Positive Psychosocial Factors and Oxytocin in the Ovarian Tumor Microenvironment.
Journal
Psychosomatic medicine
ISSN: 1534-7796
Titre abrégé: Psychosom Med
Pays: United States
ID NLM: 0376505
Informations de publication
Date de publication:
01 06 2021
01 06 2021
Historique:
entrez:
3
6
2021
pubmed:
4
6
2021
medline:
21
10
2021
Statut:
ppublish
Résumé
Clinical ovarian cancer research shows relationships between psychosocial factors and disease-promoting aspects of the stress response (e.g., norepinephrine and cortisol). However, little is known about how psychosocial factors might relate to beneficial hormones in the ovarian tumor microenvironment. Here we examine relationships between psychosocial factors and tumor-associated oxytocin, a hormone linked to survival and antitumor processes in ovarian cancer. Patients with ovarian cancer (n = 96) completed assessments of positive psychosocial factors (social support, positive affect, and purpose in life) and distress (perceived stress and depression) at the time of surgery. Levels of oxytocin and interleukin (IL) 6 in ascites fluid were obtained during surgery and analyzed by enzyme-linked immunosorbent assay. Multiple regression analyses adjusting a priori for patient age and disease stage examined associations between psychosocial factors and ascites oxytocin. IL-6 was used as a covariate in secondary analyses to examine the potentially confounding effects of inflammation in these relationships. Higher levels of positive affect (β = 0.22, p = .034), purpose in life (β = 0.31, p = .021), and social nurturance (β = 0.24, p = .024) were all related to higher levels of tumor-associated oxytocin at the time of surgery. In contrast, we found no effects for distress or social attachment. Relationships between oxytocin, purpose in life, and social nurturance were independent of IL-6, whereas positive affect was no longer significant with IL-6 in the model. Tumor-associated oxytocin may be a previously uninvestigated link in the relationship between psychosocial factors and health in ovarian cancer. Future studies should examine causal mechanisms of relationships observed in this study.
Identifiants
pubmed: 34080583
doi: 10.1097/PSY.0000000000000935
pii: 00006842-202106000-00004
pmc: PMC8175871
mid: NIHMS1685219
doi:
Substances chimiques
Oxytocin
50-56-6
Hydrocortisone
WI4X0X7BPJ
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
417-422Subventions
Organisme : NCI NIH HHS
ID : R35 CA209904
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL116387
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM108540
Pays : United States
Organisme : NIA NIH HHS
ID : P30 AG017265
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA140933
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA086862
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA109298
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA193249
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA246540
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG043404
Pays : United States
Informations de copyright
Copyright © 2021 by the American Psychosomatic Society.
Références
Cole SW, Nagaraja AS, Lutgendorf SK, Green PA, Sood AK. Sympathetic nervous system regulation of the tumour microenvironment. Nat Rev Cancer 2015;15:563–72.
Bower JE, Shiao SL, Sullivan P, Lamkin DM, Atienza R, Mercado F, Arevalo J, Asher A, Ganz PA, Cole SW. Prometastatic molecular profiles in breast tumors from socially isolated women. JNCI Cancer Spectr 2018;2:pky029.
Lutgendorf SK, De Geest K, Bender D, Ahmed A, Goodheart MJ, Dahmoush L, Zimmerman MB, Penedo FJ, Lucci JA 3rd, Ganjei-Azar P, Thaker PH, Mendez L, Lubaroff DM, Slavich GM, Cole SW, Sood AK. Social influences on clinical outcomes of patients with ovarian cancer. J Clin Oncol 2012;30:2885–90.
Davis L, Slavich GM, Thaker PH, Goodheart MJ, Bender DP, Dahmoush L, Farley DM, Markon KE, Penedo FJ, Lubaroff DM, Cole SW, Sood AK, Lutgendorf SK. Eudaimonic well-being and tumor norepinephrine in patients with epithelial ovarian cancer. Cancer 2015;121:3543–50.
Cuneo MG, Schrepf A, Slavich GM, Thaker PH, Goodheart M, Bender D, Cole SW, Sood AK, Lutgendorf SK. Diurnal cortisol rhythms, fatigue and psychosocial factors in five-year survivors of ovarian cancer. Psychoneuroendocrinology 2017;84:139–42.
Ryff CD, Singer BH, Dienberg Love G. Positive health: connecting well-being with biology. Philos Trans R Soc Lond B Biol Sci 2004;359:1383–94.
Taylor SE, Klein LC, Lewis BP, Gruenewald TL, Gurung RA, Updegraff JA. Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol Rev 2000;107:411–29.
Uvnäs-Moberg K. Oxytocin may mediate the benefits of positive social interaction and emotions. Psychoneuroendocrinology 1998;23:819–35.
Gimpl G, Fahrenholz F. The oxytocin receptor system: structure, function, and regulation. Physiol Rev 2001;81:629–83.
Neumann ID, Wigger A, Torner L, Holsboer F, Landgraf R. Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: partial action within the paraventricular nucleus. J Neuroendocrinol 2000;12:235–43.
Smith AS, Wang Z. Hypothalamic oxytocin mediates social buffering of the stress response. Biol Psychiatry 2014;76:281–8.
Heinrichs M, Baumgartner T, Kirschbaum C, Ehlert U. Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol Psychiatry 2003;54:1389–98.
Karelina K, Stuller KA, Jarrett B, Zhang N, Wells J, Norman GJ, DeVries AC. Oxytocin mediates social neuroprotection after cerebral ischemia. Stroke 2011;42:3606–11.
Norman GJ, Karelina K, Morris JS, Zhang N, Cochran M, Courtney DeVries A. Social interaction prevents the development of depressive-like behavior post nerve injury in mice: a potential role for oxytocin. Psychosom Med 2010;72:519–26.
Engert V, Koester AM, Riepenhausen A, Singer T. Boosting recovery rather than buffering reactivity: higher stress-induced oxytocin secretion is associated with increased cortisol reactivity and faster vagal recovery after acute psychosocial stress. Psychoneuroendocrinology 2016;74:111–20.
Cuneo MG, Szeto A, Schrepf A, Kinner EM, Schachner BI, Ahmed R, Thaker PH, Goodheart M, Bender D, Cole SW, McCabe PM, Sood AK, Lutgendorf SK, Mendez AJ. Oxytocin in the tumor microenvironment is associated with lower inflammation and longer survival in advanced epithelial ovarian cancer patients. Psychoneuroendocrinology 2019;106:244–51.
Mankarious A, Dave F, Pados G, Tsolakidis D, Gidron Y, Pang Y, Thomas P, Hall M, Karteris E. The pro-social neurohormone oxytocin reverses the actions of the stress hormone cortisol in human ovarian carcinoma cells in vitro. Int J Oncol 2016;48:1805–14.
Morita T, Shibata K, Kikkawa F, Kajiyama H, Ino K, Mizutani S. Oxytocin inhibits the progression of human ovarian carcinoma cells in vitro and in vivo. Int J Cancer 2004;109:525–32.
Ji H, Liu N, Yin Y, Wang X, Chen X, Li J, Li J. Oxytocin inhibits ovarian cancer metastasis by repressing the expression of MMP-2 and VEGF. J Cancer 2018;9:1379–84.
Fuchs AR. Oxytocin and ovarian function. J Reprod Fertil Suppl 1988;36:39–47.
Nation D, Szeto A, Mendez AJ, Brooks LG, Zaias J, Herderick EE, Gonzales J, Noller CM, Schneiderman N, McCabe PM. Oxytocin attenuates atherosclerosis and adipose tissue inflammation in socially isolated ApoE−/− mice. Psychosom Med 2010;72:376–82.
Petersson M, Wiberg U, Lundeberg T, Uvnas-Moberg K. Oxytocin decreases carrageenan induced inflammation in rats. Peptides 2001;22:1479–84.
Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008;9:46–56.
Macciò A, Madeddu C. Inflammation and ovarian cancer. Cytokine 2012;58:133–47.
Ryff CD. Happiness is everything, or is it? Explorations on the meaning of psychological well-being. J Pers Soc Psychol 1989;57:1069–81.
Radloff L. The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Measur 1977;1:385–401.
Cohen S, Kamarck T, Mermelstein R. A global measure of perceived stress. J Health Soc Behav 1983;24:385–96.
Cutrona C, Russell D. The provisions of social relationships and adaptation to stress. Adv Pers Relat 1987;1:37–67.
Insel TR, Young LJ. The neurobiology of attachment. Nat Rev Neurosci 2001;2:129–36.
Macdonald K, Macdonald TM. The peptide that binds: a systematic review of oxytocin and its prosocial effects in humans. Harv Rev Psychiatry 2010;18:1–21.
Ryff CD. Psychological well-being revisited: advances in the science and practice of eudaimonia. Psychother Psychosom 2014;83:10–28.
Friedman EM, Ryff CD. Living well with medical comorbidities: a biopsychosocial perspective. J Gerontol B Psychol Sci Soc Sci 2012;67:535–44.
Szeto A, McCabe PM, Nation DA, Tabak BA, Rossetti MA, McCullough ME, Schneiderman N, Mendez AJ. Evaluation of enzyme immunoassay and radioimmunoassay methods for the measurement of plasma oxytocin. Psychosom Med 2011;73:393–400.
Song MK, Lin FC, Ward SE, Fine JP. Composite variables: when and how. Nurs Res 2013;62:45–9.
Costanzo ES, Lutgendorf SK, Sood AK, Anderson B, Sorosky J, Lubaroff DM. Psychosocial factors and interleukin-6 among women with advanced ovarian cancer. Cancer 2005;104:305–13.
Leng G, Sabatier N. Measuring oxytocin and vasopressin: bioassays, immunoassays and random numbers. J Neuroendocrinol 2016;28.
McCullough ME, Churchland PS, Mendez AJ. Problems with measuring peripheral oxytocin: can the data on oxytocin and human behavior be trusted? Neurosci Biobehav Rev 2013;37:1485–92.
Glei DA, Goldman N, Ryff CD, Lin YH, Weinstein M. Social relationships and inflammatory markers: an analysis of Taiwan and the U.S. Soc Sci Med 2012;74:1891–9.
Cohen J. Statistical Power Analysis for the Behavioral Sciences. New York: Academic Press; 2013.
Cohen S, Pressman SD. Positive affect and health. Curr Dir Psychol Sci 2006;15:122–5.
Chida Y, Steptoe A. Positive psychological well-being and mortality: a quantitative review of prospective observational studies. Psychosom Med 2008;70:741–56.
Steptoe A, Dockray S, Wardle J. Positive affect and psychobiological processes relevant to health. J Pers 2009;77:1747–76.
Lutgendorf SK, DeGeest K, Sung CY, Arevalo JM, Penedo F, Lucci J 3rd, Goodheart M, Lubaroff D, Farley DM, Sood AK, Cole SW. Depression, social support, and beta-adrenergic transcription control in human ovarian cancer. Brain Behav Immun 2009;23:176–83.
Lutgendorf SK, Penedo F, Goodheart MJ, Dahmoush L, Arevalo JMG, Thaker PH, Slavich GM, Sood AK, Cole SW. Epithelial-mesenchymal transition polarization in ovarian carcinomas from patients with high social isolation. Cancer 2020;126:4407–13.
Kamiya A, Hayama Y, Kato S, Shimomura A, Shimomura T, Irie K, Kaneko R, Yanagawa Y, Kobayashi K, Ochiya T. Genetic manipulation of autonomic nerve fiber innervation and activity and its effect on breast cancer progression. Nat Neurosci 2019;22:1289–305.
Van Cappellen P, Rice EL, Catalino LI, Fredrickson BL. Positive affective processes underlie positive health behaviour change. Psychol Health 2018;33:77–97.
Ironson G, Banerjee N, Fitch C, Krause N. Positive emotional well-being, health behaviors, and inflammation measured by C-reactive protein. Soc Sci Med 2018;197:235–43.
Alizadeh AM, Heydari Z, Rahimi M, Bazgir B, Shirvani H, Alipour S, Heidarian Y, Khalighfard S, Isanejad A. Oxytocin mediates the beneficial effects of the exercise training on breast cancer. Exp Physiol 2018;103:222–35.