Polycystin Signaling Is Required for Directed Endothelial Cell Migration and Lymphatic Development

Cell Reports

Volumn 7, Issue 3, 2014, Pages 634-644

  Outeda, Patricia ^a   Huso, David L ^b   Fisher, Steven A ^a   Halushka, Marc K ^b   Kim, Hyunho ^a   Qian, Feng ^a   Germino, Gregory G ^c   Watnick, Terry ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCYSTIN 1; POLYCYSTIN 2; POLYCYSTIC KIDNEY DISEASE 1 PROTEIN; POLYCYSTIC KIDNEY DISEASE 2 PROTEIN; POLYCYSTIN; SMALL INTERFERING RNA;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ASSAY; CELL MIGRATION; CELL POLARITY; CONTROLLED STUDY; EDEMA; EMBRYO; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; FEMALE; KNOCKOUT MOUSE; LYMPH VESSEL DENSITY; LYMPHANGIOGENESIS; LYMPHATIC PARAMETERS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL EMBRYO; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL MOTION; CYTOLOGY; EMBRYOLOGY; GENETICS; HUMAN; KIDNEY POLYCYSTIC DISEASE; LYMPH NODE; LYMPH VESSEL; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; RNA INTERFERENCE; UMBILICAL VEIN ENDOTHELIAL CELL; ADULT; GENE; GENE DELETION; GENOTYPE; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PHENOTYPE; PKD1 GENE; PKD2 GENE;

ANIMALS; CELL MOVEMENT; CELL POLARITY; EMBRYO, MAMMALIAN; ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LYMPH NODES; LYMPHATIC VESSELS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; POLYCYSTIC KIDNEY, AUTOSOMAL DOMINANT; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRPP CATION CHANNELS;

MUS;

EID: 84899956827     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.03.064     Document Type: Article

References (32)

1. Arnaout M.A. The vasculopathy of autosomal dominant polycystic kidney disease: insights from animal models. Kidney Int. 2000, 58:2599-2610.
2. Banerji S., Ni J., Wang S.X., Clasper S., Su J., Tammi R., Jones M., Jackson D.G. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J. Cell Biol. 1999, 144:789-801.
3. 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.
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. Chapman A.B., Rubinstein D., Hughes R., Stears J.C., Earnest M.P., Johnson A.M., Gabow P.A., Kaehny W.D. Intracranial aneurysms in autosomal dominant polycystic kidney disease. N. Engl. J. Med. 1992, 327:916-920.
6. Coxam B., Sabine A., Bower N.I., Smith K.A., Pichol-Thievend C., Skoczylas R., Astin J.W., Frampton E., Jaquet M., Crosier P.S., et al. Pkd1 regulates lymphatic vascular morphogenesis during development. Cel. Rep. 2014, 7. Published online April 24, 2014. 10.1016/j.celrep.2014.03.063.
7. D'Amico G., Jones D.T., Nye E., Sapienza K., Ramjuan A.R., Reynolds L.E., Robinson S.D., Kostourou V., Martinez D., Aubyn D., et al. Regulation of lymphatic-blood vessel separation by endothelial Rac1. Development 2009, 136:4043-4053.
8. Edgell C.J., McDonald C.C., Graham J.B. Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc. Natl. Acad. Sci. USA 1983, 80:3734-3737.
9. Etienne-Manneville S., Hall A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 2001, 106:489-498.
10. Etienne-Manneville S., Hall A. Cell polarity: Par6, aPKC and cytoskeletal crosstalk. Curr. Opin. Cell Biol. 2003, 15:67-72.
11. Fritz-Six K.L., Dunworth W.P., Li M., Caron K.M. Adrenomedullin signaling is necessary for murine lymphatic vascular development. J. Clin. Invest. 2008, 118:40-50.
12. Gallagher A.R., Germino G.G., Somlo S. Molecular advances in autosomal dominant polycystic kidney disease. Adv. Chronic Kidney Dis. 2010, 17:118-130.
13. 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.
14. 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.
15. Harris P.C., Torres V.E. Polycystic kidney disease. Annu. Rev. Med. 2009, 60:321-337.
16. 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.
17. Kazenwadel J., Secker G.A., Betterman K.L., Harvey N.L. In vitro assays using primary embryonic mouse lymphatic endothelial cells uncover key roles for FGFR1 signalling in lymphangiogenesis. PLoS ONE 2012, 7:e40497.
18. 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.
19. Kisanuki Y.Y., Hammer R.E., Miyazaki J., Williams S.C., Richardson J.A., Yanagisawa M. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 2001, 230:230-242.
20. Muzumdar M.D., Tasic B., Miyamichi K., Li L., Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007, 45:593-605.
21. Pei Y., Watnick T., He N., Wang K., Liang Y., Parfrey P., Germino G., St George-Hyslop P. Somatic PKD2 mutations in individual kidney and liver cysts support a "two-hit" model of cystogenesis in type 2 autosomal dominant polycystic kidney disease. J. Am. Soc. Nephrol. 1999, 10:1524-1529.
22. 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.
23. Pirson Y. Extrarenal manifestations of autosomal dominant polycystic kidney disease. Adv. Chronic Kidney Dis. 2010, 17:173-180.
24. Qian F., Watnick T.J., Onuchic L.F., Germino G.G. The molecular basis of focal cyst formation in human autosomal dominant polycystic kidney disease type I. Cell 1996, 87:979-987.
25. Qian F., Germino F.J., Cai Y., Zhang X., Somlo S., Germino G.G. PKD1 interacts with PKD2 through a probable coiled-coil domain. Nat. Genet. 1997, 16:179-183.
26. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., Parsons J.T., Horwitz A.R. Cell migration: integrating signals from front to back. Science 2003, 302:1704-1709.
27. Srinivasan R.S., Dillard M.E., Lagutin O.V., Lin F.J., Tsai S., Tsai M.J., Samokhvalov I.M., Oliver G. Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev. 2007, 21:2422-2432.
28. Watnick T.J., Torres V.E., Gandolph M.A., Qian F., Onuchic L.F., Klinger K.W., Landes G., Germino G.G. Somatic mutation in individual liver cysts supports a two-hit model of cystogenesis in autosomal dominant polycystic kidney disease. Mol. Cell 1998, 2:247-251.
29. Wigle J.T., Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999, 98:769-778.
30. Wu G., Markowitz G.S., Li L., D'Agati V.D., Factor S.M., Geng L., Tibara S., Tuchman J., Cai Y., Park J.H., et al. Cardiac defects and renal failure in mice with targeted mutations in Pkd2. Nat. Genet. 2000, 24:75-78.
31. 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.
32. Zudaire E., Gambardella L., Kurcz C., Vermeren S. A computational tool for quantitative analysis of vascular networks. PLoS ONE 2011, 6:e27385.