Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-27T13:03:54.018Z Has data issue: false hasContentIssue false
  • English
  • Français

Review: Animal model and the current understanding of molecule dynamics of adipogenesis

Published online by Cambridge University Press:  18 January 2016

C. F. Campos ,
M. S. Duarte ,
S. E. F. Guimarães ,
L. L. Verardo ,
S. Wei ,
M. Du ,
Z. Jiang ,
W. G. Bergen ,
G. J. Hausman  and
M. Fernyhough-Culver
...Show all authors
C. F. Campos*
Affiliation:
Department of Animal Sciences, Universidade Federal de Viçosa, Viçosa, MG 36570-000, Brazil Department of Animal Sciences, Washington State University, Pullman, WA 99164, USA LABTEC-Animal Biotechnology Laboratory, Universidade Federal de Viçosa, Viçosa, MG 36570-000, Brazil
M. S. Duarte
Affiliation:
Department of Animal Sciences, Universidade Federal de Viçosa, Viçosa, MG 36570-000, Brazil LABTEC-Animal Biotechnology Laboratory, Universidade Federal de Viçosa, Viçosa, MG 36570-000, Brazil
S. E. F. Guimarães
Affiliation:
Department of Animal Sciences, Universidade Federal de Viçosa, Viçosa, MG 36570-000, Brazil LABTEC-Animal Biotechnology Laboratory, Universidade Federal de Viçosa, Viçosa, MG 36570-000, Brazil
L. L. Verardo
Affiliation:
Department of Animal Sciences, Universidade Federal de Viçosa, Viçosa, MG 36570-000, Brazil LABTEC-Animal Biotechnology Laboratory, Universidade Federal de Viçosa, Viçosa, MG 36570-000, Brazil
S. Wei
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, PR China
M. Du
Affiliation:
Department of Animal Sciences, Washington State University, Pullman, WA 99164, USA
Z. Jiang
Affiliation:
Department of Animal Sciences, Washington State University, Pullman, WA 99164, USA
W. G. Bergen
Affiliation:
Department of Animal Sciences, Auburn University, Auburn, AL 36849-5415, USA
G. J. Hausman
Affiliation:
Department of Animal and Dairy Science, University of Georgia, Athens, GA 30602, USA
M. Fernyhough-Culver
Affiliation:
Albitec Corporation, Columbus, OH 43215, USA
E. Albrecht
Affiliation:
Leibniz Institute for Farm Animal Biology, Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany
M. V. Dodson
Affiliation:
Department of Animal Sciences, Washington State University, Pullman, WA 99164, USA
*
†E-mail: carolina.campos@ufv.br
Get access

Abstract

Among several potential animal models that can be used for adipogenic studies, Wagyu cattle is the one that presents unique molecular mechanisms underlying the deposit of substantial amounts of intramuscular fat. As such, this review is focused on current knowledge of such mechanisms related to adipose tissue deposition using Wagyu cattle as model. So abundant is the lipid accumulation in the skeletal muscles of these animals that in many cases, the muscle cross-sectional area appears more white (adipose tissue) than red (muscle fibers). This enhanced marbling accumulation is morphologically similar to that seen in numerous skeletal muscle dysfunctions, disease states and myopathies; this might indicate cross-similar mechanisms between such dysfunctions and fat deposition in Wagyu breed. Animal models can be used not only for a better understanding of fat deposition in livestock, but also as models to an increased comprehension on molecular mechanisms behind human conditions. This revision underlies some of the complex molecular processes of fat deposition in animals.

Keywords

wagyuadipogenesislipodystrophiesobesity
Type
Review Article
Information
animal , Volume 10 , Issue 6 , June 2016 , pp. 927 - 932
Copyright
© The Animal Consortium 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aguiari, P, Leo, S, Zavan, B, Vindigni, V, Rimessi, A, Bianchi, K, Franzin, C, Cortivo, R, Rossato, M, Vettor, R, Abatangelo, G, Pozzan, T, Pinton, P and Rizzuto, R 2008. High glucose induces adipogenic differentiation of muscle-derived stem cells. Proceedings of the National Academy of Sciences of the United States of America 105, 1226–1231.Google Scholar
Albrecht, E, Gotoh, T, Ebara, JF, Xu, X, Viergutz, T, Nurnberg, G, Maak, S and Wegner, J 2011. Cellular conditions for intramuscular fat deposition in Japanese Black and Holstein steers. Meat Science 89, 13–20.Google Scholar
Caserta, F, Tchkonia, T, Civelek, VN, Prentki, M, Brown, NF, McGarry, JD, Forse, RA, Corkey, BE, Hamilton, JA and Kirkland, JL 2001. Fat depot origin affects fatty acid handling in cultured rat and human preadipocytes. American Journal of Physiology-Endocrinology and Metabolism 280, E238–E247.Google Scholar
Cristancho, AG and Lazar, MA 2011. Forming functional fat: a growing understanding of adipocyte differentiation. Nature Reviews Molecular Cell Biology 12, 722–734.Google Scholar
Dodson, MV, Hausman, GJ, Guan, L, Du, M, Rasmussen, TP, Poulos, SP, Mir, P, Bergen, WG, Fernyhough, ME, McFarland, DC, Rhoads, RP, Soret, B, Reecy, JM, Velleman, SG and Jiang, Z 2010a. Lipid metabolism, adipocyte depot physiology and utilization of meat animals as experimental models for metabolic research. International Journal of Biological Sciences 6, 691–699.Google Scholar
Dodson, MV, Vierck, JL, Hausman, GJ, Guan, LL, Fernyhough, ME, Poulos, SP, Mir, PS and Jiang, Z 2010b. Examination of adipose depot-specific PPAR moieties. Biochemical and Biophysical Research Communications 394, 241–242.Google Scholar
Du, M, Huang, Y, Das, AK, Yang, Q, Duarte, MS, Dodson, MV and Zhu, MJ 2013. Meat Science and Muscle Biology Symposium: manipulating mesenchymal progenitor cell differentiation to optimize performance and carcass value of beef cattle. Journal of Animal Science 91, 1419–1427.Google Scholar
Du, M, Yin, J and Zhu, MJ 2010. Cellular signaling pathways regulating the initial stage of adipogenesis and marbling of skeletal muscle. Meat Science 86, 103–109.Google Scholar
Du, M and Zhu, MJ 2010. Cellular signaling pathways regulating adipogenesis and marbling of skeletal muscle. Meat Science 86, 103–109.Google Scholar
Duarte, MS, Gionbelli, MP, Paulino, PV, Serao, NV, Nascimento, CS, Botelho, ME, Martins, TS, Filho, SC, Dodson, MV, Guimaraes, SE and Du, M 2014. Maternal overnutrition enhances mRNA expression of adipogenic markers and collagen deposition in skeletal muscle of beef cattle fetuses. Journal of Animal Science 92, 3846–3854.Google Scholar
Duarte, MS, Paulino, PV, Das, AK, Wei, S, Serao, NV, Fu, X, Harris, SM, Dodson, MV and Du, M 2013. Enhancement of adipogenesis and fibrogenesis in skeletal muscle of Wagyu compared with Angus cattle. Journal of Animal Science 91, 2938–2946.Google Scholar
Duarte, SF, Francischetti, EA, Genelhu, VA, Cabello, PH and Pimentel, MM 2007. LEPR p.Q223R, beta3-AR p.W64R and LEP c.-2548G>A gene variants in obese Brazilian subjects. Genetics and Molecular Research 6, 1035–1043.Google Scholar
Edelman, SV 1998. Type II diabetes mellitus. Advances in Internal Medicine 43, 449–500.Google Scholar
Fehrer, C and Lepperdinger, G 2005. Mesenchymal stem cell aging. Experimental Gerontology 40, 926–930.Google Scholar
Fernyhough, ME, Hausman, GJ, Guan, LL, Okine, E, Moore, SS and Dodson, MV 2008. Mature adipocytes may be a source of stem cells for tissue engineering. Biochemical and Biophysical Research Communications 368, 455–457.Google Scholar
Fernyhough, ME, Helterline, DL, Vierck, JL, Hausman, GJ, Hill, RA and Dodson, MV 2005. Dedifferentiation of mature adipocytes to form adipofibroblasts: more than just a possibility. Adipocytes 1, 17–24.Google Scholar
Fischer, J, Koch, L, Emmerling, C, Vierkotten, J, Peters, T, Bruning, JC and Ruther, U 2009. Inactivation of the Fto gene protects from obesity. Nature 458, 894–898.Google Scholar
Fraser, JK, Wulur, I, Alfonso, Z and Hedrick, MH 2006. Fat tissue: an underappreciated source of stem cells for biotechnology. Trends in Biotechnology 24, 150–154.Google Scholar
Graugnard, DE, Berger, LL, Faulkner, DB and Loor, JJ 2010. High-starch diets induce precocious adipogenic gene network up-regulation in longissimus lumborum of early-weaned Angus cattle. British Journal of Nutrition 103, 953–963.Google Scholar
Harper, GS and Pethick, DW 2004. How might marbling begin? Australian Journal of Experimental Agriculture 44, 653–662.CrossRefGoogle Scholar
Hausman, GJ and Dodson, MV 2012. Stromal vascular cells and adipogenesis: cells within adipose depots regulate adipogenesis. Journal of Genomics 1, 56–66.Google Scholar
Hausman, GJ, Dodson, MV, Ajuwon, K, Azain, M, Barnes, KM, Guan, LL, Jiang, Z, Poulos, SP, Sainz, RD, Smith, S, Spurlock, M, Novakofski, J, Fernyhough, ME and Bergen, WG 2009. Board-invited review: the biology and regulation of preadipocytes and adipocytes in meat animals. Journal of Animal Science 87, 1218–1246.Google Scholar
Hocquette, JF, Gondret, F, Baéza, E, Médale, F, Jurie, C and Pethick, DW 2010. Intramuscular fat content in meat-producing animals: development, genetic and nutritional control, and identification of putative markers. Animal 4, 303–319.Google Scholar
Hudson, NJ, Reverter, A, Greenwood, PL, Guo, B, Cafe, LM and Dalrymple, BP 2014. Longitudinal muscle gene expression patterns associated with differential intramuscular fat in cattle. Animal 9, 650–659.Google Scholar
Jordan, SD, Kruger, M, Willmes, DM, Redemann, N, Wunderlich, FT, Bronneke, HS, Merkwirth, C, Kashkar, H, Olkkonen, VM, Bottger, T, Braun, T, Seibler, J and Bruning, JC 2011. Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism. Nature Cell Biology 13, 434–446.Google Scholar
Kokta, TA, Dodson, MV, Gertler, A and Hill, RA 2004. Intercellular signaling between adipose tissue and muscle tissue. Domestic Animal Endocrinology 27, 303–331.Google Scholar
Komolka, K, Albrecht, E, Wimmers, K, Michal, JJ and Maak, S 2014. Molecular heterogeneities of adipose depots-potential effects on adipose-muscle cross-talk in humans, mice and farm animals. Journal of Genomics 2, 31–44.Google Scholar
Kook, SH, Choi, KC, Son, YO, Lee, KY, Hwang, IH, Lee, HJ, Chang, JS, Choi, IH and Lee, JC 2006. Satellite cells isolated from adult Hanwoo muscle can proliferate and differentiate into myoblasts and adipose-like cells. Molecules and Cells 22, 239–245.Google Scholar
Lee, EJ, Lee, HJ, Kamli, MR, Pokharel, S, Bhat, AR, Lee, YH, Choi, BH, Chun, T, Kang, SW, Lee, YS, Kim, JW, Schnabel, RD, Taylor, JF and Choi, I 2012. Depot-specific gene expression profiles during differentiation and transdifferentiation of bovine muscle satellite cells, and differentiation of preadipocytes. Genomics 100, 195–202.Google Scholar
Lehnert, SA, Wang, YH, Tan, SH and Reverter, A 2006. Gene expression-based approaches to beef quality research. Animal Production Science 46, 165–172.Google Scholar
Majka, SM, Barak, Y and Klemm, DJ 2011. Concise review: adipocyte origins: weighing the possibilities. Stem Cells 29, 1034–1040.Google Scholar
May, SG, Savell, JW, Lunt, DK, Wilson, JJ, Laurenz, JC and Smith, SB 1994. Evidence for preadipocyte proliferation during culture of subcutaneous and intramuscular adipose tissues from Angus and Wagyu crossbred steers. Journal of Animal Science 72, 3110–3117.Google Scholar
Muthuraman, P 2014. Effect of coculturing on the myogenic and adipogenic marker gene expression. Applied Biochemistry and Biotechnology 173, 571–578.Google Scholar
Oikawa, T, Sanehira, T, Sato, K, Mizoguchi, Y, Yamamoto, H and Baba, M 2000. Genetic parameters for grouth and carcass traits of Japanese Black (Wagyu) cattle. Journal of Animal Science 71, 59–64.Google Scholar
Pena, F, Molina, A, Aviles, C, Juarez, M and Horcada, A 2013. Marbling in the longissimus thoracis muscle from lean cattle breeds. Computer image analysis of fresh versus stained meat samples. Meat Science 95, 512–519.Google Scholar
Penton, CM, Thomas-Ahner, JM, Johnson, EK, McAllister, C and Montanaro, F 2013. Muscle side population cells from dystrophic or injured muscle adopt a fibro-adipogenic fate. PLoS One 8, e54553.Google Scholar
Pethick, DW, Barendse, W, Hocquette, JF, Thompson, JM and Wang, YH 2007. Regulation of marbling and body composition-growth and development, gene markers and nutritional biochemistry. In Energy and protein metabolism and nutrition (ed. I Ortigues-Marty, N Miraux and W Brand-Williams), pp. 75–88. Wageningen Academic Publishers, Wageningen, The Netherlands.Google Scholar
Pethick, DW, D’Souza, DN, Dunshea, FR and Harper, GS 2005. Fat metabolism and regional distribution in ruminants and pigs – influences of genetics and nutrition. Recent Advances in Animal Nutrition in Australia 15, 39–45.Google Scholar
Pethick, DW, Harper, GS and Oddy, VH 2004. Growth, development and nutritional manipulation of marbling in cattle: a review. Australian Journal of Experimental Agriculture 44, 705–715.Google Scholar
Reecy, JM, Miller, SA and Webster, M 2003. Recent advances that impact skeletal muscle growth and development research. Journal of Animal Scence 81, E1–E8.Google Scholar
Romao, JM, Jin, W, Dodson, MV, Hausman, GJ, Moore, SS and Guan, LL 2011. MicroRNA regulation in mammalian adipogenesis. Experimental Biology and Medicine. 236, 997–1004.Google Scholar
Ryan, KJ, Daniel, ZC, Craggs, LJ, Parr, T and Brameld, JM 2013. Dose-dependent effects of vitamin D on transdifferentiation of skeletal muscle cells to adipose cells. Journal of Endocrinology 217, 45–58.Google Scholar
Sadkowski, T, Ciecierska, A, Majewska, A, Oprzadek, J, Dasiewicz, K, Ollik, M, Wicik, Z and Motyl, T 2014. Transcriptional background of beef marbling-novel genes implicated in intramuscular fat deposition. Meat Science 97, 32–41.Google Scholar
Sainz, RD and Hasting, E 2000. Simulation of the development of adipose tissue in beef cattle. In Modelling nutrient utilization in farm animals (ed. JP McNamara, J France and DE Beever), pp. 175–182. Cabi, New York, NY, USA.Google Scholar
Scraggs, E, Zanella, R, Wojtowicz, A, Taylor, JF, Gaskins, CT, Reeves, JJ, de Avila, JM and Neibergs, HL 2014. Estimation of inbreeding and effective population size of full-blood Wagyu cattle registered with the American Wagyu Cattle Association. Journal of Animal Breeding and Genetics 131, 3–10.Google Scholar
Shirouchi, B, Albrecht, E, Nuernberg, G, Maak, S, Olavanh, S, Nakamura, Y, Sato, M, Gotoh, T and Nuernberg, K 2014. Fatty acid profiles and adipogenic gene expression of various fat depots in Japanese Black and Holstein steers. Meat Science 96, 157–164.Google Scholar
Singh, NK, Chae, HS, Hwang, IH, Yoo, YM, Ahn, CN, Lee, SH, Lee, HJ, Park, HJ and Chung, HY 2007. Transdifferentiation of porcine satellite cells to adipoblasts with ciglitizone. Journal of Animal Science 85, 1126–1135.Google Scholar
Sul, HS 2009. Minireview: Pref-1: role in adipogenesis and mesenchymal cell fate. Molecular Endocrinology 23, 1717–1725.Google Scholar
Taylor-Jones, JM, McGehee, RE, Rando, TA, Lecka-Czernik, B, Lipschitz, DA and Peterson, CA 2002. Activation of an adipogenic program in adult myoblasts with age. Mechanisms of Ageing and Development 123, 649–661.Google Scholar
Teboul, L, Gaillard, D, Staccini, L, Inadera, H, Amri, EZ and Grimaldi, PA 1995. Thiazolidinediones and fatty acids convert myogenic cells into adipose-like cells. Journal of Biological Chemistry 270, 28183–28187.Google Scholar
Wang, YH, Bower, NI, Reverter, A, Tan, SH, De Jager, N, Wang, R, McWilliam, SM, Cafe, LM, Greenwood, PL and Lehnert, SA 2009. Gene expression patterns during intramuscular fat development in cattle. Journal of Animal Science 87, 119–130.Google Scholar
Wang, YH, Byrne, KA, Reverter, A, Harper, GS, Taniguchi, M, McWilliam, SM, Mannen, H, Oyama, K and Lehnert, SA 2005. Transcriptional profiling of skeletal muscle tissue from two breeds of cattle. Mammalian Genome 16, 201–210.Google Scholar
Wei, S, Fu, X, Liang, X, Zhu, M, Jiang, Z, Parish, SM, Dodson, MV, Zan, L and Du, M 2015. Enhanced mitogenesis in stromal vascular cells derived from subcutaneous adipose tissue of Wagyu compared with those of Angus cattle. Journal of Animal Science 93, 1015–1024.Google Scholar
Wertz, AE, Berger, LL, Walker, PM, Faulkner, DB, McKeith, FK and Rodriguez-Zas, SL 2002. Early-weaning and postweaning nutritional management affect feedlot performance, carcass merit, and the relationship of 12th-rib fat, marbling score, and feed efficiency among Angus and Wagyu heifers. Journal of Animal Science 80, 28–37.Google Scholar
Yamada, T, Higuchi, M and Nakanishi, N 2014. Fat depot-specific differences in pref-1 gene expression and adipocyte cellularity between Wagyu and Holstein cattle. Biochemical and Biophysical Research Communications 445, 310–313.Google Scholar
Yamada, T, Kawakami, SI and Nakanishi, N 2007. Effects of fattening periods on the expression of adipogenic transcription factors in Wagyu beef cattle. Meat Science 76, 289–294.Google Scholar
Yamada, T, Kawakami, SI and Nakanishi, N 2009. Expression of adipogenic transcription factors in adipose tissue of fattening Wagyu and Holstein steers. Meat Science 81, 86–92.Google Scholar
Yang, A, Larsen, TW, Powell, VH and Tume, RK 1999. A comparison of fat composition of Japanese and long-term grain-fed Australian steers. Meat Science 51, 1–9.Google Scholar
Zuk, PA, Zhu, M, Ashjian, P, De Ugarte, DA, Huang, JI, Mizuno, H, Alfonso, ZC, Fraser, JK, Benhaim, P and Hedrick, MH 2002. Human adipose tissue is a source of multipotent stem cells. Molecular Biology of the Cell 13, 4279–4295.Google Scholar