Migration of smooth muscle cells from the arterial anastomosis of arteriovenous fistulas requires Notch activation to form neointima

Kidney International

Volumn 88, Issue 3, 2015, Pages 490-502

  Liang, Ming ^a,b   Wang, Yun ^b   Liang, Anlin ^b   Mitch, William E ^b   Roy Chaudhury, Prabir ^c   Han, Guofeng ^b,d   Cheng, Jizhong ^b  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF CINCINNATI   (United States)

^d PLA 455th Hospital   (China)

Author keywords

arteriovenous fistula; chronic kidney disease; fibroblast specific protein 1; neointima formation; Notch; vascular smooth muscle cell

Indexed keywords

CALVASCULIN; NOTCH RECEPTOR; NOTCH1 RECEPTOR; RBP JK PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WNT1 PROTEIN; CALCIUM BINDING PROTEIN; FSP1 PROTEIN, HUMAN; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; NOTCH1 PROTEIN, HUMAN; NOTCH1 PROTEIN, MOUSE; PROTEIN S 100; RBPJ PROTEIN, HUMAN; RBPJ PROTEIN, MOUSE; S100A4 PROTEIN, MOUSE;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOVENOUS FISTULA; ARTERY ANASTOMOSIS; ARTICLE; BINDING AFFINITY; CELL ACTIVATION; CELL MIGRATION; CLINICAL ARTICLE; COMMON CAROTID ARTERY; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; JUGULAR VEIN; MALE; MOUSE; NEOINTIMA; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TRANSCRIPTION REGULATION; VASCULAR PATENCY; ADVERSE EFFECTS; ANIMAL; ARTERIOVENOUS SHUNT; BLOOD VESSEL TRANSPLANTATION; CELL CULTURE; CELL MOTION; DEVICES; GENETIC TRANSFECTION; GENETICS; GRAFT OCCLUSION, VASCULAR; HEMODIALYSIS; METABOLISM; MIDDLE AGED; PATHOLOGY; RENAL INSUFFICIENCY, CHRONIC; RNA INTERFERENCE; SMOOTH MUSCLE CELL; SURGERY; TRANSGENIC MOUSE; VASCULAR SMOOTH MUSCLE;

AGED; ANIMALS; ARTERIOVENOUS SHUNT, SURGICAL; BLOOD VESSEL PROSTHESIS IMPLANTATION; CALCIUM-BINDING PROTEINS; CAROTID ARTERY, COMMON; CELL MOVEMENT; CELLS, CULTURED; GRAFT OCCLUSION, VASCULAR; HUMANS; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; JUGULAR VEINS; MALE; MICE, TRANSGENIC; MIDDLE AGED; MODELS, ANIMAL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA; RECEPTOR, NOTCH1; RENAL DIALYSIS; RENAL INSUFFICIENCY, CHRONIC; RNA INTERFERENCE; S100 CALCIUM-BINDING PROTEIN A4; S100 PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION; VASCULAR PATENCY;

EID: 84940797293     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2015.73     Document Type: Article

References (54)

1. Roy-Chaudhury P, Sukhatme VP, Cheung AK. Hemodialysis vascular access dysfunction: a cellular and molecular viewpoint. J Am Soc Nephrol. 2006; 17: 1112-1127.
2. Allon M, Robbin ML. Increasing arteriovenous fistulas in hemodialysis patients: problems and solutions. Kidney Int. 2002; 62: 1109-1124.
3. Dember LM, Susztak K. Notch ties a knot on fistula maturation. J Am Soc Nephrol. 2014; 25: 648-650.
4. Caplice NM, Wang S, Tracz M, et al. Neoangiogenesis and the presence of progenitor cells in the venous limb of an arteriovenous fistula in the rat. Am J Physiol Renal Physiol. 2007; 293: F470-F475.
5. Tanaka K, Sata M, Natori T, et al. Circulating progenitor cells contribute to neointimal formation in nonirradiated chimeric mice. FASEB J. 2008; 22: 428-436.
6. Arciniegas E, Frid MG, Douglas IS, et al. Perspectives on endothelial-Tomesenchymal transition: potential contribution to vascular remodeling in chronic pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2007; 293: L1-L8.
7. Bentzon JF, Weile C, Sondergaard CS, et al. Smooth muscle cells in atherosclerosis originate from the local vessel wall and not circulating progenitor cells in apoe knockout mice. Arterioscler Thromb Vasc Biol. 2006; 26: 2696-2702.
8. Hoofnagle MH, Thomas JA, Wamhoff BR, et al. Origin of neointimal smooth muscle: we've come full circle. Arterioscler Thromb Vasc Biol. 2006; 26: 2579-2581.
9. Hu Y, Zhang Z, Torsney E, et al. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in apoe-deficient mice. J Clin Invest. 2004; 113: 1258-1265.
10. Shi Y, O'Brien JE Jr, Mannion JD, et al. Remodeling of autologous saphenous vein grafts. The role of perivascular myofibroblasts. Circulation. 1997; 95: 2684-2693.
11. Jiang X, Rowitch DH, Soriano P, et al. Fate of the mammalian cardiac neural crest. Development. 2000; 127: 1607-1616.
12. Echelard Y, Vassileva G, McMahon AP. Cis-Acting regulatory sequences governing wnt-1 expression in the developing mouse cns. Development. 1994; 120: 2213-2224.
13. Hutson MR, Kirby ML. Model systems for the study of heart development and disease. Cardiac neural crest and conotruncal malformations. Semin Cell Dev Biol. 2007; 18: 101-110.
14. Waldo KL, Kumiski D, Kirby ML. Cardiac neural crest is essential for the persistence rather than the formation of an arch artery. Dev Dyn. 1996; 205: 281-292.
15. Kokubo T, Ishikawa N, Uchida H, et al. Ckd accelerates development of neointimal hyperplasia in arteriovenous fistulas. J Am Soc Nephrol. 2009; 20: 1236-1245.
16. Liang A, Wang Y, Han G, et al. Chronic kidney disease accelerates endothelial barrier dysfunction in a mouse model of an arteriovenous fistula. Am J Physiol Renal Physiol. 2013; 304: F1413-F1420.
17. Spiekerkoetter E, Guignabert C, de Jesus Perez V, et al. S100a4 and bone morphogenetic protein-2 codependently induce vascular smooth muscle cell migration via phospho-extracellular signal-regulated kinase and chloride intracellular channel 4. Circ Res. 2009; 105: 639-647.
18. Cheng J, Wang Y, Liang A, et al. Fsp-1 silencing in bone marrow cells suppresses neointima formation in vein graft. Circ Res. 2012; 110: 230-240.
19. Wang Y, Liang A, Luo J, et al. Blocking notch in endothelial cells prevents arteriovenous fistula failure despite ckd. J Am Soc Nephrol. 2014; 25: 773-783.
20. Li Y, Takeshita K, Liu P-Y, et al. Smooth muscle notch1 mediates neointimal formation after vascular injury. Circ Res. 2009; 119: 2686-2692.
21. Sakata Y, Xiang F, Chen Z, et al. Transcription factor chf1/hey2 regulates neointimal formation in vivo and vascular smooth muscle proliferation and migration in vitro. Athro Throm Vasc Biol. 2004; 24: 2069-2074.
22. Tang Y, Urs S, Boucher J, et al. Notch and transforming growth factor-beta (tgfbeta) signaling pathways cooperatively regulate vascular smooth muscle cell differentiation. J Biol Chem. 2010; 285: 17556-17563.
23. Valdez Joseph M, Zhang L, Su Q, et al. Notch and tgfb1 form a reciprocal positive regulatory loop that suppresses murine prostate basal stem/ progenitor cell activity. Cell Stem Cell. 2012; 11: 676-688.
24. Roy-Chaudhury P, Wang Y, Krishnamoorthy M, et al. Cellular phenotypes in human stenotic lesions from haemodialysis vascular access. Nephrol Dial Transplant. 2009; 24: 2786-2791.
25. Dember LM. Fistulas first-but can they last?. Clin J Am Soc Nephrol. 2011; 6: 463-464.
26. Roy-Chaudhury P, Arend L, Zhang J, et al. Neointimal hyperplasia in early arteriovenous fistula failure. Am J Kidney Dis. 2007; 50: 782-790.
27. Hagensen MK, Shim J, Falk E, et al. Flanking recipient vasculature, not circulating progenitor cells, contributes to endothelium and smooth muscle in murine allograft vasculopathy. Arterioscler Thromb Vasc Biol. 2011; 31: 808-813.
28. Tanaka K, Sata M, Hirata Y, et al. Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries. Circ Res. 2003; 93: 783-790.
29. Daniel J-M, Bielenberg W, Stieger P, et al. Time-course analysis on the differentiation of bone marrow-derived progenitor cells into smooth muscle cells during neointima formation. Arthro Throm Vascul Biol. 2010; 30: 1890-1896.
30. Diao Y, Guthrie S, Xia SL, et al. Long-Term engraftment of bone marrowderived cells in the intimal hyperplasia lesion of autologous vein grafts. Am J Pathol. 2008; 172: 839-848.
31. Skartsis N, Manning E, Wei Y, et al. Origin of neointimal cells in arteriovenous fistulae: bone marrow, artery, or the vein itself?. Semin Dial. 2011; 24: 242-248.
32. Yang B, Janardhanan R, Vohra P, et al. Adventitial transduction of lentivirus-shrna-vegf-A in arteriovenous fistula reduces venous stenosis formation. Kidney Int. 2014; 85: 289-306.
33. Shi Y, O'Brien JE, Fard A, et al. Adventitial myofibroblasts contribute to neointimal formation in injured porcine coronary arteries. Circulation. 1996; 94: 1655-1664.
34. Forbes MS, Thornhill BA, Chevalier RL. Proximal tubular injury and rapid formation of atubular glomeruli in mice with unilateral ureteral obstruction: a new look at an old model. Am J Physiol Renal Physiol. 2011; 301: F110-F117.
35. Ivaska J, Pallari HM, Nevo J, et al. Novel functions of vimentin in cell adhesion, migration, and signaling. Exp Cell Res. 2007; 313: 2050-2062.
36. Kreis S, Schonfeld HJ, Melchior C, et al. The intermediate filament protein vimentin binds specifically to a recombinant integrin alpha2/beta1 cytoplasmic tail complex and co-localizes with native alpha2/beta1 in endothelial cell focal adhesions. Exp Cell Res. 2005; 305: 110-121.
37. Dave JM, Bayless KJ. Vimentin as an integral regulator of cell adhesion and endothelial sprouting. Microcirculation. 2014; 21: 333-344.
38. Nieminen M, Henttinen T, Merinen M, et al. Vimentin function in lymphocyte adhesion and transcellular migration. Nat Cell Biol. 2006; 8: 156-162.
39. Cai WJ, Koltai S, Kocsis E, et al. Remodeling of the adventitia during coronary arteriogenesis. Am J Physiol Heart Circ Physiol. 2003; 284: H31-H40.
40. Li ZH, Bresnick AR. The s100a4 metastasis factor regulates cellular motility via a direct interaction with myosin-iia. Cancer Res. 2006; 66: 5173-5180.
41. Yammani RR, Carlson CS, Bresnick AR, et al. Increase in production of matrix metalloproteinase 13 by human articular chondrocytes due to stimulation with s100a4: role of the receptor for advanced glycation end products. Arthritis Rheum. 2006; 54: 2901-2911.
42. Bjornland K, Winberg JO, Odegaard OT, et al. S100a4 involvement in metastasis: deregulation of matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases in osteosarcoma cells transfected with an anti-s100a4 ribozyme. Cancer Res. 1999; 59: 4702-4708.
43. Brisset AC, Hao H, Camenzind E, et al. Intimal smooth muscle cells of porcine and human coronary artery express s100a4, a marker of the rhomboid phenotype in vitro. Circ Res. 2007; 100: 1055-1062.
44. Caolo V, Schulten HM, Zhuang ZW, et al. Soluble jagged-1 inhibits neointima formation by attenuating notch-herp2 signaling. Arterioscler Thromb Vasc Biol. 2011; 31: 1059-1065.
45. Chen M, Sinha M, Luxon BA, et al. Integrin alpha6beta4 controls the expression of genes associated with cell motility, invasion, and metastasis, including s100a4/metastasin. J Biol Chem. 2009; 284: 1484-1494.
46. Chen M, Sastry SK, O'Connor KL. Src kinase pathway is involved in nfat5-mediated s100a4 induction by hyperosmotic stress in colon cancer cells. Am J Physiol Cell Physiol. 2011; 300: C1155-C1163.
47. Lawrie A, Spiekerkoetter E, Martinez EC, et al. Interdependent serotonin transporter and receptor pathways regulate s100a4/mts1, a gene associated with pulmonary vascular disease. Circ Res. 2005; 97: 227-235.
48. Wong CY, de Vries MR, Wang Y, et al. Vascular remodeling and intimal hyperplasia in a novel murine model of arteriovenous fistula failure. J Vasc Surg. 2014; 59: e191.
49. Zhang L, Wang XH, Wang H, et al. Satellite cell dysfunction and impaired igf-1 signaling cause ckd-induced muscle atrophy. J Am Soc Nephrol. 2010; 21: 419-427.
50. Zhang L, Rajan V, Lin E, et al. Pharmacological inhibition of myostatin suppresses systemic inflammation and muscle atrophy in mice with chronic kidney disease. FASEB J. 2011; 25: 1653-1663.
51. Cheng J, Truong LD, Wu X, et al. Serum- And glucocorticoid-regulated kinase 1 is upregulated following unilateral ureteral obstruction causing epithelial-mesenchymal transition. Kidney Int. 2010; 78: 668-678.
52. Wu X, Cheng J, Li P, et al. Mechano-sensitive transcriptional factor egr-1 regulates insulin-like growth factor-1 receptor xpression and contributes to neointima formation in vein grafts. Arterioscler Thromb Vasc Biol. 2009; 30: 471-476.
53. Ranjzad P, Salem HK, Kingston PA. Adenovirus-mediated gene transfer of fibromodulin inhibits neointimal hyperplasia in an organ culture model of human saphenous vein graft disease. Gene Therapy. 2009; 16: 1154-1162.
54. Cheng J, Wang Y, Ma Y, et al. The mechanical stress-Activated serum-, glucocorticoid-regulated kinase 1 contributes to neointima formation in vein grafts. Circ Res. 2010; 107: 1265-1274.