Lymphangiogenesis in post-natal tissue remodeling: Lymphatic endothelial cell connection with its environment

Paupert, Jenny; Sounni, Nor Eddine; Noël, Agnès

doi:10.1016/j.mam.2011.04.002

Cited by 57 publications

(50 citation statements)

References 143 publications

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“…Lymphangiogenesis takes place under certain pathological situations, including inflammation and tissue repair (7). Upon initiation of inflammation, the lymphatic system is activated and both the extranodal lymphatic vessels at peripheral tissues and the intranodal lymphatic vessels display exuberant growth and vigorously expand in response to inflammatory stimuli (5).…”

Section: Ialmentioning

confidence: 99%

“…In this sense, under inflammatory conditions, the demand for efficient lymphatic drainage increases. Accumulating evidence suggests inflammation-associated lymphangiogenesis (IAL) is not merely an endpoint phenotype of inflammation but rather a dynamic, context-dependent reaction that can alter the natural course of the inflammatory process and/or tissue repair (3,6,7). IAL can profoundly influence the symptomatic presentation of inflammation; for example, lymphatic vessels play a role in regulating tissue fluid clearance (8,9) and macrophage/DC recruitment (10,11).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Inflammation-associated lymphangiogenesis: a double-edged sword?

Kim¹,

Kataru²,

Koh³

2014

J. Clin. Invest.

190

146

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Lymphangiogenesis and lymphatic vessel remodeling are complex biological processes frequently observed during inflammation. Accumulating evidence indicates that inflammation-associated lymphangiogenesis (IAL) is not merely an endpoint event, but actually a phenomenon actively involved in the pathophysiology of various inflammatory disorders. The VEGF-C/VEGFR-3 and VEGF-A/VEGF-R2 signaling pathways are two of the best-studied pathways in IAL. Methods targeting these molecules, such as prolymphangiogenic or antilymphatic treatments, were found to be beneficial in various preclinical and/or clinical studies. This Review focuses on the most recent achievements in the fields of lymphatic biology relevant to inflammatory conditions. Additionally, preclinical and clinical therapies that modulate IAL are summarized.

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Section: Ialmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Inflammation-associated lymphangiogenesis: a double-edged sword?

Kim¹,

Kataru²,

Koh³

2014

J. Clin. Invest.

190

146

View full text Add to dashboard Cite

show abstract

“…As reflected by its cardinal signs (namely redness, pain, heat, swelling, and loss of function), inflammation is frequently an extremely dynamic and violent process [4,5]. Lymphangiogenesis is often observed amid various types of inflammation, and accumulating evidence implies that LVs are directly and/or indirectly associated with inflammatory and/or repair processes [1,6,7].…”

Section: Reciprocal Control Of Inflammation and Lymphangiogenesismentioning

confidence: 99%

“…In adulthood, lymphangiogenesis is known to occur only during certain pathological circumstances such as tissue repair, inflammation and tumor-related conditions [7]. Lymphangiogenesis was previously thought to only proceed via sprouting of pre-existing LVs.…”

Section: Normal Lymphangiogenesis During Development and Adulthoodmentioning

confidence: 99%

Regulation and implications of inflammatory lymphangiogenesis

Kim

Kataru

Koh

2012

Trends in Immunology

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“…Lymphatic endothelial cells (LECs) interact intimately with the adjacent interstitial matrix and attach to it through anchorage filaments. 9,10 Therefore, LECs sprouting from preexisting vessels and their migration through the ECM require that they be able to negotiate an interstitial collagen barrier mainly composed of fibrillar type I collagen. Recently, evidence has accumulated demonstrating that integrins, by promoting cell-matrix interaction, influence normal lymphatic function and lymphangiogenesis.…”

Section: Introductionmentioning

confidence: 99%

Matrix metalloproteinase-2 governs lymphatic vessel formation as an interstitial collagenase

Detry

Erpicum

Paupert

et al. 2012

Blood

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Lymphatic dysfunctions are associated with several human diseases, including lymphedema and metastatic spread of cancer. Although it is well recognized that lymphatic capillaries attach directly to interstitial matrix mainly composed of fibrillar type I collagen, the interactions occurring between lymphatics and their surrounding matrix have been overlooked. In this study, we demonstrate how matrix metalloproteinase (MMP)-2 drives lymphatic morphogenesis through Mmp2-gene ablation in mice, mmp2 knockdown in zebrafish and in 3D-culture systems, and through MMP2 inhibition. In all models used in vivo (3 murine models and thoracic duct development in zebrafish) and in vitro (lymphatic ring and spheroid assays), MMP2 blockage or down-regulation leads to reduced lymphangiogenesis or altered vessel branching. Our data show that lymphatic endothelial cell (LEC) migration through collagen fibers is affected by physical matrix constraints (matrix composition, density, and crosslinking). Transmission electron microscopy and confocal reflection microscopy using DQ-collagen highlight the contribution of MMP2 to mesenchymal-like migration of LECs associated with collagen fiber remodeling. Our findings provide new mechanistic insight into how LECs negotiate an interstitial type I collagen barrier and reveal an unexpected MMP2-driven collagenolytic pathway for lymphatic vessel formation and morphogenesis. (Blood. 2012;119(21):5048-5056) IntroductionLymphatic vessels are essential for body fluid balance and immunologic surveillance. Several pathologies manifest abnormal lymphatic vessel growth (lymphangiogenesis), either excessive (inflammatory diseases, tumor metastases, cornea-graft rejection) or defective (lymphedema). [1][2][3] Our understanding of the molecular mechanisms underlying lymphangiogenesis is still in its infancy. Although several key molecular determinants (vascular endothelial growth factor [VEGF]-C/D, VEGF receptor-3, angiopoietin, ephrins, integrins, etc) have been identified, 2,4-7 the importance of cell-matrix interactions during the lymphangiogenic process is not well documented.One of the features that discriminates lymphatic capillaries from blood capillaries is the kind of extracellular matrix (ECM) to which each vessel type is exposed in its natural environment. Blood vascular endothelium is in direct contact with basement membrane components (laminin, type IV collagen), 8 whereas the basal lamina is largely absent in lymphatic capillaries. Lymphatic endothelial cells (LECs) interact intimately with the adjacent interstitial matrix and attach to it through anchorage filaments. 9,10 Therefore, LECs sprouting from preexisting vessels and their migration through the ECM require that they be able to negotiate an interstitial collagen barrier mainly composed of fibrillar type I collagen. Recently, evidence has accumulated demonstrating that integrins, by promoting cell-matrix interaction, influence normal lymphatic function and lymphangiogenesis. 5,10,11 How LECs deal with fibrillar collagens to migrate an...

show abstract

Lymphangiogenesis in post-natal tissue remodeling: Lymphatic endothelial cell connection with its environment

Cited by 57 publications

References 143 publications

Inflammation-associated lymphangiogenesis: a double-edged sword?

Inflammation-associated lymphangiogenesis: a double-edged sword?

Regulation and implications of inflammatory lymphangiogenesis

Matrix metalloproteinase-2 governs lymphatic vessel formation as an interstitial collagenase

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