Physiological and Pathological Mitochondrial Clearance Is Related to Pectoralis Major Muscle Pathogenesis in Broilers With Wooden Breast Syndrome.

Marina Hosotani,Maki Hoshino,Yasuhiro Hasegawa,Tomohito Iwasaki,Takafumi Watanabe,Hiromi Ueda,Tomohide Takaya,Naoki Takahashi,Yui Wakasa,Takeshi Kawasaki

doi:10.3389/fphys.2020.00579

Marina Hosotani, Maki Hoshino + Show 8 more

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https://doi.org/10.3389/fphys.2020.00579

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Abstract

Wooden breast syndrome (WB) constitutes an emerging myopathy in the pectoralis major muscle (PM) of broiler chickens, characterized by myofiber hypertrophy and degeneration along with severe fibrosis. WB pathogenesis has been considered to involve hypoxia induced by rapid growth of the PM. In this study, we focused on mitochondrial morphology and dynamics in the myofibers, as these organelles are sensitive to damage by hypoxia, and examined the effects on WB pathogenesis. Specifically, the PMs of a flock of 35 broilers at 50 days of age were evaluated. First, the severity of disease in each bird was determined by measuring histopathological indices including the fibrotic area (FA) in the muscle and circularity of myofibers (CM). These values were 29.4 ± 9.6% and 0.70 ± 0.042, respectively, showing variety among the flock. Myofiber vacuolization was observed in all birds including numerous small- or large-rimmed vacuoles, with the former consisting of ultrastructurally autophagosome-like vacuoles engulfing degenerated mitochondria. The large-rimmed vacuoles frequently occurred in the PMs with more severe FA and CM, indicating a relationship between altered autophagy/mitophagy and WB severity. Next, the expression levels of hypoxia-adaptive and mitochondrial dynamics-related genes were analyzed, and their correlations with the histopathological indices were examined. The histopathological indices were negatively correlated with the expression of vascular endothelial growth factor A (VEGFA), indicating that less angiogenesis owing to weakened hypoxia-inducible factor signaling induces more severe WB pathology. In addition, the observed negative correlation with mitochondrial dynamics-related genes implied that WB pathology deteriorates concomitant with reduced mitochondrial dynamics. Furthermore, the expression of mitochondrial dynamics-related genes showed strong positive correlation with that of VEGFA and autophagy-/mitophagy-related genes. These results revealed that the PMs of broilers possess the mechanism of physiological clearance of mitochondria damaged by the hypoxia resulting from the continuous mitochondrial dynamics and autophagy/mitophagy accompanying rapid PM growth. In turn, the altered mitochondrial clearance induced by chronic hypoxia and the accumulation of damaged mitochondria likely underly the severe pathological features of WB.

Highlights

In poultry production, meat quality impairment following the selective breeding of fast-growing broiler chickens necessary for supplying the large global demands of chicken meat represents an emerging problem worldwide (Kuttappan et al, 2013; Petracci et al, 2015)
The values of fibrotic area (FA) and circularity of myofibers (CM) in the pectoralis major muscle (PM) of each broiler are shown in Table 2; mean values in all birds were 29.4 ± 9.6% and 0.70 ± 0.042%, respectively
The histology of broiler PMs revealed myofiber hypertrophy and internal fibrosis, consistent with previous reports (Sihvo et al, 2014; Velleman and Clark, 2015), whereas the values of FA and CM histopathological indices differed among individuals, revealing that Wooden breast syndrome (WB) severity in the broilers varies during later life

Summary

Introduction

Meat quality impairment following the selective breeding of fast-growing broiler chickens necessary for supplying the large global demands of chicken meat represents an emerging problem worldwide (Kuttappan et al, 2013; Petracci et al, 2015). The PMs of some broilers exhibit severe hardness, pale color, and small hemorrhages upon palpation and macroscopic observation in the poultry slaughterhouse (Sihvo et al, 2014) and cannot be utilized, which produces large economic losses (Abasht et al, 2016). This emerging myopathy, termed Wooden breast syndrome (WB) (Petracci et al, 2019), are characterized by histopathological features such as hypertrophy, necrosis and regeneration of myofibers, macrophage infiltration, and fibrosis (Sihvo et al, 2014; Clark and Velleman, 2016; Kawasaki et al, 2018). WBaffected PMs start to deteriorate after approximately 2 or 3 weeks (Radaelli et al, 2017; Kawasaki et al, 2018), such that a flock of broilers at later life would include birds at both initial and chronic stages of WB

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