Vitamin D induces innate antibacterial responses in human trophoblasts via an intracrine pathway 1

Biology of Reproduction

Volumn 80, Issue 3, 2009, Pages 398-406

  Liu, N ^a   Kaplan, A T ^b   Low, J ^b   Nguyen, L ^a   Liu, G Y ^a,b   Equils, O ^b   Hewison, M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Immunology; Placenta; Steroid hormones; Trophoblast; Vitamin D

Indexed keywords

25 HYDROXYVITAMIN D; CALCITRIOL; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; DRUG VEHICLE;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL INFECTION; CELL CULTURE; CONTROLLED STUDY; ESCHERICHIA COLI; HUMAN; HUMAN CELL; HUMAN TISSUE; INNATE IMMUNITY; MACROPHAGE; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; TROPHOBLAST;

25-HYDROXYVITAMIN D3 1-ALPHA-HYDROXYLASE; ANTIMICROBIAL CATIONIC PEPTIDES; CELL DEATH; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; HUMANS; MACROPHAGES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; TROPHOBLASTS; VITAMIN D;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 62149136595     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.073577     Document Type: Article

References (63)

1. Adams JS, Hewison M. Unexpected actions of vitamin D: new perspectives on the regulation of innate and adaptive immunity. Nat Clin Pract Endocrinol Metab 2008; 4:80-90.
2. White JH. Vitamin D signaling, infectious diseases and regulation of innate immunity. Infect Immun 2008; 76:3837-3843.
3. Tavera-Mendoza LE, White JH. Cell defenses and the sunshine vitamin. Sci Am 2007; 297:62-65, 68-70, 72.
4. Hewison M. Vitamin D and innate immunity. Curr Opin lnvestig Drugs 2008; 9:485-490.
5. Liu FT, Stenger S, Tang DH, Modlin RL. Cutting Edge: Vitamin D-mediated human antimicrobial activity against Mycobacterium tuberculosis is dependent on the induction of cathelicidin. J Immunol 2007; 179: 2060-2063.
6. Wang TT, Nestel FP, Bourdeau V, Nagai Y, Wang Q, Liao J, Tavera-Mendoza L, Lin R, Hanrahan JW, Mader S, White JH. Cutting edge: 1,25-dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression. J Immunol 2004; 173:2909-2912.
7. Gombart AF, Borregaard N, Koeffler HP. 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 2005; 19:1067-1077.
8. Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik SR, Ochoa MT, Schauber J, Wu K, Meinken C, Kamen DL, Wagner M, et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 2006; 311:1770-1773.
9. Schauber J, Dorschner RA, Coda AB, Buchau AS, Liu PT, Kiken D, Helfrich YR, Kang S, Elalieh HZ, Steinmeyer A, Zugel U, Bikle DD, et al. Injury enhances TLR2 function and antimicrobial peptide expression through a vitamin D-dependent mechanism. J Clin Invest 2007; 117:803-811.
10. Yim S, Dhawan P, Ragunath C, Christakos S, Diamond G. Induction of cathelicidin in normal and CF bronchial epithelial cells by 1,25- dihydroxyvitamin D3. J Cyst Fibres 2007; 6:403-410.
11. Martineau AR, Wilkinson KA, Newton SM, Floto RA, Norman AW, Skolimowska K, Davidson RN, Sorensen OE, Kampmann B, Griffiths CJ, Wilkinson RJ. IFN-gamma- and TNF-independent vitamin D-inducible human suppression of mycobacteria: the role of cathelicidin LL-37. J Immunol 2007; 178:7190-7198.
12. Ouhara K, Komatsuzawa H, Kawai T, Nishi H, Fujiwara T, Fujiue Y, Kuwabara M, Sayama K, Hashimoto K, Sugai M. Increased resistance to cationic antimicrobial peptide LL-37 in methicillin-resistant strains of Staphylococcus aureus. J Antimicrob Chemother 2008; 61:1266-1269.
13. Komatsuzawa H, Ouhara K, Yamada S, Fujiwara T, Sayama K, Hashimoto K, Sugai M. Innate defences against methicillin-resistant Staphylococcus aureus (MRSA) infection. J Pathol 2006; 208:249-260.
14. Midorikawa K, Ouhara K, Komatsuzawa H, Kawai T, Yamada S, Fujiwara T, Yamazaki K, Sayama K, Taubman MA, Kurihara H, Hashimoto K, Sugai M. Staphylococcus aureus susceptibility to innate antimicrobial peptides, beta-defensins and CAP18, expressed by human keratinocytes. Infect Immun 2003; 71:3730-3739.
15. Howell MD, Jones JF, Kisich KO, Streib JE, Gallo RL, Leung DY. Selective killing of vaccinia virus by LL-37: implications for eczema vaccinatum. J Immunol 2004; 172:1763-1767.
16. Bergman P, Walter-Jallow L, Broliden K, Agerberth B, Soderlund J. The antimicrobial peptide LL-37 inhibits HIV-1 replication. Curr HIV Res 2007; 5:410-415.
17. Steinstraesser L, Tippler B, Mertens J, Lamme E, Homann HH, Lehnhardt M, Wildner O, Steinau HU, Liberia K. Inhibition of early steps in the lentiviral replication cycle by cathelicidin host defense peptides. Retrovirology 2005; 2:2.
18. Mookherjee N, Rehaume LM, Hancock RE. Cathelicidins and functional analogues as antisepsis molecules. Expert Opin Ther Targets 2007: 11: 993-1004.
19. Wehkamp J, Schmid M, Stange EF. Defensins and other antimicrobial peptides in inflammatory bowel disease. Curr Opin Gastroenterol 2007; 23:370-378.
20. Hiemstra PS. Defensins and cathelicidins in inflammatory lung disease: beyond antimicrobial activity. Biochem Soc Trans 2006; 34:276-278.
21. Bland R, Zehnder D, Hewison M. Expression of 25-hydroxyvitamin D3-1 alpha-hydroxylase along the nephron: new insights into renal vitamin D metabolism. Curr Opin Nephrol Hypertens 2000; 9:17-22.
22. Zehnder D, Bland R, Walker EA, Bradwell AR, Howie AJ, Hewison M, Stewart PM. Expression of 25-hydroxyvitamin D3-1 alpha-hydroxylase in the human kidney. J Am Soc Nephrol 1999; 10:2465-2473.
23. Hewison M, Burke F, Evans KN, Lammas DA, Sansom DM, Liu P, Modlin RL, Adams JS. Extra-renal 25-hydroxyvitamin D3-1 alphahydroxylase in human health and disease. J Steroid Biochem Mol Biol 2007; 103:316-321.
24. Townsend K, Evans KN, Campbell MJ, Colston KW, Adams JS, Hewison M. Biological actions of extra-renal 25-hydroxyvitamin D-l alphahydroxylase and implications for chemoprevention and treatment. J Steroid Biochem Mol Biol 2005; 97:103-109.
25. Evans KN, Nguyen L, Chan J, Innes BA, Bulmer JN, Kilby MD, Hewison M. Effects of 25-Hydroxyvitamin D3 and 1,25-dihydroxyvitamin D3 on cytokine production by human decidual cells. Biol Reprod 2006: 75:816-822.
26. Gray TK, Lester GE, Lorenc RS. Evidence for extra-renal 1 alphahydroxylation of 25-hydroxyvitamin D3 in pregnancy. Science 1979; 204: 1311-1313.
27. Weisman Y, Harell A, Edelstein S, David M, Spirer Z, Golander A. 1 alpha, 25-Dihydroxyvitamin D3 and 24,25-dihydroxyvitamin D3 in vitro synthesis by human decidua and placenta. Nature 1979; 281:317-319.
28. Zehnder D, Evans KN, Kilby MD, Bulmer JN, Innes BA, Stewart PM, Hewison M. The ontogeny of 25-hydroxyvitamin D(3) 1 alpha-hydroxylase expression in human placenta and decidua. Am J Pathol 2002; 161: 105-114
29. Evans KN, Bulmer JN, Kilby MD, Hewison M. Vitamin D and placentaldecidual function. J Soc Gynecol lnvestig 2004; 11:263-271.
30. Guleria I, Pollard JW. The trophoblast is a component of the innate immune system during pregnancy. Nat Med 2000; 6:589-593.
31. Abrahams VM, Bole-Aldo P, Kim YM, Straszewski-Chavez SL, Chaiworapongsa T, Romero R, Mor G. Divergent trophoblast responses to bacterial products mediated by TLRs. J Immunol 2004; 173:4286-4296.
32. Evans KN, Taylor H, Zehnder D, Kilby MD, Bulmer JN, Sha F, Adams JS, Hewison M. Increased expression of 25-hydroxyvitamin D-lalphahydroxylase in dysgerminomas; a novel form of humoral hypercalcemia of malignancy. Am J Pathol 2004; 165:807-813.
33. Kaplan A, Chung K, Kocak H, Bertolotto C, Uh A, Hobel CJ, Simmons CF, Doran K, Liu GY, Equils O. Group B streptococcus induces trophoblast death. Microb Pathog 2008; 45:231-235.
34. Zehnder D, Bland R, Williams MC, McNinch RW, Howie AJ, Stewart PM, Hewison M. Extrarenal expression of 25-hydroxyvitamin D(3)-l alpha-hydroxylase. J Clin Endocrinol Metab 2001; 86:888-894.
35. Vanhooke JL, Prahl JM, Kimmel-Jehan C, Mendelsohn M, Danielson EW, Healy KD, Deluca HF. CYP27B1 null mice with LacZreporter gene display no 25-hydroxyvitamin D3-l{alpha}-hydroxylase promoter activity in the skin. Proc Natl Acad Sci U S A 2006; 103:75-80.
36. Kovacs CS, Kronenberg HM. Maternal-fetal calcium and bone metabolism during pregnancy, puerperium, and lactation. Endocr Rev 1997; 18: 832-872.
37. Kovacs CS, Woodland ML, Fudge NJ, Friel JK. The vitamin D receptor is not required for fetal mineral homeostasis or for the regulation of placental calcium transfer in mice. Am J Physiol Endocrinol Metab 2005; 289: E133-E144.
38. Rebut-Bonneton C, Demignon J. Effects of 1,25-dihydroxyvitamin D3 on in vitro lymphocyte reactions: arguments for a role at the maternofetal interface. Gynecol Obstet Invest 1991; 32:134-138.
39. King AE, Kelly RW, Sallenave JM, Bocking AD, Challis JR. Innate immune defences in the human uterus during pregnancy. Placenta 2007; 28:1099-1106.
40. King AE, Paltoo A, Kelly RW, Sallenave JM, Bocking AD, Challis JR. Expression of natural antimicrobials by human placenta and fetal membranes. Placenta 2007; 28:161-169.
41. Koga K, Mor G. Expression and function of Toll-like receptors at the maternal-fetal interface. Reprod Sci 2008; 15:231-242.
42. King AE, Critchley HO, Kelly RW. Presence of secretory leukocyte protease inhibitor in human endometrium and first trimester decidua suggests an antibacterial protective role. Mol Hum Reprod 2000: 6:191-196.
43. Amarante-Paffaro A, Queiroz GS, Correa ST, Spira B, Bevilacqua E. Phagocytosis as a potential mechanism for microbial defense of mouse placental trophoblast cells. Reproduction 2004; 128:207-218.
44. Svinarich DM, Wolf NA, Gomez R, Gonik B, Romero R. Detection of human defensin 5 in reproductive tissues. Am J Obstet Gynecol 1997; 176:470-475.
45. Riding GA, Jones A, Holland MK, Hill JR, Lehnert SA. Proteomic analysis of bovine conceptus fluids during early pregnancy. Proteomics 2008; 8:160-177.
46. Tomasinsig L, Zanetti M. The cathelicidins-structure, function and evolution. Curr Protein Pept Sci 2005; 6:23-34.
47. Risso A. Leukocyte antimicrobial peptides: multifunctional effector molecules of innate immunity. J Leukoc Biol 2000; 68:785-792.
48. Faure E, Thomas L, Xu H, Medvedev A, Equils O, Arditi M. Bacterial lipopolysaccharide and IFN-gamma induce Toll-like receptor 2 and Tolllike receptor 4 expression in human endothelial cells: role of NF-kappa B activation. J Immunol 2001; 166:2018-2024.
49. Nomura F, Akashi S, Sakao Y, Sato S, Kawai T, Matsumoto M, Nakanishi K, Kimoto M, Miyake K, Takeda K, Akira S. Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with downregulation of surface toll-like receptor 4 expression. J Immunol 2000; 164:3476-3479.
50. Zehnder D, Hewison M. The renal function of 25-hydroxyvitamin D3-1 alpha-hydroxylase. Mol Cell Endocrinol 1999; 151:213-220.
51. Ren S, Nguyen L, Wu S, Encinas C, Adams JS, Hewison M. Alternative splicing of vitamin D-24-hydroxylase: a novel mechanism for the regulation of extrarenal 1,25-dihydroxyvitamin D synthesis. J Biol Chem 2005;280:20604-20611.
52. Nizet V, Ohtake T, Lauth X, Trowbridge J, Rudisill J, Dorschner RA, Pestonjamasp V, Piraino J, Huttner K, Gallo RL. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 2001; 414:454-457.
53. Gutsmann T, Larrick JW, Seydel U, Wiese A. Molecular mechanisms of interaction of rabbit CAP 18 with outer membranes of Gram-negative bacteria. Biochemistry 1999; 38:13643-13653.
54. Larsen JW, Sever JL. Group B Streptococcus and pregnancy: a review. Am J Obstet Gynecol 2008; 198:440-448; discussion, 448-450.
55. Winn HN. Group B streptococcus infection in pregnancy. Clin Perinatol 2007; 34:387-392.
56. Jones AL, Mertz RH, Carl DJ, Rubens CE. A streptococcal penicillinbinding protein is critical for resisting innate airway defenses in the neonatal lung. J Immunol 2007; 179:3196-3202.
57. Barlow PG, Li Y, Wilkinson TS, Bowdish DM, Lau YE, Cosseau C, Haslett C, Simpson AJ, Hancock RE, Davidson DJ. The human cationic host defense peptide LL-37 mediates contrasting effects on apoptotic pathways in different primary cells of the innate immune system. J Leukoc Biol 2006; 80:509-520.
58. Gan H, Lee J, Ren F, Chen M, Kornfeld H, Remold HG. Mycobacterium tuberculosis blocks crosslinking of annexin-1 and apoptotic envelope formation on infected macrophages to maintain virulence. Nat Immunol 2008;9:1189-1197.
59. Kai-Larsen Y, Agerberth B. The role of the multifunctional peptide LL-37 in host defense. Front Biosci 2008; 13:3760-3767.
60. Zanetti M. Cathelicidins, multifunctional peptides of the innate immunity. J Leukoc Biol 2004; 75:39-48.
61. Koczulla R, von Degenfeld G, Kupatt C, Krotz F, Zahler S, Gloe T, Issbrucker K, Unterberger P, Zaiou M, Lebherz C, Karl A, Raake P, et al. An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J Clin Invest 2003; 111:1665-1672.
62. Kaneider NC, Djanani A, Wiedermann CJ. Heparan sulfate proteoglycaninvolving immunomodulation by cathelicidin antimicrobial peptides LL-37 and PR-39. ScientificWorldJournal 2007; 7:1832-1838.
63. Bodnar LM, Simhan HN, Powers RW, Frank MP, Cooperstein E, Roberts JM. High prevalence of vitamin D insufficiency in black and white pregnant women residing in the northern United States and their neonates. J Nutr 2007; 137:447-452.