Placental atpase expression is a link between multiple causes of spontaneous abortion in mice

Biology of Reproduction

Volumn 85, Issue 3, 2011, Pages 626-634

  Jaiswal, Mukesh Kumar ^a   Gilman Sachs, Alice ^a   Chaouat, Gerard ^b   Beaman, Kenneth D ^a  

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

^b INSERM   (France)

Author keywords

A2v atpase; Abortion prone model; Macrophages; Placenta; Placentation; Pregnancy; Preimplantation embryo; Reproductive immunology

Indexed keywords

ADENOSINE TRIPHOSPHATASE; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN A2V; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CELL SURFACE; CONTROLLED STUDY; EMBRYO; FEMALE; FETUS; GENE EXPRESSION; HYPOTHESIS; MACROPHAGE; MALE; MATING; MOUSE; NONHUMAN; PHENOTYPE; PLACENTA; PLACENTA DEVELOPMENT; POLARIZATION; PREGNANCY OUTCOME; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SPONTANEOUS ABORTION;

ABORTION, SPONTANEOUS; ANIMALS; EMBRYONIC DEVELOPMENT; FEMALE; FETUS; MALE; MICE; MICE, INBRED STRAINS; PLACENTA; PLACENTATION; PREGNANCY; UTERUS; VACUOLAR PROTON-TRANSLOCATING ATPASES;

ANIMALIA; MURINAE; MUS;

EID: 80052518411     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.092494     Document Type: Article

References (44)

1. Trowsdale J, Betz AG. Mother's little helpers: mechanisms of maternalfetal tolerance. Nat Immunol 2006; 7:241-246.
2. Guleria I, Sayegh MH. Maternal acceptance of the fetus: true human tolerance. J Immunol 2007; 178:3345-3351.
3. Tafuri A, Alferink J, Moller P, Hammerling GJ, Arnold B. T cell awareness of paternal alloantigens during pregnancy. Science 1995; 270:630-633.
4. Jiang SP, Vacchio MS. Multiple mechanisms of peripheral T cell tolerance to the fetal "allograft." J Immunol 1998; 160:3086-3090.
5. Zhou M, Mellor AL. Expanded cohorts of maternal CD8+ T-cells specific for paternal MHC class I accumulate during pregnancy. J Reprod Immunol 1998; 40:47-62.
6. Ntrivalas E, Levine R, Kwong C, Gilman-Sachs A, Beaman K. The a2 isoform of vacuolar ATPase is a modulator of implantation and fetomaternal immune tolerance in early pregnancy. J Reprod Immunol 2010; 85:106-111.
7. Kang JA, McBey BA, Angkachatchai V, Croy BA, Beaman KD. Expression of TJ6 during pregnancy. Am J Reprod Immunol 1997; 38:183-188.
8. 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.
9. Babichev Y, Tamir A, Park M, Muallem S, Isakov N. Cloning, expression and functional characterization of the putative regeneration and tolerance factor (RTF/TJ6) as a functional vacuolar ATPase proton pump regulatory subunit with a conserved sequence of immunoreceptor tyrosine-based activation motif. Int Immunol 2005; 17:1303-1313.
10. Skinner MA, MacLaren LA, Wildeman, AG. Stage-dependent redistribution of the V-ATPase during bovine implantation. J Histochem Cytochem 1999; 47:1247-1254.
11. 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.
12. 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.
13. Derks RA, Beaman KD. Regeneration and tolerance factor prevents bystander T-cell death associated with human immunodeficiency virus infection. Clin Diagn Lab Immunol 2004; 11:835-840.
14. Kahlenberg JM, Dubyak GR. Mechanisms of caspase-1 activation by P2X7 receptor-mediated K+ release. Am J Physiol Cell Physiol 2004; 286:C1100-C1108.
15. Ntrivalas E, Derks R, Gilman-Sachs A, Kwak-Kim J, Levine R, Beaman KD. Novel role for the N-terminus domain of the a2 isoform of vacuolar ATPase in interleukin-1beta production. Hum Immunol 2007; 68:469- 477.
16. Kwong C, Sachs AG, Beaman KD. Tumor-associated a2 vacuolar ATPase acts as a key mediator of cancer-related inflammation by inducing protumorigenic properties in monocytes. J Immunol 2011; 186:1781-1789.
17. Critchley HO, Kelly RW, Lea RG, Drudy TA, Jones RL, Baird DT. Sex steroid regulation of leukocyte traffic in human decidua. Hum Reprod 1996; 11:2257-2262.
18. Jones RL, Kelly RW, Critchley HO. Chemokine and cyclooxygenase-2 expressions in human endometrium coincides with leukocyte accumulation. Hum Reprod 1997; 12:1300-1306.
19. Esplin MS, Romero R, Chaiworapongsa T, Kim YM, Edwin S, Gomez R, Mazor M, Adashi EY. Monocyte chemotactic protein-1 is increased in the amniotic fluid of women who deliver preterm in the presence or absence of intra-amniotic infection. J Matern Fetal Neonatal Med 2005; 17:365-373.
20. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008; 8:958-969.
21. Gustafsson C, Mjosberg J, Matussek A, Geffers R, Matthiesen L, Berg G, Sharma S, Buer J, Ernerudh J. Gene expression profiling of human decidual macrophages: evidence for immunosuppressive phenotype. PLoS One 3 2008; e2078.
22. Mor G, Abrahams VM. Potential role of macrophages as immunoregulators of pregnancy. Reprod Biol Endocrinol 2003; 1:119.
23. Hustin J, Jauniaux E, Schaaps JP. Histological study of the maternoembryonic interface in spontaneous abortion. Placenta 1990; 11:477-486.
24. Kadyrov M, Kingdom JC, Huppertz B. Divergent trophoblast invasion and apoptosis in placental bed spiral arteries from pregnancies complicated by maternal anemia and early-onset preeclampsia/intrauterine growth restriction. Am J Obstet Gynecol 2006; 194:557-563.
25. de Groot CJ, O'Brien TJ, Taylor RN. Biochemical evidence of impaired trophoblastic invasion of decidual stroma in women destined to have preeclampsia. Am J Obstet Gynecol 1996; 175:24-29.
26. Ball E, Bulmer JN, Ayis S, Lyall F, Robson SC. Late sporadic miscarriage is associated with abnormalities in spiral artery transformation and trophoblast invasion. J Pathol 2006; 208:535-542.
27. Clark DA, Manuel J, Lee L, Chaouat G, Gorczynski RM, Levy GA. Ecology of danger-dependent cytokine-boosted spontaneous abortion in the CBA x DBA/2 mouse model. I. Synergistic effect of LPS and (TNFalpha + IFN-gamma) on pregnancy loss. Am J Reprod Immunol 2004; 52:370-378.
28. 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.
29. Teixeira Gomes RC, Verna C, Nader HB, dos Santos Simoes R, Dreyfuss JL, Martins JR, Baracat EC, de Jesus Simões M, Soares JM Jr. Concentration and distribution of hyaluronic acid in mouse uterus throughout the estrous cycle. Fertil Steril 2009; 92:785-792.
30. Fujisaka S, Usui I, Bukhari A, Ikutani M, Oya T, Kanatani Y, Tsuneyama K, Nagai Y, Takatsu K, Urakaze M, Kobayashi M. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes 2009; 58:2574-2582.
31. Aron-Wisnewsky J, Tordjman J, Poitou C, Darakhshan F, Hugol D, Basdevant A, Aissat A, Guerre-Millo M, Clément K. Human adipose tissue macrophages: m1 and m2 cell surface markers in subcutaneous and omental depots and after weight loss. J Clin Endocrinol Metab 2009; 94:4619-4623.
32. Clark DA, Foerster K, Fung W, He L, Lee L, Mendicino M, Markert UR, Gorczynski RM, Marsden PA, Levy GA. The fgl2 prothrombinase/fibroleukin gene is required for lipopolysaccharide-triggered abortions and for normal mouse reproduction. Mol Hum Reprod 2004; 10:99-108.
33. Redecha P, van Rooijen N, Torry D, Girardi G. Pravastatin prevents miscarriages in mice: role of tissue factor in placental and fetal injury. Blood 2009; 113:4101-4109.
34. Marikawa Y, Alarcon VB. Establishment of trophectoderm and inner cell mass lineages in the mouse embryo. Mol Reprod Dev 2009; 76:1019- 1032.
35. Aplin JD. Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro. J Cell Sci 1991; 99:681-692.
36. Guvendag Guven ES, Okur H, Beksac MS. Placental fas/fas ligand expression in early pregnancy losses. Am J Reprod Immunol 2008; 60: 1-7.
37. Fitzgerald JS, Poehlmann TG, Schleussner E, Markert UR. Trophoblast invasion: the role of intracellular cytokine signalling via signal transducer and activator of transcription 3 (STAT3). Hum Reprod Update 2008; 14:335-344.
38. Bischof P, Campana A. A putative role for oncogenes in trophoblast invasion? Hum Reprod 2000; 15(suppl 6):51-58.
39. Ntrivalas E, Gilman-Sachs A, Kwak-Kim J, Beaman KD. 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.
40. 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.
41. Rubesa G, Beaman KD, Beer AE, Haller H, Rukavina D. Expression of membrane form of the pregnancy associated protein TJ6 on decidual lymphocytes in the first trimester of pregnancy. J Reprod Immunol 1996; 30:17-27.
42. Li Y, Cai L, Wang H, Wu P, Gu W, Chen Y, Hao H, Tang K, Yi P, Liu M, Miao S, Ye D. Pleiotropic regulation of macrophage polarization and tumorigenesis by formyl peptide receptor-2. Oncogene 2011; (in press). Published online ahead of print 18 April 2011; DOI 10.1038/onc.2011.112.
43. Robertson SA, Guerin LR, Bromfield JJ, Branson KM, Ahlstrom AC, Care AS. Seminal fluid drives expansion of the CD4+CD25+ T regulatory cell pool and induces tolerance to paternal alloantigens in mice. Biol Reprod 2009; 80:1036-1045.
44. Robertson SA, Sharkey DJ. The role of semen in induction of maternal immune tolerance to pregnancy. Semin Immunol 2001; 13:243-254.