The Role of Autophagy in Kidney Fibrosis and Tissue Repair Mechanisms

Introduction

The basic cellular process of degradation and recycling of damaged cellular components is autophagy. The process does play an important role in the maintenance of cellular homeostasis. In recent years, it has come under more attention regarding its significance in kidney diseases, especially on its impact on renal fibrosis and tissue repair. Kidney fibrosis is a hallmark of chronic kidney disease and is characterized by excess deposition of extracellular matrix proteins leading to progressive renal failure. Given its role in modulating cellular stress responses and inflammation, autophagy has emerged as one of the promising therapeutic targets for managing renal fibrosis. These findings elucidate further into the role of autophagy in fibrosis of the kidney and its role in relating to tissue repair mechanisms, potentially providing new therapeutic avenues that can inhibit the progression of CKD.

Understanding Autophagy and its Cellular Functions

A lysosomal pathway is the mechanism in the cells through which damaged proteins, organelles, and other cellular components are degraded. Sequestration of targeted materials into autophagosomes leads to fusion with lysosomes for degradation. The general effect of autophagy is usually activated in response to cellular stressors such as nutrient deprivation, oxidative stress, and hypoxia in the injured kidney.

The function of autophagy in kidney cells, especially renal tubular epithelial cells, has been proven to modulate several key functions, namely maintaining cellular energy balance, protection against oxidative stress, and modulation of inflammatory responses. The role becomes even more prominent during episodes of AKI, where it promotes cellular recovery and adaptation to stress.

Dual Role of Autophagy in Kidney Fibrosis

For the majority of chronic kidney diseases, the final common pathway is kidney fibrosis, which results from persistent inflammation and activation of the fibrogenic pathways. Tissue myofibroblast activation produces large amounts of the ECM components, such as collagen, which cause tissue scarring. Thus, a role of autophagy in the development of fibrosis, although generally considered protective through an enhancement of cell survival, is more complex.

In certain conditions, autophagy has been demonstrated to be antifibrotic as it breaks down pro-fibrotic proteins and inhibits the activation of myofibroblasts. For example, enhanced UUO-induced renal fibrosis in models of autophagy in renal tubular epithelial cells was associated with decreased levels of collagen deposition and accumulation of ECM. The ability of autophagy to break down mature TGF-β—the central activator of fibrosis—also suggests its antifibrotic role.   The impairment of autophagy results in overactivation of fibrogenic signaling pathways, with the effect exerted through excessive matrix deposition and fibrosis.

Although it may have sometimes pro-fibrotic effects in a certain cell context and at a specific stage of a disease, autophagy can be implicated in the regulation of fibrosis. Indeed, it was reported to support the survival of myofibroblasts and, accordingly, enhance the development of fibrosis. The dual role of autophagy as protective and deleterious implies that its timing and regulation are relevant to determining its impact on fibrosis in the kidney.

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Autophagy and the Regulation of TGF-β in Fibrosis

Transforming growth factor beta is one of the central mediators of fibrosis in many organs, including the kidneys. It stimulates the production of ECM proteins and induces the transition of fibroblasts to myofibroblasts, which are the main effector cells responsible for fibrosis. Autophagy is indicated to be involved in the regulation of TGF-β signaling pathways in the kidney.

Normal conditions can hence temper the fibrogenic activity of TGF-β through autophagic degradation, particularly of its mature forms, thus avoiding accumulation in large amounts. Autophagy has also been shown to trigger intracellular cytokine stores within TGF-β-exposed renal tubular epithelial cells, therefore curtailing their pro-fibrotic activities. The process is characterized by balance between tissue repair and fibrosis without going beyond the production of ECM proteins.

However, in impaired autophagy, TGF-β signaling is unchecked and thus activates downstream fibrogenic pathways. Models of UUO showed increased levels of TGF-β in mice that lacked key genes related to autophagy LC3B and were associated with severe kidney fibrosis. It would therefore appear that therapy to enhance autophagy might represent a useful therapeutic strategy to control TGF-β-mediated fibrosis in chronic kidney disease.

Autophagy in Epithelial-Mesenchymal Transition (EMT) and Myofibroblast Activation

The epithelial-mesenchymal transition (EMT) is another pivotal event in the production of kidney fibrosis. During EMT, renal tubular epithelial cells lose their epithelial characteristics and become mesenchymal-like cell phenotypes, which enhance their motility and invasive properties. These new cells enhance myofibroblast pools responsible for primarily generating ECM molecules.

Autophagy also modulates the EMT in kidneys by regulating cellular energy metabolism and expression of relevant markers of EMT. Such a process within cells is activated in response to hypoxia and high glucose concentrations for maintaining cellular homeostasis. On the other hand, intense autophagy during a long-standing injury may induce EMT and then fibrosis.

Overexpression of genes involved in autophagy has been associated with increased activation of EMT and myofibroblast transformation in several models of kidney fibrosis. However, inhibition of autophagy has been shown to inhibit EMT and fibrosis in other models. It further emphasizes the complexity and context-dependent character of the role of autophagy in EMT and fibrosis and suggests a balance between therapeutic modulation of autophagic activation and inhibition.

Autophagy in Kidney Repair and Regeneration

Its role in fibrosis is complex but, intuitively, more related to tissue repair. It involves the removal of degraded organelles and proteins at the recovery phase of renal damage and is known for its efficient regeneration of healthy tissue. Autophagy is also protective of surviving renal tubular cells in acute injuries, such as those associated with ischemia-reperfusion injury, protecting against damage and apoptosis.

In models of AKI, activation of autophagy promotes the restoration of kidney function by clearing out damaged mitochondria and other cellular waste. This is particularly with regard to mitophagy, which is significant in promoting the maintaining the integrity of renal tubular epithelial cells during kidney injury because of their susceptibility to mitochondrial injury. Through the removal of dysfunctional mitochondria, autophagy maintains energy supply in cells and decreases oxidative stress, both of which are vital for tissue repair.

Furthermore, autophagy facilitates resolution of inflammation, a step that is also critical for healing tissues. Inflammation is multifaceted in nature, and macrophages are functionally dual, both participating in renal damage and tissue repair. Thus, autophagy might be modulated in such a way as to have a positive influence on the maintenance of appropriate polarization status of macrophages for more effective tissue repair and lessened fibrosis. Such could thus provide a promising avenue to regulate autophagy with a potential improvement in tissue repair without an added risk of fibrosis.

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Therapeutic Applications Potential

In view of the bivalent role of autophagy in the development of kidney fibrosis versus repair, therapeutic strategies to be pursued have to be very well designed to maximize the benefit without causing risks. Enhancing autophagy selectively to maximize the potential during the early phase of kidney injury, when it favors tissue repair and limits the development of fibrosis, represents a promising strategy. In preclinical models of kidney disease, the drugs rapamycin or metformin, which activate autophagy, have been shown to reduce fibrosis and improve renal function.

The timing of activation might, however, be crucial since extended or exaggerated autophagy could exacerbate fibrosis by contributing to the survival of myofibroblasts and facilitating EMT. Thus, future therapies would have to target the creation of more selective autophagy modulators that may help fine-tune the pathway based on the stage of the disease.

Other potentially viable therapeutic options may include the manipulation of certain components within the autophagy pathway that have a role in fibrosis, such as degradation of TGF-β or regulation of EMT. As such, it would be avoided the degradation of tissue repair integrity through selectively enhancing or inhibiting certain autophagic processes.

Conclusion

Autophagy plays both protective and pro-promoting roles in the process of kidney fibrosis and tissue repair. While autophagy degrades pro-fibrotic proteins to offer some relief from fibrosis, under other conditions it takes part in fibrosis through limiting myofibroblast activation. Thus, elucidating the particular mechanisms by which autophagy exerts its modulating effects on fibrosis and repair in the kidney is critical to making thymoceptive therapies that can be exploited for their beneficial effects without promoting adverse effects. As more details come under scientific scrutiny for the study of this subject, targeting autophagy will be opening new doors for a significant number of patients suffering from chronic kidney disease.

References

  1. Ding, Y., ll Kim, S., Lee, S.Y., Koo, J.K., Wang, Z. and Choi, M.E., 2014. Autophagy regulates TGF-β expression and suppresses kidney fibrosis induced by unilateral ureteral obstruction. Journal of the American Society of Nephrology25(12), pp.2835-2846.
  2. Nakazawa, D., Kumar, S.V., Marschner, J., Desai, J., Holderied, A., Rath, L., Kraft, F., Lei, Y., Fukasawa, Y., Moeckel, G.W. and Angelotti, M.L., 2017. Histones and neutrophil extracellular traps enhance tubular necrosis and remote organ injury in ischemic AKI. Journal of the American Society of Nephrology28(6), pp.1753-1768.
  3. Humphreys, B.D., 2018. Mechanisms of renal fibrosis. Annual review of physiology80(1), pp.309-326.
  4. Chen, W., Yuan, H., Cao, W., Wang, T., Yu, H., Fu, Y., Jiang, B., Zhou, H., Guo, H. and Zhao, X., 2019. Blocking interleukin-6 trans-signaling protects against renal fibrosis by suppressing STAT3 activation. Theranostics9(14), p.3980.
  5. Imamura, M., Moon, J.S., Chung, K.P., Nakahira, K., Muthukumar, T., Shingarev, R., Ryter, S.W., Choi, A.M. and Choi, M.E., 2018. RIPK3 promotes kidney fibrosis via AKT-dependent ATP citrate lyase. JCI insight3(3).

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