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Rab35 governs apicobasal polarity through regulation of actin dynamics during sprouting angiogenesis

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  • Caitlin R. Francis

    (University of Denver)

  • Hayle Kincross

    (University of Denver)

  • Erich J. Kushner

    (University of Denver)

Abstract

In early blood vessel development, trafficking programs, such as those using Rab GTPases, are tasked with delivering vesicular cargo with high spatiotemporal accuracy. However, the function of many Rab trafficking proteins remain ill-defined in endothelial tissue; therefore, their relevance to blood vessel development is unknown. Rab35 has been shown to play an enigmatic role in cellular behaviors which differs greatly between tissue-type and organism. Importantly, Rab35 has never been characterized for its potential contribution in sprouting angiogenesis; thus, our goal was to map Rab35’s primary function in angiogenesis. Our results demonstrate that Rab35 is critical for sprout formation; in its absence, apicobasal polarity is entirely lost in vitro and in vivo. To determine mechanism, we systematically explored established Rab35 effectors and show that none are operative in endothelial cells. However, we find that Rab35 partners with DENNd1c, an evolutionarily divergent guanine exchange factor, to localize to actin. Here, Rab35 regulates actin polymerization through limiting Rac1 and RhoA activity, which is required to set up proper apicobasal polarity during sprout formation. Our findings establish that Rab35 is a potent brake of actin remodeling during blood vessel development.

Suggested Citation

  • Caitlin R. Francis & Hayle Kincross & Erich J. Kushner, 2022. "Rab35 governs apicobasal polarity through regulation of actin dynamics during sprouting angiogenesis," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32853-5
    DOI: 10.1038/s41467-022-32853-5
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    1. Ilkka Paatero & Loïc Sauteur & Minkyoung Lee & Anne K. Lagendijk & Daniel Heutschi & Cora Wiesner & Camilo Guzmán & Dimitri Bieli & Benjamin M. Hogan & Markus Affolter & Heinz-Georg Belting, 2018. "Junction-based lamellipodia drive endothelial cell rearrangements in vivo via a VE-cadherin-F-actin based oscillatory cell-cell interaction," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    2. Igor Kondrychyn & Douglas J. Kelly & Núria Taberner Carretero & Akane Nomori & Kagayaki Kato & Jeronica Chong & Hiroyuki Nakajima & Satoru Okuda & Naoki Mochizuki & Li-Kun Phng, 2020. "Marcksl1 modulates endothelial cell mechanoresponse to haemodynamic forces to control blood vessel shape and size," Nature Communications, Nature, vol. 11(1), pages 1-18, December.
    3. Kerstin Klinkert & Murielle Rocancourt & Anne Houdusse & Arnaud Echard, 2016. "Rab35 GTPase couples cell division with initiation of epithelial apico-basal polarity and lumen opening," Nature Communications, Nature, vol. 7(1), pages 1-13, September.
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