Exosomes, endogenous retroviruses and toll-like receptors: Pregnancy recognition in ewes

Reproduction

Volumn 149, Issue 3, 2015, Pages 281-291

  Ruiz González, Irene ^a   Xu, Jing ^a   Wang, Xiaoqiu ^a   Burghardt, Robert C ^a   Dunlap, Kathrin A ^a   Bazer, Fuller W ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; CALNEXIN; CD14 ANTIGEN; CD68 ANTIGEN; ENJSRV PROTEIN; HEAT SHOCK COGNATE PROTEIN 70; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 6; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 10; INTERLEUKIN 1BETA; JAAGSIEKTE SHEEP RETROVIRUS PROTEIN; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; VIRAL PROTEIN; CYTOKINE;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOMESTIC SHEEP; ENDOGENOUS RETROVIRUS; ENDOMETRIUM; ESTRUS CYCLE; EXOSOME; FEMALE; FIRST TRIMESTER PREGNANCY; GENE EXPRESSION; IN VITRO STUDY; MEMBRANE MICROPARTICLE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PREGNANCY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; UTERUS CAVITY; ANIMAL; BREEDING; GENETICS; METABOLISM; NIDATION; PHYSIOLOGY; SHEEP; UTERUS;

ANIMALS; CYTOKINES; EMBRYO IMPLANTATION; ENDOGENOUS RETROVIRUSES; ENDOMETRIUM; EXOSOMES; FEMALE; PREGNANCY; PREGNANCY, ANIMAL; SHEEP; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; UTERUS;

EID: 84936944314     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-14-0538     Document Type: Article

References (57)

1. Akira S, Uematsu S & Takeuchi O 2006 Pathogen recognition and innate immunity. Cell 124 783-801. (doi:10.1016/j.cell.2006.02.015)
2. Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, Koo GC & Calderwood SK 2000 HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nature Medicine 64 35-442.
3. Asea A, Rehli M, Kabingu E, Boch JA, Bare O, Auron PE, Stevenson MA & Calderwood SK 2002 Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. Journal of Biological Chemistry 277 15028-15034. (doi:10.1074/jbc. M200497200)
4. Asselin-Paturel C & Trinchieri G 2005 Production of type I interferons: plasmacytoid dendritic cells and beyond. Journal of Experimental Medicine 202 461-465. (doi:10.1084/jem.20051395)
5. Bailey CM & Hendrix MJC 2008 IRF6 in development and disease: a mediator of quiescence and differentiation. Cell Cycle 7 1925-1930. (doi:10.4161/cc.7.13.6221)
6. Baumann CL, Aspalter IM, Sharif O, Pichlmair A, Blüml S, Grebien F, Bruckner M, Pasierbek P, Aumayr K, Planyavsky M et al. 2010 CD14 is a coreceptor of toll-like receptors 7 and 9. Journal of Experimental Medicine 207 2689-2701. (doi:10.1084/jem.20101111)
7. Bazer FW, Burghardt RC, Johnson GA, Spencer TE & Wu G 2008 Interferons and progesterone for establishment and maintenance of pregnancy: interactions among novel cell signaling pathways. Reproductive Biology 8 179-211. (doi:10.1016/S1642-431X(12)60012-6)
8. Biggs LC, Naridze RL, DeMali KA, Lusche DF, Kuhl S, Soll DR, Schutte BC & DunnwaldM2014 Interferon regulatory factor 6 regulates keratinocyte migration. Journal of Cell Science 127 2840-2848. (doi:10.1242/jcs. 139246)
9. Black SG, Arnaud F, Burghardt RC, Satterfield MC, Fleming JA, Long CR, Hanna C, Murphy L, Biek R, Palmarini M et al. 2010 Viral particles of endogenous betaretroviruses are released in the sheep uterus and infect the conceptus trophectoderm in a transspecies embryo transfer model. Journal of Virology 84 9078-9085. (doi:10.1128/JVI.00950-10)
10. Blasius AL & Beutler B 2010 Intracellular toll-like receptors. Immunity 32 305-315. (doi:10.1016/j.immuni.2010.03.012)
11. Burns G, Brooks K, Wildung M, Navakanitworakul R, Christenson LK & Spencer TE 2014 Extracellular vesicles in luminal fluid of the ovine uterus. PLoS ONE 9 e90913. (doi:10.1371/journal.pone.0090913)
12. Chen YC, Wang SY & King CC 1999 Bacterial lipopolysaccharide inhibits dengue virus infection of primary human monocytes/macrophages by blockade of virus entry via a CD14-dependent mechanism. Journal of Virology 73 2650-2657.
13. Diebold SS, Kaisho T, Hemmi H, Akira S & Reis e Sousa C 2004 Innate antiviral responses by means of TLR7-mediated recognition of singlestranded RNA. Science 303 1529-1531. (doi:10.1126/science.1093616)
14. Dreux M, Garaigorta U, Boyd B, Décembre E, Chung J, Whitten-Bauer C, Wieland S & Chisari FV 2012 Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host & Microbe 12 558-570. (doi:10.1016/j.chom.2012. 08.010)
15. Dunlap KA, Palmarini M, Adelson DL & Spencer TE 2005 Sheep endogenous betaretroviruses (enJSRVs) at the hyaluronidase2 (HYAL2) receptor in the ovine uterus and conceptus. Biology of Reproduction 73 271-279. (doi:10.1095/biolreprod.105.039776)
16. Dunlap KA, Palmarini M, Varela M, Burghardt RC, Hayashi K, Farmer JL & Spencer TE 2006 Endogenous retroviruses regulate periimplantation placental growth and differentiation. PNAS 103 14390-14395. (doi:10. 1073/pnas.0603836103)
17. Farmer JL, Burghardt RC, Jousan FD, Hansen PJ, Bazer FW & Spencer TE 2008 Galectin 15 (LGALS15) functions in trophectoderm migration and attachment. FASEB Journal 22 548-560. (doi:10.1096/fj.07-9308com)
18. Février B & Raposo G 2004 Exosomes: endosomal-derived vesicles shipping extracellular messages. Current Opinion in Cell Biology 16 415-421.
19. Fleming JA, Song G, Choi Y, Spencer TE & Bazer FW 2009 Interferon regulatory factor 6 (IRF6) is expressed in the ovine uterus and functions as a transcriptional activator. Molecular and Cellular Endocrinology 299 252-260. (doi:10.1016/j.mce.2008.10.025)
20. González-Navajas JM, Lee J, David M & Raz E 2012 Immunomodulatory functions of type I interferons. Nature Reviews. Immunology 12 125-135.
21. Gray CA, Abbey CA, Beremand PD, Choi Y, Farmer JL, Adelson DL, Thomas TL, Bazer FW & Spencer TE 2006 Identification of endometrial genes regulated by early pregnancy, progesterone, and interferon tau in the ovine uterus. Biology of Reproduction 74 383-394. (doi:10.1095/biolreprod.105.046656)
22. György B, Szabó TG, Pásztoi M, Pál Z, Misják P, Aradi B, László V, Pállinger E, Pap E, Kittel A et al. 2011 Membrane vesicles, current stateof-the-art: emerging role of extracellular vesicles. Cellular and Molecular Life Sciences 68 2667-2688.
23. Hannafon BN & Ding WQ 2013 Intercellular communication by exosomederived microRNAs in cancer. International Journal of Molecular Sciences 14 14240-14269. (doi:10.3390/ijms140714240)
24. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, Mizutani T, Shimada N, Ohba Y, Takaoka A, Yoshida N et al. 2005 IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434 772-777. (doi:10.1038/nature03464)
25. Ito T, Wang YH & Liu YJ 2005 Plasmacytoid dendritic cell precursors/type I interferon producing-cells sense viral infection by toll-like receptor (TLR) 7 and TLR9. Springer Seminars in Immunopathology 26 221-229. (doi:10.1007/s00281-004-0180-4)
26. Johnson GA, Spencer TE, Burghardt RC & Bazer FW 1999 Ovine osteopontin: I. Cloning and expression of mRNA in the uterus during periimplantation period. Biology of Reproduction 61 884-891. (doi:10. 1095/biolreprod61.4.884)
27. Kim MY & Oglesbee M 2012 Virus-heat shock protein interaction and a novel axis for innate antiviral immunity. Cells 1 646-666. (doi:10.3390/cells1030646)
28. Kumar H, Kawai T & Akira S 2009 Toll-like receptors and innate immunity. Biochemical and Biophysical Research Communications 388 621-625. (doi:10.1016/j.bbrc.2009.08.062)
29. Kurt-Jones EA, Popova L, Kwinn L, Haynes LM, Jones LP, Tripp RA, Walsh EE, Freeman MW, Golenbock DT, Anderson LJ et al. 2000 Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nature Immunology 1 398-401. (doi:10.1038/80833)
30. Leiser R & Kaufmann P 1994 Placental structure: in a comparative aspect. Experimental and Clinical Endocrinology 102 122-134. (doi:10.1055/s-0029-1211275)
31. Lotvall J & Valadi H 2007 Cell to cell signalling via exosomes through esRNA. Cell Adhesion Migration 1 156-158.
32. Lyons-Weiler J, Watkins SC & Morelli AE 2012 Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119 756-766. (doi:10.1182/blood-2011-02-338004)
33. Macklon NS, Geraedts JP & Fauser BC 2002 Conception to ongoing pregnancy: the "black box" of early pregnancy loss. Human Reproduction Update 8 333-343. (doi:10.1093/humupd/8.4.333)
34. Mansouri-Attia N, Oliveira LJ, Forde N, Fahey AG, Browne JA, Roche JF, Sandra O, Reinaud P, Lonergan P & Fair T 2012 Pivotal role for monocytes/macrophages and dendritic cells in maternal immune response to the developing embryo in cattle. Biology of Reproduction 87 123. (doi:10.1095/biolreprod.112.101121)
35. Masciopinto F, Giovani C, Campagnoli S, Galli-Stampino L, Colombatto P, Brunetto M, Yen TSB, Houghton M, Pileri P & Abrignani S 2004 Association of hepatitis C virus envelope proteins with exosomes. European Journal of Immunology 34 2834-2842. (doi:10.1002/eji. 200424887)
36. Meckes DG Jr & Raab-Traub N 2011 Microvesicles and viral infection. Journal of Virology 85 12844-12854. (doi:10.1128/JVI.05853-11)
37. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan ML, Karlsson JM, Baty CJ, Gibson GA, Erdos G, Wang Z et al. 2012 Mechanism of transfer of functional micro RNAs between mouse dendritic cells via exosomes. Blood 119 756-766. (doi:10.1182/blood-2011-02-338004)
38. Morelli AE, Larregina AT, Shufesky WJ, SullivanML, Stolz DB, PapworthGD, Zahorchak AF, Logar AJ, Wang Z, Watkins SC et al. 2004 Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 104 3257-3266. (doi:10.1182/blood-2004-03-0824)
39. Ng YH, Rome S, Jalabert A, Forterre A, Singh H, Hincks CS & Salamonsen LA 2013 Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. PLoS ONE 8 e58502. (doi:10.1371/journal.pone. 0058502)
40. Nguyen DG, Booth A, Gould SJ & Hildreth JE 2003 Evidence that HIV budding in primarymacrophages occurs through the exosome release pathway. Journal of Biological Chemistry 278 52347-52354. (doi:10.1074/jbc.M309009200)
41. Oliveira LJ, Barreto RS, Perecin F, Mansouri-Attia N, Pereira FT & Meirelles FV 2012 Modulation of maternal immune system during pregnancy in the cow. Reproduction in Domestic Animals 47 384-393. (doi:10.1111/j.1439-0531.2012.02102.x)
42. Palmarini M, Gray CA, Carpenter K, Fan H, Bazer FW & Spencer TE 2001 Expression of endogenous betaretroviruses in the ovine uterus: effects of neonatal age, estrous cycle, pregnancy, and progesterone. Journal of Virology 75 11319-11327. (doi:10.1128/JVI.75.23.11319-11327.2001)
43. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, de Grujil TD, Würdinger T & Middeldorp JM 2010 Functional delivery of viral miRNAs via exosomes. PNAS 107 6328-6333. (doi:10.1073/pnas.0914843107)
44. Racicot K, Schmitt A & Ott T 2012 The myxovirus-resistance protein, MX1, is a component of exosomes secreted by uterine epithelial cells. American Journal of Reproductive Immunology 67 498-505. (doi:10. 1111/j.1600-0897.2012.01109.x)
45. Ramprasad MP, Terpstra V, Kondratenko N, Quehenberger O & Steinberg D 1996 Cell surface expression of mouse macrosialin and human CD68 and their role as macrophage receptors for oxidized low density lipoprotein. PNAS 93 14833-14838. (doi:10.1073/pnas.93.25.14833)
46. Raspotnig G, Fauler G, Jantscher A, Windischhofer W, Schachl K & Leis HJ 1999 Colorimetric determination of cell numbers by Janus green staining. Analytical Biochemistry 275 74-83. (doi:10.1006/abio.1999.4309)
47. Reynolds LP & Redmer DA 2001 Angiogenesis in the placenta. Biology of Reproduction 64 1033-1040. (doi:10.1095/biolreprod64.4.1033)
48. da Silveira JC, Veeramachaneni DN, Winger QA, Carnevale EM & Bouma GJ 2012 Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible form of cell communication within the ovarian follicle. Biology of Reproduction 86 71. (doi:10.1095/biolreprod.111.093252)
49. Simpson RJ, Jensen SS & Lim JW 2008 Proteomic profiling of exosomes: current perspectives. Proteomics 8 4083-4099. (doi:10.1002/pmic. 200800109)
50. Spencer TE & Bazer FW 1995 Temporal and spatial alterations in uterine estrogen receptor and progesterone receptor gene expression during the estrous cycle and early pregnancy in the ewe. Biology of Reproduction 53 1527-1543. (doi:10.1095/biolreprod53.6.1527)
51. Spencer TE & Bazer FW 2004 Conceptus signals for establishment and maintenance of pregnancy. Reproductive Biology and Endocrinology 5 2-49. (doi:10.1095/biolreprod.103.024133)
52. Spencer TE, Bartol FF, Bazer FW, Johnson GA & Joyce MM 1999 Identification and characterization of glycosilation-dependent cell adhesion molecule 1-like protein expression in the ovine uterus. Biology of Reproduction 60 241-250. (doi:10.1095/biolreprod60.2.241)
53. Spencer TE, Johnson GA, Bazer FW & Burghardt RC 2004 Implantation mechanisms: insights from the sheep. Reproduction 128 657-668. (doi:10.1530/rep.1.00398)
54. Trinchieri G 2010 Type I interferon: friend or foe? Journal of Experimental Medicine 207 2053-2063. (doi:10.1084/jem.20101664)
55. Vlassov AV, Magdaleno S, Setterquist R & Conrad R 2012 Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochimica et Biophysica Acta 1820 940-948. (doi:10.1016/j.bbagen.2012.03.017)
56. Wang R, Town T, Gokarn V, Flavell RA & Chandawarkar RY 2006 HSP70 enhances macrophage phagocytosis by interaction with lipid raftassociated TLR-7 and upregulating p38 MAPK and PI3K pathways. Journal of Surgical Research 136 58-69. (doi:10.1016/j.jss.2006.06.003)
57. Wooding FB 1992 Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta 13 101-113. (doi:10.1016/0143-4004(92)90025-O)