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• W2109584224 abstract "APPETITE, OBESITY, DIGESTION, AND METABOLISMVirus-induced obesityFrank GreenwayFrank GreenwayPublished Online:01 Jan 2006https://doi.org/10.1152/ajpregu.00607.2005MoreSectionsPDF (37 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInEmailWeChat the human adenovirus-36 (Ad-36) was first described in 1980, about the time that the prevalence of obesity began to increase (15). Prevalence of obesity increased by 30% between 1980 and 1990 and by 61% between 1990 and 2000 with no indication that this increase is lessening (12). The reason for this epidemic increase in obesity is not clear, but dietary changes, such as an increase in dietary fructose derived from corn syrup (2), increased food intake (10), and decreased physical activity (11) have all been suggested as potentially playing a role. Infectious agents such as viruses are another possible contributing factor (3).Support for Ad-36 being a contributor to the obesity epidemic has been accumulating over several years. Ad-36 has been shown to cause obesity in chickens, mice, and nonhuman primates (4, 5, 8). Obese humans have a higher prevalence of serum neutralizing antibodies to Ad-36 (30%) than lean humans (11%), and the antibody-positive obese or nonobese subjects are heavier compared with their antibody negative counterparts (1). Similarly, when human twins are discordant for antibodies to Ad-36 antibodies, the antibody-positive twin has a higher body mass index (24.5 ± 5.2 vs. 23.1 ± 4.5 kg/m2, P < 0.03) (1). Obese humans positive for antibodies to SMAM-1, an adipogenic avian virus (6), are heavier compared with their seronegative obese counterparts (7). However, because avian viruses are not thought to infect humans, this observation has been interpreted as a cross-reaction to a human virus that is antigenically similar (7).The mechanism by which Ad-36 causes obesity has been explored. Ad-36 accelerates differentiation of preadipocytes to adipocytes in 3T3-L1 cells, and this has been confirmed in human preadipocytes, as well (14). When the open reading frame E4orf1 from the Ad-36 virus was inserted into 3T3-L1 cells, C/EBP-β, PPARγ-2, and glycerol 3-phosphate dehydrogenase were all stimulated compared with the control 3T3-L1 cells, suggesting that the viral gene E4orf1 is responsible for the stimulation of adipocyte differentiation (9).If Ad-36 is responsible for a significant portion of human obesity, the logical therapeutic intervention would be to develop a vaccine to prevent future infections. If a vaccine were to be developed, one would want to ensure that all the serotypes of human adenoviruses responsible for human obesity were covered in the vaccine. If one could predict the potential of an adenovirus to cause human obesity by using an in vitro assay or even by animal testing, screening of the ∼50 human adenoviruses might be accelerated, shortening the time required for vaccine formulation. The article by Atkinson et al. in this issue of the American Journal of Physiology–Regulatory, Integrative and Comparative Physiology (16), suggests that the increased differentiation of 3T3-L1 cells caused by adenovirus type 31 does not necessarily correlate with the development of obesity in chickens. Furthermore, they report the development of obesity in chickens inoculated with Ad-37, a virus that did not show a correlation with human obesity (16). This observation suggests that the development of obesity in chickens is not necessarily predictive of a human adenovirus causing obesity in humans (16).In addition to Ad-37 causing obesity in chickens, Ad-5 was recently shown to cause obesity in mice (13). Adenovirus Ad-2 does not cause adiposity in animals and does not enhance differentiation of 3T3-L1 or human preadipocytes (14). Ad-37, Ad-31, and Ad-5 have not been tested for increased differentiation in human adipocytes. The experience with Ad-36 suggests that 3T3-L1 cells function as a good model for defining the mechanisms by which human adenoviruses induce obesity in humans, if the virus in question stimulates adipocyte differentiation in human cells. Thus it is possible that human adipocyte differentiation may be a viable in vitro assay to screen for human adenoviruses capable of inducing obesity in humans (Table 1).Antibody testing in humans suggests that the development of obesity in chickens is not an effective screening tool to identify human adenoviruses capable of causing obesity in humans. The prevalence of antibodies to Ad-2 was not different in 145 obese human subjects compared with 52 lean controls. The prevalence of antibodies to Ad-31 in 152 obese human subjects was not different compared with 49 lean controls. Because there were only 5 of 198 people positive for the Ad-37 virus, its role in the etiology of human obesity seems remote, despite its demonstrated ability to cause obesity in chickens. This may be due to a lower potential for this virus to cause infection. Infectivity of Ad-36 was 100% in studies when chickens were inoculated with this virus, because all animals developed antibodies to Ad-36 (5) but only 71% of the chickens inoculated with Ad-37 developed antibodies (16).At this point, it appears that Ad-36 is the only human adenovirus associated with human obesity based on human antibody titers. If virus infections are partially responsible for the human obesity epidemic, it will be important to define all the adenovirus serotypes responsible in formulating a vaccine. Screening of large populations for the differential prevalence of antibodies to all 50 or more human adenoviruses to define those associated with human obesity is a daunting task. Clearly, an in vitro assay would make the screening process much more efficient.The article by Atkinson and colleagues (16) suggests that 3T3-L1 cells are not an adequate in vitro model and that chickens are not an adequate in vivo model for screening adipogenic potential of adenoviruses to induce obesity in humans. Human adipocyte differentiation in vitro may hold promise, because to this point only Ad-36 has been shown to be active in that assay (Table 1).In summary, evidence is accumulating that Ad-36 plays a role in human obesity by stimulation of adipocyte differentiation. Other adenoviruses cause obesity in animals and stimulate 3T3-L1 preadipocyte differentiation, but neither of these findings correlate with the antibody prevalence in obese and lean humans shown with Ad-36. Therefore, human antibody prevalence in obese and lean human populations appears to be the only reliable method to screen adenoviruses for their potential to cause obesity in humans at the present time. An in vitro assay that correlates with human antibody prevalence would accelerate screening of adenovirus serotypes for their potential to induce human obesity. Identifying such an in vitro assay will be important to efficient vaccine development. Table 1. Adenoviruses effects in human and animal modelsVirusAd-36Ad-37Ad-31Ad-2Ad-5Differentiation in 3T3-L1 cellsYesYesYesNo?Obesity in animal modelYesYesNoNoYesDifferentiation in human adipocytesYes??No?Human antibodies higher in obeseYesNoNoNo?Only adenovirus (Ad)-36 has been shown to accelerate differentiation in 3T3-L1 preadipocytes, cause obesity in animal models, accelerate differentiation in human preadipocytes, and have a higher antibody prevalence in obese humans. Other human adenoviruses have the potential to do some of these things, but only Ad-36 has been shown to stimulate human preadipocyte differentiation and have a higher antibody prevalence in obese humans. ?, Unknown.REFERENCES1 Atkinson RL, Dhurandhar NV, Allison DB, Bowen RL, Israel BA, Albu JB, and Augustus AS. Human adenovirus-36 is associated with increased body weight and paradoxical reduction of serum lipids. Int J Obes Relat Metab Disord 29: 281–286, 2005.Crossref | PubMed | ISI | Google Scholar2 Bray GA, Nielsen SJ, and Popkin BM. Consumption of high-fructose corn syrup in beverages may play a role in the epidemic of obesity. Am J Clin Nutr 79: 537–543, 2004.Crossref | PubMed | ISI | Google Scholar3 Dhurandhar N, Atkinson R, and Ahmed A. Obesity of infectious origin–a review. Growth Genet Horm 20: 33–39, 2004.Google Scholar4 Dhurandhar NV, Israel BA, Kolesar JM, Mayhew G, Cook ME, and Atkinson RL. Transmissibility of adenovirus-induced adiposity in a chicken model. Int J Obes Relat Metab Disord 25: 990–996, 2001.Crossref | PubMed | ISI | Google Scholar5 Dhurandhar NV, Israel BA, Kolesar JM, Mayhew GF, Cook ME, and Atkinson RL. Increased adiposity in animals due to a human virus. Int J Obes Relat Metab Disord 24: 989–996, 2000.Crossref | PubMed | ISI | Google Scholar6 Dhurandhar NV, Kulkarni P, Ajinkya SM, and Sherikar A. Effect of adenovirus infection on adiposity in chicken. Vet Microbiol 31: 101–107, 1992.Crossref | PubMed | ISI | Google Scholar7 Dhurandhar NV, Kulkarni PR, Ajinkya SM, Sherikar AA, and Atkinson RL. Association of adenovirus infection with human obesity. Obes Res 5: 464–469, 1997.Crossref | PubMed | Google Scholar8 Dhurandhar NV, Whigham LD, Abbott DH, Schultz-Darken NJ, Israel BA, Bradley SM, Kemnitz JW, Allison DB, and Atkinson RL. Human adenovirus Ad-36 promotes weight gain in male rhesus and marmoset monkeys. J Nutr 132: 3155–3160, 2002.Crossref | PubMed | ISI | Google Scholar9 Fusinski K, Shaw M, and Leff T. Adenovirus-36 transcription factor E4orf1 accelerates preadipocyte differentiation (Abstract). Obes Res 12, Suppl: A2, 2004.Google Scholar10 Goldberg JP, Belury MA, Elam P, Finn SC, Hayes D, Lyle R, St Jeor S, Warren M, and Hellwig JP. The obesity crisis: don't blame it on the pyramid. J Am Diet Assoc 104: 1141–1147, 2004.Crossref | PubMed | Google Scholar11 Hill JO and Wyatt HR. Role of physical activity in preventing and treating obesity. J Appl Physiol 99: 765–770, 2005.Link | ISI | Google Scholar12 Mokdad AH, Bowman BA, Ford ES, Vinicor F, Marks JS, and Koplan JP. The continuing epidemics of obesity and diabetes in the United States. JAMA 286: 1195–1200, 2001.Crossref | PubMed | ISI | Google Scholar13 So PW, Herlihy AH, and Bell JD. Adiposity induced by adenovirus 5 inoculation. Int J Obes Relat Metab Disord 29: 603–606, 2005.Crossref | PubMed | ISI | Google Scholar14 Vangipuram SD, Sheele J, Atkinson RL, Holland TC, and Dhurandhar NV. A human adenovirus enhances preadipocyte differentiation. Obes Res 12: 770–777, 2004.Crossref | PubMed | Google Scholar15 Wigand R, Gelderblom H, and Wadell G. New human adenovirus (candidate adenovirus 36), a novel member of subgroup D. Arch Virol 64: 225–233, 1980.Crossref | PubMed | ISI | Google Scholar16 Whigham LD, Israel BA, and Atkinson RL. Adipogenic potential of multiple human adenoviruses in vivo and in vitro in animals. Am J Physiol Regul Integr Comp Physiol 290: R190–R194, 2006.Link | ISI | Google ScholarAUTHOR NOTESAddress for reprint requests and other correspondence: F. Greenway, Louisiana State Univ., Pennington Biomedical Research Center, Baton Rouge, LA (e-mail: [email protected]) Download PDF Previous Back to Top Next FiguresReferencesRelatedInformationCited ByEffects of Taenia Pisiformis Infection and Obesity on Clinical Parameters, Organometry and Fat Distribution in Male Rabbits22 October 2020 | Pathogens, Vol. 9, No. 11Viral Manipulation of the Host Metabolic Network7 April 2018Infectobesity: the evaluation of adenovirus-36 infection and obesityFuture Virology, Vol. 11, No. 4The relationship between adenovirus-36 seropositivity, obesity and metabolic profile in Turkish children and adults16 April 2015 | Epidemiology and Infection, Vol. 143, No. 16Gene expression profile in human skeletal muscle cells infected with human adenovirus type 3618 June 2012 | Journal of Medical Virology, Vol. 84, No. 8Adenovirus 36 as an Obesity Agent Maintains the Obesity State by Increasing MCP-1 and Inducing Inflammation24 January 2012 | The Journal of Infectious Diseases, Vol. 205, No. 6Adenovirus-36 Seropositivity Enhances Effects of Nutritional Intervention on Obesity, Bright Liver, and Insulin Resistance28 September 2011 | Digestive Diseases and Sciences, Vol. 57, No. 2Association of human adenovirus-36 in overweight Korean adults17 May 2011 | International Journal of Obesity, Vol. 36, No. 2Infectobesity: a New Area for Microbiological and Virological ResearchJournal of Bacteriology and Virology, Vol. 41, No. 2Human adenovirus 36 decreases fatty acid oxidation and increases de novo lipogenesis in primary cultured human skeletal muscle cells by promoting Cidec/FSP27 expression4 May 2010 | International Journal of Obesity, Vol. 34, No. 9Ad36 adipogenic adenovirus in human non-alcoholic fatty liver diseaseLiver International, Vol. 30, No. 2Human obesity relationship with Ad36 adenovirus and insulin resistance29 September 2009 | International Journal of Obesity, Vol. 33, No. 12Factors that may impede the weight loss response to exercise-based interventionsObesity Reviews, Vol. 10, No. 6Infeccions as the etiology for obesityArquivos Brasileiros de Endocrinologia & Metabologia, Vol. 53, No. 2Lipodystrophy in HIV 1-infected patients: lessons for obesity research24 July 2007 | International Journal of Obesity, Vol. 31, No. 12Viruses as an Etiology of ObesityMayo Clinic Proceedings, Vol. 82, No. 10Adipocyte, Adipose Tissue, and Infectious DiseaseInfection and Immunity, Vol. 75, No. 3Burden of Infection and Fat Mass in Healthy Middle-aged MenObesity, Vol. 15, No. 1Viral mRNA expression but not DNA replication is required for lipogenic effect of human adenovirus Ad-36 in preadipocytes2 May 2006 | International Journal of Obesity, Vol. 31, No. 1Waterborne Adenovirus More from this issue > Volume 290Issue 1January 2006Pages R188-R189 Copyright & PermissionsCopyright © 2006 the American Physiological Societyhttps://doi.org/10.1152/ajpregu.00607.2005PubMed16352860History Published online 1 January 2006 Published in print 1 January 2006 Metrics" @default.
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