Monocyte-lymphocyte cross-communication via soluble CD163 directly links innate immune system activation and adaptive immune system suppression following ischemic stroke

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  O'Connell, Grant C ^a,b   Tennant, Connie S ^a   Lucke Wold, Noelle ^a   Kabbani, Yasser ^c   Tarabishy, Abdul R ^c   Chantler, Paul D ^a,d   Barr, Taura L ^a,e,f  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b WEST VIRGINIA UNIVERSITY   (United States)

^c WEST VIRGINIA UNIVERSITY   (United States)

^d WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e WEST VIRGINIA UNIVERSITY SCHOOL OF NURSING   (United States)

^f Valtari Bio Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD163 ANTIGEN; CELL SURFACE RECEPTOR; DIFFERENTIATION ANTIGEN; LEUKOCYTE ANTIGEN; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME;

ADAPTIVE IMMUNITY; AGED; BIOLOGICAL MODEL; BLOOD; BRAIN ISCHEMIA; CELL COMMUNICATION; CELL PROLIFERATION; CEREBROVASCULAR ACCIDENT; COMPLICATION; FEMALE; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE; LYMPHOCYTE COUNT; MALE; METABOLISM; MIDDLE AGED; MONOCYTE; NEUTROPHIL; SOLUBILITY;

ADAM17 PROTEIN; ADAPTIVE IMMUNITY; AGED; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BRAIN ISCHEMIA; CELL COMMUNICATION; CELL PROLIFERATION; FEMALE; HUMANS; IMMUNITY, INNATE; LYMPHOCYTE COUNT; LYMPHOCYTES; MALE; MIDDLE AGED; MODELS, BIOLOGICAL; MONOCYTES; NEUTROPHILS; RECEPTORS, CELL SURFACE; SOLUBILITY; STROKE;

EID: 85031086479     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-13291-6     Document Type: Article

References (74)

1. Urra, X. et al. Monocytes are major players in the prognosis and risk of infection after acute stroke. Stroke 40, 1262-1268 (2009).
2. Vogelgesang, A. et al. Analysis of lymphocyte subsets in patients with stroke and their influence on infection after stroke. Stroke 39, 237-241 (2008).
3. Urra, X., Cervera, Á. & Villamor, N. Planas, a. M. & Chamorro, Á. Harms and benefits of lymphocyte subpopulations in patients with acute stroke. Neuroscience 158, 1174-1183 (2009).
4. Harms, H. et al. Preventive antibacterial therapy in acute ischemic stroke: A randomized controlled trial. PLoS One 3 (2008).
5. Planas, A. M. et al. Brain-Derived Antigens in Lymphoid Tissue of Patients with Acute Stroke. J. Immunol. 188, 2156-2163 (2012).
6. Becker, K. Autoimmune Responses to Brain FollowingStroke. Transl. Stroke Res. 3, 310-317 (2012).
7. Becker, K. J. et al. Autoimmune responses to the brain after stroke are associated with worse outcome. Stroke 42, 2763-2769 (2011).
8. Koennecke, H.-C. et al. Factors influencing in-hospital mortality and morbidity in patients treated on a stroke unit. Neurology 77, 965-972 (2011).
9. Vernino, S. et al. Cause-specific mortality after first cerebral infarction: A population-based study. Stroke 34, 1828-1832 (2003).
10. Kimura, K., Minematsu, K., Kazui, S. & Yamaguchi, T. Mortality and Cause of Death after Hospital Discharge in 10,981 Patients with Ischemic Stroke and Transient Ischemic Attack. Cerebrovasc. Dis. 19, 171 (2005).
11. Katzan, I. L., Cebul, R. D., Husak, S. H., Dawson, N. V. & Baker, D. W. The effect of pneumonia on mortality among patients hospitalized for acute stroke. Neurology 60, 620-625 (2003).
12. Brooks, S. D. et al. Admission neutrophil-lymphocyte ratio predicts 90 day outcome after endovascular stroke therapy. J. Neurointerv. Surg. 1-6, https://doi.org/10.1136/neurintsurg-2013-010780 (2013).
13. Prass, K. et al. Stroke-induced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by poststroke T helper cell type 1-like immunostimulation. J. Exp. Med. 198, 725-736 (2003).
14. Hilker, R. et al. Nosocomial pneumonia after acute stroke: Implications for neurological intensive care medicine. Stroke 34, 975-981 (2003).
15. Davenport, R. J., Dennis, M. S., Wellwood, I. & Warlow, C. P. Complications After Acute Stroke. Stroke 27, 415-420 (1996).
16. Johnston, K. C. et al. Medical and neurological complications of ischemic stroke: experience from the RANTTAS trial. RANTTAS Investigators. Stroke 29, 447-453 (1998).
17. Schaer, D. J. et al. CD163 is the macrophage scavenger receptor for native and chemically modified hemoglobins in the absence of haptoglobin. Blood 107, 373-80 (2006).
18. Lau, S. K., Chu, P. G. & Weiss, L. M. CD163: A Specific Marker of Macrophages in Paraffin-Embedded Tissue Samples. Am. J. Clin. Pathol. 122, 794-801 (2004).
19. Cunnington, A. J. et al. Prolonged neutrophil dysfunction after Plasmodium falciparum malaria is related to hemolysis and heme oxygenase-1 induction. J. Immunol. 189, 5336-46 (2012).
20. Etzerodt, A., Maniecki, M. B., Møller, K., Møller, H. J. & Moestrup, S. K. Tumor necrosis factor α-converting enzyme (TACE/ADAM17) mediates ectodomain shedding of the scavenger receptor CD163. J. Leukoc. Biol. 88, 1201-1205 (2010).
21. Etzerodt, A. et al. Structural basis for inflammation-driven shedding of CD163 ectodomain and tumor necrosis factor- in macrophages. J. Biol. Chem. 289, 778-788 (2014).
22. Frings, W., Dreier, J. & Sorg, C. Only the soluble form of the scavenger receptor CD163 acts inhibitory on phorbol ester-activated T-lymphocytes, whereas membrane-bound protein has no effect. FEBS Lett. 526, 93-6 (2002).
23. Högger, P. & Sorg, C. Soluble CD163 inhibits phorbol ester-induced lymphocyte proliferation. Biochem. Biophys. Res. Commun. 288, 841-3 (2001).
24. Timmermann, M., Buck, F., Sorg, C. & Högger, P. Interaction of soluble CD163 with activated T lymphocytes involves its association with non-muscle myosin heavy chain type A. Immunol. Cell Biol. 82, 479-487 (2004).
25. O'Connell, G. C. et al. Machine-learning approach identifies a pattern of gene expression in peripheral blood that can accurately detect ischaemic stroke. npj Genomic Med. 1, 16038 (2016).
26. Cardenas, A. et al. Upregulation of TACE/ADAM17 after ischemic preconditioning is involved in brain tolerance. J Cereb Blood Flow Metab 22, 1297-1302 (2002).
27. Katakowski, M. et al. Stroke-induced subventricular zone proliferation is promoted by tumor necrosis factor-alpha-converting enzyme protease activity. J. Cereb. Blood Flow Metab. 27, 669-78 (2007).
28. Romera, C. In Vitro Ischemic Tolerance Involves Upregulation of Glutamate Transport Partly Mediated by the TACE/ADAM17-Tumor Necrosis Factor-Pathway. J. Neurosci. 24, 1350-1357 (2004).
29. Castellanos, M. et al. Inflammation-Mediated Damage in Progressing Lacunar Infarctions. Stroke 33, 982-987 (2002).
30. Sotgiu, S. et al. Inflammatory biomarkers in blood of patients with acute brain ischemia. Eur. J. Neurol. 13, 505-513 (2006).
31. Kostić, V., Mostarica-Stojković, M., Ramić, Z., Kovǎcević, M. & Lukić, M. Serum immunoinhibitory factors in stroke patients. Eur. Neurol. 28, 331-4 (1988).
32. Tononi, G., Sporns, O. & Edelman, G. M. Measures of degeneracy and redundancy in biological networks. Proc.Natl.Acad.Sci.,USA 96, 3257-3262 (1999).
33. Maliszewski, C. R. et al. Isolation and characterization of My23, a myeloid cell-derived antigen reactive with the monoclonal antibody {AML-2-23}. J. Immunol. {(Baltimore,} Md. 1950) 135, 1929-1936 (1985).
34. Pugin, J. et al. CD14 is a pattern recognition receptor. Immunity 1, 509-516 (1994).
35. Rey Nores, J. E. et al. Soluble CD14 acts as a negative regulator of human T cell activation and function. Eur. J. Immunol. 29, 265-276 (1999).
36. Bazil, V. et al. Biochemical characterization of a soluble form of the 53-kDa monocyte surface antigen. Eur. J. Immunol. 16, 1583-9 (1986).
37. Huang, P. et al. Serum free hemoglobin as a novel potential biomarker for acute ischemic stroke. J. Neurol. 256, 625-31 (2009).
38. Subramanian, K., Du, R., Tan, N. S., Ho, B. & Ding, J. L. CD163 and IgG codefend against cytotoxic hemoglobin via autocrine and paracrine mechanisms. J. Immunol. 190, 5267-78 (2013).
39. Olsson, T., Astrom, M., Eriksson, S. & Forssell, A. Hypercortisolism revealed by the dexamethasone suppression test in patients [corrected] with acute ischemic stroke. Stroke 20, 1685-1690 (1989).
40. Nanetti, L. et al. Reactive oxygen species plasmatic levels in ischemic stroke. Mol. Cell. Biochem. 303, 19-25 (2007).
41. Timmermann, M. & Högger, P. Oxidative stress and 8-iso-prostaglandin F(2alpha) induce ectodomain shedding of CD163 and release of tumor necrosis factor-alpha from human monocytes. Free Radic. Biol. Med. 39, 98-107 (2005).
42. Buechler, C. et al. Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro-and antiinflammatory stimuli. J. Leukoc. Biol. 67, 97-103 (2000).
43. Aristoteli, L. P., Møller, H. J., Bailey, B., Moestrup, S. K. & Kritharides, L. The monocytic lineage specific soluble CD163 is a plasma marker of coronary atherosclerosis. Atherosclerosis 184, 342-347 (2006).
44. Arenillas, J. F. Intracranial atherosclerosis: Current concepts. Stroke 42 (2011).
45. Newell, E. et al. Cerebrospinal Fluid Markers of Macrophage and Lymphocyte Activation After Traumatic Brain Injury in Children. Pediatr. Crit. care Med. 16, 549-57 (2015).
46. Van Gorp, H., Van Breedam, W., Van Doorsselaere, J., Delputte, P. L. & Nauwynck, H. J. Identification of the CD163 protein domains involved in infection of the porcine reproductive and respiratory syndrome virus. J. Virol. 84, 3101-5 (2010).
47. Caì, Y. et al. Simian hemorrhagic fever virus cell entry is dependent on CD163 and uses a clathrin-mediated endocytosis-like pathway. J. Virol. 89, 844-56 (2015).
48. Zizzo, G., Hilliard, B. A., Monestier, M. & Cohen, P. L. Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK induction. J. Immunol. 189, 3508-20 (2012).
49. Klatt, N. R. et al. Availability of activated CD4+ T cells dictates the level of viremia in naturally SIV-infected sooty mangabeys. J. Clin. Invest. 118, 2039-49 (2008).
50. Rasmussen, H. S. & McCann, P. P. Matrix metalloproteinase inhibition as a novel anticancer strategy: a review with special focus on batimastat and marimastat. Pharmacol. Ther. 75, 69-75 (1997).
51. Mergenthaler, P. & Meisel, A. Do stroke models model stroke? Dis. Model. Mech. 5, 718-25 (2012).
52. Sharp, F. R. & Jickling, G. C. Modeling immunity and inflammation in stroke: differences between rodents and humans? Stroke 45, e179-e180 (2014).
53. Mestas, J. & Hughes, C. C. W. Of mice and not men: differences between mouse and human immunology. J. Immunol. 172, 2731-8 (2004).
54. Seok, J. et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. USA 110, 3507-3512 (2013).
55. Krams, M. et al. Acute Stroke Therapy by Inhibition of Neutrophils (ASTIN): An Adaptive Dose-Response Study of UK-279,276 in Acute Ischemic Stroke. Stroke 34, 2543-2548 (2003).
56. Investigators Enlimomab Acute Stroke Trial. Use of anti-ICAM-1 therapy in ischemic stroke: results of the Enlimomab Acute Stroke Trial. Neurology 57, 1428-34 (2001).
57. del Zoppo, G. J. Acute anti-inflammatory approaches to ischemic stroke. Ann. N. Y. Acad. Sci. 1207, 143-148 (2010).
58. Meisel, C. & Meisel, A. Suppressing immunosuppression after stroke. N. Engl. J. Med. 365, 2134-6 (2011).
59. Zhang, B. et al. Estradiol and G1 reduce infarct size and improve immunosuppression after experimental stroke. J. Immunol. 184, 4087-4094 (2010).
60. Maier, I. L., Karch, A., Mikolajczyk, R., Bähr, M. & Liman, J. Effect of beta-blocker therapy on the risk of infections and death after acute stroke-A historical cohort study. PLoS One 10, 1-10 (2015).
61. Smith, C. J. et al. Interleukin-1 receptor antagonist reverses stroke-associated peripheral immune suppression. Cytokine 58, 384-389 (2012).
62. Green, A. R. & Shuaib, A. Therapeutic strategies for the treatment of stroke. Drug Discov. Today 11, 681-693 (2006).
63. Tuttolomondo, A., Pecoraro, R. & Pinto, A. Studies of selective TNF inhibitors in the treatment of brain injury from stroke and trauma: a review of the evidence to date. Drug Des Devel Ther 8, 2221-2238 (2014).
64. Green, A. R. Pharmacological approaches to acute ischaemic stroke: reperfusion certainly, neuroprotection possibly. Br. J. Pharmacol. 153(Suppl), S325-38 (2008).
65. Arribas, J. & Esselens, C. ADAM17 as a therapeutic target in multiple diseases. Curr. Pharm. Des. 15, 2319-35 (2009).
66. Amantea, D. et al. Rational modulation of the innate immune system for neuroprotection in ischemic stroke. Front. Neurosci. 9, 1-20 (2015).
67. Kidwell, C. S. & Warach, S. Acute Ischemic Cerebrovascular Syndrome: Diagnostic Criteria. Stroke 34, 2995-2998 (2003).
68. Heckmann, L.-H., Sørensen, P. B., Krogh, P. H. & Sørensen, J. G. NORMA-Gene: a simple and robust method for qPCR normalization based on target gene data. BMC Bioinformatics 12, 250 (2011).
69. O'Connell, G. C. et al. Leukocyte Dynamics Influence Reference Gene Stability in Whole Blood: Data-Driven qRT-PCR Normalization Is a Robust Alternative for Measurement of Transcriptional Biomarkers. Lab. Med. 48, https://doi.org/10.1093/labmed/lmx035 in press (2017).
70. Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative C T method. Nat. Protoc. 3, 1101-1108 (2008).
71. Menck, K. et al. Isolation of human monocytes by double gradient centrifugation and their differentiation to macrophages in teflon-coated cell culture bags. J. Vis. Exp. e51554 (2014).
72. Appierto, V. et al. A lipemia-independent NanoDrop(®)-based score to identify hemolysis in plasma and serum samples. Bioanalysis 6, 1215-26 (2014).
73. Park, K., Saudek, C. D. & Hart, G. W. Increased expression of beta-N-acetylglucosaminidase in erythrocytes from individuals with pre-diabetes and diabetes. Diabetes 59, 1845-50 (2010).
74. Ross, I., Robert, G., Ihaka, R. & Gentleman, R. R: A Language for Data Analysis and Graphics. Journal of computational and graphical statistics 5, 299-314 (1996).