Symmetry breaking and cortical rotation

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Symmetry breaking in biology is the process by which uniformity is broken, or the number of points to view invariance are reduced, to generate a more structured and improbable state. [1] Symmetry breaking is the event where symmetry along a particular axis is lost to establish a polarity. Polarity is a measure for a biological system to distinguish poles along an axis. This measure is important because it is the first step to building complexity. For example, during organismal development, one of the first steps for the embryo is to distinguish its dorsal-ventral axis. The symmetry-breaking event that occurs here will determine which end of this axis will be the ventral side, and which end will be the dorsal side. Once this distinction is made, then all the structures that are located along this axis can develop at the proper location. As an example, during human development, the embryo needs to establish where is ‘back’ and where is ‘front’ before complex structures, such as the spine and lungs, can develop in the right location (where the lungs are placed ‘in front’ of the spine). This relationship between symmetry breaking and complexity was articulated by P.W. Anderson. He speculated that increasing levels of broken symmetry in many-body systems correlates with increasing complexity and functional specialization. [2] In a biological perspective, the more complex an organism is, the higher number of symmetry-breaking events can be found.

Contents

The importance of symmetry breaking in biology is also reflected in the fact that it's found at all scales. Symmetry breaking can be found at the macromolecular level, [3] at the subcellular level [4] and even at the tissues and organ level. [5] It's also interesting to note that most asymmetry on a higher scale is a reflection of symmetry breaking on a lower scale. Cells first need to establish a polarity through a symmetry-breaking event before tissues and organs themselves can be polar. For example, one model proposes that left-right body axis asymmetry in vertebrates is determined by asymmetry of cilia rotation during early development, which will produce a constant, unidirectional flow. [6] [7] However, there is also evidence that earlier asymmetries in serotonin distribution and ion-channel mRNA and protein localization occur in zebrafish, chicken and Xenopus development, [8] [9] [10] and similar to observations of intrinsic chirality generated by the cytoskeleton [11] [12] leading to organ and whole organism asymmetries in Arabidopsis [13] [14] [15] [16] this itself seems to be controlled from the macromolecular level by the cytoskeleton. [10]

There are several examples of symmetry breaking that are currently being studied. One of the most studied examples is the cortical rotation during Xenopus development, where this rotation acts as the symmetry-breaking event that determines the dorsal-ventral axis of the developing embryo. This example is discussed in more detail below.
Another example that involves symmetry breaking is the establishment of dendrites and axon during neuron development, and the PAR protein network in C. elegans . It is thought that a protein called shootin-1 determines which outgrowth in neurons eventually becomes the axon, at it does this by breaking symmetry and accumulating in only one outgrowth. [17] The PAR protein network works under similar mechanisms, where the certain PAR proteins, which are initially homogenous throughout the cell, break their symmetry and are segregated to different ends of the zygote to establish a polarity during development. [18]

Cortical rotation

Cortical rotation is a phenomenon that seems to be limited to Xenopus and few ancient teleosts, however the underlying mechanisms of cortical rotation have conserved elements that are found in other chordates.

A sperm can bind a Xenopus egg at any position of the pigmented animal hemisphere; however, once bound, this position then determines the dorsal side of the animal. The dorsal side of the egg is always directly opposite the sperm entry point. The sperm's centriole acts as an organizing center for the egg's microtubules, which transport the maternal dorsalizing factors, such as wnt11 mRNA, wnt5a mRNA, and Dishevelled protein. [19]

Molecular mechanisms

A series of experiments utilizing UV irradiation, cold temperature and pressure (all of which cause microtubule depolymerization) demonstrated that without polymerized microtubules, cortical rotation did not occur and resulted in a mutant ventral phenotype. [20] Another study also revealed that mutant phenotype could be rescued (returned to normal) by physically turning the embryo, thus mimicking cortical rotation and demonstrating that microtubules were not the determinant of dorsal development. [21] From this it was hypothesized that there were other elements within the embryo being moved during cortical rotation.

To identify these elements, researchers looked for mRNA and protein that demonstrated localization to either the vegetal pole or the dorsal side of the embryo to find candidates. The early candidates for the determinant were β-catenin and disheveled (Dsh). [22] [23] When maternal β-catenin mRNA was degraded in the oocyte, the resulting embryo developed into mutant ventral phenotype and this could be rescued by injecting the fertilized egg with β-catenin mRNA. β-catenin is obversed to be enriched in the dorsal side of the embryo following cortical rotation. The Dsh protein was fused to a GFP and tracked during cortical rotation, it was observed to be in vesicles that were couriered along microtubules to the dorsal side. This led researchers to look into other candidates of the Wnt pathway. Wnt 11 was found to be located specifically at the vegetal pole prior to cortical rotation and is moved to the dorsal side where it activates the wnt signaling pathway. [24] VegT, a T-box transcription factor, is localized to the vegetal cortex and upon cortical rotation is released in a gradient fashion into the embryo to regulate mesoderm development. [25] VegT activates Wnt expression, so while not acted on or moved during cortical rotation, it is active in dorsal-ventral axis formation.

The question still remains, how are these molecules being moved to the dorsal side? This is still not completely known, however evidence suggests that microtubule bundles within the cortex are interacting with kinesin (plus-end directed) motors to become organized into parallel arrays within the cortex and this motion of the motors is the cause of the rotation of the cortex. [26] Also unclear is whether Wnt 11 is the main dorsal determinant or is β-catenin also required, as these two molecules have both been demonstrated to be necessary and sufficient for dorsal development. This along with all of the other factors are important for activating Nodal genes that propagate normal dorsoventral development.

Related Research Articles

<i>Xenopus</i> Genus of amphibians

Xenopus is a genus of highly aquatic frogs native to sub-Saharan Africa. Twenty species are currently described within it. The two best-known species of this genus are Xenopus laevis and Xenopus tropicalis, which are commonly studied as model organisms for developmental biology, cell biology, toxicology, neuroscience and for modelling human disease and birth defects.

<span class="mw-page-title-main">Blastulation</span> Sphere of cells formed during early embryonic development in animals

Blastulation is the stage in early animal embryonic development that produces the blastula. In mammalian development the blastula develops into the blastocyst with a differentiated inner cell mass and an outer trophectoderm. The blastula is a hollow sphere of cells known as blastomeres surrounding an inner fluid-filled cavity called the blastocoel. Embryonic development begins with a sperm fertilizing an egg cell to become a zygote, which undergoes many cleavages to develop into a ball of cells called a morula. Only when the blastocoel is formed does the early embryo become a blastula. The blastula precedes the formation of the gastrula in which the germ layers of the embryo form.

<span class="mw-page-title-main">Gastrulation</span> Stage in embryonic development in which germ layers form

Gastrulation is the stage in the early embryonic development of most animals, during which the blastula, or in mammals the blastocyst is reorganized into a multilayered structure known as the gastrula. Before gastrulation, the embryo is a continuous epithelial sheet of cells; by the end of gastrulation, the embryo has begun differentiation to establish distinct cell lineages, set up the basic axes of the body, and internalized one or more cell types including the prospective gut.

An oocyte, oöcyte, or ovocyte 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 a female fetus 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.

<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.

<span class="mw-page-title-main">Symmetry in biology</span> Geometric symmetry in living beings

Symmetry in biology refers to the symmetry observed in organisms, including plants, animals, fungi, and bacteria. External symmetry can be easily seen by just looking at an organism. For example, the face of a human being has a plane of symmetry down its centre, or a pine cone displays a clear symmetrical spiral pattern. Internal features can also show symmetry, for example the tubes in the human body which are cylindrical and have several planes of symmetry.

The Wnt signaling pathways are a group of signal transduction pathways which begin with proteins that pass signals into a cell through cell surface receptors. The name Wnt is a portmanteau created from the names Wingless and Int-1. Wnt signaling pathways use either nearby cell-cell communication (paracrine) or same-cell communication (autocrine). They are highly evolutionarily conserved in animals, which means they are similar across animal species from fruit flies to humans.

<span class="mw-page-title-main">Catenin beta-1</span> Mammalian protein found in Homo sapiens

Catenin beta-1, also known as beta-catenin (β-catenin), is a protein that in humans is encoded by the CTNNB1 gene.

An asymmetric cell division produces two daughter cells with different cellular fates. This is in contrast to symmetric cell divisions which give rise to daughter cells of equivalent fates. Notably, stem cells divide asymmetrically to give rise to two distinct daughter cells: one copy of the original stem cell as well as a second daughter programmed to differentiate into a non-stem cell fate.

<span class="mw-page-title-main">Polarity in embryogenesis</span> Division of an embryo into two hemispheres (animal and vegetal poles)

In developmental biology, an embryo is divided into two hemispheres: the animal pole and the vegetal pole within a blastula. The animal pole consists of small cells that divide rapidly, in contrast with the vegetal pole below it. In some cases, the animal pole is thought to differentiate into the later embryo itself, forming the three primary germ layers and participating in gastrulation.

In the field of developmental biology, regional differentiation is the process by which different areas are identified in the development of the early embryo. The process by which the cells become specified differs between organisms.

<span class="mw-page-title-main">Cerberus (protein)</span> Protein-coding gene in the species Homo sapiens

Cerberus is a protein that in humans is encoded by the CER1 gene. Cerberus is a signaling molecule which contributes to the formation of the head, heart and left-right asymmetry of internal organs. This gene varies slightly from species to species but its overall functions seem to be similar.

<span class="mw-page-title-main">ZIC3</span> Protein-coding gene in the species Homo sapiens

ZIC3 is a member of the Zinc finger of the cerebellum (ZIC) protein family.

<span class="mw-page-title-main">Dishevelled</span> Family of proteins

Dishevelled (Dsh) is a family of proteins involved in canonical and non-canonical Wnt signalling pathways. Dsh is a cytoplasmic phosphoprotein that acts directly downstream of frizzled receptors. It takes its name from its initial discovery in flies, where a mutation in the dishevelled gene was observed to cause improper orientation of body and wing hairs. There are vertebrate homologs in zebrafish, Xenopus (Xdsh), mice and humans. Dsh relays complex Wnt signals in tissues and cells, in normal and abnormal contexts. It is thought to interact with the SPATS1 protein when regulating the Wnt Signalling pathway.

<span class="mw-page-title-main">Cell polarity</span> Polar morphology of a cell, a specific orientation of the cell structure

Cell polarity refers to spatial differences in shape, structure, and function within a cell. Almost all cell types exhibit some form of polarity, which enables them to carry out specialized functions. Classical examples of polarized cells are described below, including epithelial cells with apical-basal polarity, neurons in which signals propagate in one direction from dendrites to axons, and migrating cells. Furthermore, cell polarity is important during many types of asymmetric cell division to set up functional asymmetries between daughter cells.

The Nodal signaling pathway is a signal transduction pathway important in regional and cellular differentiation during embryonic development.

<i>Homeotic protein bicoid</i> Protein-coding gene in the species Drosophila melanogaster

Homeotic protein bicoid is encoded by the bcd maternal effect gene in Drosophilia. Homeotic protein bicoid 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.

Left-right asymmetry is the process in early embryonic development that breaks the normal symmetry in the bilateral embryo. In vertebrates, left-right asymmetry is established early in development at a structure called the left-right organizer and leads to activation of different signalling pathways on the left and right of the embryo. This in turn cause several organs in adults to develop LR asymmetry, such as the tilt of the heart, the different number lung lobes on each side of the body and the position of the stomach and spleen on the right side of the body. If this process does not occur correctly in humans it can result in the syndromes heterotaxy or situs inversus.

<span class="mw-page-title-main">Dorsal lip</span>

The dorsal lip of the blastopore is a structure that forms during early embryonic development and is important for its role in organizing the germ layers. The dorsal lip is formed during early gastrulation as folding of tissue along the involuting marginal zone of the blastocoel forms an opening known as the blastopore. It is particularly important for its role in neural induction through the default model, where signaling from the dorsal lip protects a region of the epiblast from becoming epidermis, thus allowing it to develop to its default neural tissue.

A developmental signaling center is defined as a group of cells that release various morphogens which can determine the fates, or destined cell types, of adjacent cells. This process in turn determines what tissues the adjacent cells will form. Throughout the years, various development signaling centers have been discovered.

References

  1. ↑ Li, Rong; Bruce Bowerman (2010). "Symmetry Breaking in Biology". Cold Spring Harbor Perspectives in Biology. 2 (3): a003475. doi:10.1101/cshperspect.a003475. PMC   2829966 . PMID   20300216.
  2. ↑ Anderson, Philip W. (1972). "More is Different". Science. 177 (4047): 393–396. Bibcode:1972Sci...177..393A. doi:10.1126/science.177.4047.393. PMID   17796623. S2CID   34548824.
  3. ↑ Wong, Fei (2009). "The Signaling Mechanisms Underlying Cell Polarity and Chemotaxis". Cold Spring Harbor Perspectives in Biology. 1 (4): a002980. doi:10.1101/cshperspect.a002980. PMC   2773618 . PMID   20066099.
  4. ↑ Dworkin, Jonathan (2009). "Cellular Polarity in Prokaryotic Organisms". Cold Spring Harbor Perspectives in Biology. 1 (6): a003368. doi:10.1101/cshperspect.a003368. PMC   2882128 . PMID   20457568.
  5. ↑ Nelson, James W. (2009). "Remodeling epithelial cell organization: Transitions between front-rear and apical-basal polarity". Cold Spring Harbor Perspectives in Biology. 1 (1): a000513. doi:10.1101/cshperspect.a000513. PMC   2742086 . PMID   20066074.
  6. ↑ Babu, Deepak; Sudipto Roy (2013). "Left–right asymmetry: cilia stir up new surprises in the node". Open Biology. 3 (5): 130052. doi:10.1098/rsob.130052. PMC   3866868 . PMID   23720541.
  7. ↑ Kuznetsov, A. V.; Blinov, D. G.; Avramenko, A. A.; Shevchuk, I. V.; Tyrinov, A. I.; Kuznetsov, I. A. (13 December 2013). "Approximate modelling of the leftward flow and morphogen transport in the embryonic node by specifying vorticity at the ciliated surface". Journal of Fluid Mechanics. 738: 492–521. doi:10.1017/jfm.2013.588. S2CID   123959453.
  8. ↑ Fukumoto, Takahiro; Kema, Ido P.; Levin, Michael (2005-10-05). "Serotonin Signaling Is a Very Early Step in Patterning of the Left-Right Axis in Chick and Frog Embryos". Current Biology. 15 (9): 794–803. doi: 10.1016/j.cub.2005.03.044 . ISSN   0960-9822. PMID   15886096. S2CID   14567423.
  9. ↑ Aw, Sherry; Adams, Dany S.; Qiu, Dayong; Levin, Michael (2008-03-01). "H,K-ATPase protein localization and Kir4.1 function reveal concordance of three axes during early determination of left–right asymmetry". Mechanisms of Development. 125 (3–4): 353–372. doi:10.1016/j.mod.2007.10.011. PMC   2346612 . PMID   18160269.
  10. 1 2 Lobikin, Maria; Wang, Gang; Xu, Jingsong; Hsieh, Yi-Wen; Chuang, Chiou-Fen; Lemire, Joan M.; Levin, Michael (2012-07-31). "Early, nonciliary role for microtubule proteins in left–right patterning is conserved across kingdoms". Proceedings of the National Academy of Sciences. 109 (31): 12586–12591. Bibcode:2012PNAS..10912586L. doi: 10.1073/pnas.1202659109 . ISSN   0027-8424. PMC   3412009 . PMID   22802643.
  11. ↑ Xu, Jingsong; Keymeulen, Alexandra Van; Wakida, Nicole M.; Carlton, Pete; Berns, Michael W.; Bourne, Henry R. (2007-05-29). "Polarity reveals intrinsic cell chirality". Proceedings of the National Academy of Sciences. 104 (22): 9296–9300. Bibcode:2007PNAS..104.9296X. doi: 10.1073/pnas.0703153104 . ISSN   0027-8424. PMC   1890488 . PMID   17517645.
  12. ↑ Wan, Leo Q.; Ronaldson, Kacey; Park, Miri; Taylor, Grace; Zhang, Yue; Gimble, Jeffrey M.; Vunjak-Novakovic, Gordana (2011-07-26). "Micropatterned mammalian cells exhibit phenotype-specific left-right asymmetry". Proceedings of the National Academy of Sciences. 108 (30): 12295–12300. Bibcode:2011PNAS..10812295W. doi: 10.1073/pnas.1103834108 . ISSN   0027-8424. PMC   3145729 . PMID   21709270.
  13. ↑ Nakamura, Masayoshi; Hashimoto, Takashi (2009-07-01). "A mutation in the Arabidopsis γ-tubulin-containing complex causes helical growth and abnormal microtubule branching". Journal of Cell Science. 122 (13): 2208–2217. doi: 10.1242/jcs.044131 . ISSN   0021-9533. PMID   19509058.
  14. ↑ Abe, Tatsuya; Thitamadee, Siripong; Hashimoto, Takashi (2004-02-15). "Microtubule Defects and Cell Morphogenesis in the lefty1lefty2 Tubulin Mutant of Arabidopsis thaliana". Plant and Cell Physiology. 45 (2): 211–220. doi: 10.1093/pcp/pch026 . ISSN   0032-0781. PMID   14988491.
  15. ↑ Ishida, Takashi; Hashimoto, Takashi (2007-07-20). "An Arabidopsis thaliana tubulin mutant with conditional root-skewing phenotype". Journal of Plant Research. 120 (5): 635–640. doi:10.1007/s10265-007-0105-0. ISSN   0918-9440. PMID   17641820. S2CID   22444051.
  16. ↑ Ishida, Takashi; Kaneko, Yayoi; Iwano, Megumi; Hashimoto, Takashi (2007-05-15). "Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana". Proceedings of the National Academy of Sciences. 104 (20): 8544–8549. Bibcode:2007PNAS..104.8544I. doi: 10.1073/pnas.0701224104 . ISSN   0027-8424. PMC   1895986 . PMID   17488810.
  17. ↑ Toriyama, Michinori; Tadayuki Shimada; Ki Bum Kim; Mari Mitsuba; Eiko Nomura; Kazuhiro Katsuta; Yuichi Sakumura; Peter Roepstorff; Naoyuki Inagaki (2006). "Shootin1: A protein involved in the organization of an asymmetric signal for neuronal polarization". The Journal of Cell Biology. 175 (1): 147–157. doi:10.1083/jcb.200604160. PMC   2064506 . PMID   17030985.
  18. ↑ Motegi, Fumio; Geraldine Seydoux (2013). "The PAR network: redundancy and robustness in a symmetry-breaking system". Philosophical Transactions of the Royal Society. 368 (1629): 20130010. doi:10.1098/rstb.2013.0010. PMC   3785961 . PMID   24062581.
  19. ↑ Wolpert, Lewis; Tickle, Cheryl; Arias, Alfonso Martinez; Lawrence, Peter; Lumsden, Andrew; Robertson, Elizabeth; Meyerowitz, Elliot; Smith, Jim (2015). "Vertebrate development II: Xenopus and zebrafish". Principles of development (Fifth ed.). Oxford, United Kingdom. pp. 149–150. ISBN   9780198709886.{{cite book}}: CS1 maint: location missing publisher (link)
  20. ↑ Gerhart J, Danilchik M, Doniach T, Roberts S, Rowning B, Stewart R (1989). "Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development". Development. 107 (Suppl): 37–51. doi:10.1242/dev.107.Supplement.37. PMID   2699856.
  21. ↑ Scharf SR, Gerhart JC (September 1980). "Determination of the dorsal-ventral axis in eggs of Xenopus laevis: complete rescue of UV-impaired eggs by oblique orientation before first cleavage". Dev. Biol. 79 (1): 181–98. doi:10.1016/0012-1606(80)90082-2. PMID   7409319.
  22. ↑ Heasman J, Crawford A, Goldstone K, Garner-Hamrick P, Gumbiner B, McCrea P, Kintner C, Noro CY, Wylie C (1994). "Overexpression of cadherins and underexpression of beta-catenin inhibit dorsal mesoderm induction in early Xenopus embryos". Cell. 79 (5): 791–803. doi:10.1016/0092-8674(94)90069-8. PMID   7528101. S2CID   33403560.
  23. ↑ Miller JR, Rowning BA, Larabell CA, Yang-Snyder JA, Bates RL, Moon RT (July 1999). "Establishment of the dorsal-ventral axis in Xenopus embryos coincides with the dorsal enrichment of dishevelled that is dependent on cortical rotation". J. Cell Biol. 146 (2): 427–37. doi:10.1083/jcb.146.2.427. PMC   2156185 . PMID   10427095.
  24. ↑ Tao Q, Yokota C, Puck H, Kofron M, Birsoy B, Yan D, Asashima M, Wylie CC, Lin X, Heasman J (2005). "Maternal wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos". Cell. 120 (6): 857–71. doi: 10.1016/j.cell.2005.01.013 . PMID   15797385. S2CID   10181450.
  25. ↑ Zhang J, King ML (December 1996). "Xenopus VegT RNA is localized to the vegetal cortex during oogenesis and encodes a novel T-box transcription factor involved in mesodermal patterning". Development. 122 (12): 4119–29. doi:10.1242/dev.122.12.4119. PMID   9012531. S2CID   28462527.
  26. ↑ Marrari Y, Rouviere C, Houliston E (2004). "Complementary roles for dynein and kinesins in the Xenopus egg cortical rotation". Dev Biol. 271 (1): 38–48. doi: 10.1016/j.ydbio.2004.03.018 . PMID   15196948.
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