Spermatocyte

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Spermatogenesis as the cells progress from spermatogium, to primary spermatocytes, to secondary spermatocytes, to spermatids and to sperm. Figure 28 01 04.jpg
Spermatogenesis as the cells progress from spermatogium, to primary spermatocytes, to secondary spermatocytes, to spermatids and to sperm.

Spermatocytes are a type of male gametocyte in animals. They derive from immature germ cells called spermatogonia. They are found in the testis, in a structure known as the seminiferous tubules. [1] There are two types of spermatocytes, primary and secondary spermatocytes. Primary and secondary spermatocytes are formed through the process of spermatocytogenesis. [2]

Contents

Primary spermatocytes are diploid (2N) cells. After meiosis I, two secondary spermatocytes are formed. Secondary spermatocytes are haploid (N) cells that contain half the number of chromosomes. [1]

In all animals, males produce spermatocytes, even hermaphrodites such as C. elegans, which exist as a male or hermaphrodite. In hermaphrodite C. elegans, sperm production occurs first and is then stored in the spermatheca. Once the eggs are formed, they are able to self-fertilize and produce up to 350 progeny. [3]

Development

Spermatogonia going through mitosis to form primary spermatocytes in Grasshopper testes. Mitosis (263 06) Grasshopper testes (Spermatogonia).jpg
Spermatogonia going through mitosis to form primary spermatocytes in Grasshopper testes.
Spermatocytogenesis Spermatocytogenesis.png
Spermatocytogenesis

At puberty, spermatogonia located along the walls of the seminiferous tubules within the testis will be initiated and start to divide mitotically, forming two types of A cells that contain an oval shaped nucleus with a nucleolus attached to the nuclear envelope; one is dark (Ad) and the other is pale (Ap). The Ad cells are spermatogonia that will stay in the basal compartment (outer region of the tubule); these cells are reserve spermatogonial stem cells that do not usually undergo mitosis. Type Ap are actively-dividing spermatogonial stem cells which begin differentiation to type B spermatogonia, which have round nuclei and heterochromatin attached to the nuclear envelope and the center of nucleolus. [4] Type B cells will move on to the adluminal compartment (towards the inner region of tubule) and become primary spermatocytes; this process takes about 16 days to complete. [2] [5]

The primary spermatocytes within the adluminal compartment will continue on to meiosis I and divide into two daughters cells, known as secondary spermatocytes, a process which takes 24 days to complete. Each secondary spermatocyte will form two spermatids after meiosis II. [1]

Although spermatocytes that divide mitotically and meiotically are sensitive to radiation and cancer, spermatogonial stem cells are not. Therefore, after termination of radiation therapy or chemotherapy, the spermatognia stems cells may re-initiate the formation of spermatogenesis. [6]

Hormones produced by the Pituitary gland. GnRH is secreted by the hypothalamus, which induces anterior pituitary to produce FSH and LH upon puberty. 1810 Major Pituitary Hormones.jpg
Hormones produced by the Pituitary gland. GnRH is secreted by the hypothalamus, which induces anterior pituitary to produce FSH and LH upon puberty.

Role of hormones

The formation of primary spermatocytes (a process known as spermatocytogenesis) begins in humans when a male is sexually matured at puberty, around the age of 10 through 14. [7] Formation is initiated upon the pulsated surges of gonadotropin-releasing hormone (GnRH) from the hypothalamus, which leads to the secretion of follicle-stimulating hormone (FSH) and luteinizing hormone (LH) produced by the anterior pituitary gland. The release of FSH into the testes will enhance spermatogenesis and lead to the development of Sertoli cells, which act as nursing cells where spermatids will go to mature after meiosis II. LH promotes Leydig cell secretion of testosterone into the testes and blood, which induce spermatogenesis and aid the formation of secondary sex characteristics. From this point on, the secretion of FSH and LH (inducing production of testosterone) will stimulate spermatogenesis until the male dies. [8] Increasing the hormones FSH and LH in males will not increase the rate of spermatogenesis. However, with age, the rate of production will decrease, even when the amount of hormone that is secreted is constant; this is due to higher rates of degeneration of germ cells during meiotic prophase. [1]

Cell type summary

In the following table, ploidy, copy number and chromosome/chromatid counts listed are for a single cell, generally prior to DNA synthesis and division (in G1 if applicable). Primary spermatocytes are arrested after DNA synthesis and prior to division. [1] [2]

CellTypePloidy/Chromosomes in humanDNA copy number/Chromatids in humanProcess entered by cellDuration
spermatogonium (types Ad, Ap and B) germ cells diploid (2N) / 462C / 46 spermatocytogenesis (mitosis)16 days
primary spermatocytemale gametocyte diploid (2N) / 464C / 2x46 spermatocytogenesis (meiosis I)24 days
secondary spermatocytemale gametocytehaploid (N) / 232C / 46 spermatidogenesis (meiosis II)A few hours
spermatids male gametid haploid (N) / 231C / 23 spermiogenesis 24 days
spermatozoids sperm haploid (N) / 231C / 23spermiation64 days (total)

Physiology

Damage, repair, and failure

Spermatocytes regularly overcome double-strand breaks and other DNA damages in the prophase stage of meiosis. These damages can arise by the programmed activity of Spo11, an enzyme employed in meiotic recombination, as well as by un-programmed breakages in DNA, such as those caused by oxidative free radicals produced as products of normal metabolism. These damages are repaired by homologous recombination pathways and utilize RAD1 and γH2AX, which recognize double strand breaks and modify chromatin, respectively. As a result, double strand breaks in meiotic cells, unlike mitotic cells, do not typically lead to apoptosis, or cell death. [9] Homologous recombinational repair (HRR) of double-strand breaks occurs in mice during sequential stages of spermatogenesis but is most prominent in spermatocytes. [10] In spermatocytes, HRR events occur mainly in the pachytene stage of meiosis and the gene conversion type of HRR is predominant, whereas in other stages of spermatogenesis the reciprocal exchange type of HRR is more frequent. [10] During mouse spermatogenesis, the mutation frequencies of cells at the different stages, including pachytene spermatocytes, are 5 to 10-fold lower than the mutation frequencies in somatic cells. [11] Because of their elevated DNA repair capability, spermatocytes likely play a central role in the maintenance of these lower mutation rates, and thus in the preservation of the genetic integrity of the male germ line.

It is known that heterozygous chromosomal rearrangements lead to spermatogenic disturbance or failure; however the molecular mechanisms that cause this are not as well known. It is suggested that a passive mechanism involving asynaptic region clustering in spermatocytes is a possible cause. Asynaptic regions are associated with BRCA1, kinase ATR and γH2AX presence in pachytene spermatocytes. [12]

Specific mutations

Wild-type spermatocyte progression compared to repro4 mutated spermatocytes. Repro4 mutation in Spermatocytes.jpg
Wild-type spermatocyte progression compared to repro4 mutated spermatocytes.

The gene Stimulated By Retinoic Acid 8 (STRA8) is required for the retinoic-acid signaling pathway in humans, which leads to meiosis initiation. STRA8 expression is higher in preleptotene spermatocytes (at the earliest stage of prophase I in meiosis) than in spermatogonia. STRA8-mutant spermatocytes have been shown to be capable of meiosis initiation; however, they cannot complete the process. Mutations in leptotene spermatocytes can result in premature chromosome condensation. [13]

Mutations in Mtap2, a microtubule-associated protein, as observed in repro4 mutant spermatocytes, have been shown to arrest spermatogenesis progress during the prophase of meiosis I. This is observed by a reduction in spermatid presence in repro4 mutants. [14]

Recombinant-defective mutations can occur in Spo11 , DMC1, ATM and MSH5 genes of spermatocytes. These mutations involve double strand break repair impairment, which can result in arrest of spermatogenesis at stage IV of the seminiferous epithelium cycle. [15]

History

Meiosis in Grasshopper testes (primary spermatocytes in zygotene, pachytene, prophase I). Meiosis (248 23).jpg
Meiosis in Grasshopper testes (primary spermatocytes in zygotene, pachytene, prophase I).

The spermatogenesis process has been elucidated throughout the years by researchers who divided the process into multiple stages or phases, depending on intrinsic (germ and Sertoli cells) and extrinsic (FSH and LH) factors. [16] The spermatogenesis process in mammals as a whole, involving cellular transformation, mitosis, and meiosis, has been well studied and documented from the 1950s to 1980s. However, during the 1990s and 2000s researchers have focused around increasing understanding of the regulation of spermatogenesis via genes, proteins, and signaling pathways, and the biochemical and molecular mechanisms involved in these processes. Most recently, the environmental effects on spermatogenesis have become a focus as male infertility in men has become more prevalent. [17]

An important discovery in the spermatogenesis process was the identification of the seminiferous epithelial cycle in mammals—work by C.P. Leblound and Y. Clermont in 1952 that studied the spermatogonia, spermatocyte layers and spermatids in rat seminiferous tubules. Another critical discovery was that of the hypothalamic-pituitary-testicular hormone chain, which plays a role in spermatogenesis regulation; this was studied by R. M. Sharpe in 1994. [17]

Other animals

Mesostoma ehrenbergii Mesostoma ehrenbergii.jpg
Mesostoma ehrenbergii

Primary cilia are common organelles found in eukaryotic cells; they play an important role in development of animals. Drosophila have unique properties in their spermatocyte primary cilia—they are assembled by four centrioles independently in the G2 phase and are sensitive to microtubule-targeting drugs. Normally, primary cilia will develop from one centriole in the G0/G1 phase and are not affected by microtubule targeting drugs. [18]

Mesostoma ehrenbergii is a rhabdocoel flatworm with a distinctive male meiosis stage within the formation of spermatocytes. During the pre-anaphase stage, cleavage furrows are formed in the spermatocyte cells containing four univalent chromosomes. By the end of the anaphase stage, there is one at each pole moving between the spindle poles without actually having physical interactions with one another (also known as distance segregation). These unique traits allow researchers to study the force created by the spindle poles to allow the chromosomes to move, cleavage furrow management and distance segregation. [19] [20]

See also

Related Research Articles

<span class="mw-page-title-main">Meiosis</span> Cell division producing haploid gametes

Meiosis is a special type of cell division of germ cells and apicomplexans in sexually-reproducing organisms that produces the gametes, the sperm or egg cells. It involves two rounds of division that ultimately result in four cells, each with only one copy of each chromosome (haploid). Additionally, prior to the division, genetic material from the paternal and maternal copies of each chromosome is crossed over, creating new combinations of code on each chromosome. Later on, during fertilisation, the haploid cells produced by meiosis from a male and a female will fuse to create a zygote, a cell with two copies of each chromosome again.

<span class="mw-page-title-main">Gonad</span> Gland that produces sex cells

A gonad, sex gland, or reproductive gland is a mixed gland that produces the gametes and sex hormones of an organism. Female reproductive cells are egg cells, and male reproductive cells are sperm. The male gonad, the testicle, produces sperm in the form of spermatozoa. The female gonad, the ovary, produces egg cells. Both of these gametes are haploid cells. Some hermaphroditic animals have a type of gonad called an ovotestis.

<span class="mw-page-title-main">Gametogenesis</span> Biological process

Gametogenesis is a biological process by which diploid or haploid precursor cells undergo cell division and differentiation to form mature haploid gametes. Depending on the biological life cycle of the organism, gametogenesis occurs by meiotic division of diploid gametocytes into various gametes, or by mitosis. For example, plants produce gametes through mitosis in gametophytes. The gametophytes grow from haploid spores after sporic meiosis. The existence of a multicellular, haploid phase in the life cycle between meiosis and gametogenesis is also referred to as alternation of generations.

<span class="mw-page-title-main">Germ cell</span> Gamete-producing cell

A germ cell is any cell that gives rise to the gametes of an organism that reproduces sexually. In many animals, the germ cells originate in the primitive streak and migrate via the gut of an embryo to the developing gonads. There, they undergo meiosis, followed by cellular differentiation into mature gametes, either eggs or sperm. Unlike animals, plants do not have germ cells designated in early development. Instead, germ cells can arise from somatic cells in the adult, such as the floral meristem of flowering plants.

<span class="mw-page-title-main">Spermatogenesis</span> Production of sperm

Spermatogenesis is the process by which haploid spermatozoa develop from germ cells in the seminiferous tubules of the testicle. This process starts with the mitotic division of the stem cells located close to the basement membrane of the tubules. These cells are called spermatogonial stem cells. The mitotic division of these produces two types of cells. Type A cells replenish the stem cells, and type B cells differentiate into primary spermatocytes. The primary spermatocyte divides meiotically into two secondary spermatocytes; each secondary spermatocyte divides into two equal haploid spermatids by Meiosis II. The spermatids are transformed into spermatozoa (sperm) by the process of spermiogenesis. These develop into mature spermatozoa, also known as sperm cells. Thus, the primary spermatocyte gives rise to two cells, the secondary spermatocytes, and the two secondary spermatocytes by their subdivision produce four spermatozoa and four haploid cells.

<span class="mw-page-title-main">Oogenesis</span> Egg cell production process

Oogenesis, ovogenesis, or oögenesis is the differentiation of the ovum into a cell competent to further develop when fertilized. It is developed from the primary oocyte by maturation. Oogenesis is initiated in the embryonic stage.

<span class="mw-page-title-main">Sertoli cell</span> Cells found in human testes which help produce sperm

Sertoli cells are a type of sustentacular "nurse" cell found in human testes which contribute to the process of spermatogenesis as a structural component of the seminiferous tubules. They are activated by follicle-stimulating hormone (FSH) secreted by the adenohypophysis and express FSH receptor on their membranes.

Reproductive biology includes both sexual and asexual reproduction.

<span class="mw-page-title-main">Spermatogonium</span> Undifferentiated male germ cell

A spermatogonium is an undifferentiated male germ cell. Spermatogonia undergo spermatogenesis to form mature spermatozoa in the seminiferous tubules of the testis.

<span class="mw-page-title-main">Sperm</span> Male reproductive cell in anisogamous forms of sexual reproduction

Sperm is the male reproductive cell, or gamete, in anisogamous forms of sexual reproduction. Animals produce motile sperm with a tail known as a flagellum, which are known as spermatozoa, while some red algae and fungi produce non-motile sperm cells, known as spermatia. Flowering plants contain non-motile sperm inside pollen, while some more basal plants like ferns and some gymnosperms have motile sperm.

Spermatogenesis arrest is known as the interruption of germinal cells of specific cellular type, which elicits an altered spermatozoa formation. Spermatogenic arrest is usually due to genetic factors resulting in irreversible azoospermia. However some cases may be consecutive to hormonal, thermic, or toxic factors and may be reversible either spontaneously or after a specific treatment. Spermatogenic arrest results in either oligospermia or azoospermia in men. It is quite a difficult condition to proactively diagnose as it tends to affect those who have normal testicular volumes; a diagnosis can be made however through a testicular biopsy.

<span class="mw-page-title-main">Adjudin</span> Chemical compound

Adjudin (AF-2364) is a drug which is under development as a potential non-hormonal male contraceptive drug, which acts by blocking the production of sperm in the testes, but without affecting testosterone production. It is an analogue of the chemotherapy drug lonidamine, an indazole-carboxylic acid, and further studies continue to be conducted into this family of drugs as possible contraceptives.

<span class="mw-page-title-main">Sertoli cell-only syndrome</span> Medical condition

Sertoli cell-only syndrome (SCOS), also known as germ cell aplasia, is defined by azoospermia where the testicular seminiferous tubules are lined solely with sertoli cells. Sertoli cells contribute to the formation of the blood-testis barrier and aid in sperm generation. These cells respond to follicle-stimulating hormone, which is secreted by the hypothalamus and aids in spermatogenesis.

Gonocytes are the precursors of spermatogonia that differentiate in the testis from primordial germ cells around week 7 of embryonic development and exist up until the postnatal period, when they become spermatogonia. Despite some uses of the term to refer to the precursors of oogonia, it was generally restricted to male germ cells. Germ cells operate as vehicles of inheritance by transferring genetic and epigenetic information from one generation to the next. Male fertility is centered around continual spermatogonia which is dependent upon a high stem cell population. Thus, the function and quality of a differentiated sperm cell is dependent upon the capacity of its originating spermatogonial stem cell (SSC).

<span class="mw-page-title-main">Meiotic recombination checkpoint</span>

The meiotic recombination checkpoint monitors meiotic recombination during meiosis, and blocks the entry into metaphase I if recombination is not efficiently processed.

In cellular biology, a chromatoid body is a dense structure in the cytoplasm of male germ cells. It is composed mainly of RNA and RNA-binding proteins and is thus a type of RNP granule. Chromatoid body-like granules first appear in spermatocytes and condense into a single granule in round spermatids. The structure disappears again when spermatids start to elongate. The chromatoid body is crucial for spermatogenesis, but its exact role in the process is not known. Following significant strides in the understanding of small non-coding RNA mediated gene regulation and Piwi-interacting RNA (piRNA) and their roles in germline development, the function of chromatoid bodies (CBs) has been somewhat elucidated. However, due to similarities with RNP granules found in somatic cells – such as stress granules and processing bodies – chromatoid body is thought to be involved in post-transcriptional regulation of gene expression. Postmeiotic germ cell differentiation induces the accumulation of piRNAs and proteins of piRNA machinery along with several distinct RNA regulator proteins. Although evidence suggests CB involvement in mRNA regulation and small RNA mediated gene regulation, the mechanism of action remains obscure.

<span class="mw-page-title-main">Spermatogonial stem cell</span> Spermatogonium that does not differentiate into a spermatocyte

A spermatogonial stem cell (SSC), also known as a type A spermatogonium, is a spermatogonium that does not differentiate into a spermatocyte, a precursor of sperm cells. Instead, they continue dividing into other spermatogonia or remain dormant to maintain a reserve of spermatogonia. Type B spermatogonia, on the other hand, differentiate into spermatocytes, which in turn undergo meiosis to eventually form mature sperm cells.

In vitro spermatogenesis is the process of creating male gametes (spermatozoa) outside of the body in a culture system. The process could be useful for fertility preservation, infertility treatment and may further develop the understanding of spermatogenesis at the cellular and molecular level. 

The signaled by retinoic acid 8 (Stra8) gene is activated only upon stimulation by retinoic acid and expresses a cytoplasmic protein in the gonads of male and female vertebrates. This protein functions to initiate the transition between mitosis and meiosis, aiding in spermatogenesis and oogenesis. In females, its signaling begins 12.5 days after conception, is localized in the primordial germ cells of female ovaries, and ushers in the first stage of meiosis. Male expression begins postnatally and continues throughout life, matching the need of spermatogenesis compared to the limited window of oogenesis in females. Sperm of mice that had induced null mutations for Stra8 gene were able to undergo mitotic divisions, and while some sperm were able to transition into the early stages of meiosis I, but could not transition into further sub-stages of meiosis I. Errors in chromosome pairing and chromosome condensation were observed following these failures. In female mice, loss of Stra8 signaling shows failure to enter into meiosis. Both males and females are left infertile if Stra8 signaling is absent.

The germ cell nest forms in the ovaries during their development. The nest consists of multiple interconnected oogonia formed by incomplete cell division. The interconnected oogonia are surrounded by somatic cells called granulosa cells. Later on in development, the germ cell nests break down through invasion of granulosa cells. The result is individual oogonia surrounded by a single layer of granulosa cells. There is also a comparative germ cell nest structure in the developing spermatogonia, with interconnected intracellular cytoplasmic bridges.

References

  1. 1 2 3 4 5 Boron, Walter F., MD, Ph.D., Editor; Boulpaep, Emile L. (2012). "54". Medical physiology a cellular and molecular approach (Print) (Updated second ed.). Philadelphia: Saunders Elsevier. ISBN   978-1-4377-1753-2.{{cite book}}: |first1= has generic name (help)CS1 maint: multiple names: authors list (link)[ page needed ]
  2. 1 2 3 Schöni-Affolter, Dubuis-Grieder, Strauch, Franzisk, Christine, Erik Strauch. "Spermatogenesis" . Retrieved 22 March 2014.{{cite web}}: CS1 maint: multiple names: authors list (link)
  3. ↑ Riddle, DL; Blumenthal, T; Meyer, B.J.; et al., eds. (1997). "I, The Biological Model". C. elegans II (2nd ed.). Cold Spring Harbor. NY: Cold Spring Harbor Laboratory Press . Retrieved April 13, 2014.
  4. ↑ Boitani, Carla; Di Persio, Sara; Esposito, Valentina; Vicini, Elena (2016-03-05). "Spermatogonial cells: mouse, monkey and man comparison". Seminars in Cell & Developmental Biology. 59: 79–88. doi:10.1016/j.semcdb.2016.03.002. ISSN   1096-3634. PMID   26957475.
  5. ↑ Y, Clermont (1966). "Renewal of spermatogonia in man". American Journal of Anatomy. 118 (2): 509–524. doi:10.1002/aja.1001180211. PMID   5917196.
  6. ↑ Tres, Abraham L. Kierszenbaum, Laura L. (2012). Histology and cell biology : an introduction to pathology (3rd ed.). Philadelphia, PA: Saunders. pp. Chapter 20. ISBN   9780323078429.{{cite book}}: CS1 maint: multiple names: authors list (link)
  7. ↑ Starr, Taggart, Evers, Starr, Cecie, Ralph, Christine, Lisa (January 1, 2012). Animal Structure & Function. Cengage Learning. p. 736. ISBN   9781133714071.{{cite book}}: CS1 maint: multiple names: authors list (link)
  8. ↑ Sherwood, Lauralee (2010). Human physiology : from cells to systems (7th ed.). Australia: Brooks/Cole, Cengage Learning. p. 751. ISBN   978-0495391845.
  9. ↑ Matulis S, Handel MA (August 2006). "Spermatocyte responses in vitro to induced DNA damage". Molecular Reproduction and Development. 73 (8): 1061–72. doi:10.1002/mrd.20508. PMID   16700071. S2CID   21185220.
  10. 1 2 Srivastava N, Raman MJ (2007). "Homologous recombination-mediated double-strand break repair in mouse testicular extracts and comparison with different germ cell stages". Cell Biochem. Funct. 25 (1): 75–86. doi:10.1002/cbf.1375. PMID   16989005. S2CID   24830710.
  11. ↑ Walter CA, Intano GW, McCarrey JR, McMahan CA, Walter RB (1998). "Mutation frequency declines during spermatogenesis in young mice but increases in old mice". Proc. Natl. Acad. Sci. U.S.A. 95 (17): 10015–9. Bibcode:1998PNAS...9510015W. doi: 10.1073/pnas.95.17.10015 . PMC   21453 . PMID   9707592.
  12. ↑ Sciurano RB, Rahn MI, Rey-Valzacchi G, Coco R, Solari AJ (August 2012). "The role of asynapsis in human spermatocyte failure". International Journal of Andrology. 35 (4): 541–9. doi: 10.1111/j.1365-2605.2011.01221.x . PMID   21977946.
  13. ↑ Mark, Manuel; Hugues Jacobs; Mustapha Oulad-Abdelghani; Christine Dennefeld; Betty Feret; Nadege Vernet; Carmen-Alina Codreanu; Pierre Chambon; Norbert Ghyselinck (7 July 2008). "STRA8-deficient spermatocytes initiate, but fail to complete, meiosis and undergo premature chromosome condensation". Journal of Cell Science. 121 (19): 3233–3242. doi: 10.1242/jcs.035071 . PMID   18799790.
  14. ↑ Sun, Fengyun; Mary Ann Handel (10 January 2011). "A Mutation in Mtap2 is Associated with Arrest of Mammalian Spermatocytes before the First Meiotic Division". Genes. 2 (1): 21–35. doi: 10.3390/genes2010021 . PMC   3909985 . PMID   24501684.
  15. ↑ Barchi, Marco; S. Mahadevaiah; M. Di Giacomo; F. Baudat; D. de Rooij; P. Burgoyne; M. Jasin; S. Keeney (August 2005). "Surveillance of Different Recombination Defects in Mouse Spermatocytes Yields Distinct Responses despite Elimination at an Identical Developmental Stage". Molecular and Cellular Biology. 25 (16): 7203–7215. doi:10.1128/MCB.25.16.7203-7215.2005. PMC   1190256 . PMID   16055729.
  16. ↑ Cheng, C. Yan, ed. (2008). Molecular mechanisms in spermatogenesis . New York: Springer Science+Business Media. pp. Chapter 1, page 1. ISBN   978-0-387-79990-2.
  17. 1 2 Cheng, C. Yan; Dolores D. Mruk (19 April 2010). "The biology of spermatogenesis: the past, present and future". Phil. Trans. R. Soc. B. 1546. 365 (1546): 1459–1463. doi:10.1098/rstb.2010.0024. PMC   2871927 . PMID   20403863.
  18. ↑ Riparbelli MG, Cabrera OA, Callaini G, Megraw TL (2013). "Unique properties of Drosophila spermatocyte primary cilia". Biology Open. 2 (11): 1137–47. doi:10.1242/bio.20135355. PMC   3828760 . PMID   24244850.
  19. ↑ Ferraro-Gideon J, Hoang C, Forer A (January 2014). "Meiosis-I in Mesostoma ehrenbergii spermatocytes includes distance segregation and inter-polar movements of univalents, and vigorous oscillations of bivalents". Protoplasma. 251 (1): 127–43. doi:10.1007/s00709-013-0532-9. PMID   23921676. S2CID   59941923.
  20. ↑ Ferraro-Gideon J, Hoang C, Forer A (September 2013). "Mesostoma ehrenbergii spermatocytes--a unique and advantageous cell for studying meiosis". Cell Biology International. 37 (9): 892–8. doi:10.1002/cbin.10130. hdl: 10315/38106 . PMID   23686688. S2CID   13210761.

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