Molecular signatures of immune activation and epithelial barrier remodeling are enhanced during the luteal phase of the menstrual cycle: Implications for HIV susceptibility

Journal of Virology

Volumn 89, Issue 17, 2015, Pages 8793-8805

  Birse, Kenzie ^a,b   Arnold, Kelly B ^c   Novak, Richard M ^e   McCorrister, Stuart ^d   Shaw, Souradet ^b   Westmacott, Garrett R ^d   Ball, Terry B ^a,b,f   Lauffenburger, Douglas A ^c   Burgener, Adam ^a,b,g  

^a PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

^c Massachusetts Institute of Technology Cambridge   (United States)

^d PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^e UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^f UNIVERSITY OF NAIROBI   (Kenya)

^g KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 8; CELL ADHESION MOLECULE; IL8 PROTEIN, HUMAN;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL ADHESION; CELL INFILTRATION; CELL MOTION; CERVICOVAGINAL LAVAGE; CONTROLLED STUDY; EPITHELIUM; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; INFECTION SENSITIVITY; LUTEAL PHASE; MASS SPECTROMETRY; MATHEMATICAL COMPUTING; MENSTRUAL CYCLE; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; TANDEM MASS SPECTROMETRY; TISSUE REGENERATION; VAGINAL LAVAGE; VIRUS INFECTIVITY; VIRUS TRANSMISSION; ADOLESCENT; DISEASE PREDISPOSITION; FOLLICULAR PHASE; GENE EXPRESSION PROFILING; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; METABOLISM; MIDDLE AGED; VIROLOGY; YOUNG ADULT;

PRIMATES;

ADOLESCENT; ADULT; CD4-POSITIVE T-LYMPHOCYTES; CELL ADHESION MOLECULES; DISEASE SUSCEPTIBILITY; EPITHELIUM; FEMALE; FOLLICULAR PHASE; GENE EXPRESSION PROFILING; HIV INFECTIONS; HIV-1; HUMANS; INTERLEUKIN-8; LUTEAL PHASE; MIDDLE AGED; NEUTROPHILS; TANDEM MASS SPECTROMETRY; YOUNG ADULT;

EID: 84938928921     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00756-15     Document Type: Article

References (58)

1. UNAIDS. 2012. Women out loud: how women living with HIV will help the world end AIDS. UNAIDS, Geneva, Switzerland.
2. UNAIDS. 2013. UNAIDS report on the global AIDS epidemic 2013. UNAIDS, Geneva, Switzerland.
3. Venkatesh KK, Cu-Uvin S. 2014. Anatomic and hormonal changes in the female reproductive tract immune environment during the life cycle: implications for HIV/STI prevention research. Am J Reprod Immunol 71: 495-504. http://dx.doi.org/10.1111/aji.12247.
4. Polis CB, Phillips SJ, Curtis KM, Westreich DJ, Steyn PS, Raymond E, Hannaford P, Turner AN. 2014. Hormonal contraceptive methods and risk of HIV acquisition in women: a systematic review of epidemiological evidence. Contraception 90:360-390. http://dx.doi.org/10.1016/j.contraception.2014.07.009.
5. Ralph LJ, McCoy SI, Shiu K, Padian NS. 2015. Hormonal contraceptive use and women's risk of HIV acquisition: a meta-analysis of observational studies. Lancet Infect Dis 15:181-189. http://dx.doi.org/10.1016/S1473-3099(14)71052-7.
6. Goode D, Aravantinou M, Jarl S, Truong R, Derby N, Guerra-Perez N, Kenney J, Blanchard J, Gettie A, Robbiani M, Martinelli E. 2014. Sex hormones selectively impact the endocervical mucosal microenvironment: implications for HIV transmission. PLoS One 9:e97767. http://dx.doi.org/10.1371/journal.pone.0097767.
7. Morrison CS, Chen PL, Kwok C, Baeten JM, Brown J, Crook AM, Van Damme L, Delany-Moretlwe S, Francis SC, Friedland BA, Hayes RJ, Heffron R, Kapiga S, Karim QA, Karpoff S, Kaul R, McClelland RS, McCormack S, McGrath N, Myer L, Rees H, van der Straten A, Watson-Jones D, van de Wijgert JH, Stalter R, Low N. 2015. Hormonal contraception and the risk of HIV acquisition: an individual participant data meta-analysis. PLoS Med 12:e1001778. http://dx.doi.org/10.1371/journal.pmed.1001778.
8. Vishwanathan SA, Guenthner PC, Lin CY, Dobard C, Sharma S, Adams DR, Otten RA, Heneine W, Hendry RM, McNicholl JM, Kersh EN. 2011. High susceptibility to repeated, low-dose, vaginal SHIV exposure late in the luteal phase of the menstrual cycle of pigtail macaques. J Acquir Immune Defic Syndr 57:261-264. http://dx.doi.org/10.1097/QAI.0b013e318220ebd3.
9. Kersh EN, Henning T, Vishwanathan SA, Morris M, Butler K, Adams DR, Guenthner P, Srinivasan P, Smith J, Radzio J, Garcia-Lerma JG, Dobard C, Heneine W, McNicholl J. 2014. SHIV susceptibility changes during the menstrual cycle of pigtail macaques. J Med Primatol 43:310-316. http://dx.doi.org/10.1111/jmp.12124.
10. Saba E, Origoni M, Taccagni G, Ferrari D, Doglioni C, Nava A, Lisco A, Grivel JC, Margolis L, Poli G. 2013. Productive HIV-1 infection of human cervical tissue ex vivo is associated with the secretory phase of the menstrual cycle. Mucosal Immunol 6:1081-1090. http://dx.doi.org/10.1038/mi.2013.2.
11. Heffron R, Donnell D, Rees H, Celum C, Mugo N, Were E, de Bruyn G, Nakku-Joloba E, Ngure K, Kiarie J, Coombs RW, Baeten JM, Partners in Prevention HSVHIVTST. 2012. Use of hormonal contraceptives and risk of HIV-1 transmission: a prospective cohort study. Lancet Infect Dis 12:19-26. http://dx.doi.org/10.1016/S1473-3099(11)70247-X.
12. Anderson DJ, Marathe J, Pudney J. 2014. The structure of the human vaginal stratum corneum and its role in immune defense. Am J Reprod Immunol 71:618-623. http://dx.doi.org/10.1111/aji.12230.
13. Hickey DK, Patel MV, Fahey JV, Wira CR. 2011. Innate and adaptive immunity at mucosal surfaces of the female reproductive tract: stratification and integration of immune protection against the transmission of sexually transmitted infections. J Reprod Immunol 88:185-194. http://dx.doi.org/10.1016/j.jri.2011.01.005.
14. Northern AL, Rutter SM, Peterson CM. 1994. Cyclic changes in the concentrations of peripheral blood immune cells during the normal menstrual cycle. Proc Soc Exp Biol Med 207:81-88. http://dx.doi.org/10.3181/00379727-207-43795.
15. Wira CR, Rodriguez-Garcia M, Patel MV. 2015. The role of sex hormones in immune protection of the female reproductive tract. Nat Rev Immunol 15:217-230. http://dx.doi.org/10.1038/nri3819.
16. Carias AM, McCoombe S, McRaven M, Anderson M, Galloway N, Vandergrift N, Fought AJ, Lurain J, Duplantis M, Veazey RS, Hope TJ. 2013. Defining the interaction of HIV-1 with the mucosal barriers of the female reproductive tract. J Virol 87:11388-11400. http://dx.doi.org/10.1128/JVI.01377-13.
17. Shapiro L, Pott GB, Ralston AH. 2001. Alpha-1-antitrypsin inhibits human immunodeficiency virus type 1. FASEB J 15:115-122. http://dx.doi.org/10.1096/fj.00-0311com.
18. Iqbal SM, Ball TB, Levinson P, Maranan L, Jaoko W, Wachihi C, Pak BJ, Podust VN, Broliden K, Hirbod T, Kaul R, Plummer FA. 2009. Elevated elafin/trappin-2 in the female genital tract is associated with protection against HIV acquisition. AIDS 23:1669-1677. http://dx.doi.org/10.1097/QAD.0b013e32832ea643.
19. Broliden K, Hinkula J, Devito C, Kiama P, Kimani J, Trabbatoni D, Bwayo JJ, Clerici M, Plummer F, Kaul R. 2001. Functional HIV-1 specific IgA antibodies in HIV-1 exposed, persistently IgG seronegative female sex workers. Immunol Lett 79:29-36. http://dx.doi.org/10.1016/S0165-2478(01)00263-2.
20. Bristow CL, Mercatante DR, Kole R. 2003. HIV-1 preferentially binds receptors copatched with cell-surface elastase. Blood 102:4479-4486. http://dx.doi.org/10.1182/blood-2003-05-1635.
21. Hirbod T, Kong X, Kigozi G, Ndyanabo A, Serwadda D, Prodger JL, Tobian AA, Nalugoda F, Wawer MJ, Shahabi K, Rojas OL, Gommerman JL, Broliden K, Kaul R, Gray RH. 2014. HIV acquisition is associated with increased antimicrobial peptides and reduced HIV neutralizing IgA in the foreskin prepuce of uncircumcised men. PLoS Pathog 10: e1004416. http://dx.doi.org/10.1371/journal.ppat.1004416.
22. Levinson P, Kaul R, Kimani J, Ngugi E, Moses S, MacDonald KS, Broliden K, Hirbod T, Kibera HIV Study Group. 2009. Levels of innate immune factors in genital fluids: association of alpha defensins and LL-37 with genital infections and increased HIV acquisition. AIDS 23:309-317. http://dx.doi.org/10.1097/QAD.0b013e328321809c.
23. Burgener A, Rahman S, Ahmad R, Lajoie J, Ramdahin S, Mesa C, Brunet S, Wachihi C, Kimani J, Fowke K, Carr S, Plummer F, Ball TB. 2011. Comprehensive proteomic study identifies serpin and cystatin antiproteases as novel correlates of HIV-1 resistance in the cervicovaginal mucosa of female sex workers. J Proteome Res 10:5139-5149. http://dx.doi.org/10.1021/pr200596r.
24. Rahman S, Rabbani R, Wachihi C, Kimani J, Plummer FA, Ball TB, Burgener A. 2013. Mucosal serpin A1 and A3 levels in HIV highly exposed seronegative women are affected by the menstrual cycle and hormonal contraceptives but are independent of epidemiological confounders.AmJ Reprod Immunol 69:64-72. http://dx.doi.org/10.1111/aji.12014.
25. Wira CR, Fahey JV. 2008. A new strategy to understand how HIV infects women: identification of a window of vulnerability during the menstrual cycle. AIDS 22:1909-1917. http://dx.doi.org/10.1097/QAD.0b013e3283060ea4.
26. Wira CR, Patel MV, Ghosh M, Mukura L, Fahey JV. 2011. Innate immunity in the human female reproductive tract: endocrine regulation of endogenous antimicrobial protection against HIV and other sexually transmitted infections. Am J Reprod Immunol 65:196-211. http://dx.doi.org/10.1111/j.1600-0897.2011.00970.x.
27. Burgener A, Tjernlund A, Kaldensjo T, Abou M, McCorrister S, Westmacott GR, Mogk K, Ambrose E, Broliden K, Ball B. 2013. A systems biology examination of the human female genital tract shows compartmentalization of immune factor expression. J Virol 87:5141-5150. http://dx.doi.org/10.1128/JVI.03347-12.
28. Lau KS, Schrier SB, Gierut J, Lyons J, Lauffenburger DA, Haigis KM. 2013. Network analysis of differential Ras isoform mutation effects on intestinal epithelial responses to TNF-α. Integr Biol 5:1355-1365. http://dx.doi.org/10.1039/c3ib40062j.
29. Benedict KF, Mac Gabhann F, Amanfu RK, Chavali AK, Gianchandani EP, Glaw LS, Oberhardt MA, Thorne BC, Yang JH, Papin JA, Peirce SM, Saucerman JJ, Skalak TC. 2011. Systems analysis of small signaling modules relevant to eight human diseases. Ann Biomed Eng 39:621-635. http://dx.doi.org/10.1007/s10439-010-0208-y.
30. Arnold K, Burgener A, Birse K, Dunphy L, Shahabi K, Abou M, Kwatampora J, Nyanga B, Kimani J, Liebenberg L, Masson L, Karim SS, Passmore JA, Lauffenburger DA, Kaul R, McKinnon LR. 2014. Mucosal proteomic profiles associated with female genital tract inflammation. AIDS Res Hum Retroviruses 30(Suppl 1):A235. http://dx.doi.org/10.1089/aid.2014.5518.abstract.
31. Benedict KF, Lauffenburger DA. 2013. Insights into proteomic immune cell signaling and communication via data-driven modeling. Curr Top Microbiol Immunol 363:201-233. http://dx.doi.org/10.1007/82_2012_249.
32. Birse KM, Burgener A, Westmacott GR, McCorrister S, Novak RM, Ball TB. 2013. Unbiased proteomics analysis demonstrates significant variability in mucosal immune factor expression depending on the site and method of collection. PLoS One 8:e79505. http://dx.doi.org/10.1371/journal.pone.0079505.
33. Hartlieb E, Kempf B, Partilla M, Vigh B, Spindler V, Waschke J. 2013. Desmoglein 2 is less important than desmoglein 3 for keratinocyte cohesion. PLoS One 8:e53739. http://dx.doi.org/10.1371/journal.pone.0053739.
34. Contzler R, Favre B, Huber M, Hohl D. 2005. Cornulin, a new member of the "fused gene" family, is expressed during epidermal differentiation. J Investig Dermatol 124:990-997. http://dx.doi.org/10.1111/j.0022-202X.2005.23694.x.
35. Brocklehurst K, Philpott MP. 2013. Cysteine proteases: mode of action and role in epidermal differentiation. Cell Tissue Res 351:237-244. http://dx.doi.org/10.1007/s00441-013-1557-2.
36. de Koning HD, van den Bogaard EH, Bergboer JG, Kamsteeg M, van Vlijmen-Willems IM, Hitomi K, Henry J, Simon M, Takashita N, Ishida-Yamamoto A, Schalkwijk J, Zeeuwen PL. 2012. Expression profile of cornified envelope structural proteins and keratinocyte differentiationregulating proteins during skin barrier repair. Br J Dermatol 166:1245-1254. http://dx.doi.org/10.1111/j.1365-2133.2012.10885.x.
37. Fadini GP, Albiero M, Millioni R, Poncina N, Rigato M, Scotton R, Boscari F, Brocco E, Arrigoni G, Villano G, Turato C, Biasiolo A, Pontisso P, Avogaro A. 2014. The molecular signature of impaired diabetic wound healing identifies serpinB3 as a healing biomarker. Diabetologia 57:1947-1956. http://dx.doi.org/10.1007/s00125-014-3300-2.
38. Guttman O, Baranovski BM, Schuster R, Kaner Z, Freixo-Lima GS, Bahar N, Kalay N, Mizrahi MI, Brami I, Ochayon DE, Lewis EC. 2015. Acute-phase protein α1 anti-trypsin: diverting injurious innate and adaptive immune responses from non-authentic threats. Clin Exp Immunol 179:161-172. http://dx.doi.org/10.1111/cei.12476.
39. Aboud L, Ball TB, Tjernlund A, Burgener A. 2014. The role of serpin and cystatin antiproteases in mucosal innate immunity and their defense against HIV. Am J Reprod Immunol 71:12-23. http://dx.doi.org/10.1111/aji.12166.
40. Mannan T, Jing S, Foroushania SH, Fortune F, Wan H. 2011. RNAimediated inhibition of the desmosomal cadherin (desmoglein 3) impairs epithelial cell proliferation. Cell Prolif 44:301-310. http://dx.doi.org/10.1111/j.1365-2184.2011.00765.x.
41. Presland RB, Dale BA. 2000. Epithelial structural proteins of the skin and oral cavity: function in health and disease. Crit Rev Oral Biol Med 11:383-408. http://dx.doi.org/10.1177/10454411000110040101.
42. Vandepitte J, Weiss HA, Bukenya J, Nakubulwa S, Mayanja Y, Matovu G, Kyakuwa N, Hughes P, Hayes R, Grosskurth H. 2013. Alcohol use, mycoplasma genitalium, and other STIs associated With HIV incidence among women at high risk in Kampala, Uganda. J Acquir Immune Defic Syndr 62:119-126. http://dx.doi.org/10.1097/QAI.0b013e3182777167.
43. Buve A, Jespers V, Crucitti T, Fichorova RN. 2014. The vaginal microbiota and susceptibility to HIV. AIDS 28:2333-2344. http://dx.doi.org/10.1097/QAD.0000000000000432.
44. Burgener A, Boutilier J, Wachihi C, Kimani J, Carpenter M, Westmacott G, Cheng K, Ball TB, Plummer F. 2008. Identification of differentially expressed proteins in the cervical mucosa of HIV-1-resistant sex workers. J Proteome Res 7:4446-4454. http://dx.doi.org/10.1021/pr800406r.
45. Lu RY, Yang WX, Hu YJ. 2014. The role of epithelial tight junctions involved in pathogen infections. Mol Biol Rep 41:6591-6610. http://dx.doi.org/10.1007/s11033-014-3543-5.
46. McKinnon LR, Kaul R. 2012. Quality and quantity: mucosal CD4+ T cells and HIV susceptibility. Curr Opin HIV AIDS 7:195-202. http://dx.doi.org/10.1097/COH.0b013e3283504941.
47. Evans J, Salamonsen LA. 2012. Inflammation, leukocytes, and menstruation. Rev Endocrinol Metab Disord 13:277-288. http://dx.doi.org/10.1007/s11154-012-9223-7.
48. Vishwanathan SA BA, Bosinger S, Tharp G, Guenthner P, Patel N, Birse K, Westmacott G, Henning T, Hanson D, Radzio J, Garcia-Lerma G, Ball B, McNicholl J, Kersh E. Cataloguing of potential HIV susceptibility factors during the menstrual cycle of pigtail macaques using a systems biology approach. J Virol, in press.
49. Salamonsen LA, Zhang J, Brasted M. 2002. Leukocyte networks and human endometrial remodeling. J Reprod Immunol 57:95-108. http://dx.doi.org/10.1016/S0165-0378(02)00011-6.
50. Tjernlund A, Carias AM, Andersson S, Gustafsson-Sanchez S, Rohl M, Petersson P, Introini A, Hope TJ, Broliden K. 2015. Progesterone-based intrauterine device use is associated with a thinner apical layer of the human ectocervical epithelium and a lower ZO-1 mRNA expression. Biol Reprod 92:68. http://dx.doi.org/10.1095/biolreprod.114.122887.
51. Berbic M, Ng CH, Black K, Markham R, Russell P, Basten A, Fraser IS, Hey-Cunningham AJ. 2013. A novel pilot study of endometrial stromal cells and immune cell populations in sentinel uterine-draining lymph nodes during the menstrual cycle and in endometriosis. Reprod Sci 20: 1339-1348. http://dx.doi.org/10.1177/1933719113485298.
52. Chertov O, Michiel DF, Xu L, Wang JM, Tani K, Murphy WJ, Longo DL, Taub DD, Oppenheim JJ. 1996. Identification of defensin-1, defensin-2, and CAP37/azurocidin as T-cell chemoattractant proteins released from interleukin-8-stimulated neutrophils. J Biol Chem 271:2935-2940. http://dx.doi.org/10.1074/jbc.271.6.2935.
53. Wang JM, Xu L, Murphy WJ, Taub DD, Chertov O. 1996. IL-8-induced T-lymphocyte migration: direct as well as indirect mechanisms. Methods 10:135-144. http://dx.doi.org/10.1006/meth.1996.0087.
54. Carnathan DG, Wetzel KS, Yu J, Lee ST, Johnson BA, Paiardini M, Yan J, Morrow MP, Sardesai NY, Weiner DB, Ertl HC, Silvestri G. 2015. Activated CD4+ CCR5+ T cells in the rectum predict increased SIV acquisition in SIVGag/Tat-vaccinated rhesus macaques. Proc Natl Acad Sci U S A 112:518-523. http://dx.doi.org/10.1073/pnas.1407466112.
55. Byrne EH, Anahtar M, Doherty K, Olson G, Bowman B, Padavattan N, Ndhlovu Z, Ghebremichael M, Walker B, Ndung'u T, Dong K, Kwon DS. 2014. Injectable contraceptive use correlates with increased HIV target cells at the cervix in young South African women. AIDS ResHumRetrovir 30(Suppl 1):A54-A55. http://dx.doi.org/10.1089/aid.2014.5096.abstract.
56. Guthrie BL, Introini A, Roxby AC, Choi RY, Bosire R, Lohman-Payne B, Hirbod T, Farquhar C, Broliden K. 2015. Depot medroxyprogesterone acetate (DMPA) use is associated with elevated innate immune effector molecules in cervicovaginal secretions of HIV-1-uninfected women. J Acquir Immune Defic Syndr 69:1-10. http://dx.doi.org/10.1097/QAI.0000000000000533.
57. Garza-Flores J. 1994. Pharmacokinetics of once-a-month injectable contraceptives. Contraception 49:347-359. http://dx.doi.org/10.1016/0010-7824(94)90032-9.
58. Chaban B, Links MG, Jayaprakash TP, Wagner EC, Bourque DK, Lohn Z, Albert AY, van Schalkwyk J, Reid G, Hemmingsen SM, Hill JE, Money DM. 2014. Characterization of the vaginal microbiota of healthy Canadian women through the menstrual cycle. Microbiome 2:23. http://dx.doi.org/10.1186/2049-2618-2-23.