Adenosine monophosphate deaminase 3 activation shortens erythrocyte half-life and provides malaria resistance in mice

Blood

Volumn 128, Issue 9, 2016, Pages 1290-1301

  Hortle, Elinor ^a   Nijagal, Brunda ^b   Bauer, Denis C ^c   Jensen, Lora M ^a   Ahn, Seong Beom ^d   Cockburn, Ian A ^a   Lampkin, Shelley ^a   Tull, Dedreia ^b   McConville, Malcolm J ^b   McMorran, Brendan J ^a   Foote, Simon J ^a   Burgio, Gaetan ^a  

^a Australian National University   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c CSIRO   (Australia)

^d MACQUARIE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE MONOPHOSPHATE DEAMINASE; ADENOSINE MONOPHOSPHATE DEAMINASE 3; ADENOSINE TRIPHOSPHATE; BILIRUBIN; ETHYLNITROSOUREA; GUANOSINE TRIPHOSPHATE; UNCLASSIFIED DRUG; AMPD3 PROTEIN, MOUSE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMALARIAL DRUG RESISTANCE; ARTICLE; BILIRUBIN BLOOD LEVEL; CELL AGING; CONTROLLED STUDY; ENZYME ACTIVATION; ERYPTOSIS; ERYTHROCYTE LIFESPAN; ERYTHROPOIESIS; GAIN OF FUNCTION MUTATION; INDUCED MUTATION; MACROCYTIC ANEMIA; MALE; MOUSE; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; OSMOTIC FRAGILITY; PLASMODIUM BERGHEI INFECTION; PLASMODIUM CHABAUDI INFECTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RETICULOCYTOSIS; SENESCENCE; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; ERYTHROCYTE; GENETICS; HALF LIFE TIME; IMMUNOLOGY; INNATE IMMUNITY; MALARIA; MUTATION; PARASITOLOGY; PLASMODIUM CHABAUDI;

AMP DEAMINASE; ANIMALS; CELL AGING; ERYTHROCYTES; ERYTHROPOIESIS; ETHYLNITROSOUREA; HALF-LIFE; IMMUNITY, INNATE; MALARIA; MALE; MICE; MUTATION; PLASMODIUM CHABAUDI;

EID: 84995677797     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2015-09-666834     Document Type: Article

References (46)

1. Kurata M, Suzuki M, Agar NS. Antioxidant systems and erythrocyte life-span in mammals. Comp Biochem Physiol B. 1993;106(3):477-487.
2. Lang E, Qadri SM, Lang F. Killing me softly - suicidal erythrocyte death. Int J Biochem Cell Biol. 2012;44(8):1236-1243.
3. Bosman GJ, Werre JM, Willekens FL, Novotný VM. Erythrocyte ageing in vivo and in vitro: structural aspects and implications for transfusion. Transfus Med. 2008;18(6):335-347.
4. Mock DM, Widness JA, Veng-Pedersen P, et al. Measurement of posttransfusion red cell survival with the biotin label. Transfus Med Rev. 2014; 28(3):114-125.
5. Tchernia G, Gauthier F, Mielot F, et al. Initial assessment of the beneficial effect of partial splenectomy in hereditary spherocytosis. Blood. 1993;81(8):2014-2020.
6. Lang F, Qadri SM. Mechanisms and significance of eryptosis, the suicidal death of erythrocytes. Blood Purif. 2012;33(1-3):125-130.
7. Kean LS, Brown LE, Nichols JW, Mohandas N, Archer DR, Hsu LL. Comparison of mechanisms of anemia in mice with sickle cell disease and beta-thalassemia: peripheral destruction, ineffective erythropoiesis, and phospholipid scramblase-mediated phosphatidylserine exposure. Exp Hematol. 2002;30(5):394-402.
8. Lang PA, Schenck M, Nicolay JP, et al. Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat Med. 2007; 13(2):164-170.
9. Cappellini MD, Fiorelli G. Glucose-6-phosphate dehydrogenase deficiency. Lancet. 2008; 371(9606):64-74.
10. Lelliott PM, McMorran BJ, Foote SJ, Burgio G. The influence of host genetics on erythrocytes and malaria infection: is there therapeutic potential? Malar J. 2015;14:289.
11. Malaria Genomic Epidemiology Network. Reappraisal of known malaria resistance loci in a large multicenter study. Nat Genet. 2014;46(11): 1197-1204.
12. Koka S, Föller M, Lamprecht G, et al. Iron deficiency influences the course of malaria in Plasmodium berghei infected mice. Biochem Biophys Res Commun. 2007;357(3):608-614.
13. Foller M, Bobbala D, Koka S, Huber SM, Gulbins E, Lang F. Suicide for survival: death of infected erythrocytes as a host mechanism to survive malaria. Cell Physiol Biochem. 2009;24(3-4): 133-140.
14. Totino PR, Daniel-Ribeiro CT, Ferreira-da-Cruz MF. Refractoriness of eryptotic red blood cells to Plasmodium falciparum infection: a putative host defense mechanism limiting parasitaemia. PLoS One. 2011;6(10):e26575.
15. Bhavsar SK, Gu S, Bobbala D, Lang F. Janus kinase 3 is expressed in erythrocytes, phosphorylated upon energy depletion and involved in the regulation of suicidal erythrocyte death. Cell Physiol Biochem. 2011;27(5):547-556.
16. Hitomi Y, Cirulli ET, Fellay J, et al. Inosine triphosphate protects against ribavirin-induced adenosine triphosphate loss by adenylosuccinate synthase function. Gastroenterology. 2011; 140(4):1314-1321.
17. Sabina RL, Wandersee NJ, Hillery CA. Ca2+-CaM activation of AMP deaminase contributes to adenine nucleotide dysregulation and phosphatidylserine externalization in human sickle erythrocytes. Br J Haematol. 2009;144(3): 434-445.
18. Tavazzi B, Di Pierro D, Amorini AM, et al. Energy metabolism and lipid peroxidation of human erythrocytes as a function of increased oxidative stress. Eur J Biochem. 2000;267(3):684-689.
19. Mahnke DK, Sabina RL. Calcium activates erythrocyte AMP deaminase [isoform E (AMPD3)] through a protein-protein interaction between calmodulin and the N-terminal domain of the AMPD3 polypeptide. Biochemistry. 2005;44(14): 5551-5559.
20. Bauer DC, McMorran BJ, Foote SJ, Burgio G. Genome-wide analysis of chemically induced mutations in mouse in phenotype-driven screens. BMC Genomics. 2015;16(1):866.
21. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754-1760.
22. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4): 357-359.
23. Li H, Handsaker B, Wysoker A, et al; 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and SAM tools. Bioinformatics. 2009;25(16):2078-2079.
24. McKenna A, Hanna M, Banks E, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20(9): 1297-1303.
25. Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010;38(16):e164.
26. Laemmli U. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-685.
27. Creek DJ, Jankevics A, Burgess KE, Breitling R, Barrett MP. IDEOM: an Excel interface for analysis of LC-MS-based metabolomics data. Bioinformatics. 2012;28(7):1048-1049.
28. Dunn WB, Erban A, Weber RJM, et al. Mass appeal: metabolite identification in mass spectrometry-focused untargeted metabolomics. Metabolomics. 2013;9(1):S44-S66.
29. Sumner LW, Amberg A, Barrett D, et al. Proposed minimum reporting standards for chemical analysis Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI). Metabolomics. 2007;3(3):211-221.
30. Chen K, Liu J, Heck S, Chasis JA, An X, Mohandas N. Resolving the distinct stages in erythroid differentiation based on dynamic changes in membrane protein expression during erythropoiesis. Proc Natl Acad Sci USA. 2009; 106(41):17413-17418.
31. Lelliott PM, Lampkin S, McMorran BJ, Foote SJ, Burgio G. A flow cytometric assay to quantify invasion of red blood cells by rodent Plasmodium parasites in vivo. Malar J. 2014;13:100.
32. Yap GS, Stevenson MM. Plasmodium chabaudi AS: erythropoietic responses during infection in resistant and susceptible mice. Exp Parasitol. 1992;75(3):340-352.
33. Min-Oo G, Fortin A, Tam MF, Nantel A, Stevenson MM, Gros P. Pyruvate kinase deficiency in mice protects against malaria. Nat Genet. 2003;35(4):357-362.
34. Chang KH, Stevenson MM. Malarial anaemia: mechanisms and implications of insufficient erythropoiesis during blood-stage malaria. Int J Parasitol. 2004;34(13-14):1501-1516.
35. Lowy B, Dorfman BZ. Adenylosuccinase activity in human and rabbit erythrocyte lysates. J Biol Chem. 1970;245(12):3043-3046.
36. Lowy BA, Williams MK, London IM. Enzymatic deficiencies of purine nucleotide synthesis in the human erythrocyte. J Biol Chem. 1962;237: 1622-1625.
37. Bader-Meunier B, Gauthier F, Archambaud F, et al. Long-term evaluation of the beneficial effect of subtotal splenectomy for management of hereditary spherocytosis. Blood. 2001;97(2): 399-403.
38. Lang E, Lang F. Mechanisms and pathophysiological significance of eryptosis, the suicidal erythrocyte death. Semin Cell Dev Biol. 2015;39:35-42.
39. Weiden PL, Robinett B, Graham TC, Adamson J, Storb R. Canine cyclic neutropenia. A stem cell defect. J Clin Invest. 1974;53(3):950-953.
40. Horwitz M, Benson KF, Person RE, Aprikyan AG, Dale DC. Mutations in ELA2, encoding neutrophil elastase, define a 21-day biological clock in cyclic haematopoiesis. Nat Genet. 1999; 23(4):433-436.
41. Lei J, Mackey MC. Understanding and treating cytopenia through mathematical modeling. Adv Exp Med Biol. 2014;844:279-302.
42. Dale DC, Person RE, Bolyard AA, et al. Mutations in the gene encoding neutrophil elastase in congenital and cyclic neutropenia. Blood. 2000; 96(7):2317-2322.
43. Grenda DS, Murakami M, Ghatak J, et al. Mutations of the ELA2 gene found in patients with severe congenital neutropenia induce the unfolded protein response and cellular apoptosis. Blood. 2007;110(13):4179-4187.
44. Cortes JE, Talpaz M, Kantarjian H. Chronic myelogenous leukemia: a review. Am J Med. 1996;100(5):555-570.
45. Mackey MC. Periodic auto-immune hemolytic anemia: an induced dynamical disease. Bull Math Biol. 1979;41(6):829-834.
46. Omodeo-Salè F, Motti A, Basilico N, Parapini S, Olliaro P, Taramelli D. Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum. Blood. 2003; 102(2):705-711.