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Infectious Diseases Research

Research Overview

Michael Farzan’s laboratory focuses on the generation and delivery of antibodies and antibody-like entry inhibitors for the prevention and treatment of infectious diseases, especially those caused by coronaviruses, arenaviruses, and retroviruses. We are especially committed to approaches that could prevent new viral infections and establish a functional cure for HIV-1. To do so, we develop and apply three main technologies. First, we use now well-established mRNA vaccines to deliver antigens informed by a detailed analysis of critical epitopes of the viral entry protein and properties of human immune repertoire.

Second, we use adeno-associated virus (AAV) vectors to express antibodies and antibody-like proteins that can control an established infection. Finally, we have committed to a long-term effort to combining ex vivo and in vivo editing technologies of B cells with novel vaccines and vaccination strategies. Here we modify the B-cell receptor loci of primary B cells, engraft these edited B cells back to their host, and expand these cells with antigenic stimulation. This technology allows us to use murine germinal centers to select potent and highly bioavailable human antibodies. It also provides us useful animal models to evaluate and improve vaccines, as well as a new way to address unanswered questions in B-cell biology. Finally, the chimeric antigen receptor (CAR) B cells so generated can themselves be conceived of as a therapy for many disease states including HIV infection.

Research Background

Dr. Farzan received his undergraduate degree from Harvard College in Government and his Ph.D. in Immunology from Harvard Medical School (HMS), mentored by Dr. Joseph Sodroski. He received his first faculty appointment in the HMS Department of Medicine in 2002 and was promoted to professor in the Department of Microbiology and Immunobiology in 2012. He then spent a decade as co-Chair and then Chair of the Department of Immunology and Microbiology at the Scripps Research Institute on its Florida campus, returning to HMS in 2023 as Professor of Pediatrics and as the Director of Virology Research in the Division of Infectious Diseases at Boston Children’s Hospital.

He has studied for years the HIV-1 entry process and its inhibition, for example identifying the critical role of coreceptor tyrosine-sulfation in the entry process, and discovery of the same modification on HIV-1 neutralizing antibodies. This work led to the development of the broad and potent entry inhibitor eCD4-Ig and to his current effort to the epitopes of sulfated antibodies to drive protective antibody responses to HIV and other viruses. The recent interest in coronaviruses has also highlighted his work on SARS coronavirus (SARS-CoV) including identification of the receptor ACE2, delineation of the S protein receptor-binding site, and characterization of the molecular events necessary for this virus to move from palm civets to humans.
 

Publications

  1. In vivo evolution of env in SHIV-AD8EO-infected rhesus macaques after AAV-vectored delivery of eCD4-Ig. Mol Ther. 2024 Dec 12. View Abstract
  2. In vivo affinity maturation of the CD4 domains of an HIV-1-entry inhibitor. Nat Biomed Eng. 2024 Dec; 8(12):1715-1729. View Abstract
  3. Simultaneous screening for selective SARS-CoV-2, Lassa, and Machupo virus entry inhibitors. SLAS Discov. 2024 Sep; 29(6):100178. View Abstract
  4. In vivo affinity maturation of mouse B cells reprogrammed to express human antibodies. Nat Biomed Eng. 2024 Apr; 8(4):361-379. View Abstract
  5. In vivo affinity maturation of the HIV-1 Env-binding domain of CD4. Res Sq. 2024 Feb 09. View Abstract
  6. Predicting potential SARS-CoV-2 mutations of concern via full quantum mechanical modelling. J R Soc Interface. 2024 02; 21(211):20230614. View Abstract
  7. In vivo affinity maturation of the HIV-1 Env-binding domain of CD4. bioRxiv. 2024 Feb 05. View Abstract
  8. In vivo affinity maturation of murine B cells reprogrammed to express human antibodies. bioRxiv. 2023 Oct 23. View Abstract
  9. Effect of mRNA-LNP components of two globally-marketed COVID-19 vaccines on efficacy and stability. NPJ Vaccines. 2023 Oct 11; 8(1):156. View Abstract
  10. An IgM-like inhalable ACE2 fusion protein broadly neutralizes SARS-CoV-2 variants. Nat Commun. 2023 08 25; 14(1):5191. View Abstract
  11. Heavy-chain CDR3-engineered B cells facilitate in vivo evaluation of HIV-1 vaccine candidates. Immunity. 2023 10 10; 56(10):2408-2424.e6. View Abstract
  12. A strategy for high antibody expression with low anti-drug antibodies using AAV9 vectors. Front Immunol. 2023; 14:1105617. View Abstract
  13. A lentiviral vector B cell gene therapy platform for the delivery of the anti-HIV-1 eCD4-Ig-knob-in-hole-reversed immunoadhesin. Mol Ther Methods Clin Dev. 2023 Mar 09; 28:366-384. View Abstract
  14. Highlights from the Tenth International Workshop on HIV Persistence during Therapy, December 13-16, 2022, Miami, Florida-USA. J Virus Erad. 2023 Mar; 9(1):100315. View Abstract
  15. High throughput screening for drugs that inhibit 3C-like protease in SARS-CoV-2. SLAS Discov. 2023 04; 28(3):95-101. View Abstract
  16. Probing the mutational landscape of the SARS-CoV-2 spike protein via quantum mechanical modeling of crystallographic structures. PNAS Nexus. 2022 Nov; 1(5):pgac180. View Abstract
  17. Estimation of the in vivo neutralization potency of eCD4Ig and conditions for AAV-mediated production for SHIV long-term remission. Sci Adv. 2022 Jan 14; 8(2):eabj5666. View Abstract
  18. Correction: Tickner, Z.J.; Farzan, M. Riboswitches for Controlled Expression of Therapeutic Transgenes Delivered by Adeno-Associated Viral Vectors. Pharmaceuticals 2021, 14, 554. Pharmaceuticals (Basel). 2021 Dec 06; 14(12). View Abstract
  19. Reprogramming of the heavy-chain CDR3 regions of a human antibody repertoire. Mol Ther. 2022 01 05; 30(1):184-197. View Abstract
  20. Identification of potent small molecule inhibitors of SARS-CoV-2 entry. SLAS Discov. 2022 01; 27(1):8-19. View Abstract
  21. Mechanisms of SARS-CoV-2 entry into cells. Nat Rev Mol Cell Biol. 2022 01; 23(1):3-20. View Abstract
  22. Predicting the efficacy of COVID-19 convalescent plasma donor units with the Lumit Dx anti-receptor binding domain assay. PLoS One. 2021; 16(7):e0253551. View Abstract
  23. In vitro affinity maturation of broader and more-potent variants of the HIV-1-neutralizing antibody CAP256-VRC26.25. Proc Natl Acad Sci U S A. 2021 07 20; 118(29). View Abstract
  24. Riboswitches for Controlled Expression of Therapeutic Transgenes Delivered by Adeno-Associated Viral Vectors. Pharmaceuticals (Basel). 2021 Jun 10; 14(6). View Abstract
  25. An Engineered Receptor-Binding Domain Improves the Immunogenicity of Multivalent SARS-CoV-2 Vaccines. mBio. 2021 05 11; 12(3). View Abstract
  26. How SARS-CoV-2 first adapted in humans. Science. 2021 04 30; 372(6541):466-467. View Abstract
  27. Mutations derived from horseshoe bat ACE2 orthologs enhance ACE2-Fc neutralization of SARS-CoV-2. PLoS Pathog. 2021 04; 17(4):e1009501. View Abstract
  28. Author Correction: IFITM3 functions as a PIP3 scaffold to amplify PI3K signalling in B cells. Nature. 2021 Apr; 592(7852):E3. View Abstract
  29. Donor Anti-Spike Immunity is Related to Recipient Recovery and Can Predict the Efficacy of Convalescent Plasma Units. medRxiv. 2021 Mar 01. View Abstract
  30. A more efficient CRISPR-Cas12a variant derived from Lachnospiraceae bacterium MA2020. Mol Ther Nucleic Acids. 2021 Jun 04; 24:40-53. View Abstract
  31. Hydroxychloroquine-mediated inhibition of SARS-CoV-2 entry is attenuated by TMPRSS2. PLoS Pathog. 2021 01; 17(1):e1009212. View Abstract
  32. A trimeric human angiotensin-converting enzyme 2 as an anti-SARS-CoV-2 agent. Nat Struct Mol Biol. 2021 02; 28(2):202-209. View Abstract
  33. SARS-CoV-2 spike-protein D614G mutation increases virion spike density and infectivity. Nat Commun. 2020 11 26; 11(1):6013. View Abstract
  34. An engineered receptor-binding domain improves the immunogenicity of multivalent SARS-CoV-2 vaccines. bioRxiv. 2020 Nov 18. View Abstract
  35. AAV vectors engineered to target insulin receptor greatly enhance intramuscular gene delivery. Mol Ther Methods Clin Dev. 2020 Dec 11; 19:496-506. View Abstract
  36. Functional importance of the D614G mutation in the SARS-CoV-2 spike protein. Biochem Biophys Res Commun. 2021 01 29; 538:108-115. View Abstract
  37. IFITM3 functions as a PIP3 scaffold to amplify PI3K signalling in B cells. Nature. 2020 12; 588(7838):491-497. View Abstract
  38. SARS-CoV-2 and Three Related Coronaviruses Utilize Multiple ACE2 Orthologs and Are Potently Blocked by an Improved ACE2-Ig. J Virol. 2020 10 27; 94(22). View Abstract
  39. High-Throughput Screening for Drugs That Inhibit Papain-Like Protease in SARS-CoV-2. SLAS Discov. 2020 12; 25(10):1152-1161. View Abstract
  40. A trimeric human angiotensin-converting enzyme 2 as an anti-SARS-CoV-2 agent in vitro. bioRxiv. 2020 Sep 18. View Abstract
  41. Selection of High-Affinity RNA Aptamers That Distinguish between Doxycycline and Tetracycline. Biochemistry. 2020 09 22; 59(37):3473-3486. View Abstract
  42. A Single Immunization with Nucleoside-Modified mRNA Vaccines Elicits Strong Cellular and Humoral Immune Responses against SARS-CoV-2 in Mice. Immunity. 2020 10 13; 53(4):724-732.e7. View Abstract
  43. Mutations from bat ACE2 orthologs markedly enhance ACE2-Fc neutralization of SARS-CoV-2. bioRxiv. 2020 Jun 30. View Abstract
  44. The D614G mutation in the SARS-CoV-2 spike protein reduces S1 shedding and increases infectivity. bioRxiv. 2020 Jun 12. View Abstract
  45. A Bispecific Antibody That Simultaneously Recognizes the V2- and V3-Glycan Epitopes of the HIV-1 Envelope Glycoprotein Is Broader and More Potent than Its Parental Antibodies. mBio. 2020 01 14; 11(1). View Abstract
  46. A reversible RNA on-switch that controls gene expression of AAV-delivered therapeutics in vivo. Nat Biotechnol. 2020 02; 38(2):169-175. View Abstract
  47. AAV-delivered eCD4-Ig protects rhesus macaques from high-dose SIVmac239 challenges. Sci Transl Med. 2019 07 24; 11(502). View Abstract
  48. Zika Virus-Immune Plasmas from Symptomatic and Asymptomatic Individuals Enhance Zika Pathogenesis in Adult and Pregnant Mice. mBio. 2019 07 02; 10(4). View Abstract
  49. eCD4-Ig Limits HIV-1 Escape More Effectively than CD4-Ig or a Broadly Neutralizing Antibody. J Virol. 2019 07 15; 93(14). View Abstract
  50. Circumventing cellular immunity by miR142-mediated regulation sufficiently supports rAAV-delivered OVA expression without activating humoral immunity. JCI Insight. 2019 05 21; 5. View Abstract
  51. Associating HIV-1 envelope glycoprotein structures with states on the virus observed by smFRET. Nature. 2019 04; 568(7752):415-419. View Abstract
  52. A Coreceptor-Mimetic Peptide Enhances the Potency of V3-Glycan Antibodies. J Virol. 2019 03 01; 93(5). View Abstract
  53. Anti-drug Antibody Responses Impair Prophylaxis Mediated by AAV-Delivered HIV-1 Broadly Neutralizing Antibodies. Mol Ther. 2019 03 06; 27(3):650-660. View Abstract
  54. HIV-1 inhibitory properties of eCD4-Igmim2 determined using an Env-mediated membrane fusion assay. PLoS One. 2018; 13(10):e0206365. View Abstract
  55. Diverse pathways of escape from all well-characterized VRC01-class broadly neutralizing HIV-1 antibodies. PLoS Pathog. 2018 08; 14(8):e1007238. View Abstract
  56. eCD4-Ig Variants That More Potently Neutralize HIV-1. J Virol. 2018 06 15; 92(12). View Abstract
  57. Conditional Regulation of Gene Expression by Ligand-Induced Occlusion of a MicroRNA Target Sequence. Mol Ther. 2018 05 02; 26(5):1277-1286. View Abstract
  58. eCD4-Ig promotes ADCC activity of sera from HIV-1-infected patients. PLoS Pathog. 2017 12; 13(12):e1006786. View Abstract
  59. Simian Immunodeficiency Virus SIVmac239, but Not SIVmac316, Binds and Utilizes Human CD4 More Efficiently than Rhesus CD4. J Virol. 2017 09 15; 91(18). View Abstract
  60. Cpf1 proteins excise CRISPR RNAs from mRNA transcripts in mammalian cells. Nat Chem Biol. 2017 Aug; 13(8):839-841. View Abstract
  61. Engineering antibody-like inhibitors to prevent and treat HIV-1 infection. Curr Opin HIV AIDS. 2017 May; 12(3):294-301. View Abstract
  62. Rational design of aptazyme riboswitches for efficient control of gene expression in mammalian cells. Elife. 2016 11 02; 5. View Abstract
  63. The Interferon-Stimulated Gene IFITM3 Restricts Infection and Pathogenesis of Arthritogenic and Encephalitic Alphaviruses. J Virol. 2016 10 01; 90(19):8780-94. View Abstract
  64. The Interferon-Stimulated Gene Ifitm3 Restricts West Nile Virus Infection and Pathogenesis. J Virol. 2016 09 15; 90(18):8212-25. View Abstract
  65. CD4-Induced Antibodies Promote Association of the HIV-1 Envelope Glycoprotein with CD4-Binding Site Antibodies. J Virol. 2016 09 01; 90(17):7822-32. View Abstract
  66. Envelope residue 375 substitutions in simian-human immunodeficiency viruses enhance CD4 binding and replication in rhesus macaques. Proc Natl Acad Sci U S A. 2016 06 14; 113(24):E3413-22. View Abstract
  67. Virion-associated phosphatidylethanolamine promotes TIM1-mediated infection by Ebola, dengue, and West Nile viruses. Proc Natl Acad Sci U S A. 2015 Nov 24; 112(47):14682-7. View Abstract
  68. Mechanism for Selective Synaptic Wiring of Rod Photoreceptors into the Retinal Circuitry and Its Role in Vision. Neuron. 2015 Sep 23; 87(6):1248-1260. View Abstract
  69. The Triggering Receptor Expressed on Myeloid Cells 2 Binds Apolipoprotein E. J Biol Chem. 2015 Oct 23; 290(43):26033-42. View Abstract
  70. Envelope Glycoprotein Internalization Protects Human and Simian Immunodeficiency Virus-Infected Cells from Antibody-Dependent Cell-Mediated Cytotoxicity. J Virol. 2015 Oct; 89(20):10648-55. View Abstract
  71. Neutralization properties of simian immunodeficiency viruses infecting chimpanzees and gorillas. mBio. 2015 Apr 21; 6(2). View Abstract
  72. AAV-expressed eCD4-Ig provides durable protection from multiple SHIV challenges. Nature. 2015 Mar 05; 519(7541):87-91. View Abstract
  73. IFITM-Family Proteins: The Cell's First Line of Antiviral Defense. Annu Rev Virol. 2014 Nov 01; 1:261-283. View Abstract
  74. IFITM3 polymorphism rs12252-C restricts influenza A viruses. PLoS One. 2014; 9(10):e110096. View Abstract
  75. The antiviral restriction factors IFITM1, 2 and 3 do not inhibit infection of human papillomavirus, cytomegalovirus and adenovirus. PLoS One. 2014; 9(5):e96579. View Abstract
  76. UVRAG is required for virus entry through combinatorial interaction with the class C-Vps complex and SNAREs. Proc Natl Acad Sci U S A. 2014 Feb 18; 111(7):2716-21. View Abstract
  77. A double-mimetic peptide efficiently neutralizes HIV-1 by bridging the CD4- and coreceptor-binding sites of gp120. J Virol. 2014 Mar; 88(6):3353-8. View Abstract
  78. Interferon-induced transmembrane protein 3 is a type II transmembrane protein. J Biol Chem. 2013 Nov 08; 288(45):32184-32193. View Abstract
  79. IFITM-2 and IFITM-3 but not IFITM-1 restrict Rift Valley fever virus. J Virol. 2013 Aug; 87(15):8451-64. View Abstract
  80. Dual host-virus arms races shape an essential housekeeping protein. PLoS Biol. 2013; 11(5):e1001571. View Abstract
  81. Direct expression and validation of phage-selected peptide variants in mammalian cells. J Biol Chem. 2013 Jun 28; 288(26):18803-10. View Abstract
  82. The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry. Cell Host Microbe. 2013 Apr 17; 13(4):452-64. View Abstract
  83. Lectin-dependent enhancement of Ebola virus infection via soluble and transmembrane C-type lectin receptors. PLoS One. 2013; 8(4):e60838. View Abstract
  84. TIM-family proteins promote infection of multiple enveloped viruses through virion-associated phosphatidylserine. PLoS Pathog. 2013 Mar; 9(3):e1003232. View Abstract
  85. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat Rev Immunol. 2013 Jan; 13(1):46-57. View Abstract
  86. Ifitm3 limits the severity of acute influenza in mice. PLoS Pathog. 2012 Sep; 8(9):e1002909. View Abstract
  87. Enhanced recognition and neutralization of HIV-1 by antibody-derived CCR5-mimetic peptide variants. J Virol. 2012 Nov; 86(22):12417-21. View Abstract
  88. IFITM proteins restrict antibody-dependent enhancement of dengue virus infection. PLoS One. 2012; 7(3):e34508. View Abstract
  89. Evidence for ACE2-utilizing coronaviruses (CoVs) related to severe acute respiratory syndrome CoV in bats. J Virol. 2012 Jun; 86(11):6350-3. View Abstract
  90. An antibody recognizing the apical domain of human transferrin receptor 1 efficiently inhibits the entry of all new world hemorrhagic Fever arenaviruses. J Virol. 2012 Apr; 86(7):4024-8. View Abstract
  91. Association of membrane rafts and postsynaptic density: proteomics, biochemical, and ultrastructural analyses. J Neurochem. 2011 Oct; 119(1):64-77. View Abstract
  92. Transferrin receptor 1 in the zoonosis and pathogenesis of New World hemorrhagic fever arenaviruses. Curr Opin Microbiol. 2011 Aug; 14(4):476-82. View Abstract
  93. Ebolavirus delta-peptide immunoadhesins inhibit marburgvirus and ebolavirus cell entry. J Virol. 2011 Sep; 85(17):8502-13. View Abstract
  94. A tyrosine-sulfated CCR5-mimetic peptide promotes conformational transitions in the HIV-1 envelope glycoprotein. J Virol. 2011 Aug; 85(15):7563-71. View Abstract
  95. Identification of a small-molecule entry inhibitor for filoviruses. J Virol. 2011 Apr; 85(7):3106-19. View Abstract
  96. Distinct patterns of IFITM-mediated restriction of filoviruses, SARS coronavirus, and influenza A virus. PLoS Pathog. 2011 Jan 06; 7(1):e1001258. View Abstract
  97. Structural basis for receptor recognition by New World hemorrhagic fever arenaviruses. Nat Struct Mol Biol. 2010 Apr; 17(4):438-44. View Abstract
  98. Sulfotyrosines of the Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor promote tumorigenesis through autocrine activation. J Virol. 2010 Apr; 84(7):3351-61. View Abstract
  99. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell. 2009 Dec 24; 139(7):1243-54. View Abstract
  100. Identification of a new region of SARS-CoV S protein critical for viral entry. J Mol Biol. 2009 Dec 11; 394(4):600-5. View Abstract
  101. Mutagenesis and evolution of sulfated antibodies using an expanded genetic code. Biochemistry. 2009 Sep 22; 48(37):8891-8. View Abstract
  102. A New World primate deficient in tetherin-mediated restriction of human immunodeficiency virus type 1. J Virol. 2009 Sep; 83(17):8771-80. View Abstract
  103. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe. 2009 May 08; 5(5):439-49. View Abstract
  104. Host-species transferrin receptor 1 orthologs are cellular receptors for nonpathogenic new world clade B arenaviruses. PLoS Pathog. 2009 Apr; 5(4):e1000358. View Abstract
  105. Chapter 7. Tyrosine sulfation of HIV-1 coreceptors and other chemokine receptors. Methods Enzymol. 2009; 461:147-70. View Abstract
  106. Protein evolution with an expanded genetic code. Proc Natl Acad Sci U S A. 2008 Nov 18; 105(46):17688-93. View Abstract
  107. Influenza A virus neuraminidase limits viral superinfection. J Virol. 2008 May; 82(10):4834-43. View Abstract
  108. Evolution of a TRIM5-CypA splice isoform in old world monkeys. PLoS Pathog. 2008 Feb 29; 4(2):e1000003. View Abstract
  109. Receptor determinants of zoonotic transmission of New World hemorrhagic fever arenaviruses. Proc Natl Acad Sci U S A. 2008 Feb 19; 105(7):2664-9. View Abstract
  110. The S proteins of human coronavirus NL63 and severe acute respiratory syndrome coronavirus bind overlapping regions of ACE2. Virology. 2007 Oct 25; 367(2):367-74. View Abstract
  111. Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature. 2007 Mar 01; 446(7131):92-6. View Abstract
  112. Changes in the V3 region of gp120 contribute to unusually broad coreceptor usage of an HIV-1 isolate from a CCR5 Delta32 heterozygote. Virology. 2007 May 25; 362(1):163-78. View Abstract
  113. Severe acute respiratory syndrome coronavirus entry as a target of antiviral therapies. Antivir Ther. 2007; 12(4 Pt B):639-50. View Abstract
  114. Generation and characterization of human monoclonal neutralizing antibodies with distinct binding and sequence features against SARS coronavirus using XenoMouse. Virology. 2007 Apr 25; 361(1):93-102. View Abstract
  115. Palmitoylation of the cysteine-rich endodomain of the SARS-coronavirus spike glycoprotein is important for spike-mediated cell fusion. Virology. 2007 Apr 10; 360(2):264-74. View Abstract
  116. Tyrosine sulfate trapped by amber. Nat Biotechnol. 2006 Nov; 24(11):1361-2. View Abstract
  117. Structural basis of neutralization by a human anti-severe acute respiratory syndrome spike protein antibody, 80R. J Biol Chem. 2006 Nov 10; 281(45):34610-6. View Abstract
  118. A tyrosine-sulfated peptide derived from the heavy-chain CDR3 region of an HIV-1-neutralizing antibody binds gp120 and inhibits HIV-1 infection. J Biol Chem. 2006 Sep 29; 281(39):28529-35. View Abstract
  119. Conformational states of the severe acute respiratory syndrome coronavirus spike protein ectodomain. J Virol. 2006 Jul; 80(14):6794-800. View Abstract
  120. Cross-neutralization of human and palm civet severe acute respiratory syndrome coronaviruses by antibodies targeting the receptor-binding domain of spike protein. J Immunol. 2006 May 15; 176(10):6085-92. View Abstract
  121. Animal origins of the severe acute respiratory syndrome coronavirus: insight from ACE2-S-protein interactions. J Virol. 2006 May; 80(9):4211-9. View Abstract
  122. Conserved receptor-binding domains of Lake Victoria marburgvirus and Zaire ebolavirus bind a common receptor. J Biol Chem. 2006 Jun 09; 281(23):15951-8. View Abstract
  123. Insights from the association of SARS-CoV S-protein with its receptor, ACE2. Adv Exp Med Biol. 2006; 581:209-18. View Abstract
  124. Interactions between SARS coronavirus and its receptor. Adv Exp Med Biol. 2006; 581:229-34. View Abstract
  125. SARS-CoV, but not HCoV-NL63, utilizes cathepsins to infect cells: viral entry. Adv Exp Med Biol. 2006; 581:335-8. View Abstract
  126. Infection of human airway epithelia by SARS coronavirus is associated with ACE2 expression and localization. Adv Exp Med Biol. 2006; 581:479-84. View Abstract
  127. Antibody responses against SARS coronavirus are correlated with disease outcome of infected individuals. J Med Virol. 2006 Jan; 78(1):1-8. View Abstract
  128. SARS coronavirus, but not human coronavirus NL63, utilizes cathepsin L to infect ACE2-expressing cells. J Biol Chem. 2006 Feb 10; 281(6):3198-203. View Abstract
  129. ACE2 receptor expression and severe acute respiratory syndrome coronavirus infection depend on differentiation of human airway epithelia. J Virol. 2005 Dec; 79(23):14614-21. View Abstract
  130. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science. 2005 Sep 16; 309(5742):1864-8. View Abstract
  131. A highly conserved arginine in gp120 governs HIV-1 binding to both syndecans and CCR5 via sulfated motifs. J Biol Chem. 2005 Nov 25; 280(47):39493-504. View Abstract
  132. Genetic analysis of the SARS-coronavirus spike glycoprotein functional domains involved in cell-surface expression and cell-to-cell fusion. Virology. 2005 Oct 25; 341(2):215-30. View Abstract
  133. An alternative conformation of the gp41 heptad repeat 1 region coiled coil exists in the human immunodeficiency virus (HIV-1) envelope glycoprotein precursor. Virology. 2005 Jul 20; 338(1):133-43. View Abstract
  134. JLK inhibitors: isocoumarin compounds as putative probes to selectively target the gamma-secretase pathway. Curr Alzheimer Res. 2005 Jul; 2(3):327-34. View Abstract
  135. Evaluation of human monoclonal antibody 80R for immunoprophylaxis of severe acute respiratory syndrome by an animal study, epitope mapping, and analysis of spike variants. J Virol. 2005 May; 79(10):5900-6. View Abstract
  136. Functional mimicry of a human immunodeficiency virus type 1 coreceptor by a neutralizing monoclonal antibody. J Virol. 2005 May; 79(10):6068-77. View Abstract
  137. Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J. 2005 Apr 20; 24(8):1634-43. View Abstract
  138. Recombinant modified vaccinia virus Ankara expressing the spike glycoprotein of severe acute respiratory syndrome coronavirus induces protective neutralizing antibodies primarily targeting the receptor binding region. J Virol. 2005 Mar; 79(5):2678-88. View Abstract
  139. Sulphated tyrosines mediate association of chemokines and Plasmodium vivax Duffy binding protein with the Duffy antigen/receptor for chemokines (DARC). Mol Microbiol. 2005 Mar; 55(5):1413-22. View Abstract
  140. Mapping binding residues in the Plasmodium vivax domain that binds Duffy antigen during red cell invasion. Mol Microbiol. 2005 Mar; 55(5):1423-34. View Abstract
  141. Receptor-binding domain of SARS-CoV spike protein induces highly potent neutralizing antibodies: implication for developing subunit vaccine. Biochem Biophys Res Commun. 2004 Nov 12; 324(2):773-81. View Abstract
  142. Angiotensin-converting enzyme 2: a functional receptor for SARS coronavirus. Cell Mol Life Sci. 2004 Nov; 61(21):2738-43. View Abstract
  143. Retroviruses pseudotyped with the severe acute respiratory syndrome coronavirus spike protein efficiently infect cells expressing angiotensin-converting enzyme 2. J Virol. 2004 Oct; 78(19):10628-35. View Abstract
  144. Efficient replication of severe acute respiratory syndrome coronavirus in mouse cells is limited by murine angiotensin-converting enzyme 2. J Virol. 2004 Oct; 78(20):11429-33. View Abstract
  145. N-linked glycosylation in the CXCR4 N-terminus inhibits binding to HIV-1 envelope glycoproteins. Virology. 2004 Jun 20; 324(1):140-50. View Abstract
  146. CD4-induced T-20 binding to human immunodeficiency virus type 1 gp120 blocks interaction with the CXCR4 coreceptor. J Virol. 2004 May; 78(10):5448-57. View Abstract
  147. Potent neutralization of severe acute respiratory syndrome (SARS) coronavirus by a human mAb to S1 protein that blocks receptor association. Proc Natl Acad Sci U S A. 2004 Feb 24; 101(8):2536-41. View Abstract
  148. Structural basis of tyrosine sulfation and VH-gene usage in antibodies that recognize the HIV type 1 coreceptor-binding site on gp120. Proc Natl Acad Sci U S A. 2004 Mar 02; 101(9):2706-11. View Abstract
  149. A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2. J Biol Chem. 2004 Jan 30; 279(5):3197-201. View Abstract
  150. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature. 2003 Nov 27; 426(6965):450-4. View Abstract
  151. JLK isocoumarin inhibitors: selective gamma-secretase inhibitors that do not interfere with notch pathway in vitro or in vivo. J Neurosci Res. 2003 Nov 01; 74(3):370-7. View Abstract
  152. Tyrosine sulfation of human antibodies contributes to recognition of the CCR5 binding region of HIV-1 gp120. Cell. 2003 Jul 25; 114(2):161-70. View Abstract
  153. Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor. J Biol Chem. 2003 Jan 31; 278(5):3378-85. View Abstract
  154. Tyrosine-sulfated peptides functionally reconstitute a CCR5 variant lacking a critical amino-terminal region. J Biol Chem. 2002 Oct 25; 277(43):40397-402. View Abstract
  155. Stimulation of enveloped virus infection by beta-amyloid fibrils. J Biol Chem. 2002 Sep 20; 277(38):35019-24. View Abstract
  156. Increased CCR5 affinity and reduced CCR5/CD4 dependence of a neurovirulent primary human immunodeficiency virus type 1 isolate. J Virol. 2002 Jun; 76(12):6277-92. View Abstract
  157. The role of post-translational modifications of the CXCR4 amino terminus in stromal-derived factor 1 alpha association and HIV-1 entry. J Biol Chem. 2002 Aug 16; 277(33):29484-9. View Abstract
  158. Sialylated O-glycans and sulfated tyrosines in the NH2-terminal domain of CC chemokine receptor 5 contribute to high affinity binding of chemokines. J Exp Med. 2001 Dec 03; 194(11):1661-73. View Abstract
  159. Human Mast cell progenitors can be infected by macrophagetropic human immunodeficiency virus type 1 and retain virus with maturation in vitro. J Virol. 2001 Nov; 75(22):10808-14. View Abstract
  160. Sulfated tyrosines contribute to the formation of the C5a docking site of the human C5a anaphylatoxin receptor. J Exp Med. 2001 May 07; 193(9):1059-66. View Abstract
  161. Apelin, the natural ligand of the orphan seven-transmembrane receptor APJ, inhibits human immunodeficiency virus type 1 entry. J Virol. 2000 Dec; 74(24):11972-6. View Abstract
  162. A tyrosine-sulfated peptide based on the N terminus of CCR5 interacts with a CD4-enhanced epitope of the HIV-1 gp120 envelope glycoprotein and inhibits HIV-1 entry. J Biol Chem. 2000 Oct 27; 275(43):33516-21. View Abstract
  163. BACE2, a beta -secretase homolog, cleaves at the beta site and within the amyloid-beta region of the amyloid-beta precursor protein. Proc Natl Acad Sci U S A. 2000 Aug 15; 97(17):9712-7. View Abstract
  164. Characterization of stable, soluble trimers containing complete ectodomains of human immunodeficiency virus type 1 envelope glycoproteins. J Virol. 2000 Jun; 74(12):5716-25. View Abstract
  165. Paramagnetic proteoliposomes containing a pure, native, and oriented seven-transmembrane segment protein, CCR5. Nat Biotechnol. 2000 Jun; 18(6):649-54. View Abstract
  166. Modifications that stabilize human immunodeficiency virus envelope glycoprotein trimers in solution. J Virol. 2000 May; 74(10):4746-54. View Abstract
  167. Adaptation of a CCR5-using, primary human immunodeficiency virus type 1 isolate for CD4-independent replication. J Virol. 1999 Oct; 73(10):8120-6. View Abstract
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  169. Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell. 1999 Mar 05; 96(5):667-76. View Abstract
  170. Expansion by self antigen is necessary for the induction of experimental autoimmune encephalomyelitis by T cells primed with a cross-reactive environmental antigen. J Immunol. 1998 Oct 01; 161(7):3307-14. View Abstract
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  172. The orphan seven-transmembrane receptor apj supports the entry of primary T-cell-line-tropic and dualtropic human immunodeficiency virus type 1. J Virol. 1998 Jul; 72(7):6113-8. View Abstract
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  174. The bis-azo compound FP-21399 inhibits HIV-1 replication by preventing viral entry. Virology. 1998 May 10; 244(2):530-41. View Abstract
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  176. Use of murine CXCR-4 as a second receptor by some T-cell-tropic human immunodeficiency viruses. J Virol. 1998 Feb; 72(2):1652-6. View Abstract
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  178. Two orphan seven-transmembrane segment receptors which are expressed in CD4-positive cells support simian immunodeficiency virus infection. J Exp Med. 1997 Aug 04; 186(3):405-11. View Abstract
  179. Structure-based mutagenesis of the catalytic domain of human immunodeficiency virus type 1 integrase. J Virol. 1997 May; 71(5):3507-14. View Abstract
  180. HIV-1 entry and macrophage inflammatory protein-1beta-mediated signaling are independent functions of the chemokine receptor CCR5. J Biol Chem. 1997 Mar 14; 272(11):6854-7. View Abstract
  181. Utilization of C-C chemokine receptor 5 by the envelope glycoproteins of a pathogenic simian immunodeficiency virus, SIVmac239. J Virol. 1997 Mar; 71(3):2522-7. View Abstract
  182. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature. 1997 Feb 13; 385(6617):645-9. View Abstract
  183. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature. 1996 Aug 29; 382(6594):829-33. View Abstract
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