Proteomic profiling of endorepellin angiostatic activity on human endothelial cells

Proteome Science

Volumn 6, Issue , 2008, Pages

  Zoeller, Jason J ^a   Iozzo, Renato V ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; CALRETICULIN; CHAPERONIN; ENDOREPELLIN; HEAT SHOCK PROTEIN 60; PROTEIN DISULFIDE ISOMERASE; PROTEOGLYCAN; UNCLASSIFIED DRUG; VIMENTIN;

ANTIANGIOGENIC ACTIVITY; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SYNTHESIS REGULATION; PROTEOMICS; STATISTICAL SIGNIFICANCE; STUDENT T TEST; UMBILICAL VEIN;

EID: 41549138817     PISSN: None     EISSN: 14775956     Source Type: Journal    
DOI: 10.1186/1477-5956-6-7     Document Type: Article

References (73)

1. Mathiak M Yenisey C Grant DS Sharma B Iozzo RV A role for perlecan in the suppression of growth and invasion in fibrosarcoma cells Cancer Res 1997, 57:2130-2136. 9187109
2. Hassell JR Yamada Y Arikawa-Hirasawa E Role of perlecan in skeletal development and diseases Glycoconj J 2003, 19(4-5):263-267. 10.1023/ A:1025340215261 12975604
3. Knox SM Whitelock JM Perlecan: How does one molecule do so many things? Cell Mol Life Sci 2006, 63:2435-2445. 10.1007/s00018-006-6162-z 16952056
4. Iozzo RV Basement membrane proteoglycans: From cellar to ceiling Nature Rev Mol Cell Biol 2005, 6(8):646-656. 10.1038/nrm1702 16064139
5. Nugent MA Nugent HM Iozzo RV Sanchack K Edelman ER Perlecan is required to inhibit thrombosis after deep vascular injury and contributes to endothelial cell-mediated inhibition of intimal hyperplasia Proc Natl Acad Sci USA 2000, 97:6722-6727. 18716 10841569 10.1073/pnas.97.12.6722
6. Fuki I Iozzo RV Williams KJ Perlecan heparan sulfate proteoglycan. A novel receptor that mediates a distinct pathway for ligand catabolism J Biol Chem 2000, 275:25742-25750. 10.1074/jbc.M909173199 10818109
7. Mongiat M Otto J Oldershaw R Ferrer F Sato JD Iozzo RV Fibroblast growth factor-binding protein is a novel partner for perlecan protein core J Biol Chem 2001, 276:10263-10271. 10.1074/jbc.M011493200 11148217
8. Mongiat M Fu J Oldershaw R Greenhalgh R Gown A Iozzo RV Perlecan protein core interacts with extracellular matrix protein 1 (ECM1), a glycoprotein involved in bone formation and angiogenesis J Biol Chem 2003, 278:17491-17499. 10.1074/jbc.M210529200 12604605
9. Gonzalez EM Mongiat M Slater SJ Baffa R Iozzo RV A novel interaction between perlecan protein core and progranulin: Potential effects on tumor growth J Biol Chem 2003, 278:38113-38116. 10.1074/jbc.C300310200 12900424
10. Whitelock JM Iozzo RV Heparan sulfate: A complex polymer charged with biological activity Chem Rev 2005, 105:2745-2764. 10.1021/cr010213m 16011323
11. Farach-Carson MC Carson DD Perlecan - a multifunctional extracellular proteoglycan scaffold Glycobiology 2007, 17:897-905. 10.1093/glycob/ cwm043 17442708
12. Arikawa-Hirasawa E Watanabe E Takami H Hassell JR Yamada Y Perlecan is essential for cartilage and cephalic development Nature Genet 1999, 23:354-358. 10.1038/15537 10545953
13. Costell M Gustafsson E Aszódi A Mörgelin M Bloch W Hunziker E Addicks K Timpl R Fässler R Perlecan maintains the integrity of cartilage and some basement membranes J Cell Biol 1999, 147:1109-1122. 10.1083/jcb.147.5.1109 10579729
14. Costell M Carmona R Gustafsson E González-Iriarte M Fässler R Munoz-Chápuli R Hyperplastic conotruncal endocardial cushions and transposition of great arteries in perlecan-null mice Circ Res 2002, 91:158-164. 10.1161/01.RES.0000026056.81424.DA 12142349
15. Iozzo RV San Antonio JD Heparan sulfate proteoglycans: Heavy hitters in the angiogenesis arena J Clin Invest 2001, 108:349-355. 209371 11489925 10.1172/JCI200113738
16. Aviezer D Hecht D Safran M Eisinger M David G Yayon A Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis Cell 1994, 79:1005-1013. 10.1016/ 0092-8674(94)90031-0 7528102
17. Aviezer D Iozzo RV Noonan DM Yayon A Suppression of autocrine and paracrine functions of basic fibroblast growth factor by stable expression of perlecan antisense cDNA Mol Cell Biol 1997, 17:1938-1946. 232040 9121441
18. Sharma B Handler M Eichstetter I Whitelock J Nugent MA Iozzo RV Antisense targeting of perlecan blocks tumor growth and angiogenesis in vivo J Clin Invest 1998, 102:1599-1608. 509011 9788974 10.1172/JCI3793
19. Zhou Z Wang J Cao R Morita H Soininen R Chan KM Liu B Cao Y Tryggvason K Impaired angiogenesis, delayed wound healing and retarded tumor growth in perlecan heparan sulfate-deficient mice Cancer Res 2004, 64:4699-4702. 10.1158/0008-5472.CAN-04-0810 15256433
20. Savore C Zhang C Muir C Liu R Wyrwa J Shu J Zhau HE Chung LW Carson DD Farach-Carson MC Perlecan knockdown in metastatic prostate cancer cells reduces heparin-binding growth factor responses in vitro and tumor growth in vivo Clin Exp Metastasis 2005, 22:377-390. 10.1007/ s10585-005-2339-3 16283481
21. Zhang W Chuang YJ Swanson R Li J Seo K Leung L Lau LF Olson ST Antiangiogenic antithrombin down-regulates the expression of the proangiogenic heparan sulfate proteoglycan, perlecan, in endothelial cells Blood 2004, 103:1185-1191. 10.1182/blood-2003-08-2920 14563633
22. Zhang W Chuang YJ Jin T Swanson R Xiong Y Leung L Olson ST Antiangiogenic antithrombin induces global changes in the gene expression profile of endothelial cells Cancer Research 2006, 66:5047-5055. 10.1158/0008-5472.CAN-05-4449 16707426
23. Mongiat M Sweeney S San Antonio JD Fu J Iozzo RV Endorepellin, a novel inhibitor of angiogenesis derived from the C terminus of perlecan J Biol Chem 2003, 278:4238-4249. 10.1074/jbc.M210445200 12435733
24. Bix G Fu J Gonzalez E Macro L Barker A Campbell S Zutter MM Santoro SA Kim JK Höök M Reed CC Iozzo RV Endorepellin causes endothelial cell disassembly of actin cytoskeleton and focal adhesions through the a2b1 integrin J Cell Biol 2004, 166:97-109. 10.1083/jcb.200401150 15240572 2172143
25. Senger DR Claffey KP Benes JE Perruzzi CA Sergiou AP Detmar M Angiogenesis promoted by vascular endothelial growth factor: Regulation through α1β1 and α2β1 integrins Proc Natl Acad Sci USA 1997, 94:13612-13617. 28354 9391074 10.1073/pnas.94.25.13612
26. Senger DR Perruzzi CA Streit M Koteliansky VE de Fougerolles AR Detmar M The α1β1 and α2β1 integrins provide critical support for vascular endothelial growth factor signaling, endothelial cell migration, and tumor angiogenesis Am J Pathol 2002, 160:195-204. 1867136 11786413
27. Sweeney SM DiLullo G Slater SJ Martinez J Iozzo RV Lauer-Fields JL Fields GB San Antonio JD Angiogenesis in collagen I requires α2β1 ligation of a GFP*GER sequence and possible p38 MAPK activation and focal adhesion disassembly J Biol Chem 2003, 278:30516-30524. 10.1074/jbc.M304237200 12788934
28. Davis GE Senger DR Endothelial extracellular matrix: Biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization Circ Res 2005. 97:1093-1107. 10.1161/ 01.RES.0000191547.64391.e3 16306453
29. Woodall BP Nyström A Iozzo RA Eble JA Niland S Krieg T Eckes B Pozzi A Iozzo RV Integrin α2β1 is the required receptor for endorepellin angiostatic activity. J Biol Chem 2008, 283:2335-2343. 10.1074/jbc.M708364200 18024432
30. Gonzalez EM Reed CC Bix G Fu J Zhang Y Gopalakrishnan B Greenspan DS Iozzo RV BMP-1/Tolloid-like metalloproteases process endorepellin, the angiostatic C-terminal fragment of perlecan J Biol Chem 2005, 280:7080-7087. 10.1074/jbc.M409841200 15591058
31. Bix G Castello R Burrows M Zoeller JJ Weech M Iozzo RA Cardi C Thakur MT Barker CA Camphausen KC Iozzo RV Endorepellin in vivo: Targeting the tumor vasculature and retarding cancer growth and metabolism J Natl Cancer Inst 2006, 98:1634-1646. 17105986
32. Nguyen DV Wang N Carroll RJ Evaluation of missing value estimation for microarray data J Data Sci 2004, 2:347-370.
33. Jung K Gannoun A Sitek B Apostolov O Schramm A Meyer HE Stühler K Urfer W Statistical evaluation of methods for the analysis of dynamic protein expression data from a tumor study J Cell Sci 2006, 119:1886-1895. 10.1242/jcs.02921 16636073
34. Burridge K Chrzanowska-Wodnicka M Zhong C Focal adhesion assembly Trends Cell Biol 1997, 7:342-347. 10.1016/S0962-8924(97)01127-6 17708978
35. Lamalice L Le Boeuf F Huot J Endothelial cell migration during angiogenesis Circ Res 2007, 100:782-794. 10.1161/ 01.RES.0000259593.07661.1e 17395884
36. Hoock TC Newcomb PM Herman IM β actin and its mRNA are localized at the plasma membrane and the regions of moving cytoplasm during the cellular response to injury J Cell Biol 1991, 112:653-664. 10.1083/ jcb.112.4.653 1993736
37. Kislauskis EH Zhu X Singer RH β-actin messenger RNA localization and protein synthesis augment cell motility J Cell Biol 1997, 136:1263-1270. 10.1083/jcb.136.6.1263 9087442
38. Wickström SA Veikkola T Rehn M Pihlajaniemi T Alitalo K Keski-Oja J Endostatin-induced modulation of plasminogen activation with concomitant loss of focal adhesions and actin stress fibers in cultured human endothelial cells Cancer Res 2001, 61:6511-6516. 11522648
39. Dixelius J Cross M Matsumoto T Sasaki T Timpl R Claesson-Welsh L Endostatin regulates endothelial cell adhesion and cytoskeletal organization Cancer Res 2002, 62:1944-1947. 11929807
40. Keezer SM Ivie SE Krutzsch HC Tandle A Libutti SK Roberts DD Angiogenesis inhibitors target the endothelial cell cytoskeleton through altered regulation of heat shock protein 27 and cofilin Cancer Res 2003, 63:6405-6412. 14559830
41. Coppolino MG Dedhar S Molecules in focus; calreticulin Int J Biochem Cell Biol 1998, 30:553-558. 10.1016/S1357-2725(97)00153-2 9693955
42. Pike SE Yao L Jones KD Cherney B Appella E Sakaguchi K Nakhasi H Teruya-Feldstein J Wirth P Gupta G Tosato G Vasostatin, a calreticulin fragment, inhibits angiogenesis and suppresses tumor growth J Exp Med 1998, 188:2349-2356. 10.1084/jem.188.12.2349 9858521
43. Pike SE Yao L Setsuda J Jones KD Cherney B Appella E Sakaguchi K Nakhasi H Atreya CD Teruya-Feldstein J Wirth P Gupta G Tosato G Calreticulin and calreticulin fragments are endothelial cell inhibitors that suppress tumor growth Blood 1999, 94:2461-2468. 10498619
44. Coppolino MG Woodside MJ Demaurex N Grinstein S St Arnaud R Dedhar S Calreticulin is essential for integrin-mediated calcium signalling and cell adhesion Nature 1997, 386:843-847. 10.1038/386843a0 9126744
45. Elton CM Smethurst PA Eggleton P Farndale RW Physical and functional interaction between cell-surface calreticulin and the collagen receptors integrin α2β1 and glycoprotein VI in human platelets Thromb Hemost 2002, 88:648-654.
46. Coppolino MG Dedhar S Ligand-specific, transient interaction between integrins and calreticulin during cell adhesion to extracellular matrix proteins is dependent upon phosphorylation/dephosphorylation events Biochem J 1999, 340:41-50. 1220220 10229657 10.1042/0264-6021:3400041
47. Kwon MS Park CS Choi K Ahnn J Kim JI Eom SH Kaufman SJ Song WK Calreticulin couples calcium release and calcium influx in integrin-mediated calcium signaling Mol Biol Cell 2000, 11:1433-1443. 14857 10749940
48. Coppolino M Leung-Hagesteijn C Dedhar S Wilkins J Inducible interaction of integrin α2β1 with calreticulin. Dependence on the activation state of the integrin J Biol Chem 1995, 270:23132-23138. 10.1074/jbc.270.39.23132 7559457
49. Opas M Szewczenko-Pawlikowski M Jass GK Mesaeli N Michalak M Calreticulin modulates cell adhesiveness via regulation of vinculin expression J Cell Biol 1996, 135:1913-1923. 10.1083/jcb.135.6.1913 8991101
50. Fadel MP Dziak E Lo CM Ferrier J Mesaeli N Michalak M Opas M Calreticulin affects focal contact-dependent but not close contact-dependent cell-substratum adhesion J Biol Chem 1999, 274:15085-15094. 10.1074/jbc.274.21.15085 10329714
51. Goicoechea S Orr AW Pallero MA Eggleton P Murphy-Ullrich JE Thrombospondin mediates focal adhesion disassembly through interactions with cell surface calreticulin J Biol Chem 2000, 275:36358-36368. 10.1074/jbc.M005951200 10964924
52. Goicoechea S Pallero MA Eggleton P Michalak M Murphy-Ullrich JE The anti-adhesive activity of thrombospondin is mediated by the N-terminal domain of cell surface calreticulin J Biol Chem 2002, 277:37219-37228. 10.1074/jbc.M202200200 12147682
53. Orr AW Elzie CA Kucik DF Murphy-Ullrich JE Thrombospondin signaling through the calreticulin/LDL receptor-related protein co-complex stimulates random and directed cell migration J Cell Sci 2003, 116:2917-2927. 10.1242/jcs.00600 12808019
54. Czarnecka AM Campanella C Zummo G Cappello F Mitochondrial chaperones in cancer Canc Biol Ther 2006, 5(7):714-720. Epub 2006 Jul 1. 16861898
55. Barazi HO Zhou L Templeton NS Krutzsch HC Roberts DD Identification of heat shock protein 60 as a molecular mediator of α3β1 integrin activation Cancer Res 2002, 62:1541-1548. 11888933
56. Kirchoff SR Gupta S Knowlton AA Cytosolic heat shock protein 60, apoptosis, and myocardial injury Circulation 2002, 105:2899-2904. 10.1161/01.CIR.0000019403.35847.23 12070120
57. Artwohl M Hölzenbein T Fürnsinn C Freudenthaler A Huttary N Waldhäusl WK Baumgartner-Parzer SM Thiazolidinediones inhibit apoptosis and heat shock protein 60 expression in human vascular endothelial cells Thromb Haemost 2005, 93:810-815. 15886792
58. Laplante P Raymond MA Labelle A Abe JI Iozzo RV Hebért MJ Perlecan proteolysis induces α2β1 integrin and src-family kinases dependent anti-apoptotic pathway in fibroblasts in the absence of focal adhesion kinase activation J Biol Chem 2006, 281:30383-30392. 10.1074/jbc.M606412200 16882656
59. Samali A Cai J Zhivotovsky B Jones DP Orrenius S Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of jurkat cells EMBO J 1999, 18:2040-2048. 1171288 10205158 10.1093/emboj/18.8.2040
60. Lin KM Lin B Lian IY Mestril R Scheffler IE Dillmann WH Combined and individual mitochondrial HSP60 and HSP10 expression in cardiac myocytes protects mitochondrial function and prevents apoptotic cell deaths induced by simulated ischemia-reoxygenation Circulation 2001, 103:1787-1792. 11282911
61. Chang L Goldman RD Intermediate filaments mediate cytoskeletal crosstalk Nature Rev Mol Cell Biol 2004, 5(8):601-613. 10.1038/nrm1438 15366704
62. Kreis S Schonfeld HJ Melchior C Steiner B Kieffer N The intermediate filament protein vimentin binds specifically to a recombinant integrin α2/β1 cytoplasmic tail complex and co-localizes with native α2/β1 in endothelial cell focal adhesions Exp Cell Res 2005, 305:110-121. 10.1016/j.yexcr.2004.12.023 15777792
63. Gonzales M Weksler B Tsuruta D Goldman RD Yoon KJ Hopkinson SB Flitney FW Jones JC Structure and function of a vimentin-associated matrix adhesion in endothelial cells Mol Biol Cell 2001, 12:85-100. 30570 11160825
64. Byun Y Chen F Chang R Trivedi M Green KJ Cryns VL Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis Cell Death Differ 2001, 8:443-450. 10.1038/sj.cdd.4400840 11423904
65. Kivirikko KI Myllyharju J Prolyl 4-hydroxylases and their protein disulfide isomerase subunit Matrix Biol 1998, 16(7):357-368. 10.1016/ S0945-053X(98)90009-9 9524356
66. Koivu J Myllylä R Helaakoski T Pihlajaniemi T Tasanen K Kivirikko K A single polypeptide acts both as the β subunit of prolyl 4-hydroxylase and as a protein disulfide-isomerase J Biol Chem 1987, 262:6447-6449. 3032969
67. Pihlajaniemi T Helaakoski T Tasanen K Myllylä R Huhtala ML Koivu J Kivirikko K Molecular cloning of the β-subunit of human prolyl 4-hydroxylase. This subunit and protein disulphide isomerase are products of the same gene EMBO J 1987, 6:643-649. 553446 3034602
68. Noiva R Lennarz WJ Protein disulfide isomerase J Biol Chem 1992, 267:3553-3556. 1740407
69. Wang CC Tsou CL Protein disulfide isomerase is both an enzyme and a chaperone FASEB J 1993, 7:1515-1517. 7903263
70. Cai H Wang CC Tsou CL Chaperone-like activity of protein disulfide isomerase in the refolding of a protein with no disulfide bonds J Biol Chem 1994, 269:24550-24552. 7929125
71. John DCA Grant ME Bulleid NJ Cell-free synthesis and assembly of prolyl 4-hydroxylase: The role of the β-subunit (PDI) in preventing misfolding and aggregation of the α-subunit EMBO J 1993, 12:1587-1595. 413372 8385607
72. Maeshima Y Sudhakar A Lively JC Ueki K Kharbanda S Kahn CR Sonenberg N Hynes RO Kalluri R Tumstatin, an endothelial cell-specific inhibitor of protein synthesis Science 2002, 295:140-143. 10.1126/science.1065298 11778052
73. Sudhakar A Sugimoto H Yang C Lively J Zeisberg M Kalluri R Human tumstatin and human endostatin exhibit distinct antiangiogenic activities mediated by αvβ3 and α5β1 integrins Proc Natl Acad Sci USA 2003, 100:4766-4771. 153630 12682293 10.1073/ pnas.0730882100