Table of Contents Author Guidelines Submit a Manuscript
Parkinson’s Disease
Volume 2016, Article ID 9869712, 15 pages
http://dx.doi.org/10.1155/2016/9869712
Review Article

An Integrated Review of Psychological Stress in Parkinson’s Disease: Biological Mechanisms and Symptom and Health Outcomes

1Virginia Commonwealth University School of Nursing, 1100 East Leigh Street, Richmond, VA 23219, USA
2Virginia Commonwealth University Parkinson’s and Movement Disorders Center and VCU Health Neuroscience, Orthopaedic, and Wellness Center, 11958 West Broad Street, Richmond, VA 23233, USA

Received 8 May 2016; Revised 28 September 2016; Accepted 1 November 2016

Academic Editor: Elka Stefanova

Copyright © 2016 Kim Wieczorek Austin et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Antonini, P. Barone, R. Marconi et al., “The progression of non-motor symptoms in Parkinsons disease and their contribution to motor disability and quality of life,” Journal of Neurology, vol. 259, pp. 2621–2631, 2012. View at Google Scholar
  2. C. C. Aquino and S. H. Fox, “Clinical spectrum of levodopa-induced complications,” Movement Disorders, vol. 30, no. 1, pp. 80–89, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. M. S. Clark, M. J. Bond, and J. R. Hecker, “Environmental stress, psychological stress and allostatic load,” Psychology, Health and Medicine, vol. 12, no. 1, pp. 18–30, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. T. H. Holmes and R. H. Rahe, “The social readjustment rating scale,” Journal of Psychosomatic Research, vol. 11, no. 2, pp. 213–218, 1967. View at Publisher · View at Google Scholar · View at Scopus
  5. J. K. Kiecolt-Glaser, L. McGuire, T. F. Robles, and R. Glaser, “Emotions, morbidity, and mortality: new perspectives from psychoneuroimmunology,” Annual Review of Psychology, vol. 53, pp. 83–107, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Sorenson, L. Janusek, and H. Mathews, “Psychological stress and cytokine production in multiple sclerosis: correlation with disease symptomatology,” Biological Research for Nursing, vol. 15, no. 2, pp. 226–233, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. M. C. Davis, A. J. Zautra, and J. W. Reich, “Vulnerability to stress among women in chronic pain from fibromyalgia and osteoarthritis,” Annals of Behavioral Medicine, vol. 23, no. 3, pp. 215–226, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. A. W. M. Evers, E. W. M. Verhoeven, H. Van Middendorp et al., “Does stress affect the joints? Daily stressors, stress vulnerability, immune and HPA axis activity, and short-term disease and symptom fluctuations in rheumatoid arthritis,” Annals of the Rheumatic Diseases, vol. 73, no. 9, pp. 1683–1688, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. T. E. Seeman, B. H. Singer, J. W. Rowe, R. I. Horwitz, and B. S. McEwen, “Price of adaptation—allostatic load and its health consequences,” Archives of Internal Medicine, vol. 157, no. 19, pp. 2259–2268, 1997. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Kulmala, M. B. von Bonsdorff, S. Stenholm et al., “Perceived stress symptoms in midlife predict disability in old age: a 28-year prospective cohort study,” The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, vol. 68, no. 8, pp. 984–991, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. N. L. McCain, D. P. Gray, J. M. Walter, and J. Robins, “Implementing a comprehensive approach to the study of health dynamics using the psychoneuroimmunology paradigm,” Advances in Nursing Science, vol. 28, no. 4, pp. 320–332, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. F. S. Dhabhar, “Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection and immunopathology,” NeuroImmunoModulation, vol. 16, no. 5, pp. 300–317, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. C. J. Barnum, T. W. W. Pace, F. Hu, G. N. Neigh, and M. G. Tansey, “Psychological stress in adolescent and adult mice increases neuroinflammation and attenuates the response to LPS challenge,” Journal of Neuroinflammation, vol. 9, article 9, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. R. M. De Pablos, R. F. Villarán, S. Argüelles et al., “Stress increases vulnerability to inflammation in the rat prefrontal cortex,” Journal of Neuroscience, vol. 26, no. 21, pp. 5709–5719, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. M. G. Frank, M. V. Baratta, D. B. Sprunger, L. R. Watkins, and S. F. Maier, “Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses,” Brain, Behavior, and Immunity, vol. 21, no. 1, pp. 47–59, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. M. G. Frank, B. M. Thompson, L. R. Watkins, and S. F. Maier, “Glucocorticoids mediate stress-induced priming of microglial pro-inflammatory responses,” Brain, Behavior, and Immunity, vol. 26, no. 2, pp. 337–345, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. J. L. M. Madrigal, B. García-Bueno, J. R. Caso, B. G. Pérez-Nievas, and J. C. Leza, “Stress-induced oxidative changes in brain,” CNS and Neurological Disorders—Drug Targets, vol. 5, no. 5, pp. 561–568, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. C. D. Munhoz, L. B. Lepsch, E. M. Kawamoto et al., “Chronic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-κB in the frontal cortex and hippocampus via glucocorticoid secretion,” The Journal of Neuroscience, vol. 26, no. 14, pp. 3813–3820, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. J. B. Buchanan, N. L. Sparkman, J. Chen, and R. W. Johnson, “Cognitive and neuroinflammatory consequences of mild repeated stress are exacerbated in aged mice,” Psychoneuroendocrinology, vol. 33, no. 6, pp. 755–765, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. M. G. Frank, S. A. Hershman, M. D. Weber, L. R. Watkins, and S. F. Maier, “Chronic exposure to exogenous glucocorticoids primes microglia to pro-inflammatory stimuli and induces NLRP3 mRNA in the hippocampus,” Psychoneuroendocrinology, vol. 40, no. 1, pp. 191–200, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. M. L. Block, L. Zecca, and J.-S. Hong, “Microglia-mediated neurotoxicity: uncovering the molecular mechanisms,” Nature Reviews Neuroscience, vol. 8, no. 1, pp. 57–69, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. H. A. Jurgens and R. W. Johnson, “Dysregulated neuronal–microglial cross-talk during aging, stress and inflammation,” Experimental Neurology, vol. 233, no. 1, pp. 40–48, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. H.-M. Gao, J. Jiang, B. Wilson, W. Zhang, J.-S. Hong, and B. Liu, “Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to parkinson's disease,” Journal of Neurochemistry, vol. 81, no. 6, pp. 1285–1297, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. G. Lucca, C. M. Comim, S. S. Valvassori et al., “Increased oxidative stress in submitochondrial particles into the brain of rats submitted to the chronic mild stress paradigm,” Journal of Psychiatric Research, vol. 43, no. 9, pp. 864–869, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. J. S. Myers, “Proinflammatory cytokines and sickness behavior: implications for depression and cancer-related symptoms,” Oncology Nursing Forum, vol. 35, no. 5, pp. 802–807, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Munhoz, J. L. M. Madrigal, B. García-Bueno et al., “TNF-α accounts for short-term persistence of oxidative status in rat brain after two weeks of repeated stress,” European Journal of Neuroscience, vol. 20, no. 4, pp. 1125–1130, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. J.-P. Gouin, R. Glaser, W. B. Malarkey, D. Beversdorf, and J. Kiecolt-Glaser, “Chronic stress, daily stressors, and circulating inflammatory markers,” Health Psychology, vol. 31, no. 2, pp. 264–268, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Holmin and T. Mathiesen, “Intracerebral administration of interleukin-1β and induction of inflammation, apoptosis, and vasogenic edema,” Journal of Neurosurgery, vol. 92, no. 1, pp. 108–120, 2000. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Zhou, A. W. Kusnecov, M. R. Shurin, M. DePaoli, and B. S. Rabin, “Exposure to physical and psychological stressors elevates plasma interleukin 6: Relationship to the activation of hypothalamic-pituitary-adrenal axis,” Endocrinology, vol. 133, no. 6, pp. 2523–2530, 1993. View at Publisher · View at Google Scholar · View at Scopus
  30. J. L. M. Madrigal, O. Hurtado, M. A. Moro et al., “The increase in TNF-α levels is implicated in NF-κB activation and inducible nitric oxide synthase expression in brain cortex after immobilization stress,” Neuropsychopharmacology, vol. 26, no. 2, pp. 155–163, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Bierhaus, J. Wolf, M. Andrassy et al., “A mechanism converting psychosocial stress into mononuclear cell activation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 4, pp. 1920–1925, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. Z.-Q. Liang, Y.-L. Li, X.-L. Zhao et al., “NF-κB contributes to 6-hydroxydopamine-induced apoptosis of nigral dopaminergic neurons through p53,” Brain Research, vol. 1145, no. 1, pp. 190–203, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. J. L. M. Madrigal, M. A. Moro, I. Lizasoain et al., “Induction of cyclooxygenase-2 accounts for restraint stress-induced oxidative status in rat brain,” Neuropsychopharmacology, vol. 28, no. 9, pp. 1579–1588, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Vesce, D. Rossi, L. Brambilla, and A. Volterra, “Glutamate release from astrocytes in physiological conditions and in neurodegenerative disorders characterized by neuroinflammation,” International Review of Neurobiology, vol. 82, pp. 57–71, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Yamagata, K. I. Andreasson, W. E. Kaufmann, C. A. Barnes, and P. F. Worley, “Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids,” Neuron, vol. 11, no. 2, pp. 371–386, 1993. View at Publisher · View at Google Scholar · View at Scopus
  36. S. R. Subramaniam and M.-F. Chesselet, “Mitochondrial dysfunction and oxidative stress in Parkinson's disease,” Progress in Neurobiology, vol. 106-107, pp. 17–32, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Valko, D. Leibfritz, J. Moncol, M. T. D. Cronin, M. Mazur, and J. Telser, “Free radicals and antioxidants in normal physiological functions and human disease,” The International Journal of Biochemistry & Cell Biology, vol. 39, no. 1, pp. 44–84, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. G. Lucca, C. M. Comim, S. S. Valvassori et al., “Effects of chronic mild stress on the oxidative parameters in the rat brain,” Neurochemistry International, vol. 54, no. 5-6, pp. 358–362, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. H.-M. Gao, H. Zhou, and J.-S. Hong, “NADPH oxidases: novel therapeutic targets for neurodegenerative diseases,” Trends in Pharmacological Sciences, vol. 33, no. 6, pp. 295–303, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. I. Paduraru, O. Paduraru, G. Manolidis, W. Bild, and I. Haulica, “Antioxidant activity in rat models of nociceptive stress,” Revista medico-chirurgicala a Societaţii de Medici si Naturalisti din Iasi, vol. 114, no. 1, pp. 175–179, 2010. View at Google Scholar · View at Scopus
  41. S. T. Kim, J. H. Choi, J. W. Chang, S. W. Kim, and O. Hwang, “Immobilization stress causes increases in tetrahydrobiopterin, dopamine, and neuromelanin and oxidative damage in the nigrostriatal system,” Journal of Neurochemistry, vol. 95, no. 1, pp. 89–98, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. D. T. Dextera and P. Jenner, “Parkinson disease: from pathology to molecular disease mechanisms,” Free Radical Biology and Medicine, vol. 62, pp. 132–144, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Gerhard, N. Pavese, G. Hotton et al., “In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson's disease,” Neurobiology of Disease, vol. 21, no. 2, pp. 404–412, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. Y. Ouchi, E. Yoshikawa, Y. Sekine et al., “Microglial activation and dopamine terminal loss in early Parkinson's disease,” Annals of Neurology, vol. 57, no. 2, pp. 168–175, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. A. M. Depino, C. Earl, E. Kaczmarczyk et al., “Microglial activation with atypical proinflammatory cytokine expression in a rat model of Parkinson's disease,” European Journal of Neuroscience, vol. 18, no. 10, pp. 2731–2742, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. P. Scalzo, A. Kümmer, F. Cardoso, and A. L. Teixeira, “Serum levels of interleukin-6 are elevated in patients with Parkinson's disease and correlate with physical performance,” Neuroscience Letters, vol. 468, no. 1, pp. 56–58, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Reale, C. Iarlori, A. Thomas et al., “Peripheral cytokines profile in Parkinson's disease,” Brain, Behavior, and Immunity, vol. 23, no. 1, pp. 55–63, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. J. C. Tobón-Velasco, J. H. Limón-Pacheco, M. Orozco-Ibarra et al., “6-OHDA-induced apoptosis and mitochondrial dysfunction are mediated by early modulation of intracellular signals and interaction of Nrf2 and NF-κB factors,” Toxicology, vol. 304, pp. 109–119, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. P. Teismann, K. Tieu, D.-K. Choi et al., “Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 9, pp. 5473–5478, 2003. View at Publisher · View at Google Scholar
  50. M. S. Hernandes, C. C. Café-Mendes, and L. R. G. Britto, “NADPH oxidase and the degeneration of dopaminergic neurons in Parkinsonian mice,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 157857, 13 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. T.-K. Lin, C.-H. Cheng, S.-D. Chen, C.-W. Liou, C.-R. Huang, and Y.-C. Chuang, “Mitochondrial dysfunction and oxidative stress promote apoptotic cell death in the striatum via cytochrome c/caspase-3 signaling cascade following chronic rotenone intoxication in rats,” International Journal of Molecular Sciences, vol. 13, no. 7, pp. 8722–8739, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. R. C. S. Seet, C.-Y. J. Lee, E. C. H. Lim et al., “Oxidative damage in Parkinson disease: measurement using accurate biomarkers,” Free Radical Biology & Medicine, vol. 48, no. 4, pp. 560–566, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. P. M. Keeney, J. Xie, R. A. Capaldi, and J. P. Bennett Jr., “Parkinson's disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled,” The Journal of Neuroscience, vol. 26, no. 19, pp. 5256–5264, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. D. Lindqvist, E. Kaufman, L. Brundin, S. Hall, Y. Surova, and O. Hansson, “Non-motor symptoms in patients with Parkinson's disease—correlations with inflammatory cytokines in serum,” PLoS ONE, vol. 7, no. 10, Article ID e47387, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. U. Janakiraman, T. Manivasagam, A. J. Thenmozhi et al., “Influences of chronic mild stress exposure on motor, non-motor impairments and neurochemical variables in specific brain areas of mptp/probenecid induced neurotoxicity in mice,” PLoS ONE, vol. 11, no. 1, Article ID e0146671, 2016. View at Publisher · View at Google Scholar · View at Scopus
  56. A. M. Hemmerle, J. W. Dickerson, J. P. Herman, and K. B. Seroogy, “Stress exacerbates experimental Parkinson's disease,” Molecular Psychiatry, vol. 19, no. 6, pp. 638–640, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. L. K. Smith, N. M. Jadavji, K. L. Colwell, S. K. Perehudoff, and G. A. Metz, “Stress accelerates neural degeneration and exaggerates motor symptoms in a rat model of Parkinson's disease,” European Journal of Neuroscience, vol. 27, no. 8, pp. 2133–2146, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. F. M. Howells, V. A. Russell, M. V. Mabandla, and L. A. Kellaway, “Stress reduces the neuroprotective effect of exercise in a rat model for Parkinson's disease,” Behavioural Brain Research, vol. 165, no. 2, pp. 210–220, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. K. A. Keefe, E. M. Stricker, M. J. Zigmond, and E. D. Abercrombie, “Environmental stress increases extracellular dopamine in striatum of 6-hydroxydopamine-treated rats: in vivo microdialysis studies,” Brain Research, vol. 527, no. 2, pp. 350–353, 1990. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Urakami, N. Masaki, K. Shimoda, S. Nishikawa, and K. Takahashi, “Increase of striatal dopamine turnover by stress in MPTP-treated mice,” Clinical Neuropharmacology, vol. 11, no. 4, pp. 360–368, 1988. View at Publisher · View at Google Scholar · View at Scopus
  61. A. M. Snyder, E. M. Stricker, and M. J. Zigmond, “Stress-induced neurological impairments in an animal model of parkinsonism,” Annals of Neurology, vol. 18, no. 5, pp. 544–551, 1985. View at Publisher · View at Google Scholar · View at Scopus
  62. E. Giza, Z. Katsarou, G. Georgiadis, and S. Bostantjopoulou, “Sympathetic skin response in Parkinson's disease before and after mental stress,” Clinical Neurophysiology, vol. 42, no. 3, pp. 125–131, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Rahman, H. J. Griffin, N. P. Quinn, and M. Jahanshahi, “The factors that induce or overcome freezing of gait in Parkinson's disease,” Behavioural Neurology, vol. 19, no. 3, pp. 127–136, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. M. Macht, S. Brandstetter, and H. Ellgring, “Stress affects hedonic responses but not reaching-grasping in Parkinson's disease,” Behavioural Brain Research, vol. 177, no. 1, pp. 171–174, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Macht, R. Schwarz, and H. Ellgring, “Patterns of psychological problems in Parkinson's disease,” Acta Neurologica Scandinavica, vol. 111, no. 2, pp. 95–101, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Akhtar, “The flaws and human harms of animal experimentation,” Cambridge Quarterly of Healthcare Ethics, vol. 24, no. 4, pp. 407–419, 2015. View at Publisher · View at Google Scholar · View at Scopus
  67. D. G. Hachman, “Translating animal research into clinical benefit,” British Medical Journal, vol. 334, article 163, 2007. View at Publisher · View at Google Scholar
  68. M. I. Martić-Kehl, R. Schibli, and P. A. Schubiger, “Can animal data predict human outcome? Problems and pitfalls of translational animal research,” European Journal of Nuclear Medicine and Molecular Imaging, vol. 39, no. 9, pp. 1492–1496, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. S. K. Jääskeläinen, P. Lindholm, T. Valmunen et al., “Variation in the dopamine D2 receptor gene plays a key role in human pain and its modulation by transcranial magnetic stimulation,” Pain, vol. 155, no. 10, pp. 2180–2187, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. P. J. Schwartz and S. D. Erk, “Regulation of central dopamine-2 receptor sensitivity by a proportional control thermostat in humans,” Psychiatry Research, vol. 127, no. 1-2, pp. 19–26, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. N. K. Leidy, “A physiologic analysis of stress and chronic illness,” Journal of Advanced Nursing, vol. 14, no. 10, pp. 868–876, 1989. View at Publisher · View at Google Scholar · View at Scopus
  72. J. K. Kiecolt-Glaser, L. McGuire, T. F. Robles, and R. Glaser, “Psychoneuroimmunology: psychological influences on immune function and health,” Journal of Consulting and Clinical Psychology, vol. 70, no. 3, pp. 537–547, 2002. View at Publisher · View at Google Scholar · View at Scopus
  73. A. M. Espinosa-Oliva, R. M. de Pablos, R. F. Villarán et al., “Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus,” Neurobiology of Aging, vol. 32, no. 1, pp. 85–102, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. E. Izzo, P. P. Sanna, and G. F. Koob, “Impairment of dopaminergic system function after chronic treatment with corticotropin-releasing factor,” Pharmacology, Biochemistry, and Behavior, vol. 81, no. 4, pp. 701–708, 2005. View at Publisher · View at Google Scholar · View at Scopus