Vacuolar-ATPase isoform a2 regulates macrophages and cytokine profile necessary for normal spermatogenesis in testis

Journal of Leukocyte Biology

Volumn 96, Issue 2, 2014, Pages 337-347

  Jaiswal, Mukesh K ^a   Katara, Gajendra K ^a   Mallers, Timothy ^a   Chaouat, Gerard ^b   Gilman Sachs, Alice ^a   Beaman, Kenneth D ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b SAINT LOUIS HOSPITAL   (France)

Author keywords

A2NTD; Nos2; Pregnancy loss; Tgf

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE A2; IMMUNOGLOBULIN G; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; LIF PROTEIN; MCP1 PROTEIN; PROTEIN; RANTES; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME RELEASE; FEMALE; IMMUNE RESPONSE; INNATE IMMUNITY; MACROPHAGE; MALE; MATING; MEIOSIS; MOUSE; NIDATION; NONHUMAN; PREGNANCY OUTCOME; PRIORITY JOURNAL; PROTEIN FUNCTION; SEXUAL BEHAVIOR; SPERMATOGENESIS; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; TESTIS; UPREGULATION;

A2NTD; NOS2; PREGNANCY LOSS; TGF-Β;

ANIMALS; CYTOKINES; FEMALE; MACROPHAGES; MALE; MICE; PLACENTA; PREGNANCY; SPERM MOTILITY; SPERMATOGENESIS; TESTIS; UP-REGULATION; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84904985811     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A1113-593RR     Document Type: Article

References (43)

1. Jaiswal, M. K., Mallers, T. M., Larsen, B., Kwak-Kim, J., Chaouat, G., Gilman-Sachs, A., Beaman, K. D. (2012) V-ATPase upregulation during early pregnancy: a possible link to establishment of an inflammatory response during preimplantation period of pregnancy. Reproduction 143, 713-725.
2. Jaiswal, M. K., Gilman-Sachs, A., Chaouat, G., Beaman, K. D. (2011) Placental ATPase expression is a link between multiple causes of spontaneous abortion in mice. Biol. Reprod. 85, 626-634.
3. Hedger, M. P. (2002) Macrophages and the immune responsiveness of the testis. J. Reprod. Immunol. 57, 19-34.
4. Kern, S., Robertson, S. A., Mau, V. J., Maddocks, S. (1995) Cytokine secretion by macrophages in the rat testis. Biol. Reprod. 53, 1407-1416.
5. Bergh, A., Damber, J. E., van Rooijen, N. (1993) Liposome-mediated macrophage depletion: an experimental approach to study the role of testicular macrophages in the rat. J. Endocrinol. 136, 407-413.
6. Pollard, J. W., Dominguez, M. G., Mocci, S., Cohen, P. E., Stanley, E. R. (1997) Effect of the colony-stimulating factor-1 null mutation, osteopetrotic (csfm(op), on the distribution of macrophages in the male mouse reproductive tract. Biol. Reprod. 56, 1290-1300.
7. Cohen, P. E., Chisholm, O., Arceci, R. J., Stanley, E. R., Pollard, J. W. (1996) Absence of colony-stimulating factor-1 in osteopetrotic (csfmop/csfmop) mice results in male fertility defects. Biol. Reprod. 55, 310-317.
8. Devroey, P., Fauser, B. C., Diedrich, K. (2009) Approaches to improve the diagnosis and management of infertility. Hum. Reprod. Update 15, 391-408.
9. Ota, K., Jaiswal, M. K., Ramu, S., Jeyendran, R., Kwak-Kim, J., Gilman-Sachs, A., Beaman, K. D. (2013) Expression of a2 vacuolar ATPase in spermatozoa is associated with semen quality and chemokine-cytokine profiles in infertile men. PLoS One 8, e70470.
10. Ntrivalas, E., Gilman-Sachs, A., Kwak-Kim, J., Beaman, K. (2007) The N-terminus domain of the a2 isoform of vacuolar ATPase can regulate interleukin-1β production from mononuclear cells in co-culture with JEG-3 choriocarcinoma cells. Am. J. Reprod. Immunol. 57, 201-209.
11. Sun-Wada, G. H., Imai-Senga, Y., Yamamoto, A., Murata, Y., Hirata, T., Wada, Y., Futai, M. (2002) A proton pump ATPase with testis-specific E1-subunit isoform required for acrosome acidification. J. Biol. Chem. 277, 18098-18105.
12. Sun, Z., Wada, T., Maemura, K., Uchikura, K., Hoshino, S., Diehl, A. M., Klein, A. S. (2003) Hepatic allograft-derived Kupffer cells regulate T cell response in rats. Liver Transpl. 9, 489-497.
13. Sun-Wada, G. H., Kamei, Y., Wada, Y., Futai, M. (2004) Regulatory elements directing gut expression of the GATA6 gene during mouse early development. J. Biochem. 135, 165-169.
14. Kwong, C., Gilman-Sachs, A., Beaman, K. (2011) Tumor-associated a2 vacuolar ATPase acts as a key mediator of cancer-related inflammation by inducing pro-tumorigenic properties in monocytes. J. Immunol. 186, 1781-1789.
15. Ntrivalas, E., Levine, R., Kwong, C., Gilman-Sachs, A., Beaman, K. (2010) The a2 isoform of vacuolar ATPase is a modulator of implantation and feto-maternal immune tolerance in early pregnancy. J. Reprod. Immunol. 85, 106-111.
16. Ntrivalas, E., Derks, R., Gilman-Sachs, A., Kwak-Kim, J., Levine, R., Beaman, K. (2007) Novel role for the N-terminus domain of the a2 isoform of vacuolar ATPase in interleukin-1β production. Hum. Immunol. 68, 469-477.
17. Katara, G. K., Jaiswal, M. K., Kulshrestha, A., Kolli, B., Gilman-Sachs, A., Beaman, K. D. (2013) Tumor-associated vacuolar ATPase subunit promotes tumorigenic characteristics in macrophages. Oncogene. doi: 10. 1038/onc. 2013. 532 [Epub ahead of print].
18. Cheng, C. Y., Wong, E. W., Yan, H. H., Mruk, D. D. (2010) Regulation of spermatogenesis in the microenvironment of the seminiferous epithelium: new insights and advances. Mol. Cell. Endocrinol. 315, 49-56.
19. Huleihel, M., Lunenfeld, E. (2004) Regulation of spermatogenesis by paracrine/autocrine testicular factors. Asian J. Androl. 6, 259-268.
20. O'Bryan, M. K., Hedger, M. P. (2008) Inflammatory networks in the control of spermatogenesis: chronic inflammation in an immunologically privileged tissue? Adv. Exp. Med. Biol. 636, 92-114.
21. Xia, W., Mruk, D. D., Lee, W. M., Cheng, C. Y. (2005) Cytokines and junction restructuring during spermatogenesis-a lesson to learn from the testis. Cytokine Growth Factor Rev. 16, 469-493.
22. Ribbing, S. L., Hoversland, R. C., Beaman, K. D. (1988) T-cell suppressor factors play an integral role in preventing fetal rejection. J. Reprod. Immunol. 14, 83-95.
23. Mei, H., Walters, C., Carter, R., Colledge, W. H. (2011) Gpr54-/-mice show more pronounced defects in spermatogenesis than Kiss1-/-mice and improved spermatogenesis with age when exposed to dietary phytoestrogens. Reproduction 141, 357-366.
24. Kopanja, D., Roy, N., Stoyanova, T., Hess, R. A., Bagchi, S., Raychaudhuri, P. (2011) Cul4A is essential for spermatogenesis and male fertility. Dev. Biol. 352, 278-287.
25. Wilson-Leedy, J. G., Ingermann, R. L. (2007) Development of a novel CASA system based on open source software for characterization of zebrafish sperm motility parameters. Theriogenology 67, 661-672.
26. Hedger, M. P., Robertson, D. M., de Kretser, D. M., Risbridger, G. P. (1990) The quantification of steroidogenesis-stimulating activity in testicular interstitial fluid by an in vitro bioassay employing adult rat Leydig cells. Endocrinology 127, 1967-1977.
27. Fujisaka, S., Usui, I., Bukhari, A., Ikutani, M., Oya, T., Kanatani, Y., Tsuneyama, K., Nagai, Y., Takatsu, K., Urakaze, M., Kobayashi, M., Tobe, K. (2009) Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes 58, 2574-2582.
28. Aron-Wisnewsky, J., Tordjman, J., Poitou, C., Darakhshan, F., Hugol, D., Basdevant, A., Aissat, A., Guerre-Millo, M., Clement, K. (2009) Human adipose tissue macrophages: M1 and M2 cell surface markers in subcutaneous and omental depots and after weight loss. J. Clin. Endocrinol. Metab. 94, 4619-4623.
29. Jaiswal, M. K., Agrawal, V., Mallers, T., Gilman-Sachs, A., Hirsch, E., Beaman, K. D. (2013) Regulation of apoptosis and innate immune stimuli in inflammation-induced preterm labor. J. Immunol. 191, 5702-5713.
30. Bryniarski, K., Szewczyk, K., Ptak, M., Bobek, M., Ptak, W. (2002) A two step procedure to fractionate mouse testicular macrophages with different cytokine profiles. Arch. Immunol. Ther. Exp. (Warsz). 50, 225-229.
31. Derks, R. A., Beaman, K. D. (2004) Regeneration and tolerance factor prevents bystander T-cell death associated with human immunodeficiency virus infection. Clin. Diagn. Lab. Immunol. 11, 835-840.
32. Critchley, H. O., Kelly, R. W., Lea, R. G., Drudy, T. A., Jones, R. L., Baird, D. T. (1996) Sex steroid regulation of leukocyte traffic in human decidua. Hum. Reprod. 11, 2257-2262.
33. Jones, R. L., Kelly, R. W., Critchley, H. O. (1997) Chemokine and cyclooxygenase-2 expression in human endometrium coincides with leukocyte accumulation. Hum. Reprod. 12, 1300-1306.
34. Shirley, C. R., Hayashi, S., Mounsey, S., Yanagimachi, R., Meistrich, M. L. (2004) Abnormalities and reduced reproductive potential of sperm from Tnp1-and Tnp2-null double mutant mice. Biol. Reprod. 71, 1220-1229.
35. De Kretser, D. M., Loveland, K. L., Meinhardt, A., Simorangkir, D., Wreford, N. (1998) Spermatogenesis Hum. Reprod. 13 (Suppl. 1), 1-8.
36. Winnall, W. R., Muir, J. A., Hedger, M. P. (2011) Rat resident testicular macrophages have an alternatively activated phenotype and constitutively produce interleukin-10 in vitro. J. Leukoc. Biol. 90, 133-143.
37. Maresz, K., Ponomarev, E. D., Barteneva, N., Tan, Y., Mann, M. K., Dittel, B. N. (2008) IL-13 induces the expression of the alternative activation marker Ym1 in a subset of testicular macrophages. J. Reprod. Immunol. 78, 140-148.
38. Chang, H., Brown, C. W., Matzuk, M. M. (2002) Genetic analysis of the mammalian transforming growth factor-β superfamily. Endocr. Rev. 23, 787-823.
39. Mullaney, B. P., Skinner, M. K. (1993) Transforming growth factor-β (β 1, β 2, and β 3) gene expression and action during pubertal development of the seminiferous tubule: potential role at the onset of spermatogenesis. Mol. Endocrinol. 7, 67-76.
40. Ingman, W. V., Robertson, S. A. (2002) Defining the actions of transforming growth factor β in reproduction. Bioessays 24, 904-914.
41. Lui, W. Y., Lee, W. M., Cheng, C. Y. (2003) TGF-βs: their role in testicular function and Sertoli cell tight junction dynamics. Int. J. Androl. 26, 147-160.
42. Wong, C. H., Mruk, D. D., Lui, W. Y., Cheng, C. Y. (2004) Regulation of blood-testis barrier dynamics: an in vivo study. J. Cell Sci. 117, 783-798.
43. Lee, N. P., Mruk, D. D., Wong, C. H., Cheng, C. Y. (2005) Regulation of Sertoli-germ cell adherens junction dynamics in the testis via the nitric oxide synthase (NOS)/cGMP/protein kinase G (PRKG)/β-catenin (CATNB) signaling pathway: an in vitro and in vivo study. Biol. Reprod. 73, 458-471.