Embryo mortality in Isg15-/- mice is exacerbated by environmental stress

Biology of Reproduction

Volumn 92, Issue 2, 2015, Pages

  Henkes, Luiz E ^a,c   Pru, James K ^b   Ashley, Ryan L ^a,d   Anthony, Russell V ^a   Veeramachaneni, D N Rao ^a   Gates, Katherine C ^a   Hansen, Thomas R ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c Universidade Federal de Santa Catarina Campus Curitibanos   (Brazil)

^d NEW MEXICO STATE UNIVERSITY   (United States)

Author keywords

ISG15; Knockout; Mouse; Pregnancy; Uterus

Indexed keywords

INTERFERON REGULATORY FACTOR; INTERFERON STIMULATED GENE FACTOR 15; PROGESTERONE; UNCLASSIFIED DRUG; CYTOKINE; G1P2 PROTEIN, MOUSE; UBIQUITIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL HOUSING; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIRTH; CELL MIGRATION; CONTROLLED STUDY; DECIDUA; DECIDUALIZATION; DISEASE EXACERBATION; EMBRYO; EMBRYO MORTALITY; ENVIRONMENTAL STRESS; EXPERIMENTAL HYPOXIA; FEMALE; FETUS; IMPLANTATION; INNATE IMMUNITY; LITTER SIZE; MALE; MORPHOLOGY; MOUSE; NATURAL KILLER CELL; NONHUMAN; POSTNATAL GROWTH; PRIORITY JOURNAL; PROGENY; PROGESTERONE BLOOD LEVEL; PROTEIN LOCALIZATION; PUP (RODENT); TRANSMISSION ELECTRON MICROSCOPY; TROPHOBLAST; UTERUS; ANIMAL; ANOXIA; FETUS DEATH; GENETICS; KNOCKOUT MOUSE; METABOLISM; NIDATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLACENTA; PREGNANCY;

MUS;

ANIMALS; ANOXIA; CYTOKINES; EMBRYO IMPLANTATION; FEMALE; FETAL DEATH; MICE; MICE, KNOCKOUT; PLACENTA; PREGNANCY; STRESS, PHYSIOLOGICAL; UBIQUITINS; UTERUS;

EID: 84929601056     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.122002     Document Type: Article

References (77)

1. Austin KJ, Ward SK, Teixeira MG, Dean VC, Moore DW, Hansen TR. Ubiquitin cross-reactive protein is released by the bovine uterus in response to interferon during early pregnancy. Biol Reprod 1996; 54:600-606.
2. Hansen TR, Austin KJ, Johnson GA. Transient ubiquitin cross-reactive protein gene expression in the bovine endometrium. Endocrinology 1997; 138:5079-5082.
3. Bebington C, Bell SC, Doherty FJ, Fazleabas AT, Fleming SD. Localization of ubiquitin and ubiquitin cross-reactive protein in human and baboon endometrium and decidua during the menstrual cycle and early pregnancy. Biol Reprod 1999; 60:920-928.
4. Bebington C, Doherty FJ, Fleming SD. Ubiquitin and ubiquitin-protein conjugates are present in human cytotrophoblast throughout gestation. Early Pregnancy 2000; 4:240-252.
5. Austin KJ, Bany BM, Belden EL, Rempel LA, Cross JC, Hansen TR. Interferon-stimulated gene-15 (Isg15) expression is up-regulated in the mouse uterus in response to the implanting conceptus. Endocrinology 2003; 144:3107-3113.
6. Farrell PJ, Broeze RJ, Lengyel P. Accumulation of an mRNA and protein in interferon-treated Ehrlich ascites tumour cells. Nature 1979; 279:523-525.
7. Dao CT, Zhang DE. ISG15: a ubiquitin-like enigma. Front Biosci 2005; 10:2701-2722.
8. Zhao C, Denison C, Huibregtse JM, Gygi S, Krug RM. Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc Natl Acad Sci U S A 2005; 102:10200-10205.
9. D'Cunha J, Knight E Jr, Haas AL, Truitt RL, Borden EC. Immunoregulatory properties of ISG15, an interferon-induced cytokine. Proc Natl Acad Sci U S A 1996; 93:211-215.
10. Giannakopoulos NV, Arutyunova E, Lai C, Lenschow DJ, Haas AL, Virgin HW. ISG15 Arg151 and the ISG15 conjugating enzyme UbE1L are important for innate immune control of Sindbis Virus. J Virol 2008; 83:1602-1610.
11. Giannakopoulos NV, Luo JK, Papov V, Zou W, Lenschow DJ, Jacobs BS, Borden EC, Li J, Virgin HW, Zhang DE. Proteomic identification of proteins conjugated to ISG15 in mouse and human cells. Biochem Biophys Res Commun 2005; 336:496-506.
12. Pickart CM. Mechanisms underlying ubiquitination. Annu Rev Biochem 2001; 70:503-533.
13. Krug RM, Zhao C, Beaudenon S. Properties of the ISG15 E1 enzyme UbE1L. Methods Enzymol 2005; 398:32-40.
14. Zhao C, Beaudenon SL, Kelley ML, Waddell MB, Yuan W, Schulman BA, Huibregtse JM, Krug RM. The UbcH8 ubiquitin E2 enzyme is also the E2 enzyme for ISG15, an IFN-alpha/beta-induced ubiquitin-like protein. Proc Natl Acad Sci U S A 2004; 101:7578-7582.
15. Hochrainer K, Mayer H, Baranyi U, Binder B, Lipp J, Kroismayr R. The human HERC family of ubiquitin ligases: novel members, genomic organization, expression profiling, and evolutionary aspects. Genomics 2005; 85:153-164.
16. Dastur A, Beaudenon S, Kelley M, Krug RM, Huibregtse JM. Herc5, an interferon-induced HECT E3 enzyme, is required for conjugation of ISG15 in human cells. J Biol Chem 2006; 281:4334-4338.
17. Rempel LA, Austin KJ, Ritchie KJ, Yan M, Shen M, Zhang DE, Henkes LE, Hansen TR. Ubp43 gene expression is required for normal Isg15 expression and fetal development. Reprod Biol Endocrinol 2007; 5:13.
18. Ritchie KJ, Malakhov MP, Hetherington CJ, Zhou L, Little MT, Malakhova OA, Sipe JC, Orkin SH, Zhang DE. Dysregulation of protein modification by ISG15 results in brain cell injury. Genes Dev 2002; 16:2207-2212.
19. Tokarz S, Berset C, La Rue J, Friedman K, Nakayama K, Nakayama K, Zhang DE, Lanker S. The ISG15 isopeptidase UBP43 is regulated by proteolysis via the SCFSkp2 ubiquitin ligase. J Biol Chem 2004; 279:46424-46430.
20. Desai SD, Haas AL, Wood LM, Tsai YC, Pestka S, Rubin EH, Saleem A, Nur EKA, Liu LF. Elevated expression of ISG15 in tumor cells interferes with the ubiquitin/26S proteasome pathway. Cancer Res 2006; 66:921-928.
21. Smirnova NP, Webb BT, Bielefeldt-Ohmann H, Van Campen H, Antoniazzi AQ, Morarie SE, Hansen TR. Development of fetal and placental innate immune responses during establishment of persistent infection with bovine viral diarrhea virus. Virus Res 2012; 167:329-336.
22. Komuro A, Bamming D, Horvath CM. Negative regulation of cytoplasmic RNA-mediated antiviral signaling. Cytokine 2008; 43:350-358.
23. Lenschow DJ, Lai C, Frias-Staheli N, Giannakopoulos NV, Lutz A, Wolff T, Osiak A, Levine B, Schmidt RE, Garcia-Sastre A, Leib DA, Pekosz A, et al. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc Natl Acad Sci U S A 2007; 104:1371-1376.
24. Okumura A, Pitha PM, Harty RN. ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity. Proc Natl Acad Sci U S A 2008; 105:3974-3979.
25. Malakhova OA, Zhang DE. ISG15 inhibits Nedd4 ubiquitin E3 activity and enhances the innate antiviral response. J Biol Chem 2008; 283:8783-8787.
26. Hamerman JA, Hayashi F, Schroeder LA, Gygi SP, Haas AL, Hampson L, Coughlin P, Aebersold R, Aderem A. Serpin 2a is induced in activated macrophages and conjugates to a ubiquitin homolog. J Immunol 2002; 168:2415-2423.
27. Malakhov MP, Kim KI, Malakhova OA, Jacobs BS, Borden EC, Zhang DE. High-throughput immunoblotting. Ubiquitin-like protein ISG15 modifies key regulators of signal transduction. J Biol Chem 2003; 278:16608-16613.
28. Rosario GX, Konno T, Soares MJ. Maternal hypoxia activates endovascular trophoblast cell invasion. Dev Biol 2008; 314:362-375.
29. Moore LG, Charles SM, Julian CG. Humans at high altitude: hypoxia and fetal growth. Respir Physiol Neurobiol 2011; 178:181-190.
30. Soares MJ, Konno T, Alam SM. The prolactin family: effectors of pregnancy-dependent adaptations. Trends Endocrinol Metab 2007; 18:114-121.
31. Giussani DA, Camm EJ, Niu Y, Richter HG, Blanco CE, Gottschalk R, Blake EZ, Horder KA, Thakor AS, Hansell JA, Kane AD, Wooding FB, et al. Developmental programming of cardiovascular dysfunction by prenatal hypoxia and oxidative stress. PLoS One 2012; 7:e31017.
32. Drickamer LC. Environmental factors and age of puberty in female house mice. Dev Psychobiol 1990; 23:63-73.
33. Osiak A, Utermohlen O, Niendorf S, Horak I, Knobeloch KP. ISG15, an interferon-stimulated ubiquitin-like protein, is not essential for STAT1 signaling and responses against vesicular stomatitis and lymphocytic choriomeningitis virus. Mol Cell Biol 2005; 25:6338-6345.
34. Herington JL, Bany BM. Effect of the conceptus on uterine natural killer cell numbers and function in the mouse uterus during decidualization. Biol Reprod 2007; 76:579-588.
35. Georgiades P, Watkins M, Burton GJ, Ferguson-Smith AC. Roles for genomic imprinting and the zygotic genome in placental development. Proc Natl Acad Sci U S A 2001; 98:4522-4527.
36. Dokras A, Hoffmann DS, Eastvold JS, Kienzle MF, Gruman LM, Kirby PA, Weiss RM, Davisson RL. Severe feto-placental abnormalities precede the onset of hypertension and proteinuria in a mouse model of preeclampsia. Biol Reprod 2006; 75:899-907.
37. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012; 9:671-675.
38. SAS Institute Inc. SAS/STAT 9.2 User's Guide. Cary, NC: SAS Institute Inc.; 2008.
39. Aplin JD. Adhesion molecules in implantation. Rev Reprod 1997; 2:84-93.
40. Aplin JD, Kimber SJ. Trophoblast-uterine interactions at implantation. Reprod Biol Endocrinol 2004; 2:48.
41. Marwitz S, Zeiser T, Schultz H, Kahler D, Abdullah M, Hauber HP, Zabel P, Vollmer E, Goldmann T. The human placenta releases substances that drive lung cancer into apoptosis. Diagn Pathol 2009; 4:27.
42. Haustein KO. Cigarette smoking, nicotine and pregnancy. Int J Clin Pharmacol Ther 1999; 37:417-427.
43. Agrawal A, Knopik VS, Pergadia ML, Waldron M, Bucholz KK, Martin NG, Heath AC, Madden PA. Correlates of cigarette smoking during pregnancy and its genetic and environmental overlap with nicotine dependence. Nicotine Tob Res 2008; 10:567-578.
44. Bebington C, Doherty FJ, Fleming SD. Ubiquitin cross-reactive protein gene expression is increased in decidualized endometrial stromal cells at the initiation of pregnancy. Mol Hum Reprod 1999; 5:966-972.
45. Johnson GA, Austin KJ, Van Kirk EA, Hansen TR. Pregnancy and interferon-tau induce conjugation of bovine ubiquitin cross-reactive protein to cytosolic uterine proteins. Biol Reprod 1998; 58:898-904.
46. Johnson GA, Spencer TE, Hansen TR, Austin KJ, Burghardt RC, Bazer FW. Expression of the interferon tau inducible ubiquitin cross-reactive protein in the ovine uterus. Biol Reprod 1999; 61:312-318.
47. Ashley RL, Henkes LE, Bouma GJ, Pru JK, Hansen TR. Deletion of the Isg15 gene results in up-regulation of decidual cell survival genes and down-regulation of adhesion genes: implication for regulation by IL-1beta. Endocrinology 2010; 151:4527-4536.
48. Bany BM, Cross JC. Post-implantation mouse conceptuses produce paracrine signals that regulate the uterine endometrium undergoing decidualization. Dev Biol 2006; 294:445-456.
49. Hansen TR, Pru JK. ISGylation: a conserved pathway in mammalian pregnancy. Adv Exp Med Biol 2014; 759:13-31.
50. Lenschow DJ, Lai C, Frias-Staheli N, Giannakopoulos NV, Lutz A, Wolff T, Osiak A, Levine B, Schmidt RE, Garcia-Sastre A, Leib DA, Pekosz A, et al. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc Natl Acad Sci U S A 2007; 104:1371-1376.
51. Loeb KR, Haas AL. The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins. J Biol Chem 1992; 267:7806-7813.
52. Haas AL, Ahrens P, Bright PM, Ankel H. Interferon induces a 15-kilodalton protein exhibiting marked homology to ubiquitin. J Biol Chem 1987; 262:11315-11323.
53. D'Cunha J, Ramanujam S, Wagner RJ, Witt PL, Knight E Jr, Borden EC. In vitro and in vivo secretion of human ISG15, an IFN-induced immunomodulatory cytokine. J Immunol 1996; 157:4100-4108.
54. Croy BA, Di Santo JP, Greenwood JD, Chantakru S, Ashkar AA. Transplantation into genetically alymphoid mice as an approach to dissect the roles of uterine natural killer cells during pregnancy-a review. Placenta 2000; 21(Suppl A):S77-S80.
55. Cross JC, Werb Z, Fisher SJ. Implantation and the placenta: key pieces of the development puzzle. Science 1994; 266:1508-1518.
56. Cross JC. The genetics of pre-eclampsia: a feto-placental or maternal problem? Clin Genet 2003; 64:96-103.
57. Croy BA, Chantakru S, Esadeg S, Ashkar AA, Wei Q. Decidual natural killer cells: key regulators of placental development (a review). J Reprod Immunol 2002; 57:151-168.
58. Fazleabas AT, Kim JJ, Strakova Z. Implantation: embryonic signals and the modulation of the uterine environment-a review. Placenta 2004; 25(Suppl A):S26-S31.
59. Gargosky SE, Giudice LC, Rosenfeld RG, Fazleabas AT. Different molecular and messenger ribonucleic acid forms of insulin-like growth factor-binding protein-3 in the pregnant baboon (Papio anubis). J Endocrinol 1995; 147:449-461.
60. Giudice LC, Conover CA, Bale L, Faessen GH, Ilg K, Sun I, Imani B, Suen LF, Irwin JC, Christiansen M, Overgaard MT, Oxvig C. Identification and regulation of the IGFBP-4 protease and its physiological inhibitor in human trophoblasts and endometrial stroma: evidence for paracrine regulation of IGF-II bioavailability in the placental bed during human implantation. J Clin Endocrinol Metab 2002; 87:2359-2366.
61. Murray MJ, Lessey BA. Embryo implantation and tumor metastasis: common pathways of invasion and angiogenesis. Semin Reprod Endocrinol 1999; 17:275-290.
62. Wu L, de Bruin A, Saavedra HI, Starovic M, Trimboli A, Yang Y, Opavska J, Wilson P, Thompson JC, Ostrowski MC, Rosol TJ, Woollett LA, et al. Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 2003; 421:942-947.
63. Cross JC, Baczyk D, Dobric N, Hemberger M, Hughes M, Simmons DG, Yamamoto H, Kingdom JC. Genes, development and evolution of the placenta. Placenta 2003; 24:123-130.
64. Merviel P, Evain-Brion D, Challier JC, Salat-Baroux J, Uzan S. The molecular basis of embryo implantation in humans. Zentralbl Gynakol 2001; 123:328-339.
65. Rossant J, Cross JC. Placental development: lessons from mouse mutants. Nat Rev Genet 2001; 2:538-548.
66. Alam SM, Konno T, Dai G, Lu L, Wang D, Dunmore JH, Godwin AR, Soares MJ. A uterine decidual cell cytokine ensures pregnancy-dependent adaptations to a physiological stressor. Development 2007; 134:407-415.
67. Ho-Chen JK, Ain R, Alt AR, Wood JG, Gonzalez NC, Soares MJ. Hypobaric hypoxia as a tool to study pregnancy-dependent responses at the maternal-fetal interface. Methods Mol Med 2006; 122:427-434.
68. Ho-Chen JK, Bustamante JJ, Soares MJ. Prolactin-like protein-f subfamily of placental hormones/cytokines: responsiveness to maternal hypoxia. Endocrinology 2007; 148:559-565.
69. Regnault TR, Galan HL, Parker TA, Anthony RV. Placental development in normal and compromised pregnancies-a review. Placenta 2002; 23(Suppl A):S119-S129.
70. Soleymanlou N, Jurisica I, Nevo O, Ietta F, Zhang X, Zamudio S, Post M, Caniggia I. Molecular evidence of placental hypoxia in preeclampsia. J Clin Endocrinol Metab 2005; 90:4299-4308.
71. Burton GJ, Jauniaux E. Placental oxidative stress: from miscarriage to preeclampsia. J Soc Gynecol Investig 2004; 11:342-352.
72. Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN, Burton GJ. Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol 2000; 157:2111-2122.
73. Yackerson NS, Piura B, Friger M. The influence of weather state on the incidence of preeclampsia and placental abruption in semi-arid areas. Clin Exp Obstet Gynecol 2007; 34:27-30.
74. Nicholl MJ, Robinson LH, Preston CM. Activation of cellular interferonresponsive genes after infection of human cells with herpes simplex virus type 1. J Gen Virol 2000; 81:2215-2218.
75. Nyman TA, Matikainen S, Sareneva T, Julkunen I, Kalkkinen N. Proteome analysis reveals ubiquitin-conjugating enzymes to be a new family of interferon-alpha-regulated genes. Eur J Biochem 2000; 267:4011-4019.
76. Li J, Peet GW, Balzarano D, Li X, Massa P, Barton RW, Marcu KB. Novel NEMO/IkappaB kinase and NF-kappa B target genes at the pre-B to immature B cell transition. J Biol Chem 2001; 276:18579-18590.
77. Malakhova OA, Yan M, Malakhov MP, Yuan Y, Ritchie KJ, Kim KI, Peterson LF, Shuai K, Zhang DE. Protein ISGylation modulates the JAKSTAT signaling pathway. Genes Dev 2003; 17:455-460.