Unbiased expression mapping identifies a link between the complement and cholinergic systems in the rat central nervous system

Journal of Immunology

Volumn 192, Issue 3, 2014, Pages 1138-1153

  Lindblom, Rickard P F ^a   Ström, Mikael ^a   Heinig, Matthias ^b,c   Nimer, Faiez Al ^a   Aeinehband, Shahin ^a   Berg, Alexander ^a   Dominguez, Cecilia A ^a   Vijayaraghavan, Swetha ^a   Zhang, Xing Mei ^a   Harnesk, Karin ^a   Zelano, Johan ^a   Hübner, Norbert ^b   Cullheim, Staffan ^a   Darreh Shori, Taher ^a   Diez, Margarita ^a   Piehl, Fredrik ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; CHOLINESTERASE; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C1QA; COMPLEMENT COMPONENT C1QB; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C9; FORKHEAD TRANSCRIPTION FACTOR; FORKHEAD TRANSCRIPTION FACTOR K2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CENTRAL NERVOUS SYSTEM; CHOLINERGIC ACTIVITY; CHOLINERGIC SYSTEM; COMPLEMENT ACTIVATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION SYSTEM; GENE MAPPING; GENETIC VARIABILITY; IMMUNOREGULATION; LINKAGE ANALYSIS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; QUANTITATIVE TRAIT; RAT; UPREGULATION;

ACETYLCHOLINE; ANIMALS; ANIMALS, CONGENIC; ASTROCYTES; BRAIN INJURIES; BUTYRYLCHOLINESTERASE; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CHOLINERGIC FIBERS; COMPLEMENT ACTIVATION; COMPLEMENT C1Q; COMPLEMENT C3; DENERVATION; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GENETIC LINKAGE; GENOME-WIDE ASSOCIATION STUDY; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; QUANTITATIVE TRAIT LOCI; RATS; RHIZOTOMY; SPECIFIC PATHOGEN-FREE ORGANISMS; SPINAL NERVE ROOTS; SYNAPTOPHYSIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84893412768     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301233     Document Type: Article

References (74)

1. Markiewski, M. M., and J. D. Lambris. 2007. The role of complement in inflammatory diseases from behind the scenes into the spotlight. Am. J. Pathol. 171: 715-727.
2. Ricklin, D., G. Hajishengallis, K. Yang, and J. D. Lambris. 2010. Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 11: 785-797.
3. Zipfel, P. F., and C. Skerka. 2009. Complement regulators and inhibitory proteins. Nat. Rev. Immunol. 9: 729-740.
4. Gasque, P. 2004. Complement: a unique innate immune sensor for danger signals. Mol. Immunol. 41: 1089-1098.
5. Dunkelberger, J. R., and W. C. Song. 2010. Complement and its role in innate and adaptive immune responses. Cell Res. 20: 34-50.
6. Carroll, M. C. 2004. The complement system in regulation of adaptive immunity. Nat. Immunol. 5: 981-986.
7. Sjoberg, A. P., L. A. Trouw, and A. M. Blom. 2009. Complement activation and inhibition: a delicate balance. Trends Immunol. 30: 83-90.
8. Bellander, B. M., S. K. Singhrao, M. Ohlsson, P. Mattsson, and M. Svensson. 2001. Complement activation in the human brain after traumatic head injury. J. Neurotrauma 18: 1295-1311.
9. Széplaki, G., R. Szegedi, K. Hirschberg, T. Gombos, L. Varga, I. Karádi, L. Entz, Z. Széplaki, P. Garred, Z. Prohászka, and G. Fust. 2009. Strong complement activation after acute ischemic stroke is associated with unfavorable outcomes. Atherosclerosis 204: 315-320.
10. Fonseca, M. I., J. Zhou, M. Botto, and A. J. Tenner. 2004. Absence of C1q leads to less neuropathology in transgenic mouse models of Alzheimer's disease. J. Neurosci. 24: 6457-6465.
11. Lambert, J. C., S. Heath, G. Even, D. Campion, K. Sleegers, M. Hiltunen, O. Combarros, D. Zelenika, M. J. Bullido, B. Tavernier, et al; European Alzheimer's Disease Initiative Investigators. 2009. Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat. Genet. 41: 1094-1099.
12. Bonifati, D. M., and U. Kishore. 2007. Role of complement in neurodegeneration and neuroinflammation. Mol. Immunol. 44: 999-1010.
13. Wang, Y., A. M. Hancock, J. Bradner, K. A. Chung, J. F. Quinn, E. R. Peskind, D. Galasko, J. Jankovic, C. P. Zabetian, H. M. Kim, et al. 2011. Complement 3 and factor H in human cerebrospinal fluid in Parkinson's disease, Alzheimer's disease, and multiple-system atrophy. Am. J. Pathol. 178: 1509-1516.
14. Swanberg, M., K. Duvefelt, M. Diez, J. Hillert, T. Olsson, F. Piehl, and O. Lidman. 2006. Genetically determined susceptibility to neurodegeneration is associated with expression of inflammatory genes. Neurobiol. Dis. 24: 67-88.
15. Lidman, O., M. Swanberg, L. Horvath, K. W. Broman, T. Olsson, and F. Piehl. 2003. Discrete gene loci regulate neurodegeneration, lymphocyte infiltration, and major histocompatibility complex class II expression in the CNS. J. Neurosci. 23: 9817-9823.
16. Al Nimer, F., A. D. Beyeen, R. Lindblom, M. Strom, S. Aeinehband, O. Lidman, and F. Piehl. 2011. Both MHC and non-MHC genes regulate inflammation and T-cell response after traumatic brain injury. Brain Behav. Immun. 25: 981-990.
17. Laird, P. W., A. Zijderveld, K. Linders, M. A. Rudnicki, R. Jaenisch, and A. Berns. 1991. Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19: 4293.
18. Darvasi, A., and M. Soller. 1994. Optimum spacing of genetic markers for determining linkage between marker loci and quantitative trait loci. Theor. Appl. Genet. 89: 351-357.
19. Jacob, H. J., D. M. Brown, R. K. Bunker, M. J. Daly, V. J. Dzau, A. Goodman, G. Koike, V. Kren, T. Kurtz, A. Lernmark, et al. 1995. A genetic linkage map of the laboratory rat, Rattus norvegicus. Nat. Genet. 9: 63-69.
20. Kishore, U., C. Gaboriaud, P.Waters, A. K. Shrive, T. J. Greenhough, K. B. Reid, R. B. Sim, and G. J. Arlaud. 2004. C1q and tumor necrosis factor superfamily: modularity and versatility. Trends Immunol. 25: 551-561.
21. Hrabovska, A., V. Bernard, and E. Krejci. 2010. A novel system for the efficient generation of antibodies following immunization of unique knockout mouse strains. PLoS ONE 5: e12892.
22. Dagerlind, A., K. Friberg, A. J. Bean, and T. Hokfelt. 1992. Sensitive mRNA detection using unfixed tissue: combined radioactive and non-radioactive in situ hybridization histochemistry. Histochemistry 98: 39-49.
23. de Bruijn, M. H., and G. H. Fey. 1985. Human complement component C3: cDNA coding sequence and derived primary structure. Proc. Natl. Acad. Sci. USA 82: 708-712.
24. Strom, M., F. Al Nimer, R. Lindblom, J. R. Nyengaard, and F. Piehl. 2012. Naturally occurring genetic variability in expression of Gsta4 is associated with differential survival of axotomized rat motoneurons. Neuromolecular Med. 14: 15-29.
25. Irizarry, R. A., B. Hobbs, F. Collin, Y. D. Beazer-Barclay, K. J. Antonellis, U. Scherf, and T. P. Speed. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
26. Wang, J., R. W. Williams, and K. F. Manly. 2003. WebQTL: Web-based complex trait analysis. Neuroinformatics 1: 299-308.
27. Falcon, S., and R. Gentleman. 2007. Using GOstats to test gene lists for GO term association. Bioinformatics 23: 257-258.
28. Schafer, J., and K. Strimmer. 2005. An empirical Bayes approach to inferring large-scale gene association networks. Bioinformatics 21: 754-764.
29. Heinig, M., E. Petretto, C. Wallace, L. Bottolo, M. Rotival, H. Lu, Y. Li, R. Sarwar, S. R. Langley, A. Bauerfeind, et al Cardiogenics Consortium. 2010. A trans-Acting locus regulates an anti-viral expression network and type 1 diabetes risk. Nature 467: 460-464.
30. Roider, H. G., A. Kanhere, T. Manke, and M. Vingron. 2007. Predicting transcription factor affinities to DNA from a biophysical model. Bioinformatics 23: 134-141.
31. Manke, T., H. G. Roider, and M. Vingron. 2008. Statistical modeling of transcription factor binding affinities predicts regulatory interactions. PLOS Comput. Biol. 4: e1000039.
32. Roider, H. G., T. Manke, S. O'Keeffe, M. Vingron, and S. A. Haas. 2009. PASTAA: identifying transcription factors associated with sets of co-regulated genes. Bioinformatics 25: 435-442.
33. Weitnauer, E., A. Robitzki, and P. G. Layer. 1998. Aryl acylamidase activity exhibited by butyrylcholinesterase is higher in chick than in horse, but much lower than in fetal calf serum. Neurosci. Lett. 254: 153-156.
34. Vijayaraghavan, S., A. Karami, S. Aeinehband, H. Behbahani, A. Grandien, B. Nilsson, K. N. Ekdahl, R. P. Lindblom, F. Piehl, and T. Darreh-Shori. 2013. Regulated extracellular choline acetyltransferase activity: the plausible missing link of the distant action of acetylcholine in the cholinergic anti-inflammatory pathway. PLoS ONE 8: e65936.
35. Lundberg, C., O. Lidman, R. Holmdahl, T. Olsson, and F. Piehl. 2001. Neurodegeneration and glial activation patterns after mechanical nerve injury are differentially regulated by non-MHC genes in congenic inbred rat strains. J. Comp. Neurol. 431: 75-87.
36. Stahel, P. F., M. A. Flierl, B. P. Morgan, I. Persigehl, C. Stoll, C. Conrad, B. M. Touban, W. R. Smith, K. Beauchamp, O. I. Schmidt, et al. 2009. Absence of the complement regulatory molecule CD59a leads to exacerbated neuropathology after traumatic brain injury in mice. J. Neuroinflammation 6: 2.
37. Nimer, F. A., R. Lindblom, M. Strom, A. O. Guerreiro-Cacais, R. Parsa, S. Aeinehband, T. Mathiesen, O. Lidman, and F. Piehl. 2013. Strain influences on inflammatory pathway activation, cell infiltration and complement cascade after traumatic brain injury in the rat. Brain Behav. Immun. 27: 109-122.
38. Stevens, B., N. J. Allen, L. E. Vazquez, G. R. Howell, K. S. Christopherson, N. Nouri, K. D. Micheva, A. K. Mehalow, A. D. Huberman, B. Stafford, et al. 2007. The classical complement cascade mediates CNS synapse elimination. Cell 131: 1164-1178.
39. Swanberg, M., O. Lidman, L. Padyukov, P. Eriksson, E. Akesson, M. Jagodic, A. Lobell, M. Khademi, O. Borjesson, C. M. Lindgren, et al. 2005. MHC2TA is associated with differential MHC molecule expression and susceptibility to rheumatoid arthritis, multiple sclerosis and myocardial infarction. Nat. Genet. 37: 486-494.
40. Hubner, N., C. A. Wallace, H. Zimdahl, E. Petretto, H. Schulz, F. Maciver, M. Mueller, O. Hummel, J. Monti, V. Zidek, et al. 2005. Integrated transcriptional profiling and linkage analysis for identification of genes underlying disease. Nat. Genet. 37: 243-253.
41. Ghazalpour, A., S. Doss, B. Zhang, S. Wang, C. Plaisier, R. Castellanos, A. Brozell, E. E. Schadt, T. A. Drake, A. J. Lusis, and S. Horvath. 2006. Integrating genetic and network analysis to characterize genes related to mouse weight. PLoS Genet. 2: e130.
42. Salamone, G., G. Lombardi, S. Gori, K. Nahmod, C. Jancic, M. M. Amaral, M. Vermeulen, A. Espanol, M. E. Sales, and J. Geffner. 2011. Cholinergic modulation of dendritic cell function. J. Neuroimmunol. 236: 47-56.
43. Rosas-Ballina, M., P. S. Olofsson, M. Ochani, S. I. Valdés-Ferrer, Y. A. Levine, C. Reardon, M. W. Tusche, V. A. Pavlov, U. Andersson, S. Chavan, et al. 2011. Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 334: 98-101.
44. Nguyen, H. X., M. D. Galvan, and A. J. Anderson. 2008. Characterization of early and terminal complement proteins associated with polymorphonuclear leukocytes in vitro and in vivo after spinal cord injury. J. Neuroinflammation 5: 26.
45. Darvesh, S., D. A. Hopkins, and C. Geula. 2003. Neurobiology of butyrylcholinesterase. Nat. Rev. Neurosci. 4: 131-138.
46. Tracey, K. J. 2009. Reflex control of immunity. Nat. Rev. Immunol. 9: 418-428.
47. Shi, F. D., W. H. Piao, Y. P. Kuo, D. I. Campagnolo, T. L. Vollmer, and R. J. Lukas. 2009. Nicotinic attenuation of central nervous system inflammation and autoimmunity. J. Immunol. 182: 1730-1739.
48. Mesulam, M. M., and C. Geula. 1994. Butyrylcholinesterase reactivity differentiates the amyloid plaques of aging from those of dementia. Ann. Neurol. 36: 722-727.
49. Terry, R. D., E. Masliah, D. P. Salmon, N. Butters, R. DeTeresa, R. Hill, L. A. Hansen, and R. Katzman. 1991. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30: 572-580.
50. Darvesh, S., A. M. Leblanc, I. R. Macdonald, G. A. Reid, V. Bhan, R. J. Macaulay, and J. D. Fisk. 2010. Butyrylcholinesterase activity in multiple sclerosis neuropathology. Chem. Biol. Interact. 187: 425-431.
51. Mis, K., T. Mars, M. Jevsek, M. Brank, K. Zajc-Kreft, and Z. Grubic. 2003. Localization of mRNAs encoding acetylcholinesterase and butyrylcholinesterase in the rat spinal cord by nonradioactive in situ hybridization. J. Histochem. Cytochem. 51: 1633-1644.
52. Darreh-Shori, T., S. Vijayaraghavan, S. Aeinehband, F. Piehl, R. P. Lindblom, B. Nilsson, K. N. Ekdahl, B. Langstrom, O. Almkvist, and A. Nordberg. 2013. Functional variability in butyrylcholinesterase activity regulates intrathecal cytokine and astroglial biomarker profiles in patients with Alzheimer's disease. Neurobiol. Aging 34: 2465-2481.
53. McAlpine, F. E., and M. G. Tansey. 2008. Neuroinflammation and tumor necrosis factor signaling in the pathophysiology of Alzheimer's disease. J. Inflamm. Res. 1: 29-39.
54. Stellwagen, D., and R. C. Malenka. 2006. Synaptic scaling mediated by glial TNF-Alpha. Nature 440: 1054-1059.
55. Centonze, D., L. Muzio, S. Rossi, F. Cavasinni, V. De Chiara, A. Bergami, A. Musella, M. D'Amelio, V. Cavallucci, A. Martorana, et al. 2009. Inflammation triggers synaptic alteration and degeneration in experimental autoimmune encephalomyelitis. J. Neurosci. 29: 3442-3452.
56. Shytle, R. D., T. Mori, K. Townsend, M. Vendrame, N. Sun, J. Zeng, J. Ehrhart, A. A. Silver, P. R. Sanberg, and J. Tan. 2004. Cholinergic modulation of microglial activation by a7 nicotinic receptors. J. Neurochem. 89: 337-343.
57. McCaman, R. E., D. Weinreich, and H. Borys. 1973. Endogenous levels of acetylcholine and choline in individual neurons of Aplysia. J. Neurochem. 21: 473-476.
58. Bazelyansky, M., E. Robey, and J. F. Kirsch. 1986. Fractional diffusion-limited component of reactions catalyzed by acetylcholinesterase. Biochemistry 25: 125-130.
59. Greig, N. H., T. Utsuki, Q. Yu, X. Zhu, H. W. Holloway, T. Perry, B. Lee, D. K. Ingram, and D. K. Lahiri. 2001. A new therapeutic target in Alzheimer's disease treatment: attention to butyrylcholinesterase. Curr. Med. Res. Opin. 17: 159-165.
60. Cuadra, G., K. Summers, and E. Giacobini. 1994. Cholinesterase inhibitor effects on neurotransmitters in rat cortex in vivo. J. Pharmacol. Exp. Ther. 270: 277-284.
61. Farar, V., F. Mohr, M. Legrand, B. Lamotte d'Incamps, J. Cendelin, J. Leroy, M. Abitbol, V. Bernard, F. Baud, V. Fournet, et al. 2012. Near-complete adaptation of the PRiMA knockout to the lack of central acetylcholinesterase. J. Neurochem. 122: 1065-1080.
62. Hannenhalli, S., and K. H. Kaestner. 2009. The evolution of Fox genes and their role in development and disease. Nat. Rev. Genet. 10: 233-240.
63. Jonsson, H., and S. L. Peng. 2005. Forkhead transcription factors in immunology. Cell. Mol. Life Sci. 62: 397-409.
64. Long, S. A., and J. H. Buckner. 2011. CD4+FOXP3+ T regulatory cells in human autoimmunity: more than a numbers game. J. Immunol. 187: 2061-2066.
65. Wijchers, P. J., M. F. Hoekman, J. P. Burbach, and M. P. Smidt. 2006. Identification of forkhead transcription factors in cortical and dopaminergic areas of the adult murine brain. Brain Res. 1068: 23-33.
66. Li, C., C. F. Lai, D. S. Sigman, and R. B. Gaynor. 1991. Cloning of a cellular factor, interleukin binding factor, that binds to NFAT-like motifs in the human immunodeficiency virus long terminal repeat. Proc. Natl. Acad. Sci. USA 88: 7739-7743.
67. Nirula, A., D. J. Moore, and R. B. Gaynor. 1997. Constitutive binding of the transcription factor interleukin-2 (IL-2) enhancer binding factor to the IL-2 promoter. J. Biol. Chem. 272: 7736-7745.
68. Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell 140: 805-820.
69. Areschoug, T., and S. Gordon. 2008. Pattern recognition receptors and their role in innate immunity: focus on microbial protein ligands. Contrib. Microbiol. 15: 45-60.
70. Figdor, C. G., and A. B. van Spriel. 2010. Fungal pattern-recognition receptors and tetraspanins: partners on antigen-presenting cells. Trends Immunol. 31: 91-96.
71. Hoppenbrouwers, I. A., Y. S. Aulchenko, A. C. Janssens, S. V. Ramagopalan, L. Broer, M. Kayser, G. C. Ebers, B. A. Oostra, C. M. van Duijn, and R. Q. Hintzen. 2009. Replication of CD58 and CLEC16A as genome-wide significant risk genes for multiple sclerosis. J. Hum. Genet. 54: 676-680.
72. Chen, G., C. S. Tan, B. K. Teh, and J. Lu. 2011. Molecular mechanisms for synchronized transcription of three complement C1q subunit genes in dendritic cells and macrophages. J. Biol. Chem. 286: 34941-34950.
73. Bialas, A. R., and B. Stevens. 2013. TGF-b signaling regulates neuronal C1q expression and developmental synaptic refinement. Nat. Neurosci. 16: 1773-1782.
74. Radanova, M., V. Vasilev, B. Deliyska, U. Kishore, V. Ikonomov, and D. Ivanova. 2012. Anti-C1q autoantibodies specific against the globular domain of the C1qBchain from patient with lupus nephritis inhibit C1q binding to IgG and CRP. Immunobiology 217: 684-691.