Abstract
This study evaluates human neutrophil responses to aluminum oxide membranes with different pore sizes (20 nm and 200 nm in diameter) uncoated and pre-coated with serum, collagen I, or fibrinogen. The effect of released neutrophil granule components on the survival of osteoblastic cells (MG63) bound to the alumina membranes has also been evaluated. Without protein coatings the 20 nm pore-size membranes prompt higher reactive oxygen species (ROS) production as assessed by luminol-amplified chemiluminescence than the 200 nm pore-size membranes. Such pore-size depending responses were also found on membranes pre-coated with fibrinogen, but not with collagen or serum were in fact a much lower ROS production was observed. In addition, uncoated and fibrinogen-coated membranes prompt stronger release of the granule enzymes, myeloperoxidase and elastase, than collagen or serum-coated alumina. Equally important, we found that surface-mediated phagocyte activation and the subsequent release of granule components had a significant affect on the adhesion, viability and proliferation of osteoblasts. This stresses the importance of studying not only cell/surface interactions but also cell/cell interactions in wound healing and tissue regeneration processes.
Similar content being viewed by others
References
P. H. WOOLEY, S. NASSER and R. H. FITZGERALD JR., The immune response to implant materials in humans. Clin. Orthop. 326 (1996) 63–70.
A. R. WALPOLE, E. P. BRIGGS, M. KARLSSON, E. PÅLSGÅRD and P. R. WILSHAW, Nano-porous alumina coatings for improved bone implant surfaces. Mat.-wiss. u. Werkstofftech 12(34) (2003) 1064–1068.
E. P. BRIGGS, M. KARLSSON, A. R. WALPOLE, E. PÅLSGÅRD and P. R. WILSHAW, Formation of highly adherent nano porous alumina on Ti based substrates (a novel bone implant coating). J. Mater. Sci. Mater. Med. 15 (2004) 1021–1029.
M. KARLSSON, E. PÅLSGÅRD, P. R. WILSHAW and L. DI SILVIO, Initial in vitro interaction of osteoblasts with nano-porous alumina. Biomaterials 24 (2003) 3039–3046.
L. P. TANG and J. W. EATON, Nature responses to unnature materials: A molecular mechanism for foreign body reactions. Molecular Medicine 5(6) (1999) 351–358.
L. TANG and J. W. EATON, Inflammatory responses to biomaterials. Am. J. Clin. Path. 103 (1995) 466–471.
H. NYGREN, M. BROBERG, C. ERIKSSON, H. SAHLIN and N. YAHYAPOUR, The respiratory burst response of surface-adhering leukocytes. A key to tissue engineering. Colloids and Surfaces B: Biointerfaces 22 (2001) 87–97.
J. M. ANDERSON, Mechanism of inflammation and infection with implanted devices. Cardiovasc Pathol. 2 (1993) 33S–41S.
L. TANG and J. W. EATON, Mechanism of acute inflammatory responses to biomaterials. Cells Mater. 4 (1994) 429–36.
L. TANG, Molecular mechanism of biomaterial-mediated phagocyte responses. in “Biomaterial Engineering and Devices: Human Applications, Fundamental and Vascular and Carrier Applications”, edited by D. L. Wise, J. D. Gresser, D. J. Trantolo, M. V. Cattaneo, K.-U. Lewandrowski, and M. L. Yaszemsky (The Humana Press: Totowa, NJ, 2000) p. 3–14.
M. KARLSSON, A. JOHANSSON, L. TANG and M. BOMAN, Nanoporous aluminium oxide affects neutrophil bahaviour. Microscopy Res. Tech. 63(5) (2004) 259–265.
G. A. DUNN, Contact guidance of cultured tissue cells: a survey of potentially relevant properties of the substratum. in “Cell behaviour” edited by R. Bellairs, A. Curtis and G. Dunn (Cambridge university press, London, 1982) p. 247–281.
T. A. DESAI, Micro- and nanoscale structures for tissue engineering constructs. Med. Eng. Phys. 22 (2000) 595–606.
J. TAN, H. SHEN, K. L. CARTER and W. M. SALTZMAN, Controlling human polymorphonuclear leukocytes motility using microfabrication technology. J. Biomed. Mater. Res. 51 (2000) 694–702.
R. G. FLEMMING, C. J. MURPHY, G. A. ABRAMS, S. L. GOODMAN and P. F. NEALEY, Effects of synthetic micro- and nano-structured surfaces on cell behaviour. Biomaterials 20 (1999) 573–588.
A. CURTIS and C. WILKINSON, Topographical control of cells. Biomaterials 18 (1998) 1573–1583.
P. CLARK, P. CONNOLLY, A. S. G. CURTIS, J. A. T. DOW and C. D. W. WILKINSON, Topographical control of cell behaviour, I. Simple step cues. Development 99 (1987) 439–448.
J. M. COURTNEY, N. M. K. LAMBA, S. SUNDARAM and C. D. FORBES, Biomaterials for blood-contacting applications. Biomaterials 15(10) (1994) 737–744.
J. M. LACKIE, Aspect of the behaviour of neutrophil leucocytes, in “Cell Behaviour” edited by R. Bellairs, A. Curtis, G. Dunn (Cambride university press, Cambridge, 1982) p. 319–348.
N. C. LINDFORS and M. KLOCKARS, Immunoglobuline enhances the bioactive-glass-induced chemiluminesence response of human polymorphonuclear leukocytes. J. Biomed. Mater. Res. 55 (2001) 613–617.
L. TANG and J. W. EATON, Fibrin(ogen) mediates acute inflammatory responses to biomaterials. J. Exp. Med. 178 (1993) 2147–2156.
L. HÅKANSSON and P. VENGE, The influence of serum on random migration and chemotaxis of polymorphonuclear leucocytes: Methological evaluation using sera from infection-prone patients and normals. Scandinavian J. Immunol. 11 (1980) 271–282.
C. DAHLGREN, P. FOLLIN, A. JOHANSSON, R. LOCK, H. LUNDQVIST and Å. WALAN, Chemiluminescence as means of following the function of phagocytic cells. in “Trends in photochemistry and photobiology” edited by A. Kumar (Research trends, 1991) p. 427–443.
G. D. VIRCA, G. METZ and H. P. SCHNEBLI, Similarities between human and rat leukocyte elastase and cathepsin G. Eur. J. Biochem. 144 (1984) 1–9.
G. R. NAKAYAMA, M. C. CATON, M. P. NOVA and Z. PARANDOOSH, Assessment of the alamar blue assay for cellular growth and viability in vitro. J. Imm. Meth. 204 (1997) 205–208.
R. E. MARCHANT, Cell adhesion and interaction with biomaterials. J. Adhesion. 20 (1986) 211–225.
P. M. HENSON, Mechanism of exocytosis in phagocytic inflammatory cells. in Annual meeting of the american association of pathologists (FASEB). (Anahein, California, 1980).
I. V. YANNAS, Natural materials. in “Biomaterials Science: An Introduction to Materials in Medicine” edited by B. D. Ratner, A. S. Hoffman, F. J. Schoen and J. E. Lemons (Academic Press, San Diego, 1996) p. 84–92.
L. TANG and J. W. EATON, Molecular determinants of aucte inflammatory responses to biomaterials. in “Tissue engineering of prosthetic vascular grafts” edited by P. P. Zilla and H. P. Greisler (RG Landes Company, 1999) p. 207–218.
Y. TAKAMI, S. YAMANE, K. MAKINOUCHI, G. OTSUKA, J. GLUECK, R. BENKOWSKI and Y. NOSE, Protein adsorption onto ceramic surfaces. J. Biomed. Mater. Res. 40 (1998) 24–30.
S. J. WHICHER and J. L. BRASH, Platelet-foreign surface interactions: Release of granule constituents from adherent platelets. J. Biomed. Mater. Res. 12 (1978) 181–201.
C. R. JENNEY and J. M. ANDERSON, Adsorbed serum proteins responsible for surface dependent human macrophage behaviour. J. Biomed. Mater. Res. 49 (2000) 435–447.
C. LENTNER, Blood-Plasma proteins. in “Geigy Scentific Tables 3” edited by C. Lentner (CIBA-GEIGY, Basle, 1984) p. 140–141.
E. DECLEVA, P. DRI, R. MENEGAZZI, S. BUSETTO and R. CRAMER, Evidence that TNF-induced respiratory burst of adherent PMN is mediated by integrin alpha(L)beta(2). J. Leukoc. Biol. 72(4) (2002) 718–26.
J. C. MONBOISSE, R. GARNOTEL, A. RANDOUX, J. DUFER and J. BOREL, Adhesion of human neeutrophils to and activation by type I collagen involving a β2 integrin. J. Leukoc. Biol. 50 (1991) 373–380.
M. BERGKVIST, J. CARLSSON and S. OSCARSSON, Surface dependent conformations of human plasma fibronectin adsorbed to silica, mica and hydrophobic surfaces, studied with Atomic Force Microscopy. J. Biomed. Mater. Res. 64A (2003) 349–356.
J. C. MONBOISSE, G. BELLON, A. RANDOUX, J. DUFER and J. BOREL, Activation of human neutrophils by type I collagen. Biochem. J. 270 (1990) 459–462.
J. C. MONBOISSE, G. BELLON, J. DUFER, A. RANDOUX and J. BOREL, Collagen activates superoxide anion production by human polymorphonuclear neutrophils. Biochem. J. 246 (1987) 599–603.
J. TRAVIS, J. POTEMPA, N. BANGALORE and A. KURDOWSKA, Multiple functions of neutrophil proteases and their inhibitor complexes. in “Current topics in rehabilitation: Biochemistry of pulmonary emphysema” edited by Grassi et al. (Springer verlag, London, 1992) p. 71–79.
J. TRAVIS, Structure, function and control of neutrophil proteinases. Am. J. Med. 84 (1988) 37–42.
P. M. HENSON, The immunologic release of constituents from neutrophil leukocytes, Mechanism of release during phagocytosis, and adherence to nonphagocytosable materials. J. Immunol. (1971) 1547–1557.
A. M. MOURSI, C. H. DAMSKY, J. LULL, D. ZIMMERMAN, S. B. DOTY, S. AOTA and R. K. GLOBUS, Fibronectin regulates calvarial osteoblast differentiation. J. Cell. Sci. 109 (1996) 1369–1380.
A. M. MOURSI, R. K. GLOBUS and C. H. DAMSKY, Interactions between integrin receptors and fibronectin are required for calvarial osteoblast differentiation in vitro. J. Cell. Sci. 110 (1997) 2187–2196.
R. K. GLOBUS, S. B. DOTY, J. LULL, E. HOLMUHAMEDOV, M. J. HUMPHRIES and C. H. DAMSKY, Fibronectin is a survival factor for differentiated osteoblasts. J. Cell. Sci. 111 (1998) 1385–1393.
A. G. ANDRIANARIVO, J. A. ROBINSON, K. G. MANN and R. P. TRACY, Growth on type I collagen promotes expression of the osteoblastic phenotype in human osteosarcoma MG-63 Cells. J. Cell. Phys. 153 (1992) 256–265.
L. MASI, A. FRANCHI, M. SANTUCCI, D. DANIELLI, L. ARGANINI, V. GIANNONE, L. FORMIGLI, S. BENVENUTI, A. TANINI, F. BEGHE, M. MIAN and M. L. BRANDI, Adhesion growth and matrix production by osteoblasts on collagen substrata. Calcified Tissue Int. 51 (1992) 202–212.
D. ROOS and C. C. WINTERBOURN, Lethal weapons. Science 296 (2002) 669–671.
B. FARTASH, M. HULTIN, A. GUSTAFSSON, B. ÅSMAN and K. ARVIDSON, Markers of inflammation in crevicular fluid from peri-implant mucosa surrounding single crystal sapphire implants. Clin. Oral. Impl. Res. 8 (1997) 32–38.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Karlsson, M., Tang, L. Surface morphology and adsorbed proteins affect phagocyte responses to nano-porous alumina. J Mater Sci: Mater Med 17, 1101–1111 (2006). https://doi.org/10.1007/s10856-006-0537-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10856-006-0537-4