Signal One and Two Blockade Are Both Critical for Non-Myeloablative Murine HSCT across a Major Histocompatibility Complex Barrier

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Langford Smith, Kia J ^a   Sandiford, Zara ^a   Langford Smith, Alex ^a   Wilkinson, Fiona L ^a   Jones, Simon A ^b   Wraith, J Ed ^b   Wynn, Robert F ^c   Bigger, Brian W ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b ST MARY S HOSPITAL   (United Kingdom)

^c ROYAL MANCHESTER CHILDREN S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BUSULFAN; CD4 ANTIBODY; CD40 LIGAND MONOCLONAL ANTIBODY; CD8 ANTIBODY; CELL ANTIBODY; GRANULOCYTE COLONY STIMULATING FACTOR; STROMAL CELL DERIVED FACTOR 1ALPHA; UNCLASSIFIED DRUG;

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHIMERA; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; ENGRAFTMENT; GRAFT REJECTION; IN VIVO STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MOUSE; MYELOABLATIVE CONDITIONING; NONHUMAN; NONMYELOABLATIVE CONDITIONING; REDUCED INTENSITY CONDITIONING; STEM CELL NICHE; WHOLE BODY RADIATION;

ANIMALS; BUSULFAN; GRANULOCYTE COLONY-STIMULATING FACTOR; HEMATOPOIETIC STEM CELL TRANSPLANTATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MICE; MICE, INBRED C57BL; TRANSPLANTATION CHIMERA; TRANSPLANTATION, HOMOLOGOUS;

EID: 84885797628     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077632     Document Type: Article

References (52)

1. Wynn RF, Wraith JE, Mercer J, O'Meara A, Tylee K, et al. (2009) Improved metabolic correction in patients with lysosomal storage disease treated with hematopoietic stem cell transplant compared with enzyme replacement therapy. J Pediatr 154: 609-611. doi:10.1016/j.jpeds.2008.11.005. PubMed: 19324223.
2. Wynn R, (2011) Stem cell transplantation in inherited metabolic disorders. Hematol Am Soc Hematol Education Program, 2011(2011): 285-291 PubMed: 22160047.
3. Chinen J, Buckley RH, (2010) Transplantation immunology: solid organ and bone marrow. J Allergy Clin Immunol 125: S324-S335. doi:10.1016/j.jaci.2009.11.014. PubMed: 20176267.
4. Seung E, Mordes JP, Rossini AA, Greiner DL, (2003) Hematopoietic chimerism and central tolerance created by peripheral-tolerance induction without myeloablative conditioning. J Clin Invest 112: 795-808. doi:10.1172/JCI200318599. PubMed: 12952928.
5. Graca L, Daley S, Fairchild PJ, Cobbold SP, Waldmann H, (2006) Co-receptor and co-stimulation blockade for mixed chimerism and tolerance without myelosuppressive conditioning. BMC Immunol 7: 9. doi:10.1186/1471-2172-7-9. PubMed: 16638128.
6. Daley SR, Cobbold SP, Waldmann H, (2008) Fc-disabled anti-mouse CD40L antibodies retain efficacy in promoting transplantation tolerance. Am J Transplant Off J Am Soc Transplant American Society Of Transplant Surgeons 8: 2265-2271. doi:10.1111/j.1600-6143.2008.02382.x. PubMed: 18782294.
7. Wekerle T, Nikolic B, Pearson DA, Swenson KG, Sykes M, (2002) Minimal conditioning required in a murine model of T cell depletion, thymic irradiation and high-dose bone marrow transplantation for the induction of mixed chimerism and tolerance. Transpl Int Off J European Society For Organ Transplant 15: 248-253. doi:10.1111/j.1432-2277.2002.tb00160.x.
8. Westerhuis G, Maas WG, Willemze R, Toes RE, Fibbe WE, (2005) Long-term mixed chimerism after immunologic conditioning and MHC-mismatched stem-cell transplantation is dependent on NK-cell tolerance. Blood 106: 2215-2220. doi:10.1182/blood-2005-04-1391. PubMed: 15928035.
9. Blaha P, Bigenzahn S, Koporc Z, Sykes M, Muehlbacher F, et al. (2005) Short-term immunosuppression facilitates induction of mixed chimerism and tolerance after bone marrow transplantation without cytoreductive conditioning. Transplantation 80: 237-243. doi:10.1097/01.TP.0000164510.25625.70. PubMed: 16041269.
10. Wekerle T, Kurtz J, Ito H, Ronquillo JV, Dong V, et al. (2000) Allogeneic bone marrow transplantation with co-stimulatory blockade induces macrochimerism and tolerance without cytoreductive host treatment. Nat Med 6: 464-469. doi:10.1038/74731. PubMed: 10742157.
11. Graca L, Le Moine A, Lin CY, Fairchild PJ, Cobbold SP, et al. (2004) Donor-specific transplantation tolerance: the paradoxical behavior of CD4+CD25+ T cells. Proc Natl Acad Sci U S A 101: 10122-10126. doi:10.1073/pnas.0400084101. PubMed: 15218097.
12. Westerhof GR, Ploemacher RE, Boudewijn A, Blokland I, Dillingh JH, et al. (2000) Comparison of different busulfan analogues for depletion of hematopoietic stem cells and promotion of donor-type chimerism in murine bone marrow transplant recipients. Cancer Res 60: 5470-5478. PubMed: 11034090.
13. Yeager AM, Shinn C, Pardoll DM, (1991) Lymphoid reconstitution after transplantation of congenic hematopoietic cells in busulfan-treated mice. Blood 78: 3312-3316. PubMed: 1683798.
14. Dumont FJ, Su Q, (1996) Mechanism of action of the immunosuppressant rapamycin. Life Sci 58: 373-395. PubMed: 8594303.
15. Luo B, Chan WF, Shapiro AM, Anderson CC, (2007) Non-myeloablative mixed chimerism approaches and tolerance, a split decision. Eur J Immunol 37: 1233-1242. doi:10.1002/eji.200636938. PubMed: 17390394.
16. Anam K, Black AT, Hale DA, (2006) Low dose busulfan facilitates chimerism and tolerance in a murine model. Transpl Immunol 15: 199-204. doi:10.1016/j.trim.2005.09.009. PubMed: 16431286.
17. Fehr T, Takeuchi Y, Kurtz J, Wekerle T, Sykes M, (2005) Early regulation of CD8 T cell alloreactivity by CD4+CD25- T cells in recipients of anti-CD154 antibody and allogeneic BMT is followed by rapid peripheral deletion of donor-reactive CD8+ T cells, precluding a role for sustained regulation. Eur J Immunol 35: 2679-2690. doi:10.1002/eji.200526190. PubMed: 16082727.
18. Lucas CL, Workman CJ, Beyaz S, Locascio S, Zhao G, et al. (2011) LAG-3, TGF-{beta}, and cell-intrinsic PD-1 inhibitory pathways contribute to CD8 but not CD4 T-cell tolerance induced by allogeneic BMT with anti-CD40L. Blood 117: 5532-5540. doi:10.1182/blood-2010-11-318675. PubMed: 21422469.
19. Bigenzahn S, Blaha P, Koporc Z, Pree I, Selzer E, et al. (2005) The role of non-deletional tolerance mechanisms in a murine model of mixed chimerism with costimulation blockade. Am J Transplant Off J Am Soc Transplant American Society Of Transplant Surgeons 5: 1237-1247. doi:10.1111/j.1600-6143.2005.00862.x.
20. Nierlich PN, Klaus C, Bigenzahn S, Pilat N, Koporc Z, et al. (2010) The role of natural killer T cells in costimulation blockade-based mixed chimerism. Transpl Int Off J European Society For Organ Transplant 23: 1179-1189. doi:10.1111/j.1432-2277.2010.01120.x. PubMed: 20536788.
21. Taylor PA, Lees CJ, Waldmann H, Noelle RJ, Blazar BR, (2001) Requirements for the promotion of allogeneic engraftment by anti-CD154 (anti-CD40L) monoclonal antibody under nonmyeloablative conditions. Blood 98: 467-474. doi:10.1182/blood.V98.2.467. PubMed: 11435318.
22. Takeuchi Y, Ito H, Kurtz J, Wekerle T, Ho L, et al. (2004) Earlier low-dose TBI or DST overcomes CD8+ T-cell-mediated alloresistance to allogeneic marrow in recipients of anti-CD40L. Am J Transplant Off J Am Soc Transplant American Society Of Transplant Surgeons 4: 31-40. doi:10.1111/j.1600-6135.2004.00723.x. PubMed: 14678032.
23. Quesenberry PJ, Zhong S, Wang H, Stewart M, (2001) Allogeneic chimerism with low-dose irradiation, antigen presensitization, and costimulator blockade in H-2 mismatched mice. Blood 97: 557-564. doi:10.1182/blood.V97.2.557. PubMed: 11154237.
24. Yamazaki M, Pearson T, Brehm MA, Miller DM, Mangada JA, et al. (2007) Different mechanisms control peripheral and central tolerance in hematopoietic chimeric mice. Am J Transplant Off J Am Soc Transplant American Society Of Transplant Surgeons 7: 1710-1721. doi:10.1111/j.1600-6143.2007.01839.x. PubMed: 17564635.
25. Singhal S, Powles R, Treleaven J, Kulkarni S, Sirohi B, et al. (2000) A low CD34+ cell dose results in higher mortality and poorer survival after blood or marrow stem cell transplantation from HLA-identical siblings: should 2 x 10(6) CD34+ cells/kg be considered the minimum threshold? Bone Marrow Transplant 26: 489-496. doi:10.1038/sj.bmt.1702542. PubMed: 11019837.
26. Metzler B, Gfeller P, Wieczorek G, Katopodis A, (2008) Differential promotion of hematopoietic chimerism and inhibition of alloreactive T cell proliferation by combinations of anti-CD40Ligand, anti-LFA-1, everolimus, and deoxyspergualin. Transpl Immunol 20: 106-112. doi:10.1016/j.trim.2008.07.002. PubMed: 18675355.
27. Czechowicz A, Kraft D, Weissman IL, Bhattacharya D, (2007) Efficient transplantation via antibody-based clearance of hematopoietic stem cell niches. Science 318: 1296-1299. doi:10.1126/science.1149726. PubMed: 18033883.
28. Mardiney M 3rd, Malech HL, (1996) Enhanced engraftment of hematopoietic progenitor cells in mice treated with granulocyte colony-stimulating factor before low-dose irradiation: implications for gene therapy. Blood 87: 4049-4056. PubMed: 8639760.
29. Wright DE, Bowman EP, Wagers AJ, Butcher EC, Weissman IL, (2002) Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J Exp Med 195: 1145-1154. doi:10.1084/jem.20011284. PubMed: 11994419.
30. Jopling C, Rosendaal M, (2001) A cautionary tale: how to delete mouse haemopoietic stem cells with busulphan. Br J Haematol 113: 970-974. doi:10.1046/j.1365-2141.2001.02825.x. PubMed: 11442491.
31. Wilkinson FL, Sergijenko A, Langford-Smith KJ, Malinowska M, Wynn R, et al. (2013) Busulfan conditioning enhances engraftment of hematopoietic donor-derived cells in the brain compared to irradiation. Molecular therapy: the journal of the American Society of Gene Therapy: In press.
32. de Haan G, Nijhof W, Van Zant G, (1997) Mouse strain-dependent changes in frequency and proliferation of hematopoietic stem cells during aging: correlation between lifespan and cycling activity. Blood 89: 1543-1550. PubMed: 9057635.
33. Davies JD, Cobbold SP, Waldmann H, (1997) Strain variation in susceptibility to monoclonal antibody-induced transplantation tolerance. Transplantation 63: 1570-1573. doi:10.1097/00007890-199706150-00005. PubMed: 9197347.
34. Qin SX, Wise M, Cobbold SP, Leong L, Kong YC, et al. (1990) Induction of tolerance in peripheral T cells with monoclonal antibodies. Eur J Immunol 20: 2737-2745. doi:10.1002/eji.1830201231. PubMed: 1702726.
35. Graca L, Thompson S, Lin CY, Adams E, Cobbold SP, et al. (2002) Both CD4(+)CD25(+) and CD4(+)CD25(-) regulatory cells mediate dominant transplantation tolerance. J Immunol 168: 5558-5565. PubMed: 12023351.
36. Hsieh MM, Langemeijer S, Wynter A, Phang OA, Kang EM, et al. (2007) Low-dose parenteral busulfan provides an extended window for the infusion of hematopoietic stem cells in murine hosts. Exp Hematol 35: 1415-1420. doi:10.1016/j.exphem.2007.05.009. PubMed: 17618036.
37. Ashizuka S, Peranteau WH, Hayashi S, Flake AW, (2006) Busulfan-conditioned bone marrow transplantation results in high-level allogeneic chimerism in mice made tolerant by in utero hematopoietic cell transplantation. Exp Hematol 34: 359-368. doi:10.1016/j.exphem.2005.11.011. PubMed: 16543070.
38. Meng A, Wang Y, Brown SA, Van Zant G, Zhou D, (2003) Ionizing radiation and busulfan inhibit murine bone marrow cell hematopoietic function via apoptosis-dependent and-independent mechanisms. Exp Hematol 31: 1348-1356. doi:10.1016/j.exphem.2003.08.014. PubMed: 14662344.
39. Adams AB, Durham MM, Kean L, Shirasugi N, Ha J, et al. (2001) Costimulation blockade, busulfan, and bone marrow promote titratable macrochimerism, induce transplantation tolerance, and correct genetic hemoglobinopathies with minimal myelosuppression. J Immunol 167: 1103-1111. PubMed: 11441122.
40. Honey K, Cobbold SP, Waldmann H, (1999) CD40 ligand blockade induces CD4+ T cell tolerance and linked suppression. J Immunol 163: 4805-4810. PubMed: 10528180.
41. Ito H, Kurtz J, Shaffer J, Sykes M, (2001) CD4 T cell-mediated alloresistance to fully MHC-mismatched allogeneic bone marrow engraftment is dependent on CD40-CD40 ligand interactions, and lasting T cell tolerance is induced by bone marrow transplantation with initial blockade of this pathway. J Immunol 166: 2970-2981. PubMed: 11207246.
42. Dominici M, Rasini V, Bussolari R, Chen X, Hofmann TJ, et al. (2009) Restoration and reversible expansion of the osteoblastic hematopoietic stem cell niche after marrow radioablation. Blood 114: 2333-2343. doi:10.1182/blood-2008-10-183459. PubMed: 19433859.
43. Cui J, Wahl RL, Shen T, Fisher SJ, Recker E, et al. (1999) Bone marrow cell trafficking following intravenous administration. Br J Haematol 107: 895-902. doi:10.1046/j.1365-2141.1999.01779.x. PubMed: 10606901.
44. Pree I, Wekerle T, (2006) New approaches to prevent transplant rejection: Co-stimulation blockers anti-CD40L and CTLA4Ig. Drug Discov Today Ther Strateg 3: 41-47. doi:10.1016/j.ddstr.2006.02.002.
45. Gilson CR, Milas Z, Gangappa S, Hollenbaugh D, Pearson TC, et al. (2009) Anti-CD40 monoclonal antibody synergizes with CTLA4-Ig in promoting long-term graft survival in murine models of transplantation. J Immunol 183: 1625-1635. doi:10.4049/jimmunol.0900339. PubMed: 19592649.
46. Baskiewicz-Masiuk M, Grymula K, Pius E, Halasa M, Dziedziejko V, et al. (2009) An optimization of protocol for mixed chimerism induction in mice model. Folia histochemica et cytobiologica/ Polish Academy of Sciences 47. Polish Histochemical and Cytochemical Society. pp. pp. 395-400.
47. Ferrer IR, Araki K, Ford ML, (2011) Paradoxical aspects of rapamycin immunobiology in transplantation. Am J Transplant Off J Am Soc Transplant American Society Of Transplant Surgeons 11: 654-659. doi:10.1111/j.1600-6143.2011.03473.x. PubMed: 21446969.
48. Moreland LW, Alten R, Van den Bosch F, Appelboom T, Leon M, et al. (2002) Costimulatory blockade in patients with rheumatoid arthritis: a pilot, dose-finding, double-blind, placebo-controlled clinical trial evaluating CTLA-4Ig and LEA29Y eighty-five days after the first infusion. Arthritis Rheum 46: 1470-1479. doi:10.1002/art.10294. PubMed: 12115176.
49. Wilkinson FL, Sergijenko A, Langford-Smith KJ, Malinowska M, Wynn RF, et al. (2013) Busulfan conditioning enhances engraftment of hematopoietic donor-derived cells in the brain compared with irradiation. Molecular Therapy J American Society Of Gene Therapy 21: 868-876. doi:10.1038/mt.2013.29. PubMed: 23423338.
50. Sergijenko A, Langford-Smith A, Liao A, Pickford CE, McDermott J, et al. (In press). yeloid/microglial driven autologous hematopoietic stem cell gene therapy corrects a neuronopathic lysosomal disease. Molecular therapy: the journal of The American Society of Gene Therapy.
51. Langford-Smith A, Wilkinson FL, Langford-Smith KJ, Holley RJ, Sergijenko A, et al. (2012) Hematopoietic stem cell and gene therapy corrects primary neuropathology and behavior in mucopolysaccharidosis IIIA mice. Molecular Therapy J American Society Of Gene Therapy 20: 1610-1621. doi:10.1038/mt.2012.82. PubMed: 22547151.
52. Bigger BW, Siapati EK, Mistry A, Waddington SN, Nivsarkar MS, et al. (2006) Permanent partial phenotypic correction and tolerance in a mouse model of hemophilia B by stem cell gene delivery of human factor IX. Gene Therapy 13: 117-126. doi:10.1038/sj.gt.3302638. PubMed: 16163377.