Innate immune mediator profiles and their regulation in a novel polarized immortalized epithelial cell model derived from human endocervix

Journal of Reproductive Immunology

Volumn 92, Issue 1-2, 2011, Pages 8-20

  Buckner, Lyndsey R ^a   Schust, Danny J ^b   Ding, Jian ^c   Nagamatsu, Takeshi ^b   Beatty, Wandy ^d   Chang, Theresa L ^c   Greene, Sheila J ^a   Lewis, Maria E ^a   Ruiz, Bernardo ^a   Holman, Stacey L ^a   Spagnuolo, Rae Ann ^e   Pyles, Richard B ^e   Quayle, Alison J ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b University of Missouri   (United States)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Anti microbial peptide; Cytokine; Female genital tract; Hormone

Indexed keywords

ESTRADIOL; MUCIN 5B; POLYINOSINIC POLYCYTIDYLIC ACID; POLYPEPTIDE ANTIBIOTIC AGENT; TAMOXIFEN;

ARTICLE; CELL IMMORTALIZATION; CELL MEMBRANE; CELL STIMULATION; CELL STRAIN A2EN; CONTROLLED STUDY; CYTOKINE RELEASE; EPITHELIUM CELL; EXPLANT; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREGULATION; IN VITRO STUDY; INNATE IMMUNITY; MUCUS SECRETION; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; UTERINE ENDOCERVIX;

ANTIMICROBIAL CATIONIC PEPTIDES; CELL LINE, TRANSFORMED; CELL POLARITY; CERVIX UTERI; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GONORRHEA; HUMANS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; MUCIN-5B; NEISSERIA GONORRHOEAE; POLY I-C; TOLL-LIKE RECEPTOR 3;

EID: 81555198357     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2011.08.002     Document Type: Article

References (75)

1. Abrahams V.M., Schaefer T.M., Fahey J.V., Visintin I., Wright J.A., Aldo P.B., et al. Expression and secretion of antiviral factors by trophoblast cells following stimulation by the TLR-3 agonist, Poly(I:C). Hum. Reprod. 2006, 21:2432-2439.
2. Anderson D.J., Pudney J., Schust D.J. Caveats associated with the use of human cervical tissue for HIV and microbicide research. AIDS 2010, 24:1-4.
3. Beagley K.W., Gockel C.M. Regulation of innate and adaptive immunity by the female sex hormones oestradiol and progesterone. FEMS Immunol. Med. Microbiol. 2003, 38:13-22.
4. Beatty W.L. Trafficking from CD63-positive late endocytic multivesicular bodies is essential for intracellular development of Chlamydia trachomatis. J. Cell Sci. 2006, 119:350-359.
5. Belinson J.L., Hu S., Niyazi M., Pretorius R.G., Wang H., Wen C., et al. Prevalence of type-specific human papillomavirus in endocervical, upper and lower vaginal, perineal and vaginal self-collected specimens: implications for vaginal self-collection. Int. J. Cancer 2010, 127:1151-1157.
6. Bergman P., Johansson L., Asp V., Plant L., Gudmundsson G.H., Jonsson A.B., et al. Neisseria gonorrhoeae downregulates expression of the human antimicrobial peptide LL-37. Cell. Microbiol. 2005, 7:1009-1017.
7. Brunham R.C., Paavonen J., Stevens C.E., Kiviat N., Kuo C.C., Critchlow C.W., et al. Mucopurulent cervicitis--the ignored counterpart in women of urethritis in men. N Engl J Med 1984, 311:1-6.
8. Bryant D.M., Mostov K.E. From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell Biol. 2008, 9:887-901.
9. Ding J., Chou Y.Y., Chang T.L. Defensins in viral infections. J. Innate. Immun. 2009, 1:413-420.
10. Espinosa M., Noe G., Troncoso C., Ho S.B., Villalon M. Acidic pH and increasing [Ca(2+)] reduce the swelling of mucins in primary cultures of human cervical cells. Hum. Reprod. 2002, 17:1964-1972.
11. Fahey J.V., Schaefer T.M., Channon J.Y., Wira C.R. Secretion of cytokines and chemokines by polarized human epithelial cells from the female reproductive tract. Hum. Reprod. 2005, 20:1439-1446.
12. Fahey J.V., Wright J.A., Shen L., Smith J.M., Ghosh M., Rossoll R.M., et al. Estradiol selectively regulates innate immune function by polarized human uterine epithelial cells in culture. Mucosal Immunol. 2008, 1:317-325.
13. Falk L., Fredlund H., Jensen J.S. Signs and symptoms of urethritis and cervicitis among women with or without Mycoplasma genitalium or Chlamydia trachomatis infection. Sex. Transm. Infect. 2005, 81:73-78.
14. Fichorova R.N., Anderson D.J. Differential expression of immunobiological mediators by immortalized human cervical and vaginal epithelial cells. Biol. Reprod. 1999, 60:508-514.
15. Ganz T. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 2003, 3:710-720.
16. Gipson I.K. Human endocervical mucins. Ernst Schering Res. Found. Workshop 2005, 219-244.
17. Gipson I.K., Spurr-Michaud S., Moccia R., Zhan Q., Toribara N., Ho S.B., et al. MUC4 and MUC5B transcripts are the prevalent mucin messenger ribonucleic acids of the human endocervix. Biol. Reprod. 1999, 60:58-64.
18. Gipson I.K., Moccia R., Spurr-Michaud S., Argueso P., Gargiulo A.R., Hill J.A., et al. The amount of MUC5B mucin in cervical mucus peaks at midcycle. J. Clin. Endocrinol. Metab. 2001, 86:594-600.
19. Guinan M.E., MacCalman J., Kern E.R., Overall J.C., Spruance S.L. The course of untreated recurrent genital herpes simplex infection in 27 women. N. Engl. J. Med. 1981, 304:759-763.
20. Guseva N.V., Dessus-Babus S.C., Whittimore J.D., Moore C.G., Wyrick P.B. Characterization of estrogen-responsive epithelial cell lines and their infectivity by genital Chlamydia trachomatis. Microbes Infect. 2005, 7:1469-1481.
21. Guseva N.V., Knight S.T., Whittimore J.D., Wyrick P.B. Primary cultures of female swine genital epithelial cells in vitro: a new approach for the study of hormonal modulation of Chlamydia infection. Infect. Immun. 2003, 71:4700-4710.
22. Haase A.T. Targeting early infection to prevent HIV-1 mucosal transmission. Nature 2010, 464:217-223.
23. Haase A.T. Early events in sexual transmission of HIV and SIV and opportunities for interventions. Annu. Rev. Med. 2011, 62:127-139.
24. Halldorsson S., Asgrimsson V., Axelsson I., Gudmundsson G.H., Steinarsdottir M., Baldursson O., et al. Differentiation potential of a basal epithelial cell line established from human bronchial explant. In Vitro Cell. Dev. Biol. Anim. 2007, 43:283-289.
25. Hein M., Valore E.V., Helmig R.B., Uldbjerg N., Ganz T. Antimicrobial factors in the cervical mucus plug. Am. J. Obstet. Gynecol. 2002, 187:137-144.
26. Hennings H., Michael D., Cheng C., Steinert P., Holbrook K., Yuspa S.H. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell 1980, 19:245-254.
27. Herbst-Kralovetz M.M., Quayle A.J., Ficarra M., Greene S., Rose W.A., Chesson R., et al. Quantification and comparison of toll-like receptor expression and responsiveness in primary and immortalized human female lower genital tract epithelia. Am. J. Reprod. Immunol. 2008, 59:212-224.
28. Hickey D.K., Patel M.V., Fahey J.V., Wira C.R. 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. 2011, 88:185-194.
29. Hladik F., Hope T.J. HIV infection of the genital mucosa in women. Curr. HIV/AIDS Rep. 2009, 6:20-28.
30. Hombach-Klonisch S., Kehlen A., Fowler P.A., Huppertz B., Jugert J.F., Bischoff G., et al. Regulation of functional steroid receptors and ligand-induced responses in telomerase-immortalized human endometrial epithelial cells. J. Mol. Endocrinol. 2005, 34:517-534.
31. Hughes G.C., Thomas S., Li C., Kaja M.K., Clark E.A. Cutting edge: progesterone regulates IFN-alpha production by plasmacytoid dendritic cells. J Immunol 2008, 180:2029-2033.
32. Isaka K., Nishi H., Sagawa Y., Nakada T., Osakabe Y., Serizawa H., et al. Establishment of a new human cell line (EN) with TP53 mutation derived from endometrial carcinoma. Cancer Genet. Cytogenet. 2003, 141:20-25.
33. Joly S., Compton L.M., Pujol C., Kurago Z.B., Guthmiller J.M. Loss of human beta-defensin 1, 2, and 3 expression in oral squamous cell carcinoma. Oral Microbiol. Immunol. 2009, 24:353-360.
34. Kaushic C., Roth K.L., Anipindi V., Xiu F. Increased prevalence of sexually transmitted viral infections in women: the role of female sex hormones in regulating susceptibility and immune responses. J. Reprod. Immunol. 2011, 88:204-209.
35. Kayisli U.A., Mahutte N.G., Arici A. Uterine chemokines in reproductive physiology and pathology. Am. J. Reprod. Immunol. 2002, 47:213-221.
36. Klein T.J., Mlodzik M. Planar cell polarization: an emerging model points in the right direction. Annu. Rev. Cell Dev. Biol. 2005, 21:155-176.
37. Klotman M.E., Rapista A., Teleshova N., Micsenyi A., Jarvis G.A., Lu W., et al. Neisseria gonorrhoeae-induced human defensins 5 and 6 increase HIV infectivity: role in enhanced transmission. J. Immunol. 2008, 180:6176-6185.
38. Kohlgraf K.G., Pingel L.C., Dietrich D.E., Brogden K.A. Defensins as anti-inflammatory compounds and mucosal adjuvants. Future Microbiol. 2010, 5:99-113.
39. Lea R.G., Sandra O. Immunoendocrine aspects of endometrial function and implantation. Reproduction 2007, 134:389-404.
40. Li Q., Estes J.D., Schlievert P.M., Duan L., Brosnahan A.J., Southern P.J., et al. Glycerol monolaurate prevents mucosal SIV transmission. Nature 2009, 458:1034-1038.
41. Lieberman J.A., Moscicki A.B., Sumerel J.L., Ma Y., Scott M.E. Determination of cytokine protein levels in cervical mucus samples from young women by a multiplex immunoassay method and assessment of correlates. Clin. Vaccine Immunol. 2008, 15:49-54.
42. MacDonald E.M., Savoy A., Gillgrass A., Fernandez S., Smieja M., Rosenthal K.L., et al. Susceptibility of human female primary genital epithelial cells to herpes simplex virus, type-2 and the effect of TLR3 ligand and sex hormones on infection. Biol. Reprod. 2007, 77:1049-1059.
43. Maslow A.S., Davis C.H., Choong J., Wyrick P.B. Estrogen enhances attachment of Chlamydia trachomatis to human endometrial epithelial cells in vitro. Am. J. Obstet. Gynecol. 1988, 159:1006-1014.
44. Miyaura H., Iwata M. Direct and indirect inhibition of Th1 development by progesterone and glucocorticoids. J. Immunol. 2002, 168:1087-1094.
45. Mo B., Vendrov A.E., Palomino W.A., DuPont B.R., Apparao K.B., Lessey B.A. ECC-1 cells: a well-differentiated steroid-responsive endometrial cell line with characteristics of luminal epithelium. Biol. Reprod. 2006, 75:387-394.
46. Moriyama A., Shimoya K., Ogata I., Kimura T., Nakamura T., Wada H., et al. Secretory leukocyte protease inhibitor (SLPI) concentrations in cervical mucus of women with normal menstrual cycle. Mol. Hum. Reprod. 1999, 5:656-661.
47. Ng A.B., Reagan J.W., Yen S.S. Herpes genitalis; clinical and cytopathologic experience with 256 patients. Obstet. Gynecol. 1970, 36:645-651.
48. Nussey S.S., Whitehead S.A. Ovarian control and the menstrual cycle. Endocrinology, An Integrated Approach 2001, 255-261. BIOS Scientific Publishers Ltd., Oxford, UK. S.S. Nussey, S.A. Whitehead (Eds.).
49. Ochiel D.O., Fahey J.V., Ghosh M., Haddad S.N., Wira C.R. Innate immunity in the female reproductive tract: role of sex hormones in regulating uterine epithelial cell protection against pathogens. Curr. Womens Health Rev. 2008, 4:102-117.
50. Porter E., Yang H., Yavagal S., Preza G.C., Murillo O., Lima H., et al. Distinct defensin profiles in Neisseria gonorrhoeae and Chlamydia trachomatis urethritis reveal novel epithelial cell-neutrophil interactions. Infect. Immun. 2005, 73:4823-4833.
51. Quayle A.J. The innate and early immune response to pathogen challenge in the female genital tract and the pivotal role of epithelial cells. J. Reprod. Immunol. 2002, 57:61-79.
52. Quayle A.J., Porter E.M., Nussbaum A.A., Wang Y.M., Brabec C., Yip K.P., et al. Gene expression, immunolocalization, and secretion of human defensin-5 in human female reproductive tract. Am. J. Pathol. 1998, 152:1247-1258.
53. Rasmussen S.J., Eckmann L., Quayle A.J., Shen L., Zhang Y.X., Anderson D.J., et al. Secretion of proinflammatory cytokines by epithelial cells in response to Chlamydia infection suggests a central role for epithelial cells in chlamydial pathogenesis. J. Clin. Invest. 1997, 99:77-87.
54. Redfern R.L., Reins R.Y., McDermott A.M. Toll-like receptor activation modulates antimicrobial peptide expression by ocular surface cells. Exp. Eye Res. 2011, 92:209-220.
55. Rivas-Santiago B., Hernandez-Pando R., Carranza C., Juarez E., Contreras J.L., Aguilar-Leon D., et al. Expression of cathelicidin LL-37 during Mycobacterium tuberculosis infection in human alveolar macrophages, monocytes, neutrophils, and epithelial cells. Infect. Immun. 2008, 76:935-941.
56. Schaefer T.M., Fahey J.V., Wright J.A., Wira C.R. Innate immunity in the human female reproductive tract: antiviral response of uterine epithelial cells to the TLR3 agonist poly(I:C). J. Immunol. 2005, 174:992-1002.
57. Shacklett B.L. Cell-mediated immunity to HIV in the female reproductive tract. J. Reprod. Immunol. 2009, 83:190-195.
58. Simhan H.N., Caritis S.N., Krohn M.A., Martinez de Tejada B., Landers D.V., Hillier S.L. Decreased cervical proinflammatory cytokines permit subsequent upper genital tract infection during pregnancy. Am. J. Obstet. Gynecol. 2003, 189:560-567.
59. Soler C., Allibert P., Chardonnet Y., Cros P., Mandrand B., Thivolet J. Detection of human papillomavirus types 6, 11, 16 and 18 in mucosal and cutaneous lesions by the multiplex polymerase chain reaction. J Virol Methods 1991, 35:143-157.
60. Stephens R.S. The cellular paradigm of chlamydial pathogenesis. Trends Microbiol. 2003, 11:44-51.
61. Su L., Sun Y., Ma F., Lu P., Huang H., Zhou J. Progesterone inhibits Toll-like receptor 4-mediated innate immune response in macrophages by suppressing NF-kappaB activation and enhancing SOCS1 expression. Immunol. Lett. 2009, 125:151-155.
62. Svinarich D.M., Wolf N.A., Gomez R., Gonik B., Romero R. Detection of human defensin 5 in reproductive tissues. Am. J. Obstet. Gynecol. 1997, 176:470-475.
63. Sweet R.L., Blankfort-Doyle M., Robbie M.O., Schacter J. The occurrence of chlamydial and gonococcal salpingitis during the menstrual cycle. JAMA 1986, 255:2062-2064.
64. Valore E.V., Park C.H., Quayle A.J., Wiles K.R., McCray P.B., Ganz T. Human beta-defensin-1: an antimicrobial peptide of urogenital tissues. J. Clin. Invest. 1998, 101:1633-1642.
65. Wang J., Frohlich K.J., Buckner L., Quayle A.J., Luo M., Feng X., et al. Altered protein secretion of Chlamydia trachomatis in persistently infected human endocervical epithelial cells. Microbiology 2011, Jul 7 (Epub ahead of print). 10.1099/mic.0.044917-0.
66. Wehkamp J., Schauber J., Stange E.F. Defensins and cathelicidins in gastrointestinal infections. Curr. Opin. Gastroenterol. 2007, 23:32-38.
67. Wira C.R., Fahey J.V., Ghosh M., Patel M.V., Hickey D.K., Ochiel D.O. Sex hormone regulation of innate immunity in the female reproductive tract: the role of epithelial cells in balancing reproductive potential with protection against sexually transmitted pathogens. Am. J. Reprod. Immunol. 2010, 63(6):544-565.
68. Wira C.R., Ghosh M., Smith J.M., Shen L., Connor R.I., Sundstrom P., et al. Epithelial cell secretions from the human female reproductive tract inhibit sexually transmitted pathogens and Candida albicans but not Lactobacillus. Mucosal Immunol. 2011, 4:335-342.
69. Wira C.R., Patel M.V., Ghosh M., Mukura L., Fahey J.V. 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. 2011, 65:196-211.
70. Wiszniewski L., Jornot L., Dudez T., Pagano A., Rochat T., Lacroix J.S., et al. Long-term cultures of polarized airway epithelial cells from patients with cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 2006, 34:39-48.
71. Wyrick P. Polarized epithelial cell culture for Chlamydia trachomatis. Chlamydia Genomics and Pathogenesis 2006, 323-338. Horizon Bioscience, Norfolk, UK. P. Wyrick, P. Bavoil (Eds.).
72. Yuan J.S., Reed A., Chen F., Stewart C.N. Statistical analysis of real-time PCR data. BMC Bioinformatics 2006, 7:85.
73. Zapata W., Rodriguez B., Weber J., Estrada H., Quinones-Mateu M.E., Zimermman P.A., et al. Increased levels of human beta-defensins mRNA in sexually HIV-1 exposed but uninfected individuals. Curr. HIV Res. 2008, 6:531-538.
74. Zhang Z., Schuler T., Zupancic M., Wietgrefe S., Staskus K.A., Reimann K.A., et al. Sexual transmission and propagation of SIV and HIV in resting and activated CD4+ T cells. Science 1999, 286:1353-1357.
75. Zhu Y., Maric J., Nilsson M., Brannstrom M., Janson P.O., Sundfeldt K. Formation and barrier function of tight junctions in human ovarian surface epithelium. Biol. Reprod. 2004, 71:53-59.