A selective phosphodiesterase-4 inhibitor reduces leukocyte infiltration, oxidative processes, and tissue damage after spinal cord injury

Journal of Neurotrauma

Volumn 28, Issue 6, 2011, Pages 1035-1049

  Bao, Feng ^a   Fleming, Jennifer C ^a   Golshani, Roozbeh ^b   Pearse, Damien D ^b   Kasabov, Levent ^a   Brown, Arthur ^a   Weaver, Lynne C ^a  

^a WESTERN UNIVERSITY   (Canada)

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

Author keywords

free radical; IC486051; inflammation; lipid peroxidation; phosphodiesterase type 4 inhibitor

Indexed keywords

CYCLOOXYGENASE 2; FREE RADICAL; GLYCOPROTEIN GP 91; IC 486051; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPID; MYELOPEROXIDASE; PHOSPHODIESTERASE IV; PHOSPHODIESTERASE IV INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; LEUKOCYTE; LIPID PEROXIDATION; MALE; MOTOR PERFORMANCE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; SPINAL CORD; SPINAL CORD INJURY; TISSUE INJURY;

ANIMALS; CHEMOTAXIS, LEUKOCYTE; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; DISEASE MODELS, ANIMAL; FEMALE; MALE; MYELITIS; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PHOSPHODIESTERASE 4 INHIBITORS; RATS; RATS, WISTAR; SPINAL CORD INJURIES;

EID: 79959723303     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2010.1575     Document Type: Article

References (55)

1. Agwu, D.E., McCall, C,E., and McPhail, L.C (1991). Regulation of phospholipase D-induced hydrolysis of choline-containing phosphoglycerides by cyclic AMP in human neutrophils. J. Immunol. 146, 3895-3903.
2. Anderson, R., Goolam, M.A., Theron, A.J., Ramafi, G., and Feldman, C. (1998). Effect of rolipram and dibutyryl cyclic AMP on resequestration of cytosolic calcium in FMLPactivated human neutrophils. Br. J. Pharmacol. 124, 547-555. (Pubitemid 28254512)
3. Ariga, M., Neitzert, B., Nakae, S., Mottin, G., Bertrand, C., Pruniaux, M.P., Jin, S.L., and Conti, M. (2004). Nonredundant function of phosphodiesterases 4D and 4B in neutrophil recruitment to the site of inflammation. J. Immunol. 173, 7531-7538. (Pubitemid 39628194)
4. Aronoff, D.M., Canetti, C., Serezani, C.H., Luo, M., and Peters- Golden, M. (2005). Cutting edge: macrophage inhibition by cyclic AMP (cAMP): differential roles of protein kinase A and exchange protein directly activated by cAMP-1. J. Immunol. 174, 595-599. (Pubitemid 40094248)
5. Atkins, C.M., Oliva, A.A., Jr.., Alonso, O.F., Pearse, D.D., Bramlett, H.M., and Dietrich, W.D. (2007). Modulation of the cAMP signaling pathway after traumatic brain injury. Exp. Neurol. 208, 145-158. (Pubitemid 47600157)
6. Bao, F., and Liu, D. (2004). Hydroxyl radicals generated in the rat spinal cord at the level produced by impact injury induce cell death by necrosis and apoptosis: protection by a metalloporphyrin. Neuroscience 126, 285-295. (Pubitemid 38780804)
7. Bao, F., Chen, Y., Dekaban, G.A., and Weaver, L.C. (2004a). An anti-CD11d integrin antibody reduces cyclooxygenase-2 expression and protein and DNA oxidation after spinal cord injury in rats. J. Neurochem. 90, 1194-1204. (Pubitemid 39167352)
8. Bao, F., Chen, Y., Dekaban, G.A., and Weaver, L.C. (2004b). Early anti-inflammatory treatment reduces lipid peroxidation and protein nitration after spinal cord injury in rats. J. Neurochem. 88, 1335-1344. (Pubitemid 38366908)
9. Bao, F., Dekaban, G.A., and Weaver, L.C. (2005). Anti-CD11d antibody treatment reduces free radical formation and cell death in the injured spinal cord of rats. J. Neurochem. 94, 1361-1373. (Pubitemid 41232591)
10. Basso, D.M., Beattie, M.S., and Bresnahan, J.C. (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12, 1-21.
11. Beaumont, E., Whitaker, C.M., Burke, D.A., Hetman, M., and Onifer, S.M. (2009). Effects of rolipram on adult rat oligodendrocytes and functional recovery after contusive cervical spinal cord injury. Neuroscience 163, 985-990.
12. Beavo, J.A., and Brunton, L.L. (2002). Cyclic nucleotide research-still expanding after half a century. Nat. Rev. Mol. Cell Biol. 3, 710-718. (Pubitemid 34987792)
13. Berends, C., Dijkhuizen, B., de Monchy, J.G., Dubois, A.E., Gerritsen, J., and Kauffman, H.F. (1997). Inhibition of PAFinduced expression of CD11b and shedding of L-selectin on human neutrophils and eosinophils by the type IV selective PDE inhibitor, rolipram. Eur. Respir. J. 10, 1000-1007. (Pubitemid 27201801)
14. Borland, G., Smith, B.O., and Yarwood, S.J. (2009). EPAC proteins transduce diverse cellular actions of cAMP. Br. J. Pharmacol. 158, 70-86.
15. Bretzner, F., Plemel, J.R., Liu, J., Richter, M., Roskams, A.J., and Tetzlaff, W. (2010). Combination of olfactory ensheathing cells with local versus systemic cAMP treatment after a cervical rubrospinal tract injury. J. Neurosci. Res. 88, 2833-2846.
16. Bruno, O., Brullo, C., Arduino, N., Schenone, S., Ranise, A., Bondavalli, F., Ottonello, L., Dapino, P., and Dallegri, F. (2004). Synthesis and biological evaluation of neutrophilic inflammation inhibitors. Farmaco 59, 223-235. (Pubitemid 38251620)
17. Christensen, M.D., Everhart, A.W., Pickelman, J.T., and Hulsebosch, C.E. (1996). Mechanical and thermal allodynia in chronic central pain following spinal cord injury. Pain 68, 97-107. (Pubitemid 126407761)
18. Derian, C.K., Santulli, R.J., Rao, P.E., Solomon, H.F., and Barrett, J.A. (1995). Inhibition of chemotactic peptide-induced neutrophil adhesion to vascular endothelium by cAMP modulators. J. Immunol. 154, 308-317.
19. Dinter, H., Tse, J., Halks-Miller, M., Asarnow, D., Onuffer, J., Faulds, D., Mitrovic, B., Kirsch, G., Laurent, H., Esperling, P., Seidelmann, D., Ottow, E., Schneider, H., Tuohy, V.K., Wachtel, H., and Perez, H.D. (2000). The type IV phosphodiesterase specific inhibitor mesopram inhibits experimental autoimmune encephalomyelitis in rodents. J. Neuroimmunol. 108, 136-146. (Pubitemid 30438761)
20. Fleming, J.C., Bao, F., Chen, Y., Hamilton, E.F., Relton, J.K., and Weaver, L.C. (2008). a4b1 integrin blockade after spinal cord injury decreases damage and improves neurological function. Exp. Neurol. 214, 147-159.
21. Giembycz, M.A. (2000). Phosphodiesterase 4 inhibitors and the treatment of asthma: where are we now and where do we go from here? Drugs 59, 193-212. (Pubitemid 30168507)
22. Gris, D., Marsh, D.R., Oatway, M.A., Chen, Y., Hamilton, E.F., Dekaban, G.A., and Weaver, L.C. (2004). Transient blockade of the CD11d/CD18 integrin reduces secondary damage after spinal cord injury, improving sensory, autonomic, and motor function. J. Neurosci. 24, 4043-4051. (Pubitemid 38544230)
23. Griswold, D.E, Webb, E.F., Breton, J., White, J.R., Marshall, P.J., and Torphy, T.J. (1993). Effect of selective phosphodiesterase type IV inhibitor, rolipram, on fluid and cellular phases of inflammatory response. Inflammation 17, 333-344. (Pubitemid 23161286)
24. Harvath, L., Robbins, J.D., Russell, A.A., and Seamon, K.B. (1991). cAMP and human neutrophil chemotaxis. Elevation of cAMP differentially affects chemotactic responsiveness. J. Immunol. 146, 224-232.
25. Hertz, A.L., Bender, A.T., Smith, K.C., Gilchrist, M., Amieux, P.S., Aderem, A., and Beavo, J.A. (2009). Elevated cyclic AMP and PDE4 inhibition induce chemokine expression in human monocyte-derived macrophages. Proc. Natl. Acad. Sci. USA 106, 21978-21983.
26. Houslay, M.D., and Adams, D.R. (2003). PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem. J. 370, 1-18. (Pubitemid 36259414)
27. Iannotti, C.A., Clark, M., Horn, K.P., Van Rooijen, N., Silver, J., and Steinmetz, M.P. (2010). A combination immunomodulatory treatment promotes neuroprotection and locomotor recovery after contusion SCI. Exp. Neurol.
28. Koopmans, G.C., Deumens, R., Buss, A., Geoghegan, L., Myint, A.M., Honig, W.H., Kern, N., Joosten, E.A., Noth, J., and Brook, G.A. (2009). Acute rolipram/thalidomide treatment improves tissue sparing and locomotion after experimental spinal cord injury. Exp. Neurol. 216, 490-498.
29. Mabon, P.J., Weaver, L.C., and Dekaban, G.A. (2000). Inhibition of monocyte/macrophage migration to a spinal cord injury site by an antibody to the integrin alphaD: A potential new anti-inflammatory treatment. Exp. Neurol. 166, 52-64.
30. Martin, M.C., Dransfield, I., Haslett, C., and Rossi, A.G. (2001). Cyclic AMP regulation of neutrophil apoptosis occurs via a novel protein kinase A-independent signaling pathway. J. Biol. Chem. 276, 45041-45050.
31. Nagasawa, S.Y., Takuwa, N., Sugimoto, N., Mabuchi, H., and Takuwa, Y. (2005). Inhibition of Rac activation as a mechanism for negative regulation of actin cytoskeletal reorganization and cell motility by cAMP. Biochem. J. 385, 737-744. (Pubitemid 40208834)
32. Nikulina, E., Tidwell, J.L., Dai, H.N., Bregman, B.S., and Filbin, M.T. (2004). The phosphodiesterase inhibitor rolipram delivered after a spinal cord lesion promotes axonal regeneration and functional recovery. Proc. Natl. Acad. Sci. USA 101, 8786-8790. (Pubitemid 38745849)
33. Nishiguchi, J., Kwon, D.D., Kaiho, Y., Chancellor, M.B., Kumon, H., Snyder, P.B., and Yoshimura, N. (2007). Suppression of detrusor overactivity in rats with bladder outlet obstruction by a type 4 phosphodiesterase inhibitor. BJU Int. 99, 680-686. (Pubitemid 46238850)
34. Oatway, M.A., Chen, Y., Bruce, J.C., Dekaban, G.A., and Weaver, L.C. (2005). An anti-CD11d integrin antibody treatment restores normal serotonergic projections to the dorsal, intermediate and ventral horns of the injured spinal cord. J. Neurosci. 25, 637-647.
35. Ottonello, L., Morone, M.P., Dapino, P., and Dallegri, F. (1995). Cyclic AMP-elevating agents down-regulate the oxidative burst induced by granulocyte-macrophage colony-stimulating factor (GM-CSF) in adherent neutrophils. Clin. Exp. Immunol. 101, 502-506.
36. Pearse, D.D., Lo, T.P., Jr.., Cho, K.S., Lynch, M.P., Garg, M.S., Marcillo, A.E., Sanchez, A.R., Cruz, Y., and Dietrich, W.D. (2005). Histopathological and behavioral characterization of a novel cervical spinal cord displacement contusion injury in the rat. J. Neurotrauma 22, 680-702. (Pubitemid 40840383)
37. Pearse, D.D., Pereira, F.C., Marcillo, A.E., Bates, M.L., Berrocal, Y.A., Filbin, M.T., and Bunge, M.B. (2004a). cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat. Med. 10, 610-616. (Pubitemid 38796852)
38. Pearse, D.D., Pereira, F.C., Stolyarova, A., Barakat, D.J., and Bunge, M.B. (2004b). Inhibition of tumour necrosis factoralpha by antisense targeting produces immunophenotypical and morphological changes in injury-activated microglia and macrophages. Eur. J. Neurosci. 20, 3387-3396. (Pubitemid 40013548)
39. Pryzwansky, K.B., and Madden, V.J. (2003). Type 4A cAMPspecific phosphodiesterase is stored in granules of human neutrophils and eosinophils. Cell Tissue Res. 312, 301-311. (Pubitemid 36831424)
40. Rossi, A.G., McCutcheon, J.C., Roy, N., Chilvers, E.R., Haslett, C., and Dransfield, I. (1998). Regulation of macrophage phagocytosis of apoptotic cells by cAMP. J. Immunol. 160, 3562-3568. (Pubitemid 28164752)
41. Saville, L.R., Pospisil, C.H., Mawhinney, L.A., Bao, F., Simedria, F.C., Peters, A.A., OConnell, P.J., Weaver, L.C., and Dekaban, G.A. (2004). A monoclonal antibody to CD11d reduces the inflammatory infiltrate into the injured spinal cord: A potential neuroprotective treatment. J. Neuroimmunol. 156, 42-57. (Pubitemid 39304184)
42. Schaal, S.M., Kitay, B.M., Cho, K.S., Lo, T.P., Jr.., Barakat, D.J., Marcillo, A.E., Sanchez, A.R., Andrade, C.M., and Pearse, D.D. (2007). Schwann cell transplantation improves reticulospinal axon growth and forelimb strength after severe cervical spinal cord contusion. Cell Transplant 16, 207-228. (Pubitemid 47300228)
43. Schultz, J.E., and Folkers, G. (1988). Unusual stereospecificity of the potential antidepressant rolipram on the cyclic AMP generating system from rat brain cortex. Pharmacopsychiatry 21, 83-86.
44. Semmler, J., Wachtel, H., and Endres, S. (1993). The specific type IV phosphodiesterase inhibitor rolipram suppresses tumor necrosis factor-alpha production by human mononuclear cells. Int. J. Immunopharmacol. 15, 409-413. (Pubitemid 23153552)
45. Snedecor, G., and Cochran, W.G. (1989). Statistical Methods. Iowa State University Press: Iowa City, pp. 503.
46. Snyder, P., Loughney, K., and Florio, V. (2005). Relaxation of bladder strips by inhibition of cyclic nucleotide phosphodiesterase type 4 (PDE4). J. Urol. 173, 43A.
47. Taoka, Y., Okajima, K., Uchiba, M., Murakami, K., Kushimoto, S., Johno, M., Naruo, M., Okabe, H., and Takatsuki, K. (1997). Role of neutrophils in spinal cord injury in the rat. Neuroscience 79, 1177-1182. (Pubitemid 27293767)
48. Torphy, T.J. (1998). Phosphodiesterase isozymes: molecular targets for novel antiasthma agents. Am. J. Respir. Crit. Care Med. 157, 351-370. (Pubitemid 28090521)
49. Verghese, M.W., McConnell, R.T., Lenhard, J.M., Hamacher, L., and Jin, S.L. (1995). Regulation of distinct cyclic AMP-specific phosphodiesterase (phosphodiesterase type 4) isozymes in human monocytic cells. Mol. Pharmacol. 47, 1164-1171.
50. Weaver, L.C., Verghese, P., Bruce, J.C., Fehlings, M.G., Krenz, N.R., and Marsh, D.R. (2001). Autonomic dysreflexia and primary afferent sprouting after clip-compression injury of the rat spinal cord. J. Neurotrauma 18, 1107-1119. (Pubitemid 33000679)
51. Weiss, S.J. (1989). Tissue destruction by neutrophils. N. Engl. J. Med. 320, 365-376. (Pubitemid 19106873)
52. Whitaker, C.M., Beaumont, E., Wells, M.J., Magnuson, D.S., Hetman, M., and Onifer, S.M. (2008). Rolipram attenuates acute oligodendrocyte death in the adult rat ventrolateral funiculus following contusive cervical spinal cord injury. Neurosci. Lett. 438, 200-204.
53. Wiemelt, A.P., Engleka, M.J., Skorupa, A.F., and McMorris, F.A. (1997). Immunochemical visualization and quantitation of cyclic AMP in single cells. J. Biol. Chem. 272, 31489-31495. (Pubitemid 28013289)
54. Zhu, J., Mix, E., and Winblad, B. (2001). The antidepressant and antiinflammatory effects of rolipram in the central nervous system. CNS Drug Rev. 7, 387-398. (Pubitemid 34263873)
55. Zidek, Z. (1999). Adenosine-cyclic AMP pathways and cytokine expression. Eur. Cytokine Netw. 10, 319-328. (Pubitemid 29415384)