Skip to main content
SpringerLink
Log in

Manipulating the Intersection of Angiogenesis and Inflammation

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

There exists a critical need to develop strategies that promote blood vessel formation (neovascularization) in virtually all tissue engineering and regenerative medicine efforts. While research typically focuses on understanding and exploiting the role of angiogenic factors and vascular cells on new blood vessel formation, the activity of the immune system is being increasingly recognized to impact vascular formation and adaptation. This review will provide both an overview of the intersection of angiogenesis and the immune system, and how biomaterials may be designed to promote favorable interactions between these two systems to promote effective vascularization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Ali, O. A., N. Huebsch, L. Cao, G. Dranoff, and D. J. Mooney. Infection-mimicking materials to program dendritic cells in situ. Nat. Mater. 8:151–158, 2009.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Alsberg, E., H. J. Kong, Y. Hirano, M. K. Smith, A. Albeiruti, and D. J. Mooney. Regulating bone formation via controlled scaffold degradation. J. Dent. Res. 82:903–908, 2003.

    Article  CAS  PubMed  Google Scholar 

  3. Anderson, J. M., A. Rodriguez, and D. T. Chang. Foreign body reaction to biomaterials. Semin. Immunol. 20:86–100, 2008.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Awojoodu, A. O., M. E. Ogle, L. S. Sefcik, D. T. Bowers, K. Martin, K. L. Brayman, K. R. Lynch, S. M. Peirce-Cottler, and E. Botchwey. Sphingosine 1-phosphate receptor 3 regulates recruitment of anti-inflammatory monocytes to microvessels during implant arteriogenesis. Proc. Natl. Acad. Sci. USA 110:13785–13790, 2013.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Ballotta, V., A. Driessen-Mol, C. V. Bouten, and F. P. Baaijens. Strain-dependent modulation of macrophage polarization within scaffolds. Biomaterials 35:4919–4928, 2014.

    Article  CAS  PubMed  Google Scholar 

  6. Barth, K. A., J. D. Waterfield, and D. M. Brunette. The effect of surface roughness on raw 264.7 macrophage phenotype. J. Biomed. Mater. Res. A 101:2679–2688, 2013.

    Article  PubMed  Google Scholar 

  7. Benitez-Bribiesca, L., A. Wong, D. Utrera, and E. Castellanos. The role of mast cell tryptase in neoangiogenesis of premalignant and malignant lesions of the uterine cervix. J. Histochem. Cytochem. 49:1061–1062, 2001.

    Article  CAS  PubMed  Google Scholar 

  8. Bhrany, A. D., C. A. Irvin, K. Fujitani, Z. Liu, and B. D. Ratner. Evaluation of a sphere-templated polymeric scaffold as a subcutaneous implant. JAMA Facial Plast. Surg. 15:29–33, 2013.

    Article  PubMed  Google Scholar 

  9. Blair, R. J., H. Meng, M. J. Marchese, S. Ren, L. B. Schwartz, M. G. Tonnesen, and B. L. Gruber. Human mast cells stimulate vascular tube formation. Tryptase is a novel, potent angiogenic factor. J. Clin. Investig. 99:2691–2700, 1997.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Blotnick, S., G. E. Peoples, M. R. Freeman, T. J. Eberlein, and M. Klagsbrun. T lymphocytes synthesize and export heparin-binding epidermal growth factor-like growth factor and basic fibroblast growth factor, mitogens for vascular cells and fibroblasts: differential production and release by CD4+ and CD8+ T cells. Proc. Natl. Acad. Sci. USA 91:2890–2894, 1994.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Bota, P. C., A. M. Collie, P. Puolakkainen, R. B. Vernon, E. H. Sage, B. D. Ratner, and P. S. Stayton. Biomaterial topography alters healing in vivo and monocyte/macrophage activation in vitro. J. Biomed. Mater. Res. A 95:649–657, 2010.

    Article  PubMed Central  PubMed  Google Scholar 

  12. Chan, G., and D. J. Mooney. Ca(2 +) released from calcium alginate gels can promote inflammatory responses in vitro and in vivo. Acta Biomater. 9:9281–9291, 2013.

    Article  CAS  PubMed  Google Scholar 

  13. Chehroudi, B., S. Ghrebi, H. Murakami, J. D. Waterfield, G. Owen, and D. M. Brunette. Bone formation on rough, but not polished, subcutaneously implanted ti surfaces is preceded by macrophage accumulation. J. Biomed. Mater. Res. A 93:724–737, 2010.

    PubMed  Google Scholar 

  14. Chen, W., W. Jin, N. Hardegen, K. J. Lei, L. Li, N. Marinos, G. McGrady, and S. M. Wahl. Conversion of peripheral CD4+ CD25− naive t cells to CD4+ CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198:1875–1886, 2003.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Chen, S., J. A. Jones, Y. Xu, H. Y. Low, J. M. Anderson, and K. W. Leong. Characterization of topographical effects on macrophage behavior in a foreign body response model. Biomaterials 31:3479–3491, 2010.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Conejo-Garcia, J. R., F. Benencia, M. C. Courreges, E. Kang, A. Mohamed-Hadley, R. J. Buckanovich, D. O. Holtz, A. Jenkins, H. Na, L. Zhang, D. S. Wagner, D. Katsaros, R. Caroll, and G. Coukos. Tumor-infiltrating dendritic cell precursors recruited by a beta-defensin contribute to vasculogenesis under the influence of Vegf-A. Nat. Med. 10:950–958, 2004.

    Article  CAS  PubMed  Google Scholar 

  17. Couffinhal, T., M. Silver, M. Kearney, A. Sullivan, B. Witzenbichler, M. Magner, B. Annex, K. Peters, and J. M. Isner. Impaired collateral vessel development associated with reduced expression of vascular endothelial growth factor in apoe−/− mice. Circulation 99:3188–3198, 1999.

    Article  CAS  PubMed  Google Scholar 

  18. Coussens, L. M., and Z. Werb. Inflammation and cancer. Nature 420:860–867, 2002.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Curiel, T. J., P. Cheng, P. Mottram, X. Alvarez, L. Moons, M. Evdemon-Hogan, S. Wei, L. Zou, I. Kryczek, G. Hoyle, A. Lackner, P. Carmeliet, and W. Zou. Dendritic cell subsets differentially regulate angiogenesis in human ovarian cancer. Cancer Res. 64:5535–5538, 2004.

    Article  CAS  PubMed  Google Scholar 

  20. DiPietro, L. A. Wound healing: the role of the macrophage and other immune cells. Shock 4:233–240, 1995.

    Article  CAS  PubMed  Google Scholar 

  21. Discher, D. E., P. Janmey, and Y. L. Wang. Tissue cells feel and respond to the stiffness of their substrate. Science 310:1139–1143, 2005.

    Article  CAS  PubMed  Google Scholar 

  22. Druecke, D., S. Langer, E. Lamme, J. Pieper, M. Ugarkovic, H. U. Steinau, and H. H. Homann. Neovascularization of poly(ether ester) block-copolymer scaffolds in vivo: long-term investigations using intravital fluorescent microscopy. J. Biomed. Mater. Res. A 68:10–18, 2004.

    Article  PubMed  Google Scholar 

  23. Drury, J. L., and D. J. Mooney. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24:4337–4351, 2003.

    Article  CAS  PubMed  Google Scholar 

  24. Fantin, A., J. M. Vieira, G. Gestri, L. Denti, Q. Schwarz, S. Prykhozhij, F. Peri, S. W. Wilson, and C. Ruhrberg. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of Vegf-mediated endothelial tip cell induction. Blood 116:829–840, 2010.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Franz, S., S. Rammelt, D. Scharnweber, and J. C. Simon. Immune responses to implants—a review of the implications for the design of immunomodulatory biomaterials. Biomaterials 32:6692–6709, 2011.

    Article  CAS  PubMed  Google Scholar 

  26. Freeman, M. R., F. X. Schneck, M. L. Gagnon, C. Corless, S. Soker, K. Niknejad, G. E. Peoples, and M. Klagsbrun. Peripheral blood t lymphocytes and lymphocytes infiltrating human cancers express vascular endothelial growth factor: a potential role for t cells in angiogenesis. Cancer Res. 55:4140–4145, 1995.

    CAS  PubMed  Google Scholar 

  27. Galli, S. J., N. Borregaard, and T. A. Wynn. Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat. Immunol. 12:1035–1044, 2011.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Gruber, B. L., M. J. Marchese, K. Suzuki, L. B. Schwartz, Y. Okada, H. Nagase, and N. S. Ramamurthy. Synovial procollagenase activation by human mast cell tryptase dependence upon matrix metalloproteinase 3 activation. J. Clin. Investig. 84:1657–1662, 1989.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Hao, Q., Y. Chen, Y. Zhu, Y. Fan, D. Palmer, H. Su, W. L. Young, and G. Y. Yang. Neutrophil depletion decreases Vegf-induced focal angiogenesis in the mature mouse brain. J. Cereb. Blood Flow Metab. 27:1853–1860, 2007.

    Article  CAS  PubMed  Google Scholar 

  30. Harel-Adar, T., T. Ben Mordechai, Y. Amsalem, M. S. Feinberg, J. Leor, and S. Cohen. Modulation of cardiac macrophages by phosphatidylserine-presenting liposomes improves infarct repair. Proc. Natl. Acad. Sci. USA 108:1827–1832, 2011.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Heil, M., T. Ziegelhoeffer, F. Pipp, S. Kostin, S. Martin, M. Clauss, and W. Schaper. Blood monocyte concentration is critical for enhancement of collateral artery growth. Am. J. Physiol. Heart Circ. Physiol. 283:H2411–H2419, 2002.

    Article  CAS  PubMed  Google Scholar 

  32. Heil, M., T. Ziegelhoeffer, S. Wagner, B. Fernandez, A. Helisch, S. Martin, S. Tribulova, W. A. Kuziel, G. Bachmann, and W. Schaper. Collateral artery growth (arteriogenesis) after experimental arterial occlusion is impaired in mice lacking CC-chemokine receptor-2. Circ. Res. 94:671–677, 2004.

    Article  CAS  PubMed  Google Scholar 

  33. Heissig, B., S. Rafii, H. Akiyama, Y. Ohki, Y. Sato, T. Rafael, Z. Zhu, D. J. Hicklin, K. Okumura, H. Ogawa, Z. Werb, and K. Hattori. Low-dose irradiation promotes tissue revascularization through Vegf release from mast cells and mmp-9-mediated progenitor cell mobilization. J. Exp. Med. 202:739–750, 2005.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Hellingman, A. A., J. J. Zwaginga, R. T. van Beem, R. M. S. M. C. Te, J. F. Hamming, W. E. Fibbe, P. H. Quax, and S. B. Geutskens. T-cell-pre-stimulated monocytes promote neovascularisation in a murine hind limb ischaemia model. Eur. J. Vasc. Endovasc. Surg. 41:418–428, 2011.

    Article  CAS  PubMed  Google Scholar 

  35. Hetrick, E. M., H. L. Prichard, B. Klitzman, and M. H. Schoenfisch. Reduced foreign body response at nitric oxide-releasing subcutaneous implants. Biomaterials 28:4571–4580, 2007.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Hirosue, S., I. C. Kourtis, A. J. van der Vlies, J. A. Hubbell, and M. A. Swartz. Antigen delivery to dendritic cells by poly(propylene sulfide) nanoparticles with disulfide conjugated peptides: cross-presentation and t cell activation. Vaccine 28:7897–7906, 2010.

    Article  CAS  PubMed  Google Scholar 

  37. Huebsch, N., P. R. Arany, A. S. Mao, D. Shvartsman, O. A. Ali, S. A. Bencherif, J. Rivera-Feliciano, and D. J. Mooney. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat. Mater. 9:518–526, 2010.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Hunt, T. K., D. R. Knighton, K. K. Thakral, W. H. Goodson, 3rd, and W. S. Andrews. Studies on inflammation and wound healing: angiogenesis and collagen synthesis stimulated in vivo by resident and activated wound macrophages. Surgery 96:48–54, 1984.

    CAS  PubMed  Google Scholar 

  39. Jin, R., G. Yang, and G. Li. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J. Leukoc. Biol. 87:779–789, 2010.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Jones, J. A., D. T. Chang, H. Meyerson, E. Colton, I. K. Kwon, T. Matsuda, and J. M. Anderson. Proteomic analysis and quantification of cytokines and chemokines from biomaterial surface-adherent macrophages and foreign body giant cells. J. Biomed. Mater. Res. A 83:585–596, 2007.

    Article  PubMed  Google Scholar 

  41. Kao, W. J., and D. Lee. In vivo modulation of host response and macrophage behavior by polymer networks grafted with fibronectin-derived biomimetic oligopeptides: the role of RGD and PHSRN domains. Biomaterials 22:2901–2909, 2001.

    Article  CAS  PubMed  Google Scholar 

  42. Kao, W. J., D. Lee, J. C. Schense, and J. A. Hubbell. Fibronectin modulates macrophage adhesion and FBGC formation: the role of RGD, PHSRN, and PRRARV domains. J. Biomed. Mater. Res. 55:79–88, 2001.

    Article  CAS  PubMed  Google Scholar 

  43. Kearney, C. J., and D. J. Mooney. Macroscale delivery systems for molecular and cellular payloads. Nat. Mater. 12:1004–1017, 2013.

    Article  CAS  PubMed  Google Scholar 

  44. Khmelewski, E., A. Becker, T. Meinertz, and W. D. Ito. Tissue resident cells play a dominant role in arteriogenesis and concomitant macrophage accumulation. Circ. Res. 95:E56–E64, 2004.

    Article  CAS  PubMed  Google Scholar 

  45. Kim, J., W. A. Li, W. Sands, and D. J. Mooney. Effect of pore structure of macroporous poly(lactide-co-glycolide) scaffolds on the in vivo enrichment of dendritic cells. ACS Appl. Mater. Interfaces 6:8505–8512, 2014.

    Article  CAS  PubMed  Google Scholar 

  46. Koffler, J., K. Kaufman-Francis, Y. Shandalov, D. Egozi, D. A. Pavlov, A. Landesberg, and S. Levenberg. Improved vascular organization enhances functional integration of engineered skeletal muscle grafts. Proc. Natl. Acad. Sci. USA 108:14789–14794, 2011.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. la Sala, A., L. Pontecorvo, A. Agresta, G. Rosano, and E. Stabile. Regulation of collateral blood vessel development by the innate and adaptive immune system. Trends Mol. Med. 18:494–501, 2012.

    Article  PubMed  Google Scholar 

  48. Lee, K. Y., M. C. Peters, K. W. Anderson, and D. J. Mooney. Controlled growth factor release from synthetic extracellular matrices. Nature 408:998–1000, 2000.

    Article  CAS  PubMed  Google Scholar 

  49. Li, W. A., and D. J. Mooney. Materials based tumor immunotherapy vaccines. Curr. Opin. Immunol. 25:238–245, 2013.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  50. Lin, E. Y., J. F. Li, L. Gnatovskiy, Y. Deng, L. Zhu, D. A. Grzesik, H. Qian, X. N. Xue, and J. W. Pollard. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 66:11238–11246, 2006.

    Article  CAS  PubMed  Google Scholar 

  51. Lutolf, M. P., G. P. Raeber, A. H. Zisch, N. Tirelli, and J. A. Hubbell. Cell-responsive synthetic hydrogels. Adv. Mater. 15:888–892, 2003.

    Article  CAS  Google Scholar 

  52. Lutolf, M. P., F. E. Weber, H. G. Schmoekel, J. C. Schense, T. Kohler, R. Muller, and J. A. Hubbell. Repair of bone defects using synthetic mimetics of collagenous extracellular matrices. Nat. Biotechnol. 21:513–518, 2003.

    Article  CAS  PubMed  Google Scholar 

  53. Madden, L. R., D. J. Mortisen, E. M. Sussman, S. K. Dupras, J. A. Fugate, J. L. Cuy, K. D. Hauch, M. A. Laflamme, C. E. Murry, and B. D. Ratner. Proangiogenic scaffolds as functional templates for cardiac tissue engineering. Proc. Natl. Acad. Sci. USA 107:15211–15216, 2010.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  54. Mann, B. K., R. H. Schmedlen, and J. L. West. Tethered-TGF-<i>β</i> increases extracellular matrix production of vascular smooth muscle cells. Biomaterials 22(5):439–444, 2001.

    Article  CAS  PubMed  Google Scholar 

  55. Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25:677–686, 2004.

    Article  CAS  PubMed  Google Scholar 

  56. Mantovani, A., S. Sozzani, M. Locati, P. Allavena, and A. Sica. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized m2 mononuclear phagocytes. Trends Immunol. 23:549–555, 2002.

    Article  CAS  PubMed  Google Scholar 

  57. McWhorter, F. Y., T. Wang, P. Nguyen, T. Chung, and W. F. Liu. Modulation of macrophage phenotype by cell shape. Proc. Natl. Acad. Sci. USA 110:17253–17258, 2013.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. Mokarram, N., and R. V. Bellamkonda. A perspective on immunomodulation and tissue repair. Ann. Biomed. Eng. 42:338–351, 2014.

    Article  PubMed  Google Scholar 

  59. Mor, F., F. J. Quintana, and I. R. Cohen. Angiogenesis-inflammation cross-talk: vascular endothelial growth factor is secreted by activated T cells and induces Th1 polarization. J. Immunol. 172:4618–4623, 2004.

    Article  CAS  PubMed  Google Scholar 

  60. Mosser, D. M., and J. P. Edwards. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8:958–969, 2008.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. Mountziaris, P. M., and A. G. Mikos. Modulation of the inflammatory response for enhanced bone tissue regeneration. Tissue. Eng. Part B 14:179–186, 2008.

    Article  CAS  Google Scholar 

  62. Moyano, D. F., M. Goldsmith, D. J. Solfiell, D. Landesman-Milo, O. R. Miranda, D. Peer, and V. M. Rotello. Nanoparticle hydrophobicity dictates immune response. J. Am. Chem. Soc. 134:3965–3967, 2012.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. Nikkhah, M., F. Edalat, S. Manoucheri, and A. Khademhosseini. Engineering microscale topographies to control the cell–substrate interface. Biomaterials 33:5230–5246, 2012.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. Niklason, L. E., J. Gao, W. M. Abbott, K. K. Hirschi, S. Houser, R. Marini, and R. Langer. Functional arteries grown in vitro. Science 284:489–493, 1999.

    Article  CAS  PubMed  Google Scholar 

  65. Norrby, K. Mast cells and angiogenesis. APMIS 110:355–371, 2002.

    Article  CAS  PubMed  Google Scholar 

  66. Nozawa, H., C. Chiu, and D. Hanahan. Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc. Natl. Acad. Sci. USA 103:12493–12498, 2006.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  67. Ohki, Y., B. Heissig, Y. Sato, H. Akiyama, Z. Zhu, D. J. Hicklin, K. Shimada, H. Ogawa, H. Daida, K. Hattori, and A. Ohsaka. Granulocyte colony-stimulating factor promotes neovascularization by releasing vascular endothelial growth factor from neutrophils. FASEB J. 19:2005–2007, 2005.

    CAS  PubMed  Google Scholar 

  68. Park, J., S. H. Wrzesinski, E. Stern, M. Look, J. Criscione, R. Ragheb, S. M. Jay, S. L. Demento, A. Agawu, P. Licona Limon, A. F. Ferrandino, D. Gonzalez, A. Habermann, R. A. Flavell, and T. M. Fahmy. Combination delivery of TGF-beta inhibitor and il-2 by nanoscale liposomal polymeric gels enhances tumour immunotherapy. Nat. Mater. 11:895–905, 2012.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. Patil, S. D., F. Papadimitrakopoulos, and D. J. Burgess. Dexamethasone-loaded poly(lactic-co-glycolic) acid microspheres/poly(vinyl alcohol) hydrogel composite coatings for inflammation control. Diabetes Technol. Ther. 6:887–897, 2004.

    Article  CAS  PubMed  Google Scholar 

  70. Pinhal-Enfield, G., M. Ramanathan, G. Hasko, S. N. Vogel, A. L. Salzman, G. J. Boons, and S. J. Leibovich. An angiogenic switch in macrophages involving synergy between toll-like receptors 2, 4, 7, and 9 and adenosine a(2a) receptors. Am. J. Pathol. 163:711–721, 2003.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  71. Puxeddu, I., A. Alian, A. M. Piliponsky, D. Ribatti, A. Panet, and F. Levi-Schaffer. Human peripheral blood eosinophils induce angiogenesis. Int. J. Biochem. Cell Biol. 37:628–636, 2005.

    Article  CAS  PubMed  Google Scholar 

  72. Ribatti, D., A. Vacca, A. Marzullo, B. Nico, R. Ria, L. Roncali, and F. Dammacco. Angiogenesis and mast cell density with tryptase activity increase simultaneously with pathological progression in b-cell non-hodgkin’s lymphomas. Int. J. Cancer 85:171–175, 2000.

    Article  CAS  PubMed  Google Scholar 

  73. Riboldi, E., T. Musso, E. Moroni, C. Urbinati, S. Bernasconi, M. Rusnati, L. Adorini, M. Presta, and S. Sozzani. Cutting edge: proangiogenic properties of alternatively activated dendritic cells. J. Immunol. 175:2788–2792, 2005.

    Article  CAS  PubMed  Google Scholar 

  74. Richardson, T. P., M. C. Peters, A. B. Ennett, and D. J. Mooney. Polymeric system for dual growth factor delivery. Nat. Biotechnol. 19:1029–1034, 2001.

    Article  CAS  PubMed  Google Scholar 

  75. Roh, J. D., R. Sawh-Martinez, M. P. Brennan, S. M. Jay, L. Devine, D. A. Rao, T. Yi, T. L. Mirensky, A. Nalbandian, B. Udelsman, N. Hibino, T. Shinoka, W. M. Saltzman, E. Snyder, T. R. Kyriakides, J. S. Pober, and C. K. Breuer. Tissue-engineered vascular grafts transform into mature blood vessels via an inflammation-mediated process of vascular remodeling. Proc. Natl. Acad. Sci. USA 107:4669–4674, 2010.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  76. Rowley, J. A., G. Madlambayan, and D. J. Mooney. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials 20:45–53, 1999.

    Article  CAS  PubMed  Google Scholar 

  77. Rucker, M., M. W. Laschke, D. Junker, C. Carvalho, A. Schramm, R. Mulhaupt, N. C. Gellrich, and M. D. Menger. Angiogenic and inflammatory response to biodegradable scaffolds in dorsal skinfold chambers of mice. Biomaterials 27:5027–5038, 2006.

    Article  PubMed  Google Scholar 

  78. Seong, S. Y., and P. Matzinger. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat. Rev. Immunol. 4:469–478, 2004.

    Article  CAS  PubMed  Google Scholar 

  79. Silva, E. A., E. S. Kim, H. J. Kong, and D. J. Mooney. Material-based deployment enhances efficacy of endothelial progenitor cells. Proc. Natl. Acad. Sci. USA 105:14347–14352, 2008.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  80. Silvestre, J. S., Z. Mallat, A. Tedgui, and B. I. Levy. Post-ischaemic neovascularization and inflammation. Cardiovasc. Res. 78:242–249, 2008.

    Article  CAS  PubMed  Google Scholar 

  81. Sozzani, S., M. Rusnati, E. Riboldi, S. Mitola, and M. Presta. Dendritic cell-endothelial cell cross-talk in angiogenesis. Trends Immunol. 28:385–392, 2007.

    Article  CAS  PubMed  Google Scholar 

  82. Spiller, K. L., R. R. Anfang, K. J. Spiller, J. Ng, K. R. Nakazawa, J. W. Daulton, and G. Vunjak-Novakovic. The role of macrophage phenotype in vascularization of tissue engineering scaffolds. Biomaterials 35:4477–4488, 2014.

    Article  CAS  PubMed  Google Scholar 

  83. Stabile, E., M. S. Burnett, C. Watkins, T. Kinnaird, A. Bachis, A. la Sala, J. M. Miller, M. Shou, S. E. Epstein, and S. Fuchs. Impaired arteriogenic response to acute hindlimb ischemia in CD4-knockout mice. Circulation 108:205–210, 2003.

    Article  PubMed  Google Scholar 

  84. Stabile, E., T. Kinnaird, A. la Sala, S. K. Hanson, C. Watkins, U. Campia, M. Shou, S. Zbinden, S. Fuchs, H. Kornfeld, S. E. Epstein, and M. S. Burnett. CD8+ T lymphocytes regulate the arteriogenic response to ischemia by infiltrating the site of collateral vessel development and recruiting CD4+ mononuclear cells through the expression of interleukin-16. Circulation 113:118–124, 2006.

    Article  PubMed  Google Scholar 

  85. Stack, M. S., and D. A. Johnson. Human mast cell tryptase activates single-chain urinary-type plasminogen activator (pro-urokinase). J. Biol. Chem. 269:9416–9419, 1994.

    CAS  PubMed  Google Scholar 

  86. Sunderkotter, C., K. Steinbrink, M. Goebeler, R. Bhardwaj, and C. Sorg. Macrophages and angiogenesis. J. Leukoc. Biol. 55:410–422, 1994.

    CAS  PubMed  Google Scholar 

  87. Sussman, E. M., M. C. Halpin, J. Muster, R. T. Moon, and B. D. Ratner. Porous implants modulate healing and induce shifts in local macrophage polarization in the foreign body reaction. Ann. Biomed. Eng. 42:1508–1516, 2014.

    Article  PubMed  Google Scholar 

  88. Takeda, Y., S. Costa, E. Delamarre, C. Roncal, R. Leite de Oliveira, M. L. Squadrito, V. Finisguerra, S. Deschoemaeker, F. Bruyere, M. Wenes, A. Hamm, J. Serneels, J. Magat, T. Bhattacharyya, A. Anisimov, B. F. Jordan, K. Alitalo, P. Maxwell, B. Gallez, Z. W. Zhuang, Y. Saito, M. Simons, M. De Palma, and M. Mazzone. Macrophage skewing by PHD2 haplodeficiency prevents ischaemia by inducing arteriogenesis. Nature 479:122–126, 2011.

    Article  CAS  PubMed  Google Scholar 

  89. Tang, L., T. A. Jennings, and J. W. Eaton. Mast cells mediate acute inflammatory responses to implanted biomaterials. Proc. Natl. Acad. Sci. USA 95:8841–8846, 1998.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  90. Thomas, S. N., A. J. van der Vlies, C. P. O’Neil, S. T. Reddy, S. S. Yu, T. D. Giorgio, M. A. Swartz, and J. A. Hubbell. Engineering complement activation on polypropylene sulfide vaccine nanoparticles. Biomaterials 32:2194–2203, 2011.

    Article  CAS  PubMed  Google Scholar 

  91. Tidball, J. G. Inflammatory processes in muscle injury and repair. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288:R345–R353, 2005.

    Article  CAS  PubMed  Google Scholar 

  92. van Beem, R. T., W. A. Noort, C. Voermans, M. Kleijer, A. ten Brinke, S. M. van Ham, C. E. van der Schoot, and J. J. Zwaginga. The presence of activated CD4(+) T cells is essential for the formation of colony-forming unit-endothelial cells by CD14(+) cells. J. Immunol. 180:5141–5148, 2008.

    Article  PubMed  Google Scholar 

  93. van Weel, V., R. E. Toes, L. Seghers, M. M. Deckers, M. R. de Vries, P. H. Eilers, J. Sipkens, A. Schepers, D. Eefting, V. W. van Hinsbergh, J. H. van Bockel, and P. H. Quax. Natural killer cells and CD4+ T-cells modulate collateral artery development. Arterioscler. Thromb. Vasc. Biol. 27:2310–2318, 2007.

    Article  PubMed  Google Scholar 

  94. Willenborg, S., T. Lucas, G. van Loo, J. A. Knipper, T. Krieg, I. Haase, B. Brachvogel, M. Hammerschmidt, A. Nagy, N. Ferrara, M. Pasparakis, and S. A. Eming. CCR2 recruits an inflammatory macrophage subpopulation critical for angiogenesis in tissue repair. Blood 120:613–625, 2012.

    Article  CAS  PubMed  Google Scholar 

  95. Yang, L., L. M. DeBusk, K. Fukuda, B. Fingleton, B. Green-Jarvis, Y. Shyr, L. M. Matrisian, D. P. Carbone, and P. C. Lin. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 6:409–421, 2004.

    Article  CAS  PubMed  Google Scholar 

  96. Yoshida, M., J. Mata, and J. E. Babensee. Effect of poly(lactic-co-glycolic acid) contact on maturation of murine bone marrow-derived dendritic cells. J. Biomed. Mater. Res. A 80:7–12, 2007.

    Article  PubMed  Google Scholar 

  97. Zdolsek, J., J. W. Eaton, and L. Tang. Histamine release and fibrinogen adsorption mediate acute inflammatory responses to biomaterial implants in humans. J. Transl. Med. 5:31, 2007.

    Article  PubMed Central  PubMed  Google Scholar 

  98. Zhao, X., J. Kim, C. A. Cezar, N. Huebsch, K. Lee, K. Bouhadir, and D. J. Mooney. Active scaffolds for on-demand drug and cell delivery. Proc. Natl. Acad. Sci. USA 108:67–72, 2011.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  99. Zhou, X., Y. C. Luo, W. J. Ji, L. Zhang, Y. Dong, L. Ge, R. Y. Lu, H. Y. Sun, Z. Z. Guo, G. H. Yang, T. M. Jiang, and Y. M. Li. Modulation of mononuclear phagocyte inflammatory response by liposome-encapsulated voltage gated sodium channel inhibitor ameliorates myocardial ischemia/reperfusion injury in rats. PLoS ONE 8:e74390, 2013.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors acknowledge support from the NIH (R01 DE013349 and R01 HL069957), the NSF GRFP (Grant No. DGE1144152), and the Wyss Institute.

Conflict of interest

The authors declare no conflicts of interest.

Author information

Authors and Affiliations

  1. School of Engineering and Applied Sciences, Harvard University, Pierce Hall, Room 319, Cambridge, MA, 02138, USA

    Brian J. Kwee & David J. Mooney

  2. Wyss Institute for Biologically Inspired Engineering at Harvard University, Boston, MA, 02115, USA

    Brian J. Kwee & David J. Mooney

Authors
  1. Brian J. Kwee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David J. Mooney
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David J. Mooney.

Additional information

Associate Editor Nadya Lumelsky oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kwee, B.J., Mooney, D.J. Manipulating the Intersection of Angiogenesis and Inflammation. Ann Biomed Eng 43, 628–640 (2015). https://doi.org/10.1007/s10439-014-1145-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-014-1145-y

Keywords

Search

Navigation