Ectopic expression of Wnt10b decreases adiposity and improves glucose homeostasis in obese rats

American Journal of Physiology - Endocrinology and Metabolism

Volumn 293, Issue 3, 2007, Pages

  Aslanidi, George ^a   Kroutov, Vadim ^a   Philipsberg, Glenn ^a   Lamb, Kenneth ^a   Campbell Thompson, Martha ^b   Walter, Glenn A ^b   Kurenov, Sergei ^a   Aguirre, J Ignacio ^b   Keller, Pernille ^c,d   Hankenson, Kurt ^c   MacDougald, Ormond A ^c   Zolotukhin, Sergei ^a,b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d Rigshospitalet   (Denmark)

Author keywords

Diabetes; Gene therapy; Obesity; Wnt10b

Indexed keywords

ADENOVIRUS VECTOR; BETA CATENIN; FIBROBLAST GROWTH FACTOR 4; GLYCOPROTEIN WNT10B; MOLECULAR MARKER; RECOMBINANT ADENO ASSOCIATED VIRUS; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; VASCULOTROPIN; WNT PROTEIN;

ADIPOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; BONE DENSITY; BONE STRENGTH; CONTROLLED STUDY; DRUG EFFECT; ENERGY BALANCE; FEMALE; FOOD INTAKE; GENE THERAPY; GLUCOSE HOMEOSTASIS; HYPERINSULINEMIA; IN VITRO STUDY; LIPID DIET; LIPID STORAGE; METABOLIC REGULATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OBESITY; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; WEIGHT GAIN; WEIGHT REDUCTION; WESTERN BLOTTING;

ADIPOSE TISSUE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; GENE THERAPY; GLUCOSE; HOMEOSTASIS; MUSCLE, SKELETAL; OBESITY; RATS; UP-REGULATION; WNT PROTEINS;

EID: 34548406873     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00248.2007     Document Type: Article

References (56)

1. Baron RA, Vignery A, Neff L, Silvergate A, Santa Maria A. Processing of Undecalcified Bone Specimens for Bone Histomorphometry: Techniques and Interpretation. Boca Raton, FL: CRC Press, 1983.
2. Bennett CN, Longo KA, Wright WS, Suva LJ, Lane TF, Hankenson KD, MacDougald OA. Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci USA 102: 3324-3329, 2005.
3. Bennett CN, Ross SE, Longo KA, Bajnok L, Hemati N, Johnson KW, Harrison SD, MacDougald OA. Regulation of Wnt signaling during adipogenesis. J Biol Chem 277: 30998-31004, 2002.
4. Brooks AR, Harkins RN, Wang P, Qian HS, Liu P, Rubanyi GM. Transcriptional silencing is associated with extensive methylation of the CMV promoter following adenoviral gene delivery to muscle. J Gene Med 6: 395-404, 2004.
5. Chao H, Liu Y, Rabinowitz J, Li C, Samulski RJ, Walsh CE. Several log increase in therapeutic transgene delivery by distinct adeno-associated viral serotype vectors. Mol Ther 2: 619-623, 2000.
6. Christodoulides C, Scarda A, Granzotto M, Milan G, Dalla Nora E, Keogh J, De Pergola G, Stirling H, Pannacciulli N, Sethi JK, Federspil G, Vidal-Puig A, Farooqi IS, O'Rahilly S, Vettor R. WNT10B mutations in human obesity. Diabetologia 49: 678-684, 2006.
7. Duivenvoorden I, Teusink B, Rensen PC, Romijn JA, Havekes LM, Voshol PJ. Apolipoprotein C3 deficiency results in diet-induced obesity and aggravated insulin resistance in mice. Diabetes 54: 664-671, 2005.
8. Ferreira LD, Pulawa LK, Jensen DR, Eckel RH. Overexpressing human lipoprotein lipase in mouse skeletal muscle is associated with insulin resistance. Diabetes 50: 1064-1068, 2001.
9. Fu L, John LM, Adams SH, Yu XX, Tomlinson E, Renz M, Williams PM, Soriano R, Corpuz R, Moffat B, Vandlen R, Simmons L, Foster J, Stephan JP, Tsai SP, Stewart TA. Fibroblast growth factor 19 increases metabolic rate and reverses dietary and leptin-deficient diabetes. Endocrinology 145: 2594-2603, 2004.
10. Grant SF, Thorleifsson G, Reynisdottir I, Benediktsson R, Manolescu A, Sainz J, Helgason A, Stefansson H, Emilsson V, Helgadottir A, Styrkarsdottir U, Magnusson KP, Walters GB, Palsdottir E, Jonsdottir T, Gudmundsdottir T, Gylfason A, Saemundsdottir J, Wilensky RL, Reilly MP, Rader DJ, Bagger Y, Christiansen C, Gudnason V, Sigurdsson G, Thorsteinsdottir U, Gulcher JR, Kong A, Stefansson K. Variant of transcription factor 7-like 2 (TCF7L2) gene confers risk of type 2 diabetes. Nat Genet 38: 320-323, 2006.
11. Harris HJ, Kotelevtsev Y, Mullins JJ, Seckl JR, Holmes MC. Intracellular regeneration of glucocorticoids by 11beta-hydroxysteroid dehydrogenase (11beta-HSD)-1 plays a key role in regulation of the hypothalamic-pituitary-adrenal axis: analysis of 11beta-HSD-1-deficient mice. Endocrinology 142: 114-120, 2001.
12. Hausman GJ, Wright JT, Thomas GB. Vascular and cellular development in fetal adipose tissue: lectin binding studies and immunocytochemistry for laminin and type IV collagen. Microvasc Res 41: 111-125, 1991.
13. Helgason A, Palsson S, Thorleifsson G, Grant SF, Emilsson V, Gunnarsdottir S, Adeyemo A, Chen Y, Chen G, Reynisdottir I, Benediktsson R, Hinney A, Hansen T, Andersen G, Borch-Johnsen K, Jorgensen T, Schafer H, Faruque M, Doumatey A, Zhou J, Wilensky RL, Reilly MP, Rader DJ, Bagger Y, Christiansen C, Sigurdsson G, Hebebrand J, Pedersen O, Thorsteinsdottir U, Gulcher JR, Kong A, Rotimi C, Stefansson K. Refining the impact of TCF7L2 gene variants on type 2 diabetes and adaptive evolution. Nat Genet 39: 218-225, 2007.
14. Hoover-Plow J, Ellis J, Yuen L. In vivo plasminogen deficiency reduces fat accumulation. Thromb Haemost 87: 1011-1019, 2002.
15. Kelley DE, Goodpaster BH. Skeletal muscle triglyceride. An aspect of regional adiposity and insulin resistance. Diabetes Care 24: 933-941, 2001.
16. Kennell JA, MacDougald OA. Wnt signaling inhibits adipogenesis through beta-catenin-dependent and -independent mechanisms. J Biol Chem 280: 24004-24010, 2005.
17. Kharitonenkov A, Shiyanova TL, Koester A, Ford AM, Micanovic R, Galbreath EJ, Sandusky GE, Hammond LJ, Moyers JS, Owens RA, Gromada J, Brozinick JT, Hawkins ED, Wroblewski VJ, Li DS, Mehrbod F, Jaskunas SR, Shanafelt AB. FGF-21 as a novel metabolic regulator. J Clin Invest 115: 1627-1635, 2005.
18. Kim JK, Fillmore JJ, Chen Y, Yu C, Moore IK, Pypaert M, Lutz EP, Kako Y, Velez-Carrasco W, Goldberg IJ, Breslow JL, Shulman GI. Tissue-specific overexpression of lipoprotein lipase causes tissue-specific insulin resistance. Proc Natl Acad Sci USA 98: 7522-7527, 2001.
19. Korach-Andre M, Gao J, Gounarides JS, Deacon R, Islam A, Laurent D. Relationship between visceral adiposity and intramyocellular lipid content in two rat models of insulin resistance. Am J Physiol Endocrinol Metab 288: E106-E116, 2005.
20. Kotelevtsev Y, Holmes MC, Burchell A, Houston PM, Schmoll D, Jamieson P, Best R, Brown R, Edwards CR, Seckl JR, Mullins JJ. 11beta-hydroxysteroid dehydrogenase type 1 knockout mice show attenuated glucocorticoid-inducible responses and resist hyperglycemia on obesity or stress. Proc Natl Acad Sci USA 94: 14924-14929, 1997.
21. Koza RA, Nikonova L, Hogan J, Rim JS, Mendoza T, Faulk C, Skaf J, Kozak LP. Changes in gene expression foreshadow diet-induced obesity in genetically identical mice. PLoS Genet 2: e81, 2006.
22. Kratochwil K, Galceran J, Tontsch S, Roth W, Grosschedl R. FGF4, a direct target of LEF1 and Wnt signaling, can rescue the arrest of tooth organogenesis in Lef1(-/-) mice. Genes Dev 16: 3173-3185, 2002.
23. Krishnan V, Bryant HU, Macdougald OA. Regulation of bone mass by Wnt signaling. J Clin Invest 116: 1202-1209, 2006.
24. Kuhlmann J, Neumann-Haefelin C, Belz U, Kalisch J, Juretschke HP, Stein M, Kleinschmidt E, Kramer W, Herling AW. Intramyocellular lipid and insulin resistance: a longitudinal in vivo 1H-spectroscopic study in Zucker diabetic fatty rats. Diabetes 52: 138-144, 2003.
25. Kuroda S, Kondo H, Ohya K, Kasugai S. Bone increase in rat tibiae by local administration of amino-terminally truncated rhFGF-4(73-206). Tissue Eng 13: 415-422, 2007.
26. Levin BE, Dunn-Meynell AA, Balkan B, Keesey RE. Selective breeding for diet-induced obesity and resistance in Sprague-Dawley rats. Am J Physiol Regul Integr Comp Physiol 273: R725-R730, 1997.
27. Longo KA, Wright WS, Kang S, Gerin I, Chiang SH, Lucas PC, Opp MR, MacDougald OA. Wnt10b inhibits development of white and brown adipose tissues. J Biol Chem 279: 35503-35509, 2004.
28. Masuzaki H, Paterson J, Shinyama H, Morton NM, Mullins JJ, Seckl JR, Flier JS. A transgenic model of visceral obesity and the metabolic syndrome. Science 294: 2166-2170, 2001.
29. Mick GJ, Wang X, McCormick K. White adipocyte vascular endothelial growth factor: regulation by insulin. Endocrinology 143: 948-953, 2002.
30. Morton NM, Holmes MC, Fievet C, Staels B, Tailleux A, Mullins JJ, Seckl JR. Improved lipid and lipoprotein profile, hepatic insulin sensitivity, and glucose tolerance in 11beta-hydroxysteroid dehydrogenase type 1 null mice. J Biol Chem 276: 41293-41300, 2001.
31. Negrel R, Dani C. Adipose Tissue Protocols. Totowa, NJ: Humana, 2001.
32. Neumann-Haefelin C, Kuhlmann J, Belz U, Kalisch J, Quint M, Gerl M, Juretschke HP, Herling AW. Determinants of intramyocellular lipid concentrations in rat hindleg muscle. Magn Reson Med 50: 242-248, 2003.
33. Oana F, Takeda H, Hayakawa K, Matsuzawa A, Akahane S, Isaji M, Akahane M. Physiological difference between obese (fa/fa) Zucker rats and lean Zucker rats concerning adiponectin. Metabolism 54: 995-1001, 2005.
34. Pahor M, Kritchevsky S. Research hypotheses on muscle wasting, aging, loss of function and disability. J Nutr Health Aging 2: 97-100, 1998.
35. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2: 595-610, 1987.
36. Perseghin G, Scifo P, De Cobelli F, Pagliato E, Battezzati A, Arcelloni C, Vanzulli A, Testolin G, Pozza G, Del Maschio A, Luzi L. Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes 48: 1600-1606, 1999.
37. Rankinen T, Zuberi A, Chagnon YC, Weisnagel SJ, Argyropoulos G, Walts B, Perusse L, Bouchard C. The human obesity gene map: the 2005 update. Obesity (Silver Spring) 14: 529-644, 2006.
38. Rosen ED, MacDougald OA. Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol 7: 885-896, 2006.
39. Ross SE, Erickson RL, Gerin I, DeRose PM, Bajnok L, Longo KA, Misek DE, Kuick R, Hanash SM, Atkins KB, Andresen SM, Nebb HI, Madsen L, Kristiansen K, MacDougald OA. Microarray analyses during adipogenesis: understanding the effects of Wnt signaling on adipogenesis and the roles of liver X receptor alpha in adipocyte metabolism. Mol Cell Biol 22: 5989-5999, 2002.
40. Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, MacDougald OA. Inhibition of adipogenesis by Wnt signaling. Science 289: 950-953, 2000.
41. Rupnick MA, Panigrahy D, Zhang CY, Dallabrida SM, Lowell BB, Langer R, Folkman MJ. Adipose tissue mass can be regulated through the vasculature. Proc Natl Acad Sci USA 99: 10730-10735, 2002.
42. Sladek R, Rocheleau G, Rung J, Dina C, Shen L, Serre D, Boutin P, Vincent D, Belisle A, Hadjadj S, Balkau B, Heude B, Charpentier G, Hudson TJ, Montpetit A, Pshezhetsky AV, Prentki M, Posner BI, Balding DJ, Meyre D, Polychronakos C, Froguel P. A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 445: 881-885, 2007.
43. Szczepaniak LS, Babcock EE, Schick F, Dobbins RL, Garg A, Burns DK, McGarry JD, Stein DT. Measurement of intracellular triglyceride stores by H spectroscopy: validation in vivo. Am J Physiol Endocrinol Metab 276: E977-E989, 1999.
44. Timmons JA, Wennmalm K, Larsson O, Walden TB, Lassmann T, Petrovic N, Hamilton DL, Gimeno RE, Wahlestedt C, Baar K, Nedergaard J, Cannon B. Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages. Proc Natl Acad Sci USA 104: 4401-4406, 2007.
45. Tomlinson E, Fu L, John L, Hultgren B, Huang X, Renz M, Stephan JP, Tsai SP, Powell-Braxton L, French D, Stewart TA. Transgenic mice expressing human fibroblast growth factor-19 display increased metabolic rate and decreased adiposity. Endocrinology 143: 1741-1747, 2002.
46. Turcotte LP, Swenberger JR, Zavitz Tucker M, Yee AJ. Increased fatty acid uptake and altered fatty acid metabolism in insulin-resistant muscle of obese Zucker rats. Diabetes 50: 1389-1396, 2001.
47. Unger RH. Minireview: weapons of lean body mass destruction: the role of ectopic lipids in the metabolic syndrome. Endocrinology 144: 5159-5165, 2003.
48. Urabe M, Ding C, Kotin RM. Insect cells as a factory to produce adeno-associated virus type 2 vectors. Hum Gene Ther 13: 1935-1943, 2002.
49. Vertino AM, Taylor-Jones JM, Longo KA, Bearden ED, Lane TF, McGehee RE, MacDougald OA, Peterson CA. Wnt10b deficiency promotes coexpression of myogenic and adipogenic programs in myoblasts. Mol Biol Cell 16: 2039-2048, 2005.
50. Voshol PJ, Jong MC, Dahlmans VE, Kratky D, Levak-Frank S, Zechner R, Romijn JA, Havekes LM. In muscle-specific lipoprotein lipase-overexpressing mice, muscle triglyceride content is increased without inhibition of insulin-stimulated whole-body and muscle-specific glucose uptake. Diabetes 50: 2585-2590, 2001.
51. Wente W, Efanov AM, Brenner M, Kharitonenkov A, Koster A, Sandusky GE, Sewing S, Treinies I, Zitzer H, Gromada J. Fibroblast growth factor-21 improves pancreatic beta-cell function and survival by activation of extracellular signal-regulated kinase 1/2 and Akt signaling pathways. Diabetes 55: 2470-2478, 2006.
52. Willert J, Epping M, Pollack JR, Brown PO, Nusse R. A transcriptional response to Wnt protein in human embryonic carcinoma cells. BMC Dev Biol 2: 8, 2002.
53. Wright WS, Longo KA, Dolinsky VW, Gerin I, Kang S, Bennett CN, Chiang SH, Prestwich TC, Gress C, Burant CF, Susulic VS, MacDougald OA. Wnt10b inhibits obesity in ob/ob and agouti mice. Diabetes 56: 295-303, 2007.
54. Xiao W, Chirmule N, Berta SC, McCullough B, Gao G, Wilson JM. Gene therapy vectors based on adeno-associated virus type 1. J Virol 73: 3994-4003, 1999.
55. Yau JL, Noble J, Kenyon CJ, Hibberd C, Kotelevtsev Y, Mullins JJ, Seckl JR. Lack of tissue glucocorticoid reactivation in 11beta- hydroxysteroid dehydrogenase type 1 knockout mice ameliorates age-related learning impairments. Proc Natl Acad Sci USA 98: 4716-4721, 2001.
56. Zolotukhin S, Potter M, Zolotukhin I, Sakai Y, Loiler S, Fraites TJ, Chiodo VA, Phillipsberg T, Muzyczka N, Hauswirth WW, Flotte TR, Byrne BJ, Snyder RO. Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods 28: 158-167, 2002.