Glycoconjugate Journal

, Volume 30, Issue 7, pp 667–676 | Cite as

Impact of salt exposure on N-acetylgalactosamine-4-sulfatase (arylsulfatase B) activity, glycosaminoglycans, kininogen, and bradykinin

  • Kumar Kotlo
  • Sumit Bhattacharyya
  • Bo Yang
  • Leonid Feferman
  • Shah Tejaskumar
  • Robert Linhardt
  • Robert Danziger
  • Joanne K. Tobacman
Article

Abstract

N-acetylgalactosamine-4-sulfatase (Arylsulfatase B; ARSB) is the enzyme that removes sulfate groups from the N-acetylgalactosamine-4-sulfate residue at the non-reducing end of chondroitin-4-sulfate (C4S) and dermatan sulfate (DS). Previous studies demonstrated reduction in cell-bound high molecular weight kininogen in normal rat kidney (NRK) epithelial cells when chondroitin-4-sulfate content was reduced following overexpression of ARSB activity, and chondroitinase ABC produced similar decline in cell-bound kininogen. Reduction in the cell-bound kininogen was associated with increase in secreted bradykinin. In this report, we extend the in vitro findings to in vivo models, and present findings in Dahl salt-sensitive (SS) rats exposed to high (SSH) and low salt (SSL) diets. In the renal tissue of the SSH rats, ARSB activity was significantly less than in the SSL rats, and chondroitin-4-sulfate and total sulfated glycosaminoglycan content were significantly greater. Disaccharide analysis confirmed marked increase in C4S disaccharides in the renal tissue of the SSH rats. In contrast, unsulfated, hyaluronan-derived disaccharides were increased in the rats on the low salt diet. In the SSH rats, with lower ARSB activity and higher C4S levels, cell-bound, high-molecular weight kininogen was greater and urinary bradykinin was lower. ARSB activity in renal tissue and NRK cells declined when exogenous chloride concentration was increased in vitro. The impact of high chloride exposure in vivo on ARSB, chondroitin-4-sulfation, and C4S-kininogen binding provides a mechanism that links dietary salt intake with bradykinin secretion and may be a factor in blood pressure regulation.

Keywords

Bradykinin Chondroitin Disaccharide Kininogen Sulfatase Sulfate 

Notes

Acknowledgments

The authors thank Robert Chanthimabha for his help with determinations of creatinine and electrolytes. Research was supported by VA Merit Awards to R.S. Danziger, M.D. and J.K. Tobacman, M.D. and NIDDK R21HL096031 to Dr. Danziger.

References

  1. 1.
    De Sousa, J.F., Nader, H.B., Dietrich, C.P.: Sequential degradation of chondroitin sulfate in mollusks. J. Biol. Chem. 265, 20150–20155 (1990)Google Scholar
  2. 2.
    Glaser, J.H., Conrad, H.E.: Chondroitin SO4 catabolism in chick embryo chondrocytes. J. Biol. Chem. 254, 2316–2325 (1978)Google Scholar
  3. 3.
    Ingmar, B., Wasteson, B.: Sequential degradation of a chondroitin sulfate trisaccharide by lysosomal enzymes from embryonic-chick epiphysial cartilage. Biochem. J. 179, 7–13 (1979)PubMedGoogle Scholar
  4. 4.
    Bhattacharyya, S., Kotlo, K., Danziger, R.S., Tobacman, J.K.: Arylsulfatase B regulates interaction of chondroitin-4-sulfate and kininogen in renal epithelial cells. Biochim. Biophys. Acta 1802(5), 472–477 (2010)PubMedCrossRefGoogle Scholar
  5. 5.
    Gozzo, A.J., Nunes, V.A., Carmona, A.K., Nader, H.B., von Dietrich, C.P., Silveira, V.L.F., Shimamoto, K., Ura, N., Sampaio, M.U., Sampaio, C.A.M., Araujo, M.S.: Glycosaminoglycans affect the action of human plasma kallikrein on kininogen hydrolysis and inflammation. Int. Immunopharmacol. 2, 1861–1865 (2002)Google Scholar
  6. 6.
    Renné, T., Schuh, K., Müller-Esterl, W.: Local bradykinin formation is controlled by glycosaminoglycans. J. Immunol. 175, 3377–3385 (2005)PubMedGoogle Scholar
  7. 7.
    Bhattacharyya, S., Tobacman, J.K.: Steroid sulfatase, arylsulfatases A and B, galactose 6-sulfatase, and iduronate sulfatase in mammary cells and effects of sulfated and non-sulfated estrogens on sulfatase activity. J. Steroid Biochem. Mol. Biol. 103, 20–34 (2007)PubMedCrossRefGoogle Scholar
  8. 8.
    Ferrero, G.B., Pagliardini, S., Veljkovic, A., Porta, F., Bena, C., Tardivo, I., Restagno, G., Silengo, M.C., Bignamini, D.: In vivo specific reduction of arylsulfatase B enzymatic activity in children with Cystic Fibrosis. Mol. Genet. Metab. 94, 39 (2008)CrossRefGoogle Scholar
  9. 9.
    Sharma G, Burke J, Bhattacharyya S, Sharma N, Katyal S, Park RL, Tobacman J: Reduced arylsulfatase B activity in leukocytes from cystic fibrosis patients. Pediatr. Pulmonol. (2012). doi: 10.1002/ppul.22567
  10. 10.
    Prabhu, S.V., Bhattacharyya, S., Guzman-Hartman, G., Macias, V., Kajdacsy-Balla, A., Tobacman, J.K.: Extra-lysosomal localization of arylsulfatase B in human colonic epithelium. J. Histochem. Cytochem. 59(3), 328–335 (2011)PubMedCrossRefGoogle Scholar
  11. 11.
    Bhattacharyya, S., Tobacman, J.K.: Arylsulfatase B regulates colonic epithelial cell migration by effects on MMP9 expression and RhoA activation. Clin. Exp. Metastasis 26(6), 535–545 (2009)PubMedCrossRefGoogle Scholar
  12. 12.
    Achur, R.N., Valiyaveettil, M., Gowda, D.C.: The low sulfated chondroitin sulfate proteoglycans of human placenta have sulfate group-clustered domains that can efficiently bind Plasmodium falciparum-infected erythrocytes. J. Biol. Chem. 278, 11705–11713 (2003)PubMedCrossRefGoogle Scholar
  13. 13.
    Rogerson, S.J., Brown, G.: Chondroitin sulfate A as an adherence receptor for Plasmodium falciparum-infected erythrocytes. Parasitol. Today 13, 70–75 (1997)PubMedCrossRefGoogle Scholar
  14. 14.
    Bhattacharyya, S., Solakyildirim, K., Zhang, Z., Linhardt, R.J., Tobacman, J.K.: Cell-bound IL-8 increases in bronchial epithelial cells following Arylsulfatase B silencing. Am. J. Respir. Cell. Mol. Biol. 42(1), 51–61 (2010)PubMedCrossRefGoogle Scholar
  15. 15.
    Wòjczyk, B.: Lysosomal arylsulfatases A and B from horse blood leukocytes: purification and physico-chemical properties. Biol. Cell. 57, 147–152 (1986)PubMedCrossRefGoogle Scholar
  16. 16.
    Bhattacharyya, S., Kotlo, K., Shukla, S., Danziger, R.S., Tobacman, J.K.: Distinct effects of N-acetyl-galactosamine-4-sulfatase and galactose-6-sulfatase expression on chondroitin sulfates. J. Biol. Chem. 283(15), 9523–9530 (2008)PubMedCrossRefGoogle Scholar
  17. 17.
    Bhattacharyya, S., Look, D., Tobacman, J.K.: Increased arylsulfatase B activity in cystic fibrosis cells following correction of CFTR. Clin. Chim. Acta 380(1–2), 122–127 (2007)PubMedCrossRefGoogle Scholar
  18. 18.
    Yang, B., Chang, Y., Weyers, A.M., Sterner, E., Linhardt, R.J.: Disaccharide analysis of glycosaminoglycan mixtures by ultra-high-performance liquid chromatography-mass spectrometry. J. Chromatog. A 1225, 91–98 (2012)CrossRefGoogle Scholar
  19. 19.
    Yang, B., Weyers, A., Baik, J.Y., Sterner, E., Sharfstein, S., Mousa, S.A., Zhang, F., Dordick, J.S., Linhardt, R.J.: Ultra-performance ion-pairing liquid chromatography with on-line electrospray ion trap mass spectrometry for heparin disaccharide analysis. Anal. Biochem. 314, 59–66 (2011)CrossRefGoogle Scholar
  20. 20.
    Zhang, F., Sun, P., Muñoz, E., Chi, L., Sakai, S., Toida, T., Zhang, H., Mousa, S., Linhardt, R.J.: Microscale isolation and analysis of heparin from plasma using an anion-exchange spin column. Anal. Biochem. 353, 284–286 (2006)PubMedCrossRefGoogle Scholar
  21. 21.
    Hernáiz, M.J., Linhardt, R.J.: Degradation of chondroitin sulfate and dermatan sulfate with chondroitin lyases. Methods Mol. Biol. 171, 363–371 (2001)PubMedGoogle Scholar
  22. 22.
    Solakyildirim, K., Zhang, Z., Linhardt, R.J.: Ultraperformance liquid chromatography with electrospray ionization ion trap mass spectrometry for chondroitinal disaccharide analysis. Anal. Biochem. 397(1), 24–28 (2010)PubMedCrossRefGoogle Scholar
  23. 23.
    Yang, B., Bhattacharyya, S., Linhardt, R., Tobacman, J.: Exposure to common food additive carrageenan leads to reduced sulfatase activity and increase in sulfated glycosaminoglycans in human epithelial cells. Biochimie 94(6), 1309–1316 (2012)PubMedCrossRefGoogle Scholar
  24. 24.
    Bhattacharyya, S., Solakyildirim, K., Zhang, Z., Linhardt, R.J., Tobacman, J.K.: Chloroquine reduces arylsulphatase B activity and increases chondroitin-4-sulphate: implications for mechanisms of action and resistance. Malar. J. 8(1), 303 (2009)PubMedCrossRefGoogle Scholar
  25. 25.
    Rao, G.J., Christe, M.: Inhibition of rabbit liver arylsulfatase B by phosphate esters. Biochim. Biophys. Acta 788, 58–61 (1994)CrossRefGoogle Scholar
  26. 26.
    Bilusic, M., Bataillard, A., Tschannen, M.R., Gao, L., Barreto, N.E., Vincent, M., Wang, T., Jacob, H.J., Sassard, J., Kwitek, A.E.: Mapping the genetic determinants of hypertension, metabolic diseases, and related phenotypes in the Lyon hypertensive rat. Hypertension 44, 695–701 (2004)PubMedCrossRefGoogle Scholar
  27. 27.
    Duong, C., Charron, S., Xiao, C., Hamet, P., Menard, A., Roy, J., Deng, A.Y.: Distinct quantitative trait loci for kidney, cardiac, and aortic mass dissociated from and associated with blood pressure in Dahl congenic rats. Mamm. Genome 17(12), 1147–1161 (2006)PubMedCrossRefGoogle Scholar
  28. 28.
    Garrett, M.R., Joe, B., Dene, H., Rapp, J.P.: Identification of blood pressure quantitative trait loci that differentiate two hypertensive strains. J. Hypertens. 20(12), 2399–2406 (2002)PubMedCrossRefGoogle Scholar
  29. 29.
    Garrett, M.R., Dene, H., Walder, R., Zhang, Q.Y., Cicila, G.T., Assadnia, S., Deng, A.Y., Rapp, J.P.: Genome scan and congenic strains for blood pressure QTL using Dahl salt-sensitive rats. Genome Res. 8(7), 711–723 (1998)PubMedGoogle Scholar
  30. 30.
    Schork, N.J., Krieger, J.E., Trolliet, M.R., Franchini, K.G., Koike, G., Krieger, E.M., Lander, E.S., Dzau, V.J., Jacob, H.J.: A biometrical genome search in rats reveals the multigenic basis of blood pressure variation. Genome Res. 5, 164–172 (1995)PubMedCrossRefGoogle Scholar
  31. 31.
    Ye, Z.Y., Li, D.P., Byun, H.S., Li, L., Pan, H.L.: NKCC1 upregulation disrupts chloride homeostasis in the hypothalamus and increases neuronal activity-sympathetic drive in hypertension. J. Neurosci. 32(25), 8560–8568 (2012)PubMedCrossRefGoogle Scholar
  32. 32.
    Trepiccione, F., Zacchia, M., Capasso, G.: The role of the kidney in salt-sensitive hypertension. Clin. Exp. Nephrol. 16(1), 68–72 (2012)PubMedCrossRefGoogle Scholar
  33. 33.
    Etscheid, M., Beer, N., Fink, E., Seitz, R., Johannes, D.: The hyaluronan-binding serine protease from human plasma cleaves HMW and LMW kininogen and releases bradykinin. Biol. Chem. 383(10), 1633–1643 (2002)PubMedCrossRefGoogle Scholar
  34. 34.
    Batlle, D., Redon, J., Gutterman, C., LaPointe, M., Saleh, A., Sharma, A., Rombola, G., Ye, M., Alsheikha, W., Gomez, L., Sobrero, M.: Acid–base status and intracellular pH regulation in lymphocytes from rats with genetic hypertension. J. Am. Soc. Nephrol. 5(5Suppl 1), S12–S22 (1994)PubMedGoogle Scholar
  35. 35.
    Cuthbert, A.W.: New horizons in the treatment of cystic fibrosis: Br. J. Pharmacol. 163(1), 173–183 (2011)Google Scholar
  36. 36.
    Sharma, M., Benharounga, M., Hu, W., Lukacs, G.L.: Conformation and temperature-sensitive stability defects of the ∆F508 cystic fibrosis transmembrane conductance regulator in post-endoplasmic reticulum compartments. J. Biol. Chem. 276(12), 8942–8950 (2001)PubMedCrossRefGoogle Scholar
  37. 37.
    Cosma, M.P., Pepe, S., Annunziata, I., Newbold, R.F., Grompe, M., Parenti, G., Ballabio, A.: The multiple sulfatase deficiency gene encodes an essential and limiting factor for the activity of sulfatases. Cell 113(4), 445–456 (2003)PubMedCrossRefGoogle Scholar
  38. 38.
    Roeser, D., Preusser-Kunze, A., Schmidt, B., Gasow, K., Wittmann, J.G., Dierks, T., von Figura, K., Rudolph, M.G.: A general binding mechanism for all human sulfatases by the formylglycine-generating enzyme. Proc. Natl. Acad. Sci. U. S. A. 103(1), 81–86 (2006)PubMedCrossRefGoogle Scholar
  39. 39.
    Bhattacharyya, S., Tobacman, J.K.: Hypoxia reduces arylsulfatase B activity and silencing arylsulfatase B replicates and mediates the effects of hypoxia. PLoS One 7(3), e33250 (2012)PubMedCrossRefGoogle Scholar
  40. 40.
    Roeser, D., Schmidt, B., Preusser-Kunze, A., Rudolph, M.G.: Probing the oxygen-binding site of the human formylglycine generating enzyme using halide ions. Acta Crystallog. D Biol. Crystallogr. 63(Pt 5), 621–627 (2007)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York (outside the USA) 2013

Authors and Affiliations

  • Kumar Kotlo
    • 1
    • 2
  • Sumit Bhattacharyya
    • 1
    • 2
  • Bo Yang
    • 4
  • Leonid Feferman
    • 1
    • 2
  • Shah Tejaskumar
    • 3
  • Robert Linhardt
    • 4
  • Robert Danziger
    • 1
    • 2
  • Joanne K. Tobacman
    • 1
    • 2
    • 5
  1. 1.University of Illinois at ChicagoChicagoUSA
  2. 2.Jesse Brown VA Medical CenterChicagoUSA
  3. 3.Rosalind Franklin University of Medicine and ScienceNorth ChicagoUSA
  4. 4.Rensselaer Polytechnic UniversityTroyUSA
  5. 5.Department of MedicineUniversity of Illinois at ChicagoChicagoUSA

Personalised recommendations