampaolesiM. miRNAs in ESC differentiation. Am J Physiol Heart Circ Physiol, 303: H931–H939, 2012.
20.
BessisM. [Erythroblastic island, functional unity of bone marrow]. Rev Hematol, 13: 8–11, 1958 [Article in French].
21.
BiancoP. Bone and the hematopoietic niche: a tale of two stem cells. Blood, 117: 5281–5288, 2011.
22.
BiancoP, CaoX, FrenettePS, MaoJJ, RobeyPG, SimmonsPJ, and WangCY. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat Med, 19: 35–42, 2013.
23.
BisselsU, WildS, TomiukS, HafnerM, ScheelH, MihailovicA, ChoiYH, TuschlT, and BosioA. Combined characterization of microRNA and mRNA profiles delineates early differentiation pathways of CD133+ and CD34+ hematopoietic stem and progenitor cells. Stem Cells, 29: 847–857, 2011.
24.
BoyleWJ, SimonetWS, and LaceyDL. Osteoclast differentiation and activation. Nature, 423: 337–342, 2003.
25.
BryderD, RossiDJ, and WeissmanIL. Hematopoietic stem cells: the paradigmatic tissue-specific stem cell. Am J Pathol, 169: 338–346, 2006.
26.
BrzoskaE, CiemerychMA, PrzewozniakM, and ZimowskaM. Regulation of muscle stem cells activation: the role of growth factors and extracellular matrix. Vitam Horm, 87: 239–276, 2011.
27.
BurgessA, LiM, VanellaL, KimDH, RezzaniR, RodellaL, SodhiK, CanestraroM, MartasekP, PetersonSJ, KappasA, and AbrahamNG. Adipocyte heme oxygenase-1 induction attenuates metabolic syndrome in both male and female obese mice. Hypertension, 56: 1124–1130, 2010.
28.
CamilleriS and McDonaldF. Runx2 and dental development. Eur J Oral Sci, 114: 361–373, 2006.
29.
CaoJ, PetersonSJ, SodhiK, VanellaL, BarbagalloI, RodellaLF, SchwartzmanML, AbrahamNG, and KappasA. Heme oxygenase gene targeting to adipocytes attenuates adiposity and vascular dysfunction in mice fed a high-fat diet. Hypertension, 60: 467–475, 2012.
CaoYA, WagersAJ, KarsunkyH, ZhaoH, ReevesR, WongRJ, StevensonDK, WeissmanIL, and ContagCH. Heme oxygenase-1 deficiency leads to disrupted response to acute stress in stem cells and progenitors. Blood, 112: 4494–4502, 2008.
32.
CarrerM, LiuN, GrueterCE, WilliamsAH, FrisardMI, HulverMW, Bassel-DubyR, and OlsonEN. Control of mitochondrial metabolism and systemic energy homeostasis by microRNAs 378 and 378*. Proc Natl Acad Sci U S A, 109: 15330–15335, 2012.
33.
CarriereA, CarmonaMC, FernandezY, RigouletM, WengerRH, PenicaudL, and CasteillaL. Mitochondrial reactive oxygen species control the transcription factor CHOP-10/GADD153 and adipocyte differentiation: a mechanism for hypoxia-dependent effect. J Biol Chem, 279: 40462–40469, 2004.
34.
ChaeHJ, ChinHY, LeeGY, ParkHR, YangSK, ChungHT, PaeHO, KimHM, ChaeSW, and KimHR. Carbon monoxide and nitric oxide protect against tumor necrosis factor-alpha-induced apoptosis in osteoblasts: HO-1 is necessary to mediate the protection. Clin Chim Acta, 365: 270–278, 2006.
35.
ChargeSB and RudnickiMA. Cellular and molecular regulation of muscle regeneration. Physiol Rev, 84: 209–238, 2004.
36.
ChasisJA and MohandasN. Erythroblastic islands: niches for erythropoiesis. Blood, 112: 470–478, 2008.
37.
ChenJF, MandelEM, ThomsonJM, WuQ, CallisTE, HammondSM, ConlonFL, and WangDZ. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet, 38: 228–233, 2006.
38.
ChoiJ, CostaML, MermelsteinCS, ChagasC, HoltzerS, and HoltzerH. MyoD converts primary dermal fibroblasts, chondroblasts, smooth muscle, and retinal pigmented epithelial cells into striated mononucleated myoblasts and multinucleated myotubes. Proc Natl Acad Sci U S A, 87: 7988–7992, 1990.
39.
ChuCY, ChenCF, RajendranRS, ShenCN, ChenTH, YenCC, ChuangCK, LinDS, and HsiaoCD. Overexpression of Akt1 enhances adipogenesis and leads to lipoma formation in zebrafish. PLoS One, 7: e36474, 2012.
40.
ChungSS, HuW, and ParkCY. The role of microRNAs in hematopoietic stem cell and leukemic stem cell function. Ther Adv Hematol, 2: 317–334, 2011.
41.
CleriguesV, GuillenMI, CastejonMA, GomarF, MirabetV, and AlcarazMJ. Heme oxygenase-1 mediates protective effects on inflammatory, catabolic and senescence responses induced by interleukin-1beta in osteoarthritic osteoblasts. Biochem Pharmacol, 83: 395–405, 2012.
42.
CieslaM, SkrzypekK, KozakowskaM, LobodaA, JozkowiczA, DulakJ. MicroRNAs as biomarkers of disease onset. Anal Bioanal Chem, 401: 2051-2061, 2011.
43.
CleriguesV, GuillenMI, GomarF, and AlcarazMJ. Haem oxygenase-1 counteracts the effects of interleukin-1beta on inflammatory and senescence markers in cartilage-subchondral bone explants from osteoarthritic patients. Clin Sci (Lond), 122: 239–250, 2013.
44.
DulakJ, DeshaneJ, JozkowiczA, AgarwalA. Heme oxygenase-1 and carbon monoxide in vascular pathobiology: focus on angiogenesis. Circulation, 117: 231-241, 2008.
45.
CollinoF, BrunoS, DeregibusMC, TettaC, and CamussiG. MicroRNAs and mesenchymal stem cells. Vitam Horm, 87: 291–320, 2011.
CurtisHJ, SibleyCR, and WoodMJ. Mirtrons, an emerging class of atypical miRNA. Wiley Interdiscip Rev RNA, 3: 617–632, 2012.
48.
CurtisMA, LowVF, and FaullRL. Neurogenesis and progenitor cells in the adult human brain: a comparison between hippocampal and subventricular progenitor proliferation. Dev Neurobiol, 72: 990–1005, 2012.
49.
DeanM, FojoT, and BatesS. Tumour stem cells and drug resistance. Nat Rev Cancer, 5: 275–284, 2005.
50.
DengZ, DuWW, FangL, ShanSW, QianJ, LinJ, QianW, MaJ, RutnamZJ, and YangBB. The intermediate filament vimentin mediates microRNA miR-378 function in cellular self-renewal by regulating the expression of the Sox2 transcription factor. J Biol Chem, 288: 319–331, 2013.
51.
DenschlagD, MarculescuR, UnfriedG, HeflerLA, ExnerM, HashemiA, RienerEK, KeckC, TempferCB, and WagnerO. The size of a microsatellite polymorphism of the haem oxygenase 1 gene is associated with idiopathic recurrent miscarriage. Mol Hum Reprod, 10: 211–214, 2004.
52.
DeshaneJ, ChenS, CaballeroS, Grochot-PrzeczekA, WasH, Li CalziS, LachR, HockTD, ChenB, Hill-KapturczakN, SiegalGP, DulakJ, JozkowiczA, GrantMB, and AgarwalA. Stromal cell-derived factor 1 promotes angiogenesis via a heme oxygenase 1-dependent mechanism. J Exp Med, 204: 605–618, 2007.
53.
FallerM, MatsunagaM, YinS, LooJA, and GuoF. Heme is involved in microRNA processing. Nat Struct Mol Biol, 14: 23–29, 2007.
54.
FiresteinGS. Evolving concepts of rheumatoid arthritis. Nature, 423: 356–361, 2003.
55.
Fischer-PosovszkyP, TewsD, HorenburgS, DebatinKM, and WabitschM. Differential function of Akt1 and Akt2 in human adipocytes. Mol Cell Endocrinol, 358: 135–143, 2012.
56.
FumimotoR, SakaiE, YamaguchiY, SakamotoH, FukumaY, NishishitaK, OkamotoK, and TsukubaT. The coffee diterpene kahweol prevents osteoclastogenesis via impairment of NFATc1 expression and blocking of Erk phosphorylation. J Pharmacol Sci, 118: 479–486, 2012.
57.
GaganJ, DeyBK, LayerR, YanZ, and DuttaA. MicroRNA-378 targets the myogenic repressor MyoR during myoblast differentiation. J Biol Chem, 286: 19431–19438, 2011.
58.
GarzonR, GarofaloM, MartelliMP, BriesewitzR, WangL, Fernandez-CymeringC, VoliniaS, LiuCG, SchnittgerS, HaferlachT, LisoA, DiverioD, ManciniM, MeloniG, FoaR, MartelliMF, MecucciC, CroceCM, and FaliniB. Distinctive microRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucleophosmin. Proc Natl Acad Sci U S A, 105: 3945–3950, 2008.
59.
GerinI, BommerGT, McCoinCS, SousaKM, KrishnanV, and MacDougaldOA. Roles for miRNA-378/378* in adipocyte gene expression and lipogenesis. Am J Physiol Endocrinol Metab, 299: E198–E206, 2010.
60.
GimbleJM and NuttallME. The relationship between adipose tissue and bone metabolism. Clin Biochem, 45: 874–879, 2012.
61.
GorbunovN, PetrovskiG, GurusamyN, RayD, Kim doH, and DasDK. Regeneration of infarcted myocardium with resveratrol-modified cardiac stem cells. J Cell Mol Med, 16: 174–184, 2012.
62.
Grochot-PrzeczekA, DulakJ, and JozkowiczA. Haem oxygenase-1: non-canonical roles in physiology and pathology. Clin Sci (Lond), 122: 93–103, 2012.
63.
GromakN. Intronic microRNAs: a crossroad in gene regulation. Biochem Soc Trans, 40: 759–761, 2012.
64.
GuQ, CaiY, HuangC, ShiQ, and YangH. Curcumin increases rat mesenchymal stem cell osteoblast differentiation but inhibits adipocyte differentiation. Pharmacogn Mag, 8: 202–208, 2012.
65.
GuillenM, MegiasJ, GomarF, and AlcarazM. Haem oxygenase-1 regulates catabolic and anabolic processes in osteoarthritic chondrocytes. J Pathol, 214: 515–522, 2008.
HaH, KwakHB, LeeSW, JinHM, KimHM, KimHH, and LeeZH. Reactive oxygen species mediate RANK signaling in osteoclasts. Exp Cell Res, 301: 119–127, 2004.
68.
HamaM, KirinoY, TakenoM, TakaseK, MiyazakiT, YoshimiR, UedaA, Itoh-NakadaiA, MutoA, IgarashiK, and IshigatsuboY. Bach1 regulates osteoclastogenesis in a mouse model via both heme oxygenase 1-dependent and heme oxygenase 1-independent pathways. Arthritis Rheum, 64: 1518–1528, 2012.
69.
HeasmanSA, ZaitsevaL, BowlesKM, RushworthSA, and MacewanDJ. Protection of acute myeloid leukaemia cells from apoptosis induced by front-line chemotherapeutics is mediated by haem oxygenase-1. Oncotarget, 2: 658–668, 2011.
70.
HerrmannH, KneidingerM, Cerny-ReitererS, RulickeT, WillmannM, GleixnerKV, BlattK, HormannG, PeterB, SamorapoompichitP, PicklW, BharateGY, MayerhoferM, SperrWR, MaedaH, and ValentP. The Hsp32 inhibitors SMA-ZnPP and PEG-ZnPP exert major growth-inhibitory effects on D34+/CD38+ and CD34+/CD38- AML progenitor cells. Curr Cancer Drug Targets, 12: 51–63, 2012.
71.
HinoiE, FujimoriS, WangL, HojoH, UnoK, and YonedaY. Nrf2 negatively regulates osteoblast differentiation via interfering with Runx2-dependent transcriptional activation. J Biol Chem, 281: 18015–18024, 2006.
HolstD, LuquetS, KristiansenK, and GrimaldiPA. Roles of peroxisome proliferator-activated receptors delta and gamma in myoblast transdifferentiation. Exp Cell Res, 288: 168–176, 2003.
74.
HouW, TianQ, SteuerwaldNM, SchrumLW, and BonkovskyHL. The let-7 microRNA enhances heme oxygenase-1 by suppressing Bach1 and attenuates oxidant injury in human hepatocytes. Biochim Biophys Acta, 1819: 1113–1122, 2012.
75.
HouW, TianQ, ZhengJ, and BonkovskyHL. MicroRNA-196 represses Bach1 protein and hepatitis C virus gene expression in human hepatoma cells expressing hepatitis C viral proteins. Hepatology, 51: 1494–1504, 2010.
76.
HuR, LiH, LiuW, YangL, TanYF, and LuoXH. Targeting miRNAs in osteoblast differentiation and bone formation. Expert Opin Ther Targets, 14: 1109–1120, 2010.
77.
IbrahimNG, LuttonJD, and LevereRD. The role of haem biosynthetic and degradative enzymes in erythroid colony development: the effect of haemin. Br J Haematol, 50: 17–28, 1982.
78.
InoseH, OchiH, KimuraA, FujitaK, XuR, SatoS, IwasakiM, SunamuraS, TakeuchiY, FukumotoS, SaitoK, NakamuraT, SiomiH, ItoH, AraiY, ShinomiyaK, and TakedaS. A microRNA regulatory mechanism of osteoblast differentiation. Proc Natl Acad Sci U S A, 106: 20794–20799, 2009.
79.
ItoigawaY, KishimotoKN, OkunoH, SanoH, KanekoK, and ItoiE. Hypoxia induces adipogenic differentitation of myoblastic cell lines. Biochem Biophys Res Commun, 399: 721–726, 2010.
80.
JazwaA, StepniewskiJ, ZamykalM, JagodzinskaJ, MeloniM, EmanueliC, JozkowiczA, and DulakJ. Pre-emptive hypoxia-regulated HO-1 gene therapy improves post-ischaemic limb perfusion and tissue regeneration in mice. Cardiovasc Res, 97: 115–124, 2013.
81.
JensenED, GopalakrishnanR, and WestendorfJJ. Regulation of gene expression in osteoblasts. Biofactors, 36: 25–32, 2010.
82.
JiangYB, ZhangXL, TangYL, MaGS, ShenCX, WeiQ, ZhuQ, YaoYY, and LiuNF. Effects of heme oxygenase-1 gene modulated mesenchymal stem cells on vasculogenesis in ischemic swine hearts. Chin Med J (Engl), 124: 401–407, 2011.
83.
JingQ, HuangS, GuthS, ZarubinT, MotoyamaA, ChenJ, Di PadovaF, LinSC, GramH, and HanJ. Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell, 120: 623–634, 2005.
84.
JozkowiczA and DulakJ. Effects of protoporphyrins on production of nitric oxide and expression of vascular endothelial growth factor in vascular smooth muscle cells and macrophages. Acta Biochim Pol, 50: 69–79, 2003.
85.
KapinasK and DelanyAM. MicroRNA biogenesis and regulation of bone remodeling. Arthritis Res Ther, 13: 220, 2011.
86.
KapinasK, KesslerCB, and DelanyAM. miR-29 suppression of osteonectin in osteoblasts: regulation during differentiation and by canonical Wnt signaling. J Cell Biochem, 108: 216–224, 2009.
87.
KartikasariAE, WagenerFA, YachieA, WiegerinckET, KemnaEH, and SwinkelsDW. Hepcidin suppression and defective iron recycling account for dysregulation of iron homeostasis in heme oxygenase-1 deficiency. J Cell Mol Med, 13: 3091–3102, 2009.
88.
Kearns-JonkerM, DaiW, GunthartM, FuentesT, YehHY, GerczukP, PeraM, MummeryC, and KlonerRA. Genetically engineered mesenchymal stem cells influence gene expression in donor cardiomyocytes and the recipient heart. J Stem Cell Res Ther, S1, pii: 005, 2012.
89.
KennellJA, GerinI, MacDougaldOA, and CadiganKM. The microRNA miR-8 is a conserved negative regulator of Wnt signaling. Proc Natl Acad Sci U S A, 105: 15417–15422, 2008.
90.
KieJH, KapturczakMH, TraylorA, AgarwalA, and Hill-KapturczakN. Heme oxygenase-1 deficiency promotes epithelial-mesenchymal transition and renal fibrosis. J Am Soc Nephrol, 19: 1681–1691, 2008.
91.
KimDH, BurgessAP, LiM, TsenovoyPL, AddabboF, McClungJA, PuriN, and AbrahamNG. Heme oxygenase-mediated increases in adiponectin decrease fat content and inflammatory cytokines tumor necrosis factor-alpha and interleukin-6 in Zucker rats and reduce adipogenesis in human mesenchymal stem cells. J Pharmacol Exp Ther, 325: 833–840, 2008.
92.
KimDH, LiuJ, BhatS, BenedictG, Lecka-CzernikB, PetersonSJ, EbraheimNA, and HeckBE. Peroxisome proliferator-activated receptor delta agonist attenuates nicotine suppression effect on human mesenchymal stem cell-derived osteogenesis and involves increased expression of heme oxygenase-1. J Bone Miner Metab, 31: 44–52, 2012.
93.
KimDH, VanellaL, InoueK, BurgessA, GotlingerK, ManthatiVL, KoduruSR, ZeldinDC, FalckJR, SchwartzmanML, and AbrahamNG. Epoxyeicosatrienoic acid agonist regulates human mesenchymal stem cell-derived adipocytes through activation of HO-1-pAKT signaling and a decrease in PPARgamma. Stem Cells Dev, 19: 1863–1873, 2010.
94.
KimEK, LimS, ParkJM, SeoJK, KimJH, KimKT, RyuSH, and SuhPG. Human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by AMP-activated protein kinase. J Cell Physiol, 227: 1680–1687, 2012.
KimHR, KimS, KimEJ, ParkJH, YangSH, JeongET, ParkC, YounMJ, SoHS, and ParkR. Suppression of Nrf2-driven heme oxygenase-1 enhances the chemosensitivity of lung cancer A549 cells toward cisplatin. Lung Cancer, 60: 47–56, 2008.
97.
KimKM, ParkSJ, JungSH, KimEJ, JogeswarG, AjitaJ, RheeY, KimCH, and LimSK. miR-182 is a negative regulator of osteoblast proliferation, differentiation, and skeletogenesis through targeting FoxO1. J Bone Miner Res, 27: 1669–1679, 2012.
98.
KimSH, KimKH, YooBC, and KuJL. Induction of LGR5 by H2O2 treatment is associated with cell proliferation via the JNK signaling pathway in colon cancer cells. Int J Oncol, 41: 1744–1750, 2012.
99.
KimSJ, MinKS, RyuHW, LeeHJ, and KimEC. The role of heme oxygenase-1 in the proliferation and odontoblastic differentiation of human dental pulp cells. J Endod, 36: 1326–1331, 2010.
100.
KleinU, LiaM, CrespoM, SiegelR, ShenQ, MoT, Ambesi-ImpiombatoA, CalifanoA, MigliazzaA, BhagatG, and Dalla-FaveraR. The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell, 17: 28–40, 2010.
101.
KongpetchS, KukongviriyapanV, PrawanA, SenggunpraiL, KukongviriyapanU, and BuranratB. Crucial role of heme oxygenase-1 on the sensitivity of cholangiocarcinoma cells to chemotherapeutic agents. PLoS One, 7: e34994, 2012.
102.
KookYA, LeeSK, SonDH, KimY, KangKH, ChoJH, KimSC, KimYS, LeeHJ, LeeSK, and KimEC. Effects of substance P on osteoblastic differentiation and heme oxygenase-1 in human periodontal ligament cells. Cell Biol Int, 33: 424–428, 2009.
KreiserD, NguyenX, WongR, SeidmanD, StevensonD, QuanS, AbrahamN, and DenneryPA. Heme oxygenase-1 modulates fetal growth in the rat. Lab Invest, 82: 687–692, 2002.
105.
KrishnanV, BryantHU, and MacdougaldOA. Regulation of bone mass by Wnt signaling. J Clin Invest, 116: 1202–1209, 2006.
106.
KuangS, GillespieMA, and RudnickiMA. Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell, 2: 22–31, 2008.
107.
KuangS and RudnickiMA. The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med, 14: 82–91, 2008.
108.
KuangW, TanJ, DuanY, DuanJ, WangW, JinF, JinZ, YuanX, and LiuY. Cyclic stretch induced miR-146a upregulation delays C2C12 myogenic differentiation through inhibition of Numb. Biochem Biophys Res Commun, 378: 259–263, 2009.
109.
KumarR, HalderP, SahuSK, KumarM, KumariM, JanaK, GhoshZ, SharmaP, KunduM, and BasuJ. Identification of a novel role of ESAT-6-dependent miR-155 induction during infection of macrophages with Mycobacterium tuberculosis. Cell Microbiol, 14: 1620–1631, 2012.
110.
KunathT, Saba-El-LeilMK, AlmousailleakhM, WrayJ, MelocheS, and SmithA. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development, 134: 2895–2902, 2007.
111.
LakkistoP, KytoV, ForstenH, SirenJM, SegersvardH, Voipio-PulkkiLM, LaineM, PulkkiK, and TikkanenI. Heme oxygenase-1 and carbon monoxide promote neovascularization after myocardial infarction by modulating the expression of HIF-1alpha, SDF-1alpha and VEGF-B. Eur J Pharmacol, 635: 156–164, 2010.
112.
LaumonierT, YangS, KonigS, ChauveauC, AnegonI, HoffmeyerP, and MenetreyJ. Lentivirus mediated HO-1 gene transfer enhances myogenic precursor cell survival after autologous transplantation in pig. Mol Ther, 16: 404–410, 2008.
113.
LeeH, LeeYJ, ChoiH, KoEH, and KimJW. Reactive oxygen species facilitate adipocyte differentiation by accelerating mitotic clonal expansion. J Biol Chem, 284: 10601–10609, 2009.
114.
LeeNK, ChoiYG, BaikJY, HanSY, JeongDW, BaeYS, KimN, and LeeSY. A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood, 106: 852–859, 2005.
115.
LeeSJ, LeeEJ, KimSH, ChoiI, LeeDM, LeeHJ, YoonD, and ChunT. IL-17A promotes transdifferentiation of mouse myoblast cells (C2C12) into adipocytes by increasing the expression of peroxisome proliferator-activated receptor gamma through CAAT/enhancer binding protein beta signaling. Biotechnol Lett, 33: 229–235, 2011.
116.
LeeSK, LeeCY, KookYA, LeeSK, and KimEC. Mechanical stress promotes odontoblastic differentiation via the heme oxygenase-1 pathway in human dental pulp cell line. Life Sci, 86: 107–114, 2010.
117.
LeeTC and HoIC. Expression of heme oxygenase in arsenic-resistant human lung adenocarcinoma cells. Cancer Res, 54: 1660–1664, 1994.
118.
LeeYH, LeeNH, BhattaraiG, KimGE, LeeIK, YunBS, HwangPH, and YiHK. Anti-inflammatory effect of pachymic acid promotes odontoblastic differentiation via HO-1 in dental pulp cells. Oral Dis, 19: 193–199, 2012.
119.
LefebvreV and BhattaramP. Vertebrate skeletogenesis. Curr Top Dev Biol, 90: 291–317, 2010.
120.
LiL, JulienB, GrenardP, Teixeira-ClercF, MallatA, and LotersztajnS. Molecular mechanisms regulating the antifibrogenic protein heme-oxygenase-1 in human hepatic myofibroblasts. J Hepatol, 41: 407–413, 2004.
121.
LiM, KimDH, TsenovoyPL, PetersonSJ, RezzaniR, RodellaLF, AronowWS, IkeharaS, and AbrahamNG. Treatment of obese diabetic mice with a heme oxygenase inducer reduces visceral and subcutaneous adiposity, increases adiponectin levels, and improves insulin sensitivity and glucose tolerance. Diabetes, 57: 1526–1535, 2008.
122.
LiZ, HassanMQ, JafferjiM, AqeilanRI, GarzonR, CroceCM, van WijnenAJ, SteinJL, SteinGS, and LianJB. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem, 284: 15676–15684, 2009.
123.
LiZ, HassanMQ, VoliniaS, van WijnenAJ, SteinJL, CroceCM, LianJB, and SteinGS. A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc Natl Acad Sci U S A, 105: 13906–13911, 2008.
124.
Li VoltiG, IentileR, AbrahamNG, VanellaA, CannavoG, MazzaF, CurroM, RacitiG, AvolaR, and CampisiA. Immunocytochemical localization and expression of heme oxygenase-1 in primary astroglial cell cultures during differentiation: effect of glutamate. Biochem Biophys Res Commun, 315: 517–524, 2004.
125.
LianJB, SteinGS, JavedA, van WijnenAJ, SteinJL, MontecinoM, HassanMQ, GaurT, LengnerCJ, and YoungDW. Networks and hubs for the transcriptional control of osteoblastogenesis. Rev Endocr Metab Disord, 7: 1–16, 2006.
LichnerZ, PallE, KerekesA, PallingerE, MaraghechiP, BoszeZ, and GoczaE. The miR-290–295 cluster promotes pluripotency maintenance by regulating cell cycle phase distribution in mouse embryonic stem cells. Differentiation, 81: 11–24, 2011.
128.
LinCY, PengCY, HuangTT, WuML, LaiYL, PengDH, ChenPF, ChenHF, YenBL, WuKK, and YetSF. Exacerbation of oxidative stress-induced cell death and differentiation in induced pluripotent stem cells lacking heme oxygenase-1. Stem Cells Dev, 21: 1675–1687, 2012.
129.
LinHH, ChenYH, YetSF, and ChauLY. After vascular injury, heme oxygenase-1/carbon monoxide enhances re-endothelialization via promoting mobilization of circulating endothelial progenitor cells. J Thromb Haemost, 7: 1401–1408, 2009.
130.
LinQ, WeisS, YangG, WengYH, HelstonR, RishK, SmithA, BordnerJ, PolteT, GaunitzF, and DenneryPA. Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress. J Biol Chem, 282: 20621–20633, 2007.
131.
LinTC, YenJM, GongKB, HsuTT, and ChenLR. IGF-1/IGFBP-1 increases blastocyst formation and total blastocyst cell number in mouse embryo culture and facilitates the establishment of a stem-cell line. BMC Cell Biol, 4: 14, 2003.
132.
LinTH, TangCH, HungSY, LiuSH, LinYM, FuWM, and YangRS. Upregulation of heme oxygenase-1 inhibits the maturation and mineralization of osteoblasts. J Cell Physiol, 222: 757–768, 2010.
133.
LobodaA, JazwaA, Grochot-PrzeczekA, RutkowskiAJ, CisowskiJ, AgarwalA, JozkowiczA, and DulakJ. Heme oxygenase-1 and the vascular bed: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal, 10: 1767–1812, 2008.
134.
LobodaA, WasH, JozkowiczA, and DulakJ. Janus face of Nrf2-HO-1 axis in cancer—friend in chemoprevention, foe in anticancer therapy. Lung Cancer, 60: 1–3, 2008.
135.
LoweCE, O'RahillyS, and RochfordJJ. Adipogenesis at a glance. J Cell Sci, 124: 2681–2686, 2011.
136.
MallannaSK and RizzinoA. Emerging roles of microRNAs in the control of embryonic stem cells and the generation of induced pluripotent stem cells. Dev Biol, 344: 16–25, 2010.
Martin-PuigS, FusterV, and TorresM. Heart repair: from natural mechanisms of cardiomyocyte production to the design of new cardiac therapies. Ann N Y Acad Sci, 1254: 71–81, 2012.
139.
MayerhoferM, FlorianS, KrauthMT, AichbergerKJ, BilbanM, MarculescuR, PrintzD, FritschG, WagnerO, SelzerE, SperrWR, ValentP, and SillaberC. Identification of heme oxygenase-1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res, 64: 3148–3154, 2004.
140.
MayerhoferM, GleixnerKV, MayerhoferJ, HoermannG, JaegerE, AichbergerKJ, OttRG, GreishK, NakamuraH, DerdakS, SamorapoompichitP, PicklWF, SexlV, EsterbauerH, SchwarzingerI, SillaberC, MaedaH, and ValentP. Targeting of heat shock protein 32 (Hsp32)/heme oxygenase-1 (HO-1) in leukemic cells in chronic myeloid leukemia: a novel approach to overcome resistance against imatinib. Blood, 111: 2200–2210, 2008.
141.
McCaigD and LyallF. Heme oxygenase expression in human placental villous tissue in response to exposure to in vitro ischemia-reperfusion injury. Hypertens Pregnancy, 28: 256–272, 2009.
142.
McCaigD and LyallF. Inhibitors of heme oxygenase reduce invasion of human primary cytotrophoblast cells in vitro. Placenta, 30: 536–538, 2009.
143.
McGregorRA and ChoiMS. microRNAs in the regulation of adipogenesis and obesity. Curr Mol Med, 11: 304–316, 2011.
144.
MegiasJ, GuillenMI, CleriguesV, RojoAI, CuadradoA, CastejonMA, GomarF, and AlcarazMJ. Heme oxygenase-1 induction modulates microsomal prostaglandin E synthase-1 expression and prostaglandin E(2) production in osteoarthritic chondrocytes. Biochem Pharmacol, 77: 1806–1813, 2009.
145.
MeltonC, JudsonRL, and BlellochR. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature, 463: 621–626, 2010.
146.
MerchantAA, SinghA, MatsuiW, and BiswalS. The redox-sensitive transcription factor Nrf2 regulates murine hematopoietic stem cell survival independently of ROS levels. Blood, 118: 6572–6579, 2011.
147.
MinKS, LeeYM, HongSO, and KimEC. Simvastatin promotes odontoblastic differentiation and expression of angiogenic factors via heme oxygenase-1 in primary cultured human dental pulp cells. J Endod, 36: 447–452, 2010.
MizunoY, TokuzawaY, NinomiyaY, YagiK, Yatsuka-KanesakiY, SudaT, FukudaT, KatagiriT, KondohY, AmemiyaT, TashiroH, and OkazakiY. miR-210 promotes osteoblastic differentiation through inhibition of AcvR1b. FEBS Lett, 583: 2263–2268, 2009.
150.
MotohashiH, KimuraM, FujitaR, InoueA, PanX, TakayamaM, KatsuokaF, AburataniH, BresnickEH, and YamamotoM. NF-E2 domination over Nrf2 promotes ROS accumulation and megakaryocytic maturation. Blood, 115: 677–686, 2010.
151.
MounierR, ChretienF, and ChazaudB. Blood vessels and the satellite cell niche. Curr Top Dev Biol, 96: 121–138, 2010.
152.
MurchisonEP, PartridgeJF, TamOH, CheloufiS, and HannonGJ. Characterization of Dicer-deficient murine embryonic stem cells. Proc Natl Acad Sci U S A, 102: 12135–12140, 2005.
153.
NaJ, FurueMK, and AndrewsPW. Inhibition of ERK1/2 prevents neural and mesendodermal differentiation and promotes human embryonic stem cell self-renewal. Stem Cell Res, 5: 157–169, 2010.
154.
NakamuraH, FangJ, GahininathB, TsukigawaK, and MaedaH. Intracellular uptake and behavior of two types zinc protoporphyrin (ZnPP) micelles, SMA-ZnPP and PEG-ZnPP as anticancer agents; unique intracellular disintegration of SMA micelles. J Control Release, 155: 367–375, 2011.
155.
NakasaT, ShibuyaH, NagataY, NiimotoT, and OchiM. The inhibitory effect of microRNA-146a expression on bone destruction in collagen-induced arthritis. Arthritis Rheum, 63: 1582–1590, 2011.
NowakW, BorysS, KusinskaK, Bukowaska-StrakovaK, WitekP, KoblikT, JozkowiczA, MaleckiM, and DulakJ. Number of circulating pro-angiogenic cells, growth factor and antioxidative gene profiles may be altered in type 2 diabetes with and without diabetic foot syndrome. J Diabetes Invest, 2013 [Epub ahead of print]; DOI: 10.1111/jdi.12131.
O'ConnellRM and BaltimoreD. MicroRNAs and hematopoietic cell development. Curr Top Dev Biol, 99: 145–174, 2012.
161.
O'ConnellRM, RaoDS, ChaudhuriAA, BoldinMP, TaganovKD, NicollJ, PaquetteRL, and BaltimoreD. Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J Exp Med, 205: 585–594, 2008.
162.
O'RourkeJR, GeorgesSA, SeayHR, TapscottSJ, McManusMT, GoldhamerDJ, SwansonMS, and HarfeBD. Essential role for Dicer during skeletal muscle development. Dev Biol, 311: 359–368, 2007.
163.
OdemisV, BoosmannK, DieterlenMT, and EngeleJ. The chemokine SDF1 controls multiple steps of myogenesis through atypical PKCzeta. J Cell Sci, 120: 4050–4059, 2007.
164.
OkitaK and YamanakaS. Induced pluripotent stem cells: opportunities and challenges. Philos Trans R Soc Lond B Biol Sci, 366: 2198–2207, 2011.
165.
OskowitzAZ, LuJ, PenfornisP, YlostaloJ, McBrideJ, FlemingtonEK, ProckopDJ, and PochampallyR. Human multipotent stromal cells from bone marrow and microRNA: regulation of differentiation and leukemia inhibitory factor expression. Proc Natl Acad Sci U S A, 105: 18372–18377, 2008.
166.
PariseG, O'ReillyCE, and RudnickiMA. Molecular regulation of myogenic progenitor populations. Appl Physiol Nutr Metab, 31: 773–781, 2006.
167.
ParkHJ, ChungBY, LeeMK, SongY, LeeSS, ChuGM, KangSN, SongYM, KimGS, and ChoJH. Centipede grass exerts anti-adipogenic activity through inhibition of C/EBPbeta, C/EBPalpha, and PPARgamma expression and the AKT signaling pathway in 3T3-L1 adipocytes. BMC Complement Altern Med, 12: 230, 2012.
168.
PilegaardH, OrdwayGA, SaltinB, and NeuferPD. Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab, 279: E806–E814, 2000.
169.
PopovicR, RiesbeckLE, VeluCS, ChaubeyA, ZhangJ, AchilleNJ, ErfurthFE, EatonK, LuJ, GrimesHL, ChenJ, RowleyJD, and Zeleznik-LeNJ. Regulation of mir-196b by MLL and its overexpression by MLL fusions contributes to immortalization. Blood, 113: 3314–3322, 2009.
170.
PossKD and TonegawaS. Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci U S A, 94: 10925–10930, 1997.
171.
PulkkinenKH, Yla-HerttualaS, and LevonenAL. Heme oxygenase 1 is induced by miR-155 via reduced BACH1 translation in endothelial cells. Free Radic Biol Med, 51: 2124–2131, 2011.
172.
QiuL, FanH, JinW, ZhaoB, WangY, JuY, ChenL, ChenY, DuanZ, and MengS. miR-122-induced down-regulation of HO-1 negatively affects miR-122-mediated suppression of HBV. Biochem Biophys Res Commun, 398: 771–777, 2010.
173.
RelaixF and ZammitPS. Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development, 139: 2845–2856, 2012.
174.
ReyaT, MorrisonSJ, ClarkeMF, and WeissmanIL. Stem cells, cancer, and cancer stem cells. Nature, 414: 105–111, 2001.
175.
RomaoJM, JinW, DodsonMV, HausmanGJ, MooreSS, and GuanLL. MicroRNA regulation in mammalian adipogenesis. Exp Biol Med (Maywood), 236: 997–1004, 2011.
176.
RushworthSA, BowlesKM, RaningaP, and MacEwanDJ. NF-kappaB-inhibited acute myeloid leukemia cells are rescued from apoptosis by heme oxygenase-1 induction. Cancer Res, 70: 2973–2983, 2010.
177.
RushworthSA and MacEwanDJ. HO-1 underlies resistance of AML cells to TNF-induced apoptosis. Blood, 111: 3793–3801, 2008.
178.
RyterSW, AlamJ, and ChoiAM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev, 86: 583–650, 2006.
179.
SakaiE, Shimada-SugawaraM, NishishitaK, FukumaY, NaitoM, OkamotoK, NakayamaK, and TsukubaT. Suppression of RANKL-dependent heme oxygenase-1 is required for high mobility group box 1 release and osteoclastogenesis. J Cell Biochem, 113: 486–498, 2012.
180.
SakamotoH, SakaiE, FumimotoR, YamaguchiY, FukumaY, NishishitaK, OkamotoK, and TsukubaT. Deltamethrin inhibits osteoclast differentiation via regulation of heme oxygenase-1 and NFATc1. Toxicol In Vitro, 26: 817–822, 2012.
SaxenaS, ShuklaD, SaxenaS, KhanYA, SinghM, BansalA, SairamM, and JainSK. Hypoxia preconditioning by cobalt chloride enhances endurance performance and protects skeletal muscles from exercise-induced oxidative damage in rats. Acta Physiol (Oxf), 200: 249–263, 2010.
183.
SchipperHM, SongW, ZukorH, HascaloviciJR, and ZeligmanD. Heme oxygenase-1 and neurodegeneration: expanding frontiers of engagement. J Neurochem, 110: 469–485, 2009.
184.
SchneiderKS and ChanJY. Emerging role of nrf2 in adipocytes and adipose biology. Adv Nutr, 4: 62–66, 2013.
185.
ShinDH, ParkHM, JungKA, ChoiHG, KimJA, KimDD, KimSG, KangKW, KuSK, KenslerTW, and KwakMK. The NRF2-heme oxygenase-1 system modulates cyclosporin A-induced epithelial-mesenchymal transition and renal fibrosis. Free Radic Biol Med, 48: 1051–1063, 2010.
186.
ShuT, ZengB, RenX, and LiY. HO-1 modified mesenchymal stem cells modulate MMPs/TIMPs system and adverse remodeling in infarcted myocardium. Tissue Cell, 42: 217–222, 2010.
187.
SiminovitchL, McCullochEA, and TillJE. The distribution of colony-forming cells among spleen colonies. J Cell Physiol, 62: 327–336, 1963.
188.
SinghMM, IrwinME, GaoY, BanK, ShiP, ArlinghausRB, AminHM, and ChandraJ. Inhibition of the NADPH oxidase regulates heme oxygenase 1 expression in chronic myeloid leukemia. Cancer, 118: 3433–3445, 2012.
189.
SkrzypekK, TertilM, GoldaS, CieslaM, WeglarczykK, ColletG, GuichardA, KozakowskaM, BoczkowskiJ, WasH, GilT, KuzdzalJ, MuchovaL, VitekL, LobodaA, JozkowiczA, KiedaC, and DulakJ. Interplay between heme oxygenase-1 and miR-378 affects non-small cell lung carcinoma growth, vascularization and metastasis. Antioxid Redox Signal, 19: 644–660, 2013.
190.
SoAY, Garcia-FloresY, MinisandramA, MartinA, TaganovK, BoldinM, and BaltimoreD. Regulation of APC development, immune response, and autoimmunity by Bach1/HO-1 pathway in mice. Blood, 120: 2428–2437, 2012.
191.
SodhiK, InoueK, GotlingerKH, CanestraroM, VanellaL, KimDH, ManthatiVL, KoduruSR, FalckJR, SchwartzmanML, and AbrahamNG. Epoxyeicosatrienoic acid agonist rescues the metabolic syndrome phenotype of HO-2-null mice. J Pharmacol Exp Ther, 331: 906–916, 2009.
192.
SodhiK, PuriN, InoueK, FalckJR, SchwartzmanML, and AbrahamNG. EET agonist prevents adiposity and vascular dysfunction in rats fed a high fat diet via a decrease in Bach 1 and an increase in HO-1 levels. Prostaglandins Other Lipid Mediat, 98: 133–142, 2012.
193.
SohniA and VerfaillieCM. Multipotent adult progenitor cells. Best Pract Res Clin Haematol, 24: 3–11, 2011.
194.
SokolNS. The role of microRNAs in muscle development. Curr Top Dev Biol, 99: 59–78, 2012.
195.
StachurskaA, CieslaM, KozakowskaM, WolfframS, Boesch-SaadatmandiC, RimbachG, JozkowiczA, DulakJ, and LobodaA. Cross-talk between microRNAs, nuclear factor E2-related factor 2, and heme oxygenase-1 in ochratoxin A-induced toxic effects in renal proximal tubular epithelial cells. Mol Nutr Food Res, 57: 504–515, 2013.
StavridisMP, LunnJS, CollinsBJ, and StoreyKG. A discrete period of FGF-induced Erk1/2 signalling is required for vertebrate neural specification. Development, 134: 2889–2894, 2007.
198.
StefaniG and SlackFJ. Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol, 9: 219–230, 2008.
199.
SudaT, TakuboK, and SemenzaGL. Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell, 9: 298–310, 2011.
200.
SugataniT and HruskaKA. Impaired micro-RNA pathways diminish osteoclast differentiation and function. J Biol Chem, 284: 4667–4678, 2009.
201.
SuhGY, JinY, YiAK, WangXM, and ChoiAM. CCAAT/enhancer-binding protein mediates carbon monoxide-induced suppression of cyclooxygenase-2. Am J Respir Cell Mol Biol, 35: 220–226, 2006.
202.
TakadaI, KouzmenkoAP, and KatoS. Molecular switching of osteoblastogenesis versus adipogenesis: implications for targeted therapies. Expert Opin Ther Targets, 13: 593–603, 2009.
203.
TakadaI, KouzmenkoAP, and KatoS. Wnt and PPARgamma signaling in osteoblastogenesis and adipogenesis. Nat Rev Rheumatol, 5: 442–447, 2009.
204.
TangQQ and LaneMD. Adipogenesis: from stem cell to adipocyte. Annu Rev Biochem, 81: 715–736, 2012.
205.
TangYL, TangY, ZhangYC, QianK, ShenL, and PhillipsMI. Improved graft mesenchymal stem cell survival in ischemic heart with a hypoxia-regulated heme oxygenase-1 vector. J Am Coll Cardiol, 46: 1339–1350, 2005.
206.
TaussigDC, Miraki-MoudF, Anjos-AfonsoF, PearceDJ, AllenK, RidlerC, LillingtonD, OakerveeH, CavenaghJ, AgrawalSG, ListerTA, GribbenJG, and BonnetD. Anti-CD38 antibody-mediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells. Blood, 112: 568–575, 2008.
207.
TeitelbaumSL and RossFP. Genetic regulation of osteoclast development and function. Nat Rev Genet, 4: 638–649, 2003.
208.
ThomasED, LochteHLJr., CannonJH, SahlerOD, and FerrebeeJW. Supralethal whole body irradiation and isologous marrow transplantation in man. J Clin Invest, 38: 1709–1716, 1959.
209.
TillJE and McCE. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res, 14: 213–222, 1961.
210.
TongAW and NemunaitisJ. Modulation of miRNA activity in human cancer: a new paradigm for cancer gene therapy?. Cancer Gene Ther, 15: 341–355, 2008.
211.
ToobiakS, ShaklaiM, and ShaklaiN. Carbon monoxide induced erythroid differentiation of K562 cells mimics the central macrophage milieu in erythroblastic islands. PLoS One, 7: e33940, 2012.
212.
Townley-TilsonWH, CallisTE, and WangD. MicroRNAs 1, 133, and 206: critical factors of skeletal and cardiac muscle development, function, and disease. Int J Biochem Cell Biol, 42: 1252–1255, 2010.
213.
TreiberT, TreiberN, and MeisterG. Regulation of microRNA biogenesis and function. Thromb Haemost, 107: 605–610, 2012.
214.
TrigonaWL, PorterCM, Horvath-ArcidiaconoJA, MajumdarAS, and BloomET. Could heme-oxygenase-1 have a role in modulating the recipient immune response to embryonic stem cells?. Antioxid Redox Signal, 9: 751–756, 2007.
TsubokawaT, YagiK, NakanishiC, ZukaM, NoharaA, InoH, FujinoN, KonnoT, KawashiriMA, Ishibashi-UedaH, NagayaN, and YamagishiM. Impact of anti-apoptotic and anti-oxidative effects of bone marrow mesenchymal stem cells with transient overexpression of heme oxygenase-1 on myocardial ischemia. Am J Physiol Heart Circ Physiol, 298: H1320–H1329, 2010.
217.
Valencia-SanchezMA, LiuJ, HannonGJ, and ParkerR. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev, 20: 515–524, 2006.
218.
van RooijE, QuiatD, JohnsonBA, SutherlandLB, QiX, RichardsonJA, KelmRJJr., and OlsonEN. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell, 17: 662–673, 2009.
219.
van RooijE, SutherlandLB, QiX, RichardsonJA, HillJ, and OlsonEN. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science, 316: 575–579, 2007.
220.
van TienenFH, LaeremansH, van der KallenCJ, and SmeetsHJ. Wnt5b stimulates adipogenesis by activating PPARgamma, and inhibiting the beta-catenin dependent Wnt signaling pathway together with Wnt5a. Biochem Biophys Res Commun, 387: 207–211, 2009.
VanellaL, KimDH, SodhiK, BarbagalloI, BurgessAP, FalckJR, SchwartzmanML, and AbrahamNG. Crosstalk between EET and HO-1 downregulates Bach1 and adipogenic marker expression in mesenchymal stem cell derived adipocytes. Prostaglandins Other Lipid Mediat, 96: 54–62, 2011.
223.
WangLD and WagersAJ. Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nat Rev Mol Cell Biol, 12: 643–655, 2011.
224.
WangY, MedvidR, MeltonC, JaenischR, and BlellochR. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet, 39: 380–385, 2007.
225.
Watanabe-MatsuiM, MutoA, MatsuiT, Itoh-NakadaiA, NakajimaO, MurayamaK, YamamotoM, Ikeda-SaitoM, and IgarashiK. Heme regulates B-cell differentiation, antibody class switch, and heme oxygenase-1 expression in B cells as a ligand of Bach2. Blood, 117: 5438–5448, 2011.
226.
WatanabeS, AkagiR, MoriM, TsuchiyaT, and SassaS. Marked developmental changes in heme oxygenase-1 (HO-1) expression in the mouse placenta: correlation between HO-1 expression and placental development. Placenta, 25: 387–395, 2004.
227.
WatanabeT, HasegawaG, YamamotoT, HatakeyamaK, SuematsuM, and NaitoM. Expression of heme oxygenase-1 in rat ontogeny. Arch Histol Cytol, 66: 155–162, 2003.
228.
WeissmanIL. Translating stem and progenitor cell biology to the clinic: barriers and opportunities. Science, 287: 1442–1446, 2000.
229.
WengJJ and SuY. Nuclear matrix-targeting of the osteogenic factor Runx2 is essential for its recognition and activation of the alkaline phosphatase gene. Biochim Biophys Acta, 1830, 2839–2852, 2012.
230.
WongRJ, ZhaoH, and StevensonDK. A deficiency in haem oxygenase-1 induces foetal growth restriction by placental vasculature defects. Acta Paediatr, 101: 827–834, 2012.
231.
WruckCJ, FragoulisA, GurzynskiA, BrandenburgLO, KanYW, ChanK, HassenpflugJ, Freitag-WolfS, VarogaD, LipprossS, and PufeT. Role of oxidative stress in rheumatoid arthritis: insights from the Nrf2-knockout mice. Ann Rheum Dis, 70: 844–850, 2011.
XiaZ, ChenC, ChenP, XieH, and LuoX. MicroRNAs and their roles in osteoclast differentiation. Front Med, 5: 414–419, 2011.
234.
XiaZW, ZhongWW, MeyrowitzJS, and ZhangZL. The role of heme oxygenase-1 in T cell-mediated immunity: the all encompassing enzyme. Curr Pharm Des, 14: 454–464, 2008.
235.
XuN, PapagiannakopoulosT, PanG, ThomsonJA, and KosikKS. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell, 137: 647–658, 2009.
236.
YachieA, NiidaY, WadaT, IgarashiN, KanedaH, TomaT, OhtaK, KasaharaY, and KoizumiS. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Invest, 103: 129–135, 1999.
237.
YamaguchiY, SakaiE, SakamotoH, FumimotoR, FukumaY, NishishitaK, OkamotoK, and TsukubaT. Inhibitory effects of tert-butylhydroquinone on osteoclast differentiation via up-regulation of heme oxygenase-1 and down-regulation of HMGB1 release and NFATc1 expression. J Appl Toxicol [Epub ahead of print]; DOI: DOI:10.1002/jat.2827, 2012.
238.
YeomKH, LeeY, HanJ, SuhMR, and KimVN. Characterization of DGCR8/Pasha, the essential cofactor for Drosha in primary miRNA processing. Nucleic Acids Res, 34: 4622–4629, 2006.
239.
YoderMC. Endothelial progenitor cell: a blood cell by many other names may serve similar functions. J Mol Med (Berl), 91: 285–295, 2013.
240.
YoonJS, LeeHJ, ChaeMK, LeeSY, and LeeEJ. Cigarette-smoke-extract-induced adipogenesis in Graves' orbital fibroblasts is inhibited by quercetin via reduction in oxidative stress. J Endocrinol, 216, 145–165, 2013.
241.
YounceC and KolattukudyP. MCP-1 induced protein promotes adipogenesis via oxidative stress, endoplasmic reticulum stress and autophagy. Cell Physiol Biochem, 30: 307–320, 2012.
242.
ZarjouA, JeneyV, ArosioP, PoliM, Antal-SzalmasP, AgarwalA, BallaG, and BallaJ. Ferritin prevents calcification and osteoblastic differentiation of vascular smooth muscle cells. J Am Soc Nephrol, 20: 1254–1263, 2009.
243.
ZarjouA, KimJ, TraylorAM, SandersPW, BallaJ, AgarwalA, and CurtisLM. Paracrine effects of mesenchymal stem cells in cisplatin-induced renal injury require heme oxygenase-1. Am J Physiol Renal Physiol, 300: F254–F262, 2011.
244.
ZenclussenAC, SollwedelA, BertojaAZ, GerlofK, ZenclussenML, WoiciechowskyC, and VolkHD. Heme oxygenase as a therapeutic target in immunological pregnancy complications. Int Immunopharmacol, 5: 41–51, 2005.
245.
ZenclussenML, AnegonI, BertojaAZ, ChauveauC, VogtK, GerlofK, SollwedelA, VolkHD, RitterT, and ZenclussenAC. Over-expression of heme oxygenase-1 by adenoviral gene transfer improves pregnancy outcome in a murine model of abortion. J Reprod Immunol, 69: 35–52, 2006.
246.
ZengB, ChenH, ZhuC, RenX, LinG, and CaoF. Effects of combined mesenchymal stem cells and heme oxygenase-1 therapy on cardiac performance. Eur J Cardiothorac Surg, 34: 850–856, 2008.
247.
ZhangZ, WangQ, MaJ, YiX, ZhuY, XiX, FengY, and JinZ. Reactive oxygen species regulate FSH-induced expression of vascular endothelial growth factor via Nrf2 and HIF1alpha signaling in human epithelial ovarian cancer. Oncol Rep, 29: 1429–1434, 2013.
ZhaoH, KalotaA, JinS, and GewirtzAM. The c-myb proto-oncogene and microRNA-15a comprise an active autoregulatory feedback loop in human hematopoietic cells. Blood, 113: 505–516, 2009.
250.
ZhaoH, WongRJ, DoyleTC, NayakN, VremanHJ, ContagCH, and StevensonDK. Regulation of maternal and fetal hemodynamics by heme oxygenase in mice. Biol Reprod, 78: 744–751, 2008.
251.
ZhaoH, WongRJ, KalishFS, NayakNR, and StevensonDK. Effect of heme oxygenase-1 deficiency on placental development. Placenta, 30: 861–868, 2009.
252.
ZhaoQ, WangX, LiuY, HeA, and JiaR. NFATc1: functions in osteoclasts. Int J Biochem Cell Biol, 42: 576–579, 2010.
253.
ZhouH, RamiyaVK, and VisnerGA. Bone marrow stem cells as a vehicle for delivery of heme oxygenase-1 gene. Stem Cells Dev, 15: 79–86, 2006.
254.
ZhouZ, HanJY, XiCX, XieJX, FengX, WangCY, MeiL, and XiongWC. HMGB1 regulates RANKL-induced osteoclastogenesis in a manner dependent on RAGE. J Bone Miner Res, 23: 1084–1096, 2008.
255.
ZhuW, Boachie-AdjeiO, RawlinsBA, FrenkelB, BoskeyAL, IvashkivLB, and BlobelCP. A novel regulatory role for stromal-derived factor-1 signaling in bone morphogenic protein-2 osteogenic differentiation of mesenchymal C2C12 cells. J Biol Chem, 282: 18676–18685, 2007.
256.
ZwerinaJ, TzimaS, HayerS, RedlichK, HoffmannO, Hanslik-SchnabelB, SmolenJS, KolliasG, and SchettG. Heme oxygenase 1 (HO-1) regulates osteoclastogenesis and bone resorption. Faseb J, 19: 2011–2013, 2005.
