Skip to main content
Log in

Kidney transplantation recovers the reduction level of serum sulfatide in ESRD patients via processes correlated to oxidative stress and platelet count

  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Sulfatide is a major component of glycosphingolipids in lipoproteins. Recently, we reported that a low serum level of sulfatide in hemodialysis patients might be related to the high incidence of cardiovascular diseases. However, the serum kinetics of sulfatide in kidney disease patients and the function of endogenous serum sulfatide are still unclear. To obtain novel knowledge concerning these issues, we investigated the serum kinetics of sulfatide in 5 adult kidney transplant recipients. We also analyzed the correlated factors influencing the serum sulfatide level, using multiple regression analysis. Kidney transplantation caused a dramatic increase of serum sulfatide without an alteration of its composition in all recipients in a time-dependent manner; however, the recovery speed was slower than that of the improvement of kidney function and the serum sulfatide reached a nearly normal level after 1 year. Multiple regression analysis showed that the significant correlated factor influencing the serum sulfatide level was log duration (time parameter) throughout the observation period, and the correlated factors detected in the stable phase were the decrease of serum concentration of malondialdehyde (an oxidative stress marker) as well as the elevation of platelet count. The current study results demonstrated the gradual but reliable recovery of the serum sulfatide level in kidney transplant recipients for the first time, suggesting a close correlation between serum sulfatide and kidney function. The recovery of serum sulfatide might derive from the attenuation of systemic oxidative stress. The normal level of serum sulfatide in kidney transplant recipients might affect platelet function, and contribute to the reduction of cardiovascular disease incidence.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

AKI:

Acute kidney injury

CST:

Cerebroside sulfotransferase

CVD:

Cardiovascular disease

ESRD:

End-stage renal disease

GP:

Glycoproteins

HD:

Hemodialysis therapy

LS:

Lysosulfatide

d18:2:

Sphingadienine

d18:1:

(4E)-sphingenine

d18:0:

Sphinganine

t18:0:

Phytosphingosine

d20:1:

(4E)-icosasphingenine

d20:0:

Icosasphinganine

t20:0:

4D-hydroxyicosasphinganine

MALDI-TOF MS:

Matrix-assisted laser desorption ionization-time of flight mass spectrometry

MDA:

Malondialdehyde

PD:

Peritoneal dialysis therapy

SD:

Standard deviation

vWF:

Von Willebrand factor

References

  1. Ishizuka, I.: Chemistry and functional distribution of sulfoglycolipids. Prog Lipid Res 36, 245–319 (1997)

    Article  PubMed  CAS  Google Scholar 

  2. Honke, K., Zhang, Y., Cheng, X., Kotani, N., Taniguchi, N.: Biological roles of sulfoglycolipids and pathophysiology of their deficiency. Glycoconj J 21, 59–62 (2004)

    Article  PubMed  CAS  Google Scholar 

  3. Nagai, K., Tadano-Aritomi, K., Niimura, Y., Ishizuka, I.: Higher expression of renal sulfoglycolipids in marine mammals. Glycoconj J 25, 723–726 (2008)

    Article  PubMed  CAS  Google Scholar 

  4. Hara, A., Taketomi, T.: Occurrence of sulfatide as a major glycosphingolipid in WHHL rabbit serum lipoproteins. J Biochem 102, 83–92 (1987)

    PubMed  CAS  Google Scholar 

  5. Zhu, X.H., Hara, A., Taketomi, T.: The existence of galactosylceramide I3-sulfate in serums of various mammals and its anticoagulant activity. J Biochem 110, 241–245 (1991)

    PubMed  CAS  Google Scholar 

  6. Kyogashima, M.: The role of sulfatide in thrombogenesis and haemostasis. Arch Biochem Biophys 426, 157–162 (2004)

    Article  PubMed  CAS  Google Scholar 

  7. Hara, A., Taketomi, T.: Characterization and changes of glycosphingolipids in the aorta of the Watanabe hereditable hyperlipidemic rabbit. J Biochem 109, 904–908 (1991)

    PubMed  CAS  Google Scholar 

  8. Hara, A., Uemura, K., Taketomi, T.: Sulfatide prolongs blood-coagulation time and bleeding time by forming a complex with fibrinogen. Glycoconj J 13, 187–194 (1996)

    Article  PubMed  CAS  Google Scholar 

  9. Hu, R., Li, G., Kamijo, Y., Aoyama, T., Nakajima, T., Inoue, T., Node, K., Kannagi, R., Kyogashima, M., Hara, A.: Serum sulfatides as a novel biomarker for cardiovascular disease in patients with end-stage renal failure. Glycoconj J 24, 565–571 (2007)

    Article  PubMed  CAS  Google Scholar 

  10. Zhang, X., Nakajima, T., Kamijo, Y., Li, G., Hu, R., Kannagi, R., Kyogashima, M., Aoyama, T., Hara, A.: Acute kidney injury induced by protein-overload nephropathy down-regulates gene expression of hepatic cerebroside sulfotransferase in mice, resulting in reduction of liver and serum sulfatides. Biochem Biophys Res Commun 390, 1382–1388 (2009)

    Article  PubMed  CAS  Google Scholar 

  11. Matsuo, S., Imai, E., Horio, M., Yasuda, Y., Tomita, K., Nitta, K., Yamagata, K., Tomino, Y., Yokoyama, H., Hishida, A.: Collaborators developing the Japanese equation for estimated GFR: revised equations for estimated GFR from serum creatinine in Japan. Am J Kidney Dis 53, 982–992 (2009)

    Article  PubMed  CAS  Google Scholar 

  12. Hara, A., Radin, N.S.: Lipid extraction of tissues with a low-toxicity solvent. Anal Biochem 90, 420–426 (1978)

    Article  PubMed  CAS  Google Scholar 

  13. Li, G., Hu, R., Kamijo, Y., Nakajima, T., Aoyama, T., Inoue, T., Node, K., Kannagi, R., Kyogashima, M., Hara, A.: Establishment of a quantitative, qualitative, and high-throughput analysis of sulfatides from small amounts of sera by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Anal Biochem 362, 1–7 (2007)

    Article  PubMed  CAS  Google Scholar 

  14. Sugiyama, E., Hara, A., Uemura, K.: A quantitative analysis of serum sulfatide by matrix-assisted laser desorption ionization time-of-flight mass spectrometry with delayed ion extraction. Anal Biochem 274, 90–97 (1999)

    Article  PubMed  CAS  Google Scholar 

  15. Aoyama, T., Peters, J.M., Iritani, N., Nakajima, T., Furihata, K., Hashimoto, T., Gonzalez, F.J.: Altered constitutive expression of fatty acid-metabolizing enzymes in mice lacking the peroxisome proliferator-activated receptor alpha (PPARalpha). J Biol Chem 273, 5678–5684 (1998)

    Article  PubMed  CAS  Google Scholar 

  16. Aoyama, T., Uchida, Y., Kelley, R.I., Marble, M., Hofman, K., Tonsgard, J.H., Rhead, W.J., Hashimoto, T.: A novel disease with deficiency of mitochondrial very-long-chain acyl-CoA dehydrogenase. Biochem Biophys Res Commun 191, 1369–1372 (1993)

    Article  PubMed  CAS  Google Scholar 

  17. Aoyama, T., Yamano, S., Waxman, D.J., Lapenson, D.P., Meyer, U.A., Fischer, V., Tyndale, R., Inaba, T., Kalow, W., Gelboin, H.V., Gonzalez, F.J.: Cytochrome P-450 hPCN3, a novel cytochrome P-450 IIIA gene product that is differentially expressed in adult human liver. cDNA and deduced amino acid sequence and distinct specificities of cDNA-expressed hPCN1 and hPCN3 for the metabolism of steroid hormones and cyclosporine. J Biol Chem 264, 10388–10395 (1989)

    PubMed  CAS  Google Scholar 

  18. Roberts, D.D., Rao, C.N., Magnani, J.L., Spitalnik, S.L., Liotta, L.A., Ginsburg, V.: Laminin binds specifically to sulfated glycolipids. Proc Natl Acad Sci U S A 82, 1306–1310 (1985)

    Article  PubMed  CAS  Google Scholar 

  19. Roberts, D.D., Haverstick, D.M., Dixit, V.M., Frazier, W.A., Santoro, S.A., Ginsburg, V.: The platelet glycoprotein thrombospondin binds specifically to sulfated glycolipids. J Biol Chem 260, 9405–9411 (1985)

    PubMed  CAS  Google Scholar 

  20. Roberts, D.D., Williams, S.B., Gralnick, H.R., Ginsburg, V.: Von Willebrand factor binds specifically to sulfated glycolipids. J Biol Chem 261, 3306–3309 (1986)

    PubMed  CAS  Google Scholar 

  21. Merten, M., Thiagarajan, P.: Role for sulfatides in platelet aggregation. Circulation 104, 2955–2960 (2001)

    Article  PubMed  CAS  Google Scholar 

  22. Jones, J.C., Dehart, G.W., Gonzales, M., Goldfinger, L.E.: Laminins: an overview. Microsc Res Tech 51, 211–213 (2000)

    Article  PubMed  CAS  Google Scholar 

  23. Hawiger, J.: Mechanisms involved in platelet vessel wall interaction. Thromb Haemost 74, 369–372 (1995)

    PubMed  CAS  Google Scholar 

  24. Borthakur, G., Cruz, M.A., Dong, J.F., McIntire, L., Li, F., López, J.A., Thiagarajan, P.: Sulfatides inhibit platelet adhesion to von Willebrand factor in flowing blood. J Thromb Haemost 1, 1288–1295 (2003)

    Article  PubMed  CAS  Google Scholar 

  25. Sarnak, M.J., Levey, A.S., Schoolwerth, A.C., Coresh, J., Culleton, B., Hamm, L.L., McCullough, P.A., Kasiske, B.L., Kelepouris, E., Klag, M.J., Parfrey, P., Pfeffer, M., Raij, L., Spinosa, D.J., Wilson, P.W., American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention: Kidney disease as a risk factor for development of cardiovascular disease: a statement from the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Circulation 108, 2154–2169 (2003)

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

This work was supported in part by GL Sciences (Tokyo, Japan) and Shinshu Public Utility Foundation for the Promotion of Medical Sciences (Matsumoto, Japan).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yuji Kamijo.

Additional information

Lixuan Wang and Yuji Kamijo contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, L., Kamijo, Y., Matsumoto, A. et al. Kidney transplantation recovers the reduction level of serum sulfatide in ESRD patients via processes correlated to oxidative stress and platelet count. Glycoconj J 28, 125–135 (2011). https://doi.org/10.1007/s10719-011-9329-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-011-9329-2

Keywords

Navigation