Cited by 134Bacteriophages and microbial interactionsImmunotherapy and Immune Responsesvaccines and immunoinformatics approaches

Phage display as a tool for vaccine and immunotherapy development

Open access
Hess, Krystina L., Jewell, Christopher M.·2020·Bioengineering & Translational Medicine

Abstract

Bacteriophages, or phages, are viruses that specifically infect bacteria and coopt the cellular machinery to create more phage proteins, eventually resulting in the release of new phage particles. Phages are heavily utilized in bioengineering for applications ranging from tissue engineering scaffolds to immune signal delivery. Of specific interest to vaccines and immunotherapies, phages have demonstrated an ability to activate both the innate and adaptive immune systems. The genome of these viral particles can be harnessed for DNA vaccination, or the surface proteins can be exploited for antigen display. More specifically, genes that encode an antigen of interest can be spliced into the phage genome, allowing antigenic proteins or peptides to be displayed by fusion to phage capsid proteins. Phages therefore present antigens to immune cells in a highly ordered and repetitive manner. This review discusses the use of phage with adjuvanting activity as antigen delivery vehicles for vaccination against infectious disease and cancer.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1002/btm2.10142

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Phage display technologies allow phages to be engineered to express tumor-associated antigens or immunostimulatory peptides on their capsid surfaces.

    “Phage display technologies allow phages to be engineered to express tumor-associated antigens or immunostimulatory peptides on their capsid surfaces [15,76–78]”

    From Phage therapy in oncology: opportunities for cancer prevention and treatment (2026) · cites this paper as [78]

    The section “Phage genomes can be modified to promote display of foreign antigens” (page unavailable) explains that engineered peptide or protein sequences are displayed on the phage surface. “Phage as a tumor antigen display tool > T7 phage” gives a tumor-associated peptide displayed on a capsid protein. The copy does not establish the separate claim that phages are engineered to display immunostimulatory peptides; its immunostimulatory surface-display example is a (glyco)lipid. (LLM, conf=0.82)

    Experimental — accuracy not yet measured
  • Phage platforms can function as standalone cancer vaccines or as adjuvants that enhance the efficacy of immune checkpoint blockade.

    “Such platforms can function as standalone cancer vaccines or as adjuvants that enhance the efficacy of immune checkpoint blockade [49,76,78,79]”

    From Phage therapy in oncology: opportunities for cancer prevention and treatment (2026) · cites this paper as [78]

    The “Phage as a tumor antigen display tool” section describes phage-based cancer vaccines that reduced tumors or metastases in mice. Its Qβ phage subsection also reports reduced tumor volume when phage immunization was combined with checkpoint blockade, but it does not establish that phages enhanced blockade’s efficacy relative to blockade alone. (LLM, conf=0.85)

    Experimental — accuracy not yet measured
  • By enhancing tumor antigen visibility and stimulating recruitment and activation of immune effector cells, phages can potentiate antitumor immune responses.

    “By enhancing tumor antigen visibility and stimulating the recruitment and activation of immune effector cells, phages can potentiate antitumor immune responses [15,77,78]”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 104

  1. [1]Bao Q, Li X, Han G, Zhu Y, Mao C, Yang M. Phage‐based vaccines. Adv Drug Deliv Rev. 2018 10.1016/j.addr.2018.12.013. 30594492 · DOI
  2. [2]Lin DM, Koskella B, Lin HC. Phage therapy: an alternative to antibiotics in the age of multi‐drug resistance. World J Gastrointest Pharmacol Ther. 2017; 8(3): 162‐ 173. 10.4292/wjgpt.v8.i3.162. 28828194 PMC5547374 · DOI
  3. [3]Deng X, Wang L, You X, Dai P, Zeng Y. Advances in the T7 phage display system (review). Mol Med Rep. 2018; 17(1): 714‐ 720. 10.3892/mmr.2017.7994. 29115536 · DOI
  4. [4]Ghosh D, Kohli AG, Moser F, Endy D, Belcher AM. Refactored M13 bacteriophage as a platform for tumor cell imaging and drug delivery. ACS Synth Biol. 2012; 1(12): 576‐ 582. 10.1021/sb300052u. 23656279 PMC3905571 · DOI
  5. [5]Lee YJ, Yi H, Kim W‐J, et al. Fabricating genetically engineered high‐power lithium‐ion batteries using multiple virus genes. Science. 2009; 324(5930): 1051‐ 1055. 10.1126/science.1171541. 19342549 · DOI
  6. [6]Nam KT, Kim D‐W, Yoo PJ, et al. Virus‐enabled synthesis and assembly of nanowires for lithium ion battery electrodes. Science. 2006; 312(5775): 885‐ 888. 10.1126/science.1122716. 16601154 · DOI
  7. [7]Karimi M, Mirshekari H, Moosavi Basri SM, Bahrami S, Moghoofei M, Hamblin MR. Bacteriophages and phage‐inspired nanocarriers for targeted delivery of therapeutic cargos. Adv Drug Deliv Rev. 2016; 106: 45‐ 62. 10.1016/j.addr.2016.03.003. 26994592 PMC5026880 · DOI
  8. [8]Oakes RS, Froimchuk E, Jewell CM. Engineering Biomaterials to Direct Innate Immunity. Adv Therap. 2019; 2: 1800157 10.1002/adtp.201800157 PMC6590522 31236439 · DOI
  9. [9]Chang TZ, Diambou I, Kim JR, Wang B, Champion JA. Host‐ and pathogen‐derived adjuvant coatings on protein nanoparticle vaccines. Bioeng Transl Med. 2017; 2(1): 120‐ 130. 10.1002/btm2.10052. 28516165 PMC5412930 · DOI
  10. [10]Hess KL, Andorko JI, Tostanoski LH, Jewell CM. Polyplexes assembled from self‐peptides and regulatory nucleic acids blunt toll‐like receptor signaling to combat autoimmunity. Biomaterials. 2017; 118: 51‐ 62. 10.1016/j.biomaterials.2016.11.052. 27940382 PMC5189983 · DOI
  11. [11]Krut O, Bekeredjian‐Ding I. Contribution of the immune response to phage therapy. J Immunol. 2018; 200(9): 3037‐ 3044. 10.4049/jimmunol.1701745. 29685950 · DOI
  12. [12]Tao P, Zhu J, Mahalingam M, Batra H, Rao VB. Bacteriophage T4 nanoparticles for vaccine delivery against infectious diseases. Adv Drug Deliv Rev. 2018 10.1016/j.addr.2018.06.025. PMC6759415 29981801 · DOI
  13. [13]Semler DD, Goudie AD, Finlay WH, Dennis JJ. Aerosol phage therapy efficacy in Burkholderia cepacia complex respiratory infections. Antimicrob Agents Chemother. 2014; 58(7): 4005‐ 4013. 10.1128/AAC.02388-13. 24798268 PMC4068594 · DOI
  14. [14]Cao Z, Zhang J, Niu YD, et al. Isolation and characterization of a “phiKMV‐Like” bacteriophage and its therapeutic effect on mink hemorrhagic pneumonia. PLOS One. 2015; 10(1): e0116571 10.1371/journal.pone.0116571. 25615639 PMC4304800 · DOI
  15. [15]Ryan E, Garland MJ, Singh TR, et al. Microneedle‐mediated transdermal bacteriophage delivery. Eur J Pharm Sci. 2012; 47(2): 297‐ 304. 10.1016/j.ejps.2012.06.012. 22750416 PMC3778942 · DOI
  16. [16]Holguín AV, Rangel G, Clavijo V, et al. Phage ΦPan70, a putative temperate phage, controls Pseudomonas aeruginosa in planktonic, biofilm and burn mouse model assays. Viruses. 2015; 7(8): 4602‐ 4623. 10.3390/v7082835. 26274971 PMC4576196 · DOI
  17. [17]Cisek AA, Dąbrowska I, Gregorczyk KP, Wyżewski Z. Phage therapy in bacterial infections treatment: one hundred years after the discovery of bacteriophages. Curr Microbiol. 2017; 74(2): 277‐ 283. 10.1007/s00284-016-1166-x. 27896482 PMC5243869 · DOI
  18. [18]Moelling K, Broecker F, Willy C. A wake‐up call: we need phage therapy now. Viruses. 2018; 10(12): 688 10.3390/v10120688. PMC6316858 30563034 · DOI
  19. [19]El‐Shibiny A, El‐Sahhar S. Bacteriophages: the possible solution to treat infections caused by pathogenic bacteria. Can J Microbiol. 2017; 63(11): 865‐ 879. 10.1139/cjm-2017-0030. 28863269 · DOI
  20. [20]Górski A, Międzybrodzki R, Łobocka M, et al. Phage therapy: what have we learned? Viruses. 2018; 10(6): 288 10.3390/v10060288. PMC6024844 29843391 · DOI
  21. [21]Loc‐Carrillo C, Abedon ST. Pros and cons of phage therapy. Bacteriophage. 2011; 1(2): 111‐ 114. 10.4161/bact.1.2.14590. 22334867 PMC3278648 · DOI
  22. [22]Noble J, Zimmerman A, Fromen CA. Potent immune stimulation from nanoparticle carriers relies on the interplay of adjuvant surface density and adjuvant mass distribution. ACS Biomater Sci Eng. 2017; 3(4): 560‐ 571. 10.1021/acsbiomaterials.6b00756. 33429623 · DOI
  23. [23]Zhang P, Chiu Y‐C, Tostanoski LH, Jewell CM. Polyelectrolyte multilayers assembled entirely from immune signals on gold nanoparticle templates promote antigen‐specific T cell response. ACS Nano. 2015; 9(6): 6465‐ 6477. 10.1021/acsnano.5b02153. 26035231 · DOI
  24. [24]Zhang P, Andorko JI, Jewell CM. Impact of dose, route, and composition on the immunogenicity of immune polyelectrolyte multilayers delivered on gold templates. Biotechnol Bioeng. 2017; 114(2): 423‐ 431. 10.1002/bit.26083. 27567213 PMC6033025 · DOI
  25. [25]Bookstaver ML, Hess KL, Jewell CM. Self‐assembly of immune signals improves codelivery to antigen presenting cells and accelerates signal internalization, processing kinetics, and immune activation. Small. 2018; 14(38): 1802202 10.1002/smll.201802202. PMC6252008 30146797 · DOI
  26. [26]Tsai SJ, Andorko JI, Zeng X, Gammon JM, Jewell CM. Polyplex interaction strength as a driver of potency during cancer immunotherapy. Nano Res. 2018; 11(10): 5642‐ 5656. 10.1007/s12274-018-2181-y. · DOI
  27. [27]Smith GP, Petrenko VA. Phage display. Chem Rev. 1997; 97(2): 391‐ 410. 10.1021/cr960065d 11848876 · DOI
  28. [28]Rohovie MJ, Nagasawa M, Swartz JR. Virus‐like particles: next‐generation nanoparticles for targeted therapeutic delivery. Bioeng Transl Med. 2017; 2(1): 43‐ 57. 10.1002/btm2.10049. 29313023 PMC5689521 · DOI
  29. [29]Nagano K, Tsutsumi Y. Development of novel drug delivery systems using phage display technology for clinical application of protein drugs. Proc Jpn Acad Ser B. 2016; 92(5): 156‐ 166. 10.2183/pjab.92.156. 27169349 PMC4995314 · DOI
  30. [30]Bakhshinejad B, Sadeghizadeh M. Bacteriophages and development of nanomaterials for neural regeneration. Neural Regen Res. 2014; 9(22): 1955‐ 1958. 10.4103/1673-5374.145371. 25598776 PMC4283276 · DOI
  31. [31]Sorokulova I, Olsen E, Vodyanoy V. Bacteriophage biosensors for antibiotic‐resistant bacteria. Expert Rev Med Devices. 2014; 11(2): 175‐ 186. 10.1586/17434440.2014.882767. 24506300 · DOI
  32. [32]Schmelcher M, Loessner MJ. Application of bacteriophages for detection of foodborne pathogens. Bacteriophage. 2014; 4(2): e28137 10.4161/bact.28137. 24533229 PMC3919822 · DOI
  33. [33]Li S, Li Y, Chen H, et al. Direct detection of Salmonella typhimurium on fresh produce using phage‐based magnetoelastic biosensors. Biosens Bioelectron. 2010; 26(4): 1313‐ 1319. 10.1016/j.bios.2010.07.029. 20688505 · DOI
  34. [34]Straus SK, Scott WRP, Symmons MF, Marvin DA. On the structures of filamentous bacteriophage Ff (fd, f1, M13). Eur Biophys J. 2008; 37(4): 521‐ 527. 10.1007/s00249-007-0222-7. 17943277 · DOI
  35. [35]Prisco A, De Berardinis P. Filamentous bacteriophage Fd as an antigen delivery system in vaccination. Int J Mol Sci. 2012; 13(4): 5179‐ 5194. 10.3390/ijms13045179. 22606037 PMC3344273 · DOI
  36. [36]Nicastro J, Sheldon K, Slavcev RA. Bacteriophage lambda display systems: developments and applications. Appl Microbiol Biotechnol. 2014; 98(7): 2853‐ 2866. 10.1007/s00253-014-5521-1. 24442507 · DOI
  37. [37]Qin L, Fokine A, O'Donnell E, Rao VB, Rossmann MG. Structure of the small outer capsid protein, Soc: a clamp for stabilizing capsids of T4‐like phages. J Mol Biol. 2010; 395(4): 728‐ 741. 10.1016/j.jmb.2009.10.007. 19835886 PMC2813359 · DOI
  38. [38]Fokine A, Islam MZ, Zhang Z, Bowman VD, Rao VB, Rossmann MG. Structure of the three N‐terminal immunoglobulin domains of the highly immunogenic outer capsid protein from a T4‐like bacteriophage. J Virol. 2011; 85(16): 8141‐ 8148. 10.1128/JVI.00847-11. 21632759 PMC3147960 · DOI
  39. [39]Guo F, Liu Z, Fang P‐A, et al. Capsid expansion mechanism of bacteriophage T7 revealed by multistate atomic models derived from cryo‐EM reconstructions. Proc Natl Acad Sci USA. 2014; 111(43): E4606‐ E4614. 10.1073/pnas.1407020111. 25313071 PMC4217468 · DOI
  40. [40]Hess KL, Oh E, Tostanoski LH, et al. Engineering immunological tolerance using quantum dots to tune the density of self‐antigen display. Adv Funct Mater. 2017; 27(22): 1700290 10.1002/adfm.201700290. 29503604 PMC5828250 · DOI
  41. [41]Hernando‐Pérez M, Lambert S, Nakatani‐Webster E, Catalano CE, de Pablo PJ. Cementing proteins provide extra mechanical stabilization to viral cages. Nat Commun. 2014; 5: 4520 10.1038/ncomms5520. 25072871 · DOI
  42. [42]González‐Cano P, Gamage LNA, Marciniuk K, et al. Lambda display phage as a mucosal vaccine delivery vehicle for peptide antigens. Vaccine. 2017; 35(52): 7256‐ 7263. 10.1016/j.vaccine.2017.11.010. 29153779 · DOI
  43. [43]Bookstaver ML, Tsai SJ, Bromberg JS, Jewell CM. Improving vaccine and immunotherapy design using biomaterials. Trends Immunol. 2018; 39(2): 135‐ 150. 10.1016/j.it.2017.10.002. 29249461 PMC5914493 · DOI
  44. [44]Fu Y, Li J. A novel delivery platform based on bacteriophage MS2 virus‐like particles. Virus Res. 2016; 211: 9‐ 16. 10.1016/j.virusres.2015.08.022. 26415756 PMC7114531 · DOI
  45. [45]Cui Z, Gorzelnik KV, Chang J‐Y, et al. Structures of Qβ virions, virus‐like particles, and the Qβ–MurA complex reveal internal coat proteins and the mechanism of host lysis. Proc Natl Acad Sci USA. 2017; 114(44): 11697‐ 11702. 10.1073/pnas.1707102114. 29078304 PMC5676892 · DOI
  46. [46]Reed CA, Langlais C, Wang I‐N, Young R. A2 expression and assembly regulates lysis in Qβ infections. Microbiology. 2013; 159(3): 507‐ 514. 10.1099/mic.0.064790-0. 23329676 PMC3709820 · DOI
  47. [47]Rumnieks J, Tars K. Crystal structure of the read‐through domain from bacteriophage Qβ A1 protein. Protein Sci. 2011; 20(10): 1707‐ 1712. 10.1002/pro.704. 21805520 PMC3218364 · DOI
  48. [48]Roush SW, Murphy TV, Group and the V‐PDTW. Historical comparisons of morbidity and mortality for vaccine‐preventable diseases in the United States. JAMA. 2007; 298(18): 2155‐ 2163. 10.1001/jama.298.18.2155. 18000199 · DOI
  49. [49]Steinhagen F, Kinjo T, Bode C, Klinman DM. TLR‐based immune adjuvants. Vaccine. 2011; 29(17): 3341‐ 3355. 10.1016/j.vaccine.2010.08.002. 20713100 PMC3000864 · DOI
  50. [50]Aghebati‐Maleki L, Bakhshinejad B, Baradaran B, et al. Phage display as a promising approach for vaccine development. J Biomed Sci. 2016; 23(1): 66 10.1186/s12929-016-0285-9. 27680328 PMC5041315 · DOI
  51. [51]Gao J, Wang Y, Liu Z, Wang Z. Phage display and its application in vaccine design. Ann Microbiol. 2010; 60(1): 13‐ 19. 10.1007/s13213-009-0014-7. · DOI
  52. [52]Kaur T, Nafissi N, Wasfi O, Sheldon K, Wettig S, Slavcev R. Immunocompatibility of bacteriophages as nanomedicines. J Nanotechnol. 2012; 2012: 1‐ 13. 10.1155/2012/247427. · DOI
  53. [53]Xu H, Bao X, Lu Y, et al. Immunogenicity of T7 bacteriophage nanoparticles displaying G‐H loop of foot‐and‐mouth disease virus (FMDV). Vet Microbiol. 2017; 205: 46‐ 52. 10.1016/j.vetmic.2017.04.023. 28622860 · DOI
  54. [54]Bahadir AO, Balcioglu BK, Uzyol KS, et al. Phage displayed HBV core antigen with immunogenic activity. Appl Biochem Biotechnol. 2011; 165(7): 1437‐ 1447. 10.1007/s12010-011-9365-1. 21915589 · DOI
  55. [55]Gao J, Liu Z, Huang M, Li X, Wang Z. T7 phage displaying latent membrane protein 1 of Epstein‐Barr virus elicits humoral and cellular immune responses in rats. Acta Virol. 2011; 55(2): 117‐ 121. 10.4149/av_2011_02_117. 21692559 · DOI
  56. [56]Deng L, Roose K, Job ER, et al. Oral delivery of Escherichia coli persistently infected with M2e‐displaying bacteriophages partially protects against influenza A virus. J Control Release. 2017; 264: 55‐ 65. 10.1016/j.jconrel.2017.08.020. 28842314 · DOI
  57. [57]Gong Z, Karlsson AJ. Translocation of cell‐penetrating peptides into Candida fungal pathogens. Protein Sci. 2017; 26(9): 1714‐ 1725. 10.1002/pro.3203. 28556271 PMC5563134 · DOI
  58. [58]Kim S‐H, Jang Y‐S. The development of mucosal vaccines for both mucosal and systemic immune induction and the roles played by adjuvants. Clin Exp Vaccine Res. 2017; 6(1): 15‐ 21. 10.7774/cevr.2017.6.1.15. 28168169 PMC5292352 · DOI
  59. [59]Jung C, Hugot J‐P, Barreau F. Peyer's Patches: the immune sensors of the intestine. Int J Inflam. 2010; 2010: 1‐ 12. 10.4061/2010/823710. PMC3004000 21188221 · DOI
  60. [60]Huai Y, Dong S, Zhu Y, et al. Genetically engineered virus nanofibers as an efficient vaccine for preventing fungal infection. Adv Healthc Mater. 2016; 5(7): 786‐ 794. 10.1002/adhm.201500930. 26890982 PMC4828319 · DOI
  61. [61]Ikonomova SP, Moghaddam‐Taaheri P, Jabra‐Rizk MA, Wang Y, Karlsson AJ. Engineering improved variants of the antifungal peptide histatin 5 with reduced susceptibility to Candida albicans secreted aspartic proteases and enhanced antimicrobial potency. FEBS J. 2018; 285(1): 146‐ 159. 10.1111/febs.14327. 29143452 PMC7106779 · DOI
  62. [62]Buckley P, Rivers B, Katoski S, et al. Genetic barcodes for improved environmental tracking of an anthrax simulant. Appl Environ Microbiol. 2012; 78(23): 8272‐ 8280. 10.1128/AEM.01827-12. 23001658 PMC3497392 · DOI
  63. [63]Edmonds J, Lindquist HDA, Sabol J, et al. Multigeneration cross‐contamination of mail with Bacillus anthracis spores. PLOS One. 2016; 11(4): e0152225 10.1371/journal.pone.0152225. 27123934 PMC4849716 · DOI
  64. [64]Cote CK, Buhr T, Bernhards CB, et al. A standard method to inactivate Bacillus anthracis spores to sterility via gamma irradiation. Appl Environ Microbiol. 2018; 84(12): e00106‐ e00118. 10.1128/AEM.00106-18. 29654186 PMC5981071 · DOI
  65. [65]Peachman KK, Li Q, Matyas GR, et al. Anthrax vaccine antigen‐adjuvant formulations completely protect New Zealand white rabbits against challenge with Bacillus anthracis Ames strain spores. Clin Vaccine Immunol. 2012; 19(1): 11‐ 16. 10.1128/CVI.05376-11. 22089245 PMC3255956 · DOI
  66. [66]Rao M, Peachman KK, Li Q, et al. Highly effective generic adjuvant systems for orphan or poverty‐related vaccines. Vaccine. 2011; 29(5): 873‐ 877. 10.1016/j.vaccine.2010.11.049. 21115053 PMC4190060 · DOI
  67. [67]Tao P, Mahalingam M, Zhu J, et al. A bacteriophage T4 nanoparticle‐based dual vaccine against anthrax and plague. mBio. 2018; 9(5): e01926‐ e01918. 10.1128/mBio.01926-18. 30327445 PMC6191538 · DOI
  68. [68]Gibbons HS, Krepps MD, Ouellette G, et al. Comparative genomics of 2009 seasonal plague (Yersinia pestis) in New Mexico. PLOS One. 2012; 7(2): e31604 10.1371/journal.pone.0031604. 22359605 PMC3281092 · DOI
  69. [69]Powell BS, Andrews GP, Enama JT, et al. Design and testing for a nontagged F1‐V fusion protein as vaccine antigen against bubonic and pneumonic plague. Biotechnol Prog. 2005; 21(5): 1490‐ 1510. 10.1021/bp050098r. 16209555 · DOI
  70. [70]Hashemi H, Pouyanfard S, Bandehpour M, et al. Immunization with M2e‐displaying T7 bacteriophage nanoparticles protects against influenza A virus challenge. PLOS One. 2012; 7(9): e45765 10.1371/journal.pone.0045765. 23029232 PMC3454340 · DOI
  71. [71]Putri WCWS, Muscatello DJ, Stockwell MS, Newall AT. Economic burden of seasonal influenza in the United States. Vaccine. 2018; 36(27): 3960‐ 3966. 10.1016/j.vaccine.2018.05.057. 29801998 · DOI
  72. [73]Schotsaert M, Filette MD, Fiers W, Saelens X. Universal M2 ectodomain‐based influenza A vaccines: preclinical and clinical developments. Expert Rev Vaccines. 2009; 8(4): 499‐ 508. 10.1586/erv.09.6. 19348565 PMC2706389 · DOI
  73. [74]Turley CB, Rupp RE, Johnson C, et al. Safety and immunogenicity of a recombinant M2e–flagellin influenza vaccine (STF2.4xM2e) in healthy adults. Vaccine. 2011; 29(32): 5145‐ 5152. 10.1016/j.vaccine.2011.05.041. 21624416 · DOI
  74. [76]Cuevas MBP, Kodani M, Choi Y, et al. Hepatitis B vaccination using a dissolvable microneedle patch is immunogenic in mice and rhesus macaques. Bioeng Transl Med. 2018; 3(3): 186‐ 196. 10.1002/btm2.10098. 30377659 PMC6195907 · DOI
  75. [77]Clark JR, Bartley K, Jepson CD, Craik V, March JB. Comparison of a bacteriophage‐delivered DNA vaccine and a commercially available recombinant protein vaccine against hepatitis B. FEMS Immunol Med Microbiol. 2011; 61(2): 197‐ 204. 10.1111/j.1574-695X.2010.00763.x. 21204995 · DOI
  76. [78]Zhai L, Peabody J, Pang Y‐YS, Schiller J, Chackerian B, Tumban E. A novel candidate HPV vaccine: MS2 phage VLP displaying a tandem HPV L2 peptide offers similar protection in mice to Gardasil‐9. Antiviral Res. 2017; 147: 116‐ 123. 10.1016/j.antiviral.2017.09.012. 28939477 PMC5675787 · DOI
  77. [79]Gammon JM, Dold NM, Jewell CM. Improving the clinical impact of biomaterials in cancer immunotherapy. Oncotarget. 2016; 7(13): 15421‐ 15443. 10.18632/oncotarget.7304. 26871948 PMC4941251 · DOI
  78. [80]Toy R, Roy K. Engineering nanoparticles to overcome barriers to immunotherapy. Bioeng Transl Med. 2016; 1(1): 47‐ 62. 10.1002/btm2.10005. 29313006 PMC5689503 · DOI
  79. [81]Huijbers EJM, Griffioen AW. The revival of cancer vaccines — the eminent need to activate humoral immunity. Hum Vaccin Immunother. 2017; 13(5): 1112‐ 1114. 10.1080/21645515.2016.1276140. 28118089 PMC5443398 · DOI
  80. [82]Lieser RM, Chen W, Sullivan MO. Controlled epidermal growth factor receptor ligand display on cancer suicide enzymes via unnatural amino acid engineering for enhanced intracellular delivery in breast cancer cells. Bioconjug Chem. 2019; 30(2): 432‐ 442. 10.1021/acs.bioconjchem.8b00783. 30615416 · DOI
  81. [83]Arab A, Nicastro J, Slavcev R, et al. Lambda phage nanoparticles displaying HER2‐derived E75 peptide induce effective E75‐CD8+ T response. Immunol Res. 2018; 66(1): 200‐ 206. 10.1007/s12026-017-8969-0. 29143917 · DOI
  82. [84]Barati N, Razazan A, Nicastro J, et al. Immunogenicity and antitumor activity of the superlytic λF7 phage nanoparticles displaying a HER2/neu‐derived peptide AE37 in a tumor model of BALB/c mice. Cancer Lett. 2018; 424: 109‐ 116. 10.1016/j.canlet.2018.03.030. 29580807 · DOI
  83. [85]Iwagami Y, Casulli S, Nagaoka K, et al. Lambda phage‐based vaccine induces antitumor immunity in hepatocellular carcinoma. Heliyon. 2017; 3(9): e00407 10.1016/j.heliyon.2017.e00407. 28971150 PMC5619992 · DOI
  84. [86]Ren S, Feng Y, Zuo S, et al. Inhibition of tumor angiogenesis in lung cancer by T4 phage surface displaying mVEGFR2 vaccine. Vaccine. 2011; 29(34): 5802‐ 5811. 10.1016/j.vaccine.2011.03.051. 21482223 · DOI
  85. [87]Sartorius R, D'Apice L, Barba P, et al. Vectorized delivery of alpha‐GalactosylCeramide and tumor antigen on filamentous bacteriophage fd induces protective immunity by enhancing tumor‐specific T cell response. Front Immunol. 2018; 9: 1496 10.3389/fimmu.2018.01496. 30002659 PMC6031736 · DOI
  86. [88]Sullivan BA, Kronenberg M. Activation or anergy: NKT cells are stunned by α‐galactosylceramide. J Clin Invest. 2005; 115(9): 2328‐ 2329. 10.1172/JCI26297. 16138189 PMC1193891 · DOI
  87. [89]Lynn GM, Laga R, Jewell CM. Induction of anti‐cancer T cell immunity by in situ vaccination using systemically administered nanomedicines. Cancer Lett. 2019; 459: 192‐ 203. 10.1016/j.canlet.2019.114427. 31185250 PMC6629511 · DOI
  88. [90]Arab A, Behravan N, Razazn A, et al. The viral approach to breast cancer immunotherapy. J Cell Physiol. 2019; 234(2): 1257‐ 1267. 10.1002/jcp.27150. 30146692 · DOI
  89. [92]Petrelli F, Tomasello G, Barni S, Lonati V, Passalacqua R, Ghidini M. Clinical and pathological characterization of HER2 mutations in human breast cancer: a systematic review of the literature. Breast Cancer Res Treat. 2017; 166(2): 339‐ 349. 10.1007/s10549-017-4419-x. 28762010 · DOI
  90. [93]Ahmed S, Sami A, Xiang J. HER2‐directed therapy: current treatment options for HER2‐positive breast cancer. Breast Cancer. 2015; 22(2): 101‐ 116. 10.1007/s12282-015-0587-x. 25634227 · DOI
  91. [94]Alajati A, Sausgruber N, Aceto N, et al. Mammary tumor formation and metastasis evoked by a HER2 splice variant. Cancer Res. 2013; 73(17): 5320‐ 5327. 10.1158/0008-5472.CAN-12-3186. 23867476 · DOI
  92. [95]Castagnoli L, Ghedini GC, Koschorke A, et al. Pathobiological implications of the d16HER2 splice variant for stemness and aggressiveness of HER2‐positive breast cancer. Oncogene. 2017; 36(12): 1721‐ 1732. 10.1038/onc.2016.338. 27641338 PMC5447867 · DOI
  93. [96]Tilio M, Gambini V, Wang J, et al. Irreversible inhibition of Δ16HER2 is necessary to suppress Δ16HER2‐positive breast carcinomas resistant to Lapatinib. Cancer Lett. 2016; 381(1): 76‐ 84. 10.1016/j.canlet.2016.07.028. 27475932 · DOI
  94. [97]Bartolacci C, Andreani C, Curcio C, et al. Phage‐based anti‐HER2 vaccination can circumvent immune tolerance against breast cancer. Cancer Immunol Res. 2018; 6(12): 1486‐ 1498. 10.1158/2326-6066.CIR-18-0179. 30327365 · DOI · Paper page
  95. [98]Marchini C, Gabrielli F, Iezzi M, et al. The human splice variant Δ16HER2 induces rapid tumor onset in a reporter transgenic mouse. PLOS One. 2011; 6(4): e18727 10.1371/journal.pone.0018727. 21559085 PMC3084693 · DOI
  96. [99]Pouyanfard S, Bamdad T, Hashemi H, Bandehpour M, Kazemi B. Induction of protective anti‐CTL epitope responses against HER‐2‐positive breast cancer based on multivalent T7 phage nanoparticles. PLOS One. 2012; 7(11): e49539 10.1371/journal.pone.0049539. 23166703 PMC3499470 · DOI
  97. [100]Wu X, Yin Z, McKay C, et al. Protective epitope discovery and design of MUC1‐based vaccine for effective tumor protections in immunotolerant mice. J Am Chem Soc. 2018; 140(48): 16596‐ 16609. 10.1021/jacs.8b08473. 30398345 PMC6470043 · DOI
  98. [101]Hossain MK, Wall KA. Immunological evaluation of recent MUC1 glycopeptide cancer vaccines. Vaccine. 2016; 4(3): 25 10.3390/vaccines4030025. PMC5041019 27472370 · DOI · Paper page
  99. [102]Gaidzik N, Westerlind U, Kunz H. The development of synthetic antitumour vaccines from mucin glycopeptide antigens. Chem Soc Rev. 2013; 42(10): 4421‐ 4442. 10.1039/C3CS35470A. 23440054 · DOI
  100. [103]Górski A, Międzybrodzki R, Weber‐Dąbrowska B, et al. Phage therapy: combating infections with potential for evolving from merely a treatment for complications to targeting diseases. Front Microbiol. 2016; 7: 1515 10.3389/fmicb.2016.01515. 27725811 PMC5035766 · DOI
  101. [104]Miernikiewicz P, Kłopot A, Soluch R, et al. T4 phage tail adhesin Gp12 counteracts LPS‐induced inflammation in vivo. Front Microbiol. 2016; 7: 1112 10.3389/fmicb.2016.01112. 27471503 PMC4943950 · DOI
  102. [105]Park K, Cha KE, Myung H. Observation of inflammatory responses in mice orally fed with bacteriophage T7. J Appl Microbiol. 2014; 117(3): 627‐ 633. 10.1111/jam.12565. 24916438 · DOI
  103. [106]Hess KL, Medintz IL, Jewell CM. Designing inorganic nanomaterials for vaccines and immunotherapies. Nano Today. 2019; 27: 73‐ 98. 10.1016/j.nantod.2019.04.005. PMC7156029 32292488 · DOI
  104. [107]Andorko JI, Jewell CM. Designing biomaterials with immunomodulatory properties for tissue engineering and regenerative medicine. Bioeng Transl Med. 2017; 2(2): 139‐ 155. 10.1002/btm2.10063. 28932817 PMC5579731 · DOI

Cited by

Sorted by citations

Authors
Hess, K. L., & Jewell, C. M.
Affiliations
  • U.S. Army Combat Capabilities Development Command Chemical Biological Center (US)
  • University of Maryland, Baltimore (US)
Corresponding author
Hess, Krystina L.
Venue
Bioengineering & Translational Medicine
Publisher
Wiley
Published
2019-09-18
Volume
5
Issue
1
Pages
e10142-e10142
ISSN
2380-6761 (ISSN-L)
OpenAlex
W2970959293
Cited by
134
References
0
Citations by year
2026: 18 · 2025: 18 · 2024: 21 · 2023: 31 · 2022: 18 · 2021: 17 · 2020: 10 · 2019: 1
FWCI
0.82
Type
journal article
Language
en
Open access
Locations
  • Bioengineering & Translational Medicine (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
National Institute of Biomedical Imaging and Bioengineering (R01EB026896, R01EB027143)
Topics
  • Physical Sciences › Environmental Science › Ecology › Bacteriophages and microbial interactions
  • Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › vaccines and immunoinformatics approaches
Keywords
phage display, bacteriophages, vaccine development, cancer immunotherapy, antigen display, DNA vaccine, adjuvants, antigen delivery, infectious disease vaccines

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review