Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-17T18:21:23.506Z Has data issue: false hasContentIssue false
  • English
  • Français

In Vivo Multivesicular Body and Exosome Secretion in the Intestinal Epithelial Cells of Turtles During Hibernation

Published online by Cambridge University Press:  28 October 2019

Waseem Ali Vistro ,
Yufei Huang ,
Xuebing Bai ,
Ping Yang ,
Abdul Haseeb ,
Hong Chen ,
Yifei Liu ,
Zhang Yue ,
Imran Tarique  and
Qiusheng Chen Open the ORCID record for Qiusheng Chen [Opens in a new window]
Waseem Ali Vistro
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Yufei Huang
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Xuebing Bai
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Ping Yang
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Abdul Haseeb
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Hong Chen
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Yifei Liu
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Zhang Yue
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Imran Tarique
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
Qiusheng Chen*
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, China
*
*Author for correspondence: Qiusheng Chen, E-mail: [email protected]
Get access

Abstract

The present study was designed to investigate the in vivo biological processes of multivesicular bodies (MVBs) and exosomes in mitochondria-rich cells (MRCs), goblet cells (GCs), and absorptive cells (ACs) in turtle intestines during hibernation. The exosome markers, cluster of differentiation 63 (CD63) and tumor susceptibility gene 101 (TSG101), were positively expressed in intestinal villi during turtle hibernation. The distribution and formation processes of MVBs and exosomes in turtle MRCs, GCs, and ACs were further confirmed by transmission electron microscopy. During hibernation, abundantly secreted early endosomes (ees) were localized in the luminal and basal cytoplasm of the MRCs and ACs, and late endosomes (les) were dispersed with the supranuclear parts of the MRCs and ACs. Many “heterogeneous” MVBs were identified throughout the cytoplasm of the MRCs and ACs. Interestingly, the ees, les, and MVBs were detected in the cytoplasm of the GCs during hibernation; however, they were absent during nonhibernation. Furthermore, the exocytosis pathways of exosomes and autophagic vacuoles were observed in the MRCs, GCs, and ACs during hibernation. In addition, the number of different MVBs with intraluminal vesicles (ILVs) and heterogeneous endosome–MVB–exosome complexes was significantly increased in the MRCs, GCs, and ACs during hibernation. All these findings indicate that intestinal epithelial cells potentially perform a role in the secretion of MVBs and exosomes, which are essential for mucosal immunity, during hibernation.

Keywords

absorptive cellsChinese soft-shelled turtleexosomesmucosal-immune responsemultivesicular bodies
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 25 , Issue 6 , December 2019 , pp. 1341 - 1351
Copyright
Copyright © Microscopy Society of America 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Åkesson, CP, McGovern, G, Dagleish, MP, Espenes, A, Press, CM, Landsverk, T & Jeffrey, M (2011). Exosome-producing follicle associated epithelium is not involved in uptake of PrPd from the gut of sheep (Ovis aries): An ultrastructural study. PLoS One 6(7), e22180. doi:10.1371/journal.pone.0022180.Google Scholar
Altherr, S & Freyer, D (2000). Asian turtles are threatened by extinction. Turtle Tortoise Newslett 1, 7–11.Google Scholar
Altick, AL, Baryshnikova, LM, Vu, TQ & Von Bartheld, CS (2009). Quantitative analysis of multivesicular bodies (MVBs) in the hypoglossal nerve: Evidence that neurotrophic factors do not use MVBs for retrograde axonal transport. J Comp Neurol 514(6), 641–657. doi:10.1002/cne.22047.Google Scholar
Babst, M, Odorizzi, G, Estepa, EJ & Emr, SD (2000). Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1(3), 248–258. doi:10.1034/j.1600-0854.2000.010307.Google Scholar
Bai, X, Guo, Y, Shi, Y, Lin, J, Tarique, I, Wang, X, Vistro, WA, Huang, Y, Chen, H & Haseeb, A (2019). In vivo multivesicular bodies and their exosomes in the absorptive cells of the zebrafish (Danio Rerio) gut. Fish Shellfish Immun 88, 578–586.Google Scholar
Barreto, A, Rodríguez, L-S, Rojas, OL, Wolf, M, Greenberg, HB, Franco, MA & Angel, J (2010). Membrane vesicles released by intestinal epithelial cells infected with rotavirus inhibit T-cell function. Viral Immunol 23(6), 595–608. doi:10.1089/vim.2009.0113.Google Scholar
Bentley, PJ (2002). Endocrines and Osmoregulation: A Comparative Account in Vertebrates. Springer-Verlag Berlin Heidelberg: Springer Science & Business Media.Google Scholar
Braicu, C, Tomuleasa, C, Monroig, P, Cucuianu, A, Berindan-Neagoe, I & Calin, G (2015). Exosomes as divine messengers: Are they the Hermes of modern molecular oncology? Cell Death Differ 22(1), 34. doi:10.1038/cdd.2014.130.Google Scholar
Chen, H, Yang, P, Chu, X, Huang, Y, Liu, T, Zhang, Q, Li, Q, Hu, L, Waqas, Y & Ahmed, N (2016). Cellular evidence for nano-scale exosome secretion and interactions with spermatozoa in the epididymis of the Chinese soft-shelled turtle, Pelodiscus sinensis. Oncotarget 7(15), 19242. doi:10.18632/oncotarget.8092.Google Scholar
Cocucci, E, Racchetti, G & Meldolesi, J (2009). Shedding microvesicles: Artefacts no more. Trends Cell Biol 19(2), 43–51. doi:10.1016/j.tcb.2008.11.003.Google Scholar
Elbrønd, VS, Jones, CJ & Skadhauge, E (2004). Localization, morphology and function of the mitochondria-rich cells in relation to transepithelial Na+-transport in chicken lower intestine (coprodeum). Comp Biochem Physiol Part A 137(4), 683–696.Google Scholar
Evans, DH, Piermarini, PM & Choe, KP (2005). The multifunctional fish gill: Dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85(1), 97–177. doi:10.1152/physrev.00050.2003.Google Scholar
Felli, C, Vincentini, O, Silano, M & Masotti, A (2017). HIV-1 Nef signaling in intestinal mucosa epithelium suggests the existence of an active inter-kingdom crosstalk mediated by exosomes. Front Microbiol 8, 1022. doi:10.3389/fmicb.2017.01022.Google Scholar
Galluzzi, L, Pietrocola, F, Bravo-San Pedro, JM, Amaravadi, RK, Baehrecke, EH, Cecconi, F, Codogno, P, Debnath, J, Gewirtz, DA & Karantza, V (2015). Autophagy in malignant transformation and cancer progression. EMBO J 34(7), 856–880.Google Scholar
Gruenberg, J, Griffiths, G & Howell, KE (1989). Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J Cell Biol 108(4), 1301–1316. doi:10.1083/jcb.108.4.1301.Google Scholar
Hiroi, J, Yasumasu, S, McCormick, SD, Hwang, P-P & Kaneko, T (2008). Evidence for an apical Na–Cl cotransporter involved in ion uptake in a teleost fish. J Exp Biol 211(16), 2584–2599. doi:10.1242/jeb.018663.Google Scholar
Hu, G, Gong, A-Y, Roth, AL, Huang, BQ, Ward, HD, Zhu, G, LaRusso, NF, Hanson, ND & Chen, X-M (2013). Release of luminal exosomes contributes to TLR4-mediated epithelial antimicrobial defense. PLoS Pathog 9(4), e1003261. doi:10.1371/journal.ppat.1003261.Google Scholar
Hu, L, Li, Q, Yang, P, Gandahi, JA, Arain, TS, Le, Y, Zhang, Q, Liu, T, Waqas, MY & Ahmad, N (2016). Expression of TLR2/4 on epididymal spermatozoa of the Chinese soft-shelled turtle Pelodiscus sinensis during the hibernation season. Anat Rec 299(11), 1578–1584.Google Scholar
Huang, Y, Chen, H, Yang, P, Bai, X, Shi, Y, Vistro, WA, Tarique, I, Haseeb, A & Chen, Q (2019). Hepatic lipid droplet breakdown through lipolysis during hibernation in Chinese soft-shelled turtle (Pelodiscus sinensis). Aging 11(7), 1990.Google Scholar
Hume, I, Beiglböck, C, Ruf, T, Frey-Roos, F, Bruns, U & Arnold, W (2002). Seasonal changes in morphology and function of the gastrointestinal tract of free-living alpine marmots (Marmota marmota). J Comp Physiol B 172(3), 197–207.Google Scholar
Hundorfean, G, Zimmer, K-P, Strobel, S, Gebert, A, Ludwig, D & Büning, JR (2007). Luminal antigens access late endosomes of intestinal epithelial cells enriched in MHC I and MHC II molecules: in vivo study in Crohn's ileitis. Am J Physiol Gastrointest Liver Physiol 293(4), G798–G808. doi:10.1152/ajpgi.00135.2007.Google Scholar
Huotari, J & Helenius, A (2011). Endosome maturation. EMBO J 30(17), 3481–3500. doi:10.1038/emboj.2011.286.Google Scholar
Johnstone, RM (2006). Exosomes biological significance: A concise review. Blood Cells Mol Dis 36(2), 315–321. doi:10.1016/j.bcmd.2005.12.001.Google Scholar
Kaneko, T, Hasegawa, S, Takagi, Y, Tagawa, M & Hirano, T (1995). Hypoosmoregulatory ability of eyed-stage embryos of chum salmon. Mar Biol 122(1), 165–170.Google Scholar
Kaneko, T, Watanabe, S & Lee, KM (2008). Functional Morphology of Mitochondrion-Rich Cells in Euryhaline and StenohalineTeleosts. Tokyo: Terrapub.Google Scholar
Karlsson, M, Lundin, S, Dahlgren, U, Kahu, H, Pettersson, I & Telemo, E (2001). “Tolerosomes” are produced by intestinal epithelial cells. Eur J Immunol 31(10), 2892–2900. doi:10.1002/1521-4141(2001010)31:10<2892::AID-IMMU2892>3.0.CO;2-I.3.0.CO;2-I.>Google Scholar
Kesimer, M, Scull, M, Brighton, B, DeMaria, G, Burns, K, O'Neal, W, Pickles, RJ & Sheehan, JK (2009). Characterization of exosome-like vesicles released from human tracheobronchial ciliated epithelium: A possible role in innate defense. FASEB J 23(6), 1858–1868. doi:10.1096/fj.08-119131.Google Scholar
Klöhn, P-C, Castro-Seoane, R & Collinge, J (2013). Exosome release from infected dendritic cells: A clue for a fast spread of prions in the periphery? J Infect 67(5), 359–368. doi:10.1016/j.jinf.2013.07.024.Google Scholar
Lai, KP, Li, J-W, Gu, J, Chan, T-F, Tse, WKF & Wong, CKC (2015). Transcriptomic analysis reveals specific osmoregulatory adaptive responses in gill mitochondria-rich cells and pavement cells of the Japanese eel. BMC Genomics 16(1), 1072. doi:10.1186/s12864-015-2271-0.Google Scholar
Mallegol, J, Van Niel, G, Lebreton, C, Lepelletier, Y, Candalh, C, Dugave, C, Heath, JK, Raposo, G, Cerf-Bensussan, N & Heyman, M (2007). T84-intestinal epithelial exosomes bear MHC class II/peptide complexes potentiating antigen presentation by dendritic cells. Gastroenterology 132(5), 1866–1876. doi:10.1053/j.gastro.2007.02.043.Google Scholar
Marshall, W & Grosell, M (2006). Ion transport, osmoregulation, and acid-base balance. Physiol Fishes 3, 177–230.Google Scholar
Mayhew, T, Elbrønd, V, Dantzer, V, Skadhauge, E & Møller, O (1992). Structural and enzymatic studies on the plasma membrane domains and sodium pump enzymes of absorptive epithelial cells in the avian lower intestine. Cell Tissue Res 270(3), 577–585.Google Scholar
Piper, RC & Katzmann, DJ (2007). Biogenesis and function of multivesicular bodies. Annu Rev Cell Dev Biol 23, 519–547. doi:10.1146/annurev.cellbio.23.090506.123319.Google Scholar
Raposo, G & Stoorvogel, W (2013). Extracellular vesicles: Exosomes, microvesicles, and friends. J Cell Biol 200(4), 373–383.Google Scholar
Silva, P, Solomon, R, Spokes, K & Epstein, FH (1977). Ouabain inhibition of gill Na-K-ATPase: Relationship to active chloride transport. J Exp Zool 199(3), 419–426. doi:10.1002/jez.1401990316.Google Scholar
Stern, LJ, Potolicchio, I & Santambrogio, L (2006). MHC class II compartment subtypes: Structure and function. Curr Opin Immunol 18(1), 64–69. doi:10.1016/j.coi.2005.11.005.Google Scholar
Talaei, F (2014). Modulation of mTOR and autophagy in hibernating hamster lung and the application of the potential mechanism to improve the recellularization process of decellularized lung scaffolds. J Regen Med Tissue Eng 3(1), 1.Google Scholar
Trajkovic, K, Dhaunchak, AS, Goncalves, JT, Wenzel, D, Schneider, A, Bunt, G, Nave, K-A & Simons, M (2006). Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J Cell Biol 172(6), 937–948. doi:10.1083/jcb.200509022.Google Scholar
Valadi, H, Ekström, K, Bossios, A, Sjöstrand, M, Lee, JJ & Lötvall, JO (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9(6), 654. doi:10.1038/ncb1596.Google Scholar
Van Niel, G, Charrin, S, Simoes, S, Romao, M, Rochin, L, Saftig, P, Marks, MS, Rubinstein, E & Raposo, G (2011). The tetraspanin CD63 regulates ESCRT-independent and-dependent endosomal sorting during melanogenesis. Dev Cell 21(4), 708–721. doi:10.1016/j.devcel.2011.08.019.Google Scholar
Van Niel, G, Mallegol, J, Bevilacqua, C, Candalh, C, Brugiere, S, Tomaskovic-Crook, E, Heath, JK, Cerf-Bensussan, N & Heyman, M (2003). Intestinal epithelial exosomes carry MHC class II/peptides able to inform the immune system in mice. Gut 52(12), 1690–1697. doi:10.1136/gut.52.12.1690.Google Scholar
Van Niel, G, Raposo, G, Candalh, C, Boussac, M, Hershberg, R, Cerf-Bensussan, N & Heyman, M (2001). Intestinal epithelial cells secrete exosome–like vesicles. Gastroenterology 121(2), 337–349. doi:10.1016/j.devcel.2011.08.019.Google Scholar
Villarroya-Beltri, C, Baixauli, F, Mittelbrunn, M, Fernández-Delgado, I, Torralba, D, Moreno-Gonzalo, O, Baldanta, S, Enrich, C, Guerra, S & Sánchez-Madrid, F (2016). ISGylation controls exosome secretion by promoting lysosomal degradation of MVB proteins. Nat Commun 7, 13588.Google Scholar
Wang, AL, Lukas, TJ, Yuan, M, Du, N, Tso, MO & Neufeld, AH (2009). Autophagy and exosomes in the aged retinal pigment epithelium: Possible relevance to drusen formation and age-related macular degeneration. PLoS One 4(1), e4160. doi:10.1371/journal.pone.0004160.Google Scholar
Xiangkun, H, Li, Z, Meiying, L, Huijun, B, Nainan, H & Qiusheng, C (2008). Seasonal changes of sperm storage and correlative structures in male and female soft-shelled turtles, Trionyx sinensis. Anim Reprod Sci 108(3–4), 435–445.Google Scholar
Supplementary material: Image

Vistro et al. supplementary material

Figure S1

Download Vistro et al. supplementary material(Image)
Image 15.8 MB