Hepcidin and iron homeostasis during pregnancy

Nutrients

Volumn 6, Issue 8, 2014, Pages 3062-3083

  Koenig, Mary Dawn ^a   Tussing Humphreys, Lisa ^a   Day, Jessica ^b   Cadwell, Brooke ^c   Nemeth, Elizabeta ^d  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b Sumter Family Health Center   (United States)

^c YALE UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Hepcidin; Inflammation; Ironregulation; Pregnancy

Indexed keywords

C REACTIVE PROTEIN; FERRITIN; HEPCIDIN; INTERLEUKIN 6; MATERNAL HEPCIDIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; IRON;

BIOAVAILABILITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROPOIESIS; GENE EXPRESSION; HOMEOSTASIS; HUMAN; INFLAMMATION; IRON DEFICIENCY; IRON HOMEOSTASIS; MALARIA; MASS SPECTROMETRY; NONHUMAN; OBESITY; PREECLAMPSIA; PREGNANCY; PROTEIN EXPRESSION; PUERPERIUM; REVIEW; STRESS; UMBILICAL CORD BLOOD; ANIMAL; BLOOD; CHEMISTRY; DISEASE MODEL; FACTUAL DATABASE; FEMALE; FETOMATERNAL TRANSFUSION; FETUS BLOOD; PHYSIOLOGY;

ANIMALS; BIOLOGICAL AVAILABILITY; DATABASES, FACTUAL; DISEASE MODELS, ANIMAL; FEMALE; FETAL BLOOD; HEPCIDINS; HOMEOSTASIS; HUMANS; IRON; MATERNAL-FETAL EXCHANGE; POSTPARTUM PERIOD; PREGNANCY;

EID: 84905575679     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu6083062     Document Type: Review

References (75)

1. Andrews, N. C. Disorders of iron metabolism. N. Engl. J. Med. 1999, 341, 1986-1995.
2. National Research Council. Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc; National Academy Press: Washington, DC, USA, 2001; p. 772.
3. Greer, J. P.; Ovid Technologies Inc. Wintrobe's Clinical Hematology, 12th ed.; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2009.
4. Corbett, J. V. Accidental poisoning with iron supplements. MCN Am. J. Matern. Child Nurs. 1995, 20, 234.
5. Bothwell, T. H. Iron requirements in pregnancy and strategies to meet them. Am. J. Clin. Nutr. 2000, 72, 257S-264S.
6. Allen, L. H. Biological mechanisms that might underlie iron's effects on fetal growth and preterm birth. J. Nutr. 2001, 131, 581S-589S.
7. Scott, D. E. Anemia in pregnancy. Obstet. Gynecol. Annu. 1972, 1, 219-244.
8. Tapiero, H.; Gate, L.; Tew, K. D. Iron: Deficiencies and requirements. Biomed. Pharmacother. 2001, 55, 324-332.
9. Centers for Disease Control and Prevention. Recommendations to prevent and control iron deficiency in the United States. MMWR Recomm. Rep. 1998, 47, 1-29.
10. Reshetnikova, O. S.; Burton, G. J.; Teleshova, O. V. Placental histomorphometry and morphometric diffusing capacity of the villous membrane in pregnancies complicated by maternal iron-deficiency anemia. Am. J. Obstet. Gynecol. 1995, 173, 724-727.
11. Kadyrov, M.; Kosanke, G.; Kingdom, J.; Kaufmann, P. Increased fetoplacental angiogenesis during first trimester in anaemic women. Lancet 1998, 352, 1747-1749.
12. Konijn, A. M. Iron metabolism in inflammation. Baillieres Clin. Haematol. 1994, 7, 829-849.
13. Godfrey, K. M.; Redman, C. W.; Barker, D. J.; Osmond, C. The effect of maternal anaemia and iron deficiency on the ratio of fetal weight to placental weight. Br. J. Obstet. Gynecol. 1991, 98, 886-891.
14. Collins, J. F.; Wessling-Resnick, M.; Knutson, M. D. Hepcidin regulation of iron transport. J. Nutr. 2008, 138, 2284-2288.
15. Cogswell, M. E.; Parvanta, I.; Ickes, L.; Yip, R.; Brittenham, G. M. Iron supplementation during pregnancy, anemia, and birth weight: A randomized controlled trial. Am. J. Clin. Nutr. 2003, 78, 773-781.
16. Blot, I.; Diallo, D.; Tchernia, G. Iron deficiency in pregnancy: Effects on the newborn. Curr. Opin. Hematol. 1999, 6, 65-70.
17. Earl, R. O.; Woteki, C. E.; Institute of Medicine (U. S.); Committee on the Prevention Detection and Management of Iron Deficiency Anemia among U. S.; Children and Women of Childbearing Age; Institute of Medicine (U. S.); Food and Nutrition Board. Iron Deficiency Anemia: Recommended Guidelines for the Prevention, Detection, and Management among U. S. Children and Women of Childbearing Age; National Academy Press: Washington, DC, USA, 1993; p. 6.
18. Allen, L. H. Pregnancy and iron deficiency: Unresolved issues. Nutr. Rev. 1997, 55, 91-101.
19. Malhotra, M.; Sharma, J. B.; Batra, S.; Sharma, S.; Murthy, N. S.; Arora, R. Maternal and perinatal outcome in varying degrees of anemia. Int. J. Gynaecol. Obstet. 2002, 79, 93-100.
20. Allen, L. H. Anemia and iron deficiency: Effects on pregnancy outcome. Am. J. Clin. Nutr. 2000, 71, 1280S-1284S.
21. Gulmezoglu, A. M.; Mahomed, K.; Hofmeyr, G. J.; Nikodem, V. C.; Kramer, T. Fetal and maternal catecholamine levels at delivery. J. Perinat. Med. 1996, 24, 687-691.
22. Campos, M. S.; Barrionuevo, M.; Alferez, M. J.; Gomez-Ayala, A. E.; Rodriguez-Matas, M. C.; Lopez Aliaga, I.; Lisbona, F. Interactions among iron, calcium, phosphorus and magnesium in the nutritionally iron-deficient rat. Exp. Physiol. 1998, 83, 771-781.
23. Coghetto Baccin, A.; Lauerman Lazzaretti, L.; Duarte Martins Brandao, V.; Manfredini, V.; Peralba, M. C.; Silveira Benfato, M. Oxidative stress in older patients with iron deficiency anaemia. J. Nutr. Health Aging 2009, 13, 666-670.
24. Casanueva, E.; Viteri, F. E. Iron and oxidative stress in pregnancy. J. Nutr. 2003, 133, 1700S-1708S.
25. Knutson, M. D.; Handelman, G. J.; Viteri, F. E. Methods for measuring ethane and pentane in expired air from rats and humans. Free Radic. Biol. Med. 2000, 28, 514-519.
26. Walter, P. B.; Knutson, M. D.; Paler-Martinez, A.; Lee, S.; Xu, Y.; Viteri, F. E.; Ames, B. N. Iron deficiency and iron excess damage mitochondria and mitochondrial DNA in rats. Proc. Natl. Acad. Sci. USA 2002, 99, 2264-2269.
27. Bhaskaram, P. Immunobiology of mild micronutrient deficiencies. Br. J. Nutr. 2001, 85 (Suppl. 2), S75-S80.
28. McArdle, H. J.; Lang, C.; Hayes, H.; Gambling, L. Role of the placenta in regulation of fetal iron status. Nutr. Rev. 2011, 69 (Suppl. 1), S17-S22.
29. Paterson, S.; Armstrong, N. J.; Iacopetta, B. J.; McArdle, H. J.; Morgan, E. H. Intravesicular pH and iron uptake by immature erythroid cells. J. Cell. Physiol. 1984, 120, 225-232.
30. Harris, E. D. New insights into placental iron transport. Nutr. Rev. 1992, 50, 329-331.
31. Donovan, A.; Lima, C. A.; Pinkus, J. L.; Pinkus, G. S.; Zon, L. I.; Robine, S.; Andrews, N. C. The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. Cell Metab. 2005, 1, 191-200.
32. 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.; et al. Identification of zyklopen, a new member of the vertebrate multicopper ferroxidase family, and characterization in rodents and human cells. J. Nutr. 2010, 140, 1728-1735.
33. Ganz, T. Hepcidin-A regulator of intestinal iron absorption and iron recycling by macrophages. Best Pract. Res. Clin. Haematol. 2005, 18, 171-182.
34. Ganz, T. Hepcidin and its role in regulating systemic iron metabolism. Hematol. Am. Soc. Hematol. Educ. Progr. 2006, doi: 10. 1182/asheducation-2006. 1. 29.
35. Nemeth, E.; Ganz, T. Regulation of iron metabolism by hepcidin. Annu. Rev. Nutr. 2006, 26, 323-342.
36. Murphy, A. T.; Witcher, D. R.; Luan, P.; Wroblewski, V. J. Quantitation of hepcidin from human and mouse serum using liquid chromatography tandem mass spectrometry. Blood 2007, 110, 1048-1054.
37. Ganz, T. Hepcidin, a key regulator of iron metabolism and mediator of anemia of inflammation. Blood 2003, 102, 783-788.
38. Darshan, D.; Anderson, G. J. Interacting signals in the control of hepcidin expression. Biometals 2009, 22, 77-87.
39. Hamlin, F.; Latunde-Dada, G. O. Iron bioavailibity from a tropical leafy vegetable in anaemic mice. Nutr. Metab. 2011, 8, 9.
40. Goodnough, L. T.; Nemeth, E.; Ganz, T. Detection, evaluation, and management of iron-restricted erythropoiesis. Blood 2010, 116, 4754-4761.
41. Gagliardo, B.; Kubat, N.; Faye, A.; Jaouen, M.; Durel, B.; Deschemin, J. C.; Canonne-Hergaux, F.; Sari, M. A.; Vaulont, S. Pro-hepcidin is unable to degrade the iron exporter ferroportin unless maturated by a furin-dependent process. J. Hepatol. 2009, 50, 394-401.
42. Sasu, B. J.; Li, H.; Rose, M. J.; Arvedson, T. L.; Doellgast, G.; Molineux, G. Serum hepcidin but not prohepcidin may be an effective marker for anemia of inflammation (AI). Blood Cells Mol. Dis. 2010, 45, 238-245.
43. Roe, M. A.; Spinks, C.; Heath, A. L.; Harvey, L. J.; Foxall, R.; Wimperis, J.; Wolf, C.; Fairweather-Tait, S. J. Serum prohepcidin concentration: No association with iron absorption in healthy men; and no relationship with iron status in men carrying HFE mutations, hereditary haemochromatosis patients undergoing phlebotomy treatment, or pregnant women. Br. J. Nutr. 2007, 97, 544-549.
44. Briana, D. D.; Boutsikou, T.; Baka, S.; Boutsikou, M.; Stamati, L.; Hassiakos, D.; Gourgiotis, D.; Malamitsi-Puchner, A. Perinatal role of hepcidin and iron homeostasis in full-term intrauterine growth-restricted infants. Eur. J. Haematol. 2012, 90, 37-44.
45. Simavli, S.; Derbent, A. U.; Uysal, S.; Turhan, N. O. Hepcidin, iron status, and inflammation variables among healthy pregnant women in the turkish population. J. Matern. Fetal Neonatal Med. 2014, 27, 75-79.
46. Itkonen, O.; Parkkinen, J.; Stenman, U. H.; Hamalainen, E. Preanalytical factors and reference intervals for serum hepcidin LC-MS/MS method. Clin. Chim. Acta 2012, 413, 696-701.
47. Howard, C. T.; McKakpo, U. S.; Quakyi, I. A.; Bosompem, K. M.; Addison, E. A.; Sun, K.; Sullivan, D.; Semba, R. D. Relationship of hepcidin with parasitemia and anemia among patients with uncomplicated plasmodium falciparum malaria in ghana. Am. J. Trop. Med. Hyg. 2007, 77, 623-626.
48. Rehu, M.; Punnonen, K.; Ostland, V.; Heinonen, S.; Westerman, M.; Pulkki, K.; Sankilampi, U. Maternal serum hepcidin is low at term and independent of cord blood iron status. Eur. J. Haematol. 2010, 85, 345-352.
49. Schulze, K. J.; Christian, P.; Ruczinski, I.; Ray, A. L.; Nath, A.; Wu, L. S.; Semba, R. D. Hepcidin and iron status among pregnant women in bangladesh. Asia Pac. J. Clin. Nutr. 2008, 17, 451-456.
50. Toldi, G.; Stenczer, B.; Molvarec, A.; Takats, Z.; Beko, G.; Rigo, J., Jr.; Vasarhelyi, B. Hepcidin concentrations and iron homeostasis in preeclampsia. Clin. Chem. Lab. Med. 2010, 48, 1423-1426.
51. Van Santen, S.; de Mast, Q.; Luty, A. J.; Wiegerinck, E. T.; van der Ven, A. J.; Swinkels, D. W. Iron homeostasis in mother and child during placental malaria infection. Am. J. Trop. Med. Hyg. 2011, 84, 148-151.
52. Merhi, Z. O.; Seifer, D. B.; Weedon, J.; Adeyemi, O.; Holman, S.; Anastos, K.; Golub, E. T.; Young, M.; Karim, R.; Greenblatt, R.; et al. Circulating vitamin D correlates with serum antimullerian hormone levels in late-reproductive-aged women: Women's interagency HIV study. Fertil. Steril. 2012, 98, 228-234.
53. Gyarmati, B.; Szabo, E.; Szalay, B.; Czuczy, N.; Toldi, G.; Cseh, A.; Vasarhelyi, B.; Takats, Z. Serum maternal hepcidin levels 3 days after delivery are higher compared to those measured at parturition. J. Obstet. Gynaecol. Res. 2011, 37, 1620-1624.
54. Finkenstedt, A.; Widschwendter, A.; Brasse-Lagnel, C. G.; Theurl, I.; Hubalek, M.; Dieplinger, H.; Tselepis, C.; Ward, D. G.; Vogel, W.; Zoller, H. Hepcidin is correlated to soluble hemojuvelin but not to increased GDF15 during pregnancy. Blood Cells Mol. Dis. 2012, 48, 233-237.
55. Van Santen, S.; Kroot, J. J.; Zijderveld, G.; Wiegerinck, E. T.; Spaanderman, M. E.; Swinkels, D. W. The iron regulatory hormone hepcidin is decreased in pregnancy: A prospective longitudinal study. Clin. Chem. Lab. Med. 2013, 51, 1395-1401.
56. Dao, M. C.; Sen, S.; Iyer, C.; Klebenov, D.; Meydani, S. N. Obesity during pregnancy and fetal iron status: Is hepcidin the link? J. Perinatol. 2013, 33, 177-181.
57. Nicolas, G.; Bennoun, M.; Porteu, A.; Mativet, S.; Beaumont, C.; Grandchamp, B.; Sirito, M.; Sawadogo, M.; Kahn, A.; Vaulont, S. Severe iron deficiency anemia in transgenic mice expressing liver hepcidin. Proc. Natl. Acad. Sci. USA 2002, 99, 4596-4601.
58. Neves, J. V.; Olsson, I. A.; Porto, G.; Rodrigues, P. N. Hemochromatosis and pregnancy: Iron stores in the Hfe-/-mouse are not reduced by multiple pregnancies. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298, G525-G529.
59. Gambling, L.; Czopek, A.; Andersen, H. S.; Holtrop, G.; Srai, S. K.; Krejpcio, Z.; McArdle, H. J. Fetal iron status regulates maternal iron metabolism during pregnancy in the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296, R1063-R1070.
60. Millard, K. N.; Frazer, D. M.; Wilkins, S. J.; Anderson, G. J. Changes in the expression of intestinal iron transport and hepatic regulatory molecules explain the enhanced iron absorption associated with pregnancy in the rat. Gut 2004, 53, 655-660.
61. Cornock, R.; Gambling, L.; Langley-Evans, S. C.; McArdle, H. J.; McMullen, S. The effect of feeding a low iron diet prior to and during gestation on fetal and maternal iron homeostasis in two strains of rat. Reprod. Biol. Endocrinol. 2013, 11, 32.
62. Sozo, F.; Dick, A. M.; Bensley, J. G.; Kenna, K.; Brien, J. F.; Harding, R.; de Matteo, R. Alcohol exposure during late ovine gestation alters fetal liver iron homeostasis without apparent dysmorphology. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 304, R1121-R1129.
63. Ward, D. G.; Roberts, K.; Stonelake, P.; Goon, P.; Zampronio, C. G.; Martin, A.; Johnson, P. J.; Iqbal, T.; Tselepis, C. SELDI-TOF-MS determination of hepcidin in clinical samples using stable isotope labelled hepcidin as an internal standard. Proteome Sci. 2008, 6, 28.
64. Kroot, J. J.; Laarakkers, C. M.; Geurts-Moespot, A. J.; Grebenchtchikov, N.; Pickkers, P.; van Ede, A. E.; Peters, H. P.; van Dongen-Lases, E.; Wetzels, J. F.; Sweep, F. C.; et al. Immunochemical and mass-spectrometry-based serum hepcidin assays for iron metabolism disorders. Clin. Chem. 2010, 56, 1570-1579.
65. Kroot, J. J.; Hendriks, J. C.; Laarakkers, C. M.; Klaver, S. M.; Kemna, E. H.; Tjalsma, H.; Swinkels, D. W. (Pre)analytical imprecision, between-subject variability, and daily variations in serum and urine hepcidin: Implications for clinical studies. Anal. Biochem. 2009, 389, 124-129.
66. Ganz, T.; Olbina, G.; Girelli, D.; Nemeth, E.; Westerman, M. Immunoassay for human serum hepcidin. Blood 2008, 112, 4292-4297.
67. Kemna, E. H.; Tjalsma, H.; Podust, V. N.; Swinkels, D. W. Mass spectrometry-based hepcidin measurements in serum and urine: Analytical aspects and clinical implications. Clin. Chem. 2007, 53, 620-628.
68. Finkenstedt, A.; Bianchi, P.; Theurl, I.; Vogel, W.; Witcher, D. R.; Wroblewski, V. J.; Murphy, A. T.; Zanella, A.; Zoller, H. Regulation of iron metabolism through GDF15 and hepcidin in pyruvate kinase deficiency. Br. J. Haematol. 2009, 144, 789-793.
69. Blackburn, S. T. Maternal, Fetal & Neonatal Physiology: A Clinical Perspective, 2nd ed.; Saunders: St. Louis, MO, USA, 2003; p. 238.
70. Weiss, G.; Goodnough, L. T. Anemia of chronic disease. N. Engl. J. Med. 2005, 352, 1011-1023.
71. Ganz, T.; Nemeth, E. Iron sequestration and anemia of inflammation. Semin. Hematol. 2009, 46, 387-393.
72. Park, K. H.; Sawada, T.; Kosuge, T.; Kita, J.; Shimoda, M.; Tomosugi, N.; Kubota, K. Surgical inflammation induces hepcidin production after abdominal surgery. World J. Surg. 2012, 36, 800-806.
73. Kroot, J. J.; van Herwaarden, A. E.; Tjalsma, H.; Jansen, R. T.; Hendriks, J. C.; Swinkels, D. W. Second round robin for plasma hepcidin methods: First steps toward harmonization. Am. J. Hematol. 2012, 87, 977-983.
74. Whittaker, P. G.; Lind, T. The intravascular mass of albumin during human pregnancy: A serial study in normal and diabetic women. Br. J. Obstet. Gynaecol. 1993, 100, 587-592.
75. McArdle, H. J.; Andersen, H. S.; Jones, H.; Gambling, L. Copper and iron transport across the placenta: Regulation and interactions. J. Neuroendocrinol. 2008, 20, 427-431.