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. 2021 Oct 11;12:757469. doi: 10.3389/fphys.2021.757469

TABLE 1.

Tissue turnover products cleared from blood mainly by LSECs*, the endocytosis receptor involved in the LSEC uptake, examples of rate of blood clearance of ligands taken up by LSECs following i.v. administration of the ligand, and species examined.

Ligand LSEC receptor References Examples of injected material (dose, inj. site) Species Decay of plasma/blood radioactivity (% eliminated) References
Hyaluronan Stabilin-2a Smedsrød et al., 1984; McCourt et al., 1999; Zhou et al., 2000; Politz et al., 2002 [3H]-hyaluronan (30–32 μg, marginal ear vein) Rabbit t1/2 = 2.5–4.5 min (88% uptake in liver at 19 min after injection) Fraser et al., 1981
125I-tyramine cellobiose (TC)-labeled hyaluronan (MW = 2.5 × 105) (tail vein) Rat t1/2α = 0.9 min (79% uptake in liver at 30 min after injection) Dahl et al., 1988
[3H]-hyaluronan (60–130 μg, cubital vein) Human t1/2 = 2.6-5.5min (90% was eliminated from blood after 10 min) Fraser et al., 1984
Chondroitin sulfate Stabilin-2a Smedsrød et al., 1985b; Harris and Weigel, 2008 [3H]-chondroitin sulfate (CS) and 125I-CS proteoglycan Rat Clearance rate not examined but the main uptake was in LSECs Smedsrød et al., 1985b
Heparin Stabilin-2b Harris et al., 2008, 2009; Øie et al., 2008 125I-FITC-labeled unfractionated heparin (0.1 IU/kg, tail vein) Rat t1/2 = 1.71 min (71% was recovered in liver after 15 min) Øie et al., 2008
Nidogen SR Smedsrød et al., 1989 125I-TC-nidogen (trace amounts, tail vein) Rat t1/2 = 2-3 min (78% was recovered in liver after 1 h) Smedsrød et al., 1989
Alpha chains of types I–V and XI collagen Mannosec receptor Smedsrød et al., 1985a; Smedsrød, 1990; Malovic et al., 2007 125I-FITC-labeled heat-denatured collagen (50 μg, tail vein) Rat t1/2α = 0.8 min (75%) t1/2β = 3.7 min (25%) Hellevik et al., 1996
125I-DTAF-collagen (heat-denatured) (0.04 mg/kg, tail vein) Mouse t1/2α = 0.51 min (90.25%) t1/2β = 36.9 min (9.75%) Malovic et al., 2007
N-terminal propeptide of types I and III procollagen (PINP and PIIINP) SR. Stabilin-2 Smedsrød, 1988; Melkko et al., 1994 125I-TC-PINP (5 μg, tail vein) Rat t1/2α = 0.59 min (78.5%) t1/2β = 3.3 min (21.5%) Melkko et al., 1994
C-terminal propeptide of type I procollagen (PICP) Mannose receptor Smedsrød et al., 1990a 125I-TC-PICP (10 μg, tail vein) Rat t1/2 = 8.7 min Smedsrød et al., 1990a
Tissue plasminogen activator (tPA) Mannose receptor Smedsrød and Einarsson, 1990 125I-tPA (1 μg, tail vein) Rat t1/2α = 0.6 min (65%) t1/2β = 6.4 min (35%) Smedsrød and Einarsson, 1990
Lysosomal enzymes Mannose receptor Hubbard et al., 1979; Isaksson et al., 1983; Elvevold et al., 2008a 125I-cathepsin (10 μg, tail vein) Mouse t1/2α = 0.9 min (63%) t1/2β = 8.9 min (37%) Elvevold et al., 2008a
125I-glycosyl asparaginase (trace amounts, tail vein) Rat t1/2α = 0.7 min (63%) t1/2β = 3.3 min (37%) Smedsrød and Tollersrud, 1995
125I-α-mannosidase (trace amounts, jugular vein) Pig t1/2 = 5 min (about 60% was recovered in liver, and 18% in lung after 1 h) Nedredal et al., 2003
Formaldehyde-treated serum albumin (FSA)d SR. Stabilin-1, and stabilin2 Blomhoff et al., 1984; McCourt et al., 1999; Li et al., 2011 125I-FSA (0.1 mg, femoral vein) Rat 70% was recovered in LSECs 12 min post injection Blomhoff et al., 1984
125I-FSA (2 μg, tail vein) Mouse t1/2 = approximately 1–2 mine (77% was recovered in liver after 10 min) Elvevold et al., 2008a
125I-TC-FSA (trace amounts, jugular vein) Pig t1/2 = 2 min (about 53% was recovered in liver, and 26% in lung after 1 h) Nedredal et al., 2003

A more complete overview of macromolecular ligands removed from the circulation by LSECs is presented in Sørensen et al. (2012, 2015). SR, scavenger receptor.

aThe receptor was named the hyaluronan receptor until 1999 when it was found that scavenger receptor (SR) ligands and hyaluronan (HA) bound to the same receptor on LSECs (McCourt et al., 1999). The receptor was later named stabilin-2 (Politz et al., 2002) [aka HARE (Zhou et al., 2000), FEEL-2 (Tamura et al., 2003)].

bHeparin was found to be a ligand for human stabilin-2 in Harris et al. (2008), and an antibody to the receptor partly inhibited binding of heparin in rat LSECs (Harris et al., 2009) whereas another study in rat did not find heparin binding to stabilin-2 (Øie et al., 2008).

cUptake of collagen alpha-chains was until 2007 thought to occur via a distinct collagen receptor in LSECs. In 2007 it was found that this receptor was identical to the mannose receptor (Malovic et al., 2007). Binding of denatured collagen/collagen alpha-chains occur via the fibronectin type II domain in this receptor (Martinez-Pomares et al., 2006; Napper et al., 2006).

dFSA is a non-physiological ligand that is much used in studies of LSEC function. It is an SR ligand and is internalized both via stabilin-1 and stabilin-2 in LSECs (McCourt et al., 1999; Li et al., 2011).

eThe rate of elimination of 125I-FSA from blood was not calculated in Elvevold et al. (2008a) but from the decay curve in Figure 5 of that reference we have estimated that that about 50% of the radioactivity in blood at 1 min post injection was eliminated after 2 min and more than 80% was eliminated after 5 min.