{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,2]],"date-time":"2026-11-02T13:31:08Z","timestamp":1793626268785,"version":"4.5.1"},"reference-count":35,"publisher":"Ovid Technologies (Wolters Kluwer Health)","funder":[{"name":"National Heart, Lung, and Blood Institute","award":["R01HL166608"],"award-info":[{"award-number":["R01HL166608"]}],"id":[{"id":"https:\/\/ror.org\/012pb6c26","id-type":"ROR","asserted-by":"crossref"}]},{"name":"National Institute of Nursing Research","award":["T32HL125232"],"award-info":[{"award-number":["T32HL125232"]}],"id":[{"id":"https:\/\/ror.org\/01y3zfr79","id-type":"ROR","asserted-by":"crossref"}]},{"name":"AHA Cardio-Oncology SFRN CAT-HD Center","award":["857078"],"award-info":[{"award-number":["857078"]}]},{"name":"AHA Cardio-Oncology SFRN CAT-HD Center","award":["857078"],"award-info":[{"award-number":["857078"]}]},{"name":"AHA Cardio-Oncology SFRN CAT-HD Center","award":["857078"],"award-info":[{"award-number":["857078"]}]},{"name":"AHA Cardio-Oncology SFRN CAT-HD Center","award":["857078"],"award-info":[{"award-number":["857078"]}]},{"name":"National Heart, Lung, and Blood Institute","award":["R01HL166608"],"award-info":[{"award-number":["R01HL166608"]}],"id":[{"id":"https:\/\/ror.org\/012pb6c26","id-type":"ROR","asserted-by":"crossref"}]},{"name":"Center of Cross Organ Vascular Pathology and by the Thrombosis and Hemostasis Affinity Research"}],"content-domain":{"domain":["lww.com","ovid.com"],"crossmark-restriction":true},"short-container-title":["JASN"],"abstract":"<jats:sec>\n                    <jats:title>Key Points<\/jats:title>\n                    <jats:p>\n                      <jats:list list-type=\"bullet\">\n                        <jats:list-item>\n                          <jats:p>Indoleamine 2,3-dioxygenase 1 is a central regulator of tryptophan metabolism and contributed to CKD-associated thromboinflammation and endothelial dysfunction.<\/jats:p>\n                        <\/jats:list-item>\n                        <jats:list-item>\n                          <jats:p>Indoxyl sulfate, a protein-bound uremic toxin, stabilized indoleamine 2,3-dioxygenase 1 by partially inhibiting its interaction with split-hand\/foot malformation 3 and reducing ubiquitination.<\/jats:p>\n                        <\/jats:list-item>\n                        <jats:list-item>\n                          <jats:p>Targeting indoleamine 2,3-dioxygenase 1 degradation by modulating split-hand\/foot malformation 3 may offer a novel therapeutic approach to mitigate CKD-associated arterial and venous thrombosis.<\/jats:p>\n                        <\/jats:list-item>\n                      <\/jats:list>\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>\n                      The uremic milieu of CKD is characterized by the accumulation of protein-bound uremic toxins, which contribute to thrombosis. Indoxyl sulfate, a\n                      <jats:italic toggle=\"yes\">bona fide<\/jats:italic>\n                      uremic toxin, upregulates indoleamine 2,3-dioxygenase 1 (IDO1), thereby augmenting kynurenine biogenesis. Both toxins activate tissue factor and thrombosis. Despite this pathogenic synergy, the mechanisms of indoxyl sulfate\u2013mediated IDO1 stabilization remain undefined.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>We employed targeted metabolomics, super-resolution microscopy, and gain- and loss-of-function experiments using nanoparticle-mediated gene delivery in mice to modulate split-hand\/foot malformation 3 (SHFM3) expression. This was followed by carotid artery or inferior vena cava thrombosis assays in indoxyl sulfate\u2013fed and adenine-induced CKD models.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>Among several F-box\u2013containing E3 ligases, SHFM3 downregulated IDO1 in endothelial cells. SHFM3 constitutively interacted with IDO1, which is partially disrupted by indoxyl sulfate\u2013induced nuclear sequestration of SHFM3 at concentrations corresponding to early-to-advanced CKD. SHFM3 interacted with the N-terminus of IDO1, ubiquitinated, and destabilized it. Indoxyl sulfate upregulated IDO1 activity, thereby increasing kynurenine biogenesis in N-terminus\u2013 and SHFM3-dependent manners. In an indoxyl sulfate\u2013fed mouse model, endothelial cell\u2013specific SHFM3 knockdown increased IDO1 and tissue factor while accelerating arterial thrombosis, and these effects were reversed by endothelial cell\u2013specific SHFM3 overexpression. CKD mice exhibited 55% higher venous thrombogenicity than controls. Endothelial cell\u2013specific SHFM3 overexpression significantly reversed these effects in control mice and, to a lesser extent, in CKD mice. Serum indoxyl sulfate levels significantly correlated with the global IDO1 activity and venous clot weights.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>SHFM3 functions as an indoxyl sulfate\u2013sensitive potent E3 ligase of IDO1, targeting it for degradation, even with partial interaction with IDO1 in the uremic milieu. This work also described a CKD-induced venous thrombosis model and supports the selective rewiring of uremic toxins in post-translational proteostasis, amplifying indoxyl sulfate\u2013mediated arterial and venous thrombosis.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1681\/asn.0000001203","type":"journal-article","created":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T16:00:21Z","timestamp":1787328021000},"update-policy":"https:\/\/doi.org\/10.1097\/lww.0000000000001000","source":"Crossref","is-referenced-by-count":0,"title":["Indoxyl Sulfate Promotes Uremic Arterial and Venous Thrombosis by Stabilizing Indoleamine 2,3-Dioxygenase 1 via the E3 Ligase Split-Hand\/Foot Malformation 3"],"prefix":"10.1681","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2452-5114","authenticated-orcid":false,"given":"Ricardo","family":"Almiron","sequence":"first","affiliation":[{"name":"Renal Section, Department of Medicine, Boston Medical Center, Boston University Chobanian and Avedisian School of Medicine, Boston, Massachusetts"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abbas Brahim","family":"Malloum","sequence":"additional","affiliation":[{"name":"Renal Section, Department of Medicine, Boston Medical Center, Boston University Chobanian and Avedisian School of Medicine, Boston, Massachusetts"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5560-2912","authenticated-orcid":false,"given":"Saran","family":"Lotfollahzadeh","sequence":"additional","affiliation":[{"name":"Renal Section, Department of Medicine, Boston Medical Center, Boston University Chobanian and Avedisian School of Medicine, Boston, Massachusetts"},{"name":"Department of Surgery, Boston University Chobanian and Avedisian School of Medicine, Boston, Massachusetts"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kashvi","family":"Sethuraman","sequence":"additional","affiliation":[{"name":"Renal Section, Department of Medicine, Boston Medical Center, Boston University Chobanian and Avedisian School of Medicine, Boston, Massachusetts"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5705-5470","authenticated-orcid":false,"given":"Arjun","family":"Sharma","sequence":"additional","affiliation":[{"name":"Renal Section, Department of Medicine, Boston Medical Center, Boston University Chobanian and Avedisian School of Medicine, Boston, Massachusetts"},{"name":"Division of Hemostasis and Thrombosis, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts"},{"name":"Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7432-6746","authenticated-orcid":false,"given":"Isaac","family":"Selinger","sequence":"additional","affiliation":[{"name":"Renal Section, Department of Medicine, Boston Medical Center, Boston University Chobanian and Avedisian School of Medicine, Boston, Massachusetts"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-0838-5913","authenticated-orcid":false,"given":"Anna","family":"Natrakul","sequence":"additional","affiliation":[{"name":"Renal Section, Department of Medicine, Boston Medical Center, Boston University Chobanian and Avedisian School of Medicine, Boston, Massachusetts"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-7431-6301","authenticated-orcid":false,"given":"Arjun","family":"Patel","sequence":"additional","affiliation":[{"name":"Renal Section, Department of Medicine, Boston Medical Center, Boston University Chobanian and Avedisian School of Medicine, Boston, Massachusetts"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-1074-9763","authenticated-orcid":false,"given":"David 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Lurie Children's Hospital of Chicago, Chicago, Illinois"},{"name":"Department of Pharmacology, Northwestern University Feinberg School of Medicine, Chicago, Illinois"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6745-1725","authenticated-orcid":false,"given":"Nader","family":"Rahimi","sequence":"additional","affiliation":[{"name":"Department of Pathology, Boston Medical Center, Boston University Chobanian and Avedisian School of Medicine, Boston, Massachusetts"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0041-0339","authenticated-orcid":false,"given":"You-Yang","family":"Zhao","sequence":"additional","affiliation":[{"name":"Injury Repair and Regeneration Research Section, Genetic Medicine and Nanotechnology Development Center, Stanley Manne Children's Research Institute, Ann and Robert H. 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