The multiple facets of the TGF-β family cytokine growth/differentiation factor-15/macrophage inhibitory cytokine-1

Cytokine and Growth Factor Reviews

Volumn 24, Issue 4, 2013, Pages 373-384

  Unsicker, Klaus ^a   Spittau, Björn ^a   Krieglstein, Kerstin ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Cancer; Cardiovascular disease; Inflammation; Metabolism; Neurotrophic factors

Indexed keywords

GROWTH DIFFERENTIATION FACTOR 15;

ATHEROSCLEROSIS; CARDIOVASCULAR FUNCTION; ERYTHROPOIESIS; GASTROINTESTINAL TRACT; GDF 15 GENE; GENE EXPRESSION REGULATION; GENE STRUCTURE; HUMAN; INFLAMMATION; INTEGUMENTARY SYSTEM; ISCHEMIC HEART DISEASE; MALIGNANT NEOPLASTIC DISEASE; METABOLIC DISORDER; METABOLIC REGULATION; MOLECULAR PATHOLOGY; MUSCULOSKELETAL SYSTEM; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESPIRATORY SYSTEM; REVIEW; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; UROGENITAL SYSTEM;

MAMMALIA;

CANCER; CARDIOVASCULAR DISEASE; INFLAMMATION; METABOLISM; NEUROTROPHIC FACTORS;

ANIMALS; CARDIOVASCULAR DISEASES; GENE EXPRESSION REGULATION; GROWTH DIFFERENTIATION FACTOR 15; HUMANS; INFLAMMATION; MICE; NEOPLASMS; OBESITY; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84883809336     PISSN: 13596101     EISSN: 18790305     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2013.05.003     Document Type: Review

References (120)

1. Bootcov M.R., Bauskin A.R., Valenzuela S.M., Moore A.G., Bansal M., He X.Y., et al. MIC-1, a novel macrophage inhibitory cytokine, is a divergent member of the TGF-beta superfamily. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:11514-11519.
2. Hromas R., Hufford M., Sutton J., Xu D., Li Y., Lu L. PLAB, a novel placental bone morphogenetic protein. Biochimica et Biophysica Acta 1997, 1354:40-44.
3. Lawton L.N., Bonaldo M.F., Jelenc P.C., Qiu L., Baumes S.A., Marcelino R.A., et al. Identification of a novel member of the TGF-beta superfamily highly expressed in human placenta. Gene 1997, 203:17-26.
4. Yokoyama-Kobayashi M., Saeki M., Sekine S., Kato S. Human cDNA encoding a novel TGF-beta superfamily protein highly expressed in placenta. Journal of Biochemistry 1997, 122:622-626.
5. Paralkar V.M., Vail A.L., Grasser W.A., Brown T.A., Xu H., Vukicevic S., et al. Cloning and characterization of a novel member of the transforming growth factor-beta/bone morphogenetic protein family. Journal of Biological Chemistry 1998, 273:13760-13767.
6. Böttner M., Suter-Crazzolara C., Schober A., Unsicker K. Expression of a novel member of the TGF-beta superfamily, growth/differentiation factor-15/macrophage-inhibiting cytokine-1 (GDF-15/MIC-1) in adult rat tissues. Cell and Tissue Research 1999, 297:103-110.
7. Böttner M., Laaff M., Schechinger B., Rappold G., Unsicker K., Suter-Crazzolara C. Characterization of the rat, mouse, and human genes of growth/differentiation factor-15/macrophage inhibiting cytokine-1 (GDF-15/MIC-1). Gene 1999, 237:105-111.
8. Baek S.J., Kim K.S., Nixon J.B., Wilson L.C., Eling T.E. Cyclooxygenase inhibitors regulate the expression of a TGF-beta superfamily member that has proapoptotic and antitumorigenic activities. Molecular Pharmacology 2001, 59:901-908.
9. Fairlie W.D., Moore A.G., Bauskin A.R., Russell P.K., Zhang H.P., Breit S.N. MIC-1 is a novel TGF-beta superfamily cytokine associated with macrophage activation. Journal of Leukocyte Biology 1999, 65:2-5.
10. Baek S.J., Horowitz J.M., Eling T.E. Molecular cloning and characterization of human nonsteroidal anti-inflammatory drug-activated gene promoter. Basal transcription is mediated by Sp1 and Sp3. Journal of Biological Chemistry 2001, 276:33384-33392.
11. Kannan K., Amariglio N., Rechavi G., Givol D. Profile of gene expression regulated by induced p53: connection to the TGF-beta family. FEBS Letters 2000, 470:77-82.
12. Baek S.J., Wilson L.C., Eling T.E. Resveratrol enhances the expression of non-steroidal anti-inflammatory drug-activated gene (NAG-1) by increasing the expression of p53. Carcinogenesis 2002, 23:425-434.
13. Albertoni M., Shaw P.H., Nozaki M., Godard S., Tenan M., Hamou M.F., et al. Anoxia induces macrophage inhibitory cytokine-1 (MIC-1) in glioblastoma cells independently of p53 and HIF-1. Oncogene 2002, 21:4212-4219.
14. Yang H., Filipovic Z., Brown D., Breit S.N., Vassilev L.T. Macrophage inhibitory cytokine-1: a novel biomarker for p53 pathway activation. Molecular Cancer Therapeutics 2003, 2:1023-1029.
15. Agarwal M.K., Hastak K., Jackson M.W., Breit S.N., Stark G.R., Agarwal M.L. Macrophage inhibitory cytokine 1 mediates a p53-dependent protective arrest in S phase in response to starvation for DNA precursors. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:16278-16283.
16. Bauskin A.R., Zhang H.P., Fairlie W.D., He X.Y., Russell P.K., Moore A.G., et al. The propeptide of macrophage inhibitory cytokine (MIC-1), a TGF-beta superfamily member, acts as a quality control determinant for correctly folded MIC-1. EMBO Journal 2000, 19:2212-2220.
17. Bauskin A.R., Jiang L., Luo X.W., Wu L., Brown D.A., Breit S.N. The TGF-beta superfamily cytokine MIC-1/GDF15: secretory mechanisms facilitate creation of latent stromal stores. Journal of Interferon and Cytokine Research 2010, 30:389-397.
18. Heger J., Schiegnitz E., von Waldthausen D., Anwar M.M., Piper H.M., Euler G. Growth differentiation factor 15 acts anti-apoptotic and pro-hypertrophic in adult cardiomyocytes. Journal of Cellular Physiology 2010, 224:120-126.
19. Johnen H., Lin S., Kuffner T., Brown D.A., Tsai V.W., Bauskin A.R., et al. Tumor-induced anorexia and weight loss are mediated by the TGF-beta superfamily cytokine MIC-1. Nature Medicine 2007, 13:1333-1340.
20. Subramaniam S., Strelau J., Unsicker K. Growth differentiation factor-15 prevents low potassium-induced cell death of cerebellar granule neurons by differential regulation of Akt and ERK pathways. Journal of Biological Chemistry 2003, 278:8904-8912.
21. Breit S.N., Johnen H., Cook A.D., Tsai V.W., Mohammad M.G., Kuffner T., et al. The TGF-beta superfamily cytokine, MIC-1/GDF15: a pleotrophic cytokine with roles in inflammation, cancer and metabolism. Growth Factors 2011, 29:187-195.
22. Kempf T., Zarbock A., Widera C., Butz S., Stadtmann A., Rossaint J., et al. GDF-15 is an inhibitor of leukocyte integrin activation required for survival after myocardial infarction in mice. Nature Medicine 2011, 17:581-588.
23. Rossaint J., Vestweber D., Zarbock A. GDF-15 prevents platelet integrin activation and thrombus formation. Journal of Thrombosis and Haemostasis 2013, 11:335-344.
24. de Jager S.C., Bermúdez B., Bot I., Koenen R.R., Bot M., Kavelaars A., et al. Growth differentiation factor 15 deficiency protects against atherosclerosis by attenuating CCR2-mediated macrophage chemotaxis. Journal of Experimental Medicine 2011, 208:217-225.
25. Bonaterra G.A., Zügel S., Thogersen J., Walter S.A., Haberkorn U., Strelau J., et al. Growth differentiation factor-15 deficiency inhibits atherosclerosis progression by regulating interleukin-6-dependent inflammatory response to vascular injury. Journal of American Heart Association 2012, 1:e002550.
26. Whitson R.J., Lucia M.S., Lambert J.R. Growth differentiation factor-15 (GDF-15) suppresses in vitro angiogenesis through a novel interaction with connective tissue growth factor (CCN2). Journal of Cellular Biochemistry 2013, 114:1424-1433.
27. Ferrari N., Pfeffer U., Dell'Eva R., Ambrosini C., Noonan D.M., Albini A. The transforming growth factor-beta family members bone morphogenetic protein-2 and macrophage inhibitory cytokine-1 as mediators of the antiangiogenic activity of N-(4-hydroxyphenyl)retinamide. Clinical Cancer Research 2005, 11:4610-4619.
28. Song H., Yin D., Liu Z. GDF-15 promotes angiogenesis through modulating p53/HIF-1α signaling pathway in hypoxic human umbilical vein endothelial cells. Molecular Biology Reports 2012, 39:4017-4022.
29. Mazagova M., Buikema H., Landheer S., Vavrinec P., van Buiten A., Henning R.H., et al. Growth differentiation factor 15 impairs aortic contractile and relaxing function through altered caveolar signaling of the endothelium. American Journal of Physiology. Heart and Circulatory Physiology 2013, 304:H709-H718.
30. Tchou I., Margeli A., Tsironi M., Skenderi K., Barnet M., Kanaka-Gantenbein C., et al. Growth-differentiation factor-15, endoglin and N-terminal pro-brain natriuretic peptide induction in athletes participating in an ultramarathon foot race. Biomarkers 2009, 14:418-422.
31. Eggers K.M., Kempf T., Lind L., Sundström J., Wallentin L., Wollert K.C., et al. Relations of growth-differentiation factor-15 to biomarkers reflecting vascular pathologies in a population-based sample of elderly subjects. Scandinavian Journal of Clinical and Laboratory Investigation 2012, 72:45-51.
32. Schober A., Böttner M., Strelau J., Kinscherf R., Bonaterra G.A., Barth M., et al. Expression of growth differentiation factor-15/macrophage inhibitory cytokine-1 (GDF-15/MIC-1) in the perinatal, adult, and injured rat brain. Journal of Comparative Neurology 2001, 439:32-45.
33. Xu J., Kimball T.R., Lorenz J.N., Brown D.A., Bauskin A.R., Klevitsky R., et al. GDF15/MIC-1 functions as a protective and antihypertrophic factor released from the myocardium in association with SMAD protein activation. Circulation Research 2006, 98:342-350.
34. Kempf T., Eden M., Strelau J., Naguib M., Willenbockel C., Tongers J., et al. The transforming growth factor-beta superfamily member growth-differentiation factor-15 protects the heart from ischemia/reperfusion injury. Circulation Research 2006, 98:351-360.
35. Wollert K.C. Growth-differentiation factor-15 in cardiovascular disease: from bench to bedside, and back. Basic Research in Cardiology 2007, 102:412-415.
36. Wollert K.C., Kempf T., Peter T., Olofsson S., James S., Johnston N., et al. Prognostic value of growth-differentiation factor-15 in patients with non-ST-evaluation acute coronary syndrome. Circulation 2007, 115:962-971.
37. Wollert K.C., Kempf T., Lagerqvist B., Lindahl B., Olofsson S., Allhoff T., et al. Growth differentiation factor 15 for risk stratification and selection of an invasive treatment strategy in non ST-elevation acute coronary syndrome. Circulation 2007, 116:1540-1548.
38. Bonaca M.P., Morrow D.A., Braunwald E., Cannon C.P., Jiang S., Breher S., et al. Growth differentiation factor-15 and risk of recurrent events in patients stabilized after acute coronary syndrome: observations from PROVE IT-TIMI 22. Arteriosclerosis, Thrombosis, and Vascular Biology 2011, 31:203-210.
39. Wollert K.C., Kempf T. Growth differentiation factor 15 in heart failure: an update. Current Heart Failure Reports 2012, 9:337-345.
40. Kempf T., Wollert K.C. Growth differentiation factor-15: a new biomarker in cardiovascular disease. Herz 2009, 34:594-599.
41. Xu X., Li Z., Gao W. Growth differentiation factor 15 in cardiovascular diseases: from bench to bedside. Biomarkers 2011, 16:466-475.
42. Kempf T., von Haehling S., Peter T., Allhoff T., Cicoira M., Doehner W., et al. Prognostic utility of growth differentiation factor-15 in patients with chronic heart failure. Journal of the American College of Cardiology 2007, 50:1054-1060.
43. Forejtnikovà H., Vieillevoye M., Zermati Y., Lambert M., Pellegrino R.M., Guihard S., et al. Transferrin receptor 2 is a component of the erythropoietin receptor complex and is required for efficient erythropoiesis. Blood 2010, 116:5357-5367.
44. Lakhal S., Talbot N.P., Crosby A., Stoepker C., Townsend A.R., Robbins P.A., et al. Regulation of growth differentiation factor 15 expression by intracellular iron. Blood 2009, 113:1555-1563.
45. Tanno T., Porayette P., Sripichai O., Noh S.J., Byrnes C., Bhupatiraju A., et al. Identification of TWSG1 as a second novel erythroid regulator of hepcidin expression in murine and human cells. Blood 2009, 114:181-186.
46. Casanovas G., Spasic M.V., Casu C., Rivella S., Strelau J., Unsicker K., et al. The murine growth differentiation factor 15 is not essential for systemic iron homeostasis in phlebotomized mice. Haematologica 2013, 98:444-447.
47. Santini V., Girelli D., Sanna A., Martinelli N., Duca L., Campostrini N., et al. Hepcidin levels and their determinants in different types of myelodysplastic syndromes. PLoS ONE 2011, 6:e23109.
48. Ding Q., Mracek T., Gonzalez-Muniesa P., Kos K., Wilding J., Trayhurn P., et al. Identification of macrophage inhibitory cytokine-1 in adipose tissue and its secretion as an adipokine by human adipocytes. Endocrinology 2009, 150:1688-1696.
49. Vila G., Riedl M., Anderwald C., Resl M., Handisurya A., Clodi M., et al. The relationship between insulin resistance and the cardiovascular biomarker growth differentiation factor-15 in obese patients. Clinical Chemistry 2011, 57:309-316.
50. Karczewska-Kupczewska M., Kowalska I., Nikolajuk A., Adamska A., Otziomek E., Gorska M., et al. Hyperinsulinemia acutely increases serum macrophage inhibitory cytokine-1 concentration in anorexia nervosa and obesity. Clinical Endocrinology 2012, 76:46-50.
51. Dostálová I., Roubícek T., Bártlová M., Mráz M., Lacinová Z., Haluzíková D., et al. Increased serum concentrations of macrophage inhibitory cytokine-1 in patients with obesity and type 2 diabetes mellitus: the influence of very low calorie diet. European Journal of Endocrinology 2009, 161:397-404.
52. Skipworth R.J., Deans D.A., Tan B.H., Sangster K., Paterson-Brown S., Brown D.A., et al. Plasma MIC-1 correlates with systemic inflammation but is not an independent determinant of nutritional status or survival in oesophago-gastric cancer. British Journal of Cancer 2010, 102:665-672.
53. Tsai V.W., Husaini Y., Manandhar R., Lee-Ng K.K., Zhang H.P., Harriott K., et al. Anorexia/cachexia of chronic diseases: a role for the TGF-β family cytokine MIC-1/GDF15. Journal of Cachexia Sarcopenia and Muscle 2012, 3:239-243.
54. Hsiao E.C., Koniaris L.G., Zimmers-Koniaris T., Sebald S.M., Huynh T.V., Lee S.J. Characterization of growth-differentiation factor 15, a transforming growth factor beta superfamily member induced following liver injury. Molecular and Cellular Biology 2000, 20:3742-3751.
55. Zimmers T.A., Jin X., Hsiao E.C., Perez E.A., Pierce R.H., Chavin K.D., et al. Growth differentiation factor-15: induction in liver injury through p53 and tumor necrosis factor-independent mechanisms. Journal of Surgical Research 2006, 130:45-51.
56. Zimmers T.A., Jin X., Gutierrez J.C., Acosta C., McKillop I.H., Pierce R.H., et al. Effect of in vivo loss of GDF-15 on hepatocellular carcinogenesis. Journal of Cancer Research and Clinical Oncology 2008, 134:753-759.
57. Schledzewski K., Géraud C., Arnold B., Wang S., Gröne H.J., Kempf T., et al. Deficiency of liver sinusoidal scavenger receptors stabilin-1 and -2 in mice causes glomerulofibrotic nephropathy via impaired hepatic clearance of noxious blood factors. Journal of Clinical Investigation 2011, 121:703-714.
58. Kim K.S., Baek S.J., Flake G.P., Loftin C.D., Calvo B.F., Eling T.E. Expression and regulation of nonsteroidal anti-inflammatory drug-activated gene (NAG-1) in human and mouse tissue. Gastroenterology 2002, 122:1388-1398.
59. Koopmann J., Buckhaults P., Brown D.A., Zahurak M.L., Sato N., Fukushima N., et al. Serum macrophage inhibitory cytokine 1 as a marker of pancreatic and other periampullary cancers. Clinical Cancer Research 2004, 10:2386-2392.
60. Wu Q., Jiang D., Chu H.W. Cigarette smoke induces growth differentiation factor 15 production in human lung epithelial cells: implication in mucin over-expression. Innate Immunity 2012, 18:617-626.
61. Lankeit M., Kempf T., Dellas C., Cuny M., Tapken H., Peter T., et al. Growth differentiation factor-15 for prognostic assessment of patients with acute pulmonary embolism. American Journal of Respiratory and Critical Care Medicine 2008, 177:1018-1025.
62. Nickel N., Kempf T., Tapken H., Tongers J., Laenger F., Lehmann U., et al. Growth differentiation factor-15 in idiopathic pulmonary arterial hypertension. American Journal of Respiratory and Critical Care Medicine 2008, 178:534-541.
63. Duong Van Huyen J.P., Cheval L., Bloch-Faure M., Belair M.F., Heudes D., Bruneval P., et al. GDF15 triggers homeostatic proliferation of acid-secreting collecting duct cells. Journal of the American Society of Nephrology 2008, 19:1965-1974.
64. Welsh-Bacic D., Nowik M., Kaissling B., Wagner C.A. Proliferation of acid-secretory cells in the kidney during adaptive remodelling of the collecting duct. PLoS ONE 2011, 6:e25240.
65. Breit S.N., Carrero J.J., Tsai V.W., Yagoutifam N., Luo W., Kuffner T., et al. Macrophage inhibitory cytokine-1 (MIC-1/GDF15) and mortality in end-stage renal disease. Nephrology, Dialysis, Transplantation 2012, 27:70-75.
66. Kaheki Y., Segawa T., Wu X.X., Kulkarni P., Dhir R., Getzenberg R.H. Down-regulation of macrophage inhibitory cytokine-1/prostate derived factor in benign prostatic hyperplasia. Prostate 2004, 59:351-356.
67. Welsh J.B., Sapinoso L.M., Su A.I., Kern S.G., Wang-Rodriguez J., Moskaluk C.A., et al. Analysis of gene expression identifies candidate markers and pharmacological targets in prostate cancer. Cancer Research 2001, 61:5974-5978.
68. Cheung P.K., Woolcock B., Adomat H., Sutcliffe M., Bainbridge T.C., Jones E.C., et al. Protein profiling of microdissected prostate tissue links growth differentiation factor 15 to prostate carcinogenesis. Cancer Research 2004, 64:5929-5933.
69. Rasiah K.K., Kench J.G., Gardiner-Garden M., Biankin A.V., Golovsky D., Brenner P.C., et al. Aberrant neuropeptide Y and macrophage inhibitory cytokine-1 expression are early events in prostate cancer development and are associated with poor prognosis. Cancer Epidemiology, Biomarkers and Prevention 2006, 15:711-716.
70. Karan D., Holzbeierlein J., Thrasher J.B. Macrophage inhibitory cytokine-1: possible bridge molecule of inflammation and prostate cancer. Cancer Research 2009, 69:2-5.
71. Liu T., Bauskin A.R., Zaunders J., Brown D.A., Pankhurst S., Russell P.J., et al. Macrophage inhibitory cytokine 1 reduces cell adhesion and induces apoptosis in prostate cancer cells. Cancer Research 2003, 63:5034-5040.
72. Bauskin A.R., Brown D.A., Junankar S., Rasiah K.K., Eggleton S., Hunter M., et al. The propeptide mediates formation of stromal stores of PROMIC-1: role in determining prostate cancer outcome. Cancer Research 2005, 65:2330-2336.
73. Soucek K., Slabáková E., Ovesná P., Malenovská A., Kozubík A., Hampl A. Growth/differentiation factor-15 is an abundant cytokine in human seminal plasma. Human Reproduction 2010, 25:2962-2971.
74. Seo S.K., Nam A., Jeon Y.E., Cho S., Choi Y.S., Lee B.S. Expression and possible role of non-steroidal anti-inflammatory drug-activated gene-1 (NAG-1) in the human endometrium and endometriosis. Human Reproduction 2010, 25:3043-3049.
75. Marjono A.B., Brown D.A., Horton K.E., Wallace E.M., Breit S.N., Manuelpillai U. Macrophage inhibitory cytokine-1 in gestational tissues and maternal serum in normal and pre-eclamptic pregnancy. Placenta 2003, 24:100-106.
76. Segerer S.E., Rieger L., Kapp M., Dombrowski Y., Müller N., Dietl J., et al. MIC-1 (a multifunctional modulator of dendritic cell phenotype and function) is produced by decidual stromal cells and trophoblasts. Human Reproduction 2012, 27:200-209.
77. Tong S., Marjono B., Brown D.A., Mulvey S., Breit S.N., Manuelpillai U., et al. Serum concentrations of macrophage inhibitory cytokine 1 (MIC 1) as a predictor of miscarriage. Lancet 2004, 363:129-130.
78. Tong S., Ngian G.L., Onwude J.L., Permezel M., Saglam B., Hay S., et al. Diagnostic accuracy of maternal serum macrophage inhibitory cytokine-1 and pregnancy-associated plasma protein-A at 6-10 weeks of gestation to predict miscarriage. Obstetrics and Gynecology 2012, 119:1000-1008.
79. Moore A.G., Brown D.A., Fairlie W.D., Bauskin A.R., Brown P.K., Munier M.L., et al. The transforming growth factor-ss superfamily cytokine macrophage inhibitory cytokine-1 is present in high concentrations in the serum of pregnant women. Journal of Clinical Endocrinology and Metabolism 2000, 85:4781-4788.
80. Hinoi E., Ochi H., Takarada T., Nakatani E., Iezaki T., Nakajima H., et al. Positive regulation of osteoclastic differentiation by growth differentiation factor 15 upregulated in osteocytic cells under hypoxia. Journal of Bone and Mineral Research 2012, 27:938-949.
81. Khan M.R., Donos N., Salih V., Brett P.M. The enhanced modulation of key bone matrix components by modified Titanium implant surfaces. Bone 2012, 50:1-8.
82. Vanhara P., Lincová E., Kozubík A., Jurdic P., Soucek K., Smarda J. Growth/differentiation factor-15 inhibits differentiation into osteoclasts - a novel factor involved in control of osteoclast differentiation. Differentiation 2009, 78:213-222.
83. Brown D.A., Moore J., Johnen H., Smeets T.J., Bauskin A.R., Kuffner T., et al. Serum macrophage inhibitory cytokine 1 in rheumatoid arthritis: a potential marker of erosive joint destruction. Arthritis and Rheumatism 2007, 56:753-764.
84. Strelau J., Sullivan A., Böttner M., Lingor P., Falkenstein E., Suter-Crazzolara C., et al. Growth/differentiation factor-15/macrophage inhibitory cytokine-1 is a novel trophic factor for midbrain dopaminergic neurons in vivo. Journal of Neuroscience 2000, 20:8597-8603.
85. Strelau J., Strzelczyk A., Rusu P., Bendner G., Wiese S., Diella F., et al. Progressive postnatal motoneuron loss in mice lacking GDF-15. Journal of Neuroscience 2009, 29:13640-13648.
86. Schindowski K., Von Bohlen und Halbach O., Strelau J., Ridder D.A., Herrmann O., Schober A., et al. Regulation of GDF-15, a distant TGF-β superfamily member, in a mouse model of cerebral ischemia. Cell and Tissue Research 2011, 343:399-409.
87. Charalambous P., Wang X., Thanos S., Schober A., Unsicker K. Regulation and effects of GDF-15 in the retina following optic nerve crush. Cell and Tissue Research 2013, [ahead of print]. 10.1007/s00441-013-1634-6.
88. Worthmann H., Kempf T., Widera C., Tryc A.B., Goldbecker A., Ma Y.T., et al. Growth differentiation factor 15 plasma levels and outcome after ischemic stroke. Cerebrovascular Diseases 2011, 32:72-78.
89. Gröschel K., Schnaudigel S., Edelmann F., Niehaus C.F., Weber-Krüger M., Haase B., et al. Growth-differentiation factor-15 and functional outcome after acute ischemic stroke. Journal of Neurology 2012, 259:1574-1579.
90. Mensching L., Börger A.K., Wang X., Charalambous P., Unsicker K., Haastert-Talini K. Local substitution of GDF-15 improves axonal and sensory recovery after peripheral nerve injury. Cell and Tissue Research 2012, 350:225-238.
91. Strelau J., Schmeer C., Peterziel H., Paech T., Herold-Mende C., Steiner H., et al. Expression and putative functions of GDF-15, a member of the TGF-β superfamily, in human glioma and glioblastoma cell lines. Cancer Letters 2008, 270:30-39.
92. Roth P., Junker M., Tritschler I., Mittelbronn M., Dombrowski Y., Breit S.N., et al. GDF-15 contributes to proliferation and immune escape of malignant gliomas. Clinical Cancer Research 2010, 16:3851-3859.
93. Ichikawa T., Suenaga Y., Koda T., Ozaki T., Nakagawara A. TAp63-dependent induction of growth differentiation factor 15 (GDF15) plays a critical role in the regulation of keratinocyte differentiation. Oncogene 2008, 27:409-420.
94. Akiyama M., Okano K., Fukada Y., Okano T. Macrophage inhibitory cytokine MIC-1 is upregulated by short-wavelength light in cultured normal human dermal fibroblasts. FEBS Letters 2009, 583:933-937.
95. Yanaba K., Asano Y., Tada Y., Sugaya M., Kadono T., Sato S. Clinical significance of serum growth differentiation factor-15 levels in systemic sclerosis: association with disease severity. Modern Rheumatology 2012, 22:668-675.
96. Yamashita T., Yoneta A., Hida T. Macrophage inhibitory cytokine-1: a new player in melanoma development. Journal of Investigative Dermatology 2009, 129:262-264.
97. Kluger H.M., Hoyt K., Bacchiocchi A., Mayer T., Kirsch J., Kluger Y., et al. Plasma markers for identifying patients with metastatic melanoma. Clinical Cancer Research 2011, 17:2417-2425.
98. Mauerer A., Roesch A., Hafner C., Stempfl T., Wild P., Meyer S., et al. Identification of new genes associated with melanoma. Experimental Dermatology 2011, 20:502-507.
99. Welsh J.B., Sapinoso L.M., Kern S.G., Brown D.A., Liu T., Bauskin A.R., et al. Large-scale delineation of secreted protein biomarkers overexpressed in cancer tissue and serum. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:3410-3415.
100. Bauskin A.R., Brown D.A., Kuffner T., Johnen H., Luo X.W., Hunter M., et al. Role of macrophage inhibitory cytokine-1 in tumorigenesis and diagnosis of cancer. Cancer Research 2006, 66:4983-4986.
101. Brown D.A., Ward R.L., Buckhaults P., Liu T., Romans K.E., Hawkins N.J., et al. MIC-1 serum level and genotype: associations with progress and prognosis of colorectal carcinoma. Clinical Cancer Research 2003, 9:2642-2650.
102. Brown D.A., Lindmark F., Stattin P., Bälter K., Adami H.O., Zheng S.L., et al. Macrophage inhibitory cytokine 1: a new prognostic marker in prostate cancer. Clinical Cancer Research 2009, 15:6658-6664.
103. Brown D.A., Hance K.W., Rogers C.J., Sansbury L.B., Albert P.S., Murphy G., et al. Serum macrophage inhibitory cytokine-1 (MIC-1/GDF15): a potential screening tool for the prevention of colon cancer?. Cancer Epidemiology, Biomarkers and Prevention 2012, 21:337-346.
104. Zhang L., Yang X., Pan H.Y., Zhou X.J., Li J., Chen W.T., et al. Expression of growth differentiation factor 15 is positively correlated with histopathological malignant grade and in vitro cell proliferation in oral squamous cell carcinoma. Oral Oncology 2009, 45:627-632.
105. Mimeault M., Batra S.K. Divergent molecular mechanisms underlying the pleiotropic functions of macrophage inhibitory cytokine-1 in cancer. Journal of Cellular Physiology 2010, 224:626-635.
106. Xue H., Lü B., Zhang J., Wu M., Huang Q., Wu Q., et al. Identification of serum biomarkers for colorectal cancer metastasis using a differential secretome approach. Journal of Proteome Research 2010, 9:545-555.
107. Costa V.L., Henrique R., Danielsen S.A., Duarte-Pereira S., Eknaes M., Skotheim R.I., et al. Three epigenetic biomarkers, GDF15, TMEFF2, and VIM, accurately predict bladder cancer from DNA-based analyses of urine samples. Clinical Cancer Research 2010, 16:5842-5851.
108. Wallin U., Glimelius B., Jirström K., Darmanis S., Nong R.Y., Pontén F., et al. Growth differentiation factor 15: a prognostic marker for recurrence in colorectal cancer. British Journal of Cancer 2011, 104:1619-1627.
109. Corre J., Labat E., Espagnolle N., Hébraud B., Avet-Loiseau H., Roussel M., et al. Bioactivity and prognostic significance of growth differentiation factor GDF15 secreted by bone marrow mesenchymal stem cells in multiple myeloma. Cancer Research 2012, 72:1395-1406.
110. Lee D.H., Yang Y., Lee S.J., Kim K.Y., Koo T.H., Shin S.M., et al. Macrophage inhibitory cytokine-1 induces the invasiveness of gastric cancer cells by up-regulating the urokinase-type plasminogen activator system. Cancer Research 2003, 63:4648-4655.
111. Park Y.J., Lee H., Lee J.H. Macrophage inhibitory cytokine-1 transactivates ErbB family receptors via the activation of Src in SK-BR-3 human breast cancer cells. BMB Reports 2010, 43:91-96.
112. Wollmann W., Goodman M.L., Bhat-Nakshatri P., Kishimoto H., Goulet R.J., Mehrotra S., et al. The macrophage inhibitory cytokine integrates AKT/PKB and MAP kinase signaling pathways in breast cancer cells. Carcinogenesis 2005, 26:900-907.
113. Yamaguchi K., Lee S.H., Eling T.E., Baek S.J. Identification of nonsteroidal anti-inflammatory drug-activated gene (NAG-1) as a novel downstream target of phosphatidylinositol 3-kinase/AKT/GSK-3beta pathway. Journal of Biological Chemistry 2004, 279:49617-49623.
114. Baek S.J., Kim J.S., Moore S.M., Lee S.H., Martinez J., Eling T.E. Cyclooxygenase inhibitors induce the expression of the tumor suppressor gene EGR-1, which results in the up-regulation of NAG-1, an antitumorigenic protein. Molecular Pharmacology 2005, 67:356-364.
115. Chenau J., Michelland S., de Fraipont F., Josserand V., Coll J.L., Favrot M.C., et al. The cell line secretome, a suitable tool for investigating proteins released in vivo by tumors: application to the study of p53-modulated proteins secreted in lung cancer cells. Journal of Proteome Research 2009, 8:4579-4591.
116. Cheng J.C., Chang H.M., Leung P.C. Wild-type p53 attenuates cancer cell motility by inducing growth differentiation factor-15 expression. Endocrinology 2011, 152:2987-2995.
117. Senapati S., Rachagani S., Chaudhary K., Johansson S.L., Singh R.K., Batra S.K. Overexpression of macrophage inhibitory cytokine-1 induces metastasis of human prostate cancer cells through the FAK-RhoA signaling pathway. Oncogene 2010, 29:1293-1302.
118. Giang Ho T.T., Stultiens A., Dubail J., Lapière C.M., Nusgens B.V., Colige A.C., et al. RhoGDIα-dependent balance between RhoA and RhoC is a key regulator of cancer cell tumorigenesis. Molecular Biology of the Cell 2011, 22:3263-3275.
119. Tzeh Gung A.Y., Kondo H., Aoki T., Hirono I. Growth differentiation factor 15, a novel acute phase response gene in Japanese flounder, Paralichthys olivaceus. Fish and Shellfish Immunology 2009, 26:230-234.
120. Wong E.S., Morgenstern D., Mofiz E., Gombert S., Morris K.M., Temple-Smith P., et al. Proteomics and deep sequencing comparison of seasonally active venom glands in the platypus reveals novel venom peptides and distinct expression profiles. Molecular and Cellular Proteomics 2012, 11:1354-1364.