Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-27T06:09:31.055Z Has data issue: false hasContentIssue false
  • English
  • Français

Social environment as a modulator of immunosenescence

Published online by Cambridge University Press:  01 August 2022

A. Garrido Open the ORCID record for A. Garrido [Opens in a new window] ,
I. Martínez de Toda ,
E. Díaz del Cerro ,
J. Félix ,
N. Ceprián ,
M. González-Sánchez  and
M. De la Fuente
A. Garrido*
Affiliation:
Department of Immunology and Oncology, National Centre for Biotechnology (CNB), Spanish Research Council (CSIC), Madrid, Spain
I. Martínez de Toda
Affiliation:
Department of Genetics, Physiology, and Microbiology (Physiology Unit), School of Biology, Complutense University of Madrid, Madrid, Spain Institute of Investigation of Hospital 12 de Octubre (i+12), Madrid, Spain
E. Díaz del Cerro
Affiliation:
Department of Genetics, Physiology, and Microbiology (Physiology Unit), School of Biology, Complutense University of Madrid, Madrid, Spain Institute of Investigation of Hospital 12 de Octubre (i+12), Madrid, Spain
J. Félix
Affiliation:
Department of Genetics, Physiology, and Microbiology (Physiology Unit), School of Biology, Complutense University of Madrid, Madrid, Spain Institute of Investigation of Hospital 12 de Octubre (i+12), Madrid, Spain
N. Ceprián
Affiliation:
Department of Genetics, Physiology, and Microbiology (Physiology Unit), School of Biology, Complutense University of Madrid, Madrid, Spain Institute of Investigation of Hospital 12 de Octubre (i+12), Madrid, Spain
M. González-Sánchez
Affiliation:
Department of Genetics, Physiology, and Microbiology (Physiology Unit), School of Biology, Complutense University of Madrid, Madrid, Spain Institute of Investigation of Hospital 12 de Octubre (i+12), Madrid, Spain
M. De la Fuente
Affiliation:
Department of Genetics, Physiology, and Microbiology (Physiology Unit), School of Biology, Complutense University of Madrid, Madrid, Spain Institute of Investigation of Hospital 12 de Octubre (i+12), Madrid, Spain
*
Author for correspondence: A. Garrido, E-mail: agarrido@cnb.csic.es
Get access Rights & Permissions [Opens in a new window]

Abstract

Immune system aging, a process known as immunosenescence, involves a striking rearrangement affecting all immune cells, resulting in an increased rate of infections and a major incidence of autoimmune diseases and cancer. Nonetheless, differences in how individuals of the same chronological age carry out this immunosenescence establishment and thus the aging rate have been reported. In the context of neuroimmunoendocrine communication and its role in the response to stress situations, growing evidence suggests that social environments profoundly influence all physiological responses, especially those linked to immunity. Accordingly, negative contexts (loneliness in humans/social isolation in rodents) were associated with immune impairments and decreased lifespan. However, positive social environments have been correlated with adequate immunity and increased lifespan. Therefore, the social context in which an individual lives is proposed as a decisive modulator of the immunosenescence process and, consequently, of the rate of aging. In this review, the most important findings regarding how different social environments (negative and positive) modulate immunosenescence and therefore the aging rate, as well as the role of stress responses, hormesis, and resilience in these environments will be explained. Finally, several possible molecular mechanisms underlying the effects of negative and positive environments on immunosenescence will be suggested.

Keywords

Aginghomeostatic systemsimmunosenescencelonelinesssocial environmentsocial strategystress response
Type
Review
Information
Expert Reviews in Molecular Medicine , Volume 24 , 2022 , e29
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

De la Fuente, M and Miquel, J (2009) An update of the oxidation-inflammation theory of aging. The involvement of the immune system in oxi-inflamm-aging. Current Pharmaceutical Design 15, 3003–3026.10.2174/138161209789058110CrossRefGoogle ScholarPubMed
De la Fuente, M (2018) Bio-psycho-social bridge: the psychoneuroimmune system in successful aging. In Fernández-Ballesteros, R, Benetos, A and Robie, JM (eds), Cambridge Handbook of Successful Aging. New York: Cambridge University Press, pp. 265–280.Google Scholar
Torday, JS (2015) Homeostasis as the mechanism of evolution. Biology (Basel) 4, 573–590.Google ScholarPubMed
De la Fuente, M (2021) The role of the microbiota-gut-brain axis in the health and illness condition: a focus on Alzheimer´s disease. Journal of Alzheimer's Disease 81, 1345–1360.10.3233/JAD-201587CrossRefGoogle ScholarPubMed
Martínez de Toda, I et al. (2021) The immunity clock. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 76, 1939–1945.10.1093/gerona/glab136CrossRefGoogle ScholarPubMed
Martínez de Toda, I et al. (2016) Immune function parameters as markers of biological age and predictors of longevity. Aging (Albany NY) 8, 3110–3119.10.18632/aging.101116CrossRefGoogle ScholarPubMed
Bauer, M and De la Fuente, M (2016) The role of oxidative and inflammatory stress and persistent viral infections in immunosenescence. Mechanisms of Ageing and Development 158, 27–37.10.1016/j.mad.2016.01.001CrossRefGoogle ScholarPubMed
Martínez de Toda, I et al. (2021) The role of immune cells in oxi-inflammaging. Cells 10, 2974.CrossRefGoogle Scholar
Martínez de Toda, I et al. (2019) Function, oxidative, and inflammatory stress parameters in immune cells as predictive markers of lifespan throughout aging. Oxidative Medicine and Cellular Longevity 2, 4574276.Google Scholar
De la Fuente, M (2018) Oxidation and inflammation in the immune and nervous systems, a link between aging and anxiety. In Fulop, T, Franceschi, C, Hirokawa, K and Pawelec, G (eds), Handbook of Immunosenescence. Cham: Springer Nature, pp. 1–31.Google Scholar
De la Fuente, M et al. (2011) Strategies to improve the functions and redox state of the immune system in aged subjects. Current Pharmaceutical Design 17, 3966–3993.10.2174/138161211798764861CrossRefGoogle ScholarPubMed
Henry, JP and Wang, S (1998) Effects of early stress on adult affiliative behaviors. Psychoneuroendocrinology 23, 863–875.10.1016/S0306-4530(98)00058-4CrossRefGoogle Scholar
Sayed, N et al. (2021) An inflammatory aging clock (iAge) based on deep learning tracks multimorbidity, immunosenescence, frailty and cardiovascular aging. Nature Aging 1, 598–615.10.1038/s43587-021-00082-yCrossRefGoogle ScholarPubMed
Mariotti, A (2015) The effects of chronic stress on health: new insights into the molecular mechanisms of brain-body communication. Future Science Oa 1, FSO23.10.4155/fso.15.21CrossRefGoogle ScholarPubMed
Martínez de Toda, I et al. (2019) High perceived stress in women is linked to oxidation, inflammation and immunosenescence. Biogerontology 20, 823–835.10.1007/s10522-019-09829-yCrossRefGoogle ScholarPubMed
Rattan, SI (2014) Aging is not a disease: implications for intervention. Aging and Disease 5, 196–202.Google Scholar
Kirkland, JL, Stout, MB and Sierra, F (2016) Resilience in aging mice. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 71, 1407–1414.10.1093/gerona/glw086CrossRefGoogle ScholarPubMed
Ukraintseva, S, Yashin, AI and Arbeev, KG (2016) Resilience versus robustness in aging. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 71, 1533–1534.10.1093/gerona/glw083CrossRefGoogle Scholar
Hadley, EC, Kuchel, GA and Newman, AB (2017) Report: nIA workshop on measures of physiologic resiliencies in human aging. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 72, 980–990.10.1093/gerona/glx015CrossRefGoogle ScholarPubMed
Hadley, EC et al. (2018) Corrigendum to: report: NIA workshop on measures of physiologic resiliencies in human aging. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 73, 995.10.1093/gerona/glx172CrossRefGoogle ScholarPubMed
Arbeev, KG et al. (2019) Physiological dysregulation as a promising measure of robustness and resilience in studies of aging and a new indicator of preclinical disease. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 74, 462–468.10.1093/gerona/gly136CrossRefGoogle Scholar
Schnell, S et al. (2010) The 1-year mortality of patients treated in a hip fracture program for elders. Geriatric Orthopaedic Surgery & Rehabilitation 1, 6–14.10.1177/2151458510378105CrossRefGoogle Scholar
Lin, JC-F et al. (2014) Mortality and complications of hip fracture in young adults: a nationwide population-based cohort study. BMC Musculoskeletal Disorders 15, 362.CrossRefGoogle ScholarPubMed
Ukraintseva, S et al. (2021) Decline in biological resilience as key manifestation of aging: potential mechanisms and role in health and longevity. Mechanisms of Ageing and Development 194, 111418.CrossRefGoogle ScholarPubMed
Rattan, SI (2008) Hormesis in aging. Ageing Research Reviews 7, 63–78.10.1016/j.arr.2007.03.002CrossRefGoogle Scholar
Calabrese, EJ (2018) Hormesis: path and progression to significance. International Journal of Molecular Sciences 19, 2871.CrossRefGoogle ScholarPubMed
Dhabhar, FS (2018) The short-term stress response – mother nature's mechanism for enhancing protection and performance under conditions of threat, challenge, and opportunity. Frontiers in Neuroendocrinology 49, 175–192.CrossRefGoogle ScholarPubMed
Southwick, SM et al. (2014) Resilience definitions, theory, and challenges: interdisciplinary perspectives. European Journal of Psychotraumatology 5, 25338.CrossRefGoogle ScholarPubMed
Gee, DG and Casey, BJ (2015) The impact of developmental timing for stress and recovery. Neurobiology of Stress 1, 184–194.CrossRefGoogle ScholarPubMed
VanTieghem, MR and Tottenham, N (2018) Neurobiological programming of early life stress: functional development of amygdala-prefrontal circuitry and vulnerability for stress-related psychopathology. Current Topics in Behavioral Neurosciences 38, 117–136.10.1007/7854_2016_42CrossRefGoogle ScholarPubMed
Hobfoll, SE et al. (2011) The limits of resilience: distress following chronic political violence among Palestinians. Social Science & Medicine 72, 1400–1408.CrossRefGoogle ScholarPubMed
Burns, SB et al. (2018) Plasticity of the epigenome during early-life stress. Seminars in Cell & Developmental Biology 77, 115–132.CrossRefGoogle ScholarPubMed
Kessler, RC et al. (2012) The importance of secondary trauma exposure for post-disaster mental disorder. Epidemiology and Psychiatric Sciences 21, 35–45.CrossRefGoogle ScholarPubMed
Green, JG et al. (2010) Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: associations with first onset of DSM-IV disorders. Archives of General Psychiatry 67, 113–123.CrossRefGoogle ScholarPubMed
Feder, A et al. (2019) The biology of human resilience: opportunities for enhancing resilience across the life span. Biological Psychiatry 86, 443–453.10.1016/j.biopsych.2019.07.012CrossRefGoogle ScholarPubMed
Cohen, S, Gianaros, PJ and Manuck, SB (2016) A stage model of stress and disease. Perspectives on Psychological Science 11, 456–463.CrossRefGoogle ScholarPubMed
Liu, H et al. (2018) Biological and psychological perspectives of resilience: is it possible to improve stress resistance? Frontiers in Human Neuroscience 12, 326.CrossRefGoogle ScholarPubMed
Snow-Turek, AL, Norris, MP and Tan, G (1996) Active and passive coping strategies in chronic pain patients. Pain 64, 455–462.10.1016/0304-3959(95)00190-5CrossRefGoogle ScholarPubMed
Hanton, S, Neil, R and Evans, L (2013) Hardiness and anxiety interpretation: an investigation into coping usage and effectiveness. European Journal of Sport Science 13, 96–104.10.1080/17461391.2011.635810CrossRefGoogle Scholar
Warner, LM et al. (2012) Health-specific optimism mediates between objective and perceived physical functioning in older adults. Journal of Behavioral Medicine 35, 400–406.10.1007/s10865-011-9368-yCrossRefGoogle ScholarPubMed
Maren, S (2008) Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats. European Journal of Neuroscience 28, 1661–1666.CrossRefGoogle ScholarPubMed
Farchi, M and Gidron, Y (2010) The effects of “psychological inoculation” versus ventilation on the mental resilience of Israeli citizens under continuous war stress. The Journal of Nervous and Mental Disease 198, 382–384.CrossRefGoogle ScholarPubMed
Troy, AS et al. (2010) Seeing the silver lining: cognitive reappraisal ability moderates the relationship between stress and depressive symptoms. Emotion (Washington, D.C.) 10, 783–795.CrossRefGoogle ScholarPubMed
Staub, E and Vollhardt, J (2008) Altruism born of suffering: the roots of caring and helping after victimization and other trauma. The American Journal of Orthopsychiatry 78, 267–280.CrossRefGoogle ScholarPubMed
Ozbay, F et al. (2008) Social support and resilience to stress across the life span: a neurobiologic framework. Current Psychiatry Reports 10, 304–310.10.1007/s11920-008-0049-7CrossRefGoogle ScholarPubMed
Cai, W-P et al. (2017) Relationship between cognitive emotion regulation, social support, resilience and acute stress responses in Chinese soldiers: exploring multiple mediation model. Psychiatry Research 256, 71–78.CrossRefGoogle ScholarPubMed
Armstrong, MI, Birnie-Lefcovitch, S and Ungar, MT (2005) Pathways between social support, family wellbeing, quality of parenting, and child resilience: what we know. Journal of Child and Family Studies 14, 269–281.10.1007/s10826-005-5054-4CrossRefGoogle Scholar
Conger, RD and Conger, KJ (2002) Resilience in Midwestern families: selected findings from the first decade of a prospective, longitudinal study. Journal of Marriage and Family 64, 361–373.10.1111/j.1741-3737.2002.00361.xCrossRefGoogle Scholar
Stansfeld, SA et al. (1997) Work and psychiatric disorder in the Whitehall II Study. Journal of Psychosomatic Research 43, 73–81.CrossRefGoogle ScholarPubMed
Oxman, TE and Hull, JG (2001) Social support and treatment response in older depressed primary care patients. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 56, P35–P45.Google ScholarPubMed
Johnson, DR et al. (1997) The impact of the homecoming reception on the development of posttraumatic stress disorder. The West Haven Homecoming Stress Scale (WHHSS). Journal of Traumatic Stress 10, 259–277.CrossRefGoogle Scholar
Cruces, J et al. (2014) The effect of psychological stress and social isolation on neuroimmunoendocrine communication. Current Pharmaceutical Design 20, 4608–4628.10.2174/1381612820666140130205822CrossRefGoogle ScholarPubMed
Dantzer, R et al. (2018) Resilience and immunity. Brain, Behavior, and Immunity 74, 28–42.CrossRefGoogle ScholarPubMed
Wright, CE et al. (2005) Acute infammation and negative mood: mediation by cytokine activation. Brain, Behavior, and Immunity 19, 345–350.10.1016/j.bbi.2004.10.003CrossRefGoogle Scholar
Janicki-Deverts, D et al. (2007) Infection-induced proinflammatory cytokines are associated with decreases in positive affect, but not increases in negative affect. Brain, Behavior, and Immunity 21, 301–307.CrossRefGoogle Scholar
Seeman, TE and Crimmins, (2001) Social environment effects on health and aging: integrating epidemiologic and demographic approaches and perspectives. Annals of the New York Academy of Sciences 954, 88–117.CrossRefGoogle Scholar
Wahl, H-W and Weisman, (2003) Environmental gerontology at the beginning of the new millennium: reflection on its historical, empirical, and theoretical development. The Gerontologist 43, 616–627.CrossRefGoogle Scholar
Avitsur, R et al. (2009) Social interactions, stress, and immunity. Immunology and Allergy Clinics of North America 29, 285–293.CrossRefGoogle Scholar
Cacioppo, JT et al. (2015) The neuroendocrinology of social isolation. Annual Review of Psychology 66, 733–767.CrossRefGoogle ScholarPubMed
Cacioppo, JT and Hawkley, LC (2003) Social isolation and health, with an emphasis on underlying mechanisms. Perspectives in Biology and Medicine 46, S39–S52.CrossRefGoogle ScholarPubMed
Budiu, RA et al. (2017) Restraint and social isolation stressors differentially regulate adaptive immunity and tumor angiogenesis in a breast cancer mouse model. Journal of Cancer Research and Clinical Oncology 6, 12–24.Google Scholar
Cacioppo, JT et al. (2011) Social isolation. Annals of the New York Academy of Sciences 1231, 17–22.CrossRefGoogle ScholarPubMed
Menec, VH et al. (2020) Examining social isolation and loneliness in combination in relation to social support and psychological distress using Canadian Longitudinal Study of Aging (CLSA) data. PLoS One 15, e0230673.CrossRefGoogle ScholarPubMed
Hsu, HC (2020) Typologies of loneliness, isolation and living alone Are associated with psychological well-being among older adults in Taipei: a cross-sectional study. International Journal of Environmental Research and Public Health 17, 9181.CrossRefGoogle ScholarPubMed
Naliboff, BD et al. (1991) Immunological changes in young and old adults during brief laboratory stress. Psychosomatic Medicine 53, 121–132.CrossRefGoogle Scholar
Segerstrom, SC and Miller, GE (2004) Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychological Bulletin 130, 601–630.CrossRefGoogle ScholarPubMed
Gouin, JP, Hantsoo, L and Kiecolt-Glaser, JK (2008) Immune dysregulation and chronic stress among older adults: a review. Neuroimmunomodulation 15, 251–259.CrossRefGoogle ScholarPubMed
Cruces, J et al. (2014) A higher anxiety state in old rats after social isolation is associated to an impairment of the immune response. Journal of Neuroimmunology 277, 18–25.CrossRefGoogle Scholar
Bailey, MT et al. (2007) Repeated social defeat increases the bactericidal activity of splenic macrophages through a toll-like receptor-dependent pathway. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 293, R1180–R1190.CrossRefGoogle ScholarPubMed
Khanfer, R et al. (2010) Altered human neutrophil function in response to acute psychological stress. Psychosomatic Medicine 72, 636–640.CrossRefGoogle ScholarPubMed
Kuebler, U et al. (2013) Acute stress reduces wound-induced activation of microbicidal potential of ex vivo isolated human monocyte-derived macrophages. PLoS One 8, e55875.CrossRefGoogle ScholarPubMed
Cohen, S, Tyrrel, DA and Smith, AP (1991) Psychological stress in humans and susceptibility to the common cold. The New England Journal of Medicine 325, 606–612.CrossRefGoogle ScholarPubMed
Petrie, KJ et al. (1995) Disclosure of trauma and immune response to a hepatitis B vaccination program. Journal of Consulting and Clinical Psychology 63, 787–792.CrossRefGoogle ScholarPubMed
Vedhara, K et al. (1999) Chronic stress in elderly careers of dementia patients and antibody response to influenza vaccination. Lancet (London, England) 353, 627–631.10.1016/S0140-6736(98)06098-XCrossRefGoogle Scholar
Glaser, R et al. (2000) Chronic stress modulates the immune response to a pneumococcal pneumonia vaccine. Psychosomatic Medicine 62, 804–807.CrossRefGoogle ScholarPubMed
Wu, H et al. (1999) Chronic stress associated with spousal care giving of patients with Alzheimer's dementia is associated with down regulation of B-lymphocyte GH mRNA. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 54, M212–M215.CrossRefGoogle Scholar
Glaser, R et al. (1987) Stress-related immune supression: health implications. Brain, Behavior, and Immunity 1, 7–20.CrossRefGoogle Scholar
Glaser, R and Kiecolt-Glaser, JK (1997) Chronic stress modulates the virus-specific immune response to latent herpes simplex virus type-1. Annals of Behavioral Medicine 19, 78–82.CrossRefGoogle ScholarPubMed
Glaser, R et al. (2001) Evidence for a shift in the Th-1 to Th-2 cytokine response associated with chronic stress and aging. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 56, M477–M482.10.1093/gerona/56.8.M477CrossRefGoogle ScholarPubMed
Dimsdale, J (2008) Psychological stress and cardiovascular disease. Journal of the American College of Cardiology 51, 1237–1246.CrossRefGoogle ScholarPubMed
Bartrop, RW et al. (1977) Depressed lymphocyte function after bereavement. Lancet (London, England) 1, 834–836.CrossRefGoogle ScholarPubMed
Delahanty, DL et al. (1996) Time course of natural killer cell activity and lymphocyte proliferation in response to two acute stressors in healthy men. Health Psychology 15, 48–55.CrossRefGoogle ScholarPubMed
Marshall, GD et al. (1998) Cytokine dysregulation associated with exam stress in healthy medical students. Brain, Behavior, and Immunity 12, 297–307.CrossRefGoogle ScholarPubMed
House, JS, Landis, KR and Umberson, D (1988) Social relationships and health. Science (New York, N.Y.) 241, 540–545.CrossRefGoogle ScholarPubMed
Holt-Lunstad, J, Smith, TB and Layton, JB (2010) Social relationships and mortality risk: a meta-analytic review. PLoS Medicine 7, e1000316.CrossRefGoogle ScholarPubMed
Pantell, M et al. (2013) Social isolation: a predictor of mortality comparable to traditional risk factors. American Journal of Public Health 11, 2056–2062.CrossRefGoogle Scholar
Chovatiya, R and Mdezhitov, R (2014) Stress, inflammation, and defense of homeostasis. Molecular Cell 54, 281–288.CrossRefGoogle ScholarPubMed
Garrido, A et al. (2019) Oxidative-inflammatory stress in immune cells from adult mice with premature aging. International Journal of Molecular Sciences 20, 769.CrossRefGoogle ScholarPubMed
Kearns, SM and Creaven, AM (2017) Individual differences in positive and negative emotion regulation: which strategies explain variability in loneliness? Personality and Mental Health 11, 64–74.CrossRefGoogle ScholarPubMed
Pietrabissa, G and Simpson, SG (2020) Psychological consequences of social isolation during COVID-19 outbreak. Frontiers in Psychology 11, 2201.CrossRefGoogle ScholarPubMed
Holt-Lunstad, J and Perissinotto, CM (2022) Isolation in the time of COVID: what is the true cost, and how will we know? American Journal of Health Promotion 36, 380–382.Google ScholarPubMed
Smith, AS and Wang, Z (2012) Salubrious effects of oxytocin on social stress-induced deficits. Hormones and Behavior 61, 320–330.CrossRefGoogle ScholarPubMed
Alves, GJ et al. (2006) Cohabitation with a sick cage mate: effects on noradrenaline turnover and neutrophil activity. Journal of Neuroscience Research 56, 172–179.CrossRefGoogle ScholarPubMed
Morgullis, MSFA et al. (2004) Cohabitation with a sick cage mate: consequences on behavior and on ehrlich tumor growth. Neuroimmunomodulation 11, 49–57.CrossRefGoogle Scholar
Alves, GJ et al. (2010) Odor cues from tumor-bearing mice induces neuroimmune changes. Behavioural Brain Research 214, 357–367.CrossRefGoogle ScholarPubMed
Alves, GJ, Ribeiro, A and Palermo-Neto, J (2012) The neuroimmune changes induced by cohabitation with an Ehrlich tumor-bearing cage mate rele on olfactory information. Brain, Behavior, and Immunity 26, 32–39.CrossRefGoogle Scholar
Palermo-Neto, J and Alves, GJ (2014) Neuroimmune interactions and psychological stress induced by cohabitation with a sick partner: a review. Current Pharmaceutical Design 20, 4629–4641.CrossRefGoogle ScholarPubMed
Tomiyoshi, MY et al. (2009) Cohabitation with a B16F10 melanoma-bearer cage mate influences behavior and dendritic cell phenotype in mice. Brain, Behavior, and Immunity 23, 558–567.CrossRefGoogle ScholarPubMed
Machado, TRM et al. (2017) Cohabitation with an Ehrlich tumor-bearing cagemate induces immune but not behavioral canges in male mice. Physiology & Behavior 169, 82–89.10.1016/j.physbeh.2016.11.022CrossRefGoogle ScholarPubMed
Hamasato, EK et al. (2014) Cohabitation with a sick partner increases allergic lung inflammatory response in mice. Brain, Behavior, and Immunity 42, 109–117.CrossRefGoogle ScholarPubMed
Almeida, DM et al. (2005) Do daily stress processes account for socioeconomic health disparities? The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 60, 34–39.Google ScholarPubMed
Birditt, KS, Fingerman, KL and Almeida, DM (2005) Age differences in exposure and reactions to interpersonal tensions: a daily diary study. Psychology and Aging 20, 330–340.CrossRefGoogle ScholarPubMed
Birditt, KS et al. (2020) Daily interpersonal tensions and well-being among older adults: the role of emotion regulation strategies. Psychology and Aging 35, 578–590.CrossRefGoogle ScholarPubMed
Giordano, R et al. (2005) Hypothalamus-pituitary-adrenal hyperactivity in human aging is partially refractory to stimulation by mineralocorticoid receptor blockade. The Journal of Clinical Endocrinology and Metabolism 90, 5656–5662.CrossRefGoogle ScholarPubMed
Majnaric, LT et al. (2021) Low psychological resilience in older individuals: an association with increased inflammation, oxidative stress and the presence of chronic medical conditions. International Journal of Molecular Sciences 22, 8970.CrossRefGoogle ScholarPubMed
Carroll, JE et al. (2013) Low social support is associated with shorter leukocyte telomere length in late life: multi-ethnic study of atherosclerosis. Psychosomatic Medicine 75, 171–177.CrossRefGoogle ScholarPubMed
Pressman, SD et al. (2005) Loneliness, social network size, and immune response to influenza vaccination in college freshmen. Health Psychology 24, 297–306.CrossRefGoogle ScholarPubMed
Cole, SW et al. (2007) Social regulation of gene expression in human leukocytes. Genome Biology 8, R189.CrossRefGoogle ScholarPubMed
Garrido, A et al. (2018) Improvements in behavior and immune function and increased life span of old mice cohabiting with adult animals. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 73, 873–881.CrossRefGoogle ScholarPubMed
Barth, E et al. (2019) Conserved aging-related signatures of senescence and inflammation in different tissues and species. Aging (Albany NY) 11, 8556–8572.CrossRefGoogle ScholarPubMed
Martínez de Toda, I et al. (2020) Redox parameters as markers of the rate of aging and predictors of life span. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 75, 613–620.Google ScholarPubMed
Guayerbas, N et al. (2002) Relation of behaviour and macrophage function to life span in a murine model of premature immunosenescence. Behavioural Brain Research 134, 41–48.CrossRefGoogle Scholar
Guayerbas, N and De la Fuente, M (2003) An impairment of phagocytic function is linked to a shorter life span in two strains of prematurely aging mice. Developmental & Comparative Immunology 27, 339–350.CrossRefGoogle ScholarPubMed
Viveros, MP et al. (2007) A model of premature aging in mice based on altered stress-related behavioral response and immunosenescence. Neuroimmunomodulation 14, 157–162.CrossRefGoogle Scholar
Garrido, A et al. (2019) Social environment improves immune function and redox state in several organs from prematurely aging female mice and increases their lifespan. Biogerontology 20, 49–69.CrossRefGoogle ScholarPubMed
Garrido, A et al. (2020) The ratio of prematurely aging to non-prematurely aging mice cohabiting, conditions their behavior, immunity and lifespan. Journal of Neuroimmunology 343, 577240.CrossRefGoogle ScholarPubMed
Garrido, A et al. (2018) Premature aging in behavior and immune functions in tyrosine hydroxylase haploinsufficient female mice. A longitudinal study. Brain, Behavior, and Immunity 69, 440–455.CrossRefGoogle ScholarPubMed
Garrido, A et al. (2021) Social environment ameliorates Behavioral and immune impairments in tyrosine hydroxylase haploinsufficient female mice. Journal of Neuroimmune Pharmacology 16, 548–566.10.1007/s11481-020-09947-2CrossRefGoogle ScholarPubMed
Díaz-Del Cerro, E et al. (2022) A short social interaction between adult and old mice improves the homeostatic systems and increases healthy longevity. Experimental Gerontology 158, 111653.CrossRefGoogle Scholar
Carr, EJ et al. (2016) The cellular composition of the human immune system is shaped by age and cohabitation. Nature Immunology 17, 461–468.CrossRefGoogle ScholarPubMed
Díaz Del Cerro, E, Félix, J and De La Fuente, M (2022) Prematurely aging female mice improve their behavioural response, immunity, redox state, and lifespan after a short social interaction with non-prematurely aging mice. Biogerontology 23, 307–324.CrossRefGoogle Scholar
Heinrichs, M et al. (2003) Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biological Psychiatry 54, 1389–1398.CrossRefGoogle ScholarPubMed
Maulik, PK, Eaton, WW and Bradshaw, CP (2010) The effect of social networks and social support on common mental disorders following specific late events. Acta Psychiatrica Scandinavica 122, 118–128.10.1111/j.1600-0447.2009.1511.xCrossRefGoogle Scholar
Karelina, K and DeVries, AC (2010) Modeling social influences on human health. Psychosomatic Medicine 73, 67–74.CrossRefGoogle ScholarPubMed
Zhang, Z and Tumin, D (2020) Expected social support and recovery of functional status after heart surgery. Disability and Rehabilitation 42, 1167–1172.CrossRefGoogle ScholarPubMed
Cohen, S et al. (2015) Does hugging provide stress-buffering social support? A study of susceptibility to upper respiratory infection and illness. Psychological Science 26, 135–147.CrossRefGoogle ScholarPubMed
Cohen, S (1988) Psychosocial models of the role of social support in the etiology of physical disease. Health Psychology 7, 269–297.CrossRefGoogle ScholarPubMed
Cohen, S et al. (1992) Chronic social stress, affiliation, and cellular immune response in nonhuman primates. Psychological Science 3, 301–304.CrossRefGoogle Scholar
Mesik, L et al. (2019) Sensory- and motor-related responses of layer 1 neurons in the mouse visual cortex. Journal of Neuroscience 39, 10060–10070.CrossRefGoogle ScholarPubMed
Patel, RC and Larson, J (2009) Impaired olfactory discrimination learning and decreased olfactory sensitivity in aged C57Bl/6 mice. Neurobiology of Aging 30, 829–837.CrossRefGoogle ScholarPubMed
Knutson, B, Burgdorf, J and Panksepp, J (2002) Ultrasonic vocalizations as indices of affective states in rats. Psychological Bulletin 128, 961–977.CrossRefGoogle ScholarPubMed
McGlone, F, Wessberg, J and Olausson, H (2014) Discriminative and affective touch: sensing and feeling. Neuron 82, 737–755.CrossRefGoogle ScholarPubMed
Field, T (2010) Touch for socioemotional and physical well-being. A review. Developmental Review 30, 367–383.CrossRefGoogle Scholar
Lagercrantz, H and Changeux, J-P (2009) The emergence of human consciousness: from fetal to neonatal life. Pediatric Research 65, 255–260.CrossRefGoogle ScholarPubMed
Bellieni, CV et al. (2007) Sensorial saturation for neonatal analgesia. The Clinical Journal of Pain 23, 219–221.CrossRefGoogle ScholarPubMed
Ferber, SG and Makhoul, IR (2008) Neurobehavioural assessment of skin-to-skin effects on reaction to pain in preterm infants: a randomized, controlled within-subject trial. Acta Paediatrica 97, 171–176.CrossRefGoogle ScholarPubMed
Cooijmans, KHM et al. (2017) Effectiveness of skin-to-skin contact versus care-as-usual in mothers and their full-term infants: study protocol for a parallel-group randomized controlled trial. BMC Pediatrics 17, 154.CrossRefGoogle ScholarPubMed
MacLean, K (2003) The impact of institutionalization on child development. Development and Psychopathology 15, 853–884.CrossRefGoogle ScholarPubMed
Nelson, K (2007) Development of extended memory. Journal of Physiology Paris 101, 223–229.CrossRefGoogle ScholarPubMed
Christenfeld, N and Gerin, W (2000) Social support and cardiovascular reactivity. Biomedicine & Pharmacotherapy 54, 251–257.CrossRefGoogle ScholarPubMed
Grewen, KM et al. (2003) Warm partner contact is related to lower cardiovascular reactivity. Behavioral Medicine 29, 123–130.CrossRefGoogle ScholarPubMed
Vaidis, DCF and Halimi-Falkowicz, SGM (2008) Increasing compliance with a request: two touches are more effective than one. Psychological Reports 103, 88–92.CrossRefGoogle ScholarPubMed
Finch, TL et al. (2014) Making sense of a cognitive behavioural therapy intervention for fear of falling: qualitative study of intervention development. BMC Health Services Research 14, 436.CrossRefGoogle ScholarPubMed
Celebioglu, A et al. (2015) Effects of massage therapy on pain and anxiety arising from intrathecal therapy of bone marrow aspiration in children with cancer. International Journal of Nursing Practice 21, 797–804.CrossRefGoogle ScholarPubMed
Papathanassoglou, ED and Mpouzika, MD (2012) Critical care in the era of global economic crisis: a nursing ethics perspective. Nursing in Critical Care 17, 275–278.CrossRefGoogle ScholarPubMed
Morrison, I (2016) Keep calm and cuddle on social touch as a stress buffer. Adaptive Human Behavior and Physiology 2, 344–362.CrossRefGoogle Scholar
Roosterman, D et al. (2006) Neuronal control of skin function: the skin as a neuroimmunoendocrine organ. Physiological Reviews 86, 1309–1379.CrossRefGoogle ScholarPubMed
Panzarasa, P et al. (2020) Social medical capital: how patients and caregivers can benefit from online social interactions. Journal of Medical Internet Research 22, e16337.CrossRefGoogle ScholarPubMed
Steptoe, A et al. (2004) Loneliness and neuroendocrine, cardiovascular, and inflammatory stress responses in middle-aged men and women. Psychoneuroendocrinology 29, 593–611.CrossRefGoogle ScholarPubMed
Ferland, CL and Schrader, LA (2011) Cage mate separation in pair-housed male rats evokes an acute stress corticosterone response. Neuroscience Letters 489, 154–158.CrossRefGoogle ScholarPubMed
Xavier, AM et al. (2016) Gene expression control by glucocorticoid receptors during innate immune responses. Frontiers in Endocrinology 7, 31.CrossRefGoogle ScholarPubMed
Kent, C and Agrawal, P (2020) Regulation of social stress and neural degeneration by activity-regulated genes and epigenetic mechanisms in dopaminergic neurons. Molecular Neurobiology 57, 4500–4510.CrossRefGoogle ScholarPubMed
Weaver, ICG et al. (2004) Epigenetic programming by maternal behavior. Nature Neuroscience 7, 847–854.CrossRefGoogle ScholarPubMed
Murgatroyd, C et al. (2009) Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nature Neuroscience 12, 1559–1566.CrossRefGoogle ScholarPubMed
Siuda, D et al. (2014) Social isolation-induced epigenetic changes in midbrain of adult mice. Journal of Physiology and Pharmacology 65, 247–255.Google ScholarPubMed
Wang, H-T et al. (2017) Early-life social isolation-induced depressive like behavior in rats results in microglial activation and neuronal histone methylation that are mitigated by minocycline. Neurotoxicity Research 31, 505–520.CrossRefGoogle ScholarPubMed
Gapp, N et al. (2014) Early life stress in fathers improves behavioural flexibility in their offspring. Nature Communications 5, 5466.CrossRefGoogle ScholarPubMed
Kumsta, R and Heinsrichs, M (2012) Oxytocin, stress and social behavior: neurogenetics of the human oxytocin system. Current Opinion in Neurobiology 23, 1–6.Google ScholarPubMed
Grewen, KM et al. (2005) Effects of partner support on resting oxytocin, cortisol, norepinephrine, and blood pressure before and after warm partner contact. Psychosomatic Medicine 67, 531–538.CrossRefGoogle ScholarPubMed
Holt-Lunstad, J, Birmingham, WC and Light, KC (2008) Influence of a “warm touch” support enhancement intervention among married couples on ambulatory blood pressure, oxytocin, alpha amylase and cortisol. Psychosomatic Medicine 70, 876–885.CrossRefGoogle ScholarPubMed
Scheneiderman, I et al. (2012) Oxytocin during the initial stages of romantic attachment: relations to couples’ interactive reciprocity. Psychoneuroendocrinology 37, 1277–1285.CrossRefGoogle Scholar
Plasencia, G et al. (2019) Plasma oxytocin and vasopressin levels in young and older men and women: functional relationships with attachment and cognition. Psychoneuroendocrinology 110, 104419.CrossRefGoogle Scholar
Li, T et al. (2017) Approaches mediating oxytocin regulation of the immune system. Frontiers in Immunology 7, 693.CrossRefGoogle ScholarPubMed
Hansenne, I et al. (2005) Ontogenesis and functional aspects of oxytocin and vasopressin gene expression in the thymus network. Journal of Neuroimmunology 158, 67–75.CrossRefGoogle ScholarPubMed
Yamaguchi, Y et al. (2004) Induction of uPA reléase in human peripheral blood lymphocytes by [deamino-Cysl, D-Arg8]-vasopressin (dDAVP). American Journal of Physiology - Endocrinology and Metabolism 287, E970–E976.CrossRefGoogle Scholar
Yang, H, Wang, L and Ju, G (1997) Evidence for hypothalamic paraventricular nucleus as an integrative center of neuroimmunomodulation. Neuroimmunomodulation 4, 120–127.CrossRefGoogle ScholarPubMed
Elabd, C et al. (2008) Oxytocin controls differentiation of human mensenchymal stem cells and reverses osteoporosis. Stem Cells (Dayton, Ohio) 26, 2399–2407.CrossRefGoogle Scholar
Kim, YS et al. (2012) Priming of mesenchymal stem cells with oxytocin enhances the cardiac repair in ischemia/reperfusion injury. Cells Tissues Organs 195, 428–442.CrossRefGoogle ScholarPubMed
Macciò, A et al. (2010) Oxytocin both increases proliferative response to peripheral blood lymphomonocytes to phytohemagglutinin and reverses immunosuppressive estrogen activity. In Vivo (Athens, Greece) 24, 157–163.Google ScholarPubMed
Szeto, A et al. (2008) Oxytocin attenuates NADPH-dependent superoxide activity and IL-6 secretion in macrophages and vascular cells. American Journal of Physiology - Endocrinology and Metabolism 295, E1495–E1501.CrossRefGoogle ScholarPubMed
Nation, DA et al. (2010) Oxytocin attenuates atherosclerosis and adipose tissue inflammation in socially isolated ApoE-/- mice. Psychosomatic Medicine 72, 376–382.CrossRefGoogle Scholar
Jankowski, M et al. (2010) Anti-inflammatory effect of oxytocin in rat myocardial infarction. Basic Research in Cardiology 105, 205–218.CrossRefGoogle ScholarPubMed
Oliveira-Pelegrin, GR et al. (2013) Oxytocin affects nitric oxide and cytokine production by sepsis-sensitized macrophages. Neuroimmunomodulation 20, 65–71.CrossRefGoogle ScholarPubMed
Ross, KM, McDonald-Jones, G and Miller, GE (2013) Oxytocin does not attenuate the ex vivo production of inflammatory cytokines by lipopolysaccharide-activated monocytes and macrophages from healthy male and female donors. Neuroimmunomodulation 20, 285–293.CrossRefGoogle Scholar
Kingsbury, MA and Bilbo, SD (2019) The inflammatory event of birth: how oxytocin signaling may guide the development of the brain and gastrointestinal system. Frontiers in Neuroendocrinology 55, 100794.CrossRefGoogle ScholarPubMed
Cetinel, S et al. (2010) Oxytocin treatment alleviates stress-aggravated colitis by a receptor-dependent mechanism. Regulatory Peptides 160, 146–152.CrossRefGoogle ScholarPubMed
Welch, MG et al. (2014) Oxytocin regulates gastrointestinal motility, inflammation, macromolecular permeability, and mucosal maintenance in mice. American Journal of Physiology-Gastrointestinal and Liver Physiology 307, G848–G862.CrossRefGoogle ScholarPubMed
Iseri, SO et al. (2005) Oxytocin protects against sepsis-induced multiple organ damage: role of neutrophils. Journal of Surgical Research 126, 73–81.CrossRefGoogle ScholarPubMed
Kiyikli, NK et al. (2006) Oxytocin alleviates oxidative renal injury in pyelonephritic rats via a neutrophil-dependent mechanism. Peptides 27, 2249–2257.Google Scholar
Kaneko, Y et al. (2016) Oxytocin modulates GABAAR subunits to confer neuroprotection in stroke in vitro. Scientific Reports 6, 35659.CrossRefGoogle ScholarPubMed
Glaria, E and Valledor, AF (2020) Roles of CD38 in the immune response to infection. Cells 9, 228.CrossRefGoogle ScholarPubMed
Kar, A, Mehrotra, S and Chatterjee, S (2020) CD38: T cell immune-metabolic modulator. Cells 9, 1716.CrossRefGoogle Scholar
Piedra-Quintero, ZL et al. (2020) CD38: an immunomodulatory molecule in inflammation and autoimmunity. Frontiers in Immunology 11, 597959.CrossRefGoogle ScholarPubMed
Lischke, T et al. (2013) CD38 controls the innate immune response against Listeria monocytogenes. Infection and Immunity 81, 4091–4099.CrossRefGoogle ScholarPubMed
Tolomeo, S et al. (2020) A novel role of CD38 and oxytocin as Tandem molecular moderators of human social behavior. Neuroscience & Biobehavioral Reviews 115, 251–272.CrossRefGoogle ScholarPubMed
Makhanova, A et al. (2021) CD38 is associated with bonding-relevant cognitions and relationship satisfaction over the first 3 years of marriage. Scientific Reports 11, 2965.CrossRefGoogle Scholar
Jin, D et al. (2007) CD38 is critical for social behaviour by regulating oxytocin secretion. Nature 446, 41–45.CrossRefGoogle ScholarPubMed
Suter, M and Richter, C (1999) Fragmented mitochondrial DNA is the predominant carder of oxidized DNA bases. Biochemistry 38, 459–464.CrossRefGoogle Scholar
Brand, MD (2010) The sites and topology of mitochondrial superoxide production. Experimental Gerontology 45, 466–472.CrossRefGoogle ScholarPubMed
Singh, KK, Choudhury, AR and Tiwari, HK (2017) Numtogenesis as a mechanism for development of cancer. Seminars in Cancer Biology 47, 101–109.CrossRefGoogle ScholarPubMed
Patrushev, M et al. (2004) Mitochondrial permeability transition triggers the reléase of mtDNA fragments. Cellular and Molecular Life Sciences 61, 3100–3103.CrossRefGoogle ScholarPubMed
Puertas, MJ and González-Sánchez, M (2020) Insertions of mitochondrial DNA into the nucleus-effects and role in cell evolution. Genome 63, 365–374.CrossRefGoogle ScholarPubMed
Caro, P et al. (2010) Mitochondrial DNA sequences are present inside nuclear DNA in rat tissues and increase with age. Mitochondrion 10, 479–486.CrossRefGoogle ScholarPubMed
Borges, JV et al. (2019) Social isolation and social support at adulthood affect epigenetic mechanisms, brain-derived neurotrophic factor levels and behavior of chronologically stressed rats. Behavioural Brain Research 366, 36–44.10.1016/j.bbr.2019.03.025CrossRefGoogle Scholar
Oitzl, MS et al. (2010) Brain development under stress: hypotheses of glucocorticoid actions revisited. Neuroscience & Biobehavioral Reviews 34, 853–866.CrossRefGoogle ScholarPubMed
Kanitz, E et al. (2016) Social support modulates stress-related gene expression in various brain regions of piglets. Frontiers in Behavioral Neuroscience 10, 227.CrossRefGoogle ScholarPubMed
Way, BM and Taylor, SE (2010) Social influences on health: is serotonin a critical mediator? Psychosomatic Medicine 72, 107–112.CrossRefGoogle ScholarPubMed
Pearson, R et al. (2016) Serotonin promoter polymorphism (5-HTTLPR) predicts biased attention for emotion stimuli: preliminary evidence of moderation by the social environment. Clinical Psychological Science 4, 122–128.CrossRefGoogle ScholarPubMed
Lin, S-H et al. (2011) The dopamine hypothesis of social support. Medical Hypotheses 77, 753–755.CrossRefGoogle ScholarPubMed
Sotoyama, H et al. (2022) The dual role of dopamine in the modulation of information processing in the prefrontal cortex underlying social behavior. FASEB Journal 36, e22160.10.1096/fj.202101637RCrossRefGoogle ScholarPubMed