Neuroinflammation and non-motor symptoms: The dark passenger of parkinson's disease?

Current Neurology and Neuroscience Reports

Volumn 12, Issue 4, 2012, Pages 350-358

  Barnum, Christopher J ^a   Tansey, Malú G ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Arthritis; Braak staging; Cognitive deficits; Crohn's disease; Cytokines; Depression; Gastrointestinal tract; H5N1; Helicobacter pylori; HLA DRA; Inflammation; Interleukin 1 6; Lewy body; Lipopolysaccharide; LRRK2; Microglia; Non motor symptoms; Parkin; Parkinson's disease; Psychosis; Sleep; Substantia nigra; Tumor necrosis factor

Indexed keywords

LEUCINE RICH REPEAT KINASE 2; PARKIN;

ARTICLE; CLINICAL FEATURE; COGNITIVE DEFECT; DEMENTIA; DEPRESSION; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE SEVERITY; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; INTESTINE INFECTION; LRRK2 GENE; MONOAMINERGIC SYSTEM; MUTATOR GENE; NERVE CELL NECROSIS; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; PARKIN GENE; PARKINSON DISEASE; PSYCHOSIS; SLEEP DISORDER;

ANIMALS; DOPAMINE; HUMANS; INFLAMMATION; NERVE DEGENERATION; PARKINSON DISEASE; SLEEP;

EID: 84865639699     PISSN: 15284042     EISSN: 15346293     Source Type: Journal    
DOI: 10.1007/s11910-012-0283-6     Document Type: Article

References (100)

1. Braak H, Del Tredici K. Invited article: nervous system pathology in sporadic Parkinson disease. Neurology. 2008;70(20):1916-25. (Pubitemid 351684646)
2. Braak H, Ghebremedhin E, Rüb U, et al. Stages in the development of Parkinson's disease-related pathology. Cell Tissue Res. 2004;318(1):121-34. (Pubitemid 39362633)
3. Hawkes CH, Del Tredici K, Braak H. Parkinson's disease: a dualhit hypothesis. Neuropathol Appl Neurobiol. 2007;33(6):599-614.
4. Hawkes CH, Del Tredici K, Braak H. A timeline for Parkinson's disease. Parkinsonism Relat Disord. 2010;16(2):79-84.
5. Jang H, Boltz D, Sturm-Ramirez K, et al. Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc Natl Acad Sci U S A. 2009;106(33):14063-8.
6. Tansey MG, McCoy MK, Frank-Cannon TC. Neuroinflammatory mechanisms in Parkinson's disease: potential environmental triggers, pathways, and targets for early therapeutic intervention. Exp Neurol. 2007;208(1):1-25. (Pubitemid 47603240)
7. Whitton PS. Inflammation as a causative factor in the aetiology of Parkinson's disease. Br J Pharmacol. 2007;150(8):963-76. (Pubitemid 46628616)
8. McCoy MK, Tansey MG. TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J Neuroinflammation. 2008;5:45.
9. McGeer PL, McGeer EG. Glial reactions in Parkinson's disease. Mov Disord. 2008;23(4):474-83.
10. Hirsch EC, Hunot S. Neuroinflammation in Parkinson's disease: a target for neuroprotection? Lancet Neurol. 2009;8(4):382-97.
11. Barnum CJ, Tansey MG. Modeling neuroinflammatory pathogenesis of Parkinson's disease. Prog Brain Res. 2010;184:113-132.12.
12. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH. Mechanisms underlying inflammation in neurodegeneration. Cell. 2010;140(6):918-34.
13. Tansey MG, Goldberg MS. Neuroinflammation in Parkinson's disease: its role in neuronal death and implications for therapeutic intervention. Neurobiol Dis. 2010;37(3):510-8.
14. Hamza TH, Zabetian CP, Tenesa A, et al. Common genetic variation in the HLA region is associated with late-onset sporadic Parkinson's disease. Nat Genet. 2010;42(9):781-5.
15. Boss JM, Jensen PE. Transcriptional regulation of the MHC class II antigen presentation pathway. Curr Opin Immunol. 2003;15 (1):105-11. (Pubitemid 35454200)
16. Do CB, Tung JY, Dorfman E, et al. Web-based genome-wide association study identifies two novel loci and a substantial genetic component for Parkinson's disease. PLoS Genet. 2011;7 (6):e1002141.
17. Guo Y, Deng X, Zheng W, et al. HLA rs3129882 variant in chinese han patients with late-onset sporadic Parkinson disease. Neurosci Lett. 2011;501(3):185-7.
18. Hill-Burns EM, Factor SA, Zabetian CP, et al. Evidence for more than one Parkinson's disease-associated variant within the HLA region. PLoS One. 2011;6(11):e27109.
19. Nalls MA, Plagnol V, Hernandez DG, et al. Imputation of sequence variants for identification of genetic risks for Parkinson's disease: a meta-analysis of genome-wide association studies. Lancet. 2011;377(9766):641-9.
20. Puschmann A, Verbeeck C, Heckman MG, et al. Human leukocyte antigen variation and Parkinson's disease. Parkinsonism Relat Disord. 2011;17(5):376-8.
21. Simon-Sanchez J, van Hilten JJ, van de Warrenburg B, et al. Genome-wide association study confirms extant PD risk loci among the Dutch. Eur J Hum Genet. 2011;19(6):655-61.
22. Chiang HL, Lee-Chen GJ, Chen CM, et al. Genetic analysis of HLA-DRA region variation in Taiwanese Parkinson's disease. Parkinsonism Relat Disord 2012.
23. Kruger R, Hardt C, Tschentscher F, et al. Genetic analysis of immunomodulating factors in sporadic Parkinson's disease. J Neural Transm. 2000;107(5):553-62. (Pubitemid 30251739)
24. Nishimura M, Mizuta I, Mizuta E, et al. Tumor necrosis factor gene polymorphisms in patients with sporadic Parkinson's disease. Neurosci Lett. 2001;311(1):1-4. (Pubitemid 32831488)
25. Wu YR, Feng IH, Lyu RK, et al. Tumor necrosis factor-alpha promoter polymorphism is associated with the risk of Parkinson's disease. Am J Med Genet B Neuropsychiatr Genet. 2007;144B (3):300-4.
26. Wahner AD, Sinsheimer JS, Bronstein JM, et al. Inflammatory cytokine gene polymorphisms and increased risk of Parkinson disease. Arch Neurol. 2007;64(6):836-40. (Pubitemid 46919838)
27. Bialecka M, Klodowska-Duda G, Kurzawski M, et al. Interleukin- 10 (IL10) and tumor necrosis factor alpha (TNF) gene polymorphisms in Parkinson's disease patients. Parkinsonism Relat Disord. 2008;14(8):636-40.
28. Wu YR, Chen CM, Hwang JC, et al. Interleukin-1 alpha polymorphism has influence on late-onset sporadic Parkinson's disease in Taiwan. J Neural Transm. 2007;114(9):1173-7. (Pubitemid 47313170)
29. Frank-Cannon TC, Alto LT, McAlpine FE, et al. Does neuroinflammation fan the flame in neurodegenerative diseases? Mol Neurodegener. 2009;4:47.
30. Corti O, Lesage S, Brice A. What genetics tells us about the causes and mechanisms of Parkinson's disease. Physiol Rev. 2011;91(4):1161-218.
31. Shimura H, Hattori N, Kubo S, et al. Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat Genet. 2000;25(3):302-5. (Pubitemid 30437317)
32. Narendra D, Tanaka A, Suen DF, et al. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol. 2008;183(5):795-803.
33. Goldberg MS, Fleming SM, Palacino JJ, et al. Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J Biol Chem. 2003;278(44):43628-35. (Pubitemid 37345989)
34. Zhu XR, Maskri L, Herold C, et al. Non-motor behavioural impairments in parkin-deficient mice. Eur J Neurosci. 2007;26 (7):1902-11. (Pubitemid 47493196)
35. Frank-Cannon TC, Tran T, Ruhn KA, et al. Parkin deficiency increases vulnerabiity to inflammation-related nigral degeneration. J Neurosci. 2008;28(43):10825-34.
36. Tran TA, Nguyen AD, Chang J, et al. Lipopolysaccharide and tumor necrosis factor regulate Parkin expression via nuclear factor-kappa B. PLoS One. 2011;6(8):e23660.
37. Hakimi M, Selvanantham T, Swinton E, et al. Parkinson's disease-linked LRRK2 is expressed in circulating and tissue immune cells and upregulated following recognition of microbial structures. J Neural Transm. 2011;118(5):795-808.
38. Liu Z, Lee J, Krummey S, et al. The kinase LRRK2 is a regulator of the transcription factor NFAT that modulates the severity of inflammatory bowel disease. Nat Immunol. 2011;12 (11):1063-70.
39. Monticelli S, Rao A. NFAT1 and NFAT2 are positive regulators of IL-4 gene transcription. Eur J Immunol. 2002;32(10):2971-8. (Pubitemid 35238190)
40. Menza M, Dobkin RD, Marin H, et al. The role of inflammatory cytokines in cognition and other non-motor symptoms of Parkinson's disease. Psychosomatics. 2010;51(6):474-9.
41. Blaser MJ. Who are we? Indigenous microbes and the ecology of human diseases. EMBO Rep. 2006;7(10):956-60. (Pubitemid 44480504)
42. Nielsen HH, Qiu J, Friis S, et al. Treatment for Helicobacter pylori infection and risk of parkinson's disease in Denmark. Eur J Neurol 2012.
43. Bjarnason IT, Charlett A, Dobbs RJ, et al. Role of chronic infection and inflammation in the gastrointestinal tract in the etiology and pathogenesis of idiopathic parkinsonism. Part 2: response of facets of clinical idiopathic parkinsonism to helicobacter pylori eradication. A randomized, double-blind, placebocontrolled efficacy study. Helicobacter. 2005;10(4):276-87. (Pubitemid 41104966)
44. Dobbs RJ, Dobbs SM, Weller C, et al. Helicobacter hypothesis for idiopathic parkinsonism: before and beyond. Helicobacter. 2008;13(5):309-22.
45. Forsyth CB, Shannon KM, Kordower JH, et al. Increased intestinal permeability correlates with sigmoid mucosa alphasynuclein staining and endotoxin exposure markers in early Parkinson's disease. PLoS One. 2011;6(12):e28032.
46. Savica R, Carlin JM, Grossardt BR, et al. Medical records documentation of constipation preceding Parkinson disease: a case-control study. Neurology. 2009;73(21):1752-8.
47. Leentjens AF, Van den Akker M, Metsemakers JF, et al. Higher incidence of depression preceding the onset of Parkinson's disease: a register study. Mov Disord. 2003;18(4):414-8. (Pubitemid 36527282)
48. Ishihara-Paul L, Wainwright NW, Khaw KT, et al. Prospective association between emotional health and clinical evidence of Parkinson's disease. Eur J Neurol. 2008;15(11):1148-54.
49. Blonder LX, Slevin JT. Emotional dysfunction in Parkinson's disease. Behav Neurol. 2011;24(3):201-17.
50. Aarsland D, Påhlhagen S, Ballard CG, et al. Depression in Parkinson disease-epidemiology, mechanisms and management. Nat Rev Neurol. 2012;8(1):35-47.
51. Hinnell C, Hurt CS, Landau S, et al. Nonmotor versus motor symptoms: how much do they matter to health status in Parkinson's disease? Mov Disord. 2012;27(2):236-41.
52. Musselman DL, Lawson DH, Gumnick JF, et al. Paroxetine for the prevention of depression induced by high-dose interferon alfa. N Engl J Med. 2001;344(13):961-6. (Pubitemid 32240314)
53. Raedler TJ. Inflammatory mechanisms in major depressive disorder. Curr Opin Psychiatry. 2011;24(6):519-25.
54. Raison CL, Miller AH. Is depression an inflammatory disorder? Curr Psychiatry Rep. 2011;13(6):467-75.
55. Harms A, Barnum CJ, Ruhn KA, et al. Delayed dominantnegative TNF gene therapy halts progressive loss of nigral dopaminergic neurons in a rat model of Parkinson's disease. Mol Ther. 2010;19(1):46-52.
56. McCoyMK,Martinez TN, Ruhn KA, et al. Blocking soluble tumor necrosis factor signaling with dominant-negative tumor necrosis factor inhibitor attenuates loss of dopaminergic neurons in models of Parkinson's disease. J Neurosci. 2006;26(37):9365-75. (Pubitemid 44396849)
57. McCoy MK, Ruhn KA, Martinez TN, et al. Intranigral lentiviral delivery of dominant-negative TNF attenuates neurodegeneration and behavioral deficits in hemiparkinsonian rats. Mol Ther. 2008;16(9):1572-9.
58. Harms AS, Lee JK, Nguyen TA, et al. Regulation of microglia effector functions by tumor necrosis factor signaling. Glia. 2012;60(2):189-202.
59. Dowlati Y, Herrmann N, Swardfager W, et al. A meta-analysis of cytokines in major depression. Biol Psychiatry. 2010;67(5):446-57.
60. Pålhagen S, Qi H, Mårtensson B, et al. Monoamines, BDNF, IL-6 and corticosterone in CSF in patients with Parkinson's disease and major depression. J Neurol. 2010;257(4):524-32.
61. Haroon E, Raison CL, Miller AH. Psychoneuroimmunology meets neuropsychopharmacology: translational implications of the impact of inflammation on behavior. neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology 2011.
62. Chung YC, Kim SR, Park JY, et al. Fluoxetine prevents MPTPinduced loss of dopaminergic neurons by inhibiting microglial activation. Neuropharmacology. 2011;60(6):963-74.
63. Chung YC, Kim SR, Jin BK. Paroxetine prevents loss of nigrostriatal dopaminergic neurons by inhibiting brain inflammation and oxidative stress in an experimental model of Parkinson's disease. J Immunol. 2010;185(2):1230-7.
64. Chung ES, Chung YC, Bok E, et al. Fluoxetine prevents LPSinduced degeneration of nigral dopaminergic neurons by inhibiting microglia-mediated oxidative stress. Brain Res. 2010;1363:143-50.
65. Vgontzas AN, Bixler EO, Lin HM, et al. IL-6 and its circadian secretion in humans. Neuroimmunomodulation. 2005;12(3):131-40. (Pubitemid 40868672)
66. Vgontzas AN, Papanicolaou DA, Bixler EO, et al. Circadian interleukin-6 secretion and quantity and depth of sleep. J Clin Endocrinol Metab. 1999;84(8):2603-7. (Pubitemid 30641979)
67. Irwin M, McClintick J, Costlow C, et al. Partial night sleep deprivation reduces natural killer and cellular immune responses in humans. FASEB J. 1996;10(5):643-53. (Pubitemid 26141176)
68. Shearer WT, Reuben JM, Mullington JM, et al. Soluble TNFalpha receptor 1 and IL-6 plasma levels in humans subjected to the sleep deprivation model of spaceflight. J Allergy Clin Immunol. 2001;107(1):165-70. (Pubitemid 32105261)
69. van Leeuwen WM, Lehto M, Karisola P, et al. Sleep restriction increases the risk of developing cardiovascular diseases by augmenting proinflammatory responses through IL-17 and CRP. PLoS One. 2009;4(2):e4589.
70. Chennaoui M, Sauvet F, Drogou C, et al. Effect of one night of sleep loss on changes in tumor necrosis factor alpha (TNF-alpha) levels in healthy men. Cytokine. 2011;56(2):318-24.
71. Vgontzas AN, Papanicolaou DA, Bixler EO, et al. Elevation of plasma cytokines in disorders of excessive daytime sleepiness: role of sleep disturbance and obesity. J Clin Endocrinol Metab. 1997;82(5):1313-6. (Pubitemid 27200394)
72. Vgontzas AN, Zoumakis M, Papanicolaou DA, et al. Chronic insomnia is associated with a shift of interleukin-6 and tumor necrosis factor secretion from nighttime to daytime. Metabolism. 2002;51(7):887-92. (Pubitemid 34784816)
73. Bower JE, Ganz PA, Irwin MR, et al. Inflammation and behavioral symptoms after breast cancer treatment: do fatigue, depression, and sleep disturbance share a common underlying mechanism? J Clin Oncol. 2011;29(26):3517-22.
74. Kim HJ, Barsevick AM, Fang CY, et al. Common biological pathways underlying the psychoneurological symptom cluster in cancer patients. Cancer Nurs 2012.
75. Chen R, Yin Y, Zhao Z, et al. Elevation of serum TNF-alpha levels in mild and moderate Alzheimer patients with daytime sleepiness. J Neuroimmunol, 2012.
76. Irwin MR, Carrillo C, Olmstead R. Sleep loss activates cellular markers of inflammation: sex differences. Brain Behav Immun. 2010;24(1):54-7.
77. Abad VC, Sarinas PS, Guilleminault C. Sleep and rheumatologic disorders. Sleep Med Rev. 2008;12(3):211-28. (Pubitemid 351657735)
78. Wells G, Li T, Tugwell P. Investigation into the impact of abatacept on sleep quality in patients with rheumatoid arthritis, and the validity of the MOS-sleep questionnaire sleep disturbance scale. Ann Rheum Dis. 2010;69(10):1768-73.
79. Deodhar A, Braun J, Inman RD, et al. Golimumab reduces sleep disturbance in patients with active ankylosing spondylitis: results from a randomized, placebo-controlled trial. Arthritis Care Res (Hoboken). 2010;62(9):1266-71.
80. Fragiadaki K, Tektonidou MG, Konsta M, et al. Sleep disturbances and interleukin 6 receptor inhibition in rheumatoid arthritis. J Rheumatol. 2012;39(1):60-2.
81. Williamson LL, Sholar PW, Mistry RS, et al. Microglia and memory: modulation by early-life infection. J Neurosci. 2011;31 (43):15511-21.
82. Fidalgo AR, Cibelli M, White JP, et al. Systemic inflammation enhances surgery-induced cognitive dysfunction in mice. Neurosci Lett. 2011;498(1):63-6.
83. Cibelli M, Fidalgo AR, Terrando N, et al. Role of interleukin- 1beta in postoperative cognitive dysfunction. Ann Neurol. 2010;68(3):360-8.
84. Terrando N, Monaco C, Ma D, et al. Tumor necrosis factor-alpha triggers a cytokine cascade yielding postoperative cognitive decline. Proc Natl Acad Sci U S A. 2010;107(47):20518-22.
85. Terrando N, Eriksson LI, Ryu JK, et al. Resolving postoperative neuroinflammation and cognitive decline. Ann Neurol. 2011;70 (6):986-95.
86. Jefferson AL, Massaro JM, Beiser AS, et al. Inflammatory markers and neuropsychological functioning: the framingham heart study. Neuroepidemiology. 2011;37(1):21-30.
87. Carmeli E, Imam B, Bachar A, Merrick J. Inflammation and oxidative stress as biomarkers of premature aging in persons with intellectual disability. Res Dev Disabil. 2012;33(2):369-75.
88. Kamer AR, Morse DE, Holm-Pedersen P, et al. Periodontal inflammation in relation to cognitive function in an older adult danish population. J Alzheimers Dis. 2012;28(3):613-24.
89. Kitazawa M, Cheng D, Tsukamoto MR, et al. Blocking IL-1 signaling rescues cognition, attenuates tau pathology, and restores neuronal beta-catenin pathway function in an Alzheimer's disease model. J Immunol. 2011;187(12):6539-49.
90. Parachikova A, Vasilevko V, Cribbs DH, et al. Reductions in amyloid-beta-derived neuroinflammation, with minocycline, restore cognition but do not significantly affect tau hyperphosphorylation. J Alzheimers Dis. 2010;21(2):527-42.
91. Fenelon G, Mahieux F, huon R, Ziegler M. Hallucinations in Parkinson's disease: prevalence, phenomenology and risk factors. Brain. 2000;123(Pt 4):733-45. (Pubitemid 30162723)
92. Zahodne LB, Fernandez HH. Pathophysiology and treatment of psychosis in Parkinson's disease: a review. Drugs Aging. 2008;25(8):665-82.
93. Meyer U, Weiner I, McAlonan GM, Feldon J. The neuropathological contribution of prenatal inflammation to schizophrenia. Expert Rev Neurother. 2011;11(1):29-32.
94. Mondelli V, Cattaneo A, Belvederi Murri M, et al. Stress and inflammation reduce brain-derived neurotrophic factor expression in first-episode psychosis: a pathway to smaller hippocampal volume. J Clin Psychiatry. 2011;72(12):1677-84.
95. Suvisaari J, Loo BM, Saarni SE, et al. Inflammation in psychotic disorders: a population-based study. Psychiatry Res. 2011;189 (2):305-11.
96. Arnett HA, Mason J, Marino M, et al. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat Neurosci. 2001;4(11):1116-22. (Pubitemid 34116557)
97. Garcia I, Olleros ML, Quesniaux VF, et al. Roles of soluble and membrane TNF and related ligands in mycobacterial infections: effects of selective and non-selective TNF inhibitors during infection. Adv Exp Med Biol. 2011;691:187-201.
98. Muller N. COX-2 inhibitors as antidepressants and antipsychotics: clinical evidence. Curr Opin Investig Drugs. 2010;11 (1):31-42.
99. Szabó N, Kincses ZT, Toldi J, Vécsei L. Altered tryptophan metabolism in Parkinson's disease: a possible novel therapeutic approach. J Neurol Sci. 2011;310(1-2):256-60.
100. Barnum CJ, Eskow KL, Dupre K, et al. Exogenous corticosterone reduces L-DOPA-induced dyskinesia in the hemiparkinsonian rat: role for interleukin-1beta. Neuroscience. 2008;156(1):30-41.