Comprehensive proteomic study identifies serpin and cystatin antiproteases as novel correlates of HIV-1 resistance in the cervicovaginal mucosa of female Sex workers

Journal of Proteome Research

Volumn 10, Issue 11, 2011, Pages 5139-5149

  Burgener, A ^a   Rahman, S ^a   Ahmad, R ^b   Lajoie, J ^a   Ramdahin, S ^a   Mesa, C ^d   Brunet, S ^d   Wachihi, C ^c   Kimani, J ^a,c   Fowke, K ^a,c   Carr, S ^b   Plummer, F ^a,d   Ball, T B ^a,c,d  

^a UNIVERSITY OF MANITOBA   (Canada)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF NAIROBI   (Kenya)

^d PUBLIC HEALTH AGENCY OF CANADA   (Canada)

Author keywords

biomarkers; cystatins; cysteine protease inhibitors; cytokines; HESN; HIV highly exposed seronegative individuals; HIV resistance; HIV 1; immune factors; infections; innate immunity; Kenyan sex workers; mass spectrometry; microbicides; mucosal immunity; prostitutes; proteomics; serine protease inhibitors; serpins; vaginal fluid

Indexed keywords

CYSTATIN; CYTOKINE; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; SERINE PROTEINASE INHIBITOR; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; FEMALE; FEMALE GENITAL SYSTEM; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN TISSUE; MAJOR CLINICAL STUDY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; SEXUAL BEHAVIOR; UTERINE CERVIX MUCOSA; VAGINA MUCOSA; VIRUS RESISTANCE;

ADULT; ALPHA 1-ANTITRYPSIN; ALPHA-MACROGLOBULINS; CERVIX UTERI; CYSTATIN B; DISEASE RESISTANCE; FEMALE; GENITALIA, FEMALE; HIV INFECTIONS; HIV-1; HUMANS; MIDDLE AGED; MUCOUS MEMBRANE; PHENOTYPE; PROTEOMICS; SERPINS; SEX WORKERS; VAGINA;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 80655129298     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200596r     Document Type: Article

References (72)

1. UNAIDS. Report on the global AIDS epidemic; 2009.
2. Rerks-Ngarm Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand N. Engl. J. Med. 2009, 361, 2209-2220
3. Garber, D. A.; Silvestri, G.; Feinberg, M. B. Prospects for an AIDS vaccine: three big questions, no easy answers Lancet Infect. Dis. 2004, 4 (7) 397-413 (Pubitemid 38844125)
4. Virgin, H. W.; Walker, B. D. Immunology and the elusive AIDS vaccine Nature 2010, 464, 224-31
5. Shattock, R. J.; Moore, J. P. Inhibiting sexual transmission of HIV-1 infection Nat. Rev. Microbiol. 2003, 1 (1) 25-34
6. Fowke, K. R. Resistance to HIV-1 infection among persistently seronegative prostitutes in Nairobi, Kenya Lancet 1996, 348 (9038) 1347-51 (Pubitemid 26383775)
7. Simonsen, J. N. HIV infection among lower socioeconomic strata prostitutes in Nairobi Aids 1990, 4 (2) 139-44 (Pubitemid 20108772)
8. Kaul, R. HIV-1-specific mucosal IgA in a cohort of HIV-1-resistant Kenyan sex workers Aids 1999, 13 (1) 23-9 (Pubitemid 29078060)
9. Kaul, R. HIV-1-specific mucosal CD8+ lymphocyte responses in the cervix of HIV-1-resistant prostitutes in Nairobi J. Immunol. 2000, 164 (3) 1602-11 (Pubitemid 30067280)
10. Horton, R. E. Cervical HIV-Specific IgA in a Population of Commercial Sex Workers Correlates with Repeated Exposure But Not Resistance to HIV. AIDS Res. Hum. Retroviruses 2008, not supplied.
11. Iqbal, S. M. Elevated T cell counts and RANTES expression in the genital mucosa of HIV-1-resistant Kenyan commercial sex workers J. Infect. Dis. 2005, 192 (5) 728-38 (Pubitemid 41193070)
12. Hirbod, T. HIV-1 neutralizing activity is correlated with increased levels of chemokines in saliva of HIV-1-exposed uninfected individuals Curr. HIV Res. 2008, 6 (1) 28-33 (Pubitemid 351461018)
13. Iqbal, S. M. Elevated elafin/trappin-2 in the female genital tract is associated with protection against HIV acquisition Aids 2009, 23 (13) 1669-77
14. Burgener, A. Identification of differentially expressed proteins in the cervical mucosa of HIV-1-resistant sex workers J. Proteome Res. 2008, 7 (10) 4446-54
15. Mangan, M. S.; Kaiserman, D.; Bird, P. I. The role of serpins in vertebrate immunity Tissue Antigens 2008, 72 (1) 1-10 (Pubitemid 351841645)
16. van Gent, D. Serpins: structure, function and molecular evolution Int. J. Biochem. Cell Biol. 2003, 35 (11) 1536-47 (Pubitemid 36724947)
17. Benarafa, C.; Priebe, G. P.; Remold-O'Donnell, E. The neutrophil serine protease inhibitor serpinb1 preserves lung defense functions in Pseudomonas aeruginosa infection J. Exp. Med. 2007, 204 (8) 1901-9 (Pubitemid 47236325)
18. Chertov, O. Identification of human neutrophil-derived cathepsin G and azurocidin/CAP37 as chemoattractants for mononuclear cells and neutrophils J. Exp. Med. 1997, 186 (5) 739-47 (Pubitemid 27381538)
19. Moriuchi, H.; Moriuchi, M.; Fauci, A. S. Cathepsin G, a neutrophil-derived serine protease, increases susceptibility of macrophages to acute human immunodeficiency virus type 1 infection J. Virol. 2000, 74 (15) 6849-55 (Pubitemid 30470668)
20. Janciauskiene, S. Inhibition of lipopolysaccharide-mediated human monocyte activation, in vitro, by alpha1-antitrypsin Biochem. Biophys. Res. Commun. 2004, 321 (3) 592-600 (Pubitemid 39118381)
21. Elmaleh, D. R.; Brown, N. V.; Geiben-Lynn, R. Anti-viral activity of human antithrombin III Int. J. Mol. Med. 2005, 16 (2) 191-200
22. Subramaniyam, D. TNF-alpha-induced self expression in human lung endothelial cells is inhibited by native and oxidized alpha1-antitrypsin Int. J. Biochem. Cell Biol. 2008, 40 (2) 258-71 (Pubitemid 350137878)
23. Pott, G. B. Alpha-1-antitrypsin is an endogenous inhibitor of proinflammatory cytokine production in whole blood J. Leukoc. Biol. 2009, 85 (5) 886-95
24. Congote, L. F. The C-terminal 26-residue peptide of serpin A1 is an inhibitor of HIV-1 Biochem. Biophys. Res. Commun. 2006, 343 (2) 617-22
25. Shapiro, L.; Pott, G. B.; Ralston, A. H. Alpha-1-antitrypsin inhibits human immunodeficiency virus type 1 FASEB J. 2001, 15 (1) 115-122 (Pubitemid 32061662)
26. Challacombe, S. J.; Sweet, S. P. Oral mucosal immunity and HIV infection: current status Oral Dis. 2002, 8 (Suppl 2) 55-62 (Pubitemid 41758942)
27. Ghosh, M. Trappin-2/Elafin: a novel innate anti-human immunodeficiency virus-1 molecule of the human female reproductive tract. Immunology 2009, not supplied.
28. Bingle, C. D.; Vyakarnam, A. Novel innate immune functions of the whey acidic protein family Trends Immunol. 2008, 29 (9) 444-53
29. Jensen, L. E.; Whitehead, A. S. Regulation of serum amyloid A protein expression during the acute-phase response Biochem. J. 1998, 334 (Pt 3) 489-503 (Pubitemid 28457193)
30. Li, Q. Recombinant human elafin protects airway epithelium integrity during inflammation. Mol. Biol. Rep. 2009, not supplied.
31. Taggart, C. C. Cathepsin B, L, and S cleave and inactivate secretory leucoprotease inhibitor J. Biol. Chem. 2001, 276 (36) 33345-52
32. Hasan, L. Function of liver activation-regulated chemokine/CC chemokine ligand 20 is differently affected by cathepsin B and cathepsin D processing J. Immunol. 2006, 176 (11) 6512-22 (Pubitemid 43787833)
33. Lim, J. K. N-terminal proteolytic processing by cathepsin G converts RANTES/CCL5 and related analogs into a truncated 4-68 variant J. Leukoc. Biol. 2006, 80 (6) 1395-404 (Pubitemid 44904978)
34. Bantscheff, M. Quantitative mass spectrometry in proteomics: a critical review Anal. Bioanal. Chem. 2007, 389 (4) 1017-31 (Pubitemid 47482251)
35. Venkataraman, N. Cationic polypeptides are required for anti-HIV-1 activity of human vaginal fluid J. Immunol. 2005, 175 (11) 7560-7 (Pubitemid 41713455)
36. Kramer, H. B. Elevation of intact and proteolytic fragments of acute phase proteins constitutes the earliest systemic antiviral response in HIV-1 infection PLoS Pathog. 2010, 6 (5) e1000893
37. Chen, C. H. The essentiality of alpha-2-macroglobulin in human salivary innate immunity against new H1N1 swine origin influenza A virus Proteomics 2010, 10 (12) 2396-401
38. Anderson, B. L.; Cu-Uvin, S. Clinical parameters essential to methodology and interpretation of mucosal responses Am. J. Reprod. Immunol. 2011, 65 (3) 352-60
39. Horton, R. E. Cohorts for the study of HIV-1-exposed but uninfected individuals: benefits and limitations J. Infect. Dis. 2010, 202 (Suppl 3) S377-81
40. Ball, T. B. Polymorphisms in IRF-1 associated with resistance to HIV-1 infection in highly exposed uninfected Kenyan sex workers Aids 2007, 21 (9) 1091-101 (Pubitemid 46763279)
41. Su, R. C. A transient IRF1 response in HIV-exposed, seronegative individuals differs from that in HIV-susceptible controls and is governed by epigenetic mechanisms. Blood 2011, not supplied.
42. Silverman, G. A. Serpins flex their muscle: I. Putting the clamps on proteolysis in diverse biological systems J. Biol. Chem. 2010, 285 (32) 24299-305
43. Silverman, G. A. The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions, and a revised nomenclature J. Biol. Chem. 2001, 276 (36) 33293-6
44. Whisstock, J. C. Serpins flex their muscle: II. Structural insights into target peptidase recognition, polymerization, and transport functions J. Biol. Chem. 2010, 285 (32) 24307-12
45. Ashton-Rickardt, P. G. Serine protease inhibitors and cytotoxic T lymphocytes Immunol. Rev. 2010, 235 (1) 147-58
46. Heutinck, K. M. Serine proteases of the human immune system in health and disease Mol. Immunol. 2010, 47 (11-12) 1943-55
47. Fahey, J. V. New approaches to making the microenvironment of the female reproductive tract hostile to HIV Am. J. Reprod. Immunol. 2011, 65, 334-343
48. Law, R. H. An overview of the serpin superfamily Genome Biol. 2006, 7 (5) 216
49. Askew, D. J.; Silverman, G. A. Intracellular and extracellular serpins modulate lung disease J. Perinatol. 2008, 28 (Suppl 3) S127-35
50. Wilson, T. J.; Nannuru, K. C.; Singh, R. K. Cathepsin G recruits osteoclast precursors via proteolytic activation of protease-activated receptor-1 Cancer Res. 2009, 69 (7) 3188-95
51. Sambrano, G. R. Cathepsin G activates protease-activated receptor-4 in human platelets J. Biol. Chem. 2000, 275 (10) 6819-23 (Pubitemid 30146221)
52. El Messaoudi, K. HIV-1 infectivity and host range modification by cathepsin D present in human vaginal secretions Aids 1999, 13 (3) 333-9
53. Hashemi, F. B. Myeloid-related protein (MRP)-8 from cervico-vaginal secretions activates HIV replication Aids 2001, 15 (4) 441-9 (Pubitemid 32207563)
54. Herrick, S. Up-regulation of elastase in acute wounds of healthy aged humans and chronic venous leg ulcers are associated with matrix degradation Lab. Invest. 1997, 77 (3) 281-8 (Pubitemid 27413540)
55. Ashcroft, G. S. Topical estrogen accelerates cutaneous wound healing in aged humans associated with an altered inflammatory response Am. J. Pathol. 1999, 155 (4) 1137-46 (Pubitemid 29488922)
56. Ashcroft, G. S. Secretory leukocyte protease inhibitor mediates non-redundant functions necessary for normal wound healing Nat. Med. 2000, 6 (10) 1147-53
57. Remold-O'Donnell, E.; Chin, J.; Alberts, M. Sequence and molecular characterization of human monocyte/neutrophil elastase inhibitor Proc. Natl. Acad. Sci. U.S.A. 1992, 89 (12) 5635-9
58. Schick, C. Squamous cell carcinoma antigen 2 is a novel serpin that inhibits the chymotrypsin-like proteinases cathepsin G and mast cell chymase J. Biol. Chem. 1997, 272 (3) 1849-55 (Pubitemid 27045716)
59. Jayakumar, A. Inhibition of the cysteine proteinases cathepsins K and L by the serpin headpin (SERPINB13): a kinetic analysis Arch. Biochem. Biophys. 2003, 409 (2) 367-74 (Pubitemid 36259605)
60. Oelschlager, C. Antithrombin III inhibits nuclear factor kappaB activation in human monocytes and vascular endothelial cells Blood 2002, 99 (11) 4015-20 (Pubitemid 35332042)
61. Nita, I. M.; Serapinas, D.; Janciauskiene, S. M. alpha1-Antitrypsin regulates CD14 expression and soluble CD14 levels in human monocytes in vitro Int. J. Biochem. Cell Biol. 2007, 39 (6) 1165-76 (Pubitemid 46819133)
62. Zhou, X. HIV Replication in CD4+ T Lymphocytes in the Presence and Absence of Follicular Dendritic Cells: Inhibition of Replication Mediated by {alpha}-1-Antitrypsin through Altered I{kappa}B{alpha} Ubiquitination J. Immunol. 2011, 186 (5) 3148-55
63. Li, Q. Glycerol monolaurate prevents mucosal SIV transmission Nature 2009, 458 (7241) 1034-8
64. Munch, J. Discovery and optimization of a natural HIV-1 entry inhibitor targeting the gp41 fusion peptide Cell 2007, 129 (2) 263-75 (Pubitemid 46574967)
65. Congote, L. F. Serpin A1 and CD91 as host instruments against HIV-1 infection: are extracellular antiviral peptides acting as intracellular messengers? Virus Res. 2007, 125 (2) 119-34 (Pubitemid 46589679)
66. Bryan, C. L. HIV infection is associated with reduced serum alpha-1-antitrypsin concentrations Clin. Invest. Med. 2010, 33 (6) E384-9
67. Potthoff, A. V. HIV infection in a patient with alpha-1 antitrypsin deficiency: a detrimental combination? Aids 2007, 21 (15) 2115-6 (Pubitemid 47462167)
68. McNeely, T. B. Secretory leukocyte protease inhibitor: a human saliva protein exhibiting anti-human immunodeficiency virus 1 activity in vitro J. Clin. Invest. 1995, 96 (1) 456-64
69. Schellenberg, J. J. Molecular definition of vaginal microbiota in East African commercial sex workers Appl. Environ. Microbiol. 2011, 77 (12) 4066-74
70. Miller, C. J.; Shattock, R. J. Target cells in vaginal HIV transmission Microbes Infect. 2003, 5 (1) 59-67 (Pubitemid 36197948)
71. McLaren, P. J. HIV-exposed seronegative commercial sex workers show a quiescent phenotype in the CD4+ T cell compartment and reduced expression of HIV-dependent host factors J. Infect. Dis. 2010, 202 (Suppl 3) S339-44
72. Card, C. M. Decreased immune activation in resistance to HIV-1 infection is associated with an elevated frequency of CD4(+)CD25(+)FOXP3(+) regulatory T cells J. Infect. Dis. 2009, 199 (9) 1318-22