1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Phage and Yeast Display

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • HTML
    140.08 Kb
  • PDF
    416.96 Kb
  • XML
    153.03 Kb
  • Authors: Jared Sheehan1, Wayne A. Marasco2
  • Editors: James E. Crowe Jr.3, Diana Boraschi4, Rino Rappuoli5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Cancer Immunology and AIDS, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215; 2: Department of Cancer Immunology and AIDS, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215; 3: Vanderbilt University School of Medicine, Nashville, TN; 4: National Research Council, Pisa, Italy; 5: Novartis Vaccines, Siena, Italy
    • Source: microbiolspec February 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.AID-0028-2014
  • Received 05 December 2014 Accepted 06 December 2014 Published 06 February 2015
  • Wayne A. Marasco, [email protected]
image of Phage and Yeast Display
    Preview this microbiology spectrum article:
    Preview Magnify
    Zoom in
    Zoomout

    Phage and Yeast Display, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/3/1/AID-0028-2014-1.gif /docserver/preview/fulltext/microbiolspec/3/1/AID-0028-2014-2.gif

  • Abstract:

    Despite the availability of antimicrobial drugs, the continued development of microbial resistance—established through escape mutations and the emergence of resistant strains—limits their clinical utility. The discovery of novel, therapeutic, monoclonal antibodies (mAbs) offers viable clinical alternatives in the treatment and prophylaxis of infectious diseases. Human mAb-based therapies are typically nontoxic in patients and demonstrate high specificity for the intended microbial target. This specificity prevents negative impacts on the patient microbiome and avoids driving the resistance of nontarget species. The selection of human antibody fragment libraries displayed on phage or yeast surfaces represents a group of well-established technologies capable of generating human mAbs. The advantage of these forms of microbial display is the large repertoire of human antibody fragments present during a single selection campaign. Furthermore, the selection environments of microbial surface display allow for the rapid isolation of antibodies—and their encoding genes—against infectious pathogens and their toxins that are impractical within systems, such as murine hybridomas. This article focuses on the technologies of phage display and yeast display, as these strategies relate to the discovery of human mAbs for the treatment and vaccine development of infectious diseases.

  • Citation: Sheehan J, Marasco W. 2015. Phage and Yeast Display. Microbiol Spectrum 3(1):AID-0028-2014. doi:10.1128/microbiolspec.AID-0028-2014.

References

1. Rakonjac J, Bennett NJ, Spagnuolo J, Gagic D, Russel M. 2011. Filamentous bacteriophage: biology, phage display and nanotechnology applications. Curr Issues Mol Biol 13:51–76. [PubMed]
2. Boeke JD, Model P. 1982. A prokaryotic membrane anchor sequence: carboxyl terminus of bacteriophage f1 gene III protein retains it in the membrane. Proc Natl Acad Sci USA 79:5200–5204. [PubMed][CrossRef]
3. Rakonjac J, Feng J, Model P. 1999. Filamentous phage are released from the bacterial membrane by a two-step mechanism involving a short C-terminal fragment of pIII. J Mol Biol 289:1253–1265. [PubMed][CrossRef]
4. Loeb T. 1960. Isolation of a bacteriophage for the F plus and Hfr mating types of Escherichia coli K-12. Science 131:932–933. [PubMed][CrossRef]
5. Barbas CF III, Kang AS, Lerner RA, Benkovic SJ. 1991. Assembly of combinatorial antibody libraries on phage surfaces: the gene III site. Proc Natl Acad Sci USA 88:7978–7982. [PubMed][CrossRef]
6. Clackson T, Hoogenboom HR, Griffiths AD, Winter G. 1991. Making antibody fragments using phage display libraries. Nature 352:624–628. [PubMed][CrossRef]
7. Marks JD, Hoogenboom HR, Bonnert TP, McCafferty J, Griffiths AD, Winter G. 1991. By-passing immunization. Human antibodies from V-gene libraries displayed on phage. J Mol Biol 222:581–597. [PubMed][CrossRef]
8. Marks JD, Tristem M, Karpas A, Winter G. 1991. Oligonucleotide primer for polymerase chain reaction amplification of human immunoglobulin variable genes and design of family-specific oligonucleotide probes. Eur J Immunol 21:985–991. [PubMed][CrossRef]
9. de Haard HJ, van Neer N, Reurs A, Hufton SE, Roovers RC, Henderikx P, de Bruïne AP, Arends JW, Hoogenboom HR. 1999. A large non-immunized human Fab phage library that permits rapid isolation and kinetic analysis of high affinity antibodies. J Biol Chem 274:18218–18230. [PubMed]
10. Vaughan TJ, Williams AJ, Pritchard K, Osbourn JK, Pope AR, Earnshaw JC, McCafferty J, Hodits RA, Wilton J, Johnson KS. 1996. Human antibodies with sub-nanomolar affinities isolated from a large non-immunized phage display library. Nat Biotechnol 14:309–314. [PubMed][CrossRef]
11. Gram H, Marconi LA, Barbas CF, 3rd, Collet TA, Lerner RA, Kang AS. 1992. In vitro selection and affinity maturation of antibodies from a naïve combinatorial immunoglobulin library. Proc Natl Acad Sci USA 89:3576–3580. [PubMed][CrossRef]
12. Hoogenboom HR. 2002. Overview of antibody phage-display technology and its applications, p 1–38. In O'Brien PM, Aitken R (ed), Antibody Phage Display, Methods and Protocols. Methods in Molecular Biology, Vol. 178. Humana Press, Totowa, NJ. [PubMed][CrossRef]
13. Griffiths AD, Malmqvist M, Marks JD, Bye JM, Embleton MJ, McCafferty J, Baier M, Holliger KP, Gorick BD, Hughes-Jones NC. 1993. Human anti-self antibodies with high specificity from phage display libraries. EMBO J 12:725–734. [PubMed]
14. Burton DR, Barbas CF, 3rd, Persson MA, Koenig S, Chanock RM, Lerner RA. 1991. A large array of human monoclonal antibodies to type 1 human immunodeficiency virus from combinatorial libraries of asymptomatic seropositive individuals. Proc Natl Acad Sci USA 88:10134–10137. [PubMed][CrossRef]
15. de Wildt RM, Finnern R, Ouwehand WH, Griffiths AD, van Venrooij WJ, Hoet RM. 1996. Characterization of human variable domain antibody fragments against the U1 RNA-associated A protein, selected from a synthetic and a patient-derived combinatorial V gene library. Eur J Immunol 26:629–639. [PubMed][CrossRef]
16. Barbas CF, 3rd, Burton DR. 1996. Selection and evolution of high-affinity human anti-viral antibodies. Trends Biotechnol 14:230–234. [PubMed][CrossRef]
17. Hoogenboom HR, Winter G. 1992. By-passing immunization. Human antibodies from synthetic repertoires of germline VH segments rearranged in vitro. J Mol Biol 227:381–388. [PubMed][CrossRef]
18. Zhu K, Day T. 2013. Ab initio structure prediction of the antibody hypervariable H3 loop. Proteins 81:1081–1089. [PubMed][CrossRef]
19. Hoet RM, Cohen EH, Kent RB, Rookey K, Schoonbroodt S, Hogan S, Rem L, Frans N, Daukandt M, Pieters H, van Hegelsom R, Neer NC, Nastri HG, Rondon IJ, Leeds JA, Hufton SE, Huang L, Kashin I, Devlin M, Kuang G, Steukers M, Viswanathan M, Nixon AE, Sexton DJ, Hoogenboom HR, Ladner RC. 2005. Generation of high-affinity human antibodies by combining donor-derived and synthetic complementarity-determining-region diversity. Nat Biotechnol 23:344–348. [PubMed][CrossRef]
20. Rothe C, Urlinger S, Löhning C, Prassler J, Stark Y, Jäger U, Hubner B, Bardroff M, Pradel I, Boss M, Bittlingmaier R, Bataa T, Frisch C, Brocks B, Honegger A, Urban M. 2008. The human combinatorial antibody library HuCAL GOLD combines diversification of all six CDRs according to the natural immune system with a novel display method for efficient selection of high-affinity antibodies. J Mol Biol 376:1182–1200. [PubMed][CrossRef]
21. Knappik A, Ge L, Honegger A, Pack P, Fischer M, Wellnhofer G, Hoess A, Wölle J, Plückthun A, Virnekäs B. 2000. Fully synthetic human combinatorial antibody libraries (HuCAL) based on modular consensus frameworks and CDRs randomized with trinucleotides. J Mol Biol 11:57–86. [PubMed][CrossRef]
22. Tiller T, Schuster I, Deppe D, Siegers K, Strohner R, Herrmann T, Berenguer M, Poujol D, Stehle J, Stark Y, Heßling M, Daubert D, Felderer K, Kaden S, Kölln J, Enzelberger M, Urlinger S. 2013. A fully synthetic human Fab antibody library fixed on VH/VL framework pairings with favorable biophysical properties. MAbs 5:445–470. [PubMed][CrossRef]
23. Gao C, Mao S, Lo CH, Wirsching P, Lerner RA, Janda KD. 1999. Making artificial antibodies: a format for phage display of combinatorial heterodimeric arrays. Proc Natl Acad Sci USA 96:6025–6030. [PubMed][CrossRef]
24. Jespers LS, De Keyser A, Stanssens PE. 1996. LambdaZLG6: a phage lambda vector for high-efficiency cloning and surface expression of cDNA libraries on filamentous phage. Gene 173:179–181. [PubMed][CrossRef]
25. Iannolo G, Minenkova O, Petruzzelli R, Cesareni G. 1995. Modifying filamentous phage capsid: limits in the size of the major capsid protein. J Mol Biol 248:835–844. [PubMed][CrossRef]
26. Zwick MB, Shen J, Scott JK. 2000. Homodimeric peptides displayed by the major coat protein of filamentous phage. J Mol Biol 300:307–320. [PubMed][CrossRef]
27. O'Connell D, Becerril B, Roy-Burman A, Daws M, Marks JD. 2002. Phage versus phagemid libraries for generation of human monoclonal antibodies. J Mol Biol 312:49–56. [PubMed][CrossRef]
28. Marks JD, Hoogenboom HR, Griffiths AD, Winter G. 1992. Molecular evolution of proteins on filamentous phage. Mimicking the strategy of the immune system. J Biol Chem 267:16007–16010. [PubMed]
29. de Wildt RM, Tomlinson IM, Ong JL, Holliger P. 2002. Isolation of receptor-ligand pairs by capture of long-lived multivalent interaction complexes. Proc Natl Acad Sci USA 99:8530–8535. [PubMed][CrossRef]
30. Rakonjac J, Jovanovic G, Model P. 1997. Filamentous phage infection-mediated gene expression: construction and propagation of the gIII deletion mutant helper phage R408d3. Gene 198:99–103. [PubMed][CrossRef]
31. Chasteen L, Ayriss J, Pavlik P, Bradbury AR. 2006. Eliminating helper phage from phage display. Nucleic Acid Res 34:e145. [PubMed][CrossRef]
32. Hoogenboom HR, Griffiths AD, Johnson KS, Chiswell DJ, Hudson P, Winter G. 1991. Multi-subunit proteins on the surface of filamentous phage: methodologies for displaying antibody (Fab) heavy and light chains. Nucleic Acids Res 19:4133–4137. [PubMed][CrossRef]
33. Garrard LJ, Yang M, O'Connell MP, Kelley RF, Henner DJ. 1991. Fab assembly and enrichment in a monovalent phage system. Biotechnology 9:1373–1377. [PubMed][CrossRef]
34. Chan CE, Chan AH, Lim AP, Hanson BJ. 2011. Comparison of the efficiency of antibody selection from semi-synthetic scFv and non-immune Fab phage display libraries against protein targets for rapid development of diagnostic immunoassays. J Immunol Methods 373:79–88. [PubMed][CrossRef]
35. Qi J, Ye X, Ren G, Kan F, Zhang Y, Guo M, Zhang Z, Li D. 2014. Pharmacological efficacy of anti-IL-1β scFv, Fab, and full-length antibodies in treatment of rheumatoid arthritis. Mol Immunol 57:59–65. [PubMed][CrossRef]
36. Steinwand M, Droste P, Frenzel A, Hust M, Dübel S, Schirrmann T. 2014. The influence of antibody fragment format on phage display based affinity maturation of IgG. MAbs 6:204–218. [PubMed][CrossRef]
37. Lauring AS, Frydman J, Andino R. 2013. The role of mutational robustness in RNA virus evolution. Nat Rev Microbiol 11:327–336. [PubMed][CrossRef]
38. Balmer O, Tanner M. 2011. Prevalence and implications of multiple-strain infections. Lancet Infect Dis 11:868–878. [PubMed][CrossRef]
39. Leye N, Vidal N, Ndiaye O, Diop-Ndiaye H, Wade AS, Mboup S, Delaporte E, Toure-Kane C, Peeters M. 2013. High frequency of HIV-1 infections with multiple HIV-1 strains in men having sex with men (MSM) in Senegal. Infect Genet Evol 20:206–214. [PubMed][CrossRef]
40. Yewdell JW, Spiro DJ, Golding H, Quill H, Mittelman A, Nabel GJ. 2013. Getting to the heart of influenza. Sci Transl Med 5:e191ed8. [PubMed]
41. Corti D, Lanzavecchia A. 2013. Broadly neutralizing antiviral antibodies. Annu Rev Immunol 31:705–742. [PubMed][CrossRef]
42. Marasco WA, Sui J. 2007. The growth and potential of human antiviral monoclonal antibody therapeutics. Nat Biotechnol 25:1421–1434. [PubMed][CrossRef]
43. Thie H, Meyer T, Schirrmann T, Hust M, Dübel S. 2008. Phage display derived therapeutic antibodies. Curr Pharm Biotechnol 9:439–446. [PubMed][CrossRef]
44. Jegaskanda S, Job ER, Kramski M, Laurie K, Isitman G, de Rose R, Winnall WR, Stratov I, Brooks AG, Reading PC, Kent SJ. 2013. Cross-reactive influenza-specific antibody-dependent cellular cytotoxicity antibodies in the absence of neutralizing antibodies. J Immunol 190:1837–1848. [PubMed][CrossRef]
45. Gamblin SJ, Skehel JJ. 2010. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J Biol Chem 285:38403–38409. [PubMed][CrossRef]
46. Skehal JJ, Wiley DC. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69:531–569. [PubMed][CrossRef]
47. Wiley DC, Wilson IA, Skehel JJ. 1981. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289:373–378. [PubMed][CrossRef]
48. Both GW, Sleigh MJ, Cox NJ, Kendal AP. 1983. Antigenic drift in influenza virus H3 hemagglutinin from 1968 to 1980: multiple evolutionary pathways and sequential amino acid changes at key antigenic sites. J Virol 48:52–60. [PubMed]
49. Sui J, Hwang WC, Perez S, Wei G, Aird D, Chen LM, Santelli E, Stec B, Cadwell G, Ali M, Wan H, Murakami A, Yammanuru A, Han T, Cox NJ, Bankston LA, Donis RO, Liddington RC, Marasco WA. 2009. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 16:265–273. [PubMed][CrossRef]
50. Throsby M, van den Brink E, Jongeneelen M, Poon LL, Alard P, Cornelissen L, Bakker A, Cox F, van Deventer E, Guan Y, Cinatl J, ter Meulen J, Lasters I, Carsetti R, Peiris M, de Kruif J, Goudsmit J. 2008. Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS One 3:e3942. doi:10.1371/journal.pone.0003942. [CrossRef]
51. Dreyfus C, Laursen NS, Kwaks T, Zuijdgeest D, Khayat R, Ekiert DC, Lee JH, Metlagel Z, Bujny MV, Jongeneelen M, van der Vlugt R, Lamrani M, Korse HJ, Geelen E, Sahin Ö, Sieuwerts M, Brakenhoff JP, Vogels R, Li OT, Poon LL, Peiris M, Koudstaal W, Ward AB, Wilson IA, Goudsmit J, Friesen RH. 2012. Highly conserved protective epitopes on influenza B viruses. Science 337:1343–1348. [PubMed][CrossRef]
52. Avnir Y, Tallarico AS, Zhu Q, Bennett AS, Connelly G, Sheehan J, Sui J, Fahmy A, Huang CY, Cadwell G, Bankston LA, McGuire AT, Stamatatos L, Wagner G, Liddington RC, Marasco WA. 2014. Molecular signatures of hemagglutinin stem-directed heterosubtypic human neutralizing antibodies against influenza A viruses. PLoS Pathog 10:e1004103. doi:10.1371/journal.ppat.1004103. [PubMed][CrossRef]
53. Ekiert DC, Kashyap AK, Steel J, Rubrum A, Bhabha G, Khayat R, Lee JH, Dillon MA, O'Neil RE, Faynboym AM, Horowitz M, Horowitz L, Ward AB, Palese P, Webby R, Lerner RA, Bhatt RR, Wilson IA. 2012. Cross-neutralization of influenza A viruses mediated by a single antibody loop. Nature 489:526–532. [PubMed][CrossRef]
54. Iba Y, Fujii Y, Ohshima N, Sumida T, Kubota-Koketsu R, Ikeda M, Wakiyama M, Shirouzu M, Okada J, Okuno Y, Kurosawa Y, Yokoyama S. Conserved neutralizing epitope at globular head of hemagglutinin in H3N2 influenza viruses. J Virol 88:7130–7144. [PubMed][CrossRef]
55. Caton AJ, Brownlee GG, Yewdell JW, Gerhard W. 1982. The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 31:417–427. [PubMed][CrossRef]
56. Bartesaghi A, Merk A, Borgnia MJ, Milne JL, Subramaniam S. 2013. Prefusion structure of trimeric HIV-1 envelope glycoprotein determined by cryo-electron microscopy. Nat Struct Mol Biol 20:1352–1357. [PubMed][CrossRef]
57. Taylor BS, Sobieszczyk ME, McCutchan FE, Hammer SM. The challenge of HIV-1 subtype diversity. N Engl J Med 358:1590–1602. [PubMed][CrossRef]
58. Quakkelaar ED, Bunnik EM, van Alphen FP, Boeser-Nunnink BD, van Nuenen AC, Schuitemaker H. 2007. Escape of human immunodeficiency virus type 1 from broadly neutralizing antibodies is not associated with a reduction of viral replicative capacity in vitro. Virology 363:447–453. [PubMed][CrossRef]
59. Burton DR, Barbas CF, 3rd, Persson MA, Koenig S, Chanock RM, Lerner RA. 1991. A large array of human monoclonal antibodies to type 1 human immunodeficiency virus from combinatorial libraries of asymptomatic seropositive individuals. Proc Natl Acad Sci USA 88:10134–10137. [CrossRef]
60. Burton DR, Pyati J, Kodrui R, Sharp SJ, Thornton GB, Parren PW, Sawyer LA, Hendry RM, Dunlop N, Nara PL, Lamacchia M, Garratty E, Stiehm ER, Bryson YJ, Cao Y, Moore JP, Ho DD, Barbas CF, 3rd. 1994. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266:1024–1027. [PubMed][CrossRef]
61. Zwick MB, Labrijn AF, Wang M, Spenlehauer C, Saphire EO, Binley JM, Moore JP, Stiegler G, Katinger H, Burton DR, Parren PW. 2001. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J Virol 75:10892–10905. [PubMed][CrossRef]
62. Zhu Z, Qin HR, Chen W, Zhao Q, Shen X, Schutte R, Wang Y, Ofek G, Streaker E, Prabakaran P, Fouda GG, Liao HX, Owens J, Louder M, Yang Y, Klaric KA, Moody MA, Mascola JR, Scott JK, Kwong PD, Montefiori D, Haynes BF, Tomaras GD, Dimitrov DS. 2011. Cross-reactive HIV-1-neutralizing human monoclonal antibodies identified from a patient with 2F5-like antibodies. J Virol 85:11401–11408. [PubMed][CrossRef]
63. Choudhry V, Zhang MY, Sidorov IA, Louis JM, Harris I, Dimitrov AS, Bouma P, Cham F, Choudhary A, Rybak SM, Fouts T, Montefiori DC, Broder CC, Quinnan GV, Jr, Dimitrov DS. 2007. Cross-reactive HIV-1 neutralizing monoclonal antibodies selected by screening of an immune human phage library against an envelope glycoprotein (gp140) isolated from a patient (R2) with broadly HIV-1 neutralizing antibodies. Virology 363:79–90. [PubMed][CrossRef]
64. Yoshikawa M, Mukai Y, Tsunoda S, Tsutsumi Y, Yoshioka Y, Okada N, Nakagawa S. 2011. Modifying the antigen-immunization schedule improves the variety of monoclonal antibodies obtained from immune-phage antibody libraries against HIV-1 Nef and Vif. J Biosci Bioeng 111:597–599. [PubMed][CrossRef]
65. Sui J, Li W, Murakami A, Tamin A, Matthews LJ, Wong SK, Moore MJ, Tallarico AS, Olurinde M, Choe H, Anderson LJ, Bellini WJ, Farzan M, Marasco WA. 2004. Potent neutralization of severe acute respiratory syndrome (SARS) coronavirus by a human mAb to S1 protein that blocks receptor association. Proc Natl Acad Sci USA 101:2536–2541. [PubMed][CrossRef]
66. Prabakaran P, Gan J, Feng Y, Zhu Z, Choudhry V, Xiao X, Ji X, Dimitrov DS. 2006. Structure of severe acute respiratory syndrome coronavirus receptor-binding domain complexed with neutralizing antibody. J Biol Chem 281:15829–15836. [PubMed][CrossRef]
67. Ferguson NM, Van Kerkhove MD. 2014. Identification of MERS-CoV in dromedary camels. Lancet Infect Dis 14:93–94. [PubMed][CrossRef]
68. Memish ZA, Mishra N, Olival KJ, Fagbo SF, Kapoor V, Epstein JH, Alhakeem R, Durosinloun A, Al Asmari M, Islam A, Kapoor A, Briese T, Daszak P, Al Rabeeah AA, Lipkin WI. 2013. Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis 19:1819–1823. [PubMed][CrossRef]
69. Raj VS, Mou H, Smits SL, Dekkers DH, Müller MA, Dijkman R, Muth D, Demmers JA, Zaki A, Fouchier RA, Thiel V, Drosten C, Rottier PJ, Osterhaus AD, Bosch BJ, Haagmans BL. Dipeptidyl pepetidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495:251–254. [PubMed][CrossRef]
70. Graham RL, Donaldson EF, Baric RS. A decade after SARS: strategies for controlling emerging coronaviruses. Nat Rev Microbiol 11:836–848. [PubMed][CrossRef]
71. Gierer S, Bertram S, Kaup F, Wrensch F, Heurich A, Krämer-Kühl A, Welsch K, Winkler M, Meyer B, Drosten C, Dittmer U, von Hahn T, Simmons G, Hofmann H, Pöhlmann S. 2013. The spike protein of the emerging coronavirus EMC uses a novel coronavirus receptor for entry, can be activated by TMPRSS2, and is targeted by neutralizing antibodies. J Virol 87:5502–5511. [PubMed][CrossRef]
72. Tang XC, Agnihothram SS, Jiao Y, Stanhope J, Graham RL, Peterson EC, Avnir Y, Tallarico AS, Sheehan J, Zhu Q, Baric RS, Marasco WA. 2014. Identification of human neutralizing antibodies against MERS-CoV and their role in virus adaptive evolution. Proc Natl Acad Sci USA 111:E2018–E2026. [PubMed][CrossRef]
73. Ying T, Du L, Ju TW, Prabakaran P, Lau CC, Lu L, Liu Q, Wang L, Feng Y, Wang Y, Zheng BJ, Yuen KY, Jiang S, Dimitrov DS. 2014. Exceptionally potent neutralization of Middle East respiratory syndrome coronavirus by human monoclonal antibodies. J Virol 88:7796–7805. [PubMed][CrossRef]
74. Gould LH, Sui J, Foellmer H, Oliphant T, Wang T, Ledizet M, Murakami A, Noonan K, Lambeth C, Kar K, Anderson JF, de Silva AM, Diamond MS, Koski RA, Marasco WA, Fikrig E. 2005. Protective and therapeutic capacity of human single-chain Fv-Fc fusion proteins against West Nile Virus. J Virol 79:14606–14613. [PubMed][CrossRef]
75. Throsby M, Geuijen C, Goudsmit J, Bakker AQ, Korimbocus J, Kramer RA, Clijsters-van der Horst M, de Jong M, Jongeneelen M, Thijsse S, Smit R, Visser TJ, Bijl N, Marissen WE, Loeb M, Kelvin DJ, Preiser W, ter Meulen J, de Kruif J. 2006. Isolation and charactertization of human monoclonal antibodies from individuals infected with West Nile Virus. J Virol 80:6982–6992. [PubMed][CrossRef]
76. Cabezas S, Rojas G, Pavon A, Alvarez M, Pupo M, Guillen G, Guzman MG. 2008. Selection of phage-displayed human antibody fragments on dengue virus particles captured by a monoclonal antibody: application to the four serotypes. J Virol Methods 147:235–243. [PubMed][CrossRef]
77. Zhao Y, Moreland NJ, Tay MY, Lee CC, Swaminathan K, Vasudevan SG. 2014. Identification and molecular characterization of human antibody fragments specific for dengue NS5 protein. Virus Res 179:225–230. [PubMed][CrossRef]
78. Maruyama T, Rodriguez LL, Jahrling PB, Sanchez A, Khan AS, Nichol ST, Peters CJ, Parren PW, Burton DR. 1999. Ebola virus can be effectively neutralized by antibody produced in natural human infection. J Virol 73:6024–6030. [PubMed]
79. Barbas CF, 3rd, Crowe JE, Jr, Cababa D, Jones TM, Zebedee SL, Murphy BR, Chanock RM, Burton DR. 1992. Human monoclonal Fab fragments derived from a combinatorial library bind to respiratory syncytial virus F glycoprotein and neutralize infectivity. Proc Natl Acad Sci USA 89:10164–10168. [PubMed][CrossRef]
80. Crowe JE, Jr, Murphy BR, Chanock RM, Williamson RA, Barbas CF, 3rd, Burton DR. 1994. Recombinant human respiratory syncytial virus (RSV) monoclonal antibody Fab is effective therapeutically when introduced directly into the lungs of RSV-infected mice. Proc Natl Acad Sci USA 91:1386–1390. [PubMed][CrossRef]
81. Burioni R, Williamson RA, Sanna PP, Bloom FE, Burton DR. 1994. Recombinant human Fab to glycoprotein D neutralizes infectivity and prevents cell-to-cell transmission of herpes simplex viruses 1 and 2 in vitro. Proc Natl Acad Sci USA 91:355–359. [PubMed][CrossRef]
82. Christensen DJ, Gottlin EB, Benson RE, Hamilton PT. 2001. Phage display for target-based antibacterial drug discovery. Drug Discov Today 6:721–727. [PubMed][CrossRef]
83. Lee HS, Loh YX, Lee JJ, Liu CS, Chu C. 2014. Antimicrobial consumption and resistance in five Gram-negative bacterial species in a hospital from 2003 to 2011. J Microbiol Immunol Infect S1684:1182(14)00074-7. doi:10.1016/j.jmii.2014.04.009. [PubMed][CrossRef]
84. Velayati AA, Masjedi MR, Farnia P, Tabarsi P, Ghanavi J, Ziazarifi AH, Hoffner SE. 2009. Emergence of new forms of totally drug-resistant tuberculosis bacilli: super extensively drug-resistant tuberculosis or totally drug-resistant strains in Iran. Chest 136:420–425. [PubMed][CrossRef]
85. Ford C, Yusim K, Ioerger T, Feng S, Chase M, Greene M, Korber B, Fortune S. 2012. Mycobacterium tuberculosis—heterogeneity revealed through whole genome sequencing. Tuberculosis (Edinb) 92:194–201. [PubMed][CrossRef]
86. Gronski P, Seiler FR, Schwick HG. 1991. Discovery of antitoxins and development of antibody preparations for clinical uses from 1890 to 1990. Mol Immunol 28:1321–1332. [PubMed][CrossRef]
87. Oleksiewicz MB, Nagy G, Nagy E. 2012. Anti-bacterial monoclonal antibodies: back to the future? Arch Biochem Biophys 526:124–131. [PubMed][CrossRef]
88. Amersdorfer P, Wong C, Smith T, Chen S, Deshpande S, Sheridan R, Marks JD. 2002. Genetic and immunological comparison of anti-botulinum type A antibodies from immune and non-immune human phage libraries. Vaccine 20:1640–1648. [PubMed][CrossRef]
89. Rossetto O, Pirazzini M, Bolognese P, Rigoni M, Montecucco C. 2011. An update of the mechanism of action of tetanus and botulinum neurotoxins. Acta Chim Slov 58:702–707. [PubMed]
90. Amersdorfer P, Wong C, Chen S, Smith T, Deshpande S, Sheridan R, Finnern R, Marks JD. 1997. Molecular charactertization of murine humoral immune response to botulinum neurotoxin type A binding domain as assessed by using phage antibody libraries. Infect Immun 65:3743–3752. [PubMed]
91. Marks JD. 2004. Deciphering antibody properties that lead to potent botulinum neurotoxin neutralization. Mov Disord 19(Suppl 8):S101–S108. [PubMed][CrossRef]
92. Jernigan DB, Raghunathan PL, Bell BP, Brechner R, Bresnitz EA, Butler JC, Cetron M, Cohen M, Doyle T, Fischer M, Greene C, Griffith KS, Guarner J, Hadler JL, Hayslett JA, Meyer R, Petersen LR, Phillips M, Pinner R, Popovic T, Quinn CP, Reefhuis J, Reissman D, Rosenstein N, Schuchat A, Shieh WJ, Siegal L, Swerdlow DL, Tenover FC, Traeger M, Ward JW, Weisfuse I, Wiersma S, Yeskey K, Zaki S, Ashford DA, Perkins BA, Ostroff S, Hughes J, Fleming D, Koplan JP, Gerberding JL. 2002. Investigation of bioterrorism-related anthrax, United States, 2001: epidemiologic findings. Emerg Infect Dis 8:1019–1028. [PubMed][CrossRef]
93. Chen Z, Moayeri M, Purcell R. 2011. Monoclonal antibody therapies against anthrax. Toxins (Basel) 3:1004–1019. [PubMed][CrossRef]
94. Migone TS, Subramanian GM, Zhong J, Healey LM, Corey A, Devalaraja M, Lo L, Ullrich S, Zimmerman J, Chen A, Lewis M, Meister G, Gillum K, Sanford D, Mott J, Bolmer SD. 2009. Raxibacumab for the treatment of inhalational anthrax. N Engl J Med 361:135–144. [PubMed][CrossRef]
95. Pelat T, Hust M, Laffly E, Condemine F, Bottex C, Vidal D, Lefranc MP, Dübel S, Thullier P. 2007. High-affinity, human antibody-like antibody fragment (single-chain variable fragment) neutralizing the lethal factor (LF) of Bacillus anthracis by inhibiting protective antigen-LF complex formation. Antimicrob Agents Chemother 51:2758–2764. [PubMed][CrossRef]
96. Chen Z, Moayeri M, Zhao H, Crown D, Leppla SH, Purcell RH. 2009. Potent neutralization of anthrax edema toxin by a humanized monoclonal antibody that competes with calmodulin for edema factor binding. Proc Natl Acad Sci USA 106:13487–13492. [PubMed][CrossRef]
97. Deng XK, Nesbit LA, Morrow KJ, Jr. 2003. Recombinant single-chain variable fragment antibodies directed against Clostridium difficile toxin B produced by use of an optimized phage display system. Clin Diagn Lab Immunol 10:587–595. [PubMed]
98. Neelakantam B, Sridevi NV, Shukra AM, Sugumar P, Samuel S, Rajendra L. 2014. Recombinant human antibody fragment against tetanus toxoid produced by phage display. Eur J Microbiol Immunol (Bp) 4:45–55. [PubMed][CrossRef]
99. Burnie JP, Matthews RC, Carter T, Beaulieu E, Donohoe M, Chapman C, Williamson P, Hodgetts SJ. 2000. Identification of an immunodominant ABC transporter in methicillin-resistant Staphylococcus aureus infections. Infect Immun 68:3200–3209. [PubMed][CrossRef]
100. Gera N, Hussain M, Rao BM. 2013. Protein selection using yeast surface display. Methods 60:15–26. [PubMed][CrossRef]
101. Lipke PN, Kurjan J. 2000. Sexual agglutination in budding yeasts: structure, function, and regulation of adhesion glycoproteins. Microbiol Rev 56:180–194. [PubMed]
102. Boder ET, Raeeszadeh-Sarmazdeh M, Price JV. 2012. Engineering antibodies by yeast display. Arch Biochem Biophys 526:99–106. [PubMed][CrossRef]
103. Chao G, Lau WL, Hackel BJ, Sazinsky SL, Lippow SM, Wittrup KD. 2006. Isolating and engineering human antibodies using yeast surface display. Nat Protoc 1:755–768. [PubMed][CrossRef]
104. Benatuil L, Perez JM, Belk J, Hsieh CM. 2010. An improved yeast transformation method for the generation of very large human antibody libraries. Protein Eng Des Sel 23:155–159. [PubMed][CrossRef]
105. Ferrara F, Naranjo LA, Kumar S, Gaiotto T, Mukundan H, Swanson B, Bradbury AR. 2012. Using phage and yeast display to select hundreds of monoclonal antibodies: application to antigen 85, a tuberculosis marker. PLoS One 7:e49535. doi:10.1371/journal.pone.0049535. [PubMed][CrossRef]
106. Bowley DR, Labrijn AF, Zwick MB, Burton DR. 2007. Antigen selection from an HIV-1 immune antibody library displayed on yeast yields many novel antibodies compared to selection from the same library displayed on phage. Protein Eng Des Sel 20:81–90. [PubMed][CrossRef]
107. Oliphant T, Engle M, Nybakken GE, Doane C, Johnson S, Huang L, Gorlatov S, Mehlhop E, Marri A, Chung KM, Ebel GD, Kramer LD, Fremont DH, Diamond MS. 2005. Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat Med 11:522–530. [PubMed][CrossRef]
108. Shrestha B, Brien JD, Sukupolvi-Petty S, Austin SK, Edeling MA, Kim T, O'Brien KM, Nelson CA, Johnson S, Fremont DH, Diamond MS. 2010. The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog 6:e1000823. doi:10.1371/journal.ppat.1000823. [PubMed][CrossRef]
109. Sukupolvi-Petty S, Austin SK, Engle M, Brien JD, Dowd KA, Williams KL, Johnson S, Rico-Hesse R, Harris E, Pierson TC, Fremont DH, Diamond MS. 2010. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J Virol 84:9227–9239. [PubMed][CrossRef]
110. Brien JD, Austin SK, Sukupolvi-Petty S, O'Brien KM, Johnson S, Fremont DH, Diamond MS. 2010. Genotype-specific neutralization and protection by antibodies against dengue virus type 3. J Virol 84:10630–10643. [PubMed][CrossRef]
111. Sukupolvi-Petty S, Brien JD, Austin SK, Shrestha B, Swayne S, Kahle K, Doranz BJ, Johnson S, Pierson TC, Fremont DH, Diamond MS. 2013. Functional analysis of antibodies against dengue virus type 4 reveals strain-dependent epitope exposure that impacts neutralization and protection. J Virol 87:8826–8842. [PubMed][CrossRef]
112. Puri V, Streaker E, Prabakaran P, Zhu Z, Dimitrov DS. 2013. Highly efficient selection of epitope specific antibody through competitive yeast display library sorting. MAbs 5:533–539. [PubMed][CrossRef]
113. Han T, Sui J, Bennett AS, Liddington RC, Donis RO, Zhu Q, Marasco WA. 2011. Fine epitope mapping of monoclonal antibodies against hemagglutinin of a highly pathogenic H5N1 influenza virus using yeast surface display. Biochem Biophys Res Commun 409:253–259. [PubMed][CrossRef]
114. Hu H, Voss J, Zhang G, Buchy P, Zuo T, Wang L, Wang F, Zhou F, Wang G, Tsai C, Calder L, Gamblin SJ, Zhang L, Deubel V, Zhou B, Skehel JJ, Zhou P. 2012. A human antibody recognizing a conserved epitope of H5 hemagglutinin broadly neutralizes highly pathogenic avian influenza. J Virol 86:2978–2989. [PubMed][CrossRef]
115. Gray SA, Barr JR, Kalb SR, Marks JD, Baird CL, Cangelosi GA, Miller KD, Feldhaus MJ. 2011. Synergistic capture of Clostridium botulinum type A neurotoxin by scFv antibodies to novel epitopes. Biotechnol Bioeng 108:2456–2467. [PubMed][CrossRef]
116. Garcia-Rodriguez C, Geren IN, Lou J, Conrad F, Forsyth C, Wen W, Chakraborti S, Zao H, Manzanarez G, Smith TJ, Brown J, Tepp WH, Liu N, Wijesuriya S, Tomic MT, Johnson EA, Smith LA, Marks JD. 2011. Neutralizing human monoclonal antibodies binding multiple serotypes of botulinum neutrotoxin. Protein Eng Des Sel 24:321–331. [PubMed][CrossRef]
117. Lou J, Geren I, Garcia-Rodriguez C, Forsyth CM, Wen W, Knopp K, Brown J, Smith T, Smith LA, Marks JD. 2010. Affinity maturation of human botulinum neurotoxin antibodies by light chain shuffling via yeast mating. Protein Eng Des Sel 23:311–319. [PubMed][CrossRef]
118. Makiya M, Dolan M, Agulto L, Purcell R, Chen Z. 2012. Structural basis of anthrax edema factor neutralization by a neutralizing antibody. Biochem Biophys Res Commun 417:324–329. [PubMed][CrossRef]
119. Reason D, Liberato J, Sun J, Camacho J, Zhou J. 2011. Mechanism of lethal toxin neutralization by a human monoclonal antibody specific for the PA(20) region of Bacillus anthracis protective antigen. Toxins (Basel) 3:979–990. [PubMed][CrossRef]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.AID-0028-2014
2015-02-06
2019-08-18

Abstract:

Despite the availability of antimicrobial drugs, the continued development of microbial resistance—established through escape mutations and the emergence of resistant strains—limits their clinical utility. The discovery of novel, therapeutic, monoclonal antibodies (mAbs) offers viable clinical alternatives in the treatment and prophylaxis of infectious diseases. Human mAb-based therapies are typically nontoxic in patients and demonstrate high specificity for the intended microbial target. This specificity prevents negative impacts on the patient microbiome and avoids driving the resistance of nontarget species. The selection of human antibody fragment libraries displayed on phage or yeast surfaces represents a group of well-established technologies capable of generating human mAbs. The advantage of these forms of microbial display is the large repertoire of human antibody fragments present during a single selection campaign. Furthermore, the selection environments of microbial surface display allow for the rapid isolation of antibodies—and their encoding genes—against infectious pathogens and their toxins that are impractical within systems, such as murine hybridomas. This article focuses on the technologies of phage display and yeast display, as these strategies relate to the discovery of human mAbs for the treatment and vaccine development of infectious diseases.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/3/1/AID-0028-2014.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.AID-0028-2014&mimeType=html&fmt=ahah

Figures

Phage and Yeast Display
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.AID-0028-2014-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.AID-0028-2014-1,properties={foaf_givenname=Jared, foaf_name=Jared Sheehan, foaf_surname=Sheehan, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.AID-0028-2014-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.AID-0028-2014-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.AID-0028-2014-2,properties={foaf_givenname=Wayne A., foaf_name=Wayne A. Marasco, foaf_surname=Marasco, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.AID-0028-2014-aff2]]}]]
Citation: Sheehan J, Marasco W. 2015. Phage and yeast display. microbiolspec 3(1): doi:10.1128/microbiolspec.AID-0028-2014
/content/microbiolspec/10.1128/microbiolspec.AID-0028-2014.fig1
FIGURE 1
Overview of phage antibody library production and selections. (A) The phage antibody library repertoire is derived from the B cells of naïve or immune donors. The amplified and genes are subcloned into a phage display vector for expression and library production. (B) The phage antibody library is selected against an immobilized target antigen. After washing to remove nonbinders, the Ag-reactive phage antibodies are eluted, amplified, and reselected through subsequent rounds. ELISA screens identify monoclonal, Ag-binding phage antibodies, whose heavy and light chain antibody genes are subcloned into mammalian expression vectors.
microbiolspec/3/1/AID-0028-2014-fig1_thmb.gif
microbiolspec/3/1/AID-0028-2014-fig1.gif
Image of FIGURE 1

Click to view

FIGURE 1

Overview of phage antibody library production and selections. (A) The phage antibody library repertoire is derived from the B cells of naïve or immune donors. The amplified and genes are subcloned into a phage display vector for expression and library production. (B) The phage antibody library is selected against an immobilized target antigen. After washing to remove nonbinders, the Ag-reactive phage antibodies are eluted, amplified, and reselected through subsequent rounds. ELISA screens identify monoclonal, Ag-binding phage antibodies, whose heavy and light chain antibody genes are subcloned into mammalian expression vectors.

Source: microbiolspec February 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.AID-0028-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.AID-0028-2014.fig2
FIGURE 2
Types of phage antibody display. (A) Monovalent display with the scFv or Fab fusion (green circle) to truncated pIII along with wild-type copies of pIII (purple circles). This monovalent mAb display format can also be used with pVII (olive) or pIX (light blue) separately. (B) Multivalent display with the scFv or Fab fusion to all copies of truncated pIII. Multivalent mAb display is also possible with the major coat protein pVIII (black border) separate from pIII. The pVI (red circles) coat proteins are also present in these diagrams.
microbiolspec/3/1/AID-0028-2014-fig2_thmb.gif
microbiolspec/3/1/AID-0028-2014-fig2.gif
Image of FIGURE 2

Click to view

FIGURE 2

Types of phage antibody display. (A) Monovalent display with the scFv or Fab fusion (green circle) to truncated pIII along with wild-type copies of pIII (purple circles). This monovalent mAb display format can also be used with pVII (olive) or pIX (light blue) separately. (B) Multivalent display with the scFv or Fab fusion to all copies of truncated pIII. Multivalent mAb display is also possible with the major coat protein pVIII (black border) separate from pIII. The pVI (red circles) coat proteins are also present in these diagrams.

Source: microbiolspec February 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.AID-0028-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.AID-0028-2014.fig3
FIGURE 3
Overview of yeast antibody display. The scFv (or Fab) is displayed as a fusion product with the Aga2p protein (light blue). This fusion product can be detected and normalized by fluorescent signaling through the HA tags (orange) and c-Myc tags (dark blue). During FACS selections, the Ag-reactive library variants are detected through the fluorescent avidin tag (pink) on the biotinylated target antigen (red).
microbiolspec/3/1/AID-0028-2014-fig3_thmb.gif
microbiolspec/3/1/AID-0028-2014-fig3.gif
Image of FIGURE 3

Click to view

FIGURE 3

Overview of yeast antibody display. The scFv (or Fab) is displayed as a fusion product with the Aga2p protein (light blue). This fusion product can be detected and normalized by fluorescent signaling through the HA tags (orange) and c-Myc tags (dark blue). During FACS selections, the Ag-reactive library variants are detected through the fluorescent avidin tag (pink) on the biotinylated target antigen (red).

Source: microbiolspec February 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.AID-0028-2014
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Phage and Yeast Display
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.AID-0028-2014-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.AID-0028-2014-1,properties={foaf_givenname=Jared, foaf_name=Jared Sheehan, foaf_surname=Sheehan, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.AID-0028-2014-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.AID-0028-2014-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.AID-0028-2014-2,properties={foaf_givenname=Wayne A., foaf_name=Wayne A. Marasco, foaf_surname=Marasco, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.AID-0028-2014-aff2]]}]]
Citation: Sheehan J, Marasco W. 2015. Phage and yeast display. microbiolspec 3(1): doi:10.1128/microbiolspec.AID-0028-2014
/content/microbiolspec/10.1128/microbiolspec.AID-0028-2014.T1
TABLE 1
Summary of antiviral antibodies discovered using phage display
Generic image for table

Click to view

TABLE 1

Summary of antiviral antibodies discovered using phage display

Source: microbiolspec February 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.AID-0028-2014
/content/microbiolspec/10.1128/microbiolspec.AID-0028-2014.T2
TABLE 2
Summary of antibacterial antibodies discovered using phage display
Generic image for table

Click to view

TABLE 2

Summary of antibacterial antibodies discovered using phage display

Source: microbiolspec February 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.AID-0028-2014
/content/microbiolspec/10.1128/microbiolspec.AID-0028-2014.T3
TABLE 3
Summary of antiviral antibodies discovered using yeast display
Generic image for table

Click to view

TABLE 3

Summary of antiviral antibodies discovered using yeast display

Source: microbiolspec February 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.AID-0028-2014
/content/microbiolspec/10.1128/microbiolspec.AID-0028-2014.T4
TABLE 4
Summary of antibacterial antibodies discovered using yeast display
Generic image for table

Click to view

TABLE 4

Summary of antibacterial antibodies discovered using yeast display

Source: microbiolspec February 2015 vol. 3 no. 1 doi:10.1128/microbiolspec.AID-0028-2014

Supplemental Material

No supplementary material available for this content.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error