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Cited by 192Porphyrin Metabolism and DisordersHemoglobin structure and functionIron Metabolism and Disorders

Heme and erythropoieis: more than a structural role

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Chiabrando, D., Mercurio, S., Tolosano, E.·2014·Haematologica
DOI 10.3324/haematol.2013.091991PMC PMC4040894
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Abstract

Erythropoiesis is the biological process that consumes the highest amount of body iron for heme synthesis. Heme synthesis in erythroid cells is finely coordinated with that of alpha (α) and beta (β)-globin, resulting in the production of hemoglobin, a tetramer of 2α- and 2β-globin chains, and heme as the prosthetic group. Heme is not only the structural component of hemoglobin, but it plays multiple regulatory roles during the differentiation of erythroid precursors since it controls its own synthesis and regulates the expression of several erythroid-specific genes. Heme is synthesized in developing erythroid progenitors by the stage of proerythroblast, through a series of eight enzymatic reactions divided between mitochondria and cytosol. Defects of heme synthesis in the erythroid lineage result in sideroblastic anemias, characterized by microcytic anemia associated to mitochondrial iron overload, or in erythropoietic porphyrias, characterized by porphyrin deposition in erythroid cells. Here, we focus on the heme biosynthetic pathway and on human erythroid disorders due to defective heme synthesis. The regulatory role of heme during erythroid differentiation is discussed as well as the heme-mediated regulatory mechanisms that allow the orchestration of the adaptive cell response to heme deficiency.

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  • Disruptions to erythropoiesis could lead to anemia-like symptoms, resulting in reduced physical performance, impaired feeding activity, and potential organ damage.

    “These disruptions to erythropoiesis could lead to anemia-like symptoms, resulting in reduced physical performance, impaired feeding activity, and potential organ damage (Chiabrando et al., 2014).”

    From Deciphering the toxic effects of polystyrene nanoparticles on erythropoiesis at single-cell resolution (2025) · cites this paper as Chiabrando et al., 2014

    The sections on erythroid disorders of heme biosynthesis and erythropoietic protoporphyria report anemia associated with disrupted heme synthesis; the latter also describes tissue damage and possible liver failure in that specific disorder. The paper does not report reduced physical performance or impaired feeding activity, or establish that anemia itself causes the organ damage described. Page numbers are unavailable in our copy. (LLM, conf=0.88)

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  • alas1 plays a critical role in the early stages of heme synthesis.

    “including alas1, which plays a critical role in the early stages of heme synthesis (Chiabrando et al., 2014).”

    From Deciphering the toxic effects of polystyrene nanoparticles on erythropoiesis at single-cell resolution (2025) · cites this paper as Chiabrando et al., 2014

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  1. Bishop DF, Henderson AS, Astrin KH. Human delta-aminolevulinate synthase: assignment of the housekeeping gene to 3p21 and the erythroid-specific gene to the X chromosome. Genomics. 1990;7(2):207- 14.
  2. Harigae H, Suwabe N, Weinstock PH, Nagai M, Fujita H, Yamamoto M, et al. Deficient heme and globin synthesis in embryonic stem cells lacking the erythroid-specific delta-aminolevulinate synthase gene. Blood. 1998;91(3):798-805.
  3. Sadlon TJ, Dell'Oso T, Surinya KH, May BK. Regulation of erythroid 5-aminolevulinate synthase expression during erythropoiesis. Int J Biochem Cell Biol. 1999;31(10):1153-67.
  4. Kaneko K, Furuyama K, Fujiwara T, Kobayashi R, Ishida H, Harigae H, et al. Identification of the novel erythroid-specific enhancer for ALAS2 gene and its loss-of- function mutation associated with congeni- tal sideroblastic anemia. Haematologica. 2014;99(2):252-61.
  5. Surinya KH, Cox TC, May BK. Identification and characterization of a con- served erythroid-specific enhancer located in intron 8 of the human 5-aminolevulinate synthase 2 gene. J Biol Chem. 1998;273(27): 16798-809.
  6. Hentze MW, Muckenthaler MU, Andrews NC. Balancing acts: molecular control of mammalian iron metabolism. Cell. 2004;117 (3):285-97.
  7. Ajioka RS, Phillips JD, Kushner JP. Biosynthesis of heme in mammals. Biochim Biophys Acta. 2006;1763(7):723-36.
  8. Tugores A, Magness ST, Brenner DA. A sin- gle promoter directs both housekeeping and erythroid preferential expression of the human ferrochelatase gene. J Biol Chem. 1994;269(49):30789-97.
  9. Crooks DR, Ghosh MC, Haller RG, Tong WH, Rouault TA. Posttranslational stability of the heme biosynthetic enzyme fer- rochelatase is dependent on iron availability and intact iron-sulfur cluster assembly machinery. Blood. 2010;115(4):860-9.
  10. Vaisman B, Fibach E, Konijn AM. Utilization of intracellular ferritin iron for hemoglobin synthesis in developing human erythroid precursors. Blood. 1997;90(2):831-8.
  11. Sheftel AD, Zhang AS, Brown C, Shirihai OS, Ponka P. Direct interorganellar transfer of iron from endosome to mitochondrion. Blood. 2007;110(1):125-32.
  12. Paradkar PN, Zumbrennen KB, Paw BH, Ward DM, Kaplan J. Regulation of mito- chondrial iron import through differential turnover of mitoferrin 1 and mitoferrin 2. Mol Cell Biol. 2009;29(4):1007-16.
  13. Hamza I, Dailey HA. One ring to rule them all: trafficking of heme and heme synthesis intermediates in the metazoans. Biochim Biophys Acta. 2012;1823(9):1617-32.
  14. Chen W, Dailey HA, Paw BH. Ferrochelatase forms an oligomeric complex with mitoferrin-1 and Abcb10 for erythroid heme biosynthesis. Blood. 2010;116(4):628- 30.
  15. Chen W, Paradkar PN, Li L, Pierce EL, Langer NB, Takahashi-Makise N, et al. Abcb10 physically interacts with mitoferrin-1 (Slc25a37) to enhance its stability and func- tion in the erythroid mitochondria. Proc Natl Acad Sci USA. 2009;106(38):16263-8.
  16. Palmieri F. The mitochondrial transporter family (SLC25): physiological and patholog- ical implications. Pflugers Arch. 2004;447(5): 689-709.
  17. Graf SA, Haigh SE, Corson ED, Shirihai OS. Targeting, import, and dimerization of a mammalian mitochondrial ATP binding cas- sette (ABC) transporter, ABCB10 (ABC-me). J Biol Chem. 2004;279(41):42954-63.
  18. Shirihai OS, Gregory T, Yu C, Orkin SH, Weiss MJ. ABC-me: a novel mitochondrial transporter induced by GATA-1 during ery- throid differentiation. EMBO J. 2000;19(11): 2492-502.
  19. Tang L, Bergevoet SM, Bakker-Verweij G, Harteveld CL, Giordano PC, Nijtmans L, et al. Human mitochondrial ATP-binding cas- sette transporter ABCB10 is required for effi- cient red blood cell development. Br J Haematol. 2011;157(1):151-4.
  20. Hyde BB, Liesa M, Elorza AA, Qiu W, Haigh SE, Richey L, et al. The mitochondrial trans- porter ABC-me (ABCB10), a downstream target of GATA-1, is essential for erythro- poiesis in vivo. Cell Death Differ. 2012;19 (7):1117-26.
  21. Bayeva M, Khechaduri A, Wu R, Burke MA, Wasserstrom JA, Singh N, et al. ABCB10 Regulates Early Steps of Heme Synthesis. Circ Res. 2013;113(3):279-87.
  22. Krishnamurthy PC, Du G, Fukuda Y, Sun D, Sampath J, Mercer KE, et al. Identification of a mammalian mitochondrial porphyrin transporter. Nature. 2006;443(7111):586-9.
  23. Tsuchida M, Emi Y, Kida Y, Sakaguchi M. Human ABC transporter isoform B6 (ABCB6) localizes primarily in the Golgi apparatus. Biochem Biophys Res Commun. 2008;369(2):369-75.
  24. Paterson JK, Shukla S, Black CM, Tachiwada T, Garfield S, Wincovitch S, et al. Human ABCB6 localizes to both the outer mito- chondrial membrane and the plasma mem- brane. Biochemistry. 2007;46(33):9443-52.
  25. Kiss K, Brozik A, Kucsma N, Toth A, Gera M, Berry L, et al. Shifting the paradigm: the putative mitochondrial protein ABCB6 resides in the lysosomes of cells and in the plasma membrane of erythrocytes. PLoS One. 2012;7(5):e37378.
  26. Kelter G, Steinbach D, Konkimalla VB, Tahara T, Taketani S, Fiebig HH, et al. Role of transferrin receptor and the ABC trans- porters ABCB6 and ABCB7 for resistance and differentiation of tumor cells towards artesunate. PLoS One. 2007;2(8):e798.
  27. Helias V, Saison C, Ballif BA, Peyrard T, Takahashi J, Takahashi H, et al. ABCB6 is dispensable for erythropoiesis and specifies the new blood group system Langereis. Nat Genet. 2012;44(2):170-3.
  28. Wang L, He F, Bu J, Zhen Y, Liu X, Du W, et al. ABCB6 mutations cause ocular colobo- ma. Am J Hum Genet. 2012;90(1):40-8.
  29. Ulrich DL, Lynch J, Wang Y, Fukuda Y, Nachagari D, Du G, et al. ATP-dependent mitochondrial porphyrin importer ABCB6 protects against phenylhydrazine toxicity. J Biol Chem. 2012;287(16):12679-90.
  30. Chiabrando D, Marro S, Mercurio S, Giorgi C, Petrillo S, Vinchi F, et al. The mitochondr- ial heme exporter FLVCR1b mediates ery- throid differentiation. J Clin Invest. 2012; 122(12):4569-79.
  31. Fleming MD, Hamza I. Mitochondrial heme: an exit strategy at last. J Clin Invest. 2012;122(12):4328-30.
  32. Quigley JG, Yang Z, Worthington MT, Phillips JD, Sabo KM, Sabath DE, et al. Identification of a human heme exporter that is essential for erythropoiesis. Cell. 2004;118(6):757-66.
  33. Keel SB, Doty RT, Yang Z, Quigley JG, Chen J, Knoblaugh S, et al. A heme export protein is required for red blood cell differentiation and iron homeostasis. Science. 2008;319 (5864):825-8.
  34. Law CJ, Maloney PC, Wang DN. Ins and outs of major facilitator superfamily antiporters. Annu Rev Microbiol. 2008;62: 289-305.
  35. Pao SS, Paulsen IT, Saier MH Jr. Major facili- tator superfamily. Microbiol Mol Biol Rev. 1998;62(1):1-34.
  36. Vinchi F, Ingoglia G, Chiabrando D, Mercurio S, Turco E, Silengo L, et al. The Heme Exporter FLVCR1a Regulates Heme Synthesis and Degradation and Controls Activity of Cytochromes P450. Gastroenterology. 2014;146(5):1325-38.
  37. Sinclair J, Hamza I. A novel heme-respon- sive element mediates transcriptional regula- tion in Caenorhabditis elegans. J Biol Chem. 2010;285(50):39536-43.
  38. Chen JJ. Regulation of protein synthesis by the heme-regulated eIF2alpha kinase: rele- vance to anemias. Blood. 2007;109(7):2693- 9.
  39. Faller M, Matsunaga M, Yin S, Loo JA, Guo F. Heme is involved in microRNA process- ing. Nat Struct Mol Biol. 2007;14(1):23-9.
  40. Barr I, Smith AT, Chen Y, Senturia R, Burstyn JN, Guo F. Ferric, not ferrous, heme activates RNA-binding protein DGCR8 for primary microRNA processing. Proc Natl Acad Sci USA. 2012;109(6):1919-24.
  41. Munakata H, Sun JY, Yoshida K, Nakatani T, Honda E, Hayakawa S, et al. Role of the heme regulatory motif in the heme-mediat- ed inhibition of mitochondrial import of 5- aminolevulinate synthase. J Biochem. 2004;136(2):233-8.
  42. Yamamoto M, Hayashi N, Kikuchi G. Evidence for the transcriptional inhibition by heme of the synthesis of delta-aminole- vulinate synthase in rat liver. Biochem Biophys Res Commun. 1982;105(3):985-90.
  43. Yamamoto M, Hayashi N, Kikuchi G. Translational inhibition by heme of the syn- thesis of hepatic delta-aminolevulinate syn- thase in a cell-free system. Biochem Biophys Res Commun. 1983;115(1):225-31.
  44. Kramer MF, Gunaratne P, Ferreira GC. Transcriptional regulation of the murine ery- throid-specific 5-aminolevulinate synthase gene. Gene. 2000;247(1-2):153-66.
  45. Ishikawa H, Kato M, Hori H, Ishimori K, Kirisako T, Tokunaga F, et al. Involvement of heme regulatory motif in heme-mediated ubiquitination and degradation of IRP2. Mol Cell. 2005;19(2):171-81.
  46. Reichard JF, Motz GT, Puga A. Heme oxyge- nase-1 induction by NRF2 requires inactiva- tion of the transcriptional repressor BACH1. Nucleic Acids Res. 2007;35(21):7074-86.
  47. Hintze KJ, Katoh Y, Igarashi K, Theil EC. Bach1 repression of ferritin and thioredoxin reductase1 is heme-sensitive in cells and in vitro and coordinates expression with heme oxygenase1, beta-globin, and NADP(H) quinone (oxido) reductase1. J Biol Chem. 2007;282(47):34365-71.
  48. Tahara T, Sun J, Igarashi K, Taketani S. Heme-dependent up-regulation of the alpha-globin gene expression by transcrip- tional repressor Bach1 in erythroid cells. Biochem Biophys Res Commun. 2004;324 (1):77-85.
  49. Tahara T, Sun J, Nakanishi K, Yamamoto M, Mori H, Saito T, et al. Heme positively regu- lates the expression of beta-globin at the locus control region via the transcriptional factor Bach1 in erythroid cells. J Biol Chem. 2004;279(7):5480-7.
  50. Marro S, Chiabrando D, Messana E, Stolte J, Turco E, Tolosano E, et al. Heme controls ferroportin1 (FPN1) transcription involving Bach1, Nrf2 and a MARE/ARE sequence motif at position -7007 of the FPN1 promot- er. Haematologica. 2010;95(8):1261-8.
  51. Ogawa K, Sun J, Taketani S, Nakajima O, Nishitani C, Sassa S, et al. Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1. EMBO J. 2001;20(11):2835- 43.
  52. Suzuki H, Tashiro S, Hira S, Sun J, Yamazaki C, Zenke Y, et al. Heme regulates gene expression by triggering Crm1-dependent nuclear export of Bach1. EMBO J. 2004;23(13):2544-53.
  53. Zenke-Kawasaki Y, Dohi Y, Katoh Y, Ikura T, Ikura M, Asahara T, et al. Heme induces ubiquitination and degradation of the tran- scription factor Bach1. Mol Cell Biol. 2007;27(19):6962-71.
  54. Nguyen T, Yang CS, Pickett CB. The path- ways and molecular mechanisms regulating Nrf2 activation in response to chemical stress. Free Radic Biol Med. 2004;37(4):433- 41.
  55. Eggler AL, Liu G, Pezzuto JM, van Breemen RB, Mesecar AD. Modifying specific cys- teines of the electrophile-sensing human Keap1 protein is insufficient to disrupt bind- ing to the Nrf2 domain Neh2. Proc Natl Acad Sci USA. 2005;102(29):10070-5.
  56. Crosby JS, Lee K, London IM, Chen JJ. Erythroid expression of the heme-regulated eIF-2 alpha kinase. Mol Cell Biol. 1994;14 (6):3906-14.
  57. Han AP, Yu C, Lu L, Fujiwara Y, Browne C, Chin G, et al. Heme-regulated eIF2alpha kinase (HRI) is required for translational reg- ulation and survival of erythroid precursors in iron deficiency. EMBO J. 2001;20(23): 6909-18.
  58. Han AP, Fleming MD, Chen JJ. Heme-regu- lated eIF2alpha kinase modifies the pheno- typic severity of murine models of erythro- poietic protoporphyria and beta-tha- lassemia. J Clin Invest. 2005;115(6):1562-70.
  59. Masuoka HC, Townes TM. Targeted disrup- tion of the activating transcription factor 4 gene results in severe fetal anemia in mice. Blood. 2002;99(3):736-45.
  60. Suragani RN, Zachariah RS, Velazquez JG, Liu S, Sun CW, Townes TM, et al. Heme- regulated eIF2alpha kinase activated Atf4 signaling pathway in oxidative stress and erythropoiesis. Blood. 2012;119(22):5276- 84.
  61. Fleming MD. Congenital sideroblastic ane- mias: iron and heme lost in mitochondrial translation. Hematology Am Soc Hematol Educ Program. 2011;2011:525-31.
  62. Sheftel AD, Richardson DR, Prchal J, Ponka P. Mitochondrial iron metabolism and sider- oblastic anemia. Acta Haematol. 2009;122 (2-3):120-33.
  63. Nakajima O, Takahashi S, Harigae H, Furuyama K, Hayashi N, Sassa S, et al. Heme deficiency in erythroid lineage causes differentiation arrest and cytoplasmic iron overload. EMBO J. 1999;18(22):6282-9.
  64. Brownlie A, Donovan A, Pratt SJ, Paw BH, Oates AC, Brugnara C, et al. Positional cloning of the zebrafish sauternes gene: a model for congenital sideroblastic anaemia. Nat Genet. 1998;20(3):244-50.
  65. Pondarre C, Antiochos BB, Campagna DR, Clarke SL, Greer EL, Deck KM, et al. The mitochondrial ATP-binding cassette trans- porter Abcb7 is essential in mice and partic- ipates in cytosolic iron-sulfur cluster biogen- esis. Hum Mol Genet. 2006;15(6):953-64.
  66. Clarke SL, Vasanthakumar A, Anderson SA, Pondarre C, Koh CM, Deck KM, et al. Iron- responsive degradation of iron-regulatory protein 1 does not require the Fe-S cluster. EMBO J. 2006;25(3):544-53.
  67. Tutois S, Montagutelli X, Da Silva V, Jouault H, Rouyer-Fessard P, Leroy-Viard K, et al. Erythropoietic protoporphyria in the house mouse. A recessive inherited ferrochelatase deficiency with anemia, photosensitivity, and liver disease. J Clin Invest. 1991;88(5): 1730-6.
  68. Magness ST, Maeda N, Brenner DA. An exon 10 deletion in the mouse ferrochelatase gene has a dominant-negative effect and causes mild protoporphyria. Blood. 2002;100(4):1470-7.
  69. Childs S, Weinstein BM, Mohideen MA, Donohue S, Bonkovsky H, Fishman MC. Zebrafish dracula encodes ferrochelatase and its mutation provides a model for ery- thropoietic protoporphyria. Curr Biol. 2000;10(16):1001-4.
  70. Cooperman SS, Meyron-Holtz EG, Olivierre-Wilson H, Ghosh MC, McConnell JP, Rouault TA. Microcytic anemia, erythro- poietic protoporphyria, and neurodegenera- tion in mice with targeted deletion of iron- regulatory protein 2. Blood. 2005;106(3): 1084-91.
  71. Bishop DF, Johansson A, Phelps R, Shady AA, Ramirez MC, Yasuda M, et al. Uroporphyrinogen III synthase knock-in mice have the human congenital erythropoi- etic porphyria phenotype, including the characteristic light-induced cutaneous lesions. Am J Hum Genet. 2006;78(4):645- 58.
  72. Ged C, Mendez M, Robert E, Lalanne M, Lamrissi-Garcia I, Costet P, et al. A knock-in mouse model of congenital erythropoietic porphyria. Genomics. 2006;87(1):84-92.
  73. Phillips JD, Jackson LK, Bunting M, Franklin MR, Thomas KR, Levy JE, et al. A mouse model of familial porphyria cutanea tarda. Proc Natl Acad Sci USA. 2001;98(1):259-64.
  74. Wang H, Long Q, Marty SD, Sassa S, Lin S. A zebrafish model for hepatoerythropoietic porphyria. Nat Genet. 1998;20(3):239-43.
  75. Mori M, Gotoh S, Taketani S, Hiai H, Higuchi K. Hereditary cataract of the Nakano mouse: Involvement of a hypomor- phic mutation in the coproporphyrinogen oxidase gene. Exp Eye Res. 2013;112:45-50.
  76. Ducamp S, Kannengiesser C, Touati M, Garcon L, Guerci-Bresler A, Guichard JF, et al. Sideroblastic anemia: molecular analysis of the ALAS2 gene in a series of 29 probands and functional studies of 10 missense muta- tions. Hum Mutat. 2011;32(6):590-7.
  77. Bergmann AK, Campagna DR, McLoughlin EM, Agarwal S, Fleming MD, Bottomley SS, et al. Systematic molecular genetic analysis of congenital sideroblastic anemia: evidence for genetic heterogeneity and identification of novel mutations. Pediatr Blood Cancer. 2010;54(2):273-8.
  78. Cotter PD, Baumann M, Bishop DF. Enzymatic defect in "X-linked" sideroblastic anemia: molecular evidence for erythroid delta-aminolevulinate synthase deficiency. Proc Natl Acad Sci USA. 1992;89(9):4028-32.
  79. Camaschella C. Hereditary sideroblastic anemias: pathophysiology, diagnosis, and treatment. Semin Hematol. 2009;46(4):371- 7.
  80. Kannengiesser C, Sanchez M, Sweeney M, Hetet G, Kerr B, Moran E, et al. Missense SLC25A38 variations play an important role in autosomal recessive inherited sideroblas- tic anemia. Haematologica. 2011;96(6):808- 13.
  81. Allikmets R, Raskind WH, Hutchinson A, Schueck ND, Dean M, Koeller DM. Mutation of a putative mitochondrial iron transporter gene (ABC7) in X-linked siderob- lastic anemia and ataxia (XLSA/A). Hum Mol Genet. 1999;8(5):743-9.
  82. Ye H, Jeong SY, Ghosh MC, Kovtunovych G, Silvestri L, Ortillo D, et al. Glutaredoxin 5 deficiency causes sideroblastic anemia by specifically impairing heme biosynthesis and depleting cytosolic iron in human ery- throblasts. J Clin Invest. 2010;120(5):1749- 61.
  83. Balwani M, Desnick RJ. The porphyrias: advances in diagnosis and treatment. Blood. 2012;120(23):4496-504.
  84. Sassa S, Kappas A. Molecular aspects of the inherited porphyrias. J Intern Med. 2000;247 (2):169-78.
  85. Gouya L, Puy H, Robreau AM, Bourgeois M, Lamoril J, Da Silva V, et al. The penetrance of dominant erythropoietic protoporphyria is modulated by expression of wildtype FECH. Nat Genet. 2002;30(1):27-8.
  86. Lecha M, Puy H, Deybach JC. Erythropoietic protoporphyria. Orphanet J Rare Dis. 2009;4:19.
  87. Holme SA, Worwood M, Anstey AV, Elder GH, Badminton MN. Erythropoiesis and iron metabolism in dominant erythropoietic protoporphyria. Blood. 2007;110(12):4108- 10.
  88. Rademakers LH, Koningsberger JC, Sorber CW, Baart de la Faille H, Van Hattum J, Marx JJ. Accumulation of iron in erythroblasts of patients with erythropoietic protoporphyria. Eur J Clin Invest. 1993;23(2):130-8.
  89. Whatley SD, Ducamp S, Gouya L, Grandchamp B, Beaumont C, Badminton MN, et al. C-terminal deletions in the ALAS2 gene lead to gain of function and cause X-linked dominant protoporphyria without anemia or iron overload. Am J Hum Genet. 2008;83(3):408-14.
  90. Schmitt C, Gouya L, Malonova E, Lamoril J, Camadro JM, Flamme M, et al. Mutations in human CPO gene predict clinical expression of either hepatic hereditary coproporphyria or erythropoietic harderoporphyria. Hum Mol Genet. 2005;14(20):3089-98.

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Authors
Chiabrando, D., Mercurio, S., & Tolosano, E.
Affiliations
University of Turin (IT)
ORCID
Venue
Haematologica
Publisher
Ferrata Storti Foundation (Haematologica)
Published
2014-05-31
Volume
99
Issue
6
Pages
973-983
ISSN
  • 0390-6078 (ISSN-L)
  • 1592-8721
DOI
10.3324/haematol.2013.091991
PMC
PMC4040894
OpenAlex
W2049116122
Cited by
192
References
9
Citations by year
2026: 11 · 2025: 25 · 2024: 11 · 2023: 20 · 2022: 18 · 2021: 22 · 2020: 22 · 2019: 16 · 2018: 18 · 2017: 10 · 2016: 8 · 2015: 9
FWCI
0.85
Type
journal article
Language
en
Open access
Locations
  • Haematologica (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Institutional Research Information System University of Turin (University of Turin) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
Regione Piemonte
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Porphyrin Metabolism and Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hemoglobin structure and function
  • Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
Keywords
heme biosynthesis, erythropoiesis, erythroid differentiation, hemoglobin, sideroblastic anemia, erythropoietic porphyria, heme deficiency, proerythroblasts, mitochondrial iron overload
MeSH terms
Animals, Cell Differentiation, Erythrocytes, Erythropoiesis, Gene Expression Regulation, Hematologic Diseases, Heme, Humans, Mitochondria, Biosynthetic Pathways

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