Abstract
The assembly of the mitotic centromere has been extensively studied in recent years, revealing the sequence and regulation of protein loading to this chromosome domain. However, few studies have analyzed centromere assembly during mammalian meiosis. This study specifically targets this approach on mouse spermatocytes. We have found that during prophase I, the proteins of the chromosomal passenger complex Borealin, INCENP, and Aurora-B load sequentially to the inner centromere before Shugoshin 2 and MCAK. The last proteins to be assembled are the outer kinetochore proteins BubR1 and CENP-E. All these proteins are not detected at the centromere during anaphase/telophase I and are then reloaded during interkinesis. The loading sequence of the analyzed proteins is similar during prophase I and interkinesis. These findings demonstrate that the interkinesis stage, regularly overlooked, is essential for centromere and kinetochore maturation and reorganization previous to the second meiotic division. We also demonstrate that Shugoshin 2 is necessary for the loading of MCAK at the inner centromere, but is dispensable for the loading of the outer kinetochore proteins BubR1 and CENP-E.
Highlights
Accurate chromosome segregation in mitosis is crucial to maintain a diploid chromosome number
The inner kinetochore plate is formed by the chromatin subjacent to the kinetochore, in which histone H3 is replaced by CENP-A [7,8], and additional constitutive proteins that appear at kinetochores throughout the cell cycle
The characterization of the centromeric proteins and their sequential assembly have been extensively studied in mammalian mitosis, since defective chromosome segregation is associated with birth defects and cancer
Summary
Accurate chromosome segregation in mitosis is crucial to maintain a diploid chromosome number. The centromere is the chromosome domain that directs this segregation process since it is involved in relevant events such as sister-chromatid cohesion, the spindle assembly checkpoint (SAC), the attachment to spindle microtubules (MTs) and chromosome movements [1,2,3,4]. The kinetochore is a proteinaceus structure at the centromere surface mostly involved in the attachment of spindle MTs, chromosome movements and SAC regulation [2,3,5]. In vertebrates, this domain is subdivided into three distinct regions: the inner, the central and the outer kinetochore plates [2,3,6]. The outer kinetochore plate and the fibrous corona, detected only in prometaphase, are mainly composed of MT motor proteins, such as CENP-E and cytoplasmic dynein, as well as SAC proteins, as for instance Bub, BubR1, Mad and Mad2 [2,3,5,6]
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