Vasohibin 1 Selectively Regulates Secondary Sprouting and Lymphangiogenesis in the Zebrafish Trunk

Overview

Journal Development

Specialty Biology

Date 2021 Feb 6

PMID 33547133

Citations 5

Authors

Marta Bastos de Oliveira

Katja Meier

Simone Jung

Eireen Bartels-Klein

Baptiste Coxam

Ilse Geudens

Anna Szymborska

Renae Skoczylas

Ines Fechner

Katarzyna Koltowska

Holger Gerhardt

Affiliations

Soon will be listed here.

Abstract

Previous studies have shown that Vasohibin 1 (Vash1) is stimulated by VEGFs in endothelial cells and that its overexpression interferes with angiogenesis Recently, Vash1 was found to mediate tubulin detyrosination, a post-translational modification that is implicated in many cell functions, such as cell division. Here, we used the zebrafish embryo to investigate the cellular and subcellular mechanisms of Vash1 on endothelial microtubules during formation of the trunk vasculature. We show that microtubules within venous-derived secondary sprouts are strongly and selectively detyrosinated in comparison with other endothelial cells, and that this difference is lost upon knockdown. Vash1 depletion in zebrafish specifically affected secondary sprouting from the posterior cardinal vein, increasing endothelial cell divisions and cell number in the sprouts. We show that altering secondary sprout numbers and structure upon depletion leads to defective lymphatic vessel formation and ectopic lymphatic progenitor specification in the zebrafish trunk.

Citing Articles

Tubulin tyrosination/detyrosination regulate the affinity and sorting of intraflagellar transport trains on axonemal microtubule doublets.

Chhatre A, Stepanek L, Nievergelt A, Alvarez Viar G, Diez S, Pigino G Nat Commun. 2025; 16(1):1055.

PMID: 39865093 PMC: 11770126. DOI: 10.1038/s41467-025-56098-0.

Zmiz1 is a novel regulator of lymphatic endothelial cell gene expression and function.

K C R, Patel N, Shenoy A, Scallan J, Chiang M, Galazo M PLoS One. 2024; 19(5):e0302926.

PMID: 38718095 PMC: 11078365. DOI: 10.1371/journal.pone.0302926.

The cytoskeleton adaptor protein Sorbs1 controls the development of lymphatic and venous vessels in zebrafish.

Veloso A, Bleuart A, Conrard L, Orban T, Bruyr J, Cabochette P BMC Biol. 2024; 22(1):51.

PMID: 38414014 PMC: 10900589. DOI: 10.1186/s12915-024-01850-z.

Lymphatic vessel: origin, heterogeneity, biological functions, and therapeutic targets.

Hu Z, Zhao X, Wu Z, Qu B, Yuan M, Xing Y Signal Transduct Target Ther. 2024; 9(1):9.

PMID: 38172098 PMC: 10764842. DOI: 10.1038/s41392-023-01723-x.

Identification and validation of key genes associated with atrial fibrillation in the elderly.

Liu C, Zeng J, Wu J, Wang J, Wang X, Yao M Front Cardiovasc Med. 2023; 10:1118686.

PMID: 37063972 PMC: 10090400. DOI: 10.3389/fcvm.2023.1118686.

References

Baek S, Oh T, Secker G, Sutton D, Okuda K, Paterson S . The Alternative Splicing Regulator Nova2 Constrains Vascular Erk Signaling to Limit Specification of the Lymphatic Lineage. Dev Cell. 2019; 49(2):279-292.e5. DOI: 10.1016/j.devcel.2019.03.017. View

Hogan B, Herpers R, Witte M, Helotera H, Alitalo K, Duckers H . Vegfc/Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries. Development. 2009; 136(23):4001-9. DOI: 10.1242/dev.039990. View

Akera T, Chmatal L, Trimm E, Yang K, Aonbangkhen C, Chenoweth D . Spindle asymmetry drives non-Mendelian chromosome segregation. Science. 2017; 358(6363):668-672. PMC: 5906099. DOI: 10.1126/science.aan0092. View

Kimmel C, Ballard W, Kimmel S, Ullmann B, Schilling T . Stages of embryonic development of the zebrafish. Dev Dyn. 1995; 203(3):253-310. DOI: 10.1002/aja.1002030302. View

Sanchez-Pulido L, Ponting C . Vasohibins: new transglutaminase-like cysteine proteases possessing a non-canonical Cys-His-Ser catalytic triad. Bioinformatics. 2016; 32(10):1441-5. PMC: 4866520. DOI: 10.1093/bioinformatics/btv761. View

Laloraya S . Asymmetric Tyrosination of Spindle Microtubules Facilitates Selfish Inheritance. Trends Cell Biol. 2018; 28(6):417-419. DOI: 10.1016/j.tcb.2018.03.005. View

Vale R . The molecular motor toolbox for intracellular transport. Cell. 2003; 112(4):467-80. DOI: 10.1016/s0092-8674(03)00111-9. View

Hogan B, Schulte-Merker S . How to Plumb a Pisces: Understanding Vascular Development and Disease Using Zebrafish Embryos. Dev Cell. 2017; 42(6):567-583. DOI: 10.1016/j.devcel.2017.08.015. View

Hoshijima K, Jurynec M, Shaw D, Jacobi A, Behlke M, Grunwald D . Highly Efficient CRISPR-Cas9-Based Methods for Generating Deletion Mutations and F0 Embryos that Lack Gene Function in Zebrafish. Dev Cell. 2019; 51(5):645-657.e4. PMC: 6891219. DOI: 10.1016/j.devcel.2019.10.004. View

10.

Chang W, Webster D, Salam A, Gruber D, Prasad A, Eiserich J . Alteration of the C-terminal amino acid of tubulin specifically inhibits myogenic differentiation. J Biol Chem. 2002; 277(34):30690-8. DOI: 10.1074/jbc.M204930200. View

11.

Schwartz E . Antivascular actions of microtubule-binding drugs. Clin Cancer Res. 2009; 15(8):2594-601. PMC: 2745203. DOI: 10.1158/1078-0432.CCR-08-2710. View

12.

Tozer G, Kanthou C, Parkins C, Hill S . The biology of the combretastatins as tumour vascular targeting agents. Int J Exp Pathol. 2002; 83(1):21-38. PMC: 2517662. DOI: 10.1046/j.1365-2613.2002.00211.x. View

13.

Nicenboim J, Malkinson G, Lupo T, Asaf L, Sela Y, Mayseless O . Lymphatic vessels arise from specialized angioblasts within a venous niche. Nature. 2015; 522(7554):56-61. DOI: 10.1038/nature14425. View

14.

Potente M, Gerhardt H, Carmeliet P . Basic and therapeutic aspects of angiogenesis. Cell. 2011; 146(6):873-87. DOI: 10.1016/j.cell.2011.08.039. View

15.

Liao S, Rajendraprasad G, Wang N, Eibes S, Gao J, Yu H . Molecular basis of vasohibins-mediated detyrosination and its impact on spindle function and mitosis. Cell Res. 2019; 29(7):533-547. PMC: 6796878. DOI: 10.1038/s41422-019-0187-y. View

16.

Kuchler A, Gjini E, Peterson-Maduro J, Cancilla B, Wolburg H, Schulte-Merker S . Development of the zebrafish lymphatic system requires VEGFC signaling. Curr Biol. 2006; 16(12):1244-8. DOI: 10.1016/j.cub.2006.05.026. View

17.

Shin M, Male I, Beane T, Villefranc J, Kok F, Zhu L . Vegfc acts through ERK to induce sprouting and differentiation of trunk lymphatic progenitors. Development. 2016; 143(20):3785-3795. PMC: 5087638. DOI: 10.1242/dev.137901. View

18.

Shi Y, Yuan W, Wang X, Gong J, Zhu S, Chai L . Combretastatin A-4 efficiently inhibits angiogenesis and induces neuronal apoptosis in zebrafish. Sci Rep. 2016; 6:30189. PMC: 4958954. DOI: 10.1038/srep30189. View

19.

Yaniv K, Isogai S, Castranova D, Dye L, Hitomi J, Weinstein B . Live imaging of lymphatic development in the zebrafish. Nat Med. 2006; 12(6):711-6. DOI: 10.1038/nm1427. View

20.

Habeck H, Odenthal J, Walderich B, Maischein H, Schulte-Merker S . Analysis of a zebrafish VEGF receptor mutant reveals specific disruption of angiogenesis. Curr Biol. 2002; 12(16):1405-12. DOI: 10.1016/s0960-9822(02)01044-8. View