Hematogenous macrophage depletion reduces the fibrotic scar and increases axonal growth after spinal cord injury

Neurobiology of Disease

Volumn 74, Issue , 2015, Pages 114-125

  Zhu, Y ^a   Soderblom, C ^a   Krishnan, V ^a   Ashbaugh, J ^a   Bethea, J R ^a,b   Lee, J K ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b DREXEL UNIVERSITY   (United States)

Author keywords

Axonal growth; Bone morphogenetic protein; Fibroblasts; Fibrotic scar; Hematogenous macrophages; Spinal cord injury; Tumor necrosis factor

Indexed keywords

APRIL PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 5; BONE MORPHOGENETIC PROTEIN 6; CD30 LIGAND; OSTEOGENIC PROTEIN 1; OSTEOGENIN; PROCOLLAGEN C PROTEINASE; BONE MORPHOGENETIC PROTEIN; TNFSF13 PROTEIN, MOUSE; TNFSF8 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BASEMENT MEMBRANE; BONE MARROW TRANSPLANTATION; CELL DENSITY; CELLULAR PARAMETERS; CONTROLLED STUDY; FEMALE; FIBROBLAST; FIBROTIC SCAR; GENE EXPRESSION; HEMATOGENOUS MACROPHAGE DEPLETION; MACROPHAGE; MEMBRANE FORMATION; MICROGLIA; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PROTEIN EXPRESSION; SCAR; SCAR FORMATION; SPATIOTEMPORAL ANALYSIS; SPINAL CORD INJURY; ANIMAL; AXON; C57BL MOUSE; CICATRIX; DISEASE MODEL; METABOLISM; NERVE REGENERATION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; TRANSGENIC MOUSE;

ANIMALS; AXONS; BASEMENT MEMBRANE; BONE MARROW TRANSPLANTATION; BONE MORPHOGENETIC PROTEINS; CD30 LIGAND; CICATRIX; DISEASE MODELS, ANIMAL; FEMALE; FIBROBLASTS; MACROPHAGES; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE REGENERATION; SPINAL CORD INJURIES; TUMOR NECROSIS FACTOR LIGAND SUPERFAMILY MEMBER 13;

EID: 84913593330     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.10.024     Document Type: Article

References (44)

1. Arenkiel B.R., et al. Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PLoS One 2011, 6:e29423.
2. Ashbaugh J.J., et al. IL7Ralpha contributes to experimental autoimmune encephalomyelitis through altered T cell responses and nonhematopoietic cell lineages. J. Immunol. 2013, 190:4525-4534.
3. Basso D.M., et al. Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J. Neurotrauma 2006, 23:635-659.
4. Becker K., et al. Chemical clearing and dehydration of GFP expressing mouse brains. PLoS One 2012, 7:e33916.
5. Blomster L.V., et al. Mobilisation of the splenic monocyte reservoir and peripheral CX(3)CR1 deficiency adversely affects recovery from spinal cord injury. Exp. Neurol. 2013, 247:226-240.
6. Bundesen L.Q., et al. Ephrin-B2 and EphB2 regulation of astrocyte-meningeal fibroblast interactions in response to spinal cord lesions in adult rats. J. Neurosci. 2003, 23:7789-7800.
7. Burda J.E., Sofroniew M.V. Reactive gliosis and the multicellular response to CNS damage and disease. Neuron 2014, 81:229-248.
8. Cregg J.M., et al. Functional regeneration beyond the glial scar. Exp. Neurol. 2014, 253C:197-207.
9. de Bouard S., et al. Antiangiogenic and anti-invasive effects of sunitinib on experimental human glioblastoma. Neuro Oncol. 2007, 9:412-423.
10. Dendooven A., et al. Loss of endogenous bone morphogenetic protein-6 aggravates renal fibrosis. Am. J. Pathol. 2011, 178:1069-1079.
11. Donnelly D.J., et al. Deficient CX3CR1 signaling promotes recovery after mouse spinal cord injury by limiting the recruitment and activation of Ly6Clo/iNOS+macrophages. J. Neurosci. 2011, 31:9910-9922.
12. Erturk A., et al. Three-dimensional imaging of solvent-cleared organs using 3DISCO. Nat. Protoc. 2012, 7:1983-1995.
13. Evans T.A., et al. High-resolution intravital imaging reveals that blood-derived macrophages but not resident microglia facilitate secondary axonal dieback in traumatic spinal cord injury. Exp. Neurol. 2014, 254:109-120.
14. Fenrich K.K., et al. Long- and short-term intravital imaging reveals differential spatiotemporal recruitment and function of myelomonocytic cells after spinal cord injury. J. Physiol. 2013, 591:4895-4902.
15. Fielding C.A., et al. Interleukin-6 signaling drives fibrosis in unresolved inflammation. Immunity 2014, 40:40-50.
16. Gao X., et al. Bone morphogenetic protein signaling protects against cerulein-induced pancreatic fibrosis. PLoS One 2014, 9:e89114.
17. Goritz C., et al. A pericyte origin of spinal cord scar tissue. Science 2011, 333:238-242.
18. Haas C., et al. Phenotypic analysis of astrocytes derived from glial restricted precursors and their impact on axon regeneration. Exp. Neurol. 2012, 233:717-732.
19. Hampton D.W., et al. A potential role for bone morphogenetic protein signalling in glial cell fate determination following adult central nervous system injury in vivo. Eur. J. Neurosci. 2007, 26:3024-3035.
20. Hasegawa M., Takehara K. Potential immunologic targets for treating fibrosis in systemic sclerosis: a review focused on leukocytes and cytokines. Semin. Arthritis Rheum. 2012, 42:281-296.
21. Horn K.P., et al. Another barrier to regeneration in the CNS: activated macrophages induce extensive retraction of dystrophic axons through direct physical interactions. J. Neurosci. 2008, 28:9330-9341.
22. Iannotti C.A., et al. A combination immunomodulatory treatment promotes neuroprotection and locomotor recovery after contusion SCI. Exp. Neurol. 2011, 230:3-15.
23. Jahrling N., et al. 3D-reconstruction of blood vessels by ultramicroscopy. Organogenesis 2009, 5:145-148.
24. Jetten N., et al. Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo. Angiogenesis 2014, 17:109-118.
25. Jung S., et al. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell Biol. 2000, 20:4106-4114.
26. Kaplin A.I., et al. IL-6 induces regionally selective spinal cord injury in patients with the neuroinflammatory disorder transverse myelitis. J. Clin. Invest. 2005, 115:2731-2741.
27. Kigerl K.A., et al. Comparative analysis of lesion development and intraspinal inflammation in four strains of mice following spinal contusion injury. J. Comp. Neurol. 2006, 494:578-594.
28. Lee D.H., Lee J.K. Animal models of axon regeneration after spinal cord injury. Neurosci. Bull. 2013, 29:436-444.
29. Lee J.K., et al. Up-regulation of 5-HT2 receptors is involved in the increased H-reflex amplitude after contusive spinal cord injury. Exp. Neurol. 2007, 203:502-511.
30. Lee S.M., et al. Prevention of both neutrophil and monocyte recruitment promotes recovery after spinal cord injury. J. Neurotrauma 2011, 28:1893-1907.
31. Matsushita T., et al. Elevated serum APRIL levels in patients with systemic sclerosis: distinct profiles of systemic sclerosis categorized by APRIL and BAFF. J. Rheumatol. 2007, 34:2056-2062.
32. Mawhinney L.A., et al. Differential detection and distribution of microglial and hematogenous macrophage populations in the injured spinal cord of lys-EGFP-ki transgenic mice. J. Neuropathol. Exp. Neurol. 2012, 71:180-197.
33. Min K.J., et al. Astrocytes induce hemeoxygenase-1 expression in microglia: a feasible mechanism for preventing excessive brain inflammation. J. Neurosci. 2006, 26:1880-1887.
34. Nesic O., et al. IL-1 receptor antagonist prevents apoptosis and caspase-3 activation after spinal cord injury. J. Neurotrauma 2001, 18:947-956.
35. Popovich P.G., Hickey W.F. Bone marrow chimeric rats reveal the unique distribution of resident and recruited macrophages in the contused rat spinal cord. J. Neuropathol. Exp. Neurol. 2001, 60:676-685.
36. Popovich P.G., et al. Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp. Neurol. 1999, 158:351-365.
37. Rolls A., et al. Two faces of chondroitin sulfate proteoglycan in spinal cord repair: a role in microglia/macrophage activation. PLoS Med. 2008, 5:e171.
38. Shao R.X., et al. Hepatic gene expression profiles associated with fibrosis progression and hepatocarcinogenesis in hepatitis C patients. World J. Gastroenterol. 2005, 11:1995-1999.
39. Shearer M.C., Fawcett J.W. The astrocyte/meningeal cell interface-a barrier to successful nerve regeneration?. Cell Tissue Res. 2001, 305:267-273.
40. Shechter R., et al. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med. 2009, 6:e1000113.
41. Shinozaki Y., et al. Microglia trigger astrocyte-mediated neuroprotection via purinergic gliotransmission. Sci. Rep. 2014, 4:4329.
42. Soderblom C., et al. Perivascular fibroblasts form the fibrotic scar after contusive spinal cord injury. J. Neurosci. 2013, 33:13882-13887.
43. Yata Y., et al. DNase I-hypersensitive sites enhance alpha1(I) collagen gene expression in hepatic stellate cells. Hepatology 2003, 37:267-276.
44. Yona S., et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 2013, 38:79-91.