Adenosine deaminase deficiency - more than just an immunodeficiency

Frontiers in Immunology

Volumn 7, Issue AUG, 2016, Pages

  Whitmore, Kathryn V ^a   Gaspar, Hubert B ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Adenosine deaminase; Enzyme replacement therapy; Gene therapy; Hematopoietic stem cell transplantation; Immunodeficiency; Neurological abnormalities; SCID

Indexed keywords

ADENOSINE; DEOXYADENOSINE; PURINE;

ADENOSINE DEAMINASE DEFICIENCY; AUDITORY PROCESSING DISORDER; AUTOIMMUNITY; B LYMPHOCYTE; BEHAVIOR DISORDER; CELL FUNCTION; CELL MATURATION; COGNITIVE DEFECT; ENZYME REPLACEMENT; GENE THERAPY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOPATHOLOGY; KIDNEY DYSFUNCTION; LUNG INSUFFICIENCY; MULTIPLE ORGAN FAILURE; NEUROLOGIC DISEASE; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; SKIN TUMOR; T LYMPHOCYTE; THYMOCYTE;

EID: 84989306598     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00314     Document Type: Review

References (66)

1. Sauer AV, Brigida I, Carriglio N, Aiuti A. Autoimmune dysregulation and purine metabolism in adenosine deaminase deficiency. Front Immunol (2012) 3:265. doi: 10.3389/fimmu.2012.00265
2. Hönig M, Albert MH, Schulz A, Sparber-Sauer M, Schütz C, Belohradsky B, et al. Patients with adenosine deaminase deficiency surviving after hematopoietic stem cell transplantation are at high risk of CNS complications. Blood (2007) 109:3595-602. doi:10.1182/blood-2006-07-034678
3. Gakis C. Adenosine deaminase (ADA) isoenzymes ADA1 and ADA2: diagnostic and biological role. Eur Respir J (1996) 9:632-3. doi:10.1183/09031936.96.09040632
4. Navon Elkan P, Pierce SB, Segel R, Walsh T, Barash J, Padeh S, et al. Mutant adenosine deaminase 2 in a polyarteritis nodosa vasculopathy. N Engl J Med (2014) 370:921-31. doi:10.1056/NEJMoa1307362
5. Schepp J, Bulashevska A, Mannhardt-Laakmann W, Cao H, Yang F, Seidl M, et al. Deficiency of adenosine deaminase 2 causes antibody deficiency. J Clin Immunol (2016) 36:179-86. doi:10.1007/s10875-016-0245-x
6. Zhou Q, Yang D, Ombrello AK, Zavialov AV, Toro C, Stone DL, et al. Early-onset stroke and vasculopathy associated with mutations in ADA2. N Engl J Med (2014) 370:911-20. doi:10.1056/NEJMoa1307361
7. Blackburn MR, Kellems RE. Adenosine deaminase deficiency: metabolic basis of immune deficiency and pulmonary inflammation. Adv Immunol (2005) 86:1-41. doi:10.1016/S0065-2776(04)86001-2
8. Kwan A, Abraham RS, Currier R, Brower A, Andruszewski K, Abbott JK, et al. Newborn screening for severe combined immunodeficiency in 11 screening programs in the United States. JAMA (2014) 312:729-38. doi:10.1001/jama.2014.9132
9. Nikolajeva O, Worth A, Hague R, Martinez-Alier N, Smart J, Adams S, et al. Adenosine deaminase deficient severe combined immunodeficiency presenting as atypical haemolytic uraemic syndrome. J Clin Immunol (2015) 35:366-72. doi:10.1007/s10875-015-0158-0
10. Gaspar HB, Aiuti A, Porta F, Candotti F, Hershfield MS, Notarangelo LD. How I treat ADA deficiency. Blood (2009) 114:3524-32. doi:10.1182/blood-2009-06-189209
11. Baffelli R, Notarangelo LD, Imberti L, Hershfield MS, Serana F, Santisteban I, et al. Diagnosis, treatment and long-term follow up of patients with ADA deficiency: a single-center experience. J Clin Immunol (2015) 35:624-37. doi:10.1007/s10875-015-0191-z
12. Serana F, Sottini A, Chiarini M, Zanotti C, Ghidini C, Lanfranchi A, et al. The different extent of B and T cell immune reconstitution after hematopoietic stem cell transplantation and enzyme replacement therapies in SCID patients with adenosine deaminase deficiency. J Immunol (2010) 185:7713-22. doi:10.4049/jimmunol.1001770
13. Tartibi HM, Hershfield MS, Bahna SL. A 24-year enzyme replacement therapy in an adenosine-deaminase-deficient patient. Pediatrics (2016) 137:1-5. doi:10.1542/peds.2015-2169
14. Fischer A, Notarangelo LD, Neven B, Cavazzana M, Puck JM. Severe combined immunodeficiencies and related disorders. Nat Rev Dis Primers (2015) 1:15061. doi:10.1038/nrdp.2015.61
15. Ferrua F, Brigida I, Aiuti A. Update on gene therapy for adenosine deaminase-deficient severe combined immunodeficiency. Curr Opin Allergy Clin Immunol (2010) 10:551-6. doi:10.1097/ACI.0b013e32833fea85
16. Benveniste P, Zhu W, Cohen A. Interference with thymocyte differentiation by an inhibitor of S-adenosylhomocysteine hydrolase. J Immunol (1995) 155:536-44
17. Apasov SG, Blackburn MR, Kellems RE, Smith PT, Sitkovsky MV. Adenosine deaminase deficiency increases thymic apoptosis and causes defective T cell receptor signaling. J Clin Invest (2001) 108:131-41. doi:10.1172/JCI200110360
18. Poliani PL, Facchetti F, Ravanini M, Gennery AR, Villa A, Roifman CM, et al. Early defects in human T-cell development severely affect distribution and maturation of thymic stromal cells: possible implications for the pathophysiology of Omenn syndrome. Blood (2009) 114:105-8. doi:10.1182/blood-2009-03-211029
19. Joachims ML, Marble PA, Laurent AB, Pastuszko P, Paliotta M, Blackburn MR, et al. Restoration of adenosine deaminase-deficient human thymocyte development in vitro by inhibition of deoxynucleoside kinases. J Immunol (2008) 181:8153-61. doi:10.4049/jimmunol.181.11.8153
20. Thompson LF, Van de Wiele CJ, Laurent AB, Hooker SW, Vaughn JG, Jiang H, et al. Metabolites from apoptotic thymocytes inhibit thymopoiesis in adenosine deaminase-deficient fetal thymic organ cultures. J Clin Invest (2000) 106:1149-57. doi:10.1172/JCI9944
21. Blackburn MR, Datta SK, Kellems RE. Adenosine deaminase-deficient mice generated using a two-stage genetic engineering strategy exhibit a combined immunodeficiency. J Biol Chem (1998) 273:5093-100. doi:10.1074/jbc.273.9.5093
22. Cassani B, Mirolo M, Cattaneo F, Benninghoff U, Hershfield M, Carlucci F, et al. Altered intracellular and extracellular signaling leads to impaired T-cell functions in ADA-SCID patients. Blood (2008) 111:4209-19. doi:10.1182/blood-2007-05-092429
23. Aldrich MB, Chen W, Blackburn MR, Martinez-Valdez H, Datta SK, Kellems RE. Impaired germinal center maturation in adenosine deaminase deficiency. J Immunol (2003) 171:5562-70. doi:10.4049/jimmunol.171.10.5562
24. Brigida I, Sauer AV, Ferrua F, Giannelli S, Scaramuzza S, Pistoia V, et al. B-cell development and functions and therapeutic options in adenosine deaminase-deficient patients. J Allergy Clin Immunol (2014) 133:799-806.e10. doi:10.1016/j.jaci.2013.12.1043
25. Nakazawa Y, Kawai T, Uchiyama T, Goto F, Watanabe N, Maekawa T, et al. Effects of enzyme replacement therapy on immune function in ADA deficiency patient. Clin Immunol (2015) 161:391-3. doi:10.1016/j.clim.2015.06.011
26. Gangi-Peterson L, Sorscher DH, Reynolds JW, Kepler TB, Mitchell BS. Nucleotide pool imbalance and adenosine deaminase deficiency induce alterations of N-region insertions during V(D)J recombination. J Clin Invest (1999) 103:833-41. doi:10.1172/JCI4320
27. Thompson CB. New insights into V(D)J recombination and its role in the evolution of the immune system. Immunity (1995) 3:531-9. doi:10.1016/1074-7613(95)90124-8
28. Cunningham-Rundles C. Autoimmunity in primary immune deficiency: taking lessons from our patients. Clin Exp Immunol (2011) 164(Suppl 2):6-11. doi:10.1111/j.1365-2249.2011.04388.x
29. Blackburn MR, Thompson LF. Adenosine deaminase deficiency: unanticipated benefits from the study of a rare immunodeficiency. J Immunol (2012) 188:933-5. doi:10.4049/jimmunol.1103519
30. Hershfield MS, Kredich NM, Ownby DR, Ownby H, Buckley R. In vivo inactivation of erythrocyte S-adenosylhomocysteine hydrolase by 2'-deoxyadenosine in adenosine deaminase-deficient patients. J Clin Invest (1979) 63:807-11. doi:10.1172/JCI109367
31. Yang JC, Cortopassi GA. dATP causes specific release of cytochrome C from mitochondria. Biochem Biophys Res Commun (1998) 250:454-7. doi:10.1006/bbrc.1998.9333
32. Zou H, Li Y, Liu X, Wang X. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem (1999) 274:11549-56. doi:10.1074/jbc.274.17.11549
33. Sitkovsky MV, Lukashev D, Apasov S, Kojima H, Koshiba M, Caldwell C, et al. Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors. Annu Rev Immunol (2004) 22:657-82. doi:10.1146/annurev.immunol.22.012703.104731
34. Wei CJ, Li W, Chen JF. Normal and abnormal functions of adenosine receptors in the central nervous system revealed by genetic knockout studies. Biochim Biophys Acta (2011) 1808:1358-79. doi:10.1016/j.bbamem.2010.12.018
35. Ribeiro JA, Sebastião AM, de Mendonça A. Adenosine receptors in the nervous system: pathophysiological implications. Prog Neurobiol (2002) 68:377-92. doi:10.1016/S0301-0082(02)00155-7
36. Sebastião AM, Ribeiro JA. Fine-tuning neuromodulation by adenosine. Trends Pharmacol Sci (2000) 21:341-6. doi:10.1016/S0165-6147(00)01517-0
37. Rogers MH, Lwin R, Fairbanks L, Gerritsen B, Gaspar HB. Cognitive and behavioral abnormalities in adenosine deaminase deficient severe combined immunodeficiency. J Pediatr (2001) 139:44-50. doi:10.1067/mpd.2001.115023
38. Titman P, Pink E, Skucek E, O'Hanlon K, Cole TJ, Gaspar J, et al. Cognitive and behavioral abnormalities in children after hematopoietic stem cell transplantation for severe congenital immunodeficiencies. Blood (2008) 112:3907-13. doi:10.1182/blood-2008-04-151332
39. Hershey AD. Effects of metabolic disorders on the brain: can these effects be reversed with bone marrow transplantation? J Pediatr (2001) 139:9-11. doi:10.1067/mpd.2001.116696
40. Kramer JH, Crittenden MR, DeSantes K, Cowan MJ. Cognitive and adaptive behavior 1 and 3 years following bone marrow transplantation. Bone Marrow Transplant (1997) 19:607-13. doi:10.1038/sj.bmt.1700699
41. Phipps S, Dunavant M, Srivastava DK, Bowman L, Mulhern RK. Cognitive and academic functioning in survivors of pediatric bone marrow transplantation. J Clin Oncol (2000) 18:1004-11
42. Uckan D, Cetin M, Yigitkanli I, Tezcan I, Tuncer M, Karasimav D, et al. Life-threatening neurological complications after bone marrow transplantation in children. Bone Marrow Transplant (2005) 35:71-6. doi:10.1038/sj.bmt.1704749
43. Saccucci P, Arpino C, Rizzo R, Gagliano A, Volzone A, Lalli C, et al. Association of adenosine deaminase polymorphism with mild mental retardation. J Child Neurol (2006) 21:753-6. doi:10.1177/08830738060210091201
44. Albuquerque W, Gaspar HB. Bilateral sensorineural deafness in adenosine deaminase-deficient severe combined immunodeficiency. J Pediatr (2004) 144:278-80. doi:10.1016/j.jpeds.2003.10.055
45. Tanaka C, Hara T, Suzaki I, Maegaki Y, Takeshita K. Sensorineural deafness in siblings with adenosine deaminase deficiency. Brain Dev (1996) 18:304-6. doi:10.1016/0387-7604(96)00014-9
46. Nofech-Mozes Y, Blaser SI, Kobayashi J, Grunebaum E, Roifman CM. Neurologic abnormalities in patients with adenosine deaminase deficiency. Pediatr Neurol (2007) 37:218-21. doi:10.1016/j.pediatrneurol.2007.03.011
47. Dehkordy SF, Aghamohammadi A, Ochs HD, Rezaei N. Primary immunodeficiency diseases associated with neurologic manifestations. J Clin Immunol (2012) 32:1-24. doi:10.1007/s10875-011-9593-8
48. Grunebaum E, Cohen A, Roifman CM. Recent advances in understanding and managing adenosine deaminase and purine nucleoside phosphorylase deficiencies. Curr Opin Allergy Clin Immunol (2013) 13:630-8. doi:10.1097/ACI.0000000000000006
49. Migchielsen AA, Breuer ML, van Roon MA, te Riele H, Zurcher C, Ossendorp F, et al. Adenosine-deaminase-deficient mice die perinatally and exhibit liver-cell degeneration, atelectasis and small intestinal cell death. Nat Genet (1995) 10:279-87. doi:10.1038/ng0795-279
50. Wakamiya M, Blackburn MR, Jurecic R, McArthur MJ, Geske RS, Cartwright J, et al. Disruption of the adenosine deaminase gene causes hepatocellular impairment and perinatal lethality in mice. Proc Natl Acad Sci U S A (1995) 92:3673-7. doi:10.1073/pnas.92.9.3673
51. Bollinger ME, Arredondo-Vega FX, Santisteban I, Schwarz K, Hershfield MS, Lederman HM. Brief report: hepatic dysfunction as a complication of adenosine deaminase deficiency. N Engl J Med (1996) 334:1367-71. doi:10.1056/NEJM199605233342104
52. Sokolic R, Koh C, Komarow H, Garabedian E, Silvin C, Cowen E, et al. The expanding clinical phenotype of adenosine deaminase (ADA) deficiency [abstract]. J Clin Immunol (2014) 34:139; In: 16th Biennial Meeting of the European Society for Immunodeficiencies; 2014 29 October-1 November; Prague, Czech Republic. Abstract nr ESID-0780. doi:10.1007/s10875-014-0101-9
53. Blackburn MR, Volmer JB, Thrasher JL, Zhong H, Crosby JR, Lee JJ, et al. Metabolic consequences of adenosine deaminase deficiency in mice are associated with defects in alveogenesis, pulmonary inflammation, and airway obstruction. J Exp Med (2000) 192:159-70. doi:10.1084/jem.192.2.159
54. Blackburn MR. Too much of a good thing: adenosine overload in adenosine-deaminase-deficient mice. Trends Pharmacol Sci (2003) 24:66-70. doi:10.1016/S0165-6147(02)00045-7
55. Chunn JL, Molina JG, Mi T, Xia Y, Kellems RE, Blackburn MR. Adenosine-dependent pulmonary fibrosis in adenosine deaminase-deficient mice. J Immunol (2005) 175:1937-46. doi:10.4049/jimmunol.175.3.1937
56. Dhanju R, Min W, Ackerley C, Cimpean L, Palaniyar N, Roifman CM, et al. Pulmonary alveolar proteinosis in adenosine deaminase-deficient mice. J Allergy Clin Immunol (2014) 133:1467-71, 1471.e1-4. doi:10.1016/j.jaci.2013.11.029
57. Booth C, Algar VE, Xu-Bayford J, Fairbanks L, Owens C, Gaspar HB. Non-infectious lung disease in patients with adenosine deaminase deficient severe combined immunodeficiency. J Clin Immunol (2012) 32:449-53. doi:10.1007/s10875-012-9658-3
58. Grunebaum E, Cutz E, Roifman CM. Pulmonary alveolar proteinosis in patients with adenosine deaminase deficiency. J Allergy Clin Immunol (2012) 129:1588-93. doi:10.1016/j.jaci.2012.02.003
59. Komarow HD, Sokolic R, Hershfield MS, Kohn DB, Young M, Metcalfe DD, et al. Impulse oscillometry identifies peripheral airway dysfunction in children with adenosine deaminase deficiency. Orphanet J Rare Dis (2015) 10:159. doi:10.1186/s13023-015-0365-z
60. Sauer AV, Mrak E, Hernandez RJ, Zacchi E, Cavani F, Casiraghi M, et al. ADA-deficient SCID is associated with a specific microenvironment and bone phenotype characterized by RANKL/OPG imbalance and osteoblast insufficiency. Blood (2009) 114:3216-26. doi:10.1182/blood-2009-03-209221
61. Ratech H, Greco MA, Gallo G, Rimoin DL, Kamino H, Hirschhorn R. Pathologic findings in adenosine deaminase-deficient severe combined immunodeficiency. I. Kidney, adrenal, and chondro-osseous tissue alterations. Am J Pathol (1985) 120:157-69
62. Hirschhorn R, Vawter GF, Kirkpatrick JA, Rosen FS. Adenosine deaminase deficiency: frequency and comparative pathology in autosomally recessive severe combined immunodeficiency. Clin Immunol Immunopathol (1979) 14:107-20. doi:10.1016/0090-1229(79)90131-4
63. Vallon V, Mühlbauer B, Osswald H. Adenosine and kidney function. Physiol Rev (2006) 86:901-40. doi:10.1152/physrev.00031.2005
64. Dai Y, Zhang W, Wen J, Zhang Y, Kellems RE, Xia Y. A2B adenosine receptor-mediated induction of IL-6 promotes CKD. J Am Soc Nephrol (2011) 22:890-901. doi:10.1681/ASN.2010080890
65. Roberts VS, Cowan PJ, Alexander SI, Robson SC, Dwyer KM. The role of adenosine receptors A2A and A2B signaling in renal fibrosis. Kidney Int (2014) 86:685-92. doi:10.1038/ki.2014.244
66. Kesserwan C, Sokolic R, Cowen EW, Garabedian E, Heselmeyer-Haddad K, Lee CC, et al. Multicentric dermatofibrosarcoma protuberans in patients with adenosine deaminase-deficient severe combined immune deficiency. J Allergy Clin Immunol (2012) 129:762-769.e1. doi:10.1016/j.jaci.2011.10.028