Isolating and characterizing lymphatic endothelial progenitor cells for potential therapeutic lymphangiogenic applications
Source abstract
Abstract
Lymphatic dysfunction is associated with the progression of several vascular disorders, though currently, there are limited strategies to promote new lymphatic vasculature (i.e., lymphangiogenesis) to restore lost lymphatic function. One promising approach to stimulate lymphangiogenesis involves delivering endothelial progenitor cells (EPCs), which are naturally involved in de novo blood vessel formation and have recently been identified to include a lymphatic subpopulation. However, the contribution of lymphatic EPCs in lymphangiogenesis is not clear and challenges with maintaining the activity of transplanted EPCs remain. Thus, the objective of this study was to isolate lymphatic EPCs from human umbilical cord blood and characterize their role in the initial stages of blood or lymphatic vasculature formation. Furthermore, this study also tested the applicability of alginate hydrogels to deliver lymphatic EPCs for a possible therapeutic application. We postulated and confirmed that blood and lymphatic EPC colonies could be isolated from human umbilical cord blood. Additionally, EPC populations responded to either angiogenic or lymphangiogenic growth factors and could stimulate their respective mature endothelial cells in vasculature models in vitro. Finally, lymphatic EPCs maintained their ability to promote lymphatic sprouts after prolonged interactions with the alginate hydrogel microenvironment. These results suggest EPCs have both a blood and a lymphatic population that have specific roles in promoting revascularization and highlight the potential of alginate hydrogels for the delivery of lymphatic EPCs. STATEMENT OF SIGNIFICANCE: Despite the potential therapeutic benefit of promoting lymphatic vasculature, lymphangiogenesis remains understudied. One appealing strategy for promoting lymphangiogenesis involves delivering lymphatic endothelial progenitor cells (EPCs), which are a subpopulation of EPCs involved in de novo vessel formation. Here, we investigate the role of isolated blood and lymphatic EPC subpopulations in promoting the early stages of vascularization and the utility of alginate hydrogels to deliver lymphatic EPCs. We determined that EPCs had two populations that expressed either blood or lymphatic markers, could stimulate their respective mature vasculature in tissue constructs and that alginate hydrogels maintained the therapeutic potential of lymphatic EPCs. We anticipate this work could support promising biomaterial applications of EPCs to promote revascularization, which could have many therapeutic applications.
Source: openalex_inverted_index · Quality: baseline
Research context
OpenAlex topics: Lymphatic System and Diseases · Body Contouring and Surgery
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (99)
Show source-provided references
1. Therapeutic angiogenesis in cardiovascular disease10.1186/1749-8090-2-49 ↗
2. Targets and delivery methods for therapeutic angiogenesis in peripheral artery disease10.1177/1358863X12438270 ↗
3. Therapeutic angiogenesis in cardiovascular disease10.1038/nrd1226 ↗
4. Biomaterials and Cells for Revascularization
5. The lymphatic vasculature in disease10.1038/nm.2545 ↗
6. Lymphangiogenesis in development and human disease10.1038/nature04480 ↗
7. Lymphatic vasculature mediates macrophage reverse cholesterol transport in mice10.1172/JCI63685 ↗
8. The clinical spectrum of lymphatic disease10.1196/annals.1413.015 ↗
9. Lymph, lymphocytes, and lymphatics10.1385/IR:35:1:55 ↗
10. Lymphedema10.1016/S0002-9343(00)00727-0 ↗
11. Lymphatic system in cardiovascular medicine10.1161/CIRCRESAHA.115.306544 ↗
12. The role of lymphatic vessels in the heart10.1016/j.pathophys.2009.07.006 ↗
13. Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity10.1038/ng1642 ↗
14. Selective stimulation of cardiac lymphangiogenesis reduces myocardial edema and fibrosis leading to improved cardiac function following myocardial infarction10.1161/CIRCULATIONAHA.115.020143 ↗
15. Cardiac lymph flow impairment and myocardial fibrosis. Effects of chronic obstruction in dogs
16. Impairment of left ventricular function by acute cardiac lymphatic obstruction10.1016/S0008-6363(96)00177-0 ↗
17. Angiogenesis and lymphangiogenesis and expression of lymphangiogenic factors in the atherosclerotic intima of human coronary arteries10.1016/j.humpath.2005.01.001 ↗
18. Lymphatic transport of high-density lipoproteins and chylomicrons10.1172/JCI71610 ↗
19. Human lymphedema fluid lipoproteins: particle size, cholesterol and apolipoprotein distributions, and electron microscopic structure10.1016/S0022-2275(20)34245-0 ↗
20. Prevascularization of cardiac patch on the omentum improves its therapeutic outcome10.1073/pnas.0812242106 ↗
21. Differentiation of human embryonic stem cells on three-dimensional polymer scaffolds10.1073/pnas.1735463100 ↗
22. Engineering and characterization of functional human microvessels in immunodeficient mice10.1038/labinvest.3780253 ↗
23. Engineering vascular networks in porous polymer matrices10.1002/jbm.10134 ↗
24. Endothelial cells expressing low levels of CD143 (ACE) exhibit enhanced sprouting and potency in relieving tissue ischemia10.1007/s10456-014-9414-9 ↗
25. Material-based deployment enhances efficacy of endothelial progenitor cells10.1073/pnas.0803873105 ↗
26. Guiding morphogenesis in cell-instructive microgels for therapeutic angiogenesis10.1016/j.biomaterials.2017.10.051 ↗
27. Local delivery of VEGF and SDF enhances endothelial progenitor cell recruitment and resultant recovery from ischemia10.1089/ten.tea.2014.0508 ↗
28. Role of progenitor endothelial cells in cardiovascular disease and upcoming therapies
29. Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells10.1161/CIRCRESAHA.108.178590 ↗
30. Endothelial progenitor cells for the vascularization of engineered tissues10.1089/ten.teb.2017.0127 ↗
31. Differentiation of human pluripotent stem cells to cells similar to cord-blood endothelial colony-forming cells10.1038/nbt.3048 ↗
32. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration10.1038/nm0603-702 ↗
33. Vascular incorporation of endothelial colony-forming cells is essential for functional recovery of murine ischemic tissue following cell therapy10.1161/ATVBAHA.111.239822 ↗
34. Endothelial progenitor cells10.1161/01.RES.0000137877.89448.78 ↗
35. Isolation and characterization of circulating lymphatic endothelial colony forming cells10.1016/j.yexcr.2015.11.015 ↗
36. Decreased lymphangiogenic activities and genes expression of cord blood lymphatic endothelial progenitor cells (VEGFR3(+)/Pod(+)/CD11b(+) Cells) in patient with preeclampsia10.3390/ijms22084237 ↗
37. Podoplanin-expressing cells derived from bone marrow play a crucial role in postnatal lymphatic neovascularization10.1161/CIRCULATIONAHA.110.941468 ↗
38. Endothelial cells from cord blood CD133(+)CD34(+) progenitors share phenotypic, functional and gene expression profile similarities with lymphatics10.1111/j.1582-4934.2008.00340.x ↗
39. VEGFR-3 and CD133 identify a population of CD34(+) lymphatic/vascular endothelial precursor cells10.1182/blood-2002-03-0755 ↗
40. CD34(+)VEGFR-3(+) progenitor cells have a potential to differentiate towards lymphatic endothelial cells10.1111/jcmm.12233 ↗
41. Enhancement of cardiac lymphangiogenesis by transplantation of CD34(+)VEGFR-3(+) endothelial progenitor cells and sustained release of VEGF-C10.1007/s00395-019-0752-z ↗
42. Vascular repair by circulating endothelial progenitor cells: the missing link in atherosclerosis?10.1007/s00109-004-0580-x ↗
43. Enzymatically degradable alginate hydrogel systems to deliver endothelial progenitor cells for potential revasculature applications10.1016/j.biomaterials.2018.06.038 ↗
44. Microvascular engineering: Dynamic changes in microgel-entrapped vascular cells correlates with higher vasculogenic/angiogenic potential10.1016/j.biomaterials.2019.119554 ↗
45. Viability and functionality of cells delivered from peptide conjugated scaffolds10.1016/j.biomaterials.2010.12.048 ↗
46. Computational-based design of hydrogels with predictable mesh properties10.1021/acsbiomaterials.9b01520 ↗
47. Tissue cells feel and respond to the stiffness of their substrate10.1126/science.1116995 ↗
48. How matrix properties control the self-assembly and maintenance of tissues10.1007/s10439-011-0310-9 ↗
49. Cell-cell mechanical communication through compliant substrates10.1529/biophysj.107.127662 ↗
50. Stiffness of protease sensitive and cell adhesive peg hydrogels promotes neovascularization in vivo10.1007/s10439-017-1822-8 ↗
51. Hypoxia augments outgrowth endothelial cell (OEC) sprouting and directed migration in response to sphingosine-1-phosphate (S1P)10.1371/journal.pone.0123437 ↗
52. Isolation and characterization of endothelial progenitor cells from human blood
53. Alginate hydrogels allow for bioactive and sustained release of VEGF-C and VEGF-D for lymphangiogenic therapeutic applications10.1371/journal.pone.0181484 ↗
54. Spatiotemporal control of vascular endothelial growth factor delivery from injectable hydrogels enhances angiogenesis10.1111/j.1538-7836.2007.02386.x ↗
55. Labeling pinocytotic vesicles and cytoplasm with fluorescently labeled ficoll or dextran10.1101/pdb.prot5572 ↗
56. A three-dimensional in vitro model of tumor cell intravasation10.1039/c3ib40170g ↗
57. Cancer-associated fibroblasts support vascular growth through mechanical force10.1038/s41598-017-13006-x ↗
58. Alginate type and RGD density control myoblast phenotype10.1002/jbm.1287 ↗
59. Alginate-Chitosan hydrogels provide a sustained gradient of sphingosine-1-phosphate for therapeutic angiogenesis
60. Alginate hydrogels of varied molecular weight distribution enable sustained release of sphingosine-1-phosphate and promote angiogenesis10.1002/jbm.a.36217 ↗
61. Phenotype-based high-content chemical library screening identifies statins as inhibitors of in vivo lymphangiogenesis10.1073/pnas.1206036109 ↗
62. Effects of VEGF temporal and spatial presentation on angiogenesis10.1016/j.biomaterials.2009.10.052 ↗
63. Prox1, master regulator of the lymphatic vasculature phenotype10.1007/s00441-003-0747-8 ↗
64. Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate10.1002/dvdy.10163 ↗
65. The vascular endothelial growth factor (VEGF) family: angiogenic factors in health and disease10.1186/gb-2005-6-2-209 ↗
66. Vascular endothelial growth factor (VEGF) and its receptor (VEGFR) signaling in angiogenesis: a crucial target for anti- and pro-angiogenic therapies10.1177/1947601911423031 ↗
67. Molecular mechanisms of lymphangiogenesis in health and disease10.1016/S1535-6108(02)00051-X ↗
68. Phosphorylation of Akt and ERK1/2 is required for VEGF-A/VEGFR2-induced proliferation and migration of lymphatic endothelium10.1371/journal.pone.0028947 ↗
69. Vascular endothelial growth factor receptor-2 promotes the development of the lymphatic vasculature10.1371/journal.pone.0074686 ↗
70. Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells10.1016/S0002-9440(10)63851-5 ↗
71. VEGF-A promotes tissue repair-associated lymphatic vessel formation via VEGFR-2 and the alpha1beta1 and alpha2beta1 integrins10.1096/fj.03-1179fje ↗
72. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice10.1126/science.276.5317.1423 ↗
73. Functional interaction of VEGF-C and VEGF-D with neuropilin receptors10.1096/fj.05-5646com ↗
74. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-310.1093/emboj/20.17.4762 ↗
75. Biology of vascular endothelial growth factor c in the morphogenesis of lymphatic vessels10.3389/fbioe.2018.00007 ↗
76. Transcriptional profiling of VEGF-A and VEGF-C target genes in lymphatic endothelium reveals endothelial-specific molecule-1 as a novel mediator of lymphangiogenesis10.1182/blood-2008-05-156331 ↗
77. Lymphangiogenesis: molecular mechanisms and future promise10.1016/j.cell.2010.01.045 ↗
78. Intrinsic versus microenvironmental regulation of lymphatic endothelial cell phenotype and function10.1096/fj.03-0179com ↗
79. Anti-VEGF-A therapy reduces lymphatic vessel density and expression of VEGFR-3 in an orthotopic breast tumor model10.1002/ijc.22937 ↗
80. Angiogenic sprouting and capillary lumen formation modeled by human umbilical vein endothelial cells (HUVEC) in fibrin gels: the role of fibroblasts and Angiopoietin-110.1016/S0026-2862(03)00045-1 ↗
81. VEGF and VEGF-C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane10.1006/dbio.1997.8639 ↗
82. Isolation of putative progenitor endothelial cells for angiogenesis10.1126/science.275.5302.964 ↗
83. Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance10.1111/j.1582-4934.2004.tb00474.x ↗
84. Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants10.1038/nm1340 ↗
85. Concise review: circulating endothelial progenitor cells for vascular medicine10.1002/stem.745 ↗
86. Clincal Trials
87. Endothelial progenitor cells: past, state of the art, and future10.1111/j.1582-4934.2004.tb00473.x ↗
88. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization10.1073/pnas.97.7.3422 ↗
89. Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice10.1172/JCI9087 ↗
90. Biomaterial based strategies for engineering new lymphatic vasculature10.1002/adhm.202000895 ↗
91. Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C10.1074/jbc.273.14.8413 ↗
92. Comparative expression of vascular endothelial growth factor family members, VEGF-B, -C and -D, by normal human keratinocytes and fibroblasts10.1111/j.0906-6705.2004.00137.x ↗
93. Tissue-engineered 3D human lymphatic microvascular network for in vitro studies of lymphangiogenesis10.1038/nprot.2017.025 ↗
94. Three-dimensional biomimetic model to reconstitute sprouting lymphangiogenesis in vitro10.1016/j.biomaterials.2015.11.019 ↗
95. Enhanced survival and engraftment of transplanted stem cells using growth factor sequestering hydrogels10.1016/j.biomaterials.2014.12.043 ↗
96. Cell therapy for heart failure a comprehensive overview of experimental and clinical studies, current challenges, and future directions10.1161/CIRCRESAHA.113.300219 ↗
97. Degradation of partially oxidized alginate and its potential application for tissue engineering10.1021/bp010070p ↗
98. Microencapsulated islets as bioartificial endocrine pancreas10.1126/science.6776628 ↗
99. Cell-compatible covalently reinforced beads obtained from a chemoenzymatically engineered alginate10.1016/j.biomaterials.2006.05.011 ↗