Home LiteratureArticle Details
PMID: 15696199 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Fluid shear stress inhibits vascular inflammation by decreasing thioredoxin-interacting protein in endothelial cells.

The Journal of clinical investigation ·Vol. 115 ·No. 3 ·2005-03-00 ·Pages 733-8

Yamawaki H, Pan S, Lee RT, Berk BC

Abstract

Regions in the vasculature that are exposed to steady laminar blood flow are protected from atherosclerosis as compared with regions where flow is disturbed. We found that flow decreased TNF-mediated VCAM1 expression by inhibiting JNK and p38. JNK inhibition correlated with inhibition of apoptosis signal-regulating kinase 1 (ASK1), a JNK and p38 activator. Thioredoxin-interacting protein (TXNIP) is a stress-responsive protein that inhibits thioredoxin (TRX) activity. Since thioredoxin inhibits ASK1, we hypothesized that changes in TXNIP-TRX-ASK1 interactions mediate the antiinflammatory effects of flow. To explore this, we used perfused vessels and cultured ECs. Exposure of rabbit aortae or ECs to normal flow (12 dyn/cm2, 24 hours) was associated with decreased TXNIP expression and increased TRX activity compared with exposure to low flow (0.4 dyn/cm2). Normal flow inhibited TNF activation of JNK/p38 and VCAM1 expression. In cultured ECs, reduction of TXNIP expression by small interfering RNA increased TRX binding to ASK1 and inhibited TNF activation of JNK/p38 and VCAM1 expression. Conversely, overexpression of TXNIP stimulated JNK and p38. In aortae from TXNIP-deficient mice, TNF-induced VCAM1 expression was inhibited. The data suggest that TXNIP and TRX are key components of biomechanical signal transduction and establish them as potentially novel regulators of TNF signaling and inflammation in ECs.

MeSH Terms
Animals Aorta/cytology,immunology,pathology Blood Flow Velocity Carrier Proteins/genetics,metabolism Cells, Cultured Endothelial Cells/cytology,metabolism Enzyme Activation In Vitro Techniques Inflammation/metabolism JNK Mitogen-Activated Protein Kinases/metabolism Mice RNA, Small Interfering/genetics,metabolism Rabbits Shear Strength Signal Transduction/physiology Stress, Mechanical Thioredoxins/metabolism Tumor Necrosis Factor-alpha/metabolism Vascular Cell Adhesion Molecule-1/metabolism p38 Mitogen-Activated Protein Kinases/metabolism
Chemicals
Carrier Proteins RNA, Small Interfering Tumor Necrosis Factor-alpha Vascular Cell Adhesion Molecule-1 Thioredoxins JNK Mitogen-Activated Protein Kinases p38 Mitogen-Activated Protein Kinases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Yamawaki Hideyuki
Center for Cardiovascular Research, University of Rochester, Rochester, New York 14642, USA.
Pan Shi
Lee Richard T
Berk Bradford C
References (25)
25 references, click to expand
  1. Vitamin D3 up-regulated protein 1 mediates oxidative stress via suppressing the thioredoxin function.
    J Immunol. 2000 Jun 15;164(12):6287-95 PMID: 10843682
  2. Identification of thioredoxin-binding protein-2/vitamin D(3) up-regulated protein 1 as a negative regulator of thioredoxin function and expression.
    J Biol Chem. 1999 Jul 30;274(31):21645-50 PMID: 10419473
  3. Pulsatile stretch-induced extracellular signal-regulated kinase 1/2 activation in organ culture of rabbit aorta involves reactive oxygen species.
    Arterioscler Thromb Vasc Biol. 2000 Nov;20(11):2366-72 PMID: 11073839
  4. Laminar flow inhibits TNF-induced ASK1 activation by preventing dissociation of ASK1 from its inhibitor 14-3-3.
    J Clin Invest. 2001 Apr;107(7):917-23 PMID: 11285311
  5. Fluid shear stress inhibits TNF-alpha activation of JNK but not ERK1/2 or p38 in human umbilical vein endothelial cells: Inhibitory crosstalk among MAPK family members.
    Proc Natl Acad Sci U S A. 2001 May 22;98(11):6476-81 PMID: 11353829
  6. Positional cloning of the combined hyperlipidemia gene Hyplip1.
    Nat Genet. 2002 Jan;30(1):110-6 PMID: 11753387
  7. Vitamin D(3)-up-regulated protein-1 is a stress-responsive gene that regulates cardiomyocyte viability through interaction with thioredoxin.
    J Biol Chem. 2002 Jul 19;277(29):26496-500 PMID: 12011048
  8. Vitamin D3-upregulated protein-1 (VDUP-1) regulates redox-dependent vascular smooth muscle cell proliferation through interaction with thioredoxin.
    Circ Res. 2002 Oct 18;91(8):689-95 PMID: 12386145
  9. Fluid shear stress attenuates hydrogen peroxide-induced c-Jun NH2-terminal kinase activation via a glutathione reductase-mediated mechanism.
    Circ Res. 2002 Oct 18;91(8):712-8 PMID: 12386148
  10. Role of glutaredoxin in metabolic oxidative stress. Glutaredoxin as a sensor of oxidative stress mediated by H2O2.
    J Biol Chem. 2002 Nov 29;277(48):46566-75 PMID: 12244106
  11. VDUP1 upregulated by TGF-beta1 and 1,25-dihydorxyvitamin D3 inhibits tumor cell growth by blocking cell-cycle progression.
    Oncogene. 2003 Jun 26;22(26):4035-46 PMID: 12821938
  12. Shear stress increases the amount of S-nitrosylated molecules in endothelial cells: important role for signal transduction.
    FEBS Lett. 2003 Sep 11;551(1-3):153-8 PMID: 12965221
  13. Chronic physiological shear stress inhibits tumor necrosis factor-induced proinflammatory responses in rabbit aorta perfused ex vivo.
    Circulation. 2003 Sep 30;108(13):1619-25 PMID: 12963644
  14. Thioredoxin: a key regulator of cardiovascular homeostasis.
    Circ Res. 2003 Nov 28;93(11):1029-33 PMID: 14645133
  15. Big mitogen-activated protein kinase (BMK1)/ERK5 protects endothelial cells from apoptosis.
    Circ Res. 2004 Feb 20;94(3):362-9 PMID: 14670836
  16. Thioredoxin-interacting protein controls cardiac hypertrophy through regulation of thioredoxin activity.
    Circulation. 2004 Jun 1;109(21):2581-6 PMID: 15123525
  17. Hyperglycemia promotes oxidative stress through inhibition of thioredoxin function by thioredoxin-interacting protein.
    J Biol Chem. 2004 Jul 16;279(29):30369-74 PMID: 15128745
  18. Isolation and characterization of a novel cDNA from HL-60 cells treated with 1,25-dihydroxyvitamin D-3.
    Biochim Biophys Acta. 1994 Sep 13;1219(1):26-32 PMID: 8086474
  19. Differential effects of pressure and flow on DNA and protein synthesis and on fibronectin expression by arteries in a novel organ culture system.
    Circ Res. 1995 Oct;77(4):684-94 PMID: 7554114
  20. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways.
    Science. 1997 Jan 3;275(5296):90-4 PMID: 8974401
  21. Mapping a gene for combined hyperlipidaemia in a mutant mouse strain.
    Nat Genet. 1998 Apr;18(4):374-7 PMID: 9537422
  22. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1.
    EMBO J. 1998 May 1;17(9):2596-606 PMID: 9564042
  23. Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force.
    Arterioscler Thromb Vasc Biol. 1998 May;18(5):677-85 PMID: 9598824
  24. Atherosclerosis--an inflammatory disease.
    N Engl J Med. 1999 Jan 14;340(2):115-26 PMID: 9887164
  25. Endothelial dysfunction, hemodynamic forces, and atherogenesis.
    Ann N Y Acad Sci. 2000 May;902:230-9; discussion 239-40 PMID: 10865843
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2005-03-00
Pages
733-8
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC546457
Subset
IM
Grants
NHLBI NIH HHS · R01 HL064839 · United States
NHLBI NIH HHS · HL64839 · United States
NHLBI NIH HHS · HL62826 · United States
NHLBI NIH HHS · P01 HL064858 · United States
NHLBI NIH HHS · HL64858 · United States
NHLBI NIH HHS · R01 HL062826 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com