Surfactant protein D inhibits HIV-1 infection of target cells via interference with gp120-CD4 interaction and modulates pro-inflammatory cytokine production

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Pandit, Hrishikesh ^a   Gopal, Sandhya ^a,e   Sonawani, Archana ^a   Yadav, Ajit Kumar ^a   Qaseem, Asif S ^b   Warke, Himangi ^c   Patil, Anushree ^a   Gajbhiye, Rahul ^a   Kulkarni, Vijay ^a   Al Mozaini, Maha Ahmed ^d   Idicula Thomas, Susan ^a   Kishore, Uday ^b   Madan, Taruna ^a  

^a NATIONAL INSTITUTE FOR RESEARCH IN REPRODUCTIVE HEALTH   (India)

^b BRUNEL UNIVERSITY   (United Kingdom)

^c KEM HOSPITAL   (India)

^d KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^e UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CD4 ANTIGEN; CYTOKINE; GLYCOPROTEIN GP 120; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE B; SURFACTANT PROTEIN D; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BINDING;

ADULT; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VITRO STUDY; JURKAT CELL LINE; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEMINAL PLASMA; U937 CELL LINE; VAGINAL LAVAGE; VIRUS ENTRY; VIRUS IMMUNITY; VIRUS ISOLATION; VIRUS REPLICATION; BIOSYNTHESIS; CHEMISTRY; DRUG EFFECTS; INFLAMMATION; METABOLISM; MOLECULAR DOCKING; MONOCYTE; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN CONFORMATION; SPERM; T LYMPHOCYTE; UTERINE CERVIX; VAGINA; VIROLOGY;

ADULT; ANTIGENS, CD4; CERVIX UTERI; CYTOKINES; FEMALE; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; INFLAMMATION; JURKAT CELLS; MALE; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR DOCKING SIMULATION; MONOCYTES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTO-ONCOGENE PROTEINS C-AKT; PULMONARY SURFACTANT-ASSOCIATED PROTEIN D; SEMEN; T-LYMPHOCYTES; VAGINA; VIRUS INTERNALIZATION;

EID: 84904574248     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102395     Document Type: Article

References (58)

1. Stacey AR, Norris PJ, Qin L, Haygreen EA, Taylor E, et al. (2009) 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. 83(8):3719-3733. doi: 10.1128/JVI.01844-08.
2. Herbein G, Gras G, Khan KA, Abbas W (2010) Macrophage signaling in HIV-1 infection. Retrovirology. 7: 34. doi: 10.1186/1742-4690-7-34.
3. Chun TW, Engel D, Mizell SB, Ehler LA, Fauci AS (1998) Induction of HIV-1 replication in latently infected CD4+ T cells using a combination of cytokines. J Exp Med. 6;188(1):83-91.
4. McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF (2010) The immune response during acute HIV-1 infection: clues for vaccine development. Nat. Rev. Immunol. 10(1):11-23. doi: 10.1038/nri2674.
5. Nayak A, Dodagatta-Marri E, Tsolaki AG, Kishore U (2012) An Insight into the Diverse Roles of Surfactant Proteins, SP-A and SP-D in Innate and Adaptive Immunity. Front Immunol. 7; 3: 131. doi: 10.3389/fimmu.2012.00131.
6. Kishore U, Greenhough TJ, Waters P, Shrive AK, Ghai R, et al. (2006) Surfactant proteins SP-A and SP-D: structure, function and receptors. Mol. Immunol. 43(9):1293-1315. (Pubitemid 43356370)
7. Gardai SJ, Xiao YQ, Dickinson M, Nick JA, Voelker DR, et al. (2003) By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115(1):13-23. (Pubitemid 37255314)
8. Jakel A, Qaseem AS, Kishore U, Sim RB (2013) Ligands and receptors of lung surfactant proteins SP-A and SP-D. Front Biosci 18: 1129-1140.
9. Yamazoe M, Nishitani C, Takahashi M, Katoh T, Ariki S, et al. (2008) Pulmonary surfactant protein D inhibits lipopolysaccharide (LPS)-induced inflammatory cell responses by altering LPS binding to its receptors. J Biol Chem. 283(51):35878-35888. doi: 10.1074/jbc.M807268200.
10. Borron PJ, Crouch EC, Lewis JF, Wright JR, Possmayer F, et al. (1998) Recombinant rat surfactant-associated protein D inhibits human T lymphocyte proliferation and IL-2 production. J Immunol. 161(9):4599-4603. (Pubitemid 28492032)
11. Borron PJ, Mostaghel EA, Doyle C, Walsh ES, McHeyzer-Williams MG, et al. (2002) Pulmonary surfactant proteins A and D directly suppress CD3+/CD4+ cell function: evidence for two shared mechanisms. J Immunol. 169(10):5844-5850. (Pubitemid 35291688)
12. Lin KW, Jen KY, Suarez CJ, Crouch EC, Perkins DL, et al. (2010) Surfactant protein D-mediated decrease of allergen-induced inflammation is dependent upon CTLA4. J Immunol. 184(11):6343-6349. doi: 10.4049/jimmunol. 0901947.
13. Clark H, Reid KB (2003) The potential of recombinant surfactant protein D therapy to reduce inflammation in neonatal chronic lung disease, cystic fibrosis, and emphysema. Arch Dis Child. 88(11): 981-984. doi: 10.1136/adc.88.11.981 (Pubitemid 37449404)
14. Meschi J, Crouch EC, Skolnik P, Yahya K, Holmskov U, et al. (2005) Surfactant protein D binds to human immunodeficiency virus (HIV) envelope protein gp120 and inhibits HIV replication. J Gen Virol. 86: 3097-3107. (Pubitemid 41555576)
15. Madsen J, Gaiha GD, Palaniyar N, Dong T, Mitchell DA, et al. (2013) Surfactant Protein D modulates HIV infection of both T-cells and dendritic cells. PLoS One. 8(3):e59047. doi: 10.1371/journal.pone.0059047.
16. Leth-Larsen R, Floridon C, Nielsen O, Holmskov U (2004) Surfactant protein D in the female genital tract. Mol Hum Reprod 10: 149-154. doi: 10.1093/molehr/gah022. (Pubitemid 38456015)
17. Jambo KC, French N, Zijlstra E, Gordon SB (2009) AIDS patients have increased surfactant protein D but normal mannose binding lectin levels in lung fluid. Respir Res 13;8: 42.
18. Kunisaki KM, Quick H, Baker JV (2011). HIV antiretroviral therapy reduces circulating surfactant protein-D levels. HIV Med. 12(9):580-581. doi: 10.1111/j.1468-1293.2011.00920.x.
19. Li Y, O'Dell S, Walker LM, Wu X, Guenaga J, et al. (2011) Mechanism of neutralization by the broadly neutralizing HIV-1 monoclonal antibody VRC01. J. Virol. 85(17):8954-8967. doi: 10.1128/JVI.00754-11.
20. West AP Jr, Scharf L, Horwitz J, Klein F, Nussenzweig MC, et al. (2013) Computational analysis of anti-HIV-1 antibody neutralization panel data to identify potential functional epitope residues. Proc Natl Acad Sci U S A. 110(26):10598-10603. doi: 10.1073/pnas.1309215110.
21. Clevestig P, Pramanik L, Leitner T, Ehrnst A (2006) CCR5 use by human immunodeficiency virus type 1 is associated closely with the gp120 V3 loop N-linked glycosylation site. J Gen Virol. 87(Pt 3):607-612.
22. Stokoe D, Stephens LR, Copeland T, Gaffney PR, Reese CB, et al. (1997) Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277: 567-570. (Pubitemid 27369005)
23. Bellacosa A, Chan TO, Ahmed NN, Datta K, Malstrom S, et al. (1998) Akt activation by growth factors is a multiple-step process: the role of the PH domain. Oncogene 17: 313-325. (Pubitemid 28383008)
24. François F, Klotman ME (2003) Phosphatidylinositol 3-kinase regulates human immunodeficiency virus type 1 replication following viral entry in primary CD4+ T lymphocytes and macrophages. J Virol. 77(4):2539-2549. (Pubitemid 36222778)
25. Gallo SA, Finnegan CM, Viard M, Raviv Y, Dimitrov A, et al. (2003) The HIV Env-mediated fusion reaction. Biochim Biophys Acta. 1614(1):36-50. (Pubitemid 36857094)
26. Parren PW, Mondor I, Naniche D, Ditzel HJ Klasse PJ, et al. (1998) Neutralization of human immunodeficiency virus type 1 by antibody to gp120 is determined primarily by occupancy of sites on the virion irrespective of epitope specificity. J. Virol. 72: 3512-3519. (Pubitemid 28188645)
27. Esser MT, Mori T, Mondor I, Sattentau QJ, Dey B, et al. (1999) Cyanovirin-N binds to gp120 to interfere with CD4-dependent human immunodeficiency virus type 1 virion binding, fusion, and infectivity but does not affect the CD4 binding site on gp120 or soluble CD4-induced conformational changes in gp120. J Virol. 73(5):4360-4371. (Pubitemid 29189883)
28. Scheid JF, Mouquet H, Ueberheide B, Diskin R, Klein F, et al. (2011) Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333(6049):1633-1637.
29. Balzarini J, Van Laethem K, Hatse S, Froeyen M, Peumans W, et al. (2005) Carbohydrate-binding agents cause deletions of highly conserved glycosylation sites in HIV GP120: a new therapeutic concept to hit the achilles heel of HIV. J Biol Chem. 280(49):41005-41014. (Pubitemid 41780596)
30. Li Y, O'Dell S, Walker LM, Wu X, Guenaga J, et al. (2011) Mechanism of neutralization by the broadly neutralizing HIV-1 monoclonal antibody VRC01. J Virol. Sep;85(17):8954-67. doi: 10.1128/JVI.00754-11.
31. Chirmule N, Pahwa S (1996) Envelope glycoproteins of human immunodeficiency virus type 1: Profound influences on immune functions. Microbiol Rev. 60(2):386-406. (Pubitemid 26170912)
32. Rychert J, Strick D, Bazner S, Robinson J, Rosenberg E (2010) Detection of HIV gp120 in plasma during early HIV infection is associated with increased pro-inflammatory and immunoregulatory cytokines. AIDS Res Hum Retroviruses. 26(10):1139-1145. doi: 10.1089/aid.2009.0290.
33. Longo N, Zabay JM, Sempere JM, Navarro J, Fernández-Cruz E (1993) Altered production of PGE2, IL-1 beta and TNF-alpha by peripheral blood monocytes from HIV-positive individuals at early stages of HIV infection. J Acquir Immune Defic Syndr. 6(9):1017-1023. (Pubitemid 23239773)
34. Biswas P, Poli G, Orenstein JM, Fauci AS (1994) Cytokine-mediated induction of human immunodeficiency virus (HIV) expression and cell death in chronically infected U1 cells: do tumor necrosis factor alpha and gamma interferon selectively kill HIV-infected cells? J Virol. 68(4):2598-604.
35. Zaitseva M, Lee S, Lapham C, Taffs R, King L, et al. (2000) Interferon gamma and interleukin 6 modulate the susceptibility of macrophages to human immunodeficiency virus type 1 infection. Blood 96 (9):3109-3117.
36. Poli G, Kinter AL, Fauci AS (1994) Interleukin 1 induces expression of the human immunodeficiency virus alone and in synergy with interleukin 6 in chronically infected U1 cells: inhibition of inductive effects by the interleukin 1 receptor antagonist. Proc Natl Acad Sci U S A 91(1):108-112.
37. Graziosi C, Gantt KR, Vaccarezza M, Demarest JF, Daucher M, et al. (1996) Kinetics of cytokine expression during primary human immunodeficiency virus type 1 infection. Proc Natl Acad Sci U S A 93(9):4386-4391. (Pubitemid 26144297)
38. Mengozzi M, De Filippi C, Transidico P, Biswas P, Cota M, et al. (1999) Human immunodeficiency virus replication induces monocyte chemotactic protein-1 in human macrophages and U937 promonocytic cells. Blood 93(6):1851-1857. (Pubitemid 29128486)
39. Bahbouhi B, Landay A, Al-Harthi L (2004) Dynamics of cytokine expression in HIV productively infected primary CD4 + T cells. Blood 103(12):4581-4587. (Pubitemid 38745986)
40. Ascherl G, Hohenadl C, Schatz O, Shumay E, Bogner J, et al. (1999) Infection with human immunodeficiency virus-1 increases expression of vascular endothelial cell growth factor in T cells: implications for acquired immunodeficiency syndrome-associated vasculopathy. Blood. 93(12):4232-4241. (Pubitemid 29279265)
41. LeVine AM, Whitsett JA, Hartshorn KL, Crouch EC, Korfhagen TR (2001) Surfactant Protein D Enhances Clearance of Influenza A Virus from the Lung In Vivo. J Immunol 167: 5868-5873. (Pubitemid 33062780)
42. LeVine AM, Elliott J, Whitsett JA, Srikiatkhachorn A, Crouch E, et al. (2004) Surfactant protein-D enhances phagocytosis and pulmonary clearance of respiratory syncytial virus. Am J Respir Cell Mol Biol. 31(2):193-199. (Pubitemid 39095448)
43. Popik W, Hesselger JE, Pitha PM (1998) Binding of human immunodeficiency virus type 1 to CD4 and CXCR4 receptors differentially regulates the expression of inflammatory genes and activates the MEK/ERK signaling pathway. J. Virol. 72: 6404-6413.
44. Furler RL, Uittenbogaart CH (2010) Signaling through the P38 and ERK pathways: a common link between HIV replication and the immune response. Immunol Res. 2010 48(1-3):99-109. doi: 10.1007/s12026-010-8170-1.
45. Balzarini J (2007) Carbohydrate-binding agents: a potential future cornerstone for the chemotherapy of enveloped viruses? Antivir Chem Chemother. 18(1):1-11.
46. Kankavi O, Ata A, Celik-Ozenci C, Sati L, Ciftcioglu MA, et al. (2008) Presence and subcellular localizations of surfactant proteins A and D in human spermatozoa. Fertil Steril. 90(5):1904-1909. doi: 10.1016/j.fertnstert.2007.09. 064.
47. Kankavi O, Ata A, Akif Ciftcioglu M (2006) Surfactant protein A and D in the reproductive tract of stallion. Theriogenology. 66(5):1057-1064. (Pubitemid 44232929)
48. Strong P, Kishore U, Morgan C, Lopez Bernal A, Singh M, et al. (1998) A novel method of purifying lung surfactant proteins A and D from the lung lavage of alveolar proteinosis patients and from pooled amniotic fluid. J Immunol Methods. 220(1-2):139-149. (Pubitemid 28527076)
49. Dodagatta-Marri E, Qaseem AS, Karbani N, Tsolaki AG, Waters P, et al. (2014) Purification of surfactant protein D (SP-D) from pooled amniotic fluid and bronchoalveolar lavage. Methods Mol Biol. 1100: 273-290. doi: 10.1007/978-1-62703-724-2-22.
50. Mahajan L, Madan T, Kamal N, Singh VK, Sim RB, et al. (2008) Recombinant surfactant protein-D selectively increases apoptosis in eosinophils of allergic asthmatics and enhances uptake of apoptotic eosinophils by macrophages. Int Immunol. 2008 20(8):993-1007. doi: 10.1093/intimm/dxn058
51. Ciminale V, Felber BK, Campbell M, Pavlakis GN (1990) A bioassay for HIV-1 based on Env-CD4 interaction. AIDS Res. Hum.Retrovir. 6: 1281-1287.
52. Shrive AK, Tharia HA, Strong P, Kishore U, Burns I, et al. (2003) High-resolution structural insights into ligand binding and immune cell recognition by human lung surfactant protein D. J Mol Biol. 331(2):509-523. (Pubitemid 36904033)
53. Pancera M, Majeed S, Ban YE, Chen L, Huang CC, et al. (2010) Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc Natl Acad Sci U S A. 107(3):1166-1171. doi: 10.1073/pnas.0911004107.
54. Schneidman-Duhovny D, Inbar Y, Nussinov R, Wolfson HJ (2005) PatchDock and SymmDock: servers for rigid and symmetric docking. Nucl. Acids. Res. 33:W363-367. (Pubitemid 44529944)
55. Andrusier N, Nussinov R, Wolfson HJ (2007) FireDock: Fast Interaction Refinement in Molecular Docking. Proteins 69(1):139-159. (Pubitemid 47339146)
56. Swanson MD, Winter HC, Goldstein IJ, Markovitz DM (2010) A lectin isolated from bananas is a potent inhibitor of HIV replication. J Biol Chem. 285(12):8646-8655. doi: 10.1074/jbc.M109.034926.
57. Mahajan L, Pandit H, Madan T, Gautam P, Yadav AK, et al. (2013) Human surfactant protein D alters oxidative stress and HMGA1 expression to induce p53 apoptotic pathway in eosinophil leukemic cell line. PLoS One. 8(12):e85046. doi: 10.1371/journal.pone.0085046.
58. Keller MJ, Mesquita PM, Torres NM, Cho S, Shust G, et al. (2010) Postcoital bioavailability and antiviral activity of 0.5% PRO 2000 gel: implications for future microbicide clinical trials. PLoS One. 5(1):e8781. doi: 10.1371/journal.pone.0008781.