The use of the antimicrobial peptide piscidin (PCD)-1 as a novel anti-nociceptive agent

Biomaterials

Volumn 53, Issue , 2015, Pages 1-11

  Chen, Wu Fu ^a   Huang, Shi Ying ^b   Liao, Chang Yi ^b   Sung, Chun Sung ^c,d   Chen, Jyh Yih ^e   Wen, Zhi Hong ^b  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

^c TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^d NATIONAL YANG MING UNIVERSITY   (Taiwan)

^e INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

Author keywords

Allodynia; Antimicrobial peptide; Chronic constriction injury; Hyperalgesia; Neuropathic pain; Piscidin 1

Indexed keywords

ANTIBIOTICS; CELL CULTURE; HEALTH; MICROORGANISMS; PEPTIDES; RATS;

ALLODYNIA; ANTIMICROBIAL PEPTIDE; CHRONIC CONSTRICTION INJURY; HYPERALGESIA; NEUROPATHIC PAIN; PISCIDIN;

ANTIMICROBIAL AGENTS;

ANTINOCICEPTIVE AGENT; CYCLOOXYGENASE 2; GABAPENTIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MAMMALIAN TARGET OF RAPAMYCIN; PISCIDIN 1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; ANALGESIC AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; FISH PROTEIN; MORONECIDIN PROTEIN, MORONE SAXATILIS; TARGET OF RAPAMYCIN KINASE;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ANTINOCICEPTION; ARTICLE; ASTROCYTE; BEHAVIOR CHANGE; CELL ACTIVATION; CHRONIC CONSTRICTION INJURY; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG USE; HYPERALGESIA; IN VIVO STUDY; LUMBAR SPINAL CORD; MICROGLIA; MONONEUROPATHY; MOUSE; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN; UPREGULATION; WEIGHT BEARING; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CHEMISTRY; DRUG EFFECTS; MALE; METABOLISM; MOLECULAR GENETICS; WISTAR RAT;

MAMMALIA; MURINAE; RATTUS;

AMINO ACID SEQUENCE; ANALGESICS; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; ASTROCYTES; CELL LINE; CYCLOOXYGENASE 2; FISH PROTEINS; INTERLEUKIN-1BETA; MALE; MICE; MICROGLIA; MOLECULAR SEQUENCE DATA; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, WISTAR; TOR SERINE-THREONINE KINASES; TRANSFORMING GROWTH FACTOR BETA1; UP-REGULATION;

EID: 84926311799     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.02.069     Document Type: Article

References (79)

1. Lauth X., Shike H., Burns J.C., Westerman M.E., Ostland V.E., Carlberg J.M., et al. Discovery and characterization of two isoforms of moronecidin, a novel antimicrobial peptide from hybrid striped bass. JBiol Chem 2002, 277:5030-5039.
2. Rajanbabu V., Chen J.Y. The antimicrobial peptide, tilapia hepcidin 2-3, and PMA differentially regulate the protein kinase C isoforms, TNF-alpha and COX-2, in mouse RAW264.7 macrophages. Peptides 2011, 32:333-341.
3. Jackway R.J., Maselli V.M., Musgrave I.F., Maclean M.J., Tyler M.J., Bowie J.H. Skin peptides from anurans of the Litoria rubella Group: sequence determination using electrospray mass spectrometry. Opioid activity of two major peptides. Rapid Commun Mass Spectrom 2009, 23:1189-1195.
4. Bilusich D., Jackway R.J., Musgrave I.F., Tyler M.J., Bowie J.H. The host-defence skin peptide profiles of Peron's Tree Frog Litoria peronii in winter and summer. Sequence determination by electrospray mass spectrometry and activities of the peptides. Rapid Commun Mass Spectrom 2009, 23:2628-2636.
5. Pukala T.L., Urathamakul T., Watt S.J., Beck J.L., Jackway R.J., Bowie J.H. Binding studies of nNOS-active amphibian peptides and Ca2+ calmodulin, using negative ion electrospray ionisation mass spectrometry. Rapid Commun Mass Spectrom 2008, 22:3501-3509.
6. Pukala T.L., Doyle J.R., Llewellyn L.E., Kuhn-Nentwig L., Apponyi M.A., Separovic F., et al. Cupiennin 1a, an antimicrobial peptide from the venom of the neotropical wandering spider Cupiennius salei, also inhibits the formation of nitric oxide by neuronal nitric oxide synthase. FEBS J 2007, 274:1778-1784.
7. Erdal E.P., Litzinger E.A., Seo J., Zhu Y., Ji H., Silverman R.B. Selective neuronal nitric oxide synthase inhibitors. Curr Top Med Chem 2005, 5:603-624.
8. Doyle J., Brinkworth C.S., Wegener K.L., Carver J.A., Llewellyn L.E., Olver I.N., et al. nNOS inhibition, antimicrobial and anticancer activity of the amphibian skin peptide, citropin 1.1 and synthetic modifications. The solution structure of a modified citropin 1.1. Eur J Biochem 2003, 270:1141-1153.
9. Campagna S., Saint N., Molle G., Aumelas A. Structure and mechanism of action of the antimicrobial peptide piscidin. Biochemistry 2007, 46:1771-1778.
10. Lee S.A., Kim Y.K., Lim S.S., Zhu W.L., Ko H., Shin S.Y., et al. Solution structure and cell selectivity of piscidin 1 and its analogues. Biochemistry 2007, 46:3653-3663.
11. Perrin B.S., Tian Y., Fu R., Grant C.V., Chekmenev E.Y., Wieczorek W.E., et al. High-resolution structures and orientations of antimicrobial peptides piscidin 1 and piscidin 3 in fluid bilayers reveal tilting, kinking, and bilayer immersion. JAm Chem Soc 2014, 136:3491-3504.
12. Lin H.J., Huang T.C., Muthusamy S., Lee J.F., Duann Y.F., Lin C.H. Piscidin-1, an antimicrobial peptide from fish (hybrid striped bass morone saxatilis x M. chrysops), induces apoptotic and necrotic activity in HT1080 cells. Zool Sci 2012, 29:327-332.
13. Colorni A., Ullal A., Heinisch G., Noga E.J. Activity of the antimicrobial polypeptide piscidin 2 against fish ectoparasites. JFish Dis 2008, 31:423-432.
14. Sung W.S., Lee J., Lee D.G. Fungicidal effect and the mode of action of piscidin 2 derived from hybrid striped bass. Biochem Biophys Res Commun 2008, 371:551-555.
15. Sprintz M., Tasciotti E., Allegri M., Grattoni A., Driver L.C., Ferrari M. Nanomedicine: ushering in a new era of pain management. Eur J Pain Suppl 2011, 5:317-322.
16. Melnikova I. Pain market. Nat Rev Drug Discov 2010, 9:589-590.
17. Breivik H., Collett B., Ventafridda V., Cohen R., Gallacher D. Survey of chronic pain in Europe: prevalence, impact on daily life, and treatment. Eur J Pain 2006, 10:287-333.
18. Bouhassira D., Lantéri-Minet M., Attal N., Laurent B., Touboul C. Prevalence of chronic pain with neuropathic characteristics in the general population. Pain 2008, 136:380-387.
19. Veneroni O., Maj R., Calabresi M., Faravelli L., Fariello R.G., Salvati P. Anti-allodynic effect of NW-1029, a novel Na(+) channel blocker, in experimental animal models of inflammatory and neuropathic pain. Pain 2003, 102:17-25.
20. Baron R. Neuropathic pain: a clinical perspective. Handb Exp Pharmacol 2009, 3-30.
21. Arner S., Meyerson B.A. Lack of analgesic effect of opioids on neuropathic and idiopathic forms of pain. Pain 1988, 33:11-23.
22. Kalso E., Vainio A. Morphine and oxycodone hydrochloride in the management of cancer pain. Clin Pharmacol Ther 1990, 47:639-646.
23. Clark C.M., Lee D.A. Prevention and treatment of the complications of diabetes mellitus. NEngl J Med 1995, 332:1210-1217.
24. Ossipov M.H., Porreca F. Challenges in the development of novel treatment strategies for neuropathic pain. NeuroRx 2005, 2:650-661.
25. Finnerup N.B., Sindrup S.H., Jensen T.S. The evidence for pharmacological treatment of neuropathic pain. Pain 2010, 150:573-581.
26. Quintans J.S., Antoniolli A.R., Almeida J.R., Santana-Filho V.J., Quintans-Junior L.J. Natural Products Evaluated in neuropathic pain models - a systematic review. Basic Clin Pharmacol Toxicol 2014, 114:442-450.
27. Backonja M., Glanzman R.L. Gabapentin dosing for neuropathic pain: evidence from randomized, placebo-controlled clinical trials. Clin Ther 2003, 25:81-104.
28. Moore R.A., Wiffen P.J., Derry S., McQuay H.J. Gabapentin for chronic neuropathic pain and fibromyalgia in adults. Cochrane Database Syst Rev 2011, CD007938. http://www.ncbi.nlm.nih.gov/pubmed/21412914.
29. Jean Y.H., Chen W.F., Sung C.S., Duh C.Y., Huang S.Y., Lin C.S., et al. Capnellene, a natural marine compound derived from soft coral, attenuates chronic constriction injury-induced neuropathic pain in rats. Br J Pharmacol 2009, 158:713-725.
30. Chen N.F., Huang S.Y., Lu C.H., Chen C.L., Feng C.W., Chen C.H., et al. Flexibilide obtained from cultured soft coral has anti-neuroinflammatory and analgesic effects through the upregulation of spinal transforming growth factor-beta1 in neuropathic rats. Mar Drugs 2014, 12:3792-3817.
31. Coronel M.F., Labombarda F., De Nicola A.F., Gonzalez S.L. Progesterone reduces the expression of spinal cyclooxygenase-2 and inducible nitric oxide synthase and prevents allodynia in a rat model of central neuropathic pain. Eur J Pain March 2014, 18(3):348-359.
32. Wen Z.H., Chao C.H., Wu M.H., Sheu J.H. Aneuroprotective sulfone of marine origin and the invivo anti-inflammatory activity of an analogue. Eur J Med Chem 2010, 45:5998-6004.
33. Jean Y.H., Chen W.F., Duh C.Y., Huang S.Y., Hsu C.H., Lin C.S., et al. Inducible nitric oxide synthase and cyclooxygenase-2 participate in anti-inflammatory and analgesic effects of the natural marine compound lemnalol from Formosan soft coral Lemnalia cervicorni. Eur J Pharmacol 2008, 578:323-331.
34. Milligan E.D., Watkins L.R. Pathological and protective roles of glia in chronic pain. Nat Rev Neurosci 2009, 10:23-36.
35. Marchand F., Perretti M., McMahon S.B. Role of the immune system in chronic pain. Nat Rev Neurosci 2005, 6:521-532.
36. Sweitzer S.M., Schubert P., DeLeo J.A. Propentofylline, a glial modulating agent, exhibits antiallodynic properties in a rat model of neuropathic pain. JPharmacol Exp Ther 2001, 297:1210-1217.
37. Ledeboer A., Sloane E.M., Milligan E.D., Frank M.G., Mahony J.H., Maier S.F., et al. Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation. Pain 2005, 115:71-83.
38. Lin Y.C., Huang S.Y., Jean Y.H., Chen W.F., Sung C.S., Kao E.S., et al. Intrathecal lemnalol, a natural marine compound obtained from Formosan soft coral, attenuates nociceptive responses and the activity of spinal glial cells in neuropathic rats. Behav Pharmacol 2011, 22:739-750.
39. Geranton S.M., Jimenez-Diaz L., Torsney C., Tochiki K.K., Stuart S.A., Leith J.L., et al. Arapamycin-sensitive signaling pathway is essential for the full expression of persistent pain states. JNeurosci 2009, 29:15017-15027.
40. Asante C.O., Wallace V.C., Dickenson A.H. Mammalian target of rapamycin signaling in the spinal cord is required for neuronal plasticity and behavioral hypersensitivity associated with neuropathy in the rat. JPain 2010, 11:1356-1367.
41. Chen N.F., Huang S.Y., Chen W.F., Chen C.H., Lu C.H., Chen C.L., et al. TGF-beta1 attenuates spinal neuroinflammation and the excitatory amino acid system in rats with neuropathic pain. JPain 2013, 14:1671-1685.
42. Zhang W., Sun X.F., Bo J.H., Zhang J., Liu X.J., Wu L.P., et al. Activation of mTOR in the spinal cord is required for pain hypersensitivity induced by chronic constriction injury in mice. Pharmacol Biochem Behav 2013, 111:64-70.
43. Wang L.X., Wang Z.J. Animal and cellular models of chronic pain. Adv Drug Deliv Rev 2003, 55:949-965.
44. Huang S.Y., Chen N.F., Chen W.F., Hung H.C., Lee H.P., Lin Y.Y., et al. Sinularin from indigenous soft coral attenuates nociceptive responses and spinal neuroinflammation in carrageenan-induced inflammatory rat model. Mar Drugs 2012, 10:1899-1919.
45. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. JBiol Chem 1951, 193:265-275.
46. Yaksh T.L., Rudy T.A. Chronic catheterization of the spinal subarachnoid space. Physiol Behav 1976, 17:1031-1036.
47. Bennett G.J., Xie Y.K. Aperipheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988, 33:87-107.
48. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. Anew and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
49. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. JNeurosci Methods 1994, 53:55-63.
50. Bardin L., Malfetes N., Newman-Tancredi A., Depoortere R. Chronic restraint stress induces mechanical and cold allodynia, and enhances inflammatory pain in rat: relevance to human stress-associated painful pathologies. Behav Brain Res 2009, 205:360-366.
51. Flatters S.J., Bennett G.J. Ethosuximide reverses paclitaxel- and vincristine-induced painful peripheral neuropathy. Pain 2004, 109:150-161.
52. Wen Z.H., Tang C.C., Chang Y.C., Huang S.Y., Hsieh S.P., Lee C.H., et al. Glucosamine sulfate reduces experimental osteoarthritis and nociception in rats: association with changes of mitogen-activated protein kinase in chondrocytes. Osteoarthr Cartil 2010, 18:1192-1202.
53. Urakawa S., Hida H., Masuda T., Misumi S., Kim T.S., Nishino H. Environmental enrichment brings a beneficial effect on beam walking and enhances the migration of doublecortin-positive cells following striatal lesions in rats. Neuroscience 2007, 144:920-933.
54. Sung B., Lim G., Mao J. Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats. JNeurosci 2003, 23:2899-2910.
55. Wang P.L., Lib D.Y., Xie L.R., Wu X., Hua H.M., Li Z.L. Novel decaturin alkaloids from the marine-derived fungus Penicillium oxalicum. Nat Prod Commun 2013, 8:1397-1398.
56. Sung W.S., Lee J., Lee D.G. Fungicidal effect of piscidin on Candida albicans: pore formation in lipid vesicles and activity in fungal membranes. Biol Pharm Bull 2008, 31:1906-1910.
57. Wahba M., Waln O. Asterixis related to gabapentin intake: a case report and review. Postgrad Med 2013, 125:139-141.
58. Sung C.S., Cherng C.H., Wen Z.H., Chang W.K., Huang S.Y., Lin S.L., et al. Minocycline and fluorocitrate suppress spinal nociceptive signaling in intrathecal IL-1beta-induced thermal hyperalgesic rats. Glia 2012, 60:2004-2017.
59. Lee E., Shin A., Jeong K.W., Jin B., Jnawali H.N., Shin S., et al. Role of phenylalanine and valine10 residues in the antimicrobial activity and cytotoxicity of piscidin-1. PLoS One 2014, 9:e114453.
60. Beck K.F., Eberhardt W., Frank S., Huwiler A., Messmer U.K., Muhl H., et al. Inducible NO synthase: role in cellular signalling. JExp Biol 1999, 202:645-653.
61. Li X., Kang L., Li G., Zeng H., Zhang L., Ling X., et al. Intrathecal leptin inhibits expression of the P2X2/3 receptors and alleviates neuropathic pain induced by chronic constriction sciatic nerve injury. Mol Pain 2013, 9:65.
62. Myers R.R., Campana W.M., Shubayev V.I. The role of neuroinflammation in neuropathic pain: mechanisms and therapeutic targets. Drug Discov Today 2006, 11:8-20.
63. Streit W.J., Mrak R.E., Griffin W.S. Microglia and neuroinflammation: a pathological perspective. JNeuroinflammation 2004, 1:14.
64. Garrison C.J., Dougherty P.M., Kajander K.C., Carlton S.M. Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury. Brain Res 1991, 565:1-7.
65. Colburn R.W., DeLeo J.A., Rickman A.J., Yeager M.P., Kwon P., Hickey W.F. Dissociation of microglial activation and neuropathic pain behaviors following peripheral nerve injury in the rat. JNeuroimmunol 1997, 79:163-175.
66. Colburn R.W., Rickman A.J., DeLeo J.A. The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior. Exp Neurol 1999, 157:289-304.
67. Coyle D.E. Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia 1998, 23:75-83.
68. Stuesse S.L., Cruce W.L., Lovell J.A., McBurney D.L., Crisp T. Microglial proliferation in the spinal cord of aged rats with a sciatic nerve injury. Neurosci Lett 2000, 287:121-124.
69. Stuesse S.L., Crisp T., McBurney D.L., Schechter J.B., Lovell J.A., Cruce W.L. Neuropathic pain in aged rats: behavioral responses and astrocytic activation. Exp Brain Res 2001, 137:219-227.
70. Chiang G.G., Abraham R.T. Phosphorylation of mammalian target of rapamycin (mTOR) at Ser-2448 is mediated by p70S6 kinase. JBiol Chem 2005, 280:25485-25490.
71. Dello Russo C., Lisi L., Tringali G., Navarra P. Involvement of mTOR kinase in cytokine-dependent microglial activation and cell proliferation. Biochem Pharmacol 2009, 78:1242-1251.
72. Lisi L., Navarra P., Feinstein D., Dello Russo C. The mTOR kinase inhibitor rapamycin decreases iNOS mRNA stability in astrocytes. JNeuroinflammation 2011, 8:1.
73. Dello Russo C., Lisi L., Feinstein D.L., Navarra P. mTOR kinase, a key player in the regulation of glial functions: relevance for the therapy of multiple sclerosis. Glia 2013, 61:301-311.
74. Echeverry S., Shi X.Q., Haw A., Liu H., Zhang Z.W., Zhang J. Transforming growth factor-beta1 impairs neuropathic pain through pleiotropic effects. Mol Pain 2009, 5:16.
75. Utreras E., Keller J., Terse A., Prochazkova M., Iadarola M.J., Kulkarni A.B. Transforming growth factor-beta1 regulates Cdk5 activity in primary sensory neurons. JBiol Chem 2012, 287:16917-16929.
76. Suzumura A., Sawada M., Yamamoto H., Marunouchi T. Transforming growth factor-beta suppresses activation and proliferation of microglia invitro. JImmunol 1993, 151:2150-2158.
77. Jones L.L., Kreutzberg G.W., Raivich G. Transforming growth factor beta's 1, 2 and 3 inhibit proliferation of ramified microglia on an astrocyte monolayer. Brain Res 1998, 795:301-306.
78. Vergeli M., Mazzanti B., Ballerini C., Gran B., Amaducci L., Massacesi L. Transforming growth factor-beta 1 inhibits the proliferation of rat astrocytes induced by serum and growth factors. JNeurosci Res 1995, 40:127-133.
79. Makwana M., Jones L.L., Cuthill D., Heuer H., Bohatschek M., Hristova M., et al. Endogenous transforming growth factor beta 1 suppresses inflammation and promotes survival in adult CNS. JNeurosci 2007, 27:11201-11213.