Fusome

Last updated
Drosophila ovariole: spectrosomes are the red round structures in germline stem cells. The red branched structures in 2-cell and 8-cell cysts are the fusomes. Ovariole niche.png
Drosophila ovariole: spectrosomes are the red round structures in germline stem cells. The red branched structures in 2-cell and 8-cell cysts are the fusomes.

The fusome is a membranous structure found in the developing germ cell cysts of many insect orders. [1] [2] [3] Initial description of the fusome occurred in the 19th century and since then the fusome has been extensively studied in Drosophila melanogaster male and female germline development. [3] This structure has roles in maintaining germline cysts, coordinating the number of mitotic divisions prior to meiosis, and oocyte determination by serving as a structure for intercellular communication. [3] [4] [5]

Contents

A wild type D. melanogaster testis showing the fusome (spectrin, green), DNA (DAPI, blue), and germ cells (vasa, red). The fusome connects cells in a cyst and becomes branched as the cyst grows with cell divisions. Image by S. Brantley, used with permission by the author. D melanogaster testis fusome.tif
A wild type D. melanogaster testis showing the fusome (spectrin, green), DNA (DAPI, blue), and germ cells (vasa, red). The fusome connects cells in a cyst and becomes branched as the cyst grows with cell divisions. Image by S. Brantley, used with permission by the author.

Structure

In D. melanogaster, germline cysts form from four mitotic divisions with incomplete cytokinesis that originated from one germline stem cell. [6] [7] Incomplete cytokinesis results in intercellular bridges connecting every cell in the cyst, called ring canals3. The four mitotic divisions result in cysts of 16 cells connected by 15 ring canals. [6] [7] The fusome is composed of membrane vesicles and originates from endoplasmic reticulum. [2] Fusome material is inside ring canals and can range in size from 1 to 10 um depending on the stage of development. [1] [3]

1.1 Fusome Development

The spectrosome is a round structure in germline stem cells that develops into the fusome in cyst cells. [8] Fusome divides asymmetrically into daughter cells in females by attaching to one spindle pole during meiosis, resulting in one cell receiving all fusome material. [1] [8] [9] [10] Fusome is generated de novo in the ring canal connecting the two cells. [1] [9] [10] The two fusome parts then fuse together to connect the cells. [1] Asymmetric fusome partitioning and new formation followed by fusion occurs at each mitotic division. [1] In spermatogenesis, the fusome partitioning is symmetric and the fusome is still present during the meiotic divisions. [3] [11]

1.2 Fusome components

Many proteins and organelles associate with the fusome throughout germ cell development. Cytoskeleton components, such as alpha and beta spectrins, hu-li tai shao (hts), and ankyrin were the first proteins identified in the fusome. [4] [12] Centrosomes travel along the fusome and the fusome is involved in microtubule organization. [4] [13] The interactions between the fusome and microtubules result in cyst polarity in oogenesis. [12] Associations between the fusome and microtubules change throughout the cell cycle. [13] Mitochondria associates with the fusome and travel through ring canals to the oocyte. [14] Microtubules travel through ring canals and form the tracks for transport of materials between cells. [10]

Function

There are numerous functions of the fusome as a structure necessary for cell-cell communication in developing germ cell cysts. The fusome connects cells, allowing for transport of proteins and RNAs between cells and synchronous activities. [3] [8] Mutations in essential fusome components can result in infertility. [3]

2.1 Role in cell cycle synchrony

Developing cells in germline cysts undergo mitotic divisions synchronously and in males all cells in a cyst also undergo meiosis synchronously. [7] The fusome is a track where an event can happen and then feedback mechanisms quickly communicate to each cell to ensure a specific outcome occurs simultaneously in every cell. [5] Cells in a cyst fail to divide synchronously if the fusome is disrupted. [4] [15] The rosette formation of germline cyst cells allows cells to be in the closest configuration for communication. [9]

Throughout the cell cycle, different cyclins associate with the fusome to induce synchronous cell divisions. Cyclin A and Cyclin E localize to the fusome in female germline cysts and are required for the correct number of mitotic divisions to occur. [5] [16] Abnormal cyclin levels result in too few or too many divisions. [5] [16] Cyclin E at the fusome is phosphorylated for degradation by the SCF complex and if not degraded, an extra division occurs. [16] The fusome may be the degradation site for other cell cycle proteins. [16] Myt1 kinase inhibits CycA/Cdk1 in males during G2. [17] Without Myt1 regulation, fusome and centrosome behavior is abnormal, resulting in cells with irregular spindles. [17]

2.2 Differences in male vs female fusomes

In females, the fusome plays a role in cell fate and differentiation. [9] Asymmetric fusome distribution and centriole orientation determines which cell in the developing female germline cyst becomes the oocyte. [8] One of the two cells from the first division within the cyst becomes the oocyte and contains the most fusome material. [3] [9] The fusome degrades after the 16-cell cyst forms. [3] In females, the connections are the channels through which nurse cells send proteins and RNAs to the oocyte along polarized microtubules. [10]

In males, the fusome is necessary for ensuring quality control in individual cysts. DNA damage in one cell leads to all cells in a cyst dying by communication through the fusome, either by disseminating a death signal or additive DNA damage inducing apoptosis. [18] This ensures mature sperm cells have intact genomes before fertilizing an egg. [18] In addition, the fusome connections ensure haploid spermatids have proteins and RNA made by the other chromosome for “gamete equivalency”. [3] [19]

Similar structures in other animals

Fusomes were previously thought to be specific to insect gametogenesis. Fusome-like structures have been identified in Xenopus laevis oogenesis by electron microscopy and immunostaining for fusome components such as spectrin and hts. [20] Intercellular bridges also connect developing germ cells in mammals, contributing to cell cycle synchrony and gamete quality control by sharing substances between cells. [3] Future studies are required to elucidate all of the functions that arise from cell-cell communication through intercellular bridges. [3] In addition, a future area of research is to determine why some organisms lack fusomes. Do these organisms have another structure that carries out the role of the fusome or are these roles not necessary in germline cyst development of these other organisms?

See also

Related Research Articles

Cell division Process resulting in division and partitioning of components of a cell to form more cells; may or may not be accompanied by the physical separation of a cell into distinct, individually membrane-bounded daughter cells.

Cell division is the process by which a parent cell divides into two or more daughter cells. Cell division usually occurs as part of a larger cell cycle. In eukaryotes, there are two distinct types of cell division; a vegetative division, whereby each daughter cell is genetically identical to the parent cell (mitosis), and a reproductive cell division, whereby the number of chromosomes in the daughter cells is reduced by half to produce haploid gametes (meiosis). In cell biology, mitosis (/maɪˈtoʊsɪs/) is a part of the cell cycle, in which, replicated chromosomes are separated into two new nuclei. Cell division gives rise to genetically identical cells in which the total number of chromosomes is maintained. In general, mitosis is preceded by the S stage of interphase and is often followed by telophase and cytokinesis; which divides the cytoplasm, organelles and cell membrane of one cell into two new cells containing roughly equal shares of these cellular components. The different stages of mitosis all together define the mitotic (M) phase of an animal cell cycle—the division of the mother cell into two genetically identical daughter cells. Meiosis results in four haploid daughter cells by undergoing one round of DNA replication followed by two divisions. Homologous chromosomes are separated in the first division, and sister chromatids are separated in the second division. Both of these cell division cycles are used in the process of sexual reproduction at some point in their life cycle. Both are believed to be present in the last eukaryotic common ancestor.

Cytokinesis Part of the cell division process

Cytokinesis is the part of the cell division process during which the cytoplasm of a single eukaryotic cell divides into two daughter cells. Cytoplasmic division begins during or after the late stages of nuclear division in mitosis and meiosis. During cytokinesis the spindle apparatus partitions and transports duplicated chromatids into the cytoplasm of the separating daughter cells. It thereby ensures that chromosome number and complement are maintained from one generation to the next and that, except in special cases, the daughter cells will be functional copies of the parent cell. After the completion of the telophase and cytokinesis, each daughter cell enters the interphase of the cell cycle.

Spindle apparatus Array of microtubules and associated molecules that forms between opposite poles of a eukaryotic cell during mitosis or meiosis and serves to move the duplicated chromosomes apart

In cell biology, the spindle apparatus refers to the cytoskeletal structure of eukaryotic cells that forms during cell division to separate sister chromatids between daughter cells. It is referred to as the mitotic spindle during mitosis, a process that produces genetically identical daughter cells, or the meiotic spindle during meiosis, a process that produces gametes with half the number of chromosomes of the parent cell.

Egg cell Female reproductive cell in most anisogamous organisms

The egg cell, or ovum, is the female reproductive cell, or gamete, in most anisogamous organisms. The term is used when the female gamete is not capable of movement (non-motile). If the male gamete (sperm) is capable of movement, the type of sexual reproduction is also classified as oogamous. A nonmotile female gamete formed in the oogonium of some algae, fungi, oomycetes, or bryophytes is an oosphere. When fertilized the oosphere becomes the oospore.

Germ cell Gamete-producing cell

A germ cell is any biological 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.

An oocyte, oöcyte, ovocyte, or rarely ocyte, is a female gametocyte or germ cell involved in reproduction. In other words, it is an immature ovum, or egg cell. An oocyte is produced in the ovary during female gametogenesis. The female germ cells produce a primordial germ cell (PGC), which then undergoes mitosis, forming oogonia. During oogenesis, the oogonia become primary oocytes. An oocyte is a form of genetic material that can be collected for cryoconservation.

Oogenesis

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.

<i>Drosophila</i> embryogenesis Embryogenesis of the fruit fly Drosophila, a popular model system

Drosophila embryogenesis, the process by which Drosophila embryos form, is a favorite model system for genetics and developmental biology. The study of its embryogenesis unlocked the century-long puzzle of how development was controlled, creating the field of evolutionary developmental biology. The small size, short generation time, and large brood size make it ideal for genetic studies. Transparent embryos facilitate developmental studies. Drosophila melanogaster was introduced into the field of genetic experiments by Thomas Hunt Morgan in 1909.

Maturation-promoting factor (abbreviated MPF, also called mitosis-promoting factor or M-Phase-promoting factor) is the cyclin-Cdk complex that was discovered first in frog eggs. It stimulates the mitotic and meiotic phases of the cell cycle. MPF promotes the entrance into mitosis (the M phase) from the G2 phase by phosphorylating multiple proteins needed during mitosis. MPF is activated at the end of G2 by a phosphatase, which removes an inhibitory phosphate group added earlier.

An oogonium is a small diploid cell which, upon maturation, forms a primordial follicle in a female fetus or the female gametangium of certain thallophytes.

Endoreduplication is replication of the nuclear genome in the absence of mitosis, which leads to elevated nuclear gene content and polyploidy. Endoreplication can be understood simply as a variant form of the mitotic cell cycle (G1-S-G2-M) in which mitosis is circumvented entirely, due to modulation of cyclin-dependent kinase (CDK) activity. Examples of endoreplication characterized in arthropod, mammalian, and plant species suggest that it is a universal developmental mechanism responsible for the differentiation and morphogenesis of cell types that fulfill an array of biological functions. While endoreplication is often limited to specific cell types in animals, it is considerably more widespread in plants, such that polyploidy can be detected in the majority of plant tissues.

Stem-cell niche refers to a microenvironment, within the specific anatomic location where stem cells are found, which interacts with stem cells to regulate cell fate. The word 'niche' can be in reference to the in vivo or in vitro stem-cell microenvironment. During embryonic development, various niche factors act on embryonic stem cells to alter gene expression, and induce their proliferation or differentiation for the development of the fetus. Within the human body, stem-cell niches maintain adult stem cells in a quiescent state, but after tissue injury, the surrounding micro-environment actively signals to stem cells to promote either self-renewal or differentiation to form new tissues. Several factors are important to regulate stem-cell characteristics within the niche: cell–cell interactions between stem cells, as well as interactions between stem cells and neighbouring differentiated cells, interactions between stem cells and adhesion molecules, extracellular matrix components, the oxygen tension, growth factors, cytokines, and the physicochemical nature of the environment including the pH, ionic strength and metabolites, like ATP, are also important. The stem cells and niche may induce each other during development and reciprocally signal to maintain each other during adulthood.

oskar is a gene required for the development of the Drosophila embryo. It defines the posterior pole during early embryogenesis. Its two isoforms, short and long, play different roles in Drosophila embryonic development. oskar was named after the main character from the Günter Grass novel The Tin Drum, who refuses to grow up.

PRC1

Protein Regulator of cytokinesis 1 (PRC1) is a protein that in humans is encoded by the PRC1 gene and is involved in cytokinesis.

Maternal to zygotic transition is the stage in embryonic development during which development comes under the exclusive control of the zygotic genome rather than the maternal (egg) genome. The egg contains stored maternal genetic material mRNA which controls embryo development until the onset of MZT. After MZT the diploid embryo takes over genetic control. This requires both zygotic genome activation (ZGA) and degradation of maternal products. This process is important because it is the first time that the new embryonic genome is utilized and the paternal and maternal genomes are used in combination. The zygotic genome now drives embryo development.

Vasa is an RNA binding protein with an ATP-dependent RNA helicase that is a member of the DEAD box family of proteins. The vasa gene, is essential for germ cell development and was first identified in Drosophila melanogaster, but has since been found to be conserved in a variety of vertebrates and invertebrates including humans. The Vasa protein is found primarily in germ cells in embryos and adults, where it is involved in germ cell determination and function, as well as in multipotent stem cells, where its exact function is unknown.

In molecular biology, the BESS domain is a protein domain which has been named after the three proteins that originally defined the domain: BEAF, Suvar(3)7 and Stonewall ). The BESS domain is 40 amino acid residues long and is predicted to be composed of three alpha helices, as such it might be related to the myb/SANT HTH domain. The BESS domain directs a variety of protein-protein interactions, including interactions with itself, with Dorsal, and with a TBP-associated factor. It is found in a single copy in Drosophila proteins and is often associated with the MADF domain.

The gene Maelstrom, Mael, creates a protein, which was first located in Drosophila melanogaster in the nuage perinuclear structure and has functionality analogous to the spindle, spn, gene class. Its mamallian homolog is MAEL.

<i>Bicoid</i> (gene)

Bicoid is a maternal effect gene whose protein concentration gradient patterns the anterior-posterior (A-P) axis during Drosophila embryogenesis. Bicoid was the first protein demonstrated to act as a morphogen. Although Bicoid is important for the development of Drosophila and other higher dipterans, it is absent from most other insects, where its role is accomplished by other genes.

Oogonial stem cells (OSCs), also known as egg precursor cells or female germline cells, are diploid germline cells with stem cell characteristics: the ability to renew and differentiate into other cell types, different from their tissue of origin. Present in invertebrates and some lower vertebrate species, they have been extensively studied in Caenorhabditis elegans, Drosophila melanogaster. OSCs allow the production of new female reproductive cells (oocytes) by the process of oogenesis during an organism's reproductive life.

References

  1. 1 2 3 4 5 6 Telfer, W. H. 1975. Development and physiology of the oocyte-nurse cell syncytium. Advances in insect physiology 11:223-319. DOI: 10.1016/S0065-2806(08)60164-2
  2. 1 2 Snapp, E. L., T. Iida, D. Frescas, J. Lippincott-Schwartz, and M. A. Lilly. (2004). The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts. Mol Biol Cell 15: 4512-4521. doi/10.1091/mbc.E04 – 06 – 0475.
  3. 1 2 3 4 5 6 7 8 9 10 11 12 Greenbaum, M. P., T. Iwarmori, G. M. Buchold, and M. M. Matzuk. (2011). Germ Cell Intercellular Bridges. Cold Spring Harb Perspect Biol 3:a005850 doi: 10.1101/cshperspect.a005850
  4. 1 2 3 4 de Cuevas, M., J. K. Lee, A. C. Spradling. (1996) α-spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 122: 3959-3968.
  5. 1 2 3 4 Lilly, M. A., M. de Cuevas, and A. C. Spradling. (2000). Cyclin A associates with the fusome during germline cyst formation in the Drosophila ovary. Developmental Biology 218: 53-63. doi:10.1006/dbio.1999.9570
  6. 1 2 Spradling, A. C. (1993). Developmental genetics of oogenesis. In The Development of Drosophila, M. Bate and A. Martinez-Arias, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Press), pp. 1–70.   
  7. 1 2 3 Fuller, M.T. (1993). Spermatogenesis. In The Development of Drosophila, M. Bate and A. Martinez-Arias, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Press), pp. 71–147.
  8. 1 2 3 4 Lin, H. and Spradling, A. C. (1995). Fusome asymmetry and oocyte determination in Drosophila. Dev. Genet.16: 6-12.   
  9. 1 2 3 4 5 de Cuevas, M. and A. C. Spradling. (1998). Morphogenesis of the Drosophila fusome and its implicaitons for oocyte specification. Development 125: 2781-2789.
  10. 1 2 3 4 Roth, S. and J. A. Lynch. (2009). Symmetry breaking during Drosophila oogenesis. Cold Spring Harb Perspect Biol 1:a001891 doi: 10.1101/cshperspect.a001891
  11. ↑ Hime, G. R., J. A. Brill, M. T. Fuller. (1996). Assembly of ring canals in the male germ line from structural components of the contractile ring. J. Cell Sci 109: 2779-2788   
  12. 1 2 Lin, H., L. Yue, and A. C. Spradling. (1994). The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120: 947-956.
  13. 1 2 Grieder, N., M. de Cuevas, and A. C. Spradling. (2000). The fusome organizes the microtubule network during oocyte differentiation in Drosophila. Development 127: 4253-4264.
  14. ↑ Cox, R. T. and A. C. Spradling. (2003) A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130: 1579-1590 doi:10.1242/dev.00365
  15. ↑ Deng, W. and H. Lin. (1997). Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarizes microtubules array for oocyte specification in Drosophila. Dev Biol 189: 79-94.   
  16. 1 2 3 4 Ohlmeyer, J. T. and T. Schupbach. (2003). Encore facilitates SCF-Ubiquitin-proteosome-dependent proteolysis during Drosophila oogenesis. Development 130: 6339-6349. doi:10.1242/dev.00855
  17. 1 2 Varadarajan, R., J. Ayeni, Z. Jin, E. Homola, S. D. Campbell. (2016).Myt1 inhibition of Cyclin A/Cdk1 is essential for fusome integrity and premeiotic centriole engagement in Drosophila spermatocytes. MBoC 27: 2051-2063. doi.org/10.1091/mbc.E16-02-0104   
  18. 1 2 Lu, K. L. and Y. M. Yamashita. (2017). Germ cell connectivity enhances cell death in response to DNA damage in the Drosophila testis. eLife 6:e27960. doi.org/10.7554/eLife.27960
  19. ↑ Braun, R. E., R. R. Behringer, J. J. Peschon, R. L. Brinster, and R. D. Palmiter. (1989). Genetically haploid spermatids are phenotypically diploid. Nature 337: 373-376.
  20. ↑ Kloc, M., S. Bilinski, M. T. Dougherty, E. M. Brey, and L. D. Etkin. (2004). Formation, architecture and polarity of female germline cyst in Xenopus. Dev Biol 266: 43-61. doi:10.1016/j.ydbio.2003.10.002

^PG Wilson Cell Biol Int. 2005 May;29(5):360-9.

Centrosome inheritance in the male germ line of Drosophila requires hu-li tai-shao function.

This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.