Early type i Interferon response induces upregulation of human β-defensin 1 during acute HIV-1 infection

PLoS ONE

Volumn 12, Issue 3, 2017, Pages

  Corleis, Björn ^a   Lisanti, Antonella C ^a   Körner, Christian ^a,b   Schiff, Abigail E ^a   Rosenberg, Eric S ^a   Allen, Todd M ^a   Altfeld, Marcus ^a,b   Kwon, Douglas S ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA DEFENSIN 1; RNA; BETA DEFENSIN; DEFB1 PROTEIN, HUMAN; INTERFERON;

ARTICLE; CELL ACTIVATION; CLINICAL ARTICLE; COLON TISSUE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN TISSUE; IN VITRO STUDY; INNATE IMMUNITY; MONOCYTE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; RNA EXTRACTION; UPREGULATION; VIRUS TRANSMISSION; BIOSYNTHESIS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM;

BETA-DEFENSINS; HIV INFECTIONS; HIV-1; HUMANS; INTERFERON TYPE I; MONOCYTES; UP-REGULATION;

EID: 85014348100     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0173161     Document Type: Article

References (72)

1. Hazlett L, Wu M. Defensins in innate immunity. Cell Tissue Res. 2011; 343(1):175-88. Epub 2010/08/DOI: 10.1007/s00441-010-1022-4 PMID: 20730446
2. Wiesner J, Vilcinskas A. Antimicrobial peptides: the ancient arm of the human immune system. Virulence. 2010; 1(5):440-64. Epub 2010/12/24. DOI: 10.4161/viru.1.5.12983 PMID: 21178486
3. Cederlund A, Gudmundsson GH, Agerberth B. Antimicrobial peptides important in innate immunity. Febs J. 2011; 278(20):3942-51. Epub 2011/08/19. DOI: 10.1111/j.1742-4658.2011.08302.x PMID: 21848912
4. Yang D, Biragyn A, Hoover DM, Lubkowski J, Oppenheim JJ. Multiple roles of antimicrobial defensins, cathelicidins, and eosinophil-derived neurotoxin in host defense. Annu Rev Immunol. 2004; 22:181-215. Epub 2004/03/23. DOI: 10.1146/annurev.immunol.22.012703.104603 PMID: 15032578
5. Ganz T. The role of antimicrobial peptides in innate immunity. Integr Comp Biol. 2003; 43(2):300-4. Epub 2003/04/01. DOI: 10.1093/icb/43.2.300 PMID: 21680437
6. Klotman ME, Chang TL. Defensins in innate antiviral immunity. Nature reviews Immunology. 2006; 6 (6):447-56. Epub 2006/05/26. DOI: 10.1038/nri1860 PMID: 16724099
7. Sherman H, Froy O. Expression of human beta-defensin 1 is regulated via c-Myc and the biological clock. Mol Immunol. 2008; 45(11):3163-7. Epub 2008/04/25. DOI: 10.1016/j.molimm.2008.03.004 PMID: 18433872
8. Zilbauer M, Jenke A, Wenzel G, Postberg J, Heusch A, Phillips AD, et al. Expression of human betadefensins in children with chronic inflammatory bowel disease. PLoS One. 2010; 5(10):e15389. Epub 2010/11/03. DOI: 10.1371/journal.pone.0015389 PMID: 21042595
9. Vora P, Youdim A, Thomas LS, Fukata M, Tesfay SY, Lukasek K, et al. Beta-defensin-2 expression is regulated by TLR signaling in intestinal epithelial cells. J Immunol. 2004; 173(9):5398-405. Epub 2004/10/21. PMID: 15494486
10. Meisch JP, Nishimura M, Vogel RM, Sung HC, Bednarchik BA, Ghosh SK, et al. Human beta-defensin 3 peptide is increased and redistributed in Crohn's ileitis. Inflamm Bowel Dis. 2013; 19(5):942-53. Epub 2013/03/21. DOI: 10.1097/MIB.0b013e318280b11a PMID: 23511030
11. Sun L, Finnegan CM, Kish-Catalone T, Blumenthal R, Garzino-Demo P, La Terra Maggiore GM, et al. Human beta-defensins suppress human immunodeficiency virus infection: potential role in mucosal protection. J Virol. 2005; 79(22):14318-29. Epub 2005/10/29. DOI: 10.1128/JVI.79.22.14318-14329.2005 PMID: 16254366
12. Quinones-Mateu ME, Lederman MM, Feng Z, Chakraborty B, Weber J, Rangel HR, et al. Human epithelial beta-defensins 2 and 3 inhibit HIV-1 replication. Aids. 2003; 17(16):F39-48. Epub 2003/10/23. DOI: 10.1097/01.aids.0000096878.73209.4f PMID: 14571200
13. Feng Z, Dubyak GR, Lederman MM, Weinberg A. Cutting edge: human beta defensin 3-a novel antagonist of the HIV-1 coreceptor CXCR4. J Immunol. 2006; 177(2):782-6. Epub 2006/07/05. PMID: 16818731
14. Feng Z, Dubyak GR, Jia X, Lubkowski JT, Weinberg A. Human beta-defensin-3 structure motifs that are important in CXCR4 antagonism. Febs J. 2013; 280(14):3365-75. Epub 2013/05/11. DOI: 10.1111/febs.12328 PMID: 23659571
15. Wilson SS, Wiens ME, Smith JG. Antiviral mechanisms of human defensins. Journal of molecular biology. 2013; 425(24):4965-80. Epub 2013/10/08. DOI: 10.1016/j.jmb.2013.09.038 PMID: 24095897
16. Seidel A, Ye Y, de Armas LR, Soto M, Yarosh W, Marcsisin RA, et al. Cyclic and acyclic defensins inhibit human immunodeficiency virus type-1 replication by different mechanisms. PLoS One. 2010; 5 (3):e9737. Epub 2010/03/23. DOI: 10.1371/journal.pone.0009737 PMID: 20305815
17. Lafferty MK, Sun L, DeMasi L, Lu W, Garzino-Demo A. CCR6 ligands inhibit HIV by inducing APOBEC3G. Blood. 2010; 115(8):1564-71. Epub 2009/12/22. DOI: 10.1182/blood-2009-06-226423 PMID: 20023216
18. Gallo RL, Hooper LV. Epithelial antimicrobial defence of the skin and intestine. Nat Rev Immunol. 2012; 12(7):503-16. Epub 2012/06/26. DOI: 10.1038/nri3228 PMID: 22728527
19. Mukherjee S, Hooper LV. Antimicrobial defense of the intestine. Immunity. 2015; 42(1):28-39. Epub 2015/01/22. DOI: 10.1016/j.immuni.2014.12.028 PMID: 25607457
20. Caballero S, Pamer EG. Microbiota-mediated inflammation and antimicrobial defense in the intestine. Annu Rev Immunol. 2015; 33:227-56. Epub 2015/01/13. DOI: 10.1146/annurev-immunol-032713-120238 PMID: 25581310
21. Gordon SN, Cervasi B, Odorizzi P, Silverman R, Aberra F, Ginsberg G, et al. Disruption of intestinal CD4+ T cell homeostasis is a key marker of systemic CD4+ T cell activation in HIV-infected individuals. J Immunol. 2010; 185(9):5169-79. Epub 2010/10/05. DOI: 10.4049/jimmunol.1001801 PMID: 20889546
22. Marchetti G, Bellistri GM, Borghi E, Tincati C, Ferramosca S, La Francesca M, et al. Microbial translocation is associated with sustained failure in CD4+ T-cell reconstitution in HIV-infected patients on longterm highly active antiretroviral therapy. Aids. 2008; 22(15):2035-8. Epub 2008/09/12. DOI: 10.1097/QAD.0b013e3283112d29 PMID: 18784466
23. Brenchley JM, Douek DC. The mucosal barrier and immune activation in HIV pathogenesis. Curr Opin HIV AIDS. 2008; 3(3):356-61. Epub 2009/04/18. DOI: 10.1097/COH.0b013e3282f9ae9c PMID: 19372990
24. Duits LA, Ravensbergen B, Rademaker M, Hiemstra PS, Nibbering PH. Expression of beta-defensin 1 and 2 mRNA by human monocytes, macrophages and dendritic cells. Immunology. 2002; 106(4):517-25. Epub 2002/08/03. DOI: 10.1046/j.1365-2567.2002.01430.x PMID: 12153515
25. Lehner T, Wang Y, Whittall T, Seidl T. Innate immunity and HIV-1 infection. Adv Dent Res. 2011; 23 (1):19-22. Epub 2011/03/29. DOI: 10.1177/0022034511399081 PMID: 21441475
26. McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF. The immune response during acute HIV-1 infection: clues for vaccine development. Nat Rev Immunol. 2010; 10(1):11-23. Epub 2009/12/17. DOI: 10.1038/nri2674 PMID: 20010788
27. Weinberg A, Quinones-Mateu ME, Lederman MM. Role of human beta-defensins in HIV infection. Adv Dent Res. 2006; 19(1):42-8. Epub 2006/05/05. DOI: 10.1177/154407370601900109 PMID: 16672548
28. Gao D, Wu J, Wu YT, Du F, Aroh C, Yan N, et al. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science. 2013; 341(6148):903-6. Epub 2013/08/10.DOI: 10.1126/science.1240933 PMID: 23929945
29. Biragyn A, Ruffini PA, Leifer CA, Klyushnenkova E, Shakhov A, Chertov O, et al. Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science. 2002; 298(5595):1025-9. Epub 2002/11/02. DOI: 10.1126/science.1075565 PMID: 12411706
30. Campbell JH, Hearps AC, Martin GE, Williams KC, Crowe SM. The importance of monocytes and macrophages in HIV pathogenesis, treatment, and cure. Aids. 2014. Epub 2014/08/22.
31. Iwasaki A. A virological view of innate immune recognition. Annu Rev Microbiol. 2012; 66:177-96. Epub 2012/09/22. DOI: 10.1146/annurev-micro-092611-150203 PMID: 22994491
32. Wang Y, Wang X, Li J, Zhou Y, Ho W. RIG-I activation inhibits HIV replication in macrophages. J Leukoc Biol. 2013; 94(2):337-41. Epub 2013/06/08. DOI: 10.1189/jlb.0313158 PMID: 23744645
33. Berg RK, Melchjorsen J, Rintahaka J, Diget E, Soby S, Horan KA, et al. Genomic HIV RNA induces innate immune responses through RIG-I-dependent sensing of secondary-structured RNA. PLoS One. 2012; 7(1):e29291. Epub 2012/01/12. DOI: 10.1371/journal.pone.0029291 PMID: 22235281
34. Goubau D, Deddouche S, Reis e Sousa C. Cytosolic sensing of viruses. Immunity. 2013; 38(5):855-69. Epub 2013/05/28. DOI: 10.1016/j.immuni.2013.05.007 PMID: 23706667
35. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature. 2001; 413(6857):732-8. Epub 2001/10/19. DOI: 10.1038/35099560 PMID: 11607032
36. Sanchez David RY, Combredet C, Sismeiro O, Dillies MA, Jagla B, Coppee JY, et al. Comparative analysis of viral RNA signatures on different RIG-I-like receptors. Elife. 2016; 5:e11275. Epub 2016/03/25. DOI: 10.7554/eLife.11275 PMID: 27011352
37. Fiebig EW, Wright DJ, Rawal BD, Garrett PE, Schumacher RT, Peddada L, et al. Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. Aids. 2003; 17(13):1871-9. Epub 2003/09/10.DOI: 10.1097/01.aids.0000076308.76477. b8 PMID: 12960819
38. Murooka TT, Deruaz M, Marangoni F, Vrbanac VD, Seung E, von Andrian UH, et al. HIV-infected T cells are migratory vehicles for viral dissemination. Nature. 2012; 490(7419):283-7. Epub 2012/08/03. DOI: 10.1038/nature11398 PMID: 22854780
39. Kwon DS, Gregorio G, Bitton N, Hendrickson WA, Littman DR. DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity. 2002; 16(1):135-44. Epub 2002/02/PMID: 11825572
40. Cavrois M, De Noronha C, Greene WC. A sensitive and specific enzyme-based assay detecting HIV-1 virion fusion in primary T lymphocytes. Nat Biotechnol. 2002; 20(11):1151-4. Epub 2002/10/02. DOI: 10.1038/nbt745 PMID: 12355096
41. Annicotte JS, Chavey C, Servant N, Teyssier J, Bardin A, Licznar A, et al. The nuclear receptor liver receptor homolog-1 is an estrogen receptor target gene. Oncogene. 2005; 24(55):8167-75. Epub 2005/08/11. DOI: 10.1038/sj.onc.1208950 PMID: 16091743
42. Drewes JL, Szeto GL, Engle EL, Liao Z, Shearer GM, Zink MC, et al. Attenuation of pathogenic immune responses during infection with human and simian immunodeficiency virus (HIV/SIV) by the tetracycline derivative minocycline. PLoS One. 2014; 9(4):e94375. Epub 2014/04/16. DOI: 10.1371/journal.pone. 0094375 PMID: 24732038
43. Reinwald S, Wiethe C, Westendorf AM, Breloer M, Probst-Kepper M, Fleischer B, et al. CD83 expression in CD4+ T cells modulates inflammation and autoimmunity. J Immunol. 2008; 180(9):5890-7. Epub 2008/04/22. PMID: 18424708
44. de Jonge HJ, Fehrmann RS, de Bont ES, Hofstra RM, Gerbens F, Kamps WA, et al. Evidence based selection of housekeeping genes. PLoS One. 2007; 2(9):e898. Epub 2007/09/20. DOI: 10.1371/journal. pone.0000898 PMID: 17878933
45. Tomescu C, Chehimi J, Maino VC, Montaner LJ. NK cell lysis of HIV-1-infected autologous CD4 primary T cells: requirement for IFN-mediated NK activation by plasmacytoid dendritic cells. J Immunol. 2007; 179(4):2097-104. Epub 2007/08/07. PMID: 17675468
46. Zahoor MA, Xue G, Sato H, Murakami T, Takeshima SN, Aida Y. HIV-1 Vpr induces interferon-stimulated genes in human monocyte-derived macrophages. PLoS One. 2014; 9(8):e106418. Epub 2014/08/DOI: 10.1371/journal.pone.0106418 PMID: 25170834
47. Alp S, Skrygan M, Schlottmann R, Kreuter A, Otte JM, Schmidt WE, et al. Expression of beta-defensin 1 and 2 in nasal epithelial cells and alveolar macrophages from HIV-infected patients. Eur J Med Res. 2005; 10(1):1-6. Epub 2005/03/02. PMID: 15737946
48. Fang XM, Shu Q, Chen QX, Book M, Sahl HG, Hoeft A, et al. Differential expression of alpha-and betadefensins in human peripheral blood. Eur J Clin Invest. 2003; 33(1):82-7. Epub 2002/12/21. PMID: 12492457
49. Nakatsuji T, Gallo RL. Antimicrobial peptides: old molecules with new ideas. J Invest Dermatol. 2012; 132(3 Pt 2):887-95. Epub 2011/12/14. DOI: 10.1038/jid.2011.387 PMID: 22158560
50. Nakashima H, Yamamoto N, Masuda M, Fujii N. Defensins inhibit HIV replication in vitro. Aids. 1993; 7 (8):1129. Epub 1993/08/01. PMID: 8397954
51. Jarczak J, Kosciuczuk EM, Lisowski P, Strzalkowska N, Jozwik A, Horbanczuk J, et al. Defensins: natural component of human innate immunity. Hum Immunol. 2013; 74(9):1069-79. Epub 2013/06/13. DOI: 10.1016/j.humimm.2013.05.008 PMID: 23756165
52. Neil S, Bieniasz P. Human immunodeficiency virus, restriction factors, and interferon. J Interferon Cytokine Res. 2009; 29(9):569-80. Epub 2009/08/22. DOI: 10.1089/jir.2009.0077 PMID: 19694548
53. Stacey AR, Norris PJ, Qin L, Haygreen EA, Taylor E, Heitman J, et al. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J Virol. 2009; 83(8):3719-33. Epub 2009/01/30. DOI: 10.1128/JVI.01844-08 PMID: 19176632
54. Roberts L, Passmore JA, Williamson C, Little F, Bebell LM, Mlisana K, et al. Plasma cytokine levels during acute HIV-1 infection predict HIV disease progression. Aids. 2010; 24(6):819-31. Epub 2010/03/13. DOI: 10.1097/QAD.0b013e3283367836 PMID: 20224308
55. Bosinger SE, Li Q, Gordon SN, Klatt NR, Duan L, Xu L, et al. Global genomic analysis reveals rapid control of a robust innate response in SIV-infected sooty mangabeys. J Clin Invest. 2009; 119(12):3556-72. Epub 2009/12/05. DOI: 10.1172/JCI40115 PMID: 19959874
56. Scagnolari C, Monteleone K, Selvaggi C, Pierangeli A, D'Ettorre G, Mezzaroma I, et al. ISG15 expression correlates with HIV-1 viral load and with factors regulating T cell response. Immunobiology. 2016; 221(2):282-90. Epub 2015/11/14. DOI: 10.1016/j.imbio.2015.10.007 PMID: 26563749
57. Zhou Y, Wang X, Liu M, Hu Q, Song L, Ye L, et al. A critical function of toll-like receptor-3 in the induction of anti-human immunodeficiency virus activities in macrophages. Immunology. 2010; 131(1):40-9. Epub 2010/07/20. DOI: 10.1111/j.1365-2567.2010.03270.x PMID: 20636339
58. Ryan LK, Dai J, Yin Z, Megjugorac N, Uhlhorn V, Yim S, et al. Modulation of human beta-defensin-1 (hBD-1) in plasmacytoid dendritic cells (PDC), monocytes, and epithelial cells by influenza virus, Herpes simplex virus, and Sendai virus and its possible role in innate immunity. J Leukoc Biol. 2011; 90(2):343-56. Epub 2011/05/10.DOI: 10.1189/jlb.0209079 PMID: 21551252
59. Garraud O, Cognasse F. Platelet Toll-like receptor expression: the link between "danger" ligands and inflammation. Inflamm Allergy Drug Targets. 2010; 9(5):322-33. Epub 2010/06/04. PMID: 20518724
60. Kraemer BF, Campbell RA, Schwertz H, Cody MJ, Franks Z, Tolley ND, et al. Novel anti-bacterial activities of beta-defensin 1 in human platelets: suppression of pathogen growth and signaling of neutrophil extracellular trap formation. PLoS Pathog. 2011; 7(11):e1002355. Epub 2011/11/22. DOI: 10.1371/journal.ppat.1002355 PMID: 22102811
61. Gomez AM, Ouellet M, Tremblay MJ. HIV-1-triggered release of type I IFN by plasmacytoid dendritic cells induces BAFF production in monocytes. J Immunol. 2015; 194(5):2300-8. Epub 2015/02/01. DOI: 10.4049/jimmunol.1402147 PMID: 25637018
62. Randall RE, Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol. 2008; 89(Pt 1):1-47. Epub 2007/12/20. DOI: 10.1099/vir.0.83391-0 PMID: 18089727
63. Pott J, Mahlakoiv T, Mordstein M, Duerr CU, Michiels T, Stockinger S, et al. IFN-lambda determines the intestinal epithelial antiviral host defense. Proc Natl Acad Sci U S A. 2011; 108(19):7944-9. Epub 2011/04/27. DOI: 10.1073/pnas.1100552108 PMID: 21518880
64. Mangan NE, Fung KY. Type I interferons in regulation of mucosal immunity. Immunol Cell Biol. 2012; 90(5):510-9. Epub 2012/03/21. DOI: 10.1038/icb.2012.13 PMID: 22430250
65. Kelly CJ, Glover LE, Campbell EL, Kominsky DJ, Ehrentraut SF, Bowers BE, et al. Fundamental role for HIF-1alpha in constitutive expression of human beta defensin-1. Mucosal Immunol. 2013; 6(6):1110-8. Epub 2013/03/07. DOI: 10.1038/mi.2013.6 PMID: 23462909
66. Harder J, Bartels J, Christophers E, Schroder JM. A peptide antibiotic from human skin. Nature. 1997; 387(6636):861. Epub 1997/06/26. DOI: 10.1038/43088 PMID: 9202117
67. Book M, Chen Q, Lehmann LE, Klaschik S, Weber S, Schewe JC, et al. Inducibility of the endogenous antibiotic peptide beta-defensin 2 is impaired in patients with severe sepsis. Crit Care. 2007; 11(1):R19. Epub 2007/02/17. DOI: 10.1186/cc5694 PMID: 17302973
68. Gootenberg DB, Paer JM, Luevano JM, Kwon DS. HIV-associated changes in the enteric microbial community: potential role in loss of homeostasis and development of systemic inflammation. Curr Opin Infect Dis. 2017; 30(1):31-43. Epub 2016/12/07. DOI: 10.1097/QCO.0000000000000341 PMID: 27922852
69. Milanese M, Segat L, Pontillo A, Arraes LC, de Lima Filho JL, Crovella S. DEFB1 gene polymorphisms and increased risk of HIV-1 infection in Brazilian children. Aids. 2006; 20(12):1673-5. Epub 2006/07/27. DOI: 10.1097/01.aids.0000238417.05819.40 PMID: 16868452
70. Braida L, Boniotto M, Pontillo A, Tovo PA, Amoroso A, Crovella S. A single-nucleotide polymorphism in the human beta-defensin 1 gene is associated with HIV-1 infection in Italian children. Aids. 2004; 18 (11):1598-600. Epub 2004/07/09. PMID: 15238780
71. Ricci E, Malacrida S, Zanchetta M, Montagna M, Giaquinto C, De Rossi A. Role of beta-defensin-1 polymorphisms in mother-to-child transmission of HIV-1. J Acquir Immune Defic Syndr. 2009; 51(1):13-9. Epub 2009/04/25. DOI: 10.1097/QAI.0b013e31819df249 PMID: 19390326
72. Estrada-Aguirre JA, Osuna-Ramirez I, de Oca EP, Ochoa-Ramirez LA, Ramirez M, Magallon-Zazueta LG, et al. DEFB1 5'UTR Polymorphisms Modulate the Risk of HIV-1 Infection in Mexican Women. Curr HIV Res. 2014; 12(3):220-6. Epub 2014/07/09. PMID: 25001249