Menstrual blood-derived stromal stem cells from women with and without endometriosis reveal different phenotypic and functional characteristics

Molecular Human Reproduction

Volumn 20, Issue 9, 2014, Pages 905-918

  Nikoo, Shohreh ^a   Ebtekar, Massoumeh ^b   Jeddi Tehrani, Mahmood ^a   Shervin, Adel ^a   Bozorgmehr, Mahmood ^a   Vafaei, Sedigheh ^a   Kazemnejad, Somayeh ^a   Zarnani, Amir Hassan ^a,c  

^a AVICENNA RESEARCH INSTITUTE   (Iran)

^b TARBIAT MODARES UNIVERSITY   (Iran)

^c IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Endometriosis; IDO1; Menstrual blood; Stromal stem cells; Surface marker expression

Indexed keywords

BIOLOGICAL MARKER; CYCLOOXYGENASE 2; CYTOKINE; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3-DIOXYGENASE 1, HUMAN; PTGS2 PROTEIN, HUMAN;

ADULT; ADULT STEM CELL; CELL COMMUNICATION; CELL CULTURE; CELL MOTION; CELL PROLIFERATION; COCULTURE; CYTOLOGY; ENDOMETRIOSIS; ENDOMETRIUM; ENZYMOLOGY; FEMALE; GENETICS; HUMAN; IMMUNOLOGY; IRAN; MENSTRUATION; METABOLISM; MIDDLE AGED; MONONUCLEAR CELL; PATHOLOGY; PATHOPHYSIOLOGY; SECRETION (PROCESS); SEVERITY OF ILLNESS INDEX; STROMA CELL; TUMOR CELL LINE; UPREGULATION; YOUNG ADULT;

ADULT; ADULT STEM CELLS; BIOLOGICAL MARKERS; CELL COMMUNICATION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; CYCLOOXYGENASE 2; CYTOKINES; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; IRAN; LEUKOCYTES, MONONUCLEAR; MENSTRUATION; MIDDLE AGED; SEVERITY OF ILLNESS INDEX; STROMAL CELLS; UP-REGULATION; YOUNG ADULT;

EID: 84906064987     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gau044     Document Type: Article

References (83)

1. Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril 1997;67:817-821.
2. Abdou AG. CD10 expression in tumour and stromal cells of bladder carcinoma: an association with bilharziasis. APMIS 2007;115:1206-1218.
3. AbràmoffMD, Magalhães PJ, Ram SJ. Image processing with ImageJ. Biophotonics Int 2004;11:36-43.
4. Adachi M, Nasu K, Tsuno A, Yuge A, Kawano Y, NaraharaH. Attachment to extracellular matrices is enhanced in human endometriotic stromal cells: a possible mechanism underlying the pathogenesis of endometriosis. Eur J Obst Gynecol Reprod Biol 2011;155:85-88.
5. Attar E, Bulun SE. Aromatase and other steroidogenic genes in endometriosis: translational aspects. Hum Reprod Update 2006;12:49-56.
6. Belov L, Zhou J, Christopherson RI. Cell surface markers in colorectal cancer prognosis. Int J Mol Sci 2010;12:78-113.
7. Berbic M, Hey-Cunningham AJ, Ng C, Tokushige N, Ganewatta S, Markham R, Russell P, Fraser IS. The role of Foxp3+ regulatory T-cells in endometriosis: a potential controlling mechanism for a complex, chronic immunological condition. Hum Reprod 2010;25:900-907.
8. Borgna S, Armellin M, di Gennaro A, Maestro R, Santarosa M. Mesenchymal traits are selected along with stem features in breast cancer cells grown as mammospheres. Cell Cycle 2012;11:4242-4251.
9. Boucher A, MouradW, Mailloux J, Lemay A, Akoum A. Ovarian hormones modulate monocyte chemotactic protein-1 expression in endometrial cells of women with endometriosis. Mol Hum Reprod 2000;6:618-626.
10. Brakebusch C, Fässler R. β 1 integrin function in vivo: adhesion, migration and more. Cancer Metastasis Rev 2005;24:403-411.
11. Braun D, Longman RS, Albert ML. A two-step induction of indoleamine 2, 3 dioxygenase (IDO) activity during dendritic-cell maturation. Blood 2005; 106:2375-2381.
12. Braundmeier A, Jackson K, Hastings J, Koehler J, Nowak R, Fazleabas A. Induction of endometriosis alters the peripheral and endometrial regulatory T cell population in the non-human primate. Hum Reprod 2012;27:1712-1722.
13. Buis CC, van Leeuwen FE, Mooij TM, BurgerCW, Group OP. Increased risk for ovarian cancer and borderline ovarian tumours in subfertile women with endometriosis. Hum Reprod 2013;28:3358-3369.
14. Cammarota R, Bertolini V, Pennesi G, Bucci EO, Gottardi O, Garlanda C, Laghi L, Barberis MC, Sessa F, Noonan DM et al. The tumor microenvironment of colorectal cancer: stromal TLR-4 expression as a potential prognostic marker. J Transl Med 2010;8:112.
15. Chan RW, Ng EH, Yeung WS. Identification of cells with colony-forming activity, self-renewal capacity, and multipotency in ovarian endometriosis. Am J Pathol 2011;178:2832-2844.
16. Chung HW, Lee JY, Moon HS, Hur SE, Park MH, Wen Y, Polan ML. Matrix metalloproteinase-2, membranous type 1 matrix metalloproteinase, and tissue inhibitor of metalloproteinase-2 expression in ectopic and eutopic endometrium. Fertil Steril 2002;78:787-795.
17. Cornhill JF, Levesque MJ, Herderick EE, Nerem RM, Kilman JW, Vasko JS. Quantitative study of the rabbit aortic endothelium using vascular casts. Atherosclerosis 1980;35:321-337.
18. Darzi S, Zarnani AH, Jeddi-Tehrani M, Entezami K, Mirzadegan E, Akhondi MM, Talebi S, Khanmohammadi M, Kazemnejad S. Osteogenic differentiation of stem cells derived from menstrual blood versus bone marrow in the presence of human platelet releasate. Tissue Eng Part A 2012;18:1720-1728.
19. Delbandi AA, Mahmoudi M, Shervin A, Akbari E, Jeddi-TehraniM, Sankian M, Kazemnejad S, Zarnani AH. Eutopic and ectopic stromal cells frompatients with endometriosis exhibit differential invasive, adhesive, and proliferative behavior. Fertil Steril 2013;100:761-769.
20. Dmowski WP, Gebel HM, Braun DP. The role of cell-mediated immunity in pathogenesis of endometriosis. Acta Obst Gynecol Scand Suppl 1993; 159:7-14.
21. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. Int Soc Cell Ther Position Stat Cytother 2006;8:315-317.
22. Ebert AD, Bartley J, David M. Aromatase inhibitors and cyclooxygenase-2 (COX-2) inhibitors in endometriosis: new questions-old answers? Eur J Obstet Gynecol Reprod Biol 2005;122:144-150.
23. Erovic BM, Pammer J, Hollemann D, Woegerbauer M, GeleffS, Fischer MB, Burian M, Frommlet F, Neuchrist C. Motility-related protein-1/CD9 expression in head and neck squamous cell carcinoma. Head Neck 2003; 25:848-857.
24. Fagotti A, Ferrandina G, Fanfani F, Legge F, Lauriola L, Gessi M, Castelli P, Barbieri F, Minelli L, Scambia G. Analysis of cyclooxygenase-2 (COX-2) expression in different sites of endometriosis and correlation with clinico-pathological parameters. Hum Reprod 2004;19:393-397.
25. Fallas RE. Endometriosis; demonstration for the Sampson theory by a human anomaly. Am J Obstet Gynecol 1956;72:557-561.
26. Figueira PG, Abrao MS, Krikun G, Taylor HS. Stem cells in endometrium and their role in the pathogenesis of endometriosis. Ann N Y Acad Sci 2011; 1221:10-17.
27. Gargett BE, Chan RW. Endometrial stem/progenitor cells and proliferative disorders of the endometrium. Minerva Ginecol 2006;58:511-526.
28. Gargett CE, Masuda H. Adult stem cells in the endometrium. MolHumReprod 2010;16:818-834.
29. Gargett CE, Schwab KE, Brosens JJ, Puttemans P, Benagiano G, Brosens I. Potential role of endometrial stem/progenitor cells in the pathogenesis of early-onset endometriosis. Mol Hum Reprod 2014;20:591-598.
30. Geng S, Guo Y, Wang Q, Li L, Wang J. Cancer stem-like cells enriched with CD29 and CD44 markers exhibit molecular characteristics with epithelial-mesenchymal transition in squamous cell carcinoma. Arch Dermatol Res 2013;305:35-47.
31. Giudice LC. Clinical practice. Endometriosis. N Engl J Med 2010; 362:2389-2398.
32. Griffith JS, Liu YG, Tekmal RR, Binkley PA, Holden AE, Schenken RS. Menstrual endometrial cells from women with endometriosis demonstrate increased adherence to peritoneal cells and increased expression of CD44 splice variants. Fertil Steril 2010;93:1745-1749.
33. Halme J, Hammond MG, Hulka JF, Raj SG, Talbert LM. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol 1984;64:151-154.
34. Hwang JR, Jo K, Lee Y, Sung BJ, Park YW, Lee JH. Upregulation of CD9 in ovarian cancer is related to the induction of TNF-alpha gene expression and constitutive NF-kappaB activation. Carcinogenesis 2012;33:77-83.
35. Jasper MJ, Tremellen KP, Robertson SA. Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Mol Hum Reprod 2006;12:301-308.
36. Jeddi-Tehrani M, Abbasi N, Dokouhaki P, Ghasemi J, Rezania S, Ostadkarampour M, Rabbani H, Akhondi MA, Fard ZT, Zarnani AH. Indoleamine 2,3-dioxygenase is expressed in the endometrium of cycling mice throughout the oestrous cycle. J Reprod Immunol 2009;80:41-48.
37. Jensen KB, Jones J, Watt FM. A stem cell gene expression profile of human squamous cell carcinomas. Cancer Lett 2008;272:23-31.
38. Jolicoeur C, Boutouil M, Drouin R, Paradis I, Lemay A, Akoum A. Increased expression of monocyte chemotactic protein-1 in the endometrium of women with endometriosis. Am J Pathol 1998;152:125-133.
39. Jones RK, Bulmer JN, Searle RF. Immunohistochemical characterization of proliferation, oestrogen receptor and progesterone receptor expression in endometriosis: comparison of eutopic and ectopic endometrium with normal cycling endometrium. Hum Reprod 1995;10:3272-3279.
40. Kao AP, Wang KH, Long CY, Chai CY, Tsai CF, Hsieh TH, Hsu CY, Chang CC, Lee JN, Tsai EM. Interleukin-1beta induces cyclooxygenase-2 expression and promotes the invasive ability of human mesenchymal stem cells derived from ovarian endometrioma. Fertil Steril 2011;96:678-684.e1.
41. Kazemnejad S, Akhondi M-M, Soleimani M, Zarnani AH, Khanmohammadi M, Darzi S, Alimoghadam K. Characterization and chondrogenic differentiation of menstrual blood-derived stem cells on a nanofibrous scaffold. Int J Artif Organs 2012;35:55-66.
42. Kazemnejad S, Zarnani AH, Khanmohammadi M, Mobini S. Chondrogenic differentiation of menstrual blood-derived stem cells on nanofibrous scaffolds. Methods Mol Biol 2013;1058:149-169.
43. Kazemnejad S, NajafiR, Zarnani AH, Eghtesad S. Comparative effect of human platelet derivatives on proliferation and osteogenic differentiation of menstrual blood-derived stem cells. Mol Biotechnol 2014;56: 223-231.
44. Khanjani S, Khanmohammadi M, Zarnani AH, Talebi S, Edalatkhah H, Eghtesad S, Nikokar I, Kazemnejad S. Efficient generation of functional hepatocyte-like cells from menstrual blood-derived stem cells. J Tissue Eng Regen Med 2013. doi:10.1002/term.1715.
45. Khanjani S, Khanmohammadi M, Zarnani AH, Akhondi MM, Ahani A, Ghaempanah Z, Naderi MM, Eghtesad S, Kazemnejad S. Comparative evaluation of differentiation potential of menstrual blood- versus bone marrow-derived stem cells into hepatocyte-like cells. PLOS One 2014; 9:e86075.
46. Khanmohammadi M, Khanjani S, Bakhtyari MS, Zarnani AH, Edalatkhah H, Akhondi MM, Mirzadegan E, Kamali K, Alimoghadam K, Kazemnejad S. Proliferation and chondrogenic differentiation potential of menstrual blood-and bone marrow-derived stem cells in two-dimensional culture. Int J Hematol 2012;95:484-493.
47. Klemmt PA, Carver JG, Koninckx P, McVeigh EJ, Mardon HJ. Endometrial cells from women with endometriosis have increased adhesion and proliferative capacity in response to extracellular matrix components: towards a mechanistic model for endometriosis progression. Hum Reprod 2007;22:3139-3147.
48. Kohmo S, Kijima T, Otani Y, Mori M, Minami T, Takahashi R, Nagatomo I, Takeda Y, Kida H, Goya S et al. Cell surface tetraspanin CD9 mediates chemoresistance in small cell lung cancer. Cancer Res 2010; 70:8025-8035.
49. Kyama CM, Debrock S, Mwenda JM, D'Hooghe TM. Potential involvement of the immune system in the development of endometriosis. Reprod Biol Endocrinol 2003;1:123.
50. Laschke MW, Menger MD. In vitro and in vivo approaches to study angiogenesis in the pathophysiology and therapy of endometriosis. Hum Reprod Update 2007;13:331-342.
51. Lloyd AC. The regulation of cell size. Cell 2013;154:1194-1205.
52. Matsuzaki S, Canis M, Pouly JL, Wattiez A, Okamura K, Mage G. Cyclooxygenase-2 expression in deep endometriosis and matched eutopic endometrium. Fertil Steril 2004;82:1309-1315.
53. Mei J, Jin LP, Ding D, Li MQ, Li DJ, Zhu XY. Inhibition of IDO1 suppresses cyclooxygenase-2 and matrix metalloproteinase-9 expression and decreases proliferation, adhesion and invasion of endometrial stromal cells. Mol Hum Reprod 2012;18:467-476.
54. Meng X, Ichim TE, Zhong J, Rogers A, Yin Z, Jackson J, Wang H, Ge W, Bogin V, Chan KW et al. Endometrial regenerative cells: a novel stem cell population. J Transl Med 2007;5:57.
55. Meresman GF, Auge L, Baranao RI, Lombardi E, Tesone M, Sueldo C. Oral contraceptives suppress cell proliferation and enhance apoptosis of eutopic endometrial tissue from patients with endometriosis. Fertil Steril 2002;77:1141-1147.
56. Meyer PN, Fu K, Greiner T, Smith L, Delabie J, Gascoyne R, Ott G, Rosenwald A, Braziel R, Campo E et al. The stromal cell marker SPARC predicts for survival in patients with diffuse large B-cell lymphoma treated with rituximab. Am J Clin Pathol 2011;135:54-61.
57. Mulayim N, Savlu A, Guzeloglu-Kayisli O, Kayisli UA, Arici A. Regulation of endometrial stromal cell matrix metalloproteinase activity and invasiveness by interleukin-8. Fertil Steril 2004;81(Suppl. 1):904-911.
58. Munn DH, Mellor AL, Rossi M, Young JW. Dendritic cells have the option to express IDO-mediated suppression or not. Blood 2005;105:2618.
59. Murphy MP, Wang H, Patel AN, Kambhampati S, Angle N, Chan K, Marleau AM, Pyszniak A, Carrier E, Ichim TE et al. Allogeneic endometrial regenerative cells: an 'Offthe shelf solution' for critical limb ischemia? J Transl Med 2008;6:45.
60. Nakamoto T, Murayama Y, Oritani K, Boucheix C, Rubinstein E, Nishida M, Katsube F, Watabe K, Kiso S, Tsutsui S et al. A novel therapeutic strategy with anti-CD9 antibody in gastric cancers. J Gastroenterol 2009;44:889-896.
61. Nikoo S, Ebtekar M, Jeddi-Tehrani M, Shervin A, Bozorgmehr M, Kazemnejad S, Zarnani AH. Effect of menstrual blood-derived stromal stem cells on proliferative capacity of peripheral blood mononuclear cells in allogeneic mixed lymphocyte reaction. J Obstet Gynaecol Res 2012;38:804-809.
62. Nisolle M, Casanas-Roux F, Donnez J. Immunohistochemical analysis of proliferative activity and steroid receptor expression in peritoneal and ovarian endometriosis. Fertil Steril 1997;68:912-919.
63. Ota H, Igarashi S, Sasaki M, Tanaka T. Distribution of cyclooxygenase-2 in eutopic and ectopic endometrium in endometriosis and adenomyosis. Hum Reprod 2001;16:561-566.
64. Park JS, Lee JH, Kim M, Chang HJ, Hwang KJ, Chang KH. Endometrium from women with endometriosis shows increased proliferation activity. Fertil Steril 2009;92:1246-1249.
65. Patel AN, Park E, Kuzman M, Benetti F, Silva FJ, Allickson JG. Multipotent menstrual blood stromal stem cells: isolation, characterization, and differentiation. Cell Transpl 2008;17:303-311.
66. Potlog-Nahari C, Feldman AL, Stratton P, Koziol DE, Segars J, Merino MJ, Nieman LK. CD10 immunohistochemical staining enhances the histological detection of endometriosis. Fertil Steril 2004;82:86-92.
67. Rafii A, Mirshahi P, Poupot M, Faussat AM, Simon A, Ducros E, Mery E, Couderc B, Lis R, Capdet J et al. Oncologic trogocytosis of an original stromal cells induces chemoresistance of ovarian tumours. PLOS One 2008;3:e3894.
68. Rahimi M, Mohseni-Kouchesfehani H, Zarnani AH, Mobini S, Nikoo S, Kazemnejad S. Evaluation of menstrual blood stem cells seeded in biocompatible Bombyx mori silk fibroin scaffold for cardiac tissue engineering. J Biomater Appl 2014.
69. Ritter U, Moll H. Monocyte chemotactic protein-1 stimulates the killing of leishmania major by human monocytes, acts synergistically with IFN-gamma and is antagonized by IL-4. Eur J Immunol 2000; 30:3111-3120.
70. Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol 1927;3:93-110.43.
71. Sasson IE, Taylor HS. Stem cells and the pathogenesis of endometriosis. Ann N Y Acad Sci 2008;1127:106-115.
72. Schutte SC, Taylor RN. A tissue-engineered human endometrial stroma that responds to cues for secretory differentiation, decidualization, and menstruation. Fertil Steril 2012;97:997-1003.
73. Silveira CG, Abrao MS, Dias JA Jr, Coudry RA, Soares FA, Drigo SA, Domingues MA, Rogatto SR. Common chromosomal imbalances and stemness-related protein expression markers in endometriotic lesions from different anatomical sites: the potential role of stem cells. Hum Reprod 2012;27:3187-3197.
74. Spaeth EL, Dembinski JL, Sasser AK, Watson K, Klopp A, Hall B, AndreeffM, Marini F. Mesenchymal stem cell transition to tumor-associated fibroblasts contributes to fibrovascular network expansion and tumor progression. PLOS One 2009;4:e4992.
75. Sundin M, D'Arcy P, Johansson CC, Barrett AJ, Lonnies H, Sundberg B, Nava S, Kiessling R, Mougiakakos D, Le Blanc K. Multipotent mesenchymal stromal cells express FoxP3: a marker for the immunosuppressive capacity? J Immunother 2011;34:336-342.
76. Tariverdian N, Theoharides TC, Siedentopf F, Gutiérrez G, Jeschke U, Rabinovich GA, Blois SM, Arck PC. Neuroendocrine-immune disequilibrium and endometriosis: an interdisciplinary approach. Semin Immunopathol 2007;29: 193-210.
77. Ueda M, Yamashita Y, Takehara M, Terai Y, Kumagai K, Ueki K, Kanda K, Yamaguchi H, Akise D, Hung YC et al. Survivin gene expression in endometriosis. J Clin Endocrinol Metab 2002;87:3452-3459.
78. Van der Linden P, De Goeij A, Dunselman G, Erkens H, Evers J. Expression of cadherins and integrins in human endometrium throughout the menstrual cycle. Fertil Steril 1995;63:1210-1216.
79. Vane JR, Mitchell JA, Appleton I, Tomlinson A, Bishop-Bailey D, Croxtall J, Willoughby DA. Inducible isoforms of cyclooxygenase and nitric-oxide synthase in inflammation. Proc Natl Acad Sci USA 1994;91:2046-2050.
80. von Schlippe M, Marshall JF, Perry P, Stone M, Zhu AJ, Hart IR. Functional interaction between E-cadherin and alphav-containing integrins in carcinoma cells. J Cell Sci 2000;113:425-437.
81. Wu M-Y, Yang J-H, Chao K-H, Hwang J-L, Yang Y-S, Ho H-N. Increase in the expression of killer cell inhibitory receptors on peritoneal natural killer cells in women with endometriosis. Fertil Steril 2000; 74:1187-1191.
82. Yamagami W, Susumu N, Tanaka H, Hirasawa A, Banno K, Suzuki N, Tsuda H, Tsukazaki K, Aoki D. Immunofluorescence-detected infiltration of CD4+FOXP3+ regulatory T cells is relevant to the prognosis of patients with endometrial cancer. Int J Gynecol Cancer 2011; 21:1628-1634.
83. Zarnani AH, Shahbazi M, Salek-Moghaddam A, Zareie M, Tavakoli M, Ghasemi J, Rezania S, Moravej A, Torkabadi E, Rabbani H et al. Vitamin D3 receptor is expressed in the endometrium of cycling mice throughout the estrous cycle. Fertil Steril 2010;93:2738-2743.