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PLOS ONE  2013 

Development of the Mouse Dermal Adipose Layer Occurs Independently of Subcutaneous Adipose Tissue and Is Marked by Restricted Early Expression of FABP4

DOI: 10.1371/journal.pone.0059811

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Abstract:

The laboratory mouse is a key animal model for studies of adipose biology, metabolism and disease, yet the developmental changes that occur in tissues and cells that become the adipose layer in mouse skin have received little attention. Moreover, the terminology around this adipose body is often confusing, as frequently no distinction is made between adipose tissue within the skin, and so called subcutaneous fat. Here adipocyte development in mouse dorsal skin was investigated from before birth to the end of the first hair follicle growth cycle. Using Oil Red O staining, immunohistochemistry, quantitative RT-PCR and TUNEL staining we confirmed previous observations of a close spatio-temporal link between hair follicle development and the process of adipogenesis. However, unlike previous studies, we observed that the skin adipose layer was created from cells within the lower dermis. By day 16 of embryonic development (e16) the lower dermis was demarcated from the upper dermal layer, and commitment to adipogenesis in the lower dermis was signalled by expression of FABP4, a marker of adipocyte differentiation. In mature mice the skin adipose layer is separated from underlying subcutaneous adipose tissue by the panniculus carnosus. We observed that the skin adipose tissue did not combine or intermix with subcutaneous adipose tissue at any developmental time point. By transplanting skin isolated from e14.5 mice (prior to the start of adipogenesis), under the kidney capsule of adult mice, we showed that skin adipose tissue develops independently and without influence from subcutaneous depots. This study has reinforced the developmental link between hair follicles and skin adipocyte biology. We argue that because skin adipocytes develop from cells within the dermis and independently from subcutaneous adipose tissue, that it is accurately termed dermal adipose tissue and that, in laboratory mice at least, it represents a separate adipose depot.

References

[1]  Cinti S (2007) Nutrition and Health. In: Fantuzzi G, Mazzone T, editors. Adipose Tissue and Adipokines in Health and Disease. Humana Press Incorporated, Totowa, New Jersey. 3–19.
[2]  Gesta S, Tseng YH, Kahn CR (2007) Developmental origin of fat: tracking obesity to its source. Cell 131: 242–256.
[3]  Billon N, Iannarelli P, Monteiro MC, Glavieux-Pardanaud C, Richardson WD, et al. (2007) The generation of adipocytes by the neural crest. Development 134: 2283–2292.
[4]  Billon N, Monteiro MC, Dani C (2008) Developmental origin of adipocytes: new insights into a pending question. Biology of the cell 100: 563–575.
[5]  Billon N, Dani C (2012) Developmental origins of the adipocyte lineage: new insights from genetics and genomics studies. Stem cell reviews 8: 55–66.
[6]  Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, et al. (2008) White fat progenitor cells reside in the adipose vasculature. Science 322: 583–586.
[7]  Tran KV, Gealekman O, Frontini A, Zingaretti MC, Morroni M, et al. (2012) The vascular endothelium of the adipose tissue gives rise to both white and brown fat cells. Cell metabolism 15: 222–229.
[8]  Majka SM, Barak Y, Klemm DJ (2011) Concise review: adipocyte origins: weighing the possibilities. Stem Cells 29: 1034–1040.
[9]  Poulos SP, Hausman DB, Hausman GJ (2010) The development and endocrine functions of adipose tissue. Molecular and cellular endocrinology 323: 20–34.
[10]  Poissonnet CM, Burdi AR, Garn SM (1984) The chronology of adipose tissue appearance and distribution in the human fetus. Early human development 10: 1–11.
[11]  Hausman GJ, Martin RJ (1981) Subcutaneous adipose tissue development in Yorkshire (lean) and ossawbaw (obese) pigs. Journal of animal science 52: 1442–1449.
[12]  Hausman GJ, Martin RJ (1982) The development of adipocytes located around hair follicles in the foetal pig. Journal of animal science 54: 1286–1296.
[13]  Hausman GJ, Thomas GB (1984) The development of the inner layer of back fat in foetal and young pigs. Journal of animal science 58: 1550–1560.
[14]  Hausman GJ (1985) Cellular and enzyme-histochemical aspects of adipose tissue development in obese (Ossabaw) and lean (crossbred) pig fetuses: an ontogeny study. Journal of animal science 60: 1539–1552.
[15]  Hausman GJ, Kauffman RG (1986) The histology of developing porcine adipose tissue. Journal of animal science 63: 642–658.
[16]  Anderson DB, Kauffman RG, Kastenschmidt LL (1972) Lipogenic enzyme activities and cellularity of porcine adipose tissue from various anatomical locations. Journal of lipid research 13: 593–599.
[17]  Hausman GJ, Campion DR, Richardson RL, Martin RJ (1981) Adipocyte development in the rat hypodermis. The American journal of anatomy 161: 85–100.
[18]  Tran TT, Yamamoto Y, Gesta S, Kahn CR (2008) Beneficial effects of subcutaneous fat transplantation on metabolism. Cell metabolism 7: 410–420.
[19]  Zeve D, Tang W, Graff J (2009) Fighting fat with fat: the expanding field of adipose stem cells. Cell Stem Cell 5: 472–481.
[20]  Gimble JM, Bunnell BA, Chiu ES, Guilak F (2011) Adipose-derived stromal vascular fraction cells and stem cells: let’s not get lost in translation. Stem Cells 29: 749–754.
[21]  Klein J, Permana PA, Owecki M, Chaldakov GN, B?hm M, et al. (2007) What are subcutaneous adipocytes really good for? Experimental dermatology 16: 45–70.
[22]  Gibbs HF (1941) A study of the post-natal development of the skin and hair of the mouse. The Anatomical record 80: 61–82.
[23]  Chase H, Montagna W, Malone J (1953) Changes in the skin in relation to the hair growth cycle. The Anatomical record 116: 75–82.
[24]  Borodach GN, Montagna W (1955) Fat in skin of the mouse during cycles of hair growth. The Journal of investigative dermatology 26: 229–232.
[25]  Moffat GH (1968) The growth of hair follicles and its relation to the adjacent dermal structures. Journal of anatomy 102: 527–540.
[26]  Plikus MV, Mayer JA, de la Cruz D, Baker RE, Maini PK, et al. (2008) Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 451: 340–344.
[27]  Festa E, Fretz J, Berry R, Schmidt B, Rodeheffer M, et al. (2011) Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling. Cell 146: 761–771.
[28]  Birsoy K, Berry R, Wang T, Ceyhan O, Tavazoie S, et al. (2011) Analysis of gene networks in white adipose tissue development reveals a role for ETS2 in adipogenesis. Development 138: 4709–4719.
[29]  Wojciechowicz K, Markiewicz E, Jahoda CA (2008) C/EBPalpha identifies differentiating preadipocytes around hair follicles in foetal and neonatal rat and mouse skin. Experimental dermatology 17: 675–680.
[30]  Richardson GD, Bazzi H, Fantauzzo KA, Waters JM, Crawford H, et al. (2009) KGF and EGF signalling block hair follicle induction and promote interfollicular epidermal fate in developing mouse skin. Development 136: 2153–2164.
[31]  Fantauzzo KA, Bazzi H, Jahoda CA, Christiano AM (2008) Dynamic expression of the zinc-finger transcription factor Trps1 during hair follicle morphogenesis and cycling. Gene expression patterns 8: 51–7.
[32]  Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671–675.
[33]  Wolnicka-Glubisz A, King W, Noonan FP (2005) SCA-1+ cells with an adipocyte phenotype in neonatal mouse skin. The Journal of investigative dermatology 125: 383–385.
[34]  Herrmann T, van der Hoeven F, Grone HJ, Stewart AF, Langbein L, et al. (2003) Mice with targeted disruption of the fatty acid transport protein 4 (Fatp 4, Slc27a4) gene show features of lethal restrictive dermopathy. The Journal of cell biology 161: 1105–1115.
[35]  Cinti S (2001) Morphology of the Adipose Tissue. In: Klaus S, editor. Adipose Tissues. Landes Bioscience, Austin, Texas. 11–26.
[36]  Atit R, Sgaier SK, Mohamed OA, Taketo MM, Dufort D, et al. (2006) Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Developmental biology 296: 164–176.
[37]  Hong KM, Burdick MD, Phillips RJ, Heber D, Strieter RM (2005) Characterization of human fibrocytes as circulating adipocyte progenitors and the formation of human adipose tissue in SCID mice. The Federation of the American societies for experimental biology 19: 2029–2031.
[38]  Koh YJ, Kang S, Lee HJ, Choi TS, Lee HS, et al. (2007) Bone marrow-derived circulating progenitor cells fail to transdifferentiate into adipocytes in adult adipose tissues in mice. The Journal of clinical investigation 117: 3684–3695.
[39]  van Genderen C, Okamura RM, Fari?as I, Quo RG, Parslow TG, et al. (1994) Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes and development 8: 2691–2703.
[40]  Olivera-Martinez I, Viallet JP, Michon F, Pearton DJ, Dhouailly D (2004) The different steps of skin formation in vertebrates. The International journal of developmental biology 48: 107–115.
[41]  Chen D, Jarrell A, Guo C, Lang R, Atit R (2012) Dermal β-catenin activity in response to epidermal Wnt ligands is required for fibroblast proliferation and hair follicle initiation. Development 139: 1522–1533.
[42]  Ohtola J, Myers J, Akhtar-Zaidi B, Zuzindlak D, Sandesara P, et al. (2008) beta-Catenin has sequential roles in the survival and specification of ventral dermis. Development 135: 2321–2329.
[43]  Tran TH, Jarrell A, Zentner GE, Welsh A, Brownell I, et al. (2010) Role of canonical Wnt signaling/?-catenin via Dermo1 in cranial dermal cell development. Development 137: 3973–3984.
[44]  Hausman GJ, Richardson RL (2004) Adipose tissue angiogenesis. Journal of animal science 82: 925–934.
[45]  Cao Y (2007) Angiogenesis modulates adipogenesis and obesity. The Journal of clinical investigation 117: 2362–2368.
[46]  Han J, Lee JE, Jin J, Lim JS, Oh N, et al. (2011) The spatiotemporal development of adipose tissue. Development 138: 5027–5037.
[47]  Crandall DL, Hausman GJ, Kral JG (1997) A review of the microcirculation of adipose tissue: anatomic, metabolic, and angiogenic perspectives. Microcirculation 4: 211–232.
[48]  Rodeheffer MS, Birsoy K, Friedman JM (2008) Identification of white adipocyte progenitor cells in vivo. Cell 135: 240–249.
[49]  Longo KA, Wright WS, Kang S, Gerin I, Chiang SH, et al. (2004) Wnt10b inhibits development of white and brown adipose tissues. The Journal of biological chemistry 279: 35503–35509.
[50]  Sugawara K, Schneider MR, Dahlhoff M, Kloepper JE, Paus R (2010) Cutaneous consequences of inhibiting EGF receptor signaling in vivo: normal hair follicle development, but retarded hair cycle induction and inhibition of adipocyte growth in Egfr(Wa5) mice. Journal of dermatological science 57: 155–161.
[51]  Karlsson L, Bondjers C, Betsholtz C (1999) Roles for PDGF-A and sonic hedgehog in development of mesenchymal components of the hair follicle. Development 126: 2611–2621.
[52]  Schulz TJ, Tseng YH (2009) Emerging role of bone morphogenetic proteins in adipogenesis and energy metabolism. Cytokine and growth factor reviews 20: 523–531.
[53]  Christodoulides C, Laudes M, Cawthorn WP, Schinner S, Soos M, et al. (2006) The Wnt antagonist Dickkopf-1 and its receptors are coordinately regulated during early human adipogenesis. Journal of cell science 119: 2613–2620.

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