Role of bone marrow adipocytes in bone metastasis development and progression: a systematic review

PurposeBone marrow adipocytes (BMAs) are the most plentiful cells in the bone marrow and function as an endocrine organ by producing fatty acids, cytokines, and adipokines. Consequently, BMAs can interact with tumor cells, influencing both tumor growth and the onset and progression of bone metastasi...

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Main Authors: F. Salamanna, D. Contartese, C. Errani, M. Sartori, V. Borsari, G. Giavaresi
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-08-01
Series:Frontiers in Endocrinology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fendo.2023.1207416/full
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author F. Salamanna
D. Contartese
C. Errani
M. Sartori
V. Borsari
G. Giavaresi
author_facet F. Salamanna
D. Contartese
C. Errani
M. Sartori
V. Borsari
G. Giavaresi
author_sort F. Salamanna
collection DOAJ
description PurposeBone marrow adipocytes (BMAs) are the most plentiful cells in the bone marrow and function as an endocrine organ by producing fatty acids, cytokines, and adipokines. Consequently, BMAs can interact with tumor cells, influencing both tumor growth and the onset and progression of bone metastasis. This review aims to systematically evaluate the role of BMAs in the development and progression of bone metastasis.MethodsA comprehensive search was conducted on PubMed, Web of Science, and Scopus electronic databases, following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement standards, to identify studies published from March 2013 to June 2023. Two independent reviewers assessed and screened the literature, extracted the data, and evaluated the quality of the studies. The body of evidence was evaluated and graded using the ROBINS-I tool for non-randomized studies of interventions and the Systematic Review Centre for Laboratory Animal Experimentation (SYRCLE) tool for in vivo studies. The results were synthesized using descriptive methods.ResultsThe search yielded a total of 463 studies, of which 17 studies were included in the final analysis, including 15 preclinical studies and two non-randomized clinical studies. Analysis of preclinical studies revealed that BMAs play a significant role in bone metastasis, particularly in prostate cancer followed by breast and malignant melanoma cancers. BMAs primarily influence cancer cells by inducing a glycolytic phenotype and releasing or upregulating soluble factors, chemokines, cytokines, adipokines, tumor-derived fatty acid-binding protein (FABP), and members of the nuclear receptor superfamily, such as chemokine (C-C motif) ligand 7 (CCL7), C-X-C Motif Chemokine Ligand (CXCL)1, CXCL2, interleukin (IL)-1β, IL-6, FABP4, and peroxisome proliferator-activated receptor γ (PPARγ). These factors also contribute to adipocyte lipolysis and regulate a pro-inflammatory phenotype in BMAs. However, the number of clinical studies is limited, and definitive conclusions cannot be drawn.ConclusionThe preclinical studies reviewed indicate that BMAs may play a crucial role in bone metastasis in prostate, breast, and malignant melanoma cancers. Nevertheless, further preclinical and clinical studies are needed to better understand the complex role and relationship between BMAs and cancer cells in the bone microenvironment. Targeting BMAs in combination with standard treatments holds promise as a potential therapeutic strategy for bone metastasis.
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spelling doaj.art-583de314588444c2985839dfeaecb8ad2023-08-30T08:28:09ZengFrontiers Media S.A.Frontiers in Endocrinology1664-23922023-08-011410.3389/fendo.2023.12074161207416Role of bone marrow adipocytes in bone metastasis development and progression: a systematic reviewF. Salamanna0D. Contartese1C. Errani2M. Sartori3V. Borsari4G. Giavaresi5Surgical Sciences and Technologies, IRCCS Istituto Ortopedico Rizzoli, Bologna, ItalySurgical Sciences and Technologies, IRCCS Istituto Ortopedico Rizzoli, Bologna, Italy3rd Orthopaedic and Traumatologic Clinic Prevalently Oncologic, IRCCS Istituto Ortopedico Rizzoli, Bologna, ItalySurgical Sciences and Technologies, IRCCS Istituto Ortopedico Rizzoli, Bologna, ItalySurgical Sciences and Technologies, IRCCS Istituto Ortopedico Rizzoli, Bologna, ItalySurgical Sciences and Technologies, IRCCS Istituto Ortopedico Rizzoli, Bologna, ItalyPurposeBone marrow adipocytes (BMAs) are the most plentiful cells in the bone marrow and function as an endocrine organ by producing fatty acids, cytokines, and adipokines. Consequently, BMAs can interact with tumor cells, influencing both tumor growth and the onset and progression of bone metastasis. This review aims to systematically evaluate the role of BMAs in the development and progression of bone metastasis.MethodsA comprehensive search was conducted on PubMed, Web of Science, and Scopus electronic databases, following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement standards, to identify studies published from March 2013 to June 2023. Two independent reviewers assessed and screened the literature, extracted the data, and evaluated the quality of the studies. The body of evidence was evaluated and graded using the ROBINS-I tool for non-randomized studies of interventions and the Systematic Review Centre for Laboratory Animal Experimentation (SYRCLE) tool for in vivo studies. The results were synthesized using descriptive methods.ResultsThe search yielded a total of 463 studies, of which 17 studies were included in the final analysis, including 15 preclinical studies and two non-randomized clinical studies. Analysis of preclinical studies revealed that BMAs play a significant role in bone metastasis, particularly in prostate cancer followed by breast and malignant melanoma cancers. BMAs primarily influence cancer cells by inducing a glycolytic phenotype and releasing or upregulating soluble factors, chemokines, cytokines, adipokines, tumor-derived fatty acid-binding protein (FABP), and members of the nuclear receptor superfamily, such as chemokine (C-C motif) ligand 7 (CCL7), C-X-C Motif Chemokine Ligand (CXCL)1, CXCL2, interleukin (IL)-1β, IL-6, FABP4, and peroxisome proliferator-activated receptor γ (PPARγ). These factors also contribute to adipocyte lipolysis and regulate a pro-inflammatory phenotype in BMAs. However, the number of clinical studies is limited, and definitive conclusions cannot be drawn.ConclusionThe preclinical studies reviewed indicate that BMAs may play a crucial role in bone metastasis in prostate, breast, and malignant melanoma cancers. Nevertheless, further preclinical and clinical studies are needed to better understand the complex role and relationship between BMAs and cancer cells in the bone microenvironment. Targeting BMAs in combination with standard treatments holds promise as a potential therapeutic strategy for bone metastasis.https://www.frontiersin.org/articles/10.3389/fendo.2023.1207416/fullbone marrow adipocytescancer cellsbone metastasisbone microenvironmentsystematic review
spellingShingle F. Salamanna
D. Contartese
C. Errani
M. Sartori
V. Borsari
G. Giavaresi
Role of bone marrow adipocytes in bone metastasis development and progression: a systematic review
Frontiers in Endocrinology
bone marrow adipocytes
cancer cells
bone metastasis
bone microenvironment
systematic review
title Role of bone marrow adipocytes in bone metastasis development and progression: a systematic review
title_full Role of bone marrow adipocytes in bone metastasis development and progression: a systematic review
title_fullStr Role of bone marrow adipocytes in bone metastasis development and progression: a systematic review
title_full_unstemmed Role of bone marrow adipocytes in bone metastasis development and progression: a systematic review
title_short Role of bone marrow adipocytes in bone metastasis development and progression: a systematic review
title_sort role of bone marrow adipocytes in bone metastasis development and progression a systematic review
topic bone marrow adipocytes
cancer cells
bone metastasis
bone microenvironment
systematic review
url https://www.frontiersin.org/articles/10.3389/fendo.2023.1207416/full
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