584
Views
0
CrossRef citations to date
0
Altmetric
Review Article

Psychological stressors involved in the pathogenesis of premature ovarian insufficiency and potential intervention measures

, , , , , & show all
Article: 2360085 | Received 12 Dec 2023, Accepted 14 May 2024, Published online: 30 May 2024

References

  • Nash Z, Davies M. Premature ovarian insufficiency. BMJ. 2024;384:1. doi:10.1136/bmj-2023-077469.
  • Chon SJ, Umair Z, Yoon MS. Premature ovarian insufficiency: past, present, and future. Front Cell Dev Biol. 2021;9:672890. doi:10.3389/fcell.2021.672890.
  • Fu X, Zheng Q, Zhang N, et al. CUMS promotes the development of premature ovarian insufficiency mediated by nerve growth factor and its receptor in rats. Biomed Res Int. 2020;2020:1946853–14. doi:10.1155/2020/1946853.
  • Sun J, Fan Y, Guo Y, et al. Chronic and cumulative adverse life events in women with primary ovarian insufficiency: an exploratory qualitative study. Front Endocrinol. 2022;13:856044. doi:10.3389/fendo.2022.856044.
  • Lawson CC, Johnson CY, Chavarro JE, et al. Work schedule and physically demanding work in relation to menstrual function: the nurses’ health study 3. Scand J Work Environ Health. 2015;41(2):194–203. doi:10.5271/sjweh.3482.
  • Lim Y-M, Jeong K, Lee SR, et al. Association between premature ovarian insufficiency, early menopause, socioeconomic status in a nationally representative sample from korea. Maturitas. 2019;121:22–27. doi:10.1016/j.maturitas.2018.12.004.
  • Allshouse AA, Semple AL, Santoro NF. Evidence for prolonged and unique amenorrhea-related symptoms in women with premature ovarian failure/primary ovarian insufficiency. Menopause. 2015;22(2):166–174. doi:10.1097/GME.0000000000000286.
  • Xi W, Mao H, Cui Z, et al. Scream sound-induced chronic psychological stress results in diminished ovarian reserve in adult female rat. Endocrinology. 2022;163(6):42. doi:10.1210/endocr/bqac042.
  • Zhou P, Lian H-Y, Cui W, et al. Maternal-restraint stress increases oocyte aneuploidy by impairing metaphase I spindle assembly and reducing spindle assembly checkpoint proteins in mice. Biol Reprod. 2012;86(3):83.
  • Fu XY, et al. Effects of chronic unpredictable mild stress on ovarian reserve in female rats: feasibility analysis of a rat model of premature ovarian failure. Mol Med Rep. 2018;18(1):532–540.
  • Chrousos GP, Gold PW. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. Jama. 1992;267(9):1244–1252. doi:10.1001/jama.1992.03480090092034.
  • Allen AP, et al. Biological and psychological markers of stress in humans: focus on the trier social stress test. Neurosci Biobehav Rev. 2014;38:94–124.
  • Herman JP, et al. Regulation of the hypothalamic-pituitary-adrenocortical stress response. Compr Physiol. 2016;6(2):603–621.
  • Leistner C, Menke A. Hypothalamic-pituitary-adrenal axis and stress. Handb Clin Neurol. 2020;175:55–64.
  • Chang H-M, Wu H-C, Sun Z-G, et al. Neurotrophins and glial cell line-derived neurotrophic factor in the ovary: physiological and pathophysiological implications. Hum Reprod Update. 2019;25(2):224–242. doi:10.1093/humupd/dmy047.
  • James KA, Stromin JI, Steenkamp N, et al. Understanding the relationships between physiological and psychosocial stress, cortisol and cognition. Front Endocrinol. 2023;14:1085950. doi:10.3389/fendo.2023.1085950.
  • Sammad A, Luo H, Hu L, et al. Transcriptome reveals granulosa cells coping through redox, inflammatory and metabolic mechanisms under acute heat stress. Cells. 2022;11(9):1443. doi:10.3390/cells11091443.
  • Wang XF, et al. Biological mechanisms of premature ovarian failure caused by psychological stress based on support vector regression. Int J Clin Exp Med. 2015;8(11):21393–21399.
  • Morley P, Calaresu FR, Armstrong DT. Catecholamines inhibit steroidogenesis by cultured porcine thecal cells. FEBS Lett. 1990;275(1-2):70–72.
  • Sominsky L, Hodgson DM, McLaughlin EA, et al. Linking stress and infertility: a novel role for Ghrelin. Endocr Rev. 2017;38(5):432–467. doi:10.1210/er.2016-1133.
  • Lania A, Gianotti L, Gagliardi I, et al. Functional hypothalamic and drug-induced amenorrhea: an overview. J Endocrinol Invest. 2019;42(9):1001–1010. doi:10.1007/s40618-019-01013-w.
  • Zhao L-H, Cui X-Z, Yuan H-J, et al. Restraint stress inhibits mouse implantation: temporal window and the involvement of HB-EGF, estrogen and progesterone. PLoS One. 2013;8(11):e80472. doi:10.1371/journal.pone.0080472.
  • Wu JX, Lin S, Kong SB. Psychological stress and functional endometrial disorders: update of mechanism insights. Front Endocrinol. 2021;12:690255. doi:10.3389/fendo.2021.690255.
  • Choi J-H, Gilks CB, Auersperg N, et al. Immunolocalization of gonadotropin-releasing hormone (GnRH)-I, GnRH-II, and type I GnRH receptor during follicular development in the human ovary. J Clin Endocrinol Metab. 2006;91(11):4562–4570. doi:10.1210/jc.2006-1147.
  • Hong I-S, Klausen C, Cheung AP, et al. Gonadotropin-releasing hormone-I or -II interacts with IGF-I/Akt but not connexin 43 in human granulosa cell apoptosis. J Clin Endocrinol Metab. 2012;97(2):525–534. doi:10.1210/jc.2011-1229.
  • Cheung LW, Leung PC, Wong AS. Gonadotropin-releasing hormone promotes ovarian cancer cell invasiveness through c-Jun NH2-terminal kinase-mediated activation of matrix metalloproteinase (MMP)-2 and MMP-9. Cancer Res. 2006;66(22):10902–10910. doi:10.1158/0008-5472.CAN-06-2217.
  • Walters K, Wegorzewska IN, Chin Y-P, et al. Luteinizing hormone-releasing hormone I (LHRH-I) and its metabolite in peripheral tissues. Exp Biol Med (Maywood). 2008;233(2):123–130. doi:10.3181/0707-MR-201.
  • Wypior G, Jeschke U, Kurpisz M, et al. Expression of CRH, CRH-related peptide and CRH receptor in the ovary and potential CRH signalling pathways. J Reprod Immunol. 2011;90(1):67–73.
  • Chrousos GP. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N Engl J Med. 1995;332(20):1351–1362. doi:10.1056/NEJM199505183322008.
  • Kalantaridou SN, et al. Corticotropin-releasing hormone, stress and human reproduction: an update. J Reprod Immunol. 2010;85(1):33–39.
  • Zhou H, Chen A, Lu W. Corticotropin-releasing hormone reduces basal estradiol production in zebrafish follicular cells. Mol Cell Endocrinol. 2021;527:111222.
  • Yu J, Li X-F, Tsaneva-Atanasova K, et al. Chemogenetic activation of PVN CRH neurons disrupts the estrous cycle and LH dynamics in female mice. Front Endocrinol (Lausanne). 2023;14:1322662. doi:10.3389/fendo.2023.1322662.
  • Luo E, Stephens SBZ, Chaing S, et al. Corticosterone blocks Ovarian cyclicity and the LH surge via decreased kisspeptin neuron activation in female mice. Endocrinology. 2016;157(3):1187–1199. doi:10.1210/en.2015-1711.
  • Yuan H-J, Han X, He N, et al. Glucocorticoids impair oocyte developmental potential by triggering apoptosis of ovarian cells via activating the fas system. Sci Rep. 2016;6(1):24036. doi:10.1038/srep24036.
  • Andrews CJ, Yapura J, Potter MA, et al. Prolonged glucocorticoid administration affects oocyte morphology in cats (Felis catus) undergoing an ovarian stimulation protocol. Theriogenology. 2023;208:77–87. doi:10.1016/j.theriogenology.2023.05.024.
  • Yuan X-H, Yang B-Q, Hu Y, et al. Dexamethasone altered steroidogenesis and changed redox status of granulosa cells. Endocrine. 2014;47(2):639–647. doi:10.1007/s12020-014-0250-x.
  • Balasem Z, Salamat N, Mojiri-Forushani H. Using cell culture systems from the Persian Gulf arabian yellowfin sea bream, Acanthopagrus Arabicus, to assess the effects of dexamethasone on gonad and brain aromatase activity and steroid production. Toxicol in Vitro. 2024;97:105803. doi:10.1016/j.tiv.2024.105803.
  • Whirledge S, Cidlowski JA. Glucocorticoids and reproduction: traffic control on the road to reproduction. Trends Endocrinol Metab. 2017;28(6):399–415.
  • Bódis J, Papp S, Vermes I, et al. “Platelet-associated regulatory system (PARS)” with particular reference to female reproduction. J Ovarian Res. 2014;7(1):55. doi:10.1186/1757-2215-7-55.
  • Liu B, Liu Y, Li S, et al. BDNF promotes mouse follicular development and reverses ovarian aging by promoting cell proliferation. J Ovarian Res. 2023;16(1):83. doi:10.1186/s13048-023-01163-9.
  • Chen CH, et al. The role of the PI3K/Akt/mTOR pathway in glial scar formation following spinal cord injury. Exp Neurol. 2016;278:27–41.
  • Zheng X, Chen L, Chen T, et al. The mechanisms of BDNF promoting the proliferation of porcine follicular granulosa cells: role of miR-127 and involvement of the MAPK-ERK1/2 pathway. Animals. 2023;13(6):115. doi:10.3390/ani13061115.
  • Martinowich K, Lu B. Interaction between BDNF and serotonin: role in mood disorders. Neuropsychopharmacology. 2008;33(1):73–83. doi:10.1038/sj.npp.1301571.
  • Zheng W, et al. Functional roles of the phosphatidylinositol 3-kinases (PI3Ks) signaling in the mammalian ovary. Mol Cell Endocrinol. 2012;356(1-2):24–30.
  • Yan Z, Dai Y, Fu H, et al. Curcumin exerts a protective effect against premature ovarian failure in mice. J Mol Endocrinol. 2018;60(3):261–271. doi:10.1530/JME-17-0214.
  • Chaves RN, Alves AMCV, Lima LF, et al. Role of nerve growth factor (NGF) and its receptors in folliculogenesis. Zygote. 2013;21(2):187–197. doi:10.1017/S0967199412000111.
  • Romero C, Paredes A, Dissen GA, et al. Nerve growth factor induces the expression of functional FSH receptors in newly formed follicles of the rat ovary. Endocrinology. 2002;143(4):1485–1494. doi:10.1210/en.143.4.1485.
  • Dissen GA, Parrott JA, Skinner MK, et al. Direct effects of nerve growth factor on thecal cells from antral ovarian follicles. Endocrinology. 2000;141(12):4736–4750. doi:10.1210/en.141.12.4736.
  • Salas C, Julio-Pieper M, Valladares M, et al. Nerve growth factor-dependent activation of trkA receptors in the human ovary results in synthesis of follicle-stimulating hormone receptors and estrogen secretion. J Clin Endocrinol Metab. 2006;91(6):2396–2403. doi:10.1210/jc.2005-1925.
  • Kalantaridou SN, Makrigiannakis A, Zoumakis E, et al. Stress and the female reproductive system. J Reprod Immunol. 2004;62(1-2):61–68.
  • Zhai Q-Y, Wang J-J, Tian Y, et al. Review of psychological stress on oocyte and early embryonic development in female mice. Reprod Biol Endocrinol. 2020;18(1):101. doi:10.1186/s12958-020-00657-1.
  • Wu L-M, Hu M-H, Tong X-H, et al. Chronic unpredictable stress decreases expression of brain-derived neurotrophic factor (BDNF) in mouse ovaries: relationship to oocytes developmental potential. PLoS One. 2012;7(12):e52331. doi:10.1371/journal.pone.0052331.
  • Seifer DB. Brain-derived neurotrophic factor: a novel human ovarian follicular protein. J Clin Endocrinol Metab. 2002;87(2):655–659. doi:10.1210/jc.87.2.655.
  • Manni L, et al. Ovarian expression of alpha (1)- and beta (2)-adrenoceptors and p75 neurotrophin receptors in rats with steroid-induced polycystic ovaries. Auton Neurosci. 2005;118(1-2):79–87.
  • Saller S, Merz-Lange J, Raffael S, et al. Norepinephrine, active norepinephrine transporter, and norepinephrine-metabolism are involved in the generation of reactive oxygen species in human ovarian granulosa cells. Endocrinology. 2012;153(3):1472–1483. doi:10.1210/en.2011-1769.
  • Maggi R, et al. GnRH and GnRH receptors in the pathophysiology of the human female reproductive system. Hum Reprod Update. 2016;22(3):358–381.
  • Gidron Y, Russ K, Tissarchondou H, et al. The relation between psychological factors and DNA-damage: a critical review. Biol Psychol. 2006;72(3):291–304.
  • Black CN, Bot M, Révész D, et al. The association between three major physiological stress systems and oxidative DNA and lipid damage. Psychoneuroendocrinology. 2017;80:56–66. doi:10.1016/j.psyneuen.2017.03.003.
  • Sasaki H, Hamatani T, Kamijo S, et al. Impact of oxidative stress on age-associated decline in oocyte developmental competence. Front Endocrinol. 2019;10:811. doi:10.3389/fendo.2019.00811.
  • Schieber M, Chandel NS. ROS function in redox signaling and oxidative stress. Curr Biol. 2014;24(10):R453–62.
  • Tiwari M, Prasad S, Tripathi A, et al. Involvement of reactive oxygen species in meiotic cell cycle regulation and apoptosis in mammalian oocytes. ROS. 2016;1(2):99–106. doi:10.20455/ros.2016.817.
  • Coyle CH, et al. Mechanisms of H2O2-induced oxidative stress in endothelial cells. Free Radic Biol Med. 2006;40(12):2206–2213.
  • Agarwal A, et al. Redox considerations in female reproductive function and assisted reproduction: from molecular mechanisms to health implications. Antioxid Redox Signal. 2008;10(8):1375–1403.
  • Yang Z, Wenli Hong, K Zheng, et al. Chitosan oligosaccharides alleviate H(2)O(2)-stimulated granulosa cell damage via HIF-1α signaling pathway. Oxid Med Cell Longev. 2022:4247042.
  • Agarwal A, Sajal Gupta, Rakesh K Sharma, et al. Role of Oxidative Stress in Female Reproduction. 2005;3(1):1–21.
  • Chaube SK, Shrivastav TG, Prasad S, et al. Clomiphene Citrate Induces ROS-Mediated Apoptosis in Mammalian Oocytes. 2014.
  • Ebbesen SM, et al. Stressful life events are associated with a poor in-vitro fertilization (IVF) outcome: a prospective study. Hum Reprod. 2009;24(9):2173–2182.
  • Goncharova ND, Alla VS, Tatiana NB, et al. Correlation between activity of antioxidant enzymes and circadian rhythms of corticosteroids in Macaca mulatta monkeys of different age. 2006;41(8):778–783.
  • Nelson DH, Ruhmann-Wennhold A. Inhibition of leukocyte superoxide anion production by cortisol administration to normal subjects. J Clin Endocrinol Metab. 1978;46(4):702–705.
  • Ghatebi M, et al. Implications from early life stress on the development of mouse ovarian follicles: focus on oxidative stress. J Obstet Gynaecol Res. 2019;45(8):1506–1514.
  • ]Escoter-Torres L, Caratti G, Mechtidou A, et al. Fighting the fire: mechanisms of inflammatory gene regulation by the glucocorticoid receptor. Front Immunol. 2019;10:1859. doi:10.3389/fimmu.2019.01859.
  • ] Butler KS, et al. Coordinate regulation between expression levels of telomere-binding proteins and telomere length in breast carcinomas. Cancer Med. 2012;1(2):165–175.
  • Lin J, Epel E. Stress and telomere shortening: insights from cellular mechanisms. Ageing Res Rev. 2022;73:101507.
  • ] Wu W, Liu P, Li J. Necroptosis: an emerging form of programmed cell death. Crit Rev Oncol Hematol. 2012;82(3):249–258.
  • Liang B, Wei D-L, Cheng Y-N, et al. Restraint stress impairs oocyte developmental potential in mice: role of CRH-Induced apoptosis of ovarian Cells1. Restraint Stress Impairs Oocyte Developmental Potential in Mice. 2013;89(3):64. doi:10.1095/biolreprod.113.110619.
  • Li C-Y, Li Z-B, Kong Q-Q, et al. Restraint-induced corticotrophin-releasing hormone elevation triggers apoptosis of ovarian cells and impairs oocyte competence via activation of the fas/FasL system. Biol Reprod. 2018;99(4):828–837. doi:10.1093/biolre/ioy091.
  • Xiang Y, Jiang L, Gou J, et al. Chronic unpredictable mild stress-induced mouse ovarian insufficiency by interrupting lipid homeostasis in the ovary. Front Cell Dev Biol. 2022;10:933674. doi:10.3389/fcell.2022.933674.
  • Chen Y, et al. Copper exposure induces ovarian granulosa cell apoptosis by activating the caspase-dependent apoptosis signaling pathway and corresponding changes in microRNA patterns. Ecotoxicol Environ Saf. 2023;264:115414.
  • Ratts VS, Flaws JA, Kolp R, et al. Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology. 1995;136(8):3665–3668. doi:10.1210/en.136.8.3665.
  • Knudson CM, Tung KS, Tourtellotte WG, et al. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science. 1995;270(5233):96–99. doi:10.1126/science.270.5233.96.
  • Perez GI, Robles R, Knudson CM, et al. Prolongation of ovarian lifespan into advanced chronological age by Bax-deficiency. Nat Genet. 1999;21(2):200–203. doi:10.1038/5985.
  • Keremu A, et al. Research on the establishment of chronic stress-induced premature ovarian failure the rat model and effects of Chinese medicine Muniziqi treatment. Mol Reprod Dev. 2019;86(2):175–186.
  • Gau DM, Lesnock J, Krivak T, et al. Abstract LB-70: BRCA1 impacts ovarian cancer cell migration through modulating Pfn1 expression. Cancer Research. 2014;74(19_Supplement):LB-70–LB-70. doi:10.1158/1538-7445.AM2014-LB-70.
  • Proteomic analysis of follicular fluid from women with and without endometriosis. New Therapeutic Targets and Biomarkers. 2013;80(6):441–450.
  • Ding Z, Gau D, Deasy B, et al. Both actin and polyproline interactions of profilin-1 are required for migration, invasion and capillary morphogenesis of vascular endothelial cells. Exp Cell Res. 2009;315(17):2963–2973. doi:10.1016/j.yexcr.2009.07.004.
  • Tomasello L, et al. PFN1 and integrin-β1/mTOR axis involvement in cornea differentiation of fibroblast limbal stem cells. J Cell Mol Med. 2019;23(11):7210–7221.
  • Skare P, Karlsson R. Evidence for two interaction regions for phosphatidylinositol(4,5)-bisphosphate on mammalian profilin I. FEBS Lett. 2002;522(1-3):119–124. doi:10.1016/s0014-5793(02)02913-7.
  • Sathish K, et al. Phosphorylation of profilin regulates its interaction with actin and poly (L-proline). Cell Signal. 2004;16(5):589–596.
  • Pan X, et al. Bushen Jieyu tiaochong formula reduces apoptosis of granulosa cells via the PERK-ATF4-CHOP signaling pathway in a rat model of polycystic ovary syndrome with chronic stress. J Ethnopharmacol. 2022;292:114923.
  • Neri M, et al. Correlation between cardiac oxidative stress and myocardial pathology due to acute and chronic norepinephrine administration in rats. J Cell Mol Med. 2007;11(1):156–170.
  • Li M, et al. Rno-miR-128-3p promotes apoptosis in rat granulosa cells (GCs) induced by norepinephrine through Wilms tumor 1 (WT1). In Vitro Cell Dev Biol Anim. 2021;57(8):775–785.
  • Quezada M, et al. Smad7 is a transforming growth factor-beta-inducible mediator of apoptosis in granulosa cells. Fertil Steril. 2012;97(6):1452-9.e1-6.
  • Zhang L, Gao J, Cui S. miR-21 is involved in norepinephrine-mediated rat granulosa cell apoptosis by targeting SMAD7. J Mol Endocrinol. 2017;58(4):199–210. doi:10.1530/JME-16-0248.
  • Patel NJ, Chen MJ, Russo-Neustadt AA. Norepinephrine and nitric oxide promote cell survival signaling in hippocampal neurons. Eur J Pharmacol. 2010;633(1-3):1–9.
  • Hansen KR, Hodnett GM, Knowlton N, et al. Correlation of ovarian reserve tests with histologically determined primordial follicle number. Fertil Steril. 2011;95(1):170–175.
  • Jiao X, Meng T, Zhai Y, et al. Ovarian reserve markers in premature ovarian insufficiency: within different clinical stages and different etiologies. Front Endocrinol. 2021;12:601752. doi:10.3389/fendo.2021.601752.
  • Groome NP, Illingworth PJ, O’Brien M, et al. Measurement of dimeric inhibin B throughout the human menstrual cycle. J Clin Endocrinol Metab. 1996;81(4):1401–1405. doi:10.1210/jc.81.4.1401.
  • Klein NA, et al. Age-related analysis of inhibin A, inhibin B, and activin a relative to the intercycle monotropic follicle-stimulating hormone rise in normal ovulatory women. J Clin Endocrinol Metab. 2004;89(6):2977–2981.
  • Webber L, et al. ESHRE guideline: management of women with premature ovarian insufficiency. Hum Reprod. 2016;31(5):926–937.
  • Pandey AK, et al. Impact of stress on female reproductive health disorders: possible beneficial effects of shatavari (Asparagus racemosus). Biomed Pharmacother. 2018;103:46–49.
  • Hannibal KE, Bishop MD. Chronic stress, cortisol dysfunction, and pain: a psychoneuroendocrine rationale for stress management in pain rehabilitation. Phys Ther. 2014;94(12):1816–1825. doi:10.2522/ptj.20130597.
  • Schein RL, Koenig H. The Center for Epidemiological Studies-Depression (CES-D) scale: assessment of depression in the medically ill elderly. Int J Geriatric Psychiatry. 1997;12(4):436–446.
  • Piersma HL, Reaume WM, Boes JL. The brief symptom inventory (BSI) as an outcome measure for adult psychiatric inpatients. J Clin Psychol. 1994;50(4):555–563.
  • Haemmerli Keller K, Alder G, Loewer L, et al. Treatment-related psychological stress in different in vitro fertilization therapies with and without gonadotropin stimulation. Acta Obstet Gynecol Scand. 2018;97(3):269–276. doi:10.1111/aogs.13281.
  • The WHOQOL Group. Development of the World Health Organization WHOQOL-BREF quality of life assessment. Psychol Med. 1998; 28(3):551–558.
  • Reilly J. Premature menopause: a multidisciplinary approach whurr. J Health Psychol. 2001;6(5):606–608. doi:10.1177/135910530100600512.
  • Dragojevic-Dikic S, et al. An immunological insight into premature ovarian failure (POF). Autoimmun Rev. 2010;9(11):771–774.
  • Warne E, Oxlad M, Best T. Evaluating group psychological interventions for mental health in women with infertility undertaking fertility treatment: a systematic review and meta-Analysis. Health Psychol Rev. 2023;17(3):377–401.
  • Lupien SJ, Fiocco A, Wan N, et al. Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology. 2005;30(3):225–242. doi:10.1016/j.psyneuen.2004.08.003.
  • Santoft F, et al. Cognitive behaviour therapy for depression in primary care: systematic review and meta-analysis. Psychol Med. 2019;49(8):1266–1274.
  • Linde K, et al. Effectiveness of psychological treatments for depressive disorders in primary care: systematic review and meta-analysis. Ann Fam Med. 2015;13(1):56–68.
  • Cuijpers P, et al. The effects of fifteen evidence-supported therapies for adult depression: a meta-analytic review. Psychother Res. 2020;30(3):279–293.
  • Richards DA, et al. Cost and outcome of behavioural activation versus cognitive behavioural therapy for depression (COBRA): a randomised, controlled, non-inferiority trial. Lancet. 2016;388(10047):871–880.
  • Cuijpers P, Quero S, Dowrick C, et al. Psychological treatment of depression in primary care: recent developments. Curr Psychiatry Rep. 2019;21(12):129. doi:10.1007/s11920-019-1117-x.
  • Bahari K, Lorica JD. The effects of laughter therapy on mental health: an integrative literature review. MJN. 2019;10(03):55–61. doi:10.31674/mjn.2019.v10i03.008.
  • Fonzi L, Matteucci G, Bersani G. Laughter and depression: hypothesis of pathogenic and therapeutic correlation. Riv Psichiatr. 2010;45(1):1–6.
  • Boudoures AL, Chi M, Thompson A, et al. The effects of voluntary exercise on oocyte quality in a diet-induced obese murine model. Reproduction. 2016;151(3):261–270. doi:10.1530/REP-15-0419.
  • Safdar A, et al. Amelioration of premature aging in mtDNA mutator mouse by exercise: the interplay of oxidative stress, PGC-1α, p53, and DNA damage. A hypothesis. Curr Opin Genet Dev. 2016;38:127–132.
  • Safdar A, et al. Exercise-induced mitochondrial p53 repairs mtDNA mutations in mutator mice. Skelet Muscle. 2016;6:7.
  • Han B, Du G, Yang Y, et al. Relationships between physical activity, body image, BMI, depression and anxiety in Chinese college students during the COVID-19 pandemic. BMC Public Health. 2023;23(1):24. doi:10.1186/s12889-022-14917-9.
  • Aguiar AS, Stragier E, da Luz Scheffer DJr., et al. Effects of exercise on mitochondrial function, neuroplasticity and anxio-depressive behavior of mice. Neuroscience. 2014;271:56–63., doi:10.1016/j.neuroscience.2014.04.027.
  • Bansal Y, Kuhad A. Mitochondrial dysfunction in depression. Curr Neuropharmacol. 2016;14(6):610–618.
  • Clark A, Mach N. Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes. J Int Soc Sports Nutr. 2016;13:43.
  • Sun L, Sun Q, Qi J. Adult hippocampal neurogenesis: an important target associated with antidepressant effects of exercise. Rev Neurosci. 2017;28(7):693–703. doi:10.1515/revneuro-2016-0076.
  • Lopresti AL, Hood SD, Drummond PD. A review of lifestyle factors that contribute to important pathways associated with major depression: diet, sleep and exercise. J Affect Disord. 2013;148(1):12–27.
  • LeBleu VS, O’Connell JT, Gonzalez Herrera KN, et al. PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis. Nat Cell Biol. 2014;16(10):992–1003. doi:10.1038/ncb3039.
  • Messaoudi M, Lalonde R, Violle N, et al. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr. 2011;105(5):755–764. doi:10.1017/S0007114510004319.
  • Messaoudi M, Violle N, Bisson J-F, et al. Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers. Gut Microbes. 2011;2(4):256–261. doi:10.4161/gmic.2.4.16108.
  • Dantzer R, O’Connor JC, Freund GG, et al. From inflammation to sickness and depression: When the immune system subjugates the brain. Nat Rev Neurosci. 2008;9(1):46–56. doi:10.1038/nrn2297.
  • Gleeson M, Bishop NC, Stensel DJ, et al. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol. 2011;11(9):607–615. doi:10.1038/nri3041.