Historical Review on Genetic Analysis in Hemophilia A

Seminars in Thrombosis and Hemostasis

Volumn 40, Issue 8, 2014, Pages 895-902

  Oldenburg, Johannes ^a   Pezeshkpoor, Behnaz ^a   Pavlova, Anna ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

F8 gene mutations; genetic analysis; hemophilia A; historic overview

Indexed keywords

ARTICLE; BLEEDING TENDENCY; CLINICAL FEATURE; DENATURING GRADIENT GEL ELECTROPHORESIS; DENATURING HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; DISEASE COURSE; GENE MUTATION; GENE REARRANGEMENT; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC COUNSELING; GENETIC POLYMORPHISM; GENOTYPE; GENOTYPE PHENOTYPE CORRELATION; HEMOPHILIA A; HUMAN; MUTATIONAL ANALYSIS; NEXT GENERATION SEQUENCING; POINT MUTATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; RISK ASSESSMENT; X CHROMOSOME;

EID: 84939455260     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0034-1395161     Document Type: Article

References (91)

1. Mannucci P. M., Tuddenham E. G. The hemophilias-from royal genes to gene therapy. N Engl J Med: 2001; 344 23 1773 1779
2. Ichinose A. Physiopathology and regulation of factor XIII. Thromb Haemost: 2001; 86 1 57 65
3. Oldenburg J., El-Maarri O. New insight into the molecular basis of hemophilia A. Int J Hematol: 2006; 83 2 96 102
4. Levinson B., Kenwrick S., Lakich D., Hammonds G. Jr, Gitschier J. A transcribed gene in an intron of the human factor VIII gene. Genomics: 1990; 7 1 1 11
5. Levinson B., Kenwrick S., Gamel P., Fisher K., Gitschier J. Evidence for a third transcript from the human factor VIII gene. Genomics: 1992; 14 3 585 589
6. Peters M. F., Ross C. A. Isolation of a 40-kDa Huntingtin-associated protein. J Biol Chem: 2001; 276 5 3188 3194
7. Lakich D., Kazazian H. H. Jr, Antonarakis S. E., Gitschier J. Inversions disrupting the factor VIII gene are a common cause of severe haemophilia A. Nat Genet: 1993; 5 3 236 241
8. Naylor J. A., Buck D., Green P., Williamson H., Bentley D., Giannelli F. Investigation of the factor VIII intron 22 repeated region (int22h) and the associated inversion junctions. Hum Mol Genet: 1995; 4 7 1217 1224
9. Bagnall R. D., Waseem N., Green P. M., Giannelli F. Recurrent inversion breaking intron 1 of the factor VIII gene is a frequent cause of severe hemophilia A. Blood: 2002; 99 1 168 174
10. Schröder J., El-Maarri O., Schwaab R., Müller C. R., Oldenburg J. Factor VIII intron-1 inversion: frequency and inhibitor prevalence. J Thromb Haemost: 2006; 4 5 1141 1143
11. Biggs R., Rizza C. R. The sporadic case of haemophilia A. Lancet: 1976; 2 7983 431 433
12. Kasper C. K., Lin J. C. Prevalence of sporadic and familial haemophilia. Haemophilia: 2007; 13 1 90 92
13. Oldenburg J., Schwaab R., Grimm T., et al. Direct and indirect estimation of the sex ratio of mutation frequencies in hemophilia A. Am J Hum Genet: 1993; 53 6 1229 1238
14. Vogel F. A probable sex difference in some mutation rates. Am J Hum Genet: 1977; 29 3 312 319
15. Strauss H. S. The perpetuation of hemophilia by mutation. Pediatrics: 1967; 39 2 186 193
16. Becker J., Schwaab R., Möller-Taube A., et al. Characterization of the factor VIII defect in 147 patients with sporadic hemophilia A: family studies indicate a mutation type-dependent sex ratio of mutation frequencies. Am J Hum Genet: 1996; 58 4 657 670
17. Tuddenham E. G. Flip tip inversion and haemophilia A. Lancet: 1994; 343 8893 307 308
18. Leuer M., Oldenburg J., Lavergne J. M., et al. Somatic mosaicism in hemophilia A: a fairly common event. Am J Hum Genet: 2001; 69 1 75 87
19. Oldenburg J., Rost S., El-Maarri O., et al. De novo factor VIII gene intron 22 inversion in a female carrier presents as a somatic mosaicism. Blood: 2000; 96 8 2905 2906
20. Gitschier J., Wood W. I., Goralka T. M., et al. Characterization of the human factor VIII gene. Nature: 1984; 312 5992 326 330
21. Toole J. J., Knopf J. L., Wozney J. M., et al. Molecular cloning of a cDNA encoding human antihaemophilic factor. Nature: 1984; 312 5992 342 347
22. Schwaab R., Oldenburg J., Higuchi M., et al. Haemophilia A: carrier detection by DNA analysis. Blut: 1988; 57 2 85 90
23. Schwaab R., Oldenburg J., Brackmann H. H., Hanfland P. Hemophilia A: molecular biology and carrier diagnosis [in German]. Infusionsther Transfusionsmed: 1994; 21 2 116 125
24. Peake I. R., Lillicrap D. P., Boulyjenkov V., et al. Haemophilia: strategies for carrier detection and prenatal diagnosis. Bull World Health Organ: 1993; 71 3-4 429 458
25. Bernardi F., Marchetti G., Bertagnolo V., et al. RFLP analysis in families with sporadic hemophilia A. Estimate of the mutation ratio in male and female gametes. Hum Genet: 1987; 76 3 253 256
26. Harper K., Winter R. M., Pembrey M. E., Hartley D., Davies K. E., Tuddenham E. G. A clinically useful DNA probe closely linked to haemophilia A. Lancet: 1984; 2 8393 6 8
27. Gitschier J., Lawn R. M., Rotblat F., Goldman E., Tuddenham E. G. Antenatal diagnosis and carrier detection of haemophilia A using factor VIII gene probe. Lancet: 1985; 1 8437 1093 1094
28. Wion K. L., Tuddenham E. G., Lawn R. M. A new polymorphism in the factor VIII gene for prenatal diagnosis of hemophilia A. Nucleic Acids Res: 1986; 14 11 4535 4542
29. Lalloz M. R., McVey J. H., Pattinson J. K., Tuddenham E. G. Haemophilia A diagnosis by analysis of a hypervariable dinucleotide repeat within the factor VIII gene. Lancet: 1991; 338 8761 207 211
30. Lalloz M. R., Schwaab R., McVey J. H., Michaelides K., Tuddenham E. G. Haemophilia A diagnosis by simultaneous analysis of two variable dinucleotide tandem repeats within the factor VIII gene. Br J Haematol: 1994; 86 4 804 809
31. Lin S. Y., Su Y. N., Hung C. C., et al. Mutation spectrum of 122 hemophilia A families from Taiwanese population by LD-PCR, DHPLC, multiplex PCR and evaluating the clinical application of HRM. BMC Med Genet: 2008; 9 53
32. Schwaab R., Ludwig M., Oldenburg J., et al. Identical point mutations in the factor VIII gene that have different clinical manifestations of hemophilia A. Am J Hum Genet: 1990; 47 4 743 744
33. Schwaab R., Oldenburg J., Tuddenham E. G., Brackmann H. H., Olek K. Mutations in haemophilia A. Br J Haematol: 1993; 83 3 450 458
34. Schwaab R., Oldenburg J., Schwaab U., et al. Characterization of mutations within the factor VIII gene of 73 unrelated mild and moderate haemophiliacs. Br J Haematol: 1995; 91 2 458 464
35. Higuchi M., Antonarakis S. E., Kasch L., et al. Molecular characterization of mild-to-moderate hemophilia A: detection of the mutation in 25 of 29 patients by denaturing gradient gel electrophoresis. Proc Natl Acad Sci U S A: 1991; 88 19 8307 8311
36. Higuchi M., Kazazian H. H. Jr, Kasch L., et al. Molecular characterization of severe hemophilia A suggests that about half the mutations are not within the coding regions and splice junctions of the factor VIII gene. Proc Natl Acad Sci U S A: 1991; 88 16 7405 7409
37. Lakich D., Kazazian H. H. Jr, Antonarakis S. E., Gitschier J. Inversions disrupting the factor VIII gene are a common cause of severe haemophilia A. Nat Genet.: 1993; 21 2 236 241
38. Liu Q., Nozari G., Sommer S. S. Single-tube polymerase chain reaction for rapid diagnosis of the inversion hotspot of mutation in hemophilia A. Blood: 1998; 92 4 1458 1459
39. Rossetti L. C., Radic C. P., Larripa I. B., De Brasi C. D. Genotyping the hemophilia inversion hotspot by use of inverse PCR. Clin Chem: 2005; 51 7 1154 1158
40. Brinke A., Tagliavacca L., Naylor J., Green P., Giangrande P., Giannelli F. Two chimaeric transcription units result from an inversion breaking intron 1 of the factor VIII gene and a region reportedly affected by reciprocal translocations in T-cell leukaemia. Hum Mol Genet: 1996; 5 12 1945 1951
41. Mullis K. B., Faloona F. A. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol: 1987; 155 335 350
42. Mullis K. B. Target amplification for DNA analysis by the polymerase chain reaction. Ann Biol Clin (Paris): 1990; 48 8 579 582
43. Lin S. W., Lin S. R., Shen M. C. Characterization of genetic defects of hemophilia A in patients of Chinese origin. Genomics: 1993; 18 3 496 504
44. Williams I. J., Abuzenadah A., Winship P. R., et al. Precise carrier diagnosis in families with haemophilia A: use of conformation sensitive gel electrophoresis for mutation screening and polymorphism analysis. Thromb Haemost: 1998; 79 4 723 726
45. Waseem N. H., Bagnall R., Green P. M., Giannelli F.; Haemophilia Centres. Start of UK confidential haemophilia A database: analysis of 142 patients by solid phase fluorescent chemical cleavage of mismatch. Thromb Haemost: 1999; 81 6 900 905
46. Oldenburg J., Ivaskevicius V., Rost S., et al. Evaluation of DHPLC in the analysis of hemophilia A. J Biochem Biophys Methods: 2001; 47 1-2 39 51
47. Antonarakis S. E., Kazazian H. H., Gitschier J., Hutter P., de Moerloose P., Morris M. A. Molecular etiology of factor VIII deficiency in hemophilia A. Adv Exp Med Biol: 1995; 386 19 34
48. Pezeshkpoor B., Zimmer N., Marquardt N., et al. Deep intronic 'mutations' cause hemophilia A: application of next generation sequencing in patients without detectable mutation in F8 cDNA. J Thromb Haemost: 2013; 11 9 1679 1687
49. Voelkerding K. V., Dames S., Durtschi J. D. Next generation sequencing for clinical diagnostics-principles and application to targeted resequencing for hypertrophic cardiomyopathy: a paper from the 2009 William Beaumont Hospital Symposium on Molecular Pathology. J Mol Diagn: 2010; 12 5 539 551
50. Acquila M., Pasino M., Di Duca M., Bottini F., Molinari A. C., Bicocchi M. P. MLPA assay in F8 gene mutation screening. Haemophilia: 2008; 14 3 625 627
51. Rost S., Löffler S., Pavlova A., Müller C. R., Oldenburg J. Detection of large duplications within the factor VIII gene by MLPA. J Thromb Haemost: 2008; 6 11 1996 1999
52. Oldenburg J., Schröder J., Schmitt C., Brackmann H. H., Schwaab R. Small deletion/insertion mutations within poly-A runs of the factor VIII gene mitigate the severe haemophilia A phenotype. Thromb Haemost: 1998; 79 2 452 453
53. Youssoufian H., Antonarakis S. E., Bell W., Griffin A. M., Kazazian H. H. Jr. Nonsense and missense mutations in hemophilia A: estimate of the relative mutation rate at CG dinucleotides. Am J Hum Genet: 1988; 42 5 718 725
54. El-Maarri O., Olek A., Balaban B., et al. Methylation levels at selected CpG sites in the factor VIII and FGFR3 genes, in mature female and male germ cells: implications for male-driven evolution. Am J Hum Genet: 1998; 63 4 1001 1008
55. Tavassoli K., Eigel A., Horst J. A deletion/insertion leading to the generation of a direct repeat as a result of slipped mispairing and intragenic recombination in the factor VIII gene. Hum Genet: 1999; 104 5 435 437
56. Woods-Samuels P., Kazazian H. H. Jr, Antonarakis S. E. Nonhomologous recombination in the human genome: deletions in the human factor VIII gene. Genomics: 1991; 10 1 94 101
57. Vidal F., Farssac E., Tusell J., Puig L., Gallardo D. First molecular characterization of an unequal homologous alu-mediated recombination event responsible for hemophilia. Thromb Haemost: 2002; 88 1 12 16
58. Rossetti L. C., Goodeve A., Larripa I. B., De Brasi C. D. Homeologous recombination between AluSx-sequences as a cause of hemophilia. Hum Mutat: 2004; 24 5 440
59. Van de Water N., Williams R., Ockelford P., Browett P. A 20.7kb deletion within the factor VIII gene associated with LINE-1 element insertion. Thromb Haemost: 1998; 79 5 938 942
60. Sheen C. R., Jewell U. R., Morris C. M., et al. Double complex mutations involving F8 and FUNDC2 caused by distinct break-induced replication. Hum Mutat: 2007; 28 12 1198 1206
61. Pezeshkpoor B., Rost S., Oldenburg J., El-Maarri O. Identification of a third rearrangement at Xq28 that causes severe hemophilia A as a result of homologous recombination between inverted repeats. J Thromb Haemost: 2012; 10 8 1600 1608
62. Bowen D. J. Haemophilia A and haemophilia B: molecular insights. Mol Pathol: 2002; 55 1 1 18
63. Young M., Inaba H., Hoyer L. W., Higuchi M., Kazazian H. H. Jr, Antonarakis S. E. Partial correction of a severe molecular defect in hemophilia A, because of errors during expression of the factor VIII gene. Am J Hum Genet: 1997; 60 3 565 573
64. Leyte A., van Schijndel H. B., Niehrs C., et al. Sulfation of Tyr1680 of human blood coagulation factor VIII is essential for the interaction of factor VIII with von Willebrand factor. J Biol Chem: 1991; 266 2 740 746
65. Leyte A., Voorberg J., Van Schijndel H. B., Duim B., Pannekoek H., Van Mourik J. A. The pro-polypeptide of von Willebrand factor is required for the formation of a functional factor VIII-binding site on mature von Willebrand factor. Biochem J: 1991; 274 Pt 1 257 261
66. Gilles J. G., Lavend'homme R., Peerlinck K., et al. Some factor VIII (FVIII) inhibitors recognise a FVIII epitope(s) that is present only on FVIII-vWF complexes. Thromb Haemost: 1999; 82 1 40 45
67. Stoylova S. S., Lenting P. J., Kemball-Cook G., Holzenburg A. Electron crystallography of human blood coagulation factor VIII bound to phospholipid monolayers. J Biol Chem: 1999; 274 51 36573 36578
68. Zimmermann M. A., Gehrig A., Oldenburg J., Müller C. R., Rost S. Analysis of F8 mRNA in haemophilia A patients with silent mutations or presumptive splice site mutations. Haemophilia: 2013; 19 2 310 317
69. Pahl S., Pavlova A., Driesen J., Oldenburg J. Effect of F8 B domain gene variants on synthesis, secretion, activity and stability of factor VIII protein. Thromb Haemost: 2014; 111 1 58 66
70. Castaman G., Giacomelli S. H., Mancuso M. E., et al. Deep intronic variations may cause mild hemophilia A. J Thromb Haemost: 2011; 9 8 1541 1548
71. Ogata K., Selvaraj S. R., Miao H. Z., Pipe S. W. Most factor VIII B domain missense mutations are unlikely to be causative mutations for severe hemophilia A: implications for genotyping. J Thromb Haemost: 2011; 9 6 1183 1190
72. Oldenburg J., Brackmann H. H., Schwaab R. Risk factors for inhibitor development in hemophilia A. Haematologica: 2000; 85 (10, Suppl): 7 13, discussion 13-14
73. Schwaab R., Brackmann H. H., Meyer C., et al. Haemophilia A: mutation type determines risk of inhibitor formation. Thromb Haemost: 1995; 74 6 1402 1406
74. Oldenburg J., Pavlova A. Genetic risk factors for inhibitors to factors VIII and IX. Haemophilia: 2006; 12 06 15 22
75. Schwaab R., Pavlova A., Albert T., Caspers M., Oldenburg J. Significance of F8 missense mutations with respect to inhibitor formation. Thromb Haemost: 2013; 109 3 464 470
76. Schwaab R., Oldenburg J., Kemball-Cook G., et al. Assay discrepancy in mild haemophilia A due to a factor VIII missense mutation (Asn694Ile) in a large Danish family. Br J Haematol: 2000; 109 3 523 528
77. Rodgers S. E., Duncan E. M., Barbulescu D. M., Quinn D. M., Lloyd J. V. In vitro kinetics of factor VIII activity in patients with mild haemophilia A and a discrepancy between one-stage and two-stage factor VIII assay results. Br J Haematol: 2007; 136 1 138 145
78. Oldenburg J., Pavlova A. Discrepancy between one-stage and chromogenic factor VIII activity assay results can lead to misdiagnosis of haemophilia A phenotype. Hamostaseologie: 2010; 30 4 207 211
79. Pavlova A., Delev D., Pezeshkpoor B., Müller J., Oldenburg J. Haemophilia A mutations in patients with non-severe phenotype associated with a discrepancy between one-stage and chromogenic factor VIII activity assays. Thromb Haemost: 2014; 111 5 851 861
80. Hakeos W. H., Miao H., Sirachainan N., et al. Hemophilia A mutations within the factor VIII A2-A3 subunit interface destabilize factor VIIIa and cause one-stage/two-stage activity discrepancy. Thromb Haemost: 2002; 88 5 781 787
81. Pipe S. W., Saenko E. L., Eickhorst A. N., Kemball-Cook G., Kaufman R. J. Hemophilia A mutations associated with 1-stage/2-stage activity discrepancy disrupt protein-protein interactions within the triplicated A domains of thrombin-activated factor VIIIa. Blood: 2001; 97 3 685 691
82. Pavlova A., Oldenburg J. Defining severity of hemophilia: more than factor levels. Semin Thromb Hemost: 2013; 39 7 702 710
83. Santagostino E., Gringeri A., Tagliavacca L., Mannucci P. M. Inhibitors to factor VIII in a family with mild hemophilia: molecular characterization and response to factor VIII and desmopressin. Thromb Haemost: 1995; 74 2 619 621
84. Zimmermann M. A., Oldenburg J., Müller C. R., Rost S. Characterization of duplication breakpoints in the factor VIII gene. J Thromb Haemost: 2010; 8 12 2696 2704
85. Uen C., Oldenburg J., Schröder J., et al. 2% Haemophilia A patients without mutation in the FVIII gene [in German]. Hamostaseologie: 2003; 23 1 1 5
86. El-Maarri O., Herbiniaux U., Graw J., et al. Analysis of mRNA in hemophilia A patients with undetectable mutations reveals normal splicing in the factor VIII gene. J Thromb Haemost: 2005; 3 2 332 339
87. Pezeshkpoor B., Pavlova A., Oldenburg J., El-Maarri O. F8 genetic analysis strategies when standard approaches fail. Haemostaseologie: 2014; 34 2 167 173
88. Zhang B., Cunningham M. A., Nichols W. C., et al. Bleeding due to disruption of a cargo-specific ER-to-Golgi transport complex. Nat Genet: 2003; 34 2 220 225
89. Nichols W. C., Seligsohn U., Zivelin A., et al. Mutations in the ER-Golgi intermediate compartment protein ERGIC-53 cause combined deficiency of coagulation factors V and VIII. Cell: 1998; 93 1 61 70
90. Spreafico M., Peyvandi F. Combined FV and FVIII deficiency. Haemophilia: 2008; 14 6 1201 1208
91. Zhang B., McGee B., Yamaoka J. S., et al. Combined deficiency of factor V and factor VIII is due to mutations in either LMAN1 or MCFD2. Blood: 2006; 107 5 1903 1907