Vascular wall as a reservoir for different types of stem and progenitor cells.

Tissue regeneration and several diseases such as tumor and atherosclerosis depend on new vessel formation by both angiogenesis and vasculogenesis. Endothelial cells (ECs) are widely considered to be the active cellular component in these processes, followed by contractile cells such as pericytes and smooth muscle cells. The best known sources providing these cell types or their progenitors are ECs lining the vessel lumen and bone marrow. As easily evident, the vessel wall was recognized as being a passive player to a great extent except ECs of the vascular intima. Particularly, the vascular adventitia has been considered as a passive layer rather than an active part of the vessel wall. But results provided during the last few years have led to a revision of this classical view because of an apparent stem cell niche function of the vascular adventitia. This review aims to sum up findings identifying the vessel wall as an important stem cell reservoir and discusses its impact on health and disease.

[1]  M. Bennett,et al.  Progenitor cell-derived smooth muscle cells in vascular disease. , 2010, Biochemical pharmacology.

[2]  MirkoCorselli,et al.  Perivascular Ancestors of Adult Multipotent Stem Cells , 2010 .

[3]  G. Lin,et al.  Defining adipose tissue-derived stem cells in tissue and in culture. , 2010, Histology and histopathology.

[4]  S. Ergün,et al.  Vascular wall-resident stem cells. , 2010, Histology and histopathology.

[5]  G. Angelini,et al.  Human Adult Vena Saphena Contains Perivascular Progenitor Cells Endowed With Clonogenic and Proangiogenic Potential , 2010, Circulation.

[6]  T. Katagiri,et al.  Impact of implanted bone marrow progenitor cell composition on limb salvage after cell implantation in patients with critical limb ischemia. , 2010, Atherosclerosis.

[7]  D. Stainier,et al.  Hematopoietic stem cells derive directly from aortic endothelium during development , 2009, Nature.

[8]  S. Rafii,et al.  Emerging biology of vascular wall progenitor cells in health and disease. , 2009, Trends in molecular medicine.

[9]  K. Yoshimura,et al.  Functional Implications of Cd34 Expression in Human Adipose–derived Stem/progenitor Cells , 2022 .

[10]  Mark Vermeulen,et al.  Human placenta is a potent hematopoietic niche containing hematopoietic stem and progenitor cells throughout development. , 2009, Cell stem cell.

[11]  F. Tondato,et al.  Bone marrow-derived B cells preserve ventricular function after acute myocardial infarction. , 2009, JACC. Cardiovascular interventions.

[12]  D. Stainier,et al.  Characterization of vascular mural cells during zebrafish development , 2009, Mechanisms of Development.

[13]  M. Yoder,et al.  Endothelial progenitor cell: ongoing controversy for defining these cells and their role in neoangiogenesis in the murine system , 2009, Current opinion in hematology.

[14]  Scott T. Robinson,et al.  Beyond the adventitia: exploring the outer limits of the blood vessel wall. , 2009, Circulation research.

[15]  E. Dickson,et al.  Proinflammatory Phenotype of Perivascular Adipocytes: Influence of High-Fat Feeding , 2009, Circulation research.

[16]  Shin-Ichi Nishikawa,et al.  Continuous single-cell imaging of blood generation from haemogenic endothelium , 2009, Nature.

[17]  F. Timmermans,et al.  Endothelial progenitor cells: identity defined? , 2008, Journal of cellular and molecular medicine.

[18]  J. Kovacic,et al.  Resident vascular progenitor cells: an emerging role for non-terminally differentiated vessel-resident cells in vascular biology. , 2009, Stem cell research.

[19]  M. Yoder,et al.  Endothelial progenitor cells and cardiovascular cell-based therapies. , 2009, Cytotherapy.

[20]  G. Striker,et al.  The origin of post-injury neointimal cells in the rat balloon injury model. , 2009, Cardiovascular research.

[21]  Michael S. Becker,et al.  Fate tracing reveals the endothelial origin of hematopoietic stem cells. , 2008, Cell stem cell.

[22]  G. Lin,et al.  Defining stem and progenitor cells within adipose tissue. , 2008, Stem cells and development.

[23]  S. Badylak,et al.  A perivascular origin for mesenchymal stem cells in multiple human organs. , 2008, Cell stem cell.

[24]  M. Majesky,et al.  A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells , 2008, Proceedings of the National Academy of Sciences.

[25]  S. Ergün,et al.  Endothelial and Hematopoietic Progenitor Cells (EPCs and HPCs): Hand in Hand Fate Determining Partners for Cancer Cells , 2008, Stem Cell Reviews.

[26]  Qingbo Xu,et al.  Vascular repair by endothelial progenitor cells. , 2008, Cardiovascular research.

[27]  M. Zago,et al.  Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. , 2008, Experimental hematology.

[28]  N. Guseva,et al.  Circulating endothelial progenitor cells in systemic sclerosis: relation to impaired angiogenesis and cardiovascular manifestations. , 2008, Clinical and experimental rheumatology.

[29]  Shahin Rafii,et al.  Migratory neighbors and distant invaders: tumor-associated niche cells. , 2008, Genes & development.

[30]  J. Gimble,et al.  Multipotential human adipose‐derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo , 2008, Journal of cellular physiology.

[31]  K. Kissa,et al.  Live imaging of emerging hematopoietic stem cells and early thymus colonization. , 2008, Blood.

[32]  S. Rafii,et al.  A Few to Flip the Angiogenic Switch , 2008, Science.

[33]  D. Nolan,et al.  Endothelial Progenitor Cells Control the Angiogenic Switch in Mouse Lung Metastasis , 2008, Science.

[34]  W. Arap,et al.  A Population of Multipotent CD34-Positive Adipose Stromal Cells Share Pericyte and Mesenchymal Surface Markers, Reside in a Periendothelial Location, and Stabilize Endothelial Networks , 2008, Circulation research.

[35]  D. Lyden A Few to Flip the Angiogenic , 2008 .

[36]  M. Rudnicki,et al.  Resident Endothelial Precursors in Muscle, Adipose, and Dermis Contribute to Postnatal Vasculogenesis , 2007, Stem cells.

[37]  Giselle Chamberlain,et al.  Concise Review: Mesenchymal Stem Cells: Their Phenotype, Differentiation Capacity, Immunological Features, and Potential for Homing , 2007, Stem cells.

[38]  C. Gargett,et al.  Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. , 2007, Human reproduction.

[39]  B. Sacchetti,et al.  Self-Renewing Osteoprogenitors in Bone Marrow Sinusoids Can Organize a Hematopoietic Microenvironment , 2007, Cell.

[40]  S. Ergün,et al.  Potential implications of vascular wall resident endothelial progenitor cells , 2007, Thrombosis and Haemostasis.

[41]  T. Asahara,et al.  Role of progenitor endothelial cells in cardiovascular disease and upcoming therapies , 2007, Catheterization and cardiovascular interventions : official journal of the Society for Cardiac Angiography & Interventions.

[42]  P. Tazzari,et al.  Thoracic Aortas from Multiorgan Donors Are Suitable for Obtaining Resident Angiogenic Mesenchymal Stromal Cells , 2007, Stem cells.

[43]  M. Yoder,et al.  Human CD34+AC133+VEGFR-2+ cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. , 2007, Experimental hematology.

[44]  D. Scheinberg,et al.  Bone marrow-derived endothelial progenitor cells are a major determinant of nascent tumor neovascularization. , 2007, Genes & development.

[45]  G. Invernici,et al.  Human fetal aorta contains vascular progenitor cells capable of inducing vasculogenesis, angiogenesis, and myogenesis in vitro and in a murine model of peripheral ischemia. , 2007, The American journal of pathology.

[46]  A. Zernecke,et al.  Perivascular Mast Cells Promote Atherogenesis and Induce Plaque Destabilization in Apolipoprotein E–Deficient Mice , 2007, Circulation.

[47]  M. Rudnicki,et al.  Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. , 2007, Molecular therapy : the journal of the American Society of Gene Therapy.

[48]  I. Weissman,et al.  Stem cells: Blood lines from embryo to adult , 2007, Nature.

[49]  H. Tse,et al.  Burden of carotid atherosclerosis in patients with stroke: relationships with circulating endothelial progenitor cells and hypertension , 2007, Journal of Human Hypertension.

[50]  C. Heeschen,et al.  Nonbone Marrow-Derived Circulating Progenitor Cells Contribute to Postnatal Neovascularization Following Tissue Ischemia , 2007, Circulation research.

[51]  B. Sacchetti,et al.  Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells , 2007, Nature Cell Biology.

[52]  M. Shibuya,et al.  alpha4-Integrin(+) endothelium derived from primate embryonic stem cells generates primitive and definitive hematopoietic cells. , 2006, Blood.

[53]  J. Folkman Angiogenesis: an organizing principle for drug discovery? , 2007, Nature reviews. Drug discovery.

[54]  I. Bayazitov,et al.  A perivascular niche for brain tumor stem cells. , 2007, Cancer cell.

[55]  A. Avogaro,et al.  Diabetes impairs progenitor cell mobilisation after hindlimb ischaemia–reperfusion injury in rats , 2006, Diabetologia.

[56]  G. Nickenig,et al.  Improvement of Endothelial Function by Systemic Transfusion of Vascular Progenitor Cells , 2006, Circulation research.

[57]  I. Weissman,et al.  Clonal analysis of mouse development reveals a polyclonal origin for yolk sac blood islands. , 2006, Developmental cell.

[58]  D. Stainier,et al.  A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula , 2006, Nature.

[59]  Masatomo Kobayashi,et al.  Drosophila IKK-Related Kinase Regulates Nonapoptotic Function of Caspases via Degradation of IAPs , 2006, Cell.

[60]  Kotaro Yoshimura,et al.  Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates , 2006, Journal of cellular physiology.

[61]  Lindolfo da Silva Meirelles,et al.  Mesenchymal stem cells reside in virtually all post-natal organs and tissues , 2006, Journal of Cell Science.

[62]  Raghu Kalluri,et al.  Fibroblasts in cancer , 2006, Nature Reviews Cancer.

[63]  S. Rafii,et al.  Contribution of endothelial progenitors and proangiogenic hematopoietic cells to vascularization of tumor and ischemic tissue , 2006, Current opinion in hematology.

[64]  H. Reichenspurner,et al.  Vascular wall resident progenitor cells: a source for postnatal vasculogenesis , 2006, Development.

[65]  M. Iruela-Arispe,et al.  The Ever-Elusive Endothelial Progenitor Cell: Identities, Functions and Clinical Implications , 2006, Pediatric Research.

[66]  Victor Frenkel,et al.  Magnetic Resonance Imaging and Confocal Microscopy Studies of Magnetically Labeled Endothelial Progenitor Cells Trafficking to Sites of Tumor Angiogenesis , 2006, Stem cells.

[67]  M. Frid,et al.  Hypoxia-induced pulmonary vascular remodeling requires recruitment of circulating mesenchymal precursors of a monocyte/macrophage lineage. , 2006, The American journal of pathology.

[68]  G. Nickenig,et al.  Influence of cardiovascular risk factors on endothelial progenitor cells: limitations for therapy? , 2005, Arteriosclerosis, thrombosis, and vascular biology.

[69]  Erik L Ritman,et al.  Correlation of Vasa Vasorum Neovascularization and Plaque Progression in Aortas of Apolipoprotein E−/−/Low-Density Lipoprotein−/− Double Knockout Mice , 2005, Arteriosclerosis, thrombosis, and vascular biology.

[70]  Peter Carmeliet,et al.  Angiogenesis in life, disease and medicine , 2005, Nature.

[71]  Napoleone Ferrara,et al.  Angiogenesis as a therapeutic target , 2005, Nature.

[72]  S. Rafii,et al.  VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche , 2005, Nature.

[73]  H. Miller,et al.  Transfer of Endothelial Progenitor and Bone Marrow Cells Influences Atherosclerotic Plaque Size and Composition in Apolipoprotein E Knockout Mice , 2005, Arteriosclerosis, thrombosis, and vascular biology.

[74]  Luigi Naldini,et al.  Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. , 2005, Cancer cell.

[75]  S. Morrison,et al.  Supplemental Experimental Procedures , 2022 .

[76]  Xunbin Wei,et al.  In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment , 2005, Nature.

[77]  E. Oberlin,et al.  The Vascular Wall as a Source of Stem Cells , 2005, Annals of the New York Academy of Sciences.

[78]  S. Dimmeler,et al.  Risk factors for coronary artery disease, circulating endothelial progenitor cells, and the role of HMG-CoA reductase inhibitors. , 2005, Kidney international.

[79]  M. Yoder,et al.  Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. , 2005, Blood.

[80]  M. Yamagishi,et al.  Adrenomedullin Enhances Angiogenic Potency of Bone Marrow Transplantation in a Rat Model of Hindlimb Ischemia , 2005, Circulation.

[81]  R. Jain Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy , 2005, Science.

[82]  M. Baron,et al.  Mouse embryonic explant culture system for analysis of hematopoietic and vascular development. , 2005, Methods in molecular medicine.

[83]  V. Kouskoff,et al.  Haemangioblast commitment is initiated in the primitive streak of the mouse embryo , 2004, Nature.

[84]  Mark A. Hall,et al.  Hemostasis, Thrombosis, and Vascular Biology Materials and Methods Lacz and Platelet Endothelial Cell Adhesion Molecule 1 (pecam-1) Staining , 2022 .

[85]  Evan S. Garfein,et al.  First Evidence that Bone Marrow Cells Contribute to the Construction of Tissue Engineered Vascular Autografts In Vivo , 2004 .

[86]  T. Asahara,et al.  Endothelial progenitor cells for postnatal vasculogenesis. , 2004, American journal of physiology. Cell physiology.

[87]  R. Storb,et al.  Allogeneic hematopoietic cell transplantation as treatment for hematological malignancies: a review , 2004, Springer Seminars in Immunopathology.

[88]  R. Tuan,et al.  Transdifferentiation potential of human mesenchymal stem cells derived from bone marrow , 2004, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[89]  Peter Carmeliet,et al.  Manipulating angiogenesis in medicine , 2004, Journal of internal medicine.

[90]  M. Frid,et al.  Hypoxia-induced pulmonary artery adventitial remodeling and neovascularization: contribution of progenitor cells. , 2004, American journal of physiology. Lung cellular and molecular physiology.

[91]  H. Miller,et al.  Circulating endothelial progenitor cells in patients with unstable angina: association with systemic inflammation. , 2004, European heart journal.

[92]  G. Sukhikh,et al.  Mesenchymal Stem Cells , 2002, Bulletin of Experimental Biology and Medicine.

[93]  B. Lévy,et al.  Transplantation of Bone Marrow–Derived Mononuclear Cells in Ischemic Apolipoprotein E–Knockout Mice Accelerates Atherosclerosis Without Altering Plaque Composition , 2003, Circulation.

[94]  K. Watson,et al.  Multilineage Potential of Cells From the Artery Wall , 2003, Circulation.

[95]  K. Arai,et al.  Erythropoiesis from acetyl LDL incorporating endothelial cells at the preliver stage. , 2003, Blood.

[96]  Shahin Rafii,et al.  Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration , 2003, Nature Medicine.

[97]  H. Daida,et al.  Isolation of Bone Marrow Stromal Cell–Derived Smooth Muscle Cells by a Human SM22&agr; Promoter: In Vitro Differentiation of Putative Smooth Muscle Progenitor Cells of Bone Marrow , 2003, Circulation.

[98]  S. Gronthos,et al.  Perivascular Niche of Postnatal Mesenchymal Stem Cells in Human Bone Marrow and Dental Pulp , 2003, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[99]  Y. Romanov,et al.  Searching for Alternative Sources of Postnatal Human Mesenchymal Stem Cells: Candidate MSC‐Like Cells from Umbilical Cord , 2003, Stem cells.

[100]  Koichi Hattori,et al.  Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy? , 2002, Nature Reviews Cancer.

[101]  C. Verfaillie,et al.  Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. , 2002, Experimental hematology.

[102]  T. Asahara,et al.  Bone marrow-derived endothelial progenitor cells for vascular regeneration. , 2002, Current opinion in molecular therapeutics.

[103]  M. Goodell,et al.  Hematopoietic, vascular and cardiac fates of bone marrow-derived stem cells , 2002, Gene Therapy.

[104]  E. Ritman,et al.  Chronic endothelin receptor antagonism prevents coronary vasa vasorum neovascularization in experimental hypercholesterolemia. , 2002, Journal of the American College of Cardiology.

[105]  J. Isner,et al.  Endothelial progenitor cells for vascular regeneration. , 2002, Journal of hematotherapy & stem cell research.

[106]  E. Parati,et al.  Human Vasculogenesis Ex Vivo: Embryonal Aorta as a Tool for Isolation of Endothelial Cell Progenitors , 2001, Laboratory Investigation.

[107]  S. Ergün,et al.  CEA-related cell adhesion molecule 1: a potent angiogenic factor and a major effector of vascular endothelial growth factor. , 2000, Molecular cell.

[108]  K. Pantel,et al.  In vitro differentiation of endothelial cells from AC133-positive progenitor cells. , 1999, Blood.

[109]  L. De Angelis,et al.  Skeletal Myogenic Progenitors Originating from Embryonic Dorsal Aorta Coexpress Endothelial and Myogenic Markers and Contribute to Postnatal Muscle Growth and Regeneration , 1999, The Journal of cell biology.

[110]  M. Pittenger,et al.  Multilineage potential of adult human mesenchymal stem cells. , 1999, Science.

[111]  S. Rafii,et al.  Evidence for circulating bone marrow-derived endothelial cells. , 1998, Blood.

[112]  S. Nishikawa,et al.  In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos. , 1998, Immunity.

[113]  M. Kennedy,et al.  A common precursor for hematopoietic and endothelial cells. , 1998, Development.

[114]  W. Risau,et al.  Mechanisms of angiogenesis , 1997, Nature.

[115]  Takayuki Asahara,et al.  Isolation of Putative Progenitor Endothelial Cells for Angiogenesis , 1997, Science.

[116]  K. Sueishi,et al.  Intimal neovascularization in human coronary atherosclerosis: its origin and pathophysiological significance. , 1995, Human pathology.

[117]  A. Barger,et al.  Hypothesis: vasa vasorum and neovascularization of human coronary arteries. A possible role in the pathophysiology of atherosclerosis. , 1984, The New England journal of medicine.

[118]  N. Simionescu,et al.  The Cardiovascular System , 1983 .

[119]  J. Folkman Tumor angiogenesis: therapeutic implications. , 1971, The New England journal of medicine.

[120]  J Folkman,et al.  Transplacental carcinogenesis by stilbestrol. , 1971, The New England journal of medicine.

[121]  F. Gonzalez-crussi,et al.  Vasculogenesis in the chick embryo. An ultrastructural study. , 1971, The American journal of anatomy.