Clinical Science and Molecular Medicine (1976) 51, 345-351.
Effects of parathyroid hormone on sodium
and calcium transport in the'dog nephron
R. A. L. SUTTON, N. L. M. W O N G A N D J. H. D I R K S
Renal and Electrotyte Division of the Department of Medicine, McGilI University, and
Royal Victoria Hospital, Montreal, Canada
(Received 12 Junuury 1976)
Summnrv
1. The effect of purified bovine parathyroid hormone on renal tubular reabsorption of sodium and
calcium has been studied by micropuncture in intact
and recently thyroparathyroidectomized dogs.
2. Parathyroid hormone increased the rejection of
sodium and calcium proportionately at the late
proximal tubule in both intact and operated dogs.
3. In both groups of dogs, there was increased
delivery of sodium and calcium to the distal tubule
after the hormone. However, the CaWa ratio decreased, suggesting some selective enhancement of
calcium reabsorption before the superficial distal
puncture site.
4. In the final urine, the CalNa ratio decreased
highly significantly in both groups of dogs, indicating a further selective effect of parathyroid hormone
on calcium reabsorption in or beyond the distal
convoluted tubule.
Key words :calcium, nephron, parathyroid hormone,
sodium.
Introduction
Parathyroid hormone enhances renal tubular reabsorption of calcium in several mammalian species,
thus reducingcalcium clearance(Talmage & Kraintz,
1954; Kleeman, Bernstein, Rockney, Dowling &
Maxwell, 1961). This may be an important mechanCorrespondence: Dr R. A. L. Sutton, G. F. Strong
Laboratory for Medical Rash, Faculty Of Medicine,
U.B.C.,Tenth Avenue and Heather Street, Vancouver. B.C..
Canada V5Z 1M9.
345
ism, in addition to its d u e t effect upon bone,
whereby parathyroid hormone controls the calcium
concentration of extracellular fluid (Biddulph,
Hirsch, Cooper & Munson, 1970; Biddulph &
Gallimore, 1974; Nordin & Peacock, 1969). The site
at which the hormone exerts this effect within the
renal tubule has not been clearly defined, though
stop-flow studies in the dog suggesteda distal tubular
site (Widrow & Levinsky, 1962). Agus, Puschett,
Senesky & Goldberg (1971) showed that parathyroid
hormone inhibits sodium and water reabsorption in
the proximal tubule of the dog and they postulated
that the phosphaturic effect of the hormone resulted
from associated proximal inhibition of phosphate
reabsorption, with little distal reabsorption of this
rejected phosphate. The hormone has, however, been
shown also to inhibit phosphate reabsorption in the
distal nephron (Amiel, Kuntziger & Richet, 1970;
Goldfarb, Beck, Agus & Goldberg, 1974). In micropuncture experiments in the dog, neither we
(Edwards, Baer, Sutton & Dirks, 1972) nor Agus,
Gardner, Beck & Goldberg (1973) observed any
dissociation of d c i u m from sodium transport in the
proximal tubule after parathyroid hormone. Since,
in these experiments, the hormone caused a modest
natriuresis but a fall in the fractional excretion of
calcium, there must clearly be a site (or sites) beyond
the proximal tubule at which parathyroid hormone
selectively enhances the reabsorption of calcium over
sodium. The purpose of the present study !was to
define more precisely the site of this action of parathyroid hormone by observing the effects of exoand distal
genous (bovine) hornone at the
tubule in intact and thyroparathyroidectomizeddogs.
R. A. L.Sutton, N. L. M . Wong and J. H.Dirks
346
Methods
Experiments were performed on seventeen intact and
eighteen thyroparathyroidectomized mongrel dogs
weighing 11-16 kg, allowed free access to standard
laboratory Chow and water until the day of the
experiment. Thyroparathyroidectomy was performed
1-3 days before the micropuncture experiment;
animals were maintained on intramuscular injections
of bovine parathyroid hormone (100 units of Lilly
Parathormone daily), which was stopped 24 h before
the micropuncture experiment. Recollection micropuncture techniques and analytical methods were as
previously described from this Laboratory (Edwards,
Baer, Sutton & Dirks, 1973). Late proximal, and
random distal tubules were identified after injection
of FD & C Green dye (Keystone Aniline Chemical
Co., Chicago, U.S.A.) into the renal artery.
Each experiment comprised two phases: phase I
(control) was conducted without prior volume expansion. After collection of micropuncture and
clearance samples, highly purified (Wilson) bovine
parathyroid hormone was added to the inulin infusion. The inulin infusion was maintained at 1
ml/min throughout; the hormone amount was
adjusted to 0.75-1.0 unitlmin. After 60 min of hormone infusion, phase I1 recollection was performed.
Urine samples (15 min) were collected from each
kidney during the periods of micropuncture; blood
samples were taken at the mid-point of the urine
collections. Clearance results from the two kidneys
were similar; only those from the left (micropunctured) kidney are reported. Plasma ultrafiltrates were
prepared with the use of Amicon Centriflo ultrafiltration cones. Tubule fluid samples were analysed
for inulin by the fluorimetric method of Vurek &
Pegram (1966) and for sodium and calcium by the
helium glow photometer (Montreal Polycrafters,
Montreal, Quebec, Canada). The analytical errors
for these micromethods have been previously reported (Edwards et al., 1973). Standard statistical
methods were employed, Student’s t-test being used
to determine the significance of differences between
phases. Standard formulae were used to calculate
fractional reabsorption rates in the various nephron
segments.
Results
Clearance data (Table 1)
In both intact and thyroparathyroidectomized
dogs, parathyroid hormone caused a marked phosphaturia and a significant increase in plasma ultra-
TABLE
1. Renal clearance in intact and thyroparathyroidectomized dogs before (control) and during infusion of
parathyroid hormone
Mean values+ SEM are shown. Abbreviations: n = number of dogs; V = urine flow rate; UN,V, Uc.V = urinary
excretion rates of sodium, calcium; PN.. Pc. = plasma sodium, total calcium concentration; UFc. = calcium
concentration in plasma ultrafiltrate; % UFc. = plasma ultrafiltrable calcium as percentage of total plasma
calcium; FE.,.ter, FEN., FG., FEpl = percentage in urine of filtered load of water, sodium, calcium or inorganic
phosphate; PPr = plasma protein concentration; CI.~II.= inulin clearance.
Intact (n = 17)
Control
Parathyroid
hormone
Operated (n = 18)
P
Control
Parathyroid
hormone
P
~~
V (ml/min)
C I , , ~ ~(ml/min)
~,,
UN.V (pmol/min)
Uc.V @mol/min)
PN. (mmol/l)
Pc. (mmol/l)
UF,. (mmol/l)
% UFc.
FEwater (%)
FEN. (%)
FEc. (%I
FE~JFEN.
FEPl
(%I
PPr (dl)
0.29+ 0.03
293k 1.6
29-1 5.1
0*46+0.09
150k0.7
2.61 f0.04
1.39k0.03
51-6+ 1.3
1.02k0.11
0.70+0*13
1.17k0.23
1*9+02
7 7 + 0.8
52+ 2
+
040k 0.08
27.7+ 1.8
37.1 f7.3
0*28+0.04
151kO-7
2-60f 0.02
1*47+044
55*1+ 1.4
1.41k0.23
0.87f0-17
0.69k0.10
1.2f0.2
20.3+ 2.2
47+ 1
< 0.05
> 0.05
> 0.05
< 0.02
> 0.05
> 0.05
<0.01
< 0.02
<0.02
>0.05
<0.05
<0*001
< 0401
<0.02
0*36+0.08
28.7k2.4
28.0+ 5.2
0.42+ 0.09
146f 1.2
2.09k0.12
1.21+0*06
57.9+ 1.3
1*75+0.52
0*79+0*17
1*28+0*29
2.0k0.3
4.9f 1.6
52+ 1
0.73k0.14
28.2+ 2.8
47.0+ 7.0
0*39+0.05
147+ 1.2
2*17+0.12
1-32+0*07
59-8+ 1.3
3*20+0-72
1*40+0.30
0-94kO.15
0-9fO.l
25.9k2.8
50+ 1
<0.02
> 0.05
< 0.01
> 0.05
> 005
<0.02
<0.001
> 0.05
<0.001
<0*01
>0*05
< 0.001
< 0.001
> 0.05
Parathyroid hormone and renal ion transport
347
TABLE2. Proximal tubule micropuncture results in intact and thyroparathyroidectomized dogs before (control) and during
administration of parathyroid hormone
Mean valuesf SEM are shown. Abbreviations: n = number of tubules; TF/PinUl~.,TF/PN. = ratio of inulin, sodium concentration in tubule fluid to that in plasma; TF/UFc, = ratio of concentration of calcium in tubule fluid to plasma ultrafiltrate; TF/UFcl:~. = ratio of non-reabsorbed Ca:Na (TF/UFC.:TF/PN.); RFN., RFc. = non-reabsorbed fraction of
filtered sodium and calcium arriving at site of late proximal tubule puncture.
~~
Intact
Control
TF/Piouiio
TF/PN.
TF/UFC~
TF/UFc. :N.
RFN. (%I
RFc. (%I
1-49fO.03
0.97f0.01
1.10f0.03
1*13+0*03
65
74
Parathyroid
hormone
1*38+0*04
1-00+0*01
1*07+0*02
1-08fO.03
72
78
Operated
P
n
<0*01
>0*05
>005
~0.05
Control
35
13
13
13
1)
-(
-(I)
1*70+0*07
0*99+0*01
1a 0 8 0.03
+
1*10+0*03
61-2k2.9
67.8f3.9
Parathyroid
hormone
1*51+0.07
0*98+0*01
1.01f 0.03
1*03+0*02
67.0k2.7
69.1f3.3
P
n
<0.02
24
>0*05
>0.05
~0.05
<0*05
~0.05
23
23
23
19
19
") In only six pairs of proximal tubule samples from intact dogs were Na, Ca and inulin determined. The seven additional
paired samples analysed for Na and Ca were not analysed for inulin. Hence the data for rejected fractions of Na and Ca
in this (intact) group were obtained from the mean TF/P~ou,lo,
TF/PN. and TF/UFc. data, and arc not subjected to statistical analysis.
filtrable calcium concentration. Plasma proteins fell
slightly in both groups. Packed cell volume was unchanged in both groups (4244% in intact, 4 2 4 1 %
in operated animals). There was no significant
(P>0.05)change in inulin clearance in either group.
Fractional and absolute excretion of water increased
significantly in both groups. Fractional and absolute
sodium excretion increased slightly in both grows
but this was significant only in operated dogs.
Fractional and absolute calcium excretion decreased
in both groups: this was significant only in intact
dogs. In both groups, the fractional excretion ratio
(FEc./FEN.) fell Significantly, indicating dissociation
of calcium from sodium reabsorption along the
nephron, with relative enhancement of calcium reabsorption.
Micropuncture results
Proximal (Table 2). In both intact and operated
dogs, parathyroid hormone resulted in a significant
fall in proximal TF/PlaaIld1).In neither group of
dogs was a significant change in proximal m/PN.,
TF/UFc. or in Ca/Na ratio observed after parathyroid hormone. Hence rejected fractions of Na and
Ca increased proportionately at the late proximal
(1) Abbreviations: TF/P. ratio of concentrations in tubular
fluid and plasma; FE, fractional excretion; UF, ultraliltrate.
TABLE3. Distal tubule micropuncture results in intact and thyroparathyroidectomized dogs before (control) and during
administration of parathyroid hormone
Mean v a l u e s f s e ~are shown. Abbreviations: see Table 2.
Intact
Control
TFPinulla
TF/PN.
TF/UFca
TF/UFca:~,
RFN. (%I
RFc. (%I
7.63k0.52
0.16f0.01
0.23 & 0.02
1*49fOll
2*40+0*39
3*40+0-51
Parathyroid
hormone
6*39+0-45
0.25f0.02
0.28 f 0.03
1.03+0.06
443&0*57
487f0.74
Operated
P
<0*001
<0*001
<0.05
<0*001
<0*001
<0401
n
Control
Parathyroid
hormone
42
33
31
6.78f0.38
0.19fO-02
0.3 1f 0.02
2.38f0.25
3.14f0.51
4.70f0.38
5.28f0.29
0.26f0.03
0.32f 0.02
1.74f0.19
5.13+0*71
6.67+0.76
30
31
31
P
<0*001
<O-02
>0.05
<0*01
C0.01
COO2
n
45
37
38
35
37
37
R. A . L. Sutton, N.L. M. Wong and J . H. Dirks
...
T
t
T
IProumalI tubule
FIG.I. Fraction of filtered load of sodium and calcium reaching the distal puncture site (above) and final urine (below) in
(a) intact and (b) thyroparathyroidectomized dogs before and
after administration of parathyroid hormone. Each pair of
columns shows the mean fractional delivery of the ion in the
control phase (left column) and after administration of hormone (right column). Open columns show sodium; stippled
columns show calcium (mean values+_sEMare shown). * Significant change after parathyroid hormone (P<0.05).
puncture site in both groups of dogs, though the increase in calcium rejection was not significant in the
operated dogs.
Distal (Table 3, Fig. 1 and Fig. 2). There was a
significant fall in TF/Plnulln
at the distal puncture site
in both intact and operated dogs after administration of parathyroid hormone. TF/PN,also increased
significantly in both groups; TF/UFc. increased
significantly in intact, but not in operated dogs.
In Table 3 and Fig. 1 are shown the fractions of
filtered sodium and calcium reaching the distal
puncture site. Both sodium and calcium delivery increased significantly after parathyroid hormone in
both groups of dogs.
Fig. 2 shows the ratio of non-reabsorbed Ca/Na
at the proximal and distal puncture sites and in the
final urine in both groups of dogs. The Ca/Na ratio
remained close to 1.1 under all conditions at the late
proximal tubule. At the distal tubule, Ca/Na ratio
was lower in intact than in operated dogs (1.49 vs.
2.38) and fell in both groups after parathyroid hormone (to 1.03 and 1.74 respectively), indicating a
preferential effect of the hormone upon calcium reabsorption before the distal puncture site.
In the final urine, the Ca/Na ratio fell proportionately more (1.9 to 1.2 in intact and 2.0 to 0.9 in
I
I
Distd tubule
find urine
FIG. 2. Ratio of non-reabsorbed calcium to sodium at the
proximal and distal tubule and in the final urine in intact ( 0 )
and thyroparathyroidectomized ( 0 ) dogs before and after
administration of parathyroid hormone. Mean values+ SBM
are shown.
operated dogs), indicating continuation of the selective effect of the hormone on calcium reabsorption
into the terminal nephron segment. This comparison
of micropuncture data with urine data (Fig. 1 and
Fig. 2) ignores the possibility of relative differences
in sodium and calcium transport in superficial and
deep nephrons. If such differences existed, then the
observed changes in Ca/Na ratio could result from
an altered distribution of glomerular filtration between superficial and deep glomeruli after parathyroid hormone, rather than a selectiveenhancement of
calcium transport within individual nephrons.
Since the punctured distal tubules in these experiments were unselected, and presumably included
early and late superficial convolutions, it is not
possible to be certain whether an effect beyond the
distal puncture site is occurring in the late distal
tubule, in the collecting duct, or in both.
Discussion
Parathyroid hormone reduces renal calcium clearance in the dog (Widrow & Levinsky, 1962), the rat
(MacIntyre, Boss & Troughton, 1963) and in man
(Edwards & Hodgkinson, 1965). The stop-flow
studies of Widrow & Levinsky (1962) suggested that
this effect of parathyroid hormone was mediated in
the distal nephron and the microperfusion study of
Frick, Rumrich, Ullrich & Lassiter (1965) showed no
effect of parathyroid hormone upon proximal calcium reabsorption. More recently, parathyroid hor-
Parathyroid hormone and renal ion transport
mone has been shown to result in proportionate r e
jection of water, sodium and calcium from the proximal tubule (Agus et ul., 1973), again suggesting that
there must be selective enhancement of calcium reabsorption at a more distal site. The present study
sought to localize this effect within the distal nephron
by micropuncture methods in the dog, as no such
specilic information is available.
In both intact and thyroparathyroidectomized
dogs, parathyroid hormone caused a significant fall
in the ratio of fractional excretion of calcium to
sodium, indicating preferential enhancement of calcium reabsorption. In both experimental groups in
the control phase this ratio was about 2.0. During
marked diuresis, produced by volume expansion, the
ratio usually approaches 1.0 (Walser, 1961). In these
hydropenic animals the higher urinary CalNa ratio
presumably reflects the diet before the experiment.
Furthermore, a concentrated urine may itself favour
a high Ca/Na ratio, owing to the higher concentrations of calcium-complexing anions in such urine
(Walser, 1961). The mean fractional excretion of
calcium in the control phase was somewhat higher in
the intact than in operated dogs: this may result from
dietary differences, the lower urine output in intact
dogs, and the lower mean plasma calcium concentration in operated dogs, which would itself tend to reduce fractional excretion of calcium.
In the proximal tubule after parathyroid hormone
there was increased fractional rejection of water,
sodium and calcium in intact and operated dogs.
Although plasma protein fell significantly in the
intact dogs, but not in the operated dogs, packed cell
volume was unchanged after parathyroid hormone in
both groups. Thus the fall in proximal TF/Pl,~lllin
the second phase is probably not related to volume
expansion. The ratio of non-reabsorbed calcium to
sodium was about 1.1 in both intact and operated
dogs, and did not change after parathyroid hormone.
Similar proximal Ca/Na ratios after parathyroidectomy have been reported previously in the dog (Beck
& Goldberg, 1973; Quamme, Wong, Sutton &
Dirks, 1975) and rat (Buerkert, Marcus & Jamison,
1972). However, Kuntziger, Amiel, Roinel & Morel
(1974) have reported a much higher proximal
TF/UFc. ratio in the rat (1.64) 8 h after parathyroidectomy, falling to 1.30 after infusion of cyclic AMP.
The suggestion by these authors that parathyroid
hormone may selectively enhance proximal calcium
re-absorption is at variance with the present data.
At the distal tubule, in both experimental groups,
349
delivery of water, sodium and calcium increased after
parathyroid hormone. This presumably resulted in
part from the inhibition of proximal reabsorption,
but may in addition reflect an inhibitory effect of the
hormone on sodium and calcium reabsorption in the
intervening (loop) segment. The significant fall in
distal Ca/Na ratio after parathyroid hormone indicates that calcium reabsorption was inhibited less
than sodium in the intervening segment, or altematively that parallel effects in the loop may be followed
by selective enhancement of calcium reabsorption in
the distal tubule before the distal puncture site. The
proportionately greater fall in Cams ratio in the
final urine than at the distal tubule suggests that a
major part of the selective enhancement of calcium
over sodium reabsorption produced by parathyroid
hormone is mediated in the terminal nephron segment, beyond the random distal tubule puncture site.
Such an effect might be within the distal tubule itself,
or in the collecting duct, or both. Agus, Chiu &
Goldberg (1975) have recently reported studies in the
rat which indicate that, after parathyroidectomy,
there is a selective impairment of calcium reabsorption in the nephron segment beyond the late distal
tubule, that is, presumably, in the collecting duct.
It is of interest that a major effect of parathyroid
hormone on calcium reabsorption appears to be in
the terminal nephron. The phosphaturic effect of the
hormone appears to be in part a proximal tubule
effect. However, there is strong evidence that it also
inhibits phosphate reabsorption in the distal tubule
(Amiel et al., 1970), and Knox, Haas & Lechene
(1975) have recently reported data from papillary
micropuncture in the hamster suggesting an effect
within the collecting duct.
Chabardks, Imbert, Cligne, Montegut & Morel
(1975) have recently demonstrated the presence of
parathyroid hormone-sensitiveadenylcyclase activity
in several segments of the rabbit nephron: the proximal convoluted tubule and pars recta, the thick
ascendinglimb of Henle's loop, the distal convoluted
tubule and the first, branched portion of the collecting duct. These authors suggest that the ascending
limb may be the site at which parathyroid hormone
enhancescalcium reabsorption; our data suggest that
the distal convoluted tubule and/or collecting duct
are more likely sites. Although there is good evidence
that the phosphaturic effect of the horhone is
mediated via stimulation of cortical adenyl cyclase
(Agus et al., 1971) the evidence that enhancement of
calcium reabsorption is also mediated via cyclic AMP
350
R. A . L. Sutton, N.L. M. Wong and J. H. Dirks
is less definite. Neither the infusion of cyclic AMP
in the rat (Kuntziger et al., 1974) nor of dibutyryl
cyclic AMP in the dog (Agus etal., 1973) significantly
reduced fractional urinary excretion of calcium.
Several factors have been shown to favour calcium
over sodium reabsorption in the distal nephron, including acetazolamide (Beck & Goldberg, 1973),
chlorothiazide (Edwards et al., 1973), bicarbonate
infusion (Sutton, Wong & Dirks, 1975a) and 25hydroxycholecalciferol (Sutton, Wong & Dirks,
1975b). It has even been suggested (Beck & Goldberg, 1973) that the distal nephron has an intrinsic
capacity to reabsorb all the extra calcium delivered
to it as a result of proximal inhibition, whereas some
of the sodium tends to escape reabsorption. However, bicarbonate infusion (Sutton et al., 1975a),
chlorothiazide (Costanzo & Weiner, 1974), 25hydroxycholecalciferol (Sutton et al., 1975b) and
parathyroid hormone can, under certain circumstances, actually enhance overall tubular reabsorption of calcium, despite some proximal inhibition. It
is not clear whether each of these agents acts upon
the same calcium transport process in the distal
nephron and collecting duct. Chlorothiazide, parathyroid hormone and bicarbonate infusion have in
common the production of increased distal delivery
of bicarbonate ion; it is possible that they mediate
their selective effect upon calcium reabsorption as a
result of this increased distal bicarbonate delivery or
of increased distal intraluminal pH.
Acknowledgments
The authors gratefully acknowledgethe expert technical assistance of Mrs Antoinette Ollbrich, Mrs Alison
Redensek and Mrs Evelyn Rubin. This study was
supported by the Medical Research Council (Canada)
grant MA-5279 to R.A.L.S. and MT 1915 to J.H.D.
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