Pkd1 Regulates Lymphatic Vascular Morphogenesis during Development

Cell Reports

Volumn 7, Issue 3, 2014, Pages 623-633

  Coxam, Baptiste ^a   Sabine, Amélie ^b   Bower, Neil I ^a   Smith, Kelly A ^a   Pichol Thievend, Cathy ^a   Skoczylas, Renae ^a   Astin, Jonathan W ^c   Frampton, Emmanuelle ^a   Jaquet, Muriel ^b   Crosier, Philip S ^c   Parton, Robert G ^a   Harvey, Natasha L ^d   Petrova, Tatiana V ^b   Schulte Merker, Stefan ^e   Francois, Mathias ^a   Hogan, Benjamin M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d CENTRE FOR CANCER BIOLOGY   (Australia)

^e UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCYSTIN 1; POLYCYSTIC KIDNEY DISEASE 1 PROTEIN; POLYCYSTIN; ZEBRAFISH PROTEIN;

ARTICLE; CELL JUNCTION; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; GENE; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; LYMPHANGIOGENESIS; LYMPHATIC AND CARDIAC DEFECTS 1 GENE; MORPHOGENESIS; MOUSE; NONHUMAN; PKD1 GENE; PRIORITY JOURNAL; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; CYTOLOGY; EMBRYO DEVELOPMENT; GENETICS; GROWTH, DEVELOPMENT AND AGING; KIDNEY POLYCYSTIC DISEASE; LYMPH NODE; LYMPH VESSEL; METABOLISM; MUTATION; PATHOLOGY; PHENOTYPE; TRANSGENIC ANIMAL; TRANSGENIC MOUSE; ANIMAL CELL; ANIMAL TISSUE; CELL ADHESION; CELL ELONGATION; CELL POLARITY; GENE EXPRESSION; LYC1 GENE; LYMPH VESSEL ENDOTHELIUM; MOLECULAR MIMICRY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELLS, CULTURED; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; ENDOTHELIAL CELLS; HUMANS; INTERCELLULAR JUNCTIONS; LYMPH NODES; LYMPHANGIOGENESIS; LYMPHATIC VESSELS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; PHENOTYPE; POLYCYSTIC KIDNEY, AUTOSOMAL DOMINANT; TRPP CATION CHANNELS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; MUS;

EID: 84899985698     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.03.063     Document Type: Article

References (42)

1. Boulter C., Mulroy S., Webb S., Fleming S., Brindle K., Sandford R. Cardiovascular, skeletal, and renal defects in mice with a targeted disruption of the Pkd1 gene. Proc. Natl. Acad. Sci. USA 2001, 98:12174-12179.
2. Bussmann J., Bos F.L., Urasaki A., Kawakami K., Duckers H.J., Schulte-Merker S. Arteries provide essential guidance cues for lymphatic endothelial cells in the zebrafish trunk. Development 2010, 137:2653-2657.
3. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55:611-622.
4. Castelli M., Boca M., Chiaravalli M., Ramalingam H., Rowe I., Distefano G., Carroll T., Boletta A. Polycystin-1 binds Par3/aPKC and controls convergent extension during renal tubular morphogenesis. Nat Commun 2013, 4:2658.
5. Chapin H.C., Caplan M.J. The cell biology of polycystic kidney disease. J. Cell Biol. 2010, 191:701-710.
6. François M., Caprini A., Hosking B., Orsenigo F., Wilhelm D., Browne C., Paavonen K., Karnezis T., Shayan R., Downes M., et al. Sox18 induces development of the lymphatic vasculature in mice. Nature 2008, 456:643-647.
7. François M., Short K., Secker G.A., Combes A., Schwarz Q., Davidson T.-L., Smyth I., Hong Y.-K., Harvey N.L., Koopman P. Segmental territories along the cardinal veins generate lymph sacs via a ballooning mechanism during embryonic lymphangiogenesis in mice. Dev. Biol. 2012, 364:89-98.
8. Garcia-Gonzalez M.A., Outeda P., Zhou Q., Zhou F., Menezes L.F., Qian F., Huso D.L., Germino G.G., Piontek K.B., Watnick T. Pkd1 and Pkd2 are required for normal placental development. PLoS ONE 2010, 5:5.
9. Hägerling R., Pollmann C., Andreas M., Schmidt C., Nurmi H., Adams R.H., Alitalo K., Andresen V., Schulte-Merker S., Kiefer F. A novel multistep mechanism for initial lymphangiogenesis in mouse embryos based on ultramicroscopy. EMBO J. 2013, 32:629-644.
10. Hassane S., Claij N., Jodar M., Dedman A., Lauritzen I., Duprat F., Koenderman J.S., van der Wal A., Breuning M.H., de Heer E., et al. Pkd1-inactivation in vascular smooth muscle cells and adaptation to hypertension. Lab. Invest. 2011, 91:24-32.
11. Hogan B.M., Verkade H., Lieschke G.J., Heath J.K. Manipulation of gene expression during zebrafish embryonic development using transient approaches. Methods Mol. Biol. 2008, 469:273-300.
12. Hogan B.M., Bos F.L., Bussmann J., Witte M., Chi N.C., Duckers H.J., Schulte-Merker S. Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat. Genet. 2009, 41:396-398.
13. Hogan B.M., Herpers R., Witte M., Heloterä H., Alitalo K., Duckers H.J., Schulte-Merker S. Vegfc/Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries. Development 2009, 136:4001-4009.
14. Huang P., Schier A.F. Dampened Hedgehog signaling but normal Wnt signaling in zebrafish without cilia. Development 2009, 136:3089-3098.
15. James J.M., Nalbandian A., Mukouyama Y.S. TGFβ signaling is required for sprouting lymphangiogenesis during lymphatic network development in the skin. Development 2013, 140:3903-3914.
16. Jin S.W., Beis D., Mitchell T., Chen J.N., Stainier D.Y. Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 2005, 132:5199-5209.
17. Karkkainen M.J., Haiko P., Sainio K., Partanen J., Taipale J., Petrova T.V., Jeltsch M., Jackson D.G., Talikka M., Rauvala H., et al. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 2004, 5:74-80.
18. Kartopawiro J., Bower N.I., Karnezis T., Kazenwadel J., Betterman K.L., Lesieur E., Koltowska K., Astin J., Crosier P., Vermeren S., et al. Arap3 is dysregulated in a mouse model of hypotrichosis-lymphedema-telangiectasia and regulates lymphatic vascular development. Hum. Mol. Genet. 2014, 23:1286-1297.
19. Kim K., Drummond I., Ibraghimov-Beskrovnaya O., Klinger K., Arnaout M.A. Polycystin 1 is required for the structural integrity of blood vessels. Proc. Natl. Acad. Sci. USA 2000, 97:1731-1736.
20. Koltowska K., Betterman K.L., Harvey N.L., Hogan B.M. Getting out and about: the emergence and morphogenesis of the vertebrate lymphatic vasculature. Development 2013, 140:1857-1870.
21. Krueger J., Liu D., Scholz K., Zimmer A., Shi Y., Klein C., Siekmann A., Schulte-Merker S., Cudmore M., Ahmed A., le Noble F. Flt1 acts as a negative regulator of tip cell formation and branching morphogenesis in the zebrafish embryo. Development 2011, 138:2111-2120.
22. Küchler A.M., Gjini E., Peterson-Maduro J., Cancilla B., Wolburg H., Schulte-Merker S. Development of the zebrafish lymphatic system requires VEGFC signaling. Curr. Biol. 2006, 16:1244-1248.
23. Lal M., Song X., Pluznick J.L., Di Giovanni V., Merrick D.M., Rosenblum N.D., Chauvet V., Gottardi C.J., Pei Y., Caplan M.J. Polycystin-1 C-terminal tail associates with beta-catenin and inhibits canonical Wnt signaling. Hum. Mol. Genet. 2008, 17:3105-3117.
24. Lawson N.D., Weinstein B.M. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 2002, 248:307-318.
25. Le Guen L., Karpanen T., Schulte D., Harris N.C., Koltowska K., Roukens G., Bower N.I., van Impel A., Stacker S.A., Achen M.G., et al. Ccbe1 regulates Vegfc-mediated induction of Vegfr3 signaling during embryonic lymphangiogenesis. Development 2014, 141:1239-1249.
26. Mangos S., Lam P.Y., Zhao A., Liu Y., Mudumana S., Vasilyev A., Liu A., Drummond I.A. The ADPKD genes pkd1a/b and pkd2 regulate extracellular matrix formation. Dis. Model. Mech. 2010, 3:354-365.
27. Muto S., Aiba A., Saito Y., Nakao K., Nakamura K., Tomita K., Kitamura T., Kurabayashi M., Nagai R., Higashihara E., et al. Pioglitazone improves the phenotype and molecular defects of a targeted Pkd1 mutant. Hum. Mol. Genet. 2002, 11:1731-1742.
28. Nauli S.M., Alenghat F.J., Luo Y., Williams E., Vassilev P., Li X., Elia A.E., Lu W., Brown E.M., Quinn S.J., et al. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 2003, 33:129-137.
29. Nauli S.M., Kawanabe Y., Kaminski J.J., Pearce W.J., Ingber D.E., Zhou J. Endothelial cilia are fluid shear sensors that regulate calcium signaling and nitric oxide production through polycystin-1. Circulation 2008, 117:1161-1171.
30. North T.E., Goessling W., Peeters M., Li P., Ceol C., Lord A.M., Weber G.J., Harris J., Cutting C.C., Huang P., et al. Hematopoietic stem cell development is dependent on blood flow. Cell 2009, 137:736-748.
31. Okuda K.S., Astin J.W., Misa J.P., Flores M.V., Crosier K.E., Crosier P.S. lyve1 expression reveals novel lymphatic vessels and new mechanisms for lymphatic vessel development in zebrafish. Development 2012, 139:2381-2391.
32. Outeda P., Huso D.L., Fisher S.A., Halushka M.K., Kim H., Qian F., Germino G.G., Watnick T. Polycystin signaling is required for directed endothelial cell migration and lymphatic development. Cell Rep. 2014, 7. Published online April 24, 2014. 10.1016/j.celrep.2014.03.064.
33. Piontek K.B., Huso D.L., Grinberg A., Liu L., Bedja D., Zhao H., Gabrielson K., Qian F., Mei C., Westphal H., Germino G.G. A functional floxed allele of Pkd1 that can be conditionally inactivated in vivo. J. Am. Soc. Nephrol. 2004, 15:3035-3043.
34. Roitbak T., Ward C.J., Harris P.C., Bacallao R., Ness S.A., Wandinger-Ness A. A polycystin-1 multiprotein complex is disrupted in polycystic kidney disease cells. Mol. Biol. Cell 2004, 15:1334-1346.
35. Rossetti S., Harris P.C. The genetics of vascular complications in autosomal dominant polycystic kidney disease (ADPKD). Curr. Hypertens. Rep. 2013, 9:37-43.
36. Srinivasan R.S., Geng X., Yang Y., Wang Y., Mukatira S., Studer M., Porto M.P., Lagutin O., Oliver G. The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells. Genes Dev. 2010, 24:696-707.
37. Tatin F., Taddei A., Weston A., Fuchs E., Devenport D., Tissir F., Makinen T. Planar cell polarity protein Celsr1 regulates endothelial adherens junctions and directed cell rearrangements during valve morphogenesis. Dev. Cell 2013, 26:31-44.
38. Villefranc J.A., Nicoli S., Bentley K., Jeltsch M., Zarkada G., Moore J.C., Gerhardt H., Alitalo K., Lawson N.D. A truncation allele in vascular endothelial growth factor c reveals distinct modes of signaling during lymphatic and vascular development. Development 2013, 140:1497-1506.
39. Wigle J.T., Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999, 98:769-778.
40. Yang Y., García-Verdugo J.M., Soriano-Navarro M., Srinivasan R.S., Scallan J.P., Singh M.K., Epstein J.A., Oliver G. Lymphatic endothelial progenitors bud from the cardinal vein and intersomitic vessels in mammalian embryos. Blood 2012, 120:2340-2348.
41. Yaniv K., Isogai S., Castranova D., Dye L., Hitomi J., Weinstein B.M. Live imaging of lymphatic development in the zebrafish. Nat. Med. 2006, 12:711-716.
42. Zhou J. Polycystins and primary cilia: primers for cell cycle progression. Annu. Rev. Physiol. 2009, 71:83-113.