The microtubular system and posttranslationally modified tubulin during spermatogenesis in a parasitic nematode with amoeboid and aflagellate spermatozoa

Abstract

Using transmission electron microscopy and immunologic approaches with various antibodies against general tubulin and posttranslationally modified tubulin, we investigated microtubule organization during spermatogenesis in Heligmosomoides polygyrus, a species in which a conspicuous but transient microtubular system exists in several forms: a cytoplasmic network in the spermatocyte, the meiotic spindle, a perinuclear network and a longitudinal bundle of microtubules in the spermatid. This pattern differs from most nematodes including Caenorhabditis elegans, in which spermatids have not microtubules. In the spermatozoon of H. polygyrus, immunocytochemistry does not detect tubulin, but electron microscopy reveals two centrioles with a unique structure of 10 singlets. In male germ cells, microtubules are probably involved in cell shaping and positioning of organelles but not in cell motility. In all transient tubulin structures described in spermatocytes and spermatids of H. polygyrus, detyrosination, tyrosination, and polyglutamylation were detected, but acetylation and polyglycylation were not. The presence/absence of these posttranslational modifications is apparently not stage dependent. This is the first study of posttranslationally modified tubulin in nematode spermatogenesis. Mol. Reprod. Dev. 49:150–167, 1998. © 1998 Wiley‐Liss, Inc.

How the sperm lost its tail: the evolution of aflagellate sperm

“…Motility of amoeboid sperm in nematodes is achieved with the aid of the major sperm protein (MSP). Microtubules are sometimes present in the spermatids of Heligmosomoides polygyrus (a member of the Nematoda), but they always disappear in the mature sperm (Mansir & Justine, 1998). Sperm competition has been demonstrated empirically to be an important selective force in the evolution of sperm morphology of nematodes (see LaMunyon & Ward, 1998.…”

The Post-Translational Modifications of Tubulin

“…In general, Glu-tubulin is enriched in stable microtubules, whereas microtubules containing Tyr-tubulin are labile (16,17). Glutubulin is often seen in axonemes, sperm manchettes, basal bodies, centrioles, centrosomes and the primary cilium as well as in the perinuclear region (18)(19)(20)(21)(22). In addition, the pattern of tyrosinolation in specific tissues can change during development (23,24).…”

“…Perhaps tyrosinolation makes the microtubule more flexible in this region. The tyrosinolation/detyrosinolation cycle has been seen not only in mammals, but also in a variety of invertebrates, plants, and protists (19,20,29,30) (Table 1). In corn, tyrosinolation/detyrosinolation is highly tissue-specific.…”

“…Immunohistochemistry and mass spectrometry have been used to study the distribution of polyglutamylation both phylogenetically and at the subcellular level. Polyglutamylation of tubulin occurs in animals (vertebrates, echinoderms, insects, and nematodes), plants, and protists (19,20,30,59,(75)(76)(77)(78)(79) (Table 1). The fact that Giardia tubulin is polyglutamylated suggests that this modification is very ancient (78).…”

“…As is the case with acetylation, polyglutamylation is common in stable microtubules, such as those of centrioles, basal bodies, axonemes, and axostyles (19,20,68,76,(79)(80)(81)(82). However, glutamylation also occurs on microtubules that are less stable, such as neuronal microtubules (76,81) and cochlear microtubules (where it rises and falls during development) (23,24).…”