Fetal microchimeric cells participate in tumour angiogenesis in melanomas occurring during pregnancy

American Journal of Pathology

Volumn 174, Issue 2, 2009, Pages 630-637

  Sau, Nguyen Huu ^a,b   Oster, Michèle ^a,b   Avril, Marie Françoise ^c   Boitier, Françoise ^c   Mortier, Laurent ^d   Richard, Marie Aleth ^e   Kerob, Delphine ^f   Maubec, Eve ^g   Souteyrand, Pierre ^h   Moguelet, Philippe ⁱ   Khosrotehrani, Kiarash ^a,b,i   Aractingi, Selim ^a,b,i  

^a SORBONNE UNIVERSITÉ   (France)

^b CENTRE DE RECHERCHE SAINT ANTOINE   (France)

^c Paris Descartes University   (France)

^d LILLE UNIVERSITY HOSPITAL   (France)

^e ASSISTANCE PUBLIQUE HÔPITAUX DE MARSEILLE   (France)

^f SAINT LOUIS HOSPITAL   (France)

^g BICHAT HOSPITAL   (France)

^h UNIVERSITÉ CLERMONT AUVERGNE   (France)

ⁱ HÔPITAL TENON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD31 ANTIGEN; CD34 ANTIGEN; LYVE 1 ANTIGEN; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CARCINOGENESIS; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FETUS CELL; GESTATION PERIOD; HUMAN; HUMAN TISSUE; LYMPHANGIOGENESIS; MELANOMA; MELANOMA B16; MICROCHIMERISM; MOUSE; NEVUS; NONHUMAN; PHENOTYPE; PREGNANCY; PRIORITY JOURNAL;

EID: 59649094835     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.080566     Document Type: Article

References (41)

1. Dillman RO, Vandermolen LA, Barth NM, Bransford KJ: Malignant melanoma and pregnancy ten questions. West J Med 1996, 164:156-161
2. Wong JH, Sterns EE, Kopald KH, Nizze JA, Morton DL: Prognostic significance of pregnancy in stage I melanoma. Arch Surg 1989, 124:1227-1230
3. Lishner M: Cancer in pregnancy. Ann Oncol 2003, 14(Suppl 3):iii31-iii36
4. Krabchi K, Gros-Louis F, Yan J, Bronsard M, Masse J, Forest JC, Drouin R: Quantification of all fetal nucleated cells in maternal blood between the 18th and 22nd weeks of pregnancy using molecular cytogenetic techniques. Clin Genet 2001, 60:145-150
5. Ariga H, Ohto H, Busch MP, Imamura S, Watson R, Reed W, Lee TH: Kinetics of fetal cellular and cell-free DNA in the maternal circulation during and after pregnancy: implications for noninvasive prenatal diagnosis. Transfusion 2001, 41:1524-1530
6. Bianchi DW, Zickwolf GK, Weil GJ, Sylvester S, DeMaria MA: Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum. Proc Natl Acad Sci USA 1996, 93:705-708
7. Artlett CM, Cox LA, Ramos RC, Dennis TN, Fortunato RA, Hummers LK, Jimenez SA, Smith JB: Increased microchimeric CD4+ T lymphocytes in peripheral blood from women with systemic sclerosis. Clin Immunol 2002, 103:303-308
8. O'Donoghue K, Chan J, De La Fuente J, Kennea N, Sandison A, Anderson JR, Roberts IA, Fisk NM: Microchimerism in female bone marrow and bone decades after fetal mesenchymal stem-cell trafficking in pregnancy. Lancet 2004, 364:179-182
9. Johnson KL, Samura O, Nelson JL, McDonnell M, Bianchi DW: Significant fetal cell microchimerism in a nontransfused woman with hepatitis C: evidence of long-term survival and expansion. Hepatology 2002, 36:1295-1297
10. Khosrotehrani K, Johnson KL, Cha DH, Salomon RN, Bianchi DW: Transfer of fetal cells with multilineage potential to maternal tissue. JAMA 2004, 292:75-80
11. Srivatsa B, Srivatsa S, Johnson KL, Samura O, Lee SL, Bianchi DW: Microchimerism of presumed fetal origin in thyroid specimens from women: a case-control study. Lancet 2001, 358:2034-2038
12. Khosrotehrani K, Reyes RR, Johnson KL, Freeman RB, Salomon RN, Peter I, Stroh H, Guegan S, Bianchi DW: Fetal cells participate over time in the response to specific types of murine maternal hepatic injury. Hum Reprod 2007, 22:654-661
13. Khosrotehrani K, Leduc M, Bachy V, Nguyen HS, Oster M, Abbas A, Uzan S, Aractingi S: Pregnancy allows the transfer and differentiation of fetal lymphoid progenitors into functional T and B cells in mothers. J Immunol 2008, 180:889-897
14. Cha D, Khosrotehrani K, Kim Y, Stroh H, Bianchi DW, Johnson KL: Cervical cancer and microchimerism. Obstet Gynecol 2003, 102:774-781
15. Nguyen Huu S, Oster M, Uzan S, Chareyre F, Aractingi S, Khosrotehrani K: Maternal neoangiogenesis during pregnancy partly derives from fetal endothelial progenitor cells. Proc Natl Acad Sci USA 2007, 104:1871-1876
16. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y: 'Green mice' as a source of ubiquitous green cells. FEBS Lett 1997, 407:313-319
17. Johnson KL, Zhen DK, Bianchi DW: The use of fluorescence in situ hybridization (FISH) on paraffin-embedded tissue sections for the study of microchimerism. Biotechniques 2000, 29:1220-1224
18. Khosrotehrani K, Stroh H, Bianchi DW, Johnson KL: Combined FISH and immunolabeling on paraffin-embedded tissue sections for the study of microchimerism. Biotechniques 2003, 34:242-244
19. Bianchi DW: Fetomaternal cell trafficking: a new cause of disease? Am J Med Genet 2000, 91:22-28
20. Khosrotehrani K, Bianchi DW: Multi-lineage potential of fetal cells in maternal tissue: a legacy in reverse. J Cell Sci 2005, 118:1559-1563
21. Guettier C, Sebagh M, Buard J, Feneux D, Ortin-Serrano M, Gigou M, Tricottet V, Reynès M, Samuel D, Féray C: Male cell microchimerism in normal and diseased female livers from fetal life to adulthood. Hepatology 2005, 42:35-43
22. Bayes-Genis A, Bellosillo B, de la Calle O, Salido M, Roura S, Ristol FS, Soler C, Martinez M, Espinet B, Serrano S, Bayes de Luna A, Cinca J. Identification of male cardiomyocytes of extracardiac origin in the hearts of women with male progeny: male fetal cell microchimerism of the heart. J Heart Lung Transplant 2005, 24:2179-2183
23. Wang Y, Iwatani H, Ito T, Horimoto N, Yamato M, Matsui I, Imai E, Hori M: Fetal cells in mother rats contribute to the remodeling of liver and kidney after injury. Biochem Biophys Res Commun 2004, 325:961-967
24. Tan XW, Liao H, Sun L, Okabe M, Xiao ZC, Dawe GS: 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 2005, 23:1443-1452
25. Nguyen Huu S, Dubernard G, Aractingi S, Khosrotehrani K: Feto-maternal cell trafficking: a transfer of pregnancy associated progenitor cells. Stem Cell Rev 2006, 2:111-116
26. Hirakawa S, Brown LF, Kodama S, Paavonen K, Alitalo K, Detmar M: VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood 2007, 109:1010-1017
27. Hirakawa S, Kodama S, Kunstfeld R, Kajiya K, Brown LF, Detmar M: VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 2005, 201:1089-1099
28. Pack GT, Scharnagel IM: The prognosis for malignant melanoma in the pregnant woman. Cancer 1951, 4:324-334
29. Houghton AN, Flannery J, Viola MV: Malignant melanoma of the skin occurring during pregnancy. Cancer 1981, 48:407-410
30. Reintgen DS, McCarty Jr KS, Vollmer R, Cox E, Seigler HF: Malignant melanoma and pregnancy. Cancer 1985, 55:1340-1344
31. Slingluff Jr CL, Reintgen DS, Vollmer RT, Seigler HF: Malignant melanoma arising during pregnancy. A study of 100 patients. Ann Surg 1990, 211:552-557
32. O'Meara AT, Cress R, Xing G, Danielsen B, Smith LH: Malignant melanoma in pregnancy. A population-based evaluation. Cancer 2005, 103:1217-1226
33. MacKie RM, Bufalino R, Morabito A, Sutherland C, Cascinelli N: Lack of effect of pregnancy on outcome of melanoma. For The World Health Organisation Melanoma Programme. Lancet 1991, 337:653-655
34. Travers RL, Sober AJ, Berwick M, Mihm Jr MC, Barnhill RL, Duncan LM: Increased thickness of pregnancy-associated melanoma. Br J Dermatol 1995, 132:876-883
35. Dadras SS, Lange-Asschenfeldt B, Velasco P, Nguyen L, Vora A, Muzikansky A, Jahnke K, Hauschild A, Hirakawa S, Mihm MC, Detmar M: Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes. Mod Pathol 2005, 18:1232-1242
36. Dadras SS, Paul T, Bertoncini J, Brown LF, Muzikansky A, Jackson DG, Ellwanger U, Garbe C, Mihm MC, Detmar M: Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival. Am J Pathol 2003, 162:1951-1960
37. Gadi VK, Malone KE, Guthrie KA, Porter PL, Nelson JL: Case-control study of fetal microchimerism and breast cancer. PLoS ONE 2008, 3:e1706
38. Dubernard G, Aractingi S, Oster M, Rouzier R, Mathieu MC, Uzan S, Khosrotehrani K: Breast cancer stroma frequently recruits fetal derived cells during pregnancy. Breast Cancer Res 2008, 10:R14
39. O'Donoghue K, Sultan HA, Al Allaf FA, Anderson JR, Wyatt-Ashmead J, Fisk NM: Microchimeric fetal cells cluster at sites of tissue injury in lung decades after pregnancy. Reprod Biomed Online 2008, 16:382-390
40. Nguyen Huu S, Khosrotehrani K, Oster M, Moguelet P, Espie MJ, Aractingi S: Early phase of maternal skin carcinogenesis recruits long-term engrafted fetal cells. Int J Cancer 2008, 123:2512-2517
41. Dubernard G, Oster M, Chareyre F, Antoine M, Rouzier R, Uzan S, Aractingi S, Khosrotehrani, K: Increased fetal cell microchimerism in high-grade breast carcinomas occurring during pregnancy. Int J Cancer 2008, 124:1054-1059