Adipogenic human adenovirus ad-36 induces commitment, differentiation, and lipid accumulation in human adipose-derived stem cells

Stem Cells

Volumn 26, Issue 4, 2008, Pages 969-978

  Pasarica, Magdalena ^a   Mashtalir, Nazar ^a   McAllister, Emily J ^a   Kilroy, Gail E ^a   Koska, Juraj ^b   Permana, Paska ^b   De Courten, Barbora ^b,c   Yu, Minghuan ^d   Ravussin, Eric ^a   Gimble, Jeffery M ^a   Dhurandhar, Nikhil V ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^d WAYNE STATE UNIVERSITY   (United States)

Author keywords

Adipocyte progenitors; Adipogenesis; Adiposity; Infectobesity; Lipogenesis; Obesity

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; FATTY ACID BINDING PROTEIN; LIPOPROTEIN LIPASE; LIPID;

ADENOVIRUS; ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE CELL; ADULT; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN ADENOVIRUS 36; HUMAN CELL; LIPID STORAGE; MALE; NONHUMAN; OBESITY; STEM CELL; STROMA CELL; ADIPOSE TISSUE; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; HUMAN ADENOVIRUS; LIPID METABOLISM; MIDDLE AGED; PHYSIOLOGY; VIROLOGY;

ANIMALIA; HUMAN ADENOVIRUS; RODENTIA;

ADENOVIRUSES, HUMAN; ADIPOCYTES; ADIPOGENESIS; ADIPOSE TISSUE; ADULT; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; HUMANS; LIPID METABOLISM; LIPIDS; MALE; MIDDLE AGED; STEM CELLS;

EID: 49249102406     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2007-0868     Document Type: Article

References (51)

1. Astrup A, Lundsgaard C, Stock MJ. Is obesity contagious? Int J Obes Relat Metab Disord 1998;22:375-376.
2. Powledge TM. Is obesity an infectious disease? Lancet Infect Dis 2004;4:599.
3. Rössner S. Can obesity be an infectious disease? [in Swedish]. Lakartidningen 2005;102:1896-1898.
4. Bernard A, Fevre-Montange M, Bencsik A et al. Brain structures selectively targeted by canine distemper virus in a mouse model infection. J Neuropathol Exp Neurol 1993;52:471- 480.
5. Bernard A, Fevre-Montange M, Giraudon P et al. Demonstration of viral proteins and RNA in hypothalamus of mice infected by canine distemper virus [in French]. C R Acad Sci III 1991;313:545-551.
6. Bernard A, Zwingelstein G, Meister R et al. Hyperinsulinemia induced by canine distemper virus infection of mice and its correlation with the appearance of obesity. Comp Biochem Physiol B 1988;91:691-696.
7. Carter JK, Garlich JD, Donaldson WE et al. Influence of diet on a retrovirus-induced obesity and stunting syndrome. Avian Dis 1983;27:317-322.
8. Carter JK, Ow CL, Smith RE. Rous-associated virus type 7 induces a syndrome in chickens characterized by stunting and obesity. Infect Immun 1983;39:410-422.
9. Dhurandhar NV, Israel BA, Kolesar JM et al. Transmissibility of adenovirus-induced adiposity in a chicken model. Int J Obes Relat Metab Disord 2001;25:990-996.
10. Dhurandhar NV, Israel BA, Kolesar JM et al. Increased adiposity in animals due to a human virus. Int J Obes Relat Metab Disord 2000;24:989-996.
11. Dhurandhar NV, Kulkarni P, Ajinkya SM et al. Effect of adenovirus infection on adiposity in chicken. Vet Microbiol 1992;31:101-107.
12. Dhurandhar NV, Kulkarni PR, Ajinkya SM et al. Association of adenovirus infection with human obesity. Obes Res 1997;5:464-469.
13. Dhurandhar NV, Whigham LD, Abbott DH et al. Human adenovirus Ad-36 promotes weight gain in male rhesus and marmoset monkeys. J Nutr 2002;132:3155-3160.
14. Gosztonyi G, Ludwig H. Borna disease - Neuropathology and pathogenesis. Curr Top Microbiol Immunol 1995;190:39-73.
15. Lyons MJ, Faust IM, Hemmes RB et al. A virally induced obesity syndrome in mice. Science 1982;216:82- 85.
16. So PW, Herlihy AH, Bell JD. Adiposity induced by adenovirus 5 inoculation. Int J Obes (Lond) 2005;29:603-606.
17. Atkinson RL, Dhurandhar NV, Allison DB et al. Human adenovirus-36 is associated with increased body weight and paradoxical reduction of serum lipids. Int J Obes (Lond) 2005;29:281-286.
18. Pasarica M, Shin AC, Yu M et al. Human adenovirus 36 induces adiposity, increases insulin sensitivity, and alters hypothalamic monoamines in rats. Obesity 2006;14:1905-1913.
19. Vangipuram SD, Sheele J, Atkinson RL et al. A human adenovirus enhances preadipocyte differentiation. Obes Res 2004;12:770-777.
20. Gimble JM, Guilak F. Differentiation potential of adipose derived adult stem (ADAS) cells. Curr Top Dev Biol 2003;58:137-160.
21. Whigham LD, Israel BA, Atkinson RL. Adipogenic potential of multiple human adenoviruses in vivo and in vitro in animals. Am J Physiol Regul Integr Comp Physiol 2006;290:R190-R194.
22. Halvorsen YC, Wilkison WO, Gimble JM. Adipose-derived stromal cells - Their utility and potential in bone formation. Int J Obes Relat Metab Disord 2000;24:S41-S44.
23. Ramírez-Zacarias JL, Castro-Munozledo F, Kuri-Harcuch W. Quantitation of adipose conversion and triglycerides by staining intracytoplasmic lipids with Oil red O. Histochemistry 1992;97:493-497.
24. Permana PA, Nair S, Lee YH et al. Subcutaneous abdominal preadipocyte differentiation in vitro inversely correlates with central obesity. Am J Physiol Endocrinol Metab 2004;286:E958 -E962.
25. Amedee RG, Dhurandhar NR. Fine-needle aspiration biopsy. Laryngoscope 2001;111:1551-1557.
26. Halvorsen YD, Franklin D, Bond AL et al. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng 2001;7:729-741.
27. Hicok KC, Du Laney TV, Zhou YS et al. Human adipose-derived adult stem cells produce osteoid in vivo. Tissue Eng 2004;10:371-380.
28. Caplan AI. The mesengenic process. Clin Plast Surg 1994;21:429-435.
29. Preiss-Landl K, Zimmermann R, Hammerle G et al. Lipoprotein lipase: The regulation of tissue specific expression and its role in lipid and energy metabolism. Curr Opin Lipidol 2002;13:471-481.
30. Young HE, Mancini ML, Wright RP et al., Reagan CR et al. Mesenchymal stem cells reside within the connective tissues of many organs. Dev Dyn 1995;202:137-144.
31. Yu ZK, Wright JT, Hausman GJ. Preadipocyte recruitment in stromal vascular cultures after depletion of committed preadipocytes by immunocytotoxicity. Obes Res 1997;5:9-15.
32. McIntosh K, Zvonic S, Garrett S et al. The immunogenicity of human adipose-derived cells: Temporal changes in vitro. STEM CELLS 2006;24:1246-1253.
33. Mitchell JB, McIntosh K, Zvonic S et al. Immunophenotype of human adipose-derived cells: Temporal changes in stromal-associated and stem cell-associated markers. STEM CELLS 2006;24:376-385.
34. Guilak F, Lott KE, Awad HA et al. Clonal analysis of the differentiation potential of human adipose-derived adult stem cells. J Cell Physiol 2006;206:229-237.
35. Davis RL, Weintraub H, Lassar AB. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 1987;51:987-1000.
36. Hauner H, Entenmann G, Wabitsch M et al. Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium. J Clin Invest 1989;84:1663-1670.
37. Hauner H, Entenmann G. Regional variation of adipose differentiation in cultured stromal-vascular cells from the abdominal and femoral adipose tissue of obese women. Int J Obes 1991;15:121-126.
38. Hauner H, Wabitsch M, Pfeiffer EF. Differentiation of adipocyte precursor cells from obese and nonobese adult women and from different adipose tissue sites. Horm Metab Res Suppl 1988;19:35-39.
39. Williams LB, Fawcett RL, Waechter AS et al. Leptin production in adipocytes from morbidly obese subjects: Stimulation by dexamethasone, inhibition with troglitazone, and influence of gender. J Clin Endocrinol Metab 2000;85:2678-2684.
40. Orlicky DJ, DeGregori J, Schaack J. Construction of stable coxsackievirus and adenovirus receptor-expressing 3T3-L1 cells. J Lipid Res 2001;42:910-915.
41. McBeath R, Pirone DM, Nelson CM et al. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 2004;6:483-495.
42. Gregoire FM, Smas CM, Sul HS. Understanding adipocyte differentiation. Physiol Rev 1998;78:783-809.
43. Farmer SR. Regulation of PPARgamma activity during adipogenesis. Int J Obes (Lond) 2005;29:S13-S16.
44. Ntambi JM, Young-Cheul K. Adipocyte differentiation and gene expression. J Nutr 2000;130:3122S-3126S.
45. Tchoukalova YD, Sarr MG, Jensen MD. Measuring committed preadipocytes in human adipose tissue from severely obese patients by using adipocyte fatty acid binding protein. Am J Physiol Regul Integr Comp Physiol 2004;287:R1132-R1140.
46. Goldberg IJ, Merkel M. Lipoprotein lipase: Physiology, biochemistry, and molecular biology. Front Biosci 2001;6:D388-D405.
47. Kageyama H, Hirano T, Okada K et al. Lipoprotein lipase mRNA in white adipose tissue but not in skeletal muscle is increased by pioglitazone through PPAR-gamma. Biochem Biophys Res Commun 2003;305:22-27.
48. Kumar S, Boulton AJ, Beck-Nielsen H et al. Troglitazone, an insulin action enhancer, improves metabolic control in NIDDM patients. Troglitazone Study Group. Diabetologia 1996;39:701-709.
49. Miyazaki Y, Glass L, Triplitt C et al. Effect of rosiglitazone on glucose and non-esterified fatty acid metabolism in Type II diabetic patients. Diabetologia 2001;44:2210 -2219.
50. Dubois S, Halvorsen Y, Ravussin E et al. Primary stromal cell culture from adipose tissue: From liposuction to needle biopsy. Adipocytes 2005;1:139-144.
51. Otto TC, Lane MD. Adipose development: From stem cell to adipocyte. Crit Rev Biochem Mol Biol 2005;40:229 -242.