Lupus-Associated Functional Polymorphism in PNP Causes Cell Cycle Abnormalities and Interferon Pathway Activation in Human Immune Cells

Arthritis and Rheumatology

Volumn 69, Issue 12, 2017, Pages 2328-2337

  Ghodke Puranik, Yogita ^a   Dorschner, Jessica M ^a   Vsetecka, Danielle M ^a   Amin, Shreyasee ^b   Makol, Ashima ^b   Ernste, Floranne ^b   Osborn, Thomas ^b   Moder, Kevin ^b   Chowdhary, Vaidehi ^b   Eliopoulos, Elias ^c   Zervou, Maria I ^c   Goulielmos, George N ^c   Jensen, Mark A ^a   Niewold, Timothy B ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAYO CLINIC   (United States)

^c UNIVERSITY OF CRETE   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; ADENOSINE; HYPOXANTHINE; INTERFERON; MESSENGER RNA; PURINE NUCLEOSIDE PHOSPHORYLASE; ALPHA INTERFERON; IFNA1 PROTEIN, HUMAN;

ALLELE; AMINO ACID SUBSTITUTION; ARTICLE; CELL ACTIVATION; CELL CYCLE; CELL CYCLE S PHASE; COLORIMETRY; DNA POLYMORPHISM; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FOLLOW UP; GENE EXPRESSION; GENETIC ASSOCIATION; GENOTYPE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOPHENOTYPING; LYMPHOBLASTOID CELL LINE; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN STRUCTURE; PURINE NUCLEOSIDE PHOSPHORYLASE DEFICIENCY; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTEMIC LUPUS ERYTHEMATOSUS; BLOOD; GENETICS; IMMUNOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ALLELES; CELL CYCLE; GENE EXPRESSION; GENOTYPE; HUMANS; INTERFERON-ALPHA; LUPUS ERYTHEMATOSUS, SYSTEMIC; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; PURINE-NUCLEOSIDE PHOSPHORYLASE; SIGNAL TRANSDUCTION;

EID: 85033442355     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.40304     Document Type: Article

References (41)

1. Harley JB, Kelly JA, Kaufman KM. Unraveling the genetics of systemic lupus erythematosus. Springer Semin Immunopathol 2006;28:119–30.
2. Hooks JJ, Moutsopoulos HM, Geis SA, Stahl NI, Decker JL, Notkins AL. Immune interferon in the circulation of patients with autoimmune disease. N Engl J Med 1979;301:5–8.
3. Niewold TB, Hua J, Lehman TJ, Harley JB, Crow MK. High serum IFN-α activity is a heritable risk factor for systemic lupus erythematosus. Genes Immun 2007;8:492–502.
4. Ghodke-Puranik Y, Niewold TB. Genetics of the type I interferon pathway in systemic lupus erythematosus. Int J Clin Rheumatol 2013;8:657–69.
5. Kariuki SN, Kirou KA, MacDermott EJ, Barillas-Arias L, Crow MK, Niewold TB. Cutting edge: autoimmune disease risk variant of STAT4 confers increased sensitivity to IFN-α in lupus patients in vivo. J Immunol 2009;182:34–8.
6. Niewold TB, Kelly JA, Flesch MH, Espinoza LR, Harley JB, Crow MK. Association of the IRF5 risk haplotype with high serum interferon-α activity in systemic lupus erythematosus patients. Arthritis Rheum 2008;58:2481–7.
7. Niewold TB, Kelly JA, Kariuki SN, Franek BS, Kumar AA, Kaufman KM, et al. IRF5 haplotypes demonstrate diverse serological associations which predict serum interferon α activity and explain the majority of the genetic association with systemic lupus erythematosus. Ann Rheum Dis 2012;71:463–8.
8. Kariuki SN, Ghodke-Puranik Y, Dorschner JM, Chrabot BS, Kelly JA, Tsao BP, et al. Genetic analysis of the pathogenic molecular sub-phenotype interferon-α identifies multiple novel loci involved in systemic lupus erythematosus. Genes Immun 2015;16:15–23.
9. Markert ML. Purine nucleoside phosphorylase deficiency. Immunodefic Rev 1991;3:45–81.
10. Hershfield MS, Mitchell BS. Immunodeficiency diseases caused by adenosine deaminase deficiency and purine nucleoside phosphorylase deficiency. In: Scriver CR, Beaudet AL, Sly WS, Valle D, editors. The metabolic and molecular bases of inherited disease. New York: McGraw-Hill; 1995. p. 1725–68.
11. Lipsky PE. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol 2001;2:764–6.
12. Sasaki Y, Iseki M, Yamaguchi S, Kurosawa Y, Yamamoto T, Moriwaki Y, et al. Direct evidence of autosomal recessive inheritance of Arg24 to termination codon in purine nucleoside phosphorylase gene in a family with a severe combined immunodeficiency patient. Hum Genet 1998;103:81–5.
13. Rijkers GT, Zegers BJ, Spaapen LJ, Rutgers DH, Kuis W, Roord JJ, et al. Mononuclear cells in S-phase in a patient with purine nucleoside phosphorylase deficiency. Adv Exp Med Biol 1984;165:171–4.
14. Al-Saud B, Alsmadi O, Al-Muhsen S, Al-Ghonaium A, Al-Dhekri H, Arnaout R, et al. A novel mutation in purine nucleoside phosphorylase in a child with normal uric acid levels. Clin Biochem 2009;42:1725–7.
15. Bzowska A, Kulikowska E, Shugar D. Purine nucleoside phosphorylases: properties, functions, and clinical aspects. Pharmacol Ther 2000;88:349–425.
16. Grunebaum E, Zhang J, Roifman CM. Novel mutations and hot-spots in patients with purine nucleoside phosphorylase deficiency. Nucleosides Nucleotides Nucleic Acids 2004;23:1411–5.
17. Osborne WR, Scott CR. Purine nucleoside phosphorylase deficiency: measurement of variant protein in four families with enzyme-deficient members by an enzyme-linked immunosorbent assay. Am J Hum Genet 1980;32:927–33.
18. Aust MR, Andrews LG, Barrett MJ, Norby-Slycord CJ, Markert ML. Molecular analysis of mutations in a patient with purine nucleoside phosphorylase deficiency. Am J Hum Genet 1992;51:763–72.
19. Kim BK, Cha S, Parks RE Jr. Purine nucleoside phosphorylase from human erythrocytes. Part I. Purification and properties. J Biol Chem 1968;243:1763–70.
20. Kalckar HM. Differential spectrophotometry of purine compounds by means of specific enzymes; determination of hydroxypurine compounds. J Biol Chem 1947;167:429–43.
21. Chu SY, Cashion P, Jiang M. A new colorimetric assay for purine nucleoside phosphorylase. Clin Biochem 1989;22:357–62.
22. Halfpenny AP, Brown PR. Optimized assay for purine nucleoside phosphorylase by reversed-phase high-performance liquid chromatography. J Chromatogr 1980;199:275–82.
23. Uitendaal MP, de Bruyn CH, Oei TL, Hosli P, Griscelli C. A new ultramicrochemical assay for purine nucleoside phosphorylase. Anal Biochem 1978;84:147–53.
24. Hua J, Kirou K, Lee C, Crow MK. Functional assay of type I interferon in systemic lupus erythematosus plasma and association with anti–RNA binding protein autoantibodies. Arthritis Rheum 2006;54:1906–16.
25. Niewold TB, Adler JE, Glenn SB, Lehman TJ, Harley JB, Crow MK. Age- and sex-related patterns of serum interferon-α activity in lupus families. Arthritis Rheum 2008;58:2113–9.
26. Niewold TB, Rivera TL, Buyon JP, Crow MK. Serum type I interferon activity is dependent on maternal diagnosis in anti-SSA/Ro–positive mothers of children with neonatal lupus. Arthritis Rheum 2008;58:541–6.
27. Frederiks WM, Bosch KS, van Gulik T. A quantitative histochemical procedure for the demonstration of purine nucleoside phosphorylase activity in rat and human liver using Tetranitro BT and xanthine oxidase as auxiliary enzyme. Histochem J 1993;25:86–91.
28. Erion MD, Takabayashi K, Smith HB, Kessi J, Wagner S, Honger S, et al. Purine nucleoside phosphorylase. Part 1. Structure-function studies. Biochemistry 1997;36:11725–34.
29. Sidi Y, Mitchell BS. 2′-deoxyguanosine toxicity for B and mature T lymphoid cell lines is mediated by guanine ribonucleotide accumulation. J Clin Invest 1984;74:1640–8.
30. Gough DJ, Messina NL, Clarke CJ, Johnstone RW, Levy DE. Constitutive type I interferon modulates homeostatic balance through tonic signaling. Immunity 2012;36:166–74.
31. Yamada H, Ochi K, Nakada S, Nemoto T, Horiguchi-Yamada J. Changes of cell cycle-regulating genes in interferon-treated Daudi cells. Mol Cell Biochem 1994;136:117–23.
32. Kumar R, Korutla L, Zhang K. Cell cycle-dependent modulation of α-interferon-inducible gene expression and activation of signaling components in Daudi cells. J Biol Chem 1994;269:25437–41.
33. Creasey AA, Eppstein DA, Marsh YV, Khan Z, Merigan TC. Growth regulation of melanoma cells by interferon and (2′-5′)oligoadenylate synthetase. Mol Cell Biol 1983;3:780–6.
34. Wells V, Mallucci L. Expression of the 2-5A system during the cell cycle. Exp Cell Res 1985;159:27–36.
35. Wells V, Mallucci L. Cell cycle regulation (G1) by autocrine interferon and dissociation between autocrine interferon and 2′,5′-oligoadenylate synthetase expression. J Interferon Res 1988;8:793–802.
36. Lee SH, Rozee KR. Variation of interferon production during the cell cycle. Appl Microbiol 1970;20:11–5.
37. Fitzgerald-Bocarsly P, Dai J, Singh S. Plasmacytoid dendritic cells and type I IFN: 50 years of convergent history. Cytokine Growth Factor Rev 2008;19:3–19.
38. Amit I, Garber M, Chevrier N, Leite AP, Donner Y, Eisenhaure T, et al. Unbiased reconstruction of a mammalian transcriptional network mediating pathogen responses. Science 2009;326:257–63.
39. Archambault V, Glover DM. Polo-like kinases: conservation and divergence in their functions and regulation. Nat Rev Mol Cell Biol 2009;10:265–75.
40. Seeburg DP, Pak D, Sheng M. Polo-like kinases in the nervous system. Oncogene 2005;24:292–8.
41. Chevrier N, Mertins P, Artyomov MN, Shalek AK, Iannacone M, Ciaccio MF, et al. Systematic discovery of TLR signaling components delineates viral-sensing circuits. Cell 2011;147:853–67.