The galactosylation of Nω-nitro-L-arginine enhances its anti-nocifensive or anti-allodynic effects by targeting glia in healthy and neuropathic mice

European Journal of Pharmacology

Volumn 656, Issue 1-3, 2011, Pages 52-62

  Giordano, Catia ^a   Siniscalco, Dario ^a   Melisi, Daniela ^b   Luongo, Livio ^a   Curcio, Annalisa ^b   Soukupova, Marie ^c   Palazzo, Enza ^a   Marabese, Ida ^a   De Chiaro, Maria ^a   Rimoli, Maria Grazia ^b   Rossi, Francesco ^a   Maione, Sabatino ^a   De Novellis, Vito ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Inflammatory biomarker; N nitro L arginine; Neuropathic pain; Spinal cord; Writhing test

Indexed keywords

ALPHA INTEGRIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE TRANSPORTER 3; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA CONVERTING ENZYME; N(G) NITROARGININE; N(G) NITROARGININE METHYL ESTER;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; DRUG EFFICACY; DRUG PROTEIN BINDING; DRUG TARGETING; DRUG TRANSPORT; GLIA; GLIA CELL; MALE; MOUSE; NERVE CELL STIMULATION; NERVE INJURY; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINGLE DRUG DOSE; VISCERAL PAIN;

ANALGESICS; ANIMALS; ASTROCYTES; BLOOD PRESSURE; CASPASES; GALACTOSE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE TRANSPORTER TYPE 3; HYPERALGESIA; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; NEURALGIA; NEUROGLIA; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE TYPE II; NITROARGININE; PRODRUGS; PSYCHOMOTOR PERFORMANCE; RNA, MESSENGER; SCIATIC NERVE; TIME FACTORS;

EID: 79952282771     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2011.01.045     Document Type: Article

References (81)

1. N. Abacioglu, B. Tunctan, E. Akbulut, and I. Cakici Participation of the components of L-arginine/nitric oxide/cGMP cascade by chemically-induced abdominal constriction in the mouse Life Sci. 67 2000 1127 1137 (Pubitemid 30620748)
2. T. Andrianjafiniony, S. Dupré-Aucouturier, D. Letexier, H. Couchoux, and D. Desplanches Oxidative stress, apoptosis, and proteolysis in skeletal muscle repair after unloading Am. J. Physiol. Cell Physiol. 299 2010 C307 C315
3. J.A. Avontuur, S.L. Buijk, and H.A. Bruining Distribution and metabolism of N(G)-nitro-L-arginine methyl ester in patients with septic shock Eur. J. Clin. Pharmacol. 54 1998 627 631 (Pubitemid 28531424)
4. S.A. Baldwin Mammalian passive glucose transporters: members of an ubiquitous family of active and passive transport proteins Biochim. Biophys. Acta 1154 1993 17 49 (Pubitemid 23171388)
5. F. Bonina, C. Puglia, M.G. Rimoli, D. Melisi, G. Boatto, M. Nieddu, A. Calignano, G. La Rana, and P. De Caprariis Glycosyl derivatives of dopamine and L-dopa as anti-Parkinson prodrugs: synthesis, pharmacological activity and in vitro stability studies J. Drug Target. 11 2003 25 36 (Pubitemid 36527393)
6. M. Butler, C.S. Hayes, A. Chappell, S.F. Murray, T.L. Yaksh, and X.Y. Hua Spinal distribution and metabolism of 2′-O-(2-methoxyethyl)-modified oligonucleotides after intrathecal administration in rats Neuroscience 131 2005 705 715 (Pubitemid 40261225)
7. L.C. Chang, L.T. Tsao, C.S. Chang, C.J. Chen, L.J. Huang, S.C. Kuo, R.H. Lin, and J.P. Wang Inhibition of nitric oxide production by the carbazole compound LCY-2-CHO via blockade of activator protein-1 and CCAAT/enhancer- binding protein activation in microglia Biochem. Pharmacol. 76 2008 507 519
8. J.L. Chee, X.L. Guan, J.Y. Lee, B. Dong, S.M. Leong, E.H. Ong, A.K. Liou, and T.M. Lim Compensatory caspase activation in MPP+-induced cell death in dopaminergic neurons Cell. Mol. Life Sci. 62 2005 227 238 (Pubitemid 40193047)
9. S.R. Chen, Y.Q. Cai, and H.L. Pan Plasticity and emerging role of BKCa channels in nociceptive control in neuropathic pain J. Neurochem. 110 2009 352 362
10. Y. Choi, S.N. Raja, L.C. Moore, and J.R. Tobin Neuropathic pain in rats is associated with altered nitric oxide synthase activity in neural tissue J. Neurol. Sci. 138 1996 14 20 (Pubitemid 26194271)
11. Y.C. Chu, Y. Guan, J. Skinner, S.N. Raja, R.A. Johns, and Y.X. Tao Effect of genetic knockout or pharmacologic inhibition of neuronal nitric oxide synthase on complete Freund's adjuvant induced persistent pain Pain 119 2005 113 123 (Pubitemid 41752971)
12. P. Cidad, P. Garcia-Nogales, A. Almeida, and J.P. Bolaños Expression of glucose transporter GLUT3 by endotoxin in cultured rat astrocytes: the role of nitric oxide J. Neurochem. 79 2001 17 24 (Pubitemid 32946638)
13. D. Cizkova, N. Lukacova, M. Marsala, and J. Marsala Neuropathic pain is associated with alterations of nitric oxide synthase immunoreactivity and catalytic activity in dorsal root ganglia and spinal dorsal horn Brain Res. Bull. 58 2002 161 171 (Pubitemid 34753086)
14. A.K. Clark, P.K. Yip, J. Grist, C. Gentry, A.A. Staniland, F. Marchand, M. Dehvari, G. Wotherspoon, J. Winter, J. Ullah, S. Bevan, and M. Malcangio Inhibition of spinal microglial cathepsin S for the reversal of neuropathic pain Proc. Natl Acad. Sci. USA 104 2007 10655 10660 (Pubitemid 47185720)
15. D.E. Coyle Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior Glia 23 1998 75 83 (Pubitemid 28174047)
16. V. de Novellis, D. Siniscalco, U. Galderisi, C. Fuccio, M. Nolano, L. Santoro, A. Cascino, K.A. Roth, F. Rossi, and S. Maione Blockade of glutamate mGlu5 receptors in a rat model of neuropathic pain prevents early over-expression of pro-apoptotic genes and morphological changes in dorsal horn lamina II Neuropharmacology 46 2004 468 479 (Pubitemid 38224432)
17. I. Decostered, and C.J. Woolf Spared nerve injury: an animal model of persistent peripheral neuropathic pain Pain 87 2000 149 158 (Pubitemid 30621447)
18. H. Dickel, T. Gambichler, J. Kamphowe, P. Altmeyer, and M. Skrygan Standardized tape stripping prior to patch testing induces upregulation of Hsp90, Hsp70, IL-33, TNF-α and IL-8/CXCL8 mRNA: new insights into the involvement of 'alarmins' Contact Dermat. 63 2010 215 222
19. I.D. Duarte, and S.H. Ferreira L-NAME causes antinociception by stimulation of the arginine-NO-cGMP pathway Mediators Inflamm. 9 2000 25 30 (Pubitemid 30399114)
20. S. Echeverry, X.Q. Shi, and J. Zhang Characterization of cell proliferation in rat spinal cord following peripheral nerve injury and the relationship with neuropathic pain Pain 135 2008 37 47 (Pubitemid 351193080)
21. H.Y. Fang, C.Y. Lin, K.C. Chow, H.C. Huang, and W.J. Ko Microarray detection of gene overexpression in primary spontaneous pneumothorax Exp. Lung Res. 36 2010 323 330
22. R.D. Fields, and B. Stevens-Graham New insights into neuron-glia communication Science 298 2002 556 562
23. H.S. Fischer, G. Zernig, K.F. Hauser, C. Gerard, L.B. Hersh, and A. Saria Neutral endopeptidase knockout induces hyperalgesia in a model of visceral pain, an effect related to bradykinin and nitric oxide J. Mol. Neurosci. 18 2002 129 134 (Pubitemid 34252631)
24. K.Y. Fu, A.R. Light, G.K. Matsushima, and W. Maixner Microglial reactions after subcutaneous formalin injection into the rat hind paw Brain Res. 825 1999 59 67 (Pubitemid 29222862)
25. C. Fuccio, C. Luongo, P. Capodanno, C. Giordano, M.A. Scafuro, D. Siniscalco, B. Lettieri, F. Rossi, S. Maione, and L. Berrino A single subcutaneous injection of ozone prevents allodynia and decreases the over-expression of pro-inflammatory caspases in the orbito-frontal cortex of neuropathic mice Eur. J. Pharmacol. 603 2009 42 49
26. U. Galderisi, G. Di Bernardo, M. Cipollaro, G. Peluso, A. Cascino, R. Cotrufo, and M.A. Melone Differentiation and apoptosis of neuroblastoma cells: role of N-myc gene product J. Cell. Biochem. 73 1999 97 105 (Pubitemid 29115483)
27. Y. Guan, M. Yaster, S.N. Raja, and Y.X. Tao Genetic knockout and pharmacologic inhibition of neuronal nitric oxide synthase attenuate nerve injury-induced mechanical hypersensitivity in mice Mol. Pain 3 2007 29 38
28. J.X. Hao, and X.J. Xu Treatment of a chronic allodynia-like response in spinally injured rats: effects of systemically administered nitric oxide synthase inhibitors Pain 66 1996 313 319
29. V. Hornung, A. Ablasser, M. Charrel-Dennis, F. Bauernfeind, G. Horvath, D.R. Caffrey, E. Latz, and K.A. Fitzgerald AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC Nature 458 2009 514 518
30. H.B. Jia, Y. Jin, Q. Ji, Y.F. Hu, Z.Q. Zhou, J.G. Xu, and J.J. Yang Effects of recombinant human erythropoietin on neuropathic pain and cerebral expressions of cytokines and nuclear factor-kappa B Can. J. Anaesth. 56 2009 597 603
31. E.K. Joseph, and J.D. Levine Caspase signalling in neuropathic and inflammatory pain in the rat Eur. J. Neurosci. 20 2004 2896 2902 (Pubitemid 40007283)
32. Z. Khalil, and B. Khodr A role for free radicals and nitric oxide in delayed recovery in aged rats with chronic constriction nerve injury Free Radic. Biol. Med. 31 2001 430 439 (Pubitemid 32728430)
33. T. Kishi, Y. Hirooka, Y. Mukai, H. Shimokawa, and A. Takeshita Atorvastatin causes depressor and sympatho-inhibitory effects with upregulation of nitric oxide synthases in stroke-prone spontaneously hypertensive rats J. Hypertens. 21 2003 379 386 (Pubitemid 36269710)
34. R.G. Knowles, M. Palacios, R.M. Palmer, and S. Moncada Formation of nitric oxide from L-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase Proc. Natl Acad. Sci. USA 86 1989 5159 5162 (Pubitemid 19182253)
35. K. Kobayashi, N. Inohara, L.D. Hernandez, J.E. Galan, G. Nunez, C.A. Janeway, R. Medzhitov, and R.A. Flavell RICK/Rip2/CARDIAK mediates signalling for receptors of the innate and adaptive immune systems Nature 416 2002 194 199 (Pubitemid 34246479)
36. Y. Kosuge, K. Sekikawa-Nishida, H. Negi, K. Ishige, and Y. Ito Characterization of chronic glutamate-mediated motor neuron toxicity in organotypic spinal cord culture prepared from ALS model mice Neurosci. Lett. 454 2009 165 169
37. M. Lamkanfi, M. Kalai, X. Saelens, W. Declercq, and P. Vandenabeele Caspase-1 activates nuclear factor of the kappa-enhancer in B cells independently of its enzymatic activity J. Biol. Chem. 279 2004 24785 24793 (Pubitemid 38725346)
38. D. Le Bars, M. Gozariu, and S.W. Cadden Animal models of nociception Pharmacol. Rev. 53 2001 597 652 (Pubitemid 33136239)
39. A. Ledeboer, E.M. Sloane, E.D. Milligan, M.G. Frank, J.H. Mahony, S.F. Maier, and L.R. Watkins Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation Pain 115 2005 71 83
40. D.H. Lee, J.P. Singh, and D. Lodge Experiments with nitric oxide synthase inhibitors in spinal nerve ligated rats provide no evidence of a role for nitric oxide in neuropathic mechanical allodynia Neurosci. Lett. 385 2005 179 183 (Pubitemid 40980396)
41. P. Li, H. Allen, S. Banerjee, S. Franklin, L. Herzog, C. Johnston, J. McDowell, M. Paskind, L. Rodman, J. Salfeld, E. Towne, D. Tracey, S. Wardwell, F.Y. Wei, W. Wong, R. Kamen, and S. Tara Mice deficient in IL-1β-converting enzyme are defective in production of mature IL-1β and resistant to endotoxic shock Cell 80 1995 401 411
42. S. Lisi, M. Sisto, D. Lofrumento, M.A. Frassanito, S. Caprio, M.L. Romano, V. Mitolo, and M. D'Amore Regulation of mRNA caspase-8 levels by anti-nuclear autoantibodies Clin. Exp. Med. 10 2010 199 203
43. H.J. Liu, J.P. Yang, C.H. Wang, R.C. Liu, Y. Li, and C.Y. Li Endoplasmic reticulum in the penumbra following middle cerebral artery occlusion in the rabbit Neurol. Sci. 30 2009 227 232
44. L. Luongo, M. Sajic, J. Grist, A.K. Clark, S. Maione, and M. Malcangio Spinal changes associated with mechanical hypersensitivity in a model of Guillain-Barré syndrome Neurosci. Lett. 437 2008 98 102
45. W. Ma, and J.C. Eisenach Neuronal nitric oxide synthase is upregulated in a subset of primary sensory afferents after nerve injury which are necessary for analgesia from alpha2-adrenoceptor stimulation Brain Res. 1127 2007 52 58 (Pubitemid 44854846)
46. S. Maione, D. Siniscalco, U. Galderisi, V. de Novellis, R. Uliano, G. Di Bernardo, L. Berrino, A. Cascino, and F. Rossi Apoptotic genes expression in the lumbar dorsal horn in a model neuropathic pain in rat NeuroReport 13 2002 101 106 (Pubitemid 34102035)
47. C. Martucci, A.E. Trovato, B. Costa, E. Borsani, S. Franchi, V. Magnaghi, A.E. Panerai, L.F. Rodella, A.E. Valsecchi, P. Sacerdote, and M. Colleoni The purinergic antagonist PPADS reduces pain related behaviours and interleukin-1beta, interleukin-6, iNOS and nNOS overproduction in central and peripheral nervous system after peripheral neuropathy in mice Pain 137 2008 81 95 (Pubitemid 351794401)
48. D. Melisi, A. Secondo, P. Montoro, S. Piacente, M.G. Rimoli, M. Minale, P. de Caprariis, and L. Annunziato Galactosyl derivatives of L-arginine and d-arginine: synthesis, stability, cell permeation, and nitric oxide production in pituitary GH3 cells J. Med. Chem. 49 2006 4826 4833 (Pubitemid 44201041)
49. ω-nitro-L-arginine: study of antiproliferative activity on human thyroid follicular carcinoma cells J. Cell. Physiol. 221 2009 440 447
50. S.T. Meller, and G.F. Gebhart Nitric oxide (NO) and nociceptive processing in the spinal cord Pain 52 1993 127 136 (Pubitemid 23068181)
51. S.T. Meller, P.S. Pechman, G.F. Gebhart, and T.J. Maves Nitric oxide mediates the thermal hyperalgesia produced in a model of neuropathic pain in the rat Neuroscience 50 1992 7 10
52. M.J. Millan Serotonin and pain-evidence that activation of 5-Ht1A receptors does not elicit antinociception against noxious thermal, mechanical and chemical stimuli in mice Pain 58 1994 45 61
53. E.D. Milligan, and L.R. Watkins Pathological and protective roles of glia in chronic pain Nat. Rev. Neurosci. 10 2009 23 36
54. A. Moss, S. Beggs, D. Vega-Avelaira, M. Costigan, G.J. Hathway, M.W. Salter, and M. Fitzgerald Spinal microglia and neuropathic pain in young rats Pain 128 2007 215 224 (Pubitemid 46367416)
55. V. Neugebauer, V. Galhardo, S. Maione, and S.C. Mackey Forebrain pain mechanisms Brain Res. Rev. 60 2009 226 242
56. E.A. Newman New roles for astrocytes: regulation of synaptic transmission Trends Neurosci. 26 2003 536 542 (Pubitemid 37176908)
57. E. Niederberger, and G. Geisslinger The IKK-NF-kappaB pathway: a source for novel molecular drug targets in pain therapy? FASEB J. 22 2008 3432 3442
58. N. Osada, Y. Kosuge, T. Kihara, K. Ishige, and Y. Ito Apolipoprotein E-deficient mice are more vulnerable to ER stress after transient forebrain ischemia Neurochem. Int. 54 2009 403 409
59. H. Prast, and A. Philippu Nitric oxide as modulator of neuronal function Prog. Neurobiol. 64 2001 51 68 (Pubitemid 32201889)
60. Y. Qian, D.S. Chao, D.R. Santillano, T.L. Cornwell, A.C. Nairn, P. Greengard, T.M. Lincoln, and D.S. Bredt cGMP-dependent protein kinase in dorsal root ganglion: relationship with nitric oxide synthase and nociceptive neurons J. Neurosci. 16 1996 3130 3138 (Pubitemid 26142349)
61. I. Racz, X. Nadal, J. Alferink, J.E. Baños, J. Rehnelt, M. Martín, B. Pintado, A. Gutierrez-Adan, E. Sanguino, N. Bellora, J. Manzanares, A. Zimmer, and R. Maldonado Interferon-gamma is a critical modulator of CB(2) cannabinoid receptor signaling during neuropathic pain J. Neurosci. 28 2008 12136 12145
62. K. Ren, and R. Dubner Neuron-glia crosstalk gets serious: role in pain hypersensitivity Curr. Opin. Anaesthesiol. 21 2008 570 579
63. E.A. Romero-Sandoval, R.J. Horvath, and J.A. DeLeo Neuroimmune interactions and pain: focus on glial-modulating targets Curr. Opin. Investig. Drugs 9 2008 726 734 (Pubitemid 351950869)
64. K. Satake, Y. Matsuyama, M. Kamiya, H. Kawakami, H. Iwata, K. Adachi, and K. Kiuchi Nitric oxide via macrophage iNOS induces apoptosis following traumatic spinal cord injury Mol. Brain Res. 85 2000 114 122 (Pubitemid 32056242)
65. J. Scholz, and C.J. Woolf The neuropathic pain triad: neurons, immune cells and glia Nat. Neurosci. 10 2007 1361 1368 (Pubitemid 350014681)
66. D. Siniscalco, V. de Novellis, F. Rossi, and S. Maione Neuropathic pain: is the end of suffering starting in the gene therapy? Curr. Drug Targets 6 2005 75 80 (Pubitemid 40394325)
67. D. Siniscalco, C. Fuccio, C. Giordano, F. Ferraraccio, E. Palazzo, L. Luongo, F. Rossi, K.A. Roth, S. Maione, and V. de Novellis Role of reactive oxygen species and spinal cord apoptotic genes in the development of neuropathic pain Pharmacol. Res. 55 2007 158 166 (Pubitemid 46186043)
68. D. Siniscalco, C. Giordano, C. Fuccio, L. Luongo, F. Ferraraccio, F. Rossi, V. de Novellis, K.A. Roth, and S. Maione Involvement of subtype 1 metabotropic glutamate receptors in apoptosis and caspase-7 over-expression in spinal cord of neuropathic rats Pharmacol. Res. 57 2008 223 233
69. S.H. Snyder Nitric oxide: first in a new class of neurotransmitters Science 257 1992 494 496
70. Y.J. Sung, D.T. Chiu, and R.T. Ambron Activation and retrograde transport of protein kinase G in rat nociceptive neurons after nerve injury and inflammation Neuroscience 141 2006 697 709 (Pubitemid 44066655)
71. A. Tabernero, J.M. Medina, and C. Giaume Glucose metabolism and proliferation in glia: role of astrocytic gap junctions J. Neurochem. 99 2006 1049 1061 (Pubitemid 44655272)
72. R.J. Tallarida Dose-response analysis R.J. Tallarida, Drug Synergism and Dose-Effect Data Analysis 2000 Chapman & Hall/CRC Florida 21 39
73. Q. Tang, C.I. Svensson, B. Fitzsimmons, M. Webb, T.L. Yaksh, and X.Y. Hua Inhibition of spinal constitutive NOS-2 by 1400 W attenuates tissue injury and inflammation-induced hyperalgesia and spinal p38 activation Eur. J. Neurosci. 25 2007 I2964 I2972
74. Z.E. Tóth, and E. Mezey Simultaneous visualization of multiple antigens with tyramide signal amplification using antibodies from the same species J. Histochem. Cytochem. 55 2007 545 554 (Pubitemid 46791937)
75. S. Wan, P. Shi, X. Zhang, C. Gu, and S. Fan Stronger expression of CHOP and caspase 12 in diabetic spinal cord injury rats Neurol. Res. 31 2009 1049 1055
76. L.R. Watkins, M.R. Hutchinson, E.D. Milligan, and S.F. Maier "Listening" and "talking" to neurons: implications of immune activation for pain control and increasing the efficacy of opioids Brain Res. Rev. 56 2007 148 169 (Pubitemid 350100866)
77. F. Wei, W. Guo, S. Zou, K. Ren, and R. Dubner Supraspinal glial-neuronal interactions contribute to descending pain facilitation J. Neurosci. 28 2008 10482 10495
78. J. Wu, Q. Lin, Y. Lu, W.D. Willis, and K.N. Westlund Changes in nitric oxide synthase isoforms in the spinal cord of rat following induction of chronic arthritis Exp. Brain Res. 118 1998 457 465 (Pubitemid 28056846)
79. T. Yamamoto, and N. Shimoyama Role of nitric oxide in the development of thermal hyperesthesia induced by sciatic nerve constriction injury in the rat Anesthesiology 82 1995 1266 1273
80. H.Y. Yang, H.K. Chang, J.W. Lee, Y.S. Kim, H. Kim, M.H. Lee, M.S. Shin, D.H. Ham, H.K. Park, H. Lee, and C.J. Kim Amygdalin suppresses lipopolysaccharide-induced expressions of cyclooxygenase-2 and inducible nitric oxide synthase in mouse BV2 microglial cells Neurol. Res. 29 Suppl. 1 2007 S59 S64
81. Y.W. Yoon, B. Sung, and J.M. Chung Nitric oxide mediates behavioural signs of neuropathic pain in an experimental rat model NeuroReport 9 1998 367 372 (Pubitemid 28109189)