Mouse strains to study cold-inducible beige progenitors and beige adipocyte formation and function

Nature Communications

Volumn 7, Issue , 2016, Pages

  Berry, Daniel C ^a,b   Jiang, Yuwei ^a,b   Graff, Jonathan M ^a,b  

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

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

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE;

BIOENERGETICS; BLOOD; BODY TEMPERATURE; CELLS AND CELL COMPONENTS; GENETIC ENGINEERING; GLUCOSE; MUSCLE; RODENT;

ADIPOCYTE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BEIGE ADIPOCYTE; BEIGE PROGENITOR CELL; BODY TEMPERATURE; CELL FATE; CELL LINEAGE; COLD; CONTROLLED STUDY; GENETIC ENGINEERING; HYPERGLYCEMIA; INGUINAL FAT; MALE; MOUSE; MOUSE STRAIN; MUSCLE CELL; NONHUMAN; PERICYTE; ROOM TEMPERATURE; STEM CELL; SUBCUTANEOUS FAT; WHITE ADIPOCYTE; ANIMAL; BLOOD VESSEL; CELL CULTURE; CLASSIFICATION; CYTOLOGY; GENE EXPRESSION REGULATION; INBRED MOUSE STRAIN; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE;

MUS;

ADIPOCYTES; ANIMALS; BLOOD VESSELS; CELLS, CULTURED; COLD TEMPERATURE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, INBRED STRAINS; MUSCLE, SKELETAL;

EID: 84953212703     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10184     Document Type: Article

References (62)

1. Harms, M. & Seale, P. Brown and beige fat: development, function and therapeutic potential. Nat. Med. 19, 1252-1263 (2013).
2. Yoneshiro, T. et al. Brown adipose tissue, whole-body energy expenditure, and thermogenesis in healthy adult men. Obesity (Silver Spring) 19, 13-16 (2011).
3. Boucher, P., Gotthardt, M., Li, W. P., Anderson, R. G. & Herz, J. LRP: role in vascular wall integrity and protection from atherosclerosis. Science 300, 329-332 (2003).
4. Lidell, M. E., Betz, M. J. & Enerback, S. Brown adipose tissue and its therapeutic potential. J. Intern. Med. 276, 364-377 (2014).
5. Barbatelli, G. et al. The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. Am. J. Physiol. Endocrinol. Metab. 298, E1244-E1253 (2010).
6. Smorlesi, A., Frontini, A., Giordano, A. & Cinti, S. The adipose organ: white-brown adipocyte plasticity and metabolic inflammation. Obes. Rev. 13 Suppl 2 83-96 (2012).
7. Lee, Y. H., Petkova, A. P., Konkar, A. A. & Granneman, J. G. Cellular origins of cold-induced brown adipocytes in adult mice. FASEB J. 29, 286-299 (2015).
8. Wang, Q. A., Tao, C., Gupta, R. K. & Scherer, P. E. Tracking adipogenesis during white adipose tissue development, expansion and regeneration. Nat. Med. 19, 1338-1344 (2013).
9. Sanchez-Gurmaches, J. et al. PTEN loss in the Myf5 lineage redistributes body fat and reveals subsets of white adipocytes that arise from Myf5 precursors. Cell Metab. 16, 348-362 (2012).
10. Kajimura, S., Spiegelman, B. M. & Seale, P. Brown and beige fat: physiological roles beyond heat generation. Cell Metab. 22, 546-559 (2015).
11. Long, J. Z. et al. A smooth muscle-like origin for beige adipocytes. Cell Metab. 19, 810-820 (2014).
12. Lee, Y. H., Petkova, A. P., Mottillo, E. P. & Granneman, J. G. In vivo identification of bipotential adipocyte progenitors recruited by beta3-adrenoceptor activation and high-fat feeding. Cell Metab. 15, 480-491 (2012).
13. Tang, W. et al. White fat progenitor cells reside in the adipose vasculature. Science 322, 583-586 (2008).
14. Jiang, Y., Berry, D. C., Tang, W. & Graff, J. M. Independent stem cell lineages regulate adipose organogenesis and adipose homeostasis. Cell Rep. 9, 1007-1022 (2014).
15. Sidossis, L. & Kajimura, S. Brown and beige fat in humans: thermogenic adipocytes that control energy and glucose homeostasis. J. Clin. Invest. 125, 478-486 (2015).
16. Roy, E., Neufeld, Z., Livet, J. & Khosrotehrani, K. Concise review: understanding clonal dynamics in homeostasis and injury through multicolor lineage tracing. Stem Cells 32, 3046-3054 (2014).
17. Magnuson, M. A. & Osipovich, A. B. Pancreas-specific Cre driver lines and considerations for their prudent use. Cell Metab. 18, 9-20 (2013).
18. Comai, G., Sambasivan, R., Gopalakrishnan, S. & Tajbakhsh, S. Variations in the efficiency of lineage marking and ablation confound distinctions between myogenic cell populations. Dev. Cell 31, 654-667 (2014).
19. Feil, R., Wagner, J., Metzger, D. & Chambon, P. Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem. Biophys. Res. Commun. 237, 752-757 (1997).
20. Gossen, M. & Bujard, H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl Acad. Sci. USA 89, 5547-5551 (1992).
21. Wendling, O., Bornert, J. M., Chambon, P. & Metzger, D. Efficient temporally-controlled targeted mutagenesis in smooth muscle cells of the adult mouse. Genesis 47, 14-18 (2009).
22. Imayoshi, I., Sakamoto, M. & Kageyama, R. Genetic methods to identify and manipulate newly born neurons in the adult brain. Front. Neurosci. 5, 64 (2011).
23. Soriano, P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71 (1999).
24. Golozoubova, V. et al. Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold. FASEB J. 15, 2048-2050 (2001).
25. Shabalina, I. G. et al. UCP1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Rep. 5, 1196-1203 (2013).
26. Cohen, P. et al. Ablation of PRDM16 and beige adipose causes metabolic dysfunction and a subcutaneous to visceral fat switch. Cell 156, 304-316 (2014).
27. Tang, W., Zeve, D., Seo, J., Jo, A. Y. & Graff, J. M. Thiazolidinediones regulate adipose lineage dynamics. Cell Metab. 14, 116-122 (2011).
28. Zeve, D. et al. Wnt signaling activation in adipose progenitors promotes insulin-independent muscle glucose uptake. Cell Metab. 15, 492-504 (2012).
29. Holtwick, R. et al. Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc. Natl Acad. Sci. USA 99, 7142-7147 (2002).
30. Zhu, X. et al. Age-dependent fate and lineage restriction of single NG2 cells. Development 138, 745-753 (2011).
31. Armulik, A., Genove, G. & Betsholtz, C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21, 193-215 (2011).
32. Miano, J. M., Cserjesi, P., Ligon, K. L., Periasamy, M. & Olson, E. N. Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embryogenesis. Circ. Res. 75, 803-812 (1994).
33. Owens, G. K., Kumar, M. S. & Wamhoff, B. R. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84, 767-801 (2004).
34. Seale, P. et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature 454, 961-967 (2008).
35. Potthoff, M. J. et al. Regulation of skeletal muscle sarcomere integrity and postnatal muscle function by Mef2c. Mol. Cell. Biol. 27, 8143-8151 (2007).
36. Li, S., Chang, S., Qi, X., Richardson, J. A. & Olson, E. N. Requirement of a myocardin-related transcription factor for development of mammary myoepithelial cells. Mol. Cell. Biol. 26, 5797-5808 (2006).
37. Pringle, N. P., Mudhar, H. S., Collarini, E. J. & Richardson, W. D. PDGF receptors in the rat CNS: during late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development 115, 535-551 (1992).
38. Nedergaard, J. & Cannon, B. The browning of white adipose tissue: some burning issues. Cell Metab. 20, 396-407 (2014).
39. Cannon, B. & Nedergaard, J. Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359 (2004).
40. Nedergaard, J. & Cannon, B. UCP1 mRNA does not produce heat. Biochim. Biophys. Acta 1831, 943-949 (2013).
41. Walden, T. B., Hansen, I. R., Timmons, J. A., Cannon, B. & Nedergaard, J. Recruited versus nonrecruited molecular signatures of brown, 'brite,' and white adipose tissues. Am. J. Physiol. Endocrinol. Metab. 302, E19-E31 (2012).
42. Tallquist, M. D., Weismann, K. E., Hellstrom, M. & Soriano, P. Early myotome specification regulates PDGFA expression and axial skeleton development. Development 127, 5059-5070 (2000).
43. Sanchez-Gurmaches, J. & Guertin, D. A. Adipocytes arise from multiple lineages that are heterogeneously and dynamically distributed. Nat. Commun. 5, 4099 (2014).
44. Ivanova, A. et al. In vivo genetic ablation by Cre-mediated expression of diphtheria toxin fragment A. Genesis 43, 129-135 (2005).
45. Tontonoz, P., Hu, E. & Spiegelman, B. M. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 79, 1147-1156 (1994).
46. Chawla, A., Schwarz, E. J., Dimaculangan, D. D. & Lazar, M. A. Peroxisome proliferator-activated receptor (PPAR) gamma: adipose-predominant expression and induction early in adipocyte differentiation. Endocrinology 135, 798-800 (1994).
47. Tontonoz, P. & Spiegelman, B. M. Fat and beyond: the diverse biology of PPARgamma. Annu. Rev. Biochem. 77, 289-312 (2008).
48. Bartelt, A. & Heeren, J. Adipose tissue browning and metabolic health. Nat. Rev. Endocrinol. 10, 24-36 (2014).
49. Cypess, A. M. et al. Cold but not sympathomimetics activates human brown adipose tissue in vivo. Proc. Natl Acad. Sci. USA 109, 10001-10005 (2012).
50. Cypess, A. M. et al. Activation of human brown adipose tissue by a beta3-adrenergic receptor agonist. Cell Metab. 21, 33-38 (2015).
51. Cohen, P. & Spiegelman, B. M. Brown and beige fat: molecular parts of a thermogenic machine. Diabetes 64, 2346-2351 (2015).
52. Schrauwen, P., van Marken Lichtenbelt, W. D. & Spiegelman, B. M. The future of brown adipose tissues in the treatment of type 2 diabetes. Diabetologia 58, 1704-1707 (2015).
53. Chen, Y. C. et al. Measurement of human brown adipose tissue volume and activity using anatomic MR imaging and functional MR imaging. J. Nucl. Med. 54, 1584-1587 (2013).
54. Cypess, A. M. et al. Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 360, 1509-1517 (2009).
55. Wu, J. et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366-376 (2012).
56. Kajimura, S. & Saito, M. A new era in brown adipose tissue biology: molecular control of brown fat development and energy homeostasis. Annu. Rev. Physiol. 76, 225-249 (2014).
57. Saito, M. Brown adipose tissue as a regulator of energy expenditure and body fat in humans. Diabetes Metab. J. 37, 22-29 (2013).
58. Saito, M. et al. High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58, 1526-1531 (2009).
59. Blondin, D. P. et al. Increased brown adipose tissue oxidative capacity in cold-acclimated humans. J. Clin. Endocrinol. Metab. 99, E438-E446 (2014).
60. Bolte, S. & Cordelieres, F. P. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232 (2006).
61. Berry, D. C. & Noy, N. All-trans-retinoic acid represses obesity and insulin resistance by activating both peroxisome proliferation-activated receptor beta/delta and retinoic acid receptor. Mol. Cell. Biol. 29, 3286-3296 (2009).
62. Li, S. et al. Requirement for serum response factor for skeletal muscle growth and maturation revealed by tissue-specific gene deletion in mice. Proc. Natl Acad. Sci. USA 102, 1082-1087 (2005).