Shared pathological mechanisms of systemic lupus erythematosus and affective disorders

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Abstract

The high prevalence and variability of neurological and psychiatric symptoms in systemic lupus erythematosus has become the basis for emphasizing the special neuropsychiatric form of the disorder. Affective disorders (pathological changes in mood and anxiety) are the second most common neuropsychiatric manifestations in patients with systemic lupus erythematosus. However, the current nomenclature primarily focuses on the general clinical manifestations of affective disorders in neuropsychiatric form systemic lupus erythematosus, without evaluating the problems of their etiopathogenesis. Thereby, the aim of this review is the integration of information on the pathological mechanisms of depression and anxiety in patients with systemic lupus erythematosus. The available data on the biological aspects of the anxiety and depression in systemic lupus erythematosus indicate that the complex pathological models may be the best approach for studying, diagnosing, and treating comorbid pathology. The latter can be based on expanding the existing clinical categories, supplementing them with data on pathological mechanisms specific to particular sub-cohorts of patients. Such an approach can provide the specific and most effective preventive, diagnostic and therapeutic measures for each category of patients.

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About the authors

Grigory V. Rukavishnikov

V.M. Bekhterev National Medical Research Center for Psychiatry and Neurology

Author for correspondence.
Email: grigory_v_r@mail.ru
ORCID iD: 0000-0002-5282-2036

MD, Cand. Sci. (Med.)

Russian Federation, 3 Bekhtereva str., Saint Petersburg, 192019

Anna A. Smirnova

V.M. Bekhterev National Medical Research Center for Psychiatry and Neurology

Email: annakaraseva37@mail.ru
ORCID iD: 0000-0002-4703-0712
Russian Federation, 3 Bekhtereva str., Saint Petersburg, 192019

Nikolay G. Neznanov

V.M. Bekhterev National Medical Research Center for Psychiatry and Neurology; I.P. Pavlov First Saint Petersburg State Medical University

Email: spbinstb@bekhterev.ru
ORCID iD: 0000-0001-5618-4206

MD, Dr. Sci. (Med.), Professor

Russian Federation, 3 Bekhtereva str., Saint Petersburg, 192019; Saint Petersburg

Vadim I. Mazurov

North-Western State Medical University named after I.I. Mechnikov

Email: maz.nwgmu@yandex.ru
ORCID iD: 0000-0002-0797-2051
SPIN-code: 6823-5482
Scopus Author ID: 16936315400
ResearcherId: A-8944-2016

MD, Dr. Sci. (Med.), Professor, Honoured Science Worker, Academician of the RAS

Russian Federation, 41 Kirochnaya str., Saint Petersburg, 191015

Galina E. Mazo

V.M. Bekhterev National Medical Research Center for Psychiatry and Neurology

Email: galina-mazo@yandex.ru
ORCID iD: 0000-0001-7036-5927

MD, Dr. Sci. (Med.)

Russian Federation, 3 Bekhtereva str., Saint Petersburg, 192019

References

  1. Postal M, Lapa AT, Sinicato NA, et al. Depressive symptoms are associated with tumor necrosis factor alpha in systemic lupus erythematosus. J Neuroinflammation. 2016;13:5. doi: 10.1186/s12974-015-0471-9
  2. Zhang L, Fu T, Yin R, et al. Prevalence of depression and anxiety in systemic lupus erythematosus: a systematic review and meta-analysis. BMC Psychiatry. 2017;17(1):70. doi: 10.1186/s12888-017-1234-1
  3. Primer on the Rheumatic Diseases. J.H. Klippel, J.H. Stone, L.J. Crofford, P.H. White (eds). Springer; 2008. doi: 10.1007/978-0-387-68566-3
  4. Hawro T, Krupińska-Kun M, Rabe-Jabłońska J, et al. Psychiatric disorders in patients with systemic lupus erythematosus: association of anxiety disorder with shorter disease duration. Rheumatol Int. 2011;31(10):1387–1391. doi: 10.1007/s00296-010-1689-6
  5. Kwan A, Katz P, Touma Z. The assessment of anxiety and depression and its associated factors in SLE. Curr Rheumatol Rev. 2019;15(2):90–98. doi: 10.2174/1573397114666180926101513
  6. Seawell AH, Danoff-Burg S. Body image and sexuality in women with and without systemic lupus erythematosus. Sex Roles. 2005;53(11):865–876. doi: 10.1007/s11199-005-8298-y
  7. Vivaldo JF, de Amorim JC, Julio PR, et al. Definition of NPSLE: Does the ACR nomenclature still hold? Front Med (Lausanne). 2018;5:138. doi: 10.3389/fmed.2018.00138
  8. Alsowaida N, Alrasheed M, Mayet A, et al. Medication adherence, depression and disease activity among patients with systemic lupus erythematosus. Lupus. 2018;27(2):327–332. doi: 10.1177/0961203317725585
  9. Palagini L, Mosca M, Tani C, et al. Depression and systemic lupus erythematosus: a systematic review. Lupus. 2013;22(5):409–416. doi: 10.1177/0961203313477227
  10. Xu J, Cheng YQ, Chen B, et al. Depression in systemic lupus erythematosus patients is associated with link-polymorphism but not methylation status of the 5HTT promoter region. Lupus. 2013;22(10):1001–1010. doi: 10.1177/0961203313498793
  11. Jeltsch-David H, Muller S. Neuropsychiatric systemic lupus erythematosus: pathogenesis and biomarkers. Nat Rev Neurol. 2014;10(10):579–596. doi: 10.1038/nrneurol.2014.148
  12. Dantzer R. Cytokine, sickness behavior, and depression. Immunol Allergy Clin North Am. 2009;29(2):247–264. doi: 10.1016/j.iac.2009.02.002
  13. Khairova RA, Machado-Vieira R, Du J, Manji HK. A potential role for pro-inflammatory cytokines in regulating synaptic plasticity in major depressive disorder. Int J Neuropsychopharmacol. 2009;12(4):561–578. doi: 10.1017/S1461145709009924
  14. Ménard C, Hodes GE, Russo SJ. Pathogenesis of depression: Insights from human and rodent studies. Neuroscience. 2016;321:138–162. doi: 10.1016/j.neuroscience.2015.05.053
  15. Krishnadas R, Cavanagh J. Depression: an inflammatory illness? J Neurol Neurosurg Psychiatry. 2012;83(5):495–502. doi: 10.1136/jnnp-2011-301779
  16. Himmerich H, Fulda S, Linseisen J, et al. Depression, comorbidities and the TNF-alpha system. Eur Psychiatry. 2008;23(6):421–429. doi: 10.1016/j.eurpsy.2008.03.013
  17. Berthold-Losleben M, Himmerich H. The TNF-alpha system: functional aspects in depression, narcolepsy and psychopharmacology. Curr Neuropharmacol. 2008;6(3):193–202. doi: 10.2174/157015908785777238
  18. Doczy EJ, Seroogy K, Harrison CR, Herman JP. Hypothalamo-pituitary-adrenocortical axis, glucocorticoids, and neurologic disease. Immunol Allergy Clin North Am. 2009;29(2):265–284. doi: 10.1016/j.iac.2009.02.003
  19. Black PH. Immune system-central nervous system interactions: effect and immunomodulatory consequences of immune system mediators on the brain. Antimicrob Agents Chemother. 1994;38(1):7–12. doi: 10.1128/AAC.38.1.7
  20. Vallieres L, Rivest S. Interleukin-6 is a needed proinflammatory cytokine in the prolonged neural activity and transcriptional activation of corticotropinreleasing factor during endotoxemia. Endocrinology. 1999;140(9):3890–3903. doi: 10.1210/endo.140.9.6983
  21. Chrousos GP. The hypothalamic-pituitary-adrenal axis and immunemediated inflammation. N Engl J Med. 1995;332(20):1351–1362. doi: 10.1056/NEJM199505183322008
  22. McCann SM, Lyson K, Karanth S, et al. Mechanism of action of cytokines to induce the pattern of pituitary hormone secretion in infection. Ann N Y Acad Sci. 1995;771:386–395. doi: 10.1111/j.1749-6632.1995.tb44697.x
  23. Dantzer R, Wollman E, Vitkovic L, Yirmiya R. Cytokines and depression: fortuitous or causative association? Mol Psychiatry. 1999;4(4):328–332. doi: 10.1038/sj.mp.4000572
  24. Dowlati Y, Herrmann N, Swardfager W, et al. A meta-analysis of cytokines in major depression. Biol Psychiatry. 2010;67(5):446–457. doi: 10.1016/j.biopsych.2009.09.033
  25. Zhu CB, Blakely RD, Hewlett WA. The proinflammatory cytokines interleukin-1beta and tumor necrosis factor-alpha activate serotonin transporters. Neuropsychopharmacology. 2006;31(10):2121–2131. doi: 10.1038/sj.npp.1301029
  26. Müller N, Schwarz MJ. Immunologische Aspekte bei depressiven Störungen [Immunological aspects of depressive disorders]. Nervenarzt. 2007;78(11):1261–1273. (In German). doi: 10.1007/s00115-007-2311-3
  27. Wichers M, Maes M. The psychoneuroimmuno-pathophysiology of cytokine-induced depression in humans. Int J Neuropsychopharmacol. 2002;5(4):375–388. doi: 10.1017/S1461145702003103
  28. Himmerich H, Fulda S, Linseisen J, et al. Depression, comorbidities and the TNF-alpha system. Eur Psychiatry. 2008;23(6):421–429. doi: 10.1016/j.eurpsy.2008.03.013
  29. Lang UE, Borgwardt S. Molecular mechanisms of depression: perspectives on new treatment strategies. Cell Physiol Biochem. 2013;31(6):761–777. doi: 10.1159/000350094
  30. Tisseverasinghe A, Peschken C, Hitchon C. Anxiety and mood disorders in systemic lupus erythematosus: current insights and future directions. Curr Rheumatol Rep. 2018;20(12):85. doi: 10.1007/s11926-018-0797-2
  31. Seth G, Sundaresh A, Mariaselvam CM, et al. Immunological biomarkers in neuropsychiatric systemic lupus erythematosus: a comparative cross-sectional study from a tertiary care center in South India. Lupus. 2020;29(4):413–420. doi: 10.1177/0961203320908940
  32. Figueiredo-Braga M, Cornaby C, Cortez A, et al. Depression and anxiety in systemic lupus erythematosus: The crosstalk between immunological, clinical, and psychosocial factors. Medicine (Baltimore). 2018;97(28):e11376. doi: 10.1097/MD.0000000000011376
  33. Zheng Q, Xu MJ, Cheng J, et al. Serum levels of brain-derived neurotrophic factor are associated with depressive symptoms in patients with systemic lupus erythematosus. Psychoneuroendocrinology. 2017;78:246–252. doi: 10.1016/j.psyneuen.2016.12.001
  34. Ikenouchi-Sugita A, Yoshimura R, Okamoto T, et al. Serum brain-derived neurotrophic factor levels as a novel biological marker for the activities of psychiatric symptoms in systemic lupus erythematosus. World J Biol Psychiatry. 2010;11(2):121–128. doi: 10.3109/15622970903521131
  35. Lahita RG, Bradlow HL, Kunkel HG, Fishman J. Alterations of estrogen metabolism in systemic lupus erythematosus. Arthritis Rheum. 1979;22(11):1195–1198. doi: 10.1002/art.1780221106
  36. Khan WA, Zaman GS, Alouffi S, Khan MWA. Depression and its related parameters increased the production of autoantibodies against 16α-hydroxyestrone-albumin complex in systemic lupus erythematosus. Int Immunopharmacol. 2019;71:215–223. doi: 10.1016/j.intimp.2019.03.036
  37. Weidler C, Härle P, Schedel J, et al. Patients with rheumatoid arthritis and systemic lupus erythematosus have increased renal excretion of mitogenic estrogens in relation to endogenous antiestrogens. J Rheumatol. 2004;31(3):489–494.
  38. Reichlin S. Prolactin and growth hormone secretion in stress. Adv Exp Med Biol. 1988;245:353–376. doi: 10.1007/978-1-4899-2064-5_28
  39. Dorshkind K, Horseman ND. The roles of prolactin, growth hormone, insulin-like growth factor-I, and thyroid hormones in lymphocyte development and function: insights from genetic models of hormone and hormone receptor deficiency. Endocr Rev. 2000;21(3):292–312. doi: 10.1210/edrv.21.3.0397
  40. Torner L, Toschi N, Pohlinger A, et al. Anxiolytic and anti-stress effects of brain prolactin: improved efficacy of antisense targeting of the prolactin receptor by molecular modeling. J Neurosci. 2001;21(9):3207–3214. doi: 10.1523/JNEUROSCI.21-09-03207.2001
  41. Torner L, Neumann ID. The brain prolactin system: involvement in stress response adaptations in lactation. Stress. 2002;5(4):249–257. doi: 10.1080/1025389021000048638
  42. Yu-Lee LY. Prolactin modulation of immune and inflammatory responses. Recent Prog Horm Res. 2002;57:435–455. doi: 10.1210/rp.57.1.435
  43. Cook CJ. Oxytocin and prolactin suppress cortisol responses to acute stress in both lactating and non-lactating sheep. J Dairy Res. 1997;64(3):327–339. doi: 10.1017/s0022029997002240
  44. Jara LJ, Medina G, Saavedra MA, et al. Prolactin has a pathogenic role in systemic lupus erythematosus. Immunol Res. 2017;65(2):512–523. doi: 10.1007/s12026-016-8891-x
  45. Gholamrezaei A, Bonakdar ZS, Mirbagher L, Hosseini N. Sleep disorders in systemic lupus erythematosus. Does vitamin D play a role? Lupus. 2014;23(10):1054–1058. doi: 10.1177/0961203314532563
  46. Katzav A, Solodeev I, Brodsky O, et al. Induction of autoimmune depression in mice by anti-ribosomal P antibodies via the limbic system. Arthritis Rheum. 2007;56(3):938–948. doi: 10.1002/art.22419

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Copyright (c) 2021 Rukavishnikov G.V., Smirnova A.A., Neznanov N.G., Mazurov V.I., Mazo G.E.

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