Midkine: A Novel Prognostic Biomarker for Cancer
Abstract
:1. Introduction
2. Midkine
2.1. Molecular Genetic Characterization
2.2. Mechanism of Action
2.3. Biological Significance
3. Midkine as a Novel Tumor Marker
3.1. Neuroblastoma
3.2. Hepatocellular Carcinoma
3.3. Esophageal Squamous Cell Carcinoma
3.4. Oral Squamous Cell Carcinoma
3.5. Breast Cancer
3.6. Pancreatic Cancer
4. Conclusions
Acknowledgements
References
- Kadomatsu, K.; Tomomura, M.; Muramatsu, T. cDNA cloning and sequencing of a new gene intensely expressed in early differentiation stages of embryonal carcinoma cells and in mid-gestation period of mouse embryogenesis. Biochem. Biophys. Res. Commun. 1988, 151, 1312–1318. [Google Scholar] [CrossRef]
- Kadomatsu, K.; Huang, R.P.; Suganuma, T.; Murata, F.; Muramatsu, T. A retinoic acid responsive gene MK found in the teratocarcinoma system is expressed in spatially and temporally controlled manner during mouse embryogenesis. J. Cell Biol. 1990, 110, 607–616. [Google Scholar] [CrossRef]
- Muramatsu, T. Midkine and pleiotrophin: two related proteins involved in development, survival, inflammation and tumorigenesis. J. Biochem. 2002, 132, 359–371. [Google Scholar] [CrossRef]
- Matsubara, S.; Tomomura, M.; Kadomatsu, K.; Muramatsu, T. Structure of a retinoic acid-responsive gene, MK, which is transiently activated during the differentiation of embryonal carcinoma cells and the mid-gestation period of mouse embryogenesis. J. Biol. Chem. 1990, 265, 9441–9443. [Google Scholar]
- Kaname, T.; Kuwano, A.; Murano, I.; Uehara, K.; Muramatsu, T.; Kajii, T. Midkine gene (MDK), a gene for prenatal differentiation and neuroregulation, maps to band 11p11. 2 by fluorescence in situ hybridization. Genomics 1993, 17, 514–515. [Google Scholar] [CrossRef]
- Murasugi, A.; Tohma-Aiba, Y. Production of native recombinant human midkine in the yeast, Pichia pastoris. Protein Expr. Purif. 2003, 27, 244–252. [Google Scholar] [CrossRef]
- Kadomatsu, K.; Muramatsu, T. Midkine and pleiotrophin in neural development and cancer. Cancer Lett. 2004, 204, 127–143. [Google Scholar] [CrossRef]
- Tsutsui, J.; Uehara, K.; Kadomatsu, K.; Matsubara, S.; Muramatsu, T. A new family of heparin-binding factors: strong conservation of midkine (MK) sequences between the human and the mouse. Biochem. Biophys. Res. Commun. 1991, 176, 792–797. [Google Scholar] [CrossRef]
- Fabri, L.; Maruta, H.; Muramatsu, H.; Muramatsu, T.; Simpson, R.J.; Burgess, A.W.; Nice, E.C. Structural characterization of native and recombinant forms of the neurotrophic cytokine MK. J. Chromatogr. 1993, 646, 213–226. [Google Scholar] [CrossRef]
- Iwasaki, W.; Nagata, K.; Hatanaka, H.; Inui, T.; Kimura, T.; Muramatsu, T.; Yoshida, K.; Tasumi, M.; Inagaki, F. Solution structure of midkine, a new heparin-binding growth factor. EMBO J. 1997, 16, 6936–6946. [Google Scholar] [CrossRef]
- Asai, T.; Watanabe, K.; Ichihara-Tanaka, K.; Kaneda, N.; Kojima, S.; Iguchi, A.; Inagaki, F.; Muramatsu, T. Identification of heparin-binding sites in midkine and their role in neurite-promotion. Biochem. Biophys. Res. Commun. 1997, 236, 66–70. [Google Scholar] [CrossRef]
- Akhter, S.; Ichihara-Tanaka, K.; Kojima, S.; Muramatsu, H.; Inui, T.; Kimura, T.; Kaneda, N.; Talukder, A.H.; Kadomatsu, K.; Inagaki, F.; Muramatsu, T. Clusters of basic amino acids in midkine: roles in neurite-promoting activity and plasminogen activator-enhancing activity. J. Biochem. 1998, 123, 1127–1136. [Google Scholar] [CrossRef]
- Maeda, N.; Ichihara-Tanaka, K.; Kimura, T.; Kadomatsu, K.; Muramatsu, T.; Noda, M. A receptor-like protein-tyrosine phosphatase PTPzeta/RPTPbeta binds a heparin-binding growth factor midkine. Involvement of arginine 78 of midkine in the high affinity binding to PTPzeta. J. Biol. Chem. 1999, 274, 12474–12479. [Google Scholar]
- Matsubara, S.; Take, M.; Pedraza, C.; Muramatsu, T. Mapping and characterization of a retinoic acid-responsive enhancer of midkine, a novel heparin binding growth/differentiation factor with neurotrophic activity. J. Biochem. 1994, 115, 1088–1096. [Google Scholar]
- Pedraza, C.; Matsubara, S.; Muramatsu, T. A retinoic acid-responsive element in human midkine gene. J. Biochem. 1995, 117, 845–849. [Google Scholar]
- Adachi, Y.; Matsubara, S.; Pedraza, C.; Ozawa, M.; Tsutsui, J.; Takamatsu, H.; Noguchi, H.; Akiyama, T.; Muramatsu, T. Midkine as a novel target gene for the Wilms’ tumor suppressor gene (WT1). Oncogene 1996, 13, 2197–2203. [Google Scholar]
- Yu, L.; Ugai, S.; O-Wang, J.; Namba, M.; Kadomatsu, K.; Muramatsu, T.; Matsubara, S.; Sakiyama, S.; Tagawa, M. Cell growth- and P53-dependent transcriptional activity of the midkine promoter confers suicide gene expression in tumor cells. Oncol. Rep. 2003, 10, 1301–1305. [Google Scholar]
- Kaplan, F.; Comber, J.; Sladek, R.; Hudson, T.J.; Muglia, L.J.; Macrae, T.; Gagnon, S.; Asada, M.; Brewer, J.A.; Sweezey, N.B. The growth factor midkine is modulated by both glucocorticoid and retinoid in fetal lung development. Am. J. Respir. Cell Mol. Biol. 2003, 28, 33–41. [Google Scholar] [CrossRef]
- Reynolds, P.R.; Mucenski, M.L.; Le Cras, T.D.; Nichols, W.C.; Whitsett, J.A. Midkine is regulated by hypoxia and causes pulmonary vascular remodeling. J. Biol. Chem. 2004, 279, 37124–37132. [Google Scholar]
- You, Z.; Dong, Y.; Kong, X.; Beckett, L.A.; Gandour-Edwards, R.; Melamed, J. Midkine is a NF-kappaB-inducible gene that supports prostate cancer cell survival. BMC Med. Genomics. 2008, 1, 6. [Google Scholar] [CrossRef]
- Muramatsu, H.; Zou, P.; Suzuki, H.; Oda, Y.; Chen, G.Y.; Sakaguchi, N.; Sakuma, S.; Maeda, N.; Noda, M.; Takada, Y.; Muramatsu, T. Alpha 4 beta1- and alpha 6 beta1-integrins are functional receptors for midkine, a heparin-binding growth factor. J. Cell Sci. 2004, 117, 5405–5415. [Google Scholar] [CrossRef]
- Mitsiadis, T.A.; Salmivirta, M.; Muramatsu, T.; Muramatsu, H.; Rauvala, H.; Lehtonen, E.; Jalkanen, M.; Thesleff, I. Expression of the heparin-binding cytokines, midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesia. Development 1995, 121, 37–51. [Google Scholar]
- Kojima, T.; Katsumi, A.; Yamazaki, T.; Muramatsu, T.; Nagasaka, T.; Ohsumi, K.; Saito, H. Human ryudocan from endothelial-like cells binds basic fibroblast growth factor, midkine, and tissue factor pathway inhibitor. J. Biol. Chem. 1996, 271, 5914–5920. [Google Scholar]
- Nakanishi, T.; Kadomatsu, K.; Okamoto, T.; Ichihara-Tanaka, K.; Kojima, T.; Saito, H.; Tomoda, Y.; Muramatsu, T. Expression of syndecan-1 and -3 during embryogenesis of the central nervous system in relation to binding with midkina. J. Biochem. 1997, 121, 197–205. [Google Scholar]
- Owada, K.; Sanjo, N.; Kobayashi, T.; Mizusawa, H.; Muramatsu, H.; Muramatsu, T.; Michikawa, M. Midkine inhibits caspase-dependent apoptosis via the activation of mitogenactivated protein kinase and phosphatidylinositol 3-kinase in cultured neurons. J. Neurochem. 1999, 73, 2084–2092. [Google Scholar]
- Sakaguchi, N.; Muramatsu, H.; Ichihara-Tanaka, K.; Maeda, N.; Noda, M.; Yamamoto, T.; Michikawa, M.; Ikematsu, S.; Sakuma, S.; Muramatsu, T. Receptor-type protein tyrosine phosphatase as a component of the signaling receptor complex for midkine-dependent survival of embryonicneurons. Neurosci. Res. 2003, 45, 219–224. [Google Scholar] [CrossRef]
- Stoica, G.E.; Kuo, A.; Aigner, A.; Sunitha, I.; Souttou, B.; Malerczyk, C.; Caughey, D.J.; Wen, D.; Karavanov, A.; Riegel, A.T.; et al. Identification of anaplastic lymphoma kinase as a receptor for the growth factor pleiotrophin. J. Biol. Chem. 2001, 276, 16772–16779. [Google Scholar] [CrossRef]
- Stoica, G.E.; Kuo, A.; Powers, C.; Bowden, E.T.; Sale, E.B.; Riegel, A.T.; Wellstein, A. Midkine binds to anaplastic lymphoma kinase (ALK) and acts as a growth factor for different cell types. J. Biol. Chem. 2002, 277, 35990–35998. [Google Scholar]
- Muramatsu, H.; Zou, K.; Sakaguchi, N.; Ikematsu, S.; Sakuma, S.; Muramatsu, T. LDL receptor-related protein as a component of the midkine receptor. Biochem. Biophys. Res. Commun. 2000, 270, 936–941. [Google Scholar] [CrossRef]
- Herz, J.; Beffert, U. Apolipoprotein E receptors: linking brain development and Alzheimer's disease. Nat. Rev. Neurosci. 2000, 1, 51–58. [Google Scholar] [CrossRef]
- Shibata, Y.; Muramatsu, T.; Hirai, M.; Inui, T.; Kimura, T.; Saito, H.; McCormick, L.M.; Bu, G.; Kadomatsu, K. Nuclear targeting by the growth factor midkine. Mol. Cell. Biol. 2002, 22, 6788–6796. [Google Scholar] [CrossRef]
- Chen, S.; Bu, G.; Takei, Y.; Sakamoto, K.; Ikematsu, S.; Muramatsu, T.; Kadomatsu, K. Midkine and LDL-receptor-related protein 1 contribute to the anchorage-independent cell growth of cancer cells. J. Cell Sci. 2007, 120, 4009–4015. [Google Scholar] [CrossRef]
- Mitsiadis, T.A.; Muramatsu, T.; Muramatsu, H.; Thesleff, I. Midkine (MK), a heparin-binding growth/differentiation factor, is regulated by retinoic acid and epithelial-mesenchymal interactions in the developing mouse tooth, and affects cell proliferation and morphogenesis. J. Cell Biol. 1995, 129, 267–281. [Google Scholar] [CrossRef]
- Toriyama, K.; Muramatsu, H.; Hoshino, T.; Torii, S.; Muramatsu, T. Evaluation of heparin-binding growth factors in rescuing morphogenesis of heparitinase-treated mouse embryonic lung explants. Differentiation 1997, 61, 161–167. [Google Scholar] [CrossRef]
- Sakurai, H.; Bush, K.T.; Nigam, S.K. Identification of pleiotrophin as a mesenchymal factor involved in ureteric bud branching morphogenesis. Development 2001, 128, 3283–3293. [Google Scholar]
- Vilar, J.; Lalou, C.; Duong, V.H.; Charrin, S.; Hardouin, S.; Raulais, D.; Merlet-Bénichou, C.; Leliévre-Pégorier, M. Midkine is involved in kidney development and in its regulation by retinoids. J. Am. Soc. Nephrol. 2002, 13, 668–676. [Google Scholar]
- Dreyfus, J.; Brunet-de Carvalho, N.; Duprez, D.; Raulais, D.; Vigny, M. HB-GAM/pleiotrophin but not RIHB/midkine enhances chondrogenesis in micromass culture. Exp. Cell Res. 1998, 241, 171–180. [Google Scholar] [CrossRef]
- Imai, S.; Kaksonen, M.; Raulo, E.; Kinnunen, T.; Fages, C.; Meng, X.; Lakso, M.; Rauvala, H. Osteoblast recruitment and bone formation enhanced by cell matrix-associated heparin-binding growth-associated molecule (HB-GAM). J. Cell Biol. 1998, 143, 1113–1128. [Google Scholar] [CrossRef]
- Kadomatsu, K.; Hagihara, M.; Akhter, S.; Fan, Q.W.; Muramatsu, H.; Muramatsu, T. Midkine induces the transformation of NIH3T3 cells. Br. J. Cancer. 1997, 75, 354–359. [Google Scholar] [CrossRef]
- Qi, M.; Ikematsu, S.; Maeda, N.; Ichihara-Tanaka, K.; Sakuma, S.; Noda, M.; Muramatsu, T.; Kadomatsu, K. Haptotactic migration induced by midkine. Involvement of protein-tyrosine phosphatase zeta. Mitogen-activated protein kinase, and phosphatidylinositol 3-kinase. J. Biol. Chem. 2001, 276, 15868–15875. [Google Scholar]
- Kaneda, N.; Talukder, A.H.; Nishiyama, H.; Koizumi, S.; Muramatsu, T. Midkine, a heparin-binding growth/differentiation factor, exhibits nerve cell adhesion and guidance activity for neurite outgrowth in vitro. J. Biochem. 1996, 119, 1150–1156. [Google Scholar] [CrossRef]
- Michikawa, M.; Kikuchi, S.; Muramatsu, H.; Muramatsu, T.; Kim, S.U. Retinoic acid responsive gene product, midkine, has neurotrophic functions for mouse spinal cord and dorsal root ganglion neurons in culture. J. Neurosci. Res. 1993, 35, 530–539. [Google Scholar] [CrossRef]
- Yoshida, Y.; Goto, M.; Tsutsui, J.; Ozawa, M.; Sato, E.; Osame, M.; Muramatsu, T. Midkine is present in the early stage of cerebral infarct. Brain Res. Dev. Brain Res. 1995, 85, 25–30. [Google Scholar] [CrossRef]
- Yasuhara, O.; Muramatsu, H.; Kim, S.U.; Muramatsu, T.; Maruta, H.; McGeer, P.L. Midkine, a novel neurotrophic factor, is present in senile plaques of Alzheimer disease. Biochem. Biophys. Res. Commun. 1993, 192, 246–251. [Google Scholar] [CrossRef]
- Salama, R.H.; Muramatsu, H.; Shimizu, E.; Hashimoto, K.; Ohgake, S.; Watanabe, H.; Komatsu, N.; Okamura, N.; Koike, K.; Shinoda, N.; et al. Increased midkine levels in sera from patients with Alzheimer's disease. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29, 611–616. [Google Scholar] [CrossRef]
- Wang, S.; Yoshida, Y.; Goto, M.; Moritoyo, T.; Tsutsui, J.; Izumo, S.; Sato, E.; Muramatsu, T.; Osame, M. Midkine exists in astrocytes in the early stage of cerebral infarction. Dev. Brain Res. 1998, 106, 205–209. [Google Scholar] [CrossRef]
- Mochizuki, R.; Takeda, A.; Sato, N.; Kimpara, T.; Onodera, H.; Itoyama, Y.; Muramatsu, T. Induction of midkine expression in reactive astrocytes following rat transient forebrain ischemia. Exp. Neurol. 1998, 149, 73–78. [Google Scholar] [CrossRef]
- Takada, T.; Toriyama, K.; Muramatsu, H.; Song, X.J.; Torii, S.; Muramatsu, T. Midkine, a retinoic acid-inducible heparin-binding cytokine in inflammatory responses: chemotactic activity to neutrophils and association with inflammatory synovitis. J. Biochem. 1997, 122, 453–458. [Google Scholar]
- Horiba, M.; Kadomatsu, K.; Nakamura, E.; Muramatsu, H.; Ikematsu, S.; Sakuma, S.; Hayashi, K.; Yuzawa, Y.; Matsuo, S.; Kuzuya, M.; et al. Neointima formation in a restenosis model is suppressed in midkine-deficient mice. J. Clin. Invest. 2000, 105, 489–495. [Google Scholar] [CrossRef]
- Inoh, K.; Muramatsu, H.; Ochiai, K.; Torii, S.; Muramatsu, T. Midkine, a heparin-binding cytokine, plays key roles in intraperitoneal adhesions. Biochem. Biophys. Res. Commun. 2004, 317, 108–113. [Google Scholar] [CrossRef]
- Obama, H.; Biro, S.; Tashiro, T.; Tsutsui, J.; Ozawa, M.; Yoshida, H.; Tanaka, H.; Muramatsu, T. Myocardial infarction induces expression of midkine, a heparin-binding growth factor with reparative activity. Anticancer Res. 1998, 18, 145–152. [Google Scholar]
- Horiba, M.; Kadomatsu, K.; Yasui, K.; Lee, J.K.; Takenaka, H.; Sumida, A.; Kamiya, K.; Chen, S.; Sakuma, S.; Muramatsu, T.; et al. Midkine plays a protective role against cardiac ischemia/reperfusion injury through a reduction of apoptotic reaction. Circulation 2006, 114, 1713–1720. [Google Scholar] [CrossRef]
- Garver, R.I., Jr.; Chan, C.S.; Milner, P.G. Reciprocal expression of pleiotrophin and midkine in normal versus malignant lung tissues. Am. J. Respir. Cell Mol. Biol. 1993, 9, 463–466. [Google Scholar] [CrossRef]
- Garver, R.I., Jr.; Radford, D.M.; Donis-Keller, H.; Wick, M.R.; Milner, P.G. Midkine and pleiotrophin expression in normal and malignant breast tissue. Cancer 1994, 74, 1584–1590. [Google Scholar] [CrossRef]
- Konishi, N.; Nakamura, M.; Nakaoka, S.; Hiasa, Y.; Cho, M.; Uemura, H.; Hirao, Y.; Muramatsu, T.; Kadomatsu, K. Immunohistochemical analysis of midkine expression in human prostate carcinoma. Oncology 1999, 57, 253–257. [Google Scholar] [CrossRef]
- Ye, C.; Qi, M.; Fan, Q.W.; Ito, K.; Akiyama, S.; Kasai, Y.; Matsuyama, M.; Muramatsu, T.; Kadomatsu, K. Expression of midkine in the early stage of carcinogenesis in human colorectal cancer. Br. J. Cancer. 1999, 79, 179–184. [Google Scholar] [CrossRef]
- Kojima, S.; Muramatsu, H.; Amanuma, H.; Muramatsu, T. Midkine enhances fibrinolytic activity of bovine endothelial cells. J. Biol. Chem. 1995, 270, 9590–9596. [Google Scholar] [CrossRef]
- Ohta, S.; Muramatsu, H.; Senda, T.; Zou, K.; Iwata, H.; Muramatsu, T. Midkine is expressed during repair of bone fracture and promotes chondrogenesis. J. Bone Miner. Res. 1999, 14, 1132–1144. [Google Scholar] [CrossRef]
- Ratovitski, E.A.; Kotzbauer, P.T.; Milbrandt, J.; Lowenstein, C.J.; Burrow, C.R. Midkine induces tumor cell proliferation and binds to a high affinity signaling receptor associated with JAK tyrosine kinases. J. Biol. Chem. 1998, 273, 3654–3660. [Google Scholar]
- Huang, Y.; Hoque, M.O.; Wu, F.; Trink, B.; Sidransky, D.; Ratovitski, E.A. Midkine induces epithelial-mesenchymal transition through Notch2/Jak2-Stat3 signaling in human keratinocytes. Cell Cycle 2008, 7, 1613–1622. [Google Scholar] [CrossRef]
- Huang, Y.; Sook-Kim, M.; Ratovitski, E. Midkine promotes tetraspanin-integrin interaction and induces FAK-Stat1alpha pathway contributing to migration/invasiveness of human head and neck squamous cell carcinoma cells. Biochem. Biophys. Res. Commun. 2008, 377, 474–478. [Google Scholar] [CrossRef]
- Sato, W.; Kadomatsu, K.; Yuzawa, Y.; Muramatsu, H.; Hotta, N.; Matsuo, S.; Muramatsu, T. Midkine is involved in neutrophil infiltration into the tubulointerstitium in ischemic renal injury. J. Immunol. 2001, 167, 3463–3469. [Google Scholar]
- Qi, M.; Ikematsu, S.; Ichihara-Tanaka, K.; Sakuma, S.; Muramatsu, T.; Kadomatsu, K. Midkine rescues Wilms' tumor cells from cisplatin-induced apoptosis: regulation of Bcl-2 expression by midkine. J. Biochem. 2000, 127, 269–277. [Google Scholar] [CrossRef]
- Choudhuri, R.; Zhang, H.T.; Donnini, S.; Ziche, M.; Bicknell, R. An angiogenic role for the neurokines midkine and pleiotrophin in tumorigenesis. Cancer Res. 1997, 57, 1814–1819. [Google Scholar]
- Ruan, M.; Ji, T.; Wu, Z.; Zhou, J.; Zhang, C. Evaluation of expression of midkine in oral squamous cell carcinoma and its correlation with tumour angiogenesis. Int. J. Oral Maxillofac Surg. 2007, 36, 159–164. [Google Scholar]
- Ota, K.; Fujimori, H.; Ueda, M.; Shiniriki, S.; Kudo, M.; Jono, H.; Fukuyoshi, Y.; Yamamoto, Y.; Sugiuchi, H.; Iwase, H.; Shinohara, M.; et al. Midkine as a prognostic biomarker in oral squamous cell carcinoma. Br. J. Cancer 2008, 99, 655–662. [Google Scholar] [CrossRef]
- Aridome, K.; Tsutsui, J.; Takao, S.; Kadomatsu, K.; Ozawa, M.; Aikou, T.; Muramatsu, T. Increased midkine gene expression in human gastrointestinal cancers. Jpn. J. Cancer Res. 1995, 86, 655–661. [Google Scholar] [CrossRef]
- Kato, M.; Shinozawa, T.; Kato, S.; Awaya, A.; Terada, T. Increased midkine expression in hepatocellular carcinoma. Arch. Pathol. Lab. Med. 2000, 124, 848–852. [Google Scholar]
- Kato, M.; Shinozawa, T.; Kato, S.; Endo, K.; Terada, T. Increased midkine expression in intrahepatic cholangiocarcinoma: immunohistochemical and in situ hybridization analyses. Liver 2000, 20, 216–221. [Google Scholar]
- Kato, M.; Maeta, H.; Kato, S.; Shinozawa, T.; Terada, T. Immunohistochemical and in situ hybridization analyses of midkine expression in thyroid papillary carcinoma. Mod. Pathol. 2000, 13, 1060–1065. [Google Scholar] [CrossRef]
- O'Brien, T.; Cranston, D.; Fuggle, S.; Bicknell, R.; Harris, A.L. The angiogenic factor midkine is expressed in bladder cancer, and overexpression correlates with a poor outcome in patients with invasive cancers. Cancer Res. 1996, 56, 2515–2518. [Google Scholar]
- Moon, H.S.; Park, W.I.; Sung, S.H.; Choi, E.A.; Chung, H.W.; Woo, B.H. Immunohistochemical and quantitative competitive PCR analyses of midkine and pleiotrophin expression in cervical cancer. Gynecol. Oncol. 2003, 88, 289–297. [Google Scholar] [CrossRef]
- Nakanishi, T.; Kadomatsu, K.; Okamoto, T.; Tomoda, Y.; Muramatsu, T. Expression of midkine and pleiotropin in ovarian tumors. Obstet. Gynecol. 1997, 90, 285–290. [Google Scholar] [CrossRef]
- Nakagawara, A.; Milbrandt, J.; Muramatsu, T.; Deuel, T.F.; Zhao, H.; Cnaan, A.; Brodeur, G.M. Differential expression of pleiotrophin and midkine in advanced neuroblastomas. Cancer Res. 1995, 55, 1792–1797. [Google Scholar]
- Mishima, K.; Asai, A.; Kadomatsu, K.; Ino, Y.; Nomura, K.; Narita, Y.; Muramatsu, T.; Kirino, T. Increased expression of midkine during the progression of human astrocytomas. Neurosci. Lett. 1997, 233, 29–32. [Google Scholar] [CrossRef]
- Maeda, S.; Shinchi, H.; Kurahara, H.; Mataki, Y.; Noma, H.; Maemura, K.; Aridome, K.; Yokomine, T.; Natsugoe, S.; Aikou, T.; et al. Clinical significance of midkine expression in pancreatic head carcinoma. Br. J. Cancer. 2007, 97, 405–411. [Google Scholar]
- Kaifi, J.T.; Fiegel, H.C.; Rafnsdottir, S.L.; Aridome, K.; Schurr, P.G.; Reichelt, U.; Wachowiak, R.; Kleinhans, H.; Yekebas, E.F.; Mann, O.; et al. Midkine as a prognostic marker for gastrointestinal stromal tumors. J. Cancer Res. Clin. Oncol. 2007, 133, 431–435. [Google Scholar] [CrossRef]
- Tsutsui, J.; Kadomatsu, K.; Matsubara, S.; Nakagawara, A.; Hamanoue, M.; Takao, S.; Shimazu, H.; Ohi, Y.; Muramatsu, T. A new family of heparin-binding growth/differentiation factors: increased midkine expression in Wilms' tumor and other human carcinomas. Cancer Res. 1993, 53, 1281–1285. [Google Scholar]
- Muramatsu, H.; Song, X.J.; Koide, N.; Hada, H.; Tsuji, T.; Kadomatsu, K.; Inui, T.; Kimura, T.; Sakakibara, S.; Muramatsu, T. Enzyme-linked immunoassay for midkine, and its application to evaluation of midkine levels in developing mouse brain and sera from patients with hepatocellular carcinomas. J. Biochem. 1996, 119, 1171–1175. [Google Scholar] [CrossRef]
- Ikematsu, S.; Yano, A.; Aridome, K.; Kikuchi, M.; Kumai, H.; Nagano, H.; Okamoto, K.; Oda, M.; Sakuma, S.; Aikou, T.; et al. Serum midkine levels are increased in patients with various types of carcinomas. Br. J. Cancer 2000, 83, 701–706. [Google Scholar] [CrossRef]
- Ikematsu, S.; Nakagawara, A.; Nakamura, Y.; Sakuma, S.; Wakai, K.; Muramatsu, T.; Kadomatsu, K. Correlation of elevated level of blood midkine with poor prognostic factors of human neuroblastomas. Br. J. Cancer. 2003, 88, 1522–1526. [Google Scholar] [CrossRef]
- Riley, R.D.; Heney, D.; Jones, D.R.; Sutton, A.J.; Lambert, P.C.; Abrams, K.R.; Young, B.; Wailoo, A.J.; Burchill, S.A. A systematic review of molecular and biological tumor markers in neuroblastoma. Clin. Cancer Res. 2004, 10, 4–12. [Google Scholar] [CrossRef]
- Grovas, A.; Fremgen, A.; Rauck, A.; Ruymann, F.B.; Hutchinson, C.L.; Winchester, D.P.; Menck, H.R. The National Cancer Data Base Report on patterns of childhood cancer in the United States. Cancer 1997, 80, 2321–2332. [Google Scholar] [CrossRef]
- Brodeur, G.M. Neuroblastoma: biological insights into a clinical enigma. Nat. Rev. Cancer 2003, 3, 203–216. [Google Scholar] [CrossRef]
- Henry, M.C.; Tashjian, D.B.; Breuer, C.K. Neuroblastoma update. Curr. Opin. Oncol. 2005, 17, 19–23. [Google Scholar] [CrossRef]
- Ikematsu, S.; Nakagawara, A.; Nakamura, Y.; Ohira, M.; Shinjo, M.; Kishida, S.; Kadomatsu, K. Plasma midkine level is a prognostic factor for human neuroblastoma. Cancer Sci. 2008, 99, 2070–2074. [Google Scholar] [CrossRef]
- El-Serag, H.B.; Mason, A.C. Rising incidence of hepatocellular carcinoma in the United States. N. Engl. J. Med. 1999, 340, 745–750. [Google Scholar] [CrossRef]
- Parkin, D.M.; Bray, F.; Ferlay, J.; Pisani, P. Global cancer statistics, 2002. CA Cancer J. Clin. 2005, 55, 74–108. [Google Scholar] [CrossRef]
- Poon, R.T.; Fan, S.T.; Lo, C.M.; Liu, C.L.; Wong, J. Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation. Ann. Surg. 2002, 235, 373–382. [Google Scholar] [CrossRef]
- Yuen, M.F.; Cheng, C.C.; Lauder, I.J.; Lam, S.K.; Ooi, C.G.; Lai, C.L. Early detection of hepatocellular carcinoma increases the chance of treatment: Hong Kong experience. Hepatology 2000, 31, 330–335. [Google Scholar] [CrossRef]
- Taketa, K. α-Fetoprotein: reevaluation in hepatology. Hepatology 1990, 12, 1420–1432. [Google Scholar] [CrossRef]
- Yin, Z.; Luo, X.; Kang, X.; Wu, Z.; Qian, H.; Wu, M. Correlation between midkine protein overexpression and intrahepatic metastasis in hepatocellular carcinoma. Zhonghua Zhong Liu Za Zhi 2002, 24, 27–29. [Google Scholar]
- Jia, H.L.; Ye, Q.H.; Qin, L.X.; Budhu, A.; Forgues, M.; Chen, Y.; Liu, Y.K.; Sun, H.C.; Wang, L.; Lu, H.Z.; et al. Gene expression profiling reveals potential biomarkers of human hepatocellular carcinoma. Clin. Cancer Res. 2007, 13, 1133–1139. [Google Scholar] [CrossRef]
- Daly, J.M.; Karnell, L.H.; Menck, H.R. National cancer data base report on esophageal carcinoma. Cancer 1996, 78, 1820–1828. [Google Scholar] [CrossRef]
- Hofstetter, W.; Swisher, S.G.; Correa, A.M.; Hess, K.; Putnam, J.B., Jr.; Ajani, J.A.; Dolormente, M.; Francisco, R.; Komaki, R.R.; Lara, A.; et al. Treatment outcomes of resected esophageal cancer. Ann. Surg. 2002, 236, 376–384. [Google Scholar] [CrossRef]
- Lee, J.M.; Wu, M.T.; Lee, Y.C.; Yang, S.Y.; Chen, J.S.; Hsu, H.H.; Huang, P.M.; Kuo, S.W.; Lee, C.J.; Chen, C.J. Association of GSTP1 polymorphism and survival for esophageal cancer. Clin. Cancer Res. 2005, 11, 4749–4753. [Google Scholar] [CrossRef]
- Miyauchi, M.; Shimada, H.; Kadomatsu, K.; Muramatsu, T.; Matsubara, S.; Ikematsu, S.; Takenaga, K.; Asano, T.; Ochiai, T.; Sakiyama, S.; et al. Fequent expression of midkine gene in esophageal cancer suggests a potential usage of its promoter for suicide gene therapy. Jpn. J. Cancer Res. 1999, 90, 469–475. [Google Scholar] [CrossRef]
- Shimada, H.; Nabeya, Y.; Tagawa, M.; Okazumi, S.; Matsubara, H.; Kadomatsu, K.; Muramatsu, T.; Ikematsu, S.; Sakuma, S.; Ochiai, T. Preoperative serum midkine concentration is a prognostic marker for esophageal squamous cell carcinoma. Cancer Sci. 2003, 94, 628–632. [Google Scholar] [CrossRef]
- Petersen, P.E. The World Oral Health Report 2003: continuous improvement of oral health in the 21st century – the approach of the WHO Global Oral Health Programme. Community Dent. Oral. Epidemiol. 2003, 31, 3–23. [Google Scholar] [CrossRef]
- Jemal, A.; Siegel, R.; Ward, E.; Murray, T.; Xu, J.; Smigal, C.; Thun, M.J. Cancer statistics. CA Cancer J. Clin. 2006, 56, 106–130. [Google Scholar] [CrossRef]
- Krimmel, M.; Hoffmann, J.; Krimmel, C.; Cornelius, C.P.; Schwenzer, N. (1998) Relevance of SCC-Ag, CEA, CA 19.9 and CA 125 for diagnosis and follow-up in oral cancer. J. Craniomaxillofac. Surg. 1998, 26, 243–248. [Google Scholar] [CrossRef]
- Simpson, P.T.; Reis-Filho, J.S.; Gale, T.; Lakhani, S.R. Molecular evolution of breast cancer. J. Pathol. 2005, 205, 248–254. [Google Scholar] [CrossRef]
- Alizadeh, A.A.; Ross, D.T.; Perou, C.M.; van de Rijn, M. Towards a novel classification of human malignancies based on gene expression patterns. J. Pathol. 2001, 195, 41–52. [Google Scholar]
- Rakha, E.A.; Reis-Filho, J.S.; Ellis, I.O. Combinatorial biomarker expression in breast cancer. Breast Cancer Res. Treat. 2010, in press. [Google Scholar]
- Ibusuki, M.; Fujimori, H.; Yamamoto, Y.; Ota, K.; Ueda, M.; Shinriki, S.; Taketomi, M.; Sakuma, S.; Shinohara, M.; Iwase, H.; et al. Midkine in plasma as a novel breast cancer marker. Cancer Sci. 2009, 100, 1735–1739. [Google Scholar] [CrossRef]
- Li, D.; Xie, K.; Wolff, R.; Abbruzzese, J.L. Pancreatic cancer. Lancet 2004, 363, 1049–1057. [Google Scholar] [CrossRef]
- Ohhashi, S.; Ohuchida, K,; Mizumoto, K.; Egami, T.; Yu, J.; Cui, L.; Toma, H.; Takahata, S.; Nabae, T.; Tanaka, M. Midkine mRNA is overexpressed in pancreatic cancer. Dig. Dis. Sci. 2009, 54, 811–815. [Google Scholar] [CrossRef]
- Miyashiro, I.; Kaname, T.; Nakayama, T.; Nakamori, S.; Yagyu, T.; Monden, T.; Kikkawa, N.; Nishisho, I.; Muramatsu, T.; Monden, M.; et al. Expression of truncated midkine in human colorectal cancers. Cancer Lett. 1996, 106, 287–291. [Google Scholar] [CrossRef]
- Kaname, T.; Kadomatsu, K.; Aridome, K.; Yamashita, S.; Sakamoto, K.; Ogawa, M.; Muramatsu, T.; Yamamura, K. The expression of truncated MK in human tumors. Biochem. Biophys. Res. Commun. 1996, 219, 256–260. [Google Scholar] [CrossRef]
- Miyashiro, I.; Kaname, T.; Shin, E.; Wakasugi, E.; Monden, T.; Takatsuka, Y.; Kikkawa, N.; Muramatsu, T.; Monden, M.; Akiyama, T. Midkine expression in human breast cancers: expression of truncated form. Breast Cancer Res. Treat. 1997, 43, 1–6. [Google Scholar] [CrossRef]
- Aridome, K.; Takao, S.; Kaname, T.; Kadomatsu, K.; Natsugoe, S.; Kijima, F.; Aikou, T.; Muramatsu, T. Truncated midkine as a marker of diagnosis and detection of nodal metastases in gastrointestinal carcinomas. Br. J. Cancer 1998, 78, 472–477. [Google Scholar] [CrossRef]
- Paul, S.; Mitsumoto, T.; Asano, Y.; Kato, S.; Kato, M.; Shinozawa, T. Detection of truncated midkine in Wilms' tumor by a monoclonal antibody against human recombinant truncated midkine. Cancer Lett. 2001, 163, 245–251. [Google Scholar] [CrossRef]
- Tao, P.; Xu, D.; Lin, S.; Ouyang, G.L.; Chang, Y.; Chen, Q.; Yuan, Y.; Zhuo, X.; Luo, Q.; Li, J.; et al. Abnormal expression, highly efficient detection and novel truncations of midkine in human tumors, cancers and cell lines. Cancer Lett. 2007, 253, 60–67. [Google Scholar] [CrossRef]
- Mashour, G.A.; Ratner, N.; Khan, G.A.; Wang, H.L.; Martuza, R.L.; Kurtz, A. (2001) The angiogenic factor midkine is aberrantly expressed in NFl-deficient Schwann cells and is a mitogen for neuronbroma-derived cells. Oncogene 2001, 20, 97–105. [Google Scholar] [CrossRef]
- Takei, Y.; Kadomatsu, K.; Matsuo, S.; Itoh, H.; Nakazawa, K.; Kubota, S.; Muramatsu, T. Antisense oligodeoxynucleotide targeted to Midkine, a heparin-binding growth factor, suppresses tumorigenicity of mouse rectal carcinoma cells. Cancer Res. 2001, 61, 8486–8491. [Google Scholar]
- Takei, Y.; Kadomatsum, K.; Goto, T.; Muramatsu, T. Combinational antitumor effect of siRNA against midkine and paclitaxel on growth of human prostate cancer xenografts. Cancer 2006, 107, 864–873. [Google Scholar] [CrossRef]
- Wang, Q.; Huang, Y.; Ni, Y.; Wang, H.; Hou, Y. siRNA targeting midkine inhibits gastric cancer cells growth and induces apoptosis involved caspase-3, -8, -9 activation and mitochondrial depolarization. J. Biomed. Sci. 2007, 14, 783–795. [Google Scholar] [CrossRef]
- Toyoda, E.; Doi, R.; Kami, K.; Mori, T.; Ito, D.; Koizumi, M.; Kida, A.; Nagai, K.; Ito, T.; Masui, T.; et al. Midkine promoter-based conditionally replicative adenovirus therapy for midkine-expressing human pancreatic cancer. J. Exp. Clin. Cancer Res. 2008, 21, 27–30. [Google Scholar]
- Adachi, Y.; Reynolds, P.N.; Yamamoto, M.; Grizzle, W.E.; Overturf, K.; Matsubara, S.; Muramatsu, T.; Curiel, D.T. Midkine promoter-based adenoviral vector gene delivery for pediatric solid tumors. Cancer Res. 2000, 60, 4305–4310. [Google Scholar]
- Adachi, Y.; Reynolds, P.N.; Yamamoto, M.; Wang, M.; Takayama, K.; Matsubara, S.; Muramatsu, T.; Curiel, D.T. A midkine promoter-based conditionally replicative adenovirus for treatment of pediatric solid tumors and bone marrow tumor purging. Cancer Res. 2001, 61, 7882–7888. [Google Scholar]
- Yu, L.; Hamada, K.; Namba, M.; Kadomatsu, K.; Muramatsu, T.; Matsubara, S.; Tagawa, M. Midkine promoter-driven suicide gene expression and -mediated adenovirus replication produced cytotoxic effects to immortalised and tumour cells. Eur. J. Cancer. 2004, 40, 1787–1794. [Google Scholar] [CrossRef]
- Kohno, S.; Nakagawa, K.; Hamada, K.; Harada, H.; Yamasaki, K.; Hashimoto, K.; Tagawa, M.; Nagato, S.; Furukawa, K.; Ohnishi, T. Midkine promoter-based conditionally replicative adenovirus for malignant glioma therapy. Oncol. Rep. 2004, 12, 73–78. [Google Scholar]
- Terao, S.; Shirakawa, T.; Kubo, S.; Bishunu, A.; Lee, S.J.; Goda, K.; Tsukuda, M.; Hamada, K.; Tagawa, M.; Takenaka, A.; et al. Midkine promoter-based conditionally replicative adenovirus for targeting midkine-expressing human bladder cancer model. Urology 2007, 70, 1009–1013. [Google Scholar] [CrossRef]
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Jono, H.; Ando, Y. Midkine: A Novel Prognostic Biomarker for Cancer. Cancers 2010, 2, 624-641. https://doi.org/10.3390/cancers2020624
Jono H, Ando Y. Midkine: A Novel Prognostic Biomarker for Cancer. Cancers. 2010; 2(2):624-641. https://doi.org/10.3390/cancers2020624
Chicago/Turabian StyleJono, Hirofumi, and Yukio Ando. 2010. "Midkine: A Novel Prognostic Biomarker for Cancer" Cancers 2, no. 2: 624-641. https://doi.org/10.3390/cancers2020624