Murabutide revisited: A review of its pleiotropic biological effects

Current Medicinal Chemistry

Volumn 20, Issue 16, 2013, Pages 2068-2079

  Jakopin, Ziga ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

HCV; HIV 1; Immunoadjuvant; Immunomodulator; Immunostimulant; Leprosy; Murabutide; Vaccine

Indexed keywords

CHEMOKINE; CYTOKINE; ION CHANNEL; MURABUTIDE; PHOSPHOTRANSFERASE; TRANSCRIPTION FACTOR;

ANTINEOPLASTIC ACTIVITY; CELL METABOLISM; DRUG MECHANISM; GENE EXPRESSION; HEMATOPOIESIS; HOST RESISTANCE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; LEPROSY; MACROPHAGE; NONHUMAN; PLEIOTROPY; REVIEW;

ACETYLMURAMYL-ALANYL-ISOGLUTAMINE; ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTI-HIV AGENTS; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOLOGIC FACTORS; LEPROSY; VACCINES;

EID: 84877948787     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/0929867311320160002     Document Type: Review

References (58)

1. Doyle, S. L.; O'Neill, L. A. J. Toll-like receptors: From the discovery of NF?B to new insights into transcriptional regulations in innate immunity. Biochem. Pharmacol., 2006, 72, 1102-1113. (Pubitemid 44468394)
2. Hood, J. D.; Warshakoon, H. J.; Kimbrell, M. R.; Shukla, N. M.; Malladi, S. S.; Wang, X.; David, S. A. Immunoprofiling toll-like receptor ligands: Comparison of immunostimulatory and proinflammatory profiles in ex vivo human blood models. Hum. Vaccines, 2010, 6, 322-335.
3. Fritz, J. H.; Ferrero, R. L.; Philpott, D. J.; Girardin, S. E. Nod-like proteins in immunity, inflammation and disease. Nat. Immunol., 2006, 7, 1250-1257. (Pubitemid 46111242)
4. Inohara, N.; Ogura, Y.; Fontalba, A.; Gutierrez, O.; Pons, F.; Crespo, J.; Fukase, K.; Inamura, S.; Kusumoto, S.; Hashimoto, M.; Foster, S. J.; Moran, A. P.; Fernandez-Luna, J. L.; Nunez, G. Host recognition of bacterial muramyl dipeptide mediated through NOD2. J. Biol. Chem., 2003, 278, 5509-5512. (Pubitemid 36800790)
5. Girardin, S. E.; Boneca, I. G.; Viala, J.; Chamaillard, M.; Labigne, A.; Thomas, G.; Philpott, D. J.; Sansonetti, P. J. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem., 2003, 278, 8869-8872. (Pubitemid 36800360)
6. Lecat, A.; Piette, J.; Legrand-Poels, S. The protein Nod2: An innate receptor more complex than previously assumed. Biochem. Pharmacol., 2010, 80, 2021-2031.
7. Shaw, M. H.; Kamada, N.; Warner, N.; Kim, Y. G.; Nunez, G. The ever-expanding function of NOD2: Autophagy, viral recognition, and T cell activation. Trends Immunol., 2011, 32, 73-79.
8. Windheim, M.; Lang, C.; Peggie, M.; Plater, L. A.; Cohen, P. Molecular mechanisms involved in the regulation of cytokine production by muramyl dipeptide. Biochem. J., 2007, 404, 179-190. (Pubitemid 46849589)
9. Ellouz, F.; Adam, A.; Ciorbaru, R.; Lederer, E. Minimal Requirements for Adjuvant Activity of Bacterial Peptidoglycan Derivatives, Biochem. Biophys. Res. Commun., 1974, 59, 1317-1325.
10. Bahr, G. M.; Darcissac, E.; Bevec, D.; Dukor, P.; Chedid, L. Immunopharmacological activities and clinical development of muramyl peptides with particular emphasis on murabutide. Int. J. Immunopharmacol., 1995, 17, 117-131.
11. Waters, R. V.; Terrell, T. G.; Jones, G. H. Uveitis induction in the rabbit by muramyl dipeptides. Infect. Immun., 1986, 51, 816-825. (Pubitemid 16162981)
12. Vidal, V.; Castéran, N.; Riendeau, C. J.; Kornfeld, H.; Darcissac, E. C. A.; Capron, A.; Bahr, G. M. Macrophage stimulation with Murabutide, an HIV-suppressive muramyl peptide derivative, selectively activates extracellular signal-regulated kinases 1 and 2, C/EBP? and STAT1:role of CD14 and Toll-like receptors 2 and 4. Eur. J. Immunol., 2001, 31, 1962-1971. (Pubitemid 32640711)
13. Bahr, G. M. Immune and antiviral effects of the synthetic immunomodulator murabutide. In: Hackett CJ, Harn Jr. DA, editors. Vaccine adjuvants: Immunological and clinical principles, Totowa, New Jersey: Humana Press; 2006, 193-219.
14. Vidal, V.; Dewulf, J.; Bahr, G. M. Enhanced maturation and functional capacity of monocyte-derived immature dendritic cells by the synthetic immunomodulator Murabutide. Immunology, 2001, 103, 479-487. (Pubitemid 32744395)
15. Chedid, L.; Parant, M.; Parant, F.; Lefrancier P.; Choay, J.; Lederer, E. Enhancement of nonspecific immunity to Klebsiella pneumonia infection by a synthetic immunoadjuvant (Nacetylmuramyl-L-alanyl-D-isoglutamine) and several analogs. Proc. Natl. Acad. Sci. USA, 1977, 74, 2089-2093. (Pubitemid 8123616)
16. Parant, M. Muramyl peptides as enhancers of host resistance to bacterial infections. In: Majde JA, ed. Immunopharmacology of Infectious Diseases: Vaccine Adjuvants and Modulators of Non-Specific Resistance. New York: Alan R. Liss, Inc; 1987, 235-244.
17. Phillips, N., C.; Chedid, L. Muramyl peptides and liposomes. In: Gregoriadis GE, ed. Liposomes as Drug Carriers. Chichester: John Wiley and Sons Ltd; 1988, 243-259.
18. Galelli, A.; Chedid, L. Modulation of myelopoiesis in vivo by synthetic adjuvant.active muramyl peptides: Induction of colonystimulating activity and stimulation of stem cell proliferation. Infect. Immun., 1983, 42, 1081-1085. (Pubitemid 14244380)
19. Ismair, M. G.; Vavricka, S. R.; Kullak-Ublick, G. A.; Fried, M.; Mengin-Lecreulx, D.; Girardin, S. E. hPepT1 selectively transports muramyl dipeptide but not Nod1-activating muramyl peptides. Can. J. Physiol. Pharmacol., 2006, 84, 1313-1319. (Pubitemid 46707380)
20. Charrier, L.; Merlin, D. The oligopeptide transporter hPepT1: Gateway to the innate immune response. Lab. Invest., 2006, 86, 538-546. (Pubitemid 43780435)
21. Goasduff, T.; Darcissac, E. C. A.; Vidal, V.; Capron, A.; Bahr, G. M. The transcriptional response of human macrophages to murabutide reflects a spectrum of biological effects for the synthetic immunomodulator. Clin. Exp. Immunol., 2002, 128, 474-482. (Pubitemid 34639309)
22. Bahr, G. M.; Darcissac, E.; Pouillart, P. R.; Chedid, L. A. Synergistic Effects Between Recombinant Interleukin-2 and the Synthetic Immunomodulator Murabutide: Selective Enhancement of Cytokine Release and Potentiation of Antitumor Activity. J. Interferon Cytokine Res., 1996, 16, 169-178. (Pubitemid 26071110)
23. El-Khoury, T. G.; Bahr, G. M.; Echtay, K. S. Muramyl-dipeptideinduced mitochondrial proton leak in macrophages is associated with upregulation of uncoupling protein 2 and the production of reactive oxygen and reactive nitrogen species. FEBS J., 2011, 278, 3054-3064.
24. Jakopin, Z.; Gobec, M.; Mlinarič-Raščan, I.; Sollner Dolenc, M. Immunomodulatory Properties of Novel Nucleotide Oligomerization Domain 2 (Nod2) Agonistic Desmuramyldipeptides. J. Med. Chem., 2012, 55, 6478-6488.
25. Schreck, R.; Bevec, D.; Dukor, P.; Baeuerle, P. A.; Chedid, L.; Bahr G. M. Selection of a muramyl peptide based on its lack of activation of nuclear factor-?B as a potential adjuvant for AIDS vaccines. Clin. Exp. Immunol., 1992, 90, 188-193.
26. El-Jamal, N.; Bahr, G. M.; Echtay, K. S. Effect of muramyl peptides on mitochondrial respiration. Clin. Exp. Immunol., 2008, 155, 72-78.
27. Amorij, J. P.; Kersten, G. F. A.; Saluja, V.; Tonnis, W. F.; Hinrichs, W. L. J.; Slütter, B.; Bal, S. M.; Bouwstra, J. A.; Huckriede, A.; Jiskoot, W. Towards tailored vaccine delivery: Needs, challenges and perspectives. J. Control. Release, 2012, 161, 363-376.
28. Nicholls, E. F.; Madera, L.; Hancock, R. E. W. Immunomodulators as adjuvants for vaccines and antimicrobial therapy. Ann. N.Y. Acad. Sci., 2010, 1213, 46-61.
29. Tada, H.; Aiba, S.; Shibata, K.; Ohteki, T.; Takada, H. Synergistic effect of Nod1 and Nod2 agonists with toll-like receptor agonists on human dendritic cells to generate interleukin-12 and T helper type 1 cells. Infect. Immun., 2005, 73, 7967-7976. (Pubitemid 41740282)
30. Park, J. H.; Kim, Y. G.; Shaw, M.; Kanneganti, T. D.; Fujimoto, Y.; Fukase, K.; Inohara, N.; Nunez, G. Nod1/RICK and TLR signaling regulate chemokine and antimicrobial innate immune responses in mesothelial cells. J. Immunol., 2007, 179, 514-521. (Pubitemid 46986568)
31. Fritz, J. H.; Girardin, S. E.; Fitting, C.; Werts, C.; Mengin-Lecreulx, D.; Caroff, M.; Cavaillon, J. M.; Philpott, D. J.; Adib-Conguy, M. Synergistic stimulation of human monocytes and dendritic cells by Toll-like receptor 4 and Nod1-and Nod2-activating agonists. Eur. J. Immunol., 2005, 35, 2459-2470. (Pubitemid 41179767)
32. Chedid, L. A.; Parant, M. A.; Audibert, F. M.; Riveau, G. J.; Parant, F. J.; Lederer, E.; Choay, J. P.; Lefrancier, P. L. Biological activity of a new synthetic muramyl peptide adjuvant devoid of pyrogenicity. Infect. Immun., 1982, 35, 417-424. (Pubitemid 12164730)
33. Telzak, E.; Wolff, S. M.; Dinarello, C. A.; Conlon, T.; El Kholy, A.; Bahr, G. M.; Choay, J. P.; Morin, A.; Chedid, L. Clinical Evaluation of the Immunoadjuvant Murabutide, a Derivative of MDP, Administered with a Tetanus Toxoid Vaccine. J. Infect. Dis., 1986, 153, 628-633. (Pubitemid 16135674)
34. Olberling, F.; Morin, A.; Duclos, B.; Lang, J. M.; Berchey, E. H.; Chedid, L. Enhancement of antibody response to a natural fragment of streptococcal M protein by Murabutide administered to healthy volunteers. Int. J. Immunol., 1983, 7, 398.
35. Przewlocki, G.; Audibert, F.; Jolivet, M.; Chedid, L.; Kent, S. B.; Neurath, A. R. Production of antibodies recognizing a hepatitis B virus (HBV) surface antigen by administration of murabutide assiciated to a synthetic pre-S HBV peptide conjugated to a toxoid carrier. Biochem. Biophys. Res. Commun., 1986, 140, 557-564. (Pubitemid 17190098)
36. Audibert, F. M.; Przewlocki, G.; Leclerc, C. D.; Jolivet, M. E.; Gras-Masse, H. S.; Tartar, A. L.; Chedid, L. A. Enhancement by murabutide of the immune response to natural and synthetic hepatitis B surface antigens. Infect. Immun., 1984, 45, 261-266. (Pubitemid 14078949)
37. Himes, R.; Lee, S.; McMenigall, K.; Russel-Jones, G. The influence of molecular adjuvants in the cutaneous response to antigen after topical vaccination. Vaccine, 2011, 29, 5393-5398.
38. Jackson, E. M.; Herbst-Kralovetz, M. M. Intranasal Vaccination with Murabutide Enhances Humoral and Mucosal Immune Responses to a Virus-like Particle Vaccine. PLoS ONE, 2012, 7, e41529.
39. Pouillart, P. R.; Audibert, F. M.; Chedid, L. A.; Lefrancier, P. L.; Bahr, G. M. Enhancement by muramyl peptides of the protective response of interferon-?/? against encephalomyocarditis virus infection. Int. J. Immunopharmacol., 1996, 18, 183-192.
40. Bahr, G. M.; Pouillart, P. R.; Chedid, L. A. Enhancement in vivo of the antiinflammatory and antitumor activities of type I interferon by association with the synthetic immunomodulator murabutide. J. Interferon Cytokine Res., 1996, 16, 297-306. (Pubitemid 26132342)
41. Darcissac, E. C. A.; Vidal, V.; Guillaume, M.; Thebault, J. J.; Bahr, G. M. Clinical Tolerance and Profile of Cytokine Induction in Healthy Volunteers Following the Simultaneous Administration of IFN-α and the Synthetic Immunomodulator Murabutide. J. Interferon Cytokine Res., 2001, 21, 655-661. (Pubitemid 32955695)
42. Jupin, C.; Parant, M.; Chedid, L.; Damais, C. Enhanced oxidative burst without interleukin 1 production by normal human polymorphonuclear leukocytes primed with muramyl dipeptides. Inflammation, 1987, 11, 153-161. (Pubitemid 17071814)
43. Jakopin, Z.; Corsini, E.; Gobec, M.; Mlinarič- Raščan, I.; Sollner Dolenc, M. Design, synthesis and biological evaluation of novel desmuramyldipeptide analogs. Eur. J. Med. Chem., 2011, 46, 3762-3777.
44. Parant, M.; Parant, F.; Vinit, M. A.; Jupin, C.; Noso, Y.; Chedid, L. Priming Effect of Muramyl Peptides for Induction by Lipopolysaccharide of Tumor Necrosis Factor Production in Mice. J. Leukocyte Biol., 1990, 47, 164-169. (Pubitemid 20061670)
45. Haidl, I. D.; McAlpine, S. M.; Marshall, J. S. Enhancement of Mast Cell IL-6 Production by Combined Toll-like and Nucleotide-Binding Oligomerization Domain-Like Receptor Activation. Int. Arch. Allergy Immunol., 2011, 154, 227-235.
46. Bahr, G. M. Non-specific immunotherapy of HIV-1 infection: Potential use of the synthetic immunomodulator murabutide. J. Antimicrob. Chemother., 2003, 51, 5-8. (Pubitemid 36163820)
47. Darcissac, E. C. A.; Truong, M. J.; Dewulf, J.; Mouton, Y.; Capron, A.; Bahr, G. M. The Synthetic Immunomodulator Murabutide Controls Human Immunodeficiency Virus Type 1 Replication at Multiple Levels in Macrophages and Dendritic Cells. J. Virol., 2000, 74, 7794-7802. (Pubitemid 30641624)
48. Bahr, G. M.; Darcissac, E. C. A.; Castéran, N.; Amiel, C.; Cocude, C.; Truong, M. J.; Dewulf, J.; Capron, A.; Mouton, Y. Selective Regulation of Human Immunodeficiency Virus-Infected CD4+ lymphocytes by a Synthetic Immunomodulator Leads to Potent Virus Suppression In vitro and in hu-PBL-SCID Mice. J. Virol., 2001, 75, 6941-6952. (Pubitemid 32641581)
49. Truong, M. J.; Delsart, V.; Bahr, G. M. Differentially expressed genes in HIV-1-infected macrophages following treatment with the virus-suppressive immunomodulator murabutide. Virus Res., 2004, 99, 25-33. (Pubitemid 37542487)
50. Cocude, C.; Truong, M. J.; Billaut-Mulot, O.; Delsart, V.; Darcissac, E.; Capron, A.; Mouton, Y.; Bahr, G. M. A novel cellular RNA helicase, RH116, differentially regulates cell growth, programmed cell death and human immunodeficiency virus type 1 replication. J. Gen. Virol., 2003, 84, 3215-3225. (Pubitemid 37540750)
51. Billaut-Mulot, O.; Cocude, C.; Kolesnitchenko, V.; Truong, M. J.; Chan, E. K. L.; Hachula, E.; de la Tribonnière, X.; Capron, A.; Bahr, G. M. SS-56, a novel cellular target of autoantibody responses in Sjögren syndrome and systemic lupus erythematosus. J. Clin. Invest., 2001, 108, 861-869. (Pubitemid 32880295)
52. Amiel, C.; de la Tribonnière, X.; Vidal, V.; Darcissac, E.; Mouton, Y.; Bahr, G. M. Clinical Tolerance and Immunologic Effects After Single or Repeated Administrations of the Synthetic Immunomodulator Murabutide in HIV-1 -Infected Patients. JAIDS, 2002, 30, 294-305. (Pubitemid 34774077)
53. Bahr, G. M.; de la Tribonnière, X.; Darcissac, E.; Ajana, F.; Bocket, L.; Sissoko, D.; Yazdanpanah, Y.; Dewulf, J.; Amiel, C.; Mouton, Y. Clinical and immunological effects of a 6 week immunotherapy cycle with murabutide in HIV-1 patients with unsuccessful long-term retroviral treatment. J. Antimicrob. Chemother., 2003, 51, 1377-1388. (Pubitemid 36748926)
54. Chattree, V.; Khanna, N.; Rao, D. N. Alterations in T cell signal transduction by M. leprae antigens is associated with downregulation of second messengers PKC, calcium, calcineurin, MAPK and various transcription factors in leprosy patients. Mol. Immunol., 2007, 44, 2066-2077.
55. Chattree, V.; Khanna, N.; Bisht, V.; Rao, D. N. Liposomal delivery of Mycobacterium leprae antigen(s) with murabutide and Trat peptide inhibits Fas-mediated apoptosis of peripheral blood mononuclear cells derived from leprosy patients. Indian J. Biochem. Biophys., 2007, 44, 386-393. (Pubitemid 351481357)
56. Chattree, V.; Khanna, N.; Bisht, V.; Rao, D. N. Inhibition of apoptosis, activation of NKT cell and upregulation of CD40 and CD40L mediated by M. leprae antigen(s) combined with Murabutide and Trat peptide in leprosy patients. Moll. Cell. Biochem., 2008, 309, 87-89.
57. Sridevi, K.; Khanna, N.; Chitralekha, K. T.; Arif, A. K.; Tomar, D.; Rao, D. N. Expression of costimulatory molecules (CD80, CD68, CD28, CD152), accessory molecules (TCR ?, TCR ?) and T cell lineage molecules (CD4+, CD8+) in PBMC of leprosy patients using Mycobacterium leprae antigen (MLCWA) with murabutide and T cell peptide of Trat protein. Int. Immunopharmacol., 2004, 4, 1-14. (Pubitemid 38223810)
58. Sridevi, K.; Khanna, N.; Chattree, V.; Pal, P. C.; Haq, W.; Rao, D. N. Reversal of T cell anergy in leprosy patients: In vitro presentation with Mycobacterium leprae antigens using murabutide and Trat peptide in liposomal delivery. Int. Immunopharmacol., 2003, 3, 1589-1600. (Pubitemid 37211482)