Negative feedback-defective PRPS1 mutants drive thiopurine resistance in relapsed childhood ALL

Nature Medicine

Volumn 21, Issue 6, 2015, Pages 563-571

  Li, Benshang ^a,b,c   Li, Hui ^a,b,c   Bai, Yun ^b   Kirschner Schwabe, Renate ^d,e   Yang, Jun J ^f   Chen, Yao ^a,c   Lu, Gang ^b   Tzoneva, Gannie ^g   Ma, Xiaotu ^f   Wu, Tongmin ^a,c   Li, Wenjing ^h   Lu, Haisong ⁱ   Ding, Lixia ^a,c   Liang, Huanhuan ^a   Huang, Xiaohang ^a   Yang, Minjun ^b   Jin, Lei ^b   Kang, Hui ^b   Chen, Shuting ^b   Du, Alicia ⁱ   Shen, Shuhong ^a,c   Ding, Jianping ^h   Chen, Hongzhuan ^c,j   Chen, Jing ^a   Von Stackelberg, Arend ^d   Gu, Longjun ^a   Zhang, Jinghui ^f   Ferrando, Adolfo ^g   Tang, Jingyan ^a   Wang, Shengyue ^b,j   Zhou, Bin Bing S ^a,c,j   more..

^a BEIJING HOSPITAL   (China)

^b CHINESE NATIONAL HUMAN GENOME CENTER AT SHANGHAI   (China)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^f ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^g Columbia University ^*  (United States)

^h INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

ⁱ Shanghai Chem Partner Co Ltd   (China)

^j National Center for Fetal Medicine   (China)

more..

Author keywords

[No Author keywords available]

Indexed keywords

LOMETREXOL; MERCAPTOPURINE; PHOSPHORIBOSYL PYROPHOSPHATE SYNTHETASE 1; PURINE; RIBOSEPHOSPHATE PYROPHOSPHOKINASE; UNCLASSIFIED DRUG; PRPS1 PROTEIN, HUMAN; PURINE DERIVATIVE; TETRAHYDROFOLIC ACID DERIVATIVE;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; CANCER GENETICS; CANCER RESISTANCE; CHILD; CHILDHOOD LEUKEMIA; COMPETITIVE INHIBITION; CONTROLLED STUDY; DRUG ACTIVATION; EXOME; FEMALE; GENE MUTATION; GENE SEQUENCE; HUMAN; INFANT; LEUKEMIA RELAPSE; MAJOR CLINICAL STUDY; MALE; NEGATIVE FEEDBACK; PRIORITY JOURNAL; PURINE SYNTHESIS; RECURRENT DISEASE; ADOLESCENT; BIOSYNTHESIS; CHEMISTRY; DRUG EFFECTS; FEEDBACK SYSTEM; GENETICS; HIGH THROUGHPUT SEQUENCING; LEUKEMIA, B-CELL; MUTATION; PATHOLOGY; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PRESCHOOL CHILD;

6-MERCAPTOPURINE; ADOLESCENT; CHILD; CHILD, PRESCHOOL; EXOME; FEEDBACK, PHYSIOLOGICAL; FEMALE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INFANT; LEUKEMIA, B-CELL; MALE; MUTATION; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PURINES; RECURRENCE; RIBOSE-PHOSPHATE PYROPHOSPHOKINASE; TETRAHYDROFOLATES;

EID: 84930752349     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3840     Document Type: Article

References (41)

1. Pui, C.H., Carroll, W.L., Meshinchi, S. & Arceci, R.J. Biology, risk stratification, and therapy of pediatric acute leukemias: an update. J. Clin. Oncol. 29, 551-565 (2011).
2. Pui, C.H. Recent advances in the biology and treatment of childhood acute lymphoblastic leukemia. Curr. Opin. Hematol. 5, 292-301 (1998).
3. Aarbakke, J., Janka-Schaub, G. & Elion, G.B. Thiopurine biology and pharmacology. Trends Pharmacol. Sci. 18, 3-7 (1997).
4. Wyngaarden, J.B. Regulation of purine biosynthesis and turnover. Adv. Enzyme Regul. 14, 25-42 (1976).
5. Becker, M.A. & Kim, M. Regulation of purine synthesis de novo in human fibroblasts by purine nucleotides and phosphoribosylpyrophosphate. J. Biol. Chem. 262, 14531-14537 (1987).
6. Nosal, J.M., Switzer, R.L. & Becker, M.A. Overexpression, purification, and characterization of recombinant human 5-phosphoribosyl-1-pyrophosphate synthetase isozymes I and II. J. Biol. Chem. 268, 10168-10175 (1993).
7. Meyer, J.A. et al. Relapse-specific mutations in NT5C2 in childhood acute lymphoblastic leukemia. Nat. Genet. 45, 290-294 (2013).
8. Tzoneva, G. et al. Activating mutations in the NT5C2 nucleotidase gene drive chemotherapy resistance in relapsed ALL. Nat. Med. 19, 368-371 (2013).
9. Mullighan, C.G. et al. Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science 322, 1377-1380 (2008).
10. Gu, L.J. et al. Clinical outcome of children with newly diagnosed acute lymphoblastic leukemia treated in a single center in Shanghai, China. Leuk. Lymphoma 49, 488-494 (2008).
11. Tang, J.Y. et al. [Evaluation on protocol SCMS-ALL-2005 for childhood B lineage acute lymphoblastic leukemia]. J. Chin. Med. Assoc. 92, 546-550 (2012).
12. Conter, V. et al. Molecular response to treatment redefines all prognostic factors in children and adolescents with B-cell precursor acute lymphoblastic leukemia: results in 3184 patients of the AIEOP-BFM ALL 2000 study. Blood 115, 3206-3214 (2010).
13. Escherich, G., Zimmermann, M. & Janka-Schaub, G. Doxorubicin or daunorubicin given upfront in a therapeutic window are equally effective in children with newly diagnosed acute lymphoblastic leukemia. A randomized comparison in trial CoALL 07-03. Pediatr. Blood Cancer 60, 254-257 (2013).
14. Henze, G., v Stackelberg, A. & Eckert, C. ALL-REZ BFM-the consecutive trials for children with relapsed acute lymphoblastic leukemia. Klin. Padiatr. 225(Suppl. 1), S73-S78 (2013).
15. Becker, M.A., Smith, P.R., Taylor, W., Mustafi, R. & Switzer, R.L. The genetic and functional basis of purine nucleotide feedback-resistant phosphoribosylpyrophosphate synthetase superactivity. J. Clin. Invest. 96, 2133-2141 (1995).
16. Hof, J., Szymansky, A., Stackelberg, A., Eckert, C. & Kirschner-Schwabe, R. Clinical significance of NT5C2 mutations in children with first relapse of B-cell precursor acute lymphoblastic leukemia. Abstract 3789. In 56th American Society of Hematology Annual Meeting and Exposition (San Francisco, California, USA, December 6-9, 2014) (American Society of Hematology, 2014).
17. Tang, W. et al. Expression, purification, crystallization and preliminary X-ray diffraction analysis of human phosphoribosyl pyrophosphate synthetase 1 (PRS1). Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 62, 432-434 (2006).
18. Li, S., Lu, Y., Peng, B. & Ding, J. Crystal structure of human phosphoribosylpyrophosphate synthetase 1 reveals a novel allosteric site. Biochem. J. 401, 39-47 (2007).
19. Fox, I.H. & Kelley, W.N. Human phosphoribosylpyrophosphate synthetase. Distribution, purification, and properties. J. Biol. Chem. 246, 5739-5748 (1971).
20. de Brouwer, A.P. et al. PRPS1 mutations: four distinct syndromes and potential treatment. Am. J. Hum. Genet. 86, 506-518 (2010).
21. Moran, R. et al. Phosphoribosylpyrophosphate synthetase superactivity and recurrent infections is caused by a p.Val142Leu mutation in PRS-I. Am. J. Med. Genet. A. 158A, 455-460 (2012).
22. Karran, P. & Attard, N. Thiopurines in current medical practice: molecular mechanisms and contributions to therapy-related cancer. Nat. Rev. Cancer 8, 24-36 (2008).
23. Zoref, E., De Vries, A. & Sperling, O. Mutant feedback-resistant phosphoribosylpyrophosphate synthetase associated with purine overproduction and gout. Phosphoribosylpyrophosphate and purine metabolism in cultured fibroblasts. J. Clin. Invest. 56, 1093-1099 (1975).
24. Gerhart, J. From feedback inhibition to allostery: the enduring example of aspartate transcarbamoylase. FEBS J. 281, 612-620 (2014).
25. Breton, A. et al. Lethal accumulation of guanylic nucleotides in Saccharomyces cerevisiae HPT1-deregulated mutants. Genetics 178, 815-824 (2008).
26. Christopherson, R.I., Lyons, S.D. & Wilson, P.K. Inhibitors of de novo nucleotide biosynthesis as drugs. Acc. Chem. Res. 35, 961-971 (2002).
27. Adams, J. & Elliott, P.J. New agents in cancer clinical trials. Oncogene 19, 6687-6692 (2000).
28. Tallen, G. et al. Long-term outcome in children with relapsed acute lymphoblastic leukemia after time-point and site-of-relapse stratification and intensified short-course multidrug chemotherapy: results of trial ALL-REZ BFM 90. J. Clin. Oncol. 28, 2339-2347 (2010).
29. Tong, X., Zhao, F. & Thompson, C.B. The molecular determinants of de novo nucleotide biosynthesis in cancer cells. Curr. Opin. Genet. Dev. 19, 32-37 (2009).
30. Bester, A.C. et al. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 145, 435-446 (2011).
31. Aird, K.M. et al. Suppression of nucleotide metabolism underlies the establishment and maintenance of oncogene-induced senescence. Cell Reports 3, 1252-1265 (2013).
32. Zhou, B.B. & Elledge, S.J. The DNA damage response: putting checkpoints in perspective. Nature 408, 433-439 (2000).
33. Kozhevnikova, E.N. et al. Metabolic enzyme IMPDH is also a transcription factor regulated by cellular state. Mol. Cell 47, 133-139 (2012).
34. Reddy, B.A. et al. Nucleotide biosynthetic enzyme GMP synthase is a TRIM21-controlled relay of p53 stabilization. Mol. Cell 53, 458-470 (2014).
35. Wintzerith, M., Ciesielski-Treska, J., Dierich, A. & Mandel, P. Comparative investigation of free nucleotides in two neuroblastoma clonal cell lines. J. Neurochem. 26, 205-207 (1976).
36. Cunningham, J.T., Moreno, M.V., Lodi, A., Ronen, S.M. & Ruggero, D. Protein and nucleotide biosynthesis are coupled by a single rate-limiting enzyme, PRPS2, to drive cancer. Cell 157, 1088-1103 (2014).
37. Zhang, J. et al. A novel retinoblastoma therapy from genomic and epigenetic analyses. Nature 481, 329-334 (2012).
38. Zhang, J. et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481, 157-163 (2012).
39. Alderwick, L.J. et al. Biochemical characterization of the Mycobacterium tuberculosis phosphoribosyl-1-pyrophosphate synthetase. Glycobiology 21, 410-425 (2011).
40. Eriksen, T.A., Kadziola, A., Bentsen, A.K., Harlow, K.W. & Larsen, S. Structural basis for the function of Bacillus subtilis phosphoribosyl-pyrophosphate synthetase. Nat. Struct. Biol. 7, 303-308 (2000).
41. Dervieux, T. et al. HPLC determination of thiopurine nucleosides and nucleotides in vivo in lymphoblasts following mercaptopurine therapy. Clin. Chem. 48, 61-68 (2002).