{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,11]],"date-time":"2026-08-11T06:27:53Z","timestamp":1786429673953,"version":"build-2736575974"},"reference-count":285,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,8,11]],"date-time":"2026-08-11T00:00:00Z","timestamp":1786406400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"abstract":"\n Introduction<\/jats:title>\n Chronic inflammation has long been associated with cancer initiation, yet the mechanisms linking sustained immune activation to an immune-permissive tumor microenvironment remain incompletely defined. Prevailing explanations such as immune exhaustion (IEX) or free radical mediated tissue damage, fail to account for the active state of immune tolerance, a process driven by potent negative feedback loops that systematically suppress host effector responses.<\/jats:p>\n <\/jats:sec>\n \n Methods<\/jats:title>\n \n To address this gap, we developed an\n in vitro<\/jats:italic>\n model of macrophage tolerance driven by sustained Toll-like receptor 4 (TLR4) activation using microbial-associated molecular patterns (MAMPs). This system captures the full kinetic progression of the immune response, tracking macrophages from a resting baseline, through acute activation at 24 hours, to a chronic tolerant endpoint at 7\u201311 days. Methodologically, cells were maintained under a continuous media exchange (+\/\u2212\n E. coli<\/jats:italic>\n O111:B4 LPS) featuring high glucose and an elevated volume-to-cell ratio. This setup effectively eliminates autocrine interference and toxic byproducts, successfully isolating the direct consequences of sustained TLR4 signaling across extended durations.\n <\/jats:p>\n <\/jats:sec>\n \n Results<\/jats:title>\n Whole-transcriptome sequencing, validated by RT-PCR and select protein immunoblots, revealed that both \u201cexhaustion\u201d and \u201ctolerance\u201d are mischaracterized. Rather than a passive exhaustion state or a simple trajectory of diminishing returns, the resting-acute-chronic continuum drives a potent, active negative-feedback mechanism across an eight-phase bidirectional trajectory. By days 7\u201311, macrophages shifted to a TAM-like signature, overexpressing immune checkpoints (PD-L1\/MSN, TIM-3, SPP1, CD73, CD44, LILRs) and regulatory suppressive networks (SOCS\/JAK\/STAT, IL-10, CCL2\/7\/12, CXCL2), while downregulating classical (H2-D1\/K1) and non-classical (H2-Q\/T) MHC-I antigen-presenting genes. These alterations coincided with the profound loss of interferon-stimulated genes (ISGs) including the IFIT family, Ly6e, Irf7, Rsad2\/Viperin, and the Oas gene family, fundamentally crippling the machinery required for antiviral and antitumor immune surveillance. Moreover, this chronic stage drove the upregulation of degradative proteases (cathepsins, Adam8, S100a8, Klk9, carboxypeptidase D), integrins\/adhesion molecules (Itga5, Marcks, Msr1\/CD204, Alcam), iron-storage transcripts, lipid translocases (Cd36), and fatty acid-binding proteins. Concurrently, macrophages upregulated Nos2\/Cox2 alongside the metabolic collapse of mitochondrial OXPHOS genes and Acod1 (itaconate). Uniquely, this negative feedback loop coincided with a sustained, massive surge in a cluster of poorly characterized small proline-rich proteins (SPRRs), specifically Sprr2b, 2e, 2d, 2f, 2g, 2h, 2i, 2j, and 2k.<\/jats:p>\n <\/jats:sec>\n \n Discussion<\/jats:title>\n \n Overall, these results indicate that chronic inflammatory signaling can ultimately trigger a profound coordinated negative-feedback program consistent with a reduced immune recognition and defense pathway signatures. Ultimately, this study provides a reproducible\n in vitro<\/jats:italic>\n macrophage model to investigate immune suppression. It offers deeper insights into how chronic inflammation impairs host defenses against viral and tumor cells.\n <\/jats:p>\n <\/jats:sec>","DOI":"10.3389\/fimmu.2026.1729108","type":"journal-article","created":{"date-parts":[[2026,8,11]],"date-time":"2026-08-11T05:35:39Z","timestamp":1786426539000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["The cost of persistent alarm: temporal transcriptional reprogramming of macrophages from acute activation to chronic immune suppression by day 11"],"prefix":"10.3389","volume":"17","author":[{"given":"Elizabeth A.","family":"Mazzio","sequence":"first","affiliation":[{"name":"Florida Agricultural and Mechanical University, College of Pharmacy and Pharmaceutical Sciences","place":["Tallahassee, FL, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew S.","family":"Barnes","sequence":"additional","affiliation":[{"name":"Florida Agricultural and Mechanical University, College of Pharmacy and Pharmaceutical Sciences","place":["Tallahassee, FL, United States"]},{"name":"Neuro-Infectious Disease Program, Mt. Sinai Icahn School of Medicine","place":["New York, NY, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ramesh B.","family":"Badisa","sequence":"additional","affiliation":[{"name":"Florida Agricultural and Mechanical University, College of Pharmacy and Pharmaceutical Sciences","place":["Tallahassee, FL, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Selina F.","family":"Darling-Reed","sequence":"additional","affiliation":[{"name":"Florida Agricultural and Mechanical University, College of Pharmacy and Pharmaceutical Sciences","place":["Tallahassee, FL, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karam F. 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