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Frontiers in Biology

Front. Biol.    2015, Vol. 10 Issue (5) : 387-397     DOI: 10.1007/s11515-015-1375-x
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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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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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.
FoxOForkhead box O
ATMAtaxia telangiectasia mutated
WntWingless-type MMTV
TRAF2TNF receptor-associated factor 2
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
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