Mesenchymal stromal cells orchestrate follicular lymphoma cell niche through the CCL2-dependent recruitment and polarization of monocytes

Blood

Volumn 119, Issue 11, 2012, Pages 2556-2567

  Guilloton, Fabien ^a   Caron, Gersende ^a,b   Ménard, Cédric ^a,b   Pangault, Céline ^a,b   Amé Thomas, Patricia ^a,b   Dulong, Joëlle ^a   De Vos, John ^c   Rossille, Delphine ^a   Henry, Catherine ^b   Lamy, Thierry ^a,d   Fouquet, Olivier ^d   Fest, Thierry ^a,b   Tarte, Karin ^a,b  

^a UNIVERSITÉ DE RENNES 1   (France)

^b RENNES UNIVERSITY HOSPITAL   (France)

^c HÔPITAL SAINT ELOI   (France)

^d PONTCHAILLOU UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCYTE CHEMOTACTIC PROTEIN 1;

ARTICLE; B CELL LYMPHOMA; CELL DIFFERENTIATION; CELL POLARITY; CONTROLLED STUDY; FOLLICULAR LYMPHOMA; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MACROPHAGE; MESENCHYMAL STROMA CELL; MONOCYTE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TUMOR ASSOCIATED LEUKOCYTE; UPREGULATION;

EID: 84858626097     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-08-370908     Document Type: Article

References (54)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-674.
2. Mueller MM, Fusenig NE. Friends or foes- bipolar effects of the tumour stroma in cancer. Nat Rev Cancer. 2004;4(11):839-849. (Pubitemid 39472951)
3. Haviv I, Polyak K, Qiu W, Hu M, Campbell I. Origin of carcinoma associated fibroblasts. Cell Cycle. 2009;8(4):589-595.
4. Studeny M, Marini FC, Dembinski JL, et al. Mesenchymal stem cells: potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. J Natl Cancer Inst. 2004;96(21):1593-1603. (Pubitemid 39534883)
5. Mishra PJ, Humeniuk R, Medina DJ, et al. Carcinoma-associated fibroblast-like differentiation of human mesenchymal stem cells. Cancer Res. 2008;68(11):4331-4339.
6. Shinagawa K, Kitadai Y, Tanaka M, et al. Mesenchymal stem cells enhance growth and metastasis of colon cancer. Int J Cancer. 2010;127:2323-2333.
7. Karnoub AE, Dash AB, Vo AP, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 2007; 449(7162):557-563. (Pubitemid 47525152)
8. Corre J, Mahtouk K, Attal M, et al. Bone marrow mesenchymal stem cells are abnormal in multiple myeloma. Leukemia. 2007;21(5):1079-1088. (Pubitemid 46672085)
9. Peduto L, Dulauroy S, Lochner M, et al. Inflammation recapitulates the ontogeny of lymphoid stromal cells. J Immunol. 2009;182(9):5789-5799.
10. Shields JD, Kourtis IC, Tomei AA, Roberts JM, Swartz MA. Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science. 2010;328(5979):749-752.
11. Mueller SN, Germain RN. Stromal cell contributions to the homeostasis and functionality of the immune system. Nat Rev Immunol. 2009;9(9):618-629.
12. Amé-Thomas P, Maby-El Hajjami H, Monvoisin C, et al. Human mesenchymal stem cells isolated from bone marrow and lymphoid organs support tumor B-cell growth: role of stromal cells in follicular lymphoma pathogenesis. Blood. 2007;109(2):693-702. (Pubitemid 46105971)
13. Burger JA, Ghia P, Rosenwald A, Caligaris- Cappio F. The microenvironment in mature B-cell malignancies: a target for new treatment strategies. Blood. 2009;114:3367-3375.
14. Dave SS, Wright G, Tan B, et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med. 2004;351(21):2159-2169. (Pubitemid 39507628)
15. Relander T, Johnson NA, Farinha P, Connors JM, Sehn LH, Gascoyne RD. Prognostic factors in follicular lymphoma. J Clin Oncol. 2010;28(17):2902-2913.
16. Thomazy VA, Vega F, Medeiros LJ, Davies PJ, Jones D. Phenotypic modulation of the stromal reticular network in normal and neoplastic lymph nodes: tissue transglutaminase reveals coordinate regulation of multiple cell types. Am J Pathol. 2003;163(1):165-174. (Pubitemid 36759601)
17. Lwin T, Hazlehurst LA, Li Z, et al. Bone marrow stromal cells prevent apoptosis of lymphoma cells by upregulation of anti-apoptotic proteins associated with activation of NF-kappaB (RelB/p52) in non-Hodgkin's lymphoma cells. Leukemia. 2007;21(7):1521-1531. (Pubitemid 46965295)
18. Lwin T, Crespo LA, Wu A, et al. Lymphoma cell adhesion-induced expression of B cell-activating factor of the TNF family in bone marrow stromal cells protects non-Hodgkin's B lymphoma cells from apoptosis. Leukemia. 2009;23(1):170-177.
19. Canioni D, Brice P, Lepage E, et al. Bone marrow histological patterns can predict survival of patients with grade 1 or 2 follicular lymphoma: a study from the Groupe d'Etude des Lymphomes Folliculaires. Br J Haematol. 2004;126(3):364-371. (Pubitemid 39005716)
20. Vega F, Medeiros LJ, Lang WH, Mansoor A, Bueso-Ramos C, Jones D. The stromal composition of malignant lymphoid aggregates in bone marrow: variations in architecture and phenotype in different B-cell tumours. Br J Haematol. 2002; 117(3):569-576. (Pubitemid 34539230)
21. Bognár A, Csernus B, Bodor C, et al. Clonal selection in the bone marrow involvement of follicular lymphoma. Leukemia. 2005;19(9):1656-1662. (Pubitemid 43090412)
22. Tarte K, Gaillard J, Lataillade JJ, et al. Clinicalgrade production of human mesenchymal stromal cells: occurrence of aneuploidy without transformation. Blood. 2010;115(8):1549-1553.
23. Maby-El Hajjami H, Ame-Thomas P, Pangault C, et al. Functional alteration of the lymphoma stromal cell niche by the cytokine context: role of indoleamine- 2,3 dioxygenase. Cancer Res. 2009;69(7):3228-3237.
24. Shibata KR, Aoyama T, Shima Y, et al. Expression of the p16INK4A gene is associated closely with senescence of human mesenchymal stem cells and is potentially silenced by DNA methylation during in vitro expansion. Stem Cells. 2007;25(9):2371-2382. (Pubitemid 47480497)
25. Streubel B, Chott A, Huber D, et al. Lymphoma-specific genetic aberrations in microvascular endothelial cells in B-cell lymphomas. N Engl J Med. 2004;351(3):250-259. (Pubitemid 38916042)
26. CoppéJP, Desprez PY, Krtolica A, Campisi J. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol. 2010;5:99-118.
27. Farinha P, Masoudi H, Skinnider BF, et al. Analysis of multiple biomarkers shows that lymphomaassociated macrophage (LAM) content is an independent predictor of survival in follicular lymphoma (FL). Blood. 2005;106:2169-2174. (Pubitemid 41291735)
28. Uccelli A, Moretta L, Pistoia V. Immunoregulatory function of mesenchymal stem cells. Eur J Immunol. 2006;36(10):2566-2573. (Pubitemid 44608440)
29. Cutler AJ, Limbani V, Girdlestone J, Navarrete CV. Umbilical cord-derived mesenchymal stromal cells modulate monocyte function to suppress T cell proliferation. J Immunol. 2010;185(11):6617-6623.
30. Cao Y. Positive and negative modulation of angiogenesis by VEGFR1 ligands. Sci Signal. 2009;2(59):re1.
31. Liotta F, Angeli R, Cosmi L, et al. Toll-like receptors 3 and 4 are expressed by human bone marrow-derived mesenchymal stem cells and can inhibit their T-cell modulatory activity by impairing Notch signaling. Stem Cells. 2008;26(1):279-289.
32. Shi D, Liao L, Zhang B, et al. Human adipose tissue-derived mesenchymal stem cells facilitate the immunosuppressive effect of cyclosporin A on T lymphocytes through Jagged-1-mediated inhibition of NF-kappaB signaling. Exp Hematol. 2011;39:214-224.
33. Erez N, Truitt M, Olson P, Arron ST, Hanahan D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaBdependent manner. Cancer Cell. 2010;17(2):135-147.
34. Delogu A, Schebesta A, SunQ,Aschenbrenner K, Perlot T, Busslinger M. Gene repression by Pax5 in B cells is essential for blood cell homeostasis and is reversed in plasma cells. Immunity. 2006; 24(3):269-281.
35. Roca H, Varsos ZS, Sud S, Craig MJ, Ying C, Pienta KJ. CCL2 and interleukin-6 promote survival of human CD11b+ peripheral blood mononuclear cells and induce M2-type macrophage polarization. J Biol Chem. 2009;284(49):34342-34354.
36. Qian BZ, Li J, Zhang H, et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011;475(7355):222-225.
37. Shi C, Jia T, Mendez-Ferrer S, et al. Bone marrow mesenchymal stem and progenitor cells induce monocyte emigration in response to circulating toll-like receptor ligands. Immunity. 2011;34(4):590-601.
38. Németh K, Leelahavanichkul A, Yuen PS, et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med. 2009;15(1):42-49.
39. Choi H, Lee RH, Bazhanov N, Oh JY, Prockop DJ. Anti-inflammatory protein TSG-6 secreted by activated MSCs attenuates zymosaninduced mouse peritonitis by decreasing TLR2/NF-{kappa}B signaling in resident macrophages. Blood. 2011;118:330-338.
40. Monsalve E, Ruiz-Garcia A, Baladron V, et al. Notch1 upregulates LPS-induced macrophage activation by increasing NF-kappaB activity. Eur J Immunol. 2009;39(9):2556-2570.
41. Hu X, Chung AY, Wu I, et al. Integrated regulation of Toll-like receptor responses by Notch and interferon-gamma pathways. Immunity. 2008; 29(5):691-703.
42. Chow A, Lucas D, Hidalgo A, et al. Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J Exp Med. 2011; 208(2):261-271.
43. Clear AJ, Lee AM, Calaminici M, et al. Increased angiogenic sprouting in poor prognosis FL is associated with elevated numbers of CD163+ macrophages within the immediate sprouting microenvironment. Blood. 2010;115(24):5053-5056.
44. Alvaro T, Lejeune M, Camacho FI, et al. The presence of STAT1-positive tumor-associated macrophages and their relation to outcome in patients with follicular lymphoma. Haematologica. 2006; 91(12):1605-1612. (Pubitemid 46032957)
45. Hu X, Park-Min KH, Ho HH, Ivashkiv LB. IFN-gamma-primed macrophages exhibit increased CCR2-dependent migration and altered IFN-gamma responses mediated by Stat1. J Immunol. 2005;175(6):3637-3647. (Pubitemid 41292023)
46. Mueller CG, Boix C, Kwan WH, et al. Critical role of monocytes to support normal B cell and diffuse large B cell lymphoma survival and proliferation. J Leukoc Biol. 2007;82(3):567-575. (Pubitemid 47367147)
47. Munari F, Lonardi S, Cassatella MA, et al. Tumor-associated macrophages as major source of APRIL in gastric MALT lymphoma. Blood. 2011; 117(24):6612-6616.
48. Epron G, Ame-Thomas P, Le Priol J, et al. Monocytes and T cells cooperate to favor normal and follicular lymphoma B-cell growth: role of IL-15 and CD40L signaling [published online ahead of print July 26, 2011]. Leukemia. doi:10.1038/leu. 2011.179.
49. Hideshima T, Mitsiades C, Tonon G, Richardson PG, Anderson KC. Understanding multiple myeloma pathogenesis in the bone marrow to identify new therapeutic targets. Nat Rev Cancer. 2007;7(8): 585-598. (Pubitemid 47106630)
50. Ding W, Knox TR, Tschumper RC, et al. Platelet-derived growth factor (PDGF)-PDGF receptor interaction activates bone marrow-derived mesenchymal stromal cells derived from chronic lymphocytic leukemia: implications for an angiogenic switch. Blood. 2010;116(16):2984-2993.
51. Tumanov AV, Grivennikov SI, Kruglov AA, et al. Cellular source and molecular form of TNF specify its distinct functions in organization of secondary lymphoid organs. Blood. 2010; 116(18):3456-3464.
52. Wahlin BE, Yri OE, Kimby E, et al. Clinical significance of the WHO grades of follicular lymphoma in a population-based cohort of 505 patients with long follow-up times. Br J Haematol. 2012;156(2): 225-233.
53. Pangault C, Ame-Thomas P, Ruminy P, et al. Follicular lymphoma cell niche: identification of a preeminent IL-4-dependent T(FH)-B cell axis. Leukemia. 2010;24(12):2080-2089.
54. Wang HW, Joyce JA. Alternative activation of tumor-associated macrophages by IL-4: priming for protumoral functions. Cell Cycle. 2010;9(24):4824-4835.