C K Hurley

Georgetown University, Washington, Washington, D.C., United States

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Publications (286)778.41 Total impact

  • Bin Tu · Carly Masaberg · Jar How Lee · Daniel Behm · John Sells · Paul Tausch · Lihua Hou · Jennifer Ng · Carolyn Katovich Hurley ·

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    ABSTRACT: Natural killer (NK) cells are regulated killer immunoglobulin-like receptor (KIR) interactions with HLA class I ligands. Several models of NK reactivity have been associated with improved outcomes following myeloablative allogeneic hematopoietic cell transplantation (HCT), but this issue has not been rigorously addressed in reduced-intensity conditioning (RIC) unrelated donor (URD) HCT. We studied 909 patients undergoing RIC-URD HCT. Patients with acute myeloid leukemia (AML, n=612) lacking >1 KIR ligands experienced higher grade III-IV acute graft-vs.-host disease (GvHD) (HR 1.6, 95%CI 1.16-2.28, p=0.005) compared to those with all ligands present. Absence of HLA-C2 for donor KIR2DL1 was associated with higher grade II-IV (HR 1.4, p=0.002) and III-IV acute GvHD (HR 1.5, p=0.01) compared to HLA-C2+patients. AML patients with KIR2DS1+, HLA-C2 homozygous donors had greater treatment-related mortality compared to others (HR 2.4, 95%CI 1.4-4.2, p=0.002), but did not experience lower relapse. There were no significant associations with outcomes for AML when assessing donor activating KIRs or centromeric KIR content, nor for any donor-recipient KIR-HLA assessments in patients with myelodysplastic syndrome (n=297). KIR-HLA combinations in RIC-URD HCT recapitulate some but not all KIR-HLA effects observed in myeloablative HCT. Copyright © 2015 American Society for Blood and Marrow Transplantation. Published by Elsevier Inc. All rights reserved.
    Biology of blood and marrow transplantation: journal of the American Society for Blood and Marrow Transplantation 05/2015; 21(9). DOI:10.1016/j.bbmt.2015.05.002 · 3.40 Impact Factor
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    ABSTRACT: NK cells can enhance engraftment and mediate GVL following allogeneic HSCT, but the potency of GVL mediated by naturally reconstituting NK cells following HSCT is limited. Preclinical studies demonstrate that activation of NK cells using IL-15 plus 4-1BBL upregulates activating receptor expression and augments killing capacity. In an effort to amplify the beneficial effects of NK cells post-HSCT, we conducted a first-in-human trial of adoptive transfer of donor-derived IL-15/4-1BBL activated NK cells (aNK-DLI) following HLA-matched, T cell depleted (1-2 x 10(4) T cells/kg) non-myeloablative PBSCT in children and young adults with ultra-high risk solid tumors (Clinicaltrials.gov (NCT01287104)). Activated NK-DLI were CD3(+) depleted, CD56(+) selected lymphocytes, cultured for 9-11 days with rhIL-15 plus 4-1BBL(+)IL-15Rα(+)artificial APCs. aNK-DLI demonstrated potent killing capacity and displayed high levels of activating receptor expression. Five of 9 transplant recipients experienced acute GVHD following aNK-DLI, with Grade 4 GVHD observed in 3 subjects. GVHD was more common in matched unrelated donor vs matched sibling donor recipients, and was associated with higher donor CD3 chimerism. Given that the T cell dose was below the threshold required for GVHD in this setting, we conclude that aNK-DLI contributed to the acute GVHD observed, likely by augmenting underlying T cell alloreactivity. Copyright © 2014 American Society of Hematology.
    Blood 12/2014; 125(5). DOI:10.1182/blood-2014-07-592881 · 10.45 Impact Factor
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    ABSTRACT: We examined current outcomes of unrelated donor allogeneic hematopoietic cell transplantation (HCT) to determine the clinical implications of donor-recipient HLA matching. Adult and pediatric patients who had undergone first myeloablative unrelated bone marrow or peripheral blood HCT for AML, ALL, CML, or MDS between 1999 and 2011 were included. All had high resolution typing for HLA-A, -B, -C, -DRB1. Of the total (n=8,003), cases were 8/8 (n=5,449), 7/8 (n=2,071), or 6/8 (n=483) matched. HLA mismatch (6-7/8) conferred significantly increased risk for grade II-IV and III-IV acute graft vs. host disease (GVHD), chronic GVHD, transplant-related mortality (TRM), and overall mortality compared to HLA matched cases (8/8). Type (allele/antigen) and locus (HLA-A, -B, -C, -DRB1) of mismatch were not associated with overall mortality. Among 8/8 matched cases, -DPB1 and -DQB1 mismatch resulted in increased acute GVHD, and -DPB1 mismatch had decreased relapse. Non-permissive -DPB1 allele mismatch was associated with higher TRM compared to permissive -DPB1 mismatch or -DPB1 match, and increased overall mortality compared to permissive -DPB1 mismatch in 8/8 (and 10/10) matched cases. Full matching at HLA-A, -B, -C, -DRB1 is required for optimal unrelated donor HCT survival, and avoidance of non-permissive -DPB1 mismatches in otherwise HLA-matched pairs is indicated.
    Blood 08/2014; 124(16). DOI:10.1182/blood-2014-05-576041 · 10.45 Impact Factor

  • Biology of Blood and Marrow Transplantation 02/2014; 20(2):S25–S26. DOI:10.1016/j.bbmt.2013.12.008 · 3.40 Impact Factor
  • Noriko K Steiner · Sivanesan Dakshanamurthy · Nicholas Nguyen · Carolyn Katovich Hurley ·
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    ABSTRACT: Natural killer cell stimulatory receptor gene, KIR2DS5, is polymorphic. While KIR2DS5∗002 is most frequently observed, other alleles have also been found. The proteins encoded by these alleles (KIR2DS5∗002 - ∗009) are expressed at varying levels on the surface of NKL and Jurkat transfectants. Gel electrophoresis of all allelic products showed two isoforms which differ in the extent of maturation of N-linked glycosylation. These isoforms differed in intensity and molecular weight among the allelic products. Site-directed mutagenesis was used to identify polymorphic variation at residues 123 and 157 as key in altering glycosylation and levels of surface expression.
    Human immunology 11/2013; 75(2). DOI:10.1016/j.humimm.2013.11.012 · 2.14 Impact Factor
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    ABSTRACT: For more than two decades, international cooperation and information technology have been playing key roles in the identification of suitable unrelated donors and cord blood units for hematopoietic SCT. To ensure consistent coding and interpretation of HLA data among the linked computer systems, the World Marrow Donor Association has standardized the extensions of the World Health Organization (WHO) Nomenclature for factors of the HLA system applied in practice. The first version of this report published in 2007 has become the reference for the technical validation of HLA information on donors and patients in the context of search and matching and is used by registries of volunteer unrelated hematopoietic stem cell donors and umbilical cord blood banks throughout the world. The present update became necessary after the major revision of the WHO HLA nomenclature in April 2010. It now covers issues arising when alleles are withdrawn or renamed because of the continuous updating of the WHO HLA nomenclature. In addition, formal validation and interpretation rules for the so-called 'multiple allele codes' have been added.Bone Marrow Transplantation advance online publication, 1 July 2013; doi:10.1038/bmt.2013.93.
    Bone marrow transplantation 07/2013; 48(11). DOI:10.1038/bmt.2013.93 · 3.57 Impact Factor
  • Ana Lazaro · Bin Tu · Ruyan Yang · Yi Xiao · Kanthi Kariyawasam · Jennifer Ng · Carolyn Katovich Hurley ·
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    ABSTRACT: DNA sequencing is a powerful technique for identifying allelic variation within the human leukocyte antigen (HLA) genes. Sequencing is usually focused on the most polymorphic exons of the class I (HLA-A, -B, -C) and class II (HLA-DR, -DQ, and -DP) genes. These exons encode the antigen recognition site, the region of the HLA molecule that binds peptides and interacts with the T cell receptor for antigen and natural killer cell immunoglobulin-like receptors (KIR). Sanger sequencing of amplified DNA from each HLA gene from a preparation containing one or two alleles yields a sequence that is used to identify the alleles by comparison with a reference database.
    Methods in molecular biology (Clifton, N.J.) 06/2013; 1034:161-95. DOI:10.1007/978-1-62703-493-7_9 · 1.29 Impact Factor
  • Tiernan J Mulrooney · Phillip E Posch · Carolyn Katovich Hurley ·
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    ABSTRACT: KIR aid in the regulation of NK cell activity. In this study, the effect of the interaction between the KIR2DS and their adapter, DAP12, was investigated beyond the previously defined signaling function. Flow cytometry analysis showed enhanced KIR2DS surface expression on NKL cells when cotransfected with DAP12. Conversely, KIR2DS4 surface expression on primary cells was decreased when the cells were treated with DAP12-specific siRNA. Treatment of the KIR2DS and DAP12-transfected cells with CHX or BFA repressed KIR2DS surface expression, revealing a role for DAP12 in trafficking newly synthesized KIR to the cell surface. Immunoprecipitation of DAP12 revealed an interaction of DAP12 with an immature isoform of KIR2DS, indicating that the interaction likely initiates within the ER. An internalization assay demonstrated a significant impact of DAP12 on KIR2DS surface stability. Confocal microscopy showed that internalized KIR2DS molecules are recruited to lysosomal compartments independent of DAP12 expression. Our results suggest that in vivo conditions that adversely affect DAP12 expression will indirectly reduce surface expression and stability of KIR2DS. These effects could significantly impact ligand recognition and strength of signaling through KIR2DS molecules.
    Journal of leukocyte biology 05/2013; 94(2). DOI:10.1189/jlb.0213093 · 4.29 Impact Factor
  • William R Frazier · Noriko Steiner · Lihua Hou · Sivanesan Dakshanamurthy · Carolyn Katovich Hurley ·
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    ABSTRACT: Although extensive homology exists between their extracellular domains, NK cell inhibitory receptors killer Ig-like receptor (KIR) 2DL2*001 and KIR2DL3*001 have previously been shown to differ substantially in their HLA-C binding avidity. To explore the largely uncharacterized impact of allelic diversity, the most common KIR2DL2/3 allelic products in European American and African American populations were evaluated for surface expression and binding affinity to their HLA-C group 1 and 2 ligands. Although no significant differences in the degree of cell membrane localization were detected in a transfected human NKL cell line by flow cytometry, surface plasmon resonance and KIR binding to a panel of HLA allotypes demonstrated that KIR2DL3*005 differed significantly from other KIR2DL3 allelic products in its ability to bind HLA-C. The increased affinity and avidity of KIR2DL3*005 for its ligand was also demonstrated to have a larger impact on the inhibition of IFN-γ production by the human KHYG-1 NK cell line compared with KIR2DL3*001, a low-affinity allelic product. Site-directed mutagenesis established that the combination of arginine at residue 11 and glutamic acid at residue 35 in KIR2DL3*005 were critical to the observed phenotype. Although these residues are distal to the KIR/HLA-C interface, molecular modeling suggests that alteration in the interdomain hinge angle of KIR2DL3*005 toward that found in KIR2DL2*001, another strong receptor of the KIR2DL2/3 family, may be the cause of this increased affinity. The regain of inhibitory capacity by KIR2DL3*005 suggests that the rapidly evolving KIR locus may be responding to relatively recent selective pressures placed upon certain human populations.
    The Journal of Immunology 05/2013; 190(12). DOI:10.4049/jimmunol.1300464 · 4.92 Impact Factor
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    ABSTRACT: The impact of HLA homozygosity at mismatched (MM) loci on the outcome of 2,687 myeloablative unrelated donor hematopoietic cell transplantations performed for malignant disease was evaluated among four groups: 7/8 bidirectional MM transplants (donor and recipient heterozygous MM, n=1393), 7/8 host vs. graft (HVG) vector MM (recipient homozygous, n=112), 7/8 graft vs. host (GVH) vector MM (donor homozygous, n=119), and 8/8 matches (n=1063). Multivariate analyses found 7/8 GVH (p=0.001) and bidirectional MM groups (p<0.0001) had significantly worse transplant-related mortality, overall and disease-free survival than the 8/8 match group, a difference not observed with the 7/8 HVG MM group (p>0.01). The three 7/8 groups differed only for grades 3-4 acute GVHD where HVG MM had less GVHD than the 7/8 bidirectional MM (HR 0.52, p=0.0016) and GVH MM (HR 0.43, p=0.0009) but not the 8/8 group (HR 0.83, p=0.39). There were no differences between the 7/8 groups for relapse, chronic GVHD, neutrophil engraftment or graft failure. Unidirectional GVH vector mismatches have the same risk as 7/8 bidirectional mismatches. Recipients with a 7/8 HVG MM have a reduced risk of acute GVHD without an increased risk of disease relapse or graft failure compared to a 7/8 bi-directional MM at a heterozygous locus.
    Blood 05/2013; 121(23). DOI:10.1182/blood-2013-01-480343 · 10.45 Impact Factor
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    ABSTRACT: We have updated the catalogue of common and well-documented (CWD) human leukocyte antigen (HLA) alleles to reflect current understanding of the prevalence of specific allele sequences. The original CWD catalogue designated 721 alleles at the HLA-A, -B, -C, -DRB1, -DRB3/4/5, -DQA1, -DQB1, and -DPB1 loci in IMGT (IMmunoGeneTics)/HLA Database release 2.15.0 as being CWD. The updated CWD catalogue designates 1122 alleles at the HLA-A, -B, -C, -DRB1, -DRB3/4/5, -DQA1, -DQB1, -DPA1 and -DPB1 loci as being CWD, and represents 14.3% of the HLA alleles in IMGT/HLA Database release 3.9.0. In particular, we identified 415 of these alleles as being 'common' (having known frequencies) and 707 as being 'well-documented' on the basis of ~140,000 sequence-based typing observations and available HLA haplotype data. Using these allele prevalence data, we have also assigned CWD status to specific G and P designations. We identified 147/151 G groups and 290/415 P groups as being CWD. The CWD catalogue will be updated on a regular basis moving forward, and will incorporate changes to the IMGT/HLA Database as well as empirical data from the histocompatibility and immunogenetics community. This version 2.0.0 of the CWD catalogue is available online at cwd.immunogenomics.org, and will be integrated into the Allele Frequencies Net Database, the IMGT/HLA Database and National Marrow Donor Program's bioinformatics web pages.
    Tissue Antigens 04/2013; 81(4):194-203. DOI:10.1111/tan.12093 · 2.14 Impact Factor
  • B Tu · N Cha · R Yang · J Ng · C K Hurley ·
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    ABSTRACT: In order to reduce the time required to identify a match for unrelated donor hematopoietic stem cell transplantation, a one-step DNA sequencing strategy was employed at the time of recruitment. The impact of this strategy on human leukocyte antigen (HLA) typing resolution and the effect of current registry requirements on resolution and coding of assignments were evaluated. Sanger-based DNA sequencing was used to obtain diploid exons 2 and 3 HLA-A, -B and -C assignments of 2747 unrelated African American and 1822 European American volunteers at recruitment. The results demonstrate the high resolution of the approach and challenge several aspects of the current registry typing strategy. Of the 46% of African American and 74% of European American individuals whose HLA typing resulted in alternative genotypes, the majority (≥93%) was predicted to have only a single 'common' genotype among the alternatives. The common practice of adding secondary assays to resolve alternative genotype assignments that include more than two antigen groups was also evaluated. While the percentage of assignments with greater than two antigen groups reached as high as 21% (HLA-A in European Americans), only 1.8% of individuals at most carried two common genotypes encompassing three antigen groups. The assignment of (National Marrow Donor Program) NMDP-designated allele codes to the one-pass results reduced the resolution substantially and introduced genotypes that were not included in the laboratory's assignments. We suggest the alternative strategy of using the exons 2-3 diploid nucleotide sequence as the assignment submitted to the registry with the added benefit of immortalizing the assignment in time regardless of the introduction of novel alleles. To keep pace with current donor selection criteria and with the increasing number of new alleles, it is time to rethink our recruitment typing strategies.
    Tissue Antigens 03/2013; 81(3):150-60. DOI:10.1111/tan.12072 · 2.14 Impact Factor
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    ABSTRACT: There are over 24 million registered adult donors worldwide and the numbers of unrelated donor transplantations are increasing. The optimal strategy for prioritizing among comparably HLA-matched potential donors has not been established. Therefore, the objective of the current analyses was to study the association between donor characteristics (age, sex, parity, cytomegalovirus serostatus, HLA-match and blood group ABO match) and survival after transplantation for hematologic malignancy. The association of donor characteristics with transplantation outcomes was examined using either logistic or Cox regression models, adjusting for patient disease and transplantation characteristics associated with outcomes in two independent datasets, 1988-2006 (N=6349; training cohort) and 2007-2011 (N=4690; validation cohort). All donor-recipient pairs had allele-level HLA typing at HLA-A, -B, -C and -DRB1, the current standard for selecting donors. Results of multivariate analysis adjusting for patient disease and transplantation characteristics showed that survival was better after transplantation of grafts from young donors (aged 18 - 32 years) who were HLA-matched to recipients (p<0.001). These findings were validated for transplantations that occurred between 2007 and 2011. For every 10-year increment in donor age, there is a 5.5% increase in the hazard ratio for overall mortality. Increasing HLA disparity was also associated with worsening survival. Donor age and donor-recipient HLA-match are important when selecting adult unrelated donors. Other donor characteristics such as sex, parity and cytomegalovirus serostatus were not associated with survival. The effect of ABO matching on survival is modest and must be studied further before definitive recommendations can be offered.
    Biology of Blood and Marrow Transplantation 02/2013; 19(2):S146–S147. DOI:10.1016/j.bbmt.2012.11.095 · 3.40 Impact Factor
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    ABSTRACT: The goal of the immunogenomic data analysis working group (IDAWG) is to facilitate the consistent analysis of HLA and KIR data, and the sharing of those data among the immunogenomic and larger genomic communities. However, the data management approaches currently applied by immunogenomic researchers are not widely discussed or reported in the literature, and the effect of different approaches on data analyses is not known. With ASHI's support, the IDAWG developed a 45 question survey on HLA and KIR data generation, data management and data analysis practices. Survey questions detailed the loci genotyped, typing systems used, nomenclature versions reported, computer operating systems and software used to manage and transmit data, the approaches applied to resolve HLA ambiguity and the methods used for basic population-level analyses. Respondents were invited to demonstrate their HLA ambiguity resolution approaches in simulated data sets. By May 2012, 156 respondents from 35 nations had completed the survey. These survey respondents represent a broad sampling of the Immunogenomic community; 52% were European, 30% North American, 10% Asian, 4% South American and 4% from the Pacific. The project will continue in conjunction with the 17th Workshop, with the aim of developing community data sharing standards, ambiguity resolution documentation formats, single-task data Management tools and novel data analysis methods and applications. While additional project details and plans for the 17th IHIW will be forthcoming, we welcome the input and participation in these projects from the histocompatibility and immunogenetics community.
    International Journal of Immunogenetics 12/2012; 40(1). DOI:10.1111/iji.12026 · 1.25 Impact Factor
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    B Tu · N Leahy · R Yang · N Cha · K Kariyawasam · L Hou · Y Xiao · C Masaberg · D Pulse-Earle · M Maiers · J Ng · J Kurtzberg · C K Hurley ·
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    ABSTRACT: HLA-A, -B, -C, -DRB1, -DQB1 assignments were obtained for 374 pairs of African American mothers and their umbilical cord blood units (CBU) by DNA sequencing. An algorithm developed by the National Marrow Donor Program was used to assign 1122 haplotypes by segregation. Seventy percent of the haplotypes carried assignments at all five loci. In the remainder, alleles at various loci, most often DQB1 in 48% of the haplotypes with a missing assignment, could not be assigned due to sharing of both alleles by mother and CBU. There were 652 haplotypes carrying a unique combination of alleles at the five loci; the majority (74%) were singletons. Novel B∼C and DRB1∼DQB1 associations were observed. The results show the genetic diversity in this population and provide validation for a publically available tool for pedigree analysis. Our observations underscore the need for procurement of increased numbers of units in the national cord blood inventory in order to identify matching donors for all patients requiring hematopoietic stem cell transplantation.
    Tissue Antigens 11/2012; 81(1). DOI:10.1111/tan.12035 · 2.14 Impact Factor
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    ABSTRACT: The immune responses of natural killer cells are regulated, in part, by killer cell immunoglobulin-like receptors (KIR). The 16 closely-related genes in the KIR gene system have been diversified by gene duplication and unequal crossing over, thereby generating haplotypes with variation in gene copy number. Allelic variation also contributes to diversity within the complex. In this study, we estimated allele-level haplotype frequencies and pairwise linkage disequilibrium statistics for 14 KIR loci. The typing utilized multiple methodologies by four laboratories to provide at least 2x coverage for each allele. The computational methods generated maximum-likelihood estimates of allele-level haplotypes. Our results indicate the most extensive allele diversity was observed for the KIR framework genes and for the genes localized to the telomeric region of the KIR A haplotype. Particular alleles of the stimulatory loci appear to be nearly fixed on specific, common haplotypes while many of the less frequent alleles of the inhibitory loci appeared on multiple haplotypes, some with common haplotype structures. Haplotype structures cA01 and/or tA01 predominate in this cohort, as has been observed in most populations worldwide. Linkage disequilibrium is high within the centromeric and telomeric haplotype regions but not between them and is particularly strong between centromeric gene pairs KIR2DL5∼KIR2DS3S5 and KIR2DS3S5∼KIR2DL1, and telomeric KIR3DL1∼KIR2DS4. Although 93% of the individuals have unique pairs of full-length allelic haplotypes, large genomic blocks sharing specific sets of alleles are seen in the most frequent haplotypes. These high-resolution, high-quality haplotypes extend our basic knowledge of the KIR gene system and may be used to support clinical studies beyond single gene analysis.
    PLoS ONE 11/2012; 7(11):e47491. DOI:10.1371/journal.pone.0047491 · 3.23 Impact Factor
  • Carly Masaberg · Yi Xiao · Bin Tu · Kanthi Kariyawasam · Jennifer Ng · Carolyn Hurley ·
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    ABSTRACT: Aim A proposal (Hurley et al “A One-Pass DNA Sequencing Strategy at Recruitment of Hematopoietic Stem Cell Donors - Rethinking Typing Requirements”) to reduce time and cost by one-pass DNA sequencing may result in a small percentage of individuals with greater than 2 antigen groups. We have devised a method which utilizes the speed and flexibility of SSO to resolve these ambiguities. Methods Out of 2,746 donors typed by one-pass SBT, a small number (19 B locus and 21 C locus) had HLA assignments including more than two antigen groups. These donors were typed using One Lambda’s LABType HD HLA-B and HD HLA-C kits. The SSO results have been verified by group specific amplifications performed using SBT. Results Most of the B locus ambiguities were typed as B∗35:FVSH, 49:BAXH by one-pass SBT (12 of 19). These donors were resolved to B∗35:DNXN, 49:01 with 5 additional beads. The next most common B locus ambiguity, B∗35:HADV, 51:HAFE (4 of 19) was resolved to B∗35:DNXN, 52:01:02 with 10 additional beads. The other three ambiguities (B∗15:DNG, 35:FVSH; B∗44:GNJN, 51:GNJH; B∗35:01+/39:05, 38:FXTB) were seen once and were resolved with beads used in the HD kits. Most of the samples needing C locus ambiguity resolution were C∗05:NGV, 16:AB by one-pass SBT (19 of 21). Bead 63 in the OLI C locus kit resolved these samples as either C∗05:AC, 16:01 (95%) or C∗08:02, 16:02 (5%). The other C locus ambiguity (C∗04:GHCN, 05:HDAK) could only be resolved to two common genotypes by SSO (C∗04:01+, 08:04 or C∗04:04, 08:02) and had to be resolved by separating alleles by SBT. Conclusions In order to perfect this ambiguity resolution process we propose using biotinylated primers for the generic SBT amplification so that it could also be used for the SSO ambiguity resolution. Also, new probes specific for the known ambiguities would be created which would eliminate the need for secondary amplification. Whether the SSO was performed by automation or manually, the ambiguity resolution could be performed in less than 2 hours.

Publication Stats

7k Citations
778.41 Total Impact Points


  • 1988-2015
    • Georgetown University
      • • Department of Oncology
      • • Department of Microbiology and Immunology
      • • Department of Pediatrics
      • • Lombardi Cancer Center
      Washington, Washington, D.C., United States
    • CUNY Graduate Center
      New York, New York, United States
  • 2014
    • University of Toronto
      Toronto, Ontario, Canada
  • 2000-2011
    • National Marrow Donor Program
      Minneapolis, Minnesota, United States
  • 1995-2011
    • Washington DC VA Medical Center
      Washington, Washington, D.C., United States
  • 2005
    • George Washington University
      Washington, Washington, D.C., United States
  • 2001
    • Memorial Sloan-Kettering Cancer Center
      New York, New York, United States
  • 1996
    • Blood Systems Research Institute
      San Francisco, California, United States
  • 1991
    • Fred Hutchinson Cancer Research Center
      • Division of Clinical Research
      Seattle, Washington, United States
  • 1988-1989
    • American University Washington D.C.
      Washington, Washington, D.C., United States
  • 1987
    • Howard University Hospital
      Washington, Washington, D.C., United States