Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-26T06:27:22.481Z Has data issue: false hasContentIssue false
  • English
  • Français

Interleukin 1B gene (IL1B) variation and internalizing symptoms in maltreated preschoolers

Published online by Cambridge University Press:  25 November 2014

Kathryn K. Ridout ,
Stephanie H. Parade ,
Ronald Seifer ,
Lawrence H. Price ,
Joel Gelernter ,
Paloma Feliz  and
Audrey R. Tyrka
Kathryn K. Ridout
Affiliation:
Butler Hospital Mood Disorders Research Program and Laboratory for Clinical and Translational Neuroscience Alpert Medical School of Brown University
Stephanie H. Parade
Affiliation:
Alpert Medical School of Brown University E. P. Bradley Hospital Bradley/Hasbro Children's Research Center
Ronald Seifer
Affiliation:
Alpert Medical School of Brown University E. P. Bradley Hospital Bradley/Hasbro Children's Research Center
Lawrence H. Price
Affiliation:
Butler Hospital Mood Disorders Research Program and Laboratory for Clinical and Translational Neuroscience Alpert Medical School of Brown University
Joel Gelernter
Affiliation:
Yale University School of Medicine and VA CT Healthcare Center
Paloma Feliz
Affiliation:
E. P. Bradley Hospital Bradley/Hasbro Children's Research Center
Audrey R. Tyrka*
Affiliation:
Butler Hospital Mood Disorders Research Program and Laboratory for Clinical and Translational Neuroscience Alpert Medical School of Brown University
*
Address correspondence and reprint requests to: Audrey R. Tyrka, Butler Hospital, 345 Blackstone Boulevard, Providence, RI 02906; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Evidence now implicates inflammatory proteins in the neurobiology of internalizing disorders. Genetic factors may influence individual responses to maltreatment; however, little work has examined inflammatory genetic variants in adults and none in children. The present study examined the role of an interleukin 1B gene (IL1B) variant in preschoolers exposed to maltreatment and other forms of adversity in internalizing symptom development. One hundred ninety-eight families were enrolled, with one child (age 3–5 years) from each family. Adversity measures included child protective service documentation of moderate–severe maltreatment in the last 6 months and interview-assessed contextual stressors. Internalizing symptoms were measured using the Child Behavior Checklist and the Diagnostic Infant and Preschool Assessment. Maltreated children had higher major depressive disorder (MDD) and posttraumatic stress disorder symptoms and marginally higher internalizing symptoms on the Child Behavior Checklist. Controlling for age, sex, and race, IL1B genotype was associated with MDD symptoms (p = .002). Contextual stressors were significantly associated with MDD and posttraumatic stress disorder and marginally with internalizing symptoms. The IL1B genotype interacted with contextual stress such that children homozygous for the minor allele had more MDD symptoms (p = .045). These results suggest that genetic variants of IL1B may modulate the development of internalizing symptoms in the face of childhood adversity.

Type
Regular Articles
Information
Development and Psychopathology , Volume 26 , Special Issue 4pt2: Multilevel Developmental Perspectives Toward Understanding Internalizing Psychopathology: Current Research and Future Directions , November 2014 , pp. 1277 - 1287
Copyright
Copyright © Cambridge University Press 2014 

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

Achenbach, T. M., & Ruffle, T. M. (2000). The Child Behavior Checklist and related forms for assessing behavioral/emotional problems and competencies. Pediatrics in Review, 21, 265–271.Google Scholar
Aguilera, M., Arias, B., Wichers, M., Barrantes-Vidal, N., Moya, J., Villa, H., et al. (2009). Early adversity and 5-HTT/BDNF genes: New evidence of gene–environment interactions on depressive symptoms in a general population. Psychological Medicine, 39, 1425–1432.Google Scholar
Appleton, A. A., Buka, S. L., McCormick, M. C., Koenen, K. C., Loucks, E. B., & Kubzansky, L. D. (2012). The association between childhood emotional functioning and adulthood inflammation is modified by early-life socioeconomic status. Health Psychology, 31, 413–422.Google Scholar
Aslund, C., Leppert, J., Comasco, E., Nordquist, N., Oreland, L., & Nilsson, K. W. (2009). Impact of the interaction between the 5HTTLPR polymorphism and maltreatment on adolescent depression: A population-based study. Behavior Genetics, 39, 524–531.Google Scholar
Bailey, M. T., Kinsey, S. G., Padgett, D. A., Sheridan, J. F., & Leblebicioglu, B. (2009). Social stress enhances IL-1beta and TNF-alpha production by Porphyromonas gingivalis lipopolysaccharide-stimulated CD11b+ cells. Physiology and Behavior, 98, 351–358.Google Scholar
Baker, D. G., Nievergelt, C. M., & O'Connor, D. T. (2012). Biomarkers of PTSD: Neuropeptides and immune signaling. Neuropharmacology, 62, 663–673.Google Scholar
Banny, A. M., Cicchetti, D., Rogosch, F. A., Oshri, A., & Crick, N. R. (2013). Vulnerability to depression: A moderated mediation model of the roles of child maltreatment, peer victimization, and serotonin transporter linked polymorphic region genetic variation among children from low socioeconomic status backgrounds. Development and Psychopathology, 25, 599–614.Google Scholar
Barnett, D., Manly, J. T., & Cicchetti, D. (1993). Defining child maltreatment: The interface between policy and research. In Cicchetti, D. & Toth, S. L. (Eds.), Child abuse, child development, and social policy (pp. 7–73). Norwood, NJ: Ablex.Google Scholar
Bauer, M. E., Wieck, A., Lopes, R. P., Teixeira, A. L., & Grassi-Oliveira, R. (2010). Interplay between neuroimmunoendocrine systems during post-traumatic stress disorder: A mini review. Neuroimmunomodulation, 17, 192–195.Google Scholar
Bellani, M., Nobile, M., Bianchi, V., van Os, J., & Brambilla, P. (2012). G × E interaction and neurodevelopment: I. Focus on maltreatment. Epidemiology and Psychiatric Sciences, 21, 347–351.Google Scholar
Belsky, J., Jonassaint, C., Pluess, M., Stanton, M., Brummett, B., & Williams, R. (2009). Vulnerability genes or plasticity genes? Molecular Psychiatry, 14, 746–754.Google Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885–908.Google Scholar
Benjet, C., Borges, G., & Medina-Mora, M. E. (2010). Chronic childhood adversity and onset of psychopathology during three life stages: Childhood, adolescence and adulthood. Journal of Psychiatric Research, 44, 732–740.CrossRefGoogle ScholarPubMed
Bertone-Johnson, E. R., Whitcomb, B. W., Missmer, S. A., Karlson, E. W., & Rich-Edwards, J. W. (2012). Inflammation and early-life abuse in women. American Journal of Preventive Medicine, 43, 611–620.Google Scholar
Briggs-Gowan, M. J., Carter, A. S., Bosson-Heenan, J., Guyer, A. E., & Horwitz, S. M. (2006). Are infant–toddler social–emotional and behavioral problems transient? Journal of the American Academy of Child & Adolescent Psychiatry, 45, 849–858.Google Scholar
Brydon, L., Edwards, S., Jia, H., Mohamed-Ali, V., Zachary, I., Martin, J. F., et al. (2005). Psychological stress activates interleukin-1beta gene expression in human mononuclear cells. Brain, Behavior, and Immunity, 19, 540–546.Google Scholar
Bufferd, S. J., Dougherty, L. R., Carlson, G. A., & Klein, D. N. (2011). Parent-reported mental health in preschoolers: Findings using a diagnostic interview. Comprehensive Psychiatry, 52, 359–369.Google Scholar
Carpenter, L. L., Carvalho, J. P., Tyrka, A. R., Wier, L. M., Mello, A. F., Mello, M. F., et al. (2007). Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting significant childhood maltreatment. Biological Psychiatry, 62, 1080–1087.Google Scholar
Carpenter, L. L., Shattuck, T. T., Tyrka, A. R., Geracioti, T. D., & Price, L. H. (2011). Effect of childhood physical abuse on cortisol stress response. Psychopharmacology, 214, 367–375.Google Scholar
Carr, C. P., Martins, C. M., Stingel, A. M., Lemgruber, V. B., & Juruena, M. F. (2013). The role of early life stress in adult psychiatric disorders: A systematic review according to childhood trauma subtypes. Journal of Nervous and Mental Disease, 201, 1007–1020.Google Scholar
Carrion, V. G., & Wong, S. S. (2012). Can traumatic stress alter the brain? Understanding the implications of early trauma on brain development and learning. Journal of Adolescent Health, 51(Suppl. 2), S23–S28.Google Scholar
Caso, J. R., Moro, M. A., Lorenzo, P., Lizasoain, I., & Leza, J. C. (2007). Involvement of IL-1beta in acute stress-induced worsening of cerebral ischaemia in rats. European Neuropsychopharmacology, 17, 600–607.Google Scholar
Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., et al. (2003). Influence of life stress on depression: Moderation by a polymorphism in the 5-HTT gene. Science, 301, 386–389.Google Scholar
Cicchetti, D., & Rogosch, F. A. (2012). Gene × Environment interaction and resilience: Effects of child maltreatment and serotonin, corticotropin releasing hormone, dopamine, and oxytocin genes. Development and Psychopathology, 24, 411–427.Google Scholar
Cicchetti, D., Rogosch, F. A., & Oshri, A. (2011). Interactive effects of corticotropin releasing hormone receptor 1, serotonin transporter linked polymorphic region, and child maltreatment on diurnal cortisol regulation and internalizing symptomatology. Development and Psychopathology, 23, 1125–1138.Google Scholar
Cicchetti, D., Rogosch, F. A., & Sturge-Apple, M. L. (2007). Interactions of child maltreatment and serotonin transporter and monoamine oxidase A polymorphisms: Depressive symptomatology among adolescents from low socioeconomic status backgrounds. Development and Psychopathology, 19, 1161–1180.Google Scholar
Cicchetti, D., Rogosch, F. A., & Toth, S. L. (2011). The effects of child maltreatment and polymorphisms of the serotonin transporter and dopamine D4 receptor genes on infant attachment and intervention efficacy. Development and Psychopathology, 23, 357–372.Google Scholar
Cicchetti, D., & Toth, S. L. (2005). Child maltreatment. Annual Review of Clinical Psychology, 1, 409–438.Google Scholar
Coelho, R., Viola, T. W., Walss-Bass, C., Brietzke, E., & Grassi-Oliveira, R. (2014). Childhood maltreatment and inflammatory markers: A systematic review. Acta Psychiatrica Scandinavica, 129, 180–192.Google Scholar
Cole, S. W., Arevalo, J. M., Manu, K., Telzer, E. H., Kiang, L., Bower, J. E., et al. (2011). Antagonistic pleiotropy at the human IL6 promoter confers genetic resilience to the pro-inflammatory effects of adverse social conditions in adolescence. Developmental Psychology, 47, 1173–1180.Google Scholar
Cole, S. W., Arevalo, J. M., Takahashi, R., Sloan, E. K., Lutgendorf, S. K., Sood, A. K., et al. (2010). Computational identification of gene–social environment interaction at the human IL6 locus. Proceedings of the National Academy of Sciences, 107, 5681–5686.Google Scholar
Comasco, E., Aslund, C., Oreland, L., & Nilsson, K. W. (2013). Three-way interaction effect of 5-HTTLPR, BDNF Val66Met, and childhood adversity on depression: A replication study. European Neuropsychopharmacology, 23, 1300–1306.Google Scholar
Danese, A., Moffitt, T. E., Pariante, C. M., Ambler, A., Poulton, R., & Caspi, A. (2008). Elevated inflammation levels in depressed adults with a history of childhood maltreatment. Archives of General Psychiatry, 65, 409–415.Google Scholar
Danese, A., Pariante, C. M., Caspi, A., Taylor, A., & Poulton, R. (2007). Childhood maltreatment predicts adult inflammation in a life-course study. Proceedings of the National Academy of Sciences, 104, 1319–1324.Google Scholar
Dantzer, R. (2009). Cytokine, sickness behavior, and depression. Immunology and Allergy Clinics of North America, 29, 247–264.Google Scholar
Dowlati, Y., Herrmann, N., Swardfager, W., Liu, H., Sham, L., Reim, E. K., et al. (2010). A meta-analysis of cytokines in major depression. Biological Psychiatry, 67, 446–457.Google Scholar
Dunn, E. C., Uddin, M., Subramanian, S. V., Smoller, J. W., Galea, S., & Koenen, K. C. (2011). Research review: Gene–environment interaction research in youth depression—A systematic review with recommendations for future research. Journal of Child Psychology and Psychiatry and Allied Disciplines, 52, 1223–1238.Google Scholar
Felger, J. C., & Lotrich, F. E. (2013). Inflammatory cytokines in depression: Neurobiological mechanisms and therapeutic implications. Neuroscience, 246, 199–229.Google Scholar
Ferri, C., Croce, G., Cofini, V., De Berardinis, G., Grassi, D., Casale, R., et al. (2007). C-reactive protein: Interaction with the vascular endothelium and possible role in human atherosclerosis. Current Pharmaceutical Design, 13, 1631–1645.Google Scholar
Gola, H., Engler, H., Sommershof, A., Adenauer, H., Kolassa, S., Schedlowski, M., et al. (2013). Posttraumatic stress disorder is associated with an enhanced spontaneous production of pro-inflammatory cytokines by peripheral blood mononuclear cells. BMC Psychiatry, 13, 40.Google Scholar
Green, J. G., McLaughlin, K. A., Berglund, P. A., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., 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.Google Scholar
Groer, M. W., & Morgan, K. (2007). Immune, health and endocrine characteristics of depressed postpartum mothers. Psychoneuroendocrinology, 32, 133–139.Google Scholar
Haastrup, E., Bukh, J. D., Bock, C., Vinberg, M., Thorner, L. W., Hansen, T., et al. (2012). Promoter variants in IL18 are associated with onset of depression in patients previously exposed to stressful-life events. Journal of Affective Disorders, 136, 134–138.CrossRefGoogle ScholarPubMed
Hahn, W. H., Cho, B. S., Kim, S. D., Kim, S. K., & Kang, S. (2009). Interleukin-1 cluster gene polymorphisms in childhood IgA nephropathy. Pediatric Nephrology, 24, 1329–1336.Google Scholar
Hartman, C. A., Hermanns, V. W., de Jong, P. J., & Ormel, J. (2013). Self- or parent report of (co-occurring) internalizing and externalizing problems, and basal or reactivity measures of HPA-axis functioning: A systematic evaluation of the internalizing-hyperresponsivity versus externalizing-hyporesponsivity HPA-axis hypothesis. Biological Psychology, 94, 175–184.Google Scholar
Heim, C., & Binder, E. B. (2012). Current research trends in early life stress and depression: Review of human studies on sensitive periods, gene–environment interactions, and epigenetics. Experimental Neurology, 233, 102–111.Google Scholar
Hickman, L. J., Jaycox, L. H., Setodji, C. M., Kofner, A., Schultz, D., Barnes-Proby, D., et al. (2013). How much does “how much” matter? Assessing the relationship between children's lifetime exposure to violence and trauma symptoms, behavior problems, and parenting stress. Journal of Interpersonal Violence, 28, 1338–1362.Google Scholar
Hiles, S. A., Baker, A. L., de Malmanche, T., & Attia, J. (2012). A meta-analysis of differences in IL-6 and IL-10 between people with and without depression: Exploring the causes of heterogeneity. Brain, Behavior, and Immunity, 26, 1180–1188.Google Scholar
Hoge, E. A., Brandstetter, K., Moshier, S., Pollack, M. H., Wong, K. K., & Simon, N. M. (2009). Broad spectrum of cytokine abnormalities in panic disorder and posttraumatic stress disorder. Depression and Anxiety, 26, 447–455.Google Scholar
Hornung, O. P., & Heim, C. M. (2014). Gene–environment interactions and intermediate phenotypes: Early trauma and depression. Frontiers in Endocrinology, 5, 14.Google Scholar
Kaufman, J., Yang, B. Z., Douglas-Palumberi, H., Grasso, D., Lipschitz, D., Houshyar, S., et al. (2006). Brain-derived neurotrophic factor-5-HTTLPR gene interactions and environmental modifiers of depression in children. Biological Psychiatry, 59, 673–680.Google Scholar
Kaufman, J., Yang, B. Z., Douglas-Palumberi, H., Houshyar, S., Lipschitz, D., Krystal, J. H., et al. (2004). Social supports and serotonin transporter gene moderate depression in maltreated children. Proceedings of the National Academy of Sciences, 101, 17316–17321.Google Scholar
Keller, M. C. (2014). Gene × Environment interaction studies have not properly controlled for potential confounders: The problem and the (simple) solution. Biological Psychiatry, 75, 18–24.Google Scholar
Kim-Spoon, J., Cicchetti, D., & Rogosch, F. A. (2013). A longitudinal study of emotion regulation, emotion lability-negativity, and internalizing symptomatology in maltreated and nonmaltreated children. Child Development, 84, 512–527.Google Scholar
Kim, J. M., Stewart, R., Kim, S. W., Kim, S. Y., Bae, K. Y., Kang, H. J., et al. (2013). Physical health and incident late-life depression: Modification by cytokine genes. Neurobiology of Aging, 34, e351–e359.Google Scholar
Koo, J. W., & Duman, R. S. (2008). IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proceedings of the National Academy of Sciences, 105, 751–756.Google Scholar
Lacy, P., & Stow, J. L. (2011). Cytokine release from innate immune cells: Association with diverse membrane trafficking pathways. Blood, 118, 9–18.Google Scholar
Lavie, C. J., Milani, R. V., Verma, A., & O'Keefe, J. H. (2009). C-reactive protein and cardiovascular diseases—Is it ready for primetime? American Journal of the Medical Sciences, 338, 486–492.Google Scholar
Lesch, K. P., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., Petri, S., et al. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science, 274, 1527–1531.Google Scholar
Liu, Y., Ho, R. C., & Mak, A. (2012). Interleukin (IL)-6, tumour necrosis factor alpha (TNF-alpha) and soluble interleukin-2 receptors (sIL-2R) are elevated in patients with major depressive disorder: A meta-analysis and meta-regression. Journal of Affective Disorders, 139, 230–239.Google Scholar
Low, C. A., Matthews, K. A., & Hall, M. (2013). Elevated C-reactive protein in adolescents: Roles of stress and coping. Psychosomatic Medicine, 75, 449–452.Google Scholar
Luby, J. L., Gaffrey, M. S., Tillman, R., April, L. M., & Belden, A. C. (2014). Trajectories of preschool disorders to full DSM depression at school age and early adolescence: Continuity of preschool depression. American Journal of Psychiatry. Advance online publication.Google Scholar
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434–445.Google Scholar
Mandelli, L., & Serretti, A. (2013). Gene–environment interaction studies in depression and suicidal behavior: An update. Neuroscience & Biobehavioral Reviews, 37, 2375–2397.Google Scholar
Manly, J. T., Kim, J. E., Rogosch, F. A., & Cicchetti, D. (2001). Dimensions of child maltreatment and children's adjustment: Contributions of developmental timing and subtype. Development and Psychopathology, 13, 759–782.Google Scholar
Masten, A. S., & Cicchetti, D. (2010). Developmental cascades. Development and Psychopathology, 22, 491–495.Google Scholar
Mastrolonardo, M., Alicino, D., Zefferino, R., Pasquini, P., & Picardi, A. (2007). Effect of psychological stress on salivary interleukin-1beta in psoriasis. Archives of Medical Research, 38, 206–211.Google Scholar
Mesman, J., & Koot, H. M. (2001). Early preschool predictors of preadolescent internalizing and externalizing DSM-IV diagnoses. Journal of the American Academy of Child & Adolescent Psychiatry, 40, 1029–1036.Google Scholar
Mills, N. T., Scott, J. G., Wray, N. R., Cohen-Woods, S., & Baune, B. T. (2013). Research review: The role of cytokines in depression in adolescents: A systematic review. Journal of Child Psychology and Psychiatry and Allied Disciplines, 54, 816–835.Google Scholar
Mills, R., Scott, J., Alati, R., O'Callaghan, M., Najman, J. M., & Strathearn, L. (2013). Child maltreatment and adolescent mental health problems in a large birth cohort. Child Abuse and Neglect, 37, 292–302.Google Scholar
Mitchell, R. H., & Goldstein, B. I. (2014). Inflammation in children and adolescents with neuropsychiatric disorders: A systematic review. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 274–296.Google Scholar
Morris, M. C., Compas, B. E., & Garber, J. (2012). Relations among posttraumatic stress disorder, comorbid major depression, and HPA function: A systematic review and meta-analysis. Clinical Psychology Review, 32, 301–315.Google Scholar
Moxley, G., Han, J., Stern, A. G., & Riley, B. P. (2007). Potential influence of IL1B haplotype and IL1A-IL1B-IL1RN extended haplotype on hand osteoarthritis risk. Osteoarthritis and Cartilage, 15, 1106–1112.Google Scholar
Nederhof, E., Bouma, E. M., Oldehinkel, A. J., & Ormel, J. (2010). Interaction between childhood adversity, brain-derived neurotrophic factor val/met and serotonin transporter promoter polymorphism on depression: The TRAILS study. Biological Psychiatry, 68, 209–212.Google Scholar
Nguyen, K. T., Deak, T., Owens, S. M., Kohno, T., Fleshner, M., Watkins, L. R., et al. (1998). Exposure to acute stress induces brain interleukin-1beta protein in the rat. Journal of Neuroscience, 18, 2239–2246.Google Scholar
Norman, R. E., Byambaa, M., De, R., Butchart, A., Scott, J., & Vos, T. (2012). The long-term health consequences of child physical abuse, emotional abuse, and neglect: A systematic review and meta-analysis. PLOS Medicine, 9, e1001349.Google Scholar
Nugent, N. R., Tyrka, A. R., Carpenter, L. L., & Price, L. H. (2011). Gene–environment interactions: Early life stress and risk for depressive and anxiety disorders. Psychopharmacology, 214, 175–196.Google Scholar
O'Brien, S. M., Scott, L. V., & Dinan, T. G. (2004). Cytokines: Abnormalities in major depression and implications for pharmacological treatment. Human Psychopharmacology, 19, 397–403.Google Scholar
O'Donovan, A., Sun, B., Cole, S., Rempel, H., Lenoci, M., Pulliam, L., et al. (2011). Transcriptional control of monocyte gene expression in post-traumatic stress disorder. Disease Markers, 30, 123–132.Google Scholar
Pace, T. W., Hu, F., & Miller, A. H. (2007). Cytokine-effects on glucocorticoid receptor function: Relevance to glucocorticoid resistance and the pathophysiology and treatment of major depression. Brain, Behavior, and Immunity, 21, 9–19.Google Scholar
Pace, T. W., Wingenfeld, K., Schmidt, I., Meinlschmidt, G., Hellhammer, D. H., & Heim, C. M. (2012). Increased peripheral NF-kappaB pathway activity in women with childhood abuse-related posttraumatic stress disorder. Brain, Behavior, and Immunity, 26, 13–17.Google Scholar
Pandey, G. N., Rizavi, H. S., Ren, X., Fareed, J., Hoppensteadt, D. A., Roberts, R. C., et al. (2012). Proinflammatory cytokines in the prefrontal cortex of teenage suicide victims. Journal of Psychiatric Research, 46, 57–63.Google Scholar
Pietrek, C., Elbert, T., Weierstall, R., Muller, O., & Rockstroh, B. (2013). Childhood adversities in relation to psychiatric disorders. Psychiatry Research, 206, 103–110.Google Scholar
Porterfield, V. M., Gabella, K. M., Simmons, M. A., & Johnson, J. D. (2012). Repeated stressor exposure regionally enhances beta-adrenergic receptor-mediated brain IL-1beta production. Brain, Behavior, and Immunity, 26, 1249–1255.Google Scholar
Rincon-Cortes, M., & Sullivan, R. M. (2014). Early life trauma and attachment: Immediate and enduring effects on neurobehavioral and stress axis development. Frontiers in Endocrinology, 5, 33.Google Scholar
Robles, T. F., Glaser, R., & Kiecolt-Glaser, J. K. (2005). Out of balance: A new look at chronic stress, depression, and immunity. Current Directions in Psychological Science, 14, 111–115.CrossRefGoogle Scholar
Rohleder, N. (2014). Stimulation of systemic low-grade inflammation by psychosocial stress. Psychosomatic Medicine, 76, 181–189.Google Scholar
Rooks, C., Veledar, E., Goldberg, J., Bremner, J. D., & Vaccarino, V. (2012). Early trauma and inflammation: Role of familial factors in a study of twins. Psychosomatic Medicine, 74, 146–152.Google Scholar
Roza, S. J., Hofstra, M. B., van der Ende, J., & Verhulst, F. C. (2003). Stable prediction of mood and anxiety disorders based on behavioral and emotional problems in childhood: A 14-year follow-up during childhood, adolescence, and young adulthood. American Journal of Psychiatry, 160, 2116–2121.Google Scholar
Sasayama, D., Hori, H., Iijima, Y., Teraishi, T., Hattori, K., Ota, M., et al. (2011). Modulation of cortisol responses to the DEX/CRH test by polymorphisms of the interleukin-1beta gene in healthy adults. Behavioral and Brain Functions, 7, 23.Google Scholar
Sasayama, D., Hori, H., Teraishi, T., Hattori, K., Ota, M., Iijima, Y., et al. (2011). Possible association between interleukin-1beta gene and schizophrenia in a Japanese population. Behavioral and Brain Functions, 7, 35.Google Scholar
Sasayama, D., Hori, H., Teraishi, T., Hattori, K., Ota, M., Matsuo, J., et al. (2011). Association of interleukin-1beta genetic polymorphisms with cognitive performance in elderly females without dementia. Journal of Human Genetics, 56, 613–616.Google Scholar
Saudino, K. J., Wertz, A. E., Gagne, J. R., & Chawla, S. (2004). Night and day: Are siblings as different in temperament as parents say they are? Journal of Personality and Social Psychology, 87, 698–706.Google Scholar
Scheeringa, M. S., & Haslett, N. (2010). The reliability and criterion validity of the Diagnostic Infant and Preschool Assessment: A new diagnostic instrument for young children. Child Psychiatry and Human Development, 41, 299–312.Google Scholar
Schilling, E. A., Aseltine, R. H. Jr., & Gore, S. (2007). Adverse childhood experiences and mental health in young adults: A longitudinal survey. BMC Public Health, 7, 30.CrossRefGoogle ScholarPubMed
Scott, K. M., Smith, D. R., & Ellis, P. M. (2010). Prospectively ascertained child maltreatment and its association with DSM-IV mental disorders in young adults. Archives of General Psychiatry, 67, 712–719.Google Scholar
Seifer, R., Sameroff, A., Dickstein, S., Schiller, M., & Hayden, L. C. (2004). Your own children are special: Clues to the sources of reporting bias in temperament assessments. Infant Behavior and Development, 27, 323–341.Google Scholar
Shabalina, S. A., Ogurtsov, A. Y., Spiridonov, A. N., Novichkov, P. S., Spiridonov, N. A., & Koonin, E. V. (2010). Distinct patterns of expression and evolution of intronless and intron-containing mammalian genes. Molecular Biology and Evolution, 27, 1745–1749.Google Scholar
Shikanai, H., Kimura, S., & Togashi, H. (2013). Early life stress affects the serotonergic system underlying emotional regulation. Biological and Pharmaceutical Bulletin, 36, 1392–1395.Google Scholar
Sjoberg, R. L., Nilsson, K. W., Nordquist, N., Ohrvik, J., Leppert, J., Lindstrom, L., et al. (2006). Development of depression: Sex and the interaction between environment and a promoter polymorphism of the serotonin transporter gene. International Journal of Neuropsychopharmacology, 9, 443–449.Google Scholar
Slopen, N., Kubzansky, L. D., McLaughlin, K. A., & Koenen, K. C. (2013). Childhood adversity and inflammatory processes in youth: A prospective study. Psychoneuroendocrinology, 38, 188–200.Google Scholar
Solovieva, S., Kamarainen, O. P., Hirvonen, A., Hamalainen, S., Laitala, M., Vehmas, T., et al. (2009). Association between interleukin 1 gene cluster polymorphisms and bilateral distal interphalangeal osteoarthritis. Journal of Rheumatology, 36, 1977–1986.Google Scholar
Steptoe, A., Hamer, M., & Chida, Y. (2007). The effects of acute psychological stress on circulating inflammatory factors in humans: A review and meta-analysis. Brain, Behavior, and Immunity, 21, 901–912.Google Scholar
Stetler, C., & Miller, G. E. (2011). Depression and hypothalamic–pituitary–adrenal activation: A quantitative summary of four decades of research. Psychosomatic Medicine, 73, 114–126.Google Scholar
Teicher, M. H., & Samson, J. A. (2013). Childhood maltreatment and psychopathology: A case for ecophenotypic variants as clinically and neurobiologically distinct subtypes. American Journal of Psychiatry, 170, 1114–1133.Google Scholar
Tyrka, A. R., Wier, L., Price, L. H., Ross, N. S., & Carpenter, L. L. (2008). Childhood parental loss and adult psychopathology: Effects of loss characteristics and contextual factors. International Journal of Psychiatry in Medicine, 38, 329–344.Google Scholar
von Kanel, R., Hepp, U., Kraemer, B., Traber, R., Keel, M., Mica, L. et al. (2007). Evidence for low-grade systemic proinflammatory activity in patients with posttraumatic stress disorder. Journal of Psychiatric Research, 41, 744–752.Google Scholar
Widom, C. S. (1999). Posttraumatic stress disorder in abused and neglected children grown up. American Journal of Psychiatry, 156, 1223–1229.Google Scholar
Widom, C. S., DuMont, K., & Czaja, S. J. (2007). A prospective investigation of major depressive disorder and comorbidity in abused and neglected children grown up. Archives of General Psychiatry, 64, 49–56.Google Scholar
Yamakawa, K., Matsunaga, M., Isowa, T., Kimura, K., Kasugai, K., Yoneda, M., et al. (2009). Transient responses of inflammatory cytokines in acute stress. Biological Psychology, 82, 25–32.Google Scholar
You, Z., Luo, C., Zhang, W., Chen, Y., He, J., Zhao, Q., et al. (2011). Pro- and anti-inflammatory cytokines expression in rat's brain and spleen exposed to chronic mild stress: Involvement in depression. Behavioral Brain Research, 225, 135–141.Google Scholar
Zeanah, C. H., Boris, N. W., & Scheeringa, M. S. (1997). Psychopathology in infancy. Journal of Child Psychology and Psychiatry and Allied Disciplines, 38, 81–99.Google Scholar