Genomic variants in the ASS1 gene, involved in the nitric oxide biosynthesis and signaling pathway, predict hydroxyurea treatment efficacy in compound sickle cell disease/β-thalassemia patients

Pharmacogenomics

Volumn 17, Issue 4, 2016, Pages 393-403

  Chalikiopoulou, Constantina ^a   Tavianatou, Anastasia Gerasimoula ^a   Sgourou, Argyro ^b   Kourakli, Alexandra ^c   Kelepouri, Dimitra ^a   Chrysanthakopoulou, Maria ^a   Kanelaki, Vasiliki Kaliopi ^a   Mourdoukoutas, Evangelos ^a   Siamoglou, Stavroula ^a   John, Anne ^d   Symeonidis, Argyris ^c   Ali, Bassam R ^d   Katsila, Theodora ^a   Papachatzopoulou, Adamantia ^c   Patrinos, George P ^a,d  

^a UNIVERSITY OF PATRAS   (Greece)

^b HELLENIC OPEN UNIVERSITY   (Greece)

^c UNIVERSITY OF PATRAS   (Greece)

^d UNITED ARAB EMIRATES UNIVERSITY   (United Arab Emirates)

Author keywords

ASS1; cGMP signaling; haplotype; hydroxyurea; nitric oxide; NOS1; NOS2A; pharmacogenomics; thalassemia

Indexed keywords

GUANYLATE CYCLASE; HEMOGLOBIN F; HEMOGLOBIN GAMMA CHAIN; HYDROXYUREA; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; ANTISICKLING AGENT; ARGININOSUCCINATE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NOS1 PROTEIN, HUMAN; NOS2 PROTEIN, HUMAN;

ARTICLE; ASS1 GENE; BETA THALASSEMIA; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFICACY; DRUG RESPONSE; GENE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; MAJOR CLINICAL STUDY; NOS1 GENE; NOS2A GENE; PHARMACOGENOMICS; PREDICTION; SICKLE CELL ANEMIA; SIGNAL TRANSDUCTION; ANEMIA, SICKLE CELL; BETA-THALASSEMIA; BIOSYNTHESIS; CASE CONTROL STUDY; COMPLICATION; GENETIC VARIATION; GENETICS;

ANEMIA, SICKLE CELL; ANTISICKLING AGENTS; ARGININOSUCCINATE SYNTHASE; BETA-THALASSEMIA; CASE-CONTROL STUDIES; GENETIC VARIATION; HUMANS; HYDROXYUREA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II;

EID: 84960845917     PISSN: 14622416     EISSN: 17448042     Source Type: Journal    
DOI: 10.2217/pgs.16.1     Document Type: Article

References (51)

1. Weatherall DJ. Phenotype-genotype relationships in monogenic disease: lessons from the thalassaemias. Nat. Rev. Genet. 2(4), 245-255 (2001).
2. Akinsheye I, Alsultan A, Solovieff N et al. Fetal hemoglobin in sickle cell anemia. Blood 118(1), 19-27 (2011).
3. Perrine SP, Miller BA, Greene MF et al. Butryic acid analogues augment globin gene expression in neonatal erythroid progenitors. Biochem. Biophys. Res. Commun. 148(2), 694-700 (1987).
4. Ley TJ, Desimone J, Anagnou NP et al. 5-Azacytidine selectively increases globin synthesis in a patient with thalassemia. N. Engl. J. Med. 307(24), 1469-1475 (1982).
5. Veith R, Galanello R, Papayannopoulou T, Stamatoyannopoulos G. Stimulation of F-cell production in patients with sickle-cell anemia treated with cytarabine or hydroxyurea. N. Engl. J. Med. 313(25), 1571-1575 (1985).
6. Cao A, Galanello R. Beta-thalassemia. Genet. Med. 12(2), 61-76 (2010).
7. Koren A, Levin C, Dgany O et al. Response to hydroxyurea therapy in thalassemia. Am. J. Hematol. 83(5), 366-370 (2008).
8. Cokic VP, Andric SA, Stojilkovic SS, Noguchi CT, Schechter AN. Hydroxyurea nitrosylates and activates soluble guanylyl cyclase in human erythroid cells. Blood 111(3), 1117-1123 (2008).
9. Park J-I, Choi H-S, Jeong J-S, Han J-Y, Kim I-H. Involvement of p38 kinase in hydroxyurea-induced differentiation of K562 Cells. Cell Growth Differ. 12(9), 481-486 (2001).
10. Pourfarzad F, Von Lindern M, Azarkeivan A et al. Hydroxyurea responsiveness in thalassemic patients is determined by the stress response adaptation of erythroid progenitors and their differentiation propensity. Haematologica 98(5), 696-704 (2013).
11. Gravia A, Chondrou V, Sgourou A et al. Individualizing fetal hemoglobin augmenting therapy for type hemoglobinopathies patients. Pharmacogenomics 15(10), 1355-1364 (2014).
12. Ma Q, Wyszynski DF, Farrell JJ et al. Fetal hemoglobin in sickle cell anemia: genetic determinants of response to hydroxyurea. Pharmacogenomics J. 7(6), 386-394 (2007).
13. Ware RE, Despotovic JM, Mortier NA et al. Pharmacokinetics, pharmacodynamics, and pharmacogenetics of hydroxyurea treatment for children with sickle cell anemia. Blood 118(18), 4985-4991 (2011).
14. Borg J, Phylactides M, Bartsakoulia M et al. KLF10 gene expression is associated with high fetal hemoglobin levels and with response to hydroxyurea treatment in hemoglobinopathy patients. Pharmacogenomics 13(13), 1487-1500 (2012).
15. Tafrali C, Paizi A, Borg J et al. Genomic variation in the MAP3K5 gene is associated with thalassemia disease severity and hydroxyurea treatment efficacy. Pharmacogenomics 14(5), 469-483 (2013).
16. Dupont LL, Glynos C, Bracke KR, Brouckaert P, Brusselle GG. Role of the nitric oxide-soluble guanylyl cyclase pathway in obstructive airway diseases. Pulm. Pharmacol. Ther. 29(1), 1-6 (2014).
17. Ikuta T, Ausenda S, Cappellini MD. Mechanism for fetal globin gene expression: role of the soluble guanylate cyclase-cGMP-dependent protein kinase pathway. Proc. Natl Acad. Sci. USA 98(4), 1847-1852 (2001).
18. Giannopoulou E, Bartsakoulia M, Tafrali C et al. A single nucleotide polymorphism in the HBBP1 gene in the human globin locus is associated with a mild thalassemia disease phenotype. Hemoglobin 36(5), 433-445 (2012).
19. Papachatzopoulou A, Kaimakis P, Pourfarzad F et al. Increased-globin gene expression in-thalassemia intermedia patients correlates with a mutation in 3HS1. Am. J. Hematol. 82(11), 1005-1009 (2007).
20. Papachatzopoulou A, Kourakli A, Makropoulou P et al. Genotypic heterogeneity and correlation to intergenic haplotype within high HbF-thalassemia intermedia. Eur. J. Haematol. 76(4), 322-330 (2006).
21. Patrinos GP, Grosveld FG. Pharmacogenomics and therapeutics of hemoglobinopathies. Hemoglobin 32(1-2), 229-236 (2008).
22. Broad Institute. www. broadinstitute. org
23. Johnson AD, Handsaker RE, Pulit SL, Nizzari MM, O'donnell CJ, De Bakker PIW. SNAP: A web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics 24(24), 2938-2939 (2008).
24. National Center for Biotechnology Information. http://hapmap. ncbi. nlm. nih. gov
25. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics 21(2), 263-265 (2005).
26. 1000 Genomes. www. 1000genomes. org
27. Desmet F-O, Hamroun D, Lalande M, Collod-Béroud G, Claustres M, Béroud C. Human splicing finder: An online bioinformatics tool to predict splicing signals. Nucleic Acids Res. 37(9), e67-e67 (2009).
28. RD Connect. http://rd-connect. eu
29. MicroSNiPer. http://epicenter. ie-freiburg. mpg. de
30. Barenboim M, Zoltick BJ, Guo Y, Weinberger DR. MicroSNiPer: A web tool for prediction of SNP effects on putative microRNA targets. Hum. Mutat. 31(11), 1223-1232 (2010).
31. RNAcofold. http://rna. tbi. univie. ac. at
32. Mathews DH, Disney MD, Childs JL, Schroeder SJ, Zuker M, Turner DH. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc. Natl Acad. Sci. USA 101(19), 7287-7292 (2004).
33. Weatherall DJ. Towards molecular medicine: reminiscences of the haemoglobin field, 1960-2000. Br. J. Haematol. 115(4), 729-738 (2001).
34. Cokic VP, Smith RD, Beleslin-Cokic BB et al. Hydroxyurea induces fetal hemoglobin by the nitric oxide-dependent activation of soluble guanylyl cyclase. J. Clin. Invest. 111(2), 231-239 (2003).
35. Creary LE, Ulug P, Menzel S et al. Genetic variation on Chromosome 6 influences F cell levels in healthy individuals of African Descent and HbF levels in sickle cell patients. PLoS ONE 4(1), e4218 (2009).
36. Salvemini D, Misko TP, Masferrer JL, Seibert K, Currie MG, Needleman P. Nitric oxide activates cyclooxygenase enzymes. Proc. Natl Acad. Sci. USA 90(15), 7240-7244 (1993).
37. Tetsuka T, Daphna-Iken D, Srivastava SK, Baier LD, Dumaine J, Morrison AR. Cross-talk between cyclooxygenase and nitric oxide pathways: prostaglandin E2 negatively modulates induction of nitric oxide synthase by interleukin 1. Proc. Natl Acad. Sci. USA 91(25), 12168-12172 (1994).
38. Ikuta T, Kuroyanagi Y, Odo N, Liu S. A common signaling pathway is activated in erythroid cells expressing high levels of fetal hemoglobin: A potential role for cAMP-elevating agents in-globin disorders. J. Blood Med. 4, 149-159 (2013).
39. Bailey L, Kuroyanagi Y, Franco-Penteado CF et al. Expression of the-globin gene is sustained by the cAMP-dependent pathway in-thalassaemia. Br. J. Haematol. 138(3), 382-395 (2007).
40. Kuroyanagi Y, Kaneko Y, Muta K et al. cAMP differentially regulates-globin gene expression in erythroleukemic cells and primary erythroblasts through c-Myb expression. Biochem. Biophys. Res. Commun. 344(3), 1038-1047 (2006).
41. Engel K, Höhne W, Häberle J. Mutations and polymorphisms in the human argininosuccinate synthetase (ASS1) gene. Hum. Mutat. 30(3), 300-307 (2009).
42. PharmGKB. www. pharmgkb. org/label/PA166114317
43. PharmGKB. www. pharmgkb. org/label/PA166114381
44. Roberts TC. The microRNA biology of the mammalian nucleus. Mol. Ther. Nucleic Acids 3, e188 (2014).
45. Millar DS, Horan M, Chuzhanova NA, Cooper DN. Characterisation of a functional intronic polymorphism in the human growth hormone (GHI) gene. Hum. Genomics 4(5), 289-301 (2010).
46. Cooper DN. Functional intronic polymorphisms: buried treasure awaiting discovery within our genes. Hum. Genomics 4(5), 284-288 (2010).
47. Seo S, Takayama K, Uno K et al. Functional analysis of deep intronic SNP rs13438494 in Intron 24 of PCLO gene. PLoS ONE 8(10), e76960 (2013).
48. Moyer RA, Wang D, Papp AC et al. Intronic polymorphisms affecting alternative splicing of human dopamine D2 receptor are associated with cocaine abuse. Neuropsychopharmacology 36(4), 753-762 (2011).
49. Meiler SE, Wade M, Kutlar F et al. Pomalidomide augments fetal hemoglobin production without the myelosuppressive effects of hydroxyurea in transgenic sickle cell mice. Blood 118(4), 1109-1112 (2011).
50. Deng W, Rupon JW, Krivega I et al. Reactivation of developmentally silenced globin genes by forced chromatin looping. Cell 158(4), 849-860 (2014).
51. Flanagan JM, Steward S, Howard TA et al. Hydroxycarbamide alters erythroid gene expression in children with sickle cell anaemia. Br. J. Haematol. 157(2), 240-248 (2012).