Characterization of Regulatory Dendritic Cells That Mitigate Acute Graft-versus-Host Disease in Older Mice Following Allogeneic Bone Marrow Transplantation

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Scroggins, Sabrina M ^a,b   Olivier, Alicia K ^b   Meyerholz, David K ^b   Schlueter, Annette J ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 6; MEMBRANE RECEPTOR; PAIRED IMMUNOGLOBULIN LIKE RECEPTOR B; PROGRAMMED DEATH 1 LIGAND 1; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CD274 PROTEIN, MOUSE; CYTOKINE; IMMUNOGLOBULIN RECEPTOR; PIRB PROTEIN, MOUSE;

ACUTE GRAFT VERSUS HOST DISEASE; ADOPTIVE TRANSFER; ALLOGENIC BONE MARROW TRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE MODEL; GRAFT SURVIVAL; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; REGULATORY DENDRITIC CELL; SURVIVAL RATE; ACUTE DISEASE; AGING; ALLOTRANSPLANTATION; ANIMAL; BIOSYNTHESIS; BONE MARROW TRANSPLANTATION; GENE EXPRESSION REGULATION; GRAFT VS HOST DISEASE; HUMAN; IMMUNOLOGY; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; TIME;

ACUTE DISEASE; ADOPTIVE TRANSFER; AGING; ANIMALS; ANTIGENS, CD274; BONE MARROW TRANSPLANTATION; CYTOKINES; DENDRITIC CELLS; GENE EXPRESSION REGULATION; GRAFT VS HOST DISEASE; HUMANS; IMMUNE TOLERANCE; MICE; PHENOTYPE; RECEPTORS, IMMUNOLOGIC; TIME FACTORS; TRANSPLANTATION, HOMOLOGOUS;

EID: 84883797577     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075158     Document Type: Article

References (56)

1. Johnston L, (2008) Acute graft-versus-host disease: differing risk with differing graft sources and conditioning intensity. Best Pract Res Clin Haematol 21: 177-192. doi:10.1016/j.beha.2008.02.006. PubMed: 18503985.
2. Pasquini MC, (2008) Impact of graft-versus-host disease on survival. Best Pract Res Clin Haematol 21: 193-204. doi:10.1016/j.beha.2008.02.011. PubMed: 18503986.
3. Aschan J, Ringdén O, (1994) Prognostic factors for long-term survival in leukemic marrow recipients with special emphasis on age and prophylaxis for graft-versus-host disease. Clin Transpl 8: 258-270. PubMed: 8061365.
4. Sullivan KM, Storb R, Buckner CD, Fefer A, Fisher L, et al. (1989) Graft-versus-host disease as adoptive immunotherapy in patients with advanced hematologic neoplasms. N Engl J Med 320: 828-834. doi:10.1056/NEJM198903303201303. PubMed: 2648143.
5. Hahn T, McCarthy PL Jr., Zhang MJ, Wang D, Arora M, et al. (2008) Risk factors for acute graft-versus-host disease after human leukocyte antigen-identical sibling transplants for adults with leukemia. J Clin Oncol 26: 5728-5734. doi:10.1200/JCO.2008.17.6545. PubMed: 18981462.
6. Ordemann R, Hutchinson R, Friedman J, Burakoff SJ, Reddy P, et al. (2002) Enhanced allostimulatory activity of host antigen-presenting cells in old mice intensifies acute graft-versus-host disease. J Clin Invest 109: 1249-1256. doi:10.1172/JCI0214793. PubMed: 11994414.
7. Bryson JS, Jennings CD, Caywood BE, Dix AR, Lowery DM, et al. (1997) Enhanced graft-versus-host disease in older recipient mice following allogeneic bone marrow transplantation. Bone Marrow Transplant 19: 721-728. doi:10.1038/sj.bmt.1700719. PubMed: 9156250.
8. Pasquini MC, Wang Z, Horowitz MM, Gale RP, (2010) 2010 report from the Center for International Blood and Marrow Transplant Research (CIBMTR): current uses and outcomes of hematopoietic cell transplants for blood and bone marrow disorders. Clin Transpl 24: 87-105. PubMed: 21696033.
9. Li J, Semple K, Suh WK, Liu C, Chen F, et al. (2011) Roles of CD28, CTLA4, and inducible costimulator in acute graft-versus-host disease in mice. Biol Blood Marrow Transplant 17: 962-969. doi:10.1016/j.bbmt.2011.01.018. PubMed: 21447398.
10. Amarnath S, Costanzo CM, Mariotti J, Ullman JL, Telford WG, et al. (2010) Regulatory T cells and human myeloid dendritic cells promote tolerance via programmed death ligand-1. PLOS Biol 8: e1000302. PubMed: 20126379.
11. Li W, Wang X, Chen R, Zhu H, Chen G, et al. (2012) Overexpression of programmed death ligand 1 in dendritic cells inhibits allogeneic lymphocyte activation in mice. J Surg Res 176: e79-e87. doi:10.1016/j.jss.2011.09.049. PubMed: 22381170.
12. Shlomchik WD, Couzens MS, Tang CB, McNiff J, Robert ME, et al. (1999) Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science 285: 412-415. doi:10.1126/science.285.5426.412. PubMed: 10411505.
13. Matte CC, Liu J, Cormier J, Anderson BE, Athanasiadis I, et al. (2004) Donor APCs are required for maximal GVHD but not for GVL. Nat Med 10: 987-992. doi:10.1038/nm1089. PubMed: 15286785.
14. Duffner UA, Maeda Y, Cooke KR, Reddy P, Ordemann R, et al. (2004) Host dendritic cells alone are sufficient to initiate acute graft-versus-host disease. J Immunol 172: 7393-7398. PubMed: 15187116.
15. Wang X, Li H, Matte-Martone C, Cui W, Li N, et al. (2011) Mechanisms of antigen presentation to T cells in murine graft-versus-host disease: cross-presentation and the appearance of cross-presentation. Blood 118: 6426-6437. doi:10.1182/blood-2011-06-358747. PubMed: 21963602.
16. Blazar BR, Murphy WJ, Abedi M, (2012) Advances in graft-versus-host disease biology and therapy. Nat Rev Immunol 12: 443-458. doi:10.1038/nri3212. PubMed: 22576252.
17. Ferrara JL, Levine JE, Reddy P, Holler E, (2009) Graft-versus-host disease. Lancet 373: 1550-1561. doi:10.1016/S0140-6736(09)60237-3. PubMed: 19282026.
18. Wolf D, von Lilienfeld-Toal M, Wolf AM, Schleuning M, von Bergwelt-Baildon M, et al. (2012) Novel treatment concepts for graft-versus-host disease. Blood 119: 16-25. doi:10.1182/blood-2011-08-339465. PubMed: 21948301.
19. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, et al. (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18: 767-811. doi:10.1146/annurev.immunol.18.1.767. PubMed: 10837075.
20. Belz GT, Xie W, Altman JD, Doherty PC, (2000) A Previously Unrecognized H-2Db-Restricted Peptide Prominent in the Primary Influenza A Virus-Specific CD8+T-Cell Response Is Much Less Apparent following Secondary Challenge. J Virol 74: 3486-3493. doi:10.1128/JVI.74.8.3486-3493.2000. PubMed: 10729122.
21. Morelli AE, Thomson AW, (2007) Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 7: 610-621. doi:10.1038/nri2132. PubMed: 17627284.
22. Sato K, Yamashita N, Baba M, Matsuyama T, (2003) Regulatory dendritic cells protect mice from murine acute graft-versus-host disease and leukemia relapse. Immunity 18: 367-379. doi:10.1016/S1074-7613(03)00055-4. PubMed: 12648454.
23. Zhang X, Li M, Lian D, Zheng X, Zhang ZX, et al. (2008) Generation of therapeutic dendritic cells and regulatory T cells for preventing allogeneic cardiac graft rejection. Clin Immunol 127: 313-321. doi:10.1016/j.clim.2008.01.013. PubMed: 18358783.
24. Torres-Aguilar H, Aguilar-Ruiz SR, González-Pérez G, Munguía R, Bajaña S, et al. (2010) Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD4+ T Cells. J Immunol 184: 1765-1775. doi:10.4049/jimmunol.0902133. PubMed: 20083662.
25. Chorny A, Gonzalez-Rey E, Fernandez-Martin A, Pozo D, Ganea D, et al. (2005) Vasoactive intestinal peptide induces regulatory dendritic cells with therapeutic effects on autoimmune disorders. Proc Natl Acad Sci U S A 102: 13562-13567. doi:10.1073/pnas.0504484102. PubMed: 16150720.
26. Sato K, Yamashita N, Baba M, Matsuyama T, (2003) Modified myeloid dendritic cells act as regulatory dendritic cells to induce anergic and regulatory T cells. Blood 101: 3581-3589. doi:10.1182/blood-2002-09-2712. PubMed: 12511411.
27. Fujita S, Seino K, Sato K, Sato Y, Eizumi K, et al. (2006) Regulatory dendritic cells act as regulators of acute lethal systemic inflammatory response. Blood 107: 3656-3664. doi:10.1182/blood-2005-10-4190. PubMed: 16410444.
28. Fujita S, Yamashita N, Ishii Y, Sato Y, Sato K, et al. (2008) Regulatory dendritic cells protect against allergic airway inflammation in a murine asthmatic model. J Allergy Clin Immunol 121: 95-104. doi:10.1016/j.jaci.2007.12.381. PubMed: 17920666.
29. Lan YY, Wang Z, Raimondi G, Wu W, Colvin BL, et al. (2006) "Alternatively activated" dendritic cells preferentially secrete IL-10, expand Foxp3+CD4+ T cells, and induce long-term organ allograft survival in combination with CTLA4-Ig. J Immunol 177: 5868-5877. PubMed: 17056511.
30. Chorny A, Gonzalez-Rey E, Fernandez-Martin A, Ganea D, Delgado M, (2006) Vasoactive intestinal peptide induces regulatory dendritic cells that prevent acute graft-versus-host disease while maintaining the graft-versus-tumor response. Blood 107: 3787-3794. doi:10.1182/blood-2005-11-4495. PubMed: 16418327.
31. Ujike A, Takeda K, Nakamura A, Ebihara S, Akiyama K, et al. (2002) Impaired dendritic cell maturation and increased T(H)2 responses in PIR-B(-/-) mice. Nat Immunol 3: 542-548. doi:10.1038/ni801. PubMed: 12021780.
32. Guleria I, Khosroshahi A, Ansari MJ, Habicht A, Azuma M, et al. (2005) A critical role for the programmed death ligand 1 in fetomaternal tolerance. J Exp Med 202: 231-237. doi:10.1084/jem.20050019. PubMed: 16027236.
33. Meyerholz DK, Stoltz DA, Namati E, Ramachandran S, Pezzulo AA, et al. (2010) Loss of cystic fibrosis transmembrane conductance regulator function produces abnormalities in tracheal development in neonatal pigs and young children. Am J Respir Crit Care Med 182: 1251-1261. doi:10.1164/rccm.201004-0643OC. PubMed: 20622026.
34. Nervi B, Rettig MP, Ritchey JK, Wang HL, Bauer G, et al. (2007) Factors affecting human T cell engraftment, trafficking, and associated xenogeneic graft-vs-host disease in NOD/SCID beta2mnull mice. Exp Hematol 35: 1823-1838. doi:10.1016/j.exphem.2007.06.007. PubMed: 17764813.
35. Fujita S, Sato Y, Sato K, Eizumi K, Fukaya T, et al. (2007) Regulatory dendritic cells protect against cutaneous chronic graft-versus-host disease mediated through CD4+CD25+Foxp3+ regulatory T cells. Blood 110: 3793-3803. doi:10.1182/blood-2007-04-086470. PubMed: 17687106.
36. Hadeiba H, Sato T, Habtezion A, Oderup C, Pan J, et al. (2008) CCR9 expression defines tolerogenic plasmacytoid dendritic cells able to suppress acute graft-versus-host disease. Nat Immunol 9: 1253-1260. doi:10.1038/ni.1658. PubMed: 18836452.
37. Keir ME, Butte MJ, Freeman GJ, Sharpe AH, (2008) PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 26: 677-704. doi:10.1146/annurev.immunol.26.021607.090331. PubMed: 18173375.
38. Kubagawa H, Chen CC, Ho LH, Shimada TS, Gartland L, et al. (1999) Biochemical nature and cellular distribution of the paired immunoglobulin-like receptors, PIR-A and PIR-B. J Exp Med 189: 309-318. doi:10.1084/jem.189.2.309. PubMed: 9892613.
39. Ruane DT, Lavelle EC, (2011) The role of CD103(+) dendritic cells in the intestinal mucosal immune system. Front Immunol 2: 25. PubMed: 22566815.
40. Sato K, Eizumi K, Fukaya T, Fujita S, Sato Y, et al. (2009) Naturally occurring regulatory dendritic cells regulate murine cutaneous chronic graft-versus-host disease. Blood 113: 4780-4789. doi:10.1182/blood-2008-10-183145. PubMed: 19228924.
41. Takai T, (2005) Paired immunoglobulin-like receptors and their MHC class I recognition. Immunology 115: 433-440. doi:10.1111/j.1365-2567.2005.02177.x. PubMed: 16011512.
42. Kunisaki KM, Janoff EN, (2009) Influenza in immunosuppressed populations: a review of infection frequency, morbidity, mortality, and vaccine responses. Lancet Infect Dis 9: 493-504. doi:10.1016/S1473-3099(09)70175-6. PubMed: 19628174.
43. Mou HB, Lin MF, Cen H, Yu J, Meng XJ, (2004) TGF-beta1 treated murine dendritic cells are maturation resistant and down-regulate Toll-like receptor 4 expression. J Zhejiang Univ Sci 5: 1239-1244. doi:10.1631/jzus.2004.1239. PubMed: 15362195.
44. Josefowicz SZ, Rudensky A, (2009) Control of regulatory T cell lineage commitment and maintenance. Immunity 30: 616-625. doi:10.1016/j.immuni.2009.04.009. PubMed: 19464984.
45. Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG, (2011) Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol 29: 71-109. doi:10.1146/annurev-immunol-031210-101312. PubMed: 21166540.
46. Guilliams M, Crozat K, Henri S, Tamoutounour S, Grenot P, et al. (2010) Skin-draining lymph nodes contain dermis-derived CD103- dendritic cells that constitutively produce retinoic acid and induce Foxp3+ regulatory T cells. Blood 115: 1958-1968. doi:10.1182/blood-2009-09-245274. PubMed: 20068222.
47. Scott CL, Aumeunier AM, Mowat AM, (2011) Intestinal CD103+ dendritic cells: master regulators of tolerance? Trends Immunol 32: 412-419. doi:10.1016/j.it.2011.06.003. PubMed: 21816673.
48. Del Rio M-L, Bernhardt G, Rodriguez-Barbosa J-I, Förster R, (2010) Development and functional specialization of CD103+ dendritic cells. Immunol Rev 234: 268-281. doi:10.1111/j.0105-2896.2009.00874.x. PubMed: 20193025.
49. Keir ME, Francisco LM, Sharpe AH, (2007) PD-1 and its ligands in T-cell immunity. Curr Opin Immunol 19: 309-314. doi:10.1016/j.coi.2007.04.012. PubMed: 17433872.
50. Fife BT, Pauken KE, (2011) The role of the PD-1 pathway in autoimmunity and peripheral tolerance. Ann N Y Acad Sci 1217: 45-59. doi:10.1111/j.1749-6632.2010.05919.x. PubMed: 21276005.
51. Shin T, Kennedy G, Gorski K, Tsuchiya H, Koseki H, et al. (2003) Cooperative B7-1/2 (CD80/CD86) and B7-DC costimulation of CD4+ T cells independent of the PD-1 receptor. J Exp Med 198: 31-38. doi:10.1084/jem.20030242. PubMed: 12847135.
52. Ruffner MA, Kim SH, Bianco NR, Francisco LM, Sharpe AH, et al. (2009) B7-1/2, but not PD-L1/2 molecules, are required on IL-10-treated tolerogenic DC and DC-derived exosomes for in vivo function. Eur J Immunol 39: 3084-3090. doi:10.1002/eji.200939407. PubMed: 19757438.
53. Butte MJ, Keir ME, Phamduy TB, Sharpe AH, Freeman GJ, (2007) Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity 27: 111-122. doi:10.1016/j.immuni.2007.05.016. PubMed: 17629517.
54. Yi T, Li X, Yao S, Wang L, Chen Y, et al. (2011) Host APCs augment in vivo expansion of donor natural regulatory T cells via B7H1/B7.1 in allogeneic recipients. J Immunol 186: 2739-2749. doi:10.4049/jimmunol.1002939. PubMed: 21263067.
55. Nakamura A, Kobayashi E, Takai T, (2004) Exacerbated graft-versus-host disease in Pirb-/- mice. Nat Immunol 5: 623-629. doi:10.1038/ni1074. PubMed: 15146181.
56. Zhao J, Luo Y, Wang X, Zhou H, Li Q, et al. (2010) Prevention of murine acute graft-versus-host disease by recipient-derived paired immunoglobulin-like receptor B lentivirus-transfected dendritic cells. Acta Haematol 124: 134-140. doi:10.1159/000315553. PubMed: 20881379.