Transcriptional response of the bovine endometrium and embryo to endometrial polymorphonuclear neutrophil infiltration as an indicator of subclinical inflammation of the uterine environment

Reproduction, Fertility and Development

Volumn 24, Issue 6, 2012, Pages 778-793

  Hoelker, Michael ^a   Salilew Wondim, Dessie ^a   Drillich, Marc ^b,e   Christine, Grosse Brinkhaus ^a   Ghanem, Nasser ^c   Goetze, Leopold ^d   Tesfaye, Dawit ^a   Schellander, Karl ^a   Heuwieser, Wolfgang ^b  

^a UNIVERSITY OF BONN   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c CAIRO UNIVERSITY   (Egypt)

^d PFIZER INC   (United States)

^e Clinic for Ruminants   (Austria)

Author keywords

cytobrush; gene expression; PMN; subclinical endometritis

Indexed keywords

TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLASTOCYST; CELL ADHESION; CELL CYCLE; CONTROLLED STUDY; CYTODIAGNOSIS; ENDOMETRITIS; ENDOMETRIUM; ESTRUS CYCLE; FEMALE; GENE EXPRESSION; GENETIC REGULATION; HEALTH STATUS; IMMUNOMODULATION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; NUCLEOTIDE SEQUENCE; SYSTEMATIC REVIEW;

ANIMALS; BLASTOCYST; CATTLE; CATTLE DISEASES; DAIRYING; ENDOMETRITIS; ENDOMETRIUM; ESTROUS CYCLE; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; INSEMINATION, ARTIFICIAL; NEUTROPHIL INFILTRATION; PREGNANCY; PUERPERAL DISORDERS; RNA, MESSENGER; SUPEROVULATION; TIME FACTORS; TRANSCRIPTION, GENETIC;

BOVINAE;

EID: 84863792092     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD11171     Document Type: Article

References (66)

1. Allen, M. P., and Nilsen-Hamilton, M. (1998). Granzymes D, E, F and G are regulated through pregnancy and by IL-2 and IL-15 in granulated metrial gland cells. J. Immunol. 16, 2772-2779.
2. Aumais, J. P., Williams, S. N., Luo, W., Nishino, M., Caldwell, K. A., Caldwell, G. A., Lin, S. H., and Yu-Lee, L. Y. (2003). Role for NudC, a dynein-associated nuclear movement protein, in mitosis and cytokinesis. J. Cell Sci. 116, 1991-2003. doi:10.1242/JCS.00412
3. Bade, B., Boettcher, H. E., Lohrmann, J., Hink-Schauer, C., Bratke, K., Jenne, D. E., Virchow, J. C., and Luttmann, W. (2005). Differential expression of the granzymes A, K and M and perforin in human peripheral blood lymphocytes. Int. Immunol. 17, 1419-1428. doi:10.1093/INTIMM/DXH320
4. Barlund, C. S., Carruthers, T. D., Waldner, C. L., and Palmer, C. W. (2008). A comparison of diagnostic techniques for postpartum endometritis in dairy cattle. Theriogenology 69, 714-723. doi:10.1016/J.THERIOGEN OLOGY.2007.12.005
5. Bauersachs, S., Mitko, K., Ulbrich, S. E., Blum, H., and Wolf, E. (2008). Transcriptome studies of bovine endometrium reveal molecular profiles characteristic for specific stages of estrous cycle and early pregnancy. Exp. Clin. Endocrinol. Diabetes 116, 371-384. doi:10.1055/S-2008- 1076714
6. Bauersachs, S., Ulbrich, S. E., Zakhartchenko, V., Minten, M., Reichenbach, M., Reichenbach, H. D., Blum, H., Spencer, T. E., and Wolf, E. (2009). The endometrium responds differently to cloned versus fertilized embryos. Proc. Natl Acad. Sci. USA 106, 5681-5686. doi:10.1073/ PNAS.0811841106
7. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Rev. Stat. 57, 289-300.
8. Bennett, V., and Baines, A. J. (2001). Spectrin and ankyrin-based pathways: Metazoan inventions for integrating cells into tissues. Physiol. Rev. 81, 1353-1392.
9. Cai, T. Q., Weston, P. G., Lund, L. A., Brodie, B., McKenna, D. J., and Wagner, W. C. (1994). Association between neutrophil functions and periparturient disorders in cows. Am. J. Vet. Res. 55, 934-943.
10. Chapwanya, A., Meade, K. G., Doherty, M. L., Callanan, J. J., Mee, J. F., and O'Farrelly, C. (2009). Histopathological and molecular evaluation of Holstein-Friesian cows postpartum: Toward an improved understanding of uterine innate immunity. Theriogenology 71, 1396-1407. doi:10.1016/J.THERIOGENOLOGY. 2009.01.006
11. Chitu, V., Ferguson, P. J., de Bruijn, R., Schlueter, A. J., Ochoa, L. A., Waldschmidt, T. J., Yeung, Y. G., and Stanley, E. R. (2009). Primed innate immunity leads to autoinflammatory disease in PSTPIP2- deficient cmo mice. Blood 114, 2497-2505. doi:10.1182/BLOOD- 2009-02-204925
12. Chowdhury, R., Bois, P. R., Feingold, E., Sherman, S. L., and Cheung, V. G. (2009). Genetic analysis of variation in human meiotic recombination. PLoS Genet. 5, e1000648. doi:10.1371/JOURNAL.PGEN.1000648
13. Connon, C. J., Yamasaki, K., Kawasaki, S., Quantock, A. J., Koizumi, N., and Kinoshita, S. (2004). Calcium-activated chloride channel-2 in human epithelia. J. Histochem. Cytochem. 52, 415-418. doi:10.1177/ 002215540405200313
14. Dahia, C. L., and Rao, A. J. (2006). Regulation of FSH receptor, PKIbeta, IL-6 and calcium mobilization: Possible mediators of differential action of FSH. Mol. Cell. Endocrinol. 247, 73-81. doi:10.1016/J.MCE.2005. 10.029
15. Dunne, L. D., Diskin, M. G., and Sreenan, J. M. (2000). Embryo and foetal loss in beef heifers between Day 14 of gestation and full term. Anim. Reprod. Sci. 58, 39-44. doi:10.1016/S0378-4320(99)00088-3
16. Etherington, W. G., Martin, S. W., Dohoo, I. R., and Bosu, W. T. (1985). Interrelationships between postpartum events, hormonal therapy, reproductive abnormalities and reproductive performance in dairy cows: A path analysis. Can. J. Comp. Med. 49, 261-267.
17. Falcon, S., and Gentleman, R. (2007). Using GOstats to test gene lists for GO term association. Bioinformatics 23, 257-258. doi:10.1093/ BIOINFORMATICS/BTL567
18. Farin, P. W., and Farin, C. E. (1995). Transfer of bovine embryos produced in vivo or in vitro: Survival and fetal development. Biol. Reprod. 52, 676-682. doi:10.1095/BIOLREPROD52.3.676
19. Forde, N., Spencer, T. E., Bazer, F. W., Song, G., Roche, J. F., and Lonergan, P. (2010). Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium. Physiol. Genomics 41, 53-62. doi:10.1152/ PHYSIOLGENOMICS.00162. 2009
20. Forde, N., Beltman, M. E., Duffy, G. B., Duffy, P., Mehta, J. P., O'Gaora, P., Roche, J. F., Lonergan, P., and Crowe, M. A. (2011). Changes in the endometrial transcriptome during the bovine estrous cycle: Effect of low circulating progesterone and consequences for conceptus elongation. Biol. Reprod. 84, 266-278. doi:10.1095/BIOLREPROD.110.085910
21. Gabler, C., Drillich, M., Fischer, C., Holder, C., Heuwieser, W., and Einspanier, R. (2009). Endometrial expression of selected transcripts involved in prostaglandin synthesis in cows with endometritis. Theriogenology 71, 993-1004. doi:10.1016/J.THERIOGENOLOGY.2008. 11.009
22. Gad, A., Besenfelder, U., Rings, F., Ghanem, N., Salilew-Wondim, D., Hossain, M. M., Tesfaye, D., Lonergan, P., Becker, A., Cinar, U., Schellander, K., Havlicek, V., and Hölker, M. (2011). Effect of reproductive tract environment following controlled ovarian hyperstimulation treatment on embryo development and global transcriptome profile of blastocysts: Implications for animal breeding and human assisted reproduction. Hum. Reprod. 26, 1693-1707. doi:10.1093/HUMREP/DER110
23. Gilbert, R. O., Shin, S. T., Guard, C. L., Erb, H. N., and Frajblat, M. (2005). Prevalence of endometritis and its effects on reproductive performance of dairy cows. Theriogenology 64, 1879-1888. doi:10.1016/J.THERIO GENOLOGY.2005.04.022
24. Grosse, J., Chitu, V., Marquardt, A., Hanke, P., Schmittwolf, C., Zeitlmann, L., Schropp, P., Barth, B., Yu, P., Paffenholz, R., Stumm, G., Nehls, M., and Stanley, E. R. (2006). Mutation of mouse Mayp/Pstpip2 causes a macrophage autoinflammatory disease. Blood 107, 3350-3358. doi:10.1182/BLOOD- 2005-09-3556
25. Hameed, A., Lowrey, D. M., Lichtenheld, M., and Podack, E. R. (1988). Characterization of three serine esterases isolated from human IL-2 activated killer cells. J. Immunol. 144, 3142-3147.
26. Hammon, D. S., Evjen, I. M., Dhiman, T. R., Goff, J. P., and Walters, J. L. (2006). Neutrophil function and energy status in Holstein cows with uterine health disorders. Vet. Immunol. Immunopathol. 113, 21-29. doi:10.1016/J.VETIMM. 2006.03.022
27. Herath, S., Lilly, S. T., Santos, N. R., Gilbert, R. O., Goetze, L., Bryant, C. E., White, J. O., Cronin, J., and Sheldon, I. M. (2009). Expression of genes associated with immunity in the endometrium of cattle with disparate postpartum uterine disease and fertility. Reprod. Biol. Endocrinol. 7, 55. doi:10.1186/1477-7827-7-55
28. Hoedemaker, M., Lund, L. A., and Wagner, W. C. (1992). Function of neutrophils and chemoattractant properties of fetal placental tissue during the last month of pregnancy in cows. Am. J. Vet. Res. 53, 1524-1529.
29. Jauniaux, E., Watson, A. L., Hempstock, J., Bao, Y. P., Skepper, J. N., and Burton, G. J. (2000). Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am. J. Pathol. 157, 2111-2122. doi:10.1016/S0002-9440(10)64849-3
30. Kamon, H., Kawabe, T., Kitamura, H., Lee, J., Kamimura, D., Kaisho, T., Akira, S., Iwamatsu, A., Koga, H., Murakami, M., and Hirano, T. (2006). TRIF-GEFH1-RhoB pathway is involved in MHCII expression on dendritic cells that is critical for CD4 T-cell activation. EMBO J. 25, 4108-4119. doi:10.1038/SJ.EMBOJ.7601286
31. Kane, M. T., Morgan, P. M., and Coonan, C. (1997). Peptide growth factors and preimplantation development. Hum. Reprod. Update 3, 137-157. doi:10.1093/HUMUPD/3.2.137
32. Kasimanickam, R., Duffield, T. F., Foster, R. A., Gartley, C. J., Leslie, K. E., Walton, J. S., and Johnson, W. H. (2004). Endometrial cytology and ultrasonography for the detection of subclinical endometritis in postpartum dairy cows. Theriogenology 62, 9-23. doi:10.1016/ J.THERIOGENOLOGY.2003.03.001
33. Kasimanickam, R., Duffield, T. F., Foster, R. A., Gartley, C. J., Leslie, K. E., Walton, J. S., and Johnson, W. H. (2005). The effect of a single administration of cephapirin or cloprostenol on the reproductive performance of dairy cows with subclinical endometritis. Theriogenology 63, 818-830. doi:10.1016/J.THERIOGENOLOGY. 2004.05.002
34. Kasimanickam, R., Cornwell, J. M., and Nebel, R. L. (2006). Effect of presence of clinical and subclinical endometritis at the initiation of Presynch-Ovsynch program on the first service pregnancy in dairy cows. Anim. Reprod. Sci. 95, 214-223. doi:10.1016/J.ANIREPROSCI.2005. 10.007
35. Kaufmann, T. B., Drillich, M., Tenhagen, B. A., Forderung, D., and Heuwieser, W. (2009). Prevalence of bovine subclinical endometritis 4h after insemination and its effects on first service conception rate. Theriogenology 71, 385-391. doi:10.1016/J.THERIOGENOLOGY. 2008.08.005
36. Kim, I. H., and Kang, H. G. (2003). Risk factors for postpartum endometritis and the effect of endometritis on reproductive performance in dairy cows in Korea. J. Reprod. Dev. 49, 485-491. doi:10.1262/JRD.49.485
37. Kuhlman, P. A., Hughes, C. A., Bennett, V., and Fowler, V. M. (1996). A new function for adducing. calcium/calmodulin-regulated capping of the barbed ends of actin filaments. J. Biol. Chem. 271, 7986-7991.
38. Kurschus, F. C., Bruno, R., Fellows, E., Falk, C. S., and Jenne, D. E. (2005). Membrane receptors are not required to deliver granzymeB during killer cell attack. Blood 105, 2049-2058. doi:10.1182/BLOOD-2004-06-2180
39. LeBlanc, S. J., Duffield, T. F., Leslie, K. E., Bateman, K. G., Keefe, G. P., Walton, J. S., and Johnson, W. H. (2002). Defining and diagnosing postpartum clinical endometritis and its impact on reproductive performance in dairy cows. J. Dairy Sci. 85, 2223-2236. doi:10.3168/JDS. S0022-0302(02)74302-6
40. Lincke, A., Drillich, M., and Heuwieser, W. (2007). Subclinical endometritis in dairy cattle and its effect on fertility: A review of recent publications. Berl. Munch. Tierarztl. Wochenschr. 120, 245-250. [In German]
41. Lowin, B., Hahne, B., Mattmann, C., and Tschopp, J. (1994). Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways. Nature 370, 650-652. doi:10.1038/370650A0
42. Lucy, M. C. (2001). Reproductive loss in high-producing dairy cattle: where will it end? J. Dairy Sci. 84, 1277-1293. doi:10.3168/JDS.S0022-0302 (01)70158-0
43. Mansouri-Attia, N., Aubert, J., Reinaud, P., Giraud-Delville, C., Taghouti, G., Galio, L., Everts, R. E., Degrelle, S., Richard, C., Hue, I., Yang, X., Tian, X. C., Lewin, H. A., Renard, J. P., and Sandra, O. (2009a). Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. Physiol. Genomics 39, 14-27. doi:10.1152/ PHYSIOLGENOMICS.90404. 2008
44. Mansouri-Attia, N., Sandra, O., Aubert, J., Degrelle, S., Everts, R. E., Giraud-Delville, C., Heyman, Y., Galio, L., Hue, I., Yang, X., Tian, X. C., Lewin, H. A., and Renard, J. P. (2009b). Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc. Natl Acad. Sci. USA 106, 5687-5692. doi:10.1073/PNAS.0812722106
45. Mateus, L., Lopes, D. C., Carvalho, H., Serra, P., and Robalo, S. J. (2002). Blood and intrauterine leukocyte profile and function in dairy cows that spontaneously recovered from postpartum endometritis. Reprod. Domest. Anim. 37, 176-180. doi:10.1046/J.1439-0531.2002.00351.X
46. Matsuoka, Y., Li, X., and Bennett, V. (2000). Adducin: Structure, function and regulation. Cell. Mol. Life Sci. 57, 884-895. doi:10.1007/ PL00000731
47. Mitko, K., Ulbrich, S. E., Wenigerkind, H., Sinowatz, F., Blum, H., Wolf, E., and Bauersachs, S. (2008). Dynamic changes in messengerRNAprofiles of bovine endometrium during the oestrous cycle. Reproduction 135, 225-240. doi:10.1530/REP-07-0415
48. Mitra, P., Vaughan, P. S., Stein, J. L., Stein, G. S., and Wijnen, A. J. (2001). Purification and functional analysis of a novel leucine-zipper/ nucleotide-fold protein, BZAP45, stimulatin cell cycle regulated histone H4 gene transcription. Biochemistry 40, 10693-10699. doi:10.1021/ BI010529O
49. Norimine, J., and Brown, W. C. (2005). Intrahaplotype and interhaplotype pairing of bovine leukocyte antigen DQA and DQB molecules generate functional DQ molecules important for priming CD4(+) T-lymphocyte responses. Immunogenetics 57, 750-762. doi:10.1007/S00251-005- 0045-6
50. Paisley, L. G., Mickelsen, W. D., and Anderson, P. B. (1986). Mechanisms and therapy for retained fetal membranes and uterine infections of cows: A review. Theriogenology 25, 353-381. doi:10.1016/0093-691X(86) 90045-2
51. Pieterse, M. C., Taverne, M. A., Kruip, T. A., and Willemse, A. H. (1990). Detection of corpora lutea and follicles in cows: A comparison of transvaginal ultrasonography and rectal palpation. Vet. Rec. 126, 552-554.
52. Saini, R. V., Wilson, C., Finn, M. W., Wang, T., Krensky, A. M., and Clayberger, C. (2011). Granulysin delivered by cytotoxic cells damages endoplasmatic reticulum and activates caspase-7 in target cells. J. Immunol. 186, 3497-3504. doi:10.4049/JIMMUNOL.1003409
53. Salilew-Wondim, D., Hölker, M., Rings, F., Ghanem, N., Ulas-Cinar, M., Peippo, J., Tholen, E., Looft, C., Schellander, K., and Tesfaye, D. (2010). Bovine pretransfer endometrium and embryo transcriptome fingerprints as predictors of pregnancy success after embryo transfer. Physiol. Genomics 42, 201-218. doi:10.1152/PHYSIOLGENOMICS.00047. 2010
54. Sheldon, I. M., and Dobson, H. (2004). Postpartum uterine health in cattle. Anim. Reprod. Sci. 82-83, 295-306. doi:10.1016/J.ANIREPROSCI. 2004.04.006
55. Sheldon, I. M., Lewis, G. S., LeBlanc, S., and Gilbert, R. O. (2006). Defining postpartum uterine disease in cattle. Theriogenology 65, 1516-1530. doi:10.1016/J.THERIOGENOLOGY.2005.08.021
56. Shimizu, T., Krebs, S., Bauersachs, S., Blum, H., Wolf, E., and Miyamoto, A. (2010). Actions and interactions of progesterone and estrogen on transcriptome profiles of the bovine endometrium. Physiol. Genomics 42A, 290-300. doi:10.1152/PHYSIOLGENOMICS.00107.2010
57. Smyth, G. K. (2005). Limma: Linear models for microarray data. In 'Bioinformatics and Computational Biology Solutions using R and Bioconductor'. (Eds R. Gentleman, V. Carey, S. Dudoit, R. Irizarry and W. Huber.) pp. 397-420. (Springer: New York.)
58. Spencer, T. E., Becker, W. C., George, P., Mirando, M. A., Ogle, T. F., and Bazer, F. W. (1995). Ovine interferon-tau regulates expression of endometrial receptors for estrogen and oxytocin but not progesterone. Biol. Reprod. 53, 732-745. doi:10.1095/BIOLREPROD53.3.732
59. Tsai, T., Lin, W., Yang, S., Chen, W. T. K., Lee, M., Chong, K., and Chen, C. (2010). Granzyme G is expressed in the two-cell stage mouse embryo and is required for the maternal-zygotic transition. BMC Dev. Biol. 10, 88. doi:10.1186/1471-213X-10-88
60. Tsousis, G., Sharifi, A., and Hoedemaker, M. (2010). Increased risk of conception failure in German Holstein Friesian cows with chronic endometritis. Reprod. Domest. Anim. 45, 1114-1117. doi:10.1111/ J.1439-0531.2009.01481
61. X Wang, L. Q., and James, M. O. (2005). Sulfotransferase 2A1 forms estradiol- 17-sulfate and celecoxib switches the dominant product from estradiol- 3-sulfate to estradiol-17-sulfate. J. Steroid Biochem. Mol. Biol. 96, 367-374. doi:10.1016/J.JSBMB.2005.05.002
62. Wathes, D. C., Cheng, Z., Chowdhury, W., Fenwick, M. A., Fitzpatrick, R., Morris, D. G., Patton, J., and Murphy, J. J. (2009). Negative energy balance alters global gene expression and immune responses in the uterus of postpartum dairy cows. Physiol. Genomics 39, 1-13. doi:10.1152/PHYSIOLGENOMICS.00064.2009
63. Williams, E. J., Fischer, D. P., Pfeiffer, D. U., England, G. C., Noakes, D. E., Dobson, H., and Sheldon, I. M. (2005). Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology 63, 102-117. doi:10.1016/ J.THERIOGENOLOGY.2004.03.017
64. Williams, E. J., Fischer, D. P., Noakes, D. E., England, G. C., Rycroft, A., Dobson, H., and Sheldon, I. M. (2007). The relationship between uterine pathogen growth density and ovarian function in the postpartum dairy cow. Theriogenology 68, 549-559. doi:10.1016/ J.THERIOGENOLOGY.2007.04.056
65. Wira, C. R., and Fahey, J. V. (2004). The innate immune system: Gatekeeper to the female reproductive tract. Immunology 111, 13-15. doi:10.1111/ J.1365-2567.2004.01796.X
66. Zhu, W., Saddar, S., Seetharam, D., Chambliss, K. L., Longoria, C., Silver, D. L., Yuhanna, I. S., Shaul, P. W., and Mineo, C. (2008). The scavenger receptor Class B Type I adaptor protein PDZK1 maintains endothelial monolayer integrity. Circ. Res. 102, 480-487. doi:10.1161/CIRCRE SAHA.107.159079 www.publish.