Metabolic Catastrophe in Mice Lacking Transferrin Receptor in Muscle

EBioMedicine

Volumn 2, Issue 11, 2015, Pages 1705-1717

  Barrientos, Tomasa ^a   Laothamatas, Indira ^a   Koves, Timothy R ^a   Soderblom, Erik J ^a   Bryan, Miles ^a   Moseley, M Arthur ^a   Muoio, Deborah M ^a   Andrews, Nancy C ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Hepcidin; Intermediary metabolism; Iron; Skeletal muscle; Transferrin receptor

Indexed keywords

ACONITATE HYDRATASE; BRAIN DERIVED NEUROTROPHIC FACTOR; CD71 ANTIGEN; COMPLEMENTARY DNA; ESTROGEN RELATED RECEPTOR ALPHA; FERRITIN; GLUCOSE; HEPCIDIN; INSULIN; IRON; IRON DEXTRAN; IRON REGULATORY FACTOR; KETONE; MESSENGER RNA; PANTOTHENATE KINASE; TRANSFERRIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; FATTY LIVER; FEMALE; GENE EXPRESSION REGULATION; GLUCONEOGENESIS; HOMEOSTASIS AND REGULATION; HYPOGLYCEMIA; IRON DEFICIENCY; IRON HOMEOSTASIS; IRON RESPONSIVE ELEMENT; MALE; METABOLOMICS; MICROARRAY ANALYSIS; MORPHOMETRICS; MOUSE; MUSCLE METABOLISM; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; PRIORITY JOURNAL; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR BINDING ASSAY; SKELETAL MUSCLE; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING; ANIMAL; CLUSTER ANALYSIS; DEFICIENCY; GENETICS; IRON METABOLISM DISORDER; KNOCKOUT MOUSE; LETHAL GENE; LIVER; METABOLISM; METABOLOME; MUSCLE; PATHOLOGY; PROCEDURES; TRANSGENIC MOUSE;

ANIMALS; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION; GENES, LETHAL; IRON; IRON METABOLISM DISORDERS; LIVER; METABOLOME; METABOLOMICS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUSCLES; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; RECEPTORS, TRANSFERRIN;

EID: 84958934739     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2015.09.041     Document Type: Article

References (52)

1. An J., Muoio D.M., Shiota M., Fujimoto Y., Cline G.W., Shulman G.I., Koves T.R., Stevens R., Millington D., Newgard C.B. Hepatic expression of malonyl-CoA decarboxylase reverses muscle, liver and whole-animal insulin resistance. Nat. Med. 2004, 10:268-274.
2. Anderson K.A., Hirschey M.D. Mitochondrial protein acetylation regulates metabolism. Essays Biochem. 2012, 52:23-35.
3. Andrews N.C. Medical Progress: Disorders of Iron Metabolism. N. Engl. J. Med. 1999, 341:1986-1995.
4. Baker E., Baker S.M., Morgan E.H. Characterisation of non-transferrin-bound iron (ferric citrate) uptake by rat hepatocytes in culture. Biochim. Biophys. Acta 1998, 1380:21-30.
5. Barisani D., Berg C.L., Wessling-Resnick M., Gollan J.L. Evidence for a low Km transporter for non-transferrin-bound iron in isolated rat hepatocytes. Am. J. Phys. 1995, 269:G570-G576.
6. Barrientos T., Andrews N.C. Expression Data from Wildtype and Tfr1 Skeletal Muscle KO Mice. NCBI: NCBI Gene Expression Omnibus 2015.
7. Bharathi S.S., Zhang Y., Mohsen A.W., Uppala R., Balasubramani M., Schreiber E., Uechi G., Beck M.E., Rardin M.J., Vockley J., Verdin E., Gibson B.W., Hirschey M.D., Goetzman E.S. Sirtuin 3 (SIRT3) protein regulates long-chain Acyl-CoA dehydrogenase by deacetylating conserved lysines near the active site. J. Biol. Chem. 2013, 288:33837-33847.
8. Carson F.L., Hladlik C. Oil red O Method for Neutral Fats. Histotechnology: A Self-Instructional Text 2009, American Society for Clinical Pathology Press, Chicago. F.L. Carson, C. Hladlik (Eds.).
9. Chen A.C., Donovan A., Ned-Sykes R., Andrews N.C. A Non-Canonical Role of Transferrin Receptor 1 is Essential for Intestinal Homeostasis. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:11714-11719.
10. Courselaud B., Pigeon C., Inoue Y., Inoue J., Gonzalez F.J., Leroyer P., Gilot D., Boudjema K., Guguen-Guillouzo C., Brissot P., Loreal O., Ilyin G. C/EBPalpha regulates hepatic transcription of hepcidin, an antimicrobial peptide and regulator of iron metabolism. Cross-talk between C/EBP pathway and iron metabolism. J. Biol. Chem. 2002, 277:41163-41170.
11. Crooks D.R., Natarajan T.G., Jeong S.Y., Chen C., Park S.Y., Huang H., Ghosh M.C., Tong W.H., Haller R.G., Wu C., Rouault T.A. Elevated FGF21 secretion, PGC-1alpha and ketogenic enzyme expression are hallmarks of iron-sulfur cluster depletion in human skeletal muscle. Hum. Mol. Genet. 2014, 23:24-39.
12. Finch C. Regulators of iron balance in humans. Blood 1994, 84:1697-1702.
13. Foster D.B., Liu T., Rucker J., O'Meally R.N., Devine L.R., Cole R.N., O'Rourke B. The Cardiac Acetyl-Lysine Proteome. PLoS One 2013, 8.
14. Han S.H., Jeon J.H., Ju H.R., Jung U., Kim K.Y., Yoo H.S., Lee Y.H., Song K.S., Hwang H.M., Na Y.S., Yang Y., Lee K.N., Choi I. VDUP1 upregulated by TGF-beta1 and 1,25-dihydorxyvitamin D3 inhibits tumor cell growth by blocking cell-cycle progression. Oncogene 2003, 22:4035-4046.
15. Hentze M.W., Muckenthaler M.U., Andrews N.C. Balancing acts: molecular control of mammalian iron metabolism. Cell 2004, 117:285-297.
16. Jensen M.V., Joseph J.W., Ilkayeva O., Burgess S., Lu D., Ronnebaum S.M., Odegaard M., Becker T.C., Sherry A.D., Newgard C.B. Compensatory responses to pyruvate carboxylase suppression in islet beta-cells. Preservation of glucose-stimulated insulin secretion. J. Biol. Chem. 2006, 281:22342-22351.
17. Kautz L., JUNG G., Valore E.V., Rivella S., Nemeth E., Ganz T. Identification of erythroferrone as an erythroid regulator of iron metabolism. Nat. Genet. 2014, 46:678-684.
18. Kersten S., Lichtenstein L., Steenbergen E., Mudde K., Hendriks H.F., Hesselink M.K., Schrauwen P., Muller M. Caloric restriction and exercise increase plasma ANGPTL4 levels in humans via elevated free fatty acids. Arterioscler. Thromb. Vasc. Biol. 2009, 29:969-974.
19. Kim S.C., Sprung R., Chen Y., Xu Y., Ball H., Pei J., Cheng T., Kho Y., Xiao H., Xiao L., Grishin N.V., White M., Yang X.J., Zhao Y. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 2006, 23:607-618.
20. Klempa K.L., Willis W.T., Chengson R., Dallman P.R., Brooks G.A. Iron deficiency decreases gluconeogenesis in isolated rat hepatocytes. J. Appl. Physiol. (1985) 1989, 67:1868-1872.
21. Leonardi R., Rehg J.E., Rock C.O., Jackowski S. Pantothenate kinase 1 is required to support the metabolic transition from the fed to the fasted state. PLoS One 2010, 5.
22. Levy J.E., Jin O., Fujiwara Y., Kuo F., Andrews N.C. Transferrin receptor is necessary for development of erythrocytes and the nervous system. Nat. Genet. 1999, 21:396-399.
23. Li J.Y., Paragas N., Ned R.M., Qiu A., Viltard M., Leete T., Drexler I.R., Chen X., Sanna-Cherchi S., Mohammed F., Williams D., Lin C.S., Schmidt-Ott K.M., Andrews N.C., Barasch J. Scara5 is a ferritin receptor mediating non-transferrin iron delivery. Dev. Cell 2009, 16:35-46.
24. Liuzzi J.P., Aydemir F., Nam H., Knutson M.D., Cousins R.J. Zip14 (Slc39a14) mediates non-transferrin-bound iron uptake into cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13612-13617.
25. Miniou P., Tiziano D., Frugier T., Roblot N., Le Meur M., Melki J. Gene targeting restricted to mouse striated muscle lineage. Nucleic Acids Res. 1999, 27.
26. Mohamed J.S., Lopez M.A., Cox G.A., Boriek A.M. Ankyrin repeat domain protein 2 and inhibitor of DNA binding 3 cooperatively inhibit myoblast differentiation by physical interaction. J. Biol. Chem. 2013, 288:24560-24568.
27. Mootha V.K., Lindgren C.M., Eriksson K.F., Subramanian A., Sihag S., Lehar J., Puigserver P., Carlsson E., Ridderstrale M., Laurila E., Houstis N., Daly M.J., Patterson N., Mesirov J.P., Golub T.R., Tamayo P., Spiegelman B., Lander E.S., Hirschhorn J.N., Altshuler D., Groop L.C. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 2003, 34:267-273.
28. Muoio D.M. TXNIP links redox circuitry to glucose control. Cell Metab. 2007, 5:412-414.
29. Ned R.M., Swat W., Andrews N.C. Transferrin receptor 1 is differentially required in lymphocyte development. Blood 2003, 102:3711-3718.
30. Oudit G.Y., Sun H., Trivieri M.G., Koch S.E., Dawood F., Ackerley C., Yazdanpanah M., Wilson G.J., Schwartz A., Liu P.P., Backx P.H. L-type Ca(2+) channels provide a major pathway for iron entry into cardiomyocytes in iron-overload cardiomyopathy. Nat. Med. 2003, 9:1187-1194.
31. Ozden O., Park S.H., Wagner B.A., Yong Song H., Zhu Y., Vassilopoulos A., Jung B., Buettner G.R., Gius D. SIRT3 deacetylates and increases pyruvate dehydrogenase activity in cancer cells. Free Radic. Biol. Med. 2014, 76:163-172.
32. Pashkov V., Huang J., Parameswara V.K., Kedzierski W., Kurrasch D.M., Tall G.G., Esser V., Gerard R.D., Uyeda K., Towle H.C., Wilkie T.M. Regulator of G protein signaling (RGS16) inhibits hepatic fatty acid oxidation in a carbohydrate response element-binding protein (ChREBP)-dependent manner. J. Biol. Chem. 2011, 286:15116-15125.
33. Rardin M.J., Newman J.C., Held J.M., Cusack M.P., Sorensen D.J., Li B., Schilling B., Mooney S.D., Kahn C.R., Verdin E., Gibson B.W. Label-free quantitative proteomics of the lysine acetylome in mitochondria identifies substrates of SIRT3 in metabolic pathways. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:6601-6606.
34. Rardin M.J., Wiley S.E., Naviaux R.K., Murphy A.N., Dixon J.E. Monitoring phosphorylation of the pyruvate dehydrogenase complex. Anal. Biochem. 2009, 389:157-164.
35. Rensvold J.W., Ong S.E., Jeevananthan A., Carr S.A., Mootha V.K., Pagliarini D.J. Complementary RNA and protein profiling identifies iron as a key regulator of mitochondrial biogenesis. Cell Rep. 2013, 3:237-245.
36. Seldin M.M., Peterson J.M., Byerly M.S., Wei Z., Wong G.W. Myonectin (CTRP15), a novel myokine that links skeletal muscle to systemic lipid homeostasis. J. Biol. Chem. 2012, 287:11968-11980.
37. Spinazzi M., Casarin A., Pertegato V., Ermani M., Salviati L., Angelini C. Optimization of respiratory chain enzymatic assays in muscle for the diagnosis of mitochondrial disorders. Mitochondrion 2011, 11:893-904.
38. Sturrock A., Alexander J., Lamb J., Craven C.M., Kaplan J. Characterization of a transferrin-independent uptake system for iron in HeLa cells. J. Biol. Chem. 1990, 265:3139-3145.
39. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15545-15550.
40. Thyfault J.P., Cree M.G., Zheng D., Zwetsloot J.J., Tapscott E.B., Koves T.R., Ilkayeva O., Wolfe R.R., Muoio D.M., Dohm G.L. Contraction of insulin-resistant muscle normalizes insulin action in association with increased mitochondrial activity and fatty acid catabolism. Am. J. Physiol. Cell Physiol. 2007, 292:C729-C739.
41. Trenor C.C., Campagna D.R., Sellers V.M., Andrews N.C., Fleming M.D. The molecular defect in hypotransferrinemic mice. Blood 2000, 96:1113-1118.
42. Truett G.E., Heeger P., Mynatt R.L., Truett A.A., Walker J.A., Warman M.L. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 2000, 29(52):54.
43. Vos T., Flaxman A.D., Naghavi M., Lozano R., Michaud C., Ezzati M., Shibuya K., Salomon J.A., Abdalla S., Aboyans V., Abraham J., Ackerman I., Aggarwal R., Ahn S.Y., Ali M.K., Alvarado M., Anderson H.R., Anderson L.M., Andrews K.G., Atkinson C., Baddour L.M., Bahalim A.N., Barker-Collo S., Barrero L.H., Bartels D.H., Basanez M.G., Baxter A., BELL M.L., Benjamin E.J., Bennett D., Bernabe E., Bhalla K., Bhandari B., Bikbov B., Bin Abdulhak A., Birbeck G., Black J.A., Blencowe H., Blore J.D., Blyth F., Bolliger I., Bonaventure A., Boufous S., Bourne R., Boussinesq M., Braithwaite T., Brayne C., Bridgett L., Brooker S., Brooks P., Brugha T.S., Bryan-Hancock C., Bucello C., Buchbinder R., Buckle G., Budke C.M., Burch M., Burney P., Burstein R., Calabria B., Campbell B., Canter C.E., Carabin H., Carapetis J., Carmona L., Cella C., Charlson F., Chen H., Cheng A.T., Chou D., Chugh S.S., Coffeng L.E., Colan S.D., Colquhoun S., Colson K.E., Condon J., Connor M.D., Cooper L.T., Corriere M., Cortinovis M., De Vaccaro K.C., Couser W., Cowie B.C., Criqui M.H., Cross M., Dabhadkar K.C., Dahiya M., Dahodwala N., Damsere-Derry J., Danaei G., Davis A., De Leo D., Degenhardt L., Dellavalle R., Delossantos A., Denenberg J., Derrett S., Des Jarlais D.C., Dharmaratne S.D., Dherani M., et al. Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990-2010: a systematic analysis for the global burden of disease study 2010. Lancet 2012, 380:2163-2196.
44. Walden W.E., Selezneva A.I., Dupuy J., Volbeda A., Fontecilla-Camps J.C., Theil E.C., Volz K. Structure of dual function iron regulatory protein 1 complexed with ferritin IRE-RNA. Science 2006, 314:1903-1908.
45. Walsh J.J., Edgett B.A., Tschakovsky M.E., Gurd B.J. Fasting and exercise differentially regulate BDNF mRNA expression in human skeletal muscle. Appl. Physiol. Nutr. Metab. 2015, 40:96-98.
46. Wang N.D., Finegold M.J., Bradley A., Ou C.N., Abdelsayed S.V., Wilde M.D., Taylor L.R., Wilson D.R., Darlington G.J. Impaired energy homeostasis in C/EBP alpha knockout mice. Science 1995, 269:1108-1112.
47. Wieckowski M.R., Giorgi C., Lebiedzinska M., Duszynski J., Pinton P. Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells. Nat. Protoc. 2009, 4:1582-1590.
48. Wu J.Y., Kao H.J., Li S.C., Stevens R., Hillman S., Millington D., Chen Y.T. ENU mutagenesis identifies mice with mitochondrial branched-chain aminotransferase deficiency resembling human maple syrup urine disease. J. Clin. Invest. 2004, 113:434-440.
49. Xu W., Barrientos T., Andrews N.C. Iron and copper in mitochondrial diseases. Cell Metab. 2013, 17:319-328.
50. Xu A., Lam M.C., Chan K.W., Wang Y., Zhang J., Hoo R.L., Xu J.Y., Chen B., Chow W.S., Tso A.W., Lam K.S. Angiopoietin-like protein 4 decreases blood glucose and improves glucose tolerance but induces hyperlipidemia and hepatic steatosis in mice. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:6086-6091.
51. Yang J., Goetz D., Li J.Y., Wang W., Mori K., Setlik D., Du T., Erdjument-Bromage H., Tempst P., Strong R., Barasch J. An iron delivery pathway mediated by a lipocalin. Mol. Cell 2002, 10:1045-1056.
52. Yin L., Wu N., Curtin J.C., Qatanani M., Szwergold N.R., Reid R.A., Waitt G.M., Parks D.J., Pearce K.H., Wisely G.B., Lazar M.A. Rev-Erbalpha, a heme sensor that coordinates metabolic and circadian pathways. Science 2007, 318:1786-1789.