Planar cell polarity genes frizzled4 and frizzled6 exert patterning influence on arterial vessel morphogenesis

PLoS ONE

Volumn 12, Issue 3, 2017, Pages

  Markovic, Rene ^a   Peltan, Julien ^b,c,d   Gosak, Marko ^a   Horvat, Denis ^a   Zalik, Borut ^a   Seguy, Benjamin ^b,d   Chauvel, Remi ^b,d   Malandain, Gregoire ^e   Couffinhal, Thierry ^b,c,d   Duplàa, Cecile ^b   Marhl, Marko ^a   Roux, Etienne ^b,c  

^a UNIVERSITY OF MARIBOR   (Slovenia)

^b Bordeaux Segalen University   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d BORDEAUX UNIVERSITY HOSPITAL   (France)

^e INRIA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARTERIOLE; ARTICLE; BLOOD VESSEL DIAMETER; CELL POLARITY; CONTROLLED STUDY; EMBRYO; FRIZZLED4 GENE; FRIZZLED6 GENE; GENE; GENE DELETION; GENE FUNCTION; GENE MUTATION; IMAGE PROCESSING; IMAGE RECONSTRUCTION; KIDNEY ARTERY; KIDNEY BLOOD VESSEL; MICRO-COMPUTED TOMOGRAPHY; MORPHOGENESIS; MOUSE; NONHUMAN; VASCULAR RESISTANCE; ANATOMY AND HISTOLOGY; ANGIOGENESIS; ANIMAL; ARTERY; DIAGNOSTIC IMAGING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

FRIZZLED PROTEIN; FZD4 PROTEIN, MOUSE; FZD6 PROTEIN, MOUSE;

ANIMALS; ARTERIES; CELL POLARITY; FRIZZLED RECEPTORS; MICE; MORPHOGENESIS; NEOVASCULARIZATION, PHYSIOLOGIC; X-RAY MICROTOMOGRAPHY;

EID: 85014483735     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0171033     Document Type: Article

References (54)

1. Cassot F, Lauwers F, Fouard C, Prohaska S, Lauwers-Cances V. A novel three-dimensional computer-assisted method for a quantitative study of microvascular networks of the human cerebral cortex. Micro-circulation. 2006; 13(1):1-18. doi: 10.1080/10739680500383407 PMID: 16393942
2. Zagorchev L, Oses P, Zhuang ZW, Moodie K, Mulligan-Kehoe MJ, Simons M, et al. Micro computed tomography for vascular exploration. J Angiogenes Res. 2010; 2:7. doi: 10.1186/2040-2384-2-7 PMID: 20298533
3. Leroux L, Descamps B, Tojais NF, Seguy B, Oses P, Moreau C, et al. Hypoxia preconditioned mesenchymal stem cells improve vascular and skeletal muscle fiber regeneration after ischemia through a Wnt4-dependent pathway. Mol Ther. 2010; 18(8):1545-52.
4. Descamps B, Sewduth R, Ferreira Tojais N, Jaspard B, Reynaud A, Sohet F, et al. Frizzled 4 regulates arterial network organization through noncanonical Wnt/planar cell polarity signaling. Circ Res. 2012; 110(1):47-58. doi: 10.1161/CIRCRESAHA.111.250936 PMID: 22076635
5. Dufourcq P, Leroux L, Ezan J, Descamps B, Lamaziere JM, Costet P, et al. Regulation of endothelial cell cytoskeletal reorganization by a secreted frizzled-related protein-1 and frizzled 4-and frizzled 7-dependent pathway: role in neovessel formation. Am J Pathol. 2008; 172(1):37-49. PMID: 18156211
6. Keller R, Shook D, Skoglund P. The forces that shape embryos: physical aspects of convergent extension by cell intercalation. Phys Biol. 2008; 5(1):015007. PMID: 18403829
7. Kuhl M, Geis K, Sheldahl LC, Pukrop T, Moon RT, Wedlich D. Antagonistic regulation of convergent extension movements in Xenopus by Wnt/beta-catenin and Wnt/Ca2+ signaling. Mech Dev. 2001; 106 (1-2):61-76. PMID: 11472835
8. Mlodzik M. Planar cell polarization: do the same mechanisms regulate Drosophila tissue polarity and vertebrate gastrulation? Trends Genet. 2002; 18(11):564-71. PMID: 12414186
9. Masckauchan TN, Kitajewski J. Wnt/Frizzled signaling in the vasculature: new angiogenic factors in sight. Physiology (Bethesda). 2006; 21:181-8.
10. Rao TP, Kuhl M. An updated overview on Wnt signaling pathways: a prelude for more. Circ Res. 2010; 106(12):1798-806. doi: 10.1161/CIRCRESAHA.110.219840 PMID: 20576942
11. Zerlin M, Julius MA, Kitajewski J. Wnt/Frizzled signaling in angiogenesis. Angiogenesis. 2008; 11 (1):63-9. doi: 10.1007/s10456-008-9095-3 PMID: 18253847
12. Sewduth RN, Jaspard-Vinassa B, Peghaire C, Guillabert A, Franzl N, Larrieu-Lahargue F, et al. The ubi-quitin ligase PDZRN3 is required for vascular morphogenesis through Wnt/planar cell polarity signalling. Nat Commun. 2014; 5:4832. doi: 10.1038/ncomms5832 PMID: 25198863
13. Stark MR, Rao MS, Schoenwolf GC, Yang G, Smith D, Mauch TJ. Frizzled-4 expression during chick kidney development. Mech Dev. 2000; 98(1-2):121-5. PMID: 11044615
14. Xu Q, Wang Y, Dabdoub A, Smallwood PM, Williams J, Woods C, et al. Vascular development in the retina and inner ear: control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair. Cell. 2004; 116(6):883-95. PMID: 15035989
15. Paes KT, Wang E, Henze K, Vogel P, Read R, Suwanichkul A, et al. Frizzled 4 is required for retinal angiogenesis and maintenance of the blood-retina barrier. Invest Ophthalmol Vis Sci. 2011; 52 (9):6452-61. doi: 10.1167/iovs.10-7146 PMID: 21743011
16. Chen Y, Zhang Y, Tang J, Liu F, Hu Q, Luo C, et al. Norrin protected blood-brain barrier via frizzled-4/beta-catenin pathway after subarachnoid hemorrhage in rats. Stroke. 2015; 46(2):529-36. doi: 10.1161/STROKEAHA.114.007265 PMID: 25550365
17. Wang Y, Rattner A, Zhou Y, Williams J, Smallwood PM, Nathans J. Norrin/Frizzled4 signaling in retinal vascular development and blood brain barrier plasticity. Cell. 2012; 151(6):1332-44. doi: 10.1016/j.cell. 2012.10.042 PMID: 23217714
18. Ye X, Wang Y, Cahill H, Yu M, Badea TC, Smallwood PM, et al. Norrin, frizzled-4, and Lrp5 signaling in endothelial cells controls a genetic program for retinal vascularization. Cell. 2009; 139(2):285-98. doi: 10.1016/j.cell.2009.07.047 PMID: 19837032
19. Junge HJ, Yang S, Burton JB, Paes K, Shu X, French DM, et al. TSPAN12 regulates retinal vascular development by promoting Norrin-but not Wnt-induced FZD4/beta-catenin signaling. Cell. 2009; 139 (2):299-311. doi: 10.1016/j.cell.2009.07.048 PMID: 19837033
20. Kilander MB, Dahlstrom J, Schulte G. Assessment of Frizzled 6 membrane mobility by FRAP supports G protein coupling and reveals WNT-Frizzled selectivity. Cell Signal. 2014; 26(9):1943-9. doi: 10.1016/j.cellsig.2014.05.012 PMID: 24873871
21. Kilander MB, Petersen J, Andressen KW, Ganji RS, Levy FO, Schuster J, et al. Disheveled regulates precoupling of heterotrimeric G proteins to Frizzled 6. Faseb J. 2014; 28(5):2293-305. doi: 10.1096/fj. 13-246363 PMID: 24500924
22. Lyons JP, Mueller UW, Ji H, Everett C, Fang X, Hsieh JC, et al. Wnt-4 activates the canonical beta-cate-nin-mediated Wnt pathway and binds Frizzled-6 CRD: functional implications of Wnt/beta-catenin activity in kidney epithelial cells. Exp Cell Res. 2004; 298(2):369-87. doi: 10.1016/j.yexcr.2004.04.036 PMID: 15265686
23. Golan T, Yaniv A, Bafico A, Liu G, Gazit A. The human Frizzled 6 (HFz6) acts as a negative regulator of the canonical Wnt. beta-catenin signaling cascade. J Biol Chem. 2004; 279(15):14879-88. doi: 10.1074/jbc.M306421200 PMID: 14747478
24. Hua ZL, Chang H, Wang Y, Smallwood PM, Nathans J. Partial interchangeability of Fz3 and Fz6 in tissue polarity signaling for epithelial orientation and axon growth and guidance. Development. 2014; 141 (20):3944-54. doi: 10.1242/dev.110189 PMID: 25294940
25. Guo N, Hawkins C, Nathans J. Frizzled6 controls hair patterning in mice. Proc Natl Acad Sci USA. 2004; 101(25):9277-81. doi: 10.1073/pnas.0402802101 PMID: 15169958
26. Cvjetkovic N, Maili L, Weymouth KS, Hashmi SS, Mulliken JB, Topczewski J, et al. Regulatory variant in FZD6 gene contributes to nonsyndromic cleft lip and palate in an African-American family. Mol Genet Genomic Med. 2015; 3(5):440-51. doi: 10.1002/mgg3.155 PMID: 26436110
27. Wilson NJ, Hansen CD, Azkur D, Kocabas CN, Metin A, Coskun Z, et al. Recessive mutations in the gene encoding frizzled 6 cause twenty nail dystrophy-expanding the differential diagnosis for pachyonychia congenita. J Dermatol Sci. 2013; 70(1):58-60. doi: 10.1016/j.jdermsci.2012.12.005 PMID: 23374899
28. Shi OY, Yang HY, Shen YM, Sun W, Cai CY, Cai CQ. Polymorphisms in FZD3 and FZD6 genes and risk of neural tube defects in a northern Han Chinese population. Neurol Sci. 2014; 35(11):1701-6. doi: 10.1007/s10072-014-1815-4 PMID: 24816679
29. El Abbadi NK, Al Saadi EH. Blood vessels extraction using mathematical morphology. Journal of Computer Science. 2013; 9(10):1389-95.
30. Leandro JJG, Cesar J, Jelinek HF. Blood vessels segmentation in retina: preliminary assessment of the mathematical morphology and of the wavelet transform techniques. Proceedings XIV Brazilian Symposium on Computer Graphics and Image Processing; 2001.
31. Manniesing R, Velthuis BK, van Leeuwen MS, van der Schaaf IC, van Laar PJ, Niessen WJ. Level set based cerebral vasculature segmentation and diameter quantification in CT angiography. Med Image Anal. 2006; 10(2):200-14. PMID: 16263325
32. Serra J. Image Analysis and Mathematical Morphology. Cambridge: Academic Press; 1982.
33. Xie W, Thompson RP, Perucchio R. A topology-preserving parallel 3D thinning algorithm for extracting the curve skeleton. Pattern Recognit. 2003; 36:1529-44.
34. Hagberg A, Schult D, Swart P. Exploring network structure, dynamics, and function using NetworkX. In: Varoquaux G, Vaught T, Millman J, editors. Proc SciPy 2008; 2008; Pasadena; 2008. p. 11-5. Available from http://conference.scipy.org/proceedings/scipy2008/paper-2/
35. Dijkstra EW. A note on two problems in connexion with graphs. Numerische mathematik. 1959; 1:269-71.
36. Strahler A. Quantitative analysis of watershed geomorphology. Eos, Transactions American Geophysical Union. 1957; 38(6):913-20.
37. Kassab GS, Imoto K, White FC, Rider CA, Fung YC, Bloor CM. Coronary arterial tree remodeling in right ventricular hypertrophy. Am J Physiol. 1993; 265(1 Pt 2):H366-75. PMID: 8342653
38. Kassab GS, Rider CA, Tang NJ, Fung YC. Morphometry of pig coronary arterial trees. Am J Physiol. 1993; 265(1 Pt2):H350-65. PMID: 8342652
39. Lopes R, Betrouni N. Fractal and multifractal analysis: a review. Med Image Anal. 2009; 13(4):634-49. doi: 10.1016/j.media.2009.05.003 PMID: 19535282
40. Huo Y, Kassab GS. The scaling of blood flow resistance: from a single vessel to the entire distal tree. Biophys J. 2009; 96(2):339-46. doi: 10.1016/j.bpj.2008.09.038 PMID: 19167287
41. Kaimovitz B, Lanir Y, Kassab GS. Large-scale 3-D geometric reconstruction of the porcine coronary arterial vasculature based on detailed anatomical data. Ann Biomed Eng. 2005; 33(11):1517-35. doi: 10.1007/s10439-005-7544-3 PMID: 16341920
42. Cassot F, Lauwers F, Lorthois S, Puwanarajah P, Cances-Lauwers V, Duvernoy H. Branching patterns for arterioles and venules of the human cerebral cortex. Brain Res. 2009; 1313:62-78. doi: 10.1016/j. brainres.2009.12.007 PMID: 20005216
43. Cassot F, Lauwers F, Lorthois S, Puwanarajah P, Duvernoy H. Scaling laws for branching vessels of human cerebral cortex. Microcirculation. 2009; 16(4):331-44, 2 p following 44. doi: 10.1080/10739680802662607 PMID: 19301179
44. Losa GA. The fractal geometry of life. Riv Biol. 2009; 102(1):29-59. PMID: 19718622
45. Lorthois S, Cassot F. Fractal analysis of vascular networks: insights from morphogenesis. J Theor Biol. 2009; 262(4):614-33. PMID: 19913557
46. Huo Y, Kassab GS. Scaling laws of coronary circulation in health and disease. J Biomech. 2016; 49(12):2531-9. doi: 10.1016/j.jbiomech.2016.01.044 PMID: 26921916
47. Cross SS, Start RD, Silcocks PB, Bull AD, Cotton DW, Underwood JC. Quantitation of the renal arterial tree by fractal analysis. J Pathol. 1993; 170(4):479-84. doi: 10.1002/path.1711700412 PMID: 8410497
48. Gil-Garcia J, Gimeno-Dominguez M, Murillo-Ferroll NL. The arterial pattern and fractal dimension of the dog kidney. Histol Histopathol. 1992; 7(4):563-74. PMID: 1457978
49. Denton KM, Anderson WP, Sinniah R. Effects of angiotensin II on regional afferent and efferent arteriole dimensions and the glomerular pole. Am J Physiol Regul Integr Comp Physiol. 2000; 279(2):R629-38. PMID: 10938254
50. Ren Y, D'Ambrosio MA, Liu R, Pagano PJ, Garvin JL, Carretero OA. Enhanced myogenic response in the afferent arteriole of spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol. 2008; 298(6): H1769-75.
51. Rodriguez-Gomez I, Banegas I, Wangensteen R, Quesada A, Jimenez R, Gomez-Morales M, et al. Influence of thyroid state on cardiac and renal capillary density and glomerular morphology in rats. J Endocrinol. 2013; 216(1):43-51. doi: 10.1530/JOE-12-0208 PMID: 23048210
52. Franco CA, Jones ML, Bernabeu MO, Vion AC, Barbacena P, Fan J, et al. Non-canonical Wnt signalling modulates the endothelial shear stress flow sensor in vascular remodelling. Elife. 2016; 5:e07727. doi: 10.7554/eLife.07727 PMID: 26845523
53. Korn C, Scholz B, Hu J, Srivastava K, Wojtarowicz J, Arnsperger T, et al. Endothelial cell-derived non-canonical Wnt ligands control vascular pruning in angiogenesis. Development. 2014; 141(8):1757-66. doi: 10.1242/dev.104422 PMID: 24715464
54. Stefater JA 3rd, Lewkowich I, Rao S, Mariggi G, Carpenter AC, Burr AR, et al. Regulation of angiogenesis by a non-canonical Wnt-Flt1 pathway in myeloid cells. Nature. 2011; 474(7352):511-5. doi: 10.1038/nature10085 PMID: 21623369