Modulation of mast cell adhesion, proliferation, and cytokine secretion on electrospun bioresorbable vascular grafts.

Mast cells synthesize several potent angiogenic factors and can also stimulate fibroblasts, endothelial cells, and macrophages. An understanding of how they participate in wound healing and angiogenesis is important to further our knowledge about in situ vascular prosthetic regeneration. The adhesion, proliferation, and cytokine secretion of bone marrow-derived murine mast cells (BMMC) on electrospun polydioxanone, polycaprolactone, and silk scaffolds, as well as tissue culture plastic, has been investigated in the presence or absence of IL-3, stem cell factor, IgE and IgE with a crosslinking antigen, dinitrophenol-conjugated albumin (DNP). It was previously believed that only activated BMMCs exhibit adhesion and cytokine secretion. However, this study shows nonactivated BMMC adhesion to electrospun scaffolds. Silk scaffold was not found to be conducive for mast cell adhesion and cytokine secretion. Activation by IgE and DNP significantly enhanced mast cell adhesion, proliferation, migration, and secretion of tumor necrosis factor alpha, macrophage inflammatory protein-1α, and IL-13. This indicates that mast cells might play a role in the process of biomaterial integration into the host tissue, regeneration, and possibly angiogenesis.

[1]  S. Spiegel,et al.  IL-4 and TGF-β1 Counterbalance One Another while Regulating Mast Cell Homeostasis , 2010, The Journal of Immunology.

[2]  Benjamin M. Wu,et al.  Modification of the diphenylamine assay for cell quantification in three-dimensional biodegradable polymeric scaffolds. , 2009, Journal of biomedical materials research. Part B, Applied biomaterials.

[3]  G. Bowlin,et al.  Electrospinning-aligned and random polydioxanone–polycaprolactone–silk fibroin-blended scaffolds: geometry for a vascular matrix , 2009, Biomedical materials.

[4]  G. Bowlin,et al.  Modulation of murine innate and acquired immune responses following in vitro exposure to electrospun blends of collagen and polydioxanone. , 2009, Journal of biomedical materials research. Part A.

[5]  K. Khazaie,et al.  Mast cells in tumor growth: angiogenesis, tissue remodelling and immune-modulation. , 2009, Biochimica et biophysica acta.

[6]  M. Grigioni,et al.  Structural characterization and cell response evaluation of electrospun PCL membranes: micrometric versus submicrometric fibers. , 2009, Journal of biomedical materials research. Part A.

[7]  J. L. Gomez Ribelles,et al.  Analysis of the biological response of endothelial and fibroblast cells cultured on synthetic scaffolds with various hydrophilic/hydrophobic ratios: influence of fibronectin adsorption and conformation. , 2009, Tissue engineering. Part A.

[8]  K. Fung,et al.  Leukocyte inflammatory response in a rat urinary bladder regeneration model using porcine small intestinal submucosa scaffold. , 2009, Tissue engineering. Part A.

[9]  G. Bowlin,et al.  Angiogenic potential of human macrophages on electrospun bioresorbable vascular grafts , 2009, Biomedical materials.

[10]  Robert Gurny,et al.  Degradation and Healing Characteristics of Small-Diameter Poly(&egr;-Caprolactone) Vascular Grafts in the Rat Systemic Arterial Circulation , 2008, Circulation.

[11]  Melissa A Brown,et al.  Mast Cells , 2008, Annals of the New York Academy of Sciences.

[12]  David L Kaplan,et al.  In vitro evaluation of electrospun silk fibroin scaffolds for vascular cell growth. , 2008, Biomaterials.

[13]  Analiz Rodriguez,et al.  Foreign body reaction to biomaterials. , 2008, Seminars in immunology.

[14]  J. Lannutti,et al.  Mechanical characterization of electrospun polycaprolactone (PCL): a potential scaffold for tissue engineering. , 2008, Journal of biomechanical engineering.

[15]  David L. Kaplan,et al.  Silk-based electrospun tubular scaffolds for tissue-engineered vascular grafts , 2008, Journal of biomaterials science. Polymer edition.

[16]  B. Hsiao,et al.  Functional electrospun nanofibrous scaffolds for biomedical applications. , 2007, Advanced drug delivery reviews.

[17]  Benjamin G Keselowsky,et al.  Role of plasma fibronectin in the foreign body response to biomaterials. , 2007, Biomaterials.

[18]  D. C. Knapp,et al.  Electrospun polydioxanone–elastin blends: potential for bioresorbable vascular grafts , 2006, Biomedical materials.

[19]  S. Ramakrishna,et al.  Fabrication of collagen-coated biodegradable polymer nanofiber mesh and its potential for endothelial cells growth. , 2005, Biomaterials.

[20]  T. Kawakami,et al.  Mast Cell Survival and Activation by IgE in the Absence of Antigen: A Consideration of the Biologic Mechanisms and Relevance1 , 2005, The Journal of Immunology.

[21]  Silvano Sozzani,et al.  The chemokine system in diverse forms of macrophage activation and polarization. , 2004, Trends in immunology.

[22]  E. von Stebut,et al.  Macrophage inflammatory protein-1. , 2004, The international journal of biochemistry & cell biology.

[23]  Younan Xia,et al.  Electrospinning of Nanofibers: Reinventing the Wheel? , 2004 .

[24]  Harry V. Wright,et al.  Negative Regulation of Immunoglobulin E–dependent Allergic Responses by Lyn Kinase , 2004, The Journal of experimental medicine.

[25]  C. Hughes,et al.  Of Mice and Not Men: Differences between Mouse and Human Immunology , 2004, The Journal of Immunology.

[26]  David L Kaplan,et al.  Human bone marrow stromal cell responses on electrospun silk fibroin mats. , 2004, Biomaterials.

[27]  S. Pizzo,et al.  Mast cell–derived tumor necrosis factor induces hypertrophy of draining lymph nodes during infection , 2003, Nature Immunology.

[28]  J. Oliver,et al.  IgE alone stimulates mast cell adhesion to fibronectin via pathways similar to those used by IgE + antigen but distinct from those used by Steel factor. , 2003, Blood.

[29]  David L Kaplan,et al.  Macrophage responses to silk. , 2003, Biomaterials.

[30]  K. Norrby Mast cells and angiogenesis , 2002, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[31]  G. Nilsson,et al.  Essential Role of the Prosurvival bcl-2 Homologue A1 in Mast Cell Survival After Allergic Activation , 2001, The Journal of experimental medicine.

[32]  C. Noli,et al.  The mast cell in wound healing. , 2001, Veterinary dermatology.

[33]  R. Homer,et al.  Interleukin-13 Induces Tissue Fibrosis by Selectively Stimulating and Activating Transforming Growth Factor β1 , 2001, The Journal of experimental medicine.

[34]  B. Rollins,et al.  Wound Healing in MIP-1α−/− and MCP-1−/− Mice , 2001 .

[35]  D. Carbone,et al.  Regulation of mast cell survival by IgE. , 2001, Immunity.

[36]  Levi‐Schaffer,et al.  Activation of fibroblasts in collagen lattices by mast cell extract: a model of fibrosis , 2000, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[37]  D. Metcalfe,et al.  Mast cells in innate immunity , 2000, Immunological reviews.

[38]  A. Grützkau,et al.  Adhesion of human mast cells to extracellular matrix provides a co‐stimulatory signal for cytokine production , 1999, Immunology.

[39]  M. Artuc,et al.  Mast cells and their mediators in cutaneous wound healing – active participants or innocent bystanders? , 1999, Experimental dermatology.

[40]  J. Ryan,et al.  IL-4 Inhibits Mouse Mast Cell FcεRI Expression Through a STAT6-Dependent Mechanism , 1998, The Journal of Immunology.

[41]  S. Holgate,et al.  The role of mast cell tryptase in regulating endothelial cell proliferation, cytokine release, and adhesion molecule expression: tryptase induces expression of mRNA for IL-1 beta and IL-8 and stimulates the selective release of IL-8 from human umbilical vein endothelial cells. , 1998, Journal of immunology.

[42]  J W Eaton,et al.  Mast cells mediate acute inflammatory responses to implanted biomaterials. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[43]  M. Burdick,et al.  MIP-1alpha as a critical macrophage chemoattractant in murine wound repair. , 1998, The Journal of clinical investigation.

[44]  S. Galli Complexity and Redundancy in the Pathogenesis of Asthma: Reassessing the Roles of Mast Cells and T Cells , 1997, The Journal of experimental medicine.

[45]  E. Bröcker,et al.  Interleukin‐13 selectively induces monocyte chemoattractant protein‐1 synthesis and secretion by human endothelial cells. Involvement of IL‐4Rα and Stat6 phosphorylation , 1997, Immunology.

[46]  S. Ren,et al.  Human mast cells stimulate vascular tube formation. Tryptase is a novel, potent angiogenic factor. , 1997, The Journal of clinical investigation.

[47]  K. Akazawa,et al.  Umbilical vein endothelial cells are an important source of c‐kit and stem cell factor which regulate the proliferation of haemopoietic progenitor cells , 1996, British journal of haematology.

[48]  S. Abraham,et al.  Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-α , 1996, Nature.

[49]  R. Coffman,et al.  IL-13 selectively induces vascular cell adhesion molecule-1 expression in human endothelial cells. , 1995, Journal of immunology.

[50]  G. Nilsson,et al.  Stem cell factor is a chemotactic factor for human mast cells. , 1994, Journal of immunology.

[51]  M. Tsai,et al.  The c-kit ligand, stem cell factor, promotes mast cell survival by suppressing apoptosis. , 1994, The American journal of pathology.

[52]  L. Thomas,et al.  Murine mast cells attach to and migrate on laminin‐, fibronectin‐, and matrigel‐coated surfaces in response to FcεRI‐mediated signals , 1993, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[53]  S. Galli,et al.  Regulation of mouse peritoneal mast cell secretory function by stem cell factor, IL-3 or IL-4. , 1993, Journal of immunology.

[54]  D. Metcalfe,et al.  IL-3-dependent mast cells attach to plate-bound vitronectin. Demonstration of augmented proliferation in response to signals transduced via cell surface vitronectin receptors. , 1992, Journal of immunology.

[55]  K. Zsebo,et al.  Induction of differentiation of human mast cells from bone marrow and peripheral blood mononuclear cells by recombinant human stem cell factor/kit-ligand in long-term culture. , 1992, Blood.

[56]  M. Tsai,et al.  The rat c-kit ligand, stem cell factor, induces c-kit receptor- dependent mouse mast cell activation in vivo. Evidence that signaling through the c-kit receptor can induce expression of cellular function , 1992, The Journal of experimental medicine.

[57]  G. Trinchieri,et al.  Human dermal mast cells contain and release tumor necrosis factor alpha, which induces endothelial leukocyte adhesion molecule 1. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[58]  S. Galli,et al.  Mast cells as a source of both preformed and immunologically inducible TNF-α/cachectin , 1990, Nature.

[59]  D. Metcalfe,et al.  Laminin promotes mast cell attachment. , 1989, Journal of immunology.

[60]  W. Paul,et al.  Mast cell lines produce lymphokines in response to cross-linkage of FcεRI or to calcium ionophores , 1989, Nature.

[61]  R. Clark,et al.  Potential roles of fibronectin in cutaneous wound repair. , 1988, Archives of dermatology.

[62]  H P Greisler,et al.  Arterial regeneration over polydioxanone prostheses in the rabbit. , 1987, Archives of surgery.

[63]  S. Bowald,et al.  Arterial regeneration following polyglactin 910 suture mesh grafting. , 1979, Surgery.

[64]  T. Marshall,et al.  Mast cell population density, blood vessel density and histamine content in normal human skin , 1979, The British journal of dermatology.

[65]  A. Hegyeli,et al.  A PARTIALLY BIODEGRADABLE VASCULAR PROSTHESIS , 1972, Transactions - American Society for Artificial Internal Organs.

[66]  G. Bowlin,et al.  In vitro evaluations of innate and acquired immune responses to electrospun polydioxanone-elastin blends. , 2009, Biomaterials.

[67]  David G Simpson,et al.  Suture-reinforced electrospun polydioxanone-elastin small-diameter tubes for use in vascular tissue engineering: a feasibility study. , 2008, Acta biomaterialia.

[68]  David G Simpson,et al.  Electrospinning polydioxanone for biomedical applications. , 2005, Acta biomaterialia.

[69]  S. Toda,et al.  Mast cells and angiogenesis , 2003, Microscopy research and technique.

[70]  S. Galli,et al.  Reversible expansion of primate mast cell populations in vivo by stem cell factor. , 1993, The Journal of clinical investigation.

[71]  S. Galli,et al.  Mast cell cytokines in allergy and inflammation. , 1993, Agents and actions. Supplements.

[72]  P N SAWYER,et al.  The compound prosthetic vascular graft: a pathologic survey. , 1963, Surgery.