Endogenous Fructose Production and Metabolism Drive Metabolic Dysregulation and Liver Disease in Mice with Hereditary Fructose Intolerance
Abstract
:1. Introduction
2. Materials and Methods
3. Results
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Simons, N.; Debray, F.G.; Schaper, N.C.; Feskens, E.J.M.; Hollak, C.E.M.; Bons, J.A.P.; Bierau, J.; Houben, A.; Schalkwijk, C.G.; Stehouwer, C.D.A.; et al. Kidney and vascular function in adult patients with hereditary fructose intolerance. Mol. Genet. Metab. Rep. 2020, 23, 100600. [Google Scholar] [CrossRef] [PubMed]
- Pinheiro, F.C.; Sperb-Ludwig, F.; Schwartz, I.V.D. Epidemiological aspects of hereditary fructose intolerance: A database study. Hum. Mutat. 2021, 42, 1548–1566. [Google Scholar] [CrossRef] [PubMed]
- Lanaspa, M.A.; Andres-Hernando, A.; Orlicky, D.J.; Cicerchi, C.; Jang, C.; Li, N.; Milagres, T.; Kuwabara, M.; Wempe, M.F.; Rabinowitz, J.D.; et al. Ketohexokinase C blockade ameliorates fructose-induced metabolic dysfunction in fructose-sensitive mice. J. Clin. Investig. 2018, 128, 2226–2238. [Google Scholar] [CrossRef]
- Di Dato, F.; Spadarella, S.; Puoti, M.G.; Caprio, M.G.; Pagliardini, S.; Zuppaldi, C.; Vallone, G.; Fecarotta, S.; Esposito, G.; Iorio, R.; et al. Daily Fructose Traces Intake and Liver Injury in Children with Hereditary Fructose Intolerance. Nutrients 2019, 11, 2397. [Google Scholar] [CrossRef] [PubMed]
- Lanaspa, M.A.; Ishimoto, T.; Cicerchi, C.; Tamura, Y.; Roncal-Jimenez, C.A.; Chen, W.; Tanabe, K.; Andres-Hernando, A.; Orlicky, D.J.; Finol, E.; et al. Endogenous fructose production and fructokinase activation mediate renal injury in diabetic nephropathy. J. Am. Soc. Nephrol. 2014, 25, 2526–2538. [Google Scholar] [CrossRef]
- Lanaspa, M.A.; Ishimoto, T.; Li, N.; Cicerchi, C.; Orlicky, D.J.; Ruzycki, P.; Rivard, C.; Inaba, S.; Roncal-Jimenez, C.A.; Bales, E.S.; et al. Endogenous fructose production and metabolism in the liver contributes to the development of metabolic syndrome. Nat. Commun. 2013, 4, 2434. [Google Scholar] [CrossRef]
- Lanaspa, M.A.; Kuwabara, M.; Andres-Hernando, A.; Li, N.; Cicerchi, C.; Jensen, T.; Orlicky, D.J.; Roncal-Jimenez, C.A.; Ishimoto, T.; Nakagawa, T.; et al. High salt intake causes leptin resistance and obesity in mice by stimulating endogenous fructose production and metabolism. Proc. Natl. Acad. Sci. USA 2018, 115, 3138–3143. [Google Scholar] [CrossRef]
- Sanchez-Lozada, L.G.; Andres-Hernando, A.; Garcia-Arroyo, F.E.; Cicerchi, C.; Li, N.; Kuwabara, M.; Roncal-Jimenez, C.A.; Johnson, R.J.; Lanaspa, M.A. Uric acid activates aldose reductase and the polyol pathway for endogenous fructose and fat production causing development of fatty liver in rats. J. Biol. Chem. 2019, 294, 4272–4281. [Google Scholar] [CrossRef]
- Wang, M.; Chen, W.Y.; Zhang, J.; Gobejishvili, L.; Barve, S.S.; McClain, C.J.; Joshi-Barve, S. Elevated fructose and uric acid via aldose reductase contribute to experimental and human alcoholic liver disease. Hepatology 2020, 72, 1617–1637. [Google Scholar] [CrossRef]
- Oppelt, S.A.; Sennott, E.M.; Tolan, D.R. Aldolase-B knockout in mice phenocopies hereditary fructose intolerance in humans. Mol. Genet. Metab. 2015, 114, 445–450. [Google Scholar] [CrossRef]
- Diggle, C.P.; Shires, M.; McRae, C.; Crellin, D.; Fisher, J.; Carr, I.M.; Markham, A.F.; Hayward, B.E.; Asipu, A.; Bonthron, D.T. Both isoforms of ketohexokinase are dispensable for normal growth and development. Physiol. Genom. 2010, 42A, 235–243. [Google Scholar] [CrossRef]
- Brunt, E.M.; Janney, C.G.; Di Bisceglie, A.M.; Neuschwander-Tetri, B.A.; Bacon, B.R. Nonalcoholic steatohepatitis: A proposal for grading and staging the histological lesions. Am. J. Gastroenterol. 1999, 94, 2467–2474. [Google Scholar] [CrossRef] [PubMed]
- Atkinson, D.E.; Walton, G.M. Adenosine triphosphate conservation in metabolic regulation. Rat liver citrate cleavage enzyme. J. Biol. Chem. 1967, 242, 3239–3241. [Google Scholar] [CrossRef]
- De la Fuente, I.M.; Cortes, J.M.; Valero, E.; Desroches, M.; Rodrigues, S.; Malaina, I.; Martinez, L. On the dynamics of the adenylate energy system: Homeorhesis vs homeostasis. PLoS ONE 2014, 9, e108676. [Google Scholar] [CrossRef]
- Petrash, J.M.; Shieh, B.; Ammar, D.A.; Pedler, M.G.; Orlicky, D.J. Diabetes-Independent Retinal Phenotypes in an Aldose Reductase Transgenic Mouse Model. Metabolites 2021, 11, 450. [Google Scholar] [CrossRef] [PubMed]
- Obrosova, I.G.; Fathallah, L. Evaluation of an aldose reductase inhibitor on lens metabolism, ATPases and antioxidative defense in streptozotocin-diabetic rats: An intervention study. Diabetologia 2000, 43, 1048–1055. [Google Scholar] [CrossRef]
- Morris, R.C., Jr. An experimental renal acidification defect in patients with hereditary fructose intolerance. II. Its distinction from classic renal tubular acidosis; its resemblance to the renal acidification defect associated with the Fanconi syndrome of children with cystinosis. J. Clin. Investig. 1968, 47, 1648–1663. [Google Scholar] [CrossRef]
- Steiner, G.; Wilson, D.; Vranic, M. Studies of glucose turnover and renal function in an unusual case of hereditary fructose intolerance. Am. J. Med. 1977, 62, 150–158. [Google Scholar] [CrossRef]
- Roschlau, G. The histological findings of tubular insufficiency in galactosemia, hereditary fructose intolerance, and oculocerebro-renal syndrome (Lowe-syndrome) (author’s transl). Zentralblatt Allg. Pathol. 1973, 117, 488–496. [Google Scholar]
- Mass, R.E.; Smith, W.R.; Walsh, J.R. The association of hereditary fructose intolerance and renal tubular acidosis. Am. J. Med. Sci. 1966, 251, 516–523. [Google Scholar] [CrossRef]
- Higgins, R.B.; Varney, J.K. Dissolution of renal calculi in a case of hereditary fructose intolerance and renal tubular acidosis. J. Urol. 1966, 95, 291–296. [Google Scholar] [CrossRef]
- Srikanth, K.K.; Orrick, J.A. Biochemistry, Polyol Or Sorbitol Pathways. In Disclosure: Josephine Orrick Declares No Relevant Financial Relationships with Ineligible Companies; StatPearls: Treasure Island, FL, USA, 2023. [Google Scholar]
- Yan, L.J. Redox imbalance stress in diabetes mellitus: Role of the polyol pathway. Anim. Model Exp. Med. 2018, 1, 7–13. [Google Scholar] [CrossRef]
- Lin, L.R.; Carper, D.; Yokoyama, T.; Reddy, V.N. The effect of hypertonicity on aldose reductase, alpha B-crystallin, and organic osmolytes in the retinal pigment epithelium. Investig. Ophthalmol. Vis. Sci. 1993, 34, 2352–2359. [Google Scholar]
- Tammali, R.; Saxena, A.; Srivastava, S.K.; Ramana, K.V. Aldose reductase inhibition prevents hypoxia-induced increase in hypoxia-inducible factor-1alpha (HIF-1alpha) and vascular endothelial growth factor (VEGF) by regulating 26 S proteasome-mediated protein degradation in human colon cancer cells. J. Biol. Chem. 2011, 286, 24089–24100. [Google Scholar] [CrossRef] [PubMed]
- Hwang, Y.C.; Sato, S.; Tsai, J.Y.; Yan, S.; Bakr, S.; Zhang, H.; Oates, P.J.; Ramasamy, R. Aldose reductase activation is a key component of myocardial response to ischemia. FASEB J. 2002, 16, 243–245. [Google Scholar] [CrossRef] [PubMed]
- Andres-Hernando, A.; Li, N.; Cicerchi, C.; Inaba, S.; Chen, W.; Roncal-Jimenez, C.; Le, M.T.; Wempe, M.F.; Milagres, T.; Ishimoto, T.; et al. Protective role of fructokinase blockade in the pathogenesis of acute kidney injury in mice. Nat. Commun. 2017, 8, 14181. [Google Scholar] [CrossRef] [PubMed]
- Thomas, S.A.; Curay, C.M.; Kiyatkin, E.A. Effects of alcohol on brain oxygenation and brain hypoxia induced by intravenous heroin. Neuropharmacology 2021, 197, 108713. [Google Scholar] [CrossRef]
- Nettles, J.L.; Olson, R.N. Effects of alcohol on hypoxia. JAMA 1965, 194, 1193–1194. [Google Scholar] [CrossRef] [PubMed]
- Cox, T.M. Fructose intolerance: Diet and inheritance. Proc. Nutr. Soc. 1991, 50, 305–309. [Google Scholar] [CrossRef] [PubMed]
- Gaughan, S.; Ayres, L.; Baker, P.R., II. Hereditary Fructose Intolerance; Adam, M.P., Mirzaa, G.M., Pagon, R.A., Wallace, S.E., Bean, L.J.H., Gripp, K.W., Amemiya, A., Eds.; GeneReviews((R)): Seattle, WA, USA, 1993. [Google Scholar]
- Andres-Hernando, A.; Orlicky, D.J.; Kuwabara, M.; Ishimoto, T.; Nakagawa, T.; Johnson, R.J.; Lanaspa, M.A. Deletion of Fructokinase in the Liver or in the Intestine Reveals Differential Effects on Sugar-Induced Metabolic Dysfunction. Cell Metab. 2020, 32, 117–127.e113. [Google Scholar] [CrossRef]
- Jang, C.; Wada, S.; Yang, S.; Gosis, B.; Zeng, X.; Zhang, Z.; Shen, Y.; Lee, G.; Arany, Z.; Rabinowitz, J.D. The small intestine shields the liver from fructose-induced steatosis. Nat. Metab. 2020, 2, 586–593. [Google Scholar] [CrossRef] [PubMed]
- Cho, Y.E.; Kim, D.K.; Seo, W.; Gao, B.; Yoo, S.H.; Song, B.J. Fructose Promotes Leaky Gut, Endotoxemia, and Liver Fibrosis Through Ethanol-Inducible Cytochrome P450-2E1-Mediated Oxidative and Nitrative Stress. Hepatology 2021, 73, 2180–2195. [Google Scholar] [CrossRef] [PubMed]
- Cain, A.R.; Ryman, B.E. High liver glycogen in hereditary fructose intolerance. Gut 1971, 12, 929–932. [Google Scholar] [CrossRef] [PubMed]
- Desai, B.N.; Singhal, G.; Watanabe, M.; Stevanovic, D.; Lundasen, T.; Fisher, F.M.; Mather, M.L.; Vardeh, H.G.; Douris, N.; Adams, A.C.; et al. Fibroblast growth factor 21 (FGF21) is robustly induced by ethanol and has a protective role in ethanol associated liver injury. Mol. Metab. 2017, 6, 1395–1406. [Google Scholar] [CrossRef]
- Flippo, K.H.; Trammell, S.A.J.; Gillum, M.P.; Aklan, I.; Perez, M.B.; Yavuz, Y.; Smith, N.K.; Jensen-Cody, S.O.; Zhou, B.; Claflin, K.E.; et al. FGF21 suppresses alcohol consumption through an amygdalo-striatal circuit. Cell Metab. 2022, 34, 317–328.e316. [Google Scholar] [CrossRef]
- Soberg, S.; Andersen, E.S.; Dalsgaard, N.B.; Jarlhelt, I.; Hansen, N.L.; Hoffmann, N.; Vilsboll, T.; Chenchar, A.; Jensen, M.; Grevengoed, T.J.; et al. FGF21, a liver hormone that inhibits alcohol intake in mice, increases in human circulation after acute alcohol ingestion and sustained binge drinking at Oktoberfest. Mol. Metab. 2018, 11, 96–103. [Google Scholar] [CrossRef]
- Talukdar, S.; Owen, B.M.; Song, P.; Hernandez, G.; Zhang, Y.; Zhou, Y.; Scott, W.T.; Paratala, B.; Turner, T.; Smith, A.; et al. FGF21 Regulates Sweet and Alcohol Preference. Cell Metab. 2016, 23, 344–349. [Google Scholar] [CrossRef]
- Jensen, T.; Abdelmalek, M.F.; Sullivan, S.; Nadeau, K.J.; Green, M.; Roncal, C.; Nakagawa, T.; Kuwabara, M.; Sato, Y.; Kang, D.H.; et al. Fructose and sugar: A major mediator of non-alcoholic fatty liver disease. J. Hepatol. 2018, 68, 1063–1075. [Google Scholar] [CrossRef]
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Andres-Hernando, A.; Orlicky, D.J.; Kuwabara, M.; Cicerchi, C.; Pedler, M.; Petrash, M.J.; Johnson, R.J.; Tolan, D.R.; Lanaspa, M.A. Endogenous Fructose Production and Metabolism Drive Metabolic Dysregulation and Liver Disease in Mice with Hereditary Fructose Intolerance. Nutrients 2023, 15, 4376. https://doi.org/10.3390/nu15204376
Andres-Hernando A, Orlicky DJ, Kuwabara M, Cicerchi C, Pedler M, Petrash MJ, Johnson RJ, Tolan DR, Lanaspa MA. Endogenous Fructose Production and Metabolism Drive Metabolic Dysregulation and Liver Disease in Mice with Hereditary Fructose Intolerance. Nutrients. 2023; 15(20):4376. https://doi.org/10.3390/nu15204376
Chicago/Turabian StyleAndres-Hernando, Ana, David J. Orlicky, Masanari Kuwabara, Christina Cicerchi, Michelle Pedler, Mark J. Petrash, Richard J. Johnson, Dean R. Tolan, and Miguel A. Lanaspa. 2023. "Endogenous Fructose Production and Metabolism Drive Metabolic Dysregulation and Liver Disease in Mice with Hereditary Fructose Intolerance" Nutrients 15, no. 20: 4376. https://doi.org/10.3390/nu15204376
APA StyleAndres-Hernando, A., Orlicky, D. J., Kuwabara, M., Cicerchi, C., Pedler, M., Petrash, M. J., Johnson, R. J., Tolan, D. R., & Lanaspa, M. A. (2023). Endogenous Fructose Production and Metabolism Drive Metabolic Dysregulation and Liver Disease in Mice with Hereditary Fructose Intolerance. Nutrients, 15(20), 4376. https://doi.org/10.3390/nu15204376