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Many tissues in the body constantly turn over as cells divide and are replaced within weeks. Despite this turnover, tissues are able to keep proper ratios of their different cell types.

How tissues attain this balance, called homeostasis, is unclear. Here we show that homeostasis can be achieved by circuits of cells that signal to each other using diffusible signals.

A key negative feedback loop that stabilizes these circuits is endocytosis, a common feature of biological signaling in which a cell takes up and degrades the signal molecule that makes it divide and survive. Thus, the more of that cell type the less its numbers increase. Cells in tissues communicate by secreted growth factors (GF) and other signals. An important function of cell circuits is tissue homeostasis: maintaining proper balance between the amounts of different cell types. Homeostasis requires negative feedback on the GFs, to avoid a runaway situation in which cells stimulate each other and grow without control. Feedback can be obtained in at least two ways: endocytosis in which a cell removes its cognate GF by internalization and cross-inhibition in which a GF down-regulates the production of another GF.

Here we ask whether there are design principles for cell circuits to achieve tissue homeostasis. We develop an analytically solvable framework for circuits with multiple cell types and find that feedback by endocytosis is far more robust to parameter variation and has faster responses than cross-inhibition. Endocytosis, which is found ubiquitously across tissues, can even provide homeostasis to three and four communicating cell types.

These design principles form a conceptual basis for how tissues maintain a healthy balance of cell types and how balance may be disrupted in diseases such as degeneration and fibrosis. Tissues are made of several types of cells, including organ-specific parenchymal cells, fibroblasts, macrophages, and endothelial cells. For optimal function, tissues must maintain proper ratios of these component cell types (–). In many tissues, cell-type proportions are kept constant despite the fact that cells continually turn over. This feature is called tissue homeostasis. In tissues such as liver and lung, homeostasis is often restored even after damage or perturbation (–). Loss of homeostasis is a basis for diseases: Loss of a cell type characterizes degenerative diseases, whereas hyperactivity of a cell type occurs in fibrosis.

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Maintaining tissue homeostasis is challenging, because cells must control their proliferation rates and death/removal rates. If removal exceeds proliferation, cell numbers decline to zero.

If proliferation exceeds removal, cell numbers increase until they reach a limiting factor (carrying capacity) which is defined either by extrinsic factors such as oxygen and nutrients or within tissues by spatial constrains (–). Therefore, cells must use control circuits to adjust their proliferation and removal to reach a constant concentration (), especially for cell types such as macrophages that need to be maintained far below their carrying capacity in the tissue (). What these control circuits are and what design principles guide their structure are currently unclear. Homeostasis of cell numbers through circuits of communicating cells. ( A) An ON state exists when cell numbers converge to the same steady-state concentration starting from a range of different initial conditions.