Abstract
In hypertension the pressure natriuresis set point is shifted to a higher pressure due to an increase in both renal vascular resistance and sodium (Na) reabsorption. The afferent arterioles (Af-Arts) and efferent arterioles (Ef-Arts) account for most renal vascular resistance; they control glomerular filtration rate (GFR) and peritubular pressure, and, consequently, renal function. Af-Art and Ef-Art resistance is regulated by factors similar to those in other arterioles and also by tubuloglomerular feedback (TGF). TGF operates via the macula densa, which senses increases in sodium chloride (NaCl) and sends a signal that constricts the Af-Art and dilates the Ef-Art. In the outer renal cortex, the connecting tubule (CNT) returns to the glomerular hilus and contacts the Af-Art. This morphology is compatible with cross-talk between the CNT and Af-Art, so-called connecting tubule glomerular feedback (CTGF). Our studies show that increasing NaCl delivery to the CNT results in Af-Art dilatation that can be blocked by inhibitors of Na transport. We believe cross-talk between the CNT and Af-Art is a novel mechanism that may contribute to regulation of renal blood flow and GFR.
Similar content being viewed by others
References
Goormaghtigh N (1937) L’appareil neuro-myo-arteriel juxta-glomerulaire du rein:ses reactions en pathologie et ses rapports avec le tube urinifere. C R Seances Soc Biol Fil 124:293–296
Barajas L (1979) Anatomy of the juxtaglomerular apparatus. Am J Physiol 237:333–343
Schnermann J, Briggs JP (1992) Function of the juxtaglomerular apparatus. Control of glomerular hemodynamics and renin secretion. In: Seldin DW, Giebisch G (eds) The kidney: physiology and pathology. 2nd edn. Raven Press, New York, pp 1249–1289
Thurau K, Schnermann J (1965) Die Natriumkonzentration an den Macula densa Zellen als regulierender Faktor fur das Glomerulumfiltrat (Mikropunktionsversuche). Klin Wochenschr 43:410–413
Briggs JP, Schnermann J (1987) The tubuloglomerular feedback mechanism: functional and biochemical aspects. Annu Rev Physiol 49:251–273
Schnermann J, Persson AE, Agerup B (1973) Tubuloglomerular feedback. Nonlinear relation between glomerular hydrostatic pressure and loop of Henle perfusion rate. J Clin Invest 52:862–869
Mason J, Moore LC (1982) A new way of investigating tubuloglomerular feedback: the closed loop mode. Kidney Int 22:S151–S156
Holstein-Rathlou N-H (1991) A closed-loop analysis of the tubuloglomerular feedback mechanism. Am J Physiol 261:F880–F889
Thomson SC, Blantz RC (1993) Homeostatic efficiency of tubuloglomerular feedback in hydropenia, euvolemia, and acute volume expansion. Am J Physiol 264:F930–F936
Ren Y, Arima S, Carretero OA, Ito S (2002) Possible role of adenosine in macula densa control of glomerular hemodynamics. Kidney Int 61:169–176
Schnermann J, Briggs JP (1989) Single nephron comparison of the effect of loop of Henle flow on filtration rate and pressure in control and angiotensin II-infused rats. Miner Electrolyte Metab 15:103–107
Davis JM (1991) Role of the efferent arteriole in tubuloglomerular feedback. Kidney Int 39 [Suppl 32]:S71–S73
Briggs JP, Wright FS (1979) Feedback control of glomerular filtration rate: site of the effector mechanism. Am J Physiol 236:F40–F47
Persson AE, Gushwa LC, Blantz RC (1984) Feedback pressure-flow responses in normal and angiotensin- prostaglandin blocked rats. Am J Physiol 247:F925–F931
Ren Y, Garvin JL, Carretero OA (2000) Efferent arteriole tubuloglomerular feedback in the renal nephron. Kidney Int 59:222–229
Blantz RC, Vallon V (2007) Tubuloglomerular feedback responses of the downstream efferent resistance: unmasking a role for adenosine? Kidney Int 71:837–839
Thomson S, Bao D, Deng A, Vallon V (2000) Adenosine formed by 5′-nucleotidase mediates tubuloglomerular feedback. J Clin Invest 106:289–298
Thomson SC, Blantz RC (2000) Ions and signal transduction in the macula densa. J Clin Invest 106:633–635
Schnermann J (2002) Adenosine mediates tubuloglomerular feedback. Am J Physiol Regul Integr Comp Physiol 283:R276–R277
Sun D, Samuelson LC, Yang T, Huang Y, Paliege A, Saunders T, Briggs J, Schnermann J (2001) Mediation of tubuloglomerular feedback by adenosine: evidence from mice lacking adenosine 1 receptors. Proc Natl Acad Sci USA 98:9983–9988
Bell PD, Lapointe J-Y, Sabirov R, Hayashi S, Peti-Peterdi J, Manabe K, Kovacs G, Okada Y (2003) Macula densa cell signaling involves ATP release through a maxi anion channel. Proc Natl Acad Sci USA 100:4322–4327
Jackson EK, Dubey RK (2001) Role of the extracellular cAMP-adenosine pathway in renal physiology. Am J Physiol Renal Physiol 281:F597–F612
Castrop H, Huang Y, Hashimoto S, Mizel D, Hansen P, Theilig F, Bachmann S, Deng C, Briggs J, Schnermann J (2004) Impairment of tubuloglomerular feedback regulation of GFR in ecto-5′-nucleotidase/CD73-deficient mice. J Clin Invest 114:634–642
Ren Y, Garvin JL, Liu R, Carretero OA (2004) Role of macula densa adenosine triphosphate (ATP) in tubuloglomerular feedback. Kidney Int 66:1479–1485
Huang DY, Vallon V, Zimmermann H, Koszalka P, Schrader J, Osswald H (2006) Ecto-5′-nucleotidase (cd73)-dependent and -independent generation of adenosine participates in the mediation of tubuloglomerular feedback in vivo. Am J Physiol Renal Physiol 291:F282–F288
Dietrich MS, Steinhausen M (1993) Differential reactivity of cortical and juxtamedullary glomeruli to adenosine-1 and adenosine-2 receptor stimulation and angiotensin-converting enzyme inhibition. Microvasc Res 45:122–133
Ren Y, Arima S, Carretero OA, Ito S (1993) Direct comparison of adenosine (Ado) action in isolated microperfused rabbit glomerular afferent (Af-) and efferent arterioles (Ef-Arts) (abstract). J Am Soc Nephrol 4:566
Holz FG, Steinhausen M (1987) Renovascular effects of adenosine receptor agonists. Ren Physiol 10:272–282
Ren Y, Arima S, Carretero OA, Ito S (1994) Vasodilator and constrictor action of adenosine (Ado) in isolated microperfused rabbit afferent (Af-) and efferent arterioles (Ef-Arts) (abstract). J Hypertens 12 [Suppl 3]:S160
Kishore BK, Isaac J, Tripp SR, Shi H, Hemmert A, Bollen M (2004) Cellular localization of nucleotide pyrophosphatases/phosphodiesterases (NPPs) in rat kidney. FASEB J 18:A733
Walker JP, Darvish A, Yeasting RA, Metting P (1995) Localization of AMP-specific cytosolic 5′-nucleotidase in the kidney: regional sites of intracellular adenosine production (abstract). FASEB J 9:A843
Resta R, Hooker SW, Hansen KR, Laurent AB, Park JL, Blackburn MR, Knudsen TB, Thompson LF (1993) Murine ecto-5′-nucleotidase (CD73): cDNA cloning and tissue distribution. Gene 133:171–177
Vallon V (2003) Tubuloglomerular feedback and the control of glomerular filtration rate. News Physiol Sci 18:169–174
Ren Y, Garvin JL, Liu R, Carretero OA (2007) Possible mechanism of efferent arteriole (Ef-Art) tubuloglomerular feedback. Kidney Int 71:861–866
Madsen KM, Tisher CC (1986) Structural-functional relationships along the distal nephron. Am J Physiol 250:F1–F15
Faarup P (1965) On the morphology of the juxtaglomerular apparatus. Acta Anat 60:20–38
Barajas L, Powers K, Carretero OA, Scicli AG, Inagami T (1986) Immunocytochemical localization of renin and kallikrein in the rat renal cortex. Kidney Int 29:965–970
Vio CP, Figueroa CD, Caorsi I (1988) Anatomical relationship between kallikrein-containing tubules and the juxtaglomerular apparatus in the human kidney. Am J Hypertens 1:269–271
Dørup J, Morsing P, Rasch R (1992) Tubule-tubule and tubule-arteriole contacts in rat kidney distal nephrons. A morphologic study based on computer-assisted three-dimensional reconstructions. Lab Invest 67:761–769
Morsing P, Velazquez H, Ellison D, Wright FS (1993) Resetting of tubuloglomerular feedback by interrupting early distal flow. Acta Physiol Scand 148:63–68
Ren Y, Garvin JL, Liu R, Carretero OA (2007) Crosstalk between the connecting tubule and the afferent arteriole regulates renal microcirculation. Kidney Int 71:1116–1121
Schnermann J, Ploth DW, Hermle M (1976) Activation of tubulo-glomerular feedback by chloride transport. Pflugers Arch 362:229–240
Acknowledgments
This work was supported by grants from the American Heart Association (AHA D20607) and the National Institutes of Health (HL28982).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ren, Y., Garvin, J.L., Liu, R. et al. Cross-talk between arterioles and tubules in the kidney. Pediatr Nephrol 24, 31–35 (2009). https://doi.org/10.1007/s00467-008-0852-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00467-008-0852-8