Regulation of pulmonary endothelial barrier function by kinases.
The pulmonary endothelium is the target of continuous physiological and pathological stimuli that affect its crucial barrier function. The regulation, defense, and repair of endothelial barrier function require complex biochemical processes. This review examines the role of endothelial phosphorylating enzymes, kinases, a class with profound, interdigitating influences on endothelial permeability and lung function.
Frank Reidy Research Center for Bioelectrics, Old Dominion University, Norfolk, Virginia.
Nektarios
N
Barabutis
Vascular Biology Center, Augusta University, Augusta, Georgia; and.
Alexander
A
Verin
Frank Reidy Research Center for Bioelectrics, Old Dominion University, Norfolk, Virginia, jcatrava@odu.edu.|School of Medical Diagnostic and Translational Sciences, College of Health Sciences, Old Dominion University, Norfolk, Virginia.
John D
JD
Catravas
D000818:Animals; D004730:Endothelium, Vascular / Q000201:enzymology* / Q000502:physiology*; D006801:Humans; D008168:Lung / Q000201:enzymology*; D011494:Protein Kinases / Q000378:metabolism*; D015398:Signal Transduction
D011494:Protein Kinases
barrier function; endothelium; kinases; lung; permeability
Biochem Soc Trans. 1995 May;23(2):203S
7672223
J Physiol. 2005 Dec 1;569(Pt 2):359-66
16195317
J Biol Chem. 1996 Mar 1;271(9):4733-40
8617739
J Biol Chem. 1997 Oct 10;272(41):25968-75
9325331
FEBS Lett. 2009 Jan 5;583(1):1-6
19059243
Prog Biophys Mol Biol. 1999;71(3-4):435-78
10354709
J Biomech. 1995 Dec;28(12):1439-50
8666584
Life Sci. 1999;64(21):1941-53
10353592
Microcirculation. 2005 Dec;12(8):637-43
16284005
Inflamm Res. 2012 Oct;61(10):1069-83
22692279
J Appl Physiol (1985). 2003 Nov;95(5):1889-95
12844496
PLoS One. 2010 Apr 28;5(4):e10385
20442784
Circ J. 2009 Feb;73(2):208-13
19110504
Am J Physiol. 1993 Dec;265(6 Pt 1):L606-12
8279576
Cell. 2011 Jun 24;145(7):1012-22
21703446
Am J Physiol Lung Cell Mol Physiol. 2013 Dec;305(11):L844-55
24097562
J Cell Biol. 1995 Aug;130(3):613-27
7622562
Biochem Biophys Res Commun. 2003 May 30;305(2):223-8
12745062
J Biol Chem. 2002 Nov 22;277(47):45451-7
12223477
Med Res Rev. 2013 Sep;33(5):911-33
22886693
J Clin Invest. 2008 May;118(5):1632-44
18414683
Am J Respir Cell Mol Biol. 1998 Nov;19(5):767-76
9806741
FEBS Lett. 1996 Aug 26;392(2):189-93
8772201
Mol Biol Cell. 2002 Apr;13(4):1175-89
11950930
Surgery. 2002 Aug;132(2):180-5
12219009
J Biol Chem. 1994 Jan 7;269(1):704-10
8276872
J Biol Chem. 2007 Mar 30;282(13):9364-71
17202141
Cell Mol Life Sci. 2010 Nov;67(22):3823-36
20668910
J Appl Physiol (1985). 1991 Dec;71(6):2152-9
1778906
Am J Physiol Cell Physiol. 2002 Dec;283(6):C1745-51
12388068
J Biol Chem. 1986 Jan 5;261(1):36-9
3079756
Biochim Biophys Acta. 2001 Jul 25;1540(1):1-21
11476890
Hum Mol Genet. 2001 Jul 15;10(15):1563-9
11468274
Cell Motil Cytoskeleton. 2003 Jan;54(1):1-15
12451591
Arterioscler Thromb Vasc Biol. 2001 Mar;21(3):300-11
11231907
Mol Cell Biol. 2004 Sep;24(18):8113-33
15340073
Am J Physiol Cell Physiol. 2004 Nov;287(5):C1246-55
15475517
Mol Biol Cell. 2003 Aug;14(8):3065-81
12925747
Proc Natl Acad Sci U S A. 1995 May 9;92(10):4527-31
7538674
J Cell Physiol. 1992 Oct;153(1):62-75
1522136
Anat Rec (Hoboken). 2014 May;297(5):964-72
24458982
Genomics. 1999 Apr 15;57(2):256-67
10198165
Science. 1999 Jan 29;283(5402):655-61
9924018
J Cell Biol. 2002 Apr 1;157(1):149-60
11927607
Am J Physiol. 1991 May;260(5 Pt 1):C1052-9
1709785
Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7074-8
7688470
Br J Pharmacol. 1993 Jul;109 (3):703-12
8395295
Genomics. 1999 Oct 1;61(1):44-54
10512679
EMBO J. 2000 Mar 1;19(5):964-78
10698938
Free Radic Biol Med. 1998 Dec;25(9):1021-32
9870555
J Biol Chem. 2004 Jun 4;279(23):24692-700
15056655
J Biol Chem. 1973 Jan 10;248(1):378-80
4692841
Am J Physiol. 1995 Dec;269(6 Pt 1):L829-36
8572244
Nature. 2005 Sep 22;437(7058):497-504
16177780
Br J Pharmacol. 2007 Sep;152(1):122-31
17603544
J Biol Chem. 1995 Dec 8;270(49):29051-4
7493923
Mini Rev Med Chem. 2008 Jun;8(6):628-37
18537718
Annu Rev Biochem. 2000;69:373-98
10966463
Oncogene. 1996 Aug 1;13(3):515-25
8760293
Mol Cell Biol. 2015 Dec;35(23):3990-4005
26391956
Mol Cell. 1999 Dec;4(6):915-24
10635317
Am J Physiol. 1999 Feb;276(2 Pt 2):H736-48
9950877
J Allergy Clin Immunol. 2013 Sep;132(3):665-675.e8
23632299
Curr Opin Cell Biol. 2009 Oct;21(5):676-83
19525103
Am J Physiol Lung Cell Mol Physiol. 2004 Dec;287(6):L1091-7
15286003
J Cell Physiol. 2001 Jul;188(1):106-19
11382927
J Biol Chem. 2008 Oct 31;283(44):29888-96
18713748
Chem Biol Interact. 2008 Jan 30;171(2):177-89
17897637
Science. 2002 Dec 6;298(5600):1912-34
12471243
J Cell Biol. 2000 Aug 21;150(4):797-806
10953004
Circ Res. 1992 Feb;70(2):382-91
1310449
Cell Motil Cytoskeleton. 1998;39(2):172-90
9484959
J Cell Physiol. 1995 Jun;163(3):510-22
7775594
Am J Physiol Lung Cell Mol Physiol. 2014 Dec 15;307(12):L924-35
25381026
Microvasc Res. 2012 Jan;83(1):1-2
22036672
Inflammation. 1990 Oct;14(5):571-83
2174409
Int J Cardiol. 2013 Oct 12;168(5):5042-3
23962784
Arterioscler Thromb Vasc Biol. 2007 Nov;27(11):2332-9
17761936
J Cell Biol. 2000 Aug 7;150(3):567-80
10931868
J Mol Cell Cardiol. 2010 Apr;48(4):746-56
19913548
Am J Physiol. 1992 Aug;263(2 Pt 2):H641-6
1510161
Mol Cell Biol. 1997 Mar;17(3):1129-43
9032240
Biochem Biophys Res Commun. 2005 May 27;331(1):1-14
15845350
Arterioscler Thromb Vasc Biol. 2013 Mar;33(3):565-71
23307871
Nat Cell Biol. 2006 Nov;8(11):1223-34
17060906
Pharmacol Res. 2007 Jun;55(6):467-76
17580120
Vascul Pharmacol. 2002 Nov;39(4-5):213-23
12747961
Genome Biol. 2002;3(5):reviews3007
12049672
Nat Rev Cancer. 2014 Jan;14(1):13-25
24505617
Annu Rev Nutr. 2014;34:31-55
24850385
J Surg Res. 1995 Jul;59(1):159-64
7630121
J Biol Chem. 2000 Jun 16;275(24):18366-74
10748018
Am J Physiol Lung Cell Mol Physiol. 2006 May;290(5):L919-30
16339778
Arterioscler Thromb Vasc Biol. 2008 Aug;28(8):1527-33
18497307
Am J Physiol. 1999 Jun;276(6 Pt 1):L989-98
10362724
Biochemistry (Mosc). 2002 Jan;67(1):75-84
11841342
J Cell Biol. 1997 Mar 24;136(6):1307-22
9087445
J Biol Chem. 2000 Dec 29;275(52):41201-9
10995762
Biochem J. 1993 Sep 1;294 ( Pt 2):401-6
8396912
Cell Adh Migr. 2010 Jul-Sep;4(3):342-7
20372092
J Biol Chem. 2003 May 9;278(19):17170-7
12606547
PLoS One. 2013 Dec 19;8(12):e85231
24367707
Microvasc Res. 2012 Jan;83(1):12-21
21549132
Mol Biol Cell. 2007 Jun;18(6):2346-55
17429073
Mol Cell Biol. 1996 Oct;16(10):5313-27
8816443
Am J Physiol Lung Cell Mol Physiol. 2014 Nov 15;307(10 ):L735-45
25239914
Nature. 2008 May 22;453(7194):475-80
18497816
Neurochem Int. 2004 Mar;44(4):205-14
14602083
PLoS One. 2012;7(8):e44041
22952866
J Appl Physiol (1985). 2001 Oct;91(4):1487-500
11568129
Channels (Austin). 2009 Jul-Aug;3(4):221-5
19574740
J Biol Chem. 1997 Jun 13;272(24):15442-51
9182576
Nature. 1977 Sep 22;269(5626):346-8
198667
Am J Physiol. 1994 Sep;267(3 Pt 1):L223-41
7943249
Nature. 1998 Jun 25;393(6687):805-9
9655397
Science. 1996 Jul 12;273(5272):245-8
8662509
Microvasc Res. 2009 Jan;77(1):21-5
19027754
Am J Respir Cell Mol Biol. 1998 Nov;19(5):758-66
9806740
J Leukoc Biol. 1994 May;55(5):662-75
8182345
Am J Physiol Heart Circ Physiol. 2000 Apr;278(4):H1124-33
10749706
J Cell Physiol. 2012 Feb;227(2):759-71
21465483
Circ Res. 1995 Feb;76(2):199-208
7834830
BMC Biochem. 2002 Dec 31;3:32
12509223
Am J Physiol Lung Cell Mol Physiol. 2007 Oct;293(4):L843-54
17693486
Microvasc Res. 2008 Nov;76(3):202-7
18657550
Physiol Rev. 2001 Apr;81(2):807-69
11274345
Cell. 2002 Jan 25;108(2):233-46
11832213
Genes Dev. 1996 Aug 1;10(15):1845-57
8756343
Physiol Genomics. 2000 Dec 18;4(2):137-145
11120874
Diabetes. 2013 Jul;62(7):2164-72
23801715
J Appl Physiol (1985). 1992 Jan;72(1):389-95
1311292
Cell Adh Migr. 2011 Jul-Aug;5(4):360-5
21836391
Microvasc Res. 2000 Sep;60(2):104-11
10964584
Oncogene. 1993 Nov;8(11):3133-9
8414515
Annu Rev Cell Dev Biol. 1997;13:513-609
9442882
Biochem Biophys Res Commun. 1973 Oct 15;54(4):1362-9
4356818
Circ Res. 1997 Mar;80(3):383-92
9048659
Am J Physiol. 1996 Dec;271(6 Pt 2):H2735-9
8997338
Am J Respir Cell Mol Biol. 2003 May;28(5):626-36
12707019
Lab Invest. 1990 Oct;63(4):521-31
2172648
Oncogene. 2001 Apr 12;20(16):1964-72
11360180
J Mol Cell Cardiol. 2004 Aug;37(2):537-46
15276023
J Biol Chem. 1996 Jan 12;271(2):695-701
8557675
Am J Physiol Lung Cell Mol Physiol. 2016 Jan 1;310(1):L71-85
26545901
J Biol Chem. 2001 Mar 16;276(11):8567-73
11113114
J Physiol. 2002 Mar 15;539(Pt 3):779-89
11897849
J Biol Chem. 2004 Nov 5;279(45):46621-30
15333633
Circ Res. 2004 Apr 30;94(8):1041-9
15016733
Am J Physiol Lung Cell Mol Physiol. 2005 Aug;289(2):L176-85
15764646
Am J Physiol Lung Cell Mol Physiol. 2013 Jun 15;304(12):L883-93
23585225
PLoS One. 2014 Jul 14;9(7):e99823
25020117
Mol Cell Biol. 2005 Aug;25(15):6391-403
16024778
J Biol Chem. 2010 Apr 23;285(17 ):12536-42
20164172
Am J Physiol Heart Circ Physiol. 2009 Oct;297(4):H1469-77
19666843
Science. 2006 Jun 30;312(5782):1882-3
16809515
Front Pharmacol. 2015 Nov 20;6:276
26635606
Mediators Inflamm. 2015;2015:272858
26556953
J Clin Invest. 1993 Sep;92(3):1198-206
8397221
Nature. 2009 Sep 3;461(7260):99-103
19693013
J Cell Physiol. 1997 Sep;172(3):373-81
9284957
Biochem Biophys Res Commun. 2014 May 9;447(3):520-5
24732361
EMBO J. 1996 Apr 15;15(8):1885-93
8617235
Biochem Biophys Res Commun. 2000 Mar 24;269(3):652-9
10720471
Proc Natl Acad Sci U S A. 1985 May;82(10):3187-91
3858814
J Cell Sci. 2003 Apr 15;116(Pt 8):1409-16
12640026
Cell. 1996 Feb 9;84(3):359-69
8608589
J Biol Chem. 1996 Aug 23;271(34):20246-9
8702756
Annu Rev Physiol. 2013;75:593-615
23398155
Arterioscler Thromb Vasc Biol. 2012 Dec;32(12 ):2989-99
23023377
Clin Cancer Res. 2012 Jan 1;18(1):64-76
22215907
J Biol Chem. 2012 Oct 19;287(43):36356-69
22948155
Mol Med. 2013 Nov 08;19:387-98
24091934
Mol Med Rep. 2015 Sep;12(3):4109-16
26096176
Am J Respir Cell Mol Biol. 1997 May;16(5):489-94
9160829
Circulation. 2004 Dec 14;110(24):3708-14
15569838
J Cell Biol. 2007 Feb 26;176(5):719-27
17312022
Biochem Biophys Res Commun. 2001 Aug 24;286(3):566-73
11511097
Am J Physiol Cell Physiol. 2015 Jan 15;308(2):C164-75
25377089
PLoS One. 2012;7(6):e39269
22723981
Dev Cell. 2012 Jan 17;22(1):146-57
22264731
Am J Physiol Lung Cell Mol Physiol. 2005 Jul;289(1):L75-84
15778245
EMBO J. 1998 Feb 2;17(3):754-64
9451000
J Physiol. 2003 Jun 1;549(Pt 2):489-500
12692179
Circ Res. 2010 Apr 30;106(8):1319-31
20431074
Proc Natl Acad Sci U S A. 2003 May 13;100(10):6233-8
12730364
Eur J Biochem. 1988 Aug 1;175(2):331-8
2900138
J Biol Chem. 1995 Jul 21;270(29):17582-7
7615564
Circulation. 2005 Mar 8;111(9):1184-91
15753227
Microvasc Res. 2001 Nov;62(3):263-70
11678629
Cell Syst. 2016 Jan 27;2(1):38-48
27136688
Mol Cell Biol. 2005 Jan;25(1):136-46
15601837
Circ Res. 2012 Aug 31;111(6):739-49
22798526
Am J Physiol. 1997 Mar;272(3 Pt 2):H1437-43
9087622
Circ Res. 2009 Sep 11;105(6):549-56
19679840
Circ Res. 1995 Apr;76(4):522-9
7895328
Am J Physiol. 1998 Jun;274(6 Pt 2):H1865-74
9841514
Am J Physiol Lung Cell Mol Physiol. 2015 Apr 15;308(8):L776-87
25713322
Am J Physiol Lung Cell Mol Physiol. 2013 Aug 15;305(4):L291-300
23771883
Hypertension. 2011 May;57(5):1010-7
21464390
Am J Physiol Cell Physiol. 2000 Jul;279(1):C21-30
10898713
Antioxid Redox Signal. 2011 Jun;14(11):2107-19
21194376
Am J Physiol Lung Cell Mol Physiol. 2008 Sep;295(3):L497-504
18586954
Curr Opin Genet Dev. 2004 Feb;14(1):92-101
15108811
Science. 2004 Apr 30;304(5671):743-6
15118165
Endothelium. 2000;7(4):287-308
11201526
Nat Rev Mol Cell Biol. 2005 Jan;6(1):56-68
15688067
Am J Physiol Lung Cell Mol Physiol. 2006 Aug;291(2):L129-41
16581827
Diabet Med. 2001 Dec;18(12):945-59
11903393
J Clin Invest. 2004 Mar;113(6):885-94
15067321
Mol Med. 2012 May 09;18:659-68
22396017
Physiol Rev. 2006 Jan;86(1):279-367
16371600
Cardiovasc Res. 2008 Jan;77(1):160-8
18006475
Mol Biol Cell. 2006 Aug;17(8):3508-20
16760434
J Biol Chem. 2004 May 7;279(19):20392-400
15007081
Pulm Circ. 2014 Dec;4(4):535-51
25610592
J Biol Chem. 1980 Mar 25;255(6):2308-14
6102090
Am J Pathol. 2013 Mar;182(3):1021-30
23306156
Circ Res. 1995 Nov;77(5):897-905
7554143
J Physiol. 2001 Jun 1;533(Pt 2):433-45
11389203
PLoS One. 2008 Aug 27;3(8):e3068
18728784
J Cell Sci. 1998 Jul;111 ( Pt 13):1853-65
9625748
Mol Cancer Res. 2015 Nov;13(11):1445-51
26219697
J Biol Chem. 2001 Aug 24;276(34):32115-21
11413130
Microvasc Res. 2002 Mar;63(2):172-8
11866540
Int J Biochem Cell Biol. 1998 Aug;30(8):857-62
9744077
J Physiol. 2011 Nov 15;589(Pt 22):5415-29
21930597
Tissue Barriers. 2015 Apr 03;3(1-2):e974448
25838980
Br J Pharmacol. 2003 Mar;138(5):757-66
12642376
Circ Res. 2009 Feb 27;104(4):531-40
19131646
Mol Biol Cell. 2005 Feb;16(2):649-64
15548599
Am J Physiol. 1997 Nov;273(5 Pt 2):H2442-51
9374783
Annu Rev Physiol. 2014;76:431-45
24245941
EMBO J. 1996 May 1;15(9):2208-16
8641286
J Exp Med. 2014 Mar 10;211(3):579-91
24590762
Mol Cell Biol. 2005 Jan;25(1):389-402
15601859
Science. 1999 Mar 26;283(5410):2083-5
10092231
Am J Physiol Lung Cell Mol Physiol. 2002 Jan;282(1):L146-54
11741826
Open Biol. 2014 Jan 22;4:130132
24451547
Eur J Immunol. 2000 Dec;30(12):3422-31
11093160
Genes Cells. 1996 Jan;1(1):73-86
9078368
Eur J Biochem. 1994 Jul 15;223(2):351-7
8055903
J Cell Sci. 2005 Jan 1;118(Pt 1):19-26
15615780
J Cell Biol. 2004 Aug 30;166(5):697-708
15337778
J Cell Biol. 2003 Feb 3;160(3):375-85
12551955
Biochem J. 2001 Nov 15;360(Pt 1):255-64
11696015
Proc Natl Acad Sci U S A. 1978 Mar;75(3):1567-71
206909
Methods Mol Biol. 2003;211:465-85
12489450
Am J Physiol Lung Cell Mol Physiol. 2000 Aug;279(2):L360-70
10926560
Curr Opin Cell Biol. 1998 Feb;10(1):140-4
9484606
Circ Res. 2008 Mar 14;102(5):571-80
18202317
J Cardiovasc Pharmacol. 2007 Jul;50(1):17-24
17666911
Trans Am Clin Climatol Assoc. 2008;119:155-67; discussion 167-9
18596849
Inflammation. 2000 Apr;24(2):99-113
10718113
Annu Rev Cell Dev Biol. 2005;21:247-69
16212495
Pulm Circ. 2015 Dec;5(4):707-15
26697178
Circulation. 1999 May 18;99(19):2523-9
10330383
Inflammation. 2015 Apr;38(2):623-31
25008149
Mol Metab. 2013 Dec 07;3(2):94-108
24634815
Inflammation. 1998 Aug;22(4):419-33
9675612
Microvasc Res. 2001 Nov;62(3):252-62
11678628
J Cell Biol. 2005 Aug 1;170(3):443-53
16043513
Biochim Biophys Acta. 2008 Mar;1778(3):729-56
17950242
Ann N Y Acad Sci. 2008 Mar;1123:134-45
18375586
Cell. 2009 Oct 30;139(3):468-84
19879837
FEBS Lett. 1987 Nov 2;223(2):217-22
2889619
FASEB J. 2003 Dec;17(15):2240-9
14656986
J Cell Biol. 1997 Aug 25;138(4):771-81
9265645
Am J Physiol Cell Physiol. 2000 Nov;279(5):C1656-64
11029314
Cardiovasc Res. 2010 Nov 1;88(2):344-51
20542878
Cardiovasc Res. 2010 Jul 15;87(2):272-80
20479130
Am J Physiol Cell Physiol. 2001 Dec;281(6):C1940-7
11698252
Proc Natl Acad Sci U S A. 2015 Jun 23;112(25):E3189-98
26056257
J Cell Biochem. 1999 Dec 1;75(3):481-91
10536370
Immune Netw. 2015 Aug;15(4):206-11
26330807
Oncogene. 2010 Jan 14;29(2):263-72
19802004