Functional states of resident vascular stem cells and vascular remodeling
Received date: 24 Sep 2015
Accepted date: 30 Sep 2015
Published date: 30 Oct 2015
Copyright
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.
Key words: vascular stem cell; quiescence; activation; remodeling
Desiree F. Leach , Mitzi Nagarkatti , Prakash Nagarkatti , Taixing Cui . Functional states of resident vascular stem cells and vascular remodeling[J]. Frontiers in Biology, 2015 , 10(5) : 387 -397 . DOI: 10.1007/s11515-015-1375-x
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
|
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
|
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
|
4 |
Bautch V L (2011). Stem cells and the vasculature. Nat Med, 17(11): 1437–1443
|
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
|
6 |
Blank U, Karlsson G, Karlsson S (2008). Signaling pathways governing stem-cell fate. Blood, 111(2): 492–503
|
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
|
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
|
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
|
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
|
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
|
12 |
Florian M C, Geiger H (2010). Concise review: polarity in stem cells, disease, and aging. Stem Cells, 28(9): 1623–1629
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
21 |
Kawabe J, Hasebe N (2014). Role of the vasa vasorum and vascular resident stem cells in atherosclerosis. BioMed Res Int, 2014: 701571
|
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
|
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
|
24 |
Li L, Bhatia R (2011). Stem cell quiescence. Clin Cancer Res, 17(15): 4936–4941
|
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
|
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
|
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
|
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
|
29 |
Orlandi A, Bennett M (2010). Progenitor cell-derived smooth muscle cells in vascular disease. Biochem Pharmacol, 79(12): 1706–1713
|
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
|
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
|
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
|
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
|
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
|
36 |
Psaltis P J, Simari R D (2015). Vascular wall progenitor cells in health and disease. Circ Res, 116(8): 1392–1412
|
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
|
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
|
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
|
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
|
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
|
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
|
44 |
Torsney E, Xu Q (2011). Resident vascular progenitor cells. J Mol Cell Cardiol, 50(2): 304–311
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
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
|
/
〈 | 〉 |