Abortion-Prone Mating Influences Alteration of Systemic a2 Vacuolar ATPase Expression in Spleen and Blood Immune Cells

American Journal of Reproductive Immunology

Volumn 67, Issue 5, 2012, Pages 421-433

  Jaiswal, Mukesh K ^a   Mallers, Timothy M ^a   Kwong, Christina ^a   Chaouat, Gerard ^b   Gilman Sachs, Alice ^a   Beaman, Kenneth D ^a  

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

^b INSERM   (France)

Author keywords

Abortion prone mating; Atp6v0a2; Blood; Spleen; Tolerance

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ISOENZYME;

ABORTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL POPULATION; FEMALE; FETUS RESORPTION; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOCOMPETENT CELL; MALE; MATING; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN CELL;

EID: 84858703349     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2011.01098.x     Document Type: Article

References (50)

1. Taglauer ES, Adams Waldorf KM, Petroff MG: The hidden maternal-fetal interface: events involving the lymphoid organs in maternal-fetal tolerance. Int J Dev Biol 2010; 54:421-430.
2. Soundararajan R, Rao AJ: Trophoblast 'pseudo-tumorigenesis': significance and contributory factors. Reprod Biol Endocrinol 2004; 2:15.
3. Jaiswal MK, Gilman-Sachs A, Chaouat G, Beaman KD: Placental ATPase expression is a link between multiple causes of spontaneous abortion in mice. Biol Reprod 2011; 85:626-634.
4. Ntrivalas E, Levine R, Kwong C, Gilman-Sachs A, Beaman K: The a2 isoform of vacuolar ATPase is a modulator of implantation and feto-maternal immune tolerance in early pregnancy. J Reprod Immunol 2010; 85:106-111.
5. Skinner MA, MacLaren LA, Wildeman AG: Stage-dependent redistribution of the V-ATPase during bovine implantation. J Histochem Cytochem 1999; 47:1247-1254.
6. Mas AE, Petitbarat M, Dubanchet S, Fay S, Ledee N, Chaouat G: Immune regulation at the interface during early steps of murine implantation: involvement of two new cytokines of the IL-12 family (IL-23 and IL-27) and of TWEAK. Am J Reprod Immunol 2008; 59:323-338.
7. Bobe P, Kiger N: Immunogenetic studies of spontaneous abortion in mice. III. Non-H-2 antigens and gestation. J Immunogenet 1989; 16:223-231.
8. Jin LP, Li DJ, Zhang JP, Wang MY, Zhu XY, Zhu Y, Meng Y, Yuan MM: Adoptive transfer of paternal antigen-hyporesponsive T cells induces maternal tolerance to the allogeneic fetus in abortion-prone matings. J Immunol 2004; 173:3612-3619.
9. Lattuada D, Mangioni S, Vigano P, Ntrivalas EI, Rossi M, Palotti F, Carinelli S, Beaman KD, Di Blasio AM: The placental immunomodulatory cytokine regeneration and tolerance factor is also expressed by both human cycling and early pregnant endometrium. Am J Reprod Immunol 2004; 52:224-231.
10. Ntrivalas E, Derks R, Gilman-Sachs A, Kwak-Kim J, Levine R, Beaman K: Novel role for the N-terminus domain of the a2 isoform of vacuolar ATPase in interleukin-1beta production. Hum Immunol 2007; 68:469-477.
11. Ntrivalas E, Gilman-Sachs A, Kwak-Kim J, Beaman K: The N-terminus domain of the a2 isoform of vacuolar ATPase can regulate interleukin-1beta production from mononuclear cells in co-culture with JEG-3 choriocarcinoma cells. Am J Reprod Immunol 2007; 57:201-209.
12. Ntrivalas E, Kwak-Kim J, Beaman K, Mantouvalos H, Gilman-Sachs A: An in vitro coculture model to study cytokine profiles of natural killer cells during maternal immune cell-trophoblast interactions. J Soc Gynecol Investig 2006; 13:196-202.
13. Sun-Wada G, Murata Y, Yamamoto A, Kanazawa H, Wada Y, Futai M: Acidic endomembrane organelles are required for mouse postimplantation development. Dev Biol 2000; 228:315-325.
14. Lee GW, Boomer JS, Gilman-Sachs A, Chedid A, Gudelj L, Rukavina D, Beaman KD: Regeneration and tolerance factor of the human placenta induces IL-10 production. Eur J Immunol 2001; 31:687-691.
15. Boomer JS, Lee GW, Givens TS, Gilman-Sachs A, Beaman KD: Regeneration and tolerance factor's potential role in T-cell activation and apoptosis. Hum Immunol 2000; 61:959-971.
16. Boomer JS, Derks RA, Lee GW, DuChateau BK, Gilman-Sachs A, Beaman KD: Regeneration and tolerance factor is expressed during T-lymphocyte activation and plays a role in apoptosis. Hum Immunol 2001; 62:577-588.
17. Derks R, Beaman K: Regeneration and tolerance factor modulates the effect of adenosine triphosphate-induced interleukin 1 beta secretion in human macrophages. Hum Immunol 2004; 65:676-682.
18. Ribbing SL, Hoversland RC, Beaman KD: T-cell suppressor factors play an integral role in preventing fetal rejection. J Reprod Immunol 1988; 14:83-95.
19. Levine RF, Derks R, Beaman K: Regeneration and tolerance factor. A vacuolar ATPase with consequences. Chem Immunol Allergy 2005; 89:126-134.
20. Kwong C, Gilman-Sachs A, Beaman K: Tumor-associated a2 vacuolar ATPase acts as a key mediator of cancer-related inflammation by inducing pro-tumorigenic properties in monocytes. J Immunol 2011; 186:1781-1789.
21. Allavena P, Sica A, Garlanda C, Mantovani A: The Yin-Yang of tumor-associated macrophages in neoplastic progression and immune surveillance. Immunol Rev 2008; 222:155-161.
22. Hanna J, Mandelboim O: When killers become helpers. Trends Immunol 2007; 28:201-206.
23. Simmons DG, Cross JC: Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev Biol 2005; 284:12-24.
24. Benirschke K, Kaufmann P: Pathology of the Human Placenta. New York, Springer, 2000.
25. Flori E, Doray B, Gautier E, Kohler M, Ernault P, Flori J, Costa JM: Circulating cell-free fetal DNA in maternal serum appears to originate from cyto- and syncytio-trophoblastic cells. Case report. Hum Reprod 2004; 19:723-724.
26. Erlebacher A, Vencato D, Price KA, Zhang D, Glimcher LH: Constraints in antigen presentation severely restrict T cell recognition of the allogeneic fetus. J Clin Invest 2007; 117:1399-1411.
27. Abumaree MH, Stone PR, Chamley LW: An in vitro model of human placental trophoblast deportation/shedding. Mol Hum Reprod 2006; 12:687-694.
28. Maroni ES, de Sousa MA: The lymphoid organs during pregnancy in the mouse. A comparison between a syngeneic and an allogeneic mating. Clin Exp Immunol 1973; 13:107-124.
29. Maroni ES, Parrott DM: Progressive increase in cell-mediated immunity against paternal transplantation antigens in parous mice after multiple pregnancies. Clin Exp Immunol 1973; 13:253-262.
30. Smith RN, Sternlicht M, Butcher GW: The alloantibody response in the allogeneically pregnant rat. I. The primary and secondary responses and detection of Ir gene control. J Immunol 1982; 129:771-776.
31. Smith RN, Sternlicht M: The alloantibody response in the allogeneically pregnant rat. III. The location of the alloantibody-forming cells. J Immunol 1982; 129:783-786.
32. Chavez DJ, McIntyre JA, Colliver JA, Faulk WP: Allogeneic matings and immunization have different effects on nulliparous and multiparous mice. J Immunol 1987; 139:85-88.
33. Teixeira Gomes RC, Verna C, Nader HB, dos Santos Simoes R, Dreyfuss JL, Martins JR, Baracat EC, de Jesus Simoes M, Soares JM Jr: Concentration and distribution of hyaluronic acid in mouse uterus throughout the estrous cycle. Fertil Steril 2009; 92:785-792.
34. Lee C, Ghoshal K, Beaman KD: Cloning of a cDNA for a T cell produced molecule with a putative immune regulatory role. Mol Immunol 1990; 27:1137-1144.
35. DuChateau BK, Lee GW, Westerman MP, Beaman KD: Increased expression of regeneration and tolerance factor in individuals with human immunodeficiency virus infection. Clin Diagn Lab Immunol 1999; 6:193-198.
36. Wegmann TG, Lin H, Guilbert L, Mosmann TR: Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol Today 1993; 14:353-356.
37. Abumaree MH, Stone PR, Chamley LW: The effects of apoptotic, deported human placental trophoblast on macrophages: possible consequences for pregnancy. J Reprod Immunol 2006; 72:33-45.
38. Matsuoka K, Ichinohe T, Hashimoto D, Asakura S, Tanimoto M, Teshima T: Fetal tolerance to maternal antigens improves the outcome of allogeneic bone marrow transplantation by a CD4+ CD25+ T-cell-dependent mechanism. Blood 2006; 107:404-409.
39. Fraccaroli L, Alfieri J, Larocca L, Calafat M, Mor G, Leiros CP, Ramhorst R: A potential tolerogenic immune mechanism in a trophoblast cell line through the activation of chemokine-induced T cell death and regulatory T cell modulation. Hum Reprod 2009; 24:166-175.
40. Mellor AL, Munn DH: Extinguishing maternal immune responses during pregnancy: implications for immunosuppression. Semin Immunol 2001; 13:213-218.
41. Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, Marshall B, Brown C, Mellor AL: Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998; 281:1191-1193.
42. Munn DH, Shafizadeh E, Attwood JT, Bondarev I, Pashine A, Mellor AL: Inhibition of T cell proliferation by macrophage tryptophan catabolism. J Exp Med 1999; 189:1363-1372.
43. Mellor AL, Sivakumar J, Chandler P, Smith K, Molina H, Mao D, Munn DH: Prevention of T cell-driven complement activation and inflammation by tryptophan catabolism during pregnancy. Nat Immunol 2001; 2:64-68.
44. de Waal Malefyt R, Haanen J, Spits H, Roncarolo MG, te Velde A, Figdor C, Johnson K, Kastelein R, Yssel H, de Vries JE: Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J Exp Med 1991; 174:915-924.
45. Dinarello CA: The IL-1 family and inflammatory diseases. Clin Exp Rheumatol 2002; 20:S1-S13.
46. Guerin LR, Moldenhauer LM, Prins JR, Bromfield JJ, Hayball JD, Robertson SA: Seminal fluid regulates accumulation of FOXP3+ regulatory T Cells in the preimplantation mouse uterus through expanding the FOXP3+ cell pool and CCL19-mediated recruitment. Biol Reprod 2011; 85:397-408.
47. Hetherington CM, Humber DP: The effect of pregnancy on lymph node weight in the mouse. J Immunogenet 1977; 4:271-276.
48. Ansell JD, McDougall CM, Speedy G, Inchley CJ: Changes in lymphocyte accumulation and proliferation in the lymph nodes draining the pregnant uterus. Clin Exp Immunol 1978; 31:397-407.
49. Norton MT, Fortner KA, Bizargity P, Bonney EA: Pregnancy alters the proliferation and apoptosis of mouse splenic erythroid lineage cells and leukocytes. Biol Reprod 2009; 81:457-464.
50. Mattsson R, Nilsson B, Lindahl-Kiessling K: An investigation of splenic enlargement in pregnant mice. Dev Comp Immunol 1979; 3:683-695.