Advertisement

Human Physiology

, Volume 44, Issue 6, pp 696–705 | Cite as

Multipotent Mesenchymal Stromal Cells and Extracellular Matrix: Regulation under Hypoxia

  • E. R. AndreevaEmail author
  • D. K. Matveeva
REVIEWS
  • 17 Downloads

Abstract

Over the past 20 years a significant data have been accumulated indicating that the extracellular matrix (ECM) is not just an inert substrate. The ECM acts as a multifunctional dynamic compartment that regulates the functions of various cell systems, including niches of stem and progenitor cells. The ECM is a complex network of macromolecules with different physical and biochemical properties. ECM production, deposition, and degradation play an important role in both physiological and reparative tissue remodeling. ECM biology is therefore of considerable interest for elucidating the mechanisms that govern various tissue niches in vivo and producing ECMs ex vivo for tissue engineering and regenerative medicine. The review summarizes current knowledge about the role that an important microenvironmental factor—tissue oxygen level (“physiological” hypoxia) plays in the biology of the ECM of stromal lineage cells.

Keywords:

multipotent mesenchymal stromal (stem) cells extracellular matrix “physiological” hypoxia prolyl hydrolases hypoxia-induced transcription factor (HIF) 

Notes

REFERENCES

  1. 1.
    Schofield, R., The relationship between the spleen colony-forming cell and the haemopoietic stem cell, Blood Cells, 1978, vol. 4, nos. 1–2, p. 7.Google Scholar
  2. 2.
    Watt, F.M. and Huck, W.T., Role of the extracellular matrix in regulating stem cell fate, Nat. Rev. Mol. Cell. Biol., 2013, vol. 14, p. 467.CrossRefGoogle Scholar
  3. 3.
    Lane, S.W., Williams, D.A., and Watt, F.M., Modulating the stem cell niche for tissue regeneration, Nat. Biotechnol., 2014, vol. 32, p. 795.CrossRefGoogle Scholar
  4. 4.
    Rojas-Ríos, P. and González-Reyes, A., Concise review: The plasticity of stem cell niches: a general property behind tissue homeostasis and repair, Stem Cells, 2014, vol. 32, no. 4, p. 852.CrossRefGoogle Scholar
  5. 5.
    Gattazzo, F., Urciuolo, A., and Bonaldo, P., Extracellular matrix: a dynamic microenvironment for stem cell niche, Biochim. Biophys. Acta, 2014, vol. 1840, p. 2506.CrossRefGoogle Scholar
  6. 6.
    Watt, F.M. and Hogan, B.L., Out of Eden: stem cells and their niches, Science, 2000, vol. 287, no. 5457, p. 1427.CrossRefGoogle Scholar
  7. 7.
    Kolf, C.M., Cho, E., and Tuan, R.S., Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation, Arthritis Res. Ther., 2007, vol. 9, no. 1, p. 204.CrossRefGoogle Scholar
  8. 8.
    Hynes, R.O., The extracellular matrix: not just pretty fibrils, Science, 2009, vol. 326, no. 5957, p. 1216.CrossRefGoogle Scholar
  9. 9.
    Naba, A., Clauser, K.R., Ding, H., et al., The extracellular matrix: tools and insights for the “omics” era, Matrix Biol., 2016, vol. 49, p. 10.CrossRefGoogle Scholar
  10. 10.
    Rhodes, J.M. and Simons, M., The extracellular matrix and blood vessel formation: not just a scaffold, J. Cell Mol. Med., 2007, vol. 11, p. 176.CrossRefGoogle Scholar
  11. 11.
    Yue, B., Biology of the extracellular matrix: an overview, Glaucoma, 2014, vol. 23, no. 8, p. 20.CrossRefGoogle Scholar
  12. 12.
    Ragelle, H., Naba, A., Larson, B.L., et al., Comprehensive proteomic characterization of stem cell-derived extracellular matrices, Biomaterials, 2017, vol. 128, p. 147.CrossRefGoogle Scholar
  13. 13.
    Canty, E.G. and Kadler, K.E., Procollagen trafficking, processing and fibrillogenesis, J. Cell Sci., 2005, vol. 118, no. 2005, p. 1341.Google Scholar
  14. 14.
    Kadler, K.E., Baldock, C., Bella, J., and Boot-Handford, R.P., Collagens at a glance, J. Cell Sci., 2007, vol. 120, p. 1955.CrossRefGoogle Scholar
  15. 15.
    Ricard-Blum, S., The collagen family, Cold Spring Harbor Perspect. Biol., 2011, vol. 3, no. 1, p. a004978.CrossRefGoogle Scholar
  16. 16.
    Lu, P., Takai, K., Weaver, V.M., and Werb, Z., Extracellular matrix degradation and remodeling in development and disease, Cold Spring Harbor Perspect. Biol., 2011, vol. 3, no. 12, p. a005058.CrossRefGoogle Scholar
  17. 17.
    Apte, S.S. and Parks, W.C., Metalloproteinases: a parade of functions in matrix biology and an outlook for the future, Matrix Biol., 2015, vol. 44–46, p. 1.CrossRefGoogle Scholar
  18. 18.
    Bonnans, C., Chou, J., and Werb, Z., Remodeling the extracellular matrix in development and disease, Nat. Rev. Mol. Cell Biol., 2014, vol. 15, p. 786.CrossRefGoogle Scholar
  19. 19.
    Popa, S.J., Stewart, S.E., and Moreau, K., Unconventional secretion of annexins and galectins, Semin. Cell Dev. Biol., 2018, vol. 9521, no. 17, p. 30582.Google Scholar
  20. 20.
    Karin, N., The multiple faces of CXCL12 (SDF-1α) in the regulation of immunity during health and disease, J. Leukocyte Biol., 2010, vol. 88, p. 463.CrossRefGoogle Scholar
  21. 21.
    Donato, R., Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type, Biochim. Biophys. Acta, 1999, vol. 1450, p. 191.CrossRefGoogle Scholar
  22. 22.
    Gelse, K., Poschl, E., and Aigner, T., Collagens-structure, function, and biosynthesis, Adv. Drug. Delivery Rev., 2003, vol. 55, p. 1531.CrossRefGoogle Scholar
  23. 23.
    Heng, B.C., Cao, T., Stanton, L.W., et al., Strategies for directing the differentiation of stem cells into the osteogenic lineage in vitro, J. Bone Miner. Res., 2004, vol. 19, no. 9, p. 1379.CrossRefGoogle Scholar
  24. 24.
    Lama, J. and Seguraa, T., The modulation of MSC integrin expression by RGD presentation, Biomaterials, 2013, vol. 34, no. 16, p. 3938.CrossRefGoogle Scholar
  25. 25.
    Samsonraj, R.M., Raghunath, M., Nurcombe, V., et al., Concise review: multifaceted characterization of human mesenchymal stem cells for use in regenerative medicine, Stem Cells Transl. Med., 2017, vol. 6, no. 12, p. 2173.CrossRefGoogle Scholar
  26. 26.
    Salasznyk, R.M., Williams, W.A., Boskey, A., et al., Adhesion to vitronectin and collagen I promotes osteogenic differentiation of human mesenchymal stem cells, J. Biomed. Biotechnol., 2004, vol. 2004, no. 1, p. 24.CrossRefGoogle Scholar
  27. 27.
    Mizuno, M., Fujisawa, R., and Kuboki, Y., Type I collagen-induced osteoblastic differentiation of bone-marrow cells mediated by collagen-alpha2beta1 integrin interaction, J. Cell Physiol., 2000, vol. 184, no. 2, p. 207.CrossRefGoogle Scholar
  28. 28.
    Park, Y.B., Seo, S., Kim, J.A., et al., Effect of chondrocyte-derived early extracellular matrix on chondrogenesis of placenta-derived mesenchymal stem cells, Biomed. Mater., 2015, vol. 10, no. 3, p. 035014.CrossRefGoogle Scholar
  29. 29.
    Humphrey, J.D., Eric, R. Dufresne, E.R., and Martin, A.S., Mechanotransduction and extracellular matrix homeostasis, Nat. Rev. Mol. Cell Biol., 2014, vol. 15, no. 12, p. 802.CrossRefGoogle Scholar
  30. 30.
    Li, B., Moshfegh, P., Lin, Z., et al., Mesenchymal stem cells exploit extracellular matrix as mechanotransducer, Sci. Rep., 2013, vol. 3, p. 2425.CrossRefGoogle Scholar
  31. 31.
    Qian, L. and Saltzman, W.M., Improving the expansion and neuronal differentiation of mesenchymal stem cells through culture surface modification, Biomaterials, 2004, vol. 25, p. 1331.CrossRefGoogle Scholar
  32. 32.
    Matsubara, T., Tsutsumi, S., Pan, H., et al., A new technique to expand human mesenchymal stem cells using basement membrane extracellular matrix, Biochem. Biophys. Res. Commun., 2004, vol. 313, p. 503.CrossRefGoogle Scholar
  33. 33.
    Mao, Y., Hoffman, T., Wu, A., et al., Cell type-specific extracellular matrix guided the differentiation of human mesenchymal stem cells in 3D polymeric scaffold, J. Mater. Sci. Mater. Med., 2017, vol. 28, no. 7, p. 100.CrossRefGoogle Scholar
  34. 34.
    Hashimoto, J., Kariya, Y., and Miyazaki, K., Regulation of proliferation and chondrogenic differentiation of human mesenchymal stem cells by laminin-5 (laminin-332), Stem Cells, 2006, vol. 24, p. 2346.CrossRefGoogle Scholar
  35. 35.
    Kular, J.K., Basu, S., and Sharma, R.I., The extracellular matrix: Structure, composition, age-related differences, tools for analysis and applications for tissue engineering, J. Tissue Eng., 2014, vol. 5, p. 2041731414557112.CrossRefGoogle Scholar
  36. 36.
    Qu, F., Li, Q., Wang, X., et al., Maturation state and matrix microstructure regulate interstitial cell migration in dense connective tissues, Sci. Rep., 2018, vol. 8, no. 1, p. 3295.CrossRefGoogle Scholar
  37. 37.
    Brauer, P.R., MMPs—role in cardiovascular development and disease, Front. Biosci., 2006, vol. 11, p. 447.CrossRefGoogle Scholar
  38. 38.
    Vu, T.H. and Werb, Z., Matrix metalloproteinases: effectors of development and normal physiology, Genes Dev., 2000, vol. 14, p. 2123.CrossRefGoogle Scholar
  39. 39.
    Nam, H.S., Kwon, I., Lee, B.H., et al., Effects of mesenchymal stem cell treatment on the expression of matrix metalloproteinases and angiogenesis during ischemic stroke recovery, PloS One, 2015, vol. 10, p. e0144218.CrossRefGoogle Scholar
  40. 40.
    Jiang, F., Ma, J., Liang, Y., et al., Amniotic mesenchymal stem cells can enhance angiogenic capacity via MMPs in vitro and in vivo, Biomed. Res. Int., 2015, vol. 2015, p. 324014.Google Scholar
  41. 41.
    Almalki, S.G. and Agrawal, D.K., Effects of matrix metalloproteinases on the fate of mesenchymal stem cells, Stem Cell Res. Ther., 2016, vol. 7, no. 1, p. 129.CrossRefGoogle Scholar
  42. 42.
    Kasper, G., Glaeser, J.D., Geissler, S., et al., Matrix metalloprotease activity is an essential link between mechanical stimulus and mesenchymal stem cell behavior, Stem Cells, 2007, vol. 25, p. 1985.CrossRefGoogle Scholar
  43. 43.
    Higgins, D.F., Kimura, K., Bernhardt, W.M., et al., Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition, J. Clin. Invest., 2007, vol. 117, p. 3810.Google Scholar
  44. 44.
    Halberg, N., Khan, T., Trujillo, M. E., et al., Hypoxia-inducible factor 1α induces fibrosis and insulin resistance in white adipose tissue, Mol. Cell. Biol., 2009, vol. 29, p. 4467.CrossRefGoogle Scholar
  45. 45.
    Moon, J.O., Welch, T.P., Gonzalez, F.J., and Copple, B.L., Reduced liver fibrosis in hypoxia-inducible factor-1α-deficient mice, Am. J. Physiol. Gastrointest. Liver Physiol., 2009, vol. 296, p. 582.CrossRefGoogle Scholar
  46. 46.
    Berg, J.T., Breen, E.C., Fu, Z., et al., Alveolar hypoxia increases gene expression of extracellular matrix proteins and platelet-derived growth factor-B in lung parenchyma, Am. J. Respir. Crit. Care Med., 1998, vol. 158, p. 1920.CrossRefGoogle Scholar
  47. 47.
    Roth, K.J. and Copple, B.L., Role of hypoxia-inducible factors in the development of liver fibrosis, Cell Mol. Gastroenterol. Hepatol., 2015, vol. 1, no. 6, p. 589.CrossRefGoogle Scholar
  48. 48.
    Gillies, R.J. and Gatenby, R.A., Hypoxia and adaptive landscapes in the evolution of carcinogenesis, Cancer Metastasis Rev., 2007, vol. 26, p. 311.CrossRefGoogle Scholar
  49. 49.
    Kalluri, R., The biology and function of fibroblasts in cancer, Nat. Rev. Cancer, 2016, vol. 16, p. 582.CrossRefGoogle Scholar
  50. 50.
    Conklin, M.W., Eickhoff, J.C., Riching, K.M., et al., Aligned collagen is a prognostic signature for survival in human breast carcinoma, Am. J. Pathol., 2011, vol. 178, p. 1221.CrossRefGoogle Scholar
  51. 51.
    Gilkes, B.M., Semenza, G.L., and Wirtz, D., Hypoxia and the extracellular matrix: drivers of tumour metastasis, Nat. Rev. Cancer, 2014, vol. 14, no. 6, p. 430.CrossRefGoogle Scholar
  52. 52.
    Buravkova, L.B., Andreeva, E.R., Gogvadze, V., and Zhivotovsky, B., Mesenchymal stem cells and hypoxia: Where are we? Mitochondrion, 2014, vol. 19, p. 1567.CrossRefGoogle Scholar
  53. 53.
    Riis, S., Stensballe, A., Emmersen, J., et al., Mass spectrometry analysis of adipose-derived stem cells reveals a significant effect of hypoxia on pathways regulating extracellular matrix, Stem Cell Res. Ther., 2016, vol. 7, p. 52.CrossRefGoogle Scholar
  54. 54.
    Ejtehadifar, M., Shamsasenjan, K., Movassagh-pour, A., et al., The effect of hypoxia on mesenchymal stem cell biology, Adv. Pharm. Bull., 2015, vol. 5, no. 2, p. 141.CrossRefGoogle Scholar
  55. 55.
    Volkmer, E., Kallukalam, B.C., Maertz, J., et al., Hypoxic preconditioning of human mesenchymal stem cells overcomes hypoxia-induced inhibition of osteogenic differentiation, Tissue Eng., Part A, 2010, vol. 16, no. 1, p. 153.CrossRefGoogle Scholar
  56. 56.
    Yang, D.C., Yang, M.H., Tsai, C.C., et al., Hypoxia inhibits osteogenesis in human mesenchymal stem cells through direct regulation of RUNX2 by TWIST, PloS One, 2011, vol. 6, no. 9, p. 23965.CrossRefGoogle Scholar
  57. 57.
    Fehrer, C., Brunauer, R., Laschober, G., et al., Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan, Aging Cell, 2007, vol. 6, no. 6, p. 745.CrossRefGoogle Scholar
  58. 58.
    Dos Santos, F., Andrade, P.Z., Boura, J.S., et al., Ex vivo expansion of human mesenchymal stem cells: a more effective cell proliferation kinetics and metabolism under hypoxia, J. Cell Physiol., 2010, vol. 223, no. 1, p. 27.Google Scholar
  59. 59.
    Yang, S., Pilgaard, L., Chase, L.G., et al., Defined xenogeneic-free and hypoxic environment provides superior conditions for long-term expansion of human adipose-derived stem cells, Tissue Eng., Part C, 2012, vol. 18, no. 8, p. 593.CrossRefGoogle Scholar
  60. 60.
    Tamama, K., Kawasaki, H., Kerpedjieva, S.S., et al., Differential roles of hypoxia inducible factor subunits in multipotential stromal cells under hypoxic condition, J. Cell Biochem., 2011, vol. 112, no. 3, p. 804.CrossRefGoogle Scholar
  61. 61.
    Zhang, P., Ha, N., Dai, Q., et al., Hypoxia suppresses osteogenesis of bone mesenchymal stem cells via the extracellular signal-regulated 1/2 and p38-mitogen activated protein kinase signaling pathways, Mol. Med. Rep., 2017, vol. 16, no. 4, p. 5515.CrossRefGoogle Scholar
  62. 62.
    Salim, A., Nacamuli, R.P., Morgan, E.F., et al., Transient changes in oxygen tension inhibit osteogenic differentiation and Runx2 expression in osteoblasts, J. Biol. Chem., 2004, vol. 279, no. 38, p. 40007.CrossRefGoogle Scholar
  63. 63.
    Khan, W.S., Adesida, A.B., Tew, S.R., et al., Bone marrow-derived mesenchymal stem cells express the pericyte marker 3G5 in culture and show enhanced chondrogenesis in hypoxic conditions, J. Orthop. Res., 2010, vol. 28, no. 6, p. 834.Google Scholar
  64. 64.
    Merceron, C., Vinatier, C., Portron, S., et al., Differential effects of hypoxia on osteochondrogenic potential of human adipose-derived stem cells, Am. J. Physiol. Cell Physiol., 2010, vol. 298, no. 2, p. 355.CrossRefGoogle Scholar
  65. 65.
    Shang, J., Liu, H., Li, J., and Zhou, Y., Roles of hypoxia during the chondrogenic differentiation of mesenchymal stem cells, Curr. Stem Cell Res. Ther., 2014, vol. 9, no. 2, p. 141.CrossRefGoogle Scholar
  66. 66.
    Taheem, D.K., Foyt, D.A., Loaiza, S., et al., Differential regulation of human bone marrow mesenchymal stromal cell chondrogenesis by hypoxia inducible factor-1α hydroxylase inhibitors, Stem Cells, 2018. doi 10.1002/stem.2844Google Scholar
  67. 67.
    Kumar, P., Satyam, A., Cigognini, D., et al., Low oxygen tension and macromolecular crowding accelerate extracellular matrix deposition in human corneal fibroblast culture, J. Tissue Eng. Regener. Med., 2018, vol. 12, no. 1, p. 6.CrossRefGoogle Scholar
  68. 68.
    Falanga, V., Martin, T.A., Tekasi, H., et al., Low oxygen tension increases mRNA levels of α1 (I) procollagen in human dermal fibroblasts, J. Cell Physiol., 1993, vol. 157, p. 408.CrossRefGoogle Scholar
  69. 69.
    Tamamori, M., Ito, H., Hiroe, M., et al., Stimulation of collagen synthesis in rat cardiac fibroblasts by exposure to hypoxic culture conditions and suppression of the effect by natriuretic peptides, Cell Biol. Int., 1997, vol. 21, p. 175.CrossRefGoogle Scholar
  70. 70.
    Norman, J.T., Clark, I.M., and Garcia, P.L., Hypoxia promotes fibrogenesis in human renal fibroblasts, Kidney Int., 2000, vol. 58, p. 2351.CrossRefGoogle Scholar
  71. 71.
    Yin, L.X., Motz, K.M., Samad, I., et al., Fibroblasts in hypoxic conditions mimic laryngotracheal stenosis, Otolaryngol. Head Neck Surg., 2017, vol. 156, no. 5, p. 886.CrossRefGoogle Scholar
  72. 72.
    Laitala, A. and Erler, J.T., Hypoxic signaling in tumor stroma, Front. Oncol., 2018, vol. 8, p. 189.CrossRefGoogle Scholar
  73. 73.
    Koyasu, S., Kobayashi, M., Goto, Y., et al., Regulatory mechanisms of hypoxia-inducible factor 1 activity: Two decades of knowledge, Cancer Sci., 2018, vol. 109, no. 3, p. 560.CrossRefGoogle Scholar
  74. 74.
    Aro, E., Khatri, R., Gerard-O’Riley, R., et al., Hypoxia-inducible factor-1 (HIF-1) but not HIF-2 is essential for hypoxic induction of collagen prolyl 4-hydroxylases in primary newborn mouse epiphyseal growth plate chondrocytes, J. Biol. Chem., 2012, vol. 287, p. 37134.CrossRefGoogle Scholar
  75. 75.
    Petrova, V., Annicchiarico-Petruzzelli, M., Melino, G., and Amelio, I., The hypoxic tumor microenvironment, Oncogenesis, 2018, vol. 7, no. 1, p. 10.CrossRefGoogle Scholar
  76. 76.
    Tiwari, A., Lefevre, C., Kirkland, M.A., et al., Comparative gene expression profiling of stromal cell matrices that support expansion of hematopoietic stem/progenitor cells, Stem Cell Res. Ther., 2013, vol. 3, p. 152.Google Scholar
  77. 77.
    Ries, C., Egea, V., Karow, M., et al., MMP-2, MT1-MMP, and TIMP-2 are essential for the invasive capacity of human mesenchymal stem cells: differential regulation by inflammatory cytokines, Blood, 2007, vol. 109, p. 4055.CrossRefGoogle Scholar
  78. 78.
    Lee, J. H., Yoon, Y.M., and Lee, S.H., Hypoxic preconditioning promotes the bioactivities of mesenchymal stem cells via the HIF-1α-GRP78-Akt axis, Int. J. Mol. Sci., 2017, vol. 18, no. 6, p. 1320.CrossRefGoogle Scholar
  79. 79.
    Lund, A.W., Stegemann, J.P., and Plopper, G.E., Inhibition of ERK promotes collagen gel compaction and fibrillogenesis to amplify the osteogenesis of human mesenchymal stem cells in three-dimensional collagen I culture, Stem Cells Dev., 2009, vol. 18, p. 331.CrossRefGoogle Scholar
  80. 80.
    Udartseva, O.O., Lobanova, M.V., Andreeva, E.R., et al., Acute hypoxic stress affects migration machinery of tissue O2-adapted adipose stromal cells, Stem Cells Int., 2016, vol. 2016, p. 7260562.CrossRefGoogle Scholar
  81. 81.
    Schodel, J., Grampp, S., Maher, E.R., et al., Hypoxia, hypoxia-inducible transcription factors, and renal cancer, Eur. Urol., 2016, vol. 69, no. 4, p. 646.CrossRefGoogle Scholar
  82. 82.
    Rakian, R., Block, T.J., Johnson, S.M., et al., Native extracellular matrix preserves mesenchymal stem cell “stemness” and differentiation potential under serum-free culture conditions, Stem Cell Res. Ther., 2015, vol. 6, p. 235.CrossRefGoogle Scholar
  83. 83.
    Marinkovic, M., Block, T.J., Rakian, R., et al., One size does not fit all: developing a cell-specific niche for in vitro study of cell behavior, Matrix Biol., 2016, vols. 52–54, p. 426.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  1. 1.Institute of Biomedical Problems, Russian Academy of SciencesMoscowRussia

Personalised recommendations