C3d-targeted complement inhibitors to correct complement dysregulation in aHUS patients

Atypical hemolytic uremic syndrome (aHUS) is a rare and severe thrombotic microangiopathy caused by genetic or acquired abnormalities leading to activation of the complement alternative pathway on cell surfaces. This process leads to endothelial dysfunction and microvascular thrombosis. The introduc...

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Main Authors: Valeria Guaschino, Donata Santarsiero, Sara Gastoldi, Joshua M. Thurman, V. Michael Holers, Shelia M. Violette, Fei Liu, Kelly C. Fahnoe, Chiara Guarinoni, Ariela Benigni, Giuseppe Remuzzi, Marina Noris, Sistiana Aiello
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-06-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2025.1620996/full
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author Valeria Guaschino
Donata Santarsiero
Sara Gastoldi
Joshua M. Thurman
V. Michael Holers
Shelia M. Violette
Fei Liu
Kelly C. Fahnoe
Chiara Guarinoni
Ariela Benigni
Giuseppe Remuzzi
Marina Noris
Sistiana Aiello
author_facet Valeria Guaschino
Donata Santarsiero
Sara Gastoldi
Joshua M. Thurman
V. Michael Holers
Shelia M. Violette
Fei Liu
Kelly C. Fahnoe
Chiara Guarinoni
Ariela Benigni
Giuseppe Remuzzi
Marina Noris
Sistiana Aiello
author_sort Valeria Guaschino
collection DOAJ
description Atypical hemolytic uremic syndrome (aHUS) is a rare and severe thrombotic microangiopathy caused by genetic or acquired abnormalities leading to activation of the complement alternative pathway on cell surfaces. This process leads to endothelial dysfunction and microvascular thrombosis. The introduction of anti-C5 antibodies has dramatically improved aHUS prognosis; however, these treatments require regular intravenous infusions and block systemic complement activity, exposing the patient to risk of infections. Recently complement inhibitors have been developed to selectively bind injury-associated target molecules, thereby concentrating the drug at specific cellular or tissue sites while preserving systemic complement function. This study evaluated the local complement inhibitory activity of new molecules that exploit the natural localization of C3d at complement activation sites on cells: namely the anti-C3d monoclonal antibody 3d8b conjugated with the first 10 or 17 short consensus repeats (SCRs) of complement receptor 1 (CR11–10 and CR11-17, respectively) or the first 5 SCRs of complement factor H (FH1-5). To this purpose we tested their capability to block C3 deposition and C5b-9 formation on microvascular endothelial cells (HMEC-1) exposed to serum from patients with aHUS. We also assessed their ability to prevent loss of anti-thrombogenic properties in HMEC-1 pre-exposed to aHUS serum and then perfused with control blood. We demonstrate that anti-C3d-antibody conjugated with CR11-10, or CR11-17, or FH1–5 effectively prevented aHUS serum-induced complement activation on HMEC-1, outperforming their non-targeted soluble counterparts. The efficacy of C3 convertase inhibition varied depending on the complement inhibitory component (CR11-17 > CR11-10 > FH1-5). However, all the inhibitors successfully blocked C5 convertase activity and eliminated the pro-thrombogenic effects of aHUS patients’ serum. These findings support the potential of tissue-targeted complement inhibition as a novel, non-systemic therapeutic strategy for aHUS and other diseases characterized by localized complement dysregulation.
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spelling doaj-art-94d03af5e6c44abcb187d7bc2572986b2025-08-20T02:08:02ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-06-011610.3389/fimmu.2025.16209961620996C3d-targeted complement inhibitors to correct complement dysregulation in aHUS patientsValeria Guaschino0Donata Santarsiero1Sara Gastoldi2Joshua M. Thurman3V. Michael Holers4Shelia M. Violette5Fei Liu6Kelly C. Fahnoe7Chiara Guarinoni8Ariela Benigni9Giuseppe Remuzzi10Marina Noris11Sistiana Aiello12Istituto di Ricerche Farmacologiche Mario Negri IRCCS, Clinical Research Center for Rare Diseases Aldo e Cele Daccò and Centro Anna Maria Astori, Science and Technology Park Kilometro Rosso, Bergamo, ItalyIstituto di Ricerche Farmacologiche Mario Negri IRCCS, Clinical Research Center for Rare Diseases Aldo e Cele Daccò and Centro Anna Maria Astori, Science and Technology Park Kilometro Rosso, Bergamo, ItalyIstituto di Ricerche Farmacologiche Mario Negri IRCCS, Clinical Research Center for Rare Diseases Aldo e Cele Daccò and Centro Anna Maria Astori, Science and Technology Park Kilometro Rosso, Bergamo, ItalyDepartment of Medicine, University of Colorado School of Medicine, Aurora, CO, United StatesDepartment of Medicine, University of Colorado School of Medicine, Aurora, CO, United StatesPreclinical Research, Q32 Bio Inc., Waltham, MA, United StatesPreclinical Research, Q32 Bio Inc., Waltham, MA, United StatesPreclinical Research, Q32 Bio Inc., Waltham, MA, United StatesIstituto di Ricerche Farmacologiche Mario Negri IRCCS, Clinical Research Center for Rare Diseases Aldo e Cele Daccò and Centro Anna Maria Astori, Science and Technology Park Kilometro Rosso, Bergamo, ItalyIstituto di Ricerche Farmacologiche Mario Negri IRCCS, Clinical Research Center for Rare Diseases Aldo e Cele Daccò and Centro Anna Maria Astori, Science and Technology Park Kilometro Rosso, Bergamo, ItalyIstituto di Ricerche Farmacologiche Mario Negri IRCCS, Clinical Research Center for Rare Diseases Aldo e Cele Daccò and Centro Anna Maria Astori, Science and Technology Park Kilometro Rosso, Bergamo, ItalyIstituto di Ricerche Farmacologiche Mario Negri IRCCS, Clinical Research Center for Rare Diseases Aldo e Cele Daccò and Centro Anna Maria Astori, Science and Technology Park Kilometro Rosso, Bergamo, ItalyIstituto di Ricerche Farmacologiche Mario Negri IRCCS, Clinical Research Center for Rare Diseases Aldo e Cele Daccò and Centro Anna Maria Astori, Science and Technology Park Kilometro Rosso, Bergamo, ItalyAtypical hemolytic uremic syndrome (aHUS) is a rare and severe thrombotic microangiopathy caused by genetic or acquired abnormalities leading to activation of the complement alternative pathway on cell surfaces. This process leads to endothelial dysfunction and microvascular thrombosis. The introduction of anti-C5 antibodies has dramatically improved aHUS prognosis; however, these treatments require regular intravenous infusions and block systemic complement activity, exposing the patient to risk of infections. Recently complement inhibitors have been developed to selectively bind injury-associated target molecules, thereby concentrating the drug at specific cellular or tissue sites while preserving systemic complement function. This study evaluated the local complement inhibitory activity of new molecules that exploit the natural localization of C3d at complement activation sites on cells: namely the anti-C3d monoclonal antibody 3d8b conjugated with the first 10 or 17 short consensus repeats (SCRs) of complement receptor 1 (CR11–10 and CR11-17, respectively) or the first 5 SCRs of complement factor H (FH1-5). To this purpose we tested their capability to block C3 deposition and C5b-9 formation on microvascular endothelial cells (HMEC-1) exposed to serum from patients with aHUS. We also assessed their ability to prevent loss of anti-thrombogenic properties in HMEC-1 pre-exposed to aHUS serum and then perfused with control blood. We demonstrate that anti-C3d-antibody conjugated with CR11-10, or CR11-17, or FH1–5 effectively prevented aHUS serum-induced complement activation on HMEC-1, outperforming their non-targeted soluble counterparts. The efficacy of C3 convertase inhibition varied depending on the complement inhibitory component (CR11-17 > CR11-10 > FH1-5). However, all the inhibitors successfully blocked C5 convertase activity and eliminated the pro-thrombogenic effects of aHUS patients’ serum. These findings support the potential of tissue-targeted complement inhibition as a novel, non-systemic therapeutic strategy for aHUS and other diseases characterized by localized complement dysregulation.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1620996/fullcomplement systemcomplement inhibitorsaHUSendothelial cell (EC)thrombus formation
spellingShingle Valeria Guaschino
Donata Santarsiero
Sara Gastoldi
Joshua M. Thurman
V. Michael Holers
Shelia M. Violette
Fei Liu
Kelly C. Fahnoe
Chiara Guarinoni
Ariela Benigni
Giuseppe Remuzzi
Marina Noris
Sistiana Aiello
C3d-targeted complement inhibitors to correct complement dysregulation in aHUS patients
Frontiers in Immunology
complement system
complement inhibitors
aHUS
endothelial cell (EC)
thrombus formation
title C3d-targeted complement inhibitors to correct complement dysregulation in aHUS patients
title_full C3d-targeted complement inhibitors to correct complement dysregulation in aHUS patients
title_fullStr C3d-targeted complement inhibitors to correct complement dysregulation in aHUS patients
title_full_unstemmed C3d-targeted complement inhibitors to correct complement dysregulation in aHUS patients
title_short C3d-targeted complement inhibitors to correct complement dysregulation in aHUS patients
title_sort c3d targeted complement inhibitors to correct complement dysregulation in ahus patients
topic complement system
complement inhibitors
aHUS
endothelial cell (EC)
thrombus formation
url https://www.frontiersin.org/articles/10.3389/fimmu.2025.1620996/full
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