Postinjury treatment with rolipram increases hemorrhage after traumatic brain injury

Journal of Neuroscience Research

Volumn 90, Issue 9, 2012, Pages 1861-1871

  Atkins, C M ^a   Kang, Y ^a   Furones, C ^a   Truettner, J S ^a   Alonso, O F ^a   Dietrich, W D ^a  

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

Author keywords

Blood brain barrier; CAMP; Cerebral blood flow; Cytokine; Phosphodiesterase

Indexed keywords

CYCLIC AMP; INTERLEUKIN 1BETA; ROLIPRAM; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN CONTUSION; BRAIN CORTEX; BRAIN CORTEX ATROPHY; BRAIN HEMORRHAGE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; HIPPOCAMPUS; HISTOPATHOLOGY; HYDROLYSIS; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; TRAUMATIC BRAIN INJURY; VASODILATATION;

ANIMALS; BRAIN INJURIES; CEREBRAL HEMORRHAGE; CEREBROVASCULAR CIRCULATION; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; MALE; PHOSPHODIESTERASE 4 INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; ROLIPRAM; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84863783775     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23069     Document Type: Article

References (75)

1. Ahn MJ, Sherwood ER, Prough DS, Lin CY, DeWitt DS. 2004. The effects of traumatic brain injury on cerebral blood flow and brain tissue nitric oxide levels and cytokine expression. J Neurotrauma 21: 1431-1442.
2. Ariga M, Neitzert B, Nakae S, Mottin G, Bertrand C, Pruniaux MP, Jin SL, Conti M. 2004. Nonredundant function of phosphodiesterases 4D and 4B in neutrophil recruitment to the site of inflammation. J Immunol 173: 7531-7538.
3. Atkins CM, Oliva AA Jr, Alonso OF, Pearse DD, Bramlett HM, Dietrich WD. 2007. Modulation of the cAMP signaling pathway after traumatic brain injury. Exp Neurol 208: 145-158.
4. Barad M, Bourtchouladze R, Winder DG, Golan H, Kandel E. 1998. Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc Natl Acad Sci U S A 95: 15020-15025.
5. 3H]rolipram binding. Biochem Pharmacol 51: 949-956.
6. Beaumont E, Whitaker CM, Burke DA, Hetman M, Onifer SM. 2009. Effects of rolipram on adult rat oligodendrocytes and functional recovery after contusive cervical spinal cord injury. Neuroscience 163: 985-990.
7. Birk S, Edvinsson L, Olesen J, Kruuse C. 2004. Analysis of the effects of phosphodiesterase type 3 and 4 inhibitors in cerebral arteries. Eur J Pharmacol 489: 93-100.
8. Block F, Tondar A, Schmidt W, Schwarz M. 1997. Delayed treatment with rolipram protects against neuronal damage following global ischemia in rats. Neuroreport 8: 3829-3832.
9. Block F, Schmidt W, Nolden-Koch M, Schwarz M. 2001. Rolipram reduces excitotoxic neuronal damage. Neuroreport 12: 1507-1511.
10. Bramlett HM, Dietrich WD. 2002. Quantitative structural changes in white and gray matter 1 year following traumatic brain injury in rats. Acta Neuropathol 103: 607-614.
11. 2+ responses in endothelial cells. Br J Pharmacol 154: 82-92.
12. Chang YC, Huang CC, Hung PL, Huang HM. 2008. Rolipram, a phosphodiesterase type IV inhibitor, exacerbates periventricular white matter lesions in rat pups. Pediatr Res 64: 234-239.
13. Dietrich WD, Alonso O, Busto R, Prado R, Dewanjee S, Dewanjee MK, Ginsberg MD. 1996. Widespread hemodynamic depression and focal platelet accumulation after fluid percussion brain injury: a double-label autoradiographic study in rats. J Cereb Blood Flow Metab 16: 481-489.
14. Dietrich WD, Alonso O, Busto R, Prado R, Zhao W, Dewanjee MK, Ginsberg MD. 1998. Posttraumatic cerebral ischemia after fluid percussion brain injury: an autoradiographic and histopathological study in rats. Neurosurgery 43: 585-593.
15. Dlaboga D, Hajjhussein H, O'Donnell JM. 2006. Regulation of phosphodiesterase-4 (PDE4) expression in mouse brain by repeated antidepressant treatment: comparison with rolipram. Brain Res 1096: 104-112.
16. Faul M, Xu L, Wald MM, Coronado VG. 2010. Traumatic brain injury in the United States: emergency department visits, hospitalizations and deaths. Centers for Disease Control and Prevention, National Center for Injury Prevention and Control, Atlanta, GA.
17. Foey AD, Field S, Ahmed S, Jain A, Feldmann M, Brennan FM, Williams R. 2003. Impact of VIP and cAMP on the regulation of TNF-α and IL-10 production: implications for rheumatoid arthritis. Arthritis Res Ther 5: R317-328.
18. Giorgi M, Modica A, Pompili A, Pacitti C, Gasbarri A. 2004. The induction of cyclic nucleotide phosphodiesterase 4 gene (PDE4D) impairs memory in a water maze task. Behav Brain Res 154: 99-106.
19. Goodman JC, Robertson CS, Grossman RG, Narayan RK. 1990. Elevation of tumor necrosis factor in head injury. J Neuroimmunol 30: 213-217.
20. Hatinen S, Sairanen M, Sirvio J, Jolkkonen J. 2008. Improved sensorimotor function by rolipram following focal cerebral ischemia in rats. Restor Neurol Neurosci 26: 493-499.
21. Hayward NM, Tuunanen PI, Immonen R, Ndode-Ekane XE, Pitkanen A, Grohn O. 2011. Magnetic resonance imaging of regional hemodynamic and cerebrovascular recovery after lateral fluid-percussion brain injury in rats. J Cereb Blood Flow Metab 31: 166-177.
22. Hosseini-Sharifabad A, Ghahremani MH, Sabzevari O, Naghdi N, Abdollahi M, Beyer C, Bollen E, Prickaerts J, Roghani A, Sharifzadeh M. 2012. Effects of protein kinase A and G inhibitors on hippocampal cholinergic markers expressions in rolipram- and sildenafil-induced spatial memory improvement. Pharmacol Biochem Behav 101: 311-319.
23. Houslay MD, Adams DR. 2003. PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem J 370: 1-18.
24. Hu W, Lu T, Chen A, Huang Y, Hansen R, Chandler LJ, Zhang HT. 2011. Inhibition of phosphodiesterase-4 decreases ethanol intake in mice. Psychopharmacology 218: 331-339.
25. Imanishi T, Sawa A, Ichimaru Y, Miyashiro M, Kato S, Yamamoto T, Ueki S. 1997. Ameliorating effects of rolipram on experimentally induced impairments of learning and memory in rodents. Eur J Pharmacol 321: 273-278.
26. Jacobitz S, McLaughlin MM, Livi GP, Burman M, Torphy TJ. 1996. Mapping the functional domains of human recombinant phosphodiesterase 4A: structural requirements for catalytic activity and rolipram binding. Mol Pharmacol 50: 891-899.
27. Jin SL, Lan L, Zoudilova M, Conti M. 2005. Specific role of phosphodiesterase 4B in lipopolysaccharide-induced signaling in mouse macrophages. J Immunol 175: 1523-1531.
28. Kato H, Araki T, Itoyama Y, Kogure K. 1995. Rolipram, a cyclic AMP-selective phosphodiesterase inhibitor, reduces neuronal damage following cerebral ischemia in the gerbil. Eur J Pharmacol 272: 107-110.
29. Keane RW, Kraydieh S, Lotocki G, Alonso OF, Aldana P, Dietrich WD. 2001. Apoptotic and antiapoptotic mechanisms after traumatic brain injury. J Cereb Blood Flow Metab 21: 1189-1198.
30. Kinoshita K, Chatzipanteli K, Vitarbo E, Truettner JS, Alonso OF, Dietrich WD. 2002. Interleukin-1β messenger ribonucleic acid and protein levels after fluid-percussion brain injury in rats: mportance of injury severity and brain temperature. Neurosurgery 51: 195-203.
31. Koopmans GC, Deumens R, Buss A, Geoghegan L, Myint AM, Honig WH, Kern N, Joosten EA, Noth J, Brook GA. 2009. Acute rolipram/thalidomide treatment improves tissue sparing and locomotion after experimental spinal cord injury. Exp Neurol 216: 490-498.
32. Lee HT, Chang YC, Wang LY, Wang ST, Huang CC, Ho CJ. 2004. cAMP response element-binding protein activation in ligation preconditioning in neonatal brain. Ann Neurol 56: 611-623.
33. Li LX, Cheng YF, Lin HB, Wang C, Xu JP, Zhang HT. 2011. Prevention of cerebral ischemia-induced memory deficits by inhibition of phosphodiesterase-4 in rats. Metab Brain Dis 26: 37-47.
34. Lin B, Ginsberg MD, Zhao W, Alonso OF, Belayev L, Busto R. 2001. Quantitative analysis of microvascular alterations in traumatic brain injury by endothelial barrier antigen immunohistochemistry. J Neurotrauma 18: 389-397.
35. Losco PE, Evans EW, Barat SA, Blackshear PE, Reyderman L, Fine JS, Bober LA, Anthes JC, Mirro EJ, Cuss FM. 2004. The toxicity of SCH 351591, a novel phosphodiesterase-4 inhibitor, in cynomolgus monkeys. Toxicol Pathol 32: 295-308.
36. Maeda T, Lee SM, Hovda DA. 2005. Restoration of cerebral vasoreactivity by an L-type calcium channel blocker following fluid percussion brain injury. J Neurotrauma 22: 763-771.
37. Mecklenburg L, Heuser A, Juengling T, Kohler M, Foell R, Ockert D, Tuch K, Bode G. 2006. Mesenteritis precedes vasculitis in the rat mesentery after subacute administration of a phosphodiesterase type 4 inhibitor. Toxicol Lett 163: 54-64.
38. Mehats C, Jin SL, Wahlstrom J, Law E, Umetsu DT, Conti M. 2003. PDE4D plays a critical role in the control of airway smooth muscle contraction. FASEB J 17: 1831-1841.
39. Merrill JE. 1991. Effects of interleukin-1 and tumor necrosis factor-α on astrocytes, microglia, oligodendrocytes, and glial precursors in vitro. Dev Neurosci 13: 130-137.
40. Miwa T, Mori A, Nakahara T, Ishii K. 2009. Intravenously administered phosphodiesterase 4 inhibitors dilate retinal blood vessels in rats. Eur J Pharmacol 602: 112-116.
41. Nagakura A, Niimura M, Takeo S. 2002. Effects of a phosphodiesterase IV inhibitor rolipram on microsphere embolism-induced defects in memory function and cerebral cyclic AMP signal transduction system in rats. Br J Pharmacol 135: 1783-1793.
42. Nikulina E, Tidwell JL, Dai HN, Bregman BS, Filbin MT. 2004. The phosphodiesterase inhibitor rolipram delivered after a spinal cord lesion promotes axonal regeneration and functional recovery. Proc Natl Acad Sci U S A 101: 8786-8790.
43. Park E, Bell JD, Siddiq IP, Baker AJ. 2009. An analysis of regional microvascular loss and recovery following two grades of fluid percussion trauma: a role for hypoxia-inducible factors in traumatic brain injury. J Cereb Blood Flow Metab 29: 575-584.
44. Pearse DD, Pereira FC, Marcillo AE, Bates ML, Berrocal YA, Filbin MT, Bunge MB. 2004. cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat Med 10: 610-616.
45. Prabhakar U, Lipshutz D, Bartus JO, Slivjak MJ, Smith EF3rd, Lee JC, Esser KM. 1994. Characterization of cAMP-dependent inhibition of LPS-induced TNFα production by rolipram, a specific phosphodiesterase IV (PDE IV) inhibitor. Int J Immunopharmacol 16: 805-816.
46. Reyes-Irisarri E, Sanchez AJ, Garcia-Merino JA, Mengod G. 2007. Selective induction of cAMP phosphodiesterase PDE4B2 expression in experimental autoimmune encephalomyelitis. J Neuropathol Exp Neurol 66: 923-931.
47. Ross SA, Halliday MI, Campbell GC, Byrnes DP, Rowlands BJ. 1994. The presence of tumour necrosis factor in CSF and plasma after severe head injury. Br J Neurosurg 8: 419-425.
48. Rutten K, Van Donkelaar EL, Ferrington L, Blokland A, Bollen E, Steinbusch HW, Kelly PA, Prickaerts JH. 2009. Phosphodiesterase inhibitors enhance object memory independent of cerebral blood flow and glucose utilization in rats. Neuropsychopharmacology 34: 1914-1925.
49. 14C]antipyrine. Am J Physiol 234: H59-H66.
50. Santos-Silva AJ, Cairrao E, Morgado M, Alvarez E, Verde I. 2008. PDE4 and PDE5 regulate cyclic nucleotides relaxing effects in human umbilical arteries. Eur J Pharmacol 582: 102-109.
51. Schneider HH, Schmiechen R, Brezinski M, Seidler J. 1986. Stereospecific binding of the antidepressant rolipram to brain protein structures. Eur J Pharmacol 127: 105-115.
52. Shohami E, Novikov M, Bass R, Yamin A, Gallily R. 1994. Closed head injury triggers early production of TNF α and IL-6 by brain tissue. J Cereb Blood Flow Metab 14: 615-619.
53. Si Q, Nakamura Y, Ogata T, Kataoka K, Schubert P. 1998. Differential regulation of microglial activation by propentofylline via cAMP signaling. Brain Res 812: 97-104.
54. Silvestre JS, Fernandez AG, Palacios JM. 1999. Effects of rolipram on the elevated plus-maze test in rats: a preliminary study. J Psychopharmacol 13: 274-277.
55. Souness JE, Rao S. 1997. Proposal for pharmacologically distinct conformers of PDE4 cyclic AMP phosphodiesterases. Cell Signal 9: 227-236.
56. Suzumura A, Ito A, Yoshikawa M, Sawada M. 1999. Ibudilast suppresses TNFα production by glial cells functioning mainly as type III phosphodiesterase inhibitor in the CNS. Brain Res 837: 203-212.
57. Taupin V, Toulmond S, Serrano A, Benavides J, Zavala F. 1993. Increase in IL-6, IL-1 and TNF levels in rat brain following traumatic lesion. Influence of pre- and post-traumatic treatment with Ro5 4864, a peripheral-type (p site) benzodiazepine ligand. J Neuroimmunol 42: 177-185.
58. Tilley DG, Maurice DH. 2002. Vascular smooth muscle cell phosphodiesterase (PDE) 3 and PDE4 activities and levels are regulated by cyclic AMP in vivo. Mol Pharmacol 62: 497-506.
59. Torphy TJ. 1998. Phosphodiesterase isozymes: molecular targets for novel antiasthma agents. Am J Respir Crit Care Med 157: 351-370.
60. Ueda Y, Suehiro E, Wei EP, Kontos HA, Povlishock JT. 2004. Uncomplicated rapid posthypothermic rewarming alters cerebrovascular responsiveness. Stroke 35: 601-606.
61. Verghese MW, McConnell RT, Strickland AB, Gooding RC, Stimpson SA, Yarnall DP, Taylor JD, Furdon PJ. 1995. Differential regulation of human monocyte-derived TNF α and IL-1 β by type IV cAMP-phosphodiesterase (cAMP-PDE) inhibitors. J Pharmacol Exp Ther 272: 1313-1320.
62. Vitarbo EA, Chatzipanteli K, Kinoshita K, Truettner JS, Alonso OF, Dietrich WD. 2004. Tumor necrosis factor α expression and protein levels after fluid percussion injury in rats: the effect of injury severity and brain temperature. Neurosurgery 55: 416-424.
63. Wei EP, Dietrich WD, Povlishock JT, Navari RM, Kontos HA. 1980. Functional, morphological, and metabolic abnormalities of the cerebral microcirculation after concussive brain injury in cats. Circ Res 46: 37-47.
64. Whitaker CM, Beaumont E, Wells MJ, Magnuson DS, Hetman M, Onifer SM. 2008. Rolipram attenuates acute oligodendrocyte death in the adult rat ventrolateral funiculus following contusive cervical spinal cord injury. Neurosci Lett 438: 200-204.
65. Willette RN, Shiloh AO, Sauermelch CF, Sulpizio A, Michell MP, Cieslinski LB, Torphy TJ, Ohlstein EH. 1997. Identification, characterization, and functional role of phosphodiesterase type IV in cerebral vessels: effects of selective phosphodiesterase inhibitors. J Cereb Blood Flow Metab 17: 210-219.
66. Yan HQ, Banos MA, Herregodts P, Hooghe R, Hooghe-Peters EL. 1992. Expression of interleukin (IL)-1 β, IL-6 and their respective receptors in the normal rat brain and after injury. Eur J Immunol 22: 2963-2971.
67. Yoshikawa M, Suzumura A, Tamaru T, Takayanagi T, Sawada M. 1999. Effects of phosphodiesterase inhibitors on cytokine production by microglia. Mult Scler 5: 126-133.
68. Zaloshnja E, Miller T, Langlois JA, Selassie AW. 2008. Prevalence of long-term disability from traumatic brain injury in the civilian population of the United States, 2005. J Head Trauma Rehabil 23: 394-400.
69. Zhang B, Yang L, Konishi Y, Maeda N, Sakanaka M, Tanaka J. 2002. Suppressive effects of phosphodiesterase type IV inhibitors on rat cultured microglial cells: comparison with other types of cAMP-elevating agents. Neuropharmacology 42: 262-269.
70. Zhang J, Snyder RD, Herman EH, Knapton A, Honchel R, Miller T, Espandiari P, Goodsaid FM, Rosenblum IY, Hanig JP, Sistare FD, Weaver JL. 2008. Histopathology of vascular injury in Sprague-Dawley rats treated with phosphodiesterase IV inhibitor SCH 351591 or SCH 534385. Toxicol Pathol 36: 827-839.
71. Zhang X, Chen Y, Jenkins LW, Kochanek PM, Clark RS. 2005. Bench-to-bedside review: Apoptosis/programmed cell death triggered by traumatic brain injury. Crit Care 9: 66-75.
72. 3H]rolipram. J Pharmacol Exp Ther 305: 565-572.
73. Zhu B, Kelly J, Vemavarapu L, Thompson WJ, Strada SJ. 2004. Activation and induction of cyclic AMP phosphodiesterase (PDE4) in rat pulmonary microvascular endothelial cells. Biochem Pharmacol 68: 479-491.
74. Zhu WH, Majluf-Cruz A, Omburo GA. 1998. Cyclic AMP-specific phosphodiesterase inhibitor rolipram and RO-20-1724 promoted apoptosis in HL60 promyelocytic leukemic cells via cyclic AMP-independent mechanism. Life Sci 63: 265-274.
75. Ziebell JM, Morganti-Kossmann MC. 2010. Involvement of pro- and anti-inflammatory cytokines and chemokines in the pathophysiology of traumatic brain injury. Neurotherapeutics 7: 22-30.