PARP inhibition in leukocytes diminishes inflammation via effects on integrins/cytoskeleton and protects the blood-brain barrier

Journal of Neuroinflammation

Volumn 13, Issue 1, 2016, Pages

  Rom, Slava ^a   Zuluaga Ramirez, Viviana ^a   Reichenbach, Nancy L ^a   Dykstra, Holly ^a   Gajghate, Sachin ^a   Pacher, Pal ^b   Persidsky, Yuri ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

Actin cytoskeleton; Leukocyte endothelial interaction; LFA 1; PARP 1; VLA 4

Indexed keywords

INTEGRIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TUMOR NECROSIS FACTOR;

ACTIN FILAMENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASEPTIC MENINGITIS; BLOOD BRAIN BARRIER; BRAIN CAPILLARY ENDOTHELIAL CELL; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKOCYTE; MALE; MONOCYTE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PROTEIN CONFORMATION;

EID: 84988835156     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-016-0729-x     Document Type: Article

References (86)

1. Allport JR, Ding H, Collins T, Gerritsen ME, Luscinskas FW. Endothelial-dependent mechanisms regulate leukocyte transmigration: a process involving the proteasome and disruption of the vascular endothelial-cadherin complex at endothelial cell-to-cell junctions. J Exp Med. 1997;186:517-27.
2. Alon R, Feigelson SW, Manevich E, Rose DM, Schmitz J, Overby DR, Winter E, Grabovsky V, Shinder V, Matthews BD, et al. Alpha4beta1-dependent adhesion strengthening under mechanical strain is regulated by paxillin association with the alpha4-cytoplasmic domain. J Cell Biol. 2005;171:1073-84.
3. Chigaev A, Waller A, Amit O, Halip L, Bologa CG, Sklar LA. Real-time analysis of conformation-sensitive antibody binding provides new insights into integrin conformational regulation. J Biol Chem. 2009;284:14337-46.
4. Hogg N, Patzak I, Willenbrock F. The insider's guide to leukocyte integrin signalling and function. Nat Rev Immunol. 2011;11:416-26.
5. Evans R, Lellouch AC, Svensson L, McDowall A, Hogg N. The integrin LFA-1 signals through ZAP-70 to regulate expression of high-affinity LFA-1 on T lymphocytes. Blood. 2011;117:3331-42.
6. Chigaev A, Sklar LA. Aspects of VLA-4 and LFA-1 regulation that may contribute to rolling and firm adhesion. Front Immunol. 2012;3:242.
7. Cernuda-Morollon E, Ridley AJ. Rho GTPases and leukocyte adhesion receptor expression and function in endothelial cells. Circ Res. 2006;98:757-67.
8. Rom S, Fan S, Reichenbach N, Dykstra H, Ramirez SH, Persidsky Y. Glycogen synthase kinase 3beta inhibition prevents monocyte migration across brain endothelial cells via Rac1-GTPase suppression and down-regulation of active integrin conformation. Am J Pathol. 2012;181:1414-25.
9. Rom S, Zuluaga-Ramirez V, Dykstra H, Reichenbach NL, Pacher P, Persidsky Y. Selective activation of cannabinoid receptor 2 in leukocytes suppresses their engagement of the brain endothelium and protects the blood-brain barrier. Am J Pathol. 2013;183:1548-58.
10. Cavone L, Aldinucci A, Ballerini C, Biagioli T, Moroni F, Chiarugi A. PARP-1 inhibition prevents CNS migration of dendritic cells during EAE, suppressing the encephalitogenic response and relapse severity. Mult Scler. 2011;17:794-807.
11. Martinez-Zamudio RI, Ha HC. PARP1 enhances inflammatory cytokine expression by alteration of promoter chromatin structure in microglia. Brain Behav. 2014;4:552-65.
12. Martire S, Mosca L, d'Erme M. PARP-1 involvement in neurodegeneration: a focus on Alzheimer's and Parkinson's diseases. Mech Ageing Dev. 2015;146-148:53-64.
13. Ahmad SF, Zoheir KM, Ansari MA, Korashy HM, Bakheet SA, Ashour AE, Al-Shabanah OA, Al-harbi MM, Attia SM. The role of poly (ADP-ribose) polymerase-1 inhibitor in carrageenan-induced lung inflammation in mice. Mol Immunol. 2015;63:394-405.
14. Canan S, Maegley K, Curtin N. Strategies employed for the development of PARP inhibitors. Methods Mol Biol. 2011;780:463-89.
15. Wahlberg E, Karlberg T, Kouznetsova E, Markova N, Macchiarulo A, Thorsell AG, Pol E, Frostell A, Ekblad T, Oncu D, et al. Family-wide chemical profiling and structural analysis of PARP and tankyrase inhibitors. Nat Biotechnol. 2012;30:283-8.
16. Qiu W, Lam R, Voytyuk O, Romanov V, Gordon R, Gebremeskel S, Vodsedalek J, Thompson C, Beletskaya I, Battaile KP, et al. Insights into the binding of PARP inhibitors to the catalytic domain of human tankyrase-2. Acta Crystallogr D Biol Crystallogr. 2014;70:2740-53.
17. d'Avila JC, Lam TI, Bingham D, Shi J, Won SJ, Kauppinen TM, Massa S, Liu J, Swanson RA. Microglial activation induced by brain trauma is suppressed by post-injury treatment with a PARP inhibitor. J Neuroinflammation. 2012;9:31.
18. Kauppinen TM, Suh SW, Genain CP, Swanson RA. Poly (ADP-ribose) polymerase-1 activation in a primate model of multiple sclerosis. J Neurosci Res. 2005;81:190-8.
19. Koedel U, Winkler F, Angele B, Fontana A, Pfister HW. Meningitis-associated central nervous system complications are mediated by the activation of poly (ADP-ribose) polymerase. J Cereb Blood Flow Metab. 2002;22:39-49.
20. Ahmad SF, Zoheir KM, Bakheet SA, Ashour AE, Attia SM. Poly (ADP-ribose) polymerase-1 inhibitor modulates T regulatory and IL-17 cells in the prevention of adjuvant induced arthritis in mice model. Cytokine. 2014;68:76-85.
21. Horvath B, Magid L, Mukhopadhyay P, Batkai S, Rajesh M, Park O, Tanchian G, Gao RY, Goodfellow CE, Glass M, et al. A new cannabinoid CB2 receptor agonist HU-910 attenuates oxidative stress, inflammation and cell death associated with hepatic ischaemia/reperfusion injury. Br J Pharmacol. 2012;165:2462-78.
22. Pasqualetti G, Brooks DJ, Edison P. The role of neuroinflammation in dementias. Curr Neurol Neurosci Rep. 2015;15:17.
23. Lecuyer MA, Kebir H, Prat A. Glial influences on BBB functions and molecular players in immune cell trafficking. Biochim Biophys Acta. 1862;2015:472-82.
24. Persidsky Y, Ramirez SH, Haorah J, Kanmogne GD. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol. 2006;1:223-36.
25. Gorina R, Lyck R, Vestweber D, Engelhardt B. beta2 integrin-mediated crawling on endothelial ICAM-1 and ICAM-2 is a prerequisite for transcellular neutrophil diapedesis across the inflamed blood-brain barrier. J Immunol. 2014;192:324-37.
26. Gelderblom M, Leypoldt F, Steinbach K, Behrens D, Choe CU, Siler DA, Arumugam TV, Orthey E, Gerloff C, Tolosa E, Magnus T. Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke. 2009;40:1849-57.
27. Stevens SL, Bao J, Hollis J, Lessov NS, Clark WM, Stenzel-Poore MP. The use of flow cytometry to evaluate temporal changes in inflammatory cells following focal cerebral ischemia in mice. Brain Res. 2002;932:110-9.
28. Larochelle C, Alvarez JI, Prat A. How do immune cells overcome the blood-brain barrier in multiple sclerosis? FEBS Lett. 2011;585:3770-80.
29. Prat A, Biernacki K, Lavoie JF, Poirier J, Duquette P, Antel JP. Migration of multiple sclerosis lymphocytes through brain endothelium. Arch Neurol. 2002;59:391-7.
30. Luissint AC, Artus C, Glacial F, Ganeshamoorthy K, Couraud PO. Tight junctions at the blood brain barrier: physiological architecture and disease-associated dysregulation. Fluids Barriers CNS. 2012;9:23.
31. Persidsky Y. Insights into end-organ injury in HIV infection: dynamics of monocyte trafficking to the brain in SIV encephalitis. Am J Pathol. 2015;185:1548-51.
32. Tobin MK, Bonds JA, Minshall RD, Pelligrino DA, Testai FD, Lazarov O. Neurogenesis and inflammation after ischemic stroke: what is known and where we go from here. J Cereb Blood Flow Metab. 2014;34:1573-84.
33. Fu Y, Liu Q, Anrather J, Shi FD. Immune interventions in stroke. Nat Rev Neurol. 2015;11:524-35.
34. Chamorro A, Hallenbeck J. The harms and benefits of inflammatory and immune responses in vascular disease. Stroke. 2006;37:291-3.
35. Rom S, Zuluaga-Ramirez V, Dykstra H, Reichenbach N, Ramirez SH, Persidsky Y. Poly (ADP-ribose) polymerase-1 inhibition in brain endothelium protects the blood-brain barrier under physiologic and neuroinflammatory conditions. J Cereb Blood Flow Metab. 2015;35:28-36.
36. Ramirez SH, Heilman D, Morsey B, Potula R, Haorah J, Persidsky Y. Activation of peroxisome proliferator-activated receptor gamma (PPARgamma) suppresses Rho GTPases in human brain microvascular endothelial cells and inhibits adhesion and transendothelial migration of HIV-1 infected monocytes. J Immunol. 2008;180:1854-65.
37. Bernas MJ, Cardoso FL, Daley SK, Weinand ME, Campos AR, Ferreira AJ, Hoying JB, Witte MH, Brites D, Persidsky Y, et al. Establishment of primary cultures of human brain microvascular endothelial cells to provide an in vitro cellular model of the blood-brain barrier. Nat Protoc. 2010;5:1265-72.
38. Aoyagi-Scharber M, Gardberg AS, Yip BK, Wang B, Shen Y, Fitzpatrick PA. Structural basis for the inhibition of poly (ADP-ribose) polymerases 1 and 2 by BMN 673, a potent inhibitor derived from dihydropyridophthalazinone. Acta Crystallogr F Struct Biol Commun. 2014;70:1143-9.
39. Rom S, Reichenbach NL, Dykstra H, Persidsky Y. The dual action of poly (ADP-ribose) polymerase -1 (PARP-1) inhibition in HIV-1 infection: HIV-1 LTR inhibition and diminution in Rho GTPase activity. Front Microbiol. 2015;6:878.
40. Mukhopadhyay P, Rajesh M, Cao Z, Horvath B, Park O, Wang H, Erdelyi K, Holovac E, Wang Y, Liaudet L, et al. Poly (ADP-ribose) polymerase-1 is a key mediator of liver inflammation and fibrosis. Hepatology. 2014;59:1998-2009.
41. Ramirez SH, Hasko J, Skuba A, Fan S, Dykstra H, McCormick R, Reichenbach N, Krizbai I, Mahadevan A, Zhang M, et al. Activation of cannabinoid receptor 2 attenuates leukocyte-endothelial cell interactions and blood-brain barrier dysfunction under inflammatory conditions. J Neurosciences. 2012;32:4004-16.
42. Zuluaga-Ramirez V, Rom S, Persidsky Y. Craniula: A cranial window technique for prolonged imaging of brain surface vasculature with simultaneous adjacent intracerebral injection. Fluids Barriers CNS. 2015;12:24.
43. Rom S, Dykstra H, Zuluaga-Ramirez V, Reichenbach NL, Persidsky Y. miR-98 and let-7g* protect the blood-brain barrier under neuroinflammatory conditions. J Cereb Blood Flow Metab. 2015;35:1957-65.
44. Goldey GJ, Roumis DK, Glickfeld LL, Kerlin AM, Reid RC, Bonin V, Schafer DP, Andermann ML. Removable cranial windows for long-term imaging in awake mice. Nat Protoc. 2014;9:2515-38.
45. Lescot T, Fulla-Oller L, Palmier B, Po C, Beziaud T, Puybasset L, Plotkine M, Gillet B, Meric P, Marchand-Leroux C. Effect of acute poly (ADP-ribose) polymerase inhibition by 3-AB on blood-brain barrier permeability and edema formation after focal traumatic brain injury in rats. J Neurotrauma. 2010;27:1069-79.
46. Moroni F. Poly (ADP-ribose) polymerase 1 (PARP-1) and postischemic brain damage. Curr Opin Pharmacol. 2008;8:96-103.
47. Rouleau M, Patel A, Hendzel MJ, Kaufmann SH, Poirier GG. PARP inhibition: PARP1 and beyond. Nat Rev Cancer. 2010;10:293-301.
48. Veres B, Gallyas Jr F, Varbiro G, Berente Z, Osz E, Szekeres G, Szabo C, Sumegi B. Decrease of the inflammatory response and induction of the Akt/protein kinase B pathway by poly-(ADP-ribose) polymerase 1 inhibitor in endotoxin-induced septic shock. Biochem Pharmacol. 2003;65:1373-82.
49. Lenzser G, Kis B, Snipes JA, Gaspar T, Sandor P, Komjati K, Szabo C, Busija DW. Contribution of poly (ADP-ribose) polymerase to postischemic blood-brain barrier damage in rats. J Cereb Blood Flow Metab. 2007;27:1318-26.
50. Farez MF, Quintana FJ, Gandhi R, Izquierdo G, Lucas M, Weiner HL. Toll-like receptor 2 and poly (ADP-ribose) polymerase 1 promote central nervous system neuroinflammation in progressive EAE. Nat Immunol. 2009;10:958-64.
51. Jagtap P, Szabo C. Poly (ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov. 2005;4:421-40.
52. Zhang C, Yang J, Jennings LK. Attenuation of neointima formation through the inhibition of DNA repair enzyme PARP-1 in balloon-injured rat carotid artery. Am J Physiol Heart Circ Physiol. 2004;287:H659-66.
53. Barthel SR, Johansson MW, McNamee DM, Mosher DF. Roles of integrin activation in eosinophil function and the eosinophilic inflammation of asthma. J Leukoc Biol. 2008;83:1-12.
54. Salas A, Shimaoka M, Kogan AN, Harwood C, Von Andrian UH, Springer TA. Rolling adhesion through an extended conformation of integrin alphaLbeta2 and relation to alpha I and beta I-like domain interaction. Immunity. 2004;20:393-406.
55. Lim YC, Wakelin MW, Henault L, Goetz DJ, Yednock T, Cabanas C, Sanchez-Madrid F, Lichtman AH, Luscinskas FW. Alpha4beta1-integrin activation is necessary for high-efficiency T-cell subset interactions with VCAM-1 under flow. Microcirculation. 2000;7:201-14.
56. Ferreira AM, Isaacs H, Hayflick JS, Rogers KA, Sandig M. The p110delta isoform of PI3K differentially regulates beta1 and beta2 integrin-mediated monocyte adhesion and spreading and modulates diapedesis. Microcirculation. 2006;13:439-56.
57. Sanchez-Martin L, Sanchez-Sanchez N, Gutierrez-Lopez MD, Rojo AI, Vicente-Manzanares M, Perez-Alvarez MJ, Sanchez-Mateos P, Bustelo XR, Cuadrado A, Sanchez-Madrid F, et al. Signaling through the leukocyte integrin LFA-1 in T cells induces a transient activation of Rac-1 that is regulated by Vav and PI3K/Akt-1. J Biol Chem. 2004;279:16194-205.
58. Woska Jr JR, Shih D, Taqueti VR, Hogg N, Kelly TA, Kishimoto TK. A small-molecule antagonist of LFA-1 blocks a conformational change important for LFA-1 function. J Leukoc Biol. 2001;70:329-34.
59. Bolomini-Vittori M, Montresor A, Giagulli C, Staunton D, Rossi B, Martinello M, Constantin G, Laudanna C. Regulation of conformer-specific activation of the integrin LFA-1 by a chemokine-triggered Rho signaling module. Nat Immunol. 2009;10:185-94.
60. Alevriadou BR. CAMs and Rho small GTPases: gatekeepers for leukocyte transendothelial migration. Focus on "VCAM-1-mediated Rac signaling controls endothelial cell-cell contacts and leukocyte transmigration". Am J Physiol Cell Physiol. 2003;285:C250-2.
61. Rolfe BE, Worth NF, World CJ, Campbell JH, Campbell GR. Rho and vascular disease. Atherosclerosis. 2005;183:1-16.
62. Van Buul JD, Hordijk PL. Signaling in leukocyte transendothelial migration. Arterioscler Thromb Vasc Biol. 2004;24:824-33.
63. Etienne-Manneville S, Manneville JB, Adamson P, Wilbourn B, Greenwood J, Couraud PO. ICAM-1-coupled cytoskeletal rearrangements and transendothelial lymphocyte migration involve intracellular calcium signaling in brain endothelial cell lines. J Immunol. 2000;165:3375-83.
64. Samstag Y, Eibert SM, Klemke M, Wabnitz GH. Actin cytoskeletal dynamics in T lymphocyte activation and migration. J Leukoc Biol. 2003;73:30-48.
65. Vicente-Manzanares M, Sanchez-Madrid F. Role of the cytoskeleton during leukocyte responses. Nat Rev Immunol. 2004;4:110-22.
66. Mizuno K. Signaling mechanisms and functional roles of cofilin phosphorylation and dephosphorylation. Cell Signal. 2013;25:457-69.
67. Kameoka M, Ota K, Tetsuka T, Tanaka Y, Itaya A, Okamoto T, Yoshihara K. Evidence for regulation of NF-kappaB by poly (ADP-ribose) polymerase. Biochem J. 2000;346(Pt 3):641-9.
68. Liu L, Ke Y, Jiang X, He F, Pan L, Xu L, Zeng X, Ba X. Lipopolysaccharide activates ERK-PARP-1-RelA pathway and promotes nuclear factor-kappaB transcription in murine macrophages. Hum Immunol. 2012;73:439-47.
69. Nakagawa Y, Sedukhina AS, Okamoto N, Nagasawa S, Suzuki N, Ohta T, Hattori H, Roche-Molina M, Narvaez AJ, Jeyasekharan AD, et al. NF-kB signaling mediates acquired resistance after PARP inhibition. Oncotarget. 2015;6:3825-39.
70. Vuong B, Hogan-Cann AD, Alano CC, Stevenson M, Chan WY, Anderson CM, Swanson RA, Kauppinen TM. NF-kappaB transcriptional activation by TNFalpha requires phospholipase C, extracellular signal-regulated kinase 2 and poly (ADP-ribose) polymerase-1. J Neuroinflammation. 2015;12:229.
71. Zohrabian VM, Forzani B, Chau Z, Murali R, Jhanwar-Uniyal M. Rho/ROCK and MAPK signaling pathways are involved in glioblastoma cell migration and proliferation. Anticancer Res. 2009;29:119-23.
72. Tormos Ana M, Talens-Visconti R, Jorques M, Perez-Garrido S, Bonora-Centelles A, Nebreda Angel R, Sastre J. p38alpha deficiency and oxidative stress cause cytokinesis failure in hepatocytes. Free Radic Biol Med. 2014;75(1):S19.
73. Ba X, Garg NJ. Signaling mechanism of poly (ADP-ribose) polymerase-1 (PARP-1) in inflammatory diseases. Am J Pathol. 2011;178:946-55.
74. Shimizu Y, Dobashi K, Iizuka K, Horie T, Suzuki K, Tukagoshi H, Nakazawa T, Nakazato Y, Mori M. Contribution of small gtpase rho and its target protein rock in a murine model of lung fibrosis. Am J Respir Crit Care Med. 2001;163:210-7.
75. Haider L. Inflammation, iron, energy failure, and oxidative stress in the pathogenesis of multiple sclerosis. Oxid Med Cell Longev. 2015;2015:725370.
76. Uttara B, Singh AV, Zamboni P, Mahajan RT. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol. 2009;7:65-74.
77. Milzani A, DalleDonne I, Colombo R. Prolonged oxidative stress on actin. Arch Biochem Biophys. 1997;339:267-74.
78. Bai P, Nagy L, Fodor T, Liaudet L, Pacher P. Poly (ADP-ribose) polymerases as modulators of mitochondrial activity. Trends Endocrinol Metab. 2015;26:75-83.
79. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 2007;87:315-424.
80. Mathews MT, Berk BC. PARP-1 inhibition prevents oxidative and nitrosative stress-induced endothelial cell death via transactivation of the VEGF receptor 2. Arterioscler Thromb Vasc Biol. 2008;28:711-7.
81. Venter G, Oerlemans FT, Willemse M, Wijers M, Fransen JA, Wieringa B. NAMPT-mediated salvage synthesis of NAD+ controls morphofunctional changes of macrophages. PLoS One. 2014;9, e97378.
82. Virag L, Szabo C. The therapeutic potential of poly (ADP-ribose) polymerase inhibitors. Pharmacol Rev. 2002;54:375-429.
83. Hottiger MO. Poly (ADP-ribose) polymerase inhibitor therapeutic effect: are we just scratching the surface? Expert Opin Ther Targets. 2015;19:1149-52.
84. Jin R, Yang G, Li G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J Leukoc Biol. 2010;87:779-89.
85. Del Zoppo GJ. Inflammation and the neurovascular unit in the setting of focal cerebral ischemia. Neuroscience. 2009;158:972-82.
86. Knowland D, Arac A, Sekiguchi KJ, Hsu M, Lutz SE, Perrino J, Steinberg GK, Barres BA, Nimmerjahn A, Agalliu D. Stepwise recruitment of transcellular and paracellular pathways underlies blood-brain barrier breakdown in stroke. Neuron. 2014;82:603-17.