Early Amphibian (Anuran) Morphogenesis Is Sensitive to Novel Gravitational Fields

Neff, Anton W.; Yokota, Hiroki; Chung, Hae-Moon; Wakahara, Masami; Malacinski, George M.

doi:10.1006/dbio.1993.1024

Cited by 58 publications

(39 citation statements)

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“…A similar relationship has been documented for Xenopus eggs subjected to clinostat rotation (17). It is also possible that the thickened blastocoel roof results from a failure of its cells to undergo radial interdigitation at the normal time.…”

Section: Discussionsupporting

confidence: 67%

Amphibian development in the virtual absence of gravity.

Souza

Black

Wassersug

1995

Proc. Natl. Acad. Sci. U.S.A.

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To test whether gravity is required for normal amphibian development, Xenopus laevis females were induced to ovulate aboard the orbiting Space Shuttle. Eggs were fertilized in vitro, and although early embryonic stages showed some abnormalities, the embryos were able to regulate and produce nearly normal larvae. These results demonstrate that a vertebrate can ovulate in the virtual absence of gravity and that the eggs can develop to a free-living stage.Is gravity required for normal embryonic development? Upon fertilization, most amphibian eggs rotate inside the fertilization membrane so that the animal-vegetal axis is aligned with gravity. This "rotation of fertilization" (1) is not a requirement for normal development, since eggs prevented from rotating can develop normally (2). Nevertheless, the direction of the rotation of fertilization normally has a role in determining the polarity of the embryonic axis (1), and eggs inclined with respect to gravity form the dorsal structures on the side of the egg uppermost in the gravitational field (3, 4). Thus, for over a century scientists have questioned whether gravity was required for amphibian embryogenesis (5, 6). Recent spaceflight experiments have successfully fertilized eggs of Xenopus laevis and reared the embryos to the gastrula stage. The morphology of the gastrulae was somewhat abnormal (7). We report here that ovulation and subsequent development to a free-living stage can occur at microgravity (<10-3 X g). We also examined larval swimming behavior to determine whether abnormal behaviors of Xenopus tadpoles previously observed during and following space flight (8) would occur with larvae that began their lives in the virtual absence of gravity.MATERIALS AND METHODS Preflight Procedures. X laevis frogs were obtained from J.

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Section: Discussionsupporting

confidence: 67%

Amphibian development in the virtual absence of gravity.

Souza

Black

Wassersug

1995

Proc. Natl. Acad. Sci. U.S.A.

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“…The thickness of the µG-embryo roof was related to a reduction of adhesion between ectodermal cells and not to an increase of the number of cell layers, as observed by Ubbels et al (1994) for µG-embryos of Xenopus laevis or with cell proliferation as proposed by Black et al (1996). However, the data of Neff et al (1993) who used a clinostat suggested that the thickening of the blastocoel roof of Xenopus embryos was due to a change in the latitude of the third cleavage plane rather than a modification of cell proliferation. Moreover, De Maziére et al (1996) observed in µG-Xenopus that the blastocoel shifted toward the vegetal hemisphere.…”

Section: Discussionmentioning

confidence: 80%

“…Using a clinostat on the ground to simulate microgravity, Neff et al (1993) and Yokota et al (1994) observed that the third cleavage shifted toward the embryo equator. Consequently, microgravity has effects on embryos of both Xenopus and Pleurodeles at the beginning of cleavage.…”

Section: Discussionmentioning

confidence: 99%

Effects of space environment on embryonic growth up to hatching of salamander eggs fertilized and developed during orbital flights.

et al. 2002

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In vertebrates, only few experiments have been performed in microgravity to study the embryonic development from fertilization. To date, these concern only amphibian and fish. We report here a study on the embryonic development of Pleurodeles waltl (urodele amphibian) eggs oviposited in microgravity. The experiment was performed twice on board the Mir space station and the data obtained included video recording and morphological, histological and immunocytological analyses. The data confirm that the microgravity conditions have effects during the embryonic period, particularly during cleavage and neurulation, inducing irregular segmentation and abnormal closure of the neural tube. Moreover, we observed several abnormalities hither to undescribed corresponding to cortical cytoplasm movements, a decrease of cell adhesion and a loss of cells. These abnormalities were temporary and subsequently reversible. The young larvae that hatched during the flight displayed normal morphology and swimming behavior after landing. The results obtained in the urodele Pleurodeles waltl are in accordance with those observed earlier in the anuran Xenopus laevis and in the fish Oryzias latipes.

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“…A further, not mutually exclusive, possibility is that the observed phenotypes could result from an altered proliferation of the anterior neural system. However, the observation that adult frogs raised in microgravity are indistinguishable from those raised in 1 g might indicate that, similarly to mouse ES cells, the effects of microgravity are transient (Neff et al, 1993). In general agreement with this notion, abnormalities of cytoplasm movements, and cell adhesion in response to microgravity were found temporary and, in general, reversible (Gualandris-Parisot et al, 2002).…”

Section: Microgravity Embryonic Stem Cells and Developmentmentioning

confidence: 71%

“…At the hatching tadpole stage, amphibian embryos raised in SMG had enlarged head and eyes (Neff et al, 1993), with opposite effects observed under increased gravity. These phenotypes may relate to the effects of microgravity on the cytoskeleton (summarized in Crawford-Young, 2006).…”

Section: Microgravity Embryonic Stem Cells and Developmentmentioning

confidence: 94%

Microgravity, Stem Cells, and Embryonic Development: Challenges and Opportunities for 3D Tissue Generation

Andreazzoli

Angeloni

Broccoli

et al. 2017

Front. Astron. Space Sci.

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Space is a challenging environment for the human body, due to the combined effects of reduced gravity (microgravity) and cosmic radiation. Known effects of microgravity range from the blood redistribution that affects the cardiovascular system and the eye to muscle wasting, bone loss, anemia, and immune depression. About cosmic radiation, the shielding provided by the spaceship hull is far less efficient than that afforded at ground level by the combined effects of the Earth atmosphere and magnetic field. The eye and its nervous layer (the retina) are affected by both microgravity and heavy ions exposure. Considering the importance of sight for long-term manned flights, visual research aimed at devising measures to protect the eye from environmental conditions of the outer space represents a special challenge to meet. In this review we focus on the impact of microgravity on embryonic development, discussing the roles of mechanical forces in the context of the neutral buoyancy the embryo experiences in the womb. At variance with its adverse effects on the adult human body, simulated microgravity may provide a unique tool for understanding the biomechanical events involved in the development and assembly in vitro of three-dimensional (3D) ocular tissues. Prospective benefits are the development of novel safety measures to protect the human eye from cosmic radiation in microgravity during long-term manned spaceflights in the outer space, as well as the generation of human 3D-retinas with its supporting structures to develop innovative and effective therapeutic options for degenerative eye diseases.

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Early Amphibian (Anuran) Morphogenesis Is Sensitive to Novel Gravitational Fields

Cited by 58 publications

References 0 publications

Amphibian development in the virtual absence of gravity.

Amphibian development in the virtual absence of gravity.

Effects of space environment on embryonic growth up to hatching of salamander eggs fertilized and developed during orbital flights.

Microgravity, Stem Cells, and Embryonic Development: Challenges and Opportunities for 3D Tissue Generation

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