Heparan sulfate proteoglycan mediates shear stress-induced endothelial gene expression in mouse embryonic stem cell-derived endothelial cells

Biotechnology and Bioengineering

Volumn 109, Issue 2, 2012, Pages 583-594

  Nikmanesh, Maria ^a   Shi, Zhong Dong ^a,b   Tarbell, John M ^a  

^a City University of New York   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Embryonic stem cell; Endothelial cell; Glycoclayx; Heparan sulfate proteoglycan; Mechanotransduction; Shear stress

Indexed keywords

CELL SURFACES; EMBRYONIC STEM CELLS; EMBRYONIC STEMS; GLYCOCLAYX; HEPARAN SULFATES; IMMUNOSTAINING; MARKER GENES; MECHANOTRANSDUCTION; PROTEIN GENES; PROTEOGLYCANS; STRESS EFFECTS; STRESS MODULATION; STRESS-INDUCED; TIGHT JUNCTIONS; UNDERLYING MECHANISM; VE-CADHERIN;

CELL MEMBRANES; ENDOTHELIAL CELLS; GLYCOPROTEINS; SHEAR FLOW; SHEAR STRESS; STEM CELLS; SULFUR COMPOUNDS;

GENE EXPRESSION;

CD31 ANTIGEN; CHONDROITIN SULFATE; CLD5 PROTEIN; CYCLOOXYGENASE 2; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; GLYCOSAMINOGLYCAN; HEPARIN LYASE; HYALURONIC ACID; LOW DENSITY LIPOPROTEIN; OCLD PROTEIN; PROTEIN ZO1; PROTEOHEPARAN SULFATE; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VON WILLEBRAND FACTOR;

ANIMAL CELL; ARTICLE; CELL DIVISION; CELL SURFACE; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN LOCALIZATION; SHEAR STRESS; TIGHT JUNCTION;

ANIMALS; BIOMECHANICS; CARRIER PROTEINS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HEPARAN SULFATE PROTEOGLYCANS; HISTOCYTOCHEMISTRY; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE PROTEINS; MICE; POLYSACCHARIDE-LYASES; STRESS, MECHANICAL;

EID: 83455218129     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.23302     Document Type: Article

References (56)

1. Adamo L, Naveiras O, Wenzel PL, McKinney-Freeman S, Mack PJ, Gracia-Sancho J, Suchy-Dicey A, Yoshimoto M, Lensch MW, Yoder MC, Garcia-Cardena G, Daley GQ. 2009. Biomechanical forces promote embryonic haematopoiesis. Nature 459(7250): 1131-1135.
2. Ahsan T, Nerem RM. 2010. Fluid shear stress promotes an endothelial-like phenotype during the early differentiation of embryonic stem cells. Tissue Eng Part A 16(11): 3547-3553.
3. Ainslie KM, Garanich JS, Dull RO, Tarbell JM. 2005. Vascular smooth muscle cell glycocalyx influences shear stress-mediated contractile response. J Appl Physiol 98(1): 242-249.
4. Berardi DE, Tarbell JM. 2009. Stretch and shear interactions affect intercellular junction protein expression and turnover in endothelial cells. Cell Mol Bioeng 2(3): 320-331.
5. Brower JB, Targovnik JH, Caplan MR, Massia SP. 2010. High glucose-mediated loss of cell surface heparan sulfate proteoglycan impairs the endothelial shear stress response. Cytoskeleton (Hoboken) 67(3): 135-141.
6. Cancel LM, Tarbell JM. 2010. The role of apoptosis in LDL transport through cultured endothelial cell monolayers. Atherosclerosis 208(2): 335-341.
7. Castanares C, Redondo-Horcajo M, Magan-Marchal N, ten Dijke P, Lamas S, Rodriguez-Pascual F. 2007. Signaling by ALK5 mediates TGF-beta-induced ET-1 expression in endothelial cells: A role for migration and proliferation. J Cell Sci 120(Pt 7): 1256-1266.
8. Conklin BS, Zhong DS, Zhao W, Lin PH, Chen C. 2002. Shear stress regulates occludin and VEGF expression in porcine arterial endothelial cells. J Surg Res 102(1): 13-21.
9. Dejana E. 2004. Endothelial cell-cell junctions: Happy together. Nat Rev Mol Cell Biol 5(4): 261-270.
10. Dekker RJ, van Soest S, Fontijn RD, Salamanca S, de Groot PG, VanBavel E, Pannekoek H, Horrevoets AJ. 2002. Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Kruppel-like factor (KLF2). Blood 100(5): 1689-1698.
11. DeMaio L, Chang YS, Gardner TW, Tarbell JM, Antonetti DA. 2001. Shear stress regulates occludin content and phosphorylation. Am J Physiol Heart Circ Physiol 281: 105-113.
12. Fawcett J, Buckley C, Holness CL, Bird IN, Spragg JH, Saunders J, Harris A, Simmons DL. 1995. Mapping the homotypic binding sites in CD31 and the role of CD31 adhesion in the formation of interendothelial cell contacts. J Cell Biol 128(6): 1229-1241.
13. Florian JA, Kosky JR, Ainslie K, Pang Z, Dull RO, Tarbell JM. 2003. Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ Res 93(10): e136-e142.
14. Frangos JA, McIntire LV, Eskin SG. 1988. Shear stress induced stimulation of mammalian cell metabolism. Biotechnol Bioeng 32(8): 1053-1060.
15. Fridley KM, Fernandez I, Li MT, Kettlewell RB, Roy K. 2010. Unique differentiation profile of mouse embryonic stem cells in rotary and stirred tank bioreactors. Tissue Eng Part A 16(11): 3285-3298.
16. Gloe T, Sohn HY, Meininger GA, Pohl U. 2002. Shear stress-induced release of basic fibroblast growth factor from endothelial cells is mediated by matrix interaction via integrin alpha(v)beta3. J Biol Chem 277(26): 23453-23458.
17. Hough C, Cameron CL, Notley CR, Brown C, O'Brien L, Keightley AM, Berber E, Lillicrap D. 2008. Influence of a GT repeat element on shear stress responsiveness of the VWF gene promoter. J Thromb Haemost 6(7): 1183-1190.
18. James D, Nam HS, Seandel M, Nolan D, Janovitz T, Tomishima M, Studer L, Lee G, Lyden D, Benezra R, et al. 2010. Expansion and maintenance of human embryonic stem cell-derived endothelial cells by TGFbeta inhibition is Id1 dependent. Nat Biotechnol 28(2): 161-166.
19. Jones EA, le Noble F, Eichmann A. 2006. What determines blood vessel structure? Genetic prespecification vs. hemodynamics. Physiology (Bethesda) 21: 388-395.
20. Karamanian AA. 2009. Role of claudin-5 and hemodynamics in endothelial permeability and susceptibility to atherosclerosis. Philadelphia: University of Pennsylvania.
21. Lanner F, Lee KL, Sohl M, Holmborn K, Yang H, Wilbertz J, Poellinger L, Rossant J, Farnebo F. 2010. Heparan sulfation-dependent fibroblast growth factor signaling maintains embryonic stem cells primed for differentiation in a heterogeneous state. Stem Cells 28(2): 191-200.
22. Levenberg S, Golub JS, Amit M, Itskovitz-Eldor J, Langer R. 2002. Endothelial cells derived from human embryonic stem cells. PNAS 99(7): 4391-4396.
23. Li G, Simon MJ, Cancel LM, Shi ZD, Ji X, Tarbell JM, Morrison B 3rd, Fu BM. 2010. Permeability of endothelial and astrocyte cocultures: in vitro blood-brain barrier models for drug delivery studies. Ann Biomed Eng 38(8): 2499-2511.
24. McCloskey KE, Lyons I, Rao R, Stice SL, Nerem RM. 2003. Purified and proliferating endothelial cells derived and expanded in vitro from embryonic stem cells. Endothelium 10: 329-336.
25. McCloskey KE, Smith DA, Jo H, Nerem RM. 2006. Embryonic stem cell-derived endothelial cells may lack complete functional maturation in vitro. J Vasc Res 43: 411-421.
26. Metallo CM, Vodyanik MA, de Pablo JJ, Slukvin II, Palecek SP. 2008. The response of human embryonic stem cell-derived endothelial cells to shear stress. Biotechnol Bioeng 100(4): 830-837.
27. Michel CC, Curry FE. 1999. Microvascular permeability. Physiol Rev 79(3): 703-761.
28. Pahakis MY, Kosky JR, Dull RO, Tarbell JM. 2007. The role of endothelial glycocalyx components in mechanotransduction of fluid shear stress. Biochem Biophys Res Commun 355(1): 228-233.
29. Pries AR, Secomb TW, Gaehtgens P. 2000. The endothelial surface layer. Pflugers Arch 440(5): 653-666.
30. Purpura KA, George SH, Dang SM, Choi K, Nagy A, Zandstra PW. 2008. Soluble Flt-1 regulates Flk-1 activation to control hematopoietic and endothelial development in an oxygen-responsive manner. Stem Cells 26(11): 2832-2842.
31. Sargent CY, Berguig GY, Kinney MA, Hiatt LA, Carpenedo RL, Berson RE, McDevitt TC. 2010. Hydrodynamic modulation of embryonic stem cell differentiation by rotary orbital suspension culture. Biotechnol Bioeng 105(3): 611-626.
32. Secomb TW, Hsu R, Pries AR. 2001. Effect of the endothelial surface layer on transmission of fluid shear stress to endothelial cells. Biorheology 38(2-3): 143-150.
33. Shi ZD, Tarbell JM. 2011. Fluid flow mechanotransduction in vascular smooth muscle cells and fibroblasts. Ann Biomed Eng 39(6): 1608-1619.
34. Shi ZD, Abraham G, Tarbell JM. 2010. Shear stress modulation of smooth muscle cell marker genes in 2-D and 3-D depends on mechanotransduction by heparan sulfate proteoglycans and ERK1/2. PLoS One 5(8): e12196.
35. Shi ZD, Wang H, Tarbell JM. 2011. Heparan sulfate proteoglycans mediate interstitial flow mechanotransduction regulating MMP-13 expression and cell motility via FAK-ERK in 3D collagen. PLoS One 6(1): e15956.
36. Smith AG. 2001. Embryo-derived stem cells: Of mice and men. Annu Rev Cell Dev Biol 17: 435-462.
37. Stevens HY, Melchior B, Bell KS, Yun S, Yeh JC, Frangos JA. 2008. PECAM-1 is a critical mediator of atherosclerosis. Dis Model Mech 1(2-3): 175-181 (discussion 179).
38. Tarbell JM. 2010. Shear stress and the endothelial transport barrier. Cardiovasc Res 87(2): 320-330.
39. Tarbell JM, Ebong EE. 2008. The endothelial glycocalyx: A mechano-sensor and -transducer. Sci Signal 1(40): pt8.
40. Tarbell JM, Pahakis MY. 2006. Mechanotransduction and the glycocalyx. J Intern Med 259(4): 339-350.
41. Thi MM, Tarbell JM, Weinbaum S, Spray DC. 2004. The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: A "bumper-car" model. Proc Natl Acad Sci USA 101(47): 16483-16488.
42. Toda M, Yamamoto K, Shimizu N, Obi S, Kumagaya S, Igarashi T, Kamiya A, Ando J. 2008. Differential gene responses in endothelial cells exposed to a combination of shear stress and cyclic stretch. J Biotechnol 133(2): 239-244.
43. Toh YC, Voldman J. 2011. Fluid shear stress primes mouse embryonic stem cells for differentiation in a self-renewing environment via heparan sulfate proteoglycans transduction. FASEB J 25(4): 1208-1217.
44. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, Cao G, DeLisser H, Schwartz MA. 2005. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437(7057): 426-431.
45. Wang H, Riha GM, Yan S, Li M, Chai H, Yang H, Yao Q, Chen C. 2005. Shear stress induces endothelial differentiation from a murine embryonic mesenchymal progenitor cell line. Arterioscler Thromb Vasc Biol 25(9): 1817-1823.
46. Wang H, Li M, Lin PH, Yao Q, Chen C. 2008. Fluid shear stress regulates the expression of TGF-beta1 and its signaling molecules in mouse embryo mesenchymal progenitor cells. J Surg Res 150(2): 266-270.
47. Watabe T, Nishihara A, Mishima K, Yamashita J, Shimizu K, Miyazawa K, Nishikawa S, Miyazono K. 2003. TGF-beta receptor kinase inhibitor enhances growth and integrity of embryonic stem cell-derived endothelial cells. J Cell Biol 163(6): 1303-1311.
48. Weinbaum S, Tarbell JM, Damiano ER. 2007. The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng 9: 121-167.
49. Woodfin A, Voisin MB, Nourshargh S. 2007. PECAM-1: A multi-functional molecule in inflammation and vascular biology. Arterioscler Thromb Vasc Biol 27(12): 2514-2523.
50. Wu CC, Chao YC, Chen CN, Chien S, Chen YC, Chien CC, Chiu JJ, Linju Yen B. 2008. Synergism of biochemical and mechanical stimuli in the differentiation of human placenta-derived multipotent cells into endothelial cells. J Biomech 41(4): 813-821.
51. Yamamoto K, Takahashi T, Asahara T, Ohura N, Sokabe T, Kamiya A, Ando J. 2003. Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress. J Appl Physiol 95: 2081-2088.
52. Yamamoto K, Sokabe T, Watabe T, Miyazono K, Yamashita JK, Obi S, Ohura N, Matsushita A, Kamiya A, Ando J. 2005. Fluid shear stress induces differentiation of Flk-1-positive embryonic stem cells into vascular endothelial cells in vitro. Am J Physiol Heart Circ Physiol 288: H1915-H1924.
53. Yamashita J, Itoh H, Hirashima M, Ogawa M, Nishikawa S, Yurugi T, Naito M, Nakao K. 2000. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408(6808): 92-96.
54. Yao Y, Rabodzey A, Dewey CF, Jr. 2007. Glycocalyx modulates the motility and proliferative response of vascular endothelium to fluid shear stress. Am J Physiol Heart Circ Physiol 293(2): H1023-H1030.
55. Ye C, Bai L, Yan ZQ, Wang YH, Jiang ZL. 2008. Shear stress and vascular smooth muscle cells promote endothelial differentiation of endothelial progenitor cells via activation of Akt. Clin Biomech (Bristol, Avon) 23 (Suppl. 1): S118-S124.
56. Zeng L, Xiao Q, Margariti A, Zhang Z, Zampetaki A, Patel S, Capogrossi MC, Hu Y, Xu Q. 2006. HDAC3 is crucial in shear- and VEGF-induced stem cell differentiation toward endothelial cells. J Cell Biol 174(7): 1059-1069.