Regulation of apoptosis and innate immune stimuli in inflammation-induced preterm labor

Journal of Immunology

Volumn 191, Issue 11, 2013, Pages 5702-5713

  Jaiswal, Mukesh K ^a   Agrawal, Varkha ^b   Mallers, Timothy ^a   Gilman Sachs, Alice ^a   Hirsch, Emmet ^b,c   Beaman, Kenneth D ^a  

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

^b NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

A2V ATPASE; ADENOSINE TRIPHOSPHATASE; CASPASE 3; CASPASE 8; CASPASE 9; CRYOPYRIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA CONVERTING ENZYME; PEPTIDOGLYCAN; POLYINOSINIC POLYCYTIDYLIC ACID; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL JUNCTION; CONTROLLED STUDY; DECIDUA; ENZYME ACTIVITY; FEMALE; FETUS MEMBRANE; GRAM POSITIVE INFECTION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PLACENTA; POLARIZATION; PREGNANCY; PREMATURE LABOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; UPREGULATION; UTERUS; VIRUS INFECTION; WESTERN BLOTTING;

EID: 84888316271     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301604     Document Type: Article

References (63)

1. Agrawal, V., and E. Hirsch. 2012. Intrauterine infection and preterm labor. Semin. Fetal Neonatal Med. 17: 12-19.
2. Lamont, R. F. 2003. Infection in the prediction and antibiotics in the prevention of spontaneous preterm labour and preterm birth. BJOG 110(Suppl. 20): 71-75.
3. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4: 499-511.
4. Thaxton, J. E., T. A. Nevers, and S. Sharma. 2010. TLR-mediated preterm birth in response to pathogenic agents. Infect. Dis. Obstet. Gynecol. 2010: pii: 378472.
5. Li, L., J. Kang, and W. Lei. 2010. Role of Toll-like receptor 4 in inflammation-induced preterm delivery. Mol. Hum. Reprod. 16: 267-272.
6. Koga, K., P. B. Aldo, and G. Mor. 2009. Toll-like receptors and pregnancy: trophoblast as modulators of the immune response. J. Obstet. Gynaecol. Res. 35: 191-202.
7. Ilievski, V., and E. Hirsch. 2010. Synergy between viral and bacterial toll-like receptors leads to amplification of inflammatory responses and preterm labor in the mouse. Biol. Reprod. 83: 767-773.
8. Agrawal, V., K. Smart, T. Jilling, and E. Hirsch. 2013. Surfactant protein (SP)-A suppresses preterm delivery and inflammation via TLR2. PLoS ONE 8: e63990.
9. Cardenas, I., R. E. Means, P. Aldo, K. Koga, S. M. Lang, C. J. Booth, A. Manzur, E. Oyarzun, R. Romero, and G. Mor. 2010. Viral infection of the placenta leads to fetal inflammation and sensitization to bacterial products predisposing to preterm labor. [Published erratum appears in 2011 J. Immunol. 187: 2835.] J. Immunol. 185: 1248-1257.
10. Cardenas, I., G. Mor, P. Aldo, S. M. Lang, P. Stabach, A. Sharp, R. Romero, S. Mazaki-Tovi, M. Gervasi, and R. E. Means. 2011. Placental viral infection sensitizes to endotoxin-induced pre-term labor: a double hit hypothesis. Am. J. Reprod. Immunol. 65: 110-117.
11. Trinchieri, G., and A. Sher. 2007. Cooperation of Toll-like receptor signals in innate immune defence. Nat. Rev. Immunol. 7: 179-190.
12. Aksoy, E., C. S. Zouain, F. Vanhoutte, J. Fontaine, N. Pavelka, N. Thieblemont, F. Willems, P. Ricciardi-Castagnoli, M. Goldman, M. Capron, et al. 2005. Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells. J. Biol. Chem. 280: 277-283.
13. Bosch, A. A., G. Biesbroek, K. Trzcinski, E. A. Sanders, and D. Bogaert. 2013. Viral and bacterial interactions in the upper respiratory tract. PLoS Pathog. 9: e1003057.
14. Park, J. S., D. Svetkauskaite, Q. He, J. Y. Kim, D. Strassheim, A. Ishizaka, and E. Abraham. 2004. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J. Biol. Chem. 279: 7370-7377.
15. Smiley, S. T., J. A. King, and W. W. Hancock. 2001. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J. Immunol. 167: 2887-2894.
16. Ntrivalas, E., A. Gilman-Sachs, J. Kwak-Kim, and K. Beaman. 2007. The N-terminus domain of the a2 isoform of vacuolar ATPase can regulate interleukin-1beta production from mononuclear cells in co-culture with JEG-3 choriocarcinoma cells. Am. J. Reprod. Immunol. 57: 201-209.
17. Jaiswal, M. K., A. Gilman-Sachs, G. Chaouat, and K. D. Beaman. 2011. Placental ATPase expression is a link between multiple causes of spontaneous abortion in mice. Biol. Reprod. 85: 626-634.
18. Jaiswal, M. K., T. M. Mallers, B. Larsen, J. Kwak-Kim, G. Chaouat, A. Gilman-Sachs, and K. D. Beaman. 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.
19. Ntrivalas, E., R. Levine, C. Kwong, A. Gilman-Sachs, and K. Beaman. 2010. The a2 isoform of vacuolar ATPase is a modulator of implantation and fetomaternal immune tolerance in early pregnancy. J. Reprod. Immunol. 85: 106-111.
20. Skinner, M. A., L. A. MacLaren, and A. G. Wildeman. 1999. Stage-dependent redistribution of the V-ATPase during bovine implantation. J. Histochem. Cytochem. 47: 1247-1254.
21. Nishihara, T., S. Akifusa, T. Koseki, S. Kato, M. Muro, and N. Hanada. 1995. Specific inhibitors of vacuolar type H(+)-ATPases induce apoptotic cell death. Biochem. Biophys. Res. Commun. 212: 255-262.
22. Bowman, E. J., A. Siebers, and K. Altendorf. 1988. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA 85: 7972-7976.
23. Ohta, T., H. Arakawa, F. Futagami, S. Fushida, H. Kitagawa, M. Kayahara, T. Nagakawa, K. Miwa, K. Kurashima, M. Numata, et al. 1998. Bafilomycin A1 induces apoptosis in the human pancreatic cancer cell line Capan-1. J. Pathol. 185: 324-330.
24. Xu, J., H. T. Feng, C. Wang, K. H. Yip, N. Pavlos, J. M. Papadimitriou, D. Wood, and M. H. Zheng. 2003. Effects of Bafilomycin A1: an inhibitor of vacuolar H (+)-ATPases on endocytosis and apoptosis in RAW cells and RAW cell-derived osteoclasts. J. Cell. Biochem. 88: 1256-1264.
25. Boomer, J. S., G. W. Lee, T. S. Givens, A. Gilman-Sachs, and K. D. Beaman. 2000. Regeneration and tolerance factor's potential role in T-cell activation and apoptosis. Hum. Immunol. 61: 959-971.
26. Green, D. R. 2000. Apoptotic pathways: paper wraps stone blunts scissors. Cell 102: 1-4.
27. Adams, J. M., and S. Cory. 1998. The Bcl-2 protein family: arbiters of cell survival. Science 281: 1322-1326.
28. Hengartner, M. O. 2000. The biochemistry of apoptosis. Nature 407: 770-776.
29. Nagata, S., and P. Golstein. 1995. The Fas death factor. Science 267: 1449-1456.
30. Lee, J., J. H. Richburg, S. C. Younkin, and K. Boekelheide. 1997. The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 138: 2081-2088.
31. Boomer, J. S., R. A. Derks, G. W. Lee, B. K. DuChateau, A. Gilman-Sachs, and K. D. Beaman. 2001. Regeneration and tolerance factor is expressed during T-lymphocyte activation and plays a role in apoptosis. Hum. Immunol. 62: 577-588.
32. Mussalli, G. M., R. Blanchard, S. R. Brunnert, and E. Hirsch. 1999. Inflammatory cytokines in a murine model of infection-induced preterm labor: cause or effect? J. Soc. Gynecol. Investig. 6: 188-195.
33. Hirsch, E., I. Saotome, and D. Hirsh. 1995. A model of intrauterine infection and preterm delivery in mice. Am. J. Obstet. Gynecol. 172: 1598-1603.
34. Elovitz, M. A., Z. Wang, E. K. Chien, D. F. Rychlik, and M. Phillippe. 2003. A new model for inflammation-induced preterm birth: the role of platelet-activating factor and Toll-like receptor-4. Am. J. Pathol. 163: 2103-2111.
35. Fujisaka, S., I. Usui, A. Bukhari, M. Ikutani, T. Oya, Y. Kanatani, K. Tsuneyama, Y. Nagai, K. Takatsu, M. Urakaze, et al. 2009. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes 58: 2574-2582.
36. Aron-Wisnewsky, J., J. Tordjman, C. Poitou, F. Darakhshan, D. Hugol, A. Basdevant, A. Aissat, M. Guerre-Millo, and K. Clément. 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.
37. Teixeira Gomes, R. C., C. Verna, H. B. Nader, R. dos Santos Simões, J. L. Dreyfuss, J. R. Martins, E. C. Baracat, M. de Jesus Simões, and J. M. Soares, Jr. 2009. Concentration and distribution of hyaluronic acid in mouse uterus throughout the estrous cycle. Fertil. Steril. 92: 785-792.
38. Thornberry, N. A., and Y. Lazebnik. 1998. Caspases: enemies within. Science 281: 1312-1316.
39. Hong, J., Y. Nakano, A. Yokomakura, K. Ishihara, S. Kim, Y. S. Kang, and K. Ohuchi. 2006. Nitric oxide production by the vacuolar-type (H+)-ATPase inhibitors bafilomycin A1 and concanamycin A and its possible role in apoptosis in RAW 264.7 cells. J. Pharmacol. Exp. Ther. 319: 672-681.
40. Lee, N. P., D. D. Mruk, C. H. Wong, and C. Y. Cheng. 2005. Regulation of Sertoli-germ cell adherens junction dynamics in the testis via the nitric oxide synthase (NOS)/cGMP/protein kinase G (PRKG)/beta-catenin (CATNB) signaling pathway: an in vitro and in vivo study. Biol. Reprod. 73: 458-471.
41. Gonzalez, D., A. Rojas, M. B. Herrera, and R. S. Conlan. 2012. iNOS activation regulates β-catenin association with its partners in endothelial cells. PLoS ONE 7: e52964.
42. Esplin, M. S., R. Romero, T. Chaiworapongsa, Y. M. Kim, S. Edwin, R. Gomez, M. Mazor, and E. Y. Adashi. 2005. Monocyte chemotactic protein-1 is increased in the amniotic fluid of women who deliver preterm in the presence or absence of intra-amniotic infection. J. Matern. Fetal Neonatal Med. 17: 365-373.
43. Lucas, M., L. M. Stuart, J. Savill, and A. Lacy-Hulbert. 2003. Apoptotic cells and innate immune stimuli combine to regulate macrophage cytokine secretion. J. Immunol. 171: 2610-2615.
44. Derks, R., and K. Beaman. 2004. Regeneration and tolerance factor modulates the effect of adenosine triphosphate-induced interleukin 1 beta secretion in human macrophages. Hum. Immunol. 65: 676-682.
45. Stout-Delgado, H. W., S. E. Vaughan, A. C. Shirali, R. J. Jaramillo, and K. S. Harrod. 2012. Impaired NLRP3 inflammasome function in elderly mice during influenza infection is rescued by treatment with nigericin. J. Immunol. 188: 2815-2824.
46. Mariathasan, S., D. S. Weiss, K. Newton, J. McBride, K. O'Rourke, M. Roose-Girma, W. P. Lee, Y. Weinrauch, D. M. Monack, and V. M. Dixit. 2006. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228-232.
47. Wieczorek, H., D. Brown, S. Grinstein, J. Ehrenfeld, and W. R. Harvey. 1999. Animal plasma membrane energization by proton-motive V-ATPases. Bioessays 21: 637-648.
48. Nishi, T., and M. Forgac. 2002. The vacuolar (H+)-ATPases - nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 3: 94-103.
49. Martínez-Zaguilán, R., E. A. Seftor, R. E. Seftor, Y. W. Chu, R. J. Gillies, and M. J. Hendrix. 1996. Acidic pH enhances the invasive behavior of human melanoma cells. Clin. Exp. Metastasis 14: 176-186.
50. Coakley, R. J., C. Taggart, N. G. McElvaney, and S. J. O'Neill. 2002. Cytosolic pH and the inflammatory microenvironment modulate cell death in human neutrophils after phagocytosis. Blood 100: 3383-3391.
51. Hinoki, A., K. Yoshimura, K. Fujita, M. Akita, R. Ikeda, M. Nagashima, M. Nomura, and A. Satomi. 2006. Suppression of proinflammatory cytokine production in macrophages by lansoprazole. Pediatr. Surg. Int. 22: 915-923.
52. Kwong, C., A. Gilman-Sachs, and K. Beaman. 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.
53. Kwong, C., A. Gilman-Sachs, and K. Beaman. 2013. An independent endocytic pathway stimulates different monocyte subsets by the a2 N-terminus domain of vacuolar-ATPase. OncoImmunology 2: e22978.
54. Shimaoka, M., T. Iida, A. Ohara, N. Taenaka, T. Mashimo, T. Honda, and I. Yoshiya. 1995. NOC, a nitric-oxide-releasing compound, induces dose dependent apoptosis in macrophages. Biochem. Biophys. Res. Commun. 209: 519-526.
55. Lincoln, T. M., T. L. Cornwell, P. Komalavilas, and N. Boerth. 1996. Cyclic GMP-dependent protein kinase in nitric oxide signaling. Methods Enzymol. 269: 149-166.
56. Leist, M., C. Volbracht, S. Kühnle, E. Fava, E. Ferrando-May, and P. Nicotera. 1997. Caspase-mediated apoptosis in neuronal excitotoxicity triggered by nitric oxide. Mol. Med. 3: 750-764.
57. Bandino, A., A. Compagnone, V. Bravoco, C. Cravanzola, A. Lomartire, C. Rossetto, E. Novo, S. Cannito, L. Valfrè di Bonzo, E. Zamara, et al. 2008. Beta-catenin triggers nuclear factor kappaB-dependent up-regulation of hepatocyte inducible nitric oxide synthase. Int. J. Biochem. Cell Biol. 40: 1861-1871.
58. Han, J., P. Sridevi, M. Ramirez, K. J. Ludwig, and J. Y. Wang. 2013. β-Catenin-dependent lysosomal targeting of internalized tumor necrosis factor-α suppresses caspase-8 activation in apoptosis-resistant colon cancer cells. Mol. Biol. Cell 24: 465-473.
59. Ikner, A., and A. Ashkenazi. 2011. TWEAK induces apoptosis through a death-signaling complex comprising receptor-interacting protein 1 (RIP1), Fas-associated death domain (FADD), and caspase-8. J. Biol. Chem. 286: 21546-21554.
60. Gonzalez, J. M., C. W. Franzke, F. Yang, R. Romero, and G. Girardi. 2011. Complement activation triggers metalloproteinases release inducing cervical remodeling and preterm birth in mice. Am. J. Pathol. 179: 838-849.
61. Kahlenberg, J. M., and G. R. Dubyak. 2004. Mechanisms of caspase-1 activation by P2X7 receptor-mediated K+ release. Am. J. Physiol. Cell Physiol. 286: C1100-C1108.
62. Döcke, W. D., F. Randow, U. Syrbe, D. Krausch, K. Asadullah, P. Reinke, H. D. Volk, and W. Kox. 1997. Monocyte deactivation in septic patients: restoration by IFN-gamma treatment. Nat. Med. 3: 678-681.
63. Sakao, Y., K. Takeda, H. Tsutsui, T. Kaisho, F. Nomura, H. Okamura, K. Nakanishi, and S. Akira. 1999. IL-18-deficient mice are resistant to endotoxin-induced liver injury but highly susceptible to endotoxin shock. Int. Immunol. 11: 471-480.