1932

Abstract

Technological advances in mass spectrometry have enabled the extensive identification, characterization, and quantification of proteins in any biological system. In disease processes proteins are often altered in response to external stimuli; therefore, proteomics, the large-scale study of proteins and their functions, represents an invaluable tool for understanding the molecular basis of disease. This review highlights the use of mass spectrometry–based proteomics to study the pathogenesis, etiology, and pathology of several neglected tropical diseases (NTDs), a diverse group of disabling diseases primarily associated with poverty in tropical and subtropical regions of the world. While numerous NTDs have been the subject of proteomic studies, this review focuses on Buruli ulcer, dengue, leishmaniasis, and snakebite envenoming. The proteomic studies highlighted provide substantial information on the pathogenic mechanisms driving these diseases; they also identify molecular targets for drug discovery and development and uncover promising biomarkers that can assist in early diagnosis.

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2020-06-12
2024-06-21
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Literature Cited

  1. 1. 
    World Health Organ 2018. Neglected tropical diseases. https://www.who.int/neglected_diseases/diseases/en/
  2. 2. 
    Vos T, Abajobir AA, Abate KH, Abbafati C, Abbas KM et al. 2017. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet 390:1211–59
    [Google Scholar]
  3. 3. 
    Hotez P, Aksoy S. 2017. PLOS Neglected Tropical Diseases: ten years of progress in neglected tropical disease control and elimination…More or less. PLOS Negl. Trop. Dis. 11:e0005355
    [Google Scholar]
  4. 4. 
    Chippaux JP. 1998. Snake-bites: appraisal of the global situation. Bull. World Health Organ. 76:515–24
    [Google Scholar]
  5. 5. 
    Kasturiratne A, Wickremasinghe AR, de Silva N, Gunawardena NK, Pathmeswaran A et al. 2008. The global burden of snakebite: a literature analysis and modelling based on regional estimates of envenoming and deaths. PLOS Med 5:e218
    [Google Scholar]
  6. 6. 
    Gutiérrez JM, Calvete JJ, Habib AG, Harrison RA, Williams DJ, Warrell DA 2017. Snakebite envenoming. Nat. Rev. Dis. Primers 3:17063
    [Google Scholar]
  7. 7. 
    Molyneux DH, Savioli L, Engels D 2017. Neglected tropical diseases: progress towards addressing the chronic pandemic. Lancet 389:312–25
    [Google Scholar]
  8. 8. 
    World Health Organ 2019. Dracunculiasis (guinea-worm disease). Fact Sheet, World Health Organ., Geneva. https://www.who.int/en/news-room/fact-sheets/detail/dracunculiasis-(guinea-worm-disease)
  9. 9. 
    Molyneux D, Sankara DP. 2017. Guinea worm eradication: progress and challenges—should we beware of the dog. ? PLOS Negl. Trop. Dis. 11:e0005495
    [Google Scholar]
  10. 10. 
    Hotez PJ, Molyneux DH, Fenwick A, Kumaresan J, Sachs SE et al. 2007. Control of neglected tropical diseases. N. Eng. J. Med. 357:1018–27
    [Google Scholar]
  11. 11. 
    Liese B, Rosenberg M, Schratz A 2010. Programmes, partnerships, and governance for elimination and control of neglected tropical diseases. Lancet 375:67–76
    [Google Scholar]
  12. 12. 
    Reed SL, McKerrow JH. 2018. Why funding for neglected tropical diseases should be a global priority. Clin. Infect. Dis. 67:323–326
    [Google Scholar]
  13. 13. 
    Wes PD, Holtman IR, Boddeke EW, Möller T, Eggen BJ 2016. Next generation transcriptomics and genomics elucidate biological complexity of microglia in health and disease. Glia 64:197–213
    [Google Scholar]
  14. 14. 
    McCarthy MI, MacArthur DG. 2017. Human disease genomics: from variants to biology. Genome Biol 18:20
    [Google Scholar]
  15. 15. 
    Borrageiro G, Haylett W, Seedat S, Kuivaniemi H, Bardien S 2018. A review of genome‐wide transcriptomics studies in Parkinson's disease. Eur. J. Neurosci. 47:1–16
    [Google Scholar]
  16. 16. 
    Baltimore D. 2001. Our genome unveiled. Nature 409:814–16
    [Google Scholar]
  17. 17. 
    Gygi SP, Rochon Y, Franza BR, Aebersold R 1999. Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 19:1720–30
    [Google Scholar]
  18. 18. 
    Abuin G, Freitas-Junior LH, Colli W, Alves MJM, Schenkman S 1999. Expression of trans-sialidase and 85-kDa glycoprotein genes in Trypanosoma cruzi is differentially regulated at the post-transcriptional level by labile protein factors. J. Biol. Chem. 274:13041–47
    [Google Scholar]
  19. 19. 
    Elias MCQ, Marques-Porto R, Freymüller E, Schenkman S 2001. Transcription rate modulation through the Trypanosoma cruzi life cycle occurs in parallel with changes in nuclear organisation. Mol. Biochem. Parasitol. 112:79–90
    [Google Scholar]
  20. 20. 
    Jensen LJ, Gupta R, Blom N, Devos D, Tamames J et al. 2002. Prediction of human protein function from post-translational modifications and localization features. J. Mol. Biol. 319:1257–65
    [Google Scholar]
  21. 21. 
    Hanash S. 2003. Disease proteomics. Nature 422:226–32
    [Google Scholar]
  22. 22. 
    Marko-Varga G, Fehniger TE. 2004. Proteomics and disease—the challenges for technology and discovery. J. Proteome Res. 3:167–78
    [Google Scholar]
  23. 23. 
    Kavallaris M, Marshall GM. 2005. Proteomics and disease: opportunities and challenges. Med. J. Aust. 182:575–79
    [Google Scholar]
  24. 24. 
    Issaq HJ, Veenstra TD. 2008. Two-dimensional polyacrylamide gel electrophoresis (2D-PAGE): advances and perspectives. Biotechniques 44:697–700
    [Google Scholar]
  25. 25. 
    Washburn MP, Wolters D, Yates JR 3rd 2001. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19:242–47
    [Google Scholar]
  26. 26. 
    Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM 1989. Electrospray ionization for mass spectrometry of large biomolecules. Science 246:64–71
    [Google Scholar]
  27. 27. 
    Hillenkamp F, Karas M, Beavis RC, Chait BT 1991. Matrix-assisted laser desorption/ionization mass spectrometry of biopolymers. Anal. Chem. 63:1193A–1203A
    [Google Scholar]
  28. 28. 
    Zhang Y, Fonslow BR, Shan B, Baek MC, Yates JR 3rd 2013. Protein analysis by shotgun/bottom-up proteomics. Chem. Rev. 113:2343–94
    [Google Scholar]
  29. 29. 
    Toby TK, Fornelli L, Kelleher NL 2016. Progress in top-down proteomics and the analysis of proteoforms. Annu. Rev. Anal. Chem. 9:499–519
    [Google Scholar]
  30. 30. 
    Siuti N, Kelleher NL. 2007. Decoding protein modifications using top-down mass spectrometry. Nat. Methods 4:817–21
    [Google Scholar]
  31. 31. 
    McDonald WH, Yates JR. 2002. Shotgun proteomics and biomarker discovery. Dis. Markers 18:99–105
    [Google Scholar]
  32. 32. 
    Schiess R, Wollscheid B, Aebersold R 2009. Targeted proteomic strategy for clinical biomarker discovery. Mol. Oncol. 3:33–44
    [Google Scholar]
  33. 33. 
    Geyer PE, Holdt LM, Teupser D, Mann M 2017. Revisiting biomarker discovery by plasma proteomics. Mol. Syst. Biol. 13:942
    [Google Scholar]
  34. 34. 
    Brady OJ, Gething PW, Bhatt S, Messina JP, Brownstein JS et al. 2012. Refining the global spatial limits of dengue virus transmission by evidence-based consensus. PLOS Negl. Trop. Dis. 6:1760
    [Google Scholar]
  35. 35. 
    Normile D. 2013. Surprising new dengue virus throws a spanner in disease control efforts. Science 342:415
    [Google Scholar]
  36. 36. 
    Mustafa MS, Rasotgi V, Jain S, Gupta V 2015. Discovery of fifth serotype of dengue virus (DENV-5): a new public health dilemma in dengue control. Med. J. Armed Forces India 71:67–70
    [Google Scholar]
  37. 37. 
    Rodenhuis-Zybert IA, Wilschut J, Smit JM 2010. Dengue virus life cycle: viral and host factors modulating infectivity. Cell. Mol. Life Sci. 67:2773–86
    [Google Scholar]
  38. 38. 
    Simmons CP, Farrar JJ, van Vinh Chau N, Wills B 2012. Dengue. N. Engl. J. Med. 366:1423–32
    [Google Scholar]
  39. 39. 
    World Health Organ 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control Geneva: WHO/TDR https://www.who.int/tdr/publications/documents/dengue-diagnosis.pdf
    [Google Scholar]
  40. 40. 
    Halstead SB. 1970. Observations related to pathogensis of dengue hemorrhagic fever. VI. Hypotheses and discussion. Yale J. Biol. Med. 42:350–62
    [Google Scholar]
  41. 41. 
    Burke DS, Nisalak A, Johnson DE, Scott RM 1988. A prospective study of dengue infections in Bangkok. Am. J. Trop. Med. Hyg. 38:172–80
    [Google Scholar]
  42. 42. 
    Guzmán MG, Kouri G, Bravo J, Valdes L, Susana V, Halstead SB 2002. Effect of age on outcome of secondary dengue 2 infections. Int. J. Infect. Dis. 6:118–24
    [Google Scholar]
  43. 43. 
    Recker M, Blyuss KB, Simmons CP, Hien TT, Wills B et al. 2009. Immunological serotype interactions and their effect on the epidemiological pattern of dengue. Proc. R. Soc. B. 276:2541–48
    [Google Scholar]
  44. 44. 
    Thein S, Aung MM, Shwe TN, Aye M, Zaw A et al. 1997. Risk factors in dengue shock syndrome. Am. J. Trop. Med. Hyg. 56:566–72
    [Google Scholar]
  45. 45. 
    Kuno G, Chang GJJ, Tsuchiya KR, Karabatsos N, Cropp CB 1998. Phylogeny of the genus Flavivirus. J. Virol 72:73–83
    [Google Scholar]
  46. 46. 
    Deubel V, Kinney RM, Trent DW 1988. Nucleotide sequence and deduced amino acid sequence of the nonstructural proteins of dengue type 2 virus, Jamaica genotype: comparative analysis of the full-length genome. Virology 165:234–44
    [Google Scholar]
  47. 47. 
    Perera R, Kuhn RJ. 2008. Structural proteomics of dengue virus. Curr. Opin. Microbiol. 11:369–77
    [Google Scholar]
  48. 48. 
    Dwivedi VD, Tripathi IP, Tripathi RC, Bharadwaj S, Mishra SK 2017. Genomics, proteomics and evolution of dengue virus. Brief. Funct. Genom. 16:217–27
    [Google Scholar]
  49. 49. 
    Clyde K, Kyle JL, Harris E 2006. Recent advances in deciphering viral and host determinants of dengue virus replication and pathogenesis. J. Virol. 80:11418–31
    [Google Scholar]
  50. 50. 
    Patramool S, Surasombatpattana P, Luplertlop N, Sévéno M, Choumet V et al. 2011. Proteomic analysis of an Aedes albopictus cell line infected with Dengue serotypes 1 and 3 viruses. Parasit. Vectors 4:138
    [Google Scholar]
  51. 51. 
    Tchankouo-Nguetcheu S, Khun H, Pincet L, Roux P, Bahut M et al. 2010. Differential protein modulation in midguts of Aedes aegypti infected with chikungunya and dengue 2 viruses. PLOS ONE 5:13149
    [Google Scholar]
  52. 52. 
    Chisenhall DM, Londono BL, Christofferson RC, McCracken MK, Mores CN 2014. Effect of dengue-2 virus infection on protein expression in the salivary glands of Aedes aegypti mosquitoes. Am. J. Trop. Med. Hyg. 90:431–37
    [Google Scholar]
  53. 53. 
    Zhang M, Zheng X, Wu Y, Gan M, He A et al. 2013. Differential proteomics of Aedes albopictus salivary gland, midgut and C6/36 cell induced by dengue virus infection. Virology 444:109–18
    [Google Scholar]
  54. 54. 
    Seneviratne SL, Malavige GN, De Silva HJ 2006. Pathogenesis of liver involvement during dengue viral infections. Trans. R. Soc. Trop. Med. Hyg. 100:608–14
    [Google Scholar]
  55. 55. 
    Paes MV, Lenzi HL, Nogueira ACM, Nuovo GJ, Pinhão AT et al. 2009. Hepatic damage associated with dengue-2 virus replication in liver cells of BALB/c mice. Lab. Investig. 89:1140–51
    [Google Scholar]
  56. 56. 
    Póvoa TF, Alves AM, Oliveira CA, Nuovo GJ, Chagas VL, Paes MV 2014. The pathology of severe dengue in multiple organs of human fatal cases: histopathology, ultrastructure and virus replication. PLOS ONE 9:e83386
    [Google Scholar]
  57. 57. 
    Pattanakitsakul SN, Rungrojcharoenkit K, Kanlaya R, Sinchaikul S, Noisakran S et al. 2007. Proteomic analysis of host responses in HepG2 cells during dengue virus infection. J. Proteome Res. 6:4592–600
    [Google Scholar]
  58. 58. 
    Higa LM, Caruso MB, Canellas F, Soares MR, Oliveira-Carvalho AL et al. 2008. Secretome of HepG2 cells infected with dengue virus: implications for pathogenesis. Biochim. Biophys. Acta Proteins Proteom. 1784:1607–16
    [Google Scholar]
  59. 59. 
    Strongin AY, Collier I, Bannikov G, Marmer BL, Grant GA, Goldberg GI 1995. Mechanism of cell surface activation of 72-kDa type IV collagenase isolation of the activated form of the membrane metalloprotease. J. Biol. Chem. 270:5331–38
    [Google Scholar]
  60. 60. 
    Caruso MB, Trugilho MR, Higa LM, Teixeira-Ferreira AS, Perales J et al. 2017. Proteomic analysis of the secretome of HepG2 cells indicates differential proteolytic processing after infection with dengue virus. J. Proteom. 151:106–13
    [Google Scholar]
  61. 61. 
    Kanlaya R, Pattanakitsakul SN, Sinchaikul S, Chen ST, Thongboonkerd V 2009. Alterations in actin cytoskeletal assembly and junctional protein complexes in human endothelial cells induced by dengue virus infection and mimicry of leukocyte transendothelial migration. J. Proteome Res. 8:2551–62
    [Google Scholar]
  62. 62. 
    Mourão MP, Lacerda MV, Macedo VO, Santos JB 2007. Thrombocytopenia in patients with dengue virus infection in the Brazilian Amazon. Platelets 18:605–12
    [Google Scholar]
  63. 63. 
    de Oliveira Trugilho MR, Hottz ED, Brunoro GVF, Teixeira-Ferreira A, Carvalho PC et al. 2017. Platelet proteome reveals novel pathways of platelet activation and platelet-mediated immunoregulation in dengue. PLOS Pathog 13:e1006385
    [Google Scholar]
  64. 64. 
    Wati S, Soo ML, Zilm P, Li P, Paton AW et al. 2009. Dengue virus infection induces upregulation of GRP78, which acts to chaperone viral antigen production. J. Virol. 83:12871–80
    [Google Scholar]
  65. 65. 
    Chiu HC, Hannemann H, Heesom KJ, Matthews DA, Davidson AD 2014. High-throughput quantitative proteomic analysis of dengue virus type 2 infected A549 cells. PLOS ONE 9:e93305
    [Google Scholar]
  66. 66. 
    Thayan R, Huat TL, See LLC, Tan CPL, Khairullah NS et al. 2009. The use of two-dimension electrophoresis to identify serum biomarkers from patients with dengue haemorrhagic fever. Trans. R. Soc. Trop. Med. Hyg. 103:413–19
    [Google Scholar]
  67. 67. 
    Albuquerque LM, Trugilho MR, Chapeaurouge A, Jurgilas PB, Bozza PT et al. 2009. Two-dimensional difference gel electrophoresis (DiGE) analysis of plasmas from dengue fever patients. J. Proteome Res. 8:5431–41
    [Google Scholar]
  68. 68. 
    Fragnoud R, Yugueros-Marcos J, Pachot A, Bedin F 2012. Isotope Coded Protein Labeling analysis of plasma specimens from acute severe dengue fever patients. Proteome Sci 10:60
    [Google Scholar]
  69. 69. 
    Kumar Y, Liang C, Bo Z, Rajapakse JC, Ooi EE, Tannenbaum SR. 2012. Serum proteome and cytokine analysis in a longitudinal cohort of adults with primary dengue infection reveals predictive markers of DHF. PLOS Negl. Trop. Dis. 6:e1887
    [Google Scholar]
  70. 70. 
    Fragnoud R, Flamand M, Reynier F, Buchy P, Duong V et al. 2015. Differential proteomic analysis of virus-enriched fractions obtained from plasma pools of patients with dengue fever or severe dengue. BMC Infect. Dis. 15:518
    [Google Scholar]
  71. 71. 
    Ray S, Srivastava R, Tripathi K, Vaibhav V, Patankar S, Srivastava S 2012. Serum proteome changes in dengue virus-infected patients from a dengue-endemic area of India: Towards new molecular targets?. OMICS 16:527–36
    [Google Scholar]
  72. 72. 
    Brasier AR, Garcia J, Wiktorowicz JE, Spratt HM, Comach G et al. 2012. Discovery proteomics and nonparametric modeling pipeline in the development of a candidate biomarker panel for dengue hemorrhagic fever. Clin. Transl. Sci. 5:8–20
    [Google Scholar]
  73. 73. 
    Nhi DM, Huy NT, Ohyama K, Kimura D, Lan NTP et al. 2016. A proteomic approach identifies candidate early biomarkers to predict severe dengue in children. PLOS Negl. Trop. Dis. 10:e0004435
    [Google Scholar]
  74. 74. 
    Vieira de Morais CG, Lima AKC, Terra R, dos Santos RF, Da-Silva SAG, Dutra PML 2015. The dialogue of the host-parasite relationship: Leishmania spp. and Trypanosoma cruzi infection. Biomed. Res. Int. 2015:324915
    [Google Scholar]
  75. 75. 
    World Health Organ 2019. Leishmaniasis. Fact Sheet, World Health Organ., Geneva. https://www.who.int/news-room/fact-sheets/detail/leishmaniasis
  76. 76. 
    Goto H, Angelo J, Lindoso L 2012. Cutaneous and mucocutaneous leishmaniasis. Infect. Dis. Clin. 26:293–307
    [Google Scholar]
  77. 77. 
    McCall LI, Zhang WW, Matlashewski G 2013. Determinants for the development of visceral leishmaniasis disease. PLOS Pathog 9:e1003053
    [Google Scholar]
  78. 78. 
    Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P et al. 2012. Leishmaniasis worldwide and global estimates of its incidence. PLOS ONE 7:e35671
    [Google Scholar]
  79. 79. 
    Leifso K, Cohen-Freue G, Dogra N, Murray A, McMaster WR 2007. Genomic and proteomic expression analysis of Leishmania promastigote and amastigote life stages: the Leishmania genome is constitutively expressed. Mol. Biochem. Parasitol. 152:35–46
    [Google Scholar]
  80. 80. 
    Reithinger R, Dujardin J-C, Louzir H, Pirmez C, Alexander B, Brooker S 2007. Cutaneous leishmaniasis. Lancet 7:581–96
    [Google Scholar]
  81. 81. 
    Croft SL, Sundar S, Fairlamb AH 2006. Drug resistance in leishmaniasis. Clin. Microbiol. 19:111–26
    [Google Scholar]
  82. 82. 
    Ortega V, Giorgio S, de Paula E 2017. Liposomal formulations in the pharmacological treatment of leishmaniasis: a review. J. Liposome Res. 27:234–48
    [Google Scholar]
  83. 83. 
    Handman E, Mitchell GF, Goding JW 1981. Identification and characterization of protein antigens of Leishmania tropica isolates. J. Immunol. 126:508–12
    [Google Scholar]
  84. 84. 
    Handman E, Hocking RE, Mitchell GF, Spithill TW 1983. Isolation and characterization of infective and non-infective clones of Leishmania tropica. Mol. Biochem. . Parasitol 7:111–26
    [Google Scholar]
  85. 85. 
    Saravia NG, Gemmell MA, Nance SL, Anderson NL 1984. Two-dimensional electrophoresis used to differentiate the causal agents of American tegumentary leishmaniasis. Clin. Chem. 30:2048–52
    [Google Scholar]
  86. 86. 
    de Jesus JB, Mesquita-Rodrigues C, Cuervo P 2014. Proteomics advances in the study of Leishmania parasites and Leishmaniasis. Proteins and Proteomics of Leishmania and Trypanosoma. Subcellular Biochemistry A Santos, M Branquinha, C D'Avila-Levy, L Kneipp, C Sodré 323–49 Amsterdam: Springer
    [Google Scholar]
  87. 87. 
    Nugent PG, Karsani SA, Wait R, Tempero J, Smith DF 2004. Proteomic analysis of Leishmania mexicana differentiation. Mol. Biochem. Parasitol. 136:51–62
    [Google Scholar]
  88. 88. 
    El Fakhry Y, Ouellette M, Papadopoulou B 2002. A proteomic approach to identify developmentally regulated proteins in Leishmania infantum. . Proteomics 2:1007–17
    [Google Scholar]
  89. 89. 
    Walker J, Gongora R, Vasquez JJ, Drummelsmith J, Burchmore R et al. 2012. Discovery of factors linked to antimony resistance in Leishmania panamensis through differential proteome analysis. Mol. Biochem. Parasitol. 183:166–76
    [Google Scholar]
  90. 90. 
    Lynn MA, Marr AK, McMaster WR 2013. Differential quantitative proteomic profiling of Leishmania infantum and Leishmania mexicana density gradient separated membranous fractions. J. Proteom. 82:179–92
    [Google Scholar]
  91. 91. 
    Lima BSS, Fialho LC, Pires SF, Tafuri WL, Andrade HM 2016. Immunoproteomic and bioinformatic approaches to identify secreted Leishmania amazonensis, L. braziliensis, and L. infantum proteins with specific reactivity using canine serum. Vet. Parasitol. 223:115–19
    [Google Scholar]
  92. 92. 
    de Souza Moreira D, Pescher P, Laurent C, Lenormand P, Späth GF, Murta SMF 2015. Phosphoproteomic analysis of wild-type and antimony-resistant Leishmania braziliensis lines by 2D-DIGE technology. Proteomics 15:2999–3019
    [Google Scholar]
  93. 93. 
    de Oliveira AHC, Ruiz JC, Cruz AK, Greene LJ, Rosa JC, Ward RJ 2006. Subproteomic analysis of soluble proteins of the microsomal fraction from two Leishmania species. Comp. Biochem. Physiol. D. Genom. Proteom. 1:300–8
    [Google Scholar]
  94. 94. 
    Lascu L, Giartosio A, Ransac S, Erent M 2002. Quaternary structure of nucleoside diphosphate kinases. J. Bioenerg. Biomembr. 32:227–36
    [Google Scholar]
  95. 95. 
    Drummelsmith J, Girard I, Trudel N, Ouellette M 2004. Differential protein expression analysis of Leishmania major reveals novel roles for methionine adenosyltransferase and S-adenosylmethionine in methotrexate resistance. J. Biol. Chem. 279:33273–80
    [Google Scholar]
  96. 96. 
    Marchini JFM, Cruz AK, Beverley SM, Tosi LRO 2003. The H region HTBF gene mediates terbinafine resistance in Leishmania major. Mol. Biochem. . Parasitol 131:77–81
    [Google Scholar]
  97. 97. 
    Beattie L, D'El-Rei Hermida M, Moore JWJ, Maroof A, Brown N et al. 2013. A transcriptomic network identified in uninfected macrophages responding to inflammation controls intracellular pathogen survival. Cell Host Microbe 14:357–68
    [Google Scholar]
  98. 98. 
    Rabhi I, Rabhi S, Ben-Othman R, Rasche A, Daskalaki A et al. 2012. Transcriptomic signature of Leishmania infected mice macrophages: a metabolic point of view. PLOS Negl. Trop. Dis. 6:1763
    [Google Scholar]
  99. 99. 
    Menezes JPB, Almeida TF, Petersen ALOA, Guedes CES, Mota MSV et al. 2013. Proteomic analysis reveals differentially expressed proteins in macrophages infected with Leishmania amazonensis or Leishmania major. . Microbes Infect 15:579–91
    [Google Scholar]
  100. 100. 
    Singh AK, Pandey RK, Siqueira-Neto JL, Kwon YJ, Freitas-Junior LH et al. 2015. Proteomic-based approach to gain insight into reprogramming of THP-1 cells exposed to Leishmania donovani over an early temporal window. Infect. Immun. 83:1853–68
    [Google Scholar]
  101. 101. 
    Wang L, Cummings R, Usatyuk P, Morris A, Irani K, Natarajan V 2002. Involvement of phospholipases D1 and D2 in sphingosine 1-phosphate-induced ERK (extracellular-signal-regulated kinase) activation and interleukin-8 secretion in human bronchial epithelial cells. Biochem. J. 367:751–60
    [Google Scholar]
  102. 102. 
    Corrotte M, Chasserot-Golaz S, Huang P, Du G, Ktistakis NT et al. 2006. Dynamics and function of phospholipase D and phosphatidic acid during phagocytosis. Traffic 7:365–77
    [Google Scholar]
  103. 103. 
    Isnard A, Christian JG, Kodiha M, Stochaj U, McMaster WR, Olivier M 2015. Impact of Leishmania infection on host macrophage nuclear physiology and nucleopore complex integrity. PLOS Pathog 11:e1004776
    [Google Scholar]
  104. 104. 
    Negrão F, Fernandez-Costa C, Zorgi N, Giorgio S, Eberlin MN, Yates JR 3rd 2019. Label-free proteomic analysis reveals parasite-specific protein alterations in macrophages following Leishmania amazonensis, Leishmania major or Leishmania infantum infection. ACS Infect. Dis. 14:851–62
    [Google Scholar]
  105. 105. 
    Kuroda M, Fujikura D, Nanbo A, Marzi A, Noyori O et al. 2015. Interaction between TIM-1 and NPC1 is important for cellular entry of Ebola virus. J. Virol. 89:6481–93
    [Google Scholar]
  106. 106. 
    Negrão F, Giorgio S, Eberlin MN, Yates JR 2019. Comparative proteomic analysis of murine cutaneous lesions induced by Leishmania amazonensis or Leishmania major. ACS Infect. Dis 5:1295–1305
    [Google Scholar]
  107. 107. 
    MacCallum P, Tolhurst JC, Buckle G, Sissons HA 1948. A new mycobacterial infection in man. J. Pathol. 60:93–122
    [Google Scholar]
  108. 108. 
    van der Werf TS, van der Graaf WT, Tappero JW, Asiedu K 1999. Mycobacterium ulcerans infection. Lancet 354:1013–18
    [Google Scholar]
  109. 109. 
    World Health Organ 2019. Buruli ulcer (Mycobacterium ulcerans infection). Fact Sheet, World Health Organ., Geneva. https://www.who.int/en/news-room/fact-sheets/detail/buruli-ulcer-(mycobacterium-ulcerans-infection)
  110. 110. 
    Wansbrough-Jones M, Phillips R. 2006. Buruli ulcer: emerging from obscurity. Lancet 367:1849–58
    [Google Scholar]
  111. 111. 
    Marsollier L, Stinear T, Aubry J, Saint André JP, Robert R et al. 2004. Aquatic plants stimulate the growth of and biofilm formation by Mycobacterium ulcerans in axenic culture and harbor these bacteria in the environment. Appl. Environ. Microbiol. 70:1097–103
    [Google Scholar]
  112. 112. 
    Marsollier L, Aubry J, Coutanceau E, André JPS, Small PL et al. 2005. Colonization of the salivary glands of Naucoris cimicoides by Mycobacterium ulcerans requires host plasmatocytes and a macrolide toxin, mycolactone. Cell. Microbiol. 7:935–43
    [Google Scholar]
  113. 113. 
    Etuaful S, Carbonnelle B, Grosset J, Lucas S, Horsfield C et al. 2005. Efficacy of the combination rifampin-streptomycin in preventing growth of Mycobacterium ulcerans in early lesions of Buruli ulcer in humans. Antimicrob. Agents Chemother. 49:3182–86
    [Google Scholar]
  114. 114. 
    George KM, Chatterjee D, Gunawardana G, Welty D, Hayman J et al. 1999. Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence. Science 283:854–57
    [Google Scholar]
  115. 115. 
    George KM, Pascopella L, Welty DM, Small PL 2000. A Mycobacterium ulcerans toxin, mycolactone, causes apoptosis in guinea pig ulcers and tissue culture cells. Infect. Immun. 68:877–83
    [Google Scholar]
  116. 116. 
    Mve-Obiang A, Lee RE, Portaels F, Small PLC 2003. Heterogeneity of mycolactones produced by clinical isolates of Mycobacterium ulcerans: implications for virulence. Infect. Immun. 71:774–83
    [Google Scholar]
  117. 117. 
    Tafelmeyer P, Laurent C, Lenormand P, Rousselle JC, Marsollier L et al. 2008. Comprehensive proteome analysis of Mycobacterium ulcerans and quantitative comparison of mycolactone biosynthesis. Proteomics 8:3124–38
    [Google Scholar]
  118. 118. 
    Marsollier L, Brodin P, Jackson M, Korduláková J, Tafelmeyer P et al. 2007. Impact of Mycobacterium ulcerans biofilm on transmissibility to ecological niches and Buruli ulcer pathogenesis. PLOS Pathog 3:e62
    [Google Scholar]
  119. 119. 
    Gama JB, Ohlmeier S, Martins TG, Fraga AG, Sampaio-Marques B et al. 2014. Proteomic analysis of the action of the Mycobacterium ulcerans toxin mycolactone: targeting host cells cytoskeleton and collagen. PLOS Negl. Trop. Dis. 8:e3066
    [Google Scholar]
  120. 120. 
    Krieg RE, Hockmeyer WT, Connor DH 1974. Toxin of Mycobacterium ulcerans. Production and effects in guinea pig skin. Arch. Dermatol. 110:783–88
    [Google Scholar]
  121. 121. 
    George KM, Barker LP, Welty DM, Small PL 1998. Partial purification and characterization of biological effects of a lipid toxin produced by Mycobacterium ulcerans. Infect. . Immun 66:587–93
    [Google Scholar]
  122. 122. 
    Chippaux JP. 2017. Snakebite envenomation turns again into a neglected tropical disease. ! J. Venom. Anim. Toxins 23:38
    [Google Scholar]
  123. 123. 
    Harrison RA, Hargreaves A, Wagstaff SC, Faragher B, Lalloo DG 2009. Snake envenoming: a disease of poverty. PLOS Negl. Trop. Dis. 3:e569
    [Google Scholar]
  124. 124. 
    Warrell DA. 2010. Snake bite. Lancet 375:77–88
    [Google Scholar]
  125. 125. 
    Mackessy SP. 2010. The field of reptile toxinology: snakes, lizards, and their venoms. Handbook of Venoms and Toxins of Reptiles SP Mackessy 323. Boca Raton, FL: CRC Press
    [Google Scholar]
  126. 126. 
    Pyron RA, Burbrink FT, Wiens JJ 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 13:93
    [Google Scholar]
  127. 127. 
    Calvete JJ, Juárez P, Sanz L 2007. Snake venomics. Strategy and applications. J. Mass Spectrom. 42:1405–14
    [Google Scholar]
  128. 128. 
    Calvete JJ, Sanz L, Angulo Y, Lomonte B, Gutiérrez JM 2009. Venoms, venomics, antivenomics. FEBS Lett 583:1736–43
    [Google Scholar]
  129. 129. 
    Sanz L, Gibbs HL, Mackessy SP, Calvete JJ 2006. Venom proteomes of closely related Sistrurus rattlesnakes with divergent diets. J. Proteome Res. 5:2098–12
    [Google Scholar]
  130. 130. 
    Lomonte B, Tsai WC, Ureña-Diaz JM, Sanz L, Mora-Obando D et al. 2014. Venomics of New World pit vipers: genus-wide comparisons of venom proteomes across Agkistrodon. J. . Proteom 96:103–16
    [Google Scholar]
  131. 131. 
    Alape-Girón A, Sanz L, Escolano J, Flores-Diaz M, Madrigal M et al. 2008. Snake venomics of the lancehead pitviper Bothrops asper: geographic, individual, and ontogenetic variations. J. Proteome Res. 7:3556–71
    [Google Scholar]
  132. 132. 
    Saviola AJ, Pla D, Sanz L, Castoe TA, Calvete JJ, Mackessy SP 2015. Comparative venomics of the Prairie Rattlesnake (Crotalus viridis viridis) from Colorado: identification of a novel pattern of ontogenetic changes in venom composition and assessment of the immunoreactivity of the commercial antivenom CroFab®. J. Proteom. 121:28–43
    [Google Scholar]
  133. 133. 
    Pla D, Petras D, Saviola AJ, Modahl CM, Sanz L et al. 2018. Transcriptomics-guided bottom-up and top-down venomics of neonate and adult specimens of the arboreal rear-fanged Brown Treesnake, Boiga irregularis, from Guam. J. Proteom. 174:71–84
    [Google Scholar]
  134. 134. 
    Massey DJ, Calvete JJ, Sánchez EE, Sanz L, Richards K et al. 2012. Venom variability and envenoming severity outcomes of the Crotalus scutulatus scutulatus (Mojave rattlesnake) from Southern Arizona. J. Proteom. 75:2576–87
    [Google Scholar]
  135. 135. 
    Lomonte B, Sasa M, Rey-Suárez P, Bryan W, Gutiérrez JM 2016. Venom of the coral snake Micrurus clarki: proteomic profile, toxicity, immunological cross-neutralization, and characterization of a three-finger toxin. Toxins 8:138
    [Google Scholar]
  136. 136. 
    McGivern JJ, Wray KP, Margres MJ, Couch ME, Mackessy SP, Rokyta DR 2014. RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes. BMC Genom 15:1061
    [Google Scholar]
  137. 137. 
    Modahl CM, Frietze S, Mackessy SP 2018. Transcriptome-facilitated proteomic characterization of rear-fanged snake venoms reveal abundant metalloproteinases with enhanced activity. J. Proteom. 187:223–34
    [Google Scholar]
  138. 138. 
    Gutiérrez JM, Lomonte B, León G, Rucavado A, Chaves F, Angulo Y 2007. Trends in snakebite envenomation therapy: scientific, technological and public health considerations. Curr. Pharm. Des. 13:2935–50
    [Google Scholar]
  139. 139. 
    Weinstein SA, Warrell DA, White J, Keyler DE 2011. “Venomous” Bites from Non-Venomous Snakes: A Critical Analysis of Risk and Management of “Colubrid” Snake Bites London: Elsevier
    [Google Scholar]
  140. 140. 
    Rucavado A, Escalante T, Shannon J, Gutiérrez JM, Fox JW 2011. Proteomics of wound exudate in snake venom-induced pathology: search for biomarkers to assess tissue damage and therapeutic success. J. Proteome Res. 10:1987–2005
    [Google Scholar]
  141. 141. 
    Rucavado A, Nicolau C, Escalante T, Kim J, Herrera C et al. 2016. Viperid envenomation wound exudate contributes to increased vascular permeability via a DAMPs/TLR-4 mediated pathway. Toxins 8:349
    [Google Scholar]
  142. 142. 
    Escalante T, Rucavado A, Pinto AF, Terra RM, Gutiérrez JM, Fox JW 2009. Wound exudate as a proteomic window to reveal different mechanisms of tissue damage by snake venom toxins. J. Proteome Res. 8:5120–31
    [Google Scholar]
  143. 143. 
    Macêdo JK, Joseph JK, Menon J, Escalante T, Rucavado A et al. 2019. Proteomic analysis of human blister fluids following envenomation by three snake species in India: differential markers for venom mechanisms of action. Toxins 11:246
    [Google Scholar]
  144. 144. 
    Rucavado A, Escalante T, Shannon JD, Ayala-Castro CN, Villalta M et al. 2011. Efficacy of IgG and F (ab′)2 antivenoms to neutralize snake venom-induced local tissue damage as assessed by the proteomic analysis of wound exudate. J. Proteome Res. 11:292–305
    [Google Scholar]
  145. 145. 
    Pla D, Gutiérrez JM, Calvete JJ 2012. Second generation snake antivenomics: comparing immunoaffinity and immunodepletion protocols. Toxicon 60:688–99
    [Google Scholar]
  146. 146. 
    Pla D, Rodríguez Calvete J 2017. Third generation antivenomics: pushing the limits of the in vitro preclinical assessment of antivenoms. Toxins 9:158
    [Google Scholar]
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