A high-affinity native human antibody neutralizes human cytomegalovirus infection of diverse cell types

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 3, 2015, Pages 1558-1568

  Kauvar, Lawrence M ^a   Liu, Keyi ^a   Park, Minha ^a   DeChene, Neal ^a   Stephenson, Robert ^a   Tenorio, Edgar ^a   Ellsworth, Stote L ^a   Tabata, Takako ^b   Petitt, Matthew ^b   Tsuge, Mitsuru ^b   Fang Hoover, June ^b   Adler, Stuart P ^c   Cui, Xiaohong ^d   McVoy, Michael A ^d   Pereira, Lenore ^b  

^a Trellis Bioscience   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; GLYCOPROTEIN B; NEUTRALIZING ANTIBODY; TRL345; UNCLASSIFIED DRUG; EPITOPE; IMMUNOGLOBULIN G; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; AREA UNDER THE CURVE; ARTICLE; BINDING AFFINITY; CELLS BY BODY ANATOMY; CONTROLLED STUDY; CROSS REACTION; CYTOMEGALOVIRUS INFECTION; CYTOTROPHOBLAST; DRUG CLEARANCE; DRUG HALF LIFE; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; EPITOPE MAPPING; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IMMUNOGLOBULIN PRODUCTION; MALE; MAXIMUM PLASMA CONCENTRATION; MEMORY CELL; NONHUMAN; PLACENTA; PRIORITY JOURNAL; PROTEIN TARGETING; RAT; SINGLE DRUG DOSE; SMOOTH MUSCLE FIBER; STEM CELL; TIME TO MAXIMUM PLASMA CONCENTRATION; TROPHOBLAST; VIRUS NEUTRALIZATION; VIRUS STRAIN; VIRUS TRANSMISSION; VOLUME OF DISTRIBUTION AT STEADY-STATE; ANTIBODY AFFINITY; B LYMPHOCYTE; CELL LINE; CYTOMEGALOVIRUS; FEMALE; IMMUNOLOGY; PREGNANCY; VIROLOGY;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; B-LYMPHOCYTES; CELL LINE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; ENDOTHELIAL CELLS; EPITHELIAL CELLS; EPITOPES; FEMALE; FIBROBLASTS; HUMANS; IMMUNOGLOBULIN G; MYOCYTES, SMOOTH MUSCLE; PLACENTA; PREGNANCY; VIRAL ENVELOPE PROTEINS;

EID: 84923249674     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.04295-14     Document Type: Article

References (86)

1. Kotton CN, Kumar D, Caliendo AM, Asberg A, Chou S, Danziger-Isakov L, Humar A, Transplantation Society International CMV Consensus Group. 2013. Updated international consensus guidelines on the management of cytomegalovirus in solid-organ transplantation. Transplantation 96:333-360. http://dx.doi.org/10.1097/TP.0b013e31829df29d.
2. Fowler KB, Stagno S, Pass RF, Britt WJ, Boll TJ, Alford CA. 1992. The outcome of congenital cytomegalovirus infection in relation to maternal antibody status. N Engl J Med 326:663-667. http://dx.doi.org/10.1056/NEJM199203053261003.
3. Stagno S, Pass RF, Cloud G, Britt WJ, Henderson RE, Walton PD, Veren DA, Page F, Alford CA. 1986. Primary cytomegalovirus infection in pregnancy. Incidence, transmission to fetus, and clinical outcome. JAMA 256:1904-1908.
4. Turner KM, Lee HC, Boppana SB, Carlo WA, Randolph DA. 2014. Incidence and impact of CMV infection in very low birth weight infants. Pediatrics 133:e609-e615. http://dx.doi.org/10.1542/peds.2013-2217.
5. Zavattoni M, Lombardi G, Rognoni V, Furione M, Klersy C, Stronati M, Baldanti F. 2014. Maternal, fetal, and neonatal parameters for prognosis and counseling of HCMV congenital infection. J Med Virol 86: 2163-2170. http://dx.doi.org/10.1002/jmv.23954.
6. Yamamoto AY, Mussi-Pinhata MM, Isaac Mde L, Amaral FR, Carvalheiro CG, Aragon DC, Manfredi AK, Boppana SB, Britt WJ. 2011. Congenital cytomegalovirus infection as a cause of sensorineural hearing loss in a highly immune population. Pediatr Infect Dis J 30:1043-1046. http://dx.doi.org/10.1097/INF.0b013e31822d9640.
7. Barker DJ. 1999. Fetal origins of cardiovascular disease. Ann Med 31(Suppl 1):S3-S6.
8. Syridou G, Spanakis N, Konstantinidou A, Piperaki ET, Kafetzis D, Patsouris E, Antsaklis A, Tsakris A. 2008. Detection of cytomegalovirus, parvovirus B19 and herpes simplex viruses in cases of intrauterine fetal death: association with pathological findings. J Med Virol 80:1776-1782. http://dx.doi.org/10.1002/jmv.21293.
9. Iwasenko JM, Howard J, Arbuckle S, Graf N, Hall B, Craig ME, Rawlinson WD. 2011. Human cytomegalovirus infection is detected frequently in stillbirths and is associated with fetal thrombotic vasculopathy. J Infect Dis 203:1526-1533. http://dx.doi.org/10.1093/infdis/jir121.
10. Racicot K, Cardenas I, Wunsche V, Aldo P, Guller S, Means RE, Romero R, Mor G. 2013. Viral infection of the pregnant cervix predisposes to ascending bacterial infection. J Immunol 191:934-941. http://dx.doi.org/10.4049/jimmunol.1300661.
11. Nigro G, Capretti I, Manganello AM, Best AM, Adler SP. 25 April 2014. Primary maternal cytomegalovirus infections during pregnancy: association of CMVhyperimmune globulin with gestational age at birth and birth weight. J Matern Fetal Neonatal Med, in press. http://dx.doi.org/10.3109/14767058.2014.907265.-.
12. Boppana SB, Britt WJ. 2014. Recent approaches and strategies in the generation of antihuman cytomegalovirus vaccines. Methods Mol Biol 1119:311-348. http://dx.doi.org/10.1007/978-1-62703-788-4-17.
13. McVoy MA. 2013. Cytomegalovirus vaccines. Clin Infect Dis 57(Suppl 4):S196-S199. http://dx.doi.org/10.1093/cid/cit587.
14. Samuel ER, Beloki L, Newton K, Mackinnon S, Lowdell MW. 2014. Isolation of highly suppressive CD25+ FoxP3+ T regulatory cells from G-CSF-mobilized donors with retention of cytotoxic anti-viral CTLs: application for multi-functional immunotherapy post stem cell transplantation. PLoS One 9:e85911. http://dx.doi.org/10.1371/journal.pone.0085911.
15. Bunse CE, Borchers S, Varanasi PR, Tischer S, Figueiredo C, Immenschuh S, Kalinke U, Kohl U, Goudeva L, Maecker-Kolhoff B, Ganser A, Blasczyk R, Weissinger EM, Eiz-Vesper B. 2013. Impaired functionality of antiviral T cells in G-CSF mobilized stem cell donors: implications for the selection of CTL donor. PLoS One 8:e77925. http://dx.doi.org/10.1371/journal.pone.0077925.
16. Clark AL, Gall SA. 1997. Clinical uses of intravenous immunoglobulin in pregnancy. Am J Obstet Gynecol 176:241-253. http://dx.doi.org/10.1016/S0002-9378(97)80043-9.
17. La Torre R, Nigro G, Mazzocco M, Best AM, Adler SP. 2006. Placental enlargement in women with primary maternal cytomegalovirus infection is associated with fetal and neonatal disease. Clin Infect Dis 43:994-1000. http://dx.doi.org/10.1086/507634.
18. Nigro G, Adler SP, La Torre R, Best AM, Congenital Cytomegalovirus Collaborating Group. 2005. Passive immunization during pregnancy for congenital cytomegalovirus infection.NEngl J Med 353:1350-1362. http://dx.doi.org/10.1056/NEJMoa043337.
19. Nigro G, La Torre R, Anceschi MM, Mazzocco M, Cosmi EV. 1999. Hyperimmunoglobulin therapy for a twin fetus with cytomegalovirus infection and growth restriction. Am J Obstet Gynecol 180:1222-1226. http://dx.doi.org/10.1016/S0002-9378(99)70620-4.
20. Moxley K, Knudtson EJ. 2008. Resolution of hydrops secondary to cytomegalovirus after maternal and fetal treatment with human cytomegalovirus hyperimmune globulin. Obstet Gynecol 111:524-526. http://dx.doi.org/10.1097/01.AOG.0000281669.19021.0f.
21. Moise KJ, Wolfe H. 2008. Treatment of second trimester fetal cytomegalovirus infection with maternal hyperimmune globulin. Prenat Diagn 28:264-265. http://dx.doi.org/10.1002/pd.1954.
22. Revello MG, Lazzarotto T, Guerra B, Spinillo A, Ferrazzi E, Kustermann A, Guaschino S, Vergani P, Todros T, Frusca T, Arossa A, Furione M, Rognoni V, Rizzo N, Gabrielli L, Klersy C, Gerna G, CHIP Study Group. 2014. A randomized trial of hyperimmune globulin to prevent congenital cytomegalovirus. N Engl J Med 370:1316-1326. http://dx.doi.org/10.1056/NEJMoa1310214.
23. Adler SP. 2012. Editorial commentary: primary maternal cytomegalovirus infection during pregnancy: do we have a treatment option? Clin Infect Dis 55:504-506. http://dx.doi.org/10.1093/cid/cis425.
24. Berry JD, Gaudet RG. 2011. Antibodies in infectious diseases: polyclonals, monoclonals and niche biotechnology.NBiotechnol 28:489-501. http://dx.doi.org/10.1016/j.nbt.2011.03.018.
25. Saylor C, Dadachova E, Casadevall A. 2009. Monoclonal antibody-based therapies for microbial diseases. Vaccine 27(Suppl 6):G38-G46. http://dx.doi.org/10.1016/j.vaccine.2009.09.105.
26. Mocarski ES, Jr. 2002. Immunomodulation by cytomegaloviruses: manipulative strategies beyond evasion. Trends Microbiol 10:332-339. http://dx.doi.org/10.1016/S0966-842X(02)02393-4.
27. Pass RF, Zhang C, Evans A, Simpson T, Andrews W, Huang ML, Corey L, Hill J, Davis E, Flanigan C, Cloud G. 2009. Vaccine prevention of maternal cytomegalovirus infection. N Engl J Med 360:1191-1199. http://dx.doi.org/10.1056/NEJMoa0804749.
28. Lantto J, Fletcher JM, Ohlin M. 2003. Binding characteristics determine the neutralizing potential of antibody fragments specific for antigenic domain 2 on glycoprotein B of human cytomegalovirus. Virology 305:201-209. http://dx.doi.org/10.1006/viro.2002.1752.
29. Ohlin M. 2014. A new look at a poorly immunogenic neutralization epitope on cytomegalovirus glycoprotein B. Is there cause for antigen redesign? Mol Immunol 60:95-102. http://dx.doi.org/10.1016/j.molimm.2014.03.015.
30. Ohlin M, Sundqvist VA, Mach M, Wahren B, Borrebaeck CA. 1993. Fine specificity of the human immune response to the major neutralization epitopes expressed on cytomegalovirus gp58/116 (gB), as determined with human monoclonal antibodies. J Virol 67:703-710.
31. Wang D, Shenk T. 2005. Human cytomegalovirus virion protein complex required for epithelial and endothelial cell tropism. Proc Natl Acad Sci USA 102:18153-18158. http://dx.doi.org/10.1073/pnas.0509201102.
32. Freed DC, Tang Q, Tang A, Li F, He X, Huang Z, Meng W, Xia L, Finnefrock AC, Durr E, Espeseth AS, Casimiro DR, Zhang N, Shiver JW, Wang D, An Z, Fu TM. 2013. Pentameric complex of viral glycoprotein H is the primary target for potent neutralization by a human cytomegalovirus vaccine. Proc Natl Acad Sci U S A 110:E4997-E5005. http://dx.doi.org/10.1073/pnas.1316517110.
33. Cui X, Meza BP, Adler SP, McVoy MA. 2008. Cytomegalovirus vaccines fail to induce epithelial entry neutralizing antibodies comparable to natural infection. Vaccine 26:5760-5766. http://dx.doi.org/10.1016/j.vaccine.2008.07.092.
34. Fouts AE, Chan P, Stephan JP, Vandlen R, Feierbach B. 2012. Antibodies against the gH/gL/UL128/UL130/UL131 complex comprise the majority of the anti-cytomegalovirus (anti-CMV) neutralizing antibody response in CMV hyperimmune globulin. J Virol 86:7444-7447. http://dx.doi.org/10.1128/JVI.00467-12.
35. Revello MG, Fornara C, Arossa A, Zelini P, Lilleri D. 2014. Role of human cytomegalovirus (HCMV)-specific antibody in HCMV-infected pregnant women. Early Hum Dev 90(Suppl 1):S32-S34. http://dx.doi.org/10.1016/S0378-3782(14)70011-8.
36. Macagno A, Bernasconi NL, Vanzetta F, Dander E, Sarasini A, Revello MG, Gerna G, Sallusto F, Lanzavecchia A. 2010. Isolation of human monoclonal antibodies that potently neutralize human cytomegalovirus infection by targeting different epitopes on the gH/gL/UL128-131A complex. J Virol 84:1005-1013. http://dx.doi.org/10.1128/JVI.01809-09.
37. Fouts AE, Comps-Agrar L, Stengel KF, Ellerman D, Schoeffler AJ, Warming S, Eaton DL, Feierbach B. 2014. Mechanism for neutralizing activity by the anti-CMV gH/gL monoclonal antibody MSL-109. Proc Natl Acad Sci U S A 111:8209-8214. http://dx.doi.org/10.1073/pnas.1404653111.
38. Boppana SB, Britt WJ. 1995. Antiviral antibody responses and intrauterine transmission after primary maternal cytomegalovirus infection. J Infect Dis 171:1115-1121. http://dx.doi.org/10.1093/infdis/171.5.1115.
39. Maidji E, McDonagh S, Genbacev O, Tabata T, Pereira L. 2006. Maternal antibodies enhance or prevent cytomegalovirus infection in the placenta by neonatal Fc receptor-mediated transcytosis. Am J Pathol 168: 1210-1226. http://dx.doi.org/10.2353/ajpath.2006.050482.
40. Utz U, Britt W, Vugler L, Mach M. 1989. Identification of a neutralizing epitope on glycoprotein gp58 of human cytomegalovirus. J Virol 63:1995-2001.
41. Meyer H, Sundqvist VA, Pereira L, Mach M. 1992. Glycoprotein gp116 of human cytomegalovirus contains epitopes for strain-common and strain-specific antibodies. J Gen Virol 73:2375-2383.
42. Collarini EJ, Lee FE, Foord O, Park M, Sperinde G, Wu H, Harriman WD, Carroll SF, Ellsworth SL, Anderson LJ, Tripp RA, Walsh EE, Keyt BA, Kauvar LM. 2009. Potent high-affinity antibodies for treatment and prophylaxis of respiratory syncytial virus derived from B cells of infected patients. J Immunol 183:6338-6345. http://dx.doi.org/10.4049/jimmunol.0901373.
43. Harriman WD, Collarini EJ, Sperinde GV, Strandh M, Fatholahi MM, Dutta A, Lee Y, Mettler SE, Keyt BA, Ellsworth SL, Kauvar LM. 2009. Antibody discovery via multiplexed single cell characterization. J Immunol Methods 341:135-145. http://dx.doi.org/10.1016/j.jim.2008.11.009.
44. McCutcheon KM, Gray J, Chen NY, Liu K, Park M, Ellsworth S, Tripp RA, Tompkins SM, Johnson SK, Samet S, Pereira L, Kauvar LM. 2014. Multiplexed screening of natural humoral immunity identifies antibodies at fine specificity for complex and dynamic viral targets. MAbs 6:460-473. http://dx.doi.org/10.4161/mabs.27760.
45. Ilic D, Kapidzic M, Genbacev O. 2008. Isolation of human placental fibroblasts. Curr Protoc Stem Cell Biol Chapter 1:Unit 1C.6. http://dx.doi.org/10.1002/9780470151808.sc01c06s5.
46. Genbacev O, Donne M, Kapidzic M, Gormley M, Lamb J, Gilmore J, Larocque N, Goldfien G, Zdravkovic T, McMaster MT, Fisher SJ. 2011. Establishment of human trophoblast progenitor cell lines from the chorion. Stem Cells 29:1427-1436. http://dx.doi.org/10.1002/stem.686.
47. Zydek M, Petitt M, Fang-Hoover J, Adler B, Kauvar LM, Pereira L, Tabata T. 2014. HCMV infection of human trophoblast progenitor cells of the placenta is neutralized by a human monoclonal antibody to glycoprotein B and not by antibodies to the pentamer complex. Viruses 6:1346-1364. http://dx.doi.org/10.3390/v6031346.
48. Gospodarowicz D, Moran JS. 1975. Mitogenic effect of fibroblast growth factor on early passage cultures of human and murine fibroblasts. J Cell Biol 66:451-457. http://dx.doi.org/10.1083/jcb.66.2.451.
49. Wang D, Shenk T. 2005. Human cytomegalovirus UL131 open reading frame is required for epithelial cell tropism. J Virol 79:10330-10338. http://dx.doi.org/10.1128/JVI.79.16.10330-10338.2005.
50. Cui X, Lee R, Adler SP, McVoy MA. 2013. Antibody inhibition of human cytomegalovirus spread in epithelial cell cultures. J Virol Methods 192: 44-50. http://dx.doi.org/10.1016/j.jviromet.2013.04.015.
51. Cui X, Adler SP, Davison AJ, Smith L, Habib E-SE, McVoy MA. 2012. Bacterial artificial chromosome clones of viruses comprising the Towne cytomegalovirus vaccine. J Biomed Biotechnol 2012:428498. http://dx.doi.org/10.1155/2012/428498.
52. Adler SP. 1988. Molecular epidemiology of cytomegalovirus: viral transmission among children attending a day care center, their parents, and caretakers. J Pediatr 112:366-372. http://dx.doi.org/10.1016/S0022-3476(88)80314-7.
53. Chou SW, Dennison KM. 1991. Analysis of interstrain variation in cytomegalovirus glycoprotein B sequences encoding neutralization-related epitopes. J Infect Dis 163:1229-1234. http://dx.doi.org/10.1093/infdis/163.6.1229.
54. Durocher Y, Perret S, Kamen A. 2002. High-level and high-throughput recombinant protein production by transient transfection of suspensiongrowing human 293-EBNA1 cells. Nucleic Acids Res 30:E9. http://dx.doi.org/10.1093/nar/30.2.e9.
55. Benbrook DM. 2002. An ELISA method for detection of human antibodies to an immunotoxin. J Pharmacol Toxicol Methods 47:169-175. http://dx.doi.org/10.1016/S1056-8719(02)00232-0.
56. Ho D, Fletcher T, Ni JHT. 2013. Kinetic analysis of antibodies from different cultured media. BioPharm Int 51:55.
57. Saccoccio FM, Gallagher MK, Adler SP, McVoy MA. 2011. Neutralizing activity of saliva against cytomegalovirus. Clin Vaccine Immunol 18: 1536-1542. http://dx.doi.org/10.1128/CVI.05128-11.
58. Saccoccio FM, Sauer AL, Cui X, Armstrong AE, Habib el-SE, Johnson DC, Ryckman BJ, Klingelhutz AJ, Adler SP, McVoy MA. 2011. Peptides from cytomegalovirus UL130 and UL131 proteins induce high titer antibodies that block viral entry into mucosal epithelial cells. Vaccine 29: 2705-2711. http://dx.doi.org/10.1016/j.vaccine.2011.01.079.
59. Fisher S, Genbacev O, Maidji E, Pereira L. 2000. Human cytomegalovirus infection of placental cytotrophoblasts in vitro and in utero: implications for transmission and pathogenesis. J Virol 74:6808-6820. http://dx.doi.org/10.1128/JVI.74.15.6808-6820.2000.
60. Damsky CH, Fitzgerald ML, Fisher SJ. 1992. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest 89:210-222. http://dx.doi.org/10.1172/JCI115565.
61. Feire AL, Koss H, Compton T. 2004. Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrinlike domain. Proc Natl Acad SciUSA101:15470-15475. http://dx.doi.org/10.1073/pnas.0406821101.
62. Meyer-König U, Haberland M, von Laer D, Haller O, Hufert FT. 1998. Intragenic variability of human cytomegalovirus glycoprotein B in clinical strains. J Infect Dis 177:1162-1169. http://dx.doi.org/10.1086/515262.
63. Scrivano L, Sinzger C, Nitschko H, Koszinowski UH, Adler B. 2011. HCMV spread and cell tropism are determined by distinct virus populations. PLoS Pathog 7:e1001256. http://dx.doi.org/10.1371/journal.ppat.1001256.
64. Red-Horse K, Rivera J, Schanz A, Zhou Y, Winn V, Kapidzic M, Maltepe E, Okazaki K, Kochman R, Vo KC, Giudice L, Erlebacher A, McCune JM, Stoddart CA, Fisher SJ. 2006. Cytotrophoblast induction of arterial apoptosis and lymphangiogenesis in an in vivo model of human placentation. J Clin Invest 116:2643-2652. http://dx.doi.org/10.1172/JCI27306..
65. Tabata T, Petitt M, Fang-Hoover J, Rivera J, Nozawa N, Shiboski S, Inoue N, Pereira L. 2012. Cytomegalovirus impairs cytotrophoblast induced lymphangiogenesis and vascular remodeling in an in vivo human placentation model. Am J Pathol 181:1540-1559. http://dx.doi.org/10.1016/j.ajpath.2012.08.003.
66. Buck PM, Kumar S, Wang X, Agrawal NJ, Trout BL, Singh SK. 2012. Computational methods to predict therapeutic protein aggregation. Methods Mol Biol 899:425-451. http://dx.doi.org/10.1007/978-1-61779-921-1-26.
67. Lin YS, Nguyen C, Mendoza JL, Escandon E, Fei D, Meng YG, Modi NB. 1999. Preclinical pharmacokinetics, interspecies scaling, and tissue distribution of a humanized monoclonal antibody against vascular endothelial growth factor. J Pharmacol Exp Ther 288:371-378.
68. Leach MW, Halpern WG, Johnson CW, Rojko JL, MacLachlan TK, Chan CM, Galbreath EJ, Ndifor AM, Blanset DL, Polack E, Cavagnaro JA. 2010. Use of tissue cross-reactivity studies in the development of antibody-based biopharmaceuticals: history, experience, methodology, and future directions. Toxicol Pathol 38:1138-1166. http://dx.doi.org/10.1177/0192623310382559.
69. Bumbaca D, Wong A, Drake E, Reyes AE, Jr, Lin BC, Stephan JP, Desnoyers L, Shen BQ, Dennis MS. 2011. Highly specific off-target binding identified and eliminated during the humanization of an antibody against FGF receptor 4. MAbs 3:376-386. http://dx.doi.org/10.4161/mabs.3.4.15786.
70. Kalil AC, Freifeld AG, Lyden ER, Stoner JA. 2009. Valganciclovir for cytomegalovirus prevention in solid organ transplant patients: an evidence-based reassessment of safety and efficacy. PLoS One 4:e5512. http://dx.doi.org/10.1371/journal.pone.0005512.
71. Parruti G, Polilli E, Ursini T, Tontodonati M. 2013. Properties and mechanisms of immunoglobulins for congenital cytomegalovirus disease. Clin Infect Dis 57(Suppl 4):S185-S188. http://dx.doi.org/10.1093/cid/cit584.
72. Snydman DR. 2001. Historical overview of the use of cytomegalovirus hyperimmune globulin in organ transplantation. Transpl Infect Dis 3(Suppl 2):S6-S13. http://dx.doi.org/10.1034/j.1399-3062.2001.00002.x.
73. Borucki MJ, Spritzler J, Asmuth DM, Gnann J, Hirsch MS, Nokta M, Aweeka F, Nadler PI, Sattler F, Alston B, Nevin TT, Owens S, Waterman K, Hubbard L, Caliendo A, Pollard RB, AACTG 266 Team. 2004. A phase II, double-masked, randomized, placebo-controlled evaluation of a human monoclonal anti-cytomegalovirus antibody (MSL-109) in combination with standard therapy versus standard therapy alone in the treatment of AIDS patients with cytomegalovirus retinitis. Antiviral Res 64: 103-111. http://dx.doi.org/10.1016/j.antiviral.2004.06.012.
74. Auerbach MR, Yan D, Vij R, Hongo JA, Nakamura G, Vernes JM, Meng YG, Lein S, Chan P, Ross J, Carano R, Deng R, Lewin-Koh N, Xu M, Feierbach B. 2014. A neutralizing anti-gH/gL monoclonal antibody is protective in the guinea pig model of congenital CMV infection. PLoS Pathog 10:e1004060. http://dx.doi.org/10.1371/journal.ppat.1004060.
75. Ohta A, Fujita A, Murayama T, Iba Y, Kurosawa Y, Yoshikawa T, Asano Y. 2009. Recombinant human monoclonal antibodies to human cytomegalovirus glycoprotein B neutralize virus in a complement-dependent manner. Microbes Infect 11:1029-1036. http://dx.doi.org/10.1016/j.micinf.2009.07.010.
76. Schoppel K, Schmidt C, Einsele H, Hebart H, Mach M. 1998. Kinetics of the antibody response against human cytomegalovirus-specific proteins in allogeneic bone marrow transplant recipients. J Infect Dis 178: 1233-1243. http://dx.doi.org/10.1086/314428.
77. Wille PT, Knoche AJ, Nelson JA, Jarvis MA, Johnson DC. 2010. A human cytomegalovirus gO-null mutant fails to incorporate gH/gL into the virion envelope and is unable to enter fibroblasts and epithelial and endothelial cells. J Virol 84:2585-2596. http://dx.doi.org/10.1128/JVI.02249-09.
78. Compton T, Nepomuceno RR, Nowlin DM. 1992. Human cytomegalovirus penetrates host cells by pH-independent fusion at the cell surface. Virology 191:387-395. http://dx.doi.org/10.1016/0042-6822(92)90200-9.
79. Wille PT, Wisner TW, Ryckman B, Johnson DC. 2013. Human cytomegalovirus (HCMV) glycoprotein gB promotes virus entry in trans acting as the viral fusion protein rather than as a receptor-binding protein. mBio 4(3):e00332-13. http://dx.doi.org/10.1128/mBio.00332-13.
80. Friesen RHE, Koudstaal W, Koldijk MH, Weverling GJ, Brakenhoff JPJ, Lenting PJ, Stittelaar KJ, Osterhaus ADME, Kompier R, Goudsmit J. 2010. New class of monoclonal antibodies against severe influenza: prophylactic and therapeutic efficacy in ferrets. PLoS One 5:e9106. http://dx.doi.org/10.1371/journal.pone.0009106.
81. Kauvar LM, Harcourt JL, Haynes LM, Tripp RA. 2010. Therapeutic targeting of respiratory syncytial virus G-protein. Immunotherapy 2:655-661. http://dx.doi.org/10.2217/imt.10.53.
82. Keck ZY, Angus AG, Wang W, Lau P, Wang Y, Gatherer D, Patel AH, Foung SK. 2014. Non-random escape pathways from a broadly neutralizing human monoclonal antibody map to a highly conserved region on the hepatitis C virus E2 glycoprotein encompassing amino acids 412-423. PLoS Pathog 10:e1004297. http://dx.doi.org/10.1371/journal.ppat.1004297.
83. Vecchiati A, Tellatin S, Angelini A, Iliceto S, Tona F. 2014. Coronary microvasculopathy in heart transplantation: consequences and therapeutic implications. World J Transplant 4:93-101.
84. Pereira L, Petitt M, Fong A, Tsuge M, Tabata T, Fang-Hoover J, Maidji E, Zydek M, Zhou Y, Inoue N, Loghavi S, Pepkowitz S, Kauvar LM, Ogunyemi D. 2014. Intrauterine growth restriction caused by underlying congenital cytomegalovirus infection. J Infect Dis 209:1573-1584. http://dx.doi.org/10.1093/infdis/jiu019.
85. Ishibashi K, Tokumoto T, Shirakawa H, Hashimoto K, Ikuta K, Kushida N, Yanagida T, Shishido K, Aikawa K, Toma H, Inoue N, Yamaguchi O, Tanabe K, Suzutani T. 2011. Lack of antibodies against the antigen domain 2 epitope of cytomegalovirus (CMV) glycoprotein B is associated with CMV disease after renal transplantation in recipients having the same glycoprotein H serotypes as their donors. Transpl Infect Dis 13:318-323. http://dx.doi.org/10.1111/j.1399-3062.2010.00563.x.
86. Hwang WY, Foote J. 2005. Immunogenicity of engineered antibodies. Methods 36:3-10. http://dx.doi.org/10.1016/j.ymeth.2005.01.001.