Actomyosin contractility drives bile regurgitation as an early response during obstructive cholestasis

Journal of Hepatology

Volumn 66, Issue 6, 2017, Pages 1231-1240

  Gupta, Kapish ^a   Li, Qiushi ^a,b   Fan, Jun Jun ^c,d,e   Fong, Eliza Li Shan ^b   Song, Ziwei ^c   Mo, Shupei ^c   Tang, Haoyu ^a   Ng, Inn Chuan ^b   Ng, Chan Way ^b   Pawijit, Pornteera ^b,f   Zhuo, Shuangmu ^d,g   Dong, Chen Yuan ^h   Low, Boon Chuan ^a,b   Wee, Aileen ^b   Dan, Yock Young ⁱ   Kanchanawong, Pakorn ^a,b   So, Peter ^d   Viasnoff, Virgile ^a,j   Yu, Hanry ^a,b,c,d,k  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c AGENCY FOR SCIENCE   (Singapore)

^d SINGAPORE MIT ALLIANCE FOR RESEARCH AND TECHNOLOGY   (Singapore)

^e FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^f NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^g FUJIAN NORMAL UNIVERSITY   (China)

^h NATIONAL TAIWAN UNIVERSITY   (Taiwan)

ⁱ NATIONAL UNIVERSITY HOSPITAL   (Singapore)

^j CNRS UMI 3639   (Singapore)

^k SOUTHERN MEDICAL UNIVERSITY   (China)

more..

Author keywords

Actomyosin cortex; Bile; Bile canaliculi; Blebs; Cholestasis; Hepatocytes; Vesicles

Indexed keywords

ACTIN; MYOSIN ADENOSINE TRIPHOSPHATASE;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BILE CANALICULUS; BILE REFLUX; CELL SIZE; CELL VACUOLE; CHOLESTASIS; CONTROLLED STUDY; CYTOPLASM; IN VIVO STUDY; LIVER CELL CULTURE; MOUSE; NONHUMAN; OSMOTIC PRESSURE; PRIORITY JOURNAL; ANIMAL; BILE DUCT; BIOMECHANICS; DISEASE MODEL; MALE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PRESSURE; RAT; TRANSGENIC MOUSE; WISTAR RAT;

ACTOMYOSIN; ANIMALS; BILE CANALICULI; BILE DUCTS; BILE REFLUX; BIOMECHANICAL PHENOMENA; CHOLESTASIS; DISEASE MODELS, ANIMAL; MALE; MICE; MICE, TRANSGENIC; PRESSURE; RATS; RATS, WISTAR;

EID: 85015415852     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2017.01.026     Document Type: Article

References (51)

1. Reshetnyak, V.I., Physiological and molecular biochemical mechanisms of bile formation. World J Gastroenterol 19 (2013), 7341–7360.
2. Musch, A., The unique polarity phenotype of hepatocytes. Exp Cell Res 328 (2014), 276–283.
3. Watanabe, N., Tsukada, N., Smith, C.R., Phillips, M.J., Motility of bile canaliculi in the living animal: implications for bile flow. J Cell Biol 113 (1991), 1069–1080.
4. Hartley, J.L., Davenport, M., Kelly, D.A., Biliary atresia. Lancet 374 (2009), 1704–1713.
5. Li, M.K., Crawford, J.M., The pathology of cholestasis. Semin Liver Dis 24 (2004), 21–42.
6. Wagner, M., Zollner, G., Trauner, M., New molecular insights into the mechanisms of cholestasis. J Hepatol 51 (2009), 565–580.
7. Wildhaber, B.E., Biliary atresia: 50 years after the first kasai. ISRN Surg, 2012, 2012, 132089.
8. Song, J.Y., Van Marle, J., Van Noorden, C.J., Frederiks, W.M., Disturbed structural interactions between microfilaments and tight junctions in rat hepatocytes during extrahepatic cholestasis induced by common bile duct ligation. Histochem Cell Biol 106 (1996), 573–580.
9. Song, J.Y., Van Noorden, C.J., Frederiks, W.M., Rearrangement of hepatocellular F-actin precedes the formation of rosette-like structures in parenchyma of cholestatic rat liver. Hepatology 27 (1998), 765–771.
10. Segawa, O., Miyano, T., Fujimoto, T., Watanabe, S., Hirose, M., Fujiwara, T., Actin and myosin deposition around bile canaliculi: a predictor of clinical outcome in biliary atresia. J Pediatr Surg 28 (1993), 851–856.
11. Matter, A., Orci, L., Rouiller, C., A study on the permeability barriers between Disse's space and the bile canaliculus. J Ultrastruct Res 11 (1969), 1–71.
12. Watanabe, N., Kojima, S., Takashimizu, S., Nishizaki, Y., Kagawa, T., Phillips, M.J., Initial site of bile regurgitation following extrahepatic biliary obstruction in living rats. J Gastroenterol Hepatol 22 (2007), 1983–1992.
13. Riedl, J., Flynn, K.C., Raducanu, A., Gartner, F., Beck, G., Bosl, M., et al. Lifeact mice for studying F-actin dynamics. Nat Methods 7 (2010), 168–169.
14. Ritsma, L., Steller, E.J., Beerling, E., Loomans, C.J., Zomer, A., Gerlach, C., et al. Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis. Sci Transl Med, 4, 2012, 158ra145.
15. Seglen, P.O., Preparation of isolated rat liver cells. Methods Cell Biol 13 (1976), 29–83.
16. Li, Q., Zhang, Y., Pluchon, P., Robens, J., Herr, K., Mercade, M., et al. Extracellular matrix scaffolding guides lumen elongation by inducing anisotropic intercellular mechanical tension. Nat Cell Biol 18 (2016), 311–318.
17. Abraldes, J.G., Pasarin, M., Garcia-Pagan, J.C., Animal models of portal hypertension. World J Gastroenterol, 12, 2006.
18. Strazzabosco, M., Fabris, L., Functional anatomy of normal bile ducts. Anat Rec 291 (2008), 653–660.
19. Vartak, N., Damle-Vartak, A., Richter, B., Dirsch, O., Dahmen, U., Hammad, S., et al. Cholestasis-induced adaptive remodeling of interlobular bile ducts. Hepatology 63 (2016), 951–964.
20. Sudo, R., Kohara, H., Mitaka, T., Ikeda, M., Tanishita, K., Coordinated movement of bile canalicular networks reconstructed by rat small hepatocytes. Ann Biomed Eng 33 (2005), 696–708.
21. Tsukada, N., Phillips, M.J., Bile canalicular contraction is coincident with reorganization of pericanalicular filaments and co-localization of actin and myosin-II. J Histochem Cytochem 41 (1993), 353–363.
22. Yokomori, H., Oda, M., Kamegaya, Y., Ogi, M., Tsukada, N., Ishii, H., Bile canalicular contraction and dilatation in primary culture of rat hepatocytes–possible involvement of two different types of plasma membrane Ca(2+)-Mg(2+)-ATPase and Ca(2+)-pump-ATPase. Med Electron Microsc 34 (2001), 115–122.
23. Charras, G., Paluch, E., Blebs lead the way: how to migrate without lamellipodia. Nat Rev Mol Cell Biol 9 (2008), 730–736.
24. Charras, G.T., Coughlin, M., Mitchison, T.J., Mahadevan, L., Life and times of a cellular bleb. Biophys J 94 (2008), 1836–1853.
25. Laster, S.M., Mackenzie, J.M. Jr., Bleb formation and F-actin distribution during mitosis and tumor necrosis factor-induced apoptosis. Microsc Res Tech 34 (1996), 272–280.
26. Gebala, V., Collins, R., Geudens, I., Phng, L.K., Gerhardt, H., Blood flow drives lumen formation by inverse membrane blebbing during angiogenesis in vivo. Nat Cell Biol 18 (2016), 443–450.
27. Tinevez, J.Y., Schulze, U., Salbreux, G., Roensch, J., Joanny, J.F., Paluch, E., Role of cortical tension in bleb growth. Proc Natl Acad Sci U S A 106 (2009), 18581–18586.
28. Azmaiparashvili, E., Kordzaia, D., Dzidziguri, D., Biliary hypertension as the cell proliferation trigger in bile duct ligated rats. Georgian Med News, 2009, 111–116.
29. Vital, A., Bioulac-Sage, P., Iron, A., Balabaud, C., Morphologic structure of bile canaliculi after bile duct ligation in the rat. A time-course study. Arch Pathol Lab Med 106 (1982), 464–467.
30. Charras, G.T., A short history of blebbing. J Microsc 231 (2008), 466–478.
31. Kawahara, H., French, S.W., Role of cytoskeleton in canalicular contraction in cultured differentiated hepatocytes. Am J Pathol 136 (1990), 521–532.
32. Reif, R., Karlsson, J., Gunther, G., Beattie, L., Wrangborg, D., Hammad, S., et al. Bile canalicular dynamics in hepatocyte sandwich cultures. Arch Toxicol 89 (2015), 1861–1870.
33. Fickert, P., Zollner, G., Fuchsbichler, A., Stumptner, C., Weiglein, A.H., Lammert, F., et al. Ursodeoxycholic acid aggravates bile infarcts in bile duct-ligated and Mdr2 knockout mice via disruption of cholangioles. Gastroenterology 123 (2002), 1238–1251.
34. Charras, G.T., Hu, C.K., Coughlin, M., Mitchison, T.J., Reassembly of contractile actin cortex in cell blebs. J Cell Biol 175 (2006), 477–490.
35. Fransen, J.H., Hilbrands, L.B., Ruben, J., Stoffels, M., Adema, G.J., van der Vlag, J., et al. Mouse dendritic cells matured by ingestion of apoptotic blebs induce T cells to produce interleukin-17. Arthritis Rheum 60 (2009), 2304–2313.
36. Korb, L.C., Ahearn, J.M., C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J Immunol 158 (1997), 4525–4528.
37. Paluch, E.K., Raz, E., The role and regulation of blebs in cell migration. Curr Opin Cell Biol 25 (2013), 582–590.
38. Petrie, R.J., Koo, H., Yamada, K.M., Generation of compartmentalized pressure by a nuclear piston governs cell motility in a 3D matrix. Science 345 (2014), 1062–1065.
39. Crawford, A.R., Smith, A.J., Hatch, V.C., Oude Elferink, R.P., Borst, P., Crawford, J.M., Hepatic secretion of phospholipid vesicles in the mouse critically depends on mdr2 or MDR3 P-glycoprotein expression. Visualization by electron microscopy. J Clin Invest 100 (1997), 2562–2567.
40. Torok, N.J., Larusso, E.M., McNiven, M.A., Alterations in vesicle transport and cell polarity in rat hepatocytes subjected to mechanical or chemical cholestasis. Gastroenterology 121 (2001), 1176–1184.
41. Hemery, I., Durand-Schneider, A.M., Feldmann, G., Vaerman, J.P., Maurice, M., The transcytotic pathway of an apical plasma membrane protein (B10) in hepatocytes is similar to that of IgA and occurs via a tubular pericentriolar compartment. J Cell Sci 109 (1996), 1215–1227.
42. Larkin, J.M., Coleman, H., Espinosa, A., Levenson, A., Park, M.S., Woo, B., et al. Intracellular accumulation of pIgA-R and regulators of transcytotic trafficking in cholestatic rat hepatocytes. Hepatology 38 (2003), 1199–1209.
43. Goltz, J.S., Wolkoff, A.W., Novikoff, P.M., Stockert, R.J., Satir, P., A role for microtubules in sorting endocytic vesicles in rat hepatocytes. Proc Natl Acad Sci U S A 89 (1992), 7026–7030.
44. Yoshino, K., Scanning electron microscopy on the rat liver with alpha-naphthylisothiocyanate-induced cholestasis. Gastroenterol Jap 15 (1980), 550–563.
45. Wightman, R.M., Haynes, C.L., Synaptic vesicles really do kiss and run. Nat Neurosci 7 (2004), 321–322.
46. Bow, D.A., Perry, J.L., Miller, D.S., Pritchard, J.B., Brouwer, K.L., Localization of P-gp (Abcb1) and Mrp2 (Abcc2) in freshly isolated rat hepatocytes. Drug Metab Dispos 36 (2008), 198–202.
47. Cipolla, M.J., Gokina, N.I., Osol, G., Pressure-induced actin polymerization in vascular smooth muscle as a mechanism underlying myogenic behavior. FASEB J 16 (2002), 72–76.
48. Verma, S., Han, S.P., Michael, M., Gomez, G.A., Yang, Z., Teasdale, R.D., et al. A WAVE2-Arp2/3 actin nucleator apparatus supports junctional tension at the epithelial zonula adherens. Mol Biol Cell 23 (2012), 4601–4610.
49. Yonemura, S., Wada, Y., Watanabe, T., Nagafuchi, A., Shibata, M., Alpha-Catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 12 (2010), 533–542.
50. Chen, F., Ananthanarayanan, M., Emre, S., Neimark, E., Bull, L.N., Knisely, A.S., et al. Progressive familial intrahepatic cholestasis, type 1, is associated with decreased farnesoid X receptor activity. Gastroenterology 126 (2004), 756–764.
51. Perez, M.J., Briz, O., Bile-acid-induced cell injury and protection. World J Gastroenterol 15 (2009), 1677–1689.