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Mycotoxin-Induced Elevation of Free Sphingoid Bases in Precision-Cut Rat Liver Slices: Specificity of the Response and Structure-Activity Relationships1

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Mycotoxin-Induced Elevation of Free Sphingoid Bases in Precision-Cut Rat Liver Slices: Specificity of the Response and Structure-Activity Relationships1 TOXICOLOGY AND APPLIED PHARMACOLOGY 147.63-70 (1997) 7878 ARTICLE NO. T0978272 Mycotoxin-Induced Elevation of Free Sphingoid Bases in Precision-Cut Rat Liver Slices: Specificity of the Response and Structure-Activity Relationships1 William P. Norred.*·~ Ronald D. Plattner.t Mary Ann Dombrink-Kurtzman.t Filmore 1. Meredith.* and Ronald T. Riley* *Toxicalogy and M.\·c(}/oxin Research Vnit. Richard B. Russell Agricullural Research Center. ARSIVSDA. P.O. Box 5677. Athens. Georgia 30604·5677; and tMycolOxin Research Vnil. National Cenrer for AgriculTUral Vtili:ation Research. ARSIVSDA. 18/5 N. Vnil'ersity Sneel. Peoria. lllinois 61604 Received February 24. 1997: accepted July 24. 1997 Many mycotoxins are known to cause animal diseases. can Effects of Fumonisin Analogs and Structurally Unrelated Myco­ also be phytotoxic, and are suspected causative agents of toxins on Elevation of Free Sphingoid Bases in Precision-Cut Rat some human illnesses, including cancer (Rheeder et al.. Liver Slices:)~p-ecificity of the Response and Structure Activity 1992). Fumonisins, produced by several Fusarium species. Relationships. Norred, W. P., Plattner, R. D., Meredith, F. I. and Riley, R. T. (1997). Taxieal. Appl. Pharmaeal147, 63-70. are frequent contaminants of com and corn-based feed and food (Nelson et al., 1991; Ross et al.. 1991: Sydenham et Fumonisin BI (FBI) is the predominant member of a family of toxic metabolites produced by several species of Fusarium and is al.. 1991). Fumonisin B I (FBI)' the most prevalent of several commonly found on com. FBI is a potent competitive inhibitor of naturally occurring analogs, has been shown to cause the ceramide synthase. which catalyzes the conversion of sphinganine fatal livestock diseases, equine leucoencephalomalacia and sphingosine to ceramide. The resultant accumulation of free (Marasas et al.. 1988), and porcine pulmonary edema (Har­ sphingoid bases and the disruption of sphingolipid metabolism is rison et al.. 1990). FB I has been studied in purified form in believed to be the mechanism of toxicity of the fumonisins. The laboratory rats and mice and shown to cause hepato- and objectives of this study were to determine the relative potency of nephrotoxicity (Voss et aI., 1993, 1994) and, in one study, analogs of FBI to inhibit ceramide synthase and to determine hepatocellular carcinoma (Gelderblom et aI., 1991). Several whether the inhibition is specific to mycotoxins with fumonisin­ reviews on the occurrence, toxicity, and chemistry offumon­ like structures. Fumonisins B • B • B.I , B , C , and TA toxin (a I 1 4 4 isins are available (Norred, 1993: Powell and Plattner. 1995: structurally similar mycotoxin produced by the tomato pathogen. Dutton. 1996). High rates of human esophageal cancer in Alternaria altemata f. sp. lyeapersiel) were approximately equipo­ region~ of China. South Africa. and Italy where corn is con­ tent inhibitors. Hydrolyzed fumonisins BI • B1 • and B.,. which lack the tricarballylic side chains, were only 30-409c as potent as the sumed as a staple are correlated with the presence of fumoni­ parent toxins. N-acetylated FBI (FA I) did not block ceramide syn­ sins or fumonisin-producing fungi in corn and corn-based thase. suggesting that FA I is nontoxic. Inhibition of ceramide syn­ food (Chu and Li. 1994; Sydenham et al., 1990; Logrieco thase by fumonisin analogs did not appear to be related to the ('t al.. 1995). Only recently discovered (Gelderblom et al., Iipophilicity of the compounds, as determined by computer estima­ 1988). the fumonisins are an important emerging class of tion of log P values. The ability of relatively high (10 and 100 fJ M) mycolOxins that are ofgreat concem to corn producers, com­ doses of other mycotoxins that bear no structural similarity to modity groups. and industries and to regulatory agencies fumonisins, including aflatoxin B , cyclopiazonic acid. beauveri­ 1 responsible for food safety and grain quality. cin, T-2 toxin. sterigmatocystin,luteoskyrin. verrucarin A, scirpen­ triol, and zearalenone, to block ceramide synthase was also deter­ Fumonisin B I was the first agent discovered that inhibits mined. All of the toxins tested were negative in the bioassay with ceramide synthase (sphinganine (Sa) and sphingosine (So) the exception offumonisins. indicating that disruption of sphingo­ N-acyltransferase). which catalyzes the conversion of Sa (or lipid metabolism is a specific cytotoxic response. So) to <.:eramide (Wang et aI., 1991). The fumonisins are structurally similar to these sphingoid bases, differing mainly by the presen<.:e of tricarballylic acid side chains (Fig. I), Toxic fungal metabolites. or mycotoxins. are diverse in and it was for this reason that fumonisins B and B~ were structure. biological activity' and environmental prevalen<.:e. I tested for their ability to alter the conversion of serine into sphingolipids in an in vitro assay (Wang et al., 1991). Other I Presented in pan at the 35th Annual Meeting of the Soclet~ of Tmucol· ogy. Anaheim. CA. agents thai interfere with sphingolipid metabolism have e To whom correspondence should be addressed. sin<.:c heen discovered. including compounds such as AAL 0041-008XJ97 64 NORRED ET AL. OH sphingolipid metabolism are alteration of signal transduction pathways through repression ofprotein kinase C and stimula­ H tion of cyclic AMP response elements (Huang et al.. 1995) .. Sphinganine and inhibition of protein serine/threonine phosphatases (Fu­ kuda et al.. 1996). Thus. whereas the principal subcellular effect of fumonisins appears to be simple, i.e.. inhibition of ceramide synthase, the ramifications of this action for ad­ verse biological consequences may be complex and far reaching. Disruption of sphingolipid metabolism could therefore lead to long-term toxicity and. possibly. carcinoge­ nicity. but not necessarily acute toxicity. Indeed. fumonisins are not particularly acutely toxic either in vivo or in \'itro R1 R2 R3 R4 RS (Norred and Voss, 1994). Several reviews discussing the FB1 H OH OH TCA TCA role of sphingolipids and the disruption of their metabolism in the toxicity and carcinogenicity of fumonisins are avail­ FB2 H OH H TCA TCA able (Merrill et al.. 1995a,b. 1996a: Riley et al.. 1996). FB3 HH OH TCA TCA A number of structural analogs of FBI have now been H H H TCA TCA FB4 discovered (Powell and Plattner. 1995). and it is known that FA1 COCH3 OH OH TCA TCA several of these, including fumonisins BI, B2 , B3 and hy­ HFB1 H OH OH H H drolyzed FB I (Fig. 1). share the ability to inhibit ceramide HFB2 - -- - H OH H HH synthase (Wang et al.. 1991; Merrill et al.. 1993). The pur­ HFB3 H H OH HH pose of the present study was twofold. First, we wanted to determine the relative capability of structural analogs of fumonisin B I to induce elevated levels of free sphinganine when incubated with precision-cut rat liver slices, a bioassay system which we previously reported to be a sensitive indica­ tor of FBI activity (Norred et al.. 1996). Second, we wanted to determine whether the inhibition of ceramide synthase is specific to fumonisins or fumonisin-like compounds or R1 R2 R3 R4 RS whether elevated sphinganine levels could be a generalized IFC4 H H TCA TCA CH2CH3 response of cells to toxic insult by other, structurally unre­ ITA TOXIN OH OH TCA HH lated toxins. FIG. I. Structures of sphinganine and fumonisin analogs tested. MATERIALS AND METHODS Rats and li~'er slices. Tissues were obtained from healthy male. un­ toxin (TA toxin: Merrill et al.. 1993) and australifungin fasted Sprague-Dawley rats (200-300 g; Harlan Industries. Indianapolis, (Mandala et al.. 1995). Normally. ceramide is converted to IN) maintained in stainless-steel cages mounted in racks equipped with complex sphingolipids. including sphingomyelin and glyco­ automatic drinking water and excreta flushing in temperature- and humidity­ sphingolipids (Fig. 2). The inhibition of ceramide synthase controlled animal rooms. Feed (RMH 3000 certified. Agway. Waverly. NY) caused by FBI disrupts sphingolipid metabolism. causing was analyzed as previously described to ensure fumonisin content was below 0.5 ppm (Chamberlain eT of.. 1993). Individual rats were killed during elevated levels of free intracellular Sa and So. increased the morning hours (6:30-7:30 AM) by inhalation of carbon dioxide. and amounts of sphingoid base degradation products such as the liver was quickly removed and placed in ice-cold Sack's buffer (5.5 sphinganine-l-phosphate. depletion of complex sphingoli­ mM KH~PO •• 14.3 mM NaHCO,. lOA mM K~HPO.·3H~O, 6 mM KHCO,. pids. and increased biosynthesis of phosphatidylethanolam­ 206 mM mannitol. and 3.7 mM MgCI~' 6H~O). Cores of liver (8 mm diame­ ine (Smith and Merrill. 1995: Yoo et al.. 1996). Other effects ter) were cut with minimum pressure using a stainless-steel borer filled on a specially designed drill press (Alabama Research and Development. of FB I which have been noted and which likely are end Mumford. All. The cores were placed in ice-cold Sack's buffer and trans­ results of disrupted sphingolipid metabolism, include inhibi­ ferred one at a time to a Krumdieck tissue slicer (Alabama Research and tion of cell proliferation and increased cell death (Yoo et Development). Slices (250 pm) were cut according to the manufacturer's al.. 1996: Wang et al., 1996: Tolleson et al.. 1996). reduction instructions. The slices were transferred to Teflon/titanium mesh rollers of the barrier function of endothelial cells thus allowing (Vitron. Inc.. Tucson. AZ: two slices/roller). and then the rollers were placed in 20-ml glass scintillation vials and incubated in Waymouth's me­ "leakage" of albumin across membranes (Ramasamy et al.. dium (Gibco. Grand Island. NY) with various doses of test agents dissolved 1995). and stimulation of DNA synthesis (Schroeder et al.. in 10 pi of solvent (distilled water or dimethyl sulfoxide) for' 48 hr as 1994). Other effects which could be related to disruption of previously described (Norred eT of.
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