X-linked clonality testing: Interpretation and limitations

Blood

Volumn 110, Issue 5, 2007, Pages 1411-1419

  Chen, George L ^a   Prchal, Josef T ^b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; AGING; AUTOIMMUNE DISEASE; CELL SELECTION; CLONAL VARIATION; GENE EXPRESSION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC POLYMORPHISM; GENOTYPE; HEMATOPOIETIC CELL; HUMAN; LYMPHOMA; MINIMAL RESIDUAL DISEASE; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SOMATIC MUTATION; X CHROMOSOME INACTIVATION;

EID: 34548836555     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-09-018655     Document Type: Review

References (85)

1. Adolphson CC, Prchal JT, Carroll AJ. Colonic villous adenoma: monoclonal origin. JAMA. 1982;247:829-830.
2. Adamson JW, Fialkow PJ, Murphy S, Prchal JF, Steinmann L. Polycythemia vera: stem-cell and probable clonal origin of the disease. N Engl J Med. 1976;295:913-916.
3. Prchal JT, Throckmorton DW, Carroll AJ III, Fuson EW, Gams RA, Prchal JF. A common progenitor for human myeloid and lymphoid cells. Nature. 1978;274:590-591.
4. Mesa RA, Li CY, Ketterling RP, Schroeder GS, Knudson RA, Tefferi A. Leukemic transformation in myelofibrosis with myeloid metaplasia: a single-institution experience with 91 cases. Blood. 2005;105:973-977.
5. Rowley JD. A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining [Letter]. Nature. 1973;243:290-293.
6. Bahloul M, Asnafi V, Macintyre E. Clinical impact of molecular diagnostics in low-grade lymphoma. Best Pract Res Clin Haematol. 2005;18:97-111.
7. Venditti A, Buccisano F, Del Poeta G, et al. Level of minimal residual disease after consolidation therapy predicts outcome in acute myeloid leukemia. Blood. 2000;96:3948-3952.
8. San Miguel JF, Vidriales MB, Lopez-Berges C, et al. Early immunophenotypical evaluation of minimal residual disease in acute myeloid leukemia identifies different patient risk groups and may contribute to postinduction treatment stratification. Blood. 2001;98:1746-1751.
9. Langebrake C, Brinkmann I, Teigler-Schlegel A, et al. Immunophenotypic differences between diagnosis and relapse in childhood AML: Implications for MRD monitoring. Cytometry B Clin Cytom. 2005;63:1-9.
10. Li A, Zhou J, Zuckerman D, et al. Sequence analysis of clonal immunoglobulin and T-cell receptor gene rearrangements in children with acute lymphoblastic leukemia at diagnosis and at relapse: implications for pathogenesis and for the clinical utility of PCR-based methods of minimal residual disease detection. Blood. 2003;102:4520-4526.
11. Gallagher RE, Yeap BY, Bi W, et al. Quantitative real-time RT-PCR analysis of PML-RAR alpha mRNA in acute promyelocytic leukemia: assessment of prognostic significance in adult patients from intergroup protocol 0129. Blood. 2003;101:2521-2528.
12. Nucifora G, Larson RA, Rowley JD. Persistence of the 8;21 translocation in patients with acute myeloid leukemia type M2 in long-term remission. Blood. 1993;82:712-715.
13. Potter MN, Steward CG, Oakhill A. The significance of detection of minimal residual disease in childhood acute lymphoblastic leukaemia. Br J Haematol. 1993;83:412-418.
14. Radich JP, Gehly G, Gooley T, et al. Polymerase chain reaction detection of the BCR-ABL fusion transcript after allogeneic marrow transplantation for chronic myeloid leukemia: results and implications in 346 patients. Blood. 1995;85:2632-2638.
15. Lin F, van Rhee F, Goldman JM, Cross NC. Kinetics of increasing BCR-ABL transcript numbers in chronic myeloid leukemia patients who relapse after bone marrow transplantation. Blood. 1996;87:4473-4478.
16. Olavarria E, Kanfer E, Szydlo R, et al. Early detection of BCR-ABL transcripts by quantitative reverse transcriptase-polymerase chain reaction predicts outcome after allogeneic stem cell transplantation for chronic myeloid leukemia. Blood. 2001;97:1560-1565.
17. Beutler E, Collins Z, Irwin LE. Value of genetic variants of glucose-6-phosphate dehydrogenase in tracing the origin of malignant tumors. N Engl J Med. 1967;276:389-391.
18. Beutler E, Yeh M, Fairbanks VF. The normal human female as a mosaic of X-chromosome activity: studies using the gene for C-6-PD-deficiency as a marker. Proc Natl Acad Sci U S A. 1962;48:9-16.
19. Lyon MF. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature. 1961;190:372-373.
20. Ohno S, Makino S. The single-X nature of sex chromatin in man. Lancet. 1961;1:78-79.
21. Ohno S, Hauschka TS. Allocycly of the X-chromosome in tumors and normal tissues. Cancer Res. 1960;20:541-545.
22. Brown CJ, Hendrich BD, Rupert JL, et al. The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell. 1992;71:527-542.
23. Lee JT, Davidow LS, Warshawsky D. Tsix, a gene antisense to Xist at the X-inactivation centre. Nat Genet. 1999;21:400-404.
24. Ogawa Y, Lee JT. Xite, X-inactivation intergenic transcription elements that regulate the probability of choice. Mol Cell. 2003;11:731-743.
25. Brockdorff N, Ashworth A, Kay GF, et al. The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell. 1992;71:515-526.
26. Clemson CM, McNeil JA, Willard HF, Lawrence JB. XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J Cell Biol. 1996;132:259-275.
27. Penny GD, Kay GF, Sheardown SA, Rastan S, Brockdorff N. Requirement for Xist in X chromosome inactivation. Nature. 1996;379:131-137.
28. Popova BC, Tada T, Takagi N, Brockdorff N, Nesterova TB. Attenuated spread of X-inactivation in an X-autosome translocation. Proc Natl Acad Sci U S A. 2006;103:7706-7711.
29. Lee JT. Disruption of imprinted X inactivation by parent-of-origin effects at Tsix. Cell. 2000;103:17-27.
30. Sado T, Wang Z, Sasaki H, Li E. Regulation of imprinted X-chromosome inactivation in mice by Tsix. Development. 2001;128:1275-1286.
31. Heard E. Recent advances in X-chromosome inactivation. Curr Opin Cell Biol. 2004;16:247-255.
32. Xu N, Tsai CL, Lee JT. Transient homologous chromosome pairing marks the onset of X inactivation. Science. 2006;311:1149-1152.
33. Bacher CP, Guggiari M, Brors B, et al. Transient colocalization of X-inactivation centres accompanies the initiation of X inactivation. Nat Cell Biol. 2006;8:293-299.
34. Gartler SM, Riggs AD. Mammalian X-chromosome inactivation. Annu Rev Genet. 1983;17:155-190.
35. Huynh KD, Lee JT. Inheritance of a pre-inactivated paternal X chromosome in early mouse embryos. Nature. 2003;426:857-862.
36. Okamoto I, Otte AP, Allis CD, Reinberg D, Heard E. Epigenetic dynamics of imprinted X inactivation during early mouse development. Science. 2004;303:644-649.
37. Puck JM, Stewart CC, Nussbaum RL. Maximum-likelihood analysis of human T-cell X chromosome inactivation patterns: normal women versus carriers of X-linked severe combined immunodeficiency. Am J Hum Genet. 1992;50:742-748.
38. Prchal JT, Prchal JF, Belickova M, et al. Clonal stability of blood cell lineages indicated by X-chromosomal transcriptional polymorphism. J Exp Med. 1996;183:561-567.
39. Curnutte JT, Hopkins PJ, Kuhl W, Beutler E. Studying X inactivation. Lancet. 1992;339:749.
40. Prchal JT, Guan YL. A novel clonality assay based on transcriptional analysis of the active X chromosome. Stem Cells. 1993;11(Suppl 1):62-65.
41. Gregg XT, Kralovics R, Prchal JT. A polymorphism of the X-linked gene IDS increases the number of females informative for transcriptional clonality assays. Am J Hematol. 2000;63:184-191.
42. el-Kassar N, Hetet G, Briere J, Grandchamp B. Clonality analysis of hematopoiesis in essential thrombocythemia: advantages of studying T lymphocytes and platelets. Blood. 1997;89:128-134.
43. Luhovy M, Liu Y, Belickova M, Prchal JF, Prchal JT. A novel clonality assay based on transcriptional polymorphism of X chromosome gene p55. Biol Blood Marrow Transplant. 1995;1:81-87.
44. Liu E, Jelinek J, Pastore YD, Guan Y, Prchal JF, Prchal JT. Discrimination of polycythemias and thrombocytoses by novel, simple, accurate clonality assays and comparison with PRV-1 expression and BFU-E response to erythropoietin. Blood. 2003;101:3294-3301.
45. Allen RC, Zoghbi HY, Moseley AB, Rosenblatt HM, Belmont JW. Methylation of HpaII and HhaI sites near the polymorphic CAG repeat in the human androgen-receptor gene correlates with X chromosome inactivation. Am J Hum Genet. 1992;51:1229-1239.
46. Belmont JW. Genetic control of X inactivation and processes leading to X-inactivation skewing. Am J Hum Genet. 1996;58:1101-1108.
47. Vogelstein B, Fearon ER, Hamilton SR, Feinberg AP. Use of restriction fragment length polymorphisms to determine the clonal origin of human tumors. Science. 1985;227:642-645.
48. Gale RE, Wheadon H, Linch DC. X-chromosome inactivation patterns using HPRT and PGK polymorphisms in haematologically normal and postchemotherapy females. Br J Haematol. 1991;79:193-197.
49. Carrel L, Willard HF. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature. 2005;434:400-404.
50. Liu Y, Phelan J, Go RC, Prchal JF, Prchal JT. Rapid determination of clonality by detection of two closely-linked X chromosome exonic polymorphisms using allele-specific PCR. J Clin Invest. 1997;99:1984-1990.
51. Plenge RM, Hendrich BD, Schwartz C, et al. A promoter mutation in the XIST gene in two unrelated families with skewed X-chromosome inactivation. Nat Genet. 1997;17:353-356.
52. Carroll AJ, Prchal JT, Crist WM, Prchal JF. Cellular expression of Wiskott-Aldrich allele. Lancet. 1980;1:601-602.
53. Prchal JT, Carroll AJ, Prchal JF, et al. Wiskott-Aldrich syndrome: cellular impairments and their implication for carrier detection. Blood. 1980;56:1048-1054.
54. Parolini O, Ressmann G, Haas OA, et al. X-linked Wiskott-Aldrich syndrome in a girl. N Engl J Med. 1998;338:291-295.
55. Hittner HM, Carroll AJ, Prchal JT. Linkage studies in carriers of Lowe oculo-cerebro-renal syndrome. Am J Hum Genet. 1982;34:966-971.
56. Haire RN, Ohta Y, Strong SJ, et al. Unusual patterns of exon skipping in Bruton tyrosine kinase are associated with mutations involving the intron 17 3′ splice site. Am J Hum Genet. 1997;60:798-807.
57. Luzzatto L, Usanga EA, Bienzle U, Esan GF, Fusuan FA. Imbalance in X-chromosome expression: evidence for a human X-linked gene affecting growth of hemopoietic cells. Science. 1979;205:1418-1420.
58. Filosa S, Giacometti N, Wangwei C, et al. Somatic-cell selection is a major determinant of the blood-cell phenotype in heterozygotes for glucose-6-phosphate dehydrogenase mutations causing severe enzyme deficiency. Am J Hum Genet. 1996;59:887-895.
59. Busque L, Mio R, Mattioli J, et al. Nonrandom X-inactivation patterns in normal females: lyonization ratios vary with age. Blood. 1996;88:59-65.
60. Sandovici I, Naumova AK, Leppert M, Linares Y, Sapienza C. A longitudinal study of X-inactivation ratio in human females. Hum Genet. 2004;115:387-392.
61. Kristiansen M, Knudsen GP, Bathum L, et al. Twin study of genetic and aging effects on X chromosome inactivation. Eur J Hum Genet. 2005;13:599-606.
62. Racchi O, Mangerini R, Rapezzi D, Rolfo M, Gaetani GF, Ferraris AM. X chromosome inactivation patterns in normal females. Blood Cells Mol Dis. 1998;24:439-447.
63. Abkowitz JL, Taboada M, Shelton GH, Catlin SN, Guttorp P, Kiklevich JV. An X chromosome gene regulates hematopoietic stem cell kinetics. Proc Natl Acad Sci U S A. 1998;95:3862-3866.
64. Christensen K, Kristiansen M, Hagen-Larsen H, et al. X-linked genetic factors regulate hematopoietic stem-cell kinetics in females. Blood. 2000;95:2449-2451.
65. Vickers MA, McLeod E, Spector TD, Wilson IJ. Assessment of mechanism of acquired skewed X inactivation by analysis of twins. Blood. 2001;97:1274-1281.
66. Cotter PD, May A, Fitzsimons EJ, et al. Late-onset X-linked sideroblastic anemia. Missense mutations in the erythroid delta-aminolevulinate synthase (ALAS2) gene in two pyridoxine-responsive patients initially diagnosed with acquired refractory anemia and ringed sideroblasts. J Clin Invest. 1995;96:2090-2096.
67. Invernizzi P, Miozzo M, Battezzati PM, et al. Frequency of monosomy X in women with primary biliary cirrhosis. Lancet. 2004;363:533-535.
68. Brix TH, Knudsen GP, Kristiansen M, Kyvik KO, Orstavik KH, Hegedus L. High frequency of skewed X-chromosome inactivation in females with autoimmune thyroid disease: a possible explanation for the female predisposition to thyroid autoimmunity. J Clin Endocrinol Metab. 2005;90:5949-5953.
69. Ozbalkan Z, Bagislar S, Kiraz S, et al. Skewed X chromosome inactivation in blood cells of women with scleroderma. Arthritis Rheum. 2005;52:1564-1570.
70. Ranke MB, Saenger P. Turner's syndrome. Lancet. 2001;358:309-314.
71. Invernizzi P, Miozzo M, Selmi C, et al. X chromosome monosomy: a common mechanism for autoimmune diseases. J Immunol. 2005;175:575-578.
72. Gartler SM, Goldman MA. Biology of the X chromosome. Curr Opin Pediatr. 2001;13:340-345.
73. Imrie H, Vaidya B, Perros P, et al. Evidence for a Graves' disease susceptibility locus at chromosome Xp11 in a United Kingdom population. J Clin Endocrinol Metab. 2001;86:626-630.
74. Barbesino G, Tomer Y, Concepcion ES, Davies TF, Greenberg DA. Linkage analysis of candidate genes in autoimmune thyroid disease. II. Selected gender-related genes and the X-chromosome. International Consortium for the Genetics of Autoimmune Thyroid Disease. J Clin Endocrinol Metab. 1998;83:3290-3295.
75. Campbell PJ, Baxter EJ, Beer PA, et al. Mutation of JAK2 in the myeloproliferative disorders: timing, clonality studies, cytogenetic associations, and role in leukemic transformation. Blood. 2006;108:3548-3555.
76. James C, Ugo V, Le Couedic JP, et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature. 2005;434:1144-1148.
77. Kralovics R, Passamonti F, Buser AS, et al. A gain-of-function mutation of JAK2 in myeloproliferative disorders. N Engl J Med. 2005;352:1779-1790.
78. Zhao R, Xing S, Li Z, et al. Identification of an acquired JAK2 mutation in polycythemia vera. J Biol Chem. 2005;280:22788-22792.
79. Baxter EJ, Scott LM, Campbell PJ, et al. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet. 2005;365:1054-1061.
80. Kralovics R, Teo SS, Li S, et al. Acquisition of the V617F mutation of JAK2 is a late genetic event in a subset of patients with myeloproliferative disorders. Blood. 2006;108:1377-1380.
81. Nussenzveig RH, Swierczek SI, Jelinek J, et al. Polycythemia vera is not initiated by JAK2V617F mutation. Exp Hematol. 2007;35:32-38.
82. Levine RL, Belisle C, Wadleigh M, et al. X-inactivation-based clonality analysis and quantitative JAK2V617F assessment reveal a strong association between clonality and JAK2V617F in PV but not ET/MMM, and identifies a subset of JAK2V617F-negative ET and MMM patients with clonal hematopoiesis. Blood. 2006;107:4139-4141.
83. Kiladjian JJ, Elkassar N, Cassinat B, et al. Essential thrombocythemias without V617F JAK2 mutation are clonal hematopoietic stem cell disorders. Leukemia. 2006;20:1181-1183.
84. Antonioli E, Guglielmelli P, Pancrazzi A, et al. Clinical implications of the JAK2 V617F mutation in essential thrombocythemia. Leukemia. 2005;19:1847-1849.
85. Jelinek J, Oki Y, Gharibyan V, et al. JAK2 mutation 1849G >T is rare in acute leukemias but can be found in CMML, Philadelphia-chromosome negative CML and megakaryocytic leukemia. Blood. 2005;106:3370-3373.