Abstract
Superficial fascia has abundant preadipocytes capable of spontaneous and induced differentiation and is thought to be a novel origin of adipocytes. This study aimed to quantitatively evaluate the spatial distribution and correlation of adipocytes and mast cells in rat superficial fascia. Panoramic images were obtained from whole-mounted fascia stained by toluidine blue. Adipocytes increased gradually in superficial fascia of growing rats. Abundant mast cells, with the degranulation and exocytosis of abundant secretory granules, appeared in fascia where partially differentiating adipocytes and mature adipocytes occurred. Quantitative histological analysis by variance–mean ratio and Morisita index of dispersion indicated that both mast cells and adipocytes in fascia were distributed individually in cluster, but not random or uniform. Spearman’s correlation coefficient revealed that the spatial cluster distributions of mast cells and adipocytes positively correlated with each other and correlated with increased number and size of adipocytes and adipogenic areas in fascia. Morphometry analysis indicated the strong correlation between fascial adipocytes and mast cells during the periods of rat growth. The correlation coefficient increased significantly at 8 weeks compared to 4 weeks, consistent with the increasing trend of the number and size of fascia adipocytes in growing rats. This finding provided the first quantitative histological analysis for the spatial distribution and correlation of fascia adipocytes and mast cells, which could be the histocytological basis for further exploring spatial and functional interactions between fascial mast cells and adipocytes. Also, the present data were informative for the research on physiologies and pathologies of fascia and fascia-related connective tissues.
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References
Abu-Hijleh MF, Roshier AL, Al-Shboul Q, Dharap AS, Harris PF (2006) The membranous layer of superficial fascia: evidence for its widespread distribution in the body. Surg Radiol Anat 28(6):606–619
Altintas MM, Azad A, Nayer B, Contreras G, Zaias J, Faul C, Reiser J, Nayer A (2011) Mast cells, macrophages, and crown-like structures distinguish subcutaneous from visceral fat in mice. J Lipid Res 52(3):480–488. https://doi.org/10.1194/jlr.M011338
Armstrong RA (2003) Measuring the degree of spatial correlation between histological features in thin sections of brain tissue. Neuropathology 23(4):245–253
Armstrong RA (2006) Measuring the spatial arrangement patterns of pathological lesions in histological sections of brain tissue. Folia Neuropathol 44(4):229–237
Atiakshin D, Samoilova V, Buchwalow I, Boecker W, Tiemann M (2017) Characterization of mast cell populations using different methods for their identification. Histochem Cell Biol 147(6):683–694. https://doi.org/10.1007/s00418-017-1547-7
Cawthorn WP, Scheller EL, MacDougald OA (2012) Adipose tissue stem cells meet preadipocyte commitment: going back to the future. J Lipid Res 53(2):227–246
Choi MY, Kim HI, Yang YI, Kim JT, Jang SH, Park CM, Jang WH, Youn YC, Cheong SH, Choi CS, Kim DK, Lee SJ (2012) The isolation and in situ identification of MSCs residing in loose connective tissues using a niche-preserving organ culture system. Biomaterials 33(18):4469–4479
Crivellato E, Travan L, Ribatti D (2015) The phylogenetic profile of mast cells. Methods Mol Biol 1220:11–27. https://doi.org/10.1007/978-1-4939-1568-2_2
da Silva EZ, Jamur MC, Oliver C (2014) Mast cell function: a new vision of an old cell. J Histochem Cytochem 62(10):698–738. https://doi.org/10.1369/0022155414545334
Diculescu I, Stoica M (1970) Fluorescence histochemical investigation on the adrenergic innervation of the white adipose tissue in the rat. J Neurovisc Relat 32(1):25–36
Greig-Smith P (1952) The use of random and contiguous quadrats in the study of the structure of plant communities. Ann Bot 16(2):293–316
Greig-Smith P (1983) Quantitative plant ecology, 3rd edn. University of California Press, Berkeley, CA
Han J, Lee JE, Jin J, Lim JS, Oh N, Kim K, Chang SI, Shibuya M, Kim H, Koh GY (2011) The spatiotemporal development of adipose tissue. Development 138(22):5027–5037. https://doi.org/10.1242/dev.067686
Hausman GJ, Richardson RL (2004) Adipose tissue angiogenesis. J Anim Sci 82(3):925–934. https://doi.org/10.2527/2004.823925x
Hausman GJ, Campion DR, Martin RJ (1980) Search for the adipocyte precursor cell and factors that promote its differentiation. J Lipid Res 21(6):657–670
Hellman B, Larsson S, Westman S (1963) Mast cell content and fatty acid metabolism in the epididymal fat pad of obese mice. Acta Physiol Scand 58:255–262. https://doi.org/10.1111/j.1748-1716.1963.tb02647.x
Ishijima Y, Ohmori S, Ohneda K (2013) Mast cell deficiency results in the accumulation of preadipocytes in adipose tissue in both obese and non-obese mice. FEBS Open Bio 4:18–24. https://doi.org/10.1016/j.fob.2013.11.004
Kershaw KA (1973) Quantitative and dynamic plant ecology. 2nd edn. Elsevier, New York
Li G, Zheng B, Meszaros LB, Vella JB, Usas A, Matsumoto T, Huard J (2011) Identification and characterization of chondrogenic progenitor cells in the fascia of postnatal skeletal muscle. J Mol Cell Biol 3(6):369–377
Liu J, Divoux A, Sun J, Zhang J, Clement K, Glickman JN, Sukhova GK, Wolters PJ, Du J, Gorgun CZ, Doria A, Libby P, Blumberg RS, Kahn BB, Hotamisligil GS, Shi GP (2009) Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med 15(8):940–945. https://doi.org/10.1038/nm.1994
Morisita M (1959) Measuring of the dispersion of individuals and analysis of the distributional patterns. Mem Fac Sci Kyushu Univ, Ser E 2:215–235
Morisita M (1962) I σ-Index, a measure of dispersion of individuals. Res Popul Ecol 4(1):1–7
Nakajima H, Imanishi N, Minabe T, Kishi K, Aiso S (2004) Anatomical study of subcutaneous adipofascial tissue: a concept of the protective adipofascial system (PAFS) and lubricant adipofascial system (LAFS). Scand J Plast Reconstr Surg Hand Surg 38(5):261–266
Paoletti S (2006) The fasciae: anatomy, dysfunction and treatment. Eastland Press, Seattle
Poglio S, De Toni-Costes F, Arnaud E, Laharrague P, Espinosa E, Casteilla L, Cousin B (2010) Adipose tissue as a dedicated reservoir of functional mast cell progenitors. Stem Cells 28(11):2065–2072. https://doi.org/10.1002/stem.523
Puebla-Osorio N, Sarchio SNE, Ullrich SE, Byrne SN (2017) Detection of infiltrating mast cells using a modified toluidine Blue staining. Methods Mol Biol 1627:213–222. https://doi.org/10.1007/978-1-4939-7113-8_14
Ribatti D, Crivellato E (2012) Mast cells, angiogenesis, and tumour growth. Biochim Biophys Acta 1822(1):2–8. https://doi.org/10.1016/j.bbadis.2010.11.010
Ross M (2010) Histology: a text and atlas, 6th edn. Wolters Kluwer/Lippincott Williams & Wilkins, Baltimore
Schleip R, Jager H, Klingler W (2012) What is ‘fascia’? A review of different nomenclatures. J Bodyw Mov Ther 16(4):496–502
Shen W, Wang Z, Punyanita M, Lei J, Sinav A, Kral JG, Imielinska C, Ross R, Heymsfield SB (2003) Adipose tissue quantification by imaging methods: a proposed classification. Obes Res 11(1):5–16. https://doi.org/10.1038/oby.2003.3
Sridharan G, Shankar AA (2012) Toluidine blue: a review of its chemistry and clinical utility. J Oral Maxillofac Pathol 16(2):251–255. https://doi.org/10.4103/0973-029X.99081
Standring S (2008) Gray's anatomy: the anatomical basis of clinical practice, 40th edn. Elsevier, Churchill Livingstone
Stecco C, Macchi V, Porzionato A, Duparc F, De Caro R (2011) The fascia: the forgotten structure. Ital J Anat Embryol 116(3):127–138
Su X, Lyu Y, Wang W, Zhang Y, Li D, Wei S, Du C, Geng B, Sztalryd C, Xu G (2016) Fascia origin of adipose cells. Stem Cells 34(5):1407–1419. https://doi.org/10.1002/stem.2338
Tanaka A, Nomura Y, Matsuda A, Ohmori K, Matsuda H (2011) Mast cells function as an alternative modulator of adipogenesis through 15-deoxy-delta-12, 14-prostaglandin J2. Am J Physiol Cell Physiol 301(6):C1360–C1367. https://doi.org/10.1152/ajpcell.00514.2010
Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, Tallquist MD, Graff JM (2008) White fat progenitor cells reside in the adipose vasculature. Science 322(5901):583–586
Wong HL, Siu WS, Fung CH, Zhang C, Shum WT, Zhou XL, Lau CB, Zhang JF, Leung PC, Fu WM, Ko CH (2015) Characteristics of stem cells derived from rat fascia: in vitro proliferative and multilineage potential assessment. Mol Med Rep 11(3):1982–1990
Zhang J, Shi GP (2012) Mast cells and metabolic syndrome. Biochim Biophys Acta 1822(1):14–20. https://doi.org/10.1016/j.bbadis.2010.12.012
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This work was supported by the National Natural Science Foundation of China [81570791, 31872793].
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Zhang, D., Dong, Y., Zhang, Y. et al. Spatial distribution and correlation of adipocytes and mast cells in superficial fascia in rats. Histochem Cell Biol 152, 439–451 (2019). https://doi.org/10.1007/s00418-019-01812-5
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DOI: https://doi.org/10.1007/s00418-019-01812-5