Rho-kinase/myosin light chain kinase pathway plays a key role in the impairment of bile canaliculi dynamics induced by cholestatic drugs

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Sharanek, Ahmad ^a,b   Burban, Audrey ^a,b   Burbank, Matthew ^a,b   Le Guevel, Remy ^b   Li, Ruoya ^c   Guillouzo, Andre ^a,b   Guguen Guillouzo, Christiane ^a,b,c  

^a Univ Rennes   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c Rennes University ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

1 (5 ISOQUINOLINESULFONYL) 2 METHYLPIPERAZINE; BILE ACID; CARDIAC MYOSIN; CHLORPROMAZINE; CYCLOSPORINE; FASUDIL; MYOSIN II; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN 2; MYOSIN LIGHT CHAIN KINASE; PROTEIN ZO1; RHO KINASE;

ANALOGS AND DERIVATIVES; BILE CANALICULUS; CELL CULTURE; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; HUMAN; LIVER CELL; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; TIME LAPSE IMAGING;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; BILE ACIDS AND SALTS; BILE CANALICULI; CARDIAC MYOSINS; CELL SURVIVAL; CELLS, CULTURED; CHLORPROMAZINE; CYCLOSPORINE; HEPATOCYTES; HUMANS; MICROSCOPY, FLUORESCENCE; MYOSIN LIGHT CHAINS; MYOSIN TYPE II; MYOSIN-LIGHT-CHAIN KINASE; PHOSPHORYLATION; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; TIME-LAPSE IMAGING; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84968665544     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep24709     Document Type: Article

References (43)

1. Padda, M. S., Sanchez, M., Akhtar, A. J., Boyer, J. L. Drug-induced cholestasis. Hepatology 53, 1377-1387 (2011).
2. Bjornsson, E. S., Jonasson, J. G. Drug-induced cholestasis. Clin Liver Dis 17, 191-209 (2013).
3. Morgan, R. E. et al. A multifactorial approach to hepatobiliary transporter assessment enables improved therapeutic compound development. Toxicol Sci 136, 216-241 (2013).
4. Stieger, B. Role of the bile salt export pump, BSEP, in acquired forms of cholestasis. Drug Metab Rev 42, 437-445 (2010).
5. Welch, M. A., Kock, K., Urban, T. J., Brouwer, K. L., Swaan, P. W. Toward predicting drug-induced liver injury: parallel computational approaches to identify multidrug resistance protein 4 and bile salt export pump inhibitors. Drug Metab Dispos 43, 725-734 (2015).
6. Wakabayashi, Y., Dutt, P., Lippincott-Schwartz, J., Arias, I. M. Rab11a and myosin Vb are required for bile canalicular formation in WIF-B9 cells. Proc Natl Acad Sci USA 102, 15087-15092 (2005).
7. Nossaman, B. D., Kadowitz, P. J. The role of the RhoA/rho-kinase pathway in pulmonary hypertension. Curr Drug Discov Technol 6, 59-71 (2009).
8. Lee, D. L., Webb, R. C., Jin, L. Hypertension and RhoA/Rho-kinase signaling in the vasculature: highlights from the recent literature. Hypertension 44, 796-799 (2004).
9. Mills, J. C., Stone, N. L., Erhardt, J., Pittman, R. N. Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation. J Cell Biol 140, 627-636 (1998).
10. Isotani, E. et al. Real-time evaluation of myosin light chain kinase activation in smooth muscle tissues from a transgenic calmodulinbiosensor mouse. Proc Natl Acad Sci USA 101, 6279-6284 (2004).
11. Herrema, H. et al. Rho kinase, myosin-II, and p42/44 MAPK control extracellular matrix-mediated apical bile canalicular lumen morphogenesis in HepG2 cells. Mol Biol Cell 17, 3291-3303 (2006).
12. Fu, D., Wakabayashi, Y., Lippincott-Schwartz, J., Arias, I. M. Bile acid stimulates hepatocyte polarization through a cAMP-Epac-MEK-LKB1-AMPK pathway. Proc Natl Acad Sci USA 108, 1403-1408 (2011).
13. Homolya, L. et al. LKB1/AMPK and PKA control ABCB11 trafficking and polarization in hepatocytes. Plos One 9, e91921 (2014).
14. Fu, D. et al. Coordinated elevation of mitochondrial oxidative phosphorylation and autophagy help drive hepatocyte polarization. Proc Natl Acad Sci USA 110, 7288-7293 (2013).
15. Zhou, Q. et al. Intrahepatic upregulation of RhoA and Rho-kinase signalling contributes to increased hepatic vascular resistance in rats with secondary biliary cirrhosis. Gut 55, 1296-1305 (2006).
16. Arias, I. M. et al. The biology of the bile canaliculus, 1993. Hepatology 17, 318-329 (1993).
17. LeCluyse, E. L., Audus, K. L., Hochman, J. H. Formation of extensive canalicular networks by rat hepatocytes cultured in collagensandwich configuration. Am J Physiol 266, C1764-1774 (1994).
18. Antherieu, S. et al. Oxidative stress plays a major role in chlorpromazine-induced cholestasis in human HepaRG cells. Hepatology 57, 1518-1529 (2013).
19. Sharanek, A. et al. Different dose-dependent mechanisms are involved in early cyclosporine a-induced cholestatic effects in hepaRG cells. Toxicol Sci 141, 244-253 (2014).
20. Sharanek, A. et al. Cellular Accumulation and Toxic Effects of Bile Acids in Cyclosporine A-Treated HepaRG Hepatocytes. Toxicol Sci 147, 573-587 (2015).
21. Orsler, D. J., Ahmed-Choudhury, J., Chipman, J. K., Hammond, T., Coleman, R. ANIT-induced disruption of biliary function in rat hepatocyte couplets. Toxicol Sci 47, 203-210 (1999).
22. Barnwell, S. G., Tuchweber, B., Yousef, I. M. Biliary lipid secretion in the rat during infusion of increasing doses of unconjugated bile acids. Biochim Biophys Acta 922, 221-233 (1987).
23. Miyairi, M. et al. Taurocholate accelerates bile canalicular contractions in isolated rat hepatocytes. Gastroenterology 87, 788-792 (1984).
24. Watanabe, T., Hosoya, H., Yonemura, S. Regulation of myosin II dynamics by phosphorylation and dephosphorylation of its light chain in epithelial cells. Mol Biol Cell 18, 605-616 (2007).
25. Morgan, R. E. et al. Interference with bile salt export pump function is a susceptibility factor for human liver injury in drug development. Toxicol Sci 118, 485-500 (2010).
26. Dawson, S., Stahl, S., Paul, N., Barber, J., Kenna, J. G. In vitro inhibition of the bile salt export pump correlates with risk of cholestatic drug-induced liver injury in humans. Drug Metab Dispos 40, 130-138 (2012).
27. Pedersen, J. M. et al. Early identification of clinically relevant drug interactions with the human bile salt export pump (BSEP/ABCB11). Toxicol Sci 136, 328-343 (2013).
28. Rodrigues, A. D. et al. Drug-induced perturbations of the bile acid pool, cholestasis, and hepatotoxicity: mechanistic considerations beyond the direct inhibition of the bile salt export pump. Drug Metab Dispos 42, 566-574 (2014).
29. Wood, R. L. An Electron Microscope Study of Developing Bile Canaliculi in the Rat. Anat Rec 151, 507-529 (1965).
30. Fu, D., Wakabayashi, Y., Ido, Y., Lippincott-Schwartz, J., Arias, I. M. Regulation of bile canalicular network formation and maintenance by AMP-activated protein kinase and LKB1. J Cell Sci 123, 3294-3302 (2010).
31. Bachour-El Azzi, P. et al. Comparative Localization and Functional Activity of the Main Hepatobiliary Transporters in HepaRG Cells and Primary Human Hepatocytes. Toxicol Sci 145, 157-168 (2015).
32. Oshio, C., Phillips, M. J. Contractility of bile canaliculi: implications for liver function. Science 212, 1041-1042 (1981).
33. 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, 1069-1080 (1991).
34. Adelstein, R. S., Pato, M. D., Sellers, J. R., de Lanerolle, P., Conti, M. A. Regulation of actin-myosin interaction by reversible phosphorylation of myosin and myosin kinase. Cold Spring Harb Symp Quant Biol 46 Pt 2, 921-928 (1982).
35. Watanabe, N. et al. Taurolithocholate impairs bile canalicular motility and canalicular bile secretion in isolated rat hepatocyte couplets. World J Gastroenterol 12, 5320-5325 (2006).
36. Arikawa, K., Hicks, J. L., Williams, D. S. Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors. J Cell Biol 110, 1993-1998 (1990).
37. Kamm, K. E., Stull, J. T. Dedicated myosin light chain kinases with diverse cellular functions. J Biol Chem 276, 4527-4530 (2001).
38. Somlyo, A. P., Somlyo, A. V. Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83, 1325-1358 (2003).
39. Cerec, V. et al. Transdifferentiation of hepatocyte-like cells from the human hepatoma HepaRG cell line through bipotent progenitor. Hepatology 45, 957-967 (2007).
40. Gripon, P. et al. Infection of a human hepatoma cell line by hepatitis B virus. Proc Natl Acad Sci USA 99, 15655-15660 (2002).
41. Pernelle, K. et al. Automated detection of hepatotoxic compounds in human hepatocytes using HepaRG cells and image-based analysis of mitochondrial dysfunction with JC-1 dye. Toxicol Appl Pharmacol 254, 256-266 (2011).
42. Antherieu, S., Rogue, A., Fromenty, B., Guillouzo, A., Robin, M. A. Induction of vesicular steatosis by amiodarone and tetracycline is associated with up-regulation of lipogenic genes in HepaRG cells. Hepatology 53, 1895-1905 (2011).
43. Wang, R. et al. Defective canalicular transport and toxicity of dietary ursodeoxycholic acid in the abcb11?/? mouse: transport and gene expression studies. Am J Physiol Gastrointest Liver Physiol 305, G286-294 (2013).