Stimulation of suicidal death of erythrocytes by rifampicin

Toxicology

Volumn 302, Issue 2-3, 2012, Pages 123-128

  Abed, Majed ^a,b   Towhid, Syeda T ^a   Shaik, Nazneen ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b University of Al Furat   (Syrian Arab Republic)

Author keywords

Calcium; Cell volume; Ceramide; Eryptosis; Phosphatidylserine (PS); Rifampicin

Indexed keywords

ANNEXIN; CALCIUM ION; CERAMIDE; HEMOGLOBIN; PHOSPHATIDYLSERINE; RIFAMPICIN; ANILINE DERIVATIVE; CALCIUM; FLUO 3; TUBERCULOSTATIC AGENT; XANTHENE DERIVATIVE;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL STIMULATION; CELL VOLUME; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ERYPTOSIS; ERYTHROCYTE; EXTRACELLULAR CALCIUM; FLOW CYTOMETRY; FLUORESCENCE; FLUORESCENT ANTIBODY TECHNIQUE; HEMOLYSIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECRETION; CELL DEATH; CELL MEMBRANE; CELL SIZE; CYTOLOGY; CYTOSOL; DRUG EFFECT; METABOLISM;

ANILINE COMPOUNDS; ANTIBIOTICS, ANTITUBERCULAR; APOPTOSIS; CALCIUM; CELL DEATH; CELL MEMBRANE; CELL SIZE; CERAMIDES; CYTOSOL; ERYTHROCYTES; FLOW CYTOMETRY; HEMOLYSIS; HUMANS; PHOSPHATIDYLSERINES; RIFAMPIN; XANTHENES;

EID: 84868445257     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2012.10.006     Document Type: Article

References (86)

1. Ahrens, N., Genth, R., Salama, A., 2002. Belated diagnosis in three patients with rifampicin-induced immune haemolytic anaemia. Br. J. Haematol. 117, 441-443.
2. Andrews, D.A., Low, P.S., 1999. Role of red blood cells in thrombosis. Curr. Opin. Hematol. 6, 76-82.
3. Arboleda, G., Huang, T.J., Waters, C., Verkhratsky, A., Fernyhough, P., Gibson, R.M., 2007. Insulin-like growth factor-1-dependent maintenance of neuronal metabolism through the phosphatidylinositol 3-kinase-Akt pathway is inhibited by C2-ceramide in CAD cells. Eur. J. Neurosci. 25, 3030-3038.
4. Becker, K.A., Grassme, H., Zhang, Y., Gulbins, E., 2010. Ceramide in Pseudomonas aeruginosa infections and cystic fibrosis. Cell. Physiol. Biochem. 26, 57-66.
5. Berg, C.P., Engels, I.H., Rothbart, A., Lauber, K., Renz, A., Schlosser, S.F., Schulze-Osthoff, K., Wesselborg, S., 2001. Human mature red blood cells express caspase-3 and caspase-8 but are devoid of mitochondrial regulators of apoptosis. Cell Death Differ. 8, 1197-1206.
6. Bhavsar, S.K., Bobbala, D., Xuan, N.T., Foller, M., Lang, F., 2010a. Stimulation of suicidal erythrocyte death by alpha-lipoic acid. Cell. Physiol. Biochem. 26, 859-868.
7. Bhavsar, S.K., Eberhard, M., Bobbala, D., Lang, F., 2010b. Monensin induced suicidal erythrocyte death. Cell. Physiol. Biochem. 25, 745-752.
8. Bhavsar, S.K., Gu, S., Bobbala, D., Lang, F., 2011. Janus kinase 3 is expressed in erythrocytes phosphorylated upon energy depletion and involved in the regulation of suicidal erythrocyte death. Cell. Physiol. Biochem. 27, 547-556.
9. Birka, C., Lang, P.A., Kempe, D.S., Hoefling, L., Tanneur, V., Duranton, C., Nammi, S., Henke, G., Myssina, S., Krikov, M., Huber, S.M., Wieder, T., Lang, F., 2004. Enhanced susceptibility to erythrocyte apoptosis following phosphate depletion. Pflugers Arch. 448, 471-477.
10. Bobbala, D., Alesutan, I., Foller, M., Huber, S.M., Lang, F., 2010. Effect of anandamide in Plasmodium berghei-infected mice. Cell. Physiol. Biochem. 26, 355-362.
11. Bookchin, R.M., Ortiz, O.E., Lew, V.L., 1987. Activation of calcium-dependent potassium channels in deoxygenated sickled red cells. Prog. Clin. Biol. Res. 240, 193-200.
12. Borst, O., Abed, M., Alesutan, I., Towhid, S.T., Qadri, S.M., Foller, M., Gawaz, M., Lang, F., 2012. Dynamic adhesion of eryptotic erythrocytes to endothelial cells via CXCL16/SR-PSOX. Am. J. Physiol. Cell Physiol. 302, C644-C651.
13. Brand, V.B., Sandu, C.D., Duranton, C., Tanneur, V., Lang, K.S., Huber, S.M., Lang, F., 2003. Dependence of Plasmodium falciparum in vitro growth on the cation permeability of the human host erythrocyte. Cell. Physiol. Biochem. 13, 347-356.
14. Bratosin, D., Estaquier, J., Petit, F., Arnoult, D., Quatannens, B., Tissier, J.P., Slomianny, C., Sartiaux, C., Alonso, C., Huart, J.J., Montreuil, J., Ameisen, J.C., 2001. Programmed cell death in mature erythrocytes: a model for investigating death effector pathways operating in the absence of mitochondria. Cell Death Differ. 8, 1143-1156.
15. Brugnara, C., de Franceschi, L., Alper, S.L. 1993. Inhibition of Ca(2+)-dependent K+ transport and cell dehydration in sickle erythrocytes by clotrimazole and other imidazole derivatives. J. Clin. Invest. 92, 520-526.
16. Calderon-Salinas, J.V., Munoz-Reyes, E.G., Guerrero-Romero, J.F., Rodriguez-Moran, M., Bracho-Riquelme, R.L., Carrera-Gracia, M.A., Quintanar-Escorza, M.A., 2011. Eryptosis and oxidative damage in type 2 diabetic mellitus patients with chronic kidney disease. Mol. Cell. Biochem. 357, 171-179.
17. Chen, J., Raymond, K., 2006. Roles of rifampicin in drug-drug interactions: underlying molecular mechanisms involving the nuclear pregnane X receptor. Ann. Clin. Microbiol. Antimicrob. 5, 3.
18. Chung, S.M., Bae, O.N., Lim, K.M., Noh, J.Y., Lee, M.Y., Jung, Y.S., Chung, J.H., 2007. Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler. Thromb. Vasc. Biol. 27, 414-421.
19. Closse, C., Dachary-Prigent, J., Boisseau, M.R., 1999. Phosphatidylserine-related adhesion of human erythrocytes to vascular endothelium. Br. J. Haemtol. 107, 300-302.
20. Covic, A., Goldsmith, D.J., Segall, L., Stoicescu, C., Lungu, S., Volovat, C., Covic, M., 1998. Rifampicin-induced acute renal failure: a series of 60 patients. Nephrol. Dial. Transplant 13, 924-929.
21. de la Monte, S.M., 2009. Insulin resistance and Alzheimer's disease. BMB Rep. 42, 475-481.
22. De Vriese, A.S., Robbrecht, D.L., Vanholder, R.C., Vogelaers, D.P., Lameire, N.H., 1998. Rifampicin-associated acute renal failure: pathophysiologic immunologic, and clinical features. Am. J. Kidney Dis. 31, 108-115.
23. Dhami, R., He, X., Schuchman, E.H., 2010. Acid sphingomyelinase deficiency attenuates bleomycin-induced lung inflammation and fibrosis in mice. Cell. Physiol. Biochem. 26, 749-760.
24. Donald, P.R., Maritz, J.S., Diacon, A.H., 2011. The pharmacokinetics and pharmacodynamics of rifampicin in adults and children in relation to the dosage recommended for children. Tuberculosis (Edinb.) 91, 196-207.
25. Drapeau, C.M., Grilli, E., Petrosillo, N., 2010. Rifampicin combined regimens for gramnegative infections: data from the literature. Int. J. Antimicrob. Agents 35, 39-44.
26. Eberhard, M., Ferlinz, K., Alizzi, K., Cacciato, P.M., Faggio, C., Foller, M., Lang, F., 2010. FTY720-induced suicidal erythrocyte death. Cell. Physiol. Biochem. 26, 761-766.
27. Felder, K.M., Hoelzle, K., Ritzmann, M., Kilchling, T., Schiele, D., Heinritzi, K., Groebel, K., Hoelzle, L.E., 2011. Hemotrophic mycoplasmas induce programmed cell death in red blood cells. Cell. Physiol. Biochem. 27, 557-564.
28. Foller, M., Feil, S., Ghoreschi, K., Koka, S., Gerling, A., Thunemann, M., Hofmann, F., Schuler, B., Vogel, J., Pichler, B., Kasinathan, R.S., Nicolay, J.P., Huber, S.M., Lang, F., Feil, R., 2008a. Anemia and splenomegaly in cGKI-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 105, 6771-6776.
29. Foller, M., Huber, S.M., Lang, F., 2008b. Erythrocyte programmed cell death. IUBMB Life 60, 661-668.
30. Foller, M., Kasinathan, R.S., Koka, S., Lang, C., Shumilina, E., Birnbaumer, L., Lang, F., Huber, S.M., 2008c. TRPC6 contributes to the Ca(2+) leak of human erythrocytes. Cell. Physiol. Biochem. 21, 183-192.
31. Foller, M., Bobbala, D., Koka, S., Huber, S.M., Gulbins, E., Lang, F., 2009a. Suicide for survival-death of infected erythrocytes as a host mechanism to survive malaria. Cell. Physiol. Biochem. 24, 133-140.
32. Foller, M., Mahmud, H., Gu, S., Wang, K., Floride, E., Kucherenko, Y., Luik, S., Laufer, S., Lang, F., 2009b. Participation of leukotriene C(4) in the regulation of suicidal erythrocyte death. J. Physiol. Pharmacol. 60, 135-143.
33. Foller, M., Sopjani, M., Koka, S., Gu, S., Mahmud, H., Wang, K., Floride, E., Schleicher, E., Schulz, E., Munzel, T., Lang, F., 2009c. Regulation of erythrocyte survival by AMP-activated protein kinase. FASEB J. 23, 1072-1080.
34. Gallagher, P.G., Chang, S.H., Rettig, M.P., Neely, J.E., Hillery, C.A., Smith, B.D., Low, P.S., 2003. Altered erythrocyte endothelial adherence and membrane phospholipid asymmetry in hereditary hydrocytosis. Blood 101, 4625-4627.
35. Ganesan, S., Chaurasiya, N.D., Sahu, R., Walker, L.A., Tekwani, B.L., 2012. Understanding the mechanisms for metabolism-linked hemolytic toxicity of primaquine against glucose 6-phosphate dehydrogenase deficient human erythrocytes: evaluation of eryptotic pathway. Toxicology 294, 54-60.
36. Gao, M., Cheung, K.L., Lau, I.P., Yu, W.S., Fung, K.P., Yu, B., Loo, J.F., Kong, S.K., 2012. Polyphyllin D induces apoptosis in human erythrocytes through Ca(2+) rise and membrane permeabilization. Arch. Toxicol. 86, 741-752.
37. Gao, X.F., Li, J., Yang, Z.W., Li, Y.P., 2009. Rifapentine vs. rifampicin for the treatment of pulmonary tuberculosis: a systematic review. Int. J. Tuberc. Lung Dis. 13, 810-819.
38. Gatidis, S., Zelenak, C., Fajol, A., Lang, E., Jilani, K., Michael, D., Qadri, S.M., Lang, F., 2011. p38 MAPK activation and function following osmotic shock of erythrocytes. Cell. Physiol. Biochem. 28, 1279-1286.
39. Ghashghaeinia, M., Toulany, M., Saki, M., Bobbala, D., Fehrenbacher, B., Rupec, R., Rodemann, H.P., Ghoreschi, K., Rocken, M., Schaller, M., Lang, F., Wieder, T., 2011. The NFkB pathway inhibitors bay 11-7082 and parthenolide induce programmed cell death in anucleated erythrocytes. Cell. Physiol. Biochem. 27, 45-54.
40. Greka, A., Mundel, P., 2011. Balancing calcium signals through TRPC5 and TRPC6 in podocytes. J. Am. Soc. Nephrol. 22, 1969-1980.
41. Holland, W.L., Summers, S.A., 2008. Sphingolipids insulin resistance, and metabolic disease: new insights from in vivo manipulation of sphingolipid metabolism. Endocr. Rev. 29, 381-402.
42. Kempe, D.S., Lang, P.A., Duranton, C., Akel, A., Lang, K.S., Huber, S.M., Wieder, T., Lang, F., 2006. Enhanced programmed cell death of iron-deficient erythrocytes. FASEB J. 20, 368-370.
43. Kempe, D.S., Akel, A., Lang, P.A., Hermle, T., Biswas, R., Muresanu, J., Friedrich, B., Dreischer, P., Wolz, C., Schumacher, U., Peschel, A., Gotz, F., Doring, G., Wieder, T., Gulbins, E., Lang, F., 2007. Suicidal erythrocyte death in sepsis. J. Mol. Med. 85, 273-281.
44. Klarl, B.A., Lang, P.A., Kempe, D.S., Niemoeller, O.M., Akel, A., Sobiesiak, M., Eisele, K., Podolski, M., Huber, S.M., Wieder, T., Lang, F., 2006. Protein kinase C mediates erythrocyte programmed cell death following glucose depletion. Am. J. Physiol. Cell Physiol. 290, C244-C253.
45. Koka, S., Bobbala, D., Lang, C., Boini, K.M., Huber, S.M., Lang, F., 2009. Influence of paclitaxel on parasitemia and survival of Plasmodium berghei infected mice. Cell. Physiol. Biochem. 23, 191-198.
46. Kornhuber, J., Tripal, P., Reichel, M., Muhle, C., Rhein, C., Muehlbacher, M., Groemer, T.W., Gulbins, E., 2010. Functional Inhibitors of Acid Sphingomyelinase (FIASMAs): a novel pharmacological group of drugs with broad clinical applications. Cell. Physiol. Biochem. 26, 9-20.
47. Kuebler, W.M., Yang, Y., Samapati, R., Uhlig, S., 2010. Vascular barrier regulation by PAF, ceramide, caveolae, and NO - an intricate signaling network with discrepant effects in the pulmonary and systemic vasculature. Cell. Physiol. Biochem. 26, 29-40.
48. Lang, K.S., Duranton, C., Poehlmann, H., Myssina, S., Bauer, C., Lang, F., Wieder, T., Huber, S.M., 2003. Cation channels trigger apoptotic death of erythrocytes. Cell Death Differ. 10, 249-256.
49. Lang, K.S., Myssina, S., Brand, V., Sandu, C., Lang, P.A., Berchtold, S., Huber, S.M., Lang, F., Wieder, T., 2004. Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes. Cell Death Differ. 11, 231-243.
50. Lang, P.A., Beringer, O., Nicolay, J.P., Amon, O., Kempe, D.S., Hermle, T., Attanasio, P., Akel, A., Schafer, R., Friedrich, B., Risler, T., Baur, M., Olbricht, C.J., Zimmerhackl, L.B., Zipfel, P.F., Wieder, T., Lang, F., 2006. Suicidal death of erythrocytes in recurrent hemolytic uremic syndrome. J Mol. Med. 84, 378-388.
51. Lang, P.A., Schenck, M., Nicolay, J.P., Becker, J.U., Kempe, D.S., Lupescu, A., Koka, S., Eisele, K., Klarl, B.A., Rubben, H., Schmid, K.W., Mann, K., Hildenbrand, S., Hefter, H., Huber, S.M., Wieder, T., Erhardt, A., Haussinger, D., Gulbins, E., Lang, F., 2007. Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat. Med. 13, 164-170.
52. Lang, F., Gulbins, E., Lerche, H., Huber, S.M., Kempe, D.S., Foller, M., 2008. Eryptosis a window to systemic disease. Cell. Physiol. Biochem. 22, 373-380.
53. Lang, P.A., Kasinathan, R.S., Brand, V.B., Duranton, C., Lang, C., Koka, S., Shumilina, E., Kempe, D.S., Tanneur, V., Akel, A., Lang, K.S., Foller, M., Kun, J.F., Kremsner, P.G., Wesselborg, S., Laufer, S., Clemen, C.S., Herr, C., Noegel, A.A., Wieder, T., Gulbins, E., Lang, F., Huber, S.M., 2009. Accelerated clearance of Plasmodiuminfected erythrocytes in sickle cell trait and annexin-A7 deficiency. Cell. Physiol. Biochem. 24, 415-428.
54. Lang, F., Gulbins, E., Lang, P.A., Zappulla, D., Foller, M., 2010. Ceramide in suicidal death of erythrocytes. Cell. Physiol. Biochem. 26, 21-28.
55. Lang, E., Jilani, K., Zelenak, C., Pasham, V., Bobbala, D., Qadri, S.M., Lang, F., 2011. Stimulation of suicidal erythrocyte death by benzethonium. Cell. Physiol. Biochem. 28, 347-354.
56. Lau, I.P., Chen, H., Wang, J., Ong, H.C., Leung, K.C., Ho, H.P., Kong, S.K., 2011. In vitro effect of CTAB- and PEG-coated gold nanorods on the induction of eryptosis/ erythroptosis in human erythrocytes. Nanotoxicology.
57. Li, X., Becker, K.A., Zhang, Y., 2010. Ceramide in redox signaling and cardiovascular diseases. Cell. Physiol. Biochem. 26, 41-48.
58. 2+-dependent pathway without caspase-3 activation. Arch. Toxicol. 81, 859-865.
59. Maellaro, E., Leoncini, S., Moretti, D., Del Bello, B., Tanganelli, I., De Felice, C., Ciccoli, L., 2011. Erythrocyte caspase-3 activation and oxidative imbalance in erythrocytes and in plasma of type 2 diabetic patients. Acta Diabetol.
60. Mahmud, H., Foller, M., Lang, F., 2008. Suicidal erythrocyte death triggered by cisplatin. Toxicology 249, 40-44.
61. Mahmud, H., Foller, M., Lang, F., 2009. Arsenic-induced suicidal erythrocyte death. Arch. Toxicol. 83, 107-113.
62. Muthukumar, T., Jayakumar, M., Fernando, E.M., Muthusethupathi, M.A., 2002. Acute renal failure due to rifampicin: a study of 25 patients. Am. J. Kidney Dis. 40, 690-696.
63. Myssina, S., Huber, S.M., Birka, C., Lang, P.A., Lang, K.S., Friedrich, B., Risler, T., Wieder, T., Lang, F., 2003. Inhibition of erythrocyte cation channels by erythropoietin. J. Am. Soc. Nephrol. 14, 2750-2757.
64. Nguyen, D.B., Wagner-Britz, L., Maia, S., Steffen, P., Wagner, C., Kaestner, L., Bernhardt, I., 2011. Regulation of phosphatidylserine exposure in red blood cells. Cell. Physiol. Biochem. 28, 847-856.
65. Nicolay, J.P., Schneider, J., Niemoeller, O.M., Artunc, F., Portero-Otin, M., Haik Jr., G., Thornalley, P.J., Schleicher, E., Wieder, T., Lang, F., 2006. Stimulation of suicidal erythrocyte death by methylglyoxal. Cell. Physiol. Biochem. 18, 223-232.
66. Pandolfi, A., Di Pietro, N., Sirolli, V., Giardinelli, A., Di Silvestre, S., Amoroso, L., Di Tomo, P., Capani, F., Consoli, A., Bonomini, M., 2007. Mechanisms of uremic erythrocyte-induced adhesion of human monocytes to cultured endothelial cells. J. Cell. Physiol. 213, 699-709.
67. Qadri, S.M., Bauer, J., Zelenak, C., Mahmud, H., Kucherenko, Y., Lee, S.H., Ferlinz, K., Lang, F., 2011a. Sphingosine but not sphingosine-1-phosphate stimulates suicidal erythrocyte death. Cell. Physiol. Biochem. 28, 339-346.
68. Qadri, S.M., Kucherenko, Y., Lang, F., 2011b. Beauvericin induced erythrocyte cell membrane scrambling. Toxicology 283, 24-31.
69. Qadri, S.M., Kucherenko, Y., Zelenak, C., Jilani, K., Lang, E., Lang, F., 2011c. Dicoumarol activates Ca-permeable cation channels triggering erythrocyte cell membrane scrambling. Cell. Physiol. Biochem. 28, 857-864.
70. Qadri, S.M., Mahmud, H., Lang, E., Gu, S., Bobbala, D., Zelenak, C., Jilani, K., Siegfried, A., Foller, M., Lang, F., 2012. Enhanced suicidal erythrocyte death in mice carrying a loss-of-function mutation of the adenomatous polyposis coli gene. J. Cell. Mol. Med. 16, 1085-1093.
71. Setia, M.S., Shinde, S.S., Jerajani, H.R., Boivin, J.F., 2011. Is there a role for rifampicin, ofloxacin and minocycline (ROM) therapy in the treatment of leprosy? Systematic review and meta-analysis. Trop. Med. Int. Health 16, 1541-1551.
72. Siraskar, B., Ballal, A., Bobbala, D., Foller, M., Lang, F., 2010. Effect of amphotericin B on parasitemia and survival of Plasmodium berghei-infected mice. Cell. Physiol. Biochem. 26, 347-354.
73. 2+ entry into and subsequent suicidal death of erythrocytes. Toxicology 244, 271-279.
74. 2+-mediated intercellular adhesion. Cell Calcium 50, 54-61.
75. Thee, S., Seddon, J.A., Donald, P.R., Seifart, H.I., Werely, C.J., Hesseling, A.C., Rosenkranz, B., Roll, S., Magdorf, K., Schaaf, H.S., 2011. Pharmacokinetics of isoniazid rifampin, and pyrazinamide in children younger than two years of age with tuberculosis: evidence for implementation of revised World Health Organization recommendations. Antimicrob. Agents Chemother. 55, 5560-5567.
76. Tong, M., Neusner, A., Longato, L., Lawton, M., Wands, J.R., de la Monte, S.M., 2009. Nitrosamine exposure causes insulin resistance diseases: relevance to type 2 diabetes mellitus, non-alcoholic steatohepatitis, and Alzheimer's disease. J. Alzheimers Dis. 17, 827-844.
77. Tupin, A., Gualtieri, M., Roquet-Baneres, F., Morichaud, Z., Brodolin, K., Leonetti, J.P., 2010. Resistance to rifampicin: at the crossroads between ecological, genomic and medical concerns. Int. J. Antimicrob. Agents 35, 519-523.
78. van Ingen, J., Aarnoutse, R.E., Donald, P.R., Diacon, A.H., Dawson, R., Plemper, v.B., Gillespie, S.H., Boeree, M.J. 2011. Why do we use 600 mg of rifampicin in tuberculosis treatment? Clin. Infect. Dis. 52, e194-e199.
79. Walter, S., Fassbender, K., 2010. Spingolipids in multiple sclerosis. Cell. Physiol. Biochem. 26, 49-56.
80. Wiggins, K.J., Galanos, J.W., Hill, P.A., Scott, K.V., Langham, R.G., 2007. Rifampicinassociated segmental necrotizing glomerulonephritis in staphylococcal endocarditis. J. Nephrol. 20, 489-494.
81. Wood, B.L., Gibson, D.F., Tait, J.F., 1996. Increased erythrocyte phosphatidylserine exposure in sickle cell disease: flow-cytometric measurement and clinical associations. Blood 88, 1873-1880.
82. Zappulla, D., 2008. Environmental stress, erythrocyte dysfunctions, inflammation, and the metabolic syndrome: adaptations to CO2 increases? J. Cardiometab. Syndr. 3, 30-34.
83. Zelenak, C., Eberhard, M., Jilani, K., Qadri, S.M., Macek, B., Lang, F., 2012. Protein kinase CK1alpha regulates erythrocyte survival. Cell. Physiol. Biochem. 29, 171-180.
84. Zhao, H., Przybylska, M., Wu, I.H., Zhang, J., Siegel, C., Komarnitsky, S., Yew, N.S., Cheng, S.H., 2007. Inhibiting glycosphingolipid synthesis improves glycemic control and insulin sensitivity in animal models of type 2 diabetes. Diabetes 56, 1210-1218.
85. Zigmond, E., Zangen, S.W., Pappo, O., Sklair-Levy, M., Lalazar, G., Zolotaryova, L., Raz, I., Ilan, Y., 2009. Beta-glycosphingolipids improve glucose intolerance and hepatic steatosis of the Cohen diabetic rat. Am. J. Physiol. Endocrinol. Metab. 296, E72-E78.
86. Zwaal, R.F., Comfurius, P., Bevers, E.M., 2005. Surface exposure of phosphatidylserine in pathological cells. Cell Mol. Life Sci. 62, 971-988.