Age-Related changes in scavenger receptor-mediated endocytosis in rat liver sinusoidal endothelial cells

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 65 A, Issue 9, 2010, Pages 951-960

  Simon Santamaria, Jaione ^a   Malovic, Ivana ^a   Warren, Alessandra ^b   Oteiza, Ana ^a   Le Couteur, David ^b   Smedsrød, Brd ^a   McCourt, Peter ^a   Sørensen, Karen Kristine ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Aging; Hepatic sinusoid; Porosity; Scavenger endothelial cells; Stabilin

Indexed keywords

RATTUS;

BOVINE SERUM ALBUMIN; CELL SURFACE RECEPTOR; FORMALDEHYDE; NERVE CELL ADHESION MOLECULE; STAB1 PROTEIN, MOUSE; STAB2 PROTEIN, MOUSE;

AGING; ANIMAL; ARTICLE; CELL CULTURE; CONFOCAL MICROSCOPY; CYTOLOGY; ENDOCYTOSIS; ENDOTHELIUM CELL; FISCHER 344 RAT; LIVER; MALE; METABOLISM; RAT; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

AGING; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELLS, CULTURED; ENDOCYTOSIS; ENDOTHELIAL CELLS; FORMALDEHYDE; LIVER; MALE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; RATS; RATS, INBRED F344; RECEPTORS, CELL SURFACE; SERUM ALBUMIN, BOVINE;

EID: 77955896716     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glq108     Document Type: Article

References (54)

1. Smedsrod B. Clearance function of scavenger endothelial cells. Comp Hepatol. 2004;3(suppl 1):S22.
2. Seternes T, Sorensen K, Smedsrod B. Scavenger endothelial cells of vertebrates: A nonperipheral leukocyte system for high-capacity elimination of waste macromolecules. Proc Natl Acad Sci\USA. 2002; 99:7594-7597.
3. Malovic I, Sorensen KK, Elvevold KH, et al. The mannose receptor on murine liver sinusoidal endothelial cells is the main denatured collagen clearance receptor. Hepatology. 2007;45:1454-1461.
4. Oie CI, Olsen R, Smedsrod B, Hansen JB. Liver sinusoidal endothelial cells are the principal site for elimination of unfractionated heparin from the circulation. Am J Physiol Gastrointest Liver Physiol. 2008; 294:G520-G528.
5. Elvevold K, Simon-Santamaria J, Hasvold H, McCourt P, Smedsrod B, Sorensen KK. Liver sinusoidal endothelial cells depend on man-nose receptor-mediated recruitment of lysosomal enzymes for normal degradation capacity. Hepatology. 2008;48:2007-2015.
6. Blomhoff R, Eskild W, Berg T. Endocytosis of formaldehyde-treated serum albumin via scavenger pathway in liver endothelial cells. Bio-chem J. 1984;218:81-86.
7. De Rijke YB, Biessen EA, Vogelezang CJ, van Berkel TJ. Binding characteristics of scavenger receptors on liver endothelial and Kupffer cells for modifed low-density lipoproteins. Biochem J. 1994;304(Pt 1):69-73.
8. Smedsrod B, Melkko J, Araki N, Sano H, Horiuchi S. Advanced gly-cation end products are eliminated by scavenger-receptor-mediated endocytosis in hepatic sinusoidal Kupffer and endothelial cells. Bio-chem J. 1997;322(Pt 2):567-573.
9. Lovdal T, Andersen E, Brech A, Berg T. Fc receptor mediated endocytosis of small soluble immunoglobulin G immune complexes in Kupffer and endothelial cells from rat liver. J Cell Sci. 2000;113(Pt 18):3255-3266.
10. Martin-Armas M, Simon-Santamaria J, Pettersen I, Moens U, Smedsrod B, Sveinbjornsson B. Toll-like receptor 9 (TLR9) is present in murine liver sinusoidal endothelial cells (LSECs) and mediates the effect of CpG-oligonucleotides. J Hepatol. 2006;44:939-946.
11. Le Couteur DG, Warren A, Cogger VC, et al. Old age and the hepatic sinusoid. Anat Rec (Hoboken). 2008;291:672-683.
12. Brouwer A, Barelds RJ, Knook DL. Age-related changes in the endo-cytic capacity of rat liver Kupffer and endothelial cells. Hepatology. 1985;5:362-366.
13. Caperna TJ, Garvey JS. Antigen handling in aging. II. The role of Kupffer and endothelial cells in antigen processing in Fischer 344 rats. Mech Ageing Dev. 1982;20:205-221.
14. Heil MF, Dingman AD, Garvey JS. Antigen handling in ageing. III. Age-related changes in antigen handling by liver parenchymal and nonparenchymal cells. Mech Ageing Dev. 1984;26:327-340.
15. Ito Y, Sorensen KK, Bethea NW, et al. Age-related changes in the hepatic microcirculation in mice. Exp Gerontol. 2007;42:789-797.
16. Wisse E. An ultrastructural characterization of the endothelial cell in the rat liver sinusoid under normal and various experimental conditions, as a contribution to the distinction between endothelial and Kupffer cells. J Ultrastruct Res. 1972;38:528-562.
17. Braet F, Wisse E. Structural and functional aspects of liver sinusoidal endothelial cell fenestrae: A review. Comp Hepatol. 2002;1:1.
18. McCuskey RS. The hepatic microvascular system in health and its response to toxicants. Anat Rec (Hoboken). 2008;291:661-671.
19. Le Couteur DG, Cogger VC, Markus AM, et al. Pseudocapillarization and associated energy limitation in the aged rat liver. Hepatology. 2001;33:537-543.
20. McLean AJ, Cogger VC, Chong GC, et al. Age-related pseudocapil-larization of the human liver. J Pathol. 2003;200:112-117.
21. Cogger VC, Warren A, Fraser R, Ngu M, McLean AJ, Le Couteur DG. Hepatic sinusoidal pseudocapillarization with aging in the non-human primate. Exp Gerontol. 2003;38:1101-1107.
22. Warren A, Bertolino P, Cogger VC, McLean AJ, Fraser R, Le Couteur DG. Hepatic pseudocapillarization in aged mice. Exp Gerontol. 2005; 40:807-812.
23. McCourt PA, Smedsrod BH, Melkko J, Johansson S. Characterization of a hyaluronan receptor on rat sinusoidal liver endothelial cells and its functional relationship to scavenger receptors. Hepatology. 1999; 30:1276-1286.
24. Politz O, Gratchev A, McCourt PA et al. Stabilin-1 and-2 constitute a novel family of fasciclin-like hyaluronan receptor homologues. Bio-chem J. 2002;362:155-164.
25. Smedsrod B, Pertoft H. Preparation of pure hepatocytes and reticu-loendothelial cells in high yield from a single rat liver by means of Percoll centrifugation and selective adherence. J Leukoc Biol. 1985; 38:213-230.
26. Mego JL, Bertini F, McQueen JD. The use of formaldehyde-treated 131-I-albumin in the study of digestive vacuoles and some properties of these particles from mouse liver. J Cell Biol. 1967;32:699-707.
27. McDowell EM, Trump BF. Histologic fxatives suitable for diagnostic light and electron microscopy. Arch Pathol Lab Med. 1976;100:405-414.
28. Hansen B, Longati P, Elvevold K, et al. Stabilin-1 and stabilin-2 are both directed into the early endocytic pathway in hepatic sinusoidal endothelium via interactions with clathrin/AP-2, independent of li-gand binding. Exp Cell Res. 2005;303:160-173.
29. Abramoff MD, Magelhaes P.J., Ram S.J. Image processing with ImageJ. Biophotonics Int. 2004;11:36-42.
30. Miller RA, Nadon NL. Principles of animal use for gerontological research. J Gerontol A Biol Sci Med Sci. 2000;55:B117-B123.
31. Le Couteur DG, Fraser R, Hilmer S, Rivory LP, McLean AJ. The hepatic sinusoid in aging and cirrhosis: Effects on hepatic substrate disposition and drug clearance. Clin Pharmacokinet. 2005;44:187-200.
32. Birtwistle MR, Kholodenko BN. Endocytosis and signalling: A meeting with mathematics. Mol Oncol. 2009;3:308-320.
33. Dittmer A, Dittmer J. Beta-actin is not a reliable loading control in Western blot analysis. Electrophoresis. 2006;27:2844-2845.
34. Schmucker DL. Age-related changes in liver structure and function: Implications for disease? Exp Gerontol. 2005;40:650-659.
35. Butler JM, Begg EJ. Free drug metabolic clearance in elderly people. Clin Pharmacokinet. 2008;47:297-321.
36. Hughes DA, Fraser IP, Gordon S. Murine macrophage scavenger receptor: In vivo expression and function as receptor for macrophage adhesion in lymphoid and non-lymphoid organs. Eur J Immunol. 1995;25:466-473.
37. Malerod L, Juvet K, Gjoen T, Berg T. The expression of scavenger receptor class B, type I (SR-BI) and caveolin-1 in parenchymal and nonparenchymal liver cells. Cell Tissue Res. 2002;307:173-180.
38. Zhou B, Weigel JA, Fauss L, Weigel PH. Identifcation of the hyaluronan receptor for endocytosis (HARE). J Biol Chem. 2000;275:37733-37741.
39. Adachi H, Tsujimoto M. FEEL-1, a novel scavenger receptor with in vitro bacteria-binding and angiogenesis-modulating activities. J Biol Chem. 2002;277:34264-34270.
40. Ling W, Lougheed M, Suzuki H, Buchan A, Kodama T, Steinbrecher UP. Oxidized or acetylated low density lipoproteins are rapidly cleared by the liver in mice with disruption of the scavenger receptor class A type I/II gene. J Clin Invest. 1997;100:244-252.
41. Suzuki H, Kurihara Y, Takeya M, et al. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature. 1997;386:292-296.
42. Van Berkel TJ, Van Velzen A, Kruijt JK, Suzuki H, Kodama T. Uptake and catabolism of modifed LDL in scavenger-receptor class A type I/II knock-out mice. Biochem J. 1998;331(Pt 1):29-35.
43. Hansen B, Arteta B, Smedsrod B. The physiological scavenger receptor function of hepatic sinusoidal endothelial and Kupffer cells is independent of scavenger receptor class A type I and II. Mol Cell Biochem. 2002;240:1-8.
44. Matsumoto K, Sano H, Nagai R, et al. Endocytic uptake of advanced glycation end products by mouse liver sinusoidal endothelial cells is mediated by a scavenger receptor distinct from the macrophage scavenger receptor class A. Biochem J. 2000;352(Pt 1):233-240.
45. Nakajou K, Horiuchi S, Sakai M, et al. CD36 is not involved in scavenger receptor-mediated endocytic uptake of glycolaldehyde-and methylglyoxal-modifed proteins by liver endothelial cells. J Biochem. 2005;137:607-616.
46. O'Reilly JN, Cogger VC, Le Couteur DG. Old age is associated with ultrastructural changes in isolated rat liver sinusoidal endothelial cells. J Electron Microsc. 2009;59:65-69.
47. Martinez I, Nedredal GI, Oie CI, et al. The infuence of oxygen tension on the structure and function of isolated liver sinusoidal endothelial cells. Comp Hepatol. 2008;7:4.
48. DeLeve LD, Wang X, Hu L, McCuskey MK, McCuskey RS. Rat liver sinusoidal endothelial cell phenotype is maintained by paracrine and autocrine regulation. Am J Physiol Gastrointest Liver Physiol. 2004;287:G757-G763.
49. Sorensen KK, Melkko J, Smedsrod B. Scavenger-receptor-mediated endocytosis in endocardial endothelial cells of Atlantic cod Gadus morhua. J Exp Biol. 1998;201:1707-1718.
50. Speilberg L, Evensen O, Nafstad P. Liver of juvenile Atlantic salmon, Salmo salar L.: A light, transmission, and scanning electron microscopic study, with special reference to the sinusoid. Anat Rec. 1994;240:291-307.
51. Sorensen KK, Tollersrud OK, Evjen G, Smedsrod B. Mannose-receptor- mediated clearance of lysosomal alpha-mannosidase in scavenger endothelium of cod endocardium. Comp Biochem Physiol A Mol Integr Physiol. 2001;129:615-630.
52. Dannevig BH, Struksnæs G., Skogh T., Kindberg G.M., Berg T. Endo-cytosis via the scavenger-and the mannose-receptor in rainbow trout (Salmo gairdneri) pronephros is carried out by nonphagocytic cells. Fish Physiol Biochem. 1990;8:228-238.
53. Karpen SJ. Growing old gracefully: caring for the 90-year-old liver in the 40-year-old transplant recipient. Hepatology. 2010;51:364-365.
54. Minor RK, Allard JS, Younts CM, Ward TM, de Cabo R. Dietary interventions to extend life span and health span based on calorie restriction. J Gerontol A Biol Sci Med Sci. 2010;65:695-703.