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STIM1 and STIM2 Protein Deficiency in T Lymphocytes Underlies

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STIM1 and STIM2 Protein Deficiency in T Lymphocytes Underlies Correction IMMUNOLOGY Correction for “STIM1 and STIM2 protein deficiency in T lym- phocytes underlies development of the exocrine gland autoim- mune disease, Sjögren’ssyndrome,” by Kwong Tai Cheng, Ilias Alevizos, Xibao Liu, Wiliam D. Swaim, Hongen Yin, Stefan Feske, Masatsugu Oh-hora, and Indu S. Ambudkar, which appeared in issue 36, September 4, 2012, of Proc Natl Acad Sci USA (109: 14544–14549; first published August 17, 2012; 10.1073/pnas. 1207354109). The authors note that, due to a printer’s error, the statement in the Acknowledgments, “we thank the Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Development, for continued support and funding” should instead appear as “we thank the Division of Intramural Research, National Institute of Dental and Craniofacial Re- search, for continued support and funding.” www.pnas.org/cgi/doi/10.1073/pnas.1217344109 CORRECTION www.pnas.org PNAS | November 6, 2012 | vol. 109 | no. 45 | 18625 Downloaded by guest on September 27, 2021 STIM1 and STIM2 protein deficiency in T lymphocytes underlies development of the exocrine gland autoimmune disease, Sjögren’s syndrome Kwong Tai Chenga, Ilias Alevizosb, Xibao Liua, Wiliam D. Swaima, Hongen Yinc, Stefan Fesked, Masatsugu Oh-horae,f,g, and Indu S. Ambudkara,1 aSecretory Physiology Section, bSjögren’s Syndrome Clinic, and cAAV Biology Unit, Molecular Physiology and Therapeutic Branch, National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, MD 20892; dDepartment of Pathology, New York University Langone Medical Center, New York, NY 10016; eGlobal Center of Excellence Program, International Research Center for Molecular Science in Tooth and Bone Diseases and fDepartment of Cell Signaling, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo 113-8549, Japan; and gJapan Science and Technology Agency (JST), Precursory Research for Embryonic Science and Technology (PRESTO) program, Tokyo 113-8549, Japan Edited by Michael D. Cahalan, University of California, Irvine, CA, and approved July 16, 2012 (received for review May 1, 2012) Primary Sjögren’s Syndrome (pSS) is an autoimmune disease in- of STIM1 and STIM2, SOCE and SOCE-dependent cytokine volving salivary and other exocrine glands that leads to progres- production were severely attenuated, along with a substantial sive lymphocytic infiltration into the gland, tissue damage, and decrease in the number and function of regulatory T cells (Tregs) secretory defects. The mechanism underlying this disease remains (12). These mice displayed signs of autoimmunity, including poorly understood. Here we report that mice with T-cell–targeted dermatitis, blepharitis, and lymphoproliferation, with significant deletion of Stromal Interaction Molecule (STIM) 1 and STIM2 [dou- splenomegaly and infiltration of lymphocytes into epithelial tis- ble-knockout (DKO)] mice develop spontaneous and severe pSS- sues, such as liver and lungs. like autoimmune disease, displaying major hallmarks of the disease. Primary Sjögren’s Syndrome (pSS) is a chronic autoimmune In DKO mice, diffuse lymphocytic infiltration was seen in sub- disease affecting exocrine glands, primarily salivary and lacrimal mandibular glands, a major target of pSS, by age 6 wk, progressing glands, resulting in gland destruction, xerostomia (dry mouth), to severe inflammation by age 12 wk. Sjögren’s syndrome-specific and keratoconjunctivitis sicca (dry eyes) (13). Extraglandular IMMUNOLOGY autoantibodies (SSA/Ro and SSB/La) were detected in the serum, manifestations such as arthritis, fatigue, and vasculitis, and an and progressive salivary gland destruction and loss of fluid secre- elevated incidence of non-Hodgkin lymphoma have been re- tion were also seen. Importantly, we report that peripheral blood ported as well (14). The current criteria for diagnosis of pSS mononuclear cells as well as lymphocytic infiltrates in submandib- include subjective and objective signs of dry mouth and/or dry ular glands from patients with pSS demonstrated significant reduc- eyes, the presence of anti-Ro/anti-La autoantibodies, and his- tions in STIM1 and STIM2 proteins. Store-operated calcium entry tological evaluation of leukocyte infiltration in the minor salivary was also reduced in peripheral blood mononuclear cells from pSS gland (MSG); the number of foci of infiltrate in a given area of patients compared with those from healthy controls. Thus, deficiency – 2+ tissue is graded as 0 12. Although many studies suggest a role for of STIM1 and STIM2 proteins in T cells, and consequent defects in Ca viral infections as well as various extrinsic factors as potential signaling, are associated with salivary gland autoimmunopathy in triggers, there are no conclusive data establishing the molecular DKO mice and pSS patients. These data reveal a previously unre- basis for the disease (15, 16). The late disease onset and the ported link between STIM1 and STIM2 proteins and pSS. diverse genetic background of affected individuals complicate study of the disease mechanism and pathogenesis. Although immunology | knockout mice | Orai1 | rheumatology several mouse models display a pSS-like phenotype (17–21), no single model can perfectly match the full spectrum of pSS ob- tore-operated calcium entry (SOCE) is activated in response served in humans. Sto agonist-stimulated depletion of the endoplasmic reticulum Based on the autoimmune phenotype of the STIM1 and Ca2+ store and provides critical cytosolic Ca2+ signals that de- STIM2 double-knockout (DKO) mice and the generation of termine the regulation of diverse cellular functions (1). In T lym- pSS-like disease in several mouse models with decreased Treg phocytes, SOCE is mediated by calcium release-activated cal- function (19–24), we assessed a possible link between STIM1 and cium (CRAC) channels and regulates T-cell activation and STIM2 deficiency in T cells and autoimmunopathy of the salivary function, as well as long-term responses such as gene expression glands. Here we report that DKO mice display spontaneous and (2–5). Two key components of CRAC channels are stromal in- progressive submandibular gland inflammation (within 3 mo), teraction molecule (STIM) 1, STIM2, Orai1, Orai2, and Orai3. comparable to that seen in pSS patients with severe salivary STIM1 is the primary regulator of SOCE that senses endoplas- gland damage. The mice display all of the major hallmarks of mic reticulum [Ca2+] and triggers channel activation on store pSS: damaged salivary glands, loss of stimulated fluid secretion, depletion (6, 7). STIM2 is considered a relatively poor activator and elevated pSS-specific autoantibodies. More importantly, we of SOCE, although it has not yet been fully characterized (5, 8). report that peripheral blood mononuclear cells (PBMCs) from Orai1, the pore-forming subunit of CRAC channels (9), is the critical component for SOCE in T lymphocytes and other cell types (2, 3, 8, 10). Author contributions: K.T.C., I.A., X.L., W.D.S., H.Y., S.F., M.O., and I.S.A. designed re- In humans, disruption of SOCE has major immunologic con- search; K.T.C., I.A., X.L., W.D.S., H.Y., and M.O. performed research; K.T.C., I.A., X.L., W.D.S., H.Y., S.F., M.O., and I.S.A. contributed new reagents/analytic tools; K.T.C., I.A., sequences. Although complete loss of Orai1 function results in the X.L., W.D.S., S.F., M.O., and I.S.A. analyzed data; and K.T.C., X.L., and I.S.A. wrote severe combined immune deficiency (SCID) phenotype, patients the paper. with mutations in STIM1 display autoimmunity and lymphopro- The authors declare no conflict of interest. liferation (11). The consequences of STIM2 defects in patients This article is a PNAS Direct Submission. 2+ have not yet been reported. Thus, Orai-STIM–dependent Ca 1To whom correspondence should be addressed. E-mail: [email protected]. signaling has a dominant role in the maintenance of immune This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. balance. In a mouse model with T-lymphocyte–targeted deletion 1073/pnas.1207354109/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1207354109 PNAS Early Edition | 1of6 pSS patients exhibit decreased levels of STIM1 and STIM2 proteins, as well as diminished SOCE. Taken together, these findings suggest that STIM1 and STIM2 deficiencies in T cells, and the consequent aberrations in T cell function, underlies the onset and progression of salivary gland autoimmunopathy in Sjögren’s syndrome. Results Reduction of Salivary Gland Function in DKO Mice. Saliva secretion was induced by treatment of DKO and control (CTRL) mice with the muscarinic receptor agonist pilocarpine. Litter-matched mice were used in all of the experiments. At 6 wk after birth, Fig. 2. Detection of pSS-associated autoantibodies in serum. Serum samples pilocarpine-stimulated saliva was 11.10 ± 1.13 μL/20 min/g body ± μ were collected from CTRL and DKO mice, and autoantibody levels were weight in CTRL mice and 7.40 1.80 L/20 min/g body weight measured as described in SI Materials and Methods using samples collected in DKO mice, demonstrating a 33.33% reduction in salivary flow at 12 wk and compared between CTRL mice (black) and DKO mice (red). A C in the latter (Fig. 1 and ). By 12 wk, DKO mice exhibited a Antibody levels for SSA/Ro (CTRL, 1.71 ± 0.80 OD450/540 vs. DKO, 3.89 ± 0.20 ± ± striking 56% reduction in saliva secretion compared with CTRL OD450/540)(A) and SSB/La (CTRL, 1.49 0.80 ng/mL vs. 33.03 1.53 ng/mL) (B) mice (5.14 ± 1.81 μL/20 min/g body weight vs. 11.76 ± 1.38 μL/20 are shown. Data are mean ± SD. Significant differences are shown; **P < min/g body weight; P < 0.01) (Fig. 1 B and C). 0.01, unpaired Student t test. Elevation of pSS-Specific Autoantibodies in DKO Mice. Sjögren’s ’ diffuse infiltrates.
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