Summary
Previous studies have concluded that a juxtaglomerular apparatus evolved in phylogenetic groups “higher” than elasmobranch fishes. The present study shows for the first time a distinct juxtaglomerular apparatus in four marine elasmobranchs, the spiny dogfish (Squalus acanthias), the smooth dogfish (Mustelus canis), the little skate (Raja erinacea), and the cownose ray (Rhinoptera bonasus). Serial semithin sections of these fishes' kidneys reveal the four morphological components of a juxtaglomerular apparatus at the vascular pole of the renal corpuscle: (1) an afferent arteriole surrounded by smooth muscle cells which have granules containing a material exhibiting a periodic substructure comparable to that of renin granules in higher vertebrates; (2) an efferent arteriole usually devoid of smooth muscle cells but having pericyte-like cells; (3) a macula densa portion of the distal tubule juxtaposed between the afferent and efferent arterioles; and (4) elongated, fusiform cells (Goormaghtigh cells), which are in continuity with similar cells of the abundant intra-glomerular mesangium, and fill the space bordered by the distal tubule and by the afferent and efferent vessels. The distal tubule, from the site where it lies close to the afferent arteriole, moves directly toward the urinary pole, frequently indenting the renal corpuscle. Within this indentation, the tubule may be flanked by the efferent vessel, by the extraglomerular mesangium, or by Bowman's capsule only. Facing these structures the tubular epithelial cells possess basally dilated intercellular spaces. Endothelial cells of the efferent vessel(s) are fenestrated, possessing pores which are closed by a diaphragm. Conclusion: marine elasmobranch fish possess the morphological components of a juxtaglomerular apparatus which suggests that these fishes, like most other vertebrates, possess a renin-angiotensin system and a glomerulartubular feedback mechanism.
Similar content being viewed by others
References
Barajas L (1966) The development and ultrastructure of the juxtaglomerular cell granule. J Ultrastruct Res 15:400–413
Barajas L (1979) Anatomy of the juxtaglomerular apparatus. Am J Physiol 237:F333-F343
Barajas L, Latta H (1963) A three-dimensional study of the juxtaglomerular apparatus in the rat. Light and electron microscopic observations. Lab Invest 12:257–269
Barajas L, Latta H (1965) The development of the juxtaglomerular cell granule. Anat Rec 151:321
Barajas L, Müller J (1980) Structure of the juxtaglomerular apparatus. In: Johnson JA, Anderson RR (eds) The Renin-Angiotensin System. Plenum Press, New York London, pp 85–134
Barajas L, Salido EC, Powers KV (1988) Anatomical basis of the tubuloglomerular feedback mechanism: the juxtaglomerular apparatus. In: Persson AEG, Boberg U (eds) The Juxtaglomerular Apparatus. Elsevier, Amsterdam, pp 7–26
Bean JW (1942a) On the specificity of renin and some related phenomena. Fed Proc 1:6–7
Bean JW (1942b) Specificity in the renin-angiotensinogen reaction. Am J Physiol 136:731–742
Bellocci M, Picardi R, de Martino C (1971) The juxtaglomerular apparatus in the mesonephros of newt (Triturus cristatus). A morphologic study. Z Zellforsch Mikrosk Anat 114:203–219
Biava CG (1967) Ultrastructural observations on the morphogenesis of nonspecific granules in human juxtaglomerular and renal vascular cells. Circ Res 20–21 [Suppl II]: 47–67
Biava CG, West M (1965) Lipofuscin-like granules in vascular smooth muscle and juxtaglomerular cells of human kidneys. Am J Pathol 47:287–313
Biava CG, West M (1966) Fine structure of normal human juxtaglomerular cells. I. General structure and intercellular relationships. Am J Pathol 49:679–721
Bohle A, Walvig F (1964) Beitrag zur vergleichenden Morphologie der epitheloiden Zellen der Nierenarteriolen unter besonderer Berücksichtigung der epitheloiden Zellen in den Nieren von Seewasserfischen. Klin Wochenschr 42:415–421
Cantin M (1983) Morphopathology of the renin-angiotensin system. In: Genest J, Kuchel O, Hamet P, Cantin M (eds) Hypertension, Physiopathology and Treatment. Second Edition, MacGraw-Hill, New York, pp 280–308
Capréol SV, Sutherland LE (1968) Comparative morphology of juxtaglomerular cells. I. Juxtaglomerular cells in fish. Can J Zool 46:249–256
Carroll RG (1981) Vascular response of the dogfish and sculpin to angiotensin II. Am J Physiol 240:R139-R143
Carroll RG, Opdyke DF (1982) Evolution of angiotensin II-induced catecholamine release. Am J Physiol 243:R65-R69
Casellas D (1986) A method for scanning electron microscopic observation of glomerular vascular poles in rat kidneys. J Electron Micr Tech 4:63–64
Chandra S, Skelton FR (1964) Staining juxtaglomerular cell granules with toluidine blue or with basic fuchsin for light microscopy after epon embedding. Stain Technol 39:107–110
Christensen JA, Knutsson S, Bohle A (1982) Granular epithelioid cells in the kidney of the Atlantic salmon (Salmo salar). Kidney Int 22 [Suppl 12]:179–184
Christensen JA, Taugner R, Meyer DS, Boyle A (1987) The granular epithelioid cells in the kidney of the lemon sole (Pleuronectes microcephalus Donovani). Cell Tissue Res 249:137–143
Cook WF, Pickering GW (1958) The location of renin within the kidney. J Physiol 143:78P-79P
Crockett DR, Gerst JW, Blankenship S (1973) Absence of juxtaglomerular cells in the kidneys of elasmobranch fishes. Comp Biochem Physiol 44A:673–675
Dantzler WH (1989) Comparative Physiology of the Vertebrate Kidney. Springer, Berlin
Dibona DR, Kirk KL, Johnson RD (1985) Microscopic investigation of structure and function in living epithelial tissues. Fed Proc 44:2693–2703
Edelman R, Hartroft PM (1961) Localization of renin in juxtaglomerular cells of rabbit and dog through use of the fluorescentantibody technique. Circ Res 9:1069–1077
Edwards JG (1940) The vascular pole of the glomerulus in the kidney of vertebrates. Anat Rec 76:381–389
Faarup P (1971) Morphological aspects of the renin-angiotensin system. Acta Pathol Microbiol Scand [A] [Suppl] 222:1–96
Galen FX, Devaux C, Houot AM, Menard J, Corvol P, Corvol MT, Gubler MC, Mounier F, Camilleri JP (1984) Renin biosynthesis by tumoral juxtaglomerular cells — evidence for a renin precursor. J Clin Invest 73:1144–1155
Gambaryan SP (1987) Structural characteristics of the nephron in marine cartilaginous fish. J Evol Biochem Physiol 23:142–145
Ghouse AM, Parsa B, Boylan JW, Brennan JC (1968) The anatomy, micro-anatomy, and ultrastructure of the kidney of the dogfish, Squalus acanthias. Bull Mt Desert Is Biol Lab 8:22–29
Goormaghtigh N (1940) Histological change in the ischaemic kidney with special reference to the juxtaglomerular apparatus. Am J Path 16:409–416
Hackenthal E, Metz R, Bührle CP, Taugner R (1987) Intrarenal and intracellular distribution of renin and angiotensin. Kidney Int 31 [Suppl 20]:S4-S17
Hartroft PM (1966) “Juxtaglomerular” (JG) cells of the American bullfrog as seen by light and electron microscopy. Fed Proc 25:238
Hartroft PM (1968) The juxtaglomerular complex as an endocrine gland. In: Bloodworth Jr JMB (ed) Endocrine Pathology. Williams and Wilkins, Baltimore, pp 641–677
Hazon N, Balment RJ, Perrott M, O'Toole LB (1989) The reninangiotensin system and vascular and dipsogenic regulation in elasmobranchs. Gen Comp Endocrinol 74:230–236
Henderson JW, Oliver JA, McKeever A, Hazon N (1981) Phylogenetic aspects of the renin-angiotensin system. In: Pethes G, Frenyo VL (eds) Advances in Animal and Comparative Physiology. Pergamon Press, Oxford, pp 355–363
Holcombe RF, Wilde DW, Opdyke DF (1980) Vasomotor tone in the dogfish shark. Comp Biochem Physiol 65A:135–138
Johnson OW (1979) Form and function in birds. In: King AS, McLelland J (eds) Urinary Organs. Academic Press, New York, London, Vol 1, pp 183–235
Kaissling B, Kriz W (1982) Variability of intercellular spaces between macula densa cells: a transmission electron microscopic study in rabbits and rats. Kidney Int 22:S9-S17
Kaley G, Robinson GA, Lubben B (1963) Comparative aspects of the “renin-angiotensin” system. Biol Bull 125:381
Kirk KL, Bell PD, Barfuss DW, Ribadeneira M (1985) Direct visualization of the isolated and perfused macula densa. Am J Physiol 248:F890-F894
Komadinovic D, Krstic R, Bucher O (1978) Ultrastructural and morphometric aspects of the juxtaglomerular apparatus in the monkey kidney. Cell Tissue Res 192:503–512
Krishnamurthy VG, Bern HA (1969) Correlative histologic study of the corpuscles of Stannius and the juxtaglomerular cells of teleost fishes. Gen Comp Endocrinol 13:313–335
Kriz W, Kaissling B (1985) Structural organization of the mammalian kidney. In: Seldin DW, Giebisch G (eds) The Kidney: Physiology and Pathophysiology. Raven Press, New York, pp 265–306
Lacy ER, Reale E (1985 a) The elasmobranch kidney. I. Gross anatomy and general distribution of the nephrons. Anat Embryol 173:23–34
Lacy ER, Reale E (1985 b) The elasmobranch kidney. II. Sequence and structure of the nephrons. Anat Embryol 173:163–186
Lacy ER, Reale E (1989) Granulated peripolar epithelial cells in the renal corpuscle of marine elasmobranch fish. Cell Tissue Res 257:61–67
Lacy ER, Reale E, Schlusselberg DS, Smith WK, Woodward DJ (1985) A renal countercurrent system in marine elasmobranch fish: a computer-assisted reconstruction. Science 227:1351–1354
Lacy ER, Castellucci M, Reale E (1987) The elasmobranch renal corpuscle: fine structure of Bowman's capsule and the glomerular capillary wall. Anat Rec 218:294–305
Lagios MD (1974) Granular epithelioid (juxtaglomerular) cell and renovascular morphology of the coelacanth Latimeria chalumnae Smith (Crossopterygii) compared with that of other fishes. Gen Comp Endocrinol 22:296–307
Lamers APM, van Dongen WJ, van Kemenade JAM (1973) The morphology of the juxtaglomerular apparatus in the toad, Bufo bufo. A light microscopic study. Z Zellforsch Mikrosk Anat 138:545–555
Lamers APM, van Dongen WJ, van Kemenade JAM (1974a) A ultrastructural study of the juxtaglomerular apparatus in the toad, Bufo bufo. Cell Tissue Res 153:449–464
Lamers APM, van Dongen WJ, van Kemenade JAM, Speijers GJA (1974b) A macula densa-like structure in the kidney of the toad Bufo bufo. Gen Comp Endocrinol 22:355
Lamers APM, Verhofstad AAJ, Stadhouders AM, Michelakis AM (1985) Immunohistochemical demonstration of renin in the juxtaglomerular apparatus of three Bufo species. Cell Tissue Res 239:677–682
Latta H, Maunsbach AB (1962) The juxtaglomerular apparatus as studied electron microscopically. J Ultrastruct Res 6:547–561
Lindop GBM, Lever AF (1986) Anatomy of the renin-angiotensin system in the normal and pathological kidney. Histopathology 10:335–362
Malick LE, Wilson B, Stetson D (1975) Modified thiocarbohydrazide procedure for scanning electron microscopy: routine use for normal, pathological or experimental tissues. Stain Technol 50:265–269
McKelvey RW (1963) The presence of a juxtaglomerular apparatus in non-mammalian vertebrates. Anat Rec 145:259–260
McManus JFA (1942) The juxtaglomerular complex. Lancet 2:394–396
McManus JFA (1943) Apparent reversal of position of the Golgi element in the renal tubule. Nature 152:417
McManus JFA (1947) Further observations on the glomerular root of the vertebrate kidney. Q J Microsc Sci 88:39–44
Morild I, Bohle A, Christensen JA (1985 a) Structure of the avian kidney. Anat Rec 212:33–40
Morild I, Mowinckel R, Bohle A, Christensen JA (1985 b) The juxtaglomerular apparatus in the avian kidney. Cell Tissue Res 240:209–214
Movat HZ (1961) Silver impregnation methods for electron microscopy. Am J Clin Pathol 35:528–537
Nash J (1931) The number and size of glomeruli in the kidneys of fishes, with observations on the morphology of the renal tubules of fishes. Am J Anat 47:425–445
Nishimura H (1980 a) Comparative endocrinology of renin and angiotensin. In: Johnson JA, Anderson RR (eds) The Renin-Angiotensin System. Plenum Press, New York London, pp 29–77
Nishimura H (1980 b) Evolution of the renin-angiotensin system. In: Pang PKT, Epple A (eds) Evolution of Vertebrate Endocrine System. Texas Tech Press, Lubbock, Texas, pp 373–404
Nishimura H, Ogawa M (1973) The renin-angiotensin system in fishes. Am Zool 13:823–828
Nishimura H, Oguri M, Ogawa M, Sokabe H, Imai M (1970) Absence of renin in kidneys of elasmobranchs and cyclostomes. Am J Physiol 218:911–915
Nishimura H, Ogawa M, Sawyer WH (1973) Renin-angiotensin system in primitive bony fishes and a holocephalian. Am J Physiol 224:950–956
Ogawa M, Hirano T (1982) Studies on the nephron of a freshwater stingray, Potamotrygon magdelenae. Zool Mag 91:101–105
Ogawa M, Oguri M, Sokabe H, Nishimura H (1972) Juxtaglomerular apparatus in the vertebrates. Gen Comp Endocrinol [Suppl 3]:374–381
Oguri M (1978) Presence of juxtaglomerular cells in the holocephalian kidney. Gen Comp Endocrinol 36:170–173
Oguri M, Ogawa M, Sokabe H (1970) Absence of juxtaglomerular cells in the kidneys of Chondrichthyes and Cyclostomi. Bull Jap Soc Scient Fish 36:881–884
Okkels H (1950) La zone angiotrope du segment III du tube urinaire des Mammifères. Observations cytologiques de la région dénommée “macula densa” de l'apparail urinaire. Bull Histol Appl 27:145–148
Opdyke DF, Holcombe R (1976) Response to angiotensins I and II and to AI-converting-enzyme inhibitor in a shark. Am J Physiol 231:1750–1753
Opdyke DF, Holcombe RF (1978) Effect of angiotensins and epinephrine on vascular resistance of isolated dogfish gut. Am J Physiol 234:R195-R200
Opdyke DF, Carroll RG, Keller NE, Taylor AA (1981) Angiotensin II releases catecholamines in dogfish. Comp Biochem Physiol 70C: 131–134
Riedel B, Bucher O (1967) Die Ultrastruktur des juxtaglomerularen Apparates des Meerschweinchens. Z Zellforsch Mikrosk Anat 79:244–258
Rosivall L, Taugner R (1986) The morphological basis of fluid balance in the interstitium of the juxtaglomerular apparatus. Cell Tissue Res 243:525–533
Rosivall L, Taugner R (1988) Fluid balance in the interstitium of the Goormaghtigh cell field. In: Persson AEG, Boberg U (eds) The Juxtaglomerular Apparatus. Elsevier, Amsterdam, pp 39–49
Ryan GB, Coghlan JP, Scoggins BA (1979) The granulated peripolar epithelial cells: a potential secretory component of the renal juxtaglomerular complex. Nature 277:655–656
Saladino AJ, Trump BF (1963) Evidence for the structural heterogeneity of the granules in the juxtaglomerular cells of the rabbit kidney; electron microscopic observations. Anat Rec 145:279
Schaechtelin G, Riedel B (1966) Renin-Aktivität in Nieren ohne “Renin-Granula”. Naunyn-Schmiedebergs Arch Pharmak Exp Pathol 255:65–66
Schloss G (1946) Der Regulationsapparat am Gefässpol des Nierenkörperchens in der normalen menschlichen Niere. Acta Anat 1:365–410
de Senarclens CF, Pricam CE, Banichahi FD, Vallaton MB (1977) Renin synthesis storage and release in the rat: morphological and biochemical study. Kidney Int 11:161–169
Sikri KL, Foster CL (1981) Light and electron microscopical observations on the macula densa of the Syrian hamster kidney. J Anat 132:57–69
Siller WG (1971) Structure of the kidney. In: Bell DJ, Freemann BM (eds) Physiology and Biochemistry of the Domestic Fowl, vol 1. Academic Press, New York London, pp 197–231
Simpson FO (1963) Crystalline structure of juxtaglomerular granules, as shown by electron microscopy. Proc Univ Otago Medical School 41:51
Sokabe H (1974) Phylogeny of the renal effects of angiotensin. Kidney Int 6:263–271
Sokabe H, Ogawa M (1974) Comparative studies of the juxtaglomerular apparatus. Int Rev Cytol 37:271–327
Sokabe H, Ogawa M, Oguri M, Nishimura H (1969) Evolution of the juxtaglomerular apparatus in the vertebrate kidneys. Texas Rep Biol Med 27:867–885
Sokabe H, Pang PKT, Gorbman A (1978) Some frontiers in comparative studies of the renin-angiotensin system. Jpn Heart J 19:783–790
Spanidis A, Wunsch H, Kaissling B, Kriz W (1982) Three-dimensional shape of a Goormaghtigh cell and its contact with a granular cell in the rabbit kidney. Anat Embryol 165:239–252
Taugner R, Hackenthal E (1989) The juxtaglomerular apparatus: structure and function. Springer, Berlin
Taugner R, Metz R (1986) Development and fate of the secretory granules of juxtaglomerular epithelioid cells. Cell Tissue Res 246:595–606
Taugner R, Waldherr R, Seyberth HW, Erdös EG, Menard J, Schneider D (1988) The juxtaglomerular apparatus in Bartter's syndrome and related tubulopathies. An immunocytochemical and electron microscopic study. Virchows Arch A 412:459–470
Taylor AA (1977) Comparative physiology of the renin-angiotensin system. Fed Proc 36:1776–1780
Thoenes W (1961) Zur Feinstruktur der Macula densa im Nephron der Maus. Z Zellforsch Mikrosk Anat 55:486–499
Tisher CC, Bulger RE, Trump BF (1968) Human renal ultrastructure. III. The distal tubule in healthy individuals. Lab Invest 18:655–668
Wilson J (1984) The renin-angiotensin system in nonmammalian vertebrates. Endocr Rev 5:45–61
Wilson W (1952) A new staining method for demonstrating the granules of the juxtaglomerular complex. Anat Rec 112:497–507
Wismar BL (1962) The embryonic development of the juxtaglomerular complex. Dissertation Abstracts (Ann Arbor, Mich) 22:3808–3809
Wismar BL (1963) Functionally correlated changes in the position of the Golgi apparatus in the cells of the macula densa of the maturing nephron. Anat Rec 145:301
Zavagli G, Aleotti A, Farinelli A (1983) Human renin granules: ultrastructural aspects. Nephron 33:29–33
Zimmermann KW (1933) Über den Bau des Glomerulus der Säugerniere. Weitere Mitteilungen. Z Mikrosk Anat Forsch 32:176–278
Author information
Authors and Affiliations
Additional information
Fellow of the Alexander von Humboldt Foundation
Rights and permissions
About this article
Cite this article
Lacy, E.R., Reale, E. The presence of a juxtaglomerular apparatus in elasmobranch fish. Anat Embryol 182, 249–262 (1990). https://doi.org/10.1007/BF00185518
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00185518