Autoimmune amelogenesis imperfecta in patients with APS-1 and coeliac disease

Yael Gruper, Anette S. B. Wolff*, Liad Glanz, Frantisek Spoutil, Mihaela Cuida Marthinussen, Adriana Osickova, Yonatan Herzig, Yael Goldfarb, Goretti Aranaz-Novaliches, Jan Dobeš, Noam Kadouri, Osher Ben-Nun, Amit Binyamin, Bar Lavi, Tal Givony, Razi Khalaila, Tom Gome, Tomáš Wald, Blanka Mrazkova, Carmel SochenMarine Besnard, Shifra Ben-Dor, Ester Feldmesser, Elisaveta M. Orlova, Csaba Hegedűs, István Lampé, Tamás Papp, Szabolcs Felszeghy, Radislav Sedlacek, Esti Davidovich, Noa Tal, Dror S. Shouval, Raanan Shamir, Carole Guillonneau, Zsuzsa Szondy, Knut E. A. Lundin, Radim Osicka, Jan Prochazka, Eystein S. Husebye, Jakub Abramson*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

4 Citations (Scopus)

Abstract

Ameloblasts are specialized epithelial cells in the jaw that have an indispensable role in tooth enamel formation—amelogenesis1. Amelogenesis depends on multiple ameloblast-derived proteins that function as a scaffold for hydroxyapatite crystals. The loss of function of ameloblast-derived proteins results in a group of rare congenital disorders called amelogenesis imperfecta2. Defects in enamel formation are also found in patients with autoimmune polyglandular syndrome type-1 (APS-1), caused by AIRE deficiency3,4, and in patients diagnosed with coeliac disease5–7. However, the underlying mechanisms remain unclear. Here we show that the vast majority of patients with APS-1 and coeliac disease develop autoantibodies (mostly of the IgA isotype) against ameloblast-specific proteins, the expression of which is induced by AIRE in the thymus. This in turn results in a breakdown of central tolerance, and subsequent generation of corresponding autoantibodies that interfere with enamel formation. However, in coeliac disease, the generation of such autoantibodies seems to be driven by a breakdown of peripheral tolerance to intestinal antigens that are also expressed in enamel tissue. Both conditions are examples of a previously unidentified type of IgA-dependent autoimmune disorder that we collectively name autoimmune amelogenesis imperfecta.
Original languageEnglish
Pages (from-to)653-662
Number of pages10
JournalNature
Volume624
Issue number7992
Early online date22 Nov 2023
DOIs
Publication statusPublished - 21 Dec 2023

Bibliographical note

Research in the Abramson laboratory is supported by the European Research Council (ERC-2016-CoG-724821), the Bill and Marika Glied and Family Fund, the Israel Science Foundation (1819/21), the Binational Science Foundation (BSF) and the Joseph and Sarah Bollag Fund. J.A. is an incumbent of the Eugene and Marcia Applebaum Professorial Chair and of the IOCB fellowship for sabbatical visit program (RVO 61388963). Y. Gruper is supported by Ariane de Rothschild PhD fellowship. E.S.H. was supported by The Weston Visiting Professorship program at The Weizmann Institute of Science. Additional sources of support were provided by the Ministry of Education, Youth and Sports of the Czech Republic (MEYS CR) projects LM2023053 (to R.O.), LM2018126, LM2023036 and Upgrade of the Czech Centre for Phenogenomics CZ.02.1.01/0.0/0.0/16_013/0001789 and CZ.02.1.01/0.0/0.0/18_046/0015861 by MEYS and ESIF (to R. Sedlacek), Czech Science Foundation, GACR 19-19025Y (to J.P.); Czech Academy of Science, CAS RVO 6837805 0(toR.S.); and the KG Jebsen Center for Autoimmune Disorders and The Research Council of Norway and the Western Norway Health Authorities and the University of Bergen (to A.S.B.W. and E.S.H.); and the National Research, Development and Innovation Office, NKFI, Hungary (K138162) (to Z.S.). We thank the staff at the BIOCEV Imaging Methods Core Facility (supported by MEYS CR LM2018129 and ERDF CZ.02.1.01/0.0/0.0/18_046/0016045), the Center of Molecular Structure CMS-Biocev (supported by MEYS CR LM2018127) and S. Kozubová for technical help, and P. B. Juliusson at the University of Bergen for providing healthy control sera from children.

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