A blood-based biomarker panel indicates IL-10 and IL-12/23p40 are jointly associated as predictors of β-amyloid load in an AD cohort

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Pedrini, Steve ^a,b   Gupta, Veer B ^a,b   Hone, Eugene ^a,b   Doecke, James ^c   O'Bryant, Sid ^d   James, Ian ^e   Bush, Ashley I ^b,f   Rowe, Christopher C ^g   Villemagne, Victor L ^g   Ames, David ^f,h   Masters, Colin L ^f   Martins, Ralph N ^a,b,i,j   Savage, Greg ^j   Wilson, Bill ^c   Bourgeat, Pierrick ^c   Fripp, Jurgen ^c   Gibson, Simon ^c   Leroux, Hugo ^c   McBride, Simon ^c   Salvado, Olivier ^c   Fenech, Michael ^c   Francois, Maxime ^c   Barnes, Mary ^c   Baker, Jenalle ^f   Barnham, Kevin ^k   Bellingham, Shayne ^k   Bomke, Julia ^f   Pejoska, Sveltana Bozin ^g   Buckley, Rachel ^f   Cheng, Lesley ^k   Collins, Steven ^f   Cooke, Ian ^b   Cyarto, Elizabeth ^h   Darby, David ^f   Dore, Vincent ^c   El Sheikh, Denise ^g   Faux, Noel ^f   Fowler, Christopher ^f   Harrington, Karra ^f   Hill, Andy ^k   Horne, Malcolm ^f   Jones, Gareth ^g   Kamer, Adrian ^f   Killeen, Neil ^f   Korrel, Hannah ^f   Lamb, Fiona ^g   Lautenschlager, Nicola ^h   Lennon, Kate ^f   Li, Qiao Xin ^f   Lim, Yen Ying ^f   Louey, Andrea ^f   Macaulay, Lance ^c   Mackintosh, Lucy ^f   Maruff, Paul ^l   McIlroy, Alissandra ^f   Nigro, Julie ^c   Perez, Kayla ^k   Pertile, Kelly ^f   Restrepo, Carolina ^f   Cardoso, Barbara Rita ^f   Rembach, Alan ^f   Roberts, Blaine ^f   Robertson, Jo ^f   Rumble, Rebecca ^f   Ryan, Tim ^f   Sach, Jack ^m   Silbert, Brendan ⁿ   Thai, Christine ^f   Trounson, Brett ^f   Volitakis, Irene ^f   Vovos, Michael ^f   Ward, Larry ^h   Watt, Andrew ^k   Williams, Rob ^f   Woodward, Michael ^g   Yates, Paul ^g   Ugarte, Fernanda Yevenes ^f   Zhang, Ping ^c   Bird, Sabine ^a   Brown, Belinda ^a   Burnham, Samantha ^c   Chatterjee, Pratishtha ^a   Cox, Kay ⁱ   Fernandez, Shane ^a   Fernando, Binosha ^a   Gardener, Sam ^a   Laws, Simon ^a   Lim, Florence ^a   Lim, Lucy ^a   Tegg, Michelle ^a   Lucas, Kathy ⁱ   Martins, Georgia ^a   Porter, Tenielle ^a   Rainey Smith, Stephanie ^a   Rodrigues, Mark ^a   Shen, Kaikai ^c   Sohrabi, Harmid ^a   Taddei, Kevin ^a   Taddei, Tania ^a   Tan, Sherilyn ^a   Verdile, Giuseppe ^o   Weinborn, Mike ⁱ   Farrow, Maree ^m   Frost, Shaun ⁿ   Hanson, David ^c   Hor, Maryam ^c   Kanagasingam, Yogi ^c   Leifert, Wayne ^c   Lockett, Linda ^c   Riley, Malcolm ^c   Saunders, Ian ^c   Thomas, Philip ^c   more..

^a EDITH COWAN UNIVERSITY   (Australia)

^b University of Melbourne   (Australia)

^c CSIRO   (Australia)

^d University of North   (United States)

^e MURDOCH UNIVERSITY   (Australia)

^f UNIVERSITY OF MELBOURNE   (Australia)

^g AUSTIN HEALTH   (Australia)

^h NATIONAL AGEING RESEARCH INSTITUTE   (Australia)

ⁱ UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^j MACQUARIE UNIVERSITY   (Australia)

^k UNIVERSITY OF MELBOURNE   (Australia)

^l Scientific Division   (Australia)

^m Alzheimer Australia Vic   (Australia)

ⁿ ST VINCENT S HOSPITAL   (Australia)

^o CURTIN UNIVERSITY   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85032174892     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-14020-9     Document Type: Article

References (77)

1. Price, J. L. & Morris, J. C. Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease. Annals of neurology 45, 358-368 (1999).
2. Krishnaswamy, S., Verdile, G., Groth, D., Kanyenda, L. & Martins, R. N. The structure and function of Alzheimer's gamma secretase enzyme complex. Critical reviews in clinical laboratory sciences 46, 282-301, https://doi. org/10. 3109/10408360903335821 (2009).
3. Zhang, H., Ma, Q., Zhang, Y. W. & Xu, H. Proteolytic processing of Alzheimer's beta-amyloid precursor protein. Journal of neurochemistry 120(Suppl 1), 9-21, https://doi. org/10. 1111/j. 1471-4159. 2011. 07519. x (2012).
4. Arendt, T., Bigl, V., Arendt, A. & Tennstedt, A. Loss of neurons in the nucleus basalis of Meynert in Alzheimer's disease, paralysis agitans and Korsakoff's Disease. Acta neuropathologica 61, 101-108 (1983).
5. Gomez-Isla, T. et al. Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. The Journal of neuroscience: the official journal of the Society for Neuroscience 16, 4491-4500 (1996).
6. West, M. J., Coleman, P. D., Flood, D. G. & Troncoso, J. C. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet (London, England) 344, 769-772 (1994).
7. Whitehouse, P. J. et al. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science (New York, N. Y.) 215, 1237-1239 (1982).
8. Rogers, S. L., Farlow, M. R., Doody, R. S., Mohs, R. & Friedhoff, L. T. A 24-week, double-blind, placebo-controlled trial of donepezil in patients with Alzheimer's disease. Donepezil Study Group. Neurology 50, 136-145 (1998).
9. Tariot, P. N. et al. Memantine treatment in patients with moderate to severe Alzheimer disease already receiving donepezil: a randomized controlled trial. Jama 291, 317-324, https://doi. org/10. 1001/jama. 291. 3. 317 (2004).
10. Villemagne, V. L. et al. Amyloid beta deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer's disease: a prospective cohort study. The Lancet. Neurology 12, 357-367, https://doi. org/10. 1016/s1474-4422(13)70044-9 (2013).
11. Craig-Schapiro, R. et al. Multiplexed immunoassay panel identifies novel CSF biomarkers for Alzheimer's disease diagnosis and prognosis. PloS one 6, e18850, https://doi. org/10. 1371/journal. pone. 0018850 (2011).
12. Hu, W. T. et al. Novel CSF biomarkers for frontotemporal lobar degenerations. Neurology 75, 2079-2086, https://doi. org/10. 1212/WNL. 0b013e318200d78d (2010).
13. Khan, W. et al. A Subset of Cerebrospinal Fluid Proteins from a Multi-Analyte Panel Associated with Brain Atrophy, Disease Classification and Prediction in Alzheimer's Disease. PloS one 10, e0134368, https://doi. org/10. 1371/journal. pone. 0134368 (2015).
14. Perrin, R. J. et al. Identification and validation of novel cerebrospinal fluid biomarkers for staging early Alzheimer's disease. PloS one 6, e16032, https://doi. org/10. 1371/journal. pone. 0016032 (2011).
15. Simonsen, A. H. et al. Identification of a novel panel of cerebrospinal fluid biomarkers for Alzheimer's disease. Neurobiology of aging 29, 961-968, https://doi. org/10. 1016/j. neurobiolaging. 2007. 01. 011 (2008).
16. Ray, S. et al. Classification and prediction of clinical Alzheimer's diagnosis based on plasma signaling proteins. Nature medicine 13, 1359-1362, https://doi. org/10. 1038/nm1653 (2007).
17. Gomez Ravetti, M. & Moscato, P. Identification of a 5-protein biomarker molecular signature for predicting Alzheimer's disease. PloS one 3, e3111, https://doi. org/10. 1371/journal. pone. 0003111 (2008).
18. Bjorkqvist, M., Ohlsson, M., Minthon, L. & Hansson, O. Evaluation of a previously suggested plasma biomarker panel to identify Alzheimer's disease. PloS one 7, e29868, https://doi. org/10. 1371/journal. pone. 0029868 (2012).
19. Marksteiner, J. et al. Five out of 16 plasma signaling proteins are enhanced in plasma of patients with mild cognitive impairment and Alzheimer's disease. Neurobiology of aging 32, 539-540, https://doi. org/10. 1016/j. neurobiolaging. 2009. 03. 011 (2011).
20. Doecke, J. D. et al. Blood-based protein biomarkers for diagnosis of Alzheimer disease. Archives of neurology 69, 1318-1325, https://doi. org/10. 1001/archneurol. 2012. 1282 (2012).
21. O'Bryant, S. E. et al. A blood-based screening tool for Alzheimer's disease that spans serum and plasma: findings from TARC and ADNI. PloS one 6, e28092, https://doi. org/10. 1371/journal. pone. 0028092 (2011).
22. O'Bryant, S. E. et al. A blood-based algorithm for the detection of Alzheimer's disease. Dementia and geriatric cognitive disorders 32, 55-62, https://doi. org/10. 1159/000330750 (2011).
23. Soares, H. D. et al. Identifying early markers of Alzheimer's disease using quantitative multiplex proteomic immunoassay panels. Annals of the New York Academy of Sciences 1180, 56-67, https://doi. org/10. 1111/j. 1749-6632. 2009. 05066. x (2009).
24. Soares, H. D. et al. Plasma biomarkers associated with the apolipoprotein E genotype and Alzheimer disease. Archives of neurology 69, 1310-1317, https://doi. org/10. 1001/archneurol. 2012. 1070 (2012).
25. Hu, W. T. et al. Plasma multianalyte profiling in mild cognitive impairment and Alzheimer disease. Neurology 79, 897-905, https://doi. org/10. 1212/WNL. 0b013e318266fa70 (2012).
26. Johnstone, D., Milward, E. A., Berretta, R. & Moscato, P. Multivariate protein signatures of pre-clinical Alzheimer's disease in the Alzheimer's disease neuroimaging initiative (ADNI) plasma proteome dataset. PloS one 7, e34341, https://doi. org/10. 1371/journal. pone. 0034341 (2012).
27. Laske, C. et al. Identification of a blood-based biomarker panel for classification of Alzheimer's disease. The international journal of neuropsychopharmacology/official scientific journal of the Collegium Internationale Neuropsychopharmacologicum (CINP) 14, 1147-1155, https://doi. org/10. 1017/s1461145711000459 (2011).
28. Ellis, K. A. et al. TheAustralian Imaging, Biomarkers and Lifestyle (AIBL) study of aging: methodology and baseline characteristics of 1112 individuals recruited for a longitudinal study of Alzheimer's disease. Int Psychogeriatr 21, 672-687, https://doi. org/10. 1017/s1041610209009405 (2009).
29. Folstein, M. F., Folstein, S. E. & McHugh, P. R. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. Journal of psychiatric research 12, 189-198 (1975).
30. Saxton, J. et al. Normative data on the Boston Naming Test and two equivalent 30-item short forms. The Clinical neuropsychologist 14, 526-534, https://doi. org/10. 1076/clin. 14. 4. 526. 7204 (2000).
31. McKhann, G. et al. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34, 939-944 (1984).
32. Winblad, B. et al. Mild cognitive impairment-beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J Intern Med 256, 240-246, https://doi. org/10. 1111/j. 1365-2796. 2004. 01380. x (2004).
33. Gupta, V. B. et al. Plasma apolipoprotein E and Alzheimer disease risk: the AIBL study of aging. Neurology 76, 1091-1098, https://doi. org/10. 1212/WNL. 0b013e318211c352 (2011).
34. Pike, K. E. et al. Beta-amyloid imaging and memory in non-demented individuals: evidence for preclinical Alzheimer's disease. Brain 130, 2837-2844, https://doi. org/10. 1093/brain/awm238 (2007).
35. Croom, J. & Taylor, I. L. Neuropeptide Y, peptide YY and aluminum in Alzheimer's disease: is there an etiological relationship? Journal of inorganic biochemistry 87, 51-56 (2001).
36. Ahmed, R. M. et al. Eating behavior in frontotemporal dementia: Peripheral hormones vs hypothalamic pathology. Neurology 85, 1310-1317, https://doi. org/10. 1212/wnl. 0000000000002018 (2015).
37. Westin, K. et al. CCL2 is associated with a faster rate of cognitive decline during early stages of Alzheimer's disease. PloS one 7, e30525, https://doi. org/10. 1371/journal. pone. 0030525 (2012).
38. Imai, T. et al. The T cell-directed CC chemokine TARC is a highly specific biological ligand for CC chemokine receptor 4. The Journal of biological chemistry 272, 15036-15042 (1997).
39. Maioli, S. et al. Alterations in brain leptin signalling in spite of unchanged CSF leptin levels in Alzheimer's disease. Aging cell 14, 122-129, https://doi. org/10. 1111/acel. 12281 (2015).
40. Martel, J. C., Alagar, R., Robitaille, Y. & Quirion, R. Neuropeptide Y receptor binding sites in human brain. Possible alteration in Alzheimer's disease. Brain research 519, 228-235 (1990).
41. Serrano-Pozo, A., Frosch, M. P., Masliah, E. & Hyman, B. T. Neuropathological alterations in Alzheimer disease. Cold Spring Harbor perspectives in medicine 1, a006189, https://doi. org/10. 1101/cshperspect. a006189 (2011).
42. Chakrabarty, P. et al. IL-10 alters immunoproteostasis in APP mice, increasing plaque burden and worsening cognitive behavior. Neuron 85, 519-533, https://doi. org/10. 1016/j. neuron. 2014. 11. 020 (2015).
43. Guillot-Sestier, M. V. et al. Il10 deficiency rebalances innate immunity to mitigate Alzheimer-like pathology. Neuron 85, 534-548, https://doi. org/10. 1016/j. neuron. 2014. 12. 068 (2015).
44. Oppmann, B. et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13, 715-725 (2000).
45. Radrizzani, M. et al. IL-12 inhibits apoptosis induced in a human Th1 clone by gp120/CD4 cross-linking and CD3/TCR activation or by IL-2 deprivation. Cellular immunology 161, 14-21, https://doi. org/10. 1006/cimm. 1995. 1003 (1995).
46. Capon, F. et al. Sequence variants in the genes for the interleukin-23 receptor (IL23R) and its ligand (IL12B) confer protection against psoriasis. Human genetics 122, 201-206, https://doi. org/10. 1007/s00439-007-0397-0 (2007).
47. Cargill, M. et al. A large-scale genetic association study confirms IL12B and leads to the identification of IL23R as psoriasis-risk genes. American journal of human genetics 80, 273-290, https://doi. org/10. 1086/511051 (2007).
48. Glas, J. et al. Analysis of IL12B gene variants in inflammatory bowel disease. PloS one 7, e34349, https://doi. org/10. 1371/journal. pone. 0034349 (2012).
49. Alloza, I. et al. Interleukin-12p40 polymorphism and susceptibility to multiple sclerosis. Annals of neurology 52, 524-525, https://doi. org/10. 1002/ana. 10348 (2002).
50. Begovich, A. B. et al. The autoimmune disease-associated IL12B and IL23R polymorphisms in multiple sclerosis. Human immunology 68, 934-937, https://doi. org/10. 1016/j. humimm. 2007. 09. 005 (2007).
51. Illes, Z. et al. 3UTR C2370A allele of the IL-23 receptor gene is associated with relapsing-remitting multiple sclerosis. Neuroscience letters 431, 36-38, https://doi. org/10. 1016/j. neulet. 2007. 11. 015 (2008).
52. Nunez, C. et al. IL23R: a susceptibility locus for celiac disease and multiple sclerosis? Genes and immunity 9, 289-293, https://doi. org/10. 1038/gene. 2008. 16 (2008).
53. Roos, I. M., Kockum, I. & Hillert, J. The interleukin 23 receptor gene in multiple sclerosis: a case-control study. Journal of neuroimmunology 194, 173-180, https://doi. org/10. 1016/j. jneuroim. 2007. 11. 011 (2008).
54. van Veen, T. et al. Interleukin-12p40 genotype plays a role in the susceptibility to multiple sclerosis. Annals of neurology 50, 275 (2001).
55. Javan, M. R. et al. An interleukin 12 B single nucleotide polymorphism increases IL-12p40 production and is associated with increased disease susceptibility in patients with relapsing-remitting multiple sclerosis. Neurological research 39, 435-441, https://doi. org/10. 1080/01616412. 2017. 1301623 (2017).
56. Langowski, J. L. et al. IL-23 promotes tumour incidence and growth. Nature 442, 461-465, https://doi. org/10. 1038/nature04808 (2006).
57. Tan, M. S. et al. IL12/23 p40 inhibition ameliorates Alzheimer's disease-associated neuropathology and spatial memory in SAMP8 mice. Journal of Alzheimer's disease: JAD 38, 633-646, https://doi. org/10. 3233/jad-131148 (2014).
58. Vom Berg, J. et al. Inhibition of IL-12/IL-23 signaling reduces Alzheimer's disease-like pathology and cognitive decline. Nature medicine 18, 1812-1819, https://doi. org/10. 1038/nm. 2965 (2012).
59. Johansson, P. et al. Reduced cerebrospinal fluid concentration of interleukin-12/23 subunit p40 in patients with cognitive impairment. PloS one 12, e0176760, https://doi. org/10. 1371/journal. pone. 0176760 (2017).
60. Richartz, E. et al. Diminished production of proinflammatory cytokines in patients with Alzheimer's disease. Dementia and geriatric cognitive disorders 19, 184-188, https://doi. org/10. 1159/000083497 (2005).
61. Motta, M., Imbesi, R., Di Rosa, M., Stivala, F. & Malaguarnera, L. Altered plasma cytokine levels in Alzheimer's disease: correlation with the disease progression. Immunology letters 114, 46-51, https://doi. org/10. 1016/j. imlet. 2007. 09. 002 (2007).
62. Richartz, E. et al. Decline of immune responsiveness: a pathogenetic factor in Alzheimer's disease? Journal of psychiatric research 39, 535-543, https://doi. org/10. 1016/j. jpsychires. 2004. 12. 005 (2005).
63. Rentzos, M. et al. Interleukin-12 is reduced in cerebrospinal fluid of patients with Alzheimer's disease and frontotemporal dementia. Journal of the neurological sciences 249, 110-114, https://doi. org/10. 1016/j. jns. 2006. 05. 063 (2006).
64. Kikly, K., Liu, L., Na, S. & Sedgwick, J. D. The IL-23/Th(17) axis: therapeutic targets for autoimmune inflammation. Current opinion in immunology 18, 670-675, https://doi. org/10. 1016/j. coi. 2006. 09. 008 (2006).
65. Memari, B. et al. Engagement of the Aryl Hydrocarbon Receptor in Mycobacterium tuberculosis-Infected Macrophages Has Pleiotropic Effects on Innate Immune Signaling. Journal of immunology (Baltimore, Md. : 1950) 195, 4479-4491, https://doi. org/10. 4049/jimmunol. 1501141 (2015).
66. Cua, D. J. et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421, 744-748, https://doi. org/10. 1038/nature01355 (2003).
67. Chen, J. M., Jiang, G. X., Li, Q. W., Zhou, Z. M. & Cheng, Q. Increased serum levels of interleukin-18,-23 and-17 in Chinese patients with Alzheimer's disease. Dementia and geriatric cognitive disorders 38, 321-329, https://doi. org/10. 1159/000360606 (2014).
68. Saresella, M. et al. Increased activity of Th-17 and Th-9 lymphocytes and a skewing of the post-thymic differentiation pathway are seen in Alzheimer's disease. Brain, behavior, and immunity 25, 539-547, https://doi. org/10. 1016/j. bbi. 2010. 12. 004 (2011).
69. Saresella, M. et al. A complex proinflammatory role for peripheral monocytes in Alzheimer's disease. Journal of Alzheimer's disease: JAD 38, 403-413, https://doi. org/10. 3233/jad-131160 (2014).
70. Langrish, C. L. et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. The Journal of experimental medicine 201, 233-240, https://doi. org/10. 1084/jem. 20041257 (2005).
71. Langrish, C. L. et al. IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunological reviews 202, 96-105, https://doi. org/10. 1111/j. 0105-2896. 2004. 00214. x (2004).
72. Ma, X. & Trinchieri, G. Regulation of interleukin-12 production in antigen-presenting cells. Advances in immunology 79, 55-92 (2001).
73. Vignali, D. A. & Kuchroo, V. K. IL-12 family cytokines: immunological playmakers. Nature immunology 13, 722-728, https://doi. org/10. 1038/ni. 2366 (2012).
74. Couper, K. N., Blount, D. G. & Riley, E. M. IL-10: the master regulator of immunity to infection. Journal of immunology (Baltimore, Md. : 1950) 180, (5771-5777 (2008).
75. Joss, A., Akdis, M., Faith, A., Blaser, K. & Akdis, C. A. IL-10 directly acts on T cells by specifically altering the CD28 co-stimulation pathway. European journal of immunology 30, 1683-1690, https://doi. org/10. 1002/1521-4141(200006)30: 6&60; 1683: : aidimmu1683&62; 3. 0. co; 2-a (2000).
76. Murray, P. J. The primary mechanism of the IL-10-regulated antiinflammatory response is to selectively inhibit transcription. Proceedings of the National Academy of Sciences of the United States of America 102, 8686-8691, https://doi. org/10. 1073/pnas. 0500419102 (2005).
77. Saraiva, M. & O'Garra, A. The regulation of IL-10 production by immune cells. Nature reviews. Immunology 10, 170-181, https://doi. org/10. 1038/nri2711 (2010).