In Vitro, In Vivo and In Silico Assessment of the Antimicrobial and Immunomodulatory Effects of a Water Buffalo Cathelicidin (WBCATH) in Experimental Pulmonary Tuberculosis (original) (raw)

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References (55)

  1. World Health Organization. Global Tuberculosis Report 2021; World Health Organization: Geneva, Switzerland, 2021.
  2. Bini, E.; Hernandez-Pando, R. New Chemotherapy and Immunotherapy for Tuberculosis. Curr. Respir. Med. Rev. 2014, 10, 74-87.
  3. Estrada García, I.; Hernández Pando, R.; Ivanyi, J. Editorial: Advances in Immunotherapeutic Approaches to Tuberculosis. Front. Immunol. 2021, 12, 684200. [CrossRef] [PubMed]
  4. Glaziou, P.; Floyd, K.; Raviglione, M.C. Global Epidemiology of Tuberculosis. Semin. Respir. Crit. Care Med. 2018, 39, 271-285. [CrossRef] [PubMed]
  5. Mondoni, M.; Saderi, L.; Sotgiu, G. Novel treatments in multidrug-resistant tuberculosis. Curr. Opin. Pharmacol. 2021, 59, 103-115.
  6. Rivas-Santiago, B.; Sada, E.; Tsutsumi, V.; Aguilar-Leon, D.; Contreras, J.L.; Hernandez-Pando, R. beta-Defensin gene expression during the course of experimental tuberculosis infection. J. Infect. Dis. 2006, 194, 697-701. [CrossRef]
  7. Castañeda-Delgado, J.; Hernández-Pando, R.; Serrano, C.J.; Aguilar-León, D.; León-Contreras, J.; Rivas-Santiago, C.; Méndez, R.; González-Curiel, I.; Enciso-Moreno, A.; Rivas-Santiago, B. Kinetics and cellular sources of cathelicidin during the course of experimental latent tuberculous infection and progressive pulmonary tuberculosis. Clin. Exp. Immunol. 2010, 161, 542-550.
  8. Lai, Y.; Gallo, R.L. AMPed up immunity: How antimicrobial peptides have multiple roles in immune defense. Trends Immunol. 2009, 30, 131-141. [CrossRef] [PubMed]
  9. Pachón-Ibáñez, M.E.; Smani, Y.; Pachón, J.; Sánchez-Céspedes, J. Perspectives for clinical use of engineered human host defense antimicrobial peptides. FEMS Microbiol. Rev. 2017, 41, 323-342. [CrossRef] [PubMed]
  10. Ramos-Espinosa, O.; Islas-Weinstein, L.; Peralta-Álvarez, M.P.; López-Torres, M.O.; Hernández-Pando, R. The use of immunother- apy for the treatment of tuberculosis. Expert Rev. Respir. Med. 2018, 12, 427-440. [CrossRef]
  11. Bals, R.; Wilson, J.M. Cathelicidins-A family of multifunctional antimicrobial peptides. Cell. Mol. Life Sci. CMLS 2003, 60, 711-720. [CrossRef]
  12. Tomasinsig, L.; Zanetti, M. The cathelicidins-structure, function and evolution. Curr. Protein Pept. Sci. 2005, 6, 23-34. [CrossRef] [PubMed]
  13. Henzler Wildman, K.A.; Lee, D.K.; Ramamoorthy, A. Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37. Biochemistry 2003, 42, 6545-6558. [CrossRef] [PubMed]
  14. Subbalakshmi, C.; Sitaram, N. Mechanism of antimicrobial action of indolicidin. FEMS Microbiol. Lett. 1998, 160, 91-96. [CrossRef]
  15. Agerberth, B.; Charo, J.; Werr, J.; Olsson, B.; Idali, F.; Lindbom, L.; Kiessling, R.; Jörnvall, H.; Wigzell, H.; Gudmundsson, G.H. The human antimicrobial and chemotactic peptides LL-37 and alpha-defensins are expressed by specific lymphocyte and monocyte populations. Blood 2000, 96, 3086-3093. [CrossRef] [PubMed]
  16. Niyonsaba, F.; Hirata, M.; Ogawa, H.; Nagaoka, I. Epithelial cell-derived antibacterial peptides human beta-defensins and cathelicidin: Multifunctional activities on mast cells. Curr. Drug Targets Inflamm. Allergy 2003, 2, 224-231. [CrossRef]
  17. Zaiou, M.; Gallo, R.L. Cathelicidins, essential gene-encoded mammalian antibiotics. J. Mol. Med. 2002, 80, 549-561. [CrossRef]
  18. Gennaro, R.; Zanetti, M. Structural features and biological activities of the cathelicidin-derived antimicrobial peptides. Biopolymers 2000, 55, 31-49. [CrossRef]
  19. Zhao, C.; Nguyen, T.; Boo, L.M.; Hong, T.; Espiritu, C.; Orlov, D.; Wang, W.; Waring, A.; Lehrer, R.I. RL-37, an alpha-helical antimicrobial peptide of the rhesus monkey. Antimicrob. Agents Chemother. 2001, 45, 2695-2702. [CrossRef]
  20. Bals, R.; Lang, C.; Weiner, D.J.; Vogelmeier, C.; Welsch, U.; Wilson, J.M. Rhesus monkey (Macaca mulatta) mucosal antimicrobial peptides are close homologues of human molecules. Clin. Diagn. Lab. Immunol. 2001, 8, 370-375. [CrossRef]
  21. Scocchi, M.; Wang, S.; Zanetti, M. Structural organization of the bovine cathelicidin gene family and identification of a novel member. FEBS Lett. 1997, 417, 311-315. [CrossRef]
  22. Shamova, O.; Brogden, K.A.; Zhao, C.; Nguyen, T.; Kokryakov, V.N.; Lehrer, R.I. Purification and properties of proline-rich antimicrobial peptides from sheep and goat leukocytes. Infect. Immun. 1999, 67, 4106-4111. [CrossRef] [PubMed]
  23. Skerlavaj, B.; Scocchi, M.; Gennaro, R.; Risso, A.; Zanetti, M. Structural and functional analysis of horse cathelicidin peptides. Antimicrob. Agents Chemother. 2001, 45, 715-722. [CrossRef] [PubMed]
  24. Pestonjamasp, V.K.; Huttner, K.H.; Gallo, R.L. Processing site and gene structure for the murine antimicrobial peptide CRAMP. Peptides 2001, 22, 1643-1650. [CrossRef] [PubMed]
  25. Termén, S.; Tollin, M.; Olsson, B.; Svenberg, T.; Agerberth, B.; Gudmundsson, G.H. Phylogeny, processing and expression of the rat cathelicidin CRAMP: A model for innate antimicrobial peptides. Cell. Mol. Life Sci. CMLS 2003, 60, 536-549. [CrossRef] [PubMed]
  26. Levy, O.; Weiss, J.; Zarember, K.; Ooi, C.E.; Elsbach, P. Antibacterial 15-kDa protein isoforms (p15s) are members of a novel family of leukocyte proteins. J. Biol. Chem. 1993, 268, 6058-6063. [CrossRef] [PubMed]
  27. Sang, Y.; Teresa Ortega, M.; Rune, K.; Xiau, W.; Zhang, G.; Soulages, J.L.; Lushington, G.H.; Fang, J.; Williams, T.D.; Blecha, F.; et al. Canine cathelicidin (K9CATH): Gene cloning, expression, and biochemical activity of a novel pro-myeloid antimicrobial peptide. Dev. Comp. Immunol. 2007, 31, 1278-1296. [CrossRef]
  28. Brahma, B.; Patra, M.C.; Karri, S.; Chopra, M.; Mishra, P.; De, B.C.; Kumar, S.; Mahanty, S.; Thakur, K.; Poluri, K.M.; et al. Diversity, Antimicrobial Action and Structure-Activity Relationship of Buffalo Cathelicidins. PLoS ONE 2015, 10, e0144741. [CrossRef]
  29. Borriello, G.; Capparelli, R.; Bianco, M.; Fenizia, D.; Alfano, F.; Capuano, F.; Ercolini, D.; Parisi, A.; Roperto, S.; Iannelli, D. Genetic resistance to Brucella abortus in the water buffalo (Bubalus bubalis). Infect. Immun. 2006, 74, 2115-2120. [CrossRef]
  30. Molina-Salinas, G.M.; Ramos-Guerra, M.C.; Vargas-Villarreal, J.; Mata-Cárdenas, B.D.; Becerril-Montes, P.; Said-Fernández, S. Bactericidal activity of organic extracts from Flourensiacernua DC against strains of Mycobacterium tuberculosis. Arch. Med. Res. 2006, 37, 45-49. [CrossRef] [PubMed]
  31. Fair, R.J.; Tor, Y. Antibiotics and bacterial resistance in the 21st century. Perspect. Med. Chem. 2014, 6, 25-64. [CrossRef]
  32. Mdluli, K.; Kaneko, T.; Upton, A. The tuberculosis drug discovery and development pipeline and emerging drug targets. Cold Spring Harb. Perspect. Med. 2015, 5, a021154. [CrossRef] [PubMed]
  33. Diamond, G.; Beckloff, N.; Weinberg, A.; Kisich, K.O. The roles of antimicrobial peptides in innate host defense. Curr. Pharm. Des. 2009, 15, 2377-2392. [CrossRef]
  34. Rivas-Santiago, B.; Torres-Juarez, F. Antimicrobial peptides for the treatment of pulmonary tuberculosis, allies or foes? Curr. Pharm. Des. 2018, 24, 1138-1147. [CrossRef] [PubMed]
  35. Lu, W. Antimicrobial peptides. Semin. Cell Dev. Biol. 2019, 88, 105-106. [CrossRef] [PubMed]
  36. Chanu, K.V.; Thakuria, D.; Kumar, S. Antimicrobial peptides of buffalo and their role in host defenses. Vet. World 2018, 11, 192-200. [CrossRef]
  37. Rivas-Santiago, B.; Schwander, S.K.; Sarabia, C.; Diamond, G.; Klein-Patel, M.E.; Hernandez-Pando, R.; Ellner, J.J.; Sada, E. Human β-defensin 2 is expressed and associated with Mycobacterium tuberculosisduring infection of human alveolar epithelial cells. Infect. Immun. 2005, 73, 4505-4511. [CrossRef] [PubMed]
  38. Liu, P.T.; Stenger, S.; Tang, D.H.; Modlin, R.L. Cutting edge: Vitamin D-mediated human antimicrobial activity against Mycobac- terium tuberculosis is dependent on the induction of cathelicidin. J. Immunol. 2007, 179, 2060-2063. [CrossRef] [PubMed]
  39. Panicker, V.P.; George, S. Identification of three novel myeloid cathelicidin cDNAs and their predicted peptides in buffalo (Bubalus bubalis). Indian J. Biochem. Biophys. 2013, 50, 273-277.
  40. Sonawane, A.; Santos, J.C.; Mishra, B.B.; Jena, P.; Progida, C.; Sorensen, O.E.; Gallo, R.; Appelberg, R.; Griffiths, G. Cathelicidin is involved in the intracellular killing of mycobacteria in macrophages. Cell. Microbiol. 2011, 13, 1601-1617. [CrossRef]
  41. Hollmann, A.; Martinez, M.; Maturana, P.; Semorile, L.C.; Maffia, P.C. Antimicrobial peptides: Interaction with model and biological membranes and synergism with chemical antibiotics. Front Chem. 2018, 6, 204. [CrossRef]
  42. Lewies, A.; Wentzel, J.F.; Jordaan, A.; Bezuidenhout, C.; Du Plessis, L.H. Interactions of the antimicrobial peptide nisin Z with conventional antibiotics and the use of nanostructured lipid carriers to enhance antimicrobial activity. Int. J. Pharm. 2017, 526, 244-253. [CrossRef] [PubMed]
  43. Bessa, L.J.; Eaton, P.; Dematei, A.; Plzcido, A.; Vale, N.; Gomes, P.; Delerue-Matos, C.; Sa Leite, J.R.; Gameiro, P. Synergistic and antibiofilm properties of ocellatin peptides against multidrug-resistant Pseudomonas aeruginosa. Future Microbiol. 2018, 13, 151-163. [CrossRef] [PubMed]
  44. Nijnik, A.; Pistolic, J.; Wyatt, A.; Tam, S.; Hancock, R.E. Human cathelicidin peptide LL-37 modulates the effects of IFN-gamma on APCs. J. Immunol. 2009, 183, 5788-5798. [CrossRef] [PubMed]
  45. Mily, A.; Rekha, R.S.; Kamal, S.M.; Akhtar, E.; Sarker, P.; Rahim, Z.; Gudmundsson, G.H.; Agerberth, B.; Raqib, R. Oral intake of phenylbutyrate with or without vitamin D3 upregulates the cathelicidin LL-37 in human macrophages: A dose finding study for treatment of tuberculosis. BMC Pulm. Med. 2013, 13, 23. [CrossRef]
  46. Chieosilapatham, P.; Ikeda, S.; Ogawa, H.; Niyonsaba, F. Tissue-specific Regulation of Innate Immune Responses by Human Cathelicidin LL-37. Curr. Pharm. Des. 2018, 24, 1079-1091. [CrossRef]
  47. Miao, Y.; Feher, V.A.; McCammon, J.A. Gaussian Accelerated Molecular Dynamics: Unconstrained Enhanced Sampling and Free Energy Calculation. J. Chem. Theory Comput. 2015, 11, 3584-3595. [CrossRef]
  48. Hernández-Pando, R.; Orozcoe, H.; Sampieri, A.; Pavón, L.; Velasquillo, C.; Larriva-Sahd, J.; Alcocer, J.M.; Madrid, M.V. Correlation between the kinetics of Th1, Th2 cells and pathology in a murine model of experimental pulmonary tuberculosis. Immunology 1996, 89, 26-33. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1456655/ (accessed on 30 October 2022).
  49. López-Marure, R.; Gutiérrez, G.; Mendoza, C.; Ventura, J.L.; Sánchez, L.; Reyes Maldonado, E.; Zentella, A.; Montaño, L.F. Ceramide promotes the death of human cervical tumor cells in the absence of biochemical and morphological markers of apoptosis. Biochem. Biophys. Res. Commun. 2002, 293, 1028-1036. [CrossRef]
  50. Lara-Espinosa, J.V.; Santana-Martínez, R.A.; Maldonado, P.D.; Zetter, M.; Becerril-Villanueva, E.; Pérez-Sánchez, G.; Pavón, L.; Mata-Espinosa, D.; Barrios-Payán, J.; López-Torres, M.O.; et al. Experimental Pulmonary Tuberculosis in the Absence of Detectable Brain Infection Induces Neuroinflammation and Behavioural Abnormalities in Male BALB/c Mice. Int. J. Mol. Sci. 2020, 21, 9483. [CrossRef]
  51. Schneider, C.A.; Rasband, W.S.; Eliceiri, K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9, 671-675.
  52. Schmittgen, T.D.; Livak, K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3, 1101-1108. [CrossRef] [PubMed]
  53. Jo, S.; Kim, T.; Iyer, V.G.; Im, W. CHARMM-GUI: A web-based graphical user interface for CHARMM. J. Comput. Chem. 2008, 29, 1859-1865. [CrossRef] [PubMed]
  54. Benarroch, J.M.; Asally, M. The Microbiologist's Guide to Membrane Potential Dynamics. Trends Microbiol. 2020, 28, 304-314. [CrossRef] [PubMed]
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