Differentiation-related changes in lipid classes with long-chain and very long-chain polyenoic fatty acids in rat spermatogenic cells

Abstract

Mammalian spermatogenesis is an extraordinary cell transformation process. It includes asymmetric division of spermatogonia, rapid proliferation and differentiation into primary spermatocytes, a meiotic phase in which the genetic material in spermatocytes is recombined and segregated to produce haploid cells, a postmeiotic phase in which secondary spermatocytes develop into round spermatids, and differentiation of the latter into late spermatids and spermatozoa ( 1 ). During this last stage, known as spermiogenesis, spermatids undergo relevant cytological transformations, with changes in nuclear shape, chromatin condensation, formation of acrosome and fl agellum, and disposal of surplus organelles and materials by production and release of membrane-enclosed remnants known as "residual bodies" ( 2, 3 ). These minute, densely packed particles are then engulfed by Sertoli cells ( 4 ).The sphingomyelin (SM) ( 5 ) and ceramide (Cer) ( 6 ) of cells located in mammalian seminiferous tubules are rich in very long chain (C24 to C34) polyunsaturated fatty acids (VLCPUFA) of the n-6 or the n-3 series, the main ones being 28:4n-6 and 30:5n-6, followed by 32:5n-6 in the rat. These lipids belong to spermatogenic cells, as indicated by the facts that i) in the prepubertal rat testis, VLCPUFAcontaining species of SM and Cer are not detected; ii) in

Cell-type-specific regulation of genes involved in testicular lipid metabolism: fatty acid-binding proteins, diacylglycerol acyltransferases, and perilipin 2

“…These densely packed structures, readily phagocytized by Sertoli cells (Kerr & De Kretser 1974), contain remains of cytoplasm, RNA, former organelles, and neutral lipid inclusions (Russell et al 1990). The spermatid-derived RB are clearly discernible by markers of neutral lipid droplets, in accordance with the finding that they are even richer in TAGs than spermatids (Oresti et al 2010).…”

“…In rodents, classical studies have shown that testicular glycerophospholipids (GPLs) and triacylglycerols (TAGs) become increasingly rich in long-chain polyunsaturated fatty acids (PUFAs) like docosapentaenoic acid during postnatal development, as spermatids contain more of this fatty acid in their GPLs and TAGs than spermatocytes (Beckman et al 1978, Grogan & Huth 1983. Concomitantly, there are also significant changes in unique fatty acids of testicular sphingomyelins and ceramides destined to be components of spermatozoa (Zanetti et al 2010): the proportion of 2-hydroxy very-long-chain PUFA with respect to their nonhydroxy counterparts increases considerably in both lipids from spermatocytes and spermatids (Oresti et al 2010). The regulation of fatty acid biosynthesis and exchange among intracellular organelles of germ cells during spermatogenesis are thus essential for male fertility.…”

“…In the testis, the protein was found to be present in Sertoli and Leydig cells, associated with TAG-and cholesterol estercontaining lipid droplets (Brasaemle et al 1997, Heid et al 1998. The abundance of lipid droplets containing TAG -but no cholesterol esters -in rat germ cells and RB (Oresti et al 2010) suggested the possibility that, if a similar accumulation of TAGs and lipid droplets occurs in mice as germ cell differentiation proceeds, the expression of one of the Dgat genes and Plin2 should coincide with increasing germ cell maturation.…”

Lack of testicular seipin causes teratozoospermia syndrome in men

“…Oresti et al (26) showed, that with progressing differentiation, the amount of polyunsaturated fatty acid-rich GPL per spermatid decreased with the reduction of cell size, whereas the ratio of fatty acids (22:5/20:4) in GPL was increased, but the precise requirements for particular changes in PL composition during spermiogenesis are not yet wellunderstood. The severe morphological defects of seipin-deficient sperm reported here likely result from disturbances in lipid metabolism during spermiogenesis.…”

Metabolic Cooperation in Testis as a Pharmacological Target: From Disease to Contraception

“…Moreover, our group has recently reported that SCs produce acetate at high rates [52]. This subject has been overlooked but although the exact role for this acetate produced by SCs remains largely unknown, it is known that developing germ cells exhibit a high rate of lipid synthesis and remodeling during spermatogenesis [153,154]. These peculiarities may also provide targets to develop a male contraceptive.…”