Kupffer cells are mandatory for adequate liver regeneration by mediating hyperperfusion via modulation of vasoactive proteins

Microcirculation

Volumn 15, Issue 1, 2008, Pages 37-47

  Abshagen, Kerstin ^a   Eipel, Christian ^a   Kalff, Jörg ^b,c   Menger, Michael ^d   Vollmar, Brigitte ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

^d NONE

Author keywords

Caveolin 1; Clodronate; Hepatic microcirculation; Intravital fluorescence microscopy

Indexed keywords

CAVEOLIN 1; CLODRONIC ACID; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; HEME OXYGENASE 1; LIPOSOME; MESSENGER RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL TONE; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; KUPFFER CELL; LIVER CELL; LIVER PERFUSION; LIVER REGENERATION; LIVER SINUSOID; LIVER WEIGHT; MICROCIRCULATION; MICROVASCULATURE; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEAR STRESS; SIGNAL TRANSDUCTION; VOLUMETRY; WESTERN BLOTTING;

ANIMALS; BLOOD PRESSURE; CAVEOLIN 1; CELL DIVISION; ENDOTHELIN-1; FEMALE; HEME OXYGENASE-1; KUPFFER CELLS; LIVER CIRCULATION; LIVER REGENERATION; MICE; MICE, INBRED C57BL; MICROCIRCULATION; MICROSCOPY, FLUORESCENCE; NITRIC OXIDE SYNTHASE TYPE II; RNA, MESSENGER; SIGNAL TRANSDUCTION; THYMOL; VASOCONSTRICTION;

ANIMALIA; MUS;

EID: 38049112795     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1080/10739680701412989     Document Type: Article

References (48)

1. Abshagen, K., Eipel, C., Menger, M. D. and Vollmar, B. (2006) Comprehensive analysis of the regenerating mouse liver: An in vivo fluorescence microscopic and immunohistological study. J Surg Res, 134, pp. 354-362.
2. Baier, P. K., Baumgartner, U., Hempel, S., Wolff-Vorbeck, G., von Dobschuetz, E. and Hopt, U. T. (2005) Kupffer cells infiltrate liver tissue early after ischemia-reperfusion and partial hepatectomy. Eur Surg Res, 37, pp. 290-297.
3. Bauer, I., Wanner, G. A., Rensing, H., Alte, C., Miescher, E. A., Wolf, B., Pannen, B. H., Clemens, M. G. and Bauer, M. (1998) Expression pattern of heme oxygenase isoenzymes 1 and 2 in normal and stress-exposed rat liver. Hepatology, 27, pp. 829-838.
4. Bauer, M. and Bauer, I. (2002) Heme oxygenase-1: Redox regulation and role in the hepatic response to oxidative stress. Antioxid Redox Signal, 4, pp. 749-758.
5. Chaisson, M. L., Brooling, J. T., Ladiges, W., Tsai, S. and Fausto, N. (2002) Hepatocyte-specific inhibition of NF-kappaB leads to apoptosis after TNF treatment, but not after partial hepatectomy. J Clin Invest, 10, pp. 193-202.
6. Ding, H., Peng, R., Reed, E. and Li, Q. Q. (2003) Effects of Kupffer cell inhibition on liver function and hepatocellular activity in mice. Int J Mol Med, 12, pp. 549-557.
7. Duckers, H. J., Boehm, M., True, A. L., Yet, S. F., San, H., Park, J. L., Webb, R Clinton, Lee, M. E., Nabel, G. J. and Nabel, E. G. (2001) Heme oxygenase-1 protects against vascular constriction and proliferation. Nat Med, 7, pp. 693-698.
8. Eakes, A. T. and Olson, M. S. (1998) Regulation of endothelin synthesis in hepatic endothelial cells. Am J Physiol, 274, p. G1068.
9. Eipel, C., Bordel, R., Nickels, R. M., Menger, M. D. and Vollmar, B. (2004) Impact of leukocytes and platelets in mediating hepatocyte apoptosis in a rat model of systemic endotoxemia. Am J Physiol Gastrointest Liver Physiol, 286, p. G769.
10. Eipel, C., Glanemann, M., Nuessler, A. K., Menger, M. D., Neuhaus, P. and Vollmar, B. (2005) Ischemic preconditioning impairs liver regeneration in extended reduced-size livers. Ann Surg, 241, pp. 477-484.
11. Eipel, C., Schuett, H., Glawe, C., Bordel, R., Menger, M. D. and Vollmar, B. (2005) Pifithrin-alpha induced p53 inhibition does not affect liver regeneration after partial hepatectomy in mice. J Hepatol, 43, pp. 829-835.
12. Fausto, N. (2000) Liver regeneration. J Hepatol, 32, pp. 19-31.
13. Fulton, D., Gratton, J. P. and Sessa, W. C. (2001) Post-translational control of endothelial nitric oxide synthase: Why isn't calcium/ calmodulin enough?. J Pharmacol Exp Ther, 299, pp. 818-824.
14. Garcia-Cardena, G., Fan, R., Stern, D. F., Liu, J. and Sessa, W. C. (1996) Endothelial nitric oxide is regulated by tyrosine phosphorylation and interacts with Caveolin-1. J Biol Chem, 271, pp. 27237-27240.
15. Glanemann, M., Schirmeier, A., Lippert, S., Langrehr, J. M., Neuhaus, P. and Nussler, A. K. (2005) Cobalt-protoporphyrin induced heme oxygenase overexpression and its impact on liver regeneration. Transplant Proc, 37, pp. 3223-3225.
16. Greene, A. K. and Puder, M. (2003) Partial hepatectomy in the mouse: technique and perioperative management. J Invest Surg, 16, pp. 99-102.
17. Gross, J. F. and Aroesty, J. (1972) Mathematical models of capillary flow: A critical review. Biorheology, 9, pp. 225-264.
18. Hori, N., Wiest, R. and Groszmann, R. J. (1998) Enhanced release of nitric oxide in response to changes in flow and shear stress in the superior mesenteric arteries of portal hypertensive rats. Hepatology, 28, pp. 1467-1473.
19. Immenschuh, S., Baumgart-Vogt, E., Tan, M., Iwahara, S., Ramadori, G. and Fahimi, H. D. (2003) Differential cellular and subcellular localization of heme-binding protein 23/peroxiredoxin I and heme oxygenase-1 in rat liver. J Histochem Cytochem, 51, pp. 1621-1631.
20. Keller, S. A., Paxian, M., Ashburn, J. H., Clemens, M. G. and Huynh, T. (2005) Kupffer cell ablation improves hepatic microcirculation after trauma and sepsis. J Trauma, 58, pp. 740-751.
21. Kim, Y. H. and Lee, S. M. (2004) Role of Kupffer cells in the vasoregulatory gene expression during hepatic ischemia/reperfusion. Arch Pharm Res, 1, pp. 111-117.
22. Kirillova, I., Chaisson, M. and Fausto, N. (1999) Tumor necrosis factor induces DNA replication in hepatic cells through nuclear factor κ B activation. Cell Growth Differ, 10, pp. 819-828.
23. Klyscz, T., Junger, M., Jung, F. and Zeintl, H. (1997) Cap image - a new kind of computer-assisted video image analysis system for dynamic capillary microscopy. Biomed Tech (Berl), 42, pp. 168-175.
24. Kobayashi, T., Hirano, K., Yamamoto, T., Hasegawa, G., Hatakeyama, K., Suematsu, M. and Naito, M. (2002) The protective role of Kupffer cells in the ischemia-reperfused rat liver. Arch Histol Cytol, 65, pp. 251-261.
25. Liberati, N. T., Datto, M. B., Frederick, J. P., Shen, X., Wong, C., Rougier-Chapman, E. M. and Wang, X. F. (1999) Smads bind directly to the Jun family of AP-1 transcription factors. Proc Natl Acad Sci U S A, 96, pp. 4844-4849.
26. MacPhee, P. J., Schmidt, E. E. and Groom, A. C. (1995) Intermittence of blood flow in liver sinusoids, studied by high-resolution in vivo microscopy. Am J Physiol, 269, pp. G692-G698.
27. Meijer, C., Wiezer, M. J., Diehl, A. M., Schouten, H. J., Schouten, H. J., Meijer, S., van Rooijen, N., van Lambalgen, A. A., Dijkstra, C. D. and van Leeuwen, P. A. (2000) Kupffer cell depletion by Cl2MDP-liposomes alters hepatic cytokine expression and delays liver regeneration after partial hepatectomy. Liver, 20, pp. 66-77.
28. Michalopoulos, G. K. and De Frances, M. C. (1997) Liver regeneration. Science, 276, pp. 60-66.
29. Moncada, S. and Higgs, E. A. (2006) Nitric oxide and the vascular endothelium. Handb Exp Pharmacol, 176, pp. 213-254.
30. Naito, M., Hasegawa, G., Ebe, Y. and Yamamoto, T. (2004) Differentiation and function of Kupffer cells. Med Electron Microsc, 37, pp. 16-28.
31. Oda, M., Yokomori, H. and Han, J. Y. (2003) Regulatory mechanisms of hepatic microcirculation. Clin Hemorheol Microcirc, 29, pp. 167-182.
32. Palmes, D., Minin, E., Budny, T., Uhlmann, D., Armann, B., Stratmann, U., Herbst, H. and Spiegel, H. U. (2005) The endothelin/nitric oxide balance determines small-for-size liver injury after reduced-size rat liver transplantation. Virchows Arch, 447, pp. 731-741.
33. Pannen, B. H., Bauer, M., Zhang, J., Robotham, J. L. and Clemens, M. G. (1996) A time-dependent balance between endothelins and nitric oxide regulatng portal resistance after endotoxin. Am J Physiol, 271, pp. H1953-H1961.
34. Paxian, M., Rensing, H., Rickauer, A., Schonhofen, S., Schmeck, J., Pannen, B. H., Bauer, I. and Bauer, M. (2001) Kupffer cells and neutrophils as paracrine regulators of the heme oxygenase-1 gene in hepatocytes after hemorrhagic shock. Shock, 15, pp. 438-445.
35. Rappaport, A. M. (1973) The microcirculatory hepatic unit. Microvasc Res, 6, pp. 212-228.
36. Richter, S., Vollmar, B., Mucke, I., Post, S. and Menger, M. D. (2001) Hepatic arteriolo-portal venular shunting guarantees maintenance of nutritional microvascular supply in hepatic arterial buffer response of rat livers. J Physiol, 531, pp. 193-201.
37. Rizzardini, M., Zappone, M., Villa, P., Gnocchi, P., Sironi, M., Diomede, L., Meazza, C., Monshouwer, M. and Cantoni, L. (1998) Kupffer cell depletion partially prevents hepatic heme oxygenase 1 messenger RNA accumulation in systemic inflammation in mice: Role of interleukin 1beta. Hepatology, 27, pp. 703-710.
38. Schoen, J. M., Wang, H. H., Minuk, G. Y. and Lautt, W. W. (2001) Shear stress-induced nitric oxide release triggers the liver regeneration cascade. Nitric Oxide, 5, pp. 453-464.
39. Shah, V., Toruner, M., Haddad, F., Cadelina, G., Papapetropoulos, A., Choo, K., Sessa, W. C. and Groszmann, R. J. (1999) Impaired endothelial nitric oxide synthase activity associated with enhanced caveolin binding in experimental cirrhosis in the rat. Gastroenterology, 117, pp. 1222-1228.
40. Shiratori, Y., Hongo, S., Hikiba, Y., Ohmura, K., Nagura, T., Okano, K., Kamii, K., Tanaka, T., Komatsu, Y., Ochiai, T., Tsubouchi, H. and Omata, M. (1996) Role of macrophages in regeneration of liver. Dig Dis Sci, 10, pp. 1939-1946.
41. Sonin, N., Garcia-Pagan, J., Nakanishi, K., Zhang, J. X. and Clemens, M. G. (1999) Patterns of vasoregulatory gene expression in the liver response to ischemia/reperfusion and endotoxemia. Shock, 11, pp. 175-179.
42. Suematsu, M., Kashiwagi, S., Sano, T., Goda, N., Shinoda, Y. and Ishimura, Y. (1994) Carbon monoxide as an endogenous modulator of hepatic vascular perfusion. Biochem Biophys Res Commun, 205, pp. 1333-1337.
43. Takeishi, T., Hirano, K., Kobayashi, T., Hasegawa, G., Hatakeyama, K. and Naito, M. (1999) The role of Kupffer cells in liver regeneration. Arch Histol Cytol, 62, pp. 413-422.
44. Van Rooijen, N. and Sanders, A. (1994) Liposome mediated depletion of macrophages: Mechanism of action, preparation of liposomes and applications. J Immunol Methods, 174, pp. 83-93.
45. Vogten, J. M., Smakman, N., Voest, E. E. and Rinkes, I CH Borel (2003) Intravital analysis of microcirculation in the regenerating mouse liver. J Surg Res, 113, pp. 264-269.
46. Vollmar, B., Glasz, J., Post, S. and Menger, M. D. (1994) Depressed phagocytic activity of Kupffer cells after warm ischemia-reperfusion of the liver. J Hepatol, 20, pp. 301-304.
47. Windberger, U., Bartholovitsch, A., Plasenzotti, R., Korak, K. J. and Heinze, G. (2003) Whole blood viscosity, plasma viscosity and erythrocyte aggregation in nine mammalian species: Reference values and comparison of data. Exp Physiol, 88, pp. 431-440.
48. Yang, L., Magness, S. T., Bataler, R., Rippe, R. A. and Brenner, D. A. (2005) NF-κ B activation in Kupffer cells after partial hepatectomy. Am J Physiol Gastrointest Liver Physiol, 289, pp. G530-G538.