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Cytomegalovirus Serostatus Affects Autoreactive NK Cells and Outcomes of IL2-Based Immunotherapy in Acute Myeloid Leukemia

Elin Bernson, Alexander Hallner, Frida E. Sander, Malin Nicklasson, Malin S. Nilsson, Karin Christenson, Ebru Aydin, Jan-Åke Liljeqvist, Mats Brune, Robin Foà, Johan Aurelius, Anna Martner, Kristoffer Hellstrand and Fredrik B. Thorén
Elin Bernson
1TIMM Laboratory, Sahlgrenska Cancer Center, University of Gothenburg, Gothenburg, Sweden.
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Alexander Hallner
1TIMM Laboratory, Sahlgrenska Cancer Center, University of Gothenburg, Gothenburg, Sweden.
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Frida E. Sander
1TIMM Laboratory, Sahlgrenska Cancer Center, University of Gothenburg, Gothenburg, Sweden.
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Malin Nicklasson
2Department of Infectious Diseases, University of Gothenburg, Gothenburg, Sweden.
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Malin S. Nilsson
1TIMM Laboratory, Sahlgrenska Cancer Center, University of Gothenburg, Gothenburg, Sweden.
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Karin Christenson
1TIMM Laboratory, Sahlgrenska Cancer Center, University of Gothenburg, Gothenburg, Sweden.
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Ebru Aydin
1TIMM Laboratory, Sahlgrenska Cancer Center, University of Gothenburg, Gothenburg, Sweden.
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Jan-Åke Liljeqvist
2Department of Infectious Diseases, University of Gothenburg, Gothenburg, Sweden.
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Mats Brune
3Department of Hematology, University of Gothenburg, Gothenburg, Sweden.
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Robin Foà
4Hematology, Department of Cellular Biotechnologies and Hematology, Sapienza University, Sapienza, Italy.
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Johan Aurelius
1TIMM Laboratory, Sahlgrenska Cancer Center, University of Gothenburg, Gothenburg, Sweden.
3Department of Hematology, University of Gothenburg, Gothenburg, Sweden.
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Anna Martner
1TIMM Laboratory, Sahlgrenska Cancer Center, University of Gothenburg, Gothenburg, Sweden.
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Kristoffer Hellstrand
1TIMM Laboratory, Sahlgrenska Cancer Center, University of Gothenburg, Gothenburg, Sweden.
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Fredrik B. Thorén
1TIMM Laboratory, Sahlgrenska Cancer Center, University of Gothenburg, Gothenburg, Sweden.
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  • For correspondence: fredrik.thoren@gu.se
DOI: 10.1158/2326-6066.CIR-17-0711 Published September 2018
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    Figure 1.

    NK cell differentiation status in CMV-seronegative or -seropositive AML patients receiving HDC/IL2 therapy. A and B, Frequency of NKG2C+ (A) or CD57+ (B) cells among CD56dim NKG2A− KIR+ NK cells during treatment. C, Pie charts show the fraction of NK cells from CMV− and CMV+ patients that fulfill the differentiation criteria CD16+56dim > NKG2A− > KIR+ > CD57+/− > NKG2C+/−, from samples collected before immunotherapy, n = 59. D, Box plots depict percentage (%) of KIR+CD57+NKG2C+ NK cells at C1D1 and C3D1 in CMV− and CMV+ patients. E, Box plots depict percentage (%) of NS-iKIR NK cells at onset (C1D1) and during HDC/IL2 therapy in CMV− and CMV+ patients. Mann–Whitney test; box plots show 10th to 90th percentiles.

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    Figure 2.

    Impact of CMV serostatus on clinical outcome. A and B, Leukemia-free (A) and overall (B) survival for AML patients in the Re:Mission trial that are CMV− or CMV+. C and D, Leukemia-free (C) and overall (D) survival for a historical control cohort of nontransplanted patients with AML.

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    Figure 3.

    Impact of a missing ligand genotype and CMV serostatus on outcome of AML patients receiving HDC/IL2. A and B, Leukemia-free (A) and overall (B) survival for patients with a “missing ligand” or “all iKIR ligands present” genotype, and that are either CMV+ (n = 33 and 23, respectively) or CMV− (n = 17 and 8, respectively). C and D, Leukemia-free (C) and overall (D) survival of patients with a missing iKIR ligand that are CMV− compared with all other patients (n = 17 and 64, respectively).

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    Figure 4.

    Degranulation responses in single KIR+ NK cells. A, Frequency of CD107a+ NS-iKIR or S-iKIR NK cells in degranulation assays toward Ab-coated Daudi cells (n = 10), K562 cells (n = 10), or primary AML blasts (n = 10 and n = 14 for unstimulated and IL2-stimulated, respectively). B, Frequency of CD107a+ NS-iKIR NK cells toward Ab-coated Daudi cells in CMV− (n = 6) and CMV+ donors (n = 7). C and D, Percentage of CD107a+ NS-iKIR NK cell response of total CD107a+ NK cell response toward Ab-coated Daudi cells (C) or primary AML blasts (D) in CMV− (n = 6; C, n = 5; D) and CMV+ donors (n = 7; C, n = 5; D).

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    Figure 5.

    Leukemia-free survival for AML patients receiving HDC/IL2 therapy with above or below median frequency of NS-iKIR NK cells before HDC/IL2 treatment start (C1D1; A, C) or at onset of third treatment cycle (C3D1; B, D), in patients who are CMV− (A, B) or CMV+ (C, D).

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  • Table 1.

    Univariable and multivariable analyses of the impact of CMV serostatus on LFS and OS

    Univariable analysisMultivariable analysis
    VariableHazard ratioConfidence intervalPHazard ratioConfidence intervalP
    CMV serostatus LFS0.410.19–0.890.020.460.21–1.010.05
    CMV serostatus OS0.260.08–0.870.030.280.08–0.960.04

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Cancer Immunology Research: 6 (9)
September 2018
Volume 6, Issue 9
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Cytomegalovirus Serostatus Affects Autoreactive NK Cells and Outcomes of IL2-Based Immunotherapy in Acute Myeloid Leukemia
Elin Bernson, Alexander Hallner, Frida E. Sander, Malin Nicklasson, Malin S. Nilsson, Karin Christenson, Ebru Aydin, Jan-Åke Liljeqvist, Mats Brune, Robin Foà, Johan Aurelius, Anna Martner, Kristoffer Hellstrand and Fredrik B. Thorén
Cancer Immunol Res September 1 2018 (6) (9) 1110-1119; DOI: 10.1158/2326-6066.CIR-17-0711

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Cytomegalovirus Serostatus Affects Autoreactive NK Cells and Outcomes of IL2-Based Immunotherapy in Acute Myeloid Leukemia
Elin Bernson, Alexander Hallner, Frida E. Sander, Malin Nicklasson, Malin S. Nilsson, Karin Christenson, Ebru Aydin, Jan-Åke Liljeqvist, Mats Brune, Robin Foà, Johan Aurelius, Anna Martner, Kristoffer Hellstrand and Fredrik B. Thorén
Cancer Immunol Res September 1 2018 (6) (9) 1110-1119; DOI: 10.1158/2326-6066.CIR-17-0711
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