Toll-Like receptors and Dectin-1, a C-type lectin receptor, trigger divergent functions in CNS macrophages

Journal of Neuroscience

Volumn 35, Issue 27, 2015, Pages 9966-9976

  Gensel, John C ^a   Wang, Yan ^b   Guan, Zhen ^b   Beckwith, Kyle A ^b   Braun, Kaitlyn J ^a   Wei, Ping ^b   McTigue, Dana M ^b   Popovich, Phillip G ^b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Dieback; Microglia; Neuroinflammation; Regeneration; TLR2; Zymosan

Indexed keywords

C TYPE LECTIN RECEPTOR; DECTIN 1; LECTIN RECEPTOR; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; VIMENTIN; CD11B ANTIGEN; CONDITIONED MEDIUM; LECTIN; LIPOPEPTIDE; NERVE PROTEIN; PAM2CSK4 LIPOPEPTIDE; TLR2 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 2;

ADULT; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; BRAIN DEVELOPMENT; CELL ACTIVATION; CONTROLLED STUDY; DEMYELINATING DISEASE; FEMALE; GENE INACTIVATION; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; INNATE IMMUNITY; INTRASPINAL MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MALE; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD INJURY; ANIMAL; C57BL MOUSE; CELL CULTURE; CENTRAL NERVOUS SYSTEM; CONDITIONED MEDIUM; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; NERVE CELL; PATHOLOGY; PHARMACOLOGY; PHYSIOLOGY; SPINAL GANGLION; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIGENS, CD11B; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CULTURE MEDIA, CONDITIONED; DISEASE MODELS, ANIMAL; FEMALE; GANGLIA, SPINAL; LECTINS, C-TYPE; LIPOPEPTIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD INJURIES; TOLL-LIKE RECEPTOR 2;

EID: 84936881933     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0337-15.2015     Document Type: Article

References (55)

1. Bartus K, James ND, Didangelos A, Bosch KD, Verhaagen J, Yáñez-Muñoz RJ, Rogers JH, Schneider BL, Muir EM, Bradbury EJ (2014) Large-scale chondroitin sulfate proteoglycan digestion with chondroitinase gene therapy leads to reduced pathology and modulates macrophage phenotype following spinal cord contusion injury. J Neurosci 34: 4822-4836. CrossRef Medline.
2. Benowitz LI, Popovich PG (2011) Inflammation and axon regeneration. Curr Opin Neurol 24: 577-583. CrossRef Medline.
3. Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81: 1-5. Medline.
4. Brown GD (2006) Dectin-1: a signalling non-TLR pattern-recognition receptor. Nat Rev Immunol 6: 33-43. CrossRef Medline.
5. Bsibsi M, Nomden A, van Noort JM, Baron W (2012) Toll-like receptors 2 and 3 agonists differentially affect oligodendrocyte survival, differentiation, and myelin membrane formation. J Neurosci Res 90: 388-398. CrossRef Medline.
6. BurgessAW, Metcalf D, Kozka IJ, Simpson RJ, Vairo G, Hamilton JA, Nice EC (1985) Purification of two forms of colony-stimulating factor from mouse L-cell-conditioned medium. J Biol Chem 260: 16004-16011. Medline.
7. Busch SA, Horn KP, Silver DJ, Silver J (2009) Overcoming macrophagemediated axonal dieback following CNS injury. J Neurosci 29: 9967-9976. CrossRef Medline.
8. Busch SA, Horn KP, Cuascut FX, Hawthorne AL, Bai L, Miller RH, Silver J (2010) Adult NG2+cells are permissive to neurite outgrowth and stabilize sensory axons during macrophage-induced axonal dieback after spinal cord injury. J Neurosci 30: 255-265. CrossRef Medline.
9. Cameron JS, Alexopoulou L, Sloane JA, DiBernardo AB, Ma Y, Kosaras B, Flavell R, Strittmatter SM, Volpe J, Sidman R, Vartanian T (2007) Tolllike receptor 3 is a potent negative regulator of axonal growth in mammals. J Neurosci 27: 13033-13041. CrossRef Medline.
10. Chen K, Deng S, Lu H, Zheng Y, Yang G, Kim D, Cao Q, Wu JQ (2013) RNA-Seq characterization of spinal cord injury transcriptome in acute/subacute phases: a resource for understanding the pathology at the systems level. PLoS One 8: e72567. CrossRef Medline.
11. Didangelos A, Iberl M, Vinsland E, Bartus K, Bradbury EJ (2014) Regulation of IL-10 by chondroitinase ABC promotes a distinct immune response following spinal cord injury. J Neurosci 34: 16424-16432. CrossRef Medline.
12. Donnelly DJ, Gensel JC, Ankeny DP, van Rooijen N, Popovich PG (2009) An efficient and reproducible method for quantifying macrophages in different experimental models of central nervous system pathology. J Neurosci Methods 181: 36-44. CrossRef Medline.
13. Donnelly DJ, Longbrake EE, Shawler TM, Kigerl KA, Lai W, Tovar CA, Ransohoff RM, Popovich PG (2011) Deficient CX3CR1 signaling promotes recovery after mouse spinal cord injury by limiting the recruitment and activation of Ly6Clo/iNOS+ macrophages. J Neurosci 31: 9910-9922. CrossRef Medline.
14. Evans TA, Barkauskas DS, Myers JT, Hare EG, You JQ, Ransohoff RM, Huang AY, Silver J (2014) High-resolution intravital imaging reveals that blood-derived macrophages but not resident microglia facilitate secondary axonal dieback in traumatic spinal cord injury. Exp Neurol 254: 109-120. CrossRef Medline.
15. Filous AR, Tran A, Howell CJ, Busch SA, Evans TA, Stallcup WB, Kang SH, Bergles DE, Lee SI, Levine JM, Silver J (2014) Entrapment via synapticlike connections between NG2 proteoglycan+cells and dystrophic axons in the lesion plays a role in regeneration failure after spinal cord injury. J Neurosci 34: 16369-16384. CrossRef Medline.
16. Fitch MT, Doller C, Combs CK, Landreth GE, Silver J (1999) Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J Neurosci 19: 8182-8198. Medline.
17. Gantner BN, Simmons RM, Canavera SJ, Akira S, Underhill DM (2003) Collaborative induction of inflammatory responses by dectin-1 and tolllike receptor 2. J Exp Med 197: 1107-1117. CrossRef Medline.
18. Gantner BN, Simmons RM, Underhill DM (2005) Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO J 24: 1277-1286. CrossRef Medline.
19. Gardai SJ, Bratton DL, Ogden CA, Henson PM (2006) Recognition ligands on apoptotic cells: a perspective. J Leukoc Biol 79: 896-903. CrossRef Medline.
20. Gensel JC, Nakamura S, Guan Z, van Rooijen N, Ankeny DP, Popovich PG (2009) Macrophages promote axon regeneration with concurrent neurotoxicity. J Neurosci 29: 3956-3968. CrossRef Medline.
21. Gensel JC, Schonberg DL, Alexander JK, McTigue DM, Popovich PG (2010) Semi-automated Sholl analysis for quantifying changes in growth and differentiation of neurons and glia. J Neurosci Methods 190: 71-79. CrossRef Medline.
22. Gensel JC, Kigerl KA, Mandrekar-Colucci SS, Gaudet AD, Popovich PG (2012) Achieving CNS axon regeneration by manipulating convergent neuro-immune signaling. Cell Tissue Res 349: 201-213. CrossRef Medline.
23. Goodridge HS, Reyes CN, Becker CA, Katsumoto TR, Ma J, Wolf AJ, Bose N, Chan AS, Magee AS, Danielson ME, Weiss A, Vasilakos JP, UnderhillDM (2011) Activation of the innate immune receptor dectin-1 upon formation of a "phagocytic synapse. " Nature 472: 471-475. CrossRef Medline.
24. Guth L, Zhang Z, DiProspero NA, Joubin K, Fitch MT (1994) Spinal cord injury in the rat: treatment with bacterial lipopolysaccharide and indomethacin enhances cellular repair and locomotor function. Exp Neurol 126: 76-87. CrossRef Medline.
25. Hauk TG, Leibinger M, Müller A, Andreadaki A, Knippschild U, Fischer D (2010) Stimulation of axon regeneration in the mature optic nerve by intravitreal application of the toll-like receptor 2 agonist Pam3Cys. Invest Ophthalmol Vis Sci 51: 459-464. CrossRef Medline.
26. Horn KP, Busch SA, Hawthorne AL, van Rooijen N, Silver J (2008) Another barrier to regeneration in the CNS: activated macrophages induce extensive retraction of dystrophic axons through direct physical interactions. J Neurosci 28: 9330-9341. CrossRef Medline.
27. Ikeda Y, Adachi Y, Ishii T, Miura N, Tamura H, Ohno N (2008) Dissociation of toll-like receptor 2-mediated innate immune response to zymosan by organic solvent-treatment without loss of dectin-1 reactivity. Biol Pharm Bull 31: 13-18. CrossRef Medline.
28. Kigerl KA, Popovich PG (2009) Toll-like receptors in spinal cord injury. Curr Top Microbiol Immunol 336: 121-136. Medline.
29. Kigerl KA, Lai W, Rivest S, Hart RP, Satoskar AR, Popovich PG (2007) Tolllike receptor (TLR)-2 and TLR-4 regulate inflammation, gliosis, and myelin sparing after spinal cord injury. J Neurochem 102: 37-50. CrossRef Medline.
30. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG (2009) Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 29: 13435-13444. CrossRef Medline.
31. Kigerl KA, de Rivero Vaccari JP, Dietrich WD, Popovich PG, Keane RW (2014) Pattern recognition receptors and central nervous system repair. Exp Neurol 258: 5-16. CrossRef Medline.
32. Kroner A, Greenhalgh AD, Zarruk JG, Passos Dos Santos R, Gaestel M, David S (2014) TNF and increased intracellular iron alter macrophage polarization to a detrimental M1 phenotype in the injured spinal cord. Neuron 83: 1098-1116. CrossRef Medline.
33. Lien E, Sellati TJ, Yoshimura A, Flo TH, Rawadi G, Finberg RW, Carroll JD, Espevik T, Ingalls RR, Radolf JD, Golenbock DT (1999) Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. J Biol Chem 274: 33419-33425. CrossRef Medline.
34. Lieu A, Tenorio G, Kerr BJ (2013) Protein kinase C gamma (PKC+) as a novel marker to assess the functional status of the corticospinal tract in experimental autoimmune encephalomyelitis (EAE). J Neuroimmunol 256: 43-48. CrossRef Medline.
35. Longbrake EE, Lai W, Ankeny DP, Popovich PG (2007) Characterization and modeling of monocyte-derived macrophages after spinal cord injury. J Neurochem 102: 1083-1094. CrossRef Medline.
36. Matsunaga I, Moody DB (2009) Mincle is a long sought receptor for mycobacterial cord factor. J Exp Med 206: 2865-2868. CrossRef Medline.
37. McPhail LT, Stirling DP, Tetzlaff W, Kwiecien JM, Ramer MS (2004) The contribution of activated phagocytes and myelin degeneration to axonal retraction/dieback following spinal cord injury. Eur J Neurosci 20: 1984-1994. CrossRef Medline.
38. Miyake Y, Ishikawa E, Ishikawa T, Yamasaki S (2010) Self and nonself recognition through C-type lectin receptor, Mincle. Self Nonself 1: 310-313. CrossRef Medline.
39. Okada S, Nakamura M, Katoh H, Miyao T, Shimazaki T, Ishii K, Yamane J, Yoshimura A, Iwamoto Y, Toyama Y, Okano H (2006) Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat Med 12: 829-834. CrossRef Medline.
40. Okada T, Ichikawa M, Tokita Y, Horie H, Saito K, Yoshida J, Watanabe M (2005) Intravitreal macrophage activation enables cat retinal ganglion cells to regenerate injured axons into the mature optic nerve. Exp Neurol 196: 153-163. CrossRef Medline.
41. Pierce JE, Trojanowski JQ, Graham DI, Smith DH, McIntosh TK (1996) Immunohistochemical characterization of alterations in the distribution of amyloid precursor proteins and beta-amyloid peptide after experimental brain injury in the rat. J Neurosci 16: 1083-1090. Medline.
42. Popovich PG, Guan Z, Wei P, Huitinga I, van Rooijen N, Stokes BT (1999) Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp Neurol 158: 351-365. CrossRef Medline.
43. Popovich PG, Guan Z, McGaughy V, Fisher L, Hickey WF, BassoDM (2002) The neuropathological and behavioral consequences of intraspinal microglial/macrophage activation. J Neuropathol Exp Neurol 61: 623-633. Medline.
44. Popovich PG, Tovar CA, Wei P, Fisher L, Jakeman LB, Basso DM (2012) A reassessment of a classic neuroprotective combination therapy for spinal cord injured rats: LPS/pregnenolone/indomethacin. Exp Neurol 233: 677-685. CrossRef Medline.
45. Rosas M, Liddiard K, Kimberg M, Faro-Trindade I, McDonald JU, Williams DL, Brown GD, Taylor PR (2008) The induction of inflammation by dectin-1 in vivo is dependent on myeloid cell programming and the progression of phagocytosis. J Immunol 181: 3549-3557. CrossRef Medline.
46. Schonberg DL, Popovich PG, McTigueDM (2007) Oligodendrocyte gener-ation is differentially influenced by toll-like receptor (TLR) 2 and TLR4-mediated intraspinal macrophage activation. J Neuropathol Exp Neurol 66: 1124-1135. CrossRef Medline.
47. Steinmetz MP, Horn KP, Tom VJ, Miller JH, Busch SA, Nair D, Silver DJ, Silver J (2005) Chronic enhancement of the intrinsic growth capacity of sensory neurons combined with the degradation of inhibitory proteoglycans allows functional regeneration of sensory axons through the dorsal root entry zone in the mammalian spinal cord. J Neurosci 25: 8066-8076. CrossRef Medline.
48. Stirling DP, Cummins K, Mishra M, Teo W, Yong VW, Stys P (2014) Tolllike receptor 2-mediated alternative activation of microglia is protective after spinal cord injury. Brain 137: 707-723. CrossRef Medline.
49. Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, Gordon S (2005) Macrophage receptors and immune recognition. Annu Rev Immunol 23: 901-944. CrossRef Medline.
50. Taylor PR, Tsoni SV, Willment JA, Dennehy KM, Rosas M, Findon H, Haynes K, Steele C, Botto M, Gordon S, Brown GD (2007) Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat Immunol 8: 31-38. CrossRef Medline.
51. Wang L, Hu B, Wong WM, Lu P, Wu W, Xu XM (2009) Glial and axonal responses in areas of Wallerian degeneration of the corticospinal and dorsal ascending tracts after spinal cord dorsal funiculotomy. Neuropathology 29: 230-241. CrossRef Medline.
52. Ward RE, Huang W, Kostusiak M, Pallier PN, Michael-Titus AT, Priestley JV (2014) A characterization of white matter pathology following spinal cord compression injury in the rat. Neuroscience 260: 227-239. CrossRef Medline.
53. Yin Y, Cui Q, Li Y, Irwin N, Fischer D, Harvey AR, Benowitz LI (2003) Macrophage-derived factors stimulate optic nerve regeneration. J Neurosci 23: 2284-2293. Medline.
54. Yin Y, Henzl MT, Lorber B, Nakazawa T, Thomas TT, Jiang F, Langer R, Benowitz LI (2006) Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat Neurosci 9: 843-852. CrossRef Medline.
55. Yin Y, Cui Q, Gilbert HY, Yang Y, Yang Z, Berlinicke C, Li Z, Zaverucha-do-Valle C, He H, Petkova V, Zack DJ, Benowitz LI (2009) Oncomodulin links inflammation to optic nerve regeneration. Proc Natl Acad Sci U S A 106: 19587-19592. CrossRef Medline.