title: Allogeneic T Cells That Express an Anti-CD19 Chimeric Antigen Receptor Induce Remissions of B-Cell Malignancies That Progress After Allogeneic Hematopoietic Stem-Cell Transplantation Without Causing Graft-Versus-Host Disease.
abstract: OBJECTIVE
  Progressive malignancy is the leading cause of death after allogeneic hematopoietic stem-cell transplantation (alloHSCT). After alloHSCT, B-cell malignancies often are treated with unmanipulated donor lymphocyte infusions (DLIs) from the transplant donor. DLIs frequently are not effective at eradicating malignancy and often cause graft-versus-host disease, a potentially lethal immune response against normal recipient tissues.
  
  
  METHODS
  We conducted a clinical trial of allogeneic T cells genetically engineered to express a chimeric antigen receptor (CAR) targeting the B-cell antigen CD19. Patients with B-cell malignancies that had progressed after alloHSCT received a single infusion of CAR T cells. No chemotherapy or other therapies were administered. The T cells were obtained from each recipient's alloHSCT donor.
  
  
  RESULTS
  Eight of 20 treated patients obtained remission, which included six complete remissions (CRs) and two partial remissions. The response rate was highest for acute lymphoblastic leukemia, with four of five patients obtaining minimal residual disease-negative CR. Responses also occurred in chronic lymphocytic leukemia and lymphoma. The longest ongoing CR was more than 30 months in a patient with chronic lymphocytic leukemia. New-onset acute graft-versus-host disease after CAR T-cell infusion developed in none of the patients. Toxicities included fever, tachycardia, and hypotension. Peak blood CAR T-cell levels were higher in patients who obtained remissions than in those who did not. Programmed cell death protein-1 expression was significantly elevated on CAR T cells after infusion. Presence of blood B cells before CAR T-cell infusion was associated with higher postinfusion CAR T-cell levels.
  
  
  CONCLUSIONS
  Allogeneic anti-CD19 CAR T cells can effectively treat B-cell malignancies that progress after alloHSCT. The findings point toward a future when antigen-specific T-cell therapies will play a central role in alloHSCT.
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Jennifer N
authors.initials: JN
authors.lastname: Brudno
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Robert P T
authors.initials: RP
authors.lastname: Somerville
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Victoria
authors.initials: V
authors.lastname: Shi
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Jeremy J
authors.initials: JJ
authors.lastname: Rose
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: David C
authors.initials: DC
authors.lastname: Halverson
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Daniel H
authors.initials: DH
authors.lastname: Fowler
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Juan C
authors.initials: JC
authors.lastname: Gea-Banacloche
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Steven Z
authors.initials: SZ
authors.lastname: Pavletic
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Dennis D
authors.initials: DD
authors.lastname: Hickstein
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Tangying L
authors.initials: TL
authors.lastname: Lu
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Steven A
authors.initials: SA
authors.lastname: Feldman
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Alexander T
authors.initials: AT
authors.lastname: Iwamoto
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Roger
authors.initials: R
authors.lastname: Kurlander
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Irina
authors.initials: I
authors.lastname: Maric
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Andre
authors.initials: A
authors.lastname: Goy
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Brenna G
authors.initials: BG
authors.lastname: Hansen
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Jennifer S
authors.initials: JS
authors.lastname: Wilder
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Bazetta
authors.initials: B
authors.lastname: Blacklock-Schuver
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Frances T
authors.initials: FT
authors.lastname: Hakim
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Steven A
authors.initials: SA
authors.lastname: Rosenberg
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ.
authors.forename: Ronald E
authors.initials: RE
authors.lastname: Gress
authors.affiliation: Jennifer N. Brudno, Robert P.T. Somerville, Victoria Shi, Jeremy J. Rose, David C. Halverson, Daniel H. Fowler, Juan C. Gea-Banacloche, Steven Z. Pavletic, Dennis D. Hickstein, Tangying L. Lu, Steven A. Feldman, Alexander T. Iwamoto, Brenna G. Hansen, Bazetta Blacklock-Schuver, Frances T. Hakim, Steven A. Rosenberg, Ronald E. Gress, and James N. Kochenderfer, National Cancer Institute; Roger Kurlander and Irina Maric, National Institutes of Health, Bethesda; Jennifer S. Wilder, Frederick National Laboratory for Cancer Research, Frederick, MD; and Andre Goy, John Theurer Cancer Center at Hackensack University Medical Center, Hackensack, NJ. kochendj@mail.nih.gov.
authors.forename: James N
authors.initials: JN
authors.lastname: Kochenderfer
mesh_terms: D000328:Adult; D000368:Aged; D018941:Antigens, CD19 / Q000276:immunology*; D018450:Disease Progression; D005260:Female; D006086:Graft vs Host Disease / Q000209:etiology; D018380:Hematopoietic Stem Cell Transplantation / Q000009:adverse effects; D006801:Humans; D015448:Leukemia, B-Cell / Q000276:immunology / Q000601:surgery; D015451:Leukemia, Lymphocytic, Chronic, B-Cell / Q000276:immunology* / Q000601:surgery*; D008297:Male; D008875:Middle Aged; D011948:Receptors, Antigen, T-Cell / Q000378:metabolism*; D012074:Remission Induction; D013601:T-Lymphocytes / Q000276:immunology* / Q000637:transplantation*; D018183:Transplantation Chimera; D014184:Transplantation, Homologous
chemical_list: D018941:Antigens, CD19; D011948:Receptors, Antigen, T-Cell
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