Recombinant Slit2 attenuates neuroinflammation after surgical brain injury by inhibiting peripheral immune cell infiltration via Robo1-srGAP1 pathway in a rat model

Neurobiology of Disease

Volumn 85, Issue , 2016, Pages 164-173

  Sherchan, Prativa ^a   Huang, Lei ^a,b   Wang, Yuechun ^a   Akyol, Onat ^a   Tang, Jiping ^a   Zhang, John H ^a,b  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOMA LINDA UNIVERSITY   (United States)

Author keywords

Brain edema; Cdc42; Neuroinflammation; Peripheral immune cell infiltration; Robo1; Slit2; SrGAP1; Surgical brain injury

Indexed keywords

ANTIINFLAMMATORY AGENT; CARRIER PROTEIN; CD45 ANTIGEN; MYELOPEROXIDASE; PROTEIN CDC42; RECEPTOR ROUNDABOUT 1; RECOMBINANT PROTEIN; RECOMBINANT SLIT2; ROUNDABOUT RECEPTOR; SLIT ROBO GTPASE ACTIVATING PROTEIN 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; GAP1 PROTEIN, RAT; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; IMMUNOGLOBULIN RECEPTOR; NERVE PROTEIN; SIGNAL PEPTIDE; SLIT HOMOLOG 2 PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BRAIN INJURY; BRAIN WATER; CELL INFILTRATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MALE; MIGRATION INHIBITION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SURVIVAL RATE; WESTERN BLOTTING; ANIMAL; BRAIN EDEMA; BRAIN INJURIES; DISEASE MODEL; FRONTAL LOBE; GENE SILENCING; GENE THERAPY; GENETICS; IMMUNOLOGY; INJURIES; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; INTRAOPERATIVE COMPLICATIONS; METABOLISM; PROCEDURES; SPRAGUE DAWLEY RAT; SURGERY;

ANIMALS; BRAIN EDEMA; BRAIN INJURIES; DISEASE MODELS, ANIMAL; FRONTAL LOBE; GENE KNOCKDOWN TECHNIQUES; GENETIC THERAPY; GTPASE-ACTIVATING PROTEINS; INFUSIONS, INTRAVENTRICULAR; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRAOPERATIVE COMPLICATIONS; MALE; NERVE TISSUE PROTEINS; RATS, SPRAGUE-DAWLEY; RECEPTORS, IMMUNOLOGIC; RECOMBINANT PROTEINS;

EID: 84946763550     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.11.003     Document Type: Article

References (46)

1. Altay T., McLaughlin B., Wu J.Y., Park T.S., Gidday J.M. Slit modulates cerebrovascular inflammation and mediates neuroprotection against global cerebral ischemia. Exp. Neurol. 2007, 207:186-194.
2. Altay O., Hasegawa Y., Sherchan P., Suzuki H., Khatibi N.H., Tang J., Zhang J.H. Isoflurane delays the development of early brain injury after subarachnoid hemorrhage through sphingosine-related pathway activation in mice. Crit. Care Med. 2012, 40:1908-1913.
3. Ayer R.E., Jafarian N., Chen W., Applegate R.L., Colohan A.R., Zhang J.H. Preoperative mucosal tolerance to brain antigens and a neuroprotective immune response following surgical brain injury. J. Neurosurg. 2012, 116:246-253.
4. Ballard M.S., Hinck L. A roundabout way to cancer. Adv. Cancer Res. 2012, 114:187-235.
5. Bishop A.L., Hall A. Rho GTPases and their effector proteins. Biochem. J. 2000, 348 Pt 2:241-255.
6. Bruder N.J. Awakening management after neurosurgery for intracranial tumours. Curr. Opin. Anaesthesiol. 2002, 15:477-482.
7. Chen S., Ma Q., Krafft P.R., Hu Q., Rolland W., Sherchan P., Zhang J., Tang J., Zhang J.H. P2X7R/cryopyrin inflammasome axis inhibition reduces neuroinflammation after SAH. Neurobiol. Dis. 2013, 58:296-307.
8. Doyle K.P., Yang T., Lessov N.S., Ciesielski T.M., Stevens S.L., Simon R.P., King J.S., Stenzel-Poore M.P. Nasal administration of osteopontin peptide mimetics confers neuroprotection in stroke. J. Cereb. Blood Flow Metab. 2008, 28:1235-1248.
9. Garcia J.H., Wagner S., Liu K.F., Hu X.J. Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats. Statistical validation. Stroke 1995, 26:627-634. (discussion 635).
10. Guan K.L., Rao Y. Signalling mechanisms mediating neuronal responses to guidance cues. Nat. Rev. Neurosci. 2003, 4:941-956.
11. Hagino S., Iseki K., Mori T., Zhang Y., Hikake T., Yokoya S., Takeuchi M., Hasimoto H., Kikuchi S., Wanaka A. Slit and glypican-1 mRNAs are coexpressed in the reactive astrocytes of the injured adult brain. Glia 2003, 42:130-138.
12. Hasegawa Y., Suzuki H., Altay O., Zhang J.H. Preservation of tropomyosin-related kinase B (TrkB) signaling by sodium orthovanadate attenuates early brain injury after subarachnoid hemorrhage in rats. Stroke 2011, 42:477-483.
13. Hickey W.F. Leukocyte traffic in the central nervous system: the participants and their roles. Semin. Immunol. 1999, 11:125-137.
14. Hu Q., Liang X., Chen D., Chen Y., Doycheva D., Tang J., Zhang J.H. Delayed hyperbaric oxygen therapy promotes neurogenesis through reactive oxygen species/hypoxia-inducible factor-1alpha/beta-catenin pathway in middle cerebral artery occlusion rats. Stroke 2014, 45:1807-1814.
15. Huang K.F., Hsu W.C., Hsiao J.K., Chen G.S., Wang J.Y. Collagen-glycosaminoglycan matrix implantation promotes angiogenesis following surgical brain trauma. BioMed Res. Int. 2014, 2014:672409.
16. Hyong A., Jadhav V., Lee S., Tong W., Rowe J., Zhang J.H., Tang J. Rosiglitazone, a PPAR gamma agonist, attenuates inflammation after surgical brain injury in rodents. Brain Res. 2008, 1215:218-224.
17. Jadhav V., Matchett G., Hsu F.P., Zhang J.H. Inhibition of Src tyrosine kinase and effect on outcomes in a new in vivo model of surgically induced brain injury. J. Neurosurg. 2007, 106:680-686.
18. Jadhav V., Solaroglu I., Obenaus A., Zhang J.H. Neuroprotection against surgically induced brain injury. Surg. Neurol. 2007, 67:15-20. (discussion 20).
19. Jones C.A., London N.R., Chen H., Park K.W., Sauvaget D., Stockton R.A., Wythe J.D., Suh W., Larrieu-Lahargue F., Mukouyama Y.S., Lindblom P., Seth P., Frias A., Nishiya N., Ginsberg M.H., Gerhardt H., Zhang K., Li D.Y. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat. Med. 2008, 14:448-453.
20. Jones C.A., Nishiya N., London N.R., Zhu W., Sorensen L.K., Chan A.C., Lim C.J., Chen H., Zhang Q., Schultz P.G., Hayallah A.M., Thomas K.R., Famulok M., Zhang K., Ginsberg M.H., Li D.Y. Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat. Cell Biol. 2009, 11:1325-1331.
21. Kanellis J., Garcia G.E., Li P., Parra G., Wilson C.B., Rao Y., Han S., Smith C.W., Johnson R.J., Wu J.Y., Feng L. Modulation of inflammation by slit protein in vivo in experimental crescentic glomerulonephritis. Am. J. Pathol. 2004, 165:341-352.
22. Krafft P.R., McBride D.W., Lekic T., Rolland W.B., Mansell C.E., Ma Q., Tang J., Zhang J.H. Correlation between subacute sensorimotor deficits and brain edema in two mouse models of intracerebral hemorrhage. Behav. Brain Res. 2014, 264:151-160.
23. Kumar S., Xu J., Perkins C., Guo F., Snapper S., Finkelman F.D., Zheng Y., Filippi M.D. Cdc42 regulates neutrophil migration via crosstalk between WASp, CD11b, and microtubules. Blood 2012, 120:3563-3574.
24. Li Q., Xu M., Zhou J.X. Correlation of measured and calculated serum osmolality during mannitol or hypertonic saline infusion in patients after craniotomy: a study protocol and statistical analysis plan for a randomised controlled trial. BMJ open 2014, 4.
25. Lo E.H. T time in the brain. Nat. Med. 2009, 15:844-846.
26. London N.R., Zhu W., Bozza F.A., Smith M.C., Greif D.M., Sorensen L.K., Chen L., Kaminoh Y., Chan A.C., Passi S.F., Day C.W., Barnard D.L., Zimmerman G.A., Krasnow M.A., Li D.Y. Targeting Robo4-dependent Slit signaling to survive the cytokine storm in sepsis and influenza. Sci. Transl. Med. 2010, 2.
27. Ma Q., Chen S., Hu Q., Feng H., Zhang J.H., Tang J. NLRP3 inflammasome contributes to inflammation after intracerebral hemorrhage. Ann. Neurol. 2014, 75:209-219.
28. Marillat V., Cases O., Nguyen-Ba-Charvet K.T., Tessier-Lavigne M., Sotelo C., Chedotal A. Spatiotemporal expression patterns of slit and robo genes in the rat brain. J. Comp. Neurol. 2002, 442:130-155.
29. McBride D.W., Wang Y., Sherchan P., Tang J., Zhang J.H. Correlation between subacute sensorimotor deficits and brain water content after surgical brain injury in rats. Behav. Brain Res. 2015, 290:161-171.
30. Mertsch S., Schmitz N., Jeibmann A., Geng J.G., Paulus W., Senner V. Slit2 involvement in glioma cell migration is mediated by Robo1 receptor. J. Neuro-Oncol. 2008, 87:1-7.
31. Petty M.A., Lo E.H. Junctional complexes of the blood-brain barrier: permeability changes in neuroinflammation. Prog. Neurobiol. 2002, 68:311-323.
32. Prasad A., Qamri Z., Wu J., Ganju R.K. Slit-2/Robo-1 modulates the CXCL12/CXCR4-induced chemotaxis of T cells. J. Leukoc. Biol. 2007, 82:465-476.
33. Ransohoff R.M., Kivisakk P., Kidd G. Three or more routes for leukocyte migration into the central nervous system. Nat. Rev. Immunol. 2003, 3:569-581.
34. Rhodes J. Peripheral immune cells in the pathology of traumatic brain injury?. Curr. Opin. Crit. Care 2011, 17:122-130.
35. Suzuki H., Hasegawa Y., Kanamaru K., Zhang J.H. Mechanisms of osteopontin-induced stabilization of blood-brain barrier disruption after subarachnoid hemorrhage in rats. Stroke 2010, 41:1783-1790.
36. Tole S., Mukovozov I.M., Huang Y.W., Magalhaes M.A., Yan M., Crow M.R., Liu G.Y., Sun C.X., Durocher Y., Glogauer M., Robinson L.A. The axonal repellent, Slit2, inhibits directional migration of circulating neutrophils. J. Leukoc. Biol. 2009, 86:1403-1415.
37. Wang J., Dore S. Inflammation after intracerebral hemorrhage. J. Cereb. Blood Flow Metab. 2007, 27:894-908.
38. Wong K., Ren X.R., Huang Y.Z., Xie Y., Liu G., Saito H., Tang H., Wen L., Brady-Kalnay S.M., Mei L., Wu J.Y., Xiong W.C., Rao Y. Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 2001, 107:209-221.
39. Wong K., Park H.T., Wu J.Y., Rao Y. Slit proteins: molecular guidance cues for cells ranging from neurons to leukocytes. Curr. Opin. Genet. Dev. 2002, 12:583-591.
40. Wu J.Y., Feng L., Park H.T., Havlioglu N., Wen L., Tang H., Bacon K.B., Jiang Z., Zhang X., Rao Y. The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors. Nature 2001, 410:948-952.
41. Xu F.F., Sun S., Ho A.S., Lee D., Kiang K.M., Zhang X.Q., Wang A.M., Wu E.X., Lui W.M., Liu B.Y., Leung G.K. Effects of progesterone vs. dexamethasone on brain oedema and inflammatory responses following experimental brain resection. Brain Inj. 2014, 28:1594-1601.
42. Yamaguchi M., Jadhav V., Obenaus A., Colohan A., Zhang J.H. Matrix metalloproteinase inhibition attenuates brain edema in an in vivo model of surgically-induced brain injury. Neurosurgery 2007, 61:1067-1075. (discussion 1075-1066).
43. Ye B.Q., Geng Z.H., Ma L., Geng J.G. Slit2 regulates attractive eosinophil and repulsive neutrophil chemotaxis through differential srGAP1 expression during lung inflammation. J. Immunol. 2010, 185:6294-6305.
44. Yiin J.J., Hu B., Jarzynka M.J., Feng H., Liu K.W., Wu J.Y., Ma H.I., Cheng S.Y. Slit2 inhibits glioma cell invasion in the brain by suppression of Cdc42 activity. Neuro-Oncology 2009, 11:779-789.
45. Yilmaz G., Arumugam T.V., Stokes K.Y., Granger D.N. Role of T lymphocytes and interferon-gamma in ischemic stroke. Circulation 2006, 113:2105-2112.
46. Zhao H., Anand A.R., Ganju R.K. Slit2-Robo4 pathway modulates lipopolysaccharide-nduced endothelial inflammation and its expression is dysregulated during endotoxemia. J. Immunol. 2014, 192:385-393.