Treg Cells Are Negatively Correlated with Increased Memory B Cells in Pre-eclampsia While Maintaining Suppressive Function on Autologous B-Cell Proliferation

American Journal of Reproductive Immunology

Volumn 70, Issue 6, 2013, Pages 454-463

  Zeng, Bin ^a   Kwak Kim, Joanne ^b   Liu, Ying ^a   Liao, Ai Hua ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

Memory B cell; Pre eclampsia; Pregnancy; Regulatory T cell

Indexed keywords

CD4 ANTIGEN; TRANSCRIPTION FACTOR FOXP3;

ADULT; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL ISOLATION; CELL PROLIFERATION; CLINICAL ARTICLE; FEMALE; FLOW CYTOMETRY; GESTATIONAL AGE; HUMAN; IN VITRO STUDY; MEMORY; PARITY; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; CYTOLOGY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; PATHOLOGY; PROSPECTIVE STUDY;

ADULT; B-LYMPHOCYTES; CELL PROLIFERATION; FEMALE; HUMANS; IMMUNOLOGIC MEMORY; PRE-ECLAMPSIA; PREGNANCY; PROSPECTIVE STUDIES; T-LYMPHOCYTES, REGULATORY;

EID: 84887627172     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12154     Document Type: Article

References (44)

1. Zhou CC, Irani RA, Dai Y, Blackwell SC, Hicks MJ, Ramin SM, Kellems RE, Xia Y: Autoantibody-mediated IL-6-dependent endothelin-1 elevation underlies pathogenesis in a mouse model of preeclampsia. J Immunol 2011; 186:6024-6034.
2. Serrano NC: Immunology and genetic of preeclampsia. Clin Dev Immunol 2006; 13:197-201.
3. Azizieh F, Raghupathy R, Makhseed M: Maternal cytokine production patterns in women with pre-eclampsia. Am J Reprod Immunol 2005; 54:30-37.
4. Germain SJ, Sacks GP, Sooranna SR, Sargent IL, Redman CW: Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circulating syncytiotrophoblast microparticles. J Immunol 2007; 178:5949-5956.
5. Lee VM, Quinn PA, Jennings SC, Ng LL: Neutrophil activation and production of reactive oxygen species in pre-eclampsia. J Hypertens 2003; 21:395-402.
6. Santner-Nanan B, Peek MJ, Khanam R, Richarts L, Zhu E, Fazekas de St Groth B, Nanan R: Systemic increase in the ratio between Foxp3+ and IL-17-producing CD4+ T cells in healthy pregnancy but not in preeclampsia. J Immunol 2009; 183:7023-7030.
7. Xia Y, Zhou CC, Ramin SM, Kellems RE: Angiotensin receptors, autoimmunity, and preeclampsia. J Immunol 2007; 179:3391-3395.
8. Guerin LR, Prins JR, Robertson SA: Regulatory T-cells and immune tolerance in pregnancy: a new target for infertility treatment? Hum Reprod Update 2009; 15:517-535.
9. Zenclussen AC, Gerlof K, Zenclussen ML, Sollwedel A, Bertoja AZ, Ritter T, Kotsch K, Leber J, Volk HD: Abnormal T-cell reactivity against paternal antigens in spontaneous abortion: adoptive transfer of pregnancy-induced CD4+CD25+ T regulatory cells prevents fetal rejection in a murine abortion model. Am J Pathol 2005; 166:811-822.
10. Jasper MJ, Tremellen KP, Robertson SA: Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Mol Hum Reprod 2006; 12:301-308.
11. Sasaki Y, Sakai M, Miyazaki S, Higuma S, Shiozaki A, Saito S: Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol Hum Reprod 2004; 10:347-353.
12. Toldi G, Svec P, Vasarhelyi B, Meszaros G, Rigo J, Tulassay T, Treszl A: Decreased number of FoxP3+ regulatory T cells in preeclampsia. Acta Obstet Gynecol Scand 2008; 87:1229-1233.
13. Prins JR, Boelens HM, Heimweg J, Van der Heide S, Dubois AE, Van Oosterhout AJ, Erwich JJ: Preeclampsia is associated with lower percentages of regulatory T cells in maternal blood. Hypertens Pregnancy 2009; 28:300-311.
14. Lee SK, Kim JY, Hur SE, Kim CJ, Na BJ, Lee M, Gilman-Sachs A, Kwak-Kim J: An imbalance in interleukin-17-producing T and Foxp3(+) regulatory T cells in women with idiopathic recurrent pregnancy loss. Hum Reprod 2011; 26:2964-2971.
15. Mei S, Tan J, Chen H, Chen Y, Zhang J: Changes of CD4+CD25high regulatory T cells and FOXP3 expression in unexplained recurrent spontaneous abortion patients. Fertil Steril 2010; 94:2244-2247.
16. Darmochwal-Kolarz D, Kludka-Sternik M, Tabarkiewicz J, Kolarz B, Rolinski J, Leszczynska-Gorzelak B, Oleszczuk J: The predominance of Th17 lymphocytes and decreased number and function of Treg cells in preeclampsia. J Reprod Immunol 2012; 93:75-81.
17. Sasaki Y, Darmochwal-Kolarz D, Suzuki D, Sakai M, Ito M, Shima T, Shiozaki A, Rolinski J, Saito S: Proportion of peripheral blood and decidual CD4(+) CD25(bright) regulatory T cells in pre-eclampsia. Clin Exp Immunol 2007; 149:139-145.
18. Darmochwal-Kolarz D, Saito S, Rolinski J, Tabarkiewicz J, Kolarz B, Leszczynska-Gorzelak B, Oleszczuk J: Activated T lymphocytes in pre-eclampsia. Am J Reprod Immunol 2007; 58:39-45.
19. Steinborn A, Haensch GM, Mahnke K, Schmitt E, Toermer A, Meuer S, Sohn C: Distinct subsets of regulatory T cells during pregnancy: is the imbalance of these subsets involved in the pathogenesis of preeclampsia? Clin Immunol 2008; 129:401-412.
20. Toldi G, Saito S, Shima T, Halmos A, Veresh Z, Vasarhelyi B, Rigo J Jr, Molvarec A: The frequency of peripheral blood CD4+ CD25high FoxP3+ and CD4+ CD25- FoxP3+ regulatory T cells in normal pregnancy and pre-eclampsia. Am J Reprod Immunol 2012; 68:175-180.
21. Steinborn A, Schmitt E, Kisielewicz A, Rechenberg S, Seissler N, Mahnke K, Schaier M, Zeier M, Sohn C: Pregnancy-associated diseases are characterized by the composition of the systemic regulatory T cell (Treg) pool with distinct subsets of Tregs. Clin Exp Immunol 2012; 167:84-98.
22. Xia Y, Kellems RE: Is preeclampsia an autoimmune disease? Clin Immunol 2009; 133:1-12.
23. do Prado AD, Piovesan DM, Staub HL, Horta BL: Association of anticardiolipin antibodies with preeclampsia: a systematic review and meta-analysis. Obstet Gynecol 2010; 116:1433-1443.
24. Shaarawy M, Youssef el-Mallah S, el-Yamani AM: The prevalence of serum antineutrophil cytoplasmic autoantibodies in preeclampsia and eclampsia. J Soc Gynecol Investig 1997; 4:34-39.
25. Siddiqui AH, Irani RA, Blackwell SC, Ramin SM, Kellems RE, Xia Y: Angiotensin receptor agonistic autoantibody is highly prevalent in preeclampsia: correlation with disease severity. Hypertension 2010; 55:386-393.
26. Branch DW, Mitchell MD, Miller E, Palinski W, Witztum JL: Pre-eclampsia and serum antibodies to oxidised low-density lipoprotein. Lancet 1994; 343:645-646.
27. Jensen F, Wallukat G, Herse F, Budner O, El-Mousleh T, Costa SD, Dechend R, Zenclussen AC: CD19+CD5+ cells as indicators of preeclampsia. Hypertension 2012; 59:861-868.
28. Liao AH, Liu LP, Ding WP, Zhang L: Functional changes of human peripheral B-lymphocytes in pre-eclampsia. Am J Reprod Immunol 2009; 61:313-321.
29. Lim HW, Hillsamer P, Banham AH, Kim CH: Cutting edge: direct suppression of B cells by CD4+ CD25+ regulatory T cells. J Immunol 2005; 175:4180-4183.
30. Iikuni N, Lourenco EV, Hahn BH, La Cava A: Cutting edge: regulatory T cells directly suppress B cells in systemic lupus erythematosus. J Immunol 2009; 183:1518-1522.
31. Zhao DM, Thornton AM, DiPaolo RJ, Shevach EM: Activated CD4+CD25+ T cells selectively kill B lymphocytes. Blood 2006; 107:3925-3932.
32. Turner JA: Diagnosis and management of pre-eclampsia: an update. Int J Womens Health 2010; 2:327-337.
33. Schroeder BM: ACOG practice bulletin on diagnosing and managing preeclampsia and eclampsia. American College of Obstetricians and Gynecologists. Am Fam Physician 2002; 66:330-331.
34. Rodriguez-Bayona B, Ramos-Amaya A, Perez-Venegas JJ, Rodriguez C, Brieva JA: Decreased frequency and activated phenotype of blood CD27 IgD IgM B lymphocytes is a permanent abnormality in systemic lupus erythematosus patients. Arthritis Res Ther 2010; 12:R108.
35. Asito AS, Piriou E, Jura WG, Ouma C, Odada PS, Ogola S, Fiore N, Rochford R: Suppression of circulating IgD+CD27+ memory B cells in infants living in a malaria-endemic region of Kenya. Malar J 2011; 10:362.
36. Paeschke S, Chen F, Horn N, Fotopoulou C, Zambon-Bertoja A, Sollwedel A, Zenclussen ML, Casalis PA, Dudenhausen JW, Volk HD, Zenclussen AC: Pre-eclampsia is not associated with changes in the levels of regulatory T cells in peripheral blood. Am J Reprod Immunol 2005; 54:384-389.
37. Hu D, Chen Y, Zhang W, Wang H, Wang Z, Dong M: Alteration of peripheral CD4+CD25+ regulatory T lymphocytes in pregnancy and pre-eclampsia. Acta Obstet Gynecol Scand 2008; 87:190-194.
38. Yanaba K, Bouaziz JD, Matsushita T, Magro CM, St Clair EW, Tedder TF: B-lymphocyte contributions to human autoimmune disease. Immunol Rev 2008; 223:284-299.
39. Matthiesen L, Berg G, Ernerudh J, Hakansson L: Lymphocyte subsets and mitogen stimulation of blood lymphocytes in preeclampsia. Am J Reprod Immunol 1999; 41:192-203.
40. Mahmoud F, Omu A, Abul H, El-Rayes S, Haines D: Lymphocyte subpopulations in pregnancy complicated by hypertension. J Obstet Gynaecol 2003; 23:20-26.
41. Darmochwal-Kolarz D, Leszczynska-Gorzelak B, Rolinski J, Oleszczuk J: Pre-eclampsia affects the immunophenotype of neonates. Immunol Lett 2001; 77:67-71.
42. Souto-Carneiro MM, Mahadevan V, Takada K, Fritsch-Stork R, Nanki T, Brown M, Fleisher TA, Wilson M, Goldbach-Mansky R, Lipsky PE: Alterations in peripheral blood memory B cells in patients with active rheumatoid arthritis are dependent on the action of tumour necrosis factor. Arthritis Res Ther 2009; 11:R84.
43. Hansen A, Daridon C, Dorner T: What do we know about memory B cells in primary Sjogren's syndrome? Autoimmun Rev 2010; 9:600-603.
44. Lee SK, Kim JY, Jang BW, Hur SE, Na BJ, Lee M, Fukui A, Gilman-Sachs A, Kwak-Kim J: Foxp3(high) and Foxp3(low) Treg cells differentially correlate with T helper 1 and natural killer cells in peripheral blood. Hum Immunol 2011; 72:621-626.