High-glucose diets induce mitochondrial dysfunction in Caenorhabditis elegans
Autoři:
Jonathan Alcántar-Fernández aff001; Angélica González-Maciel aff003; Rafael Reynoso-Robles aff003; Martha Elva Pérez Andrade aff002; Alain de J. Hernández-Vázquez aff002; Antonio Velázquez-Arellano aff002; Juan Miranda-Ríos aff002
Působiště autorů:
Programa de Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México (UNAM), Ciudad de México, México
aff001; Unidad de Genética de la Nutrición, Depto. de Biología Molecular y Biotecnología, Instituto de Investigaciones Biomédicas, UNAM e Instituto Nacional de Pediatría, Ciudad de México, México
aff002; Laboratorio de Morfología Celular y Tisular, Instituto Nacional de Pediatría, Ciudad de México, México
aff003
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0226652
Souhrn
Glucose is an important nutrient that dictates the development, fertility and lifespan of all organisms. In humans, a deficit in its homeostatic control might lead to hyperglucemia and the development of obesity and type 2 diabetes, which show a decreased ability to respond to and metabolize glucose. Previously, we have reported that high-glucose diets (HGD) induce alterations in triglyceride content, body size, progeny, and the mRNA accumulation of key regulators of carbohydrate and lipid metabolism, and longevity in Caenorhabditis elegans (PLoS ONE 13(7): e0199888). Herein, we show that increasing amounts of glucose in the diet induce the swelling of both mitochondria in germ and muscle cells. Additionally, HGD alter the enzymatic activities of the different respiratory complexes in an intricate pattern. Finally, we observed a downregulation of ceramide synthases (hyl-1 and hyl-2) and antioxidant genes (gcs-1 and gst-4), while mitophagy genes (pink-1 and dct-1) were upregulated, probably as part of a mitohormetic mechanism in response to glucose toxicity.
Klíčová slova:
Caenorhabditis elegans – Messenger RNA – Polymerase chain reaction – Mitochondria – Mitochondrial DNA – Glucose – Endoplasmic reticulum
Zdroje
1. Friedman F, Nunnari J. Mitochondrial form and function. Nature. 2014; 505:335–343. doi: 10.1038/nature12985 24429632
2. López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell. 2013; 153:1194–1217. doi: 10.1016/j.cell.2013.05.039 23746838
3. Sebastián D, Palacín M, Zorzano A. Mitochondrial dynamics: coupling mitochondrial fitness with healthy aging. Trends Mol Med. 2017; 23: 201–215. doi: 10.1016/j.molmed.2017.01.003 28188102
4. Szendroedi J, Phielix E, Roden M. The role of mitochondria in insulin resistance and type 2 diabetes mellitus. Nat Rev Endocrinol. 2011; 8:92–103. doi: 10.1038/nrendo.2011.138 21912398
5. Labbé K, Murley A, Nunnari J. Determinants and functions of mitochondrial behavior. Annu Rev Cell Dev Biol. 2014; 30: 357–391. doi: 10.1146/annurev-cellbio-101011-155756 25288115
6. Mishra P, Chan DC. Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol. 2014; 15: 634–646. doi: 10.1038/nrm3877 25237825
7. Cogliati S, Enriquez JA, Scorrano L. Mitochondrial cristae: where beauty meets functionality. Trends Biochem. Sci. 2016; 41:261–273. doi: 10.1016/j.tibs.2016.01.001 26857402
8. Gomes LC, Di Benedetto G, Scorrano L. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 2011; 13:589–598. doi: 10.1038/ncb2220 21478857
9. Rambold AS, Kostelecky B, Elia N, Lippincott-Schwartz J. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc Natl Acad Sci. USA. 2011; 108: 10190–10195. doi: 10.1073/pnas.1107402108 21646527
10. Svensk E, Devkota R, Ståhlman M, Ranji P, Rauthan M, Magnusson F, et al. Caenorhabditis elegans PAQR-2 and IGLR-2 protect against glucose toxicity by modulating membrane lipid composition. PLoS Genet. 2016; 12(4):e1005982. doi: 10.1371/journal.pgen.1005982 27082444
11. Mondoux MA, Love DC, Ghosh SK, Fukushige T, Bond M, Weerasinghe GR, et al. O-linked-N-acetyl- glucosamine cycling and insulin signaling are required for the glucose stress response in Caenorhabditis elegans. Genetics. 2011; 188(2):369–382. doi: 10.1534/genetics.111.126490 21441213
12. Choi SS. High glucose diets shorten lifespan of Caenorhabditis elegans via ectopic apoptosis induction. Nutr Res Pract. 2011; 5(3):214–218. doi: 10.4162/nrp.2011.5.3.214 21779524
13. Schlotterer A, Kukudov G, Bozorgmehr F, Hutter H, Du X, Oikonomou D, et al. C. elegans as model for the study of high glucose-mediated life span reduction. Diabetes. 2009; 58(11):2450–2456. doi: 10.2337/db09-0567 19675139
14. Lee SJ, Murphy CT, Kenyon C. Glucose shortens the life span of C. elegans by downregulating DAF- 16/FOXO activity and aquaporin gene expression. Cell Metab. 2009; 10(5):379–391. doi: 10.1016/j.cmet.2009.10.003 19883616
15. Garcia AM, Ladage ML, Dumesnil DR, Zaman K, Shulaev V, Azad RK, et al. Glucose Induces Sensitivity to Oxygen Deprivation and Modulates Insulin/IGF-1 Signaling and Lipid Biosynthesis in Caenorhabditis elegans. Genetics 2015; 200(1):167–184. doi: 10.1534/genetics.115.174631 25762526
16. Liggett MR, Hoy MJ, Mastroianni M, Mondoux MA. High-glucose diets have sex-specific effects on aging in C. elegans: toxic to hermaphrodites but beneficial to males. Aging (Albany NY). 2015;7(6):383–388.
17. Alcántar-Fernández J, Navarro RE, Salazar-Martínez AM, Pérez-Andrade ME, Miranda-Ríos J. Caenorhabditis elegans respond to high-glucose diets through a network of stress-responsive transcription factors. PLoS One. 2018;13(7):e0199888. doi: 10.1371/journal.pone.0199888 29990370
18. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974; 77:71–94. 4366476
19. Wood W. The nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory. 1998; 17:667.
20. Furda AM, Bess AS, Meyer JN, Van Houten B. Analysis of DNA damage and repair in nuclear and mitochondrial DNA of animal cells using quantitative PCR. Methods Mol Biol. 2012; 920:111–132. doi: 10.1007/978-1-61779-998-3_9 22941600
21. Li J, Cai T, Wu P, Cui Z, Chen X, Hou J, et al. Proteomic analysis of mitochondria from Caenorhabditis elegans. Proteomics. 2009; 9(19):4539–53. doi: 10.1002/pmic.200900101 19670372
22. Bradford MM. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding”. Anal. Biochem. 1976. 72: 248–254. doi: 10.1006/abio.1976.9999 942051
23. Spinazzi M, Casarin A, Pertegato V, Salviati L, Angelini C. Assessment of mitochondrial respiratory chain enzymatic activities on tissues and cultured cells. Nat Protoc. 2012; 7(6):1235–1246. doi: 10.1038/nprot.2012.058 22653162
24. Hoogewijs D, Houthoofd K, Matthijssens F, Vandesompele J, Vanfleteren JR. Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans. BMC Mol Biol. 2008; 9:9. doi: 10.1186/1471-2199-9-9 18211699
25. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001; 29(9):e45. doi: 10.1093/nar/29.9.e45 11328886
26. Lemire B. Mitochondrial genetics. Wormbook. 2005; 14:1–10.
27. Benard G, Faustin B, Passerieux E, Galinier A, Rocher C, Bellance N, et al. Physiological diversity of mitochondrial oxidative phosphorylation. Amm J Physiol Cell Physiol. 2006; 291(6):C1172–C1182.
28. Cristina D, Cary M. Lunceford A, Clarke C, Kenyon C. A regulated response to impaired respiration slows behavioral rates and increases lifespan in Caenorhabditis elegans. PLoS Genetics. 2009; 5:e1000450. doi: 10.1371/journal.pgen.1000450 19360127
29. Xu C, Hwang W, Jeong DE, Ryu Y, Ha CM, Lee SV, et al. Genetic inhibition of an ATP synthase subunit extends lifespan in C. elegans. Sci Rep. 2018; 8(1):14836. doi: 10.1038/s41598-018-32025-w 30287841
30. Liu F, Thatcher JD, Barral JM, Epstein HF. Bifunctional glyoxylate cycle protein of Caenorhabditis elegans: a developmentally regulated protein of intestine and muscle. Dev Biol. 1995; 169:399–414. doi: 10.1006/dbio.1995.1156 7781887
31. Montgomery MK, Turner N. Mitochondrial dysfunction and insulin resistance: an update. Endocr Connect. 2015; 4(1):R1–R5. doi: 10.1530/EC-14-0092 25385852
32. Menuz V, Howell KS, Gentina S, Epstein S, Riezman I, Fornallaz-Mulhauser M, et al. Protection of C. elegans from anoxia by HYL-2 ceramide synthase. Science. 2009; 324(5925):381–384. doi: 10.1126/science.1168532 19372430
33. An JH, Blackwell TK, SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev. 2003; 17:1882–1893. doi: 10.1101/gad.1107803 12869585
34. Oliveira RP, Abate J, Dilks K, Landis J, Ashraf J, Murphy CT, et al. 2009. Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf. Aging Cell. 2009; 8:524–541. doi: 10.1111/j.1474-9726.2009.00501.x 19575768
35. Fang EF, Hou Y, Palikaras K, Adriaanse BA, Kerr JS, Yang B, et al. Mitophagy inhibits amyloid-β and tau pathology and reverses cognitive deficits in models of Alzheimer's disease. Nat Neurosci. 2019; 22(3):401–412. doi: 10.1038/s41593-018-0332-9 30742114
36. Barbosa de Queiroz K, Honorato-Sampaio K, Rossoni Júnior JV, Andrade Leal D, Pinto AB, Kappes-Becker L, et al. Physical activity prevents alterations in mitochondrial ultrastructure and glucometabolic parameters in a high-sugar diet model. PLoS One. 2017; 12(2):e0172103. doi: 10.1371/journal.pone.0172103 28199417
37. Yang X, Borg LA, Eriksson UJ. Altered mitochondrial morphology of rat embryos in diabetic pregnancy. Anat Rec. 1995; 241(2):255–267. doi: 10.1002/ar.1092410212 7710141
38. Griparic L, van der Bliek AM. The many shapes of mitochondrial membranes. Traffic. 2001; 2:235–244. doi: 10.1034/j.1600-0854.2001.1r008.x 11285133
39. Paumard P, Vaillier J, Coulary B, Schaeffer J, Soubannier V, Mueller DM, et al. The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 2002; 21:221–230. doi: 10.1093/emboj/21.3.221 11823415
40. Lee SS, Lee RY, Fraser AG, Kamath RS, Ahringer J, Ruvkun G. A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity, Nat Genet, 2003; 33: 40–48. doi: 10.1038/ng1056 12447374
41. Ichishita R, Tanaka K, Sugiura Y, Sayano T, Mihara K, Oka T. An RNAi screen for mitochondrial proteins required to maintain the morphology of the organelle in Caenorhabditis elegans. J Biochem. 2008; 143(4):449–454. doi: 10.1093/jb/mvm245 18174190
42. Hammerschmidt P, Ostkotte D, Nolte H, Gerl MJ, Jais A, Brunner HL, et al. CerS6-derived dphingolipids interact with Mff and promote mitochondrial fragmentation in obesity. Cell. 2019;177(6):1536–1552. doi: 10.1016/j.cell.2019.05.008 31150623
43. Ban-Ishihara R, Ishihara T, Sasaki N, Mihara K, Ishihara N. Dynamics of nucleoid structure regulated by mitochondrial fission contributes to cristae reformation and release of cytochrome c. Proc. Natl. Acad. Sci. U.S.A. 2013; 110:11863–11868. doi: 10.1073/pnas.1301951110 23821750
44. Wang C, Taki M, Sato Y, Tamura Y, Yaginuma H, Okada Y, et al. A photostable fluorescent marker for the superresolution live imaging of the dynamic structure of the mitochondrial cristae. Proc Natl Acad Sci USA. 2019; 116(32):15817–15822. doi: 10.1073/pnas.1905924116 31337683
45. Jarmuszkiewicz W, Szewczyk A. Energy- dissipating hub in muscle mitochondria: potassium channels and uncoupling proteins. Arch. Biochem. Biophys. 2019; 664:102–109. doi: 10.1016/j.abb.2019.01.036 30716282
46. Giorgi C, Marchi S, Pinton P. The machineries, regulation and cellular functions of mitochondrial calcium. Nat. Rev. Mol. Cell Biol. 2018; 19:713–730. doi: 10.1038/s41580-018-0052-8 30143745
47. Nowikovsky K, Froschauer EM, Zsurka G, Samaj J, Reipert S, Kolisek M, et al. The LETM1/YOL027 gene family encodes a factor of the mitochondrial K+ homeostasis with a potential role in the Wolf–Hirschhorn syndrome. J Biol Chem. 2004; 279:30307–30315. doi: 10.1074/jbc.M403607200 15138253
48. Hasegawa A, van der Bliek AM. Inverse correlation between expression of the Wolfs Hirschhorn candidate gene Letm1 and mitochondrial volume in C. elegans and in mammalian cells. Hum Mol Genet. 2007; 16(17):2061–2071. doi: 10.1093/hmg/ddm154 17606466
49. Larsen S, Nielsen J, Hansen CN, Nielsen LB, Wibrand F, Stride N, et al. Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol. 2012; 590(14):3349–3360. doi: 10.1113/jphysiol.2012.230185 22586215
50. Reinke SN, Hu X, Sykes BD, Lemire BD. Caenorhabditis elegans diet significantly affects metabolic profile, mitochondrial DNA levels and brood size. Mol Genet Metab. 2010; 100(3): 274–282. doi: 10.1016/j.ymgme.2010.03.013 20400348
51. Moreno-Loshuertos R, Enríquez JA. Respiratory supercomplexes and the functional segmentation of the CoQ pool. Free Radic. Biol. Med. 2016;100:5–13. doi: 10.1016/j.freeradbiomed.2016.04.018 27105951
52. Sergi D, Naumovski N, Heilbronn LK, Abeywardena M, O'Callaghan N, Lionetti L, et al. Mitochondrial (dys)function and insulin resistance: from pathophysiological molecular mechanisms to the impact of diet. Front Physiol. 2019;10:532. doi: 10.3389/fphys.2019.00532 31130874
53. Kayser EB, Sedensky MM, Morgan PG, Hoppel CL. Mitochondrial oxidative phosphorylation is defective in the long-lived mutant clk-1. J Biol Chem 2004; 279:54479–54486. doi: 10.1074/jbc.M403066200 15269213
54. Suthammarak W, Morgan PG, Sedensky MM. Mutations in mitochondrial complex III uniquely affect complex I in Caenorhabditis elegans. J Biol Chem. 2010; 285:40724–40731. doi: 10.1074/jbc.M110.159608 20971856
55. Suthammarak W, Yang YY, Morgan PG, Sedensky MM. Complex I function is defective in complex IV-deficient Caenorhabditis elegans. J Biol Chem 2009; 284: 6425–6435. doi: 10.1074/jbc.M805733200 19074434
56. Schulz TJ, Zarse K, Voigt A, Urban N, Birringer M, Ristow M. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 2007; 6(4):280–293. doi: 10.1016/j.cmet.2007.08.011 17908557
57. Moreno-Arriola E, El Hafidi M, Ortega-Cuellar D, Carvajal K. AMP-Activated Protein Kinase Regulates Oxidative Metabolism in Caenorhabditis elegans through the NHR-49 and MDT-15 transcriptional regulators. PloS ONE. 2016; 11(1):e0148089. doi: 10.1371/journal.pone.0148089 26824904
58. Gallo M, Park D, Riddle DL. Increased longevity of some C. elegans mitochondrial mutants explained by activation of an alternative energy-producing pathway. Mechanisms Ageing Dev. 2011; 132:515–518.
59. Van Raamsdonk JM, Meng Y, Camp D, Yang W, Jia X, Bénard C, et al. Decreased energy metabolism extends life span in Caenorhabditis elegans without reducing oxidative damage. Genetics. 2010; 185:559–571. doi: 10.1534/genetics.110.115378 20382831
60. Copeland JM, Cho J, Lo T Jr, Hur JH, Bahadorani S, Arabyan T, et al. Extension of Drosophila life span by RNAi of the mitochondrial respiratory chain. Curr Biol. 2009; 19:1591–1598. doi: 10.1016/j.cub.2009.08.016 19747824
61. Dillin A, Hsu AL, Arantes-Oliveira N, Lehrer-Graiwer J, Hsin H, Fraser AG, et al. Rates of behavior and aging specifed by mitochondrial function during development. Science. 2002; 298:2398–2401. doi: 10.1126/science.1077780 12471266
62. Hannun YA, Obeid LM. Many ceramides. J Biol Chem. 2011; 286(32): 27855–27862. doi: 10.1074/jbc.R111.254359 21693702
63. Xia JY, Morley TS, Scherer PE. The adipokine/ceramide axis: key aspects of insulin sensitization. Biochimie. 2014; 96:130–139. doi: 10.1016/j.biochi.2013.08.013 23969158
64. Larsen PJ, Tennagels N. On ceramides, other sphingolipids and impaired glucose homeostasis. Mol. Metab. 2014; 3(3):252–260. doi: 10.1016/j.molmet.2014.01.011 24749054
65. Liu Y, Samuel BS, Breen PC, Ruvkun G. Caenorhabditis elegans pathways that surveil and defend mitochondria. Nature. 2014; 508(7496): 406–410. doi: 10.1038/nature13204 24695221
66. Deng X, Yin X, Allan R, Lu DD, Maurer CW, Haimovitz-Friedman A, et al. Ceramide biogenesis is required for radiation-induced apoptosis in the germ line of C. elegans. Science. 2008; 322(5898):110–115. doi: 10.1126/science.1158111 18832646
67. Lopez X, Goldfine AB, Holland WL, Gordillo R, Scherer PE. Plasma ceramides are elevated in female children and adolescents with type 2 diabetes. J Pediatr Endocrinol Metab. 2013; 26(9–10):995–998. doi: 10.1515/jpem-2012-0407 23612696
68. Ladage ML, King SD, Burks DJ, Quan DL, Garcia AM, Azad RK, et al. Glucose or altered ceramide biosynthesis mediate oxygen deprivation sensitivity through novel pathways revealed by transcriptome analysis in Caenorhabditis elegans. G3 (Bethesda). 2016; 6(10):3149–3160.
69. Li L, Chen Y, Chenzhao C, Fus S, Xu Q, Zhao J. Glucose negatively affects Nrf2/SKN-1-mediated immunity in C. elegans. Aging (Albany NY). 2018; 10(11):3089–3103.
70. Wang C, Zhang Y, Li F, Wei Y. Conserved roles of glucose in suppressing reactive oxygen species-induced cell death and animal survival. Aging (Albany NY). 2019;11(15):5726–5743.
71. Riedinger C, Mendler M, Schlotterer A, Fleming T, Okun J, Hammes HP, et al. High-glucose toxicity is mediated by AICAR-trasnfomylase/IMP cyclohydrolase and mitigated by AMP-activated protein kinase in Caenorhabditis elegans. J Biol Chem. 2018; 293(13):4845–4859. doi: 10.1074/jbc.M117.805879 29414769
72. Sun N, Yun J, Liu J, Malide D, Liu C, Rovira II, et al. Measuring in vivo mitophagy. Mol. Cell. 2015; 60(4):685–696. doi: 10.1016/j.molcel.2015.10.009 26549682
73. Song Y, Du Y, Zou W, Luo Y, Zhang X, Fu J. Involvement of impaired autophagy and mitophagy in Neuro-2a cell damage under hypoxic and/or high-glucose conditions. Sci. Rep. 2018; 8(1): 3301. doi: 10.1038/s41598-018-20162-1 29459731
74. Palikaras K, Lionaki E, Tavernarakis N. Coordination of mitophagy and mitochondrial biogenesis during ageing in C. elegans. Nature. 2015; 521:525–528. doi: 10.1038/nature14300 25896323
75. Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. 2012. Science. 337(6098): 1062–1065. doi: 10.1126/science.1219855 22936770
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