Placental hypoxia developed during preeclampsia induces telocytes apoptosis in chorionic villi affecting the maternal-fetus metabolic exchange

Current Stem Cell Research and Therapy

Volumn 11, Issue 5, 2016, Pages 420-425

  Becerra, Cleofina Bosco ^a   Guerra, Eugenia Díaz ^a   Rojas, Rodrigo Gutierrez ^a   Montero, Jaime González ^a   Cordero, Mauro Parra ^b   Salinas, Ramón Rodrigo ^a   Yañez, Pilar Barja ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b HOSPITAL CLÍNICO UNIVERSIDAD DE CHILE   (Chile)

Author keywords

ADAMTS 13; Apoptosis; Nitrosative stress; Placenta; Telocytes

Indexed keywords

PEROXYNITRITE; REACTIVE OXYGEN METABOLITE; VON WILLEBRAND FACTOR CLEAVING PROTEINASE;

APOPTOSIS; ARTICLE; BLOOD VESSEL TONE; CHORION VILLUS; ENDOTHELIAL DYSFUNCTION; FEMALE; HUMAN; NITROSATIVE STRESS; OXIDATIVE STRESS; PLACENTA; PLACENTA CIRCULATION; PLACENTA DISORDER; PLACENTA FUNCTION; PLACENTAL HYPOXIA; PREECLAMPSIA; PRIORITY JOURNAL; TELOCYTE; ANIMAL; FETOMATERNAL TRANSFUSION; HYPOXIA; PATHOLOGY; PREGNANCY;

ANIMALS; APOPTOSIS; CHORIONIC VILLI; FEMALE; HUMANS; HYPOXIA; MATERNAL-FETAL EXCHANGE; PRE-ECLAMPSIA; PREGNANCY; TELOCYTES;

EID: 84974662275     PISSN: 1574888X     EISSN: None     Source Type: Journal    
DOI: 10.2174/1574888x10666150202144855     Document Type: Article

References (76)

1. Popescu LM, Faussone-Pellegrini MS. TELOCYTES-a case of serendipity: the winding way from Interstitial Cells of Cajal (ICC), via Interstitial Cajal-Like Cells (ICLC) to TELOCYTES. J Cell Mol Med 2010; 14: 729-40.
2. Suciu L, Popescu LM, Gherghiceanu M. Human placenta: de visu demonstration of interstitial Cajal-like cells. J Cell Mol Med 2007; 11: 590-7.
3. Suciu L, Popescu LM, Gherghiceanu M, et al. Telocytes in human term placenta: morphology and phenotype. Cells Tissues Organs 2010; 192: 325-39.
4. Redman CWC. Current topic: pre-eclampsia and the placenta. Placenta 1991; 112: 301-8.
5. Maynard S, Epstein FH, Karumanchi SA. Preeclampsia and angiogenic imbalance. Annu Rev Med 2008; 59: 61-78.
6. Roberts JM, Cooper DW. Pathogenesis and genetics of preeclampsia. Lancet 2001; 357: 53-6.
7. Meiss PJ, Goldenberg RL, Mercer BM, et al. The preterm prediction study: risk factor for indicated preterm births. Am J Obstet Gynecol 1998; 178: 562-7.
8. Many A, Hubel CA, Fisher SJ, et al. Invasive cytotrophoblasts manifest evidence of oxidative stress in preeclampsia. Am J Pathol 2000; 156: 321-31.
9. Khalil RA, Granger JP. Vascular mechanisms of increased arterial pressure in preeclampsia: lessons from animal models. Am J Physiol Regul Integr Comp Physiol 2002; 283: R29-45.
10. Myatt L, Kossenjans W, Sahay R, et al. Oxidative stress causes vascular dysfunction in the placenta. J Matern Fetal Med 2000; 9: 79-82.
11. Bosco C, Parra M, Barja P, et al. Increased immunohistochemical expression of thrombomodulin at placental perivascular myofibroblast in severe preeclampsia (PE). Histol Histopathol 2005; 4: 1045-55.
12. Nicolescu MI, Bucur A, Dinca O, et al. Telocytes in parotid glands. Anat Rec (Hoboken). 2012; 295: 378-85.
13. Kostin S. Myocardial telocytes: a specific new cellular entity. J Cell Mol Med 2010; 14: 1917-21.
14. Zhou J, Wang Y, Zhu P, et al. Distribution and characteristics of telocytes as nurse cells in the architectural organization of engineered heart tissues. Sci China Life Sci 2014; 57: 241-7.
15. Nicolescu MI, Popescu LM. Telocytes in the interstitium of human exocrine pancreas: ultrastructural evidence. Pancreas 2012; 41: 949-56.
16. Bosco C, Díaz E, Gutiérrez R, et al. Ganglionar nervous cells and telocytes in the pancreas of Octodon degus. Auton Neurosci Basic and Clinical 2013; 177: 224-30.
17. Wang XY, Diamant NE, Huizinga JD. Interstitial cells of Cajal: pacemaker cells of the pancreatic duct? Pancreas 2011; 40: 137-43.
18. Graf R, Langer JU, Schonfelder G, et al. The extravascular contractile system in the human placenta. Morphological and immunocytochemical investigations. Anat Embryol (Berl) 1994; 190: 541-8.
19. Kohnen G, Kertschanska S, Demir R, et al. Placental villous stroma as a model system for myofibroblast differentiation. Histochem Cell Biol 1996; 105: 415-29.
20. Bosco C, Díaz E. Placental hypoxia and foetal development versus alcohol exposure in pregnancy. Alcohol Alcohol 2012; 47: 109-17.
21. Rosso P. Placental growth, development, and function in relation to maternal nutrition. Fed Proc 1980; 39: 250-4.
22. Bosco C. Alcohol and xenobiotics in placenta damage. In: Preedy VR, Watson RR, editors. Comprehensive handbook of alcohol related pathology, Vol. 2. London: Elsevier Science Press 2005. pp 921-35.
23. Bosco C. The cytotrophoblast: the first human amine precursor uptake and decarboxylation (APUD) cell. Med Sci Res 1995; 23: 205-7.
24. Castellucci M, Scheper M, Scheffen I, et al. The development of the human placental villous tree. Anat Embryol (Berl) 1990; 181(2): 117-28.
25. Farley AE, Graham CH, Smith GN. Contractile properties of human placental anchoring villi. Am J Physiol Regul Integr Comp Physiol 2004; 287: 680-5.
26. Bosco C, Díaz E, Gutiérrez R, et al. A putative role for telocytes in placental barrier impairment during preeclampsia. Med Hypotheses 2015; 84: 72-7.
27. Sanders KM, Koh SD, Ward SM. Interstitial cells of Cajal as pacemakers in the gastrointestinal tract. Annu Rev Physiol 2006; 68: 307-43.
28. Rodrigo R, Parra M, Bosco C, et al. Pathophysiological basis for the prophylaxis of preeclampsia through early supplementation with antioxidant vitamins. Pharmacol Ther 2005; 107: 177-197.
29. Bowen RS, Moodley J, Dutton MF, Theron AJ. Oxidative stress in pre-eclampsia. Acta Obstet Gynecol Scand 2001; 80: 719-25.
30. Rodrigo R, Guichard C, Charles R. Clinical pharmacology and therapeutic use of antioxidant vitamins. Fundam Clin Pharmacol 2007; 21: 111-27.
31. Serdar Z, Gür E, Develioglu O, et al. Placental and decidual lipid peroxidation and antioxidant defenses in preeclampsia. Lipid peroxidation in preeclampsia. Pathophysiology 2002; 9: 21-25.
32. Liochev SI, Fridovich I. How does superoxide dismutase protect against tumor necrosis factor: a hypothesis informed by effect of superoxide on "free" iron. Free Radic Biol Med 1997; 23: 668-671.
33. Myatt L, Cui X. Oxidative stress in the placenta. Histochem Cell Biol 2004; 122: 369-382.
34. Walsh SW, Vaughan JE, Wang Y, et al. Placental isoprostane is significantly increased in preeclampsia. FASEB J 2000; 14: 1289-96.
35. Bosco C, Buffet C, Díaz E, Rodrigo R, Morales P, Barja P, Terra R, Parra-Cordero M. VEGF in the muscular layer of placental blood vessels: immuno-expression in preeclampsia and intrauterine growth restriction and its association with the antioxidant status. Cardiovasc Hematol Agents Med Chem 2010; 8: 87-95.
36. Qanungo S, Mukherjea M. Ontogenic profile of some antioxidants and lipid peroxidation in human placental and fetal tissues. Mol Cell Biochem 2000; 215: 11-9.
37. Jones ML, Mark PJ, Lewis JL, et al. Antioxidant defenses in the rat placenta in late gestation: increased labyrinthine expression of superoxide dismutases, glutathione peroxidase 3, and uncoupling protein 2. Biol Reprod 2010; 83: 254-60.
38. Das B, Saha-Roy S, Das Gupta A, et al. Assessment of placental oxidative stress in pre-eclampsia. J Obstet Gynaecol India 2012; 62: 39-42.
39. Roberts JM, Hubel CA. Is oxidative stress the link in the two-stage model of pre-eclampsia? Lancet 1999; 354: 788-9.
40. Moretti M, Phillips M, Abouzeid A, et al. Increased breath markers of oxidative stress in normal pregnancy and in preeclampsia. Am J Obstet Gynecol 2004; 190: 1184-90.
41. Bosco C, González J, Gutiérrez R, et al. Oxidative damage to preeclamptic placenta: immunohistochemical expression of VEGF, nitrotyrosine residues and von Willebrand factor. J Matern Fetal Neonatal Med 2012; 25: 2339-45.
42. Myatt L. Review: Reactive oxygen and nitrogen species and functional adaptation of the placenta. Placenta 2010; 24: 66-9.
43. Var A, Yildirim Y, Onur E, et al. Endothelial dysfunction in preeclampsia. Increased homocysteine and decreased nitric oxide levels. Gynecol Obstet Invest 2003; 56: 221-4.
44. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996; 271: 1424-37.
45. Parra-Cordero M, Bosco C, González J, Gutiérrez R, Barja P, Rodrigo R. Immunohistochemical expression of von Willebrand factor in the preeclamptic placenta. J Mol Histol. 2011; 42: 459-65.
46. Bergmann F, Rotmensch S, Rosenzweig B, et al. The role of von Willebrand factor in pre-eclampsia. Thromb Haemost 1991; 66: 525-8.
47. Brenner B, Zwang E, Bronshtein M, et al. von Willebrand factor multimer patterns in pregnancy-induced hypertension. Thromb Haemost 1989; 62: 715-7.
48. Dong J, Moake J, Nolasco L, et al. ADAMTS-13 rapidly cleaves newly secreted ultralarge von Willebrand factor multimers on the endothelial surface under flowing conditions. Blood 2002; 100: 4033-9.
49. Li Y, Choi H, Zhou Z, et al. Covalent regulation of ULVWF string formation and elongation on endothelial cells under flow conditions. J Thromb Haemost 2008; 6: 1135-43
50. Furlan M. Proteolytic cleavage of von Willebrand factor by ADAMTS-13 prevents uninvited clumping of blood platelets. J Thromb Haemost 2004; 2: 1505-9.
51. López JA, Dong JF. Shear stress and the role of high molecular weight von Willebrand factor multimers in thrombus formation. Blood Coagul Fibrinolysis 2005; 16 Suppl 1: S11-6.
52. Joyce JM, Phernetton TM, Magness RR. Effect of uterine blood flow occlusion on shear stress-mediated nitric oxide production and endothelial nitric oxide synthase expression during ovine pregnancy. Biol Reprod 2002; 67: 320-6.
53. Lancellotti S, De Filippis V, Pozzi N, et al. Formation of methionine sulfoxide by peroxynitrite at position 1606 of von Willebrand factor inhibits its cleavage by ADAMTS-13: A new prothrombotic mechanism in diseases associated with oxidative stress. Free Radic Biol Med 2010: 48: 446-56.
54. Kanfer A, Bruch JF, Nguyen G, et al. Increased placental antibribrinolytic potential and fibrin deposits in pregnancy-induced hypertension and Preeclampsia. Lab Invest 1996; 74: 253-8.
55. Smith SC, Baker PN, Symonds EM. Placental apoptosis in normal human pregnancy. Am J Obstet Gynecol 1997; 177: 57-65.
56. Myatt L. Role of placenta in preeclampsia. Endocrine 2002; 19: 103-11.
57. Huppertz B, Kadyrov M, Kingdom JC. Apoptosis and its role in the trophoblast. Am J Obstet Gynecol 2006; 195: 29-39.
58. Allaire AD, Ballenger KA, Wells SR, et al. Placental apoptosis in preeclampsia. Obstet Gynecol 2000; 96: 271-6.
59. Aban M, Cinel L, Arslan M, et al. Expression of nuclear factorkappa β and placental apoptosis in pregnancies complicated with intrauterine growth restriction and preeclampsia: an immunohistochemical study. Tohoku J Exp Med 2004; 204: 195-202.
60. Heazell AE, Crocker IP. Live and let die-regulation of villous trophoblast apoptosis in normal and abnormal pregnancies. Placenta 2008; 29: 772-83.
61. Burton GJ, Jones CJ. Syncytial knots, sprouts, apoptosis, and trophoblast deportation from the human placenta. Taiwan J Obstet Gynecol 2009; 48: 28-37.
62. Huppertz B, Kingdom J, Caniggia I, et al. Hypoxia Favours Necrotic Versus Apoptotic Shedding of Placental Syncytiotrophoblast into the Maternal Circulation. Placenta 2003; 24: 181-90.
63. Huppertz B, Kingdom JC. Apoptosis in the trophoblast-role of apoptosis in placental morphogenesis. J Soc Gynecol Investig 2004; 11: 353-62.
64. Tjoa ML, Cindrova-Davies T, Spasic-Boskovic O, et al. Trophoblastic oxidative stress and the release of cell-free feto-placental DNA. Am J Pathol 2006; 169: 400-4.
65. Askelund KJ, Chamley LW. Trophoblast deportation part I: Review of the evidence demonstrating trophoblast shedding and deportation during human pregnancy. Placenta 2011; 32: 716-23.
66. Zhou Y, Damsky CH, Chiu K, et al. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblast. J Clin Invest 1993; 91: 950-60.
67. Ratts VS, Tao XJ, Webster CB, et al. Expression of BCL-2, BAX and BAK in the Trophoblast Layer of the Term Human Placenta: a Unique Model of Apoptosis within a Syncytium. Placenta 2000; 21: 361-6.
68. Farrugia G. Interstitial cells of Cajal in health and disease. Neurogastroenterol Motil 2008; 20: 54-63.
69. Gibbons SJ, De Giorgio R, Faussone Pellegrini MS, et al. Apoptotic cell death of human interstitial cells of Cajal. Neurogastroenterol Motil 2009; 21: 85-93.
70. Mei F, Guo S, He YT, et al. Apoptosis of interstitial cells of Cajal, smooth muscle cells, and enteric neurons induced by intestinal ischemia and reperfusion injury in adult guinea pigs. Virchows Arch 2009 454: 401-9.
71. Cobellis L, De Falco M, Torella M, et al. Modulation of Bax Expression in Physiological and Pathological Human Placentas Throughout Pregnancy. In vivo 2007; 21: 777-84.
72. Mendilcioglu I, Karaveli S, Erdogan G, et al. Apoptosis and expression of Bcl-2, Bax, p53, caspase-3, and Fas, Fas ligand in placentas complicated by preeclampsia. Clin Exp Obstet Gynecol 2011; 38: 38-42.
73. Kossenjans W, Eis A, Sahay R, et al. Role of peroxinitrite in altered fetal placental vascular reactivity in diabetes or preeclampsia. Am J Physiol Heart Circ Physiol 2000; 278: 311-9.
74. Martinez-Orgado J, Gonzalez, R, Alonso MJ, et al. Modulation of Bax Expression in Physiological and Pathological Human Placentas Throughout Pregnancy Impairment of fetal endotheliumdependent relaxation in a rat model of preeclampsia by chronic nitric oxide synthase inhibition. J Soc Gynecol Invest 2004; 11: 82-8.
75. Myatt L, Eis AL, Brockman DE, et al. Inducible (type II) nitric oxide synthase in human placental villous tissue of normotensive, pre-eclamptic and intrauterine growth-restricted pregnancies. Placenta 1997; 18: 261-8.
76. Choi JW, Im MW, Pai SH. Nitric oxide production increases during normal pregnancy and decreases in preeclampsia. Ann Clin Lab Sci 2002; 32: 257-63.