Skip to main content

Advertisement

Log in

Circulating blood monocytes traffic to and participate in the periprosthetic tissue inflammation

  • Original Research Paper
  • Published:
Inflammation Research Aims and scope Submit manuscript

Abstract

Objective

To examine the trafficking of human circulating blood monocytes and their influence on the inflammation of periprosthetic tissues using a novel mouse–human chimera model.

Methods

Periprosthetic tissue and bone chips from patients with aseptic prosthetic loosening were implanted into the muscles of immune-deficient SCID mice depleted of host macrophages by periodic intraperitoneal injection of anti-asialo GM1 rabbit sera (ASGM1). Autologous patient peripheral blood monocytes (PBMCs) were labeled with PKH2 fluorescent dye and injected intraperitoneally into the implanted animals. Mice were sacrificed 14 days after PBMC transfusion for molecular and histological analyses.

Results

Patient periprosthetic tissues were well tolerated in SCID mice and preserved a high level of viability. Cell trafficking studies revealed the accumulation of fluorescent PBMC within the xenografts, with total cell counts in the xenografts significantly increased following the systemic PBMC infusion. PBMC infusion also promoted the expression of IL-1, IL-6, TNFα, and RANK within the periprosthetic tissue.

Conclusion

Systemic PBMC migrated to the implanted periprosthetic tissues and contributed to the local inflammation. The data provide evidence that circulating blood monocytes may play a role in pathologic process during aseptic loosening of total joint replacement.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Ingham E, Fisher J. The role of macrophages in osteolysis of total joint replacement. Biomaterials. 2005;26:1271–86.

    Article  CAS  PubMed  Google Scholar 

  2. Bauer TW, Schils J. The pathology of total joint arthroplasty. II. Mechanisms of implant failure. Skeletal Radiol. 1999;28:483–97.

    Article  CAS  PubMed  Google Scholar 

  3. Santavirta S, Konttinen YT, Bergroth V, Eskola A, Tallroth K, Lindholm TS. Aggressive granulomatous lesions associated with hip arthroplasty Immunopathological studies. J Bone Joint Surg Am. 1990;72:252–8.

    CAS  PubMed  Google Scholar 

  4. Kadoya Y, Revell PA, Kobayashi A, Al-Saffar N, Scott G, Freeman MA. Wear particulate species and bone loss in failed total joint arthroplasties. Clin Orthop Relat Res. 1997;340:118–29.

    Article  PubMed  Google Scholar 

  5. Shanbhag AS, Jacobs JJ, Glant TT, Gilbert JL, Black J, Galante JO. Composition and morphology of wear debris in failed uncemented total hip replacement. J Bone Joint Surg Br. 1994;76:60–7.

    CAS  PubMed  Google Scholar 

  6. Fang HW, Ho YC, Yang CB, Liu HL, Ho FY, Lu YC, et al. Preparation of UHMWPE particles and establishment of inverted macrophage cell model to investigate wear particles induced bioactivites. J Biochem Biophys Methods. 2006;68:175–87.

    Article  CAS  PubMed  Google Scholar 

  7. Goldring SR, Schiller AL, Roelke M, Rourke CM, O’Neil DA, Harris WH. The synovial-like membrane at the bone-cement interface in loose total hip replacements and its proposed role in bone lysis. J Bone Joint Surg Am. 1983;65:575–84.

    CAS  PubMed  Google Scholar 

  8. Santavirta S, Ceponis A, Solovieva SA, Hurri H, Jin J, Takagi M, et al. Periprosthetic microvasculature in loosening of total hip replacement. Arch Orthop Trauma Surg. 1996;115:286–9.

    Article  CAS  PubMed  Google Scholar 

  9. Anderson JM, Miller KM. Biomaterial biocompatibility and the macrophage. Biomaterials. 1984;5:5–10.

    Article  CAS  PubMed  Google Scholar 

  10. Laquerriere P, Grandjean-Laquerriere A, Jallot E, Balossier G, Frayssinet P, Guenounou M. Importance of hydroxyapatite particles characteristics on cytokines production by human monocytes in vitro. Biomaterials. 2003;24:2739–47.

    Article  CAS  PubMed  Google Scholar 

  11. Yang SY, Nasser S, Markel DC, Robbins PD, Wooley PH. Human periprosthetic tissues implanted in severe combined immunodeficient mice respond to gene transfer of a cytokine inhibitor. J Bone Joint Surg Am. 2005;87:1088–97.

    Article  PubMed  Google Scholar 

  12. Geiler T, Kriegsmann J, Keyszer GM, Gay RE, Gay S. A new model for rheumatoid arthritis generated by engraftment of rheumatoid synovial tissue and normal human cartilage into SCID mice. Arthritis Rheum. 1994;37:1664–71.

    Article  CAS  PubMed  Google Scholar 

  13. Slezak SE, Horan PK. Fluorescent in vivo tracking of hematopoietic cells. Part I. Technical considerations. Blood. 1989;74:2172–7.

    CAS  PubMed  Google Scholar 

  14. Ren W, Yang SY, Wooley PH. A novel murine model of orthopaedic wear-debris associated osteolysis. Scand J Rheumatol. 2004;33:349–57.

    Article  CAS  PubMed  Google Scholar 

  15. Yang SY, Wu B, Mayton L, Mukherjee P, Robbins PD, Evans CH, et al. Protective effects of IL-1Ra or vIL-10 gene transfer on a murine model of wear debris-induced osteolysis. Gene Ther. 2004;11:483–91.

    Article  CAS  PubMed  Google Scholar 

  16. Yang S, Wu B, Mayton L, Evans CH, Robbins PD, Wooley PH. IL-1Ra and vIL-10 gene transfer using retroviral vectors ameliorates particle-associated inflammation in the murine air pouch model. Inflamm Res. 2002;51:342–50.

    Article  CAS  PubMed  Google Scholar 

  17. Harris WH. Wear and periprosthetic osteolysis: the problem. Clin Orthop Relat Res. 2001;393:66–70.

    Article  PubMed  Google Scholar 

  18. van Raay JJ, Rozing PM, Eulderink F. Tissue response to the failed Gerard double-cup. Histologic analysis of 40 uncemented hip arthroplasties. Acta Orthop Scand. 1993;64:268–72.

    Article  PubMed  Google Scholar 

  19. Bosma GC, Custer RP, Bosma MJ. A severe combined immunodeficiency mutation in the mouse. Nature. 1983;301:527–30.

    Article  CAS  PubMed  Google Scholar 

  20. Rollins BJ. Monocyte chemoattractant protein 1: a potential regulator of monocyte recruitment in inflammatory disease. Mol Med Today. 1996;2:198–204.

    Article  CAS  PubMed  Google Scholar 

  21. Sakai K, Matsuno H, Morita I, Nezuka T, Tsuji H, Shirai T, et al. Potential withdrawal of rheumatoid synovium by the induction of apoptosis using a novel in vivo model of rheumatoid arthritis. Arthritis Rheum. 1998;41:1251–7.

    Article  CAS  PubMed  Google Scholar 

  22. Koulouvaris P, Ly K, Ivashkiv LB, Bostrom MP, Nestor BJ, Sculco TP, et al. Expression profiling reveals alternative macrophage activation and impaired osteogenesis in periprosthetic osteolysis. J Orthop Res. 2008;26:106–16.

    Article  CAS  PubMed  Google Scholar 

  23. Ishiguro N, Kojima T, Ito T, Saga S, Anma H, Kurokouchi K, et al. Macrophage activation and migration in interface tissue around loosening total hip arthroplasty components. J Biomed Mater Res. 1997;35:399–406.

    Article  CAS  PubMed  Google Scholar 

  24. Askenasy N, Farkas DL. Optical imaging of PKH-labeled hematopoietic cells in recipient bone marrow in vivo. Stem Cells. 2002;20:501–13.

    Article  PubMed  Google Scholar 

  25. Horan PK, Slezak SE. Stable cell membrane labelling. Nature. 1989;340:167–8.

    Article  CAS  PubMed  Google Scholar 

  26. Murphy WJ, Kumar V, Bennett M. Rejection of bone marrow allografts by mice with severe combined immune deficiency (SCID). Evidence that natural killer cells can mediate the specificity of marrow graft rejection. J Exp Med. 1987;165:1212–7.

    Article  CAS  PubMed  Google Scholar 

  27. Sandhu J, Shpitz B, Gallinger S, Hozumi N. Human primary immune response in SCID mice engrafted with human peripheral blood lymphocytes. J Immunol. 1994;152:3806–13.

    CAS  PubMed  Google Scholar 

  28. Shpitz B, Fernandes BJ, Mullen JB, Roder JC, Gallinger S. Improved engraftment of human tumours in SCID mice pretreated with radiation and anti-asialo GM1. Anticancer Res. 1994;14:1927–34.

    CAS  PubMed  Google Scholar 

  29. Shpitz B, Chambers CA, Singhal AB, Hozumi N, Fernandes BJ, Roifman CM, et al. High level functional engraftment of severe combined immunodeficient mice with human peripheral blood lymphocytes following pretreatment with radiation and anti-asialo GM1. J Immunol Methods. 1994;169:1–15.

    Article  CAS  PubMed  Google Scholar 

  30. Yoshino H, Ueda T, Kawahata M, Kobayashi K, Ebihara Y, Manabe A, et al. Natural killer cell depletion by anti-asialo GM1 antiserum treatment enhances human hematopoietic stem cell engraftment in NOD/Shi-scid mice. Bone Marrow Transpl. 2000;26:1211–6.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Ms. Zheng Song, Bin Wu, and Li Mao for their excellent technical assistance. This work was supported by research grants from Orthopaedic Research and Education Foundation (OREF, S.-Y.Y.), NIH (5R03AR054929-02, S-Y.Y.), and Veteran Administration (Merit Award, P.H.W.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shang-You Yang.

Additional information

Responsible Editor: A. Bauhofer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, K., Jia, TH., McQueen, D. et al. Circulating blood monocytes traffic to and participate in the periprosthetic tissue inflammation. Inflamm. Res. 58, 837–844 (2009). https://doi.org/10.1007/s00011-009-0051-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00011-009-0051-5

Keywords

Navigation