Advertisement

Current trends in targeted therapy for drug-resistant infections

  • Leila Rahbarnia
  • Safar FarajniaEmail author
  • Behrooz Naghili
  • Vahideh Ahmadzadeh
  • Kamal Veisi
  • Roghayyeh Baghban
  • Sayna Toraby
Mini-Review
  • 11 Downloads

Abstract

Escalating antibiotic resistance is now a serious menace to global public health. It may be led to the emergence of “postantibiotic age” in which most of infections are untreatable. At present, there is an essential need to explore novel therapeutic strategies as a strong and sustainable pipeline to combat antibiotic-resistant infections. This review focuses on recent advances in this area including therapeutic antibodies, antimicrobial peptides, vaccines, gene therapy, genome editing, and phage therapy for tackling drug-resistant infections.

Keywords

Drug-resistant infections Antibody Antimicrobial peptides Vaccine Phage therapy Genome editing 

Notes

Funding information

This study was supported by Infectious and Tropical Diseases Research Center, Tabriz University of Medical Sciences, Tabriz, Iran.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Afacan NJ, Yeung AT, Pena OM, Hancock RE (2012) Therapeutic potential of host defense peptides in antibiotic-resistant infections. Curr Pharm Des 18(6):807–819CrossRefPubMedGoogle Scholar
  2. Ahonkhai VI, Lukacs LJ, Jonas LC, Matthews H, Vella PP, Ellis RW, Staub JM, Dolan KT, Rusk CM, Calandra GB (1990) Haemophilus influenzae type b conjugate vaccine (meningococcal protein conjugate)(PedvaxHIBTM): clinical evaluation. Pediatr. 85(4):676–681Google Scholar
  3. Alexander HE, Leidy G, Geof R, Rich D (1946) Hemophilus influenzae meningitis treated with streptomycin. JAMA. 132(8):434–440CrossRefGoogle Scholar
  4. Andersson DI, Hughes D, Kubicek-Sutherland JZ (2016) Mechanisms and consequences of bacterial resistance to antimicrobial peptides. Drug Resist Updat 26:43–57CrossRefPubMedGoogle Scholar
  5. Aoki W, Ueda M (2013) Characterization of antimicrobial peptides toward the development of novel antibiotics. Pharm. 6(8):1055–1081Google Scholar
  6. Baba MS, Zin NM, Hassan ZAA, Latip J, Pethick F, Hunter IS, Edrada-Ebel R, Herron PR (2015) In vivo antimalarial activity of the endophytic actinobacteria, Streptomyces SUK 10. J Microbiol 53(12):847–855CrossRefPubMedGoogle Scholar
  7. Bar-Or A, Vollmer T, Antel J, Arnold DL, Bodner CA, Campagnolo D, Gianettoni J, Jalili F, Kachuck N, Lapierre Y (2007) Induction of antigen-specific tolerance in multiple sclerosis after immunization with DNA encoding myelin basic protein in a randomized, placebo-controlled phase 1/2 trial. Arch Neurol 64(10):1407–1415CrossRefPubMedGoogle Scholar
  8. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233CrossRefPubMedPubMedCentralGoogle Scholar
  9. Baxter D (2007) Active and passive immunity, vaccine types, excipients and licensing. Occup Med 57(8):552–556CrossRefGoogle Scholar
  10. Beloor J, Maes N, Ullah I, Uchil P, Jackson A, Fikrig E, Lee SK, Kumar P (2018) Small interfering RNA-mediated control of virus replication in the CNS is therapeutic and enables natural immunity to West Nile virus. Cell Host Microbe 23(4):549–556Google Scholar
  11. Bhattacharyya S, Dey R, Majumder N, Bhattacharjee S, Majumdar S (2008) A novel approach to regulate experimental visceral leishmaniasis in murine macrophages using CCR5 siRNA. Scand J Immunol Suppl 67(4):345–353CrossRefGoogle Scholar
  12. Bikard D, Euler CW, Jiang W, Nussenzweig PM, Goldberg GW, Duportet X, Fischetti VA, Marraffini LA (2014) Exploiting CRISPR-Cas nucleases to produce sequence-specific antimicrobials. Nat Biotechnol 32(11):1146CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bitko V, Musiyenko A, Shulyayeva O, Barik S (2005) Inhibition of respiratory viruses by nasally administered siRNA. Nat Med 11(1):50CrossRefPubMedGoogle Scholar
  14. Blagbrough IS, Zara C (2009) Animal models for target diseases in gene therapy using DNA and siRNA delivery strategies. Pharm Res 26(1):1Google Scholar
  15. Boix V, Fedorak RN, Mullane KM, Pesant Y, Stoutenburgh U, Jin M, Adedoyin A, Chesnel L, Guris D, Larson KB, Murata Y (2017) Primary outcomes from a phase 3, randomized, double-blind, active-controlled trial of surotomycin in subjects with Clostridium difficile infection. Open Forum Infect Dis 4(1)Google Scholar
  16. Bourdin G, Navarro A, Sarker SA, Pittet A, Qadri F, Sultana S, Cravioto A, Talukder KA, Reuteler G, Brüssow H (2014) Coverage of diarrhoea associated Escherichia coli isolates from different origins with two types of phage cocktails. Microb Biotechnol 7(2):165–176CrossRefPubMedPubMedCentralGoogle Scholar
  17. Brault AC, Domi A, McDonald EM, Talmi-Frank D, McCurley N, Basu R, Robinson HL, Hellerstein M, Duggal NK, Bowen RA (2017) A Zika vaccine targeting NS1 protein protects immunocompetent adult mice in a lethal challenge model. Sci Rep 7(1):14769Google Scholar
  18. Butler MS, Blaskovich MA, Cooper MA (2017) Antibiotics in the clinical pipeline at the end of 2015. J Antibiot 70(1):3CrossRefPubMedGoogle Scholar
  19. Capela EV, Aires-Barros MR, Freire MG, Azevedo AM (2017) Monoclonal antibodies—addressing the challenges on the manufacturing processing of an advanced class of therapeutic agents. Front Clini Drug Res Anti Infect 4(4):142CrossRefGoogle Scholar
  20. Casadevall A, Scharff MD (1994) Serum therapy revisited: animal models of infection and development of passive antibody therapy. J Antimicrob Agents Chem 38(8):1695CrossRefGoogle Scholar
  21. Cassini A, Högberg LD, Plachouras D, Quattrocchi A, Hoxha A, Simonsen GS, Colomb-Cotinat M, Kretzschmar ME, Devleesschauwer B, Cecchini M, Ouakrim DA (2019) Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. Lancet Infect Dis 19(1)56–66Google Scholar
  22. Citorik RJ, Mimee M, Lu TK (2014) Sequence-specific antimicrobials using efficiently delivered RNA-guided nucleases. Nat Biotechnol 32(11):1141Google Scholar
  23. Clem AS (2011) Fundamentals of vaccine immunology. J Glob Infect Dis 3(1):73CrossRefPubMedPubMedCentralGoogle Scholar
  24. Cooper B, DeTora L, Stoddard J (2011) Menveo®: a novel quadrivalent meningococcal CRM197 conjugate vaccine against serogroups A, C, W-135 and Y. Expert Rev Vaccines 10(1):21–33CrossRefPubMedGoogle Scholar
  25. Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74(3):417–433CrossRefPubMedPubMedCentralGoogle Scholar
  26. Deeks ED (2010) Meningococcal quadrivalent (serogroups A, C, W135, and Y) conjugate vaccine (Menveo). BioDrugs 24(5):287–297Google Scholar
  27. Donlan RM (2009) Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol 17(2):66–72CrossRefPubMedGoogle Scholar
  28. Dubos RJ (1939) Studies on a bactericidal agent extracted from a soil bacillus: I. Preparation of the agent. Its activity in vitro. J Exp Med 70(1):1CrossRefPubMedPubMedCentralGoogle Scholar
  29. Dyawanapelly S, Ghodke SB, Vishwanathan R, Dandekar P, Jain R (2014) RNA interference-based therapeutics: molecular platforms for infectious diseases. J Biomed Nanotechnol 10(9):1998–2037CrossRefPubMedGoogle Scholar
  30. Eisenstein M (2011) A moving target. Nature. 474:S16–S17CrossRefPubMedGoogle Scholar
  31. El Chakhtoura NG, Saade E, Iovleva A, Yasmin M, Wilson B, Perez F, Bonomo RA (2018) Therapies for multidrug resistant and extensively drug-resistant non-fermenting gram-negative bacteria causing nosocomial infections: a perilous journey toward molecularly targeted therapy. Expert Rev Anti-Infect Ther 16(2):89–110CrossRefPubMedPubMedCentralGoogle Scholar
  32. Eyvazi S, Farajnia S, Dastmalchi S, Kanipour F, Zarredar H, Bandehpour M (2018) Antibody based EpCAM targeted therapy of cancer, review and update. Curr Cancer Drug Targets 18(9):857–868CrossRefPubMedGoogle Scholar
  33. Farajnia S, Rahbarnia L, Alimohammadian MH, Abdoli OS, Beh-pajooh A, Saeedi N, Montazer SS (2011) Molecular cloning and characterization of P4 nuclease from Leishmania infantum. Enzyme Res 2011:1–6CrossRefGoogle Scholar
  34. Fish R, Kutter E, Wheat G, Blasdel B, Kutateladze M, Kuhl S (2016) Bacteriophage treatment of intransigent diabetic toe ulcers: a case series. J Wound Care 25(Sup7):S27–S33CrossRefGoogle Scholar
  35. Girard MP, Tam JS, Pervikov Y, Katz JM (2013) Report on the first WHO integrated meeting on development and clinical trials of influenza vaccines that induce broadly protective and long-lasting immune responses: Hong Kong SAR, China, 24–26 January 2013. Vaccine. 31(37):3766–3771CrossRefPubMedGoogle Scholar
  36. Graham BS, Ambrosino DM (2015) History of passive antibody administration for prevention and treatment of infectious diseases. Curr Opin HIV AIDS 10(3):129CrossRefPubMedPubMedCentralGoogle Scholar
  37. Greenwood B (2014) The contribution of vaccination to global health: past, present and future. Phil Trans R Soc B 369(1645):20130433CrossRefPubMedGoogle Scholar
  38. Hammon WM, Coriell LL, Ludwig EH, McAllister RM, Greene AE, Sather GE, Wehrle PF (1954) Evaluation of Red Cross gamma globulin as a prophylactic agent for poliomyelitis: 5. Reanalysis of results based on laboratory-confirmed cases. J JAMA 156(1):21–27CrossRefGoogle Scholar
  39. Harrison RA, Bianco AE (2000) DNA immunization with Onchocerca volvulus genes, Ov-tmy-1 and OvB20: serological and parasitological outcomes following intramuscular or GeneGun delivery in a mouse model of onchocerciasis. Parasite Immunol 22(5):249–257Google Scholar
  40. Hashemzehi R, Doosti A, Kargar M, Jaafarinia M (2018) Cloning and expression of nlpA gene as DNA vaccine candidate against Acinetobacter baumannii. Mol Biol Rep:1–7Google Scholar
  41. Henein A (2013) What are the limitations on the wider therapeutic use of phage? Bacteriophage 3(2):e24872CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hilleman MR (1987) Yeast recombinant hepatitis B vaccine. Infection 15(1):3–7Google Scholar
  43. Huang W, Yao Y, Long Q, Yang X, Sun W, Liu C, Jin X, Chu X, Chen B, Ma Y (2014) Immunization against multidrug-resistant Acinetobacter baumannii effectively protects mice in both pneumonia and sepsis models. PloS one 9(6):e100727CrossRefPubMedPubMedCentralGoogle Scholar
  44. Hudu SA, Shinkafi SH, Shua U (2016) An overview of recombinant vaccine technology, adjuvants and vaccine delivery methods. Int J Pharm Pharm Sci 8:19–24CrossRefGoogle Scholar
  45. Infectious Diseases Society of America (IDSA) (2011) Combating antimicrobial resistance: policy recommendations to save lives. Clin Infect Dis 52(suppl_5):S397–S428CrossRefGoogle Scholar
  46. Isken O, Maquat LE (2007) Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev 21(15):1833–3856CrossRefPubMedGoogle Scholar
  47. Islam MA, Firdous J, Choi YJ, Yun CH, Cho CS (2014) Regulation of endocytosis by non-viral vectors for efficient gene activity. J biomed Nanotechnol 10(1):67–80CrossRefPubMedGoogle Scholar
  48. Jacobs WR, Snapper SB, Lugosi L, Bloom BR (1990) “Development of BCG as a recombinant vaccine vehicle,” in T-cell paradigms in parasitic and bacterial infections. Springer 153-160Google Scholar
  49. Janeway CA (1945) Use of concentrated human serum β-globulin in the prevention and attenuation of measles. Bull N Y Acad Med 21(4):202PubMedPubMedCentralGoogle Scholar
  50. Jenssen H, Hamill P, Hancock RE (2006) Peptide antimicrobial agents. Clin Microbiol Rep 19(3):491–511CrossRefGoogle Scholar
  51. Kallerup RS, Foged C (2015) Classification of vaccines. In: Subunit vaccine delivery. Springer, Berlin, pp 15–29Google Scholar
  52. Khatri NI, Rathi MN, Baradia DP, Trehan S, Misra A (2012) In vivo delivery aspects of miRNA, shRNA and siRNA. Crit Rev Ther Drug Carrier Syst 29(6):487–527CrossRefPubMedGoogle Scholar
  53. Kim H, Kim HR, Kim NR, Jeong BJ, Lee JS, Jang S, Chung DK (2015) Oral administration of Lactobacillus plantarum lysates attenuates the development of atopic dermatitis lesions in mouse models. J Microbiol 53(1):47–52Google Scholar
  54. Köhler G, Milstein C (1975) Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256(5517):495CrossRefPubMedGoogle Scholar
  55. Kucherlapati RS, Eves EM, Song KY, Morse BS, Smithies O (1984) Homologous recombination between plasmids in mammalian cells can be enhanced by treatment of input DNA. Proc Natl Acad Sci 81(10):3153–3157CrossRefPubMedGoogle Scholar
  56. Kudrimoti M, Curtis A, Azawi S, Worden F, Katz S, Adkins D, Bonomi M, Scott Z, Elder J, Sonis ST (2017) Dusquetide: reduction in oral mucositis associated with enduring ancillary benefits in tumor resolution and decreased mortality in head and neck cancer patients. Biotechnol Rep 15:24–26CrossRefGoogle Scholar
  57. Kumar M (2016) Multidrug-resistant Staphylococcus aureus, India, 2013-2015. Emerg Infect Dis 22(9):1666CrossRefPubMedPubMedCentralGoogle Scholar
  58. Lam JK, Chow MY, Zhang Y, Leung SW (2015) siRNA versus miRNA as therapeutics for gene silencing. Mol Ther Nucleic Acids 4Google Scholar
  59. Lambracht-Washington D, Rosenberg RN (2012) Active DNA Aâ42 vaccination as immunotherapy for Alzheimer disease. Transl Neurosci 3(4):307–313CrossRefPubMedPubMedCentralGoogle Scholar
  60. Lebbink RJ, De Jong DC, Wolters F, Kruse EM, Van Ham PM, Wiertz EJ, Nijhuis M (2017) A combinational CRISPR/Cas9 gene-editing approach can halt HIV replication and prevent viral escape. Sci Rep 7:41968CrossRefPubMedPubMedCentralGoogle Scholar
  61. Lenhard JR, Bulman ZP, Tsuji BT, Kaye KS (2019) Shifting gears: the future of polymyxin antibiotics. Antibiotics 8(2):42Google Scholar
  62. Lenoir AA, Granoff PD, Granoff DM (1987) Immunogenicity of Haemophilus influenzae type b polysaccharide-Neisseria meningitidis outer membrane protein conjugate vaccine in 2-to 6-month-old infants. Pediatr. 80(2):283–287Google Scholar
  63. Lewis K (2013) Platforms for antibiotic discovery. Nat Rev Drug Discov 12(5):371CrossRefPubMedGoogle Scholar
  64. Li J, Koh JJ, Liu S, Lakshminarayanan R, Verma CS, Beuerman RW (2017) Membrane active antimicrobial peptides: translating mechanistic insights to design. Front Neurosci 11:73PubMedPubMedCentralGoogle Scholar
  65. Lin DM, Koskella B, Lin HC (2017) Phage therapy: an alternative to antibiotics in the age of multi-drug resistance. World J Gastrointest Pharmacol Ther 8(3):162CrossRefPubMedPubMedCentralGoogle Scholar
  66. Mak TW, Saunders ME (2005) The immune response: basic and clinical principles. Academic Press, CambridgeGoogle Scholar
  67. McCafferty J, Griffiths AD, Winter G, Chiswell DJ (1990) Phage antibodies: filamentous phage displaying antibody variable domains. Nature 348(6301):552CrossRefPubMedGoogle Scholar
  68. McCaffrey AP, Meuse L, Pham TT, Conklin DS, Hannon GJ, Kay MA (2002) Gene expression: RNA interference in adult mice. Nature 418(6893):38CrossRefPubMedGoogle Scholar
  69. McConnell MJ, Jerónimo P (2010) Active and passive immunization against Acinetobacter baumannii using an inactivated whole cell vaccine. Vaccine. 29(1):1–5CrossRefPubMedGoogle Scholar
  70. McConnell MJ, Rumbo C, Bou G, Pachón J (2011) Outer membrane vesicles as an acellular vaccine against Acinetobacter baumannii. Vaccine. 29(34):5705–5710CrossRefPubMedGoogle Scholar
  71. Migone TS, Subramanian GM, Zhong J, Healey LM, Corey A, Devalaraja M, Lo L, Ullrich S, Zimmerman J, Chen A (2009) Raxibacumab for the treatment of inhalational anthrax. New Eng j med 361(2):135–144CrossRefPubMedGoogle Scholar
  72. Mnif S, Jardak M, Graiet I, Abid S, Driss D, Kharrat N (2019) The novel cationic cell-penetrating peptide PEP-NJSM is highly active against Staphylococcus epidermidis biofilm. Int J Biol Macromol 125:262–269CrossRefPubMedGoogle Scholar
  73. Molchanova N, Hansen PR, Franzyk H (2017) Advances in development of antimicrobial peptidomimetics as potential drugs. Molecules 22(9):1430CrossRefPubMedCentralGoogle Scholar
  74. Naafs MA (2018) The antimicrobial peptides: ready for clinical trials? Biomed J Sci Tech Res:1–4Google Scholar
  75. Navalkele BD, Chopra T (2018) Bezlotoxumab: an emerging monoclonal antibody therapy for prevention of recurrent Clostridium difficile infection. Biologics. 12:11PubMedPubMedCentralGoogle Scholar
  76. Oh YK, Park TG (2009) siRNA delivery systems for cancer treatment. Adv Drug Deliv Rev 61(10):850–862CrossRefPubMedGoogle Scholar
  77. Okuda K, Wada Y, Shimada M (2014) Recent developments in preclinical DNA vaccination. Vaccines. 2(1):89–106CrossRefPubMedPubMedCentralGoogle Scholar
  78. Oliveira H, Vilas BD, Sp M, Kluskens LD, Lavigne R, Sillankorva S, Secundo F, Azeredo J (2016) Structural and enzymatic characterization of ABgp46, a novel phage endolysin with broad anti-gram-negative bacterial activity. Front Microbiol 7:208PubMedPubMedCentralGoogle Scholar
  79. Pace D.,Pollard AJ., 2007. Meningococcal A, C, Y and W-135 polysaccharide-protein conjugate vaccines. Arch Dis Child . 92, (10) 909–915Google Scholar
  80. Papadopoulou A, von Felten S, Traud S, Rahman A, Quan J, King R, Garren H, Steinman L, Cutter G, Kappos L (2012) Evolution of MS lesions to black holes under DNA vaccine treatment. J Neurol 259(7):1375–1382CrossRefPubMedGoogle Scholar
  81. Patel A, Park DH, Davis CW, Smith TR, Leung A, Tierney K, Bryan A, Davidson E, Yu X, Racine T (2018) In vivo delivery of synthetic human DNA-encoded monoclonal antibodies protect against Ebola virus infection in a mouse model. Cell Rep 25(7):1982–1993Google Scholar
  82. Pehrsson EC, Tsukayama P, Patel S, Mejía-Bautista M, Sosa-Soto G, Navarrete KM, Calderon M, Cabrera L, Hoyos-Arango W, Bertoli MT (2016) Interconnected microbiomes and resistomes in low-income human habitats. Nature 533(7602):212CrossRefPubMedPubMedCentralGoogle Scholar
  83. Petrosillo N, Granata G, Cataldo MA (2018) Novel antimicrobials for the treatment of Clostridium difficile infection. Front Med 5:96Google Scholar
  84. Plosker GL (2014) 10-valent pneumococcal non-typeable haemophilus influenzae protein D-conjugate vaccine: a review in infants and children. Paediatr Drugs 16(5):425–444CrossRefPubMedGoogle Scholar
  85. Pöri, Pinja (2018) Development of Vaccines. theseus.fiGoogle Scholar
  86. Price AA, Sampson TR, Ratner HK, Grakoui A, Weiss DS (2015) Cas9-mediated targeting of viral RNA in eukaryotic cells. Proc Natl Acad Sci 112(19):6164–6169CrossRefPubMedGoogle Scholar
  87. Pushparaj PN, Aarthi JJ, Manikandan J, Kumar SD (2008) siRNA, miRNA, and shRNA: in vivo applications. J Dent Res 87(11):992–1003CrossRefPubMedGoogle Scholar
  88. Rabanal F, Cajal Y (2016) Therapeutic potential of antimicrobial peptides. In: New weapons to control bacterial growth. Springer, Berlin, pp 433–451CrossRefGoogle Scholar
  89. Rabanal F, Cajal Y (2017) Recent advances and perspectives in the design and development of polymyxins. Nat Prod Rep 34(7):886–908Google Scholar
  90. Raedler LA (2018) Shingrix (zoster vaccine recombinant) a new vaccine approved for herpes zoster prevention in older adults. Am Health Drug Benefits 11Google Scholar
  91. Rahbarnia L, Farajnia S, Naghili B (2012) Application of DsbA signal peptide for soluble expression of Leishmania infantum P4 nuclease in E. coli. Asian J Anim Vet Adv 7(4):326–333CrossRefGoogle Scholar
  92. Rahbarnia L, Farajnia S, Babaei H, Majidi J, Veisi K, Ahdi KS, Tanomand A (2017a) Development of a novel human scFv against EGFR L2 domain by phage display technology. Curr Pharma Des 23(13):2009–2014CrossRefGoogle Scholar
  93. Rahbarnia L, Farajnia S, Babaei H, Majidi J, Veisi K, Ahmadzadeh V, Akbari B (2017b) Evolution of phage display technology: from discovery to application. J Drug Target 25(3):216–224CrossRefPubMedGoogle Scholar
  94. Rappuoli R, Bottomley MJ, D’oro U, Finco O, De Gregorio E (2016) Reverse vaccinology 2.0: human immunology instructs vaccine antigen design. J Exp Med 213(4):469–481CrossRefPubMedPubMedCentralGoogle Scholar
  95. Ravanfar P, Satyaprakash A, Creed R, Mendoza N (2009) Existing antiviral vaccines. Dermatol Ther 22(2):110–128CrossRefPubMedGoogle Scholar
  96. Regeimbal JM, Jacobs AC, Corey BW, Henry MS, Thompson MG, Pavlicek RL, Quinones J, Hannah RM, Ghebremedhin M, Crane NJ (2016) Personalized therapeutic cocktail of wild environmental phages rescues mice from A. baumannii wound infections. Antimicrob Agents Chem AAC-02877Google Scholar
  97. Riedel, S. 2005. Edward Jenner and the history of smallpox and vaccination, Proc (Bayl Univ Med Cent) 1st edn, 18, (1), 21–25 Taylor & Francis DidcotGoogle Scholar
  98. Riley MK, Vermerris W (2017) Recent advances in nanomaterials for gene delivery review. Nanomaterials 7(5):94CrossRefPubMedCentralGoogle Scholar
  99. Robinson KA, Beverley SM (2003) Improvements in transfection efficiency and tests of RNA interference (RNAi) approaches in the protozoan parasite Leishmania. Mol Biochem Parasitol 128(2):217–228CrossRefPubMedGoogle Scholar
  100. Rodrigues M, Hullahalli K, Palmer K (2017) CRISPR-mediated removal of antibiotic resistance genes in Enterococcus faecalis populations. FASEB J 31(1_supplement):909-3Google Scholar
  101. Rouet P, Smih F, Jasin M (1994) Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol Cell Biol 14(12):8096–8106CrossRefPubMedPubMedCentralGoogle Scholar
  102. Ryther RCC, Flynt AS, Phillips Iii JA, Patton JG (2005) siRNA therapeutics: big potential from small RNAs. Gene Ther 12(1):5CrossRefPubMedGoogle Scholar
  103. Safari F, Farajnia S, Arya M, Zarredar H, Nasrolahi A (2018) CRISPR and personalized Treg therapy: new insights into the treatment of rheumatoid arthritis. Immunopharmacol Immunotoxicol 40(3):201–211CrossRefPubMedGoogle Scholar
  104. Schmelcher M, Shen Y, Nelson DC, Eugster MR, Eichenseher F, Hanke DC, Loessner MJ, Dong S, Pritchard DG, Lee JC (2015) Evolutionarily distinct bacteriophage endolysins featuring conserved peptidoglycan cleavage sites protect mice from MRSA infection. J Antimicrob Chemother 70(5):1453–1465CrossRefPubMedPubMedCentralGoogle Scholar
  105. Scott, Cheryl (2004) Classifying vaccines. BioProcesses Inter:14–23Google Scholar
  106. Semple SC, Akinc A, Chen J, Sandhu AP, Mui BL, Cho CK, Sah DW, Stebbing D, Crosley EJ, Yaworski E (2010) Rational design of cationic lipids for siRNA delivery. Nature Biotechnol 28(2):172CrossRefGoogle Scholar
  107. Shi X, Lu W, Wang Z, Pan L, Cui G, Xu J, LaBean TH (2014) Programmable DNA tile self-assembly using a hierarchical sub-tile strategy. Nanotechnology 25(7):075602CrossRefPubMedGoogle Scholar
  108. Shinefield HR (2010) Overview of the development and current use of CRM197 conjugate vaccines for pediatric use. Vaccine. 28(27):4335–4339CrossRefPubMedGoogle Scholar
  109. Sierra JM, Ester F, Rabanal F, Vinuesa T, Viñas M (2017) An overview of antimicrobial peptides and the latest advances in their development. Expert Opin Biol Ther 17(6):663–676CrossRefPubMedGoogle Scholar
  110. Sievert DM, Rudrik JT, Patel JB, McDonald LC, Wilkins MJ, Hageman JC (2008) Vancomycin-resistant Staphylococcus aureus in the United States, 2002-2006. Clin Infect Dis 46(5):668–674CrossRefPubMedGoogle Scholar
  111. Slade BA, Leidel L, Vellozzi C, Woo EJ, Hua W, Sutherland A, Izurieta HS, Ball R, Miller N, Braun MM (2009) Postlicensure safety surveillance for quadrivalent human papillomavirus recombinant vaccine. Jama. 302(7):750–757CrossRefPubMedGoogle Scholar
  112. Steiner H, Hultmark D, Engström Å, Bennich H, Boman HG (1981) Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 292(5820):246CrossRefGoogle Scholar
  113. Sucher AJ, Chahine EB, Nelson M, Sucher BJ (2011) Prevnar 13, the new 13-valent pneumococcal conjugate vaccine. Ann Pharmacother 45(12):1516–1524CrossRefPubMedGoogle Scholar
  114. Thomas M, Lu JJ, Chen J, Klibanov AM (2007) Non-viral siRNA delivery to the lung. Adv Drug Deliv Rev 59(2–3):124–133CrossRefPubMedGoogle Scholar
  115. Trevisan M, Palù G, Barzon L (2017) Genome editing technologies to fight infectious diseases. Expert Rev Anti-Infect Ther 15(11):1001–1013CrossRefPubMedGoogle Scholar
  116. Vartak A, Sucheck SJ (2016) Recent advances in subunit vaccine carriers. Vaccines 4(2):12CrossRefPubMedCentralGoogle Scholar
  117. Wang J, Lu Z, Wientjes MG, Au JLS (2010) Delivery of siRNA therapeutics: barriers and carriers. AAPS J 12(4):492–503CrossRefPubMedPubMedCentralGoogle Scholar
  118. Wang Y, Chen CH, Hu D, Ulmschneider MB, Ulmschneider JP (2016) Spontaneous formation of structurally diverse membrane channel architectures from a single antimicrobial peptide. Nature Commun 7:13535CrossRefGoogle Scholar
  119. Whitehead KA, Langer R, Anderson DG (2009) Knocking down barriers: advances in siRNA delivery. Nat Rev Drug Discov 8(2):129CrossRefGoogle Scholar
  120. Winau F, Winau R (2002) Emil von Behring and serum therapy. Microbes Infect 4(2):185–188CrossRefPubMedGoogle Scholar
  121. World Health Organization (2017) WHO guidelines on use of medically important antimicrobials in food-producing animalsGoogle Scholar
  122. Xu H, Xing J, Tang X, Sheng X, Zhan W (2019) Intramuscular administration of a DNA vaccine encoding OmpK antigen induces humoral and cellular immune responses in flounder (Paralichthys olivaceus) and improves protection against Vibrio anguillarum. Fish Shellfish Immunol 86:618–626Google Scholar
  123. Yanagihara K, Tashiro M, Fukuda Y, Ohno H, Higashiyama Y, Miyazaki Y, Hirakata Y, Tomono K, Mizuta Y, Tsukamoto K (2005) Effects of short interfering RNA against methicillin-resistant Staphylococcus aureus coagulase in vitro and in vivo. J Antimicrob Chemother 57(1):122–126CrossRefPubMedGoogle Scholar
  124. Yeaman MR, Yount NY (2003) Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 55(1):27–55CrossRefGoogle Scholar
  125. Yih WK, Nordin JD, Kulldorff M, Lewis E, Lieu TA, Shi P, Weintraub ES (2009) An assessment of the safety of adolescent and adult tetanus–diphtheria–acellular pertussis (Tdap) vaccine, using active surveillance for adverse events in the Vaccine Safety Datalink. Vaccine. 27(32):4257–4262CrossRefPubMedGoogle Scholar
  126. Zaiou M (2007) Multifunctional antimicrobial peptides: therapeutic targets in several human diseases. J Mol Med 85(4):317–329CrossRefPubMedGoogle Scholar
  127. Zarredar H, Pashapour S, Ansarin K, Khalili M, Baghban R, Farajnia S (2019) Combination therapy with KRAS siRNA and EGFR inhibitor AZD8931 suppresses lung cancer cell growth in vitro. J Cell Physiol 234(2):1560–1566CrossRefPubMedGoogle Scholar
  128. Zasloff M, Martin B, Chen HC (1988) Antimicrobial activity of synthetic magainin peptides and several analogues. Proceed Nat l Acad Sci 85(3):910–913CrossRefGoogle Scholar
  129. Zeng L, Wang D, Hu N, Zhu Q, Chen K, Dong K, Zhang Y, Yao Y, Guo X, Chang YF (2017) A novel pan-genome reverse vaccinology approach employing a negative-selection strategy for screening surface-exposed antigens against leptospirosis. Front Microbiol 8:396PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Infectious and Tropical Diseases Research CenterTabriz University of Medical SciencesTabrizIran
  2. 2.Drug Applied Research CenterTabriz University of Medical SciencesTabrizIran
  3. 3.Department of Medical Biotechnology, Faculty of MedicineKermanshah University of Medical SciencesKermanshahIran
  4. 4.Biotechnology Department, School of Advanced Technologies in MedicineShahid Beheshti University of Medical SciencesTehranIran
  5. 5.Biotechnology Research CenterTabriz University of Medical SciencesTabrizIran
  6. 6.Immunology Research CenterTabriz, University of Medical SciencesTabrizIran

Personalised recommendations