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Frontiers in Biology

Front. Biol.    2015, Vol. 10 Issue (5) : 387-397     DOI: 10.1007/s11515-015-1375-x
REVIEW |
Functional states of resident vascular stem cells and vascular remodeling
Desiree F. Leach1,Mitzi Nagarkatti2,Prakash Nagarkatti2,Taixing Cui1,*()
1. Department of Cell Biology and Anatomy, University of South Carolina School of Medicine, Columbia, SC 29209, USA
2. Department of Pathology, Microbiology and Immunology, University of South Carolina School of Medicine, Columbia, SC 29209, USA
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Abstract

Recent evidence indicates that different types of vascular stem cells (VSCs) reside within the mural layers of arteries and veins. The precise identities of these resident VSCs are still unclear; generally, postnatal vasculature contains multilineage stem cells and vascular cell lineage-specific progenitor/stem cells which may participate in both vascular repair and lesion formation. However, the underlying mechanism remains poorly understood. In this review, we summarize the potential molecular mechanisms, which may control the quiescence and activation of resident VSCs and highlight a notion that the differential states of resident VSCs are directly linked to vascular repair or lesion formation.

Keywords vascular stem cell      quiescence      activation      remodeling     
Corresponding Authors: Taixing Cui   
Just Accepted Date: 22 October 2015   Online First Date: 23 October 2015    Issue Date: 30 October 2015
 Cite this article:   
Taixing Cui,Desiree F. Leach,Mitzi Nagarkatti, et al. Functional states of resident vascular stem cells and vascular remodeling[J]. Front. Biol., 2015, 10(5): 387-397.
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http://journal.hep.com.cn/fib/EN/10.1007/s11515-015-1375-x
http://journal.hep.com.cn/fib/EN/Y2015/V10/I5/387
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Taixing Cui
Desiree F. Leach
Mitzi Nagarkatti
Prakash Nagarkatti
Year Authors Source/species Location Population described Isolation method Progenitor cell differentiation potential Cell marker expression summary Summary
2001 Alessandri et al. Human embryonic aorta rings Adventitia EPCs Immunoselection of fresh digests ECs CD31+ /CD31 CD31+/CD31 cells were capable of differentiating into ECs and forming capillary-like structures.
2004 Hu et al. Mouse thoracic aorta of ApoE−/− mice Adventitia Adventitial Sca-1+ progenitors Immunoselection of cultered tisue explant SMCs Sca-1+, c-kit+ /Lin Sca-1+ cells added to adventitial side of vein grafts in ApoE−/− mice, migration to intima observed.
2005 Covas et al. Human saphenous vein-internal surface Intima MSCs Culture of inner surface of veins Osteogenic, chondrogenic, adipogenic CD13+, CD29+, CD44+, CD54+, CD90+, HLA class+, HLA-DR Human vein wall contains mesenchymal cells with marker profile and differentiation potential similar to other MSC sources such as bone marrow and umbilical vein.
2005 Ingram et al. Human HUVEC/HAEC Intima EPCs Culture of HUVEC/HAEC ECs CD31+, CD141+, CD105+, CD145+, DCD144+, vWF+, Flk-1+ EPCs isolated from HUVEC/HAEC had proliferative and clonogenic potential similar to blood derived EPC.
2005 Howson et al. Rat Aorta Mixed tissue source PPCs Immunoselection of fresh digests Pericyte CD34/Tie-2, NG2, nestin, PDGFR Non-EC mesenchymal are capable of pericyte differentiation.
2006 Sainz et al. Mouse aorta Media SP cells Immunoselection of fresh digests ECs, SMCs Sca-1+, c-kit (−low/) Lin- CD34 (−/low) Media-derived SP cells were capable of differentiating into SMCs and ECs in response to PDGF/TGFB and VEGF, respectively.
2006 Zengin et al. Human arteries and veins Media-adventitia MPCs Arterial ring assays ECs, hematopoietic and immune cells CD34+, CD31, VEGFR2+, Tie-2 Vasculogenic zone between the media adventitia contain vascular wall progenitor cells. CD34+/CD31 were capable of forming capillary like structures.
2007 Pasquinelli et al. Human thoracic aorta Media-adventitia MSCs Culture of whole arterial wall digests ECs CD34+ or c-kit+ Isolated cells from total vessel wall expressed mesenchymal markers (CD44+, CD90+, CD105+ ) and stem cell markers (Oct4, c-kit, BCRP-1, interleukin-6) upon culture. MSCs displayed chondrogenic, adipogenic and leiomyogenic but less osteogenic potential, and formed capillary-like tubes, in vitro.
2007 Torsney et al. Human aorta and mammary arteries Atherosclerotic lesion/adventitia VPCs N/A. Immunostaining of neointimal lesion and adjacent aorta were conducted N/A CD34, c-kit, Sca-1 Progenitors identified within neointimal lesions and adventitia of human atherosclerotic vessels contained variable expression of CD34, Sca-1, c-kit and VEGFR2 markers, but no CD133 expression.
2007 Invernici et al. Human fetal aorta Adventitia VPCs Immunoselection of fresh digests ECs, mural cells, and myocytes CD34+, CD133+, VEGFR2+, and desmin VPCs formed by undifferentiated mesenchymal cells express endothelial and myogenic markers. VPCs can differentiate into ECs, mural cells or myocytes. VPCs can form 3D-cord-like vascular structures, in vivo. VPCs limproved neovascularization and muscular regeneration in a limb ischemic mouse model
2008 Passman et al. Mouse embryonic and adult arteries Adventitia Adventitial Sca-1+ progenitors Immunoselection of fresh digests SMCs Sca-1+ Cells at media-adventitia interface have an Shh signaling domain. In Shh−/− mice adventitial Sca-1 cells were reduced. Sca-1+ cells differentiated into SMCs.
2008 Hoshino et al. Human pulmonary artery Adventitia MSCs Culture of adventitial fibroblasts Osteogenic, adipogenic, and leiomyogenic Vimentin, collagen I, CD29, CD44, and CD105 Cultured vascular adventitial fibroblasts contain MSCs wich have adiopgenic and osteogenic potential.
2009 Liu et al. Human blood and transplant atherosclerotic vessels Intima EOC Culture of human mononuclear cells ECs ECs: eNOS, Tie-2, CD31, VECAD; Myeloid: CD14, CD68 Blood EOC outgrowths and ECs in neovessels of chimeric sex mismatched cardiac transplant atherosclerotic vessels express myeloid markers.
2009 Bearzi et al. Human coronary arteries and capillaries Intima, media, and adventitia VPCs Immunoselection of fresh digests ECs, SMCs and angiogenic VEGFR2+, c-kit+ VPCs, that were VEGFR2+ and c-kit+, had clonal and self-renewal capacity, and could differentiate toward EC and SMCs. VPCs also improved perfusion and generated new vessels in canine model of coronary stenosis.
2010 Pasquinelli et al. Human arteries Media-adventitia MSCs Culture of whole arterial wall digests Adipogenic, chondrogenic, leiomyogenic Oct-4, Stro-1, Sca-1, Notch-1, Mesenchymal markers (CD44, CD90, CD105, CD73, CD29, and CD166) Oct-4, Stro-1, Sca-1, Notch-1 found in vasculogenic niche. Total vessel wall isolated showed expression of stem (Stro-1, otch-1, Oct-4) and MSC lineages (CD44, CD90, CD105, CD73, CD29 and CD166).
2010 Campagnolo et al. Human saphenous vein Mixed tissue source SVPs Immunoselection of fresh digests of total vessel wall Pericyte CD34, vimentin, desmin, NG2, PDGFRb, CD44, CD90, CD105, CD29, CD13, CD59, and CD73, Sox2 Cell isolates from total vessel wall contain CD34+ /CD31 cells, which upon culture, express pericyte/mesenchymal markers. CD34+/CD31 cells could integrate into vascular networks in vitro and in vivo.
2011 Klein et al. Adult human arterial Adventitia MPSCs (i.e. MVSCs) Immunoselection of fresh digests SMCs CD44+, CD73+, CD90, CD45, CD34 Mesenchymal stem cell can function as vasculogenic cells.
2012 Tsai et al. Mouse thoracic aorta Adventitia Adventitial Sca-1+ progenitors Immunoselection of cultered tisue explant ECs, SMCs Sca-1+ Sca-1+ were able to differentiate into ECs and SMCs in response to VEGF or PDGF-BB stimulation, in vitro. In vivo, local application of VEGF to the adventitial side of the decellularized vessel increased re-endothelialization and reduced neointimal formation.
2012 Tang et al. Mouse, rat carotid arteries, and human vessels Media MVSCs Immunoselection of fresh digests and tissue explant method SMCs, adipogenic, osteogenic, and chondrogenic, and neurogenic SM-MHC-, Sox17, Sox10 S100β, NFM MVSCs were small, migratory and proliferative SM-MHC cells, that had clonal and self-renewal capacity and differentiated into mesodermal and etodermal lineages, including SMCs. MVSCs were responsible for neointimal formation in endothelial denudation model.
2012 Fang et al. Human fetal aorta Mixed tissue source VESCs Immunoselection of fresh digests ECs, SMCs, osteogenic and adipogenic Lin, CD31+, CD105+, Sca-1+, c-kit+ VESCs are clonal and have long-term self- renewal capacity. A single VESC can generate functional blood vessels, in vivo.
2012 Naito et al. Mouse hindlimb vasculature and other tissues Intima SP ECs Immunoselection of fresh digests Angiogenic Hoechst 33342/CD31+ /CD45 SP CD31CD45 Ecs were Sca-1+, VE-Cadh+, Flk-1+, CD133+, and CD34lo. They had greater clonogenic and angiogenic capacity than main population ECs and formed functional vessels in vivo.
2013 Chen et al. Mouse thoracic aorta Adventitia Adventitial Sca-1+ progenitors Immunoselection of vein graft explant SMCs, adipogenic, osteogenic, and chondrogenic Sca-1+ Sca-1+ cells reside in close proximity to the vasa vasorum during pathological conditions of vein grafts. Adventitial Sca-1+ progenitor cells can migrate across the vessel wall in response to SDF-1 for subsequent SMC differentiation, a process mediated by matrix protein/integrin interactions.
2013 Wong et al. Mouse thoracic aorta Adventitia Adventitial Sca-1+ progenitors Immunoselection of cultered tisue explant SMCs Sca-1+, Lin Sirolimus-induced progenitor cell migration and differentiation into SMC via CXCR4 and epidermal growth factor receptor/extracellular signal–regulated kinase/β-catenin signal pathways, thus implicating a novel mechanism of restenosis formation after sirolimus-eluting stent treatment.
2015 Song et al. Rat thoracic aorta Media RASMCs (i.e. MVSCs) Immunoselection of fresh digests SMCs, adipogenic, chondrogenic, and osteogenic NFM, Sox10 and S100β Traditionally cultured RASMCs probably result from the SMC differentiation of MVSCs. ROS is a negative regulator of MVSC differentiation into SMCs. Pla2g7 is a critical suppressor of MVSC differentiation into synthetic SMCs in vitro.
Tab.1  Historical findings of adult resident VSCs found in different compartments of the vessel wall
Fig.1  Diverse origin of adult resident VSCs in different compartments of the blood vessel. Distinct populations of vascular progenitor cells have been identified in the layers of the blood vessel. SMC indicates smooth muscle cell; MVSC, multipotent vascular stem cell; MPSC, multipotent stem cells; MSC, mesenchymal stromal/ stem cell; EPC, endothelial progenitor cell; SP EC, side population endothelial cell; MPC, macrophage precursor cell.
Fig.2  Adult VSC quiescence and activation. Adult VSCs at a quiescent state maintain their self-renewal and mature progenitor differentiation, which are required for vascular homeostasis, repair or regeneration. In response to injury, quiescent adult VSCs may be transformed into active VSCs, which are also precursors for mature progenitor cells for vascular repair. However, loss of the quiescence due to either dysregulated intrinsic or extrinsic signaling results in the abnormal activation and reprogramming of VSCs thereby leading to generation of premature progenitor cells and subsequent multiple lineage differentiation. This differentiation mostly likely produces various types of premature cells, such as synthetic SMCs, dysfunctional ECs, adipocytes, osteoblasts, and chondrocytes, contributing to maladaptive vascular remodeling and eventually causing vascular disease.
CYLDCylindromatosis
FoxOForkhead box O
ATMAtaxia telangiectasia mutated
WntWingless-type MMTV
TRAF2TNF receptor-associated factor 2
RhoRhodamine
PARPartition protein
SSEA-1Stage-specific embryonic antigen
CNN1Calponin 1
SM-MHCSmooth muscle myosin heavy chain
αSMAα smooth muscle actin
ApoEApolipoprotein E
SDF-1Stromal cell derived factor-1
HUVECHuman umbilical vein endothelial cells
HAECHuman aortic endothelial cells
SPSide population
BMPBone morphogenic protein
PDGFPlatelet-derived growth factor
PDGFRβPlatelet derived growth factor receptor β
TGFBTransforming growth factor beta
VEGFVascular endothelial growth factor
VEGFR2Vascular endothelial growth factor receptor 2
ShhSonic hedgehog
CXCR4C-X-C Chemokine receptor type 4
Pla2g7Phospholipase A2, group VII (platelet-activating factor acetylhydrolase, plasma)
Oct-4Octamer-binding transcription factor 4
BCRP-1Breakpoint Cluster Region Pseudogene 1
Flk-1Fetal liver kinase 1
ROSReactive oxygen species
CDK8Cyclin-dependent kinase 8
ECMExtracellular matrix
Sca-1Stem cell antigen-1
Tab.1  
1 Adler  A S, McCleland  M L, Truong  T, Lau  S, Modrusan  Z, Soukup  T M, Roose-Girma  M, Blackwood  E M, Firestein  R (2012). CDK8 maintains tumor dedifferentiation and embryonic stem cell pluripotency. Cancer Res, 72(8): 2129–2139
doi: 10.1158/0008-5472.CAN-11-3886 pmid: 22345154
2 Alessandri  G, Girelli  M, Taccagni  G, Colombo  A, Nicosia  R, Caruso  A, Baronio  M, Pagano  S, Cova  L, Parati  E (2001). Human vasculogenesis ex vivo: embryonal aorta as a tool for isolation of endothelial cell progenitors. Lab Invest, 81(6): 875–885
doi: 10.1038/labinvest.3780296 pmid: 11406648
3 Arai  F, Hirao  A, Ohmura  M, Sato  H, Matsuoka  S, Takubo  K, Ito  K, Koh  G Y, Suda  T (2004). Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell, 118(2): 149–161
doi: 10.1016/j.cell.2004.07.004 pmid: 15260986
4 Bautch  V L (2011). Stem cells and the vasculature. Nat Med, 17(11): 1437–1443
doi: 10.1038/nm.2539 pmid: 22064433
5 Bearzi  C, Leri  A, Lo Monaco  F, Rota  M, Gonzalez  A, Hosoda  T, Pepe  M, Qanud  K, Ojaimi  C, Bardelli  S, D’Amario  D, D’Alessandro  D A, Michler  R E, Dimmeler  S, Zeiher  A M, Urbanek  K, Hintze  T H, Kajstura  J, Anversa  P (2009). Identification of a coronary vascular progenitor cell in the human heart. Proc Natl Acad Sci USA, 106(37): 15885–15890
doi: 10.1073/pnas.0907622106 pmid: 19717420
6 Blank  U, Karlsson  G, Karlsson  S (2008). Signaling pathways governing stem-cell fate. Blood, 111(2): 492–503
doi: 10.1182/blood-2007-07-075168 pmid: 17914027
7 Campagnolo  P, Cesselli  D, Al Haj Zen  A, Beltrami  A P, Kränkel  N, Katare  R, Angelini  G, Emanueli  C, Madeddu  P (2010). Human adult vena saphena contains perivascular progenitor cells endowed with clonogenic and proangiogenic potential. Circulation, 121(15): 1735–1745
doi: 10.1161/CIRCULATIONAHA.109.899252 pmid: 20368523
8 Chen  Y, Wong  M M, Campagnolo  P, Simpson  R, Winkler  B, Margariti  A, Hu  Y, Xu  Q (2013). Adventitial stem cells in vein grafts display multilineage potential that contributes to neointimal formation. Arterioscler Thromb Vasc Biol, 33(8): 1844–1851
doi: 10.1161/ATVBAHA.113.300902 pmid: 23744989
9 Cheng  T, Rodrigues  N, Shen  H, Yang  Y, Dombkowski  D, Sykes  M, Scadden  D T (2000). Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science, 287(5459): 1804–1808
doi: 10.1126/science.287.5459.1804 pmid: 10710306
10 Covas  D T, Piccinato  C E, Orellana  M D, Siufi  J L, Silva  W A Jr, Proto-Siqueira  R, Rizzatti  E G, Neder  L, Silva  A R, Rocha  V, Zago  M A (2005). Mesenchymal stem cells can be obtained from the human saphena vein. Exp Cell Res, 309(2): 340–344
doi: 10.1016/j.yexcr.2005.06.005 pmid: 16018999
11 Fang  S, Wei  J, Pentinmikko  N, Leinonen  H, Salven  P (2012). Generation of functional blood vessels from a single c-kit+ adult vascular endothelial stem cell. PLoS Biol, 10(10): e1001407
doi: 10.1371/journal.pbio.1001407 pmid: 23091420
12 Florian  M C, Geiger  H (2010). Concise review: polarity in stem cells, disease, and aging. Stem Cells, 28(9): 1623–1629
doi: 10.1002/stem.481
13 Fukada  S, Uezumi  A, Ikemoto  M, Masuda  S, Segawa  M, Tanimura  N, Yamamoto  H, Miyagoe-Suzuki  Y, Takeda  S (2007). Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells, 25(10): 2448–2459
doi: 10.1634/stemcells.2007-0019 pmid: 17600112
14 Guevara  N V, Kim  H S, Antonova  E I, Chan  L (1999). The absence of p53 accelerates atherosclerosis by increasing cell proliferation in vivo. Nat Med, 5(3): 335–339
doi: 10.1038/6585 pmid: 10086392
15 Hoshino  A, Chiba  H, Nagai  K, Ishii  G, Ochiai  A (2008). Human vascular adventitial fibroblasts contain mesenchymal stem/progenitor cells. Biochem Biophys Res Commun, 368(2): 305–310
doi: 10.1016/j.bbrc.2008.01.090 pmid: 18230345
16 Howson  K M, Aplin  A C, Gelati  M, Alessandri  G, Parati  E A, Nicosia  R F (2005). The postnatal rat aorta contains pericyte progenitor cells that form spheroidal colonies in suspension culture. Am J Physiol Cell Physiol, 289(6): C1396–C1407
doi: 10.1152/ajpcell.00168.2005 pmid: 16079185
17 Hu  Y, Zhang  Z, Torsney  E, Afzal  A R, Davison  F, Metzler  B, Xu  Q (2004). Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest, 113(9): 1258–1265
doi: 10.1172/JCI19628 pmid: 15124016
18 Hüttmann  A, Liu  S L, Boyd  A W, Li  C L (2001). Functional heterogeneity within rhodamine123(lo) Hoechst33342(lo/sp) primitive hemopoietic stem cells revealed by pyronin Y. Exp Hematol, 29(9): 1109–1116
doi: 10.1016/S0301-472X(01)00684-1 pmid: 11532352
19 Ingram  D A, Mead  L E, Moore  D B, Woodard  W, Fenoglio  A, Yoder  M C (2005). Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood, 105(7): 2783–2786
doi: 10.1182/blood-2004-08-3057 pmid: 15585655
20 Invernici  G, Emanueli  C, Madeddu  P, Cristini  S, Gadau  S, Benetti  A, Ciusani  E, Stassi  G, Siragusa  M, Nicosia  R, Peschle  C, Fascio  U, Colombo  A, Rizzuti  T, Parati  E, Alessandri  G (2007). Human fetal aorta contains vascular progenitor cells capable of inducing vasculogenesis, angiogenesis, and myogenesis in vitro and in a murine model of peripheral ischemia. Am J Pathol, 170(6): 1879–1892
doi: 10.2353/ajpath.2007.060646 pmid: 17525256
21 Kawabe  J, Hasebe  N (2014). Role of the vasa vasorum and vascular resident stem cells in atherosclerosis. BioMed Res Int, 2014: 701571
doi: 10.1155/2014/701571 pmid: 24724094
22 Kippin  T E, Martens  D J, van der Kooy  D (2005). p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev, 19(6): 756–767
doi: 10.1101/gad.1272305 pmid: 15769947
23 Klein  D, Weisshardt  P, Kleff  V, Jastrow  H, Jakob  H G, Ergün  S (2011). Vascular wall-resident CD44+ multipotent stem cells give rise to pericytes and smooth muscle cells and contribute to new vessel maturation. PLoS ONE, 6(5): e20540
doi: 10.1371/journal.pone.0020540 pmid: 21637782
24 Li  L, Bhatia  R (2011). Stem cell quiescence. Clin Cancer Res, 17(15): 4936–4941
doi: 10.1158/1078-0432.CCR-10-1499 pmid: 21593194
25 Liu  C, Wang  S, Metharom  P, Caplice  N M (2009). Myeloid lineage of human endothelial outgrowth cells circulating in blood and vasculogenic endothelial-like cells in the diseased vessel wall. J Vasc Res, 46(6): 581–591
doi: 10.1159/000226226 pmid: 19571578
26 Liu  Y, Elf  S E, Miyata  Y, Sashida  G, Liu  Y, Huang  G, Di Giandomenico  S, Lee  J M, Deblasio  A, Menendez  S, Antipin  J, Reva  B, Koff  A, Nimer  S D (2009). p53 regulates hematopoietic stem cell quiescence. Cell Stem Cell, 4(1): 37–48
doi: 10.1016/j.stem.2008.11.006 pmid: 19128791
27 Majesky  M W, Dong  X R, Hoglund  V, Mahoney  W M Jr, Daum  G (2011). The adventitia: a dynamic interface containing resident progenitor cells. Arterioscler Thromb Vasc Biol, 31(7): 1530–1539
doi: 10.1161/ATVBAHA.110.221549 pmid: 21677296
28 Naito  H, Kidoya  H, Sakimoto  S, Wakabayashi  T, Takakura  N (2012). Identification and characterization of a resident vascular stem/progenitor cell population in preexisting blood vessels. EMBO J, 31(4): 842–855
doi: 10.1038/emboj.2011.465 pmid: 22179698
29 Orlandi  A, Bennett  M (2010). Progenitor cell-derived smooth muscle cells in vascular disease. Biochem Pharmacol, 79(12): 1706–1713
doi: 10.1016/j.bcp.2010.01.027 pmid: 20117099
30 Owens  G K, Kumar  M S, Wamhoff  B R (2004). Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev, 84(3): 767–801
doi: 10.1152/physrev.00041.2003 pmid: 15269336
31 Pasquinelli  G, Pacilli  A, Alviano  F, Foroni  L, Ricci  F, Valente  S, Orrico  C, Lanzoni  G, Buzzi  M, Luigi Tazzari  P, Pagliaro  P, Stella  A, Paolo Bagnara  G (2010). Multidistrict human mesenchymal vascular cells: pluripotency and stemness characteristics. Cytotherapy, 12(3): 275–287
doi: 10.3109/14653241003596679 pmid: 20230218
32 Pasquinelli  G, Tazzari  P L, Vaselli  C, Foroni  L, Buzzi  M, Storci  G, Alviano  F, Ricci  F, Bonafè  M, Orrico  C, Bagnara  G P, Stella  A, Conte  R (2007). Thoracic aortas from multiorgan donors are suitable for obtaining resident angiogenic mesenchymal stromal cells. Stem Cells, 25(7): 1627–1634
doi: 10.1634/stemcells.2006-0731 pmid: 17446560
33 Passman  J N, Dong  X R, Wu  S P, Maguire  C T, Hogan  K A, Bautch  V L, Majesky  M W (2008). A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells. Proc Natl Acad Sci USA, 105(27): 9349–9354
doi: 10.1073/pnas.0711382105 pmid: 18591670
34 Porter  D C, Farmaki  E, Altilia  S, Schools  G P, West  D K, Chen  M, Chang  B D, Puzyrev  A T, Lim  C, Rokow-Kittell  R, Friedhoff  L T, Papavassiliou  A G, Kalurupalle  S, Hurteau  G, Shi  J, Baran  P S, Gyorffy  B, Wentland  M P, Broude  E V, Kiaris  H, RRoninson  I B (2012). Cyclin-dependent kinase 8 mediates chemotherapy-induced tumor-promoting paracrine activities. Proc Natl Acad Sci USA, 109(34): 13799–13804
35 Psaltis  P J, Harbuzariu  A, Delacroix  S, Holroyd  E W, Simari  R D (2011). Resident vascular progenitor cells—diverse origins, phenotype, and function. J Cardiovasc Transl Res, 4(2): 161–176
doi: 10.1007/s12265-010-9248-9 pmid: 21116882
36 Psaltis  P J, Simari  R D (2015). Vascular wall progenitor cells in health and disease. Circ Res, 116(8): 1392–1412
doi: 10.1161/CIRCRESAHA.116.305368 pmid: 25858065
37 Ross  J J, Hong  Z, Willenbring  B, Zeng  L, Isenberg  B, Lee  E H, Reyes  M, Keirstead  S A, Weir  E K, Tranquillo  R T, Verfaillie  C M (2006). Cytokine-induced differentiation of multipotent adult progenitor cells into functional smooth muscle cells. J Clin Invest, 116(12): 3139–3149
doi: 10.1172/JCI28184 pmid: 17099777
38 Sainz  J, Al Haj Zen  A, Caligiuri  G, Demerens  C, Urbain  D, Lemitre  M, Lafont  A (2006). Isolation of “side population” progenitor cells from healthy arteries of adult mice. Arterioscler Thromb Vasc Biol, 26(2): 281–286
doi: 10.1161/01.ATV.0000197793.83391.91 pmid: 16306431
39 Song  H, Wang  H, Wu  W, Qi  L, Shao  L, Wang  F, Lai  Y, Leach  D, Mathis  B, Janicki  J S, Wang  X L, Tang  D, Cui  T (2015). Inhibitory role of reactive oxygen species in the differentiation of multipotent vascular stem cells into vascular smooth muscle cells in rats: a novel aspect of traditional culture of rat aortic smooth muscle cells. Cell Tissue Res, 362(1): 97–113
doi: 10.1007/s00441-015-2193-9 pmid: 26022334
40 Tang  Z, Wang  A, Yuan  F, Yan  Z, Liu  B, Chu  J S, Helms  J A, Li  S (2012). Differentiation of multipotent vascular stem cells contributes to vascular diseases. Nat Commun, 3: 875
doi: 10.1038/ncomms1867 pmid: 22673902
41 Tesio  M, Tang  Y, Müdder  K, Saini  M, von Paleske  L, Macintyre  E, Pasparakis  M, Waisman  A, Trumpp  A (2015). Hematopoietic stem cell quiescence and function are controlled by the CYLD-TRAF2-p38MAPK pathway. J Exp Med, 212(4): 525–538
doi: 10.1084/jem.20141438 pmid: 25824820
42 Tom  H, Cheung  T A R (2012). Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol, 29(6): 997–1003
43 Torsney  E, Mandal  K, Halliday  A, Jahangiri  M, Xu  Q (2007). Characterisation of progenitor cells in human atherosclerotic vessels. Atherosclerosis, 191(2): 259–264
doi: 10.1016/j.atherosclerosis.2006.05.033 pmid: 16787646
44 Torsney  E, Xu  Q (2011). Resident vascular progenitor cells. J Mol Cell Cardiol, 50(2): 304–311
doi: 10.1016/j.yjmcc.2010.09.006 pmid: 20850452
45 Tsai  T N, Kirton  J P, Campagnolo  P, Zhang  L, Xiao  Q, Zhang  Z, Wang  W, Hu  Y, Xu  Q (2012). Contribution of stem cells to neointimal formation of decellularized vessel grafts in a novel mouse model. Am J Pathol, 181(1): 362–373
doi: 10.1016/j.ajpath.2012.03.021 pmid: 22613026
46 Tsaousi  A, Williams  H, Lyon  C A, Taylor  V, Swain  A, Johnson  J L, George  S J (2011). Wnt4/β-catenin signaling induces VSMC proliferation and is associated with intimal thickening. Circ Res, 108(4): 427–436
doi: 10.1161/CIRCRESAHA.110.233999 pmid: 21193738
47 van Os  R, de Haan  G, Dykstra  B J (2009). Hematopoietic stem cell quiescence: yet another role for p53. Cell Stem Cell, 4(1): 7–8
doi: 10.1016/j.stem.2008.12.007 pmid: 19128788
48 Wabik  A, Jones  P H (2015). Switching roles: the functional plasticity of adult tissue stem cells. EMBO J, 34(9): 1164–1179
49 Wang  Y Z, Plane  J M, Jiang  P, Zhou  C J, Deng  W (2011). Concise review: Quiescent and active states of endogenous adult neural stem cells:  identification  and  characterization.  Stem  Cells,  29(6):  907–912
doi: 10.1002/stem.644 pmid: 21557389
50 Wong  M M, Winkler  B, Karamariti  E, Wang  X, Yu  B, Simpson  R, Chen  T, Margariti  A, Xu  Q (2013). Sirolimus stimulates vascular stem/progenitor cell migration and differentiation into smooth muscle cells via epidermal growth factor receptor/extracellular signal-regulated kinase/β-catenin signaling pathway. Arterioscler Thromb Vasc Biol, 33(10): 2397–2406
doi: 10.1161/ATVBAHA.113.301595 pmid: 23928863
51 Yoshihara  H, Arai  F, Hosokawa  K, Hagiwara  T, Takubo  K, Nakamura  Y, Gomei  Y, Iwasaki  H, Matsuoka  S, Miyamoto  K, Miyazaki  H, Takahashi  T, Suda  T (2007). Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell, 1(6): 685–697
doi: 10.1016/j.stem.2007.10.020 pmid: 18371409
52 Zengin  E, Chalajour  F, Gehling  U M, Ito  W D, Treede  H, Lauke  H, Weil  J, Reichenspurner  H, Kilic  N, Ergün  S (2006). Vascular wall resident progenitor cells: a source for postnatal vasculogenesis. Development, 133(8): 1543–1551
doi: 10.1242/dev.02315 pmid: 16524930
53 Zhang  J, Niu  C, Ye  L, Huang  H, He  X, Tong  W G, Ross  J, Haug  J, Johnson  T, Feng  J Q, Harris  S, Wiedemann  L M, Mishina  Y, Li  L (2003). Identification of the haematopoietic stem cell niche and control of the niche size. Nature, 425(6960): 836–841
doi: 10.1038/nature02041 pmid: 14574412
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