The Role of PB1 Domain Proteins in Endothelial Cell Dysfunction and Disease

Antioxidants and Redox Signaling

Volumn 22, Issue 14, 2015, Pages 1243-1256

  Burke, Ryan M ^a   Berk, Bradford C ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXIDOREDUCTASE; PROTEIN KINASE C; PROTEIN KINASE C DELTA; PROTEIN P40; PROTEIN P67; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ATHEROSCLEROSIS; AUTOPHAGY; CARDIOVASCULAR DISEASE; CELL POLARITY; ENDOTHELIUM CELL; FEEDBACK SYSTEM; HUMAN; HYPERTENSION; INFLAMMATION; LIVER DISEASE; NONHUMAN; PHOX-BEM1 PROTEIN INTERACTION DOMAIN; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; THROMBOSIS; VASCULAR DISEASE; METABOLISM; PATHOLOGY; PROTEIN TERTIARY STRUCTURE;

CARDIOVASCULAR DISEASES; ENDOTHELIAL CELLS; HUMANS; PROTEIN STRUCTURE, TERTIARY;

EID: 84928546440     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2014.6182     Document Type: Review

References (109)

1. Asakura T and Karino T. Flow patterns and spatial distribution of atherosclerotic lesions in human coronary arteries. Circ Res 66: 1045-1066, 1990.
2. Bae SH, Sung SH, Oh SY, Lim JM, Lee SK, Park YN, Lee HE, Kang D, and Rhee SG. Sestrins activate Nrf2 by promoting p62-dependent autophagic degradation of Keap1 and prevent oxidative liver damage. Cell Metab 17: 73-84, 2013.
3. Beutner F, Brendel D, Teupser D, Sass K, Baber R, Mueller M, Ceglarek U, and Thiery J. Effect of everolimus on pre-existing atherosclerosis in LDL-receptor deficient mice. Atherosclerosis 222: 337-343, 2012.
4. Bilder D, Schober M, and Perrimon N. Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat Cell Biol 5: 53-58, 2003.
5. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, and Johansen T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171: 603-614, 2005.
6. Bobryshev YV, Shchelkunova TA, Morozov IA, Rubtsov PM, Sobenin IA, Orekhov AN, and Smirnov AN. Changes of lysosomes in the earliest stages of the development of atherosclerosis. J Cell Mol Med 17: 626-635, 2013.
7. Bose R and Wrana JL. Regulation of Par6 by extracellular signals. Curr Opin Cell Biol 18: 206-212, 2006.
8. Brandes RP. Vascular functions of NADPH oxidases. Hypertension 56: 17-21, 2010.
9. Brandes RP, Weissmann N, and Schroder K. NADPH oxidases in cardiovascular disease. Free Radic Biol Med 49: 687-706, 2010.
10. Brandes RP, Weissmann N, and Schroder K. Nox family NADPH oxidases in mechano-transduction: mechanisms and consequences. Antioxid Redox Signal 20: 887-898, 2014.
11. Brandes RP, Weissmann N, and Schroder K. Redox-mediated signal transduction by cardiovascular Nox NADPH oxidases. J Mol Cell Cardiol 73C: 70-79, 2014.
12. Brichkina A and Bulavin DV. WIP-ing out atherosclerosis with autophagy. Autophagy 8: 1545-1547, 2012.
13. Bruning A. Inhibition of mTOR signaling by quercetin in cancer treatment and prevention. Anticancer Agents Med Chem 13: 1025-1031, 2013.
14. Bryant DM and Mostov KE. From cells to organs: building polarized tissue. Nat Rev Mol Cell Biol 9: 887-901, 2008.
15. Bulotta S, Cerullo A, Barsacchi R, De Palma C, Rotiroti D, Clementi E, and Borgese N. Endothelial nitric oxide synthase is segregated from caveolin-1 and localizes to the leading edge of migrating cells. Exp Cell Res 312: 877-889, 2006.
16. Caro CG, Fitz-Gerald JM, and Schroter RC. Arterial wall shear and distribution of early atheroma in man. Nature 223: 1159-1160, 1969.
17. Chalmers AD, Pambos M, Mason J, Lang S, Wylie C, and Papalopulu N. aPKC, Crumbs3 and Lgl2 control apicobasal polarity in early vertebrate development. Development 132: 977-986, 2005.
18. Chan JR, Jolicoeur C, Yamauchi J, Elliott J, Fawcett JP, Ng BK, and Cayouette M. The polarity protein Par-3 directly interacts with p75NTR to regulate myelination. Science 314: 832-836, 2006.
19. Chen J and Zhang M. The Par3/Par6/aPKC complex and epithelial cell polarity. Exp Cell Res 319: 1357-1364, 2013.
20. Conway DE, Breckenridge MT, Hinde E, Gratton E, Chen CS, and Schwartz MA. Fluid shear stress on endothelial cells modulates mechanical tension across VE-cadherin and PECAM-1. Curr Biol 23: 1024-1030, 2013.
21. Copple IM, Lister A, Obeng AD, Kitteringham NR, Jenkins RE, Layfield R, Foster BJ, Goldring CE, and Park BK. Physical and functional interaction of sequestosome 1 with Keap1 regulates the Keap1-Nrf2 cell defense pathway. J Biol Chem 285: 16782-16788, 2010.
22. Dardik A, Chen L, Frattini J, Asada H, Aziz F, Kudo FA, and Sumpio BE. Differential effects of orbital and laminar shear stress on endothelial cells. J Vasc Surg 41: 869-880, 2005.
23. Davies PF. Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat Clin Pract Cardiovasc Med 6: 16-26, 2009.
24. Desai RA, Gao L, Raghavan S, Liu WF, and Chen CS. Cell polarity triggered by cell-cell adhesion via E-cadherin. J Cell Sci 122: 905-911, 2009.
25. Du F, Yu F, Wang Y, Hui Y, Carnevale K, Fu M, Lu H, and Fan D. MicroRNA-155 deficiency results in decreased macrophage inflammation and attenuated atherogenesis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 34: 759-767, 2014.
26. Duran A, Diaz-Meco MT, and Moscat J. Essential role of RelA Ser311 phosphorylation by zetaPKC in NF-kappaB transcriptional activation. EMBO J 22: 3910-3918, 2003.
27. Erdogan E, Lamark T, Stallings-Mann M, Lee J, Pellecchia M, Thompson EA, Johansen T, and Fields AP. Aurothiomalate inhibits transformed growth by targeting the PB1 domain of protein kinase Ciota. J Biol Chem 281: 28450-28459, 2006.
28. Fan LM, Teng L, and Li JM. Knockout of p47 phox uncovers a critical role of p40 phox in reactive oxygen species production in microvascular endothelial cells. Arterioscler Thromb Vasc Biol 29: 1651-1656, 2009.
29. Fan W, Tang Z, Chen D, Moughon D, Ding X, Chen S, Zhu M, and Zhong Q. Keap1 facilitates p62-mediated ubiquitin aggregate clearance via autophagy. Autophagy 6: 614-621, 2010.
30. Feng W, Wu H, Chan LN, and Zhang M. The Par-3 NTD adopts a PB1-like structure required for Par-3 oligomerization and membrane localization. EMBO J 26: 2786-2796, 2007.
31. Garin G, Abe J, Mohan A, Lu W, Yan C, Newby AC, Rhaman A, and Berk BC. Flow antagonizes TNF-alpha signaling in endothelial cells by inhibiting caspase-dependent PKC zeta processing. Circ Res 101: 97-105, 2007.
32. Garrard SM, Capaldo CT, Gao L, Rosen MK, Macara IG, and Tomchick DR. Structure of Cdc42 in a complex with the GTPase-binding domain of the cell polarity protein, Par6. EMBO J 22: 1125-1133, 2003.
33. Hamelers IH, Olivo C, Mertens AE, Pegtel DM, van der Kammen RA, Sonnenberg A, and Collard JG. The Rac activator Tiam1 is required for (alpha)3(beta)1-mediated laminin-5 deposition, cell spreading, and cell migration. J Cell Biol 171: 871-881, 2005.
34. Harhaj NS, Felinski EA, Wolpert EB, Sundstrom JM, Gardner TW, and Antonetti DA. VEGF activation of protein kinase C stimulates occludin phosphorylation and contributes to endothelial permeability. Invest Ophthalmol Vis Sci 47: 5106-5115, 2006.
35. Helmcke I, Heumuller S, Tikkanen R, Schroder K, and Brandes RP. Identification of structural elements in Nox1 and Nox4 controlling localization and activity. Antioxid Redox Signal 11: 1279-1287, 2009.
36. Heo KS, Chang E, Le NT, Cushman H, Yeh ET, Fujiwara K, and Abe J. De-SUMOylation enzyme of sentrin/SUMO-specific protease 2 regulates disturbed flow-induced SUMOylation of ERK5 and p53 that leads to endothelial dysfunction and atherosclerosis. Circ Res 112: 911-923, 2013.
37. Heo KS, Fujiwara K, and Abe JI. Shear stress and atherosclerosis. Mol Cells 37: 435-440, 2014.
38. Hsiai TK, Cho SK, Wong PK, Ing M, Salazar A, Sevanian A, Navab M, Demer LL, and Ho CM. Monocyte recruitment to endothelial cells in response to oscillatory shear stress. FASEB J 17: 1648-1657, 2003.
39. Hsu YJ, Hsu SC, Huang SM, Lee HS, Lin SH, Tsai CS, Shih CC, and Lin CY. Hyperphosphatemia induces protective autophagy in endothelial cells through the inhibition of Akt/mTOR signaling. J Vasc Surg pii: S0741-5214(14)00269-9, 2014.
40. Hurd TW and Margolis B. Pars and polarity: taking control of Rac. Nat Cell Biol 7: 205-207, 2005.
41. Ichimura Y, Waguri S, Sou YS, Kageyama S, Hasegawa J, Ishimura R, Saito T, Yang Y, Kouno T, Fukutomi T, Hoshii T, Hirao A, Takagi K, Mizushima T, Motohashi H, Lee MS, Yoshimori T, Tanaka K, Yamamoto M, and Komatsu M. Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy. Mol Cell 51: 618-631, 2013.
42. Ito T, Matsui Y, Ago T, Ota K, and Sumimoto H. Novel modular domain PB1 recognizes PC motif to mediate functional protein-protein interactions. EMBO J 20: 3938-3946, 2001.
43. Jain A, Lamark T, Sjottem E, Larsen KB, Awuh JA, Overvatn A, McMahon M, Hayes JD, and Johansen T. p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J Biol Chem 285: 22576-22591, 2010.
44. Joberty G, Petersen C, Gao L, and Macara IG. The cellpolarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol 2: 531-539, 2000.
45. Kim GY, Nigro P, Fujiwara K, Abe J, and Berk BC. p62 binding to protein kinase C zeta regulates tumor necrosis factor alpha-induced apoptotic pathway in endothelial cells. Arterioscler Thromb Vasc Biol 32: 2974-2980, 2012.
46. Kim JH, Jun HO, Yu YS, and Kim KW. Inhibition of protein kinase C delta attenuates blood-retinal barrier breakdown in diabetic retinopathy. Am J Pathol 176: 1517-1524, 2010.
47. Koga H, Terasawa H, Nunoi H, Takeshige K, Inagaki F, and Sumimoto H. Tetratricopeptide repeat (TPR) motifs of p67(phox) participate in interaction with the small GTPase Rac and activation of the phagocyte NADPH oxidase. J Biol Chem 274: 25051-25060, 1999.
48. Komatsu M, Kurokawa H, Waguri S, Taguchi K, Kobayashi A, Ichimura Y, Sou YS, Ueno I, Sakamoto A, Tong KI, Kim M, Nishito Y, Iemura S, Natsume T, Ueno T, Kominami E, Motohashi H, Tanaka K, and Yamamoto M. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol 12: 213-223, 2010.
49. Ku DN, Giddens DP, Zarins CK, and Glagov S. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis 5: 293-302, 1985.
50. Kuchler L, Giegerich AK, Sha LK, Knape T, Wong MS, Schroder K, Brandes RP, Heide H, Wittig I, Bruene B, and von Knethen A. SYNCRIP-dependent Nox2 mRNA destabilization impairs ROS formation in M2 polarized macrophages. Antioxid Redox Signal 20: 2483-2497, 2014.
51. Lamark T, Perander M, Outzen H, Kristiansen K, Overvatn A, Michaelsen E, Bjorkoy G, and Johansen T. Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins. J Biol Chem 278: 34568-34581, 2003.
52. Lapouge K, Smith SJ, Walker PA, Gamblin SJ, Smerdon SJ, and Rittinger K. Structure of the TPR domain of p67phox in complex with Rac.GTP. Mol Cell 6: 899-907, 2000.
53. Lau A, Wang XJ, Zhao F, Villeneuve NF, Wu T, Jiang T, Sun Z, White E, and Zhang DD. A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol Cell Biol 30: 3275-3285, 2010.
54. Lau A, Whitman SA, Jaramillo MC, and Zhang DD. Arsenic-mediated activation of the Nrf2-Keap1 antioxidant pathway. J Biochem Mol Toxicol 27: 99-105, 2013.
55. Lau A, Zheng Y, Tao S, Wang H, Whitman SA, White E, and Zhang DD. Arsenic inhibits autophagic flux, activating the Nrf2-Keap1 pathway in a p62-dependent manner. Mol Cell Biol 33: 2436-2446, 2013.
56. Le Guezennec X, Brichkina A, Huang YF, Kostromina E, Han W, and Bulavin DV. Wip1-dependent regulation of autophagy, obesity, and atherosclerosis. Cell Metab 16: 68-80, 2012.
57. Li JM, Mullen AM, Yun S, Wientjes F, Brouns GY, Thrasher AJ, and Shah AM. Essential role of the NADPH oxidase subunit p47(phox) in endothelial cell superoxide production in response to phorbol ester and tumor necrosis factor-alpha. Circ Res 90: 143-150, 2002.
58. Lin D, Edwards AS, Fawcett JP, Mbamalu G, Scott JD, and Pawson T. A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat Cell Biol 2: 540-547, 2000.
59. Liu Y, Collins C, Kiosses WB, Murray AM, Joshi M, Shepherd TR, Fuentes EJ, and Tzima E. A novel pathway spatiotemporally activates Rac1 and redox signaling in response to fluid shear stress. J Cell Biol 201: 863-873, 2013.
60. Macara IG. Parsing the polarity code. Nat Rev Mol Cell Biol 5: 220-231, 2004.
61. Magid R and Davies PF. Endothelial protein kinase C isoform identity and differential activity of PKCzeta in an athero-susceptible region of porcine aorta. Circ Res 97: 443-449, 2005.
62. Maiuri MC, Grassia G, Platt AM, Carnuccio R, Ialenti A, and Maffia P. Macrophage autophagy in atherosclerosis. Mediators Inflamm 2013: 584715, 2013.
63. Malek AM, Alper SL, and Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA 282: 2035-2042, 1999.
64. Martinet W, De Loof H, and De Meyer GR. mTOR inhibition: a promising strategy for stabilization of atherosclerotic plaques. Atherosclerosis 233: 601-607, 2014.
65. Menghini R, Casagrande V, Marino A, Marchetti V, Cardellini M, Stoehr R, Rizza S, Martelli E, Greco S, Mauriello A, Ippoliti A, Martelli F, Lauro R, and Federici M. MiR-216a: a link between endothelial dysfunction and autophagy. Cell Death Dis 5: e1029, 2014.
66. Mertens AE, Rygiel TP, Olivo C, van der Kammen R, and Collard JG. The Rac activator Tiam1 controls tight junction biogenesis in keratinocytes through binding to and activation of the Par polarity complex. J Cell Biol 170: 1029-1037, 2005.
67. Mizuno K and Ohno S. Regulation of epithelial cell polarity mediated by aPKC-PAR complex. Tanpakushitsu Kakusan Koso 51: 782-788, 2006.
68. Moscat J, Diaz-Meco MT, Albert A, and Campuzano S. Cell signaling and function organized by PB1 domain interactions. Mol Cell 23: 631-640, 2006.
69. Mueller MA, Beutner F, Teupser D, Ceglarek U, and Thiery J. Prevention of atherosclerosis by the mTOR inhibitor everolimus in LDLR-/- mice despite severe hypercholesterolemia. Atherosclerosis 198: 39-48, 2008.
70. Nagel T, Resnick N, Dewey CF, Jr., and Gimbrone MA, Jr. Vascular endothelial cells respond to spatial gradients in fluid shear stress by enhanced activation of transcription factors. Arterioscler Thromb Vasc Biol 19: 1825-1834, 1999.
71. Nakamura R, Sumimoto H, Mizuki K, Hata K, Ago T, Kitajima S, Takeshige K, Sakaki Y, and Ito T. The PC motif: a novel and evolutionarily conserved sequence involved in interaction between p40phox and p67phox, SH3 domain-containing cytosolic factors of the phagocyte NADPH oxidase. Eur J Biochem 251: 583-589, 1998.
72. Nezis IP and Stenmark H. p62 at the interface of autophagy, oxidative stress signaling, and cancer. Antioxid Redox Signal 17: 786-793, 2012.
73. Nigro P, Abe J, and Berk BC. Flow shear stress and atherosclerosis: a matter of site specificity. Antioxid Redox Signal 15: 1405-1414, 2011.
74. Nigro P, Abe J, Woo CH, Satoh K, McClain C, O'Dell MR, Lee H, Lim JH, Li JD, Heo KS, Fujiwara K, and Berk BC. PKCzeta decreases eNOS protein stability via inhibitory phosphorylation of ERK5. Blood 116: 1971-1979, 2010.
75. Nigro P, Satoh K, O'Dell MR, Soe NN, Cui Z, Mohan A, Abe J, Alexis JD, Sparks JD, and Berk BC. Cyclophilin A is an inflammatory mediator that promotes atherosclerosis in apolipoprotein E-deficient mice. J Exp Med 208: 53-66, 2011.
76. Noda Y, Kohjima M, Izaki T, Ota K, Yoshinaga S, Inagaki F, Ito T, and Sumimoto H. Molecular recognition in dimerization between PB1 domains. J Biol Chem 278: 43516-43524, 2003.
77. Ouimet M. Autophagy in obesity and atherosclerosis: interrelationships between cholesterol homeostasis, lipoprotein metabolism and autophagy in macrophages and other systems. Biochim Biophys Acta 1831: 1124-1133, 2013.
78. Pang J, Hoefen R, Pryhuber GS, Wang J, Yin G, White RJ, Xu X, O'Dell MR, Mohan A, Michaloski H, Massett MP, Yan C, and Berk BC. G-protein-coupled receptor kinase interacting protein-1 is required for pulmonary vascular development. Circulation 119: 1524-1532, 2009.
79. Parker PJ, Justilien V, Riou P, Linch M, and Fields AP. Atypical protein kinase Ciota as a human oncogene and therapeutic target. Biochem Pharmacol 88: 1-11, 2014.
80. Peterson J, Zheng Y, Bender L, Myers A, Cerione R, and Bender A. Interactions between the bud emergence proteins Bem1p and Bem2p and Rho-type GTPases in yeast. J Cell Biol 127: 1395-1406, 1994.
81. Razani B, Feng C, Coleman T, Emanuel R, Wen H, Hwang S, Ting JP, Virgin HW, Kastan MB, and Semenkovich CF. Autophagy links inflammasomes to atherosclerotic progression. Cell Metab 15: 534-544, 2012.
82. Regala RP, Thompson EA, and Fields AP. Atypical protein kinase C iota expression and aurothiomalate sensitivity in human lung cancer cells. Cancer Res 68: 5888-5895, 2008.
83. Regala RP, Weems C, Jamieson L, Copland JA, Thompson EA, and Fields AP. Atypical protein kinase Ciota plays a critical role in human lung cancer cell growth and tumorigenicity. J Biol Chem 280: 31109-31115, 2005.
84. Ren J, Wang J, Wang Z, and Wu J. Structural and biochemical insights into the homotypic PB1-PB1 complex between PKCzeta and p62. Sci China Life Sci 57: 69-80, 2014.
85. Robinet P, Ritchey B, and Smith JD. Physiological difference in autophagic flux in macrophages from 2 mouse strains regulates cholesterol ester metabolism. Arterioscler Thromb Vasc Biol 33: 903-910, 2013.
86. Schroder K, Zhang M, Benkhoff S, Mieth A, Pliquett R, Kosowski J, Kruse C, Luedike P, Michaelis UR, Weissmann N, Dimmeler S, Shah AM, and Brandes RP. Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circ Res 110: 1217-1225, 2012.
87. Schweisguth F. Cell polarity and asymmetric division in the peripheral nervous system of Drosophila. J Soc Biol 197: 17-22, 2003.
88. Shrimali D, Shanmugam MK, Kumar AP, Zhang J, Tan BK, Ahn KS, and Sethi G. Targeted abrogation of diverse signal transduction cascades by emodin for the treatment of inflammatory disorders and cancer. Cancer Lett 341: 139-149, 2013.
89. Smith L, Chen L, Reyland ME, DeVries TA, Talanian RV, Omura S, and Smith JB. Activation of atypical protein kinase C zeta by caspase processing and degradation by the ubiquitin-proteasome system. J Biol Chem 275: 40620-40627, 2000.
90. Smith L, Wang Z, and Smith JB. Caspase processing activates atypical protein kinase C zeta by relieving autoinhibition and destabilizes the protein. Biochem J 375: 663-671, 2003.
91. Song HB, Jun HO, Kim JH, Yu YS, and Kim KW. Suppression of protein kinase C-zeta attenuates vascular leakage via prevention of tight junction protein decrease in diabetic retinopathy. Biochem Biophys Res Commun 444: 63-68, 2014.
92. Sorescu GP, Song H, Tressel SL, Hwang J, Dikalov S, Smith DA, Boyd NL, Platt MO, Lassegue B, Griendling KK, and Jo H. Bone morphogenic protein 4 produced in endothelial cells by oscillatory shear stress induces monocyte adhesion by stimulating reactive oxygen species production from a nox1-based NADPH oxidase. Circ Res 95: 773-779, 2004.
93. Sumimoto H, Kamakura S, and Ito T. Structure and function of the PB1 domain, a protein interaction module conserved in animals, fungi, amoebas, and plants. Sci STKE 2007: re6, 2007.
94. Suzuki A and Ohno S. The PAR-aPKC system: lessons in polarity. J Cell Sci 119: 979-987, 2006.
95. Taguchi K, Fujikawa N, Komatsu M, Ishii T, Unno M, Akaike T, Motohashi H, and Yamamoto M. Keap1 degradation by autophagy for the maintenance of redox homeostasis. Proc Natl Acad Sci U S A 109: 13561-13566, 2012.
96. Tarantino G and Capone D. Inhibition of the mTOR pathway: a possible protective role in coronary artery disease. Ann Med 45: 348-356, 2013.
97. Ushio-Fukai M. Compartmentalization of redox signaling through NADPH oxidase-derived ROS. Antioxid Redox Signal 11: 1289-1299, 2009.
98. Wang XQ, Nigro P, World C, Fujiwara K, Yan C, and Berk BC. Thioredoxin interacting protein promotes endothelial cell inflammation in response to disturbed flow by increasing leukocyte adhesion and repressing Kruppel-like factor 2. Circ Res 110: 560-568, 2012.
99. Wei DH, Jia XY, Liu YH, Guo FX, Tang ZH, Li XH, Wang Z, Liu LS, Wang GX, Jian ZS, and Ruan CG. Cathepsin L stimulates autophagy and inhibits apoptosis of ox-LDL-induced endothelial cells: potential role in atherosclerosis. Int J Mol Med 31: 400-406, 2013.
100. Wilson MI, Gill DJ, Perisic O, Quinn MT, and Williams RL. PB1 domain-mediated heterodimerization in NADPH oxidase and signaling complexes of atypical protein kinase C with Par6 and p62. Mol Cell 12: 39-50, 2003.
101. Wootton DM, and Ku DN. Fluid mechanics of vascular systems, diseases, and thrombosis. Annu Rev Biomed Eng 1: 299-329, 1999.
102. Yamaguchi Y, Ota K, and Ito T. A novel Cdc42-interacting domain of the yeast polarity establishment protein Bem1. Implications for modulation of mating pheromone signaling. J Biol Chem 282: 29-38, 2007.
103. Yamanaka T, Horikoshi Y, Suzuki A, Sugiyama Y, Kitamura K, Maniwa R, Nagai Y, Yamashita A, Hirose T, Ishikawa H, and Ohno S. PAR-6 regulates aPKC activity in a novel way and mediates cell-cell contact-induced formation of the epithelial junctional complex. Genes Cells 6: 721-731, 2001.
104. Yang Z and Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 12: 814-822, 2010.
105. Yun S, Dardik A, Haga M, Yamashita A, Yamaguchi S, Koh Y, Madri JA, and Sumpio BE. Transcription factor Sp1 phosphorylation induced by shear stress inhibits membrane type 1-matrix metalloproteinase expression in endothelium. J Biol Chem 277: 34808-34814, 2002.
106. Zarins CK, Giddens DP, Bharadvaj BK, Sottiurai VS, Mabon RF, and Glagov S. Carotid bifurcation atherosclerosis. Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ Res 53: 502-514, 1983.
107. Zhang M, Brewer AC, Schroder K, Santos CX, Grieve DJ, Wang M, Anilkumar N, Yu B, Dong X, Walker SJ, Brandes RP, and Shah AM. NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. Proc Natl Acad Sci U S A 107: 18121-18126, 2010.
108. Zhaorigetu S, Yang Z, Toma I, McCaffrey TA, and Hu CA. Apolipoprotein L6, induced in atherosclerotic lesions, promotes apoptosis and blocks Beclin 1-dependent autophagy in atherosclerotic cells. J Biol Chem 286: 27389-27398, 2011.
109. Ziegler T, Bouzourene K, Harrison VJ, Brunner HR, and Hayoz D. Influence of oscillatory and unidirectional flow environments on the expression of endothelin and nitric oxide synthase in cultured endothelial cells. Arterioscler Thromb Vasc Biol 18: 686-692, 1998.