publication . Article . 2016

Endothelial lipid phosphate phosphatase-3 deficiency that disrupts the endothelial barrier function is a modifier of cardiovascular development

Chatterjee, Ishita; Baruah, Jugajyoti; Lurie, Erin E.; Wary, Kishore K.;
Open Access English
  • Published: 01 Apr 2016 Journal: Cardiovascular Research, volume 111, issue 1, pages 105-118 (issn: 0008-6363, eissn: 1755-3245, Copyright policy)
  • Publisher: Oxford University Press
Abstract
Aims Lipid phosphate phosphatase-3 (LPP3) is expressed at high levels in endothelial cells (ECs). Although LPP3 is known to hydrolyse the phosphate group from lysolipids such as spingosine-1-phosphate and its structural homologues, the function of Lpp3 in ECs is not completely understood. In this study, we investigated how tyrosine-protein kinase receptor (TEK or Tie2) promoter–dependent deletion of Lpp3 alters EC activities. Methods and results Lpp3fl/fl mice were crossed with the tg.Tie2Cre transgenic line. Vasculogenesis occurred normally in embryos with Tie2Cre-mediated deletion of Lpp3 (called Lpp3ECKO), but embryonic lethality occurred in two waves, the fi...
Subjects
mesheuropmc: embryonic structures
free text keywords: Beta-catenin, LPP3, ORIGINAL ARTICLES, Neovascularization, VE-cadherin, PPAP2b, Vascular Biology
Funded by
WT
Project
  • Funder: Wellcome Trust (WT)
,
NIH| Center for Clinical and Translational Science
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 3UL1RR029879-03S1
  • Funding stream: NATIONAL CENTER FOR RESEARCH RESOURCES
,
NIH| Regulation of Wnt Signaling by PAP2b During Angiogenesis
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01HL079356-05
  • Funding stream: NATIONAL HEART, LUNG, AND BLOOD INSTITUTE
54 references, page 1 of 4

1 Watt FM, Hodivala KJ Cell adhesion. Fibronectin and integrin knockouts come unstuck. Curr Biol 1994;4:270–272.7522915 [PubMed]

2 Astrof S, Crowley D, Hynes RO Multiple cardiovascular defects caused by the absence of alternatively spliced segments of fibronectin. Dev Biol 2007;311:11–24.17706958 [OpenAIRE] [PubMed]

3 Gory-FauréS, Prandini MH, Pointu H, Roullot V, Pignot-Paintrand I, Vernet M, Huber P Role of vascular endothelial-cadherin in vascular morphogenesis. Development 1999;126:2093–2102.10207135 [PubMed]

4 Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oosthuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E, Clotman F, de Ruiter MC, Gittenberger-de Groot A, Poelmann R, Lupu F, Herbert JM, Collen D, Dejana E Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 1999;98:147–157.10428027 [OpenAIRE] [PubMed]

5 Cattelino A, Liebner S, Gallini R, Zanetti A, Balconi G, Corsi A, Bianco P, Wolburg H, Moore R, Oreda B, Kemler R, Dejana E The conditional inactivation of the beta-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility. J Cell Biol 2003;162:1111–1122.12975353 [OpenAIRE] [PubMed]

6 Vandenbroucke E, Mehta D, Minshall R, Malik AB Regulation of endothelial junctional permeability. Ann NY Acad Sci 2008;1123:134–145.18375586 [PubMed]

7 Clevers H Wnt/beta-catenin signaling in development and disease. Cell 2006;127:469–480.17081971 [PubMed]

8 Corada M, Nyqvist D, Orsenigo F, Caprini A, Giampietro C, Taketo MM, Iruela-Arispe ML, Adams RH, Dejana E The Wnt/beta-catenin pathway modulates vascular remodeling and specification by upregulating Dll4/Notch signaling. Dev Cell 2010;18:938–949.20627076 [OpenAIRE] [PubMed]

9 Schuijers J, Mokry M, Hatzis P, Cuppen E, Clevers H Wnt-induced transcriptional activation is exclusively mediated by TCF/LEF. EMBO J 2014;33:146–156.24413017 [OpenAIRE] [PubMed]

10 Yoon Y, Huang T, Tortelote GG, Wakamiya M, Hadjantonakis AK, Behringer RR, Rivera-Pérez JA Extra-embryonic Wnt3 regulates the establishment of the primitive streak in mice. Dev Biol 2015;403:80–88.25907228 [OpenAIRE] [PubMed]

11 Park C, Kim TM, Malik AB Transcriptional regulation of endothelial cell and vascular development. Circ Res 2013;112:1380–1400.23661712 [OpenAIRE] [PubMed]

12 Fish JE, Wythe JD The molecular regulation of arteriovenous specification and maintenance. Dev Dyn 2015;244:391–409.25641373 [PubMed]

13 Sciorra VA, Morris AJ Sequential actions of phospholipase D and phosphatidic acid phosphohydrolase 2b generate diglyceride in mammalian cells. Mol Biol Cell 1999;10:3863–3876.10564277 [OpenAIRE] [PubMed]

14 Burnett C, Howard K Fly and mammalian lipid phosphate phosphatase isoforms differ in activity both in vitro and in vivo. EMBO Rep 2003;4:793–799.12856002 [OpenAIRE] [PubMed]

15 Brindley DN, Pilquil C Lipid phosphate phosphatases and signaling. J Lipid Res 2009;50(Suppl.):S225–S230.19066402 [OpenAIRE] [PubMed]

54 references, page 1 of 4
Abstract
Aims Lipid phosphate phosphatase-3 (LPP3) is expressed at high levels in endothelial cells (ECs). Although LPP3 is known to hydrolyse the phosphate group from lysolipids such as spingosine-1-phosphate and its structural homologues, the function of Lpp3 in ECs is not completely understood. In this study, we investigated how tyrosine-protein kinase receptor (TEK or Tie2) promoter–dependent deletion of Lpp3 alters EC activities. Methods and results Lpp3fl/fl mice were crossed with the tg.Tie2Cre transgenic line. Vasculogenesis occurred normally in embryos with Tie2Cre-mediated deletion of Lpp3 (called Lpp3ECKO), but embryonic lethality occurred in two waves, the fi...
Subjects
mesheuropmc: embryonic structures
free text keywords: Beta-catenin, LPP3, ORIGINAL ARTICLES, Neovascularization, VE-cadherin, PPAP2b, Vascular Biology
Funded by
WT
Project
  • Funder: Wellcome Trust (WT)
,
NIH| Center for Clinical and Translational Science
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 3UL1RR029879-03S1
  • Funding stream: NATIONAL CENTER FOR RESEARCH RESOURCES
,
NIH| Regulation of Wnt Signaling by PAP2b During Angiogenesis
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01HL079356-05
  • Funding stream: NATIONAL HEART, LUNG, AND BLOOD INSTITUTE
54 references, page 1 of 4

1 Watt FM, Hodivala KJ Cell adhesion. Fibronectin and integrin knockouts come unstuck. Curr Biol 1994;4:270–272.7522915 [PubMed]

2 Astrof S, Crowley D, Hynes RO Multiple cardiovascular defects caused by the absence of alternatively spliced segments of fibronectin. Dev Biol 2007;311:11–24.17706958 [OpenAIRE] [PubMed]

3 Gory-FauréS, Prandini MH, Pointu H, Roullot V, Pignot-Paintrand I, Vernet M, Huber P Role of vascular endothelial-cadherin in vascular morphogenesis. Development 1999;126:2093–2102.10207135 [PubMed]

4 Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oosthuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E, Clotman F, de Ruiter MC, Gittenberger-de Groot A, Poelmann R, Lupu F, Herbert JM, Collen D, Dejana E Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 1999;98:147–157.10428027 [OpenAIRE] [PubMed]

5 Cattelino A, Liebner S, Gallini R, Zanetti A, Balconi G, Corsi A, Bianco P, Wolburg H, Moore R, Oreda B, Kemler R, Dejana E The conditional inactivation of the beta-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility. J Cell Biol 2003;162:1111–1122.12975353 [OpenAIRE] [PubMed]

6 Vandenbroucke E, Mehta D, Minshall R, Malik AB Regulation of endothelial junctional permeability. Ann NY Acad Sci 2008;1123:134–145.18375586 [PubMed]

7 Clevers H Wnt/beta-catenin signaling in development and disease. Cell 2006;127:469–480.17081971 [PubMed]

8 Corada M, Nyqvist D, Orsenigo F, Caprini A, Giampietro C, Taketo MM, Iruela-Arispe ML, Adams RH, Dejana E The Wnt/beta-catenin pathway modulates vascular remodeling and specification by upregulating Dll4/Notch signaling. Dev Cell 2010;18:938–949.20627076 [OpenAIRE] [PubMed]

9 Schuijers J, Mokry M, Hatzis P, Cuppen E, Clevers H Wnt-induced transcriptional activation is exclusively mediated by TCF/LEF. EMBO J 2014;33:146–156.24413017 [OpenAIRE] [PubMed]

10 Yoon Y, Huang T, Tortelote GG, Wakamiya M, Hadjantonakis AK, Behringer RR, Rivera-Pérez JA Extra-embryonic Wnt3 regulates the establishment of the primitive streak in mice. Dev Biol 2015;403:80–88.25907228 [OpenAIRE] [PubMed]

11 Park C, Kim TM, Malik AB Transcriptional regulation of endothelial cell and vascular development. Circ Res 2013;112:1380–1400.23661712 [OpenAIRE] [PubMed]

12 Fish JE, Wythe JD The molecular regulation of arteriovenous specification and maintenance. Dev Dyn 2015;244:391–409.25641373 [PubMed]

13 Sciorra VA, Morris AJ Sequential actions of phospholipase D and phosphatidic acid phosphohydrolase 2b generate diglyceride in mammalian cells. Mol Biol Cell 1999;10:3863–3876.10564277 [OpenAIRE] [PubMed]

14 Burnett C, Howard K Fly and mammalian lipid phosphate phosphatase isoforms differ in activity both in vitro and in vivo. EMBO Rep 2003;4:793–799.12856002 [OpenAIRE] [PubMed]

15 Brindley DN, Pilquil C Lipid phosphate phosphatases and signaling. J Lipid Res 2009;50(Suppl.):S225–S230.19066402 [OpenAIRE] [PubMed]

54 references, page 1 of 4
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