Distinct mechanisms of inadequate erythropoiesis induced by tumor necrosis factor alpha or malarial pigment

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Lamikanra, Abigail A ^a,b   Merryweather Clarke, Alison T ^a,b   Tipping, Alex J ^a,b   Roberts, David J ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; HEMOZOIN; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA; HEMOPROTEIN; INTERFERON; TUMOR NECROSIS FACTOR;

ANEMIA; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CELL STRESS; DNA REPAIR; DOWN REGULATION; ENRICHMENT CULTURE; ERYTHROBLAST; ERYTHROID CELL; ERYTHROPOIESIS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE IDENTIFICATION; GENE ONTOLOGY; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; INFLAMMATION; MALARIA; MALARIA ANEMIA; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STRESS; TRANSCRIPTION REGULATION; CELLULAR IMMUNITY; CYTOLOGY; DRUG EFFECTS; ERYTHROCYTE; GENE EXPRESSION REGULATION; GENETICS; HEMATOLOGIC DISEASES; HUMAN; METABOLISM; PARASITOLOGY; PHYSIOLOGY;

PLASMODIUM FALCIPARUM;

APOPTOSIS; CELLS, CULTURED; ERYTHROCYTES; ERYTHROPOIESIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEMATOLOGIC DISEASES; HEMEPROTEINS; HUMANS; IMMUNITY, CELLULAR; INTERFERONS; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84924942700     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119836     Document Type: Article

References (63)

1. WHO. World Malaria Report 2013. WHO Press, 2013.
2. Okiro EA, Kazembe LN, Kabaria CW, Ligomeka J, Noor AM, Ali D, et al. Childhood malaria admission rates to four hospitals in Malawi between 2000 and 2010. PloS one. 2013; 8(4):e62214. Epub 2013/05/03. doi: 10.1371/journal.pone.0062214 PMID: 23638008
3. Douglas NM, Lampah DA, Kenangalem E, Simpson JA, Poespoprodjo JR, Sugiarto P, et al. Major burden of severe anemia from non-falciparum malaria species in Southern Papua: a hospital-based surveillance study. PLoS medicine. 2013; 10(12):e1001575; discussion e. Epub 2013/12/21. doi: 10.1371/journal.pmed.1001575 PMID: 24358031
4. Weatherall DJ, Miller LH, Baruch DI, Marsh K, Doumbo OK, Casals-Pascual C, et al. Malaria and the red cell. Hematology (Am Soc Hematol Educ Program). 2002:35-57.
5. Lamikanra AA, Brown D, Potocnik A, Casals-Pascual C, Langhorne J, Roberts DJ. Malarial anemia: of mice and men. Blood. 2007; 110(1):18-28. PMID: 17341664
6. Portugal S, Carret C, Recker M, Armitage AE, Goncalves LA, Epiphanio S, et al. Host-mediated regulation of superinfection in malaria. Nat Med. 2011; 17(6):732-7. Epub 2011/05/17. doi: 10.1038/nm.2368 PMID: 21572427
7. Casals-Pascual C, Huang H, Lakhal-Littleton S, Thezenas ML, Kai O, Newton CR, et al. Hepcidin demonstrates a biphasic association with anemia in acute Plasmodium falciparum malaria. Haematologica. 2012; 97(11):1695-8. Epub 2012/06/13. doi: 10.3324/haematol.2012.065854 PMID: 22689680
8. Abdalla S, Weatherall DJ, Wickramasinghe SN, Hughes M. The anaemia of P. falciparum malaria. Br J Haematol. 1980; 46(2):171-83. PMID: 7000157
9. Casals-Pascual C, Kai O, Cheung JO, Williams S, Lowe B, Nyanoti M, et al. Suppression of erythropoiesis in malarial anemia is associated with hemozoin in vitro and in vivo. Blood. 2006.
10. Phillips RE, Pasvol G. Anaemia of Plasmodium falciparum malaria. Baillieres Clin Haematol. 1992; 5 (2):315-30. PMID: 1511178
11. Menendez C, Fleming AF, Alonso PL. Malaria-related anaemia. Parasitol Today. 2000; 16(11):469-76. PMID: 11063857
12. Abdalla SH, Wickramasinghe SN, Weatherall DJ. The deoxyuridine suppression test in severe anaemia following Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg. 1984; 78(1):60-3. PMID: 6369652
13. Dormer P, Dietrich M, Kern P, Horstmann RD. Ineffective erythropoiesis in acute human P. falciparum malaria. Blut. 1983; 46(5):279-88. PMID: 6340761
14. Kurtzhals JA, Adabayeri V, Goka BQ, Akanmori BD, Oliver-Commey JO, Nkrumah FK, et al. Low plasma concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria. Lancet. 1998; 351(9118):1768-72. PMID: 9635949
15. Othoro C, Lal AA, Nahlen B, Koech D, Orago AS, Udhayakumar V. A low interleukin-10 tumor necrosis factor-alpha ratio is associated with malaria anemia in children residing in a holoendemic malaria region in western Kenya. J Infect Dis. 1999; 179(1):279-82. PMID: 9841855
16. Giribaldi G, Prato M, Ulliers D, Gallo V, Schwarzer E, Akide-Ndunge OB, et al. Involvement of inflammatory chemokines in survival of human monocytes fed with malarial pigment. Infect Immun. 2010; 78 (11):4912-21. Epub 2010/08/25. doi: 10.1128/IAI.00455-10 PMID: 20732999
17. Pagola S, Stephens PW, Bohle DS, Kosar AD, Madsen SK. The structure of malaria pigment beta-haematin. Nature. 2000; 404(6775):307-10. PMID: 10749217
18. Goldie P, Roth EF Jr., Oppenheim J, Vanderberg JP. Biochemical characterization of Plasmodium falciparum hemozoin. Am J Trop Med Hyg. 1990; 43(6):584-96. Epub 1990/12/01. PMID: 2267961
19. Schwarzer E, Kuhn H, Valente E, Arese P. Malaria-parasitized erythrocytes and hemozoin nonenzymatically generate large amounts of hydroxy fatty acids that inhibit monocyte functions. Blood. 2003; 101(2):722-8. PMID: 12393662
20. Papadaki HA, Kritikos HD, Valatas V, Boumpas DT, Eliopoulos GD. Anemia of chronic disease in rheumatoid arthritis is associated with increased apoptosis of bone marrow erythroid cells: improvement following anti-tumor necrosis factor-alpha antibody therapy. Blood. 2002; 100(2):474-82. PMID: 12091338
21. Rusten LS, Jacobsen SE. Tumor necrosis factor (TNF)-alpha directly inhibits human erythropoiesis in vitro: role of p55 and p75 TNF receptors. Blood. 1995; 85(4):989-96. Epub 1995/02/15. PMID: 7849320
22. Morceau F, Dicato M, Diederich M. Pro-inflammatory cytokine-mediated anemia: regarding molecular mechanisms of erythropoiesis. Mediators Inflamm. 2009; 2009:405016. Epub 2009/01/01. doi: 10.1155/2009/405016 PMID: 20204172
23. Lamikanra AA, Theron M, Kooij TW, Roberts DJ. Hemozoin (malarial pigment) directly promotes apoptosis of erythroid precursors. PloS one. 2009; 4(12):e8446. doi: 10.1371/journal.pone.0008446 PMID: 20041181
24. Skorokhod OA, Caione L, Marrocco T, Migliardi G, Barrera V, Arese P, et al. Inhibition of erythropoiesis in malaria anemia: role of hemozoin and hemozoin-generated 4-hydroxynonenal. Blood. 2010; 116 (20):4328-37. doi: 10.1182/blood-2010-03-272781 PMID: 20686121
25. Irizarry R, Hobbs B, Collin F, Beazer-Barclay Y, Antonellis K, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003:249-64. PMID: 12925520
26. Merryweather-Clarke AT, Atzberger A, Soneji S, Gray N, Clark K, Waugh C, et al. Global gene expression analysis of human erythroid progenitors. Blood. 2011; 117(13):e96-108. doi: 10.1182/blood-2010-07-290825 PMID: 21270440
27. Tabas-Madrid D, Nogales-Cadenas R, Pascual-Montano A. GeneCodis3: a non-redundant and modular enrichment analysis tool for functional genomics. Nucleic acids research. 2012; 40(Web Server issue):W478-83. Epub 2012/05/11. doi: 10.1093/nar/gks402 PMID: 22573175
28. Hercus TR, Thomas D, Guthridge MA, Ekert PG, King-Scott J, Parker MW, et al. The granulocyte-macrophage colony-stimulating factor receptor: linking its structure to cell signaling and its role in disease. Blood. 2009; 114(7):1289-98. Epub 2009/05/14. doi: 10.1182/blood-2008-12-164004 PMID: 19436055
29. Kim R, Emi M, Tanabe K, Murakami S. Role of the unfolded protein response in cell death. Apoptosis. 2006; 11(1):5-13. Epub 2005/12/24. PMID: 16374548
30. Ellisen LW, Ramsayer KD, Johannessen CM, Yang A, Beppu H, Minda K, et al. REDD1, a developmentally regulated transcriptional target of p63 and p53, links p63 to regulation of reactive oxygen species. Molecular cell. 2002; 10(5):995-1005. PMID: 12453409
31. Blencowe BJ. Splicing regulation: the cell cycle connection. Curr Biol. 2003; 13(4):R149-51. Epub 2003/02/21. PMID: 12593819
32. Bulinski JC, Odde DJ, Howell BJ, Salmon TD, Waterman-Storer CM. Rapid dynamics of the microtubule binding of ensconsin in vivo. J Cell Sci. 2001; 114(Pt 21):3885-97. Epub 2001/11/24.
33. Nousiainen M, Sillje HH, Sauer G, Nigg EA, Korner R. Phosphoproteome analysis of the human mitotic spindle. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103 (14):5391-6. Epub 2006/03/28. PMID: 16565220
34. Griffiths MJ, Shafi MJ, Popper SJ, Hemingway CA, Kortok MM, Wathen A, et al. Genomewide analysis of the host response to malaria in Kenyan children. J Infect Dis. 2005; 191(10):1599-611. PMID: 15838786
35. Sexton AC, Good RT, Hansen DS, D'Ombrain MC, Buckingham L, Simpson K, et al. Transcriptional profiling reveals suppressed erythropoiesis, up-regulated glycolysis, and interferon-associated responses in murine malaria. J Infect Dis. 2004; 189(7):1245-56. PMID: 15031794
36. Awandare GA, Kempaiah P, Ochiel DO, Piazza P, Keller CC, Perkins DJ. Mechanisms of erythropoiesis inhibition by malarial pigment and malaria-induced proinflammatory mediators in an in vitro model. Am J Hematol. 2011; 86(2):155-62. Epub 2011/01/26. doi: 10.1002/ajh.21933 PMID: 21264897
37. Aguilar R, Magallon-Tejada A, Achtman AH, Moraleda C, Joice R, Cistero P, et al. Molecular evidence for the localization of Plasmodium falciparum immature gametocytes in bone marrow. Blood. 2014; 123 (7):959-66. Epub 2013/12/18. doi: 10.1182/blood-2013-08-520767 PMID: 24335496
38. Betin VM, Singleton BK, Parsons SF, Anstee DJ, Lane JD. Autophagy facilitates organelle clearance during differentiation of human erythroblasts: evidence for a role for ATG4 paralogs during autophagosome maturation. Autophagy. 2013; 9(6):881-93. Epub 2013/03/20. doi: 10.4161/auto.24172 PMID: 23508006
39. Grigorakaki C, Morceau F, Chateauvieux S, Dicato M, Diederich M. Tumor necrosis factor alpha-mediated inhibition of erythropoiesis involves GATA-1/GATA-2 balance impairment and PU.1 over-expression. Biochem Pharmacol. 2011; 82(2):156-66. Epub 2011/04/20. doi: 10.1016/j.bcp.2011.03.030 PMID: 21501595
40. Zhang L, Miles MF, Aldape KD. A model of molecular interactions on short oligonucleotide microarrays. Nat Biotechnol. 2003; 21(7):818-21. Epub 2003/06/10. PMID: 12794640
41. th 2011]. Available from: https://cellline.molbiol.ox.ac.uk/eryth/index.html.
42. Vallabhapurapu S, Karin M. Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol. 2009; 27:693-733. Epub 2009/03/24. doi: 10.1146/annurev.immunol. 021908.132641 PMID: 19302050
43. Bohmer RM. IL-3-dependent early erythropoiesis is stimulated by autocrine transforming growth factor beta. Stem cells (Dayton, Ohio). 2004; 22(2):216-24.
44. Goodman JW, Hall EA, Miller KL, Shinpock SG. Interleukin 3 promotes erythroid burst formation in "serum-free" cultures without detectable erythropoietin. Proceedings of the National Academy of Sciences of the United States of America. 1985; 82(10):3291-5. PMID: 3923475
45. Ubeda M, Vallejo M, Habener JF. CHOP enhancement of gene transcription by interactions with Jun/Fos AP-1 complex proteins. Molecular and cellular biology. 1999; 19(11):7589-99. PMID: 10523647
46. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Molecular and cellular biology. 2001; 21(4):1249-59. PMID: 11158311
47. Unal E, Heidinger-Pauli JM, Koshland D. DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science (New York, NY. 2007; 317(5835):245-8. PMID: 17626885
48. Gordillo M, Vega H, Trainer AH, Hou F, Sakai N, Luque R, et al. The molecular mechanism underlying Roberts syndrome involves loss of ESCO2 acetyltransferase activity. Human molecular genetics. 2008; 17(14):2172-80. doi: 10.1093/hmg/ddn116 PMID: 18411254
49. Monnich M, Kuriger Z, Print CG, Horsfield JA. A zebrafish model of Roberts syndrome reveals that Esco2 depletion interferes with development by disrupting the cell cycle. PloS one. 2011; 6(5):e20051. Epub 2011/06/04. doi: 10.1371/journal.pone.0020051 PMID: 21637801
50. Zhou Y, Zhang E, Berggreen C, Jing X, Osmark P, Lang S, et al. Survival of pancreatic beta cells is partly controlled by a TCF7L2-p53-p53INP1-dependent pathway. Human molecular genetics. 2012; 21 (1):196-207. Epub 2011/10/04. doi: 10.1093/hmg/ddr454 PMID: 21965303
51. Botuyan MV, Lee J, Ward IM, Kim JE, Thompson JR, Chen J, et al. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell. 2006; 127 (7):1361-73. Epub 2006/12/28. PMID: 17190600
52. Bailis JM, Forsburg SL. MCM proteins: DNA damage, mutagenesis and repair. Curr Opin Genet Dev. 2004; 14(1):17-21. Epub 2004/04/28. PMID: 15108800
53. Scian MJ, Carchman EH, Mohanraj L, Stagliano KE, Anderson MA, Deb D, et al. Wild-type p53 and p73 negatively regulate expression of proliferation related genes. Oncogene. 2008; 27(18):2583-93. Epub 2007/11/06. PMID: 17982488
54. Schrimpe AC, Wright DW. Comparative analysis of gene expression changes mediated by individual constituents of hemozoin. Chem Res Toxicol. 2009; 22(3):433-45. Epub 2009/02/05. doi: 10.1021/tx8002752 PMID: 19191707
55. Lin MH, Yen JH, Weng CY, Wang L, Ha CL, Wu MJ. Lipid peroxidation end product 4-hydroxy-trans-2-nonenal triggers unfolded protein response and heme oxygenase-1 expression in PC12 cells: Roles of ROS and MAPK pathways. Toxicology. 2014; 315:24-37. Epub 2013/12/03. doi: 10.1016/j.tox.2013. 11.007 PMID: 24291486
56. Tamez PA, Liu H, Wickrema A, Haldar K. P. falciparum modulates erythroblast cell gene expression in signaling and erythrocyte production pathways. PloS one. 2011; 6(5):e19307. Epub 2011/05/17. doi: 10.1371/journal.pone.0019307 PMID: 21573240
57. Trager W, Jensen JB. Human malaria parasites in continuous culture. Science (New York, NY. 1976; 193(4254):673-5. PMID: 781840
58. Roberts DJ, Craig AG, Berendt AR, Pinches R, Nash G, Marsh K, et al. Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature. 1992; 357(6380):689-92. PMID: 1614515
59. Fibach E, Manor D, Oppenheim A, Rachmilewitz EA. Proliferation and maturation of human erythroid progenitors in liquid culture. Blood. 1989; 73(1):100-3. PMID: 2910352
60. Inger L, Hedvig P, Martha S, Artur S, Mats W, editors. Methods In Malaria Research. Fourth ed: MR4. ATCC; 2004.
61. Sullivan DJ Jr., Gluzman IY, Russell DG, Goldberg DE. On the molecular mechanism of chloroquine's antimalarial action. Proceedings of the National Academy of Sciences of the United States of America. 1996; 93(21):11865-70. PMID: 8876229
62. Sturn A, Quackenbush J, Trajanoski Z. Genesis: cluster analysis of microarray data. Bioinformatics. 2002; 18(1):207-8. Epub 2002/02/12. PMID: 11836235
63. Jesnowski R, Backhaus C, Ringel J, Lohr M. Ribosomal highly basic 23-kDa protein as a reliable standard for gene expression analysis. Pancreatology. 2002; 2(4):421-4. Epub 2002/07/26. PMID: 12138232