{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T06:06:53Z","timestamp":1784700413979,"version":"3.55.0"},"reference-count":219,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T00:00:00Z","timestamp":1784678400000},"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":"<jats:p>\n                    Bone is one of the most common sites of distant metastasis in solid tumors, particularly breast cancer, prostate cancer, and lung cancer. Bone metastatic lesions frequently exhibit persistent resistance to multiple systemic therapies, including chemotherapy, targeted therapy, endocrine therapy, and immune checkpoint inhibitors (ICIs). Accumulating evidence suggests that metabolic reprogramming within the bone microenvironment contributes to this resistance, yet the upstream mechanisms remain incompletely understood. Intercellular mitochondrial transfer has emerged as a potential link between the bone marrow niche and tumor metabolic adaptation. Bone marrow mesenchymal stem cells (BMSCs) have been reported to deliver functional mitochondria to tumor cells through tunneling nanotubes (TNTs), extracellular vesicles (EVs), and gap junctions, a process proposed to be regulated by metabolic stress, chemokine signaling (CXCL12\/CXCR4), and inflammatory cues. The bone marrow microenvironment\u2014characterized by hypoxia, high cell density, and lipid abundance\u2014together with the intrinsic transfer capacity of BMSCs, may facilitate efficient mitochondrial delivery. Following transfer, exogenous mitochondria have been shown, largely\n                    <jats:italic>in vitro<\/jats:italic>\n                    and preclinical models, to restore oxidative phosphorylation (OXPHOS) through respiratory chain reassembly, mitochondrial DNA (mtDNA) replication, and membrane potential recovery, which may drive a metabolic shift from the Warburg phenotype toward a mixed state with enhanced fatty acid \u03b2-oxidation (FAO), glutaminolysis, and branched-chain amino acid oxidation. The resulting high adenosine triphosphate (ATP) pool and reshaped redox homeostasis have been proposed to support multiple resistance mechanisms, including ATP-dependent drug efflux, enhanced DNA damage repair, apoptosis resistance, metabolic bypass of targeted therapies, immunosuppressive nutrient competition, and cancer stem cell (CSC) maintenance with therapy-induced dormancy. Mitochondrial dynamics remodeling and metabolic\u2013epigenetic crosstalk may further establish a \u201cmetabolic memory\u201d sustaining the resistant phenotype. Notably, transfer patterns appear to exhibit tumor type specificity across breast cancer, prostate cancer, and lung cancer, with multiple myeloma (MM) considered here as a mechanistically informative, marrow-resident comparator rather than a parallel solid-tumor setting. Conceptually proposed therapeutic strategies targeting this axis encompass transfer blockade, OXPHOS and FAO inhibition, and bone-targeted nanodelivery systems, none of which has yet demonstrated efficacy specifically against mitochondrial transfer in patients with bone metastasis. Importantly, several controversies remain unresolved, including the durability and functional integrity of transferred mitochondria, the risk of dye-tracing artifacts,\n                    <jats:italic>in vivo<\/jats:italic>\n                    detection sensitivity, and the clinical translation of pathway-specific inhibitors. This review systematically examines the reported molecular mechanisms of mitochondrial transfer between BMSCs and tumor cells, its proposed role in OXPHOS reprogramming and drug resistance in bone metastasis, and emerging therapeutic strategies, aiming to provide a critical framework for developing metabolism-targeted interventions to overcome bone metastatic resistance.\n                  <\/jats:p>","DOI":"10.3389\/fimmu.2026.1863593","type":"journal-article","created":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T05:54:12Z","timestamp":1784699652000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Mitochondrial transfer-mediated metabolic reprogramming and drug resistance in bone metastasis: mechanisms and therapeutic strategies"],"prefix":"10.3389","volume":"17","author":[{"given":"Wei","family":"Deng","sequence":"first","affiliation":[{"name":"The First Affiliated Hospital of Guangzhou University of Chinese Medicine","place":["Guangzhou, China"]},{"name":"The Laboratory of Orthopaedics and Traumatology of Lingnan Medical Research Center, Guangzhou University of Chinese Medicine","place":["Guangzhou, China"]},{"name":"Guangzhou University of Chinese Medicine","place":["Guangdong, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bingyu","family":"Liu","sequence":"additional","affiliation":[{"name":"The First Affiliated Hospital of Guangzhou University of Chinese Medicine","place":["Guangzhou, China"]},{"name":"The Laboratory of Orthopaedics and Traumatology of Lingnan Medical Research Center, Guangzhou University of Chinese Medicine","place":["Guangzhou, China"]},{"name":"Guangzhou University of Chinese Medicine","place":["Guangdong, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Songtao","family":"Xiang","sequence":"additional","affiliation":[{"name":"The First Affiliated Hospital of Guangzhou University of Chinese Medicine","place":["Guangzhou, China"]},{"name":"The Laboratory of Orthopaedics and Traumatology of Lingnan Medical Research Center, Guangzhou University of Chinese Medicine","place":["Guangzhou, China"]},{"name":"Guangzhou University of Chinese Medicine","place":["Guangdong, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,7,22]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1038\/s41572-020-00216-3","article-title":"Bone metastases","volume":"6","author":"Coleman","year":"2020","journal-title":"Nat Rev Dis Primers"},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.1038\/nrurol.2015.90","article-title":"Targeting bone metastases in prostate cancer: improving clinical outcome","volume":"12","author":"Body","year":"2015","journal-title":"Nat Rev Urol"},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.1007\/s00520-015-2908-1","article-title":"Pain and analgesic use associated with skeletal-related events in patients with advanced cancer and bone metastases","volume":"24","author":"von Moos","year":"2016","journal-title":"Support Care Cancer"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1038\/nrc3055","article-title":"Cancer to bone: a fatal attraction","volume":"11","author":"Weilbaecher","year":"2011","journal-title":"Nat Rev Cancer"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2021.03.011","article-title":"The bone microenvironment invigorates metastatic seeds for further dissemination","volume":"184","author":"Zhang","year":"2021","journal-title":"Cell"},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1038\/s41588-021-00911-1","article-title":"A single-cell and spatially resolved atlas of human breast cancers","volume":"53","author":"Wu","year":"2021","journal-title":"Nat Genet"},{"key":"B7","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1016\/j.ejca.2019.04.017","article-title":"Screening for brain metastases in patients with stage III non-small-cell lung cancer, magnetic resonance imaging or computed tomography? 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