EGF receptor-mediated, c-Src-dependent, activation of Stat5b is downregulated in mitogenically responsive hepatocytes

Journal of Cellular Physiology

Volumn 196, Issue 1, 2003, Pages 113-123

  Guren, Tormod K ^a   Ødegård, John ^a   Abrahamsen, Hilde ^a   Thoresen, G Hege ^a   Susa, Mira ^b   Andersson, Yvonne ^c   Østby, Eva ^a   Christoffersen, Thoralf ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b NOVARTIS PHARMA AG   (Switzerland)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CGP 77675; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH HORMONE; MITOGEN ACTIVATED PROTEIN KINASE; PROLACTIN; PROTEIN KINASE INHIBITOR; PROTEIN SHC; PROTEIN TYROSINE KINASE; STAT5B PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ASSAY; CELL CYCLE G1 PHASE; CELL DENSITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA BINDING; DNA SYNTHESIS; DOWN REGULATION; HORMONAL REGULATION; HORMONE ACTION; IMMUNOPRECIPITATION; LIVER CELL; LIVER CELL CULTURE; MALE; MITOGENICITY; MONOLAYER CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIVISION; CELLS, CULTURED; DNA; DNA-BINDING PROTEINS; DOWN-REGULATION; EPIDERMAL GROWTH FACTOR; GROWTH HORMONE; HEPATOCYTES; MALE; MILK PROTEINS; MITOGENS; PHOSPHORYLATION; PHOSPHOSERINE; PHOSPHOTYROSINE; PROLACTIN; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS PP60(C-SRC); PYRIMIDINES; PYRROLES; RATS; RATS, WISTAR; RECEPTOR, EPIDERMAL GROWTH FACTOR; STAT5 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR ALPHA;

EID: 0038283996     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.10282     Document Type: Article

References (74)

1. Abram CL, Courtneidge SA. 2000. Src family tyrosine kinases and growth factor signaling. Exp Cell Res 254:1-13.
2. Bartoli M, Gu X, Tsai NT, Venema RC, Brooks SE, Marrero MB, Caldwell RB. 2000. Vascular endothelial growth factor activates STAT proteins in aortic endothelial cells. J Biol Chem 275:33189-33192.
3. Biscardi JS, Tice DA, Parsons SJ. 1999. c-Src, receptor tyrosine kinases, and human cancer. Adv Cancer Res 76:61-119.
4. Bowman T, Garcia R, Turkson J, Jove R. 2000. STATs in oncogenesis. Oncogene 19:2474-2488.
5. Bromberg J, Darnell JE, Jr. 2000. The role of STATs in transcriptional control and their impact on cellular function. Oncogene 19:2468-2473.
6. Bromberg JF, Fan Z, Brown C, Mendelsohn J, Darnell JE, Jr. 1998a. Epidermal growth factor-induced growth inhibition requires Stat1 activation. Cell Growth Differ 9:505-512.
7. Bromberg JF, Horvath CM, Besser D, Lathem WW, Darnell JE, Jr. 1998b. Stat3 activation is required for cellular transformation by v-src. Mol Cell Biol 18:2553-2558.
8. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, Darnell JE, Jr. 1999. Stat3 as an oncogene. Cell 98:295-303.
9. Chang L, Karin M. 2001. Mammalian MAP kinase signalling cascades. Nature 410:37-40.
10. Chin YE, Kitagawa M, Su WC, You ZH, Iwamoto Y, Fu XY. 1996. Cell growth arrest and induction of cyclin-dependent kinase inhibitor p21 WAF1/CIP1 mediated by STAT1. Science 272:719-722.
11. Christoffersen T, Refsnes M, Bronstad GO, Ostby E, Huse J, Haffner F, Sand TE, Hunt NH, Sonne O. 1984. Changes in hormone responsiveness and cyclic AMP metabolism in rat hepatocytes during primary culture and effects of supplementing the medium with insulin and dexamethasone. Eur J Biochem 138:217-226.
12. Christoffersen T, Thoresen GH, Dajani OF, Melien Ø, Guren TK, Refsnes M, Sandnes D. 2000. Mechanisms of hepatocyte growth regulation by hormones and growth factors. In: Berry MN, Edwards AM, editors. The Hepatocyte Review. Dordrecht/Boston/London: Kluwer Academic Publishers. pp 209-246.
13. Dajani OF, Sandnes D, Melien O, Rezvani F, Nilssen LS, Thoresen GH, Christoffersen T. 1999. The role of diacylglycerol in hormonal induction of S phase in hepatocytes: The diacylglycerol-dependent protein kinase C pathway is not activated by epidermal growth factor (EGF), but is involved in the enhancement of responsiveness to EGF by vasopressin, angiotensin II, and norepinephrine. J Cell Physiol 180:203-214.
14. Darnell JE. 1997. STATs and gene regulation. Science 277:1630-1635.
15. Decker T, Kovarik P. 2000. Serine phosphorylation of STATs. Oncogene 19:2628-2637.
16. Demoulin JB, Uyttenhove C, Lejeune D, Mui A, Groner B, Renauld JC. 2000. STAT5 activation is required for interleukin-9-dependent growth and transformation of lymphoid cells. Cancer Res 60:3971-3977.
17. Edwards AM, Michalopoulos GK. 2000. Conditions for growth of hepatocytes in culture. In: Berry MN, Edwards AM, editors. The Hepatocyte Review. Dordrecht/Boston/London: Kluwer Academic Publishers. pp 73-96.
18. Garcia R, Bowman TL, Niu G, Yu H, Minton S, Muro-Cacho CA, Cox CE, Falcone R, Fairclough R, Parsons S, Laudano A, Gazit A, Levitzki A, Kraker A, Jove R. 2001. Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 20:2499-2513.
19. Gesbert F, Griffin JD. 2000. Bcr/Abl activates transcription of the Bcl-X gene through STAT5. Blood 96:2269-2276.
20. Grimley PM, Dong F, Rui H. 1999. Stat5a and Stat5b: Fraternal twins of signal transduction and transcriptional activation. Cytokine Growth Factor Rev 10:131-157.
21. Groner B, Gouilleux F. 1995. Prolactin-mediated gene activation in mammary epithelial cells. Curr Opin Genet Dev 5:587-594.
22. Guren TK, Thoresen GH, Dajani OF, Taraldsrud E, Moberg ER, Christoffersen T. 1996. Epidermal growth factor behaves as a partial agonist in hepatocytes: Effects on DNA synthesis in primary culture and competition with transforming growth factor alpha. Growth Factors 13:171-179.
23. Guren TK, Abrahamsen H, Thoresen GH, Babaie E, Berg T, Christoffersen T. 1999. EGF-induced activation of Stat1, Stat3, and Stat5b is unrelated to the stimulation of DNA synthesis in cultured hepatocytes. Biochem Biophys Res Commun 258:565-571.
24. Herrington J, Smit LS, Schwartz J, Carter-Su C. 2000. The role of STAT proteins in growth hormone signaling. Oncogene 19:2585-2597.
25. Humphreys RC, Hennighausen L. 1999. Signal transducer and activator of transcription 5a influences mammary epithelial cell survival and tumorigenesis. Cell Growth Differ 10:685-694.
26. Ihle JN. 2001. The Stat family in cytokine signaling. Curr Opin Cell Biol 13:211-217.
27. Kazansky AV, Rosen JM. 2001. Signal transducers and activators of transcription 5B potentiates v-Src-mediated transformation of NIH-3T3 cells. Cell Growth Differ 12:1-7.
28. Kazansky AV, Kabotyanski EB, Wyszomierski SL, Mancini MA, Rosen JM. 1999. Differential effects of prolactin and src/abl kinases on the nuclear translocation of STAT5B and STAT5A. J Biol Chem 274:22484-22492.
29. Kirken RA, Malabarba MG, Xu J, Liu X, Farrar WL, Hennighausen L, Larner AC, Grimley PM, Rui H. 1997. Prolactin stimulates serine/tyrosine phosphorylation and formation of heterocomplexes of multiple Stat5 isoforms in Nb2 lymphocytes. J Biol Chem 272:14098-14103.
30. Kloth MT, Catling AD, Silva CM. 2002. Novel activation of STAT5b in response to epidermal growth factor. J Biol Chem 277:8693-8701.
31. Leaman DW, Leung S, Li X, Stark GR. 1996. Regulation of STAT-dependent pathways by growth factors and cytokines. FASEB J 10:1578-1588.
32. Lin JX, Leonard WJ. 2000. The role of Stat5a and Stat5b in signaling by IL-2 family cytokines. Oncogene 19:2566-2576.
33. Loyer P, Cariou S, Glaise D, Bilodeau M, Baffet G, Guguen-Guillouzo C. 1996. Growth factor dependence of progression through G1 and S phases of adult rat hepatocytes in vitro. Evidence of a mitogen restriction point in mid-late G1. J Biol Chem 271:11484-11492.
34. Luetteke NC, Qiu TH, Fenton SE, Troyer KL, Riedel RF, Chang A, Lee DC. 1999. Targeted inactivation of the EGF and amphiregulin genes reveals distinct roles for EGF receptor ligands in mouse mammary gland development. Development 126:2739-2750.
35. Matsumura I, Ishikawa J, Nakajima K, Oritani K, Tomiyama Y, Miyagawa J, Kato T, Miyazaki H, Matsuzawa Y, Kanakura Y. 1997. Thrombopoietin-induced differentiation of a human megakaryoblastic leukemia cell line, CMK, involves transcriptional activation of p21(WAF1/Cip1) by STAT5. Mol Cell Biol 17:2933-2943.
36. Matsumura I, Kitamura T, Wakao H, Tanaka H, Hashimoto K, Albanese C, Downward J, Pestell RG, Kanakura Y. 1999. Transcriptional regulation of the cyclin D1 promoter by STAT5: Its involvement in cytokine-dependent growth of hematopoietic cells. EMBO J 18:1367-1377.
37. Missbach M, Jeschke M, Feyen J, Muller K, Glatt M, Green J, Susa M. 1999. A novel inhibitor of the tyrosine kinase Src suppresses phosphorylation of its major cellular substrates and reduces bone resorption in vitro and in rodent models in vivo. Bone 24:437-449.
38. Miyoshi K, Shillingford JM, Smith GH, Grimm SL, Wagner KU, Oka T, Rosen JM, Robinson GW, Hennighausen L. 2001. Signal transducer and activator of transcription (Stat) 5 controls the proliferation and differentiation of mammary alveolar epithelium. J Cell Biol 155:531-542.
39. Moriggl R, Topham DJ, Teglund S, Sexl V, McKay C, Wang D, Hoffmeyer A, van Deursen J, Sangster MY, Bunting KD, Grosveld GC, Ihle JN. 1999. Stat5 is required for IL-2-induced cell cycle progression of peripheral T cells. Immunity 10:249-259.
40. Musallam L, Ethier C, Haddad PS, Bilodeau M. 2001. Role of EGF receptor tyrosine kinase activity in antiapoptotic effect of EGF on mouse hepatocytes. Am J Physiol Gastrointest Liver Physiol 280: G1360-G1369.
41. Nakamura T, Yoshimoto K, Nakayama Y, Tomita Y, Ichihara A. 1983. Reciprocal modulation of growth and differentiated functions of mature rat hepatocytes in primary culture by cell-cell contact and cell membranes. Proc Natl Acad Sci USA 80:7229-7233.
42. Nosaka T, Kawashima T, Misawa K, Ikuta K, Mui AL, Kitamura T. 1999. STAT5 as a molecular regulator of proliferation, differentiation, and apoptosis in hematopoietic cells. EMBO J 18:4754-4765.
43. Olayioye MA, Beuvink I, Horsch K, Daly JM, Hynes NE. 1999. ErbB receptor-induced activation of stat transcription factors is mediated by Src tyrosine kinases. J Biol Chem 274:17209-17218.
44. Olayioye MA, Neve RM, Lane HA, Hynes NE. 2000. The ErbB signaling network: Receptor heterodimerization in development and cancer. EMBO J 19:3159-3167.
45. Park SH, Yamashita H, Rui H, Waxman DJ. 2001. Serine phosphorylation of GH-activated signal transducer and activator of transcription 5a (STAT5a) and STAT5b: Impact on STAT5 transcriptional activity. Mol Endocrinol 15:2157-2171.
46. Paukku K, Valgeirsdottir S, Saharinen P, Bergman M, Heldin CH, Silvennoinen O. 2000. Platelet-derived growth factor (PDGF)-induced activation of signal transducer and activator of transcription (Stat) 5 is mediated by PDGF beta-receptor and is not dependent on c-src, fyn, jak1, or jak2 kinases. Biochem J 345:759-766.
47. Quelle FW, Wang D, Nosaka T, Thierfelder WE, Stravopodis D, Weinstein Y, Ihle JN. 1996. Erythropoietin induces activation of Stat5 through association with specific tyrosines on the receptor that are not required for a mitogenic response. Mol Cell Biol 16:1622-1631.
48. Reddy EP, Korapati A, Chaturvedi P, Rane S. 2000. IL-3 signaling and the role of Src kinases, JAKs, and STATs: A covert liaison unveiled. Oncogene 19:2532-2547.
49. Refsnes M, Thoresen GH, Dajani OF, Christoffersen T. 1994. Stimulation of hepatocyte DNA synthesis by prostaglandin E2 and prostaglandin F2 alpha: Additivity with the effect of norepinephrine, and synergism with epidermal growth factor. J Cell Physiol 159:35-40.
50. Richer JK, Lange CA, Manning NG, Owen G, Powell R, Horwitz KB. 1998. Convergence of progesterone with growth factor and cytokine signaling in breast cancer. Progesterone receptors regulate signal transducers and activators of transcription expression and activity. J Biol Chem 273:31317-31326.
51. Ruff-Jamison S, Chen K, Cohen S. 1993. Induction by EGF and interferon-gamma of tyrosine phosphorylated DNA binding proteins in mouse liver nuclei. Science 261:1733-1736.
52. Ruff-Jamison S, Zhong Z, Wen Z, Chen K, Darnell JE, Jr., Cohen S. 1994. Epidermal growth factor and lipopolysaccharide activate Stat3 transcription factor in mouse liver. J Biol Chem 269:21933-21935.
53. Ruff-Jamison S, Chen K, Cohen S. 1995. Epidermal growth factor induces the tyrosine phosphorylation and nuclear translocation of Stat 5 in mouse liver. Proc Natl Acad Sci USA 92:4215-4218.
54. Runge D, Runge DM, Drenning SD, Bowen WC, Jr., Grandis JR, Michalopoulos GK. 1998. Growth and differentiation of rat hepatocytes: Changes in transcription factors HNF-3, HNF-4, STAT-3, and STAT-5. Biochem Biophys Res Commun 250:762-768.
55. Sachsenmaier C, Sadowski HB, Cooper JA. 1999. STAT activation by the PDGF receptor requires juxtamembrane phosphorylation sites but not Src tyrosine kinase activation. Oncogene 18:3583-3592.
56. Sand TE, Christoffersen T. 1987. Temporal requirement for epidermal growth factor and insulin in the stimulation of hepatocyte DNA synthesis. J Cell Physiol 131:141-148.
57. Schlessinger J. 2000. Cell signaling by receptor tyrosine kinases. Cell 103:211-225.
58. Seglen PO. 1976. Preparation of isolated rat liver cells. Methods Cell Biol 13:29-83.
59. Sillaber C, Gesbert F, Frank DA, Sattler M, Griffin JD. 2000. STAT5 activation contributes to growth and viability in Bcr/Abl-transformed cells. Blood 95:2118-2125.
60. Socolovsky M, Fallon AE, Wang S, Brugnara C, Lodish HF. 1999. Fetal anemia and apoptosis of red cell progenitors in Stat5a-/-5b-/-mice: A direct role for Stat5 in Bcl-X(L) induction. Cell 98:181-191.
61. Song JI, Rubin Grandis J. 2000. STAT signaling in head and neck cancer. Oncogene 19:2489-2495.
62. Susa M, Missbach M, Green J. 2000. Src inhibitors: Drugs for the treatment of osteoporosis, cancer, or both? Trends Pharmacol Sci 21:489-495.
63. Talarmin H, Rescan C, Cariou S, Glaise D, Zanninelli G, Bilodeau M, Loyer P, Guguen-Guillouzo C, Baffet G. 1999. The mitogen-activated protein kinase kinase/extracellular signal-regulated kinase cascade activation is a key signalling pathway involved in the regulation of G(1) phase progression in proliferating hepatocytes. Mol Cell Biol 19:6003-6011.
64. Taub R. 1996. Liver regeneration 4: Transcriptional control of liver regeneration. FASEB J 10:413-427.
65. Thoresen GH, Guren TK, Sandnes D, Peak M, Agius L, Christoffersen T. 1998. Response to transforming growth factor alpha (TGFalpha) and epidermal growth factor (EGF) in hepatocytes: Lower EGF receptor affinity of TGFalpha is associated with more sustained activation of p42/p44 mitogen-activated protein kinase and greater efficacy in stimulation of DNA synthesis. J Cell Physiol 175:10-18.
66. Thoresen GH, Guren TK, Christoffersen T. 2003. Role of ERK, p38, and P13-kinase in EGF receptor-mediated mitogenic signaling in cultured rat hepatocytes: Requirement for sustained ERK activation. Cell Physiol Biochem, in press.
67. Turkson J, Bowman T, Garcia R, Caldenhoven E, de Groot RP, Jove R. 1998. Stat3 activation by Src induces specific gene regulation and is required for cell transformation. Mol Cell Biol 18:2545-2552.
68. Valgeirsdottir S, Paukku K, Silvennoinen O, Heldin CH, Claesson-Welsh L. 1998. Activation of Stat5 by platelet-derived growth factor (PDGF) is dependent on phosphorylation sites in PDGF beta-receptor juxtamembrane and kinase insert domains. Oncogene 16:505-515.
69. van der Geer P, Hunter T, Lindberg RA. 1994. Receptor protein-tyrosine kinases and their signal transduction pathways. Annu Rev Cell Biol 10:251-337.
70. Wakao H, Gouilleux F, Groner B. 1994. Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J 13:2182-2191.
71. Wang Y, Ripperger J, Fey GH, Samols D, Kordula T, Wetzler M, Van Etten RA, Baumann H. 1999. Modulation of hepatic acute phase gene expression by epidermal growth factor and Src protein tyrosine kinases in murine and human hepatic cells. Hepatology 30:682-697.
72. Watson CJ, Miller WR. 1995. Elevated levels of members of the STAT family of transcription factors in breast carcinoma nuclear extracts. Br J Cancer 71:840-844.
73. Wollenberg GK, Harris L, Farber E, Hayes MA. 1989. Inverse relationship between epidermal growth factor induced proliferation and expression of high affinity surface epidermal growth factor receptors in rat hepatocytes. Lab Invest 60:254-259.
74. Yamashita H, Xu J, Erwin RA, Farrar WL, Kirken RA, Rui H. 1998. Differential control of the phosphorylation state of prolinejuxtaposed serine residues Ser725 of Stat5a and Ser730 of Stat5b in prolactin-sensitive cells. J Biol Chem 273:30218-30224.