Adipocytes in both brown and white adipose tissue of adult mice are functionally connected via gap junctions: Implications for Chagas disease

Microbes and Infection

Volumn 16, Issue 11, 2014, Pages 893-901

  Burke, Shoshana ^a   Nagajyothi, Fnu ^a   Thi, Mia M ^a   Hanani, Menachem ^b   Scherer, Philipp E ^c   Tanowitz, Herbert B ^a   Spray, David C ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Adipose tissue; Chagas disease; Connexin43; Gap junctions; Trypanosoma cruzi

Indexed keywords

CONNEXIN 43; HEPTANOL; LUCIFER YELLOW; GJA1 PROTEIN, MOUSE;

ADIPOCYTE; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CELL COMMUNICATION; CHAGAS DISEASE; CONTROLLED STUDY; DOWN REGULATION; GAP JUNCTION; HORMONE RELEASE; IMMUNOHISTOCHEMISTRY; MICROELECTRODE; MOUSE; NONHUMAN; NONSHIVERING THERMOGENESIS; PROTEIN EXPRESSION; UPREGULATION; WESTERN BLOTTING; WHITE ADIPOSE TISSUE; ANIMAL; BROWN ADIPOCYTE; DISEASE MODEL; GENE EXPRESSION PROFILING; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; MALE; PATHOLOGY; PHYSIOLOGY; TRYPANOSOMA CRUZI; WHITE ADIPOCYTE;

MAMMALIA; MUS; PROTOZOA; TRYPANOSOMA CRUZI;

ADIPOCYTES, BROWN; ADIPOCYTES, WHITE; ANIMALS; CELL COMMUNICATION; CHAGAS DISEASE; CONNEXIN 43; DISEASE MODELS, ANIMAL; GAP JUNCTIONS; GENE EXPRESSION PROFILING; HOST-PATHOGEN INTERACTIONS; MALE; MICE; TRYPANOSOMA CRUZI;

EID: 84919445678     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2014.08.006     Document Type: Article

References (43)

1. Spray D.C., Hanstein R., Lopez-Quintero S.V., Stout R.F., Suadicani S.O., Thi M.M. Gap junctions and bystander effects: good samaritans and executioners. Wiley Interdiscip Rev Membr Transp Signal 2013, 2:1-15.
2. Michon L., Nlend Nlend R., Bavamian S., Bischoff L., Boucard N., Caille D., et al. Involvement of gap junctional communication in secretion. Biochim Biophys Acta 2005, 1719:82-101.
3. Halberg N., Wernstedt-Asterholm I., Scherer P.E. The adipocyte as an endocrine cell. Endocrinol Metab Clin North Am 2008, 37:753-768. x-xi.
4. Scherer P.E. Adipose tissue: from lipid storage compartment to endocrine organ. Diabetes 2006, 55:1537-1545.
5. Nedergaard J., Bengtsson T., Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 2007, 293:E444-E452.
6. Linck G., Stoeckel M.E., Porte A., Petrovic A. Demonstration of gap junctions or nexus by lanthanum in the brown fat of the European hamster (Cricetus cricetus). C R Acad Sci Hebd Seances Acad Sci D 1974, 278:87-89.
7. Revel J.P., Sheridan J.D. Electrophysiological and ultrastructural studies of intercellular junctions in brown fat. J Physiol 1968, 194:34P-35P.
8. Sheridan J.D. Electrical coupling between fat cells in newt fat body and mouse brown fat. J Cell Biol 1971, 50:795-803.
9. Yeganeh A., Stelmack G.L., Fandrich R.R., Halayko A.J., Kardami E., Zahradka P. Connexin 43 phosphorylation and degradation are required for adipogenesis. Biochim Biophys Acta 2012, 1823:1731-1744.
10. Chao L.C., Bensinger S.J., Villanueva C.J., Wroblewski K., Tontonoz P. Inhibition of adipocyte differentiation by Nur77, Nurr1, and Nor1. Mol Endocrinol 2008, 22:2596-2608.
11. Lai-Cheong J.E., Arita K., McGrath J.A. Genetic diseases of junctions. J Invest Dermatol 2007, 127:2713-2725.
12. Adesse D., Goldenberg R.C., Fortes F.S., Jasmin, Iacobas D.A., Iacobas S., et al. Gap junctions and chagas disease. Adv Parasitol 2011, 76:63-81.
13. Campos de Carvalho A.C., Roy C., Hertzberg E.L., Tanowitz H.B., Kessler J.A., Weiss L.M., et al. Gap junction disappearance in astrocytes and leptomeningeal cells as a consequence of protozoan infection. Brain Res 1998, 790:304-314.
14. de Carvalho A.C., Tanowitz H.B., Wittner M., Dermietzel R., Roy C., Hertzberg E.L., et al. Gap junction distribution is altered between cardiac myocytes infected with Trypanosoma cruzi. Circ Res 1992, 70:733-742.
15. Combs T.P., Nagajyothi, Mukherjee S., de Almeida C.J., Jelicks L.A., Schubert W., et al. The adipocyte as an important target cell for Trypanosoma cruzi infection. J Biol Chem 2005, 280:24085-24094.
16. Ferreira A.V., Segatto M., Menezes Z., Macedo A.M., Gelape C., de Oliveira Andrade L., et al. Evidence for Trypanosoma cruzi in adipose tissue in human chronic Chagas disease. Microbes Infect 2011, 13:1002-1005.
17. Nagajyothi F., Machado F.S., Burleigh B.A., Jelicks L.A., Scherer P.E., Mukherjee S., et al. Mechanisms of Trypanosoma cruzi persistence in Chagas disease. Cell Microbiol 2012, 14:634-643.
18. Tanowitz H.B., Jelicks L.A., Machado F.S., Esper L., Qi X., Desruisseaux M.S., et al. Adipose tissue, diabetes and Chagas disease. Adv Parasitol 2011, 76:235-250.
19. Jelicks L.A., Lisanti M.P., Machado F.S., Weiss L.M., Tanowitz H.B., Desruisseaux M.S. Imaging of small-animal models of infectious diseases. Am J Pathol 2013, 182:296-304.
20. Hanani M. Lucifer yellow - an angel rather than the devil. J Cell Mol Med 2012, 16:22-31.
21. Thi M.M., Urban-Maldonado M., Spray D.C., Suadicani S.O. Characterization of hTERT-immortalized osteoblast cell lines generated from wild-type and connexin43-null mouse calvaria. Am J Physiol Cell Physiol 2010, 299:C994-C1006.
22. Yan J., Burman A., Nichols C., Alila L., Showe L.C., Showe M.K., et al. Detection of differential gene expression in brown adipose tissue of hibernating arctic ground squirrels with mouse microarrays. Physiol Genomics 2006, 25:346-353.
23. Yanagiya T., Tanabe A., Hotta K. Gap-junctional communication is required for mitotic clonal expansion during adipogenesis. Obes (Silver Spring) 2007, 15:572-582.
24. Schiller P.C., D'Ippolito G., Brambilla R., Roos B.A., Howard G.A. Inhibition of gap-junctional communication induces the trans-differentiation of osteoblasts to an adipocytic phenotype invitro. J Biol Chem 2001, 276:14133-14138.
25. Umezawa A., Hata J. Expression of gap-junctional protein (connexin 43 or alpha 1 gap junction) is down-regulated at the transcriptional level during adipocyte differentiation of H-1/A marrow stromal cells. Cell Struct Funct 1992, 17:177-184.
26. Revel J.P., Yee A.G., Hudspeth A.J. Gap junctions between electrotonically coupled cells in tissue culture and in brown fat. Proc Natl Acad Sci U S A 1971, 68:2924-2927.
27. Lafontan M. Historical perspectives in fat cell biology: the fat cell as a model for the investigation of hormonal and metabolic pathways. Am J Physiol Cell Physiol 2012, 302:C327-C359.
28. Trayhurn P. Hypoxia and adipose tissue function and dysfunction in obesity. Physiol Rev 2013, 93:1-21.
29. Hazan U., Romero I.A., Cancello R., Valente S., Perrin V., Mariot V., et al. Human adipose cells express CD4, CXCR4, and CCR5 [corrected] receptors: a new target cell type for the immunodeficiency virus-1?. FASEB J 2002, 16:1254-1256.
30. Bechah Y., Paddock C.D., Capo C., Mege J.L., Raoult D. Adipose tissue serves as a reservoir for recrudescent Rickettsia prowazekii infection in a mouse model. PLoS One 2010, 5:e8547.
31. Erol A. Visceral adipose tissue specific persistence of Mycobacterium tuberculosis may be reason for the metabolic syndrome. Med Hypotheses 2008, 71:222-228.
32. Pfenniger A., Chanson M., Kwak B.R. Connexins in atherosclerosis. Biochim Biophys Acta 2013, 1828:157-166.
33. Warwick R.A., Hanani M. The contribution of satellite glial cells to chemotherapy-induced neuropathic pain. Eur J Pain 2013, 17:571-580.
34. Shoemaker J.P., Hoffman R.V. Trypanosoma cruzi: possible stimulatory factor(s) on brown adipose tissue of mice. Exp Parasitol 1974, 35:272-274.
35. Shoemaker J.P., Hoffman R.V., Huffman D.G. Trypanosoma cruzi: preference for brown adipose tissue in mice by the Tulahuen strain. Exp Parasitol 1970, 27:403-407.
36. Nagajyothi F., Desruisseaux M.S., Machado F.S., Upadhya R., Zhao D., Schwartz G.J., et al. Response of adipose tissue to early infection with Trypanosoma cruzi (Brazil strain). J Infect Dis 2012, 205:830-840.
37. Adesse D., Garzoni L.R., Huang H., Tanowitz H.B., de Nazareth Meirelles M., Spray D.C. Trypanosoma cruzi induces changes in cardiac connexin43 expression. Microbes Infect 2008, 10:21-28.
38. Brosnan C.F., Scemes E., Spray D.C. Cytokine regulation of gap junction connectivity - an open-and-shut case or changing partners at the nexus?. Am J Pathol 2001, 158:1565-1569.
39. Duffy H.S., John G.R., Lee S.C., Brosnan C.F., Spray D.C. Reciprocal regulation of the junctional proteins claudin-1 and connexin43 by interleukin-1beta in primary human fetal astrocytes. J Neurosci 2000, 20:RC114.
40. Markoullis K., Sargiannidou I., Schiza N., Hadjisavvas A., Roncaroli F., Reynolds R., et al. Gap junction pathology in multiple sclerosis lesions and normal-appearing white matter. Acta Neuropathol 2012, 123:873-886.
41. Niger C., Howell F.D., Stains J.P. Interleukin-1beta increases gap junctional communication among synovial fibroblasts via the extracellular-signal-regulated kinase pathway. Biol Cell 2010, 102:37-49.
42. Cousin B., Cinti S., Morroni M., Raimbault S., Ricquier D., Penicaud L., et al. Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization. J Cell Sci 1992, 103(Pt 4):931-942.
43. Lee Y.H., Mottillo E.P., Granneman J.G. Adipose tissue plasticity from WAT to BAT and in between. Biochim Biophys Acta 2014, 1842:358-369.