Prevention of CpG-induced pregnancy disruption by adoptive transfer of in vitro-induced regulatory T cells

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Lin, Yi ^a   Liu, Xiaorui ^a   Shan, Bin ^b   Wu, Ji ^c   Sharma, Surendra ^d   Sun, Yun ^e,f  

^a Shanghai Municipal Key Clinical Specialty Shanghai Jiao Tong University School of Medicine   (China)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

^d BROWN UNIVERSITY   (United States)

^e SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^f Shanghai Key Laboratory for Assisted Reproduction and Reproductive Genetics   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CPG 1826; FINGOLIMOD; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; NEUTRALIZING ANTIBODY; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR AGONIST; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; OLIGODEOXYRIBONUCLEOTIDE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CPG ISLAND; DISEASE MODEL; EMBRYO; EMBRYO RESORPTION; FEMALE; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PREGNANCY; PREGNANCY DISORDER; PREGNANCY OUTCOME; PREMATURE LABOR; REGULATORY T LYMPHOCYTE; SPLEEN; WILD TYPE; ABORTION, SPONTANEOUS; ANIMAL; CHEMICALLY INDUCED; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOCYTE COUNT; METABOLISM; PHENOTYPE; PREMATURE BIRTH;

ABORTION, SPONTANEOUS; ADOPTIVE TRANSFER; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; IMMUNOPHENOTYPING; INTERLEUKIN-10; LYMPHOCYTE COUNT; MALE; MICE; MICE, INBRED NOD; OLIGODEOXYRIBONUCLEOTIDES; PHENOTYPE; PREGNANCY; PREGNANCY OUTCOME; PREMATURE BIRTH; T-LYMPHOCYTES, REGULATORY;

EID: 84899440792     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094702     Document Type: Article

References (44)

1. Ewald SE, Lee BL, Lau L, Wickliffe KE, Shi GP, et al. (2008) The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature 456: 658-662.
2. Krieg AM. CpG Motifs in bacterial DNA and their immune effects (2002) Annu Rev Immunol 20: 709-760.
3. Pedersen G, Andresen L, Matthiessen MW, Rask-Madsen J, Brynskov J (2005) Expression of toll-like receptor 9 and response to bacterial CpG oligodeoxynucleotides in human intestinal epithelium. Clin Exp Immunol 141: 298-306. (Pubitemid 41003354)
4. Thaxton JE, Romero R, Sharma S (2009) TLR9 activation coupled to IL-10 deficiency induces adverse pregnancy outcomes. J Immunol 183: 1144-1154.
5. Sun Y, Qin X, Shan B, Wang W, Zhu Q, et al. (2013) Differential effects of the CpG-TLR9 axis on pregnancy outcome in nonobese diabetic mice and wildtype controls. Fertil Steril 99: 1759-1767.
6. Murphy SP, Fast LD, Hanna NN, Sharma S (2005) Uterine NK cells mediate inflammation-induced fetal demise in IL-10-null mice. J Immunol 175: 4084-4090. (Pubitemid 41292072)
7. Murphy SP, Hanna NN, Fast LD, Shaw SK, Berg G, et al. (2009) Evidence for participation of uterine NK cells in the mechanisms responsible for spontaneous preterm labor and delivery. Am J Obstet Gynecol 200: 308e1-308e9.
8. Robertson SA, Skinner RJ, Care AS (2006) Essential role for IL-10 in resistance to lipopolysaccharide-induced preterm labor in mice. J Immunol 177: 4888-4896. (Pubitemid 44469825)
9. + natural killer cell transfer in sub-fertile NOD mice. Reprod BioMed Online 18: 95-103.
10. Lin Y, Ren L, Wang W, Di J, Zeng S, et al. (2009) Effect of TLR3 and TLR7 activation in uterine NK cells from non-obese diabetic (NOD) mice. J Reprod Immunol 82: 12-23.
11. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J Exp Med 198:1875-1886.
12. + regulators. J Immunol 180: 7636-7647.
13. + regulatory T cells in NOD mice. Am J Reprod Immunol 66: 349-362.
14. Higuma-Myojo S, Sasaki Y, Miyazaki S, Sakai M, Siozaki A, et al. (2005) Cytokine profile of natural killer cells in early human pregnancy. Am J Reprod Immunol 54: 21-29. (Pubitemid 40895146)
15. Lin Y, Zhong Y, Saito S, Chen Y, Shen W, et al. (2009) Characterization of natural killer cells in nonobese diabetic/severely compromised immunodeficient mice during pregnancy. Fertil Steril 91: 2676-2686.
16. Lin Y, Chen Y, Zeng Y, Wang T, Zeng S (2005) Lymphocyte phenotyping and NK cell activity analysis in pregnant NOD/SCID mice. J Reprod Immunol 68: 39-51. (Pubitemid 41739447)
17. Rocha-Campos AC, Melki R, Zhu R, Deruytter N, Damotte D, et al. (2006) Genetic and functional analysis of the Nkt1 locus using congenic NOD mice: improved Va14-NKT cell performance but failure to protect against type 1 diabetes. Diabetes 55:1163-1170. (Pubitemid 44100196)
18. +T cell migration and prevents embryo loss in NOD mice. Fertil Steril 91: 2687-2696.
19. Li LP, Fang YC, Dong GF, Lin Y, Saito S (2012) Depletion of invariant NKT cells reduces inflammation-induced preterm delivery in mice. J Immunol 188: 4681-4689.
20. Fischer K, Anderesen R, Mackensen A (2002) An improved flow cytometric assay for the determination of cytotoxic T lymphocyte activity. J Immunol Methods 259: 159-169. (Pubitemid 33124393)
21. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, et al. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
22. Lin Y, Liang Z, Chen Y, Zeng Y (2006) TLR3-involved modulation of pregnancy tolerance in double-stranded RNA-stimulated NOD/SCID mice. J Immunol 176: 4147-4154. (Pubitemid 44264394)
23. Yin G, Li C, Shan B, Wang W, Chen H, et al. (2011) Insufficient peroxiredoxin-2 expression in uterine NK cells obtained from a murine model of abortion. J Cell Biochem 112: 773-781.
24. Li C, Wang W, Wang H, Zhong Y, Di J, et al. (2009) Proteomic analysis of proteins differentially expressed in uterine lymphocytes obtained from wild-type and NOD mice. J Cell Biochem 108: 447-457.
25. + T cells influence success and failure of pregnancy in CBA/J x DBA/2J matings. Cell Immunol 196: 71-79.
26. Parsons CH, Adang LA, Overdevest J, O'Connor CM, Taylor JR, et al. (2006) KSHV targets multiple leukocyte lineages during long-term productive infection in NOD/SCID mice. J Clin Invest 116: 1963-1973. (Pubitemid 44033320)
27. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, et al. (2006) Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 12: 1065-1074. (Pubitemid 44353388)
28. Saito S, Shiozaki A, Sasaki Y, Nakashima A, Shima T, et al. (2007) Regulatory T cells and regulatory natural killer (NK) cells play important roles in feto-maternal tolerance. Semin Immunopathol 29: 115-122. (Pubitemid 47596391)
29. Saito S, Nakashima A, Myojo-Higuma S, Shiozaki A. (2008) The balance between cytotoxic NK cells and regulatory NK cells in human pregnancy. J Reprod Immunol 77: 14-22.
30. Kalkunte SS, Mselle TF, Norris WE, Wira CR, Sentman CL, et al. (2009) Vascular endothelial growth factor C facilitates immune tolerance and endovascular activity of human uterine NK cells at the maternal-fetal interface. J Immunol 182: 4085-4092.
31. Lin Y, Li C, Shan B, Wang W, Saito S, et al. (2011) Reduced stathmin-1 expression in natural killer cells associated with spontaneous abortion. Am J Pathol 178: 506-514.
32. Kataoka S, Satoh J, Fujiya H, Toyota T, Suzuki R, et al. (1983) Immunologic aspects of the nonobese diabetic (NOD) mouse: abnormalities of cellular immunity. Diabetes 32: 247-253. (Pubitemid 13138268)
33. Aluvihare VR, Kallikourdis M, Betz AG (2004) Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 5: 266-271. (Pubitemid 38332123)
34. Zhang Z, Schluesener HJ (2007) FTY720: a most promising immunosuppressant modulating immune cell functions. Mini Rev Med Chem 7: 845-850. (Pubitemid 47304946)
35. Brinkmann V (2007) Sphingosine 1-phosphate receptors in health and disease: mechanistic insights from gene deletion studies and reverse pharmacology. Pharmacol Ther 115: 84-105.
36. Matloubian M, Lo CG, Cinamon G, Lesneski MJ, Xu Y, et al. (2004) Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427: 355-360. (Pubitemid 38133663)
37. Lee SH, Kim KS, Fodil-Cornu N, Vidal SM, Biron CA (2009) Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection. J Exp Med 206: 2235-2251.
38. Fiorentino DF, Bond MW, Mosmann TR (1989) Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med 170: 2081-2095.
39. O'Garra A, Vieira P (2004) Regulatory T cells and mechanisms of immune system control. Nat Med 10: 801-805. (Pubitemid 39070850)
40. Trinchieri G (2007) Interleukin-10 production by effector T cells: Th1 cells show self control. J Exp Med 204: 239-243.
41. Maloy KJ, Powrie F (2001) Regulatory T cells in the control of immune pathology. Nat Immunol 2: 816-822.
42. + NK cell expansion: Comparative study based on BALB/cxC57BL/6 and NOD/SCIDxC57BL/6 pregnant models. Clin Immunol 126: 104-117.
43. Serpero LD, Filaci G, Parodi A, Battaglia F, Kalli F, et al. (2013) Fingolimod modulates peripheral effector and regulatory T cells in MS patients. J Neuroimmune Pharmacol 8:1106-1113.
44. Havla J, Tackenberg B, Hellwig K, Meinl I, Krumbholz M, et al. (2013) Fingolimod reduces recurrence of disease activity after natalizumab withdrawal in multiple sclerosis. J Neurol 260:1382-1387.