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Segregation of Protein Aggregates Involves Actin and the Polarity Machinery
Beidong Liu, Lisa Larsson, Vanessa Franssens, Xinxin Hao, Sandra Malmgren Hill, Veronica Andersson, Daniel Höglund, Jia Song, Xiaoxue Yang, David Öling et al.
Cells of yeast to mammals have evolved the means of spatial quality control (SQC), which includes the transport of protein aggregates on microtubules into a structure called the aggresome (Kopito, 2000,Wang et al., 2009) and a factor-dependent compartmentalization of aggregates into juxtanuclear sites (JUNQ) and perivacuolar inclusions (IPOD) (Kaganovich et al., 2008). SQC also encompasses an actin cytoskeleton-, polarisome-, and Hsp104-dependent segregation of damaged proteins during yeast cytokinesis (Aguilaniu et al., 2003,Erjavec et al., 2007,Tessarz et al., 2009). In addition, some aggregates in yeast daughter cells were observed to move (retrograde) into the mother cell after a transient heat stress (Liu et al., 2010). In this issue of Cell, Zhou et al., 2011 now extend this analysis and, with the aid of theoretical simulations, suggest that motility of protein aggregates is characterized by random and slow diffusion, completely devoid of directional bias. Further, it is argued that aggregate asymmetry is established in a purely passive and random manner and that no active, factor-dependent (e.g., polarisome) mechanism is involved in conferring SQC. This model contrasts that of Tessarz et al., 2009 and Liu et al., 2010, which both interpret the failure of mutants with defects in polarisome and Hsp104 functions to establish damage asymmetry indicative of damage retention being a factor-dependent process.
When considering the different views on the establishment of damage asymmetry, it should be pointed out that measurements aimed at determining the frequency of aggregate movement between mother and daughter should only include budding events in which such transfer is physically possible. This is the case during the S to early G2 phase, when the polarisome is localized at the bud tip and actin cables extend from the bud into the mother compartment. When these phases are considered, our data show that there is a bias toward retrograde movement of aggregates from daughter to mother. In 393 budding events analyzed (between 56 and 84 such events were analyzed in the Zhou et al. study), we found that 15.5% showed cross-compartment movements (Figure 1A), and among these, retrograde movement from bud to mother (66.5%) is significantly more frequent than anterograde movement (25.4%; p = 0.03) and movement in both directions (8.1%; p = 0.007) (Figure 1B). Figure S1 in the Supplemental Information available online shows two budding events with simultaneously retrograde movement of aggregates (Movie S1. An Uncropped Full-Field Movie Showing Several Budding Events with Retrograde Movement is an uncropped full-field movie showing several retrograde movements).
