Journal of Reproductive Immunology
Volume 85, Issue 1 , Pages 106-111 , May 2010

The a2 isoform of vacuolar ATPase is a modulator of implantation and feto-maternal immune tolerance in early pregnancy

Received 26 August 2009 ,Revised 22 October 2009 ,Accepted 27 October 2009.

References 

  1. Aplin JD, Kimber SJ. Trophoblast–uterine interactions at implantation. Reprod. Biol. Endocrinol. 2004;2:48
  2. Arck P, Hansen PJ, Mulac Jericevic B, Piccinni MP, Szekeres-Bartho J. Progesterone during pregnancy: endocrine-immune cross talk in mammalian species and the role of stress. Am. J. Reprod. Immunol. 2007;58:268–279
  3. Babawale MO, Mobberley MA, Ryder TA, Elder MG, Sullivan MH. Ultrastructure of the early human feto-maternal interface co-cultured in vitro. Hum. Reprod. 2002;17:1351–1357
  4. 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
  5. Beaman K, Angkachatchai V, Gilman-Sachs A. TJ6: the pregnancy-associated cytokine. Am. J. Reprod. Immunol. 1996;35:338–341
  6. Brown D, Lui B, Gluck S, Sabolic I. A plasma membrane proton ATPase in specialized cells of rat epididymis. Am. J. Physiol. 1992;263:C913–C916
  7. Brown D, Smith PJ, Breton S. Role of V-ATPase-rich cells in acidification of the male reproductive tract. J. Exp. Biol. 1997;200:257–262
  8. 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
  9. Dudimah FD, Gibson C, Whalen MM. Effect of dibutyltin on ATP levels in human natural killer cells. Environ. Toxicol. 2007;22:117–123
  10. Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell. Biol. 2007;8:917–929
  11. Gorodeski GI. Effects of estrogen on proton secretion via the apical membrane in vaginal-ectocervical epithelial cells of postmenopausal women. Menopause. 2005;12:679–684
  12. Herak-Kramberger CM, Breton S, Brown D, Kraus O, Sabolic I. Distribution of the vacuolar H+ ATPase along the rat and human male reproductive tract. Biol. Reprod. 2001;64:1699–1707
  13. Inoue H, Noumi T, Nagata M, Murakami H, Kanazawa H. Targeted disruption of the gene encoding the proteolipid subunit of mouse vacuolar H(+)-ATPase leads to early embryonic lethality. Biochim. Biophys. Acta. 1999;1413:130–138
  14. Kammerer U, von Wolff M, Markert UR. Immunology of human endometrium. Immunobiology. 2004;209:569–574
  15. Kanellopoulos-Langevin C, Caucheteux M, Verbeke P, Ojcius D. Tolerance of the fetus by the maternal immune system: role of inflammatory mediators at the feto-maternal interface. Reprod. Biol. Endocrinol. 2003;1:121–126
  16. Kang JA, McBey BA, Angkachatchai V, Croy BA, Beaman KD. Expression of TJ6 during pregnancy. Am. J. Reprod. Immunol. 1997;38:183–188
  17. King A, Burrows T, Verma S, Hiby S, Loke YW. Human uterine lymphocytes. Hum. Reprod. Update. 1998;4:480–485
  18. Lattuada D, Mangioni S, Vigano P, Ntrivalas EI, Rossi M, Palotti F, et al. 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
  19. 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
  20. Lee GW, Boomer JS, Gilman-Sachs A, Chedid A, Gudelj L, Rukavina D, et al. Regeneration and tolerance factor of the human placenta induces IL-10 production. Eur. J. Immunol. 2001;31:687–691
  21. Lettau M, Schmidt H, Kabelitz D, Janssen O. Secretory lysosomes and their cargo in T and NK cells. Immunol. Lett. 2007;108:10–19
  22. Levine RF, Derks R, Beaman K. Regeneration and tolerance factor, A vacuolar ATPase with consequences. Chem. Immunol. Allergy. 2005;89:126–134
  23. Marshansky V. The V-ATPase a2-subunit as a putative endosomal pH-sensor. Biochem. Soc. Trans. 2007;35:1092–1099
  24. Nishi T, Forgac M. The vacuolar (H+)-ATPases–nature's most versatile proton pumps. Nat. Rev. Mol. Cell. Biol. 2002;3:94–103
  25. 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
  26. 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
  27. Orange JS. Formation and function of the lytic NK-cell immunological synapse. Nat. Rev. Immunol. 2008;8:713–725
  28. Qi J, Wang Y, Forgac M. The vacuolar (H+)-ATPase: subunit arrangement and in vivo regulation. J. Bioenerg. Biomembr. 2007;39:423–426
  29. 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
  30. Robertson S, Seamark RF, Guilbert LJ, Wegmann TG. The role of cytokines in gestation. Crit. Rev. Immunol. 1994;14:239–292
  31. 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
  32. Saito S. Cytokine cross-talk between mother and embryo-placenta. J. Reprod. Immunol. 2001;52:15–33
  33. Seki H, Zosmer A, Elder MG, Sullivan MH. The regulation of progesterone and hCG production from placental cells by interleukin-1beta. Biochim. Biophys. Acta. 1997;1336:342–348
  34. Skinner MA, MacLaren LA, Wildeman AG. Stage-dependent redistribution of the V-ATPase during bovine implantation. J. Histochem. Cytochem. 1999;47:1247–1254
  35. Spaggiari GM, Contini P, Negrini S, Dondero A, Carosio R, Ghio M, et al. IFN-gamma production in human NK cells through the engagement of CD8 by soluble or surface HLA class I molecules. Eur. J. Immunol. 2003;33:3049–3059
  36. 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
  37. Sun-Wada GH, Imai-Senga Y, Yamamoto A, Murata Y, Hirata T, Wada Y, et al. A proton pump ATPase with testis-specific E1-subunit isoform required for acrosome acidification. J. Biol. Chem. 2002;277:18098–18105
  38. Sun-Wada GH, Toyomura T, Murata Y, Yamamoto A, Futai M, Wada Y. The a3 isoform of V-ATPase regulates insulin secretion from pancreatic beta-cells. J. Cell. Sci. 2006;119:4531–4540
  39. Yoshinaga K. Review of factors essential for blastocyst implantation for their modulating effects on the maternal immune system. Semin. Cell. Dev. Biol. 2008;19:161–169
  40. Young JE, Friedman CI, Danforth DR. Interleukin-1 beta modulates prostaglandin and progesterone production by primate luteal cells in vitro. Biol. Reprod. 1997;56:663–667

PII: S0165-0378(09)00549-X

doi: 10.1016/j.jri.2009.10.010

Journal of Reproductive Immunology
Volume 85, Issue 1 , Pages 106-111 , May 2010