A Standard Nomenclature for Structures of the Kidney

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Kidney International, Vol. 33 (1988), pp. 1—7

EDITORIAL REVIEW

A standard nomenclature for structures of the kidney

THE RENAL COMMISSION OF THE INTERNATIONAL UNION OF PHYSIOLOGICAL SCIENCES (IUPS)

Prepared by WILHELM KRIz, Co-Chair, Heidelberg, Federal Republic of Germany LISE BANKIR, Co-Chair, Paris, France In consultation with RUTH ELLEN BULGER, Houston, USA MAURICE B. BURG, Bethesda, USA OLGA A. GONCHAREVSKAYA, Leningrad, USSR MASASHI IMAI, Osaka, Japan BRIGITTE KAISSLING, Basel, Switzerland ARVID B. MAUNSBACH, Aarhus, Denmark DAVID B. MOFFAT, Cardiff, UK FRANc0IS MOREL, Paris, France TREFOR 0. MORGAN, Melbourne, Australia YuRI V. NATOCHIN, Leningrad, USSR C. Cijo TISI-IER, Gainesville, USA MANJERI A. VENKATACHALAM, San Antonio, USA GUILLERMO WHITTEMBURY, Caracas, Venezuela FRED S. WRIGHT, New Haven, USA

Editors Note: This paper, "Standard nomenclature for struc-nephron to three types of nephrons, of four main tubular parts tures of the kidney," was prepared at the request of the Renal (proximal tubule, intermediate tubule, distal tubule, collecting Commission of the International Union of Physiological Sci-duct) to several subdivisions of those parts, and of homogeneity ences (IUPS). The information is being published, by a jointof cells within a given part to identification of several types of editorial decision, simultaneously in the January, 1988 issues ofcells within a part or subdivision. With our heightened ability to THE AMERICAN JOURNAL OF PHYSIOLOGY: RENAL, dissect the many components of the kidney, both anatomically FLUID AND ELECTROLYTE PHYSIOLOGY, KIDNEY IN- and functionally, there is an increasing need to convey to our TERNATIONAL, and PFLUGERS ARCHly. colleagues precisely which structure we were working with. The Editors have chosen, deliberately, to duplicate publica-The following standard nomenclature is disseminated to help tion of this document in the above three journals, to insure themeet that need. widest possible dissemination of this terminology, which has The project was undertaken at the request of the Renal been adopted simultaneously by each of the three journals. Commission of the International Union of Physiological Sci- ences (IUPS). It is the hope of the Commission that the JAMES A. SCHAFER, Ph.D., Editor, American Journal ofnomenclature proposed herein may be widely adopted. We Physiology: Renal, Fluid and Electrolyte Physiology recommend that when disagreement arises—as is bound to THOMAS E. ANDREOLI, M.D., Editor, Kidney Internationalhappen—the author(s) may indicate that the name which he or KLAUS THURAU, M.D., Coordinating Editor, Pflügers Archiv—she applies to a given structure is synonymous with one of the European Journal of Physiology elements designated in Table 1 or Figures 1 and 2 of the present Preamble report. Discoveries which alter the schema should be called to the attention of one of the co-chairs, W. Kriz, or L. Bankir. The kidney is an organ of complex structure and function, a References have been deliberately omitted because it would fact that is increasingly revealed as our investigations proceed.have been cumbersome to include the many sources that served We have witnessed a progression from recognition of a single as a basis for the recommendations. Those needing particulars on the sources should contact one of the co-chairs.

Kidney structure Explanation Kidney structure Explanation Main Divisions Giant bundles Fusion of several bundles. Cortex (C) Simple type The simple type contains Cortical labyrinth Complex type only descending and ascend- Cortex corticis ing vasa recta; the complex Medullary rays type includes the descending thin limbs of short loops of Medulla Henle. Outer medulla (OM) Interbundle capillary Only for the inner stripe cap- Outer stripe (OS) plexus illary plexus. Inner stripe (IS) Renal lymphatics Vascular bundles Renal nerves Interbundle region Inner medulla (IM) Renal interstitium Lipid laden interstitial Papilla The papilla is that part of the Crest inner medulla which projects cells into the pelvis. In many kidneys a crest is developed in- Nephrons stead of a papilla. Nephron—Types Renal pelvis Superficial nephrons Those originating from a su- Pelvic cavity Midcortical nephrons Pelvic extension Extensions of the pelvic cavi- perficial, midcortical, or jux- Juxtamedullary nephronstamedullary glomerulus (see ty along the blood vessels. later). A less strict definition Secondary pouches Extensions of the pelvic cavi- for a superficial nephron says ty around the edges of the that it touches the renal sur- pelvic septa. face. Renal sinus Short-looped nephrons Henle's loop turning back in Renal hilum the outer medulla (or cortex). For multilobar, multipapil- Cortical nephrons Henle's loop turning back in laty kidneys the follow- the cortex. ing additional terms are Long-looped nephrons Henle's loop turning back in necessary: the inner medulla. Renal column (Column of Bertin) N.B.: The two divisions in Major calices, minor nephron types do not always calices coincide: for example, juxta- Renal artery, anterior medullary nephron is not and posterior divisions necessarily synonymous with Segmental artery long-looped nephron. Super- ficial as well as juxtamedul- Vessels, nerves, and lary nephrons may have long interstitium or short loops. Renal vasculature Renal artery (vein) Interlobar artery (vein) Nephron—Main divisions Arcuate artery (vein) Renalcorpuscle Cortical radial artery This term is much more ap- Bowman's capsule (vein) propriate in describing the Glomerulus The term "glomerulus" (plu- course of these vessels; it re- Glomerular lobule ral: glomeruli) is widely used places the term interlobular to designate the entire renal artery. corpuscle. In the present sys- Perforating radial artery tem the glomerulus is more Stellate vein precisely termed "glomerular Afferent arteriole tuft." Efferent arteriole Urinary space Often called Bowman's Welling point space. Glomerular capillaries Tubular portions of the Peritubular capillaries nephron Descending vasa recta Proximal tubule Ascending vasa recta Intermediate tubule The term "Intermediate tu- Vascular bundles Distal tubule bule" has formerly been Primary bundles used. It is regarded as a Secondary bundles Fusion of two primary bun- very appropriate term and is dles. therefore reintroduced to designate the entire thin Abbreviations are in parenthesis. limb. Standard nomenclature 3

Kidney structure Explanation Kidney structure Explanation Proximal convolution N.B. This micro-anatomical c. Proximal tubule Loop of Henle subdivision of the nephron • Neck segment Only present in some spe- Long loop, short tubule is independent from cies; it may be considered as loop, cortical loopthe above one. The distal a tubular elongation of Bow- Distal convolution convolution does not com- man's capsule. prise the same segments as • Convoluted part Situated in the cortical laby- the distal tubule (Table 1). (pars convoluta) or rinth. The term "loop of Henle" Proximal convoluted comprises the straight part of tubule (PCT) the proximal tubule (thick de- • Straight part (pars Situated in the medullary ray scending limb), the interme- recta) or Proximal of cortex and in the outer diate tubule (thin descending straight tubule (PST) stripe of the outer medulla. and ascending limbs) and the Note that the straight parts straight part of the distal tu- of the juxtamedullary neph- bule (thick ascending limb). rons are not straight, but de- Nephron—Details scend tortuously through the a. Renal corpuscle outer stripe. They are de- Types fined as "straight parts" by their location in the outer Superficial renal cor- Those giving rise to an effer- stripe. puscles (superficial ent arteriole which touches glomeruli) the renal surface. A less Subdivisions: (de- strict definition comprises all fined ultra- glomeruli establishing the structurally) most superficial layer of gb- Sl (segment) (or P1)Comprises the beginning and meruli. SI cells middle portions of the convo- Midcortical renal cor- The term comprises all gb- luted part. Transition to S2 is puscles (midcortical meruli which are neither su- gradual. glomeruli) perficial nor juxtamedullary. S2 (segment) (or P2)Comprises the end portions Juxtamedullary renal Those giving rise to an effer- S2 cells of the convoluted part and corpuscles (juxtame-ent arteriole which turns to- the beginning portions of the dullary glomeruli) wards the medulla and splits straight part. Transition to S3 into descending vasa recta. is abrupt in some species Components (rat, dog), gradual in others (rabbit). Parietal cells of Bow- S3 (segment) (or P3)Comprises the remaining por- man's capsule S3 cells tions of the straight part. Peripolar cells These cells are modified cells Generally, all proximal tu- of Bowman's capsule which bules lying in the outer stripe contain granules. are S3 segments. Podocytes Synonymous with visceral cells of Bowman's capsule or Instead of Sl, S2, and S3 the gbomerular epithelial cells. abbreviations P1, P2, and P3 Filtration slit are widely used. The "S" re- Slit diaphragm fers to "segment" and "P" Endothelial cells to "proximal." Mesangium Mesangial cells d. Intermediate tubule Mesangial matrix Descending thin limb Glomerular basement of Henle's loop (pars membrane (GBM) descendens) (DTL) Lamina rara interna Descending thin Lamina densa limb of a short Lamina rara externa loop b. Juxtaglomerular DTL type 1 cells apparatus (JGA) Descending thin Granular cells Synonymous with epithelioid limb of a long cells. They are modified vas- loop cular smooth muscle cells. Upper part Defined by the appearance of Extraglomerular DTL type 2 the epithelium. The limit be- mesagium cells tween upper and lower part Extraglomerular Synonymous with Goor- Lower part occurs at different levels and mesangial cells maghtigh cells, lacis cells. DTL type 3 does not correspond to the Macula densa cells border between inner stripe Macula densa cells and inner medulla. 4 Standard nomenclature

Kidney structure Explanation Kidney structure Explanation Pre-bend segment Short portion before the ioop Connecting tubule duct and is functionally dif- (already ATL bend, already outlined by the cells =CNTcells ferent from both. The embry- cells) same type of epithelium that Intercalated cells = onic origin of this segment is lines the ascending limb. ICcells not considered here. It is Ascending thin limb ofInstead of the abbreviation characterized by the pres- Henle's loop (pars as- ATL, TAL has also been ence of a typical cell type, cendens) (ATL) used. However, TAL is now the CNT cell. In many spe- ATL cells widely used to designate the cies, connecting tubule epi- (type 4 thick ascending limb. thelium is observed before cells) the first junction with anoth- e. Distal tubule er nephron. Straight part (pars recta), or Distal straight Transition to the collecting tubule, or Thick as- duct (arbitrarily defined by cending limb (DST or the first appearance of its TAL) typical cell, the CD cell or Distal straight tu- principal cell, see below) is bular cells, DST gradual in most species; that cells, or TAL is, the characteristic cells of cells both segments (CNT and CD Medullary straight The transition between MTAL cells) are intermingled over a part or medullary and CTAL is gradual; the most certain distance. In the rab- thick ascending noticeable changes, however, bit, this transition is abrupt. limb (MTAL) occur close to the border be- Arcade This structure is defined ana- Cortical straight part tween IS and OS (known from tomically, not by the cell or cortical thick as- rat and rabbit). types it comprises. Arcade is cending limb not synonymous with con- (CTAL) nected tubule. Macala densa (MD)The macula densa is a cell MD cells plaque within the end portion An arcade is an ascending tu- of the thick ascending limb. bule found in the cortical labyrinth and joining deep and Post-macular Part of the cortical thick as- midcortical nephrons to a segment cending limb between the cortical collecting duct. Ar- macula densa and the transi- cades are found in many spe- tion to the convoluted part. cies to different degrees. Ui- trastructurally, they generally Convoluted part (pars Transition to the subsequent comprise CNT and CD cells convoluta) or Distal connecting tubule (see below) (plus interspersed IC cells) in convoluted tubule may be abrupt (rabbit) or proportions varying along the (DCT) gradual (most other species) arcade (such as, rat). In the DCT cells in the sense that the charac- rabbit, they are lined by teristic cells for the two tubu- CNT cells only (plus inter- lar portions (DCT-cells and spersed IC cells). CNT-cells) are found inter- Cortical collecting Collecting tubule is often mingled with each other over duct (CCD) used instead of collecting a certain distance. In those duct. Collecting duct seems cases, the connecting tubule more appropriate since this may be considered to start part of the uriniferous system with the first occurrence of emerges from the confluence CNT-cells, even if DCT-cells of many nephrons. are still present. Defined ultrastructurally by f. Collectingsystem The different segments of the the beginning of the occur- collecting system in the cor- rence of CD cells. Located tex are defined here accord- mostly in the medullary rays ing to the cell types they of the cortex. The distinction comprise (which gives each between cortical collecting segment its functional prop- duct and outer medullary col- erties) and not by their posi- lecting duct is arbitrarily tion with regard to the first based on their location within junction with another neph- the kidney. No abrupt limit is ron. recognizable ultrastructurally. Connecting tubule The "connecting tubule" (CNT) connects the distal convolut- The term "cortical collecting Two cell types: ed tubule to the collecting duct" comprises two por- Standard nomenclature 5

Kidney structure Explanation tions generally distinguished in microperfusion experi- ments: the segment from the end of the CNT to the first Cortex confluence with another CCD (ICT =initialcollecting tubule) and the unbranched 8 portion in the medullary ray (CCT =corticalcollecting tubule). Two cell types: In analogy with the denomi- collecting duct nation of cell types in the cells =CDcells; other segments, which also also called princi- may have heterogeneous cell pal cells =Pcells populations, it seems prefera- '¼ ble to use "collecting duct cell" or "CD cell" instead of "principal cell." Intercalated cells = ICcells Ct Outer medullary col- The distinction between the a) lecting duct (OMCD) outer and inner medullary Inner Inner medullary col- collecting ducts is arbitrarily Stripe lecting duct (IMCD) based on their location within the kidney. No abrupt transi- 0 tion is noticed ultrastructurally. IC cells may be found in the early IMCD in some species. Papillary ducts The fused ducts within the 12 tip of the papilla are some- Inner times called "papillary Medulla ducts" (Ducts of Bellini), but a clear definition and separa- tion from the inner medullary collecting ducts has never been done.

1 = Renal corpuscle including Bowman's capsule and the glomerulus (glomerular tuftl 2 = Proximal convoluted tubule Reprints of this article are not available. 3 = Proximal straight tubule 4 = Descending thin limb 5 Ascending thin limb 6 Distal straight tubule (thick ascending limbl Addresses of the Co-Chairs: 7 = Macula densa located within the final portion of the thick ascending limb Wilhelm Kriz 8 = Distal convoluted tubule 9 = Connecting tubule Anatomisehes Institut Connecting tubule of the juxtamedullary nephron that forms an arcade INF 307 10 Cortical collecting duct D-6900 Heidelberg, F.R.G. 11 = Outer medullary collecting duct 12 = Inner medullary collecting duct Lise Bankir Fig.1. Schema of nephron. This scheme depicts a short-looped and a INSERM Unite 90 long-looped nephron together with the collecting system. Not drawn to Hôpital Necker scale. Within the cortex a medullary ray is delineated by a dashed line. F-75743 Paris Cedex 15, France 6 Standardnomenclature

1/la = Interlobar artery and vein 2/2a = Arcuate artery and vein 3/3a = Cortical radial artery and vein 4 = Stellate vein 5 Afferent arteriole 6 = Efferent arteriole 7a/7b/7c = Superficial, midcortical, and juxtamedullary glomerulus 8/8a Juxtamedullary efferent arteriole, descending vasa recta 9/9a = Ascending vasa recta (those ascending within a vascular bundle and those independent from a bundlel

Fig.2. Schema of renal vessels. This scheme depictsthe course and distribution of the in- trarenal blood vessels; peritubular capillaries are not shown. Not drawn to scale, Within the cortex the medullary rays of the cortex (MR) are delineated from the cortical labyrinth (CL) by a dashed line. OS =outerstripe; IS =inner stripe; IM =innermedulla; P =renalpel- vis. Standard nomenclature 7

Table 1. Nomenclature

Micro- anatomical Abbrevi- terms Main divisions Subdivisions Segrpeniation ation Cell types Other frequently used denominations 0t Proximal tubule Pars convoluta Proximal S I segment S I cells I- or convoluted PCT P I segment PT convoluted part tubule S2 segment S 2 cells P 2 segment Pars recta Proximal or straight —\ PST P 3 segment PR straight part tubule S3 egment S 3 cells

Intermediate Pars decendens Descending DTL DTL cells lubule or thin of short loops Type I Short descending thin limb of Henle's loop (SDL) descending part limb of long loops upperpart Type2 Longdescending thin limb,upperpart (LDLS) tower part Type 3 Longdescending thin limb, lower part (L13L1)

pre-bend segment ATL cells 0 0. Pars ascendens Type 4 0 or Ascending thin limb ATL TAL Thin ascendinglimb (of longloops -t ascending part only)

Distal Pars recta Distal MAL Thick ascending limb of l-ienle'sloop Medultarystraightpart MTAL DST or TAL cells tubule or straight - mTALH Medultary thick limb straightpart tuble — CAL Cortical thick limb — cTALH (sect. Macula densa) or Cortical straight part 0CTAL Thick I ascending Maclila densa [MI) cells MD limb postmacular segment DCT a5 - - . - early distal Pars convoluta DCT cells tubule or Distal convoluted tubule DCT (-F IC cells) DCTb* Distal tubule convoluted part

Collecting system CNT cells DCTg5 late Connecting tubule CNT + distal Connecting segment IC cells CCTg5 tuble Cl) cells Initial collecting tubule principal cells DCTI5 Collecting Cortical collecting duct CCI) duct = lightcells 1- CCTI* Cortical collecting tubule (CC'F( IC cells intercalated cells = mitochondria-rich cells OMCD Outer medullary collecting duct = carboanhydrase-rich cells Outer medullary collecting tubule (OMCT) C55 = dark cells

0 0 CD cells Inner medullary collecting duct I MCD inner medullary collecting tubule (IMCT) principal cells Papillary collecting duct (PCI)) of ducts or Beltini

This table summarizes the nomenclature of segments and cells of the renal tubule. A continuous serpentine arrow () means that the transition between the two structures is gradual. An interrupted serpentine arrow (s)meansthat the transition is gradual in some species, abrupt in others. Abbreviations marked by a star were introduced by Morel and coworkers (Kidney mt 9, 264, 1976). They mean: DCTa, distal convoluted tubule, initial portion; DCTb, Distal convoluted tubule, bright portion; DCTg, distal convoluted tubule, granular portions; DCTI, distal convoluted tubule, light portion; CCTg, cortical collecting tubule, granular portion; CCTe, cortical collecting tubule, light portion.