Skip to main content
Log in

Artificial inversion of the left–right visceral asymmetry in vertebrates: Conceptual approaches and experimental solutions

  • Reviews
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

Externally, vertebrates are bilaterally symmetrical; however, left–right asymmetry is observed in the structure of their internal organs and systems of organs (circulatory, digestive, and respiratory). In addition to the asymmetry of internal organs (visceral), there is also functional (i.e., asymmetrical functioning of organs on the left and right sides of the body) and behavioral asymmetry. The question of a possible association between different types of asymmetry is still open. The study of the mechanisms of such association, in addition to the fundamental interest, has important applications for biomedicine, primarily for the understanding of the brain functioning in health and disease and for the development of methods of treatment of certain mental diseases, such as schizophrenia and autism, for which the disturbance of left–right asymmetry of the brain was shown. To study the deep association between different types of asymmetry, it is necessary to obtain adequate animal models (primarily animals with inverted visceral organs, situs inversus totalis). There are two main possible approaches to obtaining such model organisms: mutagenesis followed by selection of mutant strains with mutations in the genes that affect the formation of the left–right visceral asymmetry and experimental obtaining of animals with inverted internal organs. This review focuses on the second approach. We describe the theoretical models for establishing left–right asymmetry and possible experimental approaches to obtaining animals with inverted internal organs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adams, D.S., Robinson, K.R., Fukumoto, T., et al., Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates, Development, 2006, vol. 133, no. 9, pp. 1657–1671.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Afzelius, B.A., A human syndrome caused by immotile cilia, Science, 1976, vol. 193, no. 4250, pp. 317–319.

    Article  CAS  PubMed  Google Scholar 

  • Aw, S., Adams, D.S., Qiu, D., et al., H,K-ATPase protein localization and Kir4.1 function reveal concordance of three axes during early determination of left-right asymmetry, Mech. Dev., 2008, vol. 125, nos. 3–4, pp. 353–372.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bacon, R.L., Self-differentiation and induction in the heart of amblystoma, J. Exp. Zool., 1945, vol. 98, no. 2, pp. 87–125.

    Article  Google Scholar 

  • Bajoghli, B., Aghaallaei, N., Soroldoni, D., et al., The roles of Groucho/Tle in left–right asymmetry and Kupffer’s vesicle organogenesis, Dev. Biol., 2007, vol. 303, no. 1, pp. 347–361.

    Article  CAS  PubMed  Google Scholar 

  • Barth, K.A., Miklosi, A., Watkins, J., et al., FSI zebrafish show concordial reversal of laterality of viscera, neuroanatomy, and a subset of behavioral responses, Curr. Biol., 2005, vol. 15, no. 9, pp. 844–850.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Berg, C., Geipel, A., Kamil, D., et al., The syndrome of left isomerism, J. Ultrasound Med., 2005, vol. 24, no. 7, pp. 921–931.

    PubMed  Google Scholar 

  • Beyer, T., Thumberger, T., Schweickert, A., et al., Connexin 26-mediated transfer of laterality cues in Xenopus, Biol. Open., 2012, vol. 1, no. 5, pp. 473–481.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bianki, V.L., Asimmetriya mozga zhivotnykh (Animal Brain Asymmetry), Leningrad: Nauka, 1985.

    Google Scholar 

  • Bisazza, A., Cantalupo, C., Robins, A., et al., Pawedness and motor asymmetries in toads, Laterality, 1997, vol. 2, no. 1, pp. 49–64.

    CAS  PubMed  Google Scholar 

  • Blum, M., Beyer, T., Weber, T., et al., Xenopus, an ideal model system to study vertebrate left-right asymmetry, Dev. Dynam., 2009, vol. 238, no. 6, pp. 1215–1225.

    Article  Google Scholar 

  • Bunney, T.D., De Boer, A.H., and Levin, M., Fusicoccin signaling reveals 14-3-3 protein function as a novel step in left-right patterning during amphibian embryogenesis, Development, 2003, vol. 130, no. 20, pp. 4847–4858.

    Article  CAS  PubMed  Google Scholar 

  • Buznikov, G.A., The action of neurotransmitters and related substances on early embryogenesis, Pharmacol. Ther., 1984, vol. 25, no. 1, pp. 23–59.

    Article  CAS  PubMed  Google Scholar 

  • Carneiro, K., Donnet, C., Rejtar, T., et al., Histone deacetylase activity is necessary for left-right patterning during vertebrate development, BMC Dev. Biol., 2011, vol. 20, no. 11, pp. 1–29.

    Google Scholar 

  • Cleveland, M., Situs inversus viscerum an anatomic study, Arch. Surg., 1926, vol. 13, no. 3, pp. 343–368.

    Article  Google Scholar 

  • Concha, M.L., Burdine, R.D., Russel, C., et al., A nodal signalling pathway regulates the laterality of neuroanatomical asymmetries in the zebrafish forebrain, Neron, 2000, vol. 28, no. 2, pp. 399–409.

    Article  CAS  Google Scholar 

  • Corballis, M.C., The evolution and genetics of cerebral asymmetry, Philos. Trans. R. Soc. London B, 2009, vol. 364, no. 1519, pp. 867–879. Davis, E.E. and

    Article  CAS  Google Scholar 

  • Katsanis, N., The ciliopathies: a transitional model into systems biology of human genetic disease, Curr. Opin. Genet. Dev., 2012, vol. 22, no. 3, pp. 290–303.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ermakov, A.S., Establishment of visceral left-right asymmetry in mammals: the role of ciliary action and leftward fluid flow in the region of Hensen’s node, Russ. J. Dev. Biol., 2013, vol. 44, no. 5, pp. 254–266.

    Article  Google Scholar 

  • Essner, J.J., Amack, J.D., Nyholm, M.K., et al., Kupffer’s vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut, Development, 2005, vol. 132, no. 6, pp. 1247–1260.

    Article  CAS  PubMed  Google Scholar 

  • Francescatto, L., Rothschild, S.C., Myers, A.L., et al., The activation of membrane targeted CaMK-II in the zebrafish Kupffer’s vesicle is required for left-right asymmetry, Development, 2010, vol. 137, no. 16, pp. 2753–2762.

    Article  CAS  PubMed  Google Scholar 

  • Fukumoto, T., Kema, I.P., and Levin, M., Serotonin signaling is a very early step in patterning of the left-right axis in chick and frog embryos, Curr. Biol., 2005a, vol. 15, no. 9, pp. 794–803.

    Article  CAS  PubMed  Google Scholar 

  • Fukumoto, T., Blakely, R., and Levin, M., Serotonin transporter function is an early step in left right patterning in chick and frog embryos, Dev. Neurosci., 2005b, vol. 27, no. 6, pp. 349–363.

    Article  CAS  PubMed  Google Scholar 

  • Garic-Stankovic, A., Hernandez, M., Flentke, G.R., et al., A ryanodine receptor-dependent Ca2+ asymmetry at Hensen’s node mediates avian lateral identity, Development, 2008, vol. 135, no. 19, pp. 3271–3280.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hamburger, V. and Hamilton, H., A series of normal stages in the development of the chick embryo, J. Morphol., 1951, vol. 88, no. 1, pp. 49–92.

    Article  CAS  PubMed  Google Scholar 

  • Herbert, M.R., Ziegler, D.A., Deutsch, C.K., et al., Brain asymmetries in autism and developmental language disorder: a nested whole-brain analysis, Brain, 2005, vol. 128, no. 1, pp. 213–226.

    Article  CAS  PubMed  Google Scholar 

  • Hoyle, C., Brown, N.A., and Wolpert, L., Development of left/right handedness in the chick heart, Development, 1992, no. 115, pp. 1071–1078.

    CAS  PubMed  Google Scholar 

  • Kawakami, Y., Raya, A., Raya, R.M., et al., Retinoic acid signalling links left-right asymmetric patterning and bilaterally symmetric somitogenesis in the zebrafish embryo, Nature, 2005, vol. 435, no. 7039, pp. 165–171.

    Article  CAS  PubMed  Google Scholar 

  • Kennedy, D.N., O’Craven, K.M., Ticho, B.S., et al., Structural and functional brain asymmetries in human situs inversus totalis, Neurology, 1999, vol. 53, no. 6, pp. 1260–1265.

    Article  CAS  PubMed  Google Scholar 

  • Klysik, M., Ciliary syndromes and treatment, Pathology—Research and Practice, 2008, vol. 204, no. 2, pp. 77–88.

    Article  CAS  Google Scholar 

  • Korthout, H. and De Boer, A.H., A fusicoccin-binding protein belongs to the family of 14-3-3 brain protein homologs, Plant Cell, 1994, vol. 6, no. 11, pp. 1681–1692.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kramer-Zucker, A.G., Olale, F., Haycraft, C.J., et al., Ciliadriven fluid flow in the zebrafish pronephros, brain and Kupffer’s vesicle is required for normal organogenesis, Development, 2005, vol. 132, no. 8, pp. 1907–1921.

    Article  CAS  PubMed  Google Scholar 

  • Levin, M., Left-right asymmetry in vertebrate embryogenesis, BioEssays, 1997, vol. 19, no. 4, pp. 287–296.

    Article  CAS  PubMed  Google Scholar 

  • Levin, M., The embryonic origins of left-right asymmetry, Crit. Rev. Oral. Biol. Med., 2004, vol. 15, no. 4, pp. 197–206.

    Article  PubMed  Google Scholar 

  • Levin, M., Left–right asymmetry in embryonic development: a comprehensive review, Mech. Dev., 2005, vol. 122, no. 4, pp. 3–25.

    Article  CAS  PubMed  Google Scholar 

  • Levin, M., Buznikov, G.A., and Lauder, J.M., Of minds and embryos: left–right asymmetry and the serotonergic controls of pre-neural morphogenesis, Dev. Neurosci., 2006, vol. 28, no. 3, pp. 171–185.

    Article  CAS  PubMed  Google Scholar 

  • Levin, M. and Mercola, M., The compulsion of chirality: toward an understanding of left-right asymmetry, Genes Dev., 1998a, vol. 12, no. 6, pp. 763–769.

    Article  CAS  PubMed  Google Scholar 

  • Levin, M. and Mercola, M., Gap junctions are involved in the early generation of left right asymmetry, Dev. Biol., 1998b, vol. 203, no. 1, pp. 90–105.

    Article  CAS  PubMed  Google Scholar 

  • Levin, M. and Mercola, M., Gap junction-mediated transfer of left-right patterning signals in the early chick blastoderm is upstream of Shh asymmetry in the node, Development, 1999, vol. 126, no. 1, pp. 4703–4714.

    CAS  PubMed  Google Scholar 

  • Levin, M., Thorlin, T., Robinson, K.R., et al., Asymmetries in H/K-ATPase and cell membrane potentials comprise a very early step in left-right patterning, Cell, 2002, vol. 111, no. 1, pp. 77–89.

    Article  CAS  PubMed  Google Scholar 

  • Long, S., Ahmad, N., and Rebagliati, M., The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry, Development 2002, vol. 130, no. 11, pp. 2303–2316.

    Article  Google Scholar 

  • Malashichev, Y.B., One-sided limb preference is linked to alternating-limb locomotion in anuran amphibians, J. Comp. Psychol., 2006, vol. 120, no. 4, pp. 401–410.

    Article  PubMed  Google Scholar 

  • Malashichev, Y.B. and Deckel, A.W., Behavioral and Morphological Asymmetries in Vertebrates, Austin: Landes Bioscience, 2006.

    Google Scholar 

  • Malashichev, Y.B. and Rogers, L.J, Eds., Behavioural and morphological asymmetries in amphibians and reptiles, in Laterality: Asymmetries of Body, Brain, and Cognition (Special Issue), 2002, vol. 7, no. 3, pp. 195–293.

    Google Scholar 

  • Malashichev, Y. and Wassersug, R.J., Left and right in the amphibian world: which way to develop and where to turn, BioEssays, 2004, vol. 26, no. 5, pp. 512–522.

    Article  PubMed  Google Scholar 

  • McGrath, J., Somlo, S., Makova, S., et al., Two populations of node monocilia initiate left-right asymmetry in the mouse, Cell, 2003, vol. 114, no. 1, pp. 61–73.

    Article  CAS  PubMed  Google Scholar 

  • McManus, C., Reversed bodies, reversed brains, and (some) reversed behaviors: of zebrafish and men, Dev. Cell, 2005, vol. 8, no. 6, pp. 796–797.

    Article  CAS  PubMed  Google Scholar 

  • Mogi, K., Goto, M., Ohno, E., et al., Xenopus neurula leftright asymmetry is respecified by microinjecting TGF-ß5 protein, Int. J. Dev. Biol., 2003, vol. 47, no. 1, pp. 15–29.

    Article  CAS  PubMed  Google Scholar 

  • Morokuma, J., Blackiston, D., and Levin, M., KCNQ1 and KCNE1 K+ channel components are involved in early left-right patterning in Xenopus laevis embryos, Cell Physiol. Biochem., 2008, vol. 21, nos. 5–6, pp. 357–372.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • New, D.A., A new technique for the cultivation of the chick embryo in vitro, J. Embryol. Exp. Morphol., 1955, vol. 3, no. 4, pp. 320–331.

    Google Scholar 

  • Nieuwkoop, P.D. and Faber, J., Normal Table of Xenopus laevis (Daudin), Amsterdam: North-Holland Publishing Company, 1967.

    Google Scholar 

  • Nishi, T. and Forgac, M., The vacuolar (H+)-ATPases— nature’s most versatile proton pumps, Nat. Rev. Mol. Cell. Biol., 2002, vol. 3, no. 2, pp. 94–103.

    Article  CAS  PubMed  Google Scholar 

  • Nishide, K., Mugitani, M., Kumano, G., et al., Neurula rotation determines left-right asymmetry in ascidian tadpole larvae, Development, 2012, vol. 139, no. 8, pp. 1467–1475.

    Article  CAS  PubMed  Google Scholar 

  • Nonaka, S., Tanaka, Y., Okada, Y., et al., Randomization of left–right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein, Cell, 1998, vol. 95, no. 6, pp. 829–837.

    Article  CAS  PubMed  Google Scholar 

  • Nonaka, S., Shiratori, H., Saijoh, Y., et al., Determination of left–right patterning of the mouse embryo by artificial nodal flow, Nature, 2002, vol. 418, no. 6893, pp. 96–99.

    Article  CAS  PubMed  Google Scholar 

  • Norris, D.P. and Grimes, D.T., Mouse models of ciliopathies: the state of the art, Disease Models Mechanisms, 2012, vol. 5, no. 3, pp. 299–312.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Okada, Y., Takeda, S., Tanaka, Y., et al., Mechanism of nodal flow: a conserved symmetry breaking event in left–right axis determination, Cell, 2005, vol. 121, no. 4, pp. 633–644.

    Article  CAS  PubMed  Google Scholar 

  • Palmer, A.R., Symmetry breaking and the evolution of development, Science, 2004, vol. 306, no. 5697, pp. 828–833.

    Article  CAS  PubMed  Google Scholar 

  • Paulozzi, L.J. and Lary, J.M., Laterality patterns in infants with external birth defects, Teratology, 1999, vol. 60, no. 5, pp. 265–271.

    Article  CAS  PubMed  Google Scholar 

  • Petty, R.G., Structural asymmetries of the human brain and their disturbance in schizophrenia, Schizophr. Bull., 1999, vol. 25, no. 1, pp. 121–139.

    Article  CAS  PubMed  Google Scholar 

  • Polak, W.G., Chudoba, P.J., Patrzalek, D., et al., Organ donor with complete situs inversus. Case report and review of the literature, Ann. Transplant., 2006, vol. 11, no. 1, pp. 43–46.

    PubMed  Google Scholar 

  • Pressler, K., Beobachtungen und Versuche uber den normalen und inversen Situs viscerum und cordis bei Anurenlarven, Archiv fur Entwicklungsmechanik der Organismen, 1911, vol. 32, no. 1, pp. 1–35.

    Article  Google Scholar 

  • Pujol, J., Cardoner, N., Benlloch, L., et al., CSF spaces of the sylvian fissure region in severe melancholic depression, Neuroimage, 2002, vol. 15, no. 1, pp. 103–106.

    Article  PubMed  Google Scholar 

  • Rayhill, S.C., Scott, D., Orloff, S, et al., Orthotopic, but reversed implantation of the liver allograft in situs inversus totalis—a simple new approach to a difficult problem, Am. J. Transplant., 2009, vol. 9, no. 7, pp. 1602–1606.

    Article  CAS  PubMed  Google Scholar 

  • Robichon, F., Lévrier, O., Farnarier, P, et al., Developmental dyslexia: atypical asymmetry of language areas and its functional significance, Eur. J. Neurol., 2000, vol. 7, no. 1, pp. 35–46.

    Article  CAS  PubMed  Google Scholar 

  • Rogers, L.J. and Workman, L, Footedness in birds, Anim. Behav., 1993, vol. 45, no. 2, pp. 409–411.

    Article  Google Scholar 

  • Rogers, L.J, Lateralised brain function in anurans: comparison to lateralisation in other vertebrates, Laterality, 2002, vol. 7, no. 3, pp. 219–239.

    PubMed  Google Scholar 

  • Rogers, L.J. and Andrew, R., Comparative Vertebrate Lateralization, Cambridge: Cambridge University Press, 2002.

  • Roussigne, M., Bianco, I.H., Wilson, S.W, et al., Nodal signalling imposes left-right asymmetry upon neurogenesis in the habenular nuclei, Development, 2009, vol. 136, no. 9, pp. 1549–1557.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roussigne, M., Blader, P., and Wilson, S.W, Breaking symmetry: the zebrafish as a model for understanding leftright asymmetry in the developing brain, Dev. Neurobiol., 2012, vol. 72, no. 3, pp. 269–281.

    Article  PubMed  Google Scholar 

  • Salazar Del Rio, J., Influence of extrinsic factors on the development of the bulboventricular loop of the chick embryo, J. Embryol. Exp. Morphol., 1974, vol. 31, no. l, pp. 199–206.

    Google Scholar 

  • Sarmah, B., Latimer, A.J., and Appel, B, Inositol polyphosphates regulate zebrafish left-right asymmetry, Dev. Cell, 2005, vol. 9, no. 1, pp. 133–145.

    Article  CAS  PubMed  Google Scholar 

  • Schreuder, M.F, Unilateral anomalies of kidney development: why is left not right?, Kidney Int., 2011, vol. 80, no. 7, pp. 740–745.

    Article  PubMed  Google Scholar 

  • Schweickert, T., Weber, T., Beyer, P, et al., Cilia-driven leftward flow determines laterality in Xenopus, Curr. Biol., 2007, vol. 17, no. 1, pp. 60–66.

    Article  CAS  PubMed  Google Scholar 

  • Shook, D.R., Majer, C., and Keller, R, Pattern and morphogenesis of presumptive superficial mesoderm in two closely related species, Xenopus laevis and Xenopus tropicalis, Dev. Biol., 2004, vol. 270, no. 1, pp. 163–185.

    Article  CAS  PubMed  Google Scholar 

  • Smillie, D.A., Llinas, A.J., and Ryan, J.T.P, et al., Nuclear import and activity of histone deacetylase in Xenopus oocytes is regulated by phosphorylation, J. Cell Sci., 2004, vol. 117, no. 9, pp. 1857–1866.

    Article  CAS  PubMed  Google Scholar 

  • Spencer, R, Conjoined twins: theoretical embryologic basis, Teratology, 1992, vol. 45, no. 6, pp. 591–602.

    Article  CAS  PubMed  Google Scholar 

  • Spratt, N.T., A simple method for explanting and cultivating early chick embryos in vitro, Science, 1947, vol. 106, no. 2758, p. 452.

    Article  PubMed  Google Scholar 

  • Steele, J. and Uomini, N, Humans, tools and handedness, in Stone Knapping: The Necessary Conditions for a Uniquely Hominin Behaviour, Roux, V. and Bril, B., Eds., Cambridge: UK: McDonald Institute for Archaeological Research, 2005, pp. 217–239.

    Google Scholar 

  • Ströckens, F., Güntürkün, O., and Ocklenburg, S, Limb preferences in non-human vertebrates, Laterality: Asymmetries of Body, Brain and Cognition, 2013, vol. 18, no. 5, pp. 536–575.

    Google Scholar 

  • Torgersen, J, Situs inversus, asymmetry, and twinning, Am. J. Human Genet., 1950, vol. 2, no. 4, pp. 361–370.

    CAS  Google Scholar 

  • Toyoizumi, R., Kobayashi, T., Kikukawa, A, et al., Adrenergic neurotransmitters and calcium ionophore-induced situs inversus viscerum in Xenopus laevis embryos, Dev. Growth Diff., 1997, vol. 39, no. 4, pp. 505–514.

    Article  CAS  Google Scholar 

  • Toyoizumi, R., Mogi, K., and Takeuchi, S, More than 95% reversal of left-right axis induced by right-sided hypodermic microinjection of activin into Xenopus neurula embryos, Dev. Biol., 2000, vol. 221, no. 2, pp. 321–336.

    Article  CAS  PubMed  Google Scholar 

  • Toyoizumi, R., Ogasawara, T., Takeuchi, S, et al., Xenopus nodal related-1 is indispensable only for left–right axis determination, Int. J. Dev. Biol., 2005, vol. 49, no. 8, pp. 923–938.

    Article  CAS  PubMed  Google Scholar 

  • Vallortigara, G., Chiandetti, C., and Sovrano, V.A., Brain asymmetry (animal), WIREs Cogn. Sci., 2011, vol. 2, no. 2, pp. 146–157.

    Article  Google Scholar 

  • Vandenberg, L.N., Stevenson, C., and Levin, M., Low frequency vibrations induce malformations in two aquatic species in a frequency-, waveform-, and direction-specific manner, PLoS One, 2012, vol. 7, no. 12, pp. e51473.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vandenberg, L.N., Lemire, J.M., and Levin, M, Serotonin has early, cilia-independent roles in Xenopus left-right patterning, Disease Models Mechanisms, 2013, vol. 6, no. 1, pp. 261–268.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vandreberg, L.N, Laterality defects are influenced by timing of treatments and animal model, Differentiation, 2012, vol. 83, no. 1, pp. 26–37. Wood, C.O. and

    Article  Google Scholar 

  • Blalock, A, Situs inversus totalis and disease of biliary tract: survey of literature and report case, Arch. Surg., 1940, vol. 40, no. 5, pp. 885–896.

    Article  Google Scholar 

  • Yost, H.J, Regulation of vertebrate left-right asymmetries by extracellular matrix, Nature, 1992, vol. 357, no. 6374, pp. 158–161.

    Article  CAS  PubMed  Google Scholar 

  • Yu, S., Guo, H., Zhang, W, et al., Orthotopic liver transplantation in situs inversus adult from an ABO-incompatible donor with situs inversus, Gastroenterology, 2014, vol. 14, no. 46, pp. 1–4.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. S. Ermakov.

Additional information

Original Russian Text © A.S. Trulioff, Y.B. Malashichev, A.S. Ermakov, 2015, published in Ontogenez, 2015, Vol. 46, No. 6, pp. 365–384.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Trulioff, A.S., Malashichev, Y.B. & Ermakov, A.S. Artificial inversion of the left–right visceral asymmetry in vertebrates: Conceptual approaches and experimental solutions. Russ J Dev Biol 46, 307–325 (2015). https://doi.org/10.1134/S1062360415060090

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360415060090

Keywords

Navigation