Altered autophagic flux enhances inflammatory responses during inflammation-induced preterm labor

Scientific Reports

Volumn 5, Issue , 2015, Pages

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

^a NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

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

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATG4C PROTEIN, MOUSE; ATG7 PROTEIN, MOUSE; AUTOPHAGY RELATED PROTEIN; AUTOPHAGY RELATED PROTEIN 7; CYSTEINE PROTEINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LAMP1 PROTEIN, MOUSE; LIPOPOLYSACCHARIDE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MAP1LC3 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; POLYINOSINIC POLYCYTIDYLIC ACID; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; TLR2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ANIMAL; AUTOPHAGY; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; INFLAMMATION; LYSOSOME; METABOLISM; MOUSE; PATHOLOGY; PHAGOSOME; PLACENTA; PREGNANCY; PREMATURE LABOR; SIGNAL TRANSDUCTION;

ANIMALS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 7; AUTOPHAGY-RELATED PROTEINS; CYSTEINE ENDOPEPTIDASES; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; INFLAMMATION; LIPOPOLYSACCHARIDES; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NF-KAPPA B; OBSTETRIC LABOR, PREMATURE; PHAGOSOMES; PLACENTA; POLY I-C; PREGNANCY; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84925379753     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep09410     Document Type: Article

References (62)

1. Mizushima, N., Levine, B., Cuervo, A. M. & Klionsky, D. J. Autophagy fights disease through cellular self-digestion. Nature 451, 1069-75 (2008).
2. Maiuri, M. C., Zalckvar, E., Kimchi, A. & Kroemer, G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8, 741-52 (2007).
3. Kroemer, G., Marino, G. & Levine, B. Autophagy and the integrated stress response. Mol Cell 40, 280-93 (2010).
4. Cadwell, K., Stappenbeck, T. S. & Virgin, H. W. Role of autophagy and autophagy genes in inflammatory bowel disease. Curr Top Microbiol Immunol 335, 141-67 (2009).
5. Tang, D., Kang, R., Coyne, C. B., Zeh, H. J. & Lotze, M. T. PAMPs and DAMPs: signal 0s that spur autophagy and immunity. Immunol Rev 249, 158-75 (2012).
6. Deretic, V. Autophagy in immunity and cell-autonomous defense against intracellular microbes. Immunol Rev 240, 92-104 (2011).
7. Hung, T. H. et al. Increased autophagy in placentas of intrauterine growth-restricted pregnancies. PloS one 7, e40957 (2012).
8. Nakashima, A. et al. Impaired autophagy by soluble endoglin, under physiological hypoxia in early pregnant period, is involved in poor placentation in preeclampsia. Autophagy 9, 303-16 (2013).
9. Delgado, M. et al. Autophagy and pattern recognition receptors in innate immunity. Immunol Rev 227, 189-202 (2009).
10. Xu, Y. et al. Toll-like Receptor 4 Is a Sensor for Autophagy Associated with Innate Immunity. Immunity 27, 135-144 (2007).
11. Delgado, M. A., Elmaoued, R. A., Davis, A. S., Kyei, G. & Deretic, V. Toll-like receptors control autophagy. EMBO J 27, 1110-21 (2008).
12. Sanjuan, M. A. et al. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450, 1253-7 (2007).
13. Djavaheri-Mergny, M. et al. NF-kappaB activation represses tumor necrosis factor-alpha-induced autophagy. J Biol Chem 281, 30373-82 (2006).
14. Corcelle, E. et al. Control of the autophagy maturation step by the MAPK ERK and p38: lessons from environmental carcinogens. Autophagy 3, 57-9 (2007).
15. Corcelle, E. et al. Disruption of autophagy at the maturation step by the carcinogen lindane is associated with the sustained mitogen-activated protein kinase/extracellular signal-regulated kinase activity. Cancer Res 66, 6861-70 (2006).
16. Criollo, A. et al. The IKK complex contributes to the induction of autophagy. EMBO J 29, 619-31 (2010).
17. Comb, W. C., Cogswell, P., Sitcheran, R. & Baldwin, A. S. IKK-dependent, NF-kappaB-independent control of autophagic gene expression. Oncogene 30, 1727-32 (2011).
18. Agrawal, V. & Hirsch, E. Intrauterine infection and preterm labor. Semin Fetal Neonatal Med 17, 12-19 (2011).
19. Blencowe, H. et al. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet 379, 2162-72 (2012).
20. Agrawal, V., Smart, K., Jilling, T. & Hirsch, E. Surfactant Protein (SP)-A Suppresses Preterm Delivery and Inflammation via TLR2. PloS one 8, e63990 (2013).
21. Ilievski, V., Lu, S. J. & Hirsch, E. Activation of toll-like receptors 2 or 3 and preterm delivery in the mouse. Reprod Sci 14, 315-20 (2007).
22. Cardenas, I. et al. Viral infection of the placenta leads to fetal inflammation and sensitization to bacterial products predisposing to preterm labor. J of Immunol 185, 1248-57 (2010).
23. Cardenas, I. et al. Placental viral infection sensitizes to endotoxin-induced preterm labor: a double hit hypothesis. Am J Reprod Immunol 65, 110-7 (2011).
24. Ilievski, V. & Hirsch, E. Synergy between viral and bacterial toll-like receptors leads to amplification of inflammatory responses and preterm labor in the mouse. Biol Reprod 83, 767-73 (2010).
25. Zoncu, R. et al. mTORC1 Senses Lysosomal Amino Acids Through an Inside-Out Mechanism That Requires the Vacuolar H+-ATPase. Science 334, 678-683 (2011).
26. Ntrivalas, E., Gilman-Sachs, A., Kwak-Kim, J. & Beaman, K. 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, 201-9 (2007).
27. Jaiswal, M. K. et al. Abortion-prone mating influences alteration of systemic A2 vacuolar ATPase expression in spleen and blood immune cells. Am J Reprod Immunol 67, 421-33 (2012).
28. Jaiswal, M. K., Gilman-Sachs, A., Chaouat, G. & Beaman, K. D. Placental ATPase expression is a link between multiple causes of spontaneous abortion in mice. Biol Reprod 85, 626-34 (2011).
29. Ota, K. et al. Expression of a2 vacuolar ATPase in spermatozoa is associated with semen quality and chemokine-cytokine profiles in infertile men. PloS one 8, e70470 (2013).
30. Jaiswal, M. K. et al. V-ATPase upregulation during early pregnancy: a possible link to establishment of an inflammatory response during preimplantation period of pregnancy. Reproduction 143, 713-25 (2012).
31. Jaiswal, M. K. et al. Vacuolar-ATPase isoform a2 regulates macrophages and cytokine profile necessary for normal spermatogenesis in testis. J Leukoc Biol 96, 337-47 (2014).
32. Jaiswal, M. K. et al. Regulation of Apoptosis and Innate Immune Stimuli in Inflammation-Induced Preterm Labor. J Immunol 191, 5702-5713 (2013).
33. Yamamoto, A. et al. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23, 33-42 (1998).
34. Deretic, V., Saitoh, T. & Akira, S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol 13, 722-37 (2013).
35. Elovitz, M. A., Wang, Z., Chien, E. K., Rychlik, D. F. & Phillippe, M. A new model for inflammation-induced preterm birth: the role of platelet-activating factor and Toll-like receptor-4. Am J Pathol 163, 2103-11 (2003).
36. Burd, I. et al. Inflammation-induced preterm birth alters neuronal morphology in the mouse fetal brain. J Neurosci Res 88, 1872-81 (2010).
37. Dudley, D. J., Branch, D. W., Edwin, S. S. & Mitchell, M. D. Induction of preterm birth in mice by RU486. Biol Reprod 55, 992-5 (1996).
38. Mizushima, N., Yoshimori, T. & Levine, B. Methods in mammalian autophagy research. Cell 140, 313-26 (2010).
39. Xu, J. et al. 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, 1256-64 (2003).
40. Gonzalez, J. M., Franzke, C. W., Yang, F., Romero, R. & Girardi, G. Complement activation triggers metalloproteinases release inducing cervical remodeling and preterm birth in mice. Am J Pathol 179, 838-49 (2011).
41. Mackler, A. M., Iezza, G., Akin, M. R., McMillan, P. & Yellon, S. M. Macrophage trafficking in the uterus and cervix precedes parturition in the mouse. Biol Reprod 61, 879-83 (1999).
42. Eskelinen, E.-L. Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy. Mol Asp Med 27, 495-502 (2006).
43. Trocoli, A. & Djavaheri-Mergny, M. The complex interplay between autophagy and NF-kappaB signaling pathways in cancer cells. Am J Cancer Res 1, 629-49 (2011).
44. Lindstrom, T. M. & Bennett, P. R. The role of nuclear factor kappa B in human labour. Reproduction 130, 569-81 (2005).
45. Jaffer, S., Shynlova, O. & Lye, S. Mammalian target of rapamycin is activated in association with myometrial proliferation during pregnancy. Endocrinology 150, 4672-80 (2009).
46. Kyathanahalli, C. et al. Cross-species withdrawal of MCL1 facilitates postpartum uterine involution in both the mouse and baboon. Endocrinology 154, 4873-84 (2013).
47. Hirota, Y., Cha, J., Yoshie, M., Daikoku, T. & Dey, S. K. Heightened uterine mammalian target of rapamycin complex 1 (mTORC1) signaling provokes preterm birth in mice. Proc Natl Acad Sci U S A 108, 18073-8 (2011).
48. Doulaveris, G. et al. A polymorphism in an autophagy-related gene, ATG16L1, influences time to delivery in women with an unfavorable cervix who require labor induction. J Perinat Med 41, 411-4 (2013).
49. Signorelli, P. et al. Autophagy in term normal human placentas. Placenta 32, 482-5 (2011).
50. Kim, J., Kim, T. Y., Cho, K. S., Kim, H. N. & Koh, J. Y. Autophagy activation and neuroprotection by progesterone in the G93A-SOD1 transgenic mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 59, 80-5 (2013).
51. Rubinsztein, D. C., Codogno, P. & Levine, B. Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov 11, 709-30 (2012).
52. Tanaka, Y. et al. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 406, 902-6 (2000).
53. Stypmann, J. et al. LAMP-2 deficient mice show depressed cardiac contractile function without significant changes in calcium handling. Basic Res Cardiol 101, 281-91 (2006).
54. Fortunato, F. et al. Impaired autolysosome formation correlates with Lamp-2 depletion: role of apoptosis, autophagy, and necrosis in pancreatitis. Gastroenterology 137, 350-60, 360 e1-5 (2009).
55. Moscat, J. & Diaz-Meco, M. T. p62 at the crossroads of autophagy, apoptosis, and cancer. Cell 137, 1001-4 (2009).
56. Chang, C. P., Su, Y. C., Hu, C. W. & Lei, H. Y. TLR2-dependent selective autophagy regulates NF-kappaB lysosomal degradation in hepatoma-derived M2 macrophage differentiation. Cell Death Differ 20, 515-23 (2013).
57. Agrawal, V., Jaiswal, M. K., Chaturvedi, M. M., Tiwari, D. C. & Jaiswal, Y. K. Lipopolysaccharide alters the vaginal electrical resistance in cycling and pregnant mice. Am J Reprod Immunol 61, 158-66 (2009).
58. Hirsch, E., Saotome, I. & Hirsh, D. A model of intrauterine infection and preterm delivery in mice. Am J Obstet Gynecol 172, 1598-603 (1995).
59. Agrawal, V. et al. Platelet-activating factor: a role in preterm delivery and an essential interaction with toll-like receptor signaling in mice. Biol Reprod 91, 119 (2014).
60. Teixeira Gomes, R. C. et al. Concentration and distribution of hyaluronic acid in mouse uterus throughout the estrous cycle. Fertil Steril 92, 785-92 (2009).
61. Klionsky, D. J. et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4, 151-75 (2008).
62. Thornberry, N. A. & Lazebnik, Y. Caspases: enemies within. Science 281, 1312-6 (1998).