Fetal membranes as an interface between inflammation and metabolism: Increased Aquaporin 9 expression in the presence of spontaneous labor at term and chorioamnionitis

References

• Haddad R, Tromp G, Kuivaniemi H, Chaiworapongsa T, Kim YM, Mazor M, Romero R. Human spontaneous labor without histologic chorioamnionitis is characterized by an acute inflammation gene expression signature. Am J Obstet Gynecol 2006;195:394-e1–394-e14.
   Google Scholar
• Lindstrom TM, Bennett PR. The role of nuclear factor kappa B in human labour. Reproduction 2005;130:569–581.
   PubMed Web of Science ®Google Scholar
• Peltier MR. Immunology of term and preterm labor. Reprod Biol Endocrinol 2003;1:122.
   PubMedGoogle Scholar
• Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel LA, Nien JK. Inflammation in preterm and term labour and delivery. Semin Fetal Neonatal Med 2006;11:317–326.
   PubMed Web of Science ®Google Scholar
• Chaiworapongsa T, Erez O, Kusanovic JP, Vaisbuch E, Mazaki-Tovi S, Gotsch F, Than NG, Mittal P, Kim YM, Camacho N, et al Amniotic fluid heat shock protein 70 concentration in histologic chorioamnionitis, term and preterm parturition. J Matern Fetal Neonatal Med 2008;21:449–461.
   PubMed Web of Science ®Google Scholar
• Gotsch F, Romero R, Chaiworapongsa T, Erez O, Vaisbuch E, Espinoza J, Kusanovic JP, Mittal P, Mazaki-Tovi S, Kim CJ, et al Evidence of the involvement of caspase-1 under physiologic and pathologic cellular stress during human pregnancy: a link between the inflammasome and parturition. J Matern Fetal Neonatal Med 2008;21:605–616.
   PubMed Web of Science ®Google Scholar
• Richani K, Soto E, Romero R, Espinoza J, Chaiworapongsa T, Nien JK, Edwin S, Kim YM, Hong JS, Mazor M. Normal pregnancy is characterized by systemic activation of the complement system. J Matern Fetal Neonatal Med 2005;17:239–245.
   PubMed Web of Science ®Google Scholar
• Esplin MS, Romero R, Chaiworapongsa T, Kim YM, Edwin S, Gomez R, Gonzalez R, Adashi EY. Amniotic fluid levels of immunoreactive monocyte chemotactic protein-1 increase during term parturition. J Matern Fetal Neonatal Med 2003;14:51–56.
   PubMedGoogle Scholar
• Hamill N, Romero R, Gotsch F, Pedro KJ, Edwin S, Erez O, Than NG, Mittal P, Espinoza J, Friel LA, et al Exodus-1 (CCL20): evidence for the participation of this chemokine in spontaneous labor at term, preterm labor, and intrauterine infection. J Perinat Med 2008;36:217–227.
   PubMed Web of Science ®Google Scholar
• Gilbert WM, Brace RA. The missing link in amniotic fluid volume regulation: intramembranous absorption. Obstet Gynecol 1989;74:748–754.
   PubMed Web of Science ®Google Scholar
• Beall MH, van den Wijngaard JP, van Gemert MJ, Ross MG. Regulation of amniotic fluid volume. Placenta 2007;28:824–832.
   PubMed Web of Science ®Google Scholar
• Beisel WR. Metabolic response to infection. Annu Rev Med 1975;26:9–20.
   PubMedGoogle Scholar
• Jovanovic L. Glucose and insulin requirements during labor and delivery: the case for normoglycemia in pregnancies complicated by diabetes. Endocr Pract 2004;10(Suppl 2):40–45.
   PubMedGoogle Scholar
• Kashyap ML, Sivasamboo R, Sothy SP, Cheah JS, Gartside PS. Carbohydrate and lipid metabolism during human labor: free fatty acids, glucose, insulin, and lactic acid metabolism during normal and oxytocin-induced labor for postmaturity. Metabolism 1976;25:865–875.
   PubMed Web of Science ®Google Scholar
• Maheux PC, Bonin B, Dizazo A, Guimond P, Monier D, Bourque J, Chiasson JL. Glucose homeostasis during spontaneous labor in normal human pregnancy. J Clin Endocrinol Metab 1996;81:209–215.
   PubMed Web of Science ®Google Scholar
• Whaley WH, Zuspan FP, Nelson GH, Ahlquist RP. Alterations of plasma free fatty acids and glucose during labor. Am J Obstet Gynecol 1967;97:875–880.
   PubMed Web of Science ®Google Scholar
• Mazaki-Tovi S, Romero R, Kusanovic JP, Erez O, Vaisbuch E, Gotsch F, Mittal P, Than GN, Nhan-Chang C, Chaiworapongsa T, et al Adiponectin multimers in maternal plasma. J Matern Fetal Neonatal Med 2008;21:796–815.
   PubMed Web of Science ®Google Scholar
• Gunasegaram R, Peh KL, Loganath A, Ng SC, Kottegoda SR, Ratnam SS. Cholesterol synthesizing enzymes in term human fetal amnion. J Perinat Med 1985;13:143–146.
   PubMedGoogle Scholar
• Kusanovic JP, Romero R, Mazaki-Tovi S, Chaiworapongsa T, Mittal P, Gotsch F, Erez O, Vaisbuch E, Edwin SS, Than NG, et al Resistin in amniotic fluid and its association with intra-amniotic infection and inflammation. J Matern Fetal Neonatal Med 2008;21:902–916.
   PubMed Web of Science ®Google Scholar
• Mazaki-Tovi S, Romero R, Kusanovic JP, Erez O, Gotsch F, Mittal P, Than NG, Nhan-Chang CL, Hamill N, Vaisbuch E, et al Visfatin/Pre-B cell colony-enhancing factor in amniotic fluid in normal pregnancy, spontaneous labor at term, preterm labor and prelabor rupture of membranes: an association with subclinical intrauterine infection in preterm parturition. J Perinat Med 2008;36:485–496.
   PubMed Web of Science ®Google Scholar
• Nien JK, Mazaki-Tovi S, Romero R, Erez O, Kusanovic JP, Gotsch F, Pineles BL, Gomez R, Edwin S, Mazor M, et al Plasma adiponectin concentrations in non-pregnant, normal and overweight pregnant women. J Perinat Med 2007;35:522–531.
   PubMed Web of Science ®Google Scholar
• Vaisbuch E, Mazaki-Tovi S, Kusanovic JP, Erez O, Than NG, Kim SK, Dong Z, Gotsch F, Mittal P, Chaiworapongsa T, et al Retinol binding protein 4: an adipokine associated with intra-amniotic infection/inflammation. J Matern Fetal Neonatal Med 2009 In press.
   Google Scholar
• Steingrimsdottir T, Ronquist G, Ulmsten U, Waldenstrom A. Low myometrial glycogen content compared with rectus muscle in term pregnant women before labor. Gynecol Obstet Invest 1999;47:166–171.
   PubMedGoogle Scholar
• Romero R, Espinoza J, Kusanovic JP, Gotsch F, Hassan S, Erez O, Chaiworapongsa T, Mazor M. The preterm parturition syndrome. BJOG 2006;113(Suppl 3):17–42.
   PubMed Web of Science ®Google Scholar
• Preston GM, Agre P. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc Natl Acad Sci USA 1991;88:11110–11114.
   PubMed Web of Science ®Google Scholar
• Liu H, Zheng Z, Wintour EM. Aquaporins and fetal fluid balance. Placenta 2008;29:840–847.
   PubMed Web of Science ®Google Scholar
• King LS, Kozono D, Agre P. From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 2004;5:687–698.
   PubMed Web of Science ®Google Scholar
• Agre P, Kozono D. Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett 2003;555:72–78.
   PubMed Web of Science ®Google Scholar
• Carbrey JM, Gorelick-Feldman DA, Kozono D, Praetorius J, Nielsen S, Agre P. Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver. Proc Natl Acad Sci USA 2003;100:2945–2950.
   PubMed Web of Science ®Google Scholar
• Rojek AM, Skowronski MT, Fuchtbauer EM, Fuchtbauer AC, Fenton RA, Agre P, Frokiaer J, Nielsen S. Defective glycerol metabolism in aquaporin 9 (AQP9) knockout mice. Proc Natl Acad Sci USA 2007;104:3609–3614.
   PubMed Web of Science ®Google Scholar
• Ishibashi K, Kuwahara M, Gu Y, Tanaka Y, Marumo F, Sasaki S. Cloning and functional expression of a new aquaporin (AQP9) abundantly expressed in the peripheral leukocytes permeable to water and urea, but not to glycerol. Biochem Biophys Res Commun 1998;244:268–274.
   PubMed Web of Science ®Google Scholar
• Wiegman MJ, Bullinger LV, Kohlmeyer MM, Hunter TC, Cipolla MJ. Regional expression of aquaporin 1, 4, and 9 in the brain during pregnancy. Reprod Sci 2008;15:506–516.
   PubMedGoogle Scholar
• Elkjaer M, Vajda Z, Nejsum LN, Kwon T, Jensen UB, miry-Moghaddam M, Frokiaer J, Nielsen S. Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem Biophys Res Commun 2000;276:1118–1128.
   PubMed Web of Science ®Google Scholar
• Aharon R, Bar-Shavit Z. Involvement of aquaporin 9 in osteoclast differentiation. J Biol Chem 2006;281:19305–19309.
   PubMedGoogle Scholar
• Damiano A, Zotta E, Goldstein J, Reisin I, Ibarra C. Water channel proteins AQP3 and AQP9 are present in syncytiotrophoblast of human term placenta. Placenta 2001;22:776–781.
   PubMed Web of Science ®Google Scholar
• Wang S, Chen J, Beall M, Zhou W, Ross MG. Expression of aquaporin 9 in human chorioamniotic membranes and placenta. Am J Obstet Gynecol 2004;191:2160–2167.
   PubMedGoogle Scholar
• Loitto VM, Forslund T, Sundqvist T, Magnusson KE, Gustafsson M. Neutrophil leukocyte motility requires directed water influx. J Leukoc Biol 2002;71:212–222.
   PubMed Web of Science ®Google Scholar
• Tromp G, Kuivaniemi H, Romero R, Chaiworapongsa T, Kim YM, Kim MR, Maymon E, Edwin S. Genome-wide expression profiling of fetal membranes reveals a deficient expression of proteinase inhibitor 3 in premature rupture of membranes. Am J Obstet Gynecol 2004;191:1331–1338.
   PubMed Web of Science ®Google Scholar
• Redline RW, Heller D, Keating S, Kingdom J. Placental diagnostic criteria and clinical correlation – a workshop report 140. Placenta 2005;26(Suppl A):S114–S117.
   PubMed Web of Science ®Google Scholar
• Pacora P, Chaiworapongsa T, Maymon E, Kim YM, Gomez R, Yoon BH, Ghezzi F, Berry SM, Qureshi F, Jacques SM, et al Funisitis and chorionic vasculitis: the histological counterpart of the fetal inflammatory response syndrome. J Matern Fetal Neonatal Med 2002;11:18–25.
   PubMedGoogle Scholar
• Redline RW. Inflammatory responses in the placenta and umbilical cord. Semin Fetal Neonatal Med 2006;11:296–301.
   PubMed Web of Science ®Google Scholar
• R Development Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing; http://cran.r-project.org/doc/manuals/refman.pdf
   Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001;25:402–408.
   PubMed Web of Science ®Google Scholar
• Winer J, Jung CK, Shackel I, Williams PM. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem 1999;270:41–49.
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 2001;125:279–284.
   PubMed Web of Science ®Google Scholar
• Gonen T, Walz T. The structure of aquaporins. Q Rev Biophys 2006;39:361–396.
   PubMed Web of Science ®Google Scholar
• Oliveira CA, Carnes K, Franca LR, Hermo L, Hess RA. Aquaporin-1 and -9 are differentially regulated by oestrogen in the efferent ductule epithelium and initial segment of the epididymis. Biol Cell 2005;97:385–395.
   PubMed Web of Science ®Google Scholar
• Pastor-Soler N, Isnard-Bagnis C, Herak-Kramberger C, Sabolic I, Van HA, Brown D, Breton S. Expression of aquaporin 9 in the adult rat epididymal epithelium is modulated by androgens. Biol Reprod 2002;66:1716–1722.
   PubMedGoogle Scholar
• Pietrement C, Da SN, Silberstein C, James M, Marsolais M, Van HA, Brown D, Pastor-Soler N, Ameen N, Laprade R, et al Role of NHERF1, cystic fibrosis transmembrane conductance regulator, and cAMP in the regulation of aquaporin 9. J Biol Chem 2008;283:2986–2996.
   PubMedGoogle Scholar
• Shengbiao W, Amidi F, Shengli Y, Beall M, Ross MG. Cyclic adenosine monophosphate regulation of aquaporin gene expression in human amnion epithelia. Reprod Sci 2007;14:234–240.
   PubMedGoogle Scholar
• Catalan V, Gomez-Ambrosi J, Pastor C, Rotellar F, Silva C, Rodriguez A, Gil MJ, Cienfuegos JA, Salvador J, Vendrell J, et al Influence of morbid obesity and insulin resistance on gene expression levels of AQP7 in visceral adipose tissue and AQP9 in liver. Obes Surg 2008;18:695–701.
   PubMed Web of Science ®Google Scholar
• Badaut J, Petit JM, Brunet JF, Magistretti PJ, Charriaut-Marlangue C, Regli L. Distribution of Aquaporin 9 in the adult rat brain: preferential expression in catecholaminergic neurons and in glial cells. Neuroscience 2004;128:27–38.
   PubMed Web of Science ®Google Scholar
• miry-Moghaddam M, Ottersen OP. The molecular basis of water transport in the brain. Nat Rev Neurosci 2003;4:991–1001.
   PubMed Web of Science ®Google Scholar
• Badaut J, Brunet JF, Petit JM, Guerin CF, Magistretti PJ, Regli L. Induction of brain aquaporin 9 (AQP9) in catecholaminergic neurons in diabetic rats. Brain Res 2008;1188:17–24.
   PubMedGoogle Scholar
• Anderson J, Brown N, Mahendroo MS, Reese J. Utilization of different aquaporin water channels in the mouse cervix during pregnancy and parturition and in models of preterm and delayed cervical ripening. Endocrinology 2006;147:130–140.
   PubMed Web of Science ®Google Scholar
• Anderson D, Yang Q, Hohimer A, Faber J, Giraud G, Davis L. Intramembranous absorption rate is unaffected by changes in amniotic fluid composition. Am J Physiol Renal Physiol 2005;288:F964–F968.
   Google Scholar
• Mann SE, Ricke EA, Yang BA, Verkman AS, Taylor RN. Expression and localization of aquaporin 1 and 3 in human fetal membranes. Am J Obstet Gynecol 2002;187:902–907.
   PubMedGoogle Scholar
• Wang S, Kallichanda N, Song W, Ramirez BA, Ross MG. Expression of aquaporin-8 in human placenta and chorioamniotic membranes: evidence of molecular mechanism for intramembranous amniotic fluid resorption. Am J Obstet Gynecol 2001;185:1226–1231.
   PubMedGoogle Scholar
• Wang S, Amidi F, Beall M, Gui L, Ross MG. Aquaporin 3 expression in human fetal membranes and its up-regulation by cyclic adenosine monophosphate in amnion epithelial cell culture. J Soc Gynecol Investig 2006;13:181–185.
   PubMedGoogle Scholar
• Beall MH, Wang S, Yang B, Chaudhri N, Amidi F, Ross MG. Placental and membrane aquaporin water channels: correlation with amniotic fluid volume and composition. Placenta 2007;28:421–428.
   PubMed Web of Science ®Google Scholar
• Lindsay LA, Murphy CR. Aquaporins are upregulated in glandular epithelium at the time of implantation in the rat. J Mol Histol 2007;38:87–95.
   PubMed Web of Science ®Google Scholar