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doi: 10.15389/agrobiology.2021.3.415eng

UDC: 619:615.371

Acknowledgements:
Supported financially by the Russian Science Foundation (Grant No. 18-14-00044)

 

ANTHRAX: LIFE CYCLE, MECHANISMS OF PATHOGENESIS AND PROSPECTS IN THE DEVELOPMENT OF VETERINARY VACCINES (review)

O.A. Kondakova , N.A. Nikitin, E.A. Evtushenko, D.L. Granovskiy,
J.G. Atabekov, O.V. Karpova

Lomonosov Moscow State University, Biological Faculty, str. 12, 1, Leninskie gory, Moscow, 119234 Russia, e-mail olgakond1@yandex.ru (corresponding author ✉), nikitin@mail.bio.msu.ru, katecat88@mail.ru, dgran98@gmail.com, okar@genebee.msu.ru

ORCID:
Kondakova O.A. orcid.org/0000-0001-5134-6624
Granovskiy D.L. orcid.org/0000-0003-0947-1784
Nikitin N.A. orcid.org/0000-0001-9626-2336
Atabekov J.G. orcid.org/0000-0003-3407-4051
Evtushenko E.A. orcid.org/0000-0002-0679-6818
Karpova O.V. orcid.org/0000-0002-0605-9033

Received March 10, 2021

Anthrax is an acute especially dangerous disease of agricultural and wild animals, as well as humans. Anthrax is induced by the gram-positive spore-forming bacterium Bacillus anthracis. This infection is global, but the incidence rate of livestock and people varies depending on the environmental situation and the implementation of control strategies (C.J. Carlson et al., 2019). Historical and modern experience suggests that uncontrolled outbreaks of anthrax can have disastrous consequences. This review describes the life cycle of the pathogen, environmental features of the anthrax spread and mechanisms of pathogenesis.  Given these factors we discuss the optimal strategies that have been developed over the years taking into account the cost and outcome for combating the dangerous infection. The timely disposal of dead animals and the vaccination of healthy livestock, used together, can effectively stop the spread of the disease. Thus, the development of highly effective, safe and low-cost vaccines is extremely relevant and, moreover, in fact the only promising method for improving the epizootic situation with this hazardous disease. Vaccination of farm animals for several decades has significantly reduced the risk of anthrax, but it is not mandatory in many countries and is often used only after onset of the disease, and not to prevent it. Despite a significant decrease in the incidence rate, the current situation with anthrax in the Russian Federation is characterized as unstable (A.G. Ryazanova et al., 2018; E.G. Simonova et al., 2018). Animal epizootics and human cases are still being recorded in the country due to the presence of natural soil reservoirs of the pathogen and incomplete coverage of vaccination for farm animals. Currently, only live attenuated vaccines are used to vaccinate animals. The review summarizes their effectiveness and safety, as well as the limitations associated with the use of attenuated vaccines. Although existing vaccines have been shown to be effective, they have several serious flaws. Certainly, the relevance of the development of more effective veterinary vaccines against anthrax, based on modern approaches, is fully justified. In particular, there is a need to design a veterinary vaccine that does not contain the pathogen in any form and is compatible with the use of antibiotics, which are necessary, both during the outbreak of anthrax and for regular use in the treatment of various animal diseases. The application of new approaches, the devising modern recombinant vaccines and the rejection of the use of pathogens in an attenuated form is an important and promising task. This review provides an analysis of studies on the development of new candidate vaccines against anthrax. The main attention is paid to the development of subunit vaccines using B. anthracis recombinant antigens obtained in various expression systems, including vaccines for oral administration and compatible with antibiotics.

Keywords: anthrax, Bacillus anthracis, veterinary vaccines, recombinant antigens

 

REFERENCES

  1. World Health Organization. Anthrax in humans and animals. 4th ed. Geneva, WHO Press, 2008.
  2. Martin G.J., Friedlander A.M. Bacillus anthracis (anthrax). In: Mandell, Douglas, and Bennett’s principles and practice of infectious diseases /G.L. Mandell, J.E. Bennett, R. Dolin (eds.). Philadelphia, Churchill Livingstone, 2010: 2715-2725.
  3. Carlson C.J., Kracalik I.T., Ross N., Alexander K.A., Hugh-Jones M.E., Fegan M., Elkin B.T., Epp T., Shury T.K., Zhang W., Bagirova M., Getz W.M., Blackburn J.K. The global distribution of Bacillus anthracis and associated anthrax risk to humans, livestock and wildlife. Nature Microbiology, 2019, 4: 1337-1343 CrossRef
  4. Lindeque P.M., Turnbull P.C. Ecology and epidemiology of anthrax in the Etosha National Park, Namibia. Onderstepoort Journal of Veterinary Research, 1994, 61: 71-83.
  5. Hugh-Jones ME, de Vos V. Anthrax and wildlife. Revue Scientifique et Technique, 2002, 21(2): 359-83 CrossRef
  6. Hoffmann C., Zimmermann F., Biek R., Kuehl H., Nowak K., Mundry R., Agbor A., Angedakin S, Arandjelovic M., Blankenburg A., Brazolla G., Corogenes K., Couacy-Hymann E., Deschner T., Dieguez P., Dierks K., Düx A., Dupke S., Eshuis H., Formenty P., Yuh Y.G., Goedmakers A., Gogarten J.F., Granjon A.C., McGraw S., Grunow R., Hart J., Jones S., Junker J., Kiang J., Langergraber K., Lapuente J., Lee K., Leendertz S.A., Léguillon F., Leinert V., Löhrich T., Marrocoli S., Mätz-Rensing K., Meier A., Merkel K., Metzger S., Murai M., Niedorf S., De Nys H., Sachse A., van Schijndel J., Thiesen U., Ton E., Wu D., Wieler L.H., Boesch C., Klee S.R., Wittig R.M., Calvignac-Spencer S., Leendertz F.H. Persistent anthrax as a major driver of wildlife mortality in a tropical rainforest. Nature, 2017, 548(7665): 82-86 CrossRef
  7. Cossaboom C.M., Khaiseb S., Haufiku B., Katjiuanjo P., Kannyinga A., Mbai K., Shuro T., Hausiku J., Likando A., Shikesho R., Nyarko K., Miller L.A., Agolory S., Vieira A.R., SalzerJ.S., Bower W.A., Campbell L., Kolton C.B., Marston C., Gary J., Bollweg B.C., Zaki S.R., Hoffmaster A., Walke H. Anthrax epizootic in wildlife, Bwabwata National Park, Namibia, 2017. Emerging Infectious Diseases, 2019, 25(5): 947-950 CrossRef
  8. Van Ness G.B. Ecology of anthrax. Science, 1971, 172: 1303-1307 CrossRef
  9. Joyner T.A., Lukhnova L., Pazilov Y., Temiralyeva G., Hugh-Jones M.E., Aikimbayev A., Blackburn J.K. Modeling the potential distribution of Bacillus anthracis under multiple climate change scenarios for Kazakhstan. PLoS ONЕ, 2010, 5(3): e9596 CrossRef
  10. Norris M.H., Blackburn J.K. Linking geospatial and laboratory sciences to define mechanisms behind landscape level drivers of anthrax outbreaks. International Journal of Environmental Research, 2019, 16(19): 3747 CrossRef
  11. Симонова Е.Г., Картавая С.А., Титков А.В., Локтионова М.Н., Раичич С.Р., Толпин В.А, Лупян Е.А., Платонов А.Е. Сибирская язва на Ямале: оценка эпизоотологических и эпидемиологических рисков. Проблемы особо опасных инфекций, 2017, 1: 89-93 CrossRef
  12. Walsh M.G., Smalen A.W., Mor S.M. Climatic influence on anthrax suitability in warming northern latitudes. Scientific Reports, 2018, 8: 9269 CrossRef
  13. Beyer W., Turnbull P.C.B. Anthrax in animals. Molecular Aspects of Medicine, 2009, 30(6): 481-489 CrossRef
  14. Sterne M. The use of anthrax vaccines prepared from avirulent (uncapsulated) variants of Bacillus anthracis. Onderstepoort Journal of Veterinary Science and Animal Industry, 1939, 13: 307-312.
  15. Felix J.B., Chaki S.P., Ficht T.A., Rice-Ficht A.C., Cook W. Bacillus anthracis Sterne Strain 34F2 vaccine antibody dose response by subcutaneous and oral administration. Poultry, Fisheries & Wildlife Sciences, 2019, 7: 206 CrossRef
  16. Черкасский Б.Л. Эпидемиология и профилактика сибирской язвы. М., 2002.
  17. Арутюнов Ю.И. Сибирская язва и вопросы природной очаговости. Universum: Медицина и фармакология: электронный научный журнал, 2013, 1(1). Режим доступа: http://7universum.com/ru/med/archive/item/324. Дата обращения: 23.12.2019.
  18. Dragon D.C., Elkin B.T., Nishi J.S., Ellsworth T.R. A review of anthrax in Canada and implications for research on the disease in northern bison. Journal of Applied Microbiology, 1999, 87: 208-213 CrossRef
  19.  Blackburn J.K., Van Ert M., Mullins J.C., Hadfield T.L., Hugh-Jones M.E. The necrophagous fly anthrax transmission pathway: empirical and genetic evidence from wildlife epizootics. Vector-Borne and Zoonotic Diseases, 2014, 14(8): 576-83 CrossRef
  20. Basson L., Hassim A., Dekker A., Gilbert A., Beyer W., Rossouw J., Van Heerden H. Blowflies as vectors of Bacillus anthracis in the Kruger National Park. Koedoe, 2018, 60(1): a1468 CrossRef
  21. Munang’andu H.M., Banda F., Siamudaala V.M., Munyeme M., Kasanga C.J., Hamududu B. The effect of seasonal variation on anthrax epidemiology in the upper Zambezi floodplain of western Zambia. Journal of Veterinary Science, 2012, 13(3): 293-298 CrossRef
  22. Turner W., Kausrud K., Beyer W., Easterday W., Barandongo Z., Blaschke E., Blaschke E., Cloete C.C., Lazak J., Van Ert M.N., Ganz H.H., Turnbull P.C.B., Stenseth N.C., Getz W.M. Lethal exposure: An integrated approach to pathogen transmission via environmental reservoirs. Scientific Reports, 2016, 6: 27311 CrossRef
  23. Hugh-Jones M., Blackburn J. The ecology of Bacillus anthracis. Molecular Aspects of Medicine, 2009, 30: 356-367 CrossRef
  24. Колонин Г.В. О роли птиц в эпизоотологии сибирской язвы. Русский орнитологический журнал, 2017, 26(1397): 327-329.
  25. Dey R., Hoffman P.S., Glomski I.J. Germination and amplification of anthrax spores by soil-dwelling amoebas. Applied and Environmental Microbiology, 2012, 78(22): 8075-8081 CrossRef
  26. Saile E., Koehler T.M. Bacillus anthracis multiplication, persistence, and genetic exchange in the rhizosphere of grass plants. Applied and Environmental Microbiology, 2006, 72(5): 3168-3174 CrossRef
  27. Schuch R., Fischetti V.A. The secret life of the anthrax agent Bacillus anthracis: bacteriophage-mediated ecological adaptations. PLoS ONЕ, 2009, 4: e6532 CrossRef
  28. U.S EPA. Environmental persistence of vegetative Bacillus anthracis and Yersinia pestis. U.S. Environmental Protection Agency, Washington, DC, EPA/600/R-14/150, 2014.
  29. Рязанова А.Г., Семенова О.В., Еременко Е.И., Аксенова Л.Ю., Буравцева Н.П., Головинская Т.М., Куличенко А.Н. Эпидемиологическая и эпизоотологическая обстановка по сибирской язве в 2017 году, прогноз на 2018 год. Проблемы особо опасных инфекций, 2018, 1: 63-65.
  30. Картавая С.А., Симонова Е.Г., Локтионова М.Н., Колганова О.А., Ладный В.И., Раичич С.Р. Научное обоснование размеров санитарно-защитных зон сибиреязвенных захоронений на основе комплексной оценки риска. Гигиена и санитария, 2016, 95(7): 601-606.
  31. Симонова Е.Г., Картавая С.А., Раичич С.Р., Локтионова М.Н., Шабейкин А.А. Сибирская язва в Российской Федерации: совершенствование эпизоотолого- эпидемиологического надзора на современном этапе. Эпидемиология и вакцинопрофилактика, 2018, 17(2): 57-62.
  32. Черкасский Б.Л. Кадастр стационарно неблагополучных по сибирской язве пунктов Российской Федерации. М., 2005.
  33. Гаврилов В.А., Грязнева Т.Н., Селиверстров В.В. Почвенные очаги сибирской язвы: реалии и проблемы. Ветеринария, зоотехния и биотехнология, 2017, 8: 17-22.
  34. Mwakapeje E.R., Høgset S., Fyumagwa R., Nonga H.E., Mdegela R.H., Skjerve E. Anthrax outbreaks in the humans — livestock and wildlife interface areas of Northern Tanzania: a retrospective record review 2006-2016. BMC Public Health, 2018, 18(1): 106 CrossRef
  35. Попова А.Ю., Демина Ю.В., Ежлова Е.Б., Куличенко А.Н., Рязанова А.Г., Малеев В.В., Плоскирева А.А., Дятлов И.А., Тимофеев В.С., Нечепуренко Л.А., Харьков В.В. Вспышка сибирской язвы в Ямало-Ненецком автономном округе в 2016 году, эпидемиологические особенности. Проблемы особо опасных инфекций, 2016, 4: 42-46 CrossRef
  36. Croicu A.M. An optimal control model to reduce and eradicate anthrax disease in herbivorous animals. Bulletin of Mathematical Biology, 2019, 81(1): 235-255 CrossRef
  37. Makino S., Watarai M., Cheun H.I., Shirahata T., Uchida I. Effect of the lower molecular capsule released from the cell surface of Bacillus anthracis on the pathogenesis of anthrax. Journal of Infectious Diseases, 2002, 186(2): 227-233 CrossRef
  38. Sharma S., Bhatnagar R., Gaur D. Bacillus anthracis poly-γ-D-glutamate capsule inhibits opsonic phagocytosis by impeding complement activation. Frontiers in Immunology, 2020, 11: 462 CrossRef
  39. Okinaka R.T., Cloud K., Hampton O., Hoffmaster A.R., Hill K.K., Keim P., Koehler T.M., Lamke G., Kumano S., Mahillon J., Manter D., Martinez Y., Ricke D., Svensson R., Jackson P.J. Sequence and organization of pXO1, the large Bacillus anthracis plasmid harboring the anthrax toxin genes. Journal of Bacteriology, 1999, 181(20): 6509-6515.
  40. Liu S., Moayeri M., Leppla S.H. Anthrax lethal and edema toxins in anthrax pathogenesis. Trends in Microbiology, 2014, 22(6): 317-325 CrossRef
  41. Deuquet J., Lausch E., Superti-Furga A., van der Goot F.G. The dark sides of capillary morphogenesis gene 2. EMBO Journal, 2012, 31(1): 3-13 CrossRef
  42. Sun J., Jacquez P. Roles of Anthrax Toxin Receptor 2 in anthrax toxin membrane insertion and pore formation. Toxins, 2016, 8(2): 34 CrossRef
  43. Storm L., Bikker F.J., Nazmi K., Hulst A.G., der Riet-Van Oeveren D.V., Veerman E.C.I., Hays J.P., Kaman W.E. Anthrax protective antigen is a calcium-dependent serine protease. Virulence, 2018, 9(1): 1085-1091 CrossRef
  44. Bann J.G. Anthrax toxin protective antigen--insights into molecular switching from prepore to pore. Protein Science, 2012, 21(1): 1-12 CrossRef
  45. Jiang J., Pentelute B.L., Collier R.J.,  Zhou Z.H. Atomic structure of anthrax PA pore elucidates toxin translocation. Nature, 2015, 521(7553): 545-549 CrossRef
  46. Hardenbrook N.J., Liu S., Zhou K., Ghosal K., Zhou Z.H., Krantz B.A. Atomic structures of anthrax toxin protective antigen channels bound to partially unfolded lethal and edema factors.Nature Communications, 2020, 11: 840 CrossRef
  47. Alameh S., Bartolo G., O’Brien S., Henderson E.A., Gonzalez L.O., Hartmann S., Klimko C.P., Shoe J.L., Cote C.K., Grill L.K., Levitin A. Anthrax toxin component, Protective Antigen, protects insects from bacterial infections. PLoS Pathogens, 2020, 16(8): e1008836 CrossRef
  48. Duesbery N.S., Webb C.P., Leppla S.H., Gordon V.M., Klimpel K.R., Copeland T.D., Ahn N.G., Oskarsson M.K., Fukasawa K., Paull K.D., Vande Woude G.F. Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science, 1998, 280: 734-737 CrossRef
  49. Vitale G., Bernardi L., Napolitani G., Mock M., Montecucco C. Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor. Biochemical Journal, 2000, 352: 739-745 CrossRef
  50. Pellizzari R., Guidi-Rontani C., Vitale G., Mock M., Montecucco C. Anthrax lethal factor cleaves MKK3 in macrophages and inhibits the LPS/IFNgamma-induced release of NO and TNFalpha. FEBS Letters, 1999, 462: 199-204 CrossRef
  51. Leppla S.H. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proceedings of the National Academy of Sciences, 1982, 79: 3162-3166 CrossRef
  52. Bromberg-White J., Lee C.S., Duesbery N. Consequences and utility of the zinc-dependent metalloprotease activity of anthrax lethal toxin. Toxins (Basel), 2010, 2(5): 1038-1053 CrossRef
  53. Tang W.J., Guo Q. The adenylyl cyclase activity of anthrax edema factor. Molecular Aspects of Medicine, 2009, 30(6): 423-430 CrossRef
  54. Jara G.E., Martínez L. Anthrax edema factor: an ion-adaptive mechanism of catalysis with increased transition-state conformational flexibility. Journal of Physical Chemistry B, 2016, 120: 6504-6514 CrossRef
  55. Cote C.K., Rossi C.A., Kang A.S., Morrow P.R., Lee J.S., Welkos S.L. The detection of protective antigen (PA) associated with spores of Bacillus anthracis and the effects of anti-PA antibodies on spore germination and macrophage interactions. Microbial Pathogenesis, 2005, 38: 209-225 CrossRef
  56. Liu S., Zhang Y., Moayeri M., Liu J., Crown D., Fattah R.J., Wein A.N., Yu Z.-X., Finkel T., Leppla S.H. Key tissue targets responsible for anthrax-toxin-induced lethality. Nature, 2013, 501: 63-68 CrossRef
  57. Liu S., Schubert R.L., Bugge T.H., Leppla S.H. Anthrax toxin: structures, functions and tumour targeting. Expert Opin. Biol. Ther., 2003, 3: 843-853 CrossRef
  58. Hutt J.A., Lovchik J.A., Drysdale M., Sherwood R.L., Brasel T., Lipscomb M.F., Lyons C.R. Lethal factor, but not edema factor, is required to cause fatal anthrax in cynomolgus macaques after pulmonary spore challenge. The American Journal of Pathology, 2014, 184(12): 3205-3216 CrossRef
  59. Patel V.I., Booth J.L., Dozmorov M., Brown B.R., Metcalf J.P. Anthrax edema and lethal toxins differentially target human lung and blood phagocytes. Toxins (Basel), 2020, 12(7): 464 CrossRef
  60. Abrami L., Brandi L., Moayeri M., Brown M.J., Krantz B.A., Leppla S.H., van der Goot F.G. Hijacking multivesicular bodies enables long-term and exosome-mediated long-distance action of anthrax toxin. Cell Reports, 2013, 5(4): 986-996 CrossRef
  61. Hambleton P., Carman J.A., Melling J. Anthrax: the disease in relation to vaccines. Vaccine, 1984, 2(2): 125-132 CrossRef
  62. Scorpio А., Blank T.E., Day W.A., Chabot D.J. Anthrax vaccines: Pasteur to the present. Cellular and Molecular Life Sciences, 2006, 63: 2237-2248 CrossRef
  63. Thorkildson P., Kinney H.L., AuCoin D.P. Pasteur revisited: an unexpected finding in Bacillus anthracis vaccine strains. Virulence, 2016, 7(5): 506-507 CrossRef
  64. Liang X., Zhang H., Zhang E., Wei J., Li W., Wang B., Dong S., Zhu J. Identification of the pXO1 plasmid in attenuated Bacillus anthracis vaccine strains. Virulence, 2016, 7(5): 578-586 CrossRef
  65. Fasanella A., Losito S., Trotta T., Adone R., Massa S., Ciuchini F., Chiocco D. Detection of anthrax vaccine virulence factors by polymerase chain reaction. Vaccine, 2001, 19: 4214-4218 CrossRef
  66. Harrington R., Ondov B.D., Radune D., Friss M.B., Klubnik J., Diviak L., Hnath J., Cendrowski S.R., Blank T.E., Karaolis D., Friedlander A.M., Burans J.P., Rosovitz M.J., Treangen T., Phillippy A.M., Bergman N.H. Genome sequence of the attenuated Carbosap vaccine strain of Bacillus anthracis. Genome Announcements, 2013, 1(1): e00067-12 CrossRef
  67. Cataldi A., Mock M., Bentancor L. Characterization of Bacillus anthracis strains used for vaccination. Journal of Applied Microbiology, 2000, 88: 648-654 CrossRef
  68. Wobeser B.K. Anthrax vaccine associated deaths in miniature horses. Canadian Veterinary Journal, 2015, 56(4): 359-360.
  69. Cartwright M.E., McChesney A.E., Jones R.L. Vaccination-related anthrax in three llamas.  Journal of the American Veterinary Medical Association, 1987, 191(6): 715-716.
  70. Felix J.B., Chaki S.P., Xu Y., Ficht T.A., Rice-Ficht A.C., Cook W.E. Protective antibody response following oral vaccination with microencapsulated Bacillus anthracis Sterne strain 34F2 spores. npj Vaccines,2020, 5: 59 CrossRef
  71. Fasanella A., Tonello F., Garofolo G., Muraro L, Carattoli A., Adone R., Montecucco C. Protective activity and immunogenicity of two recombinant anthrax vaccines for veterinary use. Vaccine, 2008, 26(45): 5684-5688 CrossRef
  72. Turnbull P.C.B. Anthrax vaccines: past, present and future. Vaccine, 1991, 9: 533-539 CrossRef
  73. Jorge S., Dellagostin О.А. The development of veterinary vaccines: a review of traditional methods and modern biotechnology approaches. Biotechnology Research and Innovation, 2017, 1(1): 6-13 CrossRef
  74. Kondakova O.A., Nikitin N.A., Evtushenko E.A., Ryabchevskaya E.M., Atabekov J.G., Karpova O.V. Vaccines against anthrax based on recombinant protective antigen: problems and solutions. Expert Review of Vaccines, 2019, 18(8): 813-828 CrossRef
  75. Turnbull P.C.B., Leppla S.H., Broster M.G., Quinn C.P., Melling J. Antibodies to anthrax toxin in humans and guinea pigs and their relevance to protective immunity. Medical Microbiology and Immunology, 1988, 177: 293-303 CrossRef
  76. Ndumnego O.C., Köhler S.M., Craford J., van Heerden H., Beyer W. Comparative analysis of the immunologic response induced by the Sterne 34F2 live spore Bacillus anthracis vaccine in a ruminant model. Veterinary Immunology and Immunopathology, 2016, 178: 14-21 CrossRef
  77. Phaswana P.H., Ndumnego O.C., Koehler S.M., Beyer W., Crafford J.E., van Heerden H. Use of the mice passive protection test to evaluate the humoral response in goats vaccinated with Sterne 34F2 live spore vaccine. Veterinary Research, 2017, 48(1): 46 CrossRef
  78. Zhang J., Jex E., Feng T., Sivko G.S., Baillie L.W., Goldman S., Van Kampen K.R, Tang D.C. An adenovirus-vectored nasal vaccine confers rapid and sustained protection against anthrax in a single-dose regimen. Clinical and Vaccine Immunology, 2013, 20(1): 1-8 CrossRef
  79. Krishnan V., Andersen B.H., Shoemaker C., Sivko G.S. , Tordoff K.P., Stark G.V., Zhang J., Feng T., Duchars M., Roberts M.S. Efficacy and immunogenicity of single-dose AdVAV intranasal anthrax vaccine compared to anthrax vaccine absorbed in an aerosolized spore rabbit challenge model. Clinical and Vaccine Immunology, 2015, 22(4): 430-439 CrossRef
  80. Mohamadzadeh M., Duong T., Sandwick S.J., Hoover T., Klaenhammer T.R. Dendritic cell targeting of Bacillus anthracis protective antigen expressed by Lactobacillus acidophilus protects mice from lethal challenge. PNAS, 2009, 106(11): 4331-4336 CrossRef
  81. Mohamadzadeh M., Durmaz E., Zadeh M., Pakanati K.C., Gramarossa M., Cohran V., Klaenhammer T.R. Targeted expression of anthrax protective antigen by Lactobacillus gasseri as an anthrax vaccine. Future Microbiology, 2010, 5(8): 1289-1296 CrossRef
  82. Osorio M., Wu Y., Singh S., Merkel T.J., Bhattacharyya S., Blake M.S., Kopecko D.J. Anthrax protective antigen delivered by Salmonella enterica serovar Typhi Ty21a protects mice from a lethal anthrax spore challenge. Infection and Immunity, 2009, 77(4): 1475-1482 CrossRef
  83. Ramirez K., Ditamo Y., Galen J.E., Baillie L.W., Pasetti M.F. Mucosal priming of newborn mice with S. Typhi Ty21a expressing anthrax protective antigen (PA) followed by parenteral PA-boost induces B and T cell-mediated immunity that protects against infection bypassing maternal antibodies. Vaccine, 2010, 28(37): 6065-6075 CrossRef
  84. Sim B.K.L., Li M., Osorio M., Wu Y., Wai T.T., Peterson J.W., James E.R., Chakravarty S., Gao L., Xu R., Natasha K.C., Stafford R.E., Lawrence W.S., Yeager L.F., Peel J.E., Sivasubramani S.K., Ashok K., Chopra A.K., Filippova S., Hoffman S.L. Protection against inhalation anthrax by immunization with Salmonella enterica serovar Typhi Ty21a stably producing protective antigen of Bacillus anthracis. npj Vaccines, 2017, 2: 17 CrossRef
  85. Donate A., Heller R. Assessment of delivery parameters with the multi-electrode array for development of a DNA vaccine against Bacillus anthracis. Bioelectrochemistry, 2013, 94: 1-6 CrossRef
  86. Kim N.Y., Chang D.S., Kim Y., Kim C.H., Hur G.H., Yang J.M., Shin S. Enhanced immune response to DNA vaccine encoding Bacillus anthracis PA-D4 protects mice against anthrax spore challenge. PLoS ONE, 2015, 10(10): e0139671 CrossRef
  87. Köhler S.M., Baillie L.W., Beyer W. BclA and toxin antigens augment each other to protect NMRI mice from lethal Bacillus anthracis challenge. Vaccine, 2015, 33(24): 2771-2777 CrossRef
  88. Brown B.K., Cox J., Gillis A., VanCott T.C., Marovich M., Milazzo M., Antonille T.S., Wieczorek L, McKee K.T. Jr., Metcalfe K., Mallory R.M., Birx D., Polonis V.R., Robb M.L. Phase I study of safety and immunogenicity of an Escherichia coli-derived recombinant protective antigen (rPA) vaccine to prevent anthrax in adults. PLoS ONE, 2010, 5(11): e13849 CrossRef
  89. Bellanti J.A., Lin F.Y., Chu C., Shiloach J., Leppla S.H., Benavides G.A., Karpas A., Moayeri M., Guo C., Robbins J.B., Schneerson R. Phase I study of a recombinant mutant protective antigen of Bacillus anthracis. Clinical and Vaccine Immunology, 2012, 19(2): 140-145 CrossRef
  90. Chun J.H., Choi O.J., Cho M.H., Hong K.J., Seong W.K., Oh H.B., Rhie G.E. Serological correlate of protection in Guinea pigs for a recombinant protective antigen anthrax vaccine produced from bacillus brevis. Osong public health and research perspectives, 2012, 3(3): 170-176 CrossRef
  91. Reed M.D., Wilder J.A., Mega W.M., Hutt J.A., Kuehl P.J., Valderas M.W., Chew L.L., Liang B.C., Squires C.H. Immunization with a recombinant, Pseudomonas fluorescens-expressed, mutant form of Bacillus anthracis-derived protective antigen protects rabbits from anthrax infection. PloS ONE, 2015, 10(7): e0130952 CrossRef
  92. Mamedov T., Chichester J.A., Jones R.M., Ghosh A., Coffin M.V., Herschbach K., Prokhnevsky A.I., Streatfield S.J., Yusibov V. Production of functionally active and immunogenic non-glycosylated protective antigen from Bacillus anthracis in Nicotiana benthamiana by co-expression with peptide-N-glycosidase F (PNGase F) of Flavobacterium meningosepticum. PLoS ONE, 2016, 11(4): e0153956 CrossRef
  93. Li Q., Peachman K.K., Sower L., Leppla S.H., Shivachandra S.B., Matyas G.R., Peterson JW., Alving C.R., Rao M., Rao V.B. Anthrax LFn-PA hybrid antigens: biochemistry, immunogenicity, and protection against lethal ames spore challenge in rabbits. The Open Vaccine Journal, 2009, 2: 92-99 CrossRef
  94. Wu G., Hong Y., Guo A., Feng C., Cao S., Zhang C.C., Shi R., Tan Y., Liu Z. A chimeric protein that functions as both an anthrax dual-target antitoxin and a trivalent vaccine. Antimicrobial Agents and Chemotherapy, 2010, 54(11): 4750-4757 CrossRef
  95. Baillie L.W., Huwar T.B., Moore S., Mellado-Sanchez G., Rodriguez L., Neeson B.N., Flick-Smith H.C., Jenner D.C., Atkins H.S., Ingram R.J., Altmann D.M., Nataro J.P., Pasetti M.F. An anthrax subunit vaccine candidate based on protective regions of Bacillus anthracis protective antigen and lethal factor. Vaccine, 2010, 28(41): 6740-6748 CrossRef
  96. Suryanarayana N., Verma M., Thavachelvam K., Saxena N., Mankere B., Tuteja U., Hmuaka V. Generation of a novel chimeric PALFn antigen of Bacillus anthracis and its immunological characterization in mouse model. Appl. Microbiol. Biotechnol., 2016, 100(19): 8439-8451 CrossRef
  97. Varshney A., Kumar M., Nagar D.P., Pal V., Goel A.K. Development of a novel chimeric PA-LF antigen of Bacillus anthracis, its immunological characterization and evaluation as a future vaccine candidate in mouse model. Biologicals, 2019, 61: 38-43 CrossRef
  98. Aggarwal S., Somani V.K., Gupta S., Garg R., Bhatnagar R. Development of a novel multiepitope chimeric vaccine against anthrax. Medical Microbiology and Immunology, 2019,208: 185-195 CrossRef
  99. Majumder S., Das S., Somani V., Makam S.S., Kingston J.J., Bhatnagar R. A bivalent protein r-PB, comprising PA and BclA immunodominant regions for comprehensive protection against Bacillus anthracis. Scientific Reports, 2018, 8(1): 7242 CrossRef
  100. Majumder S., Das S., Somani V.K., Makam S.S., Kingston J.J., Bhatnagar R. A bivalent protein r-PAbxpB comprising PA Domain IV and Exosporium Protein BxpB confers protection against B. anthracis spores and toxin. Frontiers in Immunology, 2019, 10: 498 CrossRef
  101. Lee D.Y., Chun J.H., Ha H.J., Park J., Kim B.S., Oh H.B., Rhie G.E. Poly-gamma-d-glutamic acid and protective antigen conjugate vaccines induce functional antibodies against the protective antigen and capsule of Bacillus anthracis in guinea-pigs and rabbits. FEMS Immunol. Med. Microbiol., 2009, 57(2): 165-172 CrossRef
  102. Candela T., Dumetz F., Tosi-Couture E., Mock M., Goossens P.L., Fouet A. Cell-wall preparation containing poly-γ-D-glutamate covalently linked to peptidoglycan, a straightforward extractable molecule, protects mice against experimental anthrax infection. Vaccine, 2012, 31(1): 171-175 CrossRef
  103. Garufi G., Wang Y.T., Oh S.Y., Maier H., Missiakas D.M., Schneewind O. Sortase-conjugation generates a capsule vaccine that protects guinea pigs against Bacillus anthracis. Vaccine, 2012, 30(23): 3435-3444 CrossRef
  104. Chen Z., Schneerson R., Lovchik J.A., Dai Z., Kubler-Kielb J., Agulto L., Leppla S.H., Purcell R.H. Bacillus anthracis capsular conjugates elicit chimpanzee polyclonal antibodies that protect mice from pulmonary anthrax. Clinical and Vaccine Immunology, 2015, 22(8): 902-908 CrossRef
  105. Kumar M., Puranik N., Varshney A., Tripathi N., Pal V., Goel A.K. BA3338, a surface layer homology domain possessing protein augments immune response and protection efficacy of protective antigen against Bacillus anthracis in mouse model. Journal of Applied Microbiology, 2020, 129(2): 443-452 CrossRef
  106. Jauro S., Ndumnego O.C., Ellis C., Buys A., Beyer W., Heerden H.V. Immunogenicity of non-living anthrax vaccine candidates in cattle and protective efficacy of immune sera in A/J mouse model compared to the Sterne live spore vaccine. Pathogens, 2020, 9(7): 557 CrossRef
  107. Oh Y., Kim J.A., Kim C.H., Choi S.K., Pan J. Bacillus subtilis spore vaccines displaying protective antigen induce functional antibodies and protective potency. BMC Veterinary Research, 2020, 16: 259 CrossRef
  108. Liu K., Yin Y, Zhang J., Zai X., Li R., Ma H., Xu J., Shan J., Chen W. Polysaccharide PCP-I isolated from Poria cocos enhances the immunogenicity and protection of an anthrax protective antigen-based vaccine. Human Vaccines & Immunotherapeutics, 2020, 16(7): 1699-1707 CrossRef
  109. Weir G.M., MacDonald L.D., Rajagopalan R.,  Sivko G.S., Valderas M.W., Rayner J., Berger B.J., Sammatur L., Stanford M.M. Single dose of DPX-rPA, an enhanced-delivery anthrax vaccine formulation, protects against a lethal Bacillus anthracis spore inhalation challenge. npj Vaccines, 2019, 4: 6 CrossRef
  110. Wagner L., Verma A., Meade B.D., Reiter K., Narum D.L., Brady R.A., Little S.F., Burns D.L. Structural and immunological analysis of anthrax recombinant protective antigen adsorbed to aluminum hydroxide adjuvant. Clinical and Vaccine Immunology, 2012, 19: 1465-1473 CrossRef
  111. Domínguez-Castillo R.I., Verma A., Amador-Molina J.C., Sirota L., Arciniega J.L. Ability of ELISA and a toxin neutralization assay to detect changes in immunogenicity of a recombinant Bacillus anthracis protective antigen vaccine upon storage. Biologicals, 2013, 41(2): 111-114 CrossRef
  112. D’Souza A.J., Mar K.D., Huang J., Majumdar S., Ford B.M., Dyas B., Ulrich R.G., Sullivan V.J. Rapid deamidation of recombinant protective antigen when adsorbed on aluminum hydroxide gel correlates with reduced potency of vaccine. Journal of Pharmaceutical Sciences, 2013, 102(2): 454-461 CrossRef
  113. Ryabchevskaya E.M., Evtushenko E.A., Granovskiy D.L., Ivanov P.A., Atabekov J.G., Kondakova O.A., Nikitin N.A., Karpova O.V. Two approaches for the stabilization of Bacillus anthracis recombinant protective antigen. Human Vaccines & Immunotherapeutics, 2020, 17(2): 560-565 CrossRef
  114. Zhao T., Zhao X., Liu J., Meng Y., Feng Y., Fang T., Zhang J., Yang X., Li J., Xu J., Chen W. Diminished but not abolished effect of two His351 mutants of anthrax edema factor in a murine model. Toxins (Basel), 2016, 8(2): 35 CrossRef
  115. Koehler S.M., Buyuk F., Celebi O., Demiraslan H., Doganay M., Sahin M., Moehring J., Ndumnego O.C., Otlu S., van Heerden H., Beyer W. Protection of farm goats by combinations of recombinant peptides and formalin inactivated spores from a lethal Bacillus anthracis challenge under field conditions. BMC Veterinary Research, 2017, 13(1): 220 CrossRef
  116. Ndumnego O.C., Koehler S., Crafford J.E., Beyer W., van Heerden H. Immunogenicity of anthrax recombinant peptides and killed spores in goats and protective efficacy of immune sera in A/J mouse model. Scientific Reports, 2018, 8: 16937 CrossRef
  117. Jauro S., Ndumnego O.C., Ellis C., Buys A., Beyer W., Heerden H.V. Immunogenicity and protective efficacy of a non-living anthrax vaccine versus a live spore vaccine with simultaneous penicillin-g treatment in cattle. Vaccine (Basel), 2020, 8(4): 595 CrossRef
  118. Gorantala J., Grover S., Rahi A., Chaudhary P., Rajwanshi R, Sarin N.B., Bhatnagar R. Generation of protective immune response against anthrax by oral immunization with protective antigen plant-based vaccine. Journal of Biotechnology, 2014, 176: 1-10 CrossRef
  119. Koya V., Moayeri M., Leppla S.H., Daniell H. Plant-based vaccine: mice immunized with chloroplast-derived anthrax protective antigen survive anthrax lethal toxin challenge. Infection and Immunity, 2005, 73(12): 8266-8274 CrossRef

 

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