Adenovirus infection results in alterations of insulin signaling and glucose homeostasis

American Journal of Physiology - Endocrinology and Metabolism

Volumn 298, Issue 6, 2010, Pages

  Jiang, Shaoning ^a   Gavrikova, Tatyana A ^a   Pereboev, Alexander ^b   Messina, Joseph L ^a,c  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^c BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

Insulin receptor; Insulin receptor substrates; Kupffer cells; Liver; Tumor necrosis factor

Indexed keywords

ADENOVIRUS VECTOR; GLUCOSE; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; INSULIN RECEPTOR SUBSTRATE 2; PHOSPHATIDYLINOSITOL 3 KINASE;

ADENOVIRUS INFECTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; INSULIN RESISTANCE; KUPFFER CELL; LIVER; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADENOVIRIDAE; ADENOVIRIDAE INFECTIONS; ANIMALS; BLOTTING, WESTERN; GENETIC VECTORS; GLUCOSE; GLUCOSE TOLERANCE TEST; IMMUNOHISTOCHEMISTRY; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; KUPFFER CELLS; LIVER; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, INSULIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77952634044     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00723.2009     Document Type: Article

References (48)

1. Anderson RD, Haskell RE, Xia H, Roessler BJ, Davidson BL. A simple method for the rapid generation of recombinant adenovirus vectors. Gene Ther 7: 1034-1038, 2000.
2. Aytug S, Reich D, Sapiro LE, Bernstein D, Begum N. Impaired IRS-1/PI3-kinase signaling in patients with HCV: a mechanism for increased prevalence of type 2 diabetes. Hepatology 38: 1384-1392, 2003.
3. Barba G, Harper F, Harada T, Kohara M, Goulinet S, Matsuura Y, Eder G, Schaff Z, Chapman MJ, Miyamura T, Brechot C. Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci USA 94: 1200-1205, 1997.
4. Boura-Halfon S, Zick Y. Phosphorylation of IRS proteins, insulin action, and insulin resistance. Am J Physiol Endocrinol Metab 296: E581-E591, 2009.
5. Cheung AT, Ree D, Kolls JK, Fuselier J, Coy DH, Bryer-Ash M. An in vivo model for elucidation of the mechanism of tumor necrosis factor-alpha (TNF-alpha)-induced insulin resistance: evidence for differential regulation of insulin signaling by TNF-alpha. Endocrinology 139: 4928-4935, 1998.
6. de Luca C, Olefsky JM. Inflammation and insulin resistance. FEBS Lett 582: 97-105, 2008.
7. Dhurandhar NV. Infectobesity: obesity of infectious origin. J Nutr 131: 2794S-2797S, 2001.
8. Hardonk MJ, Dijkhuis FW, Hulstaert CE, Koudstaal J. Heterogeneity of rat liver and spleen macrophages in gadolinium chloride-induced elimination and repopulation. J Leukoc Biol 52: 296-302, 1992.
9. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 271: 665-668, 1996.
10. Ishizuka K, Usui I, Kanatani Y, Bukhari A, He J, Fujisaka S, Yamazaki Y, Suzuki H, Hiratani K, Ishiki M, Iwata M, Urakaze M, Haruta T, Kobayashi M. Chronic tumor necrosis factor-alpha treatment causes insulin resistance via insulin receptor substrate-1 serine phosphorylation and suppressor of cytokine signaling-3 induction in 3T3-L1 adipocytes. Endocrinology 148: 2994-3003, 2007.
11. Kawaguchi T, Yoshida T, Harada M, Hisamoto T, Nagao Y, Ide T, Taniguchi E, Kumemura H, Hanada S, Maeyama M, Baba S, Koga H, Kumashiro R, Ueno T, Ogata H, Yoshimura A, Sata M. Hepatitis C virus down-regulates insulin receptor substrates 1 and 2 through upregulation of suppressor of cytokine signaling 3. Am J Pathol 165: 1499-1508, 2004.
12. Knobler H, Zhornicky T, Sandler A, Haran N, Ashur Y, Schattner A. Tumor necrosis factor-alpha-induced insulin resistance may mediate the hepatitis C virus-diabetes association. Am J Gastroenterol 98: 2751-2756, 2003. (Pubitemid 38020119)
13. Kolls J, Peppel K, Silva M, Beutler B. Prolonged and effective blockade of tumor necrosis factor activity through adenovirus-mediated gene transfer. Proc Natl Acad Sci USA 91: 215-219, 1994. (Pubitemid 24018674)
14. Kumar M, Choudhury A, Manglik N, Hissar S, Rastogi A, Sakhuja P, Sarin SK. Insulin resistance in chronic hepatitis B virus infection. Am J Gastroenterol 104: 76-82, 2009.
15. Lebrun P, Van Obberghen E. SOCS proteins causing trouble in insulin action. Acta Physiol (Oxf) 192: 29-36, 2008.
16. Li L, Thompson LH, Zhao L, Messina JL. Tissue specific difference in the molecular mechanisms for the development of acute insulin resistance following injury. Endocrinology 150: 24-32, 2009.
17. Lieber A, He CY, Meuse L, Schowalter D, Kirillova I, Winther B, Kay MA. The role of Kupffer cell activation and viral gene expression in early liver toxicity after infusion of recombinant adenovirus vectors. J Virol 71: 8798-8807, 1997. (Pubitemid 27446464)
18. Liu Q, Muruve DA. Molecular basis of the inflammatory response to adenovirus vectors. Gene Ther 10: 935-940, 2003. (Pubitemid 36722427)
19. Liu Q, Zaiss AK, Colarusso P, Patel K, Haljan G, Wickham TJ, Muruve DA. The role of capsid-endothelial interactions in the innate immune response to adenovirus vectors. Hum Gene Ther 14: 627-643, 2003. (Pubitemid 36543435)
20. Lonardo A, Loria P, Carulli N. Dysmetabolic changes associated with HCV: a distinct syndrome? Intern Emerg Med 3: 99-108, 2008.
21. Ma Y, Toth B, Keeton AB, Holland LT, Chaudry IH, Messina JL. Mechanisms of hemorrhage-induced hepatic insulin resistance: role of tumor necrosis factor-alpha. Endocrinology 145: 5168-5176, 2004. (Pubitemid 39551138)
22. Ma Y, Wang P, Kuebler JF, Chaudry IH, Messina JL. Hemorrhage induces the rapid development of hepatic insulin resistance. Am J Physiol Gastrointest Liver Physiol 284: G107-G115, 2003.
23. Marette A. Molecular mechanisms of inflammation in obesity-linked insulin resistance. Int J Obes Relat Metab Disord 27, Suppl 3: S46-S48, 2003.
24. Marshall E. Gene therapy death prompts review of adenovirus vector. Science 286: 2244-2245, 1999. (Pubitemid 30016842)
25. Michael MD, Kulkarni RN, Postic C, Previs SF, Shulman GI, Magnuson MA, Kahn CR. Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell 6: 87-97, 2000.
26. Miller-Jensen K, Janes KA, Wong YL, Griffith LG, Lauffenburger DA. Adenoviral vector saturates Akt pro-survival signaling and blocks insulin-mediated rescue of tumor necrosis-factor-induced apoptosis. J Cell Sci 119: 3788-3798, 2006.
27. Moriya K, Yotsuyanagi H, Shintani Y, Fujie H, Ishibashi K, Matsuura Y, Miyamura T, Koike K. Hepatitis C virus core protein induces hepatic steatosis in transgenic mice. J Gen Virol 78 (Pt 7): 1527-1531, 1997.
28. Muruve DA. The innate immune response to adenovirus vectors. Hum Gene Ther 15: 1157-1166, 2004.
29. Muruve DA, Barnes MJ, Stillman IE, Libermann TA. Adenoviral gene therapy leads to rapid induction of multiple chemokines and acute neutrophil-dependent hepatic injury in vivo. Hum Gene Ther 10: 965-976, 1999.
30. Nakatani Y, Kaneto H, Kawamori D, Hatazaki M, Miyatsuka T, Matsuoka TA, Kajimoto Y, Matsuhisa M, Yamasaki Y, Hori M. Modulation of the JNK pathway in liver affects insulin resistance status. J Biol Chem 279: 45803-45809, 2004.
31. Parker AL, Nicklin SA, Baker AH. Interactions of adenovirus vectors with blood: implications for intravascular gene therapy applications. Curr Opin Mol Ther 10: 439-448, 2008.
32. Rui L, Yuan M, Frantz D, Shoelson S, White MF. SOCS-1 and SOCS-3 block insulin signaling by ubiquitin-mediated degradation of IRS-1 and IRS-2. J Biol Chem 277: 42394-42398, 2002.
33. Schiedner G, Bloch W, Hertel S, Johnston M, Molojavyi A, Dries V, Varga G, van Rooijen N, Kochanek S. A hemodynamic response to intravenous adenovirus vector particles is caused by systemic Kupffer cell-mediated activation of endothelial cells. Hum Gene Ther 14: 1631-1641, 2003.
34. Shayakhmetov DM, Li ZY, Ni S, Lieber A. Analysis of adenovirus sequestration in the liver, transduction of hepatic cells, and innate toxicity after injection of fiber-modified vectors. J Virol 78: 5368-5381, 2004.
35. Sheikh MY, Choi J, Qadri I, Friedman JE, Sanyal AJ. Hepatitis C virus infection: molecular pathways to metabolic syndrome. Hepatology 47: 2127-2133, 2008.
36. So PW, Herlihy AH, Bell JD. Adiposity induced by adenovirus 5 inoculation. Int J Obes (Lond) 29: 603-606, 2005.
37. Taniguchi CM, Emanuelli B, Kahn CR. Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7: 85-96, 2006.
38. Thirone AC, Huang C, Klip A. Tissue-specific roles of IRS proteins in insulin signaling and glucose transport. Trends Endocrinol Metab 17: 72-78, 2006.
39. Thomas CE, Ehrhardt A, Kay MA. Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet 4: 346-358, 2003.
40. Valverde AM, Burks DJ, Fabregat I, Fisher TL, Carretero J, White MF, Benito M. Molecular mechanisms of insulin resistance in IRS-2-deficient hepatocytes. Diabetes 52: 2239-2248, 2003.
41. Vorburger SA, Hunt KK. Adenoviral gene therapy. Oncologist 7: 46-59, 2002.
42. Wang CC, Hsu CS, Liu CJ, Kao JH, Chen DS. Association of chronic hepatitis B virus infection with insulin resistance and hepatic steatosis. J Gastroenterol Hepatol 23: 779-782, 2008.
43. White MF. IRS proteins and the common path to diabetes. Am J Physiol Endocrinol Metab 283: E413-E422, 2002.
44. Wilson JM. Adenoviruses as gene-delivery vehicles. N Engl J Med 334: 1185-1187, 1996.
45. Wolff G, Worgall S, van RN, Song WR, Harvey BG, Crystal RG. Enhancement of in vivo adenovirus-mediated gene transfer and expression by prior depletion of tissue macrophages in the target organ. J Virol 71: 624-629, 1997.
46. Xu J, Kim HT, Ma Y, Zhao L, Zhai L, Kokorina N, Wang P, Messina JL. Trauma and hemorrhage-induced acute hepatic insulin resistance: dominant role of tumor necrosis factor (TNF)-alpha. Endocrinology 149: 2369-2382, 2008.
47. Zhang J, Gao Z, Yin J, Quon MJ, Ye J. S6K directly phosphorylates IRS-1 on Ser-270 to promote insulin resistance in response to TNF-(alpha) signaling through IKK2. J Biol Chem 283: 35375-35382, 2008.
48. Zhang Y, Chirmule N, Gao GP, Qian R, Croyle M, Joshi B, Tazelaar J, Wilson JM. Acute cytokine response to systemic adenoviral vectors in mice is mediated by dendritic cells and macrophages. Mol Ther 3: 697-707, 2001.