Abstract
The fundamental contributions that blood vessels make toward organogenesis and tissue homeostasis are reflected by the considerable ramifications that loss of vascular wall integrity has on pre- and postnatal health. During both neovascularization and vessel wall remodeling after insult, the dynamic nature of vascular cell growth and replacement vitiates traditional impressions that blood vessels contain predominantly mature, terminally differentiated cell populations. Recent discoveries have verified the presence of diverse stem/progenitor cells for both vascular and non-vascular progeny within the mural layers of the vasculature. During embryogenesis, this encompasses the emergence of definitive hematopoietic stem cells and multipotent mesoangioblasts from the developing dorsal aorta. Ancestral cells have also been identified and isolated from mature, adult blood vessels, showing variable capacity for endothelial, smooth muscle, and mesenchymal differentiation. At present, the characterization of these different vascular wall progenitors remains somewhat rudimentary, but there is evidence for their constitutive residence within organized compartments in the vessel wall, most compellingly in the tunica adventitia. This review overviews the spectrum of resident stem/progenitor cells that have been documented in macro- and micro-vessels during developmental and adult life and considers the implications for a local, vascular wall stem cell niche(s) in the pathogenesis and treatment of cardiovascular and other diseases.
Similar content being viewed by others
References
Tavian, M., Zheng, B., Oberlin, E., Crisan, M., Sun, B., Huard, J., et al. (2005). The vascular wall as a source of stem cells. Annals of the New York Academy of Sciences, 1044, 41–50.
Carmeliet, P. (2003). Angiogenesis in health and disease. Natural Medicines, 9, 653–660.
Ross, R. (1993). The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature, 362, 801–809.
Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., et al. (1997). Isolation of putative progenitor endothelial cells for angiogenesis. Science, 275, 964–967.
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, 2783–2786.
Simper, D., Stalboerger, P. G., Panetta, C. J., Wang, S., & Caplice, N. M. (2002). Smooth muscle progenitor cells in human blood. Circulation, 106, 1199–1204.
Hu, Y., Zhang, Z., Torsney, E., Afzal, A. R., Davison, F., Metzler, B., et al. (2004). Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. Journal of Clinical Investigation, 113, 1258–1265.
Passman, J. N., Dong, X. R., Wu, S. P., Maguire, C. T., Hogan, K. A., Bautch, V. L., et al. (2008). A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells. Proceedings of the National Academy of Sciences of the United States of America, 105, 9349–9354.
Zengin, E., Chalajour, F., Gehling, U. M., Ito, W. D., Treede, H., Lauke, H., et al. (2006). Vascular wall resident progenitor cells: a source for postnatal vasculogenesis. Development, 133, 1543–1551.
Tintut, Y., Alfonso, Z., Saini, T., Radcliff, K., Watson, K., Bostrom, K., et al. (2003). Multilineage potential of cells from the artery wall. Circulation, 108, 2505–2510.
Sabin, F. R. (1917). Preliminary note on the differentiation of angioblasts and the method by which they produce blood-vessels, blood-plasma, and red blood-cells as seen in the living chick. The Anatomical Record, 13, 199–204.
Murray, P. D. F. (1932). The development in vitro of blood of early chick embryo. Proceedings of the Royal Society of London Biological Sciences, 111, 497–521.
Ferguson, J. E., 3rd, Kelley, R. W., & Patterson, C. (2005). Mechanisms of endothelial differentiation in embryonic vasculogenesis. Arteriosclerosis, Thrombosis, and Vascular Biology, 25, 2246–2254.
Schmidt, A., Brixius, K., & Bloch, W. (2007). Endothelial precursor cell migration during vasculogenesis. Circulation Research, 101, 125–136.
Bertrand, J. Y., Chi, N. C., Santoso, B., Teng, S., Stainier, D. Y., & Traver, D. (2010). Haematopoietic stem cells derive directly from aortic endothelium during development. Nature, 464, 108–111.
Kissa, K., & Herbomel, P. (2010). Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature, 464, 112–115.
Jaffredo, T., Gautier, R., Eichmann, A., & Dieterlen-Lievre, F. (1998). Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development, 125, 4575–4583.
Ciau-Uitz, A., Walmsley, M., & Patient, R. (2000). Distinct origins of adult and embryonic blood in Xenopus. Cell, 102, 787–796.
Medvinsky, A., & Dzierzak, E. (1996). Definitive hematopoiesis is autonomously initiated by the AGM region. Cell, 86, 897–906.
Zovein, A. C., Hofmann, J. J., Lynch, M., French, W. J., Turlo, K. A., Yang, Y., et al. (2008). Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell, 3, 625–636.
Chen, M. J., Yokomizo, T., Zeigler, B. M., Dzierzak, E., & Speck, N. A. (2009). Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature, 457, 887–891.
Boisset, J. C., van Cappellen, W., Andrieu-Soler, C., Galjart, N., Dzierzak, E., & Robin, C. (2010). In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature, 464, 116–120.
Dzierzak, E., & Speck, N. A. (2008). Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nature Immunology, 9, 129–136.
Morrison, S. J., & Spradling, A. C. (2008). Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell, 132, 598–611.
Vogeli, K. M., Jin, S. W., Martin, G. R., & Stainier, D. Y. (2006). A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature, 443, 337–339.
Eilken, H. M., Nishikawa, S., & Schroeder, T. (2009). Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature, 457, 896–900.
Choi, K., Kennedy, M., Kazarov, A., Papadimitriou, J. C., & Keller, G. (1998). A common precursor for hematopoietic and endothelial cells. Development, 125, 725–732.
Kennedy, M., D’Souza, S. L., Lynch-Kattman, M., Schwantz, S., & Keller, G. (2007). Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood, 109, 2679–2687.
Lacaud, G., Gore, L., Kennedy, M., Kouskoff, V., Kingsley, P., Hogan, C., et al. (2002). Runx1 is essential for hematopoietic commitment at the hemangioblast stage of development in vitro. Blood, 100, 458–466.
Robertson, S. M., Kennedy, M., Shannon, J. M., & Keller, G. (2000). A transitional stage in the commitment of mesoderm to hematopoiesis requiring the transcription factor SCL/tal-1. Development, 127, 2447–2459.
Fehling, H. J., Lacaud, G., Kubo, A., Kennedy, M., Robertson, S., Keller, G., et al. (2003). Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development, 130, 4217–4227.
Zambidis, E. T., Park, T. S., Yu, W., Tam, A., Levine, M., Yuan, X., et al. (2008). Expression of angiotensin-converting enzyme (CD143) identifies and regulates primitive hemangioblasts derived from human pluripotent stem cells. Blood, 112, 3601–3614.
Bailey, A. S., Jiang, S., Afentoulis, M., Baumann, C. I., Schroeder, D. A., Olson, S. B., et al. (2004). Transplanted adult hematopoietic stems cells differentiate into functional endothelial cells. Blood, 103, 13–19.
Niwa, A., Umeda, K., Chang, H., Saito, M., Okita, K., Takahashi, K., et al. (2009). Orderly hematopoietic development of induced pluripotent stem cells via Flk-1(+) hemoangiogenic progenitors. Journal of Cellular Physiology, 221, 367–377.
Cossu, G., & Bianco, P. (2003). Mesoangioblasts–vascular progenitors for extravascular mesodermal tissues. Current Opinion in Genetics & Development, 13, 537–542.
Minasi, M. G., Riminucci, M., De Angelis, L., Borello, U., Berarducci, B., Innocenzi, A., et al. (2002). The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development, 129, 2773–2783.
Le Lievre, C. S., & Le Douarin, N. M. (1975). Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. Journal of Embryology and Experimental Morphology, 34, 125–154.
Jiang, X., Rowitch, D. H., Soriano, P., McMahon, A. P., & Sucov, H. M. (2000). Fate of the mammalian cardiac neural crest. Development, 127, 1607–1616.
Wada, A. M., Willet, S. G., & Bader, D. (2003). Coronary vessel development: a unique form of vasculogenesis. Arteriosclerosis, Thrombosis, and Vascular Biology, 23, 2138–2145.
Hungerford, J. E., Owens, G. K., Argraves, W. S., & Little, C. D. (1996). Development of the aortic vessel wall as defined by vascular smooth muscle and extracellular matrix markers. Developmental Biology, 178, 375–392.
Shi, Q., Rafii, S., Wu, M. H., Wijelath, E. S., Yu, C., Ishida, A., et al. (1998). Evidence for circulating bone marrow-derived endothelial cells. Blood, 92, 362–367.
Kocher, A. A., Schuster, M. D., Szabolcs, M. J., Takuma, S., Burkhoff, D., Wang, J., et al. (2001). Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Natural Medicines, 7, 430–436.
Kawamoto, A., Gwon, H. C., Iwaguro, H., Yamaguchi, J. I., Uchida, S., Masuda, H., et al. (2001). Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation, 103, 634–637.
Losordo, D. W., Schatz, R. A., White, C. J., Udelson, J. E., Veereshwarayya, V., Durgin, M., et al. (2007). Intramyocardial transplantation of autologous CD34+ stem cells for intractable angina: a phase I/IIa double-blind, randomized controlled trial. Circulation, 115, 3165–3172.
Schwartz, S. M., & Benditt, E. P. (1977). Aortic endothelial cell replication. I. Effects of age and hypertension in the rat. Circulation Research, 41, 248–255.
Schwartz, S. M., & Benditt, E. P. (1976). Clustering of replicating cells in aortic endothelium. Proceedings of the National Academy of Sciences of the United States of America, 73, 651–653.
Nolan, D. J., Ciarrocchi, A., Mellick, A. S., Jaggi, J. S., Bambino, K., Gupta, S., et al. (2007). Bone marrow-derived endothelial progenitor cells are a major determinant of nascent tumor neovascularization. Genes & Development, 21, 1546–1558.
Asahara, T., Masuda, H., Takahashi, T., Kalka, C., Pastore, C., Silver, M., et al. (1999). Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circulation Research, 85, 221–228.
Yoon, C. H., Hur, J., Park, K. W., Kim, J. H., Lee, C. S., Oh, I. Y., et al. (2005). Synergistic neovascularization by mixed transplantation of early endothelial progenitor cells and late outgrowth endothelial cells: the role of angiogenic cytokines and matrix metalloproteinases. Circulation, 112, 1618–1627.
Werner, N., Junk, S., Laufs, U., Link, A., Walenta, K., Bohm, M., et al. (2003). Intravenous transfusion of endothelial progenitor cells reduces neointima formation after vascular injury. Circulation Research, 93, e17–e24.
Timmermans, F., Plum, J., Yoder, M. C., Ingram, D. A., Vandekerckhove, B., & Case, J. (2009). Endothelial progenitor cells: identity defined? Journal of Cellular and Molecular Medicine, 13, 87–102.
Gulati, R., Jevremovic, D., Peterson, T. E., Chatterjee, S., Shah, V., Vile, R. G., et al. (2003). Diverse origin and function of cells with endothelial phenotype obtained from adult human blood. Circulation Research, 93, 1023–1025.
Hill, J. M., Zalos, G., Halcox, J. P., Schenke, W. H., Waclawiw, M. A., Quyyumi, A. A., et al. (2003). Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. The New England Journal of Medicine, 348, 593–600.
Ingram, D. A., Mead, L. E., Tanaka, H., Meade, V., Fenoglio, A., Mortell, K., et al. (2004). Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood, 104, 2752–2760.
Peichev, M., Naiyer, A. J., Pereira, D., Zhu, Z., Lane, W. J., Williams, M., et al. (2000). Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood, 95, 952–958.
Chakroborty, D., Chowdhury, U. R., Sarkar, C., Baral, R., Dasgupta, P. S., & Basu, S. (2008). Dopamine regulates endothelial progenitor cell mobilization from mouse bone marrow in tumor vascularization. Journal of Clinical Investigation, 118, 1380–1389.
Case, J., Mead, L. E., Bessler, W. K., Prater, D., White, H. A., Saadatzadeh, M. R., et al. (2007). Human CD34+AC133+VEGFR-2+ cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. Experimental Hematology, 35, 1109–1118.
Yoder, M. C., Mead, L. E., Prater, D., Krier, T. R., Mroueh, K. N., Li, F., et al. (2007). Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood, 109, 1801–1809.
Rohde, E., Bartmann, C., Schallmoser, K., Reinisch, A., Lanzer, G., Linkesch, W., et al. (2007). Immune cells mimic the morphology of endothelial progenitor colonies in vitro. Stem Cells, 25, 1746–1752.
Rehman, J., Li, J., Orschell, C. M., & March, K. L. (2003). Peripheral blood “endothelial progenitor cells” are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation, 107, 1164–1169.
Guven, H., Shepherd, R. M., Bach, R. G., Capoccia, B. J., & Link, D. C. (2006). The number of endothelial progenitor cell colonies in the blood is increased in patients with angiographically significant coronary artery disease. Journal of the American College of Cardiology, 48, 1579–1587.
Hu, Y., Davison, F., Zhang, Z., & Xu, Q. (2003). Endothelial replacement and angiogenesis in arteriosclerotic lesions of allografts are contributed by circulating progenitor cells. Circulation, 108, 3122–3127.
Perry, T. E., Song, M., Despres, D. J., Kim, S. M., San, H., Yu, Z. X., et al. (2009). Bone marrow-derived cells do not repair endothelium in a mouse model of chronic endothelial cell dysfunction. Cardiovascular Research, 84, 317–325.
Hillebrands, J. L., Klatter, F. A., van Dijk, W. D., & Rozing, J. (2002). Bone marrow does not contribute substantially to endothelial-cell replacement in transplant arteriosclerosis. Natural Medicines, 8, 194–195.
Gothert, J. R., Gustin, S. E., van Eekelen, J. A., Schmidt, U., Hall, M. A., Jane, S. M., et al. (2004). Genetically tagging endothelial cells in vivo: bone marrow-derived cells do not contribute to tumor endothelium. Blood, 104, 1769–1777.
Majka, S. M., Jackson, K. A., Kienstra, K. A., Majesky, M. W., Goodell, M. A., & Hirschi, K. K. (2003). Distinct progenitor populations in skeletal muscle are bone marrow derived and exhibit different cell fates during vascular regeneration. Journal of Clinical Investigation, 111, 71–79.
Grenier, G., Scime, A., Le Grand, F., Asakura, A., Perez-Iratxeta, C., Andrade-Navarro, M. A., et al. (2007). Resident endothelial precursors in muscle, adipose, and dermis contribute to postnatal vasculogenesis. Stem Cells, 25, 3101–3110.
Aicher, A., Rentsch, M., Sasaki, K., Ellwart, J. W., Fandrich, F., Siebert, R., et al. (2007). Nonbone marrow-derived circulating progenitor cells contribute to postnatal neovascularization following tissue ischemia. Circulation Research, 100, 581–589.
Bearzi, C., Leri, A., Lo Monaco, F., Rota, M., Gonzalez, A., Hosoda, T., et al. (2009). Identification of a coronary vascular progenitor cell in the human heart. Proceedings of the National Academy of Sciences of the United States of America, 106, 15885–15890.
Alessandri, G., Girelli, M., Taccagni, G., Colombo, A., Nicosia, R., Caruso, A., et al. (2001). Human vasculogenesis ex vivo: embryonal aorta as a tool for isolation of endothelial cell progenitors. Laboratory Investigation, 81, 875–885.
Invernici, G., Emanueli, C., Madeddu, P., Cristini, S., Gadau, S., Benetti, A., et al. (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. The American Journal of Pathology, 170, 1879–1892.
Sata, M., Saiura, A., Kunisato, A., Tojo, A., Okada, S., Tokuhisa, T., et al. (2002). Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Natural Medicines, 8, 403–409.
Kumar, A. H., Metharom, P., Schmeckpeper, J., Weiss, S., Martin, K., & Caplice, N. M. (2010). Bone marrow-derived CX3CR1 progenitors contribute to neointimal smooth muscle cells via fractalkine CX3CR1 interaction. The FASEB Journal, 24, 81–92.
Sainz, J., Al Haj Zen, A., Caligiuri, G., Demerens, C., Urbain, D., Lemitre, M., et al. (2006). Isolation of “side population” progenitor cells from healthy arteries of adult mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 26, 281–286.
Li, G., Chen, S. J., Oparil, S., Chen, Y. F., & Thompson, J. A. (2000). Direct in vivo evidence demonstrating neointimal migration of adventitial fibroblasts after balloon injury of rat carotid arteries. Circulation, 101, 1362–1365.
Frid, M. G., Kale, V. A., & Stenmark, K. R. (2002). Mature vascular endothelium can give rise to smooth muscle cells via endothelial-mesenchymal transdifferentiation: in vitro analysis. Circulation Research, 90, 1189–1196.
Shimizu, K., Sugiyama, S., Aikawa, M., Fukumoto, Y., Rabkin, E., Libby, P., et al. (2001). Host bone-marrow cells are a source of donor intimal smooth- muscle-like cells in murine aortic transplant arteriopathy. Natural Medicines, 7, 738–741.
Hu, Y., Davison, F., Ludewig, B., Erdel, M., Mayr, M., Url, M., et al. (2002). Smooth muscle cells in transplant atherosclerotic lesions are originated from recipients, but not bone marrow progenitor cells. Circulation, 106, 1834–1839.
Caplice, N. M., Bunch, T. J., Stalboerger, P. G., Wang, S., Simper, D., Miller, D. V., et al. (2003). Smooth muscle cells in human coronary atherosclerosis can originate from cells administered at marrow transplantation. Proceedings of the National Academy of Sciences of the United States of America, 100, 4754–4759.
Deb, A., Skelding, K. A., Wang, S., Reeder, M., Simper, D., & Caplice, N. M. (2004). Integrin profile and in vivo homing of human smooth muscle progenitor cells. Circulation, 110, 2673–2677.
Sugiyama, S., Kugiyama, K., Nakamura, S., Kataoka, K., Aikawa, M., Shimizu, K., et al. (2006). Characterization of smooth muscle-like cells in circulating human peripheral blood. Atherosclerosis, 187, 351–362.
Bentzon, J. F., Sondergaard, C. S., Kassem, M., & Falk, E. (2007). Smooth muscle cells healing atherosclerotic plaque disruptions are of local, not blood, origin in apolipoprotein E knockout mice. Circulation, 116, 2053–2061.
Rodriguez-Menocal, L., St-Pierre, M., Wei, Y., Khan, S., Mateu, D., Calfa, M., et al. (2009). The origin of post-injury neointimal cells in the rat balloon injury model. Cardiovascular Research, 81, 46–53.
De Leon, H., Ollerenshaw, J. D., Griendling, K. K., & Wilcox, J. N. (2001). Adventitial cells do not contribute to neointimal mass after balloon angioplasty of the rat common carotid artery. Circulation, 104, 1591–1593.
Pasquinelli, G., Tazzari, P. L., Vaselli, C., Foroni, L., Buzzi, M., Storci, G., et al. (2007). Thoracic aortas from multiorgan donors are suitable for obtaining resident angiogenic mesenchymal stromal cells. Stem Cells, 25, 1627–1634.
Campagnolo, P., Cesselli, D., Al Haj Zen, A., Beltrami, A. P., Krankel, N., Katare, R., et al. (2010). Human adult vena saphena contains perivascular progenitor cells endowed with clonogenic and proangiogenic potential. Circulation, 121, 1735–1745.
Torsney, E., Mandal, K., Halliday, A., Jahangiri, M., & Xu, Q. (2007). Characterisation of progenitor cells in human atherosclerotic vessels. Atherosclerosis, 191, 259–264.
Majesky, M. W. (2007). Developmental basis of vascular smooth muscle diversity. Arteriosclerosis, Thrombosis, and Vascular Biology, 27, 1248–1258.
Collett, G. D., & Canfield, A. E. (2005). Angiogenesis and pericytes in the initiation of ectopic calcification. Circulation Research, 96, 930–938.
Psaltis, P. J., Zannettino, A. C., Worthley, S. G., & Gronthos, S. (2008). Concise review: mesenchymal stromal cells: potential for cardiovascular repair. Stem Cells, 26, 2201–2210.
Shi, S., & Gronthos, S. (2003). Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. Journal of Bone and Mineral Research, 18, 696–704.
Dellavalle, A., Sampaolesi, M., Tonlorenzi, R., Tagliafico, E., Sacchetti, B., Perani, L., et al. (2007). Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nature Cell Biology, 9, 255–267.
Sacchetti, B., Funari, A., Michienzi, S., Di Cesare, S., Piersanti, S., Saggio, I., et al. (2007). Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell, 131, 324–336.
Schwab, K. E., & Gargett, C. E. (2007). Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Human Reproduction, 22, 2903–2911.
Crisan, M., Yap, S., Casteilla, L., Chen, C. W., Corselli, M., Park, T. S., et al. (2008). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell, 3, 301–313.
Zannettino, A. C., Paton, S., Arthur, A., Khor, F., Itescu, S., Gimble, J. M., et al. (2008). Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. Journal of Cellular Physiology, 214, 413–421.
Peault, B., Rudnicki, M., Torrente, Y., Cossu, G., Tremblay, J. P., Partridge, T., et al. (2007). Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Molecular Therapy, 15, 867–877.
Dore-Duffy, P., Katychev, A., Wang, X., & Van Buren, E. (2006). CNS microvascular pericytes exhibit multipotential stem cell activity. Journal of Cerebral Blood Flow and Metabolism, 26, 613–624.
Caplan, A. I., & Dennis, J. E. (2006). Mesenchymal stem cells as trophic mediators. Journal of Cellular Biochemistry, 98, 1076–1084.
Traktuev, D. O., Merfeld-Clauss, S., Li, J., Kolonin, M., Arap, W., Pasqualini, R., et al. (2008). A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circulation Research, 102, 77–85.
da Silva, M. L., Caplan, A. I., & Nardi, N. B. (2008). In search of the in vivo identity of mesenchymal stem cells. Stem Cells, 26, 2287–2299.
Andreeva, E. R., Pugach, I. M., Gordon, D., & Orekhov, A. N. (1998). Continuous subendothelial network formed by pericyte-like cells in human vascular bed. Tissue & Cell, 30, 127–135.
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. American Journal of Physiology. Cell Physiology, 289, C1396–C1407.
Covas, D. T., Piccinato, C. E., Orellana, M. D., Siufi, J. L., Silva, W. A., Jr., Proto-Siqueira, R., et al. (2005). Mesenchymal stem cells can be obtained from the human saphena vein. Experimental Cell Research, 309, 340–344.
Hoshino, A., Chiba, H., Nagai, K., Ishii, G., & Ochiai, A. (2008). Human vascular adventitial fibroblasts contain mesenchymal stem/progenitor cells. Biochemical and Biophysical Research Communications, 368, 305–310.
Pasquinelli, G., Pacilli, A., Alviano, F., Foroni, L., Ricci, F., Valente, S., et al. (2010). Multidistrict human mesenchymal vascular cells: pluripotency and stemness characteristics. Cytotherapy, 12, 275–287.
Shao, J. S., Cai, J., & Towler, D. A. (2006). Molecular mechanisms of vascular calcification: lessons learned from the aorta. Arteriosclerosis, Thrombosis, and Vascular Biology, 26, 1423–1430.
Arras, M., Ito, W. D., Scholz, D., Winkler, B., Schaper, J., & Schaper, W. (1998). Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. Journal of Clinical Investigation, 101, 40–50.
Soehnlein, O., & Weber, C. (2009). Myeloid cells in atherosclerosis: initiators and decision shapers. Seminars in Immunopathology, 31, 35–47.
Lessner, S. M., Prado, H. L., Waller, E. K., & Galis, Z. S. (2002). Atherosclerotic lesions grow through recruitment and proliferation of circulating monocytes in a murine model. The American Journal of Pathology, 160, 2145–2155.
Khmelewski, E., Becker, A., Meinertz, T., & Ito, W. D. (2004). Tissue resident cells play a dominant role in arteriogenesis and concomitant macrophage accumulation. Circulation Research, 95, E56–E64.
Miyata, K., Shimokawa, H., Kandabashi, T., Higo, T., Morishige, K., Eto, Y., et al. (2000). Rho-kinase is involved in macrophage-mediated formation of coronary vascular lesions in pigs in vivo. Arteriosclerosis, Thrombosis, and Vascular Biology, 20, 2351–2358.
Bot, I., de Jager, S. C., Bot, M., van Heiningen, S. H., de Groot, P., Veldhuizen, R. W., et al. (2010). The neuropeptide substance P mediates adventitial mast cell activation and induces intraplaque hemorrhage in advanced atherosclerosis. Circulation Research, 106, 89–92.
Massberg, S., Schaerli, P., Knezevic-Maramica, I., Kollnberger, M., Tubo, N., Moseman, E. A., et al. (2007). Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell, 131, 994–1008.
Garrett, R. W., & Emerson, S. G. (2009). Bone and blood vessels: the hard and the soft of hematopoietic stem cell niches. Cell Stem Cell, 4, 503–506.
Greco, V., & Guo, S. (2010). Compartmentalized organization: a common and required feature of stem cell niches? Development, 137, 1586–1594.
Haimovici, H., & Maier, N. (1964). Fate of aortic homografts in canine atherosclerosis. 3. Study of fresh abdominal and thoracic aortic implants into thoracic aorta: role of tissue susceptibility in atherogenesis. Archives of Surgery, 89, 961–969.
Kiel, M. J., Yilmaz, O. H., Iwashita, T., Terhorst, C., & Morrison, S. J. (2005). SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell, 121, 1109–1121.
Kirton, J. P., & Xu, Q. (2010). Endothelial precursors in vascular repair. Microvascular Research, 79, 193–199.
Laird, D. J., von Andrian, U. H., & Wagers, A. J. (2008). Stem cell trafficking in tissue development, growth, and disease. Cell, 132, 612–630.
Zernecke, A., Schober, A., Bot, I., von Hundelshausen, P., Liehn, E. A., Mopps, B., et al. (2005). SDF-1alpha/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells. Circulation Research, 96, 784–791.
Grunewald, M., Avraham, I., Dor, Y., Bachar-Lustig, E., Itin, A., Jung, S., et al. (2006). VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell, 124, 175–189.
Leone, A. M., Valgimigli, M., Giannico, M. B., Zaccone, V., Perfetti, M., D’Amario, D., et al. (2009). From bone marrow to the arterial wall: the ongoing tale of endothelial progenitor cells. European Heart Journal, 30, 890–899.
Shintani, S., Murohara, T., Ikeda, H., Ueno, T., Honma, T., Katoh, A., et al. (2001). Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation, 103, 2776–2779.
Vasa, M., Fichtlscherer, S., Aicher, A., Adler, K., Urbich, C., Martin, H., et al. (2001). Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circulation Research, 89, E1–E7.
Werner, N., Kosiol, S., Schiegl, T., Ahlers, P., Walenta, K., Link, A., et al. (2005). Circulating endothelial progenitor cells and cardiovascular outcomes. The New England Journal of Medicine, 353, 999–1007.
George, J., Goldstein, E., Abashidze, S., Deutsch, V., Shmilovich, H., Finkelstein, A., et al. (2004). Circulating endothelial progenitor cells in patients with unstable angina: association with systemic inflammation. European Heart Journal, 25, 1003–1008.
Thum, T., Tsikas, D., Stein, S., Schultheiss, M., Eigenthaler, M., Anker, S. D., et al. (2005). Suppression of endothelial progenitor cells in human coronary artery disease by the endogenous nitric oxide synthase inhibitor asymmetric dimethylarginine. Journal of the American College of Cardiology, 46, 1693–1701.
Schmidt-Lucke, C., Rossig, L., Fichtlscherer, S., Vasa, M., Britten, M., Kamper, U., et al. (2005). Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair. Circulation, 111, 2981–2987.
Leone, A. M., Rutella, S., Bonanno, G., Abbate, A., Rebuzzi, A. G., Giovannini, S., et al. (2005). Mobilization of bone marrow-derived stem cells after myocardial infarction and left ventricular function. European Heart Journal, 26, 1196–1204.
Michowitz, Y., Goldstein, E., Wexler, D., Sheps, D., Keren, G., & George, J. (2007). Circulating endothelial progenitor cells and clinical outcome in patients with congestive heart failure. Heart, 93, 1046–1050.
Bonello, L., Basire, A., Sabatier, F., Paganelli, F., & Dignat-George, F. (2006). Endothelial injury induced by coronary angioplasty triggers mobilization of endothelial progenitor cells in patients with stable coronary artery disease. Journal of Thrombosis and Haemostasis, 4, 979–981.
Banerjee, S., Brilakis, E., Zhang, S., Roesle, M., Lindsey, J., Philips, B., et al. (2006). Endothelial progenitor cell mobilization after percutaneous coronary intervention. Atherosclerosis, 189, 70–75.
Padfield, G. J., Newby, D. E., & Mills, N. L. (2010). Understanding the role of endothelial progenitor cells in percutaneous coronary intervention. Journal of the American College of Cardiology, 55, 1553–1565.
Gulati, R., Jevremovic, D., Witt, T. A., Kleppe, L. S., Vile, R. G., Lerman, A., et al. (2004). Modulation of the vascular response to injury by autologous blood-derived outgrowth endothelial cells. American Journal of Physiology. Heart and Circulatory Physiology, 287, H512–H517.
Aoki, J., Serruys, P. W., van Beusekom, H., Ong, A. T., McFadden, E. P., Sianos, G., et al. (2005). Endothelial progenitor cell capture by stents coated with antibody against CD34: the HEALING-FIM (Healthy Endothelial Accelerated Lining Inhibits Neointimal Growth-First In Man) Registry. Journal of the American College of Cardiology, 45, 1574–1579.
George, J., Afek, A., Abashidze, A., Shmilovich, H., Deutsch, V., Kopolovich, J., et al. (2005). Transfer of endothelial progenitor and bone marrow cells influences atherosclerotic plaque size and composition in apolipoprotein E knockout mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 25, 2636–2641.
Zoll, J., Fontaine, V., Gourdy, P., Barateau, V., Vilar, J., Leroyer, A., et al. (2008). Role of human smooth muscle cell progenitors in atherosclerotic plaque development and composition. Cardiovascular Research, 77, 471–480.
Bentzon, J. F., Weile, C., Sondergaard, C. S., Hindkjaer, J., Kassem, M., & Falk, E. (2006). Smooth muscle cells in atherosclerosis originate from the local vessel wall and not circulating progenitor cells in ApoE knockout mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 26, 2696–2702.
Tanaka, K., Sata, M., Hirata, Y., & Nagai, R. (2003). Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries. Circulation Research, 93, 783–790.
Zalewski, A., Shi, Y., & Johnson, A. G. (2002). Diverse origin of intimal cells: smooth muscle cells, myofibroblasts, fibroblasts, and beyond? Circulation Research, 91, 652–655.
Mayr, M., Zampetaki, A., Sidibe, A., Mayr, U., Yin, X., De Souza, A. I., et al. (2008). Proteomic and metabolomic analysis of smooth muscle cells derived from the arterial media and adventitial progenitors of apolipoprotein E-deficient mice. Circulation Research, 102, 1046–1056.
Perlman, H., Maillard, L., Krasinski, K., & Walsh, K. (1997). Evidence for the rapid onset of apoptosis in medial smooth muscle cells after balloon injury. Circulation, 95, 981–987.
Barker, S. G., Tilling, L. C., Miller, G. C., Beesley, J. E., Fleetwood, G., Stavri, G. T., et al. (1994). The adventitia and atherogenesis: removal initiates intimal proliferation in the rabbit which regresses on generation of a ‘neoadventitia’. Atherosclerosis, 105, 131–144.
Langheinrich, A. C., Michniewicz, A., Sedding, D. G., Walker, G., Beighley, P. E., Rau, W. S., et al. (2006). Correlation of vasa vasorum neovascularization and plaque progression in aortas of apolipoprotein E(-/-)/low-density lipoprotein(-/-) double knockout mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 26, 347–352.
He, W., Nieponice, A., Soletti, L., Hong, Y., Gharaibeh, B., Crisan, M., et al. (2010). Pericyte-based human tissue engineered vascular grafts. Biomaterials, 31, 8235–8244.
Siow, R. C., & Churchman, A. T. (2007). Adventitial growth factor signalling and vascular remodelling: potential of perivascular gene transfer from the outside-in. Cardiovascular Research, 75, 659–668.
Acknowledgements
This work was supported by grant funding from the National Institutes of Health (HL75566). Dr Psaltis receives post-doctoral research funding from the National Health and Medical Research Council of Australia and the Royal Australasian College of Physicians. The authors have no conflicts to disclose.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Psaltis, P.J., Harbuzariu, A., Delacroix, S. et al. Resident Vascular Progenitor Cells—Diverse Origins, Phenotype, and Function. J. of Cardiovasc. Trans. Res. 4, 161–176 (2011). https://doi.org/10.1007/s12265-010-9248-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12265-010-9248-9