Skip to main content
SpringerLink
Log in

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

  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  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. Glaser, J.H., Conrad, H.E.: Chondroitin SO4 catabolism in chick embryo chondrocytes. J. Biol. Chem. 254, 2316–2325 (1978)

    Google Scholar 

  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)

    PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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. Renné, T., Schuh, K., Müller-Esterl, W.: Local bradykinin formation is controlled by glycosaminoglycans. J. Immunol. 175, 3377–3385 (2005)

    PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  Google Scholar 

  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. 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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  13. Rogerson, S.J., Brown, G.: Chondroitin sulfate A as an adherence receptor for Plasmodium falciparum-infected erythrocytes. Parasitol. Today 13, 70–75 (1997)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  15. Wòjczyk, B.: Lysosomal arylsulfatases A and B from horse blood leukocytes: purification and physico-chemical properties. Biol. Cell. 57, 147–152 (1986)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  CAS  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  21. Hernáiz, M.J., Linhardt, R.J.: Degradation of chondroitin sulfate and dermatan sulfate with chondroitin lyases. Methods Mol. Biol. 171, 363–371 (2001)

    PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  25. Rao, G.J., Christe, M.: Inhibition of rabbit liver arylsulfatase B by phosphate esters. Biochim. Biophys. Acta 788, 58–61 (1994)

    Article  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  32. Trepiccione, F., Zacchia, M., Capasso, G.: The role of the kidney in salt-sensitive hypertension. Clin. Exp. Nephrol. 16(1), 68–72 (2012)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    PubMed  CAS  Google Scholar 

  35. Cuthbert, A.W.: New horizons in the treatment of cystic fibrosis: Br. J. Pharmacol. 163(1), 173–183 (2011)

    CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  PubMed  CAS  Google Scholar 

  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)

    Article  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. University of Illinois at Chicago, Chicago, IL, 60612, USA

    Kumar Kotlo, Sumit Bhattacharyya, Leonid Feferman, Robert Danziger & Joanne K. Tobacman

  2. Jesse Brown VA Medical Center, Chicago, IL, 60612, USA

    Kumar Kotlo, Sumit Bhattacharyya, Leonid Feferman, Robert Danziger & Joanne K. Tobacman

  3. Rosalind Franklin University of Medicine and Science, North Chicago, IL, 60064, USA

    Shah Tejaskumar

  4. Rensselaer Polytechnic University, Troy, NY, USA

    Bo Yang & Robert Linhardt

  5. Department of Medicine, University of Illinois at Chicago, 840 S. Wood St., CSN 440, M/C 718, Chicago, IL, 60612, USA

    Joanne K. Tobacman

Authors
  1. Kumar Kotlo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sumit Bhattacharyya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bo Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leonid Feferman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shah Tejaskumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Robert Linhardt
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Robert Danziger
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Joanne K. Tobacman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joanne K. Tobacman.

Additional information

Kumar Kotlo and Sumit Bhattacharyya are co-first authors.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kotlo, K., Bhattacharyya, S., Yang, B. et al. Impact of salt exposure on N-acetylgalactosamine-4-sulfatase (arylsulfatase B) activity, glycosaminoglycans, kininogen, and bradykinin. Glycoconj J 30, 667–676 (2013). https://doi.org/10.1007/s10719-013-9468-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-013-9468-8

Keywords

Search

Navigation