Maternal iron status during pregnancy compared with neonatal iron status better predicts placental iron transporter expression in humans

FASEB Journal

Volumn 30, Issue 10, 2016, Pages 3541-3550

  Best, Cora M ^a   Pressman, Eva K ^b   Cao, Chang ^c   Cooper, Elizabeth ^b   Guillet, Ronnie ^b   Yost, Olivia L ^a   Galati, Jonathan ^a   Kent, Tera R ^a   O'Brien, Kimberly O ^a  

^a Cornell University ^*  (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Adolescents; Anemia; Heme; TfR1 hepcidin

Indexed keywords

ERYTHROPOIETIN; FERRITIN; FERROPORTIN; FLVCR1 PROTEIN; HEME; HEMOGLOBIN; HEPCIDIN; INTERLEUKIN 6; IRON; LRP1 PROTEIN; PCFT PROTEIN; PLACENTA PROTEIN; PROTON COUPLED FOLATE TRANSPORTER; TFR1 PROTEIN; UNCLASSIFIED DRUG; CD71 ANTIGEN; LEUKOCYTE ANTIGEN; TRANSFERRIN RECEPTOR;

ADOLESCENT; ARTICLE; BODY MASS; CONTROLLED STUDY; FELINE LEUKEMIA VIRUS; FEMALE; GESTATIONAL AGE; GESTATIONAL WEIGHT GAIN; HEMOGLOBIN BLOOD LEVEL; HUMAN; IRON DEFICIENCY; IRON TRANSPORT; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MATERNAL AGE; MATERNAL SERUM; PARENTAL CONSENT; PLACENTA; PLACENTA TISSUE; PREDICTION; PREGNANCY; PRENATAL CARE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; BLOOD; FETUS BLOOD; METABOLISM; NEWBORN;

ANTIGENS, CD; FEMALE; FERRITINS; FETAL BLOOD; HEME; HEPCIDINS; HUMANS; INFANT, NEWBORN; IRON; PLACENTA; PREGNANCY; PROTON-COUPLED FOLATE TRANSPORTER; RECEPTORS, TRANSFERRIN;

EID: 84990866294     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.201600069R     Document Type: Article

References (45)

1. Rao, R., and Georgieff, M. K. (2007) Iron in fetal and neonatal nutrition. Semin. Fetal Neonatal Med. 12, 54-63
2. Viteri, F. E. (1994) The consequences of iron deficiency and anemia in pregnancy. Adv. Exp. Med. Biol. 352, 127-139
3. Georgieff,M. K. (2007) Nutrition and the developing brain: nutrient priorities and measurement. Am. J. Clin. Nutr. 85, 614S-620S
4. Hurrell, R., and Egli, I. (2010) Iron bioavailability and dietary reference values. Am. J. Clin. Nutr. 91, 1461S-1467S
5. Bradley, J., Leibold, E. A.,Harris, Z. L., Wobken, J. D., Clarke, S., Zumbrennen, K. B., Eisenstein, R. S., and Georgieff, M. K. (2004) Influence of gestational age and fetal iron status on IRP activity and iron transporter protein expression in third-trimester human placenta. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R894-R901
6. Fuchs, R., and Ellinger, I. (2004)Endocytic and transcytotic processes in villous syncytiotrophoblast: role in nutrient transport to the human fetus. Traffic 5, 725-738
7. Georgieff, M. K., Wobken, J. K., Welle, J., Burdo, J. R., and Connor, J. R. (2000) Identification and localization of divalent metal transporter-1 (DMT-1) in term human placenta. Placenta 21, 799-804
8. Bastin, J., Drakesmith, H., Rees, M., Sargent, I., and Townsend, A. (2006) Localisation of proteins of iron metabolism in the human placenta and liver. Br. J. Haematol. 134, 532-543
9. Chen,H.,Attieh, Z.K., Syed,B.A.,Kuo,Y.M., Stevens,V., Fuqua,B.K., Andersen, H. S., Naylor,C. E., Evans, R.W., Gambling, L., Danzeisen, R., Bacouri-Haidar, M., Usta, J., Vulpe, C. D., and McArdle, H. J. (2010) Identification of zyklopen, a new member of the vertebrate multicopper ferroxidase family, and characterization in rodents and human cells. J. Nutr. 140, 1728-1735
10. Ohgami, R. S., Campagna, D. R., McDonald, A., and Fleming, M. D. (2006) The Steap proteins are metalloreductases. Blood 108, 1388-1394
11. Keel, S.B.,Doty,R. T., Yang, Z.,Quigley, J.G., Chen, J., Knoblaugh, S., Kingsley, P. D., De Domenico, I., Vaughn, M. B., Kaplan, J., Palis, J., and Abkowitz, J.L. (2008)A heme export protein is required for red blood cell differentiation and iron homeostasis. Science 319, 825-828
12. Qiu, A., Jansen,M., Sakaris, A.,Min, S.H., Chattopadhyay, S., Tsai, E., Sandoval, C., Zhao, R., Akabas, M. H., and Goldman, I. D. (2006) Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption. Cell 127, 917-928
13. Hvidberg, V., Maniecki, M. B., Jacobsen, C., Højrup, P.,Møller, H. J., and Moestrup, S. K. (2005) Identification of the receptor scavenging hemopexin-heme complexes. Blood 106, 2572-2579
14. Cao, C., and O'Brien, K. O. (2013) Pregnancy and iron homeostasis: an update. Nutr. Rev. 71, 35-51
15. Nemeth, E., and Ganz, T. (2006) Regulation of iron metabolism by hepcidin. Annu. Rev. Nutr. 26, 323-342
16. Gambling, L., Czopek, A., Andersen, H. S., Holtrop, G., Srai, S. K. S., Krejpcio, Z., and McArdle, H. J. (2009) Fetal iron status regulates maternal ironmetabolism during pregnancy in the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296, R1063-R1070
17. Evans, P., Cindrova-Davies, T.,Muttukrishna, S., Burton, G. J., Porter, J., and Jauniaux, E. (2011) Hepcidin and iron species distribution inside the first-trimester human gestational sac. Mol. Hum. Reprod. 17, 227-232
18. Balesaria, S., Hanif, R., Salama, M. F., Raja, K., Bayele, H. K., McArdle, H., and Srai, S. K. (2012) Fetal iron levels are regulated bymaternal and fetal Hfe genotype and dietary iron.Haematologica 97, 661-669
19. Martin,M.E., Nicolas, G.,Hetet, G.,Vaulont, S., Grandchamp,B., and Beaumont,C. (2004)Transferrin receptor 1mRNAis downregulated in placenta of hepcidin transgenic embryos. FEBS Lett. 574, 187-191
20. Nicolas, G., Bennoun, M., Porteu, A., Mativet, S., Beaumont, C., Grandchamp, B., Sirito, M., Sawadogo,M., Kahn, A., and Vaulont, S. (2002) Severe iron deficiency anemia in transgenic mice expressing liver hepcidin. Proc.Natl. Acad. Sci. USA 99, 4596-4601
21. Lee, S., Young, B. E., Cooper, E. M., Pressman, E., Queenan, R. A., Olson, C. M., Guillet, R., and O'Brien, K. O. (2014) Nutrient inadequacy is prevalent in pregnant adolescents, and prenatal supplement use may not fully compensate for dietary deficiencies. Infant Child Adolesc. Nutr. 6, 152-159
22. Whisner, C. M., Young, B. E., Witter, F. R., Harris, Z. L., Queenan, R. A., Cooper, E. M., and O'Brien, K. O. (2014) Reductions in heel bone quality across gestation are attenuated in pregnant adolescents with higher prepregnancyweight and greater increases in PTHacross gestation. J. Bone Miner. Res. 29, 2109-2117
23. Lee, S., Guillet, R., Cooper, E. M., Westerman, M., Orlando, M., Pressman, E., and O'Brien, K. O. (2014) Maternal inflammation at delivery affects assessment of maternal iron status. J. Nutr. 144, 1524-1532
24. Young, M. F., Pressman, E., Foehr,M. L., McNanley, T., Cooper, E., Guillet, R., Orlando, M., McIntyre, A. W., Lafond, J., and O'Brien, K.O. (2010) Impact ofmaternal andneonatal ironstatuson placental transferrin receptor expression in pregnant adolescents. Placenta 31, 1010-1014
25. Cao, C., Pressman, E. K., Cooper, E. M., Guillet, R., Westerman, M., and O'Brien, K. O. (2014) Placental heme receptor LRP1 correlates with the heme exporter FLVCR1 and neonatal iron status. Reproduction 148, 295-302
26. Young, B. E., Cooper, E. M., McIntyre, A. W., Kent, T., Witter, F., Harris, Z. L., and O'Brien, K. O. (2014) Placental vitamin D receptor (VDR) expression is related to neonatal vitamin D status, placental calcium transfer, and fetal bone length in pregnant adolescents. FASEB J. 28, 2029-2037
27. O'Brien,K. O., Li, S., Cao, C., Kent,T., Young, B. V., Queenan, R. A., Pressman, E. K., and Cooper, E. M. (2014) Placental CYP27B1 and CYP24A1 expression in human placental tissue and their association with maternal and neonatal calcitropic hormones. J. Clin. Endocrinol. Metab. 99, 1348-1356
28. Lee, S.,Guillet, R., Cooper, E.M., Westerman,M.,Orlando,M., Kent, T., Pressman, E., and O'Brien,K.O. (2016) Prevalence of anemia and associations between neonatal iron status, hepcidin, and maternal ironstatus amongneonates bornto pregnant adolescents. Pediatr. Res. 79, 42-48
29. Centers for Disease Control and Prevention. (1998) Recommendations to prevent and control iron deficiency in the United States. MMWR. Recommendations and Reports,U.S. Department ofHealth andHuman Services publication no. 47 (No. RR-3), pp. 1-29,Centers for Disease Control and Prevention, Atlanta, GA, USA
30. Committee on the Prevention, Detection, and Management of Iron Deficiency Anemia Among U.S. Children and Women of Childbearing Age. (1993) Iron Deficiency Anemia: Recommended Guidelines for the Prevention, Detection, and Management Among U.S. Children and Women of Childbearing Age (Earl, R., and Woteki, C. E., eds.), National Academies Press, Washington, DC, USA
31. Orkin, S. H., Fisher, D. E., Look, A. T., Lux, S. E., Ginsburg, D., and Nathan, D. G. (2009) Nathan and Oski's Hematology of Infancy and Childhood, Saunders Elsevier, Philadelphia
32. Jaacks,L.M., Young,M. F.,Essley,B.V.,McNanley,T. J.,Cooper,E.M., Pressman, E. K., McIntyre, A. W., Orlando, M. S., Abkowitz, J. L., Guillet, R., and O'Brien, K. O. (2011) Placental expression of the heme transporter, feline leukemia virus subgroup C receptor, is related to maternal iron status in pregnant adolescents. J. Nutr. 141, 1267-1272
33. Gleason, P. M., Boushey, C. J., Harris, J. E., and Zoellner, J. (2015) Publishing nutrition research: a review of multivariate techniques-part 3: data reduction methods. J. Acad. Nutr. Diet. 115, 1072-1082
34. Gambling, L., Danzeisen, R., Gair, S., Lea, R. G., Charania, Z., Solanky, N., Joory, K. D., Srai, S. K., and McArdle, H. J. (2001) Effect of iron deficiency on placental transfer of iron and expression of iron transport proteins in vivo and in vitro. Biochem. J. 356, 883-889
35. Garcia-Valdes, L., Campoy, C., Hayes, H., Florido, J., Rusanova, I., Miranda, M. T., and McArdle, H. J. (2015) The impact of maternal obesity on iron status, placental transferrin receptor expression and hepcidin expression in human pregnancy. Int. J. Obes. (London) 39, 571-578
36. Ganz, T. (2003) Hepcidin, a key regulator of iron metabolism and mediator of anemia of inflammation. Blood 102, 783-788
37. Muehlenbachs, A., Fried,M., Lachowitzer, J.,Mutabingwa, T. K., and Duffy, P. E. (2007) Genome-wide expression analysis of placental malaria reveals features of lymphoid neogenesis during chronic infection. J. Immunol. 179, 557-565
38. Shayeghi, M., Latunde-Dada, G. O., Oakhill, J. S., Laftah, A. H., Takeuchi, K., Halliday,N., Khan, Y.,Warley, A., McCann, F. E.,Hider, R. C., Frazer, D.M., Anderson, G. J., Vulpe, C. D., Simpson, R. J., and McKie, A. T. (2005) Identification of an intestinal heme transporter. Cell 122, 789-801
39. Latunde-Dada, G. O., Takeuchi, K., Simpson, R. J., and McKie, A. T. (2006) Haem carrier protein 1 (HCP1): expression and functional studies in cultured cells. FEBS Lett. 580, 6865-6870
40. Le Blanc, S.,Garrick,M.D., and Arredondo,M. (2012)Heme carrier protein 1 transports heme and is involved in heme-Fe metabolism. Am. J. Physiol. Cell Physiol. 302, C1780-C1785
41. Quigley, J.G., Yang, Z.,Worthington,M. T., Phillips, J.D., Sabo, K. M., Sabath, D. E., Berg, C. L., Sassa, S., Wood, B. L., and Abkowitz, J. L. (2004) Identification of a human heme exporter that is essential for erythropoiesis. Cell 118, 757-766
42. Carpenter, C. E., and Mahoney, A.W. (1992) Contributions of heme and nonheme iron to human nutrition. Crit. Rev. Food Sci. Nutr. 31, 333-367
43. Carter, A.M. (2012) Evolution of placental function inmammals: the molecular basis of gas and nutrient transfer, hormone secretion, and immune responses. Physiol. Rev. 92, 1543-1576
44. Young, M. F., Griffin, I., Pressman, E., McIntyre, A. W., Cooper, E., McNanley,T.,Harris, Z. L.,Westerman,M., and O'Brien,K.O. (2012) Maternal hepcidin is associatedwithplacental transfer of iron derived from dietary heme and nonheme sources. J. Nutr. 142, 33-39
45. Institute ofMedicine Panel onMiconutrients. (2001) Dietary Reference Intakes for VitaminA, VitaminK,Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc, National Academies Press,Washington, DC, USA