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Advances in Space Biology: Cell Behavior in Microgravity

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A special issue of Applied Sciences (ISSN 2076-3417). This special issue belongs to the section "Applied Biosciences and Bioengineering".

Deadline for manuscript submissions: closed (31 October 2020) | Viewed by 46570

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Special Issue Editors

Dr. Maria A. Mariggiò

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Guest Editor

Department of Neuroscience, Imaging and Clinical Sciences, University “G. d’Annunzio” of Chieti-Pescara, 66100 Chieti, Italy
Interests: neuronal and skeletal muscle cells differentiation; intracellular Ca²⁺ dynamics; oxidative stress; live cell imaging; biomaterials; space biology
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Dr. Giulia Ricci

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Guest Editor

Department of Experimental Medicine, Second University of Naples, Naples, Italy
Interests: reproduction; embryonic development; cancer; biomaterials; space biology
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Special Issue Information

Dear Colleagues,

The last decades have seen an increasing number of space missions that, with the ambitious goal of colonizing the Moon and reaching Mars and other distant planets, have opened new areas of scientific research, which intend to build a better understanding of how the space environment affects the living systems. Nowadays, Space Biology has become a highly topical scientific field that has increasingly earned the interest of the Scientific Community. It is well documented that the gravitational force change, experienced by living organisms during space exploration, impacts significantly on several biological processes, inducing, for instance, mass loss in the muscolo-skeletal apparatus and changes in plant tropism and microbial virulence and resistance. The common line of all the responses induced by microgravity on living organisms is represented by mechanisms induced at the cellular and molecular levels. The cellular mechanisms triggered by microgravity have been disclosed only partially and are still under investigation. However, it is clear that all cell types, from prokaryotes to eukaryotes, react to microgravity, trying to adapt to it. This area of research, even if established for space exploration, has given new fundamental knowledge on how cells perceive the gravitational force and, more generally, the “physic” microenvironment in which they are embedded.

This Special Issue, "Advances in space biology: cell behavior in microgravity", has the goal to describe how Space Biology has modified our perception of cell biology. In particular, it aims to: a) focus on the most recent discoveries on microgravity-induced cell responses and highlight the different mechanisms and biological strategies by which cells (derived from all kingdoms of life) adapt/react to the space environment; b) define the molecular and cellular mechanisms induced by microgravity and develop possible protection strategies; c) finally, discuss the experimental assessment of the effects of real and simulated microgravity in order to delineate the positive and negative aspects of the chosen approaches and facilitate the interpretation of the results obtained.

Dr. Maria A. Mariggiò
Dr. Giulia Ricci
Guest Editors

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Keywords

Cell gravity sensing
Cell shape, cytoskeleton, adhesion
Microgravity-induced gene expression and regulation.
Cell metabolism, oxidative balance, oxidative stress
Cell proliferation, differentiation, adaptation under microgravity
Eukaryotic and prokaryotic behavior at microgravity
Control of miRNA expression under microgravity
Epigenetics and microgravity
Cell sprouting in microgravity
Microgravity-induced alteration of developmental processes
Space exploration, real microgravity and technological opportunities
Experimental models: microgravity simulators and biological models
Cell bioreactor development for Space laboratories

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Published Papers (11 papers)

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Editorial

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3 pages, 194 KiB

Open AccessEditorial

Advances in Space Biology: Cell Behavior in Microgravity

by Maria A. Mariggiò and Giulia Ricci

Appl. Sci. 2022, 12(22), 11575; https://doi.org/10.3390/app122211575 - 15 Nov 2022

Viewed by 1457

Abstract

The intrinsic nature of human beings always pushes them to search for knowledge of everything that surrounds them, from the depths of the sea to the peaks of the mountains up to the space expanses [...] Full article

(This article belongs to the Special Issue Advances in Space Biology: Cell Behavior in Microgravity)

Research

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13 pages, 1940 KiB

Open AccessArticle

Preparation of Human Muscle Precursor Cells for the MyoGravity Project’s Study of Cell Cultures in Experiment Units for Space Flight Purposes

by Ester Sara Di Filippo, Sara Chiappalupi, Michele Balsamo, Marco Vukich, Guglielmo Sorci and Stefania Fulle

Appl. Sci. 2022, 12(14), 7013; https://doi.org/10.3390/app12147013 - 12 Jul 2022

Cited by 4 | Viewed by 1825

Abstract

Long-time exposure to the microgravity conditions experienced during space flights induces alterations in the homeostasis of organs and tissues, including skeletal muscles, which undergo atrophy with the loss of mass and strength due to decreased size and altered composition of myofibers. Microgravity conditions can also affect the functionality of satellite cells, i.e., the adult stem cells providing the muscle precursors that are responsible for the growth and maintenance of muscle mass in adult life, as well as for muscle regeneration following a damage. The MyoGravity project, funded by Agenzia Spaziale Italiana (ASI), aimed to send human muscle precursor cells (huMPCs) on board the International Space Station (ISS) in order to study the effects of real microgravity on the differentiation capacity of this cell type. To this end, it was necessary to use a methodology to cultivate huMPCs inside dedicated space bioreactor devices (Experiment Units, EUs) specifically designed to cultivate cell cultures and perform scientific protocols in the space environment of the ISS. Here, we report the setting of several cell culture parameters to convert the EUs into suitable devices for biomedical experiments using huMPCs for space flight purposes. Full article

(This article belongs to the Special Issue Advances in Space Biology: Cell Behavior in Microgravity)

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11 pages, 2453 KiB

Open AccessArticle

Module to Support Real-Time Microscopic Imaging of Living Organisms on Ground-Based Microgravity Analogs

by Srujana Neelam, Audrey Lee, Michael A. Lane, Ceasar Udave, Howard G. Levine and Ye Zhang

Appl. Sci. 2021, 11(7), 3122; https://doi.org/10.3390/app11073122 - 1 Apr 2021

Cited by 7 | Viewed by 2611

Abstract

Since opportunities for spaceflight experiments are scarce, ground-based microgravity simulation devices (MSDs) offer accessible and economical alternatives for gravitational biology studies. Among the MSDs, the random positioning machine (RPM) provides simulated microgravity conditions on the ground by randomizing rotating biological samples in two axes to distribute the Earth’s gravity vector in all directions over time. Real-time microscopy and image acquisition during microgravity simulation are of particular interest to enable the study of how basic cell functions, such as division, migration, and proliferation, progress under altered gravity conditions. However, these capabilities have been difficult to implement due to the constantly moving frames of the RPM as well as mechanical noise. Therefore, we developed an image acquisition module that can be mounted on an RPM to capture live images over time while the specimen is in the simulated microgravity (SMG) environment. This module integrates a digital microscope with a magnification range of 20× to 700×, a high-speed data transmission adaptor for the wireless streaming of time-lapse images, and a backlight illuminator to view the sample under brightfield and darkfield modes. With this module, we successfully demonstrated the real-time imaging of human cells cultured on an RPM in brightfield, lasting up to 80 h, and also visualized them in green fluorescent channel. This module was successful in monitoring cell morphology and in quantifying the rate of cell division, cell migration, and wound healing in SMG. It can be easily modified to study the response of other biological specimens to SMG. Full article

(This article belongs to the Special Issue Advances in Space Biology: Cell Behavior in Microgravity)

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19 pages, 7396 KiB

Open AccessFeature PaperArticle

Microgravity Induces Transient EMT in Human Keratinocytes by Early Down-Regulation of E-Cadherin and Cell-Adhesion Remodeling

by Giulia Ricci, Alessandra Cucina, Sara Proietti, Simona Dinicola, Francesca Ferranti, Marcella Cammarota, Antonio Filippini, Mariano Bizzarri and Angela Catizone

Appl. Sci. 2021, 11(1), 110; https://doi.org/10.3390/app11010110 - 24 Dec 2020

Cited by 7 | Viewed by 2847

Abstract

Changes in cell–matrix and cell-to-cell adhesion patterns are dramatically fostered by the microgravity exposure of living cells. The modification of adhesion properties could promote the emergence of a migrating and invasive phenotype. We previously demonstrated that short exposure to the simulated microgravity of human keratinocytes (HaCaT) promotes an early epithelial–mesenchymal transition (EMT). Herein, we developed this investigation to verify if the cells maintain the acquired invasive phenotype after an extended period of weightlessness exposure. We also evaluated cells’ capability in recovering epithelial characteristics when seeded again into a normal gravitational field after short microgravity exposure. We evaluated the ultra-structural junctional features of HaCaT cells by Transmission Electron Microscopy and the distribution pattern of vinculin and E-cadherin by confocal microscopy, observing a rearrangement in cell–cell and cell–matrix interactions. These results are mirrored by data provided by migration and invasion biological assay. Overall, our studies demonstrate that after extended periods of microgravity, HaCaT cells recover an epithelial phenotype by re-establishing E-cadherin-based junctions and cytoskeleton remodeling, both being instrumental in promoting a mesenchymal–epithelial transition (MET). Those findings suggest that cytoskeletal changes noticed during the first weightlessness period have a transitory character, given that they are later reversed and followed by adaptive modifications through which cells miss the acquired mesenchymal phenotype. Full article

(This article belongs to the Special Issue Advances in Space Biology: Cell Behavior in Microgravity)

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9 pages, 5742 KiB

Open AccessCommunication

Behavior of Astrocytes Derived from Human Neural Stem Cells Flown onto Space and Their Progenies

by Sophia Shaka, Nicholas Carpo, Victoria Tran and Araceli Espinosa-Jeffrey

Appl. Sci. 2021, 11(1), 41; https://doi.org/10.3390/app11010041 - 23 Dec 2020

Cited by 2 | Viewed by 3453

Abstract

Long-term travel and prolonged stays for astronauts in outer space are imminent. To date more than 500 astronauts have experienced the extreme conditions of space flight including microgravity and radiation. Here we report that human neural stem cells (NSCs) flown onto space were successfully induced to the astrocyte phenotype when grown in fetal calf serum (FCS) supplemented medium. We want to emphasize that these astrocytes were generated after the space flight through a slow process lasting several weeks. Interestingly, we also found that these cells newly formed astrocytes, proliferated slowly but significantly and they showed a tendency to continue proliferating at the same pace. Astrocytes, a major type of glial cells, are key for the normal function of the central nervous system (CNS). They are also emerging as a critical component in most neurodegenerative diseases. Knowledge on the effects of space microgravity on them is of utmost importance for long duration space travel. Full article

(This article belongs to the Special Issue Advances in Space Biology: Cell Behavior in Microgravity)

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16 pages, 12018 KiB

Open AccessFeature PaperArticle

Microgravity-Induced Cell-to-Cell Junctional Contacts Are Counteracted by Antioxidant Compounds in TCam-2 Seminoma Cells

by Angela Catizone, Caterina Morabito, Marcella Cammarota, Chiara Schiraldi, Katia Corano Scheri, Francesca Ferranti, Maria A. Mariggiò and Giulia Ricci

Appl. Sci. 2020, 10(22), 8289; https://doi.org/10.3390/app10228289 - 23 Nov 2020

Cited by 3 | Viewed by 2542

Abstract

The direct impact of microgravity exposure on male germ cells, as well as on their malignant counterparts, has not been largely studied. In previous works, we reported our findings on a cell line derived from a human seminoma lesion (TCam-2 cell line) showing that acute exposure to simulated microgravity altered microtubule orientation, induced autophagy, and modified cell metabolism stimulating ROS production. Moreover, we demonstrated that the antioxidant administration prevented both TCam-2 microgravity-induced microtubule disorientation and autophagy induction. Herein, expanding previous investigations, we report that simulated microgravity exposure for 24 h induced the appearance, at an ultrastructural level, of cell-to-cell junctional contacts that were not detectable in cells grown at 1 g. In line with this result, pan-cadherin immunofluorescence analyzed by confocal microscopy, revealed the clustering of this marker at the plasma membrane level on microgravity exposed TCam-2 cells. The upregulation of cadherin was confirmed by Western blot analyses. Furthermore, we demonstrated that the microgravity-induced ROS increase was responsible for the distribution of cadherin nearby the plasma membrane, together with beta-catenin since the administration of antioxidants prevented this microgravity-dependent phenomenon. These results shed new light on the microgravity-induced modifications of the cell adhesive behavior and highlight the role of ROS as microgravity activated signal molecules. Full article

(This article belongs to the Special Issue Advances in Space Biology: Cell Behavior in Microgravity)

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Review

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17 pages, 1484 KiB

Open AccessReview

Advantages and Limitations of Current Microgravity Platforms for Space Biology Research

by Francesca Ferranti, Marta Del Bianco and Claudia Pacelli

Appl. Sci. 2021, 11(1), 68; https://doi.org/10.3390/app11010068 - 23 Dec 2020

Cited by 59 | Viewed by 12774

Abstract

Human Space exploration has created new challenges and new opportunities for science. Reaching beyond the Earth’s surface has raised the issue of the importance of gravity for the development and the physiology of biological systems, while giving scientists the tools to study the mechanisms of response and adaptation to the microgravity environment. As life has evolved under the constant influence of gravity, gravity affects biological systems at a very fundamental level. Owing to limited access to spaceflight platforms, scientists rely heavily on on-ground facilities that reproduce, to a different extent, microgravity or its effects. However, the technical constraints of counterbalancing the gravitational force on Earth add complexity to data interpretation. In-flight experiments are also not without their challenges, including additional stressors, such as cosmic radiation and lack of convection. It is thus extremely important in Space biology to design experiments in a way that maximizes the scientific return and takes into consideration all the variables of the chosen setup, both on-ground or on orbit. This review provides a critical analysis of current ground-based and spaceflight facilities. In particular, the focus was given to experimental design to offer the reader the tools to select the appropriate setup and to appropriately interpret the results. Full article

(This article belongs to the Special Issue Advances in Space Biology: Cell Behavior in Microgravity)

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16 pages, 1340 KiB

Open AccessReview

Microgravity, Bone Homeostasis, and Insulin-Like Growth Factor-1

by John Kelly Smith

Appl. Sci. 2020, 10(13), 4433; https://doi.org/10.3390/app10134433 - 27 Jun 2020

Cited by 7 | Viewed by 3474

Abstract

Astronauts at are risk of losing 1.0–1.5% of their bone mass for every month they spend in space despite their adherence to high impact exercise training programs and diets high in nutrients, potassium, calcium, and vitamin D, all designed to preserve the skeletal system. This article reviews the basics of bone formation and resorption and details how exposure to microgravity or simulated microgravity affects the structure and function of osteoblasts, osteocytes, osteoclasts, and their mesenchymal and hematologic stem cell precursors. It details the critical roles that insulin-like growth factor-1 and its receptor insulin-like growth factor-1 receptor (GFR1) play in maintaining bone homeostasis and how exposure of bone cells to microgravity affects the function of these growth factors. Lastly, it discusses the potential of tumor necrosis factor-related apoptosis-inducing ligand, syncytin-A, sclerostin inhibitors and recombinant IGF-1 as a bone-saving treatment for astronauts in space and during their colonization of the Moon. Full article

(This article belongs to the Special Issue Advances in Space Biology: Cell Behavior in Microgravity)

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14 pages, 980 KiB

Open AccessReview

Lipid Signalling in Human Immune Response and Bone Remodelling under Microgravity

by Marina Fava, Alessandro Leuti and Mauro Maccarrone

Appl. Sci. 2020, 10(12), 4309; https://doi.org/10.3390/app10124309 - 23 Jun 2020

Cited by 3 | Viewed by 3095

Abstract

Since the first Apollo mission in 1969, microgravity has been linked to many alterations of astronauts’ physiology, among which immunosuppression, altered inflammation and bone loss represent relevant examples. In the past 40 years, extensive investigations have been conducted in order to characterize the molecular mechanisms driving the alterations caused by prolonged weightlessness on human health. However, almost all studies eluded the role played by bioactive lipids, a vastly heterogeneous class of endogenous molecules, which, under normal conditions, control immune and bone homeostasis. This is somewhat surprising, because it is widely accepted that pathological derangement of the production or signalling of these endogenous compounds leads to the onset and/or progression of numerous diseases. In particular, eicosanoids and endocannabinoids are known to play a role in immune responses and bone remodelling. Both classes represent the only lipids as yet investigated in Space, and are increasingly recognised as promising therapeutic candidates to combat different human disorders. This review summarizes evidence gathered in the past two decades on the changes in these two pivotal lipid signalling systems, through both simulated and authentic weightlessness (i.e., on board the International Space Station and in parabolic flights). Full article

(This article belongs to the Special Issue Advances in Space Biology: Cell Behavior in Microgravity)

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21 pages, 1113 KiB

Open AccessFeature PaperReview

Putative Receptors for Gravity Sensing in Mammalian Cells: The Effects of Microgravity

by Michele Aventaggiato, Federica Barreca, Enza Vernucci, Mariano Bizzarri, Elisabetta Ferretti, Matteo A. Russo and Marco Tafani

Appl. Sci. 2020, 10(6), 2028; https://doi.org/10.3390/app10062028 - 17 Mar 2020

Cited by 11 | Viewed by 5440

Abstract

Gravity is a constitutive force that influences life on Earth. It is sensed and translated into biochemical stimuli through the so called “mechanosensors”, proteins able to change their molecular conformation in order to amplify external cues causing several intracellular responses. Mechanosensors are widely represented in the human body with important structures such as otholiths in hair cells of vestibular system and statoliths in plants. Moreover, they are also present in the bone, where mechanical cues can cause bone resorption or formation and in muscle in which mechanical stimuli can increase the sensibility for mechanical stretch. In this review, we discuss the role of mechanosensors in two different conditions: normogravity and microgravity, emphasizing their emerging role in microgravity. Microgravity is a singular condition in which many molecular changes occur, strictly connected with the modified gravity force and free fall of bodies. Here, we first summarize the most important mechanosensors involved in normogravity and microgravity. Subsequently, we propose muscle LIM protein (MLP) and sirtuins as new actors in mechanosensing and signaling transduction under microgravity. Full article

(This article belongs to the Special Issue Advances in Space Biology: Cell Behavior in Microgravity)

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Other

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8 pages, 3578 KiB

Open AccessFeature PaperBrief Report

Human Neural Stem Cells Flown into Space Proliferate and Generate Young Neurons

by Carlos Cepeda, Laurent Vergnes, Nicholas Carpo, Matthew J. Schibler, Laurent A. Bentolila, Fathi Karouia and Araceli Espinosa-Jeffrey

Appl. Sci. 2019, 9(19), 4042; https://doi.org/10.3390/app9194042 - 27 Sep 2019

Cited by 11 | Viewed by 4726

Abstract

Here we demonstrate that human neural stem cells (NSCs) proliferate while in space and they express specific NSC markers after being in space. NSCs displayed both higher oxygen consumption and glycolysis than ground controls. These cells also kept their ability to become young neurons. Electrophysiological recordings of space NSC-derived neurons showed immature cell membrane properties characterized by small capacitance and very high input resistance. Current injections elicited only an incipient action potential. No spontaneous synaptic events could be detected, suggesting their immature status even though most recorded cells displayed complex morphology and numerous cell processes. Ascertaining the origin of the NSCs’ increased energy requirement is of the essence in order to design effective measures to minimize health risks associated with long-duration human spaceflight missions. Full article

(This article belongs to the Special Issue Advances in Space Biology: Cell Behavior in Microgravity)

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