Antinociceptive profile of potent opioid peptide AM94, a fluorinated analogue of biphalin with non-hydrazine linker

Journal of Peptide Science

Volumn 19, Issue 4, 2013, Pages 233-239

  Mollica, Adriano ^a   Costante, Roberto ^a   Stefanucci, Azzurra ^b   Pinnen, Francesco ^a   Lucente, Gino ^c   Fidanza, Stefano ^d   Pieretti, Stefano ^d  

^a UNIVERSITY OF CHIETI   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c CNR   (Italy)

^d ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

AM94; Analgesic; Antinociception; Biphalin; Formalin test; Molecular modeling; Opioids; Tail flick test; Variable temperature 1H NMR

Indexed keywords

AM 94; ANTINOCICEPTIVE AGENT; BIPHALIN; FORMALDEHYDE; MORPHINE; OPIATE PEPTIDE; UNCLASSIFIED DRUG;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DRUG CONFORMATION; DRUG POTENCY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; TAIL FLICK TEST; TEMPERATURE;

ANALGESICS; ANIMALS; ENKEPHALINS; MALE; MICE; MORPHINE; OPIOID PEPTIDES; PROTEIN STRUCTURE, SECONDARY; RATS; RATS, WISTAR; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, MU;

ANIMALIA; MUS; RATTUS;

EID: 84875588108     PISSN: 10752617     EISSN: 10991387     Source Type: Journal    
DOI: 10.1002/psc.2465     Document Type: Article

References (38)

1. Lipkowski AW, Konecka AM, Sroczyńska I. Double-enkephalins-synthesis, activity on guinea-pig ileum, and analgesic effect. Peptides 1982; 3: 697-700.
2. Costa T, Wüster M, Herz A, Shimohigashi Y, Chen HC, Rodbard D. Receptor binding and biological activity of bivalent enkephalins. Biochem. Pharmacol. 1985; 34: 25-30.
3. Lipkowski AW, Misicka A, Davis P, Stropova D, Janders J, Lachwa M, Porreca F, Yamamura HI, Hruby VJ. Biological activity of fragments and analogues of the potent dimeric opioid peptide, biphalin. Bioorg. Med. Chem. Lett. 1999; 9: 2763-2766.
4. Horan PJ, Mattia A, Bilsky EJ, Weber S, Davis TP, Yamamura HI, Malatynska E, Appleyard SM, Slaninova J, Misicka A, Lipkowski AW, Hruby VJ, Porreca F. Antinociceptive profile of biphalin, a dimeric enkephalin analog. J. Pharmacol. Exp. Ther. 1993; 265: 1446-1454.
5. Kosson D, Klinowiecka A, Kosson P, Bonney I, Carr DB, Mayzner-Zawadzka E, Lipkowski AW. Intrathecal antinociceptive interaction between the NMDA antagonist ketamine and the opioids, morphine and biphalin. Eur. J. Pain 2008; 12: 611-616.
6. Misterek K, Maszcynska I, Dorociak A, Gumulka SW, Carr DB, Szyfelbein SK, Lipkowski AW. Spinal co-administration of peptide substance P antagonist increases antinociceptive effect of the opioid peptide biphalin. Life Sci. 1994; 54: 939-944.
7. Abbruscato TJ, Thomas SA, Hruby VJ, Davis TP. Brain and spinal cord distribution of biphalin: correlation with opioid receptor density and mechanism of CNS entry. J. Neurochem. 1997; 69: 1236-1245.
8. Abbruscato TJ, Williams SA, Misicka A, Lipkowski AW, Hruby VJ, Davis TP. Blood-to-central nervous system entry and stability of biphalin, a unique double-enkephalin analog, and its halogenated derivatives. J. Pharmacol. Exp. Ther. 1996; 276: 1049-1057.
9. 125I-Tyr1]biphalin binding to opioid receptors of rat brain and NG108-15 cell membranes. Life Sci. 1998; 62: 199-204.
10. Yamazaki M, Suzuki T, Narita M, Lipkowski AW. The opioid peptide analogue biphalin induces less physical dependence than morphine. Life Sci. 2001; 69: 1023-1028.
11. Shen KF, Crain SM. Biphalin, an enkephalin analog with unexpectedly high antinociceptive potency and low dependence liability in vivo, selectively antagonizes excitatory opioid receptor functions of sensory neurons in culture. Brain Res. 1995; 701: 158-166.
12. Tang JL, Lipkowski AW, Specter S. Molecular assessment of the potential combination therapy of cytokines with biphalin and AZT for Friend leukemia virus infection in vitro. Pharmacol. Rep. 2008; 60: 90-98.
13. Feliciani F, Pinnen F, Stefanucci A, Costante R, Cacciatore I, Lucente G, Mollica A. Structure-Activity relationships of biphalin analogues and their biological evaluation on opioid receptors. Mini Rev. Med. Chem. 2013; published online [MRMC-EPUB-20120612-6].
14. Huber JD, Campos CR, Egleton RD, Witt K, Guo L, Roberts MJ, Bentley MD, Davis TP. Conjugation of low molecular weight poly(ethylene glycol) to biphalin enhances antinociceptive profile. J. Pharm. Sci. 2003; 92: 1377-1385.
15. Misicka A, Lipkowski AW, Horvath R, Davis P, Porreca F, Yamamura HI, Hruby VJ. Structure-activity relationship of biphalin. The synthesis and biological activities of new analogues with modifications in positions 3 and 4. Life Sci. 1997; 60: 1263-1269.
16. Li G, Haq W, Xiang L, Lou BS, Hughes R, De Leon IA, Davis P, Gillespie TJ, Romanowski M, Zhu X, Misicka A, Lipkowski AW, Porreca F, Davis TP, Yamamura HI, O'Brien DF, Hruby VJ. Modifications of the 4, 4′-residues and SAR studies of Biphalin, a highly potent opioid receptor active peptide. Bioorg. Med. Chem. Lett. 1998; 8: 555-560.
17. Mollica A, Davis P, Ma SW, Lai J, Porreca F, Hruby VJ. Synthesis and biological evaluation of new biphalin analogues with non-hydrazine linkers. Bioorg. Med. Chem. Lett. 2005; 15: 2471-2475.
18. Mollica A, Pinnen F, Feliciani F, Stefanucci A, Lucente G, Davis P, Porreca F, Ma SW, Lai J, Hruby VJ. New potent biphalin analogues containing p-fluoro-l-phenylalanine at the 4, 4′ positions and non-hydrazine linkers. Amino Acids 2011; 40: 1503-1511.
19. Leone S, Chiavaroli A, Orlando G, Mollica A, Di Nisio C, Brunetti L, Vacca M. The analgesic activity of biphalin and its analog AM 94 in rats. Eur. J. Pharmacol. 2012; 685: 70-73.
20. Foran SE, Carr DB, Lipkowski AW, Maszczynska I, Marchand JE, Misicka A, Beinborn M, Kopin AS, Kream RM. Inhibition of morphine tolerance development by a substance P-opioid peptide chimera. J. Pharmacol. Exp. Ther. 2000; 295: 1142-1148.
21. Yaksh TL, Rudy TA. Chronic catheterization of the spinal subarachnoid space. Physiol. Behav. 1976; 17: 1031-1036.
22. Jorgensen WL, Maxwell DS, Tirado-Rives J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 1996; 118: 11225-11235.
23. Grippo L, Lucidi S. A globally convergent version of the Polak-Ribiére conjugate gradient method. Math. Programming. 1997; 77: 375-391.
24. Silbert BS, Lipkowski AW, Cepeda MS, Szyfelbein SK, Osgood PF, Carr DB. Analgesic activity of novel bivalent opioid peptide compared to morphine via different routes of administration. Agents Actions 1991; 33: 382-387.
25. Andersen NH, Neidigh JW, Harris SM, Lee GM, Liu Z, Tong H. Extracting information from the temperature gradients of polypeptide NH chemical shifts. 1. The importance of conformational averaging. J. Am. Chem. Soc. 1997; 119: 8547-8561.
26. Pease LG, Watson C. Conformational and ion binding studies of a cyclic pentapeptide. Evidence for β and γ turns in solution. J. Am. Chem. Soc. 1978; 100: 1279-1286.
27. Stevens ES, Sugawara N, Bonora GM, Toniolo C. Conformational analysis of linear peptides. 3. Temperature dependence of NH chemical shifts in chloroform. J. Am. Chem. Soc. 1980; 102: 7048-7050.
28. 1H chemical shifts in proteins. J. Biomol. NMR 1997; 9: 359-369.
29. Cierpicki T, Otlewski J. Amide proton temperature coefficients as hydrogen bond indicators in proteins. J. Biomol. NMR 2001; 21: 249-261.
30. Flippen-Anderson JL, Deschamps JR, George C, Hruby VJ, Misicka A, Lipkowski AW. Crystal structure of Biphalin sulfate: a multireceptor opioid peptide. J. Pept. Res. 2002; 59: 123-133.
31. Hsieh JY, Chiang TY, Chen JL, Chen YW, Lin HC, Hwang CC. A molecular dynamics study on opioid activities of biphalin molecule. J. Mol. Model. 2011; 17: 2455-2464.
32. Stefanucci A, Pinnen F, Feliciani F, Cacciatore I, Lucente G, Mollica A. Conformationally constrained histidines in the design of peptidomimetics: strategies for the χ-space control. Int. J. Mol. Sci. 2011; 12: 2853-2890.
33. Bilsky EJ, Egleton RD, Mitchell SA, Palian MM, Davis P, Huber JD, Jones H, Yamamura HI, Janders J, Davis TP, Porreca F, Hruby VJ, Polt R. Enkephalin glycopeptide analogues produce analgesia with reduced dependence liability. J. Med. Chem. 2000; 43: 2586-2590.
34. Ananthan S. Opioid ligands with mixed μ/δ opioid receptor interactions: an emerging approach to novel analgesics AAPS J. 2006; 8: 118-125.
35. Mollica A, Davis P, Ma SW, Porreca F, Lai J, Hruby VJ. Synthesis and biological activity of the first cyclic biphalin analogues. Bioorg. Med. Chem. Lett. 2006; 16: 367-372.
36. Garrod S, Bollard ME, Nicholls AW, Connor SC, Connelly J, Nicholson JK, Holmes E. Integrated metabonomic analysis of the multiorgan effects of hydrazine toxicity in the rat. Chem. Res. Toxicol. 2005; 18: 115-122.
37. Klenø TG, Leonardsen LR, Kjeldal HØ, Laursen SM, Jensen ON, Baunsgaard D. Mechanisms of hydrazine toxicity in rat liver investigated by proteomics and multivariate data analysis. Proteomics 2004; 4: 868-880.
38. Nicholls AW, Holmes E, Lindon JC, Shockcor JP, Farrant RD, Haselden JN, Damment SJ, Waterfield CJ, Nicholson JK. Metabonomic investigations into hydrazine toxicity in the rat. Chem. Res. Toxicol. 2001; 14: 975-987.