Paracellular epithelial sodium transport maximizes energy efficiency in the kidney

Journal of Clinical Investigation

Volumn 126, Issue 7, 2016, Pages 2509-2518

  Pei, Lei ^a   Solis, Glenn ^b   Nguyen, Mien T X ^c   Kamat, Nikhil ^c   Magenheimer, Lynn ^a   Zhuo, Min ^a   Li, Jiahua ^a   Curry, Joshua ^a   McDonough, Alicia A ^c   Fields, Timothy A ^a   Welch, William J ^b   Yu, Alan S L ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 2; OXYGEN; SODIUM; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; MAGNESIUM; MALONALDEHYDE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; HENLE LOOP; HYPOXIA; INJURY SEVERITY; KIDNEY ISCHEMIA; KIDNEY MEDULLA; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE DAMAGE; KIDNEY TUBULE EPITHELIUM; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; OXYGEN TENSION; PARACELLULAR TRANSPORT; PASSIVE TRANSPORT; PRIORITY JOURNAL; PROTEIN FUNCTION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; SODIUM ABSORPTION; SODIUM CELL LEVEL; SODIUM RESTRICTION; SODIUM TRANSPORT; TRANSCYTOSIS; UPREGULATION; ANIMAL; C57BL MOUSE; DIET; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; ION TRANSPORT; KIDNEY; KNOCKOUT MOUSE; MALE; METABOLISM; PERMEABILITY; TIGHT JUNCTION; URINE;

ANIMALS; CLAUDIN-2; DIET; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION; ION TRANSPORT; KIDNEY; KIDNEY TUBULES, PROXIMAL; LOOP OF HENLE; MAGNESIUM; MALE; MALONDIALDEHYDE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXYGEN; OXYGEN CONSUMPTION; PERMEABILITY; REPERFUSION INJURY; SODIUM; TIGHT JUNCTIONS;

EID: 84978427938     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI83942     Document Type: Article

References (63)

1. Farquhar MG, Palade GE. Junctional complexes in various epithelia. J Cell Biol. 1963; 17:375-412.
2. Staehelin LA Further observations on the fine structure of freeze-cleaved tight junctions. J Cell Sci. 1973; 13 (3):763-786.
3. Whittembury G, Rawlins FA. Evidence of a paracellular pathway for ion flow in the kidney proximal tubule. Electromicroscopic demonstration of lanthanum precipitate in the tight junction. Pflugers Arch. 1971; 330 (4):302-309.
4. Machen TE, Erlij D, Wooding FB. Permeable junctional complexes. The movement of lanthanum across rabbit gallbladder and intestine. J Cell Biol. 1972; 54 (2):302-312.
5. Martínez-Palomo A, Erlij D. The distribution of lanthanum in tight junctions of the kidney tubule. Pflugers Arch. 1973; 343 (3):267-272.
6. Frömter E, Diamond J. Route of passive ion permeation in epithelia. Nature New Biol. 1972; 235 (53):9-13.
7. Tisher CC, Yarger WE. Lanthanum permeability of the tight junction (zonula occludens) in the renal tubule of the rat. Kidney Int. 1973; 3 (4):238-250.
8. Fagerberg L, Jonasson K, von Heijne G, Uhlén M, Berglund L. Prediction of the human membrane proteome. Proteomics. 2010; 10 (6):1141-1149.
9. Uhlen M, et al. Towards a knowledge based Human Protein Atlas. Nat Biotechnol. 2010; 28 (12):1248-1250.
10. McDonough AA, Thomson SC. Metabolic basis of solute transport. In: Taal MW, Chertow GM, Marsden PA, Skorecki K, Yu AS, Brenner BM, eds. Brenner and Rector's The Kidney. 9th ed. Philadelphia, Pennsylvania, USA: Elsevier; 2012:138-157.
11. Lübbers DW, Baumgärtl H. Heterogeneities and profiles of oxygen pressure in brain and kidney as examples of the pO2 distribution in the living tissue. Kidney Int. 1997; 51 (2):372-380.
12. Brodwall EK, Laake H. The relation between oxygen consumption and transport of sodium in the human kidney. Scand J Clin Lab Invest. 1964; 16:281-286.
13. Soltoff SP ATP and the regulation of renal cell function. Annu Rev Physiol. 1986; 48:9-31.
14. Kiil F, Aukland K, Refsum HE. Renal sodium transport and oxygen consumption. Am J Physiol. 1961; 201:511-516.
15. Thurau K. Renal Na-reabsorption and O2-uptake in dogs during hypoxia and hydrochlorothiazide infusion. Proc Soc Exp Biol Med. 1961; 106:714-717.
16. Knox FG, Fleming JS, Rennie DW. Effects of osmotic diuresis on sodium reabsorption and oxygen consumption of kidney. Am J Physiol. 1966; 210 (4):751-759.
17. Torelli G, Milla E, Faelli A, Costantini S. Energy requirement for sodium reabsorption in the in vivo rabbit kidney. Am J Physiol. 1966; 211 (3):576-580.
18. Neumann KH, Rector FC. Mechanism of NaCl and water reabsorption in the proximal convoluted tubule of rat kidney. J Clin Invest. 1976; 58 (5):1110-1118.
19. Berry CA, Warnock DG, Rector FC Jr Ion selectivity and proximal salt reabsorption. Am J Physiol. 1978; 235 (3):F234-F245.
20. Schafer JA, Patlak CS, Andreoli TE. A component of fluid absorption linked to passive ion flows in the superficial pars recta. J Gen Physiol. 1975; 66 (4):445-471.
21. Warnock DG, Burg MB. Urinary acidification: CO2 transport by the rabbit proximal straight tubule. Am J Physiol. 1977; 232 (1):F20-F25.
22. Barratt LJ, Rector FC Jr, Kokko JP, Seldin DW. Factors governing the transepithelial potential difference across the proximal tubule of the rat kidney. J Clin Invest. 1974; 53 (2):454-464.
23. Moe OW, Berry CA, Rector FC Jr Renal transport of glucose, amino acids, sodium, chloride and water. In: Brenner BM, ed. Brenner and Rector's The Kidney. 6th ed. Philadelphia, Pennsylvania, USA: Saunders; 2000:375-416.
24. Angelow S, Ahlstrom R, Yu AS. Biology of claudins. Am J Physiol Renal Physiol. 2008; 295 (4):F867-F876.
25. Günzel D, Yu AS. Claudins and the modulation of tight junction permeability. Physiol Rev. 2013; 93 (2):525-569.
26. Hou J, Rajagopal M, Yu AS. Claudins and the kidney. Annu Rev Physiol. 2013; 75:479-501.
27. Mineta K, et al. Predicted expansion of the claudin multigene family. FEBS Lett. 2011; 585 (4):606-612.
28. Suzuki H, et al. Crystal structure of a claudin provides insight into the architecture of tight junctions. Science. 2014; 344 (6181):304-307.
29. Enck AH, Berger UV, Yu AS. Claudin-2 is selectively expressed in proximal nephron in mouse kidney. Am J Physiol Renal Physiol. 2001; 281 (5):F966-F974.
30. Kiuchi-Saishin Y, Gotoh S, Furuse M, Takasuga A, Tano Y, Tsukita S. Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J Am Soc Nephrol. 2002; 13 (4):875-886.
31. Furuse M, Furuse K, Sasaki H, Tsukita S. Conversion of zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin-Darby canine kidney I cells. J Cell Biol. 2001; 153 (2):263-272.
32. Amasheh S, et al. Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J Cell Sci. 2002; 115 (pt 24):4969-4976.
33. Yu AS, et al. Molecular basis for cation selectivity in claudin-2-based paracellular pores: identification of an electrostatic interaction site. J Gen Physiol. 2009; 133 (1):111-127.
34. Muto S, et al. Claudin-2-deficient mice are defective in the leaky and cation-selective paracellular permeability properties of renal proximal tubules. Proc Natl Acad Sci USA. 2010; 107 (17):8011-8016.
35. Schnermann J, Huang Y, Mizel D. Fluid reabsorption in proximal convoluted tubules of mice with gene deletions of claudin-2 and/or aquaporin1. Am J Physiol Renal Physiol. 2013; 305 (9):F1352-F1364.
36. Waanders F, van Timmeren MM, Stegeman CA, Bakker SJ, van Goor H. Kidney injury molecule-1 in renal disease. J Pathol. 2010; 220 (1):7-16.
37. van Timmeren MM, van den Heuvel MC, Bailly V, Bakker SJ, van Goor H, Stegeman CA. Tubular kidney injury molecule-1 (KIM-1) in human renal disease. J Pathol. 2007; 212 (2):209-217.
38. Landwehr DM, Klose RM, Giebisch G. Renal tubular sodium and water reabsorption in the isotonic sodium chloride-loaded rat. Am J Physiol. 1967; 212 (6):1327-1333.
39. Morgan T, Berliner RW. A study by continuous microperfusion of water and electrolyte movements in the loop of Henle and distal tubule of the rat. Nephron. 1969; 6 (3):388-405.
40. Abe M, O'Connor P, Kaldunski M, Liang M, Roman RJ, Cowley AW. Effect of sodium delivery on superoxide and nitric oxide in the medullary thick ascending limb. Am J Physiol Renal Physiol. 2006; 291 (2):F350-F357.
41. Hong NJ, Garvin JL. NADPH oxidase 4 mediates flow-induced superoxide production in thick ascending limbs. Am J Physiol Renal Physiol. 2012; 303 (8):F1151-F1156.
42. Juncos R, Garvin JL. Superoxide enhances Na-K-2Cl cotransporter activity in the thick ascending limb. Am J Physiol Renal Physiol. 2005; 288 (5):F982-F987.
43. Ortiz PA, Garvin JL. Superoxide stimulates NaCl absorption by the thick ascending limb. Am J Physiol Renal Physiol. 2002; 283 (5):F957-F962.
44. Cabral PD, Garvin JL. Luminal flow regulates NO and O2 (-) along the nephron. Am J Physiol Renal Physiol. 2011; 300 (5):F1047-F1053.
45. Burg MB Thick ascending limb of Henle's loop. Kidney Int. 1982; 22 (5):454-464.
46. Stephenson JL, Tewarson RP, Mejia R. Quantitative analysis of mass and energy balance in nonideal models of the renal counterflow system. Proc Natl Acad Sci U S A. 1974; 71 (5):1618-1622.
47. Windhager EE, Giebisch G. Micropuncture study of renal tubular transfer of sodium chloride in the rat. Am J Physiol. 1961; 200:581-590.
48. Ullrich KJ, et al. Micropuncture study of composition of proximal and distal tubular fluid in rat kidney. Am J Physiol. 1963; 204:527-531.
49. Burg M, Good D. Sodium chloride coupled transport in mammalian nephrons. Annu Rev Physiol. 1983; 45:533-547.
50. Brenner BM, Troy JL, Daugharty TM. On the mechanism of inhibition in fluid reabsorption by the renal proximal tubule of the volume-expanded rat. J Clin Invest. 1971; 50 (8):1596-1602.
51. Ichikawa I, Brenner BM. Mechanism of inhibition of proximal tubule fluid reabsorption after exposure of the rat kidney to the physical effects of expansion of extracellular fluid volume. J Clin Invest. 1979; 64 (5):1466-1474.
52. + deficiency and glucose malabsorption in mouse small intestine. Gastroenterology. 2011; 140 (3):913-923.
53. Lee JW, Chou CL, Knepper MA. Deep sequencing in microdissected renal tubules identifies nephron segment-specific transcriptomes. J Am Soc Nephrol. 2015; 26 (11):2669-2677.
54. Madala Halagappa VK, Tiwari S, Riazi S, Hu X, Ecelbarger CM. Chronic candesartan alters expression and activity of NKCC2, NCC, and ENaC in the obese Zucker rat. Am J Physiol Renal Physiol. 2008; 294 (5):F1222-F1231.
55. Tiwari S, Li L, Riazi S, Halagappa VK, Ecel barger CM Sex and age result in differential regulation of the renal thiazide-sensitive NaCl cotransporter and the epithelial sodium channel in angiotensin II-infused mice. Am J Nephrol. 2009; 30 (6):554-562.
56. Zhou H, et al. Urinary marker for oxidative stress in kidneys in cisplatin-induced acute renal failure in rats. Nephrol Dial Transplant. 2006; 21 (3):616-623.
57. +, and H2O transporters' abundance along the nephron. Am J Physiol Renal Physiol. 2012; 303 (1):F92-104.
58. Welch WJ, Baumgärtl H, Lübbers D, Wilcox CS. Renal oxygenation defects in the spontaneously hypertensive rat: role of AT1 receptors. Kidney Int. 2003; 63 (1):202-208.
59. Welch WJ, Mendonca M, Aslam S, Wilcox CS. Roles of oxidative stress and AT1 receptors in renal hemodynamics and oxygenation in the postclipped 2K, 1C kidney. Hypertension. 2003; 41 (3 Pt 2):692-696.
60. Welch WJ, Blau J, Xie H, Chabrashvili T, Wilcox CS. Angiotensin-induced defects in renal oxygenation: role of oxidative stress. Am J Physiol Heart Circ Physiol. 2005; 288 (1):H22-H28.
61. Lai EY, et al. Effects of the antioxidant drug tempol on renal oxygenation in mice with reduced renal mass. Am J Physiol Renal Physiol. 2012; 303 (1):F64-F74.
62. Zhang S, et al. Dietary phosphate restriction suppresses phosphaturia but does not prevent FGF23 elevation in a mouse model of chronic kidney disease. Kidney Int. 2013; 84 (4):713-721.
63. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012; 9 (7):671-675.