Artefactual effects of oxygen on cell culture models of cellular senescence and stem cell biology

In life sciences, modelling of the in vivo conditions using in vitro models is an important tool to generate knowledge. Although aerobic organisms including mammals depend on accurate oxygen tension, mimicking physiological conditions in cell culture experiments is not very common. Due to the need for simple technical and experimental design, the requirement for simulating the in vivo oxygen tension parameters has been neglected over long time. Fortunately, due to increasing knowledge in recent years the attention has shifted towards this scientific demand. In this short review, we summarize data substantiating the necessity to adequately mimic physiological oxygen tension using cell culture models in life science research. J. Cell. Physiol. 226: 315–321, 2011. © 2010 Wiley‐Liss, Inc.

[1]  W. Tan,et al.  The effect of low oxygen tension on the in vitro life span of mouse epidermal keratinocytes , 2002 .

[2]  S. Flamant,et al.  Enhanced cloning efficiency of mouse bone marrow macrophage progenitors correlates with increased content of CSF-1 receptor of their progeny at low oxygen tension. , 2003, Microbes and infection.

[3]  T. Zglinicki,et al.  Similar gene expression pattern in senescent and hyperoxic-treated fibroblasts. , 1998, The journals of gerontology. Series A, Biological sciences and medical sciences.

[4]  V. Ferrans,et al.  Ras Proteins Induce Senescence by Altering the Intracellular Levels of Reactive Oxygen Species* , 1999, The Journal of Biological Chemistry.

[5]  S. Maynard,et al.  Fibroblasts from long‐lived Snell dwarf mice are resistant to oxygen‐induced in vitro growth arrest , 2006, Aging cell.

[6]  S. Perrault,et al.  Low oxygen delays fibroblast senescence despite shorter telomeres , 2008, Biogerontology.

[7]  S. Petersen,et al.  Preferential accumulation of single-stranded regions in telomeres of human fibroblasts. , 1998, Experimental cell research.

[8]  J. Remacle,et al.  Comparative study of oxygen toxicity in human fibroblasts and endothelial cells , 1990, Journal of cellular physiology.

[9]  M. Sporn,et al.  Hypoxia upregulates the synthesis of TGF-beta 1 by human dermal fibroblasts. , 1991, The Journal of investigative dermatology.

[10]  K. Wittern,et al.  Aging skin is functionally anaerobic: Importance of coenzyme Q10 for anti aging skin care , 2008, BioFactors.

[11]  T. Storch,et al.  Oxygen concentration regulates EGF-induced proliferation and EGF-receptor down regulation. , 1988, Biochemical and biophysical research communications.

[12]  Wasim S Khan,et al.  The matrix-forming phenotype of cultured human meniscus cells is enhanced after culture with fibroblast growth factor 2 and is further stimulated by hypoxia , 2006, Arthritis research & therapy.

[13]  N. Chondrogianni,et al.  Exposure of Human Diploid Fibroblasts to Hypoxia Extends Proliferative Life Span , 2007, Annals of the New York Academy of Sciences.

[14]  M Raes,et al.  Importance of Se-glutathione peroxidase, catalase, and Cu/Zn-SOD for cell survival against oxidative stress. , 1994, Free radical biology & medicine.

[15]  Wasim S Khan,et al.  Hypoxic conditions increase hypoxia-inducible transcription factor 2α and enhance chondrogenesis in stem cells from the infrapatellar fat pad of osteoarthritis patients , 2007, Arthritis research & therapy.

[16]  E. Papoutsakis,et al.  Oxygen tension alters the effects of cytokines on the megakaryocyte, erythrocyte, and granulocyte lineages. , 1998, Experimental hematology.

[17]  J. Remacle,et al.  Signal transduction in H2O2-induced senescence-like phenotype in human diploid fibroblasts. , 2002, Free radical biology & medicine.

[18]  J. Campisi,et al.  Oxygen accelerates the accumulation of mutations during the senescence and immortalization of murine cells in culture , 2003, Aging cell.

[19]  F. Guilak,et al.  Influence of oxygen on the proliferation and metabolism of adipose derived adult stem cells , 2005, Journal of cellular physiology.

[20]  G. Saretzki,et al.  Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence? , 1995, Experimental cell research.

[21]  R. G. Allen,et al.  Effects of ambient oxygen concentration on the growth and antioxidant defenses of of human cell cultures established from fetal and postnatal skin. , 2002, Free Radical Biology & Medicine.

[22]  S. Melov,et al.  Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts , 2003, Nature Cell Biology.

[23]  L. Hayflick,et al.  The serial cultivation of human diploid cell strains. , 1961, Experimental cell research.

[24]  Farshid Guilak,et al.  Chondrocytic differentiation of human adipose-derived adult stem cells in elastin-like polypeptide. , 2006, Biomaterials.

[25]  J. R. Smith,et al.  Extension of the lifespan of cultured normal human diploid cells by vitamin E. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[26]  C. Robert,et al.  Expression profiles of p53 and p66shc during oxidative stress-induced senescence in fetal bovine fibroblasts. , 2004, Experimental cell research.

[27]  L. Packer,et al.  Low oxygen concentration extends the lifespan of cultured human diploid cells , 1977, Nature.

[28]  J. Shay,et al.  Historical claims and current interpretations of replicative aging , 2002, Nature Biotechnology.

[29]  Feng Zhao,et al.  Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs , 2006, Journal of cellular physiology.

[30]  V. Zachar,et al.  Temporal transcriptome of mouse ATDC5 chondroprogenitors differentiating under hypoxic conditions. , 2006, Experimental cell research.

[31]  R. Kirsner,et al.  Low oxygen stimulates proliferation of fibroblasts seeded as single cells , 1993, Journal of cellular physiology.

[32]  P. Roepstorff,et al.  Role of TGF-beta1-independent changes in protein neosynthesis, p38alphaMAPK, and cdc42 in hydrogen peroxide-induced senescence-like morphogenesis. , 2008, Free radical biology & medicine.

[33]  J. Crapo,et al.  Superoxide dismutase and pulmonary oxygen toxicity. , 1974, The American journal of physiology.

[34]  Barry Halliwell,et al.  Oxidative stress in cell culture: an under‐appreciated problem? , 2003, FEBS letters.

[35]  R. Reddel.  The role of senescence and immortalization in carcinogenesis. , 2000, Carcinogenesis.

[36]  Bernard A Roos,et al.  Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. , 2006, Bone.

[37]  M. Blasco,et al.  Putting the stress on senescence. , 2001, Current opinion in cell biology.

[38]  H. Takagi,et al.  Low oxygen tension decreases receptor binding of peptide growth factors in dermal fibroblast cultures. , 1994, Experimental cell research.

[39]  D. Harman.  Aging: a theory based on free radical and radiation chemistry. , 1956, Journal of gerontology.

[40]  M. Green,et al.  Atmospheric oxygen accelerates the induction of a post-mitotic phenotype in human dermal fibroblasts: the key protective role of glutathione. , 2000, Differentiation; research in biological diversity.

[41]  R. Schofield.  The relationship between the spleen colony-forming cell and the haemopoietic stem cell. , 1978, Blood cells.

[42]  J. R. Smith,et al.  Extension of the lifespan of cultured normal human diploid cells by vitamin E: a reevaluation. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[43]  T. Zhao,et al.  Characteristics of Neural Stem Cells Expanded in Lowered Oxygen and the Potential Role of Hypoxia-Inducible Factor-1Alpha , 2007, Neurosignals.

[44]  A. Balin,et al.  Oxygen modulates the growth of skin fibroblasts , 2002, In Vitro Cellular & Developmental Biology - Animal.

[45]  G. Pawelec,et al.  Effects of a reduced oxygen tension culture system on human T cell clones as a function of in vitro age , 2004, Experimental Gerontology.

[46]  H. Ho,et al.  Low oxygen tension alleviates oxidative damage and delays cellular senescence in G6PD-deficient cells , 2007, Free radical research.

[47]  K. Okaichi,et al.  Differential Activation of ERK 1/2 and JNK in Normal Human Fibroblast-like Cells in Response to UVC Radiation Under Different Oxygen Tensions¶ , 2000, Photochemistry and photobiology.

[48]  Regina Brunauer,et al.  Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan , 2007, Aging cell.

[49]  V. Falanga,et al.  The levels and kinetics of oxygen tension detectable at the surface of human dermal fibroblast cultures , 2000, Journal of cellular physiology.

[50]  C. Verfaillie,et al.  Biology of umbilical cord blood progenitors in bone marrow niches. , 2007, Blood.

[51]  J. Shay,et al.  Hayflick, his limit, and cellular ageing , 2000, Nature Reviews Molecular Cell Biology.

[52]  G. Saretzki,et al.  MitoQ counteracts telomere shortening and elongates lifespan of fibroblasts under mild oxidative stress , 2003, Aging cell.

[53]  J. Remacle,et al.  Importance of various antioxidant enzymes for cell stability. Confrontation between theoretical and experimental data. , 1992, The Biochemical journal.

[54]  M. Sporn,et al.  Hypoxia upregulates the synthesis of tgf-β1 by human dermal fibroblasts , 1991 .

[55]  J. Glowacki,et al.  Low Oxygen Tension Enhances Chondroinduction by Demineralized Bone Matrix in Human Dermal Fibroblasts in vitro , 2005, Cells Tissues Organs.

[56]  J. Campisi,et al.  Cellular senescence: when bad things happen to good cells , 2007, Nature Reviews Molecular Cell Biology.

[57]  Alfredo Quiñones-Hinojosa,et al.  Oxygen in stem cell biology: a critical component of the stem cell niche. , 2010, Cell stem cell.

[58]  R. G. Allen,et al.  Effects of establishing cell cultures and cell culture conditions on the proliferative life span of human fibroblasts isolated from different tissues and donors of different ages. , 2002, Experimental cell research.

[59]  M. Boulton,et al.  Oxygen modulates the response of the retinal pigment epithelium to basic fibroblast growth factor and epidermal growth factor by receptor regulation. , 1996, Investigative ophthalmology & visual science.

[60]  J. White,et al.  On the control of germ cell development in Caenorhabditis elegans. , 1981, Developmental biology.

[61]  Johannes Schwarz,et al.  Low atmospheric oxygen avoids maturation, senescence and cell death of murine mesencephalic neural precursors , 2005, Journal of neurochemistry.

[62]  V. Falanga,et al.  Low oxygen tension stimulates collagen synthesis and COL1A1 transcription through the action of TGF‐β1 , 2002, Journal of cellular physiology.

[63]  M. Simon,et al.  The role of oxygen availability in embryonic development and stem cell function , 2008, Nature Reviews Molecular Cell Biology.

[64]  S. Lowe,et al.  Oncogenic ras Provokes Premature Cell Senescence Associated with Accumulation of p53 and p16INK4a , 1997, Cell.

[65]  L. Herzenberg,et al.  Importance of culturing primary lymphocytes at physiological oxygen levels , 2007, Proceedings of the National Academy of Sciences.

[66]  J. Shay,et al.  Cellular senescence as a tumor-protection mechanism: the essential role of counting. , 2001, Current opinion in genetics & development.

[67]  V. Zachar,et al.  Physiological oxygen tension is relevant to MHC-1 expression, spontaneous transformation, and interferon response of in vitro aging murine fibroblasts , 1993, Experimental Gerontology.

[68]  D. Lübbers,et al.  The cutaneous uptake of atmospheric oxygen contributes significantly to the oxygen supply of human dermis and epidermis , 2002, The Journal of physiology.