Proximal Centriole-Like

The proximal centriole-like or PCL is an atypical type of centriole found in the sperm cells of insects.[1] The PCL name is due to some similarity to the Proximal centriole found in Vertebrates sperm and the hypothesis that the two structures are homologous. The PCL is an atypical type of centriole because it does not have microtubules, a defining feature of centrioles.[2] However, the PCL is a type of centriole for several reasons. (1) the PCL formation is dependent upon the same genetic pathway that mediates the initiation of centriole formation.[1] (2) The PCL is composed of centriolar proteins.[1] (3) After fertilization, the sperm PCL function like a centriole. The PCL recruits pericentriolar material (PCM) forming a centrosome that acts as a microtubule-organizing center (MTOC).[3] The PCL also serves as a platform to form a typical centriole in the zygote, as expected from a centriole. Also, the PCL is essential to form one of the two spindle poles of the dividing zygote.[2]

The PCL was discovered in flies. However, it is also found in beetles, suggesting it is a common form of atypical centriole in insects.[4]

Another type of atypical type of centriole was discovered in human and bovine sperm.[5] This is the distal centriole of the spermatozoon, which has atypical structure and composition. This spermatozoon distal centriole is composed of splayed microtubules surrounding previously undescribed rods of centriole luminal proteins, and it has only a subset of the protein found in a typical centriole. After fertilization, the atypical distal centriole that is attached to the sperm tail recruits pericentriolar material, forming a new centriole, and localizing to the spindle pole during mitosis.[5]

During sperm swimming, the atypical distal centriole attached to the sperm tail helps couple the tail movement with head movement. The atypical distal centriole forms a dynamic basal complex (DBC) together with other structures in the sperm neck (the proximal centriole and surrounding atypical pericentriolar matrix). The dynamic basal complex facilitates a cascade of internal sliding, coupling tail beating with head kinking. Altogether, the atypical distal centriole's properties suggest that it evolved into a transmission system that couples the sperm tail motors to the whole sperm, thereby enhancing sperm function.[6]

References

  1. Blachon, S; Cai, X; Roberts, K. A; Yang, K; Polyanovsky, A; Church, A; Avidor-Reiss, T (2009). "A Proximal Centriole-Like Structure is Present in Drosophila Spermatids and Can Serve as a Model to Study Centriole Duplication". Genetics. 182 (1): 133–44. doi:10.1534/genetics.109.101709. PMC 2674812. PMID 19293139.
  2. Khire, Atul; Jo, Kyoung H; Kong, Dong; Akhshi, Tara; Blachon, Stephanie; Cekic, Anthony R; Hynek, Sarah; Ha, Andrew; Loncarek, Jadranka; Mennella, Vito; Avidor-Reiss, Tomer (2016). "Centriole Remodeling during Spermiogenesis in Drosophila". Current Biology. 26 (23): 3183–3189. doi:10.1016/j.cub.2016.07.006. PMC 5245371. PMID 28094036.
  3. Blachon, Stephanie; Khire, Atul; Avidor-Reiss, Tomer (2014). "The Origin of the Second Centriole in the Zygote of Drosophila melanogaster". Genetics. 197 (1): 199–205. doi:10.1534/genetics.113.160523. PMC 4012480. PMID 24532732.
  4. Fishman, E. L; Jo, Kyoung; Ha, Andrew; Royfman, Rachel; Zinn, Ashtyn; Krishnamurthy, Malathi; Avidor-Reiss, Tomer (2017). "Atypical centrioles are present in Tribolium sperm". Open Biology. 7 (3): 160334. doi:10.1098/rsob.160334. PMC 5376708. PMID 28298310.
  5. Fishman, Emily L; Jo, Kyoung; Nguyen, Quynh P. H; Kong, Dong; Royfman, Rachel; Cekic, Anthony R; Khanal, Sushil; Miller, Ann L; Simerly, Calvin; Schatten, Gerald; Loncarek, Jadranka; Mennella, Vito; Avidor-Reiss, Tomer (2018). "A novel atypical sperm centriole is functional during human fertilization". Nature Communications. 9 (1): 2210. doi:10.1038/s41467-018-04678-8. PMC 5992222. PMID 29880810.
  6. Khanal, S., M.R. Leung, A. Royfman, E.L. Fishman, B. Saltzman, H. Bloomfield-Gadelha, T. Zeev-Ben-Mordehai, and T. Avidor-Reiss. 2021. A dynamic basal complex modulates mammalian sperm movement. Nat Commun. 12:3808.. https://doi.org/10.1038/s41467-021-24011-0
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