Weinberg

Joanne Weinberg

Professor and Distinguished University Scholar, Emerita

Cellular & Physiological Sciences
Faculty of Medicine

Contact

Email: joanne.weinberg@ubc.ca
Office: 604-822-6214
Website: www.weinberglab.ca

Education

PhD, Stanford University Medical School
MAT, Harvard University Graduate School of Education
BA (Brown University)

Research
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Research Interests

Prenatal alcohol exposure (PAE) can have adverse consequences for the fetus, resulting in physical, neurobiological, cognitive, adaptive, health, and behavioral alterations that can persist into adulthood. The umbrella term fetal alcohol spectrum disorder (FASD) describes the full range of alcohol’s adverse effects. The consequences of PAE vary depending not only on the amount, timing, and pattern of exposure, but also on environmental, genetic, epigenetic, and other factors that influence development. Recent studies suggest that prevalence of FASD may be as high as 1%-5%, higher than that of other neurodevelopmental disorders such as Autism Spectrum Disorder and Down Syndrome. FASD is thus an international public health, education, economic, and social issue.

Our research focuses on the effects of prenatal alcohol exposure, stress, and neuroendocrine-neuroimmune regulation, with a specific focus on mechanisms underlying prenatal alcohol effects on fetal programming of neurobiological systems. Our studies have demonstrated that alcohol, in addition to its teratogenic effects, is an early life insult that programs developing systems and markedly increases risk for diseases/disorders throughout life, the “Developmental Origins of Health and Disease” (DOHaD) concept. We have developed rodent models to examine brain-behavior relationships from prenatal life through adulthood, utilizing a broad multidisciplinary approach to tackle problems from the molecular to the behavioral level. We have also collaborated actively with clinical researchers to extend our expertise on stress, programming and development to human populations.

Our animal model studies have shown that PAE results in hyperresponsiveness to stressors, and marked changes in central regulation of hypothalamic-pituitary-adrenal (HPA) or stress axis activity under both basal and stress conditions. Utilizing an animal model of adjuvant-induced arthritis, data have demonstrated marked alcohol-exposed offspring exhibit more severe and more prolonged responses to immune challenge, reflecting alterations in neuroimmune function. For the past 10 years, we have been part of the NIH/NIAAA Collaborative Initiative on FASD, providing the opportunity to translate research on animal models of PAE to cohorts of pregnant women and their children. This research is the first to identify a link between maternal alcohol consumption, inflammation, and child outcomes: Unique immune signatures in pregnant women were identified in association with whether or not they consumed alcohol and with the neurodevelopmental outcomes (typically developing/developmentally delayed) of their children. Similarly, immune profiles of the children were shown to reflect both alcohol exposure and neurodevelopmental status. This research is currently testing a “multiple hit” hypothesis that PAE results in a vulnerable organism that may be further impacted by social adversity and lack of

resources/coping skills, resulting in immune and endocrine dysregulation that in turn, may be key drivers of early-onset health and neurobehavioral problems over the life course.

Our research has been funded over the years by the BC Health Research Foundation, MRC/CIHR, Coast Capital Savings Depression Research Fund, the Human Early Learning Partnership, the Canadian Foundation on Fetal Alcohol Research, and since 1988, by NIH/ NIAAA. From 2009-20202, Dr. Weinberg held a MERIT Award.

Publications
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Publications, 2018-present

  1. Lussier, AA, Morin, AM, MacIsaac, JL, Salmon, J, Weinberg, J, Reynolds, JN, Pavlidis, P, Chudley, AE, Kobor, MS. DNA methylation as a predictor of fetal alcohol spectrum disorder. Clinical Epigenetics, 2018, 10:5. https://doi.org/10.1186/s13148-018-0439-6
  2. Lam, V.Y.Y., Raineki, C., Takeuchi, L.E., Ellis, L., Woodward, T.S., & Weinberg, J. (2018). Chronic stress alters behavior in the forced swim test and underlying neural activity in animals exposed to alcohol prenatally: Sex- and time-dependent effects. Front Behav Neurosci 2018 Mar 9;12:42. doi: 10.3389/fnbeh.2018.00042.
  3. Bodnar, TS, Raineki, C, Wertelecki, W, Yevtushok, L., Zymak-Zakutnya, N., Honerkamp-Smith, G., Wells, A., Rolland, M., Woordward, TS, Coles, CD, Kable, JA, Chambers, CD, Weinberg, J., and the CIFASD. (2018). Altered maternal immune networks are associated with adverse child neurodevelopment: Impact of alcohol consumption during pregnancy. Brain Behav Immun, 73:205-215, 2018. doi: 10.1016/j.bbi.2018.05.004.
  4. Lam VYY, Raineki C, Ellis L, Yu W, Weinberg J. (2018). Interactive effects of prenatal alcohol exposure and chronic stress in adulthood on anxiety-like behavior and central stress-related receptor mRNA expression: Sex- and time-dependent effects. Psychoneuroendocrinology. 97:8-19.
  5. Neuenschwander R, Hookenson K, Brain U, Brunau RE, Devlin AM, Weinberg J, Diamond A, Oberlander TF. (2018). Children’s stress regulation mediates the association between prenatal maternal mood and child executive functions for boys, but not girls. Development and Psychopathology. 30(3):953-969.
  6. Holman PJ, Ellis L, Morgan E, Weinberg J. (2018). Prenatal alcohol exposure disrupts male adolescent social behavior and oxytocin receptor binding in rodents. Hormones and Behavior. 105:115-127.
  7. Moukarzel S, Dyer RA, Garcia C, Wiedeman AM, Boyce G, Weinberg J, Keller B, Elango R, Innis SM (2018). Milk fat globule membrane supplementation in formula-fed rat pups improves reflex development and may alter brain lipid composition. Sci Rep 8:15277.
  8. Lussier, AA, Bodnar, TS, Mingay, M, Morin, AM, Hirst, M, Kobor, MS, Weinberg, J. (2018). Prenatal alcohol exposure: Profiling developmental DNA methylation patterns in central and peripheral tissues. Front Genet 04 December | https://doi.org/10.3389/fgene.2018.00610
  9. Lam VYY, Raineki C, Wang LY, Chiu M, Lee G, Ellis L, Yu W, Weinberg J. (2019). Role of corticosterone in anxiety- and depressive-like behavior and HPA regulation following prenatal alcohol exposure. Prog Neuropsychopharmacol Biol Psychiatry. 90:1-15.
  10. Ipsiroglu, OS, Wind, K, Hung, Y-H, Berger, M, Chan, F, Yu, W, Stockler, S, Weinberg, J. (2019). Prenatal alcohol exposure and sleep-wake behaviors: Exploratory and naturalistic observations in the clinical setting and in an animal model. Sleep Medicine 54 101-112.
  11. Raineki C, Morgan EJ, Ellis L, Weinberg J. (2019). Glucocorticoid receptor expression in the stress-limbic circuitry is differentially affected by prenatal alcohol exposure and adolescent stress. Brain Res.1718:242-251
  12. Basson, R, O’Loughlin, JI, Weinberg, J, Young, AH, Bodnar, T, Brotto, LA. (2019). Dehydroepiandrosterone and cortisol as markers of HPA axis dysregulation in women with low sexual desire. Psychoneuroendocrinology 104:259-268.
  13. Holman PJ, Baglot SL, Morgan E, Weinberg J. (2019). Effects of prenatal alcohol exposure on social competence: Asymmetry in play partner preference among heterogeneous triads of male and female rats. Dev Psychobiol 61:513-524.
  14. Eid RS, Chaiton JA, Lieblich SE, Bodnar TS, Weinberg J, Galea LAM. (2019). Early and late effects of maternal experience on hippocampal neurogenesis, microglia, and the circulating cytokine milieu. Neurobiol Aging. 2019 Jun;78:1-17. doi: 10.1016/j.neurobiolaging.2019.01.021.
  15. Bodnar TS, Raineki C, Wertelecki W, Yevtushok L, Plotka L, Granovska I, Zymak-Zakutnya N, Pashtepa A, Wells A, Honerkamp-Smith G, Coles CD, Kable JA, Chambers CD, Weinberg J, the CIFASD. (2020). Immune network dysregulation associated with child neurodevelopmental delay: Modulatory role of prenatal alcohol exposure. Journal of Neuroinflammation, 17:39. PMID: 31992316; PMICD: PMC6988366
  16. McLean, MA, Niknafs, N, Scoten, OC, Chau, CMY, MacKay, M, Weinberg, J, Synnes, A, Miller, SP, Grunau, RE. (2020). Sensory processing and cortisol at age 4 years: Procedural pain‐related stress in children born very preterm. Dev Psychobiol, Early View 29 December 2020 https://doi.org/10.1002/dev.22079.
  17. Mclean MA, Scoten OC, Yu W, Ye XY, Petrie J, Church PT, Soraisham AS, Mirea LS, Weinberg J, Synnes AR, O’Brien K, Grunau RE. Lower maternal chronic physiological stress and better child behavior at 18 months: Follow-up of a cluster randomized trial of neonatal intensive care unit family integrated care. J Pediatr. 2021 Dec 29:S0022-3476(21)01262-2. doi: 10.1016/j.jpeds.2021.12.055. PMID: 34971651
  18. Holman, P.J., Raineki, C., Chao, A., Grewal, R., Haghighat, S., Fung, C., Morgan, E., Ellis, L., Yu, W., Weinberg, J., 2021. Altered social recognition memory and hypothalamic neuropeptide expression in adolescent male and female rats following prenatal alcohol exposure and/or early-life adversity. Psychoneuroendocrinology 105146. https://doi.org/10.1016/j.psyneuen.2021.105146
  19. Lussier, A.A., Bodnar, T.S., Weinberg, J. Intersection of epigenetic and immune alterations: Implications for Fetal Alcohol Spectrum Disorder and mental health. Front. Neurosci., 03 December 2021 | https://doi.org/10.3389/fnins.2021.788630
  20. Lussier, A.A., Bodnar, T.S., Moksa, M., Hirst, M., Kobor, M.S., Weinberg, J. Prenatal adversity alters the epigenetic profile of the prefrontal cortex: Sexually dimorphic effects of prenatal alcohol exposure and food-related stress. Genes 2021, 12,1773. https://doi.org/10.3390/genes12111773
  21. Brotto LA, Zdaniuk B, Chivers ML, Jabs F, Grabovac A, Lalumière ML, Weinberg J, Schonert-Reichl KA, Basson R. A randomized trial comparing group mindfulness-based cognitive therapy with group supportive sex education and therapy for the treatment of female sexual interest/arousal disorder. J Consult Clin Psychol. 89:626-639, 2021. doi: 10.1037/ccp0000661. PMID: 34383535
  22. Bodnar, T.S., Mak, D., Hill, L.A., Ellis, L., Yu, W., Weinberg, J. Modulatory role of prenatal alcohol exposure and adolescent stress on the response to arthritis challenge in adult female rats. eBioMedicine 2022;77:103876. https://doi.org/10.1016/j.ebiom.2022.103876
  23. Bodnar, T.S., Lee, C., Wong, A., Rubin, I., Parfrey, L.W. Weinberg, J. Evidence for long-lasting alterations in the fecal microbiota following prenatal alcohol exposure. Alcohol Clin Exp Res, published online 17 February, 2022. https://doi.org/10.1111/acer.14784
  24. Clephane, K., O’Loughlin, J.I., Bodnar, T.S., Wilson, M.C., Stariha, J.T.B., Craig, A.N., Weinberg, J., Brotto, L.A., Lorenz,T.K. Lack of evidence for a relationship between salivary CRP and women’s sexual desire: An investigation across clinical and healthy samples. J.Sexual Med 2022 May;19(5):745-760. doi: 10.1016/j.jsxm.2022.02.007. Epub 2022 Mar 13.
  25. Baker, J.A., Breit, K.R., Bodnar, T.S., Weinberg J., Thomas, J.D. Choline supplementation modifies the effects of developmental alcohol exposure on immune responses in adult rats. Nutrients 2022 Jul 13;14(14):2868. doi: 10.3390/nu14142868.
  26. Baker, J.A., Bodnar, T.S., Breit, K.R., Weinberg, J., Thomas, J.D. Choline supplementation alters hippocampal cytokine levels in adolescence and adulthood in an animal model of fetal alcohol spectrum disorder. Cells 2023 Feb 8;12(4):546. doi: 10.3390/cells12040546.
  27. McLean, M.A., Nakajima, L., Chau, C.M.Y., Weinberg, J., Synnes, A.R., Miller, S.P., Grunau, R.E. Cortisol levels are related to neonatal pain exposure in children born very preterm at age 18 months in two independent cohorts. Pediatric & Neonatal Pain. Paediatr Neonatal Pain. 2023;5:86–95.
  28. Ulziikhuu, B., Gombojav, E., Banzrai, C., Batsukh, S., Enkhtuya, E., Boldbaatar, B., Bellinger, D.C., Lanphear, B.P., McCandless, L.C., Nepomnaschy, P., Salvante, K., Weinberg, J., Allen, R.W. Who benefits most from a prenatal HEPA filter air cleaner intervention on childhood cognitive development? The UGAAR randomized controlled trial. Environ Res. 2023 Apr 29;231(Pt 1):115991.
  29. Bodnar, TS, Chao, A, Holman, PJ, Ellis,L, Raineki, C, Weinberg, J. Impact of the COVID-19 pandemic on adults with Fetal Alcohol Spectrum Disorder (FASD): Linking immune function to mental health status. Front. Neurosci. 17:1214100. doi: 10.3389/fnins.2023.121410
  30. Maxwell, JR, DiDomenico J, Roberts MH, Marquez LE, Rai R, Weinberg J, Jacobson, SW, Stephen J, Bakhireva LN. Impact of low-level prenatal alcohol exposure and maternal stress on autonomic regulation. Pediatr Res (2023). https://doi.org/10.1038/s41390-023-02799-5
  31. Zusman, EZ, Chau, CMY, Bone, JM, Hookenson, K, Brain, U, Glier, MB, Grunau, RE, Weinberg, J, Devlin, AM, Oberlander, TF. Prenatal serotonin reuptake inhibitor antidepressant exposure, SLC6A4 genetic variations, and cortisol activity in 6-year-old children of depressed mothers: A cohort study, Dev Psychobiol 2023;65:e22425. https://doi.org/10.1002/dev.22425.
  32. Mclean, M.A., Weinberg, J., Synnes, A.R., Miller, S.P., Grunau, R.E. (2024) Relationships between cortisol levels across early childhood and processing speed at age 4.5 years in children born very preterm. Child Neuropsychology 2024 Feb 26:1-19. doi: 10.1080/09297049.2024.2314958. Online ahead of print.PMID: 38406870
Further publications can be found here.
Images
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Detection of glucocorticoid mRNA by in situ hybridization.