515
J. Endocrinol. Invest. 34: 515-520, 2011
DOI: 10.3275/7297
ABSTRACT. Thyroid hormone release requires degradation
of thyroglobulin (Tg) by thyroid epithelial cells, which occurs
mainly in the lysosomal pathway following Tg endocytosis.
Non-specific fluid-phase endocytosis is thought to be the
main route of Tg uptake leading to degradation, whereas re-
ceptor-mediated endocytosis is believed to lead to post-en-
docytic pathways other than degradation. To gain more in-
sights into these issues, we investigated handling of Tg by
various cell types. Tg bound similarly to thyroid (FRTL-5, FRT)
and non-thyroid (COS-7, IRPT) cells, indicating the presence
of membrane-binding sites, presumably receptors, in both
cell types. Tg was internalized and degraded by all cells and
degradation paralleled uptake, with the exception of FRTL-
5 cells, in which a lower proportion of Tg was degraded, sug-
gesting that in FRTL-5 cells mechanisms that target Tg to the
various post-endocytic pathways (either receptors or post-
receptorial factors) are differently represented. Immuno-
electronmicroscopy showed a common path of endocytosis
in FRTL-5, COS-7, and IRPT cells, namely the formation of
pseudopods engulfing Tg, followed by internalization and
accumulation of Tg in cytoplasmic vesicles and lysosomes.
The fastest rate was observed in COS-7 cells, probably re-
flecting a lower impact of endocytic receptors. Our findings
suggest that Tg uptake and degradation are not thyroid-spe-
cific, that Tg binding sites exist in different cell types, and
that uptake and/or degradation are differently regulated in
differentiated thyroid cells, presumably because of a differ-
ent impact of endocytic receptors or post-endocytic mecha-
nisms, which are probably responsible for the regulation of
hormone release.
(J. Endocrinol. Invest. 34: 515-520, 2011)
©
2011, Editrice Kurtis
INTRODUCTION
Synthesis and intrathyroidal metabolism of thyroglobu-
lin(Tg)playacrucialroleinthesecretionofthyroidhor-
monesbythyroidepithelialcells(TEC).Tgissynthesized
by TEC and then secreted into the lumen of thyroid fol-
licles, where it undergoes hormone formation by cou-
plingofitstyrosylresidueswithiodide(1).Then,Tgisei-
ther stored into follicles to form the colloid or it is pro-
cessedfurthertoundergodegradationandhormonere-
lease(1).ThemainsiteofTgdegradationisintracellular,
namely the lysosomal pathway, where Tg is partly di-
gestedfollowingitsuptakefromthecolloidbyTEC(2-4).
Inaddition,Tgcanbedegradedwithinthefolliclelumen
by extracellular proteases (5).
In rodents, TEC can internalize Tg by macropinocytosis,
butinmostspecies,includinghumans,uptakeofTgoc-
cursmainlybymicropinocytosis(1,6).Themajorityofin-
vestigatorsagreethatfluid-phasemicropinocytosisisthe
main route of uptake leading to hormone release, be-
cause of the very high concentrations of Tg within the
colloid (1, 6). Thus, fluid-phase uptake is a constitutive
processthatoccursbypassivegradientdiffusionofsub-
stancesthatarehighlyconcentratedinextracellularfluid.
Nevertheless, several studies have shown that also en-
docytic receptors can mediate Tg endocytosis (6). Most
authors believe that receptors contribute hormone re-
leaseonlytoalimitedextentandthattheyaremorelike-
ly to sort Tg molecules to post-endocytic pathways that
do not lead to lysosomal degradation, namely recycling
ortranscytosis,asdemonstratedforsomeofthem(6-14).
Consideringthatfluid-phaseuptakecannotberegulated,
the regulation of hormone release in TEC would be de-
termined by the number and the types of endocytic re-
ceptorsonthecellmembraneand/orbythepresenceof
post-endocyticmechanismsthatdirectTgtothevarious
intracellular pathways. In order to gain more insights in-
totheseissues,weinvestigatedTgbinding,uptake,and
degradationinvariouscellstypes,includingdifferentiat-
edandnon-differentiatedthyroidcells,aswellascellsof
non-thyroid origin. Our findings suggest that Tg uptake
and degradation are not thyroid-specific, that Tg bind-
ing sites exist in different cell types, and that uptake
and/ordegradationaredifferentlyregulatedindifferen-
tiated thyroid cells, presumably because of a different
impactofendocyticreceptorsorpost-endocyticmecha-
nisms,whichareprobablyresponsiblefortheregulation
of hormone release.
MATERIALS AND METHODS
Materials
HumanTg(hTg)waspurifiedfromGraves’diseasepatientsthy-
roids, obtained at surgery upon informed consent. hTg was la-
beled with
125
I-Na (Perkin Elmer, Waltham, MA) using IODO
beads (Pierce, Rockford, IL) (specific activity: 1,500-7,000
cpm/ng). hTg was labeled with 20-nm gold particles as de-
scribed (15). A rabbit anti-Tg antibody was from Axell (West-
bury, NY).
Key-words: Endocytosis, receptor, thyroglobulin, thyroid, thyroid hormone.
Correspondence: M. Marinò, MD, Department of Endocrinology, University of Pisa,
Via Paradisa 2, 56124, Pisa, Italy.
E-mail: michele.marino@med.unipi.it
Accepted May 5, 2010.
First published online October 15, 2010.
Binding, uptake, and degradation of internalized thyroglobulin
in cultured thyroid and non-thyroid cells
R. Botta
1
, S. Lisi
1
, A. Pinchera
1
, A.R. Taddei
2
, A.M. Fausto
3
, F. Giorgi
4
, and M. Marinò
1
1
Department of Endocrinology and Metabolism, University of Pisa, Pisa;
2
Interdepartimental Centre for Electron Microscopy and
3
Department of Environmental Science, University of the Tuscia, Viterbo;
4
Department of Neuroscience, University of Pisa, Pisa, Italy
©
2011, Editrice Kurtis
FOR PERSONAL USE ONLY