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Sympathetic nervous system regulation of the tumour microenvironment
Open accessAbstract
The peripheral autonomic nervous system (ANS) is known to regulate gene expression in primary tumours and their surrounding microenvironment. Activation of the sympathetic division of the ANS in particular modulates gene expression programmes that promote metastasis of solid tumours by stimulating macrophage infiltration, inflammation, angiogenesis, epithelial-mesenchymal transition and tumour invasion, and by inhibiting cellular immune responses and programmed cell death. Haematological cancers are modulated by sympathetic nervous system (SNS) regulation of stem cell biology and haematopoietic differentiation programmes. In addition to identifying a molecular basis for physiologic stress effects on cancer, these findings have also identified new pharmacological strategies to inhibit cancer progression in vivo.
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“Parallel findings in animal and in vitro models support these data [11, 16–22].”
From Living Well: Protocol for a web-based program to improve quality of life in rural and urban ovarian cancer survivors (2024) · cites this paper as [22]
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“ticularly concerning for preclinical tumor models because a growing literature in the last 15–20 y has developed demonstrating the tumor promoting effects of adrenergic stress signaling (52, 53).”
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“Activation of the sympathetic division of the ANS in particular modulates gene expression that promotes metastasis of solid tumors (23).”
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“In addition to the ECM, the interstitium consists of interstitial fluid, interstitial cells, and nerve fibers (including sympathetic nerves), that coil around local capillaries (Cole et al., 2015) (Figure 3).”
BackgroundNeurobiology of cancer: Adrenergic signaling and drug repurposing
Dong, Z.-K., Wang, Y., Li, W., & Jin, W. (2024) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2024.108750 · Cited by 33
Madden, K. S. (2016) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2016.04.015 · Cited by 31
Hylander, B. L., Eng, J. W. ‐., & Repasky, E. A. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-67577-0_12 · Cited by 33
Bae, G. E., Kim, H. S., Won, K. Y., Kim, G. Y., Sung, J., & Lim, S.-J. (2018) · Anticancer Research · doi:10.21873/anticanres.13102 · Cited by 32
Taub, C. J., Lippman, M. E., Hudson, B. I., Blomberg, B. B., Diaz, A., Fisher, H. M., Nahin, E. R., Lechner, S. C., Kwak, T., Hwang, G. H., et al. (2019) · Cancer · doi:10.1002/cncr.31965 · Cited by 31
“One process that is suggested to contribute to stress-associated elevations in leukocyte inflammatory signaling is the effusion of myeloid-derived suppressor cells(19) from the bone marrow after SNS activation.(20) It is hypothesized that these myeloid cells stimulate immune and cancer cells, among others, through the…”
BackgroundAutonomic nervous system and cancer
Simó, M., Navarro, X., Yuste, V. J., & Bruna, J. (2018) · Clinical Autonomic Research · doi:10.1007/s10286-018-0523-1 · Cited by 30
Lucido, C. T., Callejas‐Valera, J. L., Colbert, P. L., Vermeer, D. W., Miskimins, W. K., Spanos, W. C., & Vermeer, P. D. (2018) · Oncogenesis · doi:10.1038/s41389-018-0090-2 · Cited by 29
Arnold, J. T. (2022) · Journal of Ayurveda and Integrative Medicine · doi:10.1016/j.jaim.2022.100676 · Cited by 39
“These hormones influence the immune responses and inflammation, and alter tumor angiogenesis, mesenchymal differentiation, and metastasis [57].”
BackgroundPerrot, C. Y., Sawada, J., & Komatsu, M. (2018) · The FASEB Journal · doi:10.1096/fj.201700818rrr · Cited by 31
Spleen contributes to restraint stress induced hepatocellular carcinoma progression
Jiang, W., Li, Y., Wei, W., Li, J.-W., Li, L., Zhang, C., Zhang, S.-Q., Kong, G., & Li, Z. (2020) · International Immunopharmacology · doi:10.1016/j.intimp.2020.106420 · Cited by 29
Hao, M., Liu, X., Rong, P., Li, S., & Guo, S. (2021) · Scientific Reports · doi:10.1038/s41598-020-79750-9 · Cited by 33
Lopez, G., Mao, J. J. J., & Cohen, L. G. (2017) · Medical Clinics of North America · doi:10.1016/j.mcna.2017.04.011 · Cited by 29
The Central Nervous Mechanism of Stress-Promoting Cancer Progression
Hong, Y., Zhang, L., Liu, N., Xu, X., Liu, D., & Tu, J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012653 · Cited by 33
“How, then, do anxious states affect tumor growth? During states of anxiety, central brain regions involved in the stress response are activated, followed by activation of associated descending pathways, which results in abnormal secretion of various neurotransmitters, hormones, and other factors, thereby affecting tum…”
BackgroundLi, W., & Zhao, Y. (2018) · Asian Journal of Andrology · doi:10.4103/aja.aja_32_18 · Cited by 29
Moore, J. X., Andrzejak, S. E., Bevel, M., Jones, S. R., & Tingen, M. S. (2022) · SSM - Population Health · doi:10.1016/j.ssmph.2022.101185 · Cited by 30
Pérez, A. M. L., Collado‐Mateo, D., Mayo, X., Liguori, G. A., Humphreys, L. J., & Jiménez, A. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.712823 · Cited by 27
“Cancer decreases catecholamine production, with a concomitant rise in oxidative stress, inflammation, and cancer progression (Cole et al., 2015).”
BackgroundMechanisms underlying the cross‐talk between heart and cancer
Brancaccio, M., Pirozzi, F., Hirsch, E., & Ghigo, A. (2019) · The Journal of Physiology · doi:10.1113/jp276746 · Cited by 27
“In the tumour, the autonomous nerves regulate gene expression in cancer cells and cells from the tumour microenvironment, promoting inflammation, macrophage recruitment, angiogenesis, epithelial–mesenchymal transition and metastatic progression (Cole et al. 2015).”
BackgroundIntegrative Approaches to Stress Management
Carlson, L. E., Toivonen, K., & Subnis, U. B. (2019) · The Cancer Journal · doi:10.1097/ppo.0000000000000395 · Cited by 32
Stress in Metastatic Breast Cancer: To the Bone and Beyond
Lourenço, C., Conceição, F., Jerónimo, C., Lamghari, M., & Sousa, D. M. (2022) · Cancers · doi:10.3390/cancers14081881 · Cited by 28
“The catecholamines levels return to baseline in a very short amount of time (20–60 min), and therefore the activation of the acute stress responses is considered adaptive [53].”
BackgroundDrygała, S., Radzikowski, M., & Maciejczyk, M. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1489657 · Cited by 28
Beta-Blockers Use and Risk of Breast Cancer in Women with Hypertension
Zheng, G., Sundquist, J., Sundquist, K., & Ji, J. (2021) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-20-1599 · Cited by 26
“The nonselective beta-blockers (in our study propranolol) that can block beta-2 receptors are reportedly more likely to show a protective effect on cancer than the beta-1 selective blockers, which are more commonly used in cardiovascular therapy (7, 31, 32).”
BackgroundNeighborhood Disadvantage and Breast Cancer–Specific Survival in the US
Goel, N., Hernandez, A. E., & Mazul, A. L. (2024) · JAMA Network Open · doi:10.1001/jamanetworkopen.2024.7336 · Cited by 26
Zhang, Z., Lv, Z. G., Lu, M., Li, H., & Zhou, J. (2024) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2024.189121 · Cited by 27
Barr, J. L., Walz, A., Restaino, A. C., Amit, M., Barclay, S. M., Vichaya, E. G., Spanos, W. C., Dantzer, R., Talbot, S., & Vermeer, P. D. (2024) · eLife · doi:10.7554/elife.97916 · Cited by 36
“…these and other studies establish that solid peripheral tumors engage with the peripheral nervous system ( Madeo et al., 2018 ; Barr et al., 2021 ; Cole et al., 2015 ; Magnon et al., 2013 ; Sadighparvar et al., 2021 ; Chen and Ayala, 2018 ), it raises the possibility of a direct neuronal…”
Psychological stress and cancer: new evidence of an increasingly strong link
Martinelli, R. (2020) · Translational Medicine UniSa · doi:10.37825/2239-9747.1010 · Cited by 27
“adrenergic system has been associated with a upregulation of the expression of specific oncogenic signaling pathways including Sirtuin-1(Sirt-1) in cervical cancer, Src in ovarian cancer and Human Epidermal Growth Factor Receptor2 (Her2) in breast cancer [12,13].”
BackgroundHou, Y.-H., Shi, W.-C., Cai, S., Liu, H., Zheng, Z., Qi, F.-W., Li, C., Feng, X.-M., Peng, K., & Ji, F. (2021) · Drug Design Development and Therapy · doi:10.2147/dddt.s316804 · Cited by 25
“The abovementioned effects combined contribute to tumor invasion and metastasis.(24) A recent review summarizes the effects of Table 1 Patient Demographics and Surgical Characteristics”
BackgroundLutgendorf, S., Penedo, F., Goodheart, M., Dahmoush, L., Arevalo, J., Thaker, P., Slavich, G. M., Sood, A., & Cole, S. (2020) · Cancer · doi:10.1002/cncr.33060 · Cited by 25
“that alter gene expression through activation of transcription factors that subsequently alter cellular processes.(2) Because social isolation has been linked with higher lev-”
BackgroundSelf-citation
Metadata
- Authors
- Cole, S. W., Nagaraja, A. S., Lutgendorf, S. K., Green, P. A., & Sood, A. K.
- Affiliations
- The University of Texas MD Anderson Cancer Center (US)
- University of Iowa (US)
- National Cancer Institute (US)
- Venue
- Nature Reviews Cancer
- Published
- 2015-08-24
- Volume
- 15
- Issue
- 9
- Pages
- 563-572
- ISSN
- 1474-175X (ISSN-L)
- 1474-1768
- PMC
- PMC4828959
- OpenAlex
- W1959055352
- Cited by
- 576
- References
- 132
- Citations by year
- 2026: 66 · 2025: 53 · 2024: 47 · 2023: 63 · 2022: 66 · 2021: 57 · 2020: 67 · 2019: 57 · 2018: 43 · 2017: 32 · 2016: 22 · 2015: 3
- FWCI
- 4.59
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature reviews. Cancer (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (AG017265, R37AG033590, AG033590, R01AG033590, P30AG017265)
- National Cancer Institute (CA 109298, CA177909, P50CA098258, U54CA151668, R01CA177909, CA083639, CA-104825, R01CA109298, CA140933, R01CA116778, R01CA104825, CA151668, CA-116778, R01CA140933, P50CA083639, CA098258, P30CA016672)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Stress, Anesthesia, and Immune Response
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Keywords
- sympathetic nervous system, tumor microenvironment, peripheral autonomic nervous system, beta-adrenergic signaling, physiological stress, metastasis, macrophage infiltration, tumor inflammation, angiogenesis, epithelial-mesenchymal transition, tumor invasion, antitumor immunity, hematologic cancer, cancer stem cells, hematopoietic differentiation
- MeSH terms
- Cell Differentiation, Humans, Neoplasms, Neovascularization, Pathologic, Sympathetic Nervous System, Gene Expression Regulation, Neoplastic, Epithelial-Mesenchymal Transition, Tumor Microenvironment
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