Endothelial Mitogen-Activated Protein Kinase Kinase Kinase Kinase 4 Is Critical for Lymphatic Vascular Development and Function

REFERENCES

• Choi I, Lee S, Hong YK. 2012. The new era of the lymphatic system: no longer secondary to the blood vascular system. Cold Spring Harb Perspect Med 2:a006445. http://dx.doi.org/10.1101/cshperspect.a006445.
   PubMed Web of Science ®Google Scholar
• Randolph GJ, Miller NE. 2014. Lymphatic transport of high-density lipoproteins and chylomicrons. J Clin Invest 124:929–935. http://dx.doi.org/10.1172/JCI71610.
   PubMed Web of Science ®Google Scholar
• Card CM, Yu SS, Swartz MA. 2014. Emerging roles of lymphatic endothelium in regulating adaptive immunity. J Clin Invest 124:943–952. http://dx.doi.org/10.1172/JCI73316.
   PubMed Web of Science ®Google Scholar
• Alitalo K. 2011. The lymphatic vasculature in disease. Nat Med 17:1371–1380. http://dx.doi.org/10.1038/nm.2545.
   PubMed Web of Science ®Google Scholar
• Wang Y, Oliver G. 2010. Current views on the function of the lymphatic vasculature in health and disease. Genes Dev 24:2115–2126. http://dx.doi.org/10.1101/gad.1955910.
   PubMed Web of Science ®Google Scholar
• Wigle JT, Oliver G. 1999. Prox1 function is required for the development of the murine lymphatic system. Cell 98:769–778. http://dx.doi.org/10.1016/S0092-8674(00)81511-1.
   PubMed Web of Science ®Google Scholar
• Wigle JT, Harvey N, Detmar M, Lagutina I, Grosveld G, Gunn MD, Jackson DG, Oliver G. 2002. An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J 21:1505–1513. http://dx.doi.org/10.1093/emboj/21.7.1505.
   PubMed Web of Science ®Google Scholar
• Roth Flach RJ, Skoura A, Matevossian A, Danai LV, Zheng W, Cortes C, Bhattacharya SK, Aouadi M, Hagan N, Yawe JC, Vangala P, Menendez LG, Cooper MP, Fitzgibbons TP, Buckbinder L, Czech MP. 2015. Endothelial protein kinase MAP4K4 promotes vascular inflammation and atherosclerosis. Nat Commun 6:8995. http://dx.doi.org/10.1038/ncomms9995.
   PubMedGoogle Scholar
• Alva JA, Zovein AC, Monvoisin A, Murphy T, Salazar A, Harvey NL, Carmeliet P, Iruela-Arispe ML. 2006. VE-cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells. Dev Dyn 235:759–767. http://dx.doi.org/10.1002/dvdy.20643.
   PubMed Web of Science ®Google Scholar
• Lapinski PE, Kwon S, Lubeck BA, Wilkinson JE, Srinivasan RS, Sevick-Muraca E, King PD. 2012. RASA1 maintains the lymphatic vasculature in a quiescent functional state in mice. J Clin Invest 122:733–747. http://dx.doi.org/10.1172/JCI46116.
   PubMedGoogle Scholar
• Baumgartner M, Sillman AL, Blackwood EM, Srivastava J, Madson N, Schilling JW, Wright JH, Barber DL. 2006. The Nck-interacting kinase phosphorylates ERM proteins for formation of lamellipodium by growth factors. Proc Natl Acad Sci U S A 103:13391–13396. http://dx.doi.org/10.1073/pnas.0605950103.
   PubMed Web of Science ®Google Scholar
• Fitzgibbons TP, Kogan S, Aouadi M, Hendricks GM, Straubhaar J, Czech MP. 2011. Similarity of mouse perivascular and brown adipose tissues and their resistance to diet-induced inflammation. Am J Physiol Heart Circ Physiol 301:H1425–H1437. http://dx.doi.org/10.1152/ajpheart.00376.2011.
   PubMed Web of Science ®Google Scholar
• Mortimer PS, Rockson SG. 2014. New developments in clinical aspects of lymphatic disease. J Clin Invest 124:915–921. http://dx.doi.org/10.1172/JCI71608.
   PubMed Web of Science ®Google Scholar
• Petrova TV, Karpanen T, Norrmen C, Mellor R, Tamakoshi T, Finegold D, Ferrell R, Kerjaschki D, Mortimer P, Yla-Herttuala S, Miura N, Alitalo K. 2004. Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat Med 10:974–981. http://dx.doi.org/10.1038/nm1094.
   PubMed Web of Science ®Google Scholar
• Bazigou E, Lyons OT, Smith A, Venn GE, Cope C, Brown NA, Makinen T. 2011. Genes regulating lymphangiogenesis control venous valve formation and maintenance in mice. J Clin Invest 121:2984–2992. http://dx.doi.org/10.1172/JCI58050.
   PubMed Web of Science ®Google Scholar
• Vitorino P, Yeung S, Crow A, Bakke J, Smyczek T, West K, McNamara E, Eastham-Anderson J, Gould S, Harris SF, Ndubaku C, Ye W. 2015. MAP4K4 regulates integrin-FERM binding to control endothelial cell motility. Nature 519:425–430. http://dx.doi.org/10.1038/nature14323.
   PubMed Web of Science ®Google Scholar
• Su YC, Han J, Xu S, Cobb M, Skolnik EY. 1997. NIK is a new Ste20-related kinase that binds NCK and MEKK1 and activates the SAPK/JNK cascade via a conserved regulatory domain. EMBO J 16:1279–1290. http://dx.doi.org/10.1093/emboj/16.6.1279.
   PubMed Web of Science ®Google Scholar
• Ger M, Zitkus Z, Valius M. 2011. Adaptor protein Nck1 interacts with p120 Ras GTPase-activating protein and regulates its activity. Cell Signal 23:1651–1658. http://dx.doi.org/10.1016/j.cellsig.2011.05.019.
   PubMedGoogle Scholar
• Becker E, Huynh-Do U, Holland S, Pawson T, Daniel TO, Skolnik EY. 2000. Nck-interacting Ste20 kinase couples Eph receptors to c-Jun N-terminal kinase and integrin activation. Mol Cell Biol 20:1537–1545. http://dx.doi.org/10.1128/MCB.20.5.1537-1545.2000.
   PubMedGoogle Scholar
• Burrows PE, Gonzalez-Garay ML, Rasmussen JC, Aldrich MB, Guilliod R, Maus EA, Fife CE, Kwon S, Lapinski PE, King PD, Sevick-Muraca EM. 2013. Lymphatic abnormalities are associated with RASA1 gene mutations in mouse and man. Proc Natl Acad Sci U S A 110:8621–8626. http://dx.doi.org/10.1073/pnas.1222722110.
   PubMed Web of Science ®Google Scholar
• King PD, Lubeck BA, Lapinski PE. 2013. Nonredundant functions for Ras GTPase-activating proteins in tissue homeostasis. Sci Signal 6:re1. http://dx.doi.org/10.1126/scisignal.2003669.
   PubMedGoogle Scholar
• Deng Y, Atri D, Eichmann A, Simons M. 2013. Endothelial ERK signaling controls lymphatic fate specification. J Clin Invest 123:1202–1215. http://dx.doi.org/10.1172/JCI63034.
   PubMedGoogle Scholar
• Simons M, Alitalo K, Annex BH, Augustin HG, Beam C, Berk BC, Byzova T, Carmeliet P, Chilian W, Cooke JP, Davis GE, Eichmann A, Iruela-Arispe ML, Keshet E, Sinusas AJ, Ruhrberg C, Woo YJ, Dimmeler S, American Heart Association Council on Basic Cardiovascular Sciences, Council on Cardiovascular Surgery and Anesthesia. 2015. State-of-the-art methods for evaluation of angiogenesis and tissue vascularization: a scientific statement from the American Heart Association. Circ Res 116:e99–e132. http://dx.doi.org/10.1161/RES.0000000000000054.
   PubMedGoogle Scholar
• Harvey NL, Srinivasan RS, Dillard ME, Johnson NC, Witte MH, Boyd K, Sleeman MW, Oliver G. 2005. Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity. Nat Genet 37:1072–1081. http://dx.doi.org/10.1038/ng1642.
   PubMed Web of Science ®Google Scholar
• Lim HY, Rutkowski JM, Helft J, Reddy ST, Swartz MA, Randolph GJ, Angeli V. 2009. Hypercholesterolemic mice exhibit lymphatic vessel dysfunction and degeneration. Am J Pathol 175:1328–1337. http://dx.doi.org/10.2353/ajpath.2009.080963.
   PubMed Web of Science ®Google Scholar
• Lim HY, Thiam CH, Yeo KP, Bisoendial R, Hii CS, McGrath KC, Tan KW, Heather A, Alexander JS, Angeli V. 2013. Lymphatic vessels are essential for the removal of cholesterol from peripheral tissues by SR-BI-mediated transport of HDL. Cell Metab 17:671–684. http://dx.doi.org/10.1016/j.cmet.2013.04.002.
   PubMed Web of Science ®Google Scholar
• Martel C, Li W, Fulp B, Platt AM, Gautier EL, Westerterp M, Bittman R, Tall AR, Chen SH, Thomas MJ, Kreisel D, Swartz MA, Sorci-Thomas MG, Randolph GJ. 2013. Lymphatic vasculature mediates macrophage reverse cholesterol transport in mice. J Clin Invest 123:1571–1579. http://dx.doi.org/10.1172/JCI63685.
   PubMed Web of Science ®Google Scholar
• Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, Jeltsch M, Jackson DG, Talikka M, Rauvala H, Betsholtz C, Alitalo K. 2004. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol 5:74–80. http://dx.doi.org/10.1038/ni1013.
   PubMed Web of Science ®Google Scholar
• Karkkainen MJ, Saaristo A, Jussila L, Karila KA, Lawrence EC, Pajusola K, Bueler H, Eichmann A, Kauppinen R, Kettunen MI, Yla-Herttuala S, Finegold DN, Ferrell RE, Alitalo K. 2001. A model for gene therapy of human hereditary lymphedema. Proc Natl Acad Sci U S A 98:12677–12682. http://dx.doi.org/10.1073/pnas.221449198.
   PubMed Web of Science ®Google Scholar
• Makinen T, Adams RH, Bailey J, Lu Q, Ziemiecki A, Alitalo K, Klein R, Wilkinson GA. 2005. PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes Dev 19:397–410. http://dx.doi.org/10.1101/gad.330105.
   PubMed Web of Science ®Google Scholar
• Zhang G, Brady J, Liang WC, Wu Y, Henkemeyer M, Yan M. 2015. EphB4 forward signalling regulates lymphatic valve development. Nat Commun 6:6625. http://dx.doi.org/10.1038/ncomms7625.
   PubMed Web of Science ®Google Scholar
• Kawasaki J, Aegerter S, Fevurly RD, Mammoto A, Mammoto T, Sahin M, Mably JD, Fishman SJ, Chan J. 2014. RASA1 functions in EPHB4 signaling pathway to suppress endothelial mTORC1 activity. J Clin Invest 124:2774–2784. http://dx.doi.org/10.1172/JCI67084.
   PubMed Web of Science ®Google Scholar
• Ichise T, Yoshida N, Ichise H. 2010. H-, N- and Kras cooperatively regulate lymphatic vessel growth by modulating VEGFR3 expression in lymphatic endothelial cells in mice. Development 137:1003–1013. http://dx.doi.org/10.1242/dev.043489.
   PubMedGoogle Scholar
• Gupta S, Ramjaun AR, Haiko P, Wang Y, Warne PH, Nicke B, Nye E, Stamp G, Alitalo K, Downward J. 2007. Binding of ras to phosphoinositide 3-kinase p110alpha is required for ras-driven tumorigenesis in mice. Cell 129:957–968. http://dx.doi.org/10.1016/j.cell.2007.03.051.
   PubMed Web of Science ®Google Scholar
• Zuber J, Tchernitsa OI, Hinzmann B, Schmitz AC, Grips M, Hellriegel M, Sers C, Rosenthal A, Schafer R. 2000. A genome-wide survey of RAS transformation targets. Nat Genet 24:144–152. http://dx.doi.org/10.1038/72799.
   PubMed Web of Science ®Google Scholar
• Bajaj A, Zheng Q, Adam A, Vincent P, Pumiglia K. 2010. Activation of endothelial ras signaling bypasses senescence and causes abnormal vascular morphogenesis. Cancer Res 70:3803–3812. http://dx.doi.org/10.1158/0008-5472.CAN-09-2648.
   PubMedGoogle Scholar
• Srinivasan R, Zabuawala T, Huang H, Zhang J, Gulati P, Fernandez S, Karlo JC, Landreth GE, Leone G, Ostrowski MC. 2009. Erk1 and Erk2 regulate endothelial cell proliferation and migration during mouse embryonic angiogenesis. PLoS One 4:e8283. http://dx.doi.org/10.1371/journal.pone.0008283.
   PubMedGoogle Scholar
• Ndubaku CO, Crawford TD, Chen H, Boggs JW, Drobnick J, Harris SF, Jesudason R, McNamara E, Nonomiya J, Sambrone A, Schmidt S, Smyczek T, Vitorino P, Wang L, Wu P, Yeung S, Chen J, Chen K, Ding CZ, Wang T, Xu Z, Gould SE, Murray LJ, Ye W. 2015. Structure-based design of GNE-495, a potent and selective MAP4K4 inhibitor with efficacy in retinal angiogenesis. ACS Med Chem Lett 6:913–918. http://dx.doi.org/10.1021/acsmedchemlett.5b00174.
   PubMed Web of Science ®Google Scholar
• Schroder P, Forster T, Kleine S, Becker C, Richters A, Ziegler S, Rauh D, Kumar K, Waldmann H. 2015. Neuritogenic militarinone-inspired 4-hydroxypyridones target the stress pathway kinase MAP4K4. Angew Chem Int Ed Engl 54:12398–12403. http://dx.doi.org/10.1002/anie.201501515.
   PubMedGoogle Scholar