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Review
. 2018 Jan 9;27(1):68-83.
doi: 10.1016/j.cmet.2017.12.002.

Anatomical, Physiological, and Functional Diversity of Adipose Tissue

Rachel K Zwick  1 , Christian F Guerrero-Juarez  2 , Valerie Horsley  3 , Maksim V Plikus  4
Affiliations
Review

Anatomical, Physiological, and Functional Diversity of Adipose Tissue

Rachel K Zwick et al. Cell Metab. .

Abstract

Adipose tissue depots can exist in close association with other organs, where they assume diverse, often non-traditional functions. In stem cell-rich skin, bone marrow, and mammary glands, adipocytes signal to and modulate organ regeneration and remodeling. Skin adipocytes and their progenitors signal to hair follicles, promoting epithelial stem cell quiescence and activation, respectively. Hair follicles signal back to adipocyte progenitors, inducing their expansion and regeneration, as in skin scars. In mammary glands and heart, adipocytes supply lipids to neighboring cells for nutritional and metabolic functions, respectively. Adipose depots adjacent to skeletal structures function to absorb mechanical shock. Adipose tissue near the surface of skin and intestine senses and responds to bacterial invasion, contributing to the body's innate immune barrier. As the recognition of diverse adipose depot functions increases, novel therapeutic approaches centered on tissue-specific adipocytes are likely to emerge for a range of cancers and regenerative, infectious, and autoimmune disorders.

Keywords: adipose stem cells; bone marrow; dermal adipose; hair follicle; mammary gland; mesenteric adipose; regeneration; skin; stem cells; wound healing.

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Figures

Figure 1:
Figure 1:. Anatomy of adipose depots.
(A, A’) In mouse skin, dermal WAT (dWAT) forms a continuous layer (shown in yellow) separated from subcutaneous WAT (sWAT) by the panniculus carnosus muscle (shown in green). This separation is not prominent in human skin, where dWAT is continuous with underlying sWAT (orange) (A’). Dermal WAT closely associates with HFs and prominently remodels during hair growth cycles. Lower portion of actively growing HFs (shown in red, blue and green) resides within dermal WAT, in close contact with adipocytes. The upper portion of the HF, housing the hair shaft, and containing the HF stem cell compartment and sebaceous gland (shown in red and yellow, respectively) and in humans, a sweat gland (maroon) are also shown. (B, B’) In the mammary gland, adipose tissue (yellow) closely associates with the gland’s epithelium (purple) and undergoes cyclic remodeling during pregnancy, lactation and involution. As shown on D, female mice have five mammary glands, three thoracic (numbers 1, 2 and 3) and two inguinal (numbers 4 and 5), each with its own adipose pads. (C) Specialized adipose tissue is associated with the bone marrow. Micro-anatomically and functionally, it is subdivided into constitutive (yellow) and regulated (red) depots. Adipocytes are shown in yellow, hematopoietic progenitors in green and other mesenchymal bone marrow cell types in grey. Anatomic location of the following additional adipose depots in mouse and human are shown: facial and retro-orbital, epicardial, joint, mesenteric, and plantar adipose tissues.
Figure 2:
Figure 2:. Cellular and signaling basis for dermal WAT remodeling.
(A) Dermal WAT remodels in parallel with the hair growth cycle. dWAT peaks in thickness during the anagen phase, when HFs are actively growing and their proximal segments closely contact with adipocytes. dWAT contains several generations of adipocytes, earlier formed cells (yellow), that remain from the previous cycle, and later formed cells (orange), that differentiate from progenitors (blue) during new cycle. In each cycle, ~20% of adipocytes form anew from the progenitors. Anagen HFs stimulate dWAT hypertrophy and hyperplasia via several paracrine ligands for Hedgehog, BMP and, possibly IGF pathways. (B) dWAT quickly reduces in size during catagen phase, primarily via lipolysis. Signaling mechanism of catagen-associated lipolysis remains poorly understood. It likely involves loss of pro-adipogenic signaling factors, such as Shh, that are abundant during anagen, and/or production of new anti-adipogenic factors. Associated with catagen is also proliferative expansion of adipose progenitors. Early stage CD24+ ASCs (blue) proliferate to give rise to CD24− late stage progenitors, pre-adipocytes (green). Driving progenitor expansion is autocrine Pdgfa signaling. (C) dWAT reaches is smallest size during telogen phase. During early, aka refractory telogen, dermal adipocytes express BMP ligands that signal to maintain quiescent state of resting HFs. Other adipose-derived hair cycle inhibitors likely exist during this phase. (D) During late, aka competent telogen dermal adipocytes cease to express BMP ligands and telogen HFs become “alert”, able to quickly enter new anagen upon stimulation. Pdgfa, produced by adipose progenitors, can directly signal to stimulate new hair cycle entry by telogen HFs. Other adipose-derived hair cycle activators likely exist during this phase.
Figure 3:
Figure 3:. Examples of specialized adipose depots in mammals.
(A) Male orangutans display prominent fat-filled facial flanges (credit: Eric Kilby). Flanges develop in adulthood and are largely absent in adult females (credit: Victor Ulijn) and pubescent males. They are thought to determine hierarchical status, dominance and successful reproductive fitness with estrus females. (B) Cetaceans, including the bottlenose dolphin (shown here) utilize melon, specialized adipose-containing tissue for echolocation (credit: William Warby). Ultrasound is generated in the so-called phonic lips (green), and sound waves travel and collimate in the melon located above maxilla (yellow). Upon echoing, incoming sound waves pass through the adipose-filled mandible and are perceived by the auditory bullae (light green). (C) Elephants evolved prominent plantar adipose (yellow) that aids in dissipating pressure (credit: Aotaro). Similar to other species, plantar adipose protects adjacent skeletal structures from mechanical shock during gating and walking. (D) Hump in camels contain adipose tissue, that has adaptive role in the desert environment (credit: Tony Hisgett). Upon periods of fasting, camels mobilize fatty acids from hump stores. Unique positioning of the adipose tissue in the humps, away from the body core, prevents camels from overheating.
Figure 4:
Figure 4:. Diverse functions of tissue-associated adipose depots.
Distinct functions of adipose tissue are represented as color-coded segments on the diagram. Paracrine signaling function of adipose in skin, mammary gland and bone marrow is in red, innate immune function of adipose in skin and intestine is in green, biomechanical function of skeleton-associated adipose is in blue, sound modulating function of melon adipose in cetaceans is in purple, and lipid ‘feeding’ function of epicardial and mammary gland adipose is in yellow. Mechanisms that require further confirmation are designated with the question mark.
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