Immune modulation as a therapeutic strategy in bone regeneration

Journal of Experimental Orthopaedics

Volumn 2, Issue 1, 2015, Pages 1-10

  Schlundt, Claudia ^a   Schell, Hanna ^a   Goodman, Stuart B ^b   Vunjak Novakovic, Gordana ^c   Duda, Georg N ^a   Schmidt Bleek, Katharina ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b STANFORD UNIVERSITY MEDICAL CENTER   (United States)

^c Stanford University Medical Center Outpatient Center ^*  (United States)

Author keywords

Bone healing; Immune modulation; Macrophages; Osteoimmunology; Regeneration; Revascularization

Indexed keywords

ALKALINE PHOSPHATASE; BONE SIALOPROTEIN; CD163 ANTIGEN; CD68 ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OSTEOCALCIN; TRANSCRIPTION FACTOR RUNX2; VASCULOTROPIN;

ADAPTIVE IMMUNITY; ARTICLE; BONE GRAFT; BONE REGENERATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; FRACTURE HEALING; HUMAN; IMMUNOMODULATION; INNATE IMMUNITY; JOINT PROSTHESIS; MACROPHAGE; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVASCULARIZATION; SYMPOSIUM; T LYMPHOCYTE SUBPOPULATION; TISSUE ENGINEERING;

EID: 84969167088     PISSN: None     EISSN: 21971153     Source Type: Journal    
DOI: 10.1186/s40634-014-0017-6     Document Type: Article

References (49)

1. Einhorn TA, Lane JM (1998) Significant advances have been made in the way surgeons treat fractures. Clin Orthop Relat Res (355 Suppl.):S2–3
2. Schmidt-Bleek K, Petersen A, Dienelt A, Schwarz C, Duda GN (2014) Initiation and early control of tissue regeneration - bone healing as a model system for tissue regeneration. Expert Opin Biol Ther 14:247–259
3. Ai-Aql ZS, Alagl AS, Graves DT, Gerstenfeld LC, Einhorn TA (2008) Molecular mechanisms controlling bone formation during fracture healing and distraction osteogenesis. J Dent Res 87:107–118
4. Kolar P, Schmidt-Bleek K, Schell H, Gaber T, Toben D, Schmidmaier G, Perka C, Buttgereit F, Duda GN (2010) The early fracture hematoma and its potential role in fracture healing. Tissue Eng Part B Rev 16:427–434
5. Lienau J, Schmidt-Bleek K, Peters A, Haschke F, Duda GN, Perka C, Bail HJ, Schutze N, Jakob F, Schell H (2009) Differential regulation of blood vessel formation between standard and delayed bone healing. J Orthop Res 27:1133–1140
6. Mizuno K, Mineo K, Tachibana T, Sumi M, Matsubara T, Hirohata K (1990) The osteogenetic potential of fracture haematoma. Subperiosteal and intramuscular transplantation of the haematoma. J Bone Joint Surg (Br) 72:822–829
7. Park SH, Silva M, Bahk WJ, McKellop H, Lieberman JR (2002) Effect of repeated irrigation and debridement on fracture healing in an animal model. J Orthop Res 20:1197–1204
8. Einhorn TA, Majeska RJ, Rush EB, Levine PM, Horowitz MC (1995) The expression of cytokine activity by fracture callus. J Bone Miner Res 10:1272–1281
9. Arron JR, Choi Y (2000) Bone versus immune system. Nature 408:535–536
10. Bultink IE, Lems WF, Kostense PJ, Dijkmans BA, Voskuyl AE (2005) Prevalence of and risk factors for low bone mineral density and vertebral fractures in patients with systemic lupus erythematosus. Arthritis Rheum 52:2044–2050
11. Schoon EJ, Blok BM, Geerling BJ, Russel MG, Stockbrugger RW, Brummer RJ (2000) Bone mineral density in patients with recently diagnosed inflammatory bowel disease. Gastroenterology 119:1203–1208
12. Spector TD, Hall GM, McCloskey EV, Kanis JA (1993) Risk of vertebral fracture in women with rheumatoid arthritis. BMJ 306:558
13. Reinke S, Geissler S, Taylor WR, Schmidt-Bleek K, Juelke K, Schwachmeyer V, Dahne M, Hartwig T, Akyuz L, Meisel C, Unterwalder N, Singh NB, Reinke P, Haas NP, Volk HD, Duda GN (2013) Terminally Differentiated CD8+ T Cells Negatively Affect Bone Regeneration in Humans. Sci Transl Med 5:177ra136
14. Janeway CA Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216
15. Chazaud B (2014) Macrophages: supportive cells for tissue repair and regeneration. Immunobiology 219:172–178
16. Stein M, Keshav S, Harris N, Gordon S (1992) Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med 176:287–292
17. Chung ES, Chauhan SK, Jin Y, Nakao S, Hafezi-Moghadam A, van Rooijen N, Zhang Q, Chen L, Dana R (2009) Contribution of macrophages to angiogenesis induced by vascular endothelial growth factor receptor-3-specific ligands. Am J Pathol 175:1984–1992
18. Condeelis J, Pollard JW (2006) Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124:263–266
19. Godwin JW, Pinto AR, Rosenthal NA (2013) Macrophages are required for adult salamander limb regeneration. Proc Natl Acad Sci U S A 110:9415–9420
20. van Amerongen MJ, Harmsen MC, van Rooijen N, Petersen AH, van Luyn MJ (2007) Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice. Am J Pathol 170:818–829
21. Krishnamoorthy L (2006) The role of macrophages in human wound healing and their response to a tissue engineered dermal replacement in human chrinic wounds
22. Khallou-Laschet J, Varthaman A, Fornasa G, Compain C, Gaston AT, Clement M, Dussiot M, Levillain O, Graff-Dubois S, Nicoletti A, Caligiuri G (2010) Macrophage plasticity in experimental atherosclerosis. PLoS One 5:e8852
23. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG (2009) Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 29:13435–13444
24. Spiller K, Nassiri S, Witherel CE, Anfang RR, Ng J, Nakazawa KR, Vunjak-Novakovic G (2014) Sequential delivery of immunomodulatory cytokines to facilitate the M1-to-M2 transition of macrophages and enhance vascularization of bone scaffolds. Biomaterials in press
25. Spiller KL, Freytes DO, Vunjak-Novakovic G (2014) Macrophages Modulate Engineered Human Tissues for Enhanced Vascularization and Healing. Annals of biomedical engineering. [Epub ahead of print]
26. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25:677–686
27. Rao AJ, Gibon E, Ma T, Yao Z, Smith RL, Goodman SB (2012) Revision joint replacement, wear particles, and macrophage polarization. Acta Biomater 8:2815–2823
28. Nich C, Takakubo Y, Pajarinen J, Ainola M, Salem A, Sillat T, Rao AJ, Raska M, Tamaki Y, Takagi M, Konttinen YT, Goodman SB, Gallo J (2013) Macrophages-Key cells in the response to wear debris from joint replacements. Journal of biomedical materials research. Part A 101:3033–3045
29. Deshmane SL, Kremlev S, Amini S, Sawaya BE (2009) Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 29:313–326
30. Gibon E, Ma T, Ren PG, Fritton K, Biswal S, Yao Z, Smith L, Goodman SB (2012) Selective inhibition of the MCP-1-CCR2 ligand-receptor axis decreases systemic trafficking of macrophages in the presence of UHMWPE particles. J Orthop Res 30:547–553
31. Gibon E, Yao Z, Rao AJ, Zwingenberger S, Batke B, Valladares R, Smith RL, Biswal S, Gambhir SS, Goodman SB (2012) Effect of a CCR1 receptor antagonist on systemic trafficking of MSCs and polyethylene particle-associated bone loss. Biomaterials 33:3632–3638
32. Keeney M, Waters H, Barcay K, Jiang X, Yao Z, Pajarinen J, Egashira K, Goodman SB, Yang F (2013) Mutant MCP-1 protein delivery from layer-by-layer coatings on orthopedic implants to modulate inflammatory response. Biomaterials 34:10287–10295
33. Yao Z, Keeney M, Lin TH, Pajarinen J, Barcay K, Waters H, Egashira K, Yang F, Goodman S (2013) Mutant monocyte chemoattractant protein 1 protein attenuates migration of and inflammatory cytokine release by macrophages exposed to orthopedic implant wear particles. J Biomed Mater Res Part A 102:3291–3297
34. Roa A, Nich C, Dhulipale LS, Gibon E, Valladeras R, Zwingenberger S, Smith RL, Goodman SB (2013) Local effect of IL-4 delivery on polyethylene particle induced osteolysis in the murine calvarium. J Biomed Mater Res 101:1926–1934
35. Spiller KL, Anfang RR, Spiller KJ, Ng J, Nakazawa KR, Daulton JW, Vunjak-Novakovic G (2014) The role of macrophage phenotype in vascularization of tissue engineering scaffolds. Biomaterials 35:4477–4488
36. de Peppo GM, Vunjak-Novakovic G, Marolt D (2014) Cultivation of human bone-like tissue from pluripotent stem cell-derived osteogenic progenitors in perfusion bioreactors. Methods Mol Biol 1202:173–184
37. Konnecke I, Serra A, El Khassawna T, Schlundt C, Schell H, Hauser A, Ellinghaus A, Volk HD, Radbruch A, Duda GN, Schmidt-Bleek K (2014) T and B cells participate in bone repair by infiltrating the fracture callus in a two-wave fashion. Bone 64:155–165
38. Opal SM (2000) Phylogenetic and functional relationships between coagulation and the innate immune response. Crit Care Med 28:S77–80
39. Whitby DJ, Ferguson MW (1991) Immunohistochemical localization of growth factors in fetal wound healing. Dev Biol 147:207–215
40. Xing Z, Lu C, Hu D, Miclau T 3rd, Marcucio RS (2010) Rejuvenation of the inflammatory system stimulates fracture repair in aged mice. J Orthop Res 28:1000–1006
41. Sjogren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, Backhed F, Ohlsson C (2012) The gut microbiota regulates bone mass in mice. J Bone Miner Res 27:1357–1367
42. Park JE, Barbul A (2004) Understanding the role of immune regulation in wound healing. Am J Surg 187:11S–16S
43. Schaffer M, Barbul A (1998) Lymphocyte function in wound healing and following injury. Br J Surg 85:444–460
44. Pacifici R (2013) Osteoimmunology and its implications for transplantation. Am J Transplant 13:2245–2254
45. Grassi F, Cattini L, Gambari L, Manferdini C, Piacentini A, Gabusi E, Facchini A, Lisignoli G (2013) T cell subsets differently regulate osteogenic differentiation of human mesenchymal stromal cells in vitro. J Tissue Eng Regen Med. [Epub ahead of print]
46. Zaiss MM, Frey B, Hess A, Zwerina J, Luther J, Nimmerjahn F, Engelke K, Kollias G, Hunig T, Schett G, David JP (2010) Regulatory T cells protect from local and systemic bone destruction in arthritis. J Immunol 184:7238–7246
47. van Maurik A, Herber M, Wood KJ, Jones ND (2002) Cutting edge: CD4 + CD25+ alloantigen-specific immunoregulatory cells that can prevent CD8+ T cell-mediated graft rejection: implications for anti-CD154 immunotherapy. J Immunol 169:5401–5404
48. Zaiss MM, Axmann R, Zwerina J, Polzer K, Guckel E, Skapenko A, Schulze-Koops H, Horwood N, Cope A, Schett G (2007) Treg cells suppress osteoclast formation: a new link between the immune system and bone. Arthritis Rheum 56:4104–4112
49. Liu Y, Wang L, Kikuiri T, Akiyama K, Chen C, Xu X, Yang R, Chen W, Wang S, Shi S (2011) Mesenchymal stem cell-based tissue regeneration is governed by recipient T lymphocytes via IFN-gamma and TNF-alpha. Nat Med 17:1594–1601