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Anil K. Sood, … , Steven W. Cole, Susan K. Lutgendorf
Published April 12, 2010
Citation Information: J Clin Invest. 2010;120(5):1515-1523. https://doi.org/10.1172/JCI40802.
Citation Information: J Clin Invest. 2010;120(5):1515-1523. https://doi.org/10.1172/JCI40802.
Abstract
Chronic stress is associated with hormonal changes that are known to affect multiple systems, including the immune and endocrine systems, but the effects of stress on cancer growth and progression are not fully understood. Here, we demonstrate that human ovarian cancer cells exposed to either norepinephrine or epinephrine exhibit lower levels of anoikis, the process by which cells enter apoptosis when separated from ECM and neighboring cells. In an orthotopic mouse model of human ovarian cancer, restraint stress and the associated increases in norepinephrine and epinephrine protected the tumor cells from anoikis and promoted their growth by activating focal adhesion kinase (FAK). These effects involved phosphorylation of FAKY397, which was itself associated with actin-dependent Src interaction with membrane-associated FAK. Importantly, in human ovarian cancer patients, behavioral states related to greater adrenergic activity were associated with higher levels of pFAKY397, which was in turn linked to substantially accelerated mortality. These data suggest that FAK modulation by stress hormones, especially norepinephrine and epinephrine, can contribute to tumor progression in patients with ovarian cancer and may point to potential new therapeutic targets for cancer management.
Authors
Anil K. Sood, Guillermo N. Armaiz-Pena, Jyotsnabaran Halder, Alpa M. Nick, Rebecca L. Stone, Wei Hu, Amy R. Carroll, Whitney A. Spannuth, Michael T. Deavers, Julie K. Allen, Liz Y. Han, Aparna A. Kamat, Mian M.K. Shahzad, Bradley W. McIntyre, Claudia M. Diaz-Montero, Nicholas B. Jennings, Yvonne G. Lin, William M. Merritt, Koen DeGeest, Pablo E. Vivas-Mejia, Gabriel Lopez-Berestein, Michael D. Schaller, Steven W. Cole, Susan K. Lutgendorf
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B Aslan, P Monroig, MC Hsu, GA Pena, C Rodriguez-Aguayo, V Gonzalez-Villasana, R Rupaimoole, AS Nagaraja, S Mangala, HD Han, E Yuca, SY Wu, C Ivan, TJ Moss, PT Ram, H Wang, A Gol-Chambers, O Ozkayar, P Kanlikilicer, E Fuentes-Mattei, N Kahraman, S Pradeep, B Ozpolat, S Tucker, MC Hung, K Baggerly, G Bartholomeusz, G Calin, AK Sood, G Lopez-Berestein |
Nature Communications | 2015 |
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Propranolol Reduces Cancer Risk: A Population-Based Cohort Study
PY Chang, WY Huang, CL Lin, TC Huang, YY Wu, JH Chen, CH Kao |
Medicine | 2015 |
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4th international conference on tumor progression and therapeutic resistance: meeting report
VV Prabhu, WS El-Deiry |
Cancer biology & therapy | 2015 |
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Eudaimonic well-being and tumor norepinephrine in patients with epithelial ovarian cancer: Eudaimonic Well-Being and Tumor NE in Ovarian Ca
LZ Davis, GM Slavich, PH Thaker, MJ Goodheart, DP Bender, L Dahmoush, DM Farley, KE Markon, FJ Penedo, DM Lubaroff, SW Cole, AK Sood, SK Lutgendorf |
Cancer | 2015 |
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Isoprenaline induces epithelial–mesenchymal transition in gastric cancer cells
YJ Lu, ZJ Geng, XY Sun, YH Li, XB Fu, XY Zhao, B Wei |
Molecular and Cellular Biochemistry | 2015 |
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Sympathetic nervous system regulation of the tumour microenvironment
SW Cole, AS Nagaraja, SK Lutgendorf, PA Green, AK Sood |
Nature Reviews Cancer | 2015 |
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Clinical impact of selective and nonselective beta-blockers on survival in patients with ovarian cancer: Beta-Blockers and Ovarian Cancer Survival
JL Watkins, PH Thaker, AM Nick, LM Ramondetta, S Kumar, DL Urbauer, K Matsuo, KC Squires, RL Coleman, SK Lutgendorf, PT Ramirez, AK Sood |
Cancer | 2015 |
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Neural Regulation of Pancreatic Cancer: A Novel Target for Intervention
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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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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FAK in cancer: mechanistic findings and clinical applications
FJ Sulzmaier, C Jean, DD Schlaepfer |
Nature Reviews Cancer | 2014 |
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Meta-analysis of the effects of beta blocker on survival time in cancer patients
CH Choi, T Song, TH Kim, JK Choi, JY Park, A Yoon, YY Lee, TJ Kim, DS Bae, JW Lee, BG Kim |
Journal of Cancer Research and Clinical Oncology | 2014 |
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Association of increased circulating catecholamine and glucocorticoid levels with risk of psychological problems in oral neoplasm patients
H Xie, B Li, L Li, X Zou, C Zhu, Y Li, N Gao, Q Chen, L Li |
PloS one | 2014 |
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Mind-Body Practices in Cancer Care
A Chaoul, K Milbury, AK Sood, S Prinsloo, L Cohen |
Current Oncology Reports | 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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Notch3 Overexpression Promotes Anoikis Resistance in Epithelial Ovarian Cancer via Upregulation of COL4A2
CW Brown, AS Brodsky, RN Freiman |
Molecular cancer research : MCR | 2014 |
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Propranolol Inhibits Glucose Metabolism and 18F-FDG Uptake of Breast Cancer Through Posttranscriptional Downregulation of Hexokinase-2
F Kang, W Ma, X Ma, Y Shao, W Yang, X Chen, L Li, J Wang |
Journal of Nuclear Medicine | 2014 |
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Adrenergic regulation of monocyte chemotactic protein 1 leads to enhanced macrophage recruitment and ovarian carcinoma growth
Armaiz-Pena GN, Gonzalez-Villasana V, Nagaraja AS, Rodriguez-Aguayo C, Sadaoui NC, Stone RL, Matsuo K, Dalton HJ, Previs RA, Jennings NB, Dorniak P, Hansen JM, Arevalo JM, Cole SW, Lutgendorf SK, Sood AK, Lopez-Berestein G |
Oncotarget | 2014 |
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Norepinephrine promotes tumor microenvironment reactivity through β3-adrenoreceptors during melanoma progression
Calvani M, Pelon F, Comito G, Taddei ML, Moretti S, Innocenti S, Nassini R, Gerlini G, Borgognoni L, Bambi F, Giannoni E, Filippi L, Chiarugi P |
Oncotarget | 2014 |
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Behavioral Stress Accelerates Prostate Cancer Development in Mice
Sazzad Hassan, Yelena Karpova, Daniele Baiz, Dana Yancey, Ashok Pullikuth, Anabel Flores, Thomas Register, Mark Cline, Ralph D’Agostino, Nika Danial, Sandeep Robert Datta, George Kulik |
Journal of Clinical Investigation | 2013 |
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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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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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Src activation by β-adrenoreceptors is a key switch for tumour metastasis
GN Armaiz-Pena, JK Allen, A Cruz, RL Stone, AM Nick, YG Lin, LY Han, LS Mangala, GJ Villares, P Vivas-Mejia, C Rodriguez-Aguayo, AS Nagaraja, KM Gharpure, Z Wu, RD English, KV Soman, MM Shazhad, M Zigler, MT Deavers, A Zien, TG Soldatos, DB Jackson, JE Wiktorowicz, M Torres-Lugo, T Young, KD Geest, GE Gallick, M Bar-Eli, G Lopez-Berestein, SW Cole, GE Lopez, SK Lutgendorf, AK Sood |
Nature Communications | 2013 |
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Epithelial–Mesenchymal Transition Enhances Nanoscale Actin Filament Dynamics of Ovarian Cancer Cells
S Lee, Y Yang, D Fishman, MM Holl, S Hong |
The Journal of Physical Chemistry B | 2013 |
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Mechanosensitivity and compositional dynamics of cell-matrix adhesions
HB Schiller, R Fässler |
EMBO reports | 2013 |
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Regulation of cytoskeleton organization by sphingosine in a mouse cell model of progressive ovarian cancer
AL Creekmore, CL Heffron, BP Brayfield, PC Roberts, EM Schmelz |
Biomolecules | 2013 |
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Importance of adrenergic pathways in women's cancers
PH Thaker, AK Sood, LM Ramondetta |
Cancer biomarkers : section A of Disease markers | 2013 |
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β1 integrin-FAK-Cortactin signaling is essential for human head and neck cancer radioresistance
Iris Eke, Yvonne Deuse, Stephanie Hehlgans, Kristin Gurtner, Mechthild Krause, Michael Baumann, Anna Shevchenko, Veit Sandfort, Nils Cordes |
Journal of Clinical Investigation | 2012 |
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Proteomics identification of annexin A2 as a key mediator in the metastasis and proangiogenesis of endometrial cells in human adenomyosis
S Zhou, T Yi, R Liu, C Bian, X Qi, X He, K Wang, J Li, X Zhao, C Huang, Y Wei |
Molecular & cellular proteomics : MCP | 2012 |
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Diindolylmethane-mediated Gli1 protein suppression induces anoikis in ovarian cancer cells in vitro and blocks tumor formation ability in vivo
PK Kandala, SK Srivastava |
The Journal of biological chemistry | 2012 |
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Inhibition of focal adhesion kinase (FAK) activity prevents anchorage-independent ovarian carcinoma cell growth and tumor progression
KK Ward, I Tancioni, C Lawson, NL Miller, C Jean, XL Chen, S Uryu, J Kim, D Tarin, DG Stupack, SC Plaxe, DD Schlaepfer |
Clinical & Experimental Metastasis | 2012 |
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High-Anxious Individuals Show Increased Chronic Stress Burden, Decreased Protective Immunity, and Increased Cancer Progression in a Mouse Model of Squamous Cell Carcinoma
FS Dhabhar, AN Saul, TH Holmes, C Daugherty, E Neri, JM Tillie, D Kusewitt, TM Oberyszyn |
PloS one | 2012 |
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Beta-adrenergic blocking drugs in breast cancer: a perspective review
TI Barron, L Sharp, K Visvanathan |
Therapeutic advances in medical oncology | 2012 |
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Neuroendocrine influences on cancer progression
GN Armaiz-Pena, SW Cole, SK Lutgendorf, AK Sood |
Brain, Behavior, and Immunity | 2012 |
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Surgery and stress promote cancer metastasis: New outlooks on perioperative mediating mechanisms and immune involvement
E Neeman, S Ben-Eliyahu |
Brain, Behavior, and Immunity | 2012 |
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Nervous system regulation of the cancer genome
SW Cole |
Brain, Behavior, and Immunity | 2012 |
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Mechanisms of Ovarian Cancer Metastasis: Biochemical Pathways
K Nakayama, N Nakayama, H Katagiri, K Miyazaki |
International journal of molecular sciences | 2012 |
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β-blockers: a novel class of antitumor agents
Y Ji, S Chen, X Xiao, S Zheng, K Li |
OncoTargets and therapy | 2012 |
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Social influences on clinical outcomes of patients with ovarian cancer
SK Lutgendorf, KD Geest, D Bender, A Ahmed, MJ Goodheart, L Dahmoush, MB Zimmerman, FJ Penedo, JA 3rd, P Ganjei-Azar, PH Thaker, L Mendez, DM Lubaroff, GM Slavich, SW Cole, AK Sood |
Journal of Clinical Oncology | 2012 |
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A New Approach to Reducing Postsurgical Cancer Recurrence: Perioperative Targeting of Catecholamines and Prostaglandins: Figure 1
E Neeman, O Zmora, S Ben-Eliyahu |
Clinical cancer research | 2012 |
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Moving beyond VEGF for anti-angiogenesis strategies in gynecologic cancer.
Thanapprapasr D, Hu W, Sood AK, Coleman RL |
Current pharmaceutical design | 2012 |
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Toward an Integrative Analysis of the Tumor Microenvironment in Ovarian Epithelial Carcinoma
RN Serio |
Cancer Microenvironment | 2011 |
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Focal adhesion kinase and endothelial cell apoptosis
Q Lu, S Rounds |
Microvascular Research | 2011 |
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Interleukin-6 receptor enhances early colonization of the murine omentum by upregulation of a mannose family receptor, LY75, in ovarian tumor cells
PV Giridhar, HM Funk, CA Gallo, A Porollo, CA Mercer, DR Plas, AF Drew |
Clinical & Experimental Metastasis | 2011 |
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Examining the influence of beta blockers and ACE inhibitors on the risk for breast cancer recurrence: results from the LACE cohort
PA Ganz, LA Habel, EK Weltzien, BJ Caan, SW Cole |
Breast Cancer Research and Treatment | 2011 |
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Evolution of β-blockers: from anti-anginal drugs to ligand-directed signalling
JG Baker, SJ Hill, RJ Summers |
Trends in Pharmacological Sciences | 2011 |
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Integrated genomics of ovarian xenograft tumor progression and chemotherapy response
A Stuckey, A Fischer, DH Miller, S Hillenmeyer, KK Kim, A Ritz, RK Singh, BJ Raphael, L Brard, AS Brodsky |
BMC Cancer | 2011 |
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Do stress responses promote leukemia progression? An animal study suggesting a role for epinephrine and prostaglandin-E2 through reduced NK activity
S Inbar, E Neeman, R Avraham, M Benish, E Rosenne, S Ben-Eliyahu |
PloS one | 2011 |
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Stress Influences on Anoikis
AK Sood, SK Lutgendorf |
Cancer prevention research (Philadelphia, Pa.) | 2011 |
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Biobehavioral Factors and Cancer Progression: Physiological Pathways and Mechanisms
SK Lutgendorf, AK Sood |
Psychosomatic medicine | 2011 |
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Molecular Pathways: Beta-Adrenergic Signaling in Cancer: Figure 1
SW Cole, AK Sood |
Clinical cancer research | 2011 |
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Epinephrine: A Short- and Long-Term Regulator of Stress and Development of Illness: A Potential New Role for Epinephrine in Stress
DL Wong, TC Tai, DC Wong-Faull, R Claycomb, EG Meloni, KM Myers, WA Carlezon, R Kvetnansky |
Cellular and Molecular Neurobiology | 2011 |
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Impact of stress on cancer metastasis
M Moreno-Smith, SK Lutgendorf, AK Sood |
Future oncology (London, England) | 2010 |
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Catecholamine up-regulates MMP-7 expression by activating AP-1 and STAT3 in gastric cancer
M Shi, D Liu, H Duan, C Han, B Wei, L Qian, C Chen, L Guo, M Hu, M Yu, L Song, B Shen, N Guo |
Molecular Cancer | 2010 |
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Social Isolation is associated with Elevated Tumor Norepinephrine in Ovarian Carcinoma Patients
SK Lutgendorf, K DeGeest, L Dahmoush, D Farley, F Penedo, D Bender, M Goodheart, TE Buekers, L Mendez, G Krueger, L Clevenger, DM Lubaroff, AK Sood, SW Cole |
Brain, Behavior, and Immunity | 2010 |
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Surgery as a double-edged sword: a clinically feasible approach to overcome the metastasis-promoting effects of surgery by blunting stress and prostaglandin responses
M Benish, S Ben-Eliyahu |
Cancers | 2010 |
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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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