Nutritional and Physiological Regulation of Water Transport in the Conceptus.
Aquaporin
Conceptus
Fetal membrane
Nutrition
Placenta
Water transport
Journal
Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103
Informations de publication
Date de publication:
2022
2022
Historique:
entrez:
22
11
2021
pubmed:
23
11
2021
medline:
25
11
2021
Statut:
ppublish
Résumé
Water transport during pregnancy is essential for maintaining normal growth and development of conceptuses (embryo/fetus and associated membranes). Aquaporins (AQPs) are a family of small integral plasma membrane proteins that primarily transport water across the plasma membrane. At least 11 isoforms of AQPs (AQPs 1-9, 11, and 12) are differentially expressed in the mammalian placenta (amnion, allantois, and chorion), and organs (kidney, lung, brain, heart, and skin) of embryos/fetuses during prenatal development. Available evidence suggests that the presence of AQPs in the conceptus mediates water movement across the placenta to support the placentation, the homeostasis of amniotic and allantoic fluid volumes, as well as embryonic and fetal survival, growth and development. Abundances of AQPs in the conceptus can be modulated by nutritional status and physiological factors affecting the pregnant female. Here, we summarize the effects of maternal dietary factors (such as intakes of protein, arginine, lipids, all-trans retinoic acid, copper, zinc, and mercury) on the expression of AQPs in the conceptus. We also discuss the physiological changes in hormones (e.g., progesterone and estrogen), oxygen supply, nitric oxide, pH, and osmotic pressure associated with the regulation of fluid exchange between mother and fetus. These findings may help to improve the survival, growth, and development of embryo/fetus in livestock species and other mammals (including humans).
Identifiants
pubmed: 34807439
doi: 10.1007/978-3-030-85686-1_6
doi:
Substances chimiques
Aquaporins
0
Water
059QF0KO0R
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
109-125Informations de copyright
© 2022. Springer Nature Switzerland AG.
Références
Agre P, Kozono D (2003) Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett 555:72–78
pubmed: 14630322
Agren J, Sjors G, Sedin G (1998) Transepidermal water loss in infants born at 24 and 25 weeks of gestation. Acta Paediatr 87:1185–1190
pubmed: 9846922
Agren J, Zelenin S, Hakansson M, Eklof AC, Aperia A, Nejsum LN, Nielsen S, Sedin G (2003) Transepidermal water loss in developing rats: role of aquaporins in the immature skin. Pediatr Res 53:558–565
pubmed: 12612219
Alejandra R, Natalia S, Alicia ED (2018) The blocking of aquaporin-3 (AQP3) impairs extravillous trophoblast cell migration. Biochem Biophys Res Commun 499:227–232
pubmed: 29567477
Aralla M, Mobasheri A, Groppetti D, Cremonesi F, Arrighi S (2012) Expression of aquaporin water channels in canine fetal adnexa in respect to the regulation of amniotic fluid production and absorption. Placenta 33:502–510
pubmed: 22425592
Baum MA, Ruddy MK, Hosselet CA, Harris HW (1998) The perinatal expression of aquaporin-2 and aquaporin-3 in developing kidney. Pediatr Res 43:783–790
pubmed: 9621988
Bazer FW (1989) Allantoic fluid: regulation of volume and composition. In: Brace RA (ed) Fetal and neonatal body fluids. Perinatology Press, Cornell, NY, pp 135–157
Bazer FW, Spencer TE, Johnson GA, Burghardt RC, Wu G (2009) Comparative aspects of implantation. Reproduction 138:195–209
pubmed: 19502456
Bazer FW, Johnson GA, Wu G (2015) Amino acids and conceptus development during the peri-implantation period of pregnancy. Adv Exp Med Biol 843:23–52
pubmed: 25956294
Beall MH, Wang S, Yang B, Chaudhri N, Amidi F, Ross MG (2007) Placental and membrane aquaporin water channels: correlation with amniotic fluid volume and composition. Placenta 28:421–428
pubmed: 16870248
Belkacemi L, Desai M, Beall MH, Liu Q, Lin JT, Nelson DM, Ross MG (2011) Early compensatory adaptations in maternal undernourished pregnancies in rats: role of the aquaporins. J Matern Fetal Neonatal Med 24:752–759
pubmed: 20958229
Bouvier D, Rouzaire M, Marceau G, Prat C, Pereira B, Lemarié R, Deruelle P, Fajardy I, Gallot D, Blanchon L, Vambergue A, Sapin V (2015) Aquaporins and fetal Membranes from diabetic parturient women: expression abnormalities and regulation by insulin. J Clin Endocrinol Metab 100:E1270–1279
Brañes MC, Morales B, Ríos M, Villalón MJ (2005) Regulation of the immunoexpression of aquaporin 9 by ovarian hormones in the rat oviductal epithelium. Am J Physiol 288:C1048–1057
Breenan DM, Zarrow MX (1959) Water and electrolyte content of the uterus of the intact and adrenalectomized rat treated with relaxin and various steroid hormones. Endocrinology 64:907–913
pubmed: 13652907
Butkus A, Alcorn D, Earnest L, Moritz K, Giles M, Wintour EM (1997) Expression of aquaporin-1 (AQP1) in the adult and developing sheep kidney. Biol Cell 89:313–320
pubmed: 9468602
Butkus A, Earnest L, Jeyaseelan K, Moritz K, Johnston H, Tenis N, Wintour EM (1999) Ovine aquaporin-2: cDNA cloning, ontogeny and control of renal gene expression. Pediatr Nephrol 13:379–390
pubmed: 10412857
Cao Z, Xu T, Tong X, Wang Y, Zhang D, Gao D, Zhang L, Ning W, Qi X, Ma Y, Yu T, Knott JG, Zhang Y (2019) Maternal yes-associated protein participates in porcine blastocyst development via modulation of trophectoderm epithelium barrier function. Cells 8:1606
pmcid: 6952962
Castro Parodi M, Farina M, Dietrich V, Abán C, Szpilbarg N, Zotta E, Damiano AE (2011) Evidence for insulin-mediated control of AQP9 expression in human placenta. Placenta 32:1050–1056
pubmed: 22018417
Castro-Parodi M, Farina M, Dietrich V, Levi LN, Ibarra C, Damiano AE (2008) Dose dependent insulin-mediated regulation of AQP9 in human placenta. Placenta 29:120
Castro-Parodi M, Levi L, Dietrich V, Zotta E, Damiano AE (2009) CFTR may modulate AQP9 functionality in preeclamptic placentas. Placenta 30:642–648
pubmed: 19481256
Castro-Parodi M, Szpilbarg N, Dietrich V, Sordelli M, Reca A, Abán C, Maskin B, Farina MG, Damiano AE (2013) Oxygen tension modulates AQP9 expression in human placenta. Placenta 34:690–698
pubmed: 23684380
Cheung CY, Anderson DF, Brace RA (2016) Aquaporins in ovine amnion: responses to altered amniotic fluid volumes and intramembranous absorption rates. Physiol Rep 4:e12868
Cheung CY, Roberts VHJ, Frias AE, Brace RA (2018) High-fat diet effects on amniotic fluid volume and amnion aquaporin expression in non-human primates. Physiol Rep 6:e13792
Cheung CY, Anderson DF, Rouzaire M, Blanchon L, Sapin V, Brace RA (2019) Retinoic acid pathway regulation of vascular endothelial growth factor in ovine amnion. Reprod Sci 26:1351–1359
pubmed: 29587617
Chinigarzadeh A, Muniandy S, Salleh N (2017) Combinatorial effect of genistein and female sex-steroids on uterine fluid volume and secretion rate and aquaporin (AQP)-1, 2, 5, and 7 expression in the uterus in rats. Environ Toxicol 32:832–844
pubmed: 27235753
Cornock R, Langley-Evans SC, Mobasheri A, McMullen S (2010) The impact of maternal protein restriction during rat pregnancy upon renal expression of angiotensin receptors and vasopressin-related aquaporins. Reprod Biol Endocrinol 8:105
pubmed: 20807409
pmcid: 2940793
Damiano AE (2011) Review: water channel proteins in the human placenta and fetal membranes. Placenta 32(Suppl. 2):S207–S211
pubmed: 21208655
Damiano AE (2020) Chapter fifteen—aquaporins during pregnancy. Vitam Horm 112:327–355
pubmed: 32061348
Damiano AE, Zotta E, Ibarra C (2006) Functional and molecular expression of AQP9 channel and UT-A transporter in normal and preeclamptic human placentas. Placenta 27:1073–1081
pubmed: 16480766
Damiano AE, Zotta E, Goldstein J, Reisin I, Ibarra C (2001) Water channel proteins AQP3 and AQP9 are present in syncytiotrophoblast of human term placenta. Placenta 22:776–781
pubmed: 11597198
De Falco M, Cobellis L, Torella M, Acone G, Varano L, Sellitti A, Ragucci A, Coppola G, Cassandro R, Laforgia V, Varano L, De Luca A (2007) Down-regulation of aquaporin 4 in human placenta throughout pregnancy. In Vivo 21:813–817
de Oliveira V, Schaefer J, Abu-Rafea B, Vilos GA, Vilos AG, Bhattacharya M, Radovick S, Babwah AV (2020) Uterine aquaporin expression is dynamically regulated by estradiol and progesterone and ovarian stimulation disrupts embryo implantation without affecting luminal closure. Mol Hum Reprod 26:154–166
pubmed: 31977023
pmcid: 7103570
Devuyst O, Burrow CR, Smith BL, Agre P, Knepper MA, Wilson PD (1996) Expression of aquaporins-1 and -2 during nephrogenesis and in autosomal dominant polycystic kidney disease. Am J Physiol 271:F169–F183
Dietrich V, Damiano AE (2015) Activity of Na
pubmed: 26470817
Dillon EL, Wu G (2021) Cortisol enhances ctrulline synthesis from proline in enterocytes of suckling piglets. Amino Acids. http://doi.org/10.1007/s00726-021-03039-y
Ducza E, Csányi A, Gáspár R (2017) Aquaporins during pregnancy: their function and significance. Int J Mol Sci 18:2593
pmcid: 5751196
Escobar J, Gormaz M, Arduini A, Gosens K, Martinez A, Perales A, Escrig R, Tormos E, Roselló M, Orellana C, Vento M (2012) Expression of aquaporins early in human pregnancy. Early Hum Dev 88:589–594
pubmed: 22336497
Faber JJ, Anderson DF (2010) The placenta in the integrated physiology of fetal volume control. Int J Dev Biol 54:391–396
pubmed: 19876827
pmcid: 3402164
Gao H (2020) Amino acids in reproductive nutrition and health. Adv Exp Med Biol 1265:111–131
pubmed: 32761573
Gao K, Jiang Z, Lin Y, Zheng C, Zhou G, Chen F, Yang L, Wu G (2012) Dietary L-arginine supplementation enhances placental growth and reproductive performance in sows. Amino Acids 42:2207–2214
pubmed: 21691753
Geisert RD, Thatcher WW, Roberts RM, Bazer FW (1982) Establishment of pregnancy in the pig: III. Endometrial secretory response to estradiol valerate administered on day 11 of the estrous cycle. Biol Reprod 27:957–965
pubmed: 7171674
Gilbreath KR, Bazer FW, Satterfield MC, Wu G (2021) Amino acid nutrition and reproductive performance in ruminants. Adv Exp Med Biol 1285:43–61
pubmed: 33770402
Gömöri E, Pál J, Abrahám H, Vajda Z, Sulyok E, Seress L, Dóczi T (2006) Fetal development of membrane water channel proteins aquaporin-1 and aquaporin-4 in the human brain. Int J Dev Neurosci 24:295–305
pubmed: 16814974
Herring CM, Bazer FW, Johnson GA, Wu G (2018a) Impacts of maternal dietary protein intake on fetal survival, growth, and development. Exp Biol Med (Maywood) 243:525–533
Herring CM, Hu S, Bazer FW, Johnson GA, Seo H, Kramer A, McLendon B, Elmetwally M, Wu G (2018b) Dietary supplementation of 0.4% L-arginine between days 14 and 30 of gestation stimulates placental transport of water in gilts. In: Society of the study of reproduction annual meeting, July 10–13, 2018. New Orleans, LA
Hu SD, He WL, Wu G (2021) Hydroxyproline in animal metabolism, nutrition, and cell signaling. Amino Acids. http://doi.org/10.1007/s00726-021-03056-x
Hung TH, Burton GJ (2006) Hypoxia and reoxygenation: a possible mechanism for placental oxidative stress in preeclampsia. Taiwan J Obstet Gynecol 45:189–200
pubmed: 17175463
Ishibashi K (2009) New members of mammalian aquaporins: AQP10-AQP12. Handbook Exp Pharmacol 190:251–262
Ishibashi K, Hara S, Kondo S (2009) Aquaporin water channels in mammals. Clin Exp Nephrol 13:107–117
pubmed: 19085041
Jablonski EM, McConnell NA, Hughes FM Jr, Huet-Hudson YM (2003) Estrogen regulation of aquaporins in the mouse uterus: potential roles in uterine water movement. Biol Reprod 69:1481–1487
pubmed: 12855592
Jauniaux E, Johnson MR, Jurkovic D, Ramsay B, Campbell S, Meuris S (1994) The role of relaxin in the development of the uteroplacental circulation in early pregnancy. Obstetr Gynecol 84:338–342
Jiang SS, Zhu XJ, Ding SD, Wang JJ, Jiang LL, Jiang WX, Zhu XQ (2012) Expression and localization of aquaporins 8 and 9 in term placenta with oligohydramnios. Reprod Sci 19:1276–1284
pubmed: 22872487
Jiang XX, Wei FX, Zhao L, Ye XL, Xin LB, Qu Y, Wu RJ, Lin J (2015) Aquaporin 5 plays a role in estrogen-induced ectopic implantation of endometrial stromal cells in endometriosis. PLoS One 10:e0145290
Johansson M, Glazier JD, Sibley CP, Jansson T, Powell TL (2002) Activity and protein expression of the Na
pubmed: 12466372
Johnston H, Koukoulas I, Jeyaseelan K, Armugam A, Earnest L, Baird R, Dawson N, Ferraro T, Wintour EM (2000) Ontogeny of aquaporins 1 and 3 in ovine placenta and fetal membranes. Placenta 21:88–99
pubmed: 10692256
King LS, Nielsen S, Agre P (1997) Aquaporins in complex tissues. I. developmental patterns in respiratory and glandular tissues of rat. Am J Phys 273:C1541–C1548
Kitchen P, Day RE, Salman MM, Conner MT, Bill RM, Conner AC (2015) Beyond water homeostasis: diverse functional roles of mammalian aquaporins. Biochim Biophys Acta 1850:2410–2421
pubmed: 26365508
Knight JW, Bazer FW, Thatcher WW, Franke DE, Wallace HD (1977) Conceptus development in intact and unilaterally hysterectomized-ovariectomized gilts: interrelationships among hormonal status, placental development, fetal fluids and fetal growth. J Anim Sci 44:620–637
pubmed: 853021
Kobayashi M, Takahashi E, Miyagawa S, Watanabe H, Iguchi T (2006) Chromatin immunoprecipitation-mediated target identification proved aquaporin 5 is regulated directly by estrogen in the uterus. Genes Cells:1133–1143
Kordowitzki P, Kranc W, Bryl R, Kempisty B, Skowronska A, Skowronski MT (2020) The relevance of aquaporins for the physiology, pathology, and aging of the female reproductive system in mammals. Cells 9:2570
pmcid: 7760214
Li XL, Bazer FW, Johnson GA, Burghardt RC, Frank JW, Dai ZL, Wang JJ, Wu ZL, Shinzato I, Wu GY (2014) Dietary supplementation with L-arginine between days 14 and 25 of gestation enhances embryonic development and survival in gilts. Amino Acids 46:375–384
pubmed: 24337831
Lindsay LA, Murphy C (2006) Redistribution of aquaporins 1 and 5 in the rat uterus is dependent on progesterone: a study with light and electron microscopy. Reproduction 131:369–378
pubmed: 16452730
Liu C, Morrisey EE, Whitsett JA (2002) GATA-6 is required for maturation of the lung in late gestation. Am J Physiol 283:L468–L475
Liu H, Hooper SB, Armugam A, Dawson N, Ferraro T, Jeyaseelan K, Thiel A, Koukoulas I, Wintour EM (2003) Aquaporin gene expression and regulation in the ovine fetal lung. J Physiol 551:503–514
pubmed: 12819302
pmcid: 2343212
Liu H, Koukoulas I, Ross MC, Wang S, Wintour EM (2004) Quantitative comparison of placental expression of three aquaporin genes. Placenta 25:475–478
pubmed: 15135229
Liu H, Zheng Z, Wintour EM (2008) Aquaporins and fetal fluid balance. Placenta 29:840–847
pubmed: 18783826
Liu XM, Zhang D, Wang TT, Sheng JZ, Huang HF (2014) Ion/water channels for embryo implantation barrier. Physiology (Bethesda) 29:186–195
Luo H, Xie A, Hua Y, Wang J, Liu Y, Zhu X (2018) Aquaporin 1 gene deletion affects the amniotic fluid volume and composition as well as the expression of other aquaporin water channels in placenta and fetal membranes. Clin Chim Acta 482:161–165
pubmed: 29626438
Ma T, Yang B, Verkman AS (1997) Cloning of a novel water and urea-permeable aquaporin from mouse expressed strongly in colon, placenta, liver, and heart. Biochem Biophys Res Commun 240:324–328
pubmed: 9388476
Mann SE, Ricke EA, Yang BA, Verkman AS, Taylor RN (2002) Expression and localization of aquaporin 1 and 3 in human fetal membranes. Am J Obstet Gynecol 187:902–907
pubmed: 12388974
Mann SE, Ricke EA, Torres EA, Taylor RN (2005) A novel model of polyhydramnios: amniotic fluid volume is increased in aquaporin 1 knockout mice. Am J Obstet Gynecol 192:2041–2046
pubmed: 15970890
Marino G, Castro-Parodi M, Dietrich V, Damiano AE (2010) High levels of human chorionic gonadotropin (HCG) may increase aquaporin-9 (AQP9) expression in human preeclamptic placenta. Reprod Sci 17:444–453
pubmed: 20220109
Martínez N, Damiano AE (2017) Aquaporins in fetal development. Adv Exp Med Biol 969:199–212
pubmed: 28258575
Meli R, Pirozzi C, Pelagalli A (2018) New perspectives on the potential role of aquaporins (AQPs) in the physiology of inflammation. Front Physiol 16(9):101
Millar LK, Reiny R, Yamamoto SY, Okazaki K, Webster L, Bryant-Greenwood GD (2003) Relaxin causes proliferation of human amniotic epithelium by stimulation of insulin-like growth factor-II. Am J Obstetr Gynecol 188:234–241
Modena AB, Fieni S (2004) Amniotic fluid dynamics. Acta Biomed 75(Suppl 1):11–13
pubmed: 15301282
Moen V, Brudin L, Tjernberg I, Rundgren M, Irestedt L (2018) Feto-maternal osmotic balance at term. A prospective observational study. J Perinat Med 46:183–189
pubmed: 28862988
Németh-Cahalan KL, Kalman K, Froger A, Hall JE (2007) Zinc modulation of water permeability reveals that aquaporin 0 functions as a cooperative tetramer. J Gen Physiol 130:457–464
pubmed: 17938229
pmcid: 2151666
Nico B, Frigeri A, Nicchia GP, Quondamatteo F, Herken R, Errede M, Ribatti D, Svelto M, Roncali L (2001) Role of aquaporin-4 water channel in the development and integrity of the blood-brain barrier. J Cell Sci 114:1297–1307
pubmed: 11256996
Offenberg H, Barcroft LC, Caveney A, Viuff D, Thomsen PD, Watson AJ (2000) mRNAs encoding aquaporins are present during murine preimplantation development. Mol Reprod Dev 57:323–330
pubmed: 11066060
Parry LJ, Vodstrcil LA (2007) Relaxin physiology in the female reproductive tract during pregnancy. Adv Exp Med Biol 612:34–48
pubmed: 18161480
Pérez-Pérez A, Maymó JL, Gambino YP, Guadix P, Dueñas JL, Varone CL, Sánchez-Margalet V (2013) Activated translation signaling in placenta from pregnant women with gestational diabetes mellitus: possible role of leptin. Horm Metab Res 45:436–442
pubmed: 23386416
Pérez-Pérez A, Vilariño-García T, Guadix P, Dueñas JL, Sánchez-Margalet V (2020a) Leptin and nutrition in gestational diabetes. Nutrients 12:1970
Pérez-Péreza A, Vilariño-Garcíaa T, Dietrich V, Guadixc P, Dueñasc JL, Varone CL, Damiano AE, Sánchez-Margalet V (2020b) Aquaporins and placenta. Vitam Horm 112:311–326
Prat C, Blanchon L, Borel V, Gallot D, Herbet A, Bouvier D, Marceau G, Sapin V (2012) Ontogeny of aquaporins in human fetal membranes. Biol Reprod 86:48
pubmed: 22053096
Prat C, Bouvier D, Comptour A, Marceau G, Belville C, Clairefond G, Blanc P, Gallot D, Blanchon L, Sapin V (2015) All-trans-retinoic acid regulates aquaporin-3 expression and related cellular membrane permeability in the human amniotic environment. Placenta 36:881–887
pubmed: 26045060
Qi HB, Li L, Zong WJ, Hyer BJ, Huang J (2009) Expression of aquaporin 8 is diversely regulated by osmotic stress in amnion epithelial cells. J Obstet Gynaecol 35:1019–1025
Reppetti J, Reca A, Seyahian E, Medina Y, Martínez N, Szpilbarg N, Damiano AE (2020) Intact caveolae are required for proper extravillous trophoblast migration and differentiation. J Cell Physiol 235:3382–3392
pubmed: 31541456
Richard C, Gao J, Brown N, Reese J (2013) Aquaporin water channel genes are differentially expressed and regulated by ovarian steroids during the periimplantation period in the mouse. Endocrinology 144:1533–1541
Schneider H (1991) Placental transport function. Reprod Fertil Dev 3:345–353
pubmed: 1957022
Seo MJ, Lim JH, Kim DH, Bae HR (2018) Loss of aquaporin-3 in placenta and fetal membranes induces growth restriction in mice. Dev Reprod 22:263–273
pubmed: 30324163
pmcid: 6182233
Seo H, Li XL, Wu G, Bazer FW, Burghardt RC, Bayless KJ, Johnson GA (2020) Mechanotransduction drives morphogenesis to develop folding during placental development in pigs. Placenta 90:62–70
pubmed: 32056554
Sha XY, Xiong ZF, Liu HS, Di XD, Ma TH (2011a) Maternal-fetal fluid balance and aquaporins: from molecule to physiology. Acta Pharmacol Sin 32:716–720
Sha XY, Xiong ZF, Liu HS (2011b) Pregnant phenotype in aquaporin 8-deficient mice. Acta Pharmacol Sin 32:840–844
Sha XY, Liu HS, Ma TH (2015) Osmotic water permeability diversification in primary trophoblast cultures from aquaporin 1-deficient pregnant mice. J Obstet Gynaecol Res 41:1399–1405
pubmed: 26014508
Shao H, Gao S, Ying X, Zhu X, Hua Y (2021) Expression and regulation of aquaporins in pregnancy complications and reproductive dysfunctions. DNA Cell Biol 40:116–125
pubmed: 33226842
Sibley CP, Brownbill P, Glazier JD, Greenwood SL (2018) Knowledge needed about the exchange physiology of the placenta. Placenta 64(Suppl 1):S9–S15
pubmed: 29370939
Sibley CP, Glazier JD, Greenwood SL, Lacey H, Mynett K, Speake P, Jansson T, Johansson M, Powell TL (2002) Regulation of placental transfer: the Na
Soh YM, Tiwari A, Mahendroo M, Conrad KP, Parry LJ (2012) Relaxin regulates hyaluronan synthesis and aquaporins in the cervix of late pregnant mice. Endocrinology 153:6054–6064
pubmed: 23087172
pmcid: 3512066
Spencer TE, Johnson GA, Burghardt RC, Bazer FW (2004) Progesterone and placental hormone actions on the uterus: insights from domestic animals. Biol Reprod 71:2–10
pubmed: 14973264
Stenhouse C, Seo H, Wu G, Johnson GA, Bazer FW (2022) Insights into the regulation of implantation and placentation in humans, rodents, sheep, and pigs. Adv Exp Med Biol 1354:25–48
Stulc J (1997) Placental transfer of inorganic ions and water. Physiol Rev 77:805–836
pubmed: 9234966
Su WH, Qiao Y, Yi F, Guan XG, Zhang D (2010) Increased female fertility in aquaporin 8-deficient mice. IUBMB Life 62:852–857
pubmed: 21117174
Sun XL, Zhang J, Fan Y, Ding JH (2009) Aquaporin-4 deficiency induces subfertility in female mice. Fertil Steril 92:1736–1743
pubmed: 18976758
Szpilbarg N, Castro-Parodi M, Reppetti J, Repetto M, Maskin B, Martinez N, Damiano AE (2016) Placental programmed cell death: insights into the role of aquaporins. Mol Hum Reprod 22:46–56
pubmed: 26568619
Szpilbarg N, Seyahian A, Di Paola M, Castro-Parodi M, Martinez N, Farina M, Damiano AE (2018) Oxygen regulation of aquaporin-4 in human placenta. Reprod BioMed Online 37:601–612
pubmed: 30539720
Torday JS, Rehan VK (2003) Testing for fetal lung maturation: a biochemical “window” to the developing fetus. Clin Lab Med 23:361–383
pubmed: 12848449
Vilariño-García T, Pérez-Pérez A, Dietrich V, Fernández-Sánchez M, Guadix P, Dueñas JL, Varone CL, Damiano AE, Sánchez-Margalet V (2016) Increased expression of aquaporin 9 in trophoblast from gestational diabetic patients. Horm Metab Res 48:535–539
pubmed: 27082037
Vilariño-García T, Pérez-Pérez A, Dietrich V, Guadix P, Dueñas JL, Varone CL, Damiano AE, Sánchez-Margalet V (2018) Leptin up-regulates aquaporin 9 expression in human placenta in vitro. Gynecol Endocrinol 34:75–77
Wang S, Kallichanda N, Song W, Ramirez BA, Ross MG (2001) Expression of aquaporin-8 in human placenta and chorioamniotic membranes: evidence of molecular mechanism for intramembranous amniotic fluid resorption. Am J Obstet Gynecol 185:1226–1231
pubmed: 11717661
Wang S, Chen J, Beall M, Zhou W, Ross MG (2004) Expression of aquaporin 9 in human chorioamniotic membranes and placenta. Am J Obstet Gynecol 191:2160–2167
pubmed: 15592307
Watson AJ (1992) The cell biology of blastocyst development. Mol Reprod Dev 33:492–504
pubmed: 1335276
Wen H, Nagelhus EA, Amiry-Moghaddam M, Agre P, Ottersen OP, Nielsen S (1999) Ontogeny of water transport in rat brain: postnatal expression of the aquaporin-4 water channel. Eur J Neurosci 11:935–945
pubmed: 10103087
Wilbur WJ, Power GG, Longo LD (1978) Water exchange in the placenta: a mathematical model. Am J Physiol 235:R181–199
Wintour EM, Liu H, Dodic M, Moritz K (2004) Differential renal and cardiac gene expression in ovine fetuses programmed to become hypertersive adults by early glucocorticoid treatment. In: Proceedings of the 12th International Congress of Endocrinology, Lisbon, Portugal. pp 501–505
Wooding FB, Wilsher S, Benirschke K, Jones CJ, Allen WR (2015) Immunocytochemistry of the placentas of giraffe (Giraffa cameleopardalis giraffa) and okapi (Okapi johnstoni): comparison with other ruminants. Placenta 36:77–87
pubmed: 25465705
Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37:1–17
pubmed: 19301095
Wu G (2018) Principles of animal nutrition. CRC Press, Boca Raton, FL
Wu G (2021) Amino Acids: biochemistry and nutrition, 2nd edition. CRC Press, Boca Raton, Florida
Wu G (2022) Nutrition and metabolism: foundations for animal growth, development, reproduction, and health. Adv Exp Med Biol 1354:1–24
Wu G, Bazer FW, Wallace JM, Spencer TE (2006) BOARD-INVITED REVIEW: Intrauterine growth retardation: Implications for the animal sciences. J Anim Sci 84:2316–2337
Wu G, Bazer FW, Satterfield MC, Li X, Wang X, Johnson GA, Burghardt RC, Dai Z, Wang J, Wu Z (2013) Impacts of arginine nutrition on embryonic and fetal development in mammals. Amino Acids 45:241–245
pubmed: 23732998
Wu G, Bazer FW, Johnson GA, Herring C, Seo H, Dai ZL, Wang JJ, Wu ZL, Wang XL (2017) Functional amino acids in the development of the pig placenta. Mol Reprod Dev 84:879–882
Wu G, Bazer FW, Johnson GA, Knabe DA, Burghardt RC, Spencer TE, Li XL, Wang JJ (2011) TRIENNIAL GROWTH SYMPOSIUM: Important roles for L-glutamine in swine nutrition and production. J Anim Sci 89:2017–2030
Wu G, Bazer FW, Johnson GA, Hou YQ (2018) Arginine nutrition and metabolism in growing, gestating and lactating swine. J Anim Sci 96:5035–5051
pubmed: 30445424
pmcid: 6276552
Wu G, Bazer FW, Satterfield MC, Gilbreath KR, Posey EA, Sun YX (2022) L-Arginine nutrition and metabolism in ruminants. Adv Exp Med Biol 1354:177–206
Wu G, Meininger CJ, McNeal CJ, Bazer FW, Rhoads JM (2021) Role of L-arginine in nitric oxide synthesis and health in humans. Adv Exp Med Biol 1332:167–188
pubmed: 34251644
Xiong Y, Tan YJ, Xiong YM, Huang YT, Hu XL, Lu YC, Ye YH, Wang TT, Zhang D, Jin F, Huang HF, Sheng JZ (2013) Expression of aquaporins in human embryos and potential role of AQP3 and AQP7 in preimplantation mouse embryo development. Cell Physiol Biochem 31:649–658
pubmed: 23652731
Yamamoto T, Sasaki S, Fushimi K, Ishibashi K, Yaoita E, Kawasaki K, Fujinaka H, Marumo F, Kihara I (1997) Expression of AQP family in rat kidneys during development and maturation. Am J Physiol 272:F198–F204
Yang B, Song Y, Zhao D, Verkman AS (2005) Phenotype analysis of aquaporin-8 null mice. Am J Physiol 288:C1161–1170
Yasui M, Hazama A, Kwon TH, Nielsen S, Guggino WB, Agre P (1999) Rapid gating and anion permeability of an intracellular aquaporin. Nature 402:184–187
pubmed: 10647010
Zelenina M, Tritto S, Bondar AA, Zelenin S, Aperia A (2004) Copper inhibits the water and glycerol permeability of aquaporin-3. J Biol Chem 279:51939–51943
pubmed: 15456785
Zhang JM, He WL, Yi D, Zhao D, Song Z, Hou YQ, Wu G (2019) Regulation of protein synthesis in porcine mammary epithelial cells by L-valine. Amino Acids 51:717–726
pubmed: 30798466
Zhang Q, Hou YQ, Bazer FW, He WL, Posey EA, Wu G (2021) Amino acids in swine nutrition and production. Adv Exp Med Biol 1285:81–107
pubmed: 33770404
Zhao Y, Lin L, Lai A (2018) Expression and significance of aquaporin-2 and serum hormones in placenta of patients with preeclampsia. J Obstet Gynaecol 38:42–48
pubmed: 28764583
Zheng Z, Liu H, Beall M, Ma T, Hao R, Ross MG (2014) Role of aquaporin 1 in fetal fluid homeostasis. J Matern Fetal Neonatal Med 27:505–510
pubmed: 23808411
Zhu XQ, Jiang SS, Zhu XJ, Zou SW, Wang YH, Hu YC (2009) Expression of aquaporin 1 and aquaporin 3 in fetal membranes and placenta in human term pregnancies with oligohydramnios. Placenta 30:670–676
pubmed: 19545896
Zhu X, Jiang S, Hu Y, Zheng X, Zou S, Wang Y, Zhu XJ (2010) The expression of aquaporin 8 and aquaporin 9 in fetal membranes and placenta in term pregnancies complicated by idiopathic polyhydramnios. Early Hum Dev 86:657–663
pubmed: 20732771
Zhu C, Jiang Z, Bazer FW, Johnson GA, Burghardt RC, Wu G (2015) Aquaporins in the female reproductive system of mammals. Front Biosci 20:838–871
Zhu C, Ye J, Bazer F, Johnson G, Bai Y, Yang J, Chen Z, Jiang Z (2018a) L-Arginine upregulates aquaporin-3 expression and water transport by porcine trophectoderm cells through NO- and cAMP-dependent mechanisms. J Anim Sci 96(Suppl 3):303–304
Zhu C, Jiang Z, Bazer F, Johnson G, Burghardt R, Wu G (2018b) Expression of AQP 1, 3, 5, and 9 in the porcine placenta and uterine endometrium during the estrous cycle and gestation. J Anim Sci 96(Suppl 3):482–483
Zhu C, Li XL, Bazer FW, Johnson GA, Burghardt RC, Jiang ZY, Wu G (2016) Dietary L-arginine supplementation during Days 14 and 25 of gestation enhances placental aquaporin-1 expression and water transport by the pig placenta. The Society of the Study of Reproduction (SSR) Annual Meeting, July 16–20, 2016, San Diego, CA
Zhu C, Li XL, Bazer FW, Johnson GA, Burghardt RC, Jiang ZY, Wu G (2021) Dietary L-arginine supplementation during days 14-25 of gestation enhances aquaporin expression in the placentae and endometria of gestating gilts. Amino Acids 53:1287–1295
pubmed: 34241695