Suppression of insulin-like growth factor acid-labile subunit expression-A novel mechanism for deoxynivalenol-induced growth retardation

Toxicological Sciences

Volumn 113, Issue 2, 2009, Pages 412-421

  Amuzie, Chidozie J ^a   Pestka, James J ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

Author keywords

DON induced IGFALS suppression; Growth; Mycotoxin; Trichothecene

Indexed keywords

GROWTH HORMONE; INSULIN LIKE GROWTH FACTOR ACID LABILE SUBUNIT; MESSENGER RNA; SOMATOMEDIN; SOMATOMEDIN C; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG; VOMITOXIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD LEVEL; CONTROLLED STUDY; DIETARY INTAKE; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GROWTH RETARDATION; NONHUMAN; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; STEADY STATE; WEIGHT GAIN;

ANIMALS; CARRIER PROTEINS; GLYCOPROTEINS; GROWTH DISORDERS; GROWTH HORMONE; INSULIN-LIKE GROWTH FACTOR I; LIVER; MICE; RNA, MESSENGER; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRICHOTHECENES; WEIGHT GAIN;

ANIMALIA; MUS;

EID: 75349104616     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp225     Document Type: Article

References (80)

1. Abouzied, M.M., Azcona, J.I., Braselton, W.E., and Pestka, J.J. (1991). Immunochemical assessment of mycotoxins in 1989 grain foods: Evidence for deoxynivalenol (vomitoxin) contamination. Appl. Environ. Microbiol. 57(3), 672-677.
2. Amuzie, C.J., Harkema, J.R., and Pestka, J.J. (2008). Tissue distribution and proinflammatory cytokine induction by the trichothecene deoxynivalenol in the mouse: Comparison of nasal vs. oral exposure. Toxicology 248, 39-44.
3. Amuzie, C.J., Shinozuka, J., and Pestka, J.J. (2009). Induction of suppressors of cytokine signaling (SOCS) by the trichothecene deoxynivalenol in the mouse. Toxicol. Sci. 111, 277-287.
4. Arnold, D.L., Karpinski, K.F., McGuire, P.F., Nera, E.A., Zawidzka, Z.Z., Lok, E., Campbell, J.S., Tryphonas, L., and Scott, P.M. (1986). A shortterm feeding study with deoxynivalenol (vomitoxin) using rats. Fundam. Appl. Toxicol. 6(4), 691-696.
5. Azcona-Olivera, J.I., Ouyang, Y.L., Warner, R.L., Linz, J.E., and Pestka, J.J. (1995). Effects of vomitoxin (deoxynivalenol) and cycloheximide on IL-2, 4, 5 and 6 secretion and mRNA levels in murine CD4+ cells. Food Chem. Toxicol. 33(6), 433-441.
6. Bae, H.K., and Pestka, J.J. (2008). Deoxynivalenol induces p38 interaction with the ribosome in monocytes and macrophages. Toxicol. Sci. 105, 59-66.
7. Baker, J., Liu, J.P., Robertson, E.J., and Efstratiadis, A. (1993). Role of insulin-like growth-factors in embryonic and postnatal-growth. Cell 75, 73-82.
8. Bang, P., Brandt, J., Degerblad, M., Enberg, G., Kaijser, L., Thoren, M., and Hall, K. (1990). Exercise-induced changes in insulin-like growth factors and their low molecular weight binding protein in healthy subjects and patients with growth hormone deficiency. Eur. J. Clin. Invest. 20(3), 285-292.
9. Barreca, A., Ketelslegers, J.M., Arvigo, M., Minuto, F., and Thissen, J.P. (1998). Decreased acid-labile subunit (ALS) levels by endotoxin in vivo and by interleukin-1beta in vitro. Growth Horm. IGF. Res. 8(3), 217-223.
10. Bazan, J.F. (1989). A novel family of growth factor receptors: A common binding domain in the growth hormone, prolactin, erythropoietin and IL-6 receptors, and the p75 IL-2 receptor beta-chain. Biochem. Biophys. Res. Commun. 164(2), 788-795.
11. Bergsjo, B., Matre, T., and Nafstad, I. (1992). Effects of diets with graded levels of deoxynivalenol on performance in growing pigs. Zentralbl. Veterinarmed. A 39(10), 752-758.
12. Boisclair, Y.R., Wang, J., Shi, J., Hurst, K.R., and Ooi, G.T. (2000). Role of the suppressor of cytokine signaling-3 in mediating the inhibitory effects of interleukin-1beta on the growth hormone-dependent transcription of the acidlabile subunit gene in liver cells. J. Biol. Chem. 275(6), 3841-3847.
13. Canady, R.A., Coker, R.D., Rgan, S.K., Krska, R., Kuiper-Goodman, T., Olsen, M., Pestka, J.J., Resnik, S., and Schlatter, J. (2002). Deoxynivalenol. In Safety Evaluation of Certain Mycotoxins in Food. Fifty-Sixth Report of the Joint FAO/WHO Expert Committee on Food Additives 2001, International Programme on Chemical Safety, World Health Organization, Geneva, pp. 420-555.
14. Chen, Y., Sun, D., Krishnamurthy, V.M., and Rabkin, R. (2007). Endotoxin attenuates growth hormone-induced hepatic insulin-like growth factor I expression by inhibiting JAK2/STAT5 signal transduction and STAT5b DNA binding. Am. J. Physiol. Endocrinol. Metab. 292(6), E1856-E1862.
15. Chung, Y.J., Zhou, H.R., and Pestka, J.J. (2003). Transcriptional and posttranscriptional roles for p38 mitogen-activated protein kinase in upregulation of TNF-alpha expression by deoxynivalenol (vomitoxin). Toxicol. Appl. Pharmacol. 193(2), 188-201.
16. Clifford, L.J., Jia, Q., and Pestka, J.J. (2003). An improved method for the purification of the trichothecene deoxynivalenol (vomitoxin) from Fusarium graminearum culture. J. Agric. Food Chem. 51(2), 521-523.
17. De Benedetti, F., Alonzi, T., Moretta, A., Lazzaro, D., Costa, P., Poli, V., Martini, A., Ciliberto, G., and Fattori, E. (1997). Interleukin 6 causes growth impairment in transgenic mice through a decrease in insulin-like growth factor-I. A model for stunted growth in children with chronic inflammation. J. Clin. Invest. 99(4), 643-650.
18. Domene, H.M., Bengolea, S.V., Martinez, A.S., Ropelato, M.G., Pennisi, P., Scaglia, P., Heinrich, J.J., and Jasper, H.G. (2004). Deficiency of the circulating insulin-like growth factor system associated with inactivation of the acid-labile subunit gene. N. Engl. J. Med. 350(6), 570-577.
19. Dong, W., Azcona-Olivera, J.I., Brooks, K.H., Linz, J.E., and Pestka, J.J. (1994). Elevated gene expression and production of interleukins 2, 4, 5, and 6 during exposure to vomitoxin (deoxynivalenol) and cycloheximide in the EL-4 thymoma. Toxicol. Appl. Pharmacol. 127(2), 282-290.
20. Eleswarapu, S., Gu, Z., and Jiang, H. (2008). Growth hormone regulation of insulin-like growth factor-I gene expression may be mediated by multiple distal signal transducer and activator of transcription 5 binding sites. Endocrinology 149(5), 2230-2240.
21. Endo, T.A., Masuhara, M., Yokouchi, M., Suzuki, R., Sakamoto, H., Mitsui, K., Matsumoto, A., Tanimura, S., Ohtsubo, M., Misawa, H., et al. (1997). A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387(6636), 921-924.
22. Fan, J., Char, D., Kolasa, A.J., Pan, W., Maitra, S.R., Patlak, C.S., Spolarics, Z., Gelato, M.C., and Lang, C.H. (1995). Alterations in hepatic production and peripheral clearance of IGF-I after endotoxin. Am. J. Physiol. 269(1 Pt 1), E33-E42.
23. Febbraio, M.A., and Pedersen, B.K. (2005). Contraction-induced myokine production and release: Is skeletal muscle an endocrine organ? Exerc. Sport Sci. Rev. 33(3), 114-119.
24. Fitzpatrick, D.W., Boyd, K.E., and Watts, B.M. (1988). Comparison of the trichothecenes deoxynivalenol and T-2 toxin for their effects on brain biogenic monoamines in the rat. Toxicol. Lett. 40(3), 241-245.
25. Forsell, J.H., Witt, M.F., Tai, J.H., Jensen, R., and Pestka, J.J. (1986). Effects of 8-week exposure of the B6C3F1 mouse to dietary deoxynivalenol (vomitoxin) and zearalenone. Food Chem. Toxicol. 24(3), 213-219.
26. Garcia, M.C., Wernstedt, I., Berndtsson, A., Enge, M., Bell, M., Hultgren, O., Horn, M., Ahren, B., Enerback, S., Ohlsson, C., et al. (2006). Mature-onset obesity in interleukin-1 receptor I knockout mice. Diabetes 55(5), 1205-1213.
27. Glund, S., and Krook, A. (2008). Role of interleukin-6 signalling in glucose and lipid metabolism. Acta Physiol. 192, 37-48.
28. Grove, J.F. (2007). The trichothecenes and their biosynthesis. Fortschr. Chem. Org. Naturst. 88, 63-130.
29. Guler, H.P., Zapf, J., Schmid, C., and Froesch, E.R. (1989). Insulin-like growth factors I and II in healthy man. Estimations of half-lives and production rates. Acta Endocrinol. 121(6), 753-758.
30. He, P., Young, L.G., and Forsberg, C. (1992). Microbial transformation of deoxynivalenol (vomitoxin). Appl. Environ. Microbiol. 58(12), 3857-3863.
31. Heath, K.E., Argente, J., Barrios, V., Pozo, J., az-Gonzalez, F., Martos-Moreno, G.A., Caimari, M., Gracia, R., and Campos-Barros, A. (2008). Primary acid-labile subunit deficiency due to recessive IGFALS mutations results in postnatal growth deficit associated with low circulating insulin growth factor (IGF)-I, IGF binding protein-3 levels, and hyperinsulinemia. J. Clin. Endocrinol. Metab. 93(5), 1616-1624.
32. Hwang, D.L., Lee, P.D., and Cohen, P. (2008). Quantitative ontogeny of murine insulin-like growth factor (IGF)-I, IGF-binding protein-3 and the IGF-related acid-labile subunit. Growth Horm. IGF. Res. 18, 65-74.
33. Islam, Z., Gray, J.S., and Pestka, J.J. (2006). p38 Mitogen-activated protein kinase mediates IL-8 induction by the ribotoxin deoxynivalenol in human monocytes. Toxicol. Appl. Pharmacol. 213(3), 235-244.
34. Islam, Z., and Pestka, J.J. (2006). LPS priming potentiates and prolongs proinflammatory cytokine response to the trichothecene deoxynivalenol in the mouse. Toxicol. Appl. Pharmacol. 211, 53-63.
35. Iverson, F., Armstrong, C., Nera, E., Truelove, J., Fernie, S., Scott, P., Stapley, R., Hayward, S., and Gunner, S. (1995). Chronic feeding study of deoxynivalenol in B6C3F1 male and female mice. Teratog. Carcinog. Mutagen. 15(6), 283-306.
36. Lang, C.H., Hong-Brown, L., and Frost, R.A. (2005). Cytokine inhibition of JAK-STAT signaling: A new mechanism of growth hormone resistance. Pediatr. Nephrol. 20(3), 306-312.
37. Leroith, D., and Yakar, S. (2007). Mechanisms of disease: Metabolic effects of growth hormone and insulin-like growth factor 1. Nat. Clin. Pract. Endocrinol. Metab. 3(3), 302-310.
38. Mao, Y., Ling, P.R., Fitzgibbons, T.P., McCowen, K.C., Frick, G.P., Bistrian, B.R., and Smith, R.J. (1999). Endotoxin-induced inhibition of growth hormone receptor signaling in rat liver in vivo. Endocrinology 140(12), 5505-5515.
39. Morrissey, R.E., and Vesonder, R.F. (1985). Effect of deoxynivalenol (vomitoxin) on fertility, pregnancy, and postnatal-development of Sprague-Dawley rats. Appl. Environ. Microbiol. 49(5), 1062-1066.
40. Obol'skii, O. L., Kravchenko, L.V., Avren'eva, L. I., and Tutel'ian, V. A. (1998). [Effect of dietary selenium on the activity of UDP-glucuronosyltransferases and metabolism of mycotoxin deoxynivalenol in rats]. Vopr. Pitan 4, 18-23.
41. Pestka, J.J., Islam, Z., and Amuzie, C.J. (2008). Immunochemical assessment of deoxynivalenol tissue distribution following oral exposure in the mouse. Toxicol. Lett. 178(2), 83-87.
42. Pestka, J.J., Moorman, M.A., and Warner, R.L. (1989). Dysregulation of IgA production and IgA nephropathy induced by the trichothecene vomitoxin. Food Chem. Toxicol. 27(6), 361-368.
43. Pestka, J.J., and Smolinski, A.T. (2005). Deoxynivalenol: Toxicology and potential effects on humans. J. Toxicol. Environ. Health B Crit. Rev. 8, 39-69.
44. Pestka, J.J., and Zhou, H.R. (2002). Effects of tumor necrosis factor type 1 and 2 receptor deficiencies on anorexia, growth and IgA dysregulation in mice exposed to the trichothecene vomitoxin. Food Chem. Toxicol. 40(11), 1623-1631.
45. Pozo, J., Martos-Moreno, G.A., Barrios, V., and Argente, J. (2005). The IGF system in childhood: Physiology and clinical implications. J. Endocrinol. Invest. 28(Suppl. 5), 38-42.
46. Prelusky, D.B. (1993). The effect of low-level deoxynivalenol on neurotransmitter levels measured in pig cerebral spinal fluid. J. Environ. Sci. Health B 28(6), 731-761.
47. Prelusky, D.B. (1994). The effect of deoxynivalenol on serotoninergic neurotransmitter levels in pig blood. J. Environ. Sci. Health B 29(6), 1203-1218.
48. Prelusky, D.B. (1997). Effect of intraperitoneal infusion of deoxynivalenol on feed consumption and weight gain in the pig. Nat. Toxins 5(3), 121-125.
49. Prelusky, D.B., Hartin, K.E., Trenholm, H.L., and Miller, J.D. (1988). Pharmacokinetic fate of 14C-labeled deoxynivalenol in swine. Fundam. Appl. Toxicol. 10(2), 276-286.
50. Prelusky, D.B., Rotter, B.A., Thompson, B.K., and Trenholm, H.L. (1997). Effect of the appetite stimulant cyproheptadine on deoxynivalenol-induced reductions in feed consumption and weight gain in the mouse. J. Environ. Sci. Health B 32(3), 429-448.
51. Probert, L., Akassoglou, K., Alexopoulou, L., Douni, E., Haralambous, S., Hill, S., Kassiotis, G., Kontoyiannis, D., Pasparakis, M., Plows, D., et al. (1996). Dissection of the pathologies induced by transmembrane and wildtype tumor necrosis factor in transgenic mice. J. Leukoc. Biol. 59(4), 518-525.
52. Rotter, B.A., Rotter, R.G., Thompson, B.K., and Trenholm, H.L. (1992). Investigations in the use of mice exposed to mycotoxins as a model for growing pigs. J. Toxicol. Environ. Health 37(2), 329-339.
53. Rotter, B.A., Thompson, B.K., Lessard, M., Trenholm, H.L., and Tryphonas, H. (1994). Influence of low-level exposure to Fusarium mycotoxins on selected immunological and hematological parameters in young swine. Fundam. Appl. Toxicol. 23(1), 117-124.
54. Salmon, W.D., Jr., and Daughaday, W.H. (1957). A hormonally controlled serum factor which stimulates sulfate incorporation by cartilage in vitro. J. Lab Clin. Med. 49(6), 825-836.
55. Scientific Committee on Food (SCF). (2002). Opinion of the Scientific Committee on Food on Fusarium Toxins. Part 6: Group Evaluation of T-2 toxin, HT-2 Toxin, Nivalenol and Deoxynivalenol. European Commission, Brussels, Belgium.
56. Schothorst, R.C., and van Egmond, H.P. (2004). Report from SCOOP task 3.2.10 "collection of occurrence data of Fusarium toxins in food and assessment of dietary intake by the population of EU member states". Subtask: Trichothecenes. Toxicol. Lett. 153, 133-143.
57. Shumate, M.L., Yumet, G., Ahmed, T.A., and Cooney, R.N. (2005). Interleukin-1 inhibits the induction of insulin-like growth factor-I by growth hormone in CWSV-1 hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 289(2), G227-G239.
58. Smolinski, A.T., and Pestka, J.J. (2005). Comparative effects of the herbal constituent parthenolide (Feverfew) on lipopolysaccharide-induced inflammatory gene expression in murine spleen and liver. J. Inflamm. 2, 6.
59. Starr, R., Willson, T.A., Viney, E.M., Murray, L.J.L., Rayner, J.R., Jenkins, B.J., Gonda, T.J., Alexander, W.S., Metcalf, D., Nicola, N.A., et al. (1997). A family of cytokine-inducible inhibitors of signalling. Nature 387(6636), 917-921.
60. Swanson, S.P., Helaszek, C., Buck, W.B., Rood, H.D., Jr., and Haschek, W.M. (1988). The role of intestinal microflora in the metabolism of trichothecene mycotoxins. Food Chem. Toxicol. 26(10), 823-829.
61. Tanaka, T., Hasegawa, A., Yamamoto, S., Lee, U.S., Sugiura, Y., and Ueno, Y. (1988). Worldwide contamination of cereals by the Fusarium mycotoxins nivalenol, deoxynivalenol, and zearalenone. 1. Survey of 19 countries. J. Agric. Food. Chem. 36, 979-983.
62. Thissen, J.P., Davenport, M.L., Pucilowska, J.B., Miles, M.V., and Underwood, L.E. (1992). Increased serum clearance and degradation of 125I-labeled IGF-I in protein-restricted rats. Am. J. Physiol. 262(4 Pt 1), E406-E411.
63. Thissen, J.P., and Verniers, J. (1997). Inhibition by interleukin-1 beta and tumor necrosis factor-alpha of the insulin-like growth factor I messenger ribonucleic acid response to growth hormone in rat hepatocyte primary culture. Endocrinology 138(3), 1078-1084.
64. Trigo-Stockli, D.M. (2002). Effect of processing on deoxynivalenol and other trichothecenes. Adv. Exp. Med. Biol. 504, 181-188.
65. Tritscher, A.M., and Page, S.W. (2004). The risk assessment paradigm and its application for trichothecenes. Toxicol. Lett. 153, 155-163.
66. Trucksess, M.W., Thomas, F., Young, K., Stack, M.E., Fulgueras, W.J., and Page, S.W. (1995). Survey of deoxynivalenol in US 1993 Wheat and Barley Crops byEnzyme-Linked-Immunosorbent-Assay. J.AOACInt. 78(3), 631-636.
67. Turner, P.C., Burley, V.J., Rothwell, J.A., White, K.L., Cade, J.E., and Wild, C.P. (2008). Deoxynivalenol: Rationale for development and application of a urinary biomarker. Food Addit. Contam. 25(7), 864-871.
68. Ueki, I., Giesy, S.L., Harvatine, K.J., Kim, J.W., and Boisclair, Y.R. (2009). The acid-labile subunit is required for full effects of exogenous growth hormone on growth and carbohydrate metabolism. Endocrinology 150(7), 3145-3152.
69. van Egmond, H.P., Schothorst, R.C., and Jonker, M.A. (2007). Regulations relating to mycotoxins in food: Perspectives in a global and European context. Anal. Bioanal. Chem. 389, 147-157.
70. Venken, K., Schuit, F., Van, L.L., Tsukamoto, K., Kopchick, J.J., Coschigano, K., Ohlsson, C., Moverare, S., Boonen, S., Bouillon, R., et al. (2005). Growth without growth hormone receptor: Estradiol is a major growth hormone-independent regulator of hepatic IGF-I synthesis. J. Bone Miner. Res. 20(12), 2138-2149.
71. Wallenius, V., Wallenius, K., Ahren, B., Rudling, M., Carlsten, H., Dickson, S.L., Ohlsson, C., and Jansson, J.O. (2002). Interleukin-6-deficient mice develop mature-onset obesity. Nat. Med. 8, 75-79.
72. Wong, S., Schwartz, R.C., and Pestka, J.J. (2001). Superinduction of TNF-alpha and IL-6 in macrophages by vomitoxin (deoxynivalenol) modulated by mRNA stabilization. Toxicology 161(1-2), 139-149.
73. Wong, S.S., Zhou, H.R., Marin-Martinez, M.L., Brooks, K., and Pestka, J.J. (1998). Modulation of IL-1beta, IL-6 and TNF-alpha secretion and mRNA expression by the trichothecene vomitoxin in the RAW 264.7 murine macrophage cell line. Food Chem. Toxicol. 36(5), 409-419.
74. Yakar, S., Sun, H., Zhao, H., Pennisi, P., Toyoshima, Y., Setser, J., Stannard, B., Scavo, L., and Leroith, D. (2005). Metabolic effects of IGF-I deficiency: Lessons from mouse models. Pediatr. Endocrinol. Rev. 3, 11-19.
75. Yumet, G., Shumate, M.L., Bryant, P., Lin, C.M., Lang, C.H., and Cooney, R.N. (2002). Tumor necrosis factor mediates hepatic growth hormone resistance during sepsis. Am. J. Physiol. Endocrinol. Metab. 283(3), E472-E481.
76. Zhou, H.R., Islam, Z., and Pestka, J.J. (2003a). Rapid, sequential activation of mitogen-activated protein kinases and transcription factors precedes proinflammatory cytokine mRNA expression in spleens of mice exposed to the trichothecene vomitoxin. Toxicol. Sci. 72, 130-142.
77. Zhou, H.R., Jia, Q., and Pestka, J.J. (2005). Ribotoxic stress response to the trichothecene deoxynivalenol in the macrophage involves the SRC family kinase Hck. Toxicol. Sci. 85(2), 916-926.
78. Zhou, H.R., Lau, A.S., and Pestka, J.J. (2003b). Role of double-stranded RNA-activated protein kinase R (PKR) in deoxynivalenol-induced ribotoxic stress response. Toxicol. Sci. 74(2), 335-344.
79. Zhou, H.R., Yan, D., and Pestka, J.J. (1997). Differential cytokine mRNA expression in mice after oral exposure to the trichothecene vomitoxin (deoxynivalenol): Dose response and time course. Toxicol. Appl. Pharmacol. 144(2), 294-305.
80. Zhu, T., Goh, E.L., Graichen, R., Ling, L., and Lobie, P.E. (2001). Signal transduction via the growth hormone receptor. Cell Signal 13(9), 599-616.