GLUT12 deficiency during early development results in heart failure and a diabetic phenotype in zebrafish

Journal of Endocrinology

Volumn 224, Issue 1, 2015, Pages 1-15

  Jiménez Amilburu, Vanesa ^d   Jong Raadsen, Susanne ^b   Bakkers, Jeroen ^c   Spaink, Herman P ^a   Marín Juez, Rubén ^b  

^a LEIDEN UNIVERSITY   (Netherlands)

^b ZF screens BV ^*  (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

Valve dysgenesis; diabetes; Glut12; Heart failure; Zebrafish

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER; METFORMIN; RECOMBINANT HUMAN INSULIN; TRANSCRIPTOME; GLUT12 PROTEIN, ZEBRAFISH; INSULIN; ZEBRAFISH PROTEIN;

ADIPOSE TISSUE; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DIABETES MELLITUS; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE EXPRESSION; GENE SILENCING; GLUCOSE TRANSPORT; GLUCOSE TRANSPORTER 12 GENE; GLYCEMIC CONTROL; HEART ARRHYTHMIA; HEART ATRIUM CONTRACTION; HEART DEVELOPMENT; HEART EDEMA; HEART FAILURE; HEART MUSCLE; HEART VENTRICLE CONTRACTION; HYPERGLYCEMIA; INSULIN RESISTANCE; LARVA; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PHENOTYPE; PHYLOGENY; SEQUENCE ALIGNMENT; SKELETAL MUSCLE; TRANSCRIPTOMICS; VALVULAR HEART DISEASE; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; COMPLICATION; DEFICIENCY; DIABETIC CARDIOMYOPATHY; DISEASE MODEL; DRUG EFFECTS; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DIABETES MELLITUS, TYPE 2; DIABETIC CARDIOMYOPATHIES; DISEASE MODELS, ANIMAL; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; HEART FAILURE; INSULIN; METFORMIN; PHENOTYPE; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84919608680     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-14-0539     Document Type: Article

References (64)

1. Arany Z, He H, Lin J, Hoyer K, Handschin C, Toka O, Ahmad F, Matsui T, Chin S, Wu PH et al. 2005 Transcriptional coactivator PGC-1 a controls the energy state and contractile function of cardiac muscle. Cell Metabolism 1 259-271. (doi:10.1016/j.cmet.2005.03.002).
2. Bakkers J 2011 Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovascular Research 91 279-288. (doi:10.1093/cvr/cvr098).
3. Bell DS 2003a Diabetic cardiomyopathy. Diabetes Care 26 2949-2951. (doi:10.2337/diacare.26.10.2949).
4. Bell DS 2003b Heart failure: the frequent, forgotten, and often fatal complication of diabetes. Diabetes Care 26 2433-2441. (doi:10.2337/ diacare.26.8.2433).
5. Benjamini Y & Hochberg Y 1995 Controlling the false discovery rate-a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57 289-300.
6. van Bilsen M, Smeets PJ, Gilde AJ & van der Vusse GJ 2004 Metabolic remodelling of the failing heart: the cardiac burn-out syndrome? Cardiovascular Research 61 218-226. (doi:10.1016/j.cardiores.2003.11.014).
7. Burns CG & MacRae CA 2006 Purification of hearts from zebrafish embryos. BioTechniques 40 274, 276, 278 passim. (doi:10.2144/000112135).
8. Cao LZ, Tang DQ, Horb ME, Li SW & Yang LJ 2004 High glucose is necessary for complete maturation of Pdx1-VP16-expressing hepatic cells into functional insulin-producing cells. Diabetes 53 3168-3178. (doi:10.2337/diabetes.53.12.3168).
9. Chen Y, Wu B, Xu L, Li H, Xia J, Yin W, Li Z, Shi D, Li S, Lin S et al. 2012 A SNX10/V-ATPase pathway regulates ciliogenesis in vitro and in vivo. Cell Research 22 333-345. (doi:10.1038/cr.2011.134).
10. Chung S, Dzeja PP, Faustino RS, Perez-Terzic C, Behfar A & Terzic A 2007 Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nature Clinical Practice. Cardiovascular Medicine 4(Suppl 1) S60-S67. (doi:10.1038/ncpcardio0766).
11. Chung S, Arrell DK, Faustino RS, Terzic A & Dzeja PP 2010 Glycolytic network restructuring integral to the energetics of embryonic stem cell cardiac differentiation. Journal of Molecular and Cellular Cardiology 48 725-734. (doi:10.1016/j.yjmcc.2009.12.014).
12. Dekker RJ, van Soest S, Fontijn RD, Salamanca S, de Groot PG, VanBavel E, Pannekoe KH & Horrevoets AJ 2002 Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Kruppel-like factor (KLF2). Blood 100 1689-1698. (doi:10.1182/blood-2002-01-0046).
13. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC & Lempicki RA 2003 DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biology 4 P3. (doi:10.1186/gb-2003-4-5-p3).
14. Depre C, Shipley GL, Chen W, Han Q, Doenst T, Moore ML, Stepkowski S, Davies PJ & Taegtmeyer H 1998 Unloaded heart in vivo replicates fetal gene expression of cardiac hypertrophy. Nature Medicine 4 1269-1275. (doi:10.1038/3253).
15. Domenighetti AA, Danes VR, Curl CL, Favaloro JM, Proietto J & Delbridge LM 2010 Targeted GLUT-4 deficiency in the heart induces cardiomyocyte hypertrophy and impaired contractility linked with Ca(2+) and proton flux dysregulation. Journal of Molecular and Cellular Cardiology 48 663-672. (doi:10.1016/j.yjmcc.2009.11.017).
16. Farooq M, Sulochana KN, Pan X, To J, Sheng D, Gong Z & Ge R 2008 Histone deacetylase 3 (hdac3) is specifically required for liver development in zebrafish. Developmental Biology 317 336-353. (doi:10.1016/j.ydbio.2008.02.034).
17. Groenendijk BC, Hierck BP, Gittenberger-De Groot AC & Poelmann RE 2004 Development-related changes in the expression of shear stress responsive genes KLF-2, ET-1, and NOS-3 in the developing cardiovascular system of chicken embryos. Developmental Dynamics 230 57-68. (doi:10.1002/dvdy.20029).
18. Gut P, Baeza-Raja B, Andersson O, Hasenkamp L, Hsiao J, Hesselson D, Akassoglou K, Verdin E, Hirschey MD & Stainier DY 2013 Wholeorganism screening for gluconeogenesis identifies activators of fasting metabolism. Nature Chemical Biology 9 97-104. (doi:10.1038/ nchembio.1136).
19. Haslam DW & James WP 2005 Obesity. Lancet 366 1197-1209. (doi:10.1016/S0140-6736(05)67483-1).
20. Hellerstrom C & Swenne I 1991 Functional maturation and proliferation of fetal pancreatic β-cells. Diabetes 40(Suppl 2) 89-93. (doi:10.2337/ diab.40.2.S89).
21. Hove JR, Koster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE & Gharib M 2003 Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421 172-177. (doi:10.1038/ nature01282).
22. Huang CJ, Tu CT, Hsiao CD, Hsieh FJ & Tsai HJ 2003 Germ-line transmission of a myocardium-specific GFP transgene reveals critical regulatory elements in the cardiac myosin light chain 2 promoter of zebrafish. Developmental Dynamics 228 30-40. (doi:10.1002/dvdy. 10356).
23. Jorgensen SB, Richter EA & Wojtaszewski JF 2006 Role of AMPK in skeletal muscle metabolic regulation and adaptation in relation to exercise. Journal of Physiology 574 17-31. (doi:10.1113/jphysiol.2006.109942).
24. Jurczyk A, Roy N, Bajwa R, Gut P, Lipson K, Yang C, Covassin L, Racki WJ, Rossini AA, Phillips N et al. 2011 Dynamic glucoregulation and mammalian-like responses to metabolic and developmental disruption in zebrafish. General and Comparative Endocrinology 170 334-345. (doi:10.1016/j.ygcen.2010.10.010).
25. Kannel WB & McGee DL 1979 Diabetes and cardiovascular disease. The Framingham study. Journal of the American Medical Association 241 2035-2038. (doi:10.1001/jama.1979.03290450033020).
26. Katz EB, Stenbit AE, Hatton K, DePinho R & Charron MJ 1995 Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4. Nature 377 151-155. (doi:10.1038/377151a0).
27. Lawson ND & Weinstein BM 2002 In vivo imaging of embryonic vascular development using transgenic zebrafish. Developmental Biology 248 307-318. (doi:10.1006/dbio.2002.0711).
28. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM & Kelly DP 2000 Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. Journal of Clinical Investigation 106 847-856. (doi:10.1172/JCI10268).
29. Liang Q, De Windt LJ, Witt SA, Kimball TR, Markham BE & Molkentin JD 2001 The transcription factors GATA4 and GATA6 regulate cardiomyocyte hypertrophy in vitro and in vivo. Journal of Biological Chemistry 276 30245-30253. (doi:10.1074/jbc.M102174200).
30. Lopez AD, Mathers CD, Ezzati M, Jamison DT & Murray CJ 2006 Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet 367 1747-1757. (doi:10.1016/S0140-6736(06)68770-9).
31. Lorell BH & Grossman W 1987 Cardiac hypertrophy: the consequences for diastole. Journal of the American College of Cardiology 9 1189-1193. (doi:10.1016/S0735-1097(87)80326-1).
32. Louis A, Muffato M & Roest Crollius H 2013 Genomicus: five genome browsers for comparative genomics in eukaryota. Nucleic Acids Research 41 D700-D705. (doi:10.1093/nar/gks1156).
33. Macheda ML, Kelly DJ, Best JD & Rogers S 2002 Expression during rat fetal development of GLUT12-a member of the class III hexose transporter family. Anatomy and Embryology 205 441-452. (doi:10.1007/s00429-002-0263-8).
34. Marín-Juez R, Capilla E, Carvalho-Simoes F, Camps M & Planas JV 2014a Structural and functional evolution of glucose transporter 4 (GLUT4): a look at GLUT4 in fish. In Glucose Homeostasis. Ed L Szablewski. InTech: Rijeka, Croatia. (doi:10.5772/58094).
35. Maríń-Juez R, Jong-Raadsen S, Yang S & Spaink HP 2014b Hyperinsulinemia induces insulin resistance and immune suppression via Ptpn6/Shp1 in zebrafish. Journal of Endocrinology 222 229-241. (doi:10.1530/JOE-14-0178).
36. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E et al. 2003 PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nature Genetics 34 267-273. (doi:10.1038/ng1180).
37. Pagidipati NJ & Gaziano TA 2013 Estimating deaths from cardiovascular disease: a review of global methodologies of mortality measurement. Circulation 127 749-756. (doi:10.1161/CIRCULATIONAHA.112.128413).
38. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone R et al. 2003 Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. PNAS 100 8466-8471. (doi:10.1073/pnas.1032913100).
39. Puigserver P & Spiegelman BM 2003 Peroxisome proliferator-activated receptor-γ coactivator 1 α (PGC-1 α): transcriptional coactivator and metabolic regulator. Endocrine Reviews 24 78-90. (doi:10.1210/er. 2002-0012).
40. Pujol-Gimenez J, Martisova E, Perez-Mediavilla A, Lostao MP & Ramirez MJ 2014 Expression of the glucose transporter GLUT12 in Alzheimer's disease patients. Journal of Alzheimer's Disease 42 97-101. (doi:10.3233/ JAD-132498).
41. Purcell SH, Aerni-Flessner LB, Willcockson AR, Diggs-Andrews KA, Fisher SJ & Moley KH 2011 Improved insulin sensitivity by GLUT12 overexpression in mice. Diabetes 60 1478-1482. (doi:10.2337/db11-0033).
42. Razeghi P, Young ME, Alcorn JL, Moravec CS, Frazier OH & Taegtmeyer H 2001 Metabolic gene expression in fetal and failing human heart. Circulation 104 2923-2931. (doi:10.1161/hc4901.100526).
43. Rogers S, Macheda ML, Docherty SE, Carty MD, Henderson MA, Soeller WC, Gibbs EM, James DE & Best JD 2002 Identification of a novel glucose transporter-like protein-GLUT-12. American Journal of Physiology. Endocrinology and Metabolism 282 E733-E738.
44. Santalucia T, Camps M, Castello A,Munoz P, Nuel A, Testar X, Palacin M & Zorzano A 1992 Developmental regulation ofGLUT-1 (erythroid/HepG2) and GLUT-4 (muscle/fat) glucose transporter expression in rat heart, skeletal muscle, and brown adipose tissue. Endocrinology 130 837-846. (doi:10.1210/endo.130.2.1370797).
45. Scheepers A, Joost HG & Schurmann A 2004 The glucose transporter families SGLT and GLUT: molecular basis of normal and aberrant function. JPEN. Journal of Parenteral and Enteral Nutrition 28 364-371. (doi:10.1177/0148607104028005364).
46. Schertzer JD, Tamrakar AK, Magalhaes JG, Pereira S, Bilan PJ, Fullerton MD, Liu Z, Steinberg GR, Giacca A, Philpott DJ et al. 2011 NOD1 activators link innate immunity to insulin resistance. Diabetes 60 2206-2215. (doi:10.2337/db11-0004).
47. Seth A, Stemple DL & Barroso I 2013 The emerging use of zebrafish to model metabolic disease. Disease Models & Mechanisms 6 1080-1088. (doi:10.1242/dmm.011346).
48. Sliwa K, Damasceno A & Mayosi BM 2005 Epidemiology and etiology of cardiomyopathy in Africa. Circulation 112 3577-3583. (doi:10.1161/ CIRCULATIONAHA.105.542894).
49. Stenbit AE, Burcelin R, Katz EB, Tsao TS, Gautier N, Charron MJ & Le Marchand-Brustel Y 1996 Diverse effects of Glut 4 ablation on glucose uptake and glycogen synthesis in red and white skeletal muscle. Journal of Clinical Investigation 98 629-634. (doi:10.1172/JCI118833).
50. Stenbit AE, Tsao TS, Li J, Burcelin R, Geenen DL, Factor SM, Houseknecht K, Katz EB & Charron MJ 1997 GLUT4 heterozygous knockout mice develop muscle insulin resistance and diabetes. Nature Medicine 3 1096-1101. (doi:10.1038/nm1097-1096).
51. Stuart CA, Howell ME, Zhang Y & Yin D 2009 Insulin-stimulated translocation of glucose transporter (GLUT) 12 parallels that of GLUT4 in normal muscle. Journal of Clinical Endocrinology and Metabolism 94 3535-3542. (doi:10.1210/jc.2009-0162).
52. Swoap SJ, Weinshenker D, Palmiter RD & Garber G 2004 Dbh(K/K) mice are hypotensive, have altered circadian rhythms, and have abnormal responses to dieting and stress. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 286 R108-R113. (doi:10.1152/ajpregu.00405.2003).
53. Tachibana K, Jones N, Dumont DJ, Puri MC & Bernstein A 2005 Selective role of a distinct tyrosine residue on Tie2 in heart development and early hematopoiesis. Molecular and Cellular Biology 25 4693-4702. (doi:10.1128/MCB.25.11.4693-4702.2005).
54. Tessadori F, van Weerd JH, Burkhard SB, Verkerk AO, de Pater E, Boukens BJ, Vink A, Christoffels VM & Bakkers J 2012 Identification and functional characterization of cardiac pacemaker cells in zebrafish. PLoS ONE 7 e47644. (doi:10.1371/journal.pone.0047644).
55. Thisse B & Thisse C 2004 Fast release clones: a high throughput expression analysis. ZFIN Direct Data Submission ZFIN ID: ZDB-PUB-040907-1. (available at: http://zfin.org/cgi-bin/webdriver?MIval=aa-pubview2. apg&OID=ZDB-PUB-040907-1).
56. Tseng YC, Chen RD, Lee JR, Liu ST, Lee SJ & Hwang PP 2009 Specific expression and regulation of glucose transporters in zebrafish ionocytes. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 297 R275-R290. (doi:10.1152/ajpregu. 00180.2009).
57. Vermot J, Forouhar AS, Liebling M, Wu D, Plummer D, Gharib M & Fraser SE 2009 Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biology 7 e1000246. (doi:10.1371/journal.pbio.1000246).
58. Viollet B, Guigas B, Sanz Garcia N, Leclerc J, Foretz M & Andreelli F 2012 Cellular and molecular mechanisms of metformin: an overview. Clinical Science 122 253-270. (doi:10.1042/CS20110386).
59. van der Vusse GJ, van Bilsen M & Glatz JF 2000 Cardiac fatty acid uptake and transport in health and disease. Cardiovascular Research 45 279-293. (doi:10.1016/S0008-6363(99)00263-1).
60. Waller AP, George M, Kalyanasundaram A, Kang C, Periasamy M, Hu K & Lacombe VA 2013 GLUT12 functions as a basal and insulinindependent glucose transporter in the heart. Biochimica et Biophysica Acta 1832 121-127. (doi:10.1016/j.bbadis.2012.09.013).
61. Ware B, Bevier M, Nishijima Y, Rogers S, Carnes CA & Lacombe VA 2011 Chronic heart failure selectively induces regional heterogeneity of insulin-responsive glucose transporters. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 301 R1300-R1306. (doi:10.1152/ajpregu.00822.2010).
62. Zhang X, Azhar G, Chai J, Sheridan P, Nagano K, Brown T, Yang J, Khrapko K, Borras AM, Lawitts J et al. 2001 Cardiomyopathy in transgenic mice with cardiac-specific overexpression of serum response factor. American Journal of Physiology. Heart and Circulatory Physiology 280 H1782-H1792.
63. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N et al. 2001 Role of AMP-activated protein kinase in mechanism of metformin action. Journal of Clinical Investigation 108 1167-1174. (doi:10.1172/JCI13505).
64. Zuliani G, Galvani M, Maggio M, Volpato S, Bandinelli S, Corsi AM, Lauretani F, Cherubini A, Guralnik JM, Fellin R et al. 2010 Plasma soluble gp130 levels are increased in older subjects with metabolic syndrome. The role of insulin resistance. Atherosclerosis 213 319-324. (doi:10.1016/j.atherosclerosis.2010.08.074).