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Tobacco-induced hyperglycemia promotes lung cancer progression via cancer cell-macrophage interaction through paracrine IGF2/IR/NPM1-driven PD-L1 expression.

التفاصيل البيبلوغرافية
العنوان: Tobacco-induced hyperglycemia promotes lung cancer progression via cancer cell-macrophage interaction through paracrine IGF2/IR/NPM1-driven PD-L1 expression.
المؤلفون: Jang HJ; Creative Research Initiative Center for concurrent control of emphysema and lung cancer, College of Pharmacy, Seoul National University, Seoul, 08826, Republic of Korea., Min HY; Creative Research Initiative Center for concurrent control of emphysema and lung cancer, College of Pharmacy, Seoul National University, Seoul, 08826, Republic of Korea.; Natural Products Research Institute, College of Pharmacy, Seoul National University, Seoul, 08826, Republic of Korea., Kang YP; College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University, Seoul, 08826, Republic of Korea., Boo HJ; Creative Research Initiative Center for concurrent control of emphysema and lung cancer, College of Pharmacy, Seoul National University, Seoul, 08826, Republic of Korea.; Department of Histology, College of Medicine, Jeju National University, Jeju, 63243, Republic of Korea., Kim J; Creative Research Initiative Center for concurrent control of emphysema and lung cancer, College of Pharmacy, Seoul National University, Seoul, 08826, Republic of Korea., Ahn JH; Creative Research Initiative Center for concurrent control of emphysema and lung cancer, College of Pharmacy, Seoul National University, Seoul, 08826, Republic of Korea.; Department of Molecular Medicine and Biopharmaceutical Sciences, Graduate School of Convergence Science and Technology and College of Pharmacy, Seoul National University, Seoul, 08826, Republic of Korea., Oh SH; College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University, Seoul, 08826, Republic of Korea., Jung JH; PET core, Convergence Medicine Research Center, Asan Medical Center, Seoul, 05505, Republic of Korea., Park CS; Soonchunhyang University Bucheon Hospital, Bucheon-si, Gyeonggi-do, 14584, Republic of Korea., Park JS; Soonchunhyang University Bucheon Hospital, Bucheon-si, Gyeonggi-do, 14584, Republic of Korea., Kim SY; PET core, Convergence Medicine Research Center, Asan Medical Center, Seoul, 05505, Republic of Korea.; Department of Convergence Medicine, University of Ulsan College of Medicine, Seoul, 05505, Republic of Korea., Lee HY; Creative Research Initiative Center for concurrent control of emphysema and lung cancer, College of Pharmacy, Seoul National University, Seoul, 08826, Republic of Korea. hylee135@snu.ac.kr.; Natural Products Research Institute, College of Pharmacy, Seoul National University, Seoul, 08826, Republic of Korea. hylee135@snu.ac.kr.; College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University, Seoul, 08826, Republic of Korea. hylee135@snu.ac.kr.
المصدر: Nature communications [Nat Commun] 2024 Jun 08; Vol. 15 (1), pp. 4909. Date of Electronic Publication: 2024 Jun 08.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Pub. Group Country of Publication: England NLM ID: 101528555 Publication Model: Electronic Cited Medium: Internet ISSN: 2041-1723 (Electronic) Linking ISSN: 20411723 NLM ISO Abbreviation: Nat Commun Subsets: MEDLINE
أسماء مطبوعة: Original Publication: [London] : Nature Pub. Group
مواضيع طبية MeSH: Lung Neoplasms*/metabolism , Lung Neoplasms*/pathology , Lung Neoplasms*/genetics , Mice, Inbred C57BL* , Receptor, Insulin*/metabolism , Receptor, Insulin*/genetics , B7-H1 Antigen*/metabolism , B7-H1 Antigen*/genetics , Hyperglycemia*/metabolism , Benzo(a)pyrene*/toxicity , Nucleophosmin* , Insulin-Like Growth Factor II*/metabolism , Insulin-Like Growth Factor II*/genetics , Disease Progression* , Nuclear Proteins*/metabolism , Nuclear Proteins*/genetics, Animals ; Male ; Humans ; Mice ; Nitrosamines/toxicity ; Tumor-Associated Macrophages/metabolism ; Cell Line, Tumor ; Paracrine Communication ; Gene Expression Regulation, Neoplastic ; Smoking/adverse effects ; Macrophages/metabolism
مستخلص: Tobacco smoking (TS) is implicated in lung cancer (LC) progression through the development of metabolic syndrome. However, direct evidence linking metabolic syndrome to TS-mediated LC progression remains to be established. Our findings demonstrate that 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone and benzo[a]pyrene (NNK and BaP; NB), components of tobacco smoke, induce metabolic syndrome characteristics, particularly hyperglycemia, promoting lung cancer progression in male C57BL/6 J mice. NB enhances glucose uptake in tumor-associated macrophages by increasing the expression and surface localization of glucose transporter (GLUT) 1 and 3, thereby leading to transcriptional upregulation of insulin-like growth factor 2 (IGF2), which subsequently activates insulin receptor (IR) in LC cells in a paracrine manner, promoting its nuclear import. Nuclear IR binds to nucleophosmin (NPM1), resulting in IR/NPM1-mediated activation of the CD274 promoter and expression of programmed death ligand-1 (PD-L1). Restricting glycolysis, depleting macrophages, or blocking PD-L1 inhibits NB-mediated LC progression. Analysis of patient tissues and public databases reveals elevated levels of IGF2 and GLUT1 in tumor-associated macrophages, as well as tumoral PD-L1 and phosphorylated insulin-like growth factor 1 receptor/insulin receptor (pIGF-1R/IR) expression, suggesting potential poor prognostic biomarkers for LC patients. Our data indicate that paracrine IGF2/IR/NPM1/PD-L1 signaling, facilitated by NB-induced dysregulation of glucose levels and metabolic reprogramming of macrophages, contributes to TS-mediated LC progression.
(© 2024. The Author(s).)
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معلومات مُعتمدة: NRF-2016R1A3B1908631 National Research Foundation (NRF)
المشرفين على المادة: EC 2.7.10.1 (Receptor, Insulin)
0 (B7-H1 Antigen)
3417WMA06D (Benzo(a)pyrene)
117896-08-9 (Nucleophosmin)
67763-97-7 (Insulin-Like Growth Factor II)
0 (Nuclear Proteins)
0 (Npm1 protein, mouse)
0 (Nitrosamines)
0 (NPM1 protein, human)
0 (IGF2 protein, mouse)
0 (Cd274 protein, mouse)
0 (CD274 protein, human)
0 (IGF2 protein, human)
تواريخ الأحداث: Date Created: 20240608 Date Completed: 20240608 Latest Revision: 20240611
رمز التحديث: 20240611
مُعرف محوري في PubMed: PMC11162468
DOI: 10.1038/s41467-024-49199-9
PMID: 38851766
قاعدة البيانات: MEDLINE
الوصف
تدمد:2041-1723
DOI:10.1038/s41467-024-49199-9