Functional states of resident vascular stem cells and vascular remodeling

doi:10.1007/s11515-015-1375-x

Front. Biol.

2015, Vol. 10

Issue (5) : 387-397 https://doi.org/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 Cui^1,^*(

)

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 Author(s): 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.

URL:

https://academic.hep.com.cn/fib/EN/10.1007/s11515-015-1375-x
https://academic.hep.com.cn/fib/EN/Y2015/V10/I5/387

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 CD31⁻CD45⁻ 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.

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