Extravillous Trophoblast Cells-derived Exosomes Promote Vascular Smooth Muscle Cell Migration

Overview

Journal Front Pharmacol

Date 2014 Aug 27

PMID 25157233

Citations 56

Authors

Carlos Salomon

Sarah Yee

Katherin Scholz-Romero

Miharu Kobayashi

Kanchan Vaswani

David Kvaskoff

Sebastian E Illanes

Murray D Mitchell

Gregory E Rice

Affiliations

Soon will be listed here.

Abstract

Background: Vascular smooth muscle cells (VSMCs) migration is a critical process during human uterine spiral artery (SpA) remodeling and a successful pregnancy. Extravillous trophoblast cells (EVT) interact with VSMC and enhance their migration, however, the mechanisms by which EVT remodel SpA remain to be fully elucidated. We hypothesize that exosomes released from EVT promote VSMC migration.

Methods: JEG-3 and HTR-8/SVneo cell lines were used as models for EVT. Cells were cultured at 37°C and humidified under an atmosphere of 5% CO2-balanced N2 to obtain 8% O2. Cell-conditioned media were collected, and exosomes (exo-JEG-3 and exo- HTR-8/SVneo) isolated by differential and buoyant density centrifugation. The effects of exo-EVT on VSMC migration were established using a real-time, live-cell imaging system (Incucyte™). Exosomal proteins where identified by mass spectrometry and submitted to bioinformatic pathway analysis (Ingenuity software).

Results: HTR-8/SVneo cells were significantly more (~30%) invasive than JEG-3 cells. HTR-8/SVneo cells released 2.6-fold more exosomes (6.39 × 10(8) ± 2.5 × 10(8) particles/10(6) cells) compared to JEG-3 (2.86 × 10(8) ± 0.78 × 10(8) particles/10(6) cells). VSMC migration was significantly increased in the presence of exo-JEG-3 and exo-HTR-8/SVneo compared to control (-exosomes) (21.83 ± 0.49 h and 15.57 ± 0.32, respectively, vs. control 25.09 ± 0.58 h, p < 0.05). Sonication completely abolished the effect of exosomes on VSMC migration. Finally, mass spectrometry analysis identified unique exosomal proteins for each EVT cell line-derived exosomes.

Conclusion: The data obtained in this study are consistent with the hypothesis that the release, content, and bioactivity of exosomes derived from EVT-like cell lines is cell origin-dependent and differentially regulates VSMC migration. Thus, an EVT exosomal signaling pathway may contribute to SpA remodeling by promoting the migration of VSMC out of the vessel walls.

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References

Jauniaux E, Poston L, Burton G . Placental-related diseases of pregnancy: Involvement of oxidative stress and implications in human evolution. Hum Reprod Update. 2006; 12(6):747-55. PMC: 1876942. DOI: 10.1093/humupd/dml016. View

Chen G, Zhang Y, Wu X . 786-0 Renal cancer cell line-derived exosomes promote 786-0 cell migration and invasion . Oncol Lett. 2014; 7(5):1576-1580. PMC: 3997692. DOI: 10.3892/ol.2014.1962. View

Delorme-Axford E, Donker R, Mouillet J, Chu T, Bayer A, Ouyang Y . Human placental trophoblasts confer viral resistance to recipient cells. Proc Natl Acad Sci U S A. 2013; 110(29):12048-53. PMC: 3718097. DOI: 10.1073/pnas.1304718110. View

Lee H, Kim Y, Kim D . Exosomes derived from human macrophages suppress endothelial cell migration by controlling integrin trafficking. Eur J Immunol. 2013; 44(4):1156-69. DOI: 10.1002/eji.201343660. View

Pijnenborg R, Bland J, Robertson W, Brosens I . Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta. 1983; 4(4):397-413. DOI: 10.1016/s0143-4004(83)80043-5. View

Soo C, Song Y, Zheng Y, Campbell E, Riches A, Gunn-Moore F . Nanoparticle tracking analysis monitors microvesicle and exosome secretion from immune cells. Immunology. 2012; 136(2):192-7. PMC: 3403268. DOI: 10.1111/j.1365-2567.2012.03569.x. View

Jauniaux E, van Oppenraaij R, Burton G . Obstetric outcome after early placental complications. Curr Opin Obstet Gynecol. 2010; 22(6):452-7. DOI: 10.1097/GCO.0b013e3283404e44. View

Carter A . Animal models of human placentation--a review. Placenta. 2007; 28 Suppl A:S41-7. DOI: 10.1016/j.placenta.2006.11.002. View

Graham C, Hawley T, Hawley R, MacDougall J, Kerbel R, Khoo N . Establishment and characterization of first trimester human trophoblast cells with extended lifespan. Exp Cell Res. 1993; 206(2):204-11. DOI: 10.1006/excr.1993.1139. View

10.

Bulmer J, Innes B, Levey J, Robson S, Lash G . The role of vascular smooth muscle cell apoptosis and migration during uterine spiral artery remodeling in normal human pregnancy. FASEB J. 2012; 26(7):2975-85. DOI: 10.1096/fj.12-203679. View

11.

Salomon C, Kobayashi M, Ashman K, Sobrevia L, Mitchell M, Rice G . Hypoxia-induced changes in the bioactivity of cytotrophoblast-derived exosomes. PLoS One. 2013; 8(11):e79636. PMC: 3823597. DOI: 10.1371/journal.pone.0079636. View

12.

Salomon C, Torres M, Kobayashi M, Scholz-Romero K, Sobrevia L, Dobierzewska A . A gestational profile of placental exosomes in maternal plasma and their effects on endothelial cell migration. PLoS One. 2014; 9(6):e98667. PMC: 4048215. DOI: 10.1371/journal.pone.0098667. View

13.

Blackburn C, Keelan J, Taylor R, North R . Maternal serum activin A is not elevated before preeclampsia in women who are at high risk. Am J Obstet Gynecol. 2003; 188(3):807-11. DOI: 10.1067/mob.2003.173. View

14.

Yoon J, Kim J, Kim K, Kim D, Jung S, Lee H . Proteomic analysis of hypoxia-induced U373MG glioma secretome reveals novel hypoxia-dependent migration factors. Proteomics. 2014; 14(12):1494-502. DOI: 10.1002/pmic.201300554. View

15.

Thery C . Exosomes: secreted vesicles and intercellular communications. F1000 Biol Rep. 2011; 3:15. PMC: 3155154. DOI: 10.3410/B3-15. View

16.

Khong T, LIDDELL H, Robertson W . Defective haemochorial placentation as a cause of miscarriage: a preliminary study. Br J Obstet Gynaecol. 1987; 94(7):649-55. DOI: 10.1111/j.1471-0528.1987.tb03169.x. View

17.

Kam E, Gardner L, Loke Y, King A . The role of trophoblast in the physiological change in decidual spiral arteries. Hum Reprod. 1999; 14(8):2131-8. DOI: 10.1093/humrep/14.8.2131. View

18.

. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2011; 35 Suppl 1:S64-71. PMC: 3632174. DOI: 10.2337/dc12-s064. View

19.

Mincheva-Nilsson L, Nagaeva O, Chen T, Stendahl U, Antsiferova J, Mogren I . Placenta-derived soluble MHC class I chain-related molecules down-regulate NKG2D receptor on peripheral blood mononuclear cells during human pregnancy: a possible novel immune escape mechanism for fetal survival. J Immunol. 2006; 176(6):3585-92. DOI: 10.4049/jimmunol.176.6.3585. View

20.

Kohler P, Bridson W . Isolation of hormone-producing clonal lines of human choriocarcinoma. J Clin Endocrinol Metab. 1971; 32(5):683-7. DOI: 10.1210/jcem-32-5-683. View