Aster-free spindle poles in insect spermatocytes: evidence for chromosome-induced spindle formation?

Abstract

Abstract. Tipulid spermatocytes form normally functioning bipolar spindles after one of the centrosomes is experimentally dislocated from the nucleus in late diakinesis (Dietz, R., 1959, Z. Naturforsch., 14b:749-752; Dietz, R., 1963, Zool. Anz. Suppl., 23:131-138; Dietz, R., 1966, Heredity, 19:161-166). The possibility that dissociated pericentriolar material (PCM) is nevertheless responsible for the formation of the spindle in these cells cannot be ruled out based on live observation. In studying serial sections of complete cells and of lysed cells, it was found that centrosomefree spindle poles in the crane fly show neither pericentriolar-like material nor aster microtubules, whereas the displaced centrosomes appear complete, i.e., consist of a centriole pair, aster microtubules, and PCM. Exposure to a lysis buffer containing tubulin resulted in an increase of centrosomal asters due to aster micotubule polymerization. Aster-free spindle poles did not show any reaction, also indicating the absence of PCM at these poles. The results favor the hypothesis of chromosome-induced spindle pole formation at the onset of prometaphase and the dispensability of PCM in Pales.

“It Takes Two to Tango”: understanding how centrosome duplication is regulated throughout the cell cycle

“…Observations of bipolar spindle assembly in cells that lack centrosomes have revealed the existence of a second mechanism for spindle pole formation, even in cells that normally contain centrosomes (for review, see Compton 2000). Findings, some dating back almost 40 years, that male and female meiotic cells can form bipolar acentrosomal spindles challenged the notion that centrosomes are needed for the establishment of spindle bipolarity (Dietz 1966;Steffen et al 1986). More recent work with Xenopus egg extracts has revealed that bipolar spindles will assemble from initially randomly oriented microtubules assembled in the vicinity of chromatin, be it chromosomes or beads coated with DNA fragments (Heald et al 1996(Heald et al , 1997.…”

50 ways to build a spindle: the complexity of microtubule generation during mitosis

“…In addition, there is much accumulated evidence of acentrosomal meiotic systems in animal cells, such as mouse (Calarco-Gillam et al 1983), Xenopus (Heald et al 1996) and Drosophila (Matthies et al 1996). Furthermore, physical displacement of centrosomes from the nucleus in crane fly spermatocytes, or laser ablation of both centrosomes during prophase in monkey CVG-2 cells by laser microsurgery, does not disrupt bipolar spindle assembly (Steffen et al 1986;Khodjakov et al 2000). The observation that cells within a developing animal which normally contain centrosomes could, in fact, build a functional spindle in the complete absence of these organelles was confirmed genetically through removing, first core centrosomal and then core centriolar, proteins in fruit flies.…”

One to only two: a short history of the centrosome and its duplication

“…In spindle pole formation, the MTOC is the key player, be it focal in animal cells or diffuse-even invisible-in higher plant cells. Significantly, studies by Roland Dietz reported for primary crane fly spermatocytes that the centrioles could be displaced from the late diakinesis nucleus by flattening the cell; nevertheless, such cells assembled functional bipolar spindles (reviewed in [42]). Furthermore, exacting electron microscopy of such cells did not find accumulations of pericentriolar material (PCM) at these spindle poles; the PCM stayed with the centrioles [42].…”

“…Significantly, studies by Roland Dietz reported for primary crane fly spermatocytes that the centrioles could be displaced from the late diakinesis nucleus by flattening the cell; nevertheless, such cells assembled functional bipolar spindles (reviewed in [42]). Furthermore, exacting electron microscopy of such cells did not find accumulations of pericentriolar material (PCM) at these spindle poles; the PCM stayed with the centrioles [42]. In addition, for spermatocyte meiosis in the silkworm moth Bombyx mori the centrioles were not associated with astral fibres and were substantially separated from the spindle poles at metaphase [41].…”