Enriched protein screening of human bone marrow mesenchymal stromal cell secretions reveals MFAP5 and PENK as novel IL-10 modulators

Molecular Therapy

Volumn 22, Issue 5, 2014, Pages 999-1007

  Milwid, Jack M ^a,b   Elman, Jessica S ^a   Li, Matthew ^a,b   Shen, Keyue ^a   Manrai, Arjun ^b   Gabow, Aaron ^c   Yarmush, Joshua ^e   Jiao, Yunxin ^a   Fletcher, Anne ^d   Lee, Jungwoo ^a   Cima, Michael J ^b   Yarmush, Martin L ^a,e   Parekkadan, Biju ^a,f  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e RUTGERS UNIVERSITY   (United States)

^f HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; IMMUNOMODULATING AGENT; INTERLEUKIN 10; MICROFIBRILLAR ASSOCIATED PROTEIN 5; PROENKEPHALIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; CONTRACTILE PROTEIN; ENKEPHALIN; GLYCOPROTEIN; IL10 PROTEIN, HUMAN; MAGP2 PROTEIN, HUMAN; MICROFIBRILLAR PROTEIN; PROTEIN; PROTEIN PRECURSOR; SCLEROPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOASSAY; BLOOD ANALYSIS; BONE MARROW CELL; CELLULAR SECRETION; CONTROLLED STUDY; CYTOKINE STORM; DRUG EFFECT; DRUG POTENCY; ENRICHED PROTEIN SCREENING; FUNCTIONAL PROTEOMICS; GENE EXPRESSION PROFILING; GOLD STANDARD; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STROMA CELL; MONOCYTE; NONHUMAN; PROCESS DEVELOPMENT; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN TARGETING; SEPTIC SHOCK; ANIMAL; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE; PROTEIN SYNTHESIS; PROTEOMICS; SECRETION (PROCESS); SHOCK, SEPTIC;

MUS;

ANIMALS; BONE MARROW CELLS; CONTRACTILE PROTEINS; ENKEPHALINS; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION PROFILING; GLYCOPROTEINS; HUMANS; INTERLEUKIN-10; MESENCHYMAL STROMAL CELLS; MICE; PROTEIN BIOSYNTHESIS; PROTEIN PRECURSORS; PROTEINS; PROTEOMICS; SHOCK, SEPTIC;

EID: 84899960384     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.17     Document Type: Article

References (52)

1. Nakamura, T, Nishizawa, T, Hagiya, M, Seki, T, Shimonishi, M, Sugimura, A et al. (1989. Molecular cloning and expression of human hepatocyte growth factor. Nature 342: 440-443.
2. Heinzel, FP, Sadick, MD, Holaday, BJ, Coffman, RL and Locksley, RM (1989. Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets. J Exp Med 169: 59-72.
3. Leung, DW, Cachianes, G, Kuang, WJ, Goeddel, DV and Ferrara, N (1989. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246: 1306-1309.
4. Suda, T, Takahashi, T, Golstein, P and Nagata, S (1993. Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell 75: 1169-1178.
5. Daneman, D (2006. Type 1 diabetes. Lancet 367: 847-858.
6. Aggarwal, SR (2012. What's fueling the biotech engine-2011 to 2012. Nat Biotechnol 30: 1191-1197.
7. Manns, MP, McHutchison, JG, Gordon, SC, Rustgi, VK, Shiffman, M, Reindollar, R et al. (2001. Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial. Lancet 358: 958-965.
8. Taylor, PC and Feldmann, M (2009. Anti-TNF biologic agents: still the therapy of choice for rheumatoid arthritis. Nat Rev Rheumatol 5: 578-582.
9. Guzman, C, and Feuerstein, G (eds (2009. Pharmaceutical Biotechnology. Landes Bioscience and Springer Science+Business Media: Austin, Texas, USA.
10. Harrison, PM, Kumar, A, Lang, N, Snyder, M and Gerstein, M (2002. A question of size: the eukaryotic proteome and the problems in defining it. Nucleic Acids Res 30: 1083-1090.
11. Rubinstein, M, Rubinstein, S, Familletti, PC, Gross, MS, Miller, RS, Waldman, AA et al. (1978. Human leukocyte interferon purified to homogeneity. Science 202: 1289-1290.
12. Montesano, R, Matsumoto, K, Nakamura, T and Orci, L (1991. Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 67: 901-908.
13. Elias, JE and Gygi, SP (2007. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4: 207-214.
14. Sharma, K, Weber, C, Bairlein, M, Greff, Z, Kéri, G, Cox, J et al. (2009. Proteomics strategy for quantitative protein interaction profiling in cell extracts. Nat Methods 6: 741-744.
15. Jiao, Y, Milwid, JM, Yarmush, ML, and Parekkadan, B (2010. A Mesenchymal Stem Cell Potency Assay. In: Cuturi, M and Anegon, I (eds. Suppression and Regulation of Immune Responses, vol. 677. Humana Press and Springer: Totowa, New Jersey, USA.
16. Parekkadan, B and Milwid, JM (2010. Mesenchymal stem cells as therapeutics. Annu Rev Biomed Eng 12: 87-117.
17. Uccelli, A, Moretta, L and Pistoia, V (2008. Mesenchymal stem cells in health and disease. Nat Rev Immunol 8: 726-736.
18. van Poll, D, Parekkadan, B, Cho, CH, Berthiaume, F, Nahmias, Y, Tilles, AW et al. (2008. Mesenchymal stem cell-derived molecules directly modulate hepatocellular death and regeneration in vitro and in vivo. Hepatology 47: 1634-1643.
19. Tomchuck, SL, Zwezdaryk, KJ, Coffelt, SB, Waterman, RS, Danka, ES and Scandurro, AB (2008. Toll-like receptors on human mesenchymal stem cells drive their migration and immunomodulating responses. Stem Cells 26: 99-107.
20. Kwok, TC, Ricker, N, Fraser, R, Chan, AW, Burns, A, Stanley, EF et al. (2006. A smallmolecule screen in C. elegans yields a new calcium channel antagonist. Nature 441: 91-95.
21. Hung, DT, Shakhnovich, EA, Pierson, E and Mekalanos, JJ (2005. Small-molecule inhibitor of Vibrio cholerae virulence and intestinal colonization. Science 310: 670-674.
22. Sheridan, C (2008. Small molecule challenges dominance of TNF-alpha inhibitors. Nat Biotechnol 26: 143-144.
23. Gubler, U, Seeburg, P, Hoffman, BJ, Gage, LP and Udenfriend, S (1982. Molecular cloning establishes proenkephalin as precursor of enkephalin- containing peptides. Nature 295: 206-208.
24. Heagy, W, Laurance, M, Cohen, E and Finberg, R (1990. Neurohormones regulate T cell function. J Exp Med 171: 1625-1633.
25. Ohmori, H, Fujii, K, Sasahira, T, Luo, Y, Isobe, M, Tatsumoto, N et al. (2009. Methionine-enkephalin secreted by human colorectal cancer cells suppresses T lymphocytes. Cancer Sci 100: 497-502.
26. Goumon, Y, Lugardon, K, Kieffer, B, Lefèvre, JF, Van Dorsselaer, A, Aunis, D et al. (1998. Characterization of antibacterial COOH-terminal proenkephalin-A-derived peptides (PEAP in infectious fluids. Importance of enkelytin, the antibacterial PEAP209-237 secreted by stimulated chromaffin cells. J Biol Chem 273: 29847-29856.
27. Roscetti, G, Ausiello, CM, Palma, C, Gulla, P and Roda, LG (1988. Enkephalin activity on antigen-induced proliferation of human peripheral blood mononucleate cells. Int J Immunopharmacol 10: 819-823.
28. Penner, AS, Rock, MJ, Kielty, CM and Shipley, JM (2002. Microfibril-associated glycoprotein-2 interacts with fibrillin-1 and fibrillin-2 suggesting a role for MAGP-2 in elastic fiber assembly. J Biol Chem 277: 35044-35049.
29. Miyamoto, A, Lau, R, Hein, PW, Shipley, JM and Weinmaster, G (2006. Microfibrillar proteins MAGP-1 and MAGP-2 induce Notch1 extracellular domain dissociation and receptor activation. J Biol Chem 281: 10089-10097.
30. Mok, SC, Bonome, T, Vathipadiekal, V, Bell, A, Johnson, ME, Wong, KK et al. (2009. A gene signature predictive for outcome in advanced ovarian cancer identifies a survival factor: microfibril-associated glycoprotein Cancer Cell 16: 521-532.
31. Lazennec, G and Jorgensen, C (2008. Concise review: adult multipotent stromal cells and cancer: risk or benefit? Stem Cells 26: 1387-1394.
32. Hook, S, Camberis, M, Prout, M, Konig, M, Zimmer, A, Van Heeke, G et al. (1999. Preproenkephalin is a Th2 cytokine but is not required for Th2 differentiation in vitro. Immunol Cell Biol 77: 385-390.
33. Pittenger, M (2009. Sleuthing the source of regeneration by MSCs. Cell Stem Cell 5: 8-10.
34. de Waal Malefyt, R, Abrams, J, Bennett, B, Figdor, CG and de Vries, JE (1991. Interleukin 10(IL-10 inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 174: 1209-1220.
35. Bogdan, C, Vodovotz, Y and Nathan, C (1991. Macrophage deactivation by interleukin J Exp Med 174: 1549-1555.
36. Rousset, F, Garcia, E, Defrance, T, Péronne, C, Vezzio, N, Hsu, DH et al. (1992. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc Natl Acad Sci USA 89: 1890-1893.
37. Asseman, C, Mauze, S, Leach, MW, Coffman, RL and Powrie, F (1999. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 190: 995-1004.
38. Kühn, R, Löhler, J, Rennick, D, Rajewsky, K and Müller, W (1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263-274.
39. Gateva, V, Sandling, JK, Hom, G, Taylor, KE, Chung, SA, Sun, X et al. (2009. A largescale replication study identifies TNIP1, PRDM1, JAZF1, UHRF1BP1 and IL10 as risk loci for systemic lupus erythematosus. Nat Genet 41: 1228-1233.
40. Noguchi, E, Homma, Y, Kang, X, Netea, MG and Ma, X (2009. A Crohn's diseaseassociated NOD2 mutation suppresses transcription of human IL10 by inhibiting activity of the nuclear ribonucleoprotein hnRNP-A1. Nat Immunol 10: 471-479.
41. Franke, A, Balschun, T, Karlsen, TH, Sventoraityte, J, Nikolaus, S, Mayr, G et al.; IBSEN study group. (2008. Sequence variants in IL10, ARPC2 and multiple other loci contribute to ulcerative colitis susceptibility. Nat Genet 40: 1319-1323.
42. Mizuki, N, Meguro, A, Ota, M, Ohno, S, Shiota, T, Kawagoe, T et al. (2010. Genome-wide association studies identify IL23R-IL12RB2 and IL10 as Behçet's disease susceptibility loci. Nat Genet 42: 703-706.
43. Remmers, EF, Cosan, F, Kirino, Y, Ombrello, MJ, Abaci, N, Satorius, C et al. (2010. Genome-wide association study identifies variants in the MHC class I, IL10, and IL23RIL12RB2 regions associated with Behçet's disease. Nat Genet 42: 698-702.
44. Asadullah, K, Sterry, W, Stephanek, K, Jasulaitis, D, Leupold, M, Audring, H et al. (1998. IL-10 is a key cytokine in psoriasis. Proof of principle by IL-10 therapy: a new therapeutic approach. J Clin Invest 101: 783-794.
45. Keystone, E, Wherry, J and Grint, P (1998. IL-10 as a therapeutic strategy in the treatment of rheumatoid arthritis. Rheum Dis Clin North Am 24: 629-639.
46. Li, MC and He, SH (2004. IL-10 and its related cytokines for treatment of inflammatory bowel disease. World J Gastroenterol 10: 620-625.
47. Mosser, DM and Zhang, X (2008. Interleukin-10: new perspectives on an old cytokine. Immunol Rev 226: 205-218.
48. Gentleman, RC, Carey, VJ, Bates, DM, Bolstad, B, Dettling, M, Dudoit, S et al. (2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
49. Irizarry, RA, Bolstad, BM, Collin, F, Cope, LM, Hobbs, B and Speed, TP (2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15.
50. Smyth, GK (2004. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
51. Benjamini, Y, and Hochberg, Y (1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Statistical Society Series B (Methodological 57: 289-300.
52. Jiang, X, Chen, S, Asara, JM and Balk, SP (2010. Phosphoinositide 3-kinase pathway activation in phosphate and tensin homolog (PTEN-deficient prostate cancer cells is independent of receptor tyrosine kinases and mediated by the p110beta and p110delta catalytic subunits. J Biol Chem 285: 14980-14989.