Viral and bacterial coinfection as a global problem of modern medicine

Cite item


Coinfection is becoming increasingly medical-social value in the modern world, not only because of their high incidence, but also because a reliable methodological approach to their clinical evaluation, treatment and prevention is absent. This methodological approach should be based on knowledge of the mechanisms of interaction of pathogenic microorganisms with each other - direct and/or mediated through immune system. The most pathogens in сoinfections are bacteria and viruses, their association not only contributes to a severity of infection, but also greatly increases the frequency of its complications and deaths. In this review, based on the example of respiratory coinfections, malignant processes, human immunodeficiency virus associated microorganisms, the interaction of bacterial-viral pathogens examines to show their high diversity. Among the mechanisms of interaction of coinfecting agents, special attention is paid to the impact of viruses on bacterial toxin production, and bacteria on the infectivity of viruses. Coinfecting microorganisms contribute to overcoming epithelial barrier by each other, can mutually beneficial to modify the functions of the cells of the immune system and help to escape from the immune response. It was found that the gene expression of oncogenic viruses and HIV is governed by epigenomic changes caused by the bacteria that leads to carcinogenesis. It was shown that the diversity of bacterial-viral interactions in coinfections not only requires new approaches to their timely identification and control, but also generates new biotechnology and strategies for combating of coinfection development around the world.

About the authors

Irina P Balmasova

Moscow State University of Medcine and Dentistry named by A.I. Evdokimov; Peoples’ Friendship University of Russia


E S Malova

Peoples’ Friendship University of Russia


R I Sepiashvili

Peoples’ Friendship University of Russia



  1. Griffiths Е.С., Pedersen A.B., Fenton A., Petchey O.L. The nature and consequences of coinfection in humans // J Infect. 2011. V. 63. № 3. Р. 200-206.
  2. Gupta S., Tang C., Tran M., Kadouri D.E. Effect of predatory bacteria on human cell lines // PLoS ONE. 2016. V. 11. № 8. e0161242.
  3. Stanton T.B. A call for antibiotic alternatives research // Trends Microbiol. 2013. V. 21. № 3. P. 111-113.
  4. Pullan R., Brooker S. The health impact of polyparasitism in humans: are we under-estimating the burden of parasitic diseases? // Parasitology. 2008. V. 135. № 7. P. 783-794.
  5. Steinmann P., Utzinger J., Du Z.W., Zhou X.N. Multiparasitism: a neglected reality on global, regional and local scale // Adv Parasitol. 2010. V. 73. P. 21-50.
  6. Niemann S., Ehrhardt C., Medina E., Wamking K., Tuchscherr L., Heitmann V., Ludwig S., Peters G., Loffler B. Combined action of influenza virus and Staphylococcus aureus Panton-Valentine leukocidin provokes severe lung epithelium damage // J Infect Dis. 2012. V. 206. № 7. P. 1138-1148.
  7. Tashiro M., Ciborowski P., Reinacher M., Pulverer G., Klenk H.D., Rott R. Synergistic role of staphylococcal proteases in the induction of influenza virus pathogenicity. Virology. 1987. V. 157. № 2. P. 421-430.
  8. Löffler B., Niemann S., Ehrhardt C., Horn D., Lanckohr C., Lina G., Ludwig S., Peters G. Pathogenesis of Staphylococcus aureus necrotizing pneumonia: the role of PVL and an influenza coinfection // Expert Rev Anti Infect Ther. 2013. V. 11. № 10. P. 1041-1051.
  9. Nguyen T., Kyle U.G., Jaimon N., Tcharmtchi M.H., Coss-Bu J.A., Lam F., Teruya J., Loftis L. Coinfection with Staphylococcus aureus increases risk of severe coagulopathy in critically ill children with influenza A (H1N1) virus infection // Crit Care Med. 2012. V. 40, № 12. P. 3246-3250.
  10. Walters K.A., D'Agnillo F., Sheng Z.M., Kindrachuk J., Schwartzman L.M., Kuestner R.E., Chertow D.S., Golding B.T., Taubenberger J.K., Kash J.C. 1918 pandemic influenza virus and Streptococcus pneumoniae co-infection results in activation of coagulation and widespread pulmonary thrombosis in mice and humans // J Pathol. 2016. V. 238. № 1. P. 85-97.
  11. Damasio G.A., Pereira L.A., Moreira S.D., Duarte dos Santos C.N., Dalla-Costa L.M., Raboni S.M. Does virus-bacteria coinfection increase the clinical severity of acute respiratory infection? // J Med Virol. 2015. V. 87. № 9. P. 1456-1461.
  12. Hraiech S., Papazian L., Rolain J.-M., Bregeon F. Animal models of polymicrobial pneumonia // Drug Des Devel Ther. 2015. V. 9. P. 3279-3292.
  13. Morens D.M., Taubenberger J.K., Fauci A.S. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness // J Infect Dis. 2008. V. 198. № 7. P. 962-970.
  14. Davidson S., Maini M.K., Wack A. Disease-promoting effects of type I interferons in viral, bacterial, and coinfections // J Interferon Cytokine Res. 2015. V. 35. № 4. P. 252-264.
  15. Kudva A., Scheller E.V., Robinson K.M., Crowe C.R., Choi S.M., Slight S.R., Khader S.A., Dubin P.J., Enelow R.I., Kolls J.K., Alcorn J.F. Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice // J Immunol. 2011. V. 186. № 3. P. 1666-1674.
  16. Li W., Moltedo B., Moran T.M. Type I interferon induction during influenza virus infection increases susceptibility to secondary Streptococcus pneumoniae infection by negative regulation of gammadelta T cells // J Virol. 2012. V. 86. № 22. P. 12304-12312.
  17. Shahangian A., Chow E.K., Tian X., Kang J.R., Ghaffari A., Liu S.Y., Belperio J.A., Cheng G., Deng J.C. Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice // J Clin Invest. 2009. V. 119. № 7. P. 1910-1920.
  18. Cao J., Wang D., Xu F., Gong Y., Wang H., Song Z., Li D., Zhang H., Li D., Zhang L., Xia Y., Xu H., Lai X., Lin S., Zhang X., Ren G., Dai Y., Yin Y. Activation of IL-27 signalling promotes development of postinfluenza pneumococcal pneumonia // EMBO Mol Med. 2014. V. 6. № 1. P. 120-140.
  19. Nakamura S., Davis K.M., Weiser J.N. Synergistic stimulation of type I interferons during influenza virus coinfection promotes Streptococcus pneumoniae colonization in mice // J Clin Invest. 2011. V. 121. № 9. P. 3657-3665.
  20. Redford P.S., Mayer-Barber K.D., McNab F.W., Stavropoulos E., Wack A., Sher A., O'Garra A. Influenza A virus impairs control of Mycobacterium tuberculosis coinfection through a type I interferon receptor-dependent pathway // J Infect Dis. 2014. V. 209. № 2. P. 270-274.
  21. Есимова И.Е., Уразова О.И., Новицкий В.В., Хасанова Р.Р., Филинюк О.В. Секреция интерлейкинов IL-12, IL-27 мононуклеарными лейкоцитами и экспрессия их рецепторов на Т-лимфоцитах в условиях направленной индукции клеток in vitro при туберкулезе легких // Медицинская иммунология. 2014. Т. 16. № 3. С. 237-246.
  22. Hendaus M.A., Jomha E.A., Alhammadi A.H. Virus-induced secondary bacterial infection: a concise review // Ther Clin Risk Manag. 2015. V. 11. P. 1265-1271.
  23. Tief F., Hoppe C., Seeber L., Obermeier P., Chen X., Karsch K., Mühlhans S., Adamou E., Conrad T., Beresniak A., Schweiger B., Adam T., Rath B. An inception cohort study assessing the role of pneumococcal and other bacterial pathogens in children with influenza and ILI and a clinical decision model for stringent antibiotic use // Antivir Ther. 2016. V. 21. № 5. P. 413-424.
  24. Sloots T.P., Whiley M., Lambert S.B., Nissen M.D. Emerging respiratory agents: new viruses for old diseases? // J Clin Virol. 2008. V. 42. № 3. P. 233-243.
  25. Tregoning J.S., Schwarze J. Respiratory viral infections in infants: causes, clinical symptoms, virology, and immunology // Clin Microbiol Rev. 2010. V. 23. № 1. P. 74-98.
  26. Van der Zalm M.M., van Ewijk B.E., Wilbrink B., Uiterwaal C.S., Wolfs T.F., van der Ent C.K. Respiratory pathogens in children with and without respiratory symptoms // J Pediatr. 2009. V. 154. № 3. P. 396-400.
  27. Vareille M., Kieninger E., Edwards M.R., Regamey N. The airway epithelium: soldier in the fight against respiratory viruses // Clin Microbiol Rev. 2011. V. 24. № 1. P. 210-229.
  28. Voynow J.A., Rubin B.K. Mucins, mucus, and sputum // Chest. 2009. V. 135. № 2. P. 505-512.
  29. Thornton D.J., Rousseau K., McGuckin M.A. Structure and function of the polymeric mucins in airways mucus. Annu Rev Physiol. 2008. V. 70. P. 459-486.
  30. Соловьева Н.А., Кулакова Г.А., Курмаева Е.А. Мукоактивная терапия при лечении острых респираторных инфекций у детей // Практическая медицина. 2013. № 6 (75). С. 191-198.
  31. Pittet L.A., Hall-Stoodley L., Rutkowski M.R., Harmsen A.G. Influenza virus infection decrease stracheal mucociliary velocity and clearance of Streptococcus pneumoniae // Am J Respir Cell Mol Biol. 2010. V. 42. № 4. P. 450-460.
  32. Mallia P., Footitt J., Sotero R., Jepson A., Contoli M., Trujillo-Torralbo M.B., Kebadze T., Aniscenko J., Oleszkiewicz G., Gray K., Message S.D., Ito K., Barnes P.J., Adcock I.M., Papi A., Stanciu L.A., Elkin S.L., Kon O.M., Johnson M., Johnston S.L. Rhinovirus infection induces degradation of antimicrobial peptides and secondary bacterial infection in chronic obstructive pulmonary disease // Am J Respir Crit Care Med. 2012. V. 186. № 11. P. 1117-1124.
  33. Mallia P., Message S.D., Gielen V., Contoli M., Gray K., Kebadze T., Aniscenko J., Laza-Stanca V., Edwards M.R., Slater L., Papi A., Stanciu L.A., Kon O.M., Johnson M., Johnston S.L. Experimental rhinovirus infection as a human model of chronic obstructive pulmonary disease exacerbation // Am J Respir Crit Care Med. 2011. V. 183. № 6. P. 734-742.
  34. Akira S. Pathogen recognition by innate immunity and its signaling // Proc Jpn Acad Ser B Phys Biol Sci. 2009. V. 85. № 4. P. 143-156.
  35. Didierlaurent A., Goulding J., Patel S., Snelgrove R., Low L., Bebien M., Lawrence T., van Rijt L.S., Lambrecht B.N., Sirard J.C., Hussell T. Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory influenza infection // J Exp Med. 2008. V. 205. № 2. P. 323-329.
  36. Kanneganti T.D., Lamkanfi M., Nunez G. Intracellular NOD-like receptors in host defense and disease // Immunity. 2007. V. 27. P. 549-559.
  37. Message S.D., Johnston S.L. Host defense function of the airway epithelium in health and disease: clinical background // J Leukoc Biol. 2004. V. 75. № 1. P. 5-17.
  38. Ishizuka S., Yamaya M., Suzuki T., Takahashi H., Ida S., Sasaki T., Inoue D., Sekizawa K., Nishimura H., Sasaki H. Effects of rhinovirus infection on the adherence of Streptococcus pneumoniae to cultured human airway epithelial cells // J Infect Dis. 2003. V. 188. № 12. P. 1928-1939.
  39. Avadhanula V., Wang Y., Portner A., Adderson E. Non typeable Haemophilus influenzae and Streptococcus pneumoniae bind respiratory syncytial virus glycoprotein // J Med Microbiol. 2007. V. 56. P. 1133-1137.
  40. Fukasawa C., Ishiwada N., Ogita J., Hishiki H., Kohno Y. The effects of disodium cromoglycate on enhanced adherence of Haemophilus influenzae to A549 cells infected with respiratory syncytial virus // Pediatr Res. 2009. V. 66. № 2. P. 168-173.
  41. Van Ewijk B.E., Wolfs T.F., Aerts P.C., Van Kessel K.P., Fleer A., Kimpen J.L., Van der Ent C.K. RSV mediates Pseudomonas aeruginosa binding to cystic fibrosis and normal epithelial cells // Pediatr Res. 2007. V. 61. № 4. P. 398-403.
  42. Wang J.H., Kwon H.J., Jang Y.J. Rhinovirus enhances various bacterial adhesions to nasal epithelial cells simultaneously // Laryngoscope. 2009. V. 119. № 7. P. 1406-1411.
  43. Avadhanula V., Rodriguez C.A., Devincenzo J.P., Wang Y., Webby R.J., Ulett G.C., Adderson E.E. Respiratory viruses augment the adhesion of bacterial pathogens to respiratory epithelium in a viral species- and cell type-dependent manner // J Virol. 2006. V. 80. № 4. P. 1629.
  44. Kim Y.G., Park J.H., Reimer T., Baker D.P., Kawai T., Kumar H., Akira S., Wobus C., Núñez G. Viral infection augments Nod1/2 signaling to potentiate lethality // Cell Host Microbe. 2011. V. 9. № 6. P. 496-507.
  45. Heinrich A., Haarmann H., Zahradnik S., Frenzel K., Schreiber F., Klassert T.E., Heyl K.A., Endres A.-S., Schmidtke M., Hofmann J., Slevogt H. Moraxella catarrhalis decreases antiviral innate immune responses by down-regulation of TLR3 via inhibition of p53 in human bronchial epithelial cells // FASEB J. 2016. V. 30. № 6. P. 2426-2434.
  46. Doolittle J.M., Webster-Cyriaque J. Polymicrobial infection and bacterium-mediated epigenetic modification of DNA tumor viruses contribute to pathogenesis // mBio. 2014. V. 5. № 3. e01015-14.
  47. Bhende P.M., Seaman W.T., Delecluse H.J., Kenney S.C. BZLF1 activation of the methylated form of the BRLF1 immediate-early promoter is regulated by BZLF1 residue 186 // J Virol. 2005. V. 79. № 12. P. 7338-7348.
  48. Kepler G.M., Nguyen H.K., Webster-Cyriaque J., Banks H.T. A dynamic model for induced reactivation of latent virus // J Theor Biol. 2007. V. 244. № 3. P. 451-462.
  49. Morris T.L., Arnold R.R., Webster-Cyriaque J. Signaling cascades triggered by bacterial metabolic end products during reactivation of Kaposi’s sarcoma-associated herpesvirus // J Virol. 2007. V. 81. № 11. P. 6032-6042.
  50. Imai K., Inoue H., Tamura M., Cueno M.E., Inoue H., Takeichi O., Kusama K., Saito I., Ochiai K. The periodontal pathogen Porphyromonas gingivalis induces the Epstein-Barr virus lytic switch transactivator ZEBRA by histone modification // Biochimie. 2012. V. 94. № 3. P. 839-846.
  51. Imai K., Ogata Y., Ochiai K. Microbial interaction of periodontopathic bacteria and Epstein-Barr virus and their implication of periodontal diseases // J Oral Biosci. 2012. V. 54. № 3. P. 164-168.
  52. Fukayama M., Hino R., Uozaki H. Epstein-Barr virus and gastric carcinoma: virus-host interactions leading to carcinoma // Cancer Sci. 2008. V. 99. № 9. P. 1726-1733.
  53. Oue N., Oshimo Y., Nakayama H., Ito R., Yoshida K., Matsusaki K., Yasui W. DNA methylation of multiple genes in gastric carcinoma: association with histological type and CpG island methylator phenotype // Cancer Sci. 2003. V. 94. № 10. P. 901-905.
  54. Katayama Y., Takahashi M., Kuwayama H. Helicobacter pylori causes runx3 gene methylation and its loss of expression in gastric epithelial cells, which is mediated by nitric oxide produced by macrophages // Biochem Biophys Res Commun. 2009. V. 388. № 3. P. 496-500.
  55. Kitajima Y., Ohtaka K., Mitsuno M., Tanaka M., Sato S., Nakafusa Y., Miyazaki K. Helicobacter pylori infection is an independent risk factor for Runx3 methylation in gastric cancer // Oncol Rep. 2008. V. 19. № 1. P. 197-202.
  56. Chan A.O., Lam S.K., Wong B.C., Wong W.M., Yuen M.F., Yeung Y.H., Hui W.M., Rashid A., Kwong Y.L. Promoter methylation of E-cadherin gene in gastric mucosa associated with Helicobacter pylori infection and in gastric cancer // Gut. 2003. V. 52. № 4. P. 502-506.
  57. Wijnhoven B.P., Dinjens W.N., Pignatelli M. E-cadherin-catenin cell-cell adhesion complex and human cancer // Br J Surg. 2000. V. 87. № 8. P. 992-1005.
  58. Kusano M., Toyota M., Suzuki H., Akino K., Aoki F., Fujita M., Hosokawa M., Shinomura Y., Imai K., Tokino T. Genetic, epigenetic, and clinicopathologic features of gastric carcinomas with the CpG island methylator phenotype and an association with Epstein-Barr virus // Cancer. 2006. V. 106. № 7. P. 1467-1479.
  59. Sakuma K., Chong J.M., Sudo M., Ushiku T., Inoue Y., Shibahara J., Uozaki H., Nagai H., Fukayama M. High-density methylation of p14ARF and p16INK4A in Epstein-Barr virus-associated gastric carcinoma // Int J Cancer. 2004. V. 112. № 2. P. 273-278.
  60. Uthman M.M., Uthman O.A., Yahaya I. Interventions for the prevention of mycobacterium avium complex in adults and children with HIV // Cochrane Database Syst Rev. 2013. V. 30. № 4. CD007191.
  61. Gordon S. The macrophage: past, present and future // Eur J Immunol. 2007. V. 37. № 1. Р. 9-17.
  62. Maddocks S., Scandurra G.M., Nourse C., Bye C., Williams R.B., Slobedman D., Canningham A.L., Britton W.J. Gene expression in HIV-1/Mycobacterium tuberculosis co-infected macrophages is dominated by M. tuberculosis // Tuberculosis: Edinb. 2009. V. 89. № 4. Р. 285-293.
  63. Pathak S., Wentzel-Larsen T., Asjo B. Effects of in vitro HIV-1 infection on mycobacterial growth in peripheral blood monocyte-derived macrophages // Infect Immun. 2010. V. 78. № 9. P. 4022-4032.
  64. Tomlinson G.S., Bell L.C.K., Walker N.F., Tsang J., Brown J.S., Breen R., Lipman M., Katz D.R., Miller R.F., Chain B.M., Eikington P.T., Noursadeghi M. HIV-1 Infection of macrophages dysregulates innate immune responses to Mycobacterium tuberculosis by inhibition of interleukin-10 // J Infect Dis. 2014. V. 209. № 7. P. 1055-1065.
  65. Meremo A., Mshana S.E., Kidenya B.R., Kabangila R., Peck R., Kataraihya J.B. High prevalence of non-typhoid Salmonella bacteraemia among febrile HIV adult patients admitted at a tertiary hospital, north-western Tanzania // Int Arch Med. 2012. V. 5. № 1. P. 28-34.
  66. Reddy E.A., Reddy E.A., Shaw A.V., Crump J.A. Community-acquired bloodstream infections in Africa: a systematic review and meta-analysis // Lancet Infect Dis. 2010. V. 10. № 6. P. 417-432.
  67. Tabu C., Breiman R.F., Ochieng B., Aura D., Cosmas L., Audi A., Olack D., Bigogo G., Ongus J.R., Fields P., Mintz E., Burton D., Oundo J., Feikin D.R. Differing burden and epidemiology of non-Typhi Salmonella bacteremia in rural and urban Kenya // PLoS One. 2012. V. 7. № 2. e31237.
  68. Japiassu A.M., Amancio R.T., Mesquita E.C., Medeiros D.M., Bernal H.B., Nunes E.P., Luz P.M., Grinsztejn B., Bozza F.A. Sepsis is a major determinant of outcome in critically ill HIV/AIDS patients // Crit Care. 2010. V. 14. № 4. P. 152.
  69. Uhlenkott M.C., Buskin S.E., Kahle E.M., Barash E., Aboulafia D.M. Causes of death in the era of highly active antiretroviral therapy: a retrospective analysis of a hybrid hematology-oncology and HIV practice and the Seattle/King County adult/ adolescent spectrum of HIV-related diseases project // Am J Med Sci. 2008. V. 336. № 3. P. 217-223.
  70. Ramsetty S.K., Stuart L.L., Blake R.T., Parsons C.H., Salgado C.D. Risks for methicillin-resistant Staphylococcus aureus colonization or infection among patients with HIV infection // HIV Med. 2010. V. 11. № 6. P. 389-394.
  71. Crum-Cianflone N.F., Burgi A.A., Hale R.B. Increasing rates of community-acquired methicillin-resistant Staphylococcus aureus infections among HIV-infected persons // Int J STD AIDS. 2007. V. 18. № 8. P. 521-526.
  72. Gaskell K.M., Feasey N.A., Heyderman R.S. Management of severe non-TB bacterial infection in HIV-infected adults // Expert Rev Anti Infect Ther. 2015. V. 13. № 2. P. 183-195.
  73. Karp C.L., Auwaerter P.G. Coinfection with HIV and tropical infectious diseases. II. Helminthic, fungal, bacterial, and viral pathogens // Clin Infect Dis. 2007. V. 45. № 9. P. 1214-1220.
  74. Fortanier A.C., Venekamp R.P., Boonacker C.W., Hak E., Schilder A.G., Sanders E.A., Damoiseaux R.A. Pneumococcal conjugate vaccines for preventing otitis media // Cochrane Database Syst Rev. 2014. V. 4. CD001480.
  75. Nascimento-Carvalho C.M., Ribeiro C.T., Cardoso M.R., Barral A., Araújo-Neto C.A., Oliveira J.R., Sobral L.S., Viriato D., Souza A.L., Saukkoriipi A., Paldanius M., Vainionpää R., Leinonen M., Ruuskanen O. The role of respiratory viral infections among children hospitalized for community-acquired pneumonia in a developing country // Pediatr Infect Dis J. 2008. V. 27. № 10. P. 939-941.
  76. Peltola V.T., McCullers J.A. Respiratory viruses predisposing to bacterial infections: role of neuraminidase // Pediatr Infect Dis J. 2004. V. 23. Suppl 1. P. 87-97.
  77. Carbonell-Estrany X., Simões E.A., Dagan R., Hall C.D., Harris B., Hultquist M., Connor E.M., Losonsky G.A., Motavizumab Study Group. Motavizumab for prophylaxis of respiratory syncytial virus in high-risk children: a noninferiority trial // Pediatrics. 2010. V. 125. № 1. P. 35-51.
  78. Nair N., Biswas R., Götz F., Biswas L. Impact of Staphylococcus aureus on pathogenesis in polymicrobial infections // Infect Immun. 2014. V. 82. № 6. P. 2162-2169.
  79. Bassetti M., Ginocchio F., Mikulska M. New treatment options against gram-negative organisms // Crit Care. 2011. V. 15. № 2. P. 215-223.
  80. Ciofi Degli A.M., Bernaschi P., Carletti M., Luzzi I., Garcia-Fernandez A., Beryaina A., Sisyo A., Locatelli F., Raponi M. An outbreak of extremely drug-resistant Pseudomonas aeruginosa in a tertiary care pediatric hospital in Italy // BMC Infect Dis. 2014. V. 14. P. 494-501.
  81. Hraiech S., Hiblot J., Lafleur J., Lepidi H., Papazian L., Rolain J.M., Raoult D., Elias M., Silby M.W., Bzdrenga J., Bregeon F., Chabriere E. Inhaled lactonase reduces Pseudomonas aeruginosa quorum sensing and mortality in rat pneumonia // PLoS One. 2014. V. 9. № 10. e107125.
  82. Крылов С.В., Кропински А.М., Плетенева Е.А., Шабурова О.В., Буркальцева, М.В., Мирошников К.А., Крылов В.Н. Свойства нового D3 подобного бактериофага phiPMG1 Pseudomonas aeruginosa: структура генома и перспективы использования фага в фаготерапии // Генетика. 2012. Т. 48. № 9. C. 1057-1067.
  83. Mukherjee S., Brothers K.M., Shanks R.M., Kadouri D.E. Visualizing Bdellovibrio bacteriovogus by using the tdTomato Fluprescent Protein // Appl Environ Microbiol. 2015. V. 82. № 6. P. 1653-1661.
  84. Spain E.M., Núñez M.E., Kim H.J., Taylor R.J., Thomas N., Wengen M.B., Dalleska N.F., Bromley J.P., Schermerhom K.H., Ferguson M.A. Idenyification and differential production of ubiquinon-8 in the bacterial predator Bdellovibrio bacteriovorus // Res Microbiol. 2016. V. 167. № 5. P. 413-423.
  85. Скулачев В.П., Богачев А.В., Каспаринский Ф.О. Мембранная биоэнергетика. М.: Издательство Московского университета. 2010. 368 с.
  86. Zelaya H., Alvarez S., Kitazawa H., Villena J. Respiratory antiviral immunity and immunobiotics: beneficial effects on inflammation-coagulation interaction during influenza virus infection // Front immunol. 2016. V. 7. P. 633-648.
  87. Villena J., Saavedra L., Hebert E.M., Masumizu Y., Sato N., Humayun Kober A.K., Albarracin L., Clua P., Ikeda-Ohtsubo W., Kitazawa H. Draft genome sequence of Lactobacillus plantarum MPL16, a wakame-utilizing immunobiotic strain isolated from swine feces // Genome Announc. 2017. V. 5. № 10. e00006-17.
  88. Rynda-Apple A., Robinson K.M., Alcorn J.F. Influenza and bacterial superinfection: illuminating the immunologic mechanisms of disease // Infect Immun. 2015. V. 83. № 10. P. 3764-3770.

Copyright (c) 2018 Balmasova I.P., Malova E.S., Sepiashvili R.I.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies