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Fcy receptor dependency of agonistic CD40 antibody in lymphoma therapy can be overcome through antibody multimerization

Fcy receptor dependency of agonistic CD40 antibody in lymphoma therapy can be overcome through antibody multimerization
Fcy receptor dependency of agonistic CD40 antibody in lymphoma therapy can be overcome through antibody multimerization
Immunomodulatory mAbs, led by the anti-CTLA4 mAb ipilimumab, are an exciting new class of drugs capable of promoting anticancer immunity and providing durable control of some tumors. Close analysis of a number of agents has revealed a critical yet variable role for Fc? receptors in their efficacy. In this article, we reveal that agonistic anti-CD40 mAbs have an absolute requirement for cross-linking by inhibitory Fc?RIIB when used systemically to treat established BCL1 syngeneic lymphoma, and therapy is lost when using a mouse IgG2a mAb not cross-linked by Fc?RIIB. Furthermore, in Fc?RIIB-deficient mice the lymphoma itself can provide Fc?RIIB to cross-link anti-CD40 on neighboring cells, and only when this is blocked does therapy fail. The dependence on Fc?RIIB for immunostimulatory activity was not absolute, however, because when anti-CD40 mAbs were administered systemically with the TLR3 agonist polyinosinic:polycytidylic acid or were given subcutaneously, activatory Fc?R could also provide cross-linking. Using this mechanistic insight, we designed multimeric forms of anti-CD40 mAb with intrinsic Fc?R-independent activity that were highly effective in the treatment of lymphoma-bearing mice. In conclusion, Fc?R-independent anti-CD40 activation is a viable strategy in vivo. These findings have important translational implications, as humans, unlike mice, do not have IgG that binds strongly to Fc?RIIB; therefore Fc?R-independent derivatives represent an attractive therapeutic option
0022-1767
1828-1835
White, Ann
b8c81272-e959-4acb-bbfe-1adc8a6c43f0
Dou, Lang
1e311f9c-adea-44be-a14a-9c8196eff7b8
Chan, Hak
b109c93f-7e9a-44ee-ad12-da757b1b11fc
Field, Vikki
b0c062ea-d836-4bea-9d46-44c414e11b6e
Mockridge, Christopher
327aef17-4837-4f2a-a93b-3d17cd1a7f9f
Booth, Steven
c2026d9d-ed93-4b1b-bce5-6b3efc8b8ca5
Williams, Emily
1a7a7b5b-7a4d-42b8-986c-b084c691be22
French, Ruth
a95ea7a1-7aeb-4c20-998e-fde663613fd1
Al-Shamkhani, Aymen
0a40b3ce-9d71-4d41-9369-7212f0a84504
Cragg, Mark
ec97f80e-f3c8-49b7-a960-20dff648b78c
Johnson, Peter
3f6068ce-171e-4c2c-aca9-dc9b6a37413f
Glennie, Martin
9f6f0eff-4560-48c2-80cd-0ec116110ded
Beers, Stephen
a02548be-3ffd-41ab-9db8-d6e8c3b499a2
Potter, Elizabeth
b39d99bd-6d7d-482f-89a2-640898171315
Butts, Cherie
bdefca5e-c9be-40e6-bc50-63ea5058ca16
Verbeek, J.S.
84596980-e9a7-4ef5-909c-43ea5349b065
Moss, Kane
1d61e208-64a5-49f6-8873-01526595a50f
White, Ann
b8c81272-e959-4acb-bbfe-1adc8a6c43f0
Dou, Lang
1e311f9c-adea-44be-a14a-9c8196eff7b8
Chan, Hak
b109c93f-7e9a-44ee-ad12-da757b1b11fc
Field, Vikki
b0c062ea-d836-4bea-9d46-44c414e11b6e
Mockridge, Christopher
327aef17-4837-4f2a-a93b-3d17cd1a7f9f
Booth, Steven
c2026d9d-ed93-4b1b-bce5-6b3efc8b8ca5
Williams, Emily
1a7a7b5b-7a4d-42b8-986c-b084c691be22
French, Ruth
a95ea7a1-7aeb-4c20-998e-fde663613fd1
Al-Shamkhani, Aymen
0a40b3ce-9d71-4d41-9369-7212f0a84504
Cragg, Mark
ec97f80e-f3c8-49b7-a960-20dff648b78c
Johnson, Peter
3f6068ce-171e-4c2c-aca9-dc9b6a37413f
Glennie, Martin
9f6f0eff-4560-48c2-80cd-0ec116110ded
Beers, Stephen
a02548be-3ffd-41ab-9db8-d6e8c3b499a2
Potter, Elizabeth
b39d99bd-6d7d-482f-89a2-640898171315
Butts, Cherie
bdefca5e-c9be-40e6-bc50-63ea5058ca16
Verbeek, J.S.
84596980-e9a7-4ef5-909c-43ea5349b065
Moss, Kane
1d61e208-64a5-49f6-8873-01526595a50f

White, Ann, Dou, Lang, Chan, Hak, Field, Vikki, Mockridge, Christopher, Booth, Steven, Williams, Emily, French, Ruth, Al-Shamkhani, Aymen, Cragg, Mark, Johnson, Peter, Glennie, Martin, Beers, Stephen, Potter, Elizabeth, Butts, Cherie, Verbeek, J.S. and Moss, Kane (2014) Fcy receptor dependency of agonistic CD40 antibody in lymphoma therapy can be overcome through antibody multimerization. Journal of Immunology, 193 (4), 1828-1835. (doi:10.4049/jimmunol.1303204). (PMID:25024386)

Record type: Article

Abstract

Immunomodulatory mAbs, led by the anti-CTLA4 mAb ipilimumab, are an exciting new class of drugs capable of promoting anticancer immunity and providing durable control of some tumors. Close analysis of a number of agents has revealed a critical yet variable role for Fc? receptors in their efficacy. In this article, we reveal that agonistic anti-CD40 mAbs have an absolute requirement for cross-linking by inhibitory Fc?RIIB when used systemically to treat established BCL1 syngeneic lymphoma, and therapy is lost when using a mouse IgG2a mAb not cross-linked by Fc?RIIB. Furthermore, in Fc?RIIB-deficient mice the lymphoma itself can provide Fc?RIIB to cross-link anti-CD40 on neighboring cells, and only when this is blocked does therapy fail. The dependence on Fc?RIIB for immunostimulatory activity was not absolute, however, because when anti-CD40 mAbs were administered systemically with the TLR3 agonist polyinosinic:polycytidylic acid or were given subcutaneously, activatory Fc?R could also provide cross-linking. Using this mechanistic insight, we designed multimeric forms of anti-CD40 mAb with intrinsic Fc?R-independent activity that were highly effective in the treatment of lymphoma-bearing mice. In conclusion, Fc?R-independent anti-CD40 activation is a viable strategy in vivo. These findings have important translational implications, as humans, unlike mice, do not have IgG that binds strongly to Fc?RIIB; therefore Fc?R-independent derivatives represent an attractive therapeutic option

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More information

e-pub ahead of print date: 14 July 2014
Published date: 14 July 2014
Organisations: Cancer Sciences

Identifiers

Local EPrints ID: 367278
URI: http://eprints.soton.ac.uk/id/eprint/367278
ISSN: 0022-1767
PURE UUID: 4bd061ec-ec3c-4182-a323-115dcb2cf591
ORCID for Hak Chan: ORCID iD orcid.org/0000-0003-0530-9480
ORCID for Aymen Al-Shamkhani: ORCID iD orcid.org/0000-0003-0727-4189
ORCID for Mark Cragg: ORCID iD orcid.org/0000-0003-2077-089X
ORCID for Peter Johnson: ORCID iD orcid.org/0000-0003-2306-4974
ORCID for Stephen Beers: ORCID iD orcid.org/0000-0002-3765-3342

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Date deposited: 19 Aug 2014 11:36
Last modified: 15 Mar 2024 03:08

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Contributors

Author: Ann White
Author: Lang Dou
Author: Hak Chan ORCID iD
Author: Vikki Field
Author: Christopher Mockridge
Author: Steven Booth
Author: Emily Williams
Author: Ruth French
Author: Mark Cragg ORCID iD
Author: Peter Johnson ORCID iD
Author: Martin Glennie
Author: Stephen Beers ORCID iD
Author: Elizabeth Potter
Author: Cherie Butts
Author: J.S. Verbeek
Author: Kane Moss

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