Oncogenic MST1R activity in pancreatic and gastric cancer represents a valid target of HSP90 inhibitors

Anticancer Research

Volumn 32, Issue 2, 2012, Pages 427-437

  Moser, Christian ^a   Lang, Sven A ^a   Hackl, Christina ^a   Zhang, Hong ^b   Lundgren, Karen ^b   Hong, Victor ^b   McKenzie, Andres ^b   Weber, Bernhard ^c   Park, Jung S ^d   Schlitt, Hans J ^a   Geissler, Edward K ^a   Jung, Young D ^d   Stoeltzing, Oliver ^a,e  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^b BIOGEN   (United States)

^c UNIVERSITY OF REGENSBURG   (Germany)

^d Chonnam National University Medical School   (South Korea)

^e UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Gastric cancer; HPAF II cells; HSP90; L3,6 pl cells; MST1R; Pancreatic cancer; TMK 1 cells

Indexed keywords

HEAT SHOCK PROTEIN 90 INHIBITOR; LUCIFERASE; MACROPHAGE ACTIVATING FACTOR; PROTEIN TYROSINE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL GROWTH; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH CANCER; TRANSCRIPTION REGULATION; TUMOR GROWTH; WESTERN BLOTTING;

ANIMALS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; HEPATOCYTE GROWTH FACTOR; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MOLECULAR TARGETED THERAPY; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS;

EID: 84863151061     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (39)

1. Iwama A, Yamaguchi N and Suda T: STK/RON receptor tyrosine kinase mediates both apoptotic and growth signals via the multifunctional docking site conserved among the HGF receptor family. EMBO J 15(21): 5866-5875, 1996. (Pubitemid 26375508)
2. Peace BE, Hughes MJ, Degen SJ and Waltz SE: Point mutations and overexpression of Ron induce transformation, tumor formation, and metastasis. Oncogene 20(43): 6142-6151, 2001. (Pubitemid 32964426)
3. Wang MH, Dlugosz AA, Sun Y, Suda T, Skeel A and Leonard EJ: Macrophage-stimulating protein induces proliferation and migration of murine keratinocytes. Exp Cell Res 226(1): 39-46, 1996. (Pubitemid 26238925)
4. Wang MH, Wang D and Chen YQ: Oncogenic and invasive potentials of human macrophage-stimulating protein receptor, the RON receptor tyrosine kinase. Carcinogenesis 24(8): 1291-1300, 2003. (Pubitemid 37038819)
5. Camp ER, Liu W, Fan F, Yang A, Somcio R and Ellis LM: RON, a tyrosine kinase receptor involved in tumor progression and metastasis. Ann Surg Oncol 12(4): 273-281, 2005. (Pubitemid 40616491)
6. Chen YQ, Zhou YQ, Angeloni D, Kurtz AL, Qiang XZ and Wang MH: Overexpression and activation of the RON receptor tyrosine kinase in a panel of human colorectal carcinoma cell lines. Exp Cell Res 261(1): 229-238, 2000.
7. Maggiora P, Lorenzato A, Fracchioli S, Costa B, Castagnaro M, Arisio R, Katsaros D, Massobrio M, Comoglio PM and Flavia Di Renzo M: The RON and MET oncogenes are co-expressed in human ovarian carcinomas and cooperate in activating invasiveness. Exp Cell Res 288(2): 382-389, 2003. (Pubitemid 36959954)
8. Maggiora P, Marchio S, Stella MC, Giai M, Belfiore A, De Bortoli M, Di Renzo MF, Costantino A, Sismondi P and Comoglio PM: Overexpression of the RON gene in human breast carcinoma. Oncogene 16(22): 2927-2933, 1998. (Pubitemid 28383277)
9. Thomas RM, Toney K, Fenoglio-Preiser C, Revelo-Penafiel MP, Hingorani SR, Tuveson DA, Waltz SE and Lowy AM: The RON receptor tyrosine kinase mediates oncogenic phenotypes in pancreatic cancer cells and is increasingly expressed during pancreatic cancer progression. Cancer Res 67(13): 6075-6082, 2007. (Pubitemid 47037486)
10. Camp ER, Yang A, Gray MJ, Fan F, Hamilton SR, Evans DB, Hooper AT, Pereira DS, Hicklin DJ and Ellis LM: Tyrosine kinase receptor RON in human pancreatic cancer: expression, function, and validation as a target. Cancer 109(6): 1030-1039, 2007. (Pubitemid 46435380)
11. Zhou D, Pan G, Zheng C, Zheng J, Yian L and Teng X: Expression of the RON receptor tyrosine kinase and its association with gastric carcinoma versus normal gastric tissues. BMC Cancer 8: 353-359, 2008.
12. Isaacs JS, Xu W and Neckers L: Heat-shock protein 90 as a molecular target for cancer therapeutics. Cancer Cell 3(3): 213-217, 2003. (Pubitemid 37443877)
13. Neckers L: Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol Med 8(4 Suppl): 55-61, 2002.
14. Zhang H and Burrows F: Targeting multiple signal transduction pathways through inhibition of Hsp90. J Mol Med 82(8): 488-499, 2004. (Pubitemid 39149859)
15. Lang SA, Klein D, Moser C, Gaumann A, Glockzin G, Dahlke MH, Dietmaier W, Bolder U, Schlitt HJ, Geissler EK and Stoeltzing O: Inhibition of heat-shock protein 90 impairs epidermal growth factor-mediated signaling in gastric cancer cells and reduces tumor growth and vascularization in vivo. Mol Cancer Ther 6(3): 1123-1132, 2007. (Pubitemid 46554583)
16. Lang SA, Moser C, Gaumann A, Klein D, Glockzin G, Popp FC, Dahlke MH, Piso P, Schlitt HJ, Geissler EK and Stoeltzing O: Targeting heat-shock protein 90 in pancreatic cancer impairs insulin-like growth factor-I receptor signaling, disrupts an interleukin-6/signal-transducer and activator of transcription-3/hypoxia-inducible factor-1 alpha autocrine loop, and reduces orthotopic tumor growth. Clin Cancer Res 13(21): 6459-6468, 2007. (Pubitemid 350075036)
17. Germano S, Barberis D, Santoro MM, Penengo L, Citri A, Yarden Y and Gaudino G: Geldanamycins trigger a novel Ron degradative pathway, hampering oncogenic signaling. J Biol Chem 281(31): 21710-21719, 2006. (Pubitemid 44181874)
18. Santoro MM, Penengo L, Minetto M, Orecchia S, Cilli M and Gaudino G: Point mutations in the tyrosine kinase domain release the oncogenic and metastatic potential of the Ron receptor. Oncogene 17(6): 741-749, 1998. (Pubitemid 28412495)
19. Santoro MM, Penengo L, Orecchia S, Cilli M and Gaudino G: The Ron oncogenic activity induced by the MEN2B-like substitution overcomes the requirement for the multifunctional docking site. Oncogene 19(45): 5208-5211, 2000.
20. Stoeltzing O, Liu W, Reinmuth N, Fan F, Parikh AA, Bucana CD, Evans DB, Semenza GL and Ellis LM: Regulation of hypoxia-inducible factor-1alpha, vascular endothelial growth factor, and angiogenesis by an insulin-like growth factor-I receptor autocrine loop in human pancreatic cancer. Am J Pathol 163(3): 1001-1011, 2003. (Pubitemid 37040136)
21. Parikh AA, Liu WB, Fan F, Stoeltzing O, Reinmuth N, Bruns CJ, Bucana CD, Evans DB and Ellis LM: Expression and regulation of the novel vascular endothelial growth factor receptor neuropilin-1 by epidermal growth factor in human pancreatic carcinoma. Cancer 98(4): 720-729, 2003. (Pubitemid 36959267)
22. Park JS, Park JH, Khoi PN, Joo YE and Jung YD: MSP-induced RON activation upregulates uPAR expression and cell invasiveness via MAPK, AP-1 and NF-κB signals in gastric cancer cells. Carcinogenesis 32(2): 175-181, 2011.
23. Park JS, Park JH, Lee S, Joo YE and Jung YD: Small interfering RNA targeting of Recepteur d'Origine Nantais induces apoptosis via modulation of nuclear factor-kappaB and Bcl-2 family in gastric cancer cells. Oncol Rep 24(3): 709-714, 2010.
24. Shin SY, Kim JH, Baker A, Lim Y and Lee YH: Transcription factor Egr-1 is essential for maximal matrix metalloproteinase-9 transcription by tumor necrosis factor alpha. Mol Cancer Res 8(4): 507-519, 2010.
25. Lang SA, Moser C, Fichtner-Feigl S, Schachtschneider P, Hellerbrand C, Schmitz V, Schlitt HJ, Geissler EK and Stoeltzing O: Targeting heat-shock protein 90 improves efficacy of rapamycin in a model of hepatocellular carcinoma in mice. Hepatology 49(2): 523-532, 2009.
26. Workman P, Balmain A, Hickman JA, McNally NJ, Rohas AM, Mitchison NA, Pierrepoint CG, Raymond R, Rowlatt C, Stephens TC, Wallace J and Straughan DW: UKCCCR guidelines for the welfare of animals in experimental neoplasia. Lab Anim 22(3): 195-201, 1988.
27. Stoeltzing O, McCarty MF, Wey JS, Fan F, Liu W, Belcheva A, Bucana CD, Semenza GL and Ellis LM: Role of hypoxia-inducible factor-1 alpha in gastric cancer cell growth, angiogenesis, and vessel maturation. J Natl Cancer Inst 96(12): 946-956, 2004. (Pubitemid 38868141)
28. Sanderson S, Valenti M, Gowan S, Patterson L, Ahmad Z, Workman P and Eccles SA: Benzoquinone ansamycin heatshock protein 90 inhibitors modulate multiple functions required for tumor angiogenesis. Mol Cancer Ther 5(3): 522-532, 2006.
29. Burger AM, Fiebig HH, Stinson SF and Sausville EA: 17-(Allylamino)-17- demefhoxygeIdanamycin activity in human melanoma models. Anticancer Drugs 15(4): 377-387. 2004. (Pubitemid 38526763)
30. Yin X, Zhang H, Burrows F, Zhang L and Shores CG: Potent activity of a novel dimeric heat-shock protein 90 inhibitor against head and neck squamous cell carcinoma in vitro and in vivo. Clin Cancer Res 11(10): 3889-3896, 2005. (Pubitemid 40685610)
31. Bardella C, Costa B, Maggiora P, Patane S, Olivero M, Ranzani GN, De Bortoli M, Comoglio PM and Di Renzo MF: Truncated RON tyrosine kinase drives tumor cell progression and abrogates cell cell adhesion through E-cadherin transcriptional repression. Cancer Res 64(15): 5154-5161, 2004. (Pubitemid 39006533)
32. Lin HS, Berry GJ, Fee WE Jr. Terris DJ and Sun Z: Identification of tyrosine kinases overexpressed in head and neck cancer. Arch Otolaryngol Head Neck Surg 130(3): 311-316, 2004. (Pubitemid 38314230)
33. Willett CG, Wang MH, Emanuel RL, Graham SA, Smith DI, Shridhar V, Sugarbaker DJ and Sunday ME: Macrophage-stimulating protein and its receptor in non-small cell lung tumors: induction of receptor tyrosine phosphorylation and cell migration. Am J Respir Cell Mol Biol 18(4): 489-496, 1998. (Pubitemid 128353622)
34. Wang MH, Kurtz AL and Chen Y: Identification of a novel splicing product of the RON receptor tyrosine kinase in human colorectal carcinoma cells. Carcinogenesis 21(8): 1507-1512, 2000. (Pubitemid 30603978)
35. Li BQ, Wang MH, Kung HF, Ronsin C, Breathnach R, Leonard EJ and Kamata T: Macrophage-stimulating protein activates Ras by both activation and translocation of SOS nucleotide exchange factor. Biochem Biophys Res Commun 216(1): 110-118, 1995.
36. Wang MH, Montero-Julian FA, Dauny I and Leonard EJ: Requirement of phosphatidylinositol-3 kinase for epithelial cell migration activated by human macrophage stimulating protein. Oncogene 13(10): 2167-2175, 1996. (Pubitemid 26411567)
37. Thomas RM, Jaquish DV, French RP and Lowy AM: The RON tyrosine kinase receptor regulates vascular endothelial growth factor production in pancreatic cancer cells. Pancreas 39(3): 301-307, 2010.
38. O'Toole JM, Rabenau KE, Burns K, Lu D, Mangalampalli V, Balderes P, Covino N, Bassi R, Prewett M, Gottfredsen KJ, Thobe MN, Cheng Y, Li Y, Hicklin DJ, Zhu Z, Waltz SE, Hayman MJ, Ludwig DL and Pereira DS: Therapeutic implications of a human neutralizing antibody to the macrophage-stimulating protein receptor tyrosine kinase (RON), a c-MET family member. Cancer Res 66(18): 9162-9170, 2006. (Pubitemid 44521136)
39. Logan-Collins J, Thomas RM, Yu P, Jaquish D, Mose E, French R, Stuart W, McClaine R, Aronow B, Hoffman RM, Waltz SE and Lowy AM: Silencing of RON receptor signaling promotes apoptosis and gemcitabine sensitivity in pancreatic cancers. Cancer Res 70(3): 1130-1140, 2010.