Biology:Amitosis

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Short description: Cell proliferation that does not occur by mitosis

Amitosis (a- + mitosis), also called karyostenosis, direct cell division, or binary fission, is a form of asexual cell division used by most prokaryotes. It differs from other forms of cell division (e.g., mitosis, meiosis) as it does not involve the mitotic apparatus (spindle formation) nor the condensation of chromatin into chromosomes prior to cellular division.

Note that several instances of cell division formerly thought to belong to this "non-mitotic" class, such as the division of some unicellular eukaryotes, may actually occur by the process of "closed mitosis" different from open or semi-closed mitotic processes, all involving mitotic chromosomes and classified by the fate of the nuclear envelope.

Processes

Amitosis is defined as the division of cells in the interphase state, usually accomplished by a simple constriction into two sometimes unequal halves, without any regular segregation of genetic material.[1] This can lead to random numbers of parental chromosomes being distributed in the subsequent daughter cells. This is in contrast to mitosis which involves precise distribution of chromosomes in the resulting daughter cells. This phenomenon does not involve maximal condensation of chromatin into chromosomes, a molecular event that is observable by light microscopy as chromatins line up in pairs along the metaphase plate. Amitosis has been reported in ciliates, yet its role in mammalian cell proliferation continues to be met with skepticism. Interestingly, the discovery of copy number variations (CNVs) in mammalian cells within an organ[2] has challenged the age-old assumption that every cell in an organism must inherit an exact copy of the parental genome to be functional. Instead of CNVs stemming from mitosis gone awry, such variations could have arisen from amitosis, and may even be beneficial to the cells. Furthermore, ciliates possess a mechanism for adjusting copy numbers of individual genes during amitosis of the macronucleus.[3]

Discovery

Amitosis was first described in 1880 by Walther Flemming (more celebrated for describing mitosis) and others.[4] For a few years thereafter, it was common for biologists to think of cells having both the capability to divide mitotically and amitotically.[5] However, since the turn of the twentieth century, amitosis has not received much attention. Using "mitosis in mammalian cells" as a search term in the Medline database calls up more than 10,000 studies dealing with mitosis, whereas "amitosis in mammalian cells" retrieves the titles of fewer than 50 papers. This absence of data has led many scientists to conclude that amitosis does not exist, or is minimally important.

Despite that, a resurgence of interest in the role of amitosis in mammalian proliferation has been building over the past several decades. A review of the resulting literature not only affirms the involvement of amitosis in cell proliferation, but also explores the existence of more than one amitotic mechanism capable of producing "progeny nuclei" without the involvement of "mitotic chromosomes." One form of amitosis involves fissioning, a nucleus splitting in two without the involvement of chromosomes, which has been reported to occur in placental tissues and in cells grown from such tissues in rats,[6] as well as in human and mouse trophoblasts[7],.[8] Amitosis by fissioning has also been reported in mammalian liver cells[9] and human adrenal cells.[10] Chen and Wan[11] reported amitosis in rat liver and presented a mechanism for a four-stage amitotic process whereby chromatin threads are reproduced and equally distributed to daughter cells as the nucleus splits in two.

Functional role

Additional reports of non-mitotic proliferation as well as insights into its underlying mechanisms, have emerged from extensive work with polyploid cells. Such cells, long acknowledged to exist, were once believed simply to be anomalous. Accumulating research, including those involving liver cells[12] now suggest that multiple copies of the genome in a cell population may be involved in the cell's adaptation to the environment.

A couple of decades of research has shown that polyploid cells are frequently "reduced" to diploid cells by amitosis.[13] For instance, naturally occurring polyploid placental cells have been shown to be capable of producing nuclei with diploid or near-diploid complements of DNA. Furthermore, Zybina and colleagues have demonstrated that such nuclei, derived from polyploid placental cells, receive one or more copies of a microscopically identifiable region of the chromatin, demonstrating that this particular amitotic process can actually result in representative transmission of chromatin. Studying rat polyploid trophoblasts, they have also shown that the nuclear envelope of the giant nucleus is involved in this subdivision.[14] Polyploid cells may also be key to the survival processes underlying chemotherapy resistance in certain cells.

Erenpreisa et al. reported that following treatment of cultured cells with mitosis-inhibiting chemicals (similar to those used in certain chemotherapeutic protocols), a small population of induced polyploid cells survived. Eventually, this population gave rise to "normal" diploid cells by the formation of polyploid chromatin bouquets that return to an interphase state, before separating into several secondary nuclei.[15] Intriguing phenomena including controlled autophagic degradation of DNA as well as the production of nuclear envelope-limited sheets[16] accompany the process.[17] Since this process of depolyploidization involves mitotic chromosomes, it conforms to the broad definition of amitosis.

Current literature

There are also multiple reports of amitosis occurring when nuclei bud out through the plasma membrane of a polyploid cell. Such a process has been shown to occur in amniotic cells transformed by a virus[18] and in mouse embryo fibroblast lines exposed to carcinogens.[19] A similar process called extrusion has been described for mink trophoblasts, a tissue in which fissioning is also observed.[20] Asymmetric cell division has also been described in polyploid giant cancer cells and low eukaryotic cells and reported to occur by the amitotic processes of splitting, budding, or burst-like mechanisms.[21] Similarly, two different kinds of amitosis have been described in monolayers of Ishikawa endometrial cells.[22]

An example of amitosis particularly suited to the formation of multiple differentiated nuclei in a reasonably short period of time has been shown to occur during the differentiation of fluid-enclosing hemispheres called domes from adherent Ishikawa endometrial monolayer cells during an approximately 20-hour period [23],.[24] Aggregates of nuclei from monolayer syncytia become enveloped in mitochondrial membranes, forming structures (mitonucleons) that become elevated as a result of vacuole formation during the initial 6 hours of differentiation [25],.[26] Over the next 4 to 5 hours, chromatin from these aggregated nuclei becomes increasingly pycnotic, eventually undergoing karyolysis and karyorrhexis in the now-elevated predome structures.[27] In other systems, such changes accompany apoptosis but not in the differentiating Ishikawa cells, where the processes appear to accompany changes in DNA essential for the newly created, differentiated dome cells. Finally, the chromatin filaments emerging from these processes form a mass from which dozens of dome nuclei are amitotically generated[28] over a period of approximately 3 hours with the apparent involvement of nuclear envelope-limited sheets.[29]

That all of this may be an iceberg tip is suggested by research from William Thilly's laboratory. Examination of fetal gut (5 to 7 weeks), colonic adenomas, and adenocarcinomas has revealed nuclei that look like hollow bells encased in tubular syncytia. These structures can either divide symmetrically by an amitotic nuclear fission process, forming new "bells", or undergo fission asymmetrically, resulting in one of seven other nuclear morphotypes, five of which appear to be specific to development since they are rarely observed in adult organisms.[30]

In conclusion, current body of literature suggests that amitosis may very well be involved in cellular development [31] in humans, likely during the fetal and embryonic phases of development when the majority of these cells are produced, perhaps within the complexity of implantation, perhaps when large numbers of cells are being differentiated, or perhaps in cancerous cells.

References

  1. ↑ Tippit, D. H.; Pickett-Heaps, J. D. (1976-07-01). "Apparent amitosis in the binucleate dinoflagellate Peridinium Balticum". Journal of Cell Science 21 (2): 273–289. doi:10.1242/jcs.21.2.273. ISSN 0021-9533. PMID 987046. https://doi.org/10.1242/jcs.21.2.273. 
  2. ↑ O'Huallachain, M.; Karczewski, K. J.; Weissman, S. M.; Urban, A. E.; Snyder, M. P. (2012-10-30). "Extensive genetic variation in somatic human tissues" (in en). Proceedings of the National Academy of Sciences 109 (44): 18018–18023. doi:10.1073/pnas.1213736109. ISSN 0027-8424. PMID 23043118. Bibcode: 2012PNAS..10918018O. 
  3. ↑ Prescott, D. M. (June 1994). "The DNA of ciliated protozoa". Microbiological Reviews 58 (2): 233–267. doi:10.1128/MMBR.58.2.233-267.1994. ISSN 0146-0749. PMID 8078435. 
  4. ↑ Macklin, C. C. (June 1916). "Amitosis in Cells Growing in Vitro" (in en). The Biological Bulletin 30 (6): 445–[466]–1. doi:10.2307/1536358. ISSN 0006-3185. https://www.biodiversitylibrary.org/part/6457. 
  5. ↑ Holland, Nicholas (2021), "Vicenzo Colucci's 1886 memoir, Intorno alla rigenerazione degli arti e della coda nei tritoni, annotated and translated into English as: Concerning regeneration of the limbs and tail in salamanders", The European Zoological Journal 88: 837–890, doi:10.1080/24750263.2021.1943549 
  6. ↑ Ferguson, F. G.; Palm, J. (1976-02-15). "Histologic characteristics of cells cultured from rat placental tissue". American Journal of Obstetrics and Gynecology 124 (4): 415–420. doi:10.1016/0002-9378(76)90103-4. ISSN 0002-9378. PMID 1251862. 
  7. ↑ Cotte, C.; Easty, G. C.; Neville, A. M.; Monaghan, P. (August 1980). "Preparation of highly purified cytotrophoblast from human placenta with subsequent modulation to form syncytiotrophoblast in monolayer cultures". In Vitro 16 (8): 639–646. doi:10.1007/bf02619191. ISSN 0073-5655. PMID 7419234. 
  8. ↑ Kuhn, E. M.; Therman, E.; Susman, B. (May 1991). "Amitosis and endocycles in early cultured mouse trophoblast". Placenta 12 (3): 251–261. doi:10.1016/0143-4004(91)90006-2. ISSN 0143-4004. PMID 1754574. 
  9. ↑ David, H.; Uerlings, I. (September 1992). "[Ultrastructure of amitosis and mitosis of the liver]". Zentralblatt für Pathologie 138 (4): 278–283. ISSN 0863-4106. PMID 1420108. 
  10. ↑ Magalhães, M. C.; Pignatelli, D.; Magalhães, M. M. (April 1991). "Amitosis in human adrenal cells". Histology and Histopathology 6 (2): 251–256. ISSN 0213-3911. PMID 1802124. 
  11. ↑ Chen, Y. Q.; Wan, B. K. (1986). "A study on amitosis of the nucleus of the mammalian cell. I. A study under the light and transmission electron microscope". Acta Anatomica 127 (1): 69–76. ISSN 0001-5180. PMID 3788448. 
  12. ↑ Duncan, Andrew W.; Taylor, Matthew H.; Hickey, Raymond D.; Hanlon Newell, Amy E.; Lenzi, Michelle L.; Olson, Susan B.; Finegold, Milton J.; Grompe, Markus (2010-10-07). "The ploidy conveyor of mature hepatocytes as a source of genetic variation". Nature 467 (7316): 707–710. doi:10.1038/nature09414. ISSN 1476-4687. PMID 20861837. Bibcode: 2010Natur.467..707D. 
  13. ↑ Zybina, T.G.; Zybina, E.V.; Kiknadze, I.I.; Zhelezova, A.I. (2001). "Polyploidization in the Trophoblast and Uterine Glandular Epithelium of the Endotheliochorial Placenta of Silver Fox (Vulpes fulvus Desm.), as Revealed by the DNA Content" (in en). Placenta 22 (5): 490–498. doi:10.1053/plac.2001.0675. PMID 11373160. https://linkinghub.elsevier.com/retrieve/pii/S0143400401906757. 
  14. ↑ Zybina, Eugenia V.; Zybina, Tatiana G. (July 2008). "Modifications of nuclear envelope during differentiation and depolyploidization of rat trophoblast cells". Micron 39 (5): 593–606. doi:10.1016/j.micron.2007.05.006. ISSN 0968-4328. PMID 17627829. 
  15. ↑ Erenpreisa, Jekaterina; Salmina, Kristine; Huna, Anda; Kosmacek, Elizabeth A.; Cragg, Mark S.; Ianzini, Fiorenza; Anisimov, Alim P. (July 2011). "Polyploid tumour cells elicit paradiploid progeny through depolyploidizing divisions and regulated autophagic degradation". Cell Biology International 35 (7): 687–695. doi:10.1042/CBI20100762. ISSN 1095-8355. PMID 21250945. 
  16. ↑ Olins, A. L.; Buendia, B.; Herrmann, H.; Lichter, P.; Olins, D. E. (1998-11-25). "Retinoic acid induction of nuclear envelope-limited chromatin sheets in HL-60". Experimental Cell Research 245 (1): 91–104. doi:10.1006/excr.1998.4210. ISSN 0014-4827. PMID 9828104. 
  17. ↑ Erenpreisa, Jekaterina; Ivanov, Andrey; Cragg, Mark; Selivanova, Galina; Illidge, Timothy (March 2002). "Nuclear envelope-limited chromatin sheets are part of mitotic death" (in en). Histochemistry and Cell Biology 117 (3): 243–255. doi:10.1007/s00418-002-0382-6. ISSN 0948-6143. PMID 11914922. 
  18. ↑ Walen, Kirsten H. (February 2002). "The origin of transformed cells. studies of spontaneous and induced cell transformation in cell cultures from marsupials, a snail, and human amniocytes". Cancer Genetics and Cytogenetics 133 (1): 45–54. doi:10.1016/s0165-4608(01)00572-6. ISSN 0165-4608. PMID 11890989. 
  19. ↑ Sundaram, Meenakshi; Guernsey, Duane L.; Rajaraman, Murali M.; Rajaraman, Rengaswami (February 2004). "Neosis: a novel type of cell division in cancer". Cancer Biology & Therapy 3 (2): 207–218. doi:10.4161/cbt.3.2.663. ISSN 1538-4047. PMID 14726689. 
  20. ↑ Isakova, G. K.; Shilova, I. E. (July 2003). "[Frequency ratio of two forms of amitotic division of trophoblast cell nuclei in the mink blastocysts during the period of delayed implantation]". Izvestiia Akademii Nauk. Seriia Biologicheskaia (4): 395–398. ISSN 1026-3470. PMID 12942744. 
  21. ↑ Zhang, Dan; Wang, Yijia; Zhang, Shiwu (2014). "Asymmetric cell division in polyploid giant cancer cells and low eukaryotic cells". BioMed Research International 2014: 432652. doi:10.1155/2014/432652. ISSN 2314-6141. PMID 25045675. 
  22. ↑ Fleming, Honoree (2014-12-31) (in en). Unusual characteristics of opaque Ishikawa endometrial cells include the envelopment of chromosomes with material containing endogenous biotin in the latter stages of cytokinesis (Report). PeerJ PrePrints. https://peerj.com/preprints/772v1. 
  23. ↑ Fleming, Honorée (1995). "Differentiation in human endometrial cells in monolayer culture: Dependence on a factor in fetal bovine serum" (in en). Journal of Cellular Biochemistry 57 (2): 262–270. doi:10.1002/jcb.240570210. ISSN 0730-2312. PMID 7759563. https://onlinelibrary.wiley.com/doi/10.1002/jcb.240570210. 
  24. ↑ Fleming, Honoree (1999). "Structure and Function of Cultured Endometrial Epithelial Cells" (in en). Seminars in Reproductive Medicine 17 (1): 93–106. doi:10.1055/s-2007-1016215. ISSN 1526-8004. PMID 10406079. http://www.thieme-connect.de/DOI/DOI?10.1055/s-2007-1016215. 
  25. ↑ Fleming, Honoree; Condon, Rebekah; Peterson, Genevieve; Guck, Ilse; Prescott, Elizabeth; Chatfield, Kathryn; Duff, Meghan (1998-12-01). "Role of biotin-containing membranes and nuclear distribution in differentiating human endometrial cells" (in en). Journal of Cellular Biochemistry 71 (3): 400–415. doi:10.1002/(SICI)1097-4644(19981201)71:3<400::AID-JCB9>3.0.CO;2-W. PMID 9831077. https://onlinelibrary.wiley.com/doi/10.1002/(SICI)1097-4644(19981201)71:33.0.CO;2-W. 
  26. ↑ Fleming, Honoree (2016-02-09) (in en). Mitonucleons formed during differentiation of Ishikawa endometrial cells generate vacuoles that elevate monolayer syncytia: Differentiation of Ishikawa domes, Part 1 (Report). PeerJ PrePrints. doi:10.7287/peerj.preprints.1728v1. https://peerj.com/preprints/1728. 
  27. ↑ Fleming, Honoree (2016-02-09) (in en). Pyknotic chromatin in mitonucleons elevating in syncytia undergo karyorhhexis and karyolysis before coalescing into an irregular chromatin mass: Differentiation of Ishikawa Domes, Part 2 (Report). PeerJ PrePrints. doi:10.7287/peerj.preprints.1729v1. https://peerj.com/preprints/1729. 
  28. ↑ Fleming, Honoree (2016-02-09) (in en). Chomatin mass from previously aggregated, pyknotic, and fragmented monolayer nuclei is a source for dome cell nuclei generated by amitosis: Differentiation of Ishikawa Domes, Part 3 (Report). PeerJ PrePrints. doi:10.7287/peerj.preprints.1730v1. https://peerj.com/preprints/1730. 
  29. ↑ Olins, A. L.; Buendia, B.; Herrmann, H.; Lichter, P.; Olins, D. E. (1998-11-25). "Retinoic acid induction of nuclear envelope-limited chromatin sheets in HL-60". Experimental Cell Research 245 (1): 91–104. doi:10.1006/excr.1998.4210. ISSN 0014-4827. PMID 9828104. 
  30. ↑ Gostjeva, E. V.; Zukerberg, L.; Chung, D.; Thilly, W. G. (2006-01-01). "Bell-shaped nuclei dividing by symmetrical and asymmetrical nuclear fission have qualities of stem cells in human colonic embryogenesis and carcinogenesis". Cancer Genetics and Cytogenetics 164 (1): 16–24. doi:10.1016/j.cancergencyto.2005.05.005. ISSN 0165-4608. PMID 16364758. 
  31. ↑ Duncan, Andrew W.; Taylor, Matthew H.; Hickey, Raymond D.; Hanlon Newell, Amy E.; Lenzi, Michelle L.; Olson, Susan B.; Finegold, Milton J.; Grompe, Markus (2010-10-07). "The ploidy conveyor of mature hepatocytes as a source of genetic variation". Nature 467 (7316): 707–710. doi:10.1038/nature09414. ISSN 1476-4687. PMID 20861837. Bibcode: 2010Natur.467..707D. 

Further reading

Child CM. 1907 Amitosis as a factor in normal and regulatory growth. Anat Anz. 30: 271–97.

Coleman SJ, Gerza L, JonesCJ, Sibley CP, Aplin JD, Heazell AEP. 2013. Syncytial nuclear

Fleming H. 1995 Differentiation in human endometrial cells in monolayer culture: Dependence on a factor in fetal bovine serum J.Cell Biochem. 57:262-270.

Fleming H, Condon R, Peterson G, Guck I, Prescott E, Chatfield K, Duff M. 1998. Role of biotin-containing membranes and nuclear distribution in differentiating human endometrial cells. Journal of Cellular Biochemistry. 71(3): 400–415.

Fleming H. 1999 Structure and function of cultured endometrial epithelial cells. Semin Reprod Endocrinol.17(1):93-106.

Fleming H. 2014 Unusual characteristics of opaque Ishikawa endometrial cells include the envelopment of chromosomes with material containing endogenous biotin in the latter stages of cytokinesis doi:10.7287/peerj.preprints.772v1

Fleming H. 2016a. Mitonucleons formed during Differentiation of Ishikawa Endometrial Epithelial Cells are involved in Vacuole Formation that Elevates Monolayer Cells into Domes. Differentiation of Ishikawa Domes, Part 1, doi:10.7287/peerj.preprints.1728v1

Fleming H. 2016b. Pyknotic chromatin in mitonucleons elevating in syncytia undergo karyorhhexis and karyolysis before coalescing into an irregular chromatin mass: Differentiation of Ishikawa Domes, Part 2, doi:10.7287/peerj.preprints.1729v1

Fleming H. 2016c. Chromatin mass from previously aggregated, pyknotic, and fragmented monolayer nuclei is a source for dome cell nuclei generated by amitosis: Differentiation of Ishikawa Domes, Part 3, doi:10.7287/peerj.preprints.1730v1

Güttinger, S; Laurell, E; Kutay, U (2009), "Orchestrating nuclear envelope disassembly and reassembly during mitosis", Nat Rev Mol Cell Biol 10 (3): 178–191, doi:10.1038/nrm2641, PMID 19234477

Isakova GK, Shilova IE. 2000. Reproduction by "budding" of the trophoblast cells in the mink implanting blastocysts. Dokl Biol Sci. 371:214-6.

Schoenfelder KP, Fox DT 2015 The expanding implications of polyploidy. J Cell Biol. 25;209(4):485-91. doi:10.1083/jcb.201502016.

Thilly WG, Gostjeva EV, Koledova VV, Zukerberg LR, Chung D, Fomina JN, Darroudi F, Stollar BD. 2014. Metakaryotic stem cell nuclei use pangenomic dsRNA/DNA intermediates in genome replication and segregation. Organogenesis. 10(1):44-52. doi:10.4161/org.27684. Epub 2014 Jan 13.

Walen KH. 2004. Spontaneous cell transformation: karyoplasts derived from multinucleated cells produce new cell growth in senescent human epithelial cell cultures. In Vitro Cell Dev Biol Anim. 40(5-6):150-8.

Zybina EV, Zybina TG, Bogdanova MS, Stein GI 2005 Cell Biol Int. 29 (12): 1066-1070



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