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Human adenovirus-36 is associated with increased body weight and paradoxical reduction of serum lipids

Abstract

BACKGROUND:

Human adenovirus-36 (Ad-36) increases adiposity and paradoxically lowers serum cholesterol and triglycerides in chickens, mice, and non-human primates. The role of Ad-36 in human obesity is unknown.

OBJECTIVES:

To determine the prevalence of Ad-36 antibodies in obese and nonobese humans. To evaluate the association of Ad-36 antibodies with body mass index (BMI) and serum lipids.

DESIGN:

Cohort study. Volunteers from obesity treatment programs, communities, and a research study.

SUBJECTS:

Obese and nonobese volunteers at the University of Wisconsin, Madison, WI, and the Bowen Center, Naples, Florida. Obese and thin volunteer research subjects and 89 twin pairs at Columbia University, New York.

INTERVENTIONS:

Study 1: 502 subjects; serum neutralization assay for antibodies to Ad-2, Ad-31, Ad-36, and Ad-37; serum cholesterol and triglycerides assays. Study 2: BMI and %body fat in 28 twin pairs discordant for Ad-36 antibodies.

MAIN OUTCOME MEASURES:

Presence of antibodies to adenoviruses, BMI, serum cholesterol and triglycerides levels.

RESULTS:

Significant (P<0.001) association of obesity and positive Ad-36 antibody status, independent of age, sex, and collection site. Ad-36 antibodies in 30% of obese, 11% of nonobese. Lower serum cholesterol and triglycerides (P<0.003) in Ad-36 antibody-positive vs -negative subjects. Twin pairs: antibody-positive twins had higher BMIs (24.5±5.2 vs 23.1±4.5 kg/m2, P<0.03) and %body fat (29.6±9.5% vs 27.5±9.9%, P<0.04). No association of Ad-2, Ad-31, or Ad-37 antibodies with BMI or serum lipids.

CONCLUSIONS:

Ad-36 is associated with increased body weight and lower serum lipids in humans. Prospective studies are indicated to determine if Ad-36 plays a role in the etiology of human obesity.

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References

  1. Lyons MJ, Faust IM, Hemmes RB, Buskirk DR, Hirsch J, Zabriskie JB . A virally induced obesity syndrome in mice. Science 1982; 216: 82–85.

    CAS  Article  Google Scholar 

  2. Bernard A, Zwingelstein G, Meister R, Fabian Wild T . Hyperinsulinemia induced by canine distemper virus infection of mice and its correlation with the appearance of obesity. Comp Biochem Physiol 1988; 91B: 691–696.

    CAS  Google Scholar 

  3. Bernard A, Fevre-Montange M, Giraudon P, Hardin H, Fabian Wild T, Belin MF . Localization of viral proteins and RNA in hypothalamus of mice infected by canine distemper virus (French). Virology 1991; 313: 545–551.

    CAS  Google Scholar 

  4. Bernard A, Fevre-Montange M, Bencsik A, Giraudon P, Fabian Wild T, Confavreux C, Belin MF . Brain structures selectively targeted by canine distemper virus in a mouse model infection. J Neuropathol Exp Neurol 1993; 52: 471–480.

    CAS  Article  Google Scholar 

  5. Nagashima K, Zabriskie JB, Lyons MJ . Virus induced obesity in mice. Association with a hypothalamic lesion. J Neuropathol Exp Neurol 1992; 51: 101–109.

    CAS  Article  Google Scholar 

  6. Carter JK, Ow CL, Smith RE . Rous-Associated virus type 7 induces a syndrome in chickens characterized by stunting and obesity. Infection Immunity 1983; 39: 410–422.

    CAS  PubMed  Google Scholar 

  7. Carter JK, Garlich JD, Donaldson WT, Smith RE . Influence of diet on a retrovirus induced obesity and stunting syndrome. Avian Dis 1983; 27: 317–322.

    CAS  Article  Google Scholar 

  8. Gosztonyi G, Ludwig H . Borna disease: neuropathology and pathogenesis. Curr Topics Microbiol Immunol 1995; 190: 39–73.

    CAS  Google Scholar 

  9. Carp RI, Meeker H, Sersen E, Kozlowski P . Analysis of the incubation periods, induction of obesity and histopathological changes in senescence-prone and senescence-resistant mice infected with various scrapie strains. J Gen Virol 1988; 79: 2863–2869.

    Article  Google Scholar 

  10. Dhurandhar NV, Kulkarni PR, Ajinkya SM, Sherikar AA . Avian adenovirus leading to pathognomic obesity in chickens. J Bombay Vet College 1990; 2: 131–132.

    Google Scholar 

  11. Dhurandhar NV, Kulkarni PR, Ajinkya SM, Sherikar AA . Effect of adenovirus infection on adiposity in chickens. Vet Microbiol 1992; 31: 101–107.

    CAS  Article  Google Scholar 

  12. Dhurandhar NV, Kulkarni PR, Ajinkja SM, Sherikar AA, Atkinson RL . Association of adenovirus infection with human obesity. Obes Res 1997; 5: 464–469.

    CAS  Article  Google Scholar 

  13. Dhurandhar NV, Israel BA, Kolesar JM, Cook ME, Atkinson RL . Increased adiposity in animals due to a human virus. Int J Obes Relat Metab Disord 2000; 24: 989–996.

    CAS  Article  Google Scholar 

  14. Dhurandhar NV, Israel BA, Kolesar JM, Mayhew G, Cook ME, Atkinson RL . Transmissibility of adenovirus-induced adiposity in a chicken model. Int J Obes Relat Metab Disord 2001; 25: 990-–996.

    CAS  Article  Google Scholar 

  15. Dhurandhar NV, Whigham LD, Abbott DH, Schultz-Darken NJ, Israel BA, Bradley SM, Kemnitz JW, Allison DB, Atkinson RL . Human adenovirus Ad-36 promotes weight gain in male rhesus and marmoset monkeys. J Nutr 2002; 132: 3155-–3160.

    CAS  Article  Google Scholar 

  16. Preventing and managing the global epidemic of obesity: report of a WHO Consultation on Obesity. Geneva, 3–5 June, 1997. WHO/NUT/NCD98.1, Geneva; 1998.

  17. Box GEP, Cox DR . J Roy Stat Soc Series B 1964; 26: 211.

  18. Simo Minana J, Gaztambide Ganuza M, Fernandez Millan P, Pena Fernandez M . Hepatitis B vaccine immunoresponsiveness in adolescents: a revaccination proposal after primary vaccination. Vaccine 1996; 14: 103–106.

    CAS  Article  Google Scholar 

  19. Bouchard C, Tremblay A, Depres JP, Nadeau A, Lupien PJ, Theriault G, Dussault J, Moorjani S, Pinault S, Fournier G . The response to long-term overfeeding in identical twins. N Engl J Med 1990; 322: 1477–1482.

    CAS  Article  Google Scholar 

  20. Bouchard C, Tremblay A, Despres JP, Theriault G, Nadeau A, Lupien PJ, Moorjani S, Prudhomme D, Fournier G . The response to exercise with constant energy intake in identical twins. Obes Res 1994; 2: 400–410.

    CAS  Article  Google Scholar 

  21. Bouchard C, Perusse L, Rice T, Rao DC . The genetics of human obesity. In: Bray GA, Bouchard C, James WPT (eds). Handbook of Obesity. Marcel Dekker, Inc.: New York; 1998. pp 157–190.

    Google Scholar 

  22. Chagnon YC, Pérusse L, Weisnagel SJ, Rankinen T, Bouchard C . The human obesity gene map: the 1999 update. Obes Res 2000; 8: 89–117.

    CAS  Article  Google Scholar 

  23. Wigand R, Gelderblom H, Wadell G . New human adenovirus (candidate adenovirus 36), a novel member of subgroup D. Arch Virology 1980; 64: 225–233.

    CAS  Article  Google Scholar 

  24. Hierholzer JC, Wigand R, Anderson LJ, Adrian T, Gold JWM . Adenoviruses from patients with AIDS: A plethora of serotypes and a description of five new serotypes of subgenus D (Types 43-47). J Infectious Dis 1988; 158: 804–813.

    CAS  Article  Google Scholar 

  25. Vangipuram SD, Sheele J, Atkinson RL, Holland TC, Dhurandhar NV . A human adenovirus enhances preadipocyte differentiation. Obes Res 2004; 12: 770–777.

    CAS  Article  Google Scholar 

  26. Whigham LD, Dhurandhar NV, Abbott DH, Schultz-Darken N, Israel BA, Kolesar JM, Strasheim A, Atkinson RL . Presence of obesity-associated human adenovirus-36 DNA in tissues of marmosets and humans. FASEB J 2001; 15: A300 (abstract).

    Article  Google Scholar 

  27. Flegal KM, Carroll MD, Ogden CL, Johnson, CL . Prevalence and trends in obesity among US adults, 1999–2000. JAMA 2002; 288: 1723–1727.

    Article  Google Scholar 

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Acknowledgements

We gratefully acknowledge Geoffrey Letchworth and Lisa Krugner-Higby for advice on virological aspects; Sharon Gathright, Tami Wolden-Hanson, Kathleen Taylor, Wenyen Zhang, and Alexis Strasheim for laboratory assistance; Chris Mullinax for data entry and analysis; and Virginia Schmidt for secretarial assistance. The work was supported by funds from the Wisconsin Alumni Research Foundation's Beers-Murphy Clinical Nutrition Center, and in part by NIH Grants RO1-DK52227 and R01-56277.

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Correspondence to R L Atkinson.

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Atkinson, R., Dhurandhar, N., Allison, D. et al. Human adenovirus-36 is associated with increased body weight and paradoxical reduction of serum lipids. Int J Obes 29, 281–286 (2005). https://doi.org/10.1038/sj.ijo.0802830

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  • DOI: https://doi.org/10.1038/sj.ijo.0802830

Keywords

  • body mass index
  • etiology
  • serum cholesterol
  • serum triglycerides
  • twins
  • viral antibodies

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