Table of Contents
ISRN Obstetrics and Gynecology
Volume 2013, Article ID 504173, 9 pages
http://dx.doi.org/10.1155/2013/504173
Review Article

Placental Vacuolar ATPase Function Is a Key Link between Multiple Causes of Preeclampsia

1Department of Pathophysiology, Tongji Medical College, Huazhong University of Science and Technology, No. 13, Hangkong Road, Wuhan 430030, China
2Department of Dermatology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China
3Department of Dermatology, Cutaneous Biology Research Center, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02129, USA

Received 28 March 2013; Accepted 15 April 2013

Academic Editors: M. Friedrich, N. A. Ginsberg, C. Iavazzo, S. Palomba, and K. Yang

Copyright © 2013 Dongxin Zhang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Noris, N. Perico, and G. Remuzzi, “Mechanisms of disease: pre-eclampsia,” Nature Clinical Practice, vol. 1, no. 2, pp. 98–120, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. B. M. Sibai, “Diagnosis and management of gestational hypertension and preeclampsia,” Obstetrics and Gynecology, vol. 102, no. 1, pp. 181–192, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. K. Y. Lain and J. M. Roberts, “Contemporary concepts of the pathogenesis and management of preeclampsia,” Journal of the American Medical Association, vol. 287, no. 24, pp. 3183–3186, 2002. View at Google Scholar · View at Scopus
  4. C. W. Redman and I. L. Sargent, “Latest advances in understanding preeclampsia,” Science, vol. 308, no. 5728, pp. 1592–1594, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. C. W. G. Redman and I. L. Sargent, “Pre-eclampsia, the placenta and the maternal systemic inflammatory response—a review,” Placenta, vol. 24, pp. S21–S27, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. B. Schiessl, “Inflammatory response in preeclampsia,” Molecular Aspects of Medicine, vol. 28, no. 2, pp. 210–219, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. C. W. G. Redman and I. L. Sargent, “Placental debris, oxidative stress and pre-eclampsia,” Placenta, vol. 21, no. 7, pp. 597–602, 2000. View at Publisher · View at Google Scholar · View at Scopus
  8. J. B. Puschett, E. Agunanne, and M. N. Uddin, “Marinobufagenin, resibufogenin and preeclampsia,” Biochimica et Biophysica Acta, vol. 1802, no. 12, pp. 1246–1253, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Wang, S. Rana, and S. A. Karumanchi, “Preeclampsia: the role of angiogenic factors in its pathogenesis,” Physiology, vol. 24, no. 3, pp. 147–158, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. J. R. Challis, C. J. Lockwood, L. Myatt, J. E. Norman, J. F. Strauss, and F. Petraglia, “Inflammation and pregnancy,” Reproductive Sciences, vol. 16, no. 2, pp. 206–215, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Gennari-Moser, E. V. Khankin, and S. Schuller, “Regulation of placental growth by aldosterone and cortisol,” Endocrinology, vol. 152, no. 1, pp. 263–271, 2011. View at Google Scholar
  12. K. Duckitt and D. Harrington, “Risk factors for pre-eclampsia at antenatal booking: systematic review of controlled studies,” British Medical Journal, vol. 330, no. 7491, pp. 565–567, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Brewer, “Role of malnutrition in pre-eclampsia and eclampsia,” American Journal of Obstetrics and Gynecology, vol. 125, no. 2, pp. 281–282, 1976. View at Google Scholar · View at Scopus
  14. M. Forgac, “Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology,” Nature Reviews Molecular Cell Biology, vol. 8, no. 11, pp. 917–929, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. E. Ntrivalas, R. Levine, C. Kwong, A. Gilman-Sachs, and K. Beaman, “The a2 isoform of vacuolar ATPase is a modulator of implantation and feto-maternal immune tolerance in early pregnancy,” Journal of Reproductive Immunology, vol. 85, no. 1, pp. 106–111, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Qi, Y. Wang, and M. Forgac, “The vacuolar H+-ATPase: subunit arrangement and in vivo regulation,” Journal of Bioenergetics and Biomembranes, vol. 39, no. 5-6, pp. 423–426, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Babichev, A. Tamir, M. Park, S. Muallem, and N. Isakov, “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,” International Immunology, vol. 17, no. 10, pp. 1303–1313, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. E. Ntrivalas, A. Gilman-Sachs, J. Kwak-Kim, and K. Beaman, “The N-terminus domain of the a2 isoform of vacuolar ATPase can regulate interleukin-1β production from mononuclear cells in co-culture with JEG-3 choriocarcinoma cells,” American Journal of Reproductive Immunology, vol. 57, no. 3, pp. 201–209, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. M. K. Jaiswal, A. Gilman-Sachs, G. Chaouat, and K. D. Beaman, “Placental ATPase expression is a link between multiple causes of spontaneous abortion in mice,” Biology of Reproduction, vol. 85, no. 3, pp. 626–634, 2011. View at Google Scholar
  20. A. Nencioni and P. Brossart, “Crosspresentation: a matter of pH,” Blood, vol. 112, no. 12, pp. 4368–4369, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. R. A. Irani and Y. Xia, “The functional role of the renin-angiotensin system in pregnancy and preeclampsia,” Placenta, vol. 29, no. 9, pp. 763–771, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. R. A. Irani and Y. Xia, “Renin angiotensin signaling in normal pregnancy and preeclampsia,” Seminars in Nephrology, vol. 31, no. 1, pp. 47–58, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. F. Herse, R. Dechend, N. K. Harsem et al., “Dysregulation of the circulating and tissue-based renin-angiotensin system in preeclampsia,” Hypertension, vol. 49, no. 3, pp. 604–611, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. H. J. Singh, A. Rahman, E. T. Larmie, and A. Nila, “Raised prorenin and renin concentrations in pre-eclamptic placentae when measured after acid activation,” Placenta, vol. 25, no. 7, pp. 631–636, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. L. Anton, D. C. Merrill, L. A. A. Neves et al., “Activation of local chorionic villi angiotensin II levels but not angiotensin (1-7) in preeclampsia,” Hypertension, vol. 51, no. 4, pp. 1066–1072, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Kinouchi, A. Ichihara, M. Sano et al., “The (Pro)renin receptor/ATP6AP2 is essential for vacuolar H+-ATPase assembly in murine cardiomyocytes,” Circulation Research, vol. 107, no. 1, pp. 30–34, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. C. M. Cruciat, B. Ohkawara, S. P. Acebron et al., “Requirement of prorenin receptor and vacuolar H+-ATPase-mediated acidification for Wnt signaling,” Science, vol. 327, no. 5964, pp. 459–463, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. F. Rothenberger, A. Velic, P. A. Stehberger, J. Kovacikova, and C. A. Wagner, “Angiotensin II stimulates vacuolar H+-ATPase activity in renal acid-secretory intercalated cells from the outer medullary collecting duct,” Journal of the American Society of Nephrology, vol. 18, no. 7, pp. 2085–2093, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Winter, N. B. Kampik, and L. Vedovelli, “Aldosterone stimulates vacuolar H+-ATPase activity in renal acid-secretory intercalated cells mainly via a protein kinase C-dependent pathway,” American Journal of Physiology, vol. 301, no. 5, pp. C1251–C1261, 2011. View at Google Scholar
  30. D. C. A. Leite-Dellova, G. Malnic, and M. Mello-Aires, “Genomic and nongenomic stimulatory affect of aldosterone on H+-ATPase in proximal S3 segments,” American Journal of Physiology, vol. 300, no. 3, pp. F682–F691, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. D. Bikle, “Nonclassic actions of vitamin D,” Journal of Clinical Endocrinology and Metabolism, vol. 94, no. 1, pp. 26–34, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. M. F. Holick, “Medical progress: vitamin D deficiency,” The New England Journal of Medicine, vol. 357, no. 3, pp. 266–281, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. N. Q. Liu and M. Hewison, “Vitamin D, the placenta and pregnancy,” Archives of Biochemistry and Biophysics, vol. 523, no. 1, pp. 37–47, 2012. View at Google Scholar
  34. A. Halhali, A. R. Tovar, N. Torres, H. Bourges, M. Garabedian, and F. Larrea, “Preeclampsia is associated with low circulating levels of insulin-like growth factor I and 1,25-dihydroxyvitamin D in maternal and umbilical cord compartments,” Journal of Clinical Endocrinology and Metabolism, vol. 85, no. 5, pp. 1828–1833, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. L. Díaz, C. Arranz, E. Avila, A. Halhali, F. Vilchis, and F. Larrea, “Expression and activity of 25-hydroxyvitamin D-1α-hydroxylase are restricted in cultures of human syncytiotrophoblast cells from preeclamptic pregnancies,” Journal of Clinical Endocrinology and Metabolism, vol. 87, no. 8, pp. 3876–3882, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. J. R. Mora, M. Iwata, and U. H. Von Andrian, “Vitamin effects on the immune system: vitamins A and D take centre stage,” Nature Reviews Immunology, vol. 8, no. 9, pp. 685–698, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Saito, “Th17 cells and regulatory T cells: new light on pathophysiology of preeclampsia,” Immunology and Cell Biology, vol. 88, no. 6, pp. 615–617, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. F. J. Barrat, D. J. Cua, A. Boonstra et al., “In vitro generation of interleukin 10-producing regulatory CD4+ T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2-inducing cytokines,” Journal of Experimental Medicine, vol. 195, no. 5, pp. 603–616, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Joshi, L. C. Pantalena, and X. K. Liu, “1, 25-dihydroxyvitamin D(3) ameliorates Th17 autoimmunity via transcriptional modulation of interleukin-17A,” Molecular and Cellular Biology, vol. 31, no. 17, pp. 3653–3669, 2011. View at Google Scholar
  40. M. Kogawa, D. M. Findlay, P. H. Anderson et al., “Osteoclastic metabolism of 25(OH)-vitamin D3: a potential mechanism for optimization of bone resorption,” Endocrinology, vol. 151, no. 10, pp. 4613–4625, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Kinuta, H. Tanaka, T. Moriwake, K. Aya, S. Kato, and Y. Seino, “Vitamin D is an important factor in estrogen biosynthesis of both female and male gonads,” Endocrinology, vol. 141, no. 4, pp. 1317–1324, 2000. View at Publisher · View at Google Scholar · View at Scopus
  42. G. I. Gorodeski, “Effects of estrogen on proton secretion via the apical membrane in vaginal-ectocervical epithelial cells of postmenopausal women,” Menopause, vol. 12, no. 6, pp. 679–684, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Høyer-Hansen, S. P. Nordbrandt, and M. Jäättelä, “Autophagy as a basis for the health-promoting effects of vitamin D,” Trends in Molecular Medicine, vol. 16, no. 7, pp. 295–302, 2010. View at Google Scholar
  44. C. N. Serhan, N. Chiang, and T. E. van Dyke, “Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators,” Nature Reviews Immunology, vol. 8, no. 5, pp. 349–361, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. K. Tang, J. Liu, Z. Yang et al., “Microparticles mediate enzyme transfer from platelets to mast cells: a new pathway for lipoxin A4 biosynthesis,” Biochemical and Biophysical Research Communications, vol. 400, no. 3, pp. 432–436, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Hao, M. Liu, P. Wu et al., “Lipoxin A4 and its analog suppress hepatocellular carcinoma via remodeling tumor microenvironment,” Cancer Letters, vol. 309, no. 1, pp. 85–94, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Li, L. Cai, and H. Wang, “Pleiotropic regulation of macrophage polarization and tumorigenesis by formyl peptide receptor-2,” Oncogene, vol. 30, no. 36, pp. 3887–3899, 2011. View at Google Scholar
  48. D. Maldonado-Pérez, E. Golightly, F. C. Denison, H. N. Jabbour, and J. E. Norman, “A role for lipoxin A4 as anti-inflammatory and proresolution mediator in human parturition,” The FASEB Journal, vol. 25, no. 2, pp. 569–575, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. F. Lin, P. Zeng, and Z. Xu, “Treatment of Lipoxin A(4) and its analogue on low-dose endotoxin induced preeclampsia in rat and possible mechanisms,” Reproductive Toxicology, vol. 34, no. 4, pp. 677–685, 2012. View at Google Scholar
  50. J. Wang, Y. Huang, Y. Huang, J. Zhou, and X. Liu, “Effect of lipoxin A(4) on IL-1beta production of monocytes and its possible mechanism in severe preeclampsia,” Journal of Huazhong University of Science and Technology, vol. 30, no. 6, pp. 767–770, 2010. View at Google Scholar
  51. R. Russell, I. Gori, C. Pellegrini, R. Kumar, C. Achtari, and G. O. Canny, “Lipoxin A4 is a novel estrogen receptor modulator,” The FASEB Journal, vol. 25, no. 12, pp. 4326–4337, 2011. View at Google Scholar
  52. P. Maderna, D. C. Cottell, T. Toivonen et al., “FPR2/ALX receptor expression and internalization are critical for lipoxin A4 and annexin-derived peptide-stimulated phagocytosis,” The FASEB Journal, vol. 24, no. 11, pp. 4240–4249, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Recchi and P. Chavrier, “V-ATPase: a potential pH sensor,” Nature Cell Biology, vol. 8, no. 2, pp. 107–109, 2006. View at Publisher · View at Google Scholar · View at Scopus