Chemotherapeutic Potential of 17-AAG against Cutaneous Leishmaniasis Caused by Leishmania (Viannia) braziliensis

PLoS Neglected Tropical Diseases

Volumn 8, Issue 10, 2014, Pages

  Santos, Diego M ^a   Petersen, Antonio L O A ^a   Celes, Fabiana S ^a   Borges, Valeria M ^a,b   Veras, Patricia S T ^a   de Oliveira, Camila I ^a,b  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b Instituto Nacional de Ciência e Tecnologia de Investigação em Imunologia iii INCT   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; INTERLEUKIN 16; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; TANESPIMYCIN; TUMOR NECROSIS FACTOR ALPHA; BENZOQUINONE DERIVATIVE; HEAT SHOCK PROTEIN 90; INTERLEUKIN 6; MACROCYCLIC LACTAM;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; INFECTION RATE; LEISHMANIA BRAZILIENSIS; MACROPHAGE; MOUSE; NONHUMAN; PROMASTIGOTE; SKIN LEISHMANIASIS; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BIOSYNTHESIS; DRUG EFFECTS; FEMALE; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LEISHMANIASIS, CUTANEOUS; PARASITOLOGY;

AMPHOTERICIN B; ANIMALS; BENZOQUINONES; FEMALE; HSP90 HEAT-SHOCK PROTEINS; INTERLEUKIN-6; LACTAMS, MACROCYCLIC; LEISHMANIA BRAZILIENSIS; LEISHMANIASIS, CUTANEOUS; MACROPHAGES; MICE; MICE, INBRED BALB C; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84920517943     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003275     Document Type: Article

References (62)

1. den Boer M, Argaw D, Jannin J, Alvar J, (2011) Leishmaniasis impact and treatment access. Clin Microbiol Infect 17: 1471–1477.
2. Bittencourt A, Silva N, Straatmann A, Nunes VL, Follador I, et al. (2003) Post-kala-azar dermal leishmaniasis associated with AIDS. Braz J Infect Dis 7: 229–233.
3. Schubach A, Marzochi MC, Cuzzi-Maya T, Oliveira AV, Araujo ML, et al. (1998) Cutaneous scars in American tegumentary leishmaniasis patients: a site of Leishmania (Viannia) braziliensis persistence and viability eleven years after antimonial therapy and clinical cure. Am J Trop Med Hyg 58: 824–827.
4. Mendonca MG, de Brito ME, Rodrigues EH, Bandeira V, Jardim ML, et al. (2004) Persistence of leishmania parasites in scars after clinical cure of American cutaneous leishmaniasis: is there a sterile cure? J Infect Dis 189: 1018–1023.
5. Marsden PD, (1986) Mucosal leishmaniasis (“espundia” Escomel, 1911). Trans R Soc Trop Med Hyg 80: 859–876.
6. Costa JM, Marsden PD, Llanos-Cuentas EA, Netto EM, Carvalho EM, et al. (1986) Disseminated cutaneous leishmaniasis in a field clinic in Bahia, Brazil: a report of eight cases. J Trop Med Hyg 89: 319–323.
7. Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, et al. (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7: e35671.
8. Croft SL, Coombs GH, (2003) Leishmaniasis–current chemotherapy and recent advances in the search for novel drugs. Trends Parasitol 19: 502–508.
9. Berman JD, (1997) Human leishmaniasis: clinical, diagnostic, and chemotherapeutic developments in the last 10 years. Clin Infect Dis 24: 684–703.
10. Chulay JD, Oster CN, McGreevy PB, Hendricks LD, Kreutzer RD, (1988) American cutaneous leishmaniasis: presentation and problems of patient management. Rev Soc Bras Med Trop 21: 165–172.
11. Amato VS, Tuon FF, Siqueira AM, Nicodemo AC, Neto VA, (2007) Treatment of mucosal leishmaniasis in Latin America: systematic review. Am J Trop Med Hyg 77: 266–274.
12. Modabber F, Buffet PA, Torreele E, Milon G, Croft SL, (2007) Consultative meeting to develop a strategy for treatment of cutaneous leishmaniasis. Institute Pasteur, Paris. 13–15 June, 2006. Kinetoplastid Biol Dis 6: 3.
13. Llanos-Cuentas A, Tulliano G, Araujo-Castillo R, Miranda-Verastegui C, Santamaria-Castrellon G, et al. (2008) Clinical and parasite species risk factors for pentavalent antimonial treatment failure in cutaneous leishmaniasis in Peru. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 46: 223–231.
14. Machado P, Araújo C, Da Silva AT, Almeida RP, D'Oliveira Jr A, et al. (2002) Failure of early treatment of cutaneous leishmaniasis in preventing the development of an ulcer. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 34: E69–73.
15. Oliveira LF, Schubach AO, Martins MM, Passos SL, Oliveira RV, et al. (2011) Systematic review of the adverse effects of cutaneous leishmaniasis treatment in the New World. Acta Tropica 118: 87–96.
16. Mishra J, Saxena A, Singh S, (2007) Chemotherapy of leishmaniasis: past, present and future. Curr Med Chem 14: 1153–1169.
17. Morimoto RI, Kline MP, Bimston DN, Cotto JJ, (1997) The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones. Essays Biochem 32: 17–29.
18. Hartl FU, Hayer-Hartl M, (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295: 1852–1858.
19. Goetz MP, (2003) The Hsp90 chaperone complex as a novel target for cancer therapy. Annals of Oncology 14: 1169–1176.
20. Neckers L, Workman P, (2012) Hsp90 molecular chaperone inhibitors: are we there yet? Clinical cancer research: an official journal of the American Association for Cancer Research 18: 64–76.
21. Rochani AK, Singh M, Tatu U, (2013) Heat shock protein 90 inhibitors as broad spectrum anti-infectives. Current pharmaceutical design 19: 377–386.
22. Wiesgigl M, Clos J, (2001) The heat shock protein 90 of Leishmania donovani. Medical microbiology and immunology 190: 27–31.
23. Li Q, Zhou Y, Yao C, Ma X, Wang L, et al. (2009) Apoptosis caused by Hsp90 inhibitor geldanamycin in Leishmania donovani during promastigote-to-amastigote transformation stage. Parasitology research 105: 1539–1548.
24. Petersen AL, Guedes CE, Versoza CL, Lima JG, de Freitas LA, et al. (2012) 17-AAG kills intracellular Leishmania amazonensis while reducing inflammatory responses in infected macrophages. PLoS One 7: e49496.
25. Schulte TW, Neckers LM, (1998) The benzoquinone ansamycin 17-allylamino-17-demethoxygeldanamycin binds to HSP90 and shares important biologic activities with geldanamycin. Cancer Chemother Pharmacol 42: 273–279.
26. de Moura TR, Novais FO, Oliveira F, Clarencio J, Noronha A, et al. (2005) Toward a novel experimental model of infection to study American cutaneous leishmaniasis caused by Leishmania braziliensis. Infect Immun 73: 5827–5834.
27. Miranda KM, Espey MG, Wink DA, (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5: 62–71.
28. Khouri R, Bafica A, Silva Mda P, Noronha A, Kolb JP, et al. (2009) IFN-beta impairs superoxide-dependent parasite killing in human macrophages: evidence for a deleterious role of SOD1 in cutaneous leishmaniasis. J Immunol 182: 2525–2531.
29. Elstner EF, Heupel A, (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70: 616–620.
30. Liese J, Schleicher U, Bogdan C, (2008) The innate immune response against Leishmania parasites. Immunobiology 213: 377–387.
31. Roy N, Nageshan RK, Ranade S, Tatu U, (2012) Heat shock protein 90 from neglected protozoan parasites. Biochimica et biophysica acta 1823: 707–711.
32. Mout R, Xu Z-D, Wolf AKH, Jo Davisson V, Jarori GK, (2012) Anti-malarial activity of geldanamycin derivatives in mice infected with Plasmodium yoelii. Malaria journal 11: 54.
33. Devaney E, O'Neill K, Harnett W, Whitesell L, Kinnaird JH, (2005) Hsp90 is essential in the filarial nematode Brugia pahangi. International journal for parasitology 35: 627–636.
34. Wenkert D, Ramirez B, Shen Y, Kron MA, (2010) In Vitro Activity of Geldanamycin Derivatives against Schistosoma japonicum and Brugia malayi. Journal of parasitology research 2010: 716498–716498.
35. Costa JML, (2005) Epidemiologia das Leishmanioses do Brasil. Gazeta Médica da Bahia 75: 3–18.
36. Gomes IN, Calabrich AF, Tavares Rda S, Wietzerbin J, de Freitas LA, et al. (2003) Differential properties of CBA/J mononuclear phagocytes recovered from an inflammatory site and probed with two different species of Leishmania. Microbes Infect 5: 251–260.
37. Sousa-Franco J, Araujo-Mendes E, Silva-Jardim I, J LS, Faria DR, et al. (2006) Infection-induced respiratory burst in BALB/c macrophages kills Leishmania guyanensis amastigotes through apoptosis: possible involvement in resistance to cutaneous leishmaniasis. Microbes Infect 8: 390–400.
38. Matta NE, Cysne-Finkelstein L, Machado GM, Da-Cruz AM, Leon L, (2010) Differences in the antigenic profile and infectivity of murine macrophages of Leishmania (Viannia) parasites. J Parasitol 96: 509–515.
39. Carvalho LP, Passos S, Schriefer A, Carvalho EM, (2012) Protective and pathologic immune responses in human tegumentary leishmaniasis. Frontiers in immunology 3: 301.
40. Follador I, Araujo C, Bacellar O, Araujo CB, Carvalho LP, et al. (2002) Epidemiologic and immunologic findings for the subclinical form of Leishmania braziliensis infection. Clin Infect Dis 34: E54–58.
41. Shimp SK, Parson CD, Regna NL, Thomas AN, Chafin CB, et al. (2012) HSP90 inhibition by 17-DMAG reduces inflammation in J774 macrophages through suppression of Akt and nuclear factor-κB pathways. Inflammation research 61: 521–533.
42. Luo S, Wang T, Qin H, Lei H, Xia Y, (2011) Obligatory role of heat shock protein 90 in iNOS induction. Am J Physiol Cell Physiol 301: C227–233.
43. Chatterjee A, Dimitropoulou C, Drakopanayiotakis F, Antonova G, Snead C, et al. (2007) Heat shock protein 90 inhibitors prolong survival, attenuate inflammation, and reduce lung injury in murine sepsis. American journal of respiratory and critical care medicine 176: 667–675.
44. Dello Russo C, Polak PE, Mercado PR, Spagnolo A, Sharp A, et al. (2006) The heat-shock protein 90 inhibitor 17-allylamino-17-demethoxygeldanamycin suppresses glial inflammatory responses and ameliorates experimental autoimmune encephalomyelitis. J Neurochem 99: 1351–1362.
45. Madrigal-Matute J, López-Franco O, Blanco-Colio LM, Muñoz-García B, Ramos-Mozo P, et al. (2010) Heat shock protein 90 inhibitors attenuate inflammatory responses in atherosclerosis. Cardiovascular research 86: 330–337.
46. Poulaki V, Iliaki E, Mitsiades N, Mitsiades CS, Paulus YN, et al. (2007) Inhibition of Hsp90 attenuates inflammation in endotoxin-induced uveitis. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 21: 2113–2123.
47. Carvalho AK, Silveira FT, Passero LF, Gomes CM, Corbett CE, et al. (2012) Leishmania (V.) braziliensis and L. (L.) amazonensis promote differential expression of dendritic cells and cellular immune response in murine model. Parasite Immunol 34: 395–403.
48. Besteiro S, Williams RA, Morrison LS, Coombs GH, Mottram JC, (2006) Endosome sorting and autophagy are essential for differentiation and virulence of Leishmania major. J Biol Chem 281: 11384–11396.
49. Falcao S, de Moura TR, Clarencio J, Brodskyn C, Barral A, et al. (2012) The presence of Tregs does not preclude immunity to reinfection with Leishmania braziliensis. Int J Parasitol 42: 771–780.
50. Belkaid Y, Hoffmann KF, Mendez S, Kamhawi S, Udey MC, et al. (2001) The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. J Exp Med 194: 1497–1506.
51. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL, (2002) CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420: 502–507.
52. Stauch A, Duerr HP, Dujardin JC, Vanaerschot M, Sundar S, et al. (2012) Treatment of visceral leishmaniasis: model-based analyses on the spread of antimony-resistant L. donovani in Bihar, India. PLoS Negl Trop Dis 6: e1973.
53. Tuon FF, Amato VS, Graf ME, Siqueira AM, Nicodemo AC, et al. (2008) Treatment of New World cutaneous leishmaniasis–a systematic review with a meta-analysis. Int J Dermatol 47: 109–124.
54. van Griensven J, Balasegaram M, Meheus F, Alvar J, Lynen L, et al. (2010) Combination therapy for visceral leishmaniasis. Lancet Infect Dis 10: 184–194.
55. Haldar AK, Sen P, Roy S, (2011) Use of antimony in the treatment of leishmaniasis: current status and future directions. Molecular biology international 2011: 571242–571242.
56. Varela MR, Mollinedo-Gajate C, Muro A, Mollinedo F, (2013) The HSP90 inhibitor 17-AAG potentiates the antileishmanial activity of the ether lipid edelfosine. Acta Trop 131C: 32–36.
57. de Morais-Teixeira E, Gallupo MK, Rodrigues LF, Romanha AJ, Rabello A, (2014) In vitro interaction between paromomycin sulphate and four drugs with leishmanicidal activity against three New World Leishmania species. J Antimicrob Chemother 69: 150–154.
58. Trinconi CT, Reimao JQ, Yokoyama-Yasunaka JK, Miguel DC, Uliana SR (2014) Combination therapy with tamoxifen and amphotericin B in experimental cutaneous leishmaniasis. Antimicrob Agents Chemother.
59. Zhang J, Liu W, Tan J, Sun Y, Wan Z, et al. (2013) Antifungal activity of geldanamycin alone or in combination with fluconazole against Candida species. Mycopathologia 175: 273–279.
60. Egorin MJ, Zuhowski EG, Rosen DM, Sentz DL, Covey JM, et al. (2001) Plasma pharmacokinetics and tissue distribution of 17-(allylamino)-17-demethoxygeldanamycin (NSC 330507) in CD2F1 mice1. Cancer Chemother Pharmacol 47: 291–302.
61. Solit DB, Zheng FF, Drobnjak M, Munster PN, Higgins B, et al. (2002) 17-Allylamino-17-demethoxygeldanamycin induces the degradation of androgen receptor and HER-2/neu and inhibits the growth of prostate cancer xenografts. Clin Cancer Res 8: 986–993.
62. Usmani SZ, Bona R, Li Z, (2009) 17 AAG for HSP90 inhibition in cancer–from bench to bedside. Curr Mol Med 9: 654–664.