Fetal progenitor cells naturally transferred through pregnancy participate in inflammation and angiogenesis during wound healing

FASEB Journal

Volumn 26, Issue 1, 2012, Pages 149-157

  Nassar, Dany ^a,b   Droitcourt, Catherine ^a,b   Mathieu D'Argent, Emmanuelle ^a,b   Kim, Min Ji ^a,b   Khosrotehrani, Kiarash ^a,b,c   Aractingi, Selim ^a,b,d  

^a SORBONNE UNIVERSITÉ   (France)

^b INSERM   (France)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d HÔPITAL TENON   (France)

Author keywords

Microchimerism; Skin; VEGFa

Indexed keywords

BLEOMYCIN; CD11B ANTIGEN; CD34 ANTIGEN; CELL MARKER; MATRIGEL; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; CELL FATE; CELL MOTILITY; CELL TRANSFER; CIRCULATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; FETUS; FETUS CELL; FLOW CYTOMETRY; FLUORESCENCE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LEUKOCYTE; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN EXAMINATION; SKIN FIBROSIS; STEM CELL MOBILIZATION; WILD TYPE; WOUND HEALING;

ANIMALS; CHEMOTAXIS; CHIMERISM; EMBRYONIC STEM CELLS; FEMALE; GREEN FLUORESCENT PROTEINS; INFLAMMATION; MALE; MATERNAL-FETAL EXCHANGE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOVASCULARIZATION, PHYSIOLOGIC; PREGNANCY; SIGNAL TRANSDUCTION; SKIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

MUS;

EID: 84855400456     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-180695     Document Type: Article

References (33)

1. Bianchi, D. W., Zickwolf, G. K., Weil, G. J., Sylvester, S., and DeMaria, M. A. (1996) Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum. Proc. Natl. Acad. Sci. U. S. A. 93, 705-708 (Pubitemid 26041153)
2. Khosrotehrani, K., and Bianchi, D. W. (2005) Multi-lineage potential of fetal cells in maternal tissue: a legacy in reverse. J. Cell Sci. 118, 1559-1563 (Pubitemid 40691884)
3. O'Donoghue, K., Chan, J., de la Fuente, J., Kennea, N., Sandison, A., Anderson, J. R., Roberts, I. A., and Fisk, N. M. (2004) Microchimerism in female bone marrow and bone decades after fetal mesenchymal stem-cell trafficking in pregnancy. Lancet 364, 179-182 (Pubitemid 38891690)
4. Khosrotehrani, K., Johnson, K. L., Cha, D. H., Salomon, R. N., and Bianchi, D. W. (2004) Transfer of fetal cells with multilineage potential to maternal tissue. JAMA 292, 75-80 (Pubitemid 38923796)
5. Wang, Y., Iwatani, H., Ito, T., Horimoto, N., Yamato, M., Matsui, I., Imai, E., and Hori, M. (2004) Fetal cells in mother rats contribute to the remodeling of liver and kidney after injury. Biochem. Biophys. Res. Commun. 325, 961-967 (Pubitemid 39487965)
6. Tan, X. W., Liao, H., Sun, L., Okabe, M., Xiao, Z. C., and Dawe, G. S. (2005) Fetal microchimerism in the maternal mouse brain: a novel population of fetal progenitor or stem cells able to cross the blood-brain barrier? Stem Cells 23, 1443-1452 (Pubitemid 41740992)
7. Khosrotehrani, K., Leduc, M., Bachy, V., Nguyen Huu, S., Oster, M., Abbas, A., Uzan, S., and Aractingi, S. (2008) Pregnancy allows the transfer and differentiation of fetal lymphoid progenitors into functional T and B cells in mothers. J. Immunol. 180, 889-897
8. Nguyen Huu, S., Oster, M., Uzan, S., Chareyre, F., Aractingi, S., and Khosrotehrani, K. (2007) Maternal neoangiogenesis during pregnancy partly derives from fetal endothelial progenitor cells. Proc. Natl. Acad. Sci. U. S. A. 104, 1871-1876 (Pubitemid 46239871)
9. Nguyen Huu, S., Oster, M., Avril, M. F., Boitier, F., Mortier, L., Richard, M. A., Kerob, D., Maubec, E., Souteyrand, P., Moguelet, P., Khosrotehrani, K., and Aractingi, S. (2009) Fetal microchimeric cells participate in tumour angiogenesis in melanomas occurring during pregnancy. Am. J. Pathol. 174, 630-637
10. Yoder, M. C. (2010) Is endothelium the origin of endothelial progenitor cells? Arterioscler. Thromb. Vasc. Biol. 30, 1094-1103
11. Purhonen, S., Palm, J., Rossi, D., Kaskenpaa, N., Rajantie, I., Yla-Herttuala, S., Alitalo, K., Weissman, I. L., and Salven, P. (2008) Bone marrow-derived circulating endothelial precursors do not contribute to vascular endothelium and are not needed for tumor growth. Proc. Natl. Acad. Sci. U. S. A. 105, 6620-6625 (Pubitemid 351754556)
12. Singer, A. J., and Clark, R. A. (1999) Cutaneous wound healing. N. Engl. J. Med. 341, 738-746 (Pubitemid 29407375)
13. Streit, M., Velasco, P., Riccardi, L., Spencer, L., Brown, L. F., Janes, L., Lange-Asschenfeldt, B., Yano, K., Hawighorst, T., Iruela-Arispe, L., and Detmar, M. (2000) Thrombospondin-1 suppresses wound healing and granulation tissue formation in the skin of transgenic mice. EMBO J. 19, 3272-3282 (Pubitemid 30428205)
14. Fathke, C., Wilson, L., Hutter, J., Kapoor, V., Smith, A., Hocking, A., and Isik, F. (2004) Contribution of bone marrow-derived cells to skin: collagen deposition and wound repair. Stem Cells 22, 812-822 (Pubitemid 39166938)
15. Wu, Y., Chen, L., Scott, P. G., and Tredget, E. E. (2007) Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells 25, 2648-2659 (Pubitemid 47582758)
16. Sasaki, M., Abe, R., Fujita, Y., Ando, S., Inokuma, D., and Shimizu, H. (2008) Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type. J. Immunol. 180, 2581-2587
17. Tepper, O. M., Carr, J., Allen, R. J., Jr., Chang, C. C., Lin, C. D., Tanaka, R., Gupta, S. M., Levine, J. P., Saadeh, P. B., and Warren, S. M. (2010) Decreased circulating progenitor cell number and failed mechanisms of stromal cell-derived factor-1alpha mediated bone marrow mobilization impair diabetic tissue repair. Diabetes 59, 1974-1983
18. Awad, O., Jiao, C., Ma, N., Dunnwald, M., and Schatteman, G. C. (2005) Obese diabetic mouse environment differentially affects primitive and monocytic endothelial cell progenitors. Stem Cells 23, 575-583 (Pubitemid 40478496)
19. Yamamoto, T., Takagawa, S., Katayama, I., Yamazaki, K., Hamazaki, Y., Shinkai, H., and Nishioka, K. (1999) Animal model of sclerotic skin. I: Local injections of bleomycin induce sclerotic skin mimicking scleroderma. J. Invest. Dermatol. 112, 456-462 (Pubitemid 29171935)
20. Khosrotehrani, K., Wataganara, T., Bianchi, D. W., and Johnson, K. L. (2004) Fetal cell-free DNA circulates in the plasma of pregnant mice: relevance for animal models of fetomaternal trafficking. Hum. Reprod. 19, 2460-2464 (Pubitemid 39481268)
21. Khosrotehrani, K., Johnson, K. L., Guegan, S., Stroh, H., and Bianchi, D. W. (2005) Natural history of fetal cell microchimerism during and following murine pregnancy. J. Reprod. Immunol. 66, 1-12 (Pubitemid 40798123)
22. Pitchford, S. C., Furze, R. C., Jones, C. P., Wengner, A. M., and Rankin, S. M. (2009) Differential mobilization of subsets of progenitor cells from the bone marrow. Cell Stem Cell 4, 62-72
23. Goolsby, J., Marty, M. C., Heletz, D., Chiappelli, J., Tashko, G., Yarnell, D., Fishman, P. S., Dhib-Jalbut, S., Bever, C. T., Jr., Pessac, B., and Trisler, D. (2003) Hematopoietic progenitors express neural genes. Proc. Natl. Acad. Sci. U. S. A. 100, 14926-14931 (Pubitemid 37517993)
24. Parant, O., Dubernard, G., Challier, J. C., Oster, M., Uzan, S., Aractingi, S., and Khosrotehrani, K. (2009) CD34+ cells in maternal placental blood are mainly fetal in origin and express endothelial markers. Lab. Invest. 89, 915-923
25. Khosrotehrani, K., Reyes, R. R., Johnson, K. L., Freeman, R. B., Salomon, R. N., Peter, I., Stroh, H., Guegan, S., and Bianchi, D. W. (2007) Fetal cells participate over time in the response to specific types of murine maternal hepatic injury. Hum. Reprod. 22, 654-661
26. Schmeisser, A., Garlichs, C. D., Zhang, H., Eskafi, S., Graffy, C., Ludwig, J., Strasser, R. H., and Daniel, W. G. (2001) Monocytes coexpress endothelial and macrophagocytic lineage markers and form cord-like structures in Matrigel under angiogenic conditions. Cardiovasc. Res. 49, 671-680 (Pubitemid 32146430)
27. Hristov, M., Schmitz, S., Schuhmann, C., Leyendecker, T., von Hundelshausen, P., Krotz, F., Sohn, H. Y., Nauwelaers, F. A., and Weber, C. (2009) An optimized flow cytometry protocol for analysis of angiogenic monocytes and endothelial progenitor cells in peripheral blood. Cytometry A 75, 848-853
28. Hirschi, K. K., Ingram, D. A., and Yoder, M. C. (2008) Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler. Thromb. Vasc. Biol. 28, 1584-1595
29. Hildbrand, P., Cirulli, V., Prinsen, R. C., Smith, K. A., Torbett, B. E., Salomon, D. R., and Crisa, L. (2004) The role of angiopoietins in the development of endothelial cells from cord blood CD34+ progenitors. Blood 104, 2010-2019 (Pubitemid 39297851)
30. Asahara, T., Masuda, H., Takahashi, T., Kalka, C., Pastore, C., Silver, M., Kearne, M., Magner, M., and Isner, J. M. (1999) Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ. Res. 85, 221-228 (Pubitemid 29377293)
31. Galiano, R. D., Tepper, O. M., Pelo, C. R., Bhatt, K. A., Callaghan, M., Bastidas, N., Bunting, S., Steinmetz, H. G., and Gurtner, G. C. (2004) Topical vascular endothelial growth factor accelerates diabetic wound healing through increased angiogenesis and by mobilizing and recruiting bone marrow-derived cells. Am. J. Pathol. 164, 1935-1947 (Pubitemid 38669343)
32. Ishida, Y., Gao, J. L., and Murphy, P. M. (2008) Chemokine receptor CX3CR1 mediates skin wound healing by promoting macrophage and fibroblast accumulation and function. J. Immunol. 180, 569-579
33. Droitcourt, C., Khosrotehrani, K., Girot, R., and Aractingi, S. (2008) Healing of sickle cell ulcers during pregnancy: a favourable effect of foetal cell transfer? J. Eur. Acad. Dermatol. Venereol. 22, 1256-1257