Ovine trophoblasts express cathelicidin host defence peptide in response to infection

Journal of Reproductive Immunology

Volumn 117, Issue , 2016, Pages 10-16

  Coyle, Christopher ^a   Wheelhouse, Nick ^b   Jacques, Maxime ^a   Longbottom, David ^b   Svoboda, Pavel ^c   Pohl, Jan ^c   Duncan, W Colin ^d   Rae, Michael T ^a   Barlow, Peter G ^a  

^a EDINBURGH NAPIER UNIVERSITY   (United Kingdom)

^b MOREDUN RESEARCH INSTITUTE   (United Kingdom)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Antimicrobial peptide; Cathelicidin; Chlamydia related organisms; Defensin; Trophoblast; Waddlia

Indexed keywords

ANTIMICROBIAL PEPTIDE 29; BETA DEFENSIN 1; CALCITRIOL; CATHELICIDIN; LIPOPOLYSACCHARIDE; POLYPEPTIDE ANTIBIOTIC AGENT; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; CAP18 LIPOPOLYSACCHARIDE-BINDING PROTEIN; DEFENSIN; PLASMA PROTEIN; SECALCIFEROL; SMAP29 PROTEIN, OVIS ARIES;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHLAMYDIA; CONTROLLED STUDY; EMBRYO; FEMALE; HOST RESISTANCE; IN VITRO STUDY; INFECTION; NONHUMAN; PLACENTA TISSUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEEP; TROPHOBLAST; ANIMAL; BOVINE; CELL LINE; CHLAMYDIALES; GENE EXPRESSION REGULATION; GENETICS; GRAM NEGATIVE INFECTION; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; PLACENTA; PREGNANCY; SHEEP DISEASE; VETERINARY;

24,25-DIHYDROXYVITAMIN D 3; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BLOOD PROTEINS; CATHELICIDINS; CATTLE; CELL LINE; CHLAMYDIALES; DEFENSINS; FEMALE; GENE EXPRESSION REGULATION; GRAM-NEGATIVE BACTERIAL INFECTIONS; IMMUNITY, INNATE; LIPOPOLYSACCHARIDES; PLACENTA; PREGNANCY; SHEEP; SHEEP DISEASES; TROPHOBLASTS;

EID: 84976576694     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2016.06.006     Document Type: Article

References (36)

1. Abrahams, V.M., Visintin, I., Aldo, P.B., Guller, S., Romero, R., Mor, G., A role for TLRs in the regulation of immune cell migration by first trimester trophoblast cells. J. Immunol. 175 (2005), 8096–8104.
2. Barlow, P.G., Findlay, E.G., Currie, S.M., Davidson, D.J., Antiviral potential of cathelicidins. Future Microbiol. 9 (2014), 55–73.
3. Blumer, S., Greub, G., Waldvogel, A., Hassig, M., Thoma, R., Tschuor, A., Pospischil, A., Borel, N., Waddlia: Parachlamydia and Chlamydiaceae in bovine abortion. Vet. Microbiol. 152 (2011), 385–393.
4. Bowdish, D.M., Davidson, D.J., Hancock, R.E., Immunomodulatory properties of defensins and cathelicidins. Curr. Top. Microbiol. Immunol. 306 (2006), 27–66.
5. Brogden, K.A., Kalfa, V.C., Ackermann, M.R., Palmquist, D.E., Mccray, P.B. Jr., Tack, B.F., The ovine cathelicidin SMAP29 kills ovine respiratory pathogens in vitro and in an ovine model of pulmonary infection. Antimicrob. Agents Chemother. 45 (2001), 331–334.
6. Brogden, K.A., Ackermann, M., Mccray, P.B. Jr., Tack, B.F., Antimicrobial peptides in animals and their role in host defences. Int. J. Antimicrob. Agents 22 (2003), 465–478.
7. Chan, S.Y., Susarla, R., Canovas, D., Vasilopoulou, E., Ohizua, O., Mccabe, C.J., Hewison, M., Kilby, M.D., Vitamin D promotes human extravillous trophoblast invasion in vitro. Placenta 36 (2015), 403–409.
8. Entrican, G., Wattegedera, S., Wheelhouse, N., Allan, A., Rocchi, M., Immunological paradigms and the pathogenesis of ovine chlamydial abortion. Am. J. Reprod. Immunol. 64 (2010), 287–294.
9. Frohm Nilsson, M., Sandstedt, B., Sorensen, O., Weber, G., Borregaard, N., Stahle-Backdahl, M., The human cationic antimicrobial protein (hCAP18), a peptide antibiotic, is widely expressed in human squamous epithelia and colocalizes with interleukin-6. Infect. Immun. 67 (1999), 2561–2566.
10. Ganguly, D., Chamilos, G., Lande, R., Gregorio, J., Meller, S., Facchinetti, V., Homey, B., Barrat, F.J., Zal, T., Gilliet, M., Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J. Exp. Med. 206 (2009), 1983–1994.
11. Gombart, A.F., Borregaard, N., Koeffler, H.P., Human cathelicidin antimicrobial peptide (CAMP) gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by 1,25-dihydroxyvitamin D3. FASEB J. 19 (2005), 1067–1077.
12. Haldorson, G.J., Stanton, J.B., Mathison, B.A., Suarez, C.E., Baszler, T.V., Neospora caninum: antibodies directed against tachyzoite surface protein NcSRS2 inhibit parasite attachment and invasion of placental trophoblasts in vitro. Exp. Parasitol. 112 (2006), 172–178.
13. Horne, A.W., Stock, S.J., King, A.E., Innate immunity and disorders of the female reproductive tract. Reproduction 135 (2008), 739–749.
14. King, A.E., Fleming, D.C., Critchley, H.O., Kelly, R.W., Differential expression of the natural antimicrobials, beta-defensins 3 and 4, in human endometrium. J. Reprod. Immunol. 59 (2003), 1–16.
15. King, A.E., Kelly, R.W., Sallenave, J.M., Bocking, A.D., Challis, J.R., Innate immune defences in the human uterus during pregnancy. Placenta 28 (2007), 1099–1106.
16. King, A.E., Paltoo, A., Kelly, R.W., Sallenave, J.M., Bocking, A.D., Challis, J.R., Expression of natural antimicrobials by human placenta and fetal membranes. Placenta 28 (2007), 161–169.
17. Klaffenbach, D., Friedrich, D., Strick, R., Strissel, P.L., Beckmann, M.W., Rascher, W., Gessner, A., Dotsch, J., Meissner, U., Schnare, M., Contribution of different placental cells to the expression and stimulation of antimicrobial proteins (AMPs). Placenta 32 (2011), 830–837.
18. Koschwanez, M., Meli, M., Vogtlin, A., Greub, G., Sidler, X., Handke, M., Sydler, T., Kaiser, C., Pospischil, A., Borel, N., Chlamydiaceae family, Parachlamydia spp., and Waddlia spp. in porcine abortion. J. Vet. Diagn. Invest. 24 (2012), 833–839.
19. Lande, R., Gregorio, J., Facchinetti, V., Chatterjee, B., Wang, Y.H., Homey, B., Cao, W., Wang, Y.H., SU, B., Nestle, F.O., Zal, T., Mellman, I., Schroder, J.M., Liu, Y.J., Gilliet, M., Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 449 (2007), 564–569.
20. Levinson, P., Choi, R.Y., Cole, A.L., Hirbod, T., Rhedin, S., Payne, B., Guthrie, B.L., Bosire, R., Cole, A.M., Farquhar, C., Broliden, K., HIV-neutralizing activity of cationic polypeptides in cervicovaginal secretions of women in HIV-serodiscordant relationships. PLoS One, 7, 2012, e31996.
21. Liu, P.T., Stenger, S., Tang, D.H., Modlin, R.L., Cutting edge: vitamin D-mediated human antimicrobial activity against Mycobacterium tuberculosis is dependent on the induction of cathelicidin. J. Immunol. 179 (2007), 2060–2063.
22. Liu, N., Kaplan, A.T., Low, J., Nguyen, L., Liu, G.Y., Equils, O., Hewison, M., Vitamin D induces innate antibacterial responses in human trophoblasts via an intracrine pathway. Biol. Reprod. 80 (2009), 398–406.
23. Longbottom, D., Livingstone, M., Maley, S., Van Der Zon, A., Rocchi, M., Wilson, K., Wheelhouse, N., Dagleish, M., Aitchison, K., Wattegedera, S., Nath, M., Entrican, G., Buxton, D., Intranasal infection with Chlamydia abortus induces dose-dependent latency and abortion in sheep. PLoS One, 8, 2013, e57950.
24. Peschel, A., Sahl, H.G., The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol. 4 (2006), 529–536.
25. Rae, M., Grace, C., Hogg, K., Wilson, L.M., Mchaffie, S.L., Ramaswamy, S., Maccallum, J., Connolly, F., Mcneilly, A.S., Duncan, C., The pancreas is altered by in utero androgen exposure: implications for clinical conditions such as polycystic ovary syndrome (PCOS). PLoS One, 8, 2013, e56263.
26. Rietdijk, S.T., Burwell, T., Bertin, J., Coyle, A.J., Sensing intracellular pathogens-NOD-like receptors. Curr. Opin. Pharmacol. 8 (2008), 261–266.
27. Rurangirwa, F.R., Dilbeck, P.M., Crawford, T.B., Mcguire, T.C., Mcelwain, T.F., Analysis of the 16 S rRNA gene of micro-organism WSU 86–1044 from an aborted bovine foetus reveals that it is a member of the order Chlamydiales: proposal of Waddliaceae fam. nov. Waddlia chondrophila gen. nov., sp. nov. Int. J. Syst. Bacteriol. 49:Pt. 2 (1999), 577–581.
28. Sammin, D.J., Markey, B.K., Quinn, P.J., Mcelroy, M.C., Bassett, H.F., Comparison of fetal and maternal inflammatory responses in the ovine placenta after experimental infection with Chlamydophila abortus. J. Comp. Pathol. 135 (2006), 83–92.
29. Sato, E., Imafuku, S., Ishii, K., Itoh, R., Chou, B., Soejima, T., Nakayama, J., Hiromatsu, K., Vitamin D-dependent cathelicidin inhibits Mycobacterium marinum infection in human monocytic cells. J. Dermatol. Sci. 70 (2013), 166–172.
30. Skerlavaj, B., Benincasa, M., Risso, A., Zanetti, M., Gennaro, R., SMAP-29: a potent antibacterial and antifungal peptide from sheep leukocytes. FEBS Lett. 463 (1999), 58–62.
31. Storrie, S., Longbottom, D., Barlow, P.G., Wheelhouse, N., MAPK activation is essential for Waddlia chondrophila induced CXCL8 expression in human epithelial cells. PLoS One, 11, 2016, e0152193.
32. Wang, T.T., Nestel, F.P., Bourdeau, V., Nagai, Y., Wang, Q., Liao, J., Tavera-Mendoza, L., Lin, R., Hanrahan, J.W., Mader, S., White, J.H., Cutting edge: 1,25-dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression. J. Immunol. 173 (2004), 2909–2912.
33. Wheelhouse, N., Wattegedera, S., Stanton, J., Maley, S., Watson, D., Jepson, C., Deane, D., Buxton, D., Longbottom, D., Baszler, T., Entrican, G., Ovine trophoblast is a primary source of TNFalpha during Chlamydophila abortus infection. J. Reprod. Immunol. 80 (2009), 49–56.
34. Wheelhouse, N., Coyle, C., Barlow, P.G., Mitchell, S., Greub, G., Baszler, T., Rae, M.T., Longbottom, D., Waddlia chondrophila infects and multiplies in ovine trophoblast cells stimulating an inflammatory immune response. PLoS One, 9, 2014, e102386.
35. Yuk, J.M., Shin, D.M., Lee, H.M., Yang, C.S., Jin, H.S., Kim, K.K., Lee, Z.W., Lee, S.H., Kim, J.M., JO, E.K., Vitamin D3 induces autophagy in human monocytes/macrophages via cathelicidin. Cell Host Microbe 6 (2009), 231–243.
36. Zasloff, M., Antimicrobial peptides of multicellular organisms. Nature 415 (2002), 389–395.