Development and aging of the lymphatic vascular system

González-Loyola, Alejandra; Petrova, Tatiana V.

doi:10.1016/j.addr.2020.12.005

Cited by 89Lymphatic System and DiseasesLymphatic Disorders and TreatmentsVascular Malformations and Hemangiomas

Development and aging of the lymphatic vascular system

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González-Loyola, Alejandra, Petrova, Tatiana V.·2021·Advanced Drug Delivery Reviews

DOI 10.1016/j.addr.2020.12.005

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Abstract

The lymphatic vasculature has a pivotal role in regulating body fluid homeostasis, immune surveillance and dietary fat absorption. The increasing number of in vitro and in vivo studies in the last decades has shed light on the processes of lymphatic vascular development and function. Here, we will discuss the current progress in lymphatic vascular biology such as the mechanisms of lymphangiogenesis, lymphatic vascular maturation and maintenance and the emerging mechanisms of lymphatic vascular aging.

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Valve defects are associated with deficiencies or mutations in many different LEC molecules, and defective lymphatic valves underlie many forms of primary lymphedema.
“Valve defects are associated with deficiencies or mutations in many different LEC molecules, and defective lymphatic valves underlie many forms of primary lymphedema (see 37, table 1).”
From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [37]
Section 3.3 (page unavailable) says that many genes regulating lymphatic valve development are associated with lymphatic vascular defects in humans, and identifies FOXC2 and GATA2 mutations in lymphedema syndromes. This supports the link between valve-related molecules and disease, but the cited passages do not establish that defective valves themselves underlie many forms of primary lymphedema. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Murine valves begin to develop around day E16.5 and share a similar developmental program with venous valves, in which valve cells become enriched in Prox1, Gata2, Foxc2, Nfatc1, Cldn11, and laminin α5.
“Murine valves begin to develop around day E16.5 and share a similar developmental program with venous valves, in which valve cells become enriched in Prox1, Gata2, Foxc2, Nfatc1, Cldn11, and laminin α5 (37).”
From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [37]
Section 3.3 describes mouse collecting-vessel formation beginning around E15.5 and identifies PROX1-high, FOXC2-high valve-forming cells, high GATA2 expression in valve cells, and NFAT signalling in valve development. It does not establish that valves begin developing at E16.5, compare their developmental program with venous valves, or identify Cldn11 and laminin α5 as enriched valve-cell markers. Page numbers were unavailable in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Lymphedema can result from genetic mutations in critical genes controlling lymphatic vessel or valve development, surgical disruption of lymphatic networks, and/or impaired pumping of collecting lymphatic vessels.
“Lymphedema is the accumulation of excess interstitial fluid as a result of lymphatic dysfunction, and can result from genetic mutations in critical genes controlling lymphatic vessel or valve development (37), surgical disruption of lymphatic networks (131), and/or impaired pumping of collecting lymphatic vessels (49, 57).”
From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [37]

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GATA2 is required for lymphatic vessel valve development and maintenance
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Lymphatic endothelial progenitors bud from the cardinal vein and intersomitic vessels in mammalian embryos
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Dural lymphatics regulate clearance of extracellular tau from the CNS
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Connexin37 and Connexin43 deficiencies in mice disrupt lymphatic valve development and result in lymphatic disorders including lymphedema and chylothorax
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Piezo1 incorporates mechanical force signals into the genetic program that governs lymphatic valve development and maintenance
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Planar Cell Polarity Protein Celsr1 Regulates Endothelial Adherens Junctions and Directed Cell Rearrangements during Valve Morphogenesis
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Targeting lymphatic function as a novel therapeutic intervention for rheumatoid arthritis
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Lymphatic Endothelial Cells Control Initiation of Lymph Node Organogenesis
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Roles of lymphatic endothelial cells expressing peripheral tissue antigens in CD4 T-cell tolerance induction
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A Single-Cell Transcriptional Roadmap of the Mouse and Human Lymph Node Lymphatic Vasculature
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Mechanotransduction activates canonical Wnt/β-catenin signaling to promote lymphatic vascular patterning and the development of lymphatic and lymphovenous valvesPreprint
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Restoration of lymphatic function rescues obesity in Prox1-haploinsufficient mice
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Laminar flow downregulates Notch activity to promote lymphatic sprouting
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Clearance of cerebrospinal fluid from the sacral spine through lymphatic vessels
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Biology of Vascular Endothelial Growth Factor C in the Morphogenesis of Lymphatic Vessels
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Tumor-associated factors are enriched in lymphatic exudate compared to plasma in metastatic melanoma patients
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Angiopoietin 2 regulates the transformation and integrity of lymphatic endothelial cell junctions
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Endothelial ERK signaling controls lymphatic fate specification
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Vascular endothelial growth factor C attenuates joint damage in chronic inflammatory arthritis by accelerating local lymphatic drainage in mice
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Loss of ADAMTS3 activity causes Hennekam lymphangiectasia–lymphedema syndrome 3
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Lymphatic and Immune Cell Cross-Talk Regulates Cardiac Recovery After Experimental Myocardial Infarction
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Impaired Humoral Immunity and Tolerance in K14-VEGFR-3-Ig Mice That Lack Dermal Lymphatic Drainage
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Lymphatic Vessel Insufficiency in Hypercholesterolemic Mice Alters Lipoprotein Levels and Promotes Atherogenesis
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Paraxial Mesoderm Is the Major Source of Lymphatic Endothelium
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Lymphatic impairment leads to pulmonary tertiary lymphoid organ formation and alveolar damage
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EPHB4 kinase–inactivating mutations cause autosomal dominant lymphatic-related hydrops fetalis
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Akt/Protein Kinase B Is Required for Lymphatic Network Formation, Remodeling, and Valve Development
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Multiple roles of lymphatic vessels in tumor progression
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Analysis of the coding regions of VEGFR3 and VEGFC in Milroy disease and other primary lymphoedemas
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Aging-Associated Alterations in Contractility of Rat Mesenteric Lymphatic Vessels
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Multiple roles of lymphatic vessels in peripheral lymph node development
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Regulatory T cell transfer ameliorates lymphedema and promotes lymphatic vessel function
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A Second Heart Field-Derived Vasculogenic Niche Contributes to Cardiac Lymphatics
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Lymphatic Endothelial Cell Junctions: Molecular Regulation in Physiology and Diseases
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Isl1-expressing non-venous cell lineage contributes to cardiac lymphatic vessel development
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Polydom Is an Extracellular Matrix Protein Involved in Lymphatic Vessel Remodeling
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The evolving role of lymphatics in cancer metastasis
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Distribution of lymphatic vessels in normal and arthritic human synovial tissues
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Decline of lymphatic vessel density and function in murine skin during aging
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Efficient activation of the lymphangiogenic growth factor VEGF-C requires the C-terminal domain of VEGF-C and the N-terminal domain of CCBE1
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Lymphatic function is required prenatally for lung inflation at birth
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EphB4 forward signalling regulates lymphatic valve development
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HHEX is a transcriptional regulator of the VEGFC/FLT4/PROX1 signaling axis during vascular development
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A blood capillary plexus-derived population of progenitor cells contributes to genesis of the dermal lymphatic vasculature during embryonic development
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ORAI1 Activates Proliferation of Lymphatic Endothelial Cells in Response to Laminar Flow Through Krüppel-Like Factors 2 and 4
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Early rescue of lymphatic function limits atherosclerosis progression in Ldlr mice
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Specific fibroblast subpopulations and neuronal structures provide local sources of Vegfc-processing components during zebrafish lymphangiogenesis
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Aging-associated shifts in functional status of mast cells located by adult and aged mesenteric lymphatic vessels
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CCR7 and IRF4-dependent dendritic cells regulate lymphatic collecting vessel permeability
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Mesenteric lymph flow in adult and aged rats
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Vegfd modulates both angiogenesis and lymphangiogenesis during zebrafish embryonic development
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NFATc1 regulates lymphatic endothelial development
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The lymphatic vasculature: development and role in shaping immunity
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Foxc1 and Foxc2 deletion causes abnormal lymphangiogenesis and correlates with ERK hyperactivation
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Influence of exercise and aging on extracellular matrix composition in the skeletal muscle stem cell niche
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Distinct roles of VE‐cadherin for development and maintenance of specific lymph vessel beds
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EMILIN1/α9β1 Integrin Interaction Is Crucial in Lymphatic Valve Formation and Maintenance
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Interdependence of stromal and immune cells for lymph node function
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An Evolutionarily Conserved Role for Polydom/Svep1 During Lymphatic Vessel Formation
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Transgenic Induction of Vascular Endothelial Growth Factor-C Is Strongly Angiogenic in Mouse Embryos but Leads to Persistent Lymphatic Hyperplasia in Adult Tissues
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A novel mutation in GJA1 causing oculodentodigital syndrome and primary lymphoedema in a three generation family
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Steroid-Resistant Lymphatic Remodeling in Chronically Inflamed Mouse Airways
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Genetic Dissection of Tie Pathway in Mouse Lymphatic Maturation and Valve Development
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RASA1 regulates the function of lymphatic vessel valves in mice
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Epigenetic Signatures and Vascular Risk in Type 2 Diabetes: A Clinical Perspective
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Methicillin-resistant Staphylococcus aureus causes sustained collecting lymphatic vessel dysfunction
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Distinct fibroblast subsets regulate lacteal integrity through YAP/TAZ-induced VEGF-C in intestinal villi
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Complementary Wnt Sources Regulate Lymphatic Vascular Development via PROX1-Dependent Wnt/β-Catenin Signaling
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Taking the lymphatic route: dendritic cell migration to draining lymph nodes
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Lymph sacs are not required for the initiation of lymph node formation
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Temporal and spatial regulation of epsin abundance and VEGFR3 signaling are required for lymphatic valve formation and function
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Shear stimulation of FOXC1 and FOXC2 differentially regulates cytoskeletal activity during lymphatic valve maturation
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Lymphatic vessel: Origin, heterogeneity, biological functions and therapeutic targets
Hu, Z., Zhao, X., Wu, Z., Qu, B., Yuan, M., Xing, Y., Song, Y., & Wang, Z. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01723-x · Cited by 103 · see citing works
FOXC2 controls adult lymphatic endothelial specialization, function, and gut lymphatic barrier preventing multiorgan failure
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Gut-Derived Metabolite, Trimethylamine-N-oxide (TMAO) in Cardio-Metabolic Diseases: Detection, Mechanism, and Potential Therapeutics
Shanmugham, M., Bellanger, S., & Leo, C. H. (2023) · Pharmaceuticals · doi:10.3390/ph16040504 · Cited by 96 · see citing works
Homeostatic maintenance of the lymphatic vasculature
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The stromal microenvironment and ovarian aging: mechanisms and therapeutic opportunities
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The Impact of Acute and Chronic Exercise on Immunoglobulins and Cytokines in Elderly: Insights From a Critical Review of the Literature
Sellami, M., Bragazzi, N. L., Aboghaba, B., & Elrayess, M. A. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.631873 · Cited by 61 · see citing works
Buttons and Zippers: Endothelial Junctions in Lymphatic VesselsPreprint
Bałuk, P., & McDonald, D. M. (2022) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a041178 · Cited by 61 · see citing works
The novel role of lymphatic vessels in the pathogenesis of ocular diseases.
Clahsen, T., Hadrian, K., Notara, M., Schlereth, S., Howaldt, A., Prokosch, V., Volatier, T. L. A., Hos, D., Schroedl, F., Kaser-Eichberger, A., et al. (2023) · Progress in retinal and eye research · doi:10.1016/j.preteyeres.2022.101157 · Cited by 51 · see citing works
Restoration of cervical lymphatic vessel function in aging rescues cerebrospinal fluid drainage
Du, T., Raghunandan, A., Mestre, H., Plá, V., Liu, G., Ladrón-de-Guevara, A., Newbold, E. J., Tobin, P., Gahn‐Martinez, D., Pattanayak, S., et al. (2024) · Nature Aging · doi:10.1038/s43587-024-00691-3 · Cited by 53 · see citing works
Fluid flow to mimic organ function in 3D in vitro models
Juste-Lanas, Y., Hervás-Raluy, S., García‐Aznar, J. M., & González‐Loyola, A. (2023) · APL Bioengineering · doi:10.1063/5.0146000 · Cited by 50 · see citing works
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Clinical Potential of Adrenomedullin Signaling in the Cardiovascular System
Bálint, L., Nelson-Maney, N., Tian, Y., Serafin, S. D., & Caron, K. M. (2023) · Circulation Research · doi:10.1161/circresaha.123.321673 · Cited by 48 · see citing works
Molecular and metabolic orchestration of the lymphatic vasculature in physiology and pathology
Montenegro-Navarro, N., García-Báez, C., & García‐Caballero, M. (2023) · Nature Communications · doi:10.1038/s41467-023-44133-x · Cited by 45 · see citing works
Role of Gut Microbial Metabolites in Cardiovascular Diseases—Current Insights and the Road Ahead
Datta, S., Pasham, S., Sandeep, I. S., Boini, K. M., & Koka, S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms251810208 · Cited by 42 · see citing works
Transport and Immune Functions of the Lymphatic System.
Davis, M. J., Zawieja, S. D., & King, P. D. (2025) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022724-104908 · Cited by 42 · see citing works
Mechanosensitive ACKR4 scavenges CCR7 chemokines to facilitate T cell de-adhesion and passive transport by flow in inflamed afferent lymphatics
Friess, M. C., Kritikos, I., Schineis, P., Medina-Sanchez, J. D., Gkountidi, A., Vallone, A., Sigmund, E. C., Schwitter, C., Vranova, M., Matti, C., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110334 · Cited by 38 · see citing works
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Contribution of MicroRNA ‐27b‐3p to Synovial Fibrotic Responses in Knee Osteoarthritis
Tavallaee, G., Lively, S. S., Rockel, J. S., Ali, S. A., Im, M., Sarda, C., Mitchell, G. M., Rossomacha, E., Nakamura, S., Potla, P., et al. (2022) · Arthritis & Rheumatology · doi:10.1002/art.42285 · Cited by 38 · see citing works
The association between the gut microbiota metabolite trimethylamine N-oxide and heart failure
Jarmukhanov, Z., Mukhanbetzhanov, N., Kozhakhmetov, S., Nurgaziyev, M., Sailybayeva, A., Bekbossynova, M. S., & Kushugulova, A. R. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1440241 · Cited by 34 · see citing works
Transport functions of intestinal lymphatic vessels
Tso, P., Bernier‐Latmani, J., Petrova, T. V., & Liu, M. (2024) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-024-00996-z · Cited by 33 · see citing works
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The nasal lymphatic route of CSF outflow: implications for neurodegenerative disease diagnosis and monitoring
Chae, J., Choi, M., Choi, J., & Yoo, S. (2024) · Animal Cells and Systems · doi:10.1080/19768354.2024.2307559 · Cited by 29 · see citing works
Targeting synovial lymphatic function as a novel therapeutic intervention for age-related osteoarthritis in mice
Lin, X., Bell, R. D., Catheline, S., Takano, T., McDavid, A., Jonason, J. H., Schwarz, E., & Xing, L. (2023) · Arthritis & Rheumatology · doi:10.1002/art.42441 · Cited by 29 · see citing works
Mechanosensation and Mechanotransduction by Lymphatic Endothelial Cells Act as Important Regulators of Lymphatic Development and Function
Bálint, L., & Jakus, Z. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22083955 · Cited by 26 · see citing works
Physiological models for in vivo imaging and targeting the lymphatic system: Nanoparticles and extracellular vesicles
Olmeda, D., Cerezo‐Wallis, D., Castellano‐Sanz, E., Garcı́a-Silva, S., Peinado, H., & Soengas, M. S. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.113833 · Cited by 26 · see citing works
Aging-induced changes in lymphatic muscle cell transcriptomes are associated with reduced pumping of peripheral collecting lymphatic vessels in mice
Lei, P., Ruscic, K. J., Roh, K., Rajotte, J. J., O’Melia, M. J., Bouta, E. M., Marquez, M., Pereira, E. R., Kumar, A. S., Razavi, M. S., et al. (2023) · Developmental Cell · doi:10.1016/j.devcel.2024.12.010 · Cited by 25 · see citing works
Lessons of Vascular Specialization From Secondary Lymphoid Organ Lymphatic Endothelial Cells
Arroz‐Madeira, S., Bekkhus, T., Ulvmar, M. H., & Petrova, T. V. (2023) · Circulation Research · doi:10.1161/circresaha.123.322136 · Cited by 25 · see citing works
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Mechanosensitive mTORC1 signaling maintains lymphatic valves
Saygili Demir, C., Sabine, A., Gong, M., Dormond, O., & Petrova, T. V. (2023) · Journal of Cell Biology · doi:10.1083/jcb.202207049 · Cited by 24 · see citing works
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Self-citation

Authors: González-Loyola, A., & Petrova, T. V.
Affiliations: Ludwig Cancer Research (CH)
Corresponding author: Petrova, Tatiana V.
ORCID: Petrova, Tatiana V.
Venue: Advanced Drug Delivery Reviews
Publisher: Elsevier BV
Published: 2021-02
Volume: 169
Pages: 63-78
ISSN: 0169-409X (ISSN-L)
DOI: 10.1016/j.addr.2020.12.005
OpenAlex: W3111301980
Cited by: 89
References: 265
Citations by year: 2026: 8 · 2025: 17 · 2024: 24 · 2023: 20 · 2022: 9 · 2021: 11
FWCI: 1.07
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: Advanced Drug Delivery Reviews (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
IRIS (submittedVersion)
SERVAL (Université de Lausanne) (submittedVersion)
Funders: Swiss National Science Foundation (CRSII5_177191, 31ER30_160674, 31003A-156266, CRSK-3_190200)
Swiss Cancer League (KFS-4895-08-2019)
European Union's Horizon 2020 (847939)
Topics: Health Sciences › Medicine › Oncology › Lymphatic System and Diseases
Health Sciences › Medicine › Surgery › Lymphatic Disorders and Treatments
Health Sciences › Medicine › Surgery › Vascular Malformations and Hemangiomas
Keywords: lymphatic development, lymphangiogenesis, fluid homeostasis, immune surveillance, dietary fat absorption
MeSH terms: Aging, Animals, Humans, Lymphangiogenesis, Lymphatic Vessels

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