Function of the Collecting Ducts
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1 Funtion of the Colleting Duts By KARL J. ULLRICH, M.D. Urine was sampled from miroatheters situated at different levels of the olleting duts of golden hamsters. Appropriate analyses provided data onerning the funtion of the olleting duts with respet to onentrating and aidifying the urine. The onlusion is reahed that the olleting duts serve 2 funtions: a passive one, i.e., the bak-diffusion of water and urea and an ative one, i.e., the exhange of sodium for hydrogen ions and the formation of ammonia. HEIDENHAIN1 la in 187 injeted indigo armine into intat animals and found a strong onentration of olor in the olleting duts. His explanation was that there is relatively more urine in the olleting duts and that some preipitated dye is olleted by oagulation in a manner analogous to sand being swept along by a stream. He attributed no speial funtion to the ells of the olleting duts beause of their lear appearane. This interpretation was aepted for 70 years. In 199 Vimtrup,2 in the laboratory of Bodil and Knut Shmidt-Nielsen, repeated experiments with dyes on Heteromyidae whose olleting duts are very long and a good subjet for experimental study. He onluded that the urine beomes onentrated as it flows through the olleting duts. In 1931 Hargitay and Kuhn3 published their ounterurrent hypothesis, showing by experiments performed in onjuntion with Wirz, that the urine was onentrated in the olleting duts. To obtain more information about the funtion of olleting duts, Hilger, Kliimper, Eigler, Pehling and Ullrih5-8 atheterized the olleting duts of golden hamsters, whose papillae are easily aessible from the renal pelvis. The experimental proedure was as follows: 2 polyethylene miroatheters were passed from the renal pelvis into 2 olleting duts, the tips reahing different levels. Both samples of urine whih were obtainied in this From the Physiologial Institute, University of Gottingen, Gottingen, Germany. Dr. Ullrih is presently a Researh Assoiate, Department of Zoology, Duke University, Durham, N. C. 869 way were analyzed with respet to the depressions of the freezing point and the onentrations of inulin, sodium, and potassium. The results are plotted in figure 1. In 33 ases, the onentration of inulin in urine from the superfiially plaed atheter averaged 1.5 times that from the deeper one. In a seond series of animals with higher urinary osmoti pressure, the mean inrease was threefold. If it is assumed that the inrease in inulin onentration is due to the reabsorption of water, the results of both series indiate that between one-third and two-thirds of the water flowing into the portions of the olleting duts under onsideration is reabsorbed. If water alone is reabsorbed from the fluid of the olleting duts, the inrease in osmoti pressure ought to parallel the inrease in the onentration of inulin. But (fig. 2), suh parallelism was not observed: the real osmoti pressures inrease with muh less of a slope. From this disrepany one an onlude that some solutes must be reabsorbed too, thereby making the osmoti pressure of the reabsorbed solution equal to about two-thirds of that of the solution flowing into the orresponding segment of the olleting duts. In other experiments, Kliimper, Ullrih, and Hilger6 measured the onentrations of inulin alnd urea in samples obtained from miroatheterization of olleting duts. In all eases the inerease in the onentration of inulin exeeded that of urea. The ratios of the rate of inrease in the onentration of urea to the rate of inrease in the onentration of inulin varied from 0.37 to 0.97, with an average of These data indiate that the eon-
2 870 ITTLLRICH Vl t, 30 2,6 26 2, 2,2 2,0,6 a- a a Q 1,21 li L.) --Smm du/iere Morkzone innere Morkzone spitze au/iere Morkzone Figure 1 Relative hanges in the onentrations of inulin in the urine within the olleting dut, and the orresponding reabsorption of water. The data illustrated on the right side of the figure are from animals exreting a more onentrated urine than those on the left. On the absissa are plotted the distanes of sampling points from the tip of the papilla. The straight lines represent the values of the simultaneously gained samples. Data taken from Hilger, Kliimper and Ullrih.5 entration of urea in the reabsorbed solution is approximately half the onentration of the fluid flowing into the partiular segment of the olleting dut from whih samples were obtained. What hanges our in the eletrolytes during the passage of urine through the olleting duts? On the average, the inreases in the onentrations of potassium parallel the inreases in the onentrations of inulin.5 This supports the view that potassium is onentrated only by reabsorption of water in the olleting duts of the inner medullary region. The onentrations of sodium in the urine, however, fall as the urine passes through the olleting duts.5 As may be seen in figure 3, there is a steep slope, with high values for onentration in the outer medullary region. This fat indiates that a great deal of water Omm Papillen - spdtze is reabsorbed from the olleting duts of the ortex and the outer medulla. The sodium onentrations are very low at the papillary tip. Thus, sodium must be reabsorbed from the olleting duts. We may then onlude that the olleting duts an regulate the exretion of sodium by the kidney. But how an this drop in the onentration of sodium be reoniled with the oinidental rise in the osmoti pressure of urine in the same region? Simultaneous measurements of the onentrations of inulin and ammonium by Ullrih, Hilger, and Kliimper8 indiate (fig. ) that ammonium inreases muh more than inulin. Therefore, we may onlude that ammonium ions are sereted into the olleting duts. In onnetion with this observation, it is interesting to note that Rihterih-van Baerle, Goldstein, and Dearborn9 have de-
3 L--I FUNCTION OF THE COLLECTING DUCTS 871 Wasserruikresorption ous den Summelrohren osmol. Urinkonzentrationsveronderufgef (-N) im Verlouf der Somnmelrohrp,ossoge 2/: 7,8 srnol. osmol. 76 7,6 1,6 1,6 1, 1, 17 7, 1,2 7,2 7,2 II 2. 7, lp 7,10 II Qa 08 II 06 Q6 Q6 06 0, t Q2 Q2 02 i "5mm --O 1 0mm -m IN OmnYn 0u1ere hbrkzone innere Markzone Popitlenspitze ouflere Morkzone innere Morkzone Papillenspitze Figure 2 Changes in the osmoti pressure of urine along the ourse of the olleting dut. The data used for the left side of the figure were alulated from the freezing-point depression of urine obtained from the deeper level and the respetive onentrations of inulin in urine from both levels. This hypotheti figure would be expeted if only water were reabsorbed. The observed inreases in osmoti pressure (right) are less. Data taken from Hilger, Kliimp,er and Ullrih.5 K iq/l, _ F w5 I- 100 J som! 3 Z O #ugere o17f_zon7e' Nierelpo,,olle Puoii/fen- A17/ile a b Figure 3 a. Changes in the onentrations of sodium during the passage of urine through the olleting dut (26 experiments on golden hamsters). On the absissa is plotted the distane of the sampling point from the tip of the papilla. b. Changes in the onentrations of potassium during the passage of urine through the olleting dut (23 experiments). (Republished by permission of Pfiiger's Arhiv fur die gesamte Physiologie des Menshen und der Tiere.5) mal
4 872 UlTLRICH >NH II AILJ -+ NH1 r 12 2.).to o 10~ O a z 6 6. If O, Inulin 2 2. osmol Druk n I Ul - 9t ni 1 I Omm 5 3 2, Inulmn,osmol Druk / 0 mm.o I., 0, lz i 5v o ulere Markzone 3) NH + Inulin osmol Druk mm Papiltenspiltze ) I/ / NH+ Inulin osmol Druk _-fj i I. U i i 0 $ 0 v I ou0ere Morkzone, 1 0 mm Papl'ten oile 7spitze Figure Changes in the onentration of ammonia in urine during the passage through the olleting dut ompared with the hanges in the onentration of inulin and in the osmoti pressure in the same sarmples ( representative experiments). Data taken from Hulger, Kliimper and Ullrih.5 sribed a high degree of ativity of glutaminase I in the inner zone of the renal medulla of dogs and rabbits. Moreover, as may be seen in figure 5, aidifiation of urine within the olleting duts was demonstrated by a derease of ph.7 These observations were reently onfirmed by Gottshalk'0 and Giebish,1" who have also shown that aidifiation an take plae in the proximal and distal onvolutions. The present data indiate that there is an exhange of sodium ions for hydrogen ions and a seretion of amumonia in the olleting duts. The findings by the stop-flow method'12-5 are in aord with our results as far as the reabsorption of sodium and the seretion of hydrogen ions and ammonia are onerned. However, a disrepany exists with respet to the site of seretion of potassium. Aording to the stop-flow method, potassium is sereted at the same site as hydrogen ions and ammonia. However, our results indiate that potassium is not sereted in the olletinig duts of the inner medullary region, but that seretion of potassium may our at a site higher up in the olleting duts.
5 FUNCTION OF THE COLLECTING DUCTS L9 2 3fnLuLO 5 :" 3 2 7rr,rO Ma,qrAzone fiefe o'ere 'PuRpiY/ensj;,'ze-rAfoo'zone,7/efe Pu///enflR%/ze Figure 5 The ph of urine drawn simultaneously from the olleting dut at different distanes from the tip of the papilla. The graph on the left represents values of samples withdrawn without speial preautions. The values for the graph on the right were measured at a arbon dioxide tension of 0 mm. Hg. The values at absissa point 0 are values from the other (unexposed) kidney. (Republished by permission of Ergebnisse der Physiologie, Biologishen Chemie uand Experimentellen Pharmakologie.7a) To summarize, the olleting duts seem to have 2 funtions: (1) a passive one, i.e., the bak-diffusion of water and urea, and (2) an ative one, i.e., the exhange of sodium iolns for hydrogen ions and the formation of ammionia. Both funtions, passive and ative, seem to operate independently. It is partieularly surprisinog that the ells of the olletilng duts, whih are exposed to enormous hanges in the onentrations of eletrolytes and urea, and are threatened by an inadequate supply of oxygen and essenitial nutrients as a onsequene of ounterurrent diffusion, are entrusted with suh essential funtions as the exhange of sodium and hydrogen and the seretion of ammonia. 7a Referenes 1. HEIDENHAIN, R.: Mikroskopishe Beitriige zur Anatomie und Physiologie der Nieren. Areh. mikr. Anat. 10: 1, 187. la. -: Versuhe fiber den Vorgang der Harnabsonderung. Pfliugers Arh. ges. Physiol. 9: 1, VIMTRUP, B.: Histologial examinations of kidneys of Heteromyidae. Sandinav. J. Clin. & Lab. Invest. 1: 339, HARGITAY, B., AND KUHN, W.: Das Multiplikationsprinzip als Grundlage der Harnkonzentrierung in der Niere. Ztsehr. Elektrohem. 55: 539, WIRz, H., HARGITAY, B., AND KUHN, W.: Lokalisation des Konzentrierungsprozesses in der Niere durh direkte Eryoskopie. Helvet. physiol. et pharmaeol. ata 9: 196, HILGER, H. H., KLUMPER, J. D., AND ULLRICH,
6 87 ULLRICH K. J.: Wasserrflkresorption und Ionentransport durh die Sammelrohrzellen der Saugetierniere. Pflugers Arh. ges. Physiol. 267: 218, KLfiMPER, J. D., ULLRICH, K. J., AND HILGER, H. H.: Verhalten des Harnstoffs in den Sammelrohren der Saugetierniere. Pfiigers Arh. ges. Physiol. 267: 238, ULLRICH, K. J., EIGLER, F. W., AND PEHLING, G.: Sekretion von Wasserstofflonen in den Sammelrohren der Siaugetierniere. Pfluigers Arh. ges. Physiol. 267: 91, a.-: Das Nierenmark Struktur Stoffwehsel und Funktion. Ergebn. d. Physiol. 50: 33, , HILGER H. H., AND KLt-MPER, J. D.: Sekretion von Ammoniumionen in den Saminelrohren der Saugetierniere. Pfliigers Arh. ges. Physiol. 267: 2, RICHTERICH-VAx BAERLE, R., GOLDSTEIN, L., AND DEARBORN, E. H.: Ammonia prodution in the olleting duts of nmaminalian kidneys. Nature 178: 698, GOTTSCHALK, C. W., LASSITER, W. E., AND MYLLE, M.: Loalization of urine aidifiation in the mammalian kidney. Am. J. Physiol., in press. 11. GIEBISCH, G., WINDHAGER, E. E., AND PITTS, R. F.: Mehanism of urinary aidifiation. In Proeedings of the International Symposium on the Biology of Pyelonephritis. Bostoni, Little, Brown & Co., in press MALVIN, R. L., WILDE, W. S., AND SULLIVAN, L. P.: Loalization of niephron transport by stop flow analysis. Ain. J. Physiol. 19: 135, PITTS, R. F., GuRD, R. S., KESSLER, R. HI., AND HIERHOLZER, K.: Loalization of aidifiation of urine, potassium anid ammonia seretion and phosphate reabsorption in the nephron of the dog. Am. J. Physiol. 19: 125, WILDE, W. S., AN D MALVIN, R. L.: Graphial plaement of tranisport segments along the nephron from urine onentration pattern developed with stop flow tehnique. Am. J. Physiol. 195: 153, KESSLER, R. H., HIERHOLZER, K., GURD, R. S., AND PITTS, R. F.: Loalization of diureti ation of hlormerodrin in the nephron of the dog. Am. J. Physiol. 19: 50, The Animal that Fits In 1926, Marshall, browsing through omparative anatomuy, disovered that a number of fishes had been desribed whih possessed purely tubular kidneys. This fat, of ourse, immediately evoked Marshall's interest in fish urine. Unfortunately, aglonierular fishes were rather rare, but we happened to have one speies, the goosefish, at Salisburv Cove... Work on the aglomerular fishes had been undertaken independentlv by J. G. Edwards in the Naples' laboratory, and within a short time it was lear that this purely tubular kidney, whih does not even possess a signifiant arterial blood supply, but is perfused entirely by venous blood fromi the renal portal vein and at a pressure whih is probably below the osmoti pressure of the plasma proteins, an exrete all the ordinary urinary onstituents So, by 1930, the question of tubular exretion was answered in the affirmative. But, as Rihards said in the disussion when Marshall read a paper at Woods Hole on the aglomerular fish, "At last he has found an animal that fits in with his theory."-h. W. Smith. Letures on the Kidney. Lawrene, Kansas, University of Kansas Press, 193, p. 73.
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