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Sazzad Hassan, … , Sandeep Robert Datta, George Kulik
Published January 25, 2013
Citation Information: J Clin Invest. 2013;123(2):874-886. https://doi.org/10.1172/JCI63324.
Citation Information: J Clin Invest. 2013;123(2):874-886. https://doi.org/10.1172/JCI63324.
Abstract
Prostate cancer patients have increased levels of stress and anxiety. Conversely, men who take beta blockers, which interfere with signaling from the stress hormones adrenaline and noradrenaline, have a lower incidence of prostate cancer; however, the mechanisms underlying stress–prostate cancer interactions are unknown. Here, we report that stress promotes prostate carcinogenesis in mice in an adrenaline-dependent manner. Behavioral stress inhibited apoptosis and delayed prostate tumor involution both in phosphatase and tensin homolog–deficient (PTEN-deficient) prostate cancer xenografts treated with PI3K inhibitor and in prostate tumors of mice with prostate-restricted expression of c-MYC (Hi-Myc mice) subjected to androgen ablation therapy with bicalutamide. Additionally, stress accelerated prostate cancer development in Hi-Myc mice. The effects of stress were prevented by treatment with the selective β2-adrenergic receptor (ADRB2) antagonist ICI118,551 or by inducible expression of PKA inhibitor (PKI) or of BCL2-associated death promoter (BAD) with a mutated PKA phosphorylation site (BADS112A) in xenograft tumors. Effects of stress were also blocked in Hi-Myc mice expressing phosphorylation-deficient BAD (BAD3SA). These results demonstrate interactions between prostate tumors and the psychosocial environment mediated by activation of an adrenaline/ADRB2/PKA/BAD antiapoptotic signaling pathway. Our findings could be used to identify prostate cancer patients who could benefit from stress reduction or from pharmacological inhibition of stress-induced signaling.
Authors
Sazzad Hassan, Yelena Karpova, Daniele Baiz, Dana Yancey, Ashok Pullikuth, Anabel Flores, Thomas Register, J. Mark Cline, Ralph D’Agostino Jr., Nika Danial, Sandeep Robert Datta, George Kulik
Total citations by year
Citation information
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A Chang, C Kim-Fuchs, C Le, F Hollande, E Sloan |
Cancers | 2015 |
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Neural plasticity in pancreatitis and pancreatic cancer
IE Demir, H Friess, GO Ceyhan |
Nature Reviews Gastroenterology & Hepatology | 2015 |
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β2-adrenoceptor signaling regulates invadopodia formation to enhance tumor cell invasion
SJ Creed, CP Le, M Hassan, CK Pon, S Albold, KT Chan, ME Berginski, Z Huang, JE Bear, JR Lane, ML Halls, D Ferrari, CJ Nowell, EK Sloan |
Breast Cancer Research | 2015 |
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β-Adrenergic Receptor Signaling in Prostate Cancer
PR Braadland, Hà Ramberg, HH Grytli, KA Taskén |
Frontiers in Oncology | 2015 |
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Depression in cancer patients: Pathogenesis, implications and treatment (Review)
H Smith |
Oncology Letters | 2015 |
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Standard Sub-Thermoneutral Caging Temperature Influences Radiosensitivity of Hematopoietic Stem and Progenitor Cells
BJ Povinelli, KM Kokolus, JW Eng, CW Dougher, L Curtin, ML Capitano, CT Sailsbury-Ruf, EA Repasky, MJ Nemeth, Z Ivanovic |
PloS one | 2015 |
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Impact of beta-blockers on prostate cancer mortality: a meta-analysis of 16,825 patients
H Lu, X Liu, F Guo, S Tan, G Wang, H Liu, J Wang, X He, Y Mo, B Shi |
OncoTargets and therapy | 2015 |
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β2-AR signaling controls trastuzumab resistance-dependent pathway
D Liu, Z Yang, T Wang, Z Yang, H Chen, Y Hu, C Hu, L Guo, Q Deng, Y Liu, M Yu, M Shi, N Du, N Guo |
Oncogene | 2015 |
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Chronic restraint-induced stress has little modifying effect on radiation hematopoietic toxicity in mice
B Wang, K Tanaka, T Katsube, Y Ninomiya, G Vares, Q Liu, A Morita, T Nakajima, M Nenoi |
Journal of Radiation Research | 2015 |
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Effect of Chronic Psychological Stress on Liver Metastasis of Colon Cancer in Mice
L Zhao, J Xu, F Liang, A Li, Y Zhang, J Sun, OR Bandapalli |
PloS one | 2015 |
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A Her2-let-7-β2-AR circuit affects prognosis in patients with Her2-positive breast cancer
D Liu, Q Deng, L Sun, T Wang, Z Yang, H Chen, L Guo, Y Liu, Y Ma, N Guo, M Shi |
BMC Cancer | 2015 |
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Stress-Related Signaling Pathways in Lethal and Nonlethal Prostate Cancer
D Lu, JA Sinnott, U Valdimarsdottir, F Fang, T Gerke, S Tyekucheva, M Fiorentino, M Lambe, HD Sesso, CJ Sweeney, KM Wilson, EL Giovannucci, M Loda, LA Mucci, K Fall |
Clinical cancer research | 2015 |
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Sustained adrenergic signaling leads to increased metastasis in ovarian cancer via increased PGE2 synthesis
AS Nagaraja, PL Dorniak, NC Sadaoui, Y Kang, T Lin, G Armaiz-Pena, SY Wu, R Rupaimoole, JK Allen, KM Gharpure, S Pradeep, B Zand, RA Previs, JM Hansen, C Ivan, C Rodriguez-Aguayo, P Yang, G Lopez-Berestein, SK Lutgendorf, SW Cole, AK Sood |
Oncogene | 2015 |
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Norepinephrine induced epithelial–mesenchymal transition in HT-29 and A549 cells in vitro
J Zhang, Y Deng, J Liu, Y Wang, T Yi, B Huang, S He, B Zheng, Y Jiang |
Journal of Cancer Research and Clinical Oncology | 2015 |
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Signaling pathways in the development of infantile hemangioma
Y Ji, S Chen, K Li, L Li, C Xu, B Xiang |
Journal of Hematology & Oncology | 2014 |
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Gene expression profile of compressed primary human cementoblasts before and after IL-1β stimulation
K Diercke, S Zingler, A Kohl, CJ Lux, R Erber |
Clinical Oral Investigations | 2014 |
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A nervous tumor microenvironment: the impact of adrenergic stress on cancer cells, immunosuppression, and immunotherapeutic response
JW Eng, KM Kokolus, CB Reed, BL Hylander, WW Ma, EA Repasky |
Cancer Immunology, Immunotherapy | 2014 |
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Integrating new discoveries into the “vicious cycle” paradigm of prostate to bone metastases
LM Cook, G Shay, A Aruajo, CC Lynch |
Cancer and Metastasis Reviews | 2014 |
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Exogenous norepinephrine attenuates the efficacy of sunitinib in a mouse cancer model
GH Deng, J Liu, J Zhang, Y Wang, XC Peng, YQ Wei, Y Jiang |
Journal of Experimental & Clinical Cancer Research | 2014 |
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Role of the autonomic nervous system in tumorigenesis and metastasis
C Magnon |
Molecular & Cellular Oncology | 2014 |
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hTERT mediates norepinephrine-induced Slug expression and ovarian cancer aggressiveness
MJ Choi, KH Cho, S Lee, YJ Bae, KJ Jeong, SY Rha, EJ Choi, JH Park, JM Kim, JS Lee, GB Mills, HY Lee |
Oncogene | 2014 |
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Why Stress is BAD for Cancer Patients
Archana Nagaraja, Guillermo N Armaiz-Pena, Susan K Lutgendorf, Anil Sood |
Journal of Clinical Investigation | 2013 |
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Age-related changes in the innervation of the prostate gland: Implications for prostate cancer initiation and progression
CW White, JH Xie, S Ventura |
Organogenesis | 2013 |
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Lymphovascular and neural regulation of metastasis: Shared tumour signalling pathways and novel therapeutic approaches
CP Le, T Karnezis, MG Achen, SA Stacker, EK Sloan |
Best Practice & Research Clinical Anaesthesiology | 2013 |
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Systems modeling of anti-apoptotic pathways in prostate cancer: psychological stress triggers a synergism pattern switch in drug combination therapy
X Sun, J Bao, KC Nelson, KC Li, G Kulik, X Zhou |
PLoS computational biology | 2013 |
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Surgical stress delays prostate involution in mice
S Hassan, Y Karpova, A Flores, R D'Agostino, G Kulik |
PloS one | 2013 |
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The gateway theory: bridging neural and immune interactions in the CNS
D Kamimura, M Yamada, M Harada, L Sabharwal, J Meng, H Bando, H Ogura, T Atsumi, Y Arima, M Murakami |
Frontiers in neuroscience | 2013 |
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Does the autonomic nervous system contribute to the initiation and progression of prostate cancer?
S Ventura, BA Evans |
Asian Journal of Andrology | 2013 |
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Regulation of immune cell infiltration into the CNS by regional neural inputs explained by the gate theory
Y Arima, D Kamimura, L Sabharwal, M Yamada, H Bando, H Ogura, T Atsumi, M Murakami |
Mediators of Inflammation | 2013 |
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Targeting psychoemotional stress to treat prostate cancer
G Kulik |
Asian Journal of Andrology | 2013 |
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A pilot study of blood epinephrine levels and CREB phosphorylation in men undergoing prostate biopsies
S Hassan, Y Karpova, A Flores, R D’Agostino, SC Danhauer, A Hemal, G Kulik |
International Urology and Nephrology | 2013 |
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Catecholamine Stress Alters Neutrophil Trafficking and Impairs Wound Healing by β2-Adrenergic Receptor–Mediated Upregulation of IL-6
MH Kim, F Gorouhi, S Ramirez, JL Granick, BA Byrne, AM Soulika, SI Simon, RR Isseroff |
Journal of Investigative Dermatology | 2013 |
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Combination of the PI3K inhibitor ZSTK474 with a PSMA-targeted immunotoxin accelerates apoptosis and regression of prostate cancer.
Baiz D, Hassan S, Choi YA, Flores A, Karpova Y, Yancey D, Pullikuth A, Sui G, Sadelain M, Debinski W, Kulik G |
Neoplasia (New York, N.Y.) | 2013 |
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Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd |
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology | 2009 |
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