A novel, biased-like SDF-1 derivative acts synergistically with starPEG-based heparin hydrogels and improves eEPC migration in vitro

Journal of Controlled Release

Volumn 162, Issue 1, 2012, Pages 68-75

  Baumann, Lars ^a   Prokoph, Silvana ^b   Gabriel, Christian ^a   Freudenberg, Uwe ^b   Werner, Carsten ^b   Beck Sickinger, Annette G ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Biomaterial; Cardiac regeneration; Endothelial progenitor cells; Heparin; Hydrogel; SDF 1

Indexed keywords

CARDIAC REGENERATION; CHEMOKINES; COOPERATIVE EFFECTS; DIPEPTIDE; ENDOTHELIAL PROGENITOR CELLS; HEPARIN; IMMOBILIZATION EFFICIENCY; IN-VITRO; MIGRATION RATES; PROGENITOR CELL; PROTEIN RELEASE; SWITCHABLE; TIME-DEPENDENT;

AMINO ACIDS; BIOMATERIALS; DRUG DELIVERY; ENZYME ACTIVITY; PATHOLOGY; POLYSACCHARIDES; STEM CELLS;

HYDROGELS;

ALANINE; DIPEPTIDE; DIPEPTIDYL PEPTIDASE IV; HEPARIN; MACROGOL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN VARIANT; STROMAL CELL DERIVED FACTOR 1ALPHA; STROMAL CELL DERIVED FACTOR 1ALPHA VARIANT; UNCLASSIFIED DRUG;

ARTICLE; CELL MIGRATION; DRUG POTENTIATION; ENDOTHELIAL PROGENITOR CELL; ENZYME PHOSPHORYLATION; HYDROGEL; IMMOBILIZED CELL; IN VITRO STUDY; INFLAMMATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROCESSING; PROTEIN SECRETION;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CHEMOKINE CXCL12; CHROMATOGRAPHY, AFFINITY; COS CELLS; DIPEPTIDYL PEPTIDASE 4; ENDOTHELIAL CELLS; HEPARIN; HUMANS; HYDROGELS; JURKAT CELLS; MATRIX METALLOPROTEINASE 9; PANCREATIC ELASTASE; POLYETHYLENE GLYCOLS; RECOMBINANT PROTEINS; STEM CELLS; TISSUE SCAFFOLDS;

EID: 84864703375     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2012.04.049     Document Type: Article

References (53)

1. S. Stewart, K. MacIntyre, D.J. Hole, S. Capewell, and J.J. McMurray More 'malignant' than cancer? Five-year survival following a first admission for heart failure Eur. J. Heart Fail. 3 2001 315 322
2. J.C. George Stem cell therapy in acute myocardial infarction: a review of clinical trials Transl. Res. 155 2010 10 19
3. V. Schachinger, B. Assmus, M.B. Britten, J. Honold, R. Lehmann, C. Teupe, N.D. Abolmaali, T.J. Vogl, W.K. Hofmann, H. Martin, S. Dimmeler, and A.M. Zeiher Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction: final one-year results of the TOPCARE-AMI Trial J. Am. Coll. Cardiol. 44 2004 1690 1699
4. G.P. Meyer, K.C. Wollert, J. Lotz, J. Steffens, P. Lippolt, S. Fichtner, H. Hecker, A. Schaefer, L. Arseniev, B. Hertenstein, A. Ganser, and H. Drexler Intracoronary bone marrow cell transfer after myocardial infarction: eighteen months' follow-up data from the randomized, controlled BOOST (BOne marrOw transfer to enhance ST-elevation infarct regeneration) trial Circulation 113 2006 1287 1294
5. V. Schachinger, S. Erbs, A. Elsasser, W. Haberbosch, R. Hambrecht, H. Holschermann, J. Yu, R. Corti, D.G. Mathey, C.W. Hamm, T. Suselbeck, N. Werner, J. Haase, J. Neuzner, A. Germing, B. Mark, B. Assmus, T. Tonn, S. Dimmeler, and A.M. Zeiher Improved clinical outcome after intracoronary administration of bone-marrow-derived progenitor cells in acute myocardial infarction: final 1-year results of the REPAIR-AMI trial Eur. Heart J. 27 2006 2775 2783
6. A. Schuh, E.A. Liehn, A. Sasse, M. Hristov, R. Sobota, M. Kelm, M.W. Merx, and C. Weber Transplantation of endothelial progenitor cells improves neovascularization and left ventricular function after myocardial infarction in a rat model Basic Res. Cardiol. 103 2008 69 77
7. C.E. Murry, M.H. Soonpaa, H. Reinecke, H. Nakajima, H.O. Nakajima, M. Rubart, K.B. Pasumarthi, J.I. Virag, S.H. Bartelmez, V. Poppa, G. Bradford, J.D. Dowell, D.A. Williams, and L.J. Field Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts Nature 428 2004 664 668
8. L.B. Balsam, A.J. Wagers, J.L. Christensen, T. Kofidis, I.L. Weissman, and R.C. Robbins Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium Nature 428 2004 668 673
9. D.J. Ceradini, A.R. Kulkarni, M.J. Callaghan, O.M. Tepper, N. Bastidas, M.E. Kleinman, J.M. Capla, R.D. Galiano, J.P. Levine, and G.C. Gurtner Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1 Nat. Med. 10 2004 858 864
10. J. Yamaguchi, K.F. Kusano, O. Masuo, A. Kawamoto, M. Silver, S. Murasawa, M. Bosch-Marce, H. Masuda, D.W. Losordo, J.M. Isner, and T. Asahara Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization Circulation 107 2003 1322 1328
11. O. Salvucci, L. Yao, S. Villalba, A. Sajewicz, S. Pittaluga, and G. Tosato Regulation of endothelial cell branching morphogenesis by endogenous chemokine stromal-derived factor-1 Blood 99 2002 2703 2711
12. P. Proost, S. Struyf, D. Schols, C. Durinx, A. Wuyts, J.P. Lenaerts, E. De Clercq, I. De Meester, and J. Van Damme Processing by CD26/dipeptidyl- peptidase IV reduces the chemotactic and anti-HIV-1 activity of stromal-cell-derived factor-1alpha FEBS Lett. 432 1998 73 76
13. M.B. Delgado, I. Clark-Lewis, P. Loetscher, H. Langen, M. Thelen, M. Baggiolini, and M. Wolf Rapid inactivation of stromal cell-derived factor-1 by cathepsin G associated with lymphocytes Eur. J. Immunol. 31 2001 699 707
14. G.A. McQuibban, G.S. Butler, J.H. Gong, L. Bendall, C. Power, I. Clark-Lewis, and C.M. Overall Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1 J. Biol. Chem. 276 2001 43503 43508
15. A. Valenzuela-Fernandez, T. Planchenault, F. Baleux, I. Staropoli, K. Le-Barillec, D. Leduc, T. Delaunay, F. Lazarini, J.L. Virelizier, M. Chignard, D. Pidard, and F. Arenzana-Seisdedos Leukocyte elastase negatively regulates Stromal cell-derived factor-1 (SDF-1)/CXCR4 binding and functions by amino-terminal processing of SDF-1 and CXCR4 J. Biol. Chem. 277 2002 15677 15689
16. P. Misra, D. Lebeche, H. Ly, M. Schwarzkopf, G. Diaz, R.J. Hajjar, A.D. Schecter, and J.V. Frangioni Quantitation of CXCR4 expression in myocardial infarction using 99mTc-labeled SDF-1alpha J. Nucl. Med. 49 2008 963 969
17. M.V. Tsurkan, K.R. Levental, U. Freudenberg, and C. Werner Enzymatically degradable heparin-polyethylene glycol gels with controlled mechanical properties Chem. Commun. 46 2010 1141 1143
18. A. Zieris, S. Prokoph, K.R. Levental, P.B. Welzel, M. Grimmer, U. Freudenberg, and C. Werner FGF-2 and VEGF functionalization of starPEG-heparin hydrogels to modulate biomolecular and physical cues of angiogenesis Biomaterials 31 2010 7985 7994
19. A. Zieris, K. Chwalek, S. Prokoph, K.R. Levental, P.B. Welzel, U. Freudenberg, and C. Werner Dual independent delivery of pro-angiogenic growth factors from starPEG-heparin hydrogels J. Control. Release 156 2011 28 36
20. K. Chwalek, K.R. Levental, M.V. Tsurkan, A. Zieris, U. Freudenberg, and C. Werner Two-tier hydrogel degradation to boost endothelial cell morphogenesis Biomaterials 32 2011 9649 9657
21. L. Baumann, and A.G. Beck-Sickinger Identification of a potential modification site in human stromal cell-derived factor-1 Biopolymers 94 2010 771 778
22. A. Zieris, S. Prokoph, P.B. Welzel, M. Grimmer, K.R. Levental, W. Panyanuwat, U. Freudenberg, and C. Werner Analytical approaches to uptake and release of hydrogel-associated FGF-2 J. Mater. Sci. Mater. Med. 21 2010 915 923
23. U. Freudenberg, A. Hermann, P.B. Welzel, K. Stirl, S.C. Schwarz, M. Grimmer, A. Zieris, W. Panyanuwat, S. Zschoche, D. Meinhold, A. Storch, and C. Werner A star-PEG-heparin hydrogel platform to aid cell replacement therapies for neurodegenerative diseases Biomaterials 30 2009 5049 5060
24. S. Dimmeler, A. Aicher, M. Vasa, C. Mildner-Rihm, K. Adler, M. Tiemann, H. Rutten, S. Fichtlscherer, H. Martin, and A.M. Zeiher HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/Akt pathway J. Clin. Invest. 108 2001 391 397
25. S. Boyden The chemotactic effect of mixtures of antibody and antigen on polymorphonuclear leucocytes J. Exp. Med. 115 1962 453 466
26. A.M. Lambeir, C. Durinx, S. Scharpe, and I. De Meester Dipeptidyl-peptidase IV from bench to bedside: an update on structural properties, functions, and clinical aspects of the enzyme DPP IV Crit. Rev. Clin. Lab. Sci. 40 2003 209 294
27. R. Sadir, F. Baleux, A. Grosdidier, A. Imberty, and H. Lortat-Jacob Characterization of the stromal cell-derived factor-1alpha-heparin complex J. Biol. Chem. 276 2001 8288 8296
28. C.T. Veldkamp, F.C. Peterson, A.J. Pelzek, and B.F. Volkman The monomer-dimer equilibrium of stromal cell-derived factor-1 (CXCL 12) is altered by pH, phosphate, sulfate, and heparin Protein Sci. 14 2005 1071 1081
29. R. Sadir, A. Imberty, F. Baleux, and H. Lortat-Jacob Heparan sulfate/heparin oligosaccharides protect stromal cell-derived factor-1 (SDF-1)/CXCL12 against proteolysis induced by CD26/dipeptidyl peptidase IV J. Biol. Chem. 279 2004 43854 43860
30. V.F. Segers, T. Tokunou, L.J. Higgins, C. MacGillivray, J. Gannon, and R.T. Lee Local delivery of protease-resistant stromal cell derived factor-1 for stem cell recruitment after myocardial infarction Circulation 116 2007 1683 1692
31. J.T. Peterson, H. Li, L. Dillon, and J.W. Bryant Evolution of matrix metalloprotease and tissue inhibitor expression during heart failure progression in the infarcted rat Cardiovasc. Res. 46 2000 307 315
32. R.M. Rao, T.V. Betz, D.J. Lamont, M.B. Kim, S.K. Shaw, R.M. Froio, F. Baleux, F. Arenzana-Seisdedos, R. Alon, and F.W. Luscinskas Elastase release by transmigrating neutrophils deactivates endothelial-bound SDF-1alpha and attenuates subsequent T lymphocyte transendothelial migration J. Exp. Med. 200 2004 713 724
33. B. Korkmaz, T. Moreau, and F. Gauthier Neutrophil elastase, proteinase 3 and cathepsin G: physicochemical properties, activity and physiopathological functions Biochimie 90 2008 227 242
34. K. Bellmann-Sickert, and A.G. Beck-Sickinger Palmitoylated SDF1alpha shows increased resistance against proteolytic degradation in liver homogenates ChemMedChem 6 2011 193 200
35. W. Tan, D. Martin, and J.S. Gutkind The Galpha13-Rho signaling axis is required for SDF-1-induced migration through CXCR4 J. Biol. Chem. 281 2006 39542 39549
36. Z.J. Cheng, J. Zhao, Y. Sun, W. Hu, Y.L. Wu, B. Cen, G.X. Wu, and G. Pei beta-arrestin differentially regulates the chemokine receptor CXCR4-mediated signaling and receptor internalization, and this implicates multiple interaction sites between beta-arrestin and CXCR4 J. Biol. Chem. 275 2000 2479 2485
37. C. Porcile, A. Bajetto, F. Barbieri, S. Barbero, R. Bonavia, M. Biglieri, P. Pirani, T. Florio, and G. Schettini Stromal cell-derived factor-1alpha (SDF-1alpha/CXCL12) stimulates ovarian cancer cell growth through the EGF receptor transactivation Exp. Cell Res. 308 2005 241 253
38. X. Hu, S. Dai, W.J. Wu, W. Tan, X. Zhu, J. Mu, Y. Guo, R. Bolli, and G. Rokosh Stromal cell derived factor-1 alpha confers protection against myocardial ischemia/reperfusion injury: role of the cardiac stromal cell derived factor-1 alpha CXCR4 axis Circulation 116 2007 654 663
39. H. Zheng, G. Fu, T. Dai, and H. Huang Migration of endothelial progenitor cells mediated by stromal cell-derived factor-1alpha/CXCR4 via PI3K/Akt/eNOS signal transduction pathway J. Cardiovasc. Pharmacol. 50 2007 274 280
40. S. Prokoph, E. Chavakis, K.R. Levental, A. Zieris, U. Freudenberg, S. Dimmeler, and C. Werner Sustained delivery of SDF-1 from heparin-based hydrogels to attract circulating pro-angiogenic cells Biomaterials 33 2012 4792 4800
41. E. De Falco, D. Porcelli, A.R. Torella, S. Straino, M.G. Iachininoto, A. Orlandi, S. Truffa, P. Biglioli, M. Napolitano, M.C. Capogrossi, and M. Pesce SDF-1 involvement in endothelial phenotype and ischemia-induced recruitment of bone marrow progenitor cells Blood 104 2004 3472 3482
42. V.L. Ballard, and J.M. Edelberg Stem cells and the regeneration of the aging cardiovascular system Circ. Res. 100 2007 1116 1127
43. D. Kuraitis, P. Zhang, Y. Zhang, D.T. Padavan, K. McEwan, T. Sofrenovic, D. McKee, J. Zhang, M. Griffith, X. Cao, A. Musaro, M. Ruel, and E.J. Suuronen A stromal cell-derived factor-1 releasing matrix enhances the progenitor cell response and blood vessel growth in ischaemic skeletal muscle Eur. Cell. Mater. 22 2011 109 123
44. P.T. Thevenot, A.M. Nair, J. Shen, P. Lotfi, C.Y. Ko, and L. Tang The effect of incorporation of SDF-1alpha into PLGA scaffolds on stem cell recruitment and the inflammatory response Biomaterials 31 2010 3997 4008
45. T. Netelenbos, S. Zuijderduijn, J. Van Den Born, F.L. Kessler, S. Zweegman, P.C. Huijgens, and A.M. Drager Proteoglycans guide SDF-1-induced migration of hematopoietic progenitor cells J. Leukoc. Biol. 72 2002 353 362
46. C. Laguri, R. Sadir, P. Rueda, F. Baleux, P. Gans, F. Arenzana-Seisdedos, and H. Lortat-Jacob The novel CXCL12gamma isoform encodes an unstructured cationic domain which regulates bioactivity and interaction with both glycosaminoglycans and CXCR4 PLoS One 2 2007 e1110
47. Y. Wang, and D.J. Irvine Engineering chemoattractant gradients using chemokine-releasing polysaccharide microspheres Biomaterials 32 2011 4903 4913
48. A.T. Askari, S. Unzek, Z.B. Popovic, C.K. Goldman, F. Forudi, M. Kiedrowski, A. Rovner, S.G. Ellis, J.D. Thomas, P.E. DiCorleto, E.J. Topol, and M.S. Penn Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy Lancet 362 2003 697 703
49. T. Sasaki, R. Fukazawa, S. Ogawa, S. Kanno, T. Nitta, M. Ochi, and K. Shimizu Stromal cell-derived factor-1alpha improves infarcted heart function through angiogenesis in mice Pediatr. Int. 49 2007 966 971
50. A. Saxena, J.E. Fish, M.D. White, S. Yu, J.W. Smyth, R.M. Shaw, J.M. DiMaio, and D. Srivastava Stromal cell-derived factor-1alpha is cardioprotective after myocardial infarction Circulation 117 2008 2224 2231
51. N. Signoret, J. Oldridge, A. Pelchen-Matthews, P.J. Klasse, T. Tran, L.F. Brass, M.M. Rosenkilde, T.W. Schwartz, W. Holmes, W. Dallas, M.A. Luther, T.N. Wells, J.A. Hoxie, and M. Marsh Phorbol esters and SDF-1 induce rapid endocytosis and down modulation of the chemokine receptor CXCR4 J. Cell Biol. 139 1997 651 664
52. N.I. Tarasova, R.H. Stauber, and C.J. Michejda Spontaneous and ligand-induced trafficking of CXC-chemokine receptor 4 J. Biol. Chem. 273 1998 15883 15886
53. M.V. Tsurkan, K. Chwalek, K.R. Levental, U. Freudenberg, and C. Werner Modular starPEG-heparin gels with bifunctional peptide linkers Macromol Rapid Commun 31 2010 1529 1533