Intussusceptive Vascular Remodeling Precedes Pathological Neovascularization

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Intussusceptive Vascular Remodeling Precedes Pathological Neovascularization

Ali, Zaheer (author): Linköpings universitet,Avdelningen för kardiovaskulär medicin,Medicinska fakulteten

Mukwaya, Anthonny (author): Linköpings universitet,Avdelningen för neuro- och inflammationsvetenskap,Medicinska fakulteten

Biesemeier, Antje (author): Univ Tubingen, Germany

Ntzouni, Maria (author): Linköpings universitet,Avdelningen för cellbiologi,Medicinska fakulteten

Ramskold, Daniel (author): Karolinska Institutet,Karolinska Inst, Sweden

Giatrellis, Sarantis (author): Karolinska Institutet,Karolinska Inst, Sweden

Mammadzada, Parviz (author): Karolinska Institutet,Karolinska Inst, Sweden

Cao, Renhai (author): Karolinska Inst, Sweden

Lennikov, Anton (author): Linköpings universitet,Avdelningen för neuro- och inflammationsvetenskap,Medicinska fakulteten,Univ Missouri, MO 65211 USA

Marass, Michele (author): Max Planck Inst Lung and Heart Res, Germany

Gerri, Claudia (author): Max Planck Inst Lung and Heart Res, Germany

Hildesjö, Camilla (author): Linköpings universitet,Avdelningen för Kirurgi, Ortopedi och Onkologi,Medicinska fakulteten,Region Östergötland, Klinisk patologi

Taylor, Michael (author): Univ Wisconsin, WI 53706 USA

Deng, Qiaolin (author): Karolinska Institutet,Karolinska Inst, Sweden

Peebo, Beatrice (author): Linköpings universitet,Avdelningen för neuro- och inflammationsvetenskap,Medicinska fakulteten,Region Östergötland, Ögonkliniken US,Bayer AB, Sweden

del Peso, Luis (author): Universidad Autónoma de Madrid, Spain; Instituto de Investigaciones Biomédicas Alberto Sols, CSIC-UAM Madrid, Spain

Kvanta, Anders (author): Karolinska Institutet,Karolinska Inst, Sweden

Sandberg, Rickard (author): Karolinska Institutet,Karolinska Inst, Sweden

Schraermeyer, Ulrich (author): Univ Tubingen, Germany

Andre, Helder (author): Karolinska Institutet,Karolinska Inst, Sweden

Steffensen, John F. (author): Univ Copenhagen, Denmark

Lagali, Neil (author): Linköpings universitet,Avdelningen för neuro- och inflammationsvetenskap,Medicinska fakulteten,Region Östergötland, Ögonkliniken US

Cao, Yihai (author): Karolinska Institutet,Karolinska Inst, Sweden

Kele, Julianna (author): Karolinska Institutet,Karolinska Inst, Sweden

Jensen, Lasse (author): Linköpings universitet,Avdelningen för kardiovaskulär medicin,Medicinska fakulteten,Region Östergötland, Klinisk farmakologi,Univ Autonoma Madrid, Spain; UAM, Spain

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Lippincott Williams & Wilkins, 2019
2019
English.
In: Arteriosclerosis, Thrombosis and Vascular Biology. - : Lippincott Williams & Wilkins. - 1079-5642 .- 1524-4636. ; 39:7, s. 1402-1418

Related links:: https://liu.diva-por... (primary) (Raw object); show more...; https://urn.kb.se/re...; https://doi.org/10.1...; http://kipublication...; show less...

Journal article (peer-reviewed)

Abstract Subject headings

Objective—Pathological neovascularization is crucial for progression and morbidity of serious diseases such as cancer, diabetic retinopathy, and age-related macular degeneration. While mechanisms of ongoing pathological neovascularization have been extensively studied, the initiating pathological vascular remodeling (PVR) events, which precede neovascularization remains poorly understood. Here, we identify novel molecular and cellular mechanisms of preneovascular PVR, by using the adult choriocapillaris as a model.Approach and Results—Using hypoxia or forced overexpression of VEGF (vascular endothelial growth factor) in the subretinal space to induce PVR in zebrafish and rats respectively, and by analyzing choriocapillaris membranes adjacent to choroidal neovascular lesions from age-related macular degeneration patients, we show that the choriocapillaris undergo robust induction of vascular intussusception and permeability at preneovascular stages of PVR. This PVR response included endothelial cell proliferation, formation of endothelial luminal processes, extensive vesiculation and thickening of the endothelium, degradation of collagen fibers, and splitting of existing extravascular columns. RNA-sequencing established a role for endothelial tight junction disruption, cytoskeletal remodeling, vesicle- and cilium biogenesis in this process. Mechanistically, using genetic gain- and loss-of-function zebrafish models and analysis of primary human choriocapillaris endothelial cells, we determined that HIF (hypoxia-induced factor)-1α-VEGF-A-VEGFR2 signaling was important for hypoxia-induced PVR.Conclusions—Our findings reveal that PVR involving intussusception and splitting of extravascular columns, endothelial proliferation, vesiculation, fenestration, and thickening is induced before neovascularization, suggesting that identifying and targeting these processes may prevent development of advanced neovascular disease in the future.Visual Overview—An online visual overview is available for this article.

Subject headings

MEDICIN OCH HÄLSOVETENSKAP -- Medicinska och farmaceutiska grundvetenskaper -- Cell- och molekylärbiologi (hsv//swe)
MEDICAL AND HEALTH SCIENCES -- Basic Medicine -- Cell and Molecular Biology (hsv//eng)

Keyword

choroidal neovascularization; hypoxia; intussusception; macular degeneration; zebrafish

Publication and Content Type

ref (subject category)
art (subject category)

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MEDICAL AND HEALTH SCIENCES: MEDICAL AND HEAL ...; and Basic Medicine; and Cell and Molecul ...

Articles in the publication: Arteriosclerosis ...

By the university: Linköping University; Karolinska Institutet

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