Differential Gene Expression and Infection Profiles of Cutaneous and Mucosal Leishmania braziliensis Isolates from the Same Patient

PLoS Neglected Tropical Diseases

Volumn 9, Issue 9, 2015, Pages

  Alves Ferreira, Eliza V C ^a   Toledo, Juliano S ^a,b   De Oliveira, Arthur H C ^a   Ferreira, Tiago R ^a   Ruy, Patricia C ^a   Pinzan, Camila F ^a   Santos, Ramon F ^a   Boaventura, Viviane ^c,d   Rojo, David ^b   López Gonzálvez, Ángelez ^b   Rosa, Jose C ^a   Barbas, Coral ^b   Barral Netto, Manoel ^c,d   Barral, Aldina ^c,d   Cruz, Angela K ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSIDAD SAN PABLO CEU   (Spain)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

^d NONE   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GENOMIC DNA; HEAT SHOCK PROTEIN 70; INTERLEUKIN 4; PROSTAGLANDIN F2; PROTEOME;

ARTICLE; CAPILLARY ELECTROPHORESIS; CONTROLLED STUDY; DNA LIBRARY; GENE SEQUENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LEISHMANIA BRAZILIENSIS; LEISHMANIASIS; MASS FRAGMENTOGRAPHY; MUCOSAL LEISHMANIASIS; NONHUMAN; PARASITE LOAD; PARASITE VIRULENCE; PERITONEUM MACROPHAGE; PROTEIN ANALYSIS; PULSED FIELD GEL ELECTROPHORESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SKIN LEISHMANIASIS; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; BRAZIL; COMPARATIVE STUDY; DISEASE MODEL; GENE EXPRESSION PROFILING; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLOME; MICROBIOLOGY; MUCOSA; PATHOLOGY; SKIN;

ANIMALS; BRAZIL; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; HUMANS; LEISHMANIA BRAZILIENSIS; LEISHMANIASIS, MUCOCUTANEOUS; METABOLOME; MICE, INBRED BALB C; MUCOUS MEMBRANE; PROTEOME; SKIN;

EID: 84943141683     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004018     Document Type: Article

References (59)

1. Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, et al. Leishmaniasis worldwide and global estimates of its incidence. PLoS One. 2012;7(5):e35671. doi: 10.1371/journal.pone.0035671 22693548
2. de Almeida MC, Vilhena V, Barral A, Barral-Netto M, Leishmanial infection: analysis of its first steps. A review. Mem Inst Oswaldo Cruz. 2003;98(7):861–70. 14762510
3. Teixeira MJ, Teixeira CR, Andrade BB, Barral-Netto M, Barral A, Chemokines in host-parasite interactions in leishmaniasis. Trends Parasitol. 2006;22(1):32–40. 16310413
4. Andrade BB, de Oliveira CI, Brodskyn CI, Barral A, Barral-Netto M, Role of sand fly saliva in human and experimental leishmaniasis: current insights. Scand J Immunol. 2007;66(2–3):122–7. 17635789
5. Reithinger R, Dujardin JC, Louzir H, Pirmez C, Alexander B, Brooker S, Cutaneous leishmaniasis. Lancet Infect Dis. 2007;7(9):581–96. Epub 2007/08/24. 17714672
6. David CV, Craft N, Cutaneous and mucocutaneous leishmaniasis. Dermatol Ther. 2009;22(6):491–502. doi: 10.1111/j.1529-8019.2009.01272.x 19889134
7. Amato VS, Tuon FF, Bacha HA, Neto VA, Nicodemo AC, Mucosal leishmaniasis. Current scenario and prospects for treatment. Acta Trop. 2008;105(1):1–9. Epub 2007/09/22. 17884002
8. Barral A, Pedral-Sampaio D, Grimaldi G, JuniorMomen H, McMahon-Pratt D, Ribeiro de Jesus A, et al. Leishmaniasis in Bahia, Brazil: evidence that Leishmania amazonensis produces a wide spectrum of clinical disease. Am J Trop Med Hyg. 1991;44(5):536–46. Epub 1991/05/01. 2063957
9. Jara M, Adaui V, Valencia BM, Martinez D, Alba M, Castrillon C, et al. Real-time PCR assay for detection and quantification of Leishmania (Viannia) organisms in skin and mucosal lesions: exploratory study of parasite load and clinical parameters. J Clin Microbiol. 2013;51(6):1826–33. doi: 10.1128/JCM.00208-13 23554201
10. Schriefer A, Schriefer AL, Góes-Neto A, Guimarães LH, Carvalho LP, Almeida RP, et al. Multiclonal Leishmania braziliensis population structure and its clinical implication in a region of endemicity for American tegumentary leishmaniasis. Infect Immun. 2004;72(1):508–14. 14688132
11. Carvalhal DG, Barbosa A, D'El-Rei Hermida M, Clarencio J, Pinheiro NF, Veras PS, et al. The modelling of mononuclear phagocyte-connective tissue adhesion in vitro: application to disclose a specific inhibitory effect of Leishmania infection. Exp Parasitol. 2004;107(3–4):189–99. 15363945
12. Maretti-Mira AC, de Pinho Rodrigues KM, de Oliveira-Neto MP, Pirmez C, Craft N, MMP-9 activity is induced by Leishmania braziliensis infection and correlates with mucosal leishmaniasis. Acta Trop. 2011;119(2–3):160–4. doi: 10.1016/j.actatropica.2011.05.009 21663729
13. Boaventura VS, Cafe V, Costa J, Oliveira F, Bafica A, Rosato A, et al. Concomitant early mucosal and cutaneous leishmaniasis in Brazil. Am J Trop Med Hyg. 2006;75(2):267–9. Epub 2006/08/10. 16896130
14. Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M, et al. The genome of the kinetoplastid parasite, Leishmania major. Science. 2005;309(5733):436–42. Epub 2005/07/16. 16020728
15. Peacock CS, Seeger K, Harris D, Murphy L, Ruiz JC, Quail MA, et al. Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet. 2007;39(7):839–47. Epub 2007/06/19. 17572675
16. Kapler GM, Coburn CM, Beverley SM, Stable transfection of the human parasite Leishmania major delineates a 30-kilobase region sufficient for extrachromosomal replication and expression. Mol Cell Biol. 1990;10(3):1084–94. Epub 1990/03/01. 2304458
17. Smith DF, Peacock CS, Cruz AK, Comparative genomics: from genotype to disease phenotype in the leishmaniases. Int J Parasitol. 2007;37(11):1173–86. 17645880
18. Beverley SM, Characterization of the 'unusual' mobility of large circular DNAs in pulsed field-gradient electrophoresis. Nucleic Acids Res. 1988;16(3):925–39. Epub 1988/02/11. 3344223
19. Cruz A, Coburn CM, Beverley SM, Double targeted gene replacement for creating null mutants. Proc Natl Acad Sci U S A. 1991;88(16):7170–4. Epub 1991/08/15. 1651496
20. de Toledo JS, Junqueira dos Santos AF, Rodrigues de Moura T, Antoniazi SA, Brodskyn C, Indiani de Oliveira C, et al. Leishmania (Viannia) braziliensis transfectants overexpressing the miniexon gene lose virulence in vivo. Parasitol Int. 2009;58(1):45–50. Epub 2008/11/11. doi: 10.1016/j.parint.2008.09.006 18992366
21. Afonso LC, Scott P, Immune responses associated with susceptibility of C57BL/10 mice to Leishmania amazonensis. Infect Immun. 1993;61(7):2952–9. 8514400
22. Scott P, Pearce E, Natovitz P, Sher A, Vaccination against cutaneous leishmaniasis in a murine model. II. Immunologic properties of protective and nonprotective subfractions of soluble promastigote extract. J Immunol. 1987;139(9):3118–25. 3499465
23. Toledo JS, Ferreira TR, Defina TP, Dossin FeM, Beattie KA, Lamont DJ, et al. Cell homeostasis in a Leishmania major mutant overexpressing the spliced leader RNA is maintained by an increased proteolytic activity. Int J Biochem Cell Biol. 2010;42(10):1661–71. doi: 10.1016/j.biocel.2010.06.013 20601086
24. Scher R, Garcia JB, Pascoalino B, Schenkman S, Cruz AK, Characterization of anti-silencing factor 1 in Leishmania major. Mem Inst Oswaldo Cruz. 2012;107(3):377–86. 22510834
25. LeBowitz JH, Smith HQ, Rusche L, Beverley SM, Coupling of poly(A) site selection and trans-splicing in Leishmania. Genes Dev. 1993;7(6):996–1007. 8504937
26. LeBowitz JH, Coburn CM, McMahon-Pratt D, Beverley SM, Development of a stable Leishmania expression vector and application to the study of parasite surface antigen genes. Proc Natl Acad Sci U S A. 1990;87(24):9736–40. 2124701
27. Aslett M, Aurrecoechea C, Berriman M, Brestelli J, Brunk BP, Carrington M, et al. TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res. 2010;38(Database issue):D457–62. doi: 10.1093/nar/gkp851 19843604
28. Li H, Durbin R, Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754–60. doi: 10.1093/bioinformatics/btp324 19451168
29. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078–9. doi: 10.1093/bioinformatics/btp352 19505943
30. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, et al. Artemis: sequence visualization and annotation. Bioinformatics. 2000;16(10):944–5. 11120685
31. Zhang WW, Ramasamy G, McCall LI, Haydock A, Ranasinghe S, Abeygunasekara P, et al. Genetic analysis of Leishmania donovani tropism using a naturally attenuated cutaneous strain. PLoS Pathog. 2014;10(7):e1004244. doi: 10.1371/journal.ppat.1004244 24992200
32. Canuto GA, Castilho-Martins EA, Tavares MF, Rivas L, Barbas C, Lopez-Gonzalvez A, Multi-analytical platform metabolomic approach to study miltefosine mechanism of action and resistance in Leishmania. Analytical and bioanalytical chemistry. 2014;406(14):3459–76. doi: 10.1007/s00216-014-7772-1 24722876
33. Ciborowski M, Lipska A, Godzien J, Ferrarini A, Korsak J, Radziwon P, et al. Combination of LC-MS- and GC-MS-based metabolomics to study the effect of ozonated autohemotherapy on human blood. Journal of proteome research. 2012;11(12):6231–41. doi: 10.1021/pr3008946 23148940
34. Suhre K, Schmitt-Kopplin P, MassTRIX: mass translator into pathways. Nucleic acids research. 2008;36(Web Server issue):W481–4. doi: 10.1093/nar/gkn194 18442993
35. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS, MetaboAnalyst 2.0—a comprehensive server for metabolomic data analysis. Nucleic Acids Res. 2012;40(Web Server issue):W127–33. doi: 10.1093/nar/gks374 22553367
36. BRASIL MDS. Manual de Vigilância da Leishmaniose Tegumentar Americana 2007. www.saude.gov.br/svs.
37. Ives A, Ronet C, Prevel F, Ruzzante G, Fuertes-Marraco S, Schutz F, et al. Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science. 2011;331(6018):775–8. doi: 10.1126/science.1199326 21311023
38. Saito S, Hamada A, Watanabe N, Obata T, Katakura K, Ohtomo H, Eosinophil chemotactic activity in Leishmania amazonensis promastigotes. Parasitol Res. 1996;82(6):485–9. 8832727
39. Sørensen AL, Kharazmi A, Nielsen H, Leishmania interaction with human monocytes and neutrophils: modulation of the chemotactic response. APMIS. 1989;97(8):754–60. 2765277
40. Harvey KA, Walker CL, Pavlina TM, Xu Z, Zaloga GP, Siddiqui RA, Long-chain saturated fatty acids induce pro-inflammatory responses and impact endothelial cell growth. Clin Nutr. 2010;29(4):492–500. doi: 10.1016/j.clnu.2009.10.008 19926177
41. Kim MC, Kim MG, Jo YS, Song HS, Eom TI, Sim SS, Effects of C18 Fatty Acids on Intracellular Ca(2+) Mobilization and Histamine Release in RBL-2H3 Cells. Korean J Physiol Pharmacol. 2014;18(3):241–7. doi: 10.4196/kjpp.2014.18.3.241 24976764
42. Laine PS, Schwartz EA, Wang Y, Zhang WY, Karnik SK, Musi N, et al. Palmitic acid induces IP-10 expression in human macrophages via NF-kappaB activation. Biochem Biophys Res Commun. 2007;358(1):150–5. 17467667
43. Aderem AA, Protein myristoylation as an intermediate step during signal transduction in macrophages: its role in arachidonic acid metabolism and in responses to interferon gamma. J Cell Sci Suppl. 1988;9:151–67. 3151694
44. Spite M, Norling LV, Summers L, Yang R, Cooper D, Petasis NA, et al. Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature. 2009;461(7268):1287–91. doi: 10.1038/nature08541 19865173
45. Arita M, Bianchini F, Aliberti J, Sher A, Chiang N, Hong S, et al. Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J Exp Med. 2005;201(5):713–22. 15753205
46. Liao Z, Dong J, Wu W, Yang T, Wang T, Guo L, et al. Resolvin D1 attenuates inflammation in lipopolysaccharide-induced acute lung injury through a process involving the PPARγ/NF-κB pathway. Respir Res. 2012;13:110. doi: 10.1186/1465-9921-13-110 23199346
47. Oh SF, Dona M, Fredman G, Krishnamoorthy S, Irimia D, Serhan CN, Resolvin E2 formation and impact in inflammation resolution. J Immunol. 2012;188(9):4527–34. doi: 10.4049/jimmunol.1103652 22450811
48. Ramakrishnan S, Serricchio M, Striepen B, Bütikofer P, Lipid synthesis in protozoan parasites: a comparison between kinetoplastids and apicomplexans. Prog Lipid Res. 2013;52(4):488–512. doi: 10.1016/j.plipres.2013.06.003 23827884
49. Gibellini F, Smith TK, The Kennedy pathway—De novo synthesis of phosphatidylethanolamine and phosphatidylcholine. IUBMB Life. 2010;62(6):414–28. doi: 10.1002/iub.337 20503434
50. Prescott SM, Zimmerman GA, Stafforini DM, McIntyre TM, Platelet-activating factor and related lipid mediators. Annu Rev Biochem. 2000;69:419–45. 10966465
51. Gomes MT, Monteiro RQ, Grillo LA, Leite-Lopes F, Stroeder H, Ferreira-Pereira A, et al. Platelet-activating factor-like activity isolated from Trypanosoma cruzi. Int J Parasitol. 2006;36(2):165–73. 16337632
52. Tavares IA, Vine ND, Phthalic acid esters inhibit arachidonate metabolism by rat peritoneal leucocytes. J Pharm Pharmacol. 1985;37(1):67–8. 2858534
53. Kubata BK, Duszenko M, Martin KS, Urade Y, Molecular basis for prostaglandin production in hosts and parasites. Trends Parasitol. 2007;23(7):325–31. Epub 2007/05/29. 17531535
54. Ahmad S, Israf DA, Lajis NH, Shaari K, Mohamed H, Wahab AA, et al. Cardamonin, inhibits pro-inflammatory mediators in activated RAW 264.7 cells and whole blood. Eur J Pharmacol. 2006;538(1–3):188–94. 16650843
55. Lee DS, Li B, Im NK, Kim YC, Jeong GS, 4,2',5'-trihydroxy-4'-methoxychalcone from Dalbergia odorifera exhibits anti-inflammatory properties by inducing heme oxygenase-1 in murine macrophages. Int Immunopharmacol. 2013;16(1):114–21. doi: 10.1016/j.intimp.2013.03.026 23566812
56. Dea-Ayuela MA, Ordonez-Gutierrez L, Bolas-Fernandez F, Changes in the proteome and infectivity of Leishmania infantum induced by in vitro exposure to a nitric oxide donor. Int J Med Microbiol. 2009;299(3):221–32. Epub 2008/09/09. doi: 10.1016/j.ijmm.2008.07.006 18774335
57. Kubata BK, Duszenko M, Kabututu Z, Rawer M, Szallies A, Fujimori K, et al. Identification of a novel prostaglandin f(2alpha) synthase in Trypanosoma brucei. J Exp Med. 2000;192(9):1327–38. Epub 2000/11/09. 11067881
58. Cuervo P, De Jesus JB, Saboia-Vahia L, Mendonça-Lima L, Domont GB, Cupolillo E, Proteomic characterization of the released/secreted proteins of Leishmania (Viannia) braziliensis promastigotes. J Proteomics. 2009;73(1):79–92. doi: 10.1016/j.jprot.2009.08.006 19703603
59. Silverman JM, Chan SK, Robinson DP, Dwyer DM, Nandan D, Foster LJ, et al. Proteomic analysis of the secretome of Leishmania donovani. Genome Biol. 2008;9(2):R35. doi: 10.1186/gb-2008-9-2-r35 18282296