Can Perisinusoids! Cells Be Regional Stem (Progenitor) Cells of the Liver?



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Abstract

Regenerative medicine is one of quickly developing and promising areas of medicine in which there is essentially new approach to restoration of damaged organs by stimulation and Cor) use of stem (progenitor) cells for acceleration of regeneration. To realize this approach, it is necessary to know: what are stem cells? What are regional stem cells? What are their phenotype and potencies? Stem cells are already identified for a number of organs and tissues (epidermis, skeletal muscle) and their niche is determined. However liver, the organ whose regenerative abilities are known since antique times, has not opened its main secret yet - the secret of a regional stem cell. In this review on the basis of our own and literature data we discuss our hypothesis that perisinusoidal stellate liver cells can be liver stem cells.

About the authors

A A Gumerova

The Department of Normal Human Anatomy, the Kazan State Medical University

The Department of Normal Human Anatomy, the Kazan State Medical University

A P Kiyasov

The Department of Normal Human Anatomy, the Kazan State Medical University

The Department of Normal Human Anatomy, the Kazan State Medical University

References

  1. Wake К. «Sternzellen» in the liver: perisinusoidal cells with special reference to storage of vitamin A. Am. J. Anat. 1971; 132(4): 42Э-Б2.
  2. McGee J.O., Patrick R.S. The role of perisinusoidal cells in hepatic fibrogenesis. An electron microscopic study of acute carbon tetrachloride liver injury. Lab. Invest. 1972; 264: 429-40.
  3. Pinzani M., Failli P., Ruocco С et al. Fat-storing cells as liver-specific pericytes. Spatial dynamics of agonist-stimulated intracellular calcium transients. J. Clin. Invest. 1992; 90: Б42-4В.
  4. Wake K., Sato T. Intralobular heterogeneity of perisinusoidal stellate cells in porcine liver. Cell Tissue Res. 1993; 273: 227-37.
  5. Yokoi Y., NamihisaT., Kuroda H. et al. Immunocytochemical detection of desmin in fat-storing cells [Ito cells]. Hepatology 1984; 4: 709-14.
  6. Geerts A. History, heterogeneity, developmental biology, functions of quiescent hepatic stellate cells. Semin. Liver Dis. 2001; 21: 311-35.
  7. Burt A.D. Cellular and molecular aspects of hepatic fibrosis. J. Pathol. 1993; 170(2]: 105-14.
  8. B. Burt A.D., Le Bail В., Balabaud C, Bioulac-Sage P. Morphologic investigation of sinusoidal cells. Semin. Liver Dis. 1993; 13(1]: 21-38.
  9. Friedman S.L. Molecular regulation of hepatic fibrosis, an integrated cellular response to tissue injury. J. Biol. Chem. 2000; 275: 2247-50.
  10. Ramadori G., Veit Т., Schwogler S. et al. Expression of the gene of the alpha-smooth muscle-actin isoform in rat liver and in rat fat-storing (ITO] cells. Virchows Arch. B. Cell Pathol. Incl. Mol. Pathol. 1990; 59: 349-57.
  11. Kim Т.Н., Mars W.M., Stolz D.B. et al. Extracellular matrix remodeling at the early stages of liver regeneration in the rat. Hepatology 1997; 2B: 896-904.
  12. Friedman S.L. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol. Rev. 2008; 88: 125-72.
  13. Schirmacher P., Geerts A., Pietrangelo A. etal. Hepatocyte growth factor/hepatopoietin A is expressed in fat-storing cells from rat liver but not myofibroblast-like cells derived from fat-storing cells. Hepatology 1992; 15:5-11.
  14. Maher J.J. Cell-specific expression of hepatocyte growth factor in liver. Upregulation in sinusoidal endothelial cells after carbon tetrachloride. J. Clin. Invest. 1993; 91: 2244-52.
  15. Gohda E., Tsubouchi H., Nakayama H. et al. Human hepatocyte growth factor in plasma from patients with fulminant hepatic failure. Exp. Cell Res. 1986; 16Б: 139-50.
  16. Gohda E., Tsubouchi H., Nakayama H. et al. Purification and partial characterization of hepatocyte growth factor from plasma of a patient with fulminant hepatic failure. J. Clin. Invest. 1988; 81: 414-9.
  17. Weidner K.M., Arakaki N., Hartmann G. et al. Evidence for the identity of human scatter factor and human hepatocyte growth factor. PNAS USA 1991; 88: 7001-5.
  18. Birchmeier C, Gherardi E. Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol. 1998; 8: 404-10.
  19. Birchmeier C, Birchmeier W., Gherardi E., Vande Woude G.F. Met, metastasis, motility and more. Nat. Rev. Mol. Cell Biol. 2003; 4: 915-25.
  20. Bladt F., Riethmacher D., Isenmann S. et al. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 1995; 376: 7Б8-71.
  21. Schmidt С, Bladt F., Goedecke S. et al. Scatter factor/hepatocyte growth factor is essential for liver development. Nature 1995; 373: 699-702.
  22. Fujio K., Evarts R.P., Hu Z. et al. Expression of stem cell factor and its receptor, c-kit, during liver regeneration from putative stem cells in adult rat. Lab. Invest. 1994; 70: 511-6.
  23. Meyer D.H., Bachem M.G., Gressner A.M. Modulation of hepatic lipocyte proteoglycan synthesis and proliferation by Kupffer cell-derived transforming growth factors type beta 1 and type alpha. Biochem. Biophys. Res. Commun. 1990; 171: 1122-9.
  24. Bachem M.G., Meyer D., Melchior R. et al. Activation of rat liver perisinusoidal lipocytes by transforming growth factors derived from myofibroblast-like cells. A potential mechanism of self perpetuation in liver fibrogenesis. J. Clin. Invest. 1992; 89: 19-27.
  25. Mullhaupt В., Feren A., Fodor E., Jones A. Liver expression of epidermal growth factor RNA. Rapid increases in immediate-early phase of liver regeneration. J. Biol. Chem. 1994; 269: 19667-70.
  26. Yoshino R., Miura K., Segawa D. et al. Epimorphin expression and stellate cell status in mouse liver injury. Hepatol. Res. 2006; 34:238-49.
  27. Asahina K., Sato H., Yamasaki С et al. Pleiotrophin/heparin-binding growth-associated molecule as a mitogen of rat hepatocytes and its role in regeneration and development of liver. Am. J. Pathol. 2002; 160: 2191-205.
  28. Nagai H., Terada K., Watanabe G. et al. Differentiation of liver epithelial [stem-like] cells into hepatocytes induced by coculture with hepatic stellate cells. Biochem. Biophys. Res. Commun. 2002; 293(5): 1420-5.
  29. Hoppo Т., Fujii H., Hirose T. et al. Thy1-positive mesenchymal cells promote the maturation of CD49f-positive hepatic progenitor cells in the mouse fetal liver. Hepatology 2004; 39: 1362-70.
  30. Vassy J., Rigaut J.P., Briane D., Kraemer M. Confocal microscopy immunofluorescence localization of desmin and other intermediate filament proteins in fetal rat livers. Hepatology 1993; 17: 293-300.
  31. Kiassov A.P., Van Eyken P., van Pelt J.F. et al. Desmin expressing nonhematopoietic liver cells during rat liver development: an immunohistochemical and morphometric study. Differentiation 1995; 59: 253-8.
  32. Киясов А.П., Гумерова А.А., Билалов M.M. Экспрессия цитокератинов в пре- и постнатальном онтогенезе. Онтогенез 1997; 28(5): 389-93.
  33. Гумерова А.А., Киясов А.П., Калигин М.С. и др. Участие клеток Ито в гистогенезе и регенерации печени. Клеточная трансплантология и тканевая инженерия 2007; 2(4): 39-46.
  34. Maxwell Р.Н., Ferguson D.J., Osmond М.К. et al. Expression of a homologously recombined erythopoietin-SV40 T antigen fusion gene in mouse liver: evidence for erythropoietin production by Ito cells. Blood 1994; 84(6): 1823-30.
  35. Eckardt K.U. Erythropoietin production in liver and kidneys. Curr. Opin. Nephrol. Hypertens. 1996; 5(1): 28-34.
  36. Passino M.A., Adams R.A., Sikorski S.L., Akassoglou K. Regulation of hepatic stellate cell differentiation by the neurotrophin receptor p75NTR. Science 2007; 315: 1853-56.
  37. Kubota H., Yao H., Reid L.M. Identification and characterization of vitamin A-storing cells in fetal liver: implications for functional importance of hepatic stellate cells in liver development and hematopoiesis. Stem Cells 2007; 25: 2339-49.
  38. Miyake K., Medina K., Ishihara K. et al. A VCAM-like adhesion molecule on murine bone marrow stromal cells mediates binding of lymphocyte precursors in culture. J. Cell Biol. 1991; 114: 557-65.
  39. Wright D.E., Bowman E.P., Wagers A.J. et al. Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J. Exp. Med. 2002; 195: 1145-54.
  40. Lints T.J., Hartley L., Parsons L.M. et al. Mesoderm-specific expression of the divergent homeobox gene Hlx during murine embryogenesis. Dev. Dyn. 1996; 205: 457-70.
  41. Tocci A., Parolini I., Gabbianelli M. et al. Dual action of retinoic acid on human embryonic/fetal hematopoiesis: blockade of primitive progenitor proliferation and shift from multipotent/erythroid/monocytic to granulocytic differentiation program. Blood 1996; 88(8): 2878-88.
  42. Evarts R.P., Hu Z., Omori N. et al. Effect of vitamin A deficiency on the integrity of hepatocytes after partial hepatectomy. Am. J. Pathol. 1995; 147(3): 699-706.
  43. Deng X., Chen Y.-X., Zhang J.-P. et al. Hepatic stellate cells modulate the differentiate of bone marrow mesenchymal stem cells into hepatocyte-like cells. J. Cell. Physiol. 2008; 217: 138-44.
  44. Nitou M., Ishikawa K., Shiojiri N. Immunohistochemical analisys of development of desmin-positive hepatic stellate cells in mouse liver. J. Anat. 2000; 197: 635-46.
  45. Knittel Т., Kobold D., Saile B. et al. Rat myofibroblasts and hepatic stellate cells: different cell population of the fibroblast lineage with fibrogenic potential. Gastroenterol. 1999; 117: 1205-21.
  46. Sicklick J.K., Choi S.S., Bustamante M. et al. Evidence for epithelial-mesenchymal transitions in adult liver cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2006; 291 [4]; G575-83.
  47. Jelnes P., Santoni-Rugiu E., Rasmussen M. et al. Remarkable heterogeneity displayed by oval cells in rat and mouse models of stem cell-mediated liver regeneration. Hepatology 2007; 45(6]; 1462-70.
  48. Li Y., Yang J., Dai С et al. Role for integrin-linked kinase in mediating tubular epithelial to mesenchymal transition and renal interstitia fibrogenesis. J. Clin. Invest. 2003; 112: 503-16.
  49. Киясов А.П., Гумерова А.А., Титова M.A. Мезенхимально-эпителиальная трансформация клеток Ито in vitro. Клеточные технологии в биологии и медицине 2006; 3:150-4.
  50. Низамов Р.С, Киясов А.П., Алимов И.М., Ахметшин Э.Ю., Орлова О.Е. Иммуногистохимическое изучение фенотипов клеток в органотипической культуре печени эмбрионов крыс. Цитология 2001; 43(1]: 68-75.
  51. Yang L., Jung Y., Omenetti A. et al. Fate-mapping evidence that hepatic stellate cells are epithelial progenitors in adult mouse livers. Stem Cells 2008; 26(8]; 2104-13.
  52. Wang P., Liu Т., Cong M. et al. Expression of extracellular matrix genes in cultured hepatic oval cells: an origin of hepatic stellate cells through transforming growth factor beta? Liver Int. 2009; 29(4): 575-84.
  53. Fausto N. Oval cells and liver carcinogenesis: an analysis of cell lineages in hepatic tumors using oncogene transfection techniques. Prog. Clin. Biol. Res. 1990; 331: 325-34.
  54. Sell S. Is there a liver stem cell? Cancer Res. 1990; 50: 3811-5.
  55. Sigal S.H., Brill S., Fiorino A.S., Reid L.M. The liver as a stem cell and lineage system. Am. J. Physiol. 1992; 263: G139-48.
  56. Waldmann J., Feldmann G., Slater E.P. et al. Expression of the zinc-finger transcription factor Snail in adrenocortical carcinoma is associated with decreased survival. Br. J. Cancer. 2008; 99(11): 1900-7.
  57. Schmitt-Graeff A., Jing R., Nitschke R. et al. Synemin expression is widespread in liver fibrosis and is induced in proliferating and malignant biliary epithelial cells. Hum. Pathol. 2006; 37: 1200-10.
  58. Petersen B.E., Bowen W.C., Patrene K.D. et al. Bone marrow as a potential source of hepatic oval cells. Science 1999; 284(54170: 1168-70.
  59. Theise N.D., Nimmakayalu M., Gardner R. et al. Liver from bone marrow in humans. Hepatology 2000; 32(1): 11-6.
  60. Theise N.D., Badve S., Saxena R. et al. Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 2000; 31(1): 235-40.
  61. Lagasse E., Connors H., Al-Dhalimy M. et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat. Med. 2000; 6(11): 1229-34.
  62. Fiegel H.C., Lioznov M.V., Cortes-Dericks L. et al. Liver-specific gene expression in cultured human hematopoietic stem cells. Stem Cells 2003; 21(1): 98-104.
  63. Zhan Y., Wang Y., Wei L. et al. Differentiation of hematopoietic stem cells into hepatocytes in liver fibrosis in rats. Transplant. Proc. 2006; 38(9): 3082-5.
  64. Sato Y., Araki H., Kato J. et al. Human mesenchymal stem cells xenografted directly to rat liver are differentiated into human hepatocytes without fusion. Blood 2005; 106(2): 756-63.
  65. Talens-Visconti R., Bonora A., Jover R. Et al. Hepatogenic differentiation of human mesenchymal stem cells from adipose tissue in comparison with bone marrow mesenchymal stem cells. World J. Gastroenterol. 2006; 12(36): 5834-45.
  66. Talens-Visconti R., Bonora A., Jover R. Et al. Human mesenchymal stem cells from adipose tissue: Differentiation into hepatic lineage. Toxicol. In Vitro. 2007; 21(2): 324-9.
  67. Lange C, Bruns H., Kluth D. et al. Hepatocytic differentiation of mesenchymal stem cells in cocultures with fetal liver cells. World J. Gastroenterol. 2006; 12(15): 2394-7.
  68. Киясов А.П., Исламов P.P., Ризванов А.А. и др. Клеточная терапия генетически модифицированными стволовыми клетками пуповинной крови трансгенных G93A мышей, экспрессирующих фенотип бокового амиотрофического склероза. Материалы итоговой конференции по результатам выполнения мероприятий за 2007 год в рамках приоритетного направления «Живые системы» ФЦП «Исследования и разработки по приоритетным направлениям развития научно-технологического комплекса России на 2007-2012 годы»; 2007 дек. 6-7; Москва, Россия; С. 65-6.
  69. Андреева Д.И., Калигин М.С, Йылмаз Т.С. и др. Роль генетически модифицированных стволовых клеток пуповинной крови человека в регенерации печени на модели частичной гепатэктомии у крыс. Материалы Всероссийской школы-конференции «Аутологичные стволовые и прогениторные клетки: экспериментальные и клинические достижения»; 2008 июнь 9-11; Москва, Россия; С. 26.
  70. McLin V.A., Zorn A.M. Molecular Control of Liver Development. Clin. Liver Dis. 2006; 10: 1-25.
  71. Baba S., Fujii H., Hirose T. et al. Commitment of bone marrow cells to hepatic stellate cells in mouse. J. Hepatol. 2004; 40(2): 255-60.
  72. Forbes S.J., Russo F.P., Rey V. et al. A significant proportion of myofibroblasts are of the bone marrow orogin in human liver fibrosis. Gastroenterol. 2004; 126: 955-63.
  73. Russo F.P., Alison M.R., Bigger B.W. et al. The bone marrow functionally contributes to the liver fibrosis. Gastroenterol. 2006; 130: 1807-21.
  74. Sakaida I., Terai S., Yamamoto N. et al. Transplantation of bone marrow cells reduces CCI4-induced liver fibrosis in mice. Hepatology 2004; 40: 1304-11.
  75. Han Y.P., Yan С, Zhou L. et al. A matrix metalloproteinase-9 activation cascade by hepatic stellate cells in transdifferentiation in the three-dimensional extracellular matrix. J. Biol. Chem. 2007; 282: 12928-39.
  76. Киясов А.П., Одинцова A.X., Гумерова А.А. и др. Трансплантация аутогенных гемопоэтических стволовых клеток больным хроническими гепатитами. Клеточная трансплантология и тканевая инженерия 2008; 3(11:70-5.
  77. Kisseleva Т., Uchinami Н., Feirt N. Et al. Bone marrow-derived fibrocytes participate in pathogenesis of liver fibrosis. J. Hepatol. 2006; 45(3): 429-38.
  78. Ramadori G., Saile B. Mesenchymal cells in the liver - one cell type or two? Liver 2002; 22: 283-94.
  79. Arthur M.J., Stanley A., Iredale J.P. et al. Secretion of 72 kDa type IV collagenase/gelatinase by cultured human lipocytes. Analysis of gene expression, protein synthesis and proteinase activity. Biochem. J. 1992; 287:701-7.
  80. Milani S., Herbst H., Schuppan D. et al. Differential expression of matrix-metalloproteinase-1 and -2 genes in normal and fibrotic human liver. Am. J. Pathol. 1994; 144: 528-37.
  81. Vyas S.K., Leyland H., Gentry J., Arthur M.J. Rat hepatic lipocytes synthesize and secrete transin (stromelysin] in early primary culture. Gastroenterol. 1995; 109: 889-98.
  82. Schaefer В., Rivas-Estilla A.M., Meraz-Cruz N. et al. Reciprocal modulation of matrix metalloproteinase-13 and type I collagen genes in rat hepatic stellate cells. Am. J. Pathol. 2003; 162: 1771-80.
  83. Hoppo Т., Fujii H., Hirose T. et al. Thy1-positive mesenchymal cells promote the maturation of CD49f-positive hepatic progenitor cells in the mouse fetal liver. Hepatology 2004; 39: 1362-70.
  84. Petersen B.E., Goff J.P., Greenberger J.S., Michalopoulos G.K. Hepatic oval cells express the hematopoietic stem cell marker Thy-1 in the rat. Hepatology 1998; 27: 433-45.
  85. Derzso K., Jelnes P., Laszlo V. Thy-1 is expresse in hepatic myofibroblasts and not oval cells in stem cell-mediated liver regeneration. Am. J. Pathol. 2007; 171(5): 1529-37.
  86. Kordes C, Sawitza I., Mbller-Marbach A. et al. CD133+ hepatic stellate cells are progenitor cells. Biochem. Biophys. Res. Commun. 2007; 352(2): 410-7.
  87. Kordes C., Sawitza I., Haussinger D. Canonical Wnt signaling maintains the dquiescent stage of hepatic stellate cells. Biochem. Biophys. Res. Commun. 2008; 367: 116-23.
  88. Hockenbery D.M., Zutter M., Hickey W. et al. Bcl-2 protein is topographically restricted in tissues characterized by apoptotic cell death. PNAS USA 1991; 88: 6961-5.
  89. Sawitza I., Kordes C, Hausinger D. The niche of stellate cells within rat liver. Hepatology 2009; 50.
  90. Fuchs E., Tumbar Т., Guasch G. Socializing with the neighbors: stem cells and their niche. Cell 2004; 116: 769-78.
  91. Ага Т., Tokoyoda K., Sugiyama T. et al. Long-term hematopoietic stem cells require stromal cell-deriver factor-1 colonizing bone marrow during ontogeny. Immunity. 2003; 19: 257-67.
  92. Aiuti A., Webb I.J., Bleul С et al. The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J. Exp. Med. 1997; 185(1): 111-20.
  93. Katayama Y., Battista M., Kao W.-M. et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from the bone marrow. Cell 2006; 124: 407-21.
  94. Ueno Т., Inuzuka S., Torimura T. et al. Intrinsic innervation of the human liver. J. Clin. Electorn. Microsc. 1988; 21: 481-91.
  95. Bioulac-Sage P., Lafon M.E., Saric J., Balabaud С Nerves and perisinusoidal cells in human liver. J. Hepatol. 1990; 10: 105-12.
  96. Vom Dahl S., Bode J.G., Reinehr R. et al. Release of osmolytes from perfused rat liver on perivascular nerve stimulation: alpha-adrenergic control of osmolyte efflux from parenchymal and nonparenchymal liver cells. Hepatology 1999; 1: 195-204.
  97. Athary A., Hanecke K., Jungermann K. Prostaglandin F2a and D2 release from primary Ito cell cultures after stimulation with noradrenaline and ATP but not adenosine. Hepatology 1994. 20: 142-8.
  98. ReyaT., Duncan A.W., Ailes I. et al. A role for WNT signaling in self-reneval of haemotopoietic stem cell. Nature 2003; 423: 409-14.
  99. Nyfeler Y., Kirch R.D., Mantei N. et al. Jaggedl signals in the postnatal subventricular zone are required for neural stem cell self-renewal. EMBO J. 2005; 24: 3504-15.
  100. Mauro A. Satellite cell of the skeletal muscle fibers. J. Biophys. Biochem. Cytol. 1961; 9: 493-5.
  101. Oakberg E.F. Spermatogonia! stem-cell renewal in the mouse. Anat. Rec. 1971; 169: 515-31.
  102. Watt F.M., Hogan B.L. Out of Eden: stem cells and their niches. Science 2000; 287: 1427-30.
  103. Michalopoulos G.K., DeFrances M.C. Liver regeneration. Science 1997; 276: 60-6.

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